Growth differentiating factor 15 enhances the tumor-initiating and self-renewal potential of multiple myeloma cells

Blood

Volumn 123, Issue 5, 2014, Pages 725-733

  Tanno, Toshihiko ^a   Lim, Yiting ^a   Wang, Qiuju ^a   Chesi, Marta ^b   Bergsagel, P Leif ^b   Matthews, Geoff ^c   Johnstone, Ricky W ^c   Ghosh, Nilanjan ^a   Borrello, Ivan ^a   Huff, Carol Ann ^a   Matsui, William ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b MAYO CLINIC   (United States)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 15; PROTEIN KINASE B; SYNDECAN 1; TESTIS DETERMINING FACTOR; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CANCER STEM CELL; CELL EXPANSION; CELL POPULATION; CELL RENEWAL; COLONY FORMATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; MULTIPLE MYELOMA CELL LINE; NONHUMAN; PLASMA CELL; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; STROMA CELL; TUMOR CELL; TUMOR INITIATING CELL; TUMOR MICROENVIRONMENT; ANIMAL; BLOOD; C57BL MOUSE; CELL PROLIFERATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; GROWTH DIFFERENTIATION FACTOR 15; HUMANS; MICE; MICE, INBRED C57BL; MULTIPLE MYELOMA; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

EID: 84897022788     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-08-524025     Document Type: Article

References (52)

1. Palumbo A, Anderson K. Multiple myeloma. N Engl J Med. 2011;364(11):1046-1060.
2. Scadden DT. The stem-cell niche as an entity of action. Nature. 2006;441(7097):1075-1079. (Pubitemid 43990719)
3. Wang LD, Wagers AJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol. 2011;12(10):643-655.
4. Corre J, Mahtouk K, Attal M, et al. Bone marrow mesenchymal stem cells are abnormal in multiple myeloma. Leukemia. 2007;21(5):1079-1088. (Pubitemid 46672085)
5. Corre J, Labat E, Espagnolle N, et al. Bioactivity and prognostic significance of growth differentiation factor GDF15 secreted by bone marrow mesenchymal stem cells in multiple myeloma. Cancer Res. 2012;72(6):1395-1406.
6. Bootcov MR, Bauskin AR, Valenzuela SM, et al. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc Natl Acad Sci USA. 1997;94(21):11514-11519. (Pubitemid 27451030)
7. Staff AC, Trovik J, Eriksson AG, et al. Elevated plasma growth differentiation factor-15 correlates with lymph node metastases and poor survival in endometrial cancer. Clin Cancer Res. 2011;17(14):4825-4833.
8. Wallin U, Glimelius B, Jirström K, et al. Growth differentiation factor 15: a prognostic marker for recurrence in colorectal cancer. Br J Cancer. 2011;104(10):1619-1627.
9. Brown DA, Lindmark F, Stattin P, et al. Macrophage inhibitory cytokine 1: a new prognostic marker in prostate cancer. Clin Cancer Res. 2009;15(21):6658-6664.
10. Koopmann J, Rosenzweig CNW, Zhang Z, et al. Serum markers in patients with resectable pancreatic adenocarcinoma: macrophage inhibitory cytokine 1 versus CA19-9. Clin Cancer Res. 2006;12(2):442-446. (Pubitemid 43166133)
11. Matsui W, Huff CA, Wang Q, et al. Characterization of clonogenic multiple myeloma cells. Blood. 2004;103(6):2332-2336. (Pubitemid 38326254)
12. Matsui W, Wang Q, Barber JP, et al. Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res. 2008;68(1):190-197. (Pubitemid 351380120)
13. Hu Y, Smyth GK. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods. 2009;347(1-2):70-78.
14. Kempf T, Eden M, Strelau J, et al. The transforming growth factor-beta superfamily member growth-differentiation factor-15 protects the heart from ischemia/reperfusion injury. Circ Res. 2006;98(3):351-360.
15. Naka K, Hoshii T, Muraguchi T, et al. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature. 2010;463(7281):676-680.
16. Eyler CE, Foo W-C, LaFiura KM, McLendon RE, Hjelmeland AB, Rich JN. Brain cancer stem cells display preferential sensitivity to Akt inhibition. Stem Cells. 2008;26(12):3027-3036.
17. Peltier J, Conway A, Keung AJ, Schaffer DV. Akt increases sox2 expression in adult hippocampal neural progenitor cells, but increased sox2 does not promote proliferation. Stem Cells Dev. 2011;20(7):1153-1161.
18. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 2003;17(1):126-140. (Pubitemid 36062514)
19. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663-676. (Pubitemid 44233629)
20. Spisek R, Kukreja A, Chen L-C, et al. Frequent and specific immunity to the embryonal stem cell-associated antigen SOX2 in patients with monoclonal gammopathy. J Exp Med. 2007;204(4):831-840. (Pubitemid 46631612)
21. Park IK, Qian D, Kiel M, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003;423(6937):302-305. (Pubitemid 40852701)
22. Molofsky AV, Pardal R, Iwashita T, Park I-K, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425(6961):962-967. (Pubitemid 37376927)
23. Jagani Z, Wiederschain D, Loo A, et al. The Polycomb group protein Bmi-1 is essential for the growth of multiple myeloma cells. Cancer Res. 2010;70(13):5528-5538.
24. Hsiao EC, Koniaris LG, Zimmers-Koniaris T, Sebald SM, Huynh TV, Lee SJ. Characterization of growth-differentiation factor 15, a transforming growth factor beta superfamily member induced following liver injury. Mol Cell Biol. 2000;20(10):3742-3751. (Pubitemid 30243919)
25. Chesi M, Robbiani DF, Sebag M, et al. AID-dependent activation of a MYC transgene induces multiple myeloma in a conditional mouse model of post-germinal center malignancies. Cancer Cell. 2008;13(2):167-180. (Pubitemid 351163163)
26. Jakubikova J, Adamia S, Kost-Alimova M, et al. Lenalidomide targets clonogenic side population in multiple myeloma: pathophysiologic and clinical implications. Blood. 2011;117(17):4409-4419.
27. Hawley TS, Riz I, Yang W, et al. Identification of an ABCB1 (P-glycoprotein)-positive carfilzomib-resistant myeloma subpopulation by the pluripotent stem cell fluorescent dye CDy1. Am J Hematol. 2013;88(4):265-272.
28. Hess DA, Meyerrose TE, Wirthlin L, et al. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood. 2004;104(6):1648-1655. (Pubitemid 39202270)
29. Ginestier C, Hur MH, Charafe-Jauffret E, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1(5):555-567. (Pubitemid 350056407)
30. Rasheed ZA, Yang J, Wang Q, et al. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst. 2010;102(5):340-351.
31. Huff C, Wang Q, Rogers K, et al. Correlation of clonogenic cancer stem cell (CSC) growth with clinical outcomes in multiple myeloma (MM) patients undergoing treatment with high dose cyclophosphamide (Cy) and rituximab. AACR Meeting Abstracts. 2008;2008:LB-87.
32. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66(19):9339-9344.
33. Lobo NA, Shimono Y, Qian D, Clarke MF. The biology of cancer stem cells. Annu Rev Cell Dev Biol. 2007;23:675-699.
34. Billadeau D, Ahmann G, Greipp P, Van Ness B. The bone marrow of multiple myeloma patients contains B cell populations at different stages of differentiation that are clonally related to the malignant plasma cell. J Exp Med. 1993;178(3):1023-1031. (Pubitemid 23260440)
35. Kirshner J, Thulien KJ, Martin LD, et al. A unique three-dimensional model for evaluating the impact of therapy on multiple myeloma. Blood. 2008;112(7):2935-2945.
36. Chaidos A, Barnes CP, Cowan G, et al. Clinical drug resistance linked to interconvertible phenotypic and functional states of tumor-propagating cells in multiple myeloma. Blood. 2013;121(2):318-328.
37. Boucher K, Parquet N, Widen R, et al. Stemness of B-cell progenitors in multiple myeloma bone marrow. Clin Cancer Res. 2012;18(22):6155-6168.
38. Bergsagel DE, Valeriote FA. Growth characteristics of a mouse plasma cell tumor. Cancer Res. 1968;28(11):2187-2196.
39. Hamburger AW, Salmon SE. Primary bioassay of human tumor stem cells. Science. 1977;197(4302):461-463.
40. Yaccoby S, Barlogie B, Epstein J. Primary myeloma cells growing in SCID-hu mice: a model for studying the biology and treatment of myeloma and its manifestations. Blood. 1998;92(8):2908-2913. (Pubitemid 28469106)
41. Yaccoby S, Epstein J. The proliferative potential of myeloma plasma cells manifest in the SCID-hu host. Blood. 1999;94(10):3576-3582. (Pubitemid 29536154)
42. Kim D, Park CY, Medeiros BC, Weissman IL. CD19-CD45 low/- CD38 high/CD138+ plasma cells enrich for human tumorigenic myeloma cells. Leukemia. 2012;26(12):2530-2537.
43. Van Valckenborgh E, Matsui W, Agarwal P, et al. Tumor-initiating capacity of CD138- and CD138+ tumor cells in the 5T33 multiple myeloma model. Leukemia. 2012;26(6):1436-1439.
44. Jamieson CHM, Ailles LE, Dylla SJ, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med. 2004;351(7):657-667. (Pubitemid 39063268)
45. Griner SE, Joshi JP, Nahta R. Growth differentiation factor 15 stimulates rapamycin-sensitive ovarian cancer cell growth and invasion. Biochem Pharmacol. 2013;85(1):46-58.
46. Ramani VC, Purushothaman A, Stewart MD, et al. The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J. 2013;280(10):2294-2306.
47. Bauskin AR, Brown DA, Kuffner T, et al. Role of macrophage inhibitory cytokine-1 in tumorigenesis and diagnosis of cancer. Cancer Res. 2006;66(10):4983-4986. (Pubitemid 43852864)
48. Yaccoby S. The phenotypic plasticity of myeloma plasma cells as expressed by dedifferentiation into an immature, resilient, and apoptosis-resistant phenotype. Clin Cancer Res. 2005;11(21):7599-7606. (Pubitemid 41611599)
49. Matsui W, Huff CA, Vala M, Barber J, Smith BD, Jones RJ. Anti-tumour activity of interferon-alpha in multiple myeloma: role of interleukin 6 and tumor cell differentiation. Br J Haematol. 2003;121(2):251-258. (Pubitemid 36560591)
50. Mimeault M, Batra SK. Divergent molecular mechanisms underlying the pleiotropic functions of macrophage inhibitory cytokine-1 in cancer. J Cell Physiol. 2010;224(3):626-635.
51. Yang H, Filipovic Z, Brown D, Breit SN, Vassilev LT. Macrophage inhibitory cytokine-1: a novel biomarker for p53 pathway activation. Mol Cancer Ther. 2003;2(10):1023-1029.
52. Osada M, Park HL, Nagakawa Y, et al. Differential recognition of response elements determines target gene specificity for p53 and p63. Mol Cell Biol. 2005;25(14):6077-6089. (Pubitemid 40946559)