Contribution of humoral immune responses to the antitumor effects mediated by anthracyclines

Cell Death and Differentiation

Volumn 21, Issue 1, 2014, Pages 50-58

  Hannani, D ^a,b   Locher, C ^a,b   Yamazaki, T ^a,b   Colin Minard, V ^a,c   Vetizou, M ^a,b   Aymeric, L ^a,b   Viaud, S ^a,b   Sanchez, D ^d   Smyth, M J ^e,f   Bruhns, P ^g,h   Kroemer, G ^a,i,j,k,l   Zitvogel, L ^a,b,m  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c University of Paris Sud XI ^*  (France)

^d INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g INSTITUT PASTEUR   (France)

^h INSERM   (France)

ⁱ Institut Gustave Roussy   (France)

^j UNIVERSITÉ PARIS DESCARTES   (France)

^k CENTRE DE RECHERCHE DES CORDELIERS   (France)

^l HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^m Center of Clinical Investigations in Biotherapies of Cancer (CICBT)   (France)

more..

Author keywords

antibodies; cancer; chemotherapy; FcgR; humoral immunity; immunogenic cell death

Indexed keywords

ANTHRACYCLINE; AUTOANTIGEN; CALRETICULIN; CD20 ANTIBODY; CYCLOPHOSPHAMIDE; DOCETAXEL; DOXORUBICIN; EPIRUBICIN; FC RECEPTOR; FLUOROURACIL; IMMUNOGLOBULIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN RECEPTOR; NAVELBINE;

ADJUVANT THERAPY; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY TITER; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; B LYMPHOCYTE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG EFFICACY; ENDOPLASMIC RETICULUM STRESS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FOLLOW UP; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; SARCOMA; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE;

MUS;

ANIMALS; ANTHRACYCLINES; ANTIBODIES; ANTINEOPLASTIC AGENTS; APOPTOSIS; B-LYMPHOCYTES; BREAST NEOPLASMS; CALRETICULIN; CELL LINE, TUMOR; FEMALE; HUMANS; IMMUNITY, HUMORAL; MICE; MICE, INBRED C57BL; MIDDLE AGED; RECEPTORS, FC; SARCOMA; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84890071556     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.60     Document Type: Article

References (60)

1. Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G. Prognostic and predictive impact of intra- And peritumoral immune infiltrates. Cancer Res 2011; 71: 5601-5605.
2. Hanahan D, Weinberg RA. Hallmarks of cancer: The next generation. Cell 2011; 144: 646-674.
3. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007; 449: 419-426.
4. Balkwill F, Charles KA, Mantovani A. Smoldering and polarized inflammation in the initiation and promotion of malignant disease. Cancer Cell 2005; 7: 211-217.
5. Hanahan D, Coussens LM. Accessories to the crime: Functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309-322.
6. Pillai S, Mattoo H, Cariappa A. B cells and autoimmunity. Curr Opin Immunol 2011; 23: 721-731.
7. Tanchot C, Terme M, Pere H, Tran T, Benhamouda N, Strioga M et al. Tumor-infiltrating regulatory T cells: Phenotype, role, mechanism of expansion in situ and clinical significance. Cancer Microenviron 2013; 6: 147-157.
8. Andreu P, Johansson M, Affara NI, Pucci F, Tan T, Junankar S et al. FcRgamma activation regulates inflammation-Associated squamous carcinogenesis. Cancer Cell 2010; 17: 121-134.
9. de Visser KE, Korets LV, Coussens LM. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005; 7: 411-423.
10. Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S et al. B regulatory cells and the tumor-promoting actions of TNF-Alpha during squamous carcinogenesis. Proc Natl Acad Sci USA 2011; 108: 10662-10667.
11. Ammirante M, Luo JL, Grivennikov S, Nedospasov S, Karin M. B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010; 464: 302-305.
12. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16: 91-102.
13. Kroemer G, Galluzzi L, Kepp O, Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013; 31: 51-72.
14. Ruffell B, Au A, Rugo HS, Esserman LJ, Hwang ES, Coussens LM. Leukocyte composition of human breast cancer. Proc Natl Acad Sci USA 2012; 109: 2796-2801.
15. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011; 1: 54-67.
16. Ma Y, Aymeric L, Locher C, Mattarollo SR, Delahaye NF, Pereira P et al. Contribution of IL-17-producing gamma delta T cells to the efficacy of anticancer chemotherapy. J Exp Med 2011; 208: 491-503.
17. Ma Y, Adjemian S, Mattarollo SR, Yamazaki T, Aymeric L, Yang H et al. Anticancer chemotherapy-induced intratumoral recruitment and differentiation of antigen-presenting cells. Immunity 2013; 38: 729-741.
18. Angeli V, Ginhoux F, Llodra J, Quemeneur L, Frenette PS, Skobe M et al. B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 2006; 24: 203-215.
19. Horikawa M, Minard-Colin V, Matsushita T, Tedder TF. Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J Clin Invest 2011; 121: 4268-4280.
20. Minard-Colin V, Xiu Y, Poe JC, Horikawa M, Magro CM, Hamaguchi Y et al. Lymphoma depletion during CD20 immunotherapy in mice is mediated by macrophage FcgammaRI, FcgammaRIII, and FcgammaRIV. Blood 2008; 112: 1205-1213.
21. Bruhns P. Properties of mouse and human IgG receptors and their contribution to disease models. Blood 2012; 119: 5640-5649.
22. Hazenbos WL, Gessner JE, Hofhuis FM, Kuipers H, Meyer D, Heijnen IA et al. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity 1996; 5: 181-188.
23. Ioan-Facsinay A, de Kimpe SJ, Hellwig SM, van Lent PL, Hofhuis FM, van Ojik HH et al. FcgammaRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 2002; 16: 391-402.
24. Nimmerjahn F, Lux A, Albert H, Woigk M, Lehmann C, Dudziak D et al. FcgammaRIV deletion reveals its central role for IgG2a and IgG2b activity in vivo. Proc Natl Acad Sci USA 2010; 107: 19396-19401.
25. Mancardi DA, Iannascoli B, Hoos S, England P, Daeron M, Bruhns P. FcgammaRIV is a mouse IgE receptor that resembles macrophage FcepsilonRI in humans and promotes IgE-induced lung inflammation. J Clin Invest 2008; 118: 3738-3750.
26. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994; 76: 519-529.
27. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 2008; 9: 1179-1188.
28. Behler F, Steinwede K, Balboa L, Ueberberg B, Maus R, Kirchhof G et al. Role of Mincle in alveolar macrophage-dependent innate immunity against mycobacterial infections in mice. J Immunol 2012; 189: 3121-3129.
29. Galluzzi L, Kepp O, Kroemer G. Enlightening the impact of immunogenic cell death in photodynamic cancer therapy. EMBO J 2012; 31: 1055-1057.
30. Eric-Nikolic A, Milovanovic Z, Sanchez D, Pekarikova A, Dzodic R, Matic IZ et al. Overexpression of calreticulin in malignant and benign breast tumors: Relationship with humoral immunity. Oncology 2012; 82: 48-55.
31. Weber JS, Hamid O, Chasalow SD, Wu DY, Parker SM, Galbraith S et al. Ipilimumab increases activated T cells and enhances humoral immunity in patients with advanced melanoma. J Immunother 2012; 35: 89-97.
32. Yuan J, Adamow M, Ginsberg BA, Rasalan TS, Ritter E, Gallardo HF et al. Integrated NY-ESO-1 antibody and CD8+ T cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci USA 2011; 108: 16723-16728.
33. Valmori D, Souleimanian NE, Tosello V, Bhardwaj N, Adams S, O'Neill D et al. Vaccination with NY-ESO-1 protein and CpG in Montanide induces integrated antibody/Th1 responses and CD8 T cells through cross-priming. Proc Natl Acad Sci USA 2007; 104: 8947-8952.
34. Jinushi M, Hodi FS, Dranoff G. Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc Natl Acad Sci USA 2006; 103: 9190-9195.
35. Schoenfeld J, Jinushi M, Nakazaki Y, Wiener D, Park J, Soiffer R et al. Active immunotherapy induces antibody responses that target tumor angiogenesis. Cancer Res 2010; 70: 10150-10160.
36. Hodi FS, Butler M, Oble DA, Seiden MV, Haluska FG, Kruse A et al. Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-Associated antigen 4 in previously vaccinated cancer patients. Proc Natl Acad Sci USA 2008; 105: 3005-3010.
37. Fonseca C, Soiffer R, Ho V, Vanneman M, Jinushi M, Ritz J et al. Protein disulfide isomerases are antibody targets during immune-mediated tumor destruction. Blood 2009; 113: 1681-1688.
38. Hodi FS, Schmollinger JC, Soiffer RJ, Salgia R, Lynch T, Ritz J et al. ATP6S1 elicits potent humoral responses associated with immune-mediated tumor destruction. Proc Natl Acad Sci USA 2002; 99: 6919-6924.
39. Erdag G, Schaefer JT, Smolkin ME, Deacon DH, Shea SM, Dengel LT et al. Immunotype and immunohistologic characteristics of tumor-infiltrating immune cells are associated with clinical outcome in metastatic melanoma. Cancer Res 2012; 72: 1070-1080.
40. Martinet L, Garrido I, Girard JP. Tumor high endothelial venules (HEVs) predict lymphocyte infiltration and favorable prognosis in breast cancer. Oncoimmunology 2012; 1: 789-790.
41. Martinet L, Le Guellec S, Filleron T, Lamant L, Meyer N, Rochaix P et al. High endothelial venules (HEVs) in human melanoma lesions: Major gateways for tumor-infiltrating lymphocytes. Oncoimmunology, 2012; 1: 829-839.
42. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V et al. Long-Term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 2008; 26: 4410-4417.
43. Haas KM, Poe JC, Steeber DA, Tedder TF. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 2005; 23: 7-18.
44. Reuschenbach M, von Knebel Doeberitz M, Wentzensen N. A systematic review of humoral immune responses against tumor antigens. Cancer Immunol Immunother 2009; 58: 1535-1544.
45. Albanesi M, Mancardi DA, Macdonald LE, Iannascoli B, Zitvogel L, Murphy AJ et al. Cutting edge: FcgammaRIII (CD16) and FcgammaRI (CD64) are responsible for anti-glycoprotein 75 monoclonal antibody TA99 therapy for experimental metastatic B16 melanoma. J Immunol 2012; 189: 5513-5517.
46. Lejeune J, Thibault G, Ternant D, Cartron G, Watier H, Ohresser M. Evidence for linkage disequilibrium between Fcgamma RIIIa-V158F and Fcgamma RIIa-H131R polymorphisms in white patients, and for an Fcgamma RIIIa-restricted influence on the response to therapeutic antibodies. J Clin Oncol 2008; 26: 5489-5491; author reply 91-2.
47. Boehm J, Orth T, Van Nguyen P, Soling HD. Systemic lupus erythematosus is associated with increased auto-Antibody titers against calreticulin and grp94, but calreticulin is not the Ro/SS-A antigen. Eur J Clin Invest 1994; 24: 248-257.
48. El Aswad Bel D, Doenhoff MJ, El Hadidi AS, Schwaeble WJ, Lynch NJ. Use of recombinant calreticulin and cercarial transformation fluid (CTF) in the serodiagnosis of Schistosoma mansoni. Immunobiology 2011; 216: 379-385.
49. Watanabe K, Ohira H, Orikasa H, Saito K, Kanno K, Shioya Y et al. Anti-calreticulin antibodies in patients with inflammatory bowel disease. Fukushima J Med Sci 2006; 52: 1-11.
50. Winter JA, Davies OR, Brown AP, Garnett MC, Stolnik S, Pritchard DI. The assessment of hookworm calreticulin as a potential vaccine for necatoriasis. Parasite Immunol 2005; 27: 139-146.
51. Kreisel W, Siegel A, Bahler A, Spamer C, Schiltz E, Kist M et al. High prevalence of antibodies to calreticulin of the IgA class in primary biliary cirrhosis: A possible role of gut-derived bacterial antigens in its aetiology? Scand J Gastroenterol 1999; 34: 623-628.
52. Pekarikova A, Sanchez D, Palova-Jelinkova L, Simsova M, Benes Z, Hoffmanova I et al. Calreticulin is a B cell molecular target in some gastrointestinal malignancies. Clin Exp Immunol 2010; 160: 215-222.
53. Sanchez D, Palova-Jelinkova L, Felsberg J, Simsova M, Pekarikova A, Pecharova B et al. Anti-calreticulin immunoglobulin A (IgA) antibodies in refractory coeliac disease. Clin Exp Immunol 2008; 153: 351-359.
54. Abe K, Ohira H, Kobayashi H, Saito H, Takahashi A, Rai T et al. Breakthrough of immune self-Tolerance to calreticulin induced by CpG-oligodeoxynucleotides as adjuvant. Fukushima J Med Sci 2007; 53: 95-108.
55. Ribeiro CH, Lopez NC, Ramirez GA, Valck CE, Molina MC, Aguilar L et al. Trypanosoma cruzi calreticulin: A possible role in Chagas' disease autoimmunity. Mol Immunol 2009; 46: 1092-1099.
56. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC et al. Mechanisms of pre-Apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009; 28: 578-590.
57. Tufi R, Panaretakis T, Bianchi K, Criollo A, Fazi B, Di Sano F et al. Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ 2008; 15: 274-282.
58. Ladoire S, Chaba K, Martins I, Sukkurwala AQ, Adjemian S, Michaud M et al. Immunohistochemical detection of cytoplasmic LC3 puncta in human cancer specimens. Autophagy 2012; 8: 1175-1184.
59. Hamaguchi Y, Xiu Y, Komura K, Nimmerjahn F, Tedder TF. Antibody isotype-specific engagement of Fcgamma receptors regulates B lymphocyte depletion during CD20 immunotherapy. J Exp Med 2006; 203: 743-753.
60. Sanchez D, Tuckova L, Mothes T, Kreisel W, Benes Z, Tlaskalova-Hogenova H. Epitopes of calreticulin recognised by IgA autoantibodies from patients with hepatic and coeliac disease. J Autoimmun 2003; 21: 383-392.