Plasma membrane microdomains regulate TACE-dependent TNFR1 shedding in human endothelial cells
Corresponding Author
Alessio D.’Alessio
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Dr. Alessio D’ALESSIO, Sapienza University of Rome, Section of Histology and Medical Embryology, Via A. Scarpa, 14. 00161, Rome, Italy. Tel.: +39-06-49766565 Fax: +39-06-4462854 E-mail: [email protected]Search for more papers by this authorBianca Esposito
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorClaudia Giampietri
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorElio Ziparo
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorJordan S. Pober
Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA
Search for more papers by this authorAntonio Filippini
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorCorresponding Author
Alessio D.’Alessio
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Dr. Alessio D’ALESSIO, Sapienza University of Rome, Section of Histology and Medical Embryology, Via A. Scarpa, 14. 00161, Rome, Italy. Tel.: +39-06-49766565 Fax: +39-06-4462854 E-mail: [email protected]Search for more papers by this authorBianca Esposito
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorClaudia Giampietri
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorElio Ziparo
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorJordan S. Pober
Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA
Search for more papers by this authorAntonio Filippini
Istituto Pasteur-Fondazione Cenci Bolognetti, Department of Anatomy, Histology, Forensic Medicine and Orthopedics–Section of Histology and Medical Embryology, Sapienza University of Rome, Rome, Italy
Search for more papers by this authorAbstract
Upon stimulation by histamine, human vascular endothelial cells (EC) shed a soluble form of tumour necrosis factor receptor 1 (sTNFR1) that binds up free TNF, dampening the inflammatory response. Shedding occurs through proteolytic cleavage of plasma membrane-expressed TNFR1 catalysed by TNF-α converting enzyme (TACE). Surface expressed TNFR1 on EC is largely sequestered into specific plasma membrane microdomains, the lipid rafts/caveolae. The purpose of this study was to determine the role of these domains in TACE-mediated TNFR1 shedding in response to histamine. Human umbilical vein endothelial cells derived EA.hy926 cells respond to histamine via H1 receptors to shed TNFR1. Both depletion of cholesterol by methyl-β-cyclodextrin and small interfering RNA knockdown of the scaffolding protein caveolin-1 (cav-1), treatments that disrupt caveolae, reduce histamine-induced shedding of membrane-bound TNFR1. Moreover, immunoblotting of discontinuous sucrose gradient fractions show that TACE, such as TNFR1, is present within low-density membrane fractions, concentrated within caveolae, in unstimulated EA.hy926 endothelial cells and co-immunoprecipitates with cav-1. Silencing of cav-1 reduces the levels of both TACE and TNFR1 protein and displaces TACE, from low-density membrane fractions where TNFR1 remains. In summary, we show that endothelial lipid rafts/caveolae co-localize TACE to surface expressed TNFR1, promoting efficient shedding of sTNFR1 in response to histamine.
References
- 1 Chen G, Goeddel DV. TNF-R1 signaling: abeautiful pathway. Science. 2002; 296: 1634–5.
- 2 Liu Z-G. Molecular mechanism of TNF signaling and beyond. Cell Res. 2005; 15: 24–7.
- 3 Loetscher H, Schlaeger EJ, Lahm HW, et al. Purification and partial amino acid sequence analysis of two distinct tumour necrosis factor receptors from HL60 cells. J Biol Chem. 1990; 265: 20131–8.
- 4 Slowik MR, De Luca LG, Fiers W, et al. Tumour necrosis factor activates human endothelial cells through the p55 tumour necrosis factor receptor but the p75 receptor contributes to activation at low tumour necrosis factor concentration. Am J Pathol. 1993; 143: 1724–30.
- 5 Aderka D, Engelmann H, Shemer-Avni Y, et al. Variation in serum levels of the soluble TNF receptors among healthy individuals. Lymphokine Cytokine Res. 1992; 11: 157–9.
- 6 Wang J, Al-Lamki RS, Zhang H, et al. Histamine antagonizes tumour necrosis factor (TNF) signaling by stimulating TNF receptor shedding from the cell surface and Golgi storage pool. J Biol Chem. 2003; 278: 21751–60.
- 7 Bradley JR, Thiru S, Pober JS. Disparate localization of 55-kd and 75-kd tumour necrosis factor receptors in human endothelial cells. Am J Pathol. 1995; 146: 27–32.
- 8 D’Alessio A, Kluger MS, Li JH, et al. Targeting of tumour necrosis factor receptor 1 to low density plasma membrane domains in human endothelial cells. J Biol Chem. 2010; 285: 23868–79.
- 9 Black RA, Rauch CT, Kozlosky CJ, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature. 1997; 385: 729–33.
- 10 Moss ML, Jin SL, Milla ME, et al. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature. 1997; 385: 733–6.
- 11 Reddy P, Slack JL, Davis R, et al. Functional analysis of the domain structure of tumour necrosis factor-alpha converting enzyme. J Biol Chem. 2000; 275: 14608–14.
- 12 Edwards DR, Handsley MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med. 2008; 29: 258–89.
- 13 Hooper NM, Karran EH, Turner AJ. Membrane protein secretases. Biochem J. 1997; 321: 265–79.
- 14 Li X, Perez L, Pan Z, et al. The transmembrane domain of TACE regulates protein ectodomain shedding. Cell Res. 2007; 17: 985–98.
- 15 McDermott MF, Aksentijevich I, Galon J, et al. Germline mutations in the extracellular domains of the 55 kDa TNF receptor, TNFR1, define a family of dominantly inherited autoinflammatory syndromes. Cell. 1999; 97: 133–44.
- 16 Galon J, Aksentijevich I, McDermott MF, et al. TNFRSF1A mutations and autoinflammatory syndromes. Curr Opin Immunol. 2000; 12: 479–86.
- 17 Helms JB, Zurzolo C. Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic. 2004; 5: 247–54.
- 18 Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol. 1955; 1: 445–58.
- 19 Stan RV, Roberts WG, Predescu D, et al. Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol Biol Cell. 1997; 8: 595–605.
- 20 Bruns RR, Palade GE. Studies on blood capillaries. I. General organization of blood capillaries in muscle. J Cell Biol. 1968; 37: 244–76.
- 21 Simionescu M, Simionescu N, Palade GE. Morphometric data on the endothelium of blood capillaries. J Cell Biol. 1974; 60: 128–52.
- 22 Johansson BR. Size and distribution of endothelial plasmalemmal vesicles in consecutive segments of the microvasculature in cat skeletal muscle. Microvasc Res. 1979; 17: 107–17.
- 23 Vasile E, Qu H, Dvorak HF, et al. Caveolae and vesiculo-vacuolar organelles in bovine capillary endothelial cells cultured with VPF/VEGF on floating Matrigel-collagen gels. J Histochem Cytochem. 1999; 47: 159–67.
- 24 D’Alessio A, Al-Lamki RS, Bradley JR, et al. Caveolae participate in tumour necrosis factor receptor 1 signaling and internalization in a human endothelial cell line. Am J Pathol. 2005; 166: 1273–82.
- 25 Tang Z, Scherer PE, Okamoto T, et al. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem. 1996; 271: 2255–61.
- 26 Glenney JR, Jr., Soppet D. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci USA. 1992; 89: 10517–21.
- 27 Scherer PE, Okamoto T, Chun M, et al. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc Natl Acad Sci USA. 1996; 93: 131–5.
- 28 Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev. 2002; 54: 431–67.
- 29 Anderson RG. The caveolae membrane system. Annu Rev Biochem. 1998; 67: 199–225.
- 30 Lisanti MP, Scherer PE, Tang Z, et al. Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol. 1994; 4: 231–5.
- 31 Sigismund S, Woelk T, Puri C, et al. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA. 2005; 102: 2760–5.
- 32 Aguilar RC, Wendland B. Endocytosis of membrane receptors: two pathways are better than one. Proc Natl Acad Sci USA. 2005; 102: 2679–80.
- 33 Kumari S, Mg S, Mayor S. Endocytosis unplugged: multiple ways to enter the cell. Cell Res. 2010; 20: 256–75.
- 34 Tellier E, Canault M, Rebsomen L, et al. The shedding activity of ADAM17 is sequestered in lipid rafts. Exp Cell Res. 2006; 312: 3969–80.
- 35 Gil C, Cubi R, Aguilera J. Shedding of the p75NTR neurotrophin receptor is modulated by lipid rafts. FEBS Lett. 2007; 581: 1851–8.
- 36 Schuster B, Meinert W, Rose-John S, et al. The human interleukin-6 (IL-6) receptor exists as a preformed dimer in the plasma membrane. FEBS Lett. 2003; 538: 113–6.
- 37 Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem. 1985; 260: 3440–50.
- 38 Sargiacomo M, Sudol M, Tang Z, et al. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol. 1993; 122: 789–807.
- 39 Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA. 1983; 80: 3734–7.
- 40 Hill SJ, Ganellin CR, Timmerman H, et al. International Union of Pharmacology. XIII. Classification of histamine receptors. Pharmacol Rev. 1997; 49: 253–78.
- 41 Li H, Burkhardt C, Heinrich UR, et al. Histamine upregulates gene expression of endothelial nitric oxide synthase in human vascular endothelial cells. Circulation. 2003; 107: 2348–54.
- 42 Carson MR, Shasby SS, Shasby DM. Histamine and inositol phosphate accumulation in endothelium: cAMP and a G protein. Am J Physiol. 1989; 257: L259–64.
- 43 Jacob R, Merritt JE, Hallam TJ, et al. Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells. Nature. 1988; 335: 40–5.
- 44 Rotrosen D, Gallin JI. Histamine type I receptor occupancy increases endothelial cytosolic calcium, reduces F-actin, and promotes albumin diffusion across cultured endothelial monolayers. J Cell Biol. 1986; 103: 2379–87.
- 45 Ostrom RS, Insel PA. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol. 2004; 143: 235–45.
- 46 Chini B, Parenti M. G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J Mol Endocrinol. 2004; 32: 325–38.
- 47 Zimina EP, Bruckner-Tuderman L, Franzke CW. Shedding of collagen XVII ectodomain depends on plasma membrane microenvironment. J Biol Chem. 2005; 280: 34019–24.
- 48 Matthews V, Schuster B, Schutze S, et al. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J Biol Chem. 2003; 278: 38829–39.
- 49 von Tresckow B, Kallen KJ, von Strandmann EP, et al. Depletion of cellular cholesterol and lipid rafts increases shedding of CD30. J Immunol. 2004; 172: 4324–31.
- 50 Duffy MJ, McKiernan E, O’Donovan N, et al. The role of ADAMs in disease pathophysiology. Clin Chim Acta. 2009; 403: 31–6.
- 51 Duffy MJ, McKiernan E, O’Donovan N, et al. Role of ADAMs in cancer formation and progression. Clin Cancer Res. 2009; 15: 1140–4.
- 52 Huang JF, Thurmond RL. The new biology of histamine receptors. Curr Allergy Asthma Rep. 2008; 8: 21–7.
- 53 Matsuki T, Ohhashi T. Endothelium and mechanical responses of isolated monkey pulmonary veins to histamine. Am J Physiol. 1990; 259: H1032–7.
- 54 Chipman P, Glover WE. Histamine H2-receptors in the human peripheral circulation. Br J Pharmacol. 1976; 56: 494–6.
- 55 Gantz I, Schaffer M, DelValle J, et al. Molecular cloning of a gene encoding the histamine H2 receptor. Proc Natl Acad Sci USA. 1991; 88: 429–33.
- 56 Traiffort E, Ruat M, Arrang JM, et al. Expression of a cloned rat histamine H2 receptor mediating inhibition of arachidonate release and activation of cAMP accumulation. Proc Natl Acad Sci USA. 1992; 89: 2649–53.