Sequence Requirements for Myosin Gene Expression and Regulation in Caenorhabditis elegans

INVESTIGATIONS

Sequence Requirements for Myosin Gene Expression and Regulation in Caenorhabditis elegans

P. G. Okkema, S. W. Harrison, V. Plunger, A. Aryana and A. Fire
Carnegie Institution of Washington, Department of Embryology, Baltimore, Maryland 21210

Four Caenorhabditis elegans genes encode muscle-type specific myosin heavy chain isoforms: myo-1 and myo-2 are expressed in the pharyngeal muscles; unc-54 and myo-3 are expressed in body wall muscles. We have used transformation-rescue and lacZ fusion assays to determine sequence requirements for regulated myosin gene expression during development. Multiple tissue-specific activation elements are present for all four genes. For each of the four genes, sequences upstream of the coding region are tissue-specific promoters, as shown by their ability to drive expression of a reporter gene (lacZ) in the appropriate muscle type. Each gene contains at least one additional tissue-specific regulatory element, as defined by the ability to enhance expression of a heterologous promoter in the appropriate muscle type. In rescue experiments with unc-54, two further requirements apparently independent of tissue specificity were found: sequences within the 3' non-coding region are essential for activity while an intron near the 5' end augments expression levels. The general intron stimulation is apparently independent of intron sequence, indicating a mechanistic effect of splicing. To further characterize the myosin gene promoters and to examine the types of enhancer sequences in the genome, we have initiated a screen of C. elegans genomic DNA for fragments capable of enhancing the myo-2 promoter. The properties of enhancers recovered from this screen suggest that the promoter is limited to muscle cells in its ability to respond to enhancers.

This article has been cited by other articles:

C. Benard, N. Tjoe, T. Boulin, J. Recio, and O. Hobert
The Small, Secreted Immunoglobulin Protein ZIG-3 Maintains Axon Position in Caenorhabditis elegans
Genetics, November 1, 2009; 183(3): 917 - 927.
[Abstract] [Full Text] [PDF]

G. Broitman-Maduro, M. Owraghi, W. W. K. Hung, S. Kuntz, P. W. Sternberg, and M. F. Maduro
The NK-2 class homeodomain factor CEH-51 and the T-box factor TBX-35 have overlapping function in C. elegans mesoderm development
Development, August 15, 2009; 136(16): 2735 - 2746.
[Abstract] [Full Text] [PDF]

T. Kawano, H. Zheng, D. C. Merz, Y. Kohara, K. K. Tamai, K. Nishiwaki, and J. G. Culotti
C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV
Development, May 1, 2009; 136(9): 1433 - 1442.
[Abstract] [Full Text] [PDF]

H. Lei, J. Liu, T. Fukushige, A. Fire, and M. Krause
Caudal-like PAL-1 directly activates the bodywall muscle module regulator hlh-1 in C. elegans to initiate the embryonic muscle gene regulatory network
Development, April 15, 2009; 136(8): 1241 - 1249.
[Abstract] [Full Text] [PDF]

E. Marza, K. T. Simonsen, N. J. Faergeman, and G. M. Lesa
Expression of ceramide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells
J. Cell Sci., March 15, 2009; 122(6): 822 - 833.
[Abstract] [Full Text] [PDF]

V. M. Hapiak, R. J. Hobson, L. Hughes, K. Smith, G. Harris, C. Condon, P. Komuniecki, and R. W. Komuniecki
Dual Excitatory and Inhibitory Serotonergic Inputs Modulate Egg Laying in Caenorhabditis elegans
Genetics, January 1, 2009; 181(1): 153 - 163.
[Abstract] [Full Text] [PDF]

S. G. Kuntz, E. M. Schwarz, J. A. DeModena, T. De Buysscher, D. Trout, H. Shizuya, P. W. Sternberg, and B. J. Wold
Multigenome DNA sequence conservation identifies Hox cis-regulatory elements
Genome Res., December 1, 2008; 18(12): 1955 - 1968.
[Abstract] [Full Text] [PDF]

K. Ono, S. Yamashiro, and S. Ono
Essential role of ADF/cofilin for assembly of contractile actin networks in the C. elegans somatic gonad
J. Cell Sci., August 15, 2008; 121(16): 2662 - 2670.
[Abstract] [Full Text] [PDF]

W.-M. Woo, E. C. Berry, M. L. Hudson, R. E. Swale, A. Goncharov, and A. D. Chisholm
The C. elegans F-spondin family protein SPON-1 maintains cell adhesion in neural and non-neural tissues
Development, August 15, 2008; 135(16): 2747 - 2756.
[Abstract] [Full Text] [PDF]

H. Catoire, M. Y. Pasco, A. Abu-Baker, S. Holbert, C. Tourette, B. Brais, G. A. Rouleau, J. A. Parker, and C. Neri
Sirtuin inhibition protects from the polyalanine muscular dystrophy protein PABPN1
Hum. Mol. Genet., July 15, 2008; 17(14): 2108 - 2117.
[Abstract] [Full Text] [PDF]

A. B. Rose, T. Elfersi, G. Parra, and I. Korf
Promoter-Proximal Introns in Arabidopsis thaliana Are Enriched in Dispersed Signals that Elevate Gene Expression
PLANT CELL, March 1, 2008; 20(3): 543 - 551.
[Abstract] [Full Text] [PDF]

J. L. Green, T. Inoue, and P. W. Sternberg
The C. elegans ROR receptor tyrosine kinase, CAM-1, non-autonomously inhibits the Wnt pathway
Development, November 15, 2007; 134(22): 4053 - 4062.
[Abstract] [Full Text] [PDF]

Q. Liu, B. Chen, Q. Ge, and Z.-W. Wang
Presynaptic Ca2+/Calmodulin-Dependent Protein Kinase II Modulates Neurotransmitter Release by Activating BK Channels at Caenorhabditis elegans Neuromuscular Junction
J. Neurosci., September 26, 2007; 27(39): 10404 - 10413.
[Abstract] [Full Text] [PDF]

T. Bacaj and S. Shaham
Temporal Control of Cell-Specific Transgene Expression in Caenorhabditis elegans
Genetics, August 1, 2007; 176(4): 2651 - 2655.
[Abstract] [Full Text] [PDF]

G. Zhao, L. A. Schriefer, and G. D. Stormo
Identification of muscle-specific regulatory modules in Caenorhabditis elegans
Genome Res., March 1, 2007; 17(3): 348 - 357.
[Abstract] [Full Text] [PDF]

A. Hornsten, J. Lieberthal, S. Fadia, R. Malins, L. Ha, X. Xu, I. Daigle, M. Markowitz, G. O'Connor, R. Plasterk, et al.
APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability
PNAS, February 6, 2007; 104(6): 1971 - 1976.
[Abstract] [Full Text] [PDF]

D. Blanchard, H. Hutter, J. Fleenor, and A. Fire
A Differential Cytolocalization Assay for Analysis of Macromolecular Assemblies in the Eukaryotic Cytoplasm
Mol. Cell. Proteomics, November 1, 2006; 5(11): 2175 - 2184.
[Abstract] [Full Text] [PDF]

G. L. Fawcett, C. M. Santi, A. Butler, T. Harris, M. Covarrubias, and L. Salkoff
Mutant Analysis of the Shal (Kv4) Voltage-gated Fast Transient K+ Channel in Caenorhabditis elegans
J. Biol. Chem., October 13, 2006; 281(41): 30725 - 30735.
[Abstract] [Full Text] [PDF]

C. Dong, J. M. Muriel, S. Ramirez, H. Hutter, E. M. Hedgecock, L. Breydo, I. V. Baskakov, and B. E. Vogel
Hemicentin Assembly in the Extracellular Matrix Is Mediated by Distinct Structural Modules
J. Biol. Chem., August 18, 2006; 281(33): 23606 - 23610.
[Abstract] [Full Text] [PDF]

G. Broitman-Maduro, K. T.-H. Lin, W. W. K. Hung, and M. F. Maduro
Specification of the C. elegans MS blastomere by the T-box factor TBX-35
Development, August 15, 2006; 133(16): 3097 - 3106.
[Abstract] [Full Text] [PDF]

C. S. Walker, M. M. Francis, P. J. Brockie, D. M. Madsen, Y. Zheng, and A. V. Maricq
Conserved SOL-1 proteins regulate ionotropic glutamate receptor desensitization
PNAS, July 11, 2006; 103(28): 10787 - 10792.
[Abstract] [Full Text] [PDF]

S. J. Dixon, M. Alexander, R. Fernandes, N. Ricker, and P. J. Roy
FGF negatively regulates muscle membrane extension in Caenorhabditis elegans
Development, April 1, 2006; 133(7): 1263 - 1275.
[Abstract] [Full Text] [PDF]

Q. Liu, B. Chen, E. Gaier, J. Joshi, and Z.-W. Wang
Low Conductance Gap Junctions Mediate Specific Electrical Coupling in Body-wall Muscle Cells of Caenorhabditis elegans
J. Biol. Chem., March 24, 2006; 281(12): 7881 - 7889.
[Abstract] [Full Text] [PDF]

H. Wang, P. J. Lim, C. Yin, M. Rieckher, B. E. Vogel, and M. J. Monteiro
Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin
Hum. Mol. Genet., March 15, 2006; 15(6): 1025 - 1041.
[Abstract] [Full Text] [PDF]

L. Carnell, J. Illi, S. W. Hong, and S. L. McIntire
The G-Protein-Coupled Serotonin Receptor SER-1 Regulates Egg Laying and Male Mating Behaviors in Caenorhabditis elegans
J. Neurosci., November 16, 2005; 25(46): 10671 - 10681.
[Abstract] [Full Text] [PDF]

H. E. Sassi, S. Renihan, A. M. Spence, and R. L. Cooperstock
Gene CATCHR--Gene Cloning And Tagging for Caenorhabditis elegans using yeast Homologous Recombination: a novel approach for the analysis of gene expression
Nucleic Acids Res., October 27, 2005; 33(18): e163 - e163.
[Abstract] [Full Text] [PDF]

Q. Liu, B. Chen, M. Yankova, D. K. Morest, E. Maryon, A. R. Hand, M. L. Nonet, and Z.-W. Wang
Presynaptic Ryanodine Receptors Are Required for Normal Quantal Size at the Caenorhabditis elegans Neuromuscular Junction
J. Neurosci., July 20, 2005; 25(29): 6745 - 6754.
[Abstract] [Full Text] [PDF]

N. Watanabe, Y. Nagamatsu, K. Gengyo-Ando, S. Mitani, and Y. Ohshima
Control of body size by SMA-5, a homolog of MAP kinase BMK1/ERK5, in C. elegans
Development, July 15, 2005; 132(14): 3175 - 3184.
[Abstract] [Full Text] [PDF]

S. L. Hooper and J. B. Thuma
Invertebrate Muscles: Muscle Specific Genes and Proteins
Physiol Rev, July 1, 2005; 85(3): 1001 - 1060.
[Abstract] [Full Text] [PDF]

S. J. Dixon and P. J. Roy
Muscle arm development in Caenorhabditis elegans
Development, July 1, 2005; 132(13): 3079 - 3092.
[Abstract] [Full Text] [PDF]

D. GuhaThakurta, L. A. Schriefer, R. H. Waterston, and G. D. Stormo
Novel transcription regulatory elements in Caenorhabditis elegans muscle genes
Genome Res., December 1, 2004; 14(12): 2457 - 2468.
[Abstract] [Full Text] [PDF]

C. Y. Benard, H. Kebir, S. Takagi, and S. Hekimi
mau-2 acts cell-autonomously to guide axonal migrations in Caenorhabditis elegans
Development, December 1, 2004; 131(23): 5947 - 5958.
[Abstract] [Full Text] [PDF]

A. Anyanful, K. Ono, R. C. Johnsen, H. Ly, V. Jensen, D. L. Baillie, and S. Ono
The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in C. elegans
J. Cell Biol., November 22, 2004; 167(4): 639 - 647.
[Abstract] [Full Text] [PDF]

I. E. Sasson and M. J. Stern
FGF and PI3 kinase signaling pathways antagonistically modulate sex muscle differentiation in C. elegans
Development, November 1, 2004; 131(21): 5381 - 5392.
[Abstract] [Full Text] [PDF]

D. Dupuy, Q.-R. Li, B. Deplancke, M. Boxem, T. Hao, P. Lamesch, R. Sequerra, S. Bosak, L. Doucette-Stamm, I. A. Hope, et al.
A First Version of the Caenorhabditis elegans Promoterome
Genome Res., October 1, 2004; 14(10b): 2169 - 2175.
[Abstract] [Full Text] [PDF]

P. Huang and M. J. Stern
FGF signaling functions in the hypodermis to regulate fluid balance in C. elegans
Development, June 1, 2004; 131(11): 2595 - 2604.
[Abstract] [Full Text] [PDF]

M.-H. Lee and T. Schedl
Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans
Genes & Dev., May 1, 2004; 18(9): 1047 - 1059.
[Abstract] [Full Text] [PDF]

L. S. da Graca, K. K. Zimmerman, M. C. Mitchell, M. Kozhan-Gorodetska, K. Sekiewicz, Y. Morales, and G. I. Patterson,,
DAF-5 is a Ski oncoprotein homolog that functions in a neuronal TGF{beta} pathway to regulate C. elegans dauer development
Development, January 15, 2004; 131(2): 435 - 446.
[Abstract] [Full Text] [PDF]

J. P. McKay, D. M. Raizen, A. Gottschalk, W. R. Schafer, and L. Avery
eat-2 and eat-18 Are Required for Nicotinic Neurotransmission in the Caenorhabditis elegans Pharynx
Genetics, January 1, 2004; 166(1): 161 - 169.
[Abstract] [Full Text] [PDF]

I. P. de la Cruz, J. Z. Levin, C. Cummins, P. Anderson, and H. R. Horvitz
sup-9, sup-10, and unc-93 May Encode Components of a Two-Pore K+ Channel that Coordinates Muscle Contraction in Caenorhabditis elegans
J. Neurosci., October 8, 2003; 23(27): 9133 - 9145.
[Abstract] [Full Text] [PDF]

N. Moghal, L. R. Garcia, L. A. Khan, K. Iwasaki, and P. W. Sternberg
Modulation of EGF receptor-mediated vulva development by the heterotrimeric G-protein G{alpha}q and excitable cells in C. elegans
Development, October 1, 2003; 130(19): 4553 - 4566.
[Abstract] [Full Text] [PDF]

X. Huang, P. Huang, M. K. Robinson, M. J. Stern, and Y. Jin
UNC-71, a disintegrin and metalloprotease (ADAM) protein, regulates motor axon guidance and sex myoblast migration in C. elegans
Development, July 15, 2003; 130(14): 3147 - 3161.
[Abstract] [Full Text] [PDF]

D. S. Fay, E. Large, M. Han, and M. Darland
lin-35/Rb and ubc-18, an E2 ubiquitin-conjugating enzyme, function redundantly to control pharyngeal morphogenesis in C. elegans
Development, July 15, 2003; 130(14): 3319 - 3330.
[Abstract] [Full Text] [PDF]

T. Hirose, Y. Nakano, Y. Nagamatsu, T. Misumi, H. Ohta, and Y. Ohshima
Cyclic GMP-dependent protein kinase EGL-4 controls body size and lifespan in C. elegans
Development, March 15, 2003; 130(6): 1089 - 1099.
[Abstract] [Full Text] [PDF]

E. Stringham, N. Pujol, J. Vandekerckhove, and T. Bogaert
unc-53 controls longitudinal migration in C. elegans
Development, March 9, 2003; 129(14): 3367 - 3379.
[Abstract] [Full Text] [PDF]

O. Aurelio, T. Boulin, and O. Hobert
Identification of spatial and temporal cues that regulate postembryonic expression of axon maintenance factors in the C. elegans ventral nerve cord
Development, February 1, 2003; 130(3): 599 - 610.
[Abstract] [Full Text] [PDF]

S.J. MCKAY, R. JOHNSEN, J. KHATTRA, J. ASANO, D.L. BAILLIE, S. CHAN, N. DUBE, L. FANG, B. GOSZCZYNSKI, E. HA, et al.
Gene Expression Profiling of Cells, Tissues, and Developmental Stages of the Nematode C. elegans
Cold Spring Harb Symp Quant Biol, January 1, 2003; 68(0): 159 - 170.
[Abstract] [PDF]

T. Farrer, A. B. Roller, W. J. Kent, and A. M. Zahler
Analysis of the role of Caenorhabditis elegans GC-AG introns in regulated splicing
Nucleic Acids Res., August 1, 2002; 30(15): 3360 - 3367.
[Abstract] [Full Text] [PDF]

U. Pozzoli, M. Sironi, R. Cagliani, G. P. Comi, A. Bardoni, and N. Bresolin
Comparative Analysis of the Human Dystrophin and Utrophin Gene Structures
Genetics, February 1, 2002; 160(2): 793 - 798.
[Abstract] [Full Text] [PDF]

S. A. Kostas and A. Fire
The T-box factor MLS-1 acts as a molecular switch during specification of nonstriated muscle in C. elegans
Genes & Dev., January 15, 2002; 16(2): 257 - 269.
[Abstract] [Full Text] [PDF]

J. Wang, R. Tokarz, and C. Savage-Dunn
The expression of TGF{beta} signal transducers in the hypodermis regulates body size in C. elegans
Development, January 11, 2002; 129(21): 4989 - 4998.
[Abstract] [Full Text] [PDF]

A. D. Johnson, D. Fitzsimmons, J. Hagman, and H. M. Chamberlin
EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development
Development, August 1, 2001; 128(15): 2857 - 2865.
[Abstract] [Full Text] [PDF]

J. Kim, D. S. Poole, L. E. Waggoner, A. Kempf, D. S. Ramirez, P. A. Treschow, and W. R. Schafer
Genes Affecting the Activity of Nicotinic Receptors Involved in Caenorhabditis elegans Egg-Laying Behavior
Genetics, April 1, 2001; 157(4): 1599 - 1610.
[Abstract] [Full Text]

V. Praitis, E. Casey, D. Collar, and J. Austin
Creation of Low-Copy Integrated Transgenic Lines in Caenorhabditis elegans
Genetics, March 1, 2001; 157(3): 1217 - 1226.
[Abstract] [Full Text]

C. A. Wolkow, K. D. Kimura, M.-S. Lee, and G. Ruvkun
Regulation of C. elegans Life-Span by Insulinlike Signaling in the Nervous System
Science, October 6, 2000; 290(5489): 147 - 150.
[Abstract] [Full Text]

K. L. Hill, B. D. Harfe, C. A. Dobbins, and S. W. L'Hernault
dpy-18 Encodes an {alpha}-Subunit of Prolyl-4-Hydroxylase in Caenorhabditis elegans
Genetics, July 1, 2000; 155(3): 1139 - 1148.
[Abstract] [Full Text]

K. Nishiwaki, N. Hisamoto, and K. Matsumoto
A Metalloprotease Disintegrin That Controls Cell Migration in Caenorhabditis elegans
Science, June 23, 2000; 288(5474): 2205 - 2208.
[Abstract] [Full Text]

H. M. Robertson
The Large srh Family of Chemoreceptor Genes in Caenorhabditis Nematodes Reveals Processes of Genome Evolution Involving Large Duplications and Deletions and Intron Gains and Losses
Genome Res., February 1, 2000; 10(2): 192 - 203.
[Abstract] [Full Text]

A. B. Rose and J. A. Beliakoff
Intron-Mediated Enhancement of Gene Expression Independent of Unique Intron Sequences and Splicing
Plant Physiology, February 1, 2000; 122(2): 535 - 542.
[Abstract] [Full Text]

N. Szewczyk, J. Hartman, S. Barmada, and L. Jacobson
Genetic defects in acetylcholine signalling promote protein degradation in muscle cells of Caenorhabditis elegans
J. Cell Sci., January 6, 2000; 113(11): 2003 - 2010.
[Abstract] [PDF]

H Zhao and M. Nonet
A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction
Development, January 3, 2000; 127(6): 1253 - 1266.
[Abstract] [PDF]

B. Grant and D. Hirsh
Receptor-mediated Endocytosis in the Caenorhabditis elegans Oocyte
Mol. Biol. Cell, December 1, 1999; 10(12): 4311 - 4326.
[Abstract] [Full Text]

J. Hsieh, J. Liu, S. A. Kostas, C. Chang, P. W. Sternberg, and A. Fire
The RING finger/B-Box factor TAM-1 and a retinoblastoma-like protein LIN-35 modulate context-dependent gene silencing in Caenorhabditis elegans
Genes & Dev., November 15, 1999; 13(22): 2958 - 2970.
[Abstract] [Full Text]

J. Thatcher, C Haun, and P. Okkema
The DAF-3 Smad binds DNA and represses gene expression in the Caenorhabditis elegans pharynx
Development, January 1, 1999; 126(1): 97 - 107.
[Abstract] [PDF]

B. D. Harfe, A. V. Gomes, C. Kenyon, J. Liu, M. Krause, and A. Fire
Analysis of a Caenorhabditis elegans Twist homolog identifies conserved and divergent aspects of mesodermal patterning
Genes & Dev., August 15, 1998; 12(16): 2623 - 2635.
[Abstract] [Full Text]

A. Colavita, S. Krishna, H. Zheng, R. W. Padgett, and J. G. Culotti
Pioneer Axon Guidance by UNC-129, a C. elegans TGF- $beta$
Science, July 31, 1998; 281(5377): 706 - 709.
[Abstract] [Full Text]

H. M. Robertson
Two Large Families of Chemoreceptor Genes in the Nematodes Caenorhabditis elegans and Caenorhabditis briggsae Reveal Extensive Gene Duplication, Diversification, Movement, and Intron Loss
Genome Res., May 1, 1998; 8(5): 449 - 463.
[Abstract] [Full Text]

C. Haun, J. Alexander, D. Y. Stainier, and P. G. Okkema
Rescue of Caenorhabditis elegans pharyngeal development by a vertebrate heart specification gene
PNAS, April 28, 1998; 95(9): 5072 - 5075.
[Abstract] [Full Text] [PDF]

B. Harfe, C. Branda, M Krause, M. Stern, and A Fire
MyoD and the specification of muscle and non-muscle fates during postembryonic development of the C. elegans mesoderm
Development, January 7, 1998; 125(13): 2479 - 2488.
[Abstract] [PDF]

B. Harfe and A Fire
Muscle and nerve-specific regulation of a novel NK-2 class homeodomain factor in Caenorhabditis elegans
Development, January 2, 1998; 125(3): 421 - 429.
[Abstract] [PDF]

K. M. Neugebauer and M. B. Roth
Transcription units as RNA processing units
Genes & Dev., December 15, 1997; 11(24): 3279 - 3285.
[Full Text] [PDF]

J. T. Fleming, M. D. Squire, T. M. Barnes, C. Tornoe, K. Matsuda, J. Ahnn, A. Fire, J. E. Sulston, E. A. Barnard, D. B. Sattelle, et al.
Caenorhabditis elegans Levamisole Resistance Genes lev-1, unc-29, and unc-38 Encode Functional Nicotinic Acetylcholine Receptor Subunits
J. Neurosci., August 1, 1997; 17(15): 5843 - 5857.
[Abstract] [Full Text] [PDF]

P. L. Graham, J. J. Johnson, S. Wang, M. H. Sibley, M. C. Gupta, and J. M. Kramer
Type IV Collagen Is Detectable in Most, but Not All, Basement Membranes of Caenorhabditis elegans and Assembles on Tissues That Do Not Express It
J. Cell Biol., June 2, 1997; 137(5): 1171 - 1183.
[Abstract] [Full Text] [PDF]

P. Okkema, E Ha, C Haun, W Chen, and A Fire
The Caenorhabditis elegans NK-2 homeobox gene ceh-22 activates pharyngeal muscle gene expression in combination with pha-1 and is required for normal pharyngeal development
Development, January 10, 1997; 124(20): 3965 - 3973.
[Abstract] [PDF]

B Grant and I Greenwald
Structure, function, and expression of SEL-1, a negative regulator of LIN-12 and GLP-1 in C. elegans
Development, January 2, 1997; 124(3): 637 - 644.
[Abstract] [PDF]

K C Ferguson, P J Heid, and J H Rothman
The SL1 trans-spliced leader RNA performs an essential embryonic function in Caenorhabditis elegans that can also be supplied by SL2 RNA.
Genes & Dev., June 15, 1996; 10(12): 1543 - 1556.
[Abstract] [PDF]

J Ahringer
Posterior patterning by the Caenorhabditis elegans even-skipped homolog vab-7.
Genes & Dev., May 1, 1996; 10(9): 1120 - 1130.
[Abstract] [PDF]

S Strome, P Martin, E Schierenberg, and J Paulsen
Transformation of the germ line into muscle in mes-1 mutant embryos of C. elegans
Development, January 9, 1995; 121(9): 2961 - 2972.
[Abstract] [PDF]

P. Okkema and A Fire
The Caenorhabditis elegans NK-2 class homeoprotein CEH-22 is involved in combinatorial activation of gene expression in pharyngeal muscle
Development, January 8, 1994; 120(8): 2175 - 2186.
[Abstract] [PDF]

				G. Broitman-Maduro, M. Owraghi, W. W. K. Hung, S. Kuntz, P. W. Sternberg, and M. F. Maduro The NK-2 class homeodomain factor CEH-51 and the T-box factor TBX-35 have overlapping function in C. elegans mesoderm development Development, August 15, 2009; 136(16): 2735 - 2746. [Abstract] [Full Text] [PDF]

				T. Kawano, H. Zheng, D. C. Merz, Y. Kohara, K. K. Tamai, K. Nishiwaki, and J. G. Culotti C. elegans mig-6 encodes papilin isoforms that affect distinct aspects of DTC migration, and interacts genetically with mig-17 and collagen IV Development, May 1, 2009; 136(9): 1433 - 1442. [Abstract] [Full Text] [PDF]

				H. Lei, J. Liu, T. Fukushige, A. Fire, and M. Krause Caudal-like PAL-1 directly activates the bodywall muscle module regulator hlh-1 in C. elegans to initiate the embryonic muscle gene regulatory network Development, April 15, 2009; 136(8): 1241 - 1249. [Abstract] [Full Text] [PDF]

				E. Marza, K. T. Simonsen, N. J. Faergeman, and G. M. Lesa Expression of ceramide glucosyltransferases, which are essential for glycosphingolipid synthesis, is only required in a small subset of C. elegans cells J. Cell Sci., March 15, 2009; 122(6): 822 - 833. [Abstract] [Full Text] [PDF]

				V. M. Hapiak, R. J. Hobson, L. Hughes, K. Smith, G. Harris, C. Condon, P. Komuniecki, and R. W. Komuniecki Dual Excitatory and Inhibitory Serotonergic Inputs Modulate Egg Laying in Caenorhabditis elegans Genetics, January 1, 2009; 181(1): 153 - 163. [Abstract] [Full Text] [PDF]

				S. G. Kuntz, E. M. Schwarz, J. A. DeModena, T. De Buysscher, D. Trout, H. Shizuya, P. W. Sternberg, and B. J. Wold Multigenome DNA sequence conservation identifies Hox cis-regulatory elements Genome Res., December 1, 2008; 18(12): 1955 - 1968. [Abstract] [Full Text] [PDF]

				K. Ono, S. Yamashiro, and S. Ono Essential role of ADF/cofilin for assembly of contractile actin networks in the C. elegans somatic gonad J. Cell Sci., August 15, 2008; 121(16): 2662 - 2670. [Abstract] [Full Text] [PDF]

				W.-M. Woo, E. C. Berry, M. L. Hudson, R. E. Swale, A. Goncharov, and A. D. Chisholm The C. elegans F-spondin family protein SPON-1 maintains cell adhesion in neural and non-neural tissues Development, August 15, 2008; 135(16): 2747 - 2756. [Abstract] [Full Text] [PDF]

				H. Catoire, M. Y. Pasco, A. Abu-Baker, S. Holbert, C. Tourette, B. Brais, G. A. Rouleau, J. A. Parker, and C. Neri Sirtuin inhibition protects from the polyalanine muscular dystrophy protein PABPN1 Hum. Mol. Genet., July 15, 2008; 17(14): 2108 - 2117. [Abstract] [Full Text] [PDF]

				A. B. Rose, T. Elfersi, G. Parra, and I. Korf Promoter-Proximal Introns in Arabidopsis thaliana Are Enriched in Dispersed Signals that Elevate Gene Expression PLANT CELL, March 1, 2008; 20(3): 543 - 551. [Abstract] [Full Text] [PDF]

				J. L. Green, T. Inoue, and P. W. Sternberg The C. elegans ROR receptor tyrosine kinase, CAM-1, non-autonomously inhibits the Wnt pathway Development, November 15, 2007; 134(22): 4053 - 4062. [Abstract] [Full Text] [PDF]

				Q. Liu, B. Chen, Q. Ge, and Z.-W. Wang Presynaptic Ca2+/Calmodulin-Dependent Protein Kinase II Modulates Neurotransmitter Release by Activating BK Channels at Caenorhabditis elegans Neuromuscular Junction J. Neurosci., September 26, 2007; 27(39): 10404 - 10413. [Abstract] [Full Text] [PDF]

				T. Bacaj and S. Shaham Temporal Control of Cell-Specific Transgene Expression in Caenorhabditis elegans Genetics, August 1, 2007; 176(4): 2651 - 2655. [Abstract] [Full Text] [PDF]

				G. Zhao, L. A. Schriefer, and G. D. Stormo Identification of muscle-specific regulatory modules in Caenorhabditis elegans Genome Res., March 1, 2007; 17(3): 348 - 357. [Abstract] [Full Text] [PDF]

				A. Hornsten, J. Lieberthal, S. Fadia, R. Malins, L. Ha, X. Xu, I. Daigle, M. Markowitz, G. O'Connor, R. Plasterk, et al. APL-1, a Caenorhabditis elegans protein related to the human beta-amyloid precursor protein, is essential for viability PNAS, February 6, 2007; 104(6): 1971 - 1976. [Abstract] [Full Text] [PDF]

				D. Blanchard, H. Hutter, J. Fleenor, and A. Fire A Differential Cytolocalization Assay for Analysis of Macromolecular Assemblies in the Eukaryotic Cytoplasm Mol. Cell. Proteomics, November 1, 2006; 5(11): 2175 - 2184. [Abstract] [Full Text] [PDF]

				G. L. Fawcett, C. M. Santi, A. Butler, T. Harris, M. Covarrubias, and L. Salkoff Mutant Analysis of the Shal (Kv4) Voltage-gated Fast Transient K+ Channel in Caenorhabditis elegans J. Biol. Chem., October 13, 2006; 281(41): 30725 - 30735. [Abstract] [Full Text] [PDF]

				C. Dong, J. M. Muriel, S. Ramirez, H. Hutter, E. M. Hedgecock, L. Breydo, I. V. Baskakov, and B. E. Vogel Hemicentin Assembly in the Extracellular Matrix Is Mediated by Distinct Structural Modules J. Biol. Chem., August 18, 2006; 281(33): 23606 - 23610. [Abstract] [Full Text] [PDF]

				G. Broitman-Maduro, K. T.-H. Lin, W. W. K. Hung, and M. F. Maduro Specification of the C. elegans MS blastomere by the T-box factor TBX-35 Development, August 15, 2006; 133(16): 3097 - 3106. [Abstract] [Full Text] [PDF]

				C. S. Walker, M. M. Francis, P. J. Brockie, D. M. Madsen, Y. Zheng, and A. V. Maricq Conserved SOL-1 proteins regulate ionotropic glutamate receptor desensitization PNAS, July 11, 2006; 103(28): 10787 - 10792. [Abstract] [Full Text] [PDF]

				S. J. Dixon, M. Alexander, R. Fernandes, N. Ricker, and P. J. Roy FGF negatively regulates muscle membrane extension in Caenorhabditis elegans Development, April 1, 2006; 133(7): 1263 - 1275. [Abstract] [Full Text] [PDF]

				Q. Liu, B. Chen, E. Gaier, J. Joshi, and Z.-W. Wang Low Conductance Gap Junctions Mediate Specific Electrical Coupling in Body-wall Muscle Cells of Caenorhabditis elegans J. Biol. Chem., March 24, 2006; 281(12): 7881 - 7889. [Abstract] [Full Text] [PDF]

				H. Wang, P. J. Lim, C. Yin, M. Rieckher, B. E. Vogel, and M. J. Monteiro Suppression of polyglutamine-induced toxicity in cell and animal models of Huntington's disease by ubiquilin Hum. Mol. Genet., March 15, 2006; 15(6): 1025 - 1041. [Abstract] [Full Text] [PDF]

				L. Carnell, J. Illi, S. W. Hong, and S. L. McIntire The G-Protein-Coupled Serotonin Receptor SER-1 Regulates Egg Laying and Male Mating Behaviors in Caenorhabditis elegans J. Neurosci., November 16, 2005; 25(46): 10671 - 10681. [Abstract] [Full Text] [PDF]

				H. E. Sassi, S. Renihan, A. M. Spence, and R. L. Cooperstock Gene CATCHR--Gene Cloning And Tagging for Caenorhabditis elegans using yeast Homologous Recombination: a novel approach for the analysis of gene expression Nucleic Acids Res., October 27, 2005; 33(18): e163 - e163. [Abstract] [Full Text] [PDF]

				Q. Liu, B. Chen, M. Yankova, D. K. Morest, E. Maryon, A. R. Hand, M. L. Nonet, and Z.-W. Wang Presynaptic Ryanodine Receptors Are Required for Normal Quantal Size at the Caenorhabditis elegans Neuromuscular Junction J. Neurosci., July 20, 2005; 25(29): 6745 - 6754. [Abstract] [Full Text] [PDF]

				N. Watanabe, Y. Nagamatsu, K. Gengyo-Ando, S. Mitani, and Y. Ohshima Control of body size by SMA-5, a homolog of MAP kinase BMK1/ERK5, in C. elegans Development, July 15, 2005; 132(14): 3175 - 3184. [Abstract] [Full Text] [PDF]

				S. L. Hooper and J. B. Thuma Invertebrate Muscles: Muscle Specific Genes and Proteins Physiol Rev, July 1, 2005; 85(3): 1001 - 1060. [Abstract] [Full Text] [PDF]

				S. J. Dixon and P. J. Roy Muscle arm development in Caenorhabditis elegans Development, July 1, 2005; 132(13): 3079 - 3092. [Abstract] [Full Text] [PDF]

				D. GuhaThakurta, L. A. Schriefer, R. H. Waterston, and G. D. Stormo Novel transcription regulatory elements in Caenorhabditis elegans muscle genes Genome Res., December 1, 2004; 14(12): 2457 - 2468. [Abstract] [Full Text] [PDF]