Pharmacological Preventions of Brain Injury Following Experimental Germinal Matrix Hemorrhage: an Up-to-Date Review

Translational Stroke Research

Volumn 7, Issue 1, 2016, Pages 20-32

  Tang, Jun ^a   Tao, Yihao ^a   Jiang, Bing ^a   Chen, Qianwei ^a   Hua, Feng ^a   Zhang, John ^b   Zhu, Gang ^a   Chen, Zhi ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal model; Germinal matrix hemorrhage; Posthemorrhagic hydrocephalus; Therapeutic strategy

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CANNABINOID 2 RECEPTOR; CORTICOSTEROID; INDOMETACIN; MAGNESIUM; PHENOBARBITAL; TRANSFORMING GROWTH FACTOR BETA; VITAMIN K GROUP;

ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INJURY; COMMUNICATING HYDROCEPHALUS; GERMINAL MATRIX HEMORRHAGE; GESTATIONAL AGE; GLIOSIS; HEART VENTRICLE VOLUME; HUMAN; MEAN ARTERIAL PRESSURE; MESENCHYMAL STEM CELL; MICROGLIA; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; OBSTRUCTIVE HYDROCEPHALUS; OXIDATIVE STRESS; PREMATURITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SUBARACHNOID HEMORRHAGE; SUBVENTRICULAR ZONE; ANIMAL; COMPLICATION; DISEASE MODEL; HYDROCEPHALUS; INTRACRANIAL HEMORRHAGES; STROKE;

ANIMALS; BRAIN EDEMA; DISEASE MODELS, ANIMAL; HYDROCEPHALUS; INTRACRANIAL HEMORRHAGES; STROKE;

EID: 84955395147     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-015-0432-8     Document Type: Review

References (115)

1. Ballabh P, Braun A, Nedergaard M. Anatomic analysis of blood vessels in germinal matrix, cerebral cortex, and white matter in developing infants. Pediatr Res. 2004;56:117–24.
2. Bassan H, Limperopoulos C, Visconti K, Mayer DL, Feldman HA, Avery L, et al. Neurodevelopmental outcome in survivors of periventricular hemorrhagic infarction. Pediatrics. 2007;120:785–92.
3. Robinson S. Neonatal posthemorrhagic hydrocephalus from prematurity: pathophysiology and current treatment concepts. J Neurosurg Pediatr. 2012;9:242–58.
4. Heron M, Sutton PD, Xu J, Ventura SJ, Strobino DM, Guyer B. Annual summary of vital statistics: 2007. Pediatrics. 2010;125:4–15.
5. Strahle J, Garton HJ, Maher CO, Muraszko KM, Keep RF, Xi G. Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage. Translational Stroke Res. 2012;3:25–38.
6. Lekic T, Manaenko A, Rolland W, Krafft PR, Peters R, Hartman RE, et al. Rodent neonatal germinal matrix hemorrhage mimics the human brain injury, neurological consequences, and post-hemorrhagic hydrocephalus. Exp Neurol. 2012;236:69–78.
7. Shennan AH, Bewley S. Why should preterm births be rising? BMJ. 2006;332:924–5.
8. Chen Z, Gao C, Hua Y, Keep RF, Muraszko K, Xi G. Role of iron in brain injury after intraventricular hemorrhage. Stroke: J Cereb Circulation. 2011;42:465–70.
9. Chen Q, Zhang J, Guo J, Tang J, Tao Y, Li L, et al. Chronic hydrocephalus and perihematomal tissue injury developed in a rat model of intracerebral hemorrhage with ventricular extension. Translational Stroke Res. 2015;6:125–32.
10. Guo J, Chen Q, Tang J, Zhang J, Tao Y, Li L, et al. Minocycline-induced attenuation of iron overload and brain injury after experimental germinal matrix hemorrhage. Brain Res. 2015;1594:115–24.
11. Tang J, Chen Q, Guo J, Yang L, Tao Y, Li L, et al. Minocycline attenuates neonatal germinal-matrix-hemorrhage-induced neuroinflammation and brain edema by activating cannabinoid receptor 2. Mol Neurobiol. 2015. doi:10.1007/s12035-015-9154-x.
12. Tang J, Tao Y, Tan L, Yang L, Niu Y, Chen Q, et al. Cannabinoid receptor 2 attenuates microglial accumulation and brain injury following germinal matrix hemorrhage via ERK dephosphorylation in vivo and in vitro. Neuropharmacology. 2015;95:424–33.
13. Tao Y, Tang J, Chen Q, Guo J, Li L, Yang L, et al. Cannabinoid CB2 receptor stimulation attenuates brain edema and neurological deficits in a germinal matrix hemorrhage rat model. Brain Res. 2015;1602:127–35.
14. Berger R, Bender S, Sefkow S, Klingmuller V, Kunzel W, Jensen A. Peri/intraventricular haemorrhage: a cranial ultrasound study on 5286 neonates. Eur J Obstet Gynecol Reprod Biol. 1997;75:191–203.
15. Tsitouras V, Sgouros S. Infantile posthemorrhagic hydrocephalus. Childs Nerv Syst: ChNS: Off J Int Soc Pediatr Neurosurg. 2011;27:1595–608.
16. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr. 1978;92:529–34.
17. Hintz SR, Barnes PD, Bulas D, Slovis TL, Finer NN, Wrage LA, et al. Neuroimaging and neurodevelopmental outcome in extremely preterm infants. Pediatrics. 2015;135:e32–42.
18. Roberts D, Dalziel S. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev. 2006;(3):CD004454
19. Whitelaw A. Intraventricular haemorrhage and posthaemorrhagic hydrocephalus: pathogenesis, prevention and future interventions. Semin Neonatol: SN. 2001;6:135–46.
20. Fowlie PW, Davis PG. Prophylactic indomethacin for preterm infants: a systematic review and meta-analysis. Arch Dis Child Fetal Neonatal Ed. 2003;88:F464–6.
21. Bruinsma N, Stobberingh EE, Herpers MJ, Vles JS, Weber BJ, Gavilanes DA. Subcutaneous ventricular catheter reservoir and ventriculoperitoneal drain-related infections in preterm infants and young children. Clin Microbiol Infect: Off Publ Eur Soc Clin Microbiol Infect Dis. 2000;6:202–6.
22. Brockmeyer DL, Wright LC, Walker ML, Ward RM. Management of posthemorrhagic hydrocephalus in the low-birth-weight preterm neonate. Pediatr Neurosci. 1989;15:302–7. discussion 308.
23. Kormanik K, Praca J, Garton HJ, Sarkar S. Repeated tapping of ventricular reservoir in preterm infants with post-hemorrhagic ventricular dilatation does not increase the risk of reservoir infection. J Perinatol: Off J Calif Perinatal Assoc. 2010;30:218–21.
24. Perret GE, Graf CJ. Subgaleal shunt for temporary ventricle decompression and subdural drainage. J Neurosurg. 1977;47:590–5.
25. Vassilyadi M, Tataryn Z, Shamji MF, Ventureyra EC. Functional outcomes among premature infants with intraventricular hemorrhage. Pediatr Neurosurg. 2009;45:247–55.
26. Gould SJ, Howard S. Glial differentiation in the germinal layer of fetal and preterm infant brain: an immunocytochemical study. Pediatr Pathol Affiliated Int Paediatr Pathol Assoc. 1988;8:25–36.
27. Ballabh P. Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr Res. 2010;67:1–8.
28. Volpe JJ. Intraventricular hemorrhage in the premature infant—current concepts. Part I. Ann Neurol. 1989;25:3–11.
29. Antoniuk S, da Silva RV. Periventricular and intraventricular hemorrhage in the premature infants. Rev Neurol. 2000;31:238–43.
30. Kenny JD, Garcia-Prats JA, Hilliard JL, Corbet AJ, Rudolph AJ. Hypercarbia at birth: a possible role in the pathogenesis of intraventricular hemorrhage. Pediatrics. 1978;62:465–7.
31. Hill A, Shackelford GD, Volpe JJ. A potential mechanism of pathogenesis for early posthemorrhagic hydrocephalus in the premature newborn. Pediatrics. 1984;73:19–21.
32. Oi S, Di Rocco C. Proposal of “evolution theory in cerebrospinal fluid dynamics” and minor pathway hydrocephalus in developing immature brain. Childs Nerv Syst: ChNS: Off J Int Soc Pediatr Neurosurg. 2006;22:662–9.
33. Douglas-Escobar M, Weiss MD. Biomarkers of brain injury in the premature infant. Front Neurol. 2012;3:185.
34. Aquilina K, Chakkarapani E, Thoresen M. Early deterioration of cerebrospinal fluid dynamics in a neonatal piglet model of intraventricular hemorrhage and posthemorrhagic ventricular dilation. J Neurosurg Pediatr. 2012;10:529–37.
35. El-Khoury N, Braun A, Hu F, Pandey M, Nedergaard M, Lagamma EF, et al. Astrocyte end-feet in germinal matrix, cerebral cortex, and white matter in developing infants. Pediatr Res. 2006;59:673–9.
36. Fernandez-Lopez D, Faustino J, Daneman R, Zhou L, Lee SY, Derugin N, et al. Blood-brain barrier permeability is increased after acute adult stroke but not neonatal stroke in the rat. J Neurosci: Off J Soc Neurosci. 2012;32:9588–600.
37. Ballabh P, Hu F, Kumarasiri M, Braun A, Nedergaard M. Development of tight junction molecules in blood vessels of germinal matrix, cerebral cortex, and white matter. Pediatr Res. 2005;58:791–8.
38. Braun A, Xu H, Hu F, Kocherlakota P, Siegel D, Chander P, et al. Paucity of pericytes in germinal matrix vasculature of premature infants. J Neurosci: Off J Soc Neurosci. 2007;27:12012–24.
39. Deren KE, Packer M, Forsyth J, Milash B, Abdullah OM, Hsu EW, et al. Reactive astrocytosis, microgliosis and inflammation in rats with neonatal hydrocephalus. Exp Neurol. 2010;226:110–9.
40. Glees P, Hasan M. Ultrastructure of human cerebral macroglia and microglia: maturing and hydrocephalic frontal cortex. Neurosurg Rev. 1990;13:231–42.
41. Fernandez-Lopez D, Faustino J, Derugin N, Wendland M, Lizasoain I, Moro MA, et al. Reduced infarct size and accumulation of microglia in rats treated with WIN 55,212-2 after neonatal stroke. Neuroscience. 2012;207:307–15.
42. Supramaniam V, Vontell R, Srinivasan L, Wyatt-Ashmead J, Hagberg H, Rutherford M. Microglia activation in the extremely preterm human brain. Pediatr Res. 2013;73:301–9.
43. Tada T, Kanaji M, Kobayashi S. Induction of communicating hydrocephalus in mice by intrathecal injection of human recombinant transforming growth factor-beta 1. J Neuroimmunol. 1994;50:153–8.
44. Cherian S, Thoresen M, Silver IA, Whitelaw A, Love S. Transforming growth factor-betas in a rat model of neonatal posthaemorrhagic hydrocephalus. Neuropathol Appl Neurobiol. 2004;30:585–600.
45. Balasubramaniam J, Del Bigio MR. Animal models of germinal matrix hemorrhage. J Child Neurol. 2006;21:365–71.
46. Reynolds ML, Evans CA, Reynolds EO, Saunders NR, Durbin GM, Wigglesworth JS. Intracranial haemorrhage in the preterm sheep fetus. Early Hum Dev. 1979;3:163–86.
47. Ting P, Yamaguchi S, Bacher JD, Killens RH, Myers RE. Failure to produce germinal matrix or intraventricular hemorrhage by hypoxia, hypo-, or hypervolemia. Exp Neurol. 1984;83:449–60.
48. Cohn HE, Sacks EJ, Heymann MA, Rudolph AM. Cardiovascular responses to hypoxemia and acidemia in fetal lambs. Am J Obstet Gynecol. 1974;120:817–24.
49. Pond WG, Boleman SL, Fiorotto ML, Ho H, Knabe DA, Mersmann HJ, et al. Perinatal ontogeny of brain growth in the domestic pig. Proc Soc Exp Biol Med Soc Exp Biol Med. 2000;223:102–8.
50. Stankovic MR, Maulik D, Rosenfeld W, Stubblefield PG, Kofinas AD, Drexler S, et al. Real-time optical imaging of experimental brain ischemia and hemorrhage in neonatal piglets. J Perinat Med. 1999;27:279–86.
51. Leuschen MP, Nelson Jr RM. Telencephalic microvessels of premature beagle pups. Anat Rec. 1986;215:59–64.
52. Trommer BL, Groothuis DR, Pasternak JF. Quantitative analysis of cerebral vessels in the newborn puppy: the structure of germinal matrix vessels may predispose to hemorrhage. Pediatr Res. 1987;22:23–8.
53. Ment LR, Stewart WB, Duncan CC. Beagle puppy model of intraventricular hemorrhage: ethamsylate studies. Prostaglandins. 1984;27:245–56.
54. Goddard-Finegold J, Donley DK, Adham BI, Michael LH. Phenobarbital and cerebral blood flow during hypertension in the newborn beagle. Pediatrics. 1990;86:501–8.
55. Ment LR, Stewart WB, Duncan CC, Lambrecht R. Beagle puppy model of intraventricular hemorrhage. J Neurosurg. 1982;57:219–23.
56. Ment LR, Stewart WB, Duncan CC, Scott DT, Lambrecht R. Beagle puppy model of intraventricular hemorrhage. Effect of indomethacin on local cerebral glucose utilization. J Neurosurg. 1984;60:737–42.
57. Ment LR, Stewart WB, Duncan CC. Beagle puppy model of intraventricular hemorrhage. Effect of superoxide dismutase on cerebral blood flow and prostaglandins. J Neurosurg. 1985;62:563–9.
58. Kakita A, Goldman JE. Patterns and dynamics of SVZ cell migration in the postnatal forebrain: monitoring living progenitors in slice preparations. Neuron. 1999;23:461–72.
59. Levers TE, Edgar JM, Price DJ. The fates of cells generated at the end of neurogenesis in developing mouse cortex. J Neurobiol. 2001;48:265–77.
60. Altman J, Sudarshan K. Postnatal development of locomotion in the laboratory rat. Anim Behav. 1975;23:896–920.
61. Lekic T, Manaenko A, Rolland W, Fathali N, Peterson M, Tang J, et al. Protective effect of hydrogen gas therapy after germinal matrix hemorrhage in neonatal rats. Acta Neurochir Suppl. 2011;111:237–41.
62. Lekic T, Manaenko A, Rolland W, Virbel K, Hartman R, Tang J, et al. Neuroprotection by melatonin after germinal matrix hemorrhage in neonatal rats. Acta Neurochir Suppl. 2011;111:201–6.
63. Leitzke AS, Rolland WB, Krafft PR, Lekic T, Klebe D, Flores JJ, et al. Isoflurane post-treatment ameliorates GMH-induced brain injury in neonatal rats. Stroke; J Cerebral Circ. 2013;44:3587–90.
64. McCrea HJ, Ment LR. The diagnosis, management, and postnatal prevention of intraventricular hemorrhage in the preterm neonate. Clin Perinatol. 2008;35:777–92. vii.
65. Klebe D, Krafft PR, Hoffmann C, Lekic T, Flores JJ, Rolland W, et al. Acute and delayed deferoxamine treatment attenuates long-term sequelae after germinal matrix hemorrhage in neonatal rats. Stroke; J Cerebral Circ. 2014;45:2475–2479.
66. Lekic T, Manaenko A, Rolland W, Ostrowski RP, Virbel K, Tang J, et al. Beneficial effect of hyperbaric oxygenation after neonatal germinal matrix hemorrhage. Acta Neurochir Suppl. 2011;111:253–7.
67. Tosun C, Koltz MT, Kurland DB, Ijaz H, Gurakar M, Schwartzbauer G, et al. The protective effect of glibenclamide in a model of hemorrhagic encephalopathy of prematurity. Brain Sci. 2013;3:215–238
68. Ballabh P, Xu H, Hu F, Braun A, Smith K, Rivera A, et al. Angiogenic inhibition reduces germinal matrix hemorrhage. Nat Med. 2007;13:477–85.
69. Del Bigio MR, Wilson MJ, Enno T. Chronic hydrocephalus in rats and humans: white matter loss and behavior changes. Ann Neurol. 2003;53:337–46.
70. Deren KE, Forsyth J, Abdullah O, Hsu EW, Klinge PM, Silverberg GD, et al. Low levels of amyloid-beta and its transporters in neonatal rats with and without hydrocephalus. Cerebrospinal Fluid Res. 2009;6:4.
71. Mangano FT, McAllister 2nd JP, Jones HC, Johnson MJ, Kriebel RM. The microglial response to progressive hydrocephalus in a model of inherited aqueductal stenosis. Neurol Res. 1998;20:697–704.
72. Gram M, Sveinsdottir S, Ruscher K, Hansson SR, Cinthio M, Akerstrom B, et al. Hemoglobin induces inflammation after preterm intraventricular hemorrhage by methemoglobin formation. J Neuroinflammation. 2013;10:100.
73. Ahn SY, Chang YS, Sung DK, Sung SI, Yoo HS, Lee JH, et al. Mesenchymal stem cells prevent hydrocephalus after severe intraventricular hemorrhage. Stroke; J Cereb Circ. 2013;44:497–504.
74. Manaenko A, Lekic T, Barnhart M, Hartman R, Zhang JH. Inhibition of transforming growth factor-beta attenuates brain injury and neurological deficits in a rat model of germinal matrix hemorrhage. Stroke; J Cereb Circ. 2014;45:828–34.
75. Gomes FC, Sousa Vde O, Romao L. Emerging roles for TGF-beta1 in nervous system development. Int J Dev Neurosci: Off J Int Soc Dev Neurosci. 2005;23:413–24.
76. Derynck R. TGF-beta-receptor-mediated signaling. Trends Biochem Sci. 1994;19:548–53.
77. Bernard DJ, Chapman SC, Woodruff TK. An emerging role for co-receptors in inhibin signal transduction. Mol Cell Endocrinol. 2001;180:55–62.
78. Lee JY, Keep RF, He Y, Sagher O, Hua Y, Xi G. Hemoglobin and iron handling in brain after subarachnoid hemorrhage and the effect of deferoxamine on early brain injury. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab. 2010;30:1793–803.
79. Savman K, Nilsson UA, Blennow M, Kjellmer I, Whitelaw A. Non-protein-bound iron is elevated in cerebrospinal fluid from preterm infants with posthemorrhagic ventricular dilatation. Pediatr Res. 2001;49:208–12.
80. Strahle JM, Garton T, Bazzi AA, Kilaru H, Garton HJ, Maher CO, et al. Role of hemoglobin and iron in hydrocephalus after neonatal intraventricular hemorrhage. Neurosurgery. 2014;75:696–705. discussion 706.
81. Aronson AL. Pharmacotherapeutics of the newer tetracyclines. J Am Vet Med Assoc. 1980;176:1061–8.
82. Aso E, Juves S, Maldonado R, Ferrer I. CB2 cannabinoid receptor agonist ameliorates Alzheimer-like phenotype in AbetaPP/PS1 mice. J Alzheimer’s Dis: JAD. 2013;35:847–58.
83. Gomez-Galvez Y, Palomo-Garo C, Fernandez-Ruiz J, Garcia C. Potential of the cannabinoid CB2 receptor as a pharmacological target against inflammation in Parkinson’s disease. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;64:200–8.
84. Malfitano AM, Laezza C, D’Alessandro A, Procaccini C, Saccomanni G, Tuccinardi T, et al. Effects on immune cells of a new 1,8-naphthyridin-2-one derivative and its analogues as selective CB2 agonists: implications in multiple sclerosis. PLoS One. 2013;8:e62511.
85. Barichello T, Generoso JS, Simoes LR, Goularte JA, Petronilho F, Saigal P, et al. Role of microglial activation in the pathophysiology of bacterial meningitis. Mol Neurobiol. 2015. doi:10.1007/s12035-015-9107-4.
86. Yang Y, Salayandia VM, Thompson JF, Yang LY, Estrada EY, Yang Y. Attenuation of acute stroke injury in rat brain by minocycline promotes blood-brain barrier remodeling and alternative microglia/macrophage activation during recovery. J Neuroinflammation. 2015;12:26.
87. Streit WJ, Walter SA, Pennell NA. Reactive microgliosis. Prog Neurobiol. 1999;57:563–81.
88. Diz-Chaves Y, Pernia O, Carrero P, Garcia-Segura LM. Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. J Neuroinflammation. 2012;9:71.
89. Yang F, Zhou L, Wang D, Wang Z, Huang QY. Minocycline ameliorates hypoxia-induced blood-brain barrier damage by inhibition of HIF-1alpha through SIRT-3/PHD-2 degradation pathway. Neuroscience. 2015;304:250–9.
90. Zhao F, Hua Y, He Y, Keep RF, Xi G. Minocycline-induced attenuation of iron overload and brain injury after experimental intracerebral hemorrhage. Stroke; J Cereb Circ. 2011;42:3587–93.
91. Lopez-Rodriguez AB, Siopi E, Finn DP, Marchand-Leroux C, Garcia-Segura LM, Jafarian-Tehrani M, et al. CB1 and CB2 cannabinoid receptor antagonists prevent minocycline-induced neuroprotection following traumatic brain injury in mice. Cereb Cortex. 2015;25:35–45.
92. Georgiadis P, Xu H, Chua C, Hu F, Collins L, Huynh C, et al. Characterization of acute brain injuries and neurobehavioral profiles in a rabbit model of germinal matrix hemorrhage. Stroke; J Cereb Circ. 2008;39:3378–88.
93. Hua Y, Keep RF, Hoff JT, Xi G. Brain injury after intracerebral hemorrhage: the role of thrombin and iron. Stroke; J Cereb Circ. 2007;38:759–62.
94. Xi G, Keep RF, Hoff JT. Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol. 2006;5:53–63.
95. von Bernhardi R, Eugenin-von Bernhardi L, Eugenin J. Microglial cell dysregulation in brain aging and neurodegeneration. Front Aging Neurosci. 2015;7:124.
96. Takeuchi H, Suzumura A. Gap junctions and hemichannels composed of connexins: potential therapeutic targets for neurodegenerative diseases. Front Cell Neurosci. 2014;8:189.
97. Koenigsknecht J, Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J Neurosci: Off J Soc Neurosci. 2004;24:9838–46.
98. Schwab JM, Schluesener HJ. Microglia rules: insights into microglial-neuronal signaling. Cell Death Differ. 2004;11:1245–6.
99. Esiaba I, Angeles DM, Holden MS, Tan JB, Asmerom Y, Gollin G, et al. Urinary allantoin is elevated in severe intraventricular hemorrhage in the preterm newborn. Translational Stroke Res. 2015. doi:10.1007/s12975-015-0405-y.
100. Tataranno ML, Perrone S, Buonocore G. Plasma biomarkers of oxidative stress in neonatal brain injury. Clin Perinatol. 2015;42:529–39.
101. Abdel Ghany EA, Alsharany W, Ali AA, Younass ER, Hussein JS. Anti-oxidant profiles and markers of oxidative stress in preterm neonates. Paediatr Int Child Health. 2015;2046905515Y0000000017.
102. Nakamura T, Keep RF, Hua Y, Hoff JT, Xi G. Oxidative DNA injury after experimental intracerebral hemorrhage. Brain Res. 2005;1039:30–6.
103. Peeling J, Del Bigio MR, Corbett D, Green AR, Jackson DM. Efficacy of disodium 4-[(tert-butylimino)methyl]benzene-1,3-disulfonate N-oxide (NXY-059), a free radical trapping agent, in a rat model of hemorrhagic stroke. Neuropharmacology. 2001;40:433–9.
104. Morgan PJ, Barrett P, Howell HE, Helliwell R. Melatonin receptors: localization, molecular pharmacology and physiological significance. Neurochem Int. 1994;24:101–46.
105. Musshoff U, Riewenherm D, Berger E, Fauteck JD, Speckmann EJ. Melatonin receptors in rat hippocampus: molecular and functional investigations. Hippocampus. 2002;12:165–73.
106. Murphy BP, Inder TE, Rooks V, Taylor GA, Anderson NJ, Mogridge N, et al. Posthaemorrhagic ventricular dilatation in the premature infant: natural history and predictors of outcome. Arch Dis Child Fetal Neonatal Ed. 2002;87:F37–41.
107. Balabanov R, Dore-Duffy P. Role of the CNS microvascular pericyte in the blood-brain barrier. J Neurosci Res. 1998;53:637–44.
108. Hirschi KK, D’Amore PA. Control of angiogenesis by the pericyte: molecular mechanisms and significance. EXS. 1997;79:419–28.
109. von Tell D, Armulik A, Betsholtz C. Pericytes and vascular stability. Exp Cell Res. 2006;312:623–9.
110. Guasti L, Richardson D, Jhaveri M, Eldeeb K, Barrett D, Elphick MR, et al. Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain. Mol Pain. 2009;5:35.
111. Hermann DM, Peruzzotti-Jametti L, Schlechter J, Bernstock JD, Doeppner TR, Pluchino S. Neural precursor cells in the ischemic brain—integration, cellular crosstalk, and consequences for stroke recovery. Front Cell Neurosci. 2014;8:291.
112. Nash KR, Moran P, Finneran DJ, Hudson C, Robinson J, Morgan D, et al. Fractalkine over expression suppresses alpha-synuclein-mediated neurodegeneration. Mol Ther: J Am Soc Gene Ther. 2015;23:17–23.
113. Saijo K, Glass CK. Microglial cell origin and phenotypes in health and disease. Nat Rev Immunol. 2011;11:775–87.
114. Su P, Zhang J, Zhao F, Aschner M, Chen J, Luo W. The interaction between microglia and neural stem/precursor cells. Brain Res Bull. 2014;109:32–8.
115. Reshef R, Kreisel T, Beroukhim Kay D, Yirmiya R. Microglia and their CX3CR1 signaling are involved in hippocampal- but not olfactory bulb-related memory and neurogenesis. Brain Behav Immun. 2014;41:239–50.