HIF-1α inhibition blocks the cross talk between multiple myeloma plasma cells and tumor microenvironment

Experimental Cell Research

Volumn 328, Issue 2, 2014, Pages 444-455

  Borsi, Enrica ^a   Perrone, Giulia ^b   Terragna, Carolina ^a   Martello, Marina ^a   Zamagni, Elena ^a   Tacchetti, Paola ^a   Pantani, Lucia ^a   Brioli, Annamaria ^a   Dico, Angela Flores ^a   Zannetti, Beatrice Anna ^a   Rocchi, Serena ^a   Cavo, Michele ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Cell adhesion; HIF 1 ; MAPKs; Multiple myeloma; Tumor microenvironment

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; EZN 2968; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; SCLEROPROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; HIF1A PROTEIN, HUMAN; OLIGONUCLEOTIDE;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BONE MARROW STROMA CELL; CELL ADHESION; CELL INTERACTION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MULTIPLE MYELOMA; PLASMA CELL; PROTEIN DEPLETION; REDUCTION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANTAGONISTS AND INHIBITORS; BONE MARROW CELL; CELL PROLIFERATION; DRUG EFFECTS; METABOLISM; TUMOR CELL LINE;

BONE MARROW CELLS; CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; COCULTURE TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERLEUKIN-6; MULTIPLE MYELOMA; OLIGONUCLEOTIDES; OLIGONUCLEOTIDES, ANTISENSE; PLASMA CELLS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84908192338     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.09.018     Document Type: Article

References (42)

1. Lemaire M., Deleu S., De Bruyne E., Van Valckenborgh E., Menu E., Vanderkerken K. The microenvironment and molecular biology of the multiple myeloma tumor. Adv. Cancer Res. 2011, 110:19-42.
2. Klein B., Seckinger A., Moehler T., Hose D. Molecular pathogenesis of multiple myeloma: chromosomal aberrations, changes in gene expression, cytokine networks, and the bone marrow microenvironment. Recent Results Cancer Res. 2011, 183:39-86.
3. Anderson K.C., Carrasco R.D. Pathogenesis of myeloma. Annu. Rev. Pathol. 2011, 6:249-274.
4. Shain K.H., Yarde D.N., Meads M.B., Huang M., Jove R., Hazlehurst L.A., Dalton W.S. Beta1 integrin adhesion enhances IL-6-mediated STAT3 signaling in myeloma cells: implications for microenvironment influence on tumor survival and proliferation. Cancer Res. 2009, 69:1009-1015.
5. Dalton W.S. The tumor microenvironment: focus on myeloma. Cancer Treat. Rev. 2003, 29(Suppl 1):S11-S19.
6. Pennathur-Das R., Levitt L. Augmentation of in vitro human marrow erythropoiesis under physiological oxygen tensions is mediated by monocytes and T lymphocytes. Blood 1987, 69:899-907.
7. Graeber T.G., Osmanian C., Jacks T., Housman D.E., Koch C.J., Lowe S.W., Giaccia A.J. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 1996, 379:88-91.
8. Zhong H., De Marzo A.M., Laughner E., Lim M., Hilton D.A., Zagzag D., Buechler P., Isaacs W.B., Semenza G.L., Simons J.W. Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Res. 1999, 59:5830-5835.
9. Talks K.L., Turley H., Gatter K.C., Maxwell P.H., Pugh C.W., Ratcliffe P.J., Harris A.L. The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am. J. Pathol. 2000, 157:411-421.
10. Zundel W., Schindler C., Haas-Kogan D., Koong A., Kaper F., Chen E., Gottschalk A.R., Ryan H.E., Johnson R.S., Jefferson A.B., Stokoe D., Giaccia A.J. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 2000, 14:391-396.
11. Pollard P.J., Spencer-Dene B., Shukla D., Howarth K., Nye E., El-Bahrawy M., Deheragoda M., Joannou M., McDonald S., Martin A., Igarashi P., Varsani-Brown S., Rosewell I., Poulsom R., Maxwell P., Stamp G.W., Tomlinson I.P. Targeted inactivation of fh1 causes proliferative renal cyst development and activation of the hypoxia pathway. Cancer Cell 2007, 11:311-319.
12. Selak M.A., Armour S.M., MacKenzie E.D., Boulahbel H., Watson D.G., Mansfield K.D., Pan Y., Simon M.C., Thompson C.B., Gottlieb E. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
13. Kirito K., Fox N., Komatsu N., Kaushansky K. Thrombopoietin enhances expression of vascular endothelial growth factor (VEGF) in primitive hematopoietic cells through induction of HIF-1alpha. Blood 2005, 105:4258-4263.
14. Asosingh K., De Raeve H., de Ridder M., Storme G.A., Willems A., Van Riet I., Van Camp B., Vanderkerken K. Role of the hypoxic bone marrow microenvironment in 5T2MM murine myeloma tumor progression. Haematologica 2005, 90:810-817.
15. Lu L., Payvandi F., Wu L., Zhang L.H., Hariri R.J., Man H.W., Chen R.S., Muller G.W., Hughes C.C., Stirling D.I., Schafer P.H., Bartlett J.B. The anti-cancer drug lenalidomide inhibits angiogenesis and metastasis via multiple inhibitory effects on endothelial cell function in normoxic and hypoxic conditions. Microvasc. Res. 2009, 77:78-86.
16. Shin D., Chun Y.-S., Lee D., Huang L., Park J.-W. Bortezomib inhibits tumor adaptation to hypoxia by stimulating the FIH-mediated repression of hypoxia-inducible factor-1. Blood 2008, 111:3131-3136.
17. Greenberger L., Horak I., Filpula D., Sapra P., Westergaard M., Frydenlund H., Albaek C., Schrøder H., Ørum H. A RNA antagonist of hypoxia-inducible factor-1alpha, EZN-2968, inhibits tumor cell growth. Mol. Cancer Ther. 2008, 7:3598-3608.
18. Borsi E., Terragna C., Martello M., Dico A.F., Solaini G., Baracca A., Sgarbi G., Pasquinelli G., Valente S., Zamagni E., Tacchetti P., Martinelli G., Cavo M. Hypoxia inducible factor-1 alpha as a therapeutic target in multiple myeloma. Oncotarget 2014, 5(7):1779-1792.
19. Kawano M., Hirano T., Matsuda T., Taga T., Horii Y., Iwato K., Asaoku H., Tang B., Tanabe O., Tanaka H., et al. Autocrine generation and requirement of BSF-2/IL-6 for human multiple myelomas. Nature 1988, 332:83-85.
20. Neufeld G., Cohen T., Gengrinovitch S., Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999, 13:9-22.
21. Hideshima T., Catley L., Yasui H., Ishitsuka K., Raje N., Mitsiades C., Podar K., Munshi N.C., Chauhan D., Richardson P.G., Anderson K.C. Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells. Blood 2006, 107:4053-4062.
22. Semenza G.L. Life with oxygen. Science 2007, 318:62-64.
23. Rankin E.B., Giaccia A.J. The role of hypoxia-inducible factors in tumorigenesis. Cell Death Differ. 2008, 15:678-685.
24. Chaturvedi P., Gilkes D.M., Wong; C.C., W Kshitiz, Luo, Zhang H., Wei H., Takano N., Schito L., Levchenko A. G.L. Semenza, Hypoxia-inducible factor-dependent breast cancer-mesenchymal stem cell bidirectional signaling promotes metastasis. J. Clin. Invest. 2013, 123:189-205.
25. Chaturvedi P., Gilkes D.M., Takano N., Semenza G.L. Hypoxia-inducible factor-dependent signaling between triple-negative breast cancer cells and mesenchymal stem cells promotes macrophage recruitment. Proc. Natl. Acad. Sci. USA 2014, 111:E2120-E2129.
26. Jiang B.H., Agani F., Passaniti A., Semenza G.L. V-SRC induces expression of hypoxia-inducible factor 1 (HIF-1) and transcription of genes encoding vascular endothelial growth factor and enolase 1: involvement of HIF-1 in tumor progression. Cancer Res. 1997, 57:5328-5335.
27. Semenza G. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
28. Magagnin M.G., Koritzinsky M., Wouters B.G. Patterns of tumor oxygenation and their influence on the cellular hypoxic response and hypoxia-directed therapies. Drug Resist. Updates 2006, 9:185-197.
29. Colla S., Tagliaferri S., Morandi F., Lunghi P., Donofrio G., Martorana D., Mancini C., Lazzaretti M., Mazzera L., Ravanetti L., Bonomini S., Ferrari L., Miranda C., Ladetto M., Neri T., Neri A., Greco A., Mangoni M., Bonati A., Rizzoli V., Giuliani N. The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood 2007, 110:4464-4475.
30. Lee K.A., Roth R.A., LaPres J.J. Hypoxia, drug therapy and toxicity. Pharmacol. Ther. 2007, 113:229-246.
31. Hu Y., Kirito K., Yoshida K., Mitsumori T., Nakajima K., Nozaki Y., Hamanaka S., Nagashima T., Kunitama M., Sakoe K., Komatsu N. Inhibition of hypoxia-inducible factor-1 function enhances the sensitivity of multiple myeloma cells to melphalan. Mol. Cancer Ther. 2009, 8:2329-2338.
32. Semenza G. Evaluation of HIF-1 inhibitors as anticancer agents. Drug Discov. Today 2007, 12:853-859.
33. Storti P., Bolzoni M., Donofrio G., Airoldi I., Guasco D., Toscani D., Martella E., Lazzaretti M., Mancini C., Agnelli L., Patrene K., Maiga S., Franceschi V., Colla S., Anderson J., Neri A., Amiot M., Aversa F., David Roodman G., Giuliani N. Hypoxia-inducible factor (HIF)-1alpha suppression in myeloma cells blocks tumoral growth in vivo inhibiting angiogenesis and bone destruction. Leukemia 2013, 27:1697-1706.
34. Colla S., Storti P., Donofrio G., Todoerti K., Bolzoni M., Lazzaretti M., Abeltino M., Ippolito L., Neri A., Ribatti D., Rizzoli V., Martella E., Giuliani N. Low bone marrow oxygen tension and hypoxia-inducible factor-1alpha overexpression characterize patients with multiple myeloma: role on the transcriptional and proangiogenic profiles of CD138(+) cells. Leukemia 2010, 24:1967-1970.
35. Klein B., Zhang X.G., Jourdan M., Content J., Houssiau F., Aarden L., Piechaczyk M., Bataille R. Paracrine rather than autocrine regulation of myeloma-cell growth and differentiation by interleukin-6. Blood 1989, 73:517-526.
36. Anderson K.C., Jones R.M., Morimoto C., Leavitt P., Barut B.A. Response patterns of purified myeloma cells to hematopoietic growth factors. Blood 1989, 73:1915-1924.
37. Dankbar B., Padro T., Leo R., Feldmann B., Kropff M., Mesters R.M., Serve H., Berdel W.E., Kienast J. Vascular endothelial growth factor and interleukin-6 in paracrine tumor-stromal cell interactions in multiple myeloma. Blood 2000, 95:2630-2636.
38. Hideshima T., Chauhan D., Podar K., Schlossman R.L., Richardson P., Anderson K.C. Novel therapies targeting the myeloma cell and its bone marrow microenvironment. Semin. Oncol. 2001, 28:607-612.
39. Uchiyama H., Barut B.A., Mohrbacher A.F., Chauhan D., Anderson K.A. Adhesion of human myeloma-derived cell lines to bone marrow stromal cells stimulates interleukin-6 secretion. Blood 1993, 82:3712-3720.
40. Gupta D., Treon S.P., Shima Y., Hideshima T., Podar K., Tai Y.T., Lin B., Lentzsch S., Davies F.E., Chauhan D., Schlossman R.L., Richardson P., Ralph P., Wu L., Payvandi F., Muller G., Stirling D.I., Anderson K.C. Adherence of multiple myeloma cells to bone marrow stromal cells upregulates vascular endothelial growth factor secretion: therapeutic applications. Leukemia 2001, 15:1950-1961.
41. Teoh G., Anderson K.C. Interaction of tumor and host cells with adhesion and extracellular matrix molecules in the development of multiple myeloma. Hematol. Oncol. Clin. North Am. 1997, 11:27-42.
42. Abe M. Targeting the interplay between myeloma cells and the bone marrow microenvironment in myeloma. Int. J. Hematol. 2011, 94:334-343.