Side Population in Human Non-Muscle Invasive Bladder Cancer Enriches for Cancer Stem Cells That Are Maintained by MAPK Signalling

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Hepburn, Anastasia C ^a   Veeratterapillay, Rajan ^b   Williamson, Stuart C ^a   El Sherif, Amira ^c   Sahay, Neha ^a   Thomas, Huw D ^a   Mantilla, Alejandra ^a   Pickard, Robert S ^b,d   Robson, Craig N ^a   Heer, Rakesh ^a,b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b FREEMAN HOSPITAL   (United Kingdom)

^c ROYAL VICTORIA INFIRMARY   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER GROWTH; CANCER RECURRENCE; CANCER STAGING; CANCER STEM CELL; CANCER SURVIVAL; CARCINOGENESIS; COLONY FORMATION; CONTROLLED STUDY; CORRELATIONAL STUDY; ENRICHMENT CULTURE; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NON MUSCLE INVASIVE BLADDER CANCER; NONHUMAN; PHENOTYPE; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIDE POPULATION CELL; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELL LINE, TUMOR; DISEASE-FREE SURVIVAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM STAGING; NEOPLASTIC STEM CELLS; PHENOTYPE; PHOSPHOPROTEINS; RECURRENCE; SIDE-POPULATION CELLS; URINARY BLADDER NEOPLASMS;

EID: 84870591993     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050690     Document Type: Article

References (51)

1. Ploeg M, Aben KK, Kiemeney LA, (2009) The present and future burden of urinary bladder cancer in the world. World J Urol 27: 289-293.
2. SEER (2010) Surveillance, Epidemiology, and End Results (SEER) Program and the National Center for Health Statistics. Available: http://seercancergov/.
3. NIH (2010) US National Institute of Heath; National Cancer Institute: Cancer Trends Progress Report. Available: http://progressreportcancergov.
4. Sylvester RJ, van der MA, Lamm DL, (2002) Intravesical bacillus Calmette-Guerin reduces the risk of progression in patients with superficial bladder cancer: a meta-analysis of the published results of randomized clinical trials. J Urol 168: 1964-1970.
5. Shelley MD, Barber J, Mason MD (2001) Surgery versus radiotherapy for muscle invasive bladder cancer. Cochrane Database Syst Rev: CD002079.
6. Shariat SF, Karakiewicz PI, Palapattu GS, Lotan Y, Rogers CG, et al. (2006) Outcomes of radical cystectomy for transitional cell carcinoma of the bladder: a contemporary series from the Bladder Cancer Research Consortium. J Urol 176: 2414-2422.
7. Shah JB, McConkey DJ, Dinney CP, (2011) New strategies in muscle-invasive bladder cancer: on the road to personalized medicine. Clin Cancer Res 17: 2608-2612.
8. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
9. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648.
10. Vermeulen L, De Sousa EMF, van der Heijden M, Cameron K, de Jong JH, et al. (2010) Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 12: 468-476.
11. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, et al. (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445: 111-115.
12. Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, et al. (2008) Identification of cells initiating human melanomas. Nature 451: 345-349.
13. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, et al. (2006) Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66: 9339-9344.
14. Goodell MA, Brose K, Paradis G, Conner AS, Mulligan RC, (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183: 1797-1806.
15. Ho MM, Ng AV, Lam S, Hung JY, (2007) Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 67: 4827-4833.
16. Brown MD, Gilmore PE, Hart CA, Samuel JD, Ramani VA, et al. (2007) Characterization of benign and malignant prostate epithelial Hoechst 33342 side populations. Prostate 67: 1384-1396.
17. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, et al. (2009) PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 4: 226-235.
18. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, et al. (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 65: 6207-6219.
19. Oates JE, Grey BR, Addla SK, Samuel JD, Hart CA, et al. (2009) Hoechst 33342 side population identification is a conserved and unified mechanism in urological cancers. Stem Cells Dev 18: 1515-1522.
20. Knowles MA, (2008) Molecular pathogenesis of bladder cancer. Int J Clin Oncol 13: 287-297.
21. Dinney CP, McConkey DJ, Millikan RE, Wu X, Bar-Eli M, et al. (2004) Focus on bladder cancer. Cancer Cell 6: 111-116.
22. Kassouf W, Dinney CP, Brown G, McConkey DJ, Diehl AJ, et al. (2005) Uncoupling between epidermal growth factor receptor and downstream signals defines resistance to the antiproliferative effect of Gefitinib in bladder cancer cells. Cancer Res 65: 10524-10535.
23. van Rhijn BW, Lurkin I, Radvanyi F, Kirkels WJ, van der Kwast TH, et al. (2001) The fibroblast growth factor receptor 3 (FGFR3) mutation is a strong indicator of superficial bladder cancer with low recurrence rate. Cancer Res 61: 1265-1268.
24. Kassouf W, Black PC, Tuziak T, Bondaruk J, Lee S, et al. (2008) Distinctive expression pattern of ErbB family receptors signifies an aggressive variant of bladder cancer. J Urol 179: 353-358.
25. Forster JA, Paul AB, Harnden P, Knowles MA, (2011) Expression of NRG1 and its receptors in human bladder cancer. Br J Cancer 104: 1135-1143.
26. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, et al. (2001) The ABC transporter 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.
27. Imai Y, Ohmori K, Yasuda S, Wada M, Suzuki T, et al. (2009) Breast cancer resistance protein/ABCG2 is differentially regulated downstream of extracellular signal-regulated kinase. Cancer Sci 100: 1118-1127.
28. Dinney CP, Fishbeck R, Singh RK, Eve B, Pathak S, et al. (1995) Isolation and characterization of metastatic variants from human transitional cell carcinoma passaged by orthotopic implantation in athymic nude mice. J Urol 154: 1532-1538.
29. Golebiewska A, Brons NH, Bjerkvig R, Niclou SP, (2011) Critical appraisal of the side population assay in stem cell and cancer stem cell research. Cell Stem Cell 8: 136-147.
30. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, et al. (2008) An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507.
31. Camargo FD, Chambers SM, Drew E, McNagny KM, Goodell MA, (2006) Hematopoietic stem cells do not engraft with absolute efficiencies. Blood 107: 501-507.
32. Shin K, Lee J, Guo N, Kim J, Lim A, et al. (2011) Hedgehog/Wnt feedback supports regenerative proliferation of epithelial stem cells in bladder. Nature 472: 110-114.
33. Bentivegna A, Conconi D, Panzeri E, Sala E, Bovo G, et al. (2010) Biological heterogeneity of putative bladder cancer stem-like cell populations from human bladder transitional cell carcinoma samples. Cancer Sci 101: 416-424.
34. Chan KS, Espinosa I, Chao M, Wong D, Ailles L, et al. (2009) Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci U S A 106: 14016-14021.
35. He X, Marchionni L, Hansel DE, Yu W, Sood A, et al. (2009) Differentiation of a highly tumorigenic basal cell compartment in urothelial carcinoma. Stem Cells 27: 1487-1495.
36. Clifford SC, Neal DE, Lunec J, (1996) High level expression of the multidrug resistance (MDR1) gene in the normal bladder urothelium: a potential involvement in protection against carcinogens? Carcinogenesis 17: 601-604.
37. Falso MJ, Buchholz BA, White RW, (2012) Stem-like cells in bladder cancer cell lines with differential sensitivity to cisplatin. Anticancer Res 32: 733-738.
38. Volkmer JP, Sahoo D, Chin RK, Ho PL, Tang C, et al. (2012) Three differentiation states risk-stratify bladder cancer into distinct subtypes. Proc Natl Acad Sci U S A 109: 2078-2083.
39. Zhang Y, Wang Z, Yu J, Shi J, Wang C, et al. (2012) Cancer stem-like cells contribute to cisplatin resistance and progression in bladder cancer. Cancer Lett 322: 70-77.
40. Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL, et al. (2006) Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J Cell Physiol 209: 883-893.
41. Zhang X, Neganova I, Przyborski S, Yang C, Cooke M, et al. (2009) A role for NANOG in G1 to S transition in human embryonic stem cells through direct binding of CDK6 and CDC25A. J Cell Biol 184: 67-82.
42. Tabu K, Kimura T, Sasai K, Wang L, Bizen N, et al. (2010) Analysis of an alternative human CD133 promoter reveals the implication of Ras/ERK pathway in tumor stem-like hallmarks. Mol Cancer 9: 39.
43. Tsuchida R, Das B, Yeger H, Koren G, Shibuya M, et al. (2008) Cisplatin treatment increases survival and expansion of a highly tumorigenic side-population fraction by upregulating VEGF/Flt1 autocrine signaling. Oncogene 27: 3923-3934.
44. Karlou M, Saetta AA, Korkolopoulou P, Levidou G, Papanastasiou P, et al. (2009) Activation of extracellular regulated kinases (ERK1/2) predicts poor prognosis in urothelial bladder carcinoma and is not associated with B-Raf gene mutations. Pathology 41: 327-334.
45. Sunayama J, Matsuda K, Sato A, Tachibana K, Suzuki K, et al. (2010) Crosstalk between the PI3K/mTOR and MEK/ERK pathways involved in the maintenance of self-renewal and tumorigenicity of glioblastoma stem-like cells. Stem Cells 28: 1930-1939.
46. Wang YK, Zhu YL, Qiu FM, Zhang T, Chen ZG, et al. (2010) Activation of Akt and MAPK pathways enhances the tumorigenicity of CD133+ primary colon cancer cells. Carcinogenesis 31: 1376-1380.
47. Dubrovska A, Elliott J, Salamone RJ, Kim S, Aimone LJ, et al. (2010) Combination therapy targeting both tumor-initiating and differentiated cell populations in prostate carcinoma. Clin Cancer Res 16: 5692-5702.
48. Gupta PB, Onder TT, Jiang G, Tao K, Kuperwasser C, et al. (2009) Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
49. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, et al. (2006) Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441: 475-482.
50. Yeh TC, Marsh V, Bernat BA, Ballard J, Colwell H, et al. (2007) Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogen-activated protein kinase kinase 1/2 inhibitor. Clin Cancer Res 13: 1576-1583.
51. Pruthi RS, Nielsen M, Heathcote S, Wallen EM, Rathmell WK, et al. (2010) A phase II trial of neoadjuvant erlotinib in patients with muscle-invasive bladder cancer undergoing radical cystectomy: clinical and pathological results. BJU Int 106: 349-354.