Early phenotypic asymmetry of sister oligodendrocyte progenitor cells after mitosis and its modulation by aging and extrinsic factors

GLIA

Volumn 63, Issue 2, 2015, Pages 271-286

  Boda, Enrica ^a   Di Maria, Silvia ^a   Rosa, Patrizia ^b   Taylor, Verdon ^c   Abbracchio, Maria P ^b   Buffo, Annalisa ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Asymmetry; Division; Maturation; NG2 cells

Indexed keywords

BROXURIDINE; INTRINSIC FACTOR; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR NKX2.2; TRANSCRIPTION FACTOR SOX2; ANTIGEN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CHONDROITIN SULFATE PROTEOGLYCAN 4; HES5 PROTEIN, MOUSE; NERVE PROTEIN; PHOTOPROTEIN; PROTEOGLYCAN; REPRESSOR PROTEIN;

ADULT; AGING; ANAPHASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASYMMETRIC CELL DIVISION; BRAIN CORTEX; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL MATURATION; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINESIS; DAUGHTER CELL; DEMYELINATION; DOWN REGULATION; ENVIRONMENTAL FACTOR; IMMUNOPHENOTYPING; MITOSIS; MOTOR ACTIVITY; MOUSE; NONHUMAN; OLIGODENDROGLIA; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; SISTER OLIGODENDROCYTE PROGENITOR CELL; STEM CELL; TELOPHASE; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL CYCLE; CENTRAL NERVOUS SYSTEM; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

AGING; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BROMODEOXYURIDINE; CELL CYCLE; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION; LUMINESCENT PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOSIS; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PROTEOGLYCANS; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR ALPHA; REPRESSOR PROTEINS; STEM CELLS;

EID: 84922985609     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22750     Document Type: Article

References (50)

1. Agathou S, Káradóttir RT, Kazanis I. 2013. Niche derived oligodendrocyte progenitors: A source of rejuvenation or complementation for local oligodendrogenesis? Front Cell Neurosci 7:188.
2. Barres BA, Raff MC, Gaese F, Bartke I, Dechant G, Barde YA. 1994. A crucial role for neurotrophin-3 in oligodendrocyte development. Nature 367:371-375.
3. Binamé F, Sakry D, Dimou L, Jolivel V, Trotter J. 2013. NG2 regulates directional migration of oligodendrocyte precursor cells via Rho GTPases and polarity complex proteins. J Neurosci 33:10858-10874.
4. Boda E, Viganò F, Rosa P, Fumagalli M, Labat-Gest V, Tempia F, Abbracchio MP, Dimou L, Buffo A. 2011. The GPR17 receptor in NG2 expressing cells: Focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia 59:1958-1973.
5. Buffo A, Vosko MR, Erturk D, Hamann GF, Jucker M, Rowitch D, Gotz M. 2005. Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proc Natl Acad Sci USA 102:18183-18188.
6. Chen Y, Wu H, Wang S, Koito H, Li J, Ye F, Hoang J, Escobar SS, Gow A, Arnett HA, Trapp BD, Karandikar NJ, Hsieh J, Lu QR. 2009. The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 12:1398-1406.
7. Ciana P, Fumagalli M, Trincavelli ML, Verderio C, Rosa P, Lecca D, Ferrario S, Parravicini C, Capra V, Gelosa P, Guerrini U, Belcredito S, Cimino M, Sironi L, Tremoli E, Rovati GE, Martini C, Abbracchio MP. 2006. The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J 25:4615-4627.
8. Corsini NS, Sancho-Martinez I, Laudenklos S, Glagow D, Kumar S, Letellier E, Koch P, Teodorczyk M, Kleber S, Klussmann S, Wiestler B, Brüstle O, Mueller W, Gieffers C, Hill O, Thiemann M, Seedorf M, Gretz N, Sprengel R, Celikel T, Martin-Villalba A. 2009. The death receptor CD95 activates adult neural stem cells for working memory formation and brain repair. Cell Stem Cell 5:178-190.
9. Daniele S, Trincavelli ML, Fumagalli M, Zappelli E, Lecca D, Bonfanti E, Campiglia P, Abbracchio MP, Martini C.2014. Does GRK-β arrestin machinery work as a "switch on" for GPR17-mediated activation of intracellular signaling pathways? Cell Signal 26:1310-1325.
10. 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.
11. Durand B, Raff M. 2000. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 22:64-71.
12. Eizenberg O, Faber-Elman A, Gottlieb E, Oren M, Rotter V, Schwartz M. 1995. Direct involvement of p53 in programmed cell death of oligodendrocytes. EMBO J 14:1136-1144.
13. Encinas JM, Michurina TV, Peunova N, Park JH, Tordo J, Peterson DA, Fishell G, Koulakov A, Enikolopov G. 2011. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell 8:566-579.
14. Florian MC, Geiger H. 2010. Concise review: Polarity in stem cells, disease, and aging. Stem Cells 28:1623-1629.
15. Fratangeli A, Parmigiani E, Fumagalli M, Lecca D, Benfante R, Passafaro M, Buffo A, Abbracchio MP, Rosa P. 2013. The regulated expression, intracellular trafficking, and membrane recycling of the P2Y-like receptor GPR17 in Oli-neu oligodendroglial cells. J Biol Chem 288:5241-5256.
16. Fumagalli M, Daniele S, Lecca D, Lee PR, Parravicini C, Fields RD, Rosa P, Antonucci F, Verderio C, Trincavelli ML, Bramanti P, Martini C, Abbracchio MP. 2011. Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. J Biol Chem 286:10593-10604.
17. Givogri MI, Schonmann V, Cole R, De Vellis J, Bongarzone ER. 2003. Notch1 and Numb genes are inversely expressed as oligodendrocytes differentiate. Dev Neurosci 25:50-64.
18. Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A. 2009. Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27:2032-2043.
19. Hill RA, Nishiyama A. 2014. NG2 cells (polydendrocytes): Listeners to the neural network with diverse properties. Glia 62:1195-1210.
20. 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 16:668-676.
21. Ibarrola N, Mayer-Pröschel M, Rodriguez-Peña A, Noble M. 1996. Evidence for the existence of at least two timing mechanisms that contribute to oligodendrocyte generation in vitro. Dev Biol 180:1-21.
22. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA. 1994. Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1-7.
23. Knoblich JA. 2010. Asymmetric cell division: Recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849-860.
24. Kondo T, Raff M. 2000. Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development 127:2989-2998.
25. Kukley M, Kiladze M, Tognatta R, Hans M, Swandulla D, Schramm J, Dietrich D. 2008. Glial cells are born with synapses. FASEB J 22:2957-2969.
26. Kukley M, Nishiyama A, Dietrich D. 2010. The fate of synaptic input to NG2 glial cells: Neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J Neurosci 30:8320-8331.
27. 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.
28. Li J, Ghiani CA, Kim JY, Liu A, Sandoval J, DeVellis J, Casaccia-Bonnefil P. 2008. Inhibition of p53 transcriptional activity: A potential target for future development of therapeutic strategies for primary demyelination. J Neurosci 28:6118-6127.
29. Liu A, Li J, Marin-Husstege M, Kageyama R, Fan Y, Gelinas C, Casaccia-Bonnefil P. 2006. A molecular insight of Hes5-dependent inhibition of myelin gene expression: Old partners and new players. EMBO J 25:4833-4842.
30. Lu B, Jan L, Jan YN. 2000. Control of cell divisions in the nervous system: Symmetry and asymmetry. Annu Rev Neurosci 23:531-556.
31. Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, Götz M, Haas CA, Kempermann G, Taylor V, Giachino C. 2010. Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell 6:445-456.
32. Maki T, Liang AC, Miyamoto N, Lo EH, Arai K. 2013. Mechanisms of oligodendrocyte regeneration from ventricular-subventricular zone-derived progenitor cells in white matter diseases. Front Cell Neurosci 7:275.
33. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. 2006. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 26:7907-7918.
34. Nakatani H, Martin E, Hassani H, Clavairoly A, Maire CL, Viadieu A, Kerninon C, Delmasure A, Frah M, Weber M, Nakafuku M, Zalc B, Thomas JL, Guillemot F, Nait-Oumesmar B, Parras C. 2013. Ascl1/Mash1 promotes brain oligodendrogenesis during myelination and remyelination. J Neurosci 33:9752-9768.
35. Rivers LE, Young KM, Rizzi M, Jamen F, Psachoulia K, Wade A, Kessaris N, Richardson WD. 2008. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 11:1392-1401.
36. Robins SC, Villemain A, Liu X, Djogo T, Kryzskaya D, Storch KF, Kokoeva MV. 2013. Extensive regenerative plasticity among adult NG2-glia populations is exclusively based on self-renewal. Glia 61:1735-1747.
37. Rolando C, Parolisi R, Boda E, Schwab ME, Rossi F, Buffo A. 2012. Distinct roles of Nogo-a and Nogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. J Neurosci 32:17788-17799.
38. Simon C, Götz M, Dimou L. 2011. Progenitors in the adult cerebral cortex: Cell cycle properties and regulation by physiological stimuli and injury. Glia 59:869-881.
39. Sohn J, Natale J, Chew LJ, Belachew S, Cheng Y, Aguirre A, Lytle J, Nait-Oumesmar B, Kerninon C, Kanai-Azuma M, Kanai Y, Gallo V. 2006. Identification of Sox17 as a transcription factor that regulates oligodendrocyte development. J Neurosci 26:9722-9735.
40. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
41. Sugiarto S, Persson AI, Munoz EG, Waldhuber M, Lamagna C, Andor N, Hanecker P, Ayers-Ringler J, Phillips J, Siu J, Lim DA, Vandenberg S, Stallcup W, Berger MS, Bergers G, Weiss WA, Petritsch C. 2011. Asymmetry-defective oligodendrocyte progenitors are glioma precursors. Cancer Cell 20:328-340.
42. Tamura Y, Kataoka Y, Cui Y, Takamori Y, Watanabe Y, Yamada H. 2007. Intracellular translocation of glutathione S-transferase pi during oligodendrocyte differentiation in adult rat cerebral cortex in vivo. Neuroscience 148:535-540.
43. van Wijngaarden P, Franklin RJ. 2013. Ageing stem and progenitor cells: Implications for rejuvenation of the central nervous system. Development 140:2562-2575.
44. Walker AS, Goings GE, Kim Y, Miller RJ, Chenn A, Szele FG. 2010. Nestin reporter transgene labels multiple central nervous system precursor cells. Neural Plast 2010:894374.
45. Wren D, Wolswijk G, Noble M. 1992. In vitro analysis of the origin and maintenance of O-2A adult progenitor cells. J Cell Biol 116:167-176.
46. Yakovlev AY, Boucher K, Mayer-Proschel M, Noble M. 1998. Quantitative insight into proliferation and differentiation of oligodendrocyte type 2 astrocyte progenitor cells in vitro. Proc Natl Acad Sci USA 95:14164-14167.
47. Yamashita YM, Yuan H, Cheng J, Hunt AJ. 2010. Polarity in stem cell division: Asymmetric stem cell division in tissue homeostasis. Cold Spring Harb Perspect Biol 2:a001313.
48. Young KM, Psachoulia K, Tripathi RB, Dunn SJ, Cossell L, Attwell D, Tohyama K, Richardson WD. 2013. Oligodendrocyte dynamics in the healthy adult CNS: Evidence for myelin remodeling. Neuron 77:873-885.
49. Zhu Q, Zhao X, Zheng K, Li H, Huang H, Zhang Z, Mastracci T, Wegner M, Chen Y, Sussel L, Qiu M. 2014. Genetic evidence that Nkx2.2 and Pdgfra are major determinants of the timing of oligodendrocyte differentiation in the developing CNS. Development 141:548-555.
50. Zhu X, Hill RA, Dietrich D, Komitova M, Suzuki R, Nishiyama A. 2011. Age-dependent fate and lineage restriction of single NG2 cells. Development 138:745-753.