Influenza virus- and cytokine-immunoreactive cells in the murine olfactory and central autonomic nervous systems before and after illness onset

Journal of Neuroimmunology

Volumn 211, Issue 1-2, 2009, Pages 73-83

  Leyva Grado, Victor H ^a   Churchill, Lynn ^a   Wu, Melissa ^a   Williams, Timothy J ^a   Taishi, Ping ^a   Majde, Jeannine A ^a   Krueger, James M ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Acute phase response; Glia; Influenza virus; NeuN; Neuronal cytokines; Olfactory system

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BRAIN REGION; CELL COUNT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION; GLIA CELL; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; INFLUENZA; INFLUENZA VIRUS A; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS VIRULENCE;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; CYTOKINES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; INFLUENZA A VIRUS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEUROGLIA; NEURONS; OLFACTORY BULB; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 67349136855     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2009.03.016     Document Type: Article

References (96)

1. Acarin L., González B., and Castellano B. Neuronal, astroglial and microglial cytokine expression after an excitotoxic lesion in the immature rat brain. Eur. J. Neurosci. 12 (2000) 3505-3520
2. Au W.W., Treloar H.B., and Greer C.A. Sublaminar organization of the mouse olfactory bulb nerve layer. J. Comp. Neurol. 446 (2002) 68-80
3. Barbe M.E., Barr A.E., Gorzelany I., Amin M., Gaughan J.P., and Safadi F.F. Chronic repetitive reaching and grasping results in decreased motor performance and widespread tissue responses in a rat model of MSD. J. Orthop. Res. 21 (2003) 167-176
4. Ben Hur T., Rosenthal J., Itzik A., and Weidenfeld J. Adrenocortical activation by herpes virus: involvement of IL-1 beta and central noradrenergic system. Neuroreport 7 (1996) 927-931
5. Bluthé R.M., Layé S., Michaud B., Combe C., Dantzer R., and Parnet P. Role of interleukin-1beta and tumour necrosis factor-alpha in lipopolysaccharide-induced sickness behaviour: a study with interleukin-1 type I receptor-deficient mice. Eur. J. Neurosci. 12 (2000) 4447-4456
6. Bradshaw G.L., Schlesinger R.W., and Schwartz C.D. Effects of cell differentiation on replication of A/WS/33, WSN, and A/PR/8/34 influenza viruses in mouse brain cell cultures: biological and immunological characterization of products. J. Virol. 63 (1989) 1704-1714
7. Breder C.D., Tsujimoto M., Terano Y., Scott D.W., and Saper C.D. Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine central nervous system. J. Comp. Neurol. 337 (1993) 543-567
8. Breder C.D., Hazuka C., Ghayur T., Klug C., Huginin M., Yasuda K., Teng M., and Saper C.B. Regional induction of tumor necrosis factor alpha expression in the mouse brain after systemic lipopolysaccharide administration. Proc. Natl. Acad. Sci. 91 (1994) 11393-11397
9. Bulloch K., Miller M.M., Gal-Toth J., Milner T.A., Gottfried-Blackmore A., Waters E.M., Kaunzner U.W., Liu K., Lindquist R., Nussenzweig M.C., Steinman R.M., and McEwen B.S. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult and injured mouse brain. J. Comp. Neurol. 508 (2008) 687-710
10. Chen L., Duricka D., Nelson S., Mukherjee S., Bohnet S.G., Taishi P., Majde J.A., and Krueger J.M. Influenza virus-induced sleep responses in mice with targeted disruptions in neuronal or inducible nitric oxide synthases. J. Appl. Physiol. 97 (2004) 17-28
11. Chiba T., and Murata Y. Afferent and efferent connections of the medial preoptic area in the rat: a WGA-HRP study. Brain Res. Bull. 14 (1985) 261-272
12. Churchill L., Yasuda K., Yasuda T., Blindheim K.A., Falter M., Garcia-Garcia F., and Krueger J.M. Unilateral cortical application of tumor necrosis factor-α induces asymmetry in Fos- and interleukin-1β-immunoreactive cells within the corticothalamic projection. Brain Res. 1055 (2005) 15-24
13. Conn C.A., McClellan J.L., Maassab H.F., Smitka C.W., Majde J.A., and Kluger M.J. Cytokines and the acute phase response to influenza virus in mice. Am. J. Physiol. 268 (1995) R78-R84
14. Day H.E., Curran E.J., Watson Jr. S.J., and Akil H. Distinct neurochemical populations in the rat central nucleus of the amygdala and bed nucleus of the stria terminalis: evidence for their selective activation by interleukin-1beta. J. Comp. Neurol. 413 (1999) 113-128
15. Deak T., Bordner K.A., McElderry N.K., Barnum C.J., Blandino Jr. P., Deak M.M., and Tammariello S.P. Stress-induced increases in hypothalamic IL-1: a systematic analysis of multiple stressor paradigms. Brain Res. Bull. 30 (2005) 541-556
16. Deng X.H., Bertini G., Xu Y.Z., Yan Z., and Bentivoglio M. Cytokine-induced activation of glial cells in the mouse brain is enhanced at an advanced age. Neuroscience 141 (2006) 645-661
17. Deshpande P., King I.I., and Segal B.M. Cutting Edge: CNS CD11c+ cells from mice with encephalomyelitis polarize Th17 cells and support CD25+CD4+ T cell-mediated immunosuppression, suggesting dual roles in the disease process. J. Immunol. 178 (2007) 6695-6699
18. Eriksson C., Van Dam A.M., Lucassen P.J., Bol J.G., Winblad B., and Schultzberg M. Immunohistochemical localization of interleukin-1beta, interleukin-1 receptor antagonist and interleukin-1beta converting enzyme/caspase-1 in the rat brain after peripheral administration of kainic acid. Neuroscience 93 (1999) 915-930
19. Fang J., Sanborn C.K., Renegar K.B., Majde J.A., and Krueger J.M. Influenza viral infections enhance sleep in mice. Proc. Soc. Exp. Biol. Med. 210 (1995) 242-252
20. Figiel I., and Dzwonek K. TNFalpha and TNF receptor 1 expression in the mixed neuronal-glial cultures of hippocampal dentate gyrus exposed to glutamate or trimethyltin. Brain Res. 1131 (2007) 17-28
21. Frenois F., Moreau M., O Connor J., Lawson M., Micon C., Lestage J., Kelley K.W., Dantzer R., and Castanon N. Lipopolysaccharide induces delayed FosB/DeltaFosB immunostaining within the mouse extended amygdala, hippocampus and hypothalamus, that parallel the expression of depressive-like behavior. Psychoneuroendocrinology 32 (2007) 516-531
22. Gao Y., Ng Y.K., Lin J.Y., and Ling E.A. Expression of immunoregulatory cytokines in neurons of the lateral hypothalamic area and amygdaloid nuclear complex of rats immunized against human IgG. Brain Res. 859 (2000) 364-368
23. Gayle D., Ilyin S.E., and Plata-Salaman C.R. Central nervous system IL-1[beta] system and neuropeptide Y mRNAs during IL-1[beta]-induced anorexia in rats. Brain Res. Bull. 44 (1997) 311-317
24. Ghoshal A., Das S., Ghosh S., Mishra M.K., Sharma V., Koh P., Sen E., and Basu A. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55 (2007) 483-496
25. Goehler L.E., Gaykema R.P., Hansen M.K., Anderson K., Maier S.F., and Watkins L.R. Vagal immune-to-brain communication: a visceral chemosensory pathway. Auton. Neurosci. 85 (2000) 49-59
26. Guillemin G.J., and Brew B.J. Microglia, macrophages, perivascular macrophages and pericytes: a review of function and identification. J. Leukoc. Biol. 75 (2003) 388-397
27. Haberly L. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26 (2001) 551-576
28. Hansen M.K., Taishi P., Chen Z., and Krueger J.M. Vagotomy blocks the induction of interleukin-1beta (IL-1beta) mRNA in the brain of rats in response to systemic IL-1beta. J. Neurosci. 18 (1998) 2247-2253
29. Hauwel M., Furon E., Canova C., Griffiths M., Neal J., and Gasque P. Innate (inherent) control of brain infection, brain inflammation and brain repair: the role of microglia, astrocytes, "protective" glial stem cells and stromal ependymal cells. Brain Res. Rev. 48 (2005) 220-233
30. Hennet T., Ziltener H.J., Frei K., and Peterhans E. A kinetic study of immune mediators in the lungs of mice infected with influenza A virus. J. Immunol. 149 (1992) 932-939
31. Ignatowski T.A., Noble B.K., Wright J.R., Gorfien J.L., Heffner R.R., and Spengler R.N. Neuronal-associated tumor necrosis factor (TNF alpha): its role in noradrenergic functioning and modification of its expression following antidepressant drug administration. J. Neuroimmunol. 79 (1997) 84-90
32. Iwasaki T., Itamura S., Nishimura H., Sato Y., Tashiro M., Hashikawa T., and Kurata T. Productive infection in the murine central nervous system with avian influenza virus (H5N1) after intranasal inoculation. Acta Neuropathol. 108 (2004) 485-492
33. Ji J.F., Dheen S.T., Kumar S.D., He B.P., and Tay S.S. Expressions of cytokines and chemokines in the dorsal motor nucleus of the vagus nerve after right vagotomy. Mol. Brain Res. 142 (2005) 47-57
34. Johnson D.M., Illig K.R., Behan M., and Haberly L.B. New features in connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex function like "association" cortex in other sensory systems. J. Neurosci, 20 (2000) 6974-6982
35. Jolicoeur F.B., Bouali S.M., Fournier A., and St-Pierre S. Mapping of hypothalamic sites involved in the effects of NPY on body temperature and food intake. Brain Res. Bull. 36 (1995) 125-129
36. Josephson E., Padgett M.L., and Buxton D.F. The lateral and medial compartments of the olfactory tubercle and their relation to olfactory-related input as determined by artificial neural network. Brain Res. 744 (1997) 253-271
37. Kinoshita N., Mizuno T., and Yoshihara Y. Adenovirus-mediated WGA gene delivery for transsynaptic labeling of mouse olfactory pathways. Chem. Senses 27 (2002) 215-223
38. Klein M.S., Conn C.A., and Kluger M.J. Behavioral thermoregulation in mice inoculated with influenza virus. Physiol. Behav. 52 (1992) 1133-1139
39. Konsman J.P., Kelley K., and Dantzer R. Temporal and spatial relationships between lipopolysaccharide-induced expression of Fos, interleukin-1beta and inducible nitric oxide synthase in rat brain. Neuroscience 89 (1999) 535-548
40. Kozak W., Zheng H., Conn C.A., Soszynski D., Van der Ploeg L.H.T., and Kluger M.J. Thermal and behavioral effects of lipopolysaccharide and influenza in interleukin-1β deficient mice. Am. J. Physiol. 269 (1995) R969-R977
41. Krueger J.M., Walter J., Dinarello C.A., Wolff S.M., and Chedid L. Sleep-promoting effects of endogenous pyrogen (interleukin-1). Am. J. Physiol. 246 (1984) R994-R999
42. Kubota T., Fang J., Guan Z., Brown R.A., and Krueger J.M. Vagotomy attenuates tumor necrosis factor-alpha-induced sleep and EEG delta-activity in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) R1213-R1220
43. Kumar S.S., and Buckmaster P.S. Neuron-specific nuclear antigen NeuN is not detectable in gerbil substantia nigra pars reticulata. Brain Res. 1142 (2007) 54-60
44. Kumaraswamy G.K., Fu M.M., and Docherty J.J. Innate and adaptive host response during the initial phase of herpes simplex virus encephalitis in the neonatal mouse. J. Neurovirol. 12 (2006) 365-374
45. Kwon M.S., Seo Y.J., Lee J.K., Lee H.K., Jung J.S., Jang J.E., Park S.H., and Suh H.W. 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. 430 (2008) 258-263
46. LeDoux J. The amygdala. Current Biology 17 (2007) R868-R874
47. Lehnardt S., Henneke P., Lien E., Kasper D.L., Volpe J.J., Bechmann I., Nitsch R., Weber J.R., Golenbock D.T., and Vartanian T. A mechanism for neurodegeneration induced by group B streptococci through activation of the TLR2/MyD88 pathway in microglia. J. Immunol. 177 (2006) 583-592
48. Lemstra A.W., Groen in't Woud J.C., Hoozemans J.J., van Haastert E.S., Rozemuller A.J., Eikelenboom P., and van Gool W.A. Microglia activation in sepsis: a case-control study. J. Neuroinflammation 4 (2007) 4-12
49. Leung J.Y., Chapman J.A., Harris J.A., Hale D., Chung R.S., West A.K., and Chuah M.I. Olfactory ensheathing cells are attracted to, and can endocytose, bacteria. Cell Mol. Life Sci. 65 (2008) 2732-2739
50. Li Y., Field P.M., and Raisman G. Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibers. Glia 52 (2005) 245-251
51. Lim J.H., and Brunjes P.C. Activity-dependent regulation of interleukin-1 beta immunoreactivity in the developing rat olfactory bulb. Neuroscience. 93 (1999) 371-374
52. Lin L., and York D.A. Amygdala enterostatin induces c-Fos expression in regions of hypothalamus that innervate the PVN. Brain Res. 1020 (2004) 147-153
53. Liu T., Clark R.K., McDonnell P.C., Young P.R., White R.F., Barone F.C., and Feuerstein G.Z. Tumor necrosis factor-alpha expression in ischemic neurons. Stroke 25 (1994) 1481-1488
54. Majde J.A., Guha-Thakurta N., Chen Z., Bredow S., and Krueger J.M. Spontaneous release of stable viral double-stranded RNA into the extracellular medium by influenza virus-infected MDCK epithelial cells: implications for the viral acute phase response. Arch. Virol. 143 (1998) 2371-2380
55. Majde J.A., Bohnet S.G., Ellis G.A., Churchill L., Leyva-Grado V.H., Wu M., Szentirmai E., Rehman A., and Krueger J.M. Detection of mouse-adapted human influenza viruses in the olfactory bulbs of mice within hours after intranasal inoculation. J. Neurovirol. 13 (2007) 399-409
56. Mao M., Hua Y., Jiang X., Li L., Zhang L., and Mu D. Expression of tumor necrosis factor alpha and neuronal apoptosis in the developing rat brain after neonatal stroke. Neurosci. Lett. 403 (2006) 227-232
57. Matsuda K., Park C.H., Sunden Y., Kimura T., Ochiai K., Kida H., and Umemura T. The vagus nerve is one route of transneural invasion for intranasally inoculated influenza a virus in mice. Vet. Pathol. 41 (2004) 101-107
58. McQuillin J., Madeley C.R., and Kendal A.P. Monoclonal antibodies for the rapid diagnosis of influenza A and B virus infections by immunofluorescence. Lancet 2 (1985) 911-914
59. Mori I., Komatsu T., Takeuchi K., Nakakuki K., Sudo M., and Kimura Y. Viremia induced by influenza virus. Microbiol. Pathog. 19 (1995) 237-244
60. Ohtori S., Takahashi K., Moriya H., and Myers R.R. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord. Spine 29 (2004) 1082-1088
61. Parrish-Aungst S., Shipley M.T., Erdelyi F., Szabo G., and Puche A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 501 (2007) 825-836
62. Perry V.H., Hume D.A., and Gordon S. Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15 (1985) 313-326
63. Perry V.H. Modulation of microglia phenotype. Neuropathol. Appl. Neurobiol. 20 (1994) 177
64. Plata-Salaman C.R., Oomura Y., and Kai Y. Tumor necrosis factor and interleukin-1β: Suppression of food intake by direct action in the central nervous system. Brain Res. 448 (1988) 106-114
65. Price J.L., Slotnick B.M., and Revial M.F. Olfactory projections to the hypothalamus. J. Comp. Neurol. 306 (1991) 447-461
66. Price J.L. Comparative aspects of amygdala connectivity. Ann. N.Y. Acad. Sci. 985 (2003) 50-58
67. Reyes T.M., and Sawchenko P.E. Involvement of the arcuate nucleus of the hypothalamus in interleukin-1-induced anorexia. J. Neurosci. 22 (2002) 5091-5099
68. Romanovsky A.A., Almeida M.C., Aronoff D.M., Ivanov A.I., Konsman J.P., Steiner A.A., and Turek V.F. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front. Biosci. 10 (2005) 193-216
69. Rossi-George A., Urbach D., Colas D., Goldfarb Y., and Kusnecov A.W. Neuronal, endocrine, and anorexic responses to the T-cell superantigen staphylococcal enterotoxin A: dependence on tumor necrosis factor-alpha. J. Neurosci. 25 (2005) 5314-5322
70. Sagar S.M., Price K.J., Kasting N.W., and Sharp F.R. Anatomic patterns of Fos immunostaining in rat brain following systemic endotoxin administration. Brain Res. Bull. 36 (1995) 381-392
71. Scarlett J.M., Jobst E.E., Enriori P.J., Bowe D.D., Batra A.K., Grant W.F., Cowley M.A., and Marks D.L. Regulation of central melanocortin signaling by interleukin-1 beta. Endocrinology. 148 (2007) 4217-4225
72. Schlesinger R.W. Incomplete growth cycle of influenza virus in mouse brain. Proc. Soc. Exp. Biol. Med. 74 (1950) 541-548
73. Schlesinger R.W., Husak P.J., Bradshaw G.L., and Panayotov P.P. Mechanisms in natural and experimental neuropathogenicity of influenza viruses: evidence and speculation. Adv. Virus Res. 50 (1998) 289-379
74. Sellami S., and de Beaurepaire R. Hypothalamic and thalamic sites of action of interleukin-1 beta on food intake, body temperature and pain sensitivity in the rat. Brain Res 694 (1995) 69-77
75. Shipley M.T., Ennis M., and Puche A.C. Olfactory system. In: Paxinos G. (Ed). The Rat Nervous System (2004) 923-964 Chapter 25
76. Silverman M.N., Pearce B.D., Biron C.A., and Miller A.H. Immune modulation of the hypothalamic-pituitary-adrenal (HPA) axis during viral infection. Viral Immunol. 18 (2005) 41-78
77. Solomon K.A., Pesti N., Wu G., and Newton R.C. Cutting edge: a dominant negative form of TNF-alpha converting enzyme inhibits proTNF and TNFRII secretion. J. Immunol. 163 (1999) 4105-4108
78. Stangel M., and Compston A. Polyclonal immunoglobulins (IVIg) modulate nitric oxide production and microglial functions in vitro via Fc receptors. J Neuroimmunol. 112 (2001) 63-71
79. Stichel C.C., and Luebbert H. Inflammatory processes in the aging mouse brain: participation of dendritic cells and T-cells. Neurobiol. Aging 28 (2007) 1507-1521
80. Suzuki N., and Bekkers J.M. Inhibitory interneurons in the piriform cortex. Clin. Exp. Pharmacol. Physiol. 34 (2007) 1064-1069
81. Szentirmai E., and Krueger J.M. Central administration of neuropeptide Y induces wakefulness in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 (2006) R473-R480
82. Szentirmai E., Kapás L., Sun Y., Smith R.G., and Krueger J.M. Spontaneous sleep and homeostatic sleep regulation in ghrelin knockout mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293 (2007) R510-R517
83. Szymusiak R., and Satinoff E. Acute thermoregulatory effects of unilateral electrolytic lesions of the medial and lateral preoptic area in rats. Physiol Behav 28 (1982) 161-170
84. Taishi P., Churchill L., Wang M., Kay D., Davis C.J., Guan X., De A., Yasuda T., Liao F., and Krueger J.M. TNF alpha siRNA reduces brain TNF and EEG delta wave activity in rats. Brain Res. 1156 (2007) 125-132
85. Toth L.A., Rehg J.E., and Webster R.G. Strain differences in sleep and other pathophysiological sequelae of influenza virus infection in naive and immunized mice. J. Neuroimmunol. 58 (1995) 89-99
86. Ubeda-Bañon I., Novejarque A., Mohedano-Moriano A., Pro-Sistiaga P., de la Rosa-Prieto C., Insausti R., Martinez-Garcia F., Lanuza E., and Martinez-Marcos A. Projections from the posterolateral olfactory amygdala to the ventral striatum: neural basis for reinforcing properties of chemical stimuli. B.M.C. Neurosci. 8 (2007) 103-113
87. Ubink R., Halasz N., Zhang X., Dagerlind A., and Hokfelt T. Neuropeptide tyrosine is expressed in ensheathing cells around the olfactory nerves in the rat olfactory bulb. Neuroscience 60 (1994) 709-726
88. Vacheron F., Rudent A., Perin S., Labarre C., Quero A.M., and Guenounou M. Production of interleukin 1 and tumour necrosis factor activities in bronchoalveolar washings following infection of mice by influenza virus. J. Gen. Virol. 71 (1990) 477-479
89. Vincent A.J., West A.K., and Chuah M.L. Morphological and functional plasticity of olfactory ensheathing cells. J. Neurocytol. 34 (2005) 65-80
90. Vitkovic L., Konsman J.P., Bockaert J., Dantzer R., Homburger V., and Jacque C. Cytokine signals propagate through the brain. Mol. Psych. 5 (2000) 604-615
91. Walls H.H., Harmon M.W., Slagle J.J., Stocksdale C., and Kendall A.P. Characterization and evaluation of monoclonal antibodies developed for typing influenza A and influenza B viruses. J. Clin. Microbiol. 23 (1986) 240-245
92. Wang G., Zhang J., Li W., Xin G., Su Y., Gao Y., Zhang H., Lin G., Jiao X., and Li K. Apoptosis and proinflammatory cytokine responses of primary mouse microglia and astrocytes induced by human H1N1 and avian H5N1 influenza viruses. Cell Mol. Immunol. 5 (2008) 113-120
93. Wieczorek M., Swiergiel A., Pournajafi-Nazarloo H., and Dunn A.J. Physiological and behavioral responses to interleukin-1beta and LPS in vagotomized mice. Physiol. Behav. 85 (2005) 500-511
94. Weidenfeld J., Itzik A., Goshen I., Yirmiya R., and Ben-Hur T. Role of the central amygdala in modulating the pituitary-adrenocortical and clinical responses in experimental herpes simplex virus-1 encephalitis. Neuroendocrinology 81 (2005) 267-272
95. Xu Y., Day T.A., and Buller K.M. The central amygdala modulates hypothalamic-pituitary-adrenal axis responses to systemic interleukin-1beta administration. Neuroscience 94 (1999) 175-183
96. Yang L., Blumbergs P.C., Jones N.R., Manavis J., Sarvestani G.T., and Ghabriel M.N. Early expression and cellular localization of proinflammatory cytokines interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in human traumatic spinal cord injury. Spine 29 (2004) 966-971