Functional analysis of recombinant calreticulin fragment 39-272: Implications for immunobiological activities of calreticulin in health and disease

Journal of Immunology

Volumn 185, Issue 8, 2010, Pages 4561-4569

  Hong, Chao ^a,c   Qiu, Xiang ^a   Li, Yue ^a   Huang, Qianrong ^a   Zhong, Zhaoyan ^a   Zhang, Yan ^a   Liu, Xiangyuan ^b   Sun, Lin ^b   Lv, Ping ^a   Gao, Xiao Ming ^a,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b PEKING UNIVERSITY THIRD HOSPITAL   (China)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; CALRETICULIN; CARRAGEENAN; CD14 ANTIGEN; CD40 ANTIGEN; HOMODIMER; HYALURONIC ACID; HYBRID PROTEIN; IMMUNOGLOBULIN; LECTIN; OLIGOMER; POLYSACCHARIDE; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 4;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; CELL ACTIVATION; CELL MATURATION; CYTOKINE PRODUCTION; ESCHERICHIA COLI; FEMALE; HUMAN; IMMUNOBIOLOGY; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; RHEUMATOID ARTHRITIS; SERUM; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; ADOLESCENT; AMINO ACID SEQUENCE; ANIMAL; AUTOIMMUNITY; BAGG ALBINO MOUSE; C57BL MOUSE; CELL SEPARATION; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS; NUDE MOUSE; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD14; ARTHRITIS, RHEUMATOID; AUTOIMMUNITY; B-LYMPHOCYTES; BLOTTING, WESTERN; CALRETICULIN; CELL SEPARATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; MACROPHAGE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, NUDE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; YOUNG ADULT;

EID: 78049508966     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1000536     Document Type: Article

References (48)

1. Krause, K. H., and M. Michalak. 1997. Calreticulin. Cell 88:439-443.
2. Michalak, M., E. F. Corbett, N. Mesaeli, K. Nakamura, and M. Opas. 1999. Calreticulin: one protein, one gene, many functions. Biochem. J. 344:281-292.
3. Spiro, R. G., Q. Zhu, V. Bhoyroo, and H. D. Söling. 1996. Definition of the lectin-like properties of the molecular chaperone, calreticulin, and demonstration of its copurification with endomannosidase from rat liver Golgi. J. Biol. Chem. 271:11588-11594.
4. Thomson, S. P., and D. B. Williams. 2005. Delineation of the lectin site of the molecular chaperone calreticulin. Cell Stress Chaperones 10:242-251.
5. Vassilakos, A., M. Michalak, M. A. Lehrman, and D. B. Williams. 1998. Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. Biochemistry 37:3480-3490.
6. Arosa, F. A., O. de Jesus, G. Porto, A. M. Carmo, and M. de Sousa. 1999. Calreticulin is expressed on the cell surface of activated human peripheral blood T lymphocytes in association with major histocompatibility complex class I molecules. J. Biol. Chem. 274:16917-16922.
7. White, T. K., Q. Zhu, and M. L. Tanzer. 1995. Cell surface calreticulin is a putative mannoside lectin which triggers mouse melanoma cell spreading. J. Biol. Chem. 270:15926-15929.
8. Goicoechea, S., A. W. Orr, M. A. Pallero, P. Eggleton, and J. E. Murphy-Ullrich. 2000. Thrombospondin mediates focal adhesion disassembly through interactions with cell surface calreticulin. J. Biol. Chem. 275:36358-36368.
9. Cho, J. H., K. J. Homma, S. Kanegasaki, and S. Natori. 2001. Activation of human monocyte cell line U937 via cell surface calreticulin. Cell Stress Chaperones 6:148-152.
10. 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.
11. Burns, K., C. D. Helgason, R. C. Bleackley, and M. Michalak. 1992. Calreticulin in T-lymphocytes: identification of calreticulin in T-lymphocytes and demonstration that activation of T cells correlates with increased levels of calreticulin mRNA and protein. J. Biol. Chem. 267:19039-19042.
12. Porcellini, S., E. Traggiai, U. Schenk, D. Ferrera, M. Matteoli, A. Lanzavecchia, M. Michalak, and F. Grassi. 2006. Regulation of peripheral T cell activation by calreticulin. J. Exp. Med. 203:461-471.
13. Clarke, C., and M. J. Smyth. 2007. Calreticulin exposure increases cancer immunogenicity. Nat. Biotechnol. 25:192-193.
14. Zeng, G., M. E. Aldridge, X. Tian, D. Seiler, X. Zhang, Y. Jin, J. Rao, W. Li, D. Chen, M. P. Langford, et al. 2006. Dendritic cell surface calreticulin is a receptor for NY-ESO-1: direct interactions between tumor-associated antigen and the innate immune system. J. Immunol. 177:3582-3589.
15. 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.
16. 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. (Pubitemid 46067386)
17. Arnett, F. C., S. M. Edworthy, D. A. Bloch, D. J. McShane, J. F. Fries, N. S. Cooper, L. A. Healey, S. R. Kaplan, M. H. Liang, H. S. Luthra, et al. 1988. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum. 31:315-324.
18. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25:1271-1277.
19. Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553-563.
20. Kinoshita, K., M. Harigai, S. Fagarasan, M. Muramatsu, and T. Honjo. 2001. A hallmark of active class switch recombination: transcripts directed by I promoters on looped-out circular DNAs. Proc. Natl. Acad. Sci. USA 98:12620-12623.
21. Silva-Santos, B., D. J. Pennington, and A. C. Hayday. 2005. Lymphotoxinmediated regulation of γδ cell differentiation by αβ T cell progenitors. Science 307:925-928.
22. Pullen, G. R., M. G. Fitzgerald, and C. S. Hosking. 1986. Antibody avidity determination by ELISA using thiocyanate elution. J. Immunol. Methods 86:83-87.
23. Qiu, Y., and M. Michalak. 2009. Transcriptional control of the calreticulin gene in health and disease. Int. J. Biochem. Cell Biol. 41:531-538.
24. Jørgensen, C. S., L. R. Ryder, A. Steinø, P. Højrup, J. Hansen, N. H. Beyer, N. H. Heegaard, and G. Houen. 2003. Dimerization and oligomerization of the chaperone calreticulin. Eur. J. Biochem. 270:4140-4148.
25. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085-2088.
26. Castigli, E., S. A. Wilson, S. Scott, F. Dedeoglu, S. Xu, K. P. Lam, R. J. Bram, H. Jabara, and R. S. Geha. 2005. TACI and BAFF-R mediate isotype switching in B cells. J. Exp. Med. 201:35-39.
27. Armitage, R. J., W. C. Fanslow, L. Strockbine, T. A. Sato, K. N. Clifford, B. M. Macduff, D. M. Anderson, S. D. Gimpel, T. Davis-Smith, C. R. Maliszewski, et al. 1992. Molecular and biological characterization of a murine ligand for CD40. Nature 357:80-82.
28. van den Berg, R. H., C. E. Siegert, M. C. Faber-Krol, T. W. Huizinga, L. A. van Es, and M. R. Daha. 1998. Anti-C1q receptor/calreticulin autoantibodies in patients with systemic lupus erythematosus (SLE). Clin. Exp. Immunol. 111:359-364.
29. Boehm, J., T. Orth, P. Van Nguyen, and H. D. Söling. 1994. 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. 24:248-257.
30. Ghiran, I., L. B. Klickstein, and A. Nicholson-Weller. 2003. Calreticulin is at the surface of circulating neutrophils and uses CD59 as an adaptor molecule. J. Biol. Chem. 278:21024-21031.
31. 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.
32. Orlando, R. A. 2004. The low-density lipoprotein receptor-related protein associates with calnexin, calreticulin, and protein disulfide isomerase in receptorassociated-protein-deficient fibroblasts. Exp. Cell Res. 294:244-253.
33. 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.
34. 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.
35. Wallin, R. P., A. Lundqvist, S. H. Moré, A. von Bonin, R. Kiessling, and H. G. Ljunggren. 2002. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23:130-135.
36. Pockley, A. G. 2003. Heat shock proteins as regulators of the immune response. Lancet 362:469-476.
37. Martin, C. A., D. L. Kurkowski, A. M. Valentino, and F. Santiago-Schwarz. 2009. Increased intracellular, cell surface, and secreted inducible heat shock protein 70 responses are triggered during the monocyte to dendritic cell (DC) transition by cytokines independently of heat stress and infection and may positively regulate DC growth. J. Immunol. 183:388-399.
38. Cid, C., I. Regidor, P. D. Poveda, and A. Alcazar. 2009. Expression of heat shock protein 90 at the cell surface in human neuroblastoma cells. Cell Stress Chaperones 14:321-327.
39. Melendez, K., E. S. Wallen, B. S. Edwards, C. D. Mobarak, D. G. Bear, and P. L. Moseley. 2006. Heat shock protein 70 and glycoprotein 96 are differentially expressed on the surface of malignant and nonmalignant breast cells. Cell Stress Chaperones 11:334-342.
40. Martin, C. A., S. E. Carsons, R. Kowalewski, D. Bernstein, M. Valentino, and F. Santiago-Schwarz. 2003. Aberrant extracellular and dendritic cell (DC) surface expression of heat shock protein (hsp) 70 in the rheumatoid joint: possible mechanisms of hsp/DC-mediated cross-priming. J. Immunol. 171:5736-5742.
41. Gross, C., W. Koelch, A. DeMaio, N. Arispe, and G. Multhoff. 2003. Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J. Biol. Chem. 278:41173-41181.
42. Dai, J., B. Liu, M. M. Caudill, H. Zheng, Y. Qiao, E. R. Podack, and Z. Li. 2003. Cell surface expression of heat shock protein gp96 enhances cross-presentation of cellular antigens and the generation of tumor-specific T cell memory. Cancer Immun. 3:1-7.
43. Cohen-Sfady, M., G. Nussbaum, M. Pevsner-Fischer, F. Mor, P. Carmi, A. Zanin-Zhorov, O. Lider, and I. R. Cohen. 2005. Heat shock protein 60 activates B cells via the TLR4-MyD88 pathway. J. Immunol. 175:3594-3602.
44. Vabulas, R. M., P. Ahmad-Nejad, C. da Costa, T. Miethke, C. J. Kirschning, H. Häcker, and H. Wagner. 2001. Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276:31332-31339.
45. 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.
46. Kol, A., A. H. Lichtman, R. W. Finberg, P. Libby, and E. A. Kurt-Jones. 2000. Cutting edge: heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164:13-17.
47. 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.
48. Basu, S., R. J. Binder, R. Suto, K. M. Anderson, and P. K. Srivastava. 2000. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-κB pathway. Int. Immunol. 12:1539-1546.