Volume 37 Issue 4
Jul.  2016
Turn off MathJax
Article Contents
Lu-Sha LIU, Lan-Ying ZHAO, Shou-Hong WANG, Jian-Ping JIANG. Research proceedings on amphibian model organisms. Zoological Research, 2016, 37(4): 237-245. doi: 10.13918/j.issn.2095-8137.2016.4.237
Citation: Lu-Sha LIU, Lan-Ying ZHAO, Shou-Hong WANG, Jian-Ping JIANG. Research proceedings on amphibian model organisms. Zoological Research, 2016, 37(4): 237-245. doi: 10.13918/j.issn.2095-8137.2016.4.237

Research proceedings on amphibian model organisms

doi: 10.13918/j.issn.2095-8137.2016.4.237
Funds:  This study was supported by a grant from the Key Programs of the Chinese Academy of Sciences (KJZD-EW-L13), 2015 Western Light Talent Culture Project of the Chinese Academy of Sciences (Y6C3021), and the National Natural Science Foundation of China (31471964)
More Information
  • Corresponding author: Jian-Ping JIANG
  • Received Date: 2016-03-20
  • Rev Recd Date: 2016-06-10
  • Publish Date: 2016-07-18
  • Model organisms have long been important in biology and medicine due to their specific characteristics. Amphibians, especially Xenopus, play key roles in answering fundamental questions on developmental biology, regeneration, genetics, and toxicology due to their large and abundant eggs, as well as their versatile embryos, which can be readily manipulated and developed in vivo. Furthermore, amphibians have also proven to be of considerable benefit in human disease research due to their conserved cellular developmental and genomic organization. This review gives a brief introduction on the progress and limitations of these animal models in biology and human disease research, and discusses the potential and challenge of Microhyla fissipes as a new model organism.
  • loading
  • [1]
    Abu-Daya A, Sater AK, Wells DE, Mohun TJ, Zimmerman LB. 2009. Absence of heartbeat in the Xenopus tropicalis mutation muzak is caused by a nonsense mutation in cardiac myosin myh6. Developmental Biology, 336(1):20-29.
    [2]
    Amir RE, van den Veyver IB, Wan MM, Tran CQ, Francke U, Zoghbi HY. 1999. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nature Genetics, 23(2):185-188.
    [3]
    Barribeau SM, Villinger J, Waldman B. 2008. Major histocompatibility complex based resistance to a common bacterial pathogen of amphibians. PLoS One, 3(7):e2692.
    [4]
    Beck CW, Izpisúa Belmonte JC, Christen B. 2009. Beyond early development:Xenopus as an emerging model for the study of regenerative mechanisms. Developmental Dynamics, 238(6):1226-1248.
    [5]
    Berg C, Gyllenhammar I, Kvarnryd M. 2009. Xenopus tropicalis as a test system for developmental and reproductive toxicity. Journal of Toxicology and Environmental Health, Part A:Current Issues, 72(3-4):219-225.
    [6]
    Bevan CL, Porter DM, Prasad A, Howard MJ, Henderson LP. 2003. Environmental estrogens alter early development in Xenopus laevis. Environmental Health Perspectives, 111(4):488-496.
    [7]
    Bonnard C, Strobl AC, Shboul M, Lee H, Merriman B, Nelson SF, Ababneh OH, Uz E, Güran T, Kayserili H, Hamamy H, Reversade B. 2012. Mutations in IRX5 impair craniofacial development and germ cell migration via SDF1. Nature Genetics, 44(6):709-713.
    [8]
    Brockes JP. 1997. Amphibian limb regeneration:rebuilding a complex structure. Science, 276(5309):81-87.
    [9]
    Chen WY, Wang ZS, Wang XZ, Yang YH, Sun QL. 1983. A comparative study of the karyotypes from six species of frogs in Sichuan. Zoological Research, 4(1):83-88. (in Chinese)
    [10]
    Chida AS, Goyos A, Robert J. 2011. Phylogenetic and developmental study of CD4, CD8 α and β T cell co-receptor homologs in two amphibian species, Xenopus tropicalis and Xenopus laevis. Developmental & Comparative Immunology, 35(3):366-377.
    [11]
    Chien AJ, Conrad WH, Moon RT. 2009. A Wnt survival guide:from flies to human disease. Journal of Investigative Dermatology, 129(7):1614-1627.
    [12]
    Chitramuthu BP. 2013. Modeling human disease and development in zebrafish. Human Genetics & Embryology, 3(1):1000e108.
    [13]
    Ciau-Uitz A, Pinheiro P, Kirmizitas A, Zuo J, Patient R. 2013. VEGFA-dependent and -independent pathways synergise to drive Scl expression and initiate programming of the blood stem cell lineage in Xenopus. Development, 140(12):2632-2642.
    [14]
    Damjanovski S, Amano T, Li Q, Ueda S, Shi YB, Ishizuya-Oka A. 2000. Role of ECM remodeling in thyroid hormone-dependent apoptosis during anuran metamorphosis. Annals of the New York Academy of Sciences, 926:180-191.
    [15]
    Delaune E, Lemaire P, Kodjabachian L. 2005. Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development, 132(2):299-310.
    [16]
    Dent JN. 1962. Limb regeneration in larvae and metamorphosing individuals of the South African clawed toad. Journal of Morphology, 110(1):61-77.
    [17]
    Dumpert K, Zietz E. 1984. Platanna (Xenopus laevis) as a test organism for determining the embryotoxic effects of environmental chemicals. Ecotoxicology and Environmental Safety, 8(1):55-74.
    [18]
    Fei L, Ye CY, Xia Y. 1987. Study on the limb regeneration of Cynops cyanurus chuxiongensis. Chinese Journal of Zoology, 22(5):14-18. (in Chinese)
    [19]
    Fei L, Hu SQ, Ye CY, Huang YZ. 2009. Fauna of China:Amphibians (Vol. 2). Beijing:Science Press, 904-910. (in Chinese)
    [20]
    Fields S, Johnston M. 2005. Whither model organism research? Science, 307(5717):1885-1886.
    [21]
    Fites JS, Ramsey JP, Holden WM, Collier SP, Sutherland DM, Reinert LK, Gayek AS, Dermody TS, Aune TM, Oswald-Richter K, Rollins-Smith LA. 2013. The invasive chytrid fungus of amphibians paralyzes lymphocyte responses. Science, 342(6156):366-369.
    [22]
    Fites JS, Reinert LK, Chappell TM, Rollins-Smith LA. 2014. Inhibition of local immune responses by the frog-killing fungus Batrachochytrium dendrobatidis. Infection and Immunity, 82(11):4698-4706.
    [23]
    Geschwind DH. 2009. Advances in autism. Annual Review of Medicine, 60(1):367-380.
    [24]
    Gosner KL. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3):183-190.
    [25]
    Gotoh T, Villa LM, Capelluto DGS, Finkielstein CV. 2011. Regulatory pathways coordinating cell cycle progression in early Xenopus development. In:Kubiak JZ. Cell Cycle in Development:Results and Problems in Cell Differentiation, 53:171-199.
    [26]
    Grant IM, Balcha D, Hao T, Shen Y, Trivedi P, Patrushev I, Fortriede JD, Karpinka JB, Liu LM, Zorn AM, Stukenberg PT, Hill DE, Gilchrist MJ. 2015. The Xenopus ORFeome:a resource that enables functional genomics. Developmental Biology, 408(2):345-357.
    [27]
    Guo XG, Zhang TJ, Hu Z, Zhang YQ, Shi ZY, Wang QH, Cui Y, Wang FQ, Zhao H, Chen YL. 2014. Efficient RNA/Cas9-mediated genome editing in Xenopus tropicalis. Development, 141(3):707-714.
    [28]
    Gurdon JB, Elsdale TR, Fischberg M. 1958. Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature, 182(4627):64-65.
    [29]
    Hardwick LJA, Philpott A. 2015. An oncologist's friend:how Xenopus contributes to cancer research. Developmental Biology, 408(2):180-187.
    [30]
    Harland RM, Grainger RM. 2011. Xenopus research:metamorphosed by genetics and genomics. Trends in Genetics, 27(12):507-515.
    [31]
    Hartley KO, Hardcastle Z, Friday RV, Amaya E, Papalopulu N. 2001. Transgenic Xenopus embryos reveal that anterior neural development requires continued suppression of BMP signaling after gastrulation. Developmental Biology, 238(1):168-184.
    [32]
    Heimeier RA, Das B, Buchholz DR, Fiorentino M, Shi YB. 2010. Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome Biology, 11(5):R55.
    [33]
    Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu SQ, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS. 2010. The genome of the Western clawed frog Xenopus tropicalis. Science, 328(5978):633-636.
    [34]
    Hemmati-Brivanlou A, Melton DA. 1994. Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell, 77(2):273-281.
    [35]
    Hirsch N, Zimmerman LB, Grainger RM. 2002a. Xenopus, the next generation:X. Tropicalis genetics and genomics. Developmental Dynamics, 225(4):422-433.
    [36]
    Hirsch N, Zimmerman LB, Gray J, Chae J, Curran KL, Fisher M, Ogino H, Grainger RM. 2002b. Xenopus tropicalis transgenic lines and their use in the study of embryonic induction. Developmental Dynamics, 225(4):522-535.
    [37]
    Ho DM, Whitman M. 2008. TGF-β signaling is required for multiple processes during Xenopus tail regeneration. Developmental Biology, 315(1):203-216.
    [38]
    Horb M, Zorn A, Baker J, Buchholz D, Moody S, Rokhsar D, Sokol S, Veenstra G, Khokha M. Xenbase. 2014 Xenopus Community White Paper. (2014) Available at:http://www.xenbase.org/community/xenopuswhitepaper.do.
    [39]
    Ishizuya-Oka A, Kajita M, Hasebe T. 2014. Thyroid Hormone-regulated Wnt5a/Ror2 signaling is essential for dedifferentiation of larval epithelial cells into adult stem cells in the Xenopus laevis intestine. PLoS One, 9(9):e107611.
    [40]
    Khoudoli GA, Gillespie PJ, Stewart G, Andersen JS, Swedlow JR, Blow JJ. 2008. Temporal profiling of the chromatin proteome reveals system-wide responses to replication inhibition. Current Biology, 18(11):838-843.
    [41]
    Kinoshita M, Ariizumi T, Yuasa S, Miyoshi S, Komazaki S, Fukuda K, Asashima M. 2010. Creating frog heart as an organ:in vitro-induced heart functions as a circulatory organ in vivo. The International Journal of Developmental Biology, 54(5):851-856.
    [42]
    LaBonne C, Zorn AM. 2015. Modeling human development and disease in Xenopus. Developmental Biology, 408(2):179.
    [43]
    Lamb TM, Knecht AK, Smith WC, Stachel SE, Economides AN, Stahl N, Yancopolous GD, Harland RM. 1993. Neural induction by the secreted polypeptide noggin. Science, 262(5134):713-718.
    [44]
    Lee-Liu D, Moreno M, Almonacid LI, Tapia VS, Muñoz R, von Marées J, Gaete M, Melo F, Larraín J. 2014. Genome-wide expression profile of the response to spinal cord injury in Xenopus laevis reveals extensive differences between regenerative and non-regenerative stages. Neural Development, 9:12.
    [45]
    Lei Y, Guo XG, Liu Y, Cao Y, Deng Y, Chen XF, Cheng CHK, Dawid IB, Chen YL, Zhao H. 2012. Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proceedings of the National Academy of Sciences of the United States of America, 109(43):17484-17489.
    [46]
    Li J, Meyer AN, Donoghue DJ. 1995. Requirement for phosphorylation of cyclin B1 for Xenopus oocyte maturation. Molecular Biology of the Cell, 6(9):1111-1124.
    [47]
    Li JX, Xu XQ, Xu CH, Zhou WP, Zhang KY, Yu HN, Zhang YP, Zheng YT, Rees HH, Lai R, Yang DM, Wu J. 2007. Anti-infection peptidomics of amphibian skin. Molecular & Cell Proteomics, 6(5):882-894.
    [48]
    Lin GF, Slack JMW. 2008. Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Developmental Biology, 316(2):323-335.
    [49]
    Luca V, Stringaro A, Colone M, Pini A, Mangoni ML. 2013. Esculentin(1-21), an amphibian skin membrane-active peptide with potent activity on both planktonic and biofilm cells of the bacterial pathogen Pseudomonas aeruginosa. Cellular and Molecular Life Sciences, 70(15):2773-2786.
    [50]
    Makanae A, Mitogawa K, Satoh A. 2016. Cooperative inputs of Bmp and Fgf signaling induce tail regeneration in urodele amphibians. Developmental Biology, 410(1):45-55.
    [51]
    Marshak S, Meynard MM, De Vries YA, Kidane AH, Cohen-Cory S. 2012. Cell-autonomous alterations in dendritic arbor morphology and connectivity induced by overexpression of MeCP2 in Xenopus central neurons in vivo. PLoS One, 7(3):e33153.
    [52]
    Moon RT. 2001. Xenopus Embryo:β-catenin and Dorsal-Ventral Axis Formation. In:eLS.
    [53]
    Morrison JI, Lööf S, He PP, Simon A. 2006. Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. The Journal of Cell Biology, 172(3):433-440.
    [54]
    Nieuwkoop PD. 1985. Inductive interactions in early amphibian development and their general nature. Journal of Embryology and Experimental Morphology, 89(S):333-347.
    [55]
    Odelberg SJ. 2005. Cellular plasticity in vertebrate regeneration. The Anatomical Record Part B:The New Anatomist, 287B(1):25-35.
    [56]
    Ogino H, Fisher M, Grainger RM. 2008. Convergence of a head-field selector Otx2 and Notch signaling:a mechanism for lens specification. Development, 135(2):249-258.
    [57]
    Pratt KG, Khakhalin AS. 2013. Modeling human neurodevelopmental disorders in the Xenopus tadpole:from mechanisms to therapeutic targets. Disease Models & Mechanisms, 6(5):1057-1065.
    [58]
    Pyron RA, Wiens JJ. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61(2):543-583.
    [59]
    Robert J, Ohta Y. 2009. Comparative and developmental study of the immune system in Xenopus. Developmental Dynamics, 238(6):1249-1270.
    [60]
    Saka Y, Smith JC. 2001. Spatial and temporal patterns of cell division during early Xenopus embryogenesis. Developmental Biology, 229(2):307-318.
    [61]
    Salanga MC, Horb ME. 2015. Xenopus as a model for GI/Pancreas disease. Current Pathobiology Reports, 3(2):137-145.
    [62]
    Saria R, Mouchet F, Perrault A, Flahaut E, Laplanche C, Boutonnet JC, Pinelli E, Gauthier L. 2014. Short term exposure to multi-walled carbon nanotubes induce oxidative stress and DNA damage in Xenopus laevis tadpoles. Ecotoxicology and Environmental Safety, 107:22-29.
    [63]
    Sasai Y, Lu B, Steinbeisser H, De Robertis EM. 1995. Regulation of neural induction by the Chd and BMP-4 antagonistic patterning signals in Xenopus. Nature, 376(6538):333-336.
    [64]
    Satoh A, Mitogawa K, Makanae A. 2015. Regeneration inducers in limb regeneration. Development, Growth & Differentiation, 57(6):421-429.
    [65]
    Savage AE, Kiemnec-Tyburczy KM, Ellison AR, Fleischer RC, Zamudio KR. 2014. Conservation and divergence in the frog immunome:pyrosequencing and de novo assembly of immune tissue transcriptomes. Gene, 542(2):98-108.
    [66]
    Schmitt SM, Gull M, Brändli AW. 2014. Engineering Xenopus embryos for phenotypic drug discovery screening. Advanced Drug Delivery Reviews, 69-70:225-246.
    [67]
    Schweickert A, Feistel K. 2015. The Xenopus embryo:an ideal model system to study human ciliopathies. Current Pathobiology Reports, 3(2):115-127.
    [68]
    Shimizu S, Ota H. 2003. Normal development of Microhyla ornata:the first description of the complete embryonic and larval stages for the Microhylid frogs (Amphibia:Anura). Current Herpetology, 22(2):73-90.
    [69]
    Sitaram N, Sai KP, Singh S, Sankaran K, Nagaraj R. 2002. Structure-function relationship studies on the frog skin antimicrobial peptide tigerinin 1:design of analogs with improved activity and their action on clinical bacterial isolates. Antimicrobial Agents and Chemotherapy, 46(7):2279-2283.
    [70]
    Slack JMW, Beck CW, Gargioli C, Christen B. 2004. Cellular and molecular mechanisms of regeneration in Xenopus. Philosophical Transactions of the Royal Society of London Series B:Biological Sciences, 359(1445):745-751.
    [71]
    Tanaka EM, Reddien PW. 2011. The cellular basis for animal regeneration. Developmental Cell, 21(1):172-185.
    [72]
    Spallanzani L. 1768. Prodromo di un opera da imprimersi sopra la riproduzioni anamali. Giovanni Montanari, Modena.Translated in English by Maty M. 1769.An essay on animal reproduction. London:T. Becket & DeH on dt.
    [73]
    Tata JR. 1996. Metamorphosis:an exquisite model for hormonal regulation of post-embryonic development. Biochemical Society Symposia, 62(1):123-136.
    [74]
    Vernon AE, Devine C, Philpott A. 2003. The cdk inhibitor p27Xic1 is required for differentiation of primary neurones in Xenopus. Development, 130(1):85-92.
    [75]
    Wallace H. 1981. Vertebrate Limb Regeneration. New York:Wiley.
    [76]
    Whitman M. 1998. Smads and early developmental signaling by the TGFβ superfamily. Genes & Development, 12(16):2445-2462.
    [77]
    Woodland HR. 1974. Some studies on early embryonic development relevant to the study of cancer. Journal of Clinical Pathology, 7:26-30.
    [78]
    Xiang Y, Yan C, Guo XL, Zhou KF, Li SA, Gao Q, Wang X, Zhao F, Liu J, Lee WH, Zhang Y. 2014. Host-derived, pore-forming toxin-like protein and trefoil factor complex protects the host against microbial infection. Proceedings of the National Academy of Sciences of the United States of America, 111(18):6702-6707.
    [79]
    Xu XQ, Lai R. 2015. The chemistry and biological activities of peptides from amphibian skin secretions. Chemical Reviews, 115(4):1760-1846.
    [80]
    Yang J, Tan CE, Darken RS, Wilson PA, Klein PS. 2002. β-Catenin/Tcf-regulated transcription prior to the midblastula transition. Development, 129(24):5743-5752.
    [81]
    Ymlahi-Ouazzani Q, Bronchain OJ, Paillard E, Ballagny C, Chesneau A, Jadaud A, Mazabraud A, Pollet N. 2010. Reduced levels of survival motor neuron protein leads to aberrant motoneuron growth in a Xenopus model of muscular atrophy. Neurogenetics, 11(1):27-40.
    [82]
    Yokoyama H, Yonei-Tamura S, Endo T, Izpisúa Belmonte JC, Tamura K, Ide H. 2000. Mesenchyme with fgf-10 expression is responsible for regenerative capacity in Xenopus limb buds. Developmental Biology, 219(1):18-29.
    [83]
    Young JJ, Cherone JM, Doyon Y, Ankoudinova I, Faraji FM, Lee AH, Ngo C, Guschin DY, Paschon DE, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Harland RM, Zeitler B. 2011. Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proceedings of the National Academy of Sciences of the United States of America, 108(17):7052-7057.
    [84]
    Yun MH, Gates PB, Brockes JP. 2014. Sustained ERK activation underlies reprogramming in regeneration-competent salamander cells and distinguishes them from their mammalian counterparts. Stem Cell Reports, 3(1):15-23.
    [85]
    Zhao F, Yan C, Wang X, Yang Y, Wang GY, Lee W, Xiang Y, Zhang Y. 2014. Comprehensive transcriptome profiling and functional analysis of the frog (Bombina maxima) immune system. DNA Research, 21(1):1-13.
    [86]
    Zhao LY, Liu LS, Wang SH, Wang HY, Jiang JP. 2016. Transcriptome profiles of metamorphosis in the ornamented pygmy frog Microhyla fissipes clarify the functions of thyroid hormone receptors in metamorphosis. Scientific Reports. doi: 10.1038/srep27310.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (2049) PDF downloads(1516) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return