Skip to main content

Photoreceptor specific guanylate cyclases in vertebrate phototransduction

  • Chapter
Guanylate Cyclase

Abstract

Two membrane bound guanylate cyclases are expressed in vertebrate photoreceptor cells. They serve a key function in photoreceptor physiology as they synthesize the intracellular transmitter of photoexcitation guanosine 3’,5’-cyclic monophosphate (cGMP). Both cyclases named ROS-GC1 and ROS-GC2 form a subclass of membrane bound cyclases and differ in many aspects from hormone peptide receptor guanylate cyclases. One unique feature is their regulation by three small Ca2+-binding proteins called GCAPs. These regulatory proteins sense changes in the cytoplasmic Ca2+-concentration [Ca2+] during illumination and activate ROS-GCs when the [Ca2+] decreases below the value in a dark adapted cell of 500-600 nM. Recent work has identified the target regions of GCAP-1 in ROS-GC1. In addition to GCAPs several other proteins including aktin, tubulin, a glutamic-acid-rich protein and a GTPase accelerating protein (RGS9) were found to interact with ROS-GC1 and probably form a multiprotein complex. (Mol Cell Biochem 230: 97–106,2002)

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Kaupp UB, Koch K-W: Role of cGMP and Ca2+ in vertebrate photoreceptor excitation and adaptation. Annu Rev Physiol. 54: 153–175, 1992

    Article  PubMed  CAS  Google Scholar 

  2. Pugh EN Jr, Lamb TD: Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1141: 111–149, 1993

    Article  PubMed  CAS  Google Scholar 

  3. Yau K-W: Phototransduction mechanism in retinal rods and cones. Invest Ophthalmol Vis Sci 35: 9–32, 1994

    PubMed  CAS  Google Scholar 

  4. Pugh EN Jr, Duda T, Sitaramayya A, Sharma RK: Photoreceptor guanylate cyclases: A review. Biosci Rep 17: 429–473, 1997

    Article  PubMed  CAS  Google Scholar 

  5. Molday RS: Photoreceptor membrane proteins, phototransduction, and retinal degenerative diseases. Invest Ophthalmol Vis Sci 39: 2493–2513, 1998

    Google Scholar 

  6. Koch K-W: Control of photoreceptor proteins by Ca2+. Cell Calcium 18: 314–321, 1995

    Article  PubMed  CAS  Google Scholar 

  7. Koutalos Y, Yau K-W: Regulation of sensitivity in vertebrate rod photoreceptors by calcium. Trends Neurosci 19: 73–81, 1996

    Article  PubMed  CAS  Google Scholar 

  8. Pugh EN Jr, Nikonov S, Lamb TD: Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9: 410–418, 1999

    Article  PubMed  CAS  Google Scholar 

  9. Palczewski K, Polans AS, Baehr W, Ames JB: Ca2+-binding proteins in the retina: Structure, function, and the etiology of human visual diseases. BioEssays 22: 337–350, 2000

    Article  PubMed  CAS  Google Scholar 

  10. Fain GL, Matthews HR, Cornwall MC, Koutalos Y: Adaptation in vertebrate photoreceptors. Physiol Rev 81: 117–151, 2001

    PubMed  CAS  Google Scholar 

  11. Hodgkin AL, Nunn BJ: Control of light-sensitive current in salamander rods. J Physiol 403: 439–471, 1988

    PubMed  CAS  Google Scholar 

  12. Kawamura S, Murakami M: Regulation of cGMP levels by guanylate cyclase in truncated frog rod outer segments. J Gen Physiol 94: 649–668, 1989

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  14. Kutty RK, Fletcher RT, Chader GJ, Krishna G: Expression of guanylate cyclase-A mRNA in the rat retina: Detection using polymerase chain reaction. Biochem Biophys Res Commun 182: 851–857, 1992

    Article  PubMed  CAS  Google Scholar 

  15. Duda T, Goraczniak RM, Sitaramayya A, Sharma RK: Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase. Biochemistry 32: 1391–1395, 1993

    Article  PubMed  CAS  Google Scholar 

  16. Goraczniak RM, Duda T, Sitaramayya A, Sharma RK: Structural and functional characterization of the rod outer segment membrane guanylate cyclase. Biochem J 302: 455–461, 1994

    PubMed  CAS  Google Scholar 

  17. Goraczniak R, Duda T, Sharma RK: Structural 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, 1997

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  20. Yang R-B, Foster DC, Garbers DL, Fülle H-J: Two membrane forms of guanylyl cyclase found in the eye. Proc Natl Acad Sci USA 92: 602–606, 1995

    Article  PubMed  CAS  Google Scholar 

  21. Lange C, Duda T, Beyermann M, Sharma RK, Koch K-W: Regions in vertebrate photoreceptor guanylyl cyclase ROS-GC1 involved in Ca2+- dependent regulation by guanylyl cyclase-activating protein GCAP1. FEBS Lett 460: 27–31, 1999

    Article  PubMed  CAS  Google Scholar 

  22. Fülle H-J, Vassar R, Foster DC, Yang R-B, Axel R, Garbers DL: A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc Natl Acad Sci USA 92: 3571–3575, 1995

    Article  PubMed  Google Scholar 

  23. Juilfs DM, Fülle H-J, Zhao AZ, Houslay MD, Garbers DL, Beavo JA: A subset of olfactory neurons that selectively express cGMP-stimulated phosphodiesterase (PDE2) and guanylyl cyclase-D define a unique olfactory signal transduction pathway. Proc Natl Acad Sci USA 94: 3388–3395, 1997

    Article  PubMed  CAS  Google Scholar 

  24. Meyer MR, Angele A, Kremmer E, Kaupp UB, Müller F: A cGMPsignaling pathway in a subset of olfactory sensory neurons. Proc Natl Acad Sci USA 97: 10595–10600, 2000

    Article  PubMed  CAS  Google Scholar 

  25. Koch K-W: Purification and identification of photoreceptor guanylate cyclase. J Biol Chem 266: 8634–8637, 1991

    PubMed  CAS  Google Scholar 

  26. Hayashi F, Yamazaki A: Polymorphism in purified guanylate cyclase from vertebrate rod photoreceptors. Proc Natl Acad Sci USA 88: 47464750, 1991

    Google Scholar 

  27. Margulis A, Goraczniak RM, Duda T, Sharma RK, Sitaramayya A: Structural and biochemical identity of retinal rod outer segment membrane guanylate cyclase. Biochem Biophys Res Commun 194: 855–861, 1993

    Article  PubMed  CAS  Google Scholar 

  28. Koch K-W, Stryer L: Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334: 64–66, 1988

    Article  PubMed  CAS  Google Scholar 

  29. Koch K-W, Stecher P, Kellner R: Bovine retinal rod guanyl cyclase represents a new N-glycosylated subtype of membrane-bound guanyl cyclases. Eur J Biochem 222: 589–595, 1994

    Article  PubMed  CAS  Google Scholar 

  30. Dizhoor AM, Lowe DG, Olshevskaya EV, Laura RP, Laura JB: 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, 1994

    Article  PubMed  CAS  Google Scholar 

  31. Liu X, Seno K, Nishizawa Y, Hayashi F, Yamazaki A, Matsumoto H, Wakabayashi T, Usukura J: Ultrastructural localization of retinal guanylate cyclase in human and monkey retinas. Exp Eye Res 59: 761–768, 1994

    Article  PubMed  CAS  Google Scholar 

  32. Hallett MA, Delaat JL, Arikawa K, Schlamp CL, Kong F, Williams DS: Distribution of guanylate cyclase within photoreceptor outer segments. J Cell Sci 109: 1803–1812, 1996

    PubMed  CAS  Google Scholar 

  33. Cooper N, Liu L, Yoshida A, Pozdnyakov N, Margulis A, Sitaramayya A: The bovine rod outer segment guanylate cyclase, ROS-GC, is present in both outer segment and synaptic layers of the retina. J Mol Neurosci 6: 211–222, 1995

    Article  PubMed  CAS  Google Scholar 

  34. Yang R-B, Garbers DL: Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers. J Biol Chem 272: 13738–13742, 1997

    Article  PubMed  CAS  Google Scholar 

  35. Yang H, Wanner IB, Roper SD, Chaudhari N: An optimized method for in situ hybridization with signal amplification that allows the detection of rare mRNAs. J Histochem Cytochem 47: 431–445, 1999

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  37. Palczewski K, Subbaraya I, Gorczyca WA, Helekar BS, Ruiz CC, Ohguro H, Huang J, Zhao X, Crabb JW, Johnson RS, Walsh KA, Gray-Keller MP, Detwiler PB, Baehr W: Molecular cloning and characterization of retinal photoreceptor guanylyl cyclase-activating protein. Neuron 13: 395–404, 1994

    Article  PubMed  CAS  Google Scholar 

  38. Subbaraya I, Ruiz CC, Helekar BS, Zhao X, Gorczyca WA, Pettenati MJ, Rao PN, Palczewski K, Baehr W: Molecular characterization of human and mouse photoreceptor guanylate cyclase-activating protein (GCAP) and chromosomal localization of the human gene. J Biol Chem 269: 31080–31089, 1994

    PubMed  CAS  Google Scholar 

  39. Dizhoor AM, Olshevskaya EV, Henzel WJ, Wong SC, Stults JT, Ankoudinova I, Hurley JB: Cloning, sequencing, and expression of a 24-kDa Ca2+-binding protein activating photoreceptor guanylyl cyclase. J Biol Chem 270: 25200–25206, 1995

    Article  PubMed  CAS  Google Scholar 

  40. Gorczyca WA, Polans AS, Surgucheva IG, Subbaraya I, Baehr W, Palczewski K: Guanylyl cyclase activating protein. J Biol Chem 270: 22029–22036, 1995

    Article  PubMed  CAS  Google Scholar 

  41. Frins S, Bönigk W, Müller F, Kellner R, Koch K-W: Functional characterization of a guanylyl cyclase-activating protein from vertebrate rods. J Biol Chem 271: 8022–8027, 1996

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  43. Li N, Fariss RN, Zhang K, Otto-Bruc A, Haeseleer F, Bronson D, Qin N, Yamazaki A, Subbaraya I, Milam AH, Palczewski K, Baehr W: Guanylate-cyclase-inhibitory protein is a frog retinal Ca2+-binding protein related to mammalian guanylate-cyclase-activating proteins. Eur J Biochem 252: 591–599, 1998

    Article  PubMed  CAS  Google Scholar 

  44. Goraczniak RM, Duda T, Sharma RK: Calcium modulated signaling site in type 2 rod outer segment membrane guanylate cyclase (ROSGC2). Biochem Biophys Res Commun 245: 447–453, 1998

    Article  PubMed  CAS  Google Scholar 

  45. Dizhoor AM, Hurley JB: 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, 1996

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  47. Gray-Keller MP, Detwiler PB: The calcium feedback signal in the phototransduction cascade of vertebrate rods. Neuron 13: 849–861, 1994

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  50. Sokal I, Haeseleer F, Arendt A, Adman ET, Hargrave PA, Palczewski K: Identification of a guanylyl cyclase-activating protein-binding site within the catalytic domain of retinal guanylyl cyclase 1. Biochemistry 38: 1387–1393, 1999

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  52. Perrault I, Rozet J-M, Gerber S, Ghazi I, Leowski C, Ducroq D, Souied E, Dufier J-L, Munnich A, Kaplan J: Leber congenital amaurosis. Mol Genet Metab 68: 200–218, 1999

    Article  PubMed  CAS  Google Scholar 

  53. Duda T, Venkataraman V, Goraczniak R, Lange C, Koch K-W, Sharma RK: Functional consequences of a rod outer segment membrane guanylate cyclase (ROS-GC1) gene mutation linked with Leber’s congenital amaurosis. Biochemistry 38: 509–515, 1999

    Article  PubMed  CAS  Google Scholar 

  54. Krishnan A, Goraczniak RM, Duda T, Sharma RK: Third calcium-modulated rod outer segment membrane guanylate cyclase transduction mechanism. Mol Cell Biochem 178: 251–259, 1998

    Article  PubMed  CAS  Google Scholar 

  55. Sharma RK, Duda T, Goraczniak R, Sitaramayya A: Membrane guanylate cyclase signal transduction system. Ind J Biochem Biophys 34: 40–49, 1997

    Article  CAS  Google Scholar 

  56. Duda T, Yadav P, Jankowska A, Venkataraman V, Sharma RK: Three dimensional atomic model and experimental validation for the ATP-regulated module (ARM) of the atrial natriuretic factor receptor guanylate cyclase. Mol Cell Biochem 217: 165–172, 2001

    Article  PubMed  CAS  Google Scholar 

  57. Potter LR, Hunter T: Phosphorylation of the kinase homology domain is essential for activation of the A-type natriuretic peptide receptor. Mol Cell Biol 18: 2164–2172, 1998

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  59. Duda T, Goraczniak R, Sharma RK: Distinct inhibitory ATP-regulated modulatory domain (ARM) in membrane guanylate cyclases. Biochem J 319: 279–283, 1996

    PubMed  CAS  Google Scholar 

  60. Lambrecht H-G, Koch K-W: Phosphorylation of recoverin, the calcium-sensitive activator of photoreceptor guanylyl cyclase. FEBS Lett 294: 207–209, 1991

    Article  PubMed  CAS  Google Scholar 

  61. Gorczyca WA, Van Hooser JP, Palczewski K: Nucleotide inhibitors and activators of retinal guanylyl cyclase. Biochemistry 33: 3217–3222, 1994

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  63. Aparicio JG, Applebury ML: The photoreceptor guanylate cylcase is an autophosphorylating protein kinase. J Biol Chem 271: 27083–27089, 1996

    Article  PubMed  CAS  Google Scholar 

  64. Wolbring G, Schnetkamp PPM: Modulation of the calcium sensitivity of bovine retinal rod outer segment guanylyl cyclase by sodium ions and protein kinase A. Biochemistry 35: 11013–11018, 1996

    Article  PubMed  CAS  Google Scholar 

  65. Wolbring G, Schnetkamp PPM: Activation by PKC of the Ca2+- sensitive guanylyl cyclase in bovine retinal rod outer segments measured with an optical assay. Biochemistry 34: 4689–4695, 1995

    Article  PubMed  CAS  Google Scholar 

  66. Hurley JH: The adenylyl and guanylyl cyclase superfamily. Curr Opin Struct Biol 8: 770–777, 1998

    Article  PubMed  CAS  Google Scholar 

  67. Koch K-W, Eckstein F, Stryer L: Stereochemical course of the reaction catalyzed by guanylate cyclase from bovine retinal rod outer segments. J Biol Chem 265: 9659–9663, 1990

    PubMed  CAS  Google Scholar 

  68. Liu Y, Ruoho AE, Rao VD, Hurley JH: Catalytic mechanism of the adenylyl and guanylyl cyclases: Modeling and mutational analysis. Proc Natl Acad Sci USA 94: 13414–13419, 1997

    Article  PubMed  CAS  Google Scholar 

  69. Tucker CL, Hurley JH, Miller TR, Hurley JB: Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 95: 5993–5997, 1998

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  71. Kelsell RE, Gregory-Evans K, Payne AM, Perrault I, Kaplan J, Yang R-B, Garbers DL, Bird AC, Moore AT, Hunt DM: Mutations in the retinal guanylate cyclase (RETGC-I) gene in dominant cone-rod dystrophy. Hum Mol Genet 7: 1179–1184, 1998

    Article  PubMed  CAS  Google Scholar 

  72. Gregory-Evans K, Kelsell RE, Gregory-Evans CY, Downes SM, Fitzke FW, Holder GE, Simunovic M, Motion JD, Taylor R, Hunt DM, Bird AC, Moore AT: Autosomal dominant cone-rod retinal dystrophy (CORD6) from heterozygous mutation of GUCY23D, which encodes retinal guanylate cyclase. Ophthalmology 107: 5561, 2000

    Article  Google Scholar 

  73. Duda T, Krishnan A, Venkataraman V, Lange C, Koch K-W, Sharma RK: Mutations in the rod outer segment membrane guanylate cyclase in a cone-rod dystrophy cause defects in calcium signaling. Biochemistry 38: 13912–13919, 1999

    Article  PubMed  CAS  Google Scholar 

  74. Tucker CL, Woodcock SC, Kelsell RE, Ramamurthy V, Hunt DM, Hurley JB: Biochemical analysis of a dimerization domain mutation in RetGC-1 associated with dominant cone-rod dystrophy. Proc Natl Acad Sci USA 96: 9039–9044, 1999

    Article  PubMed  CAS  Google Scholar 

  75. Duda T, Venkataraman V, Jankowska A, Lange C, Koch K-W, Sharma RK: Impairment of the rod outer segment membrane guanylate cyclase dimerization in A cone-rod dystrophy results in defective calcium signaling. Biochemistry 39: 12522–12533, 2000

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  78. Schrem A, Lange C, Beyermann M, Koch K-W: Identification of a domain in guanylyl cyclase-activating protein 1 that interacts with a complex of guanylyl cyclase and tubulin in photoreceptors. J Biol Chem 274: 6244–6249, 1999

    Article  PubMed  CAS  Google Scholar 

  79. Körschen HG, Beyermann M, Müller F, Heck M, Vantler M, Koch KW, Kellner R, Wolfrum U, Bode C, Hofmann KP, Kaupp UB: Interaction of glutamic-acid-rich proteins with the cGMP signalling pathway in rod photoreceptors. Nature 400: 761–766, 1999

    Article  PubMed  Google Scholar 

  80. Körschen HG, Illing M, Seifert R, Sesti F, Williams A, Gotzes S, Colville C, Müller F, Dosé A, Godde M, Molday L, Kaupp UB, Molday RS: A 240 kDa protein represents the complete ß subunit of the cyclic nucleotide-gated channel from rod photoreceptor. Neuron 15: 627636, 1995

    Google Scholar 

  81. Allikmets R, Singh N, Sun H, Shroyer NF, Hutchinson A, Chidambaram A, Gerrard B, Baird L, Stauffer D, Pfeiffer A, Rattner A, Smallwood P, Li Y, Anderson KL, Lewis RA, Nathans J, Leppert M, Dean M, Lupski JR: A photoreceptor cell-specific ATP-binding transporter gene (ABCR) is mutated in recessive Stargardt macular dystrophy. Nature Genet 15: 236–246, 1997

    Article  PubMed  CAS  Google Scholar 

  82. Illing M, Molday LL, Molday RS: The 220-kDa rim protein of retinal rod outer segment is a member of the ABC transporter superfamily. J Biol Chem 272: 10303–10310, 1997

    Article  PubMed  CAS  Google Scholar 

  83. Sun H, Molday RS, Nathans J: Retinal stimulates ATP hydrolysis by purified and reconstituted ABCR, the photoreceptor-specific ATP-binding cassette transporter responsible for Stargardt Disease. J Biol Chem 274: 8269–8281, 1999

    Article  PubMed  CAS  Google Scholar 

  84. Seno K, Kishigami A, Ihara S, Maeda T, Bondarenko VA, Nishizawa Y, Usukura J, Yamazaki A, Hayashi F: A possible role of RGS9 in phototransduction. J Biol Chem 273: 22169–22172, 1998

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  86. Miller JL, Picones A, Korenbrot JI: Differences in transduction between rod and cone photoreceptors: an exploration of the role of calcium homeostasis. Curr Opin Neurobiol 4: 488–495, 1994

    Article  PubMed  CAS  Google Scholar 

  87. Venkataraman V, Nagele R, Duda T, Sharma RK: Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling systems in the pineal gland: Biochemical, molecular and immunohistochemical evidence. Biochemistry 39: 6042–6052, 2000

    Article  PubMed  CAS  Google Scholar 

  88. Duda T, Venkataraman V, Krishnan A, Nagele RG, Sharma RK: Negatively calcium-modulated membrane guanylate cyclase (ROSGC1) signaling systems in the rat olfactory bulb. Biochemistry 40: 2001 (in press)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Springer Science+Business Media New York

About this chapter

Cite this chapter

Koch, KW., Duda, T., Sharma, R.K. (2002). Photoreceptor specific guanylate cyclases in vertebrate phototransduction. In: Sharma, R.K. (eds) Guanylate Cyclase. Developments in Molecular and Cellular Biochemistry, vol 36. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0927-1_7

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-0927-1_7

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-5308-9

  • Online ISBN: 978-1-4615-0927-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics