The isolation and characterization of renal cancer initiating cells from human Wilms' tumour xenografts unveils new therapeutic targets

EMBO Molecular Medicine

Volumn 5, Issue 1, 2013, Pages 18-37

  Pode Shakked, Naomi ^a,b   Shukrun, Rachel ^a,b   Mark Danieli, Michal ^a   Tsvetkov, Peter ^c   Bahar, Sarit ^a,b   Pri Chen, Sara ^a   Goldstein, Ronald S ^d   Rom Gross, Eithan ^e   Mor, Yoram ^a,b   Fridman, Edward ^a,b   Meir, Karen ^e   Simon, Amos ^a   Magister, Marcus ^f   Kaminski, Naftali ^f   Goldmacher, Victor S ^g   Harari Steinberg, Orit ^a   Dekel, Benjamin ^a,b  

^a SHEBA MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d BAR ILAN UNIVERSITY   (Israel)

^e HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g IMMUNOGEN INC   (United States)

Author keywords

Cancer initiating cells; Cancer stem cells; Kidney stem cells; Renal progenitor cells; Targeted therapy

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD133 ANTIGEN; LORVOTUZUMAB MERTANSINE; MICRORNA 200; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; DRUG CONJUGATION; DRUG MEGADOSE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LOW DRUG DOSE; MOUSE; NEPHROBLASTOMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR XENOGRAFT;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD56; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; GENE EXPRESSION; GLYCOPROTEINS; HUMANS; KIDNEY NEOPLASMS; MAYTANSINE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; PEPTIDES; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY; WILMS TUMOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84871940855     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201201516     Document Type: Article

References (76)

1. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983- 3988
2. Armstrong L, Stojkovic M, Dimmick I, Ahmad S, Stojkovic P, Hole N, Lako M (2004) Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 22: 1142- 1151
3. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730- 737
4. Campbell AD, Cohn SL, Reynolds M, Seshadri R, Morgan E, Geissler G, Rademaker A, Marymount M, Kalapurakal J, Haut PR, et al (2004) Treatment of relapsed Wilms' tumor with high-dose therapy and autologous hematopoietic stem-cell rescue: the experience at Children's Memorial Hospital. J Clin Oncol 22: 2885- 2890
5. Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J, Jr., Chang HY, van de Rijn M, et al (2009) Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci USA 106: 14016- 14021
6. Chen YC, Chen YW, Hsu HS, Tseng LM, Huang PI, Lu KH, Chen DT, Tai LK, Yung MC, Chang SC, et al (2009) Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem Biophys Res Commun 385: 307- 313
7. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM (2006) Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339- 9344
8. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946- 10951
9. Dekel B, Metsuyanim S, Schmidt-Ott KM, Fridman E, Jacob-Hirsch J, Simon A, Pinthus J, Mor Y, Barasch J, Amariglio N, et al (2006) Multiple imprinted and stemness genes provide a link between normal and tumor progenitor cells of the developing human kidney. Cancer Res 66: 6040- 6049
10. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L, Pickell K, Aguilar J, Lazetic S, Smith-Berdan S, et al (2008) Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS ONE 3: e2428
11. Evseenko D, Zhu Y, Schenke-Layland K, Kuo J, Latour B, Ge S, Scholes J, Dravid G, Li X, MacLellan WR, et al (2010) Mapping the first stages of mesoderm commitment during differentiation of human embryonic stem cells. Proc Natl Acad Sci USA 107: 13742- 13747
12. Geenen MM, Cardous-Ubbink MC, Kremer LC, van den Bos C, van der Pal HJ, Heinen RC, Jaspers MW, Koning CC, Oldenburger F, Langeveld NE, et al (2007) Medical assessment of adverse health outcomes in long-term survivors of childhood cancer. JAMA 297: 2705- 2715
13. Gillespie GKFaGY (2011) Cancer stem cells and pediatric solid tumors. Cancers 298- 318
14. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555- 567
15. Green DM, Beckwith JB, Breslow NE, Faria P, Moksness J, Finklestein JZ, Grundy P, Thomas PR, Kim T, Shochat S, et al (1994) Treatment of children with stages II to IV anaplastic Wilms' tumor: a report from the National Wilms' Tumor Study Group. J Clin Oncol 12: 2126- 2131
16. Green DM, Breslow NE, Evans I, Moksness J, D'Angio GJ (1996) Treatment of children with stage IV favorable histology Wilms tumor: a report from the National Wilms Tumor Study Group. Med Pediatr Oncol 26: 147- 152
17. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, Farshid G, Vadas MA, Khew-Goodall Y, Goodall GJ (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10: 593- 601
18. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, Larue L (2003) The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 63: 2172- 2178
19. Hu Q, Gao F, Tian W, Ruteshouser EC, Wang Y, Lazar A, Stewart J, Strong LC, Behringer RR, Huff V (2011) Wt1 ablation and Igf2 upregulation in mice result in Wilms tumors with elevated ERK1/2 phosphorylation. J Clin Invest 121: 174- 183
20. Iliopoulos D, Lindahl-Allen M, Polytarchou C, Hirsch HA, Tsichlis PN, Struhl K (2010) Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761- 772
21. Iliopoulos D, Polytarchou C, Hatziapostolou M, Kottakis F, Maroulakou IG, Struhl K, Tsichlis PN (2009) MicroRNAs differentially regulated by Akt isoforms control EMT and stem cell renewal in cancer cells. Sci Signal 2: ra62
22. James RG, Kamei CN, Wang Q, Jiang R, Schultheiss TM (2006) Odd-skipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development 133: 2995- 3004
23. Jensen M, Berthold F (2007) Targeting the neural cell adhesion molecule in cancer. Cancer Lett 258: 9- 21
24. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE (2006) Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167- 1174
25. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP (2009) Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Stem Cells Dev 18: 1093- 1108
26. Kaste SC, Dome JS, Babyn PS, Graf NM, Grundy P, Godzinski J, Levitt GA, Jenkinson H (2008) Wilms tumour: prognostic factors, staging, therapy and late effects. Pediatr Radiol 38: 2- 17
27. Kobayashi A, Valerius MT, Mugford JW, Carroll TJ, Self M, Oliver G, McMahon AP (2008) Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3: 169- 181
28. Kong D, Banerjee S, Ahmad A, Li Y, Wang Z, Sethi S, Sarkar FH (2011) Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS ONE 5: e12445
29. Kozaki K, Imoto I, Mogi S, Omura K, Inazawa J (2008) Exploration of tumor-suppressive microRNAs silenced by DNA hypermethylation in oral cancer. Cancer Res 68: 2094- 2105
30. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645- 648
31. Li F, Tiede B, Massague J, Kang Y (2007) Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res 17: 3- 14
32. Li Y, VandenBoom TG, II, Kong D, Wang Z, Ali S, Philip PA, Sarkar FH (2009) Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res 69: 6704- 6712
33. Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, Guan XY (2008) Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res 6: 1146- 1153
34. Maiti S, Alam R, Amos CI, Huff V (2000) Frequent association of beta-catenin and WT1 mutations in Wilms tumors. Cancer Res 60: 6288- 6292
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704- 715
36. Martelli AM, Evangelisti C, Chiarini F, Grimaldi C, Cappellini A, Ognibene A, McCubrey JA (2010) The emerging role of the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin signaling network in normal myelopoiesis and leukemogenesis. Biochim Biophys Acta 1803: 991- 1002
37. Metsuyanim S, Harari-Steinberg O, Buzhor E, Omer D, Pode-Shakked N, Ben-Hur H, Halperin R, Schneider D, Dekel B (2009) Expression of stem cell markers in the human fetal kidney. PLoS ONE 4: e6709
38. Metsuyanim S, Pode-Shakked N, Schmidt-Ott KM, Keshet G, Rechavi G, Blumental D, Dekel B (2008) Accumulation of malignant renal stem cells is associated with epigenetic changes in normal renal progenitor genes. Stem Cells 26: 1808- 1817
39. Monticone M, Biollo E, Fabiano A, Fabbi M, Daga A, Romeo F, Maffei M, Melotti A, Giaretti W, Corte G, et al (2009) z-Leucinyl-leucinyl-norleucinal induces apoptosis of human glioblastoma tumor-initiating cells by proteasome inhibition and mitotic arrest response. Mol Cancer Res 7: 1822- 1834
40. Moss TJ, Strauss LC, Das L, Feig SA (1989) Secondary leukemia following successful treatment of Wilms' tumor. Am J Pediatr Hematol Oncol 11: 158- 161
41. Mugford JW, Sipila P, McMahon JA, McMahon AP (2008) Osr1 expression demarcates a multi-potent population of intermediate mesoderm that undergoes progressive restriction to an Osr1-dependent nephron progenitor compartment within the mammalian kidney. Dev Biol 324: 88- 98
42. Naor D, Sionov RV, Ish-Shalom D (1997) CD44: structure, function, and association with the malignant process. Adv Cancer Res 71: 241- 319
43. O'Brien CA, Pollett A, Gallinger S, Dick JE (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445: 106- 110
44. Oliver JA, Barasch J, Yang J, Herzlinger D, Al-Awqati Q (2002) Metanephric mesenchyme contains embryonic renal stem cells. Am J Physiol Renal Physiol 283: F799- F809
45. Ovcharenko D, Kelnar K, Johnson C, Leng N, Brown D (2007) Genome-scale microRNA and small interfering RNA screens identify small RNA modulators of TRAIL-induced apoptosis pathway. Cancer Res 67: 10782- 10788
46. Paterson EL, Kolesnikoff N, Gregory PA, Bert AG, Khew-Goodall Y, Goodall GJ (2008) The microRNA-200 family regulates epithelial to mesenchymal transition. Sci World J 8: 901- 904
47. Pearce DJ, Taussig D, Simpson C, Allen K, Rohatiner AZ, Lister TA, Bonnet D (2005) Characterization of cells with a high aldehyde dehydrogenase activity from cord blood and acute myeloid leukemia samples. Stem Cells 23: 752- 760
48. Peter ME (2009) Let-7 and miR-200 microRNAs: guardians against pluripotency and cancer progression. Cell Cycle 8: 843- 852
49. Pinkerton CR, Groot-Loonen JJ, Morris-Jones PH, Pritchard J (1991) Response rates in relapsed Wilms' tumor. A need for new effective agents. Cancer 67: 567- 571
50. Pode-Shakked N, Metsuyanim S, Rom-Gross E, Mor Y, Fridman E, Goldstein I, Amariglio N, Rechavi G, Keshet G, Dekel B (2009) Developmental tumourigenesis: NCAM as a putative marker for the malignant renal stem/progenitor cell population. J Cell Mol Med 13: 1792- 1808
51. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ (2008) Efficient tumour formation by single human melanoma cells. Nature 456: 593- 598
52. Reinhard H, Schmidt A, Furtwangler R, Leuschner I, Rube C, Von Schweinitz D, Zoubek A, Niggli F, Graf N (2008) Outcome of relapses of nephroblastoma in patients registered in the SIOP/GPOH trials and studies. Oncology Rep 20: 463- 467
53. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414: 105- 111
54. Ricart AD (2011) Immunoconjugates against solid tumors: mind the gap. Clin Pharmacol Ther 89: 513- 523
55. Rivera MN, Haber DA (2005) Wilms' tumour: connecting tumorigenesis and organ development in the kidney. Nat Rev 5: 699- 712
56. Rivera MN, Kim WJ, Wells J, Driscoll DR, Brannigan BW, Han M, Kim JC, Feinberg AP, Gerald WL, Vargas SO, et al (2007) An X chromosome gene, WTX, is commonly inactivated in Wilms tumor. Science (New York, NY) 315: 642- 645
57. Ronconi E, Sagrinati C, Angelotti ML, Lazzeri E, Mazzinghi B, Ballerini L, Parente E, Becherucci F, Gacci M, Carini M, et al (2009) Regeneration of glomerular podocytes by human renal progenitors. J Am Soc Nephrol 20: 322- 332
58. Roth J, Blaha I, Bitter-Suermann D, Heitz PU (1988a) Blastemal cells of nephroblastomatosis complex share an onco-developmental antigen with embryonic kidney and Wilms' tumor. An immunohistochemical study on polysialic acid distribution. Am J Pathol 133: 596- 608
59. Roth J, Zuber C, Wagner P, Blaha I, Bitter-Suermann D, Heitz PU (1988b) Presence of the long chain form of polysialic acid of the neural cell adhesion molecule in Wilms' tumor. Identification of a cell adhesion molecule as an oncodevelopmental antigen and implications for tumor histogenesis. Am J Pathol 133: 227- 240
60. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, et al (2008) Identification of cells initiating human melanomas. Nature 451: 345- 349
61. Schmelzer E, Wauthier E, Reid LM (2006) The phenotypes of pluripotent human hepatic progenitors. Stem Cells 24: 1852- 1858
62. Schnabel CA, Godin RE, Cleary ML (2003) Pbx1 regulates nephrogenesis and ureteric branching in the developing kidney. Dev Biol 254: 262- 276
63. Self M, Lagutin OV, Bowling B, Hendrix J, Cai Y, Dressler GR, Oliver G (2006) Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney. EMBO J 25: 5214- 5228
64. Silva IA, Bai S, McLean K, Yang K, Griffith K, Thomas D, Ginestier C, Johnston C, Kueck A, Reynolds RK, et al (2011) Aldehyde dehydrogenase in combination with CD133 defines angiogenic ovarian cancer stem cells that portend poor patient survival. Cancer Res 71: 3991- 4001
65. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821- 5828
66. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432: 396- 401
67. Sparano JA, Beckwith JB, Mitsudo S, Wiernik PH (1991) Complete remission in refractory anaplastic adult Wilms' tumor treated with cisplatin and etoposide. Cancer 67: 956- 959
68. Takahashi M, Yang YX, Lavery TT, Furge KA, Williams BO, Tretiakova M, Montag A, Vogelzang NJ, Re GG, Garvin AJ, Söderhäll S, Kagawa S, Hazel-Martin D, Nordenskjold A, Teh BT (2002) Gene expression profiling of favorable histology Wilms' tumors and its correlation with clinical features. Cancer Res 62: 6598- 6605
69. Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, Tamaki Y, Noguchi S (2009) Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 15: 4234- 4241
70. Thomas S, Thomas M, Wincker P, Babarit C, Xu P, Speer MC, Munnich A, Lyonnet S, Vekemans M, Etchevers HC (2008) Human neural crest cells display molecular and phenotypic hallmarks of stem cells. Hum Mol Genet 17: 3411- 3425
71. Tsokos M, Scarpa S, Ross RA, Triche TJ (1987) Differentiation of human neuroblastoma recapitulates neural crest development. Study of morphology, neurotransmitter enzymes, and extracellular matrix proteins. Am J Pathol 128: 484- 496
72. Vane D, King DR, Boles ET Jr., (1984) Secondary thyroid neoplasms in pediatric cancer patients: increased risk with improved survival. J Pediatr Surg 19: 855- 860
73. Wang FE, Zhang C, Maminishkis A, Dong L, Zhi C, Li R, Zhao J, Majerciak V, Gaur AB, Chen S, et al (2010) MicroRNA-204/211 alters epithelial physiology. FASEB J 24: 1552- 1571
74. Wang X, Luo H, Chen H, Duguid W, Wu J (1998) Role of proteasomes in T cell activation and proliferation. J Immunol 160: 788- 801
75. Wen JG, van Steenbrugge GJ, Egeler RM, Nijman RM (1997) Progress of fundamental research in Wilms' tumor. Urol Res 25: 223- 230
76. Wittmann S, Wunder C, Zirn B, Furtwangler R, Wegert J, Graf N, Gessler M (2008) New prognostic markers revealed by evaluation of genes correlated with clinical parameters in Wilms tumors. Genes Chromosomes Cancer 47: 386- 395