Low piconewton towing of CNS axons against diffusing and surface-bound repellents requires the inhibition of motor protein-associated pathways

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Kilinc, Devrim ^a   Blasiak, Agata ^a   O'Mahony, James J ^a   Lee, Gil U ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; AMIDE; CHONDROITIN SULFATE; MOLECULAR MOTOR; PYRIDINE DERIVATIVE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SEMAPHORIN 3A;

ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL CULTURE; CENTRAL NERVOUS SYSTEM; CHEMISTRY; CYTOLOGY; DIFFUSION; DRUG EFFECTS; METABOLISM; MICROFLUIDIC ANALYSIS; MOUSE; NERVE CELL; NERVE FIBER; PHYSIOLOGY;

AMIDES; ANIMALS; AXONS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; CHONDROITIN SULFATES; DIFFUSION; MICE; MICROFLUIDIC ANALYTICAL TECHNIQUES; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; NEURONS; PYRIDINES; RHOA GTP-BINDING PROTEIN; SEMAPHORIN-3A;

EID: 84934778612     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07128     Document Type: Article

References (58)

1. Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
2. Kalil, K. & Dent, E. W. Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr Opin Neurobiol 15, 521-526 (2005).
3. Suter, D. M. & Miller, K. E. The emerging role of forces in axonal elongation. Prog Neurobiol 94, 91-101 (2011).
4. Franze, K. The mechanical control of nervous system development. Development 140, 3069-3077 (2013).
5. Lamoureux, P., Buxbaum, R. E. & Heidemann, S. R. Direct evidence that growth cones pull. Nature 340, 159-162 (1989).
6. Suter, D. M. & Forscher, P. Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J Cell Biol 155, 427-438 (2001).
7. Schaefer, A. W. et al. Coordination of actin filament and microtubule dynamics during neurite outgrowth. Dev Cell 15, 146-162 (2008).
8. Bray, D. Axonal growth in response to experimentally applied mechanical tension. Dev Biol 102, 379-389 (1984).
9. Chada, S., Lamoureux, P., Buxbaum, R. E. & Heidemann, S. R. Cytomechanics of neurite outgrowth from chick brain neurons. J Cell Sci 110, 1179-1186 (1997).
10. Fass, J. N. & Odde, D. J. Tensile force-dependent neurite elicitation via anti-beta1 integrin antibody-coated magnetic beads. Biophys J 85, 623-636 (2003).
11. Lamoureux, P., Zheng, J., Buxbaum, R. E. & Heidemann, S. R. A cytomechanical investigation of neurite growth on different culture surfaces. J Cell Biol 118, 655-661 (1992).
12. Kilinc, D. & Lee, G. U. Advances in magnetic tweezers for single molecule and cell biophysics. Integr Biol (Camb) 6, 27-34 (2014).
13. Polleux, F., Giger, R. J., Ginty, D. D., Kolodkin, A. L. & Ghosh, A. Patterning of Cortical Efferent Projections by Semaphorin-Neuropilin Interactions. Science 282, 1904-1906 (1998).
14. Gallo, G. RhoA-kinase coordinates F-actin organization and myosin II activity during semaphorin-3A-induced axon retraction. J Cell Sci 119, 3413-3423 (2006).
15. Campbell, D. S. & Holt, C. E. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026 (2001).
16. Kaczmarek, J. S., Riccio, A. & Clapham, D. E. Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc Natl Acad Sci U S A 109, 7888-7892 (2012).
17. Silver, L., Michael, J. V., Goldfinger, L. E. & Gallo, G. Activation of PI3K and R-Ras signaling promotes the extension of sensory axons on inhibitory Chondroitin sulfate proteoglycans. Dev Neurobiol 74, 918-933 (2014).
18. Tan, C. L. et al. Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31, 6289-6295 (2011).
19. Borisoff, J. F. et al. Suppression of Rho-kinase activity promotes axonal growth on inhibitory CNS substrates. Mol Cell Neurosci 22, 405-416 (2003).
20. Dergham, P. et al. Rho signaling pathway targeted to promote spinal cord repair. J Neurosci 22, 6570-6577 (2002).
21. Hur, E. M. et al. Engineering neuronal growth cones to promote axon regeneration over inhibitory molecules. Proc Natl Acad Sci U S A 108, 5057-5062 (2011).
22. Lin, S. et al. Inhibition of Kinesin-5, a microtubule-based motor protein, as a strategy for enhancing regeneration of adult axons. Traffic 12, 269-286 (2011).
23. Pasterkamp, R. J. et al. Expression of the gene encoding the chemorepellent semaphorin III is induced in the fibroblast component of neural scar tissue formed following injuries of adult but not neonatal CNS. Mol Cell Neurosci 13, 143-166 (1999).
24. Bartus, K., James, N. D., Bosch, K. D. & Bradbury, E. J. Chondroitin sulphate proteoglycans: key modulators of spinal cord and brain plasticity. Exp Neurol 235, 5-17 (2012).
25. Rosoff, W. J. et al. A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients. Nat Neurosci 7, 678-682 (2004).
26. Li Jeon, N. et al. Neutrophil chemotaxis in linear and complex gradients of interleukin-8 formed in a microfabricated device. Nat Biotechnol 20, 826-830 (2002).
27. Bhattacharjee, N., Li, N., Keenan, T. M. & Folch, A. A neuron-benign microfluidic gradient generator for studying the response of mammalian neurons towards axon guidance factors. Integr Biol (Camb) 2, 669-679 (2010).
28. Taylor, A. M. et al. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2, 599-605 (2005).
29. Taylor, A. M., Dieterich, D. C., Ito, H. T., Kim, S. A. & Schuman, E. M. Microfluidic local perfusion chambers for the visualization and manipulation of synapses. Neuron 66, 57-68 (2010).
30. Shang, H. & Lee, G. U. Magnetic tweezers measurement of the bond lifetime-force behavior of the IgG-protein A specific molecular interaction. J Am Chem Soc 129, 6640-6646 (2007).
31. Snow, D. M., Smith, J. D., Cunningham, A. T., McFarlin, J. & Goshorn, E. C. Neurite elongation on chondroitin sulfate proteoglycans is characterized by axonal fasciculation. Exp Neurol 182, 310-321 (2003).
32. Bridgman, P. C., Dave, S., Asnes, C. F., Tullio, A. N. & Adelstein, R. S. Myosin IIB is required for growth cone motility. J Neurosci 21, 6159-6169 (2001).
33. 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 28, 271-284 (2007).
34. Kundu, A. et al. Superimposed topographic and chemical cues synergistically guide neurite outgrowth. Lab Chip 13, 3070-3081 (2013).
35. O'Mahony, J. J., Platt, M., Kilinc, D. & Lee, G. Synthesis of superparamagnetic particles with tunable morphologies: the role of nanoparticle-nanoparticle interactions. Langmuir 29, 2546-2553 (2013).
36. Li, P., Kilinc, D., Ran, Y. F. & Lee, G. U. Flow enhanced non-linear magnetophoretic separation of beads based on magnetic susceptibility. Lab Chip 13, 4400-4408 (2013).
37. Lamoureux, P., Altun-Gultekin, Z. F., Lin, C., Wagner, J. A. & Heidemann, S. R. Rac is required for growth cone function but not neurite assembly. J Cell Sci 110, 635-641 (1997).
38. Betz, T., Koch, D., Lu, Y. B., Franze, K. & Kas, J. A. Growth cones as soft and weak force generators. Proc Natl Acad Sci U S A 108, 13420-13425 (2011).
39. Costa, K. D. Single-cell elastography: probing for disease with the atomic force microscope. Dis Markers 19, 139-154 (2003).
40. Koch, D., Rosoff William, J., Jiang, J., Geller Herbert, M. & Urbach Jeffrey, S. Strength in the Periphery: Growth Cone Biomechanics and Substrate Rigidity Response in Peripheral and Central Nervous System Neurons. Biophys J 102, 452-460 (2012).
41. Odde, D. J., Tanaka, E. M., Hawkins, S. S. & Buettner, H. M. Stochastic dynamics of the nerve growth cone and its microtubules during neurite outgrowth. Biotechnol Bioeng 50, 452-461 (1996).
42. Fournier, A. E., Takizawa, B. T. & Strittmatter, S. M. Rho kinase inhibition enhances axonal regeneration in the injured CNS. J Neurosci 23, 1416-1423 (2003).
43. Lingor, P. et al. Inhibition of Rho kinase (ROCK) increases neurite outgrowth on chondroitin sulphate proteoglycan in vitro and axonal regeneration in the adult optic nerve in vivo. J Neurochem 103, 181-189 (2007).
44. Ahmed, Z., Berry, M. & Logan, A. ROCK inhibition promotes adult retinal ganglion cell neurite outgrowth only in the presence of growth promoting factors. Mol Cell Neurosci 42, 128-133 (2009).
45. Deleglise, B. et al. Synapto-Protective Drugs Evaluation in Reconstructed Neuronal Network. PLoS ONE 8, e71103 (2013).
46. Kilinc, D. et al. Wallerian-like degeneration of central neurons after synchronized and geometrically registered mass axotomy in a three-compartmental microfluidic chip. Neurotox Res 19, 149-161 (2011).
47. Shamloo, A., Ma, N., Poo, M. M., Sohn, L. L. & Heilshorn, S. C. Endothelial cell polarization and chemotaxis in a microfluidic device. Lab Chip 8, 1292-1299 (2008).
48. Horner, P. J. & Gage, F. H. Regenerating the damaged central nervous system. Nature 407, 963-970 (2000).
49. Li, C., Bassell, G. J. & Sasaki, Y. Fragile X Mental Retardation Protein is Involved in Protein Synthesis-Dependent Collapse of Growth Cones Induced by Semaphorin-3A. Front Neural Circuits 3, 11 (2009).
50. Qin, Q., Liao, G., Baudry, M. & Bi, X. Role of calpain-mediated p53 truncation in semaphorin 3A-induced axonal growth regulation. Proc Natl Acad Sci U S A 107, 13883-13887 (2010).
51. Nadar, V. C., Lin, S. & Baas, P. W. Microtubule redistribution in growth cones elicited by focal inactivation of kinesin-5. J Neurosci 32, 5783-5794 (2012).
52. David, S. & Aguayo, A. J. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933 (1981).
53. Shoichet, M. S., Tate, C. C., Baumann, M. D. & LaPlaca, M. C. Strategies for regeneration and repair in the injured central nervous system environment. Indwelling Neural Implants: Strategies for Contending with the In Vivo Environment Reichert, W. M. (ed.) (CRC Press, Boca Raton, FL, 2008).
54. McCreedy, D. A. & Sakiyama-Elbert, S. E. Combination therapies in the CNS: engineering the environment. Neurosci Lett 519, 115-121 (2012).
55. Pfister, B. J., Iwata, A., Meaney, D. F. & Smith, D. H. Extreme stretch growth of integrated axons. J Neurosci 24, 7978-7983 (2004).
56. Huang, J. H. et al. Long-term survival and integration of transplanted engineered nervous tissue constructs promotes peripheral nerve regeneration. Tissue Eng Part A 15, 1677-1685 (2009).
57. Polyak, B. et al. High field gradient targeting of magnetic nanoparticle-loaded endothelial cells to the surfaces of steel stents. Proc Natl Acad Sci U S A 105, 698-703 (2008).
58. Kilinc, D., Blasiak, A., O'Mahony, J. J., Suter, D. M. & Lee, G. U. Magnetic tweezers-based force clamp reveals mechanically distinct apCAM domain interactions. Biophys J 103, 1120-1129 (2012).