Autophagy in innate and adaptive immunity against intracellular pathogens

Journal of Molecular Medicine

Volumn 84, Issue 3, 2006, Pages 194-202

  Schmid, Dorothee ^a   Dengjel, Jörn ^b   Schoor, Oliver ^b   Stevanovic, Stefan ^b   Münz, Christian ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Antigen presentation; Autophagocytosis; CD4 positive T lymphocytes; MHC class II; Natural immunity

Indexed keywords

CELL NUCLEUS ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE DERIVATIVE;

ANTIGEN SPECIFICITY; AUTOPHAGY; B LYMPHOCYTE; BACTERIUM; CD4+ T LYMPHOCYTE; DENDRITIC CELL; ENDOCYTOSIS; ENDOSOME; EPITHELIUM CELL; HELPER CELL; IMMUNE SYSTEM; IMMUNITY; IMMUNOSURVEILLANCE; INFLAMMATION; INNATE IMMUNITY; LYSOSOME; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PATHOGENESIS; REVIEW; T LYMPHOCYTE; VIRUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AUTOPHAGY; BACTERIAL INFECTIONS; CD4-POSITIVE T-LYMPHOCYTES; CYTOPLASM; ENDOCYTOSIS; ENDOSOMES; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS; IMMUNITY, NATURAL; INFECTION; LYSOSOMES;

EID: 33344475671     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-005-0014-4     Document Type: Review

References (90)

1. Kloetzel PM (2001) Antigen processing by the proteasome. Nat Rev Mol Cell Biol 2:179-187
2. Kornfeld S, Mellman I (1989) The biogenesis of lysosomes. Annu Rev Cell Biol 5:483-525
3. Yewdell JW, Reits E, Neefjes J (2003) Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat Rev Immunol 3:952-961
4. Stuart LM, Ezekowitz RA (2005) Phagocytosis: elegant complexity. Immunity 22:539-550
5. Henell F, Berkenstam A, Ahlberg J, Glaumann H (1987) Degradation of short- and long-lived proteins in perfused liver and in isolated autophagic vacuoles-lysosomes. Exp Mol Pathol 46:1-14
6. Trombetta ES, Mellman I (2005) Cell biology of antigen processing in vitro and in vivo. Annu Rev Immunol 23:975-1028
7. De Duve C, Wattiaux R (1966) Functions of lysosomes. Annu Rev Physiol 28:435-492
8. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432:1032-1036
9. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721
10. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15:1101-1111
11. Cuervo AM, Dice JF (1996) A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273:501-503
12. Cuervo AM, Dice JF (2000) Unique properties of lamp2a compared to other lamp2 isoforms. J Cell Sci 113(Pt 24):4441-4450
13. Chiang HL, Terlecky SR, Plant CP, Dice JF (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246:382-385
14. Agarraberes FA, Terlecky SR, Dice JF (1997) An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation. J Cell Biol 137:825-834
15. Agarraberes FA, Dice JF (2001) Protein translocation across membranes. Biochim Biophys Acta 1513:1-24
16. Yoshimori T (2004) Autophagy: a regulated bulk degradation process inside cells. Biochem Biophys Res Commun 313:453-458
17. Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, Sibirny A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y (2003) A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539-545
18. Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395:395-398
19. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19:5720-5728
20. Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488-492
21. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V (2004) Autophagy is a defense mechanism inhibiting BCG and mycobacterium tuberculosis survival in infected macrophages. Cell 119:753-766
22. Kim J, Klionsky DJ (2000) Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu Rev Biochem 69:303-342
23. Shintani T, Huang WP, Stromhaug PE, Klionsky DJ (2002) Mechanism of cargo selection in the cytoplasm to vacuole targeting pathway. Dev Cell 3:825-837
24. Suzuki K, Kamada Y, Ohsumi Y (2002) Studies of cargo delivery to the vacuole mediated by autophagosomes in Saccharomyces cerevisiae. Dev Cell 3:815-824
25. Simonsen A, Birkeland HC, Gillooly DJ, Mizushima N, Kuma A, Yoshimori T, Slagsvold T, Brech A, Stenmark H (2004) Alfy, a novel FYVE-domain-containing protein associated with protein granules and autophagic membranes. J Cell Sci 117:4239-4251
26. Levine B (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120:159-162
27. Kirkegaard K, Taylor MP, Jackson WT (2004) Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat Rev Microbiol 2:301-314
28. Shintani T, Klionsky DJ (2004) Autophagy in health and disease: a double-edged sword. Science 306:990-995
29. Rich KA, Burkett C, Webster P (2003) Cytoplasmic bacteria can be targets for autophagy. Cell Microbiol 5:455-468
30. Nakagawa I, Amano A, Mizushima N, Yamamoto A, Yamaguchi H, Kamimoto T, Nara A, Funao J, Nakata M, Tsuda K, Hamada S, Yoshimori T (2004) Autophagy defends cells against invading group A Streptococcus. Science 306:1037-1040
31. Ogawa M, Yoshimori T, Suzuki T, Sagara H, Mizushima N, Sasakawa C (2005) Escape of intracellular shigella from autophagy. Science 307:727-731
32. Amer AO, Swanson MS (2005) Autophagy is an immediate macrophage response to Legionella pneumophila. Cell Microbiol 7:765-778
33. Talloczy Z, Jiang W, Virgin, HWt, Leib DA, Scheuner D, Kaufman RJ, Eskelinen EL, Levine B (2002) Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc Natl Acad Sci U S A 99:190-195
34. Liang XH, Kleeman LK, Jiang HH, Gordon G, Goldman JE, Berry G, Herman B, Levine B (1998) Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J Virol 72:8586-8596
35. Prentice E, Jerome WG, Yoshimori T, Mizushima N, Denison MR (2004) Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem 279:10136-10141
36. Pedersen KW, van der Meer Y, Roos N, Snijder EJ (1999) Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J Virol 73:2016-2026
37. Schlegel A, Giddings TH Jr, Ladinsky MS, Kirkegaard K (1996) Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 70:6576-6588
38. Suhy DA, Giddings TH Jr, Kirkegaard K (2000) Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 74:8953-8965
39. Jackson WT, Giddings TH Jr, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR, Kirkegaard K (2005) Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 3:e156
40. Meyers G, Stoll D, Gunn M (1998) Insertion of a sequence encoding light chain 3 of microtubule-associated proteins 1A and 1B in a pestivirus genome: connection with virus cytopathogenicity and induction of lethal disease in cattle. J Virol 72:4139-4148
41. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S (1999) SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219
42. Chicz RM, Urban RG, Gorga JC, Vignali DA, Lane WS, Strominger JL (1993) Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J Exp Med 178:27-47
43. Dongre AR, Kovats S, deRoos P, McCormack AL, Nakagawa T, Paharkova-Vatchkova V, Eng J, Caldwell H, Yates JR III, Rudensky AY (2001) In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses. Eur J Immunol 31:1485-1494
44. Dengjel J, Schoor O, Fischer R, Reich M, Kraus M, Muller M, Kreymborg K, Altenberend F, Brandenburg J, Kalbacher H, Brock R, Driessen C, Rammensee HG, Stevanovic S (2005) Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc Natl Acad Sci U S A 102:7922-7927
45. Aniento F, Roche E, Cuervo AM, Knecht E (1993) Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J Biol Chem 268:10463-10470
46. Fengsrud M, Raiborg C, Berg TO, Stromhaug PE, Ueno T, Erichsen ES, Seglen PO (2000) Autophagosome-associated variant isoforms of cytosolic enzymes. Biochem J 352(Pt 3):773-781
47. Friede T, Gnau V, Jung G, Keilholz W, Stevanovic S, Rammensee HG (1996) Natural ligand motifs of closely related HLA-DR4 molecules predict features of rheumatoid arthritis associated peptides. Biochim Biophys Acta 1316:85-101
48. Harris PE, Maffei A, Colovai AI, Kinne J, Tugulea S, Suciu-Foca N (1996) Predominant HLA-class II bound self-peptides of a hematopoietic progenitor cell line are derived from intracellular proteins. Blood 87:5104-5112
49. Rammensee HG, Bachmann J, Stevanovic S (1997) MHC ligands and peptide motifs. Springer, Berlin Heidelberg New York; Landes Bioscience, Austin
50. Seglen PO, Gordon PB (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79:1889-1892
51. Nimmerjahn F, Milosevic S, Behrends U, Jaffee EM, Pardoll DM, Bornkamm GW, Mautner J (2003) Major histocompatibility complex class II-restricted presentation of a cytosolic antigen by autophagy. Eur J Immunol 33:1250-1259
52. Brazil MI, Weiss S, Stockinger B (1997) Excessive degradation of intracellular protein in macrophages prevents presentation in the context of major histocompatibility complex class II molecules. Eur J Immunol 27:1506-1514
53. Dörfel D, Appel S, Grunebach F, Weck MM, Muller MR, Heine A, Brossart P (2005) Processing and presentation of HLA class I and II epitopes by dendritic cells after transfection with in vitro transcribed MUC1 RNA. Blood 105:3199-3205
54. Paludan C, Schmid D, Landthaler M, Vockerodt M, Kube D, Tuschl T, Münz C (2005) Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307:593-596
55. Blommaart EF, Krause U, Schellens JP, Vreeling-Sindelarova H, Meijer AJ (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243:240-246
56. Biederbick A, Kern HF, Elsasser HP (1995) Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66:3-14
57. Zhou D, Li P, Lott JM, Hislop A, Canaday DH, Brutkiewicz RR, Blum JS (2005) Lamp-2a facilitates MHC class II presentation of cytoplasmic antigens. Immunity 22:571-581
58. Lich JD, Elliott JF, Blum JS (2000) Cytoplasmic processing is a prerequisite for presentation of an endogenous antigen by major histocompatibility complex class II proteins. J Exp Med 191:1513-1524
59. Dul JL, Davis DP, Williamson EK, Stevens FJ, Argon Y (2001) Hsp70 and antifibrillogenic peptides promote degradation and inhibit intracellular aggregation of amyloidogenic light chains. J Cell Biol 152:705-716
60. Barette C, Jariel-Encontre I, Piechaczyk M, Piette J (2001) Human cyclin C protein is stabilized by its associated kinase cdk8, independently of its catalytic activity. Oncogene 20:551-562
61. Dice JF, Goldberg AL (1975) A statistical analysis of the relationship between degradative rates and molecular weights of proteins. Arch Biochem Biophys 170:213-219
62. Gueguen M, Long EO (1996) Presentation of a cytosolic antigen by major histocompatibility complex class II molecules requires a long-lived form of the antigen. Proc Natl Acad Sci U S A 93:14692-14697
63. Blake N, Lee S, Redchenko I, Thomas W, Steven N, Leese A, Steigerwald-Mullen P, Kurilla MG, Frappier L, Rickinson A (1997) Human CD8+ T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing. Immunity 7:791-802
64. Levitskaya J, Sharipo A, Leonchiks A, Ciechanover A, Masucci MG (1997) Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1. Proc Natl Acad Sci U S A 94:12616-12621
65. Lee SP, Brooks JM, Al-Jarrah H, Thomas WA, Haigh TA, Taylor GS, Humme S, Schepers A, Hammerschmidt W, Yates JL, Rickinson AB, Blake NW (2004) CD8 T cell recognition of endogenously expressed Epstein-Barr virus nuclear antigen 1. J Exp Med 199:1409-1420
66. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404:770-774
67. Reits EA, Vos JC, Gromme M, Neefjes J (2000) The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature 404:774-778
68. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, Bennink JR, Yewdell JW (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18:343-354
69. Ciechanover A, Finley D, Varshavsky A (1984) Ubiquitin dependence of selective protein degradation demonstrated in the mammalian cell cycle mutant ts85. Cell 37:57-66
70. Zwart W, Griekspoor A, Kuijl C, Marsman M, van Rheenen J, Janssen H, Calafat J, van Ham M, Janssen L, van Lith M, Jalink K, Neefjes J (2005) Spatial separation of HLA-DM/HLA-DR interactions within MIIC and phagosome-induced immune escape. Immunity 22:221-233
71. Stromhaug PE, Berg TO, Fengsrud M, Seglen PO (1998) Purification and characterization of autophagosomes from rat hepatocytes. Biochem J 335(Pt 2):217-224
72. Fengsrud M, Erichsen ES, Berg TO, Raiborg C, Seglen PO (2000) Ultrastructural characterization of the delimiting membranes of isolated autophagosomes and amphisomes by freeze-fracture electron microscopy. Eur J Cell Biol 79:871-882
73. Lajoie P, Guay G, Dennis JW, Nabi IR (2005) The lipid composition of autophagic vacuoles regulates expression of multilamellar bodies. J Cell Sci 118:1991-2003
74. Berg TO, Fengsrud M, Stromhaug PE, Berg T, Seglen PO (1998) Isolation and characterization of rat liver amphisomes. Evidence for fusion of autophagosomes with both early and late endosomes. J Biol Chem 273:21883-21892
75. Liou W, Geuze HJ, Geelen MJ, Slot JW (1997) The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 136:61-70
76. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ (1997) Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 139:639-649
77. Starr TK, Jameson SC, Hogquist KA (2003) Positive and negative selection of T cells. Annu Rev Immunol 21:139-176
78. Reith W, Mach B (2001) The bare lymphocyte syndrome and the regulation of MHC expression. Annu Rev Immunol 19:331-373
79. + T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 5:927-933
80. + T-cell response. Nat Rev Immunol 4:595-602
81. + T cell-mediated cytotoxicity. J Immunol 152:1127-1133
82. Hahn S, Gehri R, Erb P (1995) Mechanism and biological significance of CD4-mediated cytotoxicity. Immunol Rev 146:57-79
83. + CTLs ex vivo. J Immunol 168:5954-5958
84. Jellison ER, Kim SK, Welsh RM (2005) Cutting edge: MHC class II-restricted killing in vivo during viral infection. J Immunol 174:614-618
85. + Th1 cells kill Burkitt's lymphoma cells. J Immunol 169:1593-1603
86. +-T-cell clones reactive to EBNA1 inhibit epstein-barr virus-induced B-cell proliferation. J Virol 77:12088-12104
87. Stevenson PG, Cardin RD, Christensen JP, Doherty PC (1999) Immunological control of a murine gammaherpesvirus independent of CD8+ T cells. J Gen Virol 80:477-483
88. Sparks-Thissen RL, Braaten DC, Kreher S, Speck SH, Virgin HW (2004) An optimized CD4 T-cell response can control productive and latent gammaherpesvirus infection. J Virol 78:6827-6835
89. Robertson KA, Usherwood EJ, Nash AA (2001) Regression of a murine gammaherpesvirus 68-positive B-cell lymphoma mediated by CD4 T lymphocytes. J Virol 75:3480-3482
90. + T cells in the control of mouse Burkitt lymphoma in vivo. J Clin Invest 114:542-550