Abstract
There have been a limited number of studies investigating surfactant lipid changes in lung with trace elements. The present investigation was designed to examine the effect of moderate zinc deficiency on the lipid metabolism in rat lung. We also evaluated whether zinc deficiency, which is a wide-spread problem, could play a role in adult respiratory distress syndrome (ARDS). For that purpose, adult male Wistar rats were fed two diets differing in zinc concentration. The rats were divided into two groups. One group was fed a zinc-deficient diet containing 3 mg Zn/kg, and the other group received a zincadequate control diet with 30 mg Zn/kg according to AIN 93-M. After 2 mon of treatment, we observed that in the zinc-deficient group (i) total lipids, phospholipids, and cholesterol increased whereas TG decreased in whole lung; (ii) phospholipid (PC) concentration increased in lamellar bodies and alveolar macrophages and decreased in extracellular surfactant but did not change in microsomes; (iii) protein concentration decreased in whole lung, extracellular surfactant, lamellar bodies, and macrophages; (iv) the incorporation of [Me-14C]choline into PC (phospholipids) of lung slices increased; and (v) the activity of CTP/phosphocholine cytidylyltransferase bound to the microsomes increased in the lung. These results suggest that the lipid concentration in the lung (especially the phospholipids) is modified directly or indirectly by a zinc-deficient diet. In a zincdeficient diet, the lung changes the pattern of PC for an adaptive or recovery stage. Therefore, zinc deficiency implications are important for the design of therapies and public health interventions involving targeted zinc supplementation for high-risk groups or groups with certain diseases, such as ARDS.
Similar content being viewed by others
Abbreviations
- ARDS:
-
adult respiratory distress syndrome
- Co:
-
control
- CYT:
-
cytidylyltransferase
- LPC:
-
lysophosphatidylcholine
- SPH:
-
sphingomyelin
- ZD:
-
zinc deficiency
References
Hamm, H., Fabel, H., and Bartsch, W. (1992) The Surfactant System of the Adult Lung: Physiology and Clinical Perspectives, Clin. Investig. 70, 637–657.
Notter, M.D. (1989) Physical Chemistry and Physiological Activity of Pulmonary Surfactants, in Surfactant Replacement Therapy (Shapiro, D.L., and Notter, R.H., eds.), A.R. Liss, New York, pp. 19–70.
Eder, K., and Kirchgessner, M. (1994) Levels of Polyunsaturated Fatty Acids in Tissues from Zinc-Deficient Rats Fed a Linseed Oil Diet, Lipids 29, 839–844.
Eder, K., and Kirchgessner, M. (1995) Zinc Deficiency and Activities of Lipogenic and Glycolytic Enzymes in Liver of Rats Fed Coconut Oil or Linseed Oil, Lipids 30, 63–69.
Cornatzer, W.E., Haning, J.A., Wallwork, J.C., and Sandstead, H.H. (1984) Effect of Zinc Deficiency on the Biosynthesis of Phosphatidylcholine in Rat Microsomes, Biol. Trace Elem. Res. 6, 393–401.
Rooney, S.A. (1985) The Surfactant System and Lung Phospholipid Biochemistry, Am. Rev. Respir. Dis. 131, 439–460.
Mason, R.J., and Nellenbogen, J. (1984) Synthesis of Saturated Phosphatidylcholine and Phosphatidylglycerol by Freshly Isolated Rat Alveolar Type II Cells, Biochim. Biophys. Acta 794, 392–402.
Sharma, A., Gonzalez, L.W., and Ballard, P.L. (1993) Hormonal Regulation of Cholinephosphate Cytidylyltransferase in Human Fetal Lung, Biochim. Biophys. Acta 1170, 237–244.
Barr, H.A., Nicholas, T.E., and Power, J.H.T. (1989) Effect of Hypernea on Enzymes of the CDP-Choline Path for Phosphatidylcholine Synthesis in Rat Lung, Lipids 24, 709–714.
Zimmermann, L.J., Hogan, M., Carlson, K.S., Smith, B.T., and Post, M. (1993) Regulation of Phosphatidylcholine Synthesis in Fetal Type II Cells by CTP: Phosphocholine Cytidylyltransferase, Am. J. Physiol. 264 (6Pt), L575-L580.
Vojnik, C., and Hurley, L.S. (1977) Abnormal Prenatal Lung Development Resulting from Maternal Zinc Deficiency in Rats, J. Nutr. 107, 862–872.
Truong-Tran, A.Q., Carter, J., Ruffin, R., and Zalewski, P.D. (2001) New Insights into the Role of Zinc in the Respiratory Epithelium, Immunol. Cell. Biol. 79, 170–177.
Reeves, P.G., Nielsen, F.H., and Fahey, G.C., Jr. (1993) AIN-93 Purified Diets for Laboratory Rodents: Final Report of the American Institute of Nutrition ad hoc Writing Committee on the Reformulation of the AIN-76A Rodent Diet, J. Nutr. 123, 1939–1951.
National Research Council (1985) Guide for the Care and Use of Laboratory Animals, Publication 85-23 (rev.), National Institutes of Health, Bethesda.
Clegg, M.S., Keen, C.L., Lonnerdal, B., and Hurley, L.S. (1981) Influence of Ashing Techniques on the Analysis of Trace Elements in Animal Tissue. I. Wet Ashing, Biol. Trace Elem. Res. 3, 107–115.
Adachi, H., Hayashi, H., Sato, H., Dempo, K., and Akino, T. (1989) Characterization of Phospholipids Accumulated in Pulmonary Surfactant Compartments of Rats’ Intratracheally Exposed to Silica, Biochem. J. 262, 781–786.
Hara, A., and Radin, N.S. (1978) Lipid Extraction of Tissues with a Low-Toxicity Solvent, Anal. Biochem. 90, 420–426.
Rouser, G., Fluster, S., and Yamamoto, A. (1970) Two-Dimensional Thin-Layer Chromatographic Separation of Polar Lipid and Determination of Phospholipids Analysis of Spots, Lipids 5, 494–496.
Abell, L.L., Levy, B.B., Brodie, B.B., and Kendall, F.E. (1952) A Simplified Method for the Estimation of Total Cholesterol in Serum and Demonstration of Its Specificity, J. Biol. Chem. 195, 357–366.
Sardesai, V.M., and Manning, J.A. (1968) Determination of Triglycerides in Plasma and Tissues, Clin. Chem. 14, 156–161.
Kuroki, Y., and Akino, T. (1991) Pulmonary Surfactant Protein A (Sp-A) Specifically Binds Dipalmitoylphosphatidylcholine, J. Biol. Chem. 266, 3068–3073.
Haagsman, H.P., Schuurmans, E.A.J.M., Batenburg, J.J., and van Golde, L.M.G. (1988) Synthesis of Phosphatidylcholines in Ozone-Exposed Alveolar Type II Cells Isolated from Adult Rat Lung: Is Glycerolphosphate Acyltransferase a Rate-Limiting Enzyme? Exp. Lung Res. 14, 1–17.
Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent, J. Biol. Chem. 193, 265–275.
Omura, T., and Takesue, S. (1970) A New Method for Simultaneous Purification of Cytochrome b5 and NADPH-Cytochrome C Reductase from Rat Liver Microsomes, J. Biochem. 67, 249–257.
Hansen, T.L., and Andersen, H. (1983) Succinate Dehydrogenase Activity in Cultured Human Skin Fibroblasts and Amniotic Fluid Cells, A Methodological Study, Histochemistry 78, 211–225.
Avruch, J., and Wallach, D.F.H. (1971) Preparation and Properties of Plasma Membrane and Endoplasmic Reticulum Fragments from Isolated Rat Fat Cells, Biochim. Biophys. Acta 233, 334–347.
Oteiza, P.L., Olin, K.L., Fraga, C.G., and Keen, C.L. (1996) Oxidant Defense Systems in Testes from Zinc-Deficient Rats, Proc. Soc. Exptl. Biol. Med. 213, 85–91.
Chen, M.D., Song, Y.M., and Lin, P.Y. (2000) Zinc Effects on Hyperglycemia and Hypoleptinemia in Streptozotocin-Induced Diabetic Mice, Horm. Metab. Res. 32, 107–109.
Ivandija, V.R.L., Luterotti, S., Dominis-Kramaric, M., and Bozac, R. (1998) Plasma Proteins and Hematological Parameters in Fattening Pigs Fed Different Sources of Dietary Zinc, Acta Vet. Hung. 46, 111–126.
Cunnane, S.C., and Yang, J. (1995) Zinc Deficiency Impairs Whole-Body Accumulation of Polyunsaturates and Increases the Utilization of 1-14C Linoleate for de novo Lipid Synthesis in Pregnant Rats, Can. J. Physiol. Pharmacol. 73, 1246–1252.
Walsh, C.T., Sandstead, H.H., Prasad, A.S., Newberne, P.M., and Fraker, P.J. (1994) Zinc: Health Effects and Research Priorities for the 1990s, Environ. Health Perspect. 102 (Suppl. 2), 5–46.
Pattison, S.E., and Cousins, R.J. (1986) Zinc Uptake and Metabolism by Hepatocytes, Fed. Proc. 45, 2805–2809.
King, J.C. (1990) Assessment of Zinc Status, J. Nutr. 120, 1474–1479.
Shankar, A.H., and Prasad, A.S. (1998) Zinc and Immune Function: The Biological Basis of Altered Resistance to Infection, Am. J. Clin. Nutr. 68 (Suppl.), 447S-463S.
Jhala, U.S., and Baly, D.L. (1991) Zinc Deficiency Results in a Post-Transcriptional Impairment in Insulin Synthesis, FASEB J. 5, A941.
Scott, J.E. (1992) Phosphatidylcholine Synthesis, Secretion and Reutilization During Differentiation of the Surfactant-Producing Type II Alveolar Cell from Fetal Rabbit Lung, Exp. Lung Res. 18, 563–580.
Hass, M.A., and Longmore, W.J. (1980) Regulation of Lung Surfactant Cholesterol Metabolism by Serum Lipoproteins, Lipids 15, 401–406.
Hass, M.A., and Longmore, W.J. (1974) Surfactant Cholesterol Metabolism of the Isolated Perfused Rat Lung, Biochim. Biophys. Acta 573, 166–174.
Michaut, M., Carrasco, M., and Gimenez, M.S. (1992) Effects of Castration on the Incorporation of [3H2O] in Lipids of Male Rat Liver, Horm. Metab. Res. 24, 593–594.
Ojeda, M.S., Gomez, N.N., and Gimenez, M.S. (1997) Androgen Regulation of Lung Lipids in the Male Rat, Lipids 32, 57–62.
Cousins, R.J. (1999) Nutritional Regulation of Gene Expression, Am. J. Med. 106 (1A), 20S-23S.
Fisher, A.B., and Dodia, C. (1994) Regulation of Surfactant Metabolism Degradation of Internalized Alveolar Phosphatidylcholine, Prog. Respir. Res. 27, 74–83.
O’Dell, B.L. (2000) Role of Zinc in Plasma Membrane Function, J. Nutr. 130 (5S Suppl.), 1432S-1436S.
Shiratori, Y., Houweling, M., Zha, X., and Tabas, Y. (1995) Stimulation of CTP-Phosphocholine Cytidylyltransferase by Free Cholesterol Loading of Macrophages Involves Signaling Through Protein Dephosphorylation, J. Biol. Chem. 270, 29894–29903.
Muller, B., and von Wichert, P. (1993) Effect of Nitrogen Dioxide Inhalation on Surfactant Phosphatidylcholine Synthesis in Rat Alveolar Type II Cells, Biochim. Biophys. Acta 1170, 38–43.
Clejan, S., Maddaiah, V.T., Castro-Magana, M., and Collipp, P.J. (1981) Zinc Deficiency-Induced Changes in the Composition of Microsomal Membranes and in the Enzymatic Regulation of Glycerolipid Synthesis, Lipids 16, 454–460.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Gomez, N.N., Ojeda, M.S. & Gimenez, M.S. Lung lipid composition in zinc-deficient rats. Lipids 37, 291–296 (2002). https://doi.org/10.1007/s11745-002-0893-3
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11745-002-0893-3