Molecular cloning and functional characterization of a new modulatory cyclic nucleotide-gated channel subunit from mouse retina

Journal of Neuroscience

Volumn 20, Issue 4, 2000, Pages 1324-1332

  Gerstner, Andrea ^a   Zong, Xiangang ^a   Hofmann, Franz ^a   Biel, Martin ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Cation channel; Cone photoreceptor; Cyclic nucleotide; L cis diltiazem; Single channel recording

Indexed keywords

CALCIUM ION; CATION; CATION CHANNEL; COMPLEMENTARY DNA; CYCLIC NUCLEOTIDE; DILTIAZEM; ION CHANNEL; MESSENGER RNA;

AMINO ACID SEQUENCE; ARTICLE; EMBRYO; HUMAN; HUMAN CELL; MOLECULAR CLONING; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETINA;

EID: 0034652101     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-04-01324.2000     Document Type: Article

References (52)

1. Ardell MD, Aragon I, Oliveira L, Porche GE, Burke E, Pittler SJ (1996) The β subunit of human rod photoreceptor cGMP-gated cation channel is generated from a complex transcription unit. FEBS Lett 389:213-218.
2. Barnstable CJ, Wei JY (1995) Isolation and characterization of the α-subunit of the rat rod photoreceptor cGMP-gated cation channel. J Mol Neurosci 6:289-302.
3. Baylor D (1996) How photons start vision. Proc Natl Acad Sci USA 93:560-565.
4. Biel M, Zong X, Distler M, Bosse E, Klugbauer N, Murakami M, Flockerzi V, Hofmann F (1994) Another member of the cyclic nucleotide-gated channel family, expressed in testis, kidney, and heart. Proc Natl Acad Sci USA 91:3505-3509.
5. Biel M, Zong X, Ludwig A, Sautter A, Hofmann F (1996) Molecular cloning and expression of a modulatory subunit of the cyclic nucleotide-gated cation channel. J Biol Chem 271:6349-6355.
6. Biel M, Zong X, Ludwig A, Sautter A, Hofmann F (1999a) Structure and function of cyclic nucleotide-gated channels. Rev Physiol Biochem Pharmacol 135:151-171.
7. Biel M, Seeliger M, Pfeiffer A, Kohler K, Gerstner A, Ludwig A, Jaissle G, Fauser S, Zrenner E, Hofmann F (1999b) Selective loss of cone function in mice lacking the cyclic nucleotide-gated channel CNG3. Proc Natl Acad Sci USA 96:7553-7557.
8. Bönigk W, Altenhofen W, Müller F, Dose A, Illing M, Molday RS, Kaupp UB (1993) Rod and cone photoreceptor cells express distinct genes for cGMP-gated channels. Neuron 10:865-877.
9. Bönigk W, Bradley J, Müller F, Sesti F, Boekhoff I, Ronnett GV, Kaupp UB, Frings S (1999) The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. J Neurosci 19:5332-5347.
10. Bradley J, Li J, Davidson N, Lester HA, Zinn K (1994) Heteromeric olfactory cyclic nucleotide-gated channels: a new subunit that confers increased sensitivity to cAMP. Proc Natl Acad Sci USA 91:8890-8894.
11. Carter-Dawson LD, LaVail MM (1979) Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245-276.
12. Chen TY, Peng YW, Dhallan RS, Ahamed B, Reed RR, Yau KW (1993) A new subunit of the cyclic nucleotide-gated cation channel in retinal rods. Nature 362:764-767.
13. Colville CA, Molday RS (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.
14. Dhallan RS, Yau KW, Schrader KA, Reed RR (1990) Primary structure and functional expression of a cyclic nucleotide-activated channel from olfactory neurons. Nature 347:184-187.
15. Eismann E, Müller F, Heinemann SH, Kaupp UB (1994) A single negative charge within the pore region of a cGMP-gated channel controls rectification, Ca2+ blockage, and ionic selectivity. Proc Natl Acad Sci USA 91:1109-1113.
16. Finn JT, Grunwald ME, Yau KW (1996) Cyclic nucleotide-gated ion channels: an extended family with diverse functions. Annu Rev Physiol 58:395-426.
17. 2+ in cyclic nucleotide-gated channels. Proc Natl Acad Sci USA 92:10222-10226.
18. Grunwald ME, Yu WP, Yu HH, Yau KW (1998) Identification of a domain on the β-subunit of the rod cGMP-gated cation channel that mediates inhibition by calcium-calmodulin. J Biol Chem 273:9148-9157.
19. Haynes LW (1992) Block of the cyclic GMP-gated channel of vertebrate rod and cone photoreceptors by 1-cis-diltiazem. J Gen Physiol 100:783-801.
20. Haynes LW, Yau KW (1985) Cyclic GMP-sensitive conductance in outer segment membrane of catfish cones. Nature 317:61-64.
21. Haynes LW, Yau KW (1990) Single-channel measurement from the cyclic GMP-activated conductance of catfish retinal cones. J Physiol (Lond) 429:451-481.
22. Kaupp UB, Niidome T, Tanabe T, Terada S, Bönigk W, Stühmer W, Cook NJ, Kangawa K, Matsuo H, Hirose T, Miyata T, Numa S (1989) Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature 342:762-766.
23. Kohl S, Marx T, Giddings I, Jagle H, Jacobson SG, Apfelstedt SE, Zrenner E, Sharpe LT, Wissinger B (1998) Total colour blindness is caused by mutations in the gene encoding the alpha-subunit of the cone photoreceptor cGMP-gated cation channel. Nat Genet 19:257-259.
24. Körschen HG, Illing M, Seifert R, Sesti F, Williams A, Gotzes S, Colville C, Müller F, Dose A, Godde M, Molday L, Kaupp UB, Molday RS (1995) A 240 kDa protein represents the complete β subunit of the cyclic nucleotide-gated channel from rod photoreceptor. Neuron 15:627-636.
25. Körschen HG, Beyermann M, Müller F, Heck M, Vantler M, Koch KW, Kellner R, Wolfrum U, Bode C, Hofmann KP, Kaupp UB (1999) Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature 400:761-766.
26. Kusaka S, Dabin I, Barnstable CJ, Puro DG (1996) cGMP-mediated effects on the physiology of bovine and human retinal Müller (glial) cells. J Physiol (Lond) 497:725-729.
27. Liman ER, Buck LB (1994) A second subunit of the olfactory cyclic nucleotide-gated channel confers high sensitivity to cAMP. Neuron 13:611-621.
28. Liu DT, Tibbs GR, Siegelbaum SA (1996) Subunit stoichiometry of cyclic nucleotide-gated channels and effects of subunit order on channel function. Neuron 16:983-990.
29. Liu M, Chen TY, Ahamed B, Li J, Yau KW (1994) Calcium-calmodulin modulation of the olfactory cyclic nucleotide-gated cation channel. Science 266:1348-1354.
30. Ludwig A, Flockerzi V, Hofmann F (1997) Regional expression and cellular localization of the α1 and β subunits of high voltage-activated calcium channels in rat brain. J Neurosci 17:1339-1349.
31. Ludwig J, Margalit T, Eismann E, Lancet D, Kaupp UB (1990) Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett 270:24-29.
32. Nawy S, Jahr CE (1990) Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346:269-271.
33. Paoletti P, Young EC, Siegelbaum SA (1999) C-Linker of cyclic nucleotide-gated channels controls coupling of ligand binding to channel gating. J Gen Physiol 113:17-34.
34. Picones A, Korenbrot JI (1994) Analysis of fluctuations in the cGMP-dependent current of cone photoreceptor outer segments. Biophys J 66:360-365.
35. Picones A, Korenbrot JI (1995) Spontaneous, ligand-independent activity of the cGMP-gated ion channels in cone photoreceptors of fish. J Physiol (Lond) 485:699-714.
36. Pittler SJ, Lee AK, Altherr MR, Howard TA, Seldin MF, Hurwitz RL, Wasmuth JJ, Baehr W (1992) Primary structure and chromosomal localization of human and mouse rod photoreceptor cGMP-gated cation channel. J Biol Chem 267:6257-6262.
37. Quandt FN, Nicol GD, Schnetkamp PP (1991) Voltage-dependent gating and block of the cyclic-GMP-dependent current in bovine rod outer segments. Neuroscience 42:629-638.
38. Root MJ, MacKinnon R (1993) Identification of an external divalent cation-binding site in the pore of a cGMP-activated channel. Neuron 11:459-466.
39. Sautter A, Biel M, Hofmann F (1997) Molecular cloning of cyclic nucleotide-gated cation channel subunits from rat pineal gland. Brain Res Mol Brain Res. 48:171-175.
40. Sautter A, Zong X, Hofmann F, Biel M (1998) An isoform of the rod photoreceptor cyclic nucleotide-gated channel beta subunit expressed in olfactory neurons. Proc Natl Acad Sci USA 95:4696-4701.
41. Schild D, Restrepo D (1998) Transduction mechanisms in vertebrate olfactory receptor cells. Physiol Rev 78:429-466.
42. Shammat IM, Gordon SE (1999) Stoichiometry and arrangement of subunits in rod cyclic nucleotide-gated channels. Neuron 23:809-819.
43. Shiells RA, Falk G (1992) Properties of the cGMP-activated channel of retinal on-bipolar cells. Proc R Soc Lond B Biol Sci 247:21-25.
44. Stern JH, Kaupp UB, MacLeish PR (1986) Control of the light-regulated current in rod photoreceptors by cyclic GMP, calcium, and 1-cis-diltiazem. Proc Natl Acad Sci USA 83:1163-1167.
45. Sugimoto Y, Yatsunami K, Tsujimoto M, Khorana HG, Ichikawa A (1991) The amino acid sequence of a glutamic acid-rich protein from bovine retina as deduced from the cDNA sequence. Proc Natl Acad Sci USA 88:3116-3119.
46. Tibbs GR, Goulding EH, Siegelbaum SA (1997) Allosteric activation and tuning of ligand efficacy in cyclic-nucleotide-gated channels. Nature 386:612-615.
47. Weitz D, Zoche M, Müller F, Beyermann M, Körschen HG, Kaupp UB, Koch KW (1998) Calmodulin controls the rod photoreceptor CNG channel through an unconventional binding site in the N-terminus of the β-subunit. EMBO J 17:2273-2284.
48. Weyand I, Godde M, Frings S, Weiner J, Müller F, Altenhofen W, Hatt H, Kaupp UB (1994) Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature 368:859-863.
49. Wheater PR, Burkitt HG, Daniels VG (1987) Functional histology, a text and colour atlas. New York: Churchill Livingstone.
50. 2+ entry into sperm. J Cell Biol 142:473-484.
51. Yu WP, Grunwald ME, Yau KW (1996) 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.
52. Zong X, Zucker H, Hofmann F, Biel M (1998) Three amino acids in the C-linker are major determinants of gating in cyclic nucleotide-gated channels. EMBO J 17:353-362.