Stiff substrates enhance cultured neuronal network activity

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Zhang, Quan You ^a,b   Zhang, Yan Yan ^a   Xie, Jing ^a   Li, Chen Xu ^c   Chen, Wei Yi ^b   Liu, Bai Lin ^a   Wu, Xiao An ^a   Li, Shu Na ^d   Huo, Bo ^d   Jiang, Lin Hua ^e,f   Zhao, Hu Cheng ^a  

^a TSINGHUA UNIVERSITY   (China)

^b TAIYUAN UNIVERSITY OF TECHNOLOGY   (China)

^c Datong University   (China)

^d BEIJING INSTITUTE OF TECHNOLOGY   (China)

^e UNIVERSITY OF LEEDS   (United Kingdom)

^f XINXIANG MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CULTURE MEDIUM;

ANIMAL; CALCIUM SIGNALING; CELL CULTURE; CULTURE MEDIUM; CYTOLOGY; HIPPOCAMPUS; METABOLISM; MOUSE; NERVE CELL; NERVE CELL NETWORK; PC12 CELL LINE; PHYSIOLOGY; RAT;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CELLS, CULTURED; CULTURE MEDIA; HIPPOCAMPUS; MICE; NERVE NET; NEURONS; PC12 CELLS; RATS;

EID: 84907021455     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06215     Document Type: Article

References (40)

1. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell. 126, 677-689 (2006).
2. Georges, P. C., Miller, W. J., Meaney, D. F., Sawyer, E. S. & Janmey, P. A. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012-3018 (2006).
3. Solon, J., Levental, I., Sengupta, K., Georges, P. C. & Janmey, P. A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93, 4453-4461 (2007).
4. Kostic, A., Sap, J. & Sheetz, M. P. RPTPα is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J. Cell. Sci. 120, 3895-3904 (2007).
5. Previtera, M. L., Langhammer, C. G., Langrana, N. A. & Firestein, B. L. Regulation of dendrite arborization by substrate stiffness is mediated by glutamate receptors. Ann. Biomed. Eng. 38, 3733-3743 (2010).
6. Mih, J. D., Marinkovic, A., Liu, F., Sharif, A. S. & Tschumperlin, D. J. Matrix stiffness reverses the effect of actomyosin tension on cell proliferation. J. Cell. Sci. 125, 5974-5983 (2012).
7. Schiller, H. B. et al. β1-and αv-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell. Biol. 15, 625-636 (2013).
8. Sur, S., Newcomb, C. J., Webber, M. J. & Stupp, S. I. Tuning supramolecular mechanics to guide neuron development. Biomaterials. 34, 4749-4757 (2013).
9. Yip, A. K. et al. Cellular response to substrate rigidity is governed by either stress or strain. Biophys. J. 104, 19-29 (2013).
10. Place, E. S., Evans, N. D. & Stevens, M. M. Complexity in biomaterials for tissue engineering. Nat. Mater. 8, 457-470 (2009).
11. Previtera, M. L. et al. The effects of substrate elastic modulus on neural precursor cell behavior. Ann. Biomed. Eng. 41, 1193-1207 (2013).
12. Fabbro, A., Bosi, S., Ballerini, L. & Prato, M. Carbon nanotubes: artificial nanomaterials to engineer single neurons and neuronal networks. ACS Chem. Neurosci. 15, 611-618 (2012).
13. Cellot, G. et al. Carbon nanotube scaffolds tune synaptic strength in cultured neural circuits: novel frontiers in nanomaterial-tissue interactions. J. Neurosci. 31, 12945-12953 (2011).
14. Tang, T. et al. Enhancement of electrical signaling in neural networks on graphene films. Biomaterials. 34, 6402-6411 (2013).
15. Franze, K., Janmey, P. A. & Guck, J. Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15, 227-251 (2013).
16. Palchesko, R. N., Zhang, L., Sun, Y. & Feinberg, A. W. Development of polydimethylsiloxane substrates with tunable elastic modulus to study cell mechanobiology in muscle and nerve. PLoS One. 7, e51499 (2012).
17. Berridge, M. J. Neuronal calcium signaling. Neuron. 21, 13-26 (1998).
18. 2+ channelopathy. Neuron. 43, 387-400 (2004).
19. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron. 18, 243-255 (1997).
20. Bacci, A., Verderio, C., Pravettoni, E. & Matteoli, M. Synaptic and intrinsic mechanisms shape synchronous oscillations in hippocampal neurons in culture. Eur. J. Neurosci. 11, 389-397 (1999).
21. 2+ oscillations in cortical neurons. Brain Res. 767, 239-249 (1997).
22. Przewlocki, R. et al. Opioid enhancement of calcium oscillations and burst events involving NMDA receptors and L-type calcium channels in cultured hippocampal neurons. J. Neurosci. 19, 9705-9715 (1999).
23. 2+ spikes in cultured hippocampal networks through G-protein-coupled receptors. J. Neurosci. 23, 4156-4163 (2003).
24. Numakawa, T. et al. Brain-derived neurotrophic factor-induced potentiation of Ca(2+) oscillations in developing cortical neurons. J. Biol. Chem. 277, 6520-6529 (2002).
25. Chen, G., Harata, N. C. & Tsien, R. W. Paired-pulse depression of unitary quantal amplitude at single hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 101, 1063-1068 (2004).
26. Atwood, H. L. & Karunanithi, S. Diversification of synaptic strength: presynaptic elements. Nat. Rev. Neurosci. 3, 497-516 (2002).
27. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64, 355-405 (2002).
28. Williams, M. E. et al. Cadherin-9 regulates synapse specific differentiation in the developing hippocampus. Neuron. 71, 640-655 (2011).
29. Goforth, P. B., Ren, J. H., Schwartz, B. S. & Satin, L. S. Excitatory synaptic transmission and network activity are depressed following mechanical injury in cortical neurons. J. Neurophysiol. 105, 2350-2363 (2011).
30. Firestein, B. L., Langhammer, C. G., Langrana, L. N.&Firestein, B. L. Regulation of dendrite arborization by substrate stiffness is mediated by glutamate receptors. Annu. Biomed. Eng. 38, 3733-3743 (2010).
31. Shyy, J. Y. & Chien, S. Role of integrins in endothelial mechanosensing of shear stress. Circ. Res. 91, 769-755 (2002).
32. Choquet, D., Felsenfeld, D. P. & Sheetz, M. P. Extracellular matrix rigidity causes strengthening of integrin cytoskeleton linkages. Cell. 88, 39-48 (1997).
33. Lin, B., Arai, A. C., Lynch, A. G. & Gall, C. M. Integrins regulate NMDA receptor mediated synaptic currents. J. Neurophysiol. 89, 2874-2878 (2003).
34. 2+ oscillation via RhoA pathway in stem cells. J. Cell. Physiol. 218, 285-293 (2009).
35. Li, N. et al. The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials. 32, 9374-9382 (2011).
36. Kobayashi, T. & Sokabe, M. Sensing substrate rigidity by mechanosensitive ion channels with stress fibers and focal adhesions. Curr. Opin. Cell. Biol. 22, 669-676 (2010).
37. Cheng, C. M. et al. Probing localized neural mechanotransduction through surface-modified elastomeric matrices and electrophysiology. Nat. Protoc. 5, 714-724 (2010).
38. Zhang, M. G., Cao, Y. P., Li, G. Y. & Feng, X. Q. Spherical indentation method for determining the constitutive parameters of hyperelastic soft materials. Biomech. Model. Mechanobiol. (doi 10.1007/s10237-013-0481-4) (2013).
39. Beaudoin, G. M. et al. Culturing pyramidal neurons from the early postnatal mouse hippocampus and cortex. Nat. Protoc. 7, 1741-1754 (2012).
40. Lefler, Y., Yarom, Y. & Uusisaari, M. Y. Cerebellar inhibitory input to the inferior olive decreases electrical coupling and blocks subthreshold oscillations. Neuron. 81, 1389-1400 (2014).