Skip to main content
Log in

Correlation between fatty acyl composition in neutral and polar lipids and enzyme activities from various tissues of calcium-deficient rats

  • Articles
  • Published:
Lipids

Abstract

In this study we investigated the changes induced by feeding rats a calcium-deficient diet (0.5 g Ca/kg diet) during 65 d after weaning. Phospholipase A2, acyl-Co synthetase and FA Δ9-, Δ6-, and Δ5-desaturase activities were also determined. Calcium deficiency evoked a general alteration in the quality and proportion of the FA chains acylated to neutral and polar lipids from liver, lungs, spleen, brain, kidneys, fat, articular cartilage, erythrocyte ghosts, and plasmas, characterized by an increment of saturated FA and a significant depletion of polyunsaturated acids derived from linoleate and α-linolenate. Several interlipid and lipid/protein relationships were also modified in microsomes from calcium-deprived rats, with a concomitant reduction in the rotational mobility of the probe diphenylhexatriene. Phospholipase A2 and acyl-CoA synthetase activities were also decreased and increased, respectively, in some tissues from calcium-deficient rats, whereas Δ9-, Δ6- and Δ5-desaturases were significantly depressed. We conclude that changes in tissue fatty acyl composition evoked by calcium deprivation are due to alterations in the acylation/deacylation cycles via inhibition of the phospholipase A2. These changes were reflected in the physicochemical properties of the membranes, which in turn inhibits desaturase activities. A possible failure in the transcriptional rate for desaturase-mRNA was also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

18∶3n−6:

γ-linolenic acid

20∶4n−6:

arachidonic acid

CaD:

calcium-deficient

DBI:

double bond index

DPH:

1,6-diphenyl-1,3,5-hexatriene

ED:

elongation-desaturation index

PDIA:

palmitoyl desaturase index activity

S:

sufficient (control)

SDIA:

stearoyl desaturase activity index

References

  1. Marra, C.A., and Alaniz, M.J.T. de (2000) Calcium Deficiency Modifies Polyunsaturated Fatty Acid Metabolism in Growing Rats, Lipids 35, 983–990.

    Article  PubMed  CAS  Google Scholar 

  2. Huang, Y.S., McAdoo, K.R., Mitchell, J., and Horrobin, D.F. (1983) Effects of Calcium Deprivation on n−6 Fatty Acid Metabolism in Growing Rats, Biochem. Med. Metab. Biol. 40, 61–67.

    Article  Google Scholar 

  3. Bierenbaum, M.L., Fleischman, A.I., and Rachelson, R.I. (1972) Long-Term Human Studies on the Lipid Effects of Oral Calcium, Lipids 7, 202–206.

    PubMed  CAS  Google Scholar 

  4. Marra, C.A., and Alaniz, M.J.T. de (1999) Acyl-CoA Synthetase Activity in Liver Microsomes from Calcium-Deficient Rats, Lipids 34, 343–354.

    Article  PubMed  CAS  Google Scholar 

  5. Alto, L., and Dhalla, N.S. (1979) Myocardial Cation Contents During Induction of Calcium Paradox, Am. J. Physiol. 237, H713-H719.

    PubMed  CAS  Google Scholar 

  6. 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.

    PubMed  CAS  Google Scholar 

  7. National Research Council (1985) Guide for the Care and Use of Laboratory Animals, Publication No. 85-23 (rev.), National Institutes of Health, Bethesda, MD.

    Google Scholar 

  8. Marra, C.A., Alaniz, M.J.T. de, and Brenner, R.R. (1986) Modulation of Δ6 and Δ5 Rat Liver Microsomal Desaturase Activities by Dexamethasone-Induced Factor, Biochim. Biophys. Acta 879, 388–393.

    PubMed  CAS  Google Scholar 

  9. Dodge, J.T., Mitchell, C., and Hanahan, D.J. (1963) The Preparation and Chemical Characteristics of Hemoglobin-Free Ghosts of Human Erythrocytes, Arch. Biochem. Biophys. 100, 119–130.

    Article  PubMed  CAS  Google Scholar 

  10. Berlin, E., Bhathera, S.J., Judd, J.T., Nair, P.P., Jones, D.Y., and Tayler, P.R. (1989) Dietary Fat and Hormonal Effects on Erythrocyte Membrane Fluidity and Lipid Composition in Adult Women, Metabolism 8, 790–796.

    Article  Google Scholar 

  11. Marra, C.A., Mangioni, J.O., Tavella, M., Alaniz, M.J.T. de, Ortiz, D., and Sala, C. (1998) Hormonal-Induced Changes on the Lipid Composition and DPH-Fluorescence Anisotropy of Erythrocyte Ghosts from Pre- and Postmenopausal Women, Acta Physiol. Pharmacol. Toxicol. Latinoam. 17, 8–17.

    Google Scholar 

  12. Garda, H.A., Leikin, A.I., and Brenner, R.R. (1992) Determination of Fatty Acid Desaturase Activities by RP-HPLC, An. Asoc. Quim. Argent. 80, 365–371.

    CAS  Google Scholar 

  13. Marra, C.A., and Alaniz, M.J.T. de (1989) Influence of Testosterone Administration on the Biosynthesis of Unsaturated Fatty Acids in Male and Female Rats, Lipids 24, 1014–1019.

    PubMed  CAS  Google Scholar 

  14. Folch, J., Lees, M., and Sloane Stanley, G.A. (1957) A Simple Method for the Isolation and Purification of Total Lipids from Animal Tissues, J. Biol. Chem. 226, 497–509.

    PubMed  CAS  Google Scholar 

  15. Hanahan, D.J., Dittnar, J.C., and Warashima, E. (1957) A Columm Chromatographic Separation of Classes of Phospholipids, J. Biol. Chem. 228, 685–690.

    PubMed  CAS  Google Scholar 

  16. Allain, C.C., Poon, L.S., Chen, C.S.G., Richmond, W., and Fu, P.C. (1974) Enzymatic Determination of Total Serum Cholesterol, Clin. Chem. 20, 470–475.

    PubMed  CAS  Google Scholar 

  17. Marra, C.A., and Alaniz, M.J.T. de (1990) Mineralocorticoids Modify Rat Liver Δ6 Desaturase Activity and Other Parameters of Lipid Metabolism, Biochem. Int. 22, 483–493.

    PubMed  CAS  Google Scholar 

  18. Chen, P.S., Toribara, T.Y., and Warner, H. (1956) Microdetermination of Phosphorus, Anal. Chem. 33, 1405–1406.

    Google Scholar 

  19. Hirata, F., Schiffmann, E., Venkatasubramanian, K., Salomon, D., and Exelrod, J. (1980) A Phospholipase A2 Inhibitory Protein in Rabbit Neutrophile Induced by Glucocorticoids, Proc. Natl. Acad. Sci. USA 77, 2533–2536.

    Article  PubMed  CAS  Google Scholar 

  20. Irazú, C.E., Gonzáles-Rodríguez, S., and Brenner, R.R. (1993) Δ5 Desaturase Activity in Rat Kidney Microsomes, Mol. Cell. Biochem. 129, 31–37.

    Article  PubMed  Google Scholar 

  21. López Jiménez, J., Bordón, A., Hrelia, S., Rossi, C.A., Turchetto, E., Zamora Navarro, S., and Biagi, P.L. (1993) Evidence for a Detectable Δ6-Desaturase Activity in Rat Heart Microsomes: Aging Influence on Enzyme Activity, Biochem. Biophys. Res. Comm. 192, 1037–1041.

    Article  PubMed  Google Scholar 

  22. Tanaka, T., Hosaka, K., Hoshimaru, M., and Numa, S. (1979) Purification and Properties of Long-Chain Acyl-Coenzyme-A Synthetase from Rat Liver, Eur. J. Biochem. 98, 165–172.

    Article  PubMed  CAS  Google Scholar 

  23. Sambrook, J., Fritsch, E., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, New York.

    Google Scholar 

  24. Lowry, O.H., Rosebrough, M.J., Farr, A.J., and Randall, R.J. (1951) Protein Measurement with the Folin Phenol Reagent, J. Biol. Chem. 193, 275–295.

    Google Scholar 

  25. Shinitzky, M., and Barenholz, Y. (1974) Dynamics of the Hydrocarbon Layer in Liposomes of Lecithin and Sphingomyelin Containing Diacetylphosphate, J. Biol. Chem. 249, 2652–2657.

    PubMed  CAS  Google Scholar 

  26. Shinitzky, M., and Barenholz, Y. (1978) Fluidity Parameters of Lipid Regions Determined by Fluorescence, Biochim. Biophys. Acta 515, 367–394.

    PubMed  CAS  Google Scholar 

  27. Xu, H., Watkins, B.A., and Adkisson, H. (1994) Dietary Lipids Modify the Fatty Acid Composition of Cartilage, Isolated Chondrocytes and Matrix Vesicles, Lipids 29, 619–625.

    PubMed  CAS  Google Scholar 

  28. Cleland, K.A., James, M.J., Neumann, M.A., Gibson, R.A., and Cleland, L.G. (1995) Differences in Fatty Acid Composition of Immature and Mature Articular Cartilage in Humans and Sheep, Lipids 30, 949–953.

    PubMed  CAS  Google Scholar 

  29. Martínez, M., and Ballabriga, A. (1987) Effect of Parenteral Nutrition with High Doses of Linoleate on the Developing Human Liver and Brain, Lipids 22, 133–138.

    PubMed  Google Scholar 

  30. Lepage, G., Levy, E., Ronco, N., Galeano, N., and Roy, C. (1989) Direct Transesterification of Plasma Fatty Acids for Diagnosis of Essential Fatty Acid Deficiency in Gastric Fibrosis, J. Lipid Res. 30, 1483–1490.

    PubMed  CAS  Google Scholar 

  31. Brenner, R.R. (1981) Nutritional and Hormonal Factors Influencing Desaturation of Essential Fatty Acids, Prog. Lipid Res. 20, 41–48.

    Article  PubMed  CAS  Google Scholar 

  32. Brenner, R.R. (1987) Polyunsaturated Fatty Acid Metabolism and Its Regulation, in Recent Advances in Essential Fatty Acid Research (Das, V.N., ed.), Vol. I, pp. 5–18, Academic Publication, Gandhinagar, India.

    Google Scholar 

  33. Marra, C.A., and Alaniz, M.J.T. de (1997) Role of Calcium Ionophore and Phospholipase A2 Inhibitors on the Fatty Acid Composition of Hepatoma Tissue Culture Cells and Lipid Secretion, Med. Sci. Res. 25, 59–62.

    CAS  Google Scholar 

  34. Garg, M.L., Keelan, M., Thomson, A.B.R., and Clandinin, M.T. (1992) Desaturation of Linoleic Acid in the Small Bowel Is Increased by Short-Term Fasting and by Dietary Content of Linoleic Acid, Biochim. Biophys. Acta 1126, 17–25.

    PubMed  CAS  Google Scholar 

  35. De Antueno, R.J., Cantrill, R.C., Huang, Y.S., Elliot, M., and Horrobin, D.F. (1993) Relationship Between Mouse Liver Δ9 Desaturase Activity and Plasma Lipids, Lipids 28, 285–290.

    PubMed  Google Scholar 

  36. Alaniz, M.J.T. de, and Marra, C.A. (1994) Role of Δ9 Desaturase Activity in the Maintenance of High Levels of Monoenoic Fatty Acids in Hepatoma Cultured Cells, Mol. Cell. Biochem. 137, 85–90.

    Article  PubMed  Google Scholar 

  37. Marín, M.C., De Tomás, M.E., Serres, C., and Mercuri, O. (1995) Protein-Energy Malnutrition During Gestation and Lactation in Rats Affects Growth Rate, Brain Development, and Essential Fatty Acid Metabolism, J. Nutr. 125, 1017–1024.

    PubMed  Google Scholar 

  38. Marín, M.C., and Alaniz, M.J.T. de (1998) Relationship Between Dietary Oil During Gestation and Lactation and Biosynthesis of Polyunsaturated Fatty Acids in Control and in Malnourished Dam and Pup Rats, J. Nutr. Biochem. 9, 388–395.

    Article  Google Scholar 

  39. Brenner, R.R. (1981) Nutritional and Hormonal Factors Influencing Desaturation of Essential Fatty Acids, Prog. Lipid Res. 20, 41–48.

    Article  PubMed  CAS  Google Scholar 

  40. Sprecher, H. (1983) The Mechanism of Fatty Acid Chain Elongation and Desaturation in Animals, in High and Low Erucic Acid Rapeseed Oil (Kramer, J.D.G., Souer, F.D., and Pidgen, W.J., eds.), pp. 385–411, Academic Press, New York.

    Google Scholar 

  41. Brenner, R.R., Garda, H., Leikin, A.I., and Pezzano, H. (1980) Effect of Temperature on the Structure of Rat Liver Microsomes Studied by Electron Spin Resonance, Fluorescence and Activity of Enzymes Involved in Fatty Acid Biosynthesis, Acta Physiol. Latinoam. 30, 225–238.

    CAS  Google Scholar 

  42. Garda, H., and Brenner, R.R. (1982) Effect of Induced Phase Transitions on the Glucose-6-phosphate Activity and Electron Transport of Rat Liver Microsomes, Acta Physiol. Latinoam. 32, 31–52.

    CAS  Google Scholar 

  43. Virtanen, J.A., Ruonala, M., Vauhkonen, M., and Sonerharju, P. (1995) Lateral Organization of Liquid-Crystalline Cholesterol-dimyristoylphosphatidylcholine Bilayers. Evidence for Domains with Hexagonal and Centered Rectangular Cholesterol Superlattices, Biochemistry 34, 11568–11581.

    Article  PubMed  CAS  Google Scholar 

  44. Rietveld, A., and Simons, K. (1998) The Differential Miscibility of Lipids as the Basis for the Formation of Functional Membrane Rafts, Biochim. Biophys. Acta 1376, 467–479.

    PubMed  CAS  Google Scholar 

  45. Nagle, J.F., and Nagle, S.T. (2000) Structure of Lipid Bilayers, Biochim. Biophys. Acta 1469, 159–195.

    PubMed  CAS  Google Scholar 

  46. Mandon, E.C., Gómez Dumm, I.N.T. de, and Brenner, R.R. (1986) Effect of Dietary Columbinic Acid on the Fatty Acid Composition and Physical Membrane Properties of Different Tissues of EFA-Deficient Rats, Arch. Latinoam. Nutr. 36, 401–414.

    PubMed  CAS  Google Scholar 

  47. Soulages, J.L., and Brenner, R.R. (1989) Interactions Among Phospholipids of Guinea Pig Rough Microsomes, Effect of Fat Deficiency, Mol. Cell. Biochem. 90, 127–136.

    Article  PubMed  CAS  Google Scholar 

  48. Garda, H.A., and Brenner, R.R. (1984) Short-Chain Aliphatic Alcohols Increase Rat-Liver Microsomal Membrane Fluidity and Affect the Activities of Some Microsomal Membrane-Bound Enzymes, Biochim. Biophys. Acta 769, 160–170.

    Article  PubMed  CAS  Google Scholar 

  49. Garda, H.A., and Brenner, R.R. (1985) In vitro Modification of Cholesterol Content of Rat Liver Microsomes. Effects upon Membrane “Fluidity” and Activities of Glucose-6-phosphatase and Fatty Acid Desaturation Systems, Biochim. Biophys. Acta 819, 45–54.

    Article  PubMed  CAS  Google Scholar 

  50. Leikin, A.I., and Brenner, R.R. (1987) Cholesterol-Induced Microsomal Changes Modulate Desaturase Activities, Biochim. Biophys. Acta 922, 294–303.

    PubMed  CAS  Google Scholar 

  51. Garg, M.L., Wierzbicki, A.A., Thomson, A.B.R., and Clandinin, M.T. (1988) Dietary Cholesterol and/or n−3 Fatty Acid Modulate Δ9-Desaturase Activity in Rat Liver Microsomes, Biochim. Biophys. Acta 962, 330–336.

    PubMed  CAS  Google Scholar 

  52. Brenner, R.R. (1984) Effect of Unsaturated Acids on Membrane Structure and Enzyme Kinetics, Prog. Lipid Res. 23, 69–96.

    Article  PubMed  CAS  Google Scholar 

  53. Kan, H., Ruan, Y., and Malik, K.U. (1996) Involvement of Mitogen-Activated Protein Kinase and Translocation of Cytosolic Phospholipase A2 to the Nuclear Envelope in Acetylcholine-Induced Prostacyclin Synthesis in Rabbit Coronary Endothelial Cells, Mol. Pharmacol. 50, 1139–1147.

    PubMed  CAS  Google Scholar 

  54. Xing, M., and Insel, P.A. (1996) Protein Kinase C-Dependent Activation of Cytosolic Phospholipase A2 and Mitogen-Activated Protein Kinase by Alpha 1-Adrenergic Receptors in Madin-Darby Canine Kidney Cells, J. Clin. Invest. 97, 1302–1310.

    Article  PubMed  CAS  Google Scholar 

  55. Landschulz, K.T., Jump, D.B., MacDougald, O.A., and Lane, M.D. (1994) Transcriptional Control of the Stearoyl-CoA Desaturase-1 Gene by Polyunsaturated Fatty Acids, Biochem. Biophys. Res. Commun. 200, 763–768.

    Article  PubMed  CAS  Google Scholar 

  56. Kruger, M.C., and Horrobin, D.F. (1997) Calcium Metabolism, Osteoporosis, and Essential Fatty Acids: A Review, Prog. Lipid Res. 36, 131–151.

    Article  PubMed  CAS  Google Scholar 

  57. Alisio, A., Canas, F., De Bronia, D.H., Pereira, R., and Tolosa de Talamoni, N. (1997) Effect of Vitamin D Deficiency on Lipid Composition and Calcium Transport in Basolateral Membrane Vesicles from Chick Intestine, Biochem. Mol. Biol. Int. 42, 339–347.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlos A. Marra.

About this article

Cite this article

Marra, C.A., Rimoldi, O. & de Alaniz, M.J.T. Correlation between fatty acyl composition in neutral and polar lipids and enzyme activities from various tissues of calcium-deficient rats. Lipids 37, 701–714 (2002). https://doi.org/10.1007/s11745-002-0952-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-002-0952-9

Keywords

Navigation