The neuroprotective effect exerted by oligodendroglial progenitors on ischemically impaired hippocampal cells

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 685-701

  Sypecka, Joanna ^a   Sarnowska, Anna ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

CNS microenvironment; Glia; Neuroprotection; NG2 cells; Oligodendroglial progenitors; Trophic factors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYTOKINE; INTERLEUKIN 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BRAIN ISCHEMIA; CELL DEATH; CELL PROLIFERATION; CELL SURVIVAL; COCULTURE; CONTROLLED STUDY; HIPPOCAMPUS; IMMUNOLOGY; INFLAMMATION; MICROARRAY ANALYSIS; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGODENDROCYTE PROGENITOR CELL; OLIGODENDROGLIA; RAT; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL HYPOXIA; METABOLISM; NEWBORN; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL HYPOXIA; CELLS, CULTURED; COCULTURE TECHNIQUES; HIPPOCAMPUS; OLIGODENDROGLIA; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR; STEM CELLS;

EID: 84896497244     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8549-9     Document Type: Review

References (82)

1. Cao Q, He Q, Wang Y, Cheng X, Howard RM, Zhang Y, DeVries WH, Shields CB, Magnuson DS, Xu XM, Kim DH, Whittemore SR (2010) Transplantation of ciliary neurotrophic factor-expressing adult oligodendrocyte precursor cells promotes remyelination and functional recovery after spinal cord injury. J Neurosci 30:2989-3001
2. Vendrame M, Gemma C, de Mesquita D, Collier L, Bickford PC, Sanberg CD, Sanberg PR, Pennypacker KR,Willing AE (2005)Anti-inflammatory effects of human cord blood cells in a rat model of stroke. Stem Cells Dev 14:595-604 (Pubitemid 41780811)
3. Castejón OJ (2013) Increased vesicular and vacuolar transendothelial transport in traumatic human brain oedema. A review. Folia Neuropathol 51(2):93-102
4. Doetsch F, Caillé I, Lim DA, García-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703-16 (Pubitemid 29278045)
5. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726-33 (Pubitemid 38240970)
6. Suh H, Consiglio A, Ray J, Sawai T, D'Amour KA, Gage FH (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1:515-528 (Pubitemid 350056408)
7. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030-4 (Pubitemid 34193451)
8. Dawson MR, Polito A, Levine JM, Reynolds R (2003) NG2- expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24: 476-488 (Pubitemid 37311310)
9. Geha S, Pallud J, Junier MP, Devaux B, Leonard N, Chassoux F, Chneiweiss H, Daumas-Duport C, Varlet P (2010) NG2+/Olig2+ cells are the major cycle-related cell population of the adult human normal brain. Brain Pathol 20:399-411
10. Simon C, Götz M, Dimou L (2011) Progenitors in the adult cerebral cortex: cell cycle properties and regulation by physiological stimuli and injury. Glia 59:869-81
11. Hughes EG, Kang SH, Fukaya M, Bergles DE (2013) Oligodendrocyte progenitors balance growth with self-repulsion to achieve homeostasis in the adult brain. Nat Neurosci 16(6):668-76
12. Aguirre A, Gallo V (2004) Postnatal neurogenesis and gliogenesis in the olfactory bulb from NG2-expressing progenitors of the subventricular zone. J Neurosci 24:10530-10541 (Pubitemid 39552638)
13. Sypecka J, Sarnowska A, Domanska-Janik K (2009) Crucial role of the local micro-environment in fate decision of neonatal rat NG2 progenitors. Cell Prolif 42:661-71
14. Chari DM, Blakemore WF (2002) Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 37:307-313
15. Magnus T, Carmen J, Deleon J, Xue H, Pardo AC, Lepore AC, Mattson MP, Rao MS, Maragakis NJ (2008) Adult glial precursor poliferation in mutant SOD1G93A mice. Glia 56:2001-2008
16. Nait-Oumesmar B, Decker L, Lachapelle F, Avellana-Adalid V, Bachelin C, Baron-Van Evercooren A (1999) Progenitor cells of the adult mouse subventricular zone proliferate, migrate and differentiate into oligodendrocytes after demyelination. Eur J Neurosci 11:4357-4366 (Pubitemid 30009267)
17. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H (2007) Multi-directional differentiation of doublecortin- and NG2- immunopositive progenitor cells in the adult rat neocortex in vivo. Eur J Neurosci 25:3489-3498 (Pubitemid 47020456)
18. Givogri MI, Galbiati F, Fasano S, Amadio S, Perani L, Superchi D, Morana P, Del Carro U, Marchesini S, Brambilla R, Wrabetz L, Bongarzone E (2006) Oligodendroglial progenitor cell therapy limits central neurological deficit in mice with metachromatic leukodystrophy. J Neurosci 26:3109-3119
19. Keirstead HS, Levine JM, Blakemore WF (1998) Response of the oligodendrocyte progenitor cell population (defined by NG2 labelling) to demyelination of the adult spinal cord. Glia 22:161-170 (Pubitemid 28084388)
20. Watanabe M, Toyama Y, Nishiyama A (2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69:826-836 (Pubitemid 34984700)
21. Xiong M, Chen LX, Ma SM, Yang Y, Zhou WH (2013) Short-term effects of hypothermia on axonal injury, preoligodendrocyte accumulation and oligodendrocyte myelination after hypoxia-ischemia in the hippocampus of immature rat brain. Dev Neurosci 35(1):17-27
22. Dai X, Lercher LD, Clinton PM, Du Y, Livingston DL, Vieira C, Yang L, Shen MM, Dreyfus CF (2003) The trophic role of oligodendrocytes in the basal forebrain. J Neurosci 2:5846-53 (Pubitemid 36807864)
23. Markiewicz I, Sypecka J, Domanska-Janik K, Wyszomirski T, Lukomska B (2011) Cellular environment directs differentiation of human umbilical cord blood-derived neural stem cells in vitro.J. Histochem Cytochem 59(3):289-301
24. Wilkins A, Chandran S, Compston A (2001) A role for oligodendrocyte- derived IGF-1 in trophic support of cortical neurons. Glia 36:48-57
25. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182
26. Sarnowska A, Braun H, Sauerzweig S, Reymann KG (2009) The neuroprotective effect of bone marrow stem cells is not dependent on direct cell contact with hypoxic injured tissue. Exp Neurol 215(2): 317-327
27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-8 (Pubitemid 34164012)
28. Lowry OH, Rosenburg NJ, Farr AL, Randall RJ (1951) Protein mesurement with Folin phenol reagent. J Biol Chem 193:265-275
29. Kim H, Walczak P, Kerr C, Galpoththawela C, Gilad AA, Muja N, Bulte JW (2012) Immunomodulation by transplanted human embryonic stem cell-derived oligodendroglial progenitors in experimental autoimmune encephalomyelitis. Stem Cells 30(12):2820-9. doi:10.1002/stem.1218
30. Sypecka J (2011) Searching for oligodendrocyte precursors for cell replacement therapies. Acta Neurobiol Exp (Wars) 71(1):94-102
31. Walczak P, All AH, Rumpal N, Gorelik M, Kim H, Maybhate A, Agrawal G, Campanelli JT, Gilad AA, Kerr DA, Bulte JW (2011) Human glial-restricted progenitors survive, proliferate, and preserve electrophysiological function in rats with focal inflammatory spinal cord demyelination. Glia 59(3):499-510
32. Gonzalez-Perez O, Alvarez-Buylla A (2011) Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res Rev 67(1-2):147-56
33. Nait-Oumesmar B, Picard-Riera N, Kerninon C, Decker L, Seilhean D, Höglinger GU, Hirsch EC, Reynolds R, Baron-Van Evercooren A (2007) Activation of the subventricular zone in multiple sclerosis: evidence for early glial progenitors. Proc Natl Acad Sci U S A 104(11):4694-9 (Pubitemid 47186287)
34. Vukovic J, Blackmore DG, Jhaveri D, Bartlett PF (2011) Activation of neural precursors in the adult neurogenic niches.Neurochem Int 59:341-6
35. Gójska-Grymajło A, Nyka WM, Zieliński M, Jakubowski Z (2012) CD34/CXCR4 stem cell dynamics in acute stroke patients. Folia Neuropathol 50:140-6
36. Kalluri HS, Gusain A, Dempsey RJ (2013) Regulation of neural progenitor cell proliferation by D609: potential role for ERK. Mol Neurobiol 47(2):782-9
37. Bazan NG (2012) Neuroinflammation and proteostasis are modulated by endogenously biosynthesized neuroprotectin D1. Mol Neurobiol 46(1):221-6
38. Skaper SD, Facci L, Giusti P (2013) Glia and mast cells as targets for palmitoylethanolamide, an anti-inflammatory and neuroprotective lipid mediator. Mol Neurobiol 48(2):340-52
39. Xu L, Zhou S, Feng GY, Zhang LP, ZhaoDM, SunY, Liu Q, Huang F (2012) Neural stem cells enhance nerve regeneration after sciatic nerve injury in rats. Mol Neurobiol 46(2):265-74
40. Sun T, Ma QH (2013) Repairing neural injuries using human umbilical cord blood. Mol Neurobiol 47(3):938-45
41. Hattiangady B, Shetty AK (2012) Neural stem cell grafting counteracts hippocampal injury-mediated impairments in mood, memory, and neurogenesis. Stem Cells Transl Med 1(9):696-708
42. Park HW, Lim MJ, Jung H, Lee SP, Paik KS, Chang MS (2010) Human mesenchymal stem cell-derived Schwann cell-like cells exhibit neurotrophic effects, via distinct growth factor production, in a model of spinal cord injury. Glia 58(9):1118-32
43. Sowa Y, Imura T, Numajiri T, Nishino K, Fushiki S (2012) Adipose-derived stem cells produce factors enhancing peripheral nerve regeneration: influence of age and anatomic site of origin. Stem Cells Dev 21(11):1852-62
44. Whone AL, Kemp K, SunM,Wilkins A, Scolding NJ (2012) Human bone marrow mesenchymal stem cells protect catecholaminergic and serotonergic neuronal perikarya and transporter function from oxidative stress by the secretion of glial-derived neurotrophic factor. Brain Res 1431:86-96
45. Kuroda S (2013) Bone marrow stromal cell transplantation for ischemic stroke - its multi-functional feature. Acta Neurobiol Exp (Wars) 73(1):57-65
46. Růžička J, Romanyuk N, Hejčl A, Vetrík M, Hrubý M, Cocks G, Cihlár J, Přádný M, Price J, Syková E, Jendelová P (2013) Treating spinal cord injury in rats with a combination of human fetal neural stem cells and hydrogels modified with serotonin. Acta Neurobiol Exp (Wars) 73(1):102-15
47. Ghosh Z, Huang M, Hu S, Wilson KD, Dey D, Wu JC (2011) Dissecting the oncogenic and tumorigenic potential of differentiated human induced pluripotent stem cells and human embryonic stem cells. Cancer Res 71:5030-9
48. Yamaoka E, Hiyama E, Sotomaru Y, Onitake Y, Fukuba I, Sudo T, Sueda T, Hiyama K (2011) Neoplastic transformation by TERT in FGF- 2-expanded human mesenchymal stem cells. Int J Oncol 39(1):5-11
49. Zhang Y, Wang D, Chen M, Yang B, Zhang F, Cao K (2011) Intramyocardial transplantation of undifferentiated rat induced pluripotent stem cells causes tumorigenesis in the heart. PLoS One 6(4):e19012
50. Bagayogo IP, Dreyfus CF (2009) Regulated release of BDNF by cortical oligodendrocytes is mediated through metabotropic glutamate receptors and the PLC pathway. ASN Neuro 1(1). doi:10.1042/AN20090006
51. Ubhi K, Rockenstein E, Mante M, Inglis C, Adame A, Patrick C, Whitney K, Masliah E (2010) Neurodegeneration in a transgenic mouse model of multiple system atrophy is associated with altered expression of oligodendroglial-derived neurotrophic factors. J Neurosci 30(18):6236-46
52. Chapleau CA, Pozzo-Miller L (2012) Divergent roles of p75NTR and Trk receptors in BDNF's effects on dendritic spine density and morphology. Neural Plast 2012:578057
53. Choi SH, Li Y, Parada LF, Sisodia SS (2009) Regulation of hippocampal progenitor cell survival, proliferation and dendritic development by BDNF. Mol Neurodegener 4:52
54. Difato F, Tsushima H, Pesce M, Benfenati F, Blau A, Chieregatti E (2011) The formation of actin waves during regeneration after axonal lesion is enhanced by BDNF. Sci Rep 1:183
55. Hofmann SR, Rösen-Wolff A, Tsokos GC, Hedrich CM (2012) Biological properties and regulation of IL-10 related cytokines and their contribution to autoimmune disease and tissue injury. Clin Immunol 143:116-27
56. Legge KL,Min B, Bell JJ, Caprio JC, Li L, Gregg RK, Zaghouani H (2000) Coupling of peripheral tolerance to endogenous interleukin 10 promotes effective modulation of myelin-activated T cells and ameliorates experimental allergic encephalomyelitis. J Exp Med 91(12): 2039-52
57. Milligan ED, Penzkover KR, Soderquist RG, Mahoney MJ (2012) Spinal interleukin-10 therapy to treat peripheral neuropathic pain. Neuromodulation 5(6):520-6. doi:10.1111/j.1525-1403.2012.00462.x
58. Koch N, Jung M, Sabat R, Krätzschmar J, Döcke WD, Asadullah K, Volk HD, Grütz G (2009) IL-10 protects monocytes and macrophages from complement-mediated lysis. J Leukoc Biol 86(1):155-66
59. Zhou Z, Peng X, Insolera R, Fink DJ, Mata M (2009) IL-10 promotes neuronal survival following spinal cord injury. ExpNeurol 220(1):183-90
60. Cristofanilli M, Harris VK, Zigelbaum A, Goossens AM, Lu A, Rosenthal H, Sadiq SA (2011) Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice. Stem Cells Dev 20:2065-76
61. 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(12):3678-91
62. Erceg S, Ronaghi M, Oria M, Roselló MG, Aragó MA, Lopez MG, Radojevic I, Moreno-Manzano V, Rodríguez-Jiménez FJ, Bhattacharya SS, Cordoba J, Stojkovic M (2010) Transplanted oligodendrocytes and motoneuron progenitors generated from human embryonic stem cells promote locomotor recovery after spinal cord transection. Stem Cells 28:1541-9
63. Hatch MN, Schaumburg CS, Lane TE, Keirstead HS (2009) Endogenous remyelination is induced by transplant rejection in a viral model of multiple sclerosis. J Neuroimmunol 212:74-81
64. Mackenzie MA, Jordan SA, Budd PS, Jackson IJ (1997) Activation of the receptor tyrosine kinase Kit is required for the proliferation of melanoblasts in the mouse embryo. Dev Biol 192:99-107 (Pubitemid 28015649)
65. Piao CS, Li B, Zhang LJ, Zhao LR (2012) Stem cell factor and granulocyte colony-stimulating factor promote neuronal lineage commitment of neural stem cells. Differentiation 83(1):17-25
66. Takagi S, Saito Y, Hijikata A, Tanaka S, Watanabe T, Hasegawa T, Mochizuki S, Kunisawa J, Kiyono H, Koseki H, Ohara O, Saito T, Taniguchi S, Shultz LD, Ishikawa F (2012) Membrane-bound human SCF/KL promotes in vivo human hematopoietic engraftment and myeloid differentiation. Blood 119(12):2768-77
67. Erlandsson A, Larsson J, Forsberg-Nilsson K (2004) Stem cell factor is a chemoattractant and a survival factor for CNS stem cells. Exp Cell Res 301:201-10 (Pubitemid 39504973)
68. Gore BB, Wong KG, Tessier-Lavigne M (2008) Stem cell factor functions as an outgrowth-promoting factor to enable axon exit from the midline intermediate target. Neuron 57(4):501-10 (Pubitemid 351273993)
69. Sun L, Lee J, Fine HA (2004) Neuronally expressed stem cell factor induces neural stem cell migration to areas of brain injury. J Clin Invest 113(9):1364-74 (Pubitemid 39069935)
70. Dhandapani KM, Wade FM, Wakade C, Mahesh VB, Brann DW (2005) Neuroprotection by stem cell factor in rat cortical neurons involves AKT and NFkappaB. J Neurochem 95:9-19 (Pubitemid 41384421)
71. Osada T, Watanabe M, Hasuo A, Imai M, Suyama K, Sakai D, Kawada H, Matsumae M, Mochida J (2010) Efficacy of the coadministration of granulocyte colony-stimulating factor and stem cell factor in the activation of intrinsic cells after spinal cord injury in mice. J Neurosurg Spine 13(4):516-23
72. Zhao LR, Berra HH, Duan WM, Singhal S, Mehta J, Apkarian AV, Kessler JA (2007) Beneficial effects of hematopoietic growth factor therapy in chronic ischemic stroke in rats. Stroke 38(10):2804- 11
73. Burns KA, Murphy B, Danzer SC, Kuan CY (2009) Developmental and post-injury cortical gliogenesis: a genetic fate-mapping study with Nestin-CreER mice. Glia 57(10):1115-29
74. Tanaka K, Nogawa S, Suzuki S, Dembo T, Kosakai A (2003) Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in periinfarct area in the rat brain. Brain Res 989:172-179 (Pubitemid 37211420)
75. White BD, Nathe RJ, Maris DO, Nguyen NK, Goodson JM, Moon RT, Horner PJ (2010) Beta-catenin signaling increases in proliferating NG2+ progenitors and astrocytes during post-traumatic gliogenesis in the adult brain. Stem Cells 28(2):297-307
76. Naganska E, Matyja E (2011) Amyotrophic lateral sclerosis - looking for pathogenesis and effective therapy. Folia Neuropathol 49:1-13
77. Falahati S, Breu M, Waickman AT, Phillips AW, Arauz EJ, Snyder S, Porambo M, Goeral K, Comi AM, Wilson MA, Johnston MV, Fatemi A (2013) Ischemia-induced neuroinflammation is associated with disrupted development of oligodendrocyte progenitors in a model of periventricular leukomalacia. Dev Neurosci 35(2-3): 182-96
78. Sypecka J, Sarnowska A, Gadomska-Szabłowska I, Lukomska B, Domańska-Janik K (2013) Differentiation of glia-committed NG2 cells: the role of factors released from hippocampus and spinal cord. Acta Neurobiol Exp (Wars) 73(1):116-29
79. Sypecka J, Sarnowska A (2013) Heterogeneity of local tissue micro-environment influences differentiation of oligodendroglial progenitors. Folia Neuropathol 51(2):103-10
80. Clarke LE, Young KM, Hamilton NB, Li H, Richardson WD, Attwell D (2012) Properties and fate of oligodendrocyte progenitor cells in the corpus callosum, motor cortex, and piriform cortex of the mouse. J Neurosci 32:8173-85
81. Ju P, Zhang S, Yeap Y, Feng Z (2012) Induction of neuronal phenotypes from NG2+ glial progenitors by inhibiting epidermal growth factor receptor in mouse spinal cord injury. Glia 60(11):1801-14
82. Ziemka-Nałȩcz M, Stanaszek L, Zalewska T (2013) Oxygen-glucose deprivation promotes gliogenesis and microglia activation in organotypic hippocampal slice culture: involvement of metalloproteinases. Acta Neurobiol Exp (Wars) 73(1):130-42