L-Type Calcium Channels Play a Critical Role in Maintaining Lens Transparency by Regulating Phosphorylation of Aquaporin-0 and Myosin Light Chain and Expression of Connexins

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Maddala, Rupalatha ^a   Nagendran, Tharkika ^a   de Ridder, Gustaaf G ^a   Schey, Kevin L ^b   Rao, Ponugoti Vasantha ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AQUAPORIN; AQUAPORIN 0; BETA B1 CRYSTALLIN; BETA CRYSTALLIN; CALCIUM; CALCIUM CHANNEL L TYPE; COMPLEMENTARY DNA; CONNEXIN 46; CONNEXIN 50; FELODIPINE; FILENSIN; GAP JUNCTION PROTEIN; HEAT SHOCK PROTEIN 90; MYOSIN LIGHT CHAIN; NIFEDIPINE; PROTEIN 14 3 3; PROTEIN 14 3 3 EPSILON; SERINE; SPECTRIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DNA MICROARRAY; EPITHELIUM CELL; EX VIVO STUDY; FEMALE; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; LENS; LENS TRANSPARENCY; MALE; MASS SPECTROMETRY; MORPHOLOGY; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; AQUAPORINS; BETA-CRYSTALLIN B CHAIN; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS, L-TYPE; CONNEXINS; EYE PROTEINS; FELODIPINE; FEMALE; GENE EXPRESSION; IMMUNOBLOTTING; LENS, CRYSTALLINE; MALE; MICE; MICE, INBRED C57BL; MYOSIN LIGHT CHAINS; NIFEDIPINE; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84878437452     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064676     Document Type: Article

References (79)

1. Bassnett S, Shi Y, Vrensen GF, (2011) Biological glass: structural determinants of eye lens transparency. Philos Trans R Soc Lond B Biol Sci 366: 1250-1264.
2. Mathias RT, Kistler J, Donaldson P, (2007) The lens circulation. J Membr Biol 216: 1-16.
3. Lovicu FJ, McAvoy JW, (2005) Growth factor regulation of lens development. Dev Biol 280: 1-14.
4. Song S, Landsbury A, Dahm R, Liu Y, Zhang Q, et al. (2009) Functions of the intermediate filament cytoskeleton in the eye lens. J Clin Invest 119: 1837-1848.
5. Mathias RT, White TW, Gong X, (2010) Lens gap junctions in growth, differentiation, and homeostasis. Physiol Rev 90: 179-206.
6. Wistow GJ, Piatigorsky J, (1988) Lens crystallins: the evolution and expression of proteins for a highly specialized tissue. Annu Rev Biochem 57: 479-504.
7. Maddala R, Skiba NP, Lalane R, 3rd, Sherman DL, Brophy PJ, et al (2011) Periaxin is required for hexagonal geometry and membrane organization of mature lens fibers. Dev Biol 357: 179-190.
8. Straub BK, Boda J, Kuhn C, Schnoelzer M, Korf U, et al. (2003) A novel cell-cell junction system: the cortex adhaerens mosaic of lens fiber cells. J Cell Sci 116: 4985-4995.
9. Wang Z, Schey KL, (2011) Aquaporin-0 interacts with the FERM domain of ezrin/radixin/moesin proteins in the ocular lens. Invest Ophthalmol Vis Sci 52: 5079-5087.
10. More MI, Kirsch FP, Rathjen FG, (2001) Targeted ablation of NrCAM or ankyrin-B results in disorganized lens fibers leading to cataract formation. J Cell Biol 154: 187-196.
11. Ogawa Y, Rasband MN, (2008) The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol 18: 307-313.
12. Salzer JL, Brophy PJ, Peles E, (2008) Molecular domains of myelinated axons in the peripheral nervous system. Glia 56: 1532-1540.
13. Sherman DL, Brophy PJ, (2005) Mechanisms of axon ensheathment and myelin growth. Nat Rev Neurosci 6: 683-690.
14. Bennett V, Healy J, (2009) Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb Perspect Biol 1: a003012.
15. Alvarez JL, Petzhold D, Pankonien I, Behlke J, Kouno M, et al. (2010) Ahnak1 modulates L-type Ca(2+) channel inactivation of rodent cardiomyocytes. Pflugers Arch 460: 719-730.
16. Matza D, Flavell RA, (2009) Roles of Ca(v) channels and AHNAK1 in T cells: the beauty and the beast. Immunol Rev 231: 257-264.
17. Pankonien I, Alvarez JL, Doller A, Kohncke C, Rotte D, et al. (2011) Ahnak1 is a tuneable modulator of cardiac Ca(v)1.2 calcium channel activity. J Muscle Res Cell Motil 32: 281-290.
18. Shao Y, Czymmek KJ, Jones PA, Fomin VP, Akanbi K, et al. (2009) Dynamic interactions between L-type voltage-sensitive calcium channel Cav1.2 subunits and ahnak in osteoblastic cells. Am J Physiol Cell Physiol 296: C1067-1078.
19. Duncan G, Collison DJ, (2002) Calcium signalling in ocular tissues: functional activity of G-protein and tyrosine-kinase coupled receptors. Exp Eye Res 75: 377-389.
20. Rhodes JD, Sanderson J, (2009) The mechanisms of calcium homeostasis and signalling in the lens. Exp Eye Res 88: 226-234.
21. Duncan G, Jacob TJ, (1984) Calcium and the physiology of cataract. Ciba Found Symp 106: 132-152.
22. Truscott RJ, Marcantonio JM, Tomlinson J, Duncan G, (1990) Calcium-induced opacification and proteolysis in the intact rat lens. Invest Ophthalmol Vis Sci 31: 2405-2411.
23. Duncan G, Wormstone IM, (1999) Calcium cell signalling and cataract: role of the endoplasmic reticulum. Eye (Lond) 13 (Pt 3b): 480-483.
24. Sanderson J, Marcantonio JM, Duncan G, (2000) A human lens model of cortical cataract: Ca2+-induced protein loss, vimentin cleavage and opacification. Invest Ophthalmol Vis Sci 41: 2255-2261.
25. Nakamura Y, Fukiage C, Shih M, Ma H, David LL, et al. (2000) Contribution of calpain Lp82-induced proteolysis to experimental cataractogenesis in mice. Invest Ophthalmol Vis Sci 41: 1460-1466.
26. Shearer TR, Ma H, Fukiage C, Azuma M, (1997) Selenite nuclear cataract: review of the model. Mol Vis 3: 8.
27. Gao J, Sun X, Martinez-Wittinghan FJ, Gong X, White TW, et al. (2004) Connections between connexins, calcium, and cataracts in the lens. J Gen Physiol 124: 289-300.
28. Girsch SJ, Peracchia C, (1991) Calmodulin interacts with a C-terminus peptide from the lens membrane protein MIP26. Curr Eye Res 10: 839-849.
29. Gold MG, Reichow SL, O'Neill SE, Weisbrod CR, Langeberg LK, et al. (2012) AKAP2 anchors PKA with aquaporin-0 to support ocular lens transparency. EMBO Mol Med 4: 15-26.
30. Lampe PD, Bazzi MD, Nelsestuen GL, Johnson RG, (1986) Phosphorylation of lens intrinsic membrane proteins by protein kinase C. Eur J Biochem. 156: 351-357.
31. Lurtz MM, Louis CF, (2003) Calmodulin and protein kinase C regulate gap junctional coupling in lens epithelial cells. Am J Physiol Cell Physiol 285: C1475-1482.
32. Nemeth-Cahalan KL, Hall JE, (2000) pH and calcium regulate the water permeability of aquaporin 0. J Biol Chem 275: 6777-6782.
33. Nemeth-Cahalan KL, Kalman K, Hall JE, (2004) Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J Gen Physiol 123: 573-580.
34. Rose KM, Wang Z, Magrath GN, Hazard ES, Hildebrandt JD, et al. (2008) Aquaporin 0-calmodulin interaction and the effect of aquaporin 0 phosphorylation. Biochemistry 47: 339-347.
35. Varadaraj K, Kumari S, Shiels A, Mathias RT, (2005) Regulation of aquaporin water permeability in the lens. Invest Ophthalmol Vis Sci 46: 1393-1402.
36. Welsh MJ, Aster JC, Ireland M, Alcala J, Maisel H, (1982) Calmodulin binds to chick lens gap junction protein in a calcium-independent manner. Science 216: 642-644.
37. Aravind P, Mishra A, Suman SK, Jobby MK, Sankaranarayanan R, et al. (2009) The betagamma-crystallin superfamily contains a universal motif for binding calcium. Biochemistry 48: 12180-12190.
38. Cengiz M, Gurkaynak M, Atahan IL, Kilic K, Totan Y, (1999) The effect of verapamil in the prevention of radiation-induced cataract. Int J Radiat Oncol Biol Phys 43: 623-626.
39. Ettl A, Daxer A, Gottinger W, Schmid E, (2004) Inhibition of experimental diabetic cataract by topical administration of RS-verapamil hydrochloride. Br J Ophthalmol 88: 44-47.
40. Kametaka S, Kasahara T, Ueo M, Takenaka M, Saito M, et al. (2008) Effect of nifedipine on severe experimental cataract in diabetic rats. J Pharmacol Sci 106: 651-658.
41. Pierce GN, Afzal N, Kroeger EA, Lockwood MK, Kutryk MJ, et al. (1989) Cataract formation is prevented by administration of verapamil to diabetic rats. Endocrinology 125: 730-735.
42. Maddala R, Skiba N, Vasantha Rao P, (2007) Lens fiber cell elongation and differentiation is associated with a robust increase in myosin light chain phosphorylation in the developing mouse. Differentiation 75: 713-725.
43. Striessnig J, Bolz HJ, Koschak A, (2010) Channelopathies in Cav1.1, Cav1.3, and Cav1.4 voltage-gated L-type Ca2+ channels. Pflugers Arch 460: 361-374.
44. Tsien RW, Ellinor PT, Horne WA, (1991) Molecular diversity of voltage-dependent Ca2+ channels. Trends Pharmacol Sci 12: 349-354.
45. Catterall WA, (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3: a003947.
46. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J, (2005) International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57: 411-425.
47. Rampe D, Triggle DJ, (1990) New ligands for L-type Ca2+ channels. Trends Pharmacol Sci 11: 112-115.
48. Jiang JX, (2010) Gap junctions or hemichannel-dependent and independent roles of connexins in cataractogenesis and lens development. Curr Mol Med 10: 851-863.
49. Beguin P, Mahalakshmi RN, Nagashima K, Cher DH, Takahashi A, et al. (2005) 14-3-3 and calmodulin control subcellular distribution of Kir/Gem and its regulation of cell shape and calcium channel activity. J Cell Sci 118: 1923-1934.
50. Czirjak G, Vuity D, Enyedi P, (2008) Phosphorylation-dependent binding of 14-3-3 proteins controls TRESK regulation. J Biol Chem 283: 15672-15680.
51. Li Y, Wu Y, Zhou Y, (2006) Modulation of inactivation properties of CaV2.2 channels by 14-3-3 proteins. Neuron 51: 755-771.
52. Zuzarte M, Heusser K, Renigunta V, Schlichthorl G, Rinne S, et al. (2009) Intracellular traffic of the K+ channels TASK-1 and TASK-3: role of N- and C-terminal sorting signals and interaction with 14-3-3 proteins. J Physiol 587: 929-952.
53. Liang X, Da Paula AC, Bozoky Z, Zhang H, Bertrand CA, et al. (2012) Phosphorylation-dependent 14-3-3 protein interactions regulate CFTR biogenesis. Mol Biol Cell 23: 996-1009.
54. Liang X, Butterworth MB, Peters KW, Walker WH, Frizzell RA, (2008) An obligatory heterodimer of 14-3-3beta and 14-3-3epsilon is required for aldosterone regulation of the epithelial sodium channel. J Biol Chem 283: 27418-27425.
55. Somlyo AP, Somlyo AV, (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358.
56. Clapham DE, (2007) Calcium signaling. Cell 131: 1047-1058.
57. Ghosh A, Greenberg ME, (1995) Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science 268: 239-247.
58. Anderson ME, (2004) Calmodulin kinase and L-type calcium channels; a recipe for arrhythmias? Trends Cardiovasc Med 14: 152-161.
59. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME, (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294: 333-339.
60. Dai S, Hall DD, Hell JW, (2009) Supramolecular assemblies and localized regulation of voltage-gated ion channels. Physiol Rev 89: 411-452.
61. Trautwein W, Hescheler J, (1990) Regulation of cardiac L-type calcium current by phosphorylation and G proteins. Annu Rev Physiol 52: 257-274.
62. van Heyningen R, Harding JJ, (1986) Do aspirin-like analgesics protect against cataract? A case-control study. Lancet 1: 1111-1113.
63. Harding JJ, van Heyningen R, (1988) Drugs, including alcohol, that act as risk factors for cataract, and possible protection against cataract by aspirin-like analgesics and cyclopenthiazide. Br J Ophthalmol 72: 809-814.
64. Cekic O, Bardak Y, (1998) Lenticular calcium, magnesium, and iron levels in diabetic rats and verapamil effect. Ophthalmic Res 30: 107-112.
65. Devamanoharan PS, Varma SD, (1995) Inhibition of polyol formation in rat lens by verapamil. J Ocul Pharmacol Ther 11: 527-531.
66. Meissner A, Noack T, (2008) Proliferation of human lens epithelial cells (HLE-B3) is inhibited by blocking of voltage-gated calcium channels. Pflugers Arch 457: 47-59.
67. Kinoshita JH, (1974) Mechanisms initiating cataract formation. Proctor Lecture. Invest Ophthalmol 13: 713-724.
68. Reichow SL, Gonen T, (2008) Noncanonical binding of calmodulin to aquaporin-0: implications for channel regulation. Structure 16: 1389-1398.
69. Liu J, Xu J, Gu S, Nicholson BJ, Jiang JX, (2011) Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50. J Cell Sci 124: 198-206.
70. Yu XS, Jiang JX, (2004) Interaction of major intrinsic protein (aquaporin-0) with fiber connexins in lens development. J Cell Sci 117: 871-880.
71. Lichtstein D, McGowan MH, Russell P, Carper DA, (2000) Digitalis and digitalislike compounds down-regulate gene expression of the intracellular signaling protein 14-3-3 in rat lens. Hypertens Res 23Suppl: S51-53.
72. McGowan MH, Russell P, Carper DA, Lichtstein D, (1999) Na+, K+-ATPase inhibitors down-regulate gene expression of the intracellular signaling protein 14-3-3 in rat lens. J Pharmacol Exp Ther 289: 1559-1563.
73. Nguyen TA, Takemoto LJ, Takemoto DJ, (2004) Inhibition of gap junction activity through the release of the C1B domain of protein kinase Cgamma (PKCgamma) from 14-3-3: identification of PKCgamma-binding sites. J Biol Chem 279: 52714-52725.
74. Hund TJ, Koval OM, Li J, Wright PJ, Qian L, et al. (2010) A beta(IV)-spectrin/CaMKII signaling complex is essential for membrane excitability in mice. J Clin Invest 120: 3508-3519.
75. Seri M, Pecci A, Di Bari F, Cusano R, Savino M, et al. (2003) MYH9-related disease: May-Hegglin anomaly, Sebastian syndrome, Fechtner syndrome, and Epstein syndrome are not distinct entities but represent a variable expression of a single illness. Medicine (Baltimore) 82: 203-215.
76. Zhang Y, Conti MA, Malide D, Dong F, Wang A, et al. (2012) Mouse models of MYH9-related disease: mutations in nonmuscle myosin II-A. Blood 119: 238-250.
77. Rao PV, Maddala R, (2009) Abundant expression of ponsin, a focal adhesion protein, in lens and downregulation of its expression by impaired cytoskeletal signaling. Invest Ophthalmol Vis Sci 50: 1769-1777.
78. Ray R, de Ridder GG, Eu JP, Paton AW, Paton JC, et al. (2012) The Escherichia coli subtilase cytotoxin A subunit specifically cleaves cell-surface GRP78 protein and abolishes COOH-terminal-dependent signaling. J Biol Chem 287: 32755-32769.
79. Maddala R, Chauhan BK, Walker C, Zheng Y, Robinson ML, et al. (2011) Rac1 GTPase-deficient mouse lens exhibits defects in shape, suture formation, fiber cell migration and survival. Dev Biol 360: 30-43.