ACS67, a hydrogen sulfide-releasing derivative of latanoprost acid, attenuates retinal ischemia and oxidative stress to RGC-5 cells in culture

Investigative Ophthalmology and Visual Science

Volumn 51, Issue 1, 2010, Pages 284-294

  Osborne, Neville N ^a   Ji, Dan ^a   Majid, Aman S Abdul ^a   Fawcett, Rebecca J ^a   Sparatore, Anna ^a,b   Del Soldato, Piero ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MILAN   (Italy)

^c CTG Pharma   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACS 1; ACS 67; EPIGALLOCATECHIN GALLATE; GLUTATHIONE; HYDROGEN PEROXIDE; LATANOPROST; MESSENGER RNA; PROSTAGLANDIN DERIVATIVE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ACS67 COMPOUND; CASPASE; DRUG DERIVATIVE; GLIAL FIBRILLARY ACIDIC PROTEIN; HYDROGEN SULFIDE; NEURONAL NITRIC OXIDE SYNTHASE; PROSTAGLANDIN F; THIOCTIC ACID; THY 1 ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; INTRAOCULAR HYPERTENSION; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL; RETINA INJURY; RETINA ISCHEMIA; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CHEMISTRY; DISEASE MODEL; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; REPERFUSION INJURY; RETINA DISEASE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANTIGENS, THY-1; BLOTTING, WESTERN; CASPASES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ELECTRORETINOGRAPHY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTATHIONE; HYDROGEN PEROXIDE; HYDROGEN SULFIDE; NITRIC OXIDE SYNTHASE TYPE I; OXIDATIVE STRESS; PROSTAGLANDINS F, SYNTHETIC; RATS; REPERFUSION INJURY; RETINAL DISEASES; RETINAL GANGLION CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; THIOCTIC ACID;

EID: 75749143126     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.09-3999     Document Type: Article

References (68)

1. Stjernschantz J, Ocklind A, Wentzel P, Lake S, Hu DN. Latanoprostinduced increase of tyrosinase transcription in iridial melanocytes. Acta Ophthalmol Scand. 2000;78:618-622.
2. Perrino E, Uliva C, Lanzi C, Soldato PD, Masini E, Sparatore A. New prostaglandin derivative for glaucoma treatment. Bioorganic Med Chem Lett. 2009;19:1639-1642.
3. Li L, Rossoni G, Sparatore A, Lee LC, Del Soldato P, Moore PK. Anti-inflammatory and gastrointestinal effects of a novel diclofenac derivative. Free Radic Biol Med. 2007;42:706-719.
4. Szabü C. Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov. 2007;6:917-935.
5. Lefer DJ. A new gaseous signaling molecule emerges: cardioprotective role of hydrogen sulphide. Proc Natl Acad Sci. 2007;104: 17907-17908.
6. Moore PK, Bhatia M, Moochhala S. Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol Sci. 2003;24:609-611.
7. Kimura H, Nagai Y, Umenura K, Kimura Y. Physiological roles of hydrogen sulfide: synaptic modulation, neuroprotection, and smooth muscle relaxation. Antioxid Redox Signal. 2005;7:795-803.
8. Zhang H, Bhatia M. Hydrogen sulfide: a novel mediator of leukocyte activation. Immunopharmacol Immunotoxicol. 2008;30: 631-645.
9. Kimura Y, Kimura H. Hydrogen sulfide protects neurons from oxidative stress. FASEB J. 2004;18:1165-1167.
10. Abe K, Kimura H. The possible role of hydrogen sulfide as an endogenous neuromodulator. J Neurosci. 1996;16:1066-1071.
11. Olson KR. Is hydrogen sulfide a circulating "gasotransmitter" in vertebrate blood? Biochim Biophys Acta. 2009;1787(7):856-863.
12. Kimura H. Hydrogen sulphide induces cyclic AMP and modulates the NMDA receptor. Biochem Biophys Res Commun. 2000;267: 129-133.
13. Boehning D, Snyder SH. Novel neural modulators. Annu Rev Neurosci. 2003;26:105-131.
14. Kombian SB, Reiffenstein RJ, Colmers WF. The actions of hydrogen sulfide on dorsal raphe serotonergic neurons in vitro. J Neurophysiol. 1993;70:81-96.
15. Dello Russo C, Tringali G, Ragazzoni E, et al. Evidence that hydrogen sulphide can modulate hypothalamo-pituitary-adrenal axis function: in vitro and in vivo studies in the rat. J Neuroendocrinol. 2000;12:225-233.
16. Nagai Y, Tsugane M, Oka J, Kimura H. Hydrogen sulfide induces calcium waves in astrocytes. FASEB J. 2004;18:557-559.
17. Doeller JE, Isbell TS, Benavides G, et al. Polarographic measurement of hydrogen sulfide production and consumption by mammalian tissues. Anal Biochem. 2005;341:40-51.
18. Elrod JW, Calvert JW, Morrison J, et al. Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci. 2007;104:15560-15565.
19. Kimura Y, Dargusch R, Schubert D, Kimura K. Hydrogen sulphide protects HT22 neuronal cells from oxidative stress. Antioxid Redox Signal. 2006;8:661-670.
20. Sivarajah A, McDonald MC, Thiemermann C. The production of hydrogen sulfide limits myocardial ischemia and reperfusion injury and contributes to the cardioprotective effects of preconditioning with endotoxin, but not ischemia in the rat. Shock. 2006;26:154-161.
21. Umemura K, Kimura H. Hydrogen sulfide enhances reducing activity in neurons: neurotrophic role of H2S in the brain? Antioxid Redox Signal. 2007;9:2035-2041.
22. Lu M, Hu LF, Hu G, Bian JS. Hydrogen sulfide protects astrocytes against H(2)O(2)-induced neural injury via enhancing glutamate uptake. Free Radic Biol Med. 2008;45:1705-1713.
23. Tang XQ, Yang CT, Chen J, et al. Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells. Clin Exp Pharmacol Physiol. 2008;35:180-186.
24. Jha S, Calvert JW, Duranski MR, Ramachandran A, Lefer DJ. Hydrogen sulfide attenuates hepatic ischemia-reperfusion injury: role of antioxidant and antiapoptotic signaling. Am J Physiol Heart Circ Physiol. 2008;295:H801-H806.
25. Bliksøen M, Kaljusto ML, Vaage J, Stensløkken KO. Effects of hydrogen sulphide on ischaemia-reperfusion injury and ischaemic preconditioning in the isolated, perfused rat heart. Eur J Cardiothorac Surg. 2008;34:344-349.
26. Cheung NS, Peng ZF, Chen MJ, Moore PK, Whiteman M. Hydrogen sulfide induced neuronal death occurs via glutamate receptor and is associated with calpain activation and lysosomal rupture in mouse primary cortical neurons. Neuropharmacology. 2007;53: 505-514.
27. Qu K, Chen CP, Halliwell B, Moore PK, Wong PT. Hydrogen sulfide is a mediator of cerebral ischemic damage. Stroke. 2006;37:889-893.
28. Rossoni G, Sparatore A, Tazzari V, Manfredi B, Del Soldato P, Berti F. The hydrogen sulphide-releasing derivative of diclofenac protects against ischaemia-reperfusion injury in the isolated rabbit heart. Br J Pharmacol. 2008;153:100-109.
29. Sidhapuriwala J, Li L, Sparatore A, Bhatia M, Moore PK. Effect of S-diclofenac, a novel hydrogen sulfide releasing derivative, on carrageenan-induced hindpaw oedema formation in the rat. Eur J Pharmacol. 2007;569:149-154.
30. Muzaffar S, Jeremy JY, Sparatore A, Del Soldato P, Angelini GD, Shukla N. H2S-donating sildenafil (ACS6) inhibits superoxide formation and gp91phox expression in arterial endothelial cells: role of protein kinases A and G. Br J Pharmacol. 2008;155:984-994.
31. Sparatore A, Perrino E, Tazzari V, et al. Pharmacological profile of a novel H(2)S-releasing aspirin. Free Radic Biol Med. 2009;46: 586-592.
32. Osborne NN, Larsen AK. Antigens associated with specific retinal cells are affected by ischaemia caused by raised intraocular pressure: effect of glutamate antagonists. Neurochem Int. 1996; 29:263-270.
33. Nash MS, Osborne NN. Assessment of Thy-1 mRNA levels as an index of retinal ganglion cell damage. Invest Ophthalmol Vis Sci. 1999;40:1293-1298.
34. Chidlow G, Casson R, Sobrado-Calvo P, Vidal-Sanz M, Osborne NN. Measurement of retinal injury in the rat after optic nerve transection: an RT-PCR Study. Mol Vis. 2005;11:387-396.
35. Laemmli. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
36. Ahmed SA, Gogal RM Jr, Walsh JE. A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3H]thymidine incorporation assay. J Immunol Methods. 1994;170:211-224.
37. Fields RD, Lancaster MV. Dual-attribute continuous monitoring of cell proliferation/cytotoxicity. Am Biotechnol Lab. 1993;1:48-50.
38. Carter WO, Narayanan PK, Robinson JP. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J Leukoc Biol. 1994;55:253-258.
39. Cook JA, Mitchell JB. Measurement of thiols in cell populations from tumor and normal tissue. Methods Enzymol. 1995;251:203-212.
40. Zhang B, Safa R, Rusciano D, Osborne NN. Epigallocatechin gallate, an active ingredient from green tea, attenuates damaging influences to the retina caused by ischemia-reperfusion. Brain Res. 2007;23:40-53.
41. Li GY, Osborne NN. Oxidative-induced apoptosis to an immortalized ganglion cell line is caspase independent but involves the activation of poly(ADP-ribose)polymerase and apoptosis-inducing factor. Brain Res. 2008;1188:35-43.
42. Qu K, Lee SW, Bian JS, Low CM, Wong PT. Hydrogen sulfide: neurochemistry and neurobiology. Neurochem Int. 2008;52:155-165.
43. Block F, Schwarz M. The b-wave of the electroretinogram as an index of retinal ischemia. Gen Pharmacol. 1998;30:281-287.
44. Osborne NN, Casson RJ, Wood JP, Chidlow G, Graham M, Melena J. Retinal ischemia: mechanisms of damage and potential therapeutic strategies. Prog Retin Eye Res. 2004;23:91-147.
45. Casson RJ, Wood JP, Osborne NN. Hypoglycaemia exacerbates ischaemic retinal injury in rats. Br J Ophthalmol. 2004;88:816-820.
46. Ji D, Li GY, Osborne NN. Nicotinamide attenuates retinal ischemia and light insults to neurones. Neurochem Int. 2008;52:786-798.
47. Zhang B, Rusciano D, Osborne NN. Orally administered epigallocatechin gallate attenuates retinal neuronal death in vivo and light-induced apoptosis in vitro. Brain Res. 2008;10:141-152.
48. Bringmann A, Pannicke T, Grosche J, et al. Müller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
49. Nishiyama T, Nishukawa S, Hiroshi, Tomita, Tamai M. Müller cells in the preconditioned retinal ischemic injury rat. Tohoku J Exp Med. 2000;191:221-232.
50. Barnett NL, Osborne NN. Prolonged bilateral carotid artery occlusion induces electrophysiological and immunohistochemical changes to the rat retina without causing histological damage. Exp Eye Res. 1995;61:83-90.
51. Katai N, Yoshimura N. Apoptotic retinal neuronal death by ischemia-reperfusion is executed by two distinct caspase family proteases. Invest Ophthalmol Vis Sci. 1999;40:2697-2705.
52. Grütter MG. Caspases: key players in programmed cell death. Curr Opin Struct Biol. 2000;10:649-655.
53. Dawson VL, Dawson TM. Deadly conversations: nuclear-mitochondrial cross-talk. J Bioenerg Biomembr. 2004;36:287-294.
54. Hong SJ, Dawson TM, Dawson VL. Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci. 2004;25:259-264.
55. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med. 2000;6:513-519.
56. Krishnamoorthy RR, Agarwal P, Prasanna G, et al. Characterization of a transformed rat retinal ganglion cell line. Brain Res Mol Brain Res. 2001;86:1-12.
57. Osborne NN, Li G-Y, Ji D, Mortiboys HJ, Jackson S. Light affects mitochondria to cause apoptosis to cultured cells: possible relevance to ganglion cell death in certain optic neuropathies. J Neurochem. 2008;105:2013-2028.
58. Mandel SA, Avramovich-Tirosh Y, Reznichenko L, et al. Multifunctional activities of green tea catechins in neuroprotection. Modulation of cell survival genes, iron-dependent oxidative stress and PKC signaling pathway. Neurosignals. 2005;14:46-60.
59. Wang CT, Chang HH, Hsiao CH, et al. The effects of green tea (-)-epigallocatechin-3-gallate on reactive oxygen species in 3T3-L1 preadipocytes and adipocytes depend on the glutathione and 67 kDa laminin receptor pathways. Mol Nutr Food Res. 2009;53:349-360.
60. Siram N, Kalayasaran S, Sudhandrian G. Enhancement of antioxidant defense system by epigallocatechin-3-gallate during bleomycin induced experimental pulmonary fibrosis. Biol Pharm Bull. 2008;31:1306-1311.
61. Yin ST, Tang ML, Su L, et al. Effects of epigallocatechin-3-gallate on lead-induced oxidative damage. Toxicology. 2008;249:45-54.
62. Fu Y, Zheng S, Lu SC, Chen A. Epigallocatechin-3-gallate inhibits growth of activated hepatic stellate cells by enhancing the capacity of glutathione synthesis. Mol Pharmacol. 2008;73:1465-1473.
63. Ben-Yoseph O, Boxer PA, Ross BD. Assessment of the role of the glutathione and pentose phosphate pathways in the protection of primary cerebrocortical cultures from oxidative stress. J Neurochem. 1996;66:2329-2337.
64. Atkuri KR, Mantovani JJ, Herzenberg LA, Herzenberg LA. N-Acetylcysteine: a safe antidote for cysteine/glutathione deficiency. Curr Opin Pharmacol. 2007;7:355-359.
65. Roh YJ, Moon C, Kim SY, et al. Glutathione depletion induces differential apoptosis in cells of mouse retina, in vivo. Neurosci Lett. 2007;7:266-270.
66. Drago F, Valzelli S, Emmi I, Marino A, Scalia CC, Marino V. Latanoprost exerts neuroprotective activity in vitro and in vivo. Exp Eye Res. 2001;72:479-486.
67. Kudo H, Nakazawa T, Shimura M, et al. Neuroprotective effect of latanoprost on rat retinal ganglion cells. Graefes Arch Clin Exp Ophthalmol. 2006;244:1003-1009.
68. Kanamori A, Naka M, Fukuda M, Nakamura M, Negi A. Latanoprost protects rat retinal ganglion cells from apoptosis in vitro and in vivo. Exp Eye Res. 2009;88:535-541.