Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury

Experimental Neurology

Volumn 261, Issue , 2014, Pages 53-64

  Donega, Vanessa ^a   Nijboer, Cora H ^a   van Tilborg, Geralda ^b   Dijkhuizen, Rick M ^b   Kavelaars, Annemieke ^c   Heijnen, Cobi J ^a,c  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

Microglia polarization; Nasal MSC therapy; Neonatal hypoxia ischemia; Neurogenesis; Neuroregeneration; Scar formation

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; BRAIN DERIVED NEUROTROPHIC FACTOR; DOUBLECORTIN; GLIAL FIBRILLARY ACIDIC PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 2; NERVE GROWTH FACTOR; NESTIN; NEURON SPECIFIC NUCLEAR PROTEIN; NEUROTROPHIC FACTOR; FLUORESCENT DYE; NERVE PROTEIN; ORGANIC COMPOUND; PKH 26;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL MIGRATION; CELL REGENERATION; COCULTURE; CONTROLLED STUDY; GENE EXPRESSION; HIPPOCAMPUS; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTRANASAL DRUG ADMINISTRATION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MICROGLIA; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; POLARIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA ISOLATION; SCAR FORMATION; SOMATOSENSORY CORTEX; STEM CELL NICHE; WESTERN BLOTTING; ANIMAL MODEL; BDNF GENE; CELL POLARITY; FLUORESCENCE MICROSCOPY; GLIOSIS; IN VITRO STUDY; IN VIVO STUDY; NEURAL STEM CELL; NGF GENE; PROTEIN EXPRESSION; ANIMAL; BRAIN INJURIES; C57BL MOUSE; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPLICATION; DIAGNOSTIC USE; GENETICS; GLIA; HEMISPHERIC DOMINANCE; ISCHEMIA; MESENCHYMAL STROMA CELL; METABOLISM; NERVE REGENERATION; PHYSIOLOGY; TIME;

ADMINISTRATION, INTRANASAL; ANIMALS; ANIMALS, NEWBORN; BRAIN INJURIES; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL DIFFERENTIATION; CELL PROLIFERATION; COCULTURE TECHNIQUES; FLUORESCENT DYES; FUNCTIONAL LATERALITY; ISCHEMIA; MESENCHYMAL STROMAL CELLS; MICE; MICE, INBRED C57BL; NERVE GROWTH FACTOR; NERVE REGENERATION; NERVE TISSUE PROTEINS; NEUROGLIA; ORGANIC CHEMICALS; TIME FACTORS;

EID: 84905252459     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.06.009     Document Type: Article

References (37)

1. Anderova M., Vorisek I., Pivonkova H., et al. Cell death/proliferation and alterations in glial morphology contribute to changes in diffusivity in the rat hippocampus after hypoxia-ischemia. J. Cereb. Blood Flow Metab. 2011, 31:894-907.
2. Bacigaluppi M., Pluchino S., Jametti L.P., et al. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 2009, 132:2239-2251.
3. Chor V., Charpentier T.L., Lebon S., et al. Characterization of phenotype markers and neuronotoxic potential of polarized primary microglia in vitro. Brain Behav. Immun. 2013, 32:70-85.
4. Crigler L., Robey R.C., Asawachaicharn A., et al. Human mesenchymal stem cell subpopulations express a variety of neuro-regulatory molecules and promote neuronal cell survival and neuritogenesis. Exp. Neurol. 2006, 198:54-64.
5. Czeh M., Gressens P., Kaindl A.M. The Yin and Yang of microglia. Dev. Neurosci. 2011, 33:199-209.
6. Daadi M.M., Davis A.S., Arac A., et al. Human neural stem cells grafts modify microglial response and enhance axonal sprouting in neonatal hypoxic-ischemic brain injury. Stroke 2010, 41:516-523.
7. De Haan M., Wyatt J.S., Roth S., et al. Brain and cognitive-behavioural development after asphyxia at term birth. Dev. Sci. 2006, 9:350-358.
8. Donega V., van Velthoven C.T., Nijboer C.H., et al. Intranasal mesenchymal stem cell treatment for neonatal brain damage: long-term cognitive and sensorimotor improvement. PLoS One 2013, 8:e51253.
9. Donega V., Velthoven C., Nijboer C.H., et al. The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment. J. Cereb. Blood Flow Metab. 2013, 33:625-634.
10. Fagel D.M., Ganat Y., Silbereis J., et al. Cortical neurogenesis enhanced by chronic perinatal hypoxia. Exp. Neurol. 2006, 199:77-91.
11. Felling R.J., Snyder M.J., Romanko M.J., et al. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia-ischemia. J. Neurosci. 2006, 26:4359-4369.
12. Ferriero D.M. Neonatal brain injury. N. Engl. J. Med. 2004, 351:1985-1995.
13. Garcia D.R., Doan N.B., Imura T., et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat. Neurosci. 2004, 7:1233-1241.
14. Graham E.M., Ruis K.A., Hartman A.L., et al. A systematic review of the role of intrapartum hypoxia-ischemia in the causation of neonatal encephalopathy. Am. J. Obstet. Gynecol. 2008, 199:587-595.
15. Inta D., Alfonso J., von Engelhardt, et al. Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from postnatal subventricular zone. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20994-20999.
16. Kadam S.D., Mulholland J.D., McDonald J.W., et al. Neurogenesis and neuronal commitment following ischemia in a new mouse model for neonatal stroke. Brain Res. 2008, 1208:35-45.
17. Kempermann G., Jessberger S., Steiner B., et al. Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 2004, 27:447-452.
18. Kokaia Z., Martino G., Schwartz M., et al. Cross-talk between neural stem cells and immune cells: the key to better brain repair?. Nat. Rev. Neurosci. 2012, 15:1078-1087.
19. Lee J.A., Kim B.I., Jo C.H., et al. Mesenchymal stem cell transplantation for hypoxic-ischemic brain injury in a neonatal rat model. Pediatr. Res. 2010, 67:42-46.
20. Murase S.I., Horwitz A.F. Deleted in colorectal carcinoma and differentially expressed integrins mediate the directional migration of neural precursors in the rostral migratory stream. J. Neurosci. 2002, 22:3568-3579.
21. Neumann J., Gunzer M., Gutzeit H.O., et al. Microglia provide neuroprotection after ischemia. FASEB J. 2006, 20:714-720.
22. Pimentel-Coelho P.M., Magalhaes E.S., Lopes L.M., et al. 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. 2010, 19:351-358.
23. Rusnakova V., Honsa P., Dzamba D., et al. Heterogeneity of astrocytes: from development to injury-single cell gene expression. PLoS One 2013, 8:e69734.
24. Salem H.K., Thiemermann C. Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 2010, 28:585-596.
25. Sofroniew M.V. Multiple roles for astrocytes as effectors of cytokines and inflammatory mediators. Neuroscientist 2013, 20:160-172.
26. Titomanlio L., Kavelaars A., Dalous J., et al. Stem cell therapy for neonatal brain injury: perspectives and challenges. Ann. Neurol. 2011, 70:698-712.
27. Tse W.T., Pendlenton J.D., Beyer W.M., et al. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003, 75:389-397.
28. Van Handel M., Swaab H., de Vries L.S., et al. Long-term cognitive and behavioural consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur. J. Pediatr. 2007, 166:645-654.
29. van Velthoven C.T., Kavelaars A., van Bel F., et al. 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. J. Neurosci. 2010, 30:9603-9611.
30. van Velthoven C.T., Kavelaars A., van Bel F., et al. Mesenchymal stem cell transplantation changes the gene expression profile of the neonatal ischemic brain. Brain Behav. Immun. 2011, 25:1342-1350.
31. van Velthoven C.T., Braccioli L., Willemen H.L., et al. Therapeutic potential of geneticaly modified mesenchymal stem cells after neonatal hypoxic-ischemic brain damage. Mol. Ther. 2013, 22:645-654.
32. Volpe J.J. Perinatal brain injury: from pathogenesis to neuroprotection. Ment. Retard. Dev. Disabil. Res. Rev. 2001, 7:56-64.
33. Wake H., Moorhouse A.J., Miyamoto A., et al. Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci. 2013, 36:209-217.
34. Yasahura 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. 2008, 28:1804-1810.
35. Yuan T.F. BDNF signaling during olfactory bulb neurogenesis. J. Neurosci. 2008, 28:5139-5140.
36. Zhang R., Liu Y., Yan K., et al. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J. Neuroinflammation 2013, 10:106-118.
37. Zhao C., Deng W., Gage F.H. Mechanisms and functional implications of adult neurogenesis. Cell 2008, 132:645-660.