Molecular mechanisms of neuroinflammation initiation and development in a model of post-traumatic stress disorder

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Abstract

Neuroinflammation causes morphological and functional changes in the nervous tissue and it can be triggered by different kind of stressors. Progress of neuroinflammation as a result of post-traumatic stress disorder (PTSD) is associated with morphological changes in neurons and glial cells, as well as activation of microglia, however the exact molecular mechanisms of these changes are still unknown. In this review we discuss the connections between endocrine, immune and limbic systems during stress, the contributions of each system, the role of blood-brain barrier, as well as current methods and approaches in studying neuroinflammation.

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About the authors

O. P Tuchina

School of Life Sciences, Immanuel Kant Baltic Federal University

Email: otuchina@kantiana.ru

M. V Sidorova

School of Life Sciences, Immanuel Kant Baltic Federal University

A. V Turkin

School of Life Sciences, Immanuel Kant Baltic Federal University

D. A Shvaiko

School of Life Sciences, Immanuel Kant Baltic Federal University

I. G Shalaginova

School of Life Sciences, Immanuel Kant Baltic Federal University

I. A Vakolyuk

School of Life Sciences, Immanuel Kant Baltic Federal University

References

  1. The National Center for Health Statistics [US] International Statistical Classification of Diseases and Related Health Problems 10th Revision (ICD-10), 2010, http://apps.who.int/classifications/icd10/ browse/2010/en.
  2. Tovote P., Fadok J.P., Lüthi A. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 2015; 16: 317-31.
  3. Domingos da Silveira da Luz A.C., Dias G.P., Nascimento Bevilaqua M.C. et al. Translational findings on brain-derived neurotrophic factor and anxiety: contributions from basic research to clinical practice. Neuropsychobiology 2013; 68: 129-38.
  4. Matar M.A., Zohar J., Cohen H. Translationally relevant modeling of PTSD in rodents. Cell Tissue Res. 2013; 354: 127-39.
  5. Wohleb E.S., McKim D.B., Shea D.T. et al. Re-establishment of anxiety in stress-sensitized mice is caused by monocyte trafficking from the spleen to the brain. Biol. Psychiatry 2014; 75: 970-81.
  6. Deslauriers J., Powell S., Risbrough V.B. Immune signaling mechanisms of PTSD risk and symptom development: insights from animal models. Curr. Opin. Behav. Sci. 2017; 14: 123-32.
  7. Eraly S.A., Nievergelt C.M., Maihofer A.X. et al. Assessment of plasma C-reactive protein as a biomarker of posttraumatic stress disorder risk. JAMA Psychiatry 2014; 71: 423.
  8. van Zuiden M., Heijnen C.J., Maas M. et al. Glucocorticoid sensitivity of leukocytes predicts PTSD, depressive and fatigue symptoms after military deployment: a prospective study. Psychoneuroendocrinology 2012; 37: 1822-36.
  9. Jin J., Maren S. Fear renewal preferentially activates ventral hippocampal neurons projecting to both amygdala and prefrontal cortex in rats. Sci. Rep. 2015; 5: 8388.
  10. Godsil B.P., Kiss J.P., Spedding M. et al. The hippocampal-prefrontal pathway: the weak link in psychiatric disorders? Eur. J. Psychotraumatol. 2013; 23: 1165-81.
  11. Adhikari A., Topiwala M.A., Gordon J.A. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2009; 65: 257-69.
  12. Mendez-Davida I., Hen R., Gardiera A.M. et al. Adult hippocampal neurogenesis: An actor in the antidepressant-like action. Ann. Pharm. Fr. 2013; 71: 143-9.
  13. Calcia M.A., Bonsall D.R., Bloomfield P.S. et al. Stress and neuroinflammation: a systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology 2016; 233: 1637-50.
  14. Maier S.F. Bi-directional immune-brain communication: Implications for understanding stress, pain, and cognition. Brain, Behav. Immun. 2003; 17: 69-85.
  15. Jones K.A., Thomsen C. The role of the innate immune system in psychiatric disorders. Mol. Cell. Neurosci. 2013; 53: 52-62.
  16. Hou R., Baldwin D.S. A neuroimmunological perspective on anxiety disorders. Hum. Psychopharmacol. 2012; 27: 6-14.
  17. Miller A.H., Haroon E., Raison C.L. et al. Cytokine targets in the brain: impact on neurotransmitters and neurocircuits. Depress. Anxiety 2013; 30(4): 297-306.
  18. Erta M., Quintana A., Hidalgo J. Interleukin-6, a major cytokine in the central nervous system. Int. J. Biol. Sci. 2012; 8: 1254-66.
  19. Müller N., Manfred A. Psychoneuroimmunology and the cytokine action in the CNS: implications for psychiatric disorders. Prog. Neuropsychopharmacol. Biol. Psychiatry 1998; 22: l-33.
  20. Garay P.A., McAllister A.K. Novel roles for immune molecules in neural development: implications for neurodevelopmental disorders. Front. Synaptic Neurosci. 2010; 2: 136.
  21. Gola H., Engler H., Sommershof A. et al. Posttraumatic stress disorder is associated with an enhanced spontaneous production of pro-inflammatory cytokines by peripheral blood mononuclear cells. BMC Psychiatry 2013; 13: 40.
  22. Simen В.В., Duman C.H., Simen A.A. et al. TNFa signaling in depression and anxiety: behavioral consequences of individual receptor targeting. Biol. Psychiatry 2006; 59: 775-85.
  23. Andrews J.A., Neises K.D. Cells, biomarkers, and post-traumatic stress disorder: evidence for peripheral involvement in a central disease. J. Neurochem. 2012; 120: 26-36.
  24. Ajmo C.T. Jr., Vernon D.O., Collier L. et al. The spleen contributes to stroke-induced neurodegeneration. J. Neurosci. Res. 2008; 86: 2227-34.
  25. Lewitus G.M., Cohen H., Schwartz M. Reducing posttraumatic anxiety by immunization. Brain, Behav. Immun. 2008; 22: 1108-14.
  26. Haas H.S., Schauenstein K. Neuroimmunomodulation via limbic structures - the neuroanatomy of psychoimmunology. Prog. Neurobiol. 1997; 51: 195-222.
  27. Capuron L., Miller A.H. Immune system to brain signaling: neuropsychopharmacological implications. Pharmacol. Ther. 2011; 130: 226-38.
  28. Kheirbek M.A., Klemenhagen K.C., Sahay A. et al. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat. Neurosci. 2012; 15: 1613-20.
  29. Griffin G.D., Charron D., Al-Daccak R. Post-traumatic stress disorder: revisiting adrenergics, glucocorticoids, immune system effects and homeostasis. Clin. Transl. Immunology 2014; 3(11): e27.
  30. Умрюхин А.Е. Нейромедиаторные гиппокампальные механизмы стрессорного поведения и реакций избегания. Вестник новых медицинских технологий 2013; 1.
  31. Herman J.P. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog. Neuropsychopharmacol. Biol. Psychiatry 2005; 29: 1201-13.
  32. Fanselow M.S. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 2010; 65: 7-19.
  33. Nicholson L.B. The immune system. Essays Biochem. 2016; 60: 275-301.
  34. Morganti-Kossmann M.C., Rancan M., Stahel P.F. et al. Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 2002; 8: 101-5.
  35. Iłżecka J. The structure and function of blood-brain barrier in ischaemic brain stroke process. Ann. Univ. Mariae Curie Sklodowska Med. 1996; Section D: Medicina; 51: 123-7.
  36. Papadopoulos M.C., Lamb F.J., Moss R.F. et al. Faecal peritonitis causes oedema and neuronal injury in pig cerebral cortex. Clin. Sci. 1999; 96(5): 461-6.
  37. Varatharaj A., Galea I. The blood-brain barrier in systemic inflammation. Brain, Behav. Immun. 2017; 60: 1-12.
  38. Ericsson A., Liu C., Hart R.P. et al. Type 1 interleukin-1 receptor in the rat brain: distribution, regulation, and relationship to sites of IL-1-in-duced cellular activation. J. Comp. Neurol. 1995; 361(4): 681-98.
  39. Chaouloff F. Serotonin, stress and corticoids. J. Psychopharmacol. 2000; 14: 139-51.
  40. Ganong W.F. Circumventricular organs: definition and role in the regulation of endocrine and autonomic function. Clin. Exp. Pharmacol. Physiol. 2000; 27: 422-7.
  41. Cottrell G.T., Ferguson A.V. Sensory circumventricular organs: Central roles in integrated autonomic regulation. Regul. Pept. 2004; 117: 11-23.
  42. Joly J.S., Osório J., Alunni A. et al. Windows of the brain: towards a developmental biology of circumventricular and other neurohemal organs. Seminars in cell & developmental biology 2007; 18(4): 512-24.
  43. Agrawal S., Anderson P., Durbeej M. et al. Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J. Exp. Med. 2006; 203(4): 1007-19.
  44. Bush T.G., Puvanachandra N., Horner C.H. et al. Leukocyte infiltration, neuronal degeneration, and neurite outgrowth after ablation of scar-forming, reactive astrocytes in adult transgenic mice. Neuron 1999; 23(2): 297-308.
  45. Esposito P., Gheorghe D., Kandere K. et al. Acute stress increases permeability of the blood-brain-barrier through activation of brain mast cells. Brain Res. 2001; 888(1): 117-27.
  46. Roszkowski M., Bohacek J. Stress does not increase blood-brain barrier permeability in mice. J. Cereb. Blood Flow Metab. 2016; 36(7): 1304-15.
  47. Frank M., Weber M.D., Watkins L.R. et al. Stress-induced neuroinflammatory priming: A liability factor in the etiology of psychiatric disorders. Neurobiol. Stress 2016; 4: 62-70.
  48. Wohleb E.S., McKim D.B., Sheridan J.F. et al. Monocyte trafficking to the brain with stress and inflammation: a novel axis of immune-to-brain communication that influences mood and behavior. Front. Neurosci. 2015; 8: 447.
  49. Herbert J., Goodyer I.M., Grossman A.B. et al. Do corticosteroids damage the brain? J. Neuroendocrinol. 2006; 18: 393-411.
  50. Heegde F., De Rijk R.H., Vinkers C. The brain mineralocorticoid receptor and stress resilience. Psychoneuroendocrinology 2015; 52: 92-110.
  51. Walker F.R., Yirmiya R. Microglia, Physiology and Behavior: A Brief Commentary. Brain Behav. Immun. 2016; 55: 1-5.
  52. Pavlov V., Tracey K. The vagus nerve and the inflammatory reflex-linking immunity and metabolism. Nat. Rev. Endocrinol. 2012; 8: 743-54.
  53. Olshansky В. Vagus nerve modulation of inflammation: Cardiovascular implications. Trends Cardiovasc. Med. 2016; 26: 1-11.
  54. Ek M., Kurosawa M., Lundeberg T. et al. Activation of vagal afferents after intravenous injection of interleukin-1beta: role of endogenous prostaglandins. J. Neurosci. 1998; 18: 9471-9.
  55. Hosoi T., Okuma Y., Matsuda T. et al. Novel pathway for LPS-induced afferent vagus nerve activation: possible role of nodose ganglion. Auton. Neurosci. 2005; 120: 104-7.
  56. Borovikova L.V., Ivanova S., Zhang M. et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000; 405: 458-62.
  57. Wang H., Yu M., Ochani M. et al. Nicotinic acetylcholine receptor a7 subunit is an essential regulator of inflammation. Nature 2003; 421: 384-8.
  58. Gallowitsch-Puerta M., Pavlov V.A. Neuro-immune interactions via the cholinergic anti-inflammatory pathway. Life Sciences 2007; 80: 2325-9.
  59. Hamano R., Takahashi H.K., Iwagaki H. et al. Stimulation of a7 nicotinic acetylcholine receptor inhibits CD14 and the toll-like receptor 4 expression in human monocytes. Shock 2006; 26: 358-64.
  60. Rosas-Ballina M., Ochani M., Parrish W.R. et al. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. PNAS USA 2008; 105: 11008-13.
  61. Hamilton N.B., Attwell D. Do astrocytes really exocytose neurotransmitters? Nat. Rev. Neurosci. 2010; 11: 227-38.
  62. Hertz L., Zielke H.R. Astrocytic control of glutamatergic activity: astrocytes as stars of the show. Trends Neurosci. 2004; 27: 735-43.
  63. Kettenmann H., Hanisch U.K., Noda M. et al. Physiology of microglia. Physiol. Rev. 2011; 91: 461-553.
  64. Wake H., Moorhouse A.J., Jinno S. et al. Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 2009; 29: 3974-80.
  65. Chaouloff F. Serotonin, stress and corticoids. J. Psychopharmacol. 2000; 14: 139-51.
  66. Curzon G., Joseph M.H., Knott P.J. Effects of immobilization and food deprivation on rat brain tryptophan metabolism. J. Neurochem. 1972; 19: 1967-74.
  67. Neckers L., Sze P.Y. Regulation of 5-hydroxytryptamine metabolism in mouse brain by adrenal glucocorticoids. Brain Res. 1975; 93: 123-32.
  68. Dunn A.J., Welch J. Stress and endotoxin induced increases in brain tryptophan and serotonin metabolism depend on sympathetic nervous system activity. J. Neurochem. 1991; 57: 1615-22.
  69. Boadle-Biber M.C. Biosynthesis of serotonin. In: Osborne N.N., editor. Biology of Serotonergic Transmission. Chichester: John Wiley & Sons; 1982. p. 63-87.
  70. Green R.A. Neuropharmacology of 5-hydroxytryptamine. Br. J. Pharmacol. 2006; 147: 145-52.
  71. Dahlström A., Fuxe K. Localization of monoamines in the lower brain stem. Experientia 1964; 20: 398-9.
  72. Törk I. Anatomy of the serotonergic system. Ann. N.Y. Acad. Sci. 1990; 600: 9-34.
  73. Risch S.C., Nemeroff C.B. Neurochemical alterations of serotonergic neuronal systems in depression. J. Clin. Psychiatry 1992; 53: 3-7.
  74. Temel Y., Boothman L.J., Blokland A. et al. Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. PNAS USA 2007; 43: 17087-92.
  75. Graeff F.G. Role of 5-HT in defensive behavior and anxiety. Rev. Neurosci. 1993; 4: 181-212.
  76. Umbriaco D., Garcia S., Beaulieu C. et al. Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 1995; 5(6): 605-20.
  77. Bunin M.A., Wightman R.M. Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J. Neurosci. 1998; 18(13): 4854-60.
  78. Zoli M., Jansson A., Sykovâ E. et al. Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol. Sci. 1999; 20(4): 142-50.
  79. Jacobs B.L., Azmitia E.C. Structure and function of the brain serotonin system. Physiol. Rev. 1992; 72(1): 165-229.
  80. Peyron C., Petit J.M., Rampon C. et al. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neurosci. 1997; 82; 443-68.
  81. Mahe C., Loetscher E., Dev K.K. et al. Serotonin 5-HT 7 receptors coupled to induction of interleukin-6 in human microglial MC-3 cells. Neuropharmacology 2005; 49: 40-7.
  82. Kolodzie czak M., Béchade C., Gervasi N. et al. Serotonin modulates developmental microglia via 5-HT2B receptors: potential implication during synaptic refinement of retinogeniculate projections. ACS Chem. Neurosci. 2015; 6: 1219-30.
  83. MacGillivray L., Reynolds K.B., Sickand M. et al. Inhibition of the serotonin transporter induces microglial activation and downregulation of dopaminergic neurons in the substantia nigra. Synapse 2011; 65(11): 1166-72.
  84. de las Casas-Engel M., Dominguez-Soto A., Sierra-Filardi E. et al. Serotonin skews human macrophage polarization through HTR2B and HTR7. J. Immunol. 2013; 190(5): 2301-10.
  85. Hayley S., Merali Z., Anisman H. Stress and cytokine-elicited neuroendocrine and neurotransmitter sensitization: implications for depressive illness. Stress 2003; 6: 19-32.
  86. Bertrand J., José L.V. A brief overview of multitalanted microglia. In: Bertrand J., José L.V., editors. Microglia: Methods and Protocols. New York: Humana Press Inc; 2013. p. 3-8.
  87. Burrell R. Immunomodulation by bacterial endotoxin. Crit. Rev. Microbiol. 1990; 17: 189-208.
  88. Montero-Menei C.N., Sindji L., Garcion E. et al. Early events of the inflammatory reaction induced in rat brain by lipopolysaccharide intracerebral injection: relative contribution of peripheral monocytes and activated microglia. Brain Res. 1996; 724: 55-66.
  89. Pugh C.R., Kumagawa K., Fleshner M. et al. Selective effects of peripheral lipopolysaccharide administration on contextual and auditory-cue fear conditioning. Brain, Behav. Immun. 1998; 12: 212-29.
  90. Swiergiel A.H., Dunn A.J. Effects of interleukin-1beta and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol. Biochem. Behav. 2007; 86: 651-9.
  91. Silverman M.N., Macdougall M.G., Hu F. et al. Endogenous glucocorticoids protect against TNF-alpha-induced increases in anxiety-like behavior in virally infected mice. Mol. Psychiatry 2007; 12: 408-17.
  92. Koo J.W., Duman R.S. Interleukin-1 receptor null mutant mice show decreased anxiety-like behavior and enhanced fear memory. Neurosci. Lett. 2009; 456: 39-43.
  93. Murray C.L., Obiang P., Bannerman D. et al. Endogenous IL-1 in Cognitive Function and Anxiety: A Study in IL-1RI2/2 Mice. PLoS One 2013; 8: 10.
  94. Muhie S., Gautam A., Chakraborty N. et al. Molecular indicators of stress-induced neuroinflammation in a mouse model simulating features of post-traumatic stress disorder. Transl. Psychiatry 2017; 7: 5.
  95. Pulli B., Chen J.W. Imaging Neuroinflammation - from Bench to Bedside. J. Clin. Cell. Immunol. 2014; 5: 226.
  96. Cho W., Barcelon E., Lee S. Optogenetic Glia Manipulation: Possibilities and Future Prospects. Exp. Neurobiol. 2016; 25: 197-204.
  97. Almli L.M., Fani N., Smith A.K. et al. Genetic approaches to understanding post-traumatic stress disorder. Int. J. Neuropsychopharmacol. 2014; 17(2): 355-70.
  98. Breen M., Maihofer A., Glatt S. et al. Gene networks specific for innate immunity define post-traumatic stress disorder. Mol. Psychiatr. 2015; 20: 1538-45.
  99. Uddin M., Aiello A.E., Wildman D.E. et al. Epigenetic and immune function profiles associated with posttraumatic stress disorder. PNAS USA 2010; 107: 9470-5.
  100. Rusiecki J., Byrne C., Galdzicki Z. et al. PTSD and DNA methylation in select immune function gene promoter regions: a repeated measures case-control study of U.S. military service members. Front. in Psychiatry 2013; 4: 56.
  101. Albrecht D., Granziera C., Hooker J. et al. In vivo imaging of human neuroinflammation. ACS Chem. Neurosci. 2016; 7: 470-83.
  102. De Lange G.M. Understanding the cellular and molecular alterations in PTSD brains: The necessity of post-mortem brain tissue. Eur. J. Psychotraumatol. 2017; 8: 1.

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