Extracellular matrix regulates UNC-6 (netrin) axon guidance by controlling the direction of intracellular UNC-40 (DCC) outgrowth activity

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Yang, Yong ^a   Lee, Won Suk ^a   Tang, Xia ^a   Wadsworth, William G ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTEGRIN; MATRIX PROTEIN; NETRIN; NIK KINASE; PROTEIN KINASE; UNC 40; UNC 52; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CELL ADHESION MOLECULE; CYTOSKELETON PROTEIN; INA-1 PROTEIN, C ELEGANS; INTEGRIN; MEMBRANE PROTEIN; MIG-15 PROTEIN, C ELEGANS; MUSCLE PROTEIN; NERVE PROTEIN; PRIMER DNA; PROTEIN SERINE THREONINE KINASE; PROTEOGLYCAN; UNC-112 PROTEIN, C ELEGANS; UNC-40 PROTEIN, C ELEGANS; UNC-52 PROTEIN, C ELEGANS; UNC-6 PROTEIN, C ELEGANS; UNC-97 PROTEIN, C ELEGANS; VAB-19 PROTEIN, C ELEGANS;

ARTICLE; CAENORHABDITIS ELEGANS; CELL SPECIFICITY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GENE DISRUPTION; GENE MUTATION; GROWTH REGULATION; INTRACELLULAR SIGNALING; INTRACELLULAR SPACE; NERVE FIBER GROWTH; NERVE PROJECTION; NONHUMAN; PERIKARYON; PROTEIN FUNCTION; ANIMAL; CELL MOTION; COMPUTER SIMULATION; GENE VECTOR; GENETICS; METABOLISM; MUTATION; NERVE FIBER; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL MOVEMENT; COMPUTER SIMULATION; CYTOSKELETAL PROTEINS; DNA PRIMERS; EXTRACELLULAR MATRIX; GENETIC VECTORS; INTEGRINS; MEMBRANE PROTEINS; MUSCLE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PROTEIN-SERINE-THREONINE KINASES; PROTEOGLYCANS; SIGNAL TRANSDUCTION;

EID: 84901277591     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097258     Document Type: Article

References (46)

1. White J, Southgate E, Thompson J, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314: 1-340.
2. Hedgecock EM, Culotti JG, Hall DH (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. (Pubitemid 20149756)
3. Ishii N, Wadsworth WG, Stern BD, Culotti JG, Hedgecock EM (1992) UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 9: 873-881.
4. Wadsworth WG, Bhatt H, Hedgecock EM (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. (Pubitemid 26044727)
5. Asakura T, Ogura K, Goshima Y (2007) UNC-6 expression by the vulval precursor cells of Caenorhabditis elegans is required for the complex axon guidance of the HSN neurons. Dev Biol 304: 800-810. (Pubitemid 46533976)
6. Kulkarni G, Xu Z, Mohamed AM, Li H, Tang X, et al. (2013) Experimental evidence for UNC-6 (netrin) axon guidance by stochastic fluctuations of intracellular UNC-40 (DCC) outgrowth activity. Biol Open 2: 1300-1312.
7. Xu Z, Li H, Wadsworth WG (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.
8. Rogalski TM, Williams BD, Mullen GP, Moerman DG (1993) Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev 7: 1471-1484. (Pubitemid 23234342)
9. Mullen GP, Rogalski TM, Bush JA, Gorji PR, Moerman DG (1999) Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol Biol Cell 10: 3205-3221. (Pubitemid 29489556)
10. Merz DC, Alves G, Kawano T, Zheng H, Culotti JG (2003) UNC-52/perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev Biol 256: 173-186. (Pubitemid 36332212)
11. Hagedorn EJ, Ziel JW, Morrissey MA, Linden LM, Wang Z, et al. (2013) The netrin receptor DCC focuses invadopodia-driven basement membrane transmigration in vivo. J Cell Biol 201: 903-913.
12. Ziel JW, Hagedorn EJ, Audhya A, Sherwood DR (2009) UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat Cell Biol 11: 183-189.
13. Hagedorn EJ, Yashiro H, Ziel JW, Ihara S, Wang Z, et al. (2009) Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. Dev Cell 17: 187-198.
14. Shakir MA, Gill JS, Lundquist EA (2006) Interactions of UNC-34 Enabled with Rac GTPases and the NIK kinase MIG-15 in Caenorhabditis elegans axon pathfinding and neuronal migration. Genetics 172: 893-913. (Pubitemid 43345427)
15. Teulière J, Gally C, Garriga G, Labouesse M, Georges-Labouesse E (2011) MIG-15 and ERM-1 promote growth cone directional migration in parallel to UNC-116 and WVE-1. Development 138: 4475-4485.
16. Poinat P, De Arcangelis A, Sookhareea S, Zhu X, Hedgecock EM, et al. (2002) A conserved interaction between beta1 integrin/PAT-3 and Nck-interacting kinase/MIG-15 that mediates commissural axon navigation in C. elegans. Curr Biol 12: 622-631. (Pubitemid 34315845)
17. Hresko MC, Williams BD, Waterston RH (1994) Assembly of body wall muscle and muscle cell attachment structures in Caenorhabditis elegans. J Cell Biol 124: 491-506. (Pubitemid 24064461)
18. Francis R, Waterston RH (1991) Muscle cell attachment in Caenorhabditis elegans. J Cell Biol 114: 465-479. (Pubitemid 21909816)
19. Adler CE, Fetter RD, Bargmann CI (2006) UNC-6/Netrin induces neuronal asymmetry and defines the site of axon formation. Nat Neurosci 9: 511-518.
20. Rogalski TM, Gilchrist EJ, Mullen GP, Moerman DG (1995) Mutations in the unc-52 gene responsible for body wall muscle defects in adult Caenorhabditis elegans are located in alternatively spliced exons. Genetics 139: 159-169.
21. Rogalski TM, Mullen GP, Gilbert MM, Williams BD, Moerman DG (2000) The UNC-112 gene in Caenorhabditis elegans encodes a novel component of cellmatrix adhesion structures required for integrin localization in the muscle cell membrane. J Cell Biol 150: 253-264. (Pubitemid 30480998)
22. Williams BD, Waterston RH (1994) Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124: 475-490. (Pubitemid 24064460)
23. Ding M, Goncharov A, Jin Y, Chisholm AD (2003) C. elegans ankyrin repeat protein VAB-19 is a component of epidermal attachment structures and is essential for epidermal morphogenesis. Development 130: 5791-5801. (Pubitemid 37540852)
24. Hobert O, Moerman DG, Clark KA, Beckerle MC, Ruvkun G (1999) A conserved LIM protein that affects muscular adherens junction integrity and mechanosensory function in Caenorhabditis elegans. J Cell Biol 144: 45-57. (Pubitemid 29047010)
25. Gettner SN, Kenyon C, Reichardt LF (1995) Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol 129: 1127-1141.
26. Yurchenco PD, Wadsworth WG (2004) Assembly and tissue functions of early embryonic laminins and netrins. Curr Opin Cell Biol 16: 572-579. (Pubitemid 39201243)
27. Meighan CM, Schwarzbauer JE (2007) Control of C. elegans hermaphrodite gonad size and shape by vab-3/Pax6-mediated regulation of integrin receptors. Genes Dev 21: 1615-1620. (Pubitemid 47026366)
28. Baum PD, Garriga G (1997) Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19: 51-62. (Pubitemid 27332993)
29. Baumeister R, Liu Y, Ruvkun G (1996) Lineage-specific regulators couple cell lineage asymmetry to the transcription of the Caenorhabditis elegans POU gene unc-86 during neurogenesis. Genes Dev 10: 1395-1410. (Pubitemid 26260718)
30. Olsson-Carter K, Slack FJ (2010) A developmental timing switch promotes axon outgrowth independent of known guidance receptors. PLoS genetics 6.
31. Olsson-Carter K, Slack FJ (2011) The POU transcription factor UNC-86 controls the timing and ventral guidance of Caenorhabditis elegans axon growth. Developmental dynamics: an official publication of the American Association of Anatomists 240: 1815-1825.
32. Emtage L, Gu G, Hartwieg E, Chalfie M (2004) Extracellular proteins organize the mechanosensory channel complex in C. elegans touch receptor neurons. Neuron 44: 795-807. (Pubitemid 39575633)
33. Raper J, Mason C (2010) Cellular strategies of axonal pathfinding. Cold Spring Harb Perspect Biol 2: a001933.
34. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274: 1123-1133. (Pubitemid 26389268)
35. Hong K, Hinck L, Nishiyama M, Poo MM, Tessier-Lavigne M, et al. (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. (Pubitemid 29375051)
36. Bashaw GJ, Goodman CS (1999) Chimeric axon guidance receptors: the cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion. Cell 97: 917-926. (Pubitemid 29375050)
37. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF (2003) Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26: 509-563. (Pubitemid 37064943)
38. Nikolopoulos SN, Giancotti FG (2005) Netrin-integrin signaling in epithelial morphogenesis, axon guidance and vascular patterning. Cell Cycle 4: e131-135. (Pubitemid 41359711)
39. Yebra M, Montgomery AM, Diaferia GR, Kaido T, Silletti S, et al. (2003) Recognition of the neural chemoattractant Netrin-1 by integrins alpha6beta4 and alpha3beta1 regulates epithelial cell adhesion and migration. Dev Cell 5: 695-707. (Pubitemid 37362214)
40. Kolodkin AL, Tessier-Lavigne M (2011) Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb Perspect Biol 3.
41. Poon VY, Klassen MP, Shen K (2008) UNC-6/netrin and its receptor UNC-5 locally exclude presynaptic components from dendrites. Nature.
42. Park J, Knezevich PL, Wung W, O'Hanlon SN, Goyal A, et al. (2011) A conserved juxtacrine signal regulates synaptic partner recognition in Caenorhabditis elegans. Neural Dev 6: 28.
43. Colon-Ramos DA, Margeta MA, Shen K (2007) Glia promote local synaptogenesis through UNC-6 (netrin) signaling in C. elegans. Science 318: 103-106. (Pubitemid 47538042)
44. Lai Wing Sun K, Correia JP, Kennedy TE (2011) Netrins: versatile extracellular cues with diverse functions. Development 138: 2153-2169.
45. Mehlen P, Guenebeaud C (2010) Netrin-1 and its dependence receptors as original targets for cancer therapy. Curr Opin Oncol 22: 46-54.
46. Mehlen P, Delloye-Bourgeois C, Chédotal A (2011) Novel roles for Slits and netrins: axon guidance cues as anticancer targets? Nat Rev Cancer 11: 188-197.