SOX11 promotes tumor angiogenesis through transcriptional regulation of PDGFA in mantle cell lymphoma

Blood

Volumn 124, Issue 14, 2014, Pages 2235-2247

  Palomero, Jara ^a   Vegliante, Maria Carmela ^a   Rodríguez, Marta Leonor ^a   Eguileor, Álvaro ^a   Castellano, Giancarlo ^a   Planas Rigol, Ester ^b   Jares, Pedro ^a   Ribera Cortada, Inmaculada ^c   Cid, Maria C ^b   Campo, Elias ^a,c   Amador, Virginia ^a  

^a Hematopathology Unit Department of Pathology   (Spain)

^b INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

IMATINIB; PLATELET DERIVED GROWTH FACTOR A; TRANSCRIPTION FACTOR SOX11; CULTURE MEDIUM; PLATELET DERIVED GROWTH FACTOR; PLATELET-DERIVED GROWTH FACTOR A; SOX11 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FETUS; HUMAN; HUMAN CELL; IN VITRO STUDY; MANTLE CELL LYMPHOMA; MOUSE; NONHUMAN; TRANSCRIPTION REGULATION; TUMOR VASCULARIZATION; UPREGULATION; XENOGRAFT; ANIMAL; CANCER TRANSPLANTATION; CELL MOTION; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PROTEOMICS; SCID MOUSE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; ENDOTHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LYMPHOMA, MANTLE-CELL; MICE; MICE, SCID; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PLATELET-DERIVED GROWTH FACTOR; PROTEOMICS; SIGNAL TRANSDUCTION; SOXC TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84907708404     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-04-569566     Document Type: Article

References (50)

1. Swerdlow SH, Campo E, Harris NL, et al. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. Lyon, France: AIRC Press; 2008.
2. Jares P, Colomer D, Campo E. Molecular pathogenesis of mantle cell lymphoma. J Clin Invest. 2012;122(10):3416-3423.
3. Orchard J, Garand R, Davis Z, et al. A subset of t(11;14) lymphoma with mantle cell features displays mutated IgVH genes and includes patients with good prognosis, nonnodal disease. Blood. 2003;101(12):4975-4981.
4. Fernàndez V, Salamero O, Espinet B, et al. Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res. 2010;70(4):1408-1418.
5. Espinet B, Ferrer A, Bellosillo B, et al. Distinction between asymptomatic monoclonal B-cell lymphocytosis with cyclin D1 overexpression and mantle cell lymphoma: from molecular profiling to flow cytometry. Clin Cancer Res. 2014;20(4): 1007-1019.
6. Royo C, Navarro A, Clot G, et al. Non-nodal type of mantle cell lymphoma is a specific biological and clinical subgroup of the disease. Leukemia. 2012;26(8):1895-1898.
7. Sock E, Rettig SD, Enderich J, Bösl MR, Tamm ER, Wegner M. Gene targeting reveals a widespread role for the high-mobility-group transcription factor Sox11 in tissue remodeling. Mol Cell Biol. 2004;24(15):6635-6644.
8. Haslinger A, Schwarz TJ, Covic M, Lie DC. Expression of Sox11 in adult neurogenic niches suggests a stage-specific role in adult neurogenesis. Eur J Neurosci. 2009;29(11): 2103-2114.
9. Mu L, Berti L, Masserdotti G, et al. SoxC transcription factors are required for neuronal differentiation in adult hippocampal neurogenesis. J Neurosci. 2012;32(9):3067-3080.
10. Lin L, Lee VM, Wang Y, et al. Sox11 regulates survival and axonal growth of embryonic sensory neurons. Dev Dyn. 2011;240(1):52-64.
11. Weigle B, Ebner R, Temme A, et al. Highly specific overexpression of the transcription factor SOX11 in human malignant gliomas. Oncol Rep. 2005;13(1):139-144.
12. de Bont JM, Kros JM, Passier MM, et al. Differential expression and prognostic significance of SOX genes in pediatric medulloblastoma and ependymoma identified by microarray analysis. Neuro-oncol. 2008;10(5): 648-660.
13. Dictor M, Ek S, Sundberg M, et al. Strong lymphoid nuclear expression of SOX11 transcription factor defines lymphoblastic neoplasms, mantle cell lymphoma and Burkitt's lymphoma. Haematologica. 2009;94(11): 1563-1568.
14. Mozos A, Royo C, Hartmann E, et al. SOX11 expression is highly specific for mantle cell lymphoma and identifies the cyclin D1-negative subtype. Haematologica. 2009;94(11):1555-1562.
15. Vegliante MC, Palomero J, Pérez-Galán P, et al. SOX11 regulates PAX5 expression and blocks terminal B-cell differentiation in aggressive mantle cell lymphoma. Blood. 2013;121(12):2175-2185.
16. Salaverria I, Perez-Galan P, Colomer D, Campo E. Mantle cell lymphoma: from pathology and molecular pathogenesis to new therapeutic perspectives. Haematologica. 2006;91(1):11-16.
17. Navarro A, Clot G, Royo C, et al. Molecular subsets of mantle cell lymphoma defined by the IGHV mutational status and SOX11 expression have distinct biologic and clinical features. Cancer Res. 2012;72(20):5307-5316.
18. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledgebased approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-15550.
19. Vegliante MC, Royo C, Palomero J, et al. Epigenetic activation of SOX11 in lymphoid neoplasms by histone modifications. PLoS ONE. 2011;6(6):e21382.
20. Roué G, Pérez-Galán P, Mozos A, et al. The Hsp90 inhibitor IPI-504 overcomes bortezomib resistance in mantle cell lymphoma in vitro and in vivo by down-regulation of the prosurvival ER chaperone BiP/Grp78. Blood. 2011;117(4): 1270-1279.
21. Cardesa-Salzmann TM, Colomo L, Gutierrez G, et al. High microvessel density determines a poor outcome in patients with diffuse large B-cell lymphoma treated with rituximab plus chemotherapy. Haematologica. 2011;96(7): 996-1001.
22. Kubota Y, Kleinman HK, Martin GR, Lawley TJ. Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol. 1988;107(4):1589-1598.
23. Piccaluga PP, Agostinelli C, Zinzani PL, Baccarani M, Dalla Favera R, Pileri SA. Expression of platelet-derived growth factor receptor alpha in peripheral T-cell lymphoma not otherwise specified. Lancet Oncol. 2005;6(6):440.
24. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J. Vascular-specific growth factors and blood vessel formation. Nature. 2000; 407(6801):242-248.
25. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011;144(5):646-674.
26. Baeriswyl V, Christofori G. The angiogenic switch in carcinogenesis. Semin Cancer Biol. 2009; 19(5):329-337.
27. Lenz G, Wright G, Dave SS, et al; Lymphoma/Leukemia Molecular Profiling Project. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med. 2008;359(22):2313-2323.
28. Perry AM, Cardesa-Salzmann TM, Meyer PN, et al. A new biologic prognostic model based on immunohistochemistry predicts survival in patients with diffuse large B-cell lymphoma. Blood. 2012;120(11):2290-2296.
29. Korkolopoulou P, Thymara I, Kavantzas N, et al. Angiogenesis in Hodgkin's lymphoma: a morphometric approach in 286 patients with prognostic implications. Leukemia. 2005;19(6): 894-900.
30. Lozano E, Segarra M, Garciá-Martínez A, Hernández-Rodríguez J, Cid MC. Imatinib mesylate inhibits in vitro and ex vivo biological responses related to vascular occlusion in giant cell arteritis. Ann Rheum Dis. 2008;67(11): 1581-1588.
31. Schmitt CE, Woolls MJ, Jin SW. Mutant-specific gene expression profiling identifies SRY-related HMG box 11b (SOX11b) as a novel regulator of vascular development in zebrafish. Mol Cells. 2013;35(2):166-172.
32. Risau W, Drexler H, Mironov V, et al. Plateletderived growth factor is angiogenic in vivo. Growth Factors. 1992;7(4):261-266.
33. Dong J, Grunstein J, Tejada M, et al. VEGF-null cells require PDGFR alpha signaling-mediated stromal fibroblast recruitment for tumorigenesis. EMBO J. 2004;23(14):2800-2810.
34. Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature. 2005;438(7070): 967-974.
35. Ding W, Knox TR, Tschumper RC, et al. Plateletderived growth factor (PDGF)-PDGF receptor interaction activates bone marrow-derived mesenchymal stromal cells derived from chronic lymphocytic leukemia: implications for an angiogenic switch. Blood. 2010;116(16): 2984-2993.
36. Heldin CH. Targeting the PDGF signaling pathway in tumor treatment. Cell Commun Signal. 2013;11:97.
37. Andrae J, Gallini R, Betsholtz C. Role of plateletderived growth factors in physiology and medicine. Genes Dev. 2008;22(10):1276-1312.
38. Gerber DE, Gupta P, Dellinger MT, et al. Stromal platelet-derived growth factor receptor a (PDGFRa) provides a therapeutic target independent of tumor cell PDGFRa expression in lung cancer xenografts. Mol Cancer Ther. 2012; 11(11):2473-2482.
39. Zhu K, Pan Q, Zhang X, et al. MiR-146a enhances angiogenic activity of endothelial cells in hepatocellular carcinoma by promoting PDGFRA expression. Carcinogenesis. 2013;34(9): 2071-2079.
40. Goldman JM, Melo JV. Chronic myeloid leukemia-advances in biology and new approaches to treatment. N Engl J Med. 2003; 349(15):1451-1464.
41. Milojkovic D, Apperley J. Mechanisms of resistance to imatinib and second-generation tyrosine inhibitors in chronic myeloid leukemia. Clin Cancer Res. 2009;15(24):7519-7527.
42. Tauchi T, Ohyashiki K. Molecular mechanisms of resistance of leukemia to imatinib mesylate. Leuk Res. 2004;28(suppl 1):S39-S45.
43. Ruan J, Hajjar K, Rafii S, Leonard JP. Angiogenesis and antiangiogenic therapy in non- Hodgkin's lymphoma. Ann Oncol. 2009;20(3): 413-424.
44. Ruan J, Luo M, Wang C, et al. Imatinib disrupts lymphoma angiogenesis by targeting vascular pericytes. Blood. 2013;121(26):5192-5202.
45. Song K, Herzog BH, Sheng M, et al. Lenalidomide inhibits lymphangiogenesis in preclinical models of mantle cell lymphoma [published correction appears in Cancer Res. 2014;74(4):1284]. Cancer Res. 2013;73(24):7254-7264.
46. Garzia M, Sora F, Teofili L, et al. Blastoid mantle cell lymphoma occurring in a patient in complete remission of chronic myelogenous leukemia. Lab Hematol. 2007;13(1):30-33.
47. Rodler E, Welborn J, Hatcher S, et al. Blastic mantle cell lymphoma developing concurrently in a patient with chronic myelogenous leukemia and a review of the literature. Am J Hematol. 2004; 75(4):231-238.
48. Zhang J, Lu A, Li L, Yue J, Lu Y. p16 Modulates VEGF expression via its interaction with HIF-1alpha in breast cancer cells. Cancer Invest. 2010;28(6): 588-597.
49. Ousset M, Bouquet F, Fallone F, et al. Loss of ATM positively regulates the expression of hypoxia inducible factor 1 (HIF-1) through oxidative stress: Role in the physiopathology of the disease. Cell Cycle. 2010;9(14): 2814-2822.
50. Grossfeld GD, Ginsberg DA, Stein JP, et al. Thrombospondin-1 expression in bladder cancer: association with p53 alterations, tumor angiogenesis, and tumor progression. J Natl Cancer Inst. 1997;89(3):219-227.