Comparison of dynamic behavior and maturation of neural multipotent cells derived from different spinal cord developmental stages: an in vitro study

• Autorzy: Slovinska L. , Szekiova E. , Blasko J. , Devaux S. , Salzet M. , Cizkova D.
• Języki publikacji: EN

Abstrakty

EN

Neural progenitor cells (NPCs) are characterized as undifferentiated cells with the ability of self-renewal and multipotency to give rise to other cells of the nervous system. In our in vitro study we demonstrate the proliferative and differentiative potential of NPCs isolated from the spinal cord at different developmental stages (embryonal, early postnatal, adult), maintained and expanded within neurospheres (NSs). Using the NSs culture system, we examined the size, number of NSs and their fate when exposed to differentiation conditions. Based on immunocytochemical analyses for cell markers (MAP 2, GFAP, RIP) we evaluated the occurrence of various cell types: neurons, astrocytes and oligodendrocytes. The results show that NSs increased in size during cultivation time via NPC proliferation, but proliferation potential decreased during maturation stages. In addition, NPCs derived from spinal cord developmentally different stages gave rise to a consistent ratio of glial and neuronal progeny (3:1), and adult tissues represent a comparable source of NPCs compared to embryonal and early postnatal tissues. These data provide useful information for large-scale in vitro expansion of NPCs required for potential cell therapy after spinal cord injury.

Słowa kluczowe

EN

dynamic behaviour; maturation; neural progenitor cell; spinal cord; development stage; in vitro cultivation

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2015
• Tom: 75
• Numer: 1
• Opis fizyczny: p.107-114,fig.,ref.

Twórcy

autor

Slovinska L.

• Institute of Neurobiology, Slovak Academy of Sciences, Kosice, Slovak Republic

autor

Szekiova E.

• Institute of Neurobiology, Slovak Academy of Sciences, Kosice, Slovak Republic

autor

Blasko J.

• Institute of Neurobiology, Slovak Academy of Sciences, Kosice, Slovak Republic

autor

Devaux S.

• Institute of Neurobiology, Slovak Academy of Sciences, Kosice, Slovak Republic

autor

Salzet M.

• U-1192 INSERM, Laboratoire PRISM (Proteomique, Reponse Inflammatoire, Spirometrie de masse), Universite Lille, Villeneuve d’Ascq, France

autor

Cizkova D.

• Institute of Neurobiology, Slovak Academy of Sciences, Kosice, Slovak Republic
• U-1192 INSERM, Laboratoire PRISM (Proteomique, Reponse Inflammatoire, Spirometrie de masse), Universite Lille, Villeneuve d’Ascq, France

Bibliografia

• Alam S, Sen A, Behie LA, Kallos MS (2004) Cell cycle kinetics of expanding populations of neural stem and pro­genitor cells in vitro. Biotechnol Bioeng 88: 332-347.
• Alvarez-Buylla A, Garcia-Verdugo JM, Tramontin AD (2001) A unified hypothesis on the lineage of neural stem cells. Nat Rev Neurosci 2: 287-293.
• Arvidsson L, Fagerlund M, Jaff N, Ossoinak A, Jansson K, Hagerstrand A, Johansson CB, Brundin L, Svensson M (2011) Distribution and characterization of progenitor cells within the human filum terminale. PLoS One 6: e27393.
• Boros C, Lukacsi E, Horvath-Oszwald E, Rethelyi M (2008) Neurochemical architecture of the filum terminale in the rat. Brain Res 1209: 105-114.
• Cameron HA, Hazel TG, McKay RD (1998) Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 36: 287-306.
• Chiasson BJ, Tropepe V, Morshead CM, van der Kooy D (1999) Adult mammalian forebrain ependymal and sub- ependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell character­istics. J Neurosci 19: 4462-4471.
• Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D (1996) In vivo growth factor expan­sion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 16: 2649-2658.
• Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez- Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
• Foroni C, Galli R, Cipelletti B, Caumo A, Alberti S, Fiocco R, Vescovi A (2007) Resilience to transformation and inherent genetic and functional stability of adult neural stem cells ex vivo. Cancer Res 67: 3725-3733.
• Gage FH (2000) Mammalian neural stem cells. Science 287: 1433-1438.
• Gage FH, Ray J, Fisher LJ (1995) Isolation, characteriza­tion, and use of stem cells from the CNS. Annu Rev Neurosci 18: 159-192.
• Garces-Ambrossi GL, McGirt MJ, Samuels R, Sciubba DM, Bydon A, Gokaslan ZL, Jallo GI (2009) Neurological outcome after surgical management of adult tethered cord syndrome. J Neurosurg Spine 11: 304-309.
• Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL (1996) Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16: 1091­1100.
• Gritti A, Frolichsthal-Schoeller P, Galli R, Parati EA, Cova L, Pagano SF, Bjornson CR, Vescovi AL (1999) Epidermal and fibroblast growth factors behave as mitogenic regula­tors for a single multipotent stem cell-like population from the subventricular region of the adult mouse fore- brain. J Neurosci 19: 3287-3297.
• Hitoshi S, Tropepe V, Ekker M, van der Kooy D (2002) Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the develop­ing brain. Development 129: 233-244.
• Horner PJ, Power AE, Kempermann G, Kuhn HG, Palmer TD, Winkler J, Thal LJ, Gage FH (2000) Proliferation and differentiation of progenitor cells throughout the intact adult rat spinal cord. J Neurosci 20: 2218-2228.
• Hung CH, Young TH (2006) Differences in the effect on neural stem cells of fetal bovine serum in substrate-coated and soluble form. Biomaterials 27: 5901-5908.
• Jensen JB, Parmar M (2006) Strengths and limitations of the neurosphere culture system. Mol Neurobiol 34: 153­161.
• Jha RM, Chrenek R, Magnotti LM, Cardozo DL (2013) The isolation, differentiation, and survival in vivo of multipo­tent cells from the postnatal rat filum terminale. PLoS One 8: e65974.
• Kim M, Morshead CM (2003) Distinct populations of fore- brain neural stem and progenitor cells can be isolated using side-population analysis. J Neurosci 23: 10703­10709.
• Kulbatski I, Mothe AJ, Keating A, Hakamata Y, Kobayashi E, Tator CH (2007) Oligodendrocytes and radial glia derived from adult rat spinal cord progenitors: morpho­logical and immunocytochemical characterization. J Histochem Cytochem 55: 209-222.
• Lois C, Alvarez-Buylla A (1993) Proliferating subventricu­lar zone cells in the adult mammalian forebrain can dif­ferentiate into neurons and glia. Proc Natl Acad Sci U S A 90: 2074-2077.
• Louis SA, Rietze RL, Deleyrolle L, Wagey RE, Thomas TE, Eaves AC, Reynolds BA (2008) Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells 26: 988-996.
• Lu Z, Kipnis J (2010) Thrombospondin 1-a key astrocyte- derived neurogenic factor. FASEB J 24: 1925-1934.
• Martens DJ, Seaberg RM, van der Kooy D (2002) In vivo infusions of exogenous growth factors into the fourth ventricle of the adult mouse brain increase the prolifera­tion of neural progenitors around the fourth ventricle and the central canal of the spinal cord. Eur J Neurosci 16: 1045-1057.
• Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS (1997) Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19: 773­785.
• Meletis K, Barnabe-Heider F, Carlen M, Evergren E, Tomilin N, Shupliakov O, Frisen J (2008) Spinal cord injury reveals multilineage differentiation of ependymal cells. PLoS Biol 6: e182.
• Milosevic J, Storch A, Schwarz J (2005) Cryopreservation does not affect proliferation and multipotency of murine neural precursor cells. Stem Cells 23: 681-688.
• Moe MC, Varghese M, Danilov AI, Westerlund U, Ramm- Pettersen J, Brundin L, Svensson M, Berg-Johnsen J, Langmoen IA (2005) Multipotent progenitor cells from the adult human brain: neurophysiological differentiation to mature neurons. Brain 128: 2189-2199.
• Mothe AJ, Kulbatski I, Parr A, Mohareb M, Tator CH (2008) Adult spinal cord stem/progenitor cells transplanted as neurospheres preferentially differentiate into oligoden- drocytes in the adult rat spinal cord. Cell Transplant 17: 735-751.
• Mothe AJ, Zahir T, Santaguida C, Cook D, Tator CH (2011) Neural stem/progenitor cells from the adult human spinal cord are multipotent and self-renewing and differentiate after transplantation. PLoS One 6: e27079.
• Nandoe Tewarie RS, Hurtado A, Bartels RH, Grotenhuis A, Oudega M (2009) Stem cell-based therapies for spinal cord injury. J Spinal Cord Med 32: 105-114.
• Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS (2005) Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 49: 385-396.
• Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G, 2nd, Jiang L, Kang J, Nedergaard M, Goldman SA (2003) Identification and isolation of mul­tipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9: 439-447.
• Nussbaum J, Minami E, Laflamme MA, Virag JA, Ware CB, Masino A, Muskheli V, Pabon L, Reinecke H, Murry CE (2007) Transplantation of undifferentiated murine embry­onic stem cells in the heart: teratoma formation and immune response. Faseb J 21: 1345-1357.
• Okano H, Sawamoto K (2008) Neural stem cells: involve­ment in adult neurogenesis and CNS repair. Philos Trans R Soc Lond B Biol Sci 363: 2111-2122.
• Palmer TD, Takahashi J, Gage FH (1997) The adult rat hip­pocampus contains primordial neural stem cells. Mol Cell Neurosci 8: 389-404.
• Parr AM, Kulbatski I, Zahir T, Wang X, Yue C, Keating A, Tator CH (2008) Transplanted adult spinal cord-derived neural stem/progenitor cells promote early functional recovery after rat spinal cord injury. Neuroscience 155: 760-770.
• Rethelyi M, Lukacsi E, Boros C (2004) The caudal end of the rat spinal cord: transformation to and ultrastructure of the filum terminale. Brain Res 1028: 133-139.
• Rethelyi M, Horvath-Oszwald E, Boros C (2008) Caudal end of the rat spinal dorsal horn. Neurosci Lett 445: 153-157.
• Reynolds BA, Rietze RL (2005) Neural stem cells and neu- rospheres--re-evaluating the relationship. Nat Methods 2: 333-336.
• Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell pro­duces neurons and astrocytes. J Neurosci 12: 4565­4574.
• Shihabuddin LS, Ray J, Gage FH (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spi­nal cord. Exp Neurol 148: 577-586.
• Skup M, Ziemlinska E, Gajewska-Wozniak O, Platek R, Maciejewska A, Czarkowska-Bauch J (2014) The impact of training and neurotrophins on functional recovery after complete spinal cord transection: cel­lular and molecular mechanisms contributing to motor improvement. Acta Neurobiol Exp (Wars)74: 121­141.
• Sulla I, Balik V, Sarissky M (2010) A preliminary report on time dependent changes of some immunophenotypic characteristics of adult rat bone marrow derived stem/ progenitor cells. Folia Veterinaria 54: 191-195.
• Sypecka J, Sarnowska A, Gadomska-Szablowska I, Lukomska B, Domanska-Janik K (2013) Differentiation of glia-committed NG2 cells: The role of factors released from hippocampus and spinal cord. Acta Neurobiol Exp (Wars) 73: 116-129.
• Temple S, Alvarez-Buylla A (1999) Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9: 135-141.
• Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D (2001) Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30: 65-78.
• Varghese M, Olstorn H, Berg-Johnsen J, Moe MC, Murrell W, Langmoen IA (2009) Isolation of human multipotent neural progenitors from adult filum terminale. Stem Cells Dev 18: 603-613.
• Varghese M, Olstorn H, Murrell W, Langmoen IA (2010) Exploring atypical locations of mammalian neural stem cells: the human filum terminale. Arch Ital Biol 148: 85-94.
• Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, Peterson AC, Reynolds BA (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricu­lar neuroaxis. J Neurosci 16: 7599-609.
• Yamada S, Knerium DS, Mandybur GM, Schultz RL, Yamada BS (2004) Pathophysiology of tethered cord syndrome and other complex factors. Neurol Res 26: 722-726.
• Yamamoto S, Yamamoto N, Kitamura T, Nakamura K, Nakafuku M (2001) Proliferation of parenchymal neural progenitors in response to injury in the adult rat spinal cord. Exp Neurol 172: 115-127.