The modulating role of histamine in neuroimmune interactions


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Recently, the involvement of histamine in the regulation of the function of cells in the immune system has been actively studied, including the ability of the mediator to modulate inflammatory responses of different cell types to infectious agents by activating the expression of pattern-recognition receptors. The correlation of histamine with the development of visceral hypersensitivity has also been actively discussed since the mediator can act as a sensitizing agent that alters the activity of nociceptive vanilloid receptors. At the same time, although a significant amount of records has been accumulated disclosing the molecular pathways of histamine biosynthesis and metabolism, intracellular signal transduction schemes with its participation, as well as its main physiological and pathological effects in the organism, there is still no clear understanding of the role of histamine and histamine receptors in neuroimmune interactions. This work presents a review of the current state of the problem and, in particular, summarizes the information reported in the literature considering the effect of histamine on many biological functions of the organism in the context of neuroimmune interactions. The analysis of the studies has allowed establishing the physiological effects of this mediator, in particular, to be realized through innate immunity Toll-like receptors (TLRs). At that, TLRs seem to be able to regulate the expression pattern of vanilloid receptor TRPV1 on sensory neurons in a histamine-dependent manner. Hopefully, further research in this area will contribute to a better understanding of the general mechanisms of inflammatory and pain response formation.

Full Text

Restricted Access

About the authors

Elena Yurievna Bystrova

Pavlov Institute of Physiology

Email: helenbys@yandex.ru
senior researcher

Kristina Alekseevna Dvornikova

Pavlov Institute of Physiology

Email: 691442@gmail.com
junior researcher

Olga Nikolaevna Platonova

Pavlov Institute of Physiology

Email: olgaplatonova1991@mail.ru
junior researcher

Alexander Danilovich Nozdrachev

Pavlov Institute of Physiology; Saint-Petersburg State University

Email: a.d.nozdrachev@mail.ru
Head of Laboratory, professor.

References

  1. Jutel M., Akdis M., Akdis C.A. Histamine, histamine receptors and their role in immune pathology. Clinical & Experimental Allergy 2009; 39: 1786-800. https://doi.org/10.1111/j.1365-2222.2009.03374.x
  2. Krylov B.V., Rogachevskii I.V., Shelykh T.N., Plakhova V.B. New non-opioid analgesics: understanding molecular mechanisms on the basis of patch-clamp and chemical studies. Bentham Science Publishers Ltd. 2017; 203. https://doi.org/10.2174/97816080593001170101
  3. Figueroa K., Shankley N. One hundred years of histamine research. In: Thurmond R.L. (eds) Histamine in Inflammation. Advances in Experimental Medicine and Biology. Springer, Boston, MA. 2010; 709: 1-9. https://doi.org/10.1007/978-1-4419-8056-4_1
  4. Haas H.L., Sergeeva O.A., Selbach O. Histamine in the nervous system. Physiol. Rev. 2008; 88: 1183-241. https://doi.org/10.1152/physrev.00043.2007
  5. Talreja J., Kabir M.H., Filla M.B., Stechschulte D.J., Dileepan K.N. Histamine induces Toll-like receptor 2 and 4 expression in endothelial cells and enhances sensitivity to Gram-positive and Gram-negative bacterial cell wall components. Immunology 2004; 113: 224-33. https://doi.org/10.1111/j.1365-2567.2004.01946.x
  6. Сепиашвили Р.И. Физиология иммунной системы. М.: Изд-во Медицина-Здоровье, 2015; 352. ISBN: 5-94255-004-2
  7. Li Y., Chi Y., Stechschulte D.J., Dileepan K.N. Histamine-induced production of IL-6 and IL-8 by human coronary artery endothelial cells is enhanced by endotoxin and TNF-a. Microvascular Res. 2001; 61: 253-62. https://doi.org/10.1006/mvre.2001.2304
  8. Ковальзон В.М. Роль гистаминергической системы головного мозга в регуляции цикла бодрствование-сон. Физиология человека. 2013; 39 (6): 13-23. https://doi.org/10.7868/S0131164613060088
  9. Varga C., Horvath K., Berko A., Thurmond R.L., Dunford P.J., Whittle B.J. Inhibitory effects of histamine H4 receptor antagonists on experimental colitis in the rat. Eur. J. Pharmacol. 2005; 522 (1-3): 130-8. https://doi.org/10.1016/j.ejphar.2005.08.045
  10. Cianchi F., Cortesini C., Schiavone N., Perna F., Magnelli L., Fanti E., Bani D., Messerini L., Fabbroni V., Perigli G., Capaccioli S., Masini E. The role of cyclooxygenase-2 in mediating the effects of histamine on cell proliferation and vascular endothelial growth factor production in colorectal cancer. Clin. Cancer Res. 2005; 11 (19): 6807-15. https://doi.org/10.1158/1078-0432.CCR-05-0675
  11. Maslinska D., Laure-Kamionowska M., Maslinski K.T., Deregowski K., Szewczyk G., Maslinski S. Histamine H4 receptors on mammary epithelial cells of the human breast with different types of carcinoma. Inflamm. Res. 2006; 55: 77-8. https://doi.org/10.1007/s00011-005-0051-z
  12. Ноздрачев А.Д., Пальцев М.А., Поляков Е.Л., Маслюков П.М., Чернышева М.П. Нобелевские лауреаты по физиологии или медицине. Санкт-Петербург: Изд-во Гуманистика, 2019; 884. ISBN: 978-5906140-30-2
  13. Akira S., Uematsu S., Takeuchi O. Pathogen recognition and innate immunity. Cell. 2006; 124 (4): 783-801. https://doi.org/10.1016/j.cell.2006.02.015
  14. Elson G., Dunn-Siegrist I., Daubeuf B., Pugin J. Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood. 2007; 109 (4): 1574-83. https://doi.org/10.1182/blood-2006-06-032961
  15. Furness J.B. Novel gut afferents: intrinsic afferent neurons and intestinofugal neurons. Auton. Neurosci. 2006; 125 (1-2): 81-5. https://doi.org/10.1016/j.autneu.2006.01.007
  16. Buchholz B.M., Bauer A.J. Membrane TLR signaling mechanisms in the gastrointestinal tract during sepsis. Neurogastroenterol. Mot. 2010; 22 (3): 232-45. https://doi.org/10.1111/j.1365-2982.2009.01464.x
  17. Kumagai Y., Takeuchi O., Akira S. Pathogen recognition by innate receptors. J. Infect. Chemother. 2008; 14 (2): 86-92. https://doi.org/10.1007/s10156-008-0596-1
  18. Randhawa A.K., Hawn T.R. Toll-like receptors: their roles in bacterial recognition and respiratory infections. Expert Rev. Anti. Infect. Ther. 2008; 6 (4): 479-95. https://doi.org/10.1586/14787210.6.4.479
  19. Barajon I., Serrao G., Arnaboldi F., Opizzi E., Ripamonti G., Balsari A., Rumio C. Toll-like receptors 3, 4, and 7 are expressed in the enteric nervous system and dorsal root ganglia. J. Histochem. Cytochem. 2009 57 (11): 1013-23. https://doi.org/10.1369/jhc.2009.953539
  20. Филиппова Л.В., Малышев Ф.С., Быкова А.А., Ноздрачев А.Д. Экспрессия Толл-подобных рецепторов 4 в нервных сплетениях двенадцатиперстной, тощей и ободочной кишки крысы. Доклады Академии наук. 2012; 445 (3): 353-5. https://doi.org/10.1134/S0012496612040114
  21. Филиппова Л.В., Быстрова Е.Ю., Малышев Ф.С., Шпанская А.А., Ноздрачев А.Д. Особенности локализации паттерн-распознающих и ванилоидных рецепторов в нервных сплетениях кишки крысы. Доклады Академии Наук. 2013; 452 (3): 342-5. https://doi.org/10.1134/S0012496613050074
  22. Wadachi R., Hargreaves K.M. Trigeminal nociceptors express TLR-4 and CD14: a mechanism for pain due to infection. J. Dent. Res. 2006; 85 (1): 49-53. https://doi.org/10.1177/154405910608500108
  23. Levine J.D., Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim. Biophys. Acta. 2007; 1772 (8): 989-1003. https://doi.org/10.1016/j.bbadis.2007.01.008
  24. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 1997; 389 (6653): 816-24. https://doi.org/10.1038/39807
  25. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 1998; 21 (3): 531-43. https://doi.org/10.1016/s0896-6273(00)80564-4
  26. Xu H., Blair N.T., Clapham D.E. Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J. Neurosci. 2005; 25 (39): 8924-37. https://doi.org/10.1523/JNEURO-SCI.2574-05.2005
  27. Macpherson L.J., Geierstanger B.H., Viswanath V, Bandell M., Eid S.R., Hwang S., Patapoutian A. The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr. Biol. 2005; 15 (10): 929-34. https://doi.org/10.10Wj.cub.2005.04.018
  28. Yoshida T., Inoue R., Morii T., Takahashi N., Yamamoto S., Hara Y., Tominaga M., Shimizu S., Sato Y., Mori Y. Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nature Chemical Biology 2006; 2: 596-607. https://doi.org/10.1038/nchembio821
  29. Гладких Ф.В. Характеристика механизмов антиульцерогенного действия агонистов ванилоидных рецепторов (TRPV1) на модели гастропатии, индуцированной ацетилсалициловой кислотой. Фармация и фармакология. 2017; 5 (3): 283-301. https://doi.org/10.19163/2307-9266-2017-5-3-283-301
  30. Holzer P. Transient receptor potential (TRP) channels as drug targets for diseases of the digestive system. Pharmacol. Ther. 2011; 131 (1): 142-70. https://doi.org/10.10Wj.pharmthera.2011.03.006
  31. Lapointe T.K., Basso L., Iftinca M.C., Flynn R., Chapman K., Dietrich G., Vergnolle N., Altier C. TRPV1 sensitization mediates postinflammatory visceral pain following acute colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2015; 309 (2): 87-99. https://doi.org/10.1152/ajpgi.00421.2014
  32. Филиппова Л.В., Быстрова Е.Ю., Малышев Ф.С., Платонова О.Н., Ноздрачев А.Д. Экспрессия паттерн-распознающих рецепторов ноцицептивными метасимпатическими нейронами. Бюллетень экспериментальной биологии и медицины. 2015; 159 (2): 209-13. https://doi.org/10.1007/s10517-015-2934-5
  33. Филиппова Л.В., Федорова А.В., Ноздрачев А.Д. Механизм активации энтеральных ноцицептивных нейронов посредством взаимодействия рецепторов TLR4 и TRPV1. Доклады Академии Наук. 2018; 479 (1): 99-102. htt-ps://doi.org/10.7868/S0869565218010243
  34. Ноздрачев А.Д. Полимодальная интероцептивная сенсорная система. Тез. докл. Всероссийской конференции с международным участием «Интегративная физиология». СПб, Институт физиологии им. И.П. Павлова РАН. 2019; 183-6. ISBN: 978-5-6042983-9-8 (Nozdrachev A.D. Polymodal interoceptive sensory system. Abstracts National conference with international participation «Integrative physiology». Saint-Petersburg, Pavlov Institute of Physiology. 2019; 183-6. ISBN: 978-5-6042983-9-8 (in Russian)]
  35. Hou Y.F., Zhou Y.C., Zheng X.X., Wang H.Y., Fu Y.L., Fang Z.M., He S.H. Modulation of expression and function of Toll-like receptor 3 in A549 and H292 cells by histamine. Molecular Immunology. 2006; 43: 1982-92. https://doi.org/10.1016/j.molimm.2005.11.013
  36. Gutierrez-Venegas G., Cruz-Arrieta S., Ville-da-Navarro M., Mendez-Mejia J.A. Histamine promotes the expression of receptors TLR2 and TLR4 and amplifies sensitivity to lipopolysaccharide and lipoteichoic acid treatment in human gingival fibroblasts. Cell. Biol. Int. 2011; 35 (10): 1009-17. https://doi.org/10.1042/CBI20100624
  37. Aldinucci A., Bonechi E., Manuelli C., Nosi D., Masini E., Passani M.B., Ballerini C. Histamine regulates actin cytoskeleton in human Toll-like receptor 4-activated monocyte-derived dendritic cells tuning CD4+ T lymphocyte response. The J. of Biological Chemistry. 2016; 291 (28): 14803-14. https://doi.org/10.1074/jbc.M116.720680
  38. Frei R., Ferstl R., Konieczna P., Ziegler M., Simon T, Rugeles T.M., Mailand S., Watanabe T, Lauener R., Akdis C.A., O'Mahony L. Histamine receptor 2 modifies dendritic cell responses to microbial ligands. J. Allergy Clin. Immunol. 2013; 132 (1): 194-204. https://doi.org/10.10Wj.jaci.2013.01.013
  39. Dommisch H., Chung W.O., Pl tz S., Jepsen S. Influence of histamine on the expression of CCL20 in human gingival fibroblasts. J. of Periodontal Research. 2015; 50 (6): 786-92. https://doi.org/10.1111/jre.12265
  40. Stefani C.B., de Oliveira R.M., Silveira A.A.A., Ferraz L.F.C., Ribeiro M.L., Gambero A., Pedrazzoli J. Expression of Toll-like receptors in enterocromaffin-like cells and their function in histamine release. Dig. Dis. Sci. 2012; 57: 2270-7. https://doi.org/10.1007/s10620-012-2176-6
  41. Smuda C., Wechsler J.B., Bryce P.J. TLR-induced activation of neutrophils promotes histamine production via a PI3 kinase dependent mechanism. Immunol. Lett. 2011; 141 (1): 102-8. https://doi.org/10.10Wj.imlet.2011.08.002
  42. Raveendran V.V., Tan X., Sweeney M.E., Levant B., Slusser J., Stechschulte D.J., Dileepan K.N. Lipopolysaccharide induces H1 receptor expression and enhances histamine responsiveness in human coronary artery endothelial cells. Immunology. 2011; 132: 578-88. https://doi.org/10.111Vj.1365-2567.2010.03403.x
  43. Deiteren A., De Man J.G., Ruyssers N.E., Moreels T.G., Pelckmans P.A., De Winter B.Y Histamine H4 and H1 receptors contribute to postinflammatory visceral hypersensitivity. Gut. 2014; 63 (12): 1873-82. https://doi.org/10.1136/gutjnl-2013-305870
  44. Kajihara Y, Murakami M., Imagawa T., Otsuguro K., Ito S., Ohta T. Histamine potentiates acid-induced responses mediating transient receptor potential V1 in mouse primary sensory neurons. Neuroscience. 2010; 166 (1): 292-304. https://doi.org/10.10Wj.neuroscience.2009.12.001
  45. Cenac N., Altier C., Motta J.P., dAldebert E., Galeano S., Zamponi G.W., Vergnolle N. Potentiation of TRPV4 signalling by histamine and serotonin: an important mechanism for visceral hypersensitivity. Gut. 2010; 59 (4): 481-8. https://doi.org/10.1136/gut.2009.192567
  46. Wouters M.M., Balemans D., Van Wanrooy S., Dooley J., Cibert-Goton V, Alpizar Y.A., Valdez-Morales E.E., Nasser Y, Van Veldhoven P.P., Vanbrabant W, Van der Merwe S., Mols R., Ghesquiere B., Cirillo C., Kortekaas I., Peter Carmeliet P., Willy E. Peetermans WE., Vermeire S., Rutgeerts P., Augustijns P., Hellings P.W., Belmans A., Vanner S., Bulmer D.C., Talavera K., Berghe P.V., Liston A., Boeckxstaens G.E. Histamine receptor H1-mediated sensitization of TRPV1 mediates visceral hypersensitivity and symptoms in patients with irritable bowel syndrome. Gastroenterology 2016; 150 (4): 875-87. https://doi.org/10.1053/j.gastro.2015.12.034
  47. Nam Y., Min Y.S., Sohn U.D. Recent advances in pharmacological research on the management of irritable bowel syndrome. Arch. Pharm. Res. 2018; 41: 955-66. https://doi.org/10.1007/s12272-018-1068-5
  48. Min H., Lee H., Lim H., , Yong Ho Jang YH., Chung S.J., C Justin Lee C.J., Lee S.J. TLR4 enhances histamine-mediated pruritus by potentiating TRPV1 activity. Mol. Brain. 2014; 7 (59): 1-10. https://doi.org/10.1186/s13041-014-0059-9
  49. Min H., Cho W.H., Lee H., Choi B., Kim Y.J., Lee H.K., Joo Y, Jung S.J., Choi S.Y, Lee S., Lee S.J. Association of TRPV1 and TLR4 through the TIR domain potentiates TRPV1 activity by blocking activation-induced desensitization. Mol. Pain. 2018; 14: 1-10. https://doi.org/10.1177/1744806918812636
  50. Liu T, Ji R.R. New insights into the mechanisms of itch: are pain and itch controlled by distinct mechanisms? Pflugers Arch. 2013; 465 (12): 1671-85. https://doi.org/10.1007/s00424-013-1284-2

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies