Friends with Social Benefits: Host-microbe Interactions As a Driver of Brain Evolution and Development?

Overview

Journal Front Cell Infect Microbiol

Specialties Cell Biology
Infectious Diseases
Microbiology

Date 2014 Nov 18

PMID 25401092

Citations 52

Authors

Roman M Stilling

Seth R Bordenstein

Timothy G Dinan

John F Cryan

Affiliations

Soon will be listed here.

Abstract

The tight association of the human body with trillions of colonizing microbes that we observe today is the result of a long evolutionary history. Only very recently have we started to understand how this symbiosis also affects brain function and behavior. In this hypothesis and theory article, we propose how host-microbe associations potentially influenced mammalian brain evolution and development. In particular, we explore the integration of human brain development with evolution, symbiosis, and RNA biology, which together represent a "social triangle" that drives human social behavior and cognition. We argue that, in order to understand how inter-kingdom communication can affect brain adaptation and plasticity, it is inevitable to consider epigenetic mechanisms as important mediators of genome-microbiome interactions on an individual as well as a transgenerational time scale. Finally, we unite these interpretations with the hologenome theory of evolution. Taken together, we propose a tighter integration of neuroscience fields with host-associated microbiology by taking an evolutionary perspective.

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References

Graff J, Tsai L . The potential of HDAC inhibitors as cognitive enhancers. Annu Rev Pharmacol Toxicol. 2013; 53:311-30. DOI: 10.1146/annurev-pharmtox-011112-140216. View

Furusawa Y, Obata Y, Fukuda S, Endo T, Nakato G, Takahashi D . Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature. 2013; 504(7480):446-50. DOI: 10.1038/nature12721. View

Fischer A . Targeting histone-modifications in Alzheimer's disease. What is the evidence that this is a promising therapeutic avenue?. Neuropharmacology. 2014; 80:95-102. DOI: 10.1016/j.neuropharm.2014.01.038. View

Selkrig J, Wong P, Zhang X, Pettersson S . Metabolic tinkering by the gut microbiome: Implications for brain development and function. Gut Microbes. 2014; 5(3):369-80. PMC: 4153776. DOI: 10.4161/gmic.28681. View

OMahony S, Marchesi J, Scully P, Codling C, Ceolho A, Quigley E . Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry. 2008; 65(3):263-7. DOI: 10.1016/j.biopsych.2008.06.026. View

Govindarajan N, Agis-Balboa R, Walter J, Sananbenesi F, Fischer A . Sodium butyrate improves memory function in an Alzheimer's disease mouse model when administered at an advanced stage of disease progression. J Alzheimers Dis. 2011; 26(1):187-97. DOI: 10.3233/JAD-2011-110080. View

Badyaev A, Uller T . Parental effects in ecology and evolution: mechanisms, processes and implications. Philos Trans R Soc Lond B Biol Sci. 2009; 364(1520):1169-77. PMC: 2666689. DOI: 10.1098/rstb.2008.0302. View

Virgin H . The virome in mammalian physiology and disease. Cell. 2014; 157(1):142-50. PMC: 3977141. DOI: 10.1016/j.cell.2014.02.032. View

Schellekens H, Clarke G, Jeffery I, Dinan T, Cryan J . Dynamic 5-HT2C receptor editing in a mouse model of obesity. PLoS One. 2012; 7(3):e32266. PMC: 3308946. DOI: 10.1371/journal.pone.0032266. View

10.

Kovacs A, Ben-Jacob N, Tayem H, Halperin E, Iraqi F, Gophna U . Genotype is a stronger determinant than sex of the mouse gut microbiota. Microb Ecol. 2010; 61(2):423-8. DOI: 10.1007/s00248-010-9787-2. View

11.

Cryan J, OMahony S . The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011; 23(3):187-92. DOI: 10.1111/j.1365-2982.2010.01664.x. View

12.

Crumeyrolle-Arias M, Jaglin M, Bruneau A, Vancassel S, Cardona A, Dauge V . Absence of the gut microbiota enhances anxiety-like behavior and neuroendocrine response to acute stress in rats. Psychoneuroendocrinology. 2014; 42:207-17. DOI: 10.1016/j.psyneuen.2014.01.014. View

13.

Benson A, Kelly S, Legge R, Ma F, Low S, Kim J . Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc Natl Acad Sci U S A. 2010; 107(44):18933-8. PMC: 2973891. DOI: 10.1073/pnas.1007028107. View

14.

Marazzi I, Ho J, Kim J, Manicassamy B, Dewell S, Albrecht R . Suppression of the antiviral response by an influenza histone mimic. Nature. 2012; 483(7390):428-33. PMC: 3598589. DOI: 10.1038/nature10892. View

15.

Flegr J . Influence of latent Toxoplasma infection on human personality, physiology and morphology: pros and cons of the Toxoplasma-human model in studying the manipulation hypothesis. J Exp Biol. 2012; 216(Pt 1):127-33. DOI: 10.1242/jeb.073635. View

16.

Bailey M, Dowd S, Galley J, Hufnagle A, Allen R, Lyte M . Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2010; 25(3):397-407. PMC: 3039072. DOI: 10.1016/j.bbi.2010.10.023. View

17.

Dale C, Moran N . Molecular interactions between bacterial symbionts and their hosts. Cell. 2006; 126(3):453-65. DOI: 10.1016/j.cell.2006.07.014. View

18.

Meyer K, Saletore Y, Zumbo P, Elemento O, Mason C, Jaffrey S . Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons. Cell. 2012; 149(7):1635-46. PMC: 3383396. DOI: 10.1016/j.cell.2012.05.003. View

19.

Igaz L, Bekinschtein P, Vianna M, Izquierdo I, Medina J . Gene expression during memory formation. Neurotox Res. 2004; 6(3):189-204. DOI: 10.1007/BF03033221. View

20.

Williams A, Dunbar R . Big brains, meat, tuberculosis and the nicotinamide switches: co-evolutionary relationships with modern repercussions on longevity and disease?. Med Hypotheses. 2014; 83(1):79-87. DOI: 10.1016/j.mehy.2014.04.003. View