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Biotin homeostasis during the cell cycle

Published online by Cambridge University Press:  14 December 2007

Janos Zempleni  and
Donald M Mock
Janos Zempleni
Affiliation:
Department of Nutritional Science & Dietetics, University of Nebraska-Lincoln, 316 Ruth Leverton Hall, Lincoln, NE 68583, USA
Donald M Mock*
Affiliation:
Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences, 4301 W. Markham, Little Rock, AR 72205, USA
*
*Corresponding author: Dr Donald M. Mock, fax +1 501 603 1146, email mockdonaldm@exchange.uams.edu
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Abstract

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Peripheral blood mononuclear cells (PBMC) accumulate biotin by a Na-dependent energy-requiring transporter. This transporter might be the so-called Na-dependent multivitamin transporter, but kinetic observations suggest the existence of a second, more specific, biotin transporter. PBMC respond to proliferation by increased uptake of biotin; the increase is probably mediated by an increased number of transporters on the cell surface. The inferred increase in the biotin transporter synthesis is relatively specific. The increased uptake of biotin into proliferating PBMC is consistent with the hypothesis that these cells have an increased demand for biotin. Indeed, proliferating PBMC increase expression of genes encoding β-methylcrotonyl-CoA carboxylase and propionyl-CoA carboxylase, generating a quantitatively significant increased demand for biotin as a coenzyme in newly-synthesized carboxylases. Moreover, expression of the holocarboxylase synthetase gene increases, consistent with the synthesis of new holocarboxylases. In addition, proliferating PBMC increase both the density of biotinylation of histones and the mass of biotinylated histones per cell, suggesting a potential role for biotin in transcription and replication of DNA.

Keywords

BiotindCell cyclePeripheral blood mononuclear cellsNa-dependent multivitamin transporter
Type
Research Article
Information
Nutrition Research Reviews , Volume 14 , Issue 1 , June 2001 , pp. 45 - 64
Copyright
Copyright © CABI Publishing 2001

References

Ausio, J & van Holde, KE (1986) Histone hyperacetylation: its effect on nucleosome conformation and stability. Biochemistry 25, 1421–1428.CrossRefGoogle ScholarPubMed
Borboni, P, Magnaterra, R, Rabini, RA, Staffolani, R, Porzio, O, Sesti, G, Fusco, A, Mazzanti, L, Lauro, R & Marlier, LNJL (1996) Effect of biotin on glucokinase activity, mRNA expression and insulin release in cultured beta-cells. Acta Diabetologica 33, 154–158.CrossRefGoogle ScholarPubMed
Boulikas, T (1988) At least 60 ADP-ribosylated variant histones are present in nuclei from dimethylsulfate-treated and untreated cells. EMBO Journal 7, 57–67.CrossRefGoogle ScholarPubMed
Boulikas, T, Bastin, B, Boulikas, P & Dupuis, G (1990) Increase in histone poly(ADP-ribosylation) in mitogen-activated lymphoid cells. Experimental Cell Research 187, 77–84.CrossRefGoogle ScholarPubMed
Bowers-Komro, DM & McCormick, DB (1985) Biotin uptake by isolated rat liver hepatocytes. In Biotin, vol. 447, pp. 350–358 [Dakshinamurti, K and Bhagavan, HN editors]. New York: New York Academy of Sciences.Google ScholarPubMed
Chauhan, J & Dakshinamurti, K (1991) Transcriptional regulation of the glucokinase gene by biotin in starved rats. Journal of Biological Chemistry 266, 10035–10038.CrossRefGoogle ScholarPubMed
Collins, JC, Paietta, E, Green, R, Morell, AG & Stockert, RJ (1988) Biotin-dependent expression of the asialoglycoprotein receptor in HepG2. Journal of Biological Chemistry 263, 11280–11283.CrossRefGoogle ScholarPubMed
Cowan, MJ, Wara, DW, Packman, S, Yoshino, M, Sweetman, L & Nyhan, W (1979) Multiple biotin-dependent carboxylase deficiencies associated with defects in T-cell and B-cell immunity. Lancet 2, 115–118.CrossRefGoogle ScholarPubMed
Dakshinamurti, K, Chalifour, LE & Bhullar, RJ (1985) Requirement for biotin and the function of biotin in cells in culture. In Biotin, vol. 447, pp. 38–55 [Dakshinamurti, K and Bhagavan, HN editors]. New York: New York Academy of Sciences.Google ScholarPubMed
Dakshinamurti, K & Chauhan, J (1994) Biotin-binding proteins. In Vitamin Receptors: Vitamins as Ligands in Cell Communication, pp. 200–249 [Dakshinamurti, K editor]. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Dakshinamurti, K & Cheah-Tan, C (1968) Liver glucokinase of the biotin deficient rat. Canadian Journal of Biochemistry 46, 75–80.CrossRefGoogle ScholarPubMed
Dakshinamurti, K & Litvak, S (1970) Biotin and protein synthesis in rat liver. Journal of Biological Chemistry 245, 5600–5605.CrossRefGoogle ScholarPubMed
Freytag, SO & Merton, FU (1983) Regulation of the synthesis and degradation of pyruvate carboxylase in 3T3-L1 cells. Journal of Biological Chemistry 258, 6307–6312.CrossRefGoogle Scholar
Hebbes, TR, Thorne, AW & Crane-Robinson, C (1988) A direct link between core histone acetylation and transcriptionally active chromatin. EMBO Journal 7, 1395–1402.CrossRefGoogle ScholarPubMed
Hohmann, P (1983) Phosphorylation of H1 histones. Molecular and Cellular Biochemistry 57, 81–92.CrossRefGoogle ScholarPubMed
Hymes, J, Fleischhauer, K & Wolf, B (1995 a) Biotinylation of biotinidase following incubation with biocytin. Clinica Chimica Acta 233, 39–45.CrossRefGoogle ScholarPubMed
Hymes, J, Fleischhauer, K & Wolf, B (1995 b) Biotinylation of histones by human serum biotinidase: assessment of biotinyl-transferase activity in sera from normal individuals and children with biotinidase deficiency. Biochemical and Molecular Medicine 56, 76–83.CrossRefGoogle ScholarPubMed
Janeway, CA, Travers, P, Walport, M & Capra, JD (1999) Immuno Biology. London: Garland Publishing/Elsevier.Google Scholar
Johnson, LD & Hadden, JW (1975) Cyclic GMP and lymphocyte proliferation: effects on DNA-dependent RNA polymerase I and II activities. Biochemical and Biophysical Research Communications 66, 1498–1505.CrossRefGoogle ScholarPubMed
Kaye, AM & Sheratzky, D (1969) Methylation of protein (histone) in vitro: enzymic activity from the soluble fraction of rat organs. Biochimica et Biophysica Acta 190, 527–538.CrossRefGoogle ScholarPubMed
Kim, K-H (1997) Regulation of mammalian acetyl-coenzyme A carboxylase. Annual Review of Nutrition 17, 77–99.CrossRefGoogle ScholarPubMed
Knowles, JR (1989) The mechanism of biotin-dependent enzymes. Annual Review of Biochemistry 58, 195–221.CrossRefGoogle ScholarPubMed
Kumar, CK, Yanagawa, N, Ortiz, A & Said, HM (1998) Mechanism and regulation of riboflavin uptake by human renal proximal tubule epithelial cell line HK-2. American Journal of Physiology 274, F104–F110.Google ScholarPubMed
Langan, TA (1970) Phosphorylation of histones in vivo under the control of cyclic AMP and hormones. In Advances in Biochemical Psychopharmacology, pp. 307–323 [Greengard, P and Costa, E editors]. New York: Raven Press.Google Scholar
Lee, DY, Hayes, JJ, Pruss, D & Wolffe, AP (1993) A positive role for histone acetylation in transcription factor access to nucelosomal DNA. Cell 72, 73–84.CrossRefGoogle Scholar
Lernhardt, W (1990) Fatty acid requirement of B lymphocytes activated in vitro. Biochemical and Biophysical Research Communications 166, 879–885.CrossRefGoogle ScholarPubMed
Loos, JA & Roos, D (1973) Changes in the carbohydrate metabolism of mitogenically stimulated human peripheral lymphocytes. III. Stimulation by tuberculin and allogeneic cells. Experimental Cell Research 79, 136–142.CrossRefGoogle Scholar
Maeda, Y, Kawata, S, Inui, Y, Fukuda, K, Igura, T & Matsuzawa, Y (1996) Biotin deficiency decreases ornithine transcarbamylase activity and mRNA in rat liver. Journal of Nutrition 126, 61–66.CrossRefGoogle ScholarPubMed
Majerus, P & Kilburn, E (1969) Acetyl coenzyme A carboxylase. The roles of synthesis and degradation in regulation of enzyme levels in rat liver. Journal of Biological Chemistry 244, 6254–6262.CrossRefGoogle ScholarPubMed
Mock, DM (1996) Biotin. In Present Knowledge in Nutrition, pp. 220–235 [Ziegler, EE and Filer, LJ Jr editors]. Washington, DC: International Life Sciences Institutes – Nutrition Foundation.Google Scholar
Moskowitz, M & Cheng, DKS (1985) Stimulation of growth factor production in cultured cells by biotin. In Biotin, vol. 447 [Dakshinamurti, K and Bhagavan, HN editors]. New York: New York Academy of Sciences.Google ScholarPubMed
Murray, A & Hunt, T (1993) The Cell Cycle. New York: Oxford University Press.Google Scholar
Nakanishi, S & Numa, S (1970) Purification of rat liver acetyl coenzyme A carboxylase and immunochemical studies on its synthesis and degradation. European Journal of Biochemistry 16, 161–173.CrossRefGoogle ScholarPubMed
Nakatani, Y, Kitamura, H, Inayama, Y & Ogawa, N (1994) Pulmonary endodermal tumor resembling fetal lung. American Journal of Surgery and Pathology 18, 637–642.CrossRefGoogle ScholarPubMed
Paik, WK & Kim, S (1969) Enzymatic methylation of histones. Archives of Biochemistry and Biophysics 134, 632–637.CrossRefGoogle ScholarPubMed
Petrelli, F, Coderoni, S, Moretti, P & Paparelli, M (1978) Effect of biotin on phosphorylation, acetylation, methylation of rat liver histones. Molecular Biology Reports 4, 87–92.CrossRefGoogle ScholarPubMed
Petrelli, F, Marsili, G & Moretti, P (1976) RNA, DNA, histones and interactions between histone proteins and DNA in the liver of biotin deficient rats. Biochemistry and Experimental Biology 14, 461–465.Google Scholar
Pispa, J (1965) Animal biotinidase. Annales Medicinae Experimentalis et Biologiae Fenniae 43, 4–39.Google ScholarPubMed
Prasad, PD, Ramamoorthy, S, Leibach, FH & Ganapathy, V (1997) Characterization of a sodium-dependent vitamin transporter mediating the uptake of pantothenate, biotin and lipoate in human placental choriocarcinoma cells. Placenta 18, 527–533.CrossRefGoogle ScholarPubMed
Prasad, PD, Wang, H, Kekuda, R, Fujita, T, Fei, Y-J, Devoe, LD, Leibach, FH & Ganapathy, V (1998) Cloning and functional expression of a cDNA encoding a mammalian sodium-dependent vitamin transporter mediating the uptake of pantothenate, biotin, and lipoate. Journal of Biological Chemistry 273, 7501–7506.CrossRefGoogle ScholarPubMed
Rodriguez-Melendez, R, Perez-Andrade, ME, Diaz, A, Deolarte, A, Camacho-Arroyo, I, Ciceron, I, Ibarra, I & Velazquez, A (1999) Differential effects of biotin deficiency and replenishment on rat liver pyruvate and propionyl-CoA carboxylases and on their mRNAs. Molecular Genetics and Metabolism 66, 16–23.CrossRefGoogle ScholarPubMed
Roos, D, De Boer, JEG & Boom, AJ (1972) Dose-response of lymphocyte carbohydrate metabolism to phytohemagglutinin. Experimental Cell Research 75, 185–190.CrossRefGoogle Scholar
Roos, D & Loos, JA (1973) Changes in the carbohydrate metabolism of mitogenically stimulated human peripheral lymphocytes. II. Relative importance of glycolysis and oxidative phosphorylation on phytohaemagglutinin stimulation. Experimental Cell Research 77, 127–135.CrossRefGoogle ScholarPubMed
Roth, SY & Allis, CD (1992) Chromatin condensation: does histone H1 dephosphorylation play a role? Trends in Biochemical Sciences 17, 93–98.CrossRefGoogle ScholarPubMed
Said, HM, Ma, TY & Kamanna, VS (1994) Uptake of biotin by human hepatoma cell line, Hep G(2): A carrier-mediated process similar to that of normal liver. Journal of Cellular Physiology 161, 483–489.CrossRefGoogle Scholar
Said, HM, Ortiz, A, Ma, TY & McCloud, E (1998) Riboflavin uptake by the human-derived liver cells HepG2: mechanism and regulation. Journal of Cellular Physiology 176, 588–594.3.0.CO;2-W>CrossRefGoogle Scholar
Segel, GB & Lichtman, MA (1981) Amino acid transport in human lymphocytes: distinctions in the enhanced uptake with PHA treatment or amino acid deprivation. Journal of Cellular Physiology 106, 303–306.CrossRefGoogle ScholarPubMed
Shriver, BJ & Allred, JB (1990) Storage forms of biotin in rat liver. FASEB Journal 4, A501 Abstr.Google Scholar
Shriver, BJ, Roman-Shriver, C & Allred, JB (1993) Depletion and repletion of biotinyl enzymes in liver of biotin-deficient rats: Evidence of a biotin storage system. Journal of Nutrition 123, 1140–1149.Google ScholarPubMed
Sommerville, J, Baird, J & Turner, BM (1993) Histone H4 acetylation and transcription in amphibian chromatin. Journal of Cell Biology 120, 277–290.CrossRefGoogle ScholarPubMed
Spence, JT & Koudelka, AP (1984) Effects of biotin upon the intracellular level of cGMP and the activity of glucokinase in cultured rat hepatocytes. Journal of Biological Chemistry 259, 6393–6396.CrossRefGoogle ScholarPubMed
Velazquez, A, Teran, M, Baez, A, Gutierrez, J & Rodriguez, R (1995) Biotin supplementation affects lymphocyte carboxylases and plasma biotin in severe protein-energy malnutrition. American Journal of Clinical Nutrition 61, 385–391.CrossRefGoogle ScholarPubMed
Velazquez, A, Zamudio, S, Baez, A, Murguia-Corral, R, Rangel-Peniche, B & Carrasco, A (1990) Indicators of biotin status: A study of patients on prolonged total parenteral nutrition. European Journal of Clinical Nutrition 44, 11–16.Google ScholarPubMed
Vesely, DL (1982) Biotin enhances guanylate cyclase activity. Science 216, 1329–1330.CrossRefGoogle ScholarPubMed
Vesely, DL, Wormser, HC & Abramson, HN (1984) Biotin analogues activate guanylate cyclase. Molecular and Cellular Biochemistry 60, 109–114.CrossRefGoogle ScholarPubMed
Waithe, WI, Dauphinais, C, Hathaway, P & Hirschhorn, K (1975) Protein synthesis in stimulated lymphocytes. II. Amino acid requirements. Cellular Immunology 17, 323–334.CrossRefGoogle ScholarPubMed
Wang, H, Huang, W, Fei, Y-J, Xia, H, Fang-Yeng, TL, Leibach, FH, Devoe, LD, Ganapathy, V & Prasad, PD (1999) Human placental Na&+-dependent multivitamin transporter. Journal of Biological Chemistry 274, 14875–14883.CrossRefGoogle ScholarPubMed
Weinberg, MD & Utter, MF (1979) Effect of thyroid hormone on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. Journal of Biological Chemistry 254, 9492–9499.CrossRefGoogle ScholarPubMed
Weinberg, MD & Utter, MF (1980) Effect of streptozotocin-induced diabetes mellitus on the turnover of rat liver pyruvate carboxylase and pyruvate dehydrogenase. Biochemical Journal 188, 601–608.CrossRefGoogle ScholarPubMed
Williams, GT, Lau, KMK, Coote, JM & Johnstone, AP (1985) NAD metabolism and mitogen stimulation of human lymphocytes. Experimental Cell Research 160, 419–426.CrossRefGoogle ScholarPubMed
Wolf, B, Heard, GS, McVoy, JRS, & Grier, RE (1985) Biotinidase deficiency. Annals of the New York Academy of Sciences 447, 252–262.CrossRefGoogle ScholarPubMed
Wolffe, A (1998) Chromatin. San Diego, CA: Academic Press.Google ScholarPubMed
Wood, HG & Barden, RE (1977) Biotin enzymes. Annual Review of Biochemistry 46, 385–413.CrossRefGoogle ScholarPubMed
Zempleni, J & Mock, DM (1998) Uptake and metabolism of biotin by human peripheral blood mononuclear cells. American Journal of Physiology 275, C382–C388.CrossRefGoogle ScholarPubMed
Zempleni, J & Mock, DM (1999 a) The efflux of biotin from human peripheral blood mononuclear cells. Journal of Nutritional Biochemistry 10, 105–109.CrossRefGoogle ScholarPubMed
Zempleni, J & Mock, DM (1999 b) Human peripheral blood mononuclear cells: inhibition of biotin transport by reversible competition with pantothenic acid is quantitatively minor. Journal of Nutritional Biochemistry 10, 427–432.CrossRefGoogle ScholarPubMed
Zempleni, J & Mock, DM (1999 c) Mitogen-induced proliferation increases biotin uptake into human peripheral blood mononuclear cells. American Journal of Physiology 276, C1079–C1084.CrossRefGoogle ScholarPubMed
Zempleni, J & Mock, DM (2000 a) Lymphocytes increase biotin uptake during G1 phase of the cell cycle to increase biotinylation of histones. FASEB Journal 14, A243 Abstr.Google Scholar
Zempleni, J & Mock, DM (2000 b) Proliferation of peripheral blood mononuclear cells increases riboflavin influx. Proceedings of the Society for Experimental Biology and Medicine 225, 72–79.Google ScholarPubMed
Zempleni, J & Mock, DM (2000 c) Utilization of biotin in proliferating human lymphocytes. Journal of Nutrition 130, 335S–337S.CrossRefGoogle ScholarPubMed