Redox Signaling in Endosomes Using the Example of EGF Receptors: A Graphical Review
Abstract
:1. Introduction
1.1. Models of the Early Endosome
1.2. Structure of the Early Endosome
1.3. Signaling Pathways at Early Endosomes
2. The Endosomal Compartment in EGF Signaling
3. Redox Control of the Endosomal Compartment in EGF Signaling
3.1. Redoxosomes
3.2. Redox-Dependent EGFR Trans-Activation
4. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
APPL | adapter protein containing PH domain, PTB domain and leucine zipper motif 1,2 |
CD | Cluster of differentiation |
CIN85 | Cbl-interacting protein |
CLC-3 | Chloride channel 3 protein |
DUB | Deubiquitinating enzyme |
EEA | Early endosome antigen |
EGF(R) | Epidermal growth factor (Receptor) |
Eps15 | Epidermal growth factor receptor substrate 15 |
ER | Endoplasmic reticulum |
Grb-2 | Growth factor receptor-bound protein 2 |
HRP | Horseradish peroxidase 1 |
Hrs | Hepatocyte growth factor-regulated tyrosine kinase substrate |
LAMP1 | Lysosome-associated membrane protein 1 |
LPA | Lysophosphatidic acid |
MTM1 | Myotubularin 1 |
Nox | NADPH oxidase |
PIK | Phosphoinositide kinase |
PtdIns | Phosphatidylinositol |
PTP1B | Phosphotyrosine phosphatase 1 |
Rab(IP) | Ras-related protein (interacting protein) |
Rabaptin | Rab GTPase-binding effector protein |
ROS | Reactive oxygen species |
SNARE | Soluble N-ethylmaleimide-sensitive factor attachment protein receptor |
SNX | Sorting nexin |
SOD | Superoxide dismutase |
STAM | Signal transducing adaptor molecule |
TGF | Transforming growth factor |
TNF | Tumor necrosis factor |
Tsg101 | Tumor susceptibility gene 101 |
Ub | Ubiquitin |
References
- Steinman, R.M.; Mellman, I.S.; Muller, W.A.; Cohn, Z.A. Endocytosis and the recycling of plasma membrane. J. Cell Biol. 1983, 96, 1–27. [Google Scholar] [CrossRef] [PubMed]
- Bonelli, M.; Kerschbaumer, A.; Kastrati, K.; Ghoreschi, K.; Gadina, M.; Heinz, L.X.; Smolen, J.S.; Aletaha, D.; O’Shea, J.; Laurence, A. Selectivity, efficacy and safety of JAKinibs: New evidence for a still evolving story. Ann. Rheum. Dis. 2024, 83, 139–160. [Google Scholar] [CrossRef]
- Heldin, C.-H.; Lu, B.; Evans, R.; Gutkind, J.S. Signals and Receptors. Cold Spring Harb. Perspect. Biol. 2016, 8, a005900. [Google Scholar] [CrossRef] [PubMed]
- Gruenberg, J. The endocytic pathway: A mosaic of domains. Nat. Rev. Mol. Cell Biol. 2001, 2, 721–730. [Google Scholar] [CrossRef] [PubMed]
- Kumari, S.; Mg, S.; Mayor, S. Endocytosis unplugged: Multiple ways to enter the cell. Cell Res. 2010, 20, 256–275. [Google Scholar] [CrossRef]
- Huotari, J.; Helenius, A. Endosome maturation. EMBO J. 2011, 30, 3481–3500. [Google Scholar] [CrossRef] [PubMed]
- Jovic, M.; Sharma, M.; Rahajeng, J.; Caplan, S. The early endosome: A busy sorting station for proteins at the crossroads. Histol. Histopathol. 2010, 25, 99–112. [Google Scholar] [PubMed]
- Naslavsky, N.; Caplan, S. The enigmatic endosome—Sorting the ins and outs of endocytic trafficking. J. Cell Sci. 2018, 131, jcs216499. [Google Scholar] [CrossRef]
- Griffiths, G.; Gruenberg, J. The arguments for pre-existing early and late endosomes. Trends Cell Biol. 1991, 1, 5–9. [Google Scholar] [CrossRef]
- Kamentseva, R.; Kosheverova, V.; Kharchenko, M.; Zlobina, M.; Salova, A.; Belyaeva, T.; Nikolsky, N.; Kornilova, E. Functional cycle of EEA1-positive early endosome: Direct evidence for pre-existing compartment of degradative pathway. PLoS ONE 2020, 15, e0232532. [Google Scholar] [CrossRef]
- Dunn, K.W.; Maxfield, F.R. Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J. Cell Biol. 1992, 117, 301–310. [Google Scholar] [CrossRef]
- Sadowski, L.; Pilecka, I.; Miaczynska, M. Signaling from endosomes: Location makes a difference. Exp. Cell Res. 2009, 315, 1601–1609. [Google Scholar] [CrossRef]
- Scita, G.; Di Fiore, P.P. The endocytic matrix. Nature 2010, 463, 464–473. [Google Scholar] [CrossRef] [PubMed]
- Carpenter, G.; Cohen, S. Epidermal growth factor. Annu. Rev. Biochem. 1979, 48, 193–216. [Google Scholar] [CrossRef]
- Roskoski, R. The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol. Res. 2014, 79, 34–74. [Google Scholar] [CrossRef]
- Tomas, A.; Futter, C.E.; Eden, E.R. EGF receptor trafficking: Consequences for signaling and cancer. Trends Cell Biol. 2014, 24, 26–34. [Google Scholar] [CrossRef]
- Mellman, I. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 1996, 12, 575–625. [Google Scholar] [CrossRef]
- Stoorvogel, W.; Strous, G.J.; Geuze, H.J.; Oorschot, V.; Schwartzt, A.L. Late endosomes derive from early endosomes by maturation. Cell 1991, 65, 417–427. [Google Scholar] [CrossRef]
- Dammai, V. Endosomal Compartments. In Encyclopedia of Cancer; Schwab, M., Ed.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 1244–1248. [Google Scholar]
- Ferguson, S.M.; de Camilli, P. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 2012, 13, 75–88. [Google Scholar] [CrossRef]
- Lakadamyali, M.; Rust, M.J.; Zhuang, X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 2006, 124, 997–1009. [Google Scholar] [CrossRef]
- Roepstorff, K.; Grøvdal, L.; Grandal, M.; Lerdrup, M.; van Deurs, B. Endocytic downregulation of ErbB receptors: Mechanisms and relevance in cancer. Histochem. Cell Biol. 2008, 129, 563–578. [Google Scholar] [CrossRef] [PubMed]
- Bertelsen, V.; Stang, E. The Mysterious Ways of ErbB2/HER2 Trafficking. Membranes 2014, 4, 424–446. [Google Scholar] [CrossRef]
- Barral, D.C.; Staiano, L.; Guimas Almeida, C.; Cutler, D.F.; Eden, E.R.; Futter, C.E.; Galione, A.; Marques, A.R.A.; Medina, D.L.; Napolitano, G.; et al. Current methods to analyze lysosome morphology, positioning, motility and function. Traffic 2022, 23, 238–269. [Google Scholar] [CrossRef] [PubMed]
- Forgac, M. Structure and properties of the coated vesicle proton pump. Ann. N. Y. Acad. Sci. 1992, 671, 273–283. [Google Scholar] [CrossRef]
- Hara-Chikuma, M.; Yang, B.; Sonawane, N.D.; Sasaki, S.; Uchida, S.; Verkman, A.S. ClC-3 Chloride Channels Facilitate Endosomal Acidification and Chloride Accumulation. J. Biol. Chem. 2005, 280, 1241–1247. [Google Scholar] [CrossRef]
- Stein, M.-P.; Dong, J.; Wandinger-Ness, A. Rab proteins and endocytic trafficking: Potential targets for therapeutic intervention. Adv. Drug. Deliv. Rev. 2003, 55, 1421–1437. [Google Scholar] [CrossRef] [PubMed]
- Roepstorff, K.; Grandal, M.V.; Henriksen, L.; Knudsen, S.L.J.; Lerdrup, M.; Grøvdal, L.; Willumsen, B.M.; van Deurs, B. Differential effects of EGFR ligands on endocytic sorting of the receptor. Traffic 2009, 10, 1115–1127. [Google Scholar] [CrossRef]
- Tan, X.; Lambert, P.F.; Rapraeger, A.C.; Anderson, R.A. Stress-Induced EGFR Trafficking: Mechanisms, Functions, and Therapeutic Implications. Trends Cell Biol. 2016, 26, 352–366. [Google Scholar] [CrossRef]
- Schroeder, B.; Srivatsan, S.; Shaw, A.; Billadeau, D.; McNiven, M.A. CIN85 phosphorylation is essential for EGFR ubiquitination and sorting into multivesicular bodies. MBoC 2012, 23, 3602–3611. [Google Scholar] [CrossRef]
- Levkowitz, G.; Waterman, H.; Zamir, E.; Kam, Z.; Oved, S.; Langdon, W.Y.; Beguinot, L.; Geiger, B.; Yarden, Y. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 1998, 12, 3663–3674. [Google Scholar] [CrossRef]
- van Bergen En Henegouwen, P.M. Eps15: A multifunctional adaptor protein regulating intracellular trafficking. Cell Commun. Signal. 2009, 7, 24. [Google Scholar] [CrossRef] [PubMed]
- Fraser, J.; Simpson, J.; Fontana, R.; Kishi-Itakura, C.; Ktistakis, N.T.; Gammoh, N. Targeting of early endosomes by autophagy facilitates EGFR recycling and signalling. EMBO Rep. 2019, 20. [Google Scholar] [CrossRef]
- Herbst, J.J.; Opresko, L.K.; Walsh, B.J.; Lauffenburger, D.A.; Wiley, H.S. Regulation of postendocytic trafficking of the epidermal growth factor receptor through endosomal retention. J. Biol. Chem. 1994, 269, 12865–12873. [Google Scholar] [CrossRef] [PubMed]
- Rink, J.; Ghigo, E.; Kalaidzidis, Y.; Zerial, M. Rab Conversion as a Mechanism of Progression from Early to Late Endosomes. Cell 2005, 122, 735–749. [Google Scholar] [CrossRef] [PubMed]
- Willingham, M.C.; Pastan, I. The receptosome: An intermediate organelle of receptor mediated endocytosis in cultured fibroblasts. Cell 1980, 21, 67–77. [Google Scholar] [CrossRef]
- Futter, C.E.; Pearse, A.; Hewlett, L.J.; Hopkins, C.R. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol. 1996, 132, 1011–1023. [Google Scholar] [CrossRef] [PubMed]
- Bi, X.; Yin, J.; Zhang, D.; Zhang, X.; Balamkundu, S.; Lescar, J.; Dedon, P.C.; Tam, J.P.; Liu, C.-F. Tagging Transferrin Receptor with a Disulfide FRET Probe To Gauge the Redox State in Endosomal Compartments. Anal. Chem. 2020, 92, 12460–12466. [Google Scholar] [CrossRef] [PubMed]
- Shahin, W.S.; Engelhardt, J.F. Isolation of Redox-Active Endosomes (Redoxosomes) and Assessment of NOX Activity. Methods Mol. Biol. 2019, 1982, 461–472. [Google Scholar]
- Löwe, O.; Rezende, F.; Heidler, J.; Wittig, I.; Helfinger, V.; Brandes, R.P.; Schröder, K. BIAM switch assay coupled to mass spectrometry identifies novel redox targets of NADPH oxidase 4. Redox Biol. 2019, 21, 101125. [Google Scholar] [CrossRef]
- Pillay, C.S.; Elliott, E.; Dennison, C. Endolysosomal proteolysis and its regulation. Biochem. J. 2002, 363, 417–429. [Google Scholar] [CrossRef]
- Collins, D.S.; Unanue, E.R.; Harding, C.V. Reduction of disulfide bonds within lysosomes is a key step in antigen processing. J. Immunol. 1991, 147, 4054–4059. [Google Scholar] [CrossRef] [PubMed]
- Austin, C.D.; Wen, X.; Gazzard, L.; Nelson, C.; Scheller, R.H.; Scales, S.J. Oxidizing potential of endosomes and lysosomes limits intracellular cleavage of disulfide-based antibody-drug conjugates. Proc. Natl. Acad. Sci. USA 2005, 102, 17987–17992. [Google Scholar] [CrossRef] [PubMed]
- Dingjan, I.; Linders, P.T.A.; van den Bekerom, L.; Baranov, M.V.; Halder, P.; Beest, M.; ter van den Bogaart, G. Oxidized phagosomal NOX2 complex is replenished from lysosomes. J. Cell Sci. 2017, 130, 1285–1298. [Google Scholar] [CrossRef]
- Schröder, K.; Weissmann, N.; Brandes, R.P. Organizers and activators: Cytosolic Nox proteins impacting on vascular function. Free. Radic. Biol. Med. 2017, 109, 22–32. [Google Scholar] [CrossRef] [PubMed]
- Oakley, F.D.; Abbott, D.; Li, Q.; Engelhardt, J.F. Signaling Components of Redox Active Endosomes: The Redoxosomes. Antioxid. Redox Signal. 2009, 11, 1313–1333. [Google Scholar] [CrossRef]
- Spencer, N.Y.; Engelhardt, J.F. The Basic Biology of Redoxosomes in Cytokine-Mediated Signal Transduction and Implications for Disease-Specific Therapies. Biochemistry 2014, 53, 1551–1564. [Google Scholar] [CrossRef]
- Schröder, K. NADPH oxidases: Current aspects and tools. Redox Biol. 2020, 34, 101512. [Google Scholar] [CrossRef]
- Ewanchuk, B.W.; Yates, R.M. The phagosome and redox control of antigen processing. Free Radic. Biol. Med. 2018, 125, 53–61. [Google Scholar] [CrossRef]
- Moghadam, Z.M.; Henneke, P.; Kolter, J. From Flies to Men: ROS and the NADPH Oxidase in Phagocytes. Front. Cell Dev. Biol. 2021, 9, 628991. [Google Scholar] [CrossRef]
- Klomsiri, C.; Rogers, L.C.; Soito, L.; McCauley, A.K.; King, S.B.; Nelson, K.J.; Poole, L.B.; Daniel, L.W. Endosomal H2O2 production leads to localized cysteine sulfenic acid formation on proteins during lysophosphatidic acid-mediated cell signaling. Free Radic. Biol. Med. 2014, 71, 49–60. [Google Scholar] [CrossRef]
- Li, Q.; Harraz, M.M.; Zhou, W.; Zhang, L.N.; Ding, W.; Zhang, Y.; Eggleston, T.; Yeaman, C.; Banfi, B.; Engelhardt, J.F. Nox2 and Rac1 regulate H2O2-dependent recruitment of TRAF6 to endosomal interleukin-1 receptor complexes. Mol. Cell. Biol. 2006, 26, 140–154. [Google Scholar] [CrossRef]
- Fisher, A.B. Redox signaling across cell membranes. Antioxid. Redox Signal. 2009, 11, 1349–1356. [Google Scholar] [CrossRef] [PubMed]
- Miller, F.J.; Filali, M.; Huss, G.J.; Stanic, B.; Chamseddine, A.; Barna, T.J.; Lamb, F.S. Cytokine Activation of Nuclear Factor κB in Vascular Smooth Muscle Cells Requires Signaling Endosomes Containing Nox1 and ClC-3. Circ. Res. 2007, 101, 663–671. [Google Scholar] [CrossRef] [PubMed]
- Chu, Y.; Piper, R.; Richardson, S.; Watanabe, Y.; Patel, P.; Heistad, D.D. Endocytosis of extracellular superoxide dismutase into endothelial cells: Role of the heparin-binding domain. ATVB 2006, 26, 1985–1990. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Wu, S.; Wang, J.; Li, Z.; Cui, H.; Lin, S.; Zhu, J.; Chen, Q. Superoxide dismutase transcellular shuttle constructed from dendritic MOF and charge reversible protein derivatives. Chem. Sci. 2019, 10, 4476–4485. [Google Scholar] [CrossRef]
- Helmcke, I.; Heumüller, S.; Tikkanen, R.; Schröder, K.; Brandes, R.P. Identification of structural elements in Nox1 and Nox4 controlling localization and activity. Antioxid. Redox Signal. 2009, 11, 1279–1287. [Google Scholar] [CrossRef]
- Park, D.-R.; Nam, T.-S.; Kim, Y.-W.; Bae, Y.S.; Kim, U.-H. Oxidative activation of type III CD38 by NADPH oxidase-derived hydrogen peroxide in Ca2+ signaling. FASEB J. 2019, 33, 3404–3419. [Google Scholar] [CrossRef]
- Forrester, S.J.; Kawai, T.; O’Brien, S.; Thomas, W.; Harris, R.C.; Eguchi, S. Epidermal Growth Factor Receptor Transactivation: Mechanisms, Pathophysiology, and Potential Therapies in the Cardiovascular System. Annu. Rev. Pharmacol. Toxicol. 2016, 56, 627–653. [Google Scholar] [CrossRef]
- Heppner, D.E.; Hristova, M.; Dustin, C.M.; Danyal, K.; Habibovic, A.; van der Vliet, A. The NADPH Oxidases DUOX1 and NOX2 Play Distinct Roles in Redox Regulation of Epidermal Growth Factor Receptor Signaling. J. Biol. Chem. 2016, 291, 23282–23293. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Zhou, C.; Zhao, Y.; Zhang, X.; Chen, W.; Zhou, Q.; Hu, B.; Gao, D.; Raatz, L.; Wang, Z.; et al. Quiescin sulfhydryl oxidase 1 promotes sorafenib-induced ferroptosis in hepatocellular carcinoma by driving EGFR endosomal trafficking and inhibiting NRF2 activation. Redox Biol. 2021, 41, 101942. [Google Scholar] [CrossRef]
- Chakravarthi, S.; Jessop, C.E.; Willer, M.; Stirling, C.J.; Bulleid, N.J. Intracellular catalysis of disulfide bond formation by the human sulfhydryl oxidase, QSOX1. Biochem. J. 2007, 404, 403–411. [Google Scholar] [CrossRef] [PubMed]
- Kodali, V.K.; Thorpe, C. Oxidative protein folding and the Quiescin-sulfhydryl oxidase family of flavoproteins. Antioxid. Redox Signal. 2010, 13, 1217–1230. [Google Scholar] [CrossRef] [PubMed]
- Mumbengegwi, D.R.; Li, Q.; Li, C.; Bear, C.E.; Engelhardt, J.F. Evidence for a superoxide permeability pathway in endosomal membranes. Mol. Cell. Biol. 2008, 28, 3700–3712. [Google Scholar] [CrossRef] [PubMed]
- Gianni, D.; Bohl, B.; Courtneidge, S.A.; Bokoch, G.M. The Involvement of the Tyrosine Kinase c-Src in the Regulation of Reactive Oxygen Species Generation Mediated by NADPH Oxidase-1. MBoC 2008, 19, 2984–2994. [Google Scholar] [CrossRef]
- Moody, T.W.; Nuche-Berenguer, B.; Nakamura, T.; Jensen, R.T. EGFR Transactivation by Peptide G Protein-Coupled Receptors in Cancer. Curr. Drug Targets 2016, 17, 520–528. [Google Scholar] [CrossRef]
- Arteaga, C.L.; Engelman, J.A. ERBB Receptors: From Oncogene Discovery to Basic Science to Mechanism-Based Cancer Therapeutics. Cancer Cell 2014, 25, 282–303. [Google Scholar] [CrossRef]
Type I Signaling: | Type II Signaling | Type III Signaling | ||
---|---|---|---|---|
IIIA | IIIB | |||
Ligand binding to the receptor results in direct signal transduction | Upon binding of the ligand, second messengers mediate signal transduction | Binding of the ligand to its receptor induces internalization and formation of endosomes, which transduced the appropriate signaling cascade | Recruitment of cytosolic proteins to the receptor, followed by internalization and endosome formation | Fusion of the endosome with other intracellular vesicles |
e.g., Tyrosinkinase receptors | e.g., Adrenalin β-receptors | e.g., EGF-receptor | e.g., EGF- and TGFβ-receptors | e.g., TNFα-receptor fuses with the Golgi to transduce apoptosis signals |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Hebchen, D.M.; Schröder, K. Redox Signaling in Endosomes Using the Example of EGF Receptors: A Graphical Review. Antioxidants 2024, 13, 1215. https://doi.org/10.3390/antiox13101215
Hebchen DM, Schröder K. Redox Signaling in Endosomes Using the Example of EGF Receptors: A Graphical Review. Antioxidants. 2024; 13(10):1215. https://doi.org/10.3390/antiox13101215
Chicago/Turabian StyleHebchen, Dana Maureen, and Katrin Schröder. 2024. "Redox Signaling in Endosomes Using the Example of EGF Receptors: A Graphical Review" Antioxidants 13, no. 10: 1215. https://doi.org/10.3390/antiox13101215
APA StyleHebchen, D. M., & Schröder, K. (2024). Redox Signaling in Endosomes Using the Example of EGF Receptors: A Graphical Review. Antioxidants, 13(10), 1215. https://doi.org/10.3390/antiox13101215