Skip to main content
Log in

Involvement of rhodopsin and ATP in the activation of membranous guanylate cyclase in retinal photoreceptor outer segments (ROS-GC) by GC-activating proteins (GCAPs): a new model for ROS-GC activation and its link to retinal diseases

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Membranous guanylate cyclase in retinal photoreceptor outer segments (ROS-GC), a key enzyme for the recovery of photoreceptors to the dark state, has a topology identical to and cytoplasmic domains homologous to those of peptide-regulated GCs. However, under the prevailing concept, its activation mechanism is significantly different from those of peptide-regulated GCs: GC-activating proteins (GCAPs) function as the sole activator of ROS-GC in a Ca2+-sensitive manner, and neither reception of an outside signal by the extracellular domain (ECD) nor ATP binding to the kinase homology domain (KHD) is required for its activation. We have recently shown that ATP pre-binding to the KHD in ROS-GC drastically enhances its GCAP-stimulated activity, and that rhodopsin illumination, as the outside signal, is required for the ATP pre-binding. These results indicate that illuminated rhodopsin is involved in ROS-GC activation in two ways: to initiate ATP binding to ROS-GC for preparation of its activation and to reduce [Ca2+] through activation of cGMP phosphodiesterase. These two signal pathways are activated in a parallel and proportional manner and finally converge for strong activation of ROS-GC by Ca2+-free GCAPs. These results also suggest that the ECD receives the signal for ATP binding from illuminated rhodopsin. The ECD is projected into the intradiscal space, i.e., an intradiscal domain(s) of rhodopsin is also involved in the signal transfer. Many retinal disease-linked mutations are found in these intradiscal domains; however, their consequences are often unclear. This model will also provide novel insights into causal relationship between these mutations and certain retinal diseases.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Baylor DA (1987) Photoreceptor signals and vision. Invest Ophthalmol Vis Sci 28:34–49

    CAS  PubMed  Google Scholar 

  2. Miller WH (1990) Dark mimic. Invest Ophthalmol Vis Sci 31:1664–1673

    Google Scholar 

  3. Nakatani K, Chen C, Yau KW, Koutalos Y (2002) Calcium and phototransduction. Adv Exp Med Biol 514:1–20

    CAS  PubMed  Google Scholar 

  4. Shyjan AW, de Sauvage FJ, Gillett NA, Goeddel DV, Low DG (1992) Molecular cloning of a retina-specific membrane guanylyl cyclase. Neuron 9:727–737

    CAS  PubMed  Google Scholar 

  5. Goraczniak RM, Duda T, Sitaramayya A, Sharma RK (1994) Structure and functional characterization of the rod outer segment membranes guanylate cyclase. Biochem J 302:455–461

    CAS  PubMed  Google Scholar 

  6. Yang RB, Foster DC, Garbers DL, Fulle HJ (1995) Two membrane forms of guanylyl cyclase found in the eye. Proc Natl Acad Sci USA 92:602–606

    CAS  PubMed  Google Scholar 

  7. Lowe DG, Dizhoor AM, Liu K, Gu O, Laura R, Lu L, Hurley JB (1995) Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC-2. Proc Natl Acad Sci USA 92:5535–5539

    CAS  PubMed  Google Scholar 

  8. Johnston JP, Farhangfar F, Aparicio JG, Nam SH, Applebury ML (1997) The bovine guanylate cyclase GC-E gene and 5′ flanking region. Gene 193:219–227

    CAS  PubMed  Google Scholar 

  9. Goraczniak RM, Duda T, Sharma RK (1997) Structure and functional characterization of a second subfamily member of the calcium-modulated bovine rod outer segment membrane guanylate cyclase, ROS-GC2. Biochem Biophys Res Commun 234:666–670

    CAS  PubMed  Google Scholar 

  10. Baehr W, Karan S, Maeda T, Luo DG, Li S, Bronson JD, Watt CB, Yau KW, Frederick JM, Palczewski K (2007) The function of guanylate cyclase 1 and guanylate cyclase 2 in rod and cone photoreceptors. J Biol Chem 282:8837–8847

    CAS  PubMed  Google Scholar 

  11. Lucas KA, Pitari GM, Kazerounian S, Ruiz-Stewart I, Park J, Schulz S, Chepenik KP, Waldman SA (2000) Guanylyl cyclases and signaling by cGMP. Pharmacol Rev 52:375–413

    CAS  PubMed  Google Scholar 

  12. Potter LR, Hunter T (2001) Guanylyl cyclase-linked natriuretic peptide receptors: structure and regulation. J Biol Chem 276:6057–6060

    CAS  PubMed  Google Scholar 

  13. Duda T, Venkataraman V, Ravichandran S, Sharma RK (2005) ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Peptides 26:969–984

    CAS  PubMed  Google Scholar 

  14. van den Akker F (2001) Structural insights into the ligand binding domains of membrane bound guanylyl cyclases and natriuretic peptide receptors. J Mol Biol 311:923–937

    PubMed  Google Scholar 

  15. Misono KS (2002) Natriuretic peptide receptor: structure and signaling. Mol Cell Biochem 230:46–90

    Google Scholar 

  16. Lolley RN, Racz E (1982) Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res 22:1481–1486

    CAS  PubMed  Google Scholar 

  17. Pepe IM, Panfoli I, Cugnoli C (1986) Guanylate cyclase in rod outer segments of the toad retina: effect of light and Ca2+. FEBS Lett 203:73–76

    CAS  PubMed  Google Scholar 

  18. Koch KW, Stryer L (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334:64–66

    CAS  PubMed  Google Scholar 

  19. Hayashi F, Hutson LD, Kishigami A, Nagao S, Yamazaki A (1993) Preparation and characterization of guanylate cyclase from vertebrate rod photoreceptors. Methods Neurosci 15:237–247

    Google Scholar 

  20. Gorczyca WA, Grey-Keller MP, Detwiler PB, Palczewski K (1994) Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc Natl Acad Sci USA 91:4014–4018

    CAS  PubMed  Google Scholar 

  21. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Hurley JB (1994) The human photoreceptor membrane guanylyl cyclase, retGC, is present in outer segments and is regulated by calcium and a soluble activator. Neuron 12:1345–1352

    CAS  PubMed  Google Scholar 

  22. Haeseleer F, Sokal I, Li N, Pettenati M, Rao N, Bronson W, Wechter R, Baehr W, Palczewski K (1999) Molecular characterization of a third member of the guanylyl cyclase-activating protein subfamily. J Biol Chem 274:6526–6535

    CAS  PubMed  Google Scholar 

  23. Olshevskaya EV, Hughes RE, Hurley JB, Dizhoor AM (1997) Calcium binding, but not a calcium-myristory switch, controls the ability of guanylyl cyclase-activating protein GCAP-2 to regulate photoreceptor guanylyl cyclase. J Biol Chem 272:14327–14333

    CAS  PubMed  Google Scholar 

  24. Yu H, Olshevskaya E, Duda T, Seno K, Hayashi F, Sharma RK, Dizhoor AM, Yamazaki A (1999) Activation of retinal guanylyl cyclase-1 by Ca2+-binding proteins involves its dimerization. J Biol Chem 274:15547–15555

    CAS  PubMed  Google Scholar 

  25. Ramamurthy V, Tucker C, Wilkie SE, Gaggett V, Hunt D, Hurley JB (2001) Interactions within the coiled-coil domain of retGC-1 guanylyl cyclase are optimized for regulation rather than for high affinity. J Biol Chem 276:26218–26229

    CAS  PubMed  Google Scholar 

  26. Laura RP, Dizhoor AM, Hurley JB (1996) The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain. J Biol Chem 271:11646–11651

    CAS  PubMed  Google Scholar 

  27. Duda T, Goraczniak R, Surgucheva I, Rudnicka-Nawrot M, Gorczyca W, Palczewski K, Sitaramayya A, Baehr W, Sharma RK (1996) Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35:8478–8482

    CAS  PubMed  Google Scholar 

  28. Hayashi F, Yamazaki A (1991) Polymorphism in purified guanylate cyclase from vertebrate rod photoreceptors. Proc Natl Acad Sci USA 88:4746–4750

    CAS  PubMed  Google Scholar 

  29. Dizhoor AM, Hurley JB (1999) Regulation of photoreceptor membrane guanylyl cyclases by guanylyl cyclase activating proteins. Methods 19:521–531

    CAS  PubMed  Google Scholar 

  30. Yamazaki A, Yamazaki M, Yamazaki RK, Usukura J (2006) Illuminated rhodopsin is required for strong activation of retinal guanylate cyclase by guanylate cyclase-activating proteins. Biochemistry 45:1899–1909

    CAS  PubMed  Google Scholar 

  31. Sharma RK, Yadav P, Duda T (2002) Allosteric regulatory step and configuration of the ATP-binding pocket in atrial natriuretic factor receptor guanylate cyclase transduction mechanism. Can J Physiol Pharmacol 79:682–691

    Google Scholar 

  32. Joubert S, Jossart C, McNicoll N, De Lean A (2005) Atrial natriuretic peptide-dependent photolabeling of a regulatory ATP-binding site on the natriuretic peptide receptor-A. FESB J 272:5572–5583

    CAS  Google Scholar 

  33. Yamazaki A, Yu H, Yamazaki M, Honkawa H, Matsuura L, Usukura J, Yamazaki RK (2003) A critical role for ATP in the stimulation of retinal guanylyl cyclase by guanylyl cyclase-activating proteins. J Biol Chem 278:33150–33160

    CAS  PubMed  Google Scholar 

  34. Cornwall MC, Fain GL (1994) Bleached pigment activates transduction in isolated rods of the salamander retina. J Physiol 480:261–279

    CAS  PubMed  Google Scholar 

  35. Koutalos Y, Nakatani K, Tamura T, Yau KW (1995) Characterization of guanylate cyclase activity in single retinal rod outer segments. J Gen Physiol 106:863–890

    CAS  PubMed  Google Scholar 

  36. Detwiler PD (2002) Open the loop: dissecting feedback regulation of a second messenger transduction cascade. Neuron 36:3–4

    CAS  PubMed  Google Scholar 

  37. Pozdnyakov N, Yoshida A, Cooper NGF, Margulis A, Duda T, Sharma RK, Sitaramayya A (1995) A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase. Biochemistry 34:14279–14283

    CAS  PubMed  Google Scholar 

  38. Margulis A, Pozdnyakov N, Sitaramayya A (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem Biophys Res Commun 218:243–247

    CAS  PubMed  Google Scholar 

  39. Robinson WE, Hagins WA (1979) GTP hydrolysis in intact rod outer segments and the transmitter cycle in visual excitation. Nature 280:398–400

    CAS  PubMed  Google Scholar 

  40. Hwang JY, Lange C, Helten A, Hoppner-Heitmann D, Duda T, Sharma RK, Koch KW (2003) Regulatory modes of rod outer segment membrane guanylate cyclase differ in catalytic efficiency and Ca2+-sensitivity. Eur J Biochem 270:3814–3821

    CAS  PubMed  Google Scholar 

  41. Krishnan N, Fletcher RT, Chader GJ, Krishna G (1978) Characterization of guanylate cyclase of rod outer segments of the bovine retina. Biochim Biophys Acta 523:506–515

    CAS  PubMed  Google Scholar 

  42. Sitaramayya A, Marala RB, Hakki S, Sharma RK (1991) Interactions of nucleotide analogues with rod outer segment guanylate cyclase. Biochemistry 30:6742–6747

    CAS  PubMed  Google Scholar 

  43. Gorczyca WA, van Hooser P, Palczewski K (1994) Nucleotide inhibitors and activators of retinal guanylyl cyclase. Biochemistry 33:3217–3222

    CAS  PubMed  Google Scholar 

  44. Sitaramayya A, Duda T, Sharma RK (1995) Regulation of bovine rod outer segment membrane guanylate cyclase by ATP, phosphodiesterase and metal ions. Mol Cell Biochem 148:139–145

    CAS  PubMed  Google Scholar 

  45. Tucker CL, Laura RP, Hurley JB (1997) Domain-specific stabilization of photoreceptor membrane guanylyl cyclase by adenine nucleotides and guanylyl cyclase activating proteins (GCAPs). Biochemistry 36:11995–12000

    CAS  PubMed  Google Scholar 

  46. Yamazaki M, Usukura J, Yamazaki RK, Yamazaki A (2005) ATP binding is required for physiological activation of retinal guanylate cyclase. Biochem Biophys Res Commun 338:1291–1298

    CAS  PubMed  Google Scholar 

  47. Larose L, McNicoll N, Ong H, De Léan A (1991) Allosteric modulation by ATP of the bovine adrenal natriuretic factor R1 receptor functions. Biochemistry 30:8990–8995

    CAS  PubMed  Google Scholar 

  48. Jewett JRS, Koller KJ, Goeddel DV, Lowe DG (1993) Hormonal induction of low affinity receptor guanylyl cyclase. EMBO J 12:769–777

    CAS  PubMed  Google Scholar 

  49. Biernbaum MS, Bownds MD (1979) Influence of light and calcium on guanosine-5′-triphosphate in isolated frog rod outer segments. J Gen Physiol 74:649–669

    CAS  PubMed  Google Scholar 

  50. Frins S, Bönigk W, Müller F, Kellner R, Koch KW (1996) Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods: cloning, heterologous expression and localization. J Biol Chem 271:8022–8027

    CAS  PubMed  Google Scholar 

  51. Dizhoor AM, Hurley JB (1996) Inactivation of EF-hands makes GCAP-2 (p24) a constitutive activator of photoreceptor guanylyl cyclase by preventing a Ca2+-induced “activator-to-inhibitor” transition. J Biol Chem 271:19346–19350

    CAS  PubMed  Google Scholar 

  52. Otto-Bruc A, Buczylko J, Surguchheva I, Subbaraya I, Rudnicka-Nawrot M, Crabb JW, Arendt A, Hargrave P, Baehr W, Palczewski K (1997) Functional reconstitution of photoreceptor guanylate cyclase with native and mutant forms of guanylate cyclase-activating protein 1. Biochemistry 36:4295–4302

    CAS  PubMed  Google Scholar 

  53. Dizhoor AM, Boikov SG, Olshevskaya EV (1998) Constitutive activation of photoreceptor guanylate cyclase by Y99C mutant of GCAP-1: possible role in causing human autosomal dominant cone degeneration. J Biol Chem 273:17311–17314

    CAS  PubMed  Google Scholar 

  54. Olshevskaya EV, Boikov S, Ermilov A, Krylov D, Hurley JB, Dizhoor AM (1999) Mapping functional domains of the guanylate cyclase regulatory protein, GCAP-2. J Biol Chem 274:10823–10832

    CAS  PubMed  Google Scholar 

  55. Peshenko IV, Moiseyev GP, Olshevskaya EV, Dizhoor AM (2004) Factors that determine Ca2+ sensitivity of photoreceptor guanylyl cyclase. Kinetic analysis of the interaction between the Ca2+-bound and the Ca2+-free guanylyl cyclase activating proteins (GCAPs) and recombinant photoreceptor guanylyl cyclase 1 (RetGC-1). Biochemistry 43:13796–13804

    CAS  PubMed  Google Scholar 

  56. McDowell JH (1993) Preparing rod outer segment membranes, regenerating rhodopsin, and determining rhodopsin concentration. Methods Neurosci 15:123–130

    Google Scholar 

  57. Martin RE, Elliott MH, Brush RS, Anderson RE (2005) Detailed characterization of the lipid composition of detergent-resistant membranes from photoreceptor rod outer segment membranes. Invest Ophthalmol Vis Sci 46:1147–1154

    PubMed  Google Scholar 

  58. Seno K, Kishimoto M, Abe M, Higuchi Y, Mieda M, Owada Y, Yoshiyama W, Liu H, Hayashi F (2001) Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membranes rafts in rod photoreceptor outer segments. J Biol Chem 276:20813–20816

    CAS  PubMed  Google Scholar 

  59. Nair KS, Balasubramanian N, Slepak VZ (2002) Signal-dependent translocation of transducin, RGS9-1-Gb5L complex, and arrestin to detergent-resistant membrane rafts in photoreceptors. Curr Biol 12:48647–48653

    Google Scholar 

  60. Senin II, Hppöner-Heitmann D, Polkovnikova OO, Churumova VA, Tikhomirova NK, Philippov PP, Koch KW (2004) Recoverin and rhodopsin kinase activity in detergent-resistant membrane rafts from rod outer segments. J Biol Chem 279:48647–48653

    CAS  PubMed  Google Scholar 

  61. Fleischman D, Denisevich M (1979) Guanylate cyclase of isolated bovine retinal rod axonemes. Biochemistry 18:5060–5066

    CAS  PubMed  Google Scholar 

  62. Hakki S, Sitaramayya A (1990) Guanylate cyclase from bovine rod outer segments: solubilization, partial purification, and regulation by inorganic pyrophosphate. Biochemistry 29:1088–1094

    CAS  PubMed  Google Scholar 

  63. Kondo H, Miller WH (1988) Rod light adaptation may be mediated by acceleration of the phosphodiesterase-guanylate cyclase cycle. Proc Natl Acad Sci USA 85:1322–1326

    CAS  PubMed  Google Scholar 

  64. Ames A III, Walseth TF, Heyman RA, Barad M, Graeff RM, Goldberg ND (1986) Light-induced increase in cGMP metabolic flux correspond with electrical responses of photoreceptors. J Biol Chem 261:13034–13042

    CAS  PubMed  Google Scholar 

  65. Pepe IM, Boero A, Vergani L, Panfoil I, Cognoli C (1986) Effect of light and calcium on cyclic GMP synthesis in rod outer segments of toad retina. Biochim Biophys Acta 889:271–276

    CAS  PubMed  Google Scholar 

  66. Pepe IM, Panfoil I, Hamm HE (1986) Visual transduction in vertebrate photoreceptors: light activation of guanylate cyclase. Cell Biophys 14:129–137

    Google Scholar 

  67. Balasubramanian N, Slepak VZ (2003) Light-mediated activation of Rac-1 in photoreceptor outer segments. Curr Biol 13:1306–1310

    CAS  PubMed  Google Scholar 

  68. Zhang H, Huang W, Zhang H, Zhu X, Craft CM, Baehr W, Chen CK (2003) Light-dependent redistribution of visual arrestins and transducin subunits in mice with defective phototransduction. Mol Vis 9:231–237

    CAS  PubMed  Google Scholar 

  69. Mendez A, Lem J, Simon M, Chen J (2003) Light-dependent translocation of arrestin in the absence of rhodopsin phosphorylation and transducin signaling. J Neurosci 23:3124–3129

    CAS  PubMed  Google Scholar 

  70. Woodruff ML, Lem J, Fain GL (2004) Early receptor current of wild-type and transducin knockout mice: photosensitivity and light-induced Ca2+ release. J Physiol 557:821–828

    CAS  PubMed  Google Scholar 

  71. Janz JM, Fay JF, Farrens DL (2003) Stability of dark state rhodopsin is mediated by a conserved ion pair in intradiscal loop E-2. J Biol Chem 278:16982–16991

    CAS  PubMed  Google Scholar 

  72. Doi T, Molday RS, Khorana HG (1990) Role of the intradiscal domain in rhodopsin assembly and function. Proc Natl Acad Sci USA 87:4991–4995

    CAS  PubMed  Google Scholar 

  73. Anukanth A, Khorana HG (1994) Structure and function in rhodopsin: requirements of a specific structure for the intradiscal domain. J Biol Chem 269:19738–19744

    CAS  PubMed  Google Scholar 

  74. Nagata T, Terakawa A, Kandori H, Kojima D, Shichida Y, Maeda A (1997) Water and peptide backbone structure in the active center of bovine rhodopsin. Biochemistry 36:6164–6170

    CAS  PubMed  Google Scholar 

  75. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA, Trong IL, Teller DC, Okada T, Stenkamp RE, Yamamoto M, Miyano M (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289:739–745

    CAS  PubMed  Google Scholar 

  76. Okada T, Fujiyoshi Y, Silow M, Navarro J, Landau EM, Shichida Y (2002) Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography. Proc Natl Acad Sci USA 99:5982–5987

    CAS  PubMed  Google Scholar 

  77. Furutani Y, Shichida Y, Kandori H (2003) Structure changes of water molecules during the photoactivation processes in bovine rhodopsin. Biochemistry 42:9619–9625

    CAS  PubMed  Google Scholar 

  78. Fesenko EE, Kolesnikov SS, Lyubarsky AL (1985) Induction by cyclic GMP of cationic conductance in plasma membrane of retinal rod outer segment. Nature 313:310–313

    CAS  PubMed  Google Scholar 

  79. He W, Cowan CW, Wensel TG (1998) RGS9, a GTPase accelerator for phototransduction. Neuron 20:95–102

    PubMed  Google Scholar 

  80. Slep KC, Kercher MA, He W, Cowan CW, Wensel TG (2001) Structural determinants for regulation of phosphodiesterase by a G protein at 2.0 Å. Nature 409:1071–1077

    CAS  PubMed  Google Scholar 

  81. Seno K, Kishigami A, Ihara S, Maeda T, Bondarenko V, Nishizawa Y, Usukura J, Yamazaki A, Hayashi F (1998) A possible role of RGS9 in phototransduction: a bridge between the cGMP phosphodiesterase system and the guanylyl cyclase system. J Biol Chem 273:22169–22172

    CAS  PubMed  Google Scholar 

  82. Yu H, Bondarenko VA, Yamazaki A (2001) Inhibition of retinal guanylyl cyclase by the RGS9–1N-terminus. Biochem Biophys Res Commun 286:12–19

    CAS  PubMed  Google Scholar 

  83. Bondarenko VA, Yu H, Yamazaki RK, Yamazaki A (2002) A novel role of RGS9: inhibition of retinal guanylyl cyclase. Mol Cell Biochem 230:125–128

    CAS  PubMed  Google Scholar 

  84. Yamazaki A, Sen I, Bitestky MW, Casnellie JE, Greengard P (1980) Cyclic GMP-specific, high affinity, noncatalytic binding sites on light-activated phosphodiesterase. J Biol Chem 255:11619–11624

    CAS  PubMed  Google Scholar 

  85. Ovchinnikov YA, Gubanov VV, Khramtsov NV, Ischenko KA, Zagranichny VE, Muradov KG, Shuvaeva TM, Lipkin VM (1987) Cyclic GMP phosphodiesterase from bovine retina: amino acid sequence of the α-subunit and nucleotide sequence of the corresponding cDNA. FEBS Lett 223:169–173

    CAS  PubMed  Google Scholar 

  86. Lipkin VM, Khramtsov NV, Vasilevskaya IA, Atabekova NV, Muradov KG, Gubanov VV, Li T, Johnston JP, Volpp KJ, Applebury ML (1990) β-Subunit of bovine rod photoreceptor cGMP phosphodiesterase: comparison with the phosphodiesterase family. J Biol Chem 265:12955–12959

    CAS  PubMed  Google Scholar 

  87. Kajimura N, Yamazaki M, Morikawa K, Yamazaki A, Mayanagi K (2002) Three-dimensional structure of non-activated cGMP phosphodiesterase 6 and comparison of its image with those of activated form. J Struct Biol 139:27–38

    CAS  PubMed  Google Scholar 

  88. Yamazaki A, Bartucca F, Ting A, Bitensky MW (1982) Reciprocal effects of an inhibitory factor on catalytic activity and noncatalytic cGMP binding sites of rod phosphodiesterase. Proc Natl Acad Sci USA 79:3702–3706

    CAS  PubMed  Google Scholar 

  89. Cote RH, Bownds MD, Arshavsky VY (1994) cGMP binding sites on photoreceptor phosphodiesterase: role in feedback regulation of visual transduction. Proc Natl Acad Sci USA 91:4845–4849

    CAS  PubMed  Google Scholar 

  90. Cote RH, Brunnock MA (1993) Intracellular cGMP concentration in rod photoreceptors is regulated by binding to high and moderate affinity cGMP binding sites. J Biol Chem 268:17190–17198

    CAS  PubMed  Google Scholar 

  91. Milam AH, Li ZY, Fariss RN (1998) Histopathology of the human retina in retinitis pigmentosa. Prog Retin Eye Res 17:175–205

    CAS  PubMed  Google Scholar 

  92. Chapple JP, Grayson C, Hardcastle AJ, Saliba RS, van der Spuy J, Cheetham ME (2001) Unfolding retinal dystrophies: a role for molecular chaperones? Trends Mol Med 7:414–421

    CAS  PubMed  Google Scholar 

  93. Stojanovic A, Hwa J (2002) Rhodopsin and retinitis pigmentosa: shedding light on structure and function. Receptor Channels 8:33–50

    CAS  Google Scholar 

  94. Iannaccone A, Man D, Waseem N, Jennings BJ, Ganapathiraju M, Gallaher K, Reese E, Bhattacharya SS, Klein-Seetharaman J (2006) Retinitis pigmentosa associated with rhodopsin mutations: correlation between phenotype variability and molecular effects. Vis Res 46:4556–4567

    CAS  PubMed  Google Scholar 

  95. Mendes HF, van der Spuy J, Chapple JP, Cheetham ME (2005) Mechanisms of cell death in rhodopsin retinitis pigmentosa: implication for therapy. Trend Mol Med 11:177–185

    CAS  Google Scholar 

  96. Leber T (1869) Uber retinitis pigmentosa and angeborene amaurose. Graefes Arch klin Exp Ophthalmol 15:1–25

    Google Scholar 

  97. Foxman SG, Heckenliverly JR, Batemen BJ, Wirstschaffer JD (1985) Classification of congenital and early-onset retinitis pigmentosa. Arch Ophthalmol 103:1502–1506

    CAS  PubMed  Google Scholar 

  98. Perrault I, Rozet JM, Calvas P, Camuzat A, Dollfus H, Châtelin S, Souied E, Ghazi I, Leowski C, Bonnemaison M, Le Paslier D, Frézal J, Dufier JL, Pittler S, Munnich A, Kaplan J (1996) Retinal-specific guanylate cyclase gene mutations in Leber’s congenital amaurosis. Nat Gent 14:461–464

    CAS  Google Scholar 

  99. Perrault I, Rozet JM, Gerber S, Ghazi I, Ducroq D, Souied E, Leowski C, Bonnemaison M, Dufier JL, Munnich A, Kaplan J (2000) Spectrum of retGC1 mutations in Leber’s congenital amaurosis. Eur Hum Genet 8:578–582

    CAS  Google Scholar 

  100. Rozet JM, Perrault I, Gerber S, Hanein S, Barbet F, Ducroq D, Souied E, Munnich A, Kaplan J (2001) Complete abolition of the retinal-specific guanylyl cyclase (retGC-1) catalytic ability consistently leads to Laber Congenital Amaurosis (LCA). Invest Ophthalmol Vis Sci 42:1190–1192

    CAS  PubMed  Google Scholar 

  101. Tucker CL, Ramamurthy V, Pina AL, Loyer M, Dharmaraj S, Li Y, Maumenee IH, Hurley JB, Koenekoop RK (2004) Functional analysis of mutant recessive GUCY2D alleles identified in Leber congenital amaurosis patients: protein domain comparisons and dominant negative effects. Mol Vis 10:297–303

    CAS  PubMed  Google Scholar 

  102. Huo X, Abe T, Misono KS (1999) Ligand binding-dependent limited proteolysis of the atrial natriuretic peptide receptor: juxtamembrane hinge structure essential for transmembrane signal transduction. Biochemistry 38:16941–16951

    CAS  PubMed  Google Scholar 

  103. Miyagi M, Misono KS (2000) Disulfide bond structure of the atrial natriuretic peptide receptor extracellular domain: conserved disulfide bonds among guanylate cyclase-coupled receptors. Biochim Biophys Acta 1478:30–38

    CAS  PubMed  Google Scholar 

  104. Duda T, Sharma RK (2005) Two membrane juxtaposed signaling modules in ANF-RGC are interlocked. Biochem Biophys Res Commun 332:149–156

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Drs. H. Imai and Y. Shichida (Kyoto University, Kyoto, Japan) for their suggestions of the conformational change of the loop E-II by illumination. We also thank Dr. Ari Sitaramayya (Oakland University, Rochester, Michigan) for his constructive suggestions on measurement of rhodopsin concentration and for providing Ammonyx Lo. We are also indebted to Dr. Naoka Komori (The University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma) for the critical reading of the manuscript. This study was supported in part by National Institute of Health Grant EY09631 and an unrestricted grant from Research to Prevent Blindness.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akio Yamazaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bondarenko, V.A., Hayashi, F., Usukura, J. et al. Involvement of rhodopsin and ATP in the activation of membranous guanylate cyclase in retinal photoreceptor outer segments (ROS-GC) by GC-activating proteins (GCAPs): a new model for ROS-GC activation and its link to retinal diseases. Mol Cell Biochem 334, 125–139 (2010). https://doi.org/10.1007/s11010-009-0323-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-009-0323-y

Keywords

Navigation