Use of Xenopus Frogs to Study Renal Development/Repair

Chapter
Part of the Results and Problems in Cell Differentiation book series (RESULTS, volume 60)

Abstract

The Xenopus genus includes several members of aquatic frogs native to Africa but is perhaps best known for the species Xenopus laevis and Xenopus tropicalis. These species were popularized as model organisms from as early as the 1800s and have been instrumental in expanding several biological fields including cell biology, environmental toxicology, regenerative biology, and developmental biology. In fact, much of what we know about the formation and maturation of the vertebrate renal system has been acquired by examining the intricate genetic and morphological patterns that epitomize nephrogenesis in Xenopus. From these numerous reports, we have learned that the process of kidney development is as unique among organs as it is conserved among vertebrates. While development of most organs involves increases in size at a single location, development of the kidney occurs through a series of three increasingly complex nephric structures that are temporally distinct from one another and which occupy discrete spatial locales within the body. These three renal systems all serve to provide homeostatic, osmoregulatory, and excretory functions in animals. Importantly, the kidneys in amphibians, such as Xenopus, are less complex and more easily accessed than those in mammals, and thus tadpoles and frogs provide useful models for understanding our own kidney development. Several descriptive and mechanistic studies conducted with the Xenopus model system have allowed us to elucidate the cellular and molecular mediators of renal patterning and have also laid the foundation for our current understanding of kidney repair mechanisms in vertebrates. While some species-specific responses to renal injury have been observed, we still recognize the advantage of the Xenopus system due to its distinctive similarity to mammalian wound healing, reparative, and regenerative responses. In addition, the first evidence of renal regeneration in an amphibian system was recently demonstrated in Xenopus laevis. As genetic and molecular tools continue to advance, our appreciation for and utilization of this amphibian model organism can only intensify and will certainly provide ample opportunities to further our understanding of renal development and repair.

References

  1. Armstrong PB (1932) The embryonic origin of function in the pronephros through differentiation and parenchyma-vascular association. Am J Anat 51:157–188CrossRefGoogle Scholar
  2. Aronson PS (1989) The renal proximal tubule: a model for diversity of anion exchangers and stilbene-sensitive anion transporters. Annu Rev Physiol 51:419–441PubMedCrossRefGoogle Scholar
  3. Attia L, Yelin R, Schultheiss TM (2012) Analysis of nephric duct specification in the avian embryo. Development 139:4143–4151PubMedPubMedCentralCrossRefGoogle Scholar
  4. Augusto J, Smith B, Smith S, Robertson J, Reimschuessel R (1996) Gentamicin-induced nephrotoxicity and nephroneogenesis in Oreochromis nilotica, a tilapian fish. Dis Aquat Org 26:49–58CrossRefGoogle Scholar
  5. Babaeva AG (1964) Regeneration of the kidney in the red-bellied toad (Bombina bombina). Bull Exp Biol Med 57:99–103CrossRefGoogle Scholar
  6. Balinsky JB, Baldwin E (1961) The mode of excretion of ammonia and urea in Xenopus laevis. J Exp Biol 38:695–705Google Scholar
  7. Barch SH, Shaver JR, Wilson GB (1966) An electron microscopic study of the nephric unit in the frog. Trans Am Microsc Soc 85:350–359PubMedCrossRefGoogle Scholar
  8. Barker N, De Wetering MV, Clevers H (2008) The intestinal stem cell. Genes Dev 22:1856–1864PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beck CW, Christen B, Slack JMW (2003) Molecular pathways needed for regeneration of spinal cord and muscle in a vertebrate. Dev Cell 5:429–439PubMedCrossRefGoogle Scholar
  10. Beck CW, Izpisúa Belmont JC, Christen B (2009) Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms. Dev Dyn 238:1226–1248PubMedCrossRefGoogle Scholar
  11. Becker JL, Miller F, Nuovo GJ, Josepovitz C, Schubach WH, Nord EP (1999) Epstein-Barr virus infection of renal proximal tubule cells: possible role in chronic interstitial nephritis. J Clin Invest 104:1673–1681PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bengatta S, Arnould C, Letavernier E, Monge M, De Préneuf HM, Werb Z, Ronco P, Lelongt B (2009) MMP9 and SCF protect from apoptosis in acute kidney injury. J Am Soc Nephrol 20:787–797PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bernardini S, Gargioli C, Cannata SM, Filoni S (2010) Neurogenesis during optic tectum regeneration in Xenopus laevis. Develop Growth Differ 52:365–376CrossRefGoogle Scholar
  14. Bertolotti E, Malagoli D, Franchini A (2013) Skin wound healing in different aged Xenopus laevis. J Morphol 274:956–964PubMedCrossRefGoogle Scholar
  15. Bettencourt-Dias M, Mittnacht S, Brockes JP (2003) Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J Cell Sci 116:4001–4009PubMedCrossRefGoogle Scholar
  16. Birnbaum KD, Sánchez Alvarado A (2008) Slicing across kingdoms: regeneration in plants and animals. Cell 132:697–710PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bode HR (2003) Head regeneration in hydra. Dev Dyn 226:225–236PubMedCrossRefGoogle Scholar
  18. Bonasio R (2015) The expanding epigenetic landscape of non-model organisms. J Exp Biol 218:114–122PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bonventre JV (2003) Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 14:S55–S61PubMedCrossRefGoogle Scholar
  20. Boti Z, Kobor J, Ormos J (1982) Activity of glucose-6-phosphatase in regenerating tubular epithelium in rat kidney after necrosis induced with mercuric chloride: A light and electronmicroscopical study. Br J Exp Pathol 63:615–624PubMedPubMedCentralGoogle Scholar
  21. Brändli AW (1999) Towards a molecular anatomy of the Xenopus pronephric kidney. Int J Dev Biol 43:381–395PubMedGoogle Scholar
  22. Bremer JL (1916) The interrelations of the mesonephros, kidney and placenta in different classes of animals. Am J Anat 19:179–209CrossRefGoogle Scholar
  23. Brennan HC, Nijjar S, Jones EA (1998) The specification of the pronephric tubules and duct in Xenopus laevis. Mech Dev 75:127–137PubMedCrossRefGoogle Scholar
  24. Brockes JP, Kumar A (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev Mol Cell Biol 3:566–574PubMedCrossRefGoogle Scholar
  25. Bryant PJ (1971) Regeneration and duplication following operations in situ on the imaginal discs of Drosophila melanogaster. Dev Biol 26:637–651PubMedCrossRefGoogle Scholar
  26. Caine ST, McLaughlin KA (2013) Regeneration of functional pronephric proximal tubules after partial nephrectomy in Xenopus laevis. Dev Dyn 242:219–229PubMedCrossRefGoogle Scholar
  27. Carinato ME, Walter BE, Henry JJ (2000) Xenopus laevis gelatinase B (Xmmp-9): development, regeneration, and wound healing. Dev Dyn 217:377–387PubMedCrossRefGoogle Scholar
  28. Carlson BM (1978) Types of morphogenetic phenomena in vertebrate regenerating systems. Integr Comp Biol 18:869–882Google Scholar
  29. Carnevali MD, Bonasoro F, Lucca E, Thorndyke MC (1995) Pattern of cell proliferation in the early stages of arm regeneration in the feather star Antedon mediterranea. J Exp Zool 272:464–474CrossRefGoogle Scholar
  30. Carroll TJ, Vize PD (1999) Synergism between Pax-8 and lim-1 in embryonic kidney development. Dev Biol 214:46–59PubMedCrossRefGoogle Scholar
  31. Carroll T, Wallingford J, Seufert D, Vize PD (1999a) Molecular regulation of pronephric development. Curr Top Dev Biol 44:67–100PubMedCrossRefGoogle Scholar
  32. Carroll TJ, Wallingford JB, Vize PD (1999b) Dynamic patterns of gene expression in the developing pronephros of Xenopus laevis. Dev Genet 24:199–207PubMedCrossRefGoogle Scholar
  33. Chan TC, Takahashi S, Asashima M (2000) A role for Xlim-1 in pronephros development in Xenopus laevis. Dev Biol 228:256–269PubMedCrossRefGoogle Scholar
  34. Chopra DP, Simnett JD (1969) Changes in mitotic rate during compensatory renal growth in Xenopus laevis tadpoles after unilateral pronephrectomy. J Embryol Exp Morphol 21:539–548PubMedGoogle Scholar
  35. Chopra DP, Simnett JD (1970) Stimulation of cell division in pronephros of embryonic grafts following partial nephrectomy in the host (Xenopus laevis). J Embryol Exp Morphol 24:525–533PubMedGoogle Scholar
  36. Chopra DP, Simnett JD (1971) Stimulation of cell division in larval kidney (Xenopus laevis) by rat kidney antiserum. Exp Cell Res 64:396–402PubMedCrossRefGoogle Scholar
  37. Christen B, Beck CW, Lombardo A, Slack JMW (2003) Regeneration-specific expression pattern of three posterior hox genes. Dev Dyn 226:349–355PubMedCrossRefGoogle Scholar
  38. Christensen EI, Raciti D, Reggiani L, Verroust PJ, Brändli AW (2008) Gene expression analysis defines the proximal tubule as the compartment for endocytic receptor-mediated uptake in the Xenopus pronephric kidney. Pflugers Arch - Eur J Physiol 456:1163–1176CrossRefGoogle Scholar
  39. Chromek M, Tullus K, Hertting O, Jaremko G, Khalil A, Li Y, Brauner A (2003) Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinases-1 in acute pyelonephritis and renal scarring. Pediatr Res 53:698–705PubMedCrossRefGoogle Scholar
  40. Cirio MC, Hui Z, Haldin CE, Cosentino CC, Stuckenholz C, Chen X, Hong S, Dawid IB, Hukriede NA (2011) Lhx1 is required for specification of the renal progenitor cell field. PLoS One 6:e18858PubMedPubMedCentralCrossRefGoogle Scholar
  41. Cuppage FE, Tate A (1967) Repair of the nephron following injury with mercuric chloride. Am J Pathol 51:405–429PubMedPubMedCentralGoogle Scholar
  42. Cuppage FE, Chiga M, Tate A (1972) Cell cycle studies in the regenerating rat nephron following injury with mercuric chloride. Lab Investig 26:122–126PubMedGoogle Scholar
  43. Davidson AJ (2011) Uncharted waters: nephrogenesis and renal regeneration in fish and mammals. Pediatr Nephrol 26:1435–1443PubMedCrossRefGoogle Scholar
  44. Davies JA, Fisher CE (2002) Genes and proteins in renal development. Exp Nephrol 10:102–113PubMedCrossRefGoogle Scholar
  45. Dent JN (1962) Limb regeneration in larvae and metamorphosing individuals of the South African clawed toad. J Morphol 110:61–77PubMedCrossRefGoogle Scholar
  46. Diep CQ, Ma D, Deo RC, Holm TM, Naylor RW, Arora N, Wingert RA, Bollig F, Djordjevic G, Lichman B, Zhu H, Ikenaga T, Ono F, Englert C, Cowan CA, Hukriede NA, Handin RI, Davidson AJ (2011) Identification of adult nephron progenitors capable of kidney regeneration in zebrafish. Nature 470:95–101PubMedPubMedCentralCrossRefGoogle Scholar
  47. Dor Y, Stanger BZ (2007) Regeneration in liver and pancreas: time to cut the umbilical cord? Sci STKE 414:pe66Google Scholar
  48. Drawbridge J, Meighan CM, Lumpkins R, Kite ME (2003) Pronephric duct extension in amphibian embryos: migration and other mechanisms. Dev Dyn 226:1–11PubMedCrossRefGoogle Scholar
  49. Dressler GR (1996) Pax-2, kidney development, and oncogenesis. Med Pediatr Oncol 27:440–444PubMedCrossRefGoogle Scholar
  50. Dressler GR (2006) The cellular basis of kidney development. Annu Rev Cell Dev Biol 22:509–529PubMedCrossRefGoogle Scholar
  51. Drummond IA (2000) The zebrafish pronephros: a genetic system for studies of kidney development. Pediatr Nephrol 14:428–435PubMedCrossRefGoogle Scholar
  52. Drummond IA, Davidson AJ (2010) Zebrafish kidney development. Methods Cell Biol 100:233–260PubMedCrossRefGoogle Scholar
  53. Drummond IA, Majumdar A (2003) The pronephric glomus and vasculature. In: Vize PD, Woolf AS, Bard JBL (eds) The kidney: from normal development to congenital disease. Elsevier Science, San Diego, p 61CrossRefGoogle Scholar
  54. Drummond IA, Majumdar A, Hentschel H, Elger M, Solnica-Krezel L, Schier AF, Neuhauss SCF, Stemple DL, Zwartkruis F, Rangini Z, Driever W, Fishman MC (1998) Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125:4655–4667PubMedGoogle Scholar
  55. Du Pasquier L, Schwager J, Flajnik MF (1989) The immune system of Xenopus. Annu Rev Immunol 7:251–275PubMedCrossRefGoogle Scholar
  56. Eid SR, Brändli AW (2001) Xenopus Na, K-ATPase: primary sequence of the β2 subunit and in situ localization of α1, β1, and γ expression during pronephric kidney development. Differentiation 68:115–125PubMedCrossRefGoogle Scholar
  57. Elger M, Hentschel H, Litteral J, Wellner M, Kirsch T, Luft FC, Haller H (2003) Nephrogenesis is induced by partial nephrectomy in the elasmobranch Leucoraja erinacea. J Am Soc Nephrol 14:1506–1518PubMedCrossRefGoogle Scholar
  58. Ellis LC, Youson JH (1989) Ultrastructure of the pronephric kidney in upstream migrant sea lamprey, Petromyzon marinus L. Am J Anat 185:429–443PubMedCrossRefGoogle Scholar
  59. Endo T, Yokoyama H, Tamura K, Ide H (1997) Shh expression in developing and regenerating limb buds of Xenopus laevis. Dev Dyn 209:227–232PubMedCrossRefGoogle Scholar
  60. Endo T, Tamura K, Ide H (2000) Analysis of gene expressions during Xenopus forelimb regeneration. Dev Biol 220:296–306PubMedCrossRefGoogle Scholar
  61. Endo T, Yoshino J, Kado K, Tochinai S (2007) Brain regeneration in anuran amphibians. Develop Growth Differ 49:121–129CrossRefGoogle Scholar
  62. Fedorova S, Miyamoto R, Harada T, Isogai S, Hashimoto H, Ozato K, Wakamatsu Y (2008) Renal glomerulogenesis in medaka fish, Oryzias latipes. Dev Dyn 237:2342–2352PubMedCrossRefGoogle Scholar
  63. Ferretti P, Brockes JP, Brown R (1991) A newt type II keratin restricted to normal and regenerating limbs and tails is responsive to retinoic acid. Development 111:497–507PubMedGoogle Scholar
  64. Flajnik MF, Du Pasquier L (2004) Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol 25:640–644PubMedCrossRefGoogle Scholar
  65. Flink IL (2002) Cell cycle reentry of ventricular and atrial cardiomyocytes and cells within the epicardium following amputation of the ventricular apex in the axolotl, Amblystoma mexicanum: confocal microscopic immunofluorescent image analysis of bromodeoxyuridine-labeled nuclei. Anat Embryol 205:235–244PubMedCrossRefGoogle Scholar
  66. Fox H (1963) The amphibian pronephros. Q Rev Biol 38:1–25PubMedCrossRefGoogle Scholar
  67. French V, Domican J (1982) The regeneration of supernumerary cockroach antennae. J Embryol Exp Morphol 67:153–165Google Scholar
  68. Frontera JL, Cervino AS, Jungblut LD, Paz DA (2015) Brain-derived neurotrophic factor (BDNF) expression in normal and regenerating olfactory epithelium of Xenopus laevis. Ann Anat 198:41–48PubMedCrossRefGoogle Scholar
  69. Fukazawa T, Naora Y, Kunieda T, Kubo T (2009) Suppression of the immune response potentiates tadpole tail regeneration during the refractory period. Development 136:2323–2327PubMedCrossRefGoogle Scholar
  70. Fukui L, Henry JJ (2011) FGF signaling is required for lens regeneration in Xenopus laevis. Biol Bull 221:137–145PubMedPubMedCentralCrossRefGoogle Scholar
  71. Gardiner DM, Carlson MRJ, Roy S (1999) Towards a functional analysis of limb regeneration. Semin Cell Dev Biol 10:385–393PubMedCrossRefGoogle Scholar
  72. Gargioli C, Slack JMW (2004) Cell lineage tracing during Xenopus tail regeneration. Development 131:2669–2679PubMedCrossRefGoogle Scholar
  73. Ghosh S, Thorogood P, Ferretti P (1996) Regeneration of lower and upper jaws in urodeles is differentially affected by retinoic acid. Int J Dev Biol 40:1161–1170PubMedGoogle Scholar
  74. Gobé GC, Buttyan R (2002) Apoptosis in the pathogenesis of renal disease with a focus on tubulointerstitial injury. Nephrology 7:287–293CrossRefGoogle Scholar
  75. Gobé GC, Buttyan R, Wyburn KRL, Etheridge MR, Smith PJ (1995) Clusterin expression and apoptosis in tissue remodeling associated with renal regeneration. Kidney Int 47:411–420PubMedCrossRefGoogle Scholar
  76. Godwin JW, Rosenthal N (2014) Scar-free wound healing and regeneration in amphibians: Immunological influences on regenerative success. Differentiation 87:66–75PubMedCrossRefGoogle Scholar
  77. Goldin G, Fabian B (1978) The regulation of growth in the mesonephric kidney of adult Xenopus laevis by an endogenous inhibitor of proliferation. Dev Biol 66:529–538PubMedCrossRefGoogle Scholar
  78. González-Avila G, Iturria C, Vadillo-Ortega F, Ovalle C, Montaño M (1998) Changes in matrix metalloproteinases during the evolution of interstitial renal fibrosis in a rat experimental model. Pathobiology 66:196–204PubMedCrossRefGoogle Scholar
  79. Goyos A, Robert J (2009) Tumorigenesis and anti-tumor immune responses in Xenopus. Front Biosci 14:167–176CrossRefGoogle Scholar
  80. Graver HT (1978) Re-regeneration of lower jaws and the dental lamina in adult urodeles. J Morphol 157:269–276PubMedCrossRefGoogle Scholar
  81. Grow M, Neff AW, Mescher AL, King MW (2006) Global analysis of gene expression in Xenopus hindlimbs during stage-dependent complete and incomplete regeneration. Dev Dyn 235:2667–2685PubMedCrossRefGoogle Scholar
  82. Hamilton PW, Sun Y, Henry JJ (2016) Lens regeneration from the cornea requires suppression of Wnt/β-catenin signaling. Exp Eye Res 145:206–215PubMedPubMedCentralCrossRefGoogle Scholar
  83. Harty M, Neff AW, King MW, Mescher AL (2003) Regeneration or scarring: an immunologic perspective. Dev Dyn 226:268–279PubMedCrossRefGoogle Scholar
  84. Hayashi S, Kawaguchi A, Uchiyama I, Kawasumi-Kita A, Kobayashi T, Nishide H, Tsutsumi R, Tsuru K, Inoue T, Ogino H, Agata K, Tamura K, Yokoyama H (2015) Epigenetic modification maintains intrinsic limb-cell identity in Xenopus limb bud regeneration. Dev Biol 406:271–282PubMedCrossRefGoogle Scholar
  85. Heller N, Brändli AW (1997) Xenopus Pax-2 displays multiple splice forms during embryogenesis and pronephric kidney development. Mech Dev 69:83–104PubMedCrossRefGoogle Scholar
  86. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak L, 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 328:633–636PubMedPubMedCentralCrossRefGoogle Scholar
  87. Hensey C, Dolan V, Brady HR (2002) The Xenopus pronephros as a model system for the study of kidney development and pathophysiology. Nephrol Dial Transplant 17:73–74PubMedCrossRefGoogle Scholar
  88. Hewitt IK, Zucchetta P, Rigon L, Maschio F, Molinari PP, Tomasi L, Toffolo A, Pavanello L, Crivellaro C, Bellato S, Montini G (2008) Early treatment of acute pyelonephritis in children fails to reduce renal scarring: data from the Italian renal infection study trials. Pediatrics 122:486–490PubMedCrossRefGoogle Scholar
  89. Howland RB (1916) On the effect of removal of the pronephros of the amphibian embryo. Proc Natl Acad Sci USA 2:231–234PubMedPubMedCentralCrossRefGoogle Scholar
  90. Huang C, Ogawa R (2010) Mechanotransduction in bone repair and regeneration. FASEB J 24:3625–3632PubMedCrossRefGoogle Scholar
  91. Huang Y, Chen M, Chiu N, Chou H, Lin K, Chiou Y (2011) Adjunctive oral methylprednisolone in pediatric acute pyelonephritis alleviates renal scarring. Pediatrics 128:e496–e504PubMedCrossRefGoogle Scholar
  92. Humphreys BD, Duffield JS, Bonventre JV (2006) Renal stem cells in recovery from acute kidney injury. Minerva Urol Nefrol 58:329–337PubMedGoogle Scholar
  93. Humphreys BD, Valerius MT, Kobayashi A, Mugford JW, Soeung S, Duffield JS, McMahon AP, Bonventre JV (2008) Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2:284–291PubMedCrossRefGoogle Scholar
  94. Imgrund M, Gröne E, Gröne H, Kretzler M, Holzman L, Schlöndorff D, Rothenpieler UW (1999) Re-expression of the developmental gene pax-2 during experimental acute tubular necrosis in mice. Kidney Int 56:1423–1431PubMedCrossRefGoogle Scholar
  95. Imokawa Y, Brockes JP (2003) Selective activation of thrombin is a critical determinant for vertebrate lens regeneration. Curr Biol 13:877–881PubMedCrossRefGoogle Scholar
  96. Ingber DE, Levin M (2007) What lies at the interface of regenerative medicine and development? Development 134:2541–2547PubMedCrossRefGoogle Scholar
  97. Ishizuya-Oka A (2007) Regeneration of the amphibian intestinal epithelium under the control of stem cell niche. Develop Growth Differ 49:99–107CrossRefGoogle Scholar
  98. Jaffee OC (1954) Morphogenesis of the pronephros of the leopard frog (Rana pipiens). J Morphol 95:109–123CrossRefGoogle Scholar
  99. Jaffee OC (1963) Cellular differentiation in the anuran pronephros. Anat Rec 145:179–182PubMedCrossRefGoogle Scholar
  100. Jewhurst K, Levin M, McLaughlin KA (2014) Optogenetic control of apoptosis in targeted tissues of Xenopus laevis embryos. J Cell Death 13:25–31Google Scholar
  101. Jones EA (2005) Xenopus: A prince among models for pronephric kidney development. J Am Soc Nephrol 16:313–321PubMedCrossRefGoogle Scholar
  102. Kardong KV (ed) (2014) Vertebrates: comparative anatomy, function, evolution, 7th edn. McGraw Hill Higher Education, Boston, 816 pGoogle Scholar
  103. Kays SE, Schnellmann RG (1995) Regeneration of renal proximal tubule cells in primary culture following toxicant injury: response to growth factors. Toxicol Appl Pharmacol 132:273–280PubMedCrossRefGoogle Scholar
  104. King MW, Nguyen T, Calley J, Harty MW, Muzinich MC, Mescher AL, Chalfant C, N’Cho M, McLeaster K, McEntire J, Stocum D, Smith RC, Neff AW (2003) Identification of genes expressed during Xenopus laevis limb regeneration by using subtractive hybridization. Dev Dyn 226:398–409PubMedCrossRefGoogle Scholar
  105. Kingsley JS (ed) (1917) Outlines of comparative anatomy of vertebrates, 2nd edn. Revised. P. Blakiston Son’s, Philadelphia, 449 pGoogle Scholar
  106. Kispert A, Vainio S, McMahon AP (1998) Wnt-4 is a mesenchymal signal for epithelial transformation of metanephric mesenchyme in the developing kidney. Development 125:4225–4234PubMedGoogle Scholar
  107. Kobayashi C, Watanabe K, Agata K (1999) The process of pharynx regeneration in planarians. Dev Biol 211:27–38PubMedCrossRefGoogle Scholar
  108. Kobayashi A, Kwan KM, Carroll TJ, McMahon AP, Mendelsohn CL, Behringer RR (2005) Distinct and sequential tissue-specific activities of the LIM-class homeobox gene Lim1 for tubular morphogenesis during kidney development. Development 132:2809–2823PubMedCrossRefGoogle Scholar
  109. Kovacs CJ, Braunschweiger PG, Schenken LL, Burholt DR (1982) Proliferative defects in renal and intestinal epithelium after cis-dichlorodiammine platinum (II). Br J Cancer 45:286–294PubMedPubMedCentralCrossRefGoogle Scholar
  110. Kunugi S, Shimizu A, Kuwahara N, Du X, Takahashi M, Terasaki Y, Fujita E, Mii A, Nagasaka S, Akimoto T, Masuda Y, Fukuda Y (2011) Inhibition of matrix metalloproteinases reduces ischemia-reperfusion acute kidney injury. Lab Investig 91:170–180PubMedCrossRefGoogle Scholar
  111. Kuure S, Vuolteenaho R, Vainio S (2000) Kidney morphogenesis: cellular and molecular regulation. Mech Dev 92:31–45PubMedCrossRefGoogle Scholar
  112. Lee DC, Hamm LM, Moritz OL (2013) Xenopus laevis tadpoles can regenerate neural retina lost after physical excision but cannot regenerate photoreceptors lost through targeted ablation. Invest Ophthalmol Vis Sci 54:1859–1867PubMedCrossRefGoogle Scholar
  113. Legallicier B, Trugnan G, Murphy G, Lelongt B, Ronco P, Delauche M, Fontanges P (2001) Expression of the type IV collagenase system during mouse kidney development and tubule segmentation. J Am Soc Nephrol 12:2358–2369PubMedGoogle Scholar
  114. Lei Y, Guo X, Liu Y, Cao Y, Deng Y, Chen X, Cheng CH, Dawid IB, Chen Y, Zhao H (2012) Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci USA 109:17484–17489PubMedPubMedCentralCrossRefGoogle Scholar
  115. Lelongt B, Ronco P (2003) Role of extracellular matrix in kidney development and repair. Pediatr Nephrol 18:731–742PubMedCrossRefGoogle Scholar
  116. Lelongt B, Bengatta S, Delauche M, Lund LR, Werb Z, Ronco PM (2001a) Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity. J Exp Med 193:793–802PubMedPubMedCentralCrossRefGoogle Scholar
  117. Lelongt B, Legallicier B, Piedagnel R, Ronco PM (2001b) Do matrix metalloproteinases MMP-2 and MMP-9 (gelatinases) play a role in renal development, physiology and glomerular diseases? Curr Opin Nephrol Hypertens 10:7–12PubMedCrossRefGoogle Scholar
  118. Lévesque M, Guimond J, Pilote M, Leclerc S, Moldovan F, Roy S (2005) Expression of heat-shock protein 70 during limb development and regeneration in the axolotl. Dev Dyn 233:1525–1534PubMedCrossRefGoogle Scholar
  119. Lienkamp SS (2016) Using Xenopus to study genetic kidney diseases. Semin Cell Dev Biol S1084-9521:30045–30043Google Scholar
  120. Lienkamp SS, Liu K, Karner CM, Carroll TJ, Ronneberger O, Wallingford JB, Walz G (2012) Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat Genet 44:1382–1387PubMedPubMedCentralCrossRefGoogle Scholar
  121. Lipschutz JH (1998) Molecular development of the kidney: a review of the results of gene disruption studies. Am J Kidney Dis 31:383–397PubMedCrossRefGoogle Scholar
  122. Liu Y (2011) Cellular and molecular mechanisms of renal fibrosis. Nat Rev Nephrol 7:684–696PubMedPubMedCentralCrossRefGoogle Scholar
  123. Liu M, Reimschuessel R, Hassel BA (2002) Molecular cloning of the fish interferon stimulated gene, 15 kDa (ISG15) orthologue: a ubiquitin-like gene induced by nephrotoxic damage. Gene 298:129–139PubMedCrossRefGoogle Scholar
  124. Liu W, Tang N, Zhang Q (2009) Could mycophenolate mofetil combined with benazapril delay tubulointerstitial fibrosis in 5/6 nephrectomized rats? Chin Med J 122:199–204PubMedGoogle Scholar
  125. Liu Y, Zhao H, Cheng CH (2016) Mutagenesis in Xenopus and Zebrafish using TALENs. Methods Mol Biol 1338:207–227PubMedCrossRefGoogle Scholar
  126. Love NR, Chen Y, Ishibashi S, Kritsiligkou P, Lea R, Koh Y, Gallop JL, Dorey K, Amaya E (2013) Amputation-induced reactive oxygen species are required for successful Xenopus tadpole tail regeneration. Nat Cell Biol 15:222–228PubMedPubMedCentralCrossRefGoogle Scholar
  127. Malloch EL, Perry KJ, Fukui L, Johnson VR, Wever J, Beck CW, King MW, Henry JJ (2009) Gene expression profiles of lens regeneration and development in Xenopus laevis. Dev Dyn 238:2340–2356PubMedPubMedCentralCrossRefGoogle Scholar
  128. Mantur M, Kemona H, Dabrowska M, Dabrowska J, Sobolewski S, Prokopowicz J (2000) α1-microglobulin as a marker of proximal tubular damage in urinary tract infection in children. Clin Nephrol 53:283–287PubMedGoogle Scholar
  129. Martin P (1997) Wound healing – aiming for perfect skin regeneration. Science 276:75–81PubMedCrossRefGoogle Scholar
  130. Maunsbach AB, Christensen EI (1992) Functional ultrastructure of the proximal tubule. Compr Physiol (Online, 2011). Supplement 25: Handbook of Physiology, Renal Physiol 41–107Google Scholar
  131. McCampbell KK, Springer KN, Wingert RA (2015) Atlas of cellular dynamics during zebrafish adult kidney regeneration. Stem Cells Int 547636Google Scholar
  132. McMillan JI, Riordan JW, Couser WG, Pollock AS, Lovett DH (1996) Characterization of a glomerular epithelial cell metalloproteinase as matrix metalloproteinase-9 with enhanced expression in a model of membranous nephropathy. J Clin Invest 97:1094–1101PubMedPubMedCentralCrossRefGoogle Scholar
  133. Menè P, Polci R, Festuccia F (2003) Mechanisms of repair after kidney injury. J Nephrol 16:186–195PubMedGoogle Scholar
  134. Menger B, Vogt PM, Kuhbier JW, Reimers K (2010) Applying amphibian limb regeneration to human wound healing: a review. Ann Plast Surg 65:504–510PubMedCrossRefGoogle Scholar
  135. Mescher AL (1996) The cellular basis of limb regeneration in urodeles. Int J Dev Biol 40:785–795PubMedGoogle Scholar
  136. Mescher AL, Neff AW (2004) Loss of regenerative capacity: a trade-off for immune specificity? Cell Sci Rev 1:1–10Google Scholar
  137. Mescher AL, Wolf WL, Moseman EA, Hartman B, Harrison C, Nguyen E, Neff AW (2007) Cells of cutaneous immunity in Xenopus: studies during larval development and limb regeneration. Dev Comp Immunol 31:383–393PubMedCrossRefGoogle Scholar
  138. Mescher AL, Neff AW, King MW (2013) Changes in the inflammatory response to injury and its resolution during the loss of regenerative capacity in developing Xenopus limbs. PLoS One 8:e80477PubMedPubMedCentralCrossRefGoogle Scholar
  139. Mito T, Inoue Y, Kimura S, Miyawaki K, Niwa N, Shinmyo Y, Ohuchi H, Noji S (2002) Involvement of hedgehog, wingless, and dpp in the initiation of proximodistal axis formation during the regeneration of insect legs, a verification of the modified boundary model. Mech Dev 114:27–35PubMedCrossRefGoogle Scholar
  140. Møbjerg N, Larsen EH, Jespersen Å (2000) Morphology of the kidney in larvae of Bufo viridis (Amphibia, Anura, Bufonidae). J Morphol 245:177–195PubMedCrossRefGoogle Scholar
  141. Mochii M, Taniguchi Y, Shikata I (2007) Tail regeneration in the Xenopus tadpole. Dev Growth Differ 49:155–161PubMedCrossRefGoogle Scholar
  142. Mondia JP, Levin M, Omenetto FG, Orendorff RD, Branch MR, Adams DS (2011) Long-distance signals are required for morphogenesis of the regenerating Xenopus tadpole tail. PLoS One 6:e24953 PubMedPubMedCentralCrossRefGoogle Scholar
  143. Monks SP (1903) Regeneration of the body of a starfish. Proc Acad Natl Sci Phila 55:351Google Scholar
  144. Monks SP (1904) Variability and autotomy of Phataria. Proc Acad Natl Sci Phila 56:596–600Google Scholar
  145. Moritz KM, Wintour EM (1999) Functional development of the meso- and metanephros. Pediatr Nephrol 13:171–178PubMedCrossRefGoogle Scholar
  146. Moshiri A, Close J, Reh TA (2004) Retinal stem cells and regeneration. Int J Dev Biol 48:1003–1014PubMedCrossRefGoogle Scholar
  147. Muneoka K, Holler-Dinsmore G, Bryant SV (1986) Intrinsic control of regenerative loss in Xenopus laevis limbs. J Exp Zool 240:47–54PubMedCrossRefGoogle Scholar
  148. Muñoz R, Edwards-Faret G, Moreno M, Zuñiga N, Cline H, Larraín J (2015) Regeneration of Xenopus laevis spinal cord requires Sox2/3 expressing cells. Dev Biol 408:229–243PubMedPubMedCentralCrossRefGoogle Scholar
  149. Nadake S, Sakuma T, Sakane Y, Hara Y, Kurabayashi A, Kashiwago K, Yamamoto T, Obara M (2015) Homeolog-specific targeted mutagenesis in Xenopus using TALENs. In Vitro Cell Dev Biol Anim 51:879–884Google Scholar
  150. Nadasdy T, Laszik Z, Blick KE, Johnson DL, Burst-Singer K, Nast C, Cohen AH, Ormos J, Silva FG (1995) Human acute tubular necrosis: a lectin and immunohistochemical study. Hum Pathol 26:230–239PubMedCrossRefGoogle Scholar
  151. Nedelkovska H, Edholm ES, Haynes N, Robert J (2013) Effective RNAi-mediated beta2-microglobulin loss of function by transgenesis in Xenopus laevis. Biol Open 2:335–342PubMedPubMedCentralCrossRefGoogle Scholar
  152. Nieuwkoop PD (1996) What are the key advantages and disadvantages of urodele species compared to anurans as a model system for experimental analysis of early development? Int J Biol 40:617–619Google Scholar
  153. Nieuwkoop PD, Faber J (eds) (1994) Normal table of Xenopus laevis (Daudin). Garland Publishing, New York, 252 pGoogle Scholar
  154. Noël A, Jost M, Maquoi E (2008) Matrix metalloproteinases at cancer tumor-host interface. Semin Cell Dev Biol 19:52–60PubMedCrossRefGoogle Scholar
  155. Nonclercq D, Wrona S, Toubeau G, Zanen J, Heuson-Stiennon J, Schaudies RP, Laurent G (1992) Tubular injury and regeneration in the rat kidney following acute exposure to gentamicin: a time-course study. Renal Fail 14:507–521CrossRefGoogle Scholar
  156. Nony PA, Schnellmann RG (2003) Mechanisms of renal cell repair and regeneration after acute renal failure. J Pharmacol Exp Ther 304:905–912PubMedCrossRefGoogle Scholar
  157. Nye HLD, Cameron JA, Chernoff EAG, Stocum DL (2003) Regeneration of the urodele limb: a review. Dev Dyn 226:280–294PubMedCrossRefGoogle Scholar
  158. O’Connor RJ (1940) The evolutionary significance of the embryology of the amphibian nephric system. J Anat 75:95–101PubMedPubMedCentralGoogle Scholar
  159. Panetta NJ, Gupta DM, Longaker MT (2010) Bone regeneration and repair. Curr Stem Cell Res Ther 5:122–128PubMedCrossRefGoogle Scholar
  160. Pole RJ, Qi BQ, Beasley SW (2002) Patterns of apoptosis during degeneration of the pronephros and mesonephros. J Urol 167:269–271PubMedCrossRefGoogle Scholar
  161. Poss KD, Keating MT, Nechiporuk A (2003) Tales of regeneration in zebrafish. Dev Dyn 226:202–210PubMedCrossRefGoogle Scholar
  162. Raciti D, Reggiani L, Geffers L, Jiang Q, Bacchion F, Subrizi AE, Clements D, Tindal C, Davidson DR, Kaissling B, Brändli AW (2008) Organization of the pronephric kidney revealed by large-scale gene expression mapping. Genome Biol 9:R84PubMedPubMedCentralCrossRefGoogle Scholar
  163. Raghow R (1994) The role of extracellular matrix in postinflammatory wound healing and fibrosis. FASEB J 8:823–831PubMedCrossRefGoogle Scholar
  164. Rahman MM, Tae HJ, Cho HS, Shin GW, Park BY (2015) Developmental expression analysis of Na, K-ATPase α subunits in Xenopus. Dev Genes Evol 225:105–111PubMedCrossRefGoogle Scholar
  165. Reimschuessel R (2001) A fish model of renal regeneration and development. ILAR J 42:285–291PubMedCrossRefGoogle Scholar
  166. Reimschuessel R, Williams D (1995) Development of new nephrons in adult kidneys following gentamicin-induced nephrotoxicity. Ren Fail 17:101–106PubMedCrossRefGoogle Scholar
  167. Robert J, Cohen N (1998) Evolution of immune surveillance and tumor immunity: studies in Xenopus. Immunol Rev 166:231–243PubMedCrossRefGoogle Scholar
  168. Robert J, Cohen N (2011) The genus Xenopus as a multispecies model for evolutionary and comparative immunobiology of the 21st century. Dev Comp Immunol 35:916–923PubMedPubMedCentralCrossRefGoogle Scholar
  169. Robert J, Ohta Y (2009) Comparative and developmental study of the immune system in Xenopus. Dev Dyn 238:1249–1270PubMedPubMedCentralCrossRefGoogle Scholar
  170. Sakaguchi DS, Janick LM, Reh TA (1997) Basic fibroblast growth factor (FGF-2) induced transdifferentiation of retinal pigment epithelium: generation of retinal neurons and glia. Dev Dyn 209:387–398PubMedCrossRefGoogle Scholar
  171. Salice CJ, Rokous JS, Kane AS, Reimschuessel R (2001) New nephron development in goldfish (Carassius auratus) kidneys following repeated gentamicin-induced nephrotoxicosis. Comp Med 51:56–59PubMedGoogle Scholar
  172. Sánchez Alvarado A (2000) Regeneration in the metazoans: why does it happen? BioEssays 22:578–590PubMedCrossRefGoogle Scholar
  173. Sánchez Alvarado A (2004) Regeneration and the needs for simpler model organisms. Philos Trans R Soc Lond Ser B Biol Sci 359:759–763CrossRefGoogle Scholar
  174. Sánchez Alvarado A, Tsonis PA (2006) Bridging the regeneration gap: genetic insights from diverse animal models. Nat Rev Genet 7:873–884PubMedCrossRefGoogle Scholar
  175. Sato A, Asashima M, Yokota T, Nishinakamura R (2000) Cloning and expression pattern of a Xenopus pronephros-specific gene, XSMP-30. Mech Dev 92:273–275PubMedCrossRefGoogle Scholar
  176. Saulnier DME, Ghanbari H, Brändli AW (2002) Essential function of Wnt-4 for tubulogenesis in the Xenopus pronephric kidney. Dev Biol 248:13–28PubMedCrossRefGoogle Scholar
  177. Saxén L (1987) Organogenesis of the kidney. Cambridge University Press, Cambridge, 173 pCrossRefGoogle Scholar
  178. Scadding SR, Liversage RA (1974) Studies on the response of the adult newt kidney to partial nephrectomy. Am J Anat 140:349–368PubMedCrossRefGoogle Scholar
  179. Scimone ML, Srivastava M, Bell GW, Reddien PW (2011) A regulatory program for excretory system regeneration in planarians. Development 138:4387–4398PubMedPubMedCentralCrossRefGoogle Scholar
  180. Sheridan AM, Bonventre JV (2000) Cell biology and molecular mechanisms of injury in ischemic acute renal failure. Curr Opin Nephrol Hypertens 9:427–434PubMedCrossRefGoogle Scholar
  181. Simnett JD, Chopra DP (1969) Organ specific inhibitor of mitosis the amphibian kidney. Nature 222:1189–1190PubMedCrossRefGoogle Scholar
  182. Simon H, Nelson C, Goff D, Laufer E, Morgan BA, Tabin C (1995) Differential expression of myogenic regulatory genes and msx-1 during dedifferentiation and redifferentiation of regenerating amphibian limbs. Dev Dyn 202:1–12PubMedCrossRefGoogle Scholar
  183. Singer M (1951) Induction of regeneration of forelimb of the frog by augmentation of the nerve supply. Proc Soc Exp Biol Med 76:413–416PubMedCrossRefGoogle Scholar
  184. Slack JMW (2003) Regeneration research today. Dev Dyn 226:162–166PubMedCrossRefGoogle Scholar
  185. Slack JMW, Beck CW, Gargioli C, Christen B (2004) Cellular and molecular mechanisms of regeneration in Xenopus. Philos Trans R Soc Lond Ser B Biol Sci 359:745–751CrossRefGoogle Scholar
  186. Smith HW (1953) From fish to philosopher. Little, Brown, Boston, 304 pGoogle Scholar
  187. Smith SJ, Kotecha S, Towers N, Latinkic BV, Mohun TJ (2002) XPOX2-peroxidase expression and the XLURP-1 promoter reveal the site of embryonic myeloid cell development in Xenopus. Mech Dev 117:173–186PubMedCrossRefGoogle Scholar
  188. Stark K, Vainio S, Vassileva G, McMahon AP (1994) Epithelial transformation metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372:679–683PubMedCrossRefGoogle Scholar
  189. Stichel CC (1999) Inhibition of collagen IV deposition promotes regeneration of injured CMS axons. Eur J Neurosci 11:632–646PubMedCrossRefGoogle Scholar
  190. Stoick-Cooper CL, Moon RT, Weidinger G (2007) Advances in signaling in vertebrate regeneration as a prelude to regenerative medicine. Genes Dev 21:1292–1315PubMedCrossRefGoogle Scholar
  191. Sugiura T, Taniguchi Y, Tazaki A, Ueno N, Watanabe K, Mochii M (2004) Differential gene expression between the embryonic tail bud and regenerating larval tail in Xenopus laevis. Develop Growth Differ 46:97–105CrossRefGoogle Scholar
  192. Suzuki M, Yakushiji N, Nakada Y, Satoh A, Ide H, Tamura K (2006) Limb regeneration in Xenopus laevis froglet. Sci World J 6:26–37CrossRefGoogle Scholar
  193. Suzuki KT, Isoyama Y, Kashiwagi K, Sakuma T, Ochiai H, Sakamoto N, Furuno N, Kashiwagi A, Yamamoto T (2013) High efficiency TALENs enable F0 functional analysis by targeted gene disruption in Xenopus laevis embryos. Biol Open 2:448–452PubMedPubMedCentralCrossRefGoogle Scholar
  194. Swingle WW (1919) On the experimental production of edema by nephrectomy. J Genet Physiol 1:509–514CrossRefGoogle Scholar
  195. Taira M, Otani H, Jamrich M, Dawid IB (1994) Expression of the LIM class homeobox gene Xlim-1 in pronephros and CNS cell lineages of Xenopus embryos is affected by retinoic acid and exogastrulation. Development 120:1525–1536PubMedGoogle Scholar
  196. Tanaka E, Galliot B (2009) Triggering the regeneration and tissue repair programs. Development 136:349–353PubMedCrossRefGoogle Scholar
  197. Tanaka E, Reddien P (2011) The cellular basis for animal regeneration. Dev Cell 21:172–185PubMedPubMedCentralCrossRefGoogle Scholar
  198. Tandon P, Conlon F, Furlow JD, Horb ME (2016) Expanding the genetic toolkit in Xenopus: approaches and opportunities for human disease modeling. Dev Biol (in press). doi: 10.1016/j.ydbio.2016.04.009 CrossRefPubMedGoogle Scholar
  199. Tazaki A, Kitayama A, Terasaka C, Watanabe K, Ueno N, Mochii M (2005) Macroarray-based analysis of tail regeneration in Xenopus laevis larvae. Dev Dyn 233:1394–1404PubMedCrossRefGoogle Scholar
  200. Thorton CS, Shields TW (1945) Five cases of atypical regeneration in the adult frog. Am Soc Ichthyol Herpetol 1945:40–42Google Scholar
  201. Thouveny YR, Komorowski TE, Arsanto JP, Carlson BM (1991) Early innervation of skeletal muscle during tail regeneration in urodele amphibians. J Exp Zool 260:354–370PubMedCrossRefGoogle Scholar
  202. Tiedemann K, Wettstein R (1980) The mature mesonephric nephron of the rabbit embryo I. SEM studies. Cell Tissue Res 209:95–109PubMedCrossRefGoogle Scholar
  203. Tomlinson ML, Garcia-Morales C, Abu-Elmagd M, Wheeler GN (2008) Three matrix metalloproteinases are required in vivo for macrophage migration during embryonic development. Mech Dev 125:1059–1070PubMedCrossRefGoogle Scholar
  204. Tomlinson ML, Hendry AE, Wheeler GN (2012) Chemical genetics and drug discovery in Xenopus. Methods Mol Biol 917:155–166PubMedCrossRefGoogle Scholar
  205. Torok MA, Gardiner DM, Shubin NH, Bryant SV (1998) Expression of HoxD genes in developing and regenerating axolotl limbs. Dev Biol 200:225–233PubMedCrossRefGoogle Scholar
  206. Tseng AS, Levin M (2008) Tail regeneration in Xenopus laevis as a model for understanding tissue repair. J Dent Res 87:806–816PubMedCrossRefGoogle Scholar
  207. Tseng AS, Carneiro K, Lemire JM, Levin M (2011) HDAC activity is required during Xenopus tail regeneration. PLoS One 6:e26382PubMedPubMedCentralCrossRefGoogle Scholar
  208. Tsonis PA (2000) Regeneration in vertebrates. Dev Biol 221:273–284PubMedCrossRefGoogle Scholar
  209. Tsonis PA (2002) Regenerative biology: the emerging field of tissue repair and restoration. Differentiation 70:397–409PubMedCrossRefGoogle Scholar
  210. Venkatachalam MA, Bernard DB, Donohoe JF, Levinsky NG (1978) Ischemic damage and repair in the rat proximal tubule: differences among the S1, S2, and S3 segments. Kidney Int 14:31–49PubMedCrossRefGoogle Scholar
  211. Vize PD, Jones EA, Pfister R (1995) Development of the Xenopus pronephric system. Dev Biol 171:531–540PubMedCrossRefGoogle Scholar
  212. Vize PD, Seufert DW, Carroll TJ, Wallingford JB (1997) Model systems for the study of kidney development: use of the pronephros in the analysis of organ induction and patterning. Dev Biol 188:189–204PubMedCrossRefGoogle Scholar
  213. Vize PD, Carroll TJ, Wallingford JB (2003) Induction, development, and physiology of the pronephric tubules, pp 19–50. In: Vize PD, Woolf AS, JBL B (eds) The kidney: from normal development to congenital disease. Elsevier Science, California, p 519Google Scholar
  214. Wallin A, Zhang G, Jones TW, Jaken S, Stevens JL (1992) Mechanism of the nephrogenic repair response: Studies on proliferation and vimentin expression after 35S-1,2-dichlorovinyl-L-cysteine nephrotoxicity in vivo and in cultured proximal tubule epithelial cells. Lab Investig 66:474–484PubMedGoogle Scholar
  215. Wang X, Zhou Y, Tan R, Xiong M, He W, Fang L, Wen P, Jiang L, Yang J (2010) Mice lacking the matrix metalloproteinase-9 gene reduce renal interstitial fibrosis in obstructive nephropathy. Am J Physiol Renal Physiol 299:F973–F982PubMedCrossRefGoogle Scholar
  216. Wang F, Shi Z, Cui Y, Guo X, Shi YB, Chen Y (2015) Targeted gene disruption in Xenopus laevis using CRISPR/Cas 9. Cell Biosci 5:15PubMedPubMedCentralCrossRefGoogle Scholar
  217. Watanabe N, Kato M, Suzuki N, Inoue C, Fedorova S, Hashimoto H, Maruyama S, Matsuo S, Wakamatsu Y (2009) Kidney regeneration through nephron neogenesis in medaka. Develop Growth Differ 51:135–143CrossRefGoogle Scholar
  218. Wenemoser D, Lapan SW, Wilkinson AW, Bell GW, Reddien PW (2012) A molecular wound response program associated with regeneration initiation in planarians. Genes Dev 26:988–1002PubMedPubMedCentralCrossRefGoogle Scholar
  219. Wessely O, Tran U (2011) Xenopus pronephros development – past, present, and future. Pediatr Nephrol 26:1545–1551PubMedPubMedCentralCrossRefGoogle Scholar
  220. Wesson LG (1989) Compensatory growth and other growth responses of the kidney. Nephron 51:149–184PubMedCrossRefGoogle Scholar
  221. Wheeler GN, Brändli AW (2009) Simple vertebrate models for chemical genetics and drug discovery screens: lessons from zebrafish and Xenopus. Dev Dyn 238:1287–1308PubMedCrossRefGoogle Scholar
  222. Wheeler GN, Liu KJ (2012) Xenopus: An ideal system for chemical genetics. Genesis 50:207–218PubMedCrossRefGoogle Scholar
  223. Witzgall R, Brown D, Schwarz C, Bonventre JV (1994) Localization of proliferating cell nuclear antigen, vimentin, c-fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest 93:2175–2188PubMedPubMedCentralCrossRefGoogle Scholar
  224. Wrobel K, Süß F (2000) The significance of rudimentary nephrostomial tubules for the origin of the vertebrate gonad. Anat Embryol 201:273–290PubMedCrossRefGoogle Scholar
  225. Wynn TA (2008) Cellular and molecular mechanisms of fibrosis. J Pathol 214:199–210PubMedPubMedCentralCrossRefGoogle Scholar
  226. Wynn TA, Ramalingam TR (2012) Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18:1028–1040PubMedPubMedCentralCrossRefGoogle Scholar
  227. Yang EV, Gardiner DM, Carlson MRJ, Nugas CA, Bryant SV (1999) Expression of Mmp-9 and related matrix metalloproteinase genes during axolotl limb regeneration. Dev Dyn 216:2–9PubMedCrossRefGoogle Scholar
  228. Yang J, Shultz RW, Mars WM, Wegner RE, Li Y, Dai C, Nejak K, Liu Y (2002) Disruption of tissue-type plasminogen activator gene in mice reduces renal interstitial fibrosis in obstructive nephropathy. J Clin Invest 110:1525–1538PubMedPubMedCentralCrossRefGoogle Scholar
  229. Yao X, Ye S, Chen Y, Zai Z, Li X, Wang Y, Chen K (2009) Rosiglitazone protects diabetic rats against kidney injury through the suppression of renal matrix metalloproteinase-9 expression. Diabetes Obes Metab 11:519–522PubMedCrossRefGoogle Scholar
  230. 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. Dev Biol 219:18–29PubMedCrossRefGoogle Scholar
  231. Yoshii C, Ueda Y, Okamoto M, Araki M (2007) Neural retinal regeneration in the anuran amphibian Xenopus laevis post-metamorphosis: transdifferentiation of retinal pigmented epithelium regenerates the neural retina. Dev Biol 303:45–56PubMedCrossRefGoogle Scholar
  232. Zhou X, Vize PD (2004) Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322–338PubMedCrossRefGoogle Scholar
  233. Zhou W, Boucher RC, Bollig F, Englert C, Hildebrandt F (2010) Characterization of mesonephric development and regeneration using transgenic zebrafish. Am J Physiol Renal Physiol 299:F1040–F1047PubMedPubMedCentralCrossRefGoogle Scholar
  234. Zon LI (2008) Intrinsic and extrinsic control of haematopoietic stem-cell self-renewal. Nature 453:306–313PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Northeastern UniversityBostonUSA
  2. 2.Tufts UniversityMedfordUSA

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