Functional heterotypic interactions between astrocyte and oligodendrocyte connexins

GLIA

Volumn 59, Issue 1, 2011, Pages 26-34

  Magnotti, Laura M ^a   Goodenough, Daniel A ^a   Paul, David L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Connexin; Gap junction; Glia; Myelin

Indexed keywords

CONNEXIN 26; CONNEXIN 30; CONNEXIN 32; CONNEXIN 43; CONNEXIN 47;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COMMUNICATION; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; ASTROCYTES; CELL COMMUNICATION; CELLS, CULTURED; CONNEXINS; GAP JUNCTIONS; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; OLIGODENDROGLIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 78349271626     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.21073     Document Type: Article

References (50)

1. Ahn M, Lee J, Gustafsson A, Enriquez A, Lancaster E, Sul JY, Haydon PG, Paul DL, Huang Y, Abrams CK, Scherer SS. 2008. Cx29 and Cx32, two connexins expressed by myelinating glia, do not interact and are functionally distinct. J Neurosci Res 86: 992-1006.
2. Altevogt BM, Kleopa KA, Postma FR, Scherer SS, Paul DL. 2002. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J Neurosci 22: 6458-6470.
3. Altevogt BM, Paul DL. 2004. Four classes of intercellular channels between glial cells in the CNS. J Neurosci 24: 4313-4323.
4. Beltramello M, Bicego M, Piazza V, Ciubotaru CD, Mammano F, D'Andrea P. 2003. Permeability and gating properties of human connexins 26 and 30 expressed in HeLa cells. Biochem Biophys Res Commun 305: 1024-1033.
5. Elfgang C, Eckert R, Lichtenberg-Fraté H, Butterweck A, Traub O, Klein RA, Hülser DF, Willecke K. 1995. Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol 129: 805-817.
6. Filippov MA, Hormuzdi SG, Fuchs EC, Monyer H. 2003. A reporter allele for investigating connexin 26 gene expression in the mouse brain. Eur J Neurosci 18: 3183-3192.
7. Giaume C, Fromaget C, El Aoumari A, Cordier J, Glowinski J, Gros D. 1991. Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein. Neuron 6: 133-143.
8. Hanemann CO, Bergmann C, Senderek J, Zerres K, Sperfeld AD. 2003. Transient, recurrent, white matter lesions in X-linked Charcot-Marie-Tooth disease with novel connexin 32 mutation. Arch Neurol 60: 605-609.
9. Hollinshead M, Sanderson J, Vaux DJ. 1997. Anti-biotin antibodies offer superior organelle-specific labeling of mitochondria over avidin or streptavidin. J Histochem Cytochem 45: 1053-1057.
10. Hunter AW, Barker RJ, Zhu C, Gourdie RG. 2005. ZO-1 alters Connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell 16: 5686-5698.
11. Kamasawa N, Sik A, Morita M, Yasumura T, Davidson KG, Nagy JI, Rash JE. 2005. 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 136: 65-86.
12. Kettenmann H, Ransom BR. 1988. Electrical coupling between astrocytes and between oligodendrocytes studied in mammalian cell cultures. Glia 1: 64-73.
13. Kleopa KA, Orthmann JL, Enriquez A, Paul DL, Scherer SS. 2004. Unique distributions of the gap junction proteins connexin29, connexin32, and connexin47 in oligodendrocytes. Glia 47: 346-357.
14. Kleopa KA, Yum SW, Scherer SS. 2002. Cellular mechanisms of connexin32 mutations associated with CNS manifestations. J Neurosci Res 68: 522-534.
15. Kunzelmann P, Schroder W, Traub O, Steinhauser C, Dermietzel R, Willecke K. 1999. Late onset and increasing expression of the gap junction protein connexin30 in adult murine brain and long-term cultured astrocytes. Glia 25: 111-119.
16. Li X, Ionescu AV, Lynn BD, Lu S, Kamasawa N, Morita M, Davidson KG, Yasumura T, Rash JE, Nagy JI. 2004. Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and cx47 association with zonula occludens-1 (ZO-1) in mouse brain. Neuroscience 126: 611-630.
17. Li X, Kamasawa N, Ciolofan C, Olson CO, Lu S, Davidson KG, Yasumura T, Shigemoto R, Rash JE, Nagy JI. 2008. Connexin45-containing neuronal gap junctions in rodent retina also contain connexin36 in both apposing hemiplaques, forming bihomotypic gap junctions, with scaffolding contributed by zonula occludens-1. J Neurosci 28: 9769-9789.
18. Liao Y, Day KH, Damon DN, Duling BR. 2001. Endothelial cell-specific knockout of connexin 43 causes hypotension and bradycardia in mice. Proc Natl Acad Sci (USA) 98: 9989-9994.
19. Loddenkemper T, Grote K, Evers S, Oelerich M, Stogbauer F. 2002. Neurological manifestations of the oculodentodigital dysplasia syndrome. J Neurol 249: 584-595.
20. Maglione M, Tress O, Haas B, Karram K, Trotter J, Willecke K, Kettenmann H. 2010. Oligodendrocytes in mouse corpus callosum are coupled via gap junction channels formed by connexin47 and connexin32. Glia 58: 1104-1117.
21. Manthey D, Banach K, Desplantez T, Lee CG, Kozak CA, Traub O, Weingart R, Willecke K. 2001. Intracellular domains of mouse connexin26 and -30 affect diffusional and electrical properties of gap junction channels. J Membr Biol 181: 137-148.
22. Massa PT, Mugnaini E. 1982. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes: a freeze-fracture study. Neuroscience 7: 523-538.
23. Masters JR. 2002. HeLa cells 50 years on: The good, the bad and the ugly. Nat Rev Cancer 2: 315-319.
24. Menichella DM, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. 2003. Connexins are critical for normal myelination in the CNS. J Neurosci 23: 5963-5973.
25. Menichella DM, Majdan M, Awatramani R, Goodenough DA, Sirkowski E, Scherer SS, Paul DL. 2006. Genetic and physiological evidence that oligodendrocyte gap junctions contribute to spatial buffering of potassium released during neuronal activity. J Neurosci 26: 10984-10991.
26. Mercier F, Hatton GI. 2001. Connexin 26 and basic fibroblast growth factor are expressed primarily in the subpial and subependymal layers in adult brain parenchyma: Roles in stem cell proliferation and morphological plasticity? J Comp Neurol 431: 88-104.
27. Nagy JI, Ionescu AV, Lynn BD, Rash JE. 2003a. Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. J Comp Neurol 464: 356-370.
28. Nagy JI, Ionescu AV, Lynn BD, Rash JE. 2003b. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47: Implications from normal and connexin32 knockout mice. Glia 44: 205-218.
29. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA, Yasumura T, Rash JE. 2001. Connexin26 in adult rodent central nervous system: Demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. J Comp Neurol 441: 302-323.
30. Odermatt B, Wellershaus K, Wallraff A, Seifert G, Degen J, Euwens C, Fuss B, Bussow H, Schilling K, Steinhauser C, Willecke K. 2003. 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 23: 4549-4559.
31. Orkand RK, Nicholls JG, Kuffler SW. 1966. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol 29: 788-806.
32. Orthmann-Murphy JL, Freidin M, Fischer E, Scherer SS, Abrams CK. 2007. Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins. J Neurosci 27: 13949-13957.
33. Paul DL. 1986. Molecular cloning of cDNA for rat liver gap junction protein. J Cell Biol 103: 123-134.
34. Paulson HL, Garbern JY, Hoban TF, Krajewski KM, Lewis RA, Fischbeck KH, Grossman RI, Lenkinski R, Kamholz JA, Shy ME. 2002. Transient central nervous system white matter abnormality in X-linked Charcot-Marie-Tooth disease. Ann Neurol 52: 429-434.
35. Rash JE, Yasumura T, Davidson KG, Furman CS, Dudek FE, Nagy JI. 2001. Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord. Cell Adhes Commun 8: 315-320.
36. Reaume AG, De Sousa PA, Kulkarni S, Langille BL, Zhu D, Davies TC, Juneja SC, Kidder GM, Rossant J. 1995. Cardiac malformation in neonatal mice lacking connexin43. Science 267: 1831-1834.
37. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C. 2008. Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322: 1551-1555.
38. Sargiannidou I, Vavlitou N, Aristodemou S, Hadjisavvas A, Kyriacou K, Scherer SS, Kleopa KA. 2009. Connexin32 mutations cause loss of function in Schwann cells and oligodendrocytes leading to PNS, CNS myelination defects. J Neurosci 29: 4736-4749.
39. Scherer SS, Deschenes SM, Xu YT, Grinspan JB, Fischbeck KH, Paul DL. 1995. Connexin32 is a myelin-related protein in the PNS, CNS. J Neurosci 15: 8281-8294.
40. Scherer SS, Xu YT, Nelles E, Fischbeck K, Willecke K, Bone LJ. 1998. Connexin32-null mice develop demyelinating peripheral neuropathy. Glia 24: 8-20.
41. Takashima H, Nakagawa M, Umehara F, Hirata K, Suehara M, Mayumi H, Yoshishige K, Matsuyama W, Saito M, Jonosono M, Arimura K, Osame M. 2003. Gap junction protein beta 1 (GJB1) mutations and central nervous system symptoms in X-linked Charcot-Marie-Tooth disease. Acta Neurol Scand 107: 31-37.
42. Tang W, Zhang Y, Chang Q, Ahmad S, Dahlke I, Yi H, Chen P, Paul DL, Lin X. 2006. Connexin29 is highly expressed in cochlear Schwann cells, and it is required for the normal development and function of the auditory nerve of mice. J Neurosci 26: 1991-1999.
43. Taylor RA, Simon EM, Marks HG, Scherer SS. 2003. The CNS phenotype of X-linked Charcot-Marie-Tooth disease: more than a peripheral problem. Neurology 61: 1475-1478.
44. Teubner B, Degen J, Sohl G, Guldenagel M, Bukauskas FF, Trexler EB, Verselis VK, De Zeeuw CI, Lee CG, Kozak CA, Petrasch-Parwez E, Dermietzel R, Willecke K. 2000. Functional expression of the murine Connexin 36 gene coding for a neuron-specific gap junctional protein. J Membr Biol 176: 249-262.
45. Theis M, Speidel D, Willecke K. 2004. Astrocyte cultures from conditional connexin43-deficient mice. Glia 46: 130-141.
46. Uhlenberg B, Schuelke M, Ruschendorf F, Ruf N, Kaindl AM, Henneke M, Thiele H, Stoltenburg-Didinger G, Aksu F, Topaloglu H, Nurnberg P, Hubner C, Weschke B, Gartner J. 2004. Mutations in the gene encoding gap junction protein alpha 12 (connexin 46.6) cause Pelizaeus-Merzbacher-like disease. Am J Hum Genet 75: 251-260.
47. Yang JJ, Huang SH, Chou KH, Liao PJ, Su CC, Li SY. 2007. Identification of mutations in members of the connexin gene family as a cause of nonsyndromic deafness in Taiwan. Audiol Neurootol 12: 198-208.
48. Zhang JT, Nicholson BJ. 1989. Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J Cell Biol 109: 3391-3401.
49. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A. 2001. hGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31: 85-94.
50. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. 1998. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 72: 9873-9880.