Effective melanoma immunotherapy in mice by the skin-depigmenting agent monobenzone and the adjuvants imiquimod and CpG

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  van den Boorn, Jasper G ^a   Konijnenberg, Debby ^a   Tjin, Esther P M ^a   Picavet, Daisy I ^a   Meeuwenoord, Nico J ^b   Filippov, Dmitri V ^b   van der Veen, J P Wietze ^a,d   Bos, Jan D ^a   Melief, Cornelis J M ^c   Luiten, Rosalie M ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ANTONI VAN LEEUWENHOEK HOSPITAL   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BLEACHING AGENT; CPG OLIGODEOXYNUCLEOTIDE; IMIQUIMOD; IMMUNOGLOBULIN G; MELANOMA ANTIGEN; MONOBENZONE;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; B LYMPHOCYTE; C57BL 6 MOUSE; CANCER ADJUVANT THERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DEPIGMENTATION; DISEASE FREE SURVIVAL; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL MEMORY; IMMUNOSTIMULATION; MELANOCYTE; MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROGNOSIS; VITILIGO;

ADJUVANTS, IMMUNOLOGIC; AMINOQUINOLINES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DINUCLEOSIDE PHOSPHATES; HYDROQUINONES; IMMUNOGLOBULIN G; IMMUNOTHERAPY; INJECTIONS, SUBCUTANEOUS; KILLER CELLS, NATURAL; LEUKOCYTE COUNT; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MELANOMA; MICE; MICE, INBRED C57BL; PIGMENTATION; SKIN NEOPLASMS;

MUS;

EID: 77956296196     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010626     Document Type: Article

References (48)

1. Smith JL, Jr., Stehlin JS, Jr. (1965) Spontaneous regression of primary malignant melanomas with regional metastases. Cancer 18: 1399-1415.
2. Chen KG, Leapman RD, Zhang G, Lai B, Valencia JC, et al. (2009) Influence of melanosome dynamics on melanoma drug sensitivity. J Natl Cancer Inst 101: 1259-1271. djp259 [pii];10.1093/jnci/djp259 [doi].
3. Bart RS, Porzio NR, Kopf AW, Vilcek JT, Cheng EH, et al. (1980) Inhibition of growth of B16 murine malignant melanoma by exogenous interferon. Cancer Res 40: 614-619.
4. Kirkwood JM, Strawderman MH, Ernstoff MS, Smith TJ, Borden EC, et al. (1996) Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J Clin Oncol 14: 7-17.
5. Rosenberg SA, Mule JJ, Spiess PJ, Reichert CM, Schwarz SL (1985) Regression of established pulmonary metastases and subcutaneous tumor mediated by the systemic administration of high-dose recombinant interleukin 2. J Exp Med 161: 1169-1188.
6. Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, et al. (1985) Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med 313: 1485-1492.
7. Fang L, Lonsdorf AS, Hwang ST (2008) Immunotherapy for advanced melanoma. J Invest Dermatol 128: 2596-2605.
8. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME (2008) Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 8: 299-308.
9. Overwijk WW (2005) Breaking tolerance in cancer immunotherapy: time to ACT. Curr Opin Immunol 17: 187-194.
10. Adams S, O'Neill DW, Nonaka D, Hardin E, Chiriboga L, et al. (2008)Immunization of malignant melanoma patients with full-length NY-ESO-1 protein using TLR7 agonist imiquimod as vaccine adjuvant. J Immunol 181: 776-784.
11. Lonsdorf AS, Kuekrek H, Stern BV, Boehm BO, Lehmann PV, et al. (2003) Intratumor CpG-oligodeoxynucleotide injection induces protective antitumor T cell immunity. J Immunol 171: 3941-3946.
12. Najar HM, Dutz JP (2008) Topical CpG enhances the response of murine malignant melanoma to dacarbazine. J Invest Dermatol 128: 2204-2210.
13. Redondo P, del J, Lopez-Diaz dC, Inoges S, Marquina M, et al. (2007) Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol 127: 1673-1680.
14. Sidky YA, Borden EC, Weeks CE, Reiter MJ, Hatcher JF, et al. (1992) Inhibition of murine tumor growth by an interferon-inducing imidazoquinolinamine. Cancer Res 52: 3528-3533.
15. Speiser DE, Lienard D, Rufer N, Rubio-Godoy V, Rimoldi D, et al. (2005) Rapid and strong human CD8+ T cell responses to vaccination with peptide, IFA, and CpG oligodeoxynucleotide 7909. J Clin Invest 115: 739-746.
16. Wooldridge JE, Ballas Z, Krieg AM, Weiner GJ (1997) Immunostimulatory oligodeoxynucleotides containing CpG motifs enhance the efficacy of monoclonal antibody therapy of lymphoma. Blood 89: 2994-2998.
17. Ray CM, Kluk M, Grin CM, Grant-Kels JM (2005) Successful treatment of malignant melanoma in situ with topical 5% imiquimod cream. Int J Dermatol 44: 428-434.
18. Luiten RM, Kueter EW, Mooi W, Gallee MP, Rankin EM, et al. (2005) Immunogenicity, including vitiligo, and feasibility of vaccination with autologous GM-CSF-transduced tumor cells in metastatic melanoma patients. J Clin Oncol 23: 8978-8991.
19. Gogas H, Ioannovich J, Dafni U, Stavropoulou-Giokas C, Frangia K, et al. (2006) Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 354: 709-718. 354/7/709 [pii];10.1056/NEJMoa053007 [doi].
20. Quaglino P, Marenco F, Osella-Abate S, Cappello N, Ortoncelli M, et al. (2010) Vitiligo is an independent favourable prognostic factor in stage III and IV metastatic melanoma patients: results from a single-institution hospital-based observational cohort study. Ann Oncol 21: 409-414. mdp325 [pii];10.1093/annonc/mdp325 [doi].
21. Boissy RE, Manga P (2004) On the etiology of contact/occupational vitiligo. Pigment Cell Res 17: 208-214.
22. Kahn G (1970) Depigmentation caused by phenolic detergent germicides. Arch Dermatol 102: 177-187.
23. Oliver EA, Schwartz L, Warren LH (1939) Occupational leukoderma. JAMA 113: 927.
24. Solano F, Briganti S, Picardo M, Ghanem G (2006) Hypopigmenting agents: an updated review on biological, chemical and clinical aspects. Pigment Cell Res 19: 550-571.
25. Becker SW, Jr., Spencer MC (1962) Evaluation of monobenzone. JAMA 180: 279-284.
26. Forman L (1953) A note on the depigmentary properties of monobenzylether of hydroquinone. Br J Dermatol 65: 406-409.
27. Mosher DB, Parrish JA, Fitzpatrick TB (1977) Monobenzylether of hydroquinone. A retrospective study of treatment of 18 vitiligo patients and a review of the literature. Br J Dermatol 97: 669-679.
28. Grojean MF, Thivolet J, Perrot H (1982) Acquired leukomelanoderma caused by topical depigmenting agents. Ann Dermatol Venereol 109: 641-647.
29. Lyon CC, Beck MH (1998) Contact hypersensitivity to monobenzyl ether of hydroquinone used to treat vitiligo. Contact Dermatitis 39: 132-133.
30. McGuire J, Hendee J (1971) Biochemical basis for depigmentation of skin by phenolic germicides. J Invest Dermatol 57: 256-261.
31. Manini P, Napolitano A, Westerhof W, Riley PA, d'Ischia M (2009) A Reactive ortho-Quinone Generated by Tyrosinase-Catalyzed Oxidation of the Skin Depigmenting Agent Monobenzone: Self-Coupling and Thiol-Conjugation Reactions and Possible Implications for Melanocyte Toxicity. Chem Res Toxicol.
32. Menter JM, Etemadi AA, Chapman W, Hollins TD, Willis I (1993) In vivo depigmentation by hydroxybenzene derivatives. Melanoma Res 3: 443-449.
33. Tayama K, Takahama M (2002) Depigmenting action of phenylhydroquinone, an O-phenylphenol metabolite, on the skin of JY-4 black guinea-pigs. Pigment Cell Res 15: 447-453. 2o057 [pii].
34. van den Boorn JG, Konijnenberg D, Dellemijn TA, van der Veen JP, Bos JD, et al. (2009) Autoimmune Destruction of Skin Melanocytes by Perilesional T Cells from Vitiligo Patients. J Invest Dermatol.
35. Sharma S, Karakousis CP, Takita H, Shin K, Brooks SP (2003) Intra-tumoral injection of CpG results in the inhibition of tumor growth in murine Colon-26 and B-16 tumors. Biotechnol Lett 25: 149-153.
36. Switaj T, Jalili A, Jakubowska AB, Drela N, Stoksik M, et al. (2004) CpG immunostimulatory oligodeoxynucleotide 1826 enhances antitumor effect of interleukin 12 gene-modified tumor vaccine in a melanoma model in mice. Clin Cancer Res 10: 4165-4175. 10.1158/1078-0432.CCR-04-0022 [doi];10/12/4165 [pii].
37. Berghofer B, Haley G, Frommer T, Bein G, Hackstein H (2007) Natural and synthetic TLR7 ligands inhibit CpG-A- and CpG-C-oligodeoxynucleotideinduced IFN-alpha production. J Immunol 178: 4072-4079.
38. Liu C, Lou Y, Lizee G, Qin H, Liu S, et al. (2008) Plasmacytoid dendritic cells induce NK cell-dependent, tumor antigen-specific T cell cross-priming and tumor regression in mice. J Clin Invest 118: 1165-1175.
39. Schuurhuis DH, van Montfoort N, Ioan-Facsinay A, Jiawan R, Camps M, et al. (2006) Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. J Immunol 176: 4573-4580.
40. van den Boorn JG, Le Poole IC, Luiten RM (2006) T-cell avidity and tuning: the flexible connection between tolerance and autoimmunity. Int Rev Immunol 25: 235-258.
41. Nazih A, Benezra C, Lepoittevin JP (1993) Bihaptens with 5- and 6-methylsubstituted alkylcatechols and methylene lactone functional groups: tools for hapten (allergen or tolerogen)-protein interaction studies. Chem Res Toxicol 6: 215-222.
42. Palm NW, Medzhitov R (2009) Immunostimulatory activity of haptenated proteins. Proc Natl Acad Sci U S A 106: 4782-4787.
43. Hariharan V, Klarquist J, Reust MJ, Koshoffer A, McKee MD, et al. (2009) Monobenzyl Ether of Hydroquinone and 4-Tertiary Butyl Phenol Activate Markedly Different Physiological Responses in Melanocytes: Relevance to Skin Depigmentation. J Invest Dermatol; jid2009214 [pii];10.1038/jid.2009.214[doi].
44. Cormier JN, Abati A, Fetsch P, Hijazi YM, Rosenberg SA, et al. (1998) Comparative analysis of the in vivo expression of tyrosinase, MART-1/Melan- A, and gp100 in metastatic melanoma lesions: implications for immunotherapy. J Immunother 21: 27-31.
45. Anbar TS, Abdel-Raouf H, Awad SS, Ragaie MH, Abdel-Rahman AT (2009) The hair follicle melanocytes in vitiligo in relation to disease duration. J Eur Acad Dermatol Venereol 23: 934-939. JDV3233 [pii];10.1111/j.1468-3083.2009.03233.x [doi].
46. Meyer KC, Klatte JE, Dinh HV, Harries MJ, Reithmayer K, et al. (2008) Evidence that the bulge region is a site of relative immune privilege in human hair follicles. Br J Dermatol 159: 1077-1085. BJD8818 [pii];10.1111/j.1365-2133.2008.08818.x [doi].
47. Ruckert R, Hofmann U, van der Veen C, Bulfone-Paus S, Paus R (1998) MHC class I expression in murine skin: developmentally controlled and strikingly restricted intraepithelial expression during hair follicle morphogenesis and cycling, and response to cytokine treatment in vivo. J Invest Dermatol 111: 25-30. 10.1046/j.1523-1747.1998.00228.x [doi].
48. Khan S, Bijker MS, Weterings JJ, Tanke HJ, Adema GJ, et al. (2007) Distinct uptake mechanisms but similar intracellular processing of two different toll-like receptor ligand-peptide conjugates in dendritic cells. J Biol Chem 282: 21145-21159.