Histamine regulation of microglia: Gene-environment interaction in the regulation of central nervous system inflammation

Brain, Behavior, and Immunity

Volumn 57, Issue , 2016, Pages 326-337

  Frick, Luciana ^a   Rapanelli, Maximiliano ^a   Abbasi, Eeman ^a   Ohtsu, Hiroshi ^b   Pittenger, Christopher ^a,c,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TOHOKU UNIVERSITY   (Japan)

^c YALE UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Basal ganglia; H4R receptor; IGF 1; Lipopolysaccharide

Indexed keywords

HISTAMINE; HISTAMINE H4 RECEPTOR; HISTAMINE RECEPTOR; HISTIDINE DECARBOXYLASE; LIPOPOLYSACCHARIDE; SOMATOMEDIN C; INSULIN-LIKE GROWTH FACTOR-1, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; GENOTYPE ENVIRONMENT INTERACTION; HDC GENE; HISTAMINERGIC NEURON; HYPOTHALAMUS; IN VIVO STUDY; MALE; MICROGLIA; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; CENTRAL NERVOUS SYSTEM DISEASE; DEFICIENCY; GENETICS; INFLAMMATION; METABOLISM; TRANSGENIC MOUSE;

ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; CORPUS STRIATUM; GENE-ENVIRONMENT INTERACTION; HISTAMINE; HISTIDINE DECARBOXYLASE; INFLAMMATION; INSULIN-LIKE GROWTH FACTOR I; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; RECEPTORS, HISTAMINE H4;

EID: 84992187650     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.07.002     Document Type: Article

References (71)

1. Ahmari, S.E., et al. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science 340:6137 (2013), 1234–1239.
2. Arroba, A.I., Alvarez-Lindo, N., van Rooijen, N., de la Rosa, E.J., Microglia-mediated IGF-I neuroprotection in the rd10 mouse model of retinitis pigmentosa. Invest. Ophthalmol. Vis. Sci. 52:12 (2011), 9124–9130.
3. Biber, K., Neumann, H., Inoue, K., Boddeke, H.W., Neuronal ‘On’ and ‘Off’ signals control microglia. Trends Neurosci. 30:11 (2007), 596–602.
4. Bloch, M., State, M., Pittenger, C., Recent advances in Tourette syndrome. Curr. Opin. Neurol. 24:2 (2011), 119–125.
5. Butovsky, O., Talpalar, A.E., Ben-Yaakov, K., Schwartz, M., Activation of microglia by aggregated beta-amyloid or lipopolysaccharide impairs MHC-II expression and renders them cytotoxic whereas IFN-gamma and IL-4 render them protective. Mol. Cell. Neurosci. 29:3 (2005), 381–393.
6. Castellan Baldan, L., et al. Histidine decarboxylase deficiency causes Tourette syndrome: parallel findings in humans and mice. Neuron 81:1 (2014), 77–90.
7. Chen, S.K., et al. Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 141:5 (2010), 775–785.
8. Chiu, I.M., et al. T lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc. Natl. Acad. Sci. U.S.A. 105:46 (2008), 17913–17918.
9. Connelly, W.M., et al. The histamine H4 receptor is functionally expressed on neurons in the mammalian CNS. Br. J. Pharmacol. 157:1 (2009), 55–63.
10. Crain, J.M., Nikodemova, M., Watters, J.J., Microglia express distinct M1 and M2 phenotypic markers in the postnatal and adult central nervous system in male and female mice. J. Neurosci. Res. 91:9 (2013), 1143–1151.
11. Davis, L.K., et al. Partitioning the heritability of Tourette syndrome and obsessive compulsive disorder reveals differences in genetic architecture. PLoS Genet., 9(10), 2013, e1003864.
12. Dong, H., et al. Histamine induces upregulated expression of histamine receptors and increases release of inflammatory mediators from microglia. Mol. Neurobiol. 49:3 (2014), 1487–1500.
13. Duric, V., et al. Altered expression of synapse and glutamate related genes in post-mortem hippocampus of depressed subjects. Int. J. Neuropsychopharmacol. 16:1 (2013), 69–82.
14. Ercan-Sencicek, A.G., et al. L-Histidine decarboxylase and Tourette's syndrome. N. Engl. J. Med. 362:20 (2010), 1901–1908.
15. Fernandez, T.V., et al. Rare copy number variants in Tourette syndrome disrupt genes in histaminergic pathways and overlap with autism. Biol. Psychiatry 71:5 (2012), 392–402.
16. Ferreira, R., et al. Histamine modulates microglia function. J. Neuroinflammation, 9, 2012, 90.
17. Frick, L.R., Williams, K., Pittenger, C., Microglial dysregulation in psychiatric disease. Clin. Dev. Immunol., 2013, 2013, 608654.
18. Goodchild, R.E., et al. Distribution of histamine H3-receptor binding in the normal human basal ganglia: comparison with Huntington's and Parkinson's disease cases. Eur. J. Neurosci. 11:2 (1999), 449–456.
19. Greer, J.M., Capecchi, M.R., Hoxb8 is required for normal grooming behavior in mice. Neuron 33 (2002), 23–34.
20. Haas, H.L., Sergeeva, O.A., Selbach, O., Histamine in the nervous system. Physiol. Rev. 88:3 (2008), 1183–1241.
21. Henry, C.J., Huang, Y., Wynne, A.M., Godbout, J.P., Peripheral lipopolysaccharide (LPS) challenge promotes microglial hyperactivity in aged mice that is associated with exaggerated induction of both pro-inflammatory IL-1beta and anti-inflammatory IL-10 cytokines. Brain Behav. Immun. 23:3 (2009), 309–317.
22. Hong, J.J., et al. Microarray analysis in Tourette syndrome postmortem putamen. J. Neurol. Sci. 225:1–2 (2004), 57–64.
23. Hornig, M., Lipkin, W.I., Immune-mediated animal models of Tourette syndrome. Neurosci. Biobehav. Rev. 37:6 (2013), 1120–1138.
24. Iida, T., et al. Histamine H3 receptor in primary mouse microglia inhibits chemotaxis, phagocytosis, and cytokine secretion. Glia 63:7 (2015), 1213–1225.
25. Ji, K., Miyauchi, J., Tsirka, S.E., Microglia: an active player in the regulation of synaptic activity. Neural Plast., 2013, 2013, 627325.
26. John, J., et al. Greatly increased numbers of histamine cells in human narcolepsy with cataplexy. Ann. Neurol. 74:6 (2013), 786–793.
27. Karagiannidis, I., et al. Support of the histaminergic hypothesis in Tourette syndrome: association of the histamine decarboxylase gene in a large sample of families. J. Med. Genet. 50:11 (2013), 760–764.
28. Kawikova, I., et al. Decreased numbers of regulatory T cells suggest impaired immune tolerance in children with Tourette syndrome: a preliminary study. Biol. Psychiatry 61:3 (2007), 273–278.
29. Kawikova, I., et al. Children with Tourette's syndrome may suffer immunoglobulin A dysgammaglobulinemia: preliminary report. Biol. Psychiatry 67:7 (2010), 679–683.
30. Kim, D.H., et al. Early immature neuronal death initiates cerebral ischemia-induced neurogenesis in the dentate gyrus. Neuroscience 284C (2014), 42–54.
31. Kohman, R.A., DeYoung, E.K., Bhattacharya, T.K., Peterson, L.N., Rhodes, J.S., Wheel running attenuates microglia proliferation and increases expression of a proneurogenic phenotype in the hippocampus of aged mice. Brain Behav. Immun. 26:5 (2012), 803–810.
32. Krusong, K., et al. High levels of histidine decarboxylase in the striatum of mice and rats. Neurosci. Lett. 495:2 (2011), 110–114.
33. Kumar, A., Williams, M.T., Chugani, H.T., Evaluation of basal ganglia and thalamic inflammation in children with pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection and Tourette syndrome: a positron emission tomographic (PET) study using 11C-[R]-PK11195. J. Child Neurol., 2014.
34. Lalancette-Hebert, M., Gowing, G., Simard, A., Weng, Y.C., Kriz, J., Selective ablation of proliferating microglial cells exacerbates ischemic injury in the brain. J. Neurosci. 27:10 (2007), 2596–2605.
35. Leckman, J.F., et al. Increased serum levels of interleukin-12 and tumor necrosis factor-alpha in Tourette's syndrome. Biol. Psychiatry 57:6 (2005), 667–673.
36. Leckman, J.F., Bloch, M.H., Smith, M.E., Larabi, D., Hampson, M., Neurobiological substrates of Tourette's disorder. J. Child Adolesc. Psychopharmacol. 20:4 (2010), 237–247.
37. Lennington, J.B., et al. Transcriptome analysis of the human striatum in Tourette syndrome. Biol. Psychiatry, 2014.
38. Matz, J., et al. Altered monocyte activation markers in Tourette's syndrome: a case-control study. BMC Psychiatry, 12, 2012, 29.
39. Mitchell, R.H., Goldstein, B.I., Inflammation in children and adolescents with neuropsychiatric disorders: a systematic review. J. Am. Acad. Child Adolesc. Psychiatry 53:3 (2014), 274–296.
40. Morer, A., et al. Elevated expression of MCP-1, IL-2 and PTPR-N in basal ganglia of Tourette syndrome cases. Brain Behav. Immun. 24:7 (2010), 1069–1073.
41. Naddafi, F., Mirshafiey, A., The neglected role of histamine in Alzheimer's disease. Am. J. Alzheimers Dis. Other Demen. 28:4 (2013), 327–336.
42. Ohtsu, H., et al. Mice lacking histidine decarboxylase exhibit abnormal mast cells. FEBS Lett. 502:1–2 (2001), 53–56.
43. Olah, M., Biber, K., Vinet, J., Boddeke, H.W., Microglia phenotype diversity. CNS Neurol. Disord.: Drug Targets 10:1 (2011), 108–118.
44. Pannell, M., Szulzewsky, F., Matyash, V., Wolf, S.A., Kettenmann, H., The subpopulation of microglia sensitive to neurotransmitters/neurohormones is modulated by stimulation with LPS, interferon-gamma, and IL-4. Glia 62:5 (2014), 667–679.
45. Panula, P., Nuutinen, S., The histaminergic network in the brain: basic organization and role in disease. Nat. Rev. Neurosci. 14:7 (2013), 472–487.
46. Passani, M.B., Ballerini, C., Histamine and neuroinflammation: insights from murine experimental autoimmune encephalomyelitis. Front. Syst. Neurosci., 6, 2012, 32.
47. Paxinos, G., Franklin, K.B.J., The Mouse Brain in Stereotaxic Coordinates. Compact 2nd ed., 2004, Elsevier Academic Press, Amsterdam, Boston.
48. Peca, J., et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472:7344 (2011), 437–442.
49. Rapanelli, M., et al. Dysregulated intracellular signaling in the striatum in a pathophysiologically grounded model of Tourette syndrome. Eur. Neuropsychopharmacol. 24:12 (2014), 1896–1906.
50. Rapanelli, M., Frick, L.R., Bito, H., Pittenger, C., submitted for publication. Dissociable regulation of grooming and exploration by hypothalamic histaminergic neurons. Neuron.
51. Rocha, S.M., Pires, J., Esteves, M., Graca, B., Bernardino, L., Histamine: a new immunomodulatory player in the neuron-glia crosstalk. Front. Cell. Neurosci., 8, 2014, 120.
52. Schafer, D.P., Lehrman, E.K., Stevens, B., The “quad-partite” synapse: microglia-synapse interactions in the developing and mature CNS. Glia 61:1 (2013), 24–36.
53. Servello, D., Sassi, M., Gaeta, M., Ricci, C., Porta, M., Tourette syndrome (TS) bears a higher rate of inflammatory complications at the implanted hardware in deep brain stimulation (DBS). Acta Neurochir. 153:3 (2011), 629–632.
54. Shan, L., et al. Alterations in the histaminergic system in the substantia nigra and striatum of Parkinson's patients: a postmortem study. Neurobiol. Aging, 33(7), 2012 1488 e1481-1413.
55. Shan, L., Bossers, K., Unmehopa, U., Bao, A.M., Swaab, D.F., Alterations in the histaminergic system in Alzheimer's disease: a postmortem study. Neurobiol. Aging 33:11 (2012), 2585–2598.
56. Shmelkov, S.V., et al. Slitrk5 deficiency impairs corticostriatal circuitry and leads to obsessive-compulsive-like behaviors in mice. Nat. Med. 16:5 (2010), 598–602 591p following 602.
57. Siskova, Z., Tremblay, M.E., Microglia and synapse: interactions in health and neurodegeneration. Neural Plast., 2013, 2013, 425845.
58. Strakhova, M.I., et al. Localization of histamine H4 receptors in the central nervous system of human and rat. Brain Res. 1250 (2009), 41–48.
59. Ueno, M., et al. Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16:5 (2013), 543–551.
60. Valko, P.O., et al. Increase of histaminergic tuberomammillary neurons in narcolepsy. Ann. Neurol. 74:6 (2013), 794–804.
61. van Wamelen, D.J., et al. Functional increase of brain histaminergic signaling in Huntington's disease. Brain Pathol. 21:4 (2011), 419–427.
62. Weidinger, E., et al. Impaired activation of the innate immune response to bacterial challenge in Tourette syndrome. World J. Biol. Psychiatry 15:6 (2014), 453–458.
63. Welch, J.M., et al. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 448:7156 (2007), 894–900.
64. Wernersson, S., Pejler, G., Mast cell secretory granules: armed for battle. Nat. Rev. Immunol. 14:7 (2014), 478–494.
65. Williams, K., Bloch, M.H., State, M.W., Pittenger, C., Tourette syndrome. Charney, D.S., Buxbaum, J.D., Sklar, P., Nestler, E.J., (eds.) Neurobiology of Mental Illness, 4th ed., 2013, Oxford University Press, New York.
66. Xu, M., et al. Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome. Proc. Natl. Acad. Sci. U.S.A., 2015.
67. Yang, C.F., et al. Sexually dimorphic neurons in the ventromedial hypothalamus govern mating in both sexes and aggression in males. Cell 153:4 (2013), 896–909.
68. Zecharia, A.Y., et al. GABAergic inhibition of histaminergic neurons regulates active waking but not the sleep-wake switch or propofol-induced loss of consciousness. J. Neurosci. 32:38 (2012), 13062–13075.
69. Zhan, Y., et al. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17:3 (2014), 400–406.
70. Zhu, J., Qu, C., Lu, X., Zhang, S., Activation of microglia by histamine and substance P. Cell. Physiol. Biochem. 34:3 (2014), 768–780.
71. Ziv, Y., et al. Immune cells contribute to the maintenance of neurogenesis and spatial learning abilities in adulthood. Nat. Neurosci. 9:2 (2006), 268–275.