Disruption of α3 connexin gene leads to proteolysis and cataractogenesis in mice

Cell

Volumn 91, Issue 6, 1997, Pages 833-843

  Gong, Xiaohua ^a   Li, En ^b   Klier, George ^a   Huang, Qingling ^c   Wu, Ying ^a   Lei, Hong ^b   Kumar, Nalin M ^a   Horwitz, Joseph ^c   Gilula, Norton B ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c JULES STEIN EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN; BETA GALACTOSIDASE; CONNEXIN 46;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATARACTOGENESIS; CELL COMMUNICATION; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIUM CELL; GENE DISRUPTION; HOMEOSTASIS; LENS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; AGING; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; CATARACT; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MOLECULAR GENETICS; MOUSE MUTANT; PATHOLOGY; POLYMERASE CHAIN REACTION; REPORTER GENE; RESTRICTION MAPPING; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ANIMALIA; RODENTIA;

AGING; AMINO ACID SEQUENCE; ANIMALS; BETA-GALACTOSIDASE; CATARACT; CONNEXINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; LENS, CRYSTALLINE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING;

EID: 0031283282     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80471-7     Document Type: Article

References (52)

1. AI-Ghoul, K.J., Lane, C.W.,Taylor, V.L., Fowler, W.C., and Costello, M.J. (1996). Distribution and type of morphological damage in human nuclear age-related cataracts. Exp. Eye Res. 62 237-251.
2. Bassnett, S., and Mataic, D. (1997). Chromatin degradation in differentiating fiber cells of the eye lens. J. Cell Biol. 137, 37-49.
3. Bloemendal, H. (1981). Molecular and cellular biology of the eye lens. (New York: John Wiley and Sons), pp. 85-136.
4. Bond, J., Green, C., Donaldson, P., and Kistler, J. (1996). Liquefaction of cortical tissue in diabetic and galactosemic rat lenses defined by confocal laser scanning microscopy. Invest. Ophthal. and Vis. Sci. 37, 1557-1565.
5. Bonnerot, C., and Nicolas, J.F. (1993). Application of lacZ gene fusion to postimplantation development. In Methods in Enzymology, P.M. Wassarman and M.L. DePamphilis, eds., pp. 451-469.
6. Bonnerot, C., Rocancourt, D., Briand, P., Grimber, G., and Nicolas, J.F. (1987). A β-galactosidase hybrid protein targeted to nuclei as a marker for developmental studies. Proc. Natl. Acad. Sci. USA 84, 6795-6799.
7. Brady, J.P., Garland, D., Duglas-Tabor, Y., Robison, W.G., Jr., Groome, A., and Wawrousek, E.F. (1997). Targeted disruption of the mouse αA-crystallin gene induces cataract and cytoplasmic inclusion bodies containing the small heat shock protein αB-crystallin. Proc. Natl. Acad. Sci. USA 94, 884-889.
8. Brakenhoff, R.H., Henskens, H.A.M., van Rossum, M.W.P.C., Lubsen, N.H., and Schoenmakers, J.G.G. (1994). Activation of the γE-crystallin pseudogene in the human hereditary Coppock-like cataract. Hum. Mol. Genet. 3, 279-283.
9. Bruzzone, R., White, T.W., and Paul, D.L. (1996). Connections with connexins: the molecular basis of direct intercellular signaling. Eur. J. Biochem. 238, 1-27.
10. Caputo, A., James, M.N., Powers, J.C., Hudig, D., and Bleackley, R.C. (1994). Conversion of the substrate specificity of mouse proteinase granzyme B. Nat. Struct. Biol. 1, 364-367.
11. Chaudun, E., Arruti, C., Courtois, Y., Ferrag, F., Jeanny, J.C., Patel, B.N., Skidmore, C.,Torriglia, A., and Counis, M.F. (1994). DNA strand breakage during physiological apoptosis of the embryonic chick lens: free 3′ OH end single strand breaks do not accumulate even in the presence of a cation-independent deoxyribonuclease. J. Cell. Phys. 158, 354-364.
12. Costello, M.J., Mclntosh, T.J., and Robertson, D. (1989). Distribution of gap junctions and square array junctions in the mammalian lens. Invest. Ophthal. and Vis. Sci. 30, 975-989.
13. David, L.L., and Shearer, T.R. (1986). Purification of calpain II from rat lens and determination of endogenous substrates. Exp. Eye Res. 42, 227-238.
14. Duncan, G., Williams, M.R., and Riach, R.A. (1994). Calcium cell signaling and cataract. Prog. Retin. Eye Res. 13, 623-652.
15. Dunia, I., Smit, J.J.M., van der Walk, M.A., Bloemendal, H., Borst, P. and Benedetti, E.L. (1996). Human MDR3-P-Glycoprotein expression in transgenic mice induces lens membrane alterations leading to cataract. J. Cell Biol. 132, 701-716.
16. Evans, C.W., Eastwood, S., Rains, J., Gruijters, W.T., Bullivant, S., and Kistler, J. (1993). Gap junction formation during development of the mouse lens. Eur. J. Cell Biol. 60, 243-249.
17. Goodenough, D.A. (1992). The crystalline lens. A system networked by gap junctional intercellular communication. Sem. in Cell Biol. 3, 49-58.
18. Goring, D.R., Rossant, J., Clapoff, S., Breitman, M.L., and Tsui, L.C. (1987). In situ detection of β-galactosidase in lenses of transgenic mice with a γ-crystallin/lacZ gene. Science 235, 456-458.
19. Harding, J.J., and Crabbe, M.J.C. (1984). The lens: development, proteins, metabolism and cataract. In The Eye, H. Davson, ed. (Orlando, FL: Academic Press), pp. 207-492.
20. Jahngen-Hodge J., Cyr, D., Laxman, E., Taylor, A. (1992) Ubiquitin and ubiquitin conjugates in human lens. Exp. Eye Res. 55, 897-902.
21. Jarvis, L.J., Kumar, N.M., and Louis, C.F. (1993). The developmental expression of three mammalian lens fiber cell membrane proteins. Invest. Ophthal. and Vis. Sci. 34, 613-620.
22. Jiang, J.X., White, T.W., and Goodenough, D.A. (1995). Changes in connexin expression and distribution during chick lens development. Develop. Biol. 168, 649-661.
23. Kumar, N.M., and Gilula, N.B. (1996) The gap junction communication channel. Cell 84, 381-388.
24. Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926.
25. Li, W.C., Kuszak, J.R., Dunn, K., Wang, R.-R., Ma, W., Wang, G.-M., Spector, A., Lieb, M., Cotliar, A.M., Weiss, M., et al. (1995). Lens epithelial cell apoptosis appears to be a common cellular basis for non-congenital cataract development in humans and animals. J. Cell Biol. 130, 169-181.
26. Lin, J.S., Fitzgerald, S., Dong, Y., Knight, C., Donaldson, P., and Kistler, J. (1997). Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain. Eur. J. Cell Biol. 73, 141-149.
27. Lo, W.K., and Kuck, J.F.R. (1987). Alterations in fiber cell membranes of Emory mouse cataract: a morphological study. Curr. Eye Res. 6, 433-444.
28. Mackay, D., lonides, A., Berry, V., Moore, A., Bhattacharya, S., and Shiels, A. (1997). A new locus for dominant "zonular pulverulent" cataract, on chromosome 13. Am. J. Hum. Genet. 60, 1474-1478.
29. Mathias, R.T., Rae, J.L., and Baldo, G.J. (1997). Physiological properties of the normal lens. Physiol. Rev. 77, 21-49.
30. Mitton, K.P., Kamiya, T., Tumminia, S.J., and Russell, P. (1996). Cysteine protease activated by expression of HIV-1 protease in transgenic mice. MIP26 (aquaporin-0) cleavage and cataract formation in vivo and ex vivo. J. Biol. Chem. 277, 31803-31806.
31. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
32. Patel. T., Gores, G.J., and Kaufmann, S.H. (1996). The role of proteases during apoptosis. FASEB J. 10, 587-597.
33. Paul, D.L., Ebihara, L., Takemoto, L.J., Swenson, K.I., and Goodenough, D.A. (1991). Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J. Cell Biol. 115, 1077-1089.
34. Rae, J.L., Bartling, C., Rae, J., and Mathias, R.T. (1996). Dye transfer between cells of the lens. J. Mem. Biol. 150, 89-103.
35. Rao, P.V., Huang, Q.L., Horwitz, J., and Zigler, J.S., Jr. (1995). Evidence that α-crystallin prevents non-specific protein aggregation in the intact eye lens. Biochim. Biophys. Acta 1245, 439-447.
36. Risek, B., Klier, F.G., and Gilula, N.B. (1994). Developmental regulation and structural organization of connexins in epidermal gap junctions. Dev. Biol. 164, 183-196.
37. Robinson, K.R., and Patterson, J.W. (1983). Localization of steady currents in the lens. Curr. Eye Res. 2, 843-847.
38. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning, A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Press).
39. Shearer, T.R., David, L.L., Andersen, R.S., and Azuma, M. (1992). Review of selenite cataract. Curr. Eye Res. 11, 357-369.
40. Shiels, A., and Bassnett, S. (1996). Mutations in the founder of the MIP gene family underlie cataract development in the mouse. Nat. Genet. 12, 212-215.
41. Siezen, R.J., Wu, E., Kaplan, E.D., Thomson, J.A., and Benedek, G.B. (1988). Rat lens γ-crystallins. Characterization of the six gene products and their spatial and temporal distribution resulting from differential synthesis. J. Mol. Biol. 199, 475-490.
42. Spector, A. (1985). Aspects of the biochemistry of cataract. In The Ocular Lens: Structure, Function, and Pathology. H. Maisel, ed. (New York: Marcel Dekker, Inc.), pp. 405-438.
43. Srivastava, O.P., and Srivastava, K. (1996). Characterization of three isoforms of a 9 kDa γ-crystallin fragment isolated from human lenses. Exp. Eye Res. 62, 593-604.
44. Takemoto, L. (1994). Release of αA sequence 158-173 correlates with a decrease in the molecular chaperone properties of native α-crystallin. Exp. Eye Res. 59, 239-242.
45. Truscott, R.J., Marcantonio, J.M., Tomlinson, J., and Duncan, G. (1990). Calcium-induced opacification and proteolysis in the intact rat lens. Invest. Ophthal. and Vis. Sci. 31, 2405-2411.
46. Tybulewicz, V.L., Crawford, C.E., Jackson, P.K., Bronson, R.T., and Mulligan, R.C. (1991). Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65, 1153-1163.
47. White, T.W., Bruzzone, R., Goodenough, D.A., and Paul, D.L. (1992). 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.
48. Wride.M.A. (1996). Cellular and molecular features of lens differentiation: a review of recent advances. Differentiation 61, 77-94.
49. Yancey, S.B., Biswal, S., and Revel, J.P. (1992). Spatial and temporal patterns of distribution of the gap junction protein connexin 43 during mouse gastrulation and organogenesis. Development 114, 203-212.
50. Yoshida, H., Murachi, T., and Tsukahara, I. (1985). Age-related changes of calpain II and α-crystallin in the lens of hereditary cataract (Nakano) mouse. Curr. Eye Res. 4, 983-988.
51. Yoshida, H., Yumoto, N., Tsukahara, I., and Murachi, T. (1986). The degradation of α-crystallin at its carboxyl-terminal portion by calpain in bovine lens. Invest. Ophthal. and Vis. Sci. 27, 1269-1273.
52. Zampighi, G.A., Hall, J.E., Ehring, G.R., and Simon, S.A. (1989). The structural organization and protein composition of lens fiber junctions. J. Cell Biol. 108, 2255-2275.