Human osteosarcoma CD49f- CD133+ cells: Impaired in osteogenic fate while gain of tumorigenicity

Oncogene

Volumn 32, Issue 36, 2013, Pages 4252-4263

  Ying, M ^a   Liu, G ^a   Shimada, H ^a,b   Ding, W ^a   May, W A ^a,b   He, Q ^c   Adams, G B ^b   Wu, L ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

lineage differentiation; osteogenic differentiation; osteosarcoma forming cells; osteosarcoma initiating cells; self renewal; tumorigenicity

Indexed keywords

ADIPOPHILIN; ALPHA6 INTEGRIN; CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; NOTCH RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; STEM CELL FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DEVELOPMENT; CARCINOGENICITY; CELL DIFFERENTIATION; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL RENEWAL; CELL SUBPOPULATION; CELL TRACKING; CHEMOSENSITIVITY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOSARCOMA CELL; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; TRANSPLANTATION; TUMOR GROWTH; XENOTRANSPLANTATION;

ANIMALS; ANTIGENS, CD; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION; GLYCOPROTEINS; HUMANS; IMMUNOPHENOTYPING; INTEGRIN ALPHA6; MICE; NEOPLASM METASTASIS; NEOPLASTIC STEM CELLS; OSTEOGENESIS; OSTEOSARCOMA; PEPTIDES; PHENOTYPE; SPHEROIDS, CELLULAR; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 84883739482     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.438     Document Type: Article

References (47)

1. Thomas D, Kansara M. Epigenetic modifications in osteogenic differentiation and transformation. J Cell Biochem 2006; 98: 757-769.
2. Tang N, Song WX, Luo J, Haydon RC, He TC. Osteosarcoma development and stem cell differentiation. Clin Orthop Relat Res 2008; 466: 2114-2130.
3. Bakhshi S, Radhakrishnan V. Prognostic markers in osteosarcoma. Expert Rev Anticancer Ther 2010; 10: 271-287.
4. Adhikari AS, Agarwal N, Wood BM, Porretta C, Ruiz B, Pochampally RR et al. CD117 and Stro-1 identify osteosarcoma tumor-initiating cells associated with metastasis and drug resistance. Cancer Res 2010; 70: 4602-4612.
5. Di Fiore R, Santulli A, Ferrante RD, Giuliano M, De Blasio A, Messina C et al. Identification and expansion of human osteosarcoma-cancer-stem cells by long-term 3-aminobenzamide treatment. J Cell Physiol 2009; 219: 301-313.
6. Tirino V, Desiderio V, d'Aquino R, De Francesco F, Pirozzi G, Graziano A et al. Detection and characterization of CD133\+ cancer stem cells in human solid tumours. PLoS One 2008; 3: e3469.
7. Tirino V, Desiderio V, Paino F, De Rosa A, Papaccio F, Fazioli F et al. Human primary bone sarcomas contain CD133\+ cancer stem cells displaying high tumorigenicity in vivo. FASEB J 2011; 25: 2022-2030.
8. Levings PP, McGarry SV, Currie TP, Nickerson DM, McClellan S, Ghivizzani SC et al. Expression of an exogenous human Oct-4 promoter identifies tumor-initiating cells in osteosarcoma. Cancer Res 2009; 69: 5648-5655.
9. Wang L, Park P, Zhang H, La Marca F, Lin CY. Prospective identification of tumorigenic osteosarcoma cancer stem cells in OS99-1 cells based on high aldehyde dehydrogenase activity. Int J Cancer 2011; 128: 294-303.
10. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: models and concepts. Annu Rev Med 2007; 58: 267-284.
11. O'Brien CA, Kreso A, Jamieson CH. Cancer stem cells and self-renewal. Clin Cancer Res 2010; 16: 3113-3120.
12. Hong D, Gupta R, Ancliff P, Atzberger A, Brown J, Soneji S et al. Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 2008; 319: 336-339.
13. Cox CV, Evely RS, Oakhill A, Pamphilon DH, Goulden NJ, Blair A. Characterization of acute lymphoblastic leukemia progenitor cells. Blood 2004; 104: 2919-2925.
14. Cox CV, Martin HM, Kearns PR, Virgo P, Evely RS, Blair A. Characterization of a progenitor cell population in childhood T-cell acute lymphoblastic leukemia. Blood 2007; 109: 674-682.
15. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
16. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 2003; 100: 3983-3988.
17. 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: 111-115.
18. Bomken S, Fiser K, Heidenreich O, Vormoor J. Understanding the cancer stem cell. Br J Cancer 2010; 103: 439-445.
19. Wu Y, Wu PY. CD133 as a marker for cancer stem cells: progresses and concerns. Stem Cells Dev 2009; 18: 1127-1134.
20. Mizrak D, Brittan M, Alison MR. CD133: molecule of the moment. J Pathol 2008; 214: 3-9.
21. Rountree CB, Ding W, He L, Stiles B. Expansion of CD133-expressing liver cancer stem cells in liver-specific phosphatase and tensin homolog deleted on chromosome 10-deleted mice. Stem Cells 2009; 27: 290-299.
22. 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: 2111-2120.
23. Joo KM, Kim SY, Jin X, Song SY, Kong DS, Lee JI et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab Invest 2008; 88: 808-815.
24. Dylla SJ, Beviglia L, Park IK, Chartier C, Raval J, Ngan L et al. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008; 3: e2428.
25. 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: 3382-3389.
26. Joo KM, Nam DH. Prospective identification of cancer stem cells with the surface antigen CD133. Methods Mol Biol 2009; 568: 57-71.
27. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006; 9: 391-403.
28. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003; 17: 1253-1270.
29. Majeti R, Becker MW, Tian Q, Lee TL, Yan X, Liu R et al. Dysregulated gene expression networks in human acute myelogenous leukemia stem cells. Proc Natl Acad Sci USA 2009; 106: 3396-3401.
30. Luo P, Yang X, Ying M, Chaudhry P, Wang A, Shimada H et al. Retinoid-suppressed phosphorylation of RARalpha mediates the differentiation pathway of osteosarcoma cells. Oncogene 2010; 29: 2772-2783.
31. Lee RH, Seo MJ, Pulin AA, Gregory CA, Ylostalo J, Prockop DJ. The CD34-like protein PODXL and alpha6-integrin (CD49f) identify early progenitor MSCs with increased clonogenicity and migration to infarcted heart in mice. Blood 2009; 113: 816-826.
32. Lathia JD, Gallagher J, Heddleston JM, Wang J, Eyler CE, Macswords J et al. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010; 6: 421-432.
33. Noel AC, Lefebvre O, Maquoi E, VanHoorde L, Chenard MP, Mareel M et al. Stromelysin-3 expression promotes tumor take in nude mice. J Clin Invest 1996; 97: 1924-1930.
34. Ferrandina G, Petrillo M, Bonanno G, Scambia G. Targeting CD133 antigen in cancer. Expert Opin Ther Targets 2009; 13: 823-837.
35. Woodward WA, Sulman EP. Cancer stem cells: markers or biomarkers? Cancer Metastasis Rev 2008; 27: 459-470.
36. Chou AJ, Geller DS, Gorlick R. Therapy for osteosarcoma: where do we go from here? Paediatr Drugs 2008; 10: 315-327.
37. 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.
38. Dewan MZ, Ahmed S, Iwasaki Y, Ohba K, Toi M, Yamamoto N. Stromal cell-derived factor-1 and CXCR4 receptor interaction in tumor growth and metastasis of breast cancer. Biomed Pharmacother 2006; 60: 273-276.
39. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, Esterni B et al. Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 2010; 16: 45-55.
40. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007; 1: 313-323.
41. Oda Y, Yamamoto H, Tamiya S, Matsuda S, Tanaka K, Yokoyama R et al. CXCR4 and VEGF expression in the primary site and the metastatic site of human osteosarcoma: analysis within a group of patients, all of whom developed lung metastasis. Mod Pathol 2006; 19: 738-745.
42. Ikushima H, Todo T, Ino Y, Takahashi M, Miyazawa K, Miyazono K. Autocrine TGFbeta signaling maintains tumorigenicity of glioma-initiating cells through Sryrelated HMG-box factors. Cell Stem Cell 2009; 5: 504-514.
43. Wu Y, Cain-Hom C, Choy L, Hagenbeek TJ, de Leon GP, Chen Y et al. Therapeutic antibody targeting of individual Notch receptors. Nature 2010; 464: 1052-1057.
44. Luo P, Wang A, Payne KJ, Peng H, Wang JG, Parrish YK et al. Intrinsic retinoic acid receptor alpha-cyclin-dependent kinase-activating kinase signaling involves coordination of the restricted proliferation and granulocytic differentiation of human hematopoietic stem cells. Stem Cells 2007; 25: 2628-2637.
45. Kang HG, Jenabi JM, Zhang J, Keshelava N, Shimada H, May WA et al. E-cadherin cell-cell adhesion in ewing tumor cells mediates suppression of anoikis through activation of the ErbB4 tyrosine kinase. Cancer Res 2007; 67: 3094-3105.
46. Zhang W, Deng ZL, Chen L, Zuo GW, Luo Q, Shi Q et al. Retinoic acids potentiate BMP9-induced osteogenic differentiation of mesenchymal progenitor cells. PLoS One 2010; 5: e11917.
47. Maxson S, Burg KJ. Conditioned media cause increases in select osteogenic and adipogenic differentiation markers in mesenchymal stem cell cultures. J Tissue Eng Regen Med 2008 2: 147-154.