Mature adipocytes in bone marrow protect myeloma cells against chemotherapy through autophagy activation

Oncotarget

Volumn 6, Issue 33, 2015, Pages 34329-34341

  Liu, Zhiqiang ^a   Xu, Jingda ^a   He, Jin ^a   Liu, Huan ^a   Lin, Pei ^a   Wan, Xinhai ^a   Navone, Nora M ^a   Tong, Qiang ^b   Kwak, Larry W ^a   Orlowski, Robert Z ^a   Yang, Jing ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Adipocytes; Apoptosis; Autophagy; Chemotherapy resistance; Multiple myeloma

Indexed keywords

ANTINEOPLASTIC AGENT; BORTEZOMIB; CASPASE 3; CASPASE 9; COMPLEMENT FACTOR D; DEXAMETHASONE; DOXORUBICIN; INTERLEUKIN 6; JANUS KINASE; LEPTIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MELPHALAN; MONOCYTE CHEMOTACTIC PROTEIN 1; OSTEOPROTEGERIN; STAT3 PROTEIN;

ADIPOCYTE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BONE MARROW DERIVED ADIPOCYTE; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RESISTANCE; DRUG RESPONSE; FEMALE; FETUS; FIBROBLAST; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; NONHUMAN; PROADIPOCYTE; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; UPREGULATION; WHITE ADIPOCYTE; ANIMAL; BONE MARROW CELL; COCULTURE; DRUG EFFECTS; DRUG SCREENING; ENZYME LINKED IMMUNOSORBENT ASSAY; METABOLISM; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL CULTURE; TUMOR CELL LINE; WESTERN BLOTTING;

ADIPOCYTES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; BONE MARROW CELLS; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DRUG RESISTANCE, NEOPLASM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; MICE; MICE, SCID; MULTIPLE MYELOMA; REAL-TIME POLYMERASE CHAIN REACTION; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84946606662     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6020     Document Type: Article

References (49)

1. Kyle RA and Rajkumar SV. Multiple myeloma. N Engl J Med. 2004; 351:1860-1873.
2. Dispenzieri A and Kyle RA. Multiple myeloma: clinical features and indications for therapy. Best Pract Res Clin Haematol. 2005; 18:553-568.
3. Rajkumar SV. Novel approaches to the management of myeloma. Oncology (Williston Park). 2005; 19:621-625.
4. Shaughnessy JD, Jr. and Barlogie B. Using genomics to identify high-risk myeloma after autologous stem cell transplantation. Biol Blood Marrow Transplant. 2006; 12:77-80.
5. Durie BG, Waxman AD, D'Agnolo A and Williams CM. Whole-body (18)F-FDG PET identifies high-risk myeloma. J Nucl Med. 2002; 43(:1457-1463.
6. Qazilbash MH, Saliba RM, Aleman A, Lei X, Weber D, Carrasco A, Champlin RE and Giralt SA. Risk factors for relapse after complete remission with high-dose therapy for multiple myeloma. Leuk Lymphoma. 2006; 47:1360-1364.
7. Ahn JS, Yang DH, Jung SH, Park HC, Moon JH, Sohn SK, Bae SY, Kim YK, Kim HJ and Lee JJ. A comparison of bortezomib, cyclophosphamide, and dexamethasone (VelCD) chemotherapy without and with thalidomide (VelCTD) for the treatment of relapsed or refractory multiple myeloma. Ann Hematol. 2012; 91:1023-1030.
8. Epstein J and Yaccoby S. Consequences of interactions between the bone marrow stroma and myeloma. Hematol J. 2003; 4:310-314.
9. Roodman GD. Role of the bone marrow microenvironment in multiple myeloma. J Bone Miner Res. 2002; 17:1921-1925.
10. van de Donk NW, Lokhorst HM and Bloem AC. Growth factors and antiapoptotic signaling pathways in multiple myeloma. Leukemia. 2005; 19:2177-2185.
11. Zheng Y, Cai Z, Wang S, Zhang X, Qian J, Hong S, Li H, Wang M, Yang J and Yi Q. Macrophages are an abundant component of myeloma microenvironment and protect myeloma cells from chemotherapy drug-induced apoptosis. Blood. 2009; 114:3625-3628.
12. Zheng Y, Yang J, Qian J, Qiu P, Hanabuchi S, Lu Y, Wang Z, Liu Z, Li H, He J, Lin P, Weber D, Davis RE, Kwak L, Cai Z and Yi Q. PSGL-1/selectin and ICAM-1/CD18 interactions are involved in macrophage-induced drug resistance in myeloma. Leukemia. 2013; 27:702-710.
13. Chauhan D, Singh AV, Brahmandam M, Carrasco R, Bandi M, Hideshima T, Bianchi G, Podar K, Tai YT, Mitsiades C, Raje N, Jaye DL, Kumar SK, Richardson P, Munshi N and Anderson KC. Functional interaction of plasmacytoid dendritic cells with multiple myeloma cells: a therapeutic target. Cancer Cell. 2009; 16:309-323.
14. Yaccoby S. Osteoblastogenesis and tumor growth in myeloma. Leuk Lymphoma. 2010; 51:213-220.
15. Yang J, He J, Wang J, Cao Y, Ling J, Qian J, Lu Y, Li H, Zheng Y, Lan Y, Hong S, Matthews J, Starbuck MW, Navone NM, Orlowski RZ, Lin P, et al. Constitutive activation of p38 MAPK in tumor cells contributes to osteolytic bone lesions in multiple myeloma. Leukemia. 2012; 26:2114-2123.
16. Li H, Hong S, Qian J, Zheng Y, Yang J and Yi Q. Cross talk between the bone and immune systems: osteoclasts function as antigen-presenting cells and activate CD4+ and CD8+ T cells. Blood. 2010; 116:210-217.
17. Yaccoby S, Pearse RN, Johnson CL, Barlogie B, Choi Y and Epstein J. Myeloma interacts with the bone marrow microenvironment to induce osteoclastogenesis and is dependent on osteoclast activity. Br J Haematol. 2002; 116:278-290.
18. Tucci M, Stucci S, Strippoli S, Dammacco F and Silvestris F. Dendritic cells and malignant plasma cells: an alliance in multiple myeloma tumor progression? Oncologist. 2011; 16:1040-1048.
19. Treon SP and Anderson KC. Interleukin-6 in multiple myeloma and related plasma cell dyscrasias. Curr Opin Hematol. 1998; 5:42-48.
20. Oancea M, Mani A, Hussein MA and Almasan A. Apoptosis of multiple myeloma. Int J Hematol. 2004; 80:224-231.
21. Gimble JM, Robinson CE, Wu X and Kelly KA. The function of adipocytes in the bone marrow stroma: an update. Bone. 1996; 19:421-428.
22. Ciuffi S, Fabbri S, Zonefrati R, Galli G, Tanini A and Brandi ML. Subcutaneous adipocytes may become osteoblasts. Clinical cases in mineral and bone metabolism: the official journal of the Italian Society of Osteoporosis, Mineral Metabolism, and Skeletal Diseases. 2012; 9:28-30.
23. Billon N, Monteiro MC and Dani C. Developmental origin of adipocytes: new insights into a pending question. Biology of the cell/under the auspices of the European Cell Biology Organization. 2008; 100:563-575.
24. Pilch PF, Meshulam T, Ding S and Liu L. Caveolae and lipid trafficking in adipocytes. Clinical lipidology. 2011; 6:49-58.
25. Zhao SM, Wan QH, Cheng ML, Huang Y, Li WZ, Zhang YY and Gao SZ. Effect of monoclonal antibody on expression of lipid metabolism related genes in porcine adipocytes. Comp Biochem Physiol B Biochem Mol Biol. 2009; 154:449-454.
26. Ahmadian M, Wang Y and Sul HS. Lipolysis in adipocytes. Int J Biochem Cell Biol. 2010; 42:555-559.
27. Urs S, Smith C, Campbell B, Saxton AM, Taylor J, Zhang B, Snoddy J, Jones Voy B and Moustaid-Moussa N. Gene expression profiling in human preadipocytes and adipocytes by microarray analysis. The Journal of nutrition. 2004; 134:762-770.
28. Weigle DS. Leptin and other secretory products of adipocytes modulate multiple physiological functions. Annales d'endocrinologie. 1997; 58:132-136.
29. Granneman JG, Kimler VA and Moore HP. Cell Biology Symposium: imaging the organization and trafficking of lipolytic effectors in adipocytes. J Anim Sci. 2011; 89:701-710.
30. Hardaway AL, Herroon MK, Rajagurubandara E and Podgorski I. Bone marrow fat: linking adipocyte-induced inflammation with skeletal metastases. Cancer metastasis reviews. 2014; 33:527-543.
31. Bochet L, Meulle A, Imbert S, Salles B, Valet P and Muller C. Cancer-associated adipocytes promotes breast tumor radioresistance. Biochemical and biophysical research communications. 2011; 411:102-106.
32. Nieman KM, Kenny HA, Penicka CV, Ladanyi A, BuellGutbrod R, Zillhardt MR, Romero IL, Carey MS, Mills GB, Hotamisligil GS, Yamada SD, Peter ME, Gwin K and Lengyel E. Adipocytes promote ovarian cancer metastasis and provide energy for rapid tumor growth. Nature medicine. 2011; 17:1498-1503.
33. Vogl DT, Wang T, Perez WS, Stadtmauer EA, Heitjan DF, Lazarus HM, Kyle RA, Kamble R, Weisdorf D, Roy V, Gibson J, Ballen K, Holmberg L, Bashey A, McCarthy PL, Freytes C, et al. Effect of obesity on outcomes after autologous hematopoietic stem cell transplantation for multiple myeloma. Biol Blood Marrow Transplant. 2011; 17:1765-1774.
34. Islam R, Altundag K, Kurt M, Altundag O and Turen S. Association between obesity and multiple myeloma in postmenopausal women may be attributed to increased aromatization of androgen in adipose tissue. Medical hypotheses. 2005; 65:1001-1002.
35. Caers J, Deleu S, Belaid Z, De Raeve H, Van Valckenborgh E, De Bruyne E, Defresne MP, Van Riet I, Van Camp B and Vanderkerken K. Neighboring adipocytes participate in the bone marrow microenvironment of multiple myeloma cells. Leukemia. 2007; 21:1580-1584.
36. Mah LY and Ryan KM. Autophagy and cancer. Cold Spring Harb Perspect Biol. 2012; 4:a008821.
37. Wirawan E, Vanden Berghe T, Lippens S, Agostinis P and Vandenabeele P. Autophagy: for better or for worse. Cell Res. 2012; 22:43-61.
38. Hu YL, Jahangiri A, Delay M and Aghi MK. Tumor cell autophagy as an adaptive response mediating resistance to treatments such as antiangiogenic therapy. Cancer Res. 2012; 72:4294-4299.
39. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
40. Oakes ND, Thalen PG, Jacinto SM and Ljung B. Thiazolidinediones increase plasma-adipose tissue FFA exchange capacity and enhance insulin-mediated control of systemic FFA availability. Diabetes. 2001; 50:1158-1165.
41. Wang Z, Wang N, Liu P, Chen Q, Situ H, Xie T, Zhang J, Peng C, Lin Y and Chen J. MicroRNA-25 regulates chemoresistance-associated autophagy in breast cancer cells, a process modulated by the natural autophagy inducer isoliquiritigenin. Oncotarget. 2014; 5:7013-7026.
42. Abdel Malek MA, Jagannathan S, Malek E, Sayed DM, Elgammal SA, Abd El-Azeem HG, Thabet NM and Driscoll JJ. Molecular chaperone GRP78 enhances aggresome delivery to autophagosomes to promote drug resistance in multiple myeloma. Oncotarget. 2015; 6:3098-3110.
43. Jaganathan S, Malek E, Vallabhapurapu S, Vallabhapurapu S and Driscoll JJ. Bortezomib induces AMPK-dependent autophagosome formation uncoupled from apoptosis in drug resistant cells. Oncotarget. 2014; 5:12358-12370.
44. Riz I, Hawley TS and Hawley RG. KLF4-SQSTM1/p62-associated prosurvival autophagy contributes to carfilzomib resistance in multiple myeloma models. Oncotarget. 2015; 6:14814-31.
45. Zhang M, He J, Liu Z, Lu Y, Zheng Y, Li H, Xu J, Liu H, Qian J, Orlowski RZ, Kwak LW, Yi Q and Yang J. Antibeta(2)-microglobulin monoclonal antibodies overcome bortezomib resistance in multiple myeloma by inhibiting autophagy. Oncotarget. 2015; 6:8567-8578.
46. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S and Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science. 1999; 284:143-147.
47. Fernyhough ME, Vierck JL, Hausman GJ, Mir PS, Okine EK and Dodson MV. Primary adipocyte culture: adipocyte purification methods may lead to a new understanding of adipose tissue growth and development. Cytotechnology. 2004; 46:163-172.
48. Szabo E, Qiu Y, Baksh S, Michalak M and Opas M. Calreticulin inhibits commitment to adipocyte differentiation. J Cell Biol. 2008; 182:103-116.
49. Qin L, Liu X, Sun Q, Fan Z, Xia D, Ding G, Ong HL, Adams D, Gahl WA, Zheng C, Qi S, Jin L, Zhang C, Gu L, He J, Deng D, et al. Sialin (SLC17A5) functions as a nitrate transporter in the plasma membrane. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109:13434-13439