Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1987 Aug 1;105(2):713–722. doi: 10.1083/jcb.105.2.713

Three-dimensional reconstruction of a peroxisomal reticulum in regenerating rat liver: evidence of interconnections between heterogeneous segments

PMCID: PMC2114753  PMID: 2887576

Abstract

The three-dimensional (3-D) form and the interrelationship of peroxisomes (Po) in the model of regenerating rat liver after partial hepatectomy were studied by computer-assisted 3-D reconstruction of serial ultrathin sections. Po were labeled cytochemically for either catalase, which stains them all uniformly, or for D-amino acid oxidase (DAA-OX), which gives a heterogeneous reaction with lightly and darkly stained PO. In regenerating rat liver, Po exhibit marked pleomorphism with some budding forms and dumbbell-shaped ones. The 3-D reconstruction revealed many single spherical Po measuring 0.15-0.8 micron in diameter. In addition, two to five Po were found interconnected with each other via narrow 30-50-nm hourglass-shaped bridges forming a reticulum. Such aggregates of Po measured 1.5-2.5 microns across. Whereas all segments of this reticulum stained homogeneously for catalase, they exhibited a marked difference in the intensity of the DAA-OX reaction. These observations are consistent with the view of peroxisomal proliferation by budding or fragmentation from preexisting ones. Under such conditions of rapid growth as in regenerating liver, Po may be interconnected forming a reticulum. The interconnections between Po with differing DAA-OX activities suggest that they originate from the same parent organelle.

Full Text

The Full Text of this article is available as a PDF (5.7 MB).

Selected References

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

  1. Alexson S. E., Fujiki Y., Shio H., Lazarow P. B. Partial disassembly of peroxisomes. J Cell Biol. 1985 Jul;101(1):294–304. doi: 10.1083/jcb.101.1.294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Angermüller S., Fahimi H. D. Selective cytochemical localization of peroxidase, cytochrome oxidase and catalase in rat liver with 3,3'-diaminobenzidine. Histochemistry. 1981;71(1):33–44. doi: 10.1007/BF00592568. [DOI] [PubMed] [Google Scholar]
  3. Angermüller S., Fahimi H. D. Ultrastructural cytochemical localization of uricase in peroxisomes of rat liver. J Histochem Cytochem. 1986 Feb;34(2):159–165. doi: 10.1177/34.2.3080517. [DOI] [PubMed] [Google Scholar]
  4. Angermüller S., Leupold C., Zaar K., Fahimi H. D. Electron microscopic cytochemical localization of alpha-hydroxyacid oxidase in rat kidney cortex. Heterogeneous staining of peroxisomes. Histochemistry. 1986;85(5):411–418. doi: 10.1007/BF00982671. [DOI] [PubMed] [Google Scholar]
  5. Arnold G., Liscum L., Holtzman E. Ultrastructural localization of D-amino acid oxidase in microperoxisomes of the rat nervous system. J Histochem Cytochem. 1979 Mar;27(3):735–745. doi: 10.1177/27.3.39097. [DOI] [PubMed] [Google Scholar]
  6. De Duve C. Biochemical studies on the occurrence, biogenesis and life history of mammalian peroxisomes. J Histochem Cytochem. 1973 Nov;21(11):941–948. doi: 10.1177/21.11.941. [DOI] [PubMed] [Google Scholar]
  7. Essner E. Endoplasmic reticulum and the origin of microbodies in fetal mouse liver. Lab Invest. 1967 Jul;17(1):71–87. [PubMed] [Google Scholar]
  8. Fujiki Y., Rachubinski R. A., Lazarow P. B. Synthesis of a major integral membrane polypeptide of rat liver peroxisomes on free polysomes. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7127–7131. doi: 10.1073/pnas.81.22.7127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goldenberg H., Hüttinger M., Böck P., Kramar R. Influence of subtotal hepatectomy on peroxisomes and peroxisomal enzymes of rat liver and isolated liver cell fractions. Histochemistry. 1975 Jul 16;44(1):47–56. doi: 10.1007/BF00490420. [DOI] [PubMed] [Google Scholar]
  10. Goldman B. M., Blobel G. Biogenesis of peroxisomes: intracellular site of synthesis of catalase and uricase. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5066–5070. doi: 10.1073/pnas.75.10.5066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gorgas K. Peroxisomes in sebaceous glands. V. Complex peroxisomes in the mouse preputial gland: serial sectioning and three-dimensional reconstruction studies. Anat Embryol (Berl) 1984;169(3):261–270. doi: 10.1007/BF00315631. [DOI] [PubMed] [Google Scholar]
  12. Gorgas K. Serial section analysis of mouse hepatic peroxisomes. Anat Embryol (Berl) 1985;172(1):21–32. doi: 10.1007/BF00318940. [DOI] [PubMed] [Google Scholar]
  13. Gras H. A 'hidden line' algorithm for 3D-reconstruction from serial sections--an extension of the NEUREC program package for a microcomputer. Comput Programs Biomed. 1984;18(3):217–226. doi: 10.1016/0010-468x(84)90052-7. [DOI] [PubMed] [Google Scholar]
  14. Gras H., Killmann F. NEUREC - a program package for 3D-reconstruction from serial sections using a microcomputer. Comput Programs Biomed. 1983 Aug-Oct;17(1-2):145–155. doi: 10.1016/0010-468x(83)90035-1. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Hashimoto T., Kuwabara T., Usuda N., Nagata T. Purification of membrane polypeptides of rat liver peroxisomes. J Biochem. 1986 Aug;100(2):301–310. doi: 10.1093/oxfordjournals.jbchem.a121716. [DOI] [PubMed] [Google Scholar]
  17. Hruban Z., Rechcigl M., Jr Microbodies and related particles. Morphology, biochemistry, and physiology. Int Rev Cytol. 1969;(Suppl):1–296. [PubMed] [Google Scholar]
  18. Kalicharan D., Hulstaert C. E., Hardonk M. J. Prevention of penetration hindrance in cerium-based glucose-6-phosphatase cytochemistry by freezing tissue in melting nitrogen. Histochemistry. 1985;82(3):287–292. doi: 10.1007/BF00501407. [DOI] [PubMed] [Google Scholar]
  19. Köster A., Heisig M., Heinrich P. C., Just W. W. In vitro synthesis of peroxisomal membrane polypeptides. Biochem Biophys Res Commun. 1986 Jun 13;137(2):626–632. doi: 10.1016/0006-291x(86)91124-1. [DOI] [PubMed] [Google Scholar]
  20. Lazarow P. B., Fujiki Y. Biogenesis of peroxisomes. Annu Rev Cell Biol. 1985;1:489–530. doi: 10.1146/annurev.cb.01.110185.002421. [DOI] [PubMed] [Google Scholar]
  21. Lazarow P. B., Robbi M., Fujiki Y., Wong L. Biogenesis of peroxisomal proteins in vivo and in vitro. Ann N Y Acad Sci. 1982;386:285–300. doi: 10.1111/j.1749-6632.1982.tb21423.x. [DOI] [PubMed] [Google Scholar]
  22. Lazarow P. B., de Duve C. The synthesis and turnover of rat liver peroxisomes. V. Intracellular pathway of catalase synthesis. J Cell Biol. 1973 Nov;59(2 Pt 1):507–524. doi: 10.1083/jcb.59.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Le Hir M., Dubach U. C. The activities of peroxisomal oxidases in periportal and perivenous zones of the rat liver acinus. Histochemistry. 1980;69(1):95–99. doi: 10.1007/BF00508370. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Marsh M., Griffiths G., Dean G. E., Mellman I., Helenius A. Three-dimensional structure of endosomes in BHK-21 cells. Proc Natl Acad Sci U S A. 1986 May;83(9):2899–2903. doi: 10.1073/pnas.83.9.2899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miura S., Mori M., Takiguchi M., Tatibana M., Furuta S., Miyazawa S., Hashimoto T. Biosynthesis and intracellular transport of enzymes of peroxisomal beta-oxidation. J Biol Chem. 1984 May 25;259(10):6397–6402. [PubMed] [Google Scholar]
  27. Novikoff P. M., Novikoff A. B., Quintana N., Davis C. Studies on microperoxisomes. 3. Observations on human and rat hepatocytes. J Histochem Cytochem. 1973 Jun;21(6):540–558. doi: 10.1177/21.6.540. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Rigatuso J. L., Legg P. G., Wood R. L. Microbody formation in regenerating rat liver. J Histochem Cytochem. 1970 Dec;18(12):893–900. doi: 10.1177/18.12.893. [DOI] [PubMed] [Google Scholar]
  30. Stefanini S., Farrace M. G., Argento M. P. Differentiation of liver peroxisomes in the foetal and newborn rat. Cytochemistry of catalase and D-aminoacid oxidase. J Embryol Exp Morphol. 1985 Aug;88:151–163. [PubMed] [Google Scholar]
  31. Stenger R. J., Confer D. B. Hepatocellular ultrastructure during liver regeneration after subtotal hepatectomy. Exp Mol Pathol. 1966 Oct;5(5):455–474. doi: 10.1016/0014-4800(66)90026-8. [DOI] [PubMed] [Google Scholar]
  32. Stäubli W., Schweizer W., Suter J., Weibel E. R. The proliferative response of hepatic peroxidomes of neonatal rats to treatment with SU-13 437 (nafenopin). J Cell Biol. 1977 Sep;74(3):665–689. doi: 10.1083/jcb.74.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Uchiyama Y., Asari A. A morphometric study of the variations in subcellular structures of rat hepatocytes during 24 hours. Cell Tissue Res. 1984;236(2):305–315. doi: 10.1007/BF00214231. [DOI] [PubMed] [Google Scholar]
  34. Usuda N., Yokota S., Hashimoto T., Nagata T. Immunocytochemical localization of D-amino acid oxidase in the central clear matrix of rat kidney peroxisomes. J Histochem Cytochem. 1986 Dec;34(12):1709–1718. doi: 10.1177/34.12.2878022. [DOI] [PubMed] [Google Scholar]
  35. Veenhuis M., Wendelaar Bonga S. E. Cytochemical localization of catalase and several hydrogen peroxide-producing oxidases in the nucleoids and matrix of rat liver peroxisomes. Histochem J. 1979 Sep;11(5):561–572. doi: 10.1007/BF01012539. [DOI] [PubMed] [Google Scholar]
  36. Veenhuis M., van Dijken J. P., Pilon S. A., Harder W. Development of crystalline peroxisomes in methanol-grown cells of the yeast Hansenula polymorpha and its relation to environmental conditions. Arch Microbiol. 1978 May 30;117(2):153–163. doi: 10.1007/BF00402303. [DOI] [PubMed] [Google Scholar]
  37. Wanner G., Theimer R. R. Two types of microbodies in Neurospora crassa. Ann N Y Acad Sci. 1982;386:269–284. doi: 10.1111/j.1749-6632.1982.tb21422.x. [DOI] [PubMed] [Google Scholar]
  38. Wedel F. P., Berger E. R. On the quantitative stereo-morphology of microbodies in rat hepatocytes. J Ultrastruct Res. 1975 May;51(2):153–165. doi: 10.1016/s0022-5320(75)80144-4. [DOI] [PubMed] [Google Scholar]
  39. Zaar K., Angermüller S., Völkl A., Fahimi H. D. Pipecolic acid is oxidized by renal and hepatic peroxisomes. Implications for Zellweger's cerebro-hepato-renal syndrome (CHRS). Exp Cell Res. 1986 May;164(1):267–271. doi: 10.1016/0014-4827(86)90475-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES