Promoting filopodial elongation in neurons by membrane-bound magnetic nanoparticles

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 11, Issue 3, 2015, Pages 559-567

  Pita Thomas, Wolfgang ^a,b   Steketee, Michael B ^a,c   Moysidis, Stavros N ^a   Thakor, Kinjal ^a   Hampton, Blake ^a   Goldberg, Jeffrey L ^a,d  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c MCGOWAN INSTITUTE FOR REGENERATIVE MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Axon growth; Filopodia; Mechanical tension; Nanoparticles

Indexed keywords

NANOPARTICLES; NEURONS; PROTEINS;

ACTIN POLYMERIZATION; AXON GROWTH; FILOPODIA; FUTURE APPLICATIONS; MAGNETIC NANO-PARTICLES; MECHANICAL TENSION; RETINAL GANGLION CELLS; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLES;

NANOMAGNETICS;

INTEGRIN; INTEGRIN RECEPTOR; LAMININ; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE; MAGNETITE NANOPARTICLE;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL MIGRATION; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; FILOPODIUM; FORCE; GROWTH CONE; HYDRODYNAMICS; MAGNETIC FIELD; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; RAT; RETINA GANGLION CELL; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; METABOLISM; PSEUDOPODIUM; SPRAGUE DAWLEY RAT;

ANIMALS; CELLS, CULTURED; GROWTH CONES; MAGNETIC FIELDS; MAGNETITE NANOPARTICLES; PSEUDOPODIA; RATS; RATS, SPRAGUE-DAWLEY; RETINAL GANGLION CELLS;

EID: 84933524567     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2014.11.011     Document Type: Article

References (50)

1. Goldberg J.L., Klassen M.P., Hua Y., Barres B.A. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 2002, 296(5574):1860-1864.
2. Canty A.J., Huang L., Jackson J.S., Little G.E., Knott G., Maco B., et al. In-vivo single neuron axotomy triggers axon regeneration to restore synaptic density in specific cortical circuits. Nat Commun 2013, 4:2038.
3. Goldberg J.L., Espinosa J.S., Xu Y., Davidson N., Kovacs G.T., Barres B.A. Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 2002, 33(5):689-702.
4. So K.F., Aguayo A.J. Lengthy regrowth of cut axons from ganglion cells after peripheral nerve transplantation into the retina of adult rats. Brain Res 1985, 328(2):349-354.
5. Caroni P., Schwab M.E. Antibody against myelin-associated inhibitor of neurite growth neutralizes nonpermissive substrate properties of CNS white matter. Neuron 1988, 1(1):85-96.
6. Savio T., Schwab M.E. Lesioned corticospinal tract axons regenerate in myelin-free rat spinal cord. Proc Natl Acad Sci U S A 1990, 87(11):4130-4133.
7. Fawcett J.W., Asher R.A. The glial scar and central nervous system repair. Brain Res Bull 1999, 49(6):377-391.
8. Yin Y., Henzl M.T., Lorber B., Nakazawa T., Thomas T.T., Jiang F., et al. Oncomodulin is a macrophage-derived signal for axon regeneration in retinal ganglion cells. Nat Neurosci 2006, 9(6):843-852.
9. Leibinger M., Muller A., Andreadaki A., Hauk T.G., Kirsch M., Fischer D. Neuroprotective and axon growth-promoting effects following inflammatory stimulation on mature retinal ganglion cells in mice depend on ciliary neurotrophic factor and leukemia inhibitory factor. J Neurosci 2009, 29(45):14334-14341.
10. Mansour-Robaey S., Clarke D.B., Wang Y.C., Bray G.M., Aguayo A.J. Effects of ocular injury and administration of brain-derived neurotrophic factor on survival and regrowth of axotomized retinal ganglion cells. Proc Natl Acad Sci U S A 1994, 91(5):1632-1636.
11. Ellis-Behnke R.G., Liang Y.X., You S.W., Tay D.K., Zhang S., So K.F., et al. Nano neuro knitting: peptide nanofiber scaffold for brain repair and axon regeneration with functional return of vision. Proc Natl Acad Sci U S A 2006, 103(13):5054-5059.
12. Tysseling-Mattiace V.M., Sahni V., Niece K.L., Birch D., Czeisler C., Fehlings M.G., et al. Self-assembling nanofibers inhibit glial scar formation and promote axon elongation after spinal cord injury. J Neurosci 2008, 28(14):3814-3823.
13. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., et al. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322(5903):963-966.
14. Neumann S., Woolf C.J. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 1999, 23(1):83-91.
15. Sun F., Park K.K., Belin S., Wang D., Lu T., Chen G., et al. Sustained axon regeneration induced by co-deletion of PTEN and SOCS3. Nature 2011, 480(7377):372-375.
16. Luo X., Salgueiro Y., Beckerman S.R., Lemmon V.P., Tsoulfas P., Park K.K. Three-dimensional evaluation of retinal ganglion cell axon regeneration and pathfinding in whole mouse tissue after injury. Exp Neurol 2013, 247:653-662.
17. Gallo G. Mechanisms underlying the initiation and dynamics of neuronal filopodia: from neurite formation to synaptogenesis. Int Rev Cell Mol Biol 2013, 301:95-156.
18. Peskin C.S., Odell G.M., Oster G.F. Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J 1993, 65(1):316-324.
19. Miyata H., Nishiyama S., Akashi K., Kinosita K. Protrusive growth from giant liposomes driven by actin polymerization. Proc Natl Acad Sci U S A 1999, 96(5):2048-2053.
20. Bornschlogl T. How filopodia pull: what we know about the mechanics and dynamics of filopodia. Cytoskeleton 2013, 70(10):590-603.
21. Heidemann S.R., Lamoureux P., Buxbaum R.E. Growth cone behavior and production of traction force. J Cell Biol 1990, 111(5 Pt 1):1949-1957.
22. Suter D.M., Miller K.E. The emerging role of forces in axonal elongation. Prog Neurobiol 2011, 94(2):91-101.
23. Bray D. Axonal growth in response to experimentally applied mechanical tension. Dev Biol 1984, 102(2):379-389.
24. Fass J.N., Odde D.J. Tensile force-dependent neurite elicitation via anti-beta1 integrin antibody-coated magnetic beads. Biophys J 2003, 85(1):623-636.
25. Pfister B.J., Iwata A., Meaney D.F., Smith D.H. Extreme stretch growth of integrated axons. J Neurosci 2004, 24(36):7978-7983.
26. Lamoureux P., Heidemann S.R., Martzke N.R., Miller K.E. Growth and elongation within and along the axon. Dev Neurobiol 2010, 70(3):135-149.
27. Loverde J.R., Tolentino R.E., Pfister B.J. Axon stretch growth: the mechanotransduction of neuronal growth. J Vis Exp 2011, 54.
28. Gomez T.M., Letourneau P.C. Actin dynamics in growth cone motility and navigation. J Neurochem 2014, 129(2):221-234.
29. Mitchison T., Kirschner M. Cytoskeletal dynamics and nerve growth. Neuron 1988, 1(9):761-772.
30. Chan C.E., Odde D.J. Traction dynamics of filopodia on compliant substrates. Science 2008, 322(5908):1687-1691.
31. Steketee M.B., Moysidis S.N., Jin X.L., Weinstein J.E., Pita-Thomas W., Raju H.B., et al. Nanoparticle-mediated signaling endosome localization regulates growth cone motility and neurite growth. Proc Natl Acad Sci U S A 2011, 108(47):19042-19047.
32. Corredor R.G., Trakhtenberg E.F., Pita-Thomas W., Jin X., Hu Y., Goldberg J.L. Soluble adenylyl cyclase activity is necessary for retinal ganglion cell survival and axon growth. J Neurosci 2012, 32(22):7734-7744.
33. Trakhtenberg E.F., Wang Y., Morkin M.I., Fernandez S.G., Mlacker G.M., Shechter J.M., et al. Regulating set-beta's subcellular localization toggles its function between inhibiting and promoting axon growth and regeneration. J Neurosci 2014, 34(21):7361-7374.
34. Riedl J., Crevenna A.H., Kessenbrock K., Yu J.H., Neukirchen D., Bista M., et al. Lifeact: a versatile marker to visualize F-actin. Nat Methods 2008, 5(7):60-67.
35. Hansson H.A., Holmgren J., Svennerholm L. Ultrastructural localization of cell membrane GM1 ganglioside by cholera toxin. Proc Natl Acad Sci U S A 1977, 74(9):3782-3786.
36. Beale R., Osborne N.N. Localization of the Thy-1 antigen to the surfaces of rat retinal ganglion cells. Neurochem Int 1982, 4(6):587-595.
37. Mannix R.J., Kumar S., Cassiola F., Montoya-Zavala M., Feinstein E., Prentiss M., et al. Nanomagnetic actuation of receptor-mediated signal transduction. Nat Nanotechnol 2008, 3(1):36-40.
38. Costantino S., Kent C.B., Godin A.G., Kennedy T.E., Wiseman P.W., Fournier A.E. Semi-automated quantification of filopodial dynamics. J Neurosci Methods 2008, 171(1):165-173.
39. Zidovska A., Sackmann E. On the mechanical stabilization of filopodia. Biophys J 2011, 100(6):1428-1437.
40. Forscher P., Lin C.H., Thompson C. Novel form of growth cone motility involving site-directed actin filament assembly. Nature 1992, 357(6378):515-518.
41. Raucher D., Sheetz M.P. Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol 2000, 148(1):127-136.
42. Gallo G., Lefcort F.B., Letourneau P.C. The trkA receptor mediates growth cone turning toward a localized source of nerve growth factor. J Neurosci 1997, 17(14):5445-5454.
43. Steketee M.B., Tosney K.W. Contact with isolated sclerotome cells steers sensory growth cones by altering distinct elements of extension. J Neurosci 1999, 19(9):3495-3506.
44. Nguyen T.D., Hogue I.B., Cung K., Purohit P.K., McAlpine M.C. Tension-induced neurite growth in microfluidic channels. Lab Chip 2013, 13(18):3735-3740.
45. Steketee M.B., Tosney K.W. Three functionally distinct adhesions in filopodia: shaft adhesions control lamellar extension. J Neurosci 2002, 22(18):8071-8083.
46. Robles E., Gomez T.M. Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 2006, 9(10):1274-1283.
47. Stoll G., Bendszus M. New approaches to neuroimaging of central nervous system inflammation. Curr Opin Neurol 2010, 23(3):282-286.
48. Pita-Thomas D.W., Goldberg J.L. Nanotechnology and glaucoma: little particles for a big disease. Curr Opin Ophthalmol 2013, 24(2):130-135.
49. Harrison J., Bartlett C.A., Cowin G., Nicholls P.K., Evans C.W., Clemons T.D., et al. In vivo imaging and biodistribution of multimodal polymeric nanoparticles delivered to the optic nerve. Small 2012, 8(10):1579-1589.
50. Steketee M.B., Oboudiyat C., Daneman R., Trakhtenberg E., Lamoureux P., Weinstein J.E., et al. Regulation of intrinsic axon growth ability at retinal ganglion cell growth cones. Invest Ophthalmol Vis Sci 2014, 55(7):4369-4377.