Evaluation of stem cell marker gene expression in canine prostate carcinoma- and prostate cyst-derived cell lines

Anticancer Research

Volumn 33, Issue 12, 2013, Pages 5421-5431

  Moulay, Mohammed ^a   Liu, Wen ^a   Willenbrock, Saskia ^a   Sterenczak, Katharina Anna ^a   Carlson, Regina ^a   Ngezahayo, Anaclet ^b   Escobar, Hugo Murua ^a,c   Nolte, Ingo ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Cancer stem cells; Canine; CT1258; CT1258 EGFP; CT1258 EGFP HMGA2 cell lines; Prostate cancer; Stem cell marker

Indexed keywords

CD133 ANTIGEN; CD34 ANTIGEN; CELL MARKER; HERMES ANTIGEN; ITGA6 PROTEIN; MELK PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; ONCOPROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DOG; FLOW CYTOMETRY; GENE EXPRESSION; MARKER GENE; MOUSE; NONHUMAN; ONCOGENE C KIT; PRIORITY JOURNAL; PROSTATE CARCINOMA; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STEM CELL;

EID: 84891435423     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (73)

1. Society AC: Cancer Facts & Figures 2013. Atlanta. American Cancer Society 2013.
2. Rowell JL, McCarthy DO and Alvarez CE: Dog models of naturally occurring cancer. Trends Mol Med 17: 380-388, 2011.
3. Paoloni M and Khanna C: Translation of new cancer treatments from pet dogs to humans. Nat Rev Cancer 8: 147-156, 2008.
4. Lawrence JA and Saba CF: Tumors of the Male Reproductive System. Withrow & MacEwen's Small Animal Clinical Oncology 5: 557-571, 2013.
5. Leroy BE and Northrup N: Prostate cancer in dogs: comparative and clinical aspects. Vet J 180: 149-162, 2009.
6. Axiak SM and Bigio A: Canine prostatic carcinoma. Compend Contin Educ Vet 34: E1-5, 2012.
7. Dubrovska A, Kim S, Salamone RJ, Walker JR, Maira SM, Garcia-Echeverria C, Schultz PG and Reddy VA: The role of PTEN/Akt/PI3K signaling in the maintenance and viability of prostate cancer stem-like cell populations. Proc Natl Acad Sci USA 106: 268-273, 2009.
8. Petrylak DP: Hormone-refractory prostate cancer: new horizons. Rev Urol 5: 54-58, 2003.
9. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003.
10. Clarke MF and Fuller M: Stem cells and cancer: Two faces of eve. Cell 124: 1111-1115, 2006.
11. Kuranda K, Berthon C, Lepretre F, Polakowska R, Jouy N and Quesnel B: Expression of CD34 in Hematopoietic Cancer Cell Lines Reflects Tightly Regulated Stem/Progenitor-Like State. J Cell Biochem 112: 1277-1285, 2011.
12. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF and Simeone DM: Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037, 2007.
13. Cocciadiferro L, Miceli V, Kang KS, Polito LM, Trosko JE and Carruba G: Profiling cancer stem cells in androgen-responsive and refractory human prostate tumor cell lines. Ann NY Acad Sci 1155: 257-62, 2009.
14. Paronetto MP, Farini D, Sammarco I, Maturo G, Vespasiani G, Geremia R, Rossi P and Sette C: Expression of a truncated form of the c-Kit tyrosine kinase receptor and activation of Src kinase in human prostatic cancer. Am J Pathol 164: 1243-1251, 2004.
15. Lamerato-Kozicki AR, Helm KM, Jubala CM, Cutter GC and Modiano JF: Canine hemangiosarcoma originates from hematopoietic precursors with potential for endothelial differentiation. Exp Hematol 34: 870-878, 2006.
16. Nemoto Y, Maruo T, Sato T, Deguchi T, Ito T, Sugiyama H, Ishikawa T, Madarame H, Watanabe T, Shida T and Sahara H: Identification of Cancer Stem Cells Derived From a Canine Lung Adenocarcinoma Cell Line. Vet Pathol 48: 1029-1034, 2011.
17. Stoica G, Lungu G, Martini-Stoica H, Waghela S, Levine J and Smith R 3rd: Identification of cancer stem cells in dog glioblastoma. Vet Pathol 46: 391-406, 2009.
18. Zhao R, Xiang N, Domann FE and Zhong W: Effects of selenite and genistein on G2/M cell cycle arrest and apoptosis in human prostate cancer cells. Nutr Cancer 61: 397-407, 2009.
19. Navone NM, Olive M, Ozen M, Davis R, Troncoso P, Tu SM, Johnston D, Pollack A, Pathak S, von Eschenbach AC and Logothetis CJ: Establishment of two human prostate cancer cell lines derived from a single bone metastasis. Clin Cancer Res 3: 2493-2500, 1997.
20. Russell PJ and Kingsley EA: Human Prostate Cancer Cell Lines. Prostate Cancer Methods and Protocols 81: 21-39, 2003.
21. Trapasso S and Allegra E: Role of CD44 as a marker of cancer stem cells in head and neck cancer. Biologics 6: 379-383, 2012.
22. Bender JG, Unverzagt KL, Walker DE, Lee W, Vanepps DE, Smith DH, Stewart CC and To LB: Identification and Comparison of Cd34-Positive Cells and Their Subpopulations from Normal Peripheral-Blood and Bone-Marrow Using Multicolor Flow-Cytometry. Blood 77: 2591-2596, 1991.
23. Gallacher L MB, Wu D.M, Karanu F.N, Keeney M and Bhatia M: Isolation and characterization of human CD34-Lin- and CD34+Lin- hematopoietic stem cells using cell surface markers AC133 and CD7. Blood 95: 2813-2820, 2000.
24. Krams M, Parwaresch R, Sipos B, Heidorn K, Harms D and Rudolph P: Expression of the c-kit receptor characterizes a subset of neuroblastomas with favorable prognosis. Oncogene 23: 588-595, 2004.
25. Onishi T YK, Franco O.E, Kawamura J, Watanabe M, Shiraishi T and Kitazawa S: Mitogen-activated protein kinase pathway is involved in u6 integrin gene expression in androgen-independent prostate cancer cells, role of proximal Sp1 consensus sequence. Biochim Biophys Acta 1538: 218-227, 2001.
26. Desgrosellier JS and Cheresh DA: Integrins in cancer: biological implications and therapeutic opportunities. Nature Reviews Cancer 10: 9-22, 2010.
27. Hoffmann MJ, Muller M, Engers R and Schulz WA: Epigenetic control of CTCFL/BORIS and OCT4 expression in urogenital malignancies. Biochem Pharmacol 72: 1577-1588, 2006.
28. Clark EL, Hadjimichael C, Temperley R, Barnard A, Fuller-Pace FV and Robson CN: p68/DdX5 supports beta-catenin & RNAP II during androgen receptor mediated transcription in prostate cancer. PLoS One 8: 1-10, 2013.
29. Badouel C, Chartrain I, Blot J and Tassan JP: Maternal embryonic leucine zipper kinase is stabilized in mitosis by phosphorylation and is partially degraded upon mitotic exit. Exp Cell Res 316: 2166-2173, 2010.
30. Patel AN, Park E, Kuzman M, Benetti F, Silva FJ and Allickson JG: Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant 17: 303-311, 2008.
31. Shackleton M: Normal stem cells and cancer stem cells: similar and different. Semin Cancer Biol 20: 85-92, 2010.
32. Zhao W, Ji X, Zhang F, Li L and Ma L: Embryonic stem cell markers. Molecules 17: 6196-6236, 2012.
33. Wiesner C, Nabha SM, Dos Santos EB, Yamamoto H, Meng H, Melchior SW, Bittinger F, Thuroff JW, Vessella RL, Cher ML and Bonfil RD: C-kit and its ligand stem cell factor: potential contribution to prostate cancer bone metastasis. Neoplasia 10: 996-1003, 2008.
34. Pellacani D, Packer RJ, Frame FM, Oldridge EE, Berry PA, Labarthe MC, Stower MJ, Simms MS, Collins AT and Maitland NJ: Regulation of the stem cell marker CD133 is independent of promoter hypermethylation in human epithelial differentiation and cancer. Molecular Cancer 10: 1-14, 2011.
35. Liu AY: Differential expression of cell surface molecules in prostate cancer cells. Cancer Res 60: 3429-3434, 2000.
36. Clark EL, Coulson A, Dalgliesh C, Rajan P, Nicol SM, Fleming S, Heer R, Gaughan L, Leung HY, Elliott DJ, Fuller-Pace FV and Robson CN: The RNA helicase p68 is a novel androgen receptor coactivator involved in splicing and is overexpressed in prostate cancer. Cancer Research 68: 7938-7946, 2008.
37. Kuner R, Falth M, Pressinotti NC, Brase JC, Puig SB, Metzger J, Gade S, Schafer G, Bartsch G, Steiner E, Klocker H and Sultmann H: The maternal embryonic leucine zipper kinase (MELK) is upregulated in high-grade prostate cancer. Journal of Molecular Medicine-Jmm 91: 237-248, 2013.
38. Hudson TS, Perkins SN, Hursting SD, Young HA, Kim YS, Wang TC and Wang TT: Inhibition of androgen-responsive LNCaP prostate cancer cell tumor xenograft growth by dietary phenethyl isothiocyanate correlates with decreased angiogenesis and inhibition of cell attachment. Int J Oncol 40: 1113-1121, 2012.
39. Sroka I.C PGD, Nagle R.B, Porreca F, King T, Pestano G, Futscher B.W, Gard J.M, Riley J, Sathyanarayana UG and Cress AE: Human Cell Surface Receptors as Molecular Imaging Candidates for Metastatic Prostate Cancer. The Open Prostate Cancer Journal 2: 59-66, 2009.
40. Chen Y, Zhao J, Luo Y, Wang Y, Wei N and Jiang Y: Isolation and identification of cancer stem-like cells from side population of human prostate cancer cells. J Huazhong Univ Sci Technolog Med Sci 32: 697-703, 2012.
41. Wei C, Guomin W, Yujun L and Ruizhe Q: Cancer stem-like cells in human prostate carcinoma cells DU145: the seeds of the cell line? Cancer Biol Ther 6: 763-768, 2007.
42. Winkler S, Reimann-Berg N, Murua Escobar H, Loeschke S, Eberle N, Hoinghaus R, Nolte I and Bullerdiek J: Polysomy 13 in a canine prostate carcinoma underlining its significance in the development of prostate cancer. Cancer Genet Cytogenet 169: 154-158, 2006.
43. Blacking TM, Waterfall M, Samuel K and Argyle DJ: Flow cytometric techniques for detection of candidate cancer stem cell subpopulations in canine tumour models. Vet Comp Oncol 10: 252-273, 2012.
44. Taylor RA: Stem cells in prostate cancer: treating the root of the problem. Endocr Relat Cancer 17: 273-285, 2010.
45. Lawson DA, Xin L, Lukacs RU, Cheng DH and Witte ON: Isolation and functional characterization of murine prostate stem cells. Proc Natl Acad Sci USA 104: 181-186, 2007.
46. Goldstein AS, Lawson DA, Cheng DH, Sun WY, Garraway IP and Witte ON: Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc Natl Acad Sci USA 105: 20882-20887, 2008.
47. Marian CO and Shay JW: Prostate tumor-initiating cells: a new target for telomerase inhibition therapy? Biochim Biophys Acta 1792: 289-296, 2009.
48. Iczkowski KA: Cell adhesion molecule CD44: its functional roles in prostate cancer. Am J Transl Res 3: 1-7, 2010.
49. Joetzke AE, Sterenczak KA, Eberle N, Wagner S, Soller JT, Nolte I, Bullerdiek J, Murua Escobar H and Simon D: Expression of the high mobility group A1 (HMGA1) and A2 (HMGA2) genes in canine lymphoma: analysis of 23 cases and comparison to control cases. Vet Comp Oncol 8: 87-95, 2010.
50. Winkler S, Murua Escobar H, Meyer B, Simon D, Eberle N, Baumgartner W, Loeschke S, Nolte I and Bullerdiek J: HMGA2 expression in a canine model of prostate cancer. Cancer Genet Cytogenet 177: 98-102, 2007.
51. Bartuma H, Panagopoulos I, Collin A, Trombetta D, Domanski HA, Mandahl N and Mertens F: Expression levels of HMGA2 in adipocytic tumors correlate with morphologic and cytogenetic subgroups. Molecular Cancer 8: 1-11, 2009.
52. Di Cello F, Hillion J, Hristov A, Wood LJ, Mukherjee M, Schuldenfrei A, Kowalski J, Bhattacharya R, Ashfaq R and Resar LM: HMGA2 participates in transformation in human lung cancer. Molecular Cancer Research 6: 743-750, 2008.
53. Zha L, Wang Z, Tang W, Zhang N, Liao G and Huang Z: Genome-wide analysis of HMGA2 transcription factor binding sites by ChIP on chip in gastric carcinoma cells. Mol Cell Biochem 364: 243-251, 2012.
54. Collins AT, Berry PA, Hyde C, Stower MJ and Maitland NJ: Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951, 2005.
55. Vander Griend DJ, Karthaus WL, Dalrymple S, Meeker A, DeMarzo AM and Isaacs JT: The role of CD133 in normal human prostate stem cells and malignant cancer-initiating cells. Cancer Res 68: 9703-9711, 2008.
56. Fabian A, Vereb G and Szollosi J: The hitchhikers guide to cancer stem cell theory: markers, pathways and therapy. Cytometry A 83: 62-71, 2012.
57. + population in hepatocellular carcinoma. Int J Cancer 126: 2067-2078, 2010.
58. Cheng I, Plummer SJ, Neslund-Dudas C, Klein EA, Casey G, Rybicki BA and Witte JS: Prostate cancer susceptibility variants confer increased risk of disease progression. Cancer Epidemiol Biomarkers Prev 19: 2124-2132, 2010.
59. Emadi Baygi M, Soheili ZS, Essmann F, Deezagi A, Engers R, Goering W and Schulz WA: Slug/SNAI2 regulates cell proliferation and invasiveness of metastatic prostate cancer cell lines. Tumour Biol 31: 297-307, 2010.
60. Dröge P and Davey CA: Do Cells let-7 Determine Stemness? Cell Stem Cell 2: 8-9, 2008.
61. Han B, Mehra R, Dhanasekaran SM, Yu J, Menon A, Lonigro RJ, Wang X, Gong Y, Wang L, Shankar S, Laxman B, Shah RB, Varambally S, Palanisamy N, Tomlins SA, Kumar-Sinha C and Chinnaiyan AM: A fluorescence in situ hybridization screen for E26 transformation-specific aberrations: identification of DDX5-ETV4 fusion protein in prostate cancer. Cancer Res 68: 7629-7637, 2008.
62. Liu Z-R: DDX5 (DEAD (Asp-Glu-Ala-Asp) box polypeptide 5). Atlas of Genetics and Cytogenetics in Oncology and Haematology 16: 44-47, 2012.
63. Wang D, Huang J and Hu Z: RNA helicase DDX5 regulates microRNA expression and contributes to cytoskeletal reorganization in basal breast cancer cells. Molecular and Cellular Proteomics 11: 1-12, 2012.
64. Webster JD, Yuzbasiyan-Gurkan V, Kaneene JB, Miller R, Resau JH and Kiupel M: The role of c-KIT in tumorigenesis: evaluation in canine cutaneous mast cell tumors. Neoplasia 8: 104-111, 2006.
65. Le Page Y, Chartrain I, Badouel C and Tassan JP: A functional analysis of MELK in cell division reveals a transition in the mode of cytokinesis during Xenopus development. J Cell Sci 124: 958-968, 2011.
66. Tassan JP: Cortical localization of maternal embryonic leucine zipper kinase (MELK) implicated in cytokinesis in early xenopus embryos. Commun Integr Biol 4: 483-485, 2011.
67. Gilbert CA and Ross AH: Cancer stem cells: cell culture, markers, and targets for new therapies. J Cell Biochem 108: 1031-1038, 2009.
68. Chung S and Nakamura Y: MELK inhibitor, novel molecular targeted therapeutics for human cancer stem cells. Cell Cycle 12: 1655-1656, 2013.
69. Tai MH, Chang CC, Kiupel M, Webster JD, Olson LK and Trosko JE: Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26: 495-502, 2005.
70. Linn DE, Yang X, Sun F, Xie Y, Chen H, Jiang R, Chen H, Chumsri S, Burger AM and Qiu Y: A Role for OCT4 in Tumor Initiation of Drug-Resistant Prostate Cancer Cells. Genes Cancer 1: 908-916, 2010.
71. + cells. Tropical Journal of Pharmaceutical Research 8: 3-9, 2009.
72. Blacking TM, Wilson H and Argyle DJ: is cancer a stem cell disease? theory, evidence and implication. Veterinary and Comparative Oncology 5: 76-89, 2007
73. Pfeiffer MJ and Schalken JA: Stem cell characteristics in prostate cancer cell lines. Eur Urol 57: 246-254, 2010.