Stress exacerbates neuron loss and microglia proliferation in a rat model of excitotoxic lower motor neuron injury

Brain, Behavior, and Immunity

Volumn 49, Issue , 2015, Pages 246-254

  Puga, Denise A ^a   Tovar, C Amy ^a   Guan, Zhen ^a   Gensel, John C ^b   Lyman, Matthew S ^a   McTigue, Dana M ^a   Popovich, Phillip G ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Glucocorticoid receptor; Glucocorticoids; Glutamate; Hypothalamic pituitary adrenal axis; Microglia; Neuroinflammation; Spinal cord injury; Stress

Indexed keywords

GLUTAMIC ACID; AMINO ACID RECEPTOR STIMULATING AGENT;

ACUTE STRESS; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL HYPERPLASIA; CELL LOSS; CELL PROLIFERATION; CELL SURVIVAL; CHRONIC STRESS; CONTROLLED STUDY; EXCITOTOXICITY; FEMALE; FOCAL EXCITOTOXIC LOWER MOTOR NEURON INJURY; FORELIMB; GLIA; IMMOBILIZATION STRESS; MICROGLIA; MOTOR NEURON DISEASE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD MOTONEURON; STRESS; ANIMAL; DISEASE MODEL; DRUG EFFECTS; EXERCISE; MENTAL STRESS; MOTONEURON; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; SPINAL CORD INJURY; SPRAGUE DAWLEY RAT;

ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; FEMALE; GLUTAMIC ACID; MICROGLIA; MOTOR NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RESTRAINT, PHYSICAL; SPINAL CORD; SPINAL CORD INJURIES; STRESS, PSYCHOLOGICAL;

EID: 84940574039     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.06.006     Document Type: Article

References (61)

1. Ahima R.S., Harlan R.E. Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. NSC 1990, 39:579-604.
2. Batchelor P.E., Tan S., Wills T.E., Porritt M.J., Howells D.W. Comparison of inflammation in the brain and spinal cord following mechanical injury. J. Neurotrauma 2008, 25:1217-1225. 10.1089/neu.2007.0308.
3. Busch S.A., Horn K.P., Cuascut F.X., Hawthorne A.L., Bai L., Miller R.H., Silver J. Adult NG2+ cells are permissive to neurite outgrowth and stabilize sensory axons during macrophage-induced axonal dieback after spinal cord injury. J. Neurosci. 2010, 30:255-265. 10.1523/JNEUROSCI.3705-09.2010.
4. Cruse J.M., Lewis R.E., Bishop G.R., Kliesch W.F., Gaitan E., Britt R. Decreased immune reactivity and neuroendocrine alterations related to chronic stress in spinal cord injury and stroke patients. Pathobiology 1993, 61:183-192.
5. de Kloet E.R., Vreugdenhil E., Oitzl M.S., Joëls M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 1998, 19:269-301. 10.1210/edrv.19.3.0331.
6. de Pablos R.M. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J. Neurosci. 2006, 26:5709-5719. 10.1523/JNEUROSCI.0802-06.2006.
7. de Pablos R.O.M., Herrera A.J., Espinosa-Oliva A.M., Sarmiento M., Oz M.F.M., Machado A., Venero J.L. Chronic stress enhances microglia activation and exacerbates death of nigral dopaminergic neurons under conditions of inflammation. J. Neuroinflamm. 2014, 11:1-18. 10.1186/1742-2094-11-34.
8. Dhabhar F.S., McEwen B.S. Enhancing versus suppressive effects of stress hormones on skin immune function. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:1059-1064.
9. Dhabhar F.S., Satoskar A.R., Bluethmann H., David J.R., McEwen B.S. Stress-induced enhancement of skin immune function: a role for gamma interferon. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:2846-2851. 10.1073/pnas.050569397.
10. Dinkel K., MacPherson A., Sapolsky R.M. Novel glucocorticoid effects on acute inflammation in the CNS. J. Neurochem. 2003, 84:705-716.
11. Donnelly D.J., Gensel J.C., Ankeny D.P., van Rooijen N., Popovich P.G. An efficient and reproducible method for quantifying macrophages in different experimental models of central nervous system pathology. J. Neurosci. Methods 2009, 181:36-44. 10.1016/j.jneumeth.2009.04.010.
12. Ferguson A.R., Huie J.R., Crown E.D., Baumbauer K.M., Hook M.A., Garraway S.M., Lee K.H., Hoy K.C., Grau J.W. Maladaptive spinal plasticity opposes spinal learning and recovery in spinal cord injury. Front. Physiol. 2012, 3:399. 10.3389/fphys.2012.00399.
13. Fidler J.A., Treleaven C.M., Frakes A., Tamsett T.J., McCrate M., Cheng S.H., Shihabuddin L.S., Kaspar B.K., Dodge J.C. Disease progression in a mouse model of amyotrophic lateral sclerosis: the influence of chronic stress and corticosterone. FASEB J. 2011, 25:4369-4377. 10.1096/fj.11-190819.
14. Fuxe K., Härfstrand A., Agnati L.F., Yu Z.Y., Cintra A., Wikström A.C., Okret S., Cantoni E., Gustafsson J.A. Immunocytochemical studies on the localization of glucocorticoid receptor immunoreactive nerve cells in the lower brain stem and spinal cord of the male rat using a monoclonal antibody against rat liver glucocorticoid receptor. Neurosci. Lett. 1985, 60:1-6.
15. Ganter S., Northoff H., Männel D., Gebicke-Härter P.J. Growth control of cultured microglia. J. Neurosci. Res. 1992, 33:218-230. 10.1002/jnr.490330205.
16. Garraway S.M., Woller S.A., Huie J.R., Hartman J.J., Hook M.A., Miranda R.C., Huang Y.-J., Ferguson A.R., Grau J.W. Peripheral noxious stimulation reduces withdrawal threshold to mechanical stimuli after spinal cord injury: role of tumor necrosis factor alpha and apoptosis. Pain 2014, 155:2344-2359. 10.1016/j.pain.2014.08.034.
17. Gensel J.C., Tovar C.A., Hamers F.P.T., Deibert R.J., Beattie M.S., Bresnahan J.C. Behavioral and histological characterization of unilateral cervical spinal cord contusion injury in rats. J. Neurotrauma 2006, 23:36-54. 10.1089/neu.2006.23.36.
18. Girotti M., Pace T.W.W., Gaylord R.I., Rubin B.A., Herman J.P., Spencer R.L. Habituation to repeated restraint stress is associated with lack of stress-induced c-fos expression in primary sensory processing areas of the rat brain. NSC 2006, 138:1067-1081. 10.1016/j.neuroscience.2005.12.002.
19. Goshgarian H.G. The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol. 2003, 94:795-810. 10.1152/japplphysiol.00847.2002.
20. Grau, J.W., 2014. Metaplasticity and behavior: how training and inflammation affect plastic potential within the spinal cord and recovery after injury 1-23. doi:10.3389/fncir.2014.00100/abstract.
21. Groc L., Choquet D., Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat. Neurosci. 2008, 10.1038/nn.2150.
22. Herman J.P. Neural control of chronic stress adaptation. Front. Behav. Neurosci. 2013, 7:61. 10.3389/fnbeh.2013.00061.
23. Hermann G.E., Rogers R.C., Bresnahan J.C., Beattie M.S. Tumor necrosis factor-alpha induces cFOS and strongly potentiates glutamate-mediated cell death in the rat spinal cord. Neurobiol. Dis. 2001, 8:590-599. 10.1006/nbdi.2001.0414.
24. Huie J.R., Baumbauer K.M., Lee K.H., Bresnahan J.C., Beattie M.S., Ferguson A.R., Grau J.W. Glial tumor necrosis factor alpha (TNFα) generates metaplastic inhibition of spinal learning. PLoS ONE 2012, 7:e39751. 10.1371/journal.pone.0039751.
25. Johnson J.D., Campisi J., Sharkey C.M., Kennedy S.L., Nickerson M., Greenwood B.N., Fleshner M. Catecholamines mediate stress-induced increases in peripheral and central inflammatory cytokines. NSC 2005, 135:1295-1307. 10.1016/j.neuroscience.2005.06.090.
26. Johnson J.D., Zimomra Z.R., Stewart L.T. Beta-adrenergic receptor activation primes microglia cytokine production. J. Neuroimmunol. 2013, 254:161-164. 10.1016/j.jneuroim.2012.08.007.
27. Jones T.A., Schallert T. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Res. 1992, 581:156-160.
28. Kigerl K.A., Ankeny D.P., Garg S.K., Wei P., Guan Z., Lai W., McTigue D.M., Banerjee R., Popovich P.G. System xc- regulates microglia and macrophage glutamate excitotoxicity in vivo. Exp. Neurol. 2012, 233:333-341. 10.1016/j.expneurol.2011.10.025.
29. Kim J.J., Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 2002, 3:453-462. 10.1038/nrn849.
30. Kim J.J., Foy M.R., Thompson R.F. Behavioral stress modifies hippocampal plasticity through N-methyl-d-aspartate receptor activation. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4750-4753.
31. Kuzmiski J.B., Marty V., Baimoukhametova D.V., Bains J.S. Stress-induced priming of glutamate synapses unmasks associative short-term plasticity. Nat. Neurosci. 2010, 13:1257-1264. 10.1038/nn.2629.
32. Lucin K.M., Sanders V.M., Jones T.B., Malarkey W.B., Popovich P.G. Impaired antibody synthesis after spinal cord injury is level dependent and is due to sympathetic nervous system dysregulation. Exp. Neurol. 2007, 207:75-84. 10.1016/j.expneurol.2007.05.019.
33. MacPherson A., Dinkel K., Sapolsky R. Glucocorticoids worsen excitotoxin-induced expression of pro-inflammatory cytokines in hippocampal cultures. Exp. Neurol. 2005, 194:376-383. 10.1016/j.expneurol.2005.02.021.
34. Maldonado Bouchard S., Hook M.A. Psychological stress as a modulator of functional recovery following spinal cord injury. Front. Neurol. 2014, 5:44. 10.3389/fneur.2014.00044.
35. McKenna J.E., Prusky G.T., Whishaw I.Q. Cervical motoneuron topography reflects the proximodistal organization of muscles and movements of the rat forelimb: a retrograde carbocyanine dye analysis. J. Comp. Neurol. 2000, 419:286-296.
36. McTigue D.M., Wei P., Stokes B.T. Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J. Neurosci. 2001, 21:3392-3400.
37. Merrill J.E. Effects of interleukin-1 and tumor necrosis factor-alpha on astrocytes, microglia, oligodendrocytes, and glial precursors in vitro. Dev. Neurosci. 1991, 13:130-137.
38. Metz G.A., Schwab M.E., Welzl H. The effects of acute and chronic stress on motor and sensory performance in male Lewis rats. Physiol. Behav. 2001, 72:29-35.
39. Moses D.F., González S., Ortí E., De Nicola A.F. Heterogeneity and properties of transformation of corticosteroid receptors in spinal cord and hippocampus. Brain Res. 1989, 481:317-324.
40. Moses D.F., González S., McEwen B.S., De Nicola A.F. Glucocorticoid type II receptors of the spinal cord show lower affinity than hippocampal type II receptors: binding parameters obtained with different experimental protocols. J. Steroid Biochem. Mol. Biol. 1991, 39:5-12.
41. Munhoz C.D., Lepsch L.B., Kawamoto E.M., Malta M.B., Lima Lde S., Avellar M.C.W., Sapolsky R.M., Scavone C. Chronic unpredictable stress exacerbates lipopolysaccharide-induced activation of nuclear factor-kappaB in the frontal cortex and hippocampus via glucocorticoid secretion. J. Neurosci. 2006, 26:3813-3820. 10.1523/JNEUROSCI.4398-05.2006.
42. Munhoz C.D., Sorrells S.F., Caso J.R., Scavone C., Sapolsky R.M. Glucocorticoids exacerbate lipopolysaccharide-induced signaling in the frontal cortex and hippocampus in a dose-dependent manner. J. Neurosci. 2010, 30:13690-13698. 10.1523/JNEUROSCI.0303-09.2010.
43. Nair A., Bonneau R.H. Stress-induced elevation of glucocorticoids increases microglia proliferation through NMDA receptor activation. J. Neuroimmunol. 2006, 171:72-85. 10.1016/j.jneuroim.2005.09.012.
44. Patacchioli F.R., Angelucci L., Casolini P., Bottone A., Borboni P., Lauro R., Marlier L.N. Corticosterone treatment differentially affects adrenocorticoid receptors expression and binding in the hippocampus and spinal cord of the rat. J. Mol. Neurosci. 1998, 11:95-103. 10.1385/JMN:11:1:95.
45. Pavlides C., Watanabe Y., McEwen B.S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 1993, 3:183-192. 10.1002/hipo.450030210.
46. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 1997, 377:443-464.
47. Sapolsky R.M., Pulsinelli W.A. Glucocorticoids potentiate ischemic injury to neurons: therapeutic implications. Science 1985, 229:1397-1400.
48. Schnell L., Fearn S., Klassen H., Schwab M.E., Perry V.H. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 1999, 11:3648-3658.
49. Schonberg D.L., Popovich P.G., McTigue D.M. Oligodendrocyte generation is differentially influenced by toll-like receptor (TLR) 2 and TLR4-mediated intraspinal macrophage activation. J. Neuropathol. Exp. Neurol. 2007, 66:1124-1135. 10.1097/nen.0b013e31815c2530.
50. Seifi M., Corteen N.L., van der Want J.J., Metzger F., Swinny J.D. Localization of NG2 immunoreactive neuroglia cells in the rat locus coeruleus and their plasticity in response to stress. Front. Neuroanat. 2014, 8:31. 10.3389/fnana.2014.00031.
51. Smith-Swintosky V.L., Pettigrew L.C., Sapolsky R.M., Phares C., Craddock S.D., Brooke S.M., Mattson M.P. Metyrapone, an inhibitor of glucocorticoid production, reduces brain injury induced by focal and global ischemia and seizures. J. Cereb. Blood Flow Metab. 1996, 16:585-598. 10.1097/00004647-199607000-00008.
52. Sorrells S.F., Caso J.R., Munhoz C.D., Sapolsky R.M. The stressed CNS: when glucocorticoids aggravate inflammation. Neuron 2009, 64:33-39. 10.1016/j.neuron.2009.09.032.
53. Sorrells S.F., Caso J.R., Munhoz C.D., Hu C.K., Tran K.V., Miguel Z.D., Chien B.Y., Sapolsky R.M. Glucocorticoid signaling in myeloid cells worsens acute CNS injury and inflammation. J. Neurosci. 2013, 33:7877-7889. 10.1523/JNEUROSCI.4705-12.2013.
54. Stein-Behrens B.A., Elliott E.M., Miller C.A., Schilling J.W., Newcombe R., Sapolsky R.M. Glucocorticoids exacerbate kainic acid-induced extracellular accumulation of excitatory amino acids in the rat hippocampus. J. Neurochem. 1992, 58:1730-1735.
55. Takahashi J.L., Giuliani F., Power C., Imai Y., Yong V.W. Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann. Neurol. 2003, 53:588-595. 10.1002/ana.10519.
56. Tosolini A.P., Morris R. Spatial characterization of the motor neuron columns supplying the rat forelimb. NSC 2012, 200:19-30. 10.1016/j.neuroscience.2011.10.054.
57. Tynan R.J., Naicker S., Hinwood M., Nalivaiko E., Buller K.M., Pow D.V., Day T.A., Walker F.R. Chronic stress alters the density and morphology of microglia in a subset of stress-responsive brain regions. Brain Behav. Immun. 2010, 24:1058-1068. 10.1016/j.bbi.2010.02.001.
58. Webb A.A., Muir G.D. Compensatory locomotor adjustments of rats with cervical or thoracic spinal cord hemisections. J. Neurotrauma 2002, 19:239-256. 10.1089/08977150252806983.
59. Yan P., Xu J., Li Q., Chen S., Kim G.M., Hsu C.Y., Xu X.M. Glucocorticoid receptor expression in the spinal cord after traumatic injury in adult rats. J. Neurosci. 1999, 19:9355-9363.
60. Zhang B., Gensel J.C. Experimental neurology. Exp. Neurol. 2014, 258:112-120. 10.1016/j.expneurol.2014.04.007.
61. Zhang Y., Guan Z., Reader B., Shawler T., Mandrekar-Colucci S., Huang K., Weil Z., Bratasz A., Wells J., Powell N.D., Sheridan J.F., Whitacre C.C., Rabchevsky A.G., Nash M.S., Popovich P.G. Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J. Neurosci. 2013, 33:12970-12981. 10.1523/JNEUROSCI.1974-13.2013.