دورية أكاديمية

Charge-based interactions through peptide position 4 drive diversity of antigen presentation by human leukocyte antigen class I molecules.

التفاصيل البيبلوغرافية
العنوان: Charge-based interactions through peptide position 4 drive diversity of antigen presentation by human leukocyte antigen class I molecules.
المؤلفون: Jackson KR; University of Texas MD Anderson Cancer Center, UTHealth Graduate School of Biomedical Sciences, Houston, TX, USA., Antunes DA; Department of Biology and Biochemistry, University of Houston, Houston, TX, USA., Talukder AH; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Maleki AR; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Amagai K; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Salmon A; University of Texas MD Anderson Cancer Center, UTHealth Graduate School of Biomedical Sciences, Houston, TX, USA., Katailiha AS; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Chiu Y; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Fasoulis R; Department of Computer Science, Rice University, Houston, TX, USA., Rigo MM; Department of Computer Science, Rice University, Houston, TX, USA., Abella JR; Department of Computer Science, Rice University, Houston, TX, USA., Melendez BD; University of Texas MD Anderson Cancer Center, UTHealth Graduate School of Biomedical Sciences, Houston, TX, USA., Li F; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Sun Y; University of Texas MD Anderson Cancer Center, UTHealth Graduate School of Biomedical Sciences, Houston, TX, USA., Sonnemann HM; University of Texas MD Anderson Cancer Center, UTHealth Graduate School of Biomedical Sciences, Houston, TX, USA., Belousov V; BostonGene Corporation, Waltham, MA, USA., Frenkel F; BostonGene Corporation, Waltham, MA, USA., Justesen S; Immunitrack Aps, Copenhagen, Denmark., Makaju A; ThermoFisher Scientific, San Jose, CA, USA., Liu Y; ThermoFisher Scientific, San Jose, CA, USA., Horn D; ThermoFisher Scientific, San Jose, CA, USA., Lopez-Ferrer D; ThermoFisher Scientific, San Jose, CA, USA., Huhmer AF; ThermoFisher Scientific, San Jose, CA, USA., Hwu P; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Roszik J; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA., Hawke D; Department of Systems Biology, UT MD Anderson Cancer Center, Houston, TX, USA., Kavraki LE; Department of Computer Science, Rice University, Houston, TX, USA., Lizée G; Department of Melanoma, UT MD Anderson Cancer Center, Houston, TX, USA.
المصدر: PNAS nexus [PNAS Nexus] 2022 Jul 27; Vol. 1 (3), pp. pgac124. Date of Electronic Publication: 2022 Jul 27 (Print Publication: 2022).
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Oxford University Press on behalf of the National Academy of Sciences Country of Publication: England NLM ID: 9918367777906676 Publication Model: eCollection Cited Medium: Internet ISSN: 2752-6542 (Electronic) Linking ISSN: 27526542 NLM ISO Abbreviation: PNAS Nexus Subsets: PubMed not MEDLINE
أسماء مطبوعة: Original Publication: [Oxford] : Oxford University Press on behalf of the National Academy of Sciences, [2022]-
مستخلص: Human leukocyte antigen class I (HLA-I) molecules bind and present peptides at the cell surface to facilitate the induction of appropriate CD8+ T cell-mediated immune responses to pathogen- and self-derived proteins. The HLA-I peptide-binding cleft contains dominant anchor sites in the B and F pockets that interact primarily with amino acids at peptide position 2 and the C-terminus, respectively. Nonpocket peptide-HLA interactions also contribute to peptide binding and stability, but these secondary interactions are thought to be unique to individual HLA allotypes or to specific peptide antigens. Here, we show that two positively charged residues located near the top of peptide-binding cleft facilitate interactions with negatively charged residues at position 4 of presented peptides, which occur at elevated frequencies across most HLA-I allotypes. Loss of these interactions was shown to impair HLA-I/peptide binding and complex stability, as demonstrated by both in vitro and in silico experiments. Furthermore, mutation of these Arginine-65 (R65) and/or Lysine-66 (K66) residues in HLA-A*02:01 and A*24:02 significantly reduced HLA-I cell surface expression while also reducing the diversity of the presented peptide repertoire by up to 5-fold. The impact of the R65 mutation demonstrates that nonpocket HLA-I/peptide interactions can constitute anchor motifs that exert an unexpectedly broad influence on HLA-I-mediated antigen presentation. These findings provide fundamental insights into peptide antigen binding that could broadly inform epitope discovery in the context of viral vaccine development and cancer immunotherapy.
(© The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences.)
References: Front Immunol. 2020 Nov 06;11:575076. (PMID: 33240264)
Nat Med. 2015 Aug;21(8):914-921. (PMID: 26193344)
Nucleic Acids Res. 2020 Jul 2;48(W1):W449-W454. (PMID: 32406916)
Mol Immunol. 2011 Jul;48(12-13):1461-7. (PMID: 21513985)
Science. 1992 Aug 14;257(5072):964-7. (PMID: 1380181)
J Biol Chem. 2018 Mar 2;293(9):3236-3251. (PMID: 29317506)
Brief Bioinform. 2021 Nov 5;22(6):. (PMID: 34009266)
Eur J Immunol. 1994 Oct;24(10):2357-63. (PMID: 7523137)
Cell. 1993 Sep 10;74(5):929-37. (PMID: 8104103)
Scand J Immunol. 1997 Aug;46(2):137-46. (PMID: 9583994)
Mol Immunol. 2019 Aug;112:274-282. (PMID: 31226552)
Proc Natl Acad Sci U S A. 1989 May;86(9):3296-300. (PMID: 2717617)
J Immunol. 1994 Apr 15;152(8):3913-24. (PMID: 8144960)
Nucleic Acids Res. 2015 Jan;43(Database issue):D423-31. (PMID: 25414341)
Nature. 1977 Apr 7;266(5602):544-5. (PMID: 300847)
J Comput Chem. 2004 Oct;25(13):1605-12. (PMID: 15264254)
J Immunol. 2014 Nov 15;193(10):4790-802. (PMID: 25311805)
Mol Immunol. 2007 Jan;44(4):322-31. (PMID: 16597462)
Eur J Immunol. 2006 Jan;36(1):170-9. (PMID: 16323248)
Sci Rep. 2020 Nov 24;10(1):20465. (PMID: 33235258)
Proc Natl Acad Sci U S A. 2020 Dec 1;117(48):30610-30618. (PMID: 33184174)
J Virol. 2010 Nov;84(22):11849-57. (PMID: 20844028)
Nat Rev Immunol. 2021 Feb;21(2):116-128. (PMID: 32820267)
Bioinformatics. 2013 Apr 1;29(7):845-54. (PMID: 23407358)
Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W665-7. (PMID: 15215472)
J Immunol. 2016 Sep 15;197(6):2492-9. (PMID: 27511729)
Nat Commun. 2020 Oct 21;11(1):5332. (PMID: 33087697)
Front Mol Biosci. 2017 Mar 10;4:13. (PMID: 28344973)
Nucleic Acids Res. 2000 Jan 1;28(1):235-42. (PMID: 10592235)
J Immunol. 2017 Oct 1;199(7):2203-2213. (PMID: 28923982)
Cell Syst. 2020 Jul 22;11(1):42-48.e7. (PMID: 32711842)
Nat Commun. 2015 Jul 02;6:7653. (PMID: 26134632)
Eur J Immunol. 1992 Aug;22(8):2085-91. (PMID: 1639105)
J Chem Theory Comput. 2018 Jun 12;14(6):2867-2880. (PMID: 29678106)
J Immunol. 1995 Jun 1;154(11):5951-8. (PMID: 7751638)
J Biol Chem. 2012 Apr 6;287(15):12267-76. (PMID: 22343629)
Nat Rev Immunol. 2003 Dec;3(12):952-61. (PMID: 14647477)
Biopolymers. 2000 Oct 15;54(5):318-27. (PMID: 10935972)
Eur J Immunol. 1992 Sep;22(9):2453-6. (PMID: 1516632)
PLoS Pathog. 2019 Nov 25;15(11):e1008122. (PMID: 31765434)
Proc Natl Acad Sci U S A. 2016 Mar 1;113(9):E1276-85. (PMID: 26884163)
Nature. 1974 Apr 19;248(5450):701-2. (PMID: 4133807)
Protein Sci. 2021 Jan;30(1):70-82. (PMID: 32881101)
J Biol Chem. 2005 Jun 24;280(25):23900-9. (PMID: 15849183)
Immunity. 2017 Feb 21;46(2):315-326. (PMID: 28228285)
J Chem Theory Comput. 2015 Jul 14;11(7):3346-56. (PMID: 26575768)
Nat Biotechnol. 2020 Feb;38(2):199-209. (PMID: 31844290)
J Exp Med. 1989 Sep 1;170(3):797-810. (PMID: 2788708)
Biophys J. 2015 Oct 20;109(8):1528-32. (PMID: 26488642)
Immunome Res. 2009 May 05;5:2. (PMID: 19416502)
J Exp Med. 2001 Mar 5;193(5):551-62. (PMID: 11238586)
J Immunol. 1995 Nov 1;155(9):4307-12. (PMID: 7594589)
J Immunol. 2004 May 15;172(10):6175-84. (PMID: 15128805)
Cancer Immunol Res. 2020 Mar;8(3):396-408. (PMID: 31871119)
J Mol Biol. 2012 Jan 13;415(2):429-42. (PMID: 22119720)
Nucleic Acids Res. 2019 Jan 8;47(D1):D339-D343. (PMID: 30357391)
J Allergy Clin Immunol. 2010 Feb;125(2 Suppl 2):S33-40. (PMID: 20061006)
Methods Mol Biol. 2017;1607:627-641. (PMID: 28573592)
J Immunol. 2002 Sep 15;169(6):3146-54. (PMID: 12218132)
Nat Immunol. 2008 Nov;9(11):1236-43. (PMID: 18836451)
Mol Immunol. 1992 Sep;29(9):1131-40. (PMID: 1379681)
Hum Vaccin Immunother. 2013 Jul;9(7):1577-86. (PMID: 23584251)
PLoS Comput Biol. 2017 Aug 23;13(8):e1005725. (PMID: 28832583)
Int Rev Immunol. 1991;7(2):129-38. (PMID: 1753176)
Cell Syst. 2018 Jul 25;7(1):129-132.e4. (PMID: 29960884)
J Chem Theory Comput. 2012 Sep 11;8(9):3257-3273. (PMID: 23341755)
J Biomol Screen. 2009 Feb;14(2):173-80. (PMID: 19196700)
Front Immunol. 2017 Oct 04;8:1210. (PMID: 29046675)
J Biol Chem. 2017 Mar 31;292(13):5262-5270. (PMID: 28179428)
Mol Cell Proteomics. 2017 Feb;16(2):181-193. (PMID: 27920218)
J Mol Biol. 2007 Oct 19;373(2):315-27. (PMID: 17825839)
Vaccine. 2008 Jul 23;26(31):3818-26. (PMID: 18582999)
Immunogenetics. 2015 Aug;67(8):425-36. (PMID: 26040913)
J Exp Med. 1989 Dec 1;170(6):2023-35. (PMID: 2479705)
Biochemistry. 1994 Jun 21;33(24):7736-43. (PMID: 8011638)
Nucleic Acids Res. 2012 Jul;40(Web Server issue):W281-7. (PMID: 22638583)
J Chem Theory Comput. 2011 Feb 8;7(2):525-37. (PMID: 26596171)
Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8403-7. (PMID: 1325657)
J Immunol. 1992 Mar 15;148(6):1871-8. (PMID: 1541825)
EMBO J. 1988 Jan;7(1):93-100. (PMID: 2452085)
Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3889-94. (PMID: 19234124)
J Med Chem. 2010 Oct 14;53(19):7061-6. (PMID: 20806940)
معلومات مُعتمدة: R21 CA209941 United States CA NCI NIH HHS; U01 CA258512 United States CA NCI NIH HHS
فهرسة مساهمة: Keywords: computational modeling; human leukocyte antigen (HLA); mass spectrometry; molecular dynamics; peptide antigen presentation
تواريخ الأحداث: Date Created: 20220825 Latest Revision: 20240214
رمز التحديث: 20240214
مُعرف محوري في PubMed: PMC9391200
DOI: 10.1093/pnasnexus/pgac124
PMID: 36003074
قاعدة البيانات: MEDLINE
الوصف
تدمد:2752-6542
DOI:10.1093/pnasnexus/pgac124