Experimental evidence for UNC-6 (netrin) axon guidance by stochastic fluctuations of intracellular UNC-40 (DCC) outgrowth activity

Biology Open

Volumn 2, Issue 12, 2013, Pages 1300-1312

  Kulkarni, Gauri ^a   Xu, Zhennan ^a   Mohamed, Ahmed M ^a   Li, Haichang ^a   Tang, Xia ^a   Limerick, Gerard ^a   Wadsworth, William G ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Axon guidance; Caenorhabditis elegans; DCC receptor; Netrin; Neurons; Stochastic process; UNC 6; Wnt signaling

Indexed keywords

EID: 84979583915     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20136346     Document Type: Article

References (49)

1. Adler, C. E., Fetter, R. D. and Bargmann, C. I. (2006). UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat. Neurosci. 9, 511-518.
2. Alexander, M., Selman, G., Seetharaman, A., Chan, K. K., D'Souza, S. A., Byrne, A. B. and Roy, P. J. (2010). MADD-2, a homolog of the Opitz syndrome protein MID1, regulates guidance to the midline through UNC-40 in Caenorhabditis elegans. Dev. Cell 18, 961-972.
3. Arrieumerlou, C. and Meyer, T. (2005). A local coupling model and compass parameter for eukaryotic chemotaxis. Dev. Cell 8, 215-227.
4. Berg, H. C. (1993) Random Walks in Biology. Princeton, NJ: Princeton University Press.
5. Bouzigues, C., Holcman, D. and Dahan, M. (2010). A mechanism for the polarity formation of chemoreceptors at the growth cone membrane for gradient amplification during directional sensing. PLoS ONE 5, e9243.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. Brown, R. (1828). A brief account of microscopical observations made in the months of June, July, and August, 1827, on the particles contained in the pollen of plants; and on the general existence of active molecules in organic and inorganic bodies. Philos. Mag. 4, 161-173.
8. Chan, S. S., Zheng, H., Su, M. W., Wilk, R., Killeen, M. T., Hedgecock, E. M. and Culotti, J. G. (1996). UNC-40, a C. elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87, 187-195.
9. Chang, C., Adler, C. E., Krause, M., Clark, S. G., Gertler, F. B., Tessier-Lavigne, M. and Bargmann, C. I. (2006). MIG-10/lamellipodin and AGE-1/PI3K promote axon guidance and outgrowth in response to slit and netrin. Curr. Biol. 16, 854-862.
10. Codling, E. A., Plank, M. J. and Benhamou, S. (2008). Random walk models in biology. J. R. Soc. Interface 5, 813-834.
11. Desai, C., Garriga, G., McIntire, S. L. and Horvitz, H. R. (1988). A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336, 638-646.
12. Duplantier, B. (2006). Brownian motion, "diverse and undulating". In Einstein, 1905-2005 (ed. T. Damour, O. Darrigol, B. Duplantier and V. Rivasseau), pp. 201-293. Boston, MA: Birkhäuser Verlag.
13. Dyer, J. M., Savage, N. S., Jin, M., Zyla, T. R., Elston, T. C. and Lew, D. J. (2013). Tracking shallow chemical gradients by actin-driven wandering of the polarization site. Curr. Biol. 23, 32-41.
14. Einstein, A. (1906). Zur theorie der brownschen bewegung. Ann. Phys. 324, 371-381.
15. Einstein, A. (1956). Investigations on the Theory of the Brownian Movement. New York, NY: Dover Publications.
16. Feller, W. (2008). An Introduction to Probability Theory and its Applications. London; New York, NY: John Wiley and Sons.
17. Frey, E. and Kroy, K. (2005). Brownian motion: a paradigm of soft matter and biological physics. Ann. Phys. 14, 20-50.
18. Garriga, G., Desai, C. and Horvitz, H. R. (1993). Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117, 1071-1087.
19. Green, J. L., Inoue, T. and Sternberg, P. W. (2008). Opposing Wnt pathways orient cell polarity during organogenesis. Cell 134, 646-656.
20. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. and Culotti, J. G. (1993). Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330.
21. Hao, J. C., Adler, C. E., Mebane, L., Gertler, F. B., Bargmann, C. I. and Tessier-Lavigne, M. (2010). The tripartite motif protein MADD-2 functions with the receptor UNC-40 (DCC) in Netrin-mediated axon attraction and branching. Dev. Cell 18, 950-960.
22. Haw, M. D. (2002). Colloidal suspensions, Brownian motion, molecular reality: a short history. J. Phys. Condens. Matter 14, 7769.
23. Hecht, I., Skoge, M. L., Charest, P. G., Ben-Jacob, E., Firtel, R. A., Loomis, W. F., Levine, H. and Rappel, W. J. (2011). Activated membrane patches guide chemotactic cell motility. PLOS Comput. Biol. 7, e1002044.
24. Hedgecock, E. M., Culotti, J. G. and Hall, D. H. (1990). The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61-85.
25. Hekimi, S. and Kershaw, D. (1993). Axonal guidance defects in a Caenorhabditis elegans mutant reveal cell-extrinsic determinants of neuronal morphology. J. Neurosci. 13, 4254-4271.
26. Hong, K., Hinck, L., Nishiyama, M., Poo, M. M., Tessier-Lavigne, M. and Stein, E. (1999). A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927-941.
27. Keleman, K. and Dickson, B. J. (2001). Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617.
28. Keller, E. F. and Segel, L. A. (1971). Model for chemotaxis. J. Theor. Biol. 30, 225-234.
29. Kim, S., Ren, X. C., Fox, E. and Wadsworth, W. G. (1999). SDQR migrations in Caenorhabditis elegans are controlled by multiple guidance cues and changing responses to netrin UNC-6. Development 126, 3881-3890.
30. Krause, M., Leslie, J. D., Stewart, M., Lafuente, E. M., Valderrama, F., Jagannathan, R., Strasser, G. A., Rubinson, D. A., Liu, H., Way, M. et al. (2004). Lamellipodin, an Ena/VASP ligand, is implicated in the regulation of lamellipodial dynamics. Dev. Cell 7, 571-583.
31. Langevin, P. (1908). Sur la théorie du mouvement brownien. CR Acad. Sci. (Paris) 146, 530-533.
32. Leonardo, E. D., Hinck, L., Masu, M., Keino-Masu, K., Ackerman, S. L. and Tessier-Lavigne, M. (1997). Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833-838.
33. Leung-Hagesteijn, C., Spence, A. M., Stern, B. D., Zhou, Y., Su, M. W., Hedgecock, E. M. and Culotti, J. G. (1992). UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289-299.
34. Macnab, R. M. and Koshland, D. E., Jr. (1972). The gradient-sensing mechanism in bacterial chemotaxis. Proc. Natl. Acad. Sci. USA 69, 2509-2512.
35. Pan, C. L., Howell, J. E., Clark, S. G., Hilliard, M., Cordes, S., Bargmann, C. I. and Garriga, G. (2006). Multiple Wnts and frizzled receptors regulate anteriorly directed cell and growth cone migrations in Caenorhabditis elegans. Dev. Cell 10, 367-377.
36. Quinn, C. C., Pfeil, D. S., Chen, E., Stovall, E. L., Harden, M. V., Gavin, M. K., Forrester, W. C., Ryder, E. F., Soto, M. C. and Wadsworth, W. G. (2006). UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr. Biol. 16, 845-853.
37. Quinn, C. C., Pfeil, D. S. and Wadsworth, W. G. (2008). CED-10/Rac1 mediates axon guidance by regulating the asymmetric distribution of MIG-10/lamellipodin. Curr. Biol. 18, 808-813.
38. Sanchez-Alvarez, L., Visanuvimol, J., McEwan, A., Su, A., Imai, J. H. and Colavita, A. (2011). VANG-1 and PRKL-1 cooperate to negatively regulate neurite formation in Caenorhabditis elegans. PLoS Genet. 7, e1002257.
39. Schmidt, K. L., Marcus-Gueret, N., Adeleye, A., Webber, J., Baillie, D. and Stringham, E. G. (2009). The cell migration molecule UNC-53/NAV2 is linked to the ARP2/3 complex by ABI-1. Development 136, 563-574.
40. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
41. Song, S., Ge, Q., Wang, J., Chen, H., Tang, S., Bi, J., Li, X., Xie, Q. and Huang, X. (2011). TRIM-9 functions in the UNC-6/UNC-40 pathway to regulate ventral guidance. J. Genet. Genomics 38, 1-11.
42. Stein, E., Zou, Y., Poo, M. and Tessier-Lavigne, M. (2001). Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 291, 1976-1982.
43. Stringham, E. G. and Schmidt, K. L. (2009). Navigating the cell: UNC-53 and the navigators, a family of cytoskeletal regulators with multiple roles in cell migration, outgrowth and trafficking. Cell Adh. Migr. 3, 342-346.
44. Stringham, E., Pujol, N., Vandekerckhove, J. and Bogaert, T. (2002). unc-53 controls longitudinal migration in C. elegans. Development 129, 3367-3379.
45. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
46. van Haastert, P. J. and Postma, M. (2007). Biased random walk by stochastic fluctuations of chemoattractant-receptor interactions at the lower limit of detection. Biophys. J. 93, 1787-1796.
47. Vladar, E. K., Antic, D. and Axelrod, J. D. (2009). Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb. Perspect. Biol. 1, a002964.
48. Wadsworth, W. G., Bhatt, H. and Hedgecock, E. M. (1996). Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35-46.
49. Xu, Z., Li, H. and Wadsworth, W. G. (2009). The roles of multiple UNC-40 (DCC) receptor-mediated signals in determining neuronal asymmetry induced by the UNC-6 (netrin) ligand. Genetics 183, 941-949.