Mechanostimulation promotes nuclear and epigenetic changes in oligodendrocytes

Journal of Neuroscience

Volumn 36, Issue 3, 2016, Pages 806-813

  Hernandez, Marylens ^a,b   Patzig, Julia ^a   Mayoral, Sonia R ^c   Costa, Kevin D ^d   Chan, Jonah R ^c   Casaccia, Patrizia ^a,e  

^a Department of Neuroscience ^*  (United States)

^b Graduate School of Biological Sciences   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Cardiovascular Research Center   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Chromatin; Cytoskeleton; Histone; Myelin; Nucleus

Indexed keywords

F ACTIN; G ACTIN; HISTONE; LENTIVIRUS VECTOR; MEMBRANE PROTEIN; SPECTRIN REPEAT CONTAINING NUCLEAR ENVELOPE 1 GENE ENCODING PROTEIN; UNCLASSIFIED DRUG; NERVE PROTEIN; NUCLEAR PROTEIN; SYNE1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOSKELETON; EPIGENETICS; FEMALE; FLUORESCENCE MICROSCOPY; GENE; GENE SILENCING; GENETIC TRANSFECTION; HETEROCHROMATIN; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MECHANICAL STIMULATION; MECHANOSTIMULATION; MOUSE; MYELINATION; NONHUMAN; NUCLEOSKELETON; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SPECTRIN REPEAT CONTAINING NUCLEAR ENVELOPE 1 GENE; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; GENETIC EPIGENESIS; GENETICS; MECHANOTRANSDUCTION; METABOLISM; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL NUCLEUS; EPIGENESIS, GENETIC; FEMALE; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OLIGODENDROGLIA;

EID: 84955148761     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2873-15.2016     Document Type: Article

References (45)

1. Anno T, Sakamoto N, Sato M (2012) Role of nesprin-1 in nuclear deformation in endothelial cells under static and uniaxial stretching conditions. Biochem Biophys Res Commun 424:94-99. CrossRef Medline
2. Barres BA, Lazar MA, Raff MC (1994) A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120:1097-1108. Medline
3. Costa KD, Hucker WJ, Yin FC (2002) Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil Cytoskeleton 52:266-274. CrossRef Medline
4. Dugas JC, Ibrahim A, Barres BA (2012) The T3-induced gene KLF9 regulates oligodendrocyte differentiation and myelin regeneration. Mol Cell Neurosci 50:45-57. CrossRef Medline
5. Emery B, Dugas JC (2013) Purification of oligodendrocyte lineage cells from mouse cortices by immunopanning. Cold Spring Harb Protoc 2013: 854-868. Medline
6. Fortin D, Rom E, Sun H, Yayon A, Bansal R (2005) Distinct fibroblast growth factor (FGF)/FGF receptor signaling pairs initiate diverse cellular responses in the oligodendrocyte lineage. J Neurosci 25:7470-7479. CrossRef Medline
7. Fünfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS, Edgar J, Brinkmann BG, Kassmann CM, Tzvetanova ID, Möbius W, Diaz F, Meijer D, Suter U, Hamprecht B, Sereda MW, Moraes CT, Frahm J, Goebbels S, Nave KA (2012) Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517-521. Medline
8. Furusho M, Kaga Y, Ishii A, Hebert JM, Bansal R (2011) Fibroblast growth factor signaling is required for the generation of oligodendrocyte progenitors from the embryonic forebrain. J Neurosci 31:5055-5066. CrossRef Medline
9. Gao FB, Apperly J, Raff M (1998) Cell-intrinsic timers and thyroid hormone regulate the probability of cell-cycle withdrawal and differentiation of oligodendrocyte precursor cells. Dev Biol 197:54-66. CrossRef Medline
10. Hart IK, Richardson WD, Bolsover SR, Raff MC (1989) PDGF and intracel-lular signaling in the timing ofoligodendrocyte differentiation. J Cell Biol 109:3411-3417. CrossRef Medline
11. Hirata H, Sokabe M, Lim CT (2014) Molecular mechanisms underlying the force-dependent regulation of actin-to-ECM linkage at the focal adhesions. Prog Mol Biol Transl Sci 126:135-154. CrossRef Medline
12. Jagielska A, Norman AL, Whyte G, Vliet KJ, Guck J, Franklin RJ (2012) Mechanical environment modulates biological properties of oligoden-drocyte progenitor cells. Stem Cells Dev 21:2905-2914. CrossRef Medline
13. Jahed Z, Shams H, Mehrbod M, Mofrad MR (2014) Mechanotransduction pathways linking the extracellular matrixto the nucleus. Int RevCell Mol Biol 310:171-220. CrossRef Medline
14. Kaminski A, Fedorchak GR, Lammerding J (2014) The cellular mas-termind(?)-mechanotransduction and the nucleus. Prog Mol Biol Transl Sci 126:157-203. CrossRef Medline
15. Lee Y, Morrison BM, Li Y, Lengacher S, Farah MH, Hoffman PN, Liu Y, Tsingalia A, Jin L, Zhang PW, Pellerin L, Magistretti PJ, Rothstein JD (2012) Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487:443-448. CrossRef Medline
16. Li Q, Kumar A, Makhija E, Shivashankar GV (2014) The regulation of dynamic mechanical coupling between actin cytoskeleton and nucleus by matrix geometry. Biomaterials 35:961-969. CrossRef Medline
17. Liu J, Casaccia P (2010) Epigenetic regulation of oligodendrocyte identity. Trends Neurosci 33:193-201. CrossRef Medline
18. Liu J, Magri L, Zhang F, Marsh NO, Albrecht S, Huynh JL, Kaur J, Kuhlmann T, Zhang W, Slesinger PA, Casaccia P (2015) Chromatin landscape defined by repressive histone methylation during oligodendrocyte differentiation. J Neurosci 35:352-365. CrossRef Medline
19. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J (2011) The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 286:26743-26753. CrossRef Medline
20. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky I, Chan J, McMahon AP, Stiles CD, Rowitch DH (2000) Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317-329. CrossRef Medline
21. Magri L, Swiss VA, Jablonska B, Lei L, Pedre X, Walsh M, Zhang W, Gallo V, Canoll P, Casaccia P (2014) E2F1 coregulates cell cycle genes and chro-matin components during the transition of oligodendrocyte progenitors from proliferation to differentiation. J Neurosci 34:1481-1493. CrossRef Medline
22. Mammoto A, Mammoto T, Ingber DE (2012) Mechanosensitive mechanisms in transcriptional regulation. J Cell Sci 125:3061-3073. CrossRef Medline
23. Maniotis AJ, Chen CS, Ingber DE (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci U S A 94:849-854. CrossRef Medline
24. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P (2002) His-tone deacetylase activity is necessaryfor oligodendrocyte lineage progression. J Neurosci 22:10333-10345. Medline
25. Martins RP, Finan JD, Guilak F, Lee DA (2012) Mechanical regulation of nuclear structure and function. Annu Rev Biomed Eng 14:431-455. CrossRef Medline
26. Nagayama K, Yamazaki S, Yahiro Y, Matsumoto T (2014) Estimation ofthe mechanical connection between apical stress fibers and the nucleus in vascular smooth muscle cells cultured on a substrate. J Biomech 47: 1422-1429. CrossRef Medline
27. Nawaz S, Sanchez P, Schmitt S, Snaidero N, Mitkovski M, Velte C, Brückner BR, Alexopoulos I, Czopka T, Jung SY, Rhee JS, Janshoff A, Witke W, Schaap IA, Lyons DA, Simons M (2015) Actin filament turnover drives leading edge growth during myelin sheath formation in the central nervous system. Dev Cell 34:139-151. CrossRef Medline
28. Nery S, Wichterle H, Fishell G (2001) Sonic hedgehog contributes to oligo-dendrocyte specification in the mammalian forebrain. Development 128: 527-540. Medline
29. Ostlund C, Folker ES, Choi JC, Gomes ER, Gundersen GG, Worman HJ (2009) Dynamics and molecular interactions oflinker ofnucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci 122:4099-4108. CrossRef Medline
30. Pombo PM, Barettino D, Ibarrola N, Vega S, Rodríguez-Pena A (1999) Stimulation ofthe myelin basic protein gene expression by9-cis-retinoic acid and thyroid hormone: activation in the context of its native promoter. Brain Res Mol Brain Res 64:92-100. CrossRef Medline
31. Razafsky D, Hodzic D (2009) Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186:461-472. CrossRef Medline
32. Rinholm JE, Hamilton NB, Kessaris N, Richardson WD, Bergersen LH, Attwell D (2011) Regulation of oligodendrocyte development and myeli-nation by glucose and lactate. J Neurosci 31:538-548. CrossRef Medline
33. Rosenberg SS, Kelland EE, Tokar E, De la Torre AR, Chan JR (2008) The geometric and spatial constraints ofthe microenvironment induce oligo-dendrocyte differentiation. Proc Natl Acad Sci U S A 105:14662-14667. CrossRef Medline
34. Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131:4131-4142. CrossRef Medline
35. Schneider R, Grosschedl R (2007) Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev 21: 3027-3043. CrossRef Medline
36. Schregel K, Wuerfel E, Garteiser P, Gemeinhardt I, Prozorovski T, Aktas O, Merz H, Petersen D, Wuerfel J, Sinkus R (2012) Demyelination reduces brain parenchymal stiffness quantified in vivo by magnetic resonance elastography. Proc Natl Acad SciUSA 109:6650-6655. CrossRef Medline
37. Shen S, Li J, Casaccia-Bonnefil P (2005) Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain.JCell Biol 169:577-589. CrossRef Medline
38. Sher F, Boddeke E, Olah M, Copray S (2012) Dynamic changes in Ezh2 gene occupancy underlie its involvement in neural stem cell self-renewal and differentiation towards oligodendrocytes. PLoS One 7:e40399. CrossRef Medline
39. Sosa BA, Rothballer A, Kutay U, Schwartz TU (2012) LINC complexes form by binding of three KASH peptides to domain interfaces oftrimeric SUN proteins. Cell 149:1035-1047. CrossRef Medline
40. Starr DA, Fischer JA (2005) KASH 'n Karry: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. Bioessays 27:1136-1146. CrossRef Medline
41. Wang J, Zhang Y, Zhang N, Wang C, Herrler T, Li Q (2015) An updated review of mechanotransduction in skin disorders: transcriptional regulators, ion channels, and microRNAs. Cell Mol Life Sci 72:2091-2106. CrossRef Medline
42. Wu M, Hernandez M, Shen S, Sabo JK, Kelkar D, Wang J, O'Leary R, Phillips GR, Cate HS, Casaccia P (2012) Differential modulation of the oligo-dendrocyte transcriptome by sonic hedgehog and bone morphogenetic protein 4 via opposing effects on histone acetylation. J Neurosci 32:6651-6664. CrossRef Medline
43. Ye F, Chen Y, Hoang T, Montgomery RL, Zhao XH, Bu H, Hu T, Taketo MM, van Es JH, Clevers H, Hsieh J, Bassel-Duby R, Olson EN, Lu QR (2009) HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat Neurosci 12:829-838. CrossRef Medline
44. Zhou YX, Armstrong RC (2007) Interaction of fibroblast growth factor 2 (FGF2) and notch signaling components in inhibition ofoligodendrocyte progenitor (OP) differentiation. Neurosci Lett 421:27-32. CrossRef Medline
45. Zuchero JB, Fu MM, Sloan SA, Ibrahim A, Olson A, Zaremba A, Dugas JC, Wienbar S, Caprariello AV, Kantor C, Leonoudakus D, Lariosa-Willingham K, Kronenberg G, Gertz K, Soderling SH, Miller RH, Barres BA (2015) CNS myelin wrapping is driven by actin disassembly. Dev Cell 34:152-167. CrossRef Medline