Mechanosensing is critical for axon growth in the developing brain

Nature Neuroscience

Volumn 19, Issue 12, 2016, Pages 1592-1598

  Koser, David E ^a,d   Thompson, Amelia J ^a   Foster, Sarah K ^a   Dwivedy, Asha ^a   Pillai, Eva K ^a   Sheridan, Graham K ^a,e   Svoboda, Hanno ^a,f   Viana, Matheus ^b   Costa, Luciano Da F ^b   Guck, Jochen ^c,g   Holt, Christine E ^a   Franze, Kristian ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e UNIVERSITY OF BRIGHTON   (United Kingdom)

^f F HOFFMANN LA ROCHE LTD   (Switzerland)

^g DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL; ION CHANNEL PIEZO1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN STIFFNESS; BRAIN TISSUE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; IN VITRO STUDY; IN VIVO STUDY; MECHANOTRANSDUCTION; NERVE FIBER GROWTH; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RETINA GANGLION CELL; XENOPUS; ANIMAL; AXON; BRAIN; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PATHOLOGY; PHYSIOLOGY; RETINA; VISUAL SYSTEM; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALS; AXONS; BRAIN; MECHANOTRANSDUCTION, CELLULAR; NEUROGENESIS; RETINA; RETINAL GANGLION CELLS; VISUAL PATHWAYS; XENOPUS LAEVIS; ZEBRAFISH;

EID: 84988420007     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4394     Document Type: Article

References (60)

1. Sperry, R. W. Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50, 703-710 (1963).
2. Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123-1133 (1996).
3. Erskine, L. & Herrera, E. The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev. Biol. 308, 1-14 (2007).
4. Campbell, D. S. et al. Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547 (2001).
5. Piper, M. et al. Signaling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49, 215-228 (2006).
6. Atkinson-Leadbeater, K. et al. Dynamic expression of axon guidance cues required for optic tract development is controlled by fibroblast growth factor signaling. J. Neurosci. 30, 685-693 (2010).
7. Chan, C. E. & Odde, D. J. Traction dynamics of filopodia on compliant substrates. Science 322, 1687-1691 (2008).
8. Moore, S. W., Biais, N. & Sheetz, M. P. Traction on immobilized netrin-1 is sufficient to reorient axons. Science 325, 166 (2009).
9. 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 108, 13420-13425 (2011).
10. Koch, D., Rosoff, W. J., Jiang, J., Geller, H. M. & Urbach, J. 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).
11. Weiss, P. In vitro experiments on the factors determining the course of the outgrowing nerve fiber. J. Exp. Zool. 68, 393-448 (1934).
12. Flanagan, L. A., Ju, Y. E., Marg, B., Osterfield, M. & Janmey, P. A. Neurite branching on deformable substrates. Neuroreport 13, 2411-2415 (2002).
13. 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).
14. Kostic, A., Sap, J. & Sheetz, M. P. RPTPalpha is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J. Cell Sci. 120, 3895-3904 (2007).
15. Jiang, F. X., Yurke, B., Schloss, R. S., Firestein, B. L. & Langrana, N. A. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng. Part A 16, 1873-1889 (2010).
16. Balgude, A. P., Yu, X., Szymanski, A. & Bellamkonda, R. V. Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 22, 1077-1084 (2001).
17. Elkin, B. S., Azeloglu, E. U., Costa, K. D. & Morrison, B. III. Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J. Neurotrauma 24, 812-822 (2007).
18. Christ, A. F. et al. Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J. Biomech. 43, 2986-2992 (2010).
19. Franze, K. et al. Spatial mapping of the mechanical properties of the living retina using scanning force microscopy. Soft Matter 7, 3147-3154 (2011).
20. Iwashita, M., Kataoka, N., Toida, K. & Kosodo, Y. Systematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain. Development 141, 3793-3798 (2014).
21. Elkin, B. S., Ilankovan, A. & Morrison, B. III. Age-dependent regional mechanical properties of the rat hippocampus and cortex. J. Biomech. Eng. 132, 011010 (2010).
22. Koser, D. E., Moeendarbary, E., Hanne, J., Kuerten, S. & Franze, K. CNS cell distribution and axon orientation determine local spinal cord mechanical properties. Biophys. J. 108, 2137-2147 (2015).
23. Weickenmeier, J. et al. Brain stiffness increases with myelin content. Acta Biomater. 42, 265-272 (2016).
24. Moshayedi, P. et al. Mechanosensitivity of astrocytes on optimized polyacrylamide gels analyzed by quantitative morphometry. J. Phys. Condens. Matter 22, 194114 (2010).
25. Franze, K., Janmey, P. A. & Guck, J. Mechanics in neuronal development and repair. Annu. Rev. Biomed. Eng. 15, 227-251 (2013).
26. Guan, W., Puthenveedu, M. A. & Condic, M. L. Sensory neuron subtypes have unique substratum preference and receptor expression before target innervation. J. Neurosci. 23, 1781-1791 (2003).
27. Franze, K. et al. Neurite branch retraction is caused by a threshold-dependent mechanical impact. Biophys. J. 97, 1883-1890 (2009).
28. Kerstein, P. C. et al. Mechanosensitive TRPC1 channels promote calpain proteolysis of talin to regulate spinal axon outgrowth. J. Neurosci. 33, 273-285 (2013).
29. Zhang, Q. Y. et al. Stiff substrates enhance cultured neuronal network activity. Sci. Rep. 4, 6215 (2014).
30. Shibasaki, K., Murayama, N., Ono, K., Ishizaki, Y. & Tominaga, M. TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. J. Neurosci. 30, 4601-4612 (2010).
31. Pathak, M. M. et al. Stretch-activated ion channel Piezo1 directs lineage choice in human neural stem cells. Proc. Natl. Acad. Sci. USA 111, 16148-16153 (2014).
32. Coste, B. et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60 (2010).
33. Coste, B. et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483, 176-181 (2012).
34. Kim, S. E., Coste, B., Chadha, A., Cook, B. & Patapoutian, A. The role of Drosophila Piezo in mechanical nociception. Nature 483, 209-212 (2012).
35. Li, J. et al. Piezo1 integration of vascular architecture with physiological force. Nature 515, 279-282 (2014).
36. Gottlieb, P. A. & Sachs, F. Piezo1: properties of a cation selective mechanical channel. Channels (Austin) 6, 214-219 (2012).
37. Kanekar, S. et al. Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron. 19, 981-994 (1997).
38. Swift, J. et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
39. Majkut, S. et al. Heart-specific stiffening in early embryos parallels matrix and myosin expression to optimize beating. Curr. Biol. 23, 2434-2439 (2013).
40. Walz, A., Anderson, R. B., Irie, A., Chien, C. B. & Holt, C. E. Chondroitin sulfate disrupts axon pathfinding in the optic tract and alters growth cone dynamics. J. Neurobiol. 53, 330-342 (2002).
41. Pogoda, K. et al. Compression stiffening of brain and its effect on mechanosensing by glioma cells. New J. Phys. 16, 075002 (2014).
42. Lo, C. M., Wang, H. B., Dembo, M. & Wang, Y. L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152 (2000).
43. Isenberg, B. C., Dimilla, P. A., Walker, M., Kim, S. & Wong, J. Y. Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97, 1313-1322 (2009).
44. Bollmann et al. Microglia mechanics: immune activation alters traction forces and durotaxis. Front. Cell Neurosci. 9, 363 (2015).
45. Xu, G. et al. Opening angles and material properties of the early embryonic chick brain. J. Biomech. Eng. 132, 011005 (2010).
46. Franze, K. The mechanical control of nervous system development. Development 140, 3069-3077 (2013).
47. Singh, T., Meena, R. & Kumar, A. Effect of sodium sulfate on the gelling behavior of agarose and water structure inside gel networks. J. Phys. Chem. B 113, 2519-2525 (2009).
48. Höpker, V. H., Shewan, D., Tessier-Lavigne, M., Poo, M. & Holt, C. Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401, 69-73 (1999).
49. Nieuwkoop, P. D. & Faber, J. Normal table of Xenopus laevis (Daudin): a Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis (North-Holland Pub. Co., 1967).
50. Das, T., Payer, B., Cayouette, M. & Harris, W. A. In vivo time-lapse imaging of cell divisions during neurogenesis in the developing zebrafish retina. Neuron 37, 597-609 (2003).
51. Chien, C. B., Rosenthal, D. E., Harris, W. A. & Holt, C. E. Navigational errors made by growth cones without filopodia in the embryonic Xenopus brain. Neuron 11, 237-251 (1993).
52. Leung, K. M. et al. Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247-1256 (2009).
53. Kalous, A., Stake, J. I., Yisraeli, J. K. & Holt, C. E. RNA-binding protein Vg1RBP regulates terminal arbor formation but not long-range axon navigation in the developing visual system. Dev. Neurobiol. 74, 303-318 (2014).
54. Wizenmann, A. et al. Extracellular Engrailed participates in the topographic guidance of retinal axons in vivo. Neuron 64, 355-366 (2009).
55. Hutter, J. L. & Bechhoefer, J. Calibration of atomic-force microscope tips. Rev. Sci. Instrum. 64, 1868-1873 (1993).
56. Mahaffy, R. E., Shih, C. K., MacKintosh, F. C. & Käs, J. Scanning probe-based frequency-dependent microrheology of polymer gels and biological cells. Phys. Rev. Lett. 85, 880-883 (2000).
57. Franze, K. Atomic force microscopy and its contribution to understanding the development of the nervous system. Curr. Opin. Genet. Dev. 21, 530-537 (2011).
58. Sholl, D. A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87, 387-406 (1953).
59. Hertz, H. Über die Berührung fester elastischer Körper. J. Reine Angew. Math. 92, 156-171 (1881).
60. Tamada, A., Kawase, S., Murakami, F. & Kamiguchi, H. Autonomous right-screw rotation of growth cone filopodia drives neurite turning. J. Cell Biol. 188, 429-441 (2010).