Apitoxin protects rat pups brain from propionic acid-induced oxidative stress: The expression pattern of Bcl-2 and Caspase-3 apoptotic genes

NeuroToxicology

Volumn 49, Issue , 2015, Pages 121-131

  Khalil, Samah R ^a   Abd Elhakim, Yasmina M ^a   Selim, Manar E ^b,c   Al Ayadhi, Laila Y ^d  

^a Zagazig University   (Egypt)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c Ain Shams University   (Egypt)

^d KING SAUD UNIVERSITY   (Saudi Arabia)

Author keywords

Amygdala; Bee venom; Comet assay; Neural cell death; Oxidative stress Propionic acid

Indexed keywords

APITOXIN; BEE VENOM; CASPASE 3; CATALASE; DNA; GLUTATHIONE; MALONALDEHYDE; PROPIONIC ACID; PROTEIN BCL 2; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; MESSENGER RNA; PROPIONIC ACID DERIVATIVE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BCL 2 GENE; BRAIN FUNCTION; CASPASE 3 GENE; CONTROLLED STUDY; DISEASE MARKER; DNA DAMAGE; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FEMALE; GEL ELECTROPHORESIS; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; LIPID PEROXIDATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; NEWBORN; PREGNANCY; PROTEIN CARBONYLATION; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE;

APOIDEA; RATTUS;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BEE VENOMS; BRAIN; CASPASE 3; CATALASE; FEMALE; GENE EXPRESSION REGULATION; GLUTATHIONE; MALE; MALONDIALDEHYDE; OXIDATIVE STRESS; PREGNANCY; PROPIONATES; PROTEIN CARBONYLATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SUPEROXIDE DISMUTASE;

EID: 84935019896     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2015.05.011     Document Type: Article

References (88)

1. Abd-Elhakim Y.M., Khalil S.R., Awad A., AL-Ayadhi L.Y. Combined cytogenotoxic effects of bee venom and bleomycin on rat lymphocytes: an in vitro study. BioMed Res. Int. 2014, 1. 10.1155/2014/173903.
2. Acehan D., Jiang X., Morgan D.G., Heuser J.E., Wang X., et al. Three dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell 2002, 9:423-432.
3. Al-Dbass A.M. N-acetylcysteine reduces the neurotoxic effects of propionic acid in rat pups. J. King Saud Univ. 2014, 26:254-260.
4. Alfawaz H.A., Bhat R.S., Al-Ayadhi L., El-Ansary A.K. Protective and restorative potency of vitamin D on persistent biochemical autistic features induced in propionic acid-intoxicated rat pups. Complement. Altern. Med. 2014, 14:416.
5. Altieri F., Grillo C., Maceroni M., Chichiarelli S. DNA damage and repair: from molecular mechanisms to health implications. Antioxid. Redox Signal. 2008, 10:891-937.
6. Bancroft J.D., Stevens A. Theory and Practice of Histological Technique 1996, Churchill, Livingstone, New York, London, San Francisco, Tokyo. 4th ed.
7. Banks B.E., Brown C., Burgess G.M., Burnstock G., Claret M., Cocks T.M., Jenkinson D.H. Apamin blocks certain neurotransmitter-induced increases in potassium permeability. Nature 1979, 282(5737):415-417.
8. Beutler E., Dubon O.B., Kelly M. Improved method for the determination of blood glutathione. J. Lab. Clin. Med. 1963, 61:882-888.
9. Brass E.P., Beyerinck R.A. Effects of propionate and carnitine on the hepatic oxidation of short- and medium-chain-length fatty acids. J. Biochem. 1988, 250:819-825.
10. Celik I., Turker M., Tuluce Y. Abscisic acid and gibberellic acid cause increased lipid peroxidation and fluctuated antioxidant defense systems of various tissues in rats. J. Hazard. Mater. 2007, 148:623-629.
11. Cernanec J., Guilak F., Weinberg J.B., Pisetsky D.S., Fermor B. Influence of hypoxia and reoxygenation on cytokine-induced production of proinflammatory mediators in articular cartilage. Arthritis Rheum. 2002, 46(4):968-975.
12. Cho S.Y., Shim S.R., Rhee H.Y., Park H.J., Jung W.S., Moon S.K., Park J.M., Ko C.N., Cho K.H., Park S.U. Effectiveness of acupuncture and bee venom in idiopathic Parkinson's disease. Parkinsonism Relat. Disord. 2012, 18(8):948-952.
13. Chong Z.Z., Li F., Maiese K. Oxidative stress in the brain: novel cellular targets that govern survival during neurodegenerative disease. Prog. Neurobiol. 2005, 75:207-246.
14. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 1997, 326:1-16.
15. Crissman J.W., Goodman D.G., Hildebrandt P.K., Maronpot R.R., Prater D.A., Riley J.H. Best practice guideline: toxicologic histopathology. Toxicol. Pathol. 2004, 32:126-131.
16. D'Errico M., Parlanti E., Dogliotti E. Mechanism of oxidative DNA damage repair and relevance to human pathology. Mutat. Res. 2008, 659:4-14.
17. Doo A.R., Kim S.N., Kim S.T., Park J.Y., Chung S.H., Choe B.Y. Bee venom protects SH-SY5Y human neuroblastoma cells from 1-methyl-4-phenylpyridinium-induced apoptotic cell death. Brain Res. 2012, 1429:106-115.
18. Doo A.R., Kim S.T., Kim S.N., Moon W., Yin C.S., Chae Y., et al. Neuroprotective effects of bee venom pharmaceutical acupuncture in acute 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced mouse model of Parkinson's disease. Neurol. Res. 2010, 32(Suppl. 1):88-91.
19. Duncan D.B. Multiple range and multiple F-test. Biometrics 1955, 11:1-42.
20. Earnshaw W.C., Martins L.M., Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 1999, 68:383-424.
21. El-Ansary A., Nounou H., Abdelzaher E. Effectivness of creatine and cyclosporine to protect against propionic acid-induced neurotoxicity. Int. J. Pharmacol. Toxicol. Sci. 2011, 2:28-43.
22. El-Ansary A.K., Al-Daihan S., Bacha A.B., Shaker G.H., Al-Ayadhi L.A. Comparative study on the protective effect of carnosine and carnitine against pro-inflammatory/pro-oxidant effects of clindamycin and propionic acid administrations to hamsters. Afr. J. Microbiol. Res. 2013, 7(2):103-114. http://www.academicjournals.org/AJMR, 10.5897/AJMR12.1178.
23. El-Ansary A.K., Ben B.A., Kotb M. Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J. Neuroinflammation 2012, 9:74.
24. Evans P., Halliwell B. Micronutrients: oxidant/antioxidant status. Br. J. Nutr. 2001, 85:67-74.
25. Feliz B., Witt D.R., Harris B.T. Propionic acidemia: a neuropathology casereport and review of prior cases. Arch. Pathol. Lab. Med. 2003, 127:e325-e328.
26. Fernandes-Pedrosa M.F., Felix-Silva J., Menezes Y.A.S. Toxins from venomous animals: gene cloning, protein expression and biotechnological applications. An Integrated View of the Molecular Recognition and Toxinology: From Analytical Procedures to Biomedical Applications 2013, 10.5772/52380.
27. Fernandez-Garcia E., McGregor J.U. Determination of organic acids during the fermentation and cold storage of yogurt. J. Dairy Sci. 1994, 77:2934-2939.
28. Fontella F.U., Pulrolnik V., Gassen E., Wannmacher C.M., Klein A.B., Wajner M., Dutra-Filho C.S. Propionic and l-methylmalonic acids induce oxidative stress in brain of young rats. Neuroreport 2000, 11:541-544.
29. Furian A.F., Fighera M.R., Oliveira M.S., Ferreira A.P., Fiorenza N.G., de Carvalho Myskiw J., Petry J.C., Coelho R.C., Mello C.F., Royes L.F. Methylene blue prevents methylmalonate-induced seizures and oxidative damage in rat striatum. Neurochem. Int. 2007, 50:164-171.
30. Gajski G., Garaj-Vrhovac V. Radioprotective effects of honeybee venom (Apis mellifera) against 915-MHz microwave radiation-induced DNA damage in wistar rat lymphocytes: in vitro study. Int. J. Toxicol. 2009, 28:88-98.
31. Geret F., Serafim A., Barreira L., Bebianno M.J. Effect of cadmium on antioxidant enzyme activities and lipid peroxidation in the gills of the clam Ruditapes decussatus. Biomarkers 2002, 7:242-256.
32. Gupta R., Deshpande S.B. 3-Nitropropionic acid depresses spinal reflexes involving GABAergic and glycinergic transmission in neonatal rat spinal cord in vitro. Life Sci. 2008, 83(21-22):756-760.
33. Halliwell B., Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. Br. J. Pharmacol. 2004, 142:231-255.
34. Han S.M., Lee K.G., Yeo J.H., Kweon H.Y., Woo S.O., Lee M.Y., Baek H.J., Park K.K. Effect of venom from the Asian honeybee (Apis cerana Fab.) on LPS-induced nitric oxide and tumor necrosis factor-α production in RAW 264.7 cell line. J. Apic. Res. 2006, 45:131-136.
35. Han S.M., Lee K.G., Yeo J.H., Oh B.Y., Kim B.S., Lee W., et al. Effects of honeybee venom supplementation in drinking water on growth performance of broiler chickens. Poult. Sci. 2010, 89(11):2396-2400. 10.3382/ps.2010-00915.
36. Haque M.N., Chowdhury R., Islam K.M.S., Akbar1 M.A., Bang J. Propionic acid is an alternative to antibiotics in poultry diet. Anim. Sci. 2009, 38(1-2):115-122.
37. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu Sasamata M., Yuan J., Moskowitz MA: Inhibition of interleukin 1 beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:2007-2012.
38. Hartmann A., Agurell E., Beevers C., Brendler-Schwaab S., Burlinson B., Clay P., et al. Recommendations for conducting the in vivo alkaline comet assay. Mutagenesis 2003, 18:45-51.
39. Indo H.P., Davidson M., Yen H.C., Suenaga S., Tomita K., Nishii T., et al. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 2007, 7:106-118.
40. Jan G., Belzacq A.S., HaOuzi D., et al. Propionibacteria induce apoptosis of colorectal carcinoma cells via short chain fatty acids acting on mitochondria. Cell Death Differ. 2002, 9:179-188.
41. Kim J.I., Yang E.J., Lee M.S., Kim Y.S., Huh Y., Cho I.H., et al. Bee venom reduces neuroinflammation in the MPTP-induced model of Parkinson's disease. Int. J. Neurosci. 2011, 121:209-217.
42. Kim M.J., Park S.D., Lee A.R., Kim K.H., Jang J.H., Kim K.S. The effect of bee venom acupuncture on protease activity and free radical damage in synovial fluid from collagen-induced arthritis in rats. J. Korean Acu. Mox. Soc. 2002, 19(5):161-175.
43. Kim J.Y., cho S.H., kim Y.W., Jang E.C., Park S.Y., Kim E.J., Le S.K. Efects of BCG, lymphotoxin and bee venom on insulitis and development of IDDM in non-obese diabetic mice. J. Korean Med. Sci. 1999, 14(6):648-652.
44. Kim K.H., Kum Y.S., Park Y.Y., et al. The protective effect of bee venom against ethanol-induced hepatic injury via regulation of the mitochondria-related apoptotic pathway. Basic Clin. Pharmacol. Toxicol. 2010, 107:619-624.
45. Korsmeyer S.J. Bcl-2 gene family and the regulation of programmed cell death. Cancer Res. 1999, (Suppl. 59):1693s-1700s.
46. Kwon Y.B., Lee H., Han H.J., Mar W.C., Kang S.K., Yoon O.B., Beitz A.J., Lee J.H. The water-soluble fraction of bee venom produces antinociceptive and anti-inflammatory effects on rheumatoid arthritis in rats. Life Sci. 2002, 71:191-204.
47. Lee J.D., Park H.J., Chae Y., Lim S. An overview of bee venom acupuncture in the treatment of arthritis. Evid. Based Complement. Alternat. Med. 2005, 2:79-84.
48. Lee S.H., Choi S.M., Yang E.J. Melittin ameliorates the inflammation of organs in an amyotrophic lateral sclerosis animal model. Exp. Neurobiol. 2014, 23(1):86-92. 10.5607/en.2014.23.1.86.
49. Lee M.J., Jang M., Choi J., Lee G., Min H.J., Chung W.S., Kim J.I., Jee Y., Chae Y., Kim S.H., Lee S.J., Cho I.H. Bee venom acupuncture alleviates experimental autoimmune encephalomyelitis by upregulating regulatory T cells and suppressing Th1 and Th17 responses. Mol. Neurobiol. 2015, 10.1007/s12035-014-9012-2.
50. Levine R.L., Williams J.A., Stadtman E.R., Shacter E. Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 1994, 233:346-357.
51. Lin S.Y., Lai W.W., Ho C.C., Yu F.S., Chen G.W., et al. Emodin induces apoptosis of human tongue squamous cancer SCC-4 cells through reactive oxygen species and mitochondria-dependent pathways. Anticancer Res. 2009, 29:327-335.
52. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
53. Liu X., Yao J., Pisha E., Yang Y., Hua Y., Breemen R.B., Bolton J.L. Oxidative DNA damage induced in equine estrogen metabolites: role of estrogen receptor alpha. Chem. Res. Toxicol. 2002, 15:512-519.
54. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-δδCT method. Methods 2001, 25(4):402-408.
55. MacFabe D.F., Rodriguez-Capote K., Hoffman J.E., Franklin A.E., Mohammad-Asef Y., et al. A novel rodent model of autism: intraventricular infusions of propionic acid increase locomotors activity and induce neuroinflammation and oxidative stress in discrete regions of adult rat brain. Am. J. Biochem. Biotechnol. 2008, 4(2):146-166.
56. Marcos M.V., José F., Machado M., Sônia C., Daróz de M., Mônica Maria de A. Mixture of formic and propionic acid as additives in broiler feeds. Sci. Agric. 2004, 61:371-375.
57. Markesbery W.R., Lovell M.A. DNA oxidation in Alzheimer's disease. Antioxid. Redox Signal. 2006, 8:2039-2045.
58. Mirshafiey A. Venom therapy in multiple sclerosis. Neuropharmacology 2007, 53:353-361.
59. Misra H.P., Fridovich I. The role of superoxide anion autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 1972, 247:3170.
60. Moon D.O., Park S.Y., Heo M.S., Kim K.C., Park C., Ko W.S. Key regulators in bee venom-induced apoptosis are Bcl-2 and caspase-3 in human leukemic U937 cells through downregulation of ERK and Akt. Int. Immunopharmacol. 2006, 6:1796-1807.
61. Nakao S., MoriyaY, Furuyama S., et al. Propionic acid stimulates superoxide generation in human neutrophils. Cell Biol. Int. 1998, 22:331-337.
62. Nutt L.K., Chandra J., Pataer A., Fang B., Roth J.A., et al. Bax-mediated Ca2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 2002, 277:20301-20308.
63. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
64. Park H.J., Son D.J., Lee C.W., Choi M.S., Lee U.S., Song H.S., et al. Melittin inhibits inflammatory target gene expression and mediator generation via interaction with Ikappa B kinase. Biochem. Pharmacol. 2007, 73:237-247.
65. Park J.H., Kim K.H., Kim S.J., Lee W.R., Lee K.G., Park K.K. Bee venom protects hepatocytes from tumor necrosis factor-alpha and actinomycin D. Arch. Pharm. Res. 2010, 33(2):215-223. 10.1007/s12272-010-0205-6.
66. Parke D.V., Lewis D.F. Safety aspects of food preservatives. Food Addit. Contam. 1992, 9:561-577.
67. Ribas G.S., Manfredini V., de Mari J.F., Wayhs C.Y., Vanzin C.S., Biancini G.B., et al. Reduction of lipid and protein damage in patients with disorders of propionate metabolism under treatment: a possible protective role of l-carnitine supplementation. Int. J. Dev. Neurosci. 2010, 28:127-132.
68. Rigo F.K., Pasquetti L., Malfatti C.R., Fighera M.R., Coelho R.C., Petri C.Z., Mello C.F. Propionic acid induces convulsions and protein carbonylation in rats. Neurosci. Lett. 2006, 408:151-154.
69. Romero-Curiel A., López-Carpinteyro D., Gamboa C., De la Cruz F., Zamudio S., Flores G. Apamin induces plastic changes in hippocampal neurons in senile Sprague-Dawley rats. Synapse 2011, 13:1062-1072. 10.1002/syn. 20938.
70. Samson F.E., Nelson S.R. The aging brain, metals and oxygen free radicals. Cell Mol. Biol. 2000, 46:699-707.
71. Schwab M.A., Sauer S.W., Okun J.G., Nijtmans L.G., Rodenburg R.J., van den L.P., et al. Secondary mitochondrial dysfunction in propionic aciduria: a pathogenic role for endogenous mitochondrial toxins. Biochem. J. 2006, 398:107-112.
72. Shuba M.F., Vladimirova I.A. Effect of apamin on the electrical responses of smooth muscle to adenosine 5'-triphosphate and to nonadrenergic, non cholinergic nerve stimulation. Neuroscience 1980, 5(5):853-859.
73. Shultz S.R., MacFabe D.F., Ossenkopp K.P., Scratch S., Whelan J., Taylor R., Cain D.P. Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 2008, 54:901-911.
74. Singh N., McCoy M., Tice R., Schneider E. A simple technique for quantification of low levels of DNA damage in individuals cells. Exp. Cell Res. 1988, 175:184-191.
75. Sinha A.K. Colorimetric assay of catalase. Anal. Biochem. 1972, 47:389-394.
76. Somerfield S.D., Stach J.L., Mraz C., Gervais F., Skamene E. Bee venom melittin blocks neutrophil O2- production. Inflammation 1986, 10(2):175-182.
77. Son D.J., Lee J.W., Lee Y.H., Song H.S., Lee C.K., Hong J.T. Therapeutic application of anti-arthritis, pain releasing, and anti-cancer effects of bee venom and its constituent compounds. Pharmacol. Ther. 2007, 115(2):246-270.
78. Suh S.J., Kim K.S., Kim M.J., Chang Y.C., Lee S.D., Kim M.S., Kwon D.Y., Kim C.H. Effects of bee venom on protease activities and free radical damages in synovial fluid from type II collagen-induced rheumatoid arthritis rats. Toxicol. In Vitro 2006, 20(8):1465-1471. Epub 2006 Jul 28.
79. Thomas R.H., Foley K.A., Mepham J.R., Tichenoff L.J., Possmayer F., MacFabe D.F. Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J. Neurochem. 2010, 113:515-529.
80. Tu W.C., Wu C.C., Hsieh H.L., Chen C.Y., Hsu S.L. Honeybee venom induces calcium-dependent but caspase independent apoptotic cell death in human melanoma A2058 cells. Toxicon 2008, 52(2):318-329.
81. Varanda E.A., Monti R., Tavares D.C. Inhibitory effect of propolis and bee venom on the mutagenicity of some direct- and indirect-acting mutagens. Teratog. Carcinog. Mutagen. 1999, 19(6):403-413.
82. Varanda E.A., Takahashi C. Effect of pre-treatment with venom of Apis mellifera bees on the yield of gamma-ray induced chromosome aberrations in human blood lymphocytes. Rev. Bras. Genet. 1993, 16:551-559.
83. Verma R.S., Mehta A., Srivastava N. Comparative studies on chlorpyrifos and methyl parathion induced oxidative stress in different parts of rat brain: attenuation by antioxidant vitamins. Pest. Biochem. Physiol. 2009, 95:152-158.
84. Wajner M., Latini A., Wyse A.T., Dutra-Filho C.S. The role of oxidative damage in the neuropathology of organic acidurias: insights from animal studies. J. Inherit. Metab. Dis. 2004, 27:427-448.
85. Wyatt I., Farnworth M., Gyte A.J., et al. L-2-Chloropropionic acid metabolism and disposition in male rats: relevance to cerebellar injury. Arch. Toxicol. 1997, 71(11):668-676.
86. Xu F.L., Fan T., Duan J.J., Chen D. Clinical analysis of organic acidemia in neonates from neonatal intensive care units. Zhongguo Dang Dai Er Ke Za Zhi 2012, 14(5):336-339.
87. Yang E.J., Jiang J.H., Lee S.M., Yang S.C., Hwang H.S., Lee M.S., Choi S.M. Bee venom attenuates neuroinflammatory events and extends survival in amyotrophic lateral sclerosis models. Neuroinflammation 2010, 7:69. 10.1186/1742-2094-7-69.
88. Zarate G., Gonzalez S., Chaia A.P. Assessing survival of dairy propionibacteria in gastrointestinal conditions and adherence to intestinal epithelia. Methods Mol. Biol. 2004, 268:423-432.