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PMID: 12505983 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cathepsin A regulates chaperone-mediated autophagy through cleavage of the lysosomal receptor.

The EMBO journal ·Vol. 22 ·No. 1 ·2003-01-02 ·Pages 47-59

Cuervo AM, Mann L, Bonten EJ, d'Azzo A, Dice JF

Abstract

Protective protein/cathepsin A (PPCA) has a serine carboxypeptidase activity of unknown physiological function. We now demonstrate that this protease activity triggers the degradation of the lysosome-associated membrane protein type 2a (lamp2a), a receptor for chaperone-mediated autophagy (CMA). Degradation of lamp2a is important because its level in the lysosomal membrane is a rate-limiting step of CMA. Cells defective in PPCA show reduced rates of lamp2a degradation, higher levels of lamp2a and higher rates of CMA. Restoration of PPCA protease activity increases rates of lamp2a degradation, reduces levels of lysosomal lamp2a and reduces rates of CMA. PPCA associates with lamp2a on the lysosomal membrane and cleaves lamp2a near the boundary between the luminal and transmembrane domains. In addition to the well-studied role of PPCA in targeting and protecting two lysosomal glycosidases, we have defined a role for the proteolytic activity of this multifunctional protein.

MeSH Terms
Amino Acid Sequence Animals Antigens, CD/metabolism Autophagy Bone Marrow Transplantation/physiology Carboxypeptidases/chemistry,metabolism Cathepsin A Cytosol/enzymology Intracellular Membranes/enzymology Kinetics Lysosome-Associated Membrane Glycoproteins Lysosomes/metabolism Male Mice Mice, Inbred C57BL Molecular Chaperones/physiology Molecular Sequence Data Rats Rats, Wistar Serine Endopeptidases/metabolism
Chemicals
Antigens, CD Lysosome-Associated Membrane Glycoproteins Molecular Chaperones Carboxypeptidases Cathepsin A Serine Endopeptidases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Cuervo Ana Maria
Department of Anatomy and Structural Biology, Albert Einstein College of Medicine, Bronx, NY 10461, USA. [email protected]
Mann Linda
Bonten Erik J
d'Azzo Alessandra
Dice J Fred
References (37)
37 references, click to expand
  1. Altered trafficking and turnover of LAMP-1 in Pompe disease-affected cells.
    Mol Genet Metab. 1999 Mar;66(3):179-88 PMID: 10066386
  2. Direct lysosomal uptake of alpha 2-microglobulin contributes to chemically induced nephropathy.
    Kidney Int. 1999 Feb;55(2):529-45 PMID: 9987077
  3. Expression patterns of murine lysosome-associated membrane protein 2 (Lamp-2) transcripts during morphogenesis.
    Differentiation. 1999 Jul;65(1):43-58 PMID: 10448712
  4. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  5. Direct affinity purification and supramolecular organization of human lysosomal cathepsin A.
    Arch Biochem Biophys. 1994 Aug 15;313(1):64-70 PMID: 8053688
  6. Dominant chymotrypsin-like esterase activity in human lymphocyte granules is mediated by the serine carboxypeptidase called cathepsin A-like protective protein.
    J Immunol. 1994 Nov 15;153(10):4663-72 PMID: 7963538
  7. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice.
    Nature. 2000 Aug 24;406(6798):902-6 PMID: 10972293
  8. Age-related decline in chaperone-mediated autophagy.
    J Biol Chem. 2000 Oct 6;275(40):31505-13 PMID: 10806201
  9. Unique properties of lamp2a compared to other lamp2 isoforms.
    J Cell Sci. 2000 Dec;113 Pt 24:4441-50 PMID: 11082038
  10. Regulation of lamp2a levels in the lysosomal membrane.
    Traffic. 2000 Jul;1(7):570-83 PMID: 11208145
  11. The carboxypeptidase nature of cathepsin A.
    Arch Biochem Biophys. 1967 Jul;121(1):241-2 PMID: 5340654
  12. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  13. Prenatal diagnosis of sialidosis with combined neuraminidase and beta-galactosidase deficiency.
    Clin Genet. 1979 Jul;16(1):60-1 PMID: 477017
  14. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  15. Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man.
    Proc Natl Acad Sci U S A. 1982 Aug;79(15):4535-9 PMID: 6812049
  16. A rapid and simplified method for the preparation of lysosomal membranes from rat liver.
    J Biochem. 1983 Feb;93(2):547-56 PMID: 6841352
  17. Regulation of intracellular protein degradation in IMR-90 human diploid fibroblasts.
    J Cell Physiol. 1983 May;115(2):167-74 PMID: 6341382
  18. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins.
    Science. 1989 Oct 20;246(4928):382-5 PMID: 2799391
  19. Mouse "protective protein". cDNA cloning, sequence comparison, and expression.
    J Biol Chem. 1990 Mar 15;265(8):4678-84 PMID: 2106523
  20. Isolation of subcellular organelles.
    Methods Enzymol. 1990;182:203-25 PMID: 2156127
  21. A peptidase in human platelets that deamidates tachykinins. Probable identity with the lysosomal "protective protein".
    J Biol Chem. 1990 Jul 5;265(19):11265-72 PMID: 1694176
  22. Human lysosomal protective protein has cathepsin A-like activity distinct from its protective function.
    J Biol Chem. 1991 Aug 5;266(22):14754-62 PMID: 1907282
  23. Protective protein as an endogenous endothelin degradation enzyme in human tissues.
    J Biol Chem. 1995 Jan 13;270(2):515-8 PMID: 7822272
  24. Lysosomal protective protein/cathepsin A. Role of the "linker" domain in catalytic activation.
    J Biol Chem. 1995 Nov 3;270(44):26441-5 PMID: 7592859
  25. Mouse model for the lysosomal disorder galactosialidosis and correction of the phenotype with overexpressing erythroid precursor cells.
    Genes Dev. 1995 Nov 1;9(21):2623-34 PMID: 7590240
  26. A receptor for the selective uptake and degradation of proteins by lysosomes.
    Science. 1996 Jul 26;273(5274):501-3 PMID: 8662539
  27. The lysosomal compartment as intracellular calcium store in MDCK cells: a possible involvement in InsP3-mediated Ca2+ release.
    Cell Calcium. 1996 Feb;19(2):157-65 PMID: 8689673
  28. FtsH (HflB) is an ATP-dependent protease selectively acting on SecY and some other membrane proteins.
    J Biol Chem. 1996 Dec 6;271(49):31196-201 PMID: 8940120
  29. A protease complex in the Escherichia coli plasma membrane: HflKC (HflA) forms a complex with FtsH (HflB), regulating its proteolytic activity against SecY.
    EMBO J. 1996 Nov 15;15(22):6122-31 PMID: 8947034
  30. Membrane protein secretases.
    Biochem J. 1997 Jan 15;321 ( Pt 2):265-79 PMID: 9020855
  31. A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins.
    J Biol Chem. 1997 Feb 28;272(9):5606-15 PMID: 9038169
  32. An intralysosomal hsp70 is required for a selective pathway of lysosomal protein degradation.
    J Cell Biol. 1997 May 19;137(4):825-34 PMID: 9151685
  33. Degradation of hepatic stearyl CoA delta 9-desaturase.
    Mol Biol Cell. 1997 Nov;8(11):2281-90 PMID: 9362069
  34. Lysosomes, a meeting point of proteins, chaperones, and proteases.
    J Mol Med (Berl). 1998 Jan;76(1):6-12 PMID: 9462863
  35. Transport of human lysosomal neuraminidase to mature lysosomes requires protective protein/cathepsin A.
    EMBO J. 1998 Mar 16;17(6):1588-97 PMID: 9501080
  36. Lack of PPCA expression only partially coincides with lysosomal storage in galactosialidosis mice: indirect evidence for spatial requirement of the catalytic rather than the protective function of PPCA.
    Hum Mol Genet. 1998 Oct;7(11):1787-94 PMID: 9736781
  37. Intracellular transport of acid beta-glucosidase and lysosome-associated membrane proteins is affected in Gaucher's disease (G202R mutation).
    J Pathol. 1999 Aug;188(4):407-14 PMID: 10440752
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2003-01-02
Pages
47-59
Language
English
Region
England
NLM ID
8208664
PMCID
PMC140041
Subset
IM
Grants
NIDDK NIH HHS · DK52025 · United States
NIA NIH HHS · AG00829 · United States
NIDDK NIH HHS · R01 DK052025 · United States
NIA NIH HHS · AG06116 · United States
NIA NIH HHS · R01 AG006116 · United States
NIA NIH HHS · R37 AG006116 · United States
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