A new mouse model for stationary night blindness with mutant Slc24a1 explains the pathophysiology of the associated human disease

Human Molecular Genetics

Volumn 24, Issue 20, 2015, Pages 5915-5929

  Vinberg, Frans ^a   Wang, Tian ^b   Molday, Robert S ^c   Chen, Jeannie ^b   Kefalov, Vladimir J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CYCLIC GMP; MUTANT PROTEIN; SLC24A1 PROTEIN; SODIUM CALCIUM EXCHANGE PROTEIN; UNCLASSIFIED DRUG; POTASSIUM-DEPENDENT SODIUM-CALCIUM EXCHANGER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOSOMAL RECESSIVE INHERITANCE; CALCIUM HOMEOSTASIS; CONGENITAL BLINDNESS; CONGENITAL STATIONARY NIGHT BLINDNESS; CONTROLLED STUDY; FEMALE; LIGHT ADAPTATION; LIGHT EXPOSURE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PHOTORECEPTOR; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RETINA CONE; RETINA DEGENERATION; RETINA ROD OUTER SEGMENT; RETINITIS PIGMENTOSA; VISUAL DISORDER; ANIMAL; DISEASE MODEL; EYE DISEASE; GENE DELETION; GENETICS; METABOLISM; MYOPIA; NIGHT BLINDNESS; PHYSIOLOGY; RETINAL ROD OUTER SEGMENT; X CHROMOSOME LINKED DISORDER;

ANIMALS; CALCIUM; DISEASE MODELS, ANIMAL; EYE DISEASES, HEREDITARY; GENE DELETION; GENETIC DISEASES, X-LINKED; MICE; MYOPIA; NIGHT BLINDNESS; ROD CELL OUTER SEGMENT; SODIUM-CALCIUM EXCHANGER;

EID: 84943744248     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv319     Document Type: Article

References (84)

1. Farber, D.B. (1995) From mice to men: the cyclic GMP phosphodiesterase gene in vision and disease. The proctor lecture. Invest. Ophthalmol. Vis. Sci., 36, 263-275.
2. Sokal, I., Li, N., Surgucheva, I.,Warren, M.J., Payne, A.M., Bhattacharya, S.S., Baehr, W. and Palczewski, K. (1998) GCAP1 (Y99C) mutant is constitutively active in autosomal dominant cone dystrophy. Mol. Cell, 2, 129-133.
3. Rapp, L.M. and Williams, T.P. (1980) The role of ocular pigmentation in protecting against retinal light damage. Vision Res., 20, 1127-1131.
4. Dizhoor, A.M., Woodruff, M.L., Olshevskaya, E.V., Cilluffo, M. C., Cornwall, M.C., Sieving, P.A. and Fain, G.L. (2008) Night blindness and the mechanism of constitutive signaling of mutant G90D rhodopsin. J. Neurosci., 28, 11662-11672.
5. Dowling, J.E. and Wald, G. (1960) The biological function of Vitamin A acid. Proc. Natl Acad. Sci. USA, 46, 587-608.
6. Fan, J.,Woodruff, M.L., Cilluffo, M.C., Crouch, R.K. and Fain, G. L. (2005) Opsin activation of transduction in the rods of darkreared Rpe65 knockout mice. J. Physiol., 568, 83-95.
7. Redmond, T.M., Yu, S., Lee, E., Bok, D., Hamasaki, D., Chen, N., Goletz, P., Ma, J.X., Crouch, R.K. and Pfeifer, K. (1998) Rpe65 is necessary for production of 11-cis-vitamin A in the retinal visual cycle. Nat. Genet., 20, 344-351.
8. Fain, G.L. and Lisman, J.E. (1993) Photoreceptor degeneration in vitamin A deprivation and retinitis pigmentosa: the equivalent light hypothesis. Exp. Eye Res., 57, 335-340.
9. Chen, C.K., Burns, M.E., Spencer, M., Niemi, G.A., Chen, J., Hurley, J.B., Baylor, D.A. and Simon, M.I. (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc. Natl Acad. Sci. USA, 96, 3718-3722.
10. Chen, J., Simon, M.I., Matthes, M.T., Yasumura, D. and LaVail, M.M. (1999) Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest. Ophthalmol. Vis. Sci., 40, 2978-2982.
11. Fain, G.L. (2006) Why photoreceptors die (and why they don't). Bioessays, 28, 344-354.
12. Semple-Rowland, S.L., Lee, N.R., Van Hooser, J.P., Palczewski, K. and Baehr,W. (1998) A null mutation in the photoreceptor guanylate cyclase gene causes the retinal degeneration chicken phenotype. Proc. Natl Acad. Sci. USA, 95, 1271-1276.
13. Yang, R.B., Robinson, S.W., Xiong,W.H., Yau, K.W., Birch, D.G. and Garbers, D.L. (1999) Disruption of a retinal guanylyl cyclase gene leads to cone-specific dystrophy and paradoxical rod behavior. J. Neurosci., 19, 5889-5897.
14. Dryja, T.P., Finn, J.T., Peng, Y.W., McGee, T.L., Berson, E.L. and Yau, K.W. (1995) Mutations in the gene encoding the alpha subunit of the rod cGMP-gated channel in autosomal recessive retinitis pigmentosa. Proc. Natl Acad. Sci. USA, 92, 10177-10181.
15. Huttl, S., Michalakis, S., Seeliger, M., Luo, D.-G., Acar, N., Geiger, H., Hudl, K., Mader, R., Haverkamp, S., Moser, M. et al. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J. Neurosci., 25, 130-138.
16. Xu, J., Morris, L., Fliesler, S.J., Sherry, D.M. and Ding, X.-Q. (2011) Early-onset, slow progression of cone photoreceptor dysfunction and degeneration in CNG channel subunit CNGB3 deficiency. Invest. Ophthalmol. Vis. Sci., 52, 3557-3566.
17. Lisman, J. and Fain, G. (1995) Support for the equivalent light hypothesis for RP. Nat. Med., 1, 1254-1255.
18. Fain, G.L. and Lisman, J.E. (1999) Light, Ca2+, and photoreceptor death: new evidence for the equivalent-light hypothesis from arrestin knockout mice. Invest. Ophthalmol. Vis. Sci., 40, 2770-2772.
19. Schnetkamp, P.P., Jalloul, A.H., Liu, G. and Szerencsei, R.T. (2014) The SLC24 family of K(+)-dependent Na(+)-Ca(2)(+) exchangers: structure-function relationships. Curr. Top. Membr., 73, 263-287.
20. Sampath, A.P., Matthews, H.R., Cornwall, M.C. and Fain, G.L. (1998) Bleached pigment produces a maintained decrease in outer segment Ca2+ in salamander rods. J. Gen. Physiol., 111, 53-64.
21. Sampath, A.P., Matthews, H.R., Cornwall, M.C., Bandarchi, J. and Fain, G.L. (1999) Light-dependent changes in outer segment free-Ca2+ concentration in salamander cone photoreceptors. J. Gen. Physiol., 113, 267-277.
22. Gray-Keller, M.P. and Detwiler, P.B. (1994) The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron, 13, 849-861.
23. Nakatani, K. and Yau, K.W. (1988) Calcium and light adaptation in retinal rods and cones. Nature, 334, 69-71.
24. Matthews, H.R., Murphy, R.L., Fain, G.L. and Lamb, T.D. (1988) Photoreceptor light adaptation is mediated by cytoplasmic calcium concentration. Nature, 334, 67-69.
25. Arshavsky, V.Y. and Burns, M.E. (2012) Photoreceptor signaling: supporting vision across a wide range of light intensities. J. Biol. Chem., 287, 1620-1626.
26. Paquet-Durand, F., Beck, S., Michalakis, S., Goldmann, T., Huber, G., Muhlfriedel, R., Trifunovic, D., Fischer, M.D., Fahl, E., Duetsch, G. et al. (2011) A key role for cyclic nucleotide gated (CNG) channels in cGMP-related retinitis pigmentosa. Hum. Mol. Genet., 20, 941-947.
27. Woodruff, M.L., Olshevskaya, E.V., Savchenko, A.B., Peshenko, I.V., Barrett, R., Bush, R.A., Sieving, P.A., Fain, G.L. and Dizhoor, A.M. (2007) Constitutive excitation by Gly90Asp rhodopsin rescues rods from degeneration caused by elevated production of cGMP in the dark. J. Neurosci., 27, 8805-8815.
28. Riazuddin, S.A., Shahzadi, A., Zeitz, C., Ahmed, Z.M., Ayyagari, R., Chavali, V.R., Ponferrada, V.G., Audo, I., Michiels, C., Lancelot, M.E. et al. (2010) A mutation in SLC24A1 implicated in autosomal-recessive congenital stationary night blindness. Am. J. Hum. Genet., 87, 523-531.
29. Li, X.F., Kiedrowski, L., Tremblay, F., Fernandez, F.R., Perizzolo, M.,Winkfein, R.J., Turner, R.W., Bains, J.S., Rancourt, D.E. and Lytton, J. (2006) Importance of K+-dependent Na+/Ca2+-exchanger 2, NCKX2, in motor learning and memory. J. Biol. Chem., 281, 6273-6282.
30. Reid, D.M., Friedel, U., Molday, R.S. and Cook, N.J. (1990) Identification of the sodium-calcium exchanger as the major ricin-binding glycoprotein of bovine rod outer segments and its localization to the plasma membrane. Biochemistry, 29, 1601-1607.
31. Eisenfeld, A.J., Bunt-Milam, A.H. and Sarthy, P.V. (1984) Muller cell expression of glial fibrillary acidic protein after genetic and experimental photoreceptor degeneration in the rat retina. Invest. Ophthalmol. Vis. Sci., 25, 1321-1328.
32. Zhang, Y., Molday, L.L., Molday, R.S., Sarfare, S.S., Woodruff, M.L., Fain, G.L., Kraft, T.W. and Pittler, S.J. (2009) Knockout of GARPs and the beta-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J. Cell Sci., 122, 1192-1200.
33. Poetsch, A., Molday, L.L. and Molday, R.S. (2001) The cGMPgated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J. Biol. Chem., 276, 48009-48016.
34. Ardell, M.D., Makhija, A.K., Oliveira, L., Miniou, P., Viegas-Pequignot, E. and Pittler, S.J. (1995) cDNA, gene structure, and chromosomal localization of human GAR1 (CNCG3L), a homolog of the third subunit of bovine photoreceptor cGMP-gated channel. Genomics, 28, 32-38.
35. Colville, C.A. and Molday, R.S. (1996) Primary structure and expression of the human beta-subunit and related proteins of the rod photoreceptor cGMP-gated channel. J. Biol. Chem., 271, 32968-32974.
36. Chen, T.Y., Peng, Y.W., Dhallan, R.S., Ahamed, B., Reed, R.R. and Yau, K.W. (1993) A new subunit of the cyclic nucleotidegated cation channel in retinal rods. Nature, 362, 764-767.
37. Cook, N.J., Molday, L.L., Reid, D., Kaupp, U.B. and Molday, R.S. (1989) The cGMP-gated channel of bovine rod photoreceptors is localized exclusively in the plasma membrane. J. Biol. Chem., 264, 6996-6999.
38. Herrmann, R., Lobanova, E.S., Hammond, T., Kessler, C., Burns, M.E., Frishman, L.J. and Arshavsky, V.Y. (2010) Phosducin regulates transmission at the photoreceptor-to-ON-bipolar cell synapse. J. Neurosci., 30, 3239-3253.
39. Huttl, S., Michalakis, S., Seeliger, M., Luo, D.G., Acar, N., Geiger, H., Hudl, K., Mader, R., Haverkamp, S., Moser, M. et al. (2005) Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J. Neurosci., 25, 130-138.
40. Heikkinen, H., Nymark, S. and Koskelainen, A. (2008) Mouse cone photoresponses obtained with electroretinogram from the isolated retina. Vision Res., 48, 264-272.
41. Haynes, L.W., Kay, A.R. and Yau, K.W. (1986) Single cyclic GMP-activated channel activity in excised patches of rod outer segment membrane. Nature, 321, 66-70.
42. Zimmerman, A.L. and Baylor, D.A. (1986) Cyclic GMP-sensitive conductance of retinal rods consists of aqueous pores. Nature, 321, 70-72.
43. Ruiz, M., Brown, R.L., He, Y., Haley, T.L. and Karpen, J.W. (1999) The single-channel dose-response relation is consistently steep for rod cyclic nucleotide-gated channels: implications for the interpretation of macroscopic dose-response relations. Biochemistry, 38, 10642-10648.
44. Mendez, A., Burns, M.E., Sokal, I., Dizhoor, A.M., Baehr, W., Palczewski, K., Baylor, D.A. and Chen, J. (2001) Role of guanylate cyclase-activating proteins (GCAPs) in setting the flash sensitivity of rod photoreceptors. Proc. Natl Acad. Sci. USA, 98, 9948-9953.
45. Iwamoto, T.,Watano, T. and Shigekawa, M. (1996) A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1. J. Biol. Chem., 271, 22391-22397.
46. Altimimi, H.F., Szerencsei, R.T. and Schnetkamp, P.P. (2013) Functional and structural properties of the NCKX2 Na(+)-Ca (2+)/K (+) exchanger: a comparison with the NCX1 Na (+)/Ca (2+) exchanger. Adv. Exp. Med. Biol., 961, 81-94.
47. Bauer, P.J. and Drechsler, M. (1992) Association of cyclic GMPgated channels and Na(+)-Ca(2+)-K+ exchangers in bovine retinal rod outer segment plasma membranes. J. Physiol., 451, 109-131.
48. Schwarzer, A., Schauf, H. and Bauer, P.J. (2000) Binding of the cGMP-gated channel to the Na/Ca-K exchanger in rod photoreceptors. J. Biol. Chem., 275, 13448-13454.
49. Kang, K., Bauer, P.J., Kinjo, T.G., Szerencsei, R.T., Bonigk, W., Winkfein, R.J. and Schnetkamp, P.P. (2003) Assembly of retinal rod or cone Na(+)/Ca(2+)-K(+) exchanger oligomers with cGMP-gated channel subunits as probed with heterologously expressed cDNAs. Biochemistry, 42, 4593-4600.
50. Molday, R.S. and Molday, L.L. (1998) Molecular properties of the cGMP-gated channel of rod photoreceptors. Vision Res., 38, 1315-1323.
51. Cook, N.J. and Kaupp, U.B. (1988) Solubilization, purification, and reconstitution of the sodium-calcium exchanger from bovine retinal rod outer segments. J. Biol. Chem., 263, 11382-11388.
52. Reilander, H., Achilles, A., Friedel, U., Maul, G., Lottspeich, F. and Cook, N.J. (1992) Primary structure and functional expression of the Na/Ca,K-exchanger from bovine rod photoreceptors. EMBO J., 11, 1689-1695.
53. Schnetkamp, P.P. (1986) Sodium-calcium exchange in the outer segments of bovine rod photoreceptors. J. Physiol., 373, 25-45.
54. Field, G.D. and Rieke, F. (2002) Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron, 34, 773-785.
55. Sampath, A.P. and Rieke, F. (2004) Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron, 41, 431-443.
56. Schneeweis, D.M. and Schnapf, J.L. (1995) Photovoltage of rods and cones in themacaque retina. Science, 268, 1053-1056.
57. Ribelayga, C., Cao, Y. and Mangel, S.C. (2008) The circadian clock in the retina controls rod-cone coupling. Neuron, 59, 790-801.
58. Abd-El-Barr, M.M., Pennesi, M.E., Saszik, S.M., Barrow, A.J., Lem, J., Bramblett, D.E., Paul, D.L., Frishman, L.J. and Wu, S. M. (2009) Genetic dissection of rod and cone pathways in the dark-adapted mouse retina. J. Neurophysiol., 102, 1945-1955.
59. Chen, C.K., Burns, M.E., He,W.,Wensel, T.G., Baylor, D.A. and Simon, M.I. (2000) Slowed recovery of rod photoresponse in mice lacking the GTPase accelerating protein RGS9-1. Nature, 403, 557-560.
60. Baehr, W., Devlin, M.J. and Applebury, M.L. (1979) Isolation and characterization of cGMP phosphodiesterase from bovine rod outer segments. J. Biol. Chem., 254, 11669-11677.
61. Kolesnikov, A.V., Rikimaru, L., Hennig, A.K., Lukasiewicz, P.D., Fliesler, S.J., Govardovskii, V.I., Kefalov, V.J. and Kisselev, O.G. (2011) G-protein betagamma-complex is crucial for efficient signal amplification in vision. J. Neurosci., 31, 8067-8077.
62. Sokal, I., Li, N., Surgucheva, I.,Warren, M.J., Payne, A.M., Bhattacharya, S.S., Baehr, W. and Palczewski, K. (1998) GCAP1 (Y99C) mutant is constitutively active in autosomal dominant cone dystrophy. Mol. Cell, 2, 129-133.
63. Semple-Rowland, S.L., Lee, N.R., Van Hooser, J.P., Palczewski, K. and Baehr,W. (1998) A null mutation in the photoreceptor guanylate cyclase gene causes the retinal degeneration chicken phenotype. Proc. Natl Acad. Sci. USA, 95, 1271-1276.
64. Dryja, T.P., Finn, J.T., Peng, Y.W., McGee, T.L., Berson, E.L. and Yau, K.W. (1995) Mutations in the gene encoding the alpha subunit of the rod cGMP-gated channel in autosomal recessive retinitis pigmentosa. Proc. Natl Acad. Sci. USA, 92, 10177-10181.
65. Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Sparkes, R.L., Koop, B., Birch, D.G., Bergen, A.A., Prinsen, C.F., Polomeno, R. C., Gal, A. et al. (2000) Mutations in NYX, encoding the leucinerich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat. Genet., 26, 319-323.
66. Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B.,Weber, B.H., Wutz, K., Gutwillinger, N., Ruther, K., Drescher, B. et al. (1998) An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nat. Genet., 19, 260-263.
67. Audo, I., Kohl, S., Leroy, B.P., Munier, F.L., Guillonneau, X., Mohand-Said, S., Bujakowska, K., Nandrot, E.F., Lorenz, B., Preising, M. et al. (2009) TRPM1 is mutated in patients with autosomal-recessive complete congenital stationary night blindness. Am. J. Hum. Genet., 85, 720-729.
68. Dryja, T.P., Berson, E.L., Rao, V.R. and Oprian, D.D. (1993) Heterozygous missense mutation in the rhodopsin gene as a cause of congenital stationary night blindness. Nat. Genet., 4, 280-283.
69. Gal, A., Orth, U., Baehr, W., Schwinger, E. and Rosenberg, T. (1994) Heterozygous missense mutation in the rod cGMP phosphodiesterase beta-subunit gene in autosomal dominant stationary night blindness. Nat. Genet., 7, 551.
70. Dryja, T.P., Hahn, L.B., Reboul, T. and Arnaud, B. (1996) Missense mutation in the gene encoding the alpha subunit of rod transducin in the Nougaret form of congenital stationary night blindness. Nat. Genet., 13, 358-360.
71. Yamamoto, S., Sippel, K.C., Berson, E.L. and Dryja, T.P. (1997) Defects in the rhodopsin kinase gene in the Oguchi form of stationary night blindness. Nat. Genet., 15, 175-178.
72. Mattapallil, M.J., Wawrousek, E.F., Chan, C.C., Zhao, H., Roychoudhury, J., Ferguson, T.A. and Caspi, R.R. (2012) The Rd8 mutation of the Crb1 gene is present in vendor lines of C57BL/6N mice and embryonic stem cells, and confounds ocular induced mutant phenotypes. Invest. Ophthalmol. Vis. Sci., 53, 2921-2927.
73. Calvert, P.D., Krasnoperova, N.V., Lyubarsky, A.L., Isayama, T., Nicolo, M., Kosaras, B.,Wong, G., Gannon, K.S., Margolskee, R. F., Sidman, R.L. et al. (2000) Phototransduction in transgenic mice after targeted deletion of the rod transducin alpha -subunit. Proc. Natl Acad. Sci. USA, 97, 13913-13918.
74. Nikonov, S.S., Kholodenko, R., Lem, J. and Pugh, E.N. Jr. (2006) Physiological features of the S- and M-cone photoreceptors of wild-type mice from single-cell recordings. J. Gen. Physiol., 127, 359-374.
75. Chen, J., Woodruff, M.L., Wang, T., Concepcion, F.A., Tranchina, D. and Fain, G.L. (2010) Channel modulation and the mechanism of light adaptation in mouse rods. J. Neurosci., 30, 16232-16240.
76. Concepcion, F. and Chen, J. (2010) Q344ter mutation causes mislocalization of rhodopsin molecules that are catalytically active: a mouse model of Q344ter-induced retinal degeneration. PLoS One, 5, e10904.
77. MacKenzie, D., Arendt, A., Hargrave, P., McDowell, J.H. and Molday, R.S. (1984) Localization of binding sites for carboxyl terminal specific anti-rhodopsin monoclonal antibodies using synthetic peptides. Biochemistry, 23, 6544-6549.
78. Shi, G., Yau, K.W., Chen, J. and Kefalov, V.J. (2007) Signaling properties of a short-wave cone visual pigment and its role in phototransduction. J. Neurosci., 27, 10084-10093.
79. Zhu, X., Li, A., Brown, B.,Weiss, E.R., Osawa, S. and Craft, C.M. (2002) Mouse cone arrestin expression pattern: light induced translocation in cone photoreceptors. Mol. Vis., 8, 462-471.
80. Chan, S., Rubin,W.W., Mendez, A., Liu, X., Song, X., Hanson, S. M., Craft, C.M., Gurevich, V.V., Burns, M.E. and Chen, J. (2007) Functional comparisons of visual arrestins in rod photoreceptors of transgenic mice. Invest. Ophthalmol. Vis. Sci., 48, 1968-1975.
81. Hoyo, N.L., Lopez-Begines, S., Rosa, J.L., Chen, J. and Mendez, A. (2014) Functional EF-hands in neuronal calcium sensor GCAP2 determine its phosphorylation state and subcellular distribution in vivo, and are essential for photoreceptor cell integrity. PLoS Genet., 10, e1004480.
82. Umino, Y., Solessio, E. and Barlow, R.B. (2008) Speed, spatial, and temporal tuning of rod and cone vision in mouse. J. Neurosci., 28, 189-198.
83. Nymark, S., Haldin, C., Tenhu, H. and Koskelainen, A. (2006) A new method for measuring free drug concentration: retinal tissue as a biosensor. Invest. Ophthalmol. Vis. Sci., 47, 2583-2588.
84. Vinberg, F., Kolesnikov, A.V. and Kefalov, V.J. (2014) Ex vivo ERG analysis of photoreceptors using an in vivo ERG system. Vision Res., 101, 108-117.