Opposing roles for membrane bound and soluble Fas ligand in glaucoma-associated retinal ganglion cell death

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Gregory, Meredith S ^a   Hackett, Caroline G ^a   Abernathy, Emma F ^a   Lee, Karen S ^b   Saff, Rebecca R ^c   Hohlbaum, Andreas M ^b   Moody, Krishna sulayman L ^b,d   Hobson, Maura W ^a,b   Jones, Alexander ^a   Kolovou, Paraskevi ^a   Karray, Saoussen ^e   Giani, Andrea ^c   John, Simon W M ^f   Chen, Dong Feng ^a   Marshak Rothstein, Ann ^d   Ksander, Bruce R ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS LIGAND; MEMBRANE PROTEIN; METALLOPROTEINASE; TUMOR NECROSIS FACTOR ALPHA; FAS ANTIGEN; FAS PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL PROTECTION; CELL SURFACE; CONTROLLED STUDY; DISEASE ASSOCIATION; DRUG TARGETING; GLAUCOMA; MEMBRANE BINDING; MOLECULAR MECHANICS; MOUSE; NEUROTOXICITY; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN SECRETION; RETINA GANGLION CELL; ANIMAL; CELL MEMBRANE; DISEASE MODEL; DRUG EFFECT; INJECTION; METABOLISM; MICROGLIA; MOUSE MUTANT; NERVE FIBER; PATHOLOGY; PROTEIN BINDING; RETINA DEGENERATION; SIGNAL TRANSDUCTION; SOLUBILITY;

MUS;

ANIMALS; ANTIGENS, CD95; CELL DEATH; CELL MEMBRANE; CYTOPROTECTION; DISEASE MODELS, ANIMAL; FAS LIGAND PROTEIN; GLAUCOMA; INJECTIONS; MICE; MICE, MUTANT STRAINS; MICROGLIA; NERVE FIBERS; PROTEIN BINDING; RETINAL DEGENERATION; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; SOLUBILITY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79953166049     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017659     Document Type: Article

References (62)

1. Kwon YH, Fingert JH, Kuehn MH, Alward WLM, (2009) Primary open-angle glaucoma. N Engl J Med 360: 1113-1124.
2. McKinnon SJ, (1997) Glaucoma, apoptosis, and neuroprotection. Current Opinion in Ophthalmology 8: 28-37.
3. Sawada H, Fukuchi T, Tanaka T, Abe H, (2010) Tumor necrosis factor-alpha concentrations in the aqueous humor of patients with glaucoma. Invest Ophthalmol Vis Sci 51: 903-906.
4. Tezel G, Li LY, Patil RV, Wax MB, (2001) TNF-alpha and TNF-alpha receptor-1 in the retina of normal and glaucomatous eyes. Invest Ophthalmol Vis Sci 42: 1787-1794.
5. Funayama T, Ishikawa K, Ohtake Y, Tanino T, Kurosaka D, et al. (2004) Variants in optineurin gene and their association with tumor necrosis factor-alpha polymorphisms in Japanese patients with glaucoma. Invest Ophthalmol Vis Sci 45: 4359-4367.
6. Lin HJ, Tsai FJ, Chen WC, Shi YR, Hsu Y, et al. (2003) Association of tumour necrosis factor alpha-308 gene polymorphism with primary open-angle glaucoma in Chinese. Eye (Lond) 17: 31-34.
7. Nakazawa T, Nakazawa C, Matsubara A, Noda K, Hisatomi T, et al. (2006) Tumor necrosis factor-alpha mediates oligodendrocyte death and delayed retinal ganglion cell loss in a mouse model of glaucoma. J Neurosci 26: 12633-12641.
8. Yang Z, Quigley HA, Pease ME, Yang Y, Qian J, et al. (2007) Changes in gene expression in experimental glaucoma and optic nerve transection: the equilibrium between protective and detrimental mechanisms. Invest Ophthalmol Vis Sci 48: 5539-5548.
9. Kagi D, Vignaux F, Ledemann B, Burki K, Depraetere V, et al. (1994) Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 265: 528-530.
10. Ju S-T, Panka DJ, Cui H, Ettinger R, El-Khatib M, et al. (1995) Fas (CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373: 444-448.
11. Lee HO, Ferguson TA, (2003) Biology of FasL. Cytokine Growth Factor Rev 14: 325-335.
12. Rescigno M, Piguet V, Valzasina B, Lens S, Zubler R, et al. (2000) Fas engagement induces the maturation of dendritic cells (DCs), the release of interleukin (IL)-1beta, and the production of interferon gamma in the absence of IL-12 during DC-T cell cognate interaction: a new role for Fas ligand in inflammatory responses. J Exp Med 192: 1661-1668.
13. Hohlbaum AM, Gregory MS, Ju S-T, Marshak-Rothstein A, (2001) Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J Immunol 167: 6217-6224.
14. Park SM, Schickel R, Peter ME, (2005) Nonapoptotic functions of FADD-binding death receptors and their signaling molecules. Curr Opin Cell Biol 17: 610-616.
15. Wax MB, Tezel G, Yang J, Peng G, Patil RV, et al. (2008) Induced autoimmunity to heat shock proteins elicits glaucomatous loss of retinal ganglion cell neurons via activated T-cell-derived fas-ligand. J Neurosci 28: 12085-12096.
16. Apte RS, Richter J, Herndon J, Ferguson TA, (2006) Macrophages inhibit neovascularization in a murine model of age-related macular degeneration. PLoS Med 3: e310.
17. Ju KR, Kim HS, Kim JH, Lee NY, Park CK, (2006) Retinal glial cell responses and Fas/FasL activation in rats with chronic ocular hypertension. Brain Res 1122: 209-221.
18. Bazzoni F, Beutler B, (1996) The tumor necrosis factor ligand and receptor families. N Engl J Med 334: 1717-1725.
19. Perez C, Albert I, DeFay K, Zachariades N, Gooding L, et al. (1990) A nonsecretable cell surface mutant of tumor necrosis factor (TNF) kills by cell-to-cell contact. Cell 63: 251-258.
20. Sherry B, Cerami A, (1988) Cachectin/tumor necrosis factor exerts endocrine, paracrine, and autocrine control of inflammatory responses. J Cell Biol 107: 1269-1277.
21. Tanaka M, Suda T, Takahashi T, Nagata S, (1995) Expression of the soluble form of the human Fas ligand in activated lymphocytes. EMBO J 14: 1129-1135.
22. Jodo S, Xiao S, Hohlbaum AM, Strehlow D, Marshak-Rothstein A, et al. (2001) Apoptosis-inducing membrane vesicles: a novel agent with unique properties. J Biol Chem 276: 39938-39944.
23. Bossi G, Griffiths GM, (2005) CTL secretory lysosomes: biogenesis and secretion of a harmful organelle. Semin Immunol 17: 87-94.
24. Hohlbaum AH, Moe S, Marshak-Rothstein A, (2000) Opposing effects of transmembrane and soluble Fas ligand expression on inflammation and tumor cell survival. J Exp Med 191: 1209-1219.
25. Suda T, Hashimoto H, Tanaka M, Ochi T, Nagata S, (1997) Membrane Fas ligand kills human peripheral blood T lymphocytes, and soluble Fas ligand blocks the killing. J Exp Med 186: 2045-2050.
26. Aoki K, Kurooka M, Chen JJ, Petryniak J, Nabel EG, et al. (2001) Extracellular matrix interacts with soluble CD95L: retention and enhancement of cytotoxicity. Nat Immunol 2: 333-337.
27. Karray S, Kress C, Cuvellier S, Hue-Beauvais C, Damotte D, et al. (2004) Complete loss of Fas ligand gene causes massive lymphoproliferation and early death, indicating a residual activity of gld allele. J Immunol 172: 2118-2125.
28. Martinez-Lorenzo MJ, Alava MA, Gamen S, Kim KJ, Chuntharapai A, et al. (1998) Involvement of APO2 ligand/TRAIL in activation-induced death of Jurkat and human peripheral blood T cells. Eur J Immunol 28: 2714-2725.
29. Powell WC, Fingleton B, Wilson CL, Boothby M, Matrisian LM, (1999) The metalloproteinase matrilysin proteolytically generates active soluble Fas ligand and potentiates epithelial cell apoptosis. Curr Biol 9: 1441-1447.
30. Kim JS, Ishikawa H, Sung KR, Xu J, Wollstein G, et al. (2009) Retinal nerve fibre layer thickness measurement reproducibility improved with spectral domain optical coherence tomography. Br J Ophthalmol 93: 1057-1063.
31. Schuman JS, Hee MR, Puliafito CA, Wong C, Pedut-Kloizman T, et al. (1995) Quantification of nerve fiber layer thickness in normal and glaucomatous eyes using optical coherence tomography. Arch Ophthalmol 113: 586-596.
32. Wollstein G, Schuman JS, Price LL, Aydin A, Stark PC, et al. (2005) Optical coherence tomography longitudinal evaluation of retinal nerve fiber layer thickness in glaucoma. Arch Ophthalmol 123: 464-470.
33. Letellier E, Kumar S, Sancho-Martinez I, Krauth S, Funke-Kaiser A, et al. (2010) CD95-Ligand on Peripheral Myeloid Cells Activates Syk Kinase to Trigger Their Recruitment to the Inflammatory Site. Immunity 32: 240-252.
34. Anderson MG, Libby RT, Mao M, Cosma IM, Wilson LA, et al. (2006) Genetic context determines susceptibility to intraocular pressure elevation in a mouse pigmentary glaucoma. BMC Biol 4: 20.
35. Anderson MG, Smith RS, Hawes NL, Zabaleta A, Chang B, et al. (2002) Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice. Nat Genet 30: 81-85.
36. Jakobs T, Libby R, Ben Y, John S, Masland R, (2005) Retinal ganglion cell degeneration is topological but not cell type specific in DBA/2J mice. J Cell Biol 171: 313-325.
37. Theofilopoulos AN, Balderas RS, Gozes Y, Aguado MT, Hang L, et al. (1985) Association of lpr gene with graft-vs-host disease-like syndrome. J Exp Med 162: 1-18.
38. Nemazee D, Guiet C, Buerki K, Marshak-Rothstein A, (1991) B lymphocytes from the autoimmune-prone mouse strain MRL/lpr manifest an intrinsic defect in MRL/lpr &-> DBA/2 chimeras. J Immunol 147: 2536-2539.
39. Hao Z, Hampel B, Yagita H, Rajewsky K, (2004) T cell-specific ablation of Fas leads to Fas ligand-mediated lymphocyte depletion and inflammatory pulmonary fibrosis. J Exp Med 199: 1355-1365.
40. Kavurma MM, Khachigian LM, (2003) Signaling and transcriptional control of Fas ligand gene expression. Cell Death Differ 10: 36-44.
41. He JS, Ostergaard HL, (2007) CTLs contain and use intracellular stores of FasL distinct from cytolytic granules. J Immunol 179: 2339-2348.
42. Griffith TS, Brunner T, Fletcher SM, Green DR, Ferguson TA, (1995) Fas-ligand induced apoptosis as a mechanism of immune privilege. Science 270: 1189-1192.
43. Ferguson TA, Apte RS, (2008) Angiogenesis in eye disease: immunity gained or immunity lost? Semin Immunopathol 30: 111-119.
44. Hu MS, Schwartzman JD, Yeaman GR, Collins J, Seguin R, et al. (1999) Fas-FasL interaction involved in pathogenesis of ocular toxoplasmosis in mice. Infect Immun 67: 928-935.
45. Stuart PM, Pan F, PLambeck S, Ferguson TA, (2003) FasL-Fas interactions regulate neovascularization in the cornea. Invest Ophthalmol Vis Sci 44: 93-8.
46. Stuart PM, Griffith TS, Usui N, Pepose J, Yu X, et al. (1997) CD95 ligand (FasL)-induced apoptosis is necessary for corneal allograft survival. J Clin Invest 99: 396-402.
47. Sano Y, Yamada J, Ishino Y, Adachi W, Kawasaki S, et al. (2002) Non-cleavable mutant Fas ligand transfection of donor cornea abrogates ocular immune privilege. Exp Eye Res 75: 475-483.
48. Gregory MS, Repp A, Hohlbaum AM, Marshak-Rothstein A, Ksander BR, (2002) Membrane Fas ligand activates innate immunity and terminates ocular immune privilege. J Immunol 2002: 2727-2735.
49. Shudo K, Kinoshita K, Imamura R, Fan H, Hasumoto K, et al. (2001) The membrane-bound but not the soluble form of human Fas ligand is responsible for its inflammatory activity. Eur J Immunol 31: 2504-2511.
50. O' Reilly LA, Tai L, Lee L, Kruse EA, Grabow S, et al. (2009) Membrane-bound Fas ligand only is essential for Fas-induced apoptosis. Nature 461: 659-663.
51. Ohta K, Yamagami S, Taylor AW, Streilein JW, (2000) IL-6 antagonizes TGF-beta and abolishes immune privilege in eyes with endotoxin-induced uveitis. Invest Ophthalmol Vis Sci 41: 2591-2599.
52. Sotozono C, Sano Y, Suzuki T, Tada R, Ikeda T, et al. (2000) Soluble Fas ligand expression in the ocular fluids of uveitis patients. Curr Eye Res 20: 54-57.
53. Sugita S, Taguchi C, Takase H, Sagawa K, Sueda J, et al. (2000) Soluble Fas ligand and soluble Fas in ocular fluid of patients with uveitis. Br J Ophthalmol 84: 1130-1134.
54. Lei Y, Garrahan N, Hermann B, Becker DL, Hernandez MR, et al. (2008) Quantification of retinal transneuronal degeneration in human glaucoma: a novel multiphoton-DAPI approach. Invest Ophthalmol Vis Sci 49: 1940-1945.
55. Taylor DL, Jones F, Kubota ES, Pocock JM, (2005) Stimulation of microglial metabotropic glutamate receptor mGlu2 triggers tumor necrosis factor alpha-induced neurotoxicity in concert with microglial-derived Fas ligand. J Neurosci 25: 2952-2964.
56. Dace DS, Khan AA, Stark JL, Kelly J, Cross AH, et al. (2009) Interleukin-10 overexpression promotes Fas-ligand-dependent chronic macrophage-mediated demyelinating polyneuropathy. PLoS One 4: e7121.
57. Vargo-Gogola T, Crawford HC, Fingleton B, Matrisian LM, (2002) Identification of novel matrix metalloproteinase-7 (matrilysin) cleavage sites in murine and human Fas ligand. Arch Biochem Biophys 408: 155-161.
58. Agapova OA, Ricard CS, Salvador-Silva M, Hernandez MR, (2001) Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia 33: 205-216.
59. Vargo-Gogola T, Crawford HC, Fingleton B, Matrisian LM, (2002) Identification of novel matrix metalloproteinase-7 (matrilysin) cleavage sites in murine and human Fas ligand. Arch Biochem Biophys 408: 155-161.
60. Tanaka M, Itai T, Adachi M, Nagata S, (1998) Downregulation of Fas ligand by shedding. Nat Med 4: 31-36.
61. Tchedre KT, Yorio T, (2008) sigma-1 receptors protect RGC-5 cells from apoptosis by regulating intracellular calcium, Bax levels, and caspase-3 activation. Invest Ophthalmol Vis Sci 49: 2577-2588.
62. Gu H, Zou YR, Rajewsky, (1993) Independent control of immunoglobulin switch recombination at individual switch regions evidenced through Cre-loxP-mediated gene targeting. Cell 73: 1155-1164.