Specific mesothelial signature marks the heterogeneity of mesenchymal stem cells from high-grade serous ovarian cancer

Stem Cells

Volumn 32, Issue 11, 2014, Pages 2998-3011

  Verardo, Roberto ^a   Piazza, Silvano ^a   Klaric, Enio ^a   Ciani, Yari ^a   Bussadori, Giulio ^a   Marzinotto, Stefania ^b   Mariuzzi, Laura ^b   Cesselli, Daniela ^b   Beltrami, Antonio P ^b   Mano, Miguel ^c   Itoh, Masayoshi ^d   Kawaji, Hideya ^d   Lassmann, Timo ^d   Carninci, Piero ^d   Hayashizaki, Yoshihide ^d   Forrest, Alistair R R ^d   Beltrami, Carlo A ^c   Schneider, Claudio ^a,c  

^a CBM Srl Area Science Park   (Italy)

^b UNIVERSITY OF UDINE   (Italy)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^d RIKEN   (Japan)

Author keywords

Adult stem cells; Cancer; Cell biology; Genomics; Mesenchymal stem cells; Tissue specific stem cells

Indexed keywords

CELL DIFFERENTIATION; CYTOLOGY; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; METABOLISM; METHODS; NEOPLASM GRADING; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASMS, MESOTHELIAL; OVARIAN NEOPLASMS; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

CELL DIFFERENTIATION; FEMALE; HUMANS; MESENCHYMAL STROMAL CELLS; NEOPLASM GRADING; NEOPLASMS, GLANDULAR AND EPITHELIAL; NEOPLASMS, MESOTHELIAL; OVARIAN NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84907904181     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1791     Document Type: Article

References (78)

1. Uccelli A, Moretta L, Pistoia V,. Mesenchymal stem cells in health and disease. Nat Rev Immunol 2008; 8: 726-36.
2. Silva Meirelles L da, Chagastelles PC, Nardi NB,. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006; 119: 2204-13.
3. Nombela-Arrieta C, Ritz J, Silberstein LE,. The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol 2011; 12: 126-31.
4. Méndez-Ferrer S, Michurina T V, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010; 466: 829-34.
5. Bianco P,. Bone and the hematopoietic niche: a tale of two stem cells. Blood 2011; 117: 5281-8.
6. Scadden DT,. Rethinking stroma: lessons from the blood. Cell Stem Cell 2012; 10: 648-9.
7. Caplan AI, Correa D,. The MSC: an injury drugstore. Cell Stem Cell 2011; 9: 11-5.
8. Hanahan D, Weinberg RA,. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
9. Hanahan D, Coussens LM,. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-22.
10. Chen L, Tredget EE, Wu PYG, et al. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008; 3: e1886.
11. Tian LLH, Yue W, Zhu F, et al. Human mesenchymal stem cells play a dual role on tumor cell growth in vitro and in vivo. J Cell Physiol 2011; 226: 1860-1867.
12. Ren G, Zhao X, Wang Y, et al. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFα. Cell Stem Cell 2012; 11: 812-24.
13. Marx J,. Cancer biology. All in the stroma: cancer's Cosa Nostra. Science 2008; 320: 38-41.
14. Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 2007; 449: 557-63.
15. Bourkoula E, Mangoni D, Ius T, et al. Glioma-associated stem cells: A novel class of tumor-supporting cells able to predict prognosis of human low-grade gliomas. Stem Cells 2013.
16. Spaeth EL, Dembinski JL, Sasser AK, et al. Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS One 2009; 4: e4992.
17. Lis R, Touboul C, Mirshahi P, et al. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer 2011; 128: 715-25.
18. McLean K, Gong Y, Choi Y, et al. Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. J Clin Invest 2011; 121: 3206-19.
19. Lis R, Touboul C, Raynaud CM, et al. Mesenchymal cell interaction with ovarian cancer cells triggers pro-metastatic properties. PLoS One 2012; 7: e38340.
20. Touboul C, Lis R, Farsi H Al, et al. Mesenchymal stem cells enhance ovarian cancer cell infiltration through IL6 secretion in an amniochorionic membrane based 3D model. J Transl Med 2013; 11: 28.
21. Xu X, Zhang X, Wang S, et al. Isolation and comparison of mesenchymal stem-like cells from human gastric cancer and adjacent non-cancerous tissues. J Cancer Res Clin Oncol 2011; 137: 495-504.
22. Yan X-L, Jia Y-L, Chen L, et al. Hepatocellular carcinoma-associated mesenchymal stem cells promote hepatocarcinoma progression: role of the S100A4-miR155-SOCS1-MMP9 axis. Hepatology 2013; 57: 2274-86.
23. Zhang C, Zhai W, Xie Y, et al,. Mesenchymal stem cells derived from breast cancer tissue promote the proliferation and migration of the MCF-7 cell line in vitro. Oncol Lett 2013; 6: 1577-1582.
24. Gottschling S, Granzow M, Kuner R, et al. Mesenchymal stem cells in non-small cell lung cancer-different from others?. Insights from comparative molecular and functional analyses. Lung Cancer 2013; 80: 19-29.
25. Beltrami AP, Cesselli D, Bergamin N, et al. Multipotent cells can be generated in vitro from several adult human organs (heart, liver, and bone marrow). Blood 2007; 110: 3438-3446.
26. Cesselli D, Beltrami AP, Rigo S, et al,. Multipotent progenitor cells are present in human peripheral blood. Circ Res 2009; 104: 1225-1234.
27. Carvalho B, Bengtsson H, Speed TP, et al. Exploration, normalization, and genotype calls of high-density oligonucleotide SNP array data. Biostatistics 2007; 8: 485-99.
28. Eisen MB, Spellman PT, Brown PO, et al. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998; 95: 14863-8.
29. Saldanha AJ,. Java Treeview - extensible visualization of microarray data. Bioinformatics 2004; 20: 3246-8.
30. Huang DW, Sherman BT, Lempicki RA,. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
31. Gyorffy B, Lánczky A, Szállási Z,. Implementing an online tool for genome-wide validation of survival-associated biomarkers in ovarian-cancer using microarray data from 1287 patients. Endocr Relat Cancer 2012; 19: 197-208.
32. Györffy B, Lanczky A, Eklund AC, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 2010; 123: 725-31.
33. GyÅrffy B, Surowiak P, Budczies J, et al. Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer. Chellappan SP, ed. PLoS One 2013; 8: e82241.
34. Zeppieri M, Salvetat ML, Beltrami AP, et al. Human adipose-derived stem cells for the treatment of chemically burned rat cornea: preliminary results. Curr Eye Res 2013; 38: 451-63.
35. Qiu W, Hu M, Sridhar A, et al. No evidence of clonal somatic genetic alterations in cancer-associated fibroblasts from human breast and ovarian carcinomas. Nat Genet 2008; 40: 650-5.
36. Forrest ARR, Kawaji H, Rehli M, et al. A promoter-level mammalian expression atlas. Nature 2014; 507: 462-70.
37. Kanamori-Katayama M, Itoh M, Kawaji H, et al. Unamplified cap analysis of gene expression on a single-molecule sequencer. Genome Res 2011; 21: 1150-9.
38. Robinson MD, McCarthy DJ, Smyth GK,. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26: 139-40.
39. Huang DW, Sherman BT, Lempicki RA,. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
40. Rinkevich Y, Mori T, Sahoo D, et al. Identification and prospective isolation of a mesothelial precursor lineage giving rise to smooth muscle cells and fibroblasts for mammalian internal organs, and their vasculature. Nat Cell Biol 2012; 14: 1251-60.
41. Connell ND, Rheinwald JG,. Regulation of the cytoskeleton in mesothelial cells: reversible loss of keratin and increase in vimentin during rapid growth in culture. Cell 1983; 34: 245-53.
42. Onder TT, Kara N, Cherry A, et al. Chromatin-modifying enzymes as modulators of reprogramming. Nature 2012; 483: 598-602.
43. Liberzon A, Subramanian A, Pinchback R, et al. Molecular signatures database (MSigDB) 3.0. Bioinformatics 2011; 27: 1739-40.
44. Pontén F, Jirström K, Uhlen M,. The Human Protein Atlas - a tool for pathology. J Pathol 2008; 216: 387-93.
45. Barberis MC, Faleri M, Veronese S, et al. Calretinin. A selective marker of normal and neoplastic mesothelial cells in serous effusions. Acta Cytol 41: 1757-61.
46. Tigrani D-Y, Weydert JA,. Immunohistochemical expression of osteopontin in epithelioid mesotheliomas and reactive mesothelial proliferations. Am J Clin Pathol 2007; 127: 580-4.
47. LaRocca PJ, Rheinwald JG,. Coexpression of simple epithelial keratins and vimentin by human mesothelium and mesothelioma in vivo and in culture. Cancer Res 1984; 44: 2991-9.
48. Kachali C, Eltoum I, Horton D, et al. Use of mesothelin as a marker for mesothelial cells in cytologic specimens. Semin Diagn Pathol 2006; 23: 20-4.
49. Taniguchi S, Takeoka M, Ehara T, et al. Structural Fragility of Blood Vessels and Peritoneum in Calponin h1-deficient Mice, Resulting in an Increase in Hematogenous Metastasis and Peritoneal Dissemination of Malignant Tumor Cells. Cancer Res 2001; 61: 7627-7634.
50. Kanamori-Katayama M, Kaiho A, Ishizu Y, et al. LRRN4 and UPK3B are markers of primary mesothelial cells. PLoS One 2011; 6: e25391.
51. Park J-H, Kim Y-G, Shaw M, et al. Nod1/RICK and TLR signaling regulate chemokine and antimicrobial innate immune responses in mesothelial cells. J Immunol 2007; 179: 514-21.
52. Ksiazek K, Mikula-Pietrasik J, Korybalska K, et al. Senescent peritoneal mesothelial cells promote ovarian cancer cell adhesion: the role of oxidative stress-induced fibronectin. Am J Pathol 2009; 174: 1230-40.
53. Bidlingmaier S, He J, Wang Y, et al. Identification of MCAM/CD146 as the target antigen of a human monoclonal antibody that recognizes both epithelioid and sarcomatoid types of mesothelioma. Cancer Res 2009; 69: 1570-7.
54. Sato A, Torii I, Okamura Y, et al. Immunocytochemistry of CD146 is useful to discriminate between malignant pleural mesothelioma and reactive mesothelium. Mod Pathol 2010; 23: 1458-66.
55. Wagner W, Wein F, Seckinger A, et al. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005; 33: 1402-16.
56. Dominici M, Blanc K Le, Mueller I, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-7.
57. Anderson P, Carrillo-Gálvez AB, García-Pérez A, et al. CD105 (endoglin)-negative murine mesenchymal stromal cells define a new multipotent subpopulation with distinct differentiation and immunomodulatory capacities. PLoS One 2013; 8: e76979.
58. Wang Z, Yan X,. CD146, a multi-functional molecule beyond adhesion. Cancer Lett 2013; 330: 150-62.
59. Zeng Q, Li W, Lu D, et al. CD146, an epithelial-mesenchymal transition inducer, is associated with triple-negative breast cancer. Proc Natl Acad Sci USA 2012; 109: 1127-32.
60. Aldovini D, Demichelis F, Doglioni C, et al. M-CAM expression as marker of poor prognosis in epithelial ovarian cancer. Int J Cancer 2006; 119: 1920-6.
61. Espagnolle N, Guilloton F, Deschaseaux F, et al. CD146 expression on mesenchymal stem cells is associated with their vascular smooth muscle commitment. J Cell Mol Med 2014; 18: 104-14.
62. Crisan M, Yap S, Casteilla L, et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3: 301-13.
63. Tormin A, Li O, Brune JC, et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 2011; 117: 5067-77.
64. Pelekanos R a, Li J, Gongora M, et al. Comprehensive transcriptome and immunophenotype analysis of renal and cardiac MSC-like populations supports strong congruence with bone marrow MSC despite maintenance of distinct identities. Stem Cell Res 2012; 8: 58-73.
65. Sági B, Maraghechi P, Urbán VS, et al. Positional identity of murine mesenchymal stem cells resident in different organs is determined in the postsegmentation mesoderm. Stem Cells Dev 2012; 21: 814-28.
66. Chong JJH, Chandrakanthan V, Xaymardan M, et al. Adult Cardiac-Resident MSC-like Stem Cells with a Proepicardial Origin. Cell Stem Cell 2011; 9: 527-40.
67. Gaebel R, Furlani D, Sorg H, et al. Cell origin of human mesenchymal stem cells determines a different healing performance in cardiac regeneration. PLoS One 2011; 6: e15652.
68. Lai C-F, Cheng S-L,. Signal transductions induced by bone morphogenetic protein-2 and transforming growth factor-beta in normal human osteoblastic cells. J Biol Chem 2002; 277: 15514-22.
69. Varoga D, Paulsen F, Mentlein R, et al. TLR-2-mediated induction of vascular endothelial growth factor (VEGF) in cartilage in septic joint disease. J Pathol 2006; 210: 315-24.
70. Cho M-L, Ju J-H, Kim H-R, et al. Toll-like receptor 2 ligand mediates the upregulation of angiogenic factor, vascular endothelial growth factor and interleukin-8/CXCL8 in human rheumatoid synovial fibroblasts. Immunol. Lett 2007; 108: 121-8.
71. Philip S,. Osteopontin Stimulates Tumor Growth and Activation of Promatrix Metalloproteinase-2 through Nuclear Factor-kappa B-mediated Induction of Membrane Type 1 Matrix Metalloproteinase in Murine Melanoma Cells. J Biol Chem 2001; 276: 44926-44935.
72. Xu G, Nie H, Li N, et al. Role of osteopontin in amplification and perpetuation of rheumatoid synovitis. J Clin Invest 2005; 115: 1060-7.
73. Levanon K, Crum C, Drapkin R,. New insights into the pathogenesis of serous ovarian cancer and its clinical impact. J Clin Oncol 2008; 26: 5284-93.
74. Berek JS, Crum C, Friedlander M,. Cancer of the ovary, fallopian tube, and peritoneum. Int J Gynaecol Obstet 2012; 119 Suppl: S118-29.
75. Auersperg N,. The origin of ovarian cancers - hypotheses and controversies. Front Biosci (Schol. Ed) 2013; 5: 709-19.
76. Karst AM, Levanon K, Drapkin R,. Modeling high-grade serous ovarian carcinogenesis from the fallopian tube. Proc Natl Acad Sci USA 2011; 108: 7547-52.
77. Kim J, Coffey DM, Creighton CJ, et al. High-grade serous ovarian cancer arises from fallopian tube in a mouse model. Proc Natl Acad Sci USA 2012; 109: 3921-6.
78. Ko SY, Barengo N, Ladanyi A, et al. HOXA9 promotes ovarian cancer growth by stimulating cancer-associated fibroblasts. J Clin Invest 2012; 122: 3603-17.