Inducible nitric oxide synthase, Nos2, does not mediate optic neuropathy and retinopathy in the DBA/2J glaucoma model

BMC Neuroscience

Volumn 8, Issue , 2007, Pages

  Libby, Richard T ^a,e   Howell, Gareth R ^a   Pang, Iok Hou ^b   Savinova, Olga V ^a,c   Mehalow, Adrienne K ^a   Barter, Joseph W ^a   Smith, Richard S ^a,c   Clark, Abbot F ^b   John, Simon W M ^a,c,d  

^a JACKSON LABORATORY   (United States)

^b ALCON RESEARCH LTD   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOGUANIDINE; INDUCIBLE NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; RNA; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACKCROSSING; BLOOD VESSEL; CAUTERIZATION; CELL DEGENERATION; CONTROLLED STUDY; DBA 2 MOUSE; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENOTYPE; GLAUCOMA; INCIDENCE; INTRAOCULAR PRESSURE; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; NULL ALLELE; OPTIC NERVE DISEASE; PATHOGENESIS; PROTEIN EXPRESSION; RETINA GANGLION CELL; RETINOPATHY; ANIMAL; DBA MOUSE; DISEASE MODEL; ENZYMOLOGY; METABOLISM; MOUSE; OPTIC DISK; PATHOLOGY; RETINA DISEASE;

ANIMALS; DISEASE MODELS, ANIMAL; GLAUCOMA; INTRAOCULAR PRESSURE; MICE; MICE, INBRED DBA; NITRIC OXIDE SYNTHASE TYPE II; OPTIC DISK; OPTIC NERVE DISEASES; RETINAL DISEASES;

EID: 38349153822     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-8-108     Document Type: Article

References (73)

1. Quigley HA Broman AT The number of people with glaucoma worldwide in 2010 and 2020 Br J Ophthalmol 2006, 90(3):262-267. 10.1136/ bjo.2005.081224 16488940
2. Quigley HA Number of people with glaucoma worldwide Br J Ophthalmol 1996, 80(5):389-393. 505485 8695555 10.1136/bjo.80.5.389
3. Libby RT Gould DB Anderson MG John SW Complex genetics of glaucoma susceptibility Annu Rev Genomics Hum Genet 2005, 6:15-44. 10.1146/ annurev.genom.6.080604.162209 16124852
4. Gordon MO Beiser JA Brandt JD Heuer DK Higginbotham EJ Johnson CA Keltner JL Miller JP Parrish RK 2nd Wilson MR The Ocular Hypertension Treatment Study: Baseline factors that predict the onset of primary open-angle glaucoma Arch Ophthalmol 2002, 120(6):714-720. discussion 829-730 12049575
5. Quigley HA Glaucoma: Macrocosm to microcosm the Friedenwald lecture Invest Ophthalmol Vis Sci 2005, 46(8):2662-2670. 10.1167/iovs.04-1070 16043835
6. Sommer A Tielsch JM Katz J Quigley HA Gottsch JD Javitt J Singh K Relationship between intraocular pressure and primary open angle glaucoma among white and black Americans. The Baltimore Eye Survey Arch Ophthalmol 1991, 109(8):1090-1095. 1867550
7. Leske MC The epidemiology of open-angle glaucoma: A review Am J Epidemiol 1983, 118(2):166-191. 6349332
8. Leske MC Connell AM Wu SY Hyman LG Schachat AP Risk factors for open-angle glaucoma. The Barbados Eye Study Arch Ophthalmol 1995, 113(7):918-924. 7605285
9. Armaly MF Krueger DE Maunder L Becker B Hetherington J Jr Kolker AE Levene RZ Maumenee AE Pollack IP Shaffer RN Biostatistical analysis of the collaborative glaucoma study. I. Summary report of the risk factors for glaucomatous visual-field defects Arch Ophthalmol 1980, 98(12):2163-2171. 7447768
10. Leske MC Heijl A Hussein M Bengtsson B Hyman L Komaroff E Factors for glaucoma progression and the effect of treatment: The early manifest glaucoma trial Arch Ophthalmol 2003, 121(1):48-56. 12523884
11. Kass MA Heuer DK Higginbotham EJ Johnson CA Keltner JL Miller JP Parrish RK 2nd Wilson MR Gordon MO The Ocular Hypertension Treatment Study: A randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma Arch Ophthalmol 2002, 120(6):701-713. 12049574
12. AGIS Investigators 7. The relationship between control of intraocular pressure and visual field deterioration Am J Ophthalmol 2000, 130(4):429-440. 10.1016/S0002-9394(00)00538-9 11024415
13. Brown GC Bal-Price A Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria Mol Neurobiol 2003, 27(3):325-355. 10.1385/MN:27:3:325 12845153
14. Dawson VL Dawson TM Nitric oxide in neurodegeneration Prog Brain Res 1998, 118:215-229. 9932444
15. Sennlaub F Courtois Y Goureau O Inducible nitric oxide synthase mediates retinal apoptosis in ischemic proliferative retinopathy J Neurosci 2002, 22(10):3987-3993. 12019318
16. Neufeld AH Kawai S Das S Vora S Gachie E Connor JR Manning PT Loss of retinal ganglion cells following retinal ischemia: The role of inducible nitric oxide synthase Exp Eye Res 2002, 75(5):521-528. 10.1006/ exer.2002.2042 12457864
17. Hangai M Yoshimura N Hiroi K Mandai M Honda Y Inducible nitric oxide synthase in retinal ischemia-reperfusion injury Exp Eye Res 1996, 63(5):501-509. 10.1006/exer.1996.0140 8994353
18. Geyer O Almog J Lupu-Meiri M Lazar M Oron Y Nitric oxide synthase inhibitors protect rat retina against ischemic injury FEBS Lett 1995, 374(3):399-402. 10.1016/0014-5793(95)01147-7 7589579
19. Koeberle PD Ball AK Nitric oxide synthase inhibition delays axonal degeneration and promotes the survival of axotomized retinal ganglion cells Exp Neurol 1999, 158(2):366-381. 10.1006/exnr.1999.7113 10415143
20. Yuan L Neufeld AH Activated microglia in the human glaucomatous optic nerve head J Neurosci Res 2001, 64(5):523-532. 10.1002/jnr.1104 11391707
21. Neufeld AH Hernandez MR Gonzalez M Nitric oxide synthase in the human glaucomatous optic nerve head Arch Ophthalmol 1997, 115(4):497-503. 9109759
22. Liu B Neufeld AH Expression of nitric oxide synthase-2 (NOS-2) in reactive astrocytes of the human glaucomatous optic nerve head Glia 2000, 30(2):178-186. 10.1002/ (SICI)1098-1136(200004)30:2<178::AID-GLIA7<3.0.CO;2-C 10719359
23. Whitmore AV Libby RT John SW Glaucoma: Thinking in new ways-a role for autonomous axonal self-destruction and other compartmentalised processes? Prog Retin Eye Res 2005, 24(6):639-662. 10.1016/ j.preteyeres.2005.04.004 15953750
24. Quigley HA Sanchez RM Dunkelberger GR L'Hernault NL Baginski TA Chronic glaucoma selectively damages large optic nerve fibers Invest Ophthalmol Vis Sci 1987, 28(6):913-920. 3583630
25. Quigley HA Nickells RW Kerrigan LA Pease ME Thibault DJ Zack DJ Retinal ganglion cell death in experimental glaucoma and after axotomy occurs by apoptosis Invest Ophthalmol Vis Sci 1995, 36(5):774-786. 7706025
26. Quigley HA Addicks EM Chronic experimental glaucoma in primates. II. Effect of extended intraocular pressure elevation on optic nerve head and axonal transport Invest Ophthalmol Vis Sci 1980, 19(2):137-152. 6153173
27. Quigley HA Neuronal death in glaucoma Prog Retin Eye Res 1999, 18(1):39-57. 10.1016/S1350-9462(98)00014-7 9920498
28. Jakobs TC Libby RT Ben Y John SW Masland RH Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice J Cell Biol 2005, 171(2):313-325. 10.1083/jcb.200506099 16247030
29. Anderson DR Hendrickson A Effect of intraocular pressure on rapid axoplasmic transport in monkey optic nerve Invest Ophthalmol 1974, 13(10):771-783. 4137635
30. Quigley HA McKinnon SJ Zack DJ Pease ME Kerrigan-Baumrind LA Kerrigan DF Mitchell RS Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats Invest Ophthalmol Vis Sci 2000, 41(11):3460-3466. 11006239
31. Liu B Neufeld AH Nitric oxide synthase-2 in human optic nerve head astrocytes induced by elevated pressure in vitro Arch Ophthalmol 2001, 119(2):240-245. 11176986
32. Shareef S Sawada A Neufeld AH Isoforms of nitric oxide synthase in the optic nerves of rat eyes with chronic moderately elevated intraocular pressure Invest Ophthalmol Vis Sci 1999, 40(12):2884-2891. 10549648
33. Neufeld AH Das S Vora S Gachie E Kawai S Manning PT Connor JR A prodrug of a selective inhibitor of inducible nitric oxide synthase is neuroprotective in the rat model of glaucoma J Glaucoma 2002, 11(3):221-225. 10.1097/00061198-200206000-00010 12140399
34. Neufeld AH Nitric oxide: A potential mediator of retinal ganglion cell damage in glaucoma Surv Ophthalmol 1999, 43(Suppl 1):S129-135. 10.1016/ S0039-6257(99)00010-7 10416755
35. Pang IH Johnson EC Jia L Cepurna WO Shepard AR Hellberg MR Clark AF Morrison JC Evaluation of inducible nitric oxide synthase in glaucomatous optic neuropathy and pressure-induced optic nerve damage Invest Ophthalmol Vis Sci 2005, 46(4):1313-1321. 10.1167/iovs.04-0829 15790897
36. Kasmala LT Ransom NL Conner JR McKinnon SJ Oral Administration of SC-51, a Nitric Oxide Synthase Inhibitor, Does Not Protect Optic Nerve Axons in a Hypertensive Rat Model of Glaucoma Invest Ophthalmol Vis Sci 2004, 45(5):E-Abstract 904.
37. Chang B Smith RS Hawes NL Anderson MG Zabaleta A Savinova O Roderick TH Heckenlively JR Davisson MT John SW Interacting loci cause severe iris atrophy and glaucoma in DBA/2J mice Nat Genet 1999, 21(4):405-409. 10.1038/7741 10192392
38. Anderson MG Smith RS Hawes NL Zabaleta A Chang B Wiggs JL John SW Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice Nat Genet 2002, 30(1):81-85. 10.1038/ng794 11743578
39. John SW Smith RS Savinova OV Hawes NL Chang B Turnbull D Davisson M Roderick TH Heckenlively JR Essential iris atrophy, pigment dispersion, and glaucoma in DBA/2J mice Invest Ophthalmol Vis Sci 1998, 39(6):951-962. 9579474
40. Libby RT Anderson MG Pang IH Robinson ZH Savinova OV Cosma IM Snow A Wilson LA Smith RS Clark AF Inherited glaucoma in DBA/2J mice: Pertinent disease features for studying the neurodegeneration Vis Neurosci 2005, 22(5):637-648. 16332275
41. John SW Mechanistic insights into glaucoma provided by experimental genetics the cogan lecture Invest Ophthalmol Vis Sci 2005, 46(8):2649-2661. 10.1167/iovs.05-0205 16043833
42. Libby RT Li Y Savinova OV Barter J Smith RS Nickells RW John SW Susceptibility to neurodegeneration in a glaucoma is modified by Bax gene dosage PLoS Genet 2005, 1(1):17-26. 1183523 16103918 10.1371/ journal.pgen.0010004
43. Schlamp CL Li Y Dietz JA Janssen KT Nickells RW Progressive ganglion cell loss and optic nerve degeneration in DBA/2J mice is variable and asymmetric BMC Neurosci 2006, 7:66. 1621073 17018142 10.1186/ 1471-2202-7-66
44. Danias J Lee KC Zamora MF Chen B Shen F Filippopoulos T Su Y Goldblum D Podos SM Mittag T Quantitative analysis of retinal ganglion cell (RGC) loss in aging DBA/2NNia glaucomatous mice: Comparison with RGC loss in aging C57/BL6 mice Invest Ophthalmol Vis Sci 2003, 44(12):5151-5162. 10.1167/iovs.02-1101 14638711
45. Howell GR Libby RT Jakobs TC Smith RS Phalan FC Barter JW Barbay JM Marchant JK Mahesh N Porciatti V Whitmore AV Masland RH John SW Axons of retinal ganglion cells are insulted in the optic nerve early in DBA/2J glaucoma J Cell Biol 2007, 179(7):1523-1537. 10.1083/jcb.200706181 18158332
46. May CA Mittag T Optic nerve degeneration in the DBA/2NNia mouse: Is the lamina cribrosa important in the development of glaucomatous optic neuropathy? Acta Neuropathol (Berl) 2006, 111(2):158-167. 10.1007/ s00401-005-0011-2
47. Belforte N Moreno MC Cymeryng C Bordone M Keller Sarmiento MI Rosenstein RE Effect of ocular hypertension on retinal nitridergic pathway activity Invest Ophthalmol Vis Sci 2007, 48(5):2127-2133. 10.1167/iovs.06-1229 17460271
48. Laubach VE Shesely EG Smithies O Sherman PA Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death Proc Natl Acad Sci USA 1995, 92(23):10688-10692. 40677 7479866 10.1073/pnas.92.23.10688
49. Anderson MG Libby RT Mao M Cosma IM Wilson LA Smith RS John SW Genetic context determines susceptibility to intraocular pressure elevation in a mouse pigmentary glaucoma BMC Biol 2006, 4(1):20. 1543659 16827931 10.1186/1741-7007-4-20
50. Howell GR Libby RT Marchant JK Wilson LA Cosma IM Smith RS Anderson MG John SW Absence of glaucoma in DBA/2J mice homozygous for wild-type versions of Gpnmb and Tyrp1 BMC Genet 2007, 8(1):45. 1937007 17608931 10.1186/1471-2156-8-45
51. Neufeld AH Sawada A Becker B Inhibition of nitric-oxide synthase 2 by aminoguanidine provides neuroprotection of retinal ganglion cells in a rat model of chronic glaucoma Proc Natl Acad Sci USA 1999, 96(17):9944-9948. 22315 10449799 10.1073/pnas.96.17.9944
52. Schuettauf F Rejdak R Walski M Frontczak-Baniewicz M Voelker M Blatsios G Shinoda K Zagorski Z Zrenner E Grieb P Retinal neurodegeneration in the DBA/2J mouse-a model for ocular hypertension Acta Neuropathol (Berl) 2004, 107(4):352-358. 10.1007/s00401-003-0816-9
53. Ortiz PA Garvin JL Cardiovascular and renal control in NOS-deficient mouse models Am J Physiol Regul Integr Comp Physiol 2003, 284(3):R628-638. 12571071
54. Liu B Neufeld AH Activation of epidermal growth factor receptor signals induction of nitric oxide synthase-2 in human optic nerve head astrocytes in glaucomatous optic neuropathy Neurobiol Dis 2003, 13(2):109-123. 10.1016/S0969-9961(03)00010-X 12828935
55. Neufeld AH Liu B Comparison of the signal transduction pathways for the induction of gene expression of nitric oxide synthase-2 in response to two different stimuli Nitric Oxide 2003, 8(2):95-102. 10.1016/ S1089-8603(02)00164-7 12620372
56. Neufeld AH Pharmacologic neuroprotection with an inhibitor of nitric oxide synthase for the treatment of glaucoma Brain Res Bull 2004, 62(6):455-459. 10.1016/j.brainresbull.2003.07.005 15036557
57. 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(1):85-96. 10.1006/exer.1996.0184 9093024
58. Morrison JC Johnson EC Cepurna W Jia L Understanding mechanisms of pressure-induced optic nerve damage Prog Retin Eye Res 2005, 24(2):217-240. 10.1016/j.preteyeres.2004.08.003 15610974
59. Goldblum D Mittag T Prospects for relevant glaucoma models with retinal ganglion cell damage in the rodent eye Vision Res 2002, 42(4):471-478. 10.1016/S0042-6989(01)00194-8 11853763
60. Boland MV Quigley HA Risk factors and open-angle glaucoma: classification and application J Glaucoma 2007, 16(4):406-418. 10.1097/ IJG.0b013e31806540a1 17571004
61. Stefansson E Pedersen DB Jensen PK la Cour M Kiilgaard JF Bang K Eysteinsson T Optic nerve oxygenation Prog Retin Eye Res 2005, 24(3):307-332. 10.1016/j.preteyeres.2004.09.001 15708831
62. Anderson DR Introductory comments on blood flow autoregulation in the optic nerve head and vascular risk factors in glaucoma Surv Ophthalmol 1999, 43(Suppl 1):S5-9. 10.1016/S0039-6257(99)00046-6 10416742
63. Anderson DR Is Ischemia the villain in glaucomatous cupping and atrophy? Controversy in Ophthalmology 1977:312-319.
64. Hulsman CA Vingerling JR Hofman A Witteman JC de Jong PT Blood pressure, arterial stiffness, and open-angle glaucoma: The Rotterdam study Arch Ophthalmol 2007, 125(6):805-812. 10.1001/archopht.125.6.805 17562992
65. Leske MC Wu SY Hennis A Honkanen R Nemesure B BESs Study Group Risk Factors for Incident Open-angle Glaucoma The Barbados Eye Studies Ophthalmology 2008, 115(1):85-93. 10.1016/j.ophtha.2007.03.017 17629563
66. Motallebipour M Rada-Iglesias A Jansson M Wadelius C The promoter of inducible nitric oxide synthase implicated in glaucoma based on genetic analysis and nuclear factor binding Mol Vis 2005, 11:950-957. 16288199
67. Logan JF Chakravarthy U Hughes AE Patterson CC Jackson JA Rankin SJ Evidence for association of endothelial nitric oxide synthase gene in subjects with glaucoma and a history of migraine Invest Ophthalmol Vis Sci 2005, 46(9):3221-3226. 10.1167/iovs.05-0368 16123422
68. Mo JS Anderson MG Gregory M Smith RS Savinova OV Serreze DV Ksander BR Streilein JW John SW By altering ocular immune privilege, bone marrow-derived cells pathogenically contribute to DBA/2J pigmentary glaucoma J Exp Med 2003, 197(10):1335-1344. 10.1084/jem.20022041 12756269
69. Savinova OV Sugiyama F Martin JE Tomarev SI Paigen BJ Smith RS John SW Intraocular pressure in genetically distinct mice: An update and strain survey BMC Genet 2001, 2:12. 48141 11532192 10.1186/1471-2156-2-12
70. John SWM Savinova OV Intraocular Pressure Measurement in Mice: Technical Aspects Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods Boca Raton, FL: CRC Press Smith RS, John SWM, Nishina PM, Sundberg JP 2002:313-320.
71. John SW Hagaman JR MacTaggart TE Peng L Smithes O Intraocular pressure in inbred mouse strains Invest Ophthalmol Vis Sci 1997, 38(1):249-253. 9008647
72. Smith RS Zabeleta A John SW Bechtold LS Ikeda S Relyea MJ Sundberg JP Kao WW-Y Liu C-Y General and Special Histopathology Systematic Evaluation of the Mouse Eye Boca Raton: CRC Press Smith RS 2002:265-297.
73. Anderson MG Libby RT Gould DB Smith RS John SW High-dose radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma Proc Natl Acad Sci USA 2005, 102(12):4566-4571. 555465 15758074 10.1073/ pnas.0407357102