International Immunology, Vol. 12, No. 11, 1539-1546,
November 2000
© 2000 Japanese Society for Immunology
Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-
B pathway
Center for Immunotherapy of Cancer and Infectious Diseases, University of Connecticut School of Medicine, MC1601, Farmington, CT 06030-1601, USA
Correspondence to: P. K. Srivastava
Dendritic cells (DC) are key components of innate and adaptive immune responses. The identity of endogenous signals that activate DC is a crucial and unresolved question. We report here that heat shock proteins (HSP), the most abundant and conserved mammalian molecules, constitute such an internal signal. Necrotic but not apoptotic cell death leads to release of HSP gp96, calreticulin, hsp90 and hsp70. HSP stimulate macrophages to secrete cytokines, and induce expression of antigen-presenting and co-stimulatory molecules on the DC. The HSP gp96 and hsp70 act differentially, and each induces some but not all molecules. HSP interact with these antigen-presenting cells through the highly conserved NF-
B pathway. As HSP are intracellular, abundant and soluble, their presence in the extra-cellular milieu and the consequent activation of antigen-presenting cells (APC) constitutes an excellent mechanism for response to cell death. As HSP are conserved from bacteria to mammals, the ability of HSP to activate APC provides a unified mechanism for response to internal and external stimuli.
Keywords: cytokines, hsp70, hsp90, innate immunity, gp96
1 Present address: Apt A101 Osaki Houfu, Yamaguchi 747, Japan.
Transmitting editor: S. H. E. Kaufmann
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Y. Bulut, K. S. Michelsen, L. Hayrapetian, Y. Naiki, R. Spallek, M. Singh, and M. Arditi Mycobacterium Tuberculosis Heat Shock Proteins Use Diverse Toll-like Receptor Pathways to Activate Pro-inflammatory Signals J. Biol. Chem., June 3, 2005; 280(22): 20961 - 20967. [Abstract] [Full Text] [PDF]
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E. Yu. Nikitina, S. A. Desai, X. Zhao, W. Song, A. Z. Luo, R. D. Gangula, K. M. Slawin, and D. M. Spencer Versatile Prostate Cancer Treatment with Inducible Caspase and Interleukin-12 Cancer Res., May 15, 2005; 65(10): 4309 - 4319. [Abstract] [Full Text] [PDF]
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L. Pilla, P. Squarcina, J. Coppa, V. Mazzaferro, V. Huber, D. Pende, C. Maccalli, G. Sovena, L. Mariani, C. Castelli, et al. Natural Killer and NK-Like T-Cell Activation in Colorectal Carcinoma Patients Treated with Autologous Tumor-Derived Heat Shock Protein 96 Cancer Res., May 1, 2005; 65(9): 3942 - 3949. [Abstract] [Full Text] [PDF]
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S. Demaria, F. R. Santori, B. Ng, L. Liebes, S. C. Formenti, and S. Vukmanovic Select forms of tumor cell apoptosis induce dendritic cell maturation J. Leukoc. Biol., March 1, 2005; 77(3): 361 - 368. [Abstract] [Full Text] [PDF]
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F. Rharbaoui, D. Bruder, M. Vidakovic, T. Ebensen, J. Buer, and C. A. Guzman Characterization of a B220+ Lymphoid Cell Subpopulation with Immune Modulatory Functions in Nasal-Associated Lymphoid Tissues J. Immunol., February 1, 2005; 174(3): 1317 - 1324. [Abstract] [Full Text] [PDF]
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S. J. Prasad, K. J. Farrand, S. A. Matthews, J. H. Chang, R. S. McHugh, and F. Ronchese Dendritic Cells Loaded with Stressed Tumor Cells Elicit Long-Lasting Protective Tumor Immunity in Mice Depleted of CD4+CD25+ Regulatory T Cells J. Immunol., January 1, 2005; 174(1): 90 - 98. [Abstract] [Full Text] [PDF]
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B. Berwin, Y. Delneste, R. V. Lovingood, S. R. Post, and S. V. Pizzo SREC-I, a Type F Scavenger Receptor, Is an Endocytic Receptor for Calreticulin J. Biol. Chem., December 3, 2004; 279(49): 51250 - 51257. [Abstract] [Full Text] [PDF]
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A. Osterloh, F. Meier-Stiegen, A. Veit, B. Fleischer, A. von Bonin, and M. Breloer Lipopolysaccharide-free Heat Shock Protein 60 Activates T Cells J. Biol. Chem., November 12, 2004; 279(46): 47906 - 47911. [Abstract] [Full Text] [PDF]
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J. J. Lewis Therapeutic cancer vaccines: Using unique antigens PNAS, October 5, 2004; 101(suppl_2): 14653 - 14656. [Abstract] [Full Text] [PDF]
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K. Tang, H. B. Rossiter, P. D. Wagner, and E. C. Breen Lung-targeted VEGF inactivation leads to an emphysema phenotype in mice J Appl Physiol, October 1, 2004; 97(4): 1559 - 1566. [Abstract] [Full Text] [PDF]
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W. Ren, R. Strube, X. Zhang, S.-Y. Chen, and X. F. Huang Potent Tumor-Specific Immunity Induced by an In vivo Heat Shock Protein-Suicide Gene-Based Tumor Vaccine Cancer Res., September 15, 2004; 64(18): 6645 - 6651. [Abstract] [Full Text] [PDF]
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G. Nagy, M. Barcza, N. Gonchoroff, P. E. Phillips, and A. Perl Nitric Oxide-Dependent Mitochondrial Biogenesis Generates Ca2+ Signaling Profile of Lupus T Cells J. Immunol., September 15, 2004; 173(6): 3676 - 3683. [Abstract] [Full Text] [PDF]
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M.-F. Tsan and B. Gao Endogenous ligands of Toll-like receptors J. Leukoc. Biol., September 1, 2004; 76(3): 514 - 519. [Abstract] [Full Text] [PDF]
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D. SenGupta, P. J. Norris, T. J. Suscovich, M. Hassan-Zahraee, H. F. Moffett, A. Trocha, R. Draenert, P. J. R. Goulder, R. J. Binder, D. L. Levey, et al. Heat Shock Protein-Mediated Cross-Presentation of Exogenous HIV Antigen on HLA Class I and Class II J. Immunol., August 1, 2004; 173(3): 1987 - 1993. [Abstract] [Full Text] [PDF]
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D. Messmer, H. Yang, G. Telusma, F. Knoll, J. Li, B. Messmer, K. J. Tracey, and N. Chiorazzi High Mobility Group Box Protein 1: An Endogenous Signal for Dendritic Cell Maturation and Th1 Polarization J. Immunol., July 1, 2004; 173(1): 307 - 313. [Abstract] [Full Text] [PDF]
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A. D. H. Doody, J. T. Kovalchin, M. A. Mihalyo, A. T. Hagymasi, C. G. Drake, and A. J. Adler Glycoprotein 96 Can Chaperone Both MHC Class I- and Class II-Restricted Epitopes for In Vivo Presentation, but Selectively Primes CD8+ T Cell Effector Function J. Immunol., May 15, 2004; 172(10): 6087 - 6092. [Abstract] [Full Text] [PDF]
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T. B. Jones, D. P. Ankeny, Z. Guan, V. McGaughy, L. C. Fisher, D. M. Basso, and P. G. Popovich Passive or Active Immunization with Myelin Basic Protein Impairs Neurological Function and Exacerbates Neuropathology after Spinal Cord Injury in Rats J. Neurosci., April 14, 2004; 24(15): 3752 - 3761. [Abstract] [Full Text] [PDF]
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J. C. Baker-LePain, M. Sarzotti, and C. V. Nicchitta Glucose-Regulated Protein 94/Glycoprotein 96 Elicits Bystander Activation of CD4+ T Cell Th1 Cytokine Production In Vivo J. Immunol., April 1, 2004; 172(7): 4195 - 4203. [Abstract] [Full Text] [PDF]
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K. Kariko, H. Ni, J. Capodici, M. Lamphier, and D. Weissman mRNA Is an Endogenous Ligand for Toll-like Receptor 3 J. Biol. Chem., March 26, 2004; 279(13): 12542 - 12550. [Abstract] [Full Text] [PDF]
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C. Massa, C. Guiducci, I. Arioli, M. Parenza, M. P. Colombo, and C. Melani Enhanced Efficacy of Tumor Cell Vaccines Transfected with Secretable hsp70 Cancer Res., February 15, 2004; 64(4): 1502 - 1508. [Abstract] [Full Text] [PDF]
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B. Liu, J. Dai, H. Zheng, D. Stoilova, S. Sun, and Z. Li Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases PNAS, December 23, 2003; 100(26): 15824 - 15829. [Abstract] [Full Text] [PDF]
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X. F. Huang, W. Ren, L. Rollins, P. Pittman, M. Shah, L. Shen, Q. Gu, R. Strube, F. Hu, and S.-Y. Chen A Broadly Applicable, Personalized Heat Shock Protein-Mediated Oncolytic Tumor Vaccine Cancer Res., November 1, 2003; 63(21): 7321 - 7329. [Abstract] [Full Text] [PDF]
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M. H. Manjili, X.-Y. Wang, X. Chen, T. Martin, E. A. Repasky, R. Henderson, and J. R. Subjeck HSP110-HER2/neu Chaperone Complex Vaccine Induces Protective Immunity Against Spontaneous Mammary Tumors in HER-2/neu Transgenic Mice J. Immunol., October 15, 2003; 171(8): 4054 - 4061. [Abstract] [Full Text] [PDF]
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N. Jiang, C. F. Reich III, and D. S. Pisetsky Role of macrophages in the generation of circulating blood nucleosomes from dead and dying cells Blood, September 15, 2003; 102(6): 2243 - 2250. [Abstract] [Full Text] [PDF]
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S. Basu and P. K. Srivastava Fever-like temperature induces maturation of dendritic cells through induction of hsp90 Int. Immunol., September 1, 2003; 15(9): 1053 - 1061. [Abstract] [Full Text] [PDF]
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R. C. Reed, B. Berwin, J. P. Baker, and C. V. Nicchitta GRP94/gp96 Elicits ERK Activation in Murine Macrophages: A ROLE FOR ENDOTOXIN CONTAMINATION IN NF-{kappa}B ACTIVATION AND NITRIC OXIDE PRODUCTION J. Biol. Chem., August 22, 2003; 278(34): 31853 - 31860. [Abstract] [Full Text] [PDF]
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A. N. Rad, G. Pollara, S. M. A. Sohaib, C. Chiang, B. M. Chain, and D. R. Katz The Differential Influence of Allogeneic Tumor Cell Death via DNA Damage on Dendritic Cell Maturation and Antigen Presentation Cancer Res., August 15, 2003; 63(16): 5143 - 5150. [Abstract] [Full Text] [PDF]
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Y. Zeng, H. Feng, M. W. Graner, and E. Katsanis Tumor-derived, chaperone-rich cell lysate activates dendritic cells and elicits potent antitumor immunity Blood, June 1, 2003; 101(11): 4485 - 4491. [Abstract] [Full Text] [PDF]
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