HLA tapasin independence: broader peptide repertoire and HIV control

被引:53
作者
Bashirova, Arman A. [1 ]
Viard, Mathias [1 ]
Naranbhai, Vivek [2 ]
Grifoni, Alba [3 ]
Garcia-Beltran, Wilfredo [4 ,5 ]
Akdag, Marjan [1 ]
Yuki, Yuko [1 ]
Gao, Xiaojiang [1 ]
O'hUigin, Colm [1 ]
Raghavan, Malini [6 ]
Wolinsky, Steven [7 ]
Bream, Jay H. [8 ]
Duggal, Priya [9 ]
Martinson, Jeremy [10 ]
Michael, Nelson L. [11 ]
Kirk, Gregory D. [9 ]
Buchbinder, Susan P. [12 ]
Haas, David [13 ]
Goedert, James J. [14 ,15 ]
Deeks, Steven G. [16 ]
Fellay, Jacques [17 ,18 ]
Walker, Bruce [4 ,5 ]
Goulder, Philip [19 ]
Cresswell, Peter [20 ]
Elliott, Tim [21 ,22 ]
Sette, Alessandro [3 ,23 ]
Carlson, Jonathan [24 ]
Carrington, Mary [1 ,4 ,5 ]
机构
[1] Frederick Natl Lab Canc Res, Basic Sci Program, Frederick, MD 21702 USA
[2] Dana Farber Canc Inst, Dept Med Oncol, Boston, MA 02215 USA
[3] La Jolla Inst Immunol, Div Vaccine Discovery, La Jolla, CA 92037 USA
[4] MIT, Massachusetts Gen Hosp, Ragon Inst, 77 Massachusetts Ave, Cambridge, MA 02139 USA
[5] Harvard Univ, Cambridge, MA 02139 USA
[6] Univ Michigan, Sch Med, Dept Microbiol & Immunol, Ann Arbor, MI 48109 USA
[7] Northwestern Univ, Feinberg Sch Med, Div Infect Dis, Chicago, IL 60611 USA
[8] Johns Hopkins Bloomberg Sch Publ Hlth, Dept Mol Microbiol & Immunol, Baltimore, MD 21205 USA
[9] Johns Hopkins Bloomberg Sch Publ Hlth, Dept Epidemiol, Baltimore, MD 21205 USA
[10] Univ Pittsburgh, Grad Sch Publ Hlth, Dept Infect Dis & Microbiol, Pittsburgh, PA 15261 USA
[11] Walter Reed Army Inst Res, US Mil HIV Res Program, Silver Spring, MD 20910 USA
[12] San Francisco Dept Publ Hlth, HIV Res Sect, San Francisco, CA 94102 USA
[13] Vanderbilt Univ, Sch Med, Dept Pharmacol, Nashville, TN 37204 USA
[14] NIH, Infect & Immunoepidemiol Branch, Div Canc Epidemiol, Rockville, MD 20850 USA
[15] NCI, NIH, Rockville, MD 20850 USA
[16] Univ Calif San Francisco, Dept Med, San Francisco, CA 94110 USA
[17] Ecole Polytech Fed Lausanne, Sch Life Sci, CH-1015 Lausanne, Switzerland
[18] Swiss Inst Bioinformat, CH-1015 Lausanne, Switzerland
[19] Univ Oxford, Dept Paediat, Oxford OX1 4AJ, England
[20] Yale Univ, Sch Med, Dept Immunobiol, New Haven, CT 06520 USA
[21] Univ Southampton, Inst Life Sci, Southampton SO17 1BJ, Hants, England
[22] Univ Southampton, Ctr Canc Immunol, Southampton SO16 6YD, Hants, England
[23] Univ Calif San Diego, Dept Med, La Jolla, CA 92093 USA
[24] Microsoft Healthcare NExT, Immun, Redmond, WA 98052 USA
基金
美国国家卫生研究院;
关键词
HLA; tapasin; peptide repertoire; CLASS-I MOLECULES; T-CELL RESPONSES; ANTIGEN PRESENTATION; SURFACE EXPRESSION; REVEALS POLYMORPHISM; B-CELL; MECHANISM; AFFINITY; PROTEINS; ABSENCE;
D O I
10.1073/pnas.2013554117
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Human leukocyte antigen (HLA) class I allotypes vary in their ability to present peptides in the absence of tapasin, an essential component of the peptide loading complex. We quantified tapasin dependence of all allotypes that are common in European and African Americans (n = 97), which revealed a broad continuum of values. Ex vivo examination of cytotoxic T cell responses to the entire HIV-1 proteome from infected subjects indicates that tapasin-dependent allotypes present a more limited set of distinct peptides than do tapasin-independent allotypes, data supported by computational predictions. This suggests that variation in tapasin dependence may impact the strength of the immune responses by altering peptide repertoire size. In support of this model, we observed that individuals carrying HLA class I genotypes characterized by greater tapasin independence progress more slowly to AIDS and maintain lower viral loads, presumably due to increased breadth of peptide presentation. Thus, tapasin dependence level, like HLA zygosity, may serve as a means to restrict or expand breadth of the HLA-I peptide repertoire across humans, ultimately influencing immune responses to pathogens and vaccines.
引用
收藏
页码:28232 / 28238
页数:7
相关论文
共 45 条
[1]   Relative Expression Levels of the HLA Class-I Proteins in Normal and HIV-Infected Cells [J].
Apps, Richard ;
Meng, Zhaojing ;
Del Prete, Gregory Q. ;
Lifson, Jeffrey D. ;
Zhou, Ming ;
Carrington, Mary .
JOURNAL OF IMMUNOLOGY, 2015, 194 (08) :3594-+
[2]   HLA Heterozygote Advantage against HIV-1 Is Driven by Quantitative and Qualitative Differences in HLA Allele-Specific Peptide Presentation [J].
Arora, Jatin ;
Pierini, Federica ;
McLaren, Paul J. ;
Carrington, Mary ;
Fellay, Jacques ;
Lenz, Tobias L. .
MOLECULAR BIOLOGY AND EVOLUTION, 2020, 37 (03) :639-650
[3]   Selector function of MHC I molecules is determined by protein plasticity [J].
Bailey, Alistair ;
Dalchau, Neil ;
Carter, Rachel ;
Emmott, Stephen ;
Phillips, Andrew ;
Werner, Joern M. ;
Elliott, Tim .
SCIENTIFIC REPORTS, 2015, 5
[4]   HLA/KIR Restraint of HIV: Surviving the Fittest [J].
Bashirova, Arman A. ;
Thomas, Rasmi ;
Carrington, Mary .
ANNUAL REVIEW OF IMMUNOLOGY, VOL 29, 2011, 29 :295-317
[5]   Structure of the human MHC-I peptide-loading complex [J].
Blees, Andreas ;
Januliene, Dovile ;
Hofmann, Tommy ;
Koller, Nicole ;
Schmidt, Carla ;
Trowitzsch, Simon ;
Moeller, Arne ;
Tampe, Robert .
NATURE, 2017, 551 (7681) :525-+
[6]   Pathways of Antigen Processing [J].
Blum, Janice S. ;
Wearsch, Pamela A. ;
Cresswell, Peter .
ANNUAL REVIEW OF IMMUNOLOGY, VOL 31, 2013, 31 :443-473
[7]   HLA and HIV-1:: Heterozygote advantage and B*35-Cw*04 disadvantage [J].
Carrington, M ;
Nelson, GW ;
Martin, MP ;
Kissner, T ;
Vlahov, D ;
Goedert, JJ ;
Kaslow, R ;
Buchbinder, S ;
Hoots, K ;
O'Brien, SJ .
SCIENCE, 1999, 283 (5408) :1748-1752
[8]   Expression levels of MHC class I molecules are inversely correlated with promiscuity of peptide binding [J].
Chappell, Paul ;
Meziane, El Kahina ;
Harrison, Michael ;
Magiera, Lukasz ;
Hermann, Clemens ;
Mears, Laura ;
Wrobel, Antony G. ;
Durant, Charlotte ;
Nielsen, Lise Lotte ;
Buus, Soren ;
Ternette, Nicola ;
Mwangi, William ;
Butter, Colin ;
Nair, Venugopal ;
Ahyee, Trudy ;
Duggleby, Richard ;
Madrigal, Alejandro ;
Roversi, Pietro ;
Lea, Susan M. ;
Kaufman, Jim .
ELIFE, 2015, 4
[9]   Analysis of interactions in a tapasin/class I complex provides a mechanism for peptide selection [J].
Chen, Mingnan ;
Bouvier, Marlene .
EMBO JOURNAL, 2007, 26 (06) :1681-1690
[10]  
Copeman J, 1998, EUR J IMMUNOL, V28, P3783, DOI 10.1002/(SICI)1521-4141(199811)28:11<3783::AID-IMMU3783>3.0.CO