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Resiquimod As an Immunologic Adjuvant for NY-ESO-1 Protein

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Resiquimod As an Immunologic Adjuvant for NY-ESO-1 Protein Published OnlineFirst January 29, 2015; DOI: 10.1158/2326-6066.CIR-14-0202 Research Article Cancer Immunology Research Resiquimod as an Immunologic Adjuvant for NY-ESO-1 Protein Vaccination in Patients with High-Risk Melanoma Rachel Lubong Sabado1,2, Anna Pavlick1, Sacha Gnjatic2,3, Crystal M. Cruz1, Isabelita Vengco1, Farah Hasan1, Meredith Spadaccia1, Farbod Darvishian4, Luis Chiriboga4, Rose Marie Holman1, Juliet Escalon1, Caroline Muren1, Crystal Escano1, Ethel Yepes1, Dunbar Sharpe1, John P.Vasilakos5, Linda Rolnitzsky6, Judith D. Goldberg6, John Mandeli2, Sylvia Adams1, Achim Jungbluth7, Linda Pan3, Ralph Venhaus3, Patrick A. Ott1,8, and Nina Bhardwaj1,2,4 Abstract The Toll-like receptor (TLR) 7/8 agonist resiquimod has been vaccine regimens were generally well tolerated. NY-ESO-1–specific used as an immune adjuvant in cancer vaccines. We evaluated the humoral responses were induced or boosted in all patients, many safety and immunogenicity of the cancer testis antigen NY-ESO-1 of whom had high titer antibodies. In part II, 16 of 20 patients in þ þ given in combination with Montanide (Seppic) with or without both arms had NY-ESO-1–specificCD4 T-cell responses. CD8 T- resiquimod in patients with high-risk melanoma. In part I of the cell responses were only seen in 3 of 12 patients in arm B. Patients study, patients received 100 mg of full-length NY-ESO-1 protein with TLR7 SNP rs179008 had a greater likelihood of developing þ emulsified in 1.25 mL of Montanide (day 1) followed by topical NY-ESO-1–specificCD8 responses. In conclusion, NY-ESO-1 application of 1,000 mg of 0.2% resiquimod gel on days 1 and 3 protein in combination with Montanide with or without topical þ (cohort 1) versus days 1, 3, and 5 (cohort 2) of a 21-day cycle. In resiquimod is safe and induces both antibody and CD4 T-cell þ part II, patients were randomized to receive 100-mg NY-ESO-1 responses in the majority of patients; the small proportion of CD8 protein plus Montanide (day 1) followed by topical application of T-cell responses suggests that the addition of topical resiquimod to placebo gel [(arm A; n ¼ 8) or 1,000 mg of 0.2% resiquimod gel Montanide is not sufficient to induce consistent NY-ESO-1–specific þ (arm B; n ¼ 12)] using the dosing regimen established in part I. The CD8 T-cell responses. Cancer Immunol Res; 3(3); 278–87. Ó2015 AACR. Introduction responses have been observed in patients with advanced dis- ease. Induction of integrated immune responses to NY-ESO-1 NY-ESO-1 is considered widely a suitable tumor antigen for þ þ consisting of humoral and CD4 and CD8 T-cell responses vaccination due to its presence in many tumor types, its highly correlated with clinical benefitinpatientswithmelanomawho restricted expression in normal tissues, and the ability to induce received anti-CTLA4 inhibitors (2). Therefore, to achieve effec- strong spontaneous humoral and cellular immune responses þ þ tive CD4 and CD8 T-cell priming, we vaccinated individuals (1). In vitro and in vivo studies have shown that NY-ESO-1 is with the full-length recombinant NY-ESO-1 protein and eval- immunogenic with particular regions of the protein specifically þ þ uated the addition of Toll-like receptor (TLR) adjuvants to the targeted by antibodies as well as CD4 and CD8 Tcells. vaccine. Although clinical trials have demonstrated that patients have TLRs are a family of highly conserved transmembrane receptors immunity to NY-ESO-1, only a small number of clinical tumor that recognize specific molecular patterns in microbial compo- nents (3). Stimulation of different TLRs induces distinct patterns 1Cancer Institute, New York University School of Medicine, New York, of gene expression, not only activating innate immunity but also New York. 2Icahn School of Medicine at Mount Sinai Tisch Cancer directing adaptive immunity, such as the induction of a T helper 1 Institute, Boston, Massachusetts. 3Ludwig Institute for Cancer (Th1) cell response that is necessary for antitumor immune 4 Research, Boston, Massachusetts. Department of Pathology, Memo- responses (4). TLR agonists control antigen-presenting cells rial Sloan Kettering Cancer Center, New York, New York. 53M Drug Delivery Systems Division, Boston, Massachusetts. 6Division of Bio- (APC), in particular dendritic cells (DC), by triggering their statistics, NYU School of Medicine, New York, New York. 7Department maturation program, including upregulation of the expression of Pathology, Memorial Sloan Kettering Cancer Center, New York, New of human leukocyte antigen (HLA) and costimulatory molecules York. 8Dana-Farber Cancer Institute, Boston, Massachusetts. and secretion of cytokines such as TNFa, IL6, IL12, and IFNa (5). R.L. Sabado and A. Pavlick contributed equally to this article. In addition, animal models have shown that TLR agonists can Corresponding Author: Nina Bhardwaj, Tisch Cancer Institute, Icahn School of improve the efficacy of vaccines targeting self-antigens by activa- Medicine at Mount Sinai, Hess Center for Science and Medicine, 1470 Madison tion of innate immune cells and production of inflammatory Avenue, 5-116, New York, NY 10029. Phone: 212-824-8427; Fax: 646-537-9571; cytokines (6) and alter the immunosuppressive function of reg- E-mail: [email protected] ulatory T cells (Treg; ref. 7). Consequently, TLR agonists have doi: 10.1158/2326-6066.CIR-14-0202 been recognized as promising vaccine adjuvants and have been Ó2015 American Association for Cancer Research. developed for use as adjuvants for cancer vaccines in clinical trials 278 Cancer Immunol Res; 3(3) March 2015 Downloaded from cancerimmunolres.aacrjournals.org on September 27, 2021. © 2015 American Association for Cancer Research. Published OnlineFirst January 29, 2015; DOI: 10.1158/2326-6066.CIR-14-0202 NY-ESO-1 Protein and Montanide Æ Resiquimod in Melanoma (8–10). However, there is a paucity of controlled studies assessing Materials and Methods the potency of adding TLR agonists to standard adjuvants such as Study design, patients, and treatment plan Montanide (Seppic). This is a two-part study with resiquimod dose escalation in Previously, we examined the safety and immunogenicity of the part I and randomization to resiquimod versus placebo in topical TLR7 agonist imiquimod (Aldara; 3M) as an adjuvant to part II. The primary objectives of the study were safety of the NY-ESO-1 protein vaccination in patients with melanoma. vaccine regimen and assessment of humoral and cellular Although the vaccine, which was given without Montanide, þ responses to NY-ESO-1. Patients with histologically confirmed induced NY-ESO-1–specific antibodies and CD4 T-cell responses, þ resected malignant melanoma [American Joint Committee on no detectable CD8 T-cell responses were observed (11). Therefore, Cancer (AJCC) stages IIB, IIC, III, and IV] were eligible. Tumor we sought to improve upon the results of the study using another NY-ESO-1 expression was assessed by immunohistochemistry TLR agonist. Resiquimod is a TLR7/8 agonist that is chemically as previously described (21), but was not required for study related to imiquimod but has been shown to stimulate a more entry. The study (NCT00821652) was approved by the New potent immune response than imiquimod (12). In vitro studies York University School of Medicine (New York, NY) Institu- using resiquimod have shown that it can activate DC maturation by tional Review Board, and written informed consent was increasing costimulatory molecule expression and cytokine pro- obtained from all patients before enrollment. duction, and skew a Th1 cytokine profile, consequently enhancing In part I of the study, the safety of two different dosing regimens humoral and cellular immune responses (13, 14). More recently, of resiquimod was assessed in two cohorts of 3 patients each. resiquimod has been shown to promote cross-presentation of Subjects received four 3-week cycles of subcutaneous (s.c.) injec- exogenous antigens, resulting in the efficient induction of anti- þ tions with 100 mg of recombinant human NY-ESO-1 protein gen-specificCD8 T-cell responses (15). Results from animal (Ludwig Institute for Cancer Research, Boston, MA) emulsified studies have confirmed the ability of resiquimod to activate DCs in 1.25 mL Montanide (day 1) followed by topical application of (16), bias immune responses toward a predominance of Th1 cells þ 1,000 mg of resiquimod (3M Pharmaceuticals; 0.2%) gel to the (17), and enhance antigen-specificCD8 T-cell responses that can vaccination site on days 1 and 3 (cohort 1) and days 1, 3, and 5 inhibit tumor growth (18, 19). Therefore, the capacity of resiqui- (cohort 2), respectively (Fig. 1). In part II of the study, patients mod to induce local activation of immune cells, stimulate the were randomized in a blinded fashion to receive 100 mg NY-ESO-1 production of proinflammatory cytokines, and enhance antigen- protein emulsified in 1.25 mL Montanide (day 1) s.c. followed by presentation by DCs leading to activation of effective cellular topical application of placebo gel (arm A; n ¼ 8) or 1,000 mg responses are features that support its potential as a cancer vaccine of 0.2% resiquimod gel (arm B; n ¼ 12) on days 1, 3, and 5 as adjuvant (20). established in part I (Fig. 1). Study arm assignments were unblind- In this randomized study, we evaluated the safety and immu- ed after completion of the study and immune monitoring. nogenicity of vaccination with NY-ESO-1 protein emulsified in Montanide ISA-51 VG when given with or without resiquimod in Blood samples patients with resected stage IIB–IV melanoma. We observed Blood samples were collected at baseline and day 8 of each that NY-ESO-1 protein and Montanide, when given with or cycle(weeks1,4,7,and10)andduringthefirst follow-up without resiquimod, induced both humoral and cellular immune visit at weeks 12 to 14.
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