Epithelial-mesenchymal transition of ovarian tumor cells induces an angiogenic monocyte cell population

Experimental Cell Research

Volumn 315, Issue 17, 2009, Pages 2982-2994

  Collino, Federica ^a   Revelli, Alberto ^b   Massobrio, Marco ^b   Katsaros, Dionyssios ^b   Schmitt Ney, Michel ^a   Camussi, Giovanni ^a   Bussolati, Benedetta ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Angiogenesis; Monocyte differentiation; Pleiotrophin; Vasculogenesis; VEGF

Indexed keywords

CD14 ANTIGEN; PLEIOTROPHIN; VASCULOTROPIN RECEPTOR 2;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CARCINOGENESIS; CELL DIFFERENTIATION; CELL MIGRATION; CELL STIMULATION; CLINICAL ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; METASTASIS; MONOCYTE; OVARY ADENOCARCINOMA; OVARY TUMOR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR DIFFERENTIATION; TUMOR VASCULARIZATION;

EID: 70349595093     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.06.010     Document Type: Article

References (40)

1. Boyer B., Valles A.M., and Edme N. Induction and regulation of epithelial-mesenchymal transitions. Biochem. Pharmacol. 60 (2000) 1091-1099
2. Yang J., and Weinberg R.A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell. 14 (2008) 818-829
3. Reyes M., Dudek A., Jahagirdar B., Koodie L., Marker P.H., and Verfaillie C.M. Origin of endothelial progenitors in human postnatal bone marrow. J. Clin. Invest. 109 (2002) 337-346
4. Carmeliet P., and Jain R.K. Angiogenesis in cancer and other diseases. Nature 407 (2000) 249-257
5. Rafii S. Circulating endothelial precursors: mystery, reality, and promise. J. Clin. Invest. 105 (2000) 17-19
6. Asahara T., Murohara T., Sullivan A., Silver M., van der Zee R., Li T., Witzenbichler B., Schatteman G., and Isner J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997) 964-967
7. Peichev M., Naiyer A.J., Pereira D., Zhu Z., Lane W.J., Williams M., Oz M.C., Hicklin D.J., Witte L., Moore M.A., and Rafii S. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95 (2000) 952-958
8. Fernandez Pujol B., Lucibello F.C., Gehling U.M., Lindemann K., Weidner N., Zuzarte M.L., Adamkiewicz J., Elsasser H.P., Muller R., and Havemann K. Endothelial-like cells derived from human CD14 positive monocytes. Differentiation 65 (2000) 287-300
9. Kuwana M., Okazaki Y., Kodama H., Satoh T., Kawakami Y., and Ikeda Y. Endothelial differentiation potential of human monocyte-derived multipotential cells. Stem Cells 24 (2006) 2733-2743
10. Yamaguchi J., Kusano K.F., Masuo O., Kawamoto A., Silver M., Murasawa S., Bosch-Marce M., Masuda H., Losordo D.W., Isner J.M., and Asahara T. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107 (2003) 1322-1328
11. Harraz M., Jiao C., Hanlon H.D., Hartley R.S., and Schatteman G.C. CD34-blood-derived human endothelial cell progenitors. Stem Cells 19 (2001) 304-312
12. Sharpe III E.E., Teleron A.A., Li B., Price J., Sands M.S., Alford K., and Young P.P. The origin and in vivo significance of murine and human culture-expanded endothelial progenitor cells. Am. J. Pathol. 168 (2006) 1710-1721
13. Conejo-Garcia J.R., Buckanovich R.J., Benencia F., Courreges M.C., Rubin S.C., Carroll R.G., and Coukos G. Vascular leukocytes contribute to tumor vascularization. Blood 105 (2005) 679-681
14. Kusumbe A.P., Mali A.M., and Bapat S.A. CD133-expressing stem cells associated with ovarian metastases establish an endothelial hierarchy and contribute to tumor vasculature. Stem Cells 27 (2009) 498-508
15. Heintz A.P., Odicino F., Maisonneuve P., Quinn M.A., Benedet J.L., Creasman W.T., Ngan H.Y., Pecorelli S., and Beller U. Carcinoma of the ovary. FIGO 6th Annual Report on the Results of Treatment in Gynecological Cancer. Int. J. Gynaecol. Obstet. 95 Suppl. 1 (2006) S161-S192
16. Dunfield L.D., Shepherd T.G., and Nachtigal M.W. Primary culture and mRNA analysis of human ovarian cells. Biol. Proced. Online 4 (2002) 55-61
17. Ahmed N., Maines-Bandiera S., Quinn M.A., Unger W.G., Dedhar S., and Auersperg N. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am. J. Physiol. Cell. Physiol. 290 (2006) C1532-C1542
18. Ahmed N., Pansino F., Baker M., Rice G., and Quinn M. Association between alphavbeta6 integrin expression, elevated p42/44 kDa MAPK, and plasminogen-dependent matrix degradation in ovarian cancer. J. Cell. Biochem. 84 (2002) 675-686
19. Bruno S., Bussolati B., Scacciatella P., Marra S., Sanavio F., Tarella C., and Camussi G. Combined administration of G-CSF and GM-CSF stimulates monocyte-derived pro-angiogenic cells in patients with acute myocardial infarction. Cytokine 34 (2006) 56-65
20. Fonsato V., Buttiglieri S., Deregibus M.C., Bussolati B., Caselli E., Di Luca D., and Camussi G. PAX2 expression by HHV-8-infected endothelial cells induced a proangiogenic and proinvasive phenotype. Blood 111 (2008) 2806-2815
21. Schmeisser A., Garlichs C.D., Zhang H., Eskafi S., Graffy C., Ludwig J., Strasser R.H., and Daniel W.G. Monocytes coexpress endothelial and macrophagocytic lineage markers and form cord-like structures in Matrigel under angiogenic conditions. Cardiovasc. Res. 49 (2001) 671-680
22. Urbich C., Heeschen C., Aicher A., Dernbach E., Zeiher A.M., and Dimmeler S. Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108 (2003) 2511-2516
23. Salamanca C.M., Maines-Bandiera S.L., Leung P.C., Hu Y.L., and Auersperg N. Effects of epidermal growth factor/hydrocortisone on the growth and differentiation of human ovarian surface epithelium. J. Soc. Gynecol. Investig. 11 (2004) 241-251
24. Kurrey N.K., K.A., and Bapat S.A. Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol. 97 (2005) 155-165
25. Elloul S., Silins I., Trope C.G., Benshushan A., Davidson B., and Reich R. Expression of E-cadherin transcriptional regulators in ovarian carcinoma. Virchows Arch. 449 (2006) 520-528
26. Horrevoets A.J. Angiogenic monocytes: another colorful blow to endothelial progenitors. Am. J. Pathol. 174 (2009) 1594-1596
27. Kim S.J., Kim J.S., Papadopoulos J., Wook Kim S., Maya M., Zhang F., He J., Fan D., Langley R., and Fidler I.J. Circulating monocytes expressing CD31: implications for acute and chronic angiogenesis. Am. J. Pathol. 174 (2009) 1972-1980
28. Bharadwaj U., Li M., Zhang R., Chen C., and Yao Q. Elevated interleukin-6 and G-CSF in human pancreatic cancer cell conditioned medium suppress dendritic cell differentiation and activation. Cancer Res. 67 (2007) 5479-5488
29. Kaplan R.N., Riba R.D., Zacharoulis S., Bramley A.H., Vincent L., Costa C., MacDonald D.D., Jin D.K., Shido K., Kerns S.A., Zhu Z., Hicklin D., Wu Y., Port J.L., Altorki N., Port E.R., Ruggero D., Shmelkov S.V., Jensen K.K., Rafii S., and Lyden D. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438 (2005) 820-827
30. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel). 154 (1995) 8-20
31. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2 (2002) 442-454
32. Ding J.X., Feng Y.J., Yao L.Q., Yu M., Jin H.Y., and Yin L.H. The reinforcement of invasion in epithelial ovarian cancer cells by 17 beta-estradiol is associated with up-regulation of Snail. Gynecol. Oncol. 103 (2006) 623-630
33. Peinado H., Marin F., Cubillo E., Stark H.J., Fusenig N., Nieto M.A., and Cano A. Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo. J. Cell. Sci. 117 (2004) 2827-2839
34. Mironchik Y., Winnard Jr. P.T., Vesuna F., Kato Y., Wildes F., Pathak A.P., Kominsky S., Artemov D., Bhujwalla Z., Van Diest P., Burger H., Glackin C., and Raman V. Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res. 65 (2005) 10801-10809
35. Higashikawa K., Yoneda S., Taki M., Shigeishi H., Ono S., Tobiume K., and Kamata N. Gene expression profiling to identify genes associated with high-invasiveness in human squamous cell carcinoma with epithelial-to-mesenchymal transition. Cancer Lett. 264 (2008) 256-264
36. Chen H., Campbell R.A., Chang Y., Li M., Wang C.S., Li J., Sanchez E., Share M., Steinberg J., Berenson A., Shalitin D., Zeng Z., Gui D., Perez-Pinera P., Berenson R.J., Said J., Bonavida B., Deuel T.F., and Berenson J.R. Pleiotrophin produced by multiple myeloma induces transdifferentiation of monocytes into vascular endothelial cells: a novel mechanism of tumor-induced vasculogenesis. Blood 113 (2009) 1992-2002
37. Bergers G., and Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 8 (2008) 592-603
38. Ebos J.M., Lee C.R., Cruz-Munoz W., Bjarnason G.A., Christensen J.G., and Kerbel R.S. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 15 (2009) 232-239
39. Kerbel R.S. Tumor angiogenesis. N. Engl. J. Med. 358 (2008) 2039-2049
40. Paez-Ribes M., Allen E., Hudock J., Takeda T., Okuyama H., Vinals F., Inoue M., Bergers G., Hanahan D., and Casanovas O. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 15 (2009) 220-231