1932

Abstract

Our robust visual experience is based on the reliable transfer of information from our photoreceptor cells, the rods and cones, to higher brain centers. At the very first synapse of the visual system, information is split into two separate pathways, ON and OFF, which encode increments and decrements in light intensity, respectively. The importance of this segregation is borne out in the fact that receptive fields in higher visual centers maintain a separation between ON and OFF regions. In the past decade, the molecular mechanisms underlying the generation of ON signals have been identified, which are unique in their use of a G-protein signaling cascade. In this review, we consider advances in our understanding of G-protein signaling in ON-bipolar cell (BC) dendrites and how insights about signaling have emerged from visual deficits, mostly night blindness. Studies of G-protein signaling in ON-BCs reveal an intricate mechanism that permits the regulation of visual sensitivity over a wide dynamic range.

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2017-09-15
2024-05-09
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Literature Cited

  1. Agosto MA, Zhang Z, He F, Anastassov IA, Wright SJ. et al. 2014. Oligomeric state of purified transient receptor potential melastatin-1 (TRPM1), a protein essential for dim light vision. J. Biol. Chem. 289:27019–33 [Google Scholar]
  2. Anderson GR, Posokhova E, Martemyanov KA. 2009. The R7 RGS protein family: multi-subunit regulators of neuronal G protein signaling. Cell Biochem. Biophys. 54:33–46 [Google Scholar]
  3. Ashmore JF, Falk G. 1980. The single-photon signal in rod bipolar cells of the dogfish retina. J. Physiol. 300:151–66 [Google Scholar]
  4. Audo I, Kohl S, Leroy BP, Munier FL, Guillonneau X. et al. 2009. TRPM1 is mutated in patients with autosomal-recessive complete congenital stationary night blindness. Am. J. Hum. Genet. 85:720–29 [Google Scholar]
  5. Ball SL, Pardue MT, McCall MA, Gregg RG, Peachey NS. 2003. Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities. Vis. Neurosci. 20:267–72 [Google Scholar]
  6. Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B. et al. 2000. Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat. Genet. 26:319–23 [Google Scholar]
  7. Bellone RR, Brooks SA, Sandmeyer L, Murphy BA, Forsyth G. et al. 2008. Differential gene expression of TRPM1, the potential cause of congenital stationary night blindness and coat spotting patterns (LP) in the Appaloosa horse (Equus caballus). Genetics 179:1861–70 [Google Scholar]
  8. Berntson A, Smith RG, Taylor WR. 2004. Postsynaptic calcium feedback between rods and rod bipolar cells in the mouse retina. Vis. Neurosci. 21:913–24 [Google Scholar]
  9. Berson EL, Lessell S. 1988. Paraneoplastic night blindness with malignant melanoma. Am. J. Ophthalmol. 106:307–11 [Google Scholar]
  10. Bojang P Jr., Gregg RG. 2012. Topological analysis of small leucine-rich repeat proteoglycan nyctalopin. PLOS ONE 7:e33137 [Google Scholar]
  11. Brown RL, Xiong W-H, Peters JH, Tekmen-Clark M, Strycharska-Orczyk I. et al. 2015. TRPM3 expression in mouse retina. PLOS ONE 10:e0117615 [Google Scholar]
  12. Cabrera JL, De Freitas F, Satpaev DK, Slepak VZ. 1998. Identification of the Gβ5-RGS7 protein complex in the retina. Biochem. Biophys. Res. Commun. 249:898–902 [Google Scholar]
  13. Cao Y, Masuho I, Okawa H, Xie K, Asami J. et al. 2009. Retina-specific GTPase accelerator RGS11/Gβ5S/R9AP is a constitutive heterotrimer selectively targeted to mGluR6 in ON-bipolar neurons. J. Neurosci. 29:9301–13 [Google Scholar]
  14. Cao Y, Pahlberg J, Sarria I, Kamasawa N, Sampath AP, Martemyanov KA. 2012. Regulators of G protein signaling RGS7 and RGS11 determine the onset of the light response in ON bipolar neurons. PNAS 109:7905–10 [Google Scholar]
  15. Cao Y, Posokhova E, Martemyanov KA. 2011. TRPM1 forms complexes with nyctalopin in vivo and accumulates in postsynaptic compartment of ON-bipolar neurons in mGluR6-dependent manner. J. Neurosci. 31:11521–26 [Google Scholar]
  16. Cao Y, Sarria I, Fehlhaber KE, Kamasawa N, Orlandi C. et al. 2015. Mechanism for selective synaptic wiring of rod photoreceptors into the retinal circuitry and its role in vision. Neuron 87:1248–60 [Google Scholar]
  17. Cao Y, Song H, Okawa H, Sampath AP, Sokolov M, Martemyanov KA. 2008. Targeting of RGS7/Gβ5 to the dendritic tips of ON-bipolar cells is independent of its association with membrane anchor R7BP. J. Neurosci. 28:10443–49 [Google Scholar]
  18. Chakraborty R, Pardue MT. 2015. Molecular and biochemical aspects of the retina on refraction. Prog. Mol. Biol. Transl. Sci. 134:249–67 [Google Scholar]
  19. Chakraborty R, Park HN, Hanif AM, Sidhu CS, Iuvone PM, Pardue MT. 2015. ON pathway mutations increase susceptibility to form-deprivation myopia. Exp. Eye Res. 137:79–83 [Google Scholar]
  20. Chen C-K, Eversole-Cire P, Zhang H, Mancino V, Chen Y-J. et al. 2003. Instability of GGL domain-containing RGS proteins in mice lacking the G protein β-subunit Gβ5. PNAS 100:6604–9 [Google Scholar]
  21. Chen FS, Shim H, Morhardt D, Dallman R, Krahn E. et al. 2010. Functional redundancy of R7 RGS proteins in ON-bipolar cell dendrites. Investig. Ophthalmol. Vis. Sci. 51:686–93 [Google Scholar]
  22. Cibis GW, Fitzgerald KM, Harris DJ, Rothberg PG, Rupani M. 1993. The effects of dystrophin gene mutations on the ERG in mice and humans. Investig. Ophthalmol. Vis. Sci. 34:3646–52 [Google Scholar]
  23. Cohen MR, Moiseenkova-Bell VY. 2014. Structure of thermally activated TRP channels. Curr. Top. Membr. 74:181–211 [Google Scholar]
  24. Connaughton VP, Nelson R. 2000. Axonal stratification patterns and glutamate-gated conductance mechanisms in zebrafish retinal bipolar cells. J. Physiol. 524:135–46 [Google Scholar]
  25. Connors NC, Adams ME, Froehner SC, Kofuji P. 2004. The potassium channel Kir4.1 associates with the dystrophin-glycoprotein complex via α-syntrophin in glia. J. Biol. Chem. 279:28387–92 [Google Scholar]
  26. Constantin B. 2014. Dystrophin complex functions as a scaffold for signalling proteins. Biochim. Biophys. Acta 1838:635–42 [Google Scholar]
  27. Copenhagen DR, Jahr CE. 1989. Release of endogenous excitatory amino acids from turtle photoreceptors. Nature 341:536–39 [Google Scholar]
  28. Crewther DP, Crewther SG, Xie RZ. 1996. Changes in eye growth produced by drugs which affect retinal ON or OFF responses to light. J. Ocul. Pharmacol. Ther. 12:193–208 [Google Scholar]
  29. Dacheux RF, Raviola E. 1986. The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. J. Neurosci. 6:331–45 [Google Scholar]
  30. DeVries SH, Li W, Saszik S. 2006. Parallel processing in two transmitter microenvironments at the cone photoreceptor synapse. Neuron 50:735–48 [Google Scholar]
  31. Dhingra A, Faurobert E, Dascal N, Sterling P, Vardi N. 2004. A retinal-specific regulator of G-protein signaling interacts with Gαo and accelerates an expressed metabotropic glutamate receptor 6 cascade. J. Neurosci. 24:5684–93 [Google Scholar]
  32. Dhingra A, Fina ME, Neinstein A, Ramsey DJ, Xu Y. et al. 2011. Autoantibodies in melanoma-associated retinopathy target TRPM1 cation channels of retinal ON bipolar cells. J. Neurosci. 31:3962–67 [Google Scholar]
  33. Dhingra A, Jiang M, Wang TL, Lyubarsky A, Savchenko A. et al. 2002. Light response of retinal ON bipolar cells requires a specific splice variant of Gαo. J. Neurosci. 22:4878–84 [Google Scholar]
  34. Dhingra A, Lyubarsky A, Jiang MS, Pugh EN Jr., Birnbaumer L. et al. 2000. The light response of ON bipolar neurons requires Gαo. J. Neurosci. 20:9053–58 [Google Scholar]
  35. Dhingra A, Ramakrishnan H, Neinstein A, Fina ME, Xu Y. et al. 2012. Gβ3 is required for normal light ON responses and synaptic maintenance. J. Neurosci. 32:11343–55 [Google Scholar]
  36. Dhingra A, Sulaiman P, Xu Y, Fina ME, Veh RW, Vardi N. 2008. Probing neurochemical structure and function of retinal ON bipolar cells with a transgenic mouse. J. Comp. Neurol. 510:484–96 [Google Scholar]
  37. D'Souza VN, Nguyen TM, Morris GE, Karges W, Pillers DA, Ray PN. 1995. A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 4:837–42 [Google Scholar]
  38. Dunn FA, Doan T, Sampath AP, Rieke F. 2006. Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 26:3959–70 [Google Scholar]
  39. Dupré DJ, Robitaille M, Rebois RV, Hébert TE. 2009. The role of Gβγ subunits in the organization, assembly, and function of GPCR signaling complexes. Annu. Rev. Pharmacol. Toxicol. 49:31–56 [Google Scholar]
  40. Euler T, Haverkamp S, Schubert T, Baden T. 2014. Retinal bipolar cells: elementary building blocks of vision. Nat. Rev. Neurosci. 15:507–19 [Google Scholar]
  41. Field GD, Rieke F. 2002. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34:773–85 [Google Scholar]
  42. Field GD, Sampath AP, Rieke F. 2005. Retinal processing near absolute threshold: from behavior to mechanism. Annu. Rev. Physiol. 67:491–514 [Google Scholar]
  43. Gavillet B, Rougier J-S, Domenighetti AA, Behar R, Boixel C. et al. 2006. Cardiac sodium channel Nav1.5 is regulated by a multiprotein complex composed of syntrophins and dystrophin. Circ. Res. 99:407–14 [Google Scholar]
  44. Gerding H, Gullotta F, Kuchelmeister K, Busse H. 1993. Ocular findings in Walker-Warburg syndrome. Child's Nerv. Syst. 9:418–20 [Google Scholar]
  45. Ghosh KK, Bujan S, Haverkamp S, Feigenspan A, Wassle H. 2004. Types of bipolar cells in the mouse retina. J. Comp. Neurol. 469:70–82 [Google Scholar]
  46. Gilman AG. 1987. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56:615–49 [Google Scholar]
  47. Grant GB, Dowling JE. 1995. A glutamate-activated chloride current in cone-driven ON bipolar cells of the white perch retina. J. Neurosci. 15:3852–62 [Google Scholar]
  48. Gregg RG, Kamermans M, Klooster J, Lukasiewicz PD, Peachey NS. et al. 2007. Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. J. Neurophysiol. 98:3023–33 [Google Scholar]
  49. Gregg RG, Mukhopadhyay S, Candille SI, Ball SL, Pardue MT. et al. 2003. Identification of the gene and the mutation responsible for the mouse nob phenotype. Investig. Ophthalmol. Vis. Sci. 44:378–84 [Google Scholar]
  50. Gregg RG, Ray TA, Hasan N, McCall MA, Peachey NS. 2014. Interdependence among members of the mGluR6 G-protein mediated signalplex of retinal depolarizing bipolar cells. G Protein Signaling Mechanisms in the Retina KA Martemyanov, AP Sampath 67–79 New York: Springer [Google Scholar]
  51. Hervé D. 2011. Identification of a specific assembly of the G protein Golf as a critical and regulated module of dopamine and adenosine-activated cAMP pathways in the striatum. Front. Neuroanat. 5:48 [Google Scholar]
  52. Hollinger S, Hepler JR. 2002. Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharmacol. Rev. 54:527–59 [Google Scholar]
  53. Huang L, Max M, Margolskee RF, Su H, Masland RH, Euler T. 2003. G protein subunit Gγ13 is coexpressed with Gαo, Gβ3, and Gβ4 in retinal ON bipolar cells. J. Comp. Neurol. 455:1–10 [Google Scholar]
  54. Ichinose T, Fyk-Kolodziej B, Cohn J. 2014. Roles of ON cone bipolar cell subtypes in temporal coding in the mouse retina. J. Neurosci. 34:8761–71 [Google Scholar]
  55. Ishii M, Morigiwa K, Takao M, Nakanishi S, Fukuda Y. et al. 2009. Ectopic synaptic ribbons in dendrites of mouse retinal ON- and OFF-bipolar cells. Cell Tissue Res 338:355–75 [Google Scholar]
  56. Jeffrey BG, Morgans CW, Puthussery T, Wensel TG, Burke NS. et al. 2010. R9AP stabilizes RGS11-Gβ5 and accelerates the early light response of ON-bipolar cells. Vis. Neurosci. 27:9–17 [Google Scholar]
  57. Kaneko A, Tachibana M. 1985. A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. J. Physiol. 358:131–52 [Google Scholar]
  58. Kaur T, Nawy S. 2012. Characterization of Trpm1 desensitization in ON bipolar cells and its role in downstream signalling. J. Physiol. 590:179–92 [Google Scholar]
  59. Kim DS, Ross SE, Trimarchi JM, Aach J, Greenberg ME, Cepko CL. 2008. Identification of molecular markers of bipolar cells in the murine retina. J. Comp. Neurol. 507:1795–810 [Google Scholar]
  60. Knuesel I, Mastrocola M, Zuellig RA, Bornhauser B, Schaub MC, Fritschy JM. 1999. Short communication: altered synaptic clustering of GABAA receptors in mice lacking dystrophin (mdx mice). Eur. J. Neurosci. 11:4457–62 [Google Scholar]
  61. Koike C, Numata T, Ueda H, Mori Y, Furukawa T. 2010a. TRPM1: a vertebrate TRP channel responsible for retinal ON bipolar function. Cell Calcium 48:95–101 [Google Scholar]
  62. Koike C, Obara T, Uriu Y, Numata T, Sanuki R. et al. 2010b. TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. PNAS 107:332–37 [Google Scholar]
  63. Kondo H, Saito K, Urano M, Sagara Y, Uchio E, Kondo M. 2010. A case of Fukuyama congenital muscular dystrophy associated with negative electroretinograms. Jpn. J. Ophthalmol. 54:622–24 [Google Scholar]
  64. Kondo M, Sanuki R, Ueno S, Nishizawa Y, Hashimoto N. et al. 2011. Identification of autoantibodies against TRPM1 in patients with paraneoplastic retinopathy associated with ON bipolar cell dysfunction. PLOS ONE 6:e19911 [Google Scholar]
  65. Krumins AM, Gilman AG. 2006. Targeted knockdown of G protein subunits selectively prevents receptor-mediated modulation of effectors and reveals complex changes in non-targeted signaling proteins. J. Biol. Chem. 281:10250–62 [Google Scholar]
  66. Lambert S, Drews A, Rizun O, Wagner TF, Lis A. et al. 2011. Transient receptor potential melastatin 1 (TRPM1) is an ion-conducting plasma membrane channel inhibited by zinc ions. J. Biol. Chem. 286:12221–33 [Google Scholar]
  67. Lasater EM. 1988. Membrane currents of retinal bipolar cells in culture. J. Neurophysiol. 60:1460–80 [Google Scholar]
  68. Lee Y, Kameya S, Cox GA, Hsu J, Hicks W. et al. 2005. Ocular abnormalities in Largemyd and Largevls mice, spontaneous models for muscle, eye, and brain diseases. Mol. Cell Neurosci 30:160–72 [Google Scholar]
  69. Lei B, Bush RA, Milam AH, Sieving PA. 2000. Human melanoma-associated retinopathy (MAR) antibodies alter the retinal ON-response of the monkey ERG in vivo. Investig. Ophthalmol. Vis. Sci. 41:262–66 [Google Scholar]
  70. Liu J, Ball SL, Yang Y, Mei P, Zhang L. et al. 2006. A genetic model for muscle–eye–brain disease in mice lacking protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1). Mech. Dev 123:228–40 [Google Scholar]
  71. Lodha N, Loucks CM, Beaulieu C, Parboosingh JS, Bech-Hansen NT. 2012. Congenital stationary night blindness: mutation update and clinical variability. Adv. Exp. Med. Biol 723:371–79 [Google Scholar]
  72. Lu Y, Jia L, He S, Hurley MC, Leys MJ. et al. 2009. Melanoma-associated retinopathy: a paraneoplastic autoimmune complication. Arch. Ophthalmol. 127:1572–80 [Google Scholar]
  73. Makino ER, Handy JW, Li T, Arshavsky VY. 1999. The GTPase activating factor for transducin in rod photoreceptors is the complex between RGS9 and type 5 G protein β subunit. PNAS 96:1947–52 [Google Scholar]
  74. Mansergh F, Orton NC, Vessey JP, Lalonde MR, Stell WK. et al. 2005. Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum. Mol. Genet. 14:3035–46 [Google Scholar]
  75. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M. et al. 1995. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80:757–65 [Google Scholar]
  76. Milam AH, Saari JC, Jacobson SG, Lubinski WP, Feun LG, Alexander KR. 1993. Autoantibodies against retinal bipolar cells in cutaneous melanoma-associated retinopathy. Investig. Ophthalmol. Vis. Sci. 34:91–100 [Google Scholar]
  77. Miyake Y, Yagasaki K, Horiguchi M, Kawase Y, Kanda T. 1986. Congenital stationary night blindness with negative electroretinogram. A new classification. Arch. Ophthalmol. 104:1013–20 [Google Scholar]
  78. Mojumder DK, Qian Y, Wensel TG. 2009. Two R7 regulator of G-protein signaling proteins shape retinal bipolar cell signaling. J. Neurosci. 29:7753–65 [Google Scholar]
  79. Mojumder DK, Wensel TG. 2008. Variable distribution of RGS7 and RGS11 in the dendritic-tips of ON-bipolar cells in the murine retina. Investig. Ophthalmol. Vis. Sci. 49:762 [Google Scholar]
  80. Morgans CW, Ren G, Akileswaran L. 2006. Localization of nyctalopin in the mammalian retina. Eur. J. Neurosci. 23:1163–71 [Google Scholar]
  81. Morgans CW, Wensel TG, Brown RL, Perez-Leon JA, Bearnot B, Duvoisin RM. 2007. Gβ5-RGS complexes co-localize with mGluR6 in retinal ON-bipolar cells. Eur. J. Neurosci. 26:2899–905 [Google Scholar]
  82. Morgans CW, Zhang J, Jeffrey BG, Nelson SM, Burke NS. et al. 2009. TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. PNAS 106:19174–78 [Google Scholar]
  83. Nawy S. 1999. The metabotropic receptor mGluR6 may signal through Go, but not phosphodiesterase, in retinal bipolar cells. J. Neurosci. 19:2938–44 [Google Scholar]
  84. Nawy S. 2000. Regulation of the on bipolar cell mGluR6 pathway by Ca2+. J. Neurosci. 20:4471–79 [Google Scholar]
  85. Nawy S. 2004. Desensitization of the mGluR6 transduction current in tiger salamander On bipolar cells. J. Physiol. 558:137–46 [Google Scholar]
  86. Nawy S, Jahr CE. 1990. Suppression by glutamate of cGMP-activated conductance in retinal bipolar cells. Nature 346:269–71 [Google Scholar]
  87. Nelson R. 1973. A comparison of electrical properties of neurons in Necturus retina. J. Neurophysiol. 36:519–35 [Google Scholar]
  88. Neuillé M, El Shamieh S, Orhan E, Michiels C, Antonio A. et al. 2014. Lrit3 deficient mouse (nob6): a novel model of complete congenital stationary night blindness (cCSNB). PLOS ONE 9:e90342 [Google Scholar]
  89. Neuillé M, Morgans CW, Cao Y, Orhan E, Michiels C. et al. 2015. LRIT3 is essential to localize TRPM1 to the dendritic tips of depolarizing bipolar cells and may play a role in cone synapse formation. Eur. J. Neurosci. 42:1966–75 [Google Scholar]
  90. Oancea E, Vriens J, Brauchi S, Jun J, Splawski I, Clapham DE. 2009. TRPM1 forms ion channels associated with melanin content in melanocytes. Sci. Signal. 2:ra21 [Google Scholar]
  91. Okawa H, Pahlberg J, Rieke F, Birnbaumer L, Sampath AP. 2010. Coordinated control of sensitivity by two splice variants of Gαo in retinal ON bipolar cells. J. Gen. Physiol. 136:443–54 [Google Scholar]
  92. Omori Y, Araki F, Chaya T, Kajimura N, Irie S. et al. 2012. Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells. J. Neurosci. 32:6126–37 [Google Scholar]
  93. Orlandi C, Cao Y, Martemyanov KA. 2013. Orphan receptor GPR179 forms macromolecular complexes with components of metabotropic signaling cascade in retina ON-bipolar neurons. Investig. Ophthalmol. Vis. Sci. 54:7153–61 [Google Scholar]
  94. Orlandi C, Posokhova E, Masuho I, Ray TA, Hasan N. et al. 2012. GPR158/179 regulate G protein signaling by controlling localization and activity of the RGS7 complexes. J. Cell Biol. 197:711–19 [Google Scholar]
  95. Orlandi C, Xie K, Masuho I, Fajardo-Serrano A, Lujan R, Martemyanov KA. 2015. Orphan receptor GPR158 is an allosteric modulator of RGS7 catalytic activity with an essential role in dictating its expression and localization in the brain. J. Biol. Chem. 290:13622–39 [Google Scholar]
  96. Ou J, Vijayasarathy C, Ziccardi L, Chen S, Zeng Y. et al. 2015. Synaptic pathology and therapeutic repair in adult retinoschisis mouse by AAV-RS1 transfer. J. Clin. Investig. 125:2891–903 [Google Scholar]
  97. Pahlberg J, Sampath AP. 2011. Visual threshold is set by linear and nonlinear mechanisms in the retina that mitigate noise: how neural circuits in the retina improve the signal-to-noise ratio of the single-photon response. BioEssays 33:438–47 [Google Scholar]
  98. Pang J-J, Gao F, Lem J, Bramblett DE, Paul DL, Wu SM. 2010. Direct rod input to cone BCs and direct cone input to rod BCs challenge the traditional view of mammalian BC circuitry. PNAS 107:395–400 [Google Scholar]
  99. Pardue MT, Ball SL, Candille SI, McCall MA, Gregg RG, Peachey NS. 2001. nob: a mouse model of CSNB1. New Insights Into Retinal Degenerative Diseases EA Anderson, MM LaVail, JG Hollyfield 319–28 New York: Kluwer Acad./Plenum Publ. [Google Scholar]
  100. Pardue MT, Faulkner AE, Fernandes A, Yin H, Schaeffel F. et al. 2008. High susceptibility to experimental myopia in a mouse model with a retinal on pathway defect. Investig. Ophthalmol. Vis. Sci. 49:706–12 [Google Scholar]
  101. Patel S, Docampo R. 2009. In with the TRP channels: intracellular functions for TRPM1 and TRPM2. Sci. Signal. 2:pe69 [Google Scholar]
  102. Peachey NS, Pearring JN, Bojang P Jr., Hirschtritt ME, Sturgill-Short G. et al. 2012a. Depolarizing bipolar cell dysfunction due to a Trpm1 point mutation. J. Neurophysiol. 108:2442–51 [Google Scholar]
  103. Peachey NS, Ray TA, Florijn R, Rowe LB, Sjoerdsma T. et al. 2012b. GPR179 is required for depolarizing bipolar cell function and is mutated in autosomal-recessive complete congenital stationary night blindness. Am. J. Hum. Genet. 90:331–39 [Google Scholar]
  104. Pearring JN, Bojang P Jr., Shen Y, Koike C, Furukawa T. et al. 2011. A role for nyctalopin, a small leucine-rich repeat protein, in localizing the TRP melastatin 1 channel to retinal depolarizing bipolar cell dendrites. J. Neurosci. 31:10060–66 [Google Scholar]
  105. Peng Y-W, Robishaw JD, Levine MA, Yau K-W. 1992. Retinal rods and cones have distinct G protein beta and gamma subunits. PNAS 89:10882–86 [Google Scholar]
  106. Penn RD, Hagins WA. 1969. Signal transmission along retinal rods and the origin of the electroretinographic a-wave. Nature 223:201–4 [Google Scholar]
  107. Pillers DA, Bulman DE, Weleber RG, Sigesmund DA, Musarella MA. et al. 1993. Dystrophin expression in the human retina is required for normal function as defined by electroretinography. Nat. Genet. 4:82–86 [Google Scholar]
  108. Pillers DA, Weleber RG, Woodward WR, Green DG, Chapman VM, Ray PN. 1995. mdxCv3 mouse is a model for electroretinography of Duchenne/Becker muscular dystrophy. Investig. Ophthalmol. Vis. Sci. 36:462–66 [Google Scholar]
  109. Poopalasundaram S, Erskine L, Cheetham ME, Hardcastle AJ. 2005. Focus on molecules: nyctalopin. Exp. Eye Res. 81:627–28 [Google Scholar]
  110. Pusch CM, Zeitz C, Brandau O, Pesch K, Achatz H. et al. 2000. The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nat. Genet. 26:324–27 [Google Scholar]
  111. Ramakrishnan H, Dhingra A, Tummala SR, Fina ME, Li JJ. et al. 2015. Differential function of Gγ13 in rod bipolar and ON cone bipolar cells. J. Physiol. 593:1531–50 [Google Scholar]
  112. Rao A, Dallman R, Henderson S, Chen CK. 2007. Gβ5 is required for normal light responses and morphology of retinal ON-bipolar cells. J. Neurosci. 27:14199–204 [Google Scholar]
  113. Rao-Mirotznik R, Buchsbaum G, Sterling P. 1998. Transmitter concentration at a three-dimensional synapse. J. Neurophysiol. 80:3163–72 [Google Scholar]
  114. Rao-Mirotznik R, Harkins AB, Buchsbaum G, Sterling P. 1995. Mammalian rod terminal: architecture of a binary synapse. Neuron 14:561–69 [Google Scholar]
  115. Ray TA, Heath KM, Hasan N, Noel JM, Samuels IS. et al. 2014. GPR179 is required for high sensitivity of the mGluR6 signaling cascade in depolarizing bipolar cells. J. Neurosci. 34:6334–43 [Google Scholar]
  116. Ruether K, Feigenspan A, Pirngruber J, Leitges M, Baehr W, Strauss O. 2010. PKCα is essential for the proper activation and termination of rod bipolar cell response. Investig. Ophthalmol. Vis. Sci. 51:6051–58 [Google Scholar]
  117. Sampath AP, Rieke F. 2004. Selective transmission of single photon responses by saturation at the rod-to-rod bipolar synapse. Neuron 41:431–43 [Google Scholar]
  118. Sanes JR, Zipursky SL. 2010. Design principles of insect and vertebrate visual systems. Neuron 66:15–36 [Google Scholar]
  119. Sarria I, Orlandi C, McCall MA, Gregg RG, Martemyanov KA. 2016. Intermolecular interaction between anchoring subunits specify subcellular targeting and function of RGS proteins in retina ON-bipolar neurons. J. Neurosci. 36:2915–25 [Google Scholar]
  120. Sarria I, Pahlberg J, Cao Y, Kolesnikov AV, Kefalov VJ. et al. 2015. Sensitivity and kinetics of signal transmission at the first visual synapse differentially impact visually-guided behavior. eLife 4:e06358 [Google Scholar]
  121. Sato S, Omori Y, Katoh K, Kondo M, Kanagawa M. et al. 2008. Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nat. Neurosci. 11:923–31 [Google Scholar]
  122. Scalabrino ML, Boye SL, Fransen KM, Noel JM, Dyka FM. et al. 2015. Intravitreal delivery of a novel AAV vector targets ON bipolar cells and restores visual function in a mouse model of complete congenital stationary night blindness. Hum. Mol. Genet. 24:6229–39 [Google Scholar]
  123. Schmitz F, Drenckhahn D. 1997a. Dystrophin in the retina. Prog. Neurobiol. 53:547–60 [Google Scholar]
  124. Schmitz F, Drenckhahn D. 1997b. Localization of dystrophin and β-dystroglycan in bovine retinal photoreceptor processes extending into the postsynaptic dendritic complex. Histochem. Cell Biol. 108:249–55 [Google Scholar]
  125. Schneider FM, Mohr F, Behrendt M, Oberwinkler J. 2015. Properties and functions of TRPM1 channels in the dendritic tips of retinal ON-bipolar cells. Eur. J. Cell Biol. 94:420–27 [Google Scholar]
  126. Shen Y, Heimel JA, Kamermans M, Peachey NS, Gregg RG, Nawy S. 2009. A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J. Neurosci. 29:6088–93 [Google Scholar]
  127. Shen Y, Rampino MA, Carroll RC, Nawy S. 2012. G-protein–mediated inhibition of the Trp channel TRPM1 requires the Gβγ dimer. PNAS 109:8752–57 [Google Scholar]
  128. Shiells RA. 1999. Ca2+-induced light adaptation in retinal ON-bipolar cells. Keio J. Med. 48:140–46 [Google Scholar]
  129. Shiells RA, Falk G. 1990. Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proc. Biol. Sci. 242:91–94 [Google Scholar]
  130. Shiells RA, Falk G. 2002. Potentiation of ‘on’ bipolar cell flash responses by dim background light and cGMP in dogfish retinal slices. J. Physiol. 542:211–20 [Google Scholar]
  131. Shim H, Wang C-T, Chen Y-L, Chau VQ, Fu KG. et al. 2012. Defective retinal depolarizing bipolar cells (DBCs) in regulators of G-protein signaling (RGS) 7 and 11 double null mice. J. Biol. Chem. 287:14873–79 [Google Scholar]
  132. Sikkink SK, Biswas S, Parry NR, Stanga PE, Trump D. 2007. X-linked retinoschisis: an update. J. Med. Genet 44:225–32 [Google Scholar]
  133. Slaughter MM, Miller RF. 1983. Bipolar cells in the mudpuppy retina use an excitatory amino acid neurotransmitter. Nature 303:537–38 [Google Scholar]
  134. Smith EL III, Fox DA, Duncan GC. 1991. Refractive-error changes in kitten eyes produced by chronic on-channel blockade. Vis. Res. 31:833–44 [Google Scholar]
  135. Snellman J, Nawy S. 2002. Regulation of the retinal bipolar cell mGluR6 pathway by calcineurin. J. Neurophysiol. 88:1088–96 [Google Scholar]
  136. Snellman J, Nawy S. 2004. cGMP-dependent kinase regulates response sensitivity of the mouse on bipolar cell. J. Neurosci. 24:6621–28 [Google Scholar]
  137. Snow BE, Betts L, Mangion J, Sondek J, Siderovski DP. 1999. Fidelity of G protein β-subunit association by the G protein γ-subunit-like domains of RGS6, RGS7, and RGS11. PNAS 96:6489–94 [Google Scholar]
  138. Sprang SR. 2016. Invited review: activation of G proteins by GTP and the mechanism of Gα-catalyzed GTP hydrolysis. Biopolymers 105:449–62 [Google Scholar]
  139. Takada Y, Vijayasarathy C, Zeng Y, Kjellstrom S, Bush RA, Sieving PA. 2008. Synaptic pathology in retinoschisis knockout (Rs1−/y) mouse retina and modification by rAAV-Rs1 gene delivery. Investig. Ophthalmol. Vis. Sci. 49:3677–86 [Google Scholar]
  140. Tantri A, Vrabec TR, Cu-Unjieng A, Frost A, Annesley WH Jr., Donoso LA. 2004. X-linked retinoschisis: a clinical and molecular genetic review. Surv. Ophthalmol. 49:214–30 [Google Scholar]
  141. Thoreson WB. 2007. Kinetics of synaptic transmission at ribbon synapses of rods and cones. Mol. Neurobiol. 36:205–23 [Google Scholar]
  142. Tomita T. 1965. Electrophysiological study of the mechanisms subserving color coding in the fish retina. Cold Spring Harb. Symp. Quant. Biol. 30:559–66 [Google Scholar]
  143. Trifonov IU. 1968. [Study of synaptic transmission between photoreceptor and horizontal cell by electric stimulations of the retina]. Biofizika 13:809–17 [Google Scholar]
  144. Tsukamoto Y, Morigiwa K, Ueda M, Sterling P. 2001. Microcircuits for night vision in mouse retina. J. Neurosci. 21:8616–23 [Google Scholar]
  145. Tsukamoto Y, Omi N. 2014. Effects of mGluR6-deficiency on photoreceptor ribbon synapse formation: comparison of electron microscopic analysis of serial sections with random sections. Vis. Neurosci. 31:39–46 [Google Scholar]
  146. Tummala SR, Dhingra A, Fina ME, Li JJ, Ramakrishnan H, Vardi N. 2016. Lack of mGluR6-related cascade elements leads to retrograde trans-synaptic effects on rod photoreceptor synapses via matrix-associated proteins. Eur. J. Neurosci. 43:1509–22 [Google Scholar]
  147. Ueda H, Baba T, Terada N, Kato Y, Tsukahara S, Ohno S. 1997. Dystrophin in rod spherules; submembranous dense regions facing bipolar cell processes. Histochem. Cell Biol. 108:243–48 [Google Scholar]
  148. Ueda H, Kobayashi T, Mitsui K, Tsurugi K, Tsukahara S, Ohno S. 1995. Dystrophin localization at presynapse in rat retina revealed by immunoelectron microscopy. Investig. Ophthalmol. Vis. Sci. 36:2318–22 [Google Scholar]
  149. van Genderen MM, Bijveld MM, Claassen YB, Florijn RJ, Pearring JN. et al. 2009. Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. Am. J. Hum. Genet. 85:730–36 [Google Scholar]
  150. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S. et al. 2007. Regulation of capacitative calcium entries by α1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of α1-syntrophin. FASEB J 21:608–17 [Google Scholar]
  151. Vardi N. 1998. Alpha subunit of Go localizes in the dendritic tips of ON bipolar cells. J. Comp. Neurol. 395:43–52 [Google Scholar]
  152. Vardi N, Matesic DF, Manning DR, Liebman PA, Sterling P. 1993. Identification of a G-protein in depolarizing rod bipolar cells. Vis. Neurosci. 10:473–78 [Google Scholar]
  153. Waite A, Brown SC, Blake DJ. 2012. The dystrophin-glycoprotein complex in brain development and disease. Trends Neurosci 35:487–96 [Google Scholar]
  154. Wang H, Su S, Yang M, Hu N, Yao Y. et al. 2016. Association of ZNF644, GRM6, and CTNND2 genes with high myopia in the Han Chinese population: Jiangsu Eye Study. Eye 30:1017–22 [Google Scholar]
  155. Wang T, Montell C. 2007. Phototransduction and retinal degeneration in Drosophila. . Pflüg. Arch. 454:821–47 [Google Scholar]
  156. Wassle H. 2004. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5:747–57 [Google Scholar]
  157. Wassle H, Grunert U, Cook NJ, Molday RS. 1992. The cGMP-gated channel of rod outer segments is not localized in bipolar cells of the mammalian retina. Neurosci. Lett. 134:199–202 [Google Scholar]
  158. Weber BHF, Schrewe H, Molday LL, Gehrig A, White KL. et al. 2002. Inactivation of the murine X-linked juvenile retinoschisis gene, Rs1h, suggests a role of retinoschisin in retinal cell layer organization and synaptic structure. PNAS 99:6222–27 [Google Scholar]
  159. Werblin FS, Dowling JE. 1969. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32:339–55 [Google Scholar]
  160. Willardson BM, Tracy CM. 2012. Chaperone-mediated assembly of G protein complexes. Subcell. Biochem. 63:131–53 [Google Scholar]
  161. Xiong W-H, Duvoisin RM, Adamus G, Jeffrey BG, Gellman C, Morgans CW. 2013. Serum TRPM1 autoantibodies from melanoma associated retinopathy patients enter retinal on-bipolar cells and attenuate the electroretinogram in mice. PLOS ONE 8:e69506 [Google Scholar]
  162. Xiong WH, Pang JJ, Pennesi ME, Duvoisin RM, Wu SM, Morgans CW. 2015. The effect of PKCα on the light response of rod bipolar cells in the mouse retina. Investig. Ophthalmol. Vis. Sci. 56:4961–74 [Google Scholar]
  163. Xu X, Li S, Xiao X, Wang P, Guo X, Zhang Q. 2009. Sequence variations of GRM6 in patients with high myopia. Mol. Vis. 15:2094–100 [Google Scholar]
  164. Xu Y, Dhingra A, Fina ME, Koike C, Furukawa T, Vardi N. 2012. mGluR6 deletion renders the TRPM1 channel in retina inactive. J. Neurophysiol. 107:948–57 [Google Scholar]
  165. Xu Y, Orlandi C, Cao Y, Yang S, Choi CI. et al. 2016. The TRPM1 channel in ON-bipolar cells is gated by both the α and the βγ subunits of the G-protein Go. Sci. Rep. 6:20940 [Google Scholar]
  166. Xu Y, Sulaiman P, Feddersen RM, Liu J, Smith RG, Vardi N. 2008. Retinal ON bipolar cells express a new PCP2 splice variant that accelerates the light response. J. Neurosci. 28:8873–84 [Google Scholar]
  167. Yip SP, Li CC, Yiu WC, Hung WH, Lam WW. et al. 2013. A novel missense mutation in the NYX gene associated with high myopia. Ophthalmic Physiol. Opt. 33:346–53 [Google Scholar]
  168. Zeitz C, Jacobson SG, Hamel CP, Bujakowska K, Neuillé M. et al. 2013. Whole-exome sequencing identifies LRIT3 mutations as a cause of autosomal-recessive complete congenital stationary night blindness. Am. J. Hum. Genet. 92:67–75 [Google Scholar]
  169. Zeitz C, Robson AG, Audo I. 2015. Congenital stationary night blindness: an analysis and update of genotype-phenotype correlations and pathogenic mechanisms. Prog. Retin. Eye Res. 45:58–110 [Google Scholar]
  170. Zeitz C, Scherthan H, Freier S, Feil S, Suckow V. et al. 2003. NYX (nyctalopin on chromosome X), the gene mutated in congenital stationary night blindness, encodes a cell surface protein. Investig. Ophthalmol. Vis. Sci. 44:4184–91 [Google Scholar]
  171. Zhang AJ, Wu SM. 2009. Receptive fields of retinal bipolar cells are mediated by heterogeneous synaptic circuitry. J. Neurosci. 29:789–97 [Google Scholar]
  172. Zhang J, Jeffrey BG, Morgans CW, Burke NS, Haley TL. et al. 2010. RGS7 and -11 complexes accelerate the ON-bipolar cell light response. Investig. Ophthalmol. Vis. Sci. 51:1121–29 [Google Scholar]
  173. Zhang Q, Xiao X, Li S, Jia X, Yang Z. et al. 2007. Mutations in NYX of individuals with high myopia, but without night blindness. Mol. Vis. 13:330–36 [Google Scholar]
  174. Zhou L, Li T, Song X, Li Y, Li H, Dan H. 2015. NYX mutations in four families with high myopia with or without CSNB1. Mol. Vis. 21:213–23 [Google Scholar]
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