Citrullinated α-enolase is an effective target for anti-cancer immunity

References

• Pardoll DM, Topalian SL. The role of CD4+ T cell responses in antitumor immunity. Curr Opin Immunol. 1998;10:588–94. doi:10.1016/S0952-7915(98)80228-8. PMID:9794842.
   PubMed Web of Science ®Google Scholar
• Quezada SA, Peggs KS. Tumor-reactive CD4+ T cells: plasticity beyond helper and regulatory activities. Immunotherapy. 2011;3:915–7. doi:10.2217/imt.11.83. PMID:21843076.
   PubMed Web of Science ®Google Scholar
• Hung K, Hayashi R, Lafond-Walker A, Lowenstein C, Pardoll D, Levitsky H. The central role of CD4(+) T cells in the antitumor immune response. J Exp Med. 1998;188:2357–68. doi:10.1084/jem.188.12.2357. PMID:9858522.
   PubMed Web of Science ®Google Scholar
• Ossendorp F, Mengede E, Camps M, Filius R, Melief CJ. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. J Exp Med. 1998;187:693–702. doi:10.1084/jem.187.5.693. PMID:9480979.
   PubMed Web of Science ®Google Scholar
• Xie Y, Akpinarli A, Maris C, Hipkiss EL, Lane M, Kwon EK, Muranski P, Restifo NP, Antony PA. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J Exp Med. 2010;207:651–67. doi:10.1084/jem.20091921. PMID:20156973.
   PubMed Web of Science ®Google Scholar
• Hirschhorn-Cymerman D, Budhu S, Kitano S, Liu C, Zhao F, Zhong H, Lesokhin AM, Avogadri-Connors F, Yuan J, Li Y, et al. Induction of tumoricidal function in CD4+ T cells is associated with concomitant memory and terminally differentiated phenotype. J Exp Med. 2012;209:2113–26. doi:10.1084/jem.20120532. PMID:23008334.
   PubMed Web of Science ®Google Scholar
• Qui HZ, Hagymasi AT, Bandyopadhyay S, St Rose MC, Ramanarasimhaiah R, Menoret A, Mittler RS, Gordon SM, Reiner SL, Vella AT, et al. CD134 plus CD137 dual costimulation induces Eomesodermin in CD4 T cells to program cytotoxic Th1 differentiation. J Immunol. 2011;187:3555–64. doi:10.4049/jimmunol.1101244. PMID:21880986.
   PubMed Web of Science ®Google Scholar
• Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J, Lin JC, Teer JK, Cliften P, Tycksen E, et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med. 2013;19:747–52. doi:10.1038/nm.3161. PMID:23644516.
   PubMed Web of Science ®Google Scholar
• Linnemann C, van Buuren MM, Bies L, Verdegaal EM, Schotte R, Calis JJ, Behjati S, Velds A, Hilkmann H, Atmioui DE, et al. High-throughput epitope discovery reveals frequent recognition of neo-antigens by CD4+ T cells in human melanoma. Nat Med. 2015;21:81–5. doi:10.1038/nm.3773. PMID:25531942.
   PubMed Web of Science ®Google Scholar
• Lipinski KA, Barber LJ, Davies MN, Ashenden M, Sottoriva A, Gerlinger M. Cancer evolution and the limits of predictability in precision cancer medicine. Trends Cancer. 2016;2:49–63. doi:10.1016/j.trecan.2015.11.003. PMID:26949746.
   PubMed Web of Science ®Google Scholar
• Witalison EE, Thompson PR, Hofseth LJ. Protein arginine deiminases and associated citrullination: physiological functions and diseases associated with dysregulation. Curr Drug Targets. 2015;16:700–10. doi:10.2174/1389450116666150202160954. PMID:25642720.
   PubMed Web of Science ®Google Scholar
• Ireland JM, Unanue ER. Autophagy in antigen-presenting cells results in presentation of citrullinated peptides to CD4 T cells. J Exp Med. 2011;208:2625–32. doi:10.1084/jem.20110640. PMID:22162830.
   PubMed Web of Science ®Google Scholar
• Durrant LG, Metheringham RL, Brentville VA. Autophagy, citrullination and cancer. Autophagy. 2016;12:1055–6. doi:10.1080/15548627.2016.1166326. PMID:27145231.
   PubMed Web of Science ®Google Scholar
• Marino ML, Pellegrini P, Di Lernia G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hägg M, Linder S, Fais S, Codogno P, et al. Autophagy is a protective mechanism for human melanoma cells under acidic stress. J Biol Chem. 2012;287:30664–76. doi:10.1074/jbc.M112.339127. PMID:22761435.
   PubMed Web of Science ®Google Scholar
• Brentville VA, Metheringham RL, Gunn B, Symonds P, Daniels I, Gijon M, Cook K, Xue W, Durrant LG. Citrullinated vimentin presented on MHC-II in tumor cells is a target for CD4+ T-cell-mediated antitumor immunity. Cancer Res. 2016;76:548–60. doi:10.1158/0008-5472.CAN-15-1085. PMID:26719533.
   PubMed Web of Science ®Google Scholar
• Miles LA, Dahlberg CM, Plescia J, Felez J, Kato K, Plow EF. Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry. 1991;30:1682–91. doi:10.1021/bi00220a034. PMID:1847072.
   PubMed Web of Science ®Google Scholar
• Zhao M, Fang W, Wang Y, Guo S, Shu L, Wang L, Chen Y, Fu Q, Liu Y, Hua S, et al. Enolase-1 is a therapeutic target in endometrial carcinoma. Oncotarget. 2015;6:15610–27. doi:10.18632/oncotarget.3639. PMID:25951350.
   PubMed Web of Science ®Google Scholar
• Cappello P, Tomaino B, Chiarle R, Ceruti P, Novarino A, Castagnoli C, Migliorini P, Perconti G, Giallongo A, Milella M, et al. An integrated humoral and cellular response is elicited in pancreatic cancer by alpha-enolase, a novel pancreatic ductal adenocarcinoma-associated antigen. Int J Cancer. 2009;125:639–48. doi:10.1002/ijc.24355. PMID:19425054.
   PubMed Web of Science ®Google Scholar
• Fu QF, Liu Y, Fan Y, Hua SN, Qu HY, Dong SW, Li RL, Zhao MY, Zhen Y, Yu XL, et al. Alpha-enolase promotes cell glycolysis, growth, migration, and invasion in non-small cell lung cancer through FAK-mediated PI3 K/AKT pathway. J Hematol Oncol. 2015;8:22. doi:10.1186/s13045-015-0117-5. PMID:25887760.
   PubMed Web of Science ®Google Scholar
• Principe M, Ceruti P, Shih NY, Chattaragada MS, Rolla S, Conti L, Bestagno M, Zentilin L, Yang SH, Migliorini P, et al. Targeting of surface alpha-enolase inhibits the invasiveness of pancreatic cancer cells. Oncotarget. 2015;6:11098–113. doi:10.18632/oncotarget.3572. PMID:25860938.
   PubMed Web of Science ®Google Scholar
• Lundberg K, Kinloch A, Fisher BA, Wegner N, Wait R, Charles P, Mikuls TR, Venables PJ. Antibodies to citrullinated alpha-enolase peptide 1 are specific for rheumatoid arthritis and cross-react with bacterial enolase. Arthritis Rheum. 2008;58:3009–19. doi:10.1002/art.23936. PMID:18821669.
   PubMed Web of Science ®Google Scholar
• Gerstner C, Dubnovitsky A, Sandin C, Kozhukh G, Uchtenhagen H, James EA, Rönnelid J, Ytterberg AJ, Pieper J, Reed E, et al. Functional and Structural Characterization of a Novel HLA-DRB1#04:01-Restricted alpha-Enolase T Cell Epitope in Rheumatoid Arthritis. Front Immunol. 2016;7:494. doi:10.3389/fimmu.2016.00494. PMID:27895642.
   PubMed Web of Science ®Google Scholar
• Hill JA, Southwood S, Sette A, Jevnikar AM, Bell DA, Cairns E. Cutting edge: the conversion of arginine to citrulline allows for a high-affinity peptide interaction with the rheumatoid arthritis-associated HLA-DRB1#0401 MHC class II molecule. J Immunol. 2003;171:538–41. doi:10.4049/jimmunol.171.2.538. PMID:12847215.
   PubMed Web of Science ®Google Scholar
• James EA, Moustakas AK, Bui J, Papadopoulos GK, Bondinas G, Buckner JH, Kwok WW. HLA-DR1001 presents “altered-self” peptides derived from joint-associated proteins by accepting citrulline in three of its binding pockets. Arthritis Rheum. 2010;62:2909–18. doi:10.1002/art.27594. PMID:20533291.
   PubMed Web of Science ®Google Scholar
• Catalan D, Aravena O, Zuniga R, Silva N, Escobar A, Sabugo F, Wurmann P, Soto L, González R, Alfaro J, et al. Weak CD4+ T-cell responses to citrullinated vimentin in rheumatoid arthritis patients carrying HLA-DR9 alleles. Rheumatol Int. 2012;32:1819–25. doi:10.1007/s00296-011-2039-z. PMID:21769486.
   PubMed Web of Science ®Google Scholar
• Kampstra AS, van Heemst J, Moustakas AK, Papadopoulos GK, Huizinga TW, Toes RE. The increased ability to present citrullinated peptides is not unique to HLA-SE molecules: arginine-to-citrulline conversion also enhances peptide affinity for HLA-DQ molecules. Arthritis Res Ther. 2016;18:254. doi:10.1186/s13075-016-1153-4. PMID:27809896.
   PubMed Web of Science ®Google Scholar
• James EA, Rieck M, Pieper J, Gebe JA, Yue BB, Tatum M, Peda M, Sandin C, Klareskog L, Malmström V, et al. Citrulline-specific Th1 cells are increased in rheumatoid arthritis and their frequency is influenced by disease duration and therapy. Arthritis Rheumatol. 2014;66:1712–22. doi:10.1002/art.38637. PMID:24665079.
   PubMed Web of Science ®Google Scholar
• Cappello P, Rolla S, Chiarle R, Principe M, Cavallo F, Perconti G, Feo S, Giovarelli M, Novelli F. Vaccination with ENO1 DNA prolongs survival of genetically engineered mice with pancreatic cancer. Gastroenterology. 2013;144:1098–106. doi:10.1053/j.gastro.2013.01.020. PMID:23333712.
   PubMed Web of Science ®Google Scholar
• Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford). 2012;51(Suppl 5):v3–11. doi:10.1093/rheumatology/kes113. PMID:22718924.
   PubMed Web of Science ®Google Scholar
• Grunewald J, Eklund A. Role of CD4+ T cells in sarcoidosis. Proc Am Thorac Soc. 2007;4:461–4. doi:10.1513/pats.200606-130MS. PMID:17684290.
   PubMedGoogle Scholar
• Coimbra S, Figueiredo A, Castro E, Rocha-Pereira P, Santos-Silva A. The roles of cells and cytokines in the pathogenesis of psoriasis. Int J Dermatol. 2012;51:389–95; quiz 95-8. doi:10.1111/j.1365-4632.2011.05154.x. PMID:22435425.
   PubMed Web of Science ®Google Scholar
• Holmdahl R, Klareskog L, Rubin K, Larsson E, Wigzell H. T lymphocytes in collagen II-induced arthritis in mice. Characterization of arthritogenic collagen II-specific T-cell lines and clones. Scand J Immunol. 1985;22:295–306. doi:10.1111/j.1365-3083.1985.tb01884.x. PMID:2413528.
   PubMed Web of Science ®Google Scholar