Congenital hypomyelinating neuropathy with lethal conduction failure in mice carrying the Egr2 I268N mutation

Journal of Neuroscience

Volumn 29, Issue 8, 2009, Pages 2312-2321

  Baloh, Robert H ^a   Strickland, Amy ^a   Ryu, Elizabeth ^a   Le, Nam ^a   Fahrner, Timothy ^a   Yang, Mao ^a   Nagarajan, Rakesh ^a   Milbrandt, Jeffrey ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Axon; Myelin; Nerve; Neuromuscular junction; Neuropathy; Peripheral nerve

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; MYELIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NAB2; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MALFORMATION; CONGENITAL HYPOMYELINATION NEUROPATHY; CONTROLLED STUDY; CRANIAL NERVE; GENE MUTATION; GENETIC TRANSCRIPTION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; HUMAN CELL; MOUSE; NERVE BLOCK; NERVE CONDUCTION; NERVE GROWTH; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR TRANSMISSION; NEUROPATHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; SCIATIC NERVE; WEANING;

ANIMALS; ASPARAGINE; CELL LINE, TRANSFORMED; CELL PROLIFERATION; CHARCOT-MARIE-TOOTH DISEASE; CRANIAL NERVE DISEASES; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 2; HUMANS; IMMUNOPRECIPITATION; ISOLEUCINE; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MYELIN PROTEINS; NEOPLASM PROTEINS; NEURAL CONDUCTION; RANVIER'S NODES; REPRESSOR PROTEINS; SCHWANN CELLS; SCIATIC NERVE;

EID: 61449103563     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2168-08.2009     Document Type: Article

References (53)

1. Abdulkadir SA, Carbone JM, Naughton CK, Humphrey PA, Catalona WJ, Milbrandt J (2001) Frequent and early loss of the EGR1 corepressor NAB2 in human prostate carcinoma. Hum Pathol 32:935-939.
2. Bermingham JR Jr, Scherer SS, O'Connell S, Arroyo E, Kalla KA, Powell FL, Rosenfeld MG (1996) Tst-1/Oct-6/SCIP regulates a unique step in peripheral myelination and is required for normal respiration. Genes Dev 10:1751-1762.
3. Brown MC, Ironton R (1977) Motor neurone sprouting induced by prolonged tetrodotoxin block of nerve action potentials. Nature 265:459-461.
4. Burgess DL, Kohrman DC, Galt J, Plummer NW, Jones JM, Spear B, Meisler MH (1995) Mutation of a new sodium channel gene, Scn8a, in the mouse mutant 'motor endplate disease'. Nat Genet 10:461-465.
5. Charcot JM, Marie P (1886) Sur une forme particuliere d'atrophie musculaire progressive souvent familiale debutant par les pieds et les jambes et atteignant plus tard les mains. Rev Med 6:97-138.
6. Court FA, Brophy PJ, Ribchester RR (2008) Remodeling of motor nerve terminals in demyelinating axons of periaxin-null mice. Glia 56:471-479.
7. Decker L, Desmarquet-Trin-Dinh C, Taillebourg E, Ghislain J, Vallat JM, Charnay P (2006) Peripheral myelin maintenance is a dynamic process requiring constant Krox20 expression. J Neurosci 26:9771-9779.
8. Desmazières A, Decker L, Vallat JM, Charnay P, Gilardi-Hebenstreit P (2008) Disruption of Krox20-Nab interaction in the mouse leads to peripheral neuropathy with biphasic evolution. J Neurosci 28:5891-5900.
9. Devaux JJ, Scherer SS (2005) Altered ion channels in an animal model of Charcot-Marie-Tooth disease type IA. J Neurosci 25:1470-1480.
10. Duchen LW (1970) Hereditary motor end-plate disease in the mouse: light and electron microscopic studies. J Neurol Neurosurg Psychiatry 33:238-250.
11. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR (2000) Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
12. Hahn AF, Chang Y, Webster HD (1987) Development of myelinated nerve fibers in the sixth cranial nerve of the rat: a quantitative electron microscope study. J Comp Neurol 260:491-500.
13. Houlden H, Reilly MM (2006) Molecular genetics of autosomal-dominant demyelinating Charcot-Marie-Tooth disease. Neuromolecular Med 8:43-62.
14. Jessen KR, Mirsky R (2002) Signals that determine Schwann cell identity. J Anat 200:367-376.
15. Krajewski KM, Lewis RA, Fuerst DR, Turansky C, Hinderer SR, Garbern J, Kamholz J, Shy ME (2000) Neurological dysfunction and axonal degeneration in Charcot-Marie-Tooth disease type 1A. Brain 123:1516-1527.
16. Le N, Nagarajan R, Wang JY, Araki T, Schmidt RE, Milbrandt J (2005a) Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of Schwann cell differentiation and myelination. Proc Natl Acad Sci U S A 102:2596-2601.
17. Le N, Nagarajan R, Wang JY, Svaren J, LaPash C, Araki T, Schmidt RE, Milbrandt J (2005b) Nab proteins are essential for peripheral nervous system myelination. Nat Neurosci 8:932-940.
18. Leblanc SE, Srinivasan R, Ferri C, Mager GM, Gillian-Daniel AL, Wrabetz L, Svaren J (2005) Regulation of cholesterol/lipid biosynthetic genes by Egr2/Krox20 during peripheral nerve myelination. J Neurochem 93:737-748.
19. LeBlanc SE, Jang SW, Ward RM, Wrabetz L, Svaren J (2006) Direct regulation of myelin protein zero expression by the Egr2 transactivator. J Biol Chem 281:5453-5460.
20. Lewis RA, Sumner AJ, Shy ME (2000) Electrophysiological features of inherited demyelinating neuropathies: a reappraisal in the era of molecular diagnosis. Muscle Nerve 23:1472-1487.
21. Lupski JR (1997) Charcot-Marie-Tooth disease: a gene-dosage effect. Hosp Pract (Off Ed) 32:83-84, 89-91, 94-95 passim.
22. Maier M, Castagner F, Berger P, Suter U (2003) Distinct elements of the peripheral myelin protein 22 (PMP22) promoter regulate expression in Schwann cells and sensory neurons. Mol Cell Neurosci 24:803-817.
23. Mechta-Grigoriou F, Garel S, Charnay P (2000) Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain. Development 127:119-128.
24. Mirsky R, Jessen KR (1996) Schwann cell development, differentiation and myelination. Curr Opin Neurobiol 6:89-96.
25. Nagarajan R, Svaren J, Le N, Araki T, Watson M, Milbrandt J (2001) EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron 30:355-368.
26. Nicholson GA (2006) The dominantly inherited motor and sensory neuropathies: clinical and molecular advances. Muscle Nerve 33:589-597.
27. Pareyson D, Scaioli V, Laura M (2006) Clinical and electrophysiological aspects of Charcot-Marie-Tooth disease. Neuromolecular Med 8:3-22.
28. Pestronk A, Drachman DB (1978) Motor nerve sprouting and acetylcholine receptors. Science 199:1223-1225.
29. Poliak S, Peles E (2003) The local differentiation of myelinated axons at nodes of Ranvier. Nat Rev Neurosci 4:968-980.
30. Rasband MN, Trimmer JS (2001) Developmental clustering of ion channels at and near the node of Ranvier. Dev Biol 236:5-16.
31. Rasband MN, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, Shrager P (1998) Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18:36-47.
32. Russo MW, Matheny C, Milbrandt J (1993) Transcriptional activity of the zinc finger protein NGFI-A is influenced by its interaction with a cellular factor. Mol Cell Biol 13:6858-6865.
33. Russo MW, Sevetson BR, Milbrandt J (1995) Identification of NAB1, a repressor of NGFI-A and Krox20 mediated transcription. Proc Natl Acad Sci U S A 92:6873-6877.
34. Ryu EJ, Wang JY, Le N, Baloh RH, Gustin JA, Schmidt RE, Milbrandt J (2007) Misexpression of Pou3f1 results in peripheral nerve hypomyelination and axonal loss. J Neurosci 27:11552-11559.
35. Sancho S, Magyar JP, Aguzzi A, Suter U (1999) Distal axonopathy in peripheral nerves of PMP22-mutant mice. Brain 122:1563-1577.
36. Schneider-Maunoury S, Topilko P, Seitandou T, Levi G, Cohen-Tannoudji M, Pournin S, Babinet C, Charnay P (1993) Disruption of Krox-20 results in alteration of rhombomeres 3 and 5 in the developing hindbrain. Cell 75:1199-1214.
37. Sereda M, Griffiths I, Pühlhofer A, Stewart H, Rossner MJ, Zimmerman F, Magyar JP, Schneider A, Hund E, Meinck HM, Suter U, Nave KA (1996) A transgenic rat model of Charcot-Marie-Tooth disease. Neuron 16:1049-1060.
38. Sereda MW, Meyer zu Horste G, Suter U, Uzma N, Nave KA (2003) Therapeutic administration of progesterone antagonist in a model of Charcot-Marie-Tooth disease (CMT-1A). Nat Med 9:1533-1537.
39. Sevetson BR, Svaren J, Milbrandt J (2000) A novel activation function for NAB proteins in EGR-dependent transcription of the luteinizing hormone beta gene. J Biol Chem 275:9749-9757.
40. Shy ME (2004) Charcot-Marie-Tooth disease: an update. Curr Opin Neurol 17:579-585.
41. Suter U, Scherer SS (2003) Disease mechanisms in inherited neuropathies. Nat Rev Neurosci 4:714-726.
42. Svaren J, Meijer D (2008) The molecular machinery of myelin gene transcription in Schwann cells. Glia 56:1541-1551.
43. Svaren J, Sevetson BR, Apel ED, Zimonjic DB, Popescu NC, Milbrandt J (1996) NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 16:3545-3553.
44. Szigeti K, Wiszniewski W, Saifi GM, Sherman DL, Sule N, Adesina AM, Mancias P, Papasozomenos SCh, Miller G, Keppen L, Daentl D, Brophy PJ, Lupski JR (2007) Functional, histopathologic and natural history study of neuropathy associated with EGR2 mutations. Neurogenetics 8:257-262.
45. Tam SL, Gordon T (2003) Mechanisms controlling axonal sprouting at the neuromuscular junction. J Neurocytol 32:961-974.
46. Tooth H (1886) The peroneal type of progressive muscular atrophy. London: H. K. Lewis. Topilko P, Schneider-Maunoury S, Levi G, Baron-Van Evercooren A, Chennoufi AB, Seitanidou T, Babinet C, Charnay P (1994) Krox-20 controls myelination in the peripheral nervous system. Nature 371:796-799.
47. Ulzheimer JC, Peles E, Levinson SR, Martini R (2004) Altered expression of ion channel isoforms at the node of Ranvier in P0-deficient myelin mutants. Mol Cell Neurosci 25:83-94.
48. Verhoeven K, De Jonghe P, Van de Putte T, Nelis E, Zwijsen A, Verpoorten N, De Vriendt E, Jacobs A, Van Gerwen V, Francis A, Ceuterick C, Huyle-broeck D, Timmerman V (2003) Slowed conduction and thin myelination of peripheral nerves associated with mutant rho guanine-nucleotide exchange factor 10. Am J Hum Genet 73:926-932.
49. Warner LE, Mancias P, Butler IJ, McDonald CM, Keppen L, Koob KG, Lupski JR (1998) Mutations in the early growth response 2 (EGR2) gene are associated with hereditary myelinopathies. Nat Genet 18:382-384.
50. Warner LE, Svaren J, Milbrandt J, Lupski JR (1999) Functional consequences of mutations in the early growth response 2 gene (EGR2) correlate with severity of human myelinopathies. Hum Mol Genet 8:1245-1251.
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, 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.
53. Züchner S, Vance JM (2006) Mechanisms of disease: a molecular genetic update on hereditary axonal neuropathies. Nat Clin Pract Neurol 2:45-53.