Loss of cell surface CD47 clustering formation and binding avidity to SIRPα facilitate apoptotic cell clearance by macrophages

Journal of Immunology

Volumn 195, Issue 2, 2015, Pages 661-671

  Lv, Zhiyuan ^a,b   Bian, Zhen ^a,b   Shi, Lei ^a,b   Niu, Shuo ^b   Ha, Binh ^b   Tremblay, Alexandra ^b   Li, Liangwei ^b   Zhang, Xiugen ^b   Paluszynski, John ^b   Liu, Ming ^b,c   Zen, Ke ^a,b   Liu, Yuan ^b  

^a NANJING UNIVERSITY   (China)

^b GEORGIA STATE UNIVERSITY   (United States)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CD47 ANTIGEN; METHYL BETA CYCLODEXTRIN; PROTEIN SIRP ALPHA; UNCLASSIFIED DRUG; BETA CYCLODEXTRIN DERIVATIVE; CD47 PROTEIN, HUMAN; DIFFERENTIATION ANTIGEN; IMMUNOGLOBULIN RECEPTOR; METHYL-BETA-CYCLODEXTRIN; PROTEIN BINDING; SIRPA PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; LIPID RAFT; MACROPHAGE; MICROSCOPY; PHAGOCYTOSIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; ULTRAVIOLET RADIATION; ANIMAL; BINDING SITE; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MONONUCLEAR CELL; MOUSE; PRIMARY CELL CULTURE; PROTEIN TRANSPORT; RADIATION RESPONSE; SPLEEN; TUMOR CELL LINE;

ANIMALS; ANTIGENS, CD47; ANTIGENS, DIFFERENTIATION; APOPTOSIS; BETA-CYCLODEXTRINS; BINDING SITES; CELL LINE, TUMOR; EPITHELIAL CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; LEUKOCYTES, MONONUCLEAR; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; PHAGOCYTOSIS; PRIMARY CELL CULTURE; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SPLEEN; ULTRAVIOLET RAYS;

EID: 84936804591     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401719     Document Type: Article

References (50)

1. Matozaki, T., Y. Murata, H. Okazawa, and H. Ohnishi. 2009. Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol. 19: 72-80.
2. Barclay, A. N., and T. K. Van den Berg. 2014. The interaction between signal regulatory protein alpha (SIRPa) and CD47: structure, function, and therapeutic target. Annu. Rev. Immunol. 32: 25-50.
3. Oldenborg, P. A., A. Zheleznyak, Y. F. Fang, C. F. Lagenaur, H. D. Gresham, and F. P. Lindberg. 2000. Role of CD47 as a marker of self on red blood cells. Science 288: 2051-2054.
4. Ishikawa-Sekigami, T., Y. Kaneko, H. Okazawa, T. Tomizawa, J. Okajo, Y. Saito, C. Okuzawa, M. Sugawara-Yokoo, U. Nishiyama, H. Ohnishi, et al. 2006. SHPS-1 promotes the survival of circulating erythrocytes through inhibition of phagocytosis by splenic macrophages. Blood 107: 341-348.
5. Bruce, L. J., S. Ghosh, M. J. King, D. M. Layton, W. J. Mawby, G. W. Stewart, P. A. Oldenborg, J. Delaunay, and M. J. Tanner. 2002. Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex. Blood 100: 1878-1885.
6. Anniss, A. M., and R. L. Sparrow. 2002. Expression of CD47 (integrin-associated protein) decreases on red blood cells during storage. Transfus. Apher. Sci. 27: 233-238.
7. Chao, M. P., I. L. Weissman, and R. Majeti. 2012. The CD47-SIRPa pathway in cancer immune evasion and potential therapeutic implications. Curr. Opin. Immunol. 24: 225-232.
8. Lauber, K., E. Bohn, S. M. Kröber, Y. J. Xiao, S. G. Blumenthal, R. K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, S. Baksh, et al. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113: 717-730.
9. Martin, S. J., C. P. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182: 1545-1556.
10. Vandivier, R. W., C. A. Ogden, V. A. Fadok, P. R. Hoffmann, K. K. Brown, M. Botto, M. J. Walport, J. H. Fisher, P. M. Henson, and K. E. Greene. 2002. Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169: 3978-3986.
11. Ogden, C. A., A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194: 781-795.
12. Gardai, S. J., K. A. McPhillips, S. C. Frasch, W. J. Janssen, A. Starefeldt, J. E. Murphy-Ullrich, D. L. Bratton, P. A. Oldenborg, M. Michalak, and P. M. Henson. 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334.
13. Burger, P., P. Hilarius-Stokman, D. de Korte, T. K. van den Berg, and R. van Bruggen. 2012. CD47 functions as a molecular switch for erythrocyte phagocytosis. Blood 119: 5512-5521.
14. Khandelwal, S., N. van Rooijen, and R. K. Saxena. 2007. Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 47: 1725-1732.
15. Ades, E. W., F. J. Candal, R. A. Swerlick, V. G. George, S. Summers, D. C. Bosse, and T. J. Lawley. 1992. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J. Invest. Dermatol. 99: 683-690.
16. Ha, B., Z. Lv, Z. Bian, X. Zhang, A. Mishra, and Y. Liu. 2013. 'Clustering' SIRPa into the plasma membrane lipid microdomains is required for activated monocytes and macrophages to mediate effective cell surface interactions with CD47. PLoS ONE 8: e77615.
17. Liu, Y., H. J. Bühring, K. Zen, S. L. Burst, F. J. Schnell, I. R. Williams, and C. A. Parkos. 2002. Signal regulatory protein (SIRPalpha), a cellular ligand for CD47, regulates neutrophil transmigration. J. Biol. Chem. 277: 10028-10036.
18. Liu, Y., D. Merlin, S. L. Burst, M. Pochet, J. L. Madara, and C. A. Parkos. 2001. The role of CD47 in neutrophil transmigration. Increased rate of migration correlates with increased cell surface expression of CD47. J. Biol. Chem. 276: 40156-40166.
19. Zen, K., Y. Guo, Z. Bian, Z. Lv, D. Zhu, H. Ohnishi, T. Matozaki, and Y. Liu. 2013. Inflammation-induced proteolytic processing of the SIRPa cytoplasmic ITIM in neutrophils propagates a proinflammatory state. Nat. Commun. 4: 2436.
20. Liu, Y., A. Nusrat, F. J. Schnell, T. A. Reaves, S. Walsh, M. Pochet, and C. A. Parkos. 2000. Human junction adhesion molecule regulates tight junction resealing in epithelia. J. Cell Sci. 113: 2363-2374.
21. Liu, Y., Q. Tong, Y. Zhou, H. W. Lee, J. J. Yang, H. J. Bühring, Y. T. Chen, B. Ha, C. X. Chen, Y. Yang, and K. Zen. 2007. Functional elements on SIR-Palpha IgV domain mediate cell surface binding to CD47. J. Mol. Biol. 365: 680-693.
22. Liu, Y., M. B. O'Connor, K. J. Mandell, K. Zen, A. Ullrich, H. J. Bühring, and C. A. Parkos. 2004. Peptide-mediated inhibition of neutrophil transmigration by blocking CD47 interactions with signal regulatory protein alpha. J. Immunol. 172: 2578-2585.
23. Zen, K., Y. Liu, D. Cairo, and C. A. Parkos. 2002. CD11b/CD18-dependent interactions of neutrophils with intestinal epithelium are mediated by fucosy-lated proteoglycans. J. Immunol. 169: 5270-5278.
24. Bian, Z., Y. Guo, B. Ha, K. Zen, and Y. Liu. 2012. Regulation of the inflammatory response: enhancing neutrophil infiltration under chronic inflammatory conditions. J. Immunol. 188: 844-853.
25. Bian, Z., Y. Guo, Y. Luo, A. Tremblay, X. Zhang, S. Dharma, A. Mishra, and Y. Liu. 2013. CD47 deficiency does not impede polymorphonuclear neutrophil transmigration but attenuates granulopoiesis at the postacute stage of colitis. J. Immunol. 190: 411-417.
26. Shogomori, H., and A. H. Futerman. 2001. Cholera toxin is found in detergent-insoluble rafts/domains at the cell surface of hippocampal neurons but is internalized via a raft-independent mechanism. J. Biol. Chem. 276: 9182-9188.
27. Marmor, M. D., and M. Julius. 2001. Role for lipid rafts in regulating interleukin-2 receptor signaling. Blood 98: 1489-1497.
28. Di Palma, T., M. G. Filippone, G. M. Pierantoni, A. Fusco, S. Soddu, and M. Zannini. 2013. Pax8 has a critical role in epithelial cell survival and proliferation. Cell Death Dis. 4: e729.
29. Vanden Berghe, T., S. Grootjans, V. Goossens, Y. Dondelinger, D. V. Krysko, N. Takahashi, and P. Vandenabeele. 2013. Determination of apoptotic and ne-crotic cell death in vitro and in vivo. Methods 61: 117-129.
30. Krysko, D. V., T. Vanden Berghe, K. D'Herde, and P. Vandenabeele. 2008. Apoptosis and necrosis: detection, discrimination and phagocytosis. Methods 44: 205-221.
31. Huerta, S., E. J. Goulet, S. Huerta-Yepez, and E. H. Livingston. 2007. Screening and detection of apoptosis. J. Surg. Res. 139: 143-156.
32. Dogterom, M., and G. Koenderink. 2011. Cell-membrane mechanics: Vesicles in and tubes out. Nat. Mater. 10: 561-562.
33. Norman, L. L., J. Brugués, K. Sengupta, P. Sens, and H. Aranda-Espinoza. 2010. Cell blebbing and membrane area homeostasis in spreading and retracting cells. Biophys. J. 99: 1726-1733.
34. Charras, G. T., J. C. Yarrow, M. A. Horton, L. Mahadevan, and T. J. Mitchison. 2005. Non-equilibration of hydrostatic pressure in blebbing cells. Nature 435: 365-369.
35. Barros, L. F., T. Kanaseki, R. Sabirov, S. Morishima, J. Castro, C. X. Bittner, E. Maeno, Y. Ando-Akatsuka, and Y. Okada. 2003. Apoptotic and necrotic blebs in epithelial cells display similar neck diameters but different kinase dependency. Cell Death Differ. 10: 687-697.
36. Katkere, B., S. Rosa, A. Caballero, E. A. Repasky, and J. R. Drake. 2010. Physiological-range temperature changes modulate cognate antigen processing and presentation mediated by lipid raft-restricted ubiquitinated B cell receptor molecules. J. Immunol. 185: 5032-5039.
37. Otáhal, P., P. Angelisová, M. Hrdinka, T. Brdicka, P. Novák, K. Drbal, and V. Horejsí. 2010. A new type of membrane raft-like microdomains and their possible involvement in TCR signaling. J. Immunol. 184: 3689-3696.
38. Serezani, C. H., D. M. Aronoff, R. G. Sitrin, and M. Peters-Golden. 2009. FcgammaRI ligation leads to a complex with BLT1 in lipid rafts that enhances rat lung macrophage antimicrobial functions. Blood 114: 3316-3324.
39. Ikeda, H., H. Okazawa, H. Ohnishi, Y. Murata, P. A. Oldenborg, and T. Matozaki. 2006. Mutational analysis of the mechanism of negative regulation by SRC homology 2 domain-containing protein tyrosine phosphatase substrate-1 of phagocytosis in macrophages. J. Immunol. 177: 3123-3132.
40. Takizawa, H., and M. G. Manz. 2007. Macrophage tolerance: CD47-SIRP-alpha-mediated signals matter. Nat. Immunol. 8: 1287-1289.
41. Ide, K., H. Wang, H. Tahara, J. Liu, X. Wang, T. Asahara, M. Sykes, Y. G. Yang, and H. Ohdan. 2007. Role for CD47-SIRPalpha signaling in xenograft rejection by macrophages. Proc. Natl. Acad. Sci. USA 104: 5062-5066.
42. Mamtani, M., M. Sharma, M. Amin, A. Amin, A. Jawahirani, and H. Kulkarni. 2007. Erythrophagocytosis in sickle cell anemia: statistical evidence for a biological phenomenon. Med. Hypotheses 68: 1065-1070.
43. Willingham, S. B., J. P. Volkmer, A. J. Gentles, D. Sahoo, P. Dalerba, S. S. Mitra, J. Wang, H. Contreras-Trujillo, R. Martin, J. D. Cohen, et al. 2012. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc. Natl. Acad. Sci. USA 109: 6662-6667.
44. Jaiswal, S., C. H. Jamieson, W. W. Pang, C. Y. Park, M. P. Chao, R. Majeti, D. Traver, N. van Rooijen, and I. L. Weissman. 2009. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138: 271-285.
45. Mills, J. C., N. L. Stone, and R. N. Pittman. 1999. Extranuclear apoptosis. The role of the cytoplasm in the execution phase. J. Cell Biol. 146: 703-708.
46. Porter, K., D. Prescott, and J. Frye. 1973. Changes in surface morphology of Chinese hamster ovary cells during the cell cycle. J. Cell Biol. 57: 815-836.
47. Trinkaus, J. P. 1980. Formation of protrusions of the cell surface during tissue cell movement. Prog. Clin. Biol. Res. 41: 887-906.
48. Fackler, O. T., and R. Grosse. 2008. Cell motility through plasma membrane blebbing. J. Cell Biol. 181: 879-884.
49. McDonald, J. F., A. Zheleznyak, and W. A. Frazier. 2004. Cholesterol-independent interactions with CD47 enhance alphavbeta3 avidity. J. Biol. Chem. 279: 17301-17311.
50. Green, J. M., A. Zhelesnyak, J. Chung, F. P. Lindberg, M. Sarfati, W. A. Frazier, and E. J. Brown. 1999. Role of cholesterol in formation and function of a signaling complex involving alphavbeta3, integrin-associated protein (CD47), and heterotrimeric G proteins. J. Cell Biol. 146: 673-682.