Calnexin: A versatile calcium binding integral membrane-bound chaperone of endoplasmic reticulum

Calcium Binding Proteins

Volumn 2, Issue 1, 2007, Pages 36-43

  Sarwat, Maryam ^a   Tuteja, Narendra ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Calcium binding proteins; Calnexin; Calreticulin; Chaperone; Endoplasmic reticulum; ERAD; Glycoproteins; Protein folding; Unfolded protein response

Indexed keywords

EID: 35348845440     PISSN: 15548643     EISSN: 15548651     Source Type: Journal    
DOI: None     Document Type: Review

References (73)

1. Tuteja N, Mahajan S. Calcium Signaling Network in Plants. Plant Signaling Behavior 2007; 2:79-85.
2. Gray PW, Byers MG, Eddy RL, Shows TB. The assignment of the calnexin gene to the q35 region of chromosome 5. In: Human Genome Mapping Workshop 1993; 93:9.
3. Tjoelker LW, Seyfried CE, Eddy RL Jr, Byers MG, Shows TB, Calderon J, Schreiber RB, Gray PW. Human, mouse, and rat calnexin cDNA cloning: identification of potential calcium binding motifs and gene localization to human chromosome 5. Biochemistry 1994; 33:3229-36.
4. Michalak M, Milner RE, Burns K, Opas M. Calreticulin. Biochem J 1992; 285:681-692.
5. Williams DB. Calnexin: A molecular chaperone with a taste for carbohydrate. Biochem Cell Biol 1995; 73: 123-32.
6. Huang L, Franklin AE, Hoffman NE. Primary structure and characterization of an Arabidopsis thaliana calnexin-like protein. J Boil Chem 1993; 268:6560-6.
7. Wada I, Rindress D, Cameron PH, Ou WJ, Doherty JJ 2nd, Louvard D, Bell AW, Dignard D, Thomas DY, Bergeron JJ. SSR alpha and associated calnexin are major calcium binding proteins of the endoplasmic reticulum membrane. J Biol Chem 1991; 266:19599-10.
8. Swanton E, High S, Woodman P. Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J 2003; 22:2948-58.
9. Schrag JD, Bergeron JJ, Li Y, Borisova S, Hahn M, Thomas DY, Cygler M. The structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell 2001; 8:633-44.
10. Sambrook JF. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell. 1990; 61:197-9.
11. Bootman MD, Collins TJ, Peppiat CM, Prothero LS, MacKenzie L, De Smet P, Travers M, Tovey SC, Seo JT, Berridge MJ, Ciccolini F, Lipp P. Calcium signalling - an overview. Semin Cell Dev Biol 2001; 12:3-10.
12. Leach MR, Cohen-Doyle MF, Thomas DY, Williams DB. Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J Biol Chem 2002; 277:29686-97.
13. Collin P, Beauregard PB, Elagoz A, Rokeach LA. A non-chromosomal factor allows viability of Schizosaccharomyces pombe lacking the essential chaperone calnexin. J Cell Sci 2004;117:907-18.
14. Denzel A, Molinari M, Trigueros C, Martin JE, Velmurgan S, Brown S, Stamp G, Owen MJ. Early postnatal death and motor disorders in mice congenitally deficient in calnexin expression. Mol Cell Biol 2002; 22:7398-404.
15. Helenius A, Aebi M. Intracellular functions of N-linked glycans. Science 2001; 291:2364-9.
16. Hauri H, Appenzeller C, Kuhn F, Nufer O. Lectins and traffic in the secretory pathway. FEBS Lett. 2000; 476:32-37.
17. Crofts AJ, Denecke J. Calreticulin and calnexin in plants. Trends Plant Sci 1998; 3:396-9.
18. Molinari M, Eriksson KK, Calanca V, Galli C, Cresswell P, Michalak M, Helenius A. Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Molecular Cell 2004;13:125-35.
19. Lee W, Lee TH, Park BJ, Chang JW, Yu JR, Koo HS, Park H, Yoo YJ, Ahnn J. Caenorhabditis elegans calnexin is N-glycosylated and required for stress response. Biochem Biophys Res Commun 2005; 338:1018-30.
20. Lee W, Kim KR, Singaravelu G, Park BJ, Kim DH, Ahnn J, Yoo YJ. Alternative chaperone machinery may compensate for calreticulin/calnexin deficiency in Caenorhabditis elegans. Proteomics 2006; 6:1329-39.
21. 2+ regulation, and photoreceptor cell survival. Neuron 2006; 49:229-241.
22. Saito Y, Ihara Y, Leach MR, Cohen-Doyle MF, Williams DB. Calreticulin functions in vitro as a molecular chaperone for both glycosylated and non-glycosylated proteins. EMBO J 1999; 18:6718-29.
23. Ihara Y, Cohen-Doyle MF, Saito Y, Williams DB. Calnexin discriminates between protein conformational states and functions as a molecular chaperone in vitro. Mol Cell 1999; 4:331-41.
24. Zapun A, Petrescu SM, Rudd PM, Dwek RA, Thomas DY, Bergeron JJ. Conformation-independent binding of monoglucosylated ribonuclease B to calnexin. Cell 1997; 88:29-38.
25. Vassilakos A, Michalak M, Lehrman MA. Oligosaccharide binding characteristics of the molecular chaperones calnexin and calreticulin. Biochemistry 1998; 37:3480-90.
26. Nauseef WM, McCormick SJ, Clark RA. Calreticulin functions as a molecular chaperone in the biosynthesis of myeloperoxidase. J Biol Chem 1995; 270:4741-7.
27. Sousa MC, Ferrero-Garcia MA, Parodi AJ. Recognition of the oligosaccharide and protein moieties of glycoproteins by the UDP-Glc:glycoprotein glucosyltransferase. Biochemistry 1992; 31:97-105.
28. Vitale A. Uncovering secretory secrets inhibition of endoplasmic reticulum (ER) glucosidases suggests a critical role for ER quality control in plant growth and development. Plant Cell 2001; 13:1260-2.
29. Szumilo T, Kaushal GP, Albein AD. Purification and properties of glucosidase I from mung bean seedlings. Arch Biochem Biophys 1986; 247:261-71.
30. Kaushal GP, Pastuszak I, Hatana K, Elbein AD. Purification to homogeneity and properties of glucosidase II from mungbean seedlings and suspension cultured soybean cells. J Biol Chem 1990; 265:1627-9.
31. Kaushal GP, Zeng Y, Elbein AD. Biosynthesis of glucosidase II from mungbean seedlings and suspension cultured soybean cells. J Biol Chem 1993; 268:14536-42.
32. Parodi AJ, Mendelzon DH, Lederkremer GH, Martin-Barrientos J. Evidence that transient glucosylation of protein linked Man9GlcNac2, Man8Glc Nac2 and Man7Glc Nac2 occurs in rat liver and Phaseolus vulgaris cells. J Biol Chem 1984; 259:6351-7
33. Taylor MA, Ross HA, McRae D, Stewart D, Roberts I, Duncan G, Wright F, Millam S, Davies HV. A potato α-glucosidase II-like activity: Demonstration of enzyme activity and effects of downregulation in transgenic plants. Plants J 2000; 24:305-16.
34. Gillikin JW, Zhang F, Coleman CE, Bass HW, Larkins BA, Boston RS. A defective signal peptide tethers the floury-2 zein to the endoplasmic reticulum membrane. Plant Physiol 1997; 114:345-52.
35. Thomson SP, Williams DB. Delineation of the lectin site of the molecular chaperone calreticulin. Cell Stress Chaperones 2005; 10:242-51.
36. Zapun A, Darby NJ, Tessier DC, Michalak M, Bergeron JJM, Thomas DY. Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J Biol Chem 1998; 273:6009-12.
37. Pollock S, Kozlov G, Pelletier MF, Trempe JF, JansenG, Sitnikov D, Bergeron JJ, Gehring K, Ekiel I, Thomas DY. Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J 2004; 23:1020-9.
38. Nicchitta CV. Biochemical, cell biological and immunological issues surrounding the endoplasmic reticulum chaperone GRP94/gp96r. Curr Opin Immunol 1998; 10:103-9.
39. Gething MJ. Role and regulation of the ER chaperone BiP. Semin Cell Dev Biol 1999; 10:465-72.
40. Williams DB. Beyond lectins: the calnexin/ calreticulin chaperon system of the endoplasmic reticulum. J Cell Sci 2006; 119:615-23.
41. Hammond C, Braakman I, Helenius A. Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc Nad Acad Sci USA 1994; 91:913-7.
42. Hebert DN, Foellmer B, Helenius A. Glucose trimming and reglucosylation determine glycoprotein association with calnexin in the endoplasmic reticulum. Cell 1995; 81:425-33.
43. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 2000; 404:770-4.
44. Davletova S, Schlauch K, Coutu J, Mittler R. The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 2005;139:847-56.
45. 2+ binding domains. J Biol Chem 1991; 26632:21458-65.
46. Danilczyk UG, Cohen-Doyle MF, Williams DB. Functional relationship between calreticulin, calnexin, and the endoplasmic reticulum luminal domain of calnexin. J Biol Chem 2000; 275:13089-97.
47. Dickson KM, Bergeron JJM, Shames I, Colby J, Nguyen DT, Chevet E, Thomas DY, Snipes GJ. Association of calnexin with mutant peripheral myelin protein-22 ex vivo: a basis for 'gain-of-function' ER diseases. Proc Natl Acad Sci USA 2002; 99:9852-7.
48. Ellgaard L, Riek R, Herrmann T, Güntert P, Braun D, Helenius A, Wüthrich K. NMR structure of the calreticulin P-domain. Proc Nad Acad Sci USA 2001; 98:3133-8.
49. Thammavongsa V, Mancino L, Raghavan M. Polypeptide substrate recognition by calnexin requires specific conformations of the calnexin protein. J Biol Chem 2005; 280:33497-505.
50. Kwiatkowski BA, Zielinkska-Kwiatkowska AG, Migdalski A, Kleczkowski LA, Wasilweska LD. Cloning of two cDNAs encoding calnexin-like proteins from maize (Zea mays) leaves: identification of potential calcium-binding domains. Gene 1995; 65:219-22.
51. Goode JH, Settlage SB, Wilson RF, Dewey RE. Isolation of a calnexin homolog from developing soybean seeds. Plant Physiol (PGR) 1995; 108:1341.
52. Ehtesham NZ, Phan TN, Gaikwad A, Sopory SK, Tuteja N. Calnexin from Pisum sativum: cloning of the cDNA and characterization of the encoded protein. DNA Cell Biol 1999; 18:853-62.
53. 2+ spike frequency can optimize gene expression. Nature 1998; 392: 936-41.
54. 2+) oscillations via an interaction with SERCA2b. J Cell Biol 2000; 149:1235-48.
55. Apse MP, Ahaton GS, Snedden WA, Blumwald E. Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 1999; 285:1256-8.
56. Zhang HX, Hodson, JN, Williams JP, Blumwald E. Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Nad Acad Sci USA 2001; 98:12832-6.
57. Rajagopal D, Agarwal P, Tyagi W, Singla-Pareek SL, Reddy MK, Sopory SK. Characterization of an isoform of Na+/H+ antiporter from Pennisetum glaucum that confers high level of salinity tolerance in transgenic Brassica juncea. Mol Breed 2007; 19:137-51.
58. Fukuda A, Nakamura A, Tagiri A, Tanaka H, Miyao A, Hirochika H, Tanaka Y. Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 2004; 45:149-59.
59. Takizawa T, Tatematsu C, Watanabe K, Kato K, Nakanishi Y. Cleavage of calnexin caused by apoptotic stimuli: implication for the regulation of apoptosis. J Biochem (Tokyo) 2004; 136:399-405.
60. Degen E, Williams DB. Participation of a novel 88 kDa protein in the biogenesis of murine class I histocompatibility molecules. J Cell Biol 1991;112:1099-115.
61. Degen E, Cohen-Doyle MF, Williams DB. Efficient dissociation of the p88 chaperone from major histocompatibility complex class I molecules requires both beta 2-microglobulin and peptide. J Exp Med 1992;175:1653-61.
62. Hochstenbach F, David V, Watkins S, Brenner MB. Endoplasmic reticulum resident protein of 90 kilodaltons associates with the T- and B-cell antigen receptors and major histocompatibility complex antigens during their assembly. Proc Natl Acad Sci U S A. 1992; 89:4734-8.
63. Rajagopalan S, Xu Y, Brenner MB. Retention of unassembled components of integral membrane proteins by calnexin. Science 1994; 263:387-90.
64. Bergeton JJ, Brenner MB, Thomas DY, Williams DB. Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem Sci. 1994;19:124-8.
65. Wada I, Imai S, Kai M, Sakane F, Kanoh H. Chaperone function of calreticulin when expressed in the endoplasmic reticulum as the membrane-anchored and soluble forms. J Biol Chem 1995; 270:20298-304.
66. 2+. J Biol Chem 1995; 270:18051-9.
67. Arunachalam B, Cresswell P. Molecular requirements for the interaction of class II major histocompatibility complex molecules and invariant chain with calnexin. J Biol Chem 1995; 270:2784-90.
68. Boston RS, Gillikin JW, Wrobel RL. Coordinate induction of three ER lumenal stress proteins in maize endosperm mutants. J Cell Biochem 1996; 19A:143.
69. Oliver JD, van der Wal FJ, Bulleid NJ, High S. Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 1997; 275:86-8.
70. Kaufman RJ, Pipe SW, Tagliavacca L, Swaroop M, Moussalli M. Biosynthesis, assembly and secrerion of coagulation factor VIII. Blood Coag Fibrinolys 1997; 8:S13-4.
71. Frigerio L, Vitale A, Lord JM, Ceriotti A, Roberts LM. Free ricin A chain, proricin, and native toxin have different cellular fates when expressed in tobacco protoplasts. J Biol Chem 1998; 273: 14194-9.
72. Velloso LM, Svensson K, Lahtinen U, Schinder G, Petterson RF, Lindqvist Y. Expression, purification, refolding and crystallization of the carbohydrate-recognition domain of p58/ERGIC-53, an animal C-type lectin involved in export of glycoproteins from the endoplasmic reticulum. Acta Crysrallogr D Biol Crystallogr 2002; 58:536-8.
73. Kamauchi S, Nakatani H, Nakano C, Utade R. Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J 2005; 272:3461-76.