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Extending from PARs in Caenorhabditis elegans to homologues in Haemonchus contortus and other parasitic nematodes

Published online by Cambridge University Press:  16 November 2006

S. NIKOLAOU  and
R. B. GASSER
S. NIKOLAOU
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia Primary Industries Research Victoria (Animal Genetics and Genomics), 475 Mickleham Road, Attwood, Victoria 3049, Australia
R. B. GASSER
Affiliation:
Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Victoria 3030, Australia
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Abstract

Signal transduction molecules play key roles in the regulation of developmental processes, such as morphogenesis, organogenesis and cell differentiation in all organisms. They are organized into ‘pathways’ that represent a coordinated network of cell-surface receptors and intracellular molecules, being involved in sensing environmental stimuli and transducing signals to regulate or modulate cellular processes, such as gene expression and cytoskeletal dynamics. A particularly important group of molecules implicated in the regulation of the cytoskeleton for the establishment and maintenance of cell polarity is the PAR proteins (derived from partition defective in asymmetric cell division). The present article reviews salient aspects of PAR proteins involved in the early embryonic development and morphogenesis of the free-living nematode Caenorhabditis elegans and some other organisms, with an emphasis on the molecule PAR-1. Recent advances in the knowledge and understanding of PAR-1 homologues from the economically important parasitic nematode, Haemonchus contortus, of small ruminants is summarized and discussed in the context of exploring avenues for future research in this area for parasitic nematodes.

Keywords

developmentsignal transductionPAR proteinsPAR-1nematodesCaenorhabditis elegansHaemonchus contortus (Strongylida)
Type
Review Article
Information
Parasitology , Volume 134 , Issue 4 , April 2007 , pp. 461 - 482
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Aboobaker, A. A. and Blaxter, M. L. ( 2000). Medical significance of Caenorhabditis elegans. Annals of Medicine 32, 23–30.CrossRefGoogle Scholar
Aboobaker, A. A. and Blaxter, M. L. ( 2004). Functional genomics for parasitic nematodes and platyhelminths. Trends in Parasitology 20, 178–184.CrossRefGoogle Scholar
Ahringer, J. ( 2003). Control of cell polarity and mitotic spindle positioning in animal cells. Current Opinion in Cell Biology 15, 73–81.CrossRefGoogle Scholar
Baas, A. F., Smit, L. and Clevers, H. ( 2004). LKB1 tumor suppressor protein: PARtaker in cell polarity. Trends in Cell Biology 14, 312–319.CrossRefGoogle Scholar
Bachmann, M., Hennemann, H., Xing, P. X., Hoffmann, I. and Moroy, T. ( 2004). The oncogenic serine/threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint. Journal of Biological Chemistry 279, 48319–48328.CrossRefGoogle Scholar
Bayraktar, J., Zygmunt, D. and Carthew, R. W. ( 2006). Par-1 kinase establishes cell polarity and functions in Notch signaling in the Drosophila embryo. Journal of Cell Science 119, 711–721.CrossRefGoogle Scholar
Beghini, A., Magnani, I., Roversi, G., Piepoli, T., Di Terlizzi, S., Moroni, R. F., Pollo, B., Fuhrman Conti, A. M., Cowell, J. K., Finocchiaro, G. and Larizza, L. ( 2003). The neural progenitor-restricted isoform of the MARK4 gene in 19q13.2 is upregulated in human gliomas and overexpressed in a subset of glioblastoma cell lines. Oncogene 22, 2581–2591.Google Scholar
Benton, R., Palacios, I. M. and St Johnston, D. ( 2002). Drosophila 14-3-3/PAR-5 is an essential mediator of PAR-1 function in axis formation. Developmental Cell 3, 659–671.CrossRefGoogle Scholar
Benton, R. and St Johnston, D. ( 2002). Cell polarity: posterior Par-1 prevents proteolysis. Current Biology 12, R479–R481.CrossRefGoogle Scholar
Benton, R. and St Johnston, D. ( 2003). Drosophila PAR-1 and 14-3-3 inhibit Bazooka/PAR-3 to establish complementary cortical domains in polarized cells. Cell 115, 691–704.CrossRefGoogle Scholar
Berkowitz, L. A. and Strome, S. ( 2000). MES-1, a protein required for unequal divisions of the germline in early C. elegans embryos, resembles receptor tyrosine kinases and is localized to the boundary between the germline and gut cells. Development 127, 4419–4431.Google Scholar
Bertolaet, B. L., Clarke, D. J., Wolff, M., Watson, M. H., Henze, M., Divita, G. and Reed, S. I. ( 2001 a). UBA domains mediate protein–protein interactions between two DNA damage-inducible proteins. Journal of Molecular Biology 313, 955–963.Google Scholar
Bertolaet, B. L., Clarke, D. J., Wolff, M., Watson, M. H., Henze, M., Divita, G. and Reed, S. I. ( 2001 b). UBA domains of DNA damage-inducible proteins interact with ubiquitin. Nature Structural Biology 8, 417–422.Google Scholar
Bessone, S., Vidal, F., Le Bouc, Y., Epelbaum, J., Bluet-Pajot, M. T. and Darmon, M. ( 1999). EMK protein kinase-null mice: dwarfism and hypofertility associated with alterations in the somatotrope and prolactin pathways. Developmental Biology 214, 87–101.CrossRefGoogle Scholar
Bettencourt-Dias, M., Giet, R., Sinka, R., Mazumdar, A., Lock, W. G., Balloux, F., Zafiropoulos, P. J., Yamaguchi, S., Winter, S., Carthew, R. W., Cooper, M., Jones, D., Frenz, L. and Glover, D. M. ( 2004). Genome-wide survey of protein kinases required for cell cycle progression. Nature 432, 980–987.CrossRefGoogle Scholar
Biernat, J., Wu, Y. Z., Timm, T., Zheng-Fischhofer, Q., Mandelkow, E., Meijer, L. and Mandelkow, E. M. ( 2002). Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity. Molecular Biology of the Cell 13, 4013–4028.CrossRefGoogle Scholar
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. and Thomas, W. K. ( 1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71–75.CrossRefGoogle Scholar
Blumenthal, T. and Steward, K. ( 1997). RNA processing and gene structure. In C. elegans II, (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R.), pp. 117–145. Cold Spring Harbour Laboratory Press, New York.
Böhm, H., Brinkmann, V., Drab, M., Henske, A. and Kurzchalia, T. V. ( 1997). Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Current Biology 7, 603–606.Google Scholar
Bowerman, B. ( 1998). Maternal control of pattern formation in early Caenorhabditis elegans embryos. Current Topics in Developmental Biology 39, 73–117.CrossRefGoogle Scholar
Bowerman, B. ( 2000). Embryonic polarity: protein stability in asymmetric cell division. Current Biology 10, R637–R641.CrossRefGoogle Scholar
Bowerman, B., Draper, B. W., Mello, C. C. and Priess, J. R. ( 1993). The maternal skn-1 encodes a protein that is distributed unequally in early C. elegans. Cell 74, 443–452.CrossRefGoogle Scholar
Bowerman, B., Eaton, B. A. and Priess, J. R. ( 1992). skn-1, a maternally expressed gene required to specify the fate of ventral blastomeres in the early C. elegans embryo. Cell 68, 1061–1075.CrossRefGoogle Scholar
Bowerman, B., Ingram, M. K. and Hunter, C. P. ( 1997). The maternal par genes and the segregation of cell fate specification activities in early Caenorhabditis elegans embryos. Development 124, 3815–3826.Google Scholar
Boyd, L., Guo, S., Levitan, D., Stinchcomb, D. T. and Kemphues, K. J. ( 1996). PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122, 3075–3084.Google Scholar
Brajenovic, M., Joberty, G., Kuster, B., Bouwmeester, T. and Drewes, G. ( 2004). Comprehensive proteomic analysis of human Par protein complexes reveals an interconnected protein network. Journal of Biological Chemsitry 279, 12804–12811.CrossRefGoogle Scholar
Brooks, D. R. and Isaac, R. E. ( 2002). Functional genomics of parasitic worms: The dawn of a new era. Parasitology International 51, 319–325.CrossRefGoogle Scholar
Buchberger, A. ( 2002). From UBA to UBX: new words in the ubiquitin vocabulary. Trends in Cell Biology 12, 216–221.CrossRefGoogle Scholar
Bürglin, T. R., Lobos, E. and Blaxter, M. L. ( 1998). Caenorhabditis elegans as a model for parasitic nematodes. International Journal for Parasitology 28, 395–411.CrossRefGoogle Scholar
Chang, S., Bezprozvannaya, S., Li, S. and Olson, E. N. ( 2005). An expression screen reveals modulators of class II histone deacetylase phosphorylation. Proceedings of the National Academy of Sciences, USA 102, 8120–8125.CrossRefGoogle Scholar
Cheeks, R. J., Canman, J. C., Gabriel, W. N., Meyer, N., Strome, S. and Goldstein, B. ( 2004). C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Current Biology 14, 851–862.Google Scholar
Chen, L., Shinde, U., Ortolan, T. G. and Madura, K. ( 2001). Ubiquitin-associated (UBA) domains in Rad23 bind ubiquitin and promote inhibition of multi-ubiquitin chain assembly. EMBO Reports 2, 933–938.CrossRefGoogle Scholar
Cheng, N. N., Kirby, C. M. and Kemphues, K. J. ( 1995). Control of cleavage spindle orientation in Caenorhabditis elegans: the role of the genes par-2 and par-3. Genetics 139, 549–559.Google Scholar
Cohen, D., Brennwald, P. J., Rodriguez-Boulan, E. and Musch, A. ( 2004 a). Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton. Journal of Cell Biology 164, 717–727.Google Scholar
Cohen, D. and Musch, A. ( 2003). Apical surface formation in MDCK cells: regulation by the serine/threonine kinase EMK1. Methods 30, 269–276.CrossRefGoogle Scholar
Cohen, D., Rodriguez-Boulan, E. and Musch, A. ( 2004 b). Par-1 promotes a hepatic mode of apical protein trafficking in MDCK cells. Proceedings of the National Academy of Sciences, USA 101, 13792–13797.Google Scholar
Couthier, A., Smith, J., McGarr, P., Craig, B. and 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
Crittenden, S. L., Rudel, D., Binder, J., Evans, T. C. and Kimble, J. ( 1997). Genes required for GLP-1 asymmetry in the early Caenorhabditis elegans embryo. Developmental Biology 181, 36–46.CrossRefGoogle Scholar
Crump, J. G., Zhen, M., Jin, Y. and Bargmann, C. I. ( 2001). The SAD-1 kinase regulates presynaptic vesicle clustering and axon termination. Neuron 29, 115–129.CrossRefGoogle Scholar
Cuenca, A. A., Schetter, A., Aceto, D., Kemphues, K. and Seydoux, G. ( 2003). Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130, 1255–1265.Google Scholar
Cunha, A., Azevedo, R. B., Emmons, S. W. and Leroi, A. M. ( 1999). Variable cell number in nematodes. Nature 402, 253.Google Scholar
Derenzo, C., Reese, K. J. and Seydoux, G. ( 2003). Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424, 685–689.CrossRefGoogle Scholar
Derenzo, C. and Seydoux, G. ( 2004). A clean start: degradation of maternal proteins at the oocyte-to-embryo transition. Trends in Cell Biology 14, 420–426.CrossRefGoogle Scholar
Di Fiore, P. P., Polo, S. and Hofmann, K. ( 2003). When ubiquitin meets ubiquitin receptors: a signalling connection. Nature Reviews Molecular Cell Biology 4, 491–497.CrossRefGoogle Scholar
Doe, C. Q. and Bowerman, B. ( 2001). Asymmetric cell division: fly neuroblast meets worm zygote. Current Opinion in Cell Biology 13, 68–75.CrossRefGoogle Scholar
Doerflinger, H., Benton, R., Shulman, J. M. and St Johnston, D. ( 2003). The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium. Development 130, 3965–3975.CrossRefGoogle Scholar
Doerflinger, H., Benton, R., Torres, I. L., Zwart, M. F. and St Johnston, D. ( 2006). Drosophila anterior-posterior polarity requires actin-dependent PAR-1 recruitment to the oocyte posterior. Current Biology 16, 1090–1095.CrossRefGoogle Scholar
Drewes, G. ( 2004). MARKing tau for tangles and toxicity. Trends in Biochemical Sciences 29, 548–555.CrossRefGoogle Scholar
Drewes, G., Ebneth, A. and Mandelkow, E. M. ( 1998). MAPs, MARKs and microtubule dynamics. Trends in Biochemical Sciences 23, 307–311.CrossRefGoogle Scholar
Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E. M. and Mandelkow, E. ( 1997). MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297–308.CrossRefGoogle Scholar
Elbert, M., Rossi, G. and Brennwald, P. ( 2005). The yeast Par-1 homologs, Kin1 and Kin2, show genetic and physical interactions with components of the exocytic machinery. Molecular Biology of the Cell 16, 532–549.CrossRefGoogle Scholar
Espinosa, L. and Navarro, E. ( 1998). Human serine/threonine protein kinase EMK1: genomic structure and cDNA cloning of isoforms produced by alternative splicing. Cytogenetics and Cell Genetics 81, 278–282.CrossRefGoogle Scholar
Etemad-Moghadam, B., Guo, S. and Kemphues, K. J. ( 1995). Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83, 743–752.CrossRefGoogle Scholar
Felix, M. A. and Sternberg, P. W. ( 1996). Symmetry breakage in the development of one-armed gonads in nematodes. Development 122, 2129–2142.Google Scholar
Fitch, D. H. A. and Thomas, W. K. ( 1997). Evolution. In C. elegans II, ( ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R.), pp. 815–850. Cold Spring Harbour Laboratory Press, New York.
Freeman, M. ( 2000). Feedback control of intercellular signalling in development. Nature 408, 313–319.CrossRefGoogle Scholar
Gasser, R. B. and Newton, S. E. ( 2000). Genomic and genetic research on bursate nematodes: significance, implications and prospects. International Journal for Parasitology 30, 509–534.CrossRefGoogle Scholar
Geary, T. G. and Thompson, D. P. ( 2001). Caenorhabditis elegans: how good a model for veterinary parasites? Veterinary Parasitology 101, 371–386.Google Scholar
Geldhof, P., Murray, L., Couthier, A., Gilleard, J. S., McLauchlan, G., Knox, D. P. and Britton, C. ( 2006). Testing the efficacy of RNA interference in Haemonchus contortus. International Journal for Parasitology 36, 801–810.CrossRefGoogle Scholar
Georgi, J. R. and Georgi, M. E. ( 1990). Parasitology for Veterinarians (5th Edn.), W.B. Saunders Company, Philadelphia.
Gerhart, J. ( 1999). 1998 Warkany lecture: signaling pathways in development. Teratology 60, 226–239.3.0.CO;2-W>CrossRefGoogle Scholar
Gilleard, J. S. ( 2004). The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128, S49–S70.CrossRefGoogle Scholar
Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A., Kuang, B., Li, Y., Hao, Y. L., Ooi, C. E., Godwin, B., Vitols, E., Vijayadamodar, G., Pochart, P., Machineni, H., Welsh, M., Kong, Y., Zerhusen, B., Malcolm, R., Varrone, Z., Collis, A., Minto, M., Burgess, S., McDaniel, L., Stimpson, E., Spriggs, F., Williams, J., Neurath, K., Ioime, N., Agee, M., Voss, E., Furtak, K., Renzulli, R., Aanensen, N., Carrolla, S., Bickelhaupt, E., Lazovatsky, Y., Dasilva, A., Zhong, J., Stanyon, C. A., Finley, R. L. Jr., White, K. P., Braverman, M., Jarvie, T., Gold, S., Leach, M., Knight, J., Shimkets, R. A., McKenna, M. P., Chant, J. and Rothberg, J. M. ( 2003). A protein interaction map of Drosophila melanogaster. Science 302, 1727–1736.CrossRefGoogle Scholar
Golden, A. ( 2000). Cytoplasmic flow and the establishment of polarity in C. elegans 1-cell embryos. Current Opinion in Genetics and Development 10, 414–420.CrossRefGoogle Scholar
Goldstein, B. ( 1992). Induction of gut in Caenorhabditis elegans embryos. Nature 357, 255–257.CrossRefGoogle Scholar
Goldstein, B. ( 1993). Establishment of gut fate in the E lineage of C. elegans: the roles of lineage-dependent mechanisms and cell interactions. Development 118, 1267–1277.Google Scholar
Goldstein, B. ( 2001). On the evolution of early development in the Nematoda. Philosophical Transactions of the Royal Society of London, Series B. 356, 1521–1531.CrossRefGoogle Scholar
Goldstein, B., Frisse, L. M. and Thomas, W. K. ( 1998). Embryonic axis specification in nematodes: evolution of the first step in development. Current Biology 8, 157–160.CrossRefGoogle Scholar
Goldstein, B. and Hird, S. N. ( 1996). Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122, 1467–1474.Google Scholar
Gonczy, P. and Hyman, A. A. ( 1996). Cortical domains and the mechanisms of asymmetric cell division. Trends in Cell Biology 6, 382–387.CrossRefGoogle Scholar
Gotta, M. ( 2005). At the heart of cell polarity and the cytoskeleton. Developmental Cell 8, 629–633.CrossRefGoogle Scholar
Guo, S. and Kemphues, K. J. ( 1995). par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611–620.Google Scholar
Guo, S. and Kemphues, K. J. ( 1996). A non-muscle myosin required for embryonic polarity in Caenorhabditis elegans. Nature 382, 455–458.CrossRefGoogle Scholar
Haglund, K., Di Fiore, P. P. and Dikic, I. ( 2003). Distinct monoubiquitin signals in receptor endocytosis. Trends in Biochemical Sciences 28, 598–603.CrossRefGoogle Scholar
Hanna-Rose, W. and Han, M. ( 2000). Getting signals crossed in C. elegans. Current Opinion in Genetics and Development 10, 523–528.CrossRefGoogle Scholar
Hanks, S. K., Quinn, A. M. and Hunter, T. ( 1988). The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241, 42–52.CrossRefGoogle Scholar
Hanks, S. K. and Hunter, T. ( 1995). Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB Journal 9, 576–596.Google Scholar
Hao, Y., Boyd, L. and Seydoux, G. ( 2006). Stabilization of cell polarity by the C. elegans RING protein PAR-2. Developmental Cell 10, 199–208.CrossRefGoogle Scholar
Hashmi, S., Tawe, W. and Lustigman, S. ( 2001). Caenorhabditis elegans and the study of gene function in parasites. Trends in Parasitology 17, 387–393.CrossRefGoogle Scholar
Hofmann, K. and Bucher, P. ( 1996). The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway. Trends in Biochemical Sciences 21, 172–173.CrossRefGoogle Scholar
Hope, I. A. ( 1999). Background on Caenorhabditis elegans. In Caenorhabditis elegans: a Practical Approach, (ed. Hope, I. A.), pp. 1–15. Oxford University Press, New York.
Hueso, M., Beltran, V., Moreso, F., Ciriero, E., Fulladosa, X., Grinyo, J. M., Seron, D. and Navarro, E. ( 2004). Splicing alterations in human renal allografts: detection of a new splice variant of protein kinase Par1/Emk1 whose expression is associated with an increase of inflammation in protocol biopsies of transplanted patients. Biochimica et Biophysica Acta 1689, 58–65.CrossRefGoogle Scholar
Hung, T. J. and Kemphues, K. J. ( 1999). PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126, 127–135.Google Scholar
Hurd, D. D. and Kemphues, K. J. ( 2003). PAR-1 is required for morphogenesis of the Caenorhabditis elegans vulva. Developmental Biology 253, 54–65.CrossRefGoogle Scholar
Hurov, J. B., Stappenbeck, T. S., Zmasek, C. M., White, L. S., Ranganath, S. H., Russell, J. H., Chan, A. C., Murphy, K. M. and Piwnica-Worms, H. ( 2001). Immune system dysfunction and autoimmune disease in mice lacking Emk (Par-1) protein kinase. Molecular and Cellular Biology 21, 3206–3219.CrossRefGoogle Scholar
Hurov, J. B., Watkins, J. L. and Piwnica-Worms, H. ( 2004). Atypical PKC phosphorylates PAR-1 kinases to regulate localization and activity. Current Biology 14, 736–741.CrossRefGoogle Scholar
Hutchison, M., Berman, K. S. and Cobb, M. H. ( 1998). Isolation of TAO1, a protein kinase that activates MEKs in stress-activated protein kinase cascades. Journal of Biological Chemistry 273, 28625–28632.CrossRefGoogle Scholar
Hutter, H. and Schnabel, R. ( 1994). glp-1 and inductions establishing embryonic axes in C. elegans. Development 120, 2051–2064.Google Scholar
Hutter, H. and Schnabel, R. ( 1995 a). Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development 121, 3417–3424.Google Scholar
Hutter, H. and Schnabel, R. ( 1995 b). Specification of anterior-posterior differences within the AB lineage in the C. elegans embryo: a polarising induction. Development 121, 1559–1568.Google Scholar
Illenberger, S., Drewes, G., Trinczek, B., Biernat, J., Meyer, H. E., Olmsted, J. B., Mandelkow, E. M. and Mandelkow, E. ( 1996). Phosphorylation of microtubule-associated proteins MAP2 and MAP4 by the protein kinase p110mark. Phosphorylation sites and regulation of microtubule dynamics. Journal of Biological Chemistry 271, 10834–10843.Google Scholar
Inglis, J. D., Lee, M. and Hill, R. E. ( 1993). Emk, a protein kinase with homologs in yeast maps to mouse chromosome 19. Mammalian Genome 4, 401–403.CrossRefGoogle Scholar
Issa, Z., Grant, W. N., Stasiuk, S. and Shoemaker, C. B. ( 2005). Development of methods for RNA interference in the sheep gastrointestinal parasite, Trichostrongylus colubriformis. International Journal for Parasitology 35, 935–940.CrossRefGoogle Scholar
Jaleel, M., Villa, F., Deak, M., Toth, R., Prescott, A. R., Van Aalten, D. M. and Alessi, D. R. ( 2006). The ubiquitin-associated domain of AMPK-related kinases regulates conformation and LKB1-mediated phosphorylation and activation. Biochemistry Journal 394, 545–555.CrossRefGoogle Scholar
Jeon, S., Kim, Y. S., Park, J. and Bae, C. D. ( 2005). Microtubule affinity-regulating kinase 1 (MARK1) is activated by electroconvulsive shock in the rat hippocampus. Journal of Neurochemistry 95, 1608–1618.CrossRefGoogle Scholar
Jiang, M., Ryu, J., Kiraly, M., Duke, K., Reinke, V. and Kim, S. ( 2001). Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 98, 218–223.CrossRefGoogle Scholar
Kao, G., Tuck, S., Baillie, D. and Sundaram, M. V. ( 2004). C. elegans SUR-6/PR55 cooperates with LET-92/protein phosphatase 2A and promotes Raf activity independently of inhibitory Akt phosphorylation sites. Development 131, 755–765.Google Scholar
Kato, T., Satoh, S., Okabe, H., Kitahara, O., Ono, K., Kihara, C., Tanaka, T., Tsunoda, T., Yamaoka, Y., Nakamura, Y. and Furukawa, Y. ( 2001). Isolation of a novel human gene, MARKL1, homologous to MARK3 and its involvement in hepatocellular carcinogenesis. Neoplasia 3, 4–9.CrossRefGoogle Scholar
Kemphues, K. ( 2000). PARsing embryonic polarity. Cell 101, 345–348.CrossRefGoogle Scholar
Kemphues, K. J., Priess, J. R., Morton, D. G. and Cheng, N. S. ( 1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52, 311–320.CrossRefGoogle Scholar
Kirby, C., Kusch, M. and Kemphues, K. ( 1990). Mutations in the par genes of Caenorhabditis elegans affect cytoplasmic reorganization during the first cell cycle. Developmental Biology 142, 203–215.CrossRefGoogle Scholar
Kosuga, S., Tashiro, E., Kajioka, T., Ueki, M., Shimizu, Y. and Imoto, M. ( 2005). GSK-3β directly phosphorylates and activates MARK2/PAR-1. Journal of Biological Chemistry 280, 42715–42722.CrossRefGoogle Scholar
Kotze, A. C. and Bagnall, N. H. ( 2006). RNA interference in Haemonchus contortus: Suppression of beta-tubulin gene expression in L3, L4 and adult worms in vitro. Molecular and Biochemical Parasitology 145, 101–110.CrossRefGoogle Scholar
Kusakabe, M. and Nishida, E. ( 2004). The polarity-inducing kinase Par-1 controls Xenopus gastrulation in cooperation with 14-3-3 and aPKC. EMBO Journal 23, 4190–4201.CrossRefGoogle Scholar
Kuwabara, P. E. and Coulson, A. ( 2000). RNAi-prospects for a general technique for determining gene function. Parasitology Today 16, 347–349.CrossRefGoogle Scholar
Leung, B., Hermann, G. J. and Priess, J. R. ( 1999). Organogenesis of the Caenorhabditis elegans intestine. Developmental Biology 216, 114–134.CrossRefGoogle Scholar
Levin, D. E. and Bishop, J. M. ( 1990). A putative protein kinase gene (kin1+) is important for growth polarity in Schizosaccharomyces pombe. Proceedings of the National Academy of Sciences, USA 87, 8272–8276.CrossRefGoogle Scholar
Levin, D. E., Hammond, C. I., Ralston, R. O. and Bishop, J. M. ( 1987). Two yeast genes that encode unusual protein kinases. Proceedings of the National Academy of Sciences, USA 84, 6035–6039.CrossRefGoogle Scholar
Levitan, D. J., Boyd, L., Mello, C. C., Kemphues, K. J. and Stinchcomb, D. T. ( 1994). par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proceedings of the National Academy of Sciences, USA 91, 6108–6112.CrossRefGoogle Scholar
Li, S., Armstrong, C. M., Bertin, N., Ge, H., Milstein, S., Boxem, M., Vidalain, P. O., Han, J. D., Chesneau, A., Hao, T., Goldberg, D. S., Li, N., Martinez, M., Rual, J. F., Lamesch, P., Xu, L., Tewari, M., Wong, S. L., Zhang, L. V., Berriz, G. F., Jacotot, L., Vaglio, P., Reboul, J., Hirozane-Kishikawa, T., Li, Q., Gabel, H. W., Elewa, A., Baumgartner, B., Rose, D. J., Yu, H., Bosak, S., Sequerra, R., Fraser, A., Mango, S. E., Saxton, W. M., Strome, S., Van Den Heuvel, S., Piano, F., Vandenhaute, J., Sardet, C., Gerstein, M., Doucette-Stamm, L., Gunsalus, K. C., Harper, J. W., Cusick, M. E., Roth, F. P., Hill, D. E. and Vidal, M. ( 2004). A map of the interactome network of the metazoan C. elegans. Science 303, 540–543.Google Scholar
Li, J., Ashton, F. T., Gamble, H. R. and Schad, G. A. ( 2000). Sensory neuroanatomy of a passively ingested nematode parasite, Haemonchus contortus: amphidial neurons of the first stage larva. Journal of Comparative Neurology 417, 299–314.3.0.CO;2-O>CrossRefGoogle Scholar
Li, J., Zhu, X., Ashton, F. T., Gamble, H. R. and Schad, G. A. ( 2001). Sensory neuroanatomy of a passively ingested nematode parasite, Haemonchus contortus: amphidial neurons of the third-stage larva. Journal of Parasitology 87, 65–72.CrossRefGoogle Scholar
Lizcano, J. M., Goransson, O., Toth, R., Deak, M., Morrice, N. A., Boudeau, J., Hawley, S. A., Udd, L., Makela, T. P., Hardie, D. G. and Alessi, D. R. ( 2004). LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO Journal 23, 833–843.CrossRefGoogle Scholar
Lo, M. C., Gay, F., Odom, R., Shi, Y. and Lin, R. ( 2004). Phosphorylation by the beta-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans. Cell 117, 95–106.CrossRefGoogle Scholar
Macara, I. G. ( 2004). Par proteins: partners in polarization. Current Biology 14, R160–R162.CrossRefGoogle Scholar
Maduro, M. F., Meneghini, M. D., Bowerman, B., Broitman-Maduro, G. and Rothman, J. H. ( 2001). Restriction of mesendoderm to a single blastomere by the combined action of SKN-1 and a GSK-3beta homolog is mediated by MED-1 and -2 in C. elegans. Molecular Cell 7, 475–485.Google Scholar
Mandelkow, E. M., Thies, E., Trinczek, B., Biernat, J. and Mandelkow, E. ( 2004). MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J of Cell Biology 167, 99–110.CrossRefGoogle Scholar
Mango, S. E., Thorpe, C. J., Martin, P. R., Chamberlain, S. H. and Bowerman, B. ( 1994). Two maternal genes, apx-1 and pie-1, are required to distinguish the fates of equivalent blastomeres in the early Caenorhabditis elegans embryo. Development 120, 2305–2315.Google Scholar
Martin, S. G. and St Johnston, D. ( 2003). A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421, 379–384.CrossRefGoogle Scholar
Matenia, D., Griesshaber, B., Li, X. Y., Thiessen, A., Johne, C., Jiao, J., Mandelkow, E. and Mandelkow, E. M. ( 2005). PAK5 kinase is an inhibitor of MARK/Par-1, which leads to stable microtubules and dynamic actin. Molecular Biology of the Cell 16, 4410–4422.CrossRefGoogle Scholar
Mello, C. C., Draper, B. W. and 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
Meneghini, M. D., Ishitani, T., Carter, J. C., Hisamoto, N., Ninomiya-Tsuji, J., Thorpe, C. J., Hamill, D. R., Matsumoto, K. and Bowerman, B. ( 1999). MAP kinase and Wnt pathways converge to downregulate an HMG-domain repressor in Caenorhabditis elegans. Nature 399, 793–797.CrossRefGoogle Scholar
Mickey, K. M., Mello, C. C., Montgomery, M. K., Fire, A. and Priess, J. R. ( 1996). An inductive interaction in 4-cell stage C. elegans embryos involves APX-1 expression in the signalling cell. Development 122, 1791–1798.Google Scholar
Moore, C. A. and Zernicka-Goetz, M. ( 2005). PAR-1 and the microtubule-associated proteins CLASP2 and dynactin-p50 have specific localisation on mouse meiotic and first mitotic spindles. Reproduction 130, 311–320.CrossRefGoogle Scholar
Morton, D. G., Shakes, D. C., Nugent, S., Dichoso, D., Wang, W., Golden, A. and Kemphues, K. J. ( 2002). The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Developmental Biology 241, 47–58.CrossRefGoogle Scholar
Muller, J., Ory, S., Copeland, T., Piwnica-Worms, H. and Morrison, D. K. ( 2001). C-TAK1 regulates Ras signaling by phosphorylating the MAPK scaffold, KSR1. Molecular Cell 8, 983–993.CrossRefGoogle Scholar
Muller, J., Ritt, D. A., Copeland, T. D. and Morrison, D. K. ( 2003). Functional analysis of C-TAK1 substrate binding and identification of PKP2 as a new C-TAK1 substrate. EMBO Journal 22, 4431–4442.CrossRefGoogle Scholar
Munro, E. M. ( 2006). PAR proteins and the cytoskeleton: a marriage of equals. Current Opinion in Cell Biology 18, 86–94.CrossRefGoogle Scholar
Munro, E., Nance, J. and Priess, J. R. ( 2004). Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Developmental Cell 7, 413–424.CrossRefGoogle Scholar
Nance, J. ( 2005). PAR proteins and the establishment of cell polarity during C. elegans development. Bioessays 27, 126–135.Google Scholar
Nance, J., Munro, E. M. and Priess, J. R. ( 2003). C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130, 5339–5350.Google Scholar
Newman-Smith, E. D. and Rothman, J. H. ( 1998). The maternal-to-zygotic transition in embryonic patterning of Caenorhabditis elegans. Current Opinion in Genetics and Development 8, 472–480.CrossRefGoogle Scholar
Newton, S. E., Boag, P. R. and Gasser, R. B. ( 2002). Opportunities and prospects for investigating developmentally regulated and sex-specific genes and their expression in intestinal nematodes of humans. In World Class Parasites: Vol. 2. The Geohelminths: Ascaris, Trichuris and Hookworm, (ed. Holland, C. V. and Kennedy, M. W.), pp. 235–268. Kluwer Academic Publishers, Boston/Dordrecht/London.
Nikolaou, S. and Gasser, R. B. ( 2006). Prospects for exploring molecular developmental processes in Haemonchus contortus. International Journal for Parasitology 36, 859–868.CrossRefGoogle Scholar
Nikolaou, S., Hartman, D., Nisbet, A. J., Presidente, P. J. and Gasser, R. B. ( 2004). Genomic organization and expression analysis for hcstk, a serine/threonine protein kinase gene of Haemonchus contortus, and comparison with Caenorhabditis elegans par-1. Gene 343, 313–322.CrossRefGoogle Scholar
Nikolaou, S., Hartman, D., Presidente, P. J. A., Newton, S. E. and Gasser, R. B. ( 2002). HcSTK, a Caenorhabditis elegans PAR-1 homologue from the parasitic nematode, Haemonchus contortus. International Journal for Parasitology 32, 749–758.CrossRefGoogle Scholar
Nikolaou, S., Hartman, D., Nisbet, A. J. and Gasser, R. B. ( 2006 a). Haemonchus contortus: Prokaryotic expression and enzyme activity of recombinant HcSTK, a serine/threonine protein kinase. Experimental Parasitology 113, 207–214.Google Scholar
Nikolaou, S., Hu, M., Chilton, N. B., Hartman, D., Nisbet, A. J., Presidente, P. J. A. and Gasser, R. B. ( 2006 b). Class II myosins in nematodes – genetic relationships, fundamental and applied implications. Biotechnology Advances 24, 338–350.Google Scholar
Nikolaou, S., Hu, M., Chilton, N. B., Hartman, D., Nisbet, A. J., Presidente, P. J. A. and Gasser, R. B. ( 2006 c). Isolation and characterization of class II myosin genes from Haemonchus contortus. Parasitology Research 99, 200–204.Google Scholar
Nisbet, A. J., Cottee, P. and Gasser, R. B. ( 2004). Molecular biology of reproduction and development in parasitic nematodes: progress and opportunities. International Journal for Parasitology 34, 125–138.CrossRefGoogle Scholar
Nishimura, I., Yang, Y. and Lu, B. ( 2004). PAR-1 kinase plays an initiator role in a temporally ordered phosphorylation process that confers tau toxicity in Drosophila. Cell 116, 671–682.CrossRefGoogle Scholar
Ogg, S., Gabrielli, B. and Piwnica-Worms, H. ( 1994). Purification of a serine kinase that associates with and phosphorylates human Cdc25C on serine 216. Journal of Biological Chemistry 269, 30461–30469.Google Scholar
Ono, T., Kawabe, T., Sonta, S. and Okamoto, T. ( 1997). Assignment of MARK3 alias KP78 to human chromosome band 14q32.3 by in situ hybridization. Cytogenetics and Cell Genetics 79, 101–102.CrossRefGoogle Scholar
Ossipova, O., Dhawan, S., Sokol, S. and Green, J. B. ( 2005). Distinct PAR-1 proteins function in different branches of Wnt signaling during vertebrate development. Developmental Cell 8, 829–841.CrossRefGoogle Scholar
Ossipova, O., He, X. and Green, J. ( 2002). Molecular cloning and developmental expression of Par-1/MARK homologues XPar-1A and XPar-1B from Xenopus laevis. Mechanisms of Development 119 (Suppl. 1), S143–S148.CrossRefGoogle Scholar
Panneerselvam, S., Marx, A., Mandelkow, E. M. and Mandelkow, E. ( 2006). Structure of the catalytic and ubiquitin-associated domains of the protein kinase MARK/Par-1. Structure 14, 173–183.CrossRefGoogle Scholar
Parsa, I. ( 1988). Loss of a Mr 78,000 marker in chemically induced transplantable carcinomas and primary carcinoma of human pancreas. Cancer Research 48, 2265–2272.Google Scholar
Patterson, G. I. and Padgett, R. W. ( 2000). TGF beta-related pathways. Roles in Caenorhabditis elegans development. Trends in Genetics 16, 27–33.Google Scholar
Pellettieri, J., Reinke, V., Kim, S. K. and Seydoux, G. ( 2003). Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Developmental Cell 5, 451–462.CrossRefGoogle Scholar
Pellettieri, J. and Seydoux, G. ( 2002). Anterior-Posterior polarity in C. elegans and Drosophila–PARallels and differences. Science 298, 1946–1950.Google Scholar
Peng, C. Y., Graves, P. R., Ogg, S., Thoma, R. S., Byrnes, M. J., 3rd, Wu, Z., Stephenson, M. T. and Piwnica-Worms, H. ( 1998). C-TAK1 protein kinase phosphorylates human Cdc25C on serine 216 and promotes 14-3-3 protein binding. Cell Growth and Differentiation 9, 197–208.Google Scholar
Penton, A., Wodarz, A. and Nusse, R. ( 2002). A mutational analysis of dishevelled in Drosophila defines novel domains in the Dishevelled protein as well as novel suppressing alleles of axin. Genetics 161, 747–762.Google Scholar
Plasterk, R. H. ( 1999). The year of the worm. Bioessays 21, 105–109.3.0.CO;2-W>CrossRefGoogle Scholar
Reese, K. J., Dunn, M. A., Waddle, J. A. and Seydoux, G. ( 2000). Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Molecular Cell 6, 445–455.Google Scholar
Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R. ( 1997). Introduction to C. elegans. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. and Priess, J. R.), pp. 1–22. Cold Spring Harbour Laboratory Press, New York.
Riechmann, V. and Ephrussi, A. ( 2004). Par-1 regulates bicoid mRNA localisation by phosphorylating Exuperantia. Development 131, 5897–5907.CrossRefGoogle Scholar
Riechmann, V., Gutierrez, G. J., Filardo, P., Nebreda, A. R. and Ephrussi, A. ( 2002). Par-1 regulates stability of the posterior determinant Oskar by phosphorylation. Nature Cell Biology 4, 337–342.CrossRefGoogle Scholar
Rocheleau, C. E., Downs, W. D., Lin, R., Wittmann, C., Bei, Y., Cha, Y. H., Ali, M., Priess, J. R. and Mello, C. C. ( 1997). Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90, 707–716.CrossRefGoogle Scholar
Rose, L. S. and Kemphues, K. J. ( 1998). Early patterning of the C. elegans embryo. Annual Review of Genetics 32, 521–545.CrossRefGoogle Scholar
Schaar, B. T., Kinoshita, K. and McConnell, S. K. ( 2004). Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 41, 203–213.CrossRefGoogle Scholar
Schenk, P. W. and Snaar-Jagalska, B. E. ( 1999). Signal perception and transduction: the role of protein kinases. Biochimica et Biophysica Acta 1449, 1–24.CrossRefGoogle Scholar
Schierenberg, E. ( 2001). Three sons of fortune: early embryogenesis, evolution and ecology of nematodes. BioEssays 23, 841–847.CrossRefGoogle Scholar
Schlesinger, A., Shelton, C. A., Maloof, J. N., Meneghini, M. and Bowerman, B. ( 1999). Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell. Genes and Development 13, 2028–2038.CrossRefGoogle Scholar
Schneider, A., Laage, R., Von Ahsen, O., Fischer, A., Rossner, M., Scheek, S., Grunewald, S., Kuner, R., Weber, D., Kruger, C., Klaussner, B., Gotz, B., Hiemisch, H., Newrzella, D., Martin-Villalba, A., Bach, A. and Schwaninger, M. ( 2004). Identification of regulated genes during permanent focal cerebral ischaemia: characterization of the protein kinase 9b5/MARKL1/MARK4. Journal of Neurochemistry 88, 1114–1126.CrossRefGoogle Scholar
Schnell, J. D. and Hicke, L. ( 2003). Non-traditional functions of ubiquitin and ubiquitin-binding proteins. Journal of Biological Chemistry 278, 35857–35860.CrossRefGoogle Scholar
Schubert, C. M., Lin, R., De Vries, C. J., Plasterk, R. H. and Priess, J. R. ( 2000). MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Molecular Cell 5, 671–682.Google Scholar
Shelton, C. A. and Bowerman, B. ( 1996). Time-dependent responses to glp-1-mediated inductions in early C. elegans embryos. Development 122, 2043–2050.Google Scholar
Shulman, J. M., Benton, R. and St Johnston, D. ( 2000). The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377–388.Google Scholar
Sommer, R. J. ( 2000). Evolution of nematode development. Current Opinion in Genetics and Development 10, 443–448.CrossRefGoogle Scholar
Spicer, J., Rayter, S., Young, N., Elliott, R., Ashworth, A. and Smith, D. ( 2003). Regulation of the Wnt signalling component PAR1A by the Peutz-Jeghers syndrome kinase LKB1. Oncogene 22, 4752–4756.CrossRefGoogle Scholar
Sternberg, P. W. ( 1993). Intercellular signalling and signal transduction in C. elegans. Annual Review of Genetics 27, 497–521.CrossRefGoogle Scholar
Sternberg, P. W. and Felix, M. A. ( 1997). Evolution of cell lineage. Current Opinion in Genetics and Development 7, 543–550.CrossRefGoogle Scholar
Sulston, J. ( 1988). Cell lineage. In The Nematode Caenorhabditis elegans, (ed. Wood, W. B.), pp. 123–155. Cold Spring Harbor Laboratory Press, New York.
Sulston, J. E. and Horvitz, H. R. ( 1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology 56, 110–156.CrossRefGoogle Scholar
Sulston, J. E., Schierenberg, E., White, J. G. and Thomson, J. N. ( 1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.CrossRefGoogle Scholar
Sun, T. Q., Lu, B., Feng, J. J., Reinhard, C., Jan, Y. N., Fantl, W. J. and Williams, L. T. ( 2001). PAR-1 is a Dishevelled-associated kinase and a positive regulator of Wnt signalling. Nature Cell Biology 3, 628–636.CrossRefGoogle Scholar
Suzuki, A., Hirata, M., Kamimura, K., Maniwa, R., Yamanaka, T., Mizuno, K., Kishikawa, M., Hirose, H., Amano, Y., Izumi, N., Miwa, Y. and Ohno, S. ( 2004). aPKC acts upstream of PAR-1b in both the establishment and maintenance of mammalian epithelial polarity. Current Biology 14, 1425–1435.CrossRefGoogle Scholar
Suzuki, A. and Ohno, S. ( 2006). The PAR-aPKC system: lessons in polarity. Journal of Cell Science 119, 979–987.CrossRefGoogle Scholar
Taylor, S. S., Radzio-Andzelm, E. and Hunter, T. ( 1995). How do protein kinases discriminate between serine/threonine and tyrosine? Structural insights from the insulin receptor protein-tyrosine kinase. FASEB Journal 9, 1255–1266.CrossRefGoogle Scholar
THE C. ELEGANS SEQUENCING CONSORTIUM ( 1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012–2018.
Thorpe, C. J., Schlesinger, A., Carter, J. C. and Bowerman, B. ( 1997). Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90, 695–705.Google Scholar
Timm, T., Li, X. Y., Biernat, J., Jiao, J., Mandelkow, E., Vandekerckhove, J. and Mandelkow, E. M. ( 2003). MARKK, a Ste20-like kinase, activates the polarity-inducing kinase MARK/PAR-1. EMBO Journal 22, 5090–5101.CrossRefGoogle Scholar
Tomancak, P., Piano, F., Riechmann, V., Gunsalus, K. C., Kemphues, K. J. and Ephrussi, A. ( 2000). A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nature Cell Biology 2, 458–460.CrossRefGoogle Scholar
Trinczek, B., Brajenovic, M., Ebneth, A. and Drewes, G. ( 2004). MARK4 is a novel microtubule-associated proteins/microtubule affinity-regulating kinase that binds to the cellular microtubule network and to centrosomes. Journal of Biological Chemistry 279, 5915–5923.CrossRefGoogle Scholar
Vaccari, T., Rabouille, C. and Ephrussi, A. ( 2005). The Drosophila PAR-1 spacer domain is required for lateral membrane association and for polarization of follicular epithelial cells. Current Biology 15, 255–261.CrossRefGoogle Scholar
Vanfleteren, J. R., Van De Peer, Y., Blaxter, M. L., Tweedie, S. A., Trotman, C., Lu, L., Van Hauwaert, M. L. and Moens, L. ( 1994). Molecular genealogy of some nematode taxa as based on cytochrome c and globin amino acid sequences. Molecular and Phylogenetics and Evolution 3, 92–101.CrossRefGoogle Scholar
Veglia, F. ( 1915). The anatomy and life-history of the Haemonchus contortus (Rudolphi). The Third and Fourth Reports of the Director of Veterinary Research, Department of Agriculture, Union of South Africa, pp. 347–500.
Viney, M. E., Thompson, F. J. and Crook, M. ( 2005). TGF-beta and the evolution of nematode parasitism. International Journal for Parasitology 35, 1473–1475.CrossRefGoogle Scholar
Vinot, S., Le, T., Ohno, S., Pawson, T., Maro, B. and Louvet-Vallee, S. ( 2005). Asymmetric distribution of PAR proteins in the mouse embryo begins at the 8-cell stage during compaction. Developmental Biology 282, 307–319.CrossRefGoogle Scholar
Watts, J. L., Morton, D. G., Bestman, J. and Kemphues, K. J. ( 2000). The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127, 1467–1475.Google Scholar
Wiggin, G. R., Fawcett, J. P. and Pawson, T. ( 2005). Polarity proteins in axon specification and synaptogenesis. Developmental Cell 8, 803–816.CrossRefGoogle Scholar
Wilkinson, C. R., Seeger, M., Hartmann-Petersen, R., Stone, M., Wallace, M., Semple, C. and Gordon, C. ( 2001). Proteins containing the UBA domain are able to bind to multi-ubiquitin chains. Nature Cell Biology 3, 939–943.CrossRefGoogle Scholar
Wixon, J., Blaxter, M., Hope, I., Barstead, R. and Kim, S. ( 2000). Caenorhabditis elegans. Yeast 17, 37–42.Google Scholar
Wodarz, A. ( 2002). Establishing cell polarity in development. Nature Cell Biology 4, E39–E44.CrossRefGoogle Scholar
Wolstenholme, A. J., Fairweather, I., Prichard, R., Von Samson-Himmelstjerna, G. and Sangster, N. C. ( 2004). Drug resistance in veterinary helminths. Trends in Parasitology 20, 469–476.CrossRefGoogle Scholar
Wood, W. B. ( 1988). Preface. In The Nematode Caenorhabditis elegans, (ed. Wood, W. B.), pp. vii–viii. Cold Spring Harbor Laboratory Press, New York.
Yoder, J. H., Chong, H., Guan, K. L. and Han, M. ( 2004). Modulation of KSR activity in Caenorhabditis elegans by Zn ions, PAR-1 kinase and PP2A phosphatase. EMBO Journal 23, 111–119.CrossRefGoogle Scholar
Zhang, S. H., Kobayashi, R., Graves, P. R., Piwnica-Worms, H. and Tonks, N. K. ( 1997). Serine phosphorylation-dependent association of the band 4.1-related protein-tyrosine phosphatase PTPH1 with 14-3-3beta protein. Journal of Biological Chemistry 272, 27281–27287.Google Scholar