Induction of the stem-like cell regulator CD44 by Rho kinase inhibition contributes to the maintenance of colon cancer-initiating cells

Cancer Research

Volumn 72, Issue 19, 2012, Pages 5101-5110

  Ohata, Hirokazu ^a   Ishiguro, Tatsuya ^a   Aihara, Yuki ^a   Sato, Ai ^a   Sakai, Hiroaki ^a   Sekine, Shigeki ^b   Taniguchi, Hirokazu ^b   Akasu, Takayuki ^b   Fujita, Shin ^b   Nakagama, Hitoshi ^a   Okamoto, Koji ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b NATIONAL CANCER CENTER HOSPITAL   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HERMES ANTIGEN; RHO KINASE; SCATTER FACTOR RECEPTOR; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER STEM CELL; CELL DIFFERENTIATION; COLON CANCER; COLON CARCINOGENESIS; CONTROLLED STUDY; CYTOKINESIS; DOWN REGULATION; ENZYME INHIBITION; FLOW CYTOMETRY; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPHEROID CELL; WNT SIGNALING PATHWAY;

AMIDES; ANIMALS; ANTIGENS, CD44; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; COLONIC NEOPLASMS; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; HEP G2 CELLS; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HT29 CELLS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASMS, EXPERIMENTAL; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PYRIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84867116299     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-3812     Document Type: Article

References (40)

1. Clevers H. The cancer stem cell: premises, promises and challenges. Nat Med 2011;17:313-9.
2. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science 2009;324:1670-3.
3. Visvader JE, Lindeman GJ. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 2008;8:755-68.
4. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007;445:106-10. (Pubitemid 46067310)
5. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, et al. Identification and expansion of human colon-cancer-initiating cells. Nature 2007;445:111-5. (Pubitemid 46067311)
6. Haraguchi N, Ohkuma M, Sakashita H, Matsuzaki S, Tanaka F, Mimori K, et al. CD133+CD44+ population efficiently enriches colon cancer initiating cells. Ann Surg Oncol 2008;15:2927-33.
7. Carpentino JE, Hynes MJ, Appelman HD, Zheng T, Steindler DA, Scott EW, et al. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res 2009;69:8208-15.
8. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, Appelman H, et al. Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 2009;69:3382-9.
9. Du L, Wang H, He L, Zhang J, Ni B, Wang X, et al. CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res 2008;14:6751-60.
10. Chu P, Clanton DJ, Snipas TS, Lee J, Mitchell E, Nguyen M-L, et al. Characterization of a subpopulation of colon cancer cells with stem cell-like properties. Int J Cancer 2009;124:1312-21.
11. Shmelkov SV, Butler JM, Hooper AT, Hormigo A, Kushner J, Milde T, et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133- metastatic colon cancer cells initiate tumors. J Clin Invest 2008;118:2111-20. (Pubitemid 351872330)
12. Vermeulen L, De Sousa E Melo F, van der Heijden M, Cameron K, de Jong JH, Borovski T, et al. Wnt activity de fines colon cancer stem cells and is regulated by the microenvironment. Nat Cell Biol 2010;12:468-76.
13. Dalerba P, Dylla SJ, Park IK, Liu R, Wang X, Cho RW, et al. Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci U S A 2007;104:10158-63. (Pubitemid 47175279)
14. Vermeulen L, Todaro M, de Sousa Mello F, Sprick MR, Kemper K, Perez Alea M, et al. Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc Natl Acad Sci U S A 2008;105:13427-32.
15. Todaro M, Alea MP, Di Stefano AB, Cammareri P, Vermeulen L, Iovino F, et al. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007;1:389-402. (Pubitemid 47506537)
16. Emmink BL, Van Houdt WJ, Vries RG, Hoogwater FJ, Govaert KM, Verheem A, et al. Differentiated human colorectal cancer cells protect tumor-initiating cells from irinotecan. Gastroenterology 2011;141:269-78.
17. Fang DD, Kim YJ, Lee CN, Aggarwal S, McKinnon K, Mesmer D, et al. Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br J Cancer 2010;102:1265-75.
18. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 2011;141:1762-72.
19. Chen G, Hou Z, Gulbranson DR, Thomson JA. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell Stem Cell 2010;7:240-8.
20. Ohgushi M, Matsumura M, Eiraku M, Murakami K, Aramaki T, Nishiyama A, et al. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 2010;7:225-39.
21. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 2007;25:681-6. (Pubitemid 46897207)
22. Xu Y, Zhu X, Hahm HS, Wei W, Hao E, Hayek A, et al. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci U S A 2010;107:8129-34.
23. Damoiseaux R, Sherman SP, Alva JA, Peterson C, Pyle AD. Integrated chemical genomics reveals modifiers of survival in human embryonic stem cells. Stem Cells 2009;27:533-42.
24. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA, et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 2007;39:189-98. (Pubitemid 46184349)
25. Fang D, Hawke D, Zheng Y, Xia Y, Meisenhelder J, Nika H, et al. Phosphorylation of beta-catenin by AKT promotes beta-catenin transcriptional activity. J Biol Chem 2007;282:11221-9. (Pubitemid 47100795)
26. Taurin S, Sandbo N, Qin Y, Browning D, Dulin NO. Phosphorylation of beta-catenin by cyclic AMP-dependent protein kinase. J Biol Chem 2006;281:9971-6. (Pubitemid 43864529)
27. Suda T, Takubo K, Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 2011;9:298-310.
28. Zhou Y, Shingu T, Feng L, Chen Z, Ogasawara M, Keating MJ, et al. Metabolic alterations in highly tumorigenic glioblastoma cells: preference for hypoxia and high dependency on glycolysis. J Biol Chem 2011;286:32843-53.
29. Varum S, Rodrigues AS, Moura MB, Momcilovic O, Easley CAt, Ramalho-Santos J, et al. Energy metabolism in human pluripotent stem cells and their differentiated counterparts. PLoS ONE 2011;6:e20914.
30. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50. (Pubitemid 41528093)
31. Tamada M, Nagano O, Tateyama S, Ohmura M, Yae T, Ishimoto T, et al. Modulation of glucose metabolism by CD44 contributes to antioxidant status and drug resistance in cancer cells. Cancer Res 2012;72:1438-48.
32. Zöller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 2011;11:254-67.
33. Konig H, Moll J, Ponta H, Herrlich P. Trans-acting factors regulate the expression of CD44 splice variants. EMBO J 1996;15:4030-9. (Pubitemid 26289812)
34. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 2002;16:3074-86. (Pubitemid 35424194)
35. Ishimoto T, Nagano O, Yae T, Tamada M, Motohara T, Oshima H, et al. CD44 variant regulates redox status in cancer cells by stabilizing the xct subunit of system xc- and thereby promotes tumor growth. Cancer Cell 2011;19:387-400.
36. Quintin S, Gally C, Labouesse M. Epithelial morphogenesis in embryos: asymmetries, motors and brakes. Trends Genet 2008;24:221-30.
37. Roesch A, Fukunaga-Kalabis M, Schmidt EC, Zabierowski SE, Brafford PA, Vultur A, et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 2010;141:583-94.
38. Quintana E, Shackleton M, Foster HR, Fullen DR, Sabel MS, Johnson TM, et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 2010;18:510-23.
39. Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C, et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 2011;146:633-44.
40. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, et al. Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci 2011;108:7950-5.