CD47 signaling regulates the immunosuppressive activity of VEGF in T cells

Journal of Immunology

Volumn 193, Issue 8, 2014, Pages 3914-3924

  Kaur, Sukhbir ^a   Chang, Tiffany ^a   Singh, Satya P ^b   Lim, Langston ^a   Mannan, Poonam ^a   Garfield, Susan H ^a   Pendrak, Michael L ^a   Soto Pantoja, David R ^a   Rosenberg, Avi Z ^a   Jin, Shelly ^a   Roberts, David D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD47 ANTIGEN; T LYMPHOCYTE RECEPTOR; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; CD47 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN TYROSINE KINASE; THROMBOSPONDIN 1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOREGULATION; JURKAT CELL LINE; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION; ANIMAL; BIOSYNTHESIS; CD8+ T LYMPHOCYTE; CELL COMMUNICATION; CELL PROLIFERATION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHOSPHORYLATION; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD47; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; IMMUNE TOLERANCE; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; THROMBOSPONDIN 1; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84907483724     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303116     Document Type: Article

References (48)

1. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, et al. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380: 435-439.
2. Dvorak, H. F. 2002. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20: 4368-4380.
3. Ptaszynska, M. M., M. L. Pendrak, R. W. Bandle, M. L. Stracke, and D. D. Roberts. 2008. Positive feedback between vascular endothelial growth factor-A and autotaxin in ovarian cancer cells. Mol. Cancer Res. 6: 352-363.
4. Samuel, S., F. Fan, L. H. Dang, L. Xia, P. Gaur, and L. M. Ellis. 2011. Intracrine vascular endothelial growth factor signaling in survival and chemoresistance of human colorectal cancer cells. Oncogene 30: 1205-1212.
5. Cao, Y., Gu E, E. Wang, K. Pal, S. K. Dutta, D. Bar-Sagi, and D. Mukhopadhyay. 2012. VEGF exerts an angiogenesis-independent function in cancer cells to promote their malignant progression. Cancer Res. 72: 3912-3918.
6. Hamerlik, P., J. D. Lathia, R. Rasmussen, Q. Wu, J. Bartkova, M. Lee, P. Moudry, J. Bartek, Jr., W. Fischer, J. Lukas, et al. 2012. Autocrine VEGFVEGFR2-Neuropilin-1 signaling promotes glioma stem-like cell viability and tumor growth. J. Exp. Med. 209: 507-520.
7. Lee, J., T. Ku, H. Yu, K. Chong, S. W. Ryu, K. Choi, and C. Choi. 2012. Blockade of VEGF-A suppresses tumor growth via inhibition of autocrine signaling through FAK and AKT. Cancer Lett. 318: 221-225.
8. Lee, J., J. Lee, H. Yu, K. Choi, and C. Choi. 2011. Differential dependency of human cancer cells on vascular endothelial growth factor-mediated autocrine growth and survival. Cancer Lett. 309: 145-150.
9. Byrne, A. T., L. Ross, J. Holash, M. Nakanishi, L. Hu, J. I. Hofmann, G. D. Yancopoulos, and R. B. Jaffe. 2003. Vascular endothelial growth factortrap decreases tumor burden, inhibits ascites, and causes dramatic vascular remodeling in an ovarian cancer model. Clin. Cancer Res. 9: 5721-5728.
10. Casanovas, O. 2012. Cancer: Limitations of therapies exposed. Nature 484: 44-46.
11. Ferrara, N. 2005. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS 94: 209-231.
12. Bergers, G., and L. E. Benjamin. 2003. Tumorigenesis and the angiogenic switch. Nat. Rev. Cancer 3: 401-410.
13. Gabrilovich, D. I., H. L. Chen, K. R. Girgis, H. T. Cunningham, G. M. Meny, S. Nadaf, D. Kavanaugh, and D. P. Carbone. 1996. Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat. Med. 2: 1096-1103.
14. Oyama, T., S. Ran, T. Ishida, S. Nadaf, L. Kerr, D. P. Carbone, and D. I. Gabrilovich. 1998. Vascular endothelial growth factor affects dendritic cell maturation through the inhibition of nuclear factor-kappa B activation in hemopoietic progenitor cells. J. Immunol. 160: 1224-1232.
15. Gabrilovich, D., T. Ishida, T. Oyama, S. Ran, V. Kravtsov, S. Nadaf, and D. P. Carbone. 1998. Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood 92: 4150-4166.
16. Gabrilovich, D. I., T. Ishida, S. Nadaf, J. E. Ohm, and D. P. Carbone. 1999. Antibodies to vascular endothelial growth factor enhance the efficacy of cancer immunotherapy by improving endogenous dendritic cell function. Clin. Cancer Res. 5: 2963-2970.
17. Kusmartsev, S., and D. I. Gabrilovich. 2002. Immature myeloid cells and cancerassociated immune suppression. Cancer Immunol. Immunother. 51: 293-298.
18. Basu, A., A. Hoerning, D. Datta, M. Edelbauer, M. P. Stack, K. Calzadilla, S. Pal, and D. M. Briscoe. 2010. Cutting edge: Vascular endothelial growth factor-mediated signaling in human CD45RO+ CD4+ T cells promotes Akt and ERK activation and costimulates IFN-γamma production. J. Immunol. 184: 545-549.
19. Ziogas, A. C., N. G. Gavalas, M. Tsiatas, O. Tsitsilonis, E. Politi, E. Terpos, A. Rodolakis, G. Vlahos, N. Thomakos, D. Haidopoulos, et al. 2012. VEGF directly suppresses activation of T cells from ovarian cancer patients and healthy individuals via VEGF receptor Type 2. Int. J. Cancer 130: 857-864.
20. Mor, F., F. J. Quintana, and I. R. Cohen. 2004. Angiogenesis-inflammation crosstalk: vascular endothelial growth factor is secreted by activated T cells and induces Th1 polarization. J. Immunol. 172: 4618-4623.
21. Roberts, D. D., T.W. Miller, N. M. Rogers, M. Yao, and J. S. Isenberg. 2012. The matricellular protein thrombospondin-1 globally regulates cardiovascular function and responses to stress via CD47. Matrix Biol. 31: 162-169.
22. Isenberg, J. S., G. Martin-Manso, J. B. Maxhimer, and D. D. Roberts. 2009. Regulation of nitric oxide signalling by thrombospondin 1: implications for antiangiogenic therapies. Nat. Rev. Cancer 9: 182-194.
23. Kaur, S., G. Martin-Manso, M. L. Pendrak, S. H. Garfield, J. S. Isenberg, and D. D. Roberts. 2010. Thrombospondin-1 inhibits VEGF receptor-2 signaling by disrupting its association with CD47. J. Biol. Chem. 285: 38923-38932.
24. Vallejo, A. N., L. O. Mugge, P. A. Klimiuk, C. M. Weyand, and J. J. Goronzy. 2000. Central role of thrombospondin-1 in the activation and clonal expansion of inflammatory T cells. J. Immunol. 164: 2947-2954.
25. Reinhold, M. I., F. P. Lindberg, G. J. Kersh, P. M. Allen, and E. J. Brown. 1997. Costimulation of T cell activation by integrin-associated protein (CD47) is an adhesion-dependent, CD28-independent signaling pathway. J. Exp. Med. 185: 1-11.
26. Li, Z., L. He, K. Wilson, and D. Roberts. 2001. Thrombospondin-1 inhibits TCR-mediated T lymphocyte early activation. J. Immunol. 166: 2427-2436.
27. Li, Z., M. J. Calzada, J. M. Sipes, J. A. Cashel, H. C. Krutzsch, D. S. Annis, D. F. Mosher, and D. D. Roberts. 2002. Interactions of thrombospondins with alpha4beta1 integrin and CD47 differentially modulate T cell behavior. J. Cell Biol. 157: 509-519.
28. Kaur, S., S. A. Kuznetsova, M. L. Pendrak, J. M. Sipes, M. J. Romeo, Z. Li, L. Zhang, and D. D. Roberts. 2011. Heparan sulfate modification of the transmembrane receptor CD47 is necessary for inhibition of T cell receptor signaling by thrombospondin-1. J. Biol. Chem. 286: 14991-15002.
29. Miller, T. W., S. Kaur, K. Ivins-O'Keefe, and D. D. Roberts. 2013. Thrombospondin-1 is a CD47-dependent endogenous inhibitor of hydrogen sulfide signaling in T cell activation. Matrix Biol. 32: 316-324.
30. Lamy, L., A. Foussat, E. J. Brown, P. Bornstein, M. Ticchioni, and A. Bernard. 2007. Interactions between CD47 and thrombospondin reduce inflammation. J. Immunol. 178: 5930-5939.
31. Grimbert, P., S. Bouguermouh, N. Baba, T. Nakajima, Z. Allakhverdi, D. Braun, H. Saito, M. Rubio, G. Delespesse, and M. Sarfati. 2006. Thrombospondin/CD47 interaction: a pathway to generate regulatory T cells from human CD4+ CD25-T cells in response to inflammation. J. Immunol. 177: 3534-3541.
32. Manna, P. P., and W. A. Frazier. 2003. The mechanism of CD47-dependent killing of T cells: heterotrimeric Gi-dependent inhibition of protein kinase A. J. Immunol. 170: 3544-3553.
33. Barazi, H. O., Z. Li, J. A. Cashel, H. C. Krutzsch, D. S. Annis, D. F. Mosher, and D. D. Roberts. 2002. Regulation of integrin function by CD47 ligands. Differential effects on alpha vbeta 3 and alpha 4beta1 integrin-mediated adhesion. J. Biol. Chem. 277: 42859-42866.
34. Roberts, D. D., Cashel, J., and Guo, N. 1994. Purification of thrombospondin from human platelets. J. Tissue Cult. Methods 16: 217-222.
35. Maile, L. A., L. B. Allen, U. Veluvolu, B. E. Capps, W. H. Busby, M. Rowland, and D. R. Clemmons. 2009. Identification of compounds that inhibit IGF-I signaling in hyperglycemia. Exp. Diabetes Res. 2009: 267107.
36. Xu, D., M. M. Fuster, R. Lawrence, and J. D. Esko. 2011. Heparan sulfate regulates VEGF165-and VEGF121-mediated vascular hyperpermeability. J. Biol. Chem. 286: 737-745.
37. Sun, Z., X. Li, S. Massena, S. Kutschera, N. Padhan, L. Gualandi, V. Sundvold-Gjerstad, K. Gustafsson, W. W. Choy, G. Zang, et al. 2012. VEGFR2 induces c-Src signaling and vascular permeability in vivo via the adaptor protein TSAd. J. Exp. Med. 209: 1363-1377.
38. Gampel, A., L. Moss, M. C. Jones, V. Brunton, J. C. Norman, and H. Mellor. 2006. VEGF regulates the mobilization of VEGFR2/KDR from an intracellular endothelial storage compartment. Blood 108: 2624-2631.
39. Kaur, S., D. R. Soto-Pantoja, E. V. Stein, C. Liu, A. G. Elkahloun, M. L. Pendrak, A. Nicolae, S. P. Singh, Z. Nie, D. Levens, et al. 2013. Thrombospondin-1 signaling through CD47 inhibits self-renewal by regulating c-Myc and other stem cell transcription factors. Sci. Rep. 3: 1673.
40. Kang, J., P. G. Rychahou, T. A. Ishola, J. M. Mourot, B. M. Evers, and D. H. Chung. 2008. N-myc is a novel regulator of PI3K-mediated VEGF expression in neuroblastoma. Oncogene 27: 3999-4007.
41. Hu, Y. H., S. Q. Kong, H. B. Kong, J. L. Wu, and Z. Chen. 2012. Targeting c-Myc on cell growth and vascular endothelial growth factor expression in IN500 glioblastoma cells. Chin. Med. J. (Engl.) 125: 2025-2031.
42. Lerner, C. G., M. R. Horton, R. H. Schwartz, and J. D. Powell. 2000. Distinct requirements for C-C chemokine and IL-2 production by naive, previously activated, and anergic T cells. J. Immunol. 164: 3996-4002.
43. Shin, J. Y., I. H. Yoon, J. S. Kim, B. Kim, and C. G. Park. 2009. Vascular endothelial growth factor-induced chemotaxis and IL-10 from T cells. Cell. Immunol. 256: 72-78.
44. Reinhold, M. I., J. M. Green, F. P. Lindberg, M. Ticchioni, and E. J. Brown. 1999. Cell spreading distinguishes the mechanism of augmentation of T cell activation by integrin-associated protein/CD47 and CD28. Int. Immunol. 11: 707-718.
45. Futagami, Y., S. Sugita, J. Vega, K. Ishida, H. Takase, K. Maruyama, H. Aburatani, and M. Mochizuki. 2007. Role of thrombospondin-1 in T cell response to ocular pigment epithelial cells. J. Immunol. 178: 6994-7005.
46. Li, S. S., Z. Liu, M. Uzunel, and K. G. Sundqvist. 2006. Endogenous thrombospondin-1 is a cell-surface ligand for regulation of integrin-dependent Tlymphocyte adhesion. Blood 108: 3112-3120.
47. Ticchioni, M., M. Deckert, F. Mary, G. Bernard, E. J. Brown, and A. Bernard. 1997. Integrin-associated protein (CD47) is a comitogenic molecule on CD3-activated human T cells. J. Immunol. 158: 677-684.
48. Isenberg, J. S., L. A. Ridnour, J. Dimitry, W. A. Frazier, D. A. Wink, and D. D. Roberts. 2006. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J. Biol. Chem. 281: 26069-26080.