Brazilian pampa biome honey protects against mortality, locomotor deficits and oxidative stress induced by hypoxia/ reperfusion in adult Drosophila melanogaster

Neurochemical Research

Volumn 41, Issue 1-2, 2016, Pages 116-129

  Cruz, L C ^a,b   Ecker, A ^b   Dias, R S ^b   Seeger, R L ^b   Braga, M M ^a   Boligon, A A ^b   Martins, I K ^a   Costa Silva, D G ^a   Barbosa, N V ^b   Canedo A D ^a   Posser, T ^a   Franco, J L ^a  

^a UNIVERSIDADE FEDERAL DO PAMPA   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

Author keywords

Antioxidant; Drosophila; Gene expression; Honey; Hypoxia; Oxidative stress

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; 2,2' AZINOBIS(3 ETHYLBENZOTHIAZOLINE 6 SULFONIC ACID); APIGENIN; CAFFEIC ACID; CASPASE 3; CASPASE 9; CHLOROGENIC ACID; CHRYSIN; FERULIC ACID; FLAVONOID; GALLIC ACID; HEAT SHOCK PROTEIN 27; HOX PROTEIN; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KAEMPFEROL; MESSENGER RNA; NATURAL PRODUCT; PARA COUMARIC ACID; PHENOL DERIVATIVE; PROTEIN KINASE B; QUERCETIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROSMARINIC ACID; SOMATOMEDIN RECEPTOR; TRANSCRIPTION FACTOR NRF2; UBIQUINOL CYTOCHROME C REDUCTASE; ANTIOXIDANT;

ABTS RADICAL SCAVENGING ASSAY; ADULT; ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APIS MELLIFERA; ARTICLE; BRAZIL; CONTROLLED STUDY; DPPH RADICAL SCAVENGING ASSAY; DROSOPHILA MELANOGASTER; DRUG DETERMINATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HONEY; HYPOXIA; IN VITRO STUDY; LIFESPAN; LOCOMOTION; MITOCHONDRIAL MEMBRANE; MORTALITY; NEUROMUSCULAR DISEASE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PAMPAS; PHYTOCHEMISTRY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ANALYSIS; ANIMAL; GENETICS; REPERFUSION INJURY; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; ANTIOXIDANTS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DROSOPHILA MELANOGASTER; FLAVONOIDS; GENE EXPRESSION; HONEY; LOCOMOTION; OXIDATIVE STRESS; PHENOLS; REPERFUSION INJURY; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84945587327     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-015-1744-5     Document Type: Article

References (59)

1. Rodriguez BA, Mendoza S, Iturriga MH, Castano-Tostado E (2012) Quality parameters and antioxidant and antibacterial properties of some Mexican honeys. J Food Sci 77: C121-C127
2. Bogdanov S, Jurendic T, Sieber R, Gallmann P (2008) Honey for nutrition and health: a review. J Am Coll Nutr 27: 677-689
3. Wang J, Li QX (2011) Chemical composition, characterization, and differentiation of honey botanical and geographical origins. Adv Food Nutr Res 62: 89-137
4. Zalibera M, Stasko A, Slebodova A, Jancovicova V, Cermakova T, Brezova V (2008) Antioxidant and radical-scavenging activities of Slovak honeys-an electron paramagnetic resonance study. Food Chem 110: 512-521
5. Cruz LC, Batista JE, Zemolin AP, Nunes ME, Lippert DB, Royes LF, Soares FA, Pereira AB, Posser P, Franco JL (2014) A study on the quality and identity of Brazilian Pampa biome honey: evidences for its beneficial effects against oxidative stress and hyperglycemia. Int J Food Sci 2014: 1-11
6. Erejuwa OO, Sulaiman SA, Ab Wahab MS (2012) Honey: a novel antioxidant. Molecules 17: 4400-4423
7. Abdulrhman M, El Hefnawy M, Ali R, Abdel Hamid I, Abou El-Goud A, Refai D (2013) Effects of honey, sucrose and glucose on blood glucose and C-peptide in patients with type 1 diabetes mellitus. Complement Ther Clin Pract 19: 15-19
8. Erejuwa OO, Gurtu S, Sulaiman SA, Ab Wahab MS, Sirajudeen KN, Salleh MS (2010) Hypoglycemic and antioxidant effects of honey supplementation in streptozotocin-induced diabetic rats. Int J Vitam Nutr Res 80: 74-82
9. Jimenez-Del-Rio M, Guzman-Martinez C, Velez-Pardo C (2010) The effects of polyphenols on survival and locomotor activity in Drosophila melanogaster exposed to iron and paraquat. Neurochem Res 35: 227-238
10. Ortega-Arellano HF, Jimenez-Del-Rio M, Velez-Pardo C (2011) Life span and locomotor activity modification by glucose and polyphenols in Drosophila melanogaster chronically exposed to oxidative stress-stimuli: implications in Parkinson’s disease. Neurochem Res 36: 1073-1086
11. Paula MT, Zemolin AP, Vargas AP, Golombieski RM, Loreto EL, Saidelles AP, Picoloto RS, Flores EM, Pereira AB, Rocha JB, Merritt TJ, Franco JL, Posser T (2014) Effects of Hg(II) exposure on MAPK phosphorylation and antioxidant system in D. melanogaster. Environ Toxicol 29: 621-630
12. Gheldof N, Wang XH, Engeseth NJ (2002) Identification and quantification of antioxidant components of honeys from various floral sources. J Agric Food Chem 50: 5870-5877
13. Boligon AA, Piana M, Schawnz TG, Pereira RP, Rocha JB, Athayde ML (2014) Chromatographic analysis and antioxidant capacity of Tabernaemontana catharinensis. Nat Prod Commun 9: 61-64
14. Singleton VL, Orthofer R, Lamuela-Ravent’os RM (1998) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299: 152-178
15. Baltrušaityté V, Venskutonis PR, Čeksteryté V (2007) Radical scavenging activity of different floral origin honey and beebread phenolic extracts. Food Chem 101: 502-514
16. Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of '‘antioxidant power’': the FRAP assay. Anal Biochem 239: 70-76
17. Braga MM, Rico EP, Cordova SD, Pinto CB, Blaser RE, Dias RD, Rosemberg DB, Oliveira DL, Souza DO (2013) Evaluation of spontaneous recovery of behavioral and brain injury profiles in zebrafish after hypoxia. Behav Brain Res 253: 145-151
18. Azad P, Zhou D, Russo E, Haddad GG (2009) Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS One 4(4): e5371
19. Magwere T, Chapman T, Partridge L (2004) Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster. J Gerontol A-Biol 59: 3-9
20. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
21. Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77: 398-405
22. Aebi H (1984) Catalase in vitro. Methods Enzymol 105: 121-126
23. Kostyuk VA, Potapovich AI (1989) Superoxide-driven oxidation of quercetin and a simple sensitive assay for determination of superoxide dismutase. Biochem Int 19: 1117-1124
24. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7: 88-95
25. Holmgren A, Bjornstedt M (1995) Thioredoxin and thioredoxin reductase. Methods Enzymol 252: 199-208
26. Miwa S, St-Pierre J, Partridge L, Brand MD (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic Biol Med 35: 938-948
27. Puntel RL, Roos DH, Seeger RL, Rocha JB (2013) Mitochondrial electron transfer chain complexes inhibition by different organochalcogens. Toxicol In Vitro 27: 59-70
28. Perez-Severiano F, Santamaria A, Pedraza-Chaverri J, Medina-Campos ON, Rios C, Segovia J (2004) Increased formation of reactive oxygen species, but no changes in glutathione peroxidase activity, in striata of mice transgenic for the Huntington’s disease mutation. Neurochem Res 29: 729-733
29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408
30. Codex Alimentarius (2001) Revised codex standard for honey. Codex STAN 12-198
31. Sun J, Li YZ, Ding YH, Wang J, Geng J, Yang H, Ren J, Tang JY, Gao J (2014) Neuroprotective effects of gallic acid against hypoxia/reoxygenation-induced mitochondrial dysfunctions in vitro and cerebral ischemia/reperfusion injury in vivo. Brain Res 1589: 126-139
32. Pandey AK, Patnaik R, Muresanu DF, Sharma A, Sharma HS (2012) Quercetin in hypoxia-induced oxidative stress: novel target for neuroprotection. Int Rev Neurobiol 102: 107-146
33. Wei X, Zhao L, Ma Z, Holtzman DM, Yan C, Dodel RC, Hampel H, Oertel W, Farlow MR, Du Y (2004) Caffeic acid phenethyl ester prevents neonatal hypoxic-ischaemic brain injury. Brain 127: 2629-2635
34. Guven M, Aras AB, Akman T, Sen HM, Ozkan A, Salis O, Sehitoglu I, Kalkan Y, Silan C, Deniz M, Cosar M (2015) Neuroprotective effect of p-coumaric acid in rat model of embolic cerebral ischemia. Iran J Basic Med Sci 18: 356-363
35. Melstrom LG, Salabat MR, Ding XZ, Strouch MJ, Grippo PJ, Mirzoeva S, Pelling JC, Bentrem DJ (2011) Apigenin downregulates the hypoxia response genes: HIF-1alpha, GLUT-1, and VEGF in human pancreatic cancer cells. J Surg Res 167: 173-181
36. Mylonis I, Lakka A, Tsakalof A, Simos G (2010) The dietary flavonoid kaempferol effectively inhibits HIF-1 activity and hepatoma cancer cell viability under hypoxic conditions. Biochem Biophys Res Commun 398: 74-78
37. Fu B, Xue J, Li Z, Shi X, Jiang BH, Fang J (2007) Chrysin inhibits expression of hypoxia-inducible factor-1alpha through reducing hypoxia-inducible factor-1alpha stability and inhibiting its protein synthesis. Mol Cancer Ther 6: 220-226
38. Park JJ, Hwang SJ, Park JH, Lee HJ (2015) Chlorogenic acid inhibits hypoxia-induced angiogenesis via down-regulation of the HIF-1alpha/AKT pathway. Cell Oncol (Dordr) 38: 111-118
39. Lin WC, Peng YF, Hou CW (2015) Ferulic acid protects PC12 neurons against hypoxia by inhibiting the p-MAPKs and COX-2 pathways. Iran J Basic Med Sci 18: 478-484
40. Jeon YJ, Song KS, Han HJ, Park SH, Chang W, Lee MY (2014) Rosmarinic acid inhibits chemical hypoxia-induced cytotoxicity in primary cultured rat hepatocytes. Arch Pharm Res 37: 907-915
41. Li XL, Liu JX, Li P, Zheng YQ (2014) Protective effect of rosmarinic acid on hypoxia/reoxygenation injury in cardiomyocytes. Zhongguo Zhong Yao Za Zhi 39: 1897-1901
42. Chaudhary A, Bag S, Barui A, Banerjee P, Chatterjee J (2015) Honey dilution impact on in vitro wound healing: normoxic and hypoxic condition. Wound Repair Regen 23: 412-422
43. Zhao HW, Haddad GG (2011) Review: hypoxic and oxidative stress resistance in Drosophila melanogaster. Placenta 32(Suppl 2): S104-S108
44. Vigne P, Tauc M, Frelin C (2009) Strong dietary restrictions protect Drosophila against anoxia/reoxygenation injuries. PLoS ONE 4: e5422
45. Biddlestone J, Bandarra D, Rocha S (2015) The role of hypoxia in inflammatory disease (review). Int J Mol Med 35: 859-869
46. Solaini G, Baracca A, Lenaz G, Sgarbi G (2010) Hypoxia and mitochondrial oxidative metabolism. Biochim Biophys Acta 1797: 1171-1177
47. Feala JD, Coquin L, Zhou D, Haddad GG, Paternostro G, McCulloch AD (2009) Metabolism as means for hypoxia adaptation: metabolic profiling and flux balance analysis. BMC Syst Biol 3: 91
48. Jahromi SR, Haddadi M, Shivanandappa T, Ramesh SR (2013) Neuroprotective effect of Decalepis hamiltonii in paraquat-induced neurotoxicity in Drosophila melanogaster: biochemical and behavioral evidences. Neurochem Res 38: 2616-2624
49. Khurana P, Ashraf QM, Mishra OP, Delivoria-Papadopoulos M (2002) Effect of hypoxia on caspase-3,-8, and-9 activity and expression in the cerebral cortex of newborn piglets. Neurochem Res 27: 931-938
50. Papandreou I, Cairns RA, Fontana L, Lim AL, Denko NC (2006) HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab 3: 187-197
51. Perkins G, Hsiao YH, Yin S, Tjong J, Tran MT, Lau J, Xue J, Liu S, Ellisman MH, Zhou D (2012) Ultrastructural modifications in the mitochondria of hypoxia-adapted Drosophila melanogaster. PLoS ONE 7: e45344
52. Lukyanova LD (2013) Mitochondrial signaling in hypoxia. Open J Endocr Metab Dis 3: 20-32
53. Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284: 13291-13295
54. Nguyen T, Sherratt PJ, Huang HC, Yang CS, Pickett CB (2003) Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element. Degradation of Nrf2 by the 26 S proteasome. J Biol Chem 278: 4536-4541
55. Karlsson M, Kurz T, Brunk UT, Nilsson SE, Frennesson CI (2010) What does the commonly used DCF test for oxidative stress really show? Biochem J 428: 183-190
56. Copin JC, Pinteaux E, Ledig M, Tholey G (1995) 70-kDa heat shock protein expression in cultured rat astrocytes after hypoxia: regulatory effect of almitrine. Neurochem Res 20: 11-15
57. Tokyol C, Karaorman G, Bastug M (2005) Effects of acute and adaptive hypoxia on heat shock protein expression in hepatic tissue. High Alt Med Biol 6: 247-255
58. Bandarra D, Biddlestone J, Mudie S, Muller HA, Rocha S (2014) Hypoxia activates IKK-NF-kappaB and the immune response in Drosophila melanogaster. Biosci Rep 34(4): 429-440
59. Bandarra D, Biddlestone J, Mudie S, Muller HA, Rocha S (2015) HIF-1alpha restricts NF-kappaB-dependent gene expression to control innate immunity signals. Dis Model Mech 8: 169-181