Short-term TNFα shedding is independent of cytoplasmic phosphorylation or furin cleavage of ADAM17

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3355-3367

  Schwarz, Jeanette ^a   Broder, Claudia ^a   Helmstetter, Ansgard ^a   Schmidt, Stefanie ^a   Yan, Isabell ^b   Müller, Miryam ^a   Schmidt Arras, Dirk ^a   Becker Pauly, Christoph ^a   Koch Nolte, Friedrich ^b   Mittrücker, Hans Willi ^b   Rabe, Björn ^a   Rose John, Stefan ^a   Chalaris, Athena ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

ADAM17; Cell surface trafficking; Furin; Intracellular domain; Phosphorylation; TNF

Indexed keywords

ADAM PROTEIN; ADAM17 PROTEIN; ANISOMYCIN; CALYCULIN A; CANTHARIDIN; FURIN; MITOGEN ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

EID: 84886787514     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.10.005     Document Type: Article

References (69)

1. Blobel C.P. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell Biol. 2005, 6:32-43.
2. Reiss K., Saftig P. The "A Disintegrin And Metalloprotease" (ADAM) family of sheddases: physiological and cellular functions. Semin. Cell Dev. Biol. 2009, 20:126-137.
3. Saftig P., Reiss K. The "A Disintegrin And Metalloproteases" ADAM10 and ADAM17: novel drug targets with therapeutic potential?. Eur. J. Cell Biol. 2011, 90:527-535.
4. Gooz M. ADAM-17: the enzyme that does it all. Crit. Rev. Biochem. Mol. Biol. 2010, 45:146-169.
5. Rivera S., Khrestchatisky M., Kaczmarek L., Rosenberg G.A., Jaworski D.M. Metzincin proteases and their inhibitors: foes or friends in nervous system physiology?. J. Neurosci. 2010, 30:15337-15357.
6. Black R.A., Rauch C.T., Kozlosky C.J., Peschon J.J., Slack J.L., Wolfson M.F., Castner B.J., Stocking K.L., Reddy P., Srinivasan S., Nelson N., Boiani N., Schooley K.A., Gerhart M., Davis R., Fitzner J.N., Johnson R.S., Paxton R.J., March C.J., Cerretti D.P. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 1997, 385:729-733.
7. Moss M.L., Jin S.L., Milla M.E., Bickett D.M., Burkhart W., Carter H.L., Chen W.J., Clay W.C., Didsbury J.R., Hassler D., Hoffman C.R., Kost T.A., Lambert M.H., Leesnitzer M.A., McCauley P., McGeehan G., Mitchell J., Moyer M., Pahel G., Rocque W., Overton L.K., Schoenen F., Seaton T., Su J.L., Becherer J.D., et al. Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor-alpha. Nature 1997, 385:733-736.
8. Horiuchi K., Kimura T., Miyamoto T., Takaishi H., Okada Y., Toyama Y., Blobel C.P. Cutting edge: TNF-alpha-converting enzyme (TACE/ADAM17) inactivation in mouse myeloid cells prevents lethality from endotoxin shock. J. Immunol. 2007, 179:2686-2689.
9. Long C., Wang Y., Herrera A.H., Horiuchi K., Walcheck B. In vivo role of leukocyte ADAM17 in the inflammatory and host responses during E. coli-mediated peritonitis. J. Leukoc. Biol. 2010, 87:1097-1101.
10. Peschon J.J., Slack J.L., Reddy P., Stocking K.L., Sunnarborg S.W., Lee D.C., Russell W.E., Castner B.J., Johnson R.S., Fitzner J.N., Boyce R.W., Nelson N., Kozlosky C.J., Wolfson M.F., Rauch C.T., Cerretti D.P., Paxton R.J., March C.J., Black R.A. An essential role for ectodomain shedding in mammalian development. Science 1998, 282:1281-1284.
11. Brandl K., Sun L., Neppl C., Siggs O.M., Le Gall S.M., Tomisato W., Li X., Du X., Maennel D.N., Blobel C.P., Beutler B. MyD88 signaling in nonhematopoietic cells protects mice against induced colitis by regulating specific EGF receptor ligands. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:19967-19972.
12. Brandl K., Tomisato W., Beutler B. Inflammatory bowel disease and ADAM17 deletion. N. Engl. J. Med. 2012, 366:190. (author reply 190).
13. Chalaris A., Adam N., Sina C., Rosenstiel P., Lehmann-Koch J., Schirmacher P., Hartmann D., Cichy J., Gavrilova O., Schreiber S., Jostock T., Matthews V., Hasler R., Becker C., Neurath M.F., Reiss K., Saftig P., Scheller J., Rose-John S. Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J. Exp. Med. 2010, 207:1617-1624.
14. Scheller J., Chalaris A., Garbers C., Rose-John S. ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 2011, 32:380-387.
15. Schlondorff J., Becherer J.D., Blobel C.P. Intracellular maturation and localization of the tumour necrosis factor alpha convertase (TACE). Biochem. J. 2000, 347(Pt 1):131-138.
16. Chanthaphavong R.S., Loughran P.A., Lee T.Y., Scott M.J., Billiar T.R. A role for cGMP in inducible nitric-oxide synthase (iNOS)-induced tumor necrosis factor (TNF) alpha-converting enzyme (TACE/ADAM17) activation, translocation, and TNF receptor 1 (TNFR1) shedding in hepatocytes. J. Biol. Chem. 2012, 287:35887-35898.
17. Killock D.J., Ivetic A. The cytoplasmic domains of TNFalpha-converting enzyme (TACE/ADAM17) and L-selectin are regulated differently by p38 MAPK and PKC to promote ectodomain shedding. Biochem. J. 2010, 428:293-304.
18. Rousseau S., Papoutsopoulou M., Symons A., Cook D., Lucocq J.M., Prescott A.R., O'Garra A., Ley S.C., Cohen P. TPL2-mediated activation of ERK1 and ERK2 regulates the processing of pre-TNF alpha in LPS-stimulated macrophages. J. Cell Sci. 2008, 121:149-154.
19. Xu P., Derynck R. Direct activation of TACE-mediated ectodomain shedding by p38 MAP kinase regulates EGF receptor-dependent cell proliferation. Mol. Cell 2010, 37:551-566.
20. Xu P., Liu J., Sakaki-Yumoto M., Derynck R. TACE activation by MAPK-mediated regulation of cell surface dimerization and TIMP3 association. Sci. Signal. 2012, 5:ra34.
21. Zhang Q., Thomas S.M., Lui V.W., Xi S., Siegfried J.M., Fan H., Smithgall T.E., Mills G.B., Grandis J.R. Phosphorylation of TNF-alpha converting enzyme by gastrin-releasing peptide induces amphiregulin release and EGF receptor activation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:6901-6906.
22. Soond S.M., Everson B., Riches D.W., Murphy G. ERK-mediated phosphorylation of Thr735 in TNFalpha-converting enzyme and its potential role in TACE protein trafficking. J. Cell Sci. 2005, 118:2371-2380.
23. Rosso O., Piazza T., Bongarzone I., Rossello A., Mezzanzanica D., Canevari S., Orengo A.M., Puppo A., Ferrini S., Fabbi M. The ALCAM shedding by the metalloprotease ADAM17/TACE is involved in motility of ovarian carcinoma cells. Mol. Cancer Res. 2007, 5:1246-1253.
24. Hall K.C., Blobel C.P. Interleukin-1 stimulates ADAM17 through a mechanism independent of its cytoplasmic domain or phosphorylation at threonine 735. PLoS One 2012, 7:e31600.
25. Le Gall S.M., Maretzky T., Issuree P.D., Niu X.D., Reiss K., Saftig P., Khokha R., Lundell D., Blobel C.P. ADAM17 is regulated by a rapid and reversible mechanism that controls access to its catalytic site. J. Cell Sci. 2010, 123:3913-3922.
26. Maretzky T., Zhou W., Huang X.Y., Blobel C.P. A transforming Src mutant increases the bioavailability of EGFR ligands via stimulation of the cell-surface metalloproteinase ADAM17. Oncogene 2010, 30:611-618.
27. Reddy P., Slack J.L., Davis R., Cerretti D.P., Kozlosky C.J., Blanton R.A., Shows D., Peschon J.J., Black R.A. Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme. J. Biol. Chem. 2000, 275:14608-14614.
28. Li X., Perez L., Fan H. Inhibitory role of TACE/ADAM17 cytotail in protein ectodomain shedding. World J. Biol. Chem. 2011, 2:246-251.
29. Li X., Perez L., Pan Z., Fan H. The transmembrane domain of TACE regulates protein ectodomain shedding. Cell Res. 2007, 17:985-998.
30. Peiretti F., Canault M., Deprez-Beauclair P., Berthet V., Bonardo B., Juhan-Vague I., Nalbone G. Intracellular maturation and transport of tumor necrosis factor alpha converting enzyme. Exp. Cell Res. 2003, 285:278-285.
31. Li X., Yan Y., Huang W., Yang Y. The study of the inhibition of the recombinant TACE prodomain to endotoxemia in mice. Int. J. Mol. Sci. 2009, 10:5442-5454.
32. Adrain C., Zettl M., Christova Y., Taylor N., Freeman M. Tumor necrosis factor signaling requires iRhom2 to promote trafficking and activation of TACE. Science 2012, 335:225-228.
33. McIlwain D.R., Lang P.A., Maretzky T., Hamada K., Ohishi K., Maney S.K., Berger T., Murthy A., Duncan G., Xu H.C., Lang K.S., Haussinger D., Wakeham A., Itie-Youten A., Khokha R., Ohashi P.S., Blobel C.P., Mak T.W. iRhom2 regulation of TACE controls TNF-mediated protection against Listeria and responses to LPS. Science 2012, 335:229-232.
34. Waetzig G.H., Rosenstiel P., Arlt A., Till A., Brautigam K., Schafer H., Rose-John S., Seegert D., Schreiber S. Soluble tumor necrosis factor (TNF) receptor-1 induces apoptosis via reverse TNF signaling and autocrine transforming growth factor-beta1. FASEB J. 2005, 19:91-93.
35. Waetzig G.H., Rosenstiel P., Nikolaus S., Seegert D., Schreiber S. Differential p38 mitogen-activated protein kinase target phosphorylation in responders and nonresponders to infliximab. Gastroenterology 2003, 125:633-634. (author reply 635-636).
36. Waetzig G.H., Seegert D., Rosenstiel P., Nikolaus S., Schreiber S. p38 mitogen-activated protein kinase is activated and linked to TNF-alpha signaling in inflammatory bowel disease. J. Immunol. 2002, 168:5342-5351.
37. Watts A.D., Hunt N.H., Wanigasekara Y., Bloomfield G., Wallach D., Roufogalis B.D., Chaudhri G. A casein kinase I motif present in the cytoplasmic domain of members of the tumour necrosis factor ligand family is implicated in 'reverse signalling'. EMBO J. 1999, 18:2119-2126.
38. Cassonnet P., Rolloy C., Neveu G., Vidalain P.O., Chantier T., Pellet J., Jones L., Muller M., Demeret C., Gaud G., Vuillier F., Lotteau V., Tangy F., Favre M., Jacob Y. Benchmarking a luciferase complementation assay for detecting protein complexes. Nat. Methods 2011, 8:990-992.
39. Trimble R.B., Tarentino A.L. Identification of distinct endoglycosidase (endo) activities in Flavobacterium meningosepticum: endo F1, endo F2, and endo F3. Endo F1 and endo H hydrolyze only high mannose and hybrid glycans. J. Biol. Chem. 1991, 266:1646-1651.
40. Sherry B., Jue D.M., Zentella A., Cerami A. Characterization of high molecular weight glycosylated forms of murine tumor necrosis factor. Biochem. Biophys. Res. Commun. 1990, 173:1072-1078.
41. Garbers C., Janner N., Chalaris A., Moss M.L., Floss D.M., Meyer D., Koch-Nolte F., Rose-John S., Scheller J. Species specificity of ADAM10 and ADAM17 proteins in interleukin-6 (IL-6) trans-signaling and novel role of ADAM10 in inducible IL-6 receptor shedding. J. Biol. Chem. 2011, 286:14804-14811.
42. Hundhausen C., Misztela D., Berkhout T.A., Broadway N., Saftig P., Reiss K., Hartmann D., Fahrenholz F., Postina R., Matthews V., Kallen K.J., Rose-John S., Ludwig A. The disintegrin-like metalloproteinase ADAM10 is involved in constitutive cleavage of CX3CL1 (fractalkine) and regulates CX3CL1-mediated cell-cell adhesion. Blood 2003, 102:1186-1195.
43. Hundhausen C., Schulte A., Schulz B., Andrzejewski M.G., Schwarz N., von Hundelshausen P., Winter U., Paliga K., Reiss K., Saftig P., Weber C., Ludwig A. Regulated shedding of transmembrane chemokines by the disintegrin and metalloproteinase 10 facilitates detachment of adherent leukocytes. J. Immunol. 2007, 178:8064-8072.
44. Rose-John S. ADAM17, shedding, TACE as therapeutic targets. Pharmacol. Res. 2013, 71C:19-22.
45. Yu M., Lam J., Rada B., Leto T.L., Levine S.J. Double-stranded RNA induces shedding of the 34-kDa soluble TNFR1 from human airway epithelial cells via TLR3-TRIF-RIP1-dependent signaling: roles for dual oxidase 2- and caspase-dependent pathways. J. Immunol. 2011, 186:1180-1188.
46. Kyriakis J.M., Avruch J. Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol. Rev. 2012, 92:689-737.
47. Obata T., Brown G.E., Yaffe M.B. MAP kinase pathways activated by stress: the p38 MAPK pathway. Crit. Care Med. 2000, 28:N67-N77.
48. Leitges M., Plomann M., Standaert M.L., Bandyopadhyay G., Sajan M.P., Kanoh Y., Farese R.V. Knockout of PKC alpha enhances insulin signaling through PI3K. Mol. Endocrinol. 2002, 16:847-858.
49. Adams R.H., Porras A., Alonso G., Jones M., Vintersten K., Panelli S., Valladares A., Perez L., Klein R., Nebreda A.R. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell 2000, 6:109-116.
50. Marcello E., Gardoni F., Di Luca M., Perez-Otano I. An arginine stretch limits ADAM10 exit from the endoplasmic reticulum. J. Biol. Chem. 2010, 285:10376-10384.
51. Cao Y., Kang Q., Zhao Z., Zolkiewska A. Intracellular processing of metalloprotease disintegrin ADAM12. J. Biol. Chem. 2002, 277:26403-26411.
52. Godde N.J., D'Abaco G.M., Paradiso L., Novak U. Efficient ADAM22 surface expression is mediated by phosphorylation-dependent interaction with 14-3-3 protein family members. J. Cell Sci. 2006, 119:3296-3305.
53. Diaz-Rodriguez E., Montero J.C., Esparis-Ogando A., Yuste L., Pandiella A. Extracellular signal-regulated kinase phosphorylates tumor necrosis factor alpha-converting enzyme at threonine 735: a potential role in regulated shedding. Mol. Biol. Cell 2002, 13:2031-2044.
54. Nakagawa M., Nabeshima K., Asano S., Hamasaki M., Uesugi N., Tani H., Yamashita Y., Iwasaki H. Up-regulated expression of ADAM17 in gastrointestinal stromal tumors: coexpression with EGFR and EGFR ligands. Cancer Sci. 2009, 100:654-662.
55. Yu C.C., Tsai L.L., Wang M.L., Yu C.H., Lo W.L., Chang Y.C., Chiou G.Y., Chou M.Y., Chiou S.H. miR145 targets the SOX9/ADAM17 axis to inhibit tumor initiating cells and IL-6-mediated paracrine effects in head and neck cancer. Cancer Res. 2013, 73:3425-3440.
56. Trad A., Hansen H.P., Shomali M., Peipp M., Klausz K., Hedemann N., Yamamoto K., Mauermann A., Desel C., Lorenzen I., Lemke H., Rose-John S., Grotzinger J. ADAM17-overexpressing breast cancer cells selectively targeted by antibody-toxin conjugates. Cancer Immunol. Immunother. 2013, 62:411-421.
57. Yamamoto K., Trad A., Baumgart A., Huske L., Lorenzen I., Chalaris A., Grotzinger J., Dechow T., Scheller J., Rose-John S. A novel bispecific single-chain antibody for ADAM17 and CD3 induces T-cell-mediated lysis of prostate cancer cells. Biochem. J. 2012, 445:135-144.
58. Yoda M., Kimura T., Tohmonda T., Morioka H., Matsumoto M., Okada Y., Toyama Y., Horiuchi K. Systemic overexpression of TNFalpha-converting enzyme does not lead to enhanced shedding activity in vivo. PLoS One 2013, 8:e54412.
59. Lorenzen I., Trad A., Grotzinger J. Multimerisation of A Disintegrin And Metalloprotease protein-17 (ADAM17) is mediated by its EGF-like domain. Biochem. Biophys. Res. Commun. 2011, 415:330-336.
60. Dusterhoft S., Jung S., Hung C.W., Tholey A., Sonnichsen F.D., Grotzinger J., Lorenzen I. The membrane-proximal domain of ADAM17 represents the putative molecular switch of its shedding activity operated by protein-disulfide isomerase. J. Am. Chem. Soc. 2013, 135:5776-5781.
61. Willems S.H., Tape C.J., Stanley P.L., Taylor N.A., Mills I.G., Neal D.E., McCafferty J., Murphy G. Thiol isomerases negatively regulate the cellular shedding activity of ADAM17. Biochem. J. 2010, 428:439-450.
62. Wang Y., Herrera A.H., Li Y., Belani K.K., Walcheck B. Regulation of mature ADAM17 by redox agents for L-selectin shedding. J. Immunol. 2009, 182:2449-2457.
63. Le Gall S.M., Bobe P., Reiss K., Horiuchi K., Niu X.D., Lundell D., Gibb D.R., Conrad D., Saftig P., Blobel C.P. ADAMs 10 and 17 represent differentially regulated components of a general shedding machinery for membrane proteins such as transforming growth factor alpha, L-selectin, and tumor necrosis factor alpha. Mol. Biol. Cell 2009, 20:1785-1794.
64. Maretzky T., Le Gall S.M., Worpenberg-Pietruk S., Eder J., Overall C.M., Huang X.Y., Poghosyan Z., Edwards D.R., Blobel C.P. Src stimulates fibroblast growth factor receptor-2 shedding by an ADAM15 splice variant linked to breast cancer. Cancer Res. 2009, 69:4573-4576.
65. Horiuchi K., Le Gall S., Schulte M., Yamaguchi T., Reiss K., Murphy G., Toyama Y., Hartmann D., Saftig P., Blobel C.P. Substrate selectivity of epidermal growth factor-receptor ligand sheddases and their regulation by phorbol esters and calcium influx. Mol. Biol. Cell 2007, 18:176-188.
66. Chalaris A., Rabe B., Paliga K., Lange H., Laskay T., Fielding C.A., Jones S.A., Rose-John S., Scheller J. Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 2007, 110:1748-1755.
67. Matthews V., Schuster B., Schutze S., Bussmeyer I., Ludwig A., Hundhausen C., Sadowski T., Saftig P., Hartmann D., Kallen K.J., Rose-John S. Cellular cholesterol depletion triggers shedding of the human interleukin-6 receptor by ADAM10 and ADAM17 (TACE). J. Biol. Chem. 2003, 278:38829-38839.
68. Milla M.E., Gonzales P.E., Leonard J.D. The TACE zymogen: re-examining the role of the cysteine switch. Cell Biochem. Biophys. 2006, 44:342-348.
69. Jefferson T., Auf dem Keller U., Bellac C., Metz V.V., Broder C., Hedrich J., Ohler A., Maier W., Magdolen V., Sterchi E., Bond J.S., Jayakumar A., Traupe H., Chalaris A., Rose-John S., Pietrzik C.U., Postina R., Overall C.M., Becker-Pauly C. The substrate degradome of meprin metalloproteases reveals an unexpected proteolytic link between meprin beta and ADAM10. Cell Mol. Life Sci. 2013, 70:309-333.