Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-27T11:13:56.421Z Has data issue: false hasContentIssue false
  • English
  • Français

The use of Caenorhabditis elegans in parasitic nematode research

Published online by Cambridge University Press:  12 May 2005

J. S. GILLEARD
J. S. GILLEARD
Affiliation:
Department of Veterinary Parasitology, Institute of Comparative Medicine, Faculty of Veterinary Medicine, University of Glasgow, Glasgow, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

There is increasing interest in the use of the free-living nematode Caenorhabditis elegans as a tool for parasitic nematode research and there are now a number of compelling examples of its successful application. C. elegans has the potential to become a standard tool for molecular helminthology researchers, just as yeast is routinely used by molecular biologists to study vertebrate biology. However, in order to exploit C. elegans in a meaningful manner, we need a detailed understanding of the extent to which different aspects of C. elegans biology have been conserved with particular groups of parasitic nematodes. This review first considers the current state of knowledge regarding the conservation of genome organisation across the nematode phylum and then discusses some recent evolutionary development studies in free-living nematodes. The aim is to provide some important concepts that are relevant to the extrapolation of information from C. elegans to parasitic nematodes and also to the interpretation of experiments that use C. elegans as a surrogate expression system. In general, examples have been specifically chosen because they highlight the importance of careful experimentation and interpretation of data. Consequently, the focus is on the differences that have been found between nematode species rather than the similarities. Finally, there is a detailed discussion of the current status of C. elegans as a heterologous expression system to study parasite gene function and regulation using successful examples from the literature.

Keywords

NematodegenomicsevolutionparasiteCaenorhabditis
Type
Research Article
Information
Parasitology , Volume 128 , Issue S1 , October 2004 , pp. S49 - S70
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AAMODT, E. J., CHUNG, M. A. & McGHEE, J. D. ( 1991). Spatial control of gut-specific gene expression during Caenorhabditis elegans development. Science 252, 579–582.CrossRefGoogle Scholar
ABOOBAKER, A. & BLAXTER, M. ( 2003 a). Hox gene evolution in nematodes: novelty conserved. Current Opinion in Genetics and Development 13, 593–598.Google Scholar
ABOOBAKER, A. A. & BLAXTER, M. L. ( 2003 b). Use of RNA interference to investigate gene function in the human filarial nematode parasite Brugia malayi. Molecular and Biochemical Parasitology 129, 41–51.Google Scholar
ALLEN, J. E., DAUB, J., GUILIANO, D., McDONNELL, A., LIZOTTE-WANIEWSKI, M., TAYLOR, D. W. & BLAXTER, M. ( 2000). Analysis of genes expressed at the infective larval stage validates utility of Litomosoides sigmodontis as a murine model for filarial vaccine development. Infection and Immunity 68, 5454–5458.CrossRefGoogle Scholar
BIRD, D. M., OPPERMAN, C. H., JONES, S. J. & BAILLIE, D. L. ( 1999). the caenorhabditis elegans genome: A Guide in The Post Genomics Age. Annual Review of Phytopathology 37, 247–265.CrossRefGoogle Scholar
BLAXTER, M. ( 1998). Caenorhabditis elegans is a nematode. Science 282, 2041–2046.CrossRefGoogle Scholar
BLAXTER, M. ( 2002). Molecular analysis of nematode evolution. In Parasitic Nematodes. Molecular Biology, Biochemistry and Immunology (ed. Kennedy, M. & Harnett, W.), pp. 1–25. CABI publishing, Oxford.
BLAXTER, M. L., DE LEY, P., GAREY, J. R., LIU, L. X., SCHELDEMAN, P., VIERSTRAETE, A., VANFLETEREN, J. R., MACKEY, L. Y., DORRIS, M., FRISSE, L. M., VIDA, J. T. & THOMAS, W. K. ( 1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.CrossRefGoogle Scholar
BLAXTER, M. & LIU, L. ( 1996). Nematode spliced leaders – ubiquity, evolution and utility. International Journal for Parasitology 26, 1025–1033.Google Scholar
BLUMENTHAL, T., EVANS, D., LINK, C. D., GUFFANTI, A., LAWSON, D., THIERRY-MIEG, J., THIERRY-MIEG, D., CHIU, W. L., DUKE, K., KIRALY, M. & KIM, S. K. ( 2002). A global analysis of Caenorhabditis elegans operons. Nature 417, 851–854.CrossRefGoogle Scholar
BLUMENTHAL, T. & GLEASON, K. S. ( 2003). Caenorhabditis elegans operons: form and function. Nature Review Genetics 4, 112–120.CrossRefGoogle Scholar
BOYLE, J. P. & YOSHINO, T. P. ( 2003). Gene manipulation in parasitic helminths. International Journal for Parasitology 33, 1259–1268.CrossRefGoogle Scholar
BRITTON, C. & MURRAY, L. ( 2002). A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Molecular and Biochemical Parasitology 122, 21–33.CrossRefGoogle Scholar
BRITTON, C., REDMOND, D. L., KNOX, D. P., McKERROW, J. H. & BARRY, J. D. ( 1999). Identification of promoter elements of parasite nematode genes in transgenic Caenorhabditis elegans. Molecular and Biochemical Parasitology 103, 171–181.CrossRefGoogle Scholar
BROOKS, D. R. & ISAAC, R. E. ( 2002). Functional genomics of parasitic worms: the dawn of a new era. Parasitology International 51, 319–325.CrossRefGoogle Scholar
BURGLIN, T. R., LOBOS, E. & BLAXTER, M. L. ( 1998). Caenorhabditis elegans as a model for parasitic nematodes. International Journal for Parasitology 28, 395–411.CrossRefGoogle Scholar
CALLAHAN, H., CROUCH, R. & JAMES, E. ( 1988). Helminth anti-oxidant enzymes: a protective mechanism against host oxidants? Parasitology Today 4, 218–225.Google Scholar
CHANG, C. & STERNBERG, P. W. ( 1999). C. elegans vulval development as a model system to study the cancer biology of EGFR signaling. Cancer Metastasis Review 18, 203–213.Google Scholar
CLADININ, T. R., KATZ, W. S. & STERNBERG, P. W. ( 1997). Caenorhabditis elegans hom-c genes regulate the response of vulval precursor cells to inductive signal. Developmental Biology 182, 150–161.CrossRefGoogle Scholar
CLARK, S. G., CHISHOLM, A. D. & HORVITZ, H. R. ( 1993). Control of cell fates in the central body region of C. elegans by the homeobox gene lin-39. Cell 74, 43–55.Google Scholar
COGHLAN, A. & WOLFE, K. H. ( 2002). Fourfold faster rate of genome rearrangement in nematodes than in Drosophila. Genome Research 12, 857–867.CrossRefGoogle Scholar
CONNOLLY, B., TRENHOLME, K. & SMITH, D. F. ( 1996). Molecular cloning of a myod-like gene from the parasitic nematode, Trichinella spiralis. Molecular and Biochemical Parasitology 81, 137–149.CrossRefGoogle Scholar
COUTHIER, A., SMITH, J., McGARR, P., CRAIG, B. & GILLEARD, J. S. ( 2004). Ectopic expression of a Haemonchus contortus GATA transcription factor in Caenorhabditis elegans reveals conserved function in spite of extensive sequence divergence. Molecular and Biochemical Parasitology 133, 241–253.CrossRefGoogle Scholar
DAVIDSON, E. ( 2001). Genomic Regulatory Systems: Development and Evolution. Academic Press, San Diego, CA.
DAVIS, R. E., PARRA, A., LOVERDE, P. T., RIBEIRO, E., GLORIOSO, G. & HODGSON, S. ( 1999). Transient expression of DNA and RNA in parasitic helminths by using particle bombardment. Proceedings of the National Academy of Sciences, USA 96, 8687–8692.CrossRefGoogle Scholar
DE BONO, M. & HODGKIN, J. ( 1996). Evolution of sex determination in Caenorhabditis: unusually high divergence of tra-1 and its functional consequences. Genetics 144, 587–595.Google Scholar
DORRIS, M., DE LEY, P. & BLAXTER, M. L. ( 1999). Molecular analysis of nematode diversity and the evolution of parasitism. Parasitology Today 15, 188–193.CrossRefGoogle Scholar
DRISCOLL, M., DEAN, E., REILLY, E., BERGHOLZ, E. & CHALFIE, M. ( 1989). Genetic and molecular analysis of a Caenorhabditis elegans beta-tubulin that conveys benzimidazole sensitivity. Journal of Cell Biology 109, 2993–3003.CrossRefGoogle Scholar
DUGGAN, A., MA, C. & CHALFIE, M. ( 1998). Regulation of touch receptor differentiation by the Caenorhabditis elegans mec-3 and unc-86 genes. Development 125, 4107–4119.Google Scholar
EDGLEY, M., BAILLIE, D., RIDDLE, D. & AM, R. ( 1995). Genetic Balancers. In Caenorhabditis elegans Modern Biological Analysis of an Organism (ed. H. F. Epstein & D. C. Shakes), vol. 48, pp. 148–182. Academic Press, San Diego.
EGAN, C. R., CHUNG, M. A., ALLEN, F. L., HESCHL, M. F., VAN BUSKIRK, C. L. & Mcghee, J. D. ( 1995). A gut-to-pharynx/tail switch in embryonic expression of the Caenorhabditis elegans ges-1 gene centers on two GATA sequences. Developmental Biology 170, 397–419.CrossRefGoogle Scholar
EIZINGER, A., JUNGBLUT, B. & SOMMER, R. J. ( 1999). Evolutionary change in the functional specificity of genes. Trends in Genetics 15, 197–202.CrossRefGoogle Scholar
EIZINGER, A. & SOMMER, R. J. ( 1997). The homeotic gene lin-39 and the evolution of nematode epidermal cell fates. Science 278, 452–455.CrossRefGoogle Scholar
EVANS, D., ZORIO, D., MacMORRIS, M., WINTER, C. E., LEA, K. & BLUMENTHAL, T. ( 1997). Operons and SL2 trans-splicing exist in nematodes outside the genus Caenorhabditis. Proceedings of the National Academy of Sciences, USA 94, 9751–9756.CrossRefGoogle Scholar
FIRE, A., XU, S., MONTGOMERY, M. K., KOSTAS, S. A., DRIVER, S. E. & MELLO, C. C. ( 1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806–811.CrossRefGoogle Scholar
FUKUSHIGE, T., HAWKINS, M. G. & McGHEE, J. D. ( 1998). The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Developmental Biology 198, 286–302.CrossRefGoogle Scholar
GAO, D. & KIMBLE, J. ( 1995). APX-1 can substitute for its homolog LAG-2 to direct cell interactions throughout Caenorhabditis elegans development. Proceedings of the National Academy of Sciences, USA 92, 9839–9842.CrossRefGoogle Scholar
GEARY, T. G. & THOMPSON, D. P. ( 2001). Caenorhabditis elegans: how good a model for veterinary parasites? Veterinary Parasitology 101, 371–386.Google Scholar
GILLEARD, J. S., BARRY, J. D. & JOHNSTONE, I. L. ( 1997). Cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen gene dpy-7. Molecular Cell Biology 17, 2301–2311.CrossRefGoogle Scholar
GILLEARD, J. S. & McGHEE, J. D. ( 2001). Activation of hypodermal differentiation in the Caenorhabditis elegans embryo by GATA transcription factors ELT-1 and ELT-3. Molecular Cell Biology 21, 2533–2544.CrossRefGoogle Scholar
GOLDSTEIN, B. ( 1992). Induction of gut in Caenorhabditis elegans embryos. Nature 357, 255–257.CrossRefGoogle Scholar
GOLDSTEIN, B. ( 2001). On the evolution of early development in the Nematoda. Philosophical Transactions of the Royal Society London B Biological Sciences 356, 1521–1531.CrossRefGoogle Scholar
GOMEZ-ESCOBAR, N., GREGORY, W. F., BRITTON, C., MURRAY, L., CORTON, C., HALL, N., DAUB, J., BLAXTER, M. L. & MAIZELS, R. M. ( 2002). Abundant larval transcript-1 and -2 genes from Brugia malayi: diversity of genomic environments but conservation of 5′ promoter sequences functional in Caenorhabditis elegans. Molecular and Biochemical Parasitology 125, 59–71.CrossRefGoogle Scholar
GRANDIEN, K. & SOMMER, R. J. ( 2001). Functional comparison of the nematode Hox gene lin-39 in C. elegans and P. pacificus reveals evolutionary conservation of protein function despite divergence of primary sequences. Genes and Development 15, 2161–2172.Google Scholar
GREENVALD, I. ( 1997). Development of the Vulva. In C. elegans II (ed. Riddle, D., Blumenthal, T., Meyer, B. J. & Preiss, J. R.), pp. 519–542. Cold Spring Harbour Laboratory Press.
GREGORY, W. F., ATMADJA, A. K., ALLEN, J. E. & MAIZELS, R. M. ( 2000). The abundant larval transcript-1 and -2 genes of Brugia malayi encode stage-specific candidate vaccine antigens for filariasis. Infection and Immunity 68, 4174–4179.CrossRefGoogle Scholar
GUILIANO, D. B., HALL, N., JONES, S. J., CLARK, L. N., CORTON, C. H., BARRELL, B. G. & BLAXTER, M. L. ( 2002). Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes. Genome Biology 3, RESEARCH0057, 1–14.Google Scholar
HAAG, E. S., WANG, S. & KIMBLE, J. ( 2002). Rapid coevolution of the nematode sex-determining genes fem-3 and tra-2. Current Biology 12, 2035–2041.CrossRefGoogle Scholar
HARFE, B. D. & FIRE, A. ( 1998). Muscle and nerve-specific regulation of a novel NK-2 class homeodomain factor in Caenorhabditis elegans. Development 125, 421–429.Google Scholar
HASHMI, S., TAWE, W. & LUSTIGMAN, S. ( 2001). Caenorhabditis elegans and the study of gene function in parasites. Trends in Parasitology 17, 387–393.CrossRefGoogle Scholar
HIGAZI, T. B., MERRIWEATHER, A., SHU, L., DAVIS, R. & UNNASCH, T. R. ( 2002). Brugia malayi: transient transfection by microinjection and particle bombardment. Experimental Parasitology 100, 95–102.CrossRefGoogle Scholar
HOBERT, O. ( 2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728–730.Google Scholar
HOUGH, R. F., LINGAM, A. T. & BASS, B. L. ( 1999). Caenorhabditis elegans mRNAs that encode a protein similar to ADARs derive from an operon containing six genes. Nucleic Acids Research 27, 3424–3432.CrossRefGoogle Scholar
HOUTHOOFD, W., JACOBSEN, K., MERTENS, C., VANGESTEL, S., COOMANS, A. & BORGONIE, G. ( 2003). Embryonic cell lineage of the marine nematode Pellioditis marina. Developmental Biology 258, 57–69.CrossRefGoogle Scholar
HUANG, L. S., TZOU, P. & STERNBERG, P. W. ( 1994). The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development. Molecular Biology of the Cell 5, 395–411.CrossRefGoogle Scholar
HUSSEIN, A. S., KICHENIN, K. & SELKIRK, M. E. ( 2002). Suppression of secreted acetylcholinesterase expression in Nippostrongylus brasiliensis by RNA interference. Molecular and Biochemical Parasitology 122, 91–94.CrossRefGoogle Scholar
JACKSTADT, P., WILM, T. P., ZAHNER, H. & HOBOM, G. ( 1999). Transformation of nematodes via ballistic DNA transfer. Molecular and Biochemical Parasitology 103, 261–266.CrossRefGoogle Scholar
JOSEPH, G. T., HUIMA, T. & LUSTIGMAN, S. ( 1998). Characterization of an Onchocerca volvulus L3-specific larval antigen, Ov-ALT-1. Molecular and Biochemical Parasitology 96, 177–183.CrossRefGoogle Scholar
JUNGBLUT, B. & SOMMER, R. J. ( 1998). The Pristionchus pacificus mab-5 gene is involved in the regulation of ventral epidermal cell fates. Current Biology 8, 775–778.CrossRefGoogle Scholar
KAMATH, R. S., FRASER, A. G., DONG, Y., POULIN, G., DURBIN, R., GOTTA, M., KANAPIN, A., LE BOT, N., MORENO, S., SOHRMANN, M., WELCHMAN, D. P., ZIPPERLEN, P. & AHRINGER, J. ( 2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231–237.CrossRefGoogle Scholar
KAMPKOTTER, A., VOLKMANN, T. E., DE CASTRO, S. H., LEIERS, B., KLOTZ, L. O., JOHNSON, T. E., LINK, C. D. & HENKLE-DUHRSEN, K. ( 2003). Functional analysis of the glutathione S-transferase 3 from Onchocerca volvulus (Ov-GST-3): a parasite GST confers increased resistance to oxidative stress in Caenorhabditis elegans. Journal of Molecular Biology 325, 25–37.CrossRefGoogle Scholar
KELLY, W. G., XU, S., MONTGOMERY, M. K. & FIRE, A. ( 1997). Distinct requirements for somatic and germline expression of a generally expressed Caenrorhabditis elegans gene. Genetics 146, 227–238.Google Scholar
KENT, W. J. & ZAHLER, A. M. ( 2000). Conservation, regulation, synteny, and introns in a large-scale C. briggsae–C. elegans genomic alignment. Genome Research 10, 1115–1125.Google Scholar
KOH, K., PEYROT, S. M., WOOD, C. G., WAGMAISTER, J. A., MADURO, M. F., EISENMANN, D. M. & ROTHMAN, J. H. ( 2002). Cell fates and fusion in the C. elegans vulval primordium are regulated by the EGL-18 and ELT-6 GATA factors – apparent direct targets of the LIN-39 Hox protein. Development 129, 5171–5180.Google Scholar
KRAUSE, M., HARRISON, S. W., XU, S. Q., CHEN, L. & FIRE, A. ( 1994). Elements regulating cell- and stage-specific expression of the C. elegans MyoD family homolog hlh-1. Developmental Biology 166, 133–148.Google Scholar
KUWABARA, P. E. & SHAH, S. ( 1994). Cloning by synteny: identifying C. briggsae homologues of C. elegans genes. Nucleic Acids Research 22, 4414–4418.Google Scholar
KWA, M. S., VEENSTRA, J. G. & ROOS, M. H. ( 1994). Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in beta-tubulin isotype 1. Molecular and Biochemical Parasitology 63, 299–303.CrossRefGoogle Scholar
KWA, M. S., VEENSTRA, J. G., VAN DIJK, M. & ROOS, M. H. ( 1995). Beta-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans. Journal of Molecular Biology 246, 500–510.CrossRefGoogle Scholar
LAMBIE, E. J. & KIMBLE, J. ( 1991). Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 112, 231–240.Google Scholar
LARKIN, D. M., EVERTS-VAN DER WIND, A., REBEIZ, M., SCHWEITZER, P. A., BACHMAN, S., GREEN, C., WRIGHT, C. L., CAMPOS, E. J., BENSON, L. D., EDWARDS, J., LIU, L., OSOEGAWA, K., WOMACK, J. E., DE JONG, P. J. & LEWIN, H. A. ( 2003). A cattle-human comparative map built with cattle BAC-ends and human genome sequence. Genome Research 13, 1966–1972.Google Scholar
LEE, K. Z., EIZINGER, A., NANDAKUMAR, R., SCHUSTER, S. C. & SOMMER, R. J. ( 2003). Limited microsynteny between the genomes of Pristionchus pacificus and Caenorhabditis elegans. Nucleic Acids Research 31, 2553–2560.CrossRefGoogle Scholar
LEE, K. Z. & SOMMER, R. J. ( 2003). Operon structure and trans splicing in the nematode Pristionchus pacificus. Molecular Biology and Evolution, 20, 2097–2103.CrossRefGoogle Scholar
LERCHER, M. J., BLUMENTHAL, T. & HURST, L. D. ( 2003). Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Research 13, 238–243.CrossRefGoogle Scholar
LEROY, S., DUPERRAY, C. & MORAND, S. ( 2003). Flow cytometry for parasite nematode genome size measurement. Molecular and Biochemical Parasitology 128, 91–93.CrossRefGoogle Scholar
LI, X. & GREENWALD, I. ( 1997). HOP-1, a Caenorhabditis elegans presenilin, appears to be functionally redundant with SEL-12 presenilin and to facilitate LIN-12 and GLP-1 signaling. Proceedings of the National Academy of Sciences, USA 94, 12204–12209.CrossRefGoogle Scholar
LIEBAU, E., ESCHBACH, M. L., TAWE, W., SOMMER, A., FISCHER, P., WALTER, R. D. & HENKLE-DUHRSEN, K. ( 2000). Identification of a stress-responsive Onchocerca volvulus glutathinone S-transferase (Ov-GST-3) by RT-PCR differential display. Molecular and Biochemical Parasitology 109, 101–110.CrossRefGoogle Scholar
LOK, J. B. & MASSEY, H. C. Jr. ( 2002). Transgene expression in Strongyloides stercoralis following gonadal microinjection of DNA constructs. Molecular and Biochemical Parasitology 119, 279–284.CrossRefGoogle Scholar
LUDWIG, M. Z., BERGMAN, C., PATEL, N. H. & KREITMAN, M. ( 2000). Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403, 564–567.CrossRefGoogle Scholar
MADURO, M. & PILGRIM, D. ( 1996). Conservation of function and expression of unc-119 from two Caenorhabditis species despite divergence of non-coding DNA. Gene 183, 77–85.CrossRefGoogle Scholar
MALOOF, J. N. & KENYON, C. ( 1998). The Hox gene lin-39 is required during C. elegans vulval induction to select the outcome of Ras signaling. Development 125, 181–190.Google Scholar
MARSHALL, S. D. & McGHEE, J. D. ( 2001). Coordination of ges-1 expression between the Caenorhabditis pharynx and intestine. Developmental Biology 239, 350–363.CrossRefGoogle Scholar
McGHEE, J. D. ( 1995). Cell fate decisions in the early embryo of the nematode Caenorhabditis elegans. Developmental Genetics 17, 155–166.CrossRefGoogle Scholar
MELLO, C. C., DRAPER, B. W. & PRIESS, J. R. ( 1994). The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77, 95–106.CrossRefGoogle Scholar
MELLO, C. C. & FIRE, A. ( 1995). DNA transformation. In Caenorhabditis elegans: Modern Biological Analysis of an Organism (ed. H. F. Epstein & D. C. Shakes), vol. 48, pp. 452–480. Academic Press, San Diego.
NILSSON, L., TIENSUU, T. & TUCK, S. ( 2000). Caenorhabditis elegans lin-25: a study of its role in multiple cell fate specification events involving Ras and the identification and characterization of evolutionarily conserved domains. Genetics 156, 1083–1096.Google Scholar
OKKEMA, P. G., HARRISON, S. W., PLUNGER, V., ARYANA, A. & FIRE, A. ( 1993). Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385–404.Google Scholar
PAGE, A. P. ( 1997). Cyclophilin and protein disulfide isomerase genes are co-transcribed in a functionally related manner in Caenorhabditis elegans. DNA and Cell Biology 16, 1335–1343.CrossRefGoogle Scholar
PUTCHA, G. V. & JOHNSON, E. M. ( 2004). ‘Men are but worms:’ (small star, filled) neuronal cell death in C. elegans and vertebrates. Cell Death and Differentiation 11, 38–48.CrossRefGoogle Scholar
QIN, L., SMANT, G., STOKKERMANS, J., BAKKER, J., SCHOTS, A. & HELDER, J. ( 1998). Cloning of a trans-spliced glyceraldehyde-3-phosphate-dehydrogenase gene from the potato cyst nematode Globodera rostochiensis and expression of its putative promoter region in Caenorhabditis elegans. Molecular and Biochemical Parasitology 96, 59–67.CrossRefGoogle Scholar
QUINTIN, S., MICHAUX, G., McMAHON, L., GANSMULLER, A. & LABOUESSE, M. ( 2001). The Caenorhabditis elegans gene lin-26 can trigger epithelial differentiation without conferring tissue specificity. Developmental Biology 235, 410–421.CrossRefGoogle Scholar
RANZ, J. M., CASALS, F. & RUIZ, A. ( 2001). How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila. Genome Research 11, 230–239.CrossRefGoogle Scholar
REDMOND, D. L., CLUCAS, C., JOHNSTONE, I. L. & KNOX, D. P. ( 2001). Expression of Haemonchus contortus pepsinogen in Caenorhabditis elegans. Molecular and Biochemical Parasitology 112, 125–131.CrossRefGoogle Scholar
REDMOND, D. L. & KNOX, D. P. ( 2001). Haemonchus contortus SL2 trans-spliced RNA leader sequence. Molecular and Biochemical Parasitology 117, 107–110.CrossRefGoogle Scholar
ROSEN, G. M., POU, S., RAMOS, C. L., COHEN, M. S. & BRITIGAN, B. E. ( 1995). Free radicals and phagocytic cells. Faseb Journal 9, 200–209.CrossRefGoogle Scholar
RUDEL, D. & KIMBLE, J. ( 2001). Conservation of glp-1 regulation and function in nematodes. Genetics 157, 639–654.Google Scholar
RUVINSKY, I. & RUVKUN, G. ( 2003). Functional tests of enhancer conservation between distantly related species. Development 130, 5133–5142.CrossRefGoogle Scholar
SALINAS, A. E. & WONG, M. G. ( 1999). Glutathione S-transferases – a review. Current Medicinal Chemistry 6, 279–309.Google Scholar
SHABALINA, S. A. & KONDRASHOV, A. S. ( 1999). Pattern of selective constraint in C. elegans and C. briggsae genomes. Genetics Research 74, 23–30.Google Scholar
SKIBA, F. & SCHIERENBERG, E. ( 1992). Cell lineages, developmental timing, and spatial pattern formation in embryos of free-living soil nematodes. Developmental Biology 151, 597–610.CrossRefGoogle Scholar
SOMMER, R. J., EIZINGER, A., LEE, K. Z., JUNGBLUT, B., BUBECK, A. & SCHLAK, I. ( 1998). The Pristionchus hox gene Ppa-lin-39 inhibits programmed cell death to specify the vulva equivalence group and is not required during vulval induction. Development 125, 3865–3873.Google Scholar
STEIN, L. D., BAO, Z., BLASIAR, D., BLUMENTHAL, T., BRENT, M. R., CHEN, N., CHINWALLA, A., CLARKE, L., CLEE, C., COGHLAN, A., COULSON, A., D'EUSTACHIO, P., FITCH, D. H., FULTON, L. A., FULTON, R. E., GRIFFITHS-JONES, S., HARRIS, T. W., HILLIER, L. W., KAMATH, R., KUWABARA, P. E., MARDIS, E. R., MARRA, M. A., MINER, T. L., MINX, P., MULLIKIN, J. C., PLUMB, R. W., ROGERS, J., SCHEIN, J. E., SOHRMANN, M., SPIETH, J., STAJICH, J. E., WEI, C., WILLEY, D., WILSON, R. K., DURBIN, R. & WATERSTON, R. H. ( 2003). The genome sequence of Caenorhabditis briggsae: A platform for comparative genomics. PLoS Biology 1, E45.CrossRefGoogle Scholar
STONE, J. R. & WRAY, G. A. ( 2001). Rapid evolution of cis-regulatory sequences via local point mutations. Molecular Biology and Evolution 18, 1764–1770.CrossRefGoogle Scholar
STOTHARD, P. & PILGRIM, D. ( 2003). Sex-determination gene and pathway evolution in nematodes. Bioessays 25, 221–231.CrossRefGoogle Scholar
STRINGHAM, E. G., DIXON, D. K., JONES, D. & CANDIDO, E. P. ( 1992). Temporal and spatial expression patterns of the small heat shock (hsp 16) genes in transgenic Caenorhabditis elegans. Molecular Biology of the Cell 3, 221–233.CrossRefGoogle Scholar
SULSTON, J. E., SCHIERENBERG, E., WHITE, J. G. & THOMSON, J. N. ( 1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.CrossRefGoogle Scholar
THOMPSON, F. J., COCKROFT, A. C., WHEATLEY, I., BRITTON, C. & DEVANEY, E. ( 2001). Heat shock and developmental expression of hsp83 in the filarial nematode Brugia pahangi. European Journal of Biochemistry 268, 5808–5815.CrossRefGoogle Scholar
VORONOV, D. A. & PANCHIN, Y. V. ( 1998). Cell lineage in marine nematode Enoplus brevis. Development 125, 143–150.Google Scholar
WANG, X. & CHAMBERLIN, H. M. ( 2002). Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes and Development 16, 2345–2349.CrossRefGoogle Scholar
WATERSTON, R. H., LINDBLAD-TOH, K., BIRNEY, E., ROGERS, J., ABRIL, J. F., AGARWAL, P., AGARWALA, R., AINSCOUGH, R., ALEXANDERSSON, M., AN, P., ANTONARAKIS, S. E., ATTWOOD, J., BAERTSCH, R., BAILEY, J., BARLOW, K., BECK, S., BERRY, E., BIRREN, B., BLOOM, T., BORK, P., BOTCHERBY, M., BRAY, N., BRENT, M. R., BROWN, D. G., BROWN, S. D., BULT, C., BURTON, J., BUTLER, J., CAMPBELL, R. D., CARNINCI, P., CAWLEY, S., CHIAROMONTE, F., CHINWALLA, A. T., CHURCH, D. M., CLAMP, M., CLEE, C., COLLINS, F. S., COOK, L. L., COPLEY, R. R., COULSON, A., COURONNE, O., CUFF, J., CURWEN, V., CUTTS, T., DALY, M., DAVID, R., DAVIES, J., DELEHAUNTY, K. D., DERI, J., DERMITZAKIS, E. T., DEWEY, C., DICKENS, N. J., DIEKHANS, M., DODGE, S., DUBCHAK, I., DUNN, D. M., EDDY, S. R., ELNITSKI, L., EMES, R. D., ESWARA, P., EYRAS, E., FELSENFELD, A., FEWELL, G. A., FLICEK, P., FOLEY, K., FRANKEL, W. N., FULTON, L. A., FULTON, R. S., FUREY, T. S., GAGE, D., GIBBS, R. A., GLUSMAN, G., GNERRE, S., GOLDMAN, N., GOODSTADT, L., GRAFHAM, D., GRAVES, T. A., GREEN, E. D., GREGORY, S., GUIGO, R., GUYER, M., HARDISON, R. C., HAUSSLER, D., HAYASHIZAKI, Y., HILLIER, L. W., HINRICHS, A., HLAVINA, W., HOLZER, T., HSU, F., HUA, A., HUBBARD, T., HUNT, A., JACKSON, I., JAFFE, D. B., JOHNSON, L. S., JONES, M., JONES, T. A., JOY, A., KAMAL, M., KARLSSON, E. K., KAROLCHIK, D., KASPRZYK, A., KAWAI, J., KEIBLER, E., KELLS, C., KENT, W. J., KIRBY, A., KOLBE, D. L., KORF, I., KUCHERLAPATI, R. S., KULBOKAS, E. J., KULP, D., LANDERS, T., LEGER, J. P., LEONARD, S., LETUNIC, I., LEVINE, R., LI, J., LI, M., LLOYD, C., LUCAS, S., MA, B., MAGLOTT, D. R., MARDIS, E. R., MATTHEWS, L., MAUCELI, E., MAYER, J. H., McCARTHY, M., McCOMBIE, W. R., McLAREN, S., McLAY, K., McPHERSON, J. D., MELDRIM, J., MEREDITH, B., MESIROV, J. P., MILLER, W., MINER, T. L., MONGIN, E., MONTGOMERY, K. T., MORGAN, M., MOTT, R., MULLIKIN, J. C., MUZNY, D. M., NASH, W. E., NELSON, J. O., NHAN, M. N., NICOL, R., NING, Z., NUSBAUM, C., O'CONNOR, M. J., OKAZAKI, Y., OLIVER, K., OVERTON-LARTY, E., PACHTER, L., PARRA, G., PEPIN, K. H., PETERSON, J., PEVZNER, P., PLUMB, R., POHL, C. S., POLIAKOV, A., PONCE, T. C., PONTING, C. P., POTTER, S., QUAIL, M., REYMOND, A., ROE, B. A., ROSKIN, K. M., RUBIN, E. M., RUST, A. G., SANTOS, R., SAPOJNIKOV, V., SCHULTZ, B., SCHULTZ, J., SCHWARTZ, M. S., SCHWARTZ, S., SCOTT, C., SEAMAN, S., SEARLE, S., SHARPE, T., SHERIDAN, A., SHOWNKEEN, R., SIMS, S., SINGER, J. B., SLATER, G., SMIT, A., SMITH, D. R., SPENCER, B., STABENAU, A., STANGE-THOMANN, N., SUGNET, C., SUYAMA, M., TESLER, G., THOMPSON, J., TORRENTS, D., TREVASKIS, E., TROMP, J., UCLA, C., URETA-VIDAL, A., VINSON, J. P., VON NIEDERHAUSERN, A. C., WADE, C. M., WALL, M., WEBER, R. J., WEISS, R. B., WENDL, M. C., WEST, A. P., WETTERSTRAND, K., WHEELER, R., WHELAN, S., WIERZBOWSKI, J., WILLEY, D., WILLIAMS, S., WILSON, R. K., WINTER, E., WORLEY, K. C., WYMAN, D., YANG, S., YANG, S. P., ZDOBNOV, E. M., ZODY, M. C. & LANDER, E. S. ( 2002). Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562.Google Scholar
WIEGNER, O. & SCHIERENBERG, E. ( 1998). Specification of gut cell fate differs significantly between the nematodes Acrobeloides nanus and Caenorhabditis elegans. Developmental Biology 204, 3–14.CrossRefGoogle Scholar
WIEGNER, O. & SCHIERENBERG, E. ( 1999). Regulative development in a nematode embryo: a hierarchy of cell fate transformations. Developmental Biology 215, 1–12.CrossRefGoogle Scholar
WIENBERG, J. & STANYON, R. ( 1997). Comparative painting of mammalian chromosomes. Current Opinion in Genetics and Development 7, 784–791.CrossRefGoogle Scholar
WILDENBURG, G., LIEBAU, E. & HENKLE-DUHRSEN, K. ( 1998). Onchocerca volvulus: ultrastructural localization of two glutathione S-transferases. Experimental Parasitology 88, 34–42.CrossRefGoogle Scholar
WINTER, A. D., MYLLYHARJU, J. & PAGE, A. P. ( 2003). A hypodermally expressed prolyl 4-hydroxylase from the filarial nematode Brugia malayi is soluble and active in the absence of protein disulfide isomerase. Journal of Biological Chemistry 278, 2554–2562.CrossRefGoogle Scholar
YATSUDA, A. P., KRIJGSVELD, J., CORNELISSEN, A. W., HECK, A. J. & DE VRIES, E. ( 2003). Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. Journal of Biological Chemistry 278, 16941–16951.CrossRefGoogle Scholar
ZHU, J., FUKUSHIGE, T., McGHEE, J. D. & ROTHMAN, J. H. ( 1998). Reprogramming of early embryonic blastomeres into endodermal progenitors by a Caenorhabditis elegans GATA factor. Genes and Development 12, 3809–3814.CrossRefGoogle Scholar