Pathology of a mouse mutation in peripheral myelin protein P0 is characteristic of a severe and early onset form of human Charcot-Marie-Tooth type 1B disorder

Journal of Cell Biology

Volumn 165, Issue 4, 2004, Pages 565-573

  Rünker, Annette E ^a,c   Kobsar, Igor ^b   Fink, Torsten ^a   Loers, Gabriele ^a   Tilling, Thomas ^a   Putthoff, Peggy ^a   Wessig, Carsten ^b   Martini, Rudolf ^b   Schachner, Melitta ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Dominant negative effects; Myelin; Myelin P0 protein; Peripheral neuropathies; Tomacula

Indexed keywords

MYELIN PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE; GENE MUTATION; HEREDITARY MOTOR SENSORY NEUROPATHY; MISSENSE MUTATION; MOUSE; MUSCLE ACTION POTENTIAL; MYELIN DEFICIENCY; MYELIN SHEATH; MYELINATION; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; ONSET AGE; PATHOGENESIS; PERIPHERAL MYELIN PROTEIN P0 GENE; PERIPHERAL NEUROPATHY; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; SHIVERING; TRANSGENIC MOUSE;

ALLIUM CEPA; ANIMALIA; MUS MUSCULUS;

EID: 2542495972     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200402087     Document Type: Article

References (54)

1. Adlkofer, K., R. Martini, A. Aguzzi, J. Zielasek, K.V. Toyka, and U. Suter. 1995. Hypermyelination and demyelinating peripheral neuropathy in Pmp22-deficient mice. Nat. Genet. 11:274-280.
2. Adlkofer, K., R. Frei, D.H. Neuberg, J. Zielasek, K.V. Toyka, and U. Suter. 1997. Heterozygous peripheral myelin protein 22-deficient mice are affected by a progressive demyelinating tomaculous neuropathy. J. Neurosci. 17:4662-4671.
3. Archelos, J.J., K. Roggenbuck, J. Schneider-Schaulies, C. Linington, K.V. Toyka, and H.P. Hartung. 1993. Production and characterization of monoclonal antibodies to the extracellular domain of P0. J. Neurosci. Res. 35:46-53.
4. Bennett, C.L., and P.F. Chance. 2001. Molecular pathogenesis of hereditary motor, sensory and autonomic neuropathies. Curr. Opin. Neurol. 14:621-627.
5. Boerkoel, C.F., H. Takashima, P. Stankiewicz, C.A. Garcia, S.M. Leber, L. Rhee-Morris, and J.R. Lupski. 2001. Periaxin mutations cause recessive Dejerine-Sottas neuropathy. Am. J. Hum. Genet. 68:325-333.
6. Cai, Z., K. Cash, J. Swift, P. Sutton-Smith, M. Robinson, P.D. Thompson, and P.C. Blumbergs. 2001. Focal myelin swellings and tomacula in anti-MAG IgM paraproteinaemic neuropathy: novel teased nerve fiber studies. J. Peripher. Nerv. Syst. 6:95-101.
7. Cai, Z., P. Sutton-Smith, J. Swift, K. Cash, J. Finnie, A. Turnley, P.D. Thompson, and P.C. Blumbergs. 2002. Tomacula in MAG-deficient mice. J. Peripher. Nerv. Syst. 7:181-189.
8. Carenini, S., D. Montag, H. Cremer, M. Schachner, and R. Martini. 1997. Absence of the myelin-associated glycoprotein (MAG) and the neural cell adhesion molecule (N-CAM) interferes with the maintenance, but not with the formation of peripheral myelin. Cell Tissue Res. 287:3-9.
9. Carenini, S., M. Maurer, A. Werner, H. Blazyca, K.V. Toyka, C.D. Schmid, G. Raivich, and R. Martini. 2001. The role of macrophages in demyelinating peripheral nervous system of mice heterozygously deficient in P0. J. Cell Biol. 152:301-308.
10. D'Urso, D., P. Ehrhardt, and H.W. Muller. 1999. Peripheral myelin protein 22 and protein zero: a novel association in peripheral nervous system myelin. J. Neurosci. 19:3396-3403.
11. Dyck, P.J., P. Chance, R. Lebo, and J.A. Carney. 1993. Hereditary motor and sensory neuropathies. In Peripheral Neuropathy, 3rd ed. P.J. Dyck, P.K. Thomas, J.W. Griffin, P.A. Low, and J.F. Poduslo, editors. W.B. Saunders, Philadelphia. 1094-1136.
12. Fabrizi, G.M., F. Taioli, T. Cavallaro, F. Rigatelli, A. Simonati, G. Mariani, P. Perrone, and N. Rizzuto. 2000. Focally folded myelin in Charcot-Marie-Tooth neuropathy type 1B with Ser49Leu in the myelin protein zero. Acta Neuropathol. (Berl.). 100:299-304.
13. Feltri, M.L., M. D'Antonio, A. Quattrini, R. Numerato, M. Arona, S. Previtali, S.Y. Chiu, A. Messing, and L. Wrabetz. 1999. A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur. J. Neurosci. 11:1577-1586.
14. Friede, R.L. 1972. Control of myelin formation by axon caliber (with a model of the control mechanism).J. Comp. Neurol. 144:233-252.
15. Gabreëls-Festen, A.A., E.M. Joosten, F.J. Gabreels, D.F. Stegeman, A.J. Vos, and H.F. Busch. 1990. Congenital demyelinating motor and sensory neuropathy with focally folded myelin sheaths. Brain. 113:1629-1643.
16. Gabreëls-Festen, A.A., J.E. Hoogendijk, P.H. Meijerink, F.J. Gabreëls, P.A. Bolhuis, S. van Beersum, T. Kulkens, E. Nelis, F.G. Jennekens, M. de Visser, et al. 1996. Two divergent types of nerve pathology in patients with different P0 mutations in Charcot-Marie-Tooth disease. Neurology. 47:761-765.
17. Giese, K.P., R. Martini, G. Lemke, P. Soriano, and M. Schachner. 1992. Mouse P0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell. 71:565-576.
18. Gillespie, C.S., D.L. Sherman, S.M. Fleetwood-Walker, D.F. Cottrell, S. Tait, E.M. Garry, V.C. Wallace, J. Ure, I.R. Griffiths, A. Smith, and P.J. Brophy. 2000. Peripheral demyelination and neuropathic pain behavior in periaxin-deficient mice. Neuron. 26:523-531.
19. Guilbot, A., A. Williams, N. Ravise, C. Verny, A. Brice, D.L. Sherman, P.J. Brophy, E. LeGuern, V. Delague, C. Bareil, et al. 2001. A mutation in periaxin is responsible for CMT4F, an autosomal recessive form of Charcot-Marie-Tooth disease. Hum. Mol. Genet. 10:415-421.
20. Hayasaka, K., M. Himoro, W. Sato, G. Takada, K. Uyemura, N. Shimizu, T.D. Bird, P.M. Conneally, and P.F. Chance. 1993a. Charcot-Marie-Tooth neuropathy type 1B is associated with mutations of the myelin P0 gene. Nat. Genet. 5:31-34.
21. Hayasaka, K., M. Himoro, Y. Sawaishi, K. Nanao, T. Takahashi, G. Takada, G.A. Nicholson, R.A. Ouvrier, and N. Tachi. 1993b. De novo mutation of the myelin P0 gene in Dejerine-Sottas disease (hereditary motor and sensory neuropathy type III). Nat. Genet. 5:266-268.
22. Hayasaka, K., G. Takada, and V.V. Ionasescu. 1993c. Mutation of the myelin P0 gene in Charcot-Marie-Tooth neuropathy type 1B. Hum. Mol. Genet. 2:1369-1372.
23. fHogan, B., R. Beddington, F. Constantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 497 pp.
24. Inoue, H., H. Tsuruta, J. Sedzik, K. Uyemura, and D.A. Kirschner. 1999. Tetrameric assembly of full-sequence protein zero myelin glycoprotein by synchrotron X-ray scattering. Biophys. J. 76:423-437.
25. Kamholz, J., D. Menichella, A. Jani, J. Garbern, R.A. Lewis, K.M. Krajewski, J. Lilien, S.S. Scherer, and M.E. Shy. 2000. Charcot-Marie-Tooth disease type 1: molecular pathogenesis to gene therapy. Brain. 123:222-233.
26. Kirschner, D.A., and R.A. Saavedra. 1994. Mutations in demyelinating peripheral neuropathies support molecular model of myelin P0-glycoprotein extracellular domain. J. Neurosci. Res. 37:574-583.
27. Kobsar, I., M. Berghoff, M. Samsam, C. Wessig, M. Maurer, K.V. Toyka, and R. Martini. 2003. Preserved myelin integrity and reduced axonopathy in connexin32-deficient mice lacking the recombination activating gene-1. Brain. 126:804-813.
28. Kulkens, T., P.A. Bolhuis, R.A. Wolterman, S. Kemp, S. te Nijenhuis, L.J. Valentijn, G.W. Hensels, F.G. Jennekens, M. de Visser, J.E. Hoogendijk, and F. Baas. 1993. Deletion of the serine 34 codon from the major peripheral myelin protein P0 gene in Charcot-Marie-Tooth disease type 1B. Nat. Genet. 5:35-39.
29. Lemke, G., E. Lamar, and J. Patterson. 1988. Isolation and analysis of the gene encoding peripheral myelin protein zero. Neuron. 1:73-83.
30. Lindberg, R.L.P., R. Martini, M. Baumgartner, B. Erne, J. Borg, J. Zielasek, K. Ricker, A. Steck, K.V. Toyka, and U.A. Meyer. 1999. Motor neuropathy in porphobilinogen deaminase-deficient mice imitates the peripheral neuropathy of human acute porphyria. J. Clin. Invest. 103:1127-1134.
31. Martini, R. 1994. Expression and functional roles of neural cell surface molecules and extracellular matrix components during development and regeneration of peripheral nerves. J. Neurocytol. 23:1-28.
32. Martini, R. 1999. P0-deficient knockout mice as tools to understand pathomechanisms in Charcot-Marie-Tooth 1B and P0-related Dejerine-Sottas syndrome. Ann. NY Acad. Sci. 883:273-280.
33. Martini, R., and M. Schachner. 1997. Molecular bases of myelin formation as revealed by investigations on mice deficient in glial cell surface molecules. Glia. 19:298-310.
34. Martini, R., M.H. Mohajeri, S. Kasper, K.P. Giese, and M. Schachner. 1995a. 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.
35. Martini, R., J. Zielasek, K.V. Toyka, K.P. Giese, and M. Schachner. 1995b. Protein zero (P0)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat. Genet. 11:281-286.
36. Martini, R., J. Zielasek, and K.V. Toyka. 1998. Inherited demyelinating neuropathies: from gene to disease. Curr. Opin. Neurol. 11:545-556.
37. Menichella, D.M., E.J. Arroyo, R. Awatramani, T. Xu, P. Baron, J.M. Vallat, J. Balsamo, J. Lilien, G. Scarlato, J. Kamholz, et al. 2001. Protein zero is necessary for E-cadherin-mediated adherens junction formation in Schwann cells. Mol. Cell. Neurosci. 18:606-618.
38. Nakagawa, M., M. Suehara, A. Saito, H. Takashima, F. Umehara, M. Saito, N. Kanzato, T. Matsuzaki, S. Takenaga, S. Sakoda, et al. 1999. A novel MPZ gene mutation in dominantly inherited neuropathy with focally folded myelin sheaths. Neurology. 52:1271-1275.
39. Rebai, T., C. Mhiri, P. Heine, H. Charfi, C. Meyrignac, and R. Gherardi. 1989. Focal myelin thickenings in a peripheral neuropathy associated with IgM monoclonal gammopathy. Acta Neuropathol. (Berl.). 79:226-232.
40. Schneider-Schaulies, J., A. von Brunn, and M. Schachner. 1990. Recombinant peripheral myelin protein P0 confers both adhesion and neurite outgrowth-promoting properties. J. Neurosci. Res. 27:286-297.
41. Shapiro, L., J.P. Doyle, P. Hensley, D.R. Colman, and W.A. Hendrickson. 1996. Crystal structure of the extracellular domain from P0, the major structural protein of peripheral nerve myelin. Neuron. 17:435-449.
42. Shy, M.E., J.Y. Garbern, and J. Kamholz. 2002. Hereditary motor and sensory neuropathies: a biological perspective. Lancet Neurol. 1:110-118.
43. Sindou, P., J.-M. Vallat, F. Chapon, J. Archelos, F. Tabaraud, T. Anani, K. Braund, T. Maisonobe, J.-J. Hauw, and A. Vandenberghe. 1999. Ultrastructural protein zero expression in Charcot-Marie-Tooth type 1B disease. Muscle Nerve. 22:99-104.
44. Suter, U., and K.A. Nave. 1999. Transgenic mouse models of CMT1A and HNPP. Ann. NY Acad. Sci. 883:247-253.
45. Tachi, N., N. Kozuka, K. Ohya, S. Chiba, and K. Sasaki. 1997. Tomaculous neuropathy in Charcot-Marie-Tooth disease with myelin protein zero gene mutation. J. Neurol. Sci. 153:106-109.
46. Takashima, H., C.F. Boerkoel, P. De Jonghe, C. Ceuterick, J.J. Martin, T. Voit, J.M. Schroder, A. Williams, P.J. Brophy, V. Timmerman, and J.R. Lupski. 2002. Periaxin mutations cause a broad spectrum of demyelinating neuropathies. Ann. Neurol. 51:709-715.
47. Thomas, F.P., R.V. Lebo, G. Rosoklija, X.S. Ding, R.E. Lovelace, N. Latov, and A.P. Hays. 1994. Tomaculous neuropathy in chromosome 1 Charcot-Marie-Tooth syndrome. Acta Neuropathol. (Berl.). 87:91-97.
48. Warner, L.E., M.J. Hilz, S.H. Appel, J.M. Killian, E.H. Kolodry, G. Karpati, S. Carpenter, G.V. Watters, C. Wheeler, D. Witt, et al. 1996. Clinical phenotypes of different MPZ (P0) mutations may include Charcot-Marie-Tooth type 1B, Dejerine-Sottas, and congenital hypomyelination. Neuron. 17:451-460.
49. Wrabetz, L., M.L. Feltri, A. Quattrini, D. Imperiale, S. Previtali, M. D'Antonio, R. Martini, X. Yin, B.D. Trapp, L. Zhou, et al. 2000. P(0) glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J. Cell Biol. 148:1021-1034.
50. Yin, X., G.J. Kidd, L. Wrabetz, M.L. Feltri, A. Messing, and B.D. Trapp. 2000. Schwann cell myelination requires timely and precise targeting of P0 protein. J. Cell Biol. 148:1009-1020.
51. You, K.H., C.L. Hsieh, C. Hayes, N. Stahl, U. Francke, and B. Popko. 1991. DNA sequence, genomic organization, and chromosomal localization of the mouse peripheral myelin protein zero gene: identification of polymorphic alleles. Genomics. 9:751-757.
52. Young, P., and U. Suter. 2001. Disease mechanisms and potential therapeutic strategies in Charcot-Marie-Tooth disease. Brain Res. Brain Res. Rev. 36:213-221.
53. Young, P., and U. Suter. 2003. The causes of Charcot-Marie-Tooth disease. Cell. Mol. Life Sci. 60:2547-2560.
54. Zielasek, J., M. Martini, and K.V. Toyka. 1996. Functional abnormalities in P0-deficient mice resemble human hereditary neuropathies linked to P0 gene mutations. Muscle Nerve. 19:946-952.