Role of interleukin-6 in lipopolysaccharide-induced brain injury and behavioral dysfunction in neonatal rats

Neuroscience

Volumn 141, Issue 2, 2006, Pages 745-755

  Pang, Y ^a   Fan, L W ^a   Zheng, B ^a   Cai, Z ^a   Rhodes, P G ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

astrocyte; cytokine; microglia; neonatal; oligodendrocyte

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; AVOIDANCE BEHAVIOR; BEHAVIOR DISORDER; BRAIN INJURY; BRAIN SLICE; BRAIN VENTRICLE DILATATION; CELL ACTIVATION; CELL COUNT; COGNITION; CONTROLLED STUDY; FEMALE; GAIT; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LATERAL BRAIN VENTRICLE; LOCOMOTION; MACROGLIA; MALE; MAZE TEST; MICROGLIA; NONHUMAN; OLIGODENDROGLIA; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RIGHTING REFLEX; WHITE MATTER;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BODY WEIGHT; BRAIN INJURIES; CELL COUNT; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MAZE LEARNING; MOTOR ACTIVITY; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33745988227     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.04.007     Document Type: Article

References (51)

1. Ali C., Nicole O., Docagne F., Lesne S., MacKenzie E.T., Nouvelot A., Buisson A., and Vivien D. Ischemia-induced interleukin-6 as a potential endogenous neuroprotective cytokine against NMDA receptor-mediated excitotoxicity in the brain. J Cereb Blood Flow Metab 20 (2000) 956-966
2. Altman J., Sudarshan K., Das G.D., McCormick N., and Barnes D. The influence of nutrition on neural and behavioral development. 3. Development of some motor, particularly locomotor patterns during infancy. Dev Psychobiol 4 (1971) 97-114
3. Altman J., and Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim Behav 23 (1975) 896-920
4. Back S.A., Luo N.L., Borenstein N.S., Levine J.M., Volpe J.J., and Kinney H.C. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21 (2001) 1302-1312
5. Bakos J., Duncko R., Makatsori A., Pirnik Z., Kiss A., and Jezova D. Prenatal immune challenges affect growth, behavior, and brain dopamine in offspring. Ann N Y Acad Sci 1018 (2004) 281-287
6. Bazan J.F. Neuropoietic cytokines in the hematopoietic fold. Neuron 7 (1991) 197-208
7. Bensadoun J.C., de Almeida L.P., Dreano M., Aebischer P., and Deglon N. Neuroprotective effect of interleukin-6 and IL6/ILR chimera in the quinolinic acid rat model of Huntington's syndrome. Eur J Neurosci 14 (2001) 1753-1761
8. Boggess K.A. Pathophysiology of preterm birth. emerging concepts of maternal infection. Clin Perinatol 32 (2005) 561-569
9. Bracewell M., and Marlow N. Patterns of motor disability in very preterm children. Ment Retard Dev Disabil Res Rev 8 (2002) 241-248
10. Cai Z., Pang Y., Lin S., and Rhodes P.G. Differential roles of tumor necrosis factor-alpha and interleukin-1 beta in lipopolysaccharide-induced brain injury in the neonatal rat. Brain Res 975 (2003) 37-47
11. Cai Z., Lin S., Pang Y., and Rhodes P.G. Brain injury induced by intracerebral injection of interleukin-1beta and tumor necrosis factor-alpha in the neonatal rat. Pediatr Res 56 (2004) 377-384
12. Chai Z., Gatti S., Toniatti C., Poli V., and Bartfai T. Interleukin (IL-6) gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL-1beta. a study on IL-6-deficient mice. J Exp Med 183 (1996) 311-316
13. Dammann O., and Leviton A. Infection remote from the brain, neonatal white matter damage, and cerebral palsy in the preterm infant. Semin Pediatr Neurol 5 (1998) 190-201
14. Dammann O., and Leviton A. Inflammatory brain damage in preterm newborns. dry numbers, wet lab, and causal inferences. Early Hum Dev 79 (2004) 1-15
15. Deguchi K., Oguchi K., and Takashima S. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol 16 (1997) 296-300
16. Ellison V.J., Mocatta T.J., Winterbourn C.C., Darlow B.A., Volpe J.J., and Inder T.E. The relationship of CSF and plasma cytokine levels to cerebral white matter injury in the premature newborn. Pediatr Res 57 (2005) 282-286
17. Fan L.W., Pang Y., Lin S., Tien L.T., Ma T., Rhodes P.G., and Cai Z. Minocycline reduces lipopolysaccharide-induced neurological dysfunction and brain injury in the neonatal rat. J Neurosci Res 23 82 (2005) 71-82
18. Frei K., Fredrikson S., Fontana A., and Link H. Interleukin-6 is elevated in plasma in multiple sclerosis. J Neuroimmunol 31 (1991) 147-153
19. Goepfert A.R., Andrews W.W., Carlo W., Ramsey P.S., Cliver S.P., Goldenberg R.L., and Hauth J.C. Umbilical cord plasma interleukin-6 concentrations in preterm infants and risk of neonatal morbidity. Am J Obstet Gynecol 191 (2004) 1375-1381
20. Grether J.K., and Nelson K.B. Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278 (1997) 207-211
21. Hagberg H., Peebles D., and Mallard C. Models of white matter injury. comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 8 (2002) 30-38
22. Hermans R.H., Hunter D.E., McGivern R.F., Cain C.D., and Longo L.D. Behavioral sequelae in young rats of acute intermittent antenatal hypoxia. Neurotoxicol Teratol 14 (1992) 119-129
23. Klein M.A., Moller J.C., Jones L.L., Bluethmann H., Kreutzberg G.W., and Raivich G. Impaired neuroglial activation in interleukin-6-deficient mice. Glia 19 (1997) 227-233
24. Kossmann T., Hans V., Imhof H.G., Trentz O., and Morganti-Kossmann M.C. Interleukin-6 released in human cerebrospinal fluid following traumatic brain injury may trigger nerve growth factor production in astrocytes. Brain Res 713 (1996) 143-152
25. Leviton A., Paneth N., Reuss M.L., Susser M., Allred E.N., Dammann O., Kuban K., Van Marter L.J., Pagano M., Hegyi T., Hiatt M., Sanocka U., Shahrivar F., Abiri M., Disalvo D., Doubilet P., Kairam R., Kazam E., Kirpekar M., Rosenfeld D., Schonfeld S., Share J., Collins M., Genest D., Shen-Schwarz S., et al. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Developmental Epidemiology Network Investigators. Pediatr Res 46 (1999) 566-575
26. Loddick S.A., Turnbull A.V., and Rothwell N.J. Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 18 (1998) 176-179
27. Marz P., Otten U., and Rose-John S. Neural activity of IL-6-type cytokines often depend on soluble cytokine receptors. Eur J Neurosci 11 (1999) 2995-3004
28. Mendel I., Katz A., Kozak N., Ben-Nun A., and Revel M. Interleukin-6 functions in autoimmune encephalomyelitis. a study in gene-targeted mice. Eur J Immunol 28 (1998) 1727-1737
29. Muller T., Blum-Degen D., Przuntek H., and Kuhn W. Interleukin-6 levels in cerebrospinal fluid inversely correlate to severity of Parkinson's disease. Acta Neurol Scand 98 (1998) 142-144
30. Ohgi S., Akiyama T., and Fukuda M. Neurobehavioural profile of low-birthweight infants with cystic periventricular leukomalacia. Dev Med Child Neurol 47 (2005) 221-228
31. Okuda Y., Sakoda S., Fujimura H., Saeki Y., Kishimoto T., and Yanagihara T. IL-6 plays a crucial role in the induction phase of myelin oligodendrocyte glucoprotein 35-55 induced experimental autoimmune encephalomyelitis. J Neuroimmunol 101 (1999) 188-196
32. Olsen P., Vainionpaa L., Paakko E., Korkman M., Pyhtinen J., and Jarvelin M.R. Psychological findings in preterm children related to neurologic status and magnetic resonance imaging. Pediatrics 102 (1998) 329-336
33. Pang Y., Cai Z., and Rhodes P. Disturbance of oligodendrocyte development. hypomyelination and white matter injury in the neonatal rat brain after intracerebral injection of lipopolysaccharide. Brain Res Dev Brain Res 140 (2003) 205-214
34. Pang Y., Cai Z., and Rhodes P. Effect of tumor necrosis factor-alpha on developing optic nerve oligodendrocytes in culture. J Neurosci Res 80 (2005) 226-234
35. Penkowa M., Molinero A., Carrasco J., and Hidalgo J. Interleukin-6 deficiency reduces the brain inflammatory response and increases oxidative stress and neurodegeneration after kainic acid-induced seizures. Neuroscience 102 (2001) 805-818
36. Pousset F. Cytokines as mediators in the central nervous system. Biomed Pharmacother 48 (1994) 425-431
37. Roscigno C. Periventricular leukomalacia. pathophysiological concerns due to immature development of the brain. J Neurosci Nurs 34 (2002) 296-302
38. Sasaki K., Fan L.W., Tien L.T., Ma T., Loh H.H., and Ho I.K. The interaction of morphine and gamma-aminobutyric acid (GABA)ergic systems in anxiolytic behavior. using mu-opioid receptor knockout mice. Brain Res Bull 57 (2002) 689-694
39. Shen Y., Isaacson R.L., and Smotherman W.P. The behavioral and anatomical effects of prenatal umbilical cord clamping in the rat and their alteration by the prior maternal administration of nimodipine. Rest Neurol Neurosci 3 (1991) 11-22
40. Sherwin C., and Fern R. Acute lipopolysaccharide-mediated injury in neonatal white matter glia. role of TNF-α, IL-1β, and calcium. J Immunol 175 (2005) 155-161
41. Stolp H.B., Dziegielewska K.M., Ek C.J., Potter A.M., and Saunders N.R. Long-term changes in blood-brain barrier permeability and white matter following prolonged systemic inflammation in early development in the rat. Eur J Neurosci 22 (2005) 2805-2816
42. Takahashi J.L., Giuliani F., Power C., Imai Y., and Yong V.W. Interleukin-1beta promotes oligodendrocyte death through glutamate excitotoxicity. Ann Neurol 53 (2003) 588-595
43. Tien L.T., Park Y., Fan L.W., Ma T., Loh H.H., and Ho I.K. Increased dopamine D2 receptor binding and enhanced apomorphine-induced locomotor activity in mu-opioid receptor knockout mice. Brain Res Bull 61 (2003) 109-115
44. Toulmond S., Vige X., Fage D., and Benavides J. Local infusion of interleukin-6 attenuates the neurotoxic effects of NMDA on rat striatal cholinergic neurons. Neurosci Lett 144 (1992) 49-52
45. Valerio A., Ferrario M., Dreano M., Garotta G., Spano P., and Pizzi M. Soluble interleukin-6 (IL6) receptor/IL-6 fusion protein enhances in vitro differentiation of purified rat oligodendroglial lineage cells. Mol Cell Neurosci 21 (2002) 602-615
46. Vallieres L., and Rivest S. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta. J Neurochem 69 (1997) 1668-1683
47. Vallieres L., and Rivest S. Interleukin-6 is a needed proinflammatory cytokine in the prolonged neural activity and transcriptional activation of corticotropin-releasing factor during endotoxemia. Endocrinology 140 (1999) 3890-3903
48. Yamada M., and Hatanaka H. Interleukin-6 protects cultured rat hippocampal neurons against glutamate-induced cell death. Brain Res 643 (1994) 173-180
49. Yoon B.H., Jun J.K., Romero R., Park K.H., Gomez R., Choi J.H., and Kim I.O. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 177 (1997) 19-26
50. Yoon B.H., Romero R., Kim C.J., Koo J.N., Choe G., Syn H.C., and Chi J.G. High expression of tumor necrosis factor-alpha and interleukin-6 in periventricular leukomalacia. Am J Obstet Gynecol 177 (1997) 406-411
51. Yoon B.H., Park C.W., and Chaiworapongsa T. Intrauterine infection and the development of cerebral palsy. BJOG 110 (2003) 124-127