A diffusion-based neurite length-sensing mechanism involved in neuronal symmetry breaking

Molecular Systems Biology

Volumn 6, Issue , 2010, Pages

  Toriyama, Michinori ^a   Sakumura, Yuichi ^a,b   Shimada, Tadayuki ^a   Ishii, Shin ^a,b,c,d   Inagaki, Naoyuki ^a,b  

^a NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d RIKEN   (Japan)

Author keywords

feedback loop; neuronal polarity; quantitative modeling; shootin1; stochasticity

Indexed keywords

NERVE PROTEIN; PROTEIN SHOOTIN1; UNCLASSIFIED DRUG; HYBRID PROTEIN; KINESIN; SHOOTIN1 PROTEIN, RAT;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL POLARITY; EMBRYO; HIPPOCAMPUS; NERVE FIBER; NERVE FIBER GROWTH; NEURITE; NONHUMAN; PRIORITY JOURNAL; RAT; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL SHAPE; CELL SIZE; DIFFUSION; FEEDBACK SYSTEM; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; GENETICS; GROWTH CONE; METABOLISM; PRENATAL DEVELOPMENT; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TIME; VIDEO MICROSCOPY;

ANIMALS; CELL POLARITY; CELL SHAPE; CELL SIZE; CELLS, CULTURED; DIFFUSION; FEEDBACK, PHYSIOLOGICAL; GROWTH CONES; HIPPOCAMPUS; KINESIN; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NEURITES; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 77955149462     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2010.51     Document Type: Article

References (58)

1. Arimura N, Kaibuchi K (2005) Key regulators in neuronal polarity. Neuron 48: 881-884
2. Arimura N, Kaibuchi K (2007) Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat Rev Neurosci 8: 194-205
3. Barnes AP, Polleux F (2009) Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 32: 347-381
4. Boyer HF (1987) Atlas of Stress Strain Curves, Ohio: ASM International, Metals Park
5. Bradke F, Dotti CG (1997) Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19: 1175-1186
6. Bradke F, Dotti CG (1999) The role of local actin instability in axon formation. Science 283: 1931-1934
7. Craig AM, Banker G (1994) Neuronal polarity. Annu Rev Neurosci 17: 267-310
8. Dajas-Bailador F, Jones EV, Whitmarsh AJ (2008) The JIP1 scaffold protein regulates axonal development in cortical neurons. Curr Biol 18: 221-226
9. Dogterom M, Yurke B (1997) Measurement of the force-velocity relation for growing microtubules. Science 278: 856-860
10. Dolznig H, Grebien F, Sauer T, Beug H, Mullner EW (2004) Evidence for a size-sensingmechanismin animal cells. Nat Cell Biol 6: 899-905
11. Dotti CG, Sullivan CA, Banker GA (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468
12. Driever W, Nusslein-Volhard C (1988) A gradient of bicoid protein in Drosophila embryos. Cell 54: 83-93
13. Esch T, Lemmon V, Banker G (2000) Differential effects of NgCAM and N-cadherin on the development of axons and dendrites by cultured hippocampal neurons. J Neurocytol 29: 215-223
14. Ferrell Jr JE (2009) Q&A: systems biology. J Biol 8: 2
15. Fivaz M, Bandara S, Inoue T, Meyer T (2008) Robust neuronal symmetry breaking by Ras-triggered local positive feedback. Curr Biol 18: 44-50
16. Flynn KC, Pak CW, Shaw AE, Bradke F, Bamburg JR (2009) Growth cone-like waves transport actin and promote axonogenesis and neurite branching. Dev Neurobiol 69: 761-779
17. Gauss C, KalkumM, LoweM, Lehrach H, Klose J (1999) Analysis of the mouse proteome. (I) Brain proteins: separation by two-dimensional electrophoresis and identification by mass spectrometry and genetic variation. Electrophoresis 20: 575-600
18. Goslin K, Banker G (1989) Experimental observations on the development of polarity by hippocampal neurons in culture. J Cell Biol 108: 1507-1516 (Pubitemid 19097054)
19. Gregor T, Wieschaus EF, McGregor AP, Bialek W, Tank DW (2007) Stability and nuclear dynamics of the bicoid morphogen gradient. Cell 130: 141-152
20. Hill TL (1987) Linear Aggregation Theory in Cell Biology. New York: Springer-Verlag
21. Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214
22. Hodgkin AL, Huxley AF (1952a) The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol 116: 497-506
23. Hodgkin AL, Huxley AF (1952b) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500-544
24. Horiguchi K, Hanada T, Fukui Y, Chishti AH (2006) Transport of PIP3 by GAKIN, a kinesin-3 family protein, regulates neuronal cell polarity. J Cell Biol 174: 425-436
25. Inagaki N, Chihara K, Arimura N, Menager C, Kawano Y, Matsuo N, Nishimura T, Amano M, Kaibuchi K (2001) CRMP-2 induces axons in cultured hippocampal neurons. Nat Neurosci 4: 781-782
26. 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
27. Jiang H, GuoW, 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
28. Jiang H, Rao Y (2005) Axon formation: fate versus growth. Nat Neurosci 8: 544-546
29. Keener JP (2002) Computational Cell Biology. New York: Springer- Verlag, pp 171-197
30. Kondo S (2002) The reaction-diffusion system: a mechanism for autonomous pattern formation in the animal skin. Genes Cells 7: 535-541
31. Krebs A, Goldie KN, Hoenger A (2005) Structural rearrangements in tubulin following microtubule formation. EMBO Rep 6: 227-232
32. Lamoureux P, Buxbaum RE, Heidemann SR (1989) Direct evidence that growth cones pull. Nature 340: 159-162
33. Lamoureux P, Ruthel G, Buxbaum RE, Heidemann SR (2002) Mechanical tension can specify axonal fate in hippocampal neurons. J Cell Biol 159: 499-508
34. Lewis J (2008) From signals to patterns: space, time, and mathematics in developmental biology. Science 322: 399-403
35. Marshall WF (2004) Cellular length control systems. Annu Rev Cell Dev Biol 20: 677-693
36. Medeiros NA, Burnette DT, Forscher P (2006) Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8: 215-226
37. Meinhardt H (2008) Hans Meinhardt. Curr Biol 18: R401-R402
38. Meinhardt H, Gierer A (2000) Pattern formation by local self-activation and lateral inhibition. Bioessays 22: 753-760
39. Mitchison TJ, KirschnerMW(1987) Some thoughts on the partitioning of tubulin between monomer and polymer under conditions of dynamic instability. Cell Biophys 11: 35-55
40. Mogilner A, Oster G (1996) Cell motility driven by actin polymerization. Biophys J 71: 3030-3045
41. Mori T,Wada T, Suzuki T, Kubota Y, Inagaki N (2007) Singar1, a novel RUN domain-containing protein, suppresses formation of surplus axons for neuronal polarity. J Biol Chem 282: 19884-19893
42. Morris JR, Lasek RJ (1984) Monomer-polymer equilibria in the axon: direct measurement of tubulin and actin as polymer and monomer in axoplasm. J Cell Biol 98: 2064-2076
43. Neumann FR, Nurse P (2007) Nuclear size control in fission yeast. J Cell Biol 179: 593-600
44. Oliva Jr AA, Atkins CM, Copenagle L, Banker GA (2006) Activated c- Jun N-terminal kinase is required for axon formation. J Neurosci 26: 9462-9470
45. Peskin CS, Odell GM, Oster GF (1993) Cellular motions and thermal fluctuations: the Brownian ratchet. Biophys J 65: 316-324
46. 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
47. 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
48. Samuels DC, Hentschel HG, Fine A (1996) The origin of neuronal polarization: a model of axon formation. Philos Trans R Soc London B Biol Sci 351: 1147-1156
49. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM (2007) LKB1/ STRAD promotes axon initiation during neuronal polarization. Cell 129: 565-577
50. Shimada T, Toriyama M, Uemura K, Kamiguchi H, Sugiura T, Watanabe N, Inagaki N (2008) Shootin1 interacts with actin retrograde flow and L1-CAM to promote axon outgrowth. J Cell Biol 181: 817-829
51. Toriyama M, Shimada T, Kim KB, Mitsuba M, Nomura E, Katsuta K, Sakumura Y, Roepstorff P, Inagaki N (2006) Shootin1: a protein involved in the organization of an asymmetric signal for neuronal polarization. J Cell Biol 175: 147-157
52. Turing A (1952) The chemical basis of morphogenesis. Philos Trans R Soc London B Biol Sci 237: 37-72
53. Van de Water III L, Olmsted JB (1980) The quantitation of tubulin in neuroblastoma cells by radioimmunoassay. J Biol Chem 255: 10744-10751
54. van Ooyen A, Graham BP, Ramakers GJA (2001) Competition for tubulin between growing neurites during development. Neurocomputing 38: 73-78
55. White LA, Baas PW, Heidemann SR (1987) Microtubule stability in severed axons. J Neurocytol 16: 775-784
56. Witte H, Bradke F (2008) The role of the cytoskeleton during neuronal polarization. Curr Opin Neurobiol 18: 479-487
57. Yu W, Baas PW (1994) Changes in microtubule number and length during axon differentiation. J Neurosci 14: 2818-2829
58. Zhu PP, Soderblom C, Tao-Cheng JH, Stadler J, Blackstone C (2006) SPG3A protein atlastin-1 is enriched in growth cones and promotes axon elongation during neuronal development. Hum Mol Genet 15: 1343-1353