Melanocortin 1 Receptor-derived peptides are efficiently recognized by cytotoxic T lymphocytes from melanoma patients

Immunobiology

Volumn 219, Issue 3, 2014, Pages 189-197

  González, Fermín E ^a,b,c   Ramírez, Marcos ^a   Allerbring, Eva B ^b   Fasching, Nina ^b   Lundqvist, Andreas ^d   Poschke, Isabel ^e   Achour, Adnane ^b   Salazar Onfray, Flavio ^a  

^a UNIVERSITY OF CHILE   (Chile)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF CHILE   (Chile)

^d KAROLINSKA INSTITUTE   (Sweden)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Cytotoxic T lymphocytes; Immunotherapy; MC1R; Melanoma; Tumour infiltrating lymphocytes

Indexed keywords

HLA A2 ANTIGEN; MELANOCORTIN 1 RECEPTOR;

ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER STAGING; CANCER TISSUE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOGENICITY; IN VITRO STUDY; MELANOMA; MOLECULAR RECOGNITION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; TUMOR ASSOCIATED LEUKOCYTE;

CYTOTOXIC T LYMPHOCYTES; IMMUNOTHERAPY; MC1R; MELANOMA; TUMOUR INFILTRATING LYMPHOCYTES;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CELLS, CULTURED; HLA-A2 ANTIGEN; HUMANS; IMMUNODOMINANT EPITOPES; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; PEPTIDE FRAGMENTS; PROTEIN BINDING; RECEPTOR, MELANOCORTIN, TYPE 1; SKIN NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84893684165     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2013.10.002     Document Type: Article

References (50)

1. Adema G.J., de Boer A.J., Vogel A.M., Loenen W.A., Figdor C.G. Molecular characterization of the melanocyte lineage-specific antigen gp100. J. Biol. Chem. 1994, 269:20126-20133.
2. Aguilera R., Saffie C., Tittarelli A., González F.E., Ramirez M., Reyes D., Pereda C., Hevia D., Garcia T., Salazar L., Ferreira A., Hermoso M., Mendoza-Naranjo A., Ferrada C., Garrido P., Lopez M.N., Salazar-Onfray F. Heat-shock induction of tumor-derived danger signals mediates rapid monocyte differentiation into clinically effective dendritic cells. Clin. Cancer Res. 2011, 17:2474-2483.
3. Alanio C., Lemaitre F., Law H.K., Hasan M., Albert M.L. Enumeration of human antigen-specific naive CD8+ T cells reveals conserved precursor frequencies. Blood 2010, 115:3718-3725.
4. Allerbring E.B., Duru A.D., Uchtenhagen H., Madhurantakam C., Tomek M.B., Grimm S., Mazumdar P.A., Friemann R., Uhlin M., Sandalova T., Nygren P.A., Achour A. Unexpected T-cell recognition of an altered peptide ligand is driven by reversed thermodynamics. Eur. J. Immunol. 2012, 42:2990-3000.
5. Brichard V., Van Pel A., Wolfel T., Wolfel C., De Plaen E., Lethe B., Coulie P., Boon T. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 1993, 178:489-495.
6. Chen Y.T., Stockert E., Tsang S., Coplan K.A., Old L.J. Immunophenotyping of melanomas for tyrosinase: implications for vaccine development. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:8125-8129.
7. Chhajlani V., Wikberg J.E. Molecular cloning and expression of the human melanocyte stimulating hormone receptor cDNA. FEBS Lett. 1992, 309:417-420.
8. Colella T.A., Bullock T.N., Russell L.B., Mullins D.W., Overwijk W.W., Luckey C.J., Pierce R.A., Restifo N.P., Engelhard V.H. Self-tolerance to the murine homologue of a tyrosinase-derived melanoma antigen: implications for tumor immunotherapy. J. Exp. Med. 2000, 191:1221-1232.
9. Coulie P.G., Brichard V., Van Pel A., Wolfel T., Schneider J., Traversari C., Mattei S., De Plaen E., Lurquin C., Szikora J.P., Renauld J.C., Boon T. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 1994, 180:35-42.
10. Gross D.A., Graff-Dubois S., Opolon P., Cornet S., Alves P., Bennaceur-Griscelli A., Faure O., Guillaume P., Firat H., Chouaib S., Lemonnier F.A., Davoust J., Miconnet I., Vonderheide R.H., Kosmatopoulos K. High vaccination efficiency of low-affinity epitopes in antitumor immunotherapy. J. Clin. Invest. 2004, 113:425-433.
11. Grossmann M.E., Davila T., Celis T. Avoiding tolerance against prostatic antigens with subdominant peptide epitopes. J. Immunother. 2001, 24:237-241.
12. Hernandez J., Lee P.P., Davis M.M., Sherman L.A. The use of HLA A2.1/p53 peptide tetramers to visualize the impact of self tolerance on the TCR repertoire. J. Immunol. 2000, 164:596-602.
13. Kawakami Y., Eliyahu S., Delgado C.H., Robbins P.F., Rivoltini L., Topalian S.L., Miki T., Rosenberg S.A. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:3515-3519.
14. Kawakami Y., Eliyahu S., Delgado C.H., Robbins P.F., Sakaguchi K., Appella E., Yannelli J.R., Adema G.J., Miki T., Rosenberg S.A. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:6458-6462.
15. Kawakami Y., Eliyahu S., Sakaguchi K., Robbins P.F., Rivoltini L., Yannelli J.R., Appella E., Rosenberg S.A. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J. Exp. Med. 1994, 180:347-352.
16. Knutson K.L., Schiffman K., Cheever M.A., Disis M.L. Immunization of cancer patients with a HER-2/neu, HLA-A2 peptide, p369-377, results in short-lived peptide-specific immunity. Clin. Cancer Res. 2002, 8:1014-1018.
17. Kvistborg P., Shu C.J., Heemskerk B., Fankhauser M., Thrue C.A., Toebes M., van Rooij N., Linnemann C., van Buuren M.M., Urbanus J.H., Beltman J.B., Thor Straten P., Li Y.F., Robbins P.F., Besser M.J., Schachter J., Kenter G.G., Dudley M.E., Rosenberg S.A., Haanen J.B., Hadrup S.R., Schumacher T.N. TIL therapy broadens the tumor-reactive CD8(+) T cell compartment in melanoma patients. Oncoimmunology 2012, 1:409-418.
18. Leffers N., Lambeck A.J., Gooden M.J., Hoogeboom B.N., Wolf R., Hamming I.E., Hepkema B.G., Willemse P.H., Molmans B.H., Hollema H., Drijfhout J.W., Sluiter W.J., Valentijn A.R., Fathers L.M., Oostendorp J., van der Zee A.G., Melief C.J., van der Burg S.H., Daemen T., Nijman H.W. Immunization with a P53 synthetic long peptide vaccine induces P53-specific immune responses in ovarian cancer patients, a phase II trial. Int. J. Cancer 2009, 125:2104-2113.
19. Legoux F., Debeaupuis E., Echasserieau K., De La Salle H., Saulquin X., Bonneville M. Impact of TCR reactivity and HLA phenotype on naive CD8T cell frequency in humans. J. Immunol. 2010, 184:6731-6738.
20. Lopez M.N., Pereda C., Ramirez M., Mendoza-Naranjo A., Serrano A., Ferreira A., Poblete R., Kalergis A.M., Kiessling R., Salazar-Onfray F. Melanocortin 1 receptor is expressed by uveal malignant melanoma and can be considered a new target for diagnosis and immunotherapy. Invest. Ophthalmol. Vis. Sci. 2007, 48:1219-1227.
21. Lopez M.N., Pereda C., Segal G., Munoz L., Aguilera R., González F.E., Escobar A., Ginesta A., Reyes D., González R., Mendoza-Naranjo A., Larrondo M., Compan A., Ferrada C., Salazar-Onfray F. Prolonged survival of dendritic cell-vaccinated melanoma patients correlates with tumor-specific delayed type IV hypersensitivity response and reduction of tumor growth factor beta-expressing T cells. J. Clin. Oncol. 2009, 27:945-952.
22. Mavroudis D., Bolonakis I., Cornet S., Myllaki G., Kanellou P., Kotsakis A., Galanis A., Nikoloudi I., Spyropoulou M., Menez J., Miconnet I., Niniraki M., Cordopatis P., Kosmatopoulos K., Georgoulias V. A phase I study of the optimized cryptic peptide TERT(572y) in patients with advanced malignancies. Oncology 2006, 70:306-314.
23. Melief C.J., van der Burg S.H. Immunotherapy of established (pre)malignant disease by synthetic long peptide vaccines. Nat. Rev. Cancer 2008, 8:351-360.
24. Michaelsson J., Achour A., Salcedo M., Kase-Sjostrom A., Sundback J., Harris R.A., Karre K. Visualization of inhibitory Ly49 receptor specificity with soluble major histocompatibility complex class I tetramers. Eur. J. Immunol. 2000, 30:300-307.
25. Palucka K., Banchereau J. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 2012, 12:265-277.
26. Parkhurst M.R., Salgaller M.L., Southwood S., Robbins P.F., Sette A., Rosenberg S.A., Kawakami Y. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J. Immunol. 1996, 157:2539-2548.
27. Parkhurst M.R., Riley J.P., Igarashi T., Li Y., Robbins P.F., Rosenberg S.A. Immunization of patients with the hTERT: 540-548 peptide induces peptide-reactive T lymphocytes that do not recognize tumors endogenously expressing telomerase. Clin. Cancer Res. 2004, 10:4688-4698.
28. Restifo N.P., Dudley M.E., Rosenberg S.A. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 2012, 12:269-281.
29. Reynolds S.R., Celis E., Sette A., Oratz R., Shapiro R.L., Johnston D., Fotino M., Bystryn J.C. HLA-independent heterogeneity of CD8+ T cell responses to MAGE-3, Melan-A/MART-1, gp100, tyrosinase, MC1R, and TRP-2 in vaccine-treated melanoma patients. J. Immunol. 1998, 161:6970-6976.
30. Rosenberg S.A., Yang J.C., Schwartzentruber D.J., Hwu P., Marincola F.M., Topalian S.L., Restifo N.P., Dudley M.E., Schwarz S.L., Spiess P.J., Wunderlich J.R., Parkhurst M.R., Kawakami Y., Seipp C.A., Einhorn J.H., White D.E. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med. 1998, 4:321-327.
31. Sakai C., Kawakami Y., Law L.W., Furumura M., Hearing V.J. Melanosomal proteins as melanoma-specific immune targets. Melanoma Res. 1997, 7:83-95.
32. Salazar-Onfray F., Nakazawa T., Chhajlani V., Petersson M., Karre K., Masucci G., Celis E., Sette A., Southwood S., Appella E., Kiessling R. Synthetic peptides derived from the melanocyte-stimulating hormone receptor MC1R can stimulate HLA-A2-restricted cytotoxic T lymphocytes that recognize naturally processed peptides on human melanoma cells. Cancer Res. 1997, 57:4348-4355.
33. Salazar-Onfray F., Lopez M., Lundqvist A., Aguirre A., Escobar A., Serrano A., Korenblit C., Petersson M., Chhajlani V., Larsson O., Kiessling R. Tissue distribution and differential expression of melanocortin 1 receptor, a malignant melanoma marker. Br. J. Cancer 2002, 87:414-422.
34. Schaed S.G., Klimek V.M., Panageas K.S., Musselli C.M., Butterworth L., Hwu W.J., Livingston P.O., Williams L., Lewis J.J., Houghton A.N., Chapman P.B. T-cell responses against tyrosinase 368-376(370D) peptide in HLA*A0201+ melanoma patients: randomized trial comparing incomplete Freund's adjuvant, granulocyte macrophage colony-stimulating factor, and QS-21 as immunological adjuvants. Clin. Cancer Res. 2002, 8:967-972.
35. Schmollinger J.C., Vonderheide R.H., Hoar K.M., Maecker B., Schultze J.L., Hodi F.S., Soiffer R.J., Jung K., Kuroda M.J., Letvin N.L., Greenfield E.A., Mihm M., Kutok J.L., Dranoff G. Melanoma inhibitor of apoptosis protein (ML-IAP) is a target for immune-mediated tumor destruction. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:3398-3403.
36. Slingluff C.L., Yamshchikov G., Neese P., Galavotti H., Eastham S., Engelhard V.H., Kittlesen D., Deacon D., Hibbitts S., Grosh W.W., Petroni G., Cohen R., Wiernasz C., Patterson J.W., Conway B.P., Ross W.G. Phase I trial of a melanoma vaccine with gp100(280-288) peptide and tetanus helper peptide in adjuvant: immunologic and clinical outcomes. Clin. Cancer Res. 2001, 7:3012-3024.
37. Smyth M.J., Dunn G.P., Schreiber R.D. Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv. Immunol. 2006, 90:1-50.
38. Speetjens F.M., Kuppen P.J., Welters M.J., Essahsah F., Voet Van Den Brink A.M., Lantrua M.G., Valentijn A.R., Oostendorp J., Fathers L.M., Nijman H.W., Drijfhout J.W., van de Velde C.J., Melief C.J., van der Burg S.H. Induction of p53-specific immunity by a p53 synthetic long peptide vaccine in patients treated for metastatic colorectal cancer. Clin. Cancer Res. 2009, 15:1086-1095.
39. Sprent J., Surh C.D. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat. Immunol. 2011, 12:478-484.
40. Tatro J.B., Atkins M., Mier J.W., Hardarson S., Wolfe H., Smith T., Entwistle M.L., Reichlin S. Melanotropin receptors demonstrated in situ in human melanoma. J. Clin. Invest. 1990, 85:1825-1832.
41. Thornwall M., Dimitriou A., Xu X., Larsson E., Chhajlani V. Immunohistochemical detection of the melanocortin 1 receptor in human testis, ovary and placenta using specific monoclonal antibody. Horm. Res. 1997, 48:215-218.
42. Valmori D., Fonteneau J.F., Lizana C.M., Gervois N., Lienard D., Rimoldi D., Jongeneel V., Jotereau F., Cerottini J.C., Romero P. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J. Immunol. 1998, 160:1750-1758.
43. Van Der Bruggen P., Zhang Y., Chaux P., Stroobant V., Panichelli C., Schultz E.S., Chapiro J., Van Den Eynde B.J., Brasseur F., Boon T. Tumor-specific shared antigenic peptides recognized by human T cells. Immunol. Rev. 2002, 188:51-64.
44. van Stipdonk M.J., Badia-Martinez D., Sluijter M., Offringa R., van Hall T., Achour A. Design of agonistic altered peptides for the robust induction of CTL directed towards H-2Db in complex with the melanoma-associated epitope gp100. Cancer Res. 2009, 69:7784-7792.
45. Vetsika E.K., Konsolakis G., Aggouraki D., Kotsakis A., Papadimitraki E., Christou S., Menez-Jamet J., Kosmatopoulos K., Georgoulias V., Mavroudis D. Immunological responses in cancer patients after vaccination with the therapeutic telomerase-specific vaccine Vx-001. Cancer Immunol. Immunother. 2012, 61:157-168.
46. Vonderheide R.H., Domchek S.M., Schultze J.L., George D.J., Hoar K.M., Chen D.Y., Stephans K.F., Masutomi K., Loda M., Xia Z., Anderson K.S., Hahn W.C., Nadler L.M. Vaccination of cancer patients against telomerase induces functional antitumor CD8+ T lymphocytes. Clin. Cancer Res. 2004, 10:828-839.
47. Wankowicz-Kalinska A., Mailliard R.B., Olson K., Graham F., Edington H., Kirkwood J.M., Martinek S., Das P.K., Storkus W.J. Accumulation of low-avidity anti-melanocortin receptor 1 (anti-MC1R) CD8+ T cells in the lesional skin of a patient with melanoma-related depigmentation. Melanoma Res. 2006, 16:165-174.
48. Wenandy L., Sorensen R.B., Sengelov L., Svane I.M., thor Straten P., Andersen M.H. The immunogenicity of the hTERT540-548 peptide in cancer. Clin. Cancer Res. 2008, 14:4-7.
49. Winder A., Kobayashi T., Tsukamoto K., Urabe K., Aroca P., Kameyama K., Hearing V.J. The tyrosinase gene family-interactions of melanogenic proteins to regulate melanogenesis. Cell. Mol. Biol. Res. 1994, 40:613-626.
50. Xia Y., Muceniece R., Wikberg J.E. Immunological localisation of melanocortin 1 receptor on the cell surface of WM266-4 human melanoma cells. Cancer Lett. 1996, 98:157-162.