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2d and 3d echocardiography in the axolotl (ambystoma mexicanum).cardiac malfunction as a result of ischemic heart disease is a major challenge, and regenerative therapies to the heart are in high demand. a few model species such as zebrafish and salamanders that are capable of intrinsic heart regeneration hold promise for future regenerative therapies for human patients. to evaluate the outcome of cardioregenerative experiments it is imperative that heart function can be monitored. the axolotl salamander (a. mexicanum) represents a well-established model spe ...201830582577
amputation-induced reactive oxygen species signaling is required for axolotl tail regeneration.among vertebrates, salamanders are unparalleled in their ability to regenerate appendages throughput life. however, little is known about early signals that initiate regeneration in salamanders.201930569660
tracing the origins of axolotl limb regeneration.the mechanisms underlying limb regeneration in axolotl have remained elusive due to limitations in isolating and tracking the cells that replenish lost tissues. in recent work, elly tanaka and barbara treutlein unite their expertise in axolotl limb regeneration and single-cell analysis to reveal cellular mechanisms underpinning regeneration.201830562504
acquisition and reconstruction of 4d surfaces of axolotl embryos with the flipping stage robotic microscope.we have designed and constructed a flipping stage for a light microscope that can view the whole exterior surface of a 2 mm diameter developing axolotl salamander embryo. it works by rapidly inverting the bottom-heavy embryo, imaging it as it rights itself. the images are then montaged to reconstruct the whole 3d surface versus time, for a full 4d record of the surface. imaging early stage axolotl development will help discover how cell differentiation and movement takes place in the early embry ...201830554603
miniscule differences between sex chromosomes in the giant genome of a salamander.in the mexican axolotl (ambystoma mexicanum), sex is determined by a single mendelian factor, yet its sex chromosomes do not exhibit morphological differentiation typical of many vertebrate taxa that possess a single sex-determining locus. as sex chromosomes are theorized to differentiate rapidly, species with undifferentiated sex chromosomes provide the opportunity to reconstruct early events in sex chromosome evolution. whole genome sequencing of 48 salamanders, targeted chromosome sequencing ...201830552368
comparative transcriptomics of rat and axolotl after spinal cord injury dissects differences and similarities in inflammatory and matrix remodeling gene expression patterns.following spinal cord injury in mammals, maladaptive inflammation, and matrix deposition drive tissue scarring and permanent loss of function. in contrast, axolotls regenerate their spinal cord after severe injury fully and without scarring. to explore previously unappreciated molecules and pathways that drive tissue responses after spinal cord injury, we performed a 4-way intersection of rat and axolotl transcriptomics datasets and isolated shared genes with similar or differential expression a ...201830519154
transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution.regeneration of complex multi-tissue structures, such as limbs, requires the coordinated effort of multiple cell types. in axolotl limb regeneration, the wound epidermis and blastema have been extensively studied via histology, grafting, and bulk-tissue rna-sequencing. however, defining the contributions of these tissues is hindered due to limited information regarding the molecular identity of the cell types in regenerating limbs. here we report unbiased single-cell rna-sequencing on over 25,00 ...201830514844
regenerative models for the integration and regeneration of head skeletal tissues.disease of, or trauma to, the human jaw account for thousands of reconstructive surgeries performed every year. one of the most popular and successful treatment options in this context involves the transplantation of bone tissue from a different anatomical region into the affected jaw. although, this method has been largely successful, the integration of the new bone into the existing bone is often imperfect, and the integration of the host soft tissues with the transplanted bone can be inconsis ...201830486286
from axolotl to zebrafish: a comparative approach to the study of thyroid involvement in ocular development.while discussion of interactions between the thyroid gland and the eye mostly focus on thyroid eye disease, the involvement of the thyroid and its hormones on development of the eye before birth is also an important perspective that should not be forgotten. experimental models involving amphibians and fish are valuable both because the developing larvae are not constrained within the adult but can be observed and manipulated as they grow autonomously and also because they metamorphose with subst ...201930482907
application and optimization of crispr-cas9-mediated genome engineering in axolotl (ambystoma mexicanum).genomic manipulation is essential to the use of model organisms to understand development, regeneration and adult physiology. the axolotl (ambystoma mexicanum), a type of salamander, exhibits an unparalleled regenerative capability in a spectrum of complex tissues and organs, and therefore serves as a powerful animal model for dissecting mechanisms of regeneration. we describe here an optimized stepwise protocol to create genetically modified axolotls using the crispr-cas9 system. the protocol, ...201830429597
single-cell analysis uncovers convergence of cell identities during axolotl limb regeneration.amputation of the axolotl forelimb results in the formation of a blastema, a transient tissue where progenitor cells accumulate prior to limb regeneration. however, the molecular understanding of blastema formation had previously been hampered by the inability to identify and isolate blastema precursor cells in the adult tissue. we have used a combination of cre-loxp reporter lineage tracking and single-cell messenger rna sequencing (scrna-seq) to molecularly track mature connective tissue (ct) ...201830262634
using transcriptomics to enable a plethodontid salamander (bolitoglossa ramosi) for limb regeneration research.tissue regeneration is widely distributed across the tree of life. among vertebrates, salamanders possess an exceptional ability to regenerate amputated limbs and other complex structures. thus far, molecular insights about limb regeneration have come from a relatively limited number of species from two closely related salamander families. to gain a broader perspective on the molecular basis of limb regeneration and enhance the molecular toolkit of an emerging plethodontid salamander (bolitoglos ...201830253734
cell cycles during early steps of amphibian embryogenesis: a review.the published data on cell cycles during the initial (pregastrular) period of embryonic development in representatives of the class amphibia have been critically discussed. we have also used the literature data on ontogenetic diversity of these animals. the relatively small eggs of two principal model species for amphibian embryology, the mexican axolotl and the african clawed frog, undergo the extensive series of rapid synchronous cleavage divisions, after which the midblastula transition (mbt) ...201830240720
bapx1 is required for jaw joint development in amphibians.the acquisition of a movable jaw and a jaw joint are key events in gnathostome evolution. jaws are derived from the neural crest derived pharyngeal skeleton and the transition from jawless to jawed vertebrates consists of major morphological changes, which must have a genetic foundation. recent studies on the effects of bapx1 knockdown in fish and chicken indicate that bapx1 has acquired such a role in primary jaw joint development during vertebrate evolution, but evidence from amphibians is mis ...201830168254
identification of axolotl bh3-only proteins and expression in axolotl organs and apoptotic limb regeneration tissue.like other urodela amphibians, axolotls are able to regenerate lost appendages, even as adults, rendering them unique among higher vertebrates. in reaction to the severe trauma of a lost limb, apoptosis seems to be primarily implicated in the removal of injured cells and tissue homeostasis. little, however, is known about apoptotic pathways and control mechanisms. therefore, here we provide additional information regarding the mechanisms of tissue degradation. expression patterns of bcl-2 family ...201830154109
the serotonergic somatosensory projection to the tectum of normal and eyeless salamanders.the spinotectal somatosensory projection was compared in normal, genetically eyeless, and embryonically manipulated salamanders. in normal animals, serotonin fluorescence was restricted to the intermediate tectalneuropil. this same region showed both high levels of serotonin uptake and somatosensory single unit electrical activity. in mutant eyeless salamanders and in normal animals enucleated early in development, serotonin fluorescence, serotonin uptake, and somatosensory activity were present ...198130153710
i spy with my little eye: a simple behavioral assay to test color sensitivity on digital displays.passive and interactive virtual reality (vr) environments are becoming increasingly popular in the field of behavioral neuroscience. while the technique was originally developed for human observers, corresponding applications have been adopted for the research of visual-driven behavior and neural circuits in animals. rgb color reproduction using red, green and blue primary color pixels is generally calibrated for humans, questioning if the distinct parameters are also readily transferable to oth ...201830127095
[biomedical bestiary: the axolotl]. 201930125261
differences in neural stem cell identity and differentiation capacity drive divergent regenerative outcomes in lizards and salamanders.while lizards and salamanders both exhibit the ability to regenerate amputated tails, the outcomes achieved by each are markedly different. salamanders, such as ambystoma mexicanum, regenerate nearly identical copies of original tails. regenerated lizard tails, however, exhibit important morphological differences compared with originals. some of these differences concern dorsoventral patterning of regenerated skeletal and spinal cord tissues; regenerated salamander tail tissues exhibit dorsovent ...201830104374
exogenous vitamin d signaling alters skeletal patterning, differentiation, and tissue integration during limb regeneration in the axolotl.urodele amphibians such as the axolotl regenerate complete limbs as adults, and understanding how the "blueprint", or pattern, of the regenerate is established and manipulated are areas of intense interest. nutrient signaling plays an important role in pattern formation during regeneration. retinoic acid signaling is the most characterized pathway during this process. exogenous retinoic acid (ra) reprograms the pattern information in regenerating cells to a more posterior, ventral, and proximal ...201830096415
comparative transcriptomics of limb regeneration: identification of conserved expression changes among three species of ambystoma.transcriptome studies are revealing the complex gene expression basis of limb regeneration in the primary salamander model - ambystoma mexicanum (axolotl). to better understand this complexity, there is need to extend analyses to additional salamander species. using microarray and rna-seq, we performed a comparative transcriptomic study using a. mexicanum and two other ambystomatid salamanders: a. andersoni, and a. maculatum. salamanders were administered forelimb amputations and rna was isolate ...201930092345
evaluation of the anesthetic effects of ms222 in the adult mexican axolotl (ambystoma mexicanum).the mexican axolotl (ambystoma mexicanum) is a unique research model in several fields of medicine, where surgical and invasive procedures may be required. as yet, little is known about the efficacy of ms222 (tricaine methanesulfonate), which is the most commonly used anesthetic agent in amphibians. the main objectives of this study were to evaluate the anesthetic effects and physiological changes in adult axolotls following a 20-minute immersion bath, containing progressive ms222 concentrations ...201630050832
experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota.axolotl (ambystoma mexicanum) is a critically endangered salamander species and a model organism for regenerative and developmental biology. despite life-long neoteny in nature and in captive-bred colonies, metamorphosis of these animals can be experimentally induced by administering thyroid hormones (ths). however, microbiological consequences of this experimental procedure, such as host microbiota response, remain largely unknown. here, we systematically compared host bacterial microbiota asso ...201830030457
the tmem16a channel mediates the fast polyspermy block in xenopus laevis.in externally fertilizing animals, such as sea urchins and frogs, prolonged depolarization of the egg immediately after fertilization inhibits the entry of additional sperm-a phenomenon known as the fast block to polyspermy. in the african clawed frog xenopus laevis, this depolarization is driven by ca2+-activated cl- efflux. although the prominent ca2+-activated cl- currents generated in immature x. laevis oocytes are mediated by x. laevis transmembrane protein 16a (xtmem16a) channels, little i ...201830012842
changes in the appendicular skeleton during metamorphosis in the axolotl salamander (ambystoma mexicanum).axolotl salamanders (ambystoma mexicanum) remain aquatic in their natural state, during which biomechanical forces on their diarthrodial limb joints are likely reduced relative to salamanders living on land. however, even as sexually mature adults, these amphibians can be induced to metamorphose into a weight-bearing terrestrial stage by environmental stress or the exogenous administration of thyroxine hormone. in some respects, this aquatic to terrestrial transition of axolotl salamanders throu ...201829992565
formation of the pronephros and pronephric duct rudiment in the mexican axolotl.in the mexican axolotl (ambystoma mexicanum), the pronephros begins to form at the four-somite stage. it is initially continuous with the posterior-lateral region of somite 2 and the lateral margin of somites 3 and 4. by the seven-somite stage, the pronephros has become compacted, and the cells are now morphologically distinct from the somitic cells. at this stage, a mass of loosely connected cells, apparently originating from the lateral mesoderm, is seen below somites 4 and 5. by the eight-som ...198529976020
skin regeneration of amphibians: a novel model for skin regeneration as adults.adult mammals do not regenerate the dermis of the skin but form a scar after a deep skin injury. since a scar causes serious medical problems, skin regeneration, instead of formation of a scar, has been strongly desired from a clinical point of view. recent studies have suggested multiple origins of myofibroblasts, which are scar-forming cells in skin wound healing of mammals. while amphibians have skin structures that are basically common to mammals as tetrapods, both urodele and anuran amphibi ...201829947057
an integrative framework for salamander and mouse limb regeneration.appendage regeneration is not a simple task. the animal must harness all of its energy and resources to orchestrate perhaps one of the most complicated events since its development. balancing the immune response, wound healing, proliferation, patterning and differentiation is an elegant job, and how some animals achieve that still leaves researchers enchanted today. in this work, we review some of the molecular aspects of regeneration, with a focus on the axolotl, the champion of tetrapod limb r ...201829943379
bapx1 upregulation is associated with ectopic mandibular cartilage development in amphibians.the emergence of novel structures during evolution is crucial for creating variation among organisms, but the underlying processes which lead to the emergence of evolutionary novelties are poorly understood. the gnathostome jaw joint is such a novelty, and the incorporation of bapx1 expression into the intermediate first pharyngeal arch may have played a major role in the evolution of this joint. knockdown experiments revealed that loss of bapx1 function leads to the loss of the jaw joint, becau ...201829942645
retinoid x receptor α downregulation is required for tail and caudal spinal cord regeneration in the adult newt.some adult vertebrate species, such as newts, axolotls and zebrafish, have the ability to regenerate their central nervous system (cns). however, the factors that establish a permissive cns environment for correct morphological and functional regeneration in these species are not well understood. recent evidence supports a role for retinoid signaling in the intrinsic ability of neurons, in these regeneration-competent species, to regrow after cns injury. previously, we demonstrated that a specif ...201829926831
an interview with elly tanaka.elly tanaka is a senior scientist at the research institute of molecular pathology in vienna, austria. her lab's research uses the axolotl - which possesses impressive regenerative capacity - to understand the molecular and cellular mechanisms underlying limb and spinal cord regeneration. we met elly in her office in vienna on the occasion of the recent sy-stem symposium (see meeting review by porrello and kirkeby in this issue) to talk about what drew her to regeneration research and the axolot ...201829884656
lateral-line neuromast development in ambystoma mexicanum and a comparison with rana pipiens.we have examined the embryonic development of the major neuromast lines of the lateral-line system in the urodele ambystoma mexicanum both in vivo (using microsurgical techniques to transplant placodes) and in preserved embryos using scanning electron microscopy (sem). we have compared this to sem observations of embryos of the anuran rana pipiens. we have determined the approximate locations of the lateral-line placodes in a. mexicanum and the approximate timing of both the migration of the lat ...198829879797
the vascular structure of the kidney of the neotenous axolotl and its metamorphosed counterpart.the renal vascular and glomerular structures of the kidney of neotenous and experimentally metamorphosed axolotls (ambystoma mexicanum: amphibia, urodela) are investigated using light, transmission electron, and scanning electron microscopy of critical-point dried specimens and vascular corrosion casts. the blood vascular system of the kidney in the axolotl is generally similar to that in other urodeles. the glomeruli are comparatively large and distincly ovoid (mean size 267 × 201 μm). glomerul ...199229865583
brain-capillary architecture of the newt, triturus cristatus carnifex (caudata: salamandridae): scanning electron-microscopical study of vascular corrosion casts.the brain-microvascular architecture of the newt (triturus cristatus carnifex) was studied by scanning electron-microscopical examination of microvascular corrosion casts. it is characterized at the leptomeningeal level by a superficial network of single vessels that leave the meningeal sheath to form hairpin-shaped capillary loops. these loops penetrate the nervous parenchyma to varying depths and are variously bent, inclined, and twisted. each hairpin-like loop consists of descending and ascen ...199129865580
variable manifestations in the short toes (s) mutation of the axolotl.we describe a detailed histological analysis of the affected organs in the short toes (s) mutation of the mexican axolotl, ambystoma mexicanum. the s mutant animals displayed a variation in the response to the mutation such as the time of death and the degree of abnormalities of the affected organs (limbs, kidney, ducts, and reproductive structures). in addition to the numerous histological abnormalities characterized here, we also examined the presence of laminin-related molecules in s mutant k ...199329865473
author correction: the axolotl genome and the evolution of key tissue formation regulators.in the originally published version of this article, the sequenced axolotl strain (the homozygous white mutant) was denoted as 'd/d' rather than 'd/d' in fig. 1a and the accompanying legend, the main text and the methods section. the original article has been corrected online.201829795340
signaling-dependent control of apical membrane size and self-renewal in rosette-stage human neuroepithelial stem cells.in the developing nervous system, neural stem cells are polarized and maintain an apical domain facing a central lumen. the presence of apical membrane is thought to have a profound influence on maintaining the stem cell state. with the onset of neurogenesis, cells lose their polarization, and the concomitant loss of the apical domain coincides with a loss of the stem cell identity. little is known about the molecular signals controlling apical membrane size. here, we use two neuroepithelial cel ...201829779899
forever young: endocrinology of paedomorphosis in the mexican axolotl (ambystoma mexicanum).the mexican axolotl (ambystoma mexicanum) is a salamander species that does not undergo metamorphosis, resulting in the retention of juvenile characteristics in the mature breeding stage (paedomorphosis). here we review the endocrinological studies investigating the proximate cause of axolotl paedomorphosis with a focus on the hypothalamo-pituitary-thyroid (hpt) axis. it is well established that axolotl paedomorphosis is a consequence of low activity of the hpt axis. the pituitary hormone thyrot ...201829777689
induction of metamorphosis causes differences in sex-specific allocation patterns in axolotls (ambystoma mexicanum) that have different growth histories.we tested the hypothesis that salamanders growing at different rates would have allocation patterns that differ among male and female metamorphic and larval salamanders. we raised individual axolotls, ambystoma mexicanum, on four food regimes: constant high growth (throughout the experiment), constant low growth (restricted throughout the experiment), high growth switched to low growth (ad libitum switched after 140 d to restricted), and low growth switched to high growth (restricted switched af ...201529755160
ectopic fgf signaling induces the intercalary response in developing chicken limb buds.intercalary pattern formation is an important regulatory step in amphibian limb regeneration. amphibian limb regeneration is composed of multiple steps, including wounding, blastema formation, and intercalary pattern formation. attempts have been made to transfer insights from regeneration-competent animals to regeneration-incompetent animalsat each step in the regeneration process. in the present study, we focused on the intercalary mechanism in chick limb buds. in amphibian limb regeneration, ...201829721334
cancer reversion with oocyte extracts is mediated by cell cycle arrest and induction of tumour dormancy.inducing stable control of tumour growth by tumour reversion is an alternative approach to cancer treatment when eradication of the disease cannot be achieved. the process requires re-establishment of normal control mechanisms that are lost in cancer cells so that abnormal proliferation can be halted. embryonic environments can reset cellular programmes and we previously showed that axolotl oocyte extracts can reprogram breast cancer cells and reverse their tumorigenicity. in this study, we anal ...201829662623
publisher correction: virtual genome walking across the 32 gb ambystoma mexicanum genome; assembling gene models and intronic sequence.a correction to this article has been published and is linked from the html and pdf versions of this paper. the error has been fixed in the paper.201829654245
positive in vitro wound healing effects of functional inclusion bodies of a lipoxygenase from the mexican axolotl.ambloxe is a lipoxygenase, which is up-regulated during limb-redevelopment in the mexican axolotl, ambystoma mexicanum, an animal with remarkable regeneration capacity. previous studies have shown that mammalian cells transformed with the gene of this epidermal lipoxygenase display faster migration and wound closure rate during in vitro wound healing experiments.201829626934
noncanonical hox, etv4, and gli3 gene activities give insight into unique limb patterning in salamanders.limb development in salamanders is unique among tetrapods in significant ways. not only can salamanders regenerate lost limbs repeatedly and throughout their lives, but also the preaxial zeugopodial element and digits form before the postaxial ones and, hence, with a reversed polarity compared to all other tetrapods. moreover, in salamanders with free-swimming larval stages, as exemplified by the axolotl (ambystoma mexicanum), each digit buds independently, instead of undergoing a paddle stage. ...201829602205
non-invasive cell tracking of spio labeled cells in an intrinsic regenerative environment: the axolotl limb.non-invasive methods to track the progress of stem cell therapies are important in the development of future regenerative therapies. super-paramagnetic iron oxide particles (spios) have previously been applied to track cells using magnetic resonance imaging (mri) in vivo in non-regenerative animal models. to the best of the author's knowledge, the present study investigated for the first time, the feasibility of tracking spio labeled cells in an intrinsic regenerative environment, the regenerati ...201829545849
musashi and plasticity of xenopus and axolotl spinal cord ependymal cells.the differentiated state of spinal cord ependymal cells in regeneration-competent amphibians varies between a constitutively active state in what is essentially a developing organism, the tadpole of the frog xenopus laevis, and a quiescent, activatable state in a slowly growing adult salamander ambystoma mexicanum, the axolotl. ependymal cells are epithelial in intact spinal cord of all vertebrates. after transection, body region ependymal epithelium in both xenopus and the axolotl disorganizes ...201829535610
morphological and transcriptomic analyses reveal three discrete primary stages of postembryonic development in the common fire salamander, salamandra salamandra.the postembryonic development of amphibians has been characterized as divided into three predominant periods, hereafter named primary developmental stages: premetamorphosis (prem), prometamorphosis (prom), metamorphic climax (meta), and completion of metamorphosis (postm), largely based on examination of anuran development. here, we categorized the postembryonic development of larvae of a poisonous fire salamander (salamandra salamandra) by integrating morphology and gene expression (transcripto ...201829504232
protein expression pattern and analysis of differentially expressed peptides during various stages of tail regeneration in hemidactylus flaviviridis.epimorphic regeneration is a process allowing the animal to regain its lost structure which depends on the resident pluripotent stem cells as well as de-differentiation of existing cells to form multi-potent stem cells. many studies have been done to understand the appendage regeneration mechanism. the animal model used since decades is an urodele amphibian the axolotl. however, this ability is also seen in some members of reptiles, mainly lizards which on autotomy of tail regain the same by for ...201829410260
buoyancy disorders in pet axolotls ambystoma mexicanum: three cases.as far as we are aware, there are no previous reports on the pathologic conditions of buoyancy disorders in ambystoma mexicanum. herein, we describe various clinical test results, clinical outcomes, and the pathological findings of an experimental pneumonectomy procedure in 3 a. mexicanum exhibiting abnormal buoyancy. the 3 pet a. mexicanum were adults, and their respective ages and body weights were 1, 5, and 6 yr and 48, 55, and 56 g. two of these cases were confirmed via radiographic examinat ...201829384486
the axolotl genome and the evolution of key tissue formation regulators.salamanders serve as important tetrapod models for developmental, regeneration and evolutionary studies. an extensive molecular toolkit makes the mexican axolotl (ambystoma mexicanum) a key representative salamander for molecular investigations. here we report the sequencing and assembly of the 32-gigabase-pair axolotl genome using an approach that combined long-read sequencing, optical mapping and development of a new genome assembler (marvel). we observed a size expansion of introns and interg ...201829364872
complement receptor c5ar1 plays an evolutionarily conserved role in successful cardiac regeneration.background-defining conserved molecular pathways in animal models of successful cardiac regeneration could yield insight into why adult mammals have inadequate cardiac regeneration after injury. insight into the transcriptomic landscape of early cardiac regeneration from model organisms will shed light on evolutionarily conserved pathways in successful cardiac regeneration.methods-here we describe a cross-species transcriptomic screen in three model organisms for cardiac regeneration -axolotl, n ...201829348261
virtual genome walking across the 32 gb ambystoma mexicanum genome; assembling gene models and intronic sequence.large repeat rich genomes present challenges for assembly using short read technologies. the 32 gb axolotl genome is estimated to contain ~19 gb of repetitive dna making an assembly from short reads alone effectively impossible. indeed, this model species has been sequenced to 20× coverage but the reads could not be conventionally assembled. using an alternative strategy, we have assembled subsets of these reads into scaffolds describing over 19,000 gene models. we call this method virtual genom ...029330416
identification of regenerative roadblocks via repeat deployment of limb regeneration in axolotls.axolotl salamanders are powerful models for understanding how regeneration of complex body parts can be achieved, whereas mammals are severely limited in this ability. factors that promote normal axolotl regeneration can be examined in mammals to determine if they exhibit altered activity in this context. furthermore, factors prohibiting axolotl regeneration can offer key insight into the mechanisms present in regeneration-incompetent species. we sought to determine if we could experimentally co ...201729302364
tissue- and time-directed electroporation of cas9 protein-grna complexes in vivo yields efficient multigene knockout for studying gene function in regeneration.a rapid method for temporally and spatially controlled crispr-mediated gene knockout in vertebrates will be an important tool to screen for genes involved in complex biological phenomena like regeneration. here we show that in vivo injection of cas9 protein-guide rna (grna) complexes into the spinal cord lumen of the axolotl and subsequent electroporation leads to comprehensive knockout of sox2 gene expression in sox2+ neural stem cells with corresponding functional phenotypes from the gene knoc ...201629302334
limb regeneration in a direct-developing terrestrial salamander, bolitoglossa ramosi (caudata: plethodontidae): limb regeneration in plethodontid salamanders.appendage regeneration is one of the most compelling phenomena in regenerative biology and is extensively studied in axolotls and newts. however, the regenerative capacity in other families of salamanders remains poorly described. here we characterize the limb regeneration process in bolitoglossa ramosi, a direct-developing terrestrial salamander of the plethodontid family. we (1) describe the major morphological features at different stages of limb regeneration, (2) show that appendage regenera ...201729299325
transcriptional landscapes of axolotl (ambystoma mexicanum).the axolotl (ambystoma mexicanum) is the vertebrate model system with the highest regeneration capacity. experimental tools established over the past 100 years have been fundamental to start unraveling the cellular and molecular basis of tissue and limb regeneration. in the absence of a reference genome for the axolotl, transcriptomic analysis become fundamental to understand the genetic basis of regeneration. here we present one of the most diverse transcriptomic data sets for axolotl by profil ...029291975
reading and editing the pleurodeles waltl genome reveals novel features of tetrapod regeneration.salamanders exhibit an extraordinary ability among vertebrates to regenerate complex body parts. however, scarce genomic resources have limited our understanding of regeneration in adult salamanders. here, we present the ~20 gb genome and transcriptome of the iberian ribbed newt pleurodeles waltl, a tractable species suitable for laboratory research. we find that embryonic stem cell-specific mirnas mir-93b and mir-427/430/302, as well as harbinger dna transposons carrying the myb-like proto-onco ...201729273779
heart regeneration in adult xenopus tropicalis after apical resection.myocardium regeneration in adult mammals is very limited, but has enormous therapeutic potentials. however, we are far from complete understanding the cellular and molecular mechanisms by which heart tissue can regenerate. the full functional ability of amphibians to regenerate makes them powerful animal models for elucidating how damaged mature organs are naturally reconstituted in an adult organism. like other amphibians, such as newts and axolotls, adult xenopus displays high regenerative cap ...201729255592
regulation of regeneration by heparan sulfate proteoglycans in the extracellular matrix.just as the building of a house requires a blueprint, the rebuilding of lost or damaged body parts through regeneration requires a set of instructions for the assembly of the various tissues into the right places. much progress has been made in understanding how to control the differentiation of different cell types to provide the building blocks for regeneration, such as bone, muscle, blood vessels and nerves/schwann cells. these are the cells that follow the blueprint (the pattern-following ce ...201729242821
the axolotl limb regeneration model as a discovery tool for engineering the stem cell niche.recent advances in genomics and gene editing have expanded the range of model organisms to include those with interesting biological capabilities such as regeneration. among these are the classic models of regeneration biology, the salamander. although stimulating endogenous regeneration in humans likely is many years away, with advances in stem cell biology and biomedical engineering (e.g. bio-inspired materials), it is evident that there is great potential to enhance regenerative outcomes by a ...201729230380
pseudotyped baculovirus is an effective gene expression tool for studying molecular function during axolotl limb regeneration.axolotls can regenerate complex structures through recruitment and remodeling of cells within mature tissues. accessing the underlying mechanisms at a molecular resolution is crucial to understand how injury triggers regeneration and how it proceeds. however, gene transformation in adult tissues can be challenging. here we characterize the use of pseudotyped baculovirus (bv) as an effective gene transfer method both for cells within mature limb tissue and within the blastema. these cells remain ...029198566
biology's beloved amphibian - the axolotl - is racing towards extinction. 201729144487
transcriptome dynamics along axolotl regenerative development are consistent with an extensive reduction in gene expression heterogeneity in dedifferentiated cells.although in recent years the study of gene expression variation in the absence of genetic or environmental cues or gene expression heterogeneity has intensified considerably, many basic and applied biological fields still remain unaware of how useful the study of gene expression heterogeneity patterns might be for the characterization of biological systems and/or processes. largely based on the modulator effect chromatin compaction has for gene expression heterogeneity and the extensive changes ...201729134148
systemic cell cycle activation is induced following complex tissue injury in axolotl.activation of progenitor cells is crucial to promote tissue repair following injury in adult animals. in the context of successful limb regeneration following amputation, progenitor cells residing within the stump must re-enter the cell cycle to promote regrowth of the missing limb. we demonstrate that in axolotls, amputation is sufficient to induce cell-cycle activation in both the amputated limb and the intact, uninjured contralateral limb. activated cells were found throughout all major tissu ...029111100
transcriptional correlates of proximal-distal identify and regeneration timing in axolotl limbs.cells within salamander limbs retain memories that inform the correct replacement of amputated tissues at different positions along the length of the arm, with proximal and amputations completing regeneration at similar times. we investigated the possibility that positional memory is associated with variation in transcript abundances along the proximal-distal limb axis. transcripts were deeply sampled from ambystoma mexicanum limbs at the time they were administered fore arm vs upper arm amputat ...201729107037
efficient gene knockin in axolotl and its use to test the role of satellite cells in limb regeneration.salamanders exhibit extensive regenerative capacities and serve as a unique model in regeneration research. however, due to the lack of targeted gene knockin approaches, it has been difficult to label and manipulate some of the cell populations that are crucial for understanding the mechanisms underlying regeneration. here we have established highly efficient gene knockin approaches in the axolotl (ambystoma mexicanum) based on the crispr/cas9 technology. using a homology-independent method, we ...201729087939
salamander spinal cord regeneration: the ultimate positive control in vertebrate spinal cord regeneration.repairing injured tissues / organs is one of the major challenges for the maintenance of proper organ function in adulthood. in mammals, the central nervous system including the spinal cord, once established during embryonic development, has very limited capacity to regenerate. in contrast, salamanders such as axolotls can fully regenerate the injured spinal cord, making this a very powerful vertebrate model system for studying this process. here we discuss the cellular and molecular requirement ...201729030146
a new and improved algorithm for the quantification of chromatin condensation from microscopic data shows decreased chromatin condensation in regenerating axolotl limb cells.the nuclear landscape plays an important role in the regulation of tissue and positional specific genes in embryonic and developing cells. changes in this landscape can be dynamic, and are associated with the differentiation of cells during embryogenesis, and the de-differentiation of cells during induced pluripotent stem cell (ipsc) formation and in many cancers. however, tools to quantitatively characterize these changes are limited, especially in the in vivo context, where numerous tissue typ ...201729023511
propofol (2,6-diisopropylphenol) is an applicable immersion anesthetic in the axolotl with potential uses in hemodynamic and neurophysiological experiments.the mexican axolotl (ambystoma mexicanum) is an important model species in regenerative biology. traditionally, axolotls are anesthetized using benzocaine or ms-222, both of which act to inhibit voltage gated sodium channels thereby preventing action potential propagation. in some neurophysiological experiments this is not desirable; therefore we tested propofol as an alternative anesthetic in the axolotl. we evaluated benzocaine, ms-222, and propofol's cardiovascular effects, effects on action ...201728975032
a novel role for sall4 during scar-free wound healing in axolotl.the human response to serious cutaneous damage is limited to relatively primitive wound healing, whereby collagenous scar tissue fills the wound bed. scars assure structural integrity at the expense of functional regeneration. in contrast, axolotls have the remarkable capacity to functionally regenerate full thickness wounds. here, we identified a novel role for sall4 in regulating collagen transcription after injury that is essential for perfect skin regeneration in axolotl. furthermore, we ide ...201628955504
inhibition of vascular endothelial growth factor receptor decreases regenerative angiogenesis in axolotls.angiogenesis is crucial for tissue growth and repair in mammals, and is chiefly regulated by vascular endothelial growth factor (vegf) signaling. we evaluated the effect of chemical inhibition of vegf receptor signaling in animals with superior regenerative ability, axolotl salamanders, to determine the impact on vascularization and regenerative outgrowth. following tail amputation, treated animals (100 nm ptk787) and controls were examined microscopically and measured over the month-long period ...201728921926
lineage tracing of genome-edited alleles reveals high fidelity axolotl limb regeneration.salamanders are unparalleled among tetrapods in their ability to regenerate many structures, including entire limbs, and the study of this ability may provide insights into human regenerative therapies. the complex structure of the limb poses challenges to the investigation of the cellular and molecular basis of its regeneration. using crispr/cas, we genetically labelled unique cell lineages within the developing axolotl embryo and tracked the frequency of each lineage within amputated and fully ...201728917058
comparison of tissue processing methods for microvascular visualization in axolotls.the vascular system, the pipeline for oxygen and nutrient delivery to tissues, is essential for vertebrate development, growth, injury repair, and regeneration. with their capacity to regenerate entire appendages throughout their lifespan, axolotls are an unparalleled model for vertebrate regeneration, but they lack many of the molecular tools that facilitate vascular imaging in other animal models. the determination of vascular metrics requires high quality image data for the discrimination of ...201728913170
novel axolotl cardiac function analysis method using magnetic resonance imaging.the salamander axolotl is capable of complete regeneration of amputated heart tissue. however, non-invasive imaging tools for assessing its cardiac function were so far not employed. in this study, cardiac magnetic resonance imaging is introduced as a non-invasive technique to image heart function of axolotls. three axolotls were imaged with magnetic resonance imaging using a retrospectively gated fast low angle shot cine sequence. within one scanning session the axolotl heart was imaged three t ...201728837595
tail regeneration and other phenomena of wound healing and tissue restoration in lizards.wound healing is a fundamental evolutionary adaptation with two possible outcomes: scar formation or reparative regeneration. scars participate in re-forming the barrier with the external environment and restoring homeostasis to injured tissues, but are well understood to represent dysfunctional replacements. in contrast, reparative regeneration is a tissue-specific program that near-perfectly replicates that which was lost or damaged. although regeneration is best known from salamanders (includ ...201728814609
dii perfusion as a method for vascular visualization in ambystoma mexicanum.perfusion techniques have been used for centuries to visualize the circulation of tissues. axolotl (ambystoma mexicanum) is a species of salamander that has emerged as an essential model for regeneration studies. little is known about how revascularization occurs in the context of regeneration in these animals. here we report a simple method for visualization of the vasculature in axolotl via perfusion of 1,1'-dioctadecy-3,3,3',3'-tetramethylindocarbocyanine perchlorate (dii). dii is a lipophili ...201728654050
advances in decoding axolotl limb regeneration.humans and other mammals are limited in their natural abilities to regenerate lost body parts. by contrast, many salamanders are highly regenerative and can spontaneously replace lost limbs even as adults. because salamander limbs are anatomically similar to human limbs, knowing how they regenerate should provide important clues for regenerative medicine. although interest in understanding the mechanics of this process has never wavered, until recently researchers have been vexed by seemingly im ...201728648452
ion channel signaling influences cellular proliferation and phagocyte activity during axolotl tail regeneration.little is known about the potential for ion channels to regulate cellular behaviors during tissue regeneration. here, we utilized an amphibian tail regeneration assay coupled with a chemical genetic screen to identify ion channel antagonists that altered critical cellular processes during regeneration. inhibition of multiple ion channels either partially (anoctamin1/tmem16a, anoctamin2/tmem16b, kv2.1, kv2.2, l-type cav channels and h/k atpases) or completely (glyr, gabaar, kv1.5 and serca pumps) ...201728603004
the polytypic species revisited: genetic differentiation and molecular phylogenetics of the tiger salamander ambystoma tigrinum (amphibia: caudata) complex.we present a phylogenetic analysis of the ambystoma tigrinum complex, based on approximately 840 base pairs of mitochondrial-dna sequence from the rapidly evolving d-loop and an adjacent intron. our samples include populations of the continentally distributed species, a. tigrinum, plus all described species of mexican ambystomatids. sequence divergence is low, ranging from 0-8.5%, and most phylogenetic groupings are weakly supported statistically. we identified eight reasonably well-defined clad ...199628568845
caenogenesis, developmental variability, and evolution in the carpus and tarsus of the marbled newt triturus marmoratus.in this paper, after a comparative analysis of the development of triturus marmoratus, we explore the existence of caenogenetic events and their ontogenetic and phylogenetic consequences. the adult morphology of the triturus marmoratus limb, in terms of number and spatial arrangement of skeletal elements, agrees with the general pattern of urodeles. the congruence in the typical pattern of adult morphology does not hint at the striking differences in embryonic development. these differences can ...199228568662
a retrospective study of diseases in ambystoma mexicanum: a report of 97 cases.ambystoma mexicanum kept as pets are affected by a variety of diseases. however, no reports regarding the incidence of specific diseases are available. this study aimed to identify the diseases that occur frequently in this species by surveying the incidence of conditions in pet a. mexicanum specimens brought to a veterinary hospital. the sample comprised 97 pet a. mexicanum individuals brought to the authors' hospital during the 82-month period, i.e., from january 2008 to october 2014. in total ...201728529268
senescence gives insights into the morphogenetic evolution of anamniotes.senescence represents a mechanism to avoid undesired cell proliferation that plays a role in tumor suppression, wound healing and embryonic development. in order to gain insight on the evolution of senescence, we looked at its presence in developing axolotls (urodele amphibians) and in zebrafish (teleost fish), which are both anamniotes. our data indicate that cellular senescence is present in various developing structures in axolotls (pronephros, olfactory epithelium of nerve fascicles, lateral ...201728500032
a brief history of the study of nerve dependent regeneration.nerve dependence is a phenomenon observed across a stunning array of species and tissues. from zebrafish to fetal mice to humans, research across various animal models has shown that nerves are critical for the support of tissue repair and regeneration. although the study of this phenomenon has persisted for centuries, largely through research conducted in salamanders, the cellular and molecular mechanisms of nerve dependence remain poorly-understood. here we highlight the near-ubiquity and clin ...201728459075
tissue regeneration in dentistry: can salamanders provide insight?the ability to regenerate damaged tissues would be of tremendous benefit for medicine and dentistry. unfortunately, humans are unable to regenerate tissues such as teeth and fingers or to repair injured spinal cord. with an aging population, health problems are more prominent and dentistry is no exception as loss of bone tissue in the orofacial sphere from periodontal disease is on the rise. humans can repair oral soft tissues exceptionally well; however, hard tissues, such as bone and teeth, ar ...201728376251
embryonic yolk removal affects neither morphology nor escape performance of larval axolotls.maternal effects, the influences of maternal phenotype on the phenotypes of her offspring, mediate early ontogenetic traits through maternal investment. in amphibians, provisioning eggs with yolk is the main source of maternal investment. while larger eggs generally result in larger, higher-quality offspring, the relationship between egg size and offspring phenotype is complicated because offspring can evolve to be more or less responsive to variation in yolk provisions. previous studies of seve ...201728365231
studies on the process of lens induction inxenopus laevis (daudin).1. optic vesicle from stage 24 (nieuwkoop andfaber 1956) can induce lens in the ectoderm from early to mid grastrula, and even from ventral ectoderm of a tail bud stage. 2. lenses were induced from early ectoderm cultured over night before grafting even though it remained thick. 3. for lens formation and its differentiation, prolonged contact with the optic vesicle seems essential. 4. lens anlage removed from the influence of the optic vesicle as late as the stage 24 (nieuwkoop andfaber 1956) an ...195928354744
data on chemical activation of wnt/β-catenin during axolotl limb regeneration.limb amputation in axolotls was performed to obtain data demonstrating that a chemical agonist of wnt (int-related protein)/β-catenin signalling can have a role in axolotl limb regeneration (wischin et al., 2017) [1]. the data revealed that active β-catenin protein was present during limb regeneration in some leydig cells in the epithelium; after the chemical treatment, it was observed in more leydig cells. in addition, the chemical agonist of wnt generated distinct limb malformation.201728349103
evidence for a nuclear factor involved in c-myc rna degradation during axolotl oocyte maturation.we have previously described an in vivo heterologous system which has allowed us to study the stability of different xenopus c-myc rna constructs injected into axolotl oocytes. in full-grown oocytes, degradation of c-myc rna does not occur. in mature oocytes treated with progesterone, transcripts containing the coding sequence of the gene are degraded, whereas those corresponding to the 3'utr (untranslated region) alone are stable. in order to study the role of nuclear or cytoplasmic components ...199528306080
differential stability of xenopus c-myc rna during oogenesis in axolotl involvement of the 3' untranslated region in vivo.we have used the axolotl oocyte (ambystoma mexicanum shaw) to study the stability of exogenously injected xenopus rnas. three different cellular developmental stages have been analysed: (1) the growing oocyte (stage iii-iv of vitellogenesis), (2) the full-grown oocyte at the end of vitellogenesis (stage vi) and (3) the progesterone-matured stage vi oocyte. three exogenous rnas have been synthesized in vitro from a c-myc xenopus cdna clone. one transcript is 2.3 kb long (full length), the second ...199528306079
morphogenetic movements during axolotl neural tube formation tracked by digital imaging.during neurulation in vertebrate embryos, epithelial cells of the neural plate undergo complex morphogenetic movements that culminate in rolling of the plate into a tube. resolution of the determinants of this process requires an understanding of the precise movements of cells within the epithelial sheet. a computer algorithm that allows automated tracking of epithelial cells visible in digitized video images is presented. it is used to quantify the displacement field associated with morphogenet ...199628306034
effects of retinoic acid on regenerating normal and double half limbs of axolotls : histological studies.retinoids induce proximodistal (pd) pattern duplication in zeugopodial (lower arm or leg) regenerates of normal limbs and pd pattern duplication plus anteroposterior (ap) pattern completion in double anterior half zeugopodial regenerates. in contrast, retinoids inhibit the regeneration of double posterior half zeugopodia (kim and stocum, 1986). here we describe the developmental histology of regenerating normal, double anterior half and double posterior half zeugopodia in axolotls after intraper ...198628306010
stability of positional identity of axolotl blastema cells in vitro.previous grafting experiments have demonstrated that cells from non-contiguous positions within developing and regenerating limbs differ in a property referred to as positional identity. the goal of this study was to determine how long the positional identity of axolotl limb blastema cells is stable during culture in vitro. we have developed an assay for posterior positional properties such that blastema cells can be cultured and then grafted into anterior positions in host blastemas, to determi ...199328305994
mesoderm differentiation in early amphibian embryos depends on the animal cap.embryos of ambystoma mexicanum from the late morula to the late blastula stage were dissected and cultivated in varying combinations. the marginal zone (presumptive mesoderm) when isolated together with the vegetal region differentiated to notochord after dissection from early blastulae, but did not differentiate to other tissues. when isolated from middle to late blastulae, in addition myoblasts and mesenchyme were formed. the marginal zone isolated together with the animal region (presumptive ...199328305977
morphogenetic effects of 9-cis-retinoic acid on the regenerating limbs of the axolotl.9-cis-retinoic acid has recently been found to be a high affinity ligand for the retinoic x receptor (rxr). rxrs are believed to be involved in metabolic activities rather than in morphogenetic ones. interestingly, rxr has been found to form heterodimers involving other receptors from the steroid family, such as the thyroid hormone receptor, vitamin d receptor or retinoic acid receptors (rars). in this paper we examined whether or not 9-cis-retinoic acid had any morphogenetic properties on the r ...199428305887
the relationship between migration and chondrogenic potential of trunk neural crest cells in ambystoma mexicanum.based on results of transplantation experiments, it has long been believed that trunk neural crest cells are incapable of chondrogenesis. when pigmented trunk neural crest cells of ambystoma mexicanum are transplanted to cranial levels of albino (a/a) embryos, the graft cells ultimately produce ectopic fins, but are incapable of following the chondrogenic cranial neural crest pathways. therefore, heterotopic transplantation does not expose these cells to the same environment experienced by crani ...199528305867
the effects of retinoic acid on mitosis during tail and limb regeneration in the axolotl larva, ambystoma mexicanum.regenerating tails and limbs of axolotl larvae (a. mexicanum) were studied for overall growth and for mitosis after the animals received intraperitoneal injections of all-trans retinoic acid. both processes were depressed to approximately the same extent (60-70%). some mitosis always survived, even when the treatment was in effect during the entire history of the regenerate. the treatment duration was a major variable in the severity of the effect, whereas the post-amputation age of the regenera ...198728305840
in vitro control of blastema cell proliferation by extracts from epidermal cap and mesenchyme of regenerating limbs of axolotls.the presence of a mitogenic activity in limb blastemas of axolotls was detected in crude extracts of blastemas at the mid-bud stage. the mitogenicity of the extracts was estimated from the mitotic index of blastema cells grown for 6 days in the presence of limb blastema extracts, with colchicine present for the last 2 days. all the extracts tested (whole blastema, blastemal mesenchyme, epidermal cap) significantly enhanced proliferation of blastema cells. the highest stimulation factors we obser ...199028305671
serially duplicated regenerates from the anterior half of the axolotl limb after retinoic acid treatment.axolotl (ambystoma mexicanum) forearms were divided, by an incision between the radius and ulna, to produce anterior and posterior halves. these were prevented from fusing together again by a graft of head skin and amputated through the wrist. this procedure enabled independent regeneration from both halves of the stump. anterior half stumps produced a single digit while the posterior halves mainly regenerated three digits, the two halves together making a single hand. treatment with retinoic ac ...199028305663
effect of transferrin on amphibian limb regeneration: a blastema cell culture study.in order to study mitogenic control during axolotl limb regeneration, we have developed a primary blastema cell culture as a very sensitive bioassay for blastema mitogens. transferrin, an iron-binding glycoprotein which has been shown to be the neurotrophic factor for muscle cells, is the mitogen which has been analysed in the present report. addition of approximately 2 μg human transferrin/ ml of serum-free culture medium enhances blastema cell proliferation 11-fold over control levels and 2-fo ...198828305565
involvement of the cytoskeleton in early grey crescent formation in axolotl oocytes.maturing axolotl oocytes which are treated with protein synthesis inhibitors or which are heat-shocked can be induced to reorganize their cytoplasm and to form an early grey crescent. the maturing axolotl oocyte has been used as a model system to study the role of the cytoskeleton in dorsoventral polarization as visualized by grey crescent formation. results presented here provide evidence for the involvement of microtubules in the formation of the early grey crescent. whereas inhibitors of micr ...198728305553
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