The renal stem cell system in kidney repair and regeneration

Frontiers in Bioscience

Volumn 13, Issue 16, 2008, Pages 6395-6405

  Anglani, Franca ^a   Ceol, Monica ^a   Mezzabotta, Federica ^a   Torregrossa, Rossella ^a   Tiralongo, Emilia ^a   Tosetto, Enrica ^a   Del Prete, Dorella ^b   D'Angelo, Angela ^b  

^a Divisione di Nefrologia Policlinico IV piano   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

Author keywords

Acute Renal Injury; Acute Tubular Necrosis; Dedifferentiation; EMT; Kidney Regeneration; Kidney Repair; Renal Stem Cells; Review; Tubular Cell Plasticity; Tubular Cell Proliferation

Indexed keywords

MAMMALIA;

ANIMAL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CYTOLOGY; EPITHELIUM CELL; HUMAN; INJURY; ISCHEMIA; KIDNEY; KIDNEY CIRCULATION; KIDNEY TUBULE; MAMMAL; PATHOPHYSIOLOGY; PHYSIOLOGY; REFERENCE VALUE; REGENERATION; STEM CELL;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; EPITHELIAL CELLS; HUMANS; ISCHEMIA; KIDNEY; KIDNEY TUBULES; MAMMALS; REFERENCE VALUES; REGENERATION; RENAL CIRCULATION; STEM CELLS;

EID: 52049109615     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Witzgall R, D. Brown, C. Schwarz, J.V. Bonventre: 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 (1994)
2. Bonventre JV: Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol Suppl 1, S55-S6 (2003)
3. Maeshima A, S. Yamashita, Y. Nojima: Identification of renal progenitor-like tubular cells that participate in the regeneration processes of the kidney. J Am Soc Nephrol 14, 3138-3146 (2003) (Pubitemid 37509291)
4. Oliver JA, O. Maarouf, F.H. Cheema, T.P. Martens, Q. Al-Awqati: The renal papilla is a niche for adult kidney stem cells. J Clin Invest 114, 795-804 (2004) (Pubitemid 39578738)
5. Dekel B, L. Zangi, E. Shezen, S. Reich-Zeliger, S. Eventov-Friedman, H. Katchman, J. Jacob-Hirsch, N. Amariglio, G. Rechavi, R. Margalit, Y. Reisner: Isolation and characterization of nontubular sca-1+lin- multipotent stem/progenitor cells from adult mouse kidney. J Am Soc Nephrol 17, 3300-3314 (2006) (Pubitemid 44865273)
6. Gupta S, C. Verfaillie, D. Chmielewski, S. Kren, K. Eidman, J. Connaire, Y. Heremans, T. Lund, M. Blackstad, Y. Jiang, A. Luttun, M.E. Rosenberg: Isolation and characterization of kidney-derived stem cells. J Am Soc Nephrol 17, 3028-3040 (2006) (Pubitemid 44707763)
7. Poulsom R, M.R. Alison, T. Cook, R. Jeffery, E. Ryan, S.J. Forbes, T. Hunt, S. Wyles, N.A. Wright: Bone marrow stem cells contribute to healing of the kidney. J Am Soc Nephrol Suppl 1, S48-S54 (2003) (Pubitemid 36687040)
8. McTaggart SJ, K. Atkinson: Mesenchymal stem cells: immunobiology and therapeutic potential in kidney disease. Nephrology 12, 44-52 (2007)
9. Thadhani R, M.Pascual, J.V. Bonventre: Acute renal failure. N Engl J Med 334, 1448-1460 (1996) (Pubitemid 126590563)
10. Bonventre JV, D. Brown, K.S. Matlin: Polarity, integrin, and extracellular matrix dynamics in the postischemic rat kidney. Am J Physiol 275, C711-C731 (1998)
11. Sutton TA, C.J. Fisher, B.A. Molitoris: Microvascular endothelial injury and dysfunction during ischemic acute renal failure. Kidney Int 62, 1539-1549 (2002) (Pubitemid 35286261)
12. Imai E, H. Iwatani: The continuing story of renal repair with stem cells. J Am Soc Nephrol 18, 2423-2434 (2007)
13. Gupta S, M.E. Rosenberg: Do Stem Cells Exist in the Adult Kidney? Am J Nephrol 28, 607-613 (2008) (Pubitemid 351832448)
14. Yokoo T, A. Fukui, K. Matsumoto, M. Okabe: Stem cells and kidney organogenesis. Front Biosci 13, 2814-2832 (2008) (Pubitemid 351606107)
15. Vaidya VS, M.A. Ferguson, J.V. Bonventre: Biomarkers of Acute Kidney Injury. Annu Rev Pharmacol Toxicol. 48, 463-493 (2008) (Pubitemid 351738161)
16. Vogetseder A, A. Karadeniz, B. Kaissling, M. Le Hir: Tubular cell proliferation in the healthy rat kidney. Histochem Cell Biol 124, 97-104 (2005) (Pubitemid 41429764)
17. Vogetseder A, T. Palan, D. Bacic, B. Kaissling, M. Le Hir: Proximal tubular epithelial cells are generated by division of differentiated cells in the healthy kidney. Am J Physiol Cell Physiol 292, C807-C813 (2007)
18. Vogetseder A, N. Picard, A. Gaspert, M. Walch, B. Kaissling, M. Le Hir: The proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells. Am J Physiol Cell Physiol 294, C22-8 (2008)
19. Abbate M, D. Brown, J.V. Bonventre: Expression of NCAM recapitulates tubulogenic development in kidneys recovering from acute ischemia. Am J Physiol Renal Physiol 277, F454-F463 (1999) (Pubitemid 29459658)
20. Villanueva S, C. Cespedes, A. Gonzalez, C.P. Vio: bFGF induces an earlier expression of nephrogenic proteins after ischemic acute renal failure. Am J Physiol Regul Integr Comp Physiol 291 (6), R1677-R1687 (2006) (Pubitemid 44904135)
21. Villanueva S, C. Cespedes, C.P. Vio: Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am J Physiol Regul Integr Comp Physiol 290 (4), R861-R870 (2006)
22. Maeshima A, K. Maeshima, Y. Nojima, I. Kojima: Involvement of Pax-2 in the action of activin A on tubular cell regeneration. J Am Soc Nephrol 13 (12), 2850-2859 (2002) (Pubitemid 35386904)
23. Matsumoto K, T. Nakamura: Hepatocyte growth factor: renotropic role and potential therapeutics for renal diseases. Kidney Int 59, 2023-2038 (2001) (Pubitemid 32467594)
24. Anglani F, M. Forino, D. Del Prete, E. Tosetto, R. Torregrossa, A. D'Angelo: In search of adult renal stem cells. J Cell Mol Med 8 (4), 474-487 (2004) (Pubitemid 44145480)
25. Horster MF, G.S. Braun, S.M. Huber: Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation. Physiol rev 79, 1157-1191 (1999) (Pubitemid 29473314)
26. Lu H, M. Guizzetti, L.G. Costa: Inorganic lead activates the mitogen-activated protein kinase kinasemitogen- activated protein kinase-p90 (RSK) signaling pathway in human astrocytoma cells via a protein kinase Cdependent mechanism. J Pharmacol Exp Ther 300 (3), 818-823 (2002) (Pubitemid 34164984)
27. Dierick AM, M. Praet, H. Roels, P. Verbeeck, C. Robyns, W. Oosterlinck: Vimentin expression of renal cell carcinoma in relation to DNA content and histological grading: a combined light microscopic, immunocytochemical and cytophotometrical analysis. Histopathology 18 (4), 315-322 (1991)
28. Holthöfer H, A. Miettinen, V.P. Lehto, E. Lehtonen, I. Virtanen: Expression of vimentin and cytokeratin types of intermediate filament proteins in developing and adult human kidneys. Lab Invest 50 (5), 552-559 (1984) (Pubitemid 14148449)
29. Witzgall R, D. Brown, C. Schwarz, J.V. Bonventre: 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 (5), 2175-2188 (1994)
30. Hatzinger PB, Q. Chen, L.Q. Dong, J.L. Stevens: Alterations in intermediate filament proteins in rat kidney proximal tubule epithelial cells. Biochem Biophys Res Commun 157 (3), 1316-1322 (1988) (Pubitemid 19026001)
31. Wallin A, G. Zhang, T.W. Jones, S. Jaken, J.L. Stevens: 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 (4), 474-484 (1992)
32. Terzi F, R. Maunoury, E. Colucci-Guyon, C. Babinet, P. Federici, P. Briand, G. Friedlander: Normal tubular regeneration and differentiation of the post-ischemic kidney in mice lacking vimentin. Am J Pathol 150 (4), 1361-1371 (1997) (Pubitemid 27152654)
33. Runembert I, G. Queffeulou, P. Federici, F. Vrtovsnik, E. Colucci-Guyon, C. Babinet, P. Briand, G. Trugnan, G. Friedlander, F. Terzi: Vimentin affects localization and activity of sodium-glucose cotransporter SGLT1 in membrane rafts. J Cell Sci 115 (Pt 4), 713-724 (2002) (Pubitemid 34196331)
34. Runembert I, S. Couette, P. Federici, E. Colucci- Guyon, C. Babinet, P. Briand, G. Friedlander, F. Terzi: Recovery of Na-glucose cotransport activity after renal ischemia is impaired in mice lacking vimentin. Am J Physiol Renal Physiol 287 (5), F960-F968 (2004) (Pubitemid 39391093)
35. Alison M, C. Sarraf: Hepatic stem cells. J Hepatol 29, 676-682 (1998) (Pubitemid 28484959)
36. HA Crosby, AJ Strain: Adult liver stem cells: bone marrow, blood, or liver derived? Gut 48, 153-154 (2001) (Pubitemid 32141836)
37. Fausto N, J.S. Campbell: The role of hepatocytes and oval cells in liver regeneration and repopulation. Mech Dev 120, 117-130 (2003) (Pubitemid 35462100)
38. Vassilopoulos G, P.R. Wang, D.W. Russell: Transplanted bone marrow regenerates liver by cell fusion. Nature 422, 901-4 (2003) (Pubitemid 36520043)
39. Wang X, H. Willenbring, Y. Akkari, Y. Torimaru, M. Foster, M. Al-Dhalimy, E. Lagasse, M. Finegold, S. Olson, M. Grompe: Cell fusion is the principal source of bonemarrow- derived hepatocytes. Nature 422, 897-901 (2003) (Pubitemid 36520042)
40. Ferrari G, G. Cusella-De Angelis, M. Coletta, E. Paolucci, A. Stornaiuolo, G. Cossu, F. Mavilio: Muscle regeneration by bone-marrow derived myogenic progenitor. Science 279, 1528-1530 (1998) (Pubitemid 28217075)
41. Wagers AJ, I.L. Weissman: Plasticity of adult stem cells. Cell 116, 639-48 (2004) (Pubitemid 38326723)
42. Poulsom R, S. Forbes, K. Hodivala-Dilke, E. Ryan, S. Wyles, S. Navaratnarasah, R. Jeffery, T. Hunt, M. Alison, T. Cook, C. Pusey, N.A. Wright: Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 193, 1-7 (2001)
43. Grimm CP, P. Nickerson, J. Jeffery, R.C. Savani, J. Gough, R.M. McKenna, E. Stern, D.N. Rush: Neointimal and tubulointerstitial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection. N Engl J Med 345, 93-97 (2001) (Pubitemid 32634567)
44. Ito T, A. Suzuki, E. Imai, M. Okabe, M. Hori: Bone marrow is a reservoir of repopulating mesangial cells during glomerular remodeling. J Am Soc Nephrol 12, 2625-2635 (2001) (Pubitemid 33115409)
45. Gupta S, C. Verfaillie, D Chmielewski, Y. Kim, M.E. Rosenberg: A role for extrarenal cells in the regeneration following acute renal failure. Kidney Int 62, 1285-1290 (2002)
46. Fang TC, M.R. Alison, H.T. Cook, R. Jeffery, N.A. Wright, R. Poulsom: Proliferation of bone marrow-derived cells contributes to regeneration after folic acid-induced acute tubular injury. J Am Soc Nephrol 16, 1723-1732 (2005) (Pubitemid 41716478)
47. Lin F, A. Moran, P. Igarashi: Intrarenal cells, not bone marrow-derived cells, are the major source for regeneration in postischemic kidney. J Clin Invest 115, 1756-1764 (2005) (Pubitemid 40979714)
48. Duffield JS, K.M. Park, L.L. Hsiao, V.R. Kelley, D.T. Scadden, T. Ichimura, J.V. Bonventre: Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 115, 1743-1755 (2005) (Pubitemid 40979713)
49. Stokman G, J.C. Leemans, N. Claessen, J.J. Weening, S. Florquin: Hematopoietic stem cell mobilization therapy accelerates recovery of renal function independent of stem cell contribution. J Am Soc Nephrol 16, 1684-1692 (2005) (Pubitemid 41716474)
50. Duffield JS, J.V. Bonventre: Kidney tubular epithelium is restored without replacement with bone marrow-derived cells during repair after ischemic injury. Kidney Int 68, 1956-1961 (2005) (Pubitemid 43117771)
51. Humphreys BD, J.V. Bonventre: The contribution of adult stem cells to renal repair. Nephrol Ther 3, 3-10 (2007) (Pubitemid 46454395)
52. Cipolleschi MG, P. Dello Sbarba, M. Olivotto: The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 82, 2031-2037 (1993) (Pubitemid 23293984)
53. Danet GH, Y. Pan, J.L. Luongo, D.A. Bonnet, M.C. Simon: Expansion of human SCID-repopulating cells under hypoxic conditions. J. Clin. Invest 112, 126-135 (2003) (Pubitemid 38056384)
54. Nern C, S. Momma: The realized niche of adult neural stem cells. Stem Cell Rev 2, 233-40 (2006) (Pubitemid 47109401)
55. Al-Awqati Q, J.A. Oliver: The kidney papilla is a stem cells niche. Stem Cell Rev 2, 181-184 (2006) (Pubitemid 47109398)
56. Bussolati B, S. Bruno, C. Grange, S. Buttiglieri, M.C. Deregibus, D. Cantino, G. Camussi: Isolation of renal progenitor cells from adult human kidney. Am J Pathol 166, 545-555 (2005) (Pubitemid 40189050)
57. Sagrinati C, G.S. Netti, B. Mazzinghi, E. Lazzeri, F. Liotta, F. Frosali, E. Ronconi, C. Meini, M. Gacci, R. Squecco, M. Carini, L. Gesualdo, F. Francini, E. Maggi, F. Annunziato, L. Lasagni, M. Serio, S. Romagnani, P. Romagnani: Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J Am Soc Nephrol 17, 2443-2456 (2006) (Pubitemid 44300960)
58. Singh SR, W. Liu, S.X. Hou: The adult Drosophila Malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 1, 191-203 (2007) (Pubitemid 47215591)
59. Elger M, H. Hentschel, J. Litteral, M. Wellner, T. Kirsch, F.C. Luft, H. Haller: Nephrogenesis is induced by partial nephrectomy in the elasmobranch Leucoraja erinacea. J Am Soc Nephrol 14, 1506-1518 (2003) (Pubitemid 36687052)
60. Cotsarelis G, S.Z. Cheng, G. Dong, T.T. Sun, R.M. Lavker: Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57, 201-209 (1989) (Pubitemid 19112360)
61. Lavker RM, T.T. Sun: Epidermal stem cells: properties, markers, and location. Proc Natl Acad Sci USA 97, 13473-13475 (2000)
62. Goodell MA, K. Brose, G. Paradis, A.S. Conner, R.C. Mulligan: Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183, 1797-1806 (1996) (Pubitemid 26134320)
63. Zhou S, J.D. Schuetz, K.D. Bunting, A.M. Colapietro, J. Sampath, J.J. Morris, I. Lagutina, G.C. Grosveld, M. Osawa, H. Nakauchi, B.P. Sorrentino: The ABC ransporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7, 1028-1034 (2001) (Pubitemid 32937383)
64. Asakura A, P. Seale, A. Girgis-Gabardo, M.A. Rudnicki: Myogenic specification of side population cells in skeletal muscle. J Cell Biol 159, 123-134 (2002) (Pubitemid 35191524)
65. Hishikawa K, T. Marumo, S. Miura, A. Nakanishi, Y. Matsuzaki, K. Shibata, T. Ichiyanagi, H. Kohike, T. Komori, I. Takahashi, O. Takase, N. Imai, M. Yoshikawa, T. Inowa, M. Hayashi, T. Nakaki, H. Nakauchi, H. Okano, T. Fujita: Musculin/MyoR is expressed in kidney side population cells and can regulate their function. J Cell Biol 169, 921-928 (2005) (Pubitemid 41002868)
66. Challen GA, I. Bertoncello, J.A. Deane, S.D. Ricardo, M.H. Little: Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J Am Soc Nephrol 17, 1896-1912 (2006) (Pubitemid 44036174)
67. Kitamura S, Y. Yamasaki, M. Kinomura, T. Sugaya, H. Sugiyama, Y. Maeshima, H. Makino: Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J 19, 1789-1797 (2005) (Pubitemid 41598763)
68. Maeshima A, H. Sakurai, S.K. Nigam: Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J Am Soc Nephrol 17, 188-198 (2006)
69. Witzgall R: Are renal proximal tubular epithelial cells constantly prepared for an emergency? Focus on "the proliferation capacity of the renal proximal tubule involves the bulk of differentiated epithelial cells". Am J Physiol Cell Physiol 294, C1-3 (2008)
70. Fujigaki Y, T. Goto, M. Sakakima, H. Fukasawa, T. Miyaji, T. Yamamoto, A. Hishida: Kinetics and characterization of initially regenerating proximal tubules in S3 segment in response to various degrees of acute tubular injury. Nephrol Dial Transplant 21, 41-50 (2006) (Pubitemid 43057108)
71. Zavadil J, E.P. Böttinger: TGF-beta and epithelial-tomesenchymal transitions. Oncogene 24, 5764-5774 (2005)
72. Zeisberg M, R. Kalluri: The role of epithelial-tomesenchymal transition in renal fibrosis. J Mol Med 82, 175-181 (2004) (Pubitemid 38392167)
73. Kalluri R, E.G. Neilson: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112, 1776-1784 (2003) (Pubitemid 38063698)
74. Campanaro S, S. Picelli, R. Torregrossa, L. Colluto, M. Ceol, D. Del Prete, A. D'Angelo, G. Valle, F. Anglani: Genes involved in TGFbeta1-driven epithelialmesenchymal transition of renal epithelial cells are topologically related in the human interactome map. BMC Genomics (2007) doi:10.1186/1471-2164- 8-383
75. Bianchi G, A. Muraglia, A. Daga, G. Corte, R. Cancedda, R. Quarto: Microenvironment and stem properties of bone-marrow derived mesenchymal cells. Wound Repair and Regeneration 9, 460-466 (2001) (Pubitemid 34266726)