The HLH-6 transcription factor regulates C. elegans pharyngeal gland development and function

PLoS Genetics

Volumn 4, Issue 10, 2008, Pages

  Smit, Ryan B ^a   Schnabel, Ralf ^b   Gaudet, Jeb ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b TECHNICAL UNIVERSITY OF BRAUNSCHWEIG   (Germany)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; PROTEIN PGM1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HLH 6; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CAENORHABDITIS ELEGANS PROTEIN; HELMINTH DNA; HELMINTH PROTEIN; HLH 6 PROTEIN, C ELEGANS; HLH-6 PROTEIN, C ELEGANS; MUCIN;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CUTICLE; GENE EXPRESSION; NONHUMAN; ORGANOGENESIS; PHARYNX; PHENOTYPE; PROTEIN FUNCTION; ANIMAL; GENE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SECRETION; SEQUENCE HOMOLOGY; TRANSGENIC ANIMAL;

CAENORHABDITIS ELEGANS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA, HELMINTH; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENES, HELMINTH; HELMINTH PROTEINS; MUCINS; MUTATION; PHARYNX; PHENOTYPE; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 55449128042     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000222     Document Type: Article

References (83)

1. Mango SE, Lambie EJ, Kimble J (1994) The pha-4 gene is required to generate the pharyngeal primordium of Caenorhabditis elegans. Development 120: 3019-3031.
2. Horner MA, Quintin S, Domeier ME, Kimble J, Labouesse M, et al. (1998) pha-4, an HNF-3 homologue, specifies pharyngeal organ identity in Caenorhabditis elegans. Genes Dev 12: 1947-1952.
3. Kalb JM, Lau KK, Goszczynski B, Fukushige T, Moons D, et al. (1998) pha-4 is Ce-fkh-1, a fork head/HNF-3alpha,beta,gamma homolog that functions in organogenesis of the C. elegans pharynx. Development 125: 2171-2180.
4. Gaudet J, Mango SE (2002) Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295: 821-825.
5. Roy Chowdhuri S, Crum T, Woollard A, Aslam S, Okkema PG (2006) The T-box factor TBX-2 and the SUMO conjugating enzyme UBC-9 are required for ABa-derived pharyngeal muscle in C. elegans. Dev Biol 295: 664-677.
6. Morck C, Rauthan M, Wagberg F, Pilon M (2004) pha-2 encodes the C. elegans ortholog of the homeodomain protein HEX and is required for the formation of the pharyngeal isthmus. Dev Biol 272: 403-418.
7. Okkema PG, Fire A (1994) The Caenorhabditis elegans NK-2 class homeoprotein CEH-22 is involved in combinatorial activation of gene expression in pharyngeal muscle. Development 120: 2175-2186.
8. Smith PA, Mango SE (2007) Role of T-box gene tbx-2 for anterior foregut muscle development in C. elegans. Dev Biol 302: 25-39.
9. Albertson DG, Thomson JN (1976) The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275: 299-325.
10. Hoflich J, Berninsone P, Gobel C, Gravato-Nobre MJ, Libby BJ, et al. (2004) Loss of srf-3-encoded nucleotide sugar transporter activity in Caenorhabditis elegans alters surface antigenicity and prevents bacterial adherence. J Biol Chem 279: 30440-30448.
11. Ohmachi M, Sugimoto A, Iino Y, Yamamoto M (1999) kel-1, a novel Kelch-related gene in Caenorhabditis elegans, is expressed in pharyngeal gland cells and is required for the feeding process. Genes Cells 4: 325-337.
12. Singh RN, Sulston JE (1978) Some observations on moulting in Caenorhabditis elegans. Nematologica 24: 63-71.
13. Jasmer DP, Goverse A, Smant G (2003) Parasitic nematode interactions with mammals and plants. Annu Rev Phytopathol 41: 245-270.
14. Ao W, Gaudet J, Kent WJ, Muttumu S, Mango SE (2004) Environmentally induced foregut remodeling by PHA-4/FoxA and DAF-12/NHR. Science 305: 1743-1746.
15. Kohara Y (2001) NEXTDB: The Nematode Expression Pattern Database.
16. Kohara Y (2001) [Systematic analysis of gene expression of the C. elegans genome]. Tanpakushitsu Kakusan Koso 46: 2425-2431.
17. Kaplan MD, Baum BJ (1993) The functions of saliva. Dysphagia 8: 225-229.
18. Castaneda O, Sotolongo V, Amor AM, Stocklin R, Anderson AJ, et al. (1995) Characterization of a potassium channel toxin from the Caribbean Sea anemone Stichodactyla helianthus. Toxicon 33: 603-613.
19. Spieth J, Lawson D (2006) Overview of gene structure. WormBook. pp 1-10.
20. Okkema PG, Krause M (2005) Transcriptional regulation. WormBook. pp 1-40.
21. Hope IA, Albertson DG, Martinelli SD, Lynch AS, Sonnhammer E, et al. (1996) The C. elegans expression pattern database: a beginning. Trends Genet 12: 370-371.
22. Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, et al. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12: 1209-1214.
23. Ephrussi A, Church GM, Tonegawa S, Gilbert W (1985) B lineage-specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science 227: 134-140.
24. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Devel Biol 100: 64-119.
25. Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429-440.
26. Krause M, Park M, Zhang JM, Yuan J, Harfe B, et al. (1997) A C. elegans E/Daughterless bHLH protein marks neuronal but not striated muscle development. Development 124: 2179-2189.
27. Gaudet J, Muttumu S, Horner M, Mango SE (2004) Whole-genome analysis of temporal gene expression during foregut development. PLoS Biol 2: e352.
28. Harfe BD, Gomes AV, Kenyon C, Liu J, Krause M, et al. (1998) Analysis of a Caenorhabditis elegans Twist homolog identifies conserved and divergent aspects of mesodermal patterning. Genes Dev 12: 2623-2635.
29. Gengyo-Ando K, Mitani S (2000) Characterization of mutations induced by ethyl methanesulfonate, UV, and trimethylpsoralen in the nematode Caenorhabditis elegans. Biochem Biophys Res Commun 269: 64-69.
30. Raharjo I, Gaudet J (2007) Gland-specific expression of C. elegans hlh-6 requires the combinatorial action of three distinct promoter elements. Dev Biol 302: 295-308.
31. Yuan JY, Horvitz HR (1990) The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev Biol 138: 33-41.
32. Ellis HM, Horvitz HR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817-829.
33. Avery L (1993) The genetics of feeding in Caenorhabditis elegans. Genetics 133: 897-917.
34. Morck C, Pilon M (2006) C. elegans feeding defective mutants have shorter body lengths and increased autophagy. BMC Dev Biol 6: 39.
35. Ashrafi K, Chang FY, Watts JL, Fraser AG, Kamath RS, et al. (2003) Genome-wide RNAi analysis of Caenorhabditis elegans fat regulatory genes. Nature 421: 268-272.
36. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403: 560-564.
37. Schroeder LK, Kremer S, Kramer MJ, Currie E, Kwan E, et al. (2007) Function of the Caenorhabditis elegans ABC transporter PGP-2 in the biogenesis of a lysosome-related fat storage organelle. Mol Biol Cell 18: 995-1008.
38. Ashrafi K (2007) Obesity and the regulation of fat metabolism. WormBook. pp 1-20.
39. Avery L, Shtonda BB (2003) Food transport in the C. elegans pharynx. J Exp Biol 206: 2441-2457.
40. McKay JP, Raizen DM, Gottschalk A, Schafer WR, Avery L (2004) eat-2 and eat-18 are required for nicotinic neurotransmission in the Caenorhabditis elegans pharynx. Genetics 166: 161-169.
41. Ray P, Schnabel R, Okkema PG (2008) Behavioral and synaptic defects in C. elegans lacking the NK-2 homeobox gene ceh-28. Dev Neurobiol 68: 421-433.
42. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L (1999) EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J Neurosci 19: 159-167.
43. Conradt B, Horvitz HR (1998) The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93: 519-529.
44. Rauthan M, Morck C, Pilon M (2007) The C. elegans M3 neuron guides the growth cone of its sister cell M2 via the Kruppel-like zinc finger protein MNM-2. Dev Biol 311: 185-199.
45. Shu X, Shaner NC, Yarbrough CA, Tsien RY, Remington SJ (2006) Novel chromophores and buried charges control color in mFruits. Biochemistry 45: 9639-9647.
46. Loukas A, Hintz M, Linder D, Mullin NP, Parkinson J, et al. (2000) A family of secreted mucins from the parasitic nematode Toxocara canis bears diverse mucin domains but shares similar flanking six-cysteine repeat motifs. J Biol Chem 275: 39600-39607.
47. Doedens A, Loukas A, Maizels RM (2001) A cDNA encoding Tc-MUC-5, a mucin from Toxocara canis larvae identified by expression screening. Acta Trop 79: 211-217.
48. Gems D, Maizels RM (1996) An abundantly expressed mucin-like protein from Toxocara canis infective larvae: the precursor of the larval surface coat glycoproteins. Proc Natl Acad Sci U S A 93: 1665-1670.
49. Julenius K, Molgaard A, Gupta R, Brunak S (2005) Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15: 153-164.
50. Wright KA, Thomson JN (1981) The buccal capsule of Caenorhabditis elegans (Nematoda: Rhabditoidea): an ultrastructural study. Canadian Journal Zool 59: 1952-1961.
51. Okkema PG, Harrison SW, Plunger V, Aryana A, Fire A (1993) Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135: 385-404.
52. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, et al. (2004) Sequential phases of cortical specification involve Neurogenin-dependent and - independent pathways. Embo J 23: 2892-2902.
53. Tapscott SJ (2005) The circuitry of a master switch: Myod and the regulation of skeletal muscle gene transcription. Development 132: 2685-2695.
54. Ma PC, Rould MA, Weintraub H, Pabo CO (1994) Crystal structure of MyoD bHLH domain-DNA complex: perspectives on DNA recognition and implications for transcriptional activation. Cell 77: 451-459.
55. Shimizu T, Toumoto A, Ihara K, Shimizu M, Kyogoku Y, et al. (1997) Crystal structure of PHO4 bHLH domain-DNA complex: flanking base recognition. Embo J 16: 4689-4697.
56. Castro DS, Skowronska-Krawczyk D, Armant O, Donaldson IJ, Parras C, et al. (2006) Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 11: 831-844.
57. Beres TM, Masui T, Swift GH, Shi L, Henke RM, et al. (2006) PTF1 is an organ-specific and Notch-independent basic helix-loop-helix complex containing the mammalian Suppressor of Hairless (RBP-J) or its paralogue, RBP-L. Mol Cell Biol 26: 117-130.
58. Cockell M, Stevenson BJ, Strubin M, Hagenbuchle O, Wellauer PK (1989) Identification of a cell-specific DNA-binding activity that interacts with a transcriptional activator of genes expressed in the acinar pancreas. Mol Cell Biol 9: 2464-2476.
59. Huang J, Blackwell TK, Kedes L, Weintraub H (1996) Differences between MyoD DNA binding and activation site requirements revealed by functional random sequence selection. Mol Cell Biol 16: 3893-3900.
60. Blackwell TK, Weintraub H (1990) Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection. Science 250: 1104-1110.
61. Wang P, Zhao J, Corsi AK (2006) Identification of novel target genes of CeTwist and CeE/DA. Dev Biol 293: 486-498.
62. Powell LM, Zur Lage PI, Prentice DR, Senthinathan B, Jarman AP (2004) The proneural proteins Atonal and Scute regulate neural target genes through different E-box binding sites. Mol Cell Biol 24: 9517-9526.
63. Hill AA, Riley PR (2004) Differential regulation of Hand1 homodimer and Hand1-E12 heterodimer activity by the cofactor FHL2. Mol Cell Biol 24: 9835-9847.
64. Acar M, Jafar-Nejad H, Giagtzoglou N, Yallampalli S, David G, et al. (2006) Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development 133: 1979-1989.
65. Zhao Z, Fang L, Chen N, Johnsen RC, Stein L, et al. (2005) Distinct regulatory elements mediate similar expression patterns in the excretory cell of Caenorhabditis elegans. J Biol Chem 280: 38787-38794.
66. Fukushige T, Brodigan TM, Schriefer LA, Waterston RH, Krause M (2006) Defining the transcriptional redundancy of early bodywall muscle development in C. elegans: evidence for a unified theory of animal muscle development. Genes Dev 20: 3395-3406.
67. Wenick AS, Hobert O (2004) Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev Cell 6: 757-770.
68. Yoshida S, Ohbo K, Takakura A, Takebayashi H, Okada T, et al. (2001) Sgn1, a basic helix-loop-helix transcription factor delineates the salivary gland duct cell lineage in mice. Dev Biol 240: 517-530.
69. Abrams EW, Mihoulides WK, Andrew DJ (2006) Fork head and Sage maintain a uniform and patent salivary gland lumen through regulation of two downstream target genes, PH4{alpha}SG1 and PH4{alpha}SG2. Development 133: 3517-3527.
70. Seipel K, Yanze N, Schmid V (2004) Developmental and evolutionary aspects of the basic helix-loop-helix transcription factors Atonal-like 1 and Achaete-scute homolog 2 in the jellyfish. Dev Biol 269: 331-345.
71. Davis EL, Hussey RS, Baum TJ, Bakker J, Schots A, et al. (2000) Nematode Parasitism Genes. Annu Rev Phytopathol 38: 365-396.
72. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
73. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
74. Mello CC, Kramer JM, Stinchcomb D, Ambros V (1991) Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10: 3959-3970.
75. Fukushige T, Hawkins MG, McGhee JD (1998) The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev Biol 198: 286-302.
76. Mello C, Fire A (1995) DNA transformation. Methods Cell Biol 48: 451-482.
77. Schnabel R, Hutter H, Moerman D, Schnabel H (1997) Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Dev Biol 184: 234-265.
78. Timmons L, Court DL, Fire A (2001) Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263: 103-112.
79. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 220-221.
80. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
81. Altun-Gultekin Z, Andachi Y, Tsalik EL, Pilgrim D, Kohara Y, et al. (2001) A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128: 1951-1969.
82. Portereiko MF, Mango SE (2001) Early morphogenesis of the Caenorhabditis elegans pharynx. Dev Biol 233: 482-494.
83. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.