Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-20T03:00:04.858Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental arrest in Caenorhabditis elegans dauer larvae causes high expression of enzymes involved in thymidylate biosynthesis, similar to that found in Trichinella muscle larvae

Published online by Cambridge University Press:  23 May 2005

P. WIŃSKA ,
B. GOŁOS ,
J. CIEŚLA ,
Z. ZIELIŃSKI ,
T. FRĄCZYK ,
E. WAŁAJTYS-RODE  and
W. RODE
P. WIŃSKA
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
B. GOŁOS
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
J. CIEŚLA
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
Z. ZIELIŃSKI
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
T. FRĄCZYK
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
E. WAŁAJTYS-RODE
Affiliation:
Rzeszów University of Technology Faculty of Chemistry, 3 Powstańców Warszawy Street, 35-959 Rzeszów, Poland
W. RODE
Affiliation:
Nencki Institute of Experimental Biology, Polish Academy of Sciences, 3 Pasteur Street, 02-093 Warsaw, Poland
Get access Rights & Permissions [Opens in a new window]

Abstract

Crude extract specific activities of thymidylate synthase, dUTPase, thymidine kinase and dihydrofolate reductase were high during the development of Caenorhabditis elegans, the dauer larva activities being similar to those previously determined in Trichinella spiralis and T. pseudospiralis muscle larvae (with the exception of thymidine kinase, not detected in Trichinella). High thymidylate synthase expression in developmentally arrested larvae, demonstrated also at the mRNA and protein levels, is in agreement with a global cell cycle arrest of dauer larvae and indicates this unusual cell cycle regulation pattern can be shared by developmentally arrested larvae of C. elegans and the two Trichnella species. Hence, the phenomenon may be characteristic for developmentally arrested larvae of different nematodes, rather than specific for the parasitic Trichinella muscle larvae. Endogenous C. elegans thymidylate synthase was purified and its molecular properties compared with those of the recombinant protein, expression of the latter in E. coli cells confirming the NCBI database sequence identity.

Keywords

thymidylate synthasedUTPasethymidine kinasedihydrofolate reductaseCaenorhabditis elegansTrichinella sppdevelopmental arrestdauer larvamuscle larvacell cycle
Type
Research Article
Information
Parasitology , Volume 131 , Issue 2 , August 2005 , pp. 247 - 254
Copyright
2005 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

BÉKÉSI, A., ZAGYVA, I, HUNYADI-GULYÁS, E., PONGRÁCZ, V., KOVÁRI, J., NAGY, Á. O., ERDEI, A., MEDZIHRADSZKY, K. F. & VÉRTESSY, B. G. ( 2004). Developmental regulation of dUTPase in Drosophila melanogaster. Journal of Biological Chemistry 279, 22362–22370.CrossRefGoogle Scholar
BLAKLEY, R. L. ( 1984). Dihydrofolate reductase. In Folates and Pterines, Vol. 1, ( ed. Blakley, R. L. & Benkovic, S. J.), pp. 191–253. Wiley, New York.
BRENNER, S. ( 1974). The genetics of Caenorhabditis elegans. Genetics 77, 71–94.Google Scholar
BÜRGLIN, T. R., LABOS, E. & BLAXTER, M. L. ( 1998). Caenorhabditis elegans as a model for parasitic nematodes. International Journal for Parasitology 28, 395–411.CrossRefGoogle Scholar
CIEŚLA, J., GOŁOS, B., DZIK, J. M., PAWEŁCZAK, K., KEMPNY, M., MAKOWSKI, M., BRETNER, M., KULIKOWSKI, T., MACHNICKA, B., RZESZOTARSKA, B. & RODE, W. ( 1995 a). Thymidylate synthases from Hymenolepis diminuta and regenerating rat liver: purification, properties, and inhibition by substrate and cofactor analogues. Biochimica et Biophysica Acta 1249, 127–136.Google Scholar
CIEŚLA, J., WEINER, K. X. B., WEINER, R. S., RESTON, J. T., MALEY, G. F. & MALEY, F. ( 1995 b). Isolation and expression of rat thymidylate synthase cDNA: phylogenetic comparison with human and mouse thymidylate synthases. Biochimica et Biophysica Acta 1261, 233–242.Google Scholar
CIEŚLA, J., GOŁOS, B., WAŁAJTYS-RODE, E., JAGIELSKA, E., PŁUCIENNICZAK, A. & RODE, W. ( 2002). The effect of Arg 209 to Lys mutation in mouse thymidylate synthase. Acta Biochimica Polonica 49, 651–658.Google Scholar
DĄBROWSKA, M., ZIELIŃSKI, Z., WRANICZ, M., MICHALSKI, R., PAWEŁCZAK, K. & RODE, W. ( 1996). Trichinella spiralis thymidylate synthase: developmental pattern, isolation, molecular properties and inhibition by substrate and cofactor analogues. Biochemical and Biophysical Research Communications 228, 440–445.CrossRefGoogle Scholar
DĄBROWSKA, M., JAGIELSKA, E., CIEŚLA, J., PŁUCIENNICZAK, A., KWIATOWSKI, J., WRANICZ, M., BOIREAU, P. & RODE, W. ( 2004). Trichinella spiralis thymidylate synthase: cDNA cloning and sequencing, and developmental pattern of mRNA expression. Parasitology 128, 209–221.CrossRefGoogle Scholar
DESPOMMIER, D. D. ( 1998). How does Trichinella spiralis make itself at home? Parasitology Today 14, 318–323.Google Scholar
EULING, S. & AMBROS, V. ( 1996). Reversal of cell fate determination in Caenorhabditis elegans vulval development. Development 122, 2507–2515.Google Scholar
FARLAND, W. H. & MACINNIS, A. J. ( 1978). In vitro thymidine kinase activity: present in Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala) but apparently lacking in Ascaris lumbricoides (Nematoda). Journal of Parasitology 64, 564–565.CrossRefGoogle Scholar
GOŁOS, B. & RODE, W. ( 1999). An isotopic assay of dUTPase activity based on coupling with thymidylate synthase. Acta Biochimica Polonica 46, 837–840.Google Scholar
GOŁOS, B., WAŁAJTYS-RODE, E., PORĘBSKA, A., CIEŚLA, J., DĄBROWSKA, M., ZIELIŃSKI, Z. & RODE, W. ( 2002). Thymidylate synthase heterogeneity assessed by monoclonal antibodies. In Chemistry and Biology of Pteridines and Folates 2001 ( ed. Milstien, S., Kapatos, G., Levine, R. A. & Shane, B.), pp. 519–523. Kluwer Academic Publishers, Boston.
HOKARI, S., HASEGAWA, M., SAKAGISHI, Y. & KIKUCHI, G. ( 1987). Deoxyuridine triphosphate nucleotidohydrolase activity and its correlation with multiplication of erythroid cells in rat spleen. Biochemistry International 14, 851–857.Google Scholar
HONG, Y., ROY, R. & AMBROS, V. ( 1998). Developmental regulation of a cyclin-dependent kinase inhibitor controls postembryonic cell cycle progression in Caenorhabditis elegans. Development 125, 3585–3597.Google Scholar
JAFFE, J. J., COMLEY, J. C. & CHRIN, L. R. ( 1982). Thymidine kinase activity and thymidine salvage in adult Brugia pahangi and Dirofilaria immitis. Molecular and Biochemical Parasitology 5, 361–370.CrossRefGoogle Scholar
JASMER, D. P. ( 1995). Trichinella spiralis: subversion of differentiated mammalian skeletal muscle cells, Parasitology Today 11, 185–188.Google Scholar
JOHNSON, L. F., FUHRMAN, C. L. & WIEDEMANN, L. M. ( 1978). Regulation of dihydrofolate reductase gene expression in mouse fibroblasts during the transition from the resting to growing state. Journal of Cellular Physiology 97, 397–406.CrossRefGoogle Scholar
KIT, S. ( 1976). DNA synthesis and cancer. Molecular and Cellular Biochemistry 11, 161–182.CrossRefGoogle Scholar
KURATLI, S., LINDH, J. G., GOTTSTEIN, B., SMITH, D. F. & CONNOLLY, B. ( 1999). Trichinella spp: differential expression of two genes in the muscle larva of encapsulating and nonencapsulating species. Experimental Parasitology 93, 153–159.CrossRefGoogle Scholar
LEE, Y., SHEN, G. & JOHNSON, L. F. ( 1999). Complex transcriptional initiation patteren of the thymidylate synthase promoter in mouse tissues. Archives of Biochemistry and Biophysics 372, 389–392.CrossRefGoogle Scholar
LEWIS, J. A. and FLEMING, J. T. ( 1995). Basic culture methods. Methods in Cell Biology 48, 3–29.CrossRefGoogle Scholar
LIU, J., SCHMITZ, J. C., LIN, X., TAI, N., YAN, W., FARRELL, M., BAILLY, M., CHEN, T. & CHU, E. ( 2002). Thymidylate synthase as a translational regulator of cellular gene expression, Biochimica et Biophysica Acta 1587, 174–182.Google Scholar
MATHEWS, C. K., SCRIMGEOUR, K. G. & HUENNEKENS, F. M. ( 1963). Dihydrofolate reductase. Methods in Enzymology 6, 364–368.CrossRefGoogle Scholar
MIKIEWICZ, D., WROBEL, B., WĘGRZYN, G. & PŁUCIENNICZAK, A. ( 1997). Isolation and characterization of a ColE1-like plasmid from Enterobacter agglomerans with a novel variant of rom gene. Plasmid 38, 210–219.CrossRefGoogle Scholar
MORRISON, J. F. ( 1982). The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions. Trends in Biochemical Sciences 7, 102–105.CrossRefGoogle Scholar
NAKATA, R., TSUKAMOTO, I., MIYOSHI, M. & KOJO, S. ( 1985). Liver regeneration after carbon tetrachloride intoxication in the rat. Biochemical Pharmacology 34, 586–588.CrossRefGoogle Scholar
PARDEE, A. B. ( 1989). G1 events and regulation of cell proliferation. Science 246, 603–608.CrossRefGoogle Scholar
PESTALOZZI, B. C., MCGINN, C. J., KINSELLA, T. J., DRAKE, J. C., GLENNON, M. C., ALLEGRA, C. J. & JOHNSTON, P. G. ( 1995). Increased thymidylate synthase protein levels are principally associated with proliferation but not cell cycle phase in asynchronous human cancer cells. British Journal of Cancer 71, 1151–1157.CrossRefGoogle Scholar
RAHMAN, L., VOELLER, D., RAHMAN, M., LIPKOWITZ, S., ALLEGRA, C., BARRETT, J. C., KAYE, F. J. & ZAJAC-KAYE, M. ( 2004). Thymidylate synthase as an oncogene: a novel role for an essential DNA synthesis enzyme. Cancer Cell 5, 341–351.CrossRefGoogle Scholar
RIDDLE, D. L. ( 1988). The dauer larva. In The Nematode Caenorhabditis elegans (ed. Wood, W. B.), pp. 393–412. Cold Spring Harbor Laboratory Press, New York.
RIDDLE, D. L. & ALBERT, P. S. ( 1997). Genetic and environmental regulation of dauer larva development. In C. elegans II ( ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R.), pp. 739–768. Cold Spring Harbor Laboratory Press, New York.
RODE, W., DĄBROWSKA, M., ZIELIŃSKI, Z., GOŁOS, B., WRANICZ, M., FELCZAK, K. & KULIKOWSKI, T. ( 2000). Trichinella spiralis and Trichinella pseudospiralis: developmental patterns of enzymes involved in thymidylate biosynthesis and thymidylate synthase as a potential target in chemotherapy. Parasitology 120, 593–600.CrossRefGoogle Scholar
RODE, W., SCANLON, K. J., HYNES, J. and BERTINO, J. R. ( 1979). Purification of mammalian tumor (L1210) thymidylate synthetase by affinity chromatography on stable biospecific adsorbent. Stabilization of the enzyme with neutral detergents. Journal of Biological Chemistry 254, 11538–11543.Google Scholar
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. ( 1989). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor Laboratory Press, New York.
SANTI, D. V. & DANENBERG, P. V. ( 1984). Folates in pyrimidine biosynthesis. In Folates and Pterines, Vol. 1 ( ed. Blakley, R. L. & Benkovic, S. J.), pp. 345–398. Wiley, New York.
SO, N. N. C., WONG, P. C. L. & KO, R. C. ( 1992). Precursors of pyrimidine nucleotide biosynthesis for gravid Angiostrongylus cantonensis (Nematoda: Metastrongyloidea). International Journal for Parasitology 22, 427–433.CrossRefGoogle Scholar
SPECTOR, T. ( 1978). Refinement of the coomassie blue method of protein quantitation. Analytical Biochemistry 86, 142–146.CrossRefGoogle Scholar
VILPO, J. A. ( 1983). Mitogen induction of deoxyuridine triphosphatase activity in human T and B lymphocytes. Medical Biology 61, 54–58.Google Scholar
WADSWORTH, W. G. & RIDDLE, D. L. ( 1988). Acidic intracellular pH shift during Caenorhabditis elegans larval development. Proceedings of the National Academy of Sciences, USA 85, 8435–8438.CrossRefGoogle Scholar
WAHBA, A. J. & FRIEDKIN, M. ( 1961). Direct spectrophotometric evidence for the oxidation of tetrahydrofolate during the enzymatic synthesis of thymidylate. Journal of Biological Chemistry 236, PC11–PC12.Google Scholar