Administration of non-Absorbable antibiotics to pregnant mice to perturb the maternal gut microbiota is associated with alterations in offspring behavior

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Tochitani, Shiro ^a,b   Ikeno, Takahiro ^a   Ito, Tatsuhito ^a   Sakurai, Asuka ^a   Yamauchi, Tomoki ^a   Matsuzaki, Hideo ^a,b  

^a UNIVERSITY OF FUKUI   (Japan)

^b HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT;

ANIMAL; ANIMAL BEHAVIOR; DRUG EFFECTS; FECES; FEMALE; GASTROINTESTINAL ABSORPTION; INTESTINE FLORA; MICROBIOLOGY; MOTOR ACTIVITY; MOUSE; NEWBORN; PREGNANCY;

ANIMALS; ANIMALS, NEWBORN; ANTI-BACTERIAL AGENTS; BEHAVIOR, ANIMAL; FECES; FEMALE; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL MICROBIOME; MICE; MOTOR ACTIVITY; PREGNANCY;

EID: 84958211771     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0138293     Document Type: Article

References (71)

1. Sekirov I, Russell SL, Antunes LC, Finlay BB. Gut microbiota in health and disease. Physiological reviews. 2010; 90(3):859-904. Epub 2010/07/29. doi: 10.1152/physrev.00045.2009 .
2. Clemente JC, Ursell LK, Parfrey LW, Knight R. The impact of the gut microbiota on human health: An integrative view. Cell. 2012; 148(6):1258-70. Epub 2012/03/20. doi: 10.1016/j.cell.2012.01.035 .
3. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-Adrenal system for stress response in mice. The Journal of physiology. 2004; 558(Pt 1):263-75. Epub 2004/05/11. doi: 10.1113/jphysiol.2004.063388 ; PubMed Central PMCID: PMC1664925.
4. Verdu EF, Bercik P, Verma-Gandhu M, Huang XX, Blennerhassett P, JacksonW, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut. 2006; 55(2):182-90. Epub 2005/08/18. doi: 10.1136/gut.2005.066100 ; PubMed Central PMCID: PMC1856497.
5. Bercik P, Denou E, Collins J, JacksonW, Lu J, Jury J, et al. The intestinal microbiota affect central levels of brain-derived neurotropic factor and behavior in mice. Gastroenterology. 2011; 141(2):599-609, e1-3. Epub 2011/06/21. doi: 10.1053/j.gastro.2011.04.052 .
6. Cryan JF, Dinan TG. Mind-Altering microorganisms: The impact of the gut microbiota on brain and behaviour. Nature reviews Neuroscience. 2012; 13(10):701-12. Epub 2012/09/13. doi: 10.1038/nrn3346 .
7. Collins SM, Kassam Z, Bercik P. The adoptive transfer of behavioral phenotype via the intestinal microbiota: experimental evidence and clinical implications. Current opinion in microbiology. 2013; 16 (3):240-5. Epub 2013/07/13. doi: 10.1016/j.mib.2013.06.004 .
8. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013; 155 (7):1451-63. Epub 2013/12/10. doi: 10.1016/j.cell.2013.11.024 ; PubMed Central PMCID: PMC3897394.
9. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(7):3047-52. Epub 2011/02/02. doi: 10.1073/pnas.1010529108 ; PubMed Central PMCID: PMC3041077.
10. Desbonnet L, Clarke G, Shanahan F, Dinan TG, Cryan JF. Microbiota is essential for social development in the mouse. Molecular psychiatry. 2014; 19(2):146-8. Epub 2013/05/22. doi: 10.1038/mp.2013. 65 ; PubMed Central PMCID: PMC3903109.
11. Desbonnet L, Clarke G, Traplin A, O'Sullivan O, Crispie F, Moloney RD, et al. Gut microbiota depletion from early adolescence in mice: Implications for brain and behaviour. Brain, behavior, and immunity. 2015. Epub 2015/04/14. doi: 10.1016/j.bbi.2015.04.004 .
12. Braniste V, Al-Asmakh M, Kowal C, Anuar F, Abbaspour A, Toth M, et al. The gut microbiota influences blood-brain barrier permeability in mice. Science translational medicine. 2014; 6(263):263ra158. Epub 2014/11/21. doi: 10.1126/scitranslmed.3009759 ; PubMed Central PMCID: PMC4396848.
13. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004; 118(2):229-41. Epub 2004/07/21. doi: 10.1016/j.cell.2004.07.002 .
14. Zhu Q, Zou L, Jagavelu K, Simonetto DA, Huebert RC, Jiang ZD, et al. Intestinal decontamination inhibits TLR4 dependent fibronectin-mediated cross-Talk between stellate cells and endothelial cells in liver fibrosis in mice. Journal of hepatology. 2012; 56(4):893-9. Epub 2011/12/17. doi: 10.1016/j.jhep.2011. 11.013
15. Ghosh SS, Bie J, Wang J, Ghosh S. Oral supplementation with non-Absorbable antibiotics or curcumin attenuates western diet-induced atherosclerosis and glucose intolerance in LDLR-/-mice-role of intestinal permeability and macrophage activation. PloS one. 2014; 9(9):e108577. Epub 2014/09/25. doi: 10.1371/journal.pone.0108577 ; PubMed Central PMCID: PMC4177397.
16. Fombonne E. Epidemiology of pervasive developmental disorders. Pediatric research. 2009; 65 (6):591-8. Epub 2009/02/17. doi: 10.1203/PDR.0b013e31819e7203 .
17. Jacquemont S, Coe BP, Hersch M, Duyzend MH, Krumm N, Bergmann S, et al. A higher mutational burden in females supports a "female protective model" in neurodevelopmental disorders. American journal of human genetics. 2014; 94(3):415-25. Epub 2014/03/04. doi: 10.1016/j.ajhg.2014.02.001 ; PubMed Central PMCID: PMC3951938.
18. Silverman JL, Oliver CF, Karras MN, Gastrell PT, Crawley JN. AMPAKINE enhancement of social interaction in the BTBR mouse model of autism. Neuropharmacology. 2013; 64:268-82. Epub 2012/07/18. doi: 10.1016/j.neuropharm.2012.07.013 ; PubMed Central PMCID: PMC3445667.
19. Takahashi S, Tomita J, Nishioka K, Hisada T, Nishijima M. Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing. PloS one. 2014; 9(8):e105592. Epub 2014/08/22. doi: 10.1371/journal.pone.0105592 ; PubMed Central PMCID: PMC4140814.
20. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature. 2013; 499(7456):97-101. Epub 2013/06/28. doi: 10.1038/nature12347 .
21. Nagashima K, Hisada T, Sato M, Mochizuki J. Application of new primer-enzyme combinations to terminal restriction fragment length polymorphism profiling of bacterial populations in human feces. Applied and environmental microbiology. 2003; 69(2):1251-62. Epub 2003/02/07. ; PubMed Central PMCID: PMC143637.
22. Imaeda H, Fujimoto T, Takahashi K, Kasumi E, Fujiyama Y, Andoh A. Terminal-restriction fragment length polymorphism (T-RFLP) analysis for changes in the gut microbiota profiles of indomethacin-And rebamipide-Treated mice. Digestion. 2012; 86(3):250-7. Epub 2012/09/12. doi: 10.1159/000341508 .
23. Aomatsu T, Imaeda H, Fujimoto T, Takahashi K, Yoden A, Tamai H, et al. Terminal restriction fragment length polymorphism analysis of the gut microbiota profiles of pediatric patients with inflammatory bowel disease. Digestion. 2012; 86(2):129-35. Epub 2012/08/01. doi: 10.1159/000339777 .
24. Nagashima K, Mochizuki J, Takayoshi H, Suzuki S, Shimomura K. Phylogenetic analysis of 16S ribosomal RNA gene sequences from human fecal microbiota and improved utility of terminal restriction fragment length polymorphism profiling. Bioscience Microflora. 2006; 25(3):99-107.
25. Fujimoto T, Imaeda H, Takahashi K, Kasumi E, Bamba S, Fujiyama Y, et al. Decreased abundance of Faecalibacterium prausnitzii in the gut microbiota of Crohn's disease. Journal of gastroenterology and hepatology. 2013; 28(4):613-9. Epub 2012/12/12. doi: 10.1111/jgh.12073 .
26. Shiozaki A, Yoneda S, Yoneda N, Yonezawa R, Matsubayashi T, Seo G, et al. Intestinal microbiota is different in women with preterm birth: results from terminal restriction fragment length polymorphism analysis. PloS one. 2014; 9(11):e111374. Epub 2014/11/06. doi: 10.1371/journal.pone.0111374 ; PubMed Central PMCID: PMC4221021.
27. Tochitani S, Hayashizaki Y. Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation. Biochemical and biophysical research communications. 2008; 372(4):691-6. Epub 2008/06/10. doi: 10.1016/j.bbrc.2008.05.127 .
28. Gotz M, Huttner WB. The cell biology of neurogenesis. Nature reviews Molecular cell biology. 2005; 6 (10):777-88. Epub 2005/11/30. doi: 10.1038/nrm1739 .
29. Tochitani S, Sakata-Haga H, Fukui Y. Embryonic exposure to ethanol disturbs regulation of mitotic spindle orientation via GABA(A) receptors in neural progenitors in ventricular zone of developing neocortex. Neuroscience letters. 2010; 472(2):128-32. Epub 2010/02/09. doi: 10.1016/j.neulet.2010.01. 071 .
30. Crusio WE. Genetic dissection of mouse exploratory behaviour. Behavioural brain research. 2001; 125 (1-2):127-32. Epub 2001/10/30. .
31. Sampson TR, Mazmanian SK. Control of brain development, function, and behavior by the microbiome. Cell host & microbe. 2015; 17(5):565-76. Epub 2015/05/15. doi: 10.1016/j.chom.2015.04.011 ; PubMed Central PMCID: PMC4442490.
32. Desbonnet L, Clarke G, Traplin A, O'Sullivan O, Crispie F, Moloney RD, et al. Gut microbiota depletion from early adolescence in mice: Implications for brain and behaviour. Brain, behavior, and immunity. 2015; 48:165-73. Epub 2015/04/14. doi: 10.1016/j.bbi.2015.04.004 .
33. De Palma G, Blennerhassett P, Lu J, Deng Y, Park AJ, Green W, et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nature communications. 2015; 6:7735. Epub 2015/07/29. doi: 10.1038/ncomms8735 .
34. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. Human genetics shape the gut microbiome. Cell. 2014; 159(4):789-99. Epub 2014/11/25. doi: 10.1016/j.cell.2014.09.053 ; PubMed Central PMCID: PMC4255478.
35. Wang T, Hu X, Liang S, Li W, Wu X, Wang L, et al. Lactobacillus fermentum NS9 restores the antibiotic induced physiological and psychological abnormalities in rats. Beneficial microbes. 2015:1-11. Epub 2015/04/15. doi: 10.3920/BM2014.0177 .
36. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D, Ventura M. Bacteria as vitamin suppliers to their host: A gut microbiota perspective. Current opinion in biotechnology. 2013; 24(2):160-8. Epub 2012/09/04. doi: 10.1016/j.copbio.2012.08.005 .
37. Sharon G, Garg N, Debelius J, Knight R, Dorrestein PC, Mazmanian SK. Specialized metabolites from the microbiome in health and disease. Cell metabolism. 2014; 20(5):719-30. Epub 2014/12/03. doi: 10. 1016/j.cmet.2014.10.016 ; PubMed Central PMCID: PMC4337795.
38. Brown AS. The environment and susceptibility to schizophrenia. Progress in neurobiology. 2011; 93 (1):23-58. Epub 2010/10/20. doi: 10.1016/j.pneurobio.2010.09.003 ; PubMed Central PMCID: PMC3521525.
39. Bhatia HS, Agrawal R, Sharma S, Huo YX, Ying Z, Gomez-Pinilla F. Omega-3 fatty acid deficiency during brain maturation reduces neuronal and behavioral plasticity in adulthood. PloS one. 2011; 6(12): e28451. Epub 2011/12/14. doi: 10.1371/journal.pone.0028451 ; PubMed Central PMCID: PMC3233581.
40. Jacka FN, Ystrom E, Brantsaeter AL, Karevold E, Roth C, Haugen M, et al. Maternal and early postnatal nutrition and mental health of offspring by age 5 years: A prospective cohort study. Journal of the American Academy of Child and Adolescent Psychiatry. 2013; 52(10):1038-47. Epub 2013/10/01. doi: 10. 1016/j.jaac.2013.07.002 .
41. Delahaye F, Breton C, Risold PY, Enache M, Dutriez-Casteloot I, Laborie C, et al. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2008; 149(2):470-5. Epub 2007/11/17. doi: 10.1210/en.2007-1263 .
42. Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biology of reproduction. 2003; 68(2):390-400. Epub 2003/01/21. .
43. Vieau D, Sebaai N, Leonhardt M, Dutriez-Casteloot I, Molendi-Coste O, Laborie C, et al. HPA axis programming by maternal undernutrition in the male rat offspring. Psychoneuroendocrinology. 2007; 32 Suppl 1:S16-20. Epub 2007/07/24. doi: 10.1016/j.psyneuen.2007.03.014 .
44. Wattez JS, Delahaye F, Barella LF, Dickes-Coopman A, Montel V, Breton C, et al. Short-And long-Term effects of maternal perinatal undernutrition are lowered by cross-fostering during lactation in the male rat. Journal of developmental origins of health and disease. 2014; 5(2):109-20. Epub 2014/05/23. doi: 10.1017/S2040174413000548 .
45. Prado EL, Dewey KG. Nutrition and brain development in early life. Nutrition reviews. 2014; 72(4):267-84Epub 2014/04/02. doi: 10.1111/nure.12102 .
46. Allen-Blevins CR, Sela DA, Hinde K. Milk Bioactives May Manipulate Microbes to Mediate Parent-Offspring Conflict. Evolution, medicine, and public health. 2015. Epub 2015/04/04. doi: 10.1093/emph/eov007 .
47. Hinde K, Lewis ZT. MICROBIOTA. Mother's littlest helpers. Science. 2015; 348(6242):1427-8. Epub 2015/06/27. doi: 10.1126/science.aac7436 .
48. Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA. Development of the preterm infant gut microbiome: A research priority. Microbiome. 2014; 2:38. Epub 2014/10/22. doi: 10.1186/2049-2618-2-38 ; PubMed Central PMCID: PMC4203464.
49. Mikami K, Kimura M, Takahashi H. Influence of maternal bifidobacteria on the development of gut bifidobacteria in infants. Pharmaceuticals. 2012; 5(6):629-42. Epub 2012/01/01. doi: 10.3390/ph5060629 ; PubMed Central PMCID: PMC3763658.
50. Voreades N, Kozil A, Weir TL. Diet and the development of the human intestinal microbiome. Frontiers in microbiology. 2014; 5:494. Epub 2014/10/09. doi: 10.3389/fmicb.2014.00494 ; PubMed Central PMCID: PMC4170138.
51. Borre YE, O'Keeffe GW, Clarke G, Stanton C, Dinan TG, Cryan JF. Microbiota and neurodevelopmental windows: implications for brain disorders. Trends in molecular medicine. 2014; 20(9):509-18. Epub 2014/06/25. doi: 10.1016/j.molmed.2014.05.002 .
52. Borre YE, Moloney RD, Clarke G, Dinan TG, Cryan JF. The impact of microbiota on brain and behavior: mechanisms & therapeutic potential. Advances in experimental medicine and biology. 2014; 817:373-403. Epub 2014/07/06. doi: 10.1007/978-1-4939-0897-4-17 .
53. Jasarevic E, Rodgers AB, Bale TL. A novel role for maternal stress and microbial transmission in early life programming and neurodevelopment. Neurobiology of stress. 2015; 1:81-8. Epub 2014/12/23. doi: 10.1016/j.ynstr.2014.10.005 ; PubMed Central PMCID: PMC4267059.
54. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, et al. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-Adrenal responses to stress. Science. 1997; 277 (5332):1659-62. Epub 1997/09/12. .
55. Cicchetti D, Toth SL. Child maltreatment. Annual review of clinical psychology. 2005; 1:409-38. Epub 2007/08/25. doi: 10.1146/annurev.clinpsy.1.102803.144029 .
56. Toth SL, Gravener-Davis JA, Guild DJ, Cicchetti D. Relational interventions for child maltreatment: past, present, and future perspectives. Development and psychopathology. 2013; 25(4 Pt 2):1601-17. Epub 2013/12/18. doi: 10.1017/S0954579413000795 ; PubMed Central PMCID: PMC4063316.
57. Ivy AS, Rex CS, Chen Y, Dube C, Maras PM, Grigoriadis DE, et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. The Journal of neuroscience: The official journal of the Society for Neuroscience. 2010; 30(39):13005-15 PubMed Central PMCID: PMC2991143, Epub 2010/10/01. doi: 10.1523/JNEUROSCI.1784-10.2010 ; PubMed Central PMCID: PMC2991143.
58. Blaze J, Scheuing L, Roth TL. Differential methylation of genes in the medial prefrontal cortex of developing and adult rats following exposure to maltreatment or nurturing care during infancy. Developmental neuroscience. 2013; 35(4):306-16. Epub 2013/06/12. doi: 10.1159/000350716 ; PubMed Central PMCID: PMC3847900.
59. Trujillo V, Durando PE, Suarez MM. Maternal separation in early life modifies anxious behavior and Fos and glucocorticoid receptor expression in limbic neurons after chronic stress in rats: effects of tianeptine. Stress. 2015:1-31. Epub 2015/10/11. doi: 10.3109/10253890.2015.1105958 .
60. Tousen Y, Abe F, Ishida T, Uehara M, Ishimi Y. Resistant starch promotes equol production and inhibits tibial bone loss in ovariectomized mice treated with daidzein. Metabolism: clinical and experimental. 2011; 60(10):1425-32. Epub 2011/05/10. doi: 10.1016/j.metabol.2011.02.009 .
61. Yoda K, He F, Miyazawa K, Kawase M, Kubota A, Hiramatsu M. Orally administered heat-killed Lactobacillus gasseri TMC0356 alters respiratory immune responses and intestinal microbiota of dietinduced obese mice. Journal of applied microbiology. 2012; 113(1):155-62. Epub 2012/04/24. doi: 10. 1111/j.1365-2672.2012.05316.x .
62. Tanigawa T, Watanabe T, Otani K, Nadatani Y, Ohkawa F, Sogawa M, et al. Rebamipide inhibits indomethacin-induced small intestinal injury: possible involvement of intestinal microbiota modulation by upregulation of alpha-defensin 5. European journal of pharmacology. 2013; 704(1-3):64-9. Epub 2013/02/23. doi: 10.1016/j.ejphar.2013.02.010 .
63. Ishikawa H, Takaki A, Tsuzaki R, Yasunaka T, Koike K, Shimomura Y, et al. L-carnitine prevents progression of non-Alcoholic steatohepatitis in a mouse model with upregulation of mitochondrial pathway. PloS one. 2014; 9(7):e100627. Epub 2014/07/02. doi: 10.1371/journal.pone.0100627 ; PubMed Central PMCID: PMC4077577.
64. Unno T, Hisada T, Takahashi S. Hesperetin Modifies the Composition of Fecal Microbiota and Increases Cecal Levels of Short-Chain Fatty Acids in Rats. Journal of agricultural and food chemistry. 2015; 63(36):7952-7. Epub 2015/08/27. doi: 10.1021/acs.jafc.5b02649 .
65. Kohata Y, Nakahara K, Tanigawa T, Yamagami H, Shiba M, Watanabe T, et al. Rebamipide Alters the Esophageal Microbiome and Reduces the Incidence of Barrett's Esophagus in a Rat Model. Digestive diseases and sciences. 2015; 60(9):2654-61. Epub 2015/04/12. doi: 10.1007/s10620-015-3662-4 .
66. Miyazawa K, Yoda K, Kawase M, Harata G, He F. Influence of orally administered Lactobacillus GG on respiratory immune response in a murine model of diet-induced obesity. Microbiology and immunology. 2015; 59(2):99-103. Epub 2015/02/04. doi: 10.1111/1348-0421.12226 .
67. Oda Y, Ueda F, Kamei A, Kakinuma C, Abe K. Biochemical investigation and gene expression analysis of the immunostimulatory functions of an edible Salacia extract in rat small intestine. Biofactors. 2011; 37(1):31-9. doi: 10.1002/biof.132
68. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery. Genome biology. 2011; 12(6):R60. doi: 10.1186/gb-2011-12-6-r60
69. McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS computational biology. 2014; 10(4):e1003531. Epub 2014/04/05. doi: 10.1371/journal.pcbi.1003531 ; PubMed Central PMCID: PMC3974642.
70. Lopatina O, Yoshihara T, Nishimura T, Zhong J, Akther S, Fakhrul AA, et al. Anxiety-And depressionlike behavior in mice lacking the CD157/BST1 gene, a risk factor for Parkinson's disease. Frontiers in behavioral neuroscience. 2014; 8:133. Epub 2014/05/06. doi: 10.3389/fnbeh.2014.00133 ; PubMed Central PMCID: PMC4001052.
71. Crawley JN. Behavioral phenotyping strategies for mutant mice. Neuron. 2008; 57(6):809-18. Epub 2008/03/28. doi: 10.1016/j.neuron.2008.03.001