The human immune system recognizes neopeptides derived from mitochondrial DNA deletions

Journal of Immunology

Volumn 192, Issue 10, 2014, Pages 4581-4591

  Duvvuri, Bhargavi ^a   Duvvuri, Venkata R ^a   Wang, Chao ^b   Chen, Lina ^a   Wagar, Lisa E ^b   Jamnik, Veronica ^a   Wu, Jianhong ^a   Yeung, Rae S M ^b   Grigull, Jörg ^a   Watts, Tania H ^b   Wu, Gillian E ^a,c  

^a YORK UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF CANTERBURY   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HLA A ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOCHONDRIAL DNA;

ANTIGEN BINDING; ARTICLE; AUTOIMMUNITY; BACILLUS PUMILUS; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CROSS REACTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DNA SEQUENCE; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; IMMUNE RESPONSE; IMMUNOREACTIVITY; IMMUNOSURVEILLANCE; MEMORY T LYMPHOCYTE; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

ADULT; AGED; BACILLUS; BASE SEQUENCE; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSS REACTIONS; DNA, MITOCHONDRIAL; FEMALE; HLA-A2 ANTIGEN; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIAL PROTEINS; OLIGOPEPTIDES; SEQUENCE DELETION;

EID: 84901286398     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300774     Document Type: Article

References (67)

1. Anderson, S., A. T. Bankier, B. G. Barrell, M. H. de Bruijn, A. R. Coulson, J. Drouin, I. C. Eperon, D. P. Nierlich, B. A. Roe, F. Sanger, et al. 1981. Sequence and organization of the human mitochondrial genome. Nature 290: 457-465.
2. Legros, F., F. Malka, P. Frachon, A. Lombès, and M. Rojo. 2004. Organization and dynamics of human mitochondrial DNA. J. Cell Sci. 117: 2653-2662.
3. Loveland, B., C. R. Wang, H. Yonekawa, E. Hermel, and K. F. Lindahl. 1990. Maternally transmitted histocompatibility antigen of mice: a hydrophobic peptide of a mitochondrially encoded protein. Cell 60: 971-980.
4. Fischer Lindahl, K., E. Hermel, B. E. Loveland, and C. R. Wang. 1991. Maternally transmitted antigen of mice: a model transplantation antigen. Annu. Rev. Immunol. 9: 351-372.
5. Gray, M. W., G. Burger, and B. F. Lang. 1999. Mitochondrial evolution. Science 283: 1476-1481.
6. Timmis, J. N., M. A. Ayliffe, C. Y. Huang, and W. Martin. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5: 123-135.
7. Lindenborn-Fotinos, J., T. J. Sayers, and P. A. Berg. 1982. Mitochondrial antibodies in primary biliary cirrhosis. VI. Association of the complement fixing antigen with a component of the mitochondrial F1-ATPase complex. Clin. Exp. Immunol. 50: 267-274.
8. Lindenborn-Fotinos, J., H. Baum, and P. A. Berg. 1985. Mitochondrial antibodies in primary biliary cirrhosis: species and nonspecies specific determinants of M2 antigen. Hepatology 5: 763-769.
9. Yakes, F. M., and B. Van Houten. 1997. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc. Natl. Acad. Sci. USA 94: 514-519.
10. Zastawny, T. H., M. Dabrowska, T. Jaskolski, M. Klimarczyk, L. Kulinski, A. Koszela, M. Szczesniewicz, M. Sliwinska, P. Witkowski, and R. Olinski. 1998. Comparison of oxidative base damage in mitochondrial and nuclear DNA. Free Radic. Biol. Med. 24: 722-725.
11. Guo, X., K. Y. Popadin, N. Markuzon, Y. L. Orlov, Y. Kraytsberg, K. J. Krishnan, G. Zsurka, D. M. Turnbull, W. S. Kunz, and K. Khrapko. 2010. Repeats, longevity and the sources of mtDNA deletions: evidence from "deletional spectra". Trends Genet. 26: 340-343.
12. Cortopassi, G. A., D. Shibata, N. W. Soong, and N. Arnheim. 1992. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl. Acad. Sci. USA 89: 7370-7374.
13. Reeve, A. K., K. J. Krishnan, and D. Turnbull. 2008. Mitochondrial DNA mutations in disease, aging, and neurodegeneration. Ann. N. Y. Acad. Sci. 1147: 21-29.
14. Larsson, N. G. 2010. Somatic mitochondrial DNA mutations in mammalian aging. Annu. Rev. Biochem. 79: 683-706.
15. Craig, I. 1975. Letter: Mitochondria, autoimmunity, and oncogenesis. Lancet 305: 218-219.
16. Gu, Y., C. Wang, C. M. Roifman, and A. Cohen. 2003. Role of MHC class I in immune surveillance of mitochondrial DNA integrity. J. Immunol. 170: 3603-3607.
17. Da Sylva, T. R., A. Connor, Y. Mburu, E. Keystone, and G. E. Wu. 2005. Somatic mutations in the mitochondria of rheumatoid arthritis synoviocytes. Arthritis Res. Ther. 7: R844-R851.
18. Campbell, G. R., I. Ziabreva, A. K. Reeve, K. J. Krishnan, R. Reynolds, O. Howell, H. Lassmann, D. M. Turnbull, and D. J. Mahad. 2011. Mitochondrial DNA deletions and neurodegeneration in multiple sclerosis. Ann. Neurol. 69: 481-492.
19. Ruiz-Pesini, E., M. T. Lott, V. Procaccio, J. C. Poole, M. C. Brandon, D. Mishmar, C. Yi, J. Kreuziger, P. Baldi, and D. C. Wallace. 2007. An enhanced MITOMAP with a global mtDNA mutational phylogeny. Nucleic Acids Res. 35 (Database issue): D823-D828.
20. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanović. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
21. Nielsen, M., C. Lundegaard, O. Lund, and C. Keşmir. 2005. The role of the proteasome in generating cytotoxic T-cell epitopes: insights obtained from improved predictions of proteasomal cleavage. Immunogenetics 57: 33-41.
22. Reche, P. A., J. P. Glutting, and E. L. Reinherz. 2002. Prediction of MHC class I binding peptides using profile motifs. Hum. Immunol. 63: 701-709.
23. Nielsen, M., C. Lundegaard, T. Blicher, K. Lamberth, M. Harndahl, S. Justesen, G. Røder, B. Peters, A. Sette, O. Lund, and S. Buus. 2007. NetMHCpan, a method for quantitative predictions of peptide binding to any HLA-A and -B locus protein of known sequence. PLoS ONE 2: e796.
24. Henderson, R. A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D. F. Hunt, and V. H. Engelhard. 1992. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 255: 1264-1266.
25. Luft, T., M. Rizkalla, T. Y. Tai, Q. Chen, R. I. MacFarlan, I. D. Davis, E. Maraskovsky, and J. Cebon. 2001. Exogenous peptides presented by transporter associated with antigen processing (TAP)-deficient and TAP-competent cells: intracellular loading and kinetics of presentation. J. Immunol. 167: 2529-2537.
26. Bukczynski, J., T. Wen, K. Ellefsen, J. Gauldie, and T. H. Watts. 2004. Costimulatory ligand 4-1BBL (CD137L) as an efficient adjuvant for human antiviral cytotoxic T cell responses. Proc. Natl. Acad. Sci. USA 101: 1291-1296.
27. Williams, D. S., M. J. Bird, R. N. Jorissen, Y. L. Yu, F. Walker, H. H. Zhang, E. C. Nice, and A. W. Burgess. 2010. Nonsense mediated decay resistant mutations are a source of expressed mutant proteins in colon cancer cell lines with microsatellite instability. PLoS ONE 5: e16012.
28. Hamann, D., P. A. Baars, M. H. Rep, B. Hooibrink, S. R. Kerkhof-Garde, M. R. Klein, and R. A. van Lier. 1997. Phenotypic and functional separation of memory and effector human CD8+ T cells. J. Exp. Med. 186: 1407-1418.
29. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
30. Mallard, E., F. Vernel-Pauillac, T. Velu, F. Lehmann, J. P. Abastado, M. Salcedo, and N. Bercovici. 2004. IL-2 production by virus- and tumor-specific human CD8 T cells is determined by their fine specificity. J. Immunol. 172: 3963-3970.
31. Priest, F. G. 1993. Systematics and ecology of Bacillus. In Bacillus subtilis and Other Gram-Positive Bacteria: Biochemistry, Physiology, and Molecular Genetics. A. L. Sonenshein, J. A. Hoch, and R. Losick, eds. ASM Press, Washington, D.C., p. 3-16.
32. Kimouli, M., G. Vrioni, M. Papadopoulou, V. Koumaki, D. Petropoulou, A. Gounaris, A. W. Friedrich, and A. Tsakris. 2012. Two cases of severe sepsis caused by Bacillus pumilus in neonatal infants. J. Med. Microbiol. 61: 596-599.
33. Mannella, C. A. 1992. The "ins" and "outs" of mitochondrial membrane channels. Trends Biochem. Sci. 17: 315-320.
34. Hill, K., K. Model, M. T. Ryan, K. Dietmeier, F. Martin, R. Wagner, and N. Pfanner. 1998. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 395: 516-521.
35. Dengjel, J., O. Schoor, R. Fischer, M. Reich, M. Kraus, M. Muller, K. Kreymborg, F. Altenberend, J. Brandenburg, H. Kalbacher, et al. 2005. Autophagy promotes MHC class II presentation of peptides from intracellular source proteins. Proc. Natl. Acad. Sci. USA 102: 7922-7927.
36. Levine, B., and V. Deretic. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nat. Rev. Immunol. 7: 767-777.
37. Crotzer, V. L., and J. S. Blum. 2009. Autophagy and its role in MHC-mediated antigen presentation. J. Immunol. 182: 3335-3341.
38. Nedjic, J., M. Aichinger, J. Emmerich, N. Mizushima, and L. Klein. 2008. Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455: 396-400.
39. Levine, B., N. Mizushima, and H. W. Virgin. 2011. Autophagy in immunity and inflammation. Nature 469: 323-335.
40. Aichinger, M., C. Wu, J. Nedjic, and L. Klein. 2013. Macroautophagy substrates are loaded onto MHC class II of medullary thymic epithelial cells for central tolerance. J. Exp. Med. 210: 287-300.
41. Schon, E. A., R. Rizzuto, C. T. Moraes, H. Nakase, M. Zeviani, and S. DiMauro. 1989. A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA. Science 244: 346-349.
42. Samuels, D. C., E. A. Schon, and P. F. Chinnery. 2004. Two direct repeats cause most human mtDNA deletions. Trends Genet. 20: 393-398.
43. Khaidakov, M., E. R. Siegel, and R. J. Shmookler Reis. 2006. Direct repeats in mitochondrial DNA and mammalian lifespan. Mech. Ageing Dev. 127: 808-812.
44. Almasan, A., and N. C. Mishra. 1991. Recombination by sequence repeats with formation of suppressive or residual mitochondrial DNA in Neurospora. Proc. Natl. Acad. Sci. USA 88: 7684-7688.
45. Robberson, D. L., and D. A. Clayton. 1972. Replication of mitochondrial DNA in mouse L cells and their thymidine kinase2 derivatives: displacement replication on a covalently-closed circular template. Proc. Natl. Acad. Sci. USA 69: 3810-3814.
46. Yasukawa, T., A. Reyes, T. J. Cluett, M. Y. Yang, M. Bowmaker, H. T. Jacobs, and I. J. Holt. 2006. Replication of vertebrate mitochondrial DNA entails transient ribonucleotide incorporation throughout the lagging strand. EMBO J. 25: 5358-5371.
47. Holt, I. J., H. E. Lorimer, and H. T. Jacobs. 2000. Coupled leading- and laggingstrand synthesis of mammalian mitochondrial DNA. Cell 100: 515-524.
48. Krishnan, K. J., A. K. Reeve, D. C. Samuels, P. F. Chinnery, J. K. Blackwood, R. W. Taylor, S. Wanrooij, J. N. Spelbrink, R. N. Lightowlers, and D. M. Turnbull. 2008. What causes mitochondrial DNA deletions in human cells?. Nat. Genet. 40: 275-279.
49. Nakase, H., C. T. Moraes, R. Rizzuto, A. Lombes, S. DiMauro, and E. A. Schon. 1990. Transcription and translation of deleted mitochondrial genomes in Kearns- Sayre syndrome: implications for pathogenesis. Am. J. Hum. Genet. 46: 418-427.
50. Nakada, K., K. Inoue, T. Ono, K. Isobe, A. Ogura, Y. I. Goto, I. Nonaka, and J. I. Hayashi. 2001. Inter-mitochondrial complementation: mitochondria-specific system preventing mice from expression of disease phenotypes by mutant mtDNA. Nat. Med. 7: 934-940.
51. Gilkerson, R. W., E. A. Schon, E. Hernandez, and M. M. Davidson. 2008. Mitochondrial nucleoids maintain genetic autonomy but allow for functional complementation. J. Cell Biol. 181: 1117-1128.
52. Chang, Y. F., J. S. Imam, and M. F. Wilkinson. 2007. The nonsense-mediated decay RNA surveillance pathway. Annu. Rev. Biochem. 76: 51-74.
53. Zhang, J., X. Sun, Y. Qian, J. P. LaDuca, and L. E. Maquat. 1998. At least one intron is required for the nonsense-mediated decay of triosephosphate isomerase mRNA: a possible link between nuclear splicing and cytoplasmic translation. Mol. Cell. Biol. 18: 5272-5283.
54. Thermann, R., G. Neu-Yilik, A. Deters, U. Frede, K. Wehr, C. Hagemeier, M. W. Hentze, and A. E. Kulozik. 1998. Binary specification of nonsense codons by splicing and cytoplasmic translation. EMBO J. 17: 3484-3494.
55. Nagy, E., and L. E. Maquat. 1998. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23: 198-199.
56. Tiranti, V., P. Corona, M. Greco, J. W. Taanman, F. Carrara, E. Lamantea, L. Nijtmans, G. Uziel, and M. Zeviani. 2000. A novel frameshift mutation of the mtDNA COIII gene leads to impaired assembly of cytochrome c oxidase in a patient affected by Leigh-like syndrome. Hum. Mol. Genet. 9: 2733-2742.
57. Brower, R. C., R. England, T. Takeshita, S. Kozlowski, D. H. Margulies, J. A. Berzofsky, and C. Delisi. 1994. Minimal requirements for peptide mediated activation of CD8+ CTL. Mol. Immunol. 31: 1285-1293.
58. Sykulev, Y., R. J. Cohen, and H. N. Eisen. 1995. The law of mass action governs antigen-stimulated cytolytic activity of CD8+ cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 92: 11990-11992.
59. Sykulev, Y., M. Joo, I. Vturina, T. J. Tsomides, and H. N. Eisen. 1996. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4: 565-571.
60. Wallace, D. C. 2010. Mitochondrial DNA mutations in disease and aging. Environ. Mol. Mutagen. 51: 440-450.
61. Dolfi, D. V., K. D. Mansfield, A. M. Polley, S. A. Doyle, G. J. Freeman, H. Pircher, K. E. Schmader, and E. J. Wherry. 2013. Increased T-bet is associated with senescence of influenza virus-specific CD8 T cells in aged humans. J. Leukoc. Biol. 93: 825-836.
62. Zhang, Q., M. Raoof, Y. Chen, Y. Sumi, T. Sursal, W. Junger, K. Brohi, K. Itagaki, and C. J. Hauser. 2010. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107.
63. Krysko, D. V., P. Agostinis, O. Krysko, A. D. Garg, C. Bachert, B. N. Lambrecht, and P. Vandenabeele. 2011. Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol. 32: 157-164.
64. Mirabella, M., S. Di Giovanni, G. Silvestri, P. Tonali, and S. Servidei. 2000. Apoptosis in mitochondrial encephalomyopathies with mitochondrial DNA mutations: a potential pathogenic mechanism. Brain 123: 93-104.
65. Asoh, S., T. Mori, J. Hayashi, and S. Ohta. 1996. Expression of the apoptosismediator Fas is enhanced by dysfunctional mitochondria. J. Biochem. 120: 600-607.
66. Collins, L. V., S. Hajizadeh, E. Holme, I. M. Jonsson, and A. Tarkowski. 2004. Endogenously oxidized mitochondrial DNA induces in vivo and in vitro inflammatory responses. J. Leukoc. Biol. 75: 995-1000.
67. Hajizadeh, S., J. DeGroot, J. M. TeKoppele, A. Tarkowski, and L. V. Collins. 2003. Extracellular mitochondrial DNA and oxidatively damaged DNA in synovial fluid of patients with rheumatoid arthritis. Arthritis Res. Ther. 5: R234- R240.