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A Recurrent Mutation in Anaplastic Lymphoma Kinase with Distinct Neoepitope Conformations.

Toor JS, Rao AA, McShan AC, Yarmarkovich M, Nerli S, Yamaguchi K, Madejska AA, Nguyen S, Tripathi S, Maris JM, Salama SR, Haussler D, Sgourakis NG
Front Immunol 9 99 (2018)
Related entries: 5txs, 5vz5

Cited: 28 times
EuropePMC logo PMID: 29441070

Abstract

The identification of recurrent human leukocyte antigen (HLA) neoepitopes driving T cell responses against tumors poses a significant bottleneck in the development of approaches for precision cancer therapeutics. Here, we employ a bioinformatics method, Prediction of T Cell Epitopes for Cancer Therapy, to analyze sequencing data from neuroblastoma patients and identify a recurrent anaplastic lymphoma kinase mutation (ALK R1275Q) that leads to two high affinity neoepitopes when expressed in complex with common HLA alleles. Analysis of the X-ray structures of the two peptides bound to HLA-B*15:01 reveals drastically different conformations with measurable changes in the stability of the protein complexes, while the self-epitope is excluded from binding due to steric hindrance in the MHC groove. To evaluate the range of HLA alleles that could display the ALK neoepitopes, we used structure-based Rosetta comparative modeling calculations, which accurately predict several additional high affinity interactions and compare our results with commonly used prediction tools. Subsequent determination of the X-ray structure of an HLA-A*01:01 bound neoepitope validates atomic features seen in our Rosetta models with respect to key residues relevant for MHC stability and T cell receptor recognition. Finally, MHC tetramer staining of peripheral blood mononuclear cells from HLA-matched donors shows that the two neoepitopes are recognized by CD8+ T cells. This work provides a rational approach toward high-throughput identification and further optimization of putative neoantigen/HLA targets with desired recognition features for cancer immunotherapy.

Reviews - 6at9 mentioned but not cited (1)

  1. Advances in Computational and Bioinformatics Tools and Databases for Designing and Developing a Multi-Epitope-Based Peptide Vaccine. Shawan MMAK, Sharma AR, Halder SK, Arian TA, Shuvo MN, Sarker SR, Hasan MA. Int J Pept Res Ther 29 60 (2023)

Articles - 6at9 mentioned but not cited (10)

  1. Epitope-based peptide vaccines predicted against novel coronavirus disease caused by SARS-CoV-2. Lin L, Ting S, Yufei H, Wendong L, Yubo F, Jing Z. Virus Res 288 198082 (2020)
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  3. A Recurrent Mutation in Anaplastic Lymphoma Kinase with Distinct Neoepitope Conformations. Toor JS, Rao AA, McShan AC, Yarmarkovich M, Nerli S, Yamaguchi K, Madejska AA, Nguyen S, Tripathi S, Maris JM, Salama SR, Haussler D, Sgourakis NG. Front Immunol 9 99 (2018)
  4. Backbone-independent NMR resonance assignments of methyl probes in large proteins. Nerli S, De Paula VS, McShan AC, Sgourakis NG. Nat Commun 12 691 (2021)
  5. Human leukocyte antigen class-I variation is associated with atopic dermatitis: A case-control study. Margolis DJ, Mitra N, Duke JL, Berna R, Margolis JD, Hoffstad O, Kim BS, Yan AC, Zaenglein AL, Chiesa Fuxench Z, Dinou A, Wasserman J, Tairis N, Mosbruger TL, Ferriola D, Damianos G, Kotsopoulou I, Monos DS. Hum Immunol 82 593-599 (2021)
  6. Combined presentation and immunogenicity analysis reveals a recurrent RAS.Q61K neoantigen in melanoma. Peri A, Greenstein E, Alon M, Pai JA, Dingjan T, Reich-Zeliger S, Barnea E, Barbolin C, Levy R, Arnedo-Pac C, Kalaora S, Dassa B, Feldmesser E, Shang P, Greenberg P, Levin Y, Benedek G, Levesque MP, Adams DJ, Lotem M, Wilmott JS, Scolyer RA, Jönsson GB, Admon A, Rosenberg SA, Cohen CJ, Niv MY, Lopez-Bigas N, Satpathy AT, Friedman N, Samuels Y. J Clin Invest 131 e129466 (2021)
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  8. A Systematic Immuno-Informatic Approach to Design a Multiepitope-Based Vaccine Against Emerging Multiple Drug Resistant Serratia marcescens. Damas MSF, Mazur FG, Freire CCM, da Cunha AF, Pranchevicius MDS. Front Immunol 13 768569 (2022)
  9. Immunoinformatics Approach to Design a Multi-Epitope Nanovaccine against Leishmania Parasite: Elicitation of Cellular Immune Responses. Margaroni M, Agallou M, Tsanaktsidou E, Kammona O, Kiparissides C, Karagouni E. Vaccines (Basel) 11 304 (2023)
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Reviews citing this publication (4)

  1. Macromolecular modeling and design in Rosetta: recent methods and frameworks. Leman JK, Weitzner BD, Lewis SM, Adolf-Bryfogle J, Alam N, Alford RF, Aprahamian M, Baker D, Barlow KA, Barth P, Basanta B, Bender BJ, Blacklock K, Bonet J, Boyken SE, Bradley P, Bystroff C, Conway P, Cooper S, Correia BE, Coventry B, Das R, De Jong RM, DiMaio F, Dsilva L, Dunbrack R, Ford AS, Frenz B, Fu DY, Geniesse C, Goldschmidt L, Gowthaman R, Gray JJ, Gront D, Guffy S, Horowitz S, Huang PS, Huber T, Jacobs TM, Jeliazkov JR, Johnson DK, Kappel K, Karanicolas J, Khakzad H, Khar KR, Khare SD, Khatib F, Khramushin A, King IC, Kleffner R, Koepnick B, Kortemme T, Kuenze G, Kuhlman B, Kuroda D, Labonte JW, Lai JK, Lapidoth G, Leaver-Fay A, Lindert S, Linsky T, London N, Lubin JH, Lyskov S, Maguire J, Malmström L, Marcos E, Marcu O, Marze NA, Meiler J, Moretti R, Mulligan VK, Nerli S, Norn C, Ó'Conchúir S, Ollikainen N, Ovchinnikov S, Pacella MS, Pan X, Park H, Pavlovicz RE, Pethe M, Pierce BG, Pilla KB, Raveh B, Renfrew PD, Burman SSR, Rubenstein A, Sauer MF, Scheck A, Schief W, Schueler-Furman O, Sedan Y, Sevy AM, Sgourakis NG, Shi L, Siegel JB, Silva DA, Smith S, Song Y, Stein A, Szegedy M, Teets FD, Thyme SB, Wang RY, Watkins A, Zimmerman L, Bonneau R. Nat Methods 17 665-680 (2020)
  2. Targets and Antibody Formats for Immunotherapy of Neuroblastoma. Park JA, Cheung NV. J Clin Oncol 38 1836-1848 (2020)
  3. Emerging Roles of ALK in Immunity and Insights for Immunotherapy. Wang L, Lui VWY. Cancers (Basel) 12 E426 (2020)
  4. Computational Methods in Immunology and Vaccinology: Design and Development of Antibodies and Immunogens. Guarra F, Colombo G. J Chem Theory Comput 19 5315-5333 (2023)

Articles citing this publication (13)

  1. Cross-HLA targeting of intracellular oncoproteins with peptide-centric CARs. Yarmarkovich M, Marshall QF, Warrington JM, Premaratne R, Farrel A, Groff D, Li W, di Marco M, Runbeck E, Truong H, Toor JS, Tripathi S, Nguyen S, Shen H, Noel T, Church NL, Weiner A, Kendsersky N, Martinez D, Weisberg R, Christie M, Eisenlohr L, Bosse KR, Dimitrov DS, Stevanovic S, Sgourakis NG, Kiefel BR, Maris JM. Nature 599 477-484 (2021)
  2. Structure Based Prediction of Neoantigen Immunogenicity. Riley TP, Keller GLJ, Smith AR, Davancaze LM, Arbuiso AG, Devlin JR, Baker BM. Front Immunol 10 2047 (2019)
  3. Molecular determinants of chaperone interactions on MHC-I for folding and antigen repertoire selection. McShan AC, Devlin CA, Overall SA, Park J, Toor JS, Moschidi D, Flores-Solis D, Choi H, Tripathi S, Procko E, Sgourakis NG. Proc Natl Acad Sci U S A 116 25602-25613 (2019)
  4. Structural dissimilarity from self drives neoepitope escape from immune tolerance. Devlin JR, Alonso JA, Ayres CM, Keller GLJ, Bobisse S, Vander Kooi CW, Coukos G, Gfeller D, Harari A, Baker BM. Nat Chem Biol 16 1269-1276 (2020)
  5. Peptide presentation by bat MHC class I provides new insight into the antiviral immunity of bats. Lu D, Liu K, Zhang D, Yue C, Lu Q, Cheng H, Wang L, Chai Y, Qi J, Wang LF, Gao GF, Liu WJ. PLoS Biol 17 e3000436 (2019)
  6. ProTECT-Prediction of T-Cell Epitopes for Cancer Therapy. Rao AA, Madejska AA, Pfeil J, Paten B, Salama SR, Haussler D. Front Immunol 11 483296 (2020)
  7. A common allele of HLA is associated with asymptomatic SARS-CoV-2 infection. Augusto DG, Murdolo LD, Chatzileontiadou DSM, Sabatino JJ, Yusufali T, Peyser ND, Butcher X, Kizer K, Guthrie K, Murray VW, Pae V, Sarvadhavabhatla S, Beltran F, Gill GS, Lynch KL, Yun C, Maguire CT, Peluso MJ, Hoh R, Henrich TJ, Deeks SG, Davidson M, Lu S, Goldberg SA, Kelly JD, Martin JN, Vierra-Green CA, Spellman SR, Langton DJ, Dewar-Oldis MJ, Smith C, Barnard PJ, Lee S, Marcus GM, Olgin JE, Pletcher MJ, Maiers M, Gras S, Hollenbach JA. Nature 620 128-136 (2023)
  8. Case Reports Complete Response to PD-1 Inhibition in an Adolescent With Relapsed Clear Cell Adenocarcinoma of the Cervix Predicted by Neoepitope Burden and APOBEC Signature. Levinson A, Lee AG, Martell HJ, Breese MR, Zaloudek C, Van Ziffle J, Laguna B, Leung SG, Chen MD, Chen LM, Pfeil J, Ladwig NR, Shah AT, Behroozfard I, Rao AA, Salama SR, Sweet-Cordero EA, Stieglitz E. JCO Precis Oncol 4 PO.20.00132 (2020)
  9. Deciphering the selective binding mechanisms of anaplastic lymphoma kinase-derived neuroblastoma tumor neoepitopes to human leukocyte antigen. Tian W, Liu X, Wang L, Zheng B, Jiang K, Fu G, Feng W. J Mol Model 27 134 (2021)
  10. HLA3DB: comprehensive annotation of peptide/HLA complexes enables blind structure prediction of T cell epitopes. Gupta S, Nerli S, Kutti Kandy S, Mersky GL, Sgourakis NG. Nat Commun 14 6349 (2023)
  11. Conformational plasticity of RAS Q61 family of neoepitopes results in distinct features for targeted recognition. McShan AC, Flores-Solis D, Sun Y, Garfinkle SE, Toor JS, Young MC, Sgourakis NG. Nat Commun 14 8204 (2023)
  12. Physicochemical Heuristics for Identifying High Fidelity, Near-Native Structural Models of Peptide/MHC Complexes. Keller GLJ, Weiss LI, Baker BM. Front Immunol 13 887759 (2022)
  13. Targeting of intracellular oncoproteins with peptide-centric CARs. Yarmarkovich M, Marshall QF, Warrington JM, Premaratne R, Farrel A, Groff D, Li W, di Marco M, Runbeck E, Truong H, Toor JS, Tripathi S, Nguyen S, Shen H, Noel T, Church NL, Weiner A, Kendsersky N, Martinez D, Weisberg R, Christie M, Eisenlohr L, Bosse KR, Dimitrov DS, Stevanovic S, Sgourakis NG, Kiefel BR, Maris JM. Nature 623 820-827 (2023)


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