Manipulations of ACHE gene expression suggest non-catalytic involvement of acetylcholinesterase in the functioning of mammalian photoreceptors but not in retinal degeneration

Molecular Brain Research

Volumn 71, Issue 2, 1999, Pages 137-148

  Broide, Ron S ^a,b   Grifman, Mirta ^a   Loewenstein, Anat ^c   Grisaru, Dan ^c   Timberg, Rina ^a   Stone, Jonathan ^d   Shani, Moshe ^e   Patrick, James W ^b   Soreq, Hermona ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEL AVIV SOURASKY MEDICAL CENTER   (Israel)

^d UNIVERSITY OF SYDNEY   (Australia)

^e VOLCANI CENTER   (Israel)

Author keywords

Cholinesterase inhibitor; Gene, fos; In situ hybridization; Mice, transgenic; Photoreceptor, vertebrate

Indexed keywords

ACETYLCHOLINESTERASE;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; FETUS DEVELOPMENT; GENE EXPRESSION; GENE INDUCTION; HISTOCHEMISTRY; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; ONCOGENE C FOS; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA DEGENERATION; TRANSGENE;

ACETYLCHOLINESTERASE; ADULT; AGING; ANIMALS; CATALYSIS; CHOLINESTERASE INHIBITORS; DNA NUCLEOTIDYLEXOTRANSFERASE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICE; MICE, TRANSGENIC; PHENOTYPE; PHOTORECEPTORS, VERTEBRATE; RETINAL DEGENERATION;

ANIMALIA; EUKARYOTA; MAMMALIA; MURINAE; VERTEBRATA;

EID: 0032693784     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(99)00169-2     Document Type: Article

References (50)

1. Adler T.R. Mechanisms of photoreceptor death in retinal degenerations. From the cell biology of the 1990s to the ophthalmology or the 21st century? Arch. Ophthalmol. 114:1996;79-83.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 215:1990;403-410.
3. Barash I., Nathan M., Kari R., Ilan N., Shani M., Hurwitz D.R. Elements within the beta-lactoglobulin gene inhibit expression of human serum albumin cDNA and minigenes in transfected cells but rescue their expression in the mammary gland of transgenic mice. Nucleic Acids Res. 24:1996;602-610.
4. Beeri R., Andres C., Lev-Lehman E., Timberg R., Huberman T., Shani M., Soreq H. Transgenic expression of human acetylcholinesterase induces progressive cognitive deterioration in mice. Curr. Biol. 5:1995;1063-1071.
5. Blanks J.C., Adinolfi A.M., Lolley R.N. Photoreceptor degeneration and synaptogenesis in retinal-degenerative (rd) mice. J. Comp. Neurol. 156:1974;95-106.
6. Bok D., Young R.W. The renewal of diffusely distributed protein in the outer segments of rods and cones. Vision Res. 12:1972;161-168.
7. Bowes C., Li T., Danciger M., Baxter L.C., Applebury M.L., Farber D.B. Retinal degeneration in the rd mouse is caused by a defect in the beta subunit of rod cGMP-phosphodiesterase. Nature. 347:1990;677-680.
8. Buyukmihci N., Aguirre G.D. Rod disc turnover in the dog. Invest. Ophthalmol. Visual Sci. 15:1975;579-584.
9. Carricaburu P., Lacroix R., Lacroix J. Electroretinographic study of the white mouse intoxicated by organo-phosphorus: mevinphos and malathion. Toxicol. Eur. Res. 3:1981;87-91.
10. Friedman A., Kaufer D., Shemer J., Hendler I., Soreq H., Tur-Kaspa I. Pyridostigmine brain penetration under stress enhances neuronal excitability and induces early immediate transcriptional response. Nat. Med. 2:1996;1382-1385.
11. Gavrieli Y., Sherman Y., Ben Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
12. D. Glick, M. Shapira, H. Soreq, Molecular neurotoxicology implications of acetylcholinesterase inhibition, in: P. Lazarovici, D. Lester (Eds.), Site-Specific Neurotoxicology, Plenum, New York, in press.
13. Goldman A.I. The sensitivity of rat rod outer segment disc shedding to light. Invest. Ophthalmol. Visual Sci. 22:1982;695-700.
14. Greenberger L.M., Besharse J.C. Photoreceptor disc shedding in eyecups: inhibition by deletion of extracellular cations. Invest. Ophthalmol. Visual Sci. 24:1982;1456-1464.
15. Grifman M., Galyam N., Seidman S., Soreq H. Functional redundancy of acetylcholinesterase and neuroligin in mammalian neuritogenesis. Proc. Natl. Acad. Sci. U.S.A. 95:1998;13935-13940.
16. Grisaru D., Lev-Lehman E., Shapira M., Lessing J.B., Eldor A., Eckstein F., Soreq H. Human osteogenesis involves differentiation-dependent increases in the morphogenically-active 3′ alternative splicing variant of acetylcholinesterase. Mol. Cell. Biol. 19:1999;788-795.
17. Gudehithlu K.P., Neff N.H., Hadjiconstantinou M. c-Fos and NGFI-A mRNA of rat retina: evidence for light-induced augmentation and a role for cholinergic and glutamate receptors. Brain Res. 631:1993;77-82.
18. Hafezi F., Steinbach J.P., Marti A., Munz K., Wang Z.Q., Wagner E.F., Aguzzi A., Reme C.E. The absence of c-Fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat. Med. 3:1997;346-349.
19. Holmes C., Jones S.A., Budd T.C., Greenfield S.A. Non-cholinergic, trophic action of recombinant acetylcholinesterase on mid-brain dopaminergic neurons. J. Neurosci. Res. 49:1997;207-218.
20. Hutchins J.B. Acetylcholine as a neurotransmitter in the vertebrate retina. Exp. Eye Res. 45:1987;1-38.
21. Imai H., Miyata M., Uga S., Ishikawa S. Retinal degeneration in rats exposed to an organophosphate pesticide (fenthion). Environ. Res. 30:1983;453-465.
22. Ivanov V.N., Nikolic-Zugic J. Transcription factor activation during signal-induced apoptosis of immature CD4(+)CD8(+) thymocytes, A protective role of c-Fos. J. Biol. Chem. 272:1997;8558-8566.
23. D. Kaufer, A. Friedman, H. Soreq, The vicious circle: long-lasting transcriptional modulation of cholinergic neurotransmission following stress and anticholinesterase exposure, The Neuroscientist, in press.
24. Kaufer D., Friedman A., Seidman S., Soreq H. Acute stress facilitates long-lasting changes in cholinergic gene expression. Nature. 393:1998;373-377.
25. Knapp M.J., Knopman D.S., Solomon P.R., Pendlebury W.W., Davis C.S., Gracon S.I. The Tacrine study group. J. Am. Med. Assoc. 271:1994;985-991.
26. Koenigsberger C., Chiappa S., Brimijoin S. Neurite differentiation is modulated in neuroblastoma cells engineered for altered acetylcholinesterase expression. J. Neurochem. 69:1997;1389-1397.
27. LaVail M.M. Rod outer segment disk shedding in rat retina: relationship to cyclic lighting. Science. 194:1976;1071.
28. Layer P.G., Willbold E. Novel functions of cholinesterases in development, physiology and disease. Prog. Histochem. Cytochem. 29:1995;1-99.
29. Ling J.J., Yu J., Robertson R.T. Sustained inhibition of acetylcholinesterase activity does not disrupt early geniculocortical ingrowth to developing rat visual cortex. Brain Res. Dev. Brain Res. 86:1995;354-358.
30. Madreperia S.A., Johnson M.A., Nakatani K. Electrophysiologic and electroretinographic evidence for photoreceptor dysfunction as a toxic effect of digoxin. Arch. Ophthalmol. 112:1994;807-812.
31. Missler M., Fernandez-Chacon R., Sudhof T.C. The making of neurexins. J. Neurochem. 71:1998;1339-1347.
32. Nakanishi S. Second-order neurons and receptor mechanisms in visual- and olfactory-information processing. Trends Neurosci. 18:1995;359-364.
33. Olive J., Beneddi L. The structural organization of calf retinal photoreceptors derived from freeze-fracture study. Mol. Biol. Rep. 1:1974;245-249.
34. Pittler S.J., Baehr W. Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase beta-subunit gene of the rd mouse. Proc. Natl. Acad. Sci. U.S.A. 88:1991;8322-8326.
35. Ramirez G., Barat A., Donoso J.A., Fernandez H.L. Compartmentalization of acetylcholinesterase in the chick retina. J. Neurosci. Res. 22:1989;297-304.
36. Robitzki A., Mack A., Hoppe U., Chatonnet A., Layer P.G. Regulation of cholinesterase gene expression affects neuronal differentiation as revealed by transfection studies on reaggregating embryonic chicken retinal cells. Eur. J. Neurosci. 9:1997;2394-2405.
37. Roffler-Tarlov S., Brown J.J., Tarlov E., Stolarov J., Chapman D.L., Alexiou M., Papaioannou V.E. Programmed cell death in the absence of c-Fos and c-Jun. Development. 122:1996;1-9.
38. Seidman S., Sternfeld M., Ben Aziz-Aloya R., Timberg, Kaufer-Nachum D., Soreq H. Synaptic and epidermal accumulations of human acetylcholinesterase is encoded by alternative 3′-terminal exons. Mol. Cell. Biol. 15:1995;2993-3002.
39. Sharma K.V., Bigbee J.W. Acetylcholinesterase antibody treatment results in neurite detachment and reduced outgrowth from cultured neurons: further evidence for a cell adhesive role for neuronal acetylcholinesterase. J. Neurosci. Res. 53:1998;454-464.
40. Small D.H., Reed G., Whitefield B., Nurcombe V. Cholinergic regulation of neurite outgrowth from isolated chick sympathetic neurons in culture. J. Neurosci. 15:1995;144-151.
41. Smeyne R.J., Vendrell M., Hayward M., Baker S.J., Miao G.G., Schilling K., Robertson L.M., Curran T., Morgan J.I. Continuous c-Fos expression precedes programmed cell death in vivo. Nature. 363:1993;166-169.
42. Spitznas M., Hogan M.J. Outer segments of photoreceptors and the retinal pigment epithelium interrelationship in the human eye. Arch. Ophthalmol. 84:1970;810-819.
43. Sternfeld M., Ming G., Song H., Sela K., Timberg R., Poo M., Soreq H. Acetylcholinesterase enhances neurite growth and synapse development through alternative contributions of its hydrolytic capacity, core protein, and variable C termini. J. Neurosci. 18:1998;1240-1249.
44. Sternfeld M., Patrick J.D., Soreq H. Position effect variegations and brain-specific silencing in transgenic mice overexpressing human acetylcholinesterase variants. J. Physiol. (Paris). 92:1998;249-256.
45. Stone J., Itin A., Alon T., Pe'er J., Gnessin H., Chan Ling T., Keshet E. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15:1995;4738-4747.
46. Stone J.L., Barlow W.E., Humayun M.Í., de Juan E. Jr., Milam A.H. Morphometric analysis of macular photoreceptors and ganglion cells in retinas with retinitis pigmentosa. Arch. Ophthalmol. 110:1992;1634-1639.
47. Tierstein P.S., O'Brian P.J. The role of ambient lighting in circadian disc shedding in the rod outer segment of the rat retina. Invest. Ophthalmol. Visual Sci. 19:1980;1257-1265.
48. Walloe L. Excitation of photoreceptors. Acta Ophthalmol. (Copenhagen). 47:1969;1163-1175.
49. Young R.W. Cell death during differentiation of the retina in the mouse. J. Comp. Neurol. 229:1984;362-373.
50. Young R.W. The renewal of photoreceptor cell outer segments. J. Cell Biol. 33:1967;61-72.