Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1990 Feb 1;265(3):707–713. doi: 10.1042/bj2650707

Post-translational modification of apolipoprotein B by transglutaminases.

E Cocuzzi 1, M Piacentini 1, S Beninati 1, S I Chung 1
PMCID: PMC1133691  PMID: 1968333

Abstract

The major form of cross-link found in apolipoprotein B was identified as N1N12-bis-(gamma-glutamyl)spermine, a product known to be formed through the catalytic action of transglutaminases (EC 2.3.2.13). N1-(gamma-Glutamyl)spermine was present in a trace amount but epsilon-(gamma-glutamyl)lysine cross-links, which are formed during fibrin formation in plasma, were not detected. In the presence of catalytic amounts of plasma Factor XIIIa (a thrombin-dependent extracellular transglutaminase) or cellular transglutaminase (a cytosolic enzyme), apolipoprotein B and other plasma apolipoproteins (A-I, A-II and C) underwent covalently bridged polymerization and served as amine acceptor substrates. These results suggests that transglutaminases may participate in the covalent modification of apolipoproteins, either in the physiological state or during pathogenesis.

Full text

PDF
707

Images in this article

710Fig. 1.
on p.710
710Fig. 2.
on p.710

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bale M. D., Mosher D. F. Thrombospondin is a substrate for blood coagulation factor XIIIa. Biochemistry. 1986 Sep 23;25(19):5667–5673. doi: 10.1021/bi00367a048. [DOI] [PubMed] [Google Scholar]
  2. Basu S. K., Anderson R. G., Goldstein J. L., Brown M. S. Metabolism of cationized lipoproteins by human fibroblasts. Biochemical and morphologic correlations. J Cell Biol. 1977 Jul;74(1):119–135. doi: 10.1083/jcb.74.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beninati S., Piacentini M., Argento-Cerù M. P., Russo-Caia S., Autuori F. Presence of di- and polyamines covalently bound to protein in rat liver. Biochim Biophys Acta. 1985 Jul 26;841(1):120–126. doi: 10.1016/0304-4165(85)90281-8. [DOI] [PubMed] [Google Scholar]
  4. Beninati S., Piacentini M., Cocuzzi E. T., Autuori F., Folk J. E. Covalent incorporation of polyamines as gamma-glutamyl derivatives into CHO cell protein. Biochim Biophys Acta. 1988 Feb 10;952(3):325–333. doi: 10.1016/0167-4838(88)90134-3. [DOI] [PubMed] [Google Scholar]
  5. Brewer H. B., Jr Current concepts of the molecular structure and metabolism of human apolipoproteins and lipoproteins. Klin Wochenschr. 1981 Sep 15;59(18):1023–1035. doi: 10.1007/BF01747745. [DOI] [PubMed] [Google Scholar]
  6. Brown M. S., Kovanen P. T., Goldstein J. L. Regulation of plasma cholesterol by lipoprotein receptors. Science. 1981 May 8;212(4495):628–635. doi: 10.1126/science.6261329. [DOI] [PubMed] [Google Scholar]
  7. Bungay P. J., Owen R. A., Coutts I. C., Griffin M. A role for transglutaminase in glucose-stimulated insulin release from the pancreatic beta-cell. Biochem J. 1986 Apr 1;235(1):269–278. doi: 10.1042/bj2350269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bungay P. J., Potter J. M., Griffin M. The inhibition of glucose-stimulated insulin secretion by primary amines. A role for transglutaminase in the secretory mechanism. Biochem J. 1984 May 1;219(3):819–827. doi: 10.1042/bj2190819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen S. H., Yang C. Y., Chen P. F., Setzer D., Tanimura M., Li W. H., Gotto A. M., Jr, Chan L. The complete cDNA and amino acid sequence of human apolipoprotein B-100. J Biol Chem. 1986 Oct 5;261(28):12918–12921. [PubMed] [Google Scholar]
  10. Chung S. I. Comparative studies on tissue transglutaminase and factor XIII. Ann N Y Acad Sci. 1972 Dec 8;202:240–255. doi: 10.1111/j.1749-6632.1972.tb16338.x. [DOI] [PubMed] [Google Scholar]
  11. Cocuzzi E., Breckenridge W. C. The biochemistry of epsilon-amino groups of lysine residues from apolipoprotein B of human low density lipoprotein. Atherosclerosis. 1986 Jul;61(1):25–34. doi: 10.1016/0021-9150(86)90110-3. [DOI] [PubMed] [Google Scholar]
  12. Cucuianu M. P., Miloszewski K., Porutiu D., Losowsky M. S. Plasma factor XIII and platelet factor XIII in hyperlipaemia. Thromb Haemost. 1976 Dec 31;36(3):542–550. [PubMed] [Google Scholar]
  13. Cuculanu M. P., Vasile V. V., Popescu T. A., Opincaru A., Crîsnic I., Tapalagå D. Clinical studies concerning factor XIII; with special reference to hyperlipemia. Thromb Diath Haemorrh. 1973 Dec 31;30(3):480–493. [PubMed] [Google Scholar]
  14. Davies P. J., Murtaugh M. P. Transglutaminase and receptor-mediated endocytosis in macrophages and cultured fibroblasts. Mol Cell Biochem. 1984;58(1-2):69–77. doi: 10.1007/BF00240606. [DOI] [PubMed] [Google Scholar]
  15. Delcros J. G., Roch A. M., Thomas V., el Alaoui S., Moulinoux J. P., Quash G. Protein-bound polyamines in the plasma of mice grafted with the Lewis lung carcinoma. FEBS Lett. 1987 Aug 10;220(1):236–242. doi: 10.1016/0014-5793(87)80912-2. [DOI] [PubMed] [Google Scholar]
  16. Fink M. L., Chung S. I., Folk J. E. gamma-Glutamylamine cyclotransferase: specificity toward epsilon-(L-gamma-glutamyl)-L-lysine and related compounds. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4564–4568. doi: 10.1073/pnas.77.8.4564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Folk J. E., Chung S. I. Transglutaminases. Methods Enzymol. 1985;113:358–375. doi: 10.1016/s0076-6879(85)13049-1. [DOI] [PubMed] [Google Scholar]
  18. Folk J. E., Park M. H., Chung S. I., Schrode J., Lester E. P., Cooper H. L. Polyamines as physiological substrates for transglutaminases. J Biol Chem. 1980 Apr 25;255(8):3695–3700. [PubMed] [Google Scholar]
  19. Folk J. E. Transglutaminases. Annu Rev Biochem. 1980;49:517–531. doi: 10.1146/annurev.bi.49.070180.002505. [DOI] [PubMed] [Google Scholar]
  20. Francis R. T., McDonagh J., Mann K. G. Factor V is a substrate for the transamidase factor XIIIa. J Biol Chem. 1986 Jul 25;261(21):9787–9792. [PubMed] [Google Scholar]
  21. Goldstein J. L., Anderson R. G., Buja L. M., Basu S. K., Brown M. S. Overloading human aortic smooth muscle cells with low density lipoprotein-cholesteryl esters reproduces features of atherosclerosis in vitro. J Clin Invest. 1977 Jun;59(6):1196–1202. doi: 10.1172/JCI108744. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Goldstein J. L., Ho Y. K., Basu S. K., Brown M. S. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci U S A. 1979 Jan;76(1):333–337. doi: 10.1073/pnas.76.1.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Griffin M., Wilson J., Lorand L. High-pressure liquid chromatographic procedure for the determination of epsilon-(gamma-glutamyl)lysine in proteins. Anal Biochem. 1982 Aug;124(2):406–413. doi: 10.1016/0003-2697(82)90057-4. [DOI] [PubMed] [Google Scholar]
  24. Hada M., Kaminski M., Bockenstedt P., McDonagh J. Covalent crosslinking of von Willebrand factor to fibrin. Blood. 1986 Jul;68(1):95–101. [PubMed] [Google Scholar]
  25. Hatch F. T. Practical methods for plasma lipoprotein analysis. Adv Lipid Res. 1968;6:1–68. [PubMed] [Google Scholar]
  26. Hoeg J. M., Meng M. S., Ronan R., Fairwell T., Brewer H. B., Jr Human apolipoprotein A-I. Post-translational modification by fatty acid acylation. J Biol Chem. 1986 Mar 25;261(9):3911–3914. [PubMed] [Google Scholar]
  27. Hoff H. F., Heideman C. L., Gotto A. M., Jr, Gaubatz J. W. Apolipoprotein B retention in the grossly normal and atherosclerotic human aorta. Circ Res. 1977 Nov;41(5):684–690. doi: 10.1161/01.res.41.5.684. [DOI] [PubMed] [Google Scholar]
  28. Hoff H. F., Titus J. L., Bajardo R. J., Jackson R. L., Gotto A. M., DeBakey M. E., Lie J. T. Lipoproteins in atherosclerotic lesions. Localization by immunofluorescence of apo-low density lipoproteins in human atherosclerotic arteries from normal and hyperlipoproteinemics. Arch Pathol. 1975 May;99(5):253–258. [PubMed] [Google Scholar]
  29. Hopkins P. N., Williams R. R. A survey of 246 suggested coronary risk factors. Atherosclerosis. 1981 Aug-Sep;40(1):1–52. doi: 10.1016/0021-9150(81)90122-2. [DOI] [PubMed] [Google Scholar]
  30. Jackson R. L., Morrisett J. D., Gotto A. M., Jr Lipoprotein structure and metabolism. Physiol Rev. 1976 Apr;56(2):259–316. doi: 10.1152/physrev.1976.56.2.259. [DOI] [PubMed] [Google Scholar]
  31. Kane J. P. A rapid electrophoretic technique for identification of subunit species of apoproteins in serum lipoproteins. Anal Biochem. 1973 Jun;53(2):350–364. doi: 10.1016/0003-2697(73)90081-x. [DOI] [PubMed] [Google Scholar]
  32. Kane J. P. Apolipoprotein B: structural and metabolic heterogeneity. Annu Rev Physiol. 1983;45:637–650. doi: 10.1146/annurev.ph.45.030183.003225. [DOI] [PubMed] [Google Scholar]
  33. Knott T. J., Pease R. J., Powell L. M., Wallis S. C., Rall S. C., Jr, Innerarity T. L., Blackhart B., Taylor W. H., Marcel Y., Milne R. Complete protein sequence and identification of structural domains of human apolipoprotein B. Nature. 1986 Oct 23;323(6090):734–738. doi: 10.1038/323734a0. [DOI] [PubMed] [Google Scholar]
  34. Kruski A. W., Narayan K. A. A simplified procedure for protein determination of turbid lipoprotein samples. Anal Biochem. 1972 May;47(1):299–302. doi: 10.1016/0003-2697(72)90305-3. [DOI] [PubMed] [Google Scholar]
  35. Law S. W., Gray G., Brewer H. B., Jr cDNA cloning of human apoA-I: amino acid sequence of preproapoA-I. Biochem Biophys Res Commun. 1983 Apr 15;112(1):257–264. doi: 10.1016/0006-291x(83)91824-7. [DOI] [PubMed] [Google Scholar]
  36. Mosher D. F. Action of fibrin-stabilizing factor on cold-insoluble globulin and alpha2-macroglobulin in clotting plasma. J Biol Chem. 1976 Mar 25;251(6):1639–1645. [PubMed] [Google Scholar]
  37. Osborne J. C., Jr, Brewer H. B., Jr The plasma lipoproteins. Adv Protein Chem. 1977;31:253–337. doi: 10.1016/s0065-3233(08)60220-x. [DOI] [PubMed] [Google Scholar]
  38. Piacentini M., Beninati S. gamma-Glutamylamine derivatives in isolated rat hepatocyte proteins. Biochem J. 1988 Feb 1;249(3):813–817. doi: 10.1042/bj2490813. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Piacentini M., Martinet N., Beninati S., Folk J. E. Free and protein-conjugated polyamines in mouse epidermal cells. Effect of high calcium and retinoic acid. J Biol Chem. 1988 Mar 15;263(8):3790–3794. [PubMed] [Google Scholar]
  40. Pittman R. C., Attie A. D., Carew T. E., Steinberg D. Tissue sites of degradation of low density lipoprotein: application of a method for determining the fate of plasma proteins. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5345–5349. doi: 10.1073/pnas.76.10.5345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Sakata Y., Aoki N. Cross-linking of alpha 2-plasmin inhibitor to fibrin by fibrin-stabilizing factor. J Clin Invest. 1980 Feb;65(2):290–297. doi: 10.1172/JCI109671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schrode J., Folk J. E. Transglutaminase-catalyzed cross-linking through diamines and polyamines. J Biol Chem. 1978 Jul 25;253(14):4837–4840. [PubMed] [Google Scholar]
  43. Sharpe C. R., Sidoli A., Shelley C. S., Lucero M. A., Shoulders C. C., Baralle F. E. Human apolipoproteins AI, AII, CII and CIII. cDNA sequences and mRNA abundance. Nucleic Acids Res. 1984 May 11;12(9):3917–3932. doi: 10.1093/nar/12.9.3917. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Small D. M. Cellular mechanisms for lipid deposition in atherosclerosis (first of two parts). N Engl J Med. 1977 Oct 20;297(16):873–877. doi: 10.1056/NEJM197710202971608. [DOI] [PubMed] [Google Scholar]
  45. Sottrup-Jensen L., Stepanik T. M., Kristensen T., Wierzbicki D. M., Jones C. M., Lønblad P. B., Magnusson S., Petersen T. E. Primary structure of human alpha 2-macroglobulin. V. The complete structure. J Biol Chem. 1984 Jul 10;259(13):8318–8327. [PubMed] [Google Scholar]
  46. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES