Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1973 Nov 1;59(2):507–524. doi: 10.1083/jcb.59.2.507

THE SYNTHESIS AND TURNOVER OF RAT LIVER PEROXISOMES

V. Intracellular Pathway of Catalase Synthesis

Paul B Lazarow 1, Christian de Duve 1
PMCID: PMC2109097  PMID: 4805011

Abstract

The subcellular distribution of the biosynthetic intermediates of catalase was studied in the livers of rats receiving a mixture of [3H]leucine and [14C]δ-aminolevulinic acid by intraportal injection. Postnuclear supernates were fractionated by a one-step gradient centrifugation technique that separates the main subcellular organelles, partly on the basis of size, and partly on the basis of density. Labeled catalase and its biosynthetic intermediates were separated from the gradient fractions by immunoprecipitation, and the distributions of radioactivity were compared with those of marker enzymes. The results show that catalase protein is synthesized outside the peroxisomes, but rapidly appears in these particles, mostly still in the form of the first hemeless biosynthetic intermediate. Addition of heme and completion of the catalase molecule take place within the peroxisomes. During the first 15 min after [3H]leucine administration, more than half of the newly formed first intermediate was recovered in the supernatant fraction, where it was found to exist as an aposubunit of about 60,000 molecular weight.

Full Text

The Full Text of this article is available as a PDF (993.3 KB).

Selected References

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

  1. Baudhuin P., Beaufay H., Rahman-Li Y., Sellinger O. Z., Wattiaux R., Jacques P., De Duve C. Tissue fractionation studies. 17. Intracellular distribution of monoamine oxidase, aspartate aminotransferase, alanine aminotransferase, D-amino acid oxidase and catalase in rat-liver tissue. Biochem J. 1964 Jul;92(1):179–184. doi: 10.1042/bj0920179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beaufay H., Jacques P., Baudhuin P., Sellinger O. Z., Berthet J., De Duve C. Tissue fractionation studies. 18. Resolution of mitochondrial fractions from rat liver into three distinct populations of cytoplasmic particles by means of density equilibration in various gradients. Biochem J. 1964 Jul;92(1):184–205. doi: 10.1042/bj0920184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blobel G., Potter V. R. Distribution of radioactivity between the acid-soluble pool and the pools of RNA in the nuclear, nonsedimethable and ribosome fractions of rat liver after a single injection of lebaled orotic acid. Biochim Biophys Acta. 1968 Aug 23;166(1):48–57. doi: 10.1016/0005-2787(68)90489-9. [DOI] [PubMed] [Google Scholar]
  4. CARO L. G., PALADE G. E. PROTEIN SYNTHESIS, STORAGE, AND DISCHARGE IN THE PANCREATIC EXOCRINE CELL. AN AUTORADIOGRAPHIC STUDY. J Cell Biol. 1964 Mar;20:473–495. doi: 10.1083/jcb.20.3.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CHANCE B. The reactions of catalase in the presence of the notatin system. Biochem J. 1950 Apr;46(4):387–402. doi: 10.1042/bj0460387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DE DUVE C., PRESSMAN B. C., GIANETTO R., WATTIAUX R., APPELMANS F. Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochem J. 1955 Aug;60(4):604–617. doi: 10.1042/bj0600604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Duve C., Baudhuin P. Peroxisomes (microbodies and related particles). Physiol Rev. 1966 Apr;46(2):323–357. doi: 10.1152/physrev.1966.46.2.323. [DOI] [PubMed] [Google Scholar]
  8. Essner E. Endoplasmic reticulum and the origin of microbodies in fetal mouse liver. Lab Invest. 1967 Jul;17(1):71–87. [PubMed] [Google Scholar]
  9. Glaumann H. Studies on the synthesis and transport of albumin in microsomal subfractions from rat liver. Biochim Biophys Acta. 1970 Nov 12;224(1):206–218. doi: 10.1016/0005-2787(70)90634-9. [DOI] [PubMed] [Google Scholar]
  10. HIGASHI T., PETERS T., Jr STUDIES ON RAT LIVER CATALASE. I. COMBINED IMMUNOCHEMICAL AND ENZYMATIC DETERMINATION OF CATALASE IN LIVER CELL FRACTIONS. J Biol Chem. 1963 Dec;238:3945–3951. [PubMed] [Google Scholar]
  11. HIGASHI T., PETERS T., Jr STUDIES ON RAT LIVER CATALASE. II. INCORPORATION OF 14-C-LEUCINE INTO CATALASE OF LIVER CELL FRACTIONS IN VIVO. J Biol Chem. 1963 Dec;238:3952–3954. [PubMed] [Google Scholar]
  12. HRUBAN Z., SWIFT H., WISSLER R. W. Alterations in the fine structure of hepatocytes produced by beta-3-thienylalanine. J Ultrastruct Res. 1963 Apr;8:236–250. doi: 10.1016/s0022-5320(63)90005-4. [DOI] [PubMed] [Google Scholar]
  13. Higashi T., Kudo H., Kashiwagi K. Specific precipitation of catalase-synthesizing ribosomes by anti-catalase antiserum. J Biochem. 1972 Mar;71(3):463–470. [PubMed] [Google Scholar]
  14. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol. 1967 Aug;34(2):577–596. doi: 10.1083/jcb.34.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. II. Transport to condensing vacuoles and zymogen granules. J Cell Biol. 1967 Aug;34(2):597–615. doi: 10.1083/jcb.34.2.597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kashiwagi K., Tobe T., Higashi T. Studies on rat liver catalase. V. Incorporation of 14 C-leucine into catalase by isolated rat liver ribosomes. J Biochem. 1971 Nov;70(5):785–793. doi: 10.1093/oxfordjournals.jbchem.a129696. [DOI] [PubMed] [Google Scholar]
  17. Lazarow P. B., de Duve C. The synthesis and turnover of rat liver of rat liver peroxisomes. IV. Biochemical pathway of catalase synthesis. J Cell Biol. 1973 Nov;59(2 Pt 1):491–506. doi: 10.1083/jcb.59.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Legg P. G., Wood R. L. New observations on microbodies. A cytochemical study on CPIB-treated rat liver. J Cell Biol. 1970 Apr;45(1):118–129. doi: 10.1083/jcb.45.1.118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leighton F., Poole B., Beaufay H., Baudhuin P., Coffey J. W., Fowler S., De Duve C. The large-scale separation of peroxisomes, mitochondria, and lysosomes from the livers of rats injected with triton WR-1339. Improved isolation procedures, automated analysis, biochemical and morphological properties of fractions. J Cell Biol. 1968 May;37(2):482–513. doi: 10.1083/jcb.37.2.482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MINAKAMI S., YONEYAMA Y., YOSHIKAWA H. On the biosynthesis of heme and hemeproteins in liver cell. Biochim Biophys Acta. 1958 May;28(2):447–449. doi: 10.1016/0006-3002(58)90500-6. [DOI] [PubMed] [Google Scholar]
  21. NISHIDA G., LABBE R. F. Heme biosynthesis; on the incorporation of iron into protoporphyrin. Biochim Biophys Acta. 1959 Feb;31(2):519–524. doi: 10.1016/0006-3002(59)90028-9. [DOI] [PubMed] [Google Scholar]
  22. Novikoff A. B., Goldfischer S. Visualization of peroxisomes (microbodies) and mitochondria with diaminobenzidine. J Histochem Cytochem. 1969 Oct;17(10):675–680. doi: 10.1177/17.10.675. [DOI] [PubMed] [Google Scholar]
  23. PETERS T., Jr The biosynthesis of rat serum albumin. II. Intracellular phenomena in the secretion of newly formed albumin. J Biol Chem. 1962 Apr;237:1186–1189. [PubMed] [Google Scholar]
  24. Poole B., Higashi T., De Duve C. The synthesis and turnover of rat liver peroxisomes. 3. The size distribution of peroxisomes and the incorporation of new catalase. J Cell Biol. 1970 May;45(2):408–415. doi: 10.1083/jcb.45.2.408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Reddy J., Svoboda D. Microbodies in experimentally altered cells. 8. Continuities between microbodies and their possible biologic significance. Lab Invest. 1971 Jan;24(1):74–81. [PubMed] [Google Scholar]
  26. Redman C. M. Biosynthesis of serum proteins and ferritin by free and attached ribosomes of rat liver. J Biol Chem. 1969 Aug 25;244(16):4308–4315. [PubMed] [Google Scholar]
  27. Redman C. M., Grab D. J., Irukulla R. The intracellular pathway of newly formed rat liver catalase. Arch Biochem Biophys. 1972 Oct;152(2):496–501. doi: 10.1016/0003-9861(72)90244-5. [DOI] [PubMed] [Google Scholar]
  28. Redman C. M., Siekevitz P., Palade G. E. Synthesis and transfer of amylase in pigeon pancreatic micromosomes. J Biol Chem. 1966 Mar 10;241(5):1150–1158. [PubMed] [Google Scholar]
  29. SANO S., GRANICK S. Mitochondrial coproporphyrinogen oxidase and protoporphyrin formation. J Biol Chem. 1961 Apr;236:1173–1180. [PubMed] [Google Scholar]
  30. SHIBKO S., TAPPEL A. L. DISTRIBUTION OF ESTERASES IN RAT LIVER. Arch Biochem Biophys. 1964 Jul 20;106:259–266. doi: 10.1016/0003-9861(64)90186-9. [DOI] [PubMed] [Google Scholar]
  31. SIEKEVITZ P., PALADE G. E. A cytochemical study on the pancreas of the guinea pig. 5. In vivo incorporation of leucine-1-C14 into the chymotrypsinogen of various cell fractions. J Biophys Biochem Cytol. 1960 Jul;7:619–630. doi: 10.1083/jcb.7.4.619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sund H., Weber K., Mölbert E. Dissoziation der Rinderleber-Katalase in ihre Untereinheiten. Eur J Biochem. 1967 Jun;1(4):400–410. doi: 10.1111/j.1432-1033.1967.tb00088.x. [DOI] [PubMed] [Google Scholar]
  33. Svoboda D. J., Azarnoff D. L. Response of hepatic microbodies to a hypolipidemic agent, ethyl chlorophenoxyisobutyrate (CPIB). J Cell Biol. 1966 Aug;30(2):442–450. doi: 10.1083/jcb.30.2.442. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Svoboda D., Grady H., Azarnoff D. Microbodies in experimentally altered cells. J Cell Biol. 1967 Oct;35(1):127–152. doi: 10.1083/jcb.35.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Takagi M., Tanaka T., Ogata K. Functional differences in protein synthesis between free and bound polysomes of rat liver. Biochim Biophys Acta. 1970 Sep 17;217(1):148–158. doi: 10.1016/0005-2787(70)90131-0. [DOI] [PubMed] [Google Scholar]
  36. Tsukada H., Mochizuki Y., Konishi T. Morphogenesis and development of microbodies of hepatocytes of rats during pre- and postnatal growth. J Cell Biol. 1968 May;37(2):231–243. doi: 10.1083/jcb.37.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Weissmann B. A colorimetric method for alpha-naphthol and its application to assay of hydrolases. Anal Biochem. 1969 Apr 4;28(1):295–299. doi: 10.1016/0003-2697(69)90182-1. [DOI] [PubMed] [Google Scholar]
  38. Wibo M., Amar-Costesec A., Berthet J., Beaufay H. Electron microscope examination of subcellular fractions. 3. Quantitative analysis of the microsomal fraction isolated from rat liver. J Cell Biol. 1971 Oct;51(1):52–71. doi: 10.1083/jcb.51.1.52. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES