Definitive chemoradiation alters the immunologic landscape and immune checkpoints in head and neck cancer

British Journal of Cancer

Volumn 115, Issue 2, 2016, Pages 252-260

  Sridharan, Vishwajith ^a,b   Margalit, Danielle N ^a   Lynch, Stephanie A ^a   Severgnini, Mariano ^c   Zhou, Jun ^c   Chau, Nicole G ^a   Rabinowits, Guilherme ^a   Lorch, Jochen H ^a   Hammerman, Peter S ^a   Hodi, F Stephen ^a,c   Haddad, Robert I ^a   Tishler, Roy B ^a   Schoenfeld, Jonathan D ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL16 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; T LYMPHOCYTE RECEPTOR; CYTOKINE;

ADULT; ANTIBODY RESPONSE; ARTICLE; CANCER IMMUNOTHERAPY; CANCER PATIENT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHEMORADIOTHERAPY; CLINICAL ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; MALE; MIDDLE AGED; PRIORITY JOURNAL; PROTEOMICS; REGULATORY T LYMPHOCYTE; SUPPRESSOR CELL; TUMOR MICROENVIRONMENT; ANTIBODY PRODUCTION; BLOOD; CARCINOMA, SQUAMOUS CELL; HEAD AND NECK NEOPLASMS; IMMUNOLOGY;

ANTIBODY FORMATION; CARCINOMA, SQUAMOUS CELL; CHEMORADIOTHERAPY; CYTOKINES; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNITY, CELLULAR; MALE; MIDDLE AGED;

EID: 84977143008     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2016.166     Document Type: Article

References (58)

1. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, Westra WH, Chung CH, Jordan RC, Lu C, Kim H, Axelrod R, Silverman CC, Redmond KP, Gillison ML (2010) Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 363(1): 24-35.
2. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, Barlesi F, Kohlhaufl M, Arrieta O, Burgio MA, Fayette J, Lena H, Poddubskaya E, Gerber DE, Gettinger SN, Rudin CM, Rizvi N, Crino L, Blumenschein Jr. GR, Antonia SJ, Dorange C, Harbison CT, Graf Finckenstein F, Brahmer JR (2015) Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. N Engl J Med 373(17): 1627-1639.
3. Brahmer JR, Tykodi SS, Chow LQM, Hwu W-J, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366(26): 2455-2465.
4. Chandra RA, Wilhite TJ, Balboni TA, Alexander BM, Spektor A, Ott PA, Ng AK, Hodi FS, Schoenfeld JD (2015) A systematic evaluation of abscopal responses following radiotherapy in patients with metastatic melanoma treated with ipilimumab. Oncoimmunology 4(11): e1046028.
5. Cheng S, Zheng J, Zhu J, Xie C, Zhang X, Han X, Song B, Ma Y, Liu J (2015) PD-L1 gene polymorphism and high level of plasma soluble PD-L1 protein may be associated with non-small cell lung cancer. Int J Biol Markers 300(4): e364-e368.
6. de la Cruz-Merino L, Illescas-Vacas A, Grueso-Lopez A, Barco-Sanchez A, Miguez-Sanchez C. Cancer Immunotherapies Spanish G (2014) Radiation for awakening the dormant immune system, a promising challenge to be explored. Front Immunol 5: 102.
7. Deng L, Liang H, Burnette B, Beckett M, Darga T, Weichselbaum RR, Fu YX (2014a) Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 124(2): 687-695.
8. Deng L, Liang H, Xu M, Yang X, Burnette B, Arina A, Li XD, Mauceri H, Beckett M, Darga T, Huang X, Gajewski TF, Chen ZJ, Fu YX, Weichselbaum RR (2014b) STING-dependent cytosolic DNA sensing promotes radiation-induced type I Interferon-dependent antitumor immunity in immunogenic tumors. Immunity 41(5): 843-852.
9. Formenti SC, Demaria S (2013) Combining radiotherapy and cancer immunotherapy: a paradigm shift. J Natl Cancer Inst 105(4): 256-265.
10. Frigola X, Inman BA, Lohse CM, Krco CJ, Cheville JC, Thompson RH, Leibovich B, Blute ML, Dong H, Kwon ED (2011) Identification of a soluble form of B7-H1 that retains immunosuppressive activity and is associated with aggressive renal cell carcinoma. Clin Cancer Res 17(7): 1915-1923.
11. Golden EB, Demaria S, Schiff PB, Chachoua A, Formenti SC (2013) An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol Res 1(6): 365-372.
12. Grimaldi AM, Simeone E, Giannarelli D, Muto P, Falivene S, Borzillo V, Giugliano FM, Sandomenico F, Petrillo A, Curvietto M, Esposito A, Paone M, Palla M, Palmieri G, Caraco C, Ciliberto G, Mozzillo N, Ascierto PA (2014) Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy. Oncoimmunology 3: e28780.
13. Gros A, Tran E, Parkhurst M, Anna P, Ilyas S, Prickett T, Gartner J, Robbins P, Crystal J, Trebska-Mcgowan K, Wudnerlich J, Yang J, Rosenberg S (2015) Selection of circulating PD-1+ lymphocytes from cancer patients enriches for tumor-reactive and mutation-specific lymphocytes. J Immunother Cancer 3(Suppl 2): O2.
14. Gyorki DE, Callahan M, Wolchok JD, Ariyan CE (2013) The delicate balance of melanoma immunotherapy. Clin Transl Immunology 2(8): e5.
15. Hald SM, Kiselev Y, Al-Saad S, Richardsen E, Johannessen C, Eilertsen M, Kilvaer TK, Al-Shibli K, Andersen S, Busund LT, Bremnes RM, Donnem T (2015) Prognostic impact of CXCL16 and CXCR6 in non-small cell lung cancer: combined high CXCL16 expression in tumor stroma and cancer cells yields improved survival. BMC Cancer 15: 441.
16. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJM, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbé C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363(8): 711-723.
17. Hojo S, Koizumi K, Tsuneyama K, Arita Y, Cui Z, Shinohara K, Minami T, Hashimoto I, Nakayama T, Sakurai H, Takano Y, Yoshie O, Tsukada K, Saiki I (2007) High-level expression of chemokine CXCL16 by tumor cells correlates with a good prognosis and increased tumor-infiltrating lymphocytes in colorectal cancer. Cancer Res 67(10): 4725-4731.
18. Jemal A, Simard EP, Dorell C, Noone A-M, Markowitz LE, Kohler B, Eheman C, Saraiya M, Bandi P, Saslow D, Cronin KA, Watson M, Schiffman M, Henley SJ, Schymura MJ, Anderson RN, Yankey D, Edwards BK (2013) Annual Report to the Nation on the Status of Cancer, 1975-2009, featuring the burden and trends in human papillomavirus (HPV)-associated cancers and HPV vaccination coverage levels. J Natl Cancer Inst 105(3): 175-201.
19. Jinushi M, Hodi FS, Dranoff G (2006) Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc Natl Acad Sci USA 103(24): 9190-9195.
20. Jinushi M, Vanneman M, Munshi NC, Tai YT, Prabhala RH, Ritz J, Neuberg D, Anderson KC, Carrasco DR, Dranoff G (2008) MHC class I chain-related protein A antibodies and shedding are associated with the progression of multiple myeloma. Proc Natl Acad Sci USA 105(4): 1285-1290.
21. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, Redfern CH, Ferrari AC, Dreicer R, Sims RB, Xu Y, Frohlich MW, Schellhammer PF. Investigators IS (2010) Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 363(5): 411-422.
22. Kee JY, Ito A, Hojo S, Hashimoto I, Igarashi Y, Tsukada K, Irimura T, Shibahara N, Nakayama T, Yoshie O, Sakurai H, Saiki I, Koizumi K (2013) Chemokine CXCL16 suppresses liver metastasis of colorectal cancer via augmentation of tumor-infiltrating natural killer T cells in a murine model. Oncol Rep 29(3): 975-982.
23. Klug F, Prakash H, Huber PE, Seibel T, Bender N, Halama N, Pfirschke C, Voss RH, Timke C, Umansky L, Klapproth K, Schakel K, Garbi N, Jager D, Weitz J, Schmitz-Winnenthal H, Hammerling GJ, Beckhove P (2013) Low-dose irradiation programs macrophage differentiation to an iNOS(+)/M1 phenotype that orchestrates effective T cell immunotherapy. Cancer Cell 24(5): 589-602.
24. Levy A, Chargari C, Cheminant M, Simon N, Bourgier C, Deutsch E (2013) Radiation therapy and immunotherapy: implications for a combined cancer treatment. Crit Rev Oncol Hematol 85(3): 278-287.
25. Lim JY, Gerber SA, Murphy SP, Lord EM (2014) Type I interferons induced by radiation therapy mediate recruitment and effector function of CD8(+) T cells. Cancer Immunol Immunother 63(3): 259-271.
26. Lunardi S, Lim SY, Muschel RJ, Brunner TB (2015) IP-10/CXCL10 attracts regulatory T cells: Implication for pancreatic cancer. Oncoimmunology 4(9): e1027473.
27. Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, Bruno TC, Richmon JD, Wang H, Bishop JA, Chen L, Drake CG, Topalian SL, Pardoll DM, Pai SI (2013) Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 73(6): 1733-1741.
28. Lynch TJ, Bondarenko I, Luft A, Serwatowski P, Barlesi F, Chacko R, Sebastian M, Neal J, Lu H, Cuillerot JM, Reck M (2012) Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, doubleblind, multicenter phase II study. J Clin Oncol 30(17): 2046-2054.
29. Matsumura S, Demaria S (2010) Up-regulation of the pro-inflammatory chemokine CXCL16 is a common response of tumor cells to ionizing radiation. Radiat Res 173(4): 418-425.
30. Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, Babb JS, Schneider RJ, Formenti SC, Dustin ML, Demaria S (2008) Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol 181(5): 3099-3107.
31. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, Castellano D, Choueiri TK, Gurney H, Donskov F, Bono P, Wagstaff J, Gauler TC, Ueda T, Tomita Y, Schutz FA, Kollmannsberger C, Larkin J, Ravaud A, Simon JS, Xu LA, Waxman IM, Sharma P, Check Mate I (2015) Nivolumab versus everolimus in advanced renal-cell carcinoma. N Engl J Med 373(19): 1803-1813.
32. Nesslinger NJ, Sahota RA, Stone B, Johnson K, Chima N, King C, Rasmussen D, Bishop D, Rennie PS, Gleave M, Blood P, Pai H, Ludgate C, Nelson BH (2007) Standard treatments induce antigen-specific immune responses in prostate cancer. Clin Cancer Res 13(5): 1493-1502.
33. Ouyang Y, Liu K, Hao M, Zheng R, Zhang C, Wu Y, Zhang X, Li N, Zheng J, Chen D (2015) Radiofrequency ablation-increased CXCL10 is associated with earlier recurrence of hepatocellular carcinoma by promoting stemness. Tumour Biol 373(3): 3697-3704.
34. Parikh F, Duluc D, Imai N, Clark A, Misiukiewicz K, Bonomi M, Gupta V, Patsias A, Parides M, Demicco EG, Zhang DY, Kim-Schulze S, Kao J, Gnjatic S, Oh S, Posner MR, Sikora AG (2014) Chemoradiotherapy-induced upregulation of PD-1 antagonizes immunity to HPV-related oropharyngeal cancer. Cancer Res 74(24): 7205-7216.
35. Piqueras B, Connolly J, Freitas H, Palucka AK, Banchereau J (2006) Upon viral exposure, myeloid and plasmacytoid dendritic cells produce 3 waves of distinct chemokines to recruit immune effectors. Blood 107(7): 2613-2618.
36. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, Mu Z, Rasalan T, Adamow M, Ritter E, Sedrak C, Jungbluth AA, Chua R, Yang AS, Roman RA, Rosner S, Benson B, Allison JP, Lesokhin AM, Gnjatic S, Wolchok JD (2012) Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 366(10): 925-931.
37. Prestwich RJ, Errington F, Hatfield P, Merrick AE, Ilett EJ, Selby PJ, Melcher AA (2008) The immune system-is it relevant to cancer development, progression and treatment? Clin Oncol 20(2): 101-112.
38. Rentoft M, Coates PJ, Loljung L, Wilms T, Laurell G, Nylander K (2014) Expression of CXCL10 is associated with response to radiotherapy and overall survival in squamous cell carcinoma of the tongue. Tumour Biol 35(5): 4191-4198.
39. Ribas A (2012) Tumor immunotherapy directed at PD-1. N Engl J Med 366(26): 2517-2519.
40. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, Miller ML, Rekhtman N, Moreira AL, Ibrahim F, Bruggeman C, Gasmi B, Zappasodi R, Maeda Y, Sander C, Garon EB, Merghoub T, Wolchok JD, Schumacher TN, Chan TA (2015) Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348(6230): 124-128.
41. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, Lebbe C, Baurain J-F, Testori A, Grob J-J, Davidson N, Richards J, Maio M, Hauschild A, Miller WH, Gascon P, Lotem M, Harmankaya K, Ibrahim R, Francis S, Chen T-T, Humphrey R, Hoos A, Wolchok JD (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26): 2517-2526.
42. Rossille D, Gressier M, Damotte D, Maucort-Boulch D, Pangault C, Semana G, Le Gouill S, Haioun C, Tarte K, Lamy T, Milpied N, Fest T. Groupe Ouest-Est des Leucemies et Autres Maladies du S. Groupe Ouest-Est des Leucemies et Autres Maladies du S (2014) High level of soluble programmed cell death ligand 1 in blood impacts overall survival in aggressive diffuse large B-cell lymphoma: results from a French multicenter clinical trial. Leukemia 28(12): 2367-2375.
43. Schoenfeld JD (2015) Immunity in head and neck cancer. Cancer Immunol Res 3(1): 12-17.
44. Schuler PJ, Harasymczuk M, Schilling B, Saze Z, Strauss L, Lang S, Johnson JT, Whiteside TL (2013) Effects of adjuvant chemoradiotherapy on the frequency and function of regulatory T cells in patients with head and neck cancer. Clin Cancer Res 19(23): 6585-6596.
45. Segal NH, Antonia SJ, Brahmer JR, Maio M, Blake-Haskins A, Li X, Vasselli J, Ibrahim RA, Lutzky J, Khleif S (2014) Preliminary data from a multi-arm expansion study of MEDI4736, an anti-PD-L1 antibody. J Clin Oncol 32(15): 3002.
46. Seiwert TY, Burtness B, Weiss J, Gluck I, Eder JP, Pai SI, Dolled-Filhart M, Emancipator K, Pathiraja K, Gause C, Iannone R, Brown H, Houp J, Cheng JD, Chow LQM (2014) A phase Ib study of MK-3475 in patients with human papillomavirus (HPV)-associated and non-HPV-associated head and neck (H/N) cancer. J Clin Oncol 32(15): 6011.
47. Sridharan V, Schoenfeld JD (2015) Immune effects of targeted radiation therapy for cancer. Discov Med 19(104): 219-228.
48. Srivastava R, Clump D, Ferris R (2015) Anti-PD-1 mAb pre-radiotherapy (RT) loading dose and fractionated RT induce better tumor-specific immunity and tumor shrinkage than sequential administration in an HPV+ head and neck cancer model. J Immunother Cancer 3(Suppl 2): P314.
49. Teng F, Mu D, Meng X, Kong L, Zhu H, Liu S, Zhang J, Yu J (2015) Tumor infiltrating lymphocytes (TILs) before and after neoadjuvant chemoradiotherapy and its clinical utility for rectal cancer. Am J Cancer Res 5(6): 2064-2074.
50. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, Leming PD, Spigel DR, Antonia SJ, Horn L, Drake CG, Pardoll DM, Chen L, Sharfman WH, Anders RA, Taube JM, McMiller TL, Xu H, Korman AJ, Jure-Kunkel M, Agrawal S, McDonald D, Kollia GD, Gupta A, Wigginton JM, Sznol M (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366(26): 2443-2454.
51. Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, Benci JL, Xu B, Dada H, Odorizzi PM, Herati RS, Mansfield KD, Patsch D, Amaravadi RK, Schuchter LM, Ishwaran H, Mick R, Pryma DA, Xu X, Feldman MD, Gangadhar TC, Hahn SM, Wherry EJ, Vonderheide RH, Minn AJ (2015) Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520(7547): 373-377.
52. Van Allen EM, Miao D, Schilling B, Shukla SA, Blank C, Zimmer L, Sucker A, Hillen U, Foppen MH, Goldinger SM, Utikal J, Hassel JC, Weide B, Kaehler KC, Loquai C, Mohr P, Gutzmer R, Dummer R, Gabriel S, Wu CJ, Schadendorf D, Garraway LA (2015) Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 350(6257): 207-211.
53. Wang L, Wang H, Chen H, Wang WD, Chen XQ, Geng QR, Xia ZJ, Lu Y (2015) Serum levels of soluble programmed death ligand 1 predict treatment response and progression free survival in multiple myeloma. Oncotarget 6(38): 41228-41236.
54. Wang LS, Chow KC, Li WY, Liu CC, Wu YC, Huang MH (2000) Clinical significance of serum soluble interleukin 2 receptor-alpha in esophageal squamous cell carcinoma. Clin Cancer Res 6(4): 1445-1451.
55. Wei H, Zhao L, Li W, Fan K, Qian W, Hou S, Wang H, Dai M, Hellstrom I, Hellstrom KE, Guo Y (2013) Combinatorial PD-1 blockade and CD137 activation has therapeutic efficacy in murine cancer models and synergizes with cisplatin. PloS One 8(12): e84927.
56. Wherry EJ, Kurachi M (2015) Molecular and cellular insights into T cell exhaustion. Nat Rev Immunol 15(8): 486-499.
57. Wolchok JD, Chan TA (2014) Cancer: antitumour immunity gets a boost. Nature 515(7528): 496-498.
58. Zipin-Roitman A, Meshel T, Sagi-Assif O, Shalmon B, Avivi C, Pfeffer RM, Witz IP, Ben-Baruch A (2007) CXCL10 promotes invasion-related properties in human colorectal carcinoma cells. Cancer Res 67(7): 3396-3405.