PKHhigh cells within clonal human nephrospheres provide a purified adult renal stem cell population

Stem Cell Research

Volumn 11, Issue 3, 2013, Pages 1163-1177

  Bombelli, Silvia ^a   Zipeto, Maria Anna ^a   Torsello, Barbara ^a   Bovo, Giorgio ^b   Di Stefano, Vitalba ^a   Bugarin, Cristina ^b   Zordan, Paola ^c   Viganò, Paolo ^d   Cattoretti, Giorgio ^b   Strada, Guido ^d   Bianchi, Cristina ^a   Perego, Roberto A ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b SAN GERARDO HOSPITAL   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d Urology Division   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; CALBINDIN; CD133 ANTIGEN; CD24 ANTIGEN; CYTOKERATIN; FIBROCYSTIN; MICROSOMAL AMINOPEPTIDASE; NERVE CELL ADHESION MOLECULE; NESTIN; PODOCIN; SYNAPTOPODIN; UVOMORULIN; VON WILLEBRAND FACTOR;

ADULT; ADULT STEM CELL; ARTICLE; CELL ACTIVATION; CELL ASSAY; CELL CULTURE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL ISOLATION; CELL MATURATION; CELL POPULATION; CELL RENEWAL; CELL SUSPENSION; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IN VITRO STUDY; KIDNEY CELL; KIDNEY PARENCHYMA; PHENOTYPE; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROGENY;

ADULT STEM CELLS; ANIMALS; ANTIGENS, CD; ANTIGENS, CD24; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; FLUORESCENT DYES; GLYCOPROTEINS; HUMANS; KIDNEY; MICE; MICE, NUDE; ORGANIC CHEMICALS; PEPTIDES; PHENOTYPE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84883641029     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2013.08.004     Document Type: Article

References (45)

1. Alison M.R., Islam S. Attributes of adult stem cells. J. Pathol. 2009, 217(2):144-160.
2. Armstrong L., Stojkovic M., Dimmick I., Ahmad S., Stojkovic P., Hole N., et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 2004, 22(7):1142-1151.
3. Baer P.C., Nockher W.A., Haase W., Scherberich J.E. Isolation of proximal and distal tubule cells from human kidney by immunomagnetic separation. Kidney Int. 1997, 52(5):1321-1331.
4. Barker N., Rookmaaker M.B., Kujala P., Ng A., Leushacke M., Snippert H., van de Wetering M., et al. Lgr5(+ve) stem/progenitor cells contribute to nephron formation during kidney development. Cell Rep. 2012, 2(3):540-552.
5. Bianchi C., Bombelli S., Raimondo F., Torsello B., Angeloni V., Ferrero S., et al. Primary cell cultures from human renal cortex and renal-cell carcinoma evidence a differential expression of two spliced isoforms of Annexin A3. Am. J. Pathol. 2010, 176(4):1660-1670.
6. Blanpain C., Horsley V., Fuchs E. Epithelial stem cells: turning over new leaves. Cell 2007, 128(3):445-458.
7. Bussolati B., Bruno S., Grange C., Buttiglieri S., Deregibus M.C., Cantino D., et al. Isolation of renal progenitor cells from adult human kidney. Am. J. Pathol. 2005, 166(2):545-555.
8. Bussolati B., Moggio A., Collino F., Aghemo G., D'Armento G., Grange C., et al. Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors through Oct4/miR-145 balance. Am. J. Renal Physiol. 2012, 302(1):F116-F128.
9. Buzhor E., Hararri-Steinberg O., Omer D., Metsuyanim S., Jacob-Hirsch J., Noiman T., et al. Kidney spheroids recapitulate tubular organoids leading to enhanced tubulogenic potency of human kidney-derived cells. Tissue Eng. Part A 2011, 17(17-18):2305-2319.
10. Corti S., Locatelli F., Papadimitriou D., Donadoni C., Salani S., Del Bo R., et al. Identification of a primitive brain-derived neural stem cell population based on aldheyde dehydrogenase activity. Stem Cells 2006, 24(4):975-985.
11. Cicalese A., Bonizzi G., Pasi C., Faretta M., Ronzoni S., Giulini B., et al. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 2009, 138(6):1083-1095.
12. Dontu G., Abdallah W.M., Foley J.M., Jackson K.W., Clarke M.F., Kawamura M.J., et al. In vitro propagation and trascriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003, 17(10):1253-1270.
13. Eirew P., Stingl J., Raouf A., Turashvili G., Aparicio S., Emerman J.T., et al. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat. Med. 2008, 14(12):1384-1389.
14. Forino M., Torregrossa R., Ceol M., Murer L., Delle Vella M., Del Prete D., et al. TGFbeta1 induces epithelial-mesenchymal transition, but not myofibroblast transdifferentiation of human kidney tubular epithelial cells in primary culture. Int. J. Exp. Pathol. 2006, 87(3):197-208.
15. Fortini M.E. Notch signalling: the core pathway and its posttraslational regulation. Dev. Cell 2009, 16(5):633-647.
16. Hemmingsen C. Regulation of renal calbindin-D28K. Pharmacol. Toxicol. 2000, 87(Suppl. 3):5-30.
17. Hsu Y.C., Fuchs E. A family business: stem cell progeny join the niche to regulate homeostasis. Nat. Rev. Mol. Cell Biol. 2012, 13(2):103-114.
18. Jessberger S., Clemenson G.D., Gage F.H. Spontaneous fusion and nonclonal growth of adult neural stem cells. Stem Cells 2007, 25(4):871-874.
19. Keller C., Kroening S., Zuehlke J., Kunath F., Krueger B., Goppelt-Struebe M. Distinct mesenchymal alterations in N-cadherin and E-cadherin positive primary renal epithelial cells. PLoS One 2012, 7(8):e43584.
20. Lan X., Wu X.Z., Wang Y., Wu F.R., Zang C.B., Tang C., et al. CD133 silencing inhibits stemness properties and enhances chemoradiosensitivity in CD133-positive liver cancer stem cells. Int. J. Mol. Med. 2013, 31(2):315-324.
21. Lasagni L., Ballerini L., Angelotti M.L., Parente E., Sagrinati C., Mazzinghi B., et al. Notch activation differentially regulates renal progenitors proliferation and differentiation toward the podocyte lineage in glomerular disorders. Stem Cells 2010, 28(9):1674-1685.
22. Lawson D.A., Xin L., Lukacs R.U., Cheng D., Witte O.N. Isolation and functional characterization of murine prostate stem cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(1):181-186.
23. Li Z. CD133: a stem cell biomarker and beyond. Exp. Hematol. Oncol. 2013, 2(1):17.
24. Lindgren D., Bostrom A.K., Nilsson K., Hansson J., Sjolund J., Moller C., et al. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am. J. Pathol. 2011, 178(2):828-837.
25. Lusis M., Li J., Ineson J., Christensen M.E., Rice A., Little M.H. Isolation of clonogenic, long-term self renewing embryonic renal stem cells. Stem Cell Res. 2010, 5(1):23-39.
26. McCampbell K.K., Wingert R.A. Renal stem cells: fact or science fiction?. Biochem. J. 2012, 444(2):153-168.
27. McCright B. Notch signaling in kidney development. Curr. Opin. Nephrol. Hypertens. 2003, 12(1):5-10.
28. Mizutani K., Yoon K., Dang L., Tokunaga A., Gaiano N. Differential Notch signaling distinguishes neural stem cells from intermediate progenitors. Nature 2007, 449(7160):351-355.
29. Nouwen E.J., Dauwe S., van der Biest I., De Broe M.E. Stage- and segment-specific expression of cell-adhesion molecole N-CAM, A-CAM, and L-CAM in the kidney. Kidney Int. 1993, 44(1):47-58.
30. Pece S., Tosoni D., Confalonieri S., Mazzarol G., Vecchi M., Ronzoni S., et al. Biological and molecular heterogeneity of breast cancers carrelates with their cancer stem cell content. Cell 2010, 140(1):62-73.
31. Perego R.A., Corizzato M., Bianchi C., Eroini B., Bosari S. N- and C-terminal isoforms of arg quantified by real-time PCR are specifically espressed in human normal and neoplastic cells, in neoplastic cell lines, and in HL-60 cell differentiation. Mol. Carcinog. 2005, 42(4):229-239.
32. Perego R.A., Bianchi C., Corizzato M., Eroini B., Torsello B., Valsecchi C., et al. Primary cell cultures arising from normal kidney and renal cell carcinoma retain the proteomic profile of corresponding tissues. J. Proteome Res. 2005, 4(5):1503-1510.
33. Prozialeck W.C., Lamar P.C., Appelt D.M. Differential expression of E-cadherin, N-cadherin and beta-catenin in proximal and distal segments of the rat nephron. BMC Physiol. 2004, 4:10.
34. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255(5052):1707-1710.
35. Rovira M., Scott S.G., Liss A.S., Jensen J., Thayer S.P., Leach S.D. Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(1):75-80.
36. Sallustio F., Serino G., Costantino V., Curci C., Cox S.N., De Palma G., et al. miR-1915 and miR-1225-5p regulate the expression of CD133, PAX2 and TRL2 in adult renal progenitor cells. PLoS One 2013, 8(7):e68296.
37. Sagrinati C., Netti G.S., Mazzinghi B., Lazzeri E., Liotta F., Frosali F., et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J. Am. Soc. Nephrol. 2006, 17(9):2443-2456.
38. Sato T., Van H.S., Sato T., van Es J.H., Snippert H.J., Stange D.E., et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 2011, 469(7330):415-418.
39. Sharma S., Sirin Y., Susztak K. The story of Notch ancd chronic kidney disease. Curr. Opin. Nephrol. Hypertens. 2011, 20(1):56-61.
40. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., et al. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Methods 2006, 3(10):801-806.
41. Sirin Y., Susztak K. Notch in the kidney: development and disease. J. Pathol. 2012, 226(2):394-403.
42. Snippert H.J., Clevers H. Tracking adult stem cells. EMBO Rep. 2011, 12(2):113-122.
43. Surendran K., Boyle S., Barak H., Kim M., Stomberski C., McCright B., et al. The contibution of Notch1 to nephron segmentation in the developing kidney is revealed in a sensitized Notch2 background and can be augmented by reducing Mint dosage. Dev. Biol. 2010, 337(2):386-395.
44. Terskikh V.V., Vasilev A.V., Vorotelyak E.A. Label retaining cells and cutaneous stem cells. Stem Cell Rev. Rep. 2012, 8(2):414-425.
45. Zhao X., Malhotra G.K., Band H., Band V. Derivation of myoepithelial progenitor cells from bipotent mammary stem/progenitor cells. PLoS One 2012, 7(4):e35338.