Deficiency of complement component 5 ameliorates glaucoma in DBA/2J mice

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Howell, Gareth R ^a   Soto, Ileana ^a   Ryan, Margaret ^a   Graham, Leah C ^a   Smith, Richard S ^a   John, Simon W M ^a,b,c  

^a JACKSON LABORATORY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C5; COMPLEMENT MEMBRANE ATTACK COMPLEX;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; C5 GENE; CELL DEGENERATION; CONTROLLED STUDY; DBA 2 MOUSE; DISEASE SEVERITY; EYE EXAMINATION; GENE; GLAUCOMA; IMMUNOFLUORESCENCE; INTRAOCULAR PRESSURE; MOUSE; NONHUMAN; OPTIC NERVE LESION; PRESSURE MEASUREMENT; PREVALENCE; PROTEIN FUNCTION; RETINA GANGLION CELL;

EID: 84879429446     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-76     Document Type: Article

References (51)

1. Nickells RW, Howell GR, Soto I, John SW. Under pressure: cellular and molecular responses during glaucoma, a common neurodegeneration with axonopathy. Annu Rev Neurosci 2012, 35:153-179. 10.1146/annurev.neuro.051508.135728, 22524788.
2. Burgoyne CF. A biomechanical paradigm for axonal insult within the optic nerve head in aging and glaucoma. Exp Eye Res 2011, 93(2):120-132. 10.1016/j.exer.2010.09.005, 3128181, 20849846.
3. Quigley HA. Glaucoma. Lancet 2011, 377(9774):1367-1377. 10.1016/S0140-6736(10)61423-7, 21453963.
4. Howell GR, Macalinao DG, Sousa GL, Walden M, Soto I, Kneeland SC, Barbay JM, King BL, Marchant JK, Hibbs M, et al. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J Clin Invest 2011, 121(4):1429-1444. 10.1172/JCI44646, 3069778, 21383504.
5. Jha P, Banda H, Tytarenko R, Bora PS, Bora NS. Complement mediated apoptosis leads to the loss of retinal ganglion cells in animal model of glaucoma. Mol Immunol 2011, 48(15-16):2151-2158. 3653641, 21821293.
6. Rosen AM, Stevens B. The role of the classical complement cascade in synapse loss during development and glaucoma. Adv Exp Med Biol 2010, 703:75-93. 10.1007/978-1-4419-5635-4_6, 20711708.
7. Ren L, Danias J. A role for complement in glaucoma?. Adv Exp Med Biol 2010, 703:95-104. 10.1007/978-1-4419-5635-4_7, 20711709.
8. Zipfel PF. Complement and immune defense: from innate immunity to human diseases. Immunol Lett 2009, 126(1-2):1-7.
9. Stevens B, Allen NJ, Vazquez LE, Howell GR, Christopherson KS, Nouri N, Micheva KD, Mehalow AK, Huberman AD, Stafford B, et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131(6):1164-1178. 10.1016/j.cell.2007.10.036, 18083105.
10. Morgan BP. Regulation of the complement membrane attack pathway. Crit Rev Immunol 1999, 19(3):173-198.
11. Nauta AJ, Roos A, Daha MR. A regulatory role for complement in innate immunity and autoimmunity. Int Arch Allergy Immunol 2004, 134(4):310-323. 10.1159/000079261, 15218334.
12. Howell GR, Libby RT, Jakobs TC, Smith RS, Phalan FC, Barter JW, Barbay JM, Marchant JK, Mahesh N, Porciatti V, et al. 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, 2373494, 18158332.
13. 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. 10.1186/1471-2202-7-66, 1621073, 17018142.
14. Soto I, Oglesby E, Buckingham BP, Son JL, Roberson ED, Steele MR, Inman DM, Vetter ML, Horner PJ, Marsh-Armstrong N. Retinal ganglion cells downregulate gene expression and lose their axons within the optic nerve head in a mouse glaucoma model. J Neurosci 2008, 28(2):548-561. 10.1523/JNEUROSCI.3714-07.2008, 18184797.
15. Matsubara A, Nakazawa T, Husain D, Iliaki E, Connolly E, Michaud NA, Gragoudas ES, Miller JW. Investigating the effect of ciliary body photodynamic therapy in a glaucoma mouse model. Invest Ophthalmol Vis Sci 2006, 47(6):2498-2507. 10.1167/iovs.05-0959, 16723462.
16. Schuettauf F, Quinto K, Naskar R, Zurakowski D. Effects of anti-glaucoma medications on ganglion cell survival: the DBA/2J mouse model. Vision Res 2002, 42(20):2333-2337. 10.1016/S0042-6989(02)00188-8, 12350421.
17. Wong AA, Brown RE. A neurobehavioral analysis of the prevention of visual impairment in the DBA/2J mouse model of glaucoma. Invest Ophthalmol Vis Sci 2012, 53(9):5956-5966. 10.1167/iovs.12-10020, 22859742.
18. Panagis L, Zhao X, Ge Y, Ren L, Mittag TW, Danias J. Retinal gene expression changes related to IOP exposure and axonal loss in DBA/2J mice. Invest Ophthalmol Vis Sci 2011, 52(11):7807-7816. 10.1167/iovs.10-7063, 3335131, 21908583.
19. Steele MR, Inman DM, Calkins DJ, Horner PJ, Vetter ML. Microarray analysis of retinal gene expression in the DBA/2J model of glaucoma. Invest Ophthalmol Vis Sci 2006, 47(3):977-985. 10.1167/iovs.05-0865, 16505032.
20. Itagaki S, Akiyama H, Saito H, McGeer PL. Ultrastructural localization of complement membrane attack complex (MAC)-like immunoreactivity in brains of patients with Alzheimer's disease. Brain Res 1994, 645(1-2):78-84.
21. McGeer PL, Akiyama H, Itagaki S, McGeer EG. Activation of the classical complement pathway in brain tissue of Alzheimer patients. Neurosci Lett 1989, 107(1-3):341-346.
22. Webster S, Lue LF, Brachova L, Tenner AJ, McGeer PL, Terai K, Walker DG, Bradt B, Cooper NR, Rogers J. Molecular and cellular characterization of the membrane attack complex, C5b-9, in Alzheimer's disease. Neurobiol Aging 1997, 18(4):415-421. 10.1016/S0197-4580(97)00042-0, 9330973.
23. Singhrao SK, Neal JW, Morgan BP, Gasque P. Increased complement biosynthesis by microglia and complement activation on neurons in Huntington's disease. Exp Neurol 1999, 159(2):362-376. 10.1006/exnr.1999.7170, 10506508.
24. Liu L, Lioudyno M, Tao R, Eriksson P, Svensson M, Aldskogius H. Hereditary absence of complement C5 in adult mice influences Wallerian degeneration, but not retrograde responses, following injury to peripheral nerve. J Peripher Nerv Syst 1999, 4(2):123-133.
25. Araujo FG, Rosenberg LT, Remington JS. Experimental Toxoplasma gondii infection in mice: the role of the fifth component of complement. Proc Soc Exp Biol Med 1975, 149(3):800-804. 10.3181/00379727-149-38902, 1144466.
26. Wetsel RA, Fleischer DT, Haviland DL. Deficiency of the murine fifth complement component (C5). A 2-base pair gene deletion in a 5'-exon. J Biol Chem 1990, 265(5):2435-2440.
27. Smith RS, Zabaleta A, Kume T, Savinova OV, Kidson SH, Martin JE, Nishimura DY, Alward WL, Hogan BL, John SW. Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development. Hum Mol Genet 2000, 9(7):1021-1032. 10.1093/hmg/9.7.1021, 10767326.
28. Smith RZA, John SWM. Light microscopy. Systematic Evaluation of the Mouse Eye: Anatomy, Pathology and Biomethods 2002, Boca Raton, Florida: CRC Press.
29. 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.
30. 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.
31. Libby RT, Anderson MG, Pang IH, Robinson ZH, Savinova OV, Cosma IM, Snow A, Wilson LA, Smith RS, Clark AF, et al. Inherited glaucoma in DBA/2J mice: pertinent disease features for studying the neurodegeneration. Vis Neurosci 2005, 22(5):637-648.
32. 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. 10.1371/journal.pgen.0010017, 1183523, 16103918.
33. Arumugam TV, Tang SC, Lathia JD, Cheng A, Mughal MR, Chigurupati S, Magnus T, Chan SL, Jo DG, Ouyang X, et al. Intravenous immunoglobulin (IVIG) protects the brain against experimental stroke by preventing complement-mediated neuronal cell death. Proc Natl Acad Sci U S A 2007, 104(35):14104-14109. 10.1073/pnas.0700506104, 1955802, 17715065.
34. Bellander BM, Singhrao SK, Ohlsson M, Mattsson P, Svensson M. Complement activation in the human brain after traumatic head injury. J Neurotrauma 2001, 18(12):1295-1311. 10.1089/08977150152725605, 11780861.
35. Pedersen ED, Loberg EM, Vege E, Daha MR, Maehlen J, Mollnes TE. In situ deposition of complement in human acute brain ischaemia. Scand J Immunol 2009, 69(6):555-562. 10.1111/j.1365-3083.2009.02253.x, 19439017.
36. Stasi K, Nagel D, Yang X, Wang RF, Ren L, Podos SM, Mittag T, Danias J. Complement component 1Q (C1Q) upregulation in retina of murine, primate, and human glaucomatous eyes. Invest Ophthalmol Vis Sci 2006, 47(3):1024-1029. 10.1167/iovs.05-0830, 16505037.
37. Fuchs M, Scholz M, Sendelbeck A, Atorf J, Schlegel C, Enz R, Brandstatter JH. Rod photoreceptor ribbon synapses in DBA/2J mice show progressive age-related structural changes. PLoS One 2012, 7(9):e44645. 10.1371/journal.pone.0044645, 3434146, 22957094.
38. Chenoweth DE, Hugli TE. Demonstration of specific C5a receptor on intact human polymorphonuclear leukocytes. Proc Natl Acad Sci U S A 1978, 75(8):3943-3947. 10.1073/pnas.75.8.3943, 392905, 279010.
39. Gerard NP, Gerard C. The chemotactic receptor for human C5a anaphylatoxin. Nature 1991, 349(6310):614-617. 10.1038/349614a0, 1847994.
40. Hugli TE. The structural basis for anaphylatoxin and chemotactic functions of C3a, C4a, and C5a. Crit Rev Immunol 1981, 1(4):321-366.
41. Howell GR, Soto I, Zhu X, Ryan M, Macalinao DG, Sousa GL, Caddle LB, MacNicoll KH, Barbay JM, Porciatti V, et al. Radiation treatment inhibits monocyte entry into the optic nerve head and prevents neuronal damage in a mouse model of glaucoma. J Clin Invest 2012, 122(4):1246-1261. 10.1172/JCI61135, 3314470, 22426214.
42. Mukherjee P, Pasinetti GM. The role of complement anaphylatoxin C5a in neurodegeneration: implications in Alzheimer's disease. J Neuroimmunol 2000, 105(2):124-130. 10.1016/S0165-5728(99)00261-1, 10742554.
43. Osaka H, McGinty A, Hoepken UE, Lu B, Gerard C, Pasinetti GM. Expression of C5a receptor in mouse brain: role in signal transduction and neurodegeneration. Neuroscience 1999, 88(4):1073-1082. 10.1016/S0306-4522(98)00372-8, 10336122.
44. Mukherjee P, Thomas S, Pasinetti GM. Complement anaphylatoxin C5a neuroprotects through regulation of glutamate receptor subunit 2 in vitro and in vivo. J Neuroinflammation 2008, 5:5. 10.1186/1742-2094-5-5, 2246107, 18230183.
45. Howell GR, Walton DO, King BL, Libby RT, John SW. Datgan, a reusable software system for facile interrogation and visualization of complex transcription profiling data. BMC Genomics 2011, 12:429. 10.1186/1471-2164-12-429, 3171729, 21864367.
46. Kuehn MH, Kim CY, Ostojic J, Bellin M, Alward WL, Stone EM, Sakaguchi DS, Grozdanic SD, Kwon YH. Retinal synthesis and deposition of complement components induced by ocular hypertension. Exp Eye Res 2006, 83(3):620-628. 10.1016/j.exer.2006.03.002, 16677633.
47. Stahel PF, Flierl MA, Morgan BP, Persigehl I, Stoll C, Conrad C, Touban BM, Smith WR, Beauchamp K, Schmidt OI, et al. Absence of the complement regulatory molecule CD59a leads to exacerbated neuropathology after traumatic brain injury in mice. J Neuroinflammation 2009, 6:2. 10.1186/1742-2094-6-2, 2631471, 19133139.
48. Ramaglia V, King RH, Nourallah M, Wolterman R, de Jonge R, Ramkema M, Vigar MA, van der Wetering S, Morgan BP, Troost D, et al. The membrane attack complex of the complement system is essential for rapid Wallerian degeneration. J Neurosci 2007, 27(29):7663-7672. 10.1523/JNEUROSCI.5623-06.2007, 17634361.
49. Stoltzner SE, Grenfell TJ, Mori C, Wisniewski KE, Wisniewski TM, Selkoe DJ, Lemere CA. Temporal accrual of complement proteins in amyloid plaques in Down's syndrome with Alzheimer's disease. Am J Pathol 2000, 156(2):489-499. 10.1016/S0002-9440(10)64753-0, 1850044, 10666378.
50. Ramaglia V, King RH, Morgan BP, Baas F. Deficiency of the complement regulator CD59a exacerbates Wallerian degeneration. Mol Immunol 2009, 46(8-9):1892-1896.
51. Britschgi M, Takeda-Uchimura Y, Rockenstein E, Johns H, Masliah E, Wyss-Coray T. Deficiency of terminal complement pathway inhibitor promotes neuronal tau pathology and degeneration in mice. J Neuroinflammation 2012, 9:220. 10.1186/1742-2094-9-220, 3511294, 22989354.