Age-related cataracts in α3Cx46-knockout mice are dependent on a calpain 3 isoform

Investigative Ophthalmology and Visual Science

Volumn 48, Issue 6, 2007, Pages 2685-2694

  Tang, Yajun ^a   Liu, Xiangyang ^a   Zoltoski, Rebecca K ^b   Novak, Layne A ^c   Herrera, R Antonio ^a   Richard, Isabelle ^d   Kuszak, Jer R ^c   Kumar, Nalin M ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ILLINOIS COLLEGE OF OPTOMETRY   (United States)

^c RUSH UNIVERSITY MEDICAL CENTER   (United States)

^d GÉNÉTHON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALPAIN 3; CALPAIN; CAPN3 PROTEIN, MOUSE; CONNEXIN 46; GAMMA CRYSTALLIN; GAP JUNCTION PROTEIN; ISOPROTEIN; MUSCLE PROTEIN; UNCLASSIFIED DRUG;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATARACT; CATARACTOGENESIS; CONTROLLED STUDY; HISTOLOGY; HOMOZYGOTE; KNOCKOUT MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SCANNING LASER OPHTHALMOSCOPY; ANIMAL; BODY WATER; FEMALE; GENOTYPE; LENS; MALE; METABOLISM; MOUSE; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; ORGAN SIZE; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; WESTERN BLOTTING;

AGING; ANIMALS; BLOTTING, WESTERN; BODY WATER; CALCIUM; CALPAIN; CATARACT; CONNEXINS; FEMALE; GAMMA-CRYSTALLINS; GENOTYPE; LENS, CRYSTALLINE; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUSCLE PROTEINS; ORGAN CULTURE TECHNIQUES; ORGAN SIZE; PROTEIN ISOFORMS;

EID: 34347253592     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.06-0926     Document Type: Article

References (50)

1. Willecke K, Eiberger J, Degen J, et al. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 2002;383:725-737.
2. Hua VB, Chang AB, Tchieu JH, Kumar NM, Nielsen PA, Saier MH Jr. Sequence and phylogenetic analyses of 4 TMS junctional proteins of animals: connexins, innexins, claudins and occludins. J Membr Biol. 2003;194:59-76.
3. Yancey SB, Biswal S, Revel JP. Spatial and temporal patterns of distribution of the gap junction protein connexin43 during mouse gastrulation and organogenesis. Development. 1992;114:203-212.
4. Paul DL, Ebihara L, Takemoto LJ, Swenson KI, Goodenough DA. 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.
5. Church RL, Wang JH, Steele E. The human lens intrinsic membrane protein MP70 (Cx50) gene: clonal analysis and chromosome mapping. Curr Eye Res. 1995;14:215-221.
6. Gong X, Li E, Klier G, et al. Disruption of alpha3 connexin gene leads to proteolysis and cataractogenesis in mice. Cell. 1997;91: 833-843.
7. Gong X, Agopian K, Kumar NM, Gilula, NB. Genetic factors influence cataract formation in alpha 3 connexin knockout mice. Dev Genet. 1999;24:27-32.
8. Baruch A, Greenbaum D, Levy ET, et al. Defining a link between gap junction communication, proteolysis, and cataract formation. J Biol Chem. 2001;276:28999-29006.
9. Gao J, Sun X, Martinez-Wittinghan FJ, Gong X, White TW, Mathias RT. Connections between connexins, calcium, and cataracts in the lens. J Gen Physiol. 2004;124:289-300.
10. Duncan G, Jacob TJ. Calcium and the physiology of cataract. Ciba Found Symp. 1984;106:132-152.
11. Sandberg HO, Closs O. The alpha and gamma crystallin content in aqueous humor of eyes with clear lenses and with cataracts. Exp Eye Res. 1979;28:601-610.
12. Pal JD, Liu X, Mackay D, et al. Connexin46 mutations linked to congenital cataract show loss of gap junction channel function. Am J Physiol. 2000;279:C596-C602.
13. Minogue PJ, Liu X, Ebihara L, Beyer EC, Berthoud VM. An aberrant sequence in a connexin46 mutant underlies congenital cataracts. J Biol Chem. 2005;280:40788-40795.
14. Biswas S, Harris F, Dennison S, Singh J, Phoenix DA. Calpains: targets of cataract prevention? Trends Mol Med. 2004;10:78-84.
15. Tang D, Borchman D, Yappert MC, Vrensen GG, Rasi V. Influence of age, diabetes, and cataract on calcium, lipid-calcium, and protein-calcium relationships in human lenses. Invest Ophthalmol Vis Sci. 2003;44:2059-2066.
16. Ma H, Fukiage C, Azuma M, Shearer TR. Cloning and expression of mRNA for calpain Lp82 from rat lens: splice variant of p94. Invest Ophthalmol Vis Sci. 1998;39:454-461.
17. Ma H, Hata I, Shih M, et al. Lp82 is the dominant form of calpain in young mouse lens. Exp Eye Res. 1999;68:447-456.
18. Ma H, Shih M, Fukiage C, et al. Influence of specific regions in Lp82 calpain on protein stability, activity, and localization within lens. Invest Ophthalmol Vis Sci. 2000;41:4232-4239.
19. Nakamura Y, Fukiage C, Shih M, et al. Contribution of calpain Lp82-induced proteolysis to experimental cataractogenesis in mice. Invest Ophthalmol Vis Sci. 2000;41:1460-1466.
20. Tamada Y, Fukiage C, Mizutani K, et al. Calpain inhibitor, SJA6017, reduces the rate of formation of selenite cataract in rats. Curr Eye Res. 2001;22:280-285.
21. Richard I, Roudaut C, Marchand S, et al. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IkappaBalpha/nuclear factor kappaB pathway perturbation in mice. J Cell Biol. 2000;151:1583-1590.
22. Kuszak JR, Sivak JG, Weerheim JA. Lens optical quality is a direct function of lens suturai architecture. Invest Ophthalmol Vis Sci. 1991;32:2119-2129.
23. Sivak JG, Herbert KL, Peterson KL, Kuszak JR. The interrelationship of lens anatomy and optical quality. I. Non-primate lenses. Exp Eye Res. 1994;59:505-520.
24. Shiels A, Bassnett S, Varadaraj K, et al. Optical dysfunction of the crystalline lens in aquaporin-0-dencient mice. Physiol Genomics. 2001;7:179-186.
25. Al-Ghoul KJ, Kirk T, Kuszak AJ, Zoltoski RK, Shiels A, Kuszak JR. Lens structure in MIP-deficient mice. Anat Rec. 2003;273A:714-730.
26. Nielsen PA, Baruch A, Shestopalov VI, et al. Lens connexins alpha3Cx46 and alpha8Cx50 interact with zonula occludens protein-1 (ZO-1). Mol Biol Cell. 2003;14:2470-2481.
27. Xi J, Farjo R, Yoshida S, et al. A comprehensive analysis of the expression of crystalline in mouse retina. Mol Vis. 2003;9:410-419.
28. Rao PV, Huang QL, Horwitz J, et al. Evidence that α-crystallin prevents non-specific protein aggregation in the intact eye lens. Biochim Biophys Acta. 1995;1245:439-447.
29. Brady JP, Garland D, Duglas-Tabor Y, et al. 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. 1997;94:884-889.
30. Takemoto L. Release of αA sequence 158-173 correlates with a decrease in the molecular chaperone properties of native α-crystallin. Exp Eye Res. 1994;59:239-242.
31. Ueda Y, Fukiage C, Shih M, et al. Mass measurements of C-terminally truncated alpha-crystallins from two-dimensional gels identify Lp82 as a major endopeptidase in rat lens. Mol Cell Proteomics. 2002;1:357-365.
32. Harrington V, McCall S, Huynh S, et al. Crystalline in water soluble-high molecular weight protein fractions and water insoluble protein fractions in aging and cataractous human lenses. Mol Vis. 2004;10:476-489.
33. Duncan G, van Heyningen R. Distribution of non-diffusible calcium and sodium in normal and cataractous human lenses. Exp Eye Res. 1977;25:183-193.
34. Hightower KR. Cytotoxic effects of internal calcium on lens physiology: a review. Curr Eye Res. 1985;4:453-459.
35. Sanderson J, Marcantonio JM, Duncan G. A human lens model of cortical cataract: Ca2+-induced protein loss, vimentin cleavage and opacification. Invest Ophthalmol Vis Sci. 2000;41:2255-2261.
36. Sanderson J, Marcantonio JM, Duncan G. Calcium ionophore induced proteolysis and cataract: inhibition by cell permeable calpain antagonists. Biochem Biophys Res Commun. 1996;218:893-901.
37. Fougerousse F, Bullen P, Herasse M, et al. Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum Mol Genet. 2000;9:165-173.
38. Srivastava OP, Srivastava K. Degradation of gamma D- and gamma s-crystallins in human lenses. Biochem Biophys Res Commun. 1998;253:288-294.
39. Kawabata Y, Hata S, Ono Y, et al. Newly identified exons encoding novel variants of p94/calpain 3 are expressed ubiquitously and overlap the alpha-glucosidase C gene. FEBS Lett. 2003;555:623-630.
40. Sorimachi H, Toyama-Sorimachi N, Saido TC, et al. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J Biol Chem. 1993;268: 10593-10605.
41. Kuck JF, Kuck KD. The Emory mouse cataract: loss of soluble protein, glutathione, protein sulfhydryl and other changes. Exp Eye Res. 1983;36:351-362.
42. Kador PF, Fukui HN, Fukuishi S, et al. Philly mouse: a new model of hereditary cataract. Exp Eye Res. 1980;30:59-68.
43. Dilsiz N, Olcucu A, Atas M. Determination of calcium, sodium, potassium and magnesium concentrations in human senile cataractous lenses. Cell Biochem Funct. 2000;18:259-262.
44. Gao J, Sun X, Yatsula V, et al. Isoform-specific function and distribution of Na/K pumps in the frog lens epithelium. J Membr Biol. 2000;178:89-101.
45. Tamiya S, Dean WL, Paterson CA, et al. Regional distribution of Na,K-ATPase activity in porcine lens epithelium. Invest Ophthalmol Vis Sci. 2003;4:4395-4399.
46. Paterson CA, Delamere NA. ATPases and lens ion balance. Exp Eye Res. 2004;78:699-703.
47. Kobatashi S, Roy D, Spector A. Sodium/potassium ATPase in normal and cataractous human lenses. Curr Eye Res. 1983;2:327-334.
48. Duncan G, Marcantonio JM, Tomlinson J. Lens Calcium and cataract. In: Obrecht G, Lawrence WS, eds. Molecular Biology of the Lens. New York: Plenum Press; 1991;33-40.
49. Huang L, Grami V, Marrero Y, et al. Human lens phospholipid changes with age and cataract. Invest Ophthalmol Vis Sci. 2005; 46.1682-1689.
50. Mackay D, Ionides A, Berry V, et al. A new locus for dominant "zonular pulverulent" cataract, on chromosome 13. Am J Hum Genet. 1997;60:1474-1478.