CD47 blockade triggers T cell-mediated destruction of immunogenic tumors

Nature Medicine

Volumn 21, Issue 10, 2015, Pages 1209-1215

  Liu, Xiaojuan ^a,b   Pu, Yang ^a   Cron, Kyle ^a   Deng, Liufu ^a   Kline, Justin ^a   Frazier, William A ^c   Xu, Hairong ^a   Peng, Hua ^a   Fu, Yang Xin ^a   Xu, Meng Michelle ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; CD47 ANTIGEN; DNA; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; ANTINEOPLASTIC AGENT; CD47 PROTEIN, HUMAN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROSS PRESENTATION; CYTOSOL; DENDRITIC CELL; FEMALE; IMMUNOCOMPETENCE; IMMUNOTHERAPY; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; THERAPY EFFECT; TUMOR CELL DESTRUCTION; TUMOR IMMUNITY; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; DRUG SCREENING; HUMAN; IMMUNOLOGY; NEOPLASMS; PHYSIOLOGY;

ANIMALS; ANTIGENS, CD47; ANTINEOPLASTIC AGENTS; DNA; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; NEOPLASMS; T-LYMPHOCYTES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84943630992     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3931     Document Type: Article

References (50)

1. Gardai, S. J. et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334 (2005).
2. Chao, M. P. et al. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci. Transl. Med. 2, 63ra94 (2010).
3. Chao, M. P. , Majeti, R. & Weissman, I. L. Programmed cell removal: a new obstacle in the road to developing cancer. Nat. Rev. Cancer 12, 58-67 (2012).
4. Oldenborg, P. A. et al. Role of CD47 as a marker of self on red blood cells. Science 288, 2051-2054 (2000).
5. Blazar, B. R. et al. CD47 (integrin-associated protein) engagement of dendritic cell and macrophage counterreceptors is required to prevent the clearance of donor lymphohematopoietic cells. J. Exp. Med. 194, 541-549 (2001).
6. Barclay, A. N. & Van den Berg, T. K. The interaction between signal regulatory protein alpha (SIRPα) and CD47: structure, function, and therapeutic target. Annu. Rev. Immunol. 32, 25-50 (2014).
7. Yamao, T. et al. Negative regulation of platelet clearance and of the macrophage phagocytic response by the transmembrane glycoprotein SHPS-1. J. Biol. Chem. 277, 39833-39839 (2002).
8. Olsson, M. , Bruhns, P. , Frazier, W. A. , Ravetch, J. V. & Oldenborg, P. A. Platelet homeostasis is regulated by platelet expression of CD47 under normal conditions and in passive immune thrombocytopenia. Blood 105, 3577-3582 (2005).
9. Tsai, R. K. & Discher, D. E. Inhibition of "self" engulfment through deactivation of myosin-II at the phagocytic synapse between human cells. J. Cell Biol. 180, 989-1003 (2008).
10. Poels, L. G. et al. Monoclonal antibody against human ovarian tumor-associated antigens. J. Natl. Cancer Inst. 76, 781-791 (1986).
11. Jaiswal, S. et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138, 271-285 (2009).
12. Majeti, R. et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138, 286-299 (2009).
13. Rendtlew Danielsen, J. M. , Knudsen, L. M. , Dahl, I. M. , Lodahl, M. & Rasmussen, T. Dysregulation of CD47 and the ligands thrombospondin 1 and 2 in multiple myeloma. Br. J. Haematol. 138, 756-760 (2007).
14. Chan, K. S. et al. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc. Natl. Acad. Sci. USA 106, 14016-14021 (2009).
15. Chan, K. S. , Volkmer, J. P. & Weissman, I. Cancer stem cells in bladder cancer: a revisited and evolving concept. Curr. Opin. Urol. 20, 393-397 (2010).
16. Chao, M. P. et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell 142, 699-713 (2010).
17. Willingham, S. B. et al. The CD47-signal regulatory protein α (SIRPa) interaction is a therapeutic target for human solid tumors. Proc. Natl. Acad. Sci. USA 109, 6662-6667 (2012).
18. Chao, M. P. et al. Therapeutic antibody targeting of CD47 eliminates human acute lymphoblastic leukemia. Cancer Res. 71, 1374-1384 (2011).
19. Chao, M. P. et al. Extranodal dissemination of non-Hodgkin lymphoma requires CD47 and is inhibited by anti-CD47 antibody therapy. Blood 118, 4890-4901 (2011).
20. Soto-Pantoja, D. R. et al. CD47 in the tumor microenvironment limits cooperation between antitumor T-cell immunity and radiotherapy. Cancer Res. 74, 6771-6783 (2014).
21. Lee, Y. et al. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: changing strategies for cancer treatment. Blood 114, 589-595 (2009).
22. Brown, E. J. & Frazier, W. A. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 11, 130-135 (2001).
23. Weiskopf, K. et al. Engineered SIRPα variants as immunotherapeutic adjuvants to anticancer antibodies. Science 341, 88-91 (2013).
24. Tseng, D. et al. Anti-CD47 antibody-mediated phagocytosis of cancer by macrophages primes an effective antitumor T-cell response. Proc. Natl. Acad. Sci. USA 110, 11103-11108 (2013).
25. Burnette, B. C. et al. The efficacy of radiotherapy relies upon induction of type I interferon-dependent innate and adaptive immunity. Cancer Res. 71, 2488-2496 (2011).
26. Diamond, M. S. et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J. Exp. Med. 208, 1989-2003 (2011).
27. Fuertes, M. B. et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8α+ dendritic cells. J. Exp. Med. 208, 2005-2016 (2011).
28. Stagg, J. et al. Anti-ErbB-2 mAb therapy requires type I and II interferons and synergizes with anti-PD-1 or anti-CD137 mAb therapy. Proc. Natl. Acad. Sci. USA 108, 7142-7147 (2011).
29. Yang, X. et al. Targeting the tumor microenvironment with interferon-β bridges innate and adaptive immune responses. Cancer Cell 25, 37-48 (2014).
30. Chen, G. Y. & Nunez, G. Sterile inflammation: sensing and reacting to damage. Nat. Rev. Immunol. 10, 826-837 (2010).
31. Desmet, C. J. & Ishii, K. J. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat. Rev. Immunol. 12, 479-491 (2012).
32. Kono, H. & Rock, K. L. How dying cells alert the immune system to danger. Nat. Rev. Immunol. 8, 279-289 (2008).
33. ONeill, L. A. , Golenbock, D. & Bowie, A. G. The history of Toll-like receptors-redefining innate immunity. Nat. Rev. Immunol. 13, 453-460 (2013).
34. Ishikawa, H. & Barber, G. N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678 (2008).
35. Ishikawa, H. , Ma, Z. & Barber, G. N. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792 (2009).
36. Li, X. D. et al. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341, 1390-1394 (2013).
37. Sun, L. , Wu, J. , Du, F. , Chen, X. & Chen, Z. J. Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791 (2013).
38. Wu, J. et al. Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826-830 (2013).
39. Woo, S. R. et al. STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors. Immunity 41, 830-842 (2014).
40. Deng, L. et al. STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors. Immunity 41, 843-852 (2014).
41. Obeid, M. et al. Ecto-calreticulin in immunogenic chemotherapy. Immunol. Rev. 220, 22-34 (2007).
42. Obeid, M. et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54-61 (2007).
43. Takenaka, K. et al. Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat. Immunol. 8, 1313-1323 (2007).
44. Yamauchi, T. et al. Polymorphic Sirpa is the genetic determinant for NOD-based mouse lines to achieve efficient human cell engraftment. Blood 121, 1316-1325 (2013).
45. Matsushita, H. et al. Cancer exome analysis reveals a T-cell-dependent mechanism of cancer immunoediting. Nature 482, 400-404 (2012).
46. Snyder, A. et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371, 2189-2199 (2014).
47. Ma, Y. et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 38, 729-741 (2013).
48. Ma, Y. et al. CCL2/CCR2-dependent recruitment of functional antigen-presenting cells into tumors upon chemotherapy. Cancer Res. 74, 436-445 (2014).
49. Rovero, S. et al. DNA vaccination against rat her-2/Neu p185 more effectively inhibits carcinogenesis than transplantable carcinomas in transgenic BALB/c mice. J. Immunol. 165, 5133-5142 (2000).
50. Oldenborg, P. A. , Gresham, H. D. & Lindberg, F. P. CD47-signal regulatory protein α (SIRPα) regulates Fcγ and complement receptor-mediated phagocytosis. J. Exp. Med. 193, 855-862 (2001).