Imatinib disrupts lymphoma angiogenesis by targeting vascular pericytes

Blood

Volumn 121, Issue 6, 2013, Pages 5192-5202

  Ruan, Jia ^a   Luo, Min ^b   Wang, Chunjie ^a   Fan, Lei ^a   Yang, Shao Ning ^a   Cardenas, Mariano ^a   Geng, Huimin ^a   Leonard, John P ^a   Melnick, Ari ^a   Cerchietti, Leandro ^a   Hajjar, Katherine A ^b  

^a Division of Hematology Oncology   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMATINIB; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; SMALL INTERFERING RNA; ANGIOGENESIS INHIBITOR; BENZAMIDE DERIVATIVE; MESSENGER RNA; MONOCLONAL ANTIBODY; PIPERAZINE DERIVATIVE; PLATELET DERIVED GROWTH FACTOR; PYRIMIDINE DERIVATIVE; TUMOR MARKER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DENSITY; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DIFFUSE LARGE B-CELL LYMPHOMA CELL LINE; DRUG MEGADOSE; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LYMPHOMA; LYMPHOMA CELL; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN DEPLETION; RAT; RECEPTOR DOWN REGULATION; TUMOR VOLUME; TUMOR XENOGRAFT; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CELL DIFFERENTIATION; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME IMMUNOASSAY; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; LARGE CELL LYMPHOMA; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL; APOPTOSIS; BENZAMIDES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHOMA, LARGE B-CELL, DIFFUSE; LYMPHOMA, T-CELL; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PERICYTES; PIPERAZINES; PLATELET-DERIVED GROWTH FACTOR; PYRIMIDINES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 84884170348     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-03-490763     Document Type: Article

References (46)

1. Lenz G, Staudt LM. Aggressive lymphomas. N Engl J Med. 2010;362(15):1417-1429.
2. Fisher RI. Overview of non-Hodgkin's lymphoma: biology, staging, and treatment. Semin Oncol. 2003;30(2 Suppl 4):3-9.
3. Coiffier B. State-of-the-art therapeutics: diffuse large B-cell lymphoma. J Clin Oncol. 2005;23(26): 6387-6393.
4. Herrmann A, Hoster E, Zwingers T, et al. Improvement of overall survival in advanced stage mantle cell lymphoma. J Clin Oncol. 2009;27(4): 511-518.
5. Dunleavy K, Pittaluga S, Czuczman MS, et al. Differential efficacy of bortezomib plus chemotherapy within molecular subtypes of diffuse large B-cell lymphoma. Blood. 2009; 113(24):6069-6076.
6. Ci W, Polo JM, Melnick A. B-cell lymphoma 6 and the molecular pathogenesis of diffuse large B-cell lymphoma. Curr Opin Hematol. 2008;15(4): 381-390.
7. Dave SS, Wright G, Tan B, et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med. 2004;351(21):2159-2169.
8. 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.
9. Paget S. The distribution of secondary growths in cancer of the breast. Lancet. 1889;1:571-573.
10. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21): 1182-1186.
11. Folkman J, Watson K, Ingber D, Hanahan D. Induction of angiogenesis during the transition from hyperplasia to neoplasia. Nature. 1989; 339(6219):58-61.
12. Ruan J, Hajjar K, Rafii S, Leonard JP. Angiogenesis and antiangiogenic therapy in non-Hodgkin's lymphoma. Ann Oncol. 2009;20(3): 413-424.
13. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med. 2003;9(6): 669-676.
14. Stopeck AT, Unger JM, Rimsza LM, et al. A phase II trial of single agent bevacizumab in patients with relapsed, aggressive non-Hodgkin lymphoma: Southwest oncology group study S0108. Leuk Lymphoma. 2009;50(5):728-735.
15. Ganjoo KN, An CS, Robertson MJ, et al. Rituximab, bevacizumab and CHOP (RA-CHOP) in untreated diffuse large B-cell lymphoma: safety, biomarker and pharmacokinetic analysis. Leuk Lymphoma. 2006;47(6):998-1005.
16. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer. 2003;3(6): 401-410.
17. 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.
18. Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997; 277(5323):242-245.
19. Soriano P. Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes Dev. 1994;8(16):1888-1896.
20. Enge M, Bjarnegård M, Gerhardt H, et al. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J. 2002;21(16):4307-4316.
21. Nissen LJ, Cao R, Hedlund EM, et al. Angiogenic factors FGF2 and PDGF-BB synergistically promote murine tumor neovascularization and metastasis. J Clin Invest. 2007;117(10): 2766-2777.
22. Pietras K, Pahler J, Bergers G, Hanahan D. Functions of paracrine PDGF signaling in the proangiogenic tumor stroma revealed by pharmacological targeting. PLoS Med. 2008;5(1): e19.
23. Shaheen RM, Tseng WW, Davis DW, et al. Tyrosine kinase inhibition of multiple angiogenic growth factor receptors improves survival in mice bearing colon cancer liver metastases by inhibition of endothelial cell survival mechanisms. Cancer Res. 2001;61(4):1464-1468.
24. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest. 2003;111(9): 1287-1295.
25. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G. PDGFRbeta1 perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol. 2005;7(9): 870-879.
26. Kitadai Y, Sasaki T, Kuwai T, Nakamura T, Bucana CD, Fidler IJ. Targeting the expression of platelet-derived growth factor receptor by reactive stroma inhibits growth and metastasis of human colon carcinoma. Am J Pathol. 2006;169(6): 2054-2065.
27. Shen J, Vil MD, Prewett M, et al. Development of a fully human anti-PDGFRbeta antibody that suppresses growth of human tumor xenografts and enhances antitumor activity of an anti-VEGFR2 antibody. Neoplasia. 2009;11(6): 594-604.
28. Ruan J, Hyjek E, Kermani P, et al. Magnitude of stromal hemangiogenesis correlates with histologic subtype of non-Hodgkin's lymphoma. Clin Cancer Res. 2006;12(19):5622-5631.
29. Cerchietti LC, Ghetu AF, Zhu X, et al. A small-molecule inhibitor of BCL6 kills DLBCL cells in vitro and in vivo. Cancer Cell. 2010;17(4): 400-411.
30. Druker BJ, Talpaz M, Resta DJ, et al. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N Engl J Med. 2001;344(14):1031-1037.
31. Buchdunger E, Matter A, Druker BJ. Bcr-Abl inhibition as a modality of CML therapeutics. Biochim Biophys Acta. 2001;1551(1):M11-M18.
32. Wolff NC, Randle DE, Egorin MJ, Minna JD, Ilaria RL Jr. Imatinib mesylate efficiently achieves therapeutic intratumor concentrations in vivo but has limited activity in a xenograft model of small cell lung cancer. Clin Cancer Res. 2004;10(10): 3528-3534.
33. Bertolini F, Shaked Y, Mancuso P, Kerbel RS. The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer. 2006;6(11):835-845.
34. Bertolini F, Paul S, Mancuso P, Monestiroli S, Gobbi A, Shaked Y, Kerbel RS. Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res. 2003;63(15): 4342-4346.
35. Shaked Y, Bertolini F, Man S, et al. Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; Implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell. 2005;7(1):101-111.
36. Capdeville R, Buchdunger E, Zimmermann J, Matter A. Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat Rev Drug Discov. 2002;1(7):493-502.
37. Walshe TE, Saint-Geniez M, Maharaj ASR, Sekiyama E, Maldonado AE, D'Amore PA. TGF-β is required for vascular barrier function, endothelial survival and homeostasis of the adult microvasculature. PLoS ONE. 2009;4(4):e5149.
38. Rao RS, Miano JM, Olson EN, Seidel CL. The A10 cell line: a model for neonatal, neointimal, or differentiated vascular smooth muscle cells? Cardiovasc Res. 1997;36(1):118-126.
39. Lijnen HR. Plasmin and matrix metalloproteinases in vascular remodeling. Thromb Haemost. 2001; 86(1):324-333.
40. Shapiro SD. Diverse roles of macrophage matrix metalloproteinases in tissue destruction and tumor growth. Thromb Haemost. 1999;82(2): 846-849.
41. Sennino B, Falcón BL, McCauley D, et al. Sequential loss of tumor vessel pericytes and endothelial cells after inhibition of platelet-derived growth factor B by selective aptamer AX102. Cancer Res. 2007;67(15): 7358-7367.
42. Dewar AL, Cambareri AC, Zannettino ACW, Miller BL, Doherty KV, Hughes TP, Lyons AB. Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood. 2005; 105(8):3127-3132.
43. Tejada ML, Yu L, Dong J, et al. Tumor-driven paracrine platelet-derived growth factor receptor a signaling is a key determinant of stromal cell recruitment in a model of human lung carcinoma. Clin Cancer Res. 2006;12(9):2676-2688.
44. Sennino B, Kuhnert F, Tabruyn SP, Mancuso MR, Hu-Lowe DD, Kuo CJ, McDonald DM. Cellular source and amount of vascular endothelial growth factor and platelet-derived growth factor in tumors determine response to angiogenesis inhibitors. Cancer Res. 2009;69(10):4527-4536.
45. Xian X, Håkansson J, Ståhlberg A, Lindblom P, Betsholtz C, Gerhardt H, Semb H. Pericytes limit tumor cell metastasis. J Clin Invest. 2006;116(3): 642-651.
46. Yonenaga Y, Mori A, Onodera H, et al. Absence of smooth muscle actin-positive pericyte coverage of tumor vessels correlates with hematogenous metastasis and prognosis of colorectal cancer patients. Oncology. 2005;69(2):159-166.