Upregulation of intratumoral HLA class I and peritumoral Mx1 in ulcerated melanomas

References

• Allen AC, Spitz S. Malignant melanoma; a clinicopathological analysis of the criteria for diagnosis and prognosis. Cancer. 1953;6:1–11. doi:10.1002/1097-0142(195301)6:1<1::aid-cncr2820060102>3.0.co;2-c.
   PubMed Web of Science ®Google Scholar
• Balch CM, Buzaid AC, Soong SJ, Atkins MB, Cascinelli N, Coit DG, Fleming ID, Gershenwald JE, Houghton A, Kirkwood JM, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol. 2001;19:3635–3648. doi:10.1200/JCO.2001.19.16.3635.
   PubMed Web of Science ®Google Scholar
• Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, Buzaid AC, Cochran AJ, Coit DG, Ding S, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol. 2009;27:6199–6206. doi:10.1200/JCO.2009.23.4799.
   PubMed Web of Science ®Google Scholar
• American Joint Committe on Cancer (AJCC). AJCC Cancer Staging Manual Eight Edition. 2017.
   Google Scholar
• Spatz A, Cook MG, Elder DE, Piepkorn M, Ruiter DJ, Barnhill RL. Interobserver reproducibility of ulceration assessment in primary cutaneous melanomas. Eur J Cancer. 2003;39:1861–1865. doi:10.1016/s0959-8049(03)00325-3.
   PubMed Web of Science ®Google Scholar
• Kashani-Sabet M, Sagebiel RW, Ferreira CM, Nosrati M, Miller JR 3rd. Tumor vascularity in the prognostic assessment of primary cutaneous melanoma. J Clin Oncol. 2002;20:1826–1831. doi:10.1200/JCO.2002.07.082.
   PubMed Web of Science ®Google Scholar
• Straume O, Salvesen HB, Akslen LA. Angiogenesis is prognostically important in vertical growth phase melanomas. Int J Oncol. 1999;15:595–599. doi:10.3892/ijo.15.3.595.
   PubMed Web of Science ®Google Scholar
• Jewell R, Elliott F, Laye J, Nsengimana J, Davies J, Walker C, Conway C, Mitra A, Harland M, Cook MG, et al. The clinicopathological and gene expression patterns associated with ulceration of primary melanoma. Pigment Cell Melanoma Res. 2015;28:94–104. doi:10.1111/pcmr.12315.
   PubMed Web of Science ®Google Scholar
• Depasquale I, Thompson WD. Microvessel density for melanoma prognosis. Histopathology. 2005;47:186–194. doi:10.1111/j.1365-2559.2005.02193.x.
   PubMed Web of Science ®Google Scholar
• Bonnelykke-Behrndtz ML, Steiniche T, Norgaard P, Danielsen AV, Damsgaard TE, Christensen IJ, Bastholt L, Møller HJ, Schmidt H. Loss of E-cadherin as Part of a Migratory Phenotype in Melanoma Is Associated With Ulceration. Am J Dermatopathol. 2017;39:672–678. doi:10.1097/DAD.0000000000000750.
   PubMed Web of Science ®Google Scholar
• Winnepenninckx V, Lazar V, Michiels S, Dessen P, Stas M, Alonso SR, Avril M-F, Ortiz Romero PL, Robert T, Balacescu O, et al. Gene expression profiling of primary cutaneous melanoma and clinical outcome. J Natl Cancer Inst. 2006;98:472–482. doi:10.1093/jnci/djj103.
   PubMedGoogle Scholar
• Antonio N, Bonnelykke-Behrndtz ML, Ward LC, Collin J, Christensen IJ, Steiniche T, Schmidt H, Feng Y, Martin P. The wound inflammatory response exacerbates growth of pre-neoplastic cells and progression to cancer. Embo J. 2015;34:2219–2236. doi:10.15252/embj.201490147.
   PubMed Web of Science ®Google Scholar
• Koelblinger P, Emberger M, Drach M, Cheng PF, Lang R, Levesque MP, Bauer JW, Dummer R. et al. Increased tumour cell PD-L1 expression, macrophage and dendritic cell infiltration characterise the tumour microenvironment of ulcerated primary melanomas. J. Eur Acad Dermatol Venereol. 2019; 33(4):667-675.
   Google Scholar
• Elliott B, Scolyer RA, Suciu S, Lebecque S, Rimoldi D, Gugerli O, Musat E, Sharma RN, Lienard D, Keilholz U, et al. Long-term protective effect of mature DC-LAMP+ dendritic cell accumulation in sentinel lymph nodes containing micrometastatic melanoma. Clin Cancer Res. 2007;13:3825–3830. doi:10.1158/1078-0432.CCR-07-0358.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Suciu S, Santinami M, Testori A, Kruit WH, Marsden J, Punt CJA, Salès F, Gore M, Mackie R, et al. Adjuvant therapy with pegylated interferon alfa-2b versus observation alone in resected stage III melanoma: final results of EORTC 18991, a randomised phase III trial. Lancet. 2008;372:117–126. doi:10.1016/S0140-6736(08)61033-8.
   PubMed Web of Science ®Google Scholar
• McMasters KM, Edwards MJ, Ross MI, Reintgen DS, Martin RC 2nd, Urist MM, Noyes RD, Sussman JJ, Stromberg AJ, Scoggins CR. Ulceration as a predictive marker for response to adjuvant interferon therapy in melanoma. Ann Surg. 2010;252:460–465. discussion 5-6. doi:10.1097/SLA.0b013e3181f20bb1.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Suciu S, Testori A, Kruit WH, Marsden J, Punt CJ, Santinami M, Salès F, Schadendorf D, Patel P, et al. Ulceration and stage are predictive of interferon efficacy in melanoma: results of the phase III adjuvant trials EORTC 18952 and EORTC 18991. Eur J Cancer. 2012;48:218–225. doi:10.1016/j.ejca.2011.09.028.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Suciu S, Rutkowski P, Kruit WH, Punt CJ, Dummer R, Salès F, Keilholz U, de Schaetzen G, Testori A. Long term follow up of the EORTC 18952 trial of adjuvant therapy in resected stage IIB-III cutaneous melanoma patients comparing intermediate doses of interferon-alpha-2b (IFN) with observation: Ulceration of primary is key determinant for IFN-sensitivity. Eur J Cancer. 2016;55:111–121. doi:10.1016/j.ejca.2015.11.014.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Suciu S, MacKie R, Ruka W, Testori A, Kruit W, Punt CJA, Delauney M, Sales F, Groenewegen G, et al. Post-surgery adjuvant therapy with intermediate doses of interferon alfa 2b versus observation in patients with stage IIb/III melanoma (EORTC 18952): randomised controlled trial. Lancet. 2005;366:1189–1196. doi:10.1016/S0140-6736(05)67482-X.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Suciu S, Testori A, Santinami M, Kruit WH, Marsden J, Punt CJA, Salès F, Dummer R, Robert C, et al. Long-term results of the randomized phase III trial EORTC 18991 of adjuvant therapy with pegylated interferon alfa-2b versus observation in resected stage III melanoma. J Clin Oncol. 2012;30:3810–3818. doi:10.1200/JCO.2011.41.3799.
   PubMed Web of Science ®Google Scholar
• Ives NJ, Suciu S, Eggermont AMM, Kirkwood J, Lorigan P, Markovic SN, Garbe C, Wheatley K. Adjuvant interferon-alpha for the treatment of high-risk melanoma: An individual patient data meta-analysis. Eur J Cancer. 2017;82:171–183. doi:10.1016/j.ejca.2017.06.006.
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Galluzzi L, Kepp O, Smyth MJ, Kroemer G. Type I interferons in anticancer immunity. Nat Rev Immunol. 2015;15:405–414. doi:10.1038/nri3845.
   PubMed Web of Science ®Google Scholar
• Milling SW, Silvers WK, Sai T, Mintz B. Decline in MHC class I expression with increasing thickness of cutaneous melanomas in standard-strain transgenic mouse models. Melanoma Res. 2002;12:221–230.
   PubMed Web of Science ®Google Scholar
• Bui JD, Schreiber RD. Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr Opin Immunol. 2007;19:203–208. doi:10.1016/j.coi.2007.02.001.
   PubMed Web of Science ®Google Scholar
• Engels B, Engelhard VH, Sidney J, Sette A, Binder DC, Liu RB, Kranz DM, Meredith SC, Rowley DA, Schreiber H. Relapse or eradication of cancer is predicted by peptide-major histocompatibility complex affinity. Cancer Cell. 2013;23:516–526. doi:10.1016/j.ccr.2013.03.018.
   PubMed Web of Science ®Google Scholar
• Agrawal S, Reemtsma K, Bagiella E, Oluwole SF, Braunstein NS. Role of TAP-1 and/or TAP-2 antigen presentation defects in tumorigenicity of mouse melanoma. Cell Immunol. 2004;228:130–137. doi:10.1016/j.cellimm.2004.04.006.
   PubMed Web of Science ®Google Scholar
• Seliger B, Ritz U, Abele R, Bock M, Tampe R, Sutter G, Drexler I, Huber C, Ferrone S. Immune escape of melanoma: first evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. Cancer Res. 2001;61:8647–8650.
   PubMed Web of Science ®Google Scholar
• Halloran PF, Urmson J, Van der Meide PH, Autenried P. Regulation of MHC expression in vivo. II. IFN-alpha/beta inducers and recombinant IFN-alpha modulate MHC antigen expression in mouse tissues. J Immunol. 1989;142:4241–4247.
   PubMed Web of Science ®Google Scholar
• Garofalo R, Mei F, Espejo R, Ye G, Haeberle H, Baron S, Ogra PL, Reyes VE. Respiratory syncytial virus infection of human respiratory epithelial cells up-regulates class I MHC expression through the induction of IFN-beta and IL-1 alpha. J Immunol. 1996;157:2506–2513.
   PubMed Web of Science ®Google Scholar
• Ekmekcioglu S, Davies MA, Tanese K, Roszik J, Shin-Sim M, Bassett RL Jr., Milton DR, Woodman SE, Prieto VG, Gershenwald JE, et al. Inflammatory Marker Testing Identifies CD74 Expression in Melanoma Tumor Cells, and Its Expression Associates with Favorable Survival for Stage III Melanoma. Clin Cancer Res. 2016;22:3016–3024. doi:10.1158/1078-0432.CCR-15-2226.
   PubMed Web of Science ®Google Scholar
• Rodig SJ, Gusenleitner D, Jackson DG, Gjini E, Giobbie-Hurder A, Jin C, Chang H, Lovitch SB, Horak C, Weber JS, et al. MHC proteins confer differential sensitivity to CTLA-4 and PD-1 blockade in untreated metastatic melanoma. Sci Transl Med. 2018;10(450).
   Google Scholar
• Verhelst J, Parthoens E, Schepens B, Fiers W, Saelens X. Interferon-inducible protein Mx1 inhibits influenza virus by interfering with functional viral ribonucleoprotein complex assembly. J Virol. 2012;86:13445–13455. doi:10.1128/JVI.01682-12.
   PubMed Web of Science ®Google Scholar
• Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, Vitale I, Goubar A, Baracco EE, Remédios C, et al. Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med. 2014;20:1301–1309. doi:10.1038/nm.3708.
   PubMed Web of Science ®Google Scholar
• Silginer M, Nagy S, Happold C, Schneider H, Weller M, Roth P. Autocrine activation of the IFN signaling pathway may promote immune escape in glioblastoma. Neuro Oncol. 2017;19:1338–1349. doi:10.1093/neuonc/nox051.
   PubMed Web of Science ®Google Scholar
• Vannini F, Kashfi K, Nath N. The dual role of iNOS in cancer. Redox Biol. 2015;6:334–343. doi:10.1016/j.redox.2015.08.009.
   PubMed Web of Science ®Google Scholar
• Lu G, Zhang R, Geng S, Peng L, Jayaraman P, Chen C, Xu F, Yang J, Li Q, Zheng H, et al. Myeloid cell-derived inducible nitric oxide synthase suppresses M1 macrophage polarization. Nat Commun. 2015;6:6676. doi:10.1038/ncomms7676.
   PubMed Web of Science ®Google Scholar
• Farlik M, Reutterer B, Schindler C, Greten F, Vogl C, Muller M, Decker T. Nonconventional initiation complex assembly by STAT and NF-kappaB transcription factors regulates nitric oxide synthase expression. Immunity. 2010;33:25–34. doi:10.1016/j.immuni.2010.07.001.
   PubMed Web of Science ®Google Scholar
• Diefenbach A, Schindler H, Donhauser N, Lorenz E, Laskay T, MacMicking J, Röllinghoff M, Gresser I, Bogdan C. Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity. 1998;8:77–87.
   PubMed Web of Science ®Google Scholar
• Mattner J, Schindler H, Diefenbach A, Rollinghoff M, Gresser I, Bogdan C. Regulation of type 2 nitric oxide synthase by type 1 interferons in macrophages infected with Leishmania major. Eur J Immunol. 2000;30:2257–2267. doi:10.1002/1521-4141(2000)30:8<2257::AID-IMMU2257>3.0.CO;2-U.
   PubMed Web of Science ®Google Scholar
• Moreira-Teixeira L, Sousa J, McNab FW, Torrado E, Cardoso F, Machado H, Castro F, Cardoso V, Gaifem J, Wu X, et al. Type I IFN Inhibits Alternative Macrophage Activation during Mycobacterium tuberculosis Infection and Leads to Enhanced Protection in the Absence of IFN-gamma Signaling. J Immunol. 2016;197:4714–4726. doi:10.4049/jimmunol.1600584.
   PubMed Web of Science ®Google Scholar
• Douguet L, Bod L, Lengagne R, Labarthe L, Kato M, Avril MF, Prévost-Blondel A. Nitric oxide synthase 2 is involved in the pro-tumorigenic potential of gammadelta17 T cells in melanoma. Oncoimmunology. 2016;5:e1208878. doi:10.1080/2162402X.2016.1208878.
   PubMed Web of Science ®Google Scholar
• Kojima Y, Volkmer JP, McKenna K, Civelek M, Lusis AJ, Miller CL, Direnzo D, Nanda V, Ye J, Connolly AJ, et al. CD47-blocking antibodies restore phagocytosis and prevent atherosclerosis. Nature. 2016;536:86–90. doi:10.1038/nature18935.
   PubMed Web of Science ®Google Scholar
• Tong B, Wang M. CD47 is a novel potent immunotherapy target in human malignancies: current studies and future promises. Future Oncol. 2018;14:2179–2188. doi:10.2217/fon-2018-0035.
   PubMed Web of Science ®Google Scholar
• Basile MS, Mazzon E, Russo A, Mammana S, Longo A, Bonfiglio V, Fallico M, Caltabiano R, Fagone P, Nicoletti F, et al. Differential modulation and prognostic values of immune-escape genes in uveal melanoma. PLoS One. 2019;14:e0210276. doi:10.1371/journal.pone.0210276.
   PubMed Web of Science ®Google Scholar
• Ngo M, Han A, Lakatos A, Sahoo D, Hachey SJ, Weiskopf K, Beck AH, Weissman IL, Boiko AD. Antibody Therapy Targeting CD47 and CD271 Effectively Suppresses Melanoma Metastasis in Patient-Derived Xenografts. Cell Rep. 2016;16:1701–1716. doi:10.1016/j.celrep.2016.07.004.
   PubMed Web of Science ®Google Scholar
• Buback F, Renkl AC, Schulz G, Weiss JM. Osteopontin and the skin: multiple emerging roles in cutaneous biology and pathology. Exp Dermatol. 2009;18:750–759. doi:10.1111/j.1600-0625.2009.00926.x.
   PubMed Web of Science ®Google Scholar
• Conway C, Mitra A, Jewell R, Randerson-Moor J, Lobo S, Nsengimana J, Edward S, Sanders DS, Cook M, Powell B, et al. Gene expression profiling of paraffin-embedded primary melanoma using the DASL assay identifies increased osteopontin expression as predictive of reduced relapse-free survival. Clin Cancer Res. 2009;15:6939–6946. doi:10.1158/1078-0432.CCR-09-1631.
   PubMed Web of Science ®Google Scholar
• Haritoglou I, Wolf A, Maier T, Haritoglou C, Hein R, Schaller UC. Osteopontin and ‘melanoma inhibitory activity’: comparison of two serological tumor markers in metastatic uveal melanoma patients. Ophthalmologica. 2009;223:239–243. doi:10.1159/000206139.
   PubMed Web of Science ®Google Scholar
• Mandelin J, Lin EC, Hu DD, Knowles SK, Do KA, Wang X, Sage EH, Smith JW, Arap W, Pasqualini R. Extracellular and intracellular mechanisms that mediate the metastatic activity of exogenous osteopontin. Cancer. 2009;115:1753–1764. doi:10.1002/cncr.24170.
   PubMed Web of Science ®Google Scholar
• Wu Y, Jiang P, Lin Y, Chen S, Lin N, Li J. Expression of phosphorylated-STAT3 and osteopontin and their correlation in melanoma. J Huazhong Univ Sci Technolog Med Sci. 2009;29:246–250. doi:10.1007/s11596-009-0223-0.
   PubMedGoogle Scholar
• Fukunaga-Kalabis M, Martinez G, Telson SM, Liu ZJ, Balint K, Juhasz I, Elder DE, Perbal B, Herlyn M. Downregulation of CCN3 expression as a potential mechanism for melanoma progression. Oncogene. 2008;27:2552–2560. doi:10.1038/sj.onc.1210896.
   PubMed Web of Science ®Google Scholar
• McCallum L, Irvine AE. CCN3–a key regulator of the hematopoietic compartment. Blood Rev. 2009;23:79–85. doi:10.1016/j.blre.2008.07.002.
   PubMed Web of Science ®Google Scholar
• Vallacchi V, Rodolfo M. Regulatory role of CCN3 in melanoma cell interaction with the extracellular matrix. Cell Adh Migr. 2009;3:7–10. doi:10.4161/cam.3.1.6836.
   PubMed Web of Science ®Google Scholar
• Gajewski TF, Corrales L, Williams J, Horton B, Sivan A, Spranger S. Cancer Immunotherapy Targets Based on Understanding the T Cell-Inflamed Versus Non-T Cell-Inflamed Tumor Microenvironment. Adv Exp Med Biol. 2017;1036:19–31. doi:10.1007/978-3-319-67577-0_2.
   PubMed Web of Science ®Google Scholar
• Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman DR, Albright A, Cheng JD, Kang SP, Shankaran V, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017;127:2930–2940. doi:10.1172/JCI91190.
   PubMed Web of Science ®Google Scholar
• de Moll EH, Fu Y, Qian Y, Perkins SH, Wieder S, Gnjatic S, Remark R, Bernardo SG, Moskalenko M, Yao J, et al. Immune biomarkers are more accurate in prediction of survival in ulcerated than in non-ulcerated primary melanomas. Cancer Immunol Immunother. 2015;64:1193–1203. doi:10.1007/s00262-015-1726-0.
   PubMed Web of Science ®Google Scholar
• Benci JL, Xu B, Qiu Y, Wu TJ, Dada H, Twyman-Saint Victor C, Cucolo L, Lee DSM, Pauken KE, Huang AC, et al. Tumor Interferon Signaling Regulates a Multigenic Resistance Program to Immune Checkpoint Blockade. Cell. 2016;167:1540–54 e12. doi:10.1016/j.cell.2016.11.022.
   PubMed Web of Science ®Google Scholar
• Weichselbaum RR, Ishwaran H, Yoon T, Nuyten DS, Baker SW, Khodarev N, Su AW, Shaikh AY, Roach P, Kreike B, et al. An interferon-related gene signature for DNA damage resistance is a predictive marker for chemotherapy and radiation for breast cancer. Proc Natl Acad Sci U S A. 2008;105:18490–18495. doi:10.1073/pnas.0809242105.
   PubMed Web of Science ®Google Scholar
• Lee J, Sayed N, Hunter A, Au KF, Wong WH, Mocarski ES, Pera RR, Yakubov E, Cooke JP. Activation of innate immunity is required for efficient nuclear reprogramming. Cell. 2012;151:547–558. doi:10.1016/j.cell.2012.09.034.
   PubMed Web of Science ®Google Scholar
• Wang W, Edington HD, Rao UNM, Jukic DM, Land SR, Ferrone S, Kirkwood JM. Modulation of signal transducers and activators of transcription 1 and 3 signaling in melanoma by high-dose IFNalpha2b. Clin Cancer Res. 2007;13:1523–1531. doi:10.1158/1078-0432.CCR-06-1387.
   PubMed Web of Science ®Google Scholar
• Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, Hamid O, Robert C, Ascierto PA, Richards JM, et al. Prolonged Survival in Stage III Melanoma with Ipilimumab Adjuvant Therapy. N Engl J Med. 2016;375:1845–1855. doi:10.1056/NEJMoa1611299.
   PubMed Web of Science ®Google Scholar
• Eggermont AMM, Blank CU, Mandala M, Long GV, Atkinson V, Dalle S, Haydon A, Lichinitser M, Khattak A, Carlino MS, et al. Adjuvant Pembrolizumab versus Placebo in Resected Stage III Melanoma. N Engl J Med. 2018;378:1789–1801. doi:10.1056/NEJMoa1802357.
   PubMed Web of Science ®Google Scholar
• Remark R, Merghoub T, Grabe N, Litjens G, Damotte D, Wolchok JD, Kreutzfeldt M, Page N, Zimmer G, Geier F, et al. In-depth tissue profiling using multiplexed immunohistochemical consecutive staining on single slide. Sci Immunol. 2016;1:aaf6925. doi:10.1126/sciimmunol.aah6817.
   PubMed Web of Science ®Google Scholar