Effect of polyphenolic phytochemicals on ectopic oxidative phosphorylation in rod outer segments of bovine retina

British Journal of Pharmacology

Volumn 172, Issue 15, 2015, Pages 3890-3903

  Calzia, Daniela ^a   Oneto, Michele ^a   Caicci, Federico ^b   Bianchini, Paolo ^c   Ravera, Silvia ^a   Bartolucci, Martina ^a   Diaspro, Alberto ^c   Degan, Paolo ^d   Manni, Lucia ^b   Traverso, Carlo Enrico ^d   Panfoli, Isabella ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; APOPTOSOME; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 9; CURCUMIN; CYTOCHROME C; EPIGALLOCATECHIN GALLATE; HYDROGEN PEROXIDE; MALIC ACID; MALONALDEHYDE; OLIGOMYCIN; OUABAIN; PIPERINE; PROCASPASE 3; PROCASPASE 9; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVIC ACID; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; RESVERATROL; RHODOPSIN; SUCCINIC ACID; 1,3 BENZODIOXOLE DERIVATIVE; ALKALOID; AMIDE; CATECHIN; PIPERIDINE DERIVATIVE; PLANT MEDICINAL PRODUCT; STILBENE DERIVATIVE;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; BOVINE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOFLUOROMETRY; DRUG EFFECT; DRUG MECHANISM; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME INHIBITION; HYDROLYSIS; MEMBRANE POTENTIAL; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXIMETRY; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA ROD OUTER SEGMENT; SYNTHESIS; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; METABOLISM; RETINAL ROD OUTER SEGMENT; ULTRASTRUCTURE;

ADENOSINE TRIPHOSPHATE; ALKALOIDS; ANIMALS; BENZODIOXOLES; CASPASE 3; CASPASE 9; CATECHIN; CATTLE; CURCUMIN; CYTOCHROMES C; HYDROGEN PEROXIDE; MALONDIALDEHYDE; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PHYTOCHEMICALS; PIPERIDINES; POLYUNSATURATED ALKAMIDES; QUERCETIN; ROD CELL OUTER SEGMENT; STILBENES;

EID: 84937440750     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13173     Document Type: Article

References (66)

1. Aicardi G, Solaini G, (1982). Effects of niridazole and 5-nitroimidazoles on heart mitochondrial respiration. Biochem Pharmacol 31: 3703-3705.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013). The Concise Guide to PHARMACOLOGY 2013/14: Enzymes. Br J Pharmacol 170: 1797-1867.
3. Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB, (2007). Bioavailability of curcumin: problems and promises. Mol Pharm 4: 807-818.
4. Areias FM, Rego AC, Oliveira CR, Seabra RM, (2001). Antioxidant effect of flavonoids after ascorbate/Fe(2+)-induced oxidative stress in cultured retinal cells. Biochem Pharmacol 62: 111-118.
5. Baynes JW, (1991). Role of oxidative stress in development of complications in diabetes. Diabetes 40: 405-412.
6. Berman SB, Watkins SC, Hastings TG, (2000). Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: evidence for reduced sensitivity of brain mitochondria. Exp Neurol 164: 415-425.
7. Bianchini P, Calzia D, Ravera S, Candiano G, Bachi A, Morelli A, et al. (2008). Live imaging of mammalian retina: rod outer segments are stained by conventional mitochondrial dyes. J Biomed Opt 13: 54017.
8. Blanch RJ, Ahmed Z, Thompson AR, Akpan N, Snead DRJ, Berry M, et al. (2014). Caspase-9 mediates photoreceptor death after blunt ocular trauma. Invest Ophthalmol Vis Sci 55: 6350-6357.
9. Boyer PD, (1997). The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66: 717-749.
10. Bucher T, Pfleiderer G, (1955). Pyruvate kinase from muscle. Methods Enzymol 1: 435-440.
11. Calzia D, Barabino S, Bianchini P, Garbarino G, Oneto M, Caicci F, et al. (2013a). New findings in ATP supply in rod outer segments: insights for retinopathies. Biol Cell 105: 345-358.
12. Calzia D, Candiani S, Garbarino G, Caicci F, Ravera S, Bruschi M, et al. (2013b). Are rod outer segment ATP-ase and ATP-synthase activity expression of the same protein? Cell Mol Neurobiol 33: 637-649.
13. Calzia D, Garbarino G, Caicci F, Manni L, Candiani S, Ravera S, et al. (2014). Functional expression of electron transport chain complexes in mouse rod outer segments. Biochimie 102: 78-82.
14. Cao X, Liu M, Tuo J, Shen D, Chan CC, (2010). The effects of quercetin in cultured human RPE cells under oxidative stress and in Ccl2/Cx3cr1 double deficient mice. Exp Eye Res 91: 15-25.
15. Carella G, (2003). Introduction to apoptosis in ophthalmology. Eur J Ophthalmol 13 (Suppl. 3): S5-S10.
16. Chinopoulos C, Starkov AA, Fiskum G, (2003). Cyclosporin A-insensitive permeability transition in brain mitochondria: inhibition by 2-aminoethoxydiphenyl borate. J Biol Chem 278: 27382-27389.
17. Columbaro M, Ravera S, Capanni C, Panfoli I, Cuccarolo P, Stroppiana G, et al. (2014). Treatment of FANCA cells with resveratrol and N-acetylcysteine: a comparative study. PLoS ONE 9: e104857.
18. Costa BL, Fawcett R, Li GY, Safa R, Osborne NN, (2008). Orally administered epigallocatechin gallate attenuates light-induced photoreceptor damage. Brain Res Bull 76: 412-423.
19. Dunaief JL, Dentchev T, Ying GS, Milam AH, (2002). The role of apoptosis in age-related macular degeneration. Arch Ophthalmol 120: 1435-1442.
20. Fain GL, Matthews HR, Cornwall MC, Koutalos Y, (2001). Adaptation in vertebrate photoreceptors. Physiol Rev 81: 117-151.
21. Fliesler SJ, Anderson RE, (1983). Chemistry and metabolism of lipids in the vertebrate retina. Prog Lipid Res 22: 79-131.
22. Genova ML, Baracca A, Biondi A, Casalena G, Faccioli M, Falasca AI, et al. (2008). Is supercomplex organization of the respiratory chain required for optimal electron transfer activity? Biochim Biophys Acta 1777: 740-746.
23. Gledhill JR, Montgomery MG, Leslie AG, Walker JE, (2007). Mechanism of inhibition of bovine F1-ATPase by resveratrol and related polyphenols. Proc Natl Acad Sci U S A 104: 13632-13637.
24. Gupta SK, Kumar B, Nag TC, Agrawal SS, Agrawal R, Agrawal P, et al. (2011). Curcumin prevents experimental diabetic retinopathy in rats through its hypoglycemic, antioxidant, and anti-inflammatory mechanisms. J Ocul Pharmacol Ther 27: 123-130.
25. Gurib-Fakim A, (2006). Medicinal plants: traditions of yesterday and drugs of tomorrow. Mol Aspects Med 27: 1-93.
26. Higdon JV, Frei B, (2003). Tea catechins and polyphenols: health effects, metabolism, and antioxidant functions. Crit Rev Food Sci Nutr 43: 89-143.
27. Huang TC, Chang HY, Hsu CH, Kuo WH, Chang KJ, Juan HF, (2008). Targeting therapy for breast carcinoma by ATP synthase inhibitor aurovertin B. J Proteome Res 7: 1433-1444.
28. Huynh T-P, Mann SN, Mandal NA, (2013). Botanical compounds: effects on major eye diseases. Evid Based Complement Alternat Med 2013: 549174.
29. Janik-Papis K, Ulińska M, Krzyzanowska A, Stoczynska E, Borucka AI, Wozniak K, et al. (2009). Role of oxidative mechanisms in the pathogenesis of age-related macular degeneration. Klin Oczna 111: 168-173.
30. Khandhadia S, Lotery A, (2010). Oxidation and age-related macular degeneration: insights from molecular biology. Expert Rev Mol Med 12: e34.
31. Kim DH, Kim JA, Choi JS, Joo CK, (2002). Activation of caspase-3 during degeneration of the outer nuclear layer in the rd mouse retina. Ophthalmic Res 34: 150-157.
32. Kim YH, Kim YS, Roh GS, Choi WS, Cho GJ, (2012). Resveratrol blocks diabetes-induced early vascular lesions and vascular endothelial growth factor induction in mouse retinas. Acta Ophthalmol 90: e31-e37.
33. Kook D, Wolf AH, Yu AL, Neubauer AS, Priglinger SG, Kampik A, et al. (2008). The protective effect of quercetin against oxidative stress in the human RPE in vitro. Invest Ophthalmol Vis Sci 49: 1712-1720.
34. Laemmli UK, (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
35. Lam S, Tso MO, Gurne DH, (1990). Amelioration of retinal photic injury in albino rats by dimethylthiourea. Arch Ophthalmol 108: 1751-1757.
36. Lang DR, Racker E, (1974). Effects of quercetin and F1 inhibitor on mitochondrial ATPase and energy-linked reactions in submitochondrial particles. Biochim Biophys Acta 333: 180-186.
37. Lee SR, Im KJ, Suh SI, Jung JG, (2003). Protective effect of green tea polyphenol (-)-epigallocatechin gallate and other antioxidants on lipid peroxidation in gerbil brain homogenates. Phytother Res 17: 206-209.
38. Liang FQ, Godley BF, (2003). Oxidative stress-induced mitochondrial DNA damage in human retinal pigment epithelial cells: a possible mechanism for RPE aging and age-related macular degeneration. Exp Eye Res 76: 397-403.
39. Linnett PE, Beechey RB, (1979). Inhibitors of the ATP synthethase system. Methods Enzymol 55: 472-518.
40. Linsenmeier RA, Braun RD, McRipley MA, Padnick LB, Ahmed J, Hatchell DL, et al. (1998). Retinal hypoxia in long-term diabetic cats. Invest Ophthalmol Vis Sci 39: 1647-1657.
41. Lu KT, Chiou RY, Chen LG, Chen MH, Tseng WT, Hsieh HT, et al. (2006). Neuroprotective effects of resveratrol on cerebral ischemia-induced neuron loss mediated by free radical scavenging and cerebral blood flow elevation. J Agric Food Chem 54: 3126-3131.
42. Mandal MN, Patlolla JM, Zheng L, Agbaga MP, Tran JT, Wicker L, et al. (2009). Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 46: 672-679.
43. Mangiullo R, Gnoni A, Leone A, Gnoni GV, Papa S, Zanotti F, (2008). Structural and functional characterization of F(o)F(1)-ATP synthase on the extracellular surface of rat hepatocytes. Biochim Biophys Acta 1777: 1326-1335.
44. Morelli AM, Ravera S, Calzia D, Panfoli I, (2013). Hypothesis of lipid-phase-continuity proton transfer for aerobic ATP synthesis. J Cereb Blood Flow Metab 33: 1838-1842.
45. Panfoli I, Musante L, Bachi A, Ravera S, Calzia D, Cattaneo A, et al. (2008). Proteomic analysis of the retinal rod outer segment disks. J Proteome Res 7: 2654-2669.
46. Panfoli I, Calzia D, Bianchini P, Ravera S, Diaspro A, Candiano G, et al. (2009). Evidence for aerobic metabolism in retinal rod outer segment disks. Int J Biochem Cell Biol 41: 2555-2565.
47. Panfoli I, Calzia D, Ravera S, Morelli AM, Traverso CE, (2012). Extra-mitochondrial aerobic metabolism in retinal rod outer segments: new perspectives in retinopathies. Med Hypotheses 78: 423-427.
48. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledge base of drug targets and their ligands. Nucl Acids Res 42 (Database Issue): D1098-D1106.
49. Pedersen PL, Amzel LM, (1993). ATP synthases. Structure, reaction center, mechanism, and regulation of one of nature's most unique machines. J Biol Chem 268: 9937-9940.
50. van Raaij MJ, Abrahams JP, Leslie AG, Walker JE, (1996). The structure of bovine F1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc Natl Acad Sci U S A 93: 6913-6917.
51. Ranchon I, Gorrand JM, Cluzel J, Droy-Lefaix MT, Doly M, (1999). Functional protection of photoreceptors from light-induced damage by dimethylthiourea and Ginkgo biloba extract. Invest Ophthalmol Vis Sci 40: 1191-1199.
52. Ravera S, Calzia D, Bianchini P, Diaspro A, Panfoli I, (2007). Confocal laser scanning microscopy of retinal rod outer segment intact disks: new labeling technique. J Biomed Opt 12: 050501.
53. Roehlecke C, Schumann U, Ader M, Brunssen C, Bramke S, Morawietz H, et al. (2013). Stress reaction in outer segments of photoreceptors after blue light irradiation. PLoS ONE 8: e71570.
54. Schnetkamp PP, (1981). Metabolism in the cytosol of intact isolated cattle rod outer segments as indicator for cytosolic calcium and magnesium ions. Biochemistry 20: 2449-2456.
55. Schnetkamp PP, Daemen FJ, (1982). Isolation and characterization of osmotically sealed bovine rod outer segments. Methods Enzymol 81: 110-116.
56. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, et al. (1999). Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144: 281-292.
57. Stefansson E, (2006). Ocular oxygenation and the treatment of diabetic retinopathy. Surv Ophthalmol 51: 364-380.
58. Stock D, Leslie AG, Walker JE, (1999). Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700-1705.
59. Wangsa-Wirawan ND, Linsenmeier RA, (2003). Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol 121: 547-557.
60. Woo JM, Shin DY, Lee SJ, Joe Y, Zheng M, Yim JH, et al. (2012). Curcumin protects retinal pigment epithelial cells against oxidative stress via induction of heme oxygenase-1 expression and reduction of reactive oxygen. Mol Vis 18: 901-908.
61. Wu J, Gorman A, Zhou X, Sandra C, Chen E, (2002). Involvement of caspase-3 in photoreceptor cell apoptosis induced by in vivo blue light exposure. Invest Ophthalmol Vis Sci 43: 3349-3354.
62. Zanotti F, Gnoni A, Mangiullo R, Papa S, (2009). Effect of the ATPase inhibitor protein IF1 on H+ translocation in the mitochondrial ATP synthase complex. Biochem Biophys Res Commun 384: 43-48.
63. Zhang B, Osborne NN, (2006). Oxidative-induced retinal degeneration is attenuated by epigallocatechin gallate. Brain Res 1124: 176-187.
64. Zhang B, Rusciano D, Osborne NN, (2008). Orally administered epigallocatechin gallate attenuates retinal neuronal death in vivo and light-induced apoptosis in vitro. Brain Res 1198: 141-152.
65. Zheng J, Ramirez VD, (2000). Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. Br J Pharmacol 130: 1115-1123.
66. Zhuang P, Shen Y, Lin BQ, Zhang WY, Chiou GC, (2011). Effect of quercetin on formation of choroidal neovascularization (CNV) in age-related macular degeneration (AMD). Eye Sci 26: 23-29.