Myeloma cell-derived Runx2 promotes myeloma progression in bone

Blood

Volumn 125, Issue 23, 2015, Pages 3598-3608

  Trotter, Timothy N ^a   Li, Mei ^a   Pan, Qianying ^a,b   Peker, Deniz ^a   Rowan, Patrick D ^a   Li, Juan ^b   Zhan, Fenghuang ^c   Suva, Larry J ^d   Javed, Amjad ^e,f   Yang, Yang ^a,e  

^a University of Alabama at Birmingham   (United States)

^b THE FIRST AFFILIATED HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f Univ of Alabama School of Dentistry   (United States)

Author keywords

High levels of Runx2 expression are associated with a high risk myeloma population.; Myeloma cell derived Runx2 promotes myeloma progression

Indexed keywords

BETA CATENIN; CYTOKINE; DENTIN MATRIX PROTEIN 1; EPIDERMAL GROWTH FACTOR; GELATINASE B; INTERLEUKIN 9; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPONTIN; PROTEIN KINASE B; STROMAL CELL DERIVED FACTOR 1; SURVIVIN; TRANSCRIPTION FACTOR RUNX2; VASCULOTROPIN; BIRC5 PROTEIN, HUMAN; BIRC5 PROTEIN, MOUSE; INHIBITOR OF APOPTOSIS PROTEIN; REPRESSOR PROTEIN; RUNX2 PROTEIN, HUMAN; RUNX2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; GENE OVEREXPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MONOCLONAL IMMUNOGLOBULINEMIA; MOUSE; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR MICROENVIRONMENT; UPREGULATION; ANIMAL; BIOSYNTHESIS; BONE TUMOR; ETIOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; OSTEOLYSIS; PATHOLOGY; SECONDARY; TUMOR CELL LINE;

ANIMALS; BETA CATENIN; BONE NEOPLASMS; CELL LINE, TUMOR; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MICE; MULTIPLE MYELOMA; NEOPLASM METASTASIS; OSTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS;

EID: 84961159473     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-12-613968     Document Type: Article

References (70)

1. Yang Y, Macleod V, Bendre M, et al. Heparanase promotes the spontaneous metastasis of myeloma cells to bone. Blood. 2005;105(3): 1303-1309.
2. Anderson KC, Carrasco RD. Pathogenesis of myeloma. Annu Rev Pathol. 2011;6:249-274.
3. Barlogie B, Mitchell A, van Rhee F, Epstein J, Morgan GJ, Crowley J. Curing myeloma at last: defining criteria and providing the evidence. Blood. 2014;124(20):3043-3051.
4. Noll JE, Williams SA, Tong CM, et al. Myeloma plasma cells alter the bone marrow microenvironment by stimulating the proliferation of mesenchymal stromal cells. Haematologica. 2014;99(1):163-171.
5. Jagannath S. Pathophysiological underpinnings of multiple myeloma progression. J Manag Care Pharm. 2008;14(suppl 7):7-11.
6. Kania MA, Bonner AS, Duffy JB, Gergen JP. The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev. 1990;4(10):1701-1713.
7. Mori K, Kitazawa R, Kondo T, Maeda S, Yamaguchi A, Kitazawa S. Modulation of mouse RANKL gene expression by Runx2 and PKA pathway. J Cell Biochem. 2006;98(6):1629-1644.
8. Karsenty G. Transcriptional control of skeletogenesis. Annu Rev Genomics Hum Genet. 2008;9:183-196.
9. Marie PJ. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 2008;473(2):98-105.
10. van der Deen M, Akech J, Wang T, et al. The cancer-related Runx2 protein enhances cell growth and responses to androgen and TGFbeta in prostate cancer cells. J Cell Biochem. 2010; 109(4):828-837.
11. Das K, Leong DT, Gupta A, et al. Positive association between nuclear Runx2 and oestrogen-progesterone receptor gene expression characterises a biological subtype of breast cancer. Eur J Cancer. 2009;45(13): 2239-2248.
12. Khalid O, Baniwal SK, Purcell DJ, et al. Modulation of Runx2 activity by estrogen receptor-alpha: implications for osteoporosis and breast cancer. Endocrinology. 2008;149(12): 5984-5995.
13. Pratap J, Lian JB, Javed A, et al. Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev. 2006;25(4):589-600.
14. Akech J, Wixted JJ, Bedard K, et al. Runx2 association with progression of prostate cancer in patients: mechanisms mediating bone osteolysis and osteoblastic metastatic lesions. Oncogene. 2010;29(6):811-821.
15. Baniwal SK, Khalid O, Gabet Y, et al. Runx2 transcriptome of prostate cancer cells: insights into invasiveness and bone metastasis. Mol Cancer. 2010;9:258.
16. Kayed H, Jiang X, Keleg S, et al. Regulation and functional role of the Runt-related transcription factor-2 in pancreatic cancer. Br J Cancer. 2007; 97(8):1106-1115.
17. Sase T, Suzuki T, Miura K, et al. Runt-related transcription factor 2 in human colon carcinoma: a potent prognostic factor associated with estrogen receptor. Int J Cancer. 2012;131(10):2284-2293.
18. Pratap J, Javed A, Languino LR, et al. The Runx2 osteogenic transcription factor regulates matrix metalloproteinase 9 in bone metastatic cancer cells and controls cell invasion. Mol Cell Biol. 2005;25(19):8581-8591.
19. Pratap J, Wixted JJ, Gaur T, et al. Runx2 transcriptional activation of Indian Hedgehog and a downstream bone metastatic pathway in breast cancer cells. Cancer Res. 2008;68(19): 7795-7802.
20. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-1108.
21. Edwards CM, Lwin ST, Fowler JA, et al. Myeloma cells exhibit an increase in proteasome activity and an enhanced response to proteasome inhibition in the bone marrow microenvironment in vivo. Am J Hematol. 2009;84(5):268-272.
22. Bakkus MH, Asosingh K, Vanderkerken K, et al. Myeloma isotype-switch variants in the murine 5T myeloma model: evidence that myeloma IgM and IgA expressing subclones can originate from the IgG expressing tumour. Leukemia. 2001;15(7): 1127-1132.
23. Zhu D, van Arkel C, King CA, et al. Immunoglobulin VH gene sequence analysis of spontaneous murine immunoglobulin-secreting B-cell tumours with clinical features of human disease. Immunology. 1998;93(2):162-170.
24. van den Akker TW, Radl J, Franken-Postma E, Hagemeijer A. Cytogenetic findings in mouse multiple myeloma and Waldenström's macroglobulinemia. Cancer Genet Cytogenet. 1996;86(2):156-161.
25. Purushothaman A, Chen L, Yang Y, Sanderson RD. Heparanase stimulation of protease expression implicates it as a master regulator of the aggressive tumor phenotype in myeloma. J Biol Chem. 2008;283(47):32628-32636.
26. Riccardi C, Nicoletti I. Analysis of apoptosis by propidium iodide staining and flow cytometry. Nat Protoc. 2006;1(3):1458-1461.
27. Jenkinson SR, Barraclough R, West CR, Rudland PS. S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer. 2004;90(1):253-262.
28. Shaughnessy JD Jr, Zhan F, Burington BE, et al. A validated gene expression model of high-risk multiple myeloma is defined by deregulated expression of genes mapping to chromosome 1. Blood. 2007;109(6):2276-2284.
29. Zhan F, Barlogie B, Mulligan G, Shaughnessy JD Jr, Bryant B. High-risk myeloma: a gene expression based risk-stratification model for newly diagnosed multiple myeloma treated with high-dose therapy is predictive of outcome in relapsed disease treated with single-agent bortezomib or high-dose dexamethasone. Blood. 2008;111(2):968-969.
30. Zhan F, Barlogie B, Arzoumanian V, et al. Geneexpression signature of benign monoclonal gammopathy evident in multiple myeloma is linked to good prognosis. Blood. 2007;109(4): 1692-1700.
31. Kelly T, Miao HQ, Yang Y, et al. High heparanase activity in multiple myeloma is associated with elevated microvessel density. Cancer Res. 2003; 63(24):8749-8756.
32. Gold LI. The role for transforming growth factorbeta (TGF-beta) in human cancer. Crit Rev Oncog. 1999;10(4):303-360.
33. Katsuno Y, Hanyu A, Kanda H, et al. Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene. 2008; 27(49):6322-6333.
34. Hideshima T, Catley L, Raje N, et al. Inhibition of Akt induces significant downregulation of survivin and cytotoxicity in human multiple myeloma cells. Br J Haematol. 2007;138(6):783-791.
35. Nakashima N, Huang CL, Liu D, Ueno M, Yokomise H. Intratumoral Wnt1 expression affects survivin gene expression in non-small cell lung cancer. Int J Oncol. 2010;37(3):687-694.
36. Hirai H, Sootome H, Nakatsuru Y, et al. MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol Cancer Ther. 2010;9(7):1956-1967.
37. Zhang Y, Xie RL, Croce CM, et al. A program of microRNAs controls osteogenic lineage progression by targeting transcription factor Runx2. Proc Natl Acad Sci USA. 2011;108(24): 9863-9868.
38. Yang Y, Ren Y, Ramani VC, Nan L, Suva LJ, Sanderson RD. Heparanase enhances local and systemic osteolysis in multiple myeloma by upregulating the expression and secretion of RANKL. Cancer Res. 2010;70(21):8329-8338.
39. Ruan J, Trotter TN, Nan L, et al. Heparanase inhibits osteoblastogenesis and shifts bone marrow progenitor cell fate in myeloma bone disease. Bone. 2013;57(1):10-17.
40. Lauta VM. A review of the cytokine network in multiple myeloma: diagnostic, prognostic, and therapeutic implications. Cancer. 2003;97(10): 2440-2452.
41. Clowes JA, Riggs BL, Khosla S. The role of the immune system in the pathophysiology of osteoporosis. Immunol Rev. 2005;208:207-227.
42. Maes C, Coenegrachts L, Stockmans I, et al. Placental growth factor mediates mesenchymal cell development, cartilage turnover, and bone remodeling during fracture repair. J Clin Invest. 2006;116(5):1230-1242.
43. Pratap J, Imbalzano KM, Underwood JM, et al. Ectopic runx2 expression in mammary epithelial cells disrupts formation of normal acini structure: implications for breast cancer progression. Cancer Res. 2009;69(17):6807-6814.
44. Onodera Y, Miki Y, Suzuki T, et al. Runx2 in human breast carcinoma: its potential roles in cancer progression. Cancer Sci. 2010;101(12): 2670-2675.
45. Brubaker KD, Vessella RL, Brown LG, Corey E. Prostate cancer expression of runt-domain transcription factor Runx2, a key regulator of osteoblast differentiation and function. Prostate. 2003;56(1):13-22.
46. Li H, Zhou RJ, Zhang GQ, Xu JP. Clinical significance of RUNX2 expression in patients with nonsmall cell lung cancer: a 5-year follow-up study. Tumour Biol. 2013;34(3):1807-1812.
47. Li W, Xu S, Lin S, Zhao W. Overexpression of runt-related transcription factor-2 is associated with advanced tumor progression and poor prognosis in epithelial ovarian cancer. J Biomed Biotechnol. 2012;2012:456534.
48. Colla S, Morandi F, Lazzaretti M, et al. Human myeloma cells express the bone regulating gene Runx2/Cbfa1 and produce osteopontin that is involved in angiogenesis in multiple myeloma patients. Leukemia. 2005;19(12):2166-2176.
49. Javed A, Barnes GL, Pratap J, et al. Impaired intranuclear trafficking of Runx2 (AML3/CBFA1) transcription factors in breast cancer cells inhibits osteolysis in vivo. Proc Natl Acad Sci USA. 2005; 102(5):1454-1459.
50. Testa JR, Tsichlis PN. AKT signaling in normal and malignant cells. Oncogene. 2005;24(50): 7391-7393.
51. Tapia JC, Torres VA, Rodriguez DA, Leyton L, Quest AF. Casein kinase 2 (CK2) increases survivin expression via enhanced beta-catenin-T cell factor/lymphoid enhancer binding factordependent transcription. Proc Natl Acad Sci USA. 2006;103(41):15079-15084.
52. Olie RA, Simões-Wüst AP, Baumann B, et al. A novel antisense oligonucleotide targeting survivin expression induces apoptosis and sensitizes lung cancer cells to chemotherapy. Cancer Res. 2000; 60(11):2805-2809.
53. Komori T. Signaling networks in RUNX2-dependent bone development. J Cell Biochem. 2011;112(3):750-755.
54. Pande S, Browne G, Padmanabhan S, et al. Oncogenic cooperation between PI3K/Akt signaling and transcription factor Runx2 promotes the invasive properties of metastatic breast cancer cells. J Cell Physiol. 2013;228(8): 1784-1792.
55. Shevde LA, Das S, Clark DW, Samant RS. Osteopontin: an effector and an effect of tumor metastasis. Curr Mol Med. 2010;10(1):71-81.
56. Weber GF. The metastasis gene osteopontin: a candidate target for cancer therapy. Biochim Biophys Acta. 2001;1552(2):61-85.
57. John A, Tuszynski G. The role of matrix metalloproteinases in tumor angiogenesis and tumor metastasis. Pathol Oncol Res. 2001;7(1): 14-23.
58. Roodman GD. Genes associate with abnormal bone cell activity in bone metastasis. Cancer Metastasis Rev. 2012;31(3-4):569-578.
59. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006;25(1):9-34.
60. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell. 2010;141(1):52-67.
61. Teicher BA, Fricker SP. CXCL12 (SDF-1)/CXCR4 pathway in cancer. Clin Cancer Res. 2010;16(11): 2927-2931.
62. Anborgh PH, Mutrie JC, Tuck AB, Chambers AF. Role of the metastasis-promoting protein osteopontin in the tumour microenvironment. J Cell Mol Med. 2010;14(8):2037-2044.
63. Manier S, Sacco A, Leleu X, Ghobrial IM, Roccaro AM. Bone marrow microenvironment in multiple myeloma progression. J Biomed Biotechnol. 2012;2012:157496.
64. Menu E, Asosingh K, Indraccolo S, et al. The involvement of stromal derived factor 1alpha in homing and progression of multiple myeloma in the 5TMM model [published correction appears in Haematologica. 2007;92(11):1584]. Haematologica. 2006;91(5):605-612.
65. Standal T, Borset M, Sundan A. Role of osteopontin in adhesion, migration, cell survival and bone remodeling. Exp Oncol. 2004;26(3): 179-184.
66. Singhal H, Bautista DS, Tonkin KS, et al. Elevated plasma osteopontin in metastatic breast cancer associated with increased tumor burden and decreased survival. Clin Cancer Res. 1997;3(4): 605-611.
67. Rudland PS, Platt-Higgins A, El-Tanani M, et al. Prognostic significance of the metastasisassociated protein osteopontin in human breast cancer. Cancer Res. 2002;62(12):3417-3427.
68. Hotte SJ, Winquist EW, Stitt L, Wilson SM, Chambers AF. Plasma osteopontin: associations with survival and metastasis to bone in men with hormone-refractory prostate carcinoma. Cancer. 2002;95(3):506-512.
69. Standal T, Hjorth-Hansen H, Rasmussen T, et al. Osteopontin is an adhesive factor for myeloma cells and is found in increased levels in plasma from patients with multiple myeloma. Haematologica. 2004;89(2):174-182.
70. Saeki Y, Mima T, Ishii T, et al. Enhanced production of osteopontin in multiple myeloma: clinical and pathogenic implications. Br J Haematol. 2003;123(2):263-270.