Mesenchymal stem cells promote tumor engraftment and metastatic colonization in rat osteosarcoma model

International Journal of Oncology

Volumn 40, Issue 1, 2012, Pages 163-169

  Tsukamoto, Shinji ^a   Honoki, Kanya ^a   Fuji, Hiromasa ^a   Tohma, Yasuaki ^a   Kido, Akira ^a   Mori, Toshio ^a   Tsujiuchi, Toshifumi ^b   Tanaka, Yasuhito ^a  

^a NARA MEDICAL UNIVERSITY   (Japan)

^b KINKI UNIVERSITY   (Japan)

Author keywords

Cancer stem cell niche; Mesenchymal stromal cell; Metastasis; Osteosarcoma; Rat

Indexed keywords

CYTOKINE; CYTOKINE RECEPTOR; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; RNA; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL MIGRATION; FEMUR; GENE EXPRESSION; MESENCHYMAL STEM CELL; METASTASIS; NONHUMAN; OSTEOSARCOMA; PRIORITY JOURNAL; RAT; TUMOR GROWTH;

ANIMALS; BONE NEOPLASMS; CELL MOVEMENT; GENE EXPRESSION PROFILING; LUNG NEOPLASMS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; OSTEOSARCOMA; RATS; RATS, INBRED F344; TUMOR MICROENVIRONMENT;

EID: 84455163065     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2011.1220     Document Type: Article

References (56)

1. Paget S: The distribution of secondary growths in cancer of the breast. Lancet 1: 571-573, 1889.
2. Albini A and Sporn MB: The tumour microenvironment as a target for chemoprevention. Nat Rev Cancer 7: 139-147, 2007. (Pubitemid 46160989)
3. Yen BL and Yen M-L: Mesenchymal stem cells and cancer-for better or for worse? J Cancer Mol 4: 5-9, 2008. (Pubitemid 351902828)
4. Friednstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF and Keikiss-Borok IV: Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues, cloning in vitro and retransplantation in vivo. Transplantation 17: 331-340, 1974.
5. Prockop DJ: Marrow stromal cells as stem cells for non-hematopoietic tissues. Science 276: 71-74, 1997.
6. Brooke G, Cook M, Blair C, Han R: Heazelwood C, Jones B, Kambouris M, Kollar K, McTaggart S, Pelekanos R, Rice A, Rosetti T and Atkinson K: Therapeutic applications of mesenchymal stromal cells. Semin Cell Dev Biol 18: 846-858, 2007. (Pubitemid 350138458)
7. Pittenger MF, Machay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S and Marshak DR: Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147, 1999. (Pubitemid 29282067)
8. Jorgensen C, Noel D, Apparailly F and Sany J: Stem cells for repair off cartilage and bone: the next challenge in osteoarthritis and rheumatoid arthritis. Ann Rheum Dis 60: 305, 2001.
9. Nauta AJ and Fibbe WE: Immunomodulatory properties of mesenchymal stromal cells. Blood 110: 3499-3506, 2007. (Pubitemid 350159613)
10. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, Lewis I, Lanino E, Sundberg B, Bernardo ME, Remberger M, Dini G, Egeler RM, Bacigalupo A, Fibbe W and Ringden O: Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase-II study. Lancet 371: 1579-1586, 2008. (Pubitemid 351626841)
11. Devine SM, Bartholomew AM, Mahmud N, Nelson M, Patil S, Hardy W, Sturgeon C, Hewit T, Chung T, Stock W, Sher D, Weissman S, Ferrer K, Mosca J, Deans R, Moseley A and Hoffman R: Mesenchymal stem cells are capable of homing to the bone marrow of nonihuman primates following systemic infusion. Exp Hemtol 29: 244-255, 2001. (Pubitemid 32112325)
12. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N and Phinney DG: Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 100: 8407-8411, 2003. (Pubitemid 36842558)
13. Chamberlain G, Fox J, Ashton B and Middleton J: Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25: 2739-2749, 2007. (Pubitemid 350127858)
14. Studeny M, Marini FC, Champlin RE, Zompetta C, Fidler IJ and Andreeff M: Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors. Cancer Res 62: 3603-3608, 2002. (Pubitemid 34728832)
15. Dwyer RM, Potter-Beirne SM, Harrington KA, Lowery AJ, Hennessy E, Murphy JM, Barry FP, O'Brien T and Kerin MJ: Monocyte chemotactic protein-1 secreted by primary breast tumors stimulates migration of mesenchymal stem cells. Clin Cancer Res 13: 5020-5027, 2007. (Pubitemid 47502066)
16. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, Noel D and Jorgensen C: Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102: 3837-3844, 2003. (Pubitemid 37409409)
17. Djouad F, Bony C, Apparailly F, Louis-Plence P, Jorgensen C and Noel D: Earlier onset of syngenic tumors in the presence of mesenchyaml stem cells. Transplantation 82: 1060-1066, 2006.
18. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R and Weinberg RA: Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449: 557-563, 2007.
19. Beckermann BM, Kallifatiditis G, Groth A, Frommhold D, Apel A, Mattern J, Salnikov AV, Moldenhauer G, Wagner W, Diehlmann A, Saffrich R, Schubert M, Ho AD, Giese N, Buchler MW, Friess H, Buchler P and Herr I: VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 99: 622-631, 2008.
20. Annabi B, Naud E, Lee YT, Eliopoulos N and Galipeau J: Vascular progenitors derived from murine bone marrow stromal cells are regulated by fibroblast growth factor and are avidly recruited by vascularizing tumors. J Cell Biochem 91: 1146-1158, 2004.
21. Hung SC, Deng WP, Yang WK, Kiu RS, Lee CC, Su TC, Lin RJ, Yang DM, Chang CW, Chen WH, Wei HJ and Gelovani JG: Mesenchymal stem cell targeting of microscopic tumors and tumor stroma development monitored by noninvasive in vivo positron emission tomography imaging. Clin Cancer Res 11: 7749-7756, 2005. (Pubitemid 41611618)
22. Mackall CL, Meltzer PS and Helman LJ: Focus on sarcomas. Cancer Cell 2: 175-178, 2002. (Pubitemid 41043972)
23. Li Q, Hisha H, Takaki T, Adachi Y, Li M, Song C, Feng W, Okazaki S, Mizokami T, Kato J, Inaba M, Hosaka N, Maki M and Ikehara S: Transformation potential of bone marrow stromal cells into undifferentiated high-grade pleomorphic sarcoma. J Cancer Res Clin Oncol 136: 829-838, 2010.
24. Mohseny AB, Szuhai K, Romeo S, Buddingh EP, Briaire-de Bruijn I, De Jong D, van Pel M, Cleton-Jansen AM and Hogendoorn PC: Osteosarcoma originates from mesenchymal stem cells in consequence of aneuploidization and genomic loss of Cdkn2. J Pathol 219: 294-305, 2009.
25. Li N, Yang R, Zhang W, Dorfman H, Rao P and Gorlick R: Genetically transforming human mesenchymal stem cells to sarcomas: changes in cellular phenotype and multilineage differentiation potential. Cancer 115: 4795-4806, 2009.
26. Xu W-T, Bian Z-Y, Fan Q-M, Li G and Tang T-T: Human mesenchymal stem cells (hMSCs) target osteosarcoma and promote its growth and pulmonary metastasis. Cancer Lett 281: 32-41, 2009.
27. Honoki K, Tsutsumi M, Miyauchi Y, Mii Y, Tsujiuchi T, Morishita T, Miura S, Aoki M, Kobayashi E, Tamai S and Konishi Y: Increased expression of nucleoside diphosphate kinase/nm23 and c-Ha-ras mRNA is associated with spontaneous lung metastasis in rat-transplantable osteosarcomas. Cancer Res 53: 5038-5042, 1993. (Pubitemid 23326206)
28. Honoki K, Mori T, Tsutsumi M, Tsujiuchi T, Kido A, Morishita T, Miyauchi Y, Dohi Y, Mii Y, Tamai S and Konishi Y: Heterogeneous pattern of gene expression in cloned cell lines established from a rat transplantable osteosarcoma lung metastatic nodule. Cancer Lett 127: 221-228, 1998. (Pubitemid 28230807)
29. Tohma Y, Ohgushi H, Morishita T, Dohi Y, Tadokoro M, Tanaka Y and Takakura Y: Bone marrow-derived mesenchymal cells can rescue osteogenic capacity of devitalized autologous bone. J Tissue Eng Regen Med 2: 61-68, 2008.
30. Luu HH, Kang Q, Park JK, Si W, Luo Q, Jiang W, Yin H, Montag AG, Simon MA, Peabody TD, Haydon RC, Rinker-Schaeffer CW and He TC: An orthotopic model of human osteosarcoma growth and spontaneous pulmonary metastasis. Clin Exp Metastastasis 22: 319-329, 2005. (Pubitemid 41374288)
31. Mueller MM and Fusenig NE: Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 11: 839-849, 2004. (Pubitemid 39472951)
32. Roorda BD, ter Elst A, Kamps WA and De Bont ES: Bone marrow-derived cells and tumor growth: contribution of bone marrow-derived cells to tumor microenvironments with special focus on mesenchymal stem cells. Crit Rev Oncol Hematol 3: 187-198, 2009.
33. Relf M, Lejeune S, Scott PA, Fox S, Smith K, Leek R, Moghaddam A, Whitehouse R, Bicknell R and Harris AL: Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 57: 963-969, 1997. (Pubitemid 27098025)
34. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH and Verfaillie CM: Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109: 337-346, 2002. (Pubitemid 34141807)
35. Roorda BD, ter Elst A, Meeuwsen-de Boer TGJ, Kamps WA and De Bont ESJM: Mesenchymal stem cells contribute to tumor cell proliferation by direct cell-cell contact interactions. Cancer Invest Early Online: 1-9, 2010.
36. Kyriakou C, Rabin N, Pizzey A, Nathwani A and Yong K: Factors that influence short-term homing ofhuman bne marrowderived mesenchymal stem cells in a xenogenic animal model. Hematologica 93: 1457-1465, 2008.
37. Fernadez M, Simon V, Herrera G, Cao C, del Favero H and Minguell JJ: Detection of stromal cells in peripheral blood progenitor cell collections from breast cancer patients. Bone Marrow Transplant 20: 265-271, 1997. (Pubitemid 27389234)
38. Bian Z-Y, Li G, Gan Y-G, Hao Y-Q, Xu W-T and Tang T-T: Increased number of mesenchymal stem cell-like cells in peripheral blood of patients with bone sarcomas. Arch Med Res 40: 163-168, 2009.
39. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S and Gianni AM: Human bone marrow stroma cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99: 3838-3843, 2002. (Pubitemid 34534559)
40. Rasmusson I: Immune modulation by mesenchymal stem cells. Exp Cell Res 312: 2169-2217, 2006.
41. Glennie S, Soeiro I, Dyson PJ, Lam EW-F and Dazziet F: Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105: 2821-2827, 2005. (Pubitemid 40446275)
42. Corcione A, Benvenuto F, Ferretti E, Giunti D, Cappiello V, Cazzanti F, Risso M, Gualandi F, Mancardi GL, Pistoia V and Uccelli A: Human mesenchymal stem cells modulate B-cell functions. Blood 107: 367-372, 2006. (Pubitemid 43053565)
43. Rasmusson I, Ringden O, Sundberg B and Le Blanc K: Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activates cytotoxic T lymphocytes or natural killer cells. Transplantation 76: 1208-1213, 2003. (Pubitemid 37339646)
44. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD and Mao N: Human mesencymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105: 4120- 4126, 2005.
45. Aggarwal S and Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822, 2005. (Pubitemid 40223708)
46. Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR and Mosca JD: Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci 10: 228-241, 2003. (Pubitemid 36302404)
47. Hood JD and Cheresh DA: Role of integrins in cell invasion and migration. Nat Rev Cancer 2: 91-100, 2002. (Pubitemid 37328796)
48. Falcioni R, Sacchi A, Resau J and Kennel SJ: Monoclonal antibody to human carcinoma-associated protein complex: quantitation in normal and tumor tissue. Cancer Res 48: 816-821, 1988. (Pubitemid 18061869)
49. Wan X, Kim S-Y, Guenther LM, Mendoza A, Briggs J, Yeung C, Currier D, Zhang H, Mackall C, Li W-J, Tuan RS, Deyrup AT, Khanna C and Helman J: Beta4 integrin promotes osteosarcoma metastasis and interacts with ezrin. Oncogene 28: 3401-3411, 2009.
50. Simiantonaki N, Jayasinghe C and Kirkpatrick CJ: Differential endothelial CAM-expression after stimulation with supernatants of LPS-and cytokine-stimulated HT-29 and ST-ML-12 tumor cells growing as monolayer cultures and multicellular spheroids. Anticancer Res 22: 2641-2649, 2002. (Pubitemid 36069292)
51. Balkwill F: Cancer and chemokine network. Nat Rev Cancer 4: 540-550, 2004.
52. Luker K and Luker G: Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett 238: 30-40, 2006.
53. Burns JM, Summers BC, Wang Y, Melikian A, Berahovich R, Miao Z, Penfold MET, Sunshine MJ, Littman DR, Kuo CJ, Wei K, McMaster BE, Wright K, Howard MC and Shall TJ: A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. J Exp Med 203: 2201-2213, 2006. (Pubitemid 44352240)
54. Miao Z, Luker KE, Summers BC, Berahovich R, Bhojan MS, Rehemtula A, Kleer CG, Essner JJ, Nasevicius A, Luker GD, Howard MC and Schall TJ: CXCR7 (RDC1) promotes breast and lung tumor growth in vivo and is expressed on tumor-associated vasculature. Proc Natl Acad Sci USA 104: 15735-15740, 2007. (Pubitemid 350035369)
55. Honoki K: Do stem-like cells play a role in drug resistance of sarcomas? Expert Rev Anticancer Ther 10: 261-270, 2010.
56. Liu A, Ginestier C, Ou SJ, Clouthier SG, Patel SH, Monville F, Korkaya H, Heath A, Dutcher J, Kleer CG, Jung Y, Dontu G, Taichman R and Wich MS: Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res 71: 614-624, 2011.