Specialization of endoplasmic reticulum chaperones for the folding and function of myelin glycoproteins P0 and PMP22

FASEB Journal

Volumn 25, Issue 11, 2011, Pages 3929-3937

  Jung, Joanna ^a   Coe, Helen ^a   Michalak, Marek ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Calnexin; Calreticulin; ERp57; Myelin disease; Protein folding; Quality control

Indexed keywords

CALNEXIN; CALRETICULIN; CHAPERONE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOPROTEIN; OXIDOREDUCTASE; PERIPHERAL MYELIN PROTEIN 22; PROTEIN P0; PROTEIN P57; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONFOCAL MICROSCOPY; DISULFIDE BOND; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME DEFICIENCY; MOUSE; MUTATION; NONHUMAN; PATHOGENESIS; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SYNTHESIS;

ANIMALS; CALNEXIN; CALRETICULIN; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; MICE; MOLECULAR CHAPERONES; MYELIN P0 PROTEIN; MYELIN PROTEINS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING;

EID: 80355148479     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-184911     Document Type: Article

References (40)

1. Quarles, R. H. (2002) Myelin sheaths: glycoproteins involved in their formation, maintenance and degeneration. Cell. Mol. Life Sci. 59, 1851-1871
2. Mobley, C. K., Myers, J. K., Hadziselimovic, A., Ellis, C. D., and Sanders, C. R. (2007) Purification and initiation of structural characterization of human peripheral myelin protein 22, an integral membrane protein linked to peripheral neuropathies. Biochemistry 46, 11185-11195 (Pubitemid 47502784)
3. Adlkofer, K., Martini, R., Aguzzi, A., Zielasek, J., Toyka, K. V., and Suter, U. (1995) Hypermyelination and demyelinating peripheral neuropathy in Pmp22-deficient mice. Nat. Genet. 11, 274-280
4. Sereda, M., Griffiths, I., Puhlhofer, A., Stewart, H., Rossner, M. J., Zimmerman, F., Magyar, J. P., Schneider, A., Hund, E., Meinck, H. M., Suter, U., and Nave, K. A. (1996) A transgenic rat model of Charcot-Marie-Tooth disease. Neuron 16, 1049-1060 (Pubitemid 26171699)
5. Pennuto, M., Tinelli, E., Malaguti, M., Del Carro, U., D'Antonio, M., Ron, D., Quattrini, A., Feltri, M. L., and Wrabetz, L. (2008) Ablation of the UPR-mediator CHOP restores motor function and reduces demyelination in Charcot-Marie-Tooth 1B mice. Neuron 57, 393-405 (Pubitemid 351179164)
6. Hebert, D. N., and Molinari, M. (2007) In and out of the ER: protein folding, quality control, degradation, and related human diseases. Physiol. Rev. 87, 1377-1408 (Pubitemid 350041473)
7. Zapun, A., Darby, N. J., Tessier, D. C., Michalak, M., Bergeron, J. J., and Thomas, D. Y. (1998) Enhanced catalysis of ribonuclease B folding by the interaction of calnexin or calreticulin with ERp57. J. Biol. Chem. 273, 6009-6012 (Pubitemid 28144676)
8. Mesaeli, N., Nakamura, K., Zvaritch, E., Dickie, P., Dziak, E., Krause, K.-H., Opas, M., MacLennan, D. H., and Michalak, M. (1999) Calreticulin is essential for cardiac development. J. Cell Biol. 144, 857-868 (Pubitemid 29238963)
9. Coe, H., Jung, J., Groenendyk, J., Prins, D., and Michalak, M. (2009) ERp57 modulates STAT3 signalling from the lumen of the endoplasmic reticulum. J. Biol. Chem. 285, 6725-6738
10. Kraus, A., Groenendyk, J., Bedard, K., Baldwin, T. A., Krause, K. H., Dubois-Dauphin, M., Dyck, J., Rosenbaum, E. E., Korngut, L., Colley, N. J., Gosgnach, S., Zochodne, D., Todd, K., Agellon, L. B., and Michalak, M. (2010) Calnexin deficiency leads to dysmyelination. J. Biol. Chem. 285, 18928-18938
11. Suter, D. M., Cartier, L., Bettiol, E., Tirefort, D., Jaconi, M. E., Dubois-Dauphin, M., and Krause, K. H. (2006) Rapid generation of stable transgenic embryonic stem cell lines using modular lentivectors. Stem Cells 24, 615-623 (Pubitemid 44464765)
12. Nakamura, K., Zuppini, A., Arnaudeau, S., Lynch, J., Ahsan, I., Krause, R., Papp, S., De Smedt, H., Parys, J. B., Müller-Esterl, W., Lew, D. P., Krause, K.-H., Demaurex, N., Opas, M., and Michalak, M. (2001) Functional specialization of calreticulin domains. J. Cell Biol. 154, 961-972 (Pubitemid 34286176)
13. Coe, H., Bedard, K., Groenendyk, J., Jung, J., and Michalak, M. (2008) Endoplasmic reticulum stress in the absence of calnexin. Cell Stress Chaperones 13, 497-507
14. Milner, R. E., Baksh, S., Shemanko, C., Carpenter, M. R., Smillie, L., Vance, J. E., Opas, M., and Michalak, M. (1991) Calreticulin, and not calsequestrin, is the major calcium binding protein of smooth muscle sarcoplasmic reticulum and liver endoplasmic reticulum. J. Biol. Chem. 266, 7155-7165 (Pubitemid 21906346)
15. Zuppini, A., Groenendyk, J., Cormack, L. A., Shore, G., Opas, M., Bleackley, R. C., and Michalak, M. (2002) Calnexin deficiency and endoplasmic reticulum stress-induced apoptosis. Biochemistry 41, 2850-2858 (Pubitemid 34168955)
16. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
17. Keskanokwong, T., Shandro, H. J., Johnson, D. E., Kittanakom, S., Vilas, G. L., Thorner, P., Reithmeier, R. A., Akkarapatumwong, V., Yenchitsomanus, P. T., and Casey, J. R. (2007) Interaction of integrin-linked kinase with the kidney chloride/bicarbonate exchanger, kAE1. J. Biol. Chem. 282, 23205-23218 (Pubitemid 47311943)
18. Ekici, A. B., Oezbey, S., Fuchs, C., Nelis, E., Van Broeckhoven, C., Schachner, M., and Rautenstrauss, B. (2002) Tracing myelin protein zero (P0) in vivo by construction of P0-GFP fusion proteins. BMC Cell Biol. 3, 29
19. Caramelo, J. J., and Parodi, A. J. (2008) Getting in and out from calnexin/calreticulin cycles. J. Biol. Chem. 283, 10221-10225
20. Shen, S., Tan, T. H., and Tan, Y. J. (2007) Expression, glycosylation, and modification of the spike (S) glycoprotein of SARS CoV. Methods Mol. Biol. 379, 127-135 (Pubitemid 350183357)
21. Fontanini, A., Chies, R., Snapp, E. L., Ferrarini, M., Fabrizi, G. M., and Brancolini, C. (2005) Glycan-independent role of calnexin in the intracellular retention of Charcot-Marie-tooth 1A Gas3/PMP22 mutants. J. Biol. Chem. 280, 2378-2387
22. Plotkowski, M. L., Kim, S., Phillips, M. L., Partridge, A. W., Deber, C. M., and Bowie, J. U. (2007) Transmembrane domain of myelin protein zero can form dimers: possible implications for myelin construction. Biochemistry 46, 12164-12173 (Pubitemid 350022371)
23. Martini, R., Mohajeri, M. H., Kasper, S., Giese, K. P., and Schachner, M. (1995) Mice doubly deficient in the genes for P0 and myelin basic protein show that both proteins contribute to the formation of the major dense line in peripheral nerve myelin. J. Neurosci. 15, 4488-4495
24. Hasse, B., Bosse, F., Hanenberg, H., and Muller, H. W. (2004) Peripheral myelin protein 22 kDa and protein zero: domain specific trans-interactions. Mol. Cell. Neurosci. 27, 370-378 (Pubitemid 39539992)
25. Grandis, M., Vigo, T., Passalacqua, M., Jain, M., Scazzola, S., La Padula, V., Brucal, M., Benvenuto, F., Nobbio, L., Cadoni, A., Mancardi, G. L., Kamholz, J., Shy, M. E., and Schenone, A. (2008) Different cellular and molecular mechanisms for early and late-onset myelin protein zero mutations. Hum. Mol. Genet. 17, 1877-1889 (Pubitemid 351865837)
26. Zhang, K., and Filbin, M. T. (1998) Myelin Po protein mutated at Cys21 has a dominant-negative effect on adhesion of wild type Po. J. Neurosci. Res. 53, 1-6 (Pubitemid 28308976)
27. Guo, L., Groenendyk, J., Papp, S., Dabrowska, M., Knoblach, B., Kay, C., Parker, J. M. R., Opas, M., and Michalak, M. (2003) Identification of an N-domain histidine essential for chaperone function in calreticulin. J. Biol. Chem. 278, 50645-50653 (Pubitemid 37548913)
28. Pfend, G., Matthieu, J. M., Garin, N., and Tosic, M. (2001) Implication of the extracellular disulfide bond on myelin protein zero expression. Neurochem. Res. 26, 503-510 (Pubitemid 32744300)
29. Zhang, K., and Filbin, M. T. (1994) Formation of a disulfide bond in the immunoglobulin domain of the myelin P0 protein is essential for its adhesion. J. Neurochem. 63, 367-370 (Pubitemid 24184939)
30. Bedard, K., Szabo, E., Michalak, M., and Opas, M. (2005) Cellular functions of endoplasmic reticulum chaperones calreticulin, calnexin, and ERp57. Int. Rev. Cytol. 245, 91-121
31. Molinari, M., Eriksson, K. K., Calanca, V., Galli, C., Cresswell, P., Michalak, M., and Helenius, A. (2004) Contrasting functions of calreticulin and calnexin in glycoprotein folding and ER quality control. Mol. Cell. 13, 125-135 (Pubitemid 38117121)
32. Aebi, M., Bernasconi, R., Clerc, S., and Molinari, M. (2010) N-glycan structures: recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82
33. Maattanen, P., Gehring, K., Bergeron, J. J., and Thomas, D. Y. (2010) Protein quality control in the ER: the recognition of misfolded proteins. Semin. Cell. Dev. Biol. 21, 500-511
34. 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
35. Fortun, J., Li, J., Go, J., Fenstermaker, A., Fletcher, B. S., and Notterpek, L. (2005) Impaired proteasome activity and accumulation of ubiquitinated substrates in a hereditary neuropathy model. J. Neurochem. 92, 1531-1541 (Pubitemid 40389221)
36. Dickson, K. M., Bergeron, J. J., Shames, I., Colby, J., Nguyen, D. T., Chevet, E., Thomas, D. Y., and Snipes, G. J. (2002) Association of calnexin with mutant peripheral myelin protein-22 ex vivo: a basis for "gain-of- function" ER diseases. Proc. Natl. Acad. Sci. U. S. A. 99, 9852-9857 (Pubitemid 34831136)
37. Wrabetz, L., Feltri, M. L., Quattrini, A., Imperiale, D., Previtali, S., D'Antonio, M., Martini, R., Yin, X., Trapp, B. D., Zhou, L., Chiu, S. Y., and Messing, A. (2000) P(0) glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J. Cell Biol. 148, 1021-1034
38. Yin, X., Kidd, G. J., Wrabetz, L., Feltri, M. L., Messing, A., and Trapp, B. D. (2000) Schwann cell myelination requires timely and precise targeting of P(0) protein. J. Cell Biol. 148, 1009-1020
39. Solda, T., Garbi, N., Hammerling, G. J., and Molinari, M. (2006) Consequences of ERp57 deletion on oxidative folding of obligate and facultative clients of the calnexin cycle. J. Biol. Chem. 281, 6219-6226 (Pubitemid 43847552)
40. Garbi, N., Tanaka, S., Momburg, F., and Hammerling, G. J. (2006) Impaired assembly of the major histocompatibility complex class I peptide-loading complex in mice deficient in the oxidoreductase ERp57. Nat. Immunol. 7, 93-102 (Pubitemid 41823873)