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PMID: 9050893 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Identification of components of a phosphoinositide signaling pathway in retinal rod outer segments.

Peng YW, Rhee SG, Yu WP, Ho YK, Schoen T, Chader GJ, Yau KW

Abstract

Phototransduction in retinal rods involves a G protein-coupled signaling cascade that leads to cGMP hydrolysis and the closure of cGMP-gated cation channels that are open in darkness, producing a membrane hyperpolarization as the light response. For many years there have also been reports of the presence of a phosphoinositide pathway in the rod outer segment, though its functions and the molecular identities of its components are still unclear. Using immunocytochemistry with antibodies against various phosphoinositide-specific phospholipase C (PLC) isozymes (beta1-4, gamma1-2, and delta1-2), we have found PLCbeta4-like immunoreactivity in rod outer segments. Similar experiments with antibodies against the alpha-subunits of the G(q) family of G proteins, which are known to activate PLCbeta4, have also demonstrated G(alpha11)-like immunoreactivity in this location. Immunoblots of total proteins from whole retina or partially purified rod outer segments with anti-PLCbeta4 and anti-G(alpha11) antibodies gave, respectively, a single protein band of the expected molecular mass, suggesting specific labelings. The retinal locations of the two proteins were also supported by in situ hybridization experiments on mouse retina with probes specific for the corresponding mouse genes. These two proteins, or immunologically identical isoforms, therefore likely mediate the phosphoinositide signaling pathway in the rod outer segment. At present, G(alpha11) or a G(alpha11)-like protein represents the only G protein besides transducin (which mediates phototransduction) identified so far in the rod outer segment. Although absent in the outer segment layer, other PLC isoforms as well as G(alpha q) (another G(q) family member), are present elsewhere in the retina.

MeSH Terms
Animals Blotting, Western Cattle Female GTP-Binding Proteins/metabolism Immunohistochemistry In Situ Hybridization Isoenzymes/immunology,metabolism Phosphatidylinositols/metabolism Phospholipase C beta Rats Retina/metabolism Rod Cell Outer Segment/enzymology,metabolism Signal Transduction/physiology Type C Phospholipases/immunology,metabolism Uterus/enzymology Vision, Ocular
Chemicals
Isoenzymes Phosphatidylinositols Type C Phospholipases Phospholipase C beta Plcb1 protein, mouse Plcb1 protein, rat GTP-Binding Proteins
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Peng Y W
Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Rhee S G
Yu W P
Ho Y K
Schoen T
Chader G J
Yau K W
References (55)
55 references, click to expand
  1. Immunohistochemical localization of a brain isozyme of phospholipase C (PLC III) in astroglia in rat brain.
    Brain Res. 1989 Oct 9;499(1):193-7 PMID: 2804668
  2. Phospholipase C I and II brain isozymes: immunohistochemical localization in neuronal systems in rat brain.
    Proc Natl Acad Sci U S A. 1988 May;85(9):3208-12 PMID: 3362868
  3. Subspecies of arrestin from bovine retina. Equal functional binding to photoexcited rhodopsin but various isoelectric focusing phenotypes in individuals.
    Eur J Biochem. 1990 Oct 24;193(2):459-67 PMID: 2171936
  4. Calcium ion-regulated phospholipase C activity in bovine rod outer segments.
    Biochem Biophys Res Commun. 1990 Nov 30;173(1):283-8 PMID: 2175180
  5. Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminals in the vertebrate retina.
    Neuron. 1991 Apr;6(4):525-31 PMID: 1849721
  6. Diversity of G proteins in signal transduction.
    Science. 1991 May 10;252(5007):802-8 PMID: 1902986
  7. Phosphatidylinositol-stimulated phosphorylation of an inhibitory subunit of cGMP phosphodiesterase in vertebrate rod photoreceptors.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4333-7 PMID: 1852003
  8. G alpha 16, a G protein alpha subunit specifically expressed in hematopoietic cells.
    Proc Natl Acad Sci U S A. 1991 Jul 1;88(13):5587-91 PMID: 1905813
  9. Two alpha subunits of the Gq class of G proteins stimulate phosphoinositide phospholipase C-beta 1 activity.
    FEBS Lett. 1991 Jul 29;286(1-2):214-6 PMID: 1650713
  10. Phospholipase C isozymes in neurons and glial cells in culture: an immunocytochemical and immunochemical study.
    Brain Res. 1991 May 10;548(1-2):35-40 PMID: 1868346
  11. Identification and immunolocalization of phospholipase C in bovine rod outer segments.
    J Neurochem. 1991 Oct;57(4):1405-12 PMID: 1895111
  12. Involvement of protein kinase C in the phosphorylation of rhodopsin.
    J Biol Chem. 1991 Sep 25;266(27):17725-8 PMID: 1917916
  13. Rapid purification and characterization of protein kinase C from bovine retinal rod outer segments.
    Eur J Biochem. 1991 Nov 1;201(3):601-6 PMID: 1935956
  14. The cGMP-gated channel of the rod photoreceptor cell characterization and orientation of the amino terminus.
    J Biol Chem. 1991 Nov 15;266(32):21917-22 PMID: 1718987
  15. Characterization of G-protein alpha subunits in the Gq class: expression in murine tissues and in stromal and hematopoietic cell lines.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10049-53 PMID: 1946421
  16. Immunolocalization of basic fibroblast growth factor and its receptor in adult goldfish retina.
    Exp Neurol. 1992 Jan;115(1):73-8 PMID: 1309455
  17. Reconstitution of agonist-stimulated phosphatidylinositol 4,5-bisphosphate hydrolysis using purified m1 muscarinic receptor, Gq/11, and phospholipase C-beta 1.
    J Biol Chem. 1992 Apr 25;267(12):8081-8 PMID: 1341877
  18. Regulation of inositol phospholipid-specific phospholipase C isozymes.
    J Biol Chem. 1992 Jun 25;267(18):12393-6 PMID: 1319994
  19. Retinal rods and cones have distinct G protein beta and gamma subunits.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10882-6 PMID: 1438293
  20. A third form of the G protein beta subunit. 1. Immunochemical identification and localization to cone photoreceptors.
    J Biol Chem. 1992 Dec 5;267(34):24776-81 PMID: 1447215
  21. Regulation of phospholipase C by G proteins.
    Trends Biochem Sci. 1992 Dec;17(12):502-6 PMID: 1335185
  22. Cloning, sequencing, purification, and Gq-dependent activation of phospholipase C-beta 3.
    J Biol Chem. 1993 Mar 25;268(9):6654-61 PMID: 8454637
  23. Distinctive subtypes of bovine phospholipase C that have preferential expression in the retina and high homology to the norpA gene product of Drosophila.
    Proc Natl Acad Sci U S A. 1993 Jul 1;90(13):6042-6 PMID: 8327481
  24. Rhodopsin is the major in situ substrate of protein kinase C in rod outer segments of photoreceptors.
    J Biol Chem. 1993 Aug 25;268(24):18181-6 PMID: 8349693
  25. Regional distribution and quantitative measurement of the phosphoinositidase C-linked guanine nucleotide binding proteins G11 alpha and Gq alpha in rat brain.
    J Neurochem. 1993 Sep;61(3):845-51 PMID: 8395563
  26. Purification, molecular cloning, and sequencing of phospholipase C-beta 4.
    J Biol Chem. 1993 Oct 5;268(28):21318-27 PMID: 8407970
  27. Phosphorylation of bovine rod photoreceptor cyclic GMP phosphodiesterase.
    Biochem J. 1993 Oct 1;295 ( Pt 1):49-55 PMID: 8216238
  28. Distribution and relative levels of expression of the phosphoinositidase-C-linked G-proteins Gq alpha and G11 alpha: absence of G11 alpha in human platelets and haemopoietically derived cell lines.
    Biochim Biophys Acta. 1993 Nov 7;1179(2):208-12 PMID: 8218363
  29. Phototransduction mechanism in retinal rods and cones. The Friedenwald Lecture.
    Invest Ophthalmol Vis Sci. 1994 Jan;35(1):9-32 PMID: 7507907
  30. Inositol-1,4,5-trisphosphate receptors in the vertebrate retina.
    Curr Eye Res. 1993 Nov;12(11):981-92 PMID: 8306716
  31. Bovine phospholipase C highly homologous to the norpA protein of Drosophila is expressed specifically in cones.
    J Biol Chem. 1994 Feb 4;269(5):3129-31 PMID: 8106345
  32. Activation of phospholipase C beta 4 by heterotrimeric GTP-binding proteins.
    J Biol Chem. 1994 Mar 11;269(10):7593-6 PMID: 8125982
  33. Functional effect of phosphorylation of the photoreceptor phosphodiesterase inhibitory subunit by protein kinase C.
    J Biol Chem. 1994 Apr 1;269(13):9850-6 PMID: 8144577
  34. Phosphoinositide phospholipases and G proteins in hormone action.
    Annu Rev Physiol. 1994;56:349-69 PMID: 8010744
  35. Neuromedin B receptor, expressed in Xenopus laevis oocytes, selectively couples to G alpha q and not G alpha 11.
    FEBS Lett. 1994 Jul 4;348(1):89-92 PMID: 8026589
  36. Regulation of phospholipase C-beta 4 by ribonucleotides and the alpha subunit of Gq.
    J Biol Chem. 1994 Oct 14;269(41):25335-8 PMID: 7929227
  37. Kinetics and localization of the phosphorylation of rhodopsin by protein kinase C.
    J Biol Chem. 1995 Mar 24;270(12):6710-7 PMID: 7896814
  38. Activation by PKC of the Ca(2+)-sensitive guanylyl cyclase in bovine retinal rod outer segments measured with an optical assay.
    Biochemistry. 1995 Apr 11;34(14):4689-95 PMID: 7718573
  39. Molecular cloning and characterization of the G protein gamma subunit of cone photoreceptors.
    J Biol Chem. 1995 Apr 14;270(15):8495-500 PMID: 7721746
  40. Mutants of the visual pathway of Drosophila melanogaster.
    Nature. 1970 Aug 1;227(5257):518-20 PMID: 5428475
  41. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  42. Polyphosphoinositide hydrolysis in response to light stimulation of rat and chick retina and retinal rod outer segments.
    Biochim Biophys Acta. 1988 Jun 30;970(2):205-11 PMID: 2838096
  43. Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction.
    Cell. 1988 Aug 26;54(5):723-33 PMID: 2457447
  44. Cyclic GMP-activated conductance of retinal photoreceptor cells.
    Annu Rev Neurosci. 1989;12:289-327 PMID: 2467600
  45. Brain phospholipase C isozymes: differential mRNA localizations by in situ hybridization.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2923-7 PMID: 2468162
  46. Stimulation of protein phosphorylations in frog rod outer segments by protein kinase activators. Suppression of light-induced changes in membrane current and cGMP by protein kinase C activators.
    J Biol Chem. 1989 May 25;264(15):8857-64 PMID: 2542293
  47. Phosphatidylinositol 4,5-bisphosphate: light-mediated breakdown in the vertebrate retina.
    Biochem Biophys Res Commun. 1984 Oct 30;124(2):503-6 PMID: 6093803
  48. Light-mediated breakdown of phosphatidylinositol-4,5-bisphosphate in isolated rod outer segments of frog photoreceptor.
    Biochem Biophys Res Commun. 1985 Apr 30;128(2):954-9 PMID: 2986631
  49. Phosphorylation of rhodopsin by protein kinase C in vitro.
    J Biol Chem. 1986 Apr 5;261(10):4749-57 PMID: 3007475
  50. Multisite phosphorylation of the alpha subunit of transducin by the insulin receptor kinase and protein kinase C.
    Proc Natl Acad Sci U S A. 1986 Dec;83(24):9294-7 PMID: 3099281
  51. Light induces a rapid and transient increase in inositol-trisphosphate in toad rod outer segments.
    Biochem Biophys Res Commun. 1987 Aug 14;146(3):1392-6 PMID: 3113434
  52. Genetic dissection of the Drosophila nervous system by means of mosaics.
    Proc Natl Acad Sci U S A. 1970 Nov;67(3):1156-63 PMID: 5274445
  53. Purification and characterization of two immunologically distinct phosphoinositide-specific phospholipases C from bovine brain.
    J Biol Chem. 1987 Sep 15;262(26):12511-8 PMID: 3040753
  54. Phorbol ester- and light-induced endogenous phosphorylation of rat rod outer-segment proteins.
    Exp Eye Res. 1987 Oct;45(4):545-56 PMID: 3428384
  55. Phosphatidylinositol-4,5-bisphosphate phospholipase C in bovine rod outer segments.
    Biochemistry. 1990 Jun 12;29(23):5447-52 PMID: 2167127
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1997-03-04
Pages
1995-2000
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC20031
Subset
IM
Grants
NEI NIH HHS · F32 EY006837 · United States
NEI NIH HHS · R01 EY006837 · United States
NEI NIH HHS · R37 EY006837 · United States
NEI NIH HHS · EY06837 · United States
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