ROS-induced CXCR4 signaling regulates mantle cell lymphoma (MCL) cell survival and drug resistance in the bone marrow microenvironment via autophagy

Clinical Cancer Research

Volumn 22, Issue 1, 2016, Pages 187-199

  Chen, Zheng ^a   Teo, Albert E ^a   McCarty, Nami ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORTEZOMIB; CHEMOKINE RECEPTOR CXCR4; IBRUTINIB; REACTIVE OXYGEN METABOLITE; STROMAL CELL DERIVED FACTOR 1; ANTINEOPLASTIC AGENT;

ARTICLE; AUTOPHAGY; BONE MARROW; BONE MARROW STROMA CELL; CELL ADHESION; CELL PROLIFERATION; CELL SURVIVAL; COLONY FORMATION; CONTROLLED STUDY; DRUG RESISTANCE; ENGRAFTMENT; HUMAN; HUMAN CELL; LYMPHOMA CELL; MANTLE CELL LYMPHOMA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; ANTAGONISTS AND INHIBITORS; CANCER STAGING; CELL MOTION; DRUG EFFECTS; GENETICS; LYMPHOMA, MANTLE-CELL; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGICAL STRESS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; BONE MARROW; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CELL SURVIVAL; CHEMOKINE CXCL12; DRUG RESISTANCE, NEOPLASM; HUMANS; LYMPHOMA, MANTLE-CELL; MESENCHYMAL STROMAL CELLS; NEOPLASM STAGING; REACTIVE OXYGEN SPECIES; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84954513717     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-0987     Document Type: Article

References (53)

1. Leonard JP, Williams ME, Goy A, Grant S, Pfreundschuh M, Rosen ST, et al. Mantle cell lymphoma: biological insights and treatment advances. Clin Lymphoma Myeloma 2009;9:267-77.
2. Salaverria I, Perez-Galan P, Colomer D, Campo E. Mantle cell lymphoma: from pathology and molecular pathogenesis to new therapeutic perspectives. Haematologica 2006;91:11-6.
3. Weigert O, Unterhalt M, Hiddemann W, Dreyling M. Mantle cell lymphoma: state-of-the-art management and future perspective. Leuk Lymphoma 2009;50:1937-50.
4. Adams JM, Harris AW, Strasser A, Ogilvy S, Cory S. Transgenic models of lymphoid neoplasia and development of a pan-hematopoietic vector. Oncogene 1999;18:5268-77.
5. Lovec H, Grzeschiczek A, Kowalski MB, Moroy T. Cyclin D1/bcl-1 cooperates with myc genes in the generation of B-cell lymphoma in transgenic mice. EMBO J 1994;13:3487-95.
6. Hirt C, Schuler F, Dolken L, Schmidt CA, Dolken G. Low prevalence of circulating t(11;14)(q13;q32)-positive cells in the peripheral blood of healthy individuals as detected by real-time quantitative PCR. Blood 2004;104:904-5.
7. Fu K, Weisenburger DD, Greiner TC, Dave S, Wright G, Rosenwald A, et al. Cyclin D1-negative mantle cell lymphoma: a clinicopathologic study based on gene expression profiling. Blood 2005;106: 4315-21.
8. Martin P, Coleman M, Leonard JP. Progress in mantle-cell lymphoma. J Clin Oncol 2009;27:481-3.
9. Sharma M, Afrin F, Satija N, Tripathi RP, Gangenahalli GU. Stromalderived factor-1/CXCR4 signaling: indispensable role in homing and engraftment of hematopoietic stem cells in bone marrow. Stem Cells Dev 2011;20:933-46.
10. Grignani G, Perissinotto E, Cavalloni G, Carnevale Schianca F, Aglietta M. Clinical use of AMD3100 to mobilize CD34+ cells in patients affected by non-Hodgkin's lymphoma or multiple myeloma. J Clin Oncol 2005;23: 3871-2; author reply 2-3.
11. Clezardin P. Therapeutic targets for bone metastases in breast cancer. Breast Cancer Res 2011;13:207.
12. Tseng D, Vasquez-Medrano DA, Brown JM. Targeting SDF-1/CXCR4 to inhibit tumour vasculature for treatment of glioblastomas. Br J Cancer 2011;104:1805-9.
13. Mitchell B, Mahalingam M. The CXCR4/CXCL12 axis in cutaneous malignancies with an emphasis on melanoma. Histol Histopathol 2014;29: 1539-46.
14. Wu PF, Lu ZP, Cai BB, Tian L, Zou C, Jiang KR, et al. Role of CXCL12/CXCR4 signaling axis in pancreatic cancer. Chin Med J (Engl) 2013;126:3371-4.
15. Gangadhar T, Nandi S, Salgia R. The role of chemokine receptor CXCR4 in lung cancer. Cancer Biol Ther 2010;9:409-16.
16. Burger JA, Stewart DJ, Wald O, Peled A. Potential of CXCR4 antagonists for the treatment of metastatic lung cancer. Expert Rev Anticancer Ther 2011;11:621-30.
17. Zhang L, Yang J, Qian J, Li H, Romaguera JE, Kwak LW, et al. Role of the microenvironment in mantle cell lymphoma: IL-6 is an important survival factor for the tumor cells. Blood 2012;120:3783-92.
18. Tokoyoda K, Egawa T, Sugiyama T, Choi BI, Nagasawa T. Cellular niches controlling B lymphocyte behavior within bone marrow during development. Immunity 2004;20:707-18.
19. Kurtova AV, Tamayo AT, Ford RJ, Burger JA. Mantle cell lymphoma cells express high levels of CXCR4, CXCR5, and VLA-4 (CD49d): importance for interactions with the stromal microenvironment and specific targeting. Blood 2009;113:4604-13.
20. Graf L, Iwata M, Torok-Storb B. Gene expression profiling of the functionally distinct human bone marrow stromal cell lines HS-5 and HS-27a. Blood 2002;100:1509-11.
21. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 2005; 105:3793-801.
22. Lapidot T, Petit I. Current understanding of stem cell mobilization: the roles of chemokines, proteolytic enzymes, adhesion molecules, cytokines, and stromal cells. Exp Hematol 2002;30:973-81.
23. Matsui W, Huff CA, Wang Q, Malehorn MT, Barber J, Tanhehco Y, et al. Characterization of clonogenic multiple myeloma cells. Blood 2004; 103:2332-6.
24. Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999;283:845-8.
25. Chen Z, Orlowski RZ, Wang M, Kwak L, McCarty N. Osteoblastic niche supports the growth of quiescent multiple myeloma cells. Blood 2014; 123:2204-8.
26. Huang S, Law P, Francis K, Palsson BO, Ho AD. Symmetry of initial cell divisions among primitive hematopoietic progenitors is independent of ontogenic age and regulatory molecules. Blood 1999;94: 2595-604.
27. Lanzkron SM, Collector MI, Sharkis SJ. Hematopoietic stem cell tracking in vivo: a comparison of short-term and long-term repopulating cells. Blood 1999;93:1916-21.
28. Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010;140: 62-73.
29. Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 2000;106: 1331-9.
30. Richardson PG, Mitsiades C, Hideshima T, Anderson KC. Proteasome inhibition in the treatment of cancer. Cell Cycle 2005;4:290-6.
31. Chen Z, Romaguera J, Wang M, Fayad L, Kwak LW, McCarty N. Verapamil synergistically enhances cytotoxicity of bortezomib in mantle cell lymphoma via induction of reactive oxygen species production. Br J Haematol 2012;159:243-6.
32. Ohshima-Hosoyama S, Davare MA, Hosoyama T, Nelon LD, Keller C. Bortezomib stabilizes NOXA and triggers ROS-associated apoptosis in medulloblastoma. J Neurooncol 2011;105:475-83.
33. Levine B, Kroemer G. Autophagy in the pathogenesis of disease. Cell 2008;132:27-42.
34. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010; 330:1344-8.
35. Rosich L, Xargay-Torrent S, Lopez-Guerra M, Campo E, Colomer D, Roue G. Counteracting autophagy overcomes resistance to everolimus in mantle cell lymphoma. Clin Cancer Res 2012;18:5278-89.
36. Levine B. Cell biology: autophagy and cancer. Nature 2007;446: 745-7.
37. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 1998;72:8586-96.
38. Spencer JA, Ferraro F, Roussakis E, Klein A, Wu J, Runnels JM, et al. Direct measurement of local oxygen concentration in the bone marrow of live animals. Nature 2014;508:269-73.
39. Lipinski MM, Hoffman G, Ng A, Zhou W, Py BF, Hsu E, et al. A genomewide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Dev Cell 2010;18:1041-52.
40. Warr MR, Binnewies M, Flach J, Reynaud D, Garg T, Malhotra R, et al. FOXO3A directs a protective autophagy program in haematopoietic stem cells. Nature 2013;494:323-7.
41. Rothe K, Lin H, Lin KB, Leung A, Wang HM, Malekesmaeili M, et al. The core autophagy protein ATG4B is a potential biomarker and therapeutic target in CML stem/progenitor cells. Blood 2014;123:3622-34.
42. do Carmo A, Patricio I, Cruz MT, Carvalheiro H, Oliveira CR, Lopes MC. CXCL12/CXCR4 promotes motility and proliferation of glioma cells. Cancer Biol Ther 2010;9:56-65.
43. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 2005;121:335-48.
44. Scotton CJ, Wilson JL, Scott K, Stamp G, Wilbanks GD, Fricker S, et al. Multiple actions of the chemokine CXCL12 on epithelial tumor cells in human ovarian cancer. Cancer Res 2002;62:5930-8.
45. Zeng Z, Shi YX, Samudio IJ, Wang RY, Ling X, Frolova O, et al. Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood 2009; 113:6215-24.
46. Azab AK, Runnels JM, Pitsillides C, Moreau AS, Azab F, Leleu X, et al. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 2009;113: 4341-51.
47. Rausch V, Liu L, Apel A, Rettig T, Gladkich J, Labsch S, et al. Autophagy mediates survival of pancreatic tumour-initiating cells in a hypoxic microenvironment. J Pathol 2012;227:325-35.
48. Kongara S, Karantza V. The interplay between autophagy and ROS in tumorigenesis. Front Oncol 2012;2:171.
49. Li L, Ishdorj G, Gibson SB. Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic Biol Med 2012;53:1399-410.
50. Sui X, Chen R, Wang Z, Huang Z, Kong N, Zhang M, et al. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis 2013;4:e838.
51. Wan G, Xie W, Liu Z, Xu W, Lao Y, Huang N, et al. Hypoxia-induced MIR155 is a potent autophagy inducer by targeting multiple players in the MTOR pathway. Autophagy 2014;10:70-9.
52. Hu YL, DeLay M, Jahangiri A, Molinaro AM, Rose SD, Carbonell WS, et al. Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma. Cancer Res 2012;72:1773-83.
53. Oh YS, Kim HY, Song IC, Yun HJ, Jo DY, Kim S, et al. Hypoxia induces CXCR4 expression and biological activity in gastric cancer cells through activation of hypoxia-inducible factor-1alpha. Oncol Rep 2012;28: 2239-46.