Umbilical cord blood-derived CD34+ cells improve outcomes of traumatic brain injury in rats by stimulating angiogenesis and neurogenesis

Cell Transplantation

Volumn 23, Issue 8, 2014, Pages 959-979

  Chen, Sheng Hsien ^a,b   Wang, Jhi Joung ^c   Chen, Chung Hwan ^d   Chang, Hsiu Kang ^e   Lin, Mao Tsun ^c   Chang, Fong Ming ^f   Chio, Chung Ching ^c  

^a Da An Women and Children Hospital   (Taiwan)

^b SOUTHERN TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

^c CHI MEI MEDICAL CENTER   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^e Stem Cell Research Center   (Taiwan)

^f NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Angiogenesis; Apoptosis; Cytokines; Neurogenesis; Progenitor cells; Traumatic brain injury

Indexed keywords

CASPASE 3; CD34 ANTIGEN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; NEURON SPECIFIC NUCLEAR PROTEIN; PHOSPHATE BUFFERED SALINE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; ANGIOGENIC FACTOR;

ADULT; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW; BRAIN CONTUSION; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN NERVE CELL; CELL MIGRATION; CELL VIABILITY; CONTROLLED STUDY; CORD BLOOD STEM CELL TRANSPLANTATION; ENDOTHELIAL PROGENITOR CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; INFLAMMATION; INTRACRANIAL HYPERTENSION; MALE; MOTOR DYSFUNCTION; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGICAL COMPLICATION; NEUROPROTECTION; NICK END LABELING; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RAT; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURIES; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; ANTIGENS, CD34; BRAIN INJURIES; CORD BLOOD STEM CELL TRANSPLANTATION; HUMANS; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; NEUROGENESIS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84905278590     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368913X667006     Document Type: Article

References (74)

1. Bullock, R.; Zauner, A.; Woodward, J.; Young, H. F. Massive persistent release of excitatory amino acids following human occlusive stroke. Stroke 26: 2187-2189; 1995.
2. Chang, C. P.; Chio, C. C.; Cheong, C. U.; Chao, C. M.; Cheng, B. C.; Lin, M. T. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin. Sci. 124: 165-176; 2013.
3. Chang, M. W.; Young, M. S.; Lin, M. T. An inclined plane system with microcontroller to determine limb motor function of laboratory animals. J. Neurosci. Methods 168: 186-194; 2008.
4. Chen, J.; Sanberg, P. R.; Li, Y.; Wang, L.; Lu, M.; Willing, A. E.; Sanchez-Ramos, J.; Chopp, M. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke 32: 2682-2688; 2001.
5. Chen, L. W.; Egan, L.; Li, Z. W.; Greten, F. R.; Kagnoff, M. F.; Karin, M. The two faces of IKK and NF-kappa B inhibition: Prevention of systemic inflammation but increased local injury following intestinal ischemia-reperfusion. Nat. Med. 9: 575-581; 2003.
6. Chen, Q.; Long, Y.; Yuan, X.; Zou, L.; Sun, J.; Chen, S.; Perez-Polo, J. R.; Yang, K. Protective effects of bone marrow stromal cell transplantation in injured rodent brain: Synthesis of neurotrophic factors. J. Neurosci. Res. 80: 611-619; 2005.
7. Chen, S. H.; Chang, C. Y.; Chang, H. K.; Chen, W. C.; Lin, M. T.; Wang, J. J.; Chen, J. C.; Chang, F. M. Premarin stimulates estrogen receptor-alpha to protect against traumatic brain injury in male rats. Crit. Care Med. 37: 3097-3106; 2009.
8. Chen, S. H.; Chang, F. M.; Tsai, Y. C.; Huang, K. F.; Lin, M. T. Resuscitation from experimental heatstroke by transplantation of human umbilical cord blood cells. Crit. Care Med. 33: 1377-1383; 2005.
9. Chen, X.; Katakowski, M.; Li, Y.; Lu, D.; Wang, L.; Zhang, L.; Chen, J.; Xu, Y.; Gautam, S.; Mahmood, A.; Chopp, M. Human bone marrow stromal cell cultures conditioned by traumatic brain tissue extracts: Growth factor production. J. Neurosci. Res. 69: 687-691; 2002.
10. Cheng, B. C.; Chang, C. P.; Lin, M. T.; Lee, C. C. Inhibition of neuronal nitric oxide synthase causes attenuation of cerebrovascular dysfunction in experimental heatstroke. Neuropharmacology 52: 297-305; 2007.
11. Chio, C. C.; Chang, C. P.; Lin, M. T. Hypoxic preconditioning enhances the potentially therapeutic secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Science 338(6113): 1485(Suppl)59-60; 2012.
12. Chou, Y. T.; Lai, S. T.; Lee, C. C.; Lin, M. T. Hypothermia attenuates circulatory shock and cerebral ischemia in experimental heatstroke. Shock 19: 388-393; 2003.
13. Dennis, J. E.; Charbord, P. Origin and differentiation of human and murine stroma. Stem Cells 20: 205-214; 2002.
14. Drago, J.; Murphy, M.; Carroll, S. M.; Harvey, R. P.; Bartlett, P. F. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc. Natl. Acad. Sci. USA 88: 2199-2203; 1991.
15. Elfenbein, G. J.; Sackstein, R. Primed marrow for autologous and allogeneic transplantation: A review comparing primed marrow to mobilized blood and steady-state marrow. Exp. Hematol. 32: 327-339; 2004.
16. Erices, A.; Conget, P.; Minguell, J. J. Mesenchymal progenitor cells in human umbilical cord blood. Br. J. Haematol. 109: 235-242; 2000.
17. Eriksson, P. S.; Perfilieva, E.; Björk-Eriksson, T.; Alborn, A. M.; Nordborg, C.; Peterson, D. A.; Gage, F. H. Neurogenesis in the adult human hippocampus. Nat. Med. 4: 1313-1317; 1998.
18. Galvin-Parton, P. A. Screening for galc to make neonatal diagnosis and initial neonatal stem cell treatment with umbilical cord blood. Pediatr. Transplant. 7: 83-85; 2003.
19. Gennarelli, T. A.; Graham, D. I. Neuropathology of the head injuries. Semin. Clin. Neuropsychiatry 3: 160-175; 1998.
20. Ha, Y.; Choi, J. U.; Yoon, D. H.; Yeon, D. S.; Lee, J. J.; Kim, H. O.; Cho, Y. E. Neural phenotype expression of cultured human cord blood cells in vitro. Neuroreport 12: 3523-3527; 2001.
21. Hillered, L.; Persson, L. Neurochemical monitoring of the acutely injured human brain. Scan. J. Clin. Lab. Invest. Suppl. 229: 9-18; 1999.
22. Hillered, L.; Valtysson, J.; Enblad, P.; Persson, L. Interstitial glycerol as a marker for membrane phospholipid degradation in the acutely injured human brain. J. Neurol. Neurosurg. Psychiatry 64: 486-491; 1998.
23. Jin, K.; Zhu, Y.; Sun, Y.; Mao, X. O.; Xie, L.; Greenberg, D. A. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. USA. 99: 11946-11950; 2002.
24. Kadhim, H. J.; Duchateau, J.; Sébire, G. Cytokines and brain injury: Invited review. J. Intensive Care Med. 23: 236-249; 2008.
25. Keane, R. W.; Kraydieh, S.; Lotocki, G.; Alonso, O. F.; Aldana, P.; Dietrich, W. D. Apoptotic and antiapoptotic mechanisms after traumatic brain injury. J. Cereb. Blood Flow Metab. 21: 1189-1198; 2001.
26. Keeling, K. L.; Hicks, R. R.; Mahesh, J.; Billings, B. B.; Kotwal, G. J. Local neutrophil influx following lateral fluid-percussion brain injury in rats is associated with accumulation of complement activation fragments of the third component (C3) of the complement system. J. Neuroimmunol. 105: 20-30; 2000.
27. Kim, H. J.; Lee, J. H.; Kim, S. H. 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; 2010.
28. Kuo, J. R.; Lo, C. J.; Chang, C. P.; Lin, H. J.; Lin, M. T.; Chio, C. C. Brain cooling-stimulated angiogenesis and neurogenesis attenuated traumatic brain injury in rats. J. Trauma 69: 1467-1472; 2010.
29. Kuzu, M. A.; Köksoy, C.; Kuzu, I.; Gürhan, I.; Ergün, H.; Demirpence, E. Role of integrins and intracellular adhesion molecule-1 in lung injury after intestinal ischemia-reperfusion. Am. J. Surg. 183: 70-74; 2002.
30. Laurer, H. L.; Lenzlinger, P. M.; McIntosh, T. K. Models of traumatic brain injury. Eur. J. Trauma 3: 95-110; 2000.
31. Leker, R. R.; Shohami, E. Cerebral ischemia and trauma-different etiologies yet similar mechanisms: Neuroprotective opportunities. Brain Res. Brain Res. Rev. 39: 55-73; 2002.
32. Lenzlinger, P. M.; Morganti-Kossmann, M. C.; Laurer, H. L.; McIntosh, T. K. The duality of the inflammatory response to traumatic brain injury. Mol. Neurobiol. 24: 169-181; 2001.
33. Li, Y.; Douglas, S. D.; Ho, W. Human stem cells express substance P gene and its receptor. J. Hemother. Stem Cell Res. 9: 445-452; 2000.
34. Lian, Q.; Zhang, Y.; Zhang, J.; Zhang, H. K.; Wu, X.; Zhang, Y.; Lam, F. F.; Kang, S.; Xia, J. C.; Lai, W. H.; Au, K. W.; Chow, Y. Y.; Siu, C. W.; Lee, C. N.; Tse, H. F. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 121: 1113-1123; 2010.
35. Lindvall, O.; Kokaia, Z.; Martinez-Serrano, A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat. Med. 10: S42-S50; 2004.
36. Liu, W. S.; Chen, C. T.; Foo, N. H.; Huang, H. R.; Wang, J. J.; Chen, S, H.; Chen, T. J. Human umbilical cord blood cells protect against hypothalamic apoptosis and systemic inflammation response during heatstroke in rats. Pediatr. Neonatol. 50: 208-218; 2009.
37. Lu, D.; Mahmood, A.; Wang, L.; Li, Y.; Lu, M.; Chopp, M. Adult bone marrow stromal cells administered intravenously to rats after traumatic brain injury migrate into brain and improve neurological outcome. Neuroreport 12: 559-563; 2001.
38. Lu, D.; Sanberg, P. R.; Mahmood, A.; Li, Y.; Wang, L.; Sanchez-Ramos, J.; Chopp, M. Intravenous administration of human umbilical cord blood reduces neurological deficit in the rat after traumatic brain injury. Cell Transplant. 11: 275-281; 2002.
39. Mahmood, A.; Lu, D.; Chopp, M. Intravenous administration of marrow stromal cells (MSCs) increases the expression of growth factors in rat brain after traumatic brain injury. J. Neurotrauma 21: 33-39; 2004.
40. Mahmood, A.; Lu, D.; Wang, L.; Chopp, M. Intracerebral transplantation of marrow stromal cells cultured with neurotrophic factors promotes functional recovery in adult rats subjected to traumatic brain injury. J. Neurotrauma 19: 1609-1617; 2002.
41. Mahmood, A.; Lu, D.; Wang, L.; Li, Y.; Lu, M.; Chopp, M. Treatment of traumatic brain injury in female rats with intravenous administration of bone marrow stromal cells. Neurosurgery 49: 1196-1203; 2001.
42. McIntosh, T. K.; Noble, L.; Andrews, B.; Faden, A. I. Traumatic brain injury in the rat: Characterization of a midline fluid-percussion model. Cent. Nerv. Syst. Trauma 4: 119-134; 1987.
43. Morganti-Kossmann, M. C.; Rancan, M.; Otto, V. I.; Stahel, P. F.; Kossmann, T. Role of cerebral inflammation after traumatic brain injury: A revisited concept. Shock 16: 165-177; 2001.
44. Morganti-Kossmann, M. C.; Satgunaseelan, L.; Bye, N.; Kossmann, T. Modulation of immune response by head injury. Injury 38: 1392-1400; 2007.
45. Mullane, K. M.; Kraemer, R.; Smith, B. Myeloperoxidase activity as a quantitative assessment of neutrophil infiltration into ischemic myocardium. J. Pharmacol. Methods 14: 157-167; 1985.
46. Murasawa, S.; Asahara, T. Endothelial progenitor cells for vasculogenesis. Physiology 20: 36-42; 2005.
47. Nakatomi, H.; Kuriu, T.; Okabe, S.; Yamamoto, S.; Hatano, O.; Kawahara, N.; Tamura, A.; Kirino, T.; Nakafuku, M. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110: 429-441; 2002.
48. Nortje, J.; Menon, D. K. Traumatic brain injury: Physiology, mechanisms, and outcome. Curr. Opin. Neurol. 17: 711-718; 2004.
49. Olanders, K.; Sun, Z.; Börjesson, A.; Dib, M.; Andersson, E.; Lasson, A.; Ohlsson, T.; Andersson, R. The effect of intestinal ischemia and reperfusion injury on ICAM-1 expression, endothelial barrier function, neutrophil tissue influx, and protease inhibitor levels in rats. Shock 18: 86-92; 2002.
50. Palzur, E.; Vlodavsky, E.; Mulla, H.; Arieli, R.; Feinsod, M.; Soustiel, J. F. Hyperbaric oxygen therapy for reduction of secondary brain damage in head injury: An animal model of brain contusion. J. Neurotrauma 21: 41-48; 2004.
51. Paxinos, G.; Watson, C. The rat brain in stereotaxic coordinates. New York, NY: Academic Press; 1982.
52. Pierce, J. E.; Smith, D. H.; Trojanowski, J. Q.; McIntosh, T. K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 87: 359-369; 1998.
53. Plesnila, N.; von Baumgarten, L.; Retiounskaia, M.; Engel, D.; Ardeshiri, A.; Zimmermann, R.; Hoffmann, F.; Landshamer, S.; Wagner, E.; Culmsee, C. Delayed neuronal death after brain trauma involves p53-dependent inhibition of NF-kappaB transcriptional activity. Cell Death Differ. 14: 1529-1541; 2007.
54. Prockop, D. J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74; 1997.
55. Quiñones-Hinojosa, A.; Sanai, N.; Soriano-Navarro, M.; Gonzalez-Perez, O.; Mirzadeh, Z.; Gil-Perotin, S.; Romero-Rodriguez, R.; Berger, M. S.; Garcia-Verdugo, J. M.; Alvarez-Buylla, A. Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J. Comp. Neurol. 494: 415-434; 2006.
56. Raghupathi, R. Cell death mechanisms following traumatic brain injury. Brain Pathol. 14: 215-222; 2004.
57. Ray, S. K.; Dixon, C. E.; Banik, N. L. Molecular mechanisms in the pathogenesis of traumatic brain injury. Histol. Histopathol. 17: 1137-1152; 2002.
58. Sanai, N.; Tramontin, A. D.; Quiñones-Hinojosa, A.; Barbaro, N. M.; Gupta, N.; Kunwar, S.; Lawton, M. T.; McDermott, M. W.; Parsa, A. T.; Manuel-García Verdugo, J.; Berger, M. S.; Alvarez-Buylla, A. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427: 740-744; 2004.
59. Saporta, S.; Kim, J. J.; Willing, A. E.; Fu, E. S.; Davis, C. D.; Sanberg, P. R. Human umbilical cord blood stem cells infusion in spinal cord injury: Engraftment and beneficial influence on behavior. J. Hematother. Stem Cell Res. 12: 271-278; 2003.
60. Shohami, E.; Novikov, M.; Bass, R. Long-term effect of HU-211, a novel non-competitive NMDA antagonist, on motor and memory functions after closed head injury in the rat. Brain Res. 674: 55-62; 1995.
61. Shyu, W. C.; Lin, S. Z.; Chiang, M. F.; Su, C. Y.; Li, H. Intracerebral peripheral blood stem cell (CD34+) implantation induces neuroplasticity by enhancing beta1 integrinmediated angiogenesis in chronic stroke rats. J. Neurosci. 26: 3444-3453; 2006.
62. Staimirovic, D.; Satoh, K. Inflammatory mediators of cerebral endothelium: A role in ischemic brain inflammation. Brain Pathol. 10: 113-126; 2000.
63. Taguchi, A.; Soma, T.; Tanaka, H.; Kanda, T.; Nishimura, H.; Yoshikawa, H.; Tsukamoto, Y.; Iso, H.; Fujimori, Y.; Stern, D. M.; Naritomi, H.; Matsuyama, T. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 114: 330-338; 2004.
64. Vendrame, M.; Cassady, J.; Newcomb, J.; Butler, T.; Pennypacker, K. R.; Zigova, T.; Sanberg, C. D.; Sanberg, P. R.; Willing, A. E. Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke 35: 2390-2395; 2004.
65. Vlodavsky, E.; Palzur, E.; Soustiel, J. F. Hyperbaric oxygen therapy reduces neuroinflammation and expression of matrix metalloproteinase-9 in the rat model of traumatic brain injury. Neuropathol. Appl. Neurobiol. 32: 40-50; 2006.
66. Walczak, P.; Chen, N.; Hudson, J. E.; Willing, A. E.; Garbuzova-Davis, S. N.; Song, S.; Sanberg, P. R.; Sanchez-Ramos, J.; Bickford, P. C.; Zigova, I. Do hematopoietic cells exposed to a neurogenic environment mimic properties of endogenous neural precursors? J. Neurosci. Res. 76: 244-254; 2004.
67. Wang, Y.; Lin, S. Z.; Chiou, A. L.; Williams, L. R.; Hoffer, B. J. Glial cell line-derived neurotrophic factor protects against ischemia-induced injury in the cerebral cortex. J. Neurosci. 17: 4341-4348; 1997.
68. Willing, A. E.; Vendrame, M.; Mallery, J.; Cassady, C. J.; Davis, C. D.; Sanchez-Ramos, J.; Sanberg, P. R. Mobilized peripheral blood cells administered intravenously produce functional recovery in stroke. Cell Transplant. 12: 449-454; 2003.
69. Wu, J. Y.; Tsou, M. Y.; Chen, T. H.; Chen, S. J.; Tsao, C. M.; Wu, C. C. Therapeutic effects of melatonin on peritonitisinduced septic shock with multiple organ dysfunction syndrome in rats. J. Pineal Res. 45: 106-116; 2008.
70. Wyble, C. W.; Desai, T. R.; Clark, E. T.; Hynes, K. L.; Gewertz, B. L. Physiologic concentrations of TNF alpha and IL-1beta released from reperfused human intestine upregulate E-selectin and ICAM-1. J. Surg. Res. 63: 333-338; 1996.
71. Yakovlev, A. G.; Faden, A. I. Molecular biology of CNS injury. J. Neurotrauma 12: 767-777; 1995.
72. Yunoki, M.; Kawauchi, M.; Ukita, N.; Noguchi, Y.; Nishio, S.; Ono, Y.; Asari, S.; Ohmoto, T.; Asanuma, M.; Ogawa, N. Effects of lecithinized SOD on sequential change in SOD activity after cerebral contusion in rats. Acta Neurochir. Suppl. 71: 142-145; 1998.
73. Zauner, A.; Bullock, R. The role of excitatory amino acids in severe brain trauma: Opportunities for therapy: A review. J. Neurotrauma 12: 547-554; 1995.
74. Zhang, R. L.; Zhang, Z. G.; Zhang, L.; Chopp, M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience 105: 33-41; 2001.