Regulation of the stem cell marker CD133 is independent of promoter hypermethylation in human epithelial differentiation and cancer

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Pellacani, Davide ^a   Packer, Richard J ^a   Frame, Fiona M ^a   Oldridge, Emma E ^a   Berry, Paul A ^a   Labarthe, Marie Christine ^b   Stower, Michael J ^c   Simms, Matthew S ^d   Collins, Anne T ^a   Maitland, Norman J ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b Pro Cure Therapeutics Ltd   (United Kingdom)

^c YORK HOSPITAL   (United Kingdom)

^d CASTLE HILL HOSPITAL   (United Kingdom)

Author keywords

Cancer stem cells; CD133; DNA methylation; Epigenetic regulation of gene expression; Prostate cancer

Indexed keywords

CD133 ANTIGEN; HISTONE DEACETYLASE INHIBITOR; MESSENGER RNA; VERY LATE ACTIVATION ANTIGEN 2; BIOLOGICAL MARKER; GLYCOPROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; GENE CONTROL; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NEOPLASM; NONHUMAN; PROSTATE CANCER; PROSTATE EPITHELIUM; PROSTATE HYPERTROPHY; PYROSEQUENCING; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL; ADULT STEM CELL; ANIMAL; BAGG ALBINO MOUSE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; PROMOTER REGION; PROSTATE TUMOR; TRANSGENIC MOUSE; TUMOR CELL LINE; XENOGRAFT;

ADULT STEM CELLS; ANIMALS; ANTIGENS, CD; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE, TUMOR; DNA METHYLATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICE, TRANSGENIC; NEOPLASMS; PEPTIDES; PROMOTER REGIONS, GENETIC; PROSTATIC HYPERPLASIA; PROSTATIC NEOPLASMS; TRANSPLANTATION, HETEROLOGOUS;

EID: 79960879894     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-94     Document Type: Article

References (48)

1. Li X, Zhao X. Epigenetic regulation of mammalian stem cells. Stem Cells Dev 2008, 17:1043-1052. 10.1089/scd.2008.0036, 2700624, 18393635.
2. Hsieh J, Gage FH. Epigenetic control of neural stem cell fate. Curr Opin Genet Dev 2004, 14:461-469. 10.1016/j.gde.2004.07.006, 15380235.
3. Xi R, Xie T. Stem cell self-renewal controlled by chromatin remodeling factors. Science 2005, 310:1487-1489. 10.1126/science.1120140, 16322456.
4. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, Sivachenko A, Zhang X, Bernstein BE, Nusbaum C, Jaffe DB, Gnirke A, Jaenisch R, Lander ES. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 2008, 454:766-770. 2896277, 18600261.
5. Bröske AM, Vockentanz L, Kharazi S, Huska MR, Mancini E, Scheller M, Kuhl C, Enns A, Prinz M, Jaenisch R, Nerlov C, Leutz A, Andrade-Navarro MA, Jacobsen SEW, Rosenbauer F. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nature Genetics 2009, 41:1207-1215. 10.1038/ng.463, 19801979.
6. Miller SJ, Lavker RM, Sun TT. Interpreting epithelial cancer biology in the context of stem cells: tumor properties and therapeutic implications. Biochim Biophys Acta 2005, 1756:25-52.
7. Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, Olweus J, Kearney J, Buck DW. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997, 90:5002-5012.
8. Shmelkov SV, St Clair R, Lyden D, Rafii S. AC133/CD133/Prominin-1. Int J Biochem Cell Biol 2005, 37:715-719. 10.1016/j.biocel.2004.08.010, 15694831.
9. Richardson GD, Robson CN, Lang SH, Neal DE, Maitland NJ, Collins AT. CD133, a novel marker for human prostatic epithelial stem cells. J Cell Sci 2004, 117:3539-3545. 10.1242/jcs.01222, 15226377.
10. Collins AT, Habib FK, Maitland NJ, Neal DE. Identification and isolation of human prostate epithelial stem cells based on alpha(2)beta(1)-integrin expression. J Cell Sci 2001, 114:3865-3872.
11. Hudson DL, Masters JR. Prostate epithelial stem cell isolation and culture. Methods Mol Med 2003, 81:59-67.
12. Lawson DA, Xin L, Lukacs RU, Cheng D, Witte ON. Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci USA 2007, 104:181-186. 10.1073/pnas.0609684104, 1716155, 17185413.
13. Leong KG, Wang BE, Johnson L, Gao WQ. Generation of a prostate from a single adult stem cell. Nature 2008, 456:804-808. 10.1038/nature07427, 18946470.
14. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005, 65:10946-10951. 10.1158/0008-5472.CAN-05-2018, 16322242.
15. Schulz WA, Hatina J. Epigenetics of prostate cancer: beyond DNA methylation. J Cell Mol Med 2006, 10:100-125. 10.1111/j.1582-4934.2006.tb00293.x, 16563224.
16. Nakayama M, Gonzalgo ML, Yegnasubramanian S, Lin X, De Marzo AM, Nelson WG. GSTP1 CpG island hypermethylation as a molecular biomarker for prostate cancer. J Cell Biochem 2004, 91:540-552. 10.1002/jcb.10740, 14755684.
17. Baylin SB, Ohm JE. Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction?. Nat Rev Cancer 2006, 6:107-116. 10.1038/nrc1799, 16491070.
18. Feinberg AP, Ohlsson R, Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet 2006, 7:21-33. 10.1038/nrg1748, 16369569.
19. Fargeas CA, Huttner WB, Corbeil D. Nomenclature of prominin-1 (CD133) splice variants - an update. Tissue Antigens 2007, 69:602-606. 10.1111/j.1399-0039.2007.00825.x, 17498271.
20. Shmelkov SV, Jun L, St Clair R, McGarrigle D, Derderian CA, Usenko JK, Costa C, Zhang F, Guo X, Rafii S. Alternative promoters regulate transcription of the gene that encodes stem cell surface protein AC133. Blood 2004, 103:2055-2061. 10.1182/blood-2003-06-1881, 14630820.
21. Korenchuk S, Lehr JE, L MC, Lee YG, Whitney S, Vessella R, Lin DL, Pienta KJ. VCaP, a cell-based model system of human prostate cancer. In Vivo 2001, 15:163-168.
22. Birnie R, Bryce SD, Roome C, Dussupt V, Droop A, Lang SH, Berry PA, Hyde CF, Lewis JL, Stower MJ, Maitland NJ, Collins AT. Gene expression profiling of human prostate cancer stem cells reveals a pro-inflammatory phenotype and the importance of extracellular matrix interactions. Genome Biol 2008, 9:R83. 10.1186/gb-2008-9-5-r83, 2441469, 18492237.
23. Lang SH, Anderson E, Fordham R, Collins AT. Modeling the prostate stem cell niche: an evaluation of stem cell survival and expansion in vitro. Stem Cells Dev 2010, 19:537-546. 10.1089/scd.2009.0291, 20102283.
24. O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110. 10.1038/nature05372, 17122772.
25. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C, De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2007, 445:111-115. 10.1038/nature05384, 17122771.
26. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401. 10.1038/nature03128, 15549107.
27. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, Lu L, Irvin D, Black KL, Yu JS. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 2006, 5:67. 10.1186/1476-4598-5-67, 1697823, 17140455.
28. Monzani E, Facchetti F, Galmozzi E, Corsini E, Benetti A, Cavazzin C, Gritti A, Piccinini A, Porro D, Santinami M, Invernici G, Parati E, Alessandri G, La Porta CA. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 2007, 43:935-946. 10.1016/j.ejca.2007.01.017, 17320377.
29. Olempska M, Eisenach PA, Ammerpohl O, Ungefroren H, Fandrich F, Kalthoff H. Detection of tumor stem cell markers in pancreatic carcinoma cell lines. Hepatobiliary Pancreat Dis Int 2007, 6:92-97.
30. Suetsugu A, Nagaki M, Aoki H, Motohashi T, Kunisada T, Moriwaki H. Characterization of CD133+ hepatocellular carcinoma cells as cancer stem/progenitor cells. Biochem Biophys Res Commun 2006, 351:820-824. 10.1016/j.bbrc.2006.10.128, 17097610.
31. Yin S, Li J, Hu C, Chen X, Yao M, Yan M, Jiang G, Ge C, Xie H, Wan D, Yang S, Zheng S, Gu J. CD133 positive hepatocellular carcinoma cells possess high capacity for tumorigenicity. Int J Cancer 2007, 120:1444-1450. 10.1002/ijc.22476, 17205516.
32. Shepherd CJ, Rizzo S, Ledaki I, Davies M, Brewer D, Attard G, De Bono J, Hudson DL. Expression profiling of CD133+ and CD133- epithelial cells from human prostate. Prostate 2008, 68:1007-1024. 10.1002/pros.20765, 18398820.
33. Vaissière T, Sawan C, Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat Res 2008, 659:40-48. 10.1016/j.mrrev.2008.02.004, 18407786.
34. Yi JM, Tsai HC, Glöckner SC, Lin S, Ohm JE, Easwaran H, James CD, Costello JF, Riggins G, Eberhart CG, Laterra J, Vescovi AL, Ahuja N, Herman JG, Schuebel KE, Baylin SB. Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res 2008, 68:8094-8103. 10.1158/0008-5472.CAN-07-6208, 2744404, 18829568.
35. Missol-Kolka E, Karbanova J, Janich P, Haase M, Fargeas CA, Huttner WB, Corbeil D. Prominin-1 (CD133) is not restricted to stem cells located in the basal compartment of murine and human prostate. Prostate 2011, 71:254-267. 10.1002/pros.21239, 20717901.
36. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760. 10.1038/nature05236, 17051156.
37. Rich JN, Bao S. Chemotherapy and cancer stem cells. Cell Stem Cell 2007, 1:353-355. 10.1016/j.stem.2007.09.011, 18371369.
38. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5:275-284. 10.1038/nrc1590, 15803154.
39. Takenobu H, Shimozato O, Nakamura T, Ochiai H, Yamaguchi Y, Ohira M, Nakagawara A, Kamijo T. CD133 suppresses neuroblastoma cell differentiation via signal pathway modification. Oncogene 2011, 30:97-105. 10.1038/onc.2010.383, 20818439.
40. Florek M, Haase M, Marzesco AM, Freund D, Ehninger G, Huttner WB, Corbeil D. Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 2005, 319:15-26. 10.1007/s00441-004-1018-z, 15558321.
41. Antequera F, Boyes J, Bird A. High levels of de novo methylation and altered chromatin structure at CpG islands in cell lines. Cell 1990, 62:503-514. 10.1016/0092-8674(90)90015-7, 1974172.
42. Jones PA, Wolkowicz MJ, Rideout WM, Gonzales FA, Marziasz CM, Coetzee GA, Tapscott SJ. De novo methylation of the MyoD1 CpG island during the establishment of immortal cell lines. Proc Natl Acad Sci USA 1990, 87:6117-6121. 10.1073/pnas.87.16.6117, 54483, 2385586.
43. Vertino PM, Issa JP, Pereira-Smith OM, Baylin SB. Stabilization of DNA methyltransferase levels and CpG island hypermethylation precede SV40-induced immortalization of human fibroblasts. Cell Growth Differ 1994, 5:1395-1402.
44. Kondo Y, Shen L, Cheng AS, Ahmed S, Boumber Y, Charo C, Yamochi T, Urano T, Furukawa K, Kwabi-Addo B, Gold DL, Sekido Y, Huang TH-M, Issa J-PJ. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nature Genetics 2008, 40:741-750. 10.1038/ng.159, 18488029.
45. Coolen MW, Stirzaker C, Song JZ, Statham AL, Kassir Z, Moreno CS, Young AN, Varma V, Speed TP, Cowley M, Lacaze P, Kaplan W, Robinson MD, Clark SJ. Consolidation of the cancer genome into domains of repressive chromatin by long-range epigenetic silencing (LRES) reduces transcriptional plasticity. Nature Cell Biology 2010, 12:235-246. 3058354, 20173741.
46. Pfeiffer MJ, Schalken JA. Stem cell characteristics in prostate cancer cell lines. Eur Urol 2010, 57:246-254. 10.1016/j.eururo.2009.01.015, 19200636.
47. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 1996, 93:9821-9826. 10.1073/pnas.93.18.9821, 38513, 8790415.
48. Navarro P, Pichard S, Ciaudo C, Avner P, Rougeulle C. Tsix transcription across the Xist gene alters chromatin conformation without affecting Xist transcription: implications for X-chromosome inactivation. Genes Dev 2005, 19:1474-1484. 10.1101/gad.341105, 1151664, 15964997.