Stem cell therapy to protect and repair the developing brain: A review of mechanisms of action of cord blood and amnion epithelial derived cells

Frontiers in Neuroscience

Volumn , Issue 7 OCT, 2013, Pages

  Castillo Melendez, Margie ^a   Yawno, Tamara ^a   Jenkin, Graham ^a   Miller, Suzanne L ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Amnion epithelial cells; Cerebral palsy; Clinical trials; Hypoxia ischemia; Inflammation; Perinatal brain injury; Stem cells; Umbilical cord blood

Indexed keywords

AMNION CELL; BIRTH; BRAIN DEVELOPMENT; BRAIN INJURY; BRAIN PROTECTION; CEREBRAL PALSY; CLINICAL TRIAL (TOPIC); EMBRYONIC STEM CELL; ENDOTHELIAL PROGENITOR CELL; EPITHELIUM CELL; ETHICS; EVIDENCE BASED PRACTICE; EXPERIMENTAL ANIMAL; FETAL STEM CELL; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOMODULATION; MESENCHYMAL STEM CELL; NONHUMAN; PHYSIOLOGICAL PROCESS; PLACENTA; PREGNANCY; REVIEW; STEM CELL TRANSPLANTATION; TERATOMA; THERAPY EFFECT; UMBILICAL CORD BLOOD;

EID: 84888769449     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00194     Document Type: Review

References (143)

1. Akiyama, K., Chen, C., Wang, D., Xu, X., Qu, C., Yamaza, T., et al. (2012). Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 10, 544-555. doi: 10.1016/j.stem.2012.03.007
2. Akle, C. A., Adinolfi, M., Welsh, K. I., Leibowitz, S., and McColl, I. (1981). Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet 2, 1003-1005. doi: 10.1016/S0140-6736(81)91212-5
3. Alexanian, A. R., Maiman, D. J., Kurpad, S. N., and Gennarelli, T. A. (2008). In vitro and in vivo characterization of neurally modified mesenchymal stem cells induced by epigenetic modifiers and neural stem cell environment. Stem Cells Dev. 17, 1123-1130. doi: 10.1089/scd.2007.0212
4. Ali, H., and Bahbahani, H. (2010). Umbilical cord blood stem cells - potential therapeutic tool for neural injuries and disorders. Acta Neurobiol. Exp. (Wars) 70, 316-324.
5. Andressen, C. (2013). Neural stem cells: from neurobiology to clinical applications. Curr. Pharm. Biotechnol. 14, 20-28. doi: 10.2174/1389201011314010005
6. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., et al. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967. doi: 10.1126/science.275.5302.964
7. Au, P., Daheron, L. M., Duda, D. G., Cohen, K. S., Tyrrell, J. A., Lanning, R. M., et al. (2008). Differential in vivo potential of endothelial progenitor cells from human umbilical cord blood and adult peripheral blood to form functional long-lasting vessels. Blood 111, 1302-1305. doi: 10.1182/blood-2007-06-094318
8. Azzopardi, D., and Edwards, A. D. (2010). Magnetic resonance biomarkers of neuroprotective effects in infants with hypoxic ischemic encephalopathy. Semin. Fetal Neonatal Med. 15, 261-269. doi: 10.1016/j.siny.2010.03.001
9. Bailo, M., Soncini, M., Vertua, E., Signoroni, P. B., Sanzone, S., Lombardi, G., et al. (2004). Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 78, 1439-1448. doi: 10.1097/01.TP.0000144606.84234.49
10. Baumhakel, M., Werner, N., Bohm, M., and Nickenig, G. (2006). Circulating endothelial progenitor cells correlate with erectile function in patients with coronary heart disease. Eur. Heart J. 27, 2184-2188. doi: 10.1093/eurheartj/ehl202
11. Bennet, L., Roelfsema, V., Dean, J. M., Wassink, G., Power, G. G., Jensen, E. C., et al. (2007). Regulation of cytochrome oxidase redox state during umbilical cord occlusion in preterm fetal sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1569-R1576. doi: 10.1152/ajpregu.00743.2006
12. Berger, R., and Garnier, Y. (2000). Perinatal brain injury. J. Perinat. Med. 28, 261-285. doi: 10.1515/JPM.2000.034
13. Berry, M. F., Engler, A. J., Woo, Y. J., Pirolli, T. J., Bish, L. T., Jayasankar, V., et al. (2006). Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am. J. Physiol. Heart Circ. Physiol. 290, H2196-H2203. doi: 10.1152/ajpheart.01017.2005
14. Borghesi, A., Massa, M., Campanelli, R., Bollani, L., Tzialla, C., Figar, T. A., et al. (2009). Circulating endothelial progenitor cells in preterm infants with bronchopulmonary dysplasia. Am. J. Respir. Crit. Care Med. 180, 540-546. doi: 10.1164/rccm.200812-1949OC
15. Broughton, B. R., Lim, R., Arumugam, T. V., Drummond, G. R., Wallace, E. M., and Sobey, C. G. (2013). Post-stroke inflammation and the potential efficacy of novel stem cell therapies: focus on amnion epithelial cells. Front. Cell. Neurosci. 6:66. doi: 10.3389/fncel.2012.00066
16. Broxmeyer, H. E., Douglas, G. W., Hangoc, G., Cooper, S., Bard, J., English, D., et al. (1989). Human umbilical cord blood as a potential source of transplantable hematopoietic stem/progenitor cells. Proc. Natl. Acad. Sci. U.S.A. 86, 3828-3832. doi: 10.1073/pnas.86.10.3828
17. Busch, S. A., Hamilton, J. A., Horn, K. P., Cuascut, F. X., Cutrone, R., Lehman, N., et al. (2011). Multipotent adult progenitor cells prevent macrophage-mediated axonal dieback and promote regrowth after spinal cord injury. J. Neurosci. 31, 944-953. doi: 10.1523/JNEUROSCI.3566-10.2011
18. Buzanska, L., Jurga, M., Stachowiak, E. K., Stachowiak, M. K., and Domanska-Janik, K. (2006). Neural stem-like cell line derived from a nonhematopoietic population of human umbilical cord blood. Stem Cells Dev. 15, 391-406. doi: 10.1089/scd.2006.15.391
19. Campagnoli, C., Roberts, I., Kumar, S., Bennett, P. R., and Fisk, N. M. (2001). Clonal culture of fetal cells from maternal blood. Lancet 357, 962. doi: 10.1016/S0140-6736(05)71666-4
20. Caplan, A. I., and Dennis, J. E. (2006). Mesenchymal stem cells as trophic mediators. J. Cell. Biochem. 98, 1076-1084. doi: 10.1002/jcb.20886
21. Chang, Y. S., Choi, S. J., Ahn, S. Y., Sung, D. K., Sung, S. I., Yoo, H. S., et al. (2013). Timing of umbilical cord blood derived mesenchymal stem cells transplantation determines therapeutic efficacy in the neonatal hyperoxic lung injury. PLoS ONE 8:e52419. doi: 10.1371/journal.pone.0052419
22. Chen, C. I., and Keating, A. (2001). Beyond bone marrow: a new source of stem cells. CMAJ 164, 683. doi: 10.1097/PRS.0b013e31818236b7
23. Daadi, M. M., Hu, S., Klausner, J., Li, Z., Sofilos, M., Sun, G., et al. (2013). Imaging neural stem cell graft-induced structural repair in stroke. Cell Transplant. 41, 516-526. doi: 10.3727/096368912X656144
24. De Coppi, P., Bartsch, G. Jr., Siddiqui, M. M., Xu, T., Santos, C. C., Perin, L., et al. (2007). Isolation of amniotic stem cell lines with potential for therapy. Nat. Biotechnol. 25, 100-106. doi: 10.1038/nbt1274
25. Deng, J., Petersen, B. E., Steindler, D. A., Jorgensen, M. L., and Laywell, E. D. (2006). Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24, 1054-1064. doi: 10.1634/stemcells.2005-0370
26. de Paula, S., Greggio, S., Marinowic, D. R., Machado, D. C., and DaCosta, J. C. (2012). The dose-response effect of acute intravenous transplantation of human umbilical cord blood cells on brain damage and spatial memory deficits in neonatal hypoxia-ischemia. Neuroscience 210, 431-441. doi: 10.1016/j.neuroscience.2012.03.009
27. Devine, S. M. (2002). Mesenchymal stem cells: will they have a role in the clinic. J. Cell. Biochem. Suppl. 38, 73-79. doi: 10.1002/jcb.10046
28. Donega, V., van Velthoven, C. T., Nijboer, C. H., van Bel, F., Kas, M. J., Kavelaars, A., et al. (2013). Intranasal mesenchymal stem cell treatment for neonatal brain damage: long-term cognitive and sensorimotor improvement. PLoS ONE 8:e51253. doi: 10.1371/journal.pone.0051253
29. Edwards, A. D., Brocklehurst, P., Gunn, A. J., Halliday, H., Juszczak, E., Levene, M., et al. (2010). 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. doi: 10.1136/bmj.c363
30. Elwan, M. A., Thangavel, R., Ono, F., and Sakuragawa, N. (1998). Synthesis and release of catecholamines by cultured monkey amniotic epithelial cells. J. Neurosci. Res. 53, 107-113. doi: 10.1002/(SICI)1097-4547(19980701)53:1<107::AID-JNR11>3.0.CO;2-6
31. Fan, Y., Shen, F., Frenzel, T., Zhu, W., Ye, J., Liu, J., et al. (2010). Endothelial progenitor cell transplantation improves long-term stroke outcome in mice. Ann. Neurol. 67, 488-497. doi: 10.1002/ana.21919
32. Felling, R. J., Snyder, M. J., Romanko, M. J., Rothstein, R. P., Ziegler, A. N., Yang, Z., et al. (2006). Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ischemia. J. Neurosci. 26, 4359-4369. doi: 10.1523/JNEUROSCI.1898-05.2006
33. Ferriero, D. M. (2004). Neonatal brain injury. N. Engl. J. Med. 351, 1985-1995. doi: 10.1056/NEJMra041996
34. Fibbe, W. E., Nauta, A. J., and Roelofs, H. (2007). Modulation of immune responses by mesenchymal stem cells. Ann. N.Y. Acad. Sci. 1106, 272-278. doi: 10.1196/annals.1392.025
35. Galindo, L. T., Filippo, T. R., Semedo, P., Ariza, C. B., Moreira, C. M., Camara, N. O., and Porcionatto, M. A. (2011). Mesenchymal stem cell therapy modulates the inflammatory response in experimental traumatic brain injury. Neurol. Res. Int. 2011, 564089. doi: 10.1155/2011/564089
36. Geissler, M., Dinse, H. R., Neuhoff, S., Kreikemeier, K., and Meier, C. (2011). Human umbilical cord blood cells restore brain damage induced changes in rat somatosensory cortex. PLoS ONE 6:e20194. doi: 10.1371/journal.pone.0020194
37. Gerdoni, E., Gallo, B., Casazza, S., Musio, S., Bonanni, I., Pedemonte, E., et al. (2007). Mesenchymal stem cells effectively modulate pathogenic immune response in experimental autoimmune encephalomyelitis. Ann. Neurol. 61, 219-227. doi: 10.1002/ana.21076
38. Gluckman, E., Broxmeyer, H. A., Auerbach, A. D., Friedman, H. S., Douglas, G. W., Devergie, A., et al. (1989). Hematopoietic reconstitution in a patient with Fanconi's anemia by means of umbilical-cord blood from an HLA-identical sibling. N. Engl. J. Med. 321, 1174-1178. doi: 10.1056/NEJM198910263211707
39. Gunn, A. J., Battin, M., Gluckman, P. D., Gunn, T. R., and Bennet, L. (2005). Therapeutic hypothermia: from lab to NICU. J. Perinat. Med. 33, 340-346. doi: 10.1515/JPM.2005.061
40. Gunn, A. J., and Bennet, L. (2009). Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clin. Perinatol. 36, 579-593. doi: 10.1016/j.clp.2009.06.007
41. Gunn, A. J., Gluckman, P. D., and Gunn, T. R. (1998). Selective head cooling in newborn infants after perinatal asphyxia: a safety study. Pediatrics 102, 885-892. doi: 10.1542/peds.102.4.885
42. Gunn, A. J., and Thoresen, M. (2006). Hypothermic neuroprotection. NeuroRx 3, 154-169. doi: 10.1016/j.nurx.2006.01.007
43. Gussin, H. A., Bischoff, F. Z., Hoffman, R., and Elias, S. (2002). Endothelial precursor cells in the peripheral blood of pregnant women. J. Soc. Gynecol. Investig. 9, 357-361. doi: 10.1016/S1071-5576(02)00188-0
44. Harris, D. T., and Rogers, I. (2007). Umbilical cord blood: a unique source of pluripotent stem cells for regenerative medicine. Curr. Stem Cell Res. Ther. 2, 301-309. doi: 10.2174/157488807782793790
45. Harris, M. N., Carey, W. A., Ellsworth, M. A., Haas, L. R., Hartman, T. K., Lang, T. R., et al. (2013). Perceptions and practices of therapeutic hypothermia in American neonatal intensive care units. Am. J. Perinatol. doi: 10.1055/s-0033-1334454. [Epub ahead of print].
46. Hebertson, R. M., Hammond, M. E., and Bryson, M. J. (1986). Amniotic epithelial ultrastructure in normal, polyhydramnic, and oligohydramnic pregnancies. Obstet. Gynecol. 68, 74-79.
47. Hermann, A., List, C., Habisch, H. J., Vukicevic, V., Ehrhart-Bornstein, M., Brenner, R., et al. (2010). Age-dependent neuroectodermal differentiation capacity of human mesenchymal stromal cells: limitations for autologous cell replacement strategies. Cytotherapy 12, 17-30. doi: 10.3109/14653240903313941
48. Herranz, A. S., Gonzalo-Gobernado, R., Reimers, D., Asensio, M. J., Rodriguez-Serrano, M., and Bazan, E. (2010). Applications of human umbilical cord blood cells in central nervous system regeneration. Curr. Stem Cell Res. Ther. 5, 17-22. doi: 10.2174/157488810790442822
49. Higgins, R. D., Raju, T., Edwards, A. D., Azzopardi, D. V., Bose, C. L., Clark, R. H., et al. (2011). Hypothermia and other treatment options for neonatal encephalopathy: an executive summary of the Eunice Kennedy Shriver NICHD workshop. J. Pediatr. 159, 851-858.e1. doi: 10.1016/j.jpeds.2011.08.004
50. Hipp, J., and Atala, A. (2006). "GeneChips in regenerative medicine," in Principles of Regenerative Medicine, eds A. Atala, R. Lanza, J. Thomson, and R. Nerem (Philadelphia, PA: Elsevier), 562-578.
51. Hodges, R. J., Jenkin, G., Hooper, S. B., Allison, B., Lim, R., Dickinson, H., et al. (2012). Human amnion epithelial cells reduce ventilation-induced preterm lung injury in fetal sheep. Am. J. Obstet. Gynecol. 206, 448.e8-448.e15. doi: 10.1016/j.ajog.2012.02.038
52. Horn, M., and Schlote, W. (1992). [Cerebral resuscitation]. Z. Gesamte Inn. Med. 47, 115-126.
53. Hristov, M., and Weber, C. (2004). Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J. Cell. Mol. Med. 8, 498-508. doi: 10.1111/j.1582-4934.2004.tb00474.x
54. Ilancheran, S., Michalska, A., Peh, G., Wallace, E. M., Pera, M., and Manuelpillai, U. (2007). Stem cells derived from human fetal membranes display multilineage differentiation potential. Biol. Reprod. 77, 577-588. doi: 10.1095/biolreprod.106.055244
55. Ingram, D. A., Mead, L. E., Tanaka, H., Meade, V., Fenoglio, A., Mortell, K., et al. (2004). Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104, 2752-2760. doi: 10.1182/blood-2004-04-1396
56. Itoo, B. A., Al-Hawsawi, Z. M., and Khan, A. H. (2003). Hypoxic ischemic encephalopathy. Incidence and risk factors in North Western Saudi Arabia. Saudi Med. J. 24, 147-153. doi: 10.1016/j.earlhumdev.2010.05.010
57. Iwasaki, R., Matsubara, S., Takizawa, T., Takayama, T., Yashiro, T., and Suzuki, M. (2003). Human amniotic epithelial cells are morphologically homogeneous: enzymehistochemical, tracer, and freeze-substitution fixation study. Eur. J. Histochem. 47, 223-232. doi: 10.4081/831
58. Javed, M. J., Mead, L. E., Prater, D., Bessler, W. K., Foster, D., Case, J., et al. (2008). Endothelial colony forming cells and mesenchymal stem cells are enriched at different gestational ages in human umbilical cord blood. Pediatr. Res. 64, 68-73. doi: 10.1203/PDR.0b013e31817445e9
59. Johnston, M. V., Fatemi, A., Wilson, M. A., and Northington, F. (2011). Treatment advances in neonatal neuroprotection and neurointensive care. Lancet Neurol. 10, 372-382. doi: 10.1016/S1474-4422(11)70016-3
60. Kakishita, K., Elwan, M. A., Nakao, N., Itakura, T., and Sakuragawa, N. (2000). Human amniotic epithelial cells produce dopamine and survive after implantation into the striatum of a rat model of Parkinson's disease: a potential source of donor for transplantation therapy. Exp. Neurol. 165, 27-34. doi: 10.1006/exnr.2000.7449
61. Katz, L. M., Young, A. S., Frank, J. E., Wang, Y., and Park, K. (2004). Regulated hypothermia reduces brain oxidative stress after hypoxic-ischemia. Brain Res. 1017, 85-91. doi: 10.1016/j.brainres.2004.05.020
62. Kennea, N. L., Waddington, S. N., Chan, J., O'Donoghue, K., Yeung, D., Taylor, D. L., et al. (2013). Differentiation of human fetal mesenchymal stem cells into cells with an oligodendrocyte phenotype. Cell Cycle 8, 1069-1079. doi: 10.4161/cc.8.7.8121
63. Kim, D., Chun, B. G., Kim, Y. K., Lee, Y. H., Park, C. S., Jeon, I., et al. (2008). In vivo tracking of human mesenchymal stem cells in experimental stroke. Cell Transplant. 16, 1007-1012. doi: 10.3727/000000007783472381
64. Kim, H. J., Lee, J. H., and Kim, S. H. (2010). Therapeutic effects of human mesenchymal stem cells on traumatic brain injury in rats: secretion of neurotrophic factors and inhibition of apoptosis. J. Neurotrauma 27, 131-138. doi: 10.1089/neu.2008.0818
65. Kitada, M., and Dezawa, M. (2012). Parkinson's disease and mesenchymal stem cells: potential for cell-based therapy. Parkinsons Dis. 2012:873706. doi: 10.1155/2012/873706
66. Kurtzberg, J. (1996). Umbilical cord blood: a novel alternative source of hematopoietic stem cells for bone marrow transplantation. J. Hematother. 5, 95-96. doi: 10.1089/scd.1.1996.5.95
67. Le Blanc, K. (2003). Immunomodulatory effects of fetal and adult mesenchymal stem cells. Cytotherapy 5, 485-489. doi: 10.1080/14653240310003611
68. Leviton, A., and Paneth, N. (1990). White matter damage in preterm newborns-an epidemiologic perspective. Early Hum. Dev. 24, 1-22. doi: 10.1016/0378-3782(90)90002-Z
69. Li, H., Niederkorn, J. Y., Neelam, S., Mayhew, E., Word, R. A., McCulley, J. P., et al. (2005). Immunosuppressive factors secreted by human amniotic epithelial cells. Invest. Ophthalmol. Vis. Sci. 46, 900-907. doi: 10.1167/iovs.04-0495
70. Li, J., Zhu, H., Liu, Y., Li, Q., Lu, S., Feng, M., et al. (2010). Human mesenchymal stem cell transplantation protects against cerebral ischemic injury and upregulates interleukin-10 expression in Macacafascicularis. Brain Res. 1334, 65-72. doi: 10.1016/j.brainres.2010.03.080
71. Li, S. F., Lu, X. F., and Sun, M. H. (2002). [Biological characteristics of mesenchymal stem cells in vitro derived from bone marrow of banna minipig inbred line]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 16, 354-358.
72. Liu, T., Wu, J., Huang, Q., Hou, Y., Jiang, Z., Zang, S., et al. (2008). Human amniotic epithelial cells ameliorate behavioral dysfunction and reduce infarct size in the rat middle cerebral artery occlusion model. Shock 29, 603-611. doi: 10.1097/SHK.0b013e318157e845
73. Locatelli, F., Rocha, V., Chastang, C., Arcese, W., Ortega, J., Pasquini, R., et al. (1998). Cord blood transplantation for children with acute leukemia. Eurocord transplant group. Bone Marrow Transplant. 21(Suppl. 3), S63-S65.
74. Mahmood, A., Lu, D., Qu, C., Goussev, A., and Chopp, M. (2005). Human marrow stromal cell treatment provides long-lasting benefit after traumatic brain injury in rats. Neurosurgery 57, 1026-1031. discussion: 1026-1031. doi: 10.1227/01.NEU.0000181369.76323.50
75. Mamede, A. C., Carvalho, M. J., Abrantes, A. M., Laranjo, M., Maia, C. J., and Botelho, M. F. (2012). Amniotic membrane: from structure and functions to clinical applications. Cell Tissue Res. 349, 447-458. doi: 10.1007/s00441-012-1424-6
76. Massaro, A. N., Bouyssi-Kobar, M., Chang, T., Vezina, L. G., du Plessis, A. J., and Limperopoulos, C. (2013). Brain perfusion in encephalopathic newborns after therapeutic hypothermia. Am. J. Neuroradiol. 34, 1649-1655. doi: 10.3174/ajnr.A3422
77. Miller, S. L., Yan, E. B., Castillo-Melendez, M., Jenkin, G., and Walker, D. W. (2005). Melatonin provides neuroprotection in the late-gestation fetal sheep brain in response to umbilical cord occlusion. Dev. Neurosci. 27, 200-210. doi: 10.1159/000085993
78. Miranville, A., Heeschen, C., Sengenes, C., Curat, C. A., Busse, R., and Bouloumie, A. (2004). Improvement of postnatal neovascularization by human adipose tissue-derived stem cells. Circulation 110, 349-355. doi: 10.1161/01.CIR.0000135466.16823.D0
79. Munoz, J. L., Greco, S. J., Patel, S. A., Sherman, L. S., Bhatt, S., Bhatt, R. S., et al. (2012). Feline bone marrow-derived mesenchymal stromal cells (MSCs) show similar phenotype and functions with regards to neuronal differentiation as human MSCs. Differentiation 84, 214-222. doi: 10.1016/j.diff.2012.07.002
80. Munoz, J. R., Stoutenger, B. R., Robinson, A. P., Spees, J. L., and Prockop, D. J. (2005). Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc. Natl. Acad. Sci. U.S.A. 102, 18171-18176. doi: 10.1073/pnas.0508945102
81. Murphy, S., Rosli, S., Acharya, R., Mathias, L., Lim, R., Wallace, E., et al. (2010). Amnion epithelial cell isolation and characterization for clinical use. Curr. Protoc. Stem Cell Biol. Chapter 1, Unit 1E 6. doi: 10.1002/9780470151808.sc01e06s13
82. Ohta, T., Kikuta, K., Imamura, H., Takagi, Y., Nishimura, M., Arakawa, Y., et al. (2006). Administration of ex vivo-expanded bone marrow-derived endothelial progenitor cells attenuates focal cerebral ischemia-reperfusion injury in rats. Neurosurgery 59, 679-686. doi: 10.1227/01.NEU.0000229058.08706.88
83. Paolo, T. (2012). The high-risk newborns. J. Matern. Fetal. Neonatal. Med. 25(Suppl. 1), 6-7. doi: 10.3109/14767058.2012.664893
84. Parolini, O., Alviano, F., Bagnara, G. P., Bilic, G., Buhring, H. J., Evangelista, M., et al. (2008). Concise review: isolation and characterization of cells from human term placenta: outcome of the first international workshop on placenta derived stem cells. Stem Cells 26, 300-311. doi: 10.1634/stemcells.2007-0594
85. Parr, A. M., Tator, C. H., and Keating, A. (2007). Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant. 40, 609-619. doi: 10.1038/sj.bmt.1705757
86. Peichev, M., Naiyer, A. J., Pereira, D., Zhu, Z., Lane, W. J., Williams, M., et al. (2000). Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 95, 952-958. doi: 10.1016/S0008-6363(03)00252-9
87. Penrice, J., and Nussey, S. S. (1992). Recovery of adrenocortical function following treatment of tuberculous Addison's disease. Postgrad. Med. J. 68, 204-205. doi: 10.1136/pgmj.68.797.204
88. Perlman, J. M. (2004). Brain injury in the term infant. Semin. Perinatol. 28, 415-424. doi: 10.1053/j.semperi.2004.10.003
89. Pimentel-Coelho, P. M., Rosado-de-Castro, P. H., da Fonseca, L. M., and Mendez-Otero, R. (2012). Umbilical cord blood mononuclear cell transplantation for neonatal hypoxic-ischemic encephalopathy. Pediatr. Res. 71, 464-473. doi: 10.1038/pr.2011.59
90. Pipes, B. L., and Ablin, R. J. (2006). Embryonic stem cell co-transplantation revisited: utility of umbilical cord blood "embryonic-like" stem cells. Ann. Clin. Lab. Sci. 36, 105-106. doi: 10.2217/17460751.1.6.777
91. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., et al. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147. doi: 10.1126/science.284.5411.143
92. Potapova, I. A., Gaudette, G. R., Brink, P. R., Robinson, R. B., Rosen, M. R., Cohen, I. S., et al. (2007). Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro. Stem Cells 25, 1761-1768. doi: 10.1634/stemcells.2007-0022
93. Red-Horse, K., Crawford, Y., Shojaei, F., and Ferrara, N. (2007). Endothelium-microenvironment interactions in the developing embryo and in the adult. Dev. Cell 12, 181-194. doi: 10.1016/j.devcel.2007.01.013
94. Red-Horse, K., and Ferrara, N. (2006). Imaging tumor angiogenesis. J. Clin. Invest. 116, 2585-2587. doi: 10.1172/JCI30058
95. Rehman, J., Traktuev, D., Li, J., Merfeld-Clauss, S., Temm-Grove, C. J., Bovenkerk, J. E., et al. (2004). Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109, 1292-1298. doi: 10.1161/01.CIR.0000121425.42966.F1
96. Reyes, M., and Verfaillie, C. M. (2001). Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann. N.Y. Acad. Sci. 938, 231-233. discussion: 233-235. doi: 10.1111/j.1749-6632.2001.tb03593.x
97. Reynolds, B. A., Tetzlaff, W., and Weiss, S. (1992). A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12, 4565-4574.
98. Rice, J. E. 3rd., Vannucci, R. C., and Brierley, J. B. (1981). The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131-141. doi: 10.1002/ana.410090206
99. Roth, S. C., Edwards, A. D., Cady, E. B., Delpy, D. T., Wyatt, J. S., Azzopardi, D., et al. (1992). Relation between cerebral oxidative metabolism following birth asphyxia, and neurodevelopmental outcome and brain growth at one year. Dev. Med. Child Neurol. 34, 285-295. doi: 10.1111/j.1469-8749.1992.tb11432.x
100. Sakuragawa, N., Misawa, H., Ohsugi, K., Kakishita, K., Ishii, T., Thangavel, R., et al. (1997). Evidence for active acetylcholine metabolism in human amniotic epithelial cells: applicable to intracerebral allografting for neurologic disease. Neurosci. Lett. 232, 53-56. doi: 10.1016/S0304-3940(97)00570-3
101. Sakuragawa, N., Thangavel, R., Mizuguchi, M., Hirasawa, M., and Kamo, I. (1996). Expression of markers for both neuronal and glial cells in human amniotic epithelial cells. Neurosci. Lett. 209, 9-12. doi: 10.1016/0304-3940(96)12599-4
102. Seo, J. H., and Cho, S. R. (2012). Neurorestoration induced by mesenchymal stem cells: potential therapeutic mechanisms for clinical trials. Yonsei Med. J. 53, 1059-1067. doi: 10.3349/ymj.2012.53.6.1059
103. Shankaran, S., Laptook, A. R., Ehrenkranz, R. A., Tyson, J. E., McDonald, S. A., Donovan, E. F., et al. (2005). Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N. Engl. J. Med. 353, 1574-1584. doi: 10.1056/NEJMcps050929
104. Simbruner, G., Mittal, R. A., Rohlmann, F., and Muche, R. (2010). Systemic hypothermia after neonatal encephalopathy: outcomes of neo.nEURO.network RCT. Pediatrics 126, e771-e778. doi: 10.1542/peds.2009-2441
105. Slatter, M. A., Bhattacharya, A., Flood, T. J., Abinun, M., Cant, A. J., and Gennery, A. R. (2006). Use of two unrelated umbilical cord stem cell units in stem cell transplantation for Wiskott-Aldrich syndrome. Pediatr. Blood Cancer 47, 332-334. doi: 10.1002/pbc.20450
106. Solomon, A., Rosenblatt, M., Monroy, D., Ji, Z., Pflugfelder, S. C., and Tseng, S. C. (2001). Suppression of interleukin 1alpha and interleukin 1beta in human limbal epithelial cells cultured on the amniotic membrane stromal matrix. Br. J. Ophthalmol. 85, 444-449. doi: 10.1136/bjo.85.4.444
107. Sommer, L., and Rao, M. (2002). Neural stem cells and regulation of cell number. Prog. Neurobiol. 66, 1-18. doi: 10.1016/S0301-0082(01)00022-3
108. Sugawara, J., Mitsui-Saito, M., Hoshiai, T., Hayashi, C., Kimura, Y., and Okamura, K. (2005). Circulating endothelial progenitor cells during human pregnancy. J. Clin. Endocrinol. Metab. 90, 1845-1848. doi: 10.1210/jc.2004-0541
109. Swijnenburg, R. J., Tanaka, M., Vogel, H., Baker, J., Kofidis, T., Gunawan, F., et al. (2005). Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 112(9 Suppl.), I166-I172. doi: 10.1161/CIRCULATIONAHA.104.525824
110. Tajiri, N., Acosta, S., Glover, L. E., Bickford, P. C., Jacotte Simancas, A., Yasuhara, T., et al. (2012). Intravenous grafts of amniotic fluid-derived stem cells induce endogenous cell proliferation and attenuate behavioral deficits in ischemic stroke rats. PLoS ONE 7:e43779. doi: 10.1371/journal.pone.0043779
111. Tan, J. L., Chan, S. T., Wallace, E. M., and Lim, R. (2013). Human amnion epithelial cells mediate lung repair by directly modulating macrophage recruitment and polarization. Cell Transplant. doi: 10.3727/096368912X661409. [Epub ahead of print].
112. Tepper, O. M., Galiano, R. D., Capla, J. M., Kalka, C., Gagne, P. J., Jacobowitz, G. R., et al. (2002). Human endothelial progenitor cells from type II diabetics exhibit impaired proliferation, adhesion, and incorporation into vascular structures. Circulation 106, 2781-2786. doi: 10.1161/01.CIR.0000039526.42991.93
113. Titomanlio, L., Kavelaars, A., Dalous, J., Mani, S., El Ghouzzi, V., Heijnen, C., et al. (2011). Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann. Neurol. 70, 698-712. doi: 10.1002/ana.22518
114. Tiwari, A., Tursky, M. L., Mushahary, D., Wasnik, S., Collier, F. M., Suma, K., et al. (2012). Ex vivo expansion of haematopoietic stem/progenitor cells from human umbilical cord blood on acellular scaffolds prepared from MS-5 stromal cell line. J. Tissue Eng. Regen. Med. doi: 10.1002/term.1479. [Epub ahead of print].
115. Toda, A., Okabe, M., Yoshida, T., and Nikaido, T. (2007). The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J. Pharmacol. Sci. 105, 215-228. doi: 10.1254/jphs.CR0070034
116. Tursky, M. L., Collier, F. M., Ward, A. C., and Kirkland, M. A. (2012). Systematic investigation of oxygen and growth factors in clinically valid ex vivo expansion of cord blood CD34(+) hematopoietic progenitor cells. Cytotherapy 14, 679-685. doi: 10.3109/14653249.2012.666851
117. Vannucci, R. C., and Perlman, J. M. (1997). Interventions for perinatal hypoxic-ischemic encephalopathy. Pediatrics 100, 1004-1014. doi: 10.1542/peds.100.6.1004
118. van Velthoven, C. T., Kavelaars, A., van Bel, F., and Heijnen, C. J. (2011a). Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration. Brain Behav. Immun. 24, 387-393. doi: 10.1016/j.bbi.2009.10.017
119. van Velthoven, C. T., Kavelaars, A., van Bel, F., and Heijnen, C. J. (2011b). Mesenchymal stem cell transplantation changes the gene expression profile of the neonatal ischemic brain. Brain Behav. Immun. 25, 1342-1348. doi: 10.1016/j.bbi.2011.03.021
120. Vasa, M., Fichtlscherer, S., Aicher, A., Adler, K., Urbich, C., Martin, H., et al. (2001). Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ. Res. 89, E1-E7. doi: 10.1161/hc2401.092816
121. Volpe, J. J. (2001a). Perinatal brain injury: from pathogenesis to neuroprotection. Ment. Retard. Dev. Disabil. Res. Rev. 7, 56-64. doi: 10.1002/1098-2779(200102)7:1<56::AID-MRDD1008>3.0.CO;2-A
122. Volpe, J. J. (2001b). Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50, 553-562. doi: 10.1203/00006450-200111000-00003
123. Volpe, J. J. (2012). Neonatal encephalopathy: an inadequate term for hypoxic-ischemic encephalopathy. Ann. Neurol. 72, 156-166. doi: 10.1002/ana.23647
124. Vosdoganes, P., Hodges, R. J., Lim, R., Westover, A. J., Acharya, R. Y., Wallace, E. M., et al. (2011). Human amnion epithelial cells as a treatment for inflammation-induced fetal lung injury in sheep. Am. J. Obstet. Gynecol. 205, 156.e26-156.e33. doi: 10.1016/j.ajog.2011.03.054
125. Vosdoganes, P., Wallace, E. M., Chan, S. T., Acharya, R., Moss, T. J., and Lim, R. (2012). Human amnion epithelial cells repair established lung injury. Cell Transplant. 22, 1337-1349. doi: 10.3727/096368912X657657
126. Wang, F., Maeda, N., Yasuhara, T., Kameda, M., Tsuru, E., Yamashita, T., et al. (2012). The therapeutic potential of human umbilical cord blood transplantation for neonatal hypoxic-ischemic brain injury and ischemic stroke. Acta Med. Okayama 66, 429-434. doi: 10.1111/j.1582-4934.2008.00671.x
127. Wang, L., Ji, H., Zhou, J., Xie, J., Zhong, Z., Li, M., et al. (2013a). Therapeutic potential of umbilical cord mesenchymal stromal cells transplantation for cerebral palsy: a case report. Case Rep. Transplant. 2013, 146347. doi: 10.1155/2013/146347
128. Wang, X. L., Zhao, Y. S., Hu, M. Y., Sun, Y. Q., Chen, Y. X., and Bi, X. H. (2013b). Umbilical cord blood cells regulate endogenous neural stem cell proliferation via Hedgehog signaling in hypoxic-ischemic neonatal rats. Brain Res. 1518, 26-35. doi: 10.1016/j.brainres.2013.04.038
129. Wasielewski, B., Jensen, A., Roth-Harer, A., Dermietzel, R., and Meier, C. (2012). Neuroglial activation and Cx43 expression are reduced upon transplantation of human umbilical cord blood cells after perinatal hypoxic-ischemic injury. Brain Res. 1487, 39-53. doi: 10.1016/j.brainres.2012.05.066
130. Werner, N., and Nickenig, G. (2006a). Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy. Arterioscler. Thromb. Vasc. Biol. 26, 257-266. doi: 10.1161/01.ATV.0000198239.41189.5d
131. Werner, N., and Nickenig, G. (2006b). Clinical and therapeutical implications of EPC biology in atherosclerosis. J. Cell. Mol. Med. 10, 318-332. doi: 10.1111/j.1582-4934.2006.tb00402.x
132. Woodbury, D., Schwarz, E. J., Prockop, D. J., and Black, I. B. (2000). Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61, 364-370. doi: 10.1002/1097-4547(20000815)61:4<364::AID-JNR2>3.0.CO;2-C
133. Xia, G., Hong, X., Chen, X., Lan, F., Zhang, G., and Liao, L. (2010). Intracerebral transplantation of mesenchymal stem cells derived from human umbilical cord blood alleviates hypoxic ischemic brain injury in rat neonates. J. Perinat. Med. 38, 215-221. doi: 10.1515/jpm.2010.021
134. Xin, H., Li, Y., Shen, L. H., Liu, X., Wang, X., Zhang, J., et al. (2010). Increasing tPA activity in astrocytes induced by multipotent mesenchymal stromal cells facilitate neurite outgrowth after stroke in the mouse. PLoS ONE 5:e9027. doi: 10.1371/journal.pone.0009027
135. Yang, X., Song, L., Wu, N., Liu, Z., Xue, S., and Hui, G. (2010). An experimental study on intracerebroventricular transplantation of human amniotic epithelial cells in a rat model of Parkinson's disease. Neurol. Res. 32, 1054-1059. doi: 10.1179/016164110X12681290831207
136. Yawno, T., Schuilwerve, J., Moss, T. J. M., Vosdoganes, P., Westover, A. J., Afandi, E., et al. (2013). Human amnion epithelial cells reduce fetal brain injury in response to intrauterine inflammation. Dev. Neurosci. 35, 272-282. doi: 10.1159/000346683
137. Yi, E. S., Lee, S. H., Son, M. H., Kim, J. Y., Cho, E. J., Lim, S. J., et al. (2012). Hematopoietic stem cell transplantation in children with acute leukemia: similar outcomes in recipients of umbilical cord blood versus marrow or peripheral blood stem cells from related or unrelated donors. Korean J. Pediatr. 55, 93-99. doi: 10.3345/kjp.2012.55.3.93
138. Yoder, M. C., Mead, L. E., Prater, D., Krier, T. R., Mroueh, K. N., Li, F., et al. (2007). Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109, 1801-1809. doi: 10.1182/blood-2006-08-043471
139. Yoon, B. H., Park, C. W., and Chaiworapongsa, T. (2003). Intrauterine infection and the development of cerebral palsy. BJOG 110(Suppl. 20), 124-127. doi: 10.1046/j.1471-0528.2003.00063.x
140. Yu, S. J., Soncini, M., Kaneko, Y., Hess, D. C., Parolini, O., and Borlongan, C. V. (2009). Amnion: a potent graft source for cell therapy in stroke. Cell Transplant. 18, 111-118. doi: 10.3727/096368909788341243
141. Zampetaki, A., Kirton, J. P., and Xu, Q. (2008). Vascular repair by endothelial progenitor cells. Cardiovasc. Res. 78, 413-421. doi: 10.1093/cvr/cvn081
142. Zhang, Z. G., Zhang, L., Jiang, Q., and Chopp, M. (2002). Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ. Res. 90, 284-288. doi: 10.1161/hh0302.104460
143. Zilka, N., Zilkova, M., Kazmerova, Z., Sarissky, M., Cigankova, V., and Novak, M. (2011). Mesenchymal stem cells rescue the Alzheimer's disease cell model from cell death induced by misfolded truncated tau. Neuroscience 193, 330-337. doi: 10.1016/j.neuroscience.2011.06.088