Intrauterine administration of endotoxin leads to motor deficits in a rabbit model: a link between prenatal infection and cerebral palsy

American Journal of Obstetrics and Gynecology

Volumn 199, Issue 6, 2008, Pages 651.e1-651.e7

  Saadani Makki, Fadoua ^a   Kannan, Sujatha ^a   Lu, Xin ^a   Janisse, James ^a   Dawe, Elizabeth ^a   Edwin, Samuel ^b   Romero, Roberto ^a,b   Chugani, Diane ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

cerebral palsy; intrauterine inflammation; microglia; perinatal brain injury

Indexed keywords

C REACTIVE PROTEIN; ENDOTOXIN; LIPOPOLYSACCHARIDE; MYELIN; SODIUM CHLORIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CEREBRAL PALSY; CONTROLLED STUDY; FEEDING; INTRAUTERINE INFECTION; LOCOMOTION; MICROGLIA; MORTALITY; MOTOR DYSFUNCTION; MYOMETRIUM; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; RABBIT; RIGHTING REFLEX; STAINING; WHITE MATTER;

EID: 57149133787     PISSN: 00029378     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ajog.2008.06.090     Document Type: Article

References (39)

1. Bax M., Goldstein M., Rosenbaum P., et al. Proposed definition and classification of cerebral palsy, April 2005. Dev Med Child Neurol 47 (2005) 571-576
2. Koman L.A., Smith B.P., and Shilt J.S. Cerebral palsy. Lancet 363 (2004) 1619-1631
3. Dammann O., and Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42 (1997) 1-8
4. Grether J.K., and Nelson K.B. Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278 (1997) 207-211
5. Wu Y.W., and Colford Jr. J.M. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA 284 (2000) 1417-1424
6. Yoon B.H., Jun J.K., Romero R., et al. 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
7. Goepfert A.R., Andrews W.W., Carlo W., et al. Umbilical cord plasma interleukin-6 concentrations in preterm infants and risk of neonatal morbidity. Am J Obstet Gynecol 191 (2004) 1375-1381
8. Heep A., Behrendt D., Nitsch P., Fimmers R., Bartmann P., and Dembinski J. Increased serum levels of interleukin 6 are associated with severe intraventricular haemorrhage in extremely premature infants. Arch Dis Child Fetal Neonatal Ed 88 (2003) 501-504
9. Viscardi R.M., Muhumuza C.K., Rodriguez A., et al. Inflammatory markers in intrauterine and fetal blood and cerebrospinal fluid compartments are associated with adverse pulmonary and neurologic outcomes in preterm infants. Pediatr Res 55 (2004) 1009-1017
10. Redline R.W. Infections and other inflammatory conditions. Semin Diagn Pathol 24 (2007) 5-13
11. Haynes R.L., Folkerth R.D., Keefe R.J., et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 62 (2003) 441-450
12. Yoon B.H., Park C.W., and Chaiworapongsa T. Intrauterine infection and the development of cerebral palsy. BJOG 110 (2003) 124-127
13. Bell M.J., and Hallenbeck J.M. Effects of intrauterine inflammation on developing rat brain. J Neurosci Res 70 (2002) 570-579
14. Poggi S.H., Park J., Toso L., et al. No phenotype associated with established lipopolysaccharide model for cerebral palsy. Am J Obstet Gynecol 192 (2005) 727-733
15. Toso L., Poggi S., Park J., et al. Inflammatory-mediated model of cerebral palsy with developmental sequelae. Am J Obstet Gynecol 193 (2005) 933-941
16. Kannan S., Saadani-Makki F., Muzik O., et al. Microglial activation in perinatal rabbit brain induced by intrauterine inflammation: detection with 11C-(R)-PK11195 and small-animal PET. J Nucl Med 48 (2007) 946-954
17. Derrick M., Luo N.L., Bregman J.C., et al. Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy?. J Neurosci 24 (2004) 24-34
18. Castell J.V., Gómez-Lechón M.J., David M., Fabra R., Trullenque R., and Heinrich P.C. Acute-phase response of human hepatocytes: regulation of acute-phase protein synthesis by interleukin-6. Hepatology 12 (1990) 1179-1186
19. Yap S.H., Moshage H.J., Hazenberg B.P., et al. Tumor necrosis factor (TNF) inhibits interleukin (IL)-1 and/or IL-6 stimulated synthesis of C-reactive protein (CRP) and serum amyloid A (SAA) in primary cultures of human hepatocytes. Biochim Biophys Acta 1091 (1991) 405-408
20. Romem Y., and Artal R. C-reactive protein as a predictor for chorioamnionitis in cases of premature rupture of the membranes. Am J Obstet Gynecol 150 (1984) 546-550
21. Chen S.U., Ko T.M., Hwa H.L., Lu P.J., Ho H.N., and Yang Y.S. Maternal serum C-reactive protein level does not change significantly after fetal reduction: it could be used as an indicator of chorioamnionitis. J Assist Reprod Genet 18 (2001) 336-340
22. Gojnic M., Fazlagic A., Pervulov M., Petkovic S., Mostic T., and Jeremic K. The significance of C-reactive protein in the diagnosis of fetal tachycardia and therapy of chorioamnionitis. Clin Exp Obstet Gynecol 32 (2005) 114-116
23. Skrablin S., Lovric H., Banovic V., Kralik S., Dijakovic A., and Kalafatic D. Maternal plasma interleukin-6, interleukin-1beta and C-reactive protein as indicators of tocolysis failure and neonatal outcome after preterm delivery. J Matern Fetal Neonatal Med 20 (2007) 335-341
24. Drobyshevsky A., Song S.K., Gamkrelidze G., et al. Developmental changes in diffusion anisotropy coincide with immature oligodendrocyte progression and maturation of compound action potential. J Neurosci 25 (2005) 5988-5997
25. 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
26. Fields R.D. Myelination: an overlooked mechanism of synaptic plasticity?. Neuroscientist 11 (2005) 528-531
27. de Graaf-Peters V.B., and Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when?. Early Hum Dev 82 (2006) 257-266
28. Hildebrand C., Remahl S., Persson H., and Bjartman C. Myelinated nerve fibres in the CNS. Prog Neurobiol 40 (1993) 319-384
29. Craig A., Luo N.L., Beardsley D.J., et al. Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp Neurol 181 (2003) 231-240
30. Tan S., Drobyshevsky A., Jilling T., et al. Model of cerebral palsy in the perinatal rabbit. J Child Neurol 20 (2005) 972-979
31. Bass W.T., Singer G.A., and Liuzzi F.J. Transient lectin binding by white matter tract border zone microglia in the foetal rabbit brain. Histochem J 30 (1998) 657-666
32. 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
33. Rousset C.I., Chalon S., Cantagrel S., 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
34. Elovitz M.A., Wang Z., Chien E.K., Rychlik D.F., and Phillippe M. A new model for inflammation-induced preterm birth: the role of platelet activating factor and Toll-like receptor-4. Am J Pathol 163 (2003) 2103-2111
35. Back S.A., Han B.H., Luo N.L., et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22 (2002) 455-463
36. Lehnardt S., Lachance C., Patrizi S., et al. The toll-like receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 22 (2002) 2478-2486
37. Kauppinen T.M., and Swanson R.A. Poly(ADP-ribose) polymerase-1 promotes microglial activation, proliferation, and matrixmetalloproteinase-9-mediated neuron death. J Immunol 174 (2005) 2288-2296
38. Domercq M., Sánchez-Gómez M.V., Sherwin C., Etxebarria E., Fern R., and Matute C. System xc- and glutamate transporter inhibition mediates microglial toxicity to oligodendrocytes. J Immunol 178 (2007) 6549-6556
39. Billiards S.S., Haynes R.L., Folkerth R.D., et al. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol 497 (2006) 199-208