Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production

Journal of Clinical Investigation

Volumn 121, Issue 8, 2011, Pages 3206-3219

  McLean, Karen ^a   Gong, Yusong ^b   Choi, Yunjung ^b   Deng, Ning ^b   Yang, Kun ^b   Bai, Shoumei ^b   Cabrera, Lourdes ^a   Keller, Evan ^a   McCauley, Laurie ^a   Cho, Kathleen R ^a   Buckanovich, Ronald J ^a,b  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6;

ADIPOSE TISSUE CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE CELL; CANCER CELL CULTURE; CANCER STEM CELL; CARCINOGENESIS; CARTILAGE CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYMAL STEM CELL; NONHUMAN; OVARY CARCINOMA; OVARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; TUMOR GROWTH;

BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL SEPARATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MESENCHYMAL STEM CELLS; MODELS, BIOLOGICAL; NEOPLASTIC STEM CELLS; OVARIAN NEOPLASMS; PHENOTYPE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 79961006281     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI45273     Document Type: Article

References (58)

1. Stagg J. Mesenchymal stem cells in cancer. Stem Cell Reviews. 2008;4(2):119-124.
2. Qiao L, Xu Z-L, Zhao T-J, Ye L-H, Zhang X-D. Dkk-1 secreted by mesenchymal stem cells inhibits growth of breast cancer cells via depression of Wnt signalling. Cancer Letters. 2008;269(1):67-77.
3. Zhu Y, et al. Human mesenchymal stem cells inhibit cancer cell proliferation by secreting DKK-1. Leukemia. 2009;23(5):925-933.
4. Lu Y-R, et al. The growth inhibitory effect of mesenchymal stem cells on tumor cells in vitro and in vivo. Cancer Biol Ther. 2008;7(2):245-251. (Pubitemid 351590431)
5. Ramasamy R, Lam EWF, Soeiro I, Tisato V, Bonnet D, Dazzi F. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: impact on in vivo tumor growth. Leukemia. 2007;21(2):304-310. (Pubitemid 46158124)
6. Djouad F, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood. 2003;102(10):3837-3844. (Pubitemid 37409409)
7. Muehlberg FL, et al. Tissue-resident stem cells promote breast cancer growth and metastasis. Carcinogenesis. 2009;30(4):589-597.
8. Karnoub AE, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557-563. (Pubitemid 47525152)
9. Liu S, et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res. 2011;71(2):614-624.
10. Spaeth EL, et al. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS One. 2009;4(4):e4992.
11. Buckanovich RJ, et al. Tumor Vascular Proteins as Biomarkers in Ovarian Cancer. J Clin Oncol. 2007;25(7):852-861. (Pubitemid 350002886)
12. St Croix B, et al. Genes expressed in human tumor endothelium. Science. 2000;289(5482):1197-1202. (Pubitemid 30650733)
13. Haviv I, Polyak K, Qiu W, Hu M, Campbell I. Origin of carcinoma associated fibroblasts. Cell Cycle. 2009;8(4):589-595.
14. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metastasis Rev. 2006;25(3):315-322. (Pubitemid 44922352)
15. Arnulf B, et al. Phenotypic and functional characterization of bone marrow mesenchymal stem cells derived from patients with multiple myeloma. Leukemia. 2007;21(1):158-163. (Pubitemid 44921847)
16. Jootar S, et al. Bone marrow derived mesenchymal stem cells from chronic myeloid leukemia t(9;22) patients are devoid of Philadelphia chromosome and support cord blood stem cell expansion. Leuk Res. 2006;30(12):1493-1498. (Pubitemid 44573488)
17. Zhao Z-G, et al. Phenotypic and functional comparison of mesenchymal stem cells derived from the bone marrow of normal adults and patients with hematologic malignant diseases. Stem Cells Dev. 2007;16(4):637-648. (Pubitemid 47378736)
18. Garayoa M, et al. Mesenchymal stem cells from multiple myeloma patients display distinct genomic profile as compared with those from normal donors. Leukemia. 2009;23(8):1515-1527.
19. Gibbs CP, et al. Stem-like cells in bone sarcomas: implications for tumorigenesis. Neoplasia. 2005;7(11):967-976.
20. Lin TM, et al. Isolation and identification of mesenchymal stem cells from human lipoma tissue. Biochem Biophys Res Commun. 2007;361(4):883-889.
21. Yu Y, et al. Mesenchymal stem cells and adipogenesis in hemangioma involution. Stem Cells. 2006;24(6):1605-1612. (Pubitemid 44464678)
22. Matushansky I, et al. Derivation of sarcomas from mesenchymal stem cells via inactivation of the Wnt pathway. J Clin Invest. 2007;117(11):3248-3257. (Pubitemid 350096982)
23. Tasso R, et al. Development of sarcomas in mice implanted with mesenchymal stem cells seeded onto bioscaffolds. Carcinogenesis. 2009;30(1):150-157.
24. Chiba H, et al. CD105-positive cells in pulmonary arterial blood of adult human lung cancer patients include mesenchymal progenitors. Stem Cells. 2008;26(10):2523-2530.
25. Cao H, et al. Mesenchymal stem cell-like cells derived from human gastric cancer tissues. Cancer Lett. 2009;274(1):61-71.
26. Pittenger MF, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143-147. (Pubitemid 29282067)
27. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007;25(11):2739-2749. (Pubitemid 350127858)
28. Beckermann BM, et al. VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer. 2008;99(4):622-631.
29. Galie M, et al. Mesenchymal stem cells share molecular signature with mesenchymal tumor cells and favor early tumor growth in syngeneic mice. Oncogene. 2008;27(18):2542-2551. (Pubitemid 351550885)
30. Qiao L, et al. Suppression of tumorigenesis by human mesenchymal stem cells in a hepatoma model. Cell Res. 2008;18(4):500-507. (Pubitemid 351498857)
31. Deng S, et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One. 2010;5(4):e10277.
32. Silva IA, et al. Characterization of ovarian CSC using ALDH and CD133 identifies a cancer stem cell hierarchy. AACR Meeting Abstracts. 2010:403.
33. Hofer EL, et al. Mesenchymal stromal cells, colony-forming unit fibroblasts, from bone marrow of untreated advanced breast and lung cancer patients suppress fibroblast colony formation from healthy marrow. Stem Cells Dev. 2010;19(3):359-370.
34. Le Page C, et al. BMP-2 signaling in ovarian cancer and its association with poor prognosis. J Ovarian Res. 2009;2:4.
35. Chiba H, et al. CD105-positive cells in pulmonary arterial blood of adult human lung cancer patients include mesenchymal progenitors. Stem Cells. 2008;26(10):2523-2530.
36. Zhu W, et al. Mesenchymal stem cells derived from bone marrow favor tumor cell growth in vivo. Exp Mol Pathol. 2006;80(3):267-274.
37. Campioni D, Lanza F, Moretti S, Ferrari L, Cuneo A. Loss of Thy-1 (CD90) antigen expression on mesenchymal stromal cells from hematologic malignancies is induced by in vitro angiogenic stimuli and is associated with peculiar functional and phenotypic characteristics. Cytotherapy. 2008;10(1):69-82.
38. Waite KA, Eng C. From developmental disorder to heritable cancer: it's all in the BMP/TGF-beta family. Nat Rev Genet. 2003;4(10):763-773. (Pubitemid 37193268)
39. Theriault BL, Shepherd TG, Mujoomdar ML, Nachtigal MW. BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis. 2007;28(6):1153-1162. (Pubitemid 47062673)
40. Shepherd TG, Theriault BL, Nachtigal MW. Autocrine BMP4 signalling regulates ID3 proto-oncogene expression in human ovarian cancer cells. Gene. 2008;414(1-2):95-105.
41. Le Page C, et al. Gene expression profiling of primary cultures of ovarian epithelial cells identifies novel molecular classifiers of ovarian cancer. Br J Cancer. 2006;94(3):436-445. (Pubitemid 43237567)
42. Moll F, et al. Chordin is underexpressed in ovarian tumors and reduces tumor cell motility. FASEB J. 2006;20(2):240-250. (Pubitemid 44933171)
43. Ye L, Lewis-Russell JM, Kyanaston HG, Jiang WG. Bone morphogenetic proteins and their receptor signaling in prostate cancer. Histol Histopathol. 2007;22(10):1129-1147. (Pubitemid 47470307)
44. Fong YC, et al. BMP-2 increases migration of human chondrosarcoma cells via PI3K/Akt pathway. J Cell Physiol. 2008;217(3):846-855.
45. Rothhammer T, Poser I, Soncin F, Bataille F, Moser M, Bosserhoff AK. Bone morphogenic proteins are overexpressed in malignant melanoma and promote cell invasion and migration. Cancer Res. 2005;65(2):448-456.
46. Kang MH, Kim JS, Seo JE, Oh SC, Yoo YA. BMP2 accelerates the motility and invasiveness of gastric cancer cells via activation of the phosphatidylinositol 3-kinase (PI3K)/Akt pathway. Exp Cell Res. 2010;316(1):24-37.
47. Feeley BT, et al. Overexpression of noggin inhibits BMP-mediated growth of osteolytic prostate cancer lesions. Bone. 2006;38(2):154-166. (Pubitemid 43165781)
48. Feeley BT, et al. Mixed metastatic lung cancer lesions in bone are inhibited by noggin overexpression and Rank:Fc administration. J Bone Miner Res. 2006;21(10):1571-1580. (Pubitemid 44484602)
49. Kang Q, et al. A comprehensive analysis of the dual roles of BMPs in regulating adipogenic and osteogenic differentiation of mesenchymal progenitor cells. Stem Cells Dev. 2009;18(4):545-559.
50. Burkill GJ, Allen SD, A'Hern R P, Gore ME, King DM. Significance of tumour calcification in ovarian carcinoma. Br J Radiol. 2009;82(980):640-644.
51. Okada S, et al. Calcifications in mucinous and serous cystic ovarian tumors. J Nippon Med Sch. 2005;72(1):29-33. (Pubitemid 41379455)
52. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. Efficient tumour formation by single human melanoma cells. Nature. 2008;456(7222):593-598.
53. Giannoni E, et al. Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res. 2010;70(17):6945-6956.
54. Crisan M, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell. 2008;3(3):301-313.
55. Zhau HE, et al. Human prostate cancer harbors the stem cell properties of bone marrow mesenchymal stem cells. Clin Cancer Res. 2011;17(8):2159-2169.
56. Strauss R, et al. Analysis of epithelial and mesenchymal markers in ovarian cancer reveals phenotypic heterogeneity and plasticity. PLoS One. 2011;6(1):e16186.
57. Conejo-Garcia JR, et al. Vascular leukocytes contribute to tumor vascularization. Blood. 2005;105(2):679-681. (Pubitemid 40070752)
58. Pulaski HL, et al. Identifying alemtuzumab as an anti-myeloid cell antiangiogenic therapy for the treatment of ovarian cancer. J Transl Med. 2009;7:49.