Probiotic Lactobacillus casei strain Shirota relieves stress-associated symptoms by modulating the gut–brain interaction in human and animal models

Neurogastroenterology and Motility

Volumn 28, Issue 7, 2016, Pages 1027-1036

  Takada, M ^a   Nishida, K ^b   Kataoka Kato, A ^a   Gondo, Y ^a   Ishikawa, H ^a   Suda, K ^a   Kawai, M ^a   Hoshi, R ^a   Watanabe, O ^a   Igarashi, T ^a   Kuwano, Y ^b   Miyazaki, K ^a   Rokutan, K ^b  

^a YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

cortisol; gut brain axis; probiotics; stress; vagus

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; HYDROCORTISONE; PREBIOTIC AGENT; PROBIOTIC AGENT; YOGHURT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL STRAIN; BODY MASS; BRAIN FUNCTION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DOUBLE BLIND PROCEDURE; EXCITABILITY; FEMALE; GENERAL HEALTH QUESTIONNAIRE; GUT BRAIN INTERACTION; HUMAN; HUMAN EXPERIMENT; HYDROCORTISONE BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; INTESTINE FUNCTION; LACTOBACILLUS CASEI; LACTOBACILLUS CASEI STRAIN SHIROTA; MALE; MEDICAL STUDENT; MENTAL STRESS; MILK; NERVE CONDUCTION; NONHUMAN; NORMAL HUMAN; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUESTIONNAIRE; RAT; SENSORY NERVE; SEX RATIO; STATE TRAIT ANXIETY INVENTORY; YOUNG ADULT;

EID: 84977109319     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12804     Document Type: Article

References (40)

1. Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol 2012; 10: 735–42.
2. Rhee SH, Pothoulakis C, Mayer EA. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 2009; 6: 306–14.
3. Collins SM, Bercik P. The relationship between intestinal microbiota and the central nervous system in normal gastrointestinal function and disease. Gastroenterology 2009; 136: 2003–14.
4. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu X, Kubo C, Koga Y. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558: 263–75.
5. Tillisch K. The effects of gut microbiota on CNS function in humans. Gut Microbes 2014; 5: 404–10.
6. Benton D, Williams C, Brown A. Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur J Nutr 2007; 61: 355–61.
7. Rao AV, Bested AC, Beaulne TM, Katzman MA, Iorio C, Berardi JM, Logan AC. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog 2009; 1: 6.
8. Gleeson M, Bishop NC, Oliveira M, Tauler P. Daily probiotic's (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Exerc Metab 2011; 21: 55–64.
9. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 2011; 108: 16050–5.
10. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG. Effects of the probiotics Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179–88.
11. Messaoudi M, Violle N, Bisson JF, Desor D, Javelot H, Rougeot C. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2011; 2: 256–61.
12. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, Bisson JF, Rougeot C et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105: 755–64.
13. Kurokawa K, Tanahashi T, Murata A, Akaike Y, Katsuura S, Nishida K, Masuda K, Kuwano Y et al. Effects of chronic academic stress on mental state and expression of glucocorticoid receptor α and β isoforms in healthy Japanese medical students. Stress 2011; 14: 431–8.
14. Katsuura S, Kuwano Y, Yamagishi N, Kurokawa K, Kajita K, Akaike Y, Nishida K, Masuda K et al. MicroRNAs miR-144/144* and miR-16 in peripheral blood are potential biomarkers for naturalistic stress in healthy Japanese medical students. Neurosci Lett 2012; 516: 79–84.
15. Hughes C, Davoodi-Semiromi Y, Colee JC, Culpepper T, Dahl WJ, Mai V, Christman MC, Langkamp-Henken B. Galactooligosaccharide supplementation reduces stress-induced gastrointestinal dysfunction and days of cold or flu: a randomized, double-blind, controlled trial in healthy university students. Am J Clin Nutr 2011; 93: 1305–11.
16. Langkamp-Henken B, Rowe CC, Ford AL, Christman MC, Nieves C Jr, Khouri L, Specht GJ, Girard SA et al. Bifidobacterium bifidum R0071 results in a greater proportion of healthy days and a lower percentage of academically stressed students reporting a day of cold/flu: a randomized, double-blind, placebo-controlled study. Br J Nutr 2015; 113: 426–34.
17. Tanida M, Imanishi K, Akashi H, Kurata Y, Chonan O, Naito E, Kunihiro S, Kawai M et al. Injection of Lactobacillus casei strain Shirota affects autonomic nerve activities in a tissue-specific manner, and regulates glucose and lipid metabolism in rats. J Diabetes Investig 2014; 5: 153–61.
18. Tanida M, Shen J, Maeda K, Horii Y, Yamano T, Fukushima Y, Nagai K. High-fat diet-induced obesity is attenuated by probiotic strain Lactobacillus paracasei ST11 (NCC2461) in rats. Obes Res Clin Pract 2008; 2: 159–69.
19. Zung WW. A self-rating depression scale. Arch Gen Psychiatry 1965; 12: 63–70.
20. Fukuda K, Kobayashi S. How to use SDS. Kyoto, Japan: Sankyoubou Corp, 1973. (in Japanese).
21. Morimoto K. Lifestyle and health. Jpn J Hyg 2000; 54: 572–91.
22. Goldberg DP, Hillier VF. A scaled version of the General Health Questionnaire. Psychol Med 1979; 9: 139–45.
23. Spielberger CD, Gorsuch RL, Lushene RE. Manual for State-Trait Anxiety Inventory (Self-Evaluation Questionnaire). Palo Alto, CA: Consulting Psychologists Press, 1970.
24. Nakazato K, Mizuguchi T. How to use STAI. Kyoto, Japan: Sankyoubou Corp, 1982. (in Japanese).
25. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates, 2nd ed. New York: Academic Press, 1986.
26. Wang L, Martínez V, Larauche M, Taché Y. Proximal colon distension induces Fos expression in oxytocin-, vasopression-, CRF- and catecholamines-containing neurons in rat brain. Brain Res 2009; 1247: 79–91.
27. Chocyk A, Czyrak A, Wedzony K. Dopamine D1-like receptors agonist SKF 38393 increases cFOS expression in the paraventricular nucleus of the hypothalamus—impact of acute and chronic cocaine. J Physiol Pharmacol 2008; 59: 425–40.
28. Komaroff AL, Fagioli LR, Geiger AM, Doolittle TH, Lee J, Kornish RJ, Gleit MA, Guerriero RT. An examination of the working case definition of chronic fatigue syndrome. Am J Med 1996; 100: 56–64.
29. Wessely S, Chalder T, Hirsch S, Wallace P, Wright D. Psychological symptoms, somatic symptoms, and psychiatric disorder in chronic fatigue and chronic fatigue syndrome: a prospective study in the primary care setting. Am J Psychiatry 1996; 153: 1050–9.
30. Armario A, Marti O, Molina T, de Pablo J, Valdes M. Acute stress markers in humans: response of plasma glucose, cortisol and prolactin to two examinations differing in the anxiety they provoke. Psychoneuroendocrinology 1996; 21: 17–24.
31. Campbell J, Ehlert U. Acute psychosocial stress: does the emotional stress response correspond with physiological responses? Psychoneuroendocrinology 2012; 37: 1111–34.
32. Takai N, Yamaguchi M, Aragaki T, Eto K, Uchihashi K, Nishikawa Y. Effect of psychological stress on the salivary cortisol and amylase levels in healthy young adults. Arch Oral Biol 2004; 49: 963–8.
33. Noto Y, Sato T, Kudo M, Kurata K, Hirota K. The relationship between salivary biomarkers and state-trait anxiety inventory score under mental arithmetic stress: a pilot study. Anesth Analg 2005; 101: 1873–6.
34. Peters JH, Ritter RC, Simasko SM. Leptin and CCK selectively activate vagal afferent neurons innervating the stomach and duodenum. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1544–9.
35. Kentish SJ, O'Donnell TA, Isaacs NJ, Young RL, Li H, Harrington AM, Brierley SM, Wittert GA et al. Gastric vagal afferent modulation by leptin is influenced by food intake status. J Physiol 2013; 591: 1921–34.
36. Tanida M, Nagai K. Electrophysiological analysis of the mechanism of autonomic action by Lactobacilli. Biosci Microflora 2011; 30: 99–109.
37. Rinaman L. Visceral sensory inputs to the endocrine hypothalamus. Front Neuroendocrinol 2007; 28: 50–60.
38. Affleck VS, Coote JH, Pyner S. The projection and synaptic organization of NTS afferent connections with presympathetic neurons, GABA and nNOS neurons in the paraventricular nucleus of the hypothalamus. Neuroscience 2012; 219: 48–61.
39. Ansari WE, Oskrochi R, Haghgoo G. Are students' symptoms and health complaints associated with perceived stress at university? Perspectives from the United Kingdom and Egypt. Int J Environ Res Public Health 2014; 11: 9981–10002.
40. Tache Y, Bonaz B. Corticotropin-releasing factor receptors and stress-related alterations of gut motor function. J Clin Invest 2007; 117: 33–40.