Calreticulin in the immune system: Ins and outs

Trends in Immunology

Volumn 34, Issue 1, 2013, Pages 13-21

  Raghavan, Malini ^a   Wijeyesakere, Sanjeeva J ^a   Peters, Larry Robert ^a   Del Cid, Natasha ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Antitumor immunity; Calreticulin; MHC class I; Phagocytosis; Protein folding; Tapasin

Indexed keywords

CALRETICULIN; GLYCOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR VACCINE;

ANTIGEN PRESENTATION; CELL SURFACE; CYTOTOXIC T LYMPHOCYTE; ENDOPLASMIC RETICULUM; HUMAN; IMMUNE SYSTEM; IMMUNOGENICITY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PHAGOCYTOSIS; PROTEIN FOLDING; REVIEW; TUMOR CELL;

ANIMALS; CALRETICULIN; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNE SYSTEM; INTRACELLULAR SPACE; PHAGOCYTES; PROTEIN FOLDING;

EID: 84871717972     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.08.002     Document Type: Review

References (77)

1. Rutkevich L.A., Williams D.B. Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum. Curr. Opin. Cell Biol. 2011, 23:157-166.
2. Gao B., et al. Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 2002, 16:99-109.
3. Ireland B.S., et al. Lectin-deficient calreticulin retains full functionality as a chaperone for class I histocompatibility molecules. Mol. Biol. Cell 2008, 19:2413-2423.
4. Zhang Y., et al. ERp57 does not require interactions with calnexin and calreticulin to promote assembly of class I histocompatibility molecules, and it enhances peptide loading independently of its redox activity. J. Biol. Chem. 2009, 284:10160-10173.
5. Del Cid N., et al. Modes of calreticulin recruitment to the major histocompatibility complex class I assembly pathway. J. Biol. Chem. 2010, 285:4520-4535.
6. Jeffery E., et al. The polypeptide binding conformation of calreticulin facilitates its cell surface expression under conditions of ER stress. J. Biol. Chem. 2011, 286:2402-2415.
7. Wearsch P.A., et al. Essential glycan-dependent interactions optimize MHC class I peptide loading. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4950-4955.
8. Rizvi S.M., et al. Distinct function for glycans of tapasin and heavy chains in the assembly of MHC class I molecules. J. Immunol. 2011, 186:2309-2320.
9. Howe C., et al. Calreticulin-dependent recycling in the early secretory pathway mediates optimal peptide loading of MHC class I molecules. EMBO J. 2009, 28:3730-3744.
10. Gardai S.J., et al. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 2005, 123:321-334.
11. Obeid M., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 2007, 13:54-61.
12. Tesniere A., et al. Immunogenic death of colon cancer cells treated with oxaliplatin. Oncogene 2010, 29:482-491.
13. Peters L.R., Raghavan M. Endoplasmic reticulum calcium depletion impacts chaperone secretion, innate immunity, and phagocytic uptake of cells. J. Immunol. 2011, 187:919-931.
14. Panaretakis T., et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 2009, 28:578-590.
15. Chao M.P., et al. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci. Transl. Med. 2010, 2:63ra94.
16. Zitvogel L., et al. Decoding cell death signals in inflammation and immunity. Cell 2010, 140:798-804.
17. Kepp O., et al. Molecular determinants of immunogenic cell death elicited by anticancer chemotherapy. Cancer Metastasis Rev. 2011, 30:61-69.
18. Schrag J.D., et al. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol. Cell 2001, 8:633-644.
19. Ellgaard L., et al. NMR structure of the calreticulin P-domain. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:3133-3138.
20. Kozlov G., et al. Structural basis of carbohydrate recognition by calreticulin. J. Biol. Chem. 2010, 285:38612-38620.
21. Chouquet A., et al. X-ray structure of the human calreticulin globular domain reveals a peptide-binding area and suggests a multi-molecular mechanism. PLoS ONE 2011, 6:e17886.
22. Duus K., et al. Interaction of the chaperone calreticulin with proteins and peptides of different structural classes. Protein Pept. Lett. 2009, 16:1414-1423.
23. Pocanschi C.L., et al. Structural and functional relationships between the lectin and arm domains of calreticulin. J. Biol. Chem. 2011, 286:27266-27277.
24. Frickel E.M., et al. TROSY-NMR reveals interaction between ERp57 and the tip of the calreticulin P-domain. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:1954-1959.
25. Kozlov G., et al. Structural basis of cyclophilin B binding by the calnexin/calreticulin P-domain. J. Biol. Chem. 2010, 285:35551-35557.
26. Baksh S., Michalak M. Expression of calreticulin in Escherichia coli and identification of its Ca2+ binding domains. J. Biol. Chem. 1991, 266:21458-21465.
27. Nakamura K., et al. Functional specialization of calreticulin domains. J. Cell Biol. 2001, 154:961-972.
28. Wijeyesakere S.J., et al. Calreticulin is a thermostable protein with distinct structural responses to different divalent cation environments. J. Biol. Chem. 2011, 286:8771-8785.
29. Mesaeli N., et al. Calreticulin is essential for cardiac development. J. Cell Biol. 1999, 144:857-868.
30. Guo L., et al. Cardiac-specific expression of calcineurin reverses embryonic lethality in calreticulin-deficient mouse. J. Biol. Chem. 2002, 277:50776-50779.
31. Sonnichsen B., et al. Retention and retrieval: both mechanisms cooperate to maintain calreticulin in the endoplasmic reticulum. J. Cell Sci. 1994, 107:2705-2717.
32. Dancourt J., Barlowe C. Protein sorting receptors in the early secretory pathway. Annu. Rev. Biochem. 2010, 79:777-802.
33. Afshar N., et al. Retrotranslocation of the chaperone calreticulin from the endoplasmic reticulum lumen to the cytosol. Mol. Cell. Biol. 2005, 25:8844-8853.
34. Gold L.I., et al. Calreticulin: non-endoplasmic reticulum functions in physiology and disease. FASEB J. 2010, 24:665-683.
35. Raghavan M., et al. MHC class I assembly: out and about. Trends Immunol. 2008, 29:436-443.
36. Wearsch P.A., Cresswell P. The quality control of MHC class I peptide loading. Curr. Opin. Cell Biol. 2008, 20:624-631.
37. Rizvi S.M., Raghavan M. Mechanisms of function of tapasin, a critical major histocompatibility complex class I assembly factor. Traffic 2010, 11:332-347.
38. Simone L.C., et al. Influence of the tapasin C terminus on the assembly of MHC class I allotypes. Immunogenetics 2009, 61:43-54.
39. Purcell A.W., Elliott T. Molecular machinations of the MHC-I peptide loading complex. Curr. Opin. Immunol. 2008, 20:75-81.
40. Sadegh-Nasseri S., et al. The convergent roles of tapasin and HLA-DM in antigen presentation. Trends Immunol. 2008, 29:141-147.
41. Li X.C., Raghavan M. Structure and function of major histocompatibility complex class I antigens. Curr. Opin. Organ Transplant. 2010, 15:499-504.
42. Dong G., et al. Insights into MHC class I peptide loading from the structure of the tapasin-ERp57 thiol oxidoreductase heterodimer. Immunity 2009, 30:21-32.
43. Saito Y., et al. Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J. 1999, 18:6718-6729.
44. Mancino L., et al. Calreticulin recognizes misfolded HLA-A2 heavy chains. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:5931-5936.
45. Rizvi S.M., et al. A polypeptide-binding conformation of calreticulin is induced by heat-shock, calcium depletion, or by mutation of the C-terminal acidic domain. Mol. Cell 2004, 15:913-923.
46. Jorgensen C.S., et al. Dimerization and oligomerization of the chaperone calreticulin. Eur. J. Biochem. 2003, 270:4140-4148.
47. Todd D.J., et al. The endoplasmic reticulum stress response in immunity and autoimmunity. Nat. Rev. Immunol. 2008, 8:663-674.
48. Paidassi H., et al. Investigations on the C1q-calreticulin-phosphatidylserine interactions yield new insights into apoptotic cell recognition. J. Mol. Biol. 2011, 408:277-290.
49. Tarr J.M., et al. A mechanism of release of calreticulin from cells during apoptosis. J. Mol. Biol. 2010, 401:799-812.
50. Obeid M. ERP57 membrane translocation dictates the immunogenicity of tumor cell death by controlling the membrane translocation of calreticulin. J. Immunol. 2008, 181:2533-2543.
51. Panaretakis T., et al. The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ. 2008, 15:1499-1509.
52. Tufi R., et al. Reduction of endoplasmic reticulum Ca2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ. 2008, 15:274-282.
53. Booth C., Koch G.L. Perturbation of cellular calcium induces secretion of luminal ER proteins. Cell 1989, 59:729-737.
54. Thastrup O., et al. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2466-2470.
55. Fadok V.A., et al. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992, 148:2207-2216.
56. Garg A.D., et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J. 2012, 31:1062-1079.
57. Dupuis M., et al. The calcium-binding protein calreticulin is a major constituent of lytic granules in cytolytic T lymphocytes. J. Exp. Med. 1993, 177:1-7.
58. Oldenborg P.A., et al. Role of CD47 as a marker of self on red blood cells. Science (New York, N. Y.) 2000, 288:2051-2054.
59. Jaiswal S., et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009, 138:271-285.
60. Eric-Nikolic A., et al. Overexpression of calreticulin in malignant and benign breast tumors: relationship with humoral immunity. Oncology 2012, 82:48-55.
61. Chao M.P., et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell 2010, 142:699-713.
62. Majeti R., et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 2009, 138:286-299.
63. Edris B., et al. Antibody therapy targeting the CD47 protein is effective in a model of aggressive metastatic leiomyosarcoma. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6656-6661.
64. Willingham S.B., et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:6662-6667.
65. Subramanian S., et al. Membrane mobility and clustering of Integrin Associated Protein (IAP, CD47)-major differences between mouse and man and implications for signaling. Blood Cells Mol. Dis. 2006, 36:364-372.
66. Nagata S., et al. Autoimmunity and the clearance of dead cells. Cell 2010, 140:619-630.
67. Ravichandran K.S. Find-me and eat-me signals in apoptotic cell clearance: progress and conundrums. J. Exp. Med. 2010, 207:1807-1817.
68. Kuraishi T., et al. Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila. Exp. Cell Res. 2007, 313:500-510.
69. Somogyi E., et al. Calreticulin-an endoplasmic reticulum protein with calcium-binding activity is also found in the extracellular matrix. Matrix Biol. 2003, 22:179-191.
70. Tarr J.M., et al. Extracellular calreticulin is present in the joints of patients with rheumatoid arthritis and inhibits FasL (CD95L)-mediated apoptosis of T cells. Arthritis Rheum. 2010, 62:2919-2929.
71. Green D.R., et al. Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 2009, 9:353-363.
72. Obeid M., et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ. 2007, 14:1848-1850.
73. Pawaria S., Binder R.J. CD91-dependent programming of T-helper cell responses following heat shock protein immunization. Nat. Commun. 2011, 2:521.
74. Freeman G.J., et al. TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol. Rev. 2010, 235:172-189.
75. Tseng C.W., et al. Pretreatment with cisplatin enhances E7-specific CD8+ T-cell-mediated antitumor immunity induced by DNA vaccination. Clin. Cancer Res. 2008, 14:3185-3192.
76. Roy A., et al. I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 2010, 5:725-738.
77. Bjorkman P.J., et al. Structure of the human class I histocompatibility antigen, HLA-A2. Nature 1987, 329:506-512.