Neural cell alignment by patterning gradients of the extracellular matrix protein laminin

Interface Focus

Volumn 4, Issue 1, 2014, Pages

  Chelli, Beatrice ^a,b   Barbalinardo, Marianna ^a,b   Valle, Francesco ^a   Greco, Pierpaolo ^c   Bystrenova, Eva ^a   Bianchi, Michele ^a,e   Biscarini, Fabio ^a,d  

^a CNR   (Italy)

^b Nano4bio Srl ^*  (Italy)

^c SCRIBA Nanotecnologie Srl   (Italy)

^d Dip Scienze della Vita   (Italy)

^e RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

Author keywords

Laminin; Neural cells; Patterning; Protein gradients; Soft lithography

Indexed keywords

EID: 84890895644     PISSN: 20428898     EISSN: 20428901     Source Type: Journal    
DOI: 10.1098/rsfs.2013.0041     Document Type: Article

References (60)

1. Dado D, Levenberg S. 2009 Cell-scaffold mechanical interplay within engineered tissue. Semin. Cell Dev. Biol. 20, 656-664. (doi:10.1016/j.semcdb. 2009.02.001)
2. Omstead DR, Baird LG, Christenson L, Du Moulin G, Tubo R, Maxted DD, Davis J, Gentile FT. 1998 Fal voluntary guidance for the development of tissueengineered products. Tissue Eng. 4, 239-266. (doi:10.1089/ten.1998.4.239)
3. Timko BP, Cohen-Karni T, Qing Q, Tian B, Lieber CM. 2010 Design and implementation of functional nanoelectronic interfaces with biomolecules, cells, and tissue using nanowire device arrays. IEEE Trans. Nanotechnol. 9, 269-280. (doi:10.1109/TNANO. 2009.2031807)
4. Lee MR, Kwon KW, Jung H, Kim HN, Suh KY, Kim K, Kim KS. 2010 Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. Biomaterials 31, 4360-4366. (doi:10.1016/j.biomaterials. 2010.02.012)
5. Gauvin R, Khademhosseini A. 2011 Microscale technologies and modular approaches for tissue engineering: moving toward the fabrication of complex functional structures. ACS Nano 5, 4258-4264. (doi:10.1021/nn201826d)
6. von der Mark K, Park J, Bauer S, Schmuki P. 2010 Nanoscale engineering of biomimetic surfaces: cues from the extracellular matrix. Cell Tissue Res. 339, 131-153. (doi:10.1007/s00441-009-0896-5)
7. Discher DE, Mooney DJ, Zandstra PW. 2009 Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673-1677. (doi:10.1126/ science.1171643)
8. Roeder I, Loeffler M, Glauche I, Participants O. 2011 Towards a quantitative understanding of stem cellniche interaction: experiments, models, and technologies. Blood Cells Mol. Dis. 46, 308-317. (doi:10.1016/j.bcmd.2011.03.001)
9. Geiger B, Spatz JP, Bershadsky AD. 2009 Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33. (doi:10.1038/ nrm2593)
10. Ochsner M, Textor M, Vogel V, Smith ML. 2010 Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape. PLoS ONE 5, e9445. (doi:10.1371/ journal.pone.0009445)
11. Bettinger CJ, Langer R, Borenstein JT. 2009 Engineering substrate topography at the micro-and nanoscale to control cell function. Angew. Chem. Int. Ed 48, 5406-5415. (doi:10.1002/anie.200805179)
12. Dertinger SKW, Jiang XY, Li ZY, Murthy VN, Whitesides GM. 2002 Gradients of substrate-bound laminin orient axonal specification of neurons. Proc. Natl Acad. Sci. USA 99, 12542-12547. (doi:10. 1073/pnas.192457199)
13. Cai K, Dong H, Chen C, Yang L, Jandt KD, Deng L. 2009 Inkjet printing of laminin gradient to investigate endothelial cellular alignment. Colloids Surf. B Biointerfaces 72, 230-235. (doi:10.1016/j. colsurfb.2009.04.008)
14. Liu L, Ratner BD, Sage EH, Jiang S. 2007 Endothelial cell migration on surface-density gradients of fibronectin, VEGF, or both proteins. Langmuir 23, 11 168-11 173. (doi:10.1021/la701435x)
15. Smith JT, Elkin JT, Reichert WM. 2006 Directed cell migration on fibronectin gradients: effect of gradient slope. Exp. Cell Res. 312, 2424-2432. (doi:10.1016/j.yexcr.2006.04.005)
16. DeLong SA, Moon JJ, West JL. 2005 Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration. Biomaterials 26, 3227-3234. (doi:10.1016/j.biomaterials.2004.09.021)
17. Sant S, Hancock MJ, Donnelly JP, Iyer D, Khademhosseini A. 2010 Biomimetic gradient hydrogels for tissue engineering. Can. J. Chem. Eng. 88, 899-911. (doi:10.1002/cjce.20411)
18. Ventre M, Valle F, Bianchi M, Biscarini F, Netti PA. 2012 Cell fluidics: producing cellular streams on micropatterned synthetic surfaces. Langmuir 28, 714-721. (doi:10.1021/la204144k)
19. Li GN, Liu J, Hoffman-Kim D. 2008 Multi-molecular gradients of permissive and inhibitory cues direct neurite outgrowth. Ann. Biomed. Eng. 36, 889-904. (doi:10.1007/s10439-008-9486-z)
20. Loschinger J, Weth F, Bonhoeffer F. 2000 Reading of concentration gradients by axonal growth cones. Phil. Trans. R. Soc. Lond. B 355, 971-982. (doi:10.1098/rstb.2000.0633)
21. Millet LJ, Stewart ME, Nuzzo RG, Gillette MU. 2010 Guiding neuron development with planar surface gradients of substrate cues deposited using microfluidic devices. Lab Chip 10, 1525-1535. (doi:10.1039/c001552k)
22. Fricke R, Zentis PD, Rajappa LT, Hofmann B, Banzet M, Offenhaeusser A, Meffert SH. 2011 Axon guidance of rat cortical neurons by microcontact printed gradients. Biomaterials 32, 2070-2076. (doi:10.1016/j.biomaterials.2010.11.036)
23. Gumera C, Rauck B, Wang Y. 2011 Materials for central nervous system regeneration: bioactive cues. J. Mater. Chem. 21, 7033-7051. (doi:10.1039/ c0jm04335d)
24. Cossetti C, Alfaro-Cervello C, Donega M, Tyzack G, Pluchino S. 2012 New perspectives of tissue remodelling with neural stem and progenitor cellbased therapies. Cell Tissue Res. 349, 321-329. (doi:10.1007/s00441-012-1341-8)
25. Pluchino S, Zanotti L, Brini E, Ferrari S, Martino G. 2009 Regeneration and repair in multiple sclerosis: the role of cell transplantation. Neurosci. Lett. 456, 101-106. (doi:10.1016/j.neulet.2008.03.097)
26. Jaerve A, Bosse F, Mueller HW. 2012 SDF-1/CXCL12: its role in spinal cord injury. Int. J. Biochem. Cell Biol. 44, 452-456. (doi:10.1016/j.biocel.2011. 11.023)
27. Gundersen RW. 1987 Response of sensory neurites and growth cones to patterned substrata of laminin and fibronectin in vitro. Dev. Biol. 121, 423-431. (doi:10.1016/0012-1606(87)90179-5)
28. Ichikawa N et al. 2005 Identification of neurite outgrowth active sites on the laminin alpha 4 chain G domain. Biochemistry 44, 5755-5762. (doi:10. 1021/bi0476228)
29. Edgar D, Timpl R, Thoenen H. 1984 The heparinbinding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J. 3, 1463-1468.
30. Bonner J, O'Connor TP. 2001 The permissive cue laminin is essential for growth cone turning in vivo. J. Neurosci. 21, 9782-9791.
31. Mammadov B, Mammadov R, Guler MO, Tekinay AB. 2012 Cooperative effect of heparan sulfate and laminin mimetic peptide nanofibers on the promotion of neurite outgrowth. Acta Biomater. 8, 2077-2086. (doi:10.1016/j.actbio.2012.02.006)
32. Saadi W, Wang SJ, Lin F, Jeon NL. 2006 A parallelgradient microfluidic chamber for quantitative analysis of breast cancer cell chemotaxis. Biomed. Microdevices 8, 109-118. (doi:10.1007/s10544-006-7706-6)
33. Gunawan RC, Silvestre J, Gaskins HR, Kenis PJA, Leckband DE. 2006 Cell migration and polarity on microfabricated gradients of extracellular matrix proteins. Langmuir 22, 4250-4258. (doi:10.1021/ la0531493)
34. Rosentreter SM, Davenport RW, Loschinger J, Huf J, Jung JG, Bonhoeffer F. 1998 Response of retinal ganglion cell axons to striped linear gradients of repellent guidance molecules. J. Neurobiol. 37, 541-562. (doi:10.1002/(SICI) 1097-4695(199812)37:4,541::AID-NEU4.3.0. CO;2-L)
35. Adams DN, Kao EYC, Hypolite CL, Distefano MD, Hu WS, Letourneau PC. 2005 Growth cones turn and migrate up an immobilized gradient of the laminin IKVAV peptide. J. Neurobiol. 62, 134-147. (doi:10. 1002/neu.20075)
36. Welle A, Horn S, Schimmelpfeng J, Kalka D. 2005 Photo-chemically patterned polymer surfaces for controlled PC-12 adhesion and neurite guidance. J. Neurosci. Methods 142, 243-250. (doi:10.1016/j. jneumeth.2004.08.011)
37. Belisle JM, Levin LA, Costantino S. 2012 Highcontent neurite development study using optically patterned substrates. PLoS ONE 7, e35911. (doi:10. 1371/journal.pone.0035911)
38. Tang X, Ali MY, Saif MTA. 2012 A novel technique for micro-patterning proteins and cells on polyacrylamide gels. Soft Matter 8, 7197-7206. (doi:10.1039/c2sm25533b)
39. Xia YN, Whitesides GM. 1998 Soft lithography. Angew. Chem. Int. Ed. 37, 551-575. (doi:10.1002/ (SICI)1521-3773(19980316)37:5,550::AIDANIE550.3.0. CO;2-G)
40. Pan T, Wang W. 2011 From cleanroom to desktop: emerging micro-nanofabrication technology for biomedical applications. Ann. Biomed. Eng. 39, 600-620. (doi:10.1007/s10439-010-0218-9)
41. Whitesides GM, Ostuni E, Takayama S, Jiang XY, Ingber DE. 2001 Soft lithography in biology and biochemistry. Annu. Rev. Biomed. Eng. 3, 335-373. (doi:10.1146/annurev.bioeng.3.1.335)
42. Valle F, Chelli B, Bianchi M, Greco P, Bystrenova E, Tonazzini I, Biscarini F. 2010 Stable non-covalent large area patterning of inert teflon-AF surface: a new approach to multiscale cell guidance. Adv. Eng. Mater. 12, B185-B191. (doi:10.1002/adem. 201080022)
43. Biscarini F, Bianchi M, Chelli B, Valle F, Dionigi C, Bystrenova E, Greco P. 2012 Unconventional multiscale patterning of titanium dioxide: a new tool for the investigation of cell-topography interactions. Adv. Eng. Mater. 14, B208-B215. (doi:10.1002/ adem.201180061)
44. Yang IH, Co CC, Ho CC. 2005 Alteration of human neuroblastoma cell morphology and neurite extension with micropatterns. Biomaterials 26, 6599-6609. (doi:10.1016/j.biomaterials.2005. 04.024)
45. Cavallini M, Gentili D, Greco P, Valle F, Biscarini F. 2012 Micro-and nanopatterning by lithographically controlled wetting. Nat. Protoc. 7, 1668-1676. (doi:10.1038/nprot.2012.094)
46. Dos Reis G et al. 2010 Direct microfabrication of topographical and chemical cues for the guided growth of neural cell networks on polyamidoamine hydrogels. Macromol. Biosci. 10, 842-852. (doi:10. 1002/mabi.200900410)
47. Eichinger CD, Hsiao TW, Hlady V. 2012 Multiprotein microcontact printing with micrometer resolution. Langmuir 28, 2238-2243. (doi:10.1021/la2039202)
48. Cavallini M, Albonetti C, Biscarini F. 2009 Nanopatterning soluble multifunctional materials by unconventional wet lithography. Adv. Mater. 21, 1043-1053. (doi:10.1002/adma.200801979)
49. Straley JP. 1974 Ordered phases of a liquid of biaxial particles. Phys. Rev. A 10, 1881-1887. (doi:10.1103/PhysRevA.10.1881)
50. Biscarini F, Greco O, Lauria A, Zamboni R, Taliani C. 1996 Orientational ordering of domains in vacuumgrown oligomer thin films: a scanning force microscopy study. Mol. Cryst. Liq. Cryst. Sci. Technol. A 290, 203-212. (doi:10.1080/10587 259608031906)
51. Rolli CG, Nakayama H, Yamaguchi K, Spatz JP, Kemkemer R, Nakanishi J. 2012 Switchable adhesive substrates: revealing geometry dependence in collective cell behavior. Biomaterials 33, 2409-2418. (doi:10.1016/j.biomaterials.2011.12.012)
52. Krsko P, McCann TE, Thach T-T, Laabs TL, Geller HM, Libera MR. 2009 Length-scale mediated adhesion and directed growth of neural cells by surfacepatterned poly(ethylene glycol) hydrogels. Biomaterials 30, 721-729. (doi:10.1016/j.bio materials.2008.10.011)
53. Curtis ASG, Forrester JV, McInnes C, Lawrie F. 1983 Adhesion of cells to polystyrene surfaces. J. Cell Biol. 97, 1500-1506. (doi:10.1083/jcb.97.5.1500)
54. Lakard S, Herlem G, Propper A, Kastner A, Michel G, Valles-Villarreal N, Gharbi T, Fahys B. 2004 Adhesion and proliferation of cells on new polymers modified biomaterials. Bioelectrochemistry 62, 19-27. (doi:10.1016/j.bioelechem.2003.09.009)
55. Hallab NJ, Bundy KJ, Oconnor K, Clark R, Moses RL. 1995 Cell adhesion to biomaterials: correlations between surface charge, surface roughness, adsorbed protein, and cell morphology. J. Long Term Eff. Med. Implants 5, 209-231.
56. Liu BF, Ma J, Xu QY, Cui FZ. 2006 Regulation of charged groups and laminin patterns for selective neuronal adhesion. Colloids Surf. B Biointerfaces 53, 175-178. (doi:10.1016/j.colsurfb.2006.08.018)
57. Blau A, Weinl C, Mack J, Kienle S, Jung G, Ziegler C. 2001 Promotion of neural cell adhesion by electrochemically generated and functionalized polymer films. J. Neurosci. Methods 112, 65-73. (doi:10.1016/S0165-0270(01)00458-7)
58. Baier H, Bonhoeffer F. 1992 Axon guidance by gradients of a target-derived component. Science 255, 472-475. (doi:10.1126/science.1734526)
59. Kam L, Boxer SG. 2000 Formation of supported lipid bilayer composition arrays by controlled mixing and surface capture. J. Am. Chem. Soc. 122, 12 901-12 902. (doi:10.1021/ja0034038)
60. Jeon NL, Dertinger SKW, Chiu DT, Choi IS, Stroock AD, Whitesides GM. 2000 Generation of solution and surface gradients using microfluidic systems. Langmuir 16, 8311-8316. (doi:10.1021/la000600b)