Histamine H3 receptor in primary mouse microglia inhibits chemotaxis, phagocytosis, and cytokine secretion

GLIA

Volumn 63, Issue 7, 2015, Pages 1213-1225

  Iida, Tomomitsu ^a,b   Yoshikawa, Takeo ^a   Matsuzawa, Takuro ^a   Naganuma, Fumito ^a   Nakamura, Tadaho ^a   Miura, Yamato ^a   Mohsen, Attayeb S ^a   Harada, Ryuichi ^a   Iwata, Ren ^b   Yanai, Kazuhiko ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

Author keywords

Chemotaxis; Cytokine secretion; H3R; Histamine secretion; Phagocytosis

Indexed keywords

AMTHAMINE; CYCLIC AMP; FORSKOLIN; HISTAMINE H2 RECEPTOR; HISTAMINE H3 RECEPTOR; HISTAMINE METHYLTRANSFERASE; HISTIDINE DECARBOXYLASE; IMETIT; LIPOPOLYSACCHARIDE; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA; CALCIUM; CYTOKINE; HISTAMINE; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CHEMOTAXIS; CHEMOTAXIS ASSAY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HISTAMINE METABOLISM; LIGAND BINDING; MICROGLIA; MOUSE; NEWBORN; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECOND MESSENGER; ANIMAL; C57BL MOUSE; CELL CULTURE; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; CALCIUM; CELLS, CULTURED; CHEMOTAXIS; CYCLIC AMP; CYTOKINES; DINOPROSTONE; HISTAMINE; MICE, INBRED C57BL; MICROGLIA; PHAGOCYTOSIS; RECEPTORS, HISTAMINE H2; RECEPTORS, HISTAMINE H3; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84928203400     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22812     Document Type: Article

References (74)

1. Arbones L, Picatoste F, Garcia A. 1990. Histamine stimulates glycogen breakdown and increases 45Ca2+ permeability in rat astrocytes in primary culture. Mol Pharmacol 37:921-927.
2. Bader MF, Taupenot L, Ulrich G, Aunis D, Ciesielski-Treska J. 1994. Bacterial endotoxin induces [Ca2+]i transients and changes the organization of actin in microglia. Glia 11:336-344.
3. Brown RE, Stevens DR, Haas HL. 2001. The physiology of brain histamine. Prog Neurobiol 63:637-672.
4. Burban A, Faucard R, Armand V, Bayard C, Vorobjev V, Arrang JM. 2010. Histamine potentiates N-methyl-d-aspartate receptors by interacting with an allosteric site distinct from the polyamine binding site. J Pharmacol Exp Ther 332:912-921.
5. Carman-Krzan M, Lipnik-Stangelj M. 2000. Molecular properties of central and peripheral histamine H1 and H2 receptors. Pflugers Arch 439:R131-R132.
6. Chang JY, Liu LZ. 2000. Catecholamines inhibit microglial nitric oxide production. Brain Res Bull 52:525-530.
7. Chazot PL. 2009. Advances in histamine pharmacology reveal new drug targets. Br J Pharmacol 157:1-3.
8. Chikahisa S, Kodama T, Soya A, Sagawa Y, Ishimaru Y, Nishino SHS. 2013. Histamine from brain resident MAST cells promotes wakefulness and modulates behavioral states. PLoS One 8:e78434.
9. Dale HH, Laidlaw PP. 1910. The physiological action of beta-iminazolylethylamine. J Physiol 41:318-344.
10. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB. 2005. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-758.
11. Dy M, Lebel B, Schneider E. 1982. Presence of histaminase in fetal calf sera. J Immunol Methods 48:261-265.
12. Ehrhart J, Obregon D, Mori T, Hou H, Sun N, Bai Y, Klein T, Fernandez F, Tan J, Shytle RD. 2005. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2:29.
13. Espinosa-Parrilla JF, Martinez-Moreno M, Gasull X, Mahy N, Rodriguez MJ. 2014. The L-type voltage-gated calcium channel modulates microglial pro-inflammatory activity. Mol Cell Neurosci 64C:104-115.
14. Fang Q, Hu WW, Wang XF, Yang Y, Lou GD, Jin MM, Yan HJ, Zeng WZ, Shen Y, Zhang SH, Xu TL, Chen Z. 2014. Histamine up-regulates astrocytic glutamate transporter 1 and protects neurons against ischemic injury. Neuropharmacology 77:156-166.
15. Ferreira R, Santos T, Goncalves J, Baltazar G, Ferreira L, Agasse F, Bernardino L. 2012. Histamine modulates microglia function. J Neuroinflammation 9:90.
16. Gantz I, Munzert G, Tashiro T, Schaffer M, Wang L, DelValle J, Yamada T. 1991. Molecular cloning of the human histamine H2 receptor. Biochem Biophys Res Commun 178:1386-1392.
17. García-Martín E, Ayuso P, Martínez C, Blanca M, Agúndez JA. 2009. Histamine pharmacogenomics. Pharmacogenomics 10:867-883.
18. Gordon R, Hogan CE, Neal ML, Anantharam V, Kanthasamy AG, Kanthasamy A. 2011. A simple magnetic separation method for high-yield isolation of pure primary microglia. J Neurosci Methods 194:287-296.
19. Greenbaum D, Colangelo C, Williams K, Gerstein M. 2003. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117.
20. Haas HL, Sergeeva OA, Selbach O. 2008. Histamine in the nervous system. Physiol Rev 88:1183-1241.
21. Hall AA, Herrera Y, Ajmo CT Jr, Cuevas J, Pennypacker KR. 2009. Sigma receptors suppress multiple aspects of microglial activation. Glia 57:744-754.
22. Hashioka S, Klegeris A, Monji A, Kato T, Sawada M, McGeer PL, Kanba S. 2007. Antidepressants inhibit interferon-gamma-induced microglial production of IL-6 and nitric oxide. Exp Neurol 206:33-42.
23. Hayashi Y, Koyanagi S, Kusunose N, Okada R, Wu Z, Tozaki-Saitoh H, Ukai K, Kohsaka S, Inoue K, Ohdo S, Nakanishi H. 2013. The intrinsic microglial molecular clock controls synaptic strength via the circadian expression of cathepsin S. Sci Rep 3:2744.
24. Horvath RJ, Nutile-McMenemy N, Alkaitis MS, Deleo JA. 2008. Differential migration, LPS-induced cytokine, chemokine, and NO expression in immortalized BV-2 and HAPI cell lines and primary microglial cultures. J Neurochem 107:557-569.
25. Huszti Z, Prast H, Tran MH, Fischer H, Philippu A. 1998. Glial cells participate in histamine inactivation in vivo. Naunyn Schmiedebergs Arch Pharmacol 357:49-53.
26. Inocente C, Arnulf I Fau - Bastuji H, Bastuji H Fau - Thibault-Stoll A, Thibault-Stoll A Fau - Raoux A, Raoux A Fau - Reimao R, Reimao R Fau - Lin J-S, Lin Js Fau - Franco P, Franco P. 2012. Pitolisant, an inverse agonist of the histamine H3 receptor: An alternative stimulant for narcolepsy-cataplexy in teenagers with refractory sleepiness. Clin Neuropharmacol 35:55-60.
27. Inoue K. 2007. UDP facilitates microglial phagocytosis through P2Y6 receptors. Cell Adh Migr 1:131-132.
28. Irino Y, Nakamura Y, Inoue K, Kohsaka S, Ohsawa K. 2008. Akt activation is involved in P2Y12 receptor-mediated chemotaxis of microglia. J Neurosci Res 86:1511-1519.
29. Jin Y, Sato K, Tobo A, Mogi C, Tobo M, Murata N, Ishii S, Im DS, Okajima F. 2014. Inhibition of interleukin-1beta production by extracellular acidification through the TDAG8/cAMP pathway in mouse microglia. J Neurochem 129:683-695.
30. Jones BL, Kearns GL. 2011. Histamine: New thoughts about a familiar mediator. Clin Pharmacol Ther 89:189-197.
31. Juric DM, Mele T, Carman-Krzan M. 2011. Involvement of histaminergic receptor mechanisms in the stimulation of NT-3 synthesis in astrocytes. Neuropharmacology 60:1309-1317.
32. Kaindl AM, Degos V, Peineau S, Gouadon E, Chhor V, Loron G, Le Charpentier T, Josserand J, Ali C, Vivien D, Collingridge GL, Lombet A, Issa L, Rene F, Loeffler JP, Kavelaars A, Verney C, Mantz J, Gressens P. 2012. Activation of microglial N-methyl-d-aspartate receptors triggers inflammation and neuronal cell death in the developing and mature brain. Ann Neurol 72:536-549.
33. Katoh Y, Niimi M, Yamamoto Y, Kawamura T, Morimoto-Ishizuka T, Sawada M, Takemori H, Yamatodani A. 2001. Histamine production by cultured microglial cells of the mouse. Neurosci Lett 305:181-184.
34. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. 2010. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412.
35. Klegeris A, Bissonnette CJ, McGeer PL. 2003. Reduction of human monocytic cell neurotoxicity and cytokine secretion by ligands of the cannabinoid-type CB2 receptor. Br J Pharmacol 139:775-786.
36. Koizumi S, Shigemoto-Mogami Y, Nasu-Tada K, Shinozaki Y, Ohsawa K, Tsuda M, Joshi BV, Jacobson KA, Kohsaka S, Inoue K. 2007. UDP acting at P2Y6 receptors is a mediator of microglial phagocytosis. Nature 446:1091-1095.
37. Komori H, Nitta Y, Ueno H, Higuchi Y. 2012. Structural study reveals that Ser-354 determines substrate specificity on human histidine decarboxylase. J Biol Chem 287:29175-29183.
38. Lee M, Schwab C, McGeer PL. 2011. Astrocytes are GABAergic cells that modulate microglial activity. Glia 59:152-165.
39. Lipnik-Stangelj M, Carman-Krzan M. 2004. Activation of histamine H1-receptor enhances neurotrophic factor secretion from cultured astrocytes. Inflamm Res 53:245-252.
40. Liu J, Zhao X, Cao J, Xue Q, Feng X, Liu X, Zhang F, Yu B. 2011. Differential roles of PKA and epac on the production of cytokines in the endotoxin-stimulated primary cultured microglia. J Mol Neurosci 45:186-193.
41. Lovenberg TW, Roland BL, Wilson SJ, Jiang X, Pyati J, Huvar A, Jackson MR, Erlander MG. 1999. Cloning and functional expression of the human histamine H3 receptor. Mol Pharmacol 55:1101-1107.
42. Lyons SA, Morell P, McCarthy KD. 1995. Schwann cell ATP-mediated calcium increases in vitro and in situ are dependent on contact with neurons. Glia 13:27-38.
43. Martin-Moreno AM, Reigada D, Ramirez BG, Mechoulam R, Innamorato N, Cuadrado A, de Ceballos ML. 2011. Cannabidiol and other cannabinoids reduce microglial activation in vitro and in vivo: Relevance to Alzheimer's disease. Mol Pharmacol 79:964-973.
44. Masaki T, Yoshimatsu H. 2007. Neuronal histamine and histamine receptors in food intake and obesity. Mini Rev Med Chem 7:821-825.
45. McGrath JC, Drummond GB, McLachlan EM, Kilkenny C, Wainwright CL. 2010. Guidelines for reporting experiments involving animals: The ARRIVE guidelines. Br J Pharmacol 160:1573-1576.
46. Nakamura T, Yoshikawa T, Noguchi N, Sugawara A, Kasajima A, Sasano H, Yanai K. 2014. The expression and function of histamine H receptor in pancreatic beta-cells. Br J Pharmacol 171:171-185.
47. Nakano T, Andoh T, Sasaki A, Nojima H, Kuraishi Y. 2008. Different roles of capsaicin-sensitive and H1 histamine receptor-expressing sensory neurones in itch of mosquito allergy in mice. Acta Derm Venereol 88:449-454.
48. Napoli I, Neumann H. 2009. Microglial clearance function in health and disease. Neuroscience 158:1030-1038.
49. Olah M, Biber K, Vinet J, Boddeke HW. 2011. Microglia phenotype diversity. CNS Neurol Disord Drug Targets 10:108-118.
50. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R. 2003. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278:13309-13317.
51. Quan Y, Jiang J, Dingledine R. 2013. EP2 receptor signaling pathways regulate classical activation of microglia. J Biol Chem 288:9293-9302.
52. Rodriguez J, Moran J, Blanco I, Patel AJ. 1989. Effect of histamine on the development of astroglial cells in culture. Neurochem Res 14:693-700.
53. Romero-Sandoval EA, Horvath R, Landry RP, DeLeo JA. 2009. Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation. Mol Pain 5:25.
54. Ryu JK, Cho T, Choi HB, Wang YT, McLarnon JG. 2009. Microglial VEGF receptor response is an integral chemotactic component in Alzheimer's disease pathology. J Neurosci 29:3-13.
55. Saras A, Gisselmann G, Vogt-Eisele AK, Erlkamp KS, Kletke O, Pusch H, Hatt H. 2008. Histamine action on vertebrate GABAA receptors: Direct channel gating and potentiation of GABA responses. J Biol Chem 283:10470-10475.
56. Schwartz J-C. 2011. The histamine H3 receptor: From discovery to clinical trials with pitolisant. Br J Pharmacol 163:713-721.
57. Seifert S, Pannell M, Uckert W, Farber K, Kettenmann H. 2011. Transmitter- and hormone-activated ca(2+) responses in adult microglia/brain macrophages in situ recorded after viral transduction of a recombinant ca(2+) sensor. Cell Calcium 49:365-375.
58. Si Q, Nakamura Y, Ogata T, Kataoka K, Schubert P. 1998. Differential regulation of microglial activation by propentofylline via cAMP signaling. Brain Res 812:97-104.
59. Simons FER. 2004. Advances in H1-antihistamines. N Engl J Med 351:2203-2217.
60. Stansley B, Post J, Hensley K. 2012. A comparative review of cell culture systems for the study of microglial biology in Alzheimer's disease. J Neuroinflammation 9:115.
61. Strakhova MI, Nikkel AL, Manelli AM, Hsieh GC, Esbenshade TA, Brioni JD, Bitner RS. 2009. Localization of histamine H4 receptors in the central nervous system of human and rat. Brain Res 1250:41-48.
62. Strasser A, Wittmann HJ, Buschauer A, Schneider EH, Seifert R. 2013. Species-dependent activities of G-protein-coupled receptor ligands: Lessons from histamine receptor orthologs. Trends Pharmacol Sci 34:13-32.
63. Sun Y, Chauhan A, Sukumaran P, Sharma J, Singh BB, Mishra BB. 2014. Inhibition of store-operated calcium entry in microglia by helminth factors: Implications for immune suppression in neurocysticercosis. J Neuroinflammation 11:1.
64. Takeshita Y, Watanabe T, Sakata T, Munakata M, Ishibashi H, Akaike N. 1998. Histamine modulates high-voltage-activated calcium channels in neurons dissociated from the rat tuberomammillary nucleus. Neuroscience 87:797-805.
65. Taylor DL, Diemel LT, Pocock JM. 2003. Activation of microglial group III metabotropic glutamate receptors protects neurons against microglial neurotoxicity. J Neurosci 23:2150-2160.
66. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. 2003. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424:778-783.
67. Uesugi A, Kataoka A, Tozaki-Saitoh H, Koga Y, Tsuda M, Robaye B, Boeynaems JM, Inoue K. 2012. Involvement of protein kinase D in uridine diphosphate-induced microglial macropinocytosis and phagocytosis. Glia 60:1094-1105.
68. Watanabe T, Taguchi Y, Hayashi H, Tanaka J, Shiosaka S, Tohyama M, Kubota H, Terano Y, Wada H. 1983. Evidence for the presence of a histaminergic neuron system in the rat brain: An immunohistochemical analysis. Neurosci Lett 39:249-254.
69. Watanabe T, Taguchi Y, Shiosaka S, Tanaka J, Kubota H, Terano Y, Tohyama M, Wada H. 1984. Distribution of the histaminergic neuron system in the central nervous system of rats: A fluorescent immunohistochemical analysis with histidine decarboxylase as a marker. Brain Res 295:13-25.
70. Watanabe T, Yanai K. 2001. Studies on functional roles of the histaminergic neuron system by using pharmacological agents, knockout mice and positron emission tomography. Tohoku J Exp Med 195:197-217.
71. Weisler RH, Pandina GJ, Daly EJ, Cooper K, Gassmann-Mayer C, Investigators AS. 2012. Randomized clinical study of a histamine H3 receptor antagonist for the treatment of adults with attention-deficit hyperactivity disorder. CNS Drugs 26:421-434.
72. Wolfe MM, Sachs G. 2000. Acid suppression: Optimizing therapy for gastroduodenal ulcer healing, gastroesophageal reflux disease, and stress-related erosive syndrome. Gastroenterology 118:S9-S31.
73. Woo MS, Jung SH, Hyun JW, Kim HS. 2004. Differential regulation of inducible nitric oxide synthase and cytokine gene expression by forskolin and dibutyryl-cAMP in lipopolysaccharide-stimulated murine BV2 microglial cells. Neurosci Lett 356:187-190.
74. Yoshikawa T, Naganuma F, Iida T, Nakamura T, Harada R, Mohsen AS, Kasajima A, Sasano H, Yanai K. 2013. Molecular mechanism of histamine clearance by primary human astrocytes. Glia 61:905-916.