Impaired intracellular trafficking is a common disease mechanism of PMP22 point mutations in peripheral neuropathies

Neurobiology of Disease

Volumn 6, Issue 1, 1999, Pages 1-14

  Naef, Roland ^a   Suter, Ueli ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN; MYELIN PROTEIN;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; HEREDITARY MOTOR SENSORY NEUROPATHY; INTRACELLULAR TRANSPORT; MYELINATION; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PERIPHERAL NEUROPATHY; POINT MUTATION; PRIORITY JOURNAL; SCHWANN CELL;

EID: 0032894049     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1006/nbdi.1998.0227     Document Type: Article

References (78)

1. Adlkofer K., Martini R., Aguzzi A., Zielasek J., Toyka K. V., Suter U. Hypermyelination and demyelinating peripheral neuropathy in Pmp22-deficient mice. Nat. Genet. 11:1995;274-280.
2. Adlkofer K., Frei R., Neuberg D. H. H., Zielasek J., Toyka K. V., Suter U. Heterozygous peripheral myelin protein 22-deficient mice are affected by a progressive demyelinating tomaculous neuropathy. J. Neurosci. 17:1997a;4662-4671.
3. Adlkofer K., Naef R., Suter U. Analysis of compound heterozygous mice reveals that the Trembler mutation can behave as a gain-of-function allele. J. Neurosci. Res. 49:1997b;671-680.
4. Anzini P., Neuberg D. H.-H., Schachner M., Nelles E., Willecke K., Zielasek J., Toyka K., Suter U., Martini R. Structural abnormalities and deficient maintenance of peripheral nerve myelin in mice lacking the gap junction protein Connexin32. J. Neurosci. 17:1997;4545-4551.
5. Baechner D., Liehr T., Hameister H., Altenberger H., Grehl H., Suter U., Rautenstrauss B. Widespread expression of the peripheral myelin protein-22 gene (PMP22) in the neural and nonneural tissues during murine development. J. Neurosci. Res. 42:1995;733-741.
6. Bolin L. M., McNeil T., Lucian L. A., DeVaux B., Franz-Bacon K., Gorman D. M., Zurawski S., Murray R., McClanahan T. K. HNMP-1: A novel hematopoietic and neural membrane protein differentially regulated in neural development and injury. J. Neurosci. 17:1997;5493-5502.
7. Brockes J. P., Fields K. L., Raff M. C. Studies on cultured rat Schwann cells. Derivation of purified populations from cultures of peripheral nerve. Brain Res. 165:1979;105-118.
8. Chance P. F., Alderson M. K., Leppig K. A., Lensch M. W., Matsunami N., Smith B., Swanson P. D., Odelberg S. J., Disteche C. M., Bird T. D. DNA deletion associated with hereditary neuropathy with liability to pressure palsies. Cell. 72:1993;143-151.
9. D'Urso D., Muller H. W. Ins and outs of peripheral myelin protein-22: Mapping transmembrane topology and intracellular sorting. J. Neurosci. Res. 49:1997a;551-562.
10. D'Urso D., Schmalenbach C., Zoidl G., Prior R., Muller H. W. Studies on the effects of altered PMP22 expression during myelination in vitro. J. Neurosci. Res. 48:1997b;31-42.
11. D'Urso D., Prior R., Greiner-Petter R., Gabreels-Festen A. A. W. M., Muller H. W. Overloaded endoplasmic reticulum-Golgi compartments, a possible pathomechanism of peripheral neuropathies caused by mutations of the peripheral myelin protein PMP22. J. Neurosci. 18:1998;731-740.
12. De Jonghe P., Timmerman V., Nelis E., Martin J.-J., Van Broeckhoven C. Charcot-Marie-Tooth disease and related peripheral neuropathies. J. Periph. Nervous System. 2:1997;370-387.
13. de Waegh S. M., Lee V. M., Brady S. T. Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell. 68:1992;451-463.
14. Dejerine J., Sottas J. Sur la névrite interstitielle, hypertrophique et progressive de l'enfance. C. R. Soc. Biol. 45:1893;63-96.
15. Deschenes S. M., Walcott J. L., Wexler T. L., Scherer S. S., Fischbeck K. H. Altered trafficking of mutant connexin32. J. Neurosci. 17:1997;9077-9084.
16. Dyck P. J., Chance P. F., Lebo R., Carney J. A. Hereditary motor and sensory neuropathies. Peripheral Neuropathies. 1993;W. B. Saunders, Philadelphia. p. 1094-1136.
17. Fabbretti E., Edomi P., Brancolini C., Schneider C. Apoptotic phenotype induced by overexpression of wild-type gas3/PMP22: Its relation to the demyelinating peripheral neuropathy CMT1A. Genes Dev. 9:1995;1846-1856.
18. Gabreels-Festen A. A. W. M., Gabreels F. J. M., Jennekens F. G. I. Hereditary motor and sensory neuropathies: Present status of types I, II and III. Clin. Neurol. Neurosurg. 95:1993;93-107.
19. Gabreels-Festen A. A. W. M., Gabreels F. J. M., Jennekens F. G. I., Janssen-van Kempen T. W. The status of HMSN type III. Neuromuscul. Disord. 4:1994;63-69.
20. Gabreels-Festen A. A. W. M., Bolhuis P. A., Hoogendijk J. E., Valentijn L. J., Eshuis E. J. H. M., Gabreels F. J. M. Charcot-Marie-Tooth disease type 1A: morphological phenotype of the 17p duplication versus PMP22 point mutations. Acta Neuropathol. 90:1995;645-649.
21. Gow A., Grangerov A., Gard A., Colman D. R., Lazzarini R. A. Conservation of topology, but not conformation, of the proteolipid proteins of the myelin sheath. J. Neurosci. 17:1997;181-189.
22. Griffiths I. R. Myelin mutants: Model systems for the study of normal and abnormal myelination. BioEssays. 18:1996;789-797.
23. Haney C., Snipes G. J., Shooter E. M., Suter U., Garcia C., Griffin J. W., Trapp B. D. Ultrastructural distribution of PMP22 in Charcot-Marie-Tooth disease type 1A. J. Neuropathol. Exp. Neurol. 55:1996;290-299.
24. Hoogendijk J. E., Janssen E. A. M., Gabreels-Festen A. A. W. M., Ongerboer de Visser B. W., Visser M., Bolhuis P. A. Allelic heterogeneity in hereditary motor and sensory neuropathy type Charcot-Marie-Tooth disease type 1a. Neurology. 43:1993;1010-1015.
25. Huxley C., Passage E., Manson A., Putzu G., Figarella-Branger D., Pellisier J. F., Fontes M. Construction of a mouse model of Charcot-Marie-Tooth disease type 1A by pronuclear injection of human YAC DNA. Hum. Mol. Genet. 5:1996;563-569.
26. Huxley C., Passage E., Robertson A. M., Youl B., Huston S., Manson A., Saberan-Djoniedi D., Figarella-Branger D., Pellissier J. F., Thomas P. K., Fontes M. Correlation between varying levels of PMP22 expression and the degree of demyelination and reduction in nerve conduction velocity in transgenic mice. Hum. Mol. Genet. 7:1998;449-458.
27. Ionasescu V. V., Ionasescu R., Searby C., Neahring R. Dejerine-Sottas disease with de novo dominant point mutation of the PMP22 gene. Neurology. 45:1995;1766-1767.
28. Ionasescu V. V., Searby C., Greenberg S. A. Dejerine Sottas disease with sensorineural hearing loss, nystagmus, and peripheral facial nerve weakness: De Novo dominant point mutation of the PMP22 gene. J. Med. Genet. 33:1996;1048-1049.
29. Ionasescu V. V., Searby C. C., Ionasescu R., Chatkupt S., Patel N., Koenigsberger R. Dejerine-Sottas neuropathy in mother and son with same point mutation of PMP22 gene. Muscle Nerve. 20:1997;97-99.
30. Jung M., Sommer I., Schachner M., Nave K. A. Monoclonal antibody O10 defines a conformationally sensitive cell-surface epitope of proteolipid protein (PLP): Evidence that PLP misfolding underlies dysmyelination in mutant mice. J. Neurosci. 16:1996;7920-7929.
31. Lopes J., Vandenberghe A., Tardieu S., Ionasescu V., Levy N., Wood N., Tachi N., Bouche P., Latour P., Brice A., LeGuern E. Sex-dependent rearrangements resulting in CMT1A and HNPP. Nat. Genet. 17:1997;136-137.
32. Lupski J. R., Garcia C. A., Parry G. J., Patel P. I. Charcot-Marie-Tooth polyneuropathy syndrome: Clinical, elecrophysiological, and genetic aspects. Appel S. Current Neurology. 1991a;1-25 Mosby-Yearbook, Chicago.
33. Lupski J. R., de Oca Luna R. M., Slaugenhaupt S., Pentao L., Guzzetta V., Trask B. J., Saucedo-Cardenas O., Barker D. F., Killian J. M., Garcia C. A., Chakravarti A., Patel P. I. DNA duplication associated with Charcot-Marie-Tooth disease type 1A. Cell. 66:1991b;219-232.
34. Magyar J. P., Martini R., Ruelicke T., Aguzzi A., Adlkofer K., Dembic Z., Zielasek J., Toyka K. V., Suter U. Impaired differentiation of Schwann cells in transgenic mice with increased PMP22 gene dosage. J. Neurosci. 16:1996;5351-5360.
35. Marvin K. W., Fujimoto W., Jetten A. M. Identification and characterization of a novel squamous cell-associated gene related to PMP22. J. Biol. Chem. 270:1995;28910-28916.
36. Matsunami N., Smith B., Ballard L., Lensch M. W., Robertson M., Albertsen H., Hanemann C. O., Muller H. W., Bird T. D., White R., Chance P. F. Peripheral myelin protein-22 gene maps in the duplication in chromosome 17p11.2 associated with Charcot-Marie-Tooth 1A. Nat. Genet. 1:1992;176-179.
37. Naef R., Adlkofer K., Lescher B., Suter U. Aberrant protein trafficking in Trembler suggests a disease mechanism for hereditary human peripheral neuropathies. Mol. Cell. Neurosci. 9:1997;13-25.
38. Naef R., Suter U. Many facets of PMP22 in myelination and disease. Microsc. Res. Tech. 41:1998;359-371.
39. Navon R., Seifried B., Gal-On N. S., Sadeh M. A new point mutation affecting the fourth transmembrane domain of PMP22 results in severe de novo Charcot-Marie-Tooth disease. Hum. Genet. 97:1996;685-687.
40. Nelis E., Van Broeckhoven C., Consortium C. Estimation of the mutation frequencies in Charcot-Marie-Tooth disease type 1 and hereditary neuropathy with liability to pressure palsies: A European collaborative study. Eur. J. Hum. Genet. 4:1996;25-33.
41. Nelis E., Holmberg B., Adolfsson R., Holmgren G., Van Broeckhoven C. PMP22 Thr(118)Met: Recessive CMT1 mutation or polymorphism. Nat. Genet. 15:1997;13-14.
42. Notterpek L., Shooter E. M., Snipes G. J. Upregulation of the endosomal-lysosomal pathway in the trembler-J neuropathy. J. Neurosci. 17:1997;4190-4200.
43. Ohnishi A. Clinical, pathologic and molecular genetic studies of patients with hereditary motor and sensory neuropathy (HMSN). Rinsho Shinkeigaku. 35:1995;1438-1440.
44. Ouvrier R. A., McLeod J. G., Conchin T. E. The hypertrophic forms of hereditary motor and sensory neuropathy. A study of hypertrophic Charcot-Marie-Tooth disease (HMSN type I) and Dejerine-Sottas disease (HMSN type III) in childhood. Brain. 110:1987;121-148.
45. Pareek S., Suter U., Snipes G. J., Welcher A. A., Shooter E. M., Murphy R. A. Detection and processing of peripheral myelin protein PMP22 in cultured Schwann cells. J. Biol. Chem. 268:1993;10372-10379.
46. Pareek S., Notterpek L., Snipes G. J., Naef R., Sossin W., Laliberté J., Iacampo S., Suter U., Shooter E. M., Murphy R. A. Neurons promote the translocation of peripheral myelin protein 22 into myelin. J. Neurosci. 17:1997;7754-7762.
47. Parmantier E., Cabon F., Braun C., D'Urso D., Muller H. W., Zalc B. Peripheral meyelin protein-22 is expressed in rat and mouse brain and spinal cord motoneurons. Eur. J. Neurosci. 7:1995;1080-1088.
48. Parmantier E., Braun C., Thomas J. L., Peyron F., Martinez S., Zalc B. PMP-22 expression in the central nervous system of the embryonic mouse defines potential transverse segments and longitudinal columns. J. Comp. Neurol. 378:1997;159-172.
49. Patel P. I., Roa B. B., Welcher A. A., Schoener-Scott R., Trask B. J., Pentao L., Snipes G. J., Garcia C. A., Francke U., Shooter E. M., Lupski J. R., Suter U. The gene for the peripheral myelin protein PMP-22 is a candidate for Charcot-Marie-Tooth disease type 1A. Nat. Genet. 1:1992;159-165.
50. Raeymaekers P., Timmerman V., Nelis E., De Jonghe P., Hoogendijk J. E., Baas F., Barker D. F., Martin J. J., De Visser M., Bolhuis P. A., Van Broeckhoven C. Duplication in chromosome 17p11.2 in Charcot-Marie-Tooth neuropathy type 1a (CMT 1a). The HMSN Collaborative Research Group. Neuromuscul. Disord. 1:1991;93-97.
51. Roa B. B., Dyck P. J., Marks H. G., Chance P. F., Lupski J. R. Dejerine-Sottas syndrome associated with point mutation in the peripheral myelin protein 22 (PMP22) gene. Nat. Genet. 5:1993a;269-272.
52. Roa B. B., Garcia C. A., Suter U., Kulpa D. A., Wise C. A., Mueller J., Welcher A. A., Snipes G. J., Shooter E. M., Patel P. I., Lupski J. R. Charcot-Marie-Tooth disease type 1A: Association with a spontaneous point mutation in the PMP22 gene. N. Engl. J. Med. 329:1993b;96-101.
53. Roa B. B., Garcia C. A., Pentao L., Killian J. M., Trask B. J., Suter U., Snipes G. J., Shooter E. M., Patel P. I., Lupski J. R. Evidence for a recessive PMP22 point mutation in Charcot-Marie-Tooth disease type 1A. Nat. Genet. 5:1993c;189-194.
54. Scherer S. S. The biology and pathobiology of Schwann cells. Curr. Opin. Neurol. 10:1997a;386-397.
55. Scherer S. S. Molecular genetics of demyelination: New wrinkles on an old membrane. Neuron. 18:1997b;13-16.
56. Sereda M., Griffiths I., Puhlhofer A., Stewart H., Rossner M. J., Zimmermann F., Magyar J. P., Schneider A., Hund E., Meinck H.-M., Suter U., Nave K. A. A rat transgenic model for Charcot-Marie-Tooth disease. Neuron. 16:1996;1049-1060.
57. Skoff R. P. Programmed cell death in the dysmyelinating mutants. Brain Pathol. 5:1995;283-288.
58. Snipes G. J., Suter U., Welcher A. A., Shooter E. M. Characterization of a novel peripheral nervous system myelin protein (PMP-22/SR13). J. Cell Biol. 117:1992;225-238.
59. Snipes G. J., Suter U., Shooter E. M. Human peripheral myelin protein-22 carries the L2/HNK-1 carbohydrate adhesion epitope. J. Neurochem. 61:1993;1961-1964.
60. Snipes G. J., Suter U. Molecular basis of common hereditary motor and sensory neuropathies in humans and in mouse models. Brain Pathol. 5:1995;233-247.
61. Spreyer P., Kuhn G., Hanemann C. O., Gillen C., Schaal H., Kuhn R., Lemke G., Muller H. W. Axon-regulated expression of a Schwann cell transcript that is homologous to a 'growth arrest-specific' gene. EMBO J. 10:1991;3661-3668.
62. Suter U., Welcher A. A., Ozcelik T., Snipes G. J., Kosaras B., Francke U., Billings G. S., Sidman R. L., Shooter E. M. Trembler mouse carries a point mutation in a myelin gene. Nature. 356:1992a;241-244.
63. Suter U., Moskow J. J., Welcher A. A., Snipes G. J., Kosaras B., Sidman R. L., Buchberg A. M., Shooter E. M. A leucine-to-proline mutation in the putative first transmembrane domain of the 22-kDa peripheral myelin protein in the trembler-J mouse. Proc. Natl. Acad. Sci. USA. 89:1992b;4382-4386.
64. Suter U., Angst C., Tien C. L., Drinkwater C. C., Lindsay R. M., Shooter E. M. NGF/BDNF chimeric proteins: Analysis of neurotrophin specificity by homolog-scanning mutagenesis. J. Neurosci. 12:1992c;306-318.
65. Suter U., Welcher A. A., Snipes G. J. Progress in the molecular understanding of hereditary peripheral neuropathies reveals new insights into the biology of the peripheral nervous system. Trends Neurosci. 16:1993;50-56.
66. Suter U., Snipes G. J. Peripheral myelin protein 22: Facts and hypotheses. J. Neurosci. Res. 40:1995;145-151.
67. Taylor V., Welcher A. A., Suter U. Epithelial membrane protein-1, peripheral myelin protein 22 and lens membrane protein 20 define a novel gene family. J. Biol. Chem. 270:1995;28824-28833.
68. Taylor V., Suter U. Epithelial membrane protein-2 and epithelial membrane protein-3: Two novel members of the peripheral myelin protein 22 gene family. Gene. 175:1996;115-120.
69. Thomas P. J., Qu B.-H., Pedersen L. P. Defective protein folding as a basis of human disease. Trends Biochem. 20:1995;456-459.
70. Timmerman V., Nelis E., Van Hul W., Nieuwenhuijsen B. W., Chen K. L., Wang S., Ben Othman K., Cullen B., Leach R. J., Hanemann C. O., De Jonghe P., Raeymaekers P., van Ommen G.-J. B., Martin J.-J., Muller H. W., Vance J. M., Fischbeck K. H., Van Broeckhoven C. The peripheral myelin protein gene PMP-22 is contained within the Charcot-Marie-Tooth disease type 1A duplication. Nat. Genet. 1:1992;171-175.
71. Valentijn L. J., Bolhuis P. A., Zorn I., Hoogendijk J. E., van den Bosch N., Hensels G. W., Stanton J. V. P., Housman D. E., Fischbeck K. H., Ross D. A., Nicholson G. A., Meershoek E. J., Dauwerse H. G., van Ommen G.-J. B., Bass F. The peripheral myelin gene PMP-22/GAS-3 is duplicated in Charcot-Marie-Tooth disease type 1A. Nat. Genet. 1:1992a;166-170.
72. Valentijn L. J., Bass F., Wolterman R. A., Hoogendijk J. E., Bosch N. H. A., Zorn I., Gabreels-Festen A. A. W. M., de Visser M., Bolhuis P. A. Identical point mutations of PMP-22 in Trembler-J mouse and Charcot-Marie-Tooth disease type 1a. Nat. Genet. 2:1992b;288-291.
73. Valentijn L. J., Ouvrier R. A., van den Bosch N. H., Bolhuis P. A., Baas F., Nicholson G. A. Dejerine-Sottas neuropathy is associated with a de novo PMP22 mutation. Hum. Mutat. 5:1995;76-80.
74. Vallat J. M., Sindou P., Preux P. M., Tabaraud F., Milor A. M., Couratier P., LeGuern E., Brice A. Ultrastructural PMP22 expression in inherited demyelinating neuropathies. Ann. Neurol. 39:1996;813-817.
75. Welcher A. A., Suter U., De Leon M., Snipes G. J., Shooter E. M. A myelin protein is encoded by the homologue of a growth arrest-specific gene. Proc. Natl. Acad. Sci. USA. 88:1991;7195-7199.
76. Yoshimura T., Satake M., Ohnishi A., Tsutsumi Y., Fujikura Y. Mutations of connexin32 in Charcot-Marie-Tooth disease type X interfere with cell-to-cell communication but not cell proliferation and myelin-specific gene expression. J. Neurosci. Res. 51:1998;154-161.
77. Zoidl G., Blass-Kampmann S., D'Urso D., Schmalenbach C., Muller H. W. Retroviral-mediated gene transfer of the peripheral myelin protein PMP22 in Schwann cells: Modulation of cell growth. EMBO J. 14:1995;1122-1128.
78. Zoidl G., D'Urso D., Blass-Kampmann S., Schmalenbach C., Kuhn R., Muller H. W. Influence of elevated expression of rat wild-type PMP22 and its mutant PMP22Trembler on cell growth of NIH3T3 fibroblasts. Cell Tissue Res. 287:1997;459-470.