Functional GATA- and initiator-like-elements exhibit a similar arrangement in the promoters of Caenorhabditis elegans polyamine synthesis enzymes
-
Kai Lüersen
, Marie-Luise Eschbach , Eva Liebau und Rolf D. Walter
Abstract
Polyamines are essential cell constituents involved in growth processes. In Caenorhabditis elegans the polyamine synthetic pathway consists of three enzymes, ornithine decarboxylase (ODC), S-adenosylmethionine decarboxylase (AdoMetDC) and spermidine synthase. Their gene expression pattern was determined in C. elegans by microinjection of green fluorescent protein (GFP) reporter gene constructs. All transgenic animals exhibited GFP expression in their intestinal cells. For the AdoMetDC promoter, fluorescence was additionally observed in dopaminergic neurons, while the ODC promoter also drives a male-specific GFP expression in the distal part of the reproductive system. The minimal promoter regions for intestine-specific expression of the AdoMetDC and spermidine synthase genes were determined by deletion mutants. Using the Seqcomp and Family Relation programs, a similar arrangement of putative cis-regulatory elements within these regions and also within the respective regions of the orthologous Caenorhabditis briggsae genes were found. The functional conservation of the latter was confirmed by heterologous transformation experiments. Moreover, the involvement of putative GATA- and initiator-(Inr)-like-elements in gene expression was determined by mutagenesis studies. RNase protection assay revealed that the Inr-like-element does not represent the main transcriptional start site, at least of C. elegans spermidine synthase. In conclusion, a similar minimal promoter architecture was found for C. elegans as well as C. briggsae AdoMetDC and spermidine synthase, two genes that participate in the same metabolic pathway.
References
Britton, C., McKerrow, J.H. and Johnstone, I.L. (1998). Regulation of the Caenorhabditis elegans gut cysteine protease gene cpr-1: requirement for GATA motifs. J. Mol. Biol.283, 15–27.10.1006/jmbi.1998.2093Suche in Google Scholar
Brown, C.T., Rust, A.G., Clarke, P.J., Pan, Z., Schilstra, M.J., De Buysscher, T., Griffin, G., Wold, B.J., Cameron, R.A., Davidson, E.H. and Bolouri, H. (2002). New computational approaches for analysis of cis-regulatory networks. Dev. Biol.246, 86–102.10.1006/dbio.2002.0619Suche in Google Scholar
Da’dara, A.A. and Walter, R.D. (1998). Molecular and biochemical characterization of S-adenosylmethionine decarboxylase from the free-living nematode Caenorhabditis elegans. Biochem. J.336, 545–550.10.1042/bj3360545Suche in Google Scholar
Fukushige, T., Hawkins, M.G. and McGhee, J.D. (1998). The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev. Biol.198, 286–302.10.1016/S0012-1606(98)80006-7Suche in Google Scholar
Fukushige, T., Hendzel, M.J., Bazett-Jones, D.P. and McGhee, J.D. (1999). Direct visualization of the elt-2 gut-specific GATA factor binding to a target promoter inside the living Caenorhabditis elegans embryo. Proc. Natl. Acad. Sci. USA96, 11883–11888.10.1073/pnas.96.21.11883Suche in Google Scholar PubMed PubMed Central
Granato, M., Schnabel, H. and Schnabel, R. (1994). pha-1, a selectable marker for gene transfer in C. elegans. Nucleic Acids Res.22, 1762–1763.10.1093/nar/22.9.1762Suche in Google Scholar PubMed PubMed Central
Haghighi, A.P. and Cooper, E. (1998). Neuronal nicotinic acetylcholine receptors are blocked by intracellular spermine in a voltage-dependent manner. J. Neurosci.18, 4050–4062.10.1523/JNEUROSCI.18-11-04050.1998Suche in Google Scholar
Hanfrey, C., Franceschetti, M., Mayer, M.J., Illingworth, C., Elliott, K., Collier, M., Thompson, B., Perry, B. and Michael, A.J. (2003). Translational regulation of the plant S-adenosylmethionine decarboxylase. Biochem. Soc. Trans.31, 424–427.10.1042/bst0310424Suche in Google Scholar PubMed
Heby, O. (1981). Role of polyamines in the control of cell proliferation and differentiation. Differentiation19, 1–20.10.1111/j.1432-0436.1981.tb01123.xSuche in Google Scholar PubMed
Igarashi, K. and Kashiwagi, K. (2000). Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun.271, 559–564.10.1006/bbrc.2000.2601Suche in Google Scholar PubMed
Jansen, G., Hazendonk, E., Thijssen, K.L. and Plasterk, R.H. (1997). Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat. Genet.17, 119–121.10.1038/ng0997-119Suche in Google Scholar
Kirouac, M. and Sternberg, P.W. (2003). cis-Regulatory control of three cell fate-specific genes in vulval organogenesis of Caenorhabditis elegans and C. briggsae. Dev. Biol.257, 85–103.10.1016/S0012-1606(03)00032-0Suche in Google Scholar
Liston, D.R., Lau, A.O., Ortiz, D., Smale, S.T. and Johnson, P.J. (2001). Initiator recognition in a primitive eukaryote: IBP39, an initiator-binding protein from Trichomonas vaginalis. Mol. Cell. Biol.21, 7872–7882.10.1128/MCB.21.22.7872-7882.2001Suche in Google Scholar
Lu, Z. and Ding, L. (1999). Blockade of a retinal cGMP-gated channel by polyamines. J. Gen. Physiol.113, 35–43.10.1085/jgp.113.1.35Suche in Google Scholar
Macrae, M., Plasterk, R.H.A. and Coffino, P. (1995). The ornithine decarboxylase gene of Caenorhabditis elegans: cloning, mapping and mutagenesis. Genetics140, 517–525.10.1093/genetics/140.2.517Suche in Google Scholar
Macrae, M., Kramer, D.L. and Coffino, P. (1998). Developmental effect of polyamine depletion in Caenorhabditis elegans. Biochem. J.333, 309–315.10.1042/bj3330309Suche in Google Scholar
Maduro M.F. and Rothman J.H. (2002). Making worm guts: the gene regulatory network of the Caenorhabditis elegans endoderm. Dev. Biol.246, 68–85.10.1006/dbio.2002.0655Suche in Google Scholar
Mello, C. and Fire, A. (1995). DNA transformation. Methods Cell. Biol.48, 451–512.10.1016/S0091-679X(08)61399-0Suche in Google Scholar
Mello, C., Kramer, J.M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J.10, 3959–3970.Suche in Google Scholar
Moilanen, L.H., Fukushige, T. and Freedman, J.H. (1999). Regulation of metallothionein gene transcription. Identification of upstream regulatory elements and transcription factors responsible for cell-specific expression of the metallothionein genes from Caenorhabditis elegans. J. Biol. Chem.274, 29655–29665.10.1074/jbc.274.42.29655Suche in Google Scholar PubMed
Ndjonka, D., Da’dara, A.A., Walter, R.D. and Lüersen, K. (2003). Caenorhabditis elegans S-adenosylmethionine decarboxylase is highly stimulated by putrescine but exhibits a low specificity for activator binding. Biol. Chem.384, 83–91.10.1515/BC.2003.009Suche in Google Scholar PubMed
Panchenko, V.A., Glasser, C.R., Partin, K.M. and Mayer, M.L. (1999). Amino acid substitutions in the pore of rat glutamate receptors at sites influencing block by polyamines. J. Physiol.520, 337–357.10.1111/j.1469-7793.1999.t01-1-00337.xSuche in Google Scholar PubMed PubMed Central
Pearson, W.L. and Nichols, C.G. (1998). Block of the Kir2.1 channel pore by alkylamine analogues of endogenous polyamines. J. Gen. Physiol.112, 351–363.Suche in Google Scholar
Ruan, H., Shantz, L.M., Pegg, A.E. and Morris, D.R. (1996). The upstream open reading frame of the mRNA encoding S-adenosylmethionine decarboxylase is a polyamine-responsive translational control element. J. Biol. Chem.271, 29576–29582.10.1074/jbc.271.47.29576Suche in Google Scholar PubMed
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989). Molecular cloning: a Laboratory Manual, 2nd Edition (Cold Spring Harbor, NY, USA: Cold Spring Harbor Press).Suche in Google Scholar
Santel, A., Kaufmann, J., Hyland, R. and Renkawitz-Pohl, R. (2000). The initiator element of the Drosophila β2 tubulin gene core promoter contributes to gene expression in vivo but is not required for male germ-cell specific expression. Nucleic Acids Res.28, 1439–1446.10.1093/nar/28.6.1439Suche in Google Scholar PubMed PubMed Central
Smale, S.T., Jain, A., Kaufmann, J., Emami, K.H., Lo, K. and Garraway, I.P. (1998). The initiator element: a paradigm for core promoter heterogeneity within metazoan protein-coding genes. Cold Spring Harb. Symp. Quant. Biol. 63, 21–31.10.1101/sqb.1998.63.21Suche in Google Scholar PubMed
Sulston, J. (1988). Cell lineage. In: The Nematode Caenorhabditis elegans, W.B. Wood, ed. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Press), pp. 123–155.Suche in Google Scholar
Sulston, J. and Hodgkin, J. (1988). Methods. In: The Nematode Caenorhabditis elegans, W.B. Wood, ed. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Press), pp. 587–606.Suche in Google Scholar
Sulston, J., Dew, M. and Brenner, S. (1975). Dopaminergic neurons in the nematode Caenorhabditis elegans. J. Comp. Neurol.163, 215–226.10.1002/cne.901630207Suche in Google Scholar PubMed
Tabor, C.W. and Tabor, H. (1984). Polyamines. Annu. Rev. Biochem.53, 749–790.10.1146/annurev.bi.53.070184.003533Suche in Google Scholar PubMed
Thomas, T. and Thomas, T.J. (2001). Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. Cell. Mol. Life Sci.58, 244–258.10.1007/PL00000852Suche in Google Scholar PubMed
White, J. (1988). The anatomy. In: The Nematode Caenorhabditis elegans, W.B. Wood, ed. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Press), pp. 81–122.Suche in Google Scholar
© Walter de Gruyter
Artikel in diesem Heft
- Molecular genetics of human cervical cancer: role of papillomavirus and the apoptotic cascade
- Regulatory role of membrane-bound peptidases in the progression of gynecologic malignancies
- Functional genomics identifies novel and diverse molecular targets of nutrients in vivo
- Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction
- Functional GATA- and initiator-like-elements exhibit a similar arrangement in the promoters of Caenorhabditis elegans polyamine synthesis enzymes
- Fluid shear stress induces endothelial KLF2 gene expression through a defined promoter region
- Recombinant expression, purification and cross-reactivity of chenopod profilin: rChe a 2 as a good marker for profilin sensitization
- Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding
- Distinctive functional features in prokaryotic and eukaryotic Cu,Zn superoxide dismutases
- Tumour-expressed CD43 (sialophorin) mediates tumour-mesothelial cell adhesion
Artikel in diesem Heft
- Molecular genetics of human cervical cancer: role of papillomavirus and the apoptotic cascade
- Regulatory role of membrane-bound peptidases in the progression of gynecologic malignancies
- Functional genomics identifies novel and diverse molecular targets of nutrients in vivo
- Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction
- Functional GATA- and initiator-like-elements exhibit a similar arrangement in the promoters of Caenorhabditis elegans polyamine synthesis enzymes
- Fluid shear stress induces endothelial KLF2 gene expression through a defined promoter region
- Recombinant expression, purification and cross-reactivity of chenopod profilin: rChe a 2 as a good marker for profilin sensitization
- Cellular prion protein acquires resistance to proteolytic degradation following copper ion binding
- Distinctive functional features in prokaryotic and eukaryotic Cu,Zn superoxide dismutases
- Tumour-expressed CD43 (sialophorin) mediates tumour-mesothelial cell adhesion