Targeting to static endosome is required for efficient cross-presentation of endoplasmic reticulum-resident oxygen-regulated protein 150-peptide complexes

Journal of Immunology

Volumn 183, Issue 9, 2009, Pages 5861-5869

  Kutomi, Goro ^a   Tamura, Yasuaki ^a   Okuya, Koichi ^a   Yamamoto, Takashi ^a   Hirohashi, Yoshihiko ^a   Kamiguchi, Kenjiro ^a   Oura, Jun ^a   Saito, Keita ^a   Torigoe, Toshihiko ^a   Ogawa, Satoshi ^b   Hirata, Koichi ^a   Sato, Noriyuki ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KANAZAWA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; EARLY ENDOSOME ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; OVALBUMIN; OXYGEN REGULATED PROTEIN 150; RAB PROTEIN; TUMOR ANTIGEN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CONFOCAL LASER MICROSCOPY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG BINDING; DRUG EFFECT; DRUG TARGETING; ENDOPLASMIC RETICULUM; ENDOSOME; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CROSS-PRIMING; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; ENDOPLASMIC RETICULUM; ENDOSOMES; FEMALE; HSP72 HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; OXYGEN CONSUMPTION; PEPTIDE FRAGMENTS; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 77249143644     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803768     Document Type: Article

References (42)

1. Udono, H., and P. K. Srivastava. 1994. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J. Immunol. 152: 5398-5403. (Pubitemid 24152988)
2. Tamura, Y., P. Peng, K. Liu, M. Daou, and P. K. Srivastava. 1997. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science 278: 117-120.
3. Sato, K., Y. Torimoto, Y. Tamura, M. Shindo, H. Shinzaki, K. Hirai, and Y. Kohgo. 2001. Immunotherapy using heat-shock protein preparations of leukemia cells after syngeneic bone marrow transplantation in mice. Blood 98: 1852-1857.
4. Noessner, E., R. Gastpar, V. Milani, A. Brandl, P. J. Hutzler, M. C. Kuppner, M. Roos, E. Kremmer, A. Asea, S. K. Calderwood, and R. D. Issels. 2002. Tumor-derived heat shock protein 70 peptide complexes are cross-presented by human dendritic cells. J. Immunol. 169: 5424-5432.
5. Milani, V., E. Noessner, S. Ghose, M. Kuppner, B. Ahrens, A. Scharner, R. Gastpar, and R. D. Issels. 2002. Heat shock protein 70: role in antigen presentation and immune stimulation. Int. J. Hyperthermia 18: 563-575.
6. Arnold-Schild, D., D. Hanau, D. Spehner, C. Schmid, H. G. Rammensee, H. de la Salle, and H. Schild. 1999. Cutting edge: receptor-mediated endocytosis of heat shock proteins by professional antigen-presenting cells. J. Immunol. 162: 3757-3760.
7. Moroi, Y., M. Mayhew, J. Trcka, M. H. Hoe, Y. Takechi, F. U. Hartl, J. E. Rothman, and A. N. Houghton. 2000. Induction of cellular immunity by immunization with novel hybrid peptides complexed to heat shock protein 70. Proc. Natl. Acad. Sci. USA 97: 3485-3490.
8. Singh-Jasuja, H., R. E. Toes, P. Spee, C. Munz, N. Hilf, S. P. Schoenberger, P. Ricciardi-Castagnoli, J. Neefjes, H. G. Rammensee, D. Arnold-Schild, and H. Schild. 2000. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. J. Exp. Med. 191: 1965-1974.
9. Castelli, C., A. M. Ciupitu, F. Rini, L. Rivoltini, A. Mazzocchi, R. Kiessling, and G. Parmiani. 2001. Human heat shock protein 70 peptide complexes specifically activate antimelanoma T cells. Cancer Res. 61: 222-227.
10. Srivastava, P. 2002. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20: 395-425.
11. Ueda, G., Y. Tamura, I. Hirai, K. Kamiguchi, S. Ichimiya, T. Torigoe, H. Hiratsuka, H. Sunakawa, and N. Sato. 2004. Tumor-derived heat shock protein 70-pulsed dendritic cells elicit tumor-specific cytotoxic T lymphocytes (CTLs) and tumor immunity. Cancer Sci. 95: 248-253.
12. Asea, A., S. K. Kraeft, E. A. Kurt-Jones, M. A. Stevenson, L. B. Chen, R. W. Finberg, G. C. Koo, and S. K. Calderwood. 2000. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6: 435-442.
13. Asea, A., M. Rehli, E. Kabingu, J. A. Boch, O. Bare, P. E. Auron, M. A. Stevenson, and S. K. Calderwood. 2002. Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277: 15028-15034.
14. Binder, R., D. Han, and P. Srivastava. 2000. CD91: a receptor for heat shock protein gp96. Nat. Immunol. 1: 151-155.
15. Basu, S., R. J. Binder, T. Ramalingam, and P. K. Srivastava. 2001. CD91 is a common receptor for heat shock proteins gp96, hsp90, hsp70, and calreticulin. Immunity 14: 303-313.
16. Binder, R. J., and P. K. Srivastava. 2004. Essential role of CD91 in re-presentation of gp96-chaperoned peptides. Proc. Natl. Acad. Sci. USA 101: 6128-6133.
17. Delneste, Y., G. Magistrelli, J. Gauchat, J. Haeuw, J. Aubry, K. Nakamura, N. Kawakami-Honda, L. Goetsch, T. Sawamura, J. Bonnefoy, and P. Jeannin. 2002. Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity. 17: 353-362.
18. Becker, T., F. U. Hartl, and F. Wieland. 2002. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell Biol. 158: 1277-1285.
19. Berwin, B., J. P. Hart, S. Rice, C. Gass, S. V. Pizzo, S. R. Post, and C. V. Nicchitta. 2003. Scavenger receptor-A mediates gp96/GRP94 and calreticulin internalization by antigen-presenting cells. EMBO J. 22: 6127-6136.
20. Facciponte, J. G., X. Y. Wang, and J. R. Subjeck. 2007. Hsp110 and Grp170, members of the Hsp70 superfamily, bind to scavenger receptor-A and scavenger receptor expressed by endothelial cells-I. Eur. J. Immunol. 37: 2268-2279.
21. Berwin, B., Y. Delneste, R. V. Lovingood, S. R. Post, and S. V. Pizzo. 2004. SREC-I, a type F scavenger receptor, is an endocytic receptor for calreticulin. J. Biol. Chem. 279: 51250-51257.
22. Kurotaki, T., Y. Tamura, G. Ueda, J. Oura, G. Kutomi, Y. Hirohashi, H. Sahara, T. Torigoe, H. Hiratsuka, H. Sunakawa, et al. 2007. Efficient cross-presentation by heat shock protein 90-peptide complex-loaded dendritic cells via an endosomal pathway. J. Immunol. 179: 1803-1813.
23. Kuwabara, K., M. Matsumoto, J. Ikeda, O. Hori, S. Ogawa, Y. Maeda, K. Kitagawa, N. Imuta, T. Kinoshita, D. M. Stern, et al. 1996. Purification and characterization of a novel stress protein, the 150-kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J. Biol. Chem. 271: 5025-5032.
24. Ikeda, J., S. Kaneda, K. Kuwabara, S. Ogawa, T. Kobayashi, M. Matsumoto, T. Yura, and H. Yanagi. 1997. Cloning and expression of cDNA encoding the human 150 kDa oxygen-regulated protein, ORP150. Biochem. Biophys. Res. Commun. 230: 94-99.
25. Wang, X. Y., L. Kazim, E. A. Repasky, and J. R. Subjeck. 2001. Characterization of heat shock protein 110 and glucose-regulated protein 170 as cancer vaccines and the effect of fever-range hyperthermia on vaccine activity. J. Immunol. 166: 490-497.
26. + T-cell responses and reduces pulmonary metastatic disease. Int. J. Cancer 105: 226-231.
27. Wang, X. Y., H. Arnouk, X. Chen, L. Kazim, E. A. Repasky, and J. R. Subjeck. 2006. Extracellular targeting of endoplasmic reticulum chaperone glucose-regulated protein 170 enhances tumor immunity to a poorly immunogenic melanoma. J. Immunol. 177: 1543-1551.
28. Park, J. E., J. Facciponte, X. Chen, I. MacDonald, E. A. Repasky, M. H. Manjili, X. Y. Wang, and J. R. Subjeck. 2006. Chaperoning function of stress protein grp170, a member of the hsp70 superfamily, is responsible for its immunoadjuvant activity. Cancer Res. 66: 1161-1168.
29. Lakadamyali, M., M. J. Rust, and X. Zhuang. 2006. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124: 997-1009.
30. Burgdorf, S., A. Kautz, V. Bohnert, P. A. Knolle, and C. Kurts. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616.
31. b transgenic mice. Int. J. Cancer 100: 565-570.
32. Hirohashi, Y., T. Torigoe, A. Maeda, Y. Nabeta, K. Kamiguchi, T. Sato, J. Yoda, H. Ikeda, K. Hirata, N. Yamanaka, and N. Sato. 2002. An HLA-A24-restricted cytotoxic T lymphocyte epitope of a tumor-associated protein, survivin. Clin. Cancer Res. 8: 1731-1739. (Pubitemid 34633728)
33. Tsuruma, T., Y. Iwayama, T. Ohmura, T. Katsuramaki, F. Hata, T. Furuhata, K. Yamaguchi, Y. Kimura, T. Torigoe, N. Toyota, et al. 2008. Clinical and immunological evaluation of anti-apoptosis protein, survivin-derived peptide vaccine in phase I clinical study for patients with advanced or recurrent breast cancer. J. Transl. Med. 6: 24.
34. Ramirez, S. R., H. Singh-Jasuja, T. Warger, S. Braedel-Ruoff, N. Hilf, K. Wiemann, H. G. Rammensee, and H. Schild. 2005. Glycoprotein 96-activated dendritic cells induce a CD8-biased T cell response. Cell Stress Chaperones 10: 221-229.
35. Bendz, H., S. C. Ruhland, M. J. Pandya, O. Hainzl, S. Riegelsberger, C. Brauchle, M. P. Mayer, J. Buchner, R. D. Issels, and E. Noessner. 2007. Human heat shock protein 70 enhances tumor antigen presentation through complex formation and intracellular antigen delivery without innate immune signaling. J. Biol. Chem. 282: 31688-31702.
36. + T cell effector function. J. Immunol. 172: 6087-6092.
37. SenGupta, D., P. J. Norris, T. J. Suscovich, M. Hassan-Zahraee, H. F. Moffett, A. Trocha, R. Draenert, P. J. Goulder, R. J. Binder, D. L. Levey, et al. 2004. Heat shock protein-mediated cross-presentation of exogenous HIV antigen on HLA class I and class II. J. Immunol. 173: 1987-1993.
38. Asea, A. 2005. Stress proteins and initiation of immune response: chaperokine activity of hsp72. Exerc. Immunol. Rev. 11: 34-45.
39. Suto, R., and P. K. Srivastava. 1995. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 269: 1585-1588.
40. Kleijmeer, M. J., J. M. Escola, F. G. UytdeHaag, E. Jakobson, J. M. Griffith, A. D. Osterhaus, W. Stoorvogel, C. J. Melief, C. Rabouille, and H. J. Geuze. 2001. Antigen loading of MHC class I molecules in the endocytic tract. Traffic 2: 124-137.
41. Dierks, T., J. Volkmer, G. Schlenstedt, C. Jung, U. Sandholzer, K. Zachmann, P. Schlotterhose, K. Neifer, B. Schmidt, and R. Zimmermann. 1996. A microsomal ATP-binding protein involved in efficient protein transport into the mammalian endoplasmic reticulum. EMBO J. 15: 6931-6942.
42. Spee, P., J. Subjeck, and J. Neefjes. 1999. Identification of novel peptide binding proteins in the endoplasmic reticulum: ERp72, calnexin, and grp170. Biochemistry 38: 10559-10566.