Differentiation of glia-committed NG2 cells: The role of factors released from hippocampus and spinal cord

Acta Neurobiologiae Experimentalis

Volumn 73, Issue 1, 2013, Pages 116-129

  Sypecka, Joanna ^a   Sarnowska, Anna ^a   Gadomska Szabłowska, Ilona ^a   Lukomska, Barbara ^a   Domanska Janik, Krystyna ^a  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

Author keywords

Co culture; Glia; Local microenvironment; Neurogenesis; Ng2 progenitors; OPCs; Organotypic slices; Trophic factors

Indexed keywords

EID: 84878381239     PISSN: 00651400     EISSN: 16890035     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. 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.
2. Allen NJ, Barres BA (2005) Signaling between glia and neurons: Focus on synaptic plasticity. Curr Opin Neurobiol 15: 542-548.
3. Back SA, Riddle A, McClure MM (2007) Maturationdependent vulnerability of perinatal white matter in premature birth. Stroke 38 (2 Suppl): 724-30.
4. Baron W, Shattil SJ, ffrench-Constant C (2002) The oligodendrocyte precursor mitogen PDGF stimulates proliferation by activation of alpha(v)beta3 integrins. EMBO J 2: 1957-1966.
5. Belachew S, Chittajallu R, Aguirre A, Yuan X, Kirby M, Anderson S, Gallo V (2003) Postnatal NG2 proteoglycanexpressing progenitor cells are intrisically multipotent and generate functional neurons. J Cell Biol 161: 169-186.
6. Bhat MA, Rios JC, Lu Y, Garcia-Gresco GP, Ching W, St Martin M, Li J., Einheber S, Cheslerm M, Rosenbluth J, Salzer JL, Bellen HJ (2001) Axon-glia inteaactions and the domain organization of myelinated axons requires neurexin IV/ Caspr/Paranodin. Neuron 30: 369-383.
7. Boscia F, D'Avanzo C, Pannaccione A, Secondo A, Casamassa A, Formisano L, Guida N, Scorziello A, Di Renzo G, Annunziato L (2013) New Roles of NCX in Glial Cells: Activation of Microglia in Ischemia and Differentiation of Oligodendrocytes. Adv Exp Med Biol 961: 307-316.
8. Buser JR, Maire J, Riddle A, Gong X, Nguyen T, Nelson K, Luo NL, Ren J, Struve J, Sherman LS, Miller SP, Chau V, Hendson G, Ballabh P, Grafe MR, Back SA (2012) Arrested oligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 71: 93-109.
9. Buzanska L, Sypecka J, Nerini-Molteni S, Compagnoni A, Hogberg HT, del Torchio R, Domanska-Janik K, Zimmer J, Coecke S (2009) A human stem cell-based model for identifying adverse effects of organic and inorganic chemicals on the developing nervous system. Stem Cells 27: 2591-2601.
10. 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.
11. Cavaliere F, Dinkel K, Reymann K (2005) Microglia response and P2 receptor participation in oxygen/glucose deprivation-induced cortical damage. Neuroscience 136: 615-623.
12. Chari DM, Blakemore WF (2002) Efficient recolonisation of progenitor-depleted areas of the CNS by adult oligodendrocyte progenitor cells. Glia 37: 307-313.
13. Chen BY, Wang X, Wang ZY, Wang YZ, Chen LW, Luo ZJ (2013) Brain-derived neurotrophic factor stimulates proliferation and differentiation of neural stem cells, possibly by triggering the Wnt/β-catenin signaling pathway. J Neurosci Res 91: 30-41
14. 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 23: 5846-5853.
15. Dawson MR, Levine JM, Reynolds R (2000) NG2-expressing cells in the central nervous system: are they oligodendroglial progenitors? J Neurosci Res 61: 471-479.
16. 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.
17. Deng W, Wang H, Rosenberg PA, Volpe JJ, Jensen FE (2004) Role of metabotropic glutamate receptors in oligodendrocyte excitotoxicyty and oxidative stress. Proc Natl Acad Sci U S A 101: 7751-7756.
18. Dewar D, Underhill SM, Goldberg MP (2003) Oligodendrocytes and ischemic brain injury. J Cereb Blood Flow Metab 23: 263-274.
19. French HM, Reid M, Mamontov P, Simmons RA, Grinspan JB (2009) Oxidative stress disrupts oligodendrocyte maturation. J Neurosci Res 1: 3076-3087.
20. Gaughwin PM, Caldwell MA, Anderson JM, Schwienning CJ, Fawcett JW, Compston DA, Chandran S (2006) Astrocytes promote neurogenesis from oligodendrocyte precursor cells. Eur J Neurosci 23: 945-956.
21. Ge WP, Zhou W, Luo Q, Jan LY, Jan YN (2009) Dividing glial cells maintain differentiated properties including complex morphology and functional synapses. Proc Natl Acad Sci U S A 106: 328-333.
22. Göritz C, Thiebaut R, Tessier LH, Nieweg K, Moehle C, Buard I, Dupont JL, Schurgers L, Schmitz G, Pfrieger F (2007) Glia-induced neuronal differentiation by transcriptional regulation. Glia 55: 1108-1122.
23. Grinspan JB, Franceschini B (1995) Platelet-derived growth factor is a survival factor for PSA-NCAM+ oligodendrocyte pre-progenitor cells. J Neurosci Res 41: 540-551.
24. Horner PJ, Thallamir M, Gage FH (2002) Defining the NG2-expressing cell in the adult CNS. J Neurocytol 31: 469-480.
25. Jin Y, Sura K, Fischer I (2012) Differential effects of distinct central nervous system regions on cell migration and axonal extension of neural precursor transplants. J Neurosci Res 90: 2065-2073
26. Ju PJ, Liu R, Yang HJ, Xia YY, Feng ZW (2012) Clonal analysis for elucidating the lineage potential of embryonic NG2+ cells. Cytotherapy 14: 608-620.
27. Karimi-Abdolrezaee S, Eftekharpour E, Wang J, Schut D, Fehlings MG (2010) Synergistic effects of transplanted adult neural stem/progenitor cells, chondroitinase, and growth factors promote functional repair and plasticity of the chronically injured spinal cord. J Neurosci 30: 1657-1676.
28. Kasai M, Jikoh T, Fukumitsu H, Furukawa S (2010) FGF-2- responsive and spinal cord-resident cells improve locomotor function after spinal cord injury. J Neurotrauma 30: 6236-6246.
29. 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.
30. Kerr CL, Letzen BS, Hill CM, Agrawal G, Thakor NV, Sterneckert JL, Gearhart JD, All AH (2010) Efficient differentiation of human embryonic stem cells into oligodendrocyte progenitors for application in a rat contusion model of spinal cord injury. Int J Neurosci 120: 305-313.
31. Kuzhandaivel A, Margaryan G, Nistri A, Mladinic M (2010) Extensive glial apoptosis develops early after hypoxicdysmetabolic insult to the neonatal rat spinal cord in vitro. Neuroscience 169: 325-338.
32. Lee HJ, Wu J, Chung J, Wrathall JR (2013) SOX2 expression is upregulated in adult spinal cord after contusion injury in both oligodendrocyte lineage and ependymal cells. J Neurosci Res 91: 196-210.
33. Lim DA, Alvarez-Buylla A (1999) Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc Natl Acad Sci U S A 96: 7526-7531.
34. Liu H, Shubayev VI (2011) Matrix metalloproteinase-9 controls proliferation of NG2+ progenitor cells immediately after spinal cord injury. Exp Neurol 231: 236-246.
35. 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: 402-408.
36. Lobjois V, Bel-Vialar S, Trousse F, Pituello F (2008) Forcing neural progenitor cells to cycle is insufficient to alter cellfate decision and timing of neuronal differentiation in the spinal cord. Neural Dev 13: 3-4.
37. Lowry OH, Rosenburg NJ, Farr AL, Randall RJ (1951) Protein mesurement with Folin phenol reagent. J Biol Chem193: 265-275.
38. Luyt K, Varadi A, Durant CF, Molnar E (2006) Oligodendroglial metabotropic glutamate receptors are developmentally regulated and involved in the prevention of apoptosis. J Neurochem 99: 641-656.
39. Lytle J, Wrathall J (2007) Glial cell proliferation and replacement in the contused murine spinal cord. Eur J Neurosci 25: 1711-1724.
40. 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: 200-208.
41. 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: 289-301.
42. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85: 890-902.
43. 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.
44. Nakajima H, Uchida K, Yayama T, Kobayashi S, Guerrero AR, Furukawa S, Baba H (2010) Targeted retrograde gene delivery of brain-derived neurotrophic factor suppresses apoptosis of neurons and oligodendroglia after spinal cord injury in rats. Spine 35: 497-504.
45. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M (2002) Regeneration of hippocampal pyramidal neurons sfter ischemic braib injury by recruitment of endogenous neural progenitors. Cell 110: 429-441.
46. Ono K, Kagawa T, Tsumori T, Yokota S, Yasui Y (2001) Morphological changes and cellular dynamics of oligodendrocyte lineage cells in the developing vertebrate central nervous system. Dev Neurosci 23: 346-355.
47. Pozzo Miller LD, Mahanty NK, Connor JA, Landis DM (1994) Spontaneous pyramidal cell death in organotypic slice cultures from rat hippocampus is prevented by glutamate receptor antagonists. Neuroscience 63: 471-487.
48. Raff MC, Miller RH, Noble M (1983) A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium. Nature 303: 390-396.
49. Reynolds R, Dawson M, Papadopoulos D, Polito A, Di Bello IC, Pham-Dinh D, Levine J (2002) The response of NG2- expressing oligodendrocyte progenitorsto demyelination in MOG-EAE-and MS. J Neurocytol 31: 523-536.
50. Rompani SB, Cepko CL (2010) A common progenitor for retinal astrocytes and oligodendrocytes. J Neurosci 30: 4970-4980.
51. Rosenberg SS, Ng BK, Chan JR (2006) The quest for remyelination: a new role for neurotrophins and their receptors. Brain Pathol 16: 288-294.
52. Sellers DL, Horner PJ (2005) Instructive niches: environmental instructions that confound NG2 proteoglycan expression and the fate-restriction of CNS progenitors. J Anat 207: 727-734.
53. Stallcup WB (2002) The NG2 proteoglycan: past insights and future prospects. J Neurocytol 31: 423-435.
54. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37: 173-182.
55. Sypecka J (2003) Different vulnerability to cytotoxicity and succeptibility to protection of progenitors versus mature oligodendrocytes. Pol J Pharmacol 55: 881-885.
56. Sypecka J (2011) Searching for oligodendrocyte precursors for cell replacement therapies. Acta Neurobiol Exp (Wars) 71: 94-102.
57. 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: 661-671.
58. Tamura Y, Katoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H (2007) Multi-directional differentiation of doublecortinand NG2-immunopositive progenitor cells in the adult rat neocortex in vivo. Eur J Neurosci 25: 3489-3498.
59. Trapp BD, Nishiyama A, Cheng D, Macklin W (1997) Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137: 459-468.
60. Trotter J, Schachner M (1989) Cells positive for O4 surface antigen isolated by cell sorting are able to differentiate into astrocytes or oligodendrocytes. Dev Brain Res 46: 115-122.
61. Tuinstra HM, Aviles MO, Shin S, Holland SJ, Zelivyanskaya ML, Fast AG, Ko SY, Margul DJ, Bartels AK, Boehler RM, Cummings BJ, Anderson AJ, Shea LD (2012) Multifunctional, multichannel bridges that deliver neurotrophin encoding lentivirus for regeneration following spinal cord injury. Biomaterials 33: 1618-1626.
62. 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 oligodendroglialderived neurotrophic factors. J Neurosci 30: 6236-6246.
63. Van't Veer A, Du Y, Fischer TZ, Boetig DR, Wood MR, Dreyfus CF (2009) Brain-derived neurotrophic factor effects on oligodendrocyte progenitors of the basal forebrain are mediated through trkB and the MAP kinase pathway. J Neurosci Res 87: 69-78.
64. VonDran MW, Singh H, Honeywell JZ, Dreyfus CF (2011) Levels of BDNF impact oligodendrocyte lineage cells following a cuprizone lesion. J Neurosci 31: 14182-14190.
65. Wang Y, Cheng X, He Q, Zheng Y, Kim DH, Whittemore SR, Cao QL (2011) Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci 31: 6053-6058.
66. 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.
67. Watson RA, Yeung TM (2011) What is the potential of Oligodendrocyte Progenitor Cells to successfully treat human spinal cord injury? BMC Neurol 11: 113.
68. Watzlawik J, Warrington AE, Rodriguez M (2010) Importance of oligodendrocyte protection, BBB breakdown and inflammation for remyelination. Expert Rev Neurother 10: 441-457.
69. Wilkins A, Chandran S, Compston A (2001) A role for oligodendrocyte- derived IGF-1 in trophic support of cortical neurons. Glia 36: 48-57.
70. Wilkins A, Majed H, Layfield R, Compston A, Chandran S (2003) Oligodendrocytes promote neuronal survival and axonal length by distinct intracellular mechanisms: a novel role for oligodendrocyte-derived glial cell line-derived neurotrophic factor. J Neurosci 23: 4967-4974.
71. Wojcik-Stanaszek L, Gregor A, Zalewska T (2011a) Regulation of neurogenesis by extracellular matrix and integrins. Acta Neurobiol Exp (Wars) 71: 103-112.
72. Wójcik-Stanaszek L, Sypecka J, Szymczak P, Ziemka-Nalecz M, Khrestchatisky M, Rivera S, Zalewska T (2011b) The potential role of metalloproteinases in neurogenesis in the gerbil hippocampus following global forebrain ischemia. PLoS One 6: e22465.
73. Yuan X, Eisen AM, McBain CJ, Gallo VA(1998) A role for glutamate and its receptors in the regulation of the oligodendrocyte development in cerebellar tissue slices. Development 125: 2901-2914.
74. Zawadzka M, Rivers LE, Fancy SP, Zhao C, Tripathi R, Jamen F, Young K, Goncharevich A, Pohl H, Rizzi M, Rowitch DH, Kessaris N, Suter U, Richardson WD, Franklin RJ (2010) CNS-resident glial progenitor/stem cells produce Schwann cells as well as oligodendrocytes during repair of CNS demyelination. Cell Stem Cell 6: 578-590.
75. Zhang Y, Denham J, Thies R (2006) Oligodendrocyte progenitor cells derived from human embryonic stem cells express neurptrophic factors. Stem Cells Dev 15: 943-952.
76. Zhang L, Ma Z, Smith GM, Wen X, Pressman Y, Wood PM, Xu XM (2009) GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons. Glia 57: 1178-1191.
77. Zhao YY, Shi XY, Qiu X, Zhang L, Lu W, Yang S, Li C, Cheng GH, Yang ZW, Tang Y (2011) Enriched environment increases the total number of CNPase positive cells in the corpus callosum of middle-aged rats. Acta Neurobiol Exp (Wars) 71: 322-330.
78. Zheng T, Marshall GP 2nd, Laywell ED, Steindler DA (2006) Neurogenic astrocytes transplanted into the adult mouse lateral ventricle contribute to olfactory neurogenesis, and reveal a novel intrinsic subependymal neuron. Neuroscience 29: 175-185.