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Ameliorative effect of probiotics (Lactobacillus paracaseii and Protexin®) and prebiotics (propolis and bee pollen) on clindamycin and propionic acid-induced oxidative stress and altered gut microbiota in a rodent model of autism
Corresponding Author(s) : Afaf Ansary
Cellular and Molecular Biology,
Vol. 65 No. 1: Issue 1
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- References
- Belzung C, Leman S, Vourc'h, P Andres C, Rodent models for autism: a critical review, Drug Discov. Today Dis. Model. 2005;2: 93–101
- Foley KA, MacFabe DF, Vaz A, Ossenkopp KP, Kavaliers M. Sexually dimorphic effects of prenatal exposure to propionic acid and lipopolysaccharide on social behavior in neonatal, adolescent,and adult rats: implications for autism spectrum disorders. Int J Dev Neurosci. 2014b ;39:68-78.
- MacFabe, D.F. Cain, D.P. Rodriguez-Capote, K. Franklin, A.E. Hoffman, J.E. Boon, F. Taylor, A.R. Kavaliers, M. Ossenkopp, K.P. Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders, Behav. Brain Res. 2007 ;176 (1): 149–169.
- El-Ansary AK, Ben Bacha A, Kotb M Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J Neuroinflammation. 2012; 9:74.
- Xiong X, Liu D, Wang Y, Zeng T, Peng Y. Urinary 3-(3-hydroxyphenyl)-3-hydroxypropionic acid, 3-hydroxyphenylacetic acid, and 3-Hydroxyhippuric acid are elevated in children with autism spectrum disorders BioMed Res. Int. 2016 9485412, 10.1155/2016/9485412
- Salminen MK, Rautelin H, Tynkkynen S, Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin. Infect. Dis; 2004. 38, 62–69.
- Vibhute VM, Shelke RR, Chavan SD, Nage SP, Effect of probiotics supplementation on the performance of lactating crossbred cows. Vet. World 2011 4, 557–561.
- Chaucheyras F, Durand H, Probiotics in animal nutrition and health. Benef. Microbes 2010 25, 3–9.
- Preedy VR, Watson RR , Probiotics, prebiotics and synbiotics, second ed. Langford, London. 2016.
- McFarland LV. Meta-analysis of probiotics for the prevention of traveler's diarrhea. Travel Med Infect Dis. 2007;2:97-105.
- Hickson M. Probiotics in the prevention of antibiotic-associated diarrhoea and Clostridium difficile infection. Therap Adv Gastroenterol. 2011; 4(3): 185–197.
- Alison Sinclair, , Xuanqian Xie, , Lama Saab, Nandini Dendukuri, Lactobacillus probiotics in the prevention of diarrhea associated with Clostridium difficile: a systematic review and Bayesian hierarchical meta-analysis. CMAJ Open. 2016 4(4): 706–718.
- Trevor D. Lawley, Simon Clare, Alan W. Walker1., Mark D. Stares, Thomas R. Connor, Claire Raisen, David Goulding, Roland Rad, Fernanda Schreiber1, Cordelia Brandt1, Laura J. Deakin, Derek J. Pickard, Sylvia H. Duncan, Harry J. Flint, Taane G. Clark, Julian Parkhill, Gordon Dougan. Targeted Restoration of the Intestinal Microbiota with a Simple, Defined Bacteriotherapy Resolves Relapsing Clostridium difficile Disease in Mice.. PLOS pathogens, 2012 8: e1002995.
- Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H. An¬tioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsome. Steroids.1994; 159,383
- Jagota SK, Dani HMA. New colorimetric technique for the estimation of Vitamin C using Folin phenol reagent. Anal Bio¬chem.1982; 15, 178.
- Beutle E, Duran O, Kelly BM Improved method for the determi¬nation of blood glutathione. J Lab Clin Med. 1963; 61, 882.
- Habig WH, Pabst MJ, Jacoby WB, G. Glutathione-S-transferase, the first enzymatic step . J Biol Chem 1974; 249, 7130–9.
- Ewing,W.HEdwards and Ewing's identification of Enterobacteriaceae, 4th ed. Elsevier Science Publishing Co., Inc., New York, N.Y. 1986.
- Isenberg, H.D. Clinical microbiology procedures handbook. Am. Soc. Microbiol. Wash. P. 1;1994
- Al-Dbass A Effect of N-Acetylcysteine in ameliorating the neurtoxic effects of propionic acid in rat pups, King Saud university journal [science], 2014 26(4), 254–260.
- Allen J W, Shanker G. Aschner M. Methylmercury inhibits the in vitro uptake of the glutathione precursor, cystine, in astrocytes, but not in neurons. Brain Res. 2001a 894, 131–140.
- Ares AM, Valverde S, Bernal JL, Nozal MJ, Bernal J. Extraction and determination of bioactive compounds from bee pollen. J Pharm Biomed Anal. 2018 147:110-124. 8.
- Oryan A, Alemzadeh E, Moshiri A. Potential role of propolis in wound healing: Biological properties and therapeutic activities. Biomed Pharmacother. 2018 ;98:469-483. 27.
- Pasupuleti VR, Sammugam L, Ramesh N, Gan SH. Honey, Propolis, and Royal Jelly: A Comprehensive Review of Their BiologicalActions and Health Benefits. Oxid Med Cell Longev. 2017:1259510.
- Andrade JKS, Denadai M, de Oliveira CS, Nunes ML, Narain N. Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Res Int. 2017; 101:129-138.
- Nanaware S, Shelar M, Sinnathambi A, Mahadik KR, Lohidasan S. Neuroprotective effect of Indian propolis in β-amyloid induced memory deficit: Impact on behavioral and biochemical parameters in rats. Biomed Pharmacother. 2017 ; 93:543-553. 4.
- Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, et al. Probiotic yogurt improvesantioxidant status in type 2 diabetic patients.Nutrition 2012; 28(5) 539–543.
- Asemi Z, Jazayeri S, Najafi M, Samimi M, Mofid V, Shidfar F, Shakeri H, Esmaillzadeh A. Effect of daily consumption of probiotic yogurt on oxidative stress in pregnantwomen: a randomized controlled clinical trial. Annals of Nutrition and Metabolism 2012; 60(1):62-68.
- Zhang Y, Du R, Wang L, Zhang H. The antioxidative effects of probiotic Lactobacilluscasei Zhang on the hyperlipidemic rats. European Food Research and Technology 2010; 231(1)151-158.
- Wang AN,Yi XW, Yu HF, Dong B, Qiao SY. Free radical scavenging activity ofLactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs.Journal of Applied Microbiology 2009; 107(4)1140-1148.
- Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, et al. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile associated diarrhea. J Infect Dis . 2008. 197: 435–438.
- Robinson CJ, Bohannan BJ, Young VB From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 2010 74: 453–476.
- Borody TJ, Warren EF, Leis SM, Surace R, and Ashman O, et al. Bacteriotherapy using fecal flora: toying with human motions. J Clin Gastroenterol 2004. 38: 475–483.
- McFarland LV Evidence-based review of probiotics for antibioticassociated diarrhea and Clostridium difficile infections. Anaerobe 2009 15: 274–280.
- Dethlefsen L, Relman DA Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 2011; 1: 4554–4561.
- Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, et al. Reproducible community dynamics of the gastrointestinal microbiotafollowing antibiotic perturbation. Infect Immun 2009; 77: 2367–2375.
- Endt K, Stecher B, Chaffron S, Slack E, Tchitchek N, et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog 2010; 6: e1001097.
- Croswell A, Amir E, Teggatz P, Barman M, Salzman NH Prolonged Impact of Antibiotics on Intestinal Microbial Ecology and Susceptibility to Enteric Salmonella Infection. Infect Immun 2009; 77: 2741–53.
- Finegold, S. Therapy and epidemiology of autism–clostridial spores as key elements. Medical Hypotheses 2008; 70, 508–511
- Borody TJ, Khoruts A Fecal microbiota transplantation and emergingapplications. Nat Rev Gastroenterol Hepatol 2012; 9: 88–96.
References
References
Belzung C, Leman S, Vourc'h, P Andres C, Rodent models for autism: a critical review, Drug Discov. Today Dis. Model. 2005;2: 93–101
Foley KA, MacFabe DF, Vaz A, Ossenkopp KP, Kavaliers M. Sexually dimorphic effects of prenatal exposure to propionic acid and lipopolysaccharide on social behavior in neonatal, adolescent,and adult rats: implications for autism spectrum disorders. Int J Dev Neurosci. 2014b ;39:68-78.
MacFabe, D.F. Cain, D.P. Rodriguez-Capote, K. Franklin, A.E. Hoffman, J.E. Boon, F. Taylor, A.R. Kavaliers, M. Ossenkopp, K.P. Neurobiological effects of intraventricular propionic acid in rats: possible role of short chain fatty acids on the pathogenesis and characteristics of autism spectrum disorders, Behav. Brain Res. 2007 ;176 (1): 149–169.
El-Ansary AK, Ben Bacha A, Kotb M Etiology of autistic features: the persisting neurotoxic effects of propionic acid. J Neuroinflammation. 2012; 9:74.
Xiong X, Liu D, Wang Y, Zeng T, Peng Y. Urinary 3-(3-hydroxyphenyl)-3-hydroxypropionic acid, 3-hydroxyphenylacetic acid, and 3-Hydroxyhippuric acid are elevated in children with autism spectrum disorders BioMed Res. Int. 2016 9485412, 10.1155/2016/9485412
Salminen MK, Rautelin H, Tynkkynen S, Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin. Infect. Dis; 2004. 38, 62–69.
Vibhute VM, Shelke RR, Chavan SD, Nage SP, Effect of probiotics supplementation on the performance of lactating crossbred cows. Vet. World 2011 4, 557–561.
Chaucheyras F, Durand H, Probiotics in animal nutrition and health. Benef. Microbes 2010 25, 3–9.
Preedy VR, Watson RR , Probiotics, prebiotics and synbiotics, second ed. Langford, London. 2016.
McFarland LV. Meta-analysis of probiotics for the prevention of traveler's diarrhea. Travel Med Infect Dis. 2007;2:97-105.
Hickson M. Probiotics in the prevention of antibiotic-associated diarrhoea and Clostridium difficile infection. Therap Adv Gastroenterol. 2011; 4(3): 185–197.
Alison Sinclair, , Xuanqian Xie, , Lama Saab, Nandini Dendukuri, Lactobacillus probiotics in the prevention of diarrhea associated with Clostridium difficile: a systematic review and Bayesian hierarchical meta-analysis. CMAJ Open. 2016 4(4): 706–718.
Trevor D. Lawley, Simon Clare, Alan W. Walker1., Mark D. Stares, Thomas R. Connor, Claire Raisen, David Goulding, Roland Rad, Fernanda Schreiber1, Cordelia Brandt1, Laura J. Deakin, Derek J. Pickard, Sylvia H. Duncan, Harry J. Flint, Taane G. Clark, Julian Parkhill, Gordon Dougan. Targeted Restoration of the Intestinal Microbiota with a Simple, Defined Bacteriotherapy Resolves Relapsing Clostridium difficile Disease in Mice.. PLOS pathogens, 2012 8: e1002995.
Ruiz-Larrea MB, Leal AM, Liza M, Lacort M, de Groot H. An¬tioxidant effects of estradiol and 2-hydroxyestradiol on iron-induced lipid peroxidation of rat liver microsome. Steroids.1994; 159,383
Jagota SK, Dani HMA. New colorimetric technique for the estimation of Vitamin C using Folin phenol reagent. Anal Bio¬chem.1982; 15, 178.
Beutle E, Duran O, Kelly BM Improved method for the determi¬nation of blood glutathione. J Lab Clin Med. 1963; 61, 882.
Habig WH, Pabst MJ, Jacoby WB, G. Glutathione-S-transferase, the first enzymatic step . J Biol Chem 1974; 249, 7130–9.
Ewing,W.HEdwards and Ewing's identification of Enterobacteriaceae, 4th ed. Elsevier Science Publishing Co., Inc., New York, N.Y. 1986.
Isenberg, H.D. Clinical microbiology procedures handbook. Am. Soc. Microbiol. Wash. P. 1;1994
Al-Dbass A Effect of N-Acetylcysteine in ameliorating the neurtoxic effects of propionic acid in rat pups, King Saud university journal [science], 2014 26(4), 254–260.
Allen J W, Shanker G. Aschner M. Methylmercury inhibits the in vitro uptake of the glutathione precursor, cystine, in astrocytes, but not in neurons. Brain Res. 2001a 894, 131–140.
Ares AM, Valverde S, Bernal JL, Nozal MJ, Bernal J. Extraction and determination of bioactive compounds from bee pollen. J Pharm Biomed Anal. 2018 147:110-124. 8.
Oryan A, Alemzadeh E, Moshiri A. Potential role of propolis in wound healing: Biological properties and therapeutic activities. Biomed Pharmacother. 2018 ;98:469-483. 27.
Pasupuleti VR, Sammugam L, Ramesh N, Gan SH. Honey, Propolis, and Royal Jelly: A Comprehensive Review of Their BiologicalActions and Health Benefits. Oxid Med Cell Longev. 2017:1259510.
Andrade JKS, Denadai M, de Oliveira CS, Nunes ML, Narain N. Evaluation of bioactive compounds potential and antioxidant activity of brown, green and red propolis from Brazilian northeast region. Food Res Int. 2017; 101:129-138.
Nanaware S, Shelar M, Sinnathambi A, Mahadik KR, Lohidasan S. Neuroprotective effect of Indian propolis in β-amyloid induced memory deficit: Impact on behavioral and biochemical parameters in rats. Biomed Pharmacother. 2017 ; 93:543-553. 4.
Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, et al. Probiotic yogurt improvesantioxidant status in type 2 diabetic patients.Nutrition 2012; 28(5) 539–543.
Asemi Z, Jazayeri S, Najafi M, Samimi M, Mofid V, Shidfar F, Shakeri H, Esmaillzadeh A. Effect of daily consumption of probiotic yogurt on oxidative stress in pregnantwomen: a randomized controlled clinical trial. Annals of Nutrition and Metabolism 2012; 60(1):62-68.
Zhang Y, Du R, Wang L, Zhang H. The antioxidative effects of probiotic Lactobacilluscasei Zhang on the hyperlipidemic rats. European Food Research and Technology 2010; 231(1)151-158.
Wang AN,Yi XW, Yu HF, Dong B, Qiao SY. Free radical scavenging activity ofLactobacillus fermentum in vitro and its antioxidative effect on growing-finishing pigs.Journal of Applied Microbiology 2009; 107(4)1140-1148.
Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, et al. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile associated diarrhea. J Infect Dis . 2008. 197: 435–438.
Robinson CJ, Bohannan BJ, Young VB From structure to function: the ecology of host-associated microbial communities. Microbiol Mol Biol Rev 2010 74: 453–476.
Borody TJ, Warren EF, Leis SM, Surace R, and Ashman O, et al. Bacteriotherapy using fecal flora: toying with human motions. J Clin Gastroenterol 2004. 38: 475–483.
McFarland LV Evidence-based review of probiotics for antibioticassociated diarrhea and Clostridium difficile infections. Anaerobe 2009 15: 274–280.
Dethlefsen L, Relman DA Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci 2011; 1: 4554–4561.
Antonopoulos DA, Huse SM, Morrison HG, Schmidt TM, Sogin ML, et al. Reproducible community dynamics of the gastrointestinal microbiotafollowing antibiotic perturbation. Infect Immun 2009; 77: 2367–2375.
Endt K, Stecher B, Chaffron S, Slack E, Tchitchek N, et al. The microbiota mediates pathogen clearance from the gut lumen after non-typhoidal Salmonella diarrhea. PLoS Pathog 2010; 6: e1001097.
Croswell A, Amir E, Teggatz P, Barman M, Salzman NH Prolonged Impact of Antibiotics on Intestinal Microbial Ecology and Susceptibility to Enteric Salmonella Infection. Infect Immun 2009; 77: 2741–53.
Finegold, S. Therapy and epidemiology of autism–clostridial spores as key elements. Medical Hypotheses 2008; 70, 508–511
Borody TJ, Khoruts A Fecal microbiota transplantation and emergingapplications. Nat Rev Gastroenterol Hepatol 2012; 9: 88–96.