The alarmin HMGN1 contributes to antitumor immunity and is a potent immunoadjuvant

Cancer Research

Volumn 74, Issue 21, 2014, Pages 5989-5998

  Wei, Feng ^a,b   Yang, De ^a,b   Tewary, Poonam ^a   Li, Yana ^a   Li, Sandra ^a   Chen, Xin ^a   Howard, O M Zack ^a   Bustin, Michael ^c   Oppenheim, Joost J ^a  

^a FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GLYCOPROTEIN GP 100; HIGH MOBILITY GROUP N1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; HYBRID PROTEIN; IMMUNOLOGICAL ADJUVANT; MELANOCYTE PROTEIN PMEL 17; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DNA IMMUNIZATION; GENE GUN; HOST RESISTANCE; IN VIVO STUDY; MELANOMA B16; MOUSE; NONHUMAN; TH1 CELL; THYMOMA; TUMOR GROWTH; ANIMAL; ANTIGEN PRESENTING CELL; EXPERIMENTAL MELANOMA; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; PATHOLOGY; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGEN-PRESENTING CELLS; CD8-POSITIVE T-LYMPHOCYTES; GP100 MELANOMA ANTIGEN; HMGN1 PROTEIN; HUMANS; IMMUNITY, CELLULAR; MELANOMA, EXPERIMENTAL; MICE; RECOMBINANT FUSION PROTEINS; TOLL-LIKE RECEPTOR 4; VACCINATION;

EID: 84909639439     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2042     Document Type: Article

References (43)

1. Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L, et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J Clin Oncol 1999;17:2639-48.
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
3. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011;480:480-9.
4. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15.
5. Gajewski TF, Meng Y, Blank C, Brown I, Kacha A, Kline J, et al. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev 2006;213:131-45.
6. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 2005;17:359-65.
7. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007;81:1-5.
8. Yang D, Tewary P, de la Rosa G, Wei F, Oppenheim JJ. The alarmin functions of high-mobility group proteins. Biochim Biophys Acta 2010;1799:157-63.
9. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ. Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 2004;22:181-315.
10. Lillard JW Jr, Boyaka PN, Chertov O, Oppenheim JJ, McGhee JR. Mechanisms for induction of acquired host immunity by neutrophil peptide defensins. Proc Natl Acad Sci U S A 1999;96:651-6.
11. Yang D, Chertov O, Bykovskaia SN, Chen Q, Buffo MJ, Shogan J, et al. b-Defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 1999;286:525-8.
12. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, Chertov O, et al. Toll-like receptor 4-dependent activation of dendritic cells by b-defensin 2. Science 2002;298:1025-9.
13. Kurosaka K, Chen Q, Yarovinsky F, Oppenheim JJ, Yang D. Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J Immunol 2005;174: 6257-65.
14. Yang D, Chen Q, Su SB, Zhang P, Kurosaka K, Caspi RR, et al. Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J Exp Med 2008;205:79-90.
15. Rovere-Querini P, Capobianco A, Scaffidi P, Valentinis B, Catalanotti F, Giazzon M, et al. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep 2004;5:825-30.
16. Urbonaviciute V, Furnrohr BG, Meister S, Munoz L, Heyder P, De Marchis F, et al. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J Exp Med 2008;205:3007-18.
17. Quintana FJ, Cohen IR. Heat shock proteins as endogenous adjuvants in sterile and septic inflammation. J Immunol 2005;175:2777-82.
18. Tewary P, Yang D, de la Rosa G, Li Y, Finn MW, Krensky AM, et al. Granulysin activates antigen-presenting cells through TLR4 and acts as an immune alarmin. Blood 2010;116:3465-74.
19. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007;13: 1042-9.
20. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003;425:516-21.
21. Kool M, Willart MA, van Nimwegen M, Bergen I, Pouliot P, Virchow JC, et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 2011;34:527-40.
22. Lande R, Gregorio J, Facchinetti V, Chatterjee B, Wang YH, Homey B, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007;449:564-9.
23. Gregorio J, Meller S, Conrad C, Di Nardo A, Homey B, Lauerma A, et al. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med 2010;207:2921-30.
24. Flohe SB, Bruggemann J, Lendemans S, Nikulina M, Meierhoff G, Flohe S, et al. Human heat shock protein 60 induces maturation of dendritic cells versus a Th1-promoting phenotype. J Immunol 2003;170:2340-8.
25. Yang D, Postnikov YV, Li Y, Tewary P, de la Rosa G, Wei F, et al. Highmobility group nucleosome-binding protein 1 acts as an alarmin and is critical for lipopolysaccharide-induced immune responses. J Exp Med 2012;209:157-71.
26. Robinson HL, Pertmer TM. Nucleic acid immunizations. Curr Protoc Immunol 2001;27:2.14.1-2.
27. Palmer DC, Balasubramaniam S, Hanada K, Wrzesinski C, Yu Z, Farid S, et al. Vaccine-stimulated, adoptively transferred CD8+ T cells traffic indiscriminately and ubiquitously while mediating specific tumor destruction. J Immunol 2004;173:7209-16.
28. MooreMW,Carbone FR, Bevan MJ. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988;54:777-85.
29. Biragyn A, Surenhu M, Yang D, Ruffini PA, Haines BA, Klyushnenkova E, et al. Mediators of innate immunity that target immature, but not mature, dendritic cells induce antitumor immunity when genetically fused with nonimmunogenic tumor antigens. J Immunol 2001;167: 6644-53.
30. Hock R, Furusawa T, Ueda T, Bustin M.HMGchromosomal proteins in development and disease. Trends Cell Biol 2007;17:72-9.
31. Birger Y, West KL, Postnikov YV, Lim JH, FurusawaT, Wagner JP, et al. Chromosomal protein HMGN1 enhances the rate of DNA repair in chromatin. EMBO J 2003;22:1665-75.
32. Birger Y, Catez F, Furusawa T, Lim JH, Prymakowska-Bosak M, West KL, et al. Increased tumorigenicity and sensitivity to ionizing radiation upon loss of chromosomal protein HMGN1. Cancer Res 2005;65: 6711-8.
33. Bonifaz L, Bonnyay D, Mahnke K, Rivera M, Nussenzweig MC, Steinman RM. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med 2002;196:1627-38.
34. Ma XT, Xu B, An LL, Dong CY, Lin YM, Shi Y, et al. Vaccine with betadefensin 2-transduced leukemic cells activates innate and adaptive immunity to elicit potent antileukemia responses. Cancer Res 2006;66:1169-76.
35. Wang L, Rollins L, Gu Q, Chen SY, Huang XF. A Mage3/heat shock protein70 DNA vaccine induces both innate and adaptive immune responses for the antitumor activity. Vaccine 2009;28:561-70.
36. Chang CL, Tsai YC, He L, Wu TC, Hung CF. Cancer immunotherapy using irradiated tumor cells secreting heat shock protein 70. Cancer Res 2007;67:10047-57.
37. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007;13:1050-9.
38. Biragyn A, Ruffini PA, Coscia M, Harvey LK, Neelapu SS, Baskar S, et al. Chemokine receptor-mediated delivery directs self-tumor antigen efficiently into the class II processing pathway in vitro and induces protective immunity in vivo. Blood 2004;104:1961-9.
39. Messmer D, Yang H, Telusma G, Knoll F, Li J, Messmer B, et al. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 2004;173:307-13.
40. Kuppner MC, Gastpar R, Gelwer S, Nossner E, Ochmann O, Scharner A, et al. The role of heat shock protein (hsp70) in dendritic cell maturation: hsp70 induces the maturation of immature dendritic cells but reduces DC differentiation from monocyte precursors. Eur J Immunol 2001;31:1602-9.
41. Yang D, Chen Q, Yang H, Tracey KJ, Bustin M, Oppenheim JJ. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J Leukoc Biol 2007;81:59-66.
42. Wu Z, Hoover DM, Yang D, Boulegue C, Santamaria F, Oppenheim JJ, et al. Engineering disulfide bridges to dissect antimicrobial and chemotactic activities of human b-defensin 3. Proc Natl Acad Sci U S A 2003;100:8880-5.
43. Venereau E, Casalgrandi M, Schiraldi M, Antoine DJ, Cattaneo A, De Marchis F, et al. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J Exp Med 2012;209:1519-28.