Evidence for phagocytosis of influenza virus-infected, apoptotic cells by neutrophils and macrophages in mice

Journal of Immunology

Volumn 178, Issue 4, 2007, Pages 2448-2457

  Hashimoto, Yumi ^a   Moki, Takeshi ^a   Takizawa, Takenori ^b   Shiratsuchi, Akiko ^a   Nakanishi, Yoshinobu ^a  

^a KANAZAWA UNIVERSITY   (Japan)

^b TOYAMA INSTITUTE OF HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

TOLL LIKE RECEPTOR 4;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; C57BL MOUSE; CONTROLLED STUDY; FEMALE; HISTOCHEMISTRY; HOST RESISTANCE; IN VIVO STUDY; INFLUENZA; INFLUENZA VIRUS A; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REGULATORY MECHANISM; VIRUS INHIBITION; VIRUS LOAD;

EID: 33846931100     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.4.2448     Document Type: Article

References (43)

1. Lipatov, A. S., E. A. Govorkova, R. J. Webby, H. Ozaki, M. Peiris, Y. Guan, L. Poon, and R. G. Webster. 2004. Influenza: emergence and control. J. Virol. 78: 8951-8959.
2. Janeway, C. A., Jr. 2001. How the immune system works to protect the host from infection: a personal view. Proc. Natl. Acad. Sci. USA 98: 7461-7468.
3. Hoebe, K., E. Janssen, and B. Beutler, 2004. The interface between innate and adaptive immunity. Nat. Immunol. 5: 971-974.
4. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
5. Underhill, D. M., and A. Ozinsky. 2002. Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 20: 825-852.
6. Stuart, L. M., and R. A. B. Ezekowitz. 2005. Phagocytosis: elegant complexity. Immunity 22: 539-550.
7. Aderem, A., and D. M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17: 593-623.
8. Barber, G. N. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8: 113-126.
9. Ren, Y., and J. Savill. 1998. Apoptosis: the importance of being eaten. Cell Death Differ. 5: 563-568.
10. Teodoro, J. G., and P. E. Branton. 1997. Regulation of apoptosis by viral gene products. J. Virol. 71: 1739-1746.
11. Granville, D. J., C. M. Carthy, D. Yang, D. W. C. Hunt, and B. M. McManus. 1998. Interaction of viral proteins with host cell death machinery. Cell Death Differ. 5: 653-659.
12. Takizawa, T., S. Matsukawa, Y. Higuchi, S. Nakamura, Y. Nakanishi, and R. Fukuda. 1993. Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells. J. Gen. Virol. 74: 2347-2355.
13. Hinshaw, V. S., C. W. Olsen, N. Dybdahl-Sissoko, and D. Evans. 1994. Apoptosis: a mechanism of cell killing by influenza A and B viruses. J. Virol. 68: 3667-3673.
14. Fasq, H., M. Bacher, M. Nain, and D. Gemsa. 1994. Programmed cell death (apoptosis) in human monocytes infected by influenza A virus. Immnobiology 190: 175-182.
15. Mori, I., T. Komatsu, K. Takeuchi, K. Nakakuki, M. Sudo, and Y. Kimura. 1995. In vivo induction of apoptosis by influenza virus. J. Gen. Virol. 76: 2869-2873.
16. Fujimoto, I., T. Takizawa, Y. Ohba, and Y. Nakanishi. 1998. Co-expression of Fas and Fas-ligand on the surface of influenza virus-infected cells. Cell Death Differ. 5: 426-431.
17. Ishikawa, E., M. Nakazawa, M. Yoshinari, and M. Minami. 2005. Role of tumor necrosis factor-related apoptosis-inducing ligand in immune response to influenza virus infection in mice. J. Virol. 79: 7658-7663.
18. Shiratsuchi, A., M. Kaido, T. Takizawa, and Y. Nakanishi. 2000. Phosphatidyl-serine-mediated phagocytosis of influenza A virus-infected cells by mouse peritoneal macrophages. J. Virol. 74: 9240-9244.
19. Watanabe, Y., A. Shiratsuchi, K. Shimizu, T. Takizawa, and Y. Nakanishi. 2002. Role of phosphatidylserine exposure and sugar chain desialylation at the surface of influenza virus-infected cells in efficient phagocytosis by macrophages. J. Biol. Chem. 277: 18222-18228.
20. Watanabe, Y., A. Shiratsuchi, K. Shimizu, T. Takizawa, and Y. Nakanishi. 2004. Stimulation of phagocytosis of influenza virus-infected cell through surface desialylation of macrophages by viral neuraminidase. Microbiol. Immunol. 48: 875-881.
21. Fujimoto, I., J. Pan, T. Takizawa, and Y. Nakanishi. 2000. Virus clearance through apoptosis-dependent phagocytosis of influenza A virus-infected cells by macrophages. J. Virol. 74: 3399-3403.
22. Watanabe, Y., Y. Hashimoto, A. Shiratsuchi, T. Takizawa, and Y. Nakanishi. 2005. Augmentation of fatality of influenza in mice by inhibition of phagocytosis. Biochem. Biophys. Res. Commun. 337: 881-886.
23. Hoshino, K., O. Takeuchi, T. Kawai, H. Sanjo, T. Ogawa, Y. Takeda, K. Takeda, and S. Akira. 1999. Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162: 3749-3752.
24. Li, C. Y., K. W. Lam, and L. T. Yam. 1973. Esterases in human leukocytes. J. Histochem. Cytochem. 21: 1-12.
25. Shiratsuchi, A., I. Watanabe, O. Takeuchi, S. Akira, and Y. Nakanishi. 2004. Inhibitory effect of Toll-like receptor 4 on fusion between phagosomes and endosomes/lysosomes in macrophages. J. Immunol. 172: 2039-2047.
26. Shiratsuchi, A., M. Umeda, Y. Ohba, and Y. Nakanishi. 1997. Recognition of phosphatidylserine on the surface of apoptotic spermatogenic cells and subsequent phagocytosis by Sertoli cells of the rat. J. Biol. Chem. 272: 2354-2358.
27. Iyoda, T., K. Nagata, M. Akashi, and Y. Kobayashi. 2005. Neutrophils accelerate macrophage-mediated digestion of apoptotic cells in vivo as well as in vitro. J. Immunol. 175: 3475-3483.
28. Oka, K., T. Sawamura, K.-I. Kikuta, S. Itokawa, N. Kume, T. Kita, and T. Masaki. 1998. Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc. Natl. Acad. Sci. USA 95: 9535-9540.
29. Kawasaki, Y., A. Nakagawa, K. Nagaosa, A. Shiratsuchi, and Y. Nakanishi. 2002. Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular Sertoli cells. J. Biol. Chem. 277: 27559-27566.
30. Weitzman, J. B. 2004. The curious world of apoptotic cell clearance. J. Biol. 3: 13.
31. Williamson, P., and R. A. Schlegel. 2004. Hide and seek: the secret identity of the phosphatidylserine receptor. J. Biol. 3: 14.
32. Ishimoto, Y., K. Ohashi, K. Mizuno, and T. Nakano. 2000. Promotion of the uptake of PS liposomes and apoptotic cells by a product of growth arrest-specific gene, gas6. J. Biochem. 127: 411-417.
33. Anderson, H. A., C. A. Maylock, J. A. Williams, C. P. Paweletz, H. Shu, and E. Shacter. 2002. Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat. Immunol. 4: 87-91.
34. Hanayama, R., M. Tanaka, K. Miwa, A. Shinohara, A. Iwamatsu, and S. Nagata. 2002. Identification of a factor that links apoptotic cells to phagocytes. Nature 417: 182-187.
35. Hanayama, R., M. Tanaka, K. Miwa, and S. Nagata. 2004. Expression of developmental endothelial locus-1 in a subset of macrophages for engulfment of apoptotic cells. J. Immunol. 172: 3876-3882.
36. Schagat, T. L., J. A. Wofford, and J. R. Wright. 2001. Surfactant protein A enhances alveolar macrophage phagocytosis of apoptotic neutrophils. J. Immunol. 166: 2727-2733.
37. Uchide, N., K. Ohyama, B. Yuan, T. Bessho, and T. Yamakawa. 2002. Differentiation of monocytes to macrophages induced by influenza virus-infected apoptotic cells. J. Gen. Virol. 83: 747-751.
38. 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.
39. Cathelin, S., C. Rébé, L. Haddaoui, N. Simioni, F. Verdier, M. Fontenay, S. Launay, P. Mayeux, and E. Solary. 2006. Identification of proteins cleaved downstream of caspase activation in monocytes undergoing macrophage differentiation. J. Biol. Chem. 281: 17779-17788.
40. Ludwig, S., S. Pleschka, O. Planz, and T. Wolff. 2006. Ringing the alarm bells: signalling and apoptosis in influenza virus infected cells. Cell. Microbiol. 8: 375-386.
41. Haynes, L. M., D. D. Moore, E. A. Kurt-Jones, R. W. Finberg, L. J. Anderson, and R. A. Tripp. 2001. Involvement of Toll-like receptor 4 in innate immunity to respiratory syncytial virus. J. Virol. 75: 10730-10737.
42. van der Sluijs, K. F., L. van Eiden, M. Nijhuis, R. Schuurman, S. Florquin, H. M. Jansen, R. Lutter, and T. van der Poll. 2003. Toll-like receptor 4 is not involved in host defense against respiratory tract infection with Sendai virus. Immunol. Lett. 89: 201-206.
43. Cluff, C. W., J. R. Baldridge, A. G. Stöver, J. T. Evans, D. A. Johnson, M. J. Lacy, V. G. Clawson, V. M. Yorgensen, C. L. Johnson, M. T. Livesay, et al. 2005. Synthetic Toll-like receptor 4 agonists stimulate innate resistance to infectious challenge. Infect. Immun. 73: 3044-3052.