Effects of Emotional Stress on Astrocytes and Their Implications in Stress-Related Disorders

  • Christian Luis Bender
  • Gastón Diego Calfa
  • Víctor Alejandro Molina
Chapter

Abstract

Stress is a major risk factor in the etiology of several psychiatric diseases, such as anxiety disorders and depression. On the other hand, a growing body of evidence has demonstrated that astrocytes play a pivotal role in the normal functioning of the nervous system. Hence, understanding the effects of stress on astrocytes is crucial for a better comprehension of stress-related mental disorders. Here, we describe the evidence showing astrocyte changes induced by stress in animals and how this plasticity could operate to induce behavioral sequelae. In addition, human data linking astrocytes with psychiatric disorders related to stress are also discussed. Altogether, the data indicate that both chronic and acute stressors are capable of changing the morphology and function of astrocytes in the brain areas that are known to play a critical role in emotional processing, such as the prefrontal cortex, hippocampus, and amygdala. Furthermore, different lines of evidence suggest that astrocyte plasticity may contribute to the behavioral consequences of stress.

Keywords

Astrocytes Chronic stress Acute stress Plasticity Anxiety Depression 

Abbreviations

AQP4

Aquaporin 4

ATP

Adenosine triphosphate

CUS

Chronic unpredictable stress

Cx43

Connexin 43

FGF2

Astrocytic fibroblast growth factor

GABA

Gamma aminobutyric acid

GFAP

Glial fibrillary acidic protein

GLAST

Glutamate aspartate transporter, also known as excitatory amino acid transporter 1 (EAAT1)

GLT-1

Glutamate transporter-1, also known as excitatory amino acid transporter 2 (EAAT2)

GS

Glutamine synthetase

IP3

Inositol triphosphate receptors

S100β

Calcium-binding protein β

Notes

Acknowledgments

This research was supported by grants from MinCyT-Cordoba, SECYT-UNC, CONICET, and Agencia Nacional de Promoción Científica y Tecnológica–FONCYT (Argentina) to Victor A Molina and SECYT-UNC, CONICET, and Agencia Nacional de Promoción Científica y Tecnológica–FONCYT (Argentina) to Gaston Calfa.

References

  1. 1.
    Christoffel DJ, Golden SA, Russo SJ. Structural and synaptic plasticity in stress-related disorders. Rev Neurosci. 2011;22(5):535–49.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Davidson RJ, McEwen BS. Social influences on neuroplasticity: stress and interventions to promote well-being. Nat Neurosci. 2012;15(5):689–95.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Giachero M, Calfa GD, Molina VA. Hippocampal structural plasticity accompanies the resulting contextual fear memory following stress and fear conditioning. Learn Mem. 2013;20(11):611–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci U S A. 2005;102(26):9371–6.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Martijena ID, Molina VA. The influence of stress on fear memory processes. Braz J Med Biol Res. 2012;45(4):308–13.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Etkin A, Wager TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry. 2007;164(10):1476–88.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Hilgetag CC, Barbas H. Are there ten times more glia than neurons in the brain? Brain Struct Funct. 2009;213(4–5):365–6.PubMedCrossRefGoogle Scholar
  8. 8.
    Herculano-Houzel S. The glia/neuron ratio: how it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia. 2014;62(9):1377–91.PubMedCrossRefGoogle Scholar
  9. 9.
    Araque A, Parpura V, Sanzgiri RP, Haydon PG. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999;22(5):208–15.PubMedCrossRefGoogle Scholar
  10. 10.
    Walker FR, Nilsson M, Jones K. Acute and chronic stress-induced disturbances of microglial plasticity, phenotype and function. Curr Drug Targets. 2013;14(11):1262–76.PubMedCrossRefGoogle Scholar
  11. 11.
    Delpech JC, Madore C, Nadjar A, Joffre C, Wohleb ES, Layé S. Microglia in neuronal plasticity: influence of stress. Neuropharmacol. 2015;96(Pt A):19–28.CrossRefGoogle Scholar
  12. 12.
    Edgar N, Sibille E. A putative functional role for oligodendrocytes in mood regulation. Transl Psychiatry. 2012;2:e109.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010;119(1):7–35.PubMedCrossRefGoogle Scholar
  14. 14.
    Middeldorp J, Hol EM. GFAP in health and disease. Prog Neurobiol. 2011;93(3):421–43.PubMedCrossRefGoogle Scholar
  15. 15.
    Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG. Synaptic islands defined by the territory of a single astrocyte. J Neurosci. 2007;27(24):6473–7.PubMedCrossRefGoogle Scholar
  16. 16.
    Ogata K, Kosaka T. Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience. 2002;113(1):221–33.PubMedCrossRefGoogle Scholar
  17. 17.
    Bernardinelli Y, Muller D, Nikonenko I. Astrocyte-synapse structural plasticity. Neural Plast. 2014;2014:232105.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Oberheim NA, Takano T, Han X, He W, Lin JH, Wang F, Xu Q, Wyatt JD, Pilcher W, Ojemann JG, Ransom BR, Goldman SA, Nedergaard M. Uniquely hominid features of adult human astrocytes. J Neurosci. 2009;29(10):3276–87.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Han X, Chen M, Wang F, Windrem M, Wang S, Shanz S, Xu Q, Oberheim NA, Bekar L, Betstadt S, Silva AJ, Takano T, Goldman SA, Nedergaard M. Forebrain engraftment by human glial progenitor cells enhances synaptic plasticity and learning in adult mice. Cell Stem Cell. 2013;12(3):342–53.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Barres BA. The mystery and magic of glia: a perspective on their roles in health and disease. Biol Psychiatry. 2008;64(10):863–70.CrossRefGoogle Scholar
  21. 21.
    Kimelberg HK. Functions of mature mammalian astrocytes: a current view. Neuroscientist. 2010;16(1):79–106.PubMedCrossRefGoogle Scholar
  22. 22.
    Perea G, Araque A. GLIA modulates synaptic transmission. Brain Res Rev. 2010;63(1–2):93–102.PubMedCrossRefGoogle Scholar
  23. 23.
    Haydon PG, Nedergaard M. How do astrocytes participate in neural plasticity? Cold Spring Harb Perspect Biol. 2014;7(3):a020438.Google Scholar
  24. 24.
    McEwen BS, Gianaros PJ. Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. Ann N Y Acad Sci. 2010;1186:190–222.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flügge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, Richter-Levin G, Sgoifo A, Steimer T, Stiedl O, van Dijk G, Wöhr M, Fuchs E. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev. 2011;35(5):1291–301.PubMedCrossRefGoogle Scholar
  26. 26.
    Franklin TB, Saab BJ, Mansuy IM. Neural mechanisms of stress resilience and vulnerability. Neuron. 2012;75(5):747–61.PubMedCrossRefGoogle Scholar
  27. 27.
    Shin LM, Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology. 2010;35(1):169–91.PubMedCrossRefGoogle Scholar
  28. 28.
    Guimaraes F, Joca SR, Padovani CM, Molina VA. Mood disorders. In: Neurobiology of mental disorders. Nova Science Publishers: New York, 2006, p. 95–124.Google Scholar
  29. 29.
    Edwards S, Baynes BB, Carmichael CY, Zamora-Martinez ER, Barrus M, Koob GF, Gilpin NW. Traumatic stress reactivity promotes excessive alcohol drinking and alters the balance of prefrontal cortex-amygdala activity. Transl Psychiatry. 2013;3:e296.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Papp M, Gruca P, Lason-Tyburkiewicz M, Litwa E, Willner P. Effects of chronic mild stress on the development of drug dependence in rats. Behav Pharmacol. 2014;25(5–6):518–31.PubMedGoogle Scholar
  31. 31.
    Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, Zohar J, Richter-Levin G, Cohen H. Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology. 2009;34(6):844–58.Google Scholar
  32. 32.
    Bignante A, Paglini G, Molina VA. Previous stress exposure enhances both anxiety-like behaviour and p 35 levels in the basolateral amygdala complex: modulation by midazolam. Eur Neuropsychopharmacol. 2010;20(6):388–97.PubMedCrossRefGoogle Scholar
  33. 33.
    Elizalde N, García-García AL, Totterdell S, Gendive N, Venzala E, Ramirez MJ, Del Rio J, Tordera RM. Sustained stress-induced changes in mice as a model for chronic depression. Psychopharmacology. 2010;210(3):393–406.PubMedCrossRefGoogle Scholar
  34. 34.
    Zhu S, Shi R, Wang J, Wang JF, Li XM. Unpredictable chronic mild stress not chronic restraint stress induces depressive behaviours in mice. Neuroreport. 2014;25(14):1151–5.PubMedCrossRefGoogle Scholar
  35. 35.
    Reichenbach A, Derouiche A, Kirchhoff F. Morphology and dynamics of perisynaptic glia. Brain Res Rev. 2010;63(1–2):11–25.PubMedCrossRefGoogle Scholar
  36. 36.
    Haber M, Zhou L, Murai KK. Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J Neurosci. 2006;26(35):8881–91.PubMedCrossRefGoogle Scholar
  37. 37.
    Rodnight RB, Gottfried C. Morphological plasticity of rodent astroglia. J Neurochem. 2013;124(3):263–75.PubMedCrossRefGoogle Scholar
  38. 38.
    Saab AS, Neumeyer A, Jahn HM, Cupido A, Šimek AA, Boele HJ, Scheller A, Le Meur K, Götz M, Monyer H, Sprengel R, Rubio ME, Deitmer JW, De Zeeuw CI, Kirchhoff F. Bergmann glial AMPA receptors are required for fine motor coordination. Science. 2012;337(6095):749–53.PubMedCrossRefGoogle Scholar
  39. 39.
    Theodosis DT, Poulain DA, Oliet SH. Activity-dependent structural and functional plasticity of astrocyte–neuron interactions. Physiol Rev. 2008;88(3):983–1008.PubMedCrossRefGoogle Scholar
  40. 40.
    Weinstein DE, Shelanski ML, Liem RK. Suppression by antisense mRNA demonstrates a requirement for the glial fibrillary acidic protein in the formation of stable astrocytic processes in response to neurons. J Cell Biol. 1991;112(6):1205–13.PubMedCrossRefGoogle Scholar
  41. 41.
    Hughes EG, Maguire JL, McMinn MT, Scholz RE, Sutherland ML. Loss of glial fibrillary acidic protein results in decreased glutamate transport and inhibition of PKA-induced EAAT2 cell surface trafficking. Brain Res Mol Brain Res. 2004;124(2):114–23.PubMedCrossRefGoogle Scholar
  42. 42.
    Czéh B, Simon M, Schmelting B, Hiemke C, Fuchs E. Astroglial plasticity in the hippocampus is affected by chronic psychosocial stress and concomitant fluoxetine treatment. Neuropsychopharmacology. 2006;31(8):1616–26.PubMedCrossRefGoogle Scholar
  43. 43.
    Tynan RJ, Beynon SB, Hinwood M, Johnson SJ, Nilsson M, Woods JJ. Walker FR Chronic stress-induced disruption of the astrocyte network is driven by structural atrophy and not loss of astrocytes. Acta Neuropathol. 2013;126(1):75–91.PubMedCrossRefGoogle Scholar
  44. 44.
    Banasr M, Duman RS. Glial loss in the prefrontal cortex is sufficient to induce depressive-like behaviors. Biol Psychiatry. 2008;64(10):863–70.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Liu Q, Li B, Zhu HY, Wang YQ, Yu J, Wu GC. Clomipramine treatment reversed the glial pathology in a chronic unpredictable stress-induced rat model of depression. Eur Neuropsychopharmacol. 2009;19(11):796–805.PubMedCrossRefGoogle Scholar
  46. 46.
    Liu Q, Li B, Zhu HY, Wang YQ, Yu J, Wu GC. Glia atrophy in the hippocampus of chronic unpredictable stress-induced depression model rats is reversed by electroacupuncture treatment. J Affect Disord. 2011;128(3):309–13.PubMedCrossRefGoogle Scholar
  47. 47.
    Ye Y, Wang G, Wang H, Wang X. Brain-derived neurotrophic factor (BDNF) infusion restored astrocytic plasticity in the hippocampus of a rat model of depression. Neurosci Lett. 2011;503(1):15–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Sun JD, Liu Y, Yuan YH, Li J, Chen NH. Gap junction dysfunction in the prefrontal cortex induces depressive-like behaviors in rats. Neuropsychopharmacology. 2012;37(5):1305–20.PubMedCrossRefGoogle Scholar
  49. 49.
    Li LF, Yang J, Ma SP, Qu R. Magnolol treatment reversed the glial pathology in an unpredictable chronic mild stress-induced rat model of depression. Eur J Pharmacol. 2013;711(1–3):42–9.PubMedGoogle Scholar
  50. 50.
    Gosselin RD, Gibney S, O’Malley D, Dinan TG, Cryan JF. Region specific decrease in glial fibrillary acidic protein immunoreactivity in the brain of a rat model of depression. Neuroscience. 2009;159(2):915–25.PubMedCrossRefGoogle Scholar
  51. 51.
    Kassem MS, Lagopoulos J, Stait-Gardner T, Price WS, Chohan TW, Arnold JC, Hatton SN, Bennett MR. Stress-induced grey matter loss determined by MRI is primarily due to loss of dendrites and their synapses. Mol Neurobiol. 2013;47(2):645–61.PubMedCrossRefGoogle Scholar
  52. 52.
    Araya-Callís C, Hiemke C, Abumaria N, Flugge G. Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus. Psychopharmacology. 2012;224(1):209–22.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Banasr M, Chowdhury GM, Terwilliger R, Newton SS, Duman RS, Behar KL, Sanacora G. Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry. 2010;15(5):501–11.PubMedCrossRefGoogle Scholar
  54. 54.
    Jang S, Suh SH, Yoo HS, Lee YM, Oh S. Changes in iNOS, GFAP and NR1 expression in various brain regions and elevation of sphingosine-1-phosphate in serum after immobilized stress. Neurochem Res. 2008;33(5):842–51.PubMedCrossRefGoogle Scholar
  55. 55.
    Kwon MS, Seo YJ, Lee JK, Lee HK, Jung JS, Jang JE, Park SH, Suh HW. The repeated immobilization stress increases IL-1beta immunoreactivities in only neuron, but not astrocyte or microglia in hippocampal CA1 region, striatum and paraventricular nucleus. Neurosci Lett. 2008;430(3):258–63.PubMedCrossRefGoogle Scholar
  56. 56.
    Imbe H, Kimura A, Donishi T, Kaneoke Y. Chronic restraint stress decreases glial fibrillary acidic protein and glutamate transporter in the periaqueductal gray matter. Neuroscience. 2012;223:209–18.PubMedCrossRefGoogle Scholar
  57. 57.
    Imbe H, Kimura A, Donishi T, Kaneoke Y. Effects of restraint stress on glial activity in the rostral ventromedial medulla. Neuroscience. 2013;241:10–21.PubMedCrossRefGoogle Scholar
  58. 58.
    Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I. S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta. 2009;1793(6):1008–22.PubMedCrossRefGoogle Scholar
  59. 59.
    Rong H, Wang G, Liu T, Wang H, Wan Q, Weng S. Chronic mild stress induces fluoxetine-reversible decreases in hippocampal and cerebrospinal fluid levels of the neurotrophic factor S100B and its specific receptor. Int J Mol Sci. 2010;11(12):5310–22.Google Scholar
  60. 60.
    Sugama S, Takenouchi T, Sekiyama K, Kitani H, Hashimoto M. Immunological responses of astroglia in the rat brain under acute stress: interleukin 1 beta co-localized in astroglia. Neuroscience. 2011;192:429–37.Google Scholar
  61. 61.
    Xia L, Zhai M, Wang L, Miao D, Zhu X, Wang W. FGF2 blocks PTSD symptoms via an astrocyte-based mechanism. Behav Brain Res. 2013;256:472–80.PubMedCrossRefGoogle Scholar
  62. 62.
    Margis R, Zanatto VC, Tramontina F, Vinade E, Lhullier F, Portela LV, Souza DO, Dalmaz C, Kapczinski F, Gonçalves CA. Changes in S100B cerebrospinal fluid levels of rats subjected to predator stress. Brain Res. 2004;1028(2):213–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Scaccianoce S, Del Bianco P, Pannitteri G, Passarelli F. Relationship between stress and circulating levels of S100B protein. Brain Res. 2004;1004(1–2):208–11.PubMedCrossRefGoogle Scholar
  64. 64.
    Kirby ED, Muroy SE, Sun WG, Covarrubias D, Leong MJ, Barchas LA, Kaufer D. Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2. Elife. 2013;2:e00362.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Ponomarev I, Rau V, Eger EI, Harris RA, Fanselow MS. Amygdala transcriptome and cellular mechanisms underlying stress-enhanced fear learning in a rat model of posttraumatic stress disorder. Neuropsychopharmacology. 2010;35(6):1402–11.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Daskalakis NP, Yehuda R, Diamond DM. Animal models in translational studies of PTSD. Psychoneuroendocrinology. 2013;38(9):1895–911.Google Scholar
  67. 67.
    Cao X, Li LP, Wang Q, Wu Q, Hu HH, Zhang M, Fang YY, Zhang J, Li SJ, Xiong WC, Yan HC, Gao YB, Liu JH, Li XW, Sun LR, Zeng YN, Zhu XH, Gao TM. Astrocyte-derived ATP modulates depressive-like behaviors. Nat Med. 2013;19(6):773–7.PubMedCrossRefGoogle Scholar
  68. 68.
    Domin H, Szewczyk B, Woźniak M, Wawrzak-Wleciał A, Śmiałowska M. Antidepressant-like effect of the mGluR5 antagonist MTEP in an astroglial degeneration model of depression. Behav Brain Res. 2014;273:23–33.PubMedCrossRefGoogle Scholar
  69. 69.
    Lee Y, Son H, Kim G, Kim S, Lee DH, Roh GS, Kang SS, Cho GJ, Choi WS, Kim HJ. Glutamine deficiency in the prefrontal cortex increases depressive-like behaviours in male mice. J Psychiatry Neurosci. 2013;38(3):183–91.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    John CS, Smith KL, Van’t Veer A, Gompf HS, Carlezon Jr WA, Cohen BM, Öngür D, Bechtholt-Gompf AJ. Blockade of astrocytic glutamate uptake in the prefrontal cortex induces anhedonia. Neuropsychopharmacology. 2012;37(11):2467–75.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Abu-Ghanem Y, Cohen H, Buskila Y, Grauer E, Amitai Y. Enhanced stress reactivity in nitric oxidesynthase type 2 mutant mice: findings in support of astrocytic nitrosative modulation of behavior. Neuroscience. 2008;156(2):257–65.PubMedCrossRefGoogle Scholar
  72. 72.
    Petravicz J, Boyt KM, McCarthy KD. Astrocyte IP3R2-dependent Ca(2+) signaling is not a major modulator of neuronal pathways governing behavior. Front Behav Neurosci. 2014;8:384.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Li D, Agulhon C, Schmidt E, Oheim M, Ropert N. New tools for investigating astrocyte-to-neuron communication. Front Cell Neurosci. 2013;7:193.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Tanaka M, Shih PY, Gomi H, Yoshida T, Nakai J, Ando R, Furuichi T, Mikoshiba K, Semyanov A, Itohara S. Astrocytic Ca2+ signals are required for the functional integrity of tripartite synapses. Mol Brain. 2013;6:6.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci. 2011;13(1):22–37.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Rodriguez Manzanares P, Nora I, Carrer H, Molina VA. Prior stress facilitates fear memory, attenuates GABAergic inhibition and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci. 2005;25(38):8725–34.PubMedCrossRefGoogle Scholar
  77. 77.
    Yoon BE, Lee CJ. GABA as a rising gliotransmitter. Front Neural Circuits. 2014;8:141.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Liu ZP, Song C, Wang M, He Y, Xu XB, Pan HQ, Chen WB, Peng WJ, Pan BX. Chronic stress impairs GABAergic control of amygdala through suppressing the tonic GABAA receptor currents. Mol Brain. 2014;7:32.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Christian CA, Huguenard JR. Astrocytes potentiate GABAergic transmission in the thalamic reticular nucleus via endozepine signaling. Proc Natl Acad Sci U S A. 2013;110(50):20278–83.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Farb CR, Chang W, Ledoux JE. Ultrastructural characterization of noradrenergic axons and Beta-adrenergic receptors in the lateral nucleus of the amygdala. Front Behav Neurosci. 2010;4:162.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Aoki C, Venkatesan C, Go CG, Forman R, Kurose H. Cellular and subcellular sites for noradrenergic action in the monkey dorsolateral prefrontal cortex as revealed by the immunocytochemical localization of noradrenergic receptors and axons. Cereb Cortex. 1998;8(3):269–77.PubMedCrossRefGoogle Scholar
  82. 82.
    Bohn MC, Howard E, Vielkind U, Krozowski Z. Glial cells express both mineralocorticoid and glucocorticoid receptors. J Steroid Biochem Mol Biol. 1991;40(1–3):105–11.PubMedCrossRefGoogle Scholar
  83. 83.
    Cintra A, Bhatnagar M, Chadi G, Tinner B, Lindberg J, Gustafsson JA, Agnati LF, Fuxe K. Glial and neuronal glucocorticoid receptor immunoreactive cell populations in developing, adult, and aging brain. Ann N Y Acad Sci. 1994;746:42–61.PubMedCrossRefGoogle Scholar
  84. 84.
    Wang Q, Verweij EW, Krugers HJ, Joels M, Swaab DF, Lucassen PJ. Distribution of the glucocorticoid receptor in the human amygdala; changes in mood disorder patients. Brain Struct Funct. 2014;219(5):1615–26.PubMedCrossRefGoogle Scholar
  85. 85.
    Wang Q, Van Heerikhuize J, Aronica E, Kawata M, Seress L, Joels M, Swaab DF, Lucassen PJ. Glucocorticoid receptor protein expression in human hippocampus; stability with age. Neurobiol Aging. 2013;34(6):1662–73.PubMedCrossRefGoogle Scholar
  86. 86.
    Komatsuzaki Y, Hatanaka Y, Murakami G, Mukai H, Hojo Y, Saito M, Kimoto T, Kawato S. Corticosterone induces rapid spinogenesis via synaptic glucocorticoid receptors and kinase networks in hippocampus. PLoS One. 2012;7(4):e34124.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Chatterjee S, Sikdar SK. Corticosterone treatment results in enhanced release of peptidergic vesicles in astrocytes via cytoskeletal rearrangements. Glia. 2013;61(12):2050–62.PubMedCrossRefGoogle Scholar
  88. 88.
    O’Callaghan JP, Brinton RE, McEwen BS. Glucocorticoids regulate the synthesis of glial fibrillary acidic protein in intact and adrenalectomized rats but do not affect its expression following brain injury. J Neurochem. 1991;57(3):860–9.PubMedCrossRefGoogle Scholar
  89. 89.
    Nichols NR, Osterburg HH, Masters JN, Millar SL, Finch CE. Messenger RNA for glial fibrillary acidic protein is decreased in rat brain following acute and chronic corticosterone treatment. Brain Res Mol Brain Res. 1990;7(1):1–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Paukert M, Agarwal A, Cha J, Doze VA, Kang JU, Bergles DE. Norepinephrine controls astroglial responsiveness to local circuit activity. Neuron. 2014;82(6):1263–70.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Ding F, O’Donnell J, Thrane AS, Zeppenfeld D, Kang H, Xie L, Wang F, Nedergaard M. α1-Adrenergic receptors mediate coordinated Ca2+ signaling of cortical astrocytes in awake, behaving mice. Cell Calcium. 2013;54(6):387–94.PubMedCrossRefGoogle Scholar
  92. 92.
    Mobley PL, Combs DL. Norepinephrine-mediated protein phosphorylation in astrocytes. Brain Res Bull. 1992;29(3–4):289–95.PubMedCrossRefGoogle Scholar
  93. 93.
    Takemura M, Gomi H, Colucci-Guyon E, Itohara S. Protective role of phosphorylation in turnover of glial fibrillary acidic protein in mice. J Neurosci. 2002;22(16):6972–9.PubMedGoogle Scholar
  94. 94.
    Rajkowska G, Stockmeier CA. Astrocyte pathology in major depressive disorder: insights from human postmortem brain tissue. Curr Drug Targets. 2013;14(11):1225–36.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Torres-Platas SG, Hercher C, Davoli MA, Maussion G, Labonté B, Turecki G, Mechawar N. Astrocytic hypertrophy in anterior cingulate white matter of depressed suicides. Neuropsychopharmacology. 2011;36(13):2650–8.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Müller MB, Lucassen PJ, Yassouridis A, Hoogendijk WJ, Holsboer F, Swaab DF. Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur J Neurosci. 2001;14(10):1603–12.PubMedCrossRefGoogle Scholar
  97. 97.
    Miguel-Hidalgo JJ, Baucom C, Dilley G, Overholser JC, Meltzer HY, Stockmeier CA, Rajkowska G. Glial fibrillary acidic protein immunoreactivity in the prefrontal cortex distinguishes younger from older adults in major depressive disorder. Biol Psychiatry. 2000;48(8):861–73.PubMedCrossRefGoogle Scholar
  98. 98.
    Miguel-Hidalgo JJ, Waltzer R, Whittom AA, Austin MC, Rajkowska G, Stockmeier CA. Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. J Affect Disord. 2010;127(1–3):230–40.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Gos T, Schroeter ML, Lessel W, Bernstein HG, Dobrowolny H, Schiltz K, Bogerts B, Steiner J. S100B-immunopositive astrocytes and oligodendrocytes in the hippocampus are differentially afflicted in unipolar and bipolar depression: a postmortem study. J Psychiatr Res. 2013;47(11):1694–9.PubMedCrossRefGoogle Scholar
  100. 100.
    Altshuler LL, Abulseoud OA, Foland-Ross L, Bartzokis G, Chang S, Mintz J, Hellemann G, Vinters HV. Amygdala astrocyte reduction in subjects with major depressive disorder but not bipolar disorder. Bipolar Disord. 2010;12(5):541–9.PubMedCrossRefGoogle Scholar
  101. 101.
    Hamidi M, Drevets WC, Price JL. Glial reduction in amygdala in major depressive disorder is due to oligodendrocytes. Biol Psychiatry. 2004;55(6):563–9.PubMedCrossRefGoogle Scholar
  102. 102.
    Bernard R, Kerman IA, Thompson RC, Jones EG, Bunney WE, Barchas JD, Schatzberg AF, Myers RM, Akil H, Watson SJ. Altered expression of glutamate signaling, growth factor, and glia genes in the locus coeruleus of patients with major depression. Mol Psychiatry. 2011;16(6):634–46.PubMedCrossRefGoogle Scholar
  103. 103.
    Choudary PV, Molnar M, Evans SJ, Tomita H, Li JZ, Vawter MP, Myers RM, Bunney Jr WE, Akil H, Watson SJ, Jones EG. Altered cortical glutamatergic and GABAergic signal transmission with glial involvement in depression. Proc Natl Acad Sci U S A. 2005;102(43):15653–8.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Miguel-Hidalgo JJ, Wilson BA, Hussain S, Meshram A, Rajkowska G, Stockmeier CA. Reduced connexin 43 immunolabeling in the orbitofrontal cortex in alcohol dependence and depression. J Psychiatr Res. 2014;55:101–9.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Rajkowska G, Hughes J, Stockmeier CA, Javier Miguel-Hidalgo J, Maciag D. Coverage of blood vessels by astrocytic endfeet is reduced in major depressive disorder. Biol Psychiatry. 2013;73(7):613–21.PubMedCrossRefGoogle Scholar
  106. 106.
    Kryger R, Wilce PA. The effects of alcoholism on the human basolateral amygdala. Neuroscience. 2010;167(2):361–71.PubMedCrossRefGoogle Scholar
  107. 107.
    Schroeter ML, Abdul-Khaliq H, Krebs M, Diefenbacher A, Blasig IE. Serum markers support disease-specific glial pathology in major depression. J Affect Disord. 2008;111(2–3):271–80.PubMedCrossRefGoogle Scholar
  108. 108.
    Bergh CD, Bäckström M, Axelsson K, Jönsson H, Johnsson P. Protein S100B after cardiac surgery: an indicator of long-term anxiety? Scand Cardiovasc J. 2007;41(2):109–13.PubMedCrossRefGoogle Scholar
  109. 109.
    Li X, Wilder-Smith CH, Kan ME, Lu J, Cao Y, Wong RK. Combat-training stress in soldiers increases S100B, a marker of increased blood-brain-barrier permeability, and induces immune activation. Neuro Endocrinol Lett. 2014;35(1):58–63.PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Christian Luis Bender
    • 1
  • Gastón Diego Calfa
    • 1
  • Víctor Alejandro Molina
    • 1
  1. 1.IFEC-CONICET, Departamento de Farmacología, Facultad de Ciencias QuímicasUniversidad Nacional de CórdobaCórdobaArgentina

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