Advances in the cell-based treatment of neonatal hypoxic-ischemic brain injury

Future Neurology

Volumn 8, Issue 2, 2013, Pages 193-203

  Pabon, Mibel M ^a   Borlongan, Cesar V ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

cerebral palsy; combination therapy; consortium; hypothermia; neurorestoration; stem cell; translational

Indexed keywords

ERYTHROPOIETIN; HELIUM;

CLINICAL PROTOCOL; DISEASE MODEL; FEASIBILITY STUDY; HUMAN; HYPOTHERMIA; HYPOXIC ISCHEMIC ENCEPHALOPATHY; NEWBORN; NONHUMAN; PRACTICE GUIDELINE; PRIORITY JOURNAL; REVIEW; RODENT; SAFETY; STEM CELL TRANSPLANTATION; SYMPTOM; TREATMENT RESPONSE; VALIDATION STUDY;

EID: 84874621970     PISSN: 14796708     EISSN: 17486971     Source Type: Journal    
DOI: 10.2217/fnl.12.85     Document Type: Review

References (128)

1. Hypoxia Ischemia: Pathogenesis and Neuropathology (6th Edition). Vannucci R (Ed.). Mosby, St Louis, MO, USA (1997).
2. Kurinczuk JJ, White-Koning M, Badawi N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum. Dev. 86(6), 329-338 (2010).
3. Low JA, Lindsay BG, Derrick EJ. Threshold of metabolic acidosis associated with newborn complications. Am. J. Obstet. Gynecol. 177(6), 1391-1394 (1997).
4. Mulligan JC, Painter MJ, O'Donoghue PA, MacDonald HM, Allan AC, Taylor PM. Neonatal asphyxia. II. Neonatal mortality and long-term sequelae. J. Pediatr. 96(5), 903-907 (1980).
5. Nelson KB. Neonatal encephalopathy: etiology and outcome. Dev. Med. Child Neurol. 47(5), 292 (2005).
6. Nelson KB, Leviton A. Hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 354(15), 1643-1645 (2006).
7. Dammann O, Ferriero D, Gressens P. Neonatal encephalopathy or hypoxic-ischemic encephalopathy? Appropriate terminology matters. Pediatr. Res. 70(1), 1-2 (2011).
8. Leviton A. Why the term neonatal encephalopathy should be preferred over neonatal hypoxic-ischemic encephalopathy. Am. J. Obstet. Gynecol. doi:10.1016/j.ajog. 2012.07.020 (2012) (Epub ahead of print).
9. Blume HK, Loch CM, Li CI. Neonatal encephalopathy and socioeconomic status: population-based case-control study. Arch. Pediatr. Adolesc. Med. 161(7), 663-668 (2007).
10. De Vries LS, Van Haastert IC, Benders MJ, Groenendaal F. Myth: cerebral palsy cannot be predicted by neonatal brain imaging. Semin. Fetal Neonatal Med. 16(5), 279-287 (2011).
11. Volpe JJ. The encephalopathy of prematurity - brain injury and impaired brain development inextricably intertwined. Semin. Pediatr. Neurol. 16(4), 167-178 (2009).
12. MacDonald HM, Mulligan JC, Allen AC, Taylor PM. Neonatal asphyxia. I. Relationship of obstetric and neonatal complications to neonatal mortality in 38,405 consecutive deliveries. J. Pediatr. 96(5), 898-902 (1980).
13. Finer NN, Robertson CM, Richards RT, Pinnell LE, Peters KL. Hypoxic-ischemic encephalopathy in term neonates: perinatal factors and outcome. J. Pediatr. 98(1), 112-117 (1981).
14. Robertson CM, Finer NN, Grace MG. School performance of survivors of neonatal encephalopathy associated with birth asphyxia at term. J. Pediatr. 114(5), 753-760 (1989).
15. Raju TN. Ischemic perinatal stroke: challenge and opportunities. Int. J. Stroke 3(3), 169-172 (2008).
16. Khwaja O, Volpe JJ. Pathogenesis of cerebral white matter injury of prematurity. Arch. Dis. Child Fetal Neonatal Ed. 93(2), F153-F161 (2008).
17. Chen HJ, Wei KL, Yao YJ. [Multicenter investigation for incidence of periventricular leukomalacia in premature infants in China]. Zhongguo Dang Dai Er Ke Za Zhi 10(6), 686-692 (2008).
18. Baud O, D'Allest AM, Lacaze-Masmonteil T et al. The early diagnosis of periventricular leukomalacia in premature infants with positive rolandic sharp waves on serial electroencephalography. J. Pediatr. 132(5), 813-817 (1998).
19. Olsen P, Paakko E, Vainionpaa L, Pyhtinen J, Jarvelin MR. Magnetic resonance imaging of periventricular leukomalacia and its clinical correlation in children. Ann. Neurol. 41(6), 754-761 (1997).
20. Johnston MV, Fatemi A, Wilson MA, Northington F. Treatment advances in neonatal neuroprotection and neurointensive care. Lancet Neurol. 10(4), 372-382 (2011).
21. Hope PL, Reynolds EO. Investigation of cerebral energy metabolism in newborn infants by phosphorus nuclear magnetic resonance spectroscopy. Clin. Perinatol. 12(1), 261-275 (1985).
22. Azzopardi DV, Strohm B, Edwards AD et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N. Engl. J. Med. 361(14), 1349-1358 (2009).
23. Gluckman PD, Wyatt JS, Azzopardi D et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet 365(9460), 663-670 (2005).
24. Shankaran S, Laptook AR, Ehrenkranz RA et al. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 353(15), 1574-1584 (2005).
25. Rutherford MA, Azzopardi D, Whitelaw A et al. Mild hypothermia and the distribution of cerebral lesions in neonates with hypoxic-ischemic encephalopathy. Pediatrics 116(4), 1001-1006 (2005).
26. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke 30(12), 2752-2758 (1999).
27. Recommendations for clinical trial evaluation of acute stroke therapies. Stroke 32(7), 1598-1606 (2001).
28. Feuerstein GZ, Zaleska MM, Krams M et al. Missing steps in the STAIR case: a translational medicine perspective on the development of NXY-059 for treatment of acute ischemic stroke. J. Cereb. Blood Flow Metab. 28(1), 217-219 (2008).
29. Fisher M, Feuerstein G, Howells DW et al. Update of the stroke therapy academic industry roundtable preclinical recommendations. Stroke 40(6), 2244-2250 (2009).
30. Chopp M, Steinberg GK, Kondziolka D et al. Who's in favor of translational cell therapy for stroke: STEPS forward please? Cell Transplant. 18(7), 691-693 (2009).
31. Borlongan CV, Chopp M, Steinberg GK et al. Potential of stem/progenitor cells in treating stroke: the missing steps in translating cell therapy from laboratory to clinic. Regen. Med. 3(3), 249-250 (2008).
32. Borlongan CV. Cell therapy for stroke: remaining issues to address before embarking on clinical trials. Stroke 40(Suppl. 3), S146-S148 (2009).
33. Stem Cell Therapies as an Emerging Paradigm in Stroke (STEPS). Bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke. Stroke 40(2), 510-515 (2009).
34. Northington FJ. Brief update on animal models of hypoxic-ischemic encephalopathy and neonatal stroke. ILAR J. 47(1), 32-38 (2006).
35. Vannucci RC, Vannucci SJ. Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev. Neurosci. 27(2-4), 81-86 (2005).
36. Ditelberg JS, Sheldon RA, Epstein CJ, Ferriero DM. Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatr. Res. 39(2), 204-208 (1996).
37. Sheldon RA, Sedik C, Ferriero DM. Strainrelated brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 810(1-2), 114-122 (1998).
38. Fullerton HJ, Ditelberg JS, Chen SF et al. Copper/zinc superoxide dismutase transgenic brain accumulates hydrogen peroxide after perinatal hypoxia ischemia. Ann. Neurol. 44(3), 357-364 (1998).
39. Graham EM, Sheldon RA, Flock DL et al. Neonatal mice lacking functional Fas death receptors are resistant to hypoxic-ischemic brain injury. Neurobiol. Dis. 17(1), 89-98 (2004).
40. Hagberg H, Wilson MA, Matsushita H et al. PARP-1 gene disruption in mice preferentially protects males from perinatal brain injury. J. Neurochem. 90(5), 1068-1075 (2004).
41. Mcquillen PS, Sheldon RA, Shatz CJ, Ferriero DM. Selective vulnerability of subplate neurons after early neonatal hypoxiaischemia. J. Neurosci. 23(8), 3308-3315 (2003).
42. Wang S, Wu EX, Cai K, Lau HF, Cheung PT, Khong PL. Mild hypoxic-ischemic injury in the neonatal rat brain: longitudinal evaluation of white matter using diffusion tensor MR imaging. AJNR Am. J. Neuroradiol. 30(10), 1907-1913 (2009).
43. Huang Z, Liu J, Cheung PY, Chen C. Longterm cognitive impairment and myelination deficiency in a rat model of perinatal hypoxic-ischemic brain injury. Brain Res. 1301, 100-109 (2009).
44. Wang S, Wu EX, Tam CN, Lau HF, Cheung PT, Khong PL. Characterization of white matter injury in a hypoxic-ischemic neonatal rat model by diffusion tensor MRI. Stroke 39(8), 2348-2353 (2008).
45. Chang YC, Huang CC, Hung PL, Huang HM. Rolipram, a phosphodiesterase type IV inhibitor, exacerbates periventricular white matter lesions in rat pups. Pediatr. Res. 64(3), 234-239 (2008).
46. Wen TC, Rogido M, Peng H, Genetta T, Moore J, Sola A. Gender differences in longterm beneficial effects of erythropoietin given after neonatal stroke in postnatal day-7 rats. Neuroscience 139(3), 803-811 (2006).
47. Guo TL, Germolec DR, Musgrove DL et al. Myelotoxicity in genistein-, nonylphenol-, methoxychlor-, vinclozolin- or ethinyl estradiol-exposed F1 generations of Sprague-Dawley rats following developmental and adult exposures. Toxicology 211(3), 207-219 (2005).
48. Pequignot JM, Spielvogel H, Caceres E et al. Influence of gender and endogenous sex steroids on catecholaminergic structures involved in physiological adaptation to hypoxia. Pflugers Arch. 433(5), 580-586 (1997).
49. Raju TN. Some animal models for the study of perinatal asphyxia. Biol. Neonate 62(4), 202-214 (1992).
50. Bjorkman ST, Miller SM, Rose SE, Burke C, Colditz PB. Seizures are associated with brain injury severity in a neonatal model of hypoxia-ischemia. Neuroscience 166(1), 157-167 (2010).
51. Zhang D, Hathi M, Yang ZJ, Ding H, Koehler R, Thakor N. Hypoxic-ischemic brain injury in neonatal piglets with different histological outcomes: An amplitudeintegrated EEG study. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 1127-1130 (2009).
52. Yager JY, Ashwal S. Animal models of perinatal hypoxic-ischemic brain damage. Pediatr. Neurol. 40(3), 156-167 (2009).
53. Tai WC, Burke KA, Dominguez JF, Gundamraj L, Turman JE Jr. Growth deficits in a postnatal day 3 rat model of hypoxic-ischemic brain injury. Behav. Brain Res. 202(1), 40-49 (2009).
54. Derrick M, Luo NL, Bregman JC et al. Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J. Neurosci. 24(1), 24-34 (2004).
55. Laptook AR, Corbett RJ, Burns D, Sterett R. Neonatal ischemic neuroprotection by modest hypothermia is associated with attenuated brain acidosis. Stroke 26(7), 1240-1246 (1995).
56. Iwata O, Iwata S, Thornton JS et al. 'Therapeutic time window' duration decreases with increasing severity of cerebral hypoxiaischaemia under normothermia and delayed hypothermia in newborn piglets. Brain Res. 1154, 173-180 (2007).
57. Borlongan CV, Tajima Y, Trojanowski JQ, Lee VM, Sanberg PR. Transplantation of cryopreserved human embryonal carcinomaderived neurons (NT2N cells) promotes functional recovery in ischemic rats. Exp. Neurol. 149(2), 310-321 (1998).
58. Kondziolka D, Wechsler L, Goldstein S et al. Transplantation of cultured human neuronal cells for patients with stroke. Neurology 55(4), 565-569 (2000).
59. Nelson PT, Kondziolka D, Wechsler L et al. Clonal human (hNT) neuron grafts for stroke therapy: neuropathology in a patient 27 months after implantation. Am. J. Pathol. 160(4), 1201-1206 (2002).
60. Hara K, Yasuhara T, Maki M et al. Neural progenitor NT2N cell lines from teratocarcinoma for transplantation therapy in stroke. Prog. Neurobiol. 85(3), 318-334 (2008).
61. Yu G, Fournier C, Hess DC, Borlongan CV. Transplantation of carotid body cells in the treatment of neurological disorders. Neurosci. Biobehav. Rev. 28(8), 803-810 (2005).
62. Sun J, Allison J, Mclaughlin C et al. Differences in quality between privately and publicly banked umbilical cord blood units: a pilot study of autologous cord blood infusion in children with acquired neurologic disorders. Transfusion 50(9), 1980-1987 (2010).
63. Portmann-Lanz CB, Schoeberlein A, Huber A et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am. J. Obstet. Gynecol. 194(3), 664-673 (2006).
64. Robertson CM, Finer NN. Long-term follow-up of term neonates with perinatal asphyxia. Clin. Perinatol. 20(2), 483-500 (1993).
65. Lauterbach MD, Raz S, Sander CJ. Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery. Neuropsychology 15(3), 411-420 (2001).
66. Espy KA, Senn TE, Charak DA, Tyler J, Wiebe SA. Perinatal pH and neuropsychological outcomes at age 3 years in children born preterm: an exploratory study. Dev. Neuropsychol. 32(2), 669-682 (2007).
67. Kaandorp JJ, Benders MJ, Rademaker CM et al. Antenatal allopurinol for reduction of birth asphyxia induced brain damage (ALLO-Trial); a randomized double blind placebo controlled multicenter study. BMC Pregnancy Childbirth 10, 8 (2010).
68. Hobbs C, Thoresen M, Tucker A, Aquilina K, Chakkarapani E, Dingley J. Xenon and hypothermia combine additively, offering long-term functional and histopathologic neuroprotection after neonatal hypoxia/ischemia. Stroke 39(4), 1307-1313 (2008).
69. Carroll JE, Borlongan CV. Adult stem cell therapy for acute brain injury in children. CNS Neurol. Disord. Drug Targets 7(4), 361-369 (2008).
70. Kim CT, Han J, Kim H. Pediatric stroke recovery: a descriptive analysis. Arch. Phys. Med. Rehabil. 90(4), 657-662 (2009).
71. Yasuhara T, Hara K, Maki M et al. Intravenous grafts recapitulate the neurorestoration afforded by intracerebrally delivered multipotent adult progenitor cells in neonatal hypoxic-ischemic rats. J. Cereb. Blood Flow Metab. 28(11), 1804-1810 (2008).
72. Hess DC, Borlongan CV. Stem cells and neurological diseases. Cell Prolif. 41(Suppl. 1), 94-114 (2008).
73. Hess DC, Borlongan CV. Cell-based therapy in ischemic stroke. Expert Rev. Neurother. 8(8), 1193-1201 (2008).
74. Parolini O, Alviano F, Bergwerf I et al. Toward cell therapy using placenta-derived cells: disease mechanisms, cell biology, preclinical studies, and regulatory aspects at the round table. Stem Cells Dev. 19(2), 143-154 (2010).
75. Hoehn M, Wiedermann D, Justicia C et al. Cell tracking using magnetic resonance imaging. J. Physiol. 584(Pt 1), 25-30 (2007).
76. Modo M, Mellodew K, Cash D et al. Mapping transplanted stem cell migration after a stroke: a serial, in vivo magnetic resonance imaging study. Neuroimage 21(1), 311-317 (2004).
77. Jendelova P, Herynek V, Urdzikova L et al. Magnetic resonance tracking of transplanted bone marrow and embryonic stem cells labeled by iron oxide nanoparticles in rat brain and spinal cord. J. Neurosci. Res. 76(2), 232-243 (2004).
78. Shyu WC, Chen CP, Lin SZ, Lee YJ, Li H. Efficient tracking of non-iron-labeled mesenchymal stem cells with serial MRI in chronic stroke rats. Stroke 38(2), 367-374 (2007).
79. Song M, Kim Y, Ryu S, Song I, Kim SU, Yoon BW. MRI tracking of intravenously transplanted human neural stem cells in rat focal ischemia model. Neurosci. Res. 64(2), 235-239 (2009).
80. Daadi MM, Li Z, Arac A et al. Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain. Mol. Ther. 17(7), 1282-1291 (2009).
81. Lee ES, Chan J, Shuter B et al. Microgel iron oxide nanoparticles for tracking human fetal mesenchymal stem cells through magnetic resonance imaging. Stem Cells 27(8), 1921-1931 (2009).
82. Ashwal S, Obenaus A, Snyder EY. Neuroimaging as a basis for rational stem cell therapy. Pediatr. Neurol. 40(3), 227-236 (2009).
83. Chau V, Poskitt KJ, Miller SP. Advanced neuroimaging techniques for the term newborn with encephalopathy. Pediatr. Neurol. 40(3), 181-188 (2009).
84. Agrawal N, Johnston SC, Wu YW, Sidney S, Fullerton HJ. Imaging data reveal a higher pediatric stroke incidence than prior US estimates. Stroke 40(11), 3415-3421 (2009).
85. Liao Y, Cotten M, Tan S, Kurtzberg J, Cairo MS. Rescuing the neonatal brain from hypoxic injury with autologous cord blood. Bone Marrow Transplant. doi:10.1038/ bmt.169 (2012) (Epub ahead of print).
86. Li M, Yu A, Zhang F et al. Treatment of one case of cerebral palsy combined with posterior visual pathway injury using autologousbone marrow mesenchymal stem cells. J. Transl. Med. 10(1), 100 (2012).
87. Jordan LC, Rafay MF, Smith SE et al. Antithrombotic treatment in neonatal cerebral sinovenous thrombosis: results of the International Pediatric Stroke Study. J. Pediatr. 156(5), 704-710, 710.e1-710.e2 (2010).
88. Grunwald IQ, Walter S, Shamdeen MG et al. New mechanical recanalization devices -the future in pediatric stroke treatment? J. Invasive Cardiol. 22(2), 63-66 (2010).
89. Normann S, De Veber G, Fobker M et al. Role of endogenous testosterone concentration in pediatric stroke. Ann. Neurol. 66(6), 754-758 (2009).
90. Kenet G, Lutkhoff LK, Albisetti M et al. Impact of thrombophilia on risk of arterial ischemic stroke or cerebral sinovenous thrombosis in neonates and children: a systematic review and meta-analysis of observational studies. Circulation 121(16), 1838-1847 (2010).
91. Ganesan V. Pediatric stroke guidelines: where will these take future research and treatment options for childhood stroke? Expert Rev. Neurother. 9(5), 639-648 (2009).
92. Amlie-Lefond C, Bernard TJ, Sebire G et al. Predictors of cerebral arteriopathy in children with arterial ischemic stroke: results of the International Pediatric Stroke Study. Circulation 119(10), 1417-1423 (2009).
93. Berman DR, Liu Y, Barks J, Mozurkewich E. Treatment with docosahexaenoic acid after hypoxia-ischemia improves forepaw placing in a rat model of perinatal hypoxia-ischemia. Am. J. Obstet. Gynecol. 203(4), 385.e1-385.e5 (2010).
94. Zhou Y, Fathali N, Lekic T et al. Remote limb ischemic postconditioning protects against neonatal hypoxic-ischemic brain injury in rat pups by the opioid receptor/Akt pathway. Stroke 42(2), 439-444 (2011).
95. Shankaran S, Laptook A, Wright LL et al. Whole-body hypothermia for neonatal encephalopathy: animal observations as a basis for a randomized, controlled pilot study in term infants. Pediatrics 110(2 Pt 1), 377-385 (2002).
96. Lei B, Tan X, Cai H, Xu Q, Guo Q. Effect of moderate hypothermia on lipid peroxidation in canine brain tissue after cardiac arrest and resuscitation. Stroke 25(1), 147-152 (1994).
97. Thoresen M, Penrice J, Lorek A et al. Mild hypothermia after severe transient hypoxiaischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr. Res. 37(5), 667-670 (1995).
98. Battin MR, Dezoete JA, Gunn TR, Gluckman PD, Gunn AJ. Neurodevelopmental outcome of infants treated with head cooling and mild hypothermia after perinatal asphyxia. Pediatrics 107(3), 480-484 (2001).
99. Battin MR, Penrice J, Gunn TR, Gunn AJ. Treatment of term infants with head cooling and mild systemic hypothermia (35.0 degrees C and 34.5 degrees C) after perinatal asphyxia. Pediatrics 111(2), 244-251 (2003).
100. Bergstedt K, Hu BR, Wieloch T. Postischaemic changes in protein synthesis in the rat brain: effects of hypothermia. Exp. Brain Res. 95(1), 91-99 (1993).
101. Tagin MA, Woolcott CG, Vincer MJ, Whyte RK, Stinson DA. Hypothermia for neonatal hypoxic-ischemic encephalopathy: an updated systematic review and meta-analysis. Arch. Pediatr. Adolesc. Med. 166(6), 558-566 (2012).
102. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11(5), 339-350 (2010).
103. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 12(12), 723-738 (2011).
104. Yenari M, Kitagawa K, Lyden P, Perez-Pinzon M. Metabolic downregulation: a key to successful neuroprotection? Stroke 39(10), 2910-2917 (2008).
105. Robertson NJ, Nakakeeto M, Hagmann C et al. Therapeutic hypothermia for birth asphyxia in low-resource settings: a pilot randomised controlled trial. Lancet 372(9641), 801-803 (2008).
106. Glass HC, Nash KB, Bonifacio SL et al. Seizures and magnetic resonance imagingdetected brain injury in newborns cooled for hypoxic-ischemic encephalopathy. J. Pediatr. 159(5), 731-735.e1 (2011).
107. Higgins RD, Raju T, Edwards AD et al. Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop. J. Pediatr. 159(5), 851-858.e1 (2011).
108. Jatana M, Singh I, Singh AK, Jenkins D. Combination of systemic hypothermia and N-acetylcysteine attenuates hypoxic-ischemic brain injury in neonatal rats. Pediatr. Res. 59(5), 684-689 (2006).
109. Jenkins DD, Chang E, Singh I. Neuroprotective interventions: is it too late? J. Child Neurol. 24(9), 1212-1219 (2009).
110. Wu YW, Bauer LA, Ballard RA et al. Erythropoietin for neuroprotection in neonatal encephalopathy: safety and pharmacokinetics. Pediatrics, 130(4), 683-691 (2012).
111. Xiong T, Qu Y, Mu D, Ferriero D. Erythropoietin for neonatal brain injury: opportunity and challenge. Int. J. Dev. Neurosci. 29(6), 583-591 (2011).
112. Dickinson R, Franks NP. Bench-to-bedside review: molecular pharmacology and clinical use of inert gases in anesthesia and neuroprotection. Crit. Care 14(4), 229 (2010).
113. Ferriero DM. Neonatal brain injury. N. Engl. J. Med. 351(19), 1985-1995 (2004).
114. Bonifacio SL, Glass HC, Peloquin S, Ferriero DM. A new neurological focus in neonatal intensive care. Nat. Rev. Neurol. 7(9), 485-494 (2011).
115. Borlongan CV, Glover LE, Tajiri N, Kaneko Y, Freeman TB. The great migration of bone marrow-derived stem cells toward the ischemic brain: therapeutic implications for stroke and other neurological disorders. Prog. Neurobiol. 95(2), 213-228 (2011).
116. Borlongan CV, Kaneko Y, Maki M et al. Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev. 19(4), 439-452 (2010).
117. Ozawa K, Sato K, Oh I et al. Cell and gene therapy using mesenchymal stem cells (MSCs). J. Autoimmun. 30(3), 121-127 (2008).
118. Gunn AJ, Gunn TR. The 'pharmacology' of neuronal rescue with cerebral hypothermia. Early Hum. Dev. 53(1), 19-35 (1998).
119. Iadecola C, Anrather J. Stroke research at a crossroad: asking the brain for directions. Nat. Neurosci. 14(11), 1363-1368 (2011).
120. Edwards AD, Brocklehurst P, Gunn AJ 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 340, c363 (2010).
121. Borlongan CV, Lind JG, Dillon-Carter O et al. Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats. Brain Res. 1010(1-2), 108-116 (2004).
122. Borlongan CV, Lind JG, Dillon-Carter O et al. Intracerebral xenografts of mouse bone marrow cells in adult rats facilitate restoration of cerebral blood flow and blood-brain barrier. Brain Res. 1009(1-2), 26-33 (2004).
123. Boutin H, Dauphin F, Mackenzie ET, Jauzac P. Differential time-course decreases in nonselective, mu-, delta-, and kappa-opioid receptors after focal cerebral ischemia in mice. Stroke 30(6), 1271-1277; discussion 1278 (1999).
124. Kevelaitis E, Peynet J, Mouas C, Launay JM, Menasche P. Opening of potassium channels: the common cardioprotective link between preconditioning and natural hibernation? Circulation 99(23), 3079-3085 (1999).
125. Tsai SY, Lee CT, Hayashi T, Freed WJ, Su TP. Delta opioid peptide DADLE and naltrexone cause cell cycle arrest and differentiation in a CNS neural progenitor cell line. Synapse 64(4), 267-273 (2010).
126. Borlongan CV, Su TP, Wang Y. Treatment with delta opioid peptide enhances in vitro and in vivo survival of rat dopaminergic neurons. Neuroreport 11(5), 923-926 (2000).
127. Kaneko Y, Tajiri N, Su TP, Wang Y, Borlongan CV. Combination treatment of hypothermia and mesenchymal stromal cells amplifies neuroprotection in primary rat neurons exposed to hypoxic-ischemic-like injury in vitro: role of the opioid system. PLoS ONE 7(10), e47583 (2012).
128. Borlongan CV, Weiss MD. Baby STEPS. A giant leap for cell therapy in neonatal brain injury. Pediatr. Res. 70(1), 3-9 (2011).