Erythropoietin and Neonatal Neuroprotection

Clinics in Perinatology

Volumn 42, Issue 3, 2015, Pages 469-481

  Juul, Sandra E ^a   Pet, Gillian C ^a  

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

Author keywords

Apoptosis; Autophagy; Brain injury; Erythropoietin; Extreme prematurity; Hypoxic ischemic encephalopathy; Necrosis

Indexed keywords

ERYTHROPOIETIN;

APOPTOSIS; AUTOPHAGY; BRAIN INJURY; DEVELOPMENTAL DISORDER; DISEASE SEVERITY; DRUG MECHANISM; HIGH RISK POPULATION; HORMONE ACTION; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NEUROPROTECTION; NEWBORN; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; REVIEW; HYPOXIA-ISCHEMIA, BRAIN;

ERYTHROPOIETIN; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INFANT, NEWBORN; NEUROPROTECTION;

EID: 84938546803     PISSN: 00955108     EISSN: 15579840     Source Type: Journal    
DOI: 10.1016/j.clp.2015.04.004     Document Type: Review

References (98)

1. Stoll B.J., Hansen N.I., Bell E.F., et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics 2010, 126(3):443-456.
2. Gargus R.A., Vohr B.R., Tyson J.E., et al. Unimpaired outcomes for extremely low birth weight infants at 18 to 22 months. Pediatrics 2009, 124(1):112-121.
3. McQuillen P.S., Miller S.P. Congenital heart disease and brain development. Ann N Y Acad Sci 2010, 1184:68-86.
4. Miller S.P., McQuillen P.S., Hamrick S., et al. Abnormal brain development in newborns with congenital heart disease. NEngl J Med 2007, 357(19):1928-1938.
5. Edwards A.D., Brocklehurst P., Gunn A.J., et al. Neurological outcomes at 18 months of age after moderate hypothermia for perinatal hypoxic ischaemic encephalopathy: synthesis and meta-analysis of trial data. BMJ 2010, 340:c363.
6. Hamilton B.E., Hoyert D.L., Martin J.A., et al. Annual summary of vital statistics: 2010-2011. Pediatrics 2013, 131(3):548-558.
7. Wu Y.W., Escobar G.J., Grether J.K., et al. Chorioamnionitis and cerebral palsy in term and near-term infants. JAMA 2003, 290(20):2677-2684.
8. Wu Y.W., Backstrand K.H., Zhao S., et al. Declining diagnosis of birth asphyxia in California: 1991-2000. Pediatrics 2004, 114(6):1584-1590.
9. Wu Y.W., Croen L.A., Shah S.J., et al. Cerebral palsy in a term population: risk factors and neuroimaging findings. Pediatrics 2006, 118(2):690-697.
10. Tagin M.A., Woolcott C.G., Vincer M.J., et al. Hypothermia for neonatal hypoxic ischemic encephalopathy: an updated systematic review and meta-analysis. Arch Pediatr Adolesc Med 2012, 166(6):558-566.
11. Leavitt A.M., Watchko J.F., Bennett F.C., et al. Neurodevelopmental outcome following persistent pulmonary hypertension of the neonate. JPerinatol 1987, 7(4):288-291.
12. Rohana J., Boo N.Y., Chandran V., et al. Neurodevelopmental outcome of newborns with persistent pulmonary hypertension. Malays J Med Sci 2011, 18(4):58-62.
13. Rosenberg A.A., Lee N.R., Vaver K.N., et al. School-age outcomes of newborns treated for persistent pulmonary hypertension. JPerinatol 2010, 30(2):127-134.
14. Eriksen V., Nielsen L.H., Klokker M., et al. Follow-up of 5- to 11-year-old children treated for persistent pulmonary hypertension of the newborn. Acta Paediatr 2009, 98(2):304-309.
15. Miller S.P., McQuillen P.S., Vigneron D.B., et al. Preoperative brain injury in newborns with transposition of the great arteries. Ann Thorac Surg 2004, 77(5):1698-1706.
16. McQuillen P.S., Barkovich A.J., Hamrick S.E., et al. Temporal and anatomic risk profile of brain injury with neonatal repair of congenital heart defects. Stroke 2007, 38(Suppl 2):736-741.
17. Miller S.P., McQuillen P.S. Neurology of congenital heart disease: insight from brain imaging. Arch Dis Child Fetal Neonatal Ed 2007, 92(6):F435-F437.
18. Wu Y.W., Lynch J.K., Nelson K.B. Perinatal arterial stroke: understanding mechanisms and outcomes. Semin Neurol 2005, 25(4):424-434.
19. Nelson K.B. Perinatal ischemic stroke. Stroke 2007, 38(Suppl 2):742-745.
20. Raju T.N., Nelson K.B., Ferriero D., NICHD-NINDS Perinatal Stroke Workshop Participants, et al. Ischemic perinatal stroke: summary of a workshop sponsored by the National Institute of Child Health and Human Development and the National Institute of Neurological Disorders and Stroke. Pediatrics 2007, 120(3):609-616.
21. Lynch J.K., Nelson K.B. Epidemiology of perinatal stroke. Curr Opin Pediatr 2001, 13(6):499-505.
22. Rajagopalan V., Scott J.A., Habas P.A., et al. Local tissue growth patterns underlying normal fetal human brain gyrification quantified in utero. JNeurosci 2011, 31(8):2878-2887.
23. Lodygensky G.A., Vasung L., Sizonenko S.V., et al. Neuroimaging of cortical development and brain connectivity in human newborns and animal models. JAnat 2010, 217(4):418-428.
24. Huppi P.S. Growth and development of the brain and impact on cognitive outcomes. Nestle Nutr Workshop Ser Pediatr Program 2010, 65:137-149. [discussion 149-51].
25. Zhang L.L., Fina M.E., Vardi N. Regulation of KCC2 and NKCC during development: membrane insertion and differences between cell types. JComp Neurol 2006, 499(1):132-143.
26. Li H., Khirug S., Cai C., et al. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 2007, 56(6):1019-1033.
27. McQuillen P.S., Ferriero D.M. Selective vulnerability in the developing central nervous system. Pediatr Neurol 2004, 30(4):227-235.
28. Volpe J.J. The encephalopathy of prematurity-brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 2009, 16(4):167-178.
29. Back S.A., Riddle A., McClure M.M. Maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 2007, 38(Suppl 2):724-730.
30. Back S.A., Gan X., Li Y., et al. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. JNeurosci 1998, 18(16):6241-6253.
31. Volpe J.J. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009, 8(1):110-124.
32. Ment L.R., Bada H.S., Barnes P., et al. Practice parameter: neuroimaging of the neonate: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology 2002, 58(12):1726-1738.
33. Buser J.R., Maire J., Riddle A., et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012, 71(1):93-109.
34. Riddle A., Dean J., Buser J.R., et al. Histopathological correlates of magnetic resonance imaging-defined chronic perinatal white matter injury. Ann Neurol 2011, 70(3):493-507.
35. Mallard C., Davidson J.O., Tan S., et al. Astrocytes and microglia in acute cerebral injury underlying cerebral palsy associated with preterm birth. Pediatr Res 2014, 75(1-2):234-240.
36. Hintz S.R., Kendrick D.E., Stoll B.J., et al. Neurodevelopmental and growth outcomes of extremely low birth weight infants after necrotizing enterocolitis. Pediatrics 2005, 115(3):696-703.
37. Back S.A. Cerebral white and gray matter injury in newborns: new insights into pathophysiology and management. Clin Perinatol 2014, 41(1):1-24.
38. Kidokoro H., Neil J.J., Inder T.E. New MR imaging assessment tool to define brain abnormalities in very preterm infants at term. AJNR Am J Neuroradiol 2013, 34(11):2208-2214.
39. Strunk T., Inder T., Wang X., et al. Infection-induced inflammation and cerebral injury in preterm infants. Lancet Infect Dis 2014, 14(8):751-762.
40. Robertson N.J., Tan S., Groenendaal F., et al. Which neuroprotective agents are ready for bench to bedside translation in the newborn infant?. JPediatr 2012, 160(4):544-552.e4.
41. Northington F.J., Ferriero D.M., Graham E.M., et al. Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis. Neurobiol Dis 2001, 8(2):207-219.
42. Chavez-Valdez R., Martin L.J., Northington F.J. Programmed necrosis: a prominent mechanism of cell death following neonatal brain injury. Neurol Res Int 2012, 2012:257563.
43. Boland B., Nixon R.A. Neuronal macroautophagy: from development to degeneration. Mol Aspects Med 2006, 27(5-6):503-519.
44. Chaabane W., User S.D., El-Gazzah M., et al. Autophagy, apoptosis, mitoptosis and necrosis: interdependence between those pathways and effects on cancer. Arch Immunol Ther Exp (Warsz) 2013, 61(1):43-58.
45. Lakhani R., Vogel K.R., Till A., et al. Defects in GABA metabolism affect selective autophagy pathways and are alleviated by mTOR inhibition. EMBO Mol Med 2014, 6(4):551-566.
46. Bendix I., Schulze C., Haefen C., et al. Erythropoietin modulates autophagy signaling in the developing rat brain in an invivo model of oxygen-toxicity. Int J Mol Sci 2012, 13(10):12939-12951.
47. Zheng Y., Hou J., Liu J., et al. Inhibition of autophagy contributes to melatonin-mediated neuroprotection against transient focal cerebral ischemia in rats. JPharmacol Sci 2014, 124(3):354-364.
48. Jiang T., Yu J.T., Zhu X.C., et al. Ischemic preconditioning provides neuroprotection by induction of AMP-activated protein kinase-dependent autophagy in a rat model of ischemic stroke. Mol Neurobiol 2015, 51:220-229.
49. Zhu C., Xu F., Wang X., et al. Different apoptotic mechanisms are activated in male and female brains after neonatal hypoxia-ischaemia. JNeurochem 2006, 96(4):1016-1027.
50. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 1997, 57(10):1835-1840.
51. Tsujimoto Y., Shimizu S., Eguchi Y., et al. Bcl-2 and Bcl-xL block apoptosis as well as necrosis: possible involvement of common mediators in apoptotic andnecrotic signal transduction pathways. Leukemia 1997, 11(Suppl 3):380-382.
52. Yu X., Shacka J.J., Eells J.B., et al. Erythropoietin receptor signalling is required for normal brain development. Development 2002, 129(2):505-516.
53. Jantzie L.L., Miller R.H., Robinson S. Erythropoietin signaling promotes oligodendrocyte development following prenatal systemic hypoxic-ischemic brain injury. Pediatr Res 2013, 74(6):658-667.
54. Juul S.E., Yachnis A.T., Rojiani A.M., et al. Immunohistochemical localization of erythropoietin and its receptor in the developing human brain. Pediatr Dev Pathol 1999, 2(2):148-158.
55. Chen Z.Y., Warin R., Noguchi C.T. Erythropoietin and normal brain development: receptor expression determines multi-tissue response. Neurodegener Dis 2006, 3(1-2):68-75.
56. Chen Z.Y., Asavaritikrai P., Prchal J.T., et al. Endogenous erythropoietin signaling is required for normal neural progenitor cell proliferation. JBiol Chem 2007, 282(35):25875-25883.
57. Sakanaka M., Wen T.C., Matsuda S., et al. Invivo evidence that erythropoietin protects neurons from ischemic damage. Proc Natl Acad Sci USA 1998, 95(8):4635-4640.
58. Juul S.E., Anderson D.K., Li Y., et al. Erythropoietin and erythropoietin receptor in the developing human central nervous system. Pediatr Res 1998, 43(1):40-49.
59. Masuda S., Nagao M., Sasaki R. Erythropoietic, neurotrophic, and angiogenic functions of erythropoietin and regulation of erythropoietin production. Int J Hematol 1999, 70(1):1-6.
60. Masuda S., Okano M., Yamagishi K., et al. Anovel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. JBiol Chem 1994, 269(30):19488-19493.
61. Sugawa M., Sakurai Y., Ishikawa-Ieda Y., et al. Effects of erythropoietin on glial cell development; oligodendrocyte maturation and astrocyte proliferation. Neurosci Res 2002, 44(4):391-403.
62. Teramo K.A., Widness J.A., Clemons G.K., et al. Amniotic fluid erythropoietin correlates with umbilical plasma erythropoietin in normal and abnormal pregnancy. Obstet Gynecol 1987, 69(5):710-716.
63. Buescher U., Hertwig K., Wolf C., et al. Erythropoietin in amniotic fluid as a marker of chronic fetal hypoxia. Int J Gynaecol Obstet 1998, 60(3):257-263.
64. Teramo K.A., Widness J.A. Increased fetal plasma and amniotic fluid erythropoietin concentrations: markers of intrauterine hypoxia. Neonatology 2009, 95(2):105-116.
65. Mikovic Z., Mandic V., Parovic V., et al. Erythropoietin in amniotic fluid as a potential marker in distinction between growth restricted and constitutionally small fetuses. JMatern Fetal Neonatal Med 2014, 27(11):1134-1137.
66. Traudt C.M., McPherson R.J., Bauer L.A., et al. Concurrent erythropoietin and hypothermia treatment improve outcomes in a term nonhuman primate model of perinatal asphyxia. Dev Neurosci 2013, 35(6):491-503.
67. Brines M., Grasso G., Fiordaliso F., et al. Erythropoietin mediates tissue protection through an erythropoietin and common beta-subunit heteroreceptor. Proc Natl Acad Sci USA 2004, 101(41):14907-14912.
68. Juul S.E., Beyer R.P., Bammler T.K., et al. Microarray analysis of high-dose recombinant erythropoietin treatment of unilateral brain injury in neonatal mouse hippocampus. Pediatr Res 2009, 65(5):485-492.
69. Rangarajan V., Juul S.E. Erythropoietin: emerging role of erythropoietin in neonatal neuroprotection. Pediatr Neurol 2014, 51(4):481-488.
70. Shingo T., Sorokan S.T., Shimazaki T., et al. Erythropoietin regulates the invitro and invivo production of neuronal progenitors by mammalian forebrain neural stem cells. JNeurosci 2001, 21(24):9733-9743.
71. Tsai P.T., Ohab J.J., Kertesz N., et al. Acritical role of erythropoietin receptor in neurogenesis and post-stroke recovery. JNeurosci 2006, 26(4):1269-1274.
72. Wang L., Zhang Z., Wang Y., et al. Treatment of stroke with erythropoietin enhances neurogenesis and angiogenesis and improves neurological function in rats. Stroke 2004, 35(7):1732-1737.
73. Jantzie L.L., Corbett C.J., Firl D.J., et al. Postnatal erythropoietin mitigates impaired cerebral cortical development following subplate loss from prenatal hypoxia-ischemia. Cereb Cortex 2014, 10.1093/cercor/bhu066.
74. Juul S.E., Ferriero D.M. Pharmacologic neuroprotective strategies in neonatal brain injury. Clin Perinatol 2014, 41(1):119-131.
75. Digicaylioglu M., Lipton S.A. Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 2001, 412(6847):641-647.
76. Masuda S., Kada E., Nagao M., et al. Invitro neuroprotective action of recombinant rat erythropoietin produced by astrocyte cell lines and comparative studies with erythropoietin produced by Chinese hamster ovary cells. Cytotechnology 1999, 29(3):207-213.
77. Gunnarson E., Song Y., Kowalewski J.M., et al. Erythropoietin modulation of astrocyte water permeability as a component of neuroprotection. Proc Natl Acad Sci USA 2009, 106(5):1602-1607.
78. Sinor A.D., Greenberg D.A. Erythropoietin protects cultured cortical neurons, but not astroglia, from hypoxia and AMPA toxicity. Neurosci Lett 2000, 290(3):213-215.
79. Cho Y.K., Kim G., Park S., et al. Erythropoietin promotes oligodendrogenesis and myelin repair following lysolecithin-induced injury in spinal cord slice culture. Biochem Biophys Res Commun 2012, 417(2):753-759.
80. Iwai M., Stetler R.A., Xing J., et al. Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury. Stroke 2010, 41(5):1032-1037.
81. van der Kooij M.A., Groenendaal F., Kavelaars A., et al. Neuroprotective properties and mechanisms of erythropoietin in invitro and invivo experimental models for hypoxia/ischemia. Brain Res Rev 2008, 59(1):22-33.
82. Fan X., van Bel F., van der Kooij M.A., et al. Hypothermia and erythropoietin forneuroprotection after neonatal brain damage. Pediatr Res 2013, 73(1):18-23.
83. Fang A.Y., Gonzalez F.F., Sheldon R.A., et al. Effects of combination therapy using hypothermia and erythropoietin in a rat model of neonatal hypoxia-ischemia. Pediatr Res 2013, 73(1):12-17.
84. Juul S.E., McPherson R.J., Bauer L.A., et al. Aphase I/II trial of high-dose erythropoietin in extremely low birth weight infants: pharmacokinetics and safety. Pediatrics 2008, 122(2):383-391.
85. Fauchere J.C., Dame C., Vonthein R., et al. An approach to using recombinant erythropoietin for neuroprotection in very preterm infants. Pediatrics 2008, 122(2):375-382.
86. Ohls R.K., Kamath-Rayne B.D., Christensen R.D., et al. Cognitive outcomes of preterm infants randomized to darbepoetin. Pediatrics 2014, 10.1542/peds.2013-4307.
87. Leuchter R.H., Gui L., Poncet A., et al. Association between early administration of high-dose erythropoietin in preterm infants and brain MRI abnormality at term-equivalent age. JAMA 2014, 312(8):817-824.
88. Zhu C., Kang W., Xu F., et al. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics 2009, 124(2):e218-e226.
89. Wu Y.W., Bauer L.A., Ballard R.A., et al. Erythropoietin for neuroprotection in neonatal encephalopathy: safety and pharmacokinetics. Pediatrics 2012, 130(4):683-691.
90. Benders M.J., van der Aa N.E., Roks M., et al. Feasibility and safety of erythropoietin for neuroprotection after perinatal arterial ischemic stroke. JPediatr 2014, 164(3):481-486.e1-2.
91. Andropoulos D.B., Brady K., Easley R.B., et al. Erythropoietin neuroprotection in neonatal cardiac surgery: a phase I/II safety and efficacy trial. JThorac Cardiovasc Surg 2013, 146(1):124-131.
92. Kellert B.A., McPherson R.J., Juul S.E. Acomparison of high-dose recombinant erythropoietin treatment regimens in brain-injured neonatal rats. Pediatr Res 2007, 61(4):451-455.
93. Statler P.A., McPherson R.J., Bauer L.A., et al. Pharmacokinetics of high-dose recombinant erythropoietin in plasma and brain of neonatal rats. Pediatr Res 2007, 61(6):671-675.
94. Rogers E.E., Bonifacio S.L., Glass H.C., et al. Erythropoietin and hypothermia for hypoxic-ischemic encephalopathy. Pediatr Neurol 2014, 51(5):657-662.
95. McAdams R.M., McPherson R.J., Mayock D.E., et al. Outcomes of extremely low birth weight infants given early high-dose erythropoietin. JPerinatol 2013, 33(3):226-230.
96. Elmahdy H., El-Mashad A.R., El-Bahrawy H., et al. Human recombinant erythropoietin in asphyxia neonatorum: pilot trial. Pediatrics 2010, 125(5):e1135-e1142.
97. Pett G.C., Juul S.E. The potential of erythropoietin to treat asphyxia in newborns. Res Rep Neonatol 2014, 4:195-207.
98. Xiong Y., Mahmood A., Qu C., et al. Erythropoietin improves histological and functional outcomes after traumatic brain injury in mice in the absence of the neural erythropoietin receptor. JNeurotrauma 2010, 27(1):205-215.