CNGA3 achromatopsia-associated mutation potentiates the phosphoinositide sensitivity of cone photoreceptor CNG channels by altering intersubunit interactions

American Journal of Physiology - Cell Physiology

Volumn 305, Issue 2, 2013, Pages

  Dai, Gucan ^a   Varnum, Michael D ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Achromatopsia; cAMP; cGMP; Channel; CLZ; CNG; Phosphoinositide; PIP2; PIP3

Indexed keywords

CYCLIC AMP; CYCLIC GMP; CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL A3; ENHANCED GREEN FLUORESCENT PROTEIN; LEUCINE; PHOSPHATIDYLINOSITIDE; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; COLOR BLINDNESS; CONCENTRATION RESPONSE; DISEASE ASSOCIATION; DISEASE COURSE; HETEROLOGOUS EXPRESSION; IN VITRO STUDY; LINKAGE ANALYSIS; MEMBRANE ELECTROPHYSIOLOGY; MUTANT; MUTATION; NONHUMAN; PATCH CLAMP; PHOTORECEPTOR OUTER SEGMENT; PRIORITY JOURNAL; RETINA CONE; THERMODYNAMICS; WILD TYPE;

ACHROMATOPSIA; CAMP; CGMP; CHANNEL; CLZ; CNG; PHOSPHOINOSITIDE; PIP2; PIP3;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CELL MEMBRANE; COLOR VISION DEFECTS; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; GENE EXPRESSION REGULATION; HUMANS; MUTAGENESIS, SITE-DIRECTED; OOCYTES; PHOSPHATIDYLINOSITOLS; POINT MUTATION; PROTEIN SUBUNITS; RETINAL CONE PHOTORECEPTOR CELLS; XENOPUS LAEVIS;

EID: 84880161274     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00037.2013     Document Type: Article

References (72)

1. Biel M, Michalakis S. Function and dysfunction of CNG channels: insights from channelopathies and mouse models. Mol Neurobiol 35: 266-277, 2007.
2. Bönigk W, Altenhofen W, Müller F, Dose A, Illing M, Molday RS, Kaupp UB. Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron 10: 865-877, 1993.
3. Brady JD, Rich ED, Martens JR, Karpen JW, Varnum MD, Brown RL. Interplay between PIP3 and calmodulin regulation of olfactory cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 103: 15635-15640, 2006.
4. Bright SR, Rich ED, Varnum MD. Regulation of human cone cyclic nucleotide-gated channels by endogenous phospholipids and exogenously applied phosphatidylinositol 3,4,5-trisphosphate. Mol Pharmacol 71: 176-183, 2007.
5. Burns ME, Arshavsky VY. Beyond counting photons: trials and trends in vertebrate visual transduction. Neuron 48: 387-401, 2005.
6. Chen SK, Ko GYP, Dryer SE. Somatostatin peptides produce multiple effects on gating properties of native cone photoreceptor cGMP-gated channels that depend on circadian phase and previous illumination. J Neurosci 27: 12168-12175, 2007. 6a. Cioffi DL, Rich TC. Feedback regulation of cone cyclic nucleotide channels by phosphoinositides. Focus on "CNGA3 achromatopsia-associated mutation potentiates the phosphoinositide sensitivity of cone photoreceptor CNG channels by altering intersubunit interactions. " Am J Physiol Cell Physiol (May 15, 2013). doi:10.1152/ajpcell.00136.2013.
7. Cioffi DL, Rich TC. Feedback regulation of cone cyclic nucleotide channels by phosphoinositides. Focus on "CNGA3 achromatopsia-associated mutation potentiates the phosphoinositide sensitivity of cone photoreceptor CNG channels by altering intersubunit interactions. " Am J Physiol Cell Physiol (May 15). doi:10.1152/ajpcell.00136.2013. 2013
8. Craven KB, Olivier NB, Zagotta WN. C-terminal movement during gating in cyclic nucleotide-modulated channels. J Biol Chem 283: 14728-14738, 2008.
9. Dai G, Peng C, Liu C, Varnum MD. Two structural components in CNGA3 support regulation of cone CNG channels by phosphoinositides. J Gen Physiol 141: 413-430, 2013.
10. Ding XQ, Matveev A, Singh A, Komori N, Matsumoto H. Biochemical characterization of cone cyclic nucleotide-gated (CNG) channel using the infrared fluorescence detection system. Adv Exp Med Biol 723: 769-775, 2012.
11. Fain GL, Matthews HR, Cornwall MC, Koutalos Y. Adaptation in vertebrate photoreceptors. Physiol Rev 81: 117-151, 2001.
12. Fesenko EE, Kolesnikov SS, Lyubarsky AL. Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313: 310-313, 1985.
13. Flynn GE, Black KD, Islas LD, Sankaran B, Zagotta WN. Structure and rearrangements in the carboxy-terminal region of SpIH channels. Structure 15: 671-682, 2007.
14. Flynn GE, Johnson JP Jr, Zagotta WN. Cyclic nucleotide-gated channels: shedding light on the opening of a channel pore. Nat Rev Neurosci 2: 643-651, 2001.
15. Gamper N, Shapiro MS. Regulation of ion transport proteins by membrane phosphoinositides. Nat Rev Neurosci 8: 921-934, 2007.
16. Gerstner A, Zong X, Hofmann F, Biel M. Molecular cloning and functional characterization of a new modulatory cyclic nucleotide-gated channel subunit from mouse retina. J Neurosci 20: 1324-1332, 2000.
17. Golebiewska U, Nyako M, Woturski W, Zaitseva I, McLaughlin S. Diffusion coefficient of fluorescent phosphatidylinositol 4,5-bisphosphate in the plasma membrane of cells. Mol Biol Cell 19: 1663-1669, 2008.
18. Gordon SE, Downing-Park J, Zimmerman AL. Modulation of the cGMP-gated ion channel in frog rods by calmodulin and an endogenous inhibitory factor. J Physiol 486: 533-546, 1995.
19. Goto-Omoto S, Hayashi T, Gekka T, Kubo A, Takeuchi T, Kitahara K. Compound heterozygous CNGA3 mutations (R436W, L633P) in a Japanese patient with congenital achromatopsia. Vis Neurosci 23: 395-402, 2006.
20. Grunwald ME, Zhong H, Lai J, Yau KW. Molecular determinants of the modulation of cyclic nucleotide-activated channels by calmodulin. Proc Natl Acad Sci USA 96: 13444-13449, 1999.
21. Guido ME, Garbarino Pico E, Caputto BL. Circadian regulation of phospholipid metabolism in retinal photoreceptors and ganglion cells. J Neurochem 76: 835-845, 2001.
22. Gustina AS, Trudeau MC. hERG potassium channel gating is mediated by N-and C-terminal region interactions. J Gen Physiol 137: 315-325, 2011.
23. Hackos DH, Korenbrot JI. Calcium modulation of ligand affinity in the cyclic GMP-gated ion channels of cone photoreceptors. J Gen Physiol 110: 515-528, 1997.
24. Hardie RC, Raghu P, Moore S, Juusola M, Baines RA, Sweeney ST. Calcium influx via TRP channels is required to maintain PIP2 levels in Drosophila photoreceptors. Neuron 30: 149-159, 2001.
25. Haynes LW, Stotz SC. Modulation of rod, but not cone, cGMP-gated photoreceptor channels by calcium-calmodulin. Vis Neurosci 14: 233-239, 1997.
26. Hilgemann DW. Local PIP2 signals: when, where, how? Pflügers Arch 455: 55-67, 2007.
27. Hsu YT, Molday RS. Modulation of the cGMP-gated channel of rod photoreceptor cells by calmodulin. Nature 361: 76-79, 1993.
28. Ivanovic I, Anderson RE, Le YZ, Fliesler SJ, Sherry DM, Rajala RV. Deletion of the p85alpha regulatory subunit of phosphoinositide 3-kinase in cone photoreceptor cells results in cone photoreceptor degeneration. Invest Ophthalmol Vis Sci 52: 3775-3783, 2011.
29. Jan LY, Jan YN. A superfamily of ion channels. Nature 345: 672, 1990.
30. Kaupp UB, Niidome T, Tanabe T, Terada S, Bönigk W, Stühmer W, Cook NJ, Kangawa K, Matsuo H, Hirose T. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342: 762-766, 1989.
31. Kaupp UB, Seifert R. Cyclic nucleotide-gated ion channels. Physiol Rev 82: 769-824, 2002.
32. Kusch J, Zimmer T, Holschuh J, Biskup C, Schulz E, Nache V, Benndorf K. Role of the S4-S5 linker in CNG channel activation. Biophys J 99: 2488-2496, 2010.
33. Li G, Rajala A, Wiechmann AF, Anderson RE, Rajala RVS. Activation and membrane binding of retinal protein kinase Balpha/Akt1 is regulated through light-dependent generation of phosphoinositides. J Neurochem 107: 1382-1397, 2008.
34. Liu C, Varnum MD. Functional consequences of progressive cone dystrophy-associated mutations in the human cone photoreceptor cyclic nucleotide-gated channel CNGA3 subunit. Am J Physiol Cell Physiol 289: C187-C198, 2005.
35. + channel. Science 309: 897-903, 2005.
36. MacArthur MW, Thornton JM. Influence of proline residues on protein conformation. J Mol Biol 218: 397-412, 1991.
37. + channel subunits does not ensure the stoichiometry of expressed channels. Biophys J 63: 1406-1411, 1992.
38. Michalakis S, Zong X, Becirovic E, Hammelmann V, Wein T, Wanner KT, Biel M. The glutamic acid-rich protein is a gating inhibitor of cyclic nucleotide-gated channels. J Neurosci 31: 133-141, 2011.
39. + channel deactivation gating from the solution structure of the EAG domain. J Biol Chem 286: 6184-6191, 2011.
40. Nelson DL, Cox MM. Lehninger Principles of Biochemistry (5th ed). New York: W. H. Freeman, 2008.
41. Nishiguchi KM, Sandberg MA, Gorji N, Berson EL, Dryja TP. Cone cGMP-gated channel mutations and clinical findings in patients with achromatopsia, macular degeneration, and other hereditary cone diseases. Hum Mutat 25: 248-258, 2005.
42. Peng C, Rich ED, Thor CA, Varnum MD. Functionally important calmodulin-binding sites in both NH2-and COOH-terminal regions of the cone photoreceptor cyclic nucleotide-gated channel CNGB3 subunit. J Biol Chem 278: 24617-24623, 2003.
43. Peng C, Rich ED, Varnum MD. Achromatopsia-associated mutation in the human cone photoreceptor cyclic nucleotide-gated channel CNGB3 subunit alters the ligand sensitivity and pore properties of heteromeric channels. J Biol Chem 278: 34533-34540, 2003.
44. Peng C, Rich ED, Varnum MD. Subunit configuration of heteromeric cone cyclic nucleotide-gated channels. Neuron 42: 401-410, 2004.
45. Pugh EN Jr, Nikonov S, Lamb TD. Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9: 410-418, 1999.
46. Rajala RVS. Phosphoinositide 3-kinase signaling in the vertebrate retina. J Lipid Res 51: 4-22, 2010.
47. Rattner A, Sun H, Nathans J. Molecular genetics of human retinal disease. Annu Rev Genet 33: 89-131, 1999.
48. Rebrik TI, Botchkina I, Arshavsky VY, Craft CM, Korenbrot JI. CNGmodulin: a novel Ca-dependent modulator of ligand sensitivity in cone photoreceptor cGMP-gated ion channels. J Neurosci 32: 3142-3153, 2012.
49. 2+-dependent modulation of cGMP-gated ion channels is detectable in cones but not in rods. J Gen Physiol 123: 63-75, 2004.
50. Reuter P, Koeppen K, Ladewig T, Kohl S, Baumann B, Wissinger B. Mutations in CNGA3 impair trafficking or function of cone cyclic nucleotidegated channels, resulting in achromatopsia. Hum Mutat 29: 1228-1236, 2008.
51. Rosenbaum T, Gordon SE. Dissecting intersubunit contacts in cyclic nucleotide-gated ion channels. Neuron 33: 703-713, 2002.
52. Sakmann B, Neher E (Eds.). Single-Channel Recording (2nd ed). New York: Plenum, 1995.
53. Shuart NG, Haitin Y, Camp SS, Black KD, Zagotta WN. Molecular mechanism for 3:1 subunit stoichiometry of rod cyclic nucleotide-gated ion channels. Nat Commun 2: 457, 2011.
54. Simunovic MP, Moore AT. The cone dystrophies. Eye (Lond) 12: 553-565, 1998.
55. Suh BC, Hille B. PIP2 is a necessary cofactor for ion channel function: how and why? Annu Rev Biophys 37: 175-195, 2008.
56. Sundin OH, Yang JM, Li Y, Zhu D, Hurd JN, Mitchell TN, Silva ED, Maumenee IH. Genetic basis of total colourblindness among the Pingelapese islanders. Nat Genet 25: 289-293, 2000.
57. Taraska JW, Puljung MC, Olivier NB, Flynn GE, Zagotta WN. Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nat Methods 6: 532-537, 2009.
58. Trudeau MC, Zagotta WN. Mechanism of calcium/calmodulin inhibition of rod cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 99: 8424-8429, 2002.
59. Trudeau MC, Zagotta WN. Calcium/calmodulin modulation of olfactory and rod cyclic nucleotide-gated ion channels. J Biol Chem 278: 18705-18708, 2003.
60. Tytgat J, Hess P. Evidence for cooperative interactions in potassium channel gating. Nature 359: 420-423, 1992.
61. Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70: 535-602, 2001.
62. Varnum MD, Black KD, Zagotta WN. Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels. Neuron 15: 619-625, 1995.
63. Varnum MD, Zagotta WN. Interdomain interactions underlying activation of cyclic nucleotide-gated channels. Science 278: 110-113, 1997.
64. Wall-Lacelle S, Hossain MI, Sauvé R, Blunck R, Parent L. Double mutant cycle analysis identified a critical leucine residue in the IIS4S5 linker for the activation of the Ca(V)2.3 calcium channel. J Biol Chem 286: 27197-27205, 2011.
65. Wissinger B, Gamer D, Jägle H, Giorda R, Marx T, Mayer S, Tippmann S, Broghammer M, Jurklies B, Rosenberg T, Jacobson SG, Sener EC, Tatlipinar S, Hoyng CB, Castellan C, Bitoun P, Andreasson S, Rudolph G, Kellner U, Lorenz B, Wolff G, Verellen-Dumoulin C, Schwartz M, Cremers FP, Apfelstedt-Sylla E, Zrenner E, Salati R, Sharpe LT, Kohl S. CNGA3 mutations in hereditary cone photoreceptor disorders. Am J Hum Genet 69: 722-737, 2001.
66. Womack KB, Gordon SE, He F, Wensel TG, Lu CC, Hilgemann DW. Do phosphatidylinositides modulate vertebrate phototransduction? J Neurosci 20: 2792-2799, 2000.
67. Yu WP, Grunwald ME, Yau KW. Molecular cloning, functional expression and chromosomal localization of a human homolog of the cyclic nucleotide-gated ion channel of retinal cone photoreceptors. FEBS Lett 393: 211-215, 1996.
68. Zheng J, Trudeau MC, Zagotta WN. Rod cyclic nucleotide-gated channels have a stoichiometry of three CNGA1 subunits and one CNGB1 subunit. Neuron 36: 891-896, 2002.
69. 2+-calmodulin modulation of cyclic nucleotidegated channels. J Neurosci 23: 8167-8175, 2003.
70. Zhong H, Lai J, Yau KW. Selective heteromeric assembly of cyclic nucleotidegated channels. Proc Natl Acad Sci USA 100: 5509-5513, 2003.
71. Zhong H, Molday LL, Molday RS, Yau KW. The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 420: 193-198, 2002.
72. Zhou L, Siegelbaum SA. Gating of HCN channels by cyclic nucleotides: residue contacts that underlie ligand binding, selectivity, and efficacy. Structure 15: 655-670, 2007.