Multiple myeloma exosomes establish a favourable bone marrow microenvironment with enhanced angiogenesis and immunosuppression

Journal of Pathology

Volumn 239, Issue 2, 2016, Pages 162-173

  Wang, Jinheng ^a   De Veirman, Kim ^a   Faict, Sylvia ^a   Frassanito, Maria Antonia ^b   Ribatti, Domenico ^b,c   Vacca, Angelo ^b   Menu, Eline ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b UNIVERSITY OF BARI MEDICAL SCHOOL   (Italy)

^c NATIONAL CANCER INSTITUTE GIOVANNI PAOLO II   (Italy)

Author keywords

angiogenesis; exosomes; immunosuppression; multiple myeloma; myeloid derived suppressor cells; STAT3

Indexed keywords

CD11B ANTIGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; PROTEIN P53; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; ENDOTHELIUM CELL; EXOSOME; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; MICROENVIRONMENT; MOUSE; MULTIPLE MYELOMA; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STROMA CELL; SUPPRESSOR CELL; UPREGULATION; ANIMAL; C57BL MOUSE; DISEASE COURSE; DISEASE MODEL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MESENCHYMAL STROMA CELL; METABOLISM; MYELOID-DERIVED SUPPRESSOR CELL; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; VASCULARIZATION;

ANIMALS; BONE MARROW; CELL LINE, TUMOR; CELL PROLIFERATION; CELLULAR MICROENVIRONMENT; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EXOSOMES; HUMANS; IMMUNE TOLERANCE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; MULTIPLE MYELOMA; MYELOID-DERIVED SUPPRESSOR CELLS; NEOVASCULARIZATION, PATHOLOGIC; NITRIC OXIDE SYNTHASE TYPE II; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84962885569     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4712     Document Type: Article

References (55)

1. Ribatti D, Moschetta M, Vacca A,. Microenvironment and multiple myeloma spread. Thromb Res 2014; 133 (Suppl 2): S102-S106.
2. Romano A, Conticello C, Cavalli M, et al., Immunological dysregulation in multiple myeloma microenvironment. Biomed Res Int 2014; 2014: 198539.
3. Lemaire M, Deleu S, De Bruyne E, et al., The microenvironment and molecular biology of the multiple myeloma tumor. Adv Cancer Res 2011; 110: 19-42.
4. Rajkumar SV, Mesa RA, Fonseca R, et al., Bone marrow angiogenesis in 400 patients with monoclonal gammopathy of undetermined significance, multiple myeloma, and primary amyloidosis. Clin Cancer Res 2002; 8: 2210-2216.
5. Sezer O, Jakob C, Eucker J, et al., Serum levels of the angiogenic cytokines basic fibroblast growth factor (bFGF), vascular endothelial growth factor (VEGF) and hepatocyte growth factor (HGF) in multiple myeloma. Eur J Haematol 2001; 66: 83-88.
6. Di Raimondo F, Azzaro MP, Palumbo G, et al., Angiogenic factors in multiple myeloma: higher levels in bone marrow than in peripheral blood. Haematologica 2000; 85: 800-805.
7. Ramachandran IR, Martner A, Pisklakova A, et al., Myeloid-derived suppressor cells regulate growth of multiple myeloma by inhibiting T cells in bone marrow. J Immunol 2013; 190: 3815-3823.
8. De Veirman K, Van Ginderachter JA, Lub S, et al., Multiple myeloma induces Mcl-1 expression and survival of myeloid-derived suppressor cells. Oncotarget 2015; 6: 10532-10547.
9. Thery C, Ostrowski M, Segura E,. Membrane vesicles as conveyors of immune responses. Nature Rev Immunol 2009; 9: 581-593.
10. Raposo G, Stoorvogel W,. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200: 373-383.
11. Taylor DD, Gercel-Taylor C,. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008; 110: 13-21.
12. Ghosh AK, Secreto CR, Knox TR, et al., Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood 2010; 115: 1755-1764.
13. Taylor DD, Gercel-Taylor C,. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 2011; 33: 441-454.
14. Peinado H, Aleckovic M, Lavotshkin S, et al., Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nature Med 2012; 18: 883-891.
15. Yu S, Liu C, Su K, et al., Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol 2007; 178: 6867-6875.
16. Al-Nedawi K, Meehan B, Rak J,. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 2009; 8: 2014-2018.
17. Chalmin F, Ladoire S, Mignot G, et al., Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010; 120: 457-471.
18. Wang J, Hendrix A, Hernot S, et al., Bone marrow stromal cell-derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood 2014; 124: 555-566.
19. Roccaro AM, Sacco A, Maiso P, et al., BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 2013; 123: 1542-1555.
20. Umezu T, Tadokoro H, Azuma K, et al., Exosomal miR-135b shed from hypoxic multiple myeloma cells enhances angiogenesis by targeting factor-inhibiting HIF-1. Blood 2014; 124: 3748-3757.
21. Raimondi L, De Luca A, Amodio N, et al., Involvement of multiple myeloma cell-derived exosomes in osteoclast differentiation. Oncotarget 2015; 6: 13772-13789.
22. Imai K, Kobayashi M, Wang J, et al., Selective transendothelial migration of hematopoietic progenitor cells: a role in homing of progenitor cells. Blood 1999; 93: 149-156.
23. Ribatti D, Nico B, Vacca A, et al., The gelatin sponge-chorioallantoic membrane assay. Nature Protoc 2006; 1: 85-91.
24. Nur H, Rao L, Frassanito MA, et al., Stimulation of invariant natural killer T cells by alpha-galactosylceramide activates the JAK-STAT pathway in endothelial cells and reduces angiogenesis in the 5 T33 multiple myeloma model. Br J Haematol 2014; 167: 651-663.
25. Shelke GV, Lasser C, Gho YS, et al., Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J Extracell Vesicles 2014; 3: 24783.
26. Ochando JC, Chen SH,. Myeloid-derived suppressor cells in transplantation and cancer. Immunol Res 2012; 54: 275-285.
27. Van Valckenborgh E, Schouppe E, Movahedi K, et al., Multiple myeloma induces the immunosuppressive capacity of distinct myeloid-derived suppressor cell subpopulations in the bone marrow. Leukemia 2012; 26: 2424-2428.
28. Condamine T, Gabrilovich DI,. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 2011; 32: 19-25.
29. Gabrilovich DI, Nagaraj S,. Myeloid-derived suppressor cells as regulators of the immune system. Nature Rev Immunol 2009; 9: 162-174.
30. Di Noto G, Paolini L, Zendrini A, et al., C-src enriched serum microvesicles are generated in malignant plasma cell dyscrasia. PloS One 2013; 8: e70811.
31. Caivano A, Laurenzana I, De Luca L, et al., High serum levels of extracellular vesicles expressing malignancy-related markers are released in patients with various types of hematological neoplastic disorders. Tumour Biol 2015; 36: 9739-9752.
32. Benameur T, Chappard D, Fioleau E, et al., Plasma cells release membrane microparticles in a mouse model of multiple myeloma. Micron 2013; 54-55: 75-81.
33. Xiang X, Poliakov A, Liu C, et al., Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 2009; 124: 2621-2633.
34. Chowdhury R, Webber JP, Gurney M, et al., Cancer exosomes trigger mesenchymal stem cell differentiation into pro-angiogenic and pro-invasive myofibroblasts. Oncotarget 2015; 6: 715-731.
35. Paggetti J, Haderk F, Seiffert M, et al., Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015; 126: 1106-1117.
36. Marton A, Vizler C, Kusz E, et al., Melanoma cell-derived exosomes alter macrophage and dendritic cell functions in vitro. Immunol Lett 2012; 148: 34-38.
37. Hood JL, Pan H, Lanza GM, et al., Paracrine induction of endothelium by tumor exosomes. Lab Invest 2009; 89: 1317-1328.
38. Chan YK, Zhang H, Liu P, et al., Proteomic analysis of exosomes from nasopharyngeal carcinoma cell identifies intercellular transfer of angiogenic proteins. Int J Cancer 2015; 137: 1830-1841.
39. Taverna S, Flugy A, Saieva L, et al., Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int J Cancer 2012; 130: 2033-2043.
40. Mineo M, Garfield SH, Taverna S, et al., Exosomes released by K562 chronic myeloid leukemia cells promote angiogenesis in a Src-dependent fashion. Angiogenesis 2012; 15: 33-45.
41. Jakob C, Sterz J, Zavrski I, et al., Angiogenesis in multiple myeloma. Eur J Cancer 2006; 42: 1581-1590.
42. Sun L, Ma K, Wang H, et al., JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J Cell Biol 2007; 179: 129-138.
43. Bianchi G, Munshi NC,. Pathogenesis beyond the cancer clone(s) in multiple myeloma. Blood 2015; 125: 3049-3058.
44. Mahindra A, Hideshima T, Anderson KC,. Multiple myeloma: biology of the disease. Blood Rev 2010; 24 (Suppl 1): S5-S11.
45. Wang J, De Veirman K, De Beule N, et al., The bone marrow microenvironment enhances multiple myeloma progression by exosome-mediated activation of myeloid-derived suppressor cells. Oncotarget 2015; 6: 43992-44004.
46. Orimo A, Gupta PB, Sgroi DC, et al., Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005; 121: 335-348.
47. Frassanito MA, Rao L, Moschetta M, et al., Bone marrow fibroblasts parallel multiple myeloma progression in patients and mice: in vitro and in vivo studies. Leukemia 2014; 28: 904-916.
48. Erez N, Truitt M, Olson P, et al., Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010; 17: 135-147.
49. De Veirman K, Van Valckenborgh E, Lahmar Q, et al., Myeloid-derived suppressor cells as therapeutic target in hematological malignancies. Front Oncol 2014; 4: 349.
50. Gorgun GT, Whitehill G, Anderson JL, et al., Tumor-promoting immune-suppressive myeloid-derived suppressor cells in the multiple myeloma microenvironment in humans. Blood 2013; 121: 2975-2987.
51. Botta C, Gulla A, Correale P, et al., Myeloid-derived suppressor cells in multiple myeloma: pre-clinical research and translational opportunities. Front Oncol 2014; 4: 348.
52. Matsumoto Y, Fujita T, Hirai I, et al., Immunosuppressive effect on T cell activation by interleukin-16- and interleukin-10-cDNA-double-transfected human squamous cell line. Burns 2009; 35: 383-389.
53. Cruikshank WW, Lim K, Theodore AC, et al., IL-16 inhibition of CD3-dependent lymphocyte activation and proliferation. J Immunol 1996; 157: 5240-5248.
54. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V,. Coordinated regulation of myeloid cells by tumours. Nature Rev Immunol 2012; 12: 253-268.
55. Kusmartsev S, Gabrilovich DI,. STAT1 signaling regulates tumor-associated macrophage-mediated T cell deletion. J Immunol 2005; 174: 4880-4891.