The peripheral neuropathy-linked Trembler and Trembler-J mutant forms of peripheral myelin protein 22 are folding-destabilized

Biochemistry

Volumn 47, Issue 40, 2008, Pages 10620-10629

  Myers, Jeffrey K ^a,b   Mobley, Charles K ^a,c   Sanders, Charles R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DAVIDSON COLLEGE   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABERRATIONS; ANIMAL CELL CULTURE; COPPER; CUSTOMER SATISFACTION; DICHROISM; ELECTRIC RESISTANCE; MECHANISMS; NUCLEAR MAGNETIC RESONANCE; OPTICAL PROPERTIES; QUALITY ASSURANCE; QUALITY FUNCTION DEPLOYMENT; SPECTROSCOPIC ANALYSIS; THREE DIMENSIONAL; TOTAL QUALITY MANAGEMENT; ZINC; ZINC COMPOUNDS;

CIRCULAR DICHROISM; CONFORMATIONAL INSTABILITY; CU; ENDOPLASMIC RETICULUM; HUMAN DISEASES; MEMBRANE PROTEINS; MICROMOLAR AFFINITY; MISFOLDING; MOLECULAR DEFECTS; MOUSE MODELS; PERIPHERAL NEUROPATHY; REFOLDING; SPECTROSCOPIC STUDIES; THREE-DIMENSIONAL STRUCTURING; TOOTH TYPE; WILD-TYPE;

PROTEIN FOLDING;

CUPRIC ION; DETERGENT; DIPALMITOYLPHOSPHATIDYLCHOLINE; LAURYLSARCOSINE; MUTANT PROTEIN; PERIPHERAL MYELIN PROTEIN 22; UNCLASSIFIED DRUG; ZINC;

AMINO ACID SEQUENCE; ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; HEREDITARY MOTOR SENSORY NEUROPATHY; METAL BINDING; MICELLE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PERIPHERAL NEUROPATHY; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; WILD TYPE;

CATIONS, DIVALENT; CIRCULAR DICHROISM; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MYELIN PROTEINS; PERIPHERAL NERVOUS SYSTEM DISEASES; PROTEIN BINDING; PROTEIN FOLDING; TEMPERATURE; ZINC;

EID: 53249125616     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801157p     Document Type: Article

References (69)

1. Bronstein, J. M. (2000) Function of tetraspan proteins in the myelin sheath. Curr. Opin. Neurobiol. 10, 552-557.
2. Quarles, R. H. (2002) Myelin sheaths: Glycoproteins involved in their formation, maintenance and degeneration. Cell. Mol. Life Sci. 59, 1851-1871.
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. Carenini, S., Neuberg, D., Schachner, M., Suter, U., and Martini, R. (1999) Localization and functional roles of PMP22 in peripheral nerves of PO-deficient mice. Glia 28, 256-264.
5. Taylor, V., Zgraggen, C., Naef, R., and Suter, U. (2000) Membrane topology of peripheral myelin protein 22. J. Neurosci. Res. 62, 15-27.
6. 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.
7. Van Itallie, C. M., and Anderson, J. M. (2006) Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68, 403-429.
8. Notterpek, L., Roux, K. J., Amici, S. A., Yazdanpour, A., Rahner, C., and Fletcher, B. S. (2001) Peripheral myelin protein 22 is a constituent of intercellular junctions in epithelia. Proc. Natl. Acad. Sci. U.S.A. 98, 14404-14409.
9. Takeda, Y., Notsu, T., Kitamura, K., and Uyemura, K. (2001) Functional analysis for peripheral myelin protein PASII/PMP22: Is it a member of claudin superfamily? Neurochem. Res. 26, 599-607.
10. Wilson, H. L., Wilson, S. A., Surprenant, A., and North, R. A. (2002) Epithelial membrane proteins induce membrane blebbing and interact with the P2X7 receptor C terminus. J. Biol. Chem. 277, 34017-34023.
11. Van Itallie, C. M., and Anderson, J. M. (2006) Claudins and epithelial paracellular transport. Annu. Rev. Physiol. 68, 403-429.
12. Berger, P., Niemann, A., and Suter, U. (2006) Schwann cells and the pathogenesis of inherited motor and sensory neuropathies (Charcot-Marie-Tooth disease). Glia 54, 243-257.
13. Jetten, A. M., and Suter, U. (2000) The peripheral myelin protein 22 and epithelial membrane protein family. Prog. Nucleic Acid Res. Mol. Biol. 64, 97-129.
14. Ryan, M. C., Shooter, E. M., and Notterpek, L. (2002) Aggresome formation in neuropathy models based on peripheral myelin protein 22 mutations. Neurobiol. Dis. 10, 109-118.
15. Sanders, C. R., Ismail-Beigi, F., and McEnery, M. W. (2001) Mutations of peripheral myelin protein 22 result in defective trafficking through mechanisms which may be common to diseases involving tetraspan membrane proteins. Biochemistry 40, 9453-9459.
16. 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.
17. Colby, J., Nicholson, R., Dickson, K. M., Orfali, W., Naef, R., Suter, U., and Snipes, G. J. (2000) PMP22 carrying the trembler or trembler-J mutation is intracellularly retained in myelinating Schwann cells. Neurobiol. Dis. 7, 561-573.
18. Young, P., and Suter, U. (2001) Disease mechanisms and potential therapeutic strategies in Charcot-Marie-Tooth disease. Brain Res. Brain Res. Rev. 36, 213-221.
19. D'Urso, D., Prior, R., Greiner-Petter, R., Gabreels-Festen, A. A., and Muller, H. W. (1998) Overloaded endoplasmic reticulum-Golgi compartments, a possible pathomechanism of peripheral neuropathies caused by mutations of the peripheral myelin protein PMP22. J. Neurosci. 18, 731-740.
20. Fortun, J., Dunn, W. A., Jr., Joy, S., Li, J., and Notterpek, L. (2003) Emerging role for autophagy in the removal of aggresomes in Schwann cells. J. Neurosci. 23, 10672-10680.
21. 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.
22. Fortun, J., Verrier, J. D., Go, J. C., Madorsky, I., Dunn, W. A., and Notterpek, L. (2007) The formation of peripheral myelin protein 22 aggregates is hindered by the enhancement of autophagy and expression of cytoplasmic chaperones. Neurobiol. Dis. 25, 252-265.
23. Liu, N., Yamauchi, J., and Shooter, E. M. (2004) Recessive, but not dominant, mutations in peripheral myelin protein 22 gene show unique patterns of aggregation and intracellular trafficking. Neurobiol. Dis. 17, 300-309.
24. Naef, R., and Suter, U. (1999) Impaired intracellular trafficking is a common disease mechanism of PMP22 point mutations in peripheral neuropathies. Neurobiol. Dis. 6, 1-14.
25. Notterpek, L., Ryan, M. C., Tobler, A. R., and Shooter, E. M. (1999) PMP22 accumulation in aggresomes: Implications for CMT1A pathology. Neurobiol. Dis. 6, 450-460.
26. Tobler, A. R., Notterpek, L., Naef, R., Taylor, V., Suter, U., and Shooter, E. M. (1999) Transport of Trembler-J mutant peripheral myelin protein 22 is blocked in the intermediate compartment and affects the transport of the wild-type protein by direct interaction. J. Neurosci. 19, 2027-2036.
27. Tobler, A. R., Liu, N., Mueller, L., and Shooter, E. M. (2002) Differential aggregation of the Trembler and Trembler J mutants of peripheral myelin protein 22. Proc. Natl. Acad. Sci. U.S.A. 99, 483-488.
28. Dickson, K. M., Bergeron, J. J. M., 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.
29. Sedzik, J., Kotake, Y., and Uyemura, K. (1998) Purification of PASII/PMP22: An extremely hydrophobic glycoprotein of PNS myelin membrane. NeuroReport 9, 1595-1600.
30. Sedzik, J., Uyemura, K., and Tsukihara, T. (2002) Towards crystallization of hydrophobic myelin glycoproteins: P0 and PASII/PMP22. Protein Expression Purif. 26, 368-377.
31. Frederickson, C. J., Suh, S. W., Silva, D., Frederickson, C. J., and Thompson, R. B. (2000) Importance of zinc in the central nervous system: The zinc-containing neuron. J. Nutr. 130, 1471S-1483S.
32. Que, E. L., Domaille, D. W., and Chang, C. J. (2008) Metals in neurobiology: Probing their chemistry and biology with molecular imaging. Chem. Rev. 108, 1517-1549.
33. Unal, B., Tan, H., Orbak, Z., Kiki, I., Bilici, M., Bilici, N., Aslan, H., and Kaplan, S. (2005) Morphological alterations produced by zinc deficiency in rat sciatic nerve: A histological, electron microscopic, and stereological study. Brain Res. 1048, 228-234.
34. Gong, H., and Amemiya, T. (2001) Optic nerve changes in zinc-deficient rats. Exp. Eye Res. 72, 363-369.
35. Kursula, P., Merilainen, G., Lehto, V. P., and Heape, A. M. (1999) The small myelin-associated glycoprotein is a zinc-binding protein. J. Neurochem. 73, 2110-2118.
36. Riccio, P., Giovannelli, S., Bobba, A., Romito, E., Fasano, A., Bleve-Zacheo, T., Favilla, R., Quagliariello, E., and Cavatorta, P. (1995) Specificity of zinc binding to myelin basic protein. Neurochem. Res. 20, 1107-1113.
37. Tsang, D., Tsang, Y. S., Ho, W. K., and Wong, R. N. (1997) Myelin basic protein is a zinc-binding protein in brain: Possible role in myelin compaction. Neurochem. Res. 22, 811-819.
38. Pace, C. N., and Scholtz, J. M. (1997) Measuring the conformational stability of a protein. In Protein Structure: A Practical Approach (Creighton, T. E., Ed.) pp 299-321, IRL Press, Oxford, U.K.
39. Weigelt, J., Miles, C. S., Dixon, N. E., and Otting, G. (1998) Backbone NMR assignments and secondary structure of the N-terminal domain of DnaB helicase from E. coli. J. Biomol. NMR 11, 233-234.
40. Lau, F. W., and Bowie, J. U. (1997) A method for assessing the stability of a membrane protein. Biochemistry 36, 5884-5892.
41. Sehgal, P., Mogensen, J. E., and Otzen, D. E. (2005) Using micellar mole fractions to assess membrane protein stability in mixed micelles. Biochim. Biophys. Acta 1716, 59-68.
42. Lorch, M., and Booth, P. J. (2004) Insertion kinetics of a denatured α helical membrane protein into phospholipid bilayer vesicles. J. Mol. Biol. 344, 1109-1121.
43. Nagy, J. K., and Sanders, C. R. (2004) Destabilizing mutations promote membrane protein misfolding. Biochemistry 43, 19-25.
44. Mackenzie, K. R. (2006) Folding and stability of α-helical integral membrane proteins. Chem. Rev. 106, 1931-1977.
45. Seddon, A. M., Curnow, P., and Booth, P. J. (2004) Membrane proteins, lipids and detergents: Not just a soap opera. Biochim. Biophys. Acta 1666, 105-117.
46. Stanley, A. M., and Fleming, K. G. (2008) The process of folding proteins into membranes: Challenges and progress. Arch. Biochem. Biophys. 469, 46-66.
47. Popot, J. L., and Engelman, D. M. (1990) Membrane protein folding and oligomerization: The two-stage model. Biochemistry 29, 4031-4037.
48. Sanders, C. R., and Myers, J. K. (2004) Disease-related misassembly of membrane proteins. Annu. Rev. Biophys. Biomol. Struct. 33, 25-51.
49. Krebs, M. P., Noorwez, S. M., Malhotra, R., and Kaushal, S. (2004) Quality control of integral membrane proteins. Trends Biochem. Sci. 29, 648-655.
50. Helenius, A., and Aebi, M. (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049.
51. Anelli, T., and Sitia, R. (2008) Protein quality control in the early secretory pathway. EMBO J. 27, 315-327.
52. Brodsky, J. L. (2007) The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem. J. 404, 353-363.
53. 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.
54. Wiseman, R. L., Koulov, A., Powers, E., Kelly, J. W., and Balch, W. E. (2007) Protein energetics in maturation of the early secretory pathway. Curr. Opin. Cell Biol. 19, 359-367.
55. Pareek, S., Notterpek, L., Snipes, G. J., Naef, R., Sossin, W., Laliberte, J., Iacampo, S., Suter, U., Shooter, E. M., and Murphy, R. A. (1997) Neurons promote the translocation of peripheral myelin protein 22 into myelin. J. Neurosci. 17, 7754-7762.
56. Tobler, A. R., Liu, N., Mueller, L., and Shooter, E. M. (2002) Differential aggregation of the Trembler and Trembler J mutants of peripheral myelin protein 22. Proc. Natl. Acad. Sci. U.S.A. 99, 483-488.
57. 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.
58. Booth, P. J., Templer, R. H., Meijberg, W., Allen, S. J., Curran, A. R., and Lorch, M. (2001) In vitro studies of membrane protein folding. Crit. Rev. Biochem. Mol. Biol. 36, 501-603.
59. Nagy, J. K., Lonzer, W. L., and Sanders, C. R. (2001) Kinetic study of folding and misfolding of diacylglycerol kinase in model membranes. Biochemistry 40, 8971-8980.
60. Otzen, D. E. (2003) Folding of DsbB in mixed micelles: A kinetic analysis of the stability of a bacterial membrane protein. J. Mol. Biol. 330, 641-649.
61. Tamm, L. K., Hong, H., and Liang, B. (2004) Folding and assembly of β-barrel membrane proteins. Biochim. Biophys. Acta 1666, 250-263.
62. Partridge, A. W., Therien, A. G., and Deber, C. M. (2004) Missense mutations in transmembrane domains of proteins: Phenotypic propensity of polar residues for human disease. Proteins 54, 648-656.
63. Sanders, C. R. (2005) Post-integration misassembly of membrane protein and disease. In Protein-Lipid Interactions (Tamm, L. K., Ed.) pp 81-94, Wiley-VCH, Weinheim, Germany.
64. Korkhov, V. M., Milan-Lobo, L., Zuber, B., Farhan, H., Schmid, J. A., Freissmuth, M., and Sitte, H. H. (2008) Peptide-based interactions with calnexin target misassembled membrane proteins into endoplasmic reticulum-derived multilamellar bodies. J. Mol. Biol. 378, 337-352.
65. Bond, P. J., and Sansom, M. S. (2003) Membrane protein dynamics versus environment: Simulations of OmpA in a micelle and in a bilayer. J. Mol. Biol. 329, 1035-1053.
66. Cloez, I., and Bourre, J. M. (1987) Copper, manganese and zinc in the developing brain of control and quaking mice. Neurosci. Lett. 83, 118-122.
67. 2 on membrane interactions in myelin of normal and shiverer mice. Biochim. Biophys. Acta 776, 197-208.
68. D'Urso, D., Ehrhardt, P., and Muller, H. W. (1999) Peripheral myelin protein 22 and protein zero: A novel association in peripheral nervous system myelin. J. Neurosci. 19, 3396-3403.
69. 2+-immobilized metal affinity chromatography. Neurochem. Res. 24, 723-732.