Retina-derived microglial cells induce photoreceptor cell death in vitro

Brain Research

Volumn 836, Issue 1-2, 1999, Pages 110-119

  Roque, Rouel S ^a   Rosales, Armando A ^a   Jingjing, Liu ^a   Agarwal, Neeraj ^a   Al Ubaidi, Muayyad R ^b  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Apoptosis; Lactate dehydrogenase; Microglia; Muller cell; Necrosis; Nick end labeling; Photoreceptor cell; Retinal degeneration

Indexed keywords

DNA; LACTATE DEHYDROGENASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; MICROGLIA; MUELLER CELL; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; RAT; RETINA; RETINA DEGENERATION;

ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; APOPTOSIS; BIOLOGICAL MARKERS; CELL DEATH; CELL DIVISION; CELL LINE; IN SITU NICK-END LABELING; L-LACTATE DEHYDROGENASE; MICE; MICE, TRANSGENIC; MICROGLIA; PHOTORECEPTORS, VERTEBRATE; RATS; RETINA;

EID: 0033620899     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01625-X     Document Type: Article

References (40)

1. Agarwal N., Crawford M.J., Krishnamoorthy R., Sheedlo H.J., Roque R.S., Organisciak D.T., Al-Ubaidi M.R. Characterization of an SV40 T-antigen transformed 661 mouse photoreceptor cell line. Invest. Ophthalmol. Visual Sci. 39:1998;S1055.
2. Agarwal N., Jomary C., Jones S.E., O'Rourke K., Chaitin M.H., Wordinger R.J., Murphy B.F. Immunocytochemical colocalization of clusterin in apoptotic photoreceptor cells in retinal degeneration slow rds mutant mouse retinas. Biochem. Biophys. Res. Commun. 225:1996;84-91.
3. Aguirre G.D., Rubin L.F. Rod-cone dysplasia (progressive retinal atrophy) in Irish setters. J. Am. Vet. Med. Assoc. 166:1975;157-164.
4. Al-Ubaidi M.R., Font R.L., Quiambao A.B., Keener M.J., Loiu G.I., Overbeek P.A., Baehr W. Bilateral retinal and brain tumors in transgenic mice expressing simian virus 40 large T-antigen under control of the human interphotoreceptor retinoid-binding protein promoter. J. Cell Biol. 119:1992;1681-1687.
5. Banati R.B., Gehrmann J., Schubert P., Kreutzberg G.W. Cytotoxicity of microglia. Glia. 7:1993;111-118.
6. Berson E.L. Retinitis pigmentosa: unfolding its mystery. Proc. Natl. Acad. Sci. U.S.A. 93:1996;4526-4528.
7. Boje K.M., Arora P.K. Microglia-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death. Brain Res. 587:1992;250-256.
8. Bok D., Hall M.O. The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. J. Cell Biol. 49:1971;664-682.
9. Caley D.W., Johnson C., Liebelt R.A. The postnatal development of the retina in the normal and rodless CBA mouse: a light and electron microscopic study. Am. J. Anat. 133:1972;179-212.
10. Chang G.-Q., Hao Y., Wong F. Apoptosis: the final common pathway of photoreceptor death in rd, rds, and rhodopsin mutant mice. Neuron. 11:1993;595-605.
11. Colton C.A., Gilbert D.L. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Letters. 223:1987;284-288.
12. Donoso L.A., Rodrigues M., Vrabec T.R., Sery T.W., Fong S.L. IRBP: preparation and characterization of site-specific monoclonal antibodies. Curr. Eye Res. 9:1990;357-362.
13. Essner E., Gorrin G. An electron microscopic study of macrophages in rats with inherited retinal dystrophy. Invest. Ophthalmol. Visual Sci. 18:1979;11-24.
14. Farrar G.J., Kenna P., Jordan Kumar-Singh R., Humphries M.M., Sharp E.M., Sheills D.M., Humphries P. A three-base-pair deletion in the peripherin-RDS gene in one form of retinitis pigmentosa. Nature. 354:1991;478-480.
15. Frade J.M., Barde Y.-A. Microglia-derived nerve growth factor causes cell death in the developing retina. Neuron. 20:1998;35-41.
16. Frade J.M., Rodriguez-Tébar A., Barde Y.-A. Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature. 383:1996;166-168.
17. 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.
18. Giulian D., Vaca K., Corpuz M. Brain glia release factors with opposing actions upon neuronal survival. J. Neurosci. 13:1993;29-37.
19. Herron W.L. Jr., Riegel B.W., Myers O.E., Rubin M.L. Retinal dystrophy in the rat: a pigment epithelial disease. Invest. Ophthalmol. 8:1969;595-604.
20. Jacobson M.D., Burne J.F., King M.P., Miyashita T., Reed J.C., Raff M.C. Bcl-2 blocks apoptosis in cells lacking mitochondrial DNA. Nature. 361:1993;365-369.
21. Kajiwara K., Hahn L.B., Mukai S., Travis G.H., Berson E.L., Dryja T.P. Mutations in the human retinal degeneration slow gene in autosomal dominant retinitis pigmentosa. Nature. 354:1991;480-482.
22. Krishnamoorthy R.R., Crawford M.J., Chaturvedi M.M., Jain S.K., Aggarwal B.B., Al-Ubaidi M.R., Agarwal N. Photo-oxidative stress down-modulates the activity of NF-kB via involvement of caspase-1, leading to apoptosis of photoreceptor cells. J. Biol. Chem. 274:1999.
23. M.M. LaVail, The retinal pigment epithelium in mice and rats with inherited retinal degeneration, in: K.M. Zinn, M.F. Marmor (Eds.), The Retinal Pigment Epithelium, Harvard University Press, Cambridge, MA, 1979, pp. 357-380.
24. Lieb W.E., Smith-Lang L., Dua H.S., Christensen A.C., Donoso L.A. Identification of an S-antigen-like molecule in Drosophila melanogaster: an immunohistochemical study. Exp. Eye Res. 53:1991;171-178.
25. Lynch M.P., Nawaz S., Gerschenson L.E. Evidence for soluble factors regulating cell death and cell proliferation in primary cultures of rabbit endometrial cells grown on collagen. Proc. Natl. Acad. Sci. 83:1986;4784-4790.
26. O'Steen W.K., Karcioglu Z.A. Phagocytosis in the light-damaged albino rat eye: light and electron microscopic study. Am. J. Anat. 139:1974;503-518.
27. Papermaster D.S., Schneider B.G., Zorn M.A., Kraenbuhl J.P. Immunocytochemical localization of opsin in outer segments and golgi zones of frog photoreceptors. J. Cell Biol. 77:1978;196-210.
28. Papermaster D.S., Windle J. Death at an early age: apoptosis in inherited retinal degnerations. Invest. Ophthalmol. Visual Sci. 36:1995;977-983.
29. Roque R.S., Agarwal N., Wordinger R.J., Brun A.M., Xue Y., Huang L.C., Nguyen L.P., Shay J.W. Human papillomavirus-16 E6/E7 transfected retinal cell line expresses the Müller cell phenotype. Exp. Eye Res. 64:1997;519-527.
30. Roque R.S., Caldwell R.B. Isolation and culture of retinal microglia. Curr. Eye Res. 12:1993;285-290.
31. Roque R.S., Caldwell R.B., Behzadian M.A. Cultured Müller cells have high levels of epidermal growth factor receptors. Invest. Ophthalmol. Visual Sci. 33:1992;2587-2595.
32. Roque R.S., Imperial C.J., Caldwell R.B. Microglial cells invade the outer retina as photoreceptors degenerate in Royal College of Surgeons rats. Invest. Ophthalmol. Visual Sci. 37:1996;196-203.
33. Rosales A.A., Roque R.S. Microglia-derived cytotoxic factors: Part I. Inhibition of tumor cell growth in vitro. Brain Res. 748:1997;195-204.
34. V. Sarthy, Reactive gliosis in the retinal degenerations, in: R.E. Anderson, J.G. Hollyfield, M.M. LaVail (Eds.), Retinal Degenerations, CRC Press, Boca Raton, FL, 1991, pp. 109-116.
35. Sawada M., Kondo N., Suzumura A., Morunouchi T. Production of tumor necrosis factor-alpha by microglia and astrocytes in culture. Brain Res. 491:1989;394-397.
36. Streit W.J., Graeber M.B., Kreutzberg G.W. Functional plasticity of microglia: a review. Glia. 1:1988;301-310.
37. Thanos S. Sick photoreceptors attract activated microglia from the ganglion cell layer: a model to study the inflammatory cascades in rats with inherited retinal dystrophy. Brain Res. 588:1992;21-28.
38. Thanos S., Richter W. The migratory potential of vitally labelled microglial cells within the retina of rats with hereditary photoreceptor dystrophy. Int. J. Dev. Neurosci. 11:1993;671-680.
39. S. Thanos, W. Richter, H.-J. Thiel, The protective role of microglia-inhibitory factor in the retina suffering of hereditary photoreceptor degeneration, in: U. Pleyer, K. Schmidt, H.-J. Thiel (Eds.), Cell and Tissue Protection in Ophthalmology, Hippokrates, Stuttgart, 1995, pp. 195-203.
40. Tso M.O.M., Zhang C., Abler A.S. Apoptosis leads to photoreceptor degeneration in inherited retinal dystrophy of RCS rats. Invest. Ophthalmol. Visual Sci. 35:1994;2693-2699.