Modulation of oligodendrocyte differentiation and maturation by combined biochemical and mechanical cues

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Lourenço, Tânia ^a,b   Paes De Faria, Joana ^c,d   Bippes, Christian A ^e   Maia, Joaõ ^f   Lopes Da Silva, José A ^g   Relvas, Joaõ B ^c,d   Graõs, Mário ^a,b  

^a Bioinformatics Unit   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e Nanosurf AG   (Switzerland)

^f UNIVERSITY OF COIMBRA   (Portugal)

^g UNIVERSITY OF AVEIRO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ACRYLIC ACID RESIN; FIBRONECTIN; LAMININ; MYELIN BASIC PROTEIN; POLYACRYLAMIDE GELS; PROTEOLIPID PROTEIN;

ANIMAL; BIOMECHANICS; CELL DIFFERENTIATION; CELL LINE; CHEMISTRY; CYTOLOGY; EXTRACELLULAR MATRIX; METABOLISM; OLIGODENDROGLIA; PHYSIOLOGY; RAT;

ACRYLIC RESINS; ANIMALS; BIOMECHANICAL PHENOMENA; CELL DIFFERENTIATION; CELL LINE; EXTRACELLULAR MATRIX; FIBRONECTINS; LAMININ; MYELIN BASIC PROTEIN; MYELIN PROTEOLIPID PROTEIN; OLIGODENDROGLIA; RATS;

EID: 84958568082     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21563     Document Type: Article

References (60)

1. Kessaris, N., Pringle, N., Richardson, W. D. Specification of CNS glia from neural stem cells in the embryonic neuroepithelium. Philos Trans R Soc Lond B Biol Sci 363, 71-85, doi: 10.1098/rstb.2006.2013 (2008).
2. Bogler, O., Wren, D., Barnett, S. C., Land, H., Noble, M. Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2 A) progenitor cells. Proc Natl Acad Sci USA 87, 6368-6372, doi: 10.1073/pnas.87.16.6368 (1990).
3. Miller, R. H. Regulation of oligodendrocyte development in the vertebrate CNS. Prog Neurobiol 67, 451-467, doi: 10.16/S0301-0082(02)00058-8 (2002).
4. Richardson, W. D., Kessaris, N., Pringle, N. Oligodendrocyte wars. Nat Rev Neurosci 7, 11-18, doi: 10.38/nrn1826 (2006).
5. Rivera, F. J. et al. Deciphering the oligodendrogenic program of neural progenitors: cell intrinsic and extrinsic regulators. Stem Cells Dev 19, 595-606, doi: 10.89/scd.2009.0293 (2010).
6. Rowitch, D. H. Glial specification in the vertebrate neural tube. Nat Rev Neurosci 5, 409-419, doi: 10.38/nrn1389 (2004).
7. Barres, B. A., Lazar, M. A., Raff, M. C. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 120, 1097-1108 (1994).
8. Lourenco, A. S., Baldeiras, I., Graos, M., Duarte, C. B. Proteomics-based technologies in the discovery of biomarkers for multiple sclerosis in the cerebrospinal fluid. Curr Mol Med 11, 326-349, doi: 10.2174/156652411795677981 (2011).
9. Câmara, J., ffrench-Constant, C. Lessons from oligodendrocyte biology on promoting repair in multiple sclerosis. Journal of Neurology 254, I15-I22, doi: 10.07/s00415-007-1004-y (2007).
10. Franklin, R. J., Ffrench-Constant, C. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9, 839-855, doi: 10.38/nrn2480 (2008).
11. McTigue, D. M., Tripathi, R. B. The life, death, and replacement of oligodendrocytes in the adult CNS. J Neurochem 107, 1-19, doi: 10.1111/j.1471-4159.2008.05570.x (2008).
12. Baumann, N., Pham-Dinh, D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 81, 871-927 (2001).
13. Bauer, N. G., ffrench-Constant, C. Physical forces in myelination and repair: a question of balance? J Biol 8, 78, doi: 10.1186/jbiol169 (2009).
14. Frantz, C., Stewart, K. M., Weaver, V. M. The extracellular matrix at a glance. J Cell Sci 123, 4195-4200, doi: 10.1242/jcs.023820 (2010).
15. Baron, W., Decker, L., Colognato, H., ffrench-Constant, C. Regulation of integrin growth factor interactions in oligodendrocytes by lipid raft microdomains. Curr Biol 13, 151-155, doi: 10.16/S0960-9822(02)01437-9 (2003).
16. Buttery, P. C., ffrench-Constant, C. Laminin-2/integrin interactions enhance myelin membrane formation by oligodendrocytes. Mol Cell Neurosci 14, 199-212, doi: 10.06/mcne.1999.0781 (1999).
17. Chun, S. J., Rasband, M. N., Sidman, R. L., Habib, A. A., Vartanian, T. Integrin-linked kinase is required for laminin-2-induced oligodendrocyte cell spreading and CNS myelination. J Cell Biol 163, 397-408, doi: 10.83/jcb.200304154 (2003).
18. Colognato, H., Ramachandrappa, S., Olsen, I. M., ffrench-Constant, C. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167, 365-375, doi: 10.83/jcb.200404076 (2004).
19. Stoffels, J. M. et al. Fibronectin aggregation in multiple sclerosis lesions impairs remyelination. Brain 136, 116-131, doi: 10.93/brain/aws313 (2013).
20. ffrench-Constant, C., Colognato, H. Integrins: versatile integrators of extracellular signals. Trends Cell Biol 14, 678-686, doi: 10.16/j.tcb.2004.10.005 (2004).
21. Engler, A. J., Sen, S., Sweeney, H. L., Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689, doi: 10.16/j.cell.2006.06.044 (2006).
22. Saha, K. et al. Substrate modulus directs neural stem cell behavior. Biophys J 95, 4426-4438, doi: 10.1529/biophysj.108.132217 (2008).
23. Jagielska, A. et al. Mechanical environment modulates biological properties of oligodendrocyte progenitor cells. Stem Cells Dev 21, 2905-2914, doi: 10.89/scd.2012.0189 (2012).
24. Kippert, A., Fitzner, D., Helenius, J., Simons, M. Actomyosin contractility controls cell surface area of oligodendrocytes. BMC Cell Biol 10, 71, doi: 10.1186/1471-2121-10-71 (2009).
25. Moore, S. W., Roca-Cusachs, P., Sheetz, M. P. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 19, 194-206, doi: 10.16/j.devcel.2010.07.018 (2010).
26. Soofi, S. S., Last, J. A., Liliensiek, S. J., Nealey, P. F., Murphy, C. J. The elastic modulus of Matrigel as determined by atomic force microscopy. J Struct Biol 167, 216-219, doi: 10.16/j.jsb.2009.05.005 (2009).
27. Trappmann, B. et al. Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 11, 642-649, doi: 10.38/nmat3339 (2012).
28. Wen, J. H. et al. Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat Mater 13, 979-987, doi: 10.38/nmat4051 (2014).
29. Gutierrez, E., Groisman, A. Measurements of elastic moduli of silicone gel substrates with a microfluidic device. PLoS One 6, e25534, doi: 10.1371/journal.pone.0025534 (2011).
30. Saha, K. et al. Surface creasing instability of soft polyacrylamide cell culture substrates. Biophys J 99, L94-96, doi: 10.16/j. bpj.2010.09.045 (2010).
31. Louis, J. C., Magal, E., Muir, D., Manthorpe, M., Varon, S. CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J Neurosci Res 31, 193-204, doi: 10.02/jnr.490310125 (1992).
32. Behar, T. N. Analysis of fractal dimension of O2A glial cells differentiating in vitro. Methods 24, 331-339, doi: 10.06/meth.2001.1203 (2001).
33. Fernandez, E., Jelinek, H. F. Use of fractal theory in neuroscience: methods, advantages, and potential problems. Methods 24, 309-321, doi: 10.06/meth.2001.1201 (2001).
34. Aulic, S. et al. Defined alpha-synuclein prion-like molecular assemblies spreading in cell culture. BMC Neurosci 15, 69, doi: 10.1186/1471-2202-15-69 (2014).
35. Dai, J., Bercury, K. K., Ahrendsen, J. T., Macklin, W. B. Olig1 function is required for oligodendrocyte differentiation in the mouse brain. J Neurosci 35, 4386-4402, doi: 10.1523/JNEUROSCI.4962-14.2015 (2015).
36. Guardiola-Diaz, H. M., Ishii, A., Bansal, R. Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation. Glia 60, 476-486, doi: 10.1002/glia.22281 (2012).
37. Fischer, R., Wajant, H., Kontermann, R., Pfizenmaier, K., Maier, O. Astrocyte-specific activation of TNFR2 promotes oligodendrocyte maturation by secretion of leukemia inhibitory factor. Glia 62, 272-283, doi: 10.02/glia.22605 (2014).
38. Zhang, K. et al. A curve fitting method of quantifying green fluorescent protein expression level in Escherichia coli. J Microbiol Methods 80, 172-177, doi: 10.16/j.mimet.2009.12.003 (2010).
39. Osterhout, D. J., Wolven, A., Wolf, R. M., Resh, M. D., Chao, M. V. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145, 1209-1218, doi: 10.83/jcb.145.6.1209 (1999).
40. Wang, H., Tewari, A., Einheber, S., Salzer, J. L., Melendez-Vasquez, C. V. Myosin II has distinct functions in PNS and CNS myelin sheath formation. J Cell Biol 182, 1171-1184, doi: 10.83/jcb.200802091 (2008).
41. Wang, H. et al. Myosin II is a negative regulator of oligodendrocyte morphological differentiation. J Neurosci Res 90, 1547-1556, doi: 10.02/jnr.23036 (2012).
42. Bauer, N. G., Richter-Landsberg, C., Ffrench-Constant, C. Role of the oligodendroglial cytoskeleton in differentiation and myelination. Glia 57, 1691-1705, doi: 10.02/glia.20885 (2009).
43. Kramer-Albers, E. M., White, R. From axon-glial signalling to myelination: the integrating role of oligodendroglial Fyn kinase. Cell Mol Life Sci 68, 2003-2012, doi: 10.07/s00018-010-0616-z (2011).
44. Clark, K., Langeslag, M., Figdor, C. G., van Leeuwen, F. N. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol 17, 178-186, doi: 10.16/j.tcb.2007.02.002 (2007).
45. Cretu, A., Castagnino, P., Assoian, R. Studying the effects of matrix stiffness on cellular function using acrylamide-based hydrogels. J Vis Exp. e2089, doi: 10.3791/2089 (2010).
46. Hoffecker, I. T., Guo, W. H., Wang, Y. L. Assessing the spatial resolution of cellular rigidity sensing using a micropatterned hydrogel-photoresist composite. Lab Chip 11, 3538-3544, doi: 10.39/c1lc20504h (2011).
47. Polio, S. R., Rothenberg, K. E., Stamenovic, D., Smith, M. L. A micropatterning and image processing approach to simplify measurement of cellular traction forces. Acta Biomater 8, 82-88, doi: 10.16/j.actbio.2011.08.013 (2012).
48. Buxboim, A., Rajagopal, K., Brown, A. E., Discher, D. E. How deeply cells feel: methods for thin gels. J Phys Condens Matter 22, 194116, doi: 10.88/0953-8984/22/19/194116 (2010).
49. Tse, J. R., Engler, A. J. Preparation of hydrogel substrates with tunable mechanical properties. Curr Protoc Cell Biol Chapter 10, Unit 10 16, doi: 10.02/0471143030.cb1016s47 (2010).
50. Sader, J. E., Chon, J. W. M., Mulvaney, P. Calibration of rectangular atomic force microscope cantilevers. Review of Scientific Instruments 70, 3967-3969, doi: 10.1063/1.1150021 (1999).
51. Sneddon, I. N. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 3, 47-57 (1965).
52. Young, D. A., Choi, Y. S., Engler, A. J., Christman, K. L. Stimulation of adipogenesis of adult adipose-derived stem cells using substrates that mimic the stiffness of adipose tissue. Biomaterials 34, 8581-8588, doi: 10.16/j.biomaterials.2013.07.103 (2013).
53. Domke, J., Radmacher, M. Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir 14, 3320-3325, doi: 10.1021/la9713006 (1998).
54. Engler, A. J., Rehfeldt, F., Sen, S., Discher, D. E. Microtissue Elasticity: Measurements by Atomic Force Microscopy and Its Influence on Cell Differentiation. In Methods in Cell Biology. Vol. 83, 521-545 (Academic Press, 2007).
55. Liu, G. J., Madsen, B. W. PACAP38 modulates activity of NMDA receptors in cultured chick cortical neurons. J Neurophysiol 78, 2231-2234 (1997).
56. Ji, S., Doucette, J. R., Nazarali, A. J. Sirt2 is a novel in vivo downstream target of Nkx2.2 and enhances oligodendroglial cell differentiation. J Mol Cell Biol 3, 351-359, doi: 10.93/jmcb/mjr009 (2011).
57. McCarthy, K. D., de Vellis, J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85, 890-902, doi: 10.83/jcb.85.3.890 (1980).
58. Milner, R., ffrench-Constant, C. A developmental analysis of oligodendroglial integrins in primary cells: changes in alpha v-associated beta subunits during differentiation. Development 120, 3497-3506 (1994).
59. Bottenstein, J. E., Sato, G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proceedings of the National Academy of Sciences 76, 514-517 (1979).
60. Leite, C. et al. Differentiation of human umbilical cord matrix mesenchymal stem cells into neural-like progenitor cells and maturation into an oligodendroglial-like lineage. PLoS One 9, e111059, doi: 10.1371/journal.pone.0111059 (2014).