Endoplasmic reticulum calcium depletion impacts chaperone secretion, innate immunity, and phagocytic uptake of cells

Journal of Immunology

Volumn 187, Issue 2, 2011, Pages 919-931

  Peters, Larry Robert ^a   Raghavan, Malini ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CALRETICULIN; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; BONE MARROW; CALCIUM DEPLETION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FIBROBLAST; INNATE IMMUNITY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN SECRETION;

AMINO ACID SEQUENCE; ANIMALS; BONE MARROW CELLS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CALRETICULIN; CELL LINE, TUMOR; CELLS, CULTURED; DENDRITIC CELLS; FIBROBLASTS; HUMANS; IMMUNITY, INNATE; INFLAMMATION MEDIATORS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PHAGOCYTOSIS; SARCOPLASMIC RETICULUM; THAPSIGARGIN;

EID: 79960551691     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100690     Document Type: Article

References (60)

1. Görlach, A., P. Klappa, and T. Kietzmann. 2006. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid. Redox Signal. 8: 1391-1418.
2. Michalak, M., J. Groenendyk, E. Szabo, L. I. Gold, and M. Opas. 2009. Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 417: 651-666.
3. Gold, L. I., P. Eggleton, M. T. Sweetwyne, L. B. Van Duyn, M. R. Greives, S. M. Naylor, M. Michalak, and J. E. Murphy-Ullrich. 2010. Calreticulin: nonendoplasmic reticulum functions in physiology and disease. FASEB J. 24: 665-683.
4. Green, D. R., T. Ferguson, L. Zitvogel, and G. Kroemer. 2009. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9: 353-363.
5. Gardai, S. J., K. A. McPhillips, S. C. Frasch, W. J. Janssen, A. Starefeldt, J. E. Murphy-Ullrich, D. L. Bratton, P. A. Oldenborg, M. Michalak, and P. M. Henson. 2005. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123: 321-334.
6. Obeid, M., T. Panaretakis, N. Joza, R. Tufi, A. Tesniere, P. van Endert, L. Zitvogel, and G. Kroemer. 2007. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ. 14: 1848-1850. (Pubitemid 47423653)
7. Obeid, M., A. Tesniere, F. Ghiringhelli, G. M. Fimia, L. Apetoh, J. L. Perfettini, M. Castedo, G. Mignot, T. Panaretakis, N. Casares, et al. 2007. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13: 54-61.
8. Panaretakis, T., O. Kepp, U. Brockmeier, A. Tesniere, A. C. Bjorklund, D. C. Chapman, M. Durchschlag, N. Joza, G. Pierron, P. van Endert, et al. 2009. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 28: 578-590.
9. Kuraishi, T., J. Manaka, M. Kono, H. Ishii, N. Yamamoto, K. Koizumi, A. Shiratsuchi, B. L. Lee, H. Higashida, and Y. Nakanishi. 2007. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Exp. Cell Res. 313: 500-510.
10. Hong, C., X. Qiu, Y. Li, Q. Huang, Z. Zhong, Y. Zhang, X. Liu, L. Sun, P. Lv, and X. M. Gao. 2010. Functional analysis of recombinant calreticulin fragment 39-272: implications for immunobiological activities of calreticulin in health and disease. J. Immunol. 185: 4561-4569.
11. Henderson, B., S. K. Calderwood, A. R. Coates, I. Cohen, W. van Eden, T. Lehner, and A. G. Pockley. 2010. Caught with their PAMPs down? The extracellular signalling actions of molecular chaperones are not due to microbial contaminants. Cell Stress Chaperones 15: 123-141.
12. Spisek, R., A. Charalambous, A. Mazumder, D. H. Vesole, S. Jagannath, and M. V. Dhodapkar. 2007. Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood 109: 4839-4845.
13. Tsan, M. F., and B. Gao. 2009. Heat shock proteins and immune system. J. Leukoc. Biol. 85: 905-910.
14. Liu, B., J. Dai, H. Zheng, D. Stoilova, S. Sun, and Z. Li. 2003. Cell surface expression of an endoplasmic reticulum resident heat shock protein gp96 triggers MyD88-dependent systemic autoimmune diseases. Proc. Natl. Acad. Sci. USA 100: 15824-15829.
15. Drummond, I. A., A. S. Lee, E. Resendez, Jr., and R. A. Steinhardt. 1987. Depletion of intracellular calcium stores by calcium ionophore A23187 induces the genes for glucose-regulated proteins in hamster fibroblasts. J. Biol. Chem. 262: 12801-12805.
16. Booth, C., and G. L. Koch. 1989. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 59: 729-737.
17. Thastrup, O., P. J. Cullen, B. K. Drøbak, M. R. Hanley, and A. P. Dawson. 1990. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl. Acad. Sci. USA 87: 2466-2470.
18. Tufi, R., T. Panaretakis, K. Bianchi, A. Criollo, B. Fazi, F. Di Sano, A. Tesniere, O. Kepp, P. Paterlini-Brechot, L. Zitvogel, et al. 2008. Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ. 15: 274-282.
19. Delpino, A., and M. Castelli. 2002. The 78 kDa glucose-regulated protein (GRP78/BIP) is expressed on the cell membrane, is released into cell culture medium and is also present in human peripheral circulation. Biosci. Rep. 22: 407-420.
20. Zhang, Y., R. Liu, M. Ni, P. Gill, and A. S. Lee. 2010. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J. Biol. Chem. 285: 15065-15075.
21. Jeffery, E., L. R. Peters, and M. Raghavan. 2011. The polypeptide binding conformation of calreticulin facilitates its cell-surface expression under conditions of endoplasmic reticulum stress. J. Biol. Chem. 286: 2402-2415.
22. Stevens, F. J., and Y. Argon. 1999. Protein folding in the ER. Semin. Cell Dev. Biol. 10: 443-454.
23. Sambrook, J. F. 1990. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61: 197-199.
24. Zhang, K., and R. J. Kaufman. 2008. From endoplasmic-reticulum stress to the inflammatory response. Nature 454: 455-462.
25. Rutkowski, D. T., and R. J. Kaufman. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14: 20-28.
26. Panaretakis, T., N. Joza, N. Modjtahedi, A. Tesniere, I. Vitale, M. Durchschlag, G. M. Fimia, O. Kepp, M. Piacentini, K. U. Froehlich, et al. 2008. The cotranslocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ. 15: 1499-1509.
27. Obeid, M. 2008. ERP57 membrane translocation dictates the immunogenicity of tumor cell death by controlling the membrane translocation of calreticulin. J. Immunol. 181: 2533-2543.
28. Bost, K. L., and M. J. Mason. 1995. Thapsigargin and cyclopiazonic acid initiate rapid and dramatic increases of IL-6 mRNA expression and IL-6 secretion in murine peritoneal macrophages. J. Immunol. 155: 285-296.
29. Del Cid, N., E. Jeffery, S. M. Rizvi, E. Stamper, L. R. Peters, W. C. Brown, C. Provoda, and M. Raghavan. 2010. Modes of calreticulin recruitment to the major histocompatibility complex class I assembly pathway. J. Biol. Chem. 285: 4520-4535.
30. Torchinsky, M. B., J. Garaude, A. P. Martin, and J. M. Blander. 2009. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 458: 78-82.
31. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148: 2207-2216.
32. Chao, M. P., S. Jaiswal, R. Weissman-Tsukamoto, A. A. Alizadeh, A. J. Gentles, J. Volkmer, K. Weiskopf, S. B. Willingham, T. Raveh, C. Y. Park, R. Majeti, and I. L. Weissman. 2010. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl. Med. 2: 63ra94.
33. Okada, T., K. Haze, S. Nadanaka, H. Yoshida, N. G. Seidah, Y. Hirano, R. Sato, M. Negishi, and K. Mori. 2003. A serine protease inhibitor prevents endoplasmic reticulum stress-induced cleavage but not transport of the membrane-bound transcription factor ATF6. J. Biol. Chem. 278: 31024-31032.
34. Winnay, J. N., J. Boucher, M. A. Mori, K. Ueki, and C. R. Kahn. 2010. A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat. Med. 16: 438-445.
35. Llewellyn, D. H., J. M. Kendall, F. N. Sheikh, and A. K. Campbell. 1996. Induction of calreticulin expression in HeLa cells by depletion of the endoplasmic reticulum Ca2+ store and inhibition of N-linked glycosylation. Biochem. J. 318: 555-560.
36. Waser, M., N. Mesaeli, C. Spencer, and M. Michalak. 1997. Regulation of calreticulin gene expression by calcium. J. Cell Biol. 138: 547-557. (Pubitemid 27349837)
37. Frickel, E. M., R. Riek, I. Jelesarov, A. Helenius, K. Wuthrich, and L. Ellgaard. 2002. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. USA 99: 1954-1959.
38. Martin, V., J. Groenendyk, S. S. Steiner, L. Guo, M. Dabrowska, J. M. Parker, W. Mü ller-Esterl, M. Opas, and M. Michalak. 2006. Identification by mutational analysis of amino acid residues essential in the chaperone function of calreticulin. J. Biol. Chem. 281: 2338-2346.
39. Rizvi, S. M., L. Mancino, V. Thammavongsa, R. L. Cantley, and M. Raghavan. 2004. A polypeptide binding conformation of calreticulin is induced by heat shock, calcium depletion, or by deletion of the C-terminal acidic region. Mol. Cell 15: 913-923. (Pubitemid 39277988)
40. Tarr, J. M., P. J. Young, R. Morse, D. J. Shaw, R. Haigh, P. G. Petrov, S. J. Johnson, P. G. Winyard, and P. Eggleton. 2010. A mechanism of release of calreticulin from cells during apoptosis. J. Mol. Biol. 401: 799-812.
41. Martinon, F., X. Chen, A. H. Lee, and L. H. Glimcher. 2010. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat. Immunol. 11: 411-418.
42. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
43. Goodall, J. C., C. Wu, Y. Zhang, L. McNeill, L. Ellis, V. Saudek, and J. S. Gaston. 2010. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. USA 107: 17698-17703.
44. Pahl, H. L., and P. A. Baeuerle. 1995. A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NFkappa B. EMBO J. 14: 2580-2588.
45. Hsieh, Y. H., I. J. Su, H. Y. Lei, M. D. Lai, W. W. Chang, and W. Huang. 2007. Differential endoplasmic reticulum stress signaling pathways mediated by iNOS. Biochem. Biophys. Res. Commun. 359: 643-648.
46. Smith, J. A., M. J. Turner, M. L. DeLay, E. I. Klenk, D. P. Sowders, and R. A. Colbert. 2008. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur. J. Immunol. 38: 1194-1203.
47. Martins, I., O. Kepp, F. Schlemmer, S. Adjemian, M. Tailler, S. Shen, M. Michaud, L. Menger, A. Gdoura, N. Tajeddine, et al. 2011. Restoration of the immunogenicity of cisplatin-induced cancer cell death by endoplasmic reticulum stress. Oncogene 30: 1147-1158.
48. Coe, H., and M. Michalak. 2009. Calcium binding chaperones of the endoplasmic reticulum. Gen. Physiol. Biophys. 28 Spec No Focus: F96-F103.
49. Sönnichsen, B., J. Füllekrug, P. Nguyen Van, W. Diekmann, D. G. Robinson, and G. Mieskes. 1994. Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J. Cell Sci. 107: 2705-2717. (Pubitemid 24340892)
50. Kim, P. S., S. A. Hossain, Y. N. Park, I. Lee, S. E. Yoo, and P. Arvan. 1998. A single amino acid change in the acetylcholinesterase-like domain of thyroglobulin causes congenital goiter with hypothyroidism in the cog/cog mouse: a model of human endoplasmic reticulum storage diseases. Proc. Natl. Acad. Sci. USA 95: 9909-9913.
51. Pahl, H. L., and P. A. Baeuerle. 1997. The ER-overload response: activation of NF-kappa B. Trends Biochem. Sci. 22: 63-67.
52. Ivashkiv, L. B. 2008. A signal-switch hypothesis for cross-regulation of cytokine and TLR signalling pathways. Nat. Rev. Immunol. 8: 816-822.
53. Turnbull, I. R., and M. Colonna. 2007. Activating and inhibitory functions of DAP12. Nat. Rev. Immunol. 7: 155-161.
54. Davies, M. J., E. Miranda, B. D. Roussel, R. J. Kaufman, S. J. Marciniak, and D. A. Lomas. 2009. Neuroserpin polymers activate NF-kappaB by a calcium signaling pathway that is independent of the unfolded protein response. J. Biol. Chem. 284: 18202-18209.
55. Bak, S. P., E. Amiel, J. J. Walters, and B. Berwin. 2008. Calreticulin requires an ancillary adjuvant for the induction of efficient cytotoxic T cell responses. Mol. Immunol. 45: 1414-1423.
56. Krysko, D. V., and P. Vandenabeele. 2008. From regulation of dying cell engulfment to development of anti-cancer therapy. Cell Death Differ. 15: 29-38. (Pubitemid 350286170)
57. Park, Y. J., G. Liu, E. F. Lorne, X. Zhao, J. Wang, Y. Tsuruta, J. Zmijewski, and E. Abraham. 2008. PAI-1 inhibits neutrophil efferocytosis. Proc. Natl. Acad. Sci. USA 105: 11784-11789.
58. Apetoh, L., F. Ghiringhelli, A. Tesniere, M. Obeid, C. Ortiz, A. Criollo, G. Mignot, M. C. Maiuri, E. Ullrich, P. Saulnier, et al. 2007. Toll-like receptor 4- dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13: 1050-1059.
59. Ghiringhelli, F., L. Apetoh, A. Tesniere, L. Aymeric, Y. Ma, C. Ortiz, K. Vermaelen, T. Panaretakis, G. Mignot, E. Ullrich, et al. 2009. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat. Med. 15: 1170-1178.
60. Janssen, S., D. M. Rosen, R. M. Ricklis, C. A. Dionne, H. Lilja, S. B. Christensen, J. T. Isaacs, and S. R. Denmeade. 2006. Pharmacokinetics, biodistribution, and antitumor efficacy of a human glandular kallikrein 2 (hK2)-activated thapsigargin prodrug. Prostate 66: 358-368.