Adaptor protein 1 promotes cross-presentation through the same tyrosine signal in major histocompatibility complex class I as that targeted by HIV-1

Journal of Virology

Volumn 87, Issue 14, 2013, Pages 8085-8098

  Kulpa, Deanna A ^a   Del Cid, Natasha ^a   Peterson, Kirsten A ^a   Collins, Kathleen L ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 1; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NEF PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ALLOTYPE; ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CONTROLLED STUDY; CROSS PRESENTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE EVASION; MOLECULAR MODEL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADAPTOR PROTEIN COMPLEX 1; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN-PRESENTING CELLS; BLOTTING, WESTERN; CROSS-PRIMING; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HIV-1; HUMANS; IMMUNOPRECIPITATION; LENTIVIRUS; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; NEF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TYROSINE;

EID: 84880253155     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00701-13     Document Type: Article

References (39)

1. Collins K, Chen B, Kalams S, Walker B, Baltimore D. 1998. HIV-1 Nef protein protects infected primary human cells from killing by cytotoxic T lymphocytes. Nature 391:397-401.
2. Schwartz O, Marechal V, Le Gall S, Lemonnier F, Heard J. 1996. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat. Med. 2:338-342.
3. Swigut T, Alexander L, Morgan J, Lifson J, Mansfield KG, Lang S, Johnson RP, Skowronski J, Desrosiers R. 2004. Impact of Nef-mediated downregulation of major histocompatibility complex class I on immune response to simian immunodeficiency virus. J. Virol. 78:13335-13344.
4. Le Gall S, Erdtmann L, Benichou S, Berlloz-Torrent C, Liu L, Benarous R, Heard J, Schwartz O. 1998. Nef interacts with mu subunit of clathrin adaptor complexes and reveals a cryptic sorting signal in MHC I molecules. Immunity 8:483-495.
5. Kulpa DA, Collins KL. 2011. The emerging role of HLA-C in HIV-1 infection. Immunology 134:116-122.
6. Wonderlich ER, Williams M, Collins KL. 2008. The tyrosine-binding pocket in the adaptor protein 1 (AP-1) mu1 subunit is necessary for Nef to recruit AP-1 to the major histocompatibility complex class I cytoplasmic tail. J. Biol. Chem. 283:3011-3022.
7. Robinson MS. 2004. Adaptable adaptors for coated vesicles. Trends Cell Biol. 14:167-174.
8. Jia X, Singh R, Homann S, Yang H, Guatelli J, Xiong Y. 2012. Structural basis of evasion of cellular adaptive immunity by HIV-1 Nef. Nat. Struct. Mol. Biol. 19:701-706.
9. Amigorena S, Savina A. 2010. Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22:109-117.
10. Lizee G, Basha G, Tiong J, Julien JP, Tian M, Biron KE, Jefferies WA. 2003. Control of dendritic cell cross-presentation by the major histocompatibility complex class I cytoplasmic domain. Nat. Immunol. 4:1065-1073.
11. Roeth JF, Williams M, Kasper MR, Filzen TM, Collins KL. 2004. HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. J. Cell Biol. 167:903-913.
12. Schaefer MR, Wonderlich ER, Roeth JF, Leonard JA, Collins KL. 2008. HIV-1 Nef targets MHC-I and CD4 for degradation via a final common beta-COP-dependent pathway in T cells. PLoS Pathog. 4:e1000131. doi: 10.1371/journal.ppat.1000131.
13. Schaefer MR, Williams M, Kulpa DA, Blakely PK, Yaffee AQ, Collins KL. 2008. A novel trafficking signal within the HLA-C cytoplasmic tail allows regulated expression upon differentiation of macrophages. J. Immunol. 180:7804-7817.
14. Carter CC, Onafuwa-Nuga A, McNamara LA, Riddell J, IV, Bixby D, Savona MR, Collins KL. 2010. HIV-1 infects multipotent progenitor cells causing cell death and establishing latent cellular reservoirs. Nat. Med. 16:446-451.
15. Van Parijs L, Refaeli Y, Lord JD, Nelson BH, Abbas AK, Baltimore D. 1999. Uncoupling IL-2 signals that regulate T cell proliferation, survival, and Fas-mediated activation-induced cell death. Immunity 11:281-288.
16. Robinson A, Meredith C, Austen BM. 1986. Isolation and properties of the signal region from ovalbumin. FEBS Lett. 203:243-246.
17. Williams M, Roeth JF, Kasper MR, Filzen T, Collins KL. 2005. Human immunodeficiency virus type 1 Nef domains required for disruption of major histocompatibility complex class I trafficking are also necessary for coprecipitation of Nef with HLA-A2. J. Virol. 79:632-636.
18. Pear WS, Nolan GP, Scott ML, Baltimore D. 1993. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U. S. A. 90:8392-8396.
19. Naviaux RK, Costanzi E, Haas M, Verma IM. 1996. The pCL vector system: rapid production of helper-free, high-titer, recombinant retroviruses. J. Virol. 70:5701-5705.
20. Burns JC, Friedmann T, Driever W, Burrascano M, Yee JK. 1993. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and nonmammalian cells. Proc. Natl. Acad. Sci. U. S. A. 90:8033-8037.
21. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471.
22. Hopkins N. 1993. High titers of retrovirus (vesicular stomatitis virus) pseudotypes, at last. Proc. Natl. Acad. Sci. U. S. A. 90:8759-8760.
23. Parham P, Brodsky FM. 1981. Partial purification and some properties of BB7.2. A cytotoxic monoclonal antibody with specificity for HLA-A2 and a variant of HLA-A28. Hum. Immunol. 3:277-299.
24. Kasper MR, Collins KL. 2003. Nef-mediated disruption of HLA-A2 transport to the cell surface in T cells. J. Virol. 77:3041-3049.
25. Traub LM, Kornfeld S, Ungewickell E. 1995. Different domains of the AP-1 adaptor complex are required for Golgi membrane binding and clathrin recruitment. J. Biol. Chem. 270:4933-4942.
26. National Institutes of Health. 2002. Public Health Service policy on humane care and use of laboratory animals. Office of Laboratory Animal Welfare, National Institutes of Health, Bethesda, MD. http://grants.nih.gov/grants/olaw/references/phspol.htm.
27. Porgador A, Yewdell JW, Deng Y, Bennink JR, Germain RN. 1997. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 6:715-726.
28. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76:17-27.
29. Ackerman AL, Kyritsis C, Tampe R, Cresswell P. 2003. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. U. S. A. 100: 12889-12894.
30. Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, Van Endert P, Amigorena S. 2003. ER-phagosome fusion defines an MHC class I crosspresentation compartment in dendritic cells. Nature 425:397-402.
31. Houde M, Bertholet S, Gagnon E, Brunet S, Goyette G, Laplante A, Princiotta MF, Thibault P, Sacks D, Desjardins M. 2003. Phagosomes are competent organelles for antigen cross-presentation. Nature 425:402-406.
32. Donaldson JG, Williams DB. 2009. Intracellular assembly and trafficking of MHC class I molecules. Traffic 10:1745-1752.
33. Basha G, Omilusik K, Chavez-Steenbock A, Reinicke AT, Lack N, Choi KB, Jefferies WA. 2012. A CD74-dependent MHC class I endolysosomal cross-presentation pathway. Nat. Immunol. 13:237-245.
34. Cohen GB, Gandhi RT, Davis DM, Mandelboim O, Chen BK, Strominger JL, Baltimore D. 1999. The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIVinfected cells from NK cells. Immunity 10:661-671.
35. Thomas R, Apps R, Qi Y, Gao X, Male V, O'hUigin C, O'Connor G, Ge D, Fellay J, Martin JN, Margolick J, Goedert JJ, Buchbinder S, Kirk GD, Martin MP, Telenti A, Deeks SG, Walker BD, Goldstein D, McVicar DW, Moffett A, Carrington M. 2009. HLA-C cell surface expression and control of HIV/AIDS correlate with a variant upstream of HLA-C. Nat. Genet. 41:1290-1294.
36. Wonderlich ER, Leonard JA, Kulpa DA, Leopold KE, Norman JM, Collins KL. 2011. ADP ribosylation factor 1 activity is required to recruit AP-1 to the major histocompatibility complex class I (MHC-I) cytoplasmic tail and disrupt MHC-I trafficking in HIV-1-infected primary T cells. J. Virol. 85:12216-12226.
37. Najar HM, Dutz JP. 2007. Topical TLR9 agonists induce more efficient cross-presentation of injected protein antigen than parenteral TLR9 agonists do. Eur. J. Immunol. 37:2242-2256.
38. Robson NC, McAlpine T, Knights AJ, Schnurr M, Shin A, Chen W, Maraskovsky E, Cebon J. 2010. Processing and cross-presentation of individual HLA-A, -B, or -C epitopes from NY-ESO-1 or an HLA-A epitope for Melan-A differ according to the mode of antigen delivery. Blood 116:218-225.
39. Schnurr M, Orban M, Robson NC, Shin A, Braley H, Airey D, Cebon J, Maraskovsky E, Endres S. 2009. ISCOMATRIX adjuvant induces efficient cross-presentation of tumor antigen by dendritic cells via rapid cytosolic antigen delivery and processing via tripeptidyl peptidase II. J. Immunol. 182:1253-1259