Connexin pathology in acute multiple sclerosis, Baló’s disease and neuromyelitis optica

Clinical and Experimental Neuroimmunology

Volumn 4, Issue , 2013, Pages 36-44

  Masaki, Katsuhisa ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Aquaporin 4; Bal s disease; Connexin; Multiple sclerosis; Neuromyelitis optica

Indexed keywords

GAP JUNCTION PROTEIN; MYELIN;

ACUTE DISEASE; ASTROCYTE; AUTOPSY; CENTRAL NERVOUS SYSTEM; DISEASE EXACERBATION; HOMEOSTASIS; HUMAN; MULTIPLE SCLEROSIS; MYELINATION; MYELOOPTIC NEUROPATHY; NONHUMAN; OLIGODENDROGLIA; PELIZAEUS MERZBACHER DISEASE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

EID: 84979612568     PISSN: None     EISSN: 17591961     Source Type: Journal    
DOI: 10.1111/cen3.12062     Document Type: Review

References (66)

1. Bruzzone R, White TW, Paul DL. Connections with connexins: The molecular basis of direct intercellular signaling. Eur J Biochem. 1996; 238: 1–27.
2. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Güldenagel M, et al. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 2002; 383: 725–37.
3. Massa PT, Mugnaini E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: A freezefracture study. Neuroscience. 1982; 7: 523–38.
4. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA, et al. Connexin26 in adult rodent central nervous system: Demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. J Comp Neurol. 2001; 441: 302–23.
5. Rash JE, Yasumura T, Dudek FE, Nagy JI. Cell specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci. 2001; 21: 1983–2000.
6. Kamasawa N, Sik A, Morita M, Yasumura T, Davidson KG, Nagy JI, et al. Connexin-47 and connexin-32 in gap junctions of oligodendrocyte somata, myelin sheaths, paranodal loops and Schmidt-Lanterman incisures: Implications for ionic homeostasis and potassium siphoning. Neuroscience. 2005; 136: 65–86.
7. Orthmann-Murphy JL, Abrams CK, Scherer SS. Gap junctions couple astrocytes and oligodendrocytes. J Mol Neurosci. 2008; 35: 101–16.
8. Kleopa KA, Orthmann JL, Enriquez A, Paul DL, Scherer SS. Unique distribution of gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia. 2004; 47: 346–57.
9. Scherer SS, Deschênes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL. Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci. 1995; 15: 8281–94.
10. Altevogt BM, Kleopa KA, Postma FR, Scherer SS, Paul DL. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J Neurosci. 2002; 22: 6458–70.
11. Ahn M, Lee J, Gustafsson A, Enriquez A, Lancaster E, Sul JY, et al. Cx29 and Cx32, two connexins expressed by myelinating glia, do not interact and are functionally distinct. J Neurosci Res. 2008; 86: 992–1006.
12. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, et al. Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci. 2003; 23: 4549–59.
13. Nelles E, Butzler C, Jung D, Temme A, Gabriel HD, Dahl U, et al. Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32- deficient mice. Proc Natl Acad Sci USA. 1996; 93: 9565–70.
14. Menichella DM, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. Connexins are critical for normal myelination in the CNS. J Neurosci. 2003; 23: 5963–73.
15. Scherer SS. Molecular genetics of demyelination: New wrinkles on an old membrane. Neuron. 1997; 18: 13–6.
16. Bergoffen J, Scherer SS, Wang S, Scott MO, Bone LJ, Paul DL, et al. Connexin mutations in X-linked Charcot-Marie- Tooth disease. Science. 1993; 262: 2039–42.
17. Kleopa KA. The role of gap junctions in Charcot-Marie- Tooth Disease. J Neurosci. 2011; 31: 17753–60.
18. Isoardo G, Di Vito N, Nobile M, Benetton G, Fassio F. X-linked Charcot-Marie-Tooth disease and progressiverelapsing central demyelinating disease. Neurology. 2005; 65: 1672–3.
19. Parman Y, Ciftci F, Poyraz M, Halefoglu AM, Oge AE, Eraksoy M, et al. X-linked Charcot-Marie-Tooth disease and multiple sclerosis. J Neurol. 2007; 254: 953–5.
20. Srinivasan J, Leventer RJ, Kornberg AJ, Dahl HH, Ryan MM. Central nervous system signs in X-Linked Charcot- Marie-Tooth disease after hyperventilation. Pediatr Neurol. 2008; 38: 293–5.
21. Taylor RA, Simon EM, Marks HG, Scherer SS. The CNS phenotype of X-linked Charcot-Marie-Tooth disease: More than a peripheral problem. Neurology. 2003; 61: 1475–8.
22. Paulson HL, Garbern JY, Hoban TF, Krajewski KM, Lewis RA, Fischbeck KH, et al. Transient central nervous system white matter abnormality in X-linked Charcot-Marie- Tooth disease. Ann Neurol. 2002; 52: 429–34.
23. Schelhaas HJ, Van Engelen BG, Gabreëls-Festen AA, Hageman G, Vliegen JH, Van Der Knaap MS, et al. Transient cerebral white matter lesions in a patient with connexin 32 missense mutation. Neurology. 2002; 59: 2007–8.
24. Hanemann CO, Bergmann C, Senderek J, Zerres K, Sperfeld AD. Transient, recurrent, white matter lesions in X-linked Charcot-Marie-Tooth disease with novel connexin 32 mutation. Arch Neurol. 2003; 60: 605–9.
25. Fusco C, Frattini D, Pisani F, Spaggiari F, Ferlini A, Della Giustina E. Coexistent central and peripheral nervous system involvement in a Charcot-Marie-Tooth syndrome X-linked patient. J Child Neurol. 2010; 25: 759–63.
26. Uhlenberg B, Schuelke M, Rüschendorf F, Ruf N, Kaindl AM, Henneke M, et al. Mutations in the gene encoding gap junction protein alpha 12 (Connexin 46.6) cause Pelizaeus-Merzbacher-like disease. Am J Hum Genet. 2004; 75: 251–60.
27. Orthmann-Murphy JL, Salsano E, Abrams CK, Bizzi A, Uziel G, Freidin MM, et al. Hereditary spastic paraplegia is a novel phenotype for GJA12/GJC2 mutations. Brain. 2009; 132: 426–38.
28. Osaka H, Hamanoue H, Yamamoto R, Nezu A, Sasaki M, Saitsu H, et al. Disrupted SOX10 regulation on GJC2 transcription causes Pelizaeus-Merzbacher-Like disease. Ann Neurol. 2010; 68: 250–4.
29. Meyer E, Kurian MA, Morgan NV, McNeill A, Pasha S, Tee L, et al. Promoter mutation is a common variant in GJC2-associated Pelizaeus-Merzbacher-like disease. Mol Genet Metab. 2011; 104: 637–43.
30. Dermietzel R, Hertberg EL, Kessler JA, Spray DC. Gap junctions between cultured astrocytes: Immunocytochemical, molecular, and electrophysiological analysis. J Neurosci. 1991; 11: 1421–32.
31. Giaume C, Fromaget C, el Aoumari A, Cordier J, Glowinski J, Gros D. Gap junctions in cultured astrocytes: Single-channel currents and characterization of channelforming protein. Neuron. 1991; 6: 133–43.
32. Yamamoto T, Ochalski A, Hertzberg EL, Nagy JI. LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain. Brain Res. 1990; 508: 313–9.
33. Simard M, Arcuino G, Takano T, Liu QS, Nedergaard M. Signaling at the gliovascular interface. J Neurosci. 2003; 23: 9254–62.
34. Nagy JI, Patel D, Ochalski PA, Stelmack GL. Connexin30 in rodent, cat and human brain: Selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance. Neuroscience. 1999; 88: 447–68.
35. Lutz SE, Zhao Y, Gulinello M, Lee SC, Raine CS, Brosnan CF. Deletion of astrocyte connexins 43 and 30 leads to a dysmyelinating phenotype and hippocampal CA1 vacuolation. J Neurosci. 2009; 29: 7743–52.
36. Ezan P, André P, Cisternino S, Saubaméa B, Boulay AC, Doutremer S, et al. Deletion of astroglial connexins weakens the blood-brain barrier. J Cereb Blood Flow Metab. 2012; 32: 1457–67.
37. Paznekas WA, Boyadjiev SA, Shapiro RE, Daniels O, Wollnik B, Keegan CE, et al. Connexin 43 (GJA1) mutations cause the pleiotropic phenotype of oculodentodigital dysplasia. Am J Hum Genet. 2003; 72: 408–18.
38. Loddenkemper T, Grote K, Evers S, Oelerich M, Stögbauer F. Neurological manifestations of the oculodentodigital dysplasia syndrome. J Neurol. 2002; 249: 584–95.
39. Lamartine J, Munhoz Essenfelder G, Kibar Z, Lanneluc I, Callouet E, Laoudj D, et al. Mutations in GJB6 cause hidrotic ectodermal dysplasia. Nat Genet. 2000; 26: 142–4.
40. Suigura K, Teranishi M, Matsumoto Y, Akiyama M. Clouston syndrome with heterozygous GJB6 mutation p.Ala88Val and GJB2 variant p.Val27Ile revealing mild sensorineural hearing loss and photophobia. JAMA Dermatol. 2013 doi: 10.1001/jamadermatol.2013.4766.
41. Markoullis K, Sargiannidou I, Gardner C, Hadjisavvas A, Reynolds R, Kleopa KA. Disruption of oligodendrocyte gap junctions in experimental autoimmune encephalomyelitis. Glia. 2012; 60: 1053–66.
42. Brand-Schieber E, Werner P, Iacobas DA, Iacobas S, Beelitz M, Lowery SL, et al. Connexin43, the major gap junction protein of astrocytes, is down-regulated in inflamed white matter in an animal model of multiple sclerosis. J Neurosci Res. 2005; 80: 798–808.
43. Sharma R, Fischer MT, Bauer J, Felts PA, Smith KJ, Misu T, et al. Inflammation induced by innate immunity in the central nervous system leads to primary astrocyte dysfunction followed by demyelination. Acta Neuropathol. 2010; 120: 223–36.
44. Zhang F, Yao SY, Whetsell WO Jr, Sriram S. Astrogliopathy and oligodendrogliopathy are early events in CNS demyelination. Glia. 2013; 61: 1261–73.
45. Yao DL, Webster HD, Hudson LD, Brenner M, Liu DS, Escobar AI, et al. Concentric sclerosis (Baló): Morphometric and in situ hybridization study of lesions in six patients. Ann Neurol. 1994; 35: 18–30.
46. Matsuoka T, Suzuki SO, Iwaki T, Tabira T, Ordinario AT, Kira J. Aquaporin-4 astrocytopathy in Baló’s disease. Acta Neuropathol. 2010; 120: 651–60.
47. Masaki K, Suzuki SO, Matsushita T, Yonekawa T, Matsuoka T, Isobe N, et al. Extensive loss of connexins in Baló’s disease: Evidence for an auto-antibody-independent astrocytopathy via impaired astrocyteoligodendrocyte/ myelin interaction. Acta Neuropathol. 2012; 123: 887–900.
48. Lucchinetti C, Brück W, Parisi J, Scheithauer B, Rodriguez M, Lassmann H. Heterogeneity of multiple sclerosis lesions: Implications for the pathogenesis of demyelination. Ann Neurol. 2000; 47: 707–17.
49. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, et al. A serum autoantibody marker of neuromyelitis optica: Distinction from multiple sclerosis. Lancet. 2004; 364: 2106–12.
50. Lennon VA, Kryzer TJ, Pittock SJ, Verkman AS, Hinson SR. IgG marker of optic-spinal multiple sclerosis binds to the aquaporin-4 water channel. J Exp Med. 2005; 202: 473–7.
51. Misu T, Fujihara K, Kakita A, Konno H, Nakamura M, Watanabe S, et al. Loss of aquaporin 4 in lesions of neuromyelitis optica: Distinction from multiple sclerosis. Brain. 2007; 130: 1224–34.
52. Roemer SF, Parisi JE, Lennon VA, Benarroch EE, Lassmann H, Bruck W, et al. Pattern-specific loss of aquaporin- 4 immunoreactivity distinguishes neuromyelitis optica from multiple sclerosis. Brain. 2007; 130: 1194–205.
53. Matsuoka T, Suzuki SO, Suenaga T, Iwaki T, Kira J. Reappraisal of aquaporin-4 astrocytopathy in Asian neuromyelitis optica and multiple sclerosis patients. Brain Pathol. 2011; 11: 516–32.
54. Parratt JD, Prineas JW. Neuromyelitis optica: A demyelinating disease characterized by acute destruction and regeneration of perivascular astrocytes. Mult Scler. 2010; 16: 1156–72.
55. Kira J. Autoimmunity in neuromyelitis optica and opticospinal multiple sclerosis: Astrocytopathy as a common denominator in demyelinating disorders. J Neurol Sci. 2011; 311: 69–77.
56. Masaki K, Suzuki SO, Matsushita T, Matsuoka T, Imamura S, Yamasaki R, et al. Connexin 43 astrocytopathy linked to rapidly progressive multiple sclerosis and neuromyelitis optica. PLoS ONE. 2013; 8: E72919. doi:10.1371/journal.pone.0072919
57. Markoullis K, Sargiannidou I, Schiza N, Hadjisavvas A, Roncaroli F, Reynolds R, et al. Gap junction pathology in multiple sclerosis lesions and in normal appearing white matter. Acta Neuropathol. 2012; 123: 873–86.
58. Brück W, Popescu B, Lucchinetti CF, Markovic-Plese S, Gold R, Thal DR, et al. Neuromyelitis optica lesions may inform multiple sclerosis heterogeneity debate. Ann Neurol. 2012; 72: 385–94.
59. Misu T, Höftberger R, Fujihara K, Wimmer I, Takai Y, Nishiyama S, et al. Presence of six different lesion types suggests diverse mechanisms of tissue injury in neuromyelitis optica. Acta Neuropathol. 2013; 125: 815–27.
60. Orellana JA, Froger N, Ezan P, Jiang JX, Bennett MV, Naus CC, et al. ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels. J Neurochem. 2011; 118: 826–40.
61. Ye ZC, Wyeth MS, Baltan-Tekkok S, Ransom BR. Functional hemichannels in astrocytes: A novel mechanism of glutamate release. J Neurosci. 2003; 23: 3588–96.
62. Orthmann-Murphy JL, Enriquez AD, Abrams CK, Scherer SS. Loss-of-function connexin47 mutations cause Pelizaeus- Merzbacher-like disease. Mol Cell Neurosci. 2007; 34: 629–41.
63. Quist AP, Rhee SK, Lin H, Lal R. Physiological role of gapjunctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol. 2000; 148: 1063–74.
64. Rodriguez-Sinovas A, Cabestrero A, Lopez D, Torre I, Morente M, Abellán A, et al. The modulatory effects of connexin 43 on cell death/survival beyond cell coupling. Prog Biophys Mol Biol. 2007; 94: 219–32.
65. Shijie J, Takeuchi H, Yawata I, Harada Y, Sonobe Y, Doi Y, et al. Blockade of glutamate release from microglia attenuates experimental autoimmune encephalomyelitis in mice. Tohoku J Exp Med. 2009; 217: 87–92.
66. Endong L, Shijie J, Sonobe Y, Di M, Hua L, Kawanokuchi J, et al. The gap-junction inhibitor carbenoxolone suppresses the differentiation of Th17 cells through inhibition of IL-23 expression in antigen presenting cells. J Neuroimmunol. 2011; 240–241: 58–64.