Decoding the pathophysiology and the genetics of multiple myeloma to identify new therapeutic targets

Seminars in Oncology

Volumn 40, Issue 5, 2013, Pages 537-548

  Lawasut, Panisinee ^a,b   Groen, Richard W J ^a,c   Dhimolea, Eugen ^a   Richardson, Paul G ^a   Anderson, Kenneth C ^a   Mitsiades, Constantine S ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CHULALONGKORN UNIVERSITY   (Thailand)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

1 (1 CYANO 1 METHYLETHYL) 3 METHYL 8 (3 QUINOLINYL)IMIDAZO[4,5 C]QUINOLIN 2(1H,3H) ONE; ALKYLATING AGENT; ANTHRACYCLINE; B RAF KINASE; BORTEZOMIB; CYCLIN D; EXPORTIN 1; FIBROBLAST GROWTH FACTOR RECEPTOR 3; GLUCOCORTICOID; HISTONE METHYLTRANSFERASE; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 6; K RAS PROTEIN; MICRORNA; MICRORNA 29B; MYC PROTEIN; NOTCH RECEPTOR; PROTEIN P53; THALIDOMIDE; TRANSCRIPTION FACTOR HOXA9; VASCULOTROPIN; WNT PROTEIN;

ARTICLE; CELL ADHESION; CELL INTERACTION; CELL PROLIFERATION; GENE CONTROL; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE MUTATION; HUMAN; LOSS OF FUNCTION MUTATION; MOLECULAR GENETICS; MONOCLONAL IMMUNOGLOBULINEMIA; MULTIPLE MYELOMA; NONHUMAN; ONCOGENE N RAS; OSTEOCLAST; OSTEOLYSIS; PRIORITY JOURNAL; RNA PROCESSING; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR MICROENVIRONMENT; UNFOLDED PROTEIN RESPONSE;

ANIMALS; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; IMMUNOTHERAPY; MICE; MICRORNAS; MULTIPLE MYELOMA; MUTATION; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION;

EID: 84886931146     PISSN: 00937754     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.seminoncol.2013.07.010     Document Type: Article

References (126)

1. P.L. Bergsagel, and W.M. Kuehl Molecular pathogenesis and a consequent classification of multiple myeloma J Clin Oncol 23 2005 6333 6338
2. G.J. Morgan, and M.F. Kaiser How to use new biology to guide therapy in multiple myeloma Hematology/Education Program of the American Society of Hematology American Society of Hematology Education Program 2012 2012 342 349
3. W.M. Kuehl, and P.L. Bergsagel Molecular pathogenesis of multiple myeloma and its premalignant precursor J Clin Invest 122 2012 3456 3463
4. J.J. Keats, R. Fonseca, and M. Chesi Promiscuous mutations activate the noncanonical NF-kappaB pathway in multiple myeloma Cancer Cell 12 2007 131 144
5. L. Billecke, E.M. Penas, and A.M. May Similar incidences of TP53 deletions in extramedullary organ infiltrations, soft tissue and osteolyses of patients with multiple myeloma Anticancer Res 32 2012 2031 2034
6. R.E. Tiedemann, N. Gonzalez-Paz, and R.A. Kyle Genetic aberrations and survival in plasma cell leukemia Leukemia 22 2008 1044 1052
7. P.L. Bergsagel, F. Davies, and H. Avet-Loiseau Epidemiology, etiology, and molecular pathogenesis of multiple myeloma P.G. Richardson, K.C. Anderson, Multiple myeloma 2nd ed 2011 Remedica Chicago 1 18
8. B. Nair, F. van Rhee, and J.D. Shaughnessy Jr. Superior results of Total Therapy 3 (2003-33) in gene expression profiling-defined low-risk multiple myeloma confirmed in subsequent trial 2006-66 with VRD maintenance Blood 115 2010 4168 4173
9. B.A. Walker, P.E. Leone, and L. Chiecchio A compendium of myeloma-associated chromosomal copy number abnormalities and their prognostic value Blood 116 2010 e56 e65
10. P.L. Bergsagel, M.V. Mateos, N.C. Gutierrez, S.V. Rajkumar, and J.F. San Miguel Improving overall survival and overcoming adverse prognosis in the treatment of cytogenetically high-risk multiple myeloma Blood 121 2012 884 892
11. R. Fonseca, E. Blood, and M. Rue Clinical and biologic implications of recurrent genomic aberrations in myeloma Blood 101 2003 4569 4575
12. K.D. Boyd, F.M. Ross, and L. Chiecchio A novel prognostic model in myeloma based on co-segregating adverse FISH lesions and the ISS: analysis of patients treated in the MRC Myeloma IX trial Leukemia 26 2012 349 355
13. H. Avet-Loiseau, F. Malard, and L. Campion Translocation t(14;16) and multiple myeloma: is it really an independent prognostic factor? Blood 117 2011 2009 2011
14. F. Zhan, Y. Huang, and S. Colla The molecular classification of multiple myeloma Blood 108 2006 2020 2028
15. A. Broyl, D. Hose, and H. Lokhorst Gene expression profiling for molecular classification of multiple myeloma in newly diagnosed patients Blood 116 2010 2543 2553
16. S. Kumar, R. Fonseca, and R.P. Ketterling Trisomies in multiple myeloma: impact on survival in patients with high-risk cytogenetics Blood 119 2012 2100 2105
17. M.A. Chapman, M.S. Lawrence, and J.J. Keats Initial genome sequencing and analysis of multiple myeloma Nature 471 2011 467 472
18. A.L. Shaffer, N.C. Emre, and L. Lamy IRF4 addiction in multiple myeloma Nature 454 2008 226 231
19. J.B. Egan, C.X. Shi, and W. Tembe Whole-genome sequencing of multiple myeloma from diagnosis to plasma cell leukemia reveals genomic initiating events, evolution, and clonal tides Blood 120 2012 1060 1066
20. E. Martinez-Garcia, R. Popovic, and D.J. Min The MMSET histone methyl transferase switches global histone methylation and alters gene expression in t(4;14) multiple myeloma cells Blood 117 2011 211 220
21. B.A. Walker, C.P. Wardell, and L. Melchor Intraclonal heterogeneity and distinct molecular mechanisms characterize the development of t(4;14) and t(11;14) myeloma Blood 120 2012 1077 1086
22. J.L. Brito, B. Walker, and M. Jenner MMSET deregulation affects cell cycle progression and adhesion regulons in t(4;14) myeloma plasma cells Haematologica 94 2009 78 86
23. H. Pei, L. Zhang, and K. Luo MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites Nature 470 2011 124 128
24. R. Popovic, E. Martinez, and Q. Zhang MMSET dysregulates gene expression in myeloma through global and focal changes in H3K36 and H3K27 methylation ASH Annual Meeting Abstracts 120 2012 523
25. J. LoBello, M. Gale, A. Watanabe, G. Hostetter, R. Fonseca, and B. Salhia The role of the histone demethyltransferase gene JMJD1C and H3K9 methylation in multiple myeloma ASH Annual Meeting Abstracts 120 2012 3527
26. B.A. Walker, C.P. Wardell, and L. Chiecchio Aberrant global methylation patterns affect the molecular pathogenesis and prognosis of multiple myeloma Blood 117 2011 553 562
27. S.A. Forbes, N. Bindal, and S. Bamford COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer Nucleic Acids Res 39 2011 D945 D950
28. J.J. Keats, M. Chesi, and J.B. Egan Clonal competition with alternating dominance in multiple myeloma Blood 120 2012 1067 1076
29. J. Egan, K.M. Kortuem, and C.-X. Shi The myeloma genome in drug refractory extra-medullary disease identifies mutations in proteasome, cereblon and glucocorticoid pathways ASH Annual Meeting Abstracts 120 2012 3968
30. Y.X. Zhu, E. Braggio, and C.X. Shi Cereblon expression is required for the antimyeloma activity of lenalidomide and pomalidomide Blood 118 2011 4771 4779
31. A. Lopez-Girona, D. Mendy, and T. Ito Cereblon is a direct protein target for immunomodulatory and antiproliferative activities of lenalidomide and pomalidomide Leukemia 26 2012 2326 2335
32. M.N. Needle, B. Harrison, and C. Hoban The Multiple Myeloma Research Foundation (MMRF) CoMMpassSM study: a longitudinal study in newly-diagnosed multiple myeloma patients to assess genomic profiles, immunophenotypes and clinical outcomes ASH Annual Meeting Abstracts 120 2012 3980
33. F. Pichiorri, S.S. Suh, and M. Ladetto MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis Proc Natl Acad Sci U S A 105 2008 12885 12890
34. Y. Zhou, L. Chen, and B. Barlogie High-risk myeloma is associated with global elevation of miRNAs and overexpression of EIF2C2/AGO2 Proc Natl Acad Sci U S A 107 2010 7904 7909
35. L. Benetatos, and G. Vartholomatos Deregulated microRNAs in multiple myeloma Cancer 118 2012 878 887
36. P. Tagliaferri, M. Rossi, and M.T. Di Martino Promises and challenges of microRNA-based treatment of multiple myeloma Curr Cancer Drug Targets 12 2012 838 846
37. T.C. Chang, D. Yu, and Y.S. Lee Widespread microRNA repression by Myc contributes to tumorigenesis Nat Genet 40 2008 43 50
38. N. Amodio, M.T.D. Martino, and U. Foresta MiR-29b exerts anti-multiple myeloma activity by targeting key oncogenic pathways and modulating DNA methylation profile ASH Annual Meeting Abstracts 120 2012 2941
39. N. Amodio, M. Leotta, and D. Bellizzi DNA-demethylating and anti-tumor activity of synthetic miR-29b mimics in multiple myeloma Oncotarget 3 2012 1246 1258
40. E. Stebner, P. Neri, and J. Johnson Mir-34a sensitizes multiple myeloma (MM) cells to the proteasome inhibitor bortezomib ASH Annual Meeting Abstracts 118 2011 138
41. M.T. Di Martino, E. Leone, and N. Amodio Synthetic miR-34a mimics as a novel therapeutic agent for multiple myeloma: in vitro and in vivo evidence Clin Cancer Res 18 2012 6260 6270
42. P. Wu, L. Agnelli, and B.A. Walker Improved risk stratification in myeloma using microrna-based classifier ASH Annual Meeting Abstracts 120 2012 932
43. M. Rossi, M.R. Pitari, and N. Amodio miR-29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma-related bone disease J Cell Physiol 228 2013 1506 1515
44. M. Wade, Y.C. Li, and G.M. Wahl MDM2, MDMX and p53 in oncogenesis and cancer therapy Nat Rev Cancer 13 2012 83 96
45. D. Chauhan, H. Uchiyama, and Y. Akbarali Multiple myeloma cell adhesion-induced interleukin-6 expression in bone marrow stromal cells involves activation of NF-kappa B Blood 87 1996 1104 1112
46. D.W. McMillin, J. Delmore, and E. Weisberg Tumor cell-specific bioluminescence platform to identify stroma-induced changes to anticancer drug activity Nature Med 16 2010 483 489
47. T. Steinbrunn, T. Stuhmer, C. Sayehli, M. Chatterjee, H. Einsele, and R.C. Bargou Combined targeting of MEK/MAPK and PI3K/Akt signalling in multiple myeloma Br J Haematol 159 2012 430 440
48. C.M. Annunziata, L. Hernandez, and R.E. Davis A mechanistic rationale for MEK inhibitor therapy in myeloma based on blockade of MAF oncogene expression Blood 117 2011 2396 2404
49. A. Zollinger, T. Stuhmer, and M. Chatterjee Combined functional and molecular analysis of tumor cell signaling defines 2 distinct myeloma subgroups: Akt-dependent and Akt-independent multiple myeloma Blood 112 2008 3403 3411
50. T. Hideshima, P.L. Bergsagel, W.M. Kuehl, and K.C. Anderson Advances in biology of multiple myeloma: clinical applications Blood 104 2004 607 618
51. T.R. Peterson, M. Laplante, and C.C. Thoreen DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival Cell 137 2009 873 886
52. K.D. Boyd, B.A. Walker, and C.P. Wardell High expression levels of the mammalian target of rapamycin inhibitor DEPTOR are predictive of response to thalidomide in myeloma Leuk Lymphoma 51 2010 2126 2129
53. V. Fernandez-Saiz, B.S. Targosz, and S. Lemeer SCF(Fbxo9) and CK2 direct the cellular response to growth factor withdrawal via Tel2/Tti1 degradation and promote survival in multiple myeloma Nature Cell Biol 15 2013 72 81
54. D.W. McMillin, M. Ooi, and J. Delmore Antimyeloma activity of the orally bioavailable dual phosphatidylinositol 3-kinase/mammalian target of rapamycin inhibitor NVP-BEZ235 Cancer Res 69 2009 5835 5842
55. P. Baumann, L. Schneider, S. Mandl-Weber, F. Oduncu, and R. Schmidmaier Simultaneous targeting of PI3K and mTOR with NVP-BGT226 is highly effective in multiple myeloma Anticancer Drugs 23 2012 131 138
56. P. Maiso, Y. Liu, and B. Morgan Defining the role of TORC1/2 in multiple myeloma Blood 118 2011 6860 6870
57. N. Mimura, H. Ohguchi, and D. Cirstea TAS-117, a novel selective Akt inhibitor demonstrates significant growth inhibition in multiple myeloma cells in vitro and in vivo ASH Annual Meeting Abstracts 120 2012 942
58. M. Colombo, L. Mirandola, and N. Platonova Notch-directed microenvironment reprogramming in myeloma: a single path to multiple outcomes Leukemia 27 2013 1009 1018
59. S. Manier, A. Sacco, X. Leleu, I.M. Ghobrial, and A.M. Roccaro Bone marrow microenvironment in multiple myeloma progression J Biomed Biotechnol 2012 2012 157496
60. D. Xu, J. Hu, and E. De Bruyne Dll1/Notch activation contributes to bortezomib resistance by upregulating CYP1A1 in multiple myeloma Biochem Biophys Res Commun 428 2012 518 524
61. L. Mirandola, L. Apicella, and M. Colombo Anti-Notch treatment prevents multiple myeloma cells localization to the bone marrow via the chemokine system CXCR4/SDF-1 Leukemia 27 2013 1558 1566
62. S. Blotta, J. Jakubikova, and T. Calimeri Canonical and noncanonical Hedgehog pathway in the pathogenesis of multiple myeloma Blood 120 2012 5002 5013
63. C.D. Peacock, Q. Wang, and G.S. Gesell Hedgehog signaling maintains a tumor stem cell compartment in multiple myeloma Proc Natl Acad Sci U S A 104 2007 4048 4053
64. M. Axelson, K. Liu, and X. Jiang US Food and drug administration approval: vismodegib for recurrent, locally advanced, or metastatic basal cell carcinoma Clin Cancer Res 19 2013 2289 2293
65. S. Pozzi, M. Fulciniti, and H. Yan In vivo and in vitro effects of a novel anti-Dkk1 neutralizing antibody in multiple myeloma Bone 53 2013 487 496
66. K.A. Kocemba, R.W. Groen, and H. van Andel Transcriptional silencing of the Wnt-antagonist DKK1 by promoter methylation is associated with enhanced Wnt signaling in advanced multiple myeloma PloS One 7 2012 e30359
67. B.A. Narayanan, N.A. Doudican, and J. Park Antagonistic effect of small-molecule inhibitors of Wnt/beta-catenin in multiple myeloma Anticancer Res 32 2012 4697 4707
68. E.M. Hurt, A. Wiestner, and A. Rosenwald Overexpression of c-maf is a frequent oncogenic event in multiple myeloma that promotes proliferation and pathological interactions with bone marrow stroma Cancer Cell 5 2004 191 199
69. P.L. Bergsagel, W.M. Kuehl, F. Zhan, J. Sawyer, B. Barlogie, and J. Shaughnessy Jr Cyclin D dysregulation: an early and unifying pathogenic event in multiple myeloma Blood 106 2005 296 303
70. H. Avet-Loiseau, M. Attal, and P. Moreau Genetic abnormalities and survival in multiple myeloma: the experience of the Intergroupe Francophone du Myelome Blood 109 2007 3489 3495
71. M. Chesi, D.F. Robbiani, and M. Sebag AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies Cancer Cell 13 2008 167 180
72. J.E. Delmore, G.C. Issa, and M.E. Lemieux BET bromodomain inhibition as a therapeutic strategy to target c-Myc Cell 146 2011 904 917
73. S.R. Schuster, K.M. Kortuem, and Y.X. Zhu Cereblon expression predicts response, progression free and overall survival after pomalidomide and dexamethasone therapy in multiple myeloma ASH Annual Meeting Abstracts 120 2012 194
74. R.E. Tiedemann, X. Mao, and C.X. Shi Identification of kinetin riboside as a repressor of CCND1 and CCND2 with preclinical antimyeloma activity J Clin Invest 118 2008 1750 1764
75. G. Tchakarska, A. Le Lan-Leguen, L. Roth, and B. Sola The targeting of the sole cyclin D1 is not adequate for mantle cell lymphoma and myeloma therapies Haematologica 94 2009 1781 1782
76. S.K. Kumar, B.R. LaPlant, and W.J. Chng Phase 1/2 trial of a novel CDK inhibitor dinaciclib (SCH727965) in patients with relapsed multiple myeloma demonstrates encouraging single agent activity ASH Annual Meeting Abstracts 120 2012 76
77. W.G. Tong, R. Chen, and W. Plunkett Phase I and pharmacologic study of SNS-032, a potent and selective Cdk2, 7, and 9 inhibitor, in patients with advanced chronic lymphocytic leukemia and multiple myeloma J Clin Oncol 28 2010 3015 3022
78. P.L. Bergsagel, M. Affer, and O.K. Glebov ASH Annual Meeting Abstracts Promiscuous cryptic rearrangements of the MYC locus cis-dysregulate MYC expression and are present in the majority of patients with hyperdiploid myeloma. ASH Annual Meeting Abstracts 120 2012 724
79. J.A. Mertz, A.R. Conery, and B.M. Bryant Targeting MYC dependence in cancer by inhibiting BET bromodomains Proc Natl Acad Sci U S A 108 2011 16669 16674
80. H. Chang, S. Sloan, and D. Li The t(4;14) is associated with poor prognosis in myeloma patients undergoing autologous stem cell transplant Br J Haematol 125 2004 64 68
81. F. Quintero-Rivera, R. El-Sabbagh Badr, and P.N. Rao FGFR3 amplification in the absence of IGH@-FGFR3 fusion t(4;14) in myeloma Cancer Genet Cytogenet 195 2009 92 93
82. J. Qing, X. Du, and Y. Chen Antibody-based targeting of FGFR3 in bladder carcinoma and t(4;14)-positive multiple myeloma in mice J Clin Invest 119 2009 1216 1229
83. S. Trudel, Z.H. Li, and E. Wei CHIR-258, a novel, multitargeted tyrosine kinase inhibitor for the potential treatment of t(4;14) multiple myeloma Blood 105 2005 2941 2948
84. M. Chesi, and P.L. Bergsagel Many multiple myelomas: making more of the molecular mayhem Hematology/Education Program of the American Society of Hematology American Society of Hematology Education Program 2011 2011 344 353
85. M. Andrulis, N. Lehners, and D. Capper Targeting the BRAF V600E mutation in multiple myeloma Cancer Disc 2013
86. N. Sheth, J. Yeung, and H. Chang p53 nuclear accumulation is associated with extramedullary progression of multiple myeloma Leuk Res 33 2009 1357 1360
87. M.G. Ooi, P.J. Hayden, and V. Kotoula Interactions of the Hdm2/p53 and proteasome pathways may enhance the antitumor activity of bortezomib Clin Cancer Res 15 2009 7153 7160
88. M.N. Saha, H. Jiang, Y. Yang, D. Reece, and H. Chang Small molecule MIRA-1 induces p53-independent apoptosis in multiple myeloma cells through activation of the p38 MAPK signaling pathway ASH Annual Meeting Abstracts 120 2012 2937
89. S. Lehmann, V.J. Bykov, and D. Ali Targeting p53 in vivo: a first-in-human study with p53-targeting compound APR-246 in refractory hematologic malignancies and prostate cancer J Clin Oncol 30 2012 3633 3639
90. B.J. Tunquist, R.D. Woessner, and D.H. Walker Mcl-1 stability determines mitotic cell fate of human multiple myeloma tumor cells treated with the kinesin spindle protein inhibitor ARRY-520 Mol Cancer Therapeut 9 2010 2046 2056
91. J.J. Shah, J.A. Zonder, and A. Cohen The novel KSP inhibitor ARRY-520 is active both with and without low-dose dexamethasone in patients with multiple myeloma refractory to bortezomib and lenalidomide: results from a phase 2 study ASH Annual Meeting Abstracts 120 2012 449
92. J.J. Shah, D.M. Weber, and S.K. Thomas Phase 1 study of the novel kinesin spindle protein inhibitor ARRY-520 + carfilzomib in patients with relapsed and/or refractory multiple myeloma ASH Annual Meeting Abstracts 120 2012 4082
93. R.E. Tiedemann, Y.X. Zhu, and J. Schmidt Identification of molecular vulnerabilities in human multiple myeloma cells by RNA interference lethality screening of the druggable genome Cancer Res 72 2012 757 768
94. J. Schmidt, E. Braggio, and M. Chesi Genome wide studies in multiple myeloma identify XPO1/CRM-1 as a critical target validated using the selective inhibitor of nuclear export (SINE) KPT-276 ASH Annual Meeting Abstracts 120 2012 573
95. J. Schmidt, E. Braggio, and K.M. Kortuem Genome-wide studies in multiple myeloma identify XPO1/CRM1 as a critical target validated using the selective nuclear export inhibitor KPT-276 Leukemia. Epub 2013 Jun 11 10.1038/leu.2013. Available from: www.nature.com.
96. Y.-T. Tai, Y. Landesman, and C. Acharya CRM1 blockade by novel inhibitors of nuclear export (SINEs) inhibits multiple myeloma cell growth, osteoclastogenesis, and myeloma-induced osteolysis ASH Annual Meeting Abstracts 120 2012 326
97. I. Borrello Can we change the disease biology of multiple myeloma? Leuk Res 36Suppl 1 2012 S3 12
98. J. Rosenblatt, I. Avivi, and B. Vasir Blockade of PD-1 in combination with dendritic cell/myeloma fusion cell vaccination following autologous stem cell transplantation ASH Annual Meeting Abstracts 120 2012 578
99. T. Plesner, H. Lokhorst, P. Gimsing, H. Nahi, S. Lisby, and P.G. Richardson Daratumumab, a CD38 monoclonal antibody in patients with multiple myeloma - data from a dose-escalation phase I/II study ASH Annual Meeting Abstracts 120 2012 73
100. A.J. Jakubowiak, D.M. Benson, and W. Bensinger Phase I trial of anti-CS1 monoclonal antibody elotuzumab in combination with bortezomib in the treatment of relapsed/refractory multiple myeloma J Clin Oncol 30 2012 1960 1965
101. S. Lonial, R. Vij, and J.L. Harousseau Elotuzumab in combination with lenalidomide and low-dose dexamethasone in relapsed or refractory multiple myeloma J Clin Oncol 30 2012 1953 1959
102. P.G. Richardson, S. Jagannath, and P. Moreau A phase 2 study of elotuzumab (Elo) in combination with lenalidomide and low-dose dexamethasone (Ld) in patients (pts) with relapsed/refractory multiple myeloma (R/R MM): updated results ASH Annual Meeting Abstracts 120 2012 202
103. J.A. Zonder, A.F. Mohrbacher, and S. Singhal A phase 1, multicenter, open-label, dose escalation study of elotuzumab in patients with advanced multiple myeloma Blood 120 2012 552 559
104. M.K. Brimnes, A.J. Vangsted, and L.M. Knudsen Increased level of both CD4+FOXP3+ regulatory T cells and CD14+HLA-DR(-)/low myeloid-derived suppressor cells and decreased level of dendritic cells in patients with multiple myeloma Scand J Immunol 72 2010 540 547
105. G.T. Gorgun, G. Whitehill, and J.L. Anderson Tumor-promoting immune-suppressive myeloid-derived suppressor cells in the multiple myeloma microenvironment in humans Blood 121 2013 2975 2987
106. I.R. Ramachandran, A. Martner, and A. Pisklakova Myeloid-derived suppressor cells regulate growth of multiple myeloma by inhibiting T cells in bone marrow J Immunol 190 2013 3815 3823
107. E. Van Valckenborgh, E. Schouppe, and K. Movahedi Multiple myeloma induces the immunosuppressive capacity of distinct myeloid-derived suppressor cell subpopulations in the bone marrow Leukemia 26 2012 2424 2428
108. J.M. Negri, D.W. McMillin, and J. Delmore In vitro anti-myeloma activity of the Aurora kinase inhibitor VE-465 Br J Haematol 147 2009 672 676
109. D.W. McMillin, J. Delmore, and J. Negri Microenvironmental influence on pre-clinical activity of polo-like kinase inhibition in multiple myeloma: implications for clinical translation PloS One 6 2011 e20226
110. S. Cao, D.W. McMillin, G. Tamayo, J. Delmore, C.S. Mitsiades, and J. Clardy Inhibition of tumor cells interacting with stromal cells by xanthones isolated from a Costa Rican Penicillium sp J Natural Prod 75 2012 793 797
111. D.W. McMillin, J. Delmore, and J.M. Negri Compartment-specific bioluminescence imaging platform for the high-throughput evaluation of antitumor immune function Blood 119 2012 e131 e138
112. D.W. McMillin, and C.S. Mitsiades High-throughput approaches to discover novel immunomodulatory agents for cancer Oncoimmunology 1 2012 1406 1408
113. D.W. McMillin, J.M. Negri, and C.S. Mitsiades The role of tumour-stromal interactions in modifying drug response: challenges and opportunities Nature Rev Drug Disc 12 2013 217 228
114. M.F. Kaiser, U. Heider, and M. Mieth Induction of CXCL1 in osteoblasts by myeloma cells promotes migration of osteoclast precursors ASH Annual Meeting Abstracts 120 2012 441
115. M. Fulciniti, P. Tassone, and T. Hideshima Anti-DKK1 mAb (BHQ880) as a potential therapeutic agent for multiple myeloma Blood 114 2009 371 379
116. S. Yaccoby, W. Ling, F. Zhan, R. Walker, B. Barlogie, and J.D. Shaughnessy Jr Antibody-based inhibition of DKK1 suppresses tumor-induced bone resorption and multiple myeloma growth in vivo Blood 109 2007 2106 2111
117. C.M. Edwards, J.R. Edwards, and S.T. Lwin Increasing Wnt signaling in the bone marrow microenvironment inhibits the development of myeloma bone disease and reduces tumor burden in bone in vivo Blood 111 2008 2833 2842
118. G.T. Gorgun, G. Whitehill, and J.L. Anderson Tumor promoting immune suppressive myeloid derived suppressor cells in multiple myeloma microenvironment Blood 121 2013 2975 2987
119. G.J. Morgan, F.E. Davies, and W.M. Gregory First-line treatment with zoledronic acid as compared with clodronic acid in multiple myeloma (MRC Myeloma IX): a randomised controlled trial Lancet 376 2010 1989 1999
120. D. Chauhan, A.V. Singh, and M. Brahmandam Functional interaction of plasmacytoid dendritic cells with multiple myeloma cells: a therapeutic target Cancer Cell 16 2009 309 323
121. J.R. Nair, M. Murray, C. Koorella, L.M. Carlson, L.H. Boise, and K.P. Lee Targeting the cellular and molecular components of CD28 mediated survival signaling in multiple myeloma ASH Annual Meeting Abstracts 120 2012 722
122. M.E. Murray, J.R. Nair, and K.P. Lee CD28-mediated pro-survival signaling in multiple myeloma ASH Annual Meeting Abstracts 120 2012 941
123. S. Koduru, E. Wong, and T. Strowig Dendritic cell-mediated activation-induced cytidine deaminase (AID)-dependent induction of genomic instability in human myeloma Blood 119 2012 2302 2309
124. Y. Zheng, J. Yang, and J. Qian PSGL-1/selectin and ICAM-1/CD18 interactions are involved in macrophage-induced drug resistance in myeloma Leukemia 27 2013 702 710
125. E. Hebron, C. Hope, and J. Kim MAP3K8 kinase regulates myeloma growth by cell-autonomous and non-autonomous mechanisms involving myeloma-associated monocytes/macrophages Br J Haematol 160 2013 779 784
126. J. Hu, D.R. Handisides, and E. Van Valckenborgh Targeting the multiple myeloma hypoxic niche with TH-302, a hypoxia-activated prodrug Blood 116 2010 1524 1527