Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function

Journal of Neuroscience

Volumn 30, Issue 28, 2010, Pages 9603-9611

  Van Velthoven, Cindy T J ^a   Kavelaars, Annemieke ^a,b   Van Bel, Frank ^a   Heijnen, Cobi J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN EXTRACT; MICROTUBULE ASSOCIATED PROTEIN 2; MYELIN BASIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN ISCHEMIA; CELL DIFFERENTIATION; CELL GROWTH; CELL MATURATION; CELL SURVIVAL; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NERVE CELL; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PYRAMIDAL TRACT; SENSORIMOTOR FUNCTION; SPINAL CORD; STAINING;

ANALYSIS OF VARIANCE; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; HYPOXIA-ISCHEMIA, BRAIN; MESENCHYMAL STEM CELL TRANSPLANTATION; MICE; MOTOR SKILLS; NEURONS; OLIGODENDROGLIA; PYRAMIDAL TRACTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ROTAROD PERFORMANCE TEST;

EID: 77954736319     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1835-10.2010     Document Type: Article

References (50)

1. Allan SM, Tyrrell PJ, Rothwell NJ (2005) Interleukin-1 and neuronal injury. Nat Rev Immunol 5:629-640.
2. Carlson NG, Wieggel WA, Chen J, Bacchi A, Rogers SW, Gahring LC (1999) Inflammatory cytokines IL-1 alpha, IL-1 beta, IL-6, and TNF-alpha impart neuroprotection to an excitotoxin through distinct pathways. J Immunol 163:3963-3968. (Pubitemid 29450925)
3. Carmichael ST (2006) Cellular and molecular mechanisms of neural repair after stroke: making waves. Ann Neurol 59:735-742.
4. Chang YS, Mu D, Wendland M, Sheldon RA, Vexler ZS, McQuillen PS, Ferriero DM (2005) Erythropoietin improves functional and histological outcome in neonatal stroke. Pediatr Res 58:106-111. (Pubitemid 40967438)
5. Chehrehasa F, Meedeniya AC, Dwyer P, Abrahamsen G, Mackay-Sim A (2009) EdU, a new thymidine analogue for labelling proliferating cells in the nervous system. J Neurosci Methods 177:122-130.
6. Chen J, Li Y, Katakowski M, Chen X, Wang L, Lu D, Lu M, Gautam SC, Chopp M (2003) Intravenous bone marrow stromal cell therapy reduces apoptosis and promotes endogenous cell proliferation after stroke in female rat. J Neurosci Res 73:778-786. (Pubitemid 37071731)
7. Daadi MM, Davis AS, Arac A, Li Z, Maag AL, Bhatnagar R, Jiang K, Sun G, Wu JC, Steinberg GK (2010) Human neural stem cell grafts modify microglial response and enhance axonal sprouting in neonatal hypoxicischemic brain injury. Stroke 41:516-523.
8. Deng J, Petersen BE, Steindler DA, Jorgensen ML, Laywell ED (2006) Mesenchymal stem cells spontaneously express neural proteins in culture and are neurogenic after transplantation. Stem Cells 24:1054-1064. (Pubitemid 44464738)
9. Ferriero DM (2004) Neonatal brain injury. N Engl J Med 351:1985-1995.
10. Frielingsdorf H, Simpson DR, Thal LJ, Pizzo DP (2007) Nerve growth factor promotes survival of new neurons in the adult hippocampus. Neurobiol Dis 26:47-55. (Pubitemid 46442788)
11. Fromm C, Evarts EV (1982) Pyramidal tract neurons in somatosensory cortex: central and peripheral inputs during voluntary movement. Brain Res 238:186-191. (Pubitemid 12158447)
12. Hama T, Kushima Y, Miyamoto M, Kubota M, Takei N, Hatanaka H (1991) Interleukin-6 improves the survival of mesencephalic catecholaminergic and septal cholinergic neurons from postnatal, two-week-old rats in cultures. Neuroscience 40:445-452.
13. Hsu JY, Stein SA, Xu XM (2006) Development of the corticospinal tract in the mouse spinal cord: a quantitative ultrastructural analysis. Brain Res 1084:16-27.
14. Iwaniuk AN, Whishaw IQ (2000) On the origin of skilled forelimb movements. Trends Neurosci 23:372-376.
15. Koike N, Kassai Y, Kouta Y, Miwa H, Konishi M, Itoh N (2007) Brorin, a novel secreted bone morphogenetic protein antagonist, promotes neurogenesis in mouse neural precursor cells. J Biol Chem 282:15843-15850. (Pubitemid 47093316)
16. Lapash Daniels CM, Ayers KL, Finley AM, Culver JP, Goldberg MP (2009) Axon sprouting in adult mouse spinal cord after motor cortex stroke. Neurosci Lett 450:191-195.
17. Leclerc N, Beesley PW, Brown I, Colonnier M, Gurd JW, Paladino T, Hawkes R (1989) Synaptophysin expression during synaptogenesis in the rat cerebellar cortex. J Comp Neurol 280:197-212. (Pubitemid 19042132)
18. Lee JA, Kim BI, Jo CH, Choi CW, Kim EK, Kim HS, Yoon KS, Choi JH (2010) Mesenchymal stem cell transplantation for hypoxic-ischemic brain injury in neonatal rat model. Pediatr Res 67:42-46.
19. Li Y, Chen J, Chen XG, Wang L, Gautam SC, Xu YX, Katakowski M, Zhang LJ, Lu M, Janakiraman N, Chopp M (2002) Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery. Neurology 59:514-523.
20. Li Y, Chen J, Zhang CL, Wang L, Lu D, Katakowski M, Gao Q, Shen LH, Zhang J, Lu M, Chopp M (2005) Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 49:407-417. (Pubitemid 40222918)
21. Liu Z, Zhang RL, Li Y, Cui Y, Chopp M (2009) Remodeling of the corticospinal innervation and spontaneous behavioral recovery after ischemic stroke in adult mice. Stroke 40:2546-2551.
22. Loddick SA, Turnbull AV, Rothwell NJ (1998) Cerebral interleukin-6 is neuroprotective during permanent focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 18:176-179. (Pubitemid 28082514)
23. Ma M, Ma Y, Yi X, Guo R, Zhu W, Fan X, Xu G, Frey WH 2nd, Liu X (2008) Intranasal delivery of transforming growth factor-beta1 in mice after stroke reduces infarct volume and increases neurogenesis in the subventricular zone. BMC Neurosci 9:117.
24. Mason JL, Suzuki K, Chaplin DD, Matsushima GK (2001) Interleukin-1beta promotes repair of the CNS. J Neurosci 21:7046-7052.
25. Meier C, Middelanis J, Wasielewski B, Neuhoff S, Roth-Haerer A, Gantert M, Dinse HR, Dermietzel R, Jensen A (2006) Spastic paresis after perinatal brain damage in rats is reduced by human cord blood mononuclear cells. Pediatr Res 59:244-249.
26. Meiri KF, Saffell JL, Walsh FS, Doherty P (1998) Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci 18:10429-10437.
27. Mezey E, Chandross KJ, Harta G, Maki RA, McKercher SR (2000) Turning blood into brain: cells bearing neuronal antigens generated in vivo from bone marrow. Science 290:1779-1782. (Pubitemid 32004811)
28. Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T (2001) BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci U S A 98:5868-5873.
29. Nijboer CH, Kavelaars A, Vroon A, Groenendaal F, van Bel F, Heijnen CJ (2008) Low endogenous G-protein-coupled receptor kinase 2 sensitizes the immature brain to hypoxia-ischemia-induced gray and white matter damage. J Neurosci 28:3324-3332. (Pubitemid 351469332)
30. Ohtaki H, Ylostalo JH, Foraker JE, Robinson AP, Reger RL, Shioda S, Prockop DJ (2008) Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci U S A 105:14638-14643.
31. Pimentel-Coelho PM, Mendez-Otero R (2010) Cell therapy for neonatal hypoxic-ischemic encephalopathy. Stem Cells Dev 19:299-310.
32. Pimentel-Coelho PM, Magalhães ES, Lopes LM, deAzevedo LC, Santiago MF, Mendez-Otero R (2010) Human cord blood transplantation in a neonatal rat model of hypoxic-ischemic brain damage: functional outcome related to neuroprotection in the striatum. Stem Cells Dev 19:351-358.
33. Qu R, Li Y, Gao Q, Shen L, Zhang J, Liu Z, Chen X, Chopp M (2007) Neurotrophic and growth factor gene expression profiling of mouse bone marrow stromal cells induced by ischemic brain extracts. Neuropathology 27:355-363. (Pubitemid 47063283)
34. Relton JK, Rothwell NJ (1992) Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res Bull 29:243-246.
35. Schneider A, Krüger C, Steigleder T, Weber D, Pitzer C, Laage R, Aronowski J, Maurer MH, Gassler N, Mier W, Hasselblatt M, Kollmar R, Schwab S, Sommer C, Bach A, Kuhn HG, Schäbitz WR (2005) The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest 115:2083-2098.
36. Shen LH, Li Y, Chen J, Cui Y, Zhang C, Kapke A, Lu M, Savant-Bhonsale S, Chopp M (2007) One-year follow-up after bone marrow stromal cell treatment in middle-aged female rats with stroke. Stroke 38:2150-2156. (Pubitemid 47012282)
37. Shyu WC, Lin SZ, Yang HI, Tzeng YS, Pang CY, Yen PS, Li H (2004) Functional recovery of stroke rats induced by granulocyte colony-stimulating factor-stimulated stem cells. Circulation 110:1847-1854.
38. Temporin K, Tanaka H, Kuroda Y, Okada K, Yachi K, Moritomo H, Murase T, Yoshikawa H (2008) IL-1beta promotes neurite outgrowth by deactivating RhoA via p38 MAPK pathway. Biochem Biophys Res Commun 365:375-380. (Pubitemid 350137300)
39. Toulmond S, Vige X, Fage D, Benavides J (1992) Local infusion of interleukin-6 attenuates the neurotoxic effects of NMDA on rat striatal cholinergic neurons. Neurosci Lett 144:49-52.
40. van der Kooij MA, Ohl F, Arndt SS, Kavelaars A, van Bel F, Heijnen CJ (2010) Mild neonatal hypoxia-ischemia induces long-term motor- and cognitive impairments in mice. Brain Behav Immun 24:850-856.
41. van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2009) Regeneration of the ischemic brain by engineered stem cells: fuelling endogenous repair processes. Brain Res Rev 61:1-13.
42. van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2010) 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.
43. Volpe JJ (2001) Neurology of the newborn. Philadelphia: Saunders.
44. Weidner N, Ner A, Salimi N, Tuszynski MH (2001) Spontaneous corticospinal axonal plasticity and functional recovery after adult central nervous system injury. Proc Natl Acad Sci U S A 98:3513-3518. (Pubitemid 32220876)
45. Yang J, Jiang Z, Fitzgerald DC, Ma C, Yu S, Li H, Zhao Z, Li Y, Ciric B, Curtis M, Rostami A, Zhang GX (2009) Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. J Clin Invest 119:3678-3691.
46. Yasuhara T, Matsukawa N, Yu G, Xu L, Mays RW, Kovach J, Deans RJ, Hess DC, Carroll JE, Borlongan CV (2006) Behavioral and histological characterization of intrahippocampal grafts of human bone marrow-derived multipotent progenitor cells in neonatal rats with hypoxic-ischemic injury. Cell Transplant 15:231-238.
47. Yasuhara T, Hara K, Maki M, Mays RW, Deans RJ, Hess DC, Carroll JE, Borlongan CV (2008) Intravenous grafts recapitulate the neurorestoration afforded by intracerebrally delivered multipotent adult progenitor cells in neonatal hypoxic-ischemic rats. J Cereb Blood Flow Metab 28:1804-1810.
48. Zhang C, Li Y, Chen J, Gao Q, Zacharek A, Kapke A, Chopp M (2006) Bone marrow stromal cells upregulate expression of bone morphogenetic proteins 2 and 4, gap junction protein connexin-43 and synaptophysin after stroke in rats. Neuroscience 141:687-695. (Pubitemid 44066656)
49. Zhang ZG, Chopp M (2009) Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic. Lancet Neurol 8:491-500.
50. Zhang ZH, Wang RZ, Wang RZ, Li GL, Wei JJ, Li ZJ, Feng M, Kang J, Du WC, Ma WB, Li YN, Yang Y, Kong YG (2008) Transplantation of neural stem cells modified by human neurotrophin-3 promotes functional recovery after transient focal cerebral ischemia in rats. Neurosci Lett 444:227-230.