Senescence-associated release of transmembrane proteins involves proteolytic processing by ADAM17 and microvesicle shedding

FASEB Journal

Volumn 28, Issue 11, 2014, Pages 4847-4856

  Effenberger, Timo ^a   Von Der Heyde, Jan ^a   Bartsch, Kareen ^a   Garbers, Christoph ^a   Schulze Osthoff, Klaus ^b,c   Chalaris, Athena ^a   Murphy, Gillian ^d   Rose John, Stefan ^a   Rabe, Björn ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Exosomes; ICAM 1; P38; SASP; TNFRI

Indexed keywords

AMPHIREGULIN; CELL SURFACE PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR RECEPTOR 1; ADAM PROTEIN; CYTOKINE; SIGNAL PEPTIDE; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE;

ARTICLE; BIOTINYLATION; CELL SURFACE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN SECRETION; SENESCENCE; WESTERN BLOTTING; CELL AGING; CELL CULTURE; METABOLISM; MICROVASCULATURE; PHOSPHORYLATION;

ADAM PROTEINS; CELL AGING; CELLS, CULTURED; CYTOKINES; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROVESSELS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION;

EID: 84912081105     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-254565     Document Type: Article

References (41)

1. Rodier, F., and Campisi, J. (2011) Four faces of cellular senescence. J. Cell Biol. 192, 547-556
2. Shay, J. W., and Roninson, I. B. (2004) Hallmarks of senescence in carcinogenesis and cancer therapy. Oncogene 23, 2919-2933
3. Coppe, J. P., Desprez, P. Y., Krtolica, A., and Campisi, J. (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu. Rev. Pathol. 5, 99-118
4. Kuilman, T., and Peeper, D. S. (2009) Senescence-messaging secretome: SMS-ing cellular stress. Nat. Rev. Cancer 9, 81-94
5. Xue, W., Zender, L., Miething, C., Dickins, R. A., Hernando, E., Krizhanovsky, V., Cordon-Cardo, C., and Lowe, S. W. (2007) Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445, 656-660
6. Ventura, A., Kirsch, D. G., McLaughlin, M. E., Tuveson, D. A., Grimm, J., Lintault, L., Newman, J., Reczek, E. E., Weissleder, R., and Jacks, T. (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445, 661-665
7. Bavik, C., Coleman, I., Dean, J. P., Knudsen, B., Plymate, S., and Nelson, P. S. (2006) The gene expression program of prostate fibroblast senescence modulates neoplastic epithelial cell proliferation through paracrine mechanisms. Cancer Res. 66, 794-802
8. Coppe, J. P., Kauser, K., Campisi, J., and Beausejour, C. M. (2006) Secretion of vascular endothelial growth factor by primary human fibroblasts at senescence. J. Biol. Chem. 281, 29568-29574
9. Coppe, J. P., Patil, C. K., Rodier, F., Sun, Y., Munoz, D. P., Goldstein, J., Nelson, P. S., Desprez, P. Y., and Campisi, J. (2008) Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868
10. Coppe, J. P., Patil, C. K., Rodier, F., Krtolica, A., Beausejour, C. M., Parrinello, S., Hodgson, J. G., Chin, K., Desprez, P. Y., and Campisi, J. (2010) A human-like senescence-associated secretory phenotype is conserved in mouse cells dependent on physiological oxygen. PLoS ONE 5, e9188
11. Kang, M. K., Kameta, A., Shin, K. H., Baluda, M. A., Kim, H. R., and Park, N. H. (2003) Senescence-associated genes in normal human oral keratinocytes. Exp. Cell Res. 287, 272-281
12. Millis, A. J., Hoyle, M., McCue, H. M., and Martini, H. (1992) Differential expression of metalloproteinase and tissue inhibitor of metalloproteinase genes in aged human fibroblasts. Exp. Cell Res. 201, 373-379
13. Lehmann, B. D., Paine, M. S., Brooks, A. M., McCubrey, J. A., Renegar, R. H., Wang, R., and Terrian, D. M. (2008) Senescence- associated exosome release from human prostate cancer cells. Cancer Res. 68, 7864-7871
14. 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., and Cerretti, D. P. (1997) A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729-733
15. 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., and Becherer, J. D. (1997) Cloning of a disintegrin metalloproteinase that processes precursor tumour-necrosis factor- alpha. Nature 385, 733-736
16. Scheller, J., Chalaris, A., Garbers, C., and Rose-John, S. (2011) ADAM17: a molecular switch to control inflammation and tissue regeneration. Trends Immunol. 32, 380-387
17. Kenny, P. A., and Bissell, M. J. (2007) Targeting TACE-dependent EGFR ligand shedding in breast cancer. J. Clin. Invest. 117, 337-345
18. Rodland, K. D., Bollinger, N., Ippolito, D., Opresko, L. K., Coffey, R. J., Zangar, R., and Wiley, H. S. (2008) Multiple mechanisms are responsible for transactivation of the epidermal growth factor receptor in mammary epithelial cells. J. Biol. Chem. 283, 31477-31487
19. Alexander, E., Hildebrand, D. G., Kriebs, A., Obermayer, K., Manz, M., Rothfuss, O., Schulze-Osthoff, K., and Essmann, F. (2013) IkappaBzeta is a regulator of the senescence-associated secretory phenotype in DNA damage- and oncogene-induced senescence. J. Cell Sci. 126, 3738-3745
20. Jorissen, E., Prox, J., Bernreuther, C., Weber, S., Schwanbeck, R., Serneels, L., Snellinx, A., Craessaerts, K., Thathiah, A., Tesseur, I., Bartsch, U., Weskamp, G., Blobel, C. P., Glatzel, M., De Strooper, B., and Saftig, P. (2010) The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J. Neurosci. 30, 4833-4844
21. Trad, A., Hedemann, N., Shomali, M., Pawlak, V., Grotzinger, J., and Lorenzen, I. (2011) Development of sandwich ELISA for detection and quantification of human and murine a disintegrin and metalloproteinase17. J. Immunol. Methods 371, 91-96
22. Yamamoto, K., Trad, A., Baumgart, A., Huske, L., Lorenzen, I., Chalaris, A., Grotzinger, J., Dechow, T., Scheller, J., and Rose- John, S. (2012) A novel bispecific single-chain antibody for ADAM17 and CD3 induces T-cell-mediated lysis of prostate cancer cells. Biochem. J. 445, 135-144
23. Tape, C. J., Willems, S. H., Dombernowsky, S. L., Stanley, P. L., Fogarasi, M., Ouwehand, W., McCafferty, J., and Murphy, G. (2011) Cross-domain inhibition of TACE ectodomain. Proc. Natl. Acad. Sci. U. S. A. 108, 5578-5583
24. Chalaris, A., Rabe, B., Paliga, K., Lange, H., Laskay, T., Fielding, C. A., Jones, S. A., Rose-John, S., and Scheller, J. (2007) Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood 110, 1748-1755
25. Hawari, F. I., Rouhani, F. N., Cui, X., Yu, Z. X., Buckley, C., Kaler, M., and Levine, S. J. (2004) Release of full-length 55-kDa TNF receptor 1 in exosome-like vesicles: a mechanism for generation of soluble cytokine receptors. Proc. Natl. Acad. Sci. U. S. A. 101, 1297-1302
26. Madge, L. A., Sierra-Honigmann, M. R., and Pober, J. S. (1999) Apoptosis-inducing agents cause rapid shedding of tumor necrosis factor receptor 1 (TNFR1). A nonpharmacological explanation for inhibition of TNF-mediated activation. J. Biol. Chem. 274, 13643-13649
27. Walcheck, B., Herrera, A. H., St Hill, C., Mattila, P. E., Whitney, A. R., and Deleo, F. R. (2006) ADAM17 activity during human neutrophil activation and apoptosis. Eur. J. Immunol. 36, 968-976
28. Xu, P., and Derynck, R. (2010) Direct activation of TACEmediated ectodomain shedding by p38 MAP kinase regulates EGF receptor-dependent cell proliferation. Mol. Cell 37, 551-566
29. Soond, S. M., Everson, B., Riches, D. W., and Murphy, G. (2005) ERK-mediated phosphorylation of Thr735 in TNFalpha-converting enzyme and its potential role in TACE protein trafficking. J. Cell Sci. 118, 2371-2380
30. Rodier, F., Coppe, J. P., Patil, C. K., Hoeijmakers, W. A., Munoz, D. P., Raza, S. R., Freund, A., Campeau, E., Davalos, A. R., and Campisi, J. (2009) Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat. Cell Biol. 11, 973-979
31. Freund, A., Patil, C. K., and Campisi, J. (2011) p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 30, 1536-1548
32. Essick, E., Sithu, S., Dean, W., and D'Souza, S. (2008) Pervanadate- induced shedding of the intercellular adhesion molecule (ICAM)-1 ectodomain is mediated by membrane type-1 matrix metalloproteinase (MT1-MMP). Mol. Cell. Biochem. 314, 151-159
33. Tsakadze, N. L., Sithu, S. D., Sen, U., English, W. R., Murphy, G., and D'Souza, S. E. (2006) Tumor necrosis factor-alpha-converting enzyme (TACE/ADAM-17) mediates the ectodomain cleavage of intercellular adhesion molecule-1 (ICAM-1). J. Biol. Chem. 281, 3157-3164
34. Fiore, E., Fusco, C., Romero, P., and Stamenkovic, I. (2002) Matrix metalloproteinase 9 (MMP-9/gelatinase B) proteolytically cleaves ICAM-1 and participates in tumor cell resistance to natural killer cell-mediated cytotoxicity. Oncogene 21, 5213-5223
35. Segura, E., Nicco, C., Lombard, B., Veron, P., Raposo, G., Batteux, F., Amigorena, S., and Thery, C. (2005) ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106, 216-223
36. Freund, A., Orjalo, A. V., Desprez, P. Y., and Campisi, J. (2010) Inflammatory networks during cellular senescence: causes and consequences. Trends Mol. Med. 16, 238-246
37. Salama, R., Sadaie, M., Hoare, M., and Narita, M. (2014) Cellular senescence and its effector programs. Genes Dev. 28, 99-114
38. Garbers, C., Kuck, F., Aparicio-Siegmund, S., Konzak, K., Kessenbrock, M., Sommerfeld, A., Haussinger, D., Lang, P. A., Brenner, D., Mak, T. W., Rose-John, S., Essmann, F., Schulze- Osthoff, K., Piekorz, R. P., and Scheller, J. (2013) Cellular senescence or EGFR signaling induces interleukin 6 (IL-6) receptor expression controlled by mammalian target of rapamycin (mTOR). Cell Cycle 12, 3421-3432
39. Murphy, G. (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat. Rev. Cancer 8, 929-941
40. Cocucci, E., Racchetti, G., and Meldolesi, J. (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol. 19, 43-51
41. Kharaziha, P., Ceder, S., Li, Q., and Panaretakis, T. (2012) Tumor cell-derived exosomes: a message in a bottle. Biochim. Biophys. Acta 1826, 103-111