A developmental timing switch promotes axon outgrowth independent of known guidance receptors

PLoS Genetics

Volumn 6, Issue 8, 2010, Pages

  Olsson Carter, Katherine ^a   Slack, Frank J ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; MICRORNA; PROTEIN DCC; PROTEIN LIN 14; PROTEIN LIN 28; PROTEIN SAX 3; PROTEIN UNC 40; REGULATOR PROTEIN; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DOWN REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SWITCHING; HERMAPHRODITISM; MOTONEURON; NERVE CELL DIFFERENTIATION; NERVE ELONGATION; NERVE FIBER GROWTH; NONHUMAN; TRANSCRIPTION REGULATION;

ANIMALS; AXONS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; MICRORNAS; MOTOR NEURONS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RECEPTORS, IMMUNOLOGIC; REPRESSOR PROTEINS;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 77957341454     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001054     Document Type: Article

References (77)

1. Polleux F, Ince-Dunn G, Ghosh A (2007) Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci 8: 331-340.
2. O'Donnell M, Chance RK, Bashaw GJ (2009) Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32: 383-412.
3. Kennedy TE (2000) Cellular mechanisms of netrin function: long-range and short-range actions. Biochem Cell Biol 78: 569-575.
4. Butler SJ, Tear G (2007) Getting axons onto the right path: the role of transcription factors in axon guidance. Development 134: 439-448.
5. 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.
6. Chan SS, Zheng H, Su MW, Wilk R, Killeen MT, et al. (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.
7. 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.
8. Quinn CC, Pfeil DS, Chen E, Stovall EL, Harden MV, et al. (2006) UNC-6/netrin and SLT-1/slit guidance cues orient axon outgrowth mediated by MIG-10/RIAM/lamellipodin. Curr Biol 16: 845-853.
9. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, et al. (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78: 409-424.
10. 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.
11. White JG, Southgate E, Thomson JN, Brenner S (1986) The Structure of the nervous system of the nematode Caenorhabditis elegans. Phil Trans Royal Soc London Series B 314: 1-340.
12. Ruvkun G, Giusto J (1989) The Caenorhabditis elegans heterochronic gene lin-14 encodes a nuclear protein that forms a temporal developmental switch. Nature 338: 313-319.
13. Hristova M, Birse D, Hong Y, Ambros V (2005) The Caenorhabditis elegans heterochronic regulator LIN-14 is a novel transcription factor that controls the developmental timing of transcription from the insulin/insulin-like growth factor gene ins-33 by direct DNA binding. Mol Cell Biol 25: 11059-11072.
14. Hallam SJ, Jin Y (1998) Lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans. Nature 395: 78-82.
15. Ambros V (1989) A hierarchy of regulatory genes controls a larva-to-adult developmental switch in C. elegans. Cell 57: 49-57.
16. Ambros V, Horvitz HR (1987) The lin-14 locus of Caenorhabditis elegans controls the time of expression of specific postembryonic developmental events. Genes Dev 1: 398-414.
17. Ambros V, Horvitz HR (1984) Heterochronic mutants of the nematode Caenorhabditis elegans. Science 226: 409-416.
18. Moss EG (2007) Heterochronic Genes and the Nature of Developmental Time. Current Biology 17: R425-R434.
19. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
20. Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.
21. Martinez NJ, Ow MC, Reece-Hoyes JS, Barrasa MI, Ambros VR, et al. (2008) Genome-scale spatiotemporal analysis of Caenorhabditis elegans microRNA promoter activity. Genome Res 18: 2005-2015.
22. Lin SY, Johnson SM, Abraham M, Vella MC, Pasquinelli AE, et al. (2003) The C elegans hunchback homolog, hbl-1, controls temporal patterning and is a probable microRNA target. Dev Cell 4: 639-650.
23. Abrahante JE, Daul AL, Li M, Volk ML, Tennessen JM, et al. (2003) The Caenorhabditis elegans hunchback-like gene lin-57/hbl-1 controls developmental time and is regulated by microRNAs. Dev Cell 4: 625-637.
24. Moss EG, Lee RC, Ambros V (1997) The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA. Cell 88: 637-646.
25. Antebi A, Culotti JG, Hedgecock EM (1998) Daf-12 regulates developmental age and the dauer alternative in Caenorhabditis elegans. Development 125: 1191-1205.
26. Horvitz HR, Sulston JE (1980) Isolation and genetic characterization of celllineage mutants of the nematode Caenorhabditis elegans. Genetics 96: 435-454.
27. Stefani G, Slack FJ (2008) Small non-coding RNAs in animal development. Nat Rev Mol Cell Biol 9: 219-230.
28. Gao FB (2008) Posttranscriptional control of neuronal development by microRNA networks. Trends Neurosci 31: 20-26.
29. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS (2003) A microRNA array reveals extensive regulation of microRNAs during brain development. Rna 9: 1274-1281.
30. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, et al. (2004) Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5: R68.
31. Sempere LF, Freemantle S, Pitha-Rowe I, Moss EG, Dmitrovsky E, et al. (2004) Expression profiling of mammalian microRNAs uncovers a subset of brainexpressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5: R13.
32. Schafer WF (2006) Genetics of egg-laying in worms. Annu Rev Genet 40: 487-509.
33. Desai C, Garriga G, McIntire SL, Horvitz HR (1988) A genetic pathway for the development of the Caenorhabditis elegans HSN motor neurons. Nature 336: 638-646.
34. Finney M, Ruvkun G (1990) The unc-86 gene product couples cell lineage and cell identity in C. elegans. Cell 63: 895-905.
35. Stark A, Brennecke J, Russell RB, Cohen SM (2003) Identification of Drosophila MicroRNA targets. PLoS Biol 1: e60. doi:10.1371/journal.pbio.0000060.
36. Chen CZ, Li L, Lodish HF, Bartel DP (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303: 83-86.
37. Slack F, Ruvkun G (1997) Temporal pattern formation by heterochronic genes. Annu Rev Genet 31: 611-634.
38. Moss EG, Tang L (2003) Conservation of the heterochronic regulator Lin-28, its developmental expression and microRNA complementary sites. Dev Biol 258: 432-442.
39. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, et al. (2002) Identification of tissue-specific microRNAs from mouse. Curr Biol 12: 735-739.
40. Balzer E, Heine C, Jiang Q, Lee VM, Moss EG (2010) LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro. Development 137: 891-900.
41. Viswanathan SR, Daley GQ, Gregory RI (2008) Selective Blockade of MicroRNA Processing by Lin-28. Science.
42. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
43. Hong Y, Lee RC, Ambros V (2000) Structure and function analysis of LIN-14, a temporal regulator of postembryonic developmental events in Caenorhabditis elegans. Mol Cell Biol 20: 2285-2295.
44. Wightman B, Burglin TR, Gatto J, Arasu P, Ruvkun G (1991) Negative regulatory sequences in the lin-14 39-untranslated region are necessary to generate a temporal switch during Caenorhabditis elegans development. Genes Dev 5: 1813-1824.
45. Ha I, Wightman B, Ruvkun G (1996) A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. Genes Dev 10: 3041-3050.
46. Abrahante JE, Miller EA, Rougvie AE (1998) Identification of heterochronic mutants in Caenorhabditis elegans. Temporal misexpression of a collagen: green fluorescent protein fusion gene. Genetics 149: 1335-1351.
47. Morita K, Han M (2006) Multiple mechanisms are involved in regulating the expression of the developmental timing regulator lin-28 in Caenorhabditis elegans. Embo J 25: 5794-5804.
48. Seggerson K, Tang L, Moss EG (2002) Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation. Dev Biol 243: 215-225.
49. Dixon SJ, Alexander M, Chan KK, Roy PJ (2008) Insulin-like signaling negatively regulates muscle arm extension through DAF-12 in Caenorhabditis elegans. Dev Biol 318: 153-161.
50. Boehm M, Slack F (2005) A developmental timing microRNA and its target regulate life span in C. elegans. Science 310: 1954-1957.
51. Esquela-Kerscher A, Johnson SM, Bai L, Saito K, Partridge J, et al. (2005) Postembryonic expression of C. elegans microRNAs belonging to the lin-4 and let-7 families in the hypodermis and the reproductive system. Dev Dyn 234: 868-877.
52. Shen K, Bargmann CI (2003) The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112: 619-630.
53. Gitai Z, Yu TW, Lundquist EA, Tessier-Lavigne M, Bargmann CI (2003) The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37: 53-65.
54. 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.
55. 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.
56. Levy-Strumpf N, Culotti J (2007) VAB-8, UNC-73 and MIG-2 regulate axon polarity and cell migration functions of UNC-40 in C. elegans. Nat Neurosci 10: 161-168.
57. Zallen JA, Yi BA, Bargmann CI (1998) The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans. Cell 92: 217-227.
58. Desai AR, McConnell SK (2000) Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127: 2863-2872.
59. Isshiki T, Pearson BJ, Holbrook S, Doe CQ (2001) Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106: 511-521.
60. Livesey FJ, Cepko CL (2001) Vertebrate neural cell-fate determination: lessons from the retina. Nat Rev Neurosci 2: 109-118.
61. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427-437.
62. Pearson BJ, Doe CQ (2004) Specification of temporal identity in the developing nervous system. Annu Rev Cell Dev Biol 20: 619-647.
63. Nguyen L, Besson A, Roberts JM, Guillemot F (2006) Coupling cell cycle exit, neuronal differentiation and migration in cortical neurogenesis. Cell Cycle 5: 2314-2318.
64. Ohnuma S, Philpott A, Harris WA (2001) Cell cycle and cell fate in the nervous system. Curr Opin Neurobiol 11: 66-73.
65. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, et al. (2008) Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57: 378-392.
66. Sestan N, Artavanis-Tsakonas S, Rakic P (1999) Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286: 741-746.
67. Desai C, Horvitz HR (1989) Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying. Genetics 121: 703-721.
68. Arasu P, Wightman B, Ruvkun G (1991) Temporal regulation of lin-14 by the antagonistic action of two other heterochronic genes, lin-4 and lin-28. Genes Dev 5: 1825-1833.
69. Aurelio O, Boulin T, Hobert O (2003) Identification of spatial and temporal cues that regulate postembryonic expression of axon maintenance factors in the C. elegans ventral nerve cord. Development 130: 599-610.
70. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, et al. (2000) The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403: 901-906.
71. da Silva JS, Dotti CG (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3: 694-704.
72. Goldberg JL (2003) How does an axon grow? Genes Dev 17: 941-958.
73. Smirnova L, Gräfe A, Seiler A, Schumacher S, Nitsch R, et al. (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21: 1469-1477.
74. Wu L, Belasco JG (2005) Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Mol Cell Biol 25: 9198-9208.
75. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
76. Sze JY, Victor M, Loer CM, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564.
77. Mello CC, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451-482.