Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain

European Journal of Cell Biology

Volumn 73, Issue 2, 1997, Pages 141-149

  Lin, Jun Sheng ^a   Fitzgerald, Sandra ^a   Dong, Yimin ^a   Knight, Catriona ^a   Donaldson, Paul ^a   Kistler, Joerg ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Calpain; Connexins; Gap junctions; Lens; Proteolysis

Indexed keywords

CALPAIN; GAP JUNCTION PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CELL JUNCTION; CELL MEMBRANE; LENS; MEMBRANE STRUCTURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SHEEP;

ANIMALIA; MAMMALIA; OVIS; OVIS ARIES;

EID: 0030958516     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Azuma, M. T. R. Shearer, T. Matsumoto, L. L. David, T. Murachi: Calpain II in two in vivo models of sugar cataract. Exp. Eye Res. 51, 393-401 (1990).
2. Azuma M., L. L. David, T. R. Shearer: Cysteine protease inhibitor E64 reduces the rate of formation of selenite cataract in the whole animal. Curr. Eye Res. 10, 657-666 (1991).
3. Baldo, G. J., R. T. Mathias: Spatial variations in membrane properties in the intact rat lens. Biophys. J. 63, 518-529 (1992).
4. Bassnett, S., D. C. Beebe: Coincident loss of mitochondria and nuclei during lens fiber cell differentiation. Dev. Dynam. 194, 85-93 (1992).
5. Becker, D. L., W. H. Evans, C. R. Green, A. Warner: Functional analysis of amino acid sequences in connexin43 involved in intercellular communication through gap junctions. J. Cell Sci. 108, 1455-1467 (1995).
6. Bennett, M., L. C. Barrio, T. A. Bargiello, D. C. Spray, E. Hertzberg, J. C. Saez: Gap junctions - new tools, new answers, new questions. Neuron 6, 305-320 (1991).
7. Beyer, E. C., D. L. Paul, D. A. Goodenough: Connexin43: a protein from the rat heart homologous to a gap junction protein from the liver. J. Cell Biol. 105, 2621-2629 (1987).
8. Beyer, E. C.: Gap junctions. Int. Rev. Cytol. 137, 1-37 (1993).
9. Church, R. L., J. H. Wang, E. Steele: The human lens intrinsic membrane protein MP70 (Cx50) gene: clonal analysis and chromosome mapping. Curr. Eye Res. 14, 215-221 (1995).
10. Croall, E., G. N. Demartino: Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol. Rev. 71, 813-847 (1991).
11. Crow, D. S., E. C. Beyer, D. L. Paul, S. S. Kobe, A. F. Lau: Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus transformed mammalian fibroblasts. Mol. Cell. Biol. 10, 1754-1763 (1990).
12. David, L. L., T. R. Shearer, M. Shih: Sequence analysis of lens β-crystallins suggests involvement of calpain in cataract formation. J. Biol. Chem. 268, 1937-1940 (1993).
13. Duncan, G., M. R. Williams, R. A. Riach: Calcium, cell signalling and cataract. Prog. Retin. Eye Res. 13, 623-652 (1994).
14. Evans, C. W., S. Eastwood, J. Rains, W. T. M. Gruijters, S. Bullivant, J. Kistler: Gap junction formation during development of the mouse lens. Eur. J. Cell Biol. 60, 243-249 (1993).
15. Filson, A. J., R. Azarnia, E. C. Beyer, W. R. Loewenstein, J. S. Brugge: Tyrosine phosphorylation of a gap junction protein correlates with inhibition of cell-to-cell communication. Cell Growth Differ. 1, 661-668 (1990).
16. Fishman, G. I., A. P. Moreno, D. C. Spray, L. A. Leinwand: Functional analysis of human cardiac gap junction channel mutants. Proc Natl. Acad. Sci. USA 88, 3525-3529 (1991).
17. Ghoshroy, S., D. A. Goodenough, G. E. Sosinsky: Preparation, characterization, and structure of half gap junctional layers split with urea and EGTA. J. Membr. Biol. 146, 15-28 (1995).
18. Goodenough, D. A., L. S. Musil: Gap junctions and tissue business - problems and strategies for developing specific functional reagents. J. Cell Sci. Suppl. 17, 133-138 (1993).
19. Goodenough, D. A., D. L. Paul, L. Jesaitis: Topological distribution of two connexin32 antigenic sites in intact and split rodent hepatocyte gap junctions. J. Cell Biol. 107, 1817-1824 (1988).
20. Gruijters, W. T. M., J. Kistler, S. Bullivant: Formation, distribution and dissociation of intercellular junctions in the lens. J. Cell Sci. 88, 351-359 (1987).
21. Gupta, V. K., V. M. Berthoud, N. Atal, J. A. Jarillo, L. C. Barrio, E. C. Beyer: Bovine connexin44, a lens gap junction protein: molecular cloning, immunologic characterization, and functional expression. Invest. Ophthalmol. Visual Sci. 35, 3747-3758 (1994).
22. Kistler, J., S. Bullivant: Protein processing in lens intercellular junctions: cleavage of MP70 to MP38. Invest. Ophthalmol. Visual Sci. 28, 1687-1692 (1987).
23. Kistler, J., D. Christie, S. Bullivant: Homologies between gap junction proteins in lens, heart and liver. Nature 331, 721-723 (1988).
24. Kistler, J., K. Goldie, P. Donaldson, A. Engel: Reconstitution of native-type noncrystalline lens fiber gap junctions from isolated hemi-channels. J. Cell Biol. 126, 1047-1058 (1994).
25. Kistler, J., B. Kirkland, S. Bullivant: Identification of a 70000-D protein in lens membrane junctional domains. J. Cell Biol. 101, 28-35 (1985).
26. Kistler, J., J. Schaller, H. Sigrist: MP38 contains the membrane-embedded domain of the lens fiber gap junction protein MP70. J. Biol. Chem. 265, 13357-13361 (1990).
27. Konig, N., G. A. Zampighi: Purification of bovine lens cell-to-cell channels composed of connexin44 and connexin50. J. Cell Sci. 108, 3091-3098 (1995).
28. Kumar, N. M., N. B. Gilula: The gap junction communication channel. Cell 84, 381-388 (1996).
29. Liu, S. G., S. Taffet, L. Stoner, M. Delmar, M. L. Vallano, J. Jalife: A structural basis for the unequal sensitivity of the major cardiac and liver gap junctions to intracellular acidification - the carboxyl tail length. Biophys. J. 64, 1422-1433 (1993).
30. Loo, L. W., J. M. Berestecky, M. Y. Kanemitsu, A. F. Lau: pp60src-mediated phosphorylation of connexin 43, a gap junction protein. J. Biol. Chem. 270, 12751-12761 (1995).
31. Makowski, L., D. L. D. Caspar, W. C. Phillips, D. A. Goodenough: Gap junction structures. II. Analysis of the X-ray diffraction data. J. Cell Biol. 74, 629-645 (1977).
32. Manjunath, C. K., G. E. Goings, E. Page: Proteolysis of cardiac gap junctions during their isolation from rat hearts. J. Membr. Biol. 85, 159-168 (1985).
33. Milks, L. C., N. M. Kumar, R. Houghten, N. Unwin, N. B. Gilula: Topology of the 32-kd liver gap junction protein determined by site-directed antibody localizations. EMBO J. 7, 2967-2975 (1988).
34. Murachi, T.: Intracellular regulatory system involving calpain and calpastatin. Biochem. Int. 18, 263-294 (1989).
35. Musil, L. S., D. A. Goodenough: Gap junctional intercellular communication and the regulation of connexin expression and function. Curr. Opin. Cell Biol. 2, 875-880 (1990).
36. Paul, D. L., L. Ebihara, L. J. Takemoto, K. I. Swenson, D. A. Goodenough: Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J. Cell Biol. 115, 1077-1089 (1991).
37. Prescott, A., G. Duncan, J. Vanmarle, G. Vrensen: A correlated study of metabolic cell communication and gap junction distribution in the adult frog lens. Exp. Eye Res. 58, 737-746 (1994).
38. Sandilands, A., A. R. Prescott, J. M. Carter, A. N. Hutcheson, R. A. Ouinlan, J. Richards, P. G. Fitzgerald: Vimentin and CP49/filensin form distinct networks in the lens which are independently modulated during lens fibre cell differentiation. J. Cell Sci. 108, 1397-1406 (1995).
39. Savart, M., M. Belamri, V. Pallet, A. Ducastaing: Association of calpains 1 and 2 with protein kinase C activities. FEBS Lett. 216, 22-26 (1987).
40. Shibata, Y., C. K. Manjunath, E. Page: Differences between cytoplasmic surfaces of deep-etched heart and liver gap junctions. Am. J. Physiol. 249, H690-H693 (1985).
41. Sosinsky, G. E.: Image analysis of gap junction structures. Electron Microsc. Rev. 5, 59-76 (1992).
42. Suzuki, K., S. Ohno: Calcium activated neutral protease -structure-function relationship and functional implications. Cell Struct. Func. 15, 1-6 (1990).
43. Swenson, K. I., I. R. Jordan, E. C. Beyer, D. L. Paul: Formation of gap junctions by expression of connexins in Xenopus oocyte pairs. Cell 57, 145-155 (1989).
44. Ten Broek, E. M., R. Johnson, C. F. Louis: Cell-to-cell communication in a differentiating ovine lens culture system. Invest. Ophthalmol. Visual Sci. 35, 215-228 (1994).
45. Unwin, P. N. T., P. D. Ennis: Two configurations of a channel forming protein. Nature 307, 609-613 (1984).
46. Vrensen, G. F. J., J. Graw, A. De Wolf: Nuclear breakdown during terminal differentiation of primary lens fibres in mice: a transmission electron microscopic study. Exp. Eye Res. 52, 647-659 (1991).
47. White, T. W., R. Bruzzone, D. A. Goodenough, D. L. Paul: Mouse Cx50, a functional member of the connexin family of gap junction proteins, is the lens fiber protein, MP70. Mol. Biol. Cell 3, 711-720 (1992).
48. White, T. W., R. Bruzzone, D. L. Paul: The connexin family of intercellular channel forming proteins. Kidney Int. 48, 1148-1157 (1995).
49. Willecke, K., H. Hennemann, E. Dahl, S. Jungbluth, R. Heynkes: The diversity of connexin genes encoding gap junctional proteins. Eur. J. Cell Biol. 56, 1-7 (1991).
50. Yang, D. I., C. F. Louis: Molecular cloning of sheep connexin49 and its identity with MP70. Curr. Eye Res. 15, 307-314 (1996).
51. Yeager, M., N. B. Gilula: Membrane topology and quaternary structure of cardiac gap junction ion channels. J. Mol. Biol. 223, 929-948 (1992).
52. Yeager, M.: Electron microscopic image analysis of cardiac gap junction membrane crystals. Microsc. Res. Techn. 31, 452-466 (1995).
53. Yoshida, H., T. Murachi, I. Tsukahara: Distribution of calpain I, calpain II and calpastatin in bovine lens. Invest. Ophthamol. Visual Sci. 26, 953-956 (1985).
54. Zhang, J.-T., B. Nicholson: Sequence and tissue distribution of a second protein of hepatic gap junctions, Cx26, as deduced from its cDNA. J. Cell Biol. 109, 3391-34401 (1989).
55. Zhang, J. T., B. J. Nicholson: The topological structure of connexin26 and its distribution compared to connexin32 in hepatic gap junctions. J. Membr. Biol. 139, 15-29 (1994).