Lens Fiber Connexin Turnover and Caspase-3-Mediated Cleavage Are Regulated Alternately by Phosphorylation

REFERENCES

• Aviel S, Winberg G, Massucci M, Ciechanover A. Degradation of the Epstein-Barr latent membrane protein 1 (LMP) by the ubiquitin-proteasome pathway-targeting via ubiquitination of the N-terminal residue. J Biol Chem 2000; 275: 23491–23499
   PubMed Web of Science ®Google Scholar
• Bassnett S. Lens organelle degradation. Exp Eye Res 2002; 74: 1–6
   PubMed Web of Science ®Google Scholar
• Bassnett S, Duncan G. Direct measurement of pH in the rat lens by ion-sensitive microelectrodes. Exp Eye Res 1985; 40: 585–590
   PubMed Web of Science ®Google Scholar
• Berthoud V M, Bassnett S, Beyer E C. Cultured chicken embryo lens cells resemble differentiating fiber cells in vivo and contain two kinetic pools of connexin56. Exp Eye Res 1999; 68: 475–484
   PubMed Web of Science ®Google Scholar
• Cheng H L, Louis C F. Endogenous casein kinase I catalyzes the phosphorylation of the lens fiber cell connexin49. Eur J Biochem 1999; 263: 276–286
   PubMedGoogle Scholar
• Cheng H L, Louis C F. Functional effects of casein kinaes I-catalyzed phosphorylation on lens cell-to-cell coupling. J Membr Biol 2001; 181: 21–30
   PubMed Web of Science ®Google Scholar
• Cottrell G T, Lin R, Warn-Cramer B J, Lau A F, Burt J M. Mechanism of v-Src-and mitogen-activated protein kinase-induced reduction of gap junction communication. Am J Physiol 2003; 284: C511–C520
   PubMed Web of Science ®Google Scholar
• Dahm R. Lens fibre cell differentiation—A link with apoptosis?. Ophthalmic Res 1999; 31: 163–183
   PubMed Web of Science ®Google Scholar
• Donaldson P, Kistler J, Mathias R T. Molecular solutions to mammalian lens transparency. News Physiol 2001; 16: 118–123
   PubMedGoogle Scholar
• Girao H, Pereira P. Phosphorylation of connexin 43 acts as a stimuli for proteasome-dependent degradation of the protein in lens epithelial cells. Mol Vis 2003; 9: 24–30
   PubMed Web of Science ®Google Scholar
• Gong X, Li E, Klier G, Huang Q, Wu Y, Lei H, Kumar N M, Horwitz J, Gilua N B. Disruption of α 3 connexin gene leads to proteolysis and cataractogenesis in mice. Cell 1997; 91: 833–843
   PubMed Web of Science ®Google Scholar
• Goodenough D A. The crystalline lens: a system networked by gap junctional intercellular communication. Seminars in Cell Biology, N. B. Gilula. Sauders Scientific Pub./Academic Press, London 1992; 49–58
   Google Scholar
• Gu S, Yu X S, Yin X, Jiang J X. Stimulation of lens cell differentiation by gap junction protein connexin 45.6. Invest Ophthalmol Vis Sci 2003; 44: 2103–2111
   PubMed Web of Science ®Google Scholar
• Guan X J, Ruch R J. Gap junction endocytosis and lysosomal degradation of connexin43-p2 in wb-f344 rat liver epithelial cells treated with ddt and lindane. Carcinogenesis 1996; 17: 1791–1798
   PubMedGoogle Scholar
• Hertlein B, Butterweck A, Haubrich S, Willecke K, Traub O. Phosphorylated carboxy terminal serine residues stabilize the mouse gap junction protein connexin45 against degradation. J Membr Biol 1998; 162: 247–257
   PubMed Web of Science ®Google Scholar
• Hicke L. Gettin'down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 1999; 9: 107–112
   PubMed Web of Science ®Google Scholar
• Hicke L, Zanolari B, Riezman H. Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J Cell Biol 1998; 141: 349–358
   PubMed Web of Science ®Google Scholar
• Hossain M Z, Ao P, Boynton A L. Rapid disruption of gap junctional communication and phosphorylation of connexin43 by platelet-derived growth factor in T51B rat liver epithelial cells expressing platelet-derived growth factor receptor. J Cell Physiol 1998; 174: 66–77
   PubMed Web of Science ®Google Scholar
• Hughes S H, Greenhouse J J, Petropoulos C J, Sutrave P. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J Virol 1987; 61: 3004–3012
   PubMed Web of Science ®Google Scholar
• Jiang J X. Use of retroviruses to express connexins. Connexin methods and protocols, R. Bruzzone, C. Giaume. Humana Press, Totowa 2001; 159–174
   Google Scholar
• Jiang J X, Goodenough D A. Phosphorylation of lens fiber connexins by protein kinase C. Eur J Biochem 1998a; 255: 37–44
   PubMedGoogle Scholar
• Jiang J X, Goodenough D A. Retroviral expression of connexins in embryonic chick lens. Invest Ophthalmol Vis Sci 1998b; 39: 537–543
   PubMed Web of Science ®Google Scholar
• Jiang J X, White T W, Goodenough D A, Paul D L. Molecular cloning and functional characterization of chick lens fiber connexin45.6. Mol Biol Cell 1994; 5: 363–373
   PubMed Web of Science ®Google Scholar
• Kelly S M, VanSlyke J K, Musil L S. Regulation of ubiquitin-proteasome system-mediated degradation by cytosolic stress. Mol. Biol. Cell 2007; 18: 4279–4291
   PubMed Web of Science ®Google Scholar
• Kuroki T, Inoguchi T, Umeda F, Ueda F, Nawata H. High glucose induces alteration of gap junction permeability and phosphorylation of connexin-43 in cultured aortic smooth muscle cells. Diabetes 1998; 47: 931–936
   PubMed Web of Science ®Google Scholar
• Laing J G, Beyer E C. The gap junction protein connexin43 is degraded via the ubiquitin proteasome pathway. J Biol Chem 1995; 270: 26399–26403
   PubMed Web of Science ®Google Scholar
• Laing J G, Tadros P N, Green K, Saffitz J E, Beyer E C. Proteolysis of connexin43-containing gap junctions in normal and heat-stressed cardiac myocytes. Cardiovasc Res 1998; 38: 711–718
   PubMed Web of Science ®Google Scholar
• Laird D W. Connexin phosphorylation as a regulatory event linked to gap junction internalization and degradation. Biochim Biiophys Acta 2005; 1711: 172–182
   PubMed Web of Science ®Google Scholar
• Laird D W, Puranam K L, Revel J P. Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem J 1991; 273: 67–72
   PubMed Web of Science ®Google Scholar
• Leykauf K, Salek M, Bomke J, Frech M, Lehmann W-D, Durst M, Alonso A. Ubiquitin protein ligase Nedd4 binds to connexin43 by a phosphorylation-modulated process. J Cell Sci 2006; 119: 3634–3642
   PubMed Web of Science ®Google Scholar
• Lin H K, Wang L, Hu Y C, Altuwaijri S, Chang C. Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J 2002; 21: 4037–4048
   PubMed Web of Science ®Google Scholar
• Lin J S, Eckert R, Kistler J, Donaldson P. Spatial differences in gap junction gating in the lens are a consequence of connexin cleavage. Eur J Cell Biol 1998; 76: 246–250
   PubMed Web of Science ®Google Scholar
• Lin J S, Fitzgerald S, Dong Y, Knight C, Donaldson P, Kistler J. Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain. Eur J Cell Biol 1997; 73: 141–149
   PubMed Web of Science ®Google Scholar
• Menko A S, Klukas K A, Johnson R G. Chicken embryo lens cultures mimic differentiation in the lens. Dev Biol 1984; 103: 129–141
   PubMedGoogle Scholar
• Moreno A P, Lau A F. Gap junction channel gating modulated through protein phosphorylation. Prog Biophys Mol Biol 2007; 94: 107–119
   PubMed Web of Science ®Google Scholar
• Musil L S, Beyer E C, Goodenough D A. Expression of the gap junction protein connexin43 in embryonic chick lens: molecular cloning, ultrastructural localization, and post-translational phosphorylation. J Membr Biol 1990; 116: 163–175
   PubMed Web of Science ®Google Scholar
• Musil L S, Goodenough D A. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol 1991; 115: 1357–1374
   PubMed Web of Science ®Google Scholar
• Musil L S, Le A-CN, VanSlyke J K, Roberts L M. Regulation of connexin degradation as a mechanism to increase gap junction assembly and function. J Biol Chem 2000; 275: 25207–25215
   PubMed Web of Science ®Google Scholar
• Paul D L, Ebihara L, Takemoto L J, Swenson K I, Goodenough D A. Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J Cell Biol 1991; 115: 1077–1089
   PubMed Web of Science ®Google Scholar
• Pereira P, Shang F, Hobbs M, Girao H, Taylor A. Lens fibers have a fully functional ubiquitin-proteasome pathway. Exp Eye Res 2003; 76: 623–631
   PubMed Web of Science ®Google Scholar
• Qin H, Shao Q, Igdoura S A, Alaoui-Jamali M A, Laird D W. Lysosomal and proteasomal degradation play distinct roles in the life cycle of Cx43 in gap junctional intercellular communication-deficient and-competent breast tumor cells. J Biol Chem 2003; 278: 30005–30014
   PubMed Web of Science ®Google Scholar
• Rong P, Wang X, Niesman I, Wu Y, Benedetti L E, Dunia I, Levy E, Gong X. Disruption of Gja8 (α 8 connexin) in mice leads to microphthalmia associated with retardation of lens growth and lens fiber maturation. Development 2002; 129: 167–174
   PubMed Web of Science ®Google Scholar
• Rup D M, Veenstra R D, Wang Z, Brink P R, Beyer E C. Chick connexin-56, a novel lens gap junction protein. J Biol Chem 1993; 268: 706–712
   PubMed Web of Science ®Google Scholar
• Saffitz J E, Laing J G, Yamada K A. Connexin expression and turnover-implications for cardiac excitability. Cir Res 2000; 86: 723–728
   PubMed Web of Science ®Google Scholar
• Shang F, Gong X, McAvoy J W, Chamberlain C, Nowell T R, Taylor A. Ubiquitin-dependent pathway is up-regulated in differentiating lens cells. Exp Eye Res 1999; 68: 179–192
   PubMed Web of Science ®Google Scholar
• Solan J L, Lampe P D. Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biiochim Biophys Acta 2005; 1711: 154–163
   PubMed Web of Science ®Google Scholar
• Tedesco D, Lukas J, Reed S I. The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF (Skp2). Genes Dev 2002; 16: 2946–2957
   PubMed Web of Science ®Google Scholar
• VanSlyke J K, Deschenes S M, Musil L S. Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction protein. Mole Biol Cell 2000; 11: 1933–1946
   PubMed Web of Science ®Google Scholar
• VanSlyke J K, Musil L S. Dislocation and degradation from the ER are regulated by cytosolic stress. J Cell Biol 2002; 157: 381–394
   PubMed Web of Science ®Google Scholar
• White T W. Unique and redundant connexin contributions to lens development. Science 2002; 295: 319–320
   Google Scholar
• White T W, Bruzzone R, Goodenough D A, Paul D L. Mouse Cx50, a functional member of the connexin family of gap junction proteins, is the lens fiber protein MP70. Mol Biol Cell 1992; 3: 711–720
   PubMed Web of Science ®Google Scholar
• White T W, Goodenough D A, Paul D L. Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J Cell Biol 1998; 143: 815–825
   PubMed Web of Science ®Google Scholar
• Winston J T, Strack P, Beer-Romero P, Chu C Y, Elledge S J, Harper J W. The SCFβTRCP- ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in Iκ Bα and β-catenin and stimulates Iκ Bα ubiquitination in vitro. Genes Dev 1999; 13: 270–283
   PubMed Web of Science ®Google Scholar
• Wride M A. Minireview: apoptosis as seen through a lens. Apoptosis 2000; 5: 203–209
   PubMed Web of Science ®Google Scholar
• Wride M A, Parker E, Sanders E J. Members of the Bcl-2 and caspase families regulate nuclear degeneration during chick lens fire differentiation. Dev Biol 1999; 213: 142–156
   PubMed Web of Science ®Google Scholar
• Yin X, Gu S, Jiang J X. The development-associated cleavage of lens connexin 45.6 by caspase-3-like protease is regulated by casein kinase II-mediated phosphorylation. J Biol Chem 2001; 276: 34567–34572
   PubMed Web of Science ®Google Scholar
• Yin X, Jedrzejewski P T, Jiang J X. Casein kinase II phosphorylates lens connexin 45.6 and is involved in its degradation. J Biol Chem 2000; 275: 6850–6856
   PubMed Web of Science ®Google Scholar