Molecular and cellular mechanisms of ectodomain shedding - PubMed (original) (raw)
Review
Molecular and cellular mechanisms of ectodomain shedding
Kazutaka Hayashida et al. Anat Rec (Hoboken). 2010 Jun.
Abstract
The extracellular domain of several membrane-anchored proteins is released from the cell surface as soluble proteins through a regulated proteolytic mechanism called ectodomain shedding. Cells use ectodomain shedding to actively regulate the expression and function of surface molecules, and modulate a wide variety of cellular and physiological processes. Ectodomain shedding rapidly converts membrane-associated proteins into soluble effectors and, at the same time, rapidly reduces the level of cell surface expression. For some proteins, ectodomain shedding is also a prerequisite for intramembrane proteolysis, which liberates the cytoplasmic domain of the affected molecule and associated signaling factors to regulate transcription. Ectodomain shedding is a process that is highly regulated by specific agonists, antagonists, and intracellular signaling pathways. Moreover, only about 2% of cell surface proteins are released from the surface by ectodomain shedding, indicating that cells selectively shed their protein ectodomains. This review will describe the molecular and cellular mechanisms of ectodomain shedding, and discuss its major functions in lung development and disease.
Figures
Fig. 1
Regulatory mechanisms of ectodomain shedding. Mechanisms as diverse as protein–protein interactions, phosphorylation, intracellular trafficking, polarized secretion, and activation of sheddases contribute to the regulation of ectodomain shedding at the cell surface. Several examples are shown. (1) Intracellular protein–protein interaction: Calmodulin constitutively bound to the cytoplasmic tail of substrates (e.g., L-selectin, ACE) inhibits ectodomain shedding, and the dissociation of calmodulin induced by calmodulin kinase enhances shedding. In contrast, PMA stimulation induces the association of moesin, potentiating the shedding of substrates (e.g., L-selectin). (2) Extracellular protein–protein interaction: Binding of ARTS-1 to cytokine receptors, such as TNFRI and IL-6R, activates shedding possibly by inducing a conformational change in the substrate or by displacing an inhibitory factor from the substrate. (3) Intracellular trafficking of substrate: BiP binds to substrates (e.g., ACE) and retains the substrate in the ER, preventing its encounter with the sheddase at the cell surface. (4) Phosphorylation of sheddase: PTKs or PKCs may activate the sheddase through Tyr or Ser/Thr phosphorylation of the cytoplasmic tail of the membrane-associated sheddase. (5) Activation of sheddase: Sheddases belonging to the ADAM or MMP family are activated by removal of the prodomain by furin and furin-like PCs in the trans Golgi compartment and also at the cell surface. (6) Intracellular trafficking of sheddase: TACE/ADAM17 is trafficked to the cell surface in a phosphorylation-dependent manner. For example, gastrin-releasing peptide activates a Src-PI3K-PDK pathway that induces Ser/Thr phosphorylation and promotes ADAM translocation to the cell surface. (7) Mobilization to specific membrane compartments: The substrate and sheddase can be secreted or sequestered in a polarized fashion to a specific membrane compartment on the cell surface or in intracellular compartments, which can accelerate the encounter of sheddase and substrate. (8) Interaction with modifying proteins on an adjacent cell: Binding of DSL ligand to heterodimeric Notch on an adjacent cell induces the endocytosis of the Notch-DSL ligand complex by DSL ligand expressing cells, providing a mechanical force to dissociate heterodimeric Notch and activate Notch shedding and signaling.
Similar articles
- Proteolytic ectodomain shedding of membrane proteins in mammals-hardware, concepts, and recent developments.
Lichtenthaler SF, Lemberg MK, Fluhrer R. Lichtenthaler SF, et al. EMBO J. 2018 Aug 1;37(15):e99456. doi: 10.15252/embj.201899456. Epub 2018 Jul 5. EMBO J. 2018. PMID: 29976761 Free PMC article. Review. - Functional and biochemical characterization of ADAMs and their predicted role in protein ectodomain shedding.
Blobel CP. Blobel CP. Inflamm Res. 2002 Feb;51(2):83-4. doi: 10.1007/BF02684007. Inflamm Res. 2002. PMID: 11926318 Review. - Protein-Labeling Fluorescent Probe Reveals Ectodomain Shedding of Transmembrane Carbonic Anhydrases.
Lin FL, Yen JT, Fang PW, Xu SQ, Lin JC, Tan KT. Lin FL, et al. ACS Chem Biol. 2022 Nov 18;17(11):3218-3228. doi: 10.1021/acschembio.2c00679. Epub 2022 Nov 1. ACS Chem Biol. 2022. PMID: 36318872 - Control of ErbB signaling through metalloprotease mediated ectodomain shedding of EGF-like factors.
Sanderson MP, Dempsey PJ, Dunbar AJ. Sanderson MP, et al. Growth Factors. 2006 Jun;24(2):121-36. doi: 10.1080/08977190600634373. Growth Factors. 2006. PMID: 16801132 Review. - SheddomeDB: the ectodomain shedding database for membrane-bound shed markers.
Tien WS, Chen JH, Wu KP. Tien WS, et al. BMC Bioinformatics. 2017 Mar 14;18(Suppl 3):42. doi: 10.1186/s12859-017-1465-7. BMC Bioinformatics. 2017. PMID: 28361715 Free PMC article. Review.
Cited by
- A bispecific anti-PD-1 and PD-L1 antibody induces PD-1 cleavage and provides enhanced anti-tumor activity.
Albu DI, Wolf BJ, Qin Y, Wang X, Daniel Ulumben A, Su M, Li V, Ding E, Angel Gonzalo J, Kong J, Jadhav R, Kuklin N, Visintin A, Gong B, Schuetz TJ. Albu DI, et al. Oncoimmunology. 2024 Feb 16;13(1):2316945. doi: 10.1080/2162402X.2024.2316945. eCollection 2024. Oncoimmunology. 2024. PMID: 38379869 Free PMC article. - ADAM10 mediates shedding of carbonic anhydrase IX ectodomain non‑redundantly to ADAM17.
Zatovicova M, Kajanova I, Takacova M, Jelenska L, Sedlakova O, Labudova M, Pastorekova S. Zatovicova M, et al. Oncol Rep. 2023 Feb;49(2):27. doi: 10.3892/or.2022.8464. Epub 2022 Dec 16. Oncol Rep. 2023. PMID: 36524367 Free PMC article. - EpCAM and the biology of hepatic stem/progenitor cells.
Dollé L, Theise ND, Schmelzer E, Boulter L, Gires O, van Grunsven LA. Dollé L, et al. Am J Physiol Gastrointest Liver Physiol. 2015 Feb 15;308(4):G233-50. doi: 10.1152/ajpgi.00069.2014. Epub 2014 Dec 4. Am J Physiol Gastrointest Liver Physiol. 2015. PMID: 25477371 Free PMC article. Review. - Roles for trafficking and O-linked glycosylation in the turnover of model cell surface proteins.
Karabasheva D, Cole NB, Donaldson JG. Karabasheva D, et al. J Biol Chem. 2014 Jul 11;289(28):19477-90. doi: 10.1074/jbc.M114.564666. Epub 2014 Jun 2. J Biol Chem. 2014. PMID: 24891503 Free PMC article. - Colocalization with MMP-7 in the Distal Colon is Crucial for Syndecan-2 Shedding in Dextran Sulfate Sodium-Induced Colitis Mice.
Hong H, Song HK, Jang B, Park E, Han DS, Kim SE, Oh ES. Hong H, et al. J Inflamm Res. 2021 Sep 29;14:4987-5000. doi: 10.2147/JIR.S329234. eCollection 2021. J Inflamm Res. 2021. PMID: 34616168 Free PMC article.
References
- Abel S, Hundhausen C, Mentlein R, Schulte A, Berkhout TA, Broadway N, Hartmann D, Sedlacek R, Dietrich S, Muetze B, Schuster B, Kallen KJ, Saftig P, Rose-John S, Ludwig A. The transmembrane CXC-chemokine ligand 16 is induced by IFN-gamma and TNF-alpha and shed by the activity of the disintegrin-like metalloproteinase ADAM10. J Immunol. 2004;172:6362–6372. - PubMed
- Ahmed Z, Mazibrada G, Seabright RJ, Dent RG, Berry M, Logan A. TACE-induced cleavage of NgR and p75NTR in dorsal root ganglion cultures disinhibits outgrowth and promotes branching of neurites in the presence of inhibitory CNS myelin. FASEB J. 2006;20:1939–1941. - PubMed
- Alele J, Jiang J, Goldsmith JF, Yang X, Maheshwari HG, Black RA, Baumann G, Frank SJ. Blockade of growth hormone receptor shedding by a metalloprotease inhibitor. Endocrinology. 1998;139:1927–1935. - PubMed
- Arribas J, Coodly L, Vollmer P, Kishimoto TK, Rose-John S, Massague J. Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J Biol Chem. 1996;271:11376–11382. - PubMed
- Arribas J, Lopez-Casillas F, Massague J. 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;272:17160–17165. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- HL81474/HL/NHLBI NIH HHS/United States
- R01 HL069050/HL/NHLBI NIH HHS/United States
- HL73725/HL/NHLBI NIH HHS/United States
- R01 HL081474/HL/NHLBI NIH HHS/United States
- HL69050/HL/NHLBI NIH HHS/United States
- R01 HL073725/HL/NHLBI NIH HHS/United States
LinkOut - more resources
Full Text Sources