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Virchows Archiv B

, Volume 36, Issue 1, pp 219–234 | Cite as

Autophagy, heterophagy, microautophagy and crinophagy as the means for intracellular degradation

  • L. Marzella
  • J. Ahlberg
  • H. Glaumann
Article

Summary

It is generally accepted that the lysosomal compartment plays an important role in the degradation of cellular components.

In this communication we discuss various experimental models which have been used to study mechanisms of intralysosomal degradation and also discuss the evidence obtained in support of the following proposals:
  1. 1.

    The autophagosomes can be isolated into high purity and are the subcellular locus of induced protein degradation.

     
  2. 2.

    Different membrane components such as proteins and lipids are degraded at different rates inside the lysosomes. Intralysosomal hydrolysis is not the rate limiting step in degradation.

     
  3. 3.

    Lysosomes take up soluble material in vitro by invagination and pinching off of their membranes (microautophagy).

     
  4. 4.

    Secretory vesicles can degrade their secretory contents by fusing with the lysosomes.

     

Key words

Lysosomes Autophagosomes Isolation Proteolysis Microautophagy Crinophagy 

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References

  1. Ballard JF (1977) Intracellular protein degradation. In: Campbell PN, Aldridge WN (ed) Essays in biochemistry, 13 Academic Press, London and New York, pp 1–37Google Scholar
  2. Barrett AJ, Heath MF (1977) Lysosomal enzymes. In: Dingle JT (ed) Lysosomes: a laboratory handbook, 2nd ed., Elsevier/North Holland, Biomedical Press, Amsterdam, pp 19–45Google Scholar
  3. Bolender RP, Weibel ER (1973) A morphometric study of the removal of phenobarbital-induced membranes from hepatocytes after cessation of treatment. J Cell Biol 56:746–761PubMedCrossRefGoogle Scholar
  4. Dean RT (1977) Lysosomes and membrane recycling. A Hypothesis Biochem J 168:603–605Google Scholar
  5. Dean RT (1979) Macrophage protein turnover. Evidence for lysosomal participation in basal proteolysis. Biochem J 180:339–345PubMedGoogle Scholar
  6. Debeer LJ, Thomas J, de Schepper PJ, Mannaerts GP (1979) Lysosomal triacylglycerol lipase and lipolysis in isolated rat hepatocytes. J Biol Chem 254:8841–8846PubMedGoogle Scholar
  7. De Duve C, Wattiaux R (1966) Functions of lysosomes. Ann Rev Physiol 28:435–492CrossRefGoogle Scholar
  8. Deter RL, Baudhuin P, de Duve C (1967) Participation of lysosomes in cellular autophagy induced in rat liver by glucagon. J Cell Biol 35:C11-C16PubMedCrossRefGoogle Scholar
  9. Edelson PJ, Cohn ZA (1974) Effects of concanavalin A on mouse peritoneal macrophages. II. Metabolism of endocytosed proteins and reversibility of the effects by mannose. J Exp Med 140:1387–1403PubMedCrossRefGoogle Scholar
  10. Ericsson, JLE (1969) Studies on induced cellular autophagy. I. Electron microscopy of cells with in vivo labelled lysosomes. Exp Cell Res 55:95–105PubMedCrossRefGoogle Scholar
  11. Fowler S, de Duve C (1969) Digestive activity of lysosomes. III. The digestion of lipids by extracts of rat liver lysosomes. J Biol Chem 244:471–481PubMedGoogle Scholar
  12. Garlick PJ, Waterlow JC, Swick RW (1976) Measurement of protein turnover in rat liver. Analysis of the complex curve for decay of label in a mixture of proteins. Biochem J 156:657–663PubMedGoogle Scholar
  13. Glaumann H, Berezesky IK, Ericsson JLE, Trump BF (1975) Lysosomal degradation of cell organelles. I. Ultrastructural analysis of uptake and digestion of intravenously injected mitochondria by Kupffer cells. Lab Invest 33:239–251PubMedGoogle Scholar
  14. Glaumann H, Fredzell J, Jubner A, Ericsson JLE (1979) Uptake and degradation of glycogen by Kupffer cells. Exp Mol Pathol 31:70–80PubMedCrossRefGoogle Scholar
  15. Glaumann H, Marzella L (1981) Degradation of membrane components by Kupffer cell lysosomes. Lab Invest (Accepted for publication)Google Scholar
  16. Glaumann H, Trump BF (1975). Lysosomal degradation of cell organelles. III. Uptake and disappearance in Kupffer cells of intravenously injected isotope-labelled mitochondria and microsomes in vivo and in vitro. Lab. Invest 33:262–272PubMedGoogle Scholar
  17. Halban PA, Wollheim CR (1980) Intracellular degradation of insulin stores by rat pancreatic islets in vitro. An alternative pathway for homeostatis of pancreatic insulin content. J Biol Chem 255:6003–6006PubMedGoogle Scholar
  18. Hamberg H, Brunk U, Ericsson JLE, Jung B (1977) Cytoplasmic effects of X-irradiation on cultured cells in a non-dividing stage. Alterations in lysosomes, plasma membrane, Golgi apparatus and related structures. Acta Path Microbiol Scand Sect A85:625–639Google Scholar
  19. Hirsimäki P, Trump BF, Arstila AU (1976) Studies on vinblastine-induced autophagocytosis in the mouse liver. I. The relation of lysosomal changes to general injurious effects. Virchows Arch [Cell Pathol] 22:89–109Google Scholar
  20. Ingelman-Sundberg M, Glaumann H (1980) Incorporation of purified components of rabbit liver microsomal hydroxylase system into phospholipid vesicles. Biochem Biophys Acta 599:417–435PubMedCrossRefGoogle Scholar
  21. Locke M, Collins JV (1980) Organelle turnover. In: Trump BF, Arstila AU (eds) Pathobiology of cell membranes, vol II. Academic Press, London, p 223Google Scholar
  22. Marzella L, Glaumann H (1980a) Increased degradation in rat liver induced by vinblastine. I. Biochemical characterization. Lab Invest 42:8–17PubMedGoogle Scholar
  23. Marzella L, Glaumann H (1980b) Increased degradation in rat liver induced by vinblastine. II. Morphological characterization. Lab Invest 4Virchows Archiv 42:18–27Google Scholar
  24. Marzella L, Ahlberg J, Glaumann H (1980a) In vitro uptake of particles by lysosomes. Exp Cell Res 129:460–465PubMedCrossRefGoogle Scholar
  25. Marzella L, Sandberg P-O, Glaumann H (1980 b) Autophagic degradation in rat liver after vinblastine treatment. Exp Cell Res 128:291–301PubMedCrossRefGoogle Scholar
  26. Marzella L, Ahlberg J, Glaumann H (1981) Isolation of autophagosomes from rat liver. Morphological and biochemical characterization. J Cell Biol (Accepted for publication)Google Scholar
  27. Mortimore GE, Mondon CE (1970) Inhibition by insulin of valin turnover in liver. Evidence for a general control of proteolysis. J Biol Chem 245:2375–2383PubMedGoogle Scholar
  28. Mortimore GE, Schworer CM (1977) Induction of autophagy by aminoacid deprivation in perfused rat liver. Nature 270:174–176PubMedCrossRefGoogle Scholar
  29. Neely AN, Cox JR, Fortney JA, Schworer CM, Mortimore GE (1977) Alterations of lysosomal size and density during rat liver perfusion. Suppression by insulin and amino acids. J Biol Chem 252:6948–6954PubMedGoogle Scholar
  30. Omura T, Siekevitz P, Palade GE (1967) Turnover of constituents of the endoplasmic reticulum membranes of rat hepatocytes. J Biol Chem 242:2398–2396Google Scholar
  31. Pfeifer U (1970) Über Endocytose in Kupfferschen Sternzellen nach Parenchymschädigung durch 3/4-Teilhepatektomie. Virchows Arch B Zellpath 6:263–280Google Scholar
  32. Pfeifer U, Werder E, Bergeest H (1978) Inhibition by insulin of the formation of autophagic vacuoles in rat liver. A morphometric approach to the kinetics of intracellular degradation by autophagy. J Cell Biol 78:152–167PubMedCrossRefGoogle Scholar
  33. Saito T, Ogawa K (1974) Lysosomal changes in rat hepatic parenchymal cells after glucagon administration. Acta Histochem Cytochem 7:1–18Google Scholar
  34. Scornik OA, Ledbetter MLS, Malter JS (1980) Role of aminoacylation of histidyl-tRNA in the regulation of protein degradation in Chinese hamster ovary cells. J Biol Chem 255:6322–6329PubMedGoogle Scholar
  35. Seglen PO, Grinde B, Solheim AE (1979) Inhibition of the lysosomal pathway of protein degradation in isolated rat hepatocytes by ammonia, methylamine, chloroquine and leupeptin. Eur J Biochem 95:215–225PubMedCrossRefGoogle Scholar
  36. Smith RE, Farquhar MG (1966) Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J Cell Biol 31:319–347CrossRefGoogle Scholar
  37. Wattiaux R, Wattiaux-de Coninck S, Roneveaux-Dupal MF, Dubois F (1978) Isolation of rat liver lysosomes in a metrizamide gradient. J Cell Biol 78:349–364PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • L. Marzella
    • 1
  • J. Ahlberg
    • 1
  • H. Glaumann
    • 1
  1. 1.Department of Pathology, Karolinska InstitutetHuddinge University HospitalHuddingeSweden

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