Role of paraoxonase-1 in the protection of hydrogen sulfide-donating sildenafil (ACS6) against homocysteine-induced neurotoxicity

Journal of Molecular Neuroscience

Volumn 50, Issue 1, 2013, Pages 70-77

  Tang, Xiao Qing ^a   Chen, Rong Qian ^a,e   Dong, Ling ^a   Ren, Yan Kai ^a   Del Soldato, Piero ^c   Sparatore, Anna ^d   Liao, Duan Fang ^b  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b HUNAN UNIVERSITY OF CHINESE MEDICINE   (China)

^c CTG Pharma   (Italy)

^d UNIVERSITY OF MILAN   (Italy)

^e Chuzhou City Vocation College   (China)

Author keywords

H2S releasing sildenafil; Homocysteine; Neurotoxicity; Paraoxonase 1; Reactive oxygen species

Indexed keywords

ARYLDIALKYLPHOSPHATASE 1; HOMOCYSTEINE; HYDROGEN SULFIDE DONATING SILDENAFIL; QUINOLINOL DERIVATIVE; REACTIVE OXYGEN METABOLITE; SILDENAFIL; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SYNTHESIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANIMALS; APOPTOSIS; ARYLDIALKYLPHOSPHATASE; HOMOCYSTEINE; NEUROPROTECTIVE AGENTS; PC12 CELLS; PIPERAZINES; RATS; REACTIVE OXYGEN SPECIES; SULFONES;

EID: 84876157801     PISSN: 08958696     EISSN: 15591166     Source Type: Journal    
DOI: 10.1007/s12031-012-9862-x     Document Type: Article

References (51)

1. Ataie A, Sabetkasaei M, Haghparast A, Moghaddam AH, Ataee R, Moghaddam SN (2010) Curcumin exerts neuroprotective effects against homocysteine intracerebroventricular injection-induced cognitive impairment and oxidative stress in rat brain. J Med Food 13:821-826
2. Aviram M, Rosenblat M (2005) Paraoxonases and cardiovascular diseases: pharmacological and nutritional influences. Curr Opin Lipidol 16:393-399 (Pubitemid 41017622)
3. Aviram M, Rosenblat M, Billecke S, Erogul J, Sorenson R, Bisgaier CL, Newton RS, La Du B (1999) Human serum paraoxonase (PON 1) is inactivated by oxidized low density lipoprotein and preserved by antioxidants. Free Radic Biol Med 26:892-904 (Pubitemid 29198362)
4. Borowczyk K, Shih DM, Jakubowski H (2012) Metabolism and neurotoxicity of homocysteine thiolactone in mice: evidence for a protective role of paraoxonase 1. J Alzheimers Dis. doi: 10.3233/JAD-2012-111940
5. Cathcart R, Schwiers E, Ames BN (1983) Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal Biochem 134:111-116 (Pubitemid 14231364)
6. Chasse JF (2005) Inverse correlation between phenylacetate hydrolase activity of the serum PON1 protein and homocysteinemia in humans. Thromb Haemost 93:182-183 (Pubitemid 40142600)
7. Christie LA, Riedel G, Algaidi SA, Whalley LJ, Platt B (2005) Enhanced hippocampal long-term potentiation in rats after chronic exposure to homocysteine. Neurosci Lett 373:119-124 (Pubitemid 39572973)
8. Grieve A, Butcher SP, Griffiths R (1992) Synaptosomal plasma membrane transport of excitatory sulphur amino acid transmitter candidates: kinetic characterisation and analysis of carrier specificity. J Neurosci Res 32:60-68
9. Hamelet J, Ait-Yahya-Graison E, Matulewicz E, Noll C, Badel-Chagnon A, Camproux AC, Demuth K, Paul JL, Delabar JM, Janel N (2007) Homocysteine threshold value based on cystathionine beta synthase and paraoxonase 1 activities in mice. Eur J Clin Invest 37:933-938 (Pubitemid 350151181)
10. Heinecke JW, Rosen H, Suzuki LA, Chait A (1987) The role of sulfur-containing amino acids in superoxide production and modification of low density lipoprotein by arterial smooth muscle cells. J Biol Chem 262:10098-10103
11. Ho PI, Collins SC, Dhitavat S, Ortiz D, Ashline D, Rogers E, Shea TB (2001) Homocysteine potentiates beta-amyloid neurotoxicity: role of oxidative stress. J Neurochem 78:249-253 (Pubitemid 32664406)
12. Ho YS, Yu MS, Yang XF, So KF, Yuen WH, Chang RC (2010) Neuroprotective effects of polysaccharides from wolfberry, the fruits of Lycium barbarum, against homocysteine-induced toxicity in rat cortical neurons. J Alzheimers Dis 19:813-827
13. Hooshmand B, Solomon A, Kareholt I, Leiviska J, Rusanen M, Ahtiluoto S, Winblad B, Laatikainen T, Soininen H, Kivipelto M (2010) Homocysteine and holotranscobalamin and the risk of Alzheimer disease: a longitudinal study. Neurology 75:1408-1414
14. Isobe C, Abe T, Terayama Y (2009) Homocysteine may contribute to pathogenesis of RNA damage in brains with Alzheimer's disease. Neurodegener Dis 6:252-257
15. Jakubowski H (2010) The role of paraoxonase 1 in the detoxification of homocysteine thiolactone. Adv Exp Med Biol 660:113-127
16. Karikas GA, Kriebardis A, Samara I, Schulpis K, Papachristodoulou M, Fytou-Pallikari A (2006) Serum homocysteine levels and paraoxonase 1 activity in preschool aged children in Greece. Clin Chem Lab Med 44:623-627 (Pubitemid 43735637)
17. Kim JH, Cho SY, Lee JH, Jeong SM, Yoon IS, Lee BH, Pyo MK, Lee SM, Chung JM, Kim S, Rhim H, Oh JW, Nah SY (2007) Neuroprotective effects of ginsenoside Rg3 against homocysteine-induced excitotoxicity in rat hippocampus. Brain Res 1136:190-199 (Pubitemid 46217786)
18. Kim HJ, Cho HK, Kwon YH (2008) Synergistic induction of ER stress by homocysteine and beta-amyloid in SH-SY5Y cells. J Nutr Biochem 19:754-761
19. Kuszczyk M, Gordon-Krajcer W, Lazarewicz JW (2009) Homocysteine-induced acute excitotoxicity in cerebellar granule cells in vitro is accompanied by PP2A-mediated dephosphorylation of tau. Neurochem Int 55:174-180
20. Leduc V, Theroux L, Dea D, Robitaille Y, Poirier J (2009) Involvement of paraoxonase 1 genetic variants in Alzheimer's disease neuropathology. Eur J Neurosci 30:1823-1830
21. Li L, Whiteman M, Guan YY, Neo KL, Cheng Y, Lee SW, Zhao Y, Baskar R, Tan CH, Moore PK (2008) Characterization of a novel, water-soluble hydrogen sulfide-releasing molecule (GYY4137): new insights into the biology of hydrogen sulfide. Circulation 117:2351-2360 (Pubitemid 351653553)
22. Loureiro SO, Heimfarth L, Pelaez Pde L, Vanzin CS, Viana L, Wyse AT, Pessoa-Pureur R (2008) Homocysteine activates calcium-mediated cell signaling mechanisms targeting the cytoskeleton in rat hippocampus. Int J Dev Neurosci 26:447-455
23. Marsillach J, Mackness B, Mackness M, Riu F, Beltran R, Joven J, Camps J (2008) Immunohistochemical analysis of paraoxonases-1, 2, and 3 expression in normal mouse tissues. Free Radic Biol Med 45:146-157
24. Muzaffar S, Jeremy JY, Sparatore A, Del Soldato P, Angelini GD, Shukla N (2008) H2S-donating sildenafil (ACS6) inhibits superoxide formation and gp91phox expression in arterial endothelial cells: role of protein kinases A and G. Br J Pharmacol 155:984-994
25. Ng CJ, Shih DM, Hama SY, Villa N, Navab M, Reddy ST (2005) The paraoxonase gene family and atherosclerosis. Free Radic Biol Med 38:153-163 (Pubitemid 39656127)
26. Oldreive CE, Doherty GH (2007) Neurotoxic effects of homocysteine on cerebellar Purkinje neurons in vitro. Neurosci Lett 413:52-57 (Pubitemid 46149191)
27. Park YJ, Jang Y, Kwon YH (2010) Protective effect of isoflavones against homocysteine-mediated neuronal degeneration in SH-SY5Y cells. Amino Acids 39:785-794
28. Perna AF, Ingrosso D, De Santo NG (2003) Homocysteine and oxidative stress. Amino Acids 25:409-417 (Pubitemid 38041275)
29. Prudova A, Bauman Z, Braun A, Vitvitsky V, Lu SC, Banerjee R (2006) S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity. Proc Natl Acad Sci USA 103:6489-6494
30. Qu K, Lee SW, Bian JS, Low CM, Wong PT (2008) Hydrogen sulfide: neurochemistry and neurobiology. Neurochem Int 52:155-165 (Pubitemid 350235691)
31. Rajagopalan P, Hua X, Toga AW, Jack CR Jr, Weiner MW, Thompson PM (2011) Homocysteine effects on brain volumes mapped in 732 elderly individuals. Neuroreport 22:391-395
32. Rozenberg O, Shiner M, Aviram M, Hayek T (2008) Paraoxonase 1 (PON1) attenuates diabetes development in mice through its antioxidative properties. Free Radic Biol Med 44:1951-1959
33. Selhub J (1999) Homocysteine metabolism. Annu Rev Nutr 19:217-246 (Pubitemid 29380603)
34. Seshadri S, Beiser A, Selhub J, Jacques PF, Rosenberg IH, D'Agostino RB, Wilson PW, Wolf PA (2002) Plasma homocysteine as a risk factor for dementia and Alzheimer's disease. N Engl J Med 346:476-483 (Pubitemid 34441738)
35. Smach MA, Jacob N, Golmard JL, Charfeddine B, Lammouchi T, Ben Othman L, Dridi H, Bennamou S, Limem K (2011) Folate and homocysteine in the cerebrospinal fluid of patients with Alzheimer's disease or dementia: a case control study. Eur Neurol 65:270-278
36. Szabo C (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6:917-935 (Pubitemid 350042399)
37. Tan BH, Wong PT, Bian JS (2010) Hydrogen sulfide: a novel signaling molecule in the central nervous system. Neurochem Int 56:3-10
38. Tang XQ, Yang CT, Chen J, Yin WL, Tian SW, Hu B, Feng JQ, Li YJ (2008) Effect of hydrogen sulphide on beta-amyloid-induced damage in PC12 cells. Clin Exp Pharmacol Physiol 35:180-186
39. Tang XQ, Shen XT, Huang YE, Ren YK, Chen RQ, Hu B, He JQ, Yin WL, Xu JH, Jiang ZS (2010) Hydrogen sulfide antagonizes homocysteine-induced neurotoxicity in PC12 cells. Neurosci Res 68:241-249
40. Tang XQ, Chen RQ, Ren YK, Soldato PD, Sparatore A, Zhuang YY, Fang HR, Wang CY (2011a) ACS6, a hydrogen sulfide-donating derivative of sildenafil, inhibits homocysteine-induced apoptosis by preservation of mitochondrial function. Med Gas Res 1:20
41. Tang XQ, Fan LL, Li YJ, Shen XT, Zhuan YY, He JQ, Xu JH, Hu B (2011b) Inhibition of hydrogen sulfide generation contributes to 1-methy-4- phenylpyridinium ion-induced neurotoxicity. Neurotox Res 19:403-411
42. Thiersch M, Raffelsberger W, Frigg R, Samardzija M, Wenzel A, Poch O, Grimm C (2008) Analysis of the retinal gene expression profile after hypoxic preconditioning identifies candidate genes for neuroprotection. BMC Genomics 9:73 (Pubitemid 351437041)
43. Uzun H, Yanardag H, Gelisgen R, Genc H, Uygun S, Vehid S, Karter Y, Demirci S (2008) Levels of paraoxonase, an index of antioxidant defense, in patients with active sarcoidosis. Curr Med Res Opin 24:1651-1657 (Pubitemid 351929063)
44. Van Dam F, Van Gool WA (2009) Hyperhomocysteinemia and Alzheimer's disease: a systematic review. Arch Gerontol Geriatr 48:425-430
45. Wehr H, Bednarska-Makaruk M, Graban A, Lipczynska-Lojkowska W, Rodo M, Bochynska A, Ryglewicz D (2009) Paraoxonase activity and dementia. J Neurol Sci 283:107-108
46. White AR, Huang X, Jobling MF, Barrow CJ, Beyreuther K, Masters CL, Bush AI, Cappai R (2001) Homocysteine potentiates copper- and amyloid beta peptide-mediated toxicity in primary neuronal cultures: possible risk factors in the Alzheimer's-type neurodegenerative pathways. J Neurochem 76:1509-1520 (Pubitemid 32198255)
47. Whiteman M, Armstrong JS, Chu SH, Jia-Ling S, Wong BS, Cheung NS, Halliwell B, Moore PK (2004) The novel neuromodulator hydrogen sulfide: an endogenous peroxynitrite 'scavenger'? J Neurochem 90:765-768 (Pubitemid 38989409)
48. Yan SK, Chang T, Wang H, Wu L, Wang R, Meng QH (2006) Effects of hydrogen sulfide on homocysteine-induced oxidative stress in vascular smooth muscle cells. Biochem Biophys Res Commun 351:485-491 (Pubitemid 44755144)
49. Yildiz H, Durmus AS, Simsek H, Yaman I (2011) Effects of sildenafil citrate on torsion/detorsion-induced changes in red blood cell and plasma lipid peroxidation, antioxidants, and blood hematology of male rats. Eur J Obstet Gynecol Reprod Biol 159:359-363
50. Yin WL, He JQ, Hu B, Jiang ZS, Tang XQ (2009) Hydrogen sulfide inhibits MPP(+)-induced apoptosis in PC12 cells. Life Sci 85:269-275
51. Zhuo JM, Wang H, Pratico D (2011) Is hyperhomocysteinemia an Alzheimer's disease (AD) risk factor, an AD marker, or neither? Trends Pharmacol Sci 32:562-571