Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T23:04:49.512Z Has data issue: false hasContentIssue false
  • English
  • Français

Intracellular trafficking of micronutrients: from gene regulation to nutrient requirements

Published online by Cambridge University Press:  19 December 2008

John E. Hesketh  and
Stéphane Villette
John E. Hesketh*
Affiliation:
Department of Biological and Nutritional Sciences, University of Newcastle, Newcastle-upon-Tyne NE1 7RU, UK
*
*Corresponding author: Professor John Hesketh, fax +44 191 222 8684, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Résumé

La distribution intracellulaire des micronutriments ainsi que leur absorption sont importantes pour les fonctions cellulaires. Dans certains cas la distribution des micronutriments ou des protéines associées est déterminée par des mécanismes liés à l'expression des gènes. La région 3' non traduite (3'UTR) de l'ARNm de la métallothioneine-1 détermine la localisation de ce message et, par conséquent, la localisation intracellulaire de la protéine qu'il code. En utilisant des cellules transfectées nous avons montré que la métallothioneine-1 est transportée vers le noyau ou elle exerce un rôle dans la protection contre le stress oxydant et les dommages causés à l'ADN. Quand l'apport nutritionnel en Se est limité, l'expression des sélénoproteines est altérée. Toutefois celle-ci n'est pas affectée de fac¸on identique pour toutes les sélénoproteines; le Se disponible étant utilisé de fac¸on prioritaire pour la synthèse de certaines d'entre elles. Cet ordre de priorité met en jeu des différences dans la traduction et la stabilité de leur ARNm qui sont sous le controle de séquences dans la région 3' non traduite. Potentiellement, des variations génétiques affectant ces mécanismes régulateurs peuvent moduler les besoins en nutriments. Des polymorphismes génétiques ont été décrits dans le 3'UTR des ARNm de deux sélénoproteines; l'un d'entre eux affectant la synthèse de la sélénoproteine correspondante. Ces exemples illustrent comment des approches moléculaires peuvent contribuer à accroître notre compréhension du métabolisme et des besoins en nutriments à différents niveaux. Premièrement, elles permettent d'étudier les effets régulateurs des gènes et de leurs produits. Ensuite, la compréhension de ces effets peut fournir un modèle pour étudier le métabolisme des nutriments au niveau cellulaire. Ainsi, lorsque des effets essentiels sont identifiés, la connaissance du génome humain et les bases de données sur les polymorphismes génétiques constituent des outils complémentaires pour définir l'étendue de la variation génétique des gènes revêtant une importance nutritionnelle. Enfin, la fonctionnalité de ces variations peut être définie et des sous-groupes de la population, possédant des besoins nutritionnels différents, peuvent etre identifiés.

Keywords

Nutrient-gene interactionsPolymorphismSeleniumMetallothionein3' Untranslated region
Type
Symposium on ‘Nutrition in the post-genomic era’ Plenary session 2: Nutrient regulation of gene expression
Information
Proceedings of the Nutrition Society , Volume 61 , Issue 4 , November 2002 , pp. 405 - 414
Copyright
Copyright © The Nutrition Society 2002

References

Apostolova, MD, Ivanova, IA & Cherian, MG (1999) Metallothionein and apoptosis during differentiation of myo- blasts to myotubes: protection against free radical toxicity. Toxicology and Applied Pharmacology 159, 175–184.CrossRefGoogle Scholar
Apostolova, MD, Ivanova, IA & Cherian, MG (2000) Signal transduction pathways and nuclear translocation of zinc and metallothionein during differentiation of myoblasts. Biochemistry and Cell Biology 78, 27–37.CrossRefGoogle ScholarPubMed
Beck, MA (1996) The role of nutrition in viral disease. Nutritional Biochemistry 17, 683–690.CrossRefGoogle Scholar
Behne, D, Hilmert, H, Scheid, S, Gessner, H & Elger, W (1998) Evidence for specific selenium target tissues and new biologically important selenoproteins. Biochimica et Biophysica Acta 966, 12–21.CrossRefGoogle Scholar
Bermano, G, Arthur, JR & Hesketh, JE (1996) Role of the 3' untranslated region in the regulation of cytosolic glutathione peroxidase and phospholipid-hydroperoxide glutathione peroxidase gene expression by selenium supply. Biochemical Journal 320, 891–895.CrossRefGoogle ScholarPubMed
Bermano, G, Nicol, F, Dyer, A, Sunde, RA, Beckett, GJ, Arthur, JR & Hesketh, JE (1995) Tissue-specific regulation of selenoenzyme gene expression during selenium deficiency in rats. Biochemical Journal 311, 425–430.CrossRefGoogle ScholarPubMed
Bernlohr, DA, Coe, NR & Licata, VJ (1999) Fatty acid trafficking in the adipocyte. Seminars in Cell and Developmental Biology 10, 43–49.Google Scholar
Berry, MJ, Banu, L, Chen, YY, Mandel, SJ, Kieffer, JD, Harney, JW & Larsen, PR (1991a) Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3' untranslated region. Nature 353, 273–276.CrossRefGoogle ScholarPubMed
Berry, MJ, Banu, L, Harney, JW & Larsen, PR (1993) Functional characterization of the eukaryotic SECIS elements which direct selenocysteine insertion at UGA codons. EMBO Journal 12, 3315–3322.CrossRefGoogle ScholarPubMed
Berry, MJ, Banu, L & Larsen, PR (1991b) Type-I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature 349, 438–440.CrossRefGoogle ScholarPubMed
Berry, MJ & Larsen, PR (1993) Recognition of UGA as a selenocysteine codon in eukaryotes: a review of recent progress. Biochemical Society Transactions 21, 827–832.CrossRefGoogle ScholarPubMed
Berry, MJ, Tujebajeva, RM, Copeland, PR, Xu, XM, Carlson, BA, Martin GW, III, Low, SC, Mansell, JB, Grundner-Culemann, E, Harney, JW, Driscoll, DM & Hatfield, DF (2001) Selenocysteine incorporation directed from the 3'UTR: Characterization of eukaryotic EFsec and mechanistic implications. BioFactors 14, 17–24.CrossRefGoogle ScholarPubMed
Bremner, I & Beattie, JH (1990) Metallothioneins and the trace minerals. Annual Reviews of Nutrition 10, 63–83.CrossRefGoogle ScholarPubMed
Brigelius-Flohé, R (1999) Tissue-specific functions of individual glutathione peroxidases. Free Radical Biology and Medicine 27, 951–965.CrossRefGoogle ScholarPubMed
Brown, KM, Pickard, K, Nicol, F, Beckett, GJ, Duthie, GG & Arthur, JR (2000) Effects of organic and inorganic selenium supplementation on selenoenzyme activity in blood lymphoctyes, granulocytes, platelets and erythrocytes. Clinical Science 98, 593–599.CrossRefGoogle Scholar
Chambers, I & Harrison, PR (1987) A new puzzle in selenoprotein biosynthesis - Selenocysteine seems to be encoded by the Stop codon, UGA. Trends In Biochemical Sciences 12, 255–256.CrossRefGoogle Scholar
Clark, LC, Combs, GF, Turnbull, BW, Slate, E, Alberts, D, Abele, D, Allison, R, Bradshaw, J, Chalker, D, Chow, J, Curtis, D, Dalen, J, Davis, L, Deal, R & Dellasega, M (1997) The nutritional prevention of cancer with selenium 1983-1993: a randomized clinical trial. Journal of the American Medical Association 276, 1957–1963.CrossRefGoogle Scholar
Copeland, PR, Fletcher, JR, Carlson, BA, Hatfield, DL & Driscoll, DM (2000) A novel RNA binding protein, SBP2, is required for the translation of mammalian selenoprotein mRNAs. EMBO Journal 19, 306–314.CrossRefGoogle ScholarPubMed
Dalgleish, GD, Veyrune, J-L, Blanchard, J-M & Hesketh, JE (2001) mRNA localization by a 145- nucleotide region of the c-fos 3' untranslated region. Journal of Biological Chemistry 276, 13593–13599.CrossRefGoogle ScholarPubMed
Desvergne, B & Wahli, W (1999) Peroxisome-proliferator activated receptors: nuclear control of metabolism. Endocrine Review 20, 649–688.Google ScholarPubMed
Diamond, AM, Hu, YJ & Mansur, DB (2001) Glutathione peroxidase and viral replication: Implications for viral evolution and chemoprevention. BioFactors 14, 205–210.CrossRefGoogle ScholarPubMed
Fletcher, JE, Copeland, PR, Driscoll, DM & Krol, A (2001) The selenocysteine incorporation machinery: Interactions between the SECIS RNA and the SECIS-binding protein SBP2. RNA 7, 1442–1453.Google ScholarPubMed
Gaub, M-P, Lutz, Y, Ghyselinck, NB, Scheuer, I, Pfister, V, Chambon, P & Rochette-Egly, C (1998) Nuclear detection of cellular retinoic acid binding proteins I and II with new antibodies. Journal of Histochemistry and Cytochemistry 46, 1103–1111.CrossRefGoogle ScholarPubMed
Gustafson, A-L, Donovan, M, Annerwall, E, Dencker, L & Eriksson, U (1996) Nuclear import of cellular retinoic acid-binding protein type I in mouse embryonic cells. Mechanisms in Development 58, 27–38.CrossRefGoogle ScholarPubMed
Heider, J, Baron, C & Bock, A (1992) Coding from a distance - Dissection of the messenger - RNA determinants required for the incorporation of selenocysteine into protein. EMBO Journal 11, 3759–3766.CrossRefGoogle ScholarPubMed
Hentze, MW & Kulozik, AE (1999) A perfect message: RNA surveillance and nonsense-mediated decay. Cell 96, 307–310.CrossRefGoogle ScholarPubMed
Hesketh, JE, Campbell, GP, Piechaczyk, M & Blanchard, J-M (1994) Targeting of c-myc and ß-globin coding sequences to cytoskeletal-bound polysomes by c-myc 3' untranslated region. Biochemical Journal 298, 143–148.CrossRefGoogle Scholar
Hesketh, JE, Vasconcelos, MH & Bermano, G (1998) Regulatory signals in messenger RNA: determinants of nutrient-gene interaction and metabolic compartmentation. British Journal of Nutrition 80, 307–321.Google ScholarPubMed
Hill, KE, Lloyd, RS & Burk, RF (1993) Conserved nucleotide sequences in the open reading frame and 3' untranslated region of selenoprotein P mRNA. Proceedings of the National Academy of Sciences USA 90, 537–541.CrossRefGoogle ScholarPubMed
Hu, YJ, Korotkov, KV, Mehta, R, Hatfield, DL, Rotimi, CN, Luke, A, Prewitt, TE, Cooper, RS, Stock, W, Vokes, EE, Dolan, ME, Gladyshev, VN & Diamond, AM (2001) Distribution and functional consequences of nucleotide polymorphisms in the 3'-untranslated region of the human Sep15 gene. Cancer Research 61, 2307–2310.Google ScholarPubMed
Hubert, N, Walczak, R, Carbon, P & Krol, A (1996) A protein binds the selenocysteine insertion element in the 3'UTR of mammalian selenoprotein mRNAs. Nucleic Acids Research 24, 464–469.CrossRefGoogle Scholar
Kim, IY & Stadtman, TC (1995) Selenophosphate synthetase - Detection in extracts of rat-tissues by immunoblot assay and partial-purification of the enzyme from the archean Methanococcus-Vannielii. Proceedings of the National Academy of Sciences USA 92, 7710–7713.CrossRefGoogle Scholar
Kislauskis, EH, Li, Z, Taneja, KL & Singer, RH (1993) Isoform-specific 3'untranslated sequences sort α-cardiac and ß-cytoplasmic actin messenger RNAs to different cytoplasmic compartments. Journal of Cell Biology 123, 165–172.CrossRefGoogle Scholar
Kohrle, J, Brigelius-Flohé, R, Bock, A, Gartner, R, Meyer, O & Flohé, L (2000) Selenium in biology: Facts and medical perspectives. Biological Chemistry 381, 849–864.CrossRefGoogle Scholar
Koonin, EV, Bork, P & Sander, C (1994) A novel RNA-binding motif in omnipotent suppressor of translation termination, ribosomal-proteins and a ribosome modification enzyme. Nucleic Acids Research 22, 2166–2167.CrossRefGoogle Scholar
Lei, XG, Evenson, JK, Thompson, KM & Sunde, RA (1995) Glutathione peroxidase and phospholipid hydroperoxide glutathione peroxidase are differentially regulated in rats by dietary selenium. Journal of Nutrition 125, 1438–1446.Google ScholarPubMed
Lesoon, A, Metha, A, Singh, R, Chisolm, GM & Driscoll, DM (1997) An RNA-binding protein recognizes a mammalian selenocysteine insertion sequence element required for cotranslational incorporation of selenocysteine. Molecular and Cellular Biology 17, 1977–1985.CrossRefGoogle ScholarPubMed
Levadoux, M, Mahon, C, Beattie, JH, Wallace, HM & Hesketh, JE (1999) Nuclear import of metallothionein requires its mRNA to be associated with the perinuclear cytoskeleton. Journal of Biological Chemistry 274, 34961–34966.CrossRefGoogle ScholarPubMed
Levadoux-Martin, M & Hesketh, JE (2002) Localisation of metallothionein in CHO cells requires a 41-nucleotide sequence within the 3' untranslated region. Biochemical Society Transactions (In the Press).Google Scholar
Levadoux-Martin, M, Hesketh, JE, Beattie, JH & Wallace, HM (2001) Influence of metallothionein-1 localisation on its function. Biochemical Journal 355, 473–479.CrossRefGoogle ScholarPubMed
Low, SC, Grundner-Culemann, E, Harney, JW & Berry, MJ (2000) SECIS-SBP2 interactions dictate selenocysteine incorporation efficiency and selenoprotein hierarchy. EMBO Journal 19, 6882–6890.CrossRefGoogle ScholarPubMed
Low, SC, Harney, JW & Berry, MJ (1995) Cloning and functional characterization of human selenophosphate synthetase, an essential component of selenoprotein synthesis. Journal of Biological Chemistry 270, 21659–21664.CrossRefGoogle ScholarPubMed
Maehira, F, Luyo, GA, Miyagi, I, Oshiro, M, Yamane, N, Kuba, M & Nakazato, Y (2002) Alterations of serum selenium concentrations in the acute phase of pathological conditions. Clinica Chimica Acta 316, 137–146.CrossRefGoogle ScholarPubMed
Mahon, P, Beattie, JH, Glover, LA & Hesketh, JE (1995) Localisation of metallothionein isoform mRNAs in rat hepatoma (H4) cells. FEBS Letters 373, 76–80.CrossRefGoogle ScholarPubMed
Mahon, PC, Partridge, K, Beattie, JM, Glover, LA & Hesketh, JE (1997) The 3'untranslated region plays a rôle in the targeting of metallothionein-1 mRNA to the perinuclear cytoplasm and cytoskeletal-bound polysomes. Biochimica et Biophysica Acta 1358, 153–162.CrossRefGoogle Scholar
Maquat, LE (2001) Evidence that selenium deficiency results in the cytoplasmic decay of GPX1 mRNA dependent on pre-mRNA splicing proteins bound to the mRNA exon-exon junction. Bio Factors 14, 37–42.Google Scholar
Ministry of Agriculture, Fisheries and Food (1997) Dietary Intake of Selenium. Food Surveillance Information Sheet No. 127. London: H.M. Stationery Office.Google Scholar
Molnar, J, MacPherson, A, Barclay, I & Molnar, P (1995) Selenium content of convenience and fast foods in Ayrshire, Scotland. International Journal of Food Sciences and Nutrition 46, 343–352.CrossRefGoogle ScholarPubMed
Nagy, E & Maquat, LE (1998) A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends In Biochemical Sciences 23, 198–199.CrossRefGoogle ScholarPubMed
Noy, N (2001) Retinoid-binding proteins: mediators of retinoid action. Biochemical Journal 348, 481–495.CrossRefGoogle Scholar
Pagmantidis, V, Bermano, G, Broom, I, Arthur, JR & Hesketh, JE (2002) Selenoprotein expression in the rat colon during Se deficiency. Proceedings of Nutrition Society 61, 51A.Google Scholar
Panemangalore, M, Banerjee, D, Onosaka, S & Cherian, MG (1983) Changes in the intracellular accumulation and distribution of metallothionein in rat liver and kidney during postnatal development. Developmental Biology 97, 95–102.CrossRefGoogle ScholarPubMed
Rayman, MP (2000) The importance of selenium to human health. Lancet 356, 233–241.CrossRefGoogle ScholarPubMed
Ruff, SJ & Ong, DE (2000) Cellular retinoic acid binding protein is associated with mitochondria. FEBS Letters 487, 282–286.CrossRefGoogle ScholarPubMed
Salvatore, D, Low, SC, Berry, MJ, Maia, AL, Harney, JW, Croteau, W, St, Germain DL & Larsen, PR (1995) Type-3 iodothyronine deiodinase - Cloning, in-vitro expression, and functional-analysis of the placental selenoenzyme. Journal of Clinical Investigation 96, 2421–2430.CrossRefGoogle ScholarPubMed
Schmidt, C & Beyersmann, D (1999) Transient peaks in zinc and metallothionein levels during differentiation of 3T3-L1 cells. Archives of Biochemistry and Biophysics 364, 91–98.CrossRefGoogle Scholar
Schwarz, K & Foltz, CM (1957) Selenium as an integral part of factor 3 against necrotic dietary liver degeneration. Journal of the American Chemical Society 79, 3292–3293.CrossRefGoogle Scholar
Shen, Q, Chu, FF & Newburger, PE (1993) Sequences in the 3'-untranslated region of the human cellular glutathione peroxidase gene are necessary and sufficient for selenocysteine incorporation at the UGA codon. Journal of Biological Chemistry 268, 11463–11469.CrossRefGoogle ScholarPubMed
Shen, Q, McQuilkin, PA & Newburger, PE (1995) RNA-binding proteins that specifically recognize the selenocysteine insertion sequence of human cellular glutathione peroxidase mRNA. Journal of Biological Chemistry 270, 30448–30452.CrossRefGoogle ScholarPubMed
Shortt, CT, Duthie, GG, Robertson, JD, Morrice, PC, Nicol, F & Arthur, JR (1997) Selenium status in a group of scottish adults. European Journal of Clinical Nutrition 51, 400–404.CrossRefGoogle Scholar
Templeton, DM, Banerjee, D & Cherian, MG (1985) Metallothionein synthesis and localisation in relation to metal storage in rat liver during gestation. Biochemistry and Cell Biology 63, 16–22.CrossRefGoogle ScholarPubMed
Tsujikawa, K, Imai, T, Kakutani, M, Kayamori, Y, Mimura, Y, Otaki, N, Kimura, M, Fukuyama, R & Shimizu, N (1991) Localization of metallothionein in nuclei of growing primary adult rat hepatocytes. FEBS Letters 283, 239–242.CrossRefGoogle Scholar
Tujebajeva, RM, Copeland, PR, Xu, XM, Carlson, BA, Harney, JW, Driscoll, DM, Hatfield, DL & Berry, MJ (2000) Decoding apparatus for eukaryotic selenocysteine insertion. EMBO Reports 1, 158–163.CrossRefGoogle ScholarPubMed
Venepally, P, Reddy, LG & Sani, BC (1996) Analysis of the effects of CRABPI expression on the RA-induced transcription mediated by retinoid receptors. Biochemistry 35, 9974–9982.CrossRefGoogle Scholar
Veyrune, J-L, Campbell, GP, Wiseman, J, Blanchard, J-M & Hesketh, JE (1996) A localisation signal in the 3'untranslated region of c-myc mRNA targets c-myc mRNA and ß-globin reporter sequences to the perinuclear cytoplasm and cytoskeletal- bound polysomes. Journal of Cell Science 109, 1185–1194.CrossRefGoogle Scholar
Villette, S, Arthur, JR, Bermano, G & Hesketh, JE (1998) Thyroid stimulating hormone and selenium supply interact to regulate selenoenzyme gene expression in thyroid cells (FRTL-5) in culture. FEBS Letters 438, 81–84.CrossRefGoogle ScholarPubMed
Villette, S, Kyle, JAM, Brown, KM, Pickard, K, Milne, JS, Nicol, F, Arthur, JR & Hesketh, JE (2002) A novel single nucleotide polymorphism in the 3' untranslated region of human glutathione peroxidase 4 influences lipoxygenase metabolism. Blood cells, Molecules and Disease (In the Press).Google Scholar
Walczak, R, Carbon, P & Krol, A (1998) An essential non-Watson-Crick base pair motif in the 3'UTR to mediate selenoprotein translation. RNA 4, 74–84.Google Scholar
Walczak, R, Westhof, E, Carbon, P & Krol, A (1996) A novel RNA structural motif in the selenocysteine insertion element of eukaryotic selenoprotein mRNAs. RNA 2, 367–369.Google ScholarPubMed
Weiss, SL & Sunde, RA (1998) Cis-acting elements are required for selenium regulation of glutathione peroxidase-1 mRNA levels. RNA 4, 816–827.CrossRefGoogle ScholarPubMed
Wingler, K, Bocher, M, Flohé, L, Kollmus, H & Brigelius-Flohé, R (1999) mRNA stability and selenocysteine insertion sequence efficiency rank gastrointestinal glutathione peroxidase high in the hierarchy of selenoproteins. European Journal of Biochemistry 259, 149–157.CrossRefGoogle ScholarPubMed
Wingler, K, Muller, C & Brigelius-Flohé, R (2000) Stability of gastrointestinal glutathione peroxidase mRNA in selenium deficiency depends on its 3'UTR. Biofactors 12, 1–8.Google Scholar
Wolfrum, C, Borrmann, CM, Borchers, T & Spener, F (2001) Fatty acids and hypolipidemic drugs regulate peroxisome proliferator-activated receptors α and γ-mediated gene expression via liver fatty acid binding protein: A signalling pathway to the nucleus. Proceedings of National Academy of Sciences USA 98, 2323–2328.CrossRefGoogle ScholarPubMed
Woo, ES & Lazo, JS (1997) Nucleocytoplasmic functionality of metallothionein. Cancer Research 57, 4236–4241.Google ScholarPubMed
Wu, R, Shen, Q & Newburger, PE (2000) Recognition and binding of the human selenocysteine insertion sequence by nucleolin. Journal of Cellular Biochemistry 77, 507–516.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Yang, G, Chen, J, Wen, Z, Ge, K & Zhu, L (1984) The role of selenium in Keshan disease. Advances in Nutrition Research 6, 203–231.CrossRefGoogle ScholarPubMed