Lipopolysaccharide-induced inflammation and perinatal brain injury

Seminars in Fetal and Neonatal Medicine

Volumn 11, Issue 5, 2006, Pages 343-353

  Wang, Xiaoyang ^a   Rousset, Catherine I ^a   Hagberg, Henrik ^a   Mallard, Carina ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Brain development; Inflammation; LPS; White matter damage

Indexed keywords

CYTOKINE; LIPOPOLYSACCHARIDE; MYELIN;

ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; EXPOSURE; HUMAN; INFLAMMATION; INFLAMMATORY CELL; NONHUMAN; OLIGODENDROGLIA; PERINATAL MORBIDITY; PREDICTOR VARIABLE; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; BRAIN INJURIES; DISEASE MODELS, ANIMAL; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; RATS; RISK FACTORS; SHEEP;

EID: 33745862750     PISSN: 1744165X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.siny.2006.04.002     Document Type: Article

References (60)

1. Wu Y.W. Systematic review of chorioamnionitis and cerebral palsy. Ment Retard Dev Disabil Res Rev 8 (2002) 25-29
2. Leviton A., Paneth N., Reuss M.L., Susser M., Allred E.N., Dammann O., 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
3. Yoon B.H., Romero R., Park J.S., Kim C.J., Kim S.H., Choi J.H., et al. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol 182 (2000) 675-681
4. Yoon B.H., Romero R., Yang S.H., Jun J.K., Kim I.O., Choi J.H., et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 174 (1996) 1433-1440
5. Grether J.K., and Nelson K.B. Maternal infection and cerebral palsy in infants of normal birth weight. J Am Med Assoc 278 (1997) 207-211
6. Nelson K.B., and Grether J.K. Potentially asphyxiating conditions and spastic cerebral palsy in infants of normal birth weight. Am J Obstet Gynecol 179 (1998) 507-513
7. Wu Y.W., Escobar G.J., Grether J.K., Croen L.A., Greene J.D., and Newman T.B. Chorioamnionitis and cerebral palsy in term and near-term infants. JAMA 290 (2003) 2677-2684
8. Redline R.W., and O'Riordan M.A. Placental lesions associated with cerebral palsy and neurologic impairment following term birth. Arch Pathol Lab Med 124 (2000) 1785-1791
9. Park J.S., Romero R., Yoon B.H., Moon J.B., Oh S.Y., Han S.Y., et al. The relationship between amniotic fluid matrix metalloproteinase-8 and funisitis. Am J Obstet Gynecol 185 (2001) 1156-1161
10. Neufeld M.D., Frigon C., Graham A.S., and Mueller B.A. Maternal infection and risk of cerebral palsy in term and preterm infants. J Perinatol 25 (2005) 108-113
11. Morgan K.L. Management of UTIs during pregnancy. MCN Am J Matern Child Nurs 29 (2004) 254-258
12. 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
13. Hagberg H., and Mallard C. Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 18 (2005) 117-123
14. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282 (1998) 2085-2088
15. Akira S., Uematsu S., and Takeuchi O. Pathogen recognition and innate immunity. Cell 124 (2006) 783-801
16. Beutler B. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430 (2004) 257-263
17. Coumans A.B., Middelanis J.S., Garnier Y., Vaihinger H.M., Leib S.L., Von Duering M.U., et al. Intracisternal application of endotoxin enhances the susceptibility to subsequent hypoxic-ischemic brain damage in neonatal rats. Pediatr Res 53 (2003) 770-775
18. Lehnardt S., Lachance C., Patrizi S., Lefebvre S., Follett P.L., Jensen F.E., et al. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22 (2002) 2478-2486
19. Pang Y., Cai Z., and Rhodes P.G. 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
20. 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
21. Duncan J.R., Cock M.L., Scheerlinck J.P., Westcott K.T., McLean C., Harding R., et al. White matter injury after repeated endotoxin exposure in the preterm ovine fetus. Pediatr Res 52 (2002) 941-949
22. Mallard C., Welin A.K., Peebles D., Hagberg H., and Kjellmer I. White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 28 (2003) 215-223
23. Peebles D.M., Miller S., Newman J.P., Scott R., and Hanson M.A. The effect of systemic administration of lipopolysaccharide on cerebral haemodynamics and oxygenation in the 0.65 gestation ovine fetus in utero. Br J Obstet Gynaecol 110 (2003) 735-743
24. Garnier Y., Berger R., Alm S., von Duering M.U., Coumans A.B., Michetti F., et al. Systemic endotoxin administration results in increased S100B protein blood levels and periventricular brain white matter injury in the preterm fetal sheep. Eur J Obstet Gynecol Reprod Biol 124 (2006) 15-22
25. Svedin P., Kjellmer I., Welin A.K., Blad S., and Mallard C. Maturational effects of lipopolysaccharide on white-matter injury in fetal sheep. J Child Neurol 20 (2005) 960-967
26. Back S.A., Han B.H., Luo N.L., Chricton C.A., Xanthoudakis S., Tam J., et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22 (2002) 455-463
27. Duncan J.R., Cock M.L., Suzuki K., Scheerlinck J.P., Harding R., and Rees S.M. Chronic endotoxin exposure causes brain injury in the ovine fetus in the absence of hypoxemia. J Soc Gynecol Investig 13 (2006) 87-96
28. Rounioja S., Rasanen J., Glumoff V., Ojaniemi M., Makikallio K., and Hallman M. Intra-amniotic lipopolysaccharide leads to fetal cardiac dysfunction. A mouse model for fetal inflammatory response. Cardiovasc Res 60 (2003) 156-164
29. Bell M.J., Hallenbeck J.M., and Gallo V. Determining the fetal inflammatory response in an experimental model of intrauterine inflammation in rats. Pediatr Res 56 (2004) 541-546
30. Elovitz M.A., Mrinalini C., and Sammel M.D. Elucidating the early signal transduction pathways leading to fetal brain injury in preterm birth. Pediatr Res 59 (2006) 50-55
31. Kramer B.W., Moss T.J., Willet K.E., Newnham J.P., Sly P.D., Kallapur S.G., et al. Dose and time response after intraamniotic endotoxin in preterm lambs. Am J Respir Crit Care Med 164 (2001) 982-988
32. Poggi S.H., Park J., Toso L., Abebe D., Roberson R., Woodard J.E., et al. No phenotype associated with established lipopolysaccharide model for cerebral palsy. Am J Obstet Gynecol 192 (2005) 727-733
33. Bell M.J., and Hallenbeck J.M. Effects of intrauterine inflammation on developing rat brain. J Neurosci Res 70 (2002) 570-579
34. Silver R.M., Edwin S.S., Trautman M.S., Simmons D.L., Branch D.W., Dudley D.J., et al. Bacterial lipopolysaccharide-mediated fetal death. Production of a newly recognized form of inducible cyclooxygenase (COX-2) in murine decidua in response to lipopolysaccharide. J Clin Invest 95 (1995) 725-731
35. Cai Z., Pan Z.L., Pang Y., Evans O.B., and Rhodes P.G. Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr Res 47 (2000) 64-72
36. Paintlia M.K., Paintlia A.S., Barbosa E., Singh I., and Singh A.K. N-acetylcysteine prevents endotoxin-induced degeneration of oligodendrocyte progenitors and hypomyelination in developing rat brain. J Neurosci Res 78 (2004) 347-361
37. Deb K., Chaturvedi M.M., and Jaiswal Y.K. A 'minimum dose' of lipopolysaccharide required for implantation failure: assessment of its effect on the maternal reproductive organs and interleukin-1alpha expression in the mouse. Reproduction 128 (2004) 87-97
38. Ashdown H., Dumont Y., Ng M., Poole S., Boksa P., and Luheshi G.N. The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol Psychiatr 11 (2006) 47-55
39. Kohmura Y., Kirikae T., Kirikae F., Nakano M., and Sato I. Lipopolysaccharide (LPS)-induced intra-uterine fetal death (IUFD) in mice is principally due to maternal cause but not fetal sensitivity to LPS. Microbiol Immunol 44 (2000) 897-904
40. Urakubo A., Jarskog L.F., Lieberman J.A., and Gilmore J.H. Prenatal exposure to maternal infection alters cytokine expression in the placenta, amniotic fluid, and fetal brain. Schizophr Res 47 (2001) 27-36
41. Gayle D.A., Beloosesky R., Desai M., Amidi F., Nunez S.E., and Ross M.G. Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain. Am J Physiol Regul Integr Comp Physiol 286 (2004) R1024-R1029
42. Beloosesky R., Gayle D.A., Amidi F., Nunez S.E., Babu J., Desai M., et al. N-acetyl-cysteine suppresses amniotic fluid and placenta inflammatory cytokine responses to lipopolysaccharide in rats. Am J Obstet Gynecol 194 (2006) 268-273
43. Rousset C.I., Chalon S., Cantagrel S., Bodard S., Andres C., Gressens P., et al. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 59 (2006) 428-433
44. Gilmore J.H., Jarskog L.F., and Vadlamudi S. Maternal infection regulates BDNF and NGF expression in fetal and neonatal brain and maternal-fetal unit of the rat. J Neuroimmunol 138 (2003) 49-55
45. Golan H.M., Lev V., Hallak M., Sorokin Y., and Huleihel M. Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 48 (2005) 903-917
46. Ling Z., Chang Q.A., Tong C.W., Leurgans S.E., Lipton J.W., and Carvey P.M. Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Exp Neurol 190 (2004) 373-383
47. Bilbo S.D., Biedenkapp J.C., Der-Avakian A., Watkins L.R., Rudy J.W., and Maier S.F. Neonatal infection-induced memory impairment after lipopolysaccharide in adulthood is prevented via caspase-1 inhibition. J Neurosci 25 (2005) 8000-8009
48. 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
49. Eklind S, Hagberg H, Wang X, Sävman K, Hedtjärn M, Leverin AL, et al. Effect of lipopolysaccharide on global gene expression in the immature rat brain. Pediatr Res, in press.
50. Eklind S., Mallard C., Leverin A.L., Gilland E., Blomgren K., Mattsby-Baltzer I., et al. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 13 (2001) 1101-1106
51. Yang L., Sameshima H., Ikeda T., and Ikenoue T. Lipopolysaccharide administration enhances hypoxic-ischemic brain damage in newborn rats. J Obstet Gynaecol Res 30 (2004) 142-147
52. Yang L., Sameshima H., Yamaguchi M., and Ikenoue T. Expression of inducible nitric oxide synthase and cyclooxygenase-2 mRNA in brain damage induced by lipopolysaccharide and intermittent hypoxia-ischemia in neonatal rats. J Obstet Gynaecol Res 31 (2005) 185-191
53. Ikeda T., Mishima K., Aoo N., Liu A.X., Egashira N., Iwasaki K., et al. Dexamethasone prevents long-lasting learning impairment following a combination of lipopolysaccharide and hypoxia-ischemia in neonatal rats. Am J Obstet Gynecol 192 (2005) 719-726
54. Lehnardt S., Massillon L., Follett P., Jensen F.E., Ratan R., Rosenberg P.A., et al. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci U S A 100 (2003) 8514-8519
55. Eklind S., Arvidsson P., Hagberg H., and Mallard C. The role of glucose in brain injury following the combination of lipopolysaccharide or lipoteichoic acid and hypoxia-ischemia in neonatal rats. Dev Neurosci 26 (2004) 61-67
56. Eklind S., Mallard C., Arvidsson P., and Hagberg H. Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 58 (2005) 112-116
57. Larouche A., Roy M., Kadhim H., Tsanaclis A.M., Fortin D., and Sebire G. Neuronal injuries induced by perinatal hypoxic-ischemic insults are potentiated by prenatal exposure to lipopolysaccharide: animal model for perinatally acquired encephalopathy. Dev Neurosci 27 (2005) 134-142
58. Spencer S.J., Auer R.N., and Pittman Q.J. Rat neonatal immune challenge alters adult responses to cerebral ischaemia. J Cereb Blood Flow Metab (2005)
59. Ikeda T., Yang L., Ikenoue T., Mallard C., and Hagberg H. Endotoxin-induced hypoxic-ischemic tolerance is mediated by up-regulation of corticosterone in neonatal rat. Pediatr Res 59 (2006) 56-60
60. Perry V.H., Newman T.A., and Cunningham C. The impact of systemic infection on the progression of neurodegenerative disease. Nat Rev Neurosci 4 (2003) 103-112