Lactobacillus helveticus and Bifidobacterium longum taken in combination reduce the apoptosis propensity in the limbic system after myocardial infarction in a rat model
Open accessAbstract
Myocardial infarction (MI) stimulates the release of pro-inflammatory substances that induce apoptosis in the limbic system. Pro-inflammatory cytokines are considered as the root cause of apoptosis, although the mechanism is not fully explained and/or understood at this time. In addition, depression may induce gastrointestinal perturbations that maintain the elevated levels of pro-inflammatory cytokines. It has been shown that some specific probiotic formulations may reduce gastrointestinal problems induced by stress and the pro/anti-inflammatory cytokine ratio. Therefore, we hypothesised that probiotics, when given prophylactically, may diminish the apoptosis propensity in the limbic system following a MI. Male adult Sprague–Dawley rats were given probiotics (Lactobacillus helveticus and Bifidobacterium longum in combination) or placebo in their drinking-water for four consecutive weeks. A MI was then induced in the rats by occluding the left anterior coronary artery for 40 min. Rats were killed following a 72 h reperfusion period. Infarct size was not different in the two groups. Bax/Bcl-2 (pro-apoptotic/anti-apoptotic) ratio and caspase-3 (pro-apoptotic) activity were reduced in the amygdala (lateral and medial), as well as in the dentate gyrus in the probiotics group when compared with the placebo. Akt activity (anti-apoptotic) was increased in these same three regions. No significant difference was observed in Ca1 and Ca3 for the different markers measured. In conclusion, the probiotics L. helveticus and B. longum, given in combination as preventive therapy, reduced the predisposition of apoptosis found in different cerebral regions following a MI.
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In laboratory rats subjected to experimental myocardial infarction, the same probiotic combination reduced the increase in intestinal permeability and stress-induced cerebral apoptosis.
“When administered to laboratory rats subjected to experimental myocardial infarction, the same probiotic combination reduced the increase in intestinal permeability127 and stress-induced cerebral apoptosis128 found in animals that underwent infarction without probiotic pretreatment.”
From The Gut Microbiome and the Brain (2014) · cites this paper as [128]
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery
Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y., & Greenberg, M. E. (1997) · Cell · doi:10.1016/s0092-8674(00)80405-5 · Cited by 5,689 · see citing works
Depression Following Myocardial Infarction
Frasure‐Smith, N. (1993) · JAMA · doi:10.1001/jama.1993.03510150053029 · Cited by 2,028 · see citing works
Lawlor, M. A., & Alessi, D. R. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.16.2903 · Cited by 1,071 · see citing works
Yan, F., Cao, H., Cover, T. L., Whitehead, R. H., Washington, M. K., & Polk, D. B. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.11.022 · Cited by 828 · see citing works
Ways of dying: multiple pathways to apoptosisPreprint
Adams, J. M. (2003) · Genes & Development · doi:10.1101/gad.1126903 · Cited by 776 · see citing works
Lespérance, F., Frasure‐Smith, N., Talajic, M. R., & Bourassa, M. G. (2002) · Circulation · doi:10.1161/hc0902.104707 · Cited by 722 · see citing works
Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury
Vinten-Johansen, J. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.10.011 · Cited by 676 · see citing works
Depression following Myocardial Infarction
Forrester, A. W., Lipsey, J. R., Teitelbaum, M. L., DePaulo, J. R., Andrzejewski, P. L., & Robinson, R. G. (1992) · The International Journal of Psychiatry in Medicine · doi:10.2190/cj9d-32c2-8cm7-ft3d · Cited by 635 · see citing works
Psychological stress in IBD: new insights into pathogenic and therapeutic implications
Mawdsley, J. E., & Rampton, D. S. (2005) · Gut · doi:10.1136/gut.2005.064261 · Cited by 622 · see citing works
Maes, M. H. J., Kubera, M., & Leunis, J. (2008) · PubMed · Cited by 607 · see citing works
Probiotic Bacterium Prevents Cytokine-induced Apoptosis in Intestinal Epithelial Cells*
Yan, F., & Polk, D. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m207050200 · Cited by 599 · see citing works
Mechanisms of action of probiotics: Recent advances
Ng, S. C., Hart, A. L., Kamm, M. A., Stagg, A. J., & Knight, S. C. (2009) · Inflammatory Bowel Diseases · doi:10.1002/ibd.20602 · Cited by 596 · see citing works
Gareau, M. G., Jury, J., MacQueen, G., Sherman, P. M., & Perdue, M. H. (2007) · Gut · doi:10.1136/gut.2006.117176 · Cited by 472 · see citing works
Role of Stress in Functional Gastrointestinal Disorders
Mönnikes, H., Tebbe, J. J., Hildebrandt, M., Arck, P., Osmanoglou, E., Rose, M., Klapp, B., Wiedenmann, B., & Heymann-Mönnikes, I. (2001) · Digestive Diseases · doi:10.1159/000050681 · Cited by 298 · see citing works
Lammers, K. M., Brigidi, P., Vitali, B., Gionchetti, P., Rizzello, F., Caramelli, E., Matteuzzi, D., & Campieri, M. (2003) · FEMS Immunology & Medical Microbiology · doi:10.1016/s0928-8244(03)00144-5 · Cited by 282 · see citing works
Akt Is a Direct Target of the Phosphatidylinositol 3-Kinase
Datta, K., Bellacosa, A., Chan, T. O., & Tsichlis, P. N. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.48.30835 · Cited by 279 · see citing works
Neuronal death/survival signaling pathways in cerebral ischemia
Sugawara, T., Fujimura, M., Noshita, N., Kim, G. W., Saito, A., Hayashi, T., Narasimhan, P., Maier, C. M., & Chan, P. H. (2004) · NeuroRX · doi:10.1602/neurorx.1.1.17 · Cited by 270 · see citing works
Pathophysiological Mechanisms of Stress-Induced Intestina Damage
Gareau, M., Silva, M., & Perdue, M. (2008) · Current Molecular Medicine · doi:10.2174/156652408784533760 · Cited by 268 · cited 2× · see citing works
“The mechanisms are not clearly established, but it has been suggested that prolonged exposure to stress can induce low-grade inflammation, causing ultrastructural epithelial abnormalities, alter bacterial–host interactions allowing an increase in bacteria translocation((10)), which in turn affects the brain.”
BackgroundSherman, P. M., Johnson-Henry, K. C., Yeung, H. P., Ngo, P. S. C., Goulet, J., & Tompkins, T. A. (2005) · Infection and Immunity · doi:10.1128/iai.73.8.5183-5188.2005 · Cited by 246 · see citing works
Self-citationImproved myocardial ischemia/reperfusion injury in mice lacking tumor necrosis factor-α
Maekawa, N., Wada, H., Kanda, T., Niwa, T., Yamada, Y., Saito, K., Fujiwara, H., Sekikawa, K., & Seishima, M. (2002) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)01738-2 · Cited by 205 · see citing works
Acute myocardial infarction induces hypothalamic cytokine synthesis
Francis, J., Chu, Y., Johnson, A. K., Weiss, R. M., & Felder, R. B. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01072.2003 · Cited by 172 · see citing works
Diop, L., Guillou, S., & Durand, H. (2008) · Nutrition Research · doi:10.1016/j.nutres.2007.10.001 · Cited by 162 · see citing works
Antidepressants Attenuate Increased Susceptibility to Colitis in a Murine Model of Depression
Varghese, A. K., Verdu, E. F., Berčík, P., Khan, W. I., Blennerhassett, P. A., Szechtman, H., & Collins, S. M. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.02.007 · Cited by 128 · see citing works
Wallace, T. D., Bradley, S., Buckley, N. D., & Green-Johnson, J. M. (2003) · Journal of Food Protection · doi:10.4315/0362-028x-66.3.466 · Cited by 120 · see citing works
Neural regulation of the proinflammatory cytokine response to acute myocardial infarction
Francis, J., Zhang, Z., Weiss, R. M., et al. (2004) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00099.2004 · Cited by 111 · see citing works
The blood–brain barrier as a regulatory interface in the gut–brain axes
Banks, W. A. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.07.004 · Cited by 84 · see citing works
Wann, B. P., Bah, T. M., Kaloustian, S., Boucher, M., Dufort, A., Marec, N. L., Godbout, R., & Rousseau, G. (2008) · Journal of Psychopharmacology · doi:10.1177/0269881108089820 · Cited by 73 · see citing works
Self-citationDAWN, B. (2004) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2004.03.012 · Cited by 70 · see citing works
Bai, A.-P., Ouyang, Q., Xiao, X.-R., & Li, S.-F. (2006) · International Journal of Clinical Practice · doi:10.1111/j.1368-5031.2006.00833.x · Cited by 69 · see citing works
Apoptosis Detected in the Amygdala Following Myocardial Infarction in the Rat
Wann, B. P., Boucher, M., Kaloustian, S., Nim, S., Godbout, R., & Rousseau, G. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.07.018 · Cited by 60 · see citing works
Self-citationWann, B. P., Bah, T. M., Boucher, M., Courtemanche, J., Marec, N. L., Rousseau, G., & Godbout, R. (2007) · Journal of Psychiatry and Neuroscience · doi:10.1139/jpn.0702 · Cited by 60 · see citing works
Self-citationVerdu, E. F., Bercik, P., Huang, X. X., Lu, J., Al-Mutawaly, N., Sakai, H., Tompkins, T. A., Croitoru, K., Tsuchida, E., Perdue, M., et al. (2008) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90316.2008 · Cited by 57 · see citing works
Self-citationGu, Q., Yang, X. P., Bonde, P., DiPaula, A., Fox-Talbot, K., & Becker, L. C. (2006) · Journal of Cardiovascular Pharmacology · doi:10.1097/01.fjc.0000250079.46526.38 · Cited by 56 · see citing works
TNFα is required to confer protection in an in vivo model of classical ischaemic preconditioning
Deuchar, G. A., Opie, L. H., & Lecour, S. (2007) · Life Sciences · doi:10.1016/j.lfs.2007.01.040 · Cited by 48 · see citing works
Boucher, M., Wann, B. P., Kaloustian, S., et al. (2006) · APOPTOSIS · doi:10.1007/s10495-006-6313-6 · Cited by 26 · see citing works
Self-citationProtein Kinase C and Apoptosis
Reyland, M. E. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-199-4_2 · Cited by 23 · see citing works
Spacial and temporal profiles of neutrophil accumulation in the reperfused ischemic myocardium.
de Lorgeril, M., Rousseau, G., Basmadjian, A., et al. (1990) · PubMed · Cited by 22 · see citing works
Self-citationApoptosis, Cell Signaling, and Human Diseases
Srivastava, R. K. (2007) · Humana Press eBooks · doi:10.1007/978-1-59745-199-4 · Cited by 19 · see citing works
Synbiotic Therapy Improves Quality of Life and Reduces Symptoms in Pediatric Ulcerative Colitis
Haskey, N., & Dahl, W. J. (2009) · ICAN Infant Child & Adolescent Nutrition · doi:10.1177/1941406409332930 · Cited by 15 · see citing works
McVey, M. J., Perrone, M. H., & Clark, K. L. (1999) · General Pharmacology The Vascular System · doi:10.1016/s0306-3623(98)00050-0 · Cited by 8 · see citing works
Requirement for Akt-mediated survival in cell transformation by the dbl oncogene
Morley, S., Wagner, J., Kauppinen, K. P., et al. (2006) · Cellular Signalling · doi:10.1016/j.cellsig.2006.06.005 · Cited by 8 · see citing works
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Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
Messaoudi, M., Lalonde, R., Violle, N., Javelot, H., Desor, D., Nejdi, A., Bisson, J.-F., Rougeot, C., Pichelin, M., Cazaubiel, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114510004319 · Cited by 1,324 · see citing works
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Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999 · see citing works
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Gareau, M. G., Wine, E., Rodrigues, D. M., Cho, J. H., Whary, M. T., Philpott, D. J., MacQueen, G., & Sherman, P. M. (2011) · Gut · doi:10.1136/gut.2009.202515 · Cited by 909 · see citing works
“Probiotics also have extra-intestinal effects, such as prevention of myocardial infarctinduced apoptosis in the limbic region of the brain.(39) To determine the mechanism of action of microbe-induced memory deficits, the hippocampus was studied.”
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Galland, L. (2014) · Journal of Medicinal Food · doi:10.1089/jmf.2014.7000 · Cited by 648 · see citing works
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Selhub, E. M., Logan, A. C., & Bested, A. C. (2014) · Journal of Physiological Anthropology · doi:10.1186/1880-6805-33-2 · Cited by 280 · see citing works
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Li, Q., & Zhou, J.-M. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.03.013 · Cited by 253 · see citing works
Liu, J., Sun, J., Wang, F., Yu, X., Ling, Z., Li, H., Zhang, H., Jin, J., Chen, W., Pang, M., et al. (2015) · BioMed Research International · doi:10.1155/2015/412946 · Cited by 225 · see citing works
Arseneault-Bréard, J., Rondeau, I., Gilbert, K., Girard, S.-A., Tompkins, T. A., Godbout, R., & Rousseau, G. (2012) · British Journal of Nutrition · doi:10.1017/s0007114511005137 · Cited by 205 · see citing works
Self-citationRole of the intestinal microbiome, intestinal barrier and psychobiotics in depression
Trzeciak, P., & Herbet, M. (2021) · Nutrients · doi:10.3390/nu13030927 · Cited by 139 · see citing works
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Ebel, B., Lemetais, G., Beney, L., Cachon, R., Sokol, H., Langella, P., & Gervais, P. (2014) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2011.579361 · Cited by 97 · see citing works
Bested, A. C., Logan, A. C., & Selhub, E. M. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-4 · Cited by 84 · see citing works
- Authors
- Girard, S.-A., Bah, T. M., Kaloustian, S., Lada-Moldovan, L., Rondeau, I., Tompkins, T. A., Godbout, R., & Rousseau, G.
- Affiliations
- Hôpital du Sacré-Cœur de Montréal (CA)
- Lallemand (Canada) (CA)
- Corresponding author
- Rousseau, Guy
- Venue
- British Journal of Nutrition
- Publisher
- Cambridge University Press (CUP)
- Published
- 2009-06-29
- Volume
- 102
- Issue
- 10
- Pages
- 1420-1425
- ISSN
- 0007-1145 (ISSN-L)
- 1475-2662
- OpenAlex
- W2061164668
- Cited by
- 70
- References
- 42
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 9 · 2021: 5 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 2 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 9 · 2012: 4
- FWCI
- 7.89
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- British Journal Of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Libraries (submittedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada (250234-07)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- Lactobacillus helveticus, Bifidobacterium longum, probiotics, myocardial infarction, apoptosis, limbic system, amygdala, dentate gyrus, Bax/Bcl-2 ratio, caspase-3, Akt, inflammatory cytokines, depression, ischemia-reperfusion injury, gut-brain axis
- MeSH terms
- Animals, Bifidobacterium, Diet, Enzyme Activation, Limbic System, Male, Myocardial Infarction, Nutritional Physiological Phenomena, Rats, Sprague-Dawley, Apoptosis, Proto-Oncogene Proteins c-bcl-2, Probiotics, bcl-2-Associated X Protein, Rats, Lactobacillus helveticus, Caspase 3
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