Arginylated calreticulin at plasma membrane increases susceptibility of cells to apoptosis

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22043-22054

  Sambrooks, Cecilia López ^a   Carpio, Marcos A ^a   Hallak, Marta E ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC RESPONSE; ARGINYLATION; CALRETICULIN; CELL FATES; CELL FUNCTIONS; CELL SURFACES; ENDOPLASMIC RETICULUM; INTRACELLULAR LOCALIZATION; POST-TRANSLATIONAL MODIFICATIONS; WILD-TYPE CELLS;

CELL MEMBRANES; PROTEINS;

CELL DEATH;

ARGININE; ARGINYLTRANSFERASE; ARSENIC TRIOXIDE; CALRETICULIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL COUNT; CELL FUNCTION; CELL GRANULE; CELL MEMBRANE; CELL SURFACE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; FLOW CYTOMETRY; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ARGINYLATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; STRESS GRANULE; WILD TYPE;

AMINOACYLTRANSFERASES; ANIMALS; APOPTOSIS; ARGININE; BIOTINYLATION; CALCIUM; CALRETICULIN; CELL MEMBRANE; ENDOPLASMIC RETICULUM; FIBROBLASTS; FLOW CYTOMETRY; MICE; MICE, TRANSGENIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; STREPTAVIDIN;

EID: 84862663642     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338335     Document Type: Article

References (55)

1. Decca, M. B., Carpio, M. A., Bosc, C., Galiano, M. R., Job, D., Andrieux, A., and Hallak, M. E. (2007) Post-translational arginylation of calreticulin. A new isospecies of calreticulin component of stress granules. J. Biol. Chem. 282, 8237-8245
2. Carpio, M. A., López Sambrooks, C., Durand, E. S., and Hallak, M. E. (2010) The arginylation-dependent association of calreticulin with stress granules is regulated by calcium. Biochem. J. 429, 63-72
3. Coppolino, M. G., Woodside, M. J., Demaurex, N., Grinstein, S., St-Arnaud, R., and Dedhar, S. (1997) Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature 386, 843-847
4. Timchenko, L. T., Iakova, P., Welm, A. L., Cai, Z. J., and Timchenko, N. A. (2002) Calreticulin interacts with C/EBPα and C/EBPβ mRNAs and represses translation of C/EBP proteins. Mol. Cell Biol. 22, 7242-7257
5. Singh, N. K., Atreya, C. D., and Nakhasi, H. L. (1994) Identification of calreticulin as a rubella virus RNA binding protein. Proc. Natl. Acad. Sci. U.S.A. 91, 12770-12774
6. Iakova, P., Wang, G. L., Timchenko, L., Michalak, M., Pereira-Smith, O. M., Smith, J. R., and Timchenko, N. A. (2004) Competition of CUGBP1 and calreticulin for the regulation of p21 translation determines cell fate. EMBO J. 23, 406-417
7. Holaska, J. M., Black, B. E., Love, D. C., Hanover, J. A., Leszyk, J., and Paschal, B. M. (2001) Calreticulin is a receptor for nuclear export. J. Cell Biol. 152, 127-140
8. Olkku, A., and Mahonen, A. (2009) Calreticulin mediated glucocorticoid receptor export is involved in β-catenin translocation and Wnt signalling inhibition in human osteoblastic cells. Bone 44, 555-565
9. Gold, L. I., Rahman, M., Blechman, K. M., Greives, M. R., Churgin, S., Michaels, J., Callaghan, M. J., Cardwell, N. L., Pollins, A. C., Michalak, M., Siebert, J. W., Levine, J. P., Gurtner, G. C., Nanney, L. B., Galiano, R. D., and Cadacio, C. L. (2006) Overview of the role for calreticulin in the enhancement of wound healing through multiple biological effects. J. Investig. Dermatol. Symp. Proc. 11, 57-65
10. Nanney, L. B., Woodrell, C. D., Greives, M. R., Cardwell, N. L., Pollins, A. C., Bancroft, T. A., Chesser, A., Michalak, M., Rahman, M., Siebert, J. W., and Gold, L. I. (2008) Calreticulin enhances porcine wound repair by diverse biological effects. Am. J. Pathol. 173, 610-630
11. Gao, B., Adhikari, R., Howarth, M., Nakamura, K., Gold, M. C., Hill, A. B., Knee, R., Michalak, M., and Elliott, T. (2002) Assembly and antigen-presenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16, 99-109
12. Donnelly, S., Roake, W., Brown, S., Young, P., Naik, H., Wordsworth, P., Isenberg, D. A., Reid, K. B., and Eggleton, P. (2006) Impaired recognition of apoptotic neutrophils by the C1q/calreticulin and CD91 pathway in systemic lupus erythematosus. Arthritis Rheum. 54, 1543-1556
13. Goicoechea, S., Pallero, M. A., Eggleton, P., Michalak, M., and Murphy- Ullrich, J. E. (2002) The anti-adhesive activity of thrombospondin is mediated by the N-terminal domain of cell surface calreticulin. J. Biol. Chem. 277, 37219-37228
14. Orr, A. W., Pedraza, C. E., Pallero, M. A., Elzie, C. A., Goicoechea, S., Strickland, D. K., and Murphy-Ullrich, J. E. (2003) Low density lipoprotein receptor-related protein is a calreticulin coreceptor that signals focal adhesion disassembly. J. Cell Biol. 161, 1179-1189
15. Orr, A. W., Elzie, C. A., Kucik, D. F., and Murphy-Ullrich, J. E. (2003) Thrombospondin signaling through the calreticulin/LDL receptor-related protein co-complex stimulates random and directed cell migration. J. Cell Sci. 116, 2917-2927
16. Orr, A. W., Pallero, M. A., and Murphy-Ullrich, J. E. (2002) Thrombospondin stimulates focal adhesion disassembly through Gi- and phosphoinositide 3-kinase-dependent ERK activation. J. Biol. Chem. 277, 20453-20460
17. Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P. A., Michalak, M., and Henson, P. M. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334
18. Catanzariti, A. M., Soboleva, T. A., Jans, D. A., Board, P. G., and Baker, R. T. (2004) An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci. 13, 1331-1339
19. Gray, A. J., Park, P. W., Broekelmann, T. J., Laurent, G. J., Reeves, J. T., Stenmark, K. R., and Mecham, R. P. (1995) The mitogenic effects of the B β chain of fibrinogen are mediated through cell surface calreticulin. J. Biol. Chem. 270, 26602-26606
20. Arosa, F. A., de Jesus, O., Porto, G., Carmo, A. M., and de Sousa, M. (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
21. Eggleton, P., Lieu, T. S., Zappi, E. G., Sastry, K., Coburn, J., Zaner, K. S., Sontheimer, R. D., Capra, J. D., Ghebrehiwet, B., and Tauber, A. I. (1994) Calreticulin is released from activated neutrophils and binds to C1q and mannan-binding protein. Clin. Immunol. Immunopathol. 72, 405-409
22. Xiao, G., Chung, T. F., Fine, R. E., and Johnson, R. J. (1999) Calreticulin is transported to the surface of NG108-15 cells where it forms surface patches and is partially degraded in an acidic compartment. J. Neurosci. Res. 58, 652-662
23. Zhu, Q., Zelinka, P., White, T., and Tanzer, M. L. (1997) Calreticulinintegrin bidirectional signaling complex. Biochem. Biophys. Res. Commun. 232, 354-358
24. Lim, S., Chang, W., Lee, B. K., Song, H., Hong, J. H., Lee, S., Song, B. W., Kim, H. J., Cha, M. J., Jang, Y., Chung, N., Choi, S. Y., and Hwang, K. C. (2008) Enhanced calreticulin expression promotes calcium-dependent apoptosis in postnatal cardiomyocytes. Mol. Cells 25, 390-396
25. Rong, Y., and Distelhorst, C. W. (2008) Bcl-2 protein family members. Versatile regulators of calcium signaling in cell survival and apoptosis. Annu. Rev. Physiol. 70, 73-91
26. 2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ. 15, 274-282
27. Nakamura, K., Bossy-Wetzel, E., Burns, K., Fadel, M. P., Lozyk, M., Goping, I. S., Opas, M., Bleackley, R. C., Green, D. R., and Michalak, M. (2000) Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J. Cell Biol. 150, 731-740
28. Mizushima, N., and Yoshimori, T. (2007) How to interpret LC3 immunoblotting. Autophagy 3, 542-545
29. Liang, X. H., Jackson, S., Seaman, M., Brown, K., Kempkes, B., Hibshoosh, H., and Levine, B. (1999) Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676
30. Chen, D., Texada, D. E., Duggan, C., Liang, C., Reden, T. B., Kooragayala, L. M., and Langford, M. P. (2005) Surface calreticulin mediates muramyl dipeptide-induced apoptosis in RK13 cells. J. Biol. Chem. 280, 22425-22436
31. Obeid, M., Tesniere, A., Ghiringhelli, F., Fimia, G. M., Apetoh, L., Perfettini, J. L., Castedo, M., Mignot, G., Panaretakis, T., Casares, N., Métivier, D., Larochette, N., van Endert, P., Ciccosanti, F., Piacentini, M., Zitvogel, L., and Kroemer, G. (2007) Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54-61
32. Tarr, J. M., Young, P. J., Morse, R., Shaw, D. J., Haigh, R., Petrov, P. G., Johnson, S. J., Winyard, P. G., and Eggleton, P. (2010) A mechanism of release of calreticulin from cells during apoptosis. J. Mol. Biol. 401, 799-812
33. Panaretakis, T., Kepp, O., Brockmeier, U., Tesniere, A., Bjorklund, A. C., Chapman, D. C., Durchschlag, M., Joza, N., Pierron, G., van Endert, P., Yuan, J., Zitvogel, L., Madeo, F., Williams, D. B., and Kroemer, G. (2009) Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J. 28, 578-590
34. Hamilton, M. H., Cook, L. A., McRackan, T. R., Schey, K. L., and Hildebrandt, J. D. (2003) Gamma 2 subunit ofGprotein heterotrimer is an N-end rule ubiquitylation substrate. Proc. Natl. Acad. Sci. U.S.A. 100, 5081-5086
35. Karakozova, M., Kozak, M., Wong, C. C., Bailey, A. O., Yates, J. R., 3rd, Mogilner, A., Zebroski, H., and Kashina, A. (2006) Arginylation of β-actin regulates actin cytoskeleton and cell motility. Science 313, 192-196
36. Michalak, M., Groenendyk, J., Szabo, E., Gold, L. I., and Opas, M. (2009) Calreticulin, a multi-process calcium-buffering chaperone of the endoplasmic reticulum. Biochem. J. 417, 651-666
37. Obeid, M., Panaretakis, T., Joza, N., Tufi, R., Tesniere, A., van Endert, P., Zitvogel, L., and Kroemer, G. (2007) Calreticulin exposure is required for the immunogenicity of γ-irradiation and UVC light-induced apoptosis. Cell Death Differ. 14, 1848-1850
38. Gardai, S. J., Xiao, Y. Q., Dickinson, M., Nick, J. A., Voelker, D. R., Greene, K. E., and Henson, P. M. (2003) By binding SIRPalpha or calreticulin/ CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13-23
39. Obeid, M., Panaretakis, T., Tesniere, A., Joza, N., Tufi, R., Apetoh, L., Ghiringhelli, F., Zitvogel, L., and Kroemer, G. (2007) Leveraging the immune system during chemotherapy. Moving calreticulin to the cell surface converts apoptotic death from "silent" to immunogenic. Cancer Res. 67, 7941-7944
40. Obeid, M., Tesniere, A., Panaretakis, T., Tufi, R., Joza, N., van Endert, P., Ghiringhelli, F., Apetoh, L., Chaput, N., Flament, C., Ullrich, E., de Botton, S., Zitvogel, L., and Kroemer, G. (2007) Ecto-calreticulin in immunogenic chemotherapy. Immunol. Rev. 220, 22-34
41. Zhang, X. W., Yan, X. J., Zhou, Z. R., Yang, F. F., Wu, Z. Y., Sun, H. B., Liang, W. X., Song, A. X., Lallemand-Breitenbach, V., Jeanne, M., Zhang, Q. Y., Yang, H. Y., Huang, Q. H., Zhou, G. B., Tong, J. H., Zhang, Y., Wu, J. H., Hu, H. Y., de Thé, H., Chen, S. J., and Chen, Z. (2010) Arsenic trioxide controls the fate of the PML-RARα oncoprotein by directly binding PML. Science 328, 240-243
42. Afshar, N., Black, B. E., and Paschal, B. M. (2005) Retrotranslocation of the chaperone calreticulin from the endoplasmic reticulum lumen to the cytosol. Mol. Cell Biol. 25, 8844-8853
43. Corbett, E. F., Michalak, K. M., Oikawa, K., Johnson, S., Campbell, I. D., Eggleton, P., Kay, C., and Michalak, M. (2000) The conformation of calreticulin is influenced by the endoplasmic reticulum luminal environment. J. Biol. Chem. 275, 27177-27185
44. Buchan, J. R., and Parker, R. (2009) Eukaryotic stress granules. The ins and outs of translation. Mol. Cell 36, 932-941
45. Anderson, P., and Kedersha, N. (2008) Stress granules. The Tao of RNA triage. Trends Biochem. Sci. 33, 141-150
46. Thomas, M. G., Loschi, M., Desbats, M. A., and Boccaccio, G. L. (2011) RNA granules. The good, the bad and the ugly. Cell Signal. 23, 324-334
47. Arimoto, K., Fukuda, H., Imajoh-Ohmi, S., Saito, H., and Takekawa, M. (2008) Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 10, 1324-1332
48. Kwon, S., Zhang, Y., and Matthias, P. (2007) The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev. 21, 3381-3394
49. Gareau, C., Fournier, M. J., Filion, C., Coudert, L., Martel, D., Labelle, Y., and Mazroui, R. (2011) p21(WAF1/CIP1) upregulation through the stress granule-associated protein CUGBP1 confers resistance to bortezomibmediated apoptosis. PLoS One 6, e20254
50. Xie, W., and Denman, R. B. (2011) Protein methylation and stress granules. Posttranslational remodeler or innocent bystander? Mol. Biol. Int. 2011, 137459
51. Mazroui, R., Di Marco, S., Kaufman, R. J., and Gallouzi, I. E. (2007) Inhibition of the ubiquitin-proteasome system induces stress granule formation. Mol. Biol. Cell 18, 2603-2618
52. Dolzhanskaya, N., Merz, G., Aletta, J. M., and Denman, R. B. (2006) Methylation regulates the intracellular protein-protein and protein-RNA interactions of FMRP. J. Cell Sci. 119, 1933-1946
53. Anderson, P., and Kedersha, N. (2002) Stressful initiations. J. Cell Sci. 115, 3227-3234
54. Mokas, S., Mills, J. R., Garreau, C., Fournier, M. J., Robert, F., Arya, P., Kaufman, R. J., Pelletier, J., and Mazroui, R. (2009) Uncoupling stress granule assembly and translation initiation inhibition. Mol. Biol. Cell 20, 2673-2683
55. Kepp, O., Galluzzi, L., Giordanetto, F., Tesniere, A., Vitale, I., Martins, I., Schlemmer, F., Adjemian, S., Zitvogel, L., and Kroemer, G. (2009) Disruption of the PP1/GADD34 complex induces calreticulin exposure. Cell Cycle 8, 3971-3977