Regeneration of Functional Pronephric Proximal Tubules After Partial Nephrectomy in Xenopus laevis

Developmental Dynamics

Volumn 242, Issue 3, 2013, Pages 219-229

  Caine, Shoshoni T ^a   Mclaughlin, Kelly A ^a  

^a TUFTS UNIVERSITY   (United States)

Author keywords

Apoptosis; Kidney regeneration; Mmp 9; Pronephros; Renal repair; Wound healing; Xenopus laevis

Indexed keywords

GELATINASE B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; IMMUNOHISTOCHEMISTRY; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; NONHUMAN; PARTIAL NEPHRECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TISSUE REGENERATION; TISSUE REPAIR; UNINEPHRECTOMY; WOUND HEALING; XENOPUS LAEVIS;

ANIMALS; KIDNEY TUBULES, PROXIMAL; LARVA; NEPHRECTOMY; PRONEPHROS; REGENERATION; XENOPUS LAEVIS;

AMPHIBIA; XENOPUS LAEVIS;

EID: 84874189026     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23916     Document Type: Article

References (84)

1. Arnould C, Lelièvre-Pégorier M, Ronco P, Lelongt B. 2009. MMP9 limits apoptosis and stimulates branching morphogenesis during kidney development. J Am Soc Nephrol 20:2171-2180.
2. Augusto J, Smith B, Smith S, Robertson J, Reimschuessel R. 1996. Gentamicin-induced nephrotoxicity and nephroneogenesis in Oreochromis nilotica, a tilapian fish. Dis Aquatic Org 26:49-58.
3. Barletta GM, Kovari IA, Verma RK, Kerjaschki D, Holzman LB. 2003. Nephrin and Neph1 co-localize at the podocyte foot process intercellular junction and form cis hetero-oligomers. J Biol Chem 278:19266-19271.
4. Bengatta S, Arnould C, Letavernier E, Monge M, DePréneuf HM, Werb Z, Ronco P, Lelongt B. 2009. MMP9 and SCF protect from apoptosis in acute kidney injury. J Am Soc Nephrol 20:787-797.
5. Bettencourt-Dias M, Mittnacht S, Brockes JP. 2003. Heterogeneous proliferative potential in regenerative adult newt cardiomyocytes. J Cell Sci 116:4001-4009.
6. Bigg HF, Rowan AD, Barker MD, Cawston TE. 2007. Activity of matrix metalloproteinase-9 against native collagen types I and III. FEBS J 274:1246-1255.
7. Birn H, Fyfe JC, Jacobsen C, Mounier F, Verroust PJ, Orskov H, Willnow TE, Moestrup SK, Christensen EI. 2000. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J Clin Invest 105:1353-1361.
8. Bonventre JV. 2003. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol 14(suppl 1)S55-S61.
9. Bonventre JV. 2010. Mechanisms of acute kidney injury and repair. In: Jörres A, Ronco C, Kellum JA, editors. Management of acute kidney problems. Berlin: Springer. p 13-20.
10. 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 63:615-624.
11. Brändli AW. 1999. Towards a molecular anatomy of the Xenopus pronephric kidney. Int J Dev Biol 43:381-395.
12. Carinato ME, Walter BE, Henry JJ. 2000. Xenopus laevis gelatinase B (Xmmp-9): development, regeneration, and wound healing. Dev Dyn 217:377-387.
13. Carlson MRJ, Komine Y, Bryant SV, Gardiner DM. 2001. Expression of Hoxb13 and Hoxc10 in developing and regenerating axolotl limbs and tails. Dev Biol 229:396-406.
14. Carroll T, Wallingford J, Seufert D, Vize PD. 1999a. Molecular regulation of pronephric development. Curr Top Dev Biol 44:67-100.
15. Carroll TJ, Wallingford JB, Vize PD. 1999b. Dynamic patterns of gene expression in the developing pronephros of Xenopus laevis. Dev Genet 24:199-207.
16. Christensen EI, Raciti D, Reggiani L, Verroust PJ, Brandli AW. 2008. Gene expression analysis defines the proximal tubule as the compartment for endocytic receptor-mediated uptake in the Xenopus pronephric kidney. Pflug Arch Eur J Physiol 456:1163-1176.
17. Chromek M, Tullus K, Hertting O, Jaremko G, Khalil A, Li YH, Brauner A. 2003. Matrix metalloproteinase-9 and tissue inhibitor of metalloproteinases-1 in acute pyelonephritis and renal scarring. Pediatr Res 53:698-705.
18. Chromek M, Tullus K, Lundahl J, Brauner A. 2004. Tissue inhibitor of metalloproteinase 1 activates normal human granulocytes, protects them from apoptosis, and blocks their transmigration during inflammation. Infect Immun 72:82-88.
19. Cuppage FE, Chiga M, Tate A. 1972. Cell cycle studies in the regenerating rat nephron following injury with mercuric chloride. Lab Invest 26:122-126.
20. 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 470:95-101.
21. Dressler GR. 2006. The cellular basis of kidney development. Annu Rev Cell Dev Biol 22:509-529.
22. 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 125:4655-4667.
23. 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 14:1506-1518.
24. Fini ME, Cook JR, Mohan R. 1998. Proteolytic mechanisms in corneal ulceration and repair. Arch Dermatol Res Suppl 290(suppl):S12-S23.
25. 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 205:235-244.
26. Gardiner DM, Carlson MRJ, Roy S. 1999. Towards a functional analysis of limb regeneration. Semin Cell Dev Biol 10:385-393.
27. Gargioli C, Slack JMW. 2004. Cell lineage tracing during Xenopus tail regeneration. Development 131:2669-2679.
28. Gobe G, Buttyan R. 2002. Apoptosis in the pathogenesis of renal disease with a focus on tubulointerstitial injury. Nephrology 7:287-293.
29. Gobé GC, Buttyan R, Wyburn KRL, Etheridge MR, Smith PJ. 1995. Clusterin expression and apoptosis in tissue remodeling associated with renal regeneration. Kidney Int 47:411-420.
30. González-Avila G, Iturria C, Vadillo-Ortega F, Ovalle C, Montano M. 1998. Changes in matrix metalloproteinases during the evolution of interstitial renal fibrosis in a rat experimental model. Pathobiology 66:196-204.
31. Harland RM. 1991. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36:685-695.
32. Harty M, Neff AW, King MW, Mescher AL. 2003. Regeneration or scarring: an immunologic perspective. Dev Dyn 226:268-279.
33. Hentschel DM, Kwon MP, Cilenti L, Zervos AS, Drummond I, Bonventre JV. 2005. Acute renal failure in zebrafish: a novel system to study a complex disease. Am J Physiol Renal Physiol 288:F923-F929.
34. 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 122:486-490.
35. Huang YY, Chen MJ, Chiu NT, Chou HH, Lin KY, Chiou YY. 2011. Adjunctive oral methylprednisolone in pediatric acute pyelonephritis alleviates renal scarring. Pediatrics 128:e496-e504.
36. Humphreys BD. 2011. Genetic tracing of the epithelial lineage during mammalian kidney repair. Int Soc Nephrol 1:83-86.
37. Humphreys BD, Czerniak S, DiRocco DP, Hasnain W, Cheema R, Bonventre JV. 2011. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci U S A 108:9226-9231.
38. 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 2:284-291.
39. Imgrund M, Grone E, Grone HJ, Kretzler M, Holzman L, Schlondorff D, Rothenpieler UW. 1999. Re-expression of the developmental gene Pax-2 during experimental acute tubular necrosis in mice. Kidney Int 56:1423-1431.
40. Johnson CS, Holzemer NF, Wingert RA. 2011. Laser ablation of the zebrafish pronephros to study renal epithelial regeneration. J Vis Exp 54:2845.
41. Johnson LL, Dyer R, Hupe DJ. 1998. Matrix metalloproteinases. Curr Opin Chem Biol 2:466-471.
42. Kay BK, Peng HB, editors. 1991. Methods in cell biology. Xenopus laevis: practical uses in cell and molecular biology. San Diego, CA: Academic Press Inc. 718 p.
43. Kays SE, Schnellmann RG. 1995. Regeneration of renal proximal tubule cells in primary culture following toxicant injury: response to growth factors. Toxicol Appl Pharmacol 132:273-280.
44. Kovacs CJ, Braunschweiger PG, Schenken LL, Burholt DR. 1982. Proliferative defects in renal and intestinal epithelium after cis-dichlorodiammine platinum (II). Br J Cancer 45:286-294.
45. Kuure S, Vuolteenaho R, Vainio S. 2000. Kidney morphogenesis: cellular and molecular regulation. Mech Dev 92:31-45.
46. Lauriola L, Tallini G, Sentinelli S, Massi G. 1986. Protein absorption by tubular mesonephric and metanephric structures in the human embryo. An immunohistochemical study. Cell Tissue Res 246:77-80.
47. Lazzara MJ, Deen WM. 2007. Model of albumin reabsorption in the proximal tubule. Am J Physiol Renal Physiol 292:F430-F439.
48. Lelongt B, Trugnan G, Murphy G, Ronco PM. 1997. Matrix metalloproteinases MMP2 and MMP9 are produced in early stages of kidney morphogenesis but only MMP9 is required for renal organogenesis in vitro. J Cell Biol 136:1363-1373.
49. 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 298:129-139.
50. Liu Y. 2011. Cellular and molecular mechanisms of renal fibrosis. Nat Rev Nephrol 7:684-696.
51. Liu Y, Min D, Bolton T, Nube V, Twigg SM, Yue DK, Mclennan SV. 2009. Increased matrix metalloproteinase-9 predicts poor wound healing in diabetic foot ulcers. Diabetes Care 32:117-119.
52. Lo DC, Allen F, Brockes JP. 1993. Reversal of muscle differentiation during urodele limb regeneration. Proc Natl Acad Sci U S A 90:7230-7234.
53. Matrisian LM. 1992. The matrix-degrading metalloproteinases. Bioessays 14:455-463.
54. Menè P, Polci R, Festuccia F. 2003. Mechanisms of repair after kidney injury. J Nephrol 16:186-195.
55. 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 26:230-239.
56. Nakajima K, Fujimoto K, Yaoita Y. 2005. Programmed cell death during amphibian metamorphosis. Sem Cell Dev Biol 16:271-280.
57. Nieuwkoop PD, Faber J, editors. 1994. Normal table of Xenopus laevis (daudin). New York: Garland Publishing, Inc. 252 p.
58. Nonclercq D, Wrona S, Toubeau G, Zanen J, Heuson-Stiennon JA, Schaudies RP, Laurent G. 1992. Tubular injury and regeneration in the rat kidney following acute exposure to gentamicin: a time-course study. Ren Fail 14:507-521.
59. Nony PA, Schnellmann RG. 2003. Mechanisms of renal cell repair and regeneration after acute renal failure. J Pharmacol Exp Ther 304:905-912.
60. Poss KD, Wilson LG, Keating MT. 2002. Heart regeneration in zebrafish. Science 298:2188-2190.
61. Price J, Allen S. 2004. Exploring the mechanisms regulating regeneration of deer antlers. Philos Trans R Soc Lond Ser B Biol Sci 359:809-822.
62. Reimschuessel R. 2001. A fish model of renal regeneration and development. ILAR J 42:285-291.
63. Reimschuessel R, Williams D. 1995. Development of new nephrons in adult kidneys following gentamicin-induced nephrotoxicity. Ren Fail 17:101-106.
64. Robert J, Cohen N. 1998. Evolution of immune surveillance and tumor immunity: studies in Xenopus. Immunol Rev 166:231-243.
65. Salice CJ, Rokous JS, Kane AS, Reimschuessel R. 2001. New nephron development in goldfish (Carassius auratus) kidneys following repeated gentamicin-induced nephrotoxicosis. Comp Med 51:56-59.
66. Salo T, Makela M, Kylmaniemi M, Autio-Harmainen H, Larjava H. 1994. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab Invest 70:176-182.
67. Saxén L. 1987. Organogenesis of the kidney. Cambridge, UK: Cambridge University Press. 173 p.
68. Sheridan AM, Bonventre JV. 2000. Cell biology and molecular mechanisms of injury in ischemic acute renal failure. Curr Opin Nephrol Hypertens 9:427-434.
69. Tseng AS, Adams DS, Qiu D, Koustubhan P, Levin M. 2007. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev Biol 301:62-69.
70. Tucker B, Klassen H, Yang L, Chen DF, Young MJ. 2008. Elevated MMP expression in the MRL mouse retina creates a permissive environment for retinal regeneration. Invest Ophthalmol Vis Sci 49:1686-1695.
71. 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 14:31-49.
72. Verroust PJ, Birn H, Nielsen R, Kozyraki R, Christensen EI. 2002. The tandem endocytic receptors megalin and cubilin are important proteins in renal pathology. Kidney Int 62:745-756.
73. Vize PD, Jones EA, Pfister R. 1995. Development of the Xenopus pronephric system. Dev Biol 171:531-540.
74. 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 188:189-204.
75. 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 Invest 66:474-484.
76. 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: original article. Dev Growth Differ 51:135-143.
77. Wesson LG. 1989. Compensatory growth and other growth responses of the kidney. Nephron 51:149-184.
78. 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 93:2175-2188.
79. Wynn TA. 2008. Cellular and molecular mechanisms of fibrosis. J Pathol 214:199-210.
80. 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 216:2-9.
81. 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 303:45-56.
82. 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:F1040-1047.
83. Zhou X, Vize PD. 2004. Proximo-distal specialization of epithelial transport processes within the Xenopus pronephric kidney tubules. Dev Biol 271:322-338.
84. Zukor KA, Kent DT, Odelberg SJ. 2011. Meningeal cells and glia establish a permissive environment for axon regeneration after spinal cord injury in newts. Neural Dev 6:1.