Home LiteratureArticle Details
PMID: 9801367 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Intraocular gene transfer of ciliary neurotrophic factor prevents death and increases responsiveness of rod photoreceptors in the retinal degeneration slow mouse.

Cayouette M, Behn D, Sendtner M, Lachapelle P, Gravel C

Abstract

Several mutations causing both photoreceptor degeneration and malfunction have been identified in humans and animals. Although intraocular injection of trophic factors has been shown to reduce photoreceptor death in a few conditions of rapid photoreceptor loss, it is unclear whether long-term beneficial changes in functional properties of affected photoreceptors can be obtained by treatment with these factors. The rds/rds mouse is a spontaneous mutant bearing a null mutation in the rds/peripherin gene, which is linked to many forms of dominant retinal degenerations in humans. Here, we report that intraocular adenovirus-mediated gene transfer of ciliary neurotrophic factor (CNTF) in this mutant reduces photoreceptor loss, causes a significant increase in the length of photoreceptor segments, and results in a redistribution and an increase in the retinal content of the photopigment rhodopsin. These effects are accompanied by a significant increase in the amplitude of the a- and b-waves of the scotopic electroretinogram. These results suggest that continuous administration of CNTF could potentially be useful for the treatment of some forms of retinal degeneration.

MeSH Terms
Adenoviridae Animals Apoptosis/physiology Ciliary Neurotrophic Factor Disease Models, Animal Electroretinography Gene Transfer Techniques Homozygote Lac Operon Mice Mice, Inbred BALB C Mice, Mutant Strains Nerve Growth Factors/genetics Nerve Tissue Proteins/genetics Retinal Rod Photoreceptor Cells/chemistry,cytology,physiology Retinitis Pigmentosa/genetics,physiopathology Rhodopsin/physiology
Chemicals
Ciliary Neurotrophic Factor Nerve Growth Factors Nerve Tissue Proteins Rhodopsin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cayouette M
Laboratoire de Transfert de Gènes, Centre de Recherche Université Laval Robert-Giffard, Beauport, Québec, Canada, G1J 2G3.
Behn D
Sendtner M
Lachapelle P
Gravel C
References (59)
59 references, click to expand
  1. Immunocytochemical localization of opsin in the cell membrane of developing rat retinal photoreceptors.
    J Cell Biol. 1984 May;98(5):1788-95 PMID: 6233288
  2. Apoptotic photoreceptor cell death in mouse models of retinitis pigmentosa.
    Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):974-8 PMID: 8302876
  3. Choroid coat extract and ciliary neurotrophic factor strongly promote neurite outgrowth in the embryonic chick retina.
    Int J Dev Neurosci. 1994 Oct;12(6):567-78 PMID: 7892786
  4. Ciliary neurotrophic factor promotes chick photoreceptor development in vitro.
    Development. 1995 Aug;121(8):2695-706 PMID: 7671829
  5. Postnatal development of photoreceptor-specific proteins in mice with hereditary retinal degeneration. An immunocytochemical study.
    Exp Biol. 1990;48(6):305-12 PMID: 2142100
  6. Ciliary neurotrophic factor stimulates neurite outgrowth from spinal cord neurons.
    J Comp Neurol. 1996 Jan 01;364(1):68-77 PMID: 8789276
  7. CNTF exerts opposite effects on in vitro development of rat and chick photoreceptors.
    Neuroreport. 1996 Feb 29;7(3):697-700 PMID: 8733724
  8. Rhodopsin, 11-cis vitamin A, and interstitial retinol-binding protein (IRBP) during retinal development in normal and rd mutant mice.
    Dev Biol. 1986 Aug;116(2):431-8 PMID: 3732615
  9. The neurotrophins and CNTF: two families of collaborative neurotrophic factors.
    Annu Rev Neurosci. 1996;19:491-515 PMID: 8833452
  10. The development of the rod photoresponse from dark-adapted rats.
    Invest Ophthalmol Vis Sci. 1995 May;36(6):1038-45 PMID: 7730013
  11. Rod and cone system contributions to oscillatory potentials: an explanation for the conditioning flash effect.
    Vision Res. 1987;27(6):859-66 PMID: 3499028
  12. Leukemia inhibitory factor and ciliary neurotrophic factor regulate dendritic growth in cultures of rat sympathetic neurons.
    Brain Res Dev Brain Res. 1997 Dec 19;104(1-2):101-10 PMID: 9466712
  13. Ciliary neurotrophic factor, unlike nerve growth factor, supports neurite outgrowth but not synapse formation by adult Lymnaea neurons.
    J Neurobiol. 1996 Mar;29(3):293-303 PMID: 8907159
  14. Photoreceptor cell rescue in retinal degeneration (rd) mice by in vivo gene therapy.
    Nat Med. 1996 Jun;2(6):649-54 PMID: 8640555
  15. Heterologous expression of photoreceptor peripherin/rds and Rom-1 in COS-1 cells: assembly, interactions, and localization of multisubunit complexes.
    Biochemistry. 1995 Oct 31;34(43):14213-9 PMID: 7578020
  16. Basic fibroblast growth factor and local injury protect photoreceptors from light damage in the rat.
    J Neurosci. 1992 Sep;12(9):3554-67 PMID: 1527595
  17. In vivo transfer of a reporter gene to the retina mediated by an adenoviral vector.
    Invest Ophthalmol Vis Sci. 1994 Apr;35(5):2543-9 PMID: 8163343
  18. A new speculum electrode for electroretinography.
    J Neurosci Methods. 1990 Jun;32(3):245-9 PMID: 2385141
  19. Cloning of the cDNA for a novel photoreceptor membrane protein (rom-1) identifies a disk rim protein family implicated in human retinopathies.
    Neuron. 1992 Jun;8(6):1171-84 PMID: 1610568
  20. Mice lacking the CNTF receptor, unlike mice lacking CNTF, exhibit profound motor neuron deficits at birth.
    Cell. 1995 Oct 20;83(2):313-22 PMID: 7585948
  21. Müller-cell-derived leukaemia inhibitory factor arrests rod photoreceptor differentiation at a postmitotic pre-rod stage of development.
    Development. 1997 Jun;124(12):2345-54 PMID: 9199361
  22. Mammalian retinal pigment epithelial cells in vitro respond to the neurokines ciliary neurotrophic factor and leukemia inhibitory factor.
    Biochem Cell Biol. 1997;75(2):119-25 PMID: 9250359
  23. Phenotype correction in retinal pigment epithelium in murine mucopolysaccharidosis VII by adenovirus-mediated gene transfer.
    Proc Natl Acad Sci U S A. 1995 Aug 15;92(17):7700-4 PMID: 7644479
  24. Regional distribution, developmental changes, and cellular localization of CNTF-mRNA and protein in the rat brain.
    J Cell Biol. 1991 Oct;115(2):447-59 PMID: 1918150
  25. Peripherin. A rim-specific membrane protein of rod outer segment discs.
    Invest Ophthalmol Vis Sci. 1987 Jan;28(1):50-61 PMID: 2433249
  26. The oscillatory potentials in response to stimuli of photopic intensities delivered in dark-adaptation: an explanation for the conditioning flash effect.
    Vision Res. 1990;30(4):503-13 PMID: 2339504
  27. Light-induced binding of 48-kDa protein to photoreceptor membranes is highly enhanced by phosphorylation of rhodopsin.
    FEBS Lett. 1984 Oct 29;176(2):473-8 PMID: 6436059
  28. Generation and analysis of transgenic mice expressing P216L-substituted rds/peripherin in rod photoreceptors.
    Invest Ophthalmol Vis Sci. 1997 Feb;38(2):498-509 PMID: 9040483
  29. The effect of peripherin/rds haploinsufficiency on rod and cone photoreceptors.
    J Neurosci. 1997 Nov 1;17(21):8118-28 PMID: 9334387
  30. Diffusible rod-promoting signals in the developing rat retina.
    Development. 1992 Apr;114(4):899-906 PMID: 1618151
  31. The relation of retinal sensitivity and rhodopsin in developing rat retina.
    Invest Ophthalmol Vis Sci. 1984 Jun;25(6):647-51 PMID: 6724834
  32. Adenovirus vector-mediated in vivo gene transfer into adult murine retina.
    Invest Ophthalmol Vis Sci. 1994 Apr;35(5):2535-42 PMID: 8163342
  33. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor.
    Nature. 1990 Sep 6;347(6288):83-6 PMID: 2168521
  34. FK506 immunosuppression to control the immune reactions triggered by first-generation adenovirus-mediated gene transfer.
    Hum Gene Ther. 1995 Nov;6(11):1391-401 PMID: 8573612
  35. Molecular genetics of retinitis pigmentosa.
    Hum Mol Genet. 1995;4 Spec No:1739-43 PMID: 8541873
  36. Postmitotic cells fated to become rod photoreceptors can be respecified by CNTF treatment of the retina.
    Development. 1997 Mar;124(5):1055-67 PMID: 9056780
  37. Defective subunit assembly underlies a digenic form of retinitis pigmentosa linked to mutations in peripherin/rds and rom-1.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13726-30 PMID: 8943002
  38. Mouse models of human disease. Part II: recent progress and future directions.
    Genes Dev. 1997 Jan 1;11(1):11-43 PMID: 9000048
  39. Apoptosis: final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice.
    Neuron. 1993 Oct;11(4):595-605 PMID: 8398150
  40. Evidence for multiple, local functions of ciliary neurotrophic factor (CNTF) in retinal development: expression of CNTF and its receptors and in vitro effects on target cells.
    J Neurochem. 1997 Mar;68(3):979-90 PMID: 9048743
  41. Immunocytochemical localization of opsin in the inner segment and ciliary plasma membrane of photoreceptors in retinas of rds mutant mice.
    Invest Ophthalmol Vis Sci. 1986 May;27(5):836-40 PMID: 2939037
  42. Development and degeneration of retina in rds mutant mice: electron microscopy.
    J Comp Neurol. 1984 Mar 20;224(1):71-84 PMID: 6715580
  43. A comparative study of methods of photoreceptor morphometry.
    Invest Ophthalmol Vis Sci. 1991 Feb;32(2):280-4 PMID: 1993578
  44. Multiple growth factors, cytokines, and neurotrophins rescue photoreceptors from the damaging effects of constant light.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11249-53 PMID: 1454803
  45. Molecular cloning, membrane topology, and localization of bovine rom-1 in rod and cone photoreceptor cells.
    Invest Ophthalmol Vis Sci. 1996 Feb;37(2):352-62 PMID: 8603840
  46. Monoclonal antibodies to rhodopsin: characterization, cross-reactivity, and application as structural probes.
    Biochemistry. 1983 Feb 1;22(3):653-60 PMID: 6188482
  47. Adenovirus-mediated gene transfer of ciliary neurotrophic factor can prevent photoreceptor degeneration in the retinal degeneration (rd) mouse.
    Hum Gene Ther. 1997 Mar 1;8(4):423-30 PMID: 9054517
  48. Complete rescue of photoreceptor dysplasia and degeneration in transgenic retinal degeneration slow (rds) mice.
    Neuron. 1992 Jul;9(1):113-9 PMID: 1385966
  49. Rescue of photoreceptor function by AAV-mediated gene transfer in a mouse model of inherited retinal degeneration.
    Gene Ther. 1997 Jul;4(7):683-90 PMID: 9282169
  50. Development and degeneration of retina in rds mutant mice: immunoassay of the rod visual pigment rhodopsin.
    Biochim Biophys Acta. 1990 Jan 29;1033(1):103-9 PMID: 2137350
  51. Intravitreal injections of neurotrophic factors support the survival of axotomized retinal ganglion cells in adult rats in vivo.
    Brain Res. 1993 Feb 5;602(2):304-17 PMID: 8448673
  52. Development and degeneration of retina in rds mutant mice: the electroretinogram.
    Neurosci Lett. 1984 Jul 27;48(2):231-7 PMID: 6483282
  53. Disruption of the CNTF gene results in motor neuron degeneration.
    Nature. 1993 Sep 2;365(6441):27-32 PMID: 8361533
  54. Effects of the neurotrophins and CNTF on developing statoacoustic neurons: comparison with an otocyst-derived factor.
    Dev Biol. 1993 Sep;159(1):353-65 PMID: 8365572
  55. Nerve growth factor delays retinal degeneration in C3H mice.
    Graefes Arch Clin Exp Ophthalmol. 1996 Aug;234 Suppl 1:S96-100 PMID: 8871157
  56. Development and degeneration of retina in rds mutant mice: light microscopy.
    J Comp Neurol. 1980 Nov 1;194(1):193-207 PMID: 7440795
  57. Ciliary neurotrophic factor induces type-2 astrocyte differentiation in culture.
    Nature. 1988 Sep 1;335(6185):70-3 PMID: 3412463
  58. Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy.
    Nature. 1992 Aug 6;358(6386):502-4 PMID: 1641039
  59. Protection of mouse photoreceptors by survival factors in retinal degenerations.
    Invest Ophthalmol Vis Sci. 1998 Mar;39(3):592-602 PMID: 9501871
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
1998-11-15
Pages
9282-93
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6792873
Subset
IM
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]