Hypoxic preconditioning and erythropoietin protect retinal neurons from degeneration

Advances in Experimental Medicine and Biology

Volumn 588, Issue , 2006, Pages 119-131

  Grimm, Christian ^a   Wenzel, A ^a   Acar, N ^b   Keller, S ^a   Seeliger, M ^b   Gassmann, Max ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Apoptosis; Blinding disease; Hypoxia inducible factor 1; Overexpression of EPO; Photoreceptor

Indexed keywords

EID: 84934436556     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-0-387-34817-9_11     Document Type: Conference Paper

References (69)

1. Barbe MF, Tytell M, Gower DJ, and Welch WJ. Hyperthermia protects against light damage in the rat retina. Science 241: 1817-1820, 1988.
2. Brinchmann-Hansen O and Myhre K. The effect of hypoxia upon macular recovery time in normal humans. Aviat Space Environ Med 60: 1183-1186, 1989.
3. Camenisch G, Stroka DM, Gassmann M, and Wenger RH. Attenuation of HIF-1 DNA-binding activity limits hypoxia-inducible endothelin-1 expression. Pflugers Arch 443: 240-249, 2001.
4. Camenisch G, Tini M, Chilov D, Kvietikova I, Srinivas V, Caro J, Spielmann P, Wenger RH, and Gassmann M. General applicability of chicken egg yolk antibodies: the performance of IgY immunoglobulins raised against the hypoxia-inducible factor 1alpha. Faseb J l3: 81-88, 1999.
5. Casson RJ, Chidlow G, Wood JP, Vidal-Sanz M, and Osborne NN. The effect of retinal ganglion cell injury on light-induced photoreceptor degeneration. Invest Ophthalmol Vis Sci 45: 685-693, 2004.
6. Casson RJ, Wood JP, Melena J, Chidlow G, and Osborne NN. The effect of ischemic preconditioning on light-induced photoreceptor injury. Invest Ophthalmol Vis Sci 44: 1348-1354, 2003.
7. Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, and Heckenlively JR. Retinal degeneration mutants in the mouse. Vision Res 42: 517-525, 2002.
8. Chen CK, Burns ME, Spencer M, Niemi GA, Chen J, Hurley JB, Baylor DA, and Simon MI. Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96: 3718-3722, 1999.
9. Chen J, Simon MI, Matthes MT, Yasumura D, and LaVail MM. Increased susceptibility to light damage in an arrestin knockout mouse model of Oguchi disease (stationary night blindness). Invest Ophthalmol Vis Sci 40: 2978-2982, 1999.
10. Cideciyan AV, Hood DC, Huang Y, Banin E, Li ZY, Stone EM, Milam AH, and Jacobson SG. Disease sequence from mutant rhodopsin allele to rod and cone photoreceptor degeneration in man. Proc Natl Acad Sci U S A 95: 7103-7108, 1998.
11. Cruickshanks KJ, Klein R, and Klein BE. Sunlight and age-related macular degeneration. The Beaver Dam Eye Study. Arch Ophthalmol 111: 514-518, 1993.
12. Cruickshanks KJ, Klein R, Klein BE, and Nondahl DM. Sunlight and the 5-year incidence of early age-related maculopathy: the beaver dam eye study. Arch Ophthalmol 119: 246-250, 2001.
13. Digicaylioglu M, Bichet S, Marti HH, Wenger RH, Rivas LA, Bauer C, and Gassmann M. Localization of specific erythropoietin binding sites in defined areas of the mouse brain. Proc Natl Acad Sci U S A 92: 3717-3720., 1995.
14. Ehrenreich H, Hasselblatt M, Dembowski C, Cepek L, Lewczuk P, Stiefel M, Rustenbeck HH, Breiter N, Jacob S, Knerlich F, Bohn M, Poser W, Ruther E, Kochen M, Gefeller O, Gleiter C, Wessel TC, De Ryck M, Itri L, Prange H, Cerami A, Brines M, and Siren AL. Erythropoietin therapy for acute stroke is both safe and beneficial. Mol Med 8: 495-505, 2002.
15. Eid T and Brines M. Recombinant human erythropoietin for neuroprotection: what is the evidence? Clin Breast Cancer 3 Suppl 3: S109-115, 2002.
16. Eisen A, Fisman EZ, Rubenfire M, Freimark D, McKechnie R, Tenenbaum A, Motro M, and Adler Y. Ischemic preconditioning: nearly two decades of research. A comprehensive review. Atherosclerosis 172: 201-210, 2004.
17. Gassmann M, Heinicke K, Soliz J, and Ogunshola OO. Non-erythroid functions of erythropoietin. Adv Exp Med Biol 543: 323-330, 2003.
18. Ghezzi P and Brines M. Erythropoietin as an antiapoptotic, tissue-protective cytokine. Cell Death Differ 11 Suppl 1: S37-44, 2004.
19. Goto Y, Peachey NS, Ziroli NE, Seiple WH, Gryczan C, Pepperberg DR, and Naash MI. Rod phototransduction in transgenic mice expressing a mutant opsin gene. J Opt Soc Am A 13: 577-585., 1996.
20. Grimm C, Wenzel A, Groszer M, Mayser H, Seeliger M, Samardzija M, Bauer C, Gassmann M, and Reme CE. HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med 8: 718-724, 2002.
21. Grimm C, Wenzel A, Stanescu D, Samardzija M, Hotop S, Groszer M, Naash M, Gassmann M, and Reme C. Constitutive overexpression of human erythropoietin protects the mouse retina against induced but not inherited retinal degeneration. J Neurosci 24: 5651-5658, 2004.
22. Hafezi F, Grimm C, Simmen BC, Wenzel A, and Reme CE. Molecular ophthalmology: an update on animal models for retinal degenerations and dystrophies. Br J Ophthalmol 84: 922-927, 2000.
23. Hafezi F, Steinbach JP, Marti A, Munz K, Wang ZQ, Wagner EF, Aguzzi A, and Reme CE. The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat Med 3: 346-349, 1997.
24. Hopfl G, Ogunshola O, and Gassmann M. HIFs and tumors - causes and consequences. Am J Physiol Regul Integr Comp Physiol 286: R608-623, 2004.
25. Hopfl G, Ogunshola O, and Gassmann M. Hypoxia and high altitude. The molecular response. Adv Exp Med Biol 543: 89-115, 2003.
26. Huttl S, Michalakis S, Seeliger M, Luo DG, Acar N, Geiger H, Hudl K, Mader R, Haverkamp S, Moser M, Pfeifer A, Gerstner A, Yau KW, and Biel M. Impaired channel targeting and retinal degeneration in mice lacking the cyclic nucleotide-gated channel subunit CNGB1. J Neurosci 25: 130-138, 2005.
27. Jelkmann W. Erythropoietin: structure, control of production, and function. Physiol Rev 72: 449-489., 1992.
28. Jewell UR, Kvietikova I, Scheid A, Bauer C, Wenger RH, and Gassmann M. Induction of HIF-1alpha in response to hypoxia is instantaneous. Faseb J 15: 1312-1314., 2001.
29. Junk AK, Mammis A, Savitz SI, Singh M, Roth S, Malhotra S, Rosenbaum PS, Cerami A, Brines M, and Rosenbaum DM. Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci U S A 99: 10659-10664, 2002.
30. Kaldi I, Martin RE, Huang H, Brush RS, Morrison KA, and Anderson RE. Bright cyclic rearing protects albino mouse retina against acute light-induced apoptosis. Mol Vis 9: 337-344, 2003.
31. Keller C, Grimm C, Wenzel A, Hafezi F, and Reme C. Protective effect of halothane anesthesia on retinal light damage: inhibition of metabolic rhodopsin regeneration. Invest Ophthalmol Vis Sci 42: 476-480, 2001.
32. Kobrick JL, Zwick H, Witt CE, and Devine JA. Effects of extended hypoxia on night vision. Aviat Space Environ Med 55: 191-195, 1984.
33. LaVail MM, Gorrin GM, Yasumura D, and Matthes MT. Increased susceptibility to constant light in nr and pcd mice with inherited retinal degeneration. Invest Ophthalmol Vis Sci 40: 1020-1024, 1999.
34. Leber LL, Roscoe SN, and Southward GM. Mild hypoxia and visual performance with night vision goggles. Aviat Space Environ Med 57: 318-324, 1986.
35. Li F, Cao W, and Anderson RE. Protection of photoreceptor cells in adult rats from light-induced degeneration by adaptation to bright cyclic light. Exp Eye Res 73: 569-577, 2001.
36. Li Y, Roth S, Laser M, Ma JX, and Crosson CE. Retinal preconditioning and the induction of heat-shock protein 27. Invest Ophthalmol Vis Sci 44: 1299-1304, 2003.
37. Liu C, Peng M, Laties AM, and Wen R. Preconditioning with bright light evokes a protective response against light damage in the rat retina. J Neurosci 18: 1337-1344, 1998.
38. Marti HH. Erythropoietin and the hypoxic brain. J Exp Biol 207: 3233-3242, 2004.
39. Marti HH, Wenger RH, Rivas LA, Straumann U, Digicaylioglu M, Henn V, Yonekawa Y, Bauer C, and Gassmann M. Erythropoietin gene expression in human, monkey and murine brain. Eur J Neurosci 8: 666-676., 1996.
40. Marti HJ, Bernaudin M, Bellail A, Schoch H, Euler M, Petit E, and Risau W. Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 156: 965-976., 2000.
41. Nir I, Harrison JM, Liu C, and Wen R. Extended photoreceptor viability by light stress in the RCS rats but not in the opsin P23H mutant rats. Invest Ophthalmol Vis Sci 42: 842-849, 2001.
42. Nir I, Liu C, and Wen R. Light treatment enhances photoreceptor survival in dystrophic retinas of Royal College of Surgeons rats. Invest Ophthalmol Vis Sci 40: 2383-2390, 1999.
43. O'Steen WK, Bare DJ, Tytell M, Morris M, and Gower DJ. Water deprivation protects photoreceptors against light damage. Brain Res 534: 99-105, 1990.
44. Organisciak DT, Li M, Darrow RM, and Farber DB. Photoreceptor cell damage by light in young Royal College of Surgeons rats. Curr Eye Res 19: 188-196, 1999.
45. Ostroy SE, Gaitatzes CG, and Friedmann AL. Hypoxia inhibits rhodopsin regeneration in the excised mouse eye. Invest Ophthalmol Vis Sci 34: 447-452, 1993.
46. Quaschning T, Ruschitzka F, Stallmach T, Shaw S, Morawietz H, Goettsch W, Hermann M, Slowinski T, Theuring F, Hocher B, Luscher TF, and Gassmann M. Erythropoietin-induced excessive erythrocytosis activates the tissue endothelin system in mice. Faseb J 17: 259-261, 2003.
47. Reme CE, Grimm C, Hafezi F, Iseli HP, and Wenzel A. Why study rod cell death in retinal degenerations and how? Doc Ophthalmol 106: 25-29, 2003.
48. Reme CE, Grimm C, Hafezi F, Marti A, and Wenzel A. Apoptotic cell death in retinal degenerations. Prog Retin Eye Res 17: 443-464, 1998.
49. Rex TS, Allocca M, Domenici L, Surace EM, Maguire AM, Lyubarsky A, Cellerino A, Bennett J, and Auricchio A. Systemic but not intraocular Epo gene transfer protects the retina from light-and genetic-induced degeneration. Mol Ther 10: 855-861, 2004.
50. Ruschitzka FT, Wenger RH, Stallmach T, Quaschning T, de Wit C, Wagner K, Labugger R, Kelm M, Noll G, Rulicke T, Shaw S, Lindberg RL, Rodenwaldt B, Lutz H, Bauer C, Luscher TF, and Gassmann M. Nitric oxide prevents cardiovascular disease and determines survival in polyglobulic mice overexpressing erythropoietin. Proc Natl Acad Sci U S A 97: 11609-11613, 2000.
51. Sakanaka M, Wen TC, Matsuda S, Masuda S, Morishita E, Nagao M, and Sasaki R. In vivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci U S A 95: 4635-4640., 1998.
52. Sanyal S and Hawkins RK. Development and degeneration of retina in rds mutant mice: effects of light on the rate of degeneration in albino and pigmented homozygous and heterozygous mutant and normal mice. Vision Res 26: 1177-1185, 1986.
53. Schofield CJ and Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354, 2004.
54. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19: 176-182, 2004.
55. Shibata J, Hasegawa J, Siemens HJ, Wolber E, Dibbelt L, Li D, Katschinski DM, Fandrey J, Jelkmann W, Gassmann M, Wenger RH, and Wagner KF. Hemostasis and coagulation at a hematocrit level of 0.85: functional consequences of erythrocytosis. Blood 101: 4416-4422, 2003.
56. Sieving PA, Chaudhry P, Kondo M, Provenzano M, Wu D, Carison TJ, Bush RA, and Thompson DA. Inhibition of the visual cycle in vivo by 13-cis retinoic acid protects from light damage and provides a mechanism for night blindness in isotretinoin therapy. Proc Natl Acad Sci U S A 98: 1835-1840, 2001.
57. Simons K. Artificial light and early-life exposure in age-related macular degeneration and in cataractogenic phototoxicity. Arch Ophthalmol 111: 297-298, 1993.
58. Stroka DM, Burkhardt T, Desbaillets I, Wenger RH, Neil DA, Bauer C, Gassmann M, and Candinas D. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. Faseb J 15: 2445-2453., 2001.
59. Tan CC, Eckardt KU, Firth JD, and Ratcliffe PJ. Feedback modulation of renal and hepatic erythropoietin mRNA in response to graded anemia and hypoxia. Am J Physiol 263: F474-481, 1992.
60. Taylor HR, Munoz B, West S, Bressler NM, Bressler SB, and Rosenthal FS. Visible light and risk of age-related macular degeneration. Trans Am Ophthalmol Soc 88: 163-173, 1990.
61. Vogel J, Kiessling I, Heinicke K, Stallmach T, Ossent P, Vogel O, Aulmann M, Frietsch T, Schmid-Schonbein H, Kuschinsky W, and Gassmann M. Transgenic mice overexpressing erythropoietin adapt to excessive erythrocytosis by regulating blood viscosity. Blood 102: 2278-2284, 2003.
62. Wagner KF, Katschinski DM, Hasegawa J, Schumacher D, Meller B, Gembruch U, Schramm U, Jelkmann W, Gassmann M, and Fandrey J. Chronic inborn erythrocytosis leads to cardiac dysfunction and premature death in mice overexpressing erythropoietin. Blood 97: 536-542, 2001.
63. Wang M, Lam TT, Tso MO, and Naash MI. Expression of a mutant opsin gene increases the susceptibility of the retina to light damage. Vis Neurosci 14: 55-62, 1997.
64. Wenzel A, Grimm C, Marti A, Kueng-Hitz N, Hafezi F, Niemeyer G, and Reme CE. c-fos controls the "private pathway" of light-induced apoptosis of retinal photoreceptors. J Neurosci 20: 81-88, 2000.
65. Wenzel A, Grimm C, Samardzija M, and Reme CE. The genetic modifier Rpe65Leu(450): effect on light damage susceptibility in c-Fos-deficient mice. Invest Ophthalmol Vis Sci 44: 2798-2802, 2003.
66. Wenzel A, Grimm C, Samardzija M, and Reme CE. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res 24: 275-306, 2005.
67. Wenzel A, Grimm C, Seeliger MW, Jaissle G, Hafezi F, Kretschmer R, Zrenner E, and Reme CE. Prevention of photoreceptor apoptosis by activation of the glucocorticoid receptor. Invest Ophthalmol Vis Sci 42: 1653-1659, 2001.
68. Wenzel A, Reme CE, Williams TP, Hafezi F, and Grimm C. The Rpe65 Leu450Met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci 21: 53-58, 2001.
69. Zhang C, Rosenbaum DM, Shaikh AR, Li Q, Rosenbaum PS, Pelham DJ, and Roth S. Ischemic preconditioning attenuates apoptotic cell death in the rat retina. Invest Ophthalmol Vis Sci 43: 3059-3066, 2002.