Hemoglobin expression and regulation in glaucoma: Insights into retinal ganglion cell oxygenation

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 2, 2010, Pages 907-919

  Tezel, Gülgün ^a   Yang, Xiangjun ^a   Luo, Cheng ^a   Cai, Jian ^a   Kain, Angela D ^a   Powell, David W ^a   Kuehn, Markus H ^b   Pierce, William M ^a  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; HEMOGLOBIN; RECOMBINANT ERYTHROPOIETIN; ALPHA GLOBIN; BETA GLOBIN; EYE PROTEIN; MESSENGER RNA; OXYGEN;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GLAUCOMA; HUMAN; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; INTRAOCULAR HYPERTENSION; MACROGLIA; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTIC NERVE; OXYGENATION; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEOMICS; RAT; RETINA; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BROWN NORWAY RAT; CELL CULTURE; DISEASE MODEL; GENETICS; MASS SPECTROMETRY; METABOLISM; OPTIC DISK; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

AGED; AGED, 80 AND OVER; ALPHA-GLOBINS; ANIMALS; BETA-GLOBINS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; ERYTHROPOIETIN, RECOMBINANT; EYE PROTEINS; GLAUCOMA; HEMOGLOBINS; HUMANS; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; OCULAR HYPERTENSION; OPTIC DISK; OXYGEN; RATS; RATS, INBRED BN; RETINA; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 77449160981     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-4014     Document Type: Article

References (63)

1. Hayreh SS. Pathogenesis of optic nerve damage and visual field defects. In: Heilman K, Richardson KT, eds. Glaucoma, Conceptions of a Disease. Philadelphia: WB Saunders; 1978;104-180.
2. Osborne NN, Melena J, Chidlow G, Wood JP. A hypothesis to explain ganglion cell death caused by vascular insults at the optic nerve head: possible implication for the treatment of glaucoma. Br J Ophthalmol. 2001;85:1252-1259.
3. Cioffi GA. Three common assumptions about ocular blood flow and glaucoma. Surv Ophthalmol. 2001;45(suppl 3):S325-S331; discussion S332-S334.
4. Flammer J, Orgul S, Costa VP, et al. The impact of ocular blood flow in glaucoma. Prog Retin Eye Res. 2002;21:359-393.
5. Werne A, Harris A, Moore D, BenZion I, Siesky B. The circadian variations in systemic blood pressure, ocular perfusion pressure, and ocular blood flow: risk factors for glaucoma? Surv Ophthalmol. 2008;53:559-567.
6. Tezel G, Wax MB. Hypoxia-inducible factor 1alpha in the glaucomatous retina and optic nerve head. Arch Ophthalmol. 2004;122: 1348-1356.
7. Semenza GL. Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol. 1999;15:551-578.
8. Wangsa-Wirawan ND, Linsenmeier RA. Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol. 2003;121:547-557.
9. Riva CE, Sinclair SH, Grunwald JE. Autoregulation of retinal circulation in response to decrease of perfusion pressure. Invest Ophthalmol Vis Sci. 1981;21:34-38.
10. Yu DY, Cringle SJ. Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease. Prog Retin Eye Res. 2001;20:175-208.
11. Mackenzie PJ, Cioffi GA. Vascular anatomy of the optic nerve head. Can J Ophthalmol. 2008;43:308-312.
12. Tezel G, Chauhan BC, LeBlanc RP, Wax MB. Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest Ophthalmol Vis Sci. 2003;44:3025-3033.
13. Edsall JT. Understanding blood and hemoglobin: an example of international relations in science. Perspect Biol Med. 1986;29: S107-S123.
14. Tezel TH, Geng L, Lato EB, et al. Synthesis and secretion of hemoglobin by retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2009;50:1911-1919.
15. Tezel G, Wax MB. Increased production of tumor necrosis factoralpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000;20:8693-8700.
16. Tezel G, Yang X, Cai J. Proteomic identification of oxidatively modified retinal proteins in a chronic pressure-induced rat model of glaucoma. Invest Ophthalmol Vis Sci. 2005;46:3177-3187.
17. Yang X, Luo C, Cai J, Pierce WM, Tezel G. Phosphorylationdependent interaction with 14-3-3 in the regulation of bad trafficking in retinal ganglion cells. Invest Ophthalmol Vis Sci. 2008; 49:2483-2494.
18. Morrison JC, Moore CG, Deppmeier LM, Gold BG, Meshul CK, Johnson EC. A rat model of chronic pressure-induced optic nerve damage. Exp Eye Res. 1997;64:85-96.
19. Tezel G, Luo C, Yang X. Accelerated aging in glaucoma: immunohistochemical assessment of advanced glycation end products in the human retina and optic nerve head. Invest Ophthalmol Vis Sci. 2007;48:1201-1211.
20. Tezel G, Yang X. Caspase-independent component of retinal ganglion cell death, in vitro. Invest Ophthalmol Vis Sci. 2004;45: 4049-4059.
21. Tezel G, Yang X. Comparative gene array analysis of TNF-alphainduced MAPK and NF-kappaB signaling pathways between retinal ganglion cells and glial cells. Exp Eye Res. 2005;81:207-217.
22. Tezel G, Yang X, Luo C, Peng Y, Sun SL, Sun D. Mechanisms of immune system activation in glaucoma: oxidative stress-stimulated antigen presentation by the retina and optic nerve head glia. Invest Ophthalmol Vis Sci. 2007;48:705-714.
23. Mi H, Barres BA. Purification and characterization of astrocyte precursor cells in the developing rat optic nerve. J Neurosci. 1999;19:1049-1061.
24. Yang J, Yang P, Tezel G, Patil RV, Hernandez MR, Wax MB. Induction of HLA-DR expression in human lamina cribrosa astrocytes by cytokines and simulated ischemia. Invest Ophthalmol Vis Sci. 2001;42:365-371.
25. Uriarte SM, Powell DW, Luerman GC, et al. Comparison of proteins expressed on secretory vesicle membranes and plasma membranes of human neutrophils. J Immunol. 2008;180:5575-5581.
26. Powell DW, Weaver CM, Jennings JL, et al. Cluster analysis of mass spectrometry data reveals a novel component of SAGA. Mol Cell Biol. 2004;24:7249-7259.
27. McAfee KJ, Duncan DT, Assink M, Link AJ. Analyzing proteomes and protein function using graphical comparative analysis of tan-dem mass spectrometry results. Mol Cell Proteomics. 2006;5: 1497-1513.
28. Cummins TD, Powell DW. Use of quantitative mass spectrometry analysis in kidney research. Semin Nephrol. 2007;27:574-583.
29. Heller M, Mattou H, Menzel C, Yao X. Trypsin catalyzed 16O-to-18O exchange for comparative proteomics: tandem mass spectrometry comparison using MALDI-TOF, ESI-QTOF, and ESI-ion trap mass spectrometers. J Am Soc Mass Spectrom. 2003;14:704-718.
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods. 2001;25:402-408.
31. Wakabayashi S, Matsubara H, Webster DA. Primary sequence of a dimeric bacterial haemoglobin from Vitreoscilla. Nature. 1986; 322:481-483.
32. Bogusz D, Appleby CA, Landsmann J, Dennis ES, Trinick MJ, Peacock WJ. Functioning haemoglobin genes in non-nodulating plants. Nature. 1988;331:178-180.
33. Poyart C, Wajcman H, Kister J. Molecular adaptation of hemoglobin function in mammals. Respir Physiol. 1992;90:3-17.
34. Blalock EM, Chen KC, Sharrow K, et al. Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci. 2003;23:3807-3819.
35. Ohyagi Y, Yamada T, Goto I. Hemoglobin as a novel protein developmentally regulated in neurons. Brain Res. 1994;635:323-327.
36. Slemmon JR, Hughes CM, Campbell GA, Flood DG. Increased levels of hemoglobin-derived and other peptides in Alzheimer's disease cerebellum. J Neurosci. 1994;14:2225-2235.
37. Wu CW, Liao PC, Yu L, et al. Hemoglobin promotes Abeta oligomer formation and localizes in neurons and amyloid deposits. Neurobiol Dis. 2004;17:367-377.
38. He Y, Hua Y, Liu W, Hu H, Keep RF, Xi G. Effects of cerebral ischemia on neuronal hemoglobin. J Cereb Blood Flow Metab. 2009;29(3):596-605.
39. Liu L, Zeng M, Stamler JS. Hemoglobin induction in mouse macrophages. Proc Natl Acad Sci U S A. 1999;96:6643-6647.
40. Newton DA, Rao KM, Dluhy RA, Baatz JE. Hemoglobin is expressed by alveolar epithelial cells. J Biol Chem. 2006;281:5668-5676.
41. Royer WE Jr. Structures of red blood cell hemoglobins: oxygen carriers in blood and tissues. In: Mangum, CE ed. Advances in Comparative and Environmental Physiology. Vol. 13. Berlin Heidelberg: Springer Verlag; 1992:87-116.
42. Kraus DW, Colacino JM. Extended oxygen delivery from the nerve hemoglobin of tellina alternata (bivalvia). Science. 1986;232:90-92.
43. Vandergon TL, Riggs CK, Gorr TA, Colacino JM, Riggs AF. The mini-hemoglobins in neural and body wall tissue of the nemertean worm, Cerebratulus lacteus. J Biol Chem. 1998;273:16998-17011.
44. Tezel G. Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog Retin Eye Res. 2006;25:490-513.
45. Osborne NN. Pathogenesis of ganglion "cell death" in glaucoma and neuroprotection: focus on ganglion cell axonal mitochondria. Prog Brain Res. 2008;173:339-352.
46. Ruscher K, Freyer D, Karsch M, et al. Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci. 2002;22:10291-10301.
47. Tsai JC, Wu L, Worgul B, Forbes M, Cao J. Intravitreal administration of erythropoietin and preservation of retinal ganglion cells in an experimental rat model of glaucoma. Curr Eye Res. 2005;30: 1025-1031.
48. Fu QL, Wu W, Wang H, Li X, Lee VW, So KF. Up-regulated endogenous erythropoietin/erythropoietin receptor system and exogenous erythropoietin rescue Retinal ganglion cells after chronic ocular hypertension. Cell Mol Neurobiol. 2008;28(2):317-329.
49. Zhong L, Bradley J, Schubert W, et al. Erythropoietin promotes survival of retinal ganglion cells in DBA/2J glaucoma mice. Invest Ophthalmol Vis Sci. 2007;48:1212-1218.
50. Burmester T, Weich B, Reinhardt S, Hankeln T. A vertebrate globin expressed in the brain. Nature. 2000;407:520-523.
51. Schmidt M, Giessl A, Laufs T, Hankeln T, Wolfrum U, Burmester T. How does the eye breathe?-evidence for neuroglobin-mediated oxygen supply in the mammalian retina. J Biol Chem. 2003;278: 1932-1935.
52. Ostojic J, Sakaguchi DS, de Lathouder Y, et al. Neuroglobin and cytoglobin: oxygen-binding proteins in retinal neurons. Invest Ophthalmol Vis Sci. 2006;47:1016-1023.
53. Rajendram R, Rao NA. Neuroglobin in normal retina and retina from eyes with advanced glaucoma. Br J Ophthalmol. 2007;91: 663-666.
54. Herold S, Fago A, Weber RE, Dewilde S, Moens L. Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress. J Biol Chem. 2004;279: 22841-22847.
55. Fago A, Hundahl C, Malte H, Weber RE. Functional properties of neuroglobin and cytoglobin: insights into the ancestral physiological roles of globins. IUBMB Life. 2004;56:689-696.
56. Brunori M, Vallone B. A globin for the brain. FASEB J. 2006;20: 2192-2197.
57. Geuens E, Brouns I, Flamez D, Dewilde S, Timmermans JP, Moens L. A globin in the nucleus! J Biol Chem. 2003;278:30417-30420.
58. Rogers B, Yakopson V, Teng ZP, Guo Y, Regan RF. Heme oxygenase-2 knockout neurons are less vulnerable to hemoglobin toxicity. Free Radic Biol Med. 2003;35:872-881.
59. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5:53-63.
60. Dringen R, Bishop GM, Koeppe M, Dang TN, Robinson SR. The pivotal role of astrocytes in the metabolism of iron in the brain. Neurochem Res. 2007;32(11):1884-1890.
61. Farkas RH, Chowers I, Hackam AS, et al. Increased expression of iron-regulating genes in monkey and human glaucoma. Invest Ophthalmol Vis Sci. 2004;45:1410-1417.
62. Stasi K, Nagel D, Yang X, Ren L, Mittag T, Danias J. Ceruloplasmin upregulation in retina of murine and human glaucomatous eyes. Invest Ophthalmol Vis Sci. 2007;48:727-732.
63. Liu Q, Ju WK, Crowston JG, et al. Oxidative stress is an early event in hydrostatic pressure induced retinal ganglion cell damage. Invest Ophthalmol Vis Sci. 2007;48:4580-4589.