Essential role for autophagy in the maintenance of immunological memory against influenza infection

Nature Medicine

Volumn 20, Issue 5, 2014, Pages 503-510

  Chen, Min ^a   Hong, Monica Jeongsoo ^a   Sun, Huanhuan ^a   Wang, Lei ^a   Shi, Xiurong ^a   Gilbert, Brian E ^a   Corry, David B ^a,b   Kheradmand, Farrah ^a,b   Wang, Jin ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY RELATED PROTEIN 7; INFLUENZA VACCINE; VIRUS ANTIBODY;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BRONCHOALVEOLAR LAVAGE FLUID; CELL DEATH; CELLS; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; HONG KONG INFLUENZA; IMMUNIZATION; IMMUNOLOGICAL MEMORY; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VACCINATION; LIPID PEROXIDATION; MEMORY CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; VIRUS LOAD; ANIMAL; B LYMPHOCYTE; BIOSYNTHESIS; HUMAN; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A H1N1;

ANIMALS; ANTIBODIES, VIRAL; AUTOPHAGY; B-LYMPHOCYTES; HUMANS; IMMUNIZATION; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; MICE;

EID: 84902954600     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3521     Document Type: Article

References (64)

1. Pulendran, B. & Ahmed, R. Immunological mechanisms of vaccination. Nat. Immunol. 12, 509–517 (2011).
2. Lenardo, M. et al. Mature T lymphocyte apoptosis—immune regulation in a dynamic and unpredictable antigenic environment. Annu. Rev. Immunol. 17, 221–253 (1999).
3. Strasser, A., Jost, P.J. & Nagata, S. The many roles of FAS receptor signaling in the immune system. Immunity 30, 180–192 (2009).
4. Krammer, P.H., Arnold, R. & Lavrik, I.N. Life and death in peripheral T cells. Nat. Rev. Immunol. 7, 532–542 (2007).
5. Kalia, V., Sarkar, S., Gourley, T.S., Rouse, B.T. & Ahmed, R. Differentiation of memory B and T cells. Curr. Opin. Immunol. 18, 255–264 (2006).
6. Lanzavecchia, A. & Sallusto, F. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2, 982–987 (2002).
7. McHeyzer-Williams, M., Okitsu, S., Wang, N. & McHeyzer-Williams, L. Molecular programming of B cell memory. Nat. Rev. Immunol. 12, 24–34 (2012).
8. Kurosaki, T., Aiba, Y., Kometani, K., Moriyama, S. & Takahashi, Y. Unique properties of memory B cells of different isotypes. Immunol. Rev. 237, 104–116 (2010).
9. Kasturi, S.P. et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470, 543–547 (2011).
10. Pape, K.A., Taylor, J.J., Maul, R.W., Gearhart, P.J. & Jenkins, M.K. Different B cell populations mediate early and late memory during an endogenous immune response. Science 331, 1203–1207 (2011).
11. Ridderstad, A. & Tarlinton, D.M. Kinetics of establishing the memory B cell population as revealed by CD38 expression. J. Immunol. 160, 4688–4695 (1998).
12. Shlomchik, M.J. & Weisel, F. Germinal center selection and the development of memory B and plasma cells. Immunol. Rev. 247, 52–63 (2012).
13. McHeyzer-Williams, L.J. & McHeyzer-Williams, M.G. Antigen-specific memory B cell development. Annu. Rev. Immunol. 23, 487–513 (2005).
14. Burton, D.R. Antibodies, viruses and vaccines. Nat. Rev. Immunol. 2, 706–713 (2002).
15. Neumann, G., Noda, T. & Kawaoka, Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459, 931–939 (2009).
16. Nakaya, H.I. et al. Systems biology of vaccination for seasonal influenza in humans. Nat. Immunol. 12, 786–795 (2011).
17. Yu, X. et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455, 532–536 (2008).
18. van Riet, E., Ainai, A., Suzuki, T. & Hasegawa, H. Mucosal IgA responses in influenza virus infections; thoughts for vaccine design. Vaccine 30, 5893–5900 (2012).
19. Gomez Lorenzo, M.M. & Fenton, M.J. Immunobiology of influenza vaccines. Chest 143, 502–510 (2013).
20. Maruyama, M., Lam, K.P. & Rajewsky, K. Memory B-cell persistence is independent of persisting immunizing antigen. Nature 407, 636–642 (2000).
21. Smith, K.G. et al. Bcl-2 transgene expression inhibits apoptosis in the germinal center and reveals differences in the selection of memory B cells and bone marrow antibody-forming cells. J. Exp. Med. 191, 475–484 (2000).
22. Fischer, S.F. et al. Proapoptotic BH3-only protein Bim is essential for developmentally programmed death of germinal center-derived memory B cells and antibody-forming cells. Blood 110, 3978–3984 (2007).
23. Clybouw, C. et al. Regulation of memory B-cell survival by the BH3-only protein Puma. Blood 118, 4120–4128 (2011).
24. Levine, B. & Klionsky, D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463–477 (2004).
25. Deretic, V. Autophagy in infection. Curr. Opin. Cell Biol. 22, 252–262 (2010).
26. Levine, B., Mizushima, N. & Virgin, H.W. Autophagy in immunity and inflammation. Nature 469, 323–335 (2011).
27. Lum, J.J. et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120, 237–248 (2005).
28. Komatsu, M. et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880–884 (2006).
29. Hara, T. et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885–889 (2006).
30. Pengo, N. et al. Plasma cells require autophagy for sustainable immunoglobulin production. Nat. Immunol. 14, 298–305 (2013).
31. Kabeya, Y. et al. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117, 2805–2812 (2004).
32. Russell, R.C. et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat. Cell Biol. 15, 741–750 (2013).
33. Liang, X.H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672–676 (1999).
34. Hara, T. et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J. Cell Biol. 181, 497–510 (2008).
35. Liang, C. et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 8, 688–699 (2006).
36. Itakura, E., Kishi, C., Inoue, K. & Mizushima, N. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19, 5360–5372 (2008).
37. Xie, Z. & Klionsky, D.J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102–1109 (2007).
38. Seglen, P.O. & Gordon, P.B. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 79, 1889–1892 (1982).
39. Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425–434 (2005).
40. Miller, B.C. et al. The autophagy gene ATG5 plays an essential role in B lymphocyte development. Autophagy 4, 309–314 (2008).
41. Takahashi, Y., Ohta, H. & Takemori, T. Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14, 181–192 (2001).
42. Lebecque, S., de Bouteiller, O., Arpin, C., Banchereau, J. & Liu, Y.J. Germinal center founder cells display propensity for apoptosis before onset of somatic mutation. J. Exp. Med. 185, 563–571 (1997).
43. Caserta, T.M., Smith, A.N., Gultice, A.D., Reedy, M.A. & Brown, T.L. Q-VD-OPh, a broad spectrum caspase inhibitor with potent antiapoptotic properties. Apoptosis 8, 345–352 (2003).
44. Degterev, A. et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 1, 112–119 (2005).
45. Kim, H.J. et al. NecroX as a novel class of mitochondrial reactive oxygen species and ONOO scavenger. Arch. Pharm. Res. 33, 1813–1823 (2010).
46. Mitchell, J., Jiang, H., Berry, L. & Meyrick, B. Effect of antioxidants on lipopolysaccharide-stimulated induction of mangano superoxide dismutase mRNA in bovine pulmonary artery endothelial cells. J. Cell. Physiol. 169, 333–340 (1996).
47. Reddan, J.R. et al. The superoxide dismutase mimic TEMPOL protects cultured rabbit lens epithelial cells from hydrogen peroxide insult. Exp. Eye Res. 56, 543–554 (1993).
48. Green, D.R., Galluzzi, L. & Kroemer, G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333, 1109–1112 (2011).
49. Gottlieb, E., Vander Heiden, M.G. & Thompson, C.B. Bcl-xL prevents the initial decrease in mitochondrial membrane potential and subsequent reactive oxygen species production during tumor necrosis factor α-induced apoptosis. Mol. Cell. Biol. 20, 5680–5689 (2000).
50. Guéraud, F. et al. Chemistry and biochemistry of lipid peroxidation products. Free Radic. Res. 44, 1098–1124 (2010).
51. Drummen, G.P., van Liebergen, L.C., Op den Kamp, J.A. & Post, J.A. C11-BODIPY(581/591), an oxidation-sensitive fluorescent lipid peroxidation probe: (micro)spectroscopic characterization and validation of methodology. Free Radic. Biol. Med. 33, 473–490 (2002).
52. Catalá, A. Lipid peroxidation modifies the picture of membranes from the “Fluid Mosaic Model” to the “Lipid Whisker Model”. Biochimie 94, 101–109 (2012).
53. Maccarrone, M., Catani, M.V., Agro, A.F. & Melino, G. Involvement of 5-lipoxygenase in programmed cell death of cancer cells. Cell Death Differ. 4, 396–402 (1997).
54. 2+-independent phospholipase A2 and 5-lipoxygenase in macrophages. Prostaglandins Other Lipid Mediat. 88, 51–61 (2009).
55. Ezekwudo, D.E., Wang, R.C. & Elegbede, J.A. Methyl jasmonate induced apoptosis in human prostate carcinoma cells via 5-lipoxygenase dependent pathway. J. Exp. Ther. Oncol. 6, 267–277 (2007).
56. Hamouda, T. et al. Efficacy, immunogenicity and stability of a novel intranasal nanoemulsion-adjuvanted influenza vaccine in a murine model. Hum. Vaccin. 6, 585–594 (2010).
57. McKinstry, K.K. et al. IL-10 deficiency unleashes an influenza-specific TH17 response and enhances survival against high-dose challenge. J. Immunol. 182, 7353–7363 (2009).
58. Tai, W. et al. Multistrain influenza protection induced by a nanoparticulate mucosal immunotherapeutic. Mucosal Immunol. 4, 197–207 (2011).
59. Rubinsztein, D.C., Gestwicki, J.E., Murphy, L.O. & Klionsky, D.J. Potential therapeutic applications of autophagy. Nat. Rev. Drug Discov. 6, 304–312 (2007).
60. Förster, I. & Rajewsky, K. The bulk of the peripheral B-cell pool in mice is stable and not rapidly renewed from the bone marrow. Proc. Natl. Acad. Sci. USA 87, 4781–4784 (1990).
61. Araki, K. et al. mTOR regulates memory CD8 T-cell differentiation. Nature 460, 108–112 (2009).
62. Kheradmand, F. et al. A protease-activated pathway underlying Th cell type 2 activation and allergic lung disease. J. Immunol. 169, 5904–5911 (2002).
63. Hornung, F., Zheng, L. & Lenardo, M.J. Maintenance of clonotype specificity in CD95/Apo-1/Fas-mediated apoptosis of mature T lymphocytes. J. Immunol. 159, 3816–3822 (1997).
64. Grumelli, S. et al. An immune basis for lung parenchymal destruction in chronic obstructive pulmonary disease and emphysema. PLoS Med. 1, e8 (2004).