Myelin loss and axonal ion channel adaptations associated with gray matter neuronal hyperexcitability

Journal of Neuroscience

Volumn 35, Issue 18, 2015, Pages 7272-7286

  Hamada, Mustafa S ^a   Kole, Maarten H P ^a,b  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Axon; Axon initial segment; Demyelination; Kv7.3; Nav1.6; Node of Ranvier

Indexed keywords

ION CHANNEL; MYELIN PROTEIN; CUPRIZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; AXON INITIAL SEGMENT; AXONAL ION CHANNEL ADAPTATION; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CONTROLLED STUDY; DEMYELINATION; GRAY MATTER NEURONAL HYPEREXCITABILITY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CONDUCTION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; QUANTITATIVE ASSAY; RANVIER NODE; SOMATOSENSORY STIMULATION; WHOLE CELL PATCH CLAMP; ANIMAL; AXON; C57BL MOUSE; CHEMICALLY INDUCED; DEMYELINATING DISEASE; DRUG EFFECTS; GRAY MATTER; MYELIN SHEATH; MYELINATED NERVE; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; AXONS; CUPRIZONE; DEMYELINATING DISEASES; GRAY MATTER; ION CHANNELS; MALE; MICE; MICE, INBRED C57BL; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURONS;

EID: 84929359355     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4747-14.2015     Document Type: Article

References (63)

1. Baker M, Bostock H (1992) Ectopic activity in demyelinated spinal root axons of the rat. J Physiol 451:539-552. CrossRef Medline
2. Battefeld A, Tran BT, Gavrilis J, Cooper EC, Kole MH (2014) Heteromeric Kv7.2/7.3 channels differentially regulate action potential initiation and conduction in neocortical myelinated axons. J Neurosci 34:3719-3732. CrossRef Medline
3. Beltramo R, D'Urso G, Dal Maschio M, Farisello P, Bovetti S, Clovis Y, Lassi G, Tucci V, De Pietri Tonelli D, Fellin T (2013) Layer-specific excitatory circuits differentially control recurrent network dynamics in the neocortex. Nat Neurosci 16:227-234. CrossRef Medline
4. Boggs JM (2006) Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 63:1945-1961. CrossRef Medline
5. Bostock H, Sears TA (1978) The internodal axon membrane: electrical excitability and continuous conduction in segmental demyelination. J Physiol 280:273-301. CrossRef Medline
6. Buffington SA, Rasband MN (2011) The axon initial segment in nervous system disease and injury. Eur J Neurosci 34:1609-1619. CrossRef Medline
7. Chiaravalloti ND, DeLuca J (2008) Cognitive impairment in multiple sclerosis. Lancet Neurol 7:1139-1151. CrossRef Medline
8. Clarner T, Diederichs F, Berger K, Denecke B, Gan L, van der Valk P, Beyer C, Amor S, Kipp M (2012) Myelin debris regulates inflammatory responses in an experimental demyelination animal model and multiple sclerosis lesions. Glia 60:1468-1480. CrossRef Medline
9. Coggan JS, Prescott SA, Bartol TM, Sejnowski TJ (2010) Imbalance of ionic conductances contributes to diverse symptoms of demyelination. Proc Natl Acad Sci U S A 107:20602-20609. CrossRef Medline
10. Craner MJ, Newcombe J, Black JA, Hartle C, Cuzner ML, Waxman SG (2004) Molecular changes in neurons in multiple sclerosis: altered axonal expression of Navi.2 and Navl.6 sodium channels and Na+/Ca2+ exchanger. Proc Natl Acad Sci U S A 101:8168-8173. CrossRef Medline
11. Crawford DK, Mangiardi M, Xia X, López-Valdés HE, Tiwari-Woodruff SK (2009) Functional recovery of callosal axons following demyelination: a critical window. Neuroscience 164:1407-1421. CrossRef Medline
12. Dupree JL, Mason JL, Marcus JR, Stull M, Levinson R, Matsushima GK, Popko B (2004) Oligodendrocytes assist in the maintenance of sodium channel clusters independent of the myelin sheath. Neuron Glia Biol 1:179-192. CrossRef Medline
13. Dutta R, Chomyk AM, Chang A, Ribaudo MV, Deckard SA, Doud MK, Edberg DD, Bai B, Li M, Baranzini SE, Fox RJ, Staugaitis SM, Macklin WB, Trapp BD (2013) Hippocampal demyelination and memory dysfunction are associated with increased levels of the neuronal micro RNA miR-124 and reduced AMPA receptors. Ann Neurol 73:637-645. CrossRef Medline
14. Dzhashiashvili Y, Zhang Y, Galinska J, Lam I, Grumet M, Salzer JL (2007) Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol 177:857-870. CrossRef Medline
15. Felts PA, Kapoor R, Smith KJ (1995) A mechanism for ectopic firing in central demyelinated axons. Brain 118:1225-1231. CrossRef Medline
16. Felts PA, Baker TA, Smith KJ (1997) Conduction in segmentally demyelinated mammalian central axons. J Neurosci 17:7267-7277. Medline
17. Fisniku LK, Chard DT, Jackson JS, Anderson VM, Altmann DR, Miszkiel KA, Thompson AJ, Miller DH (2008) Gray matter atrophy is related to longterm disability in multiple sclerosis. Ann Neurol 64:247-254. CrossRef Medline
18. Foster RE, Whalen CC, Waxman SG (1980) Reorganization of the axon membrane in demyelinated peripheral nerve fibers: morphological evidence. Science 210:661-663. CrossRef Medline
19. Galiano MR, Jha S, Ho TS, Zhang C, Ogawa Y, Chang KJ, Stankewich MC, Mohler PJ, Rasband MN (2012) A distal axonal cytoskeleton forms an intra-axonal boundary that controls axon initial segment assembly. Cell 149:1125-1139. CrossRef Medline
20. Geurts JJ, Barkhof F (2008) Grey matter pathology in multiple sclerosis. Lancet Neurol 7:841-851. CrossRef Medline
21. Geurts JJ, Pouwels PJ, Uitdehaag BM, Polman CH, Barkhof F, Castelijns JA (2005) Intracortical lesions in multiple sclerosis: improved detection with 3D double inversion-recoveryMR imaging. Radiology 236:254-260. CrossRef Medline
22. Grubb MS, Burrone J (2010) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465:1070-1074. CrossRef Medline
23. Hallermann S, de Kock CP, Stuart GJ, Kole MH (2012) State and location dependence of action potential metabolic cost in cortical pyramidal neurons. Nat Neurosci 15:1007-1014. CrossRef Medline
24. Hattox AM, Nelson SB (2007) Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol 98:3330-3340. CrossRef Medline
25. Hill AS, Nishino A, Nakajo K, Zhang G, Fineman JR, Selzer ME, Okamura Y, Cooper EC (2008) Ion channel clustering at the axon initial segment and node of Ranvier evolved sequentially in early chordates. PLoS Genet 4:e 1000317. CrossRef Medline
26. Hines ML, Carnevale NT (2001) NEURON: a tool for neuroscientists. Neuroscientist 7:123-135. CrossRef Medline
27. Hinman JD, Rasband MN, Carmichael ST (2013) Remodeling of the axon initial segment after focal cortical and white matter stroke. Stroke 44:182-189. CrossRef Medline
28. Kapoor R, Smith KJ, Felts PA, Davies M (1993) Internodal potassium currents can generate ectopic impulses in mammalian myelinated axons. Brain Res 611:165-169. CrossRef Medline
29. Kapoor R, Li YG, Smith KJ (1997) Slow sodium-dependent potential oscillations contribute to ectopic firing in mammalian demyelinated axons. Brain 120:647-652. CrossRef Medline
30. Kapoor R, Furby J, Hayton T, Smith KJ, Altmann DR, Brenner R, Chataway J, Hughes RA, Miller DH (2010) Lamotrigine for neuroprotection in secondary progressive multiple sclerosis: a randomised, double-blind, placebo-controlled, parallel-group trial. Lancet Neurol 9:681-688. CrossRef Medline
31. Kipp M, Clarner T, Dang J, Copray S, Beyer C (2009) The cuprizone animal model: new insights into an old story. Acta Neuropathol 118:723-736. CrossRef Medline
32. Kole MH (2011) First node of Ranvier facilitates high-frequency burst encoding. Neuron 71:671-682. CrossRef Medline
33. Kole MH, Stuart GJ (2012) Signal processing in the axon initial segment. Neuron 73:235-247. CrossRef Medline
34. Kole MH, Hallermann S, Stuart GJ (2006) Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26:1677-1687. CrossRef Medline
35. Kole MH, Ilschner SU, KampaBM, Williams SR, Ruben PC, Stuart GJ (2008) Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11:178-186. CrossRef Medline
36. Kuba H, Ishii TM, Ohmori H (2006) Axonal site of spike initiation enhances auditory coincidence detection. Nature 444:1069-1072. CrossRef Medline
37. Kuba H, Oichi Y, Ohmori H (2010) Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 465:1075-1078. CrossRef Medline
38. Le Bon-Jego M, Yuste R (2007) Persistently active, pacemaker-like neurons in neocortex. Front Neurosci 1:123-129. CrossRef Medline
39. Lindner M, Heine S, Haastert K, Garde N, Fokuhl J, Linsmeier F, Grothe C, Baumgartner W, Stangel M (2008) Sequential myelin protein expression during remyelination reveals fast and efficient repair after central nervous system demyelination. Neuropathol Appl Neurobiol 34:105-114. Medline
40. Mathis C, Denisenko-Nehrbass N, Girault JA, Borrelli E (2001) Essential role of oligodendrocytes in the formation and maintenance of central nervous system nodal regions. Development 128:4881-4890. Medline
41. Ng K, Howells J, Pollard JD, Burke D (2008) Up-regulation of slow K(+) channels in peripheral motor axons: a transcriptional channelopathy in multiple sclerosis. Brain 131:3062-3071. CrossRef Medline
42. Oberlaender M, Boudewijns ZS, Kleele T, Mansvelder HD, Sakmann B, de Kock CP (2011) Three-dimensional axon morphologies of individual layer 5 neurons indicate cell type-specific intracortical pathways for whisker motion and touch. Proc Natl Acad Sci USA 108:4188-4193. CrossRef Medline
43. Ogawa Y, Rasband MN (2008) The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol 18:307-313. CrossRef Medline
44. Palmer LM, Clark BA, Gründemann J, Roth A, Stuart GJ, Häusser M (2010) Initiation of simple and complex spikes in cerebellar Purkinje cells. J Physiol 588:1709-1717. CrossRef Medline
45. Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, Bennett V, Scherer SS, Cooper EC (2006) A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26:2599-2613. CrossRef Medline
46. Rasband MN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552-562. CrossRef Medline
47. Rash JE (2010) Molecular disruptions of the panglial syncytium block potassium siphoning and axonal saltatory conduction: pertinence to neuro-myelitis optica and other demyelinating diseases of the central nervous system. Neuroscience 168:982-1008. CrossRef Medline
48. Rasminsky M (1978) Ectopic generation of impulses and cross-talk in spinal nerve roots of "dystrophic" mice. Ann Neurol 3:351-357. CrossRef Medline
49. Roza C, Lopez-Garcia JA (2008) Retigabine, the specific KCNQ channel opener, blocks ectopic discharges in axotomized sensory fibres. Pain 138: 537-545. CrossRef Medline
50. Roza C, Castillejo S, Lopez-García JA (2011) Accumulation of Kv7.2 channels in putative ectopic transduction zones of mice nerve-end neuromas. Mol Pain 7:58. CrossRef Medline
51. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027-1034. CrossRef Medline
52. Schmidt-Hieber C, Bischofberger J (2010) Fast sodium channel gating supports localized and efficient axonal action potential initiation. J Neurosci 30:10233-10242. CrossRef Medline
53. Shrager P, Rubinstein CT (1990) Optical measurement of conduction in single demyelinated axons. J Gen Physiol 95:867-889. CrossRef Medline
54. Stafstrom CE, Grippon S, Kirkpatrick P (2011) Ezogabine (retigabine). Nat Rev Drug Discov 10:729-730. CrossRef Medline
55. Straub H, Köhling R, Höhling J, Rundfeldt C, Tuxhom I, Ebner A, Wolf P, Pannek H, Speckmann E (2001) Effects of retigabine on rhythmic synchronous activity of human neocortical slices. Epilepsy Res 44:155-165. Medline
56. Stys PK, You H, Zamponi GW (2012) Copper-dependent regulation of NMDA receptors by cellular prion protein: implications for neurodegen-erative disorders. J Physiol 590:1357-1368. CrossRef Medline
57. Susuki K, Chang KJ, Zollinger DR, Liu Y, Ogawa Y, Eshed-Eisenbach Y, Dours-Zimmermann MT, Oses-Prieto JA, Burlingame AL, Seidenbecher Cl, Zimmermann DR, Oohashi T, Peles E, Rasband MN (2013) Three mechanisms assemble central nervous system nodes of Ranvier. Neuron 78:469-482. CrossRef Medline
58. Sutor B, Schmolke C, Teubner B, Schirmer C, Willecke K (2000) Myelination defects and neuronal hyperexcitability in the neocortex of connexin 32-deficient mice. Cereb Cortex 10:684-697. CrossRef Medline
59. Tian C, Wang K, Ke W, Guo H, Shu Y (2014) Molecular identity of axonal sodium channels in human cortical pyramidal cells. Front Cell Neurosci 8:297. CrossRef Medline
60. Tomassy GS, Berger DR, Chen HH, Kasthuri N, Hayworth KJ, Vercelli A, Seung HS, Lichtman JW, Arlotta P (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319-324. CrossRef Medline
61. Wang HS, Brown BS, McKinnon D, Cohen IS (2000) Molecular basis for differential sensitivity of KCNQ and I(Ks) channels to the cognitive enhancer XE991. Mol Pharmacol 57:1218-1223. Medline
62. Waxman SG (2008) Mechanisms of disease: sodium channels and neuroprotection in multiple sclerosis-current status. Nat Clin Pract Neurol 4:159-169. CrossRef Medline
63. Waxman SG, Craner MJ, Black JA (2004) Na+ channel expression along axons in multiple sclerosis and its models. Trends Pharmacol Sci 25:584-591. CrossRef Medline