BAAV mediated GJB2 gene transfer restores gap junction coupling in cochlear organotypic cultures from deaf Cx26Sox10Cre mice

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Crispino, Giulia ^a,b   Di Pasquale, Giovanni ^c   Scimemi, Pietro ^b   Rodriguez, Laura ^a,b   Ramirez, Fabian Galindo ^a   de Siati, Romolo Daniele ^b   Santarelli, Rosa Maria ^b   Arslan, Edoardo ^b   Bortolozzi, Mario ^a,b,d   Chiorini, John A ^c   Mammano, Fabio ^a,b,d  

^a Istituto Veneto di Medicina Molecolare   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CONNEXIN 26; CONNEXIN 30; CRE RECOMBINASE; GAP JUNCTION PROTEIN; HYBRID PROTEIN; INTEGRASE; SOX10 PROTEIN, MOUSE; TRANSCRIPTION FACTOR SOX;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCHLEA POTENTIAL; CONTROLLED STUDY; CORTI ORGAN; CROSS BREEDING; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FUNCTIONAL ASSESSMENT; GAP JUNCTION; GENE; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE LOCUS; GENETIC ASSOCIATION; GJB2 GENE; HAIR CELL; HEARING IMPAIRMENT; IN VIVO STUDY; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; TRANSGENIC MOUSE; VIRAL GENE DELIVERY SYSTEM; VIRUS RECOMBINANT; ANIMAL; CATTLE; CELL JUNCTION; COCHLEA; ELECTROPHYSIOLOGY; GENE THERAPY; GENETIC TRANSDUCTION; GENETICS; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; PERMEABILITY; TIME;

ADENO-ASSOCIATED VIRUS; BOVINE ADENO-ASSOCIATED VIRUS; MUS;

ANIMALS; CATTLE; COCHLEA; CONNEXINS; DEAFNESS; DEPENDOVIRUS; ELECTROPHYSIOLOGICAL PHENOMENA; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GAP JUNCTIONS; GENE THERAPY; HAIR CELLS, AUDITORY; INTEGRASES; MICE; ORGAN CULTURE TECHNIQUES; ORGAN OF CORTI; PERMEABILITY; RECOMBINANT FUSION PROTEINS; SOXE TRANSCRIPTION FACTORS; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 80051850929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023279     Document Type: Article

References (50)

1. Goodenough DA, Paul DL, (2009) Gap junctions. Cold Spring Harb Perspect Biol 1: a002576.
2. Kelsell DP, Dunlop J, Stevens HP, Lench NJ, Liang JN, et al. (1997) Connexin 26 mutations in hereditary non-syndromic sensorineural deafness. Nature 387: 80-83.
3. Denoyelle F, Lina-Granade G, Plauchu H, Bruzzone R, Chaib H, et al. (1998) Connexin 26 gene linked to a dominant deafness. Nature 393: 319-320.
4. Hilgert N, Smith RJ, Van Camp G, (2009) Function and expression pattern of nonsyndromic deafness genes. Curr Mol Med 9: 546-564.
5. Gasparini P, Estivill X, Volpini V, Totaro A, Castellvi-Bel S, et al. (1997) Linkage of DFNB1 to non-syndromic neurosensory autosomal-recessive deafness in Mediterranean families. Eur J Hum Genet 5: 83-88.
6. Grifa A, Wagner CA, D'Ambrosio L, Melchionda S, Bernardi F, et al. (1999) Mutations in GJB6 cause nonsyndromic autosomal dominant deafness at DFNA3 locus. Nat Genet 23: 16-18.
7. Maeda S, Nakagawa S, Suga M, Yamashita E, Oshima A, et al. (2009) Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature 458: 597-602.
8. Martinez AD, Acuna R, Figueroa V, Maripillan J, Nicholson B, (2009) Gap-junction channels dysfunction in deafness and hearing loss. Antioxid Redox Signal 11: 309-322.
9. Nickel R, Forge A, (2008) Gap junctions and connexins in the inner ear: their roles in homeostasis and deafness. Curr Opin Otolaryngol Head Neck Surg 16: 452-457.
10. Kikuchi T, Kimura RS, Paul DL, Takasaka T, Adams JC, (2000) Gap junction systems in the mammalian cochlea. Brain Res Brain Res Rev 32: 163-166.
11. Hibino H, Kurachi Y, (2006) Molecular and physiological bases of the K+ circulation in the mammalian inner ear. Physiology (Bethesda) 21: 336-345.
12. Sadanaga M, Morimitsu T, (1995) Development of endocochlear potential and its negative component in mouse cochlea. Hear Res 89: 155-161.
13. Leibovici M, Safieddine S, Petit C, (2008) Mouse models for human hereditary deafness. Curr Top Dev Biol 84: 385-429.
14. Cohen-Salmon M, Ott T, Michel V, Hardelin JP, Perfettini I, et al. (2002) Targeted ablation of connexin26 in the inner ear epithelial gap junction network causes hearing impairment and cell death. Curr Biol 12: 1106-1111.
15. Teubner B, Michel V, Pesch J, Lautermann J, Cohen-Salmon M, et al. (2003) Connexin30 (Gjb6)-deficiency causes severe hearing impairment and lack of endocochlear potential. Hum Mol Genet 12: 13-21.
16. Cohen-Salmon M, Regnault B, Cayet N, Caille D, Demuth K, et al. (2007) Connexin30 deficiency causes instrastrial fluid-blood barrier disruption within the cochlear stria vascularis. Proc Natl Acad Sci U S A 104: 6229-6234.
17. Chang Q, Tang W, Ahmad S, Zhou B, Lin X, (2008) Gap junction mediated intercellular metabolite transfer in the cochlea is compromised in connexin30 null mice. PLoS One 3: e4088.
18. Sun Y, Tang W, Chang Q, Wang Y, Kong W, et al. (2009) Connexin30 null and conditional connexin26 null mice display distinct pattern and time course of cellular degeneration in the cochlea. J Comp Neurol 516: 569-579.
19. Anselmi F, Hernandez VH, Crispino G, Seydel A, Ortolano S, et al. (2008) ATP release through connexin hemichannels and gap junction transfer of second messengers propagate Ca2+ signals across the inner ear. Proc Natl Acad Sci U S A 105: 18770-18775.
20. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, et al. (2005) Neural crest origins of the neck and shoulder. Nature 436: 347-355.
21. Bry C, Maass K, Miyoshi K, Willecke K, Ott T, et al. (2004) Loss of connexin 26 in mammary epithelium during early but not during late pregnancy results in unscheduled apoptosis and impaired development. Dev Biol 267: 418-429.
22. Watanabe K, Takeda K, Katori Y, Ikeda K, Oshima T, et al. (2000) Expression of the Sox10 gene during mouse inner ear development. Brain Res Mol Brain Res 84: 141-145.
23. Shibata SB, Di Pasquale G, Cortez SR, Chiorini JA, Raphael Y, (2009) Gene transfer using bovine adeno-associated virus in the guinea pig cochlea. Gene Ther 16: 990-997.
24. Lautermann J, Frank HG, Jahnke K, Traub O, Winterhager E, (1999) Developmental expression patterns of connexin26 and -30 in the rat cochlea. Dev Genet 25: 306-311.
25. Ortolano S, Di Pasquale G, Crispino G, Anselmi F, Mammano F, et al. (2008) Coordinated control of connexin 26 and connexin 30 at the regulatory and functional level in the inner ear. Proc Natl Acad Sci U S A 105: 18776-18781.
26. Schutz M, Scimemi P, Majumder P, De Siati RD, Crispino G, et al. (2010) The human deafness-associated connexin 30 T5M mutation causes mild hearing loss and reduces biochemical coupling among cochlear non-sensory cells in knock-in mice. Hum Mol Genet 19: 4759-4773.
27. Wade MH, Trosko JE, Schindler M, (1986) A fluorescence photobleaching assay of gap junction-mediated communication between human cells. Science 232: 525-528.
28. Eggston AA, Wolff D, (1947) Embryology of the ear. Histopathology of the ear, nose, and throat Baltimore Williams and Wilkins Co pp. 37-64.
29. Bermingham-McDonogh O, Oesterle EC, Stone JS, Hume CR, Huynh HM, et al. (2006) Expression of Prox1 during mouse cochlear development. J Comp Neurol 496: 172-186.
30. Rabut G, Ellenberg J, (2005) Photobleaching techniques to study mobility and molecular dynamics of proteins in live cells: FRAP, iFRAP, and FLIP. In: Goldman RD, Spector DL, editors. Live Cell Imaging New York Cold Spring Harbor Laboratory pp. 101-126.
31. Majumder P, Crispino G, Rodriguez L, Ciubotaru CD, Anselmi F, et al. (2010) ATP-mediated cell-cell signaling in the organ of Corti: the role of connexin channels. Purinergic Signalling 6: 167-187.
32. Rozental R, Miduturu S, Spray DC, (2001) How to close a gap junction channel. In: Bruzzone R, Giaume C, editors. Connexin Methods and Protocols Totowa, NJ Humana Press pp. 447-476.
33. Sheffield AM, Gubbels SP, Hildebrand MS, Newton SS, Chiorini JA, et al. (2011) Viral vector tropism for supporting cells in the developing murine cochlea. Hear Res.
34. Di Pasquale G, Rzadzinska A, Schneider ME, Bossis I, Chiorini JA, et al. (2005) A novel bovine virus efficiently transduces inner ear neuroepithelial cells. Mol Ther 11: 849-855.
35. Di Pasquale G, Kaludov N, Agbandje-McKenna M, Chiorini JA, (2010) BAAV transcytosis requires an interaction with beta-1-4 linked- glucosamine and gp96. PLoS One 5: e9336.
36. Schmidt M, Chiorini JA, (2006) Gangliosides are essential for bovine adeno-associated virus entry. J Virol 80: 5516-5522.
37. Maguchi S, Gasa S, Matsushima J, Saga Y, Kawano M, et al. (1991) Glycolipids in rat cochlea. Auris Nasus Larynx 18: 1-8.
38. Santi PA, Mancini P, Barnes C, (1994) Identification and localization of the GM1 ganglioside in the cochlea using thin-layer chromatography and cholera toxin. J Histochem Cytochem 42: 705-716.
39. Yoshikawa M, Go S, Takasaki K, Kakazu Y, Ohashi M, et al. (2009) Mice lacking ganglioside GM3 synthase exhibit complete hearing loss due to selective degeneration of the organ of Corti. Proc Natl Acad Sci U S A 106: 9483-9488.
40. Levin M, (2007) Gap junctional communication in morphogenesis. Prog Biophys Mol Biol 94: 186-206.
41. Harris AL, (2007) Connexin channel permeability to cytoplasmic molecules. Prog Biophys Mol Biol 94: 120-143.
42. Beltramello M, Piazza V, Bukauskas FF, Pozzan T, Mammano F, (2005) Impaired permeability to Ins(1,4,5)P3 in a mutant connexin underlies recessive hereditary deafness. Nat Cell Biol 7: 63-69.
43. Zhang Y, Tang W, Ahmad S, Sipp JA, Chen P, et al. (2005) Gap junction-mediated intercellular biochemical coupling in cochlear supporting cells is required for normal cochlear functions. Proc Natl Acad Sci U S A 102: 15201-15206.
44. Evans WH, De Vuyst E, Leybaert L, (2006) The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem J 397: 1-14.
45. Zhao HB, Yu N, Fleming CR, (2005) Gap junctional hemichannel-mediated ATP release and hearing controls in the inner ear. Proc Natl Acad Sci U S A 102: 18724-18729.
46. Kelly JJ, Forge A, Jagger DJ, (2011) Development of gap junctional intercellular communication within the lateral wall of the rat cochlea. Neuroscience 180: 360-369.
47. Schmidt M, Katano H, Bossis I, Chiorini JA, (2004) Cloning and characterization of a bovine adeno-associated virus. J Virol 78: 6509-6516.
48. Steel KP, Barkway C, (1989) Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development 107: 453-463.
49. Santarelli R, Arslan E, Carraro L, Conti G, Capello M, et al. (2003) Effects of isoflurane on the auditory brainstem responses and middle latency responses of rats. Acta Otolaryngol 123: 176-181.
50. Di Virgilio F, Steinberg TH, Silverstein SC, (1989) Organic-anion transport inhibitors to facilitate measurement of cytosolic free Ca2+ with fura-2. Methods Cell Biol 31: 453-462.