Home LiteratureArticle Details
PMID: 9334383 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Developmental expression pattern of phototransduction components in mammalian pineal implies a light-sensing function.

Blackshaw S, Snyder SH

Abstract

Whereas the pineal organs of lower vertebrates have been shown to be photosensitive, photic regulation of pineal function in adult mammals is thought be mediated entirely by retinal photoreceptors. Extraretinal regulation of pineal function has been reported in neonatal rodents, although both the site and molecular basis of extraretinal photoreception have remained obscure. In this study we examine the developmental expression pattern of all of the principal components of retinal phototransduction in rat pineal via cRNA in situ hybridization. All of the components needed to reconstitute a functional phototransduction pathway are expressed in the majority of neonatal pinealocytes, although the expression levels of many of these genes decline dramatically during development. These findings strongly support the theory that the neonatal rat pineal itself is photosensitive. In addition, we observe in neonatal pinealocytes the expression of both rod-specific and cone-specific phototransduction components, implying the existence of functionally different subtypes of pinealocytes that express varying combinations of phototransduction enzymes.

MeSH Terms
Animals Animals, Newborn Arrestin/biosynthesis,genetics Calcium-Binding Proteins/biosynthesis,genetics Eye Proteins/biosynthesis,genetics G-Protein-Coupled Receptor Kinase 1 Gene Expression Regulation, Developmental/radiation effects Hippocalcin In Situ Hybridization Ion Channel Gating Light Lipoproteins Mice Mice, Inbred C57BL Models, Biological Nerve Tissue Proteins/biosynthesis,genetics Organ Specificity Phosphoric Diester Hydrolases/biosynthesis,genetics Pineal Gland/cytology,growth & development,metabolism,radiation effects Protein Kinases/biosynthesis,genetics RNA, Messenger/biosynthesis,genetics Rats Rats, Sprague-Dawley Recoverin Retinol-Binding Proteins/biosynthesis,genetics Rhodopsin/biosynthesis,genetics Signal Transduction/physiology,radiation effects Transducin/biosynthesis,genetics
Chemicals
Arrestin Calcium-Binding Proteins Eye Proteins Lipoproteins Nerve Tissue Proteins RNA, Messenger Rcvrn protein, mouse Rcvrn protein, rat Retinol-Binding Proteins interstitial retinol-binding protein Recoverin Hippocalcin Rhodopsin Protein Kinases G-Protein-Coupled Receptor Kinase 1 Grk1 protein, mouse Grk1 protein, rat Phosphoric Diester Hydrolases Transducin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Blackshaw S
Johns Hopkins University School of Medicine, Department of Neuroscience, Baltimore, Maryland 21205, USA.
Snyder S H
References (77)
77 references, click to expand
  1. Rhodopsin kinase inhibition by recoverin. Function of recoverin myristoylation.
    J Biol Chem. 1995 Oct 13;270(41):24127-9 PMID: 7592614
  2. Isolation and characterization of a cDNA encoding the alpha' subunit of human cone cGMP-phosphodiesterase.
    Gene. 1995 Dec 12;166(2):205-11 PMID: 8543163
  3. A comparison of some photoreceptor characteristics in the pineal and retina. II. The Djungarian hamster (Phodopus sungorus).
    J Comp Physiol A. 1989 Aug;165(4):565-72 PMID: 2527978
  4. Neural response mechanisms in the photoreceptive pineal organ of goldfish.
    Comp Biochem Physiol A Comp Physiol. 1986;84(3):467-73 PMID: 2874927
  5. Characterization of the mouse rod transducin alpha subunit gene.
    J Biol Chem. 1989 May 5;264(13):7122-8 PMID: 2708360
  6. Expression of cone transducin, Gz alpha, and other G-protein alpha-subunit messenger ribonucleic acids in pancreatic islets.
    Endocrinology. 1994 Jul;135(1):31-7 PMID: 8013366
  7. The pineal organ as a component of the biological clock. Phylogenetic and ontogenetic considerations.
    Ann N Y Acad Sci. 1994 May 31;719:13-42 PMID: 8010588
  8. SURVEY OF THE DEVELOPMENT AND COMPARATIVE MORPHOLOGY OF THE PINEAL ORGAN.
    Prog Brain Res. 1965;10:3-29 PMID: 14281614
  9. Interphotoreceptor retinoid-binding protein in retinal rod cells and pineal gland.
    Invest Ophthalmol Vis Sci. 1986 May;27(5):844-50 PMID: 3700035
  10. Rhodopsin kinase activity in the mammalian pineal gland and other tissues.
    Science. 1984 Oct 12;226(4671):182-4 PMID: 6091271
  11. Parapinopsin, a novel catfish opsin localized to the parapineal organ, defines a new gene family.
    J Neurosci. 1997 Nov 1;17(21):8083-92 PMID: 9334384
  12. Effects of light and temperature on the pineal gland in suckling rats.
    Neuroendocrinology. 1973-1974;13(4):255-63 PMID: 4779326
  13. Vasoactive intestinal peptide stimulation of cyclic guanosine monophosphate formation: further evidence for a role of nitric oxide synthase and cytosolic guanylate cyclase in rat pinealocytes.
    Endocrinology. 1993 Jun;132(6):2513-7 PMID: 7684978
  14. Molecular cloning and localization of rhodopsin kinase in the mammalian pineal.
    Vis Neurosci. 1997 Mar-Apr;14(2):225-32 PMID: 9147475
  15. Pineal N-acetyltransferase activity in 10-day-old rats: a paradigm for studying the developing circadian system.
    Endocrinology. 1984 Sep;115(3):918-25 PMID: 6745194
  16. Expression of cyclic nucleotide-gated cation channels in non-sensory tissues and cells.
    Neuropharmacology. 1994 Nov;33(11):1275-82 PMID: 7532814
  17. Response patterns and neuronal networks of photosensory pineal organs.
    Arch Histol Cytol. 1989;52 Suppl:469-75 PMID: 2510802
  18. Antagonistic chromatic mechanisms in photoreceptors of the parietal eye of lizards.
    Nature. 1993 Jul 29;364(6436):442-5 PMID: 8332214
  19. Retinal photoreceptor neurons and pinealocytes accumulate mRNA for interphotoreceptor retinoid-binding protein (IRBP).
    FEBS Lett. 1986 Nov 10;208(1):133-7 PMID: 3770208
  20. Different types of pinealocytes as revealed by immunoelectron microscopy of anti-S-antigen and antiopsin binding sites in the pineal organ of toad, frog, hedgehog and bat.
    Exp Biol. 1986;45(1):27-43 PMID: 2937652
  21. Cone arrestin identified by targeting expression of a functional family.
    J Biol Chem. 1994 Feb 11;269(6):4613-9 PMID: 8308033
  22. Circadian serotonin rhythm control: sympathetic and nonsympathetic pathways in rat pineals of different ages.
    Endocrinology. 1969 Nov;85(5):846-8 PMID: 5812129
  23. Recoverin in pineal organs and retinae of various vertebrate species including man.
    Brain Res. 1992 Nov 6;595(1):57-66 PMID: 1467959
  24. Harderian gland: an extraretinal photoreceptor influencing the pineal gland in neonatal rats?
    Science. 1970 Feb 6;167(3919):884-5 PMID: 5410852
  25. Chicken red-sensitive cone visual pigment retains a binding domain for transducin.
    FEBS Lett. 1989 Mar 27;246(1-2):69-72 PMID: 2707441
  26. Development of a circadian rhythm in the activity of pineal serotonin N-acetyltransferase.
    J Neurochem. 1972 May;19(5):1335-41 PMID: 5025129
  27. The electrical responses of the trout pineal photoreceptors to brief and prolonged illumination.
    Prog Brain Res. 1993;95:3-13 PMID: 7684140
  28. Sympathetic regulation of circadian rhythm of serotonin N-acetyltransferase activity in pineal gland of infant rat.
    J Neurochem. 1982 Mar;38(3):797-802 PMID: 7057192
  29. The patterning and onset of opsin expression in vertebrate retinae.
    Curr Opin Neurobiol. 1996 Aug;6(4):542-6 PMID: 8794108
  30. Rhodopsin-like photosensitivity of isolated chicken pineal gland.
    Nature. 1981 Apr 23;290(5808):706-7 PMID: 7219554
  31. Complete cDNA sequences of mouse rod photoreceptor cGMP phosphodiesterase alpha- and beta-subunits, and identification of beta'-, a putative beta-subunit isozyme produced by alternative splicing of the beta-subunit gene.
    FEBS Lett. 1991 Jan 14;278(1):107-14 PMID: 1847109
  32. PENETRATION OF LIGHT INTO THE BRAIN OF MAMMALS.
    Ann N Y Acad Sci. 1964 Sep 10;117:217-27 PMID: 14196642
  33. Molecular cloning, functional expression and chromosomal localization of a human homolog of the cyclic nucleotide-gated ion channel of retinal cone photoreceptors.
    FEBS Lett. 1996 Sep 16;393(2-3):211-5 PMID: 8814292
  34. Cloning and widespread distribution of the rat rod-type cyclic nucleotide-gated cation channel.
    Am J Physiol. 1997 Apr;272(4 Pt 1):C1335-44 PMID: 9142860
  35. Photomechanical coupling in the vertebrate sphincter pupillae.
    Crit Rev Neurobiol. 1989;4(4):325-66 PMID: 2655940
  36. Pinopsin is a chicken pineal photoreceptive molecule.
    Nature. 1994 Nov 3;372(6501):94-7 PMID: 7969427
  37. Mode of action of pineal nerve fibers in frogs.
    J Neurophysiol. 1962 May;25:405-29 PMID: 13886872
  38. Pineal nitric oxide synthase: characteristics, adrenergic regulation and function.
    Brain Res. 1994 Jul 18;651(1-2):160-8 PMID: 7522930
  39. Identification of competitive antagonists of the rod photoreceptor cGMP-gated cation channel: beta-phenyl-1,N2-etheno-substituted cGMP analogues as probes of the cGMP-binding site.
    Biochemistry. 1996 Dec 24;35(51):16815-23 PMID: 8988020
  40. The effect of NO-donors in bovine and rat pineal cells: stimulation of cGMP and cGMP-independent inhibition of melatonin synthesis.
    J Neuroendocrinol. 1995 Mar;7(3):207-14 PMID: 7606247
  41. Neurobiological aspects of extraretinal photoreceptive systems: structure and function.
    Experientia. 1982 Sep 15;38(9):991-6 PMID: 6751862
  42. Rod-opsin immunoreaction in the pineal organ of the pigmented mouse does not indicate the presence of a functional photopigment.
    Cell Tissue Res. 1993 Oct;274(1):71-8 PMID: 8242713
  43. Pineal glands of immature rats: rise and fall in N-acetyltransferase activity in vitro.
    J Neurobiol. 1981 Mar;12(2):167-73 PMID: 6111585
  44. Light-induced changes in pineal gland N-acetyltransferase activity: developmental aspects.
    Neuroendocrinology. 1990 Feb;51(2):139-46 PMID: 2106094
  45. Pinealocyte projections into the mammalian brain revealed with S-antigen antiserum.
    Science. 1986 Feb 14;231(4739):735-7 PMID: 3454660
  46. Molecular, enzymatic and functional properties of rhodopsin kinase from rat pineal gland.
    Vision Res. 1990;30(8):1129-37 PMID: 2402884
  47. Circadian rhythm of serotonin in the pineal body of immunosympathectomized immature rats.
    Science. 1969 Apr 25;164(3878):442-3 PMID: 5777218
  48. Development and regulation of rhodopsin kinase in rat pineal and retina.
    J Neurochem. 1986 Apr;46(4):1176-9 PMID: 3950623
  49. The mammalian pineal expresses the cone but not the rod cyclic GMP phosphodiesterase.
    J Neurochem. 1995 Sep;65(3):1085-92 PMID: 7643086
  50. Immunocytochemical demonstration of retinal S-antigen in the pineal organ of four mammalian species.
    Cell Tissue Res. 1985;239(1):81-5 PMID: 3967288
  51. Two membrane forms of guanylyl cyclase found in the eye.
    Proc Natl Acad Sci U S A. 1995 Jan 17;92(2):602-6 PMID: 7831337
  52. Recoverin immunoreactivity in mammalian cone bipolar cells.
    Vis Neurosci. 1993 Jan-Feb;10(1):1-12 PMID: 8424920
  53. Activation of transducin by a Xenopus short wavelength visual pigment.
    J Biol Chem. 1997 Jan 10;272(2):1095-100 PMID: 8995408
  54. Interstitial retinol-binding protein and cellular retinal-binding protein in the mammalian pineal.
    Vision Res. 1987;27(12):2049-60 PMID: 3447356
  55. Two alternatively spliced forms of the cGMP-gated channel alpha-subunit from cone photoreceptor are expressed in the chick pineal organ.
    J Neurosci. 1996 Dec 1;16(23):7458-68 PMID: 8922401
  56. The mammalian Harderian gland: morphology, biochemistry, function and phylogeny.
    Arch Histol Jpn. 1981 Sep;44(4):299-333 PMID: 7030263
  57. Immunocytochemical demonstration of rod-opsin, S-antigen, and neuron-specific proteins in the human pineal gland.
    Cell Tissue Res. 1992 Mar;267(3):493-8 PMID: 1533347
  58. alpha-Transducin immunoreactivity in retinae and sensory pineal organs of adult vertebrates.
    Proc Natl Acad Sci U S A. 1986 Feb;83(4):912-6 PMID: 3513166
  59. Morphologic evidence of photoreceptor differentiation of pinealocytes in the neonatal rat.
    J Cell Biol. 1975 Jul;66(1):60-75 PMID: 1141380
  60. Cellular mechanism for norepinephrine suppression of pineal photoreceptor-like cell differentiation in rat pineal cultures.
    Dev Biol. 1992 Feb;149(2):440-7 PMID: 1730393
  61. On the presence of different populations of pinealocytes in the mammalian pineal gland.
    J Neural Transm. 1977;40(4):289-304 PMID: 328826
  62. Adrenergic control of pineal N-acetyltransferase activity: developmental aspects.
    Am J Physiol. 1977 Sep;233(3):E141-6 PMID: 910899
  63. Interphotoreceptor retinoid-binding protein (IRBP). Molecular biology and physiological role in the visual cycle of rhodopsin.
    Mol Neurobiol. 1993 Spring;7(1):61-85 PMID: 8318167
  64. Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species.
    Cell Tissue Res. 1985;242(3):645-8 PMID: 2934135
  65. Intracellular dynamic response characteristics of pineal photoreceptors.
    Ophthalmic Res. 1984;16(1-2):119-22 PMID: 6728419
  66. Evidence for a nonretinal pathway of light to the pineal gland of newborn rats.
    Proc Natl Acad Sci U S A. 1966 Aug;56(2):515-20 PMID: 5229974
  67. Origin of the slow potential in the pineal organ of the rainbow trout.
    Vision Res. 1975 Jun;15(6):737-40 PMID: 1138492
  68. Morphological and immunocytochemical heterogeneity of cultured pinealocytes from one-week- and two-month-old rats: planimetric and densitometric investigations.
    J Pineal Res. 1993 Apr;14(3):128-37 PMID: 8336274
  69. Light affects neonatal rat pineal gland N-acetyltransferase activity by an extra-retinal mechanism.
    J Neural Transm Gen Sect. 1990;80(1):67-77 PMID: 2306342
  70. Differential expression of mRNA and protein encoding retinal and pineal S-antigen during the light/dark cycle.
    J Neurochem. 1990 Nov;55(5):1461-73 PMID: 2213004
  71. Cloning and sequencing of the 23 kDa mouse photoreceptor cell-specific protein.
    FEBS Lett. 1992 May 11;302(2):172-6 PMID: 1386025
  72. PHOTOSENSITIVITY OF THE PINEAL ORGAN IN THE TELEOST, SALMO IRIDEUS (GIBBONS).
    Experientia. 1963 Dec 15;19:642-3 PMID: 14099867
  73. Pineal opsin: a nonvisual opsin expressed in chick pineal.
    Science. 1995 Mar 10;267(5203):1502-6 PMID: 7878470
  74. Extraretinal light perception in the sparrow. 3. The eyes do not participate in photoperiodic photoreception.
    Proc Natl Acad Sci U S A. 1970 Sep;67(1):320-5 PMID: 5272320
  75. Isolation and coding sequence of the rat rod opsin gene.
    J Mol Neurosci. 1994 Fall;5(3):207-9 PMID: 7654522
  76. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes.
    Histochemistry. 1993 Dec;100(6):431-40 PMID: 7512949
  77. Extraretinal light perception in the sparrow. II. Photoperiodic stimulation of testis growth.
    Proc Natl Acad Sci U S A. 1968 May;60(1):146-51 PMID: 5241517
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1997-11-01
Pages
8074-82
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6573733
Subset
IM
Grants
NIDA NIH HHS · DA-00074 · United States
NIDA NIH HHS · DA-00266 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]