Adapting to environmental stresses: The role of the microbiota in controlling innate immunity and behavioral responses

Immunological Reviews

Volumn 245, Issue 1, 2012, Pages 250-264

  Fagundes, Caio T ^a   Amaral, Flávio A ^a   Teixeira, Antônio L ^a   Souza, Danielle G ^a   Teixeira, Mauro M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Behavior; Germ free mice; Inflammation; Microbiota; Pain; Stress

Indexed keywords

ANTIBIOTIC AGENT; BCG VACCINE; BRAIN DERIVED NEUROTROPHIC FACTOR; CARRAGEENAN; CPG DNA; CPG OLIGODEOXYNUCLEOTIDE; CXCL1 CHEMOKINE; CYTOKINE; DOPAMINE; GLUCOCORTICOID; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; INTERLEUKIN 1BETA; LIPOCORTIN 1; LIPOPOLYSACCHARIDE; LIPOTEICHOIC ACID; LIPOXIN A; LIPOXYGENASE INHIBITOR; MESSENGER RNA; NORADRENALIN; PROBIOTIC AGENT; PROSTAGLANDIN E2; SEROTONIN; SHORT CHAIN FATTY ACID; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ABDOMINAL PAIN; ADAPTIVE IMMUNITY; ALLODYNIA; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC THERAPY; ANTIINFLAMMATORY ACTIVITY; ANXIETY DISORDER; ATTENUATION; BACTERIAL COLONIZATION; BACTEROIDES; BEHAVIOR CHANGE; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM; CLOSTRIDIUM; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG EFFICACY; DRUG MEGADOSE; ECOSYSTEM RESILIENCE; ENTERITIS; ENVIRONMENTAL STRESS; GENE EXPRESSION; GERMFREE ANIMAL; HELP SEEKING BEHAVIOR; HISTOPATHOLOGY; HOST; HOST PATHOGEN INTERACTION; HUMAN; HYPERALGESIA; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFECTION; INFLAMMATION; INNATE IMMUNITY; INTESTINE FLORA; INTESTINE ISCHEMIA; KLEBSIELLA PNEUMONIAE; KLEBSIELLA PNEUMONIAE INFECTION; LACTOBACILLUS PARACASEI; LEUKOCYTE; LEUKOCYTE MOTILITY; LUNG INFECTION; MACROPHAGE; MEDIATOR; MICROFLORA; NEUROTRANSMISSION; NEUTROPHIL; NEUTROPHIL COUNT; NOCICEPTION; NONHUMAN; PAIN; PAIN THRESHOLD; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; SYNAPTOGENESIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; T LYMPHOCYTE; TISSUE INJURY; VISCERAL PAIN;

ADAPTATION, BIOLOGICAL; ANIMALS; BACTERIAL INFECTIONS; BEHAVIOR; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; NOCICEPTORS; STRESS, PHYSIOLOGICAL;

EID: 83655193474     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2011.01077.x     Document Type: Review

References (122)

1. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007;449:819-826.
2. Adlerberth I, Wold AE. Establishment of the gut microbiota in Western infants. Acta Paediatr 2009;98:229-238.
3. Eckburg PB, et al. Diversity of the human intestinal microbial flora. Science 2005;308:1635-1638.
4. Gill SR, et al. Metagenomic analysis of the human distal gut microbiome. Science 2006;312:1355-1359.
5. Momose Y, Hirayama K, Itoh K. Competition for proline between indigenous Escherichia coli and E. coli O157:H7 in gnotobiotic mice associated with infant intestinal microbiota and its contribution to the colonization resistance against E. coli O157:H7. Antonie Van Leeuwenhoek 2008;94:165-171.
6. Servin AL, Coconnier MH. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract Res Clin Gastroenterol 2003;17:741-754.
7. Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 2004;28:405-440.
8. Czerucka D, Roux I, Rampal P. Saccharomyces boulardii inhibits secretagogue-mediated adenosine 3′, 5′-cyclic monophosphate induction in intestinal cells. Gastroenterology 1994;106:65-72.
9. Brandao RL, et al. Intracellular signal triggered by cholera toxin in Saccharomyces boulardii and Saccharomyces cerevisiae. Appl Environ Microbiol 1998;64:564-568.
10. Sonnenburg JL, et al. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 2005;307:1955-1959.
11. Qin J, et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 2010;464:59-65.
12. Gustafsson BE. Vitamin K deficiency in germfree rats. Ann NY Acad Sci 1959;78:166-174.
13. Abrams GD, Bauer H, Sprinz H. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab Invest 1963;12:355-364.
14. Smith K, McCoy KD, Macpherson AJ. Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota. Semin Immunol 2007;19:59-69.
15. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 2008;105:20858-20863.
16. Hooper LV, Macpherson AJ. Immune adaptations that maintain homeostasis with the intestinal microbiota. Nat Rev Immunol 2010;10:159-169.
17. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009;9:313-323.
18. Lee YK, Mazmanian SK. Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 2010;330:1768-1773.
19. Medzhitov R. Origin and physiological roles of inflammation. Nature 2008;454:428-435.
20. Sudo N, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004;558:263-275.
21. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011;23:187-192.
22. Starling JR, Balish E. Lysosomal enzyme activity in pulmonary alveolar macrophages from conventional, germfree, monoassociated, and conventionalized rats. J Reticuloendothel Soc 1981;30:497-505.
23. Mitsuyama M, Ohara R, Amako K, Nomoto K, Yokokura T. Ontogeny of macrophage function to release superoxide anion in conventional and germfree mice. Infect Immun 1986;52:236-239.
24. Ohkubo T, Tsuda M, Tamura M, Yamamura M. Impaired superoxide production in peripheral blood neutrophils of germ-free rats. Scand J Immunol 1990;32:727-729.
25. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 2010;16:228-231.
26. Souza DG, et al. The essential role of the intestinal microbiota in facilitating acute inflammatory responses. J Immunol 2004;173:4137-4146.
27. Granger DN. Ischemia-reperfusion: mechanisms of microvascular dysfunction and the influence of risk factors for cardiovascular disease. Microcirculation 1999;6:167-178.
28. Goldberg M, Fine J. Traumatic Shock. Xi. Intestinal Absorption in Hemorrhagic Shock. J Clin Invest 1945;24:445-450.
29. Grotz MR, Ding J, Guo W, Huang Q, Deitch EA. Comparison of plasma cytokine levels in rats subjected to superior mesenteric artery occlusion or hemorrhagic shock. Shock 1995;3:362-368.
30. Turnage RH, Guice KS, Oldham KT. Endotoxemia and remote organ injury following intestinal reperfusion. J Surg Res 1994;56:571-578.
31. Swank GM, Deitch EA. Role of the gut in multiple organ failure: bacterial translocation and permeability changes. World J Surg 1996;20:411-417.
32. Cicalese L, Billiar TR, Rao AS, Bauer AJ. Interaction between ischemia/reperfusion-induced leukocyte emigration and translocating bacterial enterotoxins on enteric muscle function. Transplant Proc 1997;29:1815.
33. Cicalese L, Yacoub W, Rogers J, Fung JJ, Rao AS, Starzl TE. Translocation of bacteria from the GI tract: protection afforded by lisofylline. Transplant Proc 1999;31:575-576.
34. Nezu Y, Tagawa M, Sakaue Y, Hara Y, Tsuchida S, Ogawa R. Kinetics of endotoxin concentration and tumor necrosis factor-alpha, interleukin-1beta, and interleukin-6 activities in the systemic and portal circulation during small intestinal ischemia and reperfusion in dogs. Am J Vet Res 2002;63:1680-1686.
35. Souza DG, Teixeira MM. The balance between the production of tumor necrosis factor-alpha and interleukin-10 determines tissue injury and lethality during intestinal ischemia and reperfusion. Mem Inst Oswaldo Cruz 2005;100(Suppl):59-66.
36. Souza DG, et al. The required role of endogenously produced lipoxin A4 and annexin-1 for the production of IL-10 and inflammatory hyporesponsiveness in mice. J Immunol 2007;179:8533-8543.
37. Serhan CN. Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am J Pathol 2010;177:1576-1591.
38. Perretti M, D'Acquisto F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat Rev Immunol 2009;9:62-70.
39. Oliveira MR, et al. Germ-free mice produce high levels of interferon-gamma in response to infection with Leishmania major but fail to heal lesions. Parasitology 2005;131:477-488.
40. Duarte R, Silva AM, Vieira LQ, Afonso LC, Nicoli JR. Trypanosoma cruzi: influence of predominant bacteria from indigenous digestive microbiota on experimental infection in mice. Exp Parasitol 2005;111:87-96.
41. dos Santos LM, Santos MM, de Souza Silva HP, Arantes RM, Nicoli JR, Vieira LQ. Monoassociation with probiotic Lactobacillus delbrueckii UFV-H2b20 stimulates the immune system and protects germfree mice against Listeria monocytogenes infection. Med Microbiol Immunol 2011;200:29-38.
42. Fagundes CT, et al. Control of host inflammatory responsiveness by indigenous microbiota reveals an adaptive component of the innate immune system. Microbes Infect 2011.
43. Amaral FA, et al. Commensal microbiota is fundamental for the development of inflammatory pain. Proc Natl Acad Sci USA 2008;105:2193-2197.
44. Maslowski KM, et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009;461:1282-1286.
45. Matzinger P. The danger model: a renewed sense of self. Science 2002;296:301-305.
46. Millan MJ. The induction of pain: an integrative review. Prog Neurobiol 1999;57:1-164.
47. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature 2001;413:203-210.
48. Basbaum AI, Bautista DM, Scherrer G, Julius D. Cellular and molecular mechanisms of pain. Cell 2009;139:267-284.
49. Verri WA Jr, Cunha TM, Parada CA, Poole S, Cunha FQ, Ferreira SH. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 2006;112:116-138.
50. Anand P. Neurotrophic factors and their receptors in human sensory neuropathies. Prog Brain Res 2004;146:477-492.
51. Stucky CL, Gold MS, Zhang X. Mechanisms of pain. Proc Natl Acad Sci USA 2001;98:11845-11846.
52. Mayer EA, Tillisch K. The brain-gut axis in abdominal pain syndromes. Annu Rev Med 2011;62:381-396.
53. Mayer EA, Naliboff BD, Chang L, Coutinho SV. V. Stress and irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol 2001;280:G519-24.
54. Thompson WG. Irritable bowel syndrome: a management strategy. Baillieres Best Pract Res Clin Gastroenterol 1999;13:453-460.
55. Parkes GC, Sanderson JD, Whelan K. Treating irritable bowel syndrome with probiotics: the evidence. Proc Nutr Soc 2010;69:187-194.
56. Verdu EF, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 2006;55:182-190.
57. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 2010;22:1029-1035.
58. Rousseaux C, et al. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 2007;13:35-37.
59. Hannington-Kiff JG. Intravenous regional sympathetic block with guanethidine. Lancet 1974;1:1019-10120.
60. Nakamura M, Ferreira SH. A peripheral sympathetic component in inflammatory hyperalgesia. Eur J Pharmacol 1987;135:145-153.
61. Duarte ID, Nakamura M, Ferreira SH. Participation of the sympathetic system in acetic acid-induced writhing in mice. Braz J Med Biol Res 1988;21:341-343.
62. Cunha TM, Verri WA Jr, Silva JS, Poole S, Cunha FQ, Ferreira SH. A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc Natl Acad Sci USA 2005;102:1755-1760.
63. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006;440:237-241.
64. Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol 2009;27:229-265.
65. Franchi L, Eigenbrod T, Munoz-Planillo R, Nunez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 2009;10:241-247.
66. Collins SM, Bercik P. The relationship between intestinal microbiota and the central nervous system in normal GI function and disease. Gastroenterology 2009;136:2003-2014.
67. Strauss E, da Costa MF. The importance of bacterial infections as precipating factors of chronic hepatic encephalopathy in cirrhosis. Hepatogastroenterology 1998;45:900-904.
68. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI. Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001;291:881-884.
69. Uribe A, Alam M, Johansson O, Midtvedt T, Theodorsson E. Microflora modulates endocrine cells in the GI mucosa of the rat. Gastroenterology 1994;107:1259-1269.
70. Husebye E, Hellstrom PM, Sundler F, Chen J, Midtvedt T. Influence of microbial species on small intestinal myoelectric activity and transit in germ-free rats. Am J Physiol Gastrointest Liver Physiol 2001;280:G368-G380.
71. Caenepeel P, Janssens J, Vantrappen G, Eyssen H, Coremans G. Interdigestive myoelectric complex in germ-free rats. Dig Dis Sci 1989;34:1180-1184.
72. Burton MB, Gebhart GF. Effects of intracolonic acetic acid on responses to colorectal distension in the rat. Brain Res 1995;672:77-82.
73. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008;43:164-174.
74. Sudo N. Stress and gut microbiota: does postnatal microbial colonization program the hypothalamic-pituitary-adrenal system for stress response? Int Congr Ser 2006;1287:350-354.
75. Heijtz RD, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci USA 2011;108:3047-3052.
76. Bercik P, et al. The Intestinal Microbiota Affect Central Levels of Brain-Derived Neurotropic Factor and Behavior in Mice. Gastroenterology 2011;141:599-609. e3.
77. Gaykema RP, Goehler LE, Lyte M. Brain response to cecal infection with Campylobacter jejuni: analysis with Fos immunohistochemistry. Brain Behav Immun 2004;18:238-245.
78. Goehler LE, Gaykema RP, Opitz N, Reddaway R, Badr N, Lyte M. Activation in vagal afferents and central autonomic pathways: early responses to intestinal infection with Campylobacter jejuni. Brain Behav Immun 2005;19:334-344.
79. Lyte M, Li W, Opitz N, Gaykema RP, Goehler LE. Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Physiol Behav 2006;89:350-357.
80. Goehler LE, Park SM, Opitz N, Lyte M, Gaykema RP. Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 2008;22:354-366.
81. Neufeld KM, Kang N, Bienenstock J, Foster JA. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2011;23:255-264.
82. Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J. Mood and gut feelings. Brain Behav Immun 2010;24:9-16.
83. Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol Behav 2009;96:557-567.
84. Seckl JR, Meaney MJ. Glucocorticoid programming. Ann NY Acad Sci 2004;1032:63-84.
85. Bilbo SD, Levkoff LH, Mahoney JH, Watkins LR, Rudy JW, Maier SF. Neonatal infection induces memory impairments following an immune challenge in adulthood. Behav Neurosci 2005;119:293-301.
86. Sullivan R, et al. The International Society for Developmental Psychobiology annual meeting symposium: Impact of early life experiences on brain and behavioral development. Dev Psychobiol 2006;48:583-602.
87. Lupien SJ, McEwen BS, Gunnar MR, Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009;10:434-445.
88. O'Mahony SM, et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 2009;65:263-267.
89. Freestone PP, Sandrini SM, Haigh RD, Lyte M. Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 2008;16:55-64.
90. Dowd SE, Callaway TR, Morrow-Tesch J. Handling may cause increased shedding of Escherichia coli and total coliforms in pigs. Foodborne Pathog Dis 2007;4:99-102.
91. Clarke MB, Hughes DT, Zhu C, Boedeker EC, Sperandio V. The QseC sensor kinase: a bacterial adrenergic receptor. Proc Natl Acad Sci USA 2006;103:10420-10425.
92. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011;25:397-407.
93. O'Mahony L, et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005;128:541-551.
94. Iyer LM, Aravind L, Coon SL, Klein DC, Koonin EV. Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role? Trends Genet 2004;20:292-299.
95. Wikoff WR, et al. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sc3i USA 2009;106:3698-703.
96. Hoverstad T, Midtvedt T. Short-chain fatty acids in germfree mice and rats. J Nutr 1986;116:1772-1776.
97. Schroeder FA, Lin CL, Crusio WE, Akbarian S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 2007;62:55-64.
98. MacFabe DF, et al. 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;176:149-169.
99. Wang R. Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J 2002;16:1792-1798.
100. Gilad GM, Gilad VH. Overview of the brain polyamine-stress-response: regulation, development, and modulation by lithium and role in cell survival. Cell Mol Neurobiol 2003;23:637-649.
101. Gilad GM, Gilad VH, Casanova MF, Casero RA Jr. Polyamines and their metabolizing enzymes in human frontal cortex and hippocampus: preliminary measurements in affective disorders. Biol Psychiatry 1995;38:227-234.
102. Ziv Y, Schwartz M. Immune-based regulation of adult neurogenesis: implications for learning and memory. Brain Behav Immun 2008;22:167-176.
103. Ziv Y, et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat Neurosci 2006;9:268-275.
104. Kipnis J, Cohen H, Cardon M, Ziv Y, Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc Natl Acad Sci USA 2004;101:8180-8185.
105. Butovsky O, et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci 2006;31:149-160.
106. Carro E, Trejo JL, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates the protective effects of physical exercise against brain insults of different etiology and anatomy. J Neurosci 2001;21:5678-5684.
107. Trejo JL, Carro E, Torres-Aleman I. Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 2001;21:1628-1634.
108. Chen SK, et al. Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 2010;141:775-785.
109. Johnson JD, et al. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. Neuroscience 2005;135:1295-1307.
110. Campisi J, Leem Th, Fleshner M. Acute stress decreases inflammation at the site of infection. A role for nitric oxide. Physiol Behav 2002;77:291-299.
111. Campisi J, Leem Th, Fleshner M. Stress-induced extracellular Hsp72 is a functionally significant danger signal to the immune system. Cell Stress Chaperones 2003;8:272-286.
112. Deak T, et al. Evidence that brief stress may induce the acute phase response in rats. Am J Physiol 1997;273:R1998-R2004.
113. Ashwell JD, Lu FW, Vacchio MS. Glucocorticoids in T cell development and function. Annu Rev Immunol 2000;18:309-345.
114. Battista D, Ferrari CC, Gage FH, Pitossi FJ. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur J Neurosci 2006;23:83-93.
115. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999;2:894-897.
116. Livnat S, Felten SY, Carlson SL, Bellinger DL, Felten DL. Involvement of peripheral and central catecholamine systems in neural-immune interactions. J Neuroimmunol 1985;10:5-30.
117. Lyte M, Ernst S, Driemeyer J, Baissa B. Strain-specific enhancement of splenic T cell mitogenesis and macrophage phagocytosis following peripheral axotomy. J Neuroimmunol 1991;31:1-8.
118. Katayama Y, et al. Signals from the sympathetic nervous system regulate hematopoietic stem cell egress from bone marrow. Cell 2006;124:407-421.
119. Finegold SM, et al. Gastrointestinal microflora studies in late-onset autism. Clin Infect Dis 2002;35:S6-S16.
120. Mittal VA, Ellman LM, Cannon TD. Gene-environment interaction and covariation in schizophrenia: the role of obstetric complications. Schizophr Bull 2008;34:1083-1094.
121. Wu HJ, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010;32:815-827.
122. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2010;108(Suppl):4615-4622.