Topological journey of parasite-derived antigens for presentation by MHC class I molecules

Trends in Immunology

Volumn 31, Issue 11, 2010, Pages 414-421

  Blanchard, Nicolas ^a,b   Shastri, Nilabh ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHU PURPAN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PARASITE ANTIGEN;

AMINO TERMINAL SEQUENCE; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CYTOPLASM; CYTOSOL; DENDRITIC CELL; ENDOPLASMIC RETICULUM; HOST CELL; HUMAN; INTRACELLULAR SIGNALING; INTRACELLULAR TRANSPORT; LEISHMANIA; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PARASITE; PATHOGENESIS; PHAGOSOME; PLASMODIUM; PROTEIN DEGRADATION; REVIEW; TRYPANOSOMA CRUZI; VIRUS CELL INTERACTION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; ANTIGENS; CYTOPLASM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS;

EID: 78049287610     PISSN: 14714906     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.it.2010.08.004     Document Type: Review

References (88)

1. Bevan M.J. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 1976, 143:1283-1288.
2. Bevan M.J. Cross-priming. Nat. Immunol. 2006, 7:363-365.
3. den Haan J.M., et al. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 2000, 192:1685-1696.
4. Allan R.S., et al. Epidermal viral immunity induced by CD8alpha+ dendritic cells but not by Langerhans cells. Science 2003, 301:1925-1928.
5. Belz G.T., et al. Cutting edge: conventional CD8 alpha+ dendritic cells are generally involved in priming CTL immunity to viruses. J. Immunol. 2004, 172:1996-2000.
6. Hildner K., et al. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 2008, 322:1097-1100.
7. Rock K.L., Shen L. Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 2005, 207:166-183.
8. Cresswell P., et al. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev. 2005, 207:145-157.
9. Hansen T.H., Bouvier M. MHC class I antigen presentation: learning from viral evasion strategies. Nat. Rev. Immunol. 2009, 9:503-513.
10. Krysko D.V., et al. Clearance of apoptotic and necrotic cells and its immunological consequences. Apoptosis 2006, 11:1709-1726.
11. Lutz M.B., Kurts C. Induction of peripheral CD4+ T-cell tolerance and CD8+ T-cell cross-tolerance by dendritic cells. Eur. J. Immunol. 2009, 39:2325-2330.
12. Belz G.T., et al. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J. Exp. Med. 2002, 196:1099-1104.
13. Nimmerjahn F., Ravetch J.V. Fcgamma receptors as regulators of immune responses. Nat. Rev. Immunol. 2008, 8:34-47.
14. Harbers S.O., et al. Antibody-enhanced cross-presentation of self antigen breaks T cell tolerance. J. Clin. Invest. 2007, 117:1361-1369.
15. Maurer T., et al. CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur. J. Immunol. 2002, 32:2356-2364.
16. Weck M.M., et al. TLR ligands differentially affect uptake and presentation of cellular antigens. Blood 2007, 109:3890-3894.
17. Norbury C.C., et al. Class I MHC presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 1995, 3:783-791.
18. Brossart P., Bevan M.J. Presentation of exogenous protein antigens on major histocompatibility complex class I molecules by dendritic cells: pathway of presentation and regulation by cytokines. Blood 1997, 90:1594-1599.
19. Kovacsovics-Bankowski M., Rock K.L. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science 1995, 267:243-246.
20. Schulz O., Reis e Sousa C. Cross-presentation of cell-associated antigens by CD8alpha+ dendritic cells is attributable to their ability to internalize dead cells. Immunology 2002, 107:183-189.
21. Fonteneau J.F., et al. Characterization of the MHC class I cross-presentation pathway for cell-associated antigens by human dendritic cells. Blood 2003, 102:4448-4455.
22. Houde M., et al. Phagosomes are competent organelles for antigen cross-presentation. Nature 2003, 425:402-406.
23. Guermonprez P., et al. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003, 425:397-402.
24. Zwickey H.L., Potter T.A. Antigen secreted from noncytosolic Listeria monocytogenes is processed by the classical MHC class I processing pathway. J. Immunol. 1999, 162:6341-6350.
25. Delamarre L., et al. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005, 307:1630-1634.
26. Savina A., et al. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006, 126:205-218.
27. Savina A., et al. The small GTPase Rac2 controls phagosomal alkalinization and antigen crosspresentation selectively in CD8(+) dendritic cells. Immunity 2009, 30:544-555.
28. Bougneres L., et al. A role for lipid bodies in the cross-presentation of phagocytosed antigens by MHC class I in dendritic cells. Immunity 2009, 31:232-244.
29. Taylor G.A., et al. Control of IFN-gamma-mediated host resistance to intracellular pathogens by immunity-related GTPases (p47 GTPases). Microbes Infect. 2007, 9:1644-1651.
30. Shen L., et al. Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 2004, 21:155-165.
31. Liao H., et al. Insulin-regulated aminopeptidase marks an antigen-stimulated recycling compartment in mast cells. Traffic 2006, 7:155-167.
32. Saveanu L., et al. IRAP identifies an endosomal compartment required for MHC class I cross-presentation. Science 2009, 325:213-217.
33. Rodriguez A., et al. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1999, 1:362-368.
34. Imai J., et al. Exogenous antigens are processed through the endoplasmic reticulum-associated degradation (ERAD) in cross-presentation by dendritic cells. Int. Immunol. 2005, 17:45-53.
35. Ackerman A.L., et al. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 2006, 25:607-617.
36. Touret N., et al. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 2005, 123:157-170.
37. Gagnon E., et al. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002, 110:119-131.
38. Goldszmid R.S., et al. Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J. Exp. Med. 2009, 206:399-410.
39. Giles D.K., Wyrick P.B. Trafficking of chlamydial antigens to the endoplasmic reticulum of infected epithelial cells. Microbes Infect. 2008, 10:1494-1503.
40. Ackerman A.L., et al. Access of soluble antigens to the endoplasmic reticulum can explain cross-presentation by dendritic cells. Nat. Immunol. 2005, 6:107-113.
41. Burgdorf S., et al. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 2008, 9:558-566.
42. Hammer G.E., et al. The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat. Immunol. 2006, 7:103-112.
43. Blanchard N., et al. Endoplasmic reticulum aminopeptidase associated with antigen processing defines the composition and structure of MHC class I peptide repertoire in normal and virus-infected cells. J. Immunol. 2010, 184:3033-3042.
44. Firat E., et al. The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in cross-presentation. J. Immunol. 2007, 178:2241-2248.
45. Yan J., et al. In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J. Exp. Med. 2006, 203:647-659.
46. Ackerman A.L., et al. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:12889-12894.
47. Romero P., et al. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature 1989, 341:323-326.
48. Starnbach M.N., et al. An inclusion membrane protein from Chlamydia trachomatis enters the MHC class I pathway and stimulates a CD8+ T cell response. J. Immunol. 2003, 171:4742-4749.
49. Blanchard N., et al. Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nat. Immunol. 2008, 9:937-944.
50. Villanueva M.S., et al. Listeriolysin is processed efficiently into an MHC class I-associated epitope in Listeria monocytogenes-infected cells. J. Immunol. 1995, 155:5227-5233.
51. Kamath A.B., et al. Cytolytic CD8+ T cells recognizing CFP10 are recruited to the lung after Mycobacterium tuberculosis infection. J. Exp. Med. 2004, 200:1479-1489.
52. Tarun A.S., et al. A combined transcriptome and proteome survey of malaria parasite liver stages. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:305-310.
53. Xia D., et al. The proteome of Toxoplasma gondii: integration with the genome provides novel insights into gene expression and annotation. Genome Biol. 2008, 9:R116.
54. Kwok L.Y., et al. The induction and kinetics of antigen-specific CD8 T cells are defined by the stage specificity and compartmentalization of the antigen in murine toxoplasmosis. J. Immunol. 2003, 170:1949-1957.
55. Bertholet S., et al. Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J. Immunol. 2006, 177:3525-3533.
56. Plebanski M., et al. Direct processing and presentation of antigen from malaria sporozoites by professional antigen-presenting cells in the induction of CD8 T-cell responses. Immunol. Cell Biol. 2005, 83:307-312.
57. Chakravarty S., et al. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 2007, 13:1035-1041.
58. Tvinnereim A.R., et al. Neutrophil involvement in cross-priming CD8+ T cell responses to bacterial antigens. J. Immunol. 2004, 173:1994-2002.
59. Bertholet S., et al. Antigen requirements for efficient priming of CD8+ T cells by Leishmania major-infected dendritic cells. Infect. Immun. 2005, 73:6620-6628.
60. Gubbels M.J., et al. Class I major histocompatibility complex presentation of antigens that escape from the parasitophorous vacuole of Toxoplasma gondii. Infect. Immun. 2005, 73:703-711.
61. Bongfen S.E., et al. Processing of the circumsporozoite protein in infected hepatocytes is not dependent on aspartic proteases. Parasite Immunol. 2008, 30:375-378.
62. Lewinsohn D.M., et al. Characterization of human CD8+ T cells reactive with Mycobacterium tuberculosis-infected antigen-presenting cells. J. Exp. Med. 1998, 187:1633-1640.
63. Gervassi A.L., et al. Functional characterization of class Ia- and non-class Ia-restricted Chlamydia-reactive CD8+ T cell responses in humans. J. Immunol. 2003, 171:4278-4286.
64. Harty J.T., Pamer E.G. CD8 T lymphocytes specific for the secreted p60 antigen protect against Listeria monocytogenes infection. J. Immunol. 1995, 154:4642-4650.
65. Teitelbaum R., et al. Mycobacterial infection of macrophages results in membrane-permeable phagosomes. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:15190-15195.
66. Smith J., et al. Evidence for pore formation in host cell membranes by ESX-1-secreted ESAT-6 and its role in Mycobacterium marinum escape from the vacuole. Infect. Immun. 2008, 76:5478-5487.
67. Schwab J.C., et al. The parasitophorous vacuole membrane surrounding intracellular Toxoplasma gondii functions as a molecular sieve. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:509-513.
68. Desai S.A., Rosenberg R.L. Pore size of the malaria parasite's nutrient channel. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:2045-2049.
69. Fling S.P., et al. CD8+ T cells recognize an inclusion membrane-associated protein from the vacuolar pathogen Chlamydia trachomatis. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1160-1165.
70. Hiller N.L., et al. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004, 306:1934-1937.
71. Saeij J.P., et al. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 2006, 314:1780-1783.
72. Taylor S., et al. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 2006, 314:1776-1780.
73. Singh A.P., et al. Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 2007, 131:492-504.
74. de Koning-Ward T.F., et al. A newly discovered protein export machine in malaria parasites. Nature 2009, 459:945-949.
75. Howard J. The IRG proteins: a function in search of a mechanism. Immunobiology 2008, 213:367-375.
76. Ling Y.M., et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J. Exp. Med. 2006, 203:2063-2071.
77. Dzierszinski F., et al. Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infect. Immun. 2007, 75:5200-5209.
78. MacMicking J.D., et al. Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 2003, 302:654-659.
79. Singh S.B., et al. Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 2006, 313:1438-1441.
80. Coers J., et al. Chlamydia muridarum evades growth restriction by the IFN-gamma-inducible host resistance factor Irgb10. J. Immunol. 2008, 180:6237-6245.
81. Santiago H.C., et al. Mice deficient in LRG-47 display enhanced susceptibility to Trypanosoma cruzi infection associated with defective hemopoiesis and intracellular control of parasite growth. J. Immunol. 2005, 175:8165-8172.
82. Frickel E.M., et al. Parasite stage-specific recognition of endogenous Toxoplasma gondii-derived CD8+ T cell epitopes. J. Infect. Dis. 2008, 198:1625-1633.
83. Tewalt E.F., et al. Viral sequestration of antigen subverts cross presentation to CD8(+) T cells. PLoS Pathog. 2009, 5:e1000457.
84. Baena A., Porcelli S.A. Evasion and subversion of antigen presentation by Mycobacterium tuberculosis. Tissue Antigens 2009, 74:189-204.
85. Hinchey J., et al. Enhanced priming of adaptive immunity by a proapoptotic mutant of Mycobacterium tuberculosis. J. Clin. Invest. 2007, 117:2279-2288.
86. Shastri N., et al. All the peptides that fit: the beginning, the middle, and the end of the MHC class I antigen-processing pathway. Immunol. Rev. 2005, 207:31-41.
87. Peaper D.R., Cresswell P. Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 2008, 24:343-368.
88. Blanchard N., Shastri N. Coping with loss of perfection in the MHC class I peptide repertoire. Curr. Opin. Immunol. 2008, 20:82-88.