Proteolipid protein cannot replace P0 protein as the major structural protein of peripheral nervous system myelin

GLIA

Volumn 63, Issue 1, 2015, Pages 66-77

  Yin, Xinghua ^a   Kiryu Seo, Sumiko ^a   Kidd, Grahame J ^a   Feltri, M Laura ^b   Wrabetz, Lawrence ^b   Trapp, Bruce D ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Axon; Hypomyelination; Myelin compaction; Myelin evolution; Schwann cell

Indexed keywords

MYELIN; PROTEIN P0; PROTEOLIPID PROTEIN; STRUCTURAL PROTEIN; UNCLASSIFIED DRUG; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN PROTEIN;

ANIMAL CELL; ARTICLE; CAUSE OF DEATH; CYTOPLASM; DISABILITY; GENETIC MANIPULATION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LIFESPAN; MOTOR PERFORMANCE; MOUSE; MYELIN SHEATH; MYELINATED NERVE; MYELINATION; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PERIODICITY; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SCHWANN CELL; SCIATIC NERVE; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING; WILD TYPE; ANIMAL; AXON; GENETICS; METABOLISM;

ANIMALS; AXONS; MICE; MYELIN P0 PROTEIN; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; MYELIN-ASSOCIATED GLYCOPROTEIN; PERIPHERAL NERVOUS SYSTEM; SCHWANN CELLS; SCIATIC NERVE;

EID: 84911986715     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22733     Document Type: Article

References (57)

1. Anderson TJ, Montague P, Nadon N, Nave KA, Griffiths IR. 1997. Modification of Schwann cell phenotype with Plp transgenes: Evidence that the PLP and DM20 isoproteins are targeted to different cellular domains. J Neurosci Res 50:13-22.
2. Balice-Gordon RJ, Bone LJ, Scherer SS. 1998. Functional gap junctions in the Schwann cell myelin sheath. J Cell Biol 142:1095-1104.
3. D'Urso D, Brophy PJ, Staugaitis SM, Gillespie CS, Frey AB, Stempak JG, Colman DR. 1990. Protein zero of peripheral nerve myelin: Biosynthesis, membrane insertion, and evidence for homotypic interaction. Neuron 2:449-460.
4. Dhaunchak AS, Colman DR, Nave KA. 2011. Misalignment of PLP/DM20 transmembrane domains determines protein misfolding in Pelizaeus-Merzbacher disease. J Neurosci 31:14961-14971.
5. Edgar JM, McLaughlin M, Yool D, Zhang SC, Fowler JH, Montague P, Barrie JA, McCulloch MC, Duncan ID, Garbern J, Nave KA, Griffiths IR. 2004. Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J Cell Biol 166:121-131.
6. Feltri ML, D'antonio M, Quattrini A, Numerato R, Arona M, Previtali S, Chiu SY, Messing A, Wrabetz L. 1999. A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur J Neurosci 11:1577-1586.
7. 0 protein as a homophilic adhesion molecule. Nature 344:871-872.
8. 0 gene disruption leads to hypomyelination, abnormal expression of recognition molecules, and degeneration of myelin and axons. Cell 71:565-576.
9. Gow A, Lazzarini RA. 1996. A cellular mechanism governing the severity of Pelizaeus-Merzbacher disease. Nat Genet 13:422-428.
10. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave K-A. 1998. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610-1613.
11. 0 protein and the myelin-associated glycoprotein in peripheral nerves from Trembler mice. J Neurocytol 20:439-449.
12. Hodes ME, Woodward K, Spinner NB, Emanuel BS, Enrico-Simon A, Kamholz J, Stambolian D, Zackai EH, Pratt VM, Thomas IT, Crandall K, Dlouhy SR, Malcolm S. 2000. Additional copies of the proteolipid protein gene causing Pelizaeus-Merzbacher disease arise by separate integration into the X chromosome. Am J Hum Genet 67:14-22.
13. Horvath LI, Brophy PJ, Marsh D. 1988. Exchange rates at the lipid-protein interface of myelin proteolipid protein studied by spin-label electron spin resonance. Biochemistry 27:46-52.
14. Hoyer H, Braathen GJ, Eek AK, Skjelbred CF, Russel MB. 2011. Charcot-Marie-Tooth caused by a copy number variation in myelin protein zero. Eur J Med Genet 54:e580-e583.
15. Hudson LD. 2004. Proteolipid protein gene. In: Lazzarini RA, editor. Myelin biology and disorders. San Diego: Elsevier Academic Press. pp 401-420.
16. Inouye H, Tsuruta H, Sedzik J, Uyemura K, Kirschner DA. 1999. Tetrameric assembly of full-sequence protein zero myelin glycoprotein by synchrotron X-ray scattering. Biophys J 76:423-437.
17. Karim SA, Barrie JA, McCulloch MC, Montague P, Edgar JM, Kirkham D, Anderson TJ, Nave KA, Griffiths IR, McLaughlin M. 2007. PLP overexpression perturbs myelin protein composition and myelination in a mouse model of Pelizaeus-Merzbacher disease. Glia 55:341-351.
18. Karim SA, Barrie JA, McCulloch MC, Montague P, Edgar JM, Iden DL, Anderson TJ, Nave KA, Griffiths IR, McLaughlin M. 2010. PLP/DM20 expression and turnover in a transgenic mouse model of Pelizaeus-Merzbacher disease. Glia 58:1727-1738.
19. Kirschner DA, Blaurock AE. 1992. Organization, phylogenetic variations and dynamic transitions of myelin structure. In: Martenson RE, editor. Myelin: Biology and chemistry. Boca Raton, FL: CRC Press. pp 3-78.
20. Kirschner DA, Inouye H, Ganser AL, Mann V. 1989. Myelin membrane structure and composition correlated: A phylogenetic study. J Neurochem 53:1599-1609.
21. Kirschner DA, Wrabetz L, Feltri ML. 2004. The P0 gene. Myelin biology and disorders. San Diego: Elsevier (USA). pp 523-545.
22. Klugmann M, Schwab MH, Puhlhofer A, Schneider A, Zimmermann F, Griffiths IR, Nave KA. 1997. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18:59-70.
23. Kurihara T, Sakuma M, Gojobori T. 1997. Molecular evolution of myelin proteolipid protein. Biochem Biophys Res Commun 237:559-561.
24. Lemke G, Axel R. 1985. Isolation and sequence of a cDNA encoding the major structural protein of peripheral myelin. Cell 40:501-508.
25. Macklin WB, Campagnoni CW, Deininger PL, Gardinier MV. 1987. Structure and expression of the mouse myelin proteolipid gene. J Neurosci Res 18:383-394.
26. Maeda MH, Mitsui J, Soong BW, Takahashi Y, Ishiura H, Hayashi S, Shirota Y, Ichikawa Y, Matsumoto H, Arai M, Okamoto T, Miyama S, Shimizu J, Inazawa J, Goto J, Tsuji S. 2012. Increased gene dosage of myelin protein zero causes Charcot-Marie-Tooth disease. Ann Neurol 71:84-92.
27. 0-related Dejerine-Sottas syndrome. Ann N Y Acad Sci 883:273-280.
28. 0)-deficient mice show myelin degeneration in peripheral nerves characteristic of inherited human neuropathies. Nat Genet 11:281-286.
29. Milner RJ, Lai C, Nave K-A, Lenoir D, Ogata J, Sutcliffe JG. 1985. Nucleotide sequences of two mRNAs for rat brain myelin proteolipid protein. Cell 42:931-939.
30. Nave KA. 2010. Myelination and the trophic support of long axons. Nat Rev Neurosci 11:275-283.
31. Nave K-A, Boespflug-Tanguy O. 1996. X-linked developmental defects in myelination: From mouse mutants to human genetic diseases. Neuroscientist 2:33-43.
32. Nave K-A, Trapp BD. 2008. Axon-glial signaling and the glial support of axon function. Ann Rev Neurosci 31:535-561.
33. Nave K-A, Lai C, Bloom F, Milner RJ. 1987. Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM20 protein of central nervous system myelin. Proc Natl Acad Sci USA 84:5665-5669.
34. Pedraza L, Huang JK, Colman DR. 2001. Organizing principles of the axoglial apparatus. Neuron 30:335-344.
35. Puckett C, Hudson L, Ono K, Friedrich V, Benecke J, Dubois-Dalcq M, Lazzarini RA. 1987. Myelin-specific proteolipid protein is expressed in myelinating Schwann cells but is not incorporated into myelin sheaths. J Neurosci Res 18:511-518.
36. Rasband MN, Tayler J, Kaga Y, Yang Y, Lappe-Siefke C, Nave KA, Bansal R. 2005. CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50:86-90.
37. Saavedra RA, Fors L, Aebersold RH, Arden B, Horvath S, Sanders J, Hood L. 1989. The myelin proteins of the shark brain are similar to the myelin proteins of the mammalian peripheral nervous system. J Mol Evol 29:149-156.
38. Salzer JL, Brophy PJ, Peles E. 2008. Molecular domains of myelinated axons in the peripheral nervous system. Glia 56:1532-1540.
39. Scherer SS, Deschenes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL. 1995. Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci 15:8281-8294.
40. 0, the major structural protein of peripheral nerve myelin. Neuron 17:435-449.
41. Sporkel O, Uschkureit T, Bussow H, Stoffel W. 2002. Oligodendrocytes expressing exclusively the DM20 isoform of the proteolipid protein gene: Myelination and development. Glia 37:19-30.
42. Sternberger NH, Quarles RH, Itoyama Y, Webster Hd. 1979. Myelin-associated glycoprotein demonstrated immunocytochemically in myelin and myelin-forming cells of developing rats. Proc Natl Acad Sci USA 76:1510-1514.
43. ter Beest MB, Hoekstra K, Sein A, Hoekstra D. 1994. Reconstitution of proteolipid protein: Some properties and its role in interlamellar attachment. Biochem J 300:545-552.
44. Thompson AJ, Cronin MS, Kirschner DA. 2002. Myelin protein zero exists as dimers and tetramers in native membranes of Xenopus laevis peripheral nerve. J Neurosci Res 67:766-771.
45. Trapp BD, Quarles RH. 1982. Presence of the myelin-associated glycoprotein correlates with alterations in the periodicity of peripheral myelin. J Cell Biol 92:877-882.
46. Trapp BD, Kidd GJ. 2004. Structure of the myelinated axon. In: Lazzarini R, editor. Myelin biology and disorders. Amsterdam: Elsevier. pp 3-25.
47. 0 protein in Golgi complex membranes and myelin of developing rat Schwann cells. J Cell Biol 90:1-6.
48. Trapp BD, Andrews SB, Cootauco C, Quarles RH. 1989. The myelin-associated glycoprotein is enriched in multivesicular bodies and periaxonal membranes of actively myelinating oligodendrocytes. J Cell Biol 109:2417-2426.
49. Waehneldt TV. 1990. Phylogeny of myelin proteins. Ann N Y Acad Sci 605:15-28.
50. Waehneldt TV, Matthieu JM, Jeserich G. 1986. Appearance of myelin proteins during vertebrate evolution. Neurochem Int 9:463-474.
51. Wrabetz L, Feltri ML, Quattrini A, Imperiale D, Previtali S, D'antonio M, Martini R, Yin X, Trapp BD, Zhou L, Chiu SY, Messing A. 2000. P(0) glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J Cell Biol 148:1021-1034.
52. Yin X, Crawford TO, Griffin JW, Tu P-H, Lee VMY, Li C, Roder J, Trapp BD. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J Neurosci 18:1953-1962.
53. Yin X, Kidd GJ, Wrabetz L, Feltri ML, Messing A, Trapp BD. 2000. Schwann cell myelination requires timely and precise targeting of P(0) protein. J Cell Biol 148:1009-1020.
54. Yin X, Kidd GJ, Pioro EP, McDonough J, Dutta R, Feltri ML, Wrabetz L, Messing A, Wyatt RM, Balice-Gordon RJ, Trapp BD. 2004. Dysmyelinated lower motor neurons retract and regenerate dysfunctional synaptic terminals. J Neurosci 24:3890-3898.
55. Yin X, Baek RC, Kirschner DA, Peterson A, Fujii Y, Nave KA, Macklin WB, Trapp BD. 2006. Evolution of a neuroprotective function of central nervous system myelin. J Cell Biol 172:469-478.
56. Yin X, Kidd GJ, Nave KA, Trapp BD. 2008. P0 protein is required for and can induce formation of Schmidt-Lantermann incisures in myelin internodes. J Neurosci 28:7068-7073.
57. Yoshida M, Colman DR. 1996. Parallel evolution and coexpression of the proteolipid proteins and protein zero in vertebrate myelin. Neuron 16:1115-1126.