Growth cone-like waves transport actin and promote axonogenesis and neurite branching

Developmental Neurobiology

Volumn 69, Issue 12, 2009, Pages 761-779

  Flynn, Kevin C ^a,b   Pak, Chi W ^a   Shaw, Alisa E ^a   Bradke, Frank ^b   Bamburg, James R ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Actin transport; Axonogenesis; Growth cones; Neurite branching; Organotypic hippocampal culture

Indexed keywords

ACTIN; GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; FILOPODIUM; GROWTH CONE; HIPPOCAMPUS; HUMAN; IMAGING; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER TRANSPORT; NEURITE; NEUROBIOLOGY; NONHUMAN; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT; SPIKE WAVE;

ACTINS; ANIMALS; AXONAL TRANSPORT; AXONS; CELL MOVEMENT; CELLS, CULTURED; GENE TRANSFER TECHNIQUES; GROWTH CONES; HIPPOCAMPUS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; NEURITES; NEURONS; ORGAN CULTURE TECHNIQUES; RATS;

EID: 69749090329     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20734     Document Type: Article

References (70)

1. Abe H, Ohshima S, Obinata T. 1989. A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. J Biochem 106:696-702. (Pubitemid 19241841)
2. Abe T, Kato M, Miki H, Takenawa T, Endo T. 2003. Small GTPase Tc10 and its homologue RhoT induce N-WASP-mediated long process formation and neurite outgrowth. J Cell Sci 116:155-168. (Pubitemid 36113974)
3. Aizawa H, Wakatsuki S, Ishii A, Moriyama K, Sasaki Y, Ohashi K, Sekine-Aizawa Y, et al. 2001. Phosphorylation of cofilin by LIM-kinase is necessary for semaphorin 3A-induced growth cone collapse. Nat Neurosci 4:367-373. (Pubitemid 32260112)
4. Alberts P, Rudge R, Irinopoulou T, Danglot L, Gauthier- Rouviere C, Galli T. 2006. Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane. Mol Biol Cell 17:1194-1203. (Pubitemid 43376541)
5. Baas PW, Buster DW. 2004. Slow axonal transport and the genesis of neuronal morphology. J Neurobiol 58:3-17.
6. Black MM, Lasek RJ. 1979. Axonal transport of actin: Slow component b is the principal source of actin for the axon. Brain Res 171:401-413.
7. Bradke F, Dotti CG. 1997. Neuronal polarity: Vectorial cytoplasmic flow precedes axon formation. Neuron 19: 1175-1186. (Pubitemid 28030538)
8. Bradke F, Dotti CG. 1999. The role of local actin instability in axon formation. Science 283:1931-1934. (Pubitemid 129504147)
9. Bradke F, Dotti CG. 2000. Establishment of neuronal polarity: Lessons from cultured hippocampal neurons. Curr Op Neurobiol 10:574-581. (Pubitemid 30846342)
10. Bretschneider T, Anderson K, Ecke M, Müller-Taubenberger A, Schroth-Diez B, Ishikawa-Ankerhold HC, Gerisch G. 2009. The three-dimensional dynamics of actin waves, a model of cytoskeletal self-organization. Biophys J 96:2888-2900.
11. Bridgman PC, Dave S, Asnes CF, Tullio AN, Adelstein RS. 2001. Myosin IIB is required for growth cone motility. J Neurosci 21:6159-6169. (Pubitemid 32737748)
12. Brown A, Wang L, Jung P. 2005. Stochastic simulation of neurofilament transport in axons: The "stop-and-go" hypothesis. Mol Biol Cell 16:4243-4255.
13. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. 2002. A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99:7877-7882.
14. Craig AM, Banker G. 1994. Neuronal polarity. Annu Rev Neurosci 17:267-310.
15. da Silva JS, Dotti CG. 2002. Breaking the neuronal sphere: Regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3:694-704. (Pubitemid 135706675)
16. Dailey ME, Buchanan J, Bergles DE, Smith SJ. 1994. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J Neurosci 14:1060-1078. (Pubitemid 24081904)
17. Davis RC, Maloney MT, Minamide LS, Flynn KC, Stonebraker MA, Bamburg JR. Mapping cofilin-actin rods in stressed hippocampal slices and the role of cdc42 in amyloid β-induced rods. J Alz Dis, in press.
18. de Hoop MJ, Meyn L, Dotti CG. 1998. Culturing Hippocampal Neurons and Astrocytes from Fetal Rodent Brain. San Diego: Academic Press, pp 154-163.
19. De la Monte SM, Federoff HJ, Ng SC, Grabczyk E, Fishman MC. 1989. GAP-43 gene expression during development: Persistence in a distinctive set of neurons in the mature central nervous system. Brain Res Dev Brain Res 46:161-168. (Pubitemid 19088751)
20. Dent EW, Kalil K. 2001. Axon branching requires interactions between dynamic microtubules and actin filaments. J Neurosci 21:9757-9769. (Pubitemid 34184061)
21. Dent EW, Kwiatkowski AV, Mebane LM, Philippar U, Barzik M, Rubinson DA, Gupton S, et al. 2007. Filopodia are required for cortical neurite initiation. Nat Cell Biol 9:1347-1359. (Pubitemid 350201748)
22. Endo M, Ohashi K, Mizuno K. 2007. LIM kinase and sling-shot are critical for neurite extension. J Biol Chem 282: 13692-13702. (Pubitemid 47100568)
23. Endo M, Ohashi K, Sasaki Y, Goshima Y, Niwa R, Uemura T, Mizuno K. 2003. Control of growth cone motility and morphology by LIM kinase and Slingshot via phosphorylation and dephosphorylation of cofilin. J Neurosci 23: 2527-2537. (Pubitemid 36418586)
24. Esch T, Lemmon V, Banker G. 1999. Local presentation of substrate molecules directs axon specification by cultured hippocampal neurons. J Neurosci 19:6417-6426. (Pubitemid 29347441)
25. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, et al. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28:41-51.
26. Forss-Petter S, Danielson PE, Catsicas S, Battenberg E, Price J, Nerenberg M, Sutcliffe JG. 1990. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron 5:187-197. (Pubitemid 20262697)
27. Gallo G, Letourneau PC. 2004. Regulation of growth cone actin filaments by guidance cues. J Neurobiol 58: 92-102. (Pubitemid 37543341)
28. Gallo G, Yee HF Jr, Letourneau PC. 2002. Actin turnover is required to prevent axon retraction driven by endogenous actomyosin contractility. J Cell Biol 158:1219-1228.
29. Garvalov BK, Flynn KC, Neukirchen D, Meyn L, Teusch N, Wu X, Brakebusch C, Bamburg JR, Bradke F. 2007. Cdc42 regulates cofilin during the establishment of neuronal polarity. J Neurosci 27:13117-13129. (Pubitemid 350220488)
30. Gomez-Di Cesare CM, Smith KL, Rice FL, Swann JW. 1997. Axonal remodeling during postnatal maturation of CA3 hippocampal pyramidal neurons. J Comp Neurol 384:165-180.
31. Gurskaya NG, Verkhusha VV, Shcheglov AS, Staroverov DB, Chepurnykh TV, Fradkov AF, Lukyanov S, et al. 2006. Engineering of a monomeric green-to-red photo-activatable fluorescent protein induced by blue light. Nat Biotechnol 24:461-465.
32. Heidemann SR, Reynolds M, Ngo K, Lamoureux P. 2003. The culture of chick forebrain neurons. Methods Cell Biol 71:51-65.
33. Horton AC, Ehlers MD. 2003. Neuronal polarity and trafficking. Neuron 40:277-295.
34. Hutchins BI, Kalil K. 2008. Differential outgrowth of axons and their branches is regulated by localized calcium transients. J Neurosci 28:143-153.
35. Inagaki N, Chihara K, Arimura N, Menager C, Kawano Y, Matsuo N, Nishimura T, et al. 2001. CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 4: 781-782. (Pubitemid 32702507)
36. Jacobson C, Schnapp B, Banker GA. 2006. A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49: 797-804. (Pubitemid 43376077)
37. Jiang H, Guo W, Liang X, Rao Y. 2005. Both the establishment and the maintenance of neuronal polarity require active mechanisms: Critical roles of GSK-3beta and its upstream regulators. Cell 120:123-135. (Pubitemid 40094608)
38. Kim Y, Chang S. 2004. Modulation of actomyosin contractility by myosin light chain phosphorylation/dephosphorylation through Rho GTPases signaling specifies axon formation in neurons. Biochem Biophys Res Commun 318:579-587. (Pubitemid 38553818)
39. Knoll B, Kretz O, Fiedler C, Alberti S, Schutz G, Frotscher M, Nordheim A. 2006. Serum response factor controls neuronal circuit assembly in the hippocampus. Nat Neurosci 9:195-204. (Pubitemid 43164542)
40. Kuhn TB, Meberg PJ, Brown MD, Bernstein BW, Minamide LS, Jensen JR, Okada K, et al. 2000. Regulating actin dynamics in neuronal growth cones by ADF/cofilin and rho family GTPases. J Neurobiol 44:126-144.
41. Kunda P, Paglini G, Quiroga S, Kosik K, Caceres A. 2001. Evidence for the involvement of Tiam1 in axon formation. J Neurosci 21:2361-2372. (Pubitemid 32240533)
42. Letourneau PC, Shattuck TA, Ressler AH. 1987. "Pull" and "push" in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskeleton 8:193-209.
43. Luo L, O'Leary DD. 2005. Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28: 127-156. (Pubitemid 41098902)
44. Ma Y, Shakiryanova D, Vardya I, Popov SV. 2004. Quantitative analysis of microtubule transport in growing nerve processes. Curr Biol 14:725-730. (Pubitemid 38503611)
45. Marsh L, Letourneau PC. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047. (Pubitemid 15181865)
46. Mattson MP, Kater SB. 1988. Isolated hippocampal neurons in cryopreserved long-term cultures: Development of neuroarchitecture and sensitivity to NMDA. Int J Dev Neurosci 6:439-452.
47. McQuarrie IG, Jacob JM. 1991. Conditioning nerve crush accelerates cytoskeletal protein transport in sprouts that form after a subsequent crush. J Comp Neurol 305:139-147.
48. Meberg PJ, Bamburg JR. 2000. Increase in neurite outgrowth mediated by overexpression of actin depolymerizing factor. J Neurosci 20:2459-2469.
49. Meberg PJ, Ono S, Minamide LS, Takahashi M, Bamburg JR. 1998. Actin depolymerizing factor and cofilin phosphorylation dynamics: Response to signals that regulate neurite extension. Cell Motil Cytoskeleton 39: 172-190. (Pubitemid 28079648)
50. Mills RG, Minamide LS, Yuan A, Bamburg JR, Bray JJ. 1996. Slow axonal transport of soluble actin with actin depolymerizing factor, cofilin, and profilin suggests actin moves in an unassembled form. J Neurochem 67:1225-1234. (Pubitemid 26277936)
51. Minamide LS, Shaw AE, Sarmiere PD, Wiggan O, Maloney MT, Bernstein BW, Sneider JM, et al. 2003. Production and use of replication-deficient adenovirus for transgene expression in neurons. Methods Cell Biol 71:387-416. (Pubitemid 137639606)
52. Minamide LS, Striegl AM, Boyle JA, Meberg PJ, Bamburg JR. 2000. Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat Cell Biol 2:628-636.
53. O'Leary DD, Terashima T. 1988. Cortical axons branch to multiple subcortical targets by interstitial axon budding: implications for target recognition and "waiting periods". Neuron 1:901-910.
54. Popov S, Poo MM. 1992. Diffusional transport of macromolecules in developing nerve processes. J Neurosci 12: 77-85.
55. Rosso S, Bollati F, Bisbal M, Peretti D, Sumi T, Nakamura T, Quiroga S, et al. 2004. LIMK1 regulates golgi dynamics, traffic of golgi-derived vesicles, and process extension in primary cultured neurons. Mol Biol Cell 15:3433-3449. (Pubitemid 38850135)
56. Ruthel G, Banker G. 1998. Actin-dependent anterograde movement of growth-cone-like structures along growing hippocampal axons: A novel form of axonal transport? Cell Motil Cytoskeleton 40:160-173.
57. Ruthel G, Banker G. 1999. Role of moving growth cone-like "wave" structures in the outgrowth of cultured hippocampal axons and dendrites. J Neurobiol 39:97-106.
58. Ruthel G, Hollenbeck PJ. 2000. Growth cones are not required for initial establishment of polarity or differential axon branch growth in cultured hippocampal neurons. J Neurosci 20:2266-2274. (Pubitemid 30230080)
59. Schwamborn JC, Muller M, Becker AH, Puschel AW. 2007. Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 26:1410-1422. (Pubitemid 46398703)
60. Schwamborn JC, Puschel AW. 2004. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat Neurosci 7:923-929.
61. Shi SH, Jan LY, Jan YN. 2003. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 112:63-75.
62. Strasser GA, Rahim NA, VanderWaal KE, Gertler FB, Lanier LM. 2004. Arp2/3 is a negative regulator of growth cone translocation. Neuron 43:81-94.
63. Tang F, Kalil K. 2005. Netrin-1 induces axon branching in developing cortical neurons by frequency-dependent calcium signaling pathways. J Neurosci 25:6702-6715. (Pubitemid 40995303)
64. Toriyama M, Shimada T, Kim KB, Mitsuba M, Nomura E, Katsuta K, Sakumura Y, et al. 2006. Shootin1: A protein involved in the organization of an asymmetric signal for neuronal polarization. J Cell Biol 175:147-157. (Pubitemid 44537206)
65. Tursun B, Schluter A, Peters MA, Viehweger B, Ostendorff HP, Soosairajah J, Drung A, et al. 2005. The ubiquitin ligase Rnf6 regulates local LIM kinase 1 levels in axonal growth cones. Genes Dev 19:2307-2319. (Pubitemid 41396908)
66. Wang L, Brown A. 2001. Rapid intermittent movement of axonal neurofilaments observed by fluorescence photo-bleaching. Mol Biol Cell 12:3257-3267. (Pubitemid 33062977)
67. Wang L, Brown A. 2002. Rapid movement of microtubules in axons. Curr Biol 12:1496-1501.
68. Wen Z, Han L, Bamburg JR, Shim S, Ming GL, Zheng JQ. 2007. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J Cell Biol 178:107-119. (Pubitemid 47026406)
69. Witte H, Bradke F. 2008. The role of the cytoskeleton during neuronal polarization. Curr Opin Neurobiol 18:479-487.
70. Wujek JR, Lasek RJ. 1983. Correlation of axonal regeneration and slow component B in two branches of a single axon. J Neurosci 3:243-251.