Extending neurites sense the depth of the underlying topography during neuronal differentiation and contact guidance

Biomaterials

Volumn 35, Issue 27, 2014, Pages 7750-7761

  Chua, Jie Shi ^a,b   Chng, Choon Peng ^c   Moe, Aung Aung Kywe ^a   Tann, Jason Y ^a,d   Goh, Eyleen L K ^a   Chiam, Keng Hwee ^b,c   Yim, Evelyn K F ^b,d,e  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c BIOINFORMATICS INSTITUTE   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Modelling; Nanotopography; Neural progenitor cells; Neural tissue engineering; Neuronal differentiation

Indexed keywords

ASPECT RATIO; CELL ENGINEERING; CELLS; CYTOLOGY; MICROOPTICS; MODELS; TISSUE ENGINEERING; TOPOGRAPHY;

CELL DIFFERENTIATION; EXTRACELLULAR MICROENVIRONMENT; NANOTOPOGRAPHIES; NEURAL PROGENITOR CELLS; NEURAL TISSUE ENGINEERING; NEURONAL DIFFERENTIATION; PATTERNED SURFACE; QUANTITATIVE MODELING;

NEURONS;

DIMETICONE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL ADHESION; CELL ELONGATION; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; CYTOSKELETON; EXPERIMENT; GRATING; GROWTH CONE; HIPPOCAMPUS; IMMUNOFLUORESCENCE; MEMBRANE STRUCTURE; MICROENVIRONMENT; MICROTUBULE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NEURITE; NONHUMAN; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SURFACE PROPERTY; ANIMAL; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECTS; METABOLISM; ULTRASTRUCTURE;

MURINAE;

ANIMALS; ASTROCYTES; CELL COMMUNICATION; CELL DIFFERENTIATION; DIMETHYLPOLYSILOXANES; HIPPOCAMPUS; MICE; MODELS, BIOLOGICAL; NEURAL STEM CELLS; NEURITES;

EID: 84903442153     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.06.008     Document Type: Article

References (56)

1. Okano H. Stem cell biology of the central nervous system. JNeurosci Res 2002, 69:698-707.
2. Ogawa Y., Sawamoto K., Miyata T., Miyao S., Watanabe M., Nakamura M., et al. Transplantation of invitro-expanded fetal neural progenitor cells results in neurogenesis and functional recovery after spinal cord contusion injury in adult rats. JNeurosci Res 2002, 69:925-933.
3. Iwanami A., Kaneko S., Nakamura M., Kanemura Y., Mori H., Kobayashi S., et al. Transplantation of human neural stem cells for spinal cord injury in primates. JNeurosci Res 2005, 80:182-190.
4. Kim S.U., de Vellis J. Stem cell-based cell therapy in neurological diseases: a review. JNeurosci Res 2009, 87:2183-2200.
5. Rossi F., Cattaneo E. Neural stem cell therapy for neurological diseases: dreams and reality. Nat Rev Neurosci 2002, 3:401-409.
6. Malatesta P., Appolloni I., Calzolari F. Radial glia and neural stem cells. Cell Tissue Res 2008, 331:165-178.
7. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001, 409:714-720.
8. Griffin J.W., Thompson W.J. Biology and pathology of nonmyelinating Schwann cells. Glia 2008, 56:1518-1531.
9. Dowell-Mesfin N.M., Abdul-Karim M.A., Turner A.M.P., Schanz S., Craighead H.G., Roysam B., et al. Topographically modified surfaces affect orientation and growth of hippocampal neurons. JNeural Eng 2004, 1:78-90.
10. Hanson J.N., Motala M.J., Heien M.L., Gillette M., Sweedler J., Nuzzo R.G. Textural guidance cues for controlling process outgrowth of mammalian neurons. Lab Chip 2009, 9:122-131.
11. Clark P., Connolly P., Curtis A.S., Dow J.A., Wilkinson C.D. Topographical control of cell behaviour: II. Multiple grooved substrata. Development 1990, 108:635-644.
12. Nagata I., Kawana A., Nakatsuji N. Perpendicular contact guidance of CNS neuroblasts on artificial microstructures. Development 1993, 117:401-408.
13. Rajnicek A., Britland S., McCaig C. Contact guidance of CNS neurites on grooved quartz: influence of groove dimensions, neuronal age and cell type. JCell Sci 1997, 110(Pt 23):2905-2913.
14. Mahoney M.J., Chen R.R., Tan J., Saltzman W.M. The influence of microchannels on neurite growth and architecture. Biomaterials 2005, 26:771-778.
15. Johansson F., Carlberg P., Danielsen N., Montelius L., Kanje M. Axonal outgrowth on nano-imprinted patterns. Biomaterials 2006, 27:1251-1258.
16. Gomez N., Chen S., Schmidt C.E. Polarization of hippocampal neurons with competitive surface stimuli: contact guidance cues are preferred over chemical ligands. JR Soc Interface 2007, 4:223-233.
17. Cecchini M., Ferrari A., Beltram F. PC12 polarity on biopolymer nanogratings. JPhys Conf Ser 2008, 100:012003.
18. Morelli S., Salerno S., Piscioneri A., Papenburg B.J., Di Vito A., Giusi G., et al. Influence of micro-patterned PLLA membranes on outgrowth and orientation of hippocampal neurites. Biomaterials 2010, 31:7000-7011.
19. Béduer A., Vieu C., Arnauduc F., Sol J.-C.C., Loubinoux I., Vaysse L. Engineering of adult human neural stem cells differentiation through surface micropatterning. Biomaterials 2012, 33:504-514.
20. Schnell E., Klinkhammer K., Balzer S., Brook G., Klee D., Dalton P., et al. Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-epsilon-caprolactone and a collagen/poly-epsilon-caprolactone blend. Biomaterials 2007, 28:3012-3025.
21. Silva G.A., Czeisler C., Niece K.L., Beniash E., Harrington D.A., Kessler J.A., et al. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 2004, 303:1352-1355.
22. Recknor J.B., Sakaguchi D.S., Mallapragada S.K. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 2006, 27:4098-4108.
23. Walsh J.F., Manwaring M.E., Tresco P.A. Directional neurite outgrowth is enhanced by engineered meningeal cell-coated substrates. Tissue Eng 2005, 11:1085-1094.
24. Gomez N., Lu Y., Chen S., Schmidt C.E. Immobilized nerve growth factor and microtopography have distinct effects on polarization versus axon elongation in hippocampal cells in culture. Biomaterials 2007, 28:271-284.
25. Moe A.A.K., Suryana M., Marcy G., Keat S., Ankam S., Wen J.Z., et al. Microarray with micro- and nano-topographies enables identification of the optimal topography for directing the differentiation of primary murine neural progenitor cells. Small 2012, 8:3050-3061.
26. Yang F., Murugan R., Wang S., Ramakrishna S. Electrospinning of nano/micro scale poly(L-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 2005, 26:2603-2610.
27. Qi L., Li N., Huang R., Song Q., Wang L., Zhang Q., et al. The effects of topographical patterns and sizes on neural stem cell behavior. PLoS ONE 2013, 8:e59022.
28. Bedi R.S., Beving D.E., Zanello L.P., Yan Y. Biocompatibility of corrosion-resistant zeolite coatings for titanium alloy biomedical implants. Acta Biomater 2009, 5:3265-3271.
29. Bedi R.S., Chow G., Wang J., Zanello L., Yan Y.S. Bioactive materials for regenerative medicine: zeolite-hydroxyapatite bone mimetic coatings. Adv Eng Mater 2012, 14:200-206.
30. Flanagan L.A., Rebaza L.M., Derzic S., Schwartz P.H., Monuki E.S. Regulation of human neural precursor cells by laminin and integrins. JNeurosci Res 2006, 83:845-856.
31. Ankam S., Suryana M., Chan L.Y., Kywe A.A., Teo B.K., Law J.B., et al. Substrate topography and size determine the fate of human embryonic stem cells to neuronal or glial lineage. Acta Biomater 2013, 9:4535-4545.
32. Buettner H.M., Pittman R.N., Ivins J.K. Amodel of neurite extension across regions of nonpermissive substrate: simulations based on experimental measurement of growth cone motility and filopodial dynamics. Dev Biol 1994, 163:407-422.
33. Conde C., Cáceres A. Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 2009, 10:319-332.
34. Costa L.D.F., Manoel E.T.M., Faucereau F., Chelly J., van Pelt J., Ramakers G. Ashape analysis framework for neuromorphometry. Network 2002, 13:283-310.
35. Hjorth J.J., van Pelt J., Mansvelder H.D., van Ooyen A. Competitive dynamics during resource-driven neurite outgrowth. PLoS ONE 2014, 9:e86741.
36. Curtis A., Wilkinson C. Topographical control of cells. Biomaterials 1997, 18:1573-1583.
37. Crouch A.S., Miller D., Luebke K.J., Hu W. Correlation of anisotropic cell behaviors with topographic aspect ratio. Biomaterials 2009, 30:1560-1567.
38. Biela S.A., Su Y., Spatz J.P., Kemkemer R. Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater 2009, 5:2460-2466.
39. Ferrari A., Cecchini M., Dhawan A., Micera S., Tonazzini I., Stabile R., et al. Nanotopographic control of neuronal polarity. Nano Lett 2011, 11:505-511.
40. Franco D., Klingauf M., Bednarzik M., Cecchini M., Kurtcuoglu V., Gobrecht J., et al. Control of initial endothelial spreading by topographic activation of focal adhesion kinase. Soft Matter 2011, 7:7313-7324.
41. Miller C., Jeftinija S., Mallapragada S. Synergistic effects of physical and chemical guidance cues on neurite alignment and outgrowth on biodegradable polymer substrates. Tissue Eng 2002, 8:367-378.
42. Clark P., Connolly P., Curtis A.S., Dow J.A., Wilkinson C.D. Topographical control of cell behaviour. I. Simple step cues. Development 1987, 99:439-448.
43. Dunn G.A., Heath J.P. Anew hypothesis of contact guidance in tissue cells. Exp Cell Res 1976, 101:1-14.
44. Betz T., Koch D., Lu Y.-B., Franze K., Käs J.A. Growth cones as soft and weak force generators. Proc Natl Acad Sci USA 2011, 108:13420-13425.
45. Zhou F.-Q., Cohan C.S. How actin filaments and microtubules steer growth cones to their targets. JNeurobiol 2004, 58:84-91.
46. Ferrari A., Cecchini M., Serresi M., Faraci P., Pisignano D., Beltram F. Neuronal polarity selection by topography-induced focal adhesion control. Biomaterials 2010, 31:4682-4694.
47. Chan L.Y., Birch W.R., Yim E.K., Choo A.B. Temporal application of topography to increase the rate of neural differentiation from human pluripotent stem cells. Biomaterials 2013, 34:382-392.
48. Lee M.R.R., Kwon K.W.W., Jung H., Kim H.N.N., Suh K.Y., Kim K., et al. Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. Biomaterials 2010, 31:4360-4366.
49. Yim E.K., Pang S.W., Leong K.W. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 2007, 313:1820-1829.
50. Kim S.-J.J., Kyoo J., Won J., Jung J.-W.W., Seo K., Park S.-B.B., et al. Surface modification of polydimethylsiloxane (PDMS) induced proliferation and neural-like cells differentiation of umbilical cord blood-derived mesenchymal stem cells. JMater Sci Mater Med 2008, 19:2953-2962.
51. Dalby M.J., Riehle M.O., Sutherland D.S., Agheli H., Curtis A.S.G. Morphological and microarray analysis of human fibroblasts cultured on nanocolumns produced by colloidal lithography. Eur Cell Mater 2005, 9:1-8.
52. Vogel V., Sheetz M. Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 2006, 7:265-275.
53. Teo B.K., Wong S.T., Lim C.K., Kung T.Y.S., Yap C.H., Ramagopal Y., et al. Nanotopography modulates mechanotransduction of stem cells and induces differentiation through focal adhesion kinase. ACS Nano 2013, 7:4785-4798.
54. Valiente M., Ciceri G., Rico B., Marín O. Focal adhesion kinase modulates radial glia-dependent neuronal migration through connexin-26. JNeurosci 2011, 31:11678-11691.
55. Thomas C.H., Collier J.H., Sfeir C.S., Healy K.E. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc Natl Acad Sci USA 2002, 99:1972-1977.
56. McBride S.H., Knothe Tate M.L. Modulation of stem cell shape and fate A: the role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng Part A 2008, 14:1561-1572.