Skip to main content
×
×
Home

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

  • P. WIŃSKA (a1), B. GOŁOS (a1), J. CIEŚLA (a1), Z. ZIELIŃSKI (a1), T. FRĄCZYK (a1), E. WAŁAJTYS-RODE (a2) and W. RODE (a1)...
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.

Copyright
Corresponding author
Nencki Institute of Experimental Biology, 3 Pasteur Street, 02-093 Warszawa, Poland. Fax: +48 22 822 5342. E-mail: rode@nencki.gov.pl
References
Hide All

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, 2236222370.
BLAKLEY, R. L. ( 1984). Dihydrofolate reductase. In Folates and Pterines, Vol. 1, ( ed. Blakley, R. L. & Benkovic, S. J.), pp. 191253. Wiley, New York.
BRENNER, S. ( 1974). The genetics of Caenorhabditis elegans. Genetics 77, 7194.
BÜRGLIN, T. R., LABOS, E. & BLAXTER, M. L. ( 1998). Caenorhabditis elegans as a model for parasitic nematodes. International Journal for Parasitology 28, 395411.
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, 127136.
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, 233242.
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, 651658.
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, 440445.
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, 209221.
DESPOMMIER, D. D. ( 1998). How does Trichinella spiralis make itself at home? Parasitology Today 14, 318323.
EULING, S. & AMBROS, V. ( 1996). Reversal of cell fate determination in Caenorhabditis elegans vulval development. Development 122, 25072515.
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, 564565.
GOŁOS, B. & RODE, W. ( 1999). An isotopic assay of dUTPase activity based on coupling with thymidylate synthase. Acta Biochimica Polonica 46, 837840.
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. 519523. 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, 851857.
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, 35853597.
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, 361370.
JASMER, D. P. ( 1995). Trichinella spiralis: subversion of differentiated mammalian skeletal muscle cells, Parasitology Today 11, 185188.
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, 397406.
KIT, S. ( 1976). DNA synthesis and cancer. Molecular and Cellular Biochemistry 11, 161182.
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, 153159.
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, 389392.
LEWIS, J. A. and FLEMING, J. T. ( 1995). Basic culture methods. Methods in Cell Biology 48, 329.
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, 174182.
MATHEWS, C. K., SCRIMGEOUR, K. G. & HUENNEKENS, F. M. ( 1963). Dihydrofolate reductase. Methods in Enzymology 6, 364368.
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, 210219.
MORRISON, J. F. ( 1982). The slow-binding and slow, tight-binding inhibition of enzyme-catalysed reactions. Trends in Biochemical Sciences 7, 102105.
NAKATA, R., TSUKAMOTO, I., MIYOSHI, M. & KOJO, S. ( 1985). Liver regeneration after carbon tetrachloride intoxication in the rat. Biochemical Pharmacology 34, 586588.
PARDEE, A. B. ( 1989). G1 events and regulation of cell proliferation. Science 246, 603608.
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, 11511157.
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, 341351.
RIDDLE, D. L. ( 1988). The dauer larva. In The Nematode Caenorhabditis elegans (ed. Wood, W. B.), pp. 393412. 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. 739768. 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, 593600.
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, 1153811543.
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. 345398. 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, 427433.
SPECTOR, T. ( 1978). Refinement of the coomassie blue method of protein quantitation. Analytical Biochemistry 86, 142146.
VILPO, J. A. ( 1983). Mitogen induction of deoxyuridine triphosphatase activity in human T and B lymphocytes. Medical Biology 61, 5458.
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, 84358438.
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, PC11PC12.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 3
Total number of PDF views: 8 *
Loading metrics...

Abstract views

Total abstract views: 66 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 12th June 2018. This data will be updated every 24 hours.