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PMID: 11463349 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Constitutive shedding of the amyloid precursor protein ectodomain is up-regulated by tumour necrosis factor-alpha converting enzyme.

The Biochemical journal ·Vol. 357 ·No. Pt 3 ·2001-08-01 ·Pages 787-94

Slack BE, Ma LK, Seah CC

Abstract

The amyloid precursor protein (APP) of Alzheimer's disease is a transmembrane protein that is cleaved within its extracellular domain, liberating a soluble N-terminal fragment (sAPP alpha). Putative mediators of this process include three members of the ADAM (a disintegrin and metalloprotease) family, ADAM9, ADAM10 and ADAM17/TACE (tumour necrosis factor-alpha converting enzyme). Tumour necrosis factor-alpha protease inhibitor (TAPI-1), an inhibitor of ADAMs, reduced constitutive and muscarinic receptor-stimulated sAPP alpha release in HEK-293 cells stably expressing M3 muscarinic receptors. However, the former was less sensitive to TAPI-1 (IC(50)=8.09 microM) than the latter (IC(50)=3.61 microM), suggesting that these processes may be mediated by different metalloproteases. Constitutive sAPP alpha release was increased several-fold in cells transiently transfected with TACE, and this increase was proportional to TACE expression. In contrast, muscarinic-receptor-activated sAPP alpha release was not altered in TACE transfectants. TACE-dependent constitutive release of co-transfected APP(695) was inhibited by TAPI-1 with an IC(50) of 0.92 microm, a value significantly lower than the IC(50)s for inhibition of either constitutive or receptor-regulated sAPP alpha shedding mediated by endogenous secretases. The results indicate that TACE is capable of catalysing constitutive alpha-secretory cleavage of APP, but it is likely that additional members of the ADAM family mediate endogenous constitutive and receptor-coupled release of sAPP alpha in HEK-293 cells.

MeSH Terms
ADAM Proteins ADAM17 Protein Amyloid Precursor Protein Secretases Amyloid beta-Protein Precursor/chemistry,metabolism Aspartic Acid Endopeptidases Cells, Cultured Dipeptides/pharmacology Endopeptidases/metabolism Humans Hydroxamic Acids/pharmacology Metalloendopeptidases/antagonists & inhibitors,genetics,metabolism Protease Inhibitors/pharmacology Protein Structure, Tertiary Receptor, Muscarinic M3 Receptors, Muscarinic/genetics,metabolism Transfection
Chemicals
Amyloid beta-Protein Precursor Dipeptides Hydroxamic Acids N-((2-(hydroxyaminocarbonyl)methyl)-4-methylpentanoyl)-3-(2'-naphthyl)alanylalanine, 2-aminoethylamide Protease Inhibitors Receptor, Muscarinic M3 Receptors, Muscarinic Amyloid Precursor Protein Secretases Endopeptidases Aspartic Acid Endopeptidases BACE1 protein, human ADAM Proteins Metalloendopeptidases ADAM17 Protein ADAM17 protein, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Slack B E
Department of Pathology and Laboratory Medicine, Boston University School of Medicine, 85 East Newton Street, Rm. M1007, Boston, MA 02118, USA. bslack@bu.edu
Ma L K
Seah C C
References (57)
57 references, click to expand
  1. Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors.
    Science. 1992 Oct 9;258(5080):304-7 PMID: 1411529
  2. Tyrosine phosphorylation and proteolysis. Pervanadate-induced, metalloprotease-dependent cleavage of the ErbB-4 receptor and amphiregulin.
    J Biol Chem. 1998 Aug 7;273(32):20589-95 PMID: 9685416
  3. Non-amyloidogenic cleavage of the beta-amyloid precursor protein by an integral membrane metalloendopeptidase.
    J Biol Chem. 1994 Jan 28;269(4):3111-6 PMID: 8300647
  4. Protection against a lethal dose of endotoxin by an inhibitor of tumour necrosis factor processing.
    Nature. 1994 Jul 21;370(6486):218-20 PMID: 8028669
  5. Transforming growth factor-alpha and beta-amyloid precursor protein share a secretory mechanism.
    J Cell Biol. 1995 Feb;128(3):433-41 PMID: 7844156
  6. Synaptotrophic effects of human amyloid beta protein precursors in the cortex of transgenic mice.
    Brain Res. 1994 Dec 15;666(2):151-67 PMID: 7882025
  7. Cell-surface beta-amyloid precursor protein stimulates neurite outgrowth of hippocampal neurons in an isoform-dependent manner.
    J Neurosci. 1995 Mar;15(3 Pt 2):2157-67 PMID: 7891158
  8. Proprotein convertase activity contributes to the processing of the Alzheimer's beta-amyloid precursor protein in human cells: evidence for a role of the prohormone convertase PC7 in the constitutive alpha-secretase pathway.
    J Neurochem. 1999 Nov;73(5):2056-62 PMID: 10537065
  9. Ectodomain shedding of TGF-alpha and other transmembrane proteins is induced by receptor tyrosine kinase activation and MAP kinase signaling cascades.
    EMBO J. 1999 Dec 15;18(24):6962-72 PMID: 10601018
  10. Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-golgi network.
    J Biol Chem. 2000 Jan 28;275(4):2568-75 PMID: 10644715
  11. The ADAM gene family: surface proteins with adhesion and protease activity.
    Trends Genet. 2000 Feb;16(2):83-7 PMID: 10652535
  12. Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase.
    J Cell Biol. 2000 Feb 21;148(4):811-24 PMID: 10684261
  13. Altered cell-matrix associated ADAM proteins in Alzheimer disease.
    J Neurosci Res. 2000 Mar 1;59(5):680-4 PMID: 10686596
  14. Intracellular maturation and localization of the tumour necrosis factor alpha convertase (TACE).
    Biochem J. 2000 Apr 1;347 Pt 1:131-8 PMID: 10727411
  15. Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme.
    J Biol Chem. 2000 May 12;275(19):14608-14 PMID: 10799547
  16. The role of proteolysis in Alzheimer's disease.
    Adv Exp Med Biol. 2000;477:379-90 PMID: 10849764
  17. Metalloprotease-disintegrin (ADAM) genes are widely and differentially expressed in the adult CNS.
    Mol Cell Neurosci. 2000 Jun;15(6):547-60 PMID: 10860581
  18. Regulation of APP cleavage by alpha-, beta- and gamma-secretases.
    FEBS Lett. 2000 Oct 13;483(1):6-10 PMID: 11033346
  19. Coordinated expression of beta-amyloid precursor protein and the putative beta-secretase BACE and alpha-secretase ADAM10 in mouse and human brain.
    J Neurochem. 2000 Nov;75(5):2133-43 PMID: 11032903
  20. Pro-tumor necrosis factor-alpha processing activity is tightly controlled by a component that does not affect notch processing.
    J Biol Chem. 1998 Sep 18;273(38):24955-62 PMID: 9733803
  21. Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor.
    J Biol Chem. 1998 Oct 23;273(43):27765-7 PMID: 9774383
  22. ADAMs: focus on the protease domain.
    Curr Opin Cell Biol. 1998 Oct;10(5):654-9 PMID: 9818177
  23. The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease.
    Trends Cell Biol. 1998 Nov;8(11):447-53 PMID: 9854312
  24. A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCdelta are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor.
    EMBO J. 1998 Dec 15;17(24):7260-72 PMID: 9857183
  25. Processing of the notch ligand delta by the metalloprotease Kuzbanian.
    Science. 1999 Jan 1;283(5398):91-4 PMID: 9872749
  26. Metalloprotease-disintegrin MDC9: intracellular maturation and catalytic activity.
    J Biol Chem. 1999 Feb 5;274(6):3531-40 PMID: 9920899
  27. Regulation of amyloid precursor protein cleavage.
    J Neurochem. 1999 Feb;72(2):443-60 PMID: 9930716
  28. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):3922-7 PMID: 10097139
  29. Notch signaling: cell fate control and signal integration in development.
    Science. 1999 Apr 30;284(5415):770-6 PMID: 10221902
  30. Evidence for a role of a tumor necrosis factor-alpha (TNF-alpha)-converting enzyme-like protease in shedding of TRANCE, a TNF family member involved in osteoclastogenesis and dendritic cell survival.
    J Biol Chem. 1999 May 7;274(19):13613-8 PMID: 10224132
  31. Activity of alpha-secretase as the common final effector of protein kinase C-dependent and -independent modulation of amyloid precursor protein metabolism.
    J Neurochem. 1999 Jun;72(6):2464-70 PMID: 10349856
  32. Rationalizing a pharmacological intervention on the amyloid precursor protein metabolism.
    Trends Pharmacol Sci. 1999 Oct;20(10):418-23 PMID: 10498955
  33. Membrane-anchored metalloprotease MDC9 has an alpha-secretase activity responsible for processing the amyloid precursor protein.
    Biochem J. 1999 Oct 15;343 Pt 2:371-5 PMID: 10510302
  34. Specific sequence elements are required for the expression of functional tumor necrosis factor-alpha-converting enzyme (TACE).
    J Biol Chem. 1999 Oct 22;274(43):30563-70 PMID: 10521439
  35. Metalloprotease-disintegrins: modular proteins capable of promoting cell-cell interactions and triggering signals by protein-ectodomain shedding.
    J Cell Sci. 1999 Nov;112 ( Pt 21):3603-17 PMID: 10523497
  36. Protein kinase C regulation of intracellular and cell surface amyloid precursor protein (APP) cleavage in CHO695 cells.
    Biochemistry. 2000 Dec 12;39(49):15282-90 PMID: 11106509
  37. Constitutive alpha-secretase cleavage of the beta-amyloid precursor protein in the furin-deficient LoVo cell line: involvement of the pro-hormone convertase 7 and the disintegrin metalloprotease ADAM10.
    J Neurochem. 2001 Mar;76(5):1532-9 PMID: 11238737
  38. Cleavage of the membrane precursor for transforming growth factor alpha is a regulated process.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1726-30 PMID: 2000380
  39. Multiple signals activate cleavage of the membrane transforming growth factor-alpha precursor.
    J Biol Chem. 1991 Mar 25;266(9):5769-73 PMID: 2005114
  40. Membrane proteins with soluble counterparts: role of proteolysis in the release of transmembrane proteins.
    Biochemistry. 1991 Oct 22;30(42):10065-74 PMID: 1931937
  41. Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors.
    J Biol Chem. 1996 May 10;271(19):11376-82 PMID: 8626692
  42. Shedding of the lymphocyte L-selectin adhesion molecule is inhibited by a hydroxamic acid-based protease inhibitor. Identification with an L-selectin-alkaline phosphatase reporter.
    J Biol Chem. 1996 Mar 22;271(12):7019-24 PMID: 8636132
  43. Molecular cloning of MADM: a catalytically active mammalian disintegrin-metalloprotease expressed in various cell types.
    Biochem J. 1996 Jul 1;317 ( Pt 1):45-50 PMID: 8694785
  44. Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation.
    J Biol Chem. 1996 Aug 2;271(31):18989-95 PMID: 8702564
  45. Pervanadate activation of intracellular kinases leads to tyrosine phosphorylation and shedding of syndecan-1.
    Biochem J. 1996 Oct 1;319 ( Pt 1):39-47 PMID: 8870647
  46. Membrane protein secretases.
    Biochem J. 1997 Jan 15;321 ( Pt 2):265-79 PMID: 9020855
  47. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells.
    Nature. 1997 Feb 20;385(6618):729-33 PMID: 9034190
  48. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha.
    Nature. 1997 Feb 20;385(6618):733-6 PMID: 9034191
  49. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation.
    J Biol Chem. 1997 Jun 6;272(23):14713-20 PMID: 9169435
  50. Role of the juxtamembrane domains of the transforming growth factor-alpha precursor and the beta-amyloid precursor protein in regulated ectodomain shedding.
    J Biol Chem. 1997 Jul 4;272(27):17160-5 PMID: 9202036
  51. Metalloprotease-disintegrins: links to cell adhesion and cleavage of TNF alpha and Notch.
    Cell. 1997 Aug 22;90(4):589-92 PMID: 9288739
  52. Identification and characterization of a pro-tumor necrosis factor-alpha-processing enzyme from the ADAM family of zinc metalloproteases.
    J Biol Chem. 1997 Sep 26;272(39):24588-93 PMID: 9305925
  53. Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives.
    Physiol Rev. 1997 Oct;77(4):1081-132 PMID: 9354812
  54. The beta-amyloid precursor protein of Alzheimer's disease enhances neuron viability and modulates neuronal polarity.
    J Neurosci. 1997 Dec 15;17(24):9407-14 PMID: 9390996
  55. Alzheimer's amyloid precursor protein alpha-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase.
    Biochemistry. 1998 Feb 10;37(6):1680-5 PMID: 9484239
  56. The secretases that cleave angiotensin converting enzyme and the amyloid precursor protein are distinct from tumour necrosis factor-alpha convertase.
    FEBS Lett. 1998 Jul 10;431(1):63-5 PMID: 9684866
  57. Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer beta/A4 amyloid protein precursor.
    Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10075-8 PMID: 1359534
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2001-08-01
Pages
787-94
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1222008
Subset
IM
Grants
NINDS NIH HHS · NS30791 · United States
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