Isolation of clonogenic, long-term self renewing embryonic renal stem cells

Stem Cell Research

Volumn 5, Issue 1, 2010, Pages 23-39

  Lusis, M ^a,c   Li, J ^a,c   Ineson, J ^a,c   Christensen, M E ^b   Rice, A ^b   Little, M H ^a,c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MATER MEDICAL RESEARCH INSTITUTE   (Australia)

^c Australian Stem Cell Centre   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; THROMBIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EYA1; TRANSCRIPTION FACTOR HOXA11; TRANSCRIPTION FACTOR OSR1; TRANSCRIPTION FACTOR SALL1; TRANSCRIPTION FACTOR SIX1; TRANSCRIPTION FACTOR SIX2; UNCLASSIFIED DRUG; WT1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL IMMORTALIZATION; CELL ISOLATION; CELL POPULATION; CELL RENEWAL; CELL SURVIVAL; CLONOGENESIS; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EXPLANT; KIDNEY DEVELOPMENT; KIDNEY EPITHELIUM; KIDNEY INTERSTITIUM; KIDNEY STEM CELL; MESENCHYME CELL; MOUSE; MULTIPOTENT STEM CELL; NEPHRON; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; EMBRYONIC STEM CELLS; GENE EXPRESSION; IMMUNOPHENOTYPING; KIDNEY; MICE; TIME FACTORS;

EID: 77953288762     PISSN: 18735061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.scr.2010.03.003     Document Type: Article

References (71)

1. Appel D., Kershaw D., Smeets B., Yuan G., Fuss A., Frye B., Elger M., Kriz W., Floege J., and Moeller M.J. Derivation of podocytes from the parietal cell compartment. J. Am. Soc. Nephrol. 20 2 (2009) 333-343
2. Bartholomew A., Sturgeon C., Siatskas M., Ferrer K., McIntosh K., Patil S., Hardy W., Devine S., Ucker D., Deans R., Moseley A., and Hoffman R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30 (2002) 42-48
3. Bearzi C., Rota M., Hosoda T., Tillmanns J., Nascimbene A., De Angelis A., Yasuzawa-Amano S., Trofimova I., Siggins R.W., Lecapitaine N., Cascapera S., Beltrami A.P., D'Alessandro D.A., Zias E., Quaini F., Urbanek K., Michler R.E., Bolli R., Kajstura J., Leri A., and Anversa A.P. Human cardiac stem cells. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 14068-14073
4. Bowes III R.C., Lightfoot R.T., van de Water B., and Stevens J.L. Hepatocyte growth factor induces tubulogenesis of primary renal proximal tubular epithelial cells. J. Cell. Physiol. 180 (1999) 81-90
5. Brophy P.D., Ostrom L., Lang K.M., and Dressler G.R. Regulation of ureteric bud outgrowth by Pax2-dependent activation of the glial derived neurotrophic factor gene. Development 128 (2001) 4747-4756
6. Bussolati B., Bruno S., Grange C., Buttiglieri S., Deregibus M.C., Cantino D., Camussi M., and Isolation M. of renal progenitor cells from adult human kidney. Am. J. Pathol. 166 (2005) 545-555
7. Bussolati B., Bruno S., Grange C., Buttiglieri S., Deregibus M.C., Cantino D., and Camussi G. Isolation of renal progenitor cells from adult human kidney. Am. J. Pathol. 166 (2005) 545-555
8. Campos L.S., Leone D.P., Relvas J.B., Brakebusch C., Fassler R., Suter U., and French-Constant C. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131 (2004) 3433-3444
9. Carroll T.J., Park J.S., Hayashi S., Majumdar A., and McMahon A.P. Wnt9b plays a central role in the regulation of mesenchymal to epithelial transitions underlying organogenesis of the mammalian urogenital system. Dev. Cell. 9 2 (2005) 283-292
10. Challen G.A., Bertoncello I., Deane J., Ricardo S., and Little M.H. Kidney side population cells represent a non-haematopoietic but heterogeneous population with multilineage and renal potential. J. Am. Soc. Nephrol. 17 7 (2006) 1896-1912
11. Coresh J., Selvin E., Stevens L.A., Manzi J., Kusek J.W., Eggers P., et al. Prevalence of chronic kidney disease in the United States. JAMA 298 (2007) 2038-2047
12. Cucina A., Borrelli V., Lucarelli M., Sterpetti A.V., Cavallaro A., Strom R., Santoro-D'Angelo L., and Scarpa S. Autocrine production of basic fibroblast growth factor translated from novel synthesized mRNA mediates thrombin-induced mitogenesis in smooth muscle cells. Cell Biochem. Funct. 20 (2002) 39-46
13. De Strooper B., Van der Schueren B., Jaspers M., Saison M., Spaepen M., Van Leuven F., Van den Berghe H., and Cassiman J.J. Distribution of the beta 1 subgroup of the integrins in human cells and tissues. J. Histochem. Cytochem. 37 (1989) 299-307
14. Dekel B., Zangi L., Shezen E., Reich-Zeliger S., Eventov-Friedman S., Katchman H., Jacob-Hirsch J., Amariglio N., Rechavi G., Margalit R., and Reisner Y. Isolation and characterization of nontubular sca-1+lin- multipotent stem/progenitor cells from adult mouse kidney. J. Am. Soc. Nephrol. 17 (2006) 3300-3314
15. Di Rocco G., Iachininoto M.G., Tritarelli A., Straino S., Zacheo A., Germani A., and Crea F. Capogrossi MC.Myogenic potential of adipose-tissue-derived cells. J. Cell Sci. 119 (2006) 2945-2952
16. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F., Krause D., Deans R., Keating A., Prockop D., and Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8 (2006) 315-317
17. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.S., and Wicha M.S. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17 (2003) 1253-1270
18. Fadini G.P., Avogaro A., and Agostini C. Critical assessment of putative endothelial progenitor phenotypes. Exp. Hematol. 35 (2007) 1479-1480
19. Gee K., Kryworuchko M., and Kumar A. Recent advances in the regulation of CD44 expression and its role in inflammation and autoimmune diseases. Arch. Immunol. Ther. Exp. (Warsz) 52 (2004) 13-26
20. Gritti A., Parati E.A., Cova L., Frolichsthal P., Galli R., Wanke E., Faravelli L., Morassutti D.J., Roisen F., Nickel D.D., and Vescovi A.L. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J. Neurosci. 16 (1996) 1091-1100
21. Gupta S., Verfaillie C., Chmielewski D., Kren S., Eidman K., Connaire J., Heremans Y., Lund T., Blackstad M., Jiang Y., Luttun A., and Rosenberg M.E. Isolation and characterization of kidney-derived stem cells. J. Am. Soc. Nephrol. 17 (2006) 3028-3040
22. Hadjantonakis A.K., Gertsenstein M., Ikawa M., Okabe M., and Nagy A. Generating green fluorescent mice by germline transmission of green fluorescent ES cells. Mech. Dev. 76 (1998) 79-90
23. Han H.J., Sigurdson W.J., Nickerson P.A., and Taub M. Both mitogen activated protein kinase and the mammalian target of rapamycin modulate the development of functional renal proximal tubules in matrigel. J. Cell Sci. 117 (2004) 1821-1833
24. Haniffa M.A., Wang X.N., Holtick U., Rae M., Isaacs J.D., Dickinson A.M., Hilkens C.M., and Collin M.P. Adult human fibroblasts are potent immunoregulatory cells and functionally equivalent to mesenchymal stem cells. J. Immunol. 179 (2007) 1595-1604
25. Hartman H.A., Lai H.L., and Patterson L.T. Cessation of renal morphogenesis in mice. Dev. Biol. 310 2 (2007) 379-387
26. Hopkins C., Li J., Rae F., and Little M.H. Stem cell options for kidney disease. J. Pathol. 217 2 (2009) 265-281
27. Humphreys B.D., Valerius M.T., Kobayashi A., Mugford J.W., Soeung S., Duffield J.S., et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2 (2008) 284-291
28. Imokawa Y., and Brockes J.P. Selective activation of thrombin is a critical determinant for vertebrate lens regeneration. Curr. Biol. 13 (2003) 877-881
29. Imokawa Y., Simon A., and Brockes J.P. A critical role for thrombin in vertebrate lens regeneration. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359 (2004) 765-776
30. James R.G., Kamei C.N., Wang Q., Jiang R., and Schultheiss T.M. Odd-skipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development 133 (2006) 2995-3004
31. Jessberger S., Clemenson Jr. G.D., and Gage F.H. Spontaneous fusion and nonclonal growth of adult neural stem cells. Stem Cells 25 (2007) 871-874
32. Kartsanis G., Douros K., Ravazoula P., and Fokaefs E. Adult Wilms' tumor: a case report and review of literature. Int. Urol. Nephrol. 39 1 (2007) 3-6
33. Kispert A., Vainio S., and McMahon A.P. Wnt-4 is a mesenchymal signal for epithelial transformation of metanephric mesenchyme in the developing kidney. Development 125 (1998) 4225-4234
34. Kitamura S., Yamasaki Y., Kinomura M., Sugaya T., Sugiyama H., Maeshima Y., and Makino H. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. Faseb J. 19 (2005) 1789-1797
35. Kobayashi A., Valerius M.T., Mugford J.W., Carroll T.J., Self M., Oliver G., and McMahon A.P. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell. 3 2 (2008) 169-181
36. Kreidberg J.A., Sariola H., Loring J.M., Maeda M., Pelletier J., Housman D., and Jaenisch R. WT-1 is required for early kidney development. Cell 74 (1993) 679-691
37. Lawson D.A., Xin L., Lukacs R.U., Cheng D., and Witte O.N. Isolation and functional characterization of murine prostate stem cells. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 181-186
38. Little M.H. Starting the kidney over again. Developmental Biology of Neoplastic Growth. Prog. Mol. Subcell Biol. vol. 40 (2005), Springer-Verlag 107-132
39. Maeshima A., Yamashita S., and Nojima Y. Identification of renal progenitor-like tubular cells that participate in the regeneration processes of the kidney. J. Am. Soc. Nephrol. 14 (2003) 3138-3146
40. Maeshima A., Sakurai H., and Nigam S. Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J. Am. Soc. Nephrol. 17 (2006) 188-198
41. Meirelles L., Chagastelles P.C., and Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 119 (2006) 2204-2213
42. 3 into male rats and mice. Am. J. Anat. 106 (1960) 247-285
43. Messina E., De Angelis L., Frati G., Morrone S., Chimenti S., Fiordaliso F., Salio M., Battaglia M., Latronico M.V., Coletta M., Vivarelli E., Frati L., Cossu G., and Giacomello A. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ. Res. 95 (2004) 911-921
44. Metsuyanim S., Pode-Shakked N., Schmidt-Ott K.M., Keshet G., Rechavi G., Blumental D., and Dekel B. Accumulation of malignant renal stem cells is associated with epigenetic changes in normal renal progenitor genes. Stem Cells 26 7 (2008) 1808-1817
45. Murphy A.J., Viero S., Ho M., and Thorner P.S. Diagnostic utility of nestin expression in pediatric tumors in the region of the kidney. Appl. Immunohistochem. Mol. Morphol. 17 6 (2009) 517-523
46. Oliver J.A., Barasch J., Yang J., and Herzlinger D. D., Q. Al-Awqati. Metanephric mesenchyme contains embryonic renal stem cells. Am. J. Physiol. Renal. Physiol. 283 (2002) F799-F809
47. Oliver J., Maarouf O., Cheema F.H., Martens T.P., and Al-Awqati Q. The renal papilla is a niche for adult kidney stem cells. J. Clin. Invest. 114 (2004) 795-804
48. Osafune K., Takasato M., Kispert A., Asashima M., and Nishinakamura R. Identification of multipotent progenitors in the embryonic mouse kidney by a novel colony-forming assay. Development 133 (2006) 151-161
49. Phelps D.E., and Dressler G.R. Aberrant expression of Pax-2 in Danforth's short tail (Sd) mice. Dev. Biol. 157 (1993) 251-258
50. Pode-Shakked N., Metsuyanim S., Rom-Gross E., Mor Y., Fridman E., Goldstein I., Amariglio N., Rechavi G., Keshet G., and Dekel B. Developmental tumourigenesis: NCAM as a putative marker for the malignant renal stem/progenitor cell population. J. Cell. Mol. Med. 13 8B (2009) 1792-1808
51. Reynolds B.A., and Rietze R.L. Neural stem cells and neurospheres-re-evaluating the relationship. Nat. Meth. 2 (2005) 333-336
52. Reynolds B.A., and Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255 (1992) 1707-1710
53. Robertson N.J. P.J., Fairchild, H. Waldmann. Ectopic transplantation of tissues under the kidney capsule. Methods Mol. Biol. 380 (2007) 347-354
54. Ronconi E., Sagrinati C., Angelotti M.L., Lazzeri E., Mazzinghi B., Ballerini L., Parente E., Becherucci F., Gacci M., Carini M., Maggi E., Serio M., Vannelli G.B., Lasagni L., Romagnani S., and Romagnani P. Regeneration of glomerular podocytes by human renal progenitors. J. Am. Soc. Nephrol. 20 2 (2009) 322-332
55. Rothenpieler U.W., and Dressler G.R. Pax-2 is required for mesenchyme-to-epithelium conversion during kidney development. Development 119 (1993) 711-720
56. Santos O.F., Nigam S.K., and HGF-induced S.K. tubulogenesis and branching of epithelial cells is modulated by extracellular matrix and TGF-beta. Dev. Biol. 160 (1993) 293-302
57. Self M., Lagutin O.V., Bowling B., Hendrix J., Cai Y., Dressler G.R., and Oliver G. Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J. 25 (2006) 5214-5228
58. Short B.J., Brouard N., and Simmons P.J. Prospective isolation of mesenchymal stem cells from mouse compact bone. Methods Mol. Biol. 482 (2009) 259-268
59. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., Frotscher M., and Snyder E.Y. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Meth. 3 (2006) 801-806
60. Srinivas S., Goldberg M.R., Watanabe T., D'Agati V., al-Awqati Q., and Costantini F. Expression of green fluorescent protein in the ureteric bud of transgenic mice: a new tool for the analysis of ureteric bud morphogenesis. Dev. Genet. 24 3-4 (1999) 241-251
61. Stark K., Vainio S., Vassileva G., and McMahon A.P. Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature 372 (1994) 679-683
62. Takasato M., Osafune K., Matsumoto Y., Kataoka Y., Yoshida N., Meguro H., Aburatani H., Asashima M., and Nishinakamura R. Identification of kidney mesenchymal genes by a combination of microarray analysis and Sall1-GFP knockin mice. Mech. Dev. 121 (2004) 547-557
63. Taub M., Wang Y., Szczesny T.M., and Kleinman H.K. Epidermal growth factor or transforming growth factor alpha is required for kidney tubulogenesis in matrigel cultures in serum-free medium. Proc. Natl Acad. Sci. U. S. A. 87 (1990) 4002-4006
64. Toma T.G., McKenzie I.A., Bagli D., and Miller F.D. Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23 (2005) 727-737
65. Torres M., Gomez-Pardo E., Dressler G.R., and Gruss P. P. Pax-2 controls multiple steps of urogenital development. Development 121 (1995) 4057-4065
66. Turner B.E., Kambouris M.E., Sinfield L., Lange J., Burns A.M., Lourie R., Atkinson K., Hart D.N., Munster D.J., and Rice A.M. Reduced intensity conditioning for allogeneic hematopoietic stem-cell transplant determines the kinetics of acute graft-versus-host disease. Transplantation 86 7 (2008) 968-976
67. Usui J., Yamada R., Kanemoto K., Koyama A., and Nagata M. Murine metanephric mesenchyme possesses characteristics of vascular endothelial cells in vitro. Nephron. Exp. Nephrol. 102 (2006) e93-e98
68. Valerius M.T., Patterson L.T., Witte D.P., and Potter S.S. Microarray analysis of novel cell lines representing two stages of metanephric mesenchyme differentiation. Mech. Dev. 112 (2002) 219-232
69. Wachs F.P., Couillard-Despres S., Engelhardt M., Wilhelm D., Ploetz S., Vroemen M., Kaesbauer J., Uyanik G., Klucken J., Karl C., Tebbing J., Svendsen C., Weidner N., Kuhn H.G., Winkler J., and Aigner L. High efficacy of clonal growth and expansion of adult neural stem cells. Lab. Invest. 83 (2003) 949-962
70. Weiss R.H., and Maduri M. The mitogenic effect of thrombin in vascular smooth muscle cells is largely due to basic fibroblast growth factor. J. Biol. Chem. 268 (1993) 5724-5727
71. Weiss R.H., and Nuccitelli R. Inhibition of tyrosine phosphorylation prevents thrombin-induced mitogenesis, but not intracellular free calcium release, in vascular smooth muscle cells. J. Biol. Chem. 267 (1992) 5608-5613