Erythropoietin is neuroprotective in a preterm ovine model of endotoxin-induced brain injury

Journal of Neuropathology and Experimental Neurology

Volumn 69, Issue 3, 2010, Pages 306-319

  Rees, Sandra ^a   Hale, Nadia ^a   De Matteo, Robert ^b   Cardamone, Lisa ^b   Tolcos, Mary ^a   Loeliger, Michelle ^a   MacKintosh, Anna ^a   Shields, Amy ^a   Probyn, Megan ^b   Greenwood, Deanne ^a   Harding, Richard ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

Erythropoietin; Fetal brain injury; Inflammation; Neuroprotection

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; HEMOGLOBIN; INTERLEUKIN 6; LACTIC ACID; LIPOPOLYSACCHARIDE; MYELIN ASSOCIATED GLYCOPROTEIN; MYELIN BASIC PROTEIN; NEURON SPECIFIC NUCLEAR PROTEIN; RECOMBINANT ERYTHROPOIETIN; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL PH; ARTICLE; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN INFARCTION; BRAIN INJURY; BRAIN WEIGHT; CARBON DIOXIDE TENSION; CELL DEATH; CELL LINEAGE; CONTROLLED STUDY; FETUS; FETUS HYPOXIA; FETUS WEIGHT; GESTATIONAL AGE; HEMATOCRIT; HISTOPATHOLOGY; HYPOTENSION; MEAN ARTERIAL PRESSURE; MYELINATION; NEUROFILAMENT; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; OPTIC NERVE INJURY; OXYGEN SATURATION; OXYGEN TENSION; PREMATURITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYRAMIDAL TRACT; SHEEP; WHITE MATTER;

ANIMALS; BRAIN; BRAIN DAMAGE, CHRONIC; DEMYELINATING DISEASES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENCEPHALITIS; ENDOTOXINS; ERYTHROPOIETIN; FEMALE; FETAL DISEASES; FETAL HYPOXIA; INJECTIONS, INTRAVENOUS; LIPOPOLYSACCHARIDES; NERVE FIBERS, MYELINATED; NEUROPROTECTIVE AGENTS; OPTIC NERVE; PREGNANCY; SHEEP, DOMESTIC; TREATMENT OUTCOME;

EID: 77649246718     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3181d27138     Document Type: Article

References (54)

1. Holling EE, Leviton A. Characteristics of cranial ultrasound white-matter echolucencies that predict disability: A review. Dev Med Child Neurol 1999;41:136-139
2. Marlow N, Wolke D, Bracewell MA, et al. Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 2005;352:9-19
3. Hack M. Young adult outcomes of very-low-birth-weight children. Semin Fetal Neonatal Med 2006;11:127-137
4. Dammann O, Leviton A. Intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 1997;42:1-8
5. Dammann O, Leviton A. Inflammatory brain damage in preterm newbornsVdry numbers, wet lab, and causal inferences. Early Hum Dev 2004;79:1-15
6. Volpe JJ. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001;50:553-562
7. Yoon BH, Jun JK, Romero R, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1 beta, and tumor necrosis factor-alpha), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997;177:19-26
8. Duggan PJ, Maalouf EF, Watts TL, et al. Intrauterine T-cell activation and increased proinflammatory cytokine concentrations in preterm infants with cerebral lesions. Lancet 2001;358:1699-1700
9. Deguchi K, Mizuguchi M, Takashima S. Immunohistochemical expression of tumor necrosis factor alpha in neonatal leukomalacia. Pediatr Neurol 1996;14:13-16
10. Duncan JR, Cock ML, Scheerlinck JP, et al. White matter injury after repeated endotoxin exposure in the preterm ovine fetus. Pediatr Res 2002;52:941-949
11. Eklind S, Mallard C, Leverin AL, et al. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001;13: 1101-6
12. Duncan JR, Cock ML, Suzuki K, et al. Chronic endotoxin exposure causes brain injury in the ovine fetus in the absence of hypoxemia. J Soc Gynecol Investig 2006;13:87-96
13. Gluckman PD, Wyatt JS, Azzopardi D, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: Multicentre randomised trial. Lancet 2005;365:663-670
14. Gunn AJ, Wyatt JS, Whitelaw A, et al. Therapeutic hypothermia changes the prognostic value of clinical evaluation of neonatal enceph-alopathy. J Pediatr 2008;152:55-58
15. Gorio A, Gokmen N, Erbayraktar S, et al. Recombinant human erythropoietin counteracts secondary injury and markedly enhances neurological recovery from experimental spinal cord trauma. Proc Natl Acad Sci USA 2002;99:9450-9455
16. Siren AL, Fratelli M, Brines M, et al. Erythropoietin prevents neuronal apoptosis after cerebral ischemia and metabolic stress. Proc Natl Acad Sci USA 2001;98:4044-4049
17. Kawakami M, Sekiguchi M, Sato K, et al. Erythropoietin receptor-mediated inhibition of exocytotic glutamate release confers neuro-protection during chemical ischemia. J Biol Chem 2001;276:39469-39475
18. Genc K, Ggenc S, Baskin H, et al. Erythropoietin decreases cytotoxicity and nitric oxide formation induced by inflammatory stimuli in rat oligodendrocytes. Physiol Res 2006;55:33
19. Wang L, Zhang Z, Wang Y, et al. Treatment of stroke with erythropoi-etin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004;35:1732-1737
20. Kumral A, Baskin H, Gokmen N, et al. Selective inhibition of nitric oxide in hypoxic-ischemic brain model in newborn rats: Is it an explanation for the protective role of erythropoietin? Biol Neonate 2004;85:51-54
21. Campana WM, Myers RR. Erythropoietin and erythropoietin receptors in the peripheral nervous system: Changes after nerve injury. FASEB J 2001;15:1804-1806
22. Sakanaka M, Wen TC, Matsuda S, et al. In vivo evidence that erythropoi-etin protects neurons from ischemic damage. Proc Natl Acad Sci USA 1998;95:4635-4640
23. Demers EJ, McPherson RJ, Juul SE. Erythropoietin protects dopaminer-gic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005;58:297-301
24. Sola A, Wen TC, Hamrick SE, et al. Potential for protection and repair following injury to the developing brain: A role for erythropoietin? Pediatr Res 2005;57:110RY17R
25. Sun Y, Calvert JW, Zhang JH. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke 2005;36:1672-1678
26. Juul SE, McPherson RJ, Farrell FX, et al. Erythropoietin concentrations in cerebrospinal fluid of nonhuman primates and fetal sheep following high-dose recombinant erythropoietin. Biol Neonate 2004;85: 138-44
27. Loeliger M, Duncan J, Louey S, et al. Fetal growth restriction induced by chronic placental insufficiency has long-term effects on the retina but not the optic nerve. Invest Ophthalmol Vis Sci 2005;46:3300-3308
28. Stadelmann C, Lassmann H. Detection of apoptosis in tissue sections. Cell Tissue Res 2000;301:19-31
29. Munro K, Rees S, O'Dowd R, et al. Developmental profile of erythropoietin and its receptor in guinea-pig retina. Cell Tissue Res 2009;336:21-29
30. Jin Y, Silverman AJ, Vannucci SJ. Mast cell stabilization limits hypoxic-ischemic brain damage in the immature rat. Dev Neurosci 2007;29:373-384
31. Gundersen HJG, Jensen EB. The efficiency of systematic-sampling in stereology and its prediction. J Microsc 1987;147:229-263
32. Rees S, Stringer M, Just Y, et al. The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation. Brain Res Dev Brain Res 1997; 103:103-118
33. Loeliger M, Duncan J, Cock M, et al. Vulnerability of dopaminergic amacrine cells and optic nerve myelination to prenatal endotoxin exposure. Invest Ophthalmol Vis Sci 2007;48:472-478
34. Wu YW, Escobar GJ, Grether JK, et al. Chorioamnionitis and cerebral palsy in term and near-term infants. JAMA 2003;290:2677-2684
35. Dalitz P, Harding R, Rees SM, et al. Prolonged reductions in placental blood flow and cerebral oxygen delivery in preterm fetal sheep exposed to endotoxin: Possible factors in white matter injury after acute infection. J Soc Gynecol Investig 2003;10:283
36. Inder TE, Anderson NJ, Spencer C, et al. White matter injury in the premature infant: A comparison between serial cranial sonographic and MR findings at term. Am J Neuroradiol 2003;24:805-809
37. Stewart RM. Observations on the pathology of cerebral diplegia. Proc R Soc Med 1942;36:25-32
38. Staudt M, Pavlova M, Bohm S, et al. Pyramidal tract damage correlates with motor dysfunction in bilateral periventricular leukomalacia (PVL). Neuropediatrics 2003;34:182-188
39. Segovia KN, McClure M, Moravec M, et al. Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann Neurol 2008;63:520-530
40. Billiards SS, Haynes RL, Folkerth RD, et al. Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 2008;18:153-163
41. Rees S, Clark M, Snowden M, et al. The effects of intrauterine growth retardation on the structural development of cranial nerves (optic, trochlear) in fetal sheep. Int J Dev Neurosci 1990;8:133-141
42. Martinez-Estrada OM, Rodriguez-Millan E, Gonzalez-de Vicente E, et al. Erythropoietin protects the in vitro blood-brain barrier against VEGF-induced permeability. Eur J Neurosci 2003;18:2538-2544
43. Dawson DA, Martin D, Hallenbeck JM. Inhibition of tumor necrosis factor-alpha reduces focal cerebral ischemic injury in the spontaneously hypertensive rat. Neurosci Lett 1996;218:41-44
44. Tamatani M, Che YH, Matsuzaki H, et al. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NF kappa B activation in primary hippocampal neurons. J Biol Chem 1999;274:8531-8538
45. Taoufik E, Petit E, Divoux D, et al. TNF receptor I sensitizes neurons to erythropoietin-and VEGF-mediated neuroprotection after ischemic and excitotoxic injury. Proc Natl Acad Sci USA 2008;105: 6185-90
46. Villa P, Bigini P, Mennini T, et al. Erythropoietin selectively attenuates cytokine production and inflammation in cerebral ischemia by targeting neuronal apoptosis. J Exp Med 2003;198:971-975
47. Tahraoui SL, Marret S, Bodenant C, et al. Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 2001;11:56-71
48. Kinney HC. Human myelination and perinatal white matter disorders. J Neurol Sci 2005;228:190-192
49. Wilms H, Schwabedissen B, Sievers J, et al. Erythropoietin does not attenuate cytokine production and inflammation in microglia-implications for the neuroprotective effect of erythropoietin in neurological diseases. J Neuroimmunol 2009;212:106-111
50. Sharangpani A, Takanohashi A, Bell MJ. Caspase activation in fetal rat brain following experimental intrauterine inflammation. Brain Res 2008; 1200:138-145
51. Kellert BA, McPherson RJ, Juul SE. A comparison of high-dose re-combinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr Res 2007;61:451-455
52. Aher S, Ohlsson A. Late erythropoietin for preventing red blood cell transfusion in preterm and/or low birth weight infants [Review]. Cochrane Database Syst Rev 2006;3:CD004868.
53. Fauchere JC, Dame C, Vonthein R, et al. An approach to using recombinant erythropoietin for neuroprotection in very preterm infants. Pediatrics 2008;122:375-382
54. Juul SE, McPherson RJ, Bauer LA, et al. A phase I/II trial of high-dose erythropoietin in extremely low birth weight infants: Pharmacokinetics and safety. Pediatrics 2008;122:383-391