Overexpression of rod photoreceptor glutamic acid rich protein 2 (GARP2) increases gain and slows recovery in mouse retina

Cell Communication and Signaling

Volumn 12, Issue 1, 2014, Pages

  Sarfare, Shanta ^a,b   McKeown, Alex S ^a   Messinger, Jeffrey ^c   Rubin, Glen ^a,d   Wei, Hongjun ^a,e   Kraft, Timothy W ^a   Pittler, Steven J ^a,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d Impulse Monitoring Inc   (United States)

^e Department of Pathology   (United States)

Author keywords

CGMP gated cation channel; Cngb1a; Phototransduction; Retina; Rod photoreceptor

Indexed keywords

CYCLIC GMP PHOSPHODIESTERASE; GLUTAMIC ACID RICH PROTEIN 2; GUANYLATE CYCLASE; GUANYLATE CYCLASE 1; OPSIN; PERIPHERIN; PERIPHERIN 2; RECEPTOR PROTEIN; UNCLASSIFIED DRUG; MEMBRANE PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ELECTRORETINOGRAPHY; GARP2 GENE; GENE; GENE OVEREXPRESSION; IN VITRO STUDY; MOUSE; NONHUMAN; PHOTOTRANSDUCTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA ROD; ANIMAL; C57BL MOUSE; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; ELECTRORETINOGRAPHY; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, TRANSGENIC; RETINAL ROD PHOTORECEPTOR CELLS;

EID: 84963558663     PISSN: None     EISSN: 1478811X     Source Type: Journal    
DOI: 10.1186/s12964-014-0067-5     Document Type: Article

References (53)

1. Korenbrot JI: Speed, sensitivity, and stability of the light response in rod and cone photoreceptors: facts and models. Prog Retin Eye Res 2012, 31:442-466.
2. Rieke F, Baylor DA: Origin and functional impact of dark noise in retinal cones. Neuron 2000, 26:181-186.
3. Fu Y, Yau KW: Phototransduction in mouse rods and cones. Pflugers Arch 2007, 454:805-819.
4. Luo DG, Yau KW: Rod sensitivity of neonatal mouse and rat. J Gen Physiol 2005, 126:263-269.
5. Yau KW, Hardie RC: Phototransduction motifs and variations. Cell 2009, 139:246-264.
6. Zheng J, Trudeau MC, Zagotta WN: Rod cyclic nucleotide-gated channels have a stoichiometry of three CNGA1 subunits and one CNGB1 subunit. Neuron 2002, 36:891-896.
7. Zhong H, Molday LL, Molday RS, Yau KW: The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature 2002, 420:193-198.
8. Weitz D, Ficek N, Kremmer E, Bauer PJ, Kaupp UB: Subunit stoichiometry of the CNG channel of rod photoreceptors. Neuron 2002, 36:881-889.
9. Ardell MD, Aragon I, Oliveira L, Porche GE, Burke E, Pittler SJ: The beta subunit of human rod photoreceptor cGMP-gated cation channel is generated from a complex transcription unit. FEBS Lett 1996, 389:213-218.
10. Colville CA, Molday RS: Primary structure and expression of the human beta-subunit and related proteins of the rod photoreceptor cGMP-gated channel. J Biol Chem 1996, 271:32968-32974.
11. Ardell MD, Bedsole DL, Schoborg RV, Pittler SJ: Genomic organization of the human rod photoreceptor cGMP-gated cation channel beta-subunit gene. Gene 2000, 245:311-318.
12. Korschen HG, Illing M, Seifert R, Sesti F, Williams A, Gotzes S, Colville C, Muller F, Dose A, Godde M, Molday LL, Kaupp UB: A 240 Kda Protein Represents the Complete Beta-Subunit of the Cyclic Nucleotide-Gated Channel from Rod Photoreceptor. Neuron 1995, 15:627-636.
13. Batra-Safferling R, Abarca-Heidemann K, Korschen HG, Tziatzios C, Stoldt M, Budyak I, Willbold D, Schwalbe H, Klein-Seetharaman J, Kaupp UB: Glutamic acid-rich proteins of rod photoreceptors are natively unfolded. J Biol Chem 2006, 281:1449-1460.
14. Korschen HG, Beyermann M, Muller 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 1999, 400:761-766.
15. Michalakis S, Zong X, Becirovic E, Hammelmann V, Wein T, Wanner KT, Biel M: The glutamic acid-rich protein is a gating inhibitor of cyclic nucleotide-gated channels. J Neurosci 2011, 31:133-141.
16. Poetsch A, Molday LL, Molday RS: The cGMP-gated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes. J Biol Chem 2001, 276:48009-48016.
17. Sugimoto Y, Yatsunami K, Tsujimoto M, Khorana HG, Ichikawa A: The amino acid sequence of a glutamic acid-rich protein from bovine retina as deduced from the cDNA sequence. Proc Natl Acad Sci U S A 1991, 88:3116-3119.
18. Pentia DC, Hosier S, Cote RH: The glutamic acid-rich protein-2 (GARP2) is a high affinity rod photoreceptor phosphodiesterase (PDE6)-binding protein that modulates its catalytic properties. J Biol Chem 2006, 281:5500-5505.
19. Yao W, Cote RH: Regulation of photoreceptor phosphodiesterase (PDE6) by the rod photoreceptor-specific glutamic acid-rich protein 2 (GARP2). FASEB J 2013, 27:1.
20. Tsang SH, Woodruff ML, Chen CK, Yamashita CY, Cilluffo MC, Rao AL, Farber DB, Fain GL: GAP-independent termination of photoreceptor light response by excess gamma subunit of the cGMP-phosphodiesterase. J Neurosci 2006, 26:4472-4480.
21. Tsang SH, Burns ME, Calvert PD, Gouras P, Baylor DA, Goff SP, Arshavsky VY: Role for the target enzyme in deactivation of photoreceptor G protein in vivo. Science 1998, 282:117-121.
22. Lem J, Applebury ML, Falk JD, Flannery JG, Simon MI: Tissue-specific and developmental regulation of rod opsin chimeric genes in transgenic mice. Neuron 1991, 6:201-210.
23. Johnson PA, Peschon JJ, Yelick PC, Palmiter RD, Hecht NB: Sequence homologies in the mouse protamine 1 and 2 genes. Biochim Biophys Acta 1988, 950:45-53.
24. Michon JJ, Li ZL, Shioura N, Anderson RJ, Tso MO: A comparative study of methods of photoreceptor morphometry. Invest Ophthalmol Vis Sci 1991, 32:280-284.
25. LaVail MM: Kinetics of rod outer segment renewal in the developing mouse retina. J Cell Biol 1973, 58:650-661.
26. Nickell S, Park PS, Baumeister W, Palczewski K: Three-dimensional architecture of murine rod outer segments determined by cryoelectron tomography. J Cell Biol 2007, 177:917-925.
27. Lamb TD, Pugh EN Jr: A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. J Physiol 1992, 449:719-758.
28. Hood DC, Birch DG: Assessing abnormal rod photoreceptor activity with the a-wave of the electroretinogram: applications and methods. Doc Ophthalmol 1996, 92:253-267.
29. Vinberg F, Koskelainen A: Calcium sets the physiological value of the dominant time constant of saturated mouse rod photoresponse recovery. PLoS One 2010, 5:e13025.
30. McKeown AS, Kraft TW: Adaptive potentiation in rod photoreceptors after light exposure. J Gen Physiol 2014, 143:733-743.
31. He W, Cowan CW, Wensel TG: RGS9, a GTPase accelerator for phototransduction. Neuron 1998, 20:95-102.
32. Krispel C, Chen D, Melling N, Chen Y, Martemyanov K, Quillinan N, Arshavsky V, Wensel T, Chen C, Burns M: RGS expression rate-limits recovery of rod photoresponses. Neuron 2006, 51:409-416.
33. Tsang SH, Woodruff ML, Janisch KM, Cilluffo MC, Farber DB, Fain GL: Removal of phosphorylation sites of gamma subunit of phosphodiesterase 6 alters rod light response. J Physiol 2007, 579:303-312.
34. Pepperberg D, Cornwall M, Kahlert M, Hofmann K, Jin J, Jones G, Ripps H: Light-dependent delay in the falling phase of the retinal rod photoresponse. Vis Neurosci 1992, 8:9-18.
35. Lamb TD: Gain and kinetics of activation in the G-protein cascade of phototransduction. Proc Natl Acad Sci U S A 1996, 93:566-570.
36. Barlow HB: Increment thresholds at low intensities considered as signal/noise discriminations. J Physiol 1957, 136:469-488.
37. Barlow RB, Birge RR, Kaplan E, Tallent JR: On the molecular origin of photoreceptor noise. Nature 1993, 366:64-66.
38. Rieke F, Baylor DA: Molecular origin of continuous dark noise in rod photoreceptors. Biophys J 1996, 71:2553-2572.
39. Pugh EN Jr, Lamb TD: Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1993, 1141:111-149.
40. Makino CL, Wen XH, Michaud NA, Covington HI, DiBenedetto E, Hamm HE, Lem J, Caruso G: Rhodopsin expression level affects rod outer segment morphology and photoresponse kinetics. PLoS One 2012, 7:e37832.
41. Guo LW, Ruoho AE: N-terminal half of the cGMP phosphodiesterase gamma-subunit contributes to stabilization of the GTPase-accelerating protein complex. J Biol Chem 2011, 286:15260-15267.
42. Fain G, Matthews H, Cornwall M, Koutalos Y: Adaptation in vertebrate photoreceptors. Physiol Rev 2001, 81:118-144.
43. Haber-Pohlmeier S, Abarca-Heidemann K, Korschen HG, Dhiman HK, Heberle J, Schwalbe H, Klein-Seetharaman J, Kaupp UB, Pohlmeier A: Binding of Ca2+ to glutamic acid-rich polypeptides from the rod outer segment. Biophys J 2007, 92:3207-3214.
44. Hood DC, Birch DG: Rod phototransduction in retinitis pigmentosa: estimation and interpretation of parameters derived from the rod a-wave. Invest Ophthalmol Vis Sci 1994, 35:2948-2961.
45. Coleman JA, Kwok MC, Molday RS: Localization, purification, and functional reconstitution of the P4-ATPase Atp8a2, a phosphatidylserine flippase in photoreceptor disc membranes. J Biol Chem 2009, 284:32670-32679.
46. Wu L, Nagasaki T, Sparrow JR: Photoreceptor cell degeneration in Abcr (-/-) mice. Adv Exp Med Biol 2010, 664:533-539.
47. Fulton AB, Rushton WA: Rod ERG of the mudpuppy: effect of dim red backgrounds. Vision Res 1978, 18:785-792.
48. Peachey NS, Alexander KR, Fishman GA: The luminance-response function of the dark-adapted human electroretinogram. Vision Res 1989, 29:263-270.
49. Bush RA, Sieving PA: A proximal retinal component in the primate photopic ERG a-wave. Invest Ophthalmol Vis Sci 1994, 35:635-645.
50. Saszik SM, Robson JG, Frishman LJ: The scotopic threshold response of the dark-adapted electroretinogram of the mouse. J Physiol 2002, 543:899-916.
51. Baylor DA, Nunn BJ, Schnapf JL: The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J Physiol 1984, 357:575-607.
52. Schnapf JL, Kraft TW, Nunn BJ, Baylor DA: Spectral sensitivity of primate photoreceptors. Vis Neurosci 1988, 1:255-261.
53. Zhang Y, Molday LL, Molday RS, Sarfare SS, Woodruff ML, Fain GL, Kraft TW, Pittler SJ: Knockout of GARPs and the beta-subunit of the rod cGMP-gated channel disrupts disk morphogenesis and rod outer segment structural integrity. J Cell Sci 2009, 122:1192-1200.