The disintegrin domain of ADAM17 antagonises fibroblast‑carcinoma cell interactions

Trad,Ahmad; Riese,Michel; Shomali,Mohammad; Hedeman,Nina; Effenberger,Timo; Grötzinger,Joachim; Lorenzen,Inken

doi:10.3892/ijo.2013.1864

The disintegrin domain of ADAM17 antagonises fibroblast‑carcinoma cell interactions

Authors:
- Ahmad Trad
- Michel Riese
- Mohammad Shomali
- Nina Hedeman
- Timo Effenberger
- Joachim Grötzinger
- Inken Lorenzen
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Affiliations: Institute of Biochemistry, Christian-Albrechts University of Kiel, D-24118 Kiel, Germany
Published online on: March 26, 2013 https://doi.org/10.3892/ijo.2013.1864
Pages: 1793-1800

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Abstract

The malignant phenotype of carcinoma cells depends on their ability to invade into their microenvironment promoting metastasis. Therefore, carcinoma cells overexpress many proteins, including A disintegrin and metalloproteases (ADAMs). ADAM17 is expressed by different cancer cell lines and possesses adhesive as well as enzymatic activities. To address the adhesive properties in tumour progression the recombinantly expressed soluble disintegrin domain of ADAM17 was employed. Fibroblasts and carcinoma cells adhere to the immobilized disintegrin domain. Additionally, the soluble disintegrin domain impaired fibroblast-carcinoma cell interactions and increased the shedding activity of ADAM17. Silencing of ADAM17 in fibroblasts or in carcinoma cells decreases cell-cell interaction between these cells. In summary, our results show that the adhesive properties of ADAM17 are mediated by its disintegrin domain and enables carcinoma cells to interact with their microenvironment.

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1.	Brocker CN, Vasiliou V and Nebert DW: Evolutionary divergence and functions of the ADAM and ADAMTS gene families. Hum Genomics. 4:43–55. 2009. View Article : Google Scholar : PubMed/NCBI
2.	White JM: ADAMs: modulators of cell-cell and cell-matrix interactions. Curr Opin Cell Biol. 15:598–606. 2003. View Article : Google Scholar : PubMed/NCBI
3.	Takeda S: Three-dimensional domain architecture of the ADAM family proteinases. Semin Cell Dev Biol. 20:146–152. 2009. View Article : Google Scholar : PubMed/NCBI
4.	Liu H, Shim AH and He X: Structural characterization of the ectodomain of a disintegrin and metalloproteinase-22 (ADAM22), a neural adhesion receptor instead of metalloproteinase: insights on ADAM function. J Biol Chem. 284:29077–29086. 2009. View Article : Google Scholar : PubMed/NCBI
5.	Janes PW, Saha N, Barton WA, et al: Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell. 123:291–304. 2005. View Article : Google Scholar : PubMed/NCBI
6.	Reiss K and Saftig P: The ‘a disintegrin and metalloprotease’ (ADAM) family of sheddases: physiological and cellular functions. Semin Cell Dev Biol. 20:126–137. 2009.
7.	Bax DV, Messent AJ, Tart J, et al: Integrin alpha5beta1 and ADAM-17 interact in vitro and co-localize in migrating HeLa cells. J Biol Chem. 279:22377–22386. 2004. View Article : Google Scholar : PubMed/NCBI
8.	McGinn OJ, English WR, Roberts S, Ager A, Newham P and Murphy G: Modulation of integrin alpha4beta1 by ADAM28 promotes lymphocyte adhesion and transendothelial migration. Cell Biol Int. 35:1043–1053. 2011. View Article : Google Scholar : PubMed/NCBI
9.	Saha A, Backert S, Hammond CE, Gooz M and Smolka AJ: Helicobacter pylori CagL activates ADAM17 to induce repression of the gastric H, K-ATPase alpha subunit. Gastroenterology. 139:239–248. 2010. View Article : Google Scholar
10.	Gooz P, Dang Y, Higashiyama S, Twal WO, Haycraft CJ and Gooz M: A disintegrin and metalloenzyme (ADAM) 17 activation is regulated by alpha5beta1 integrin in kidney mesangial cells. PLoS One. 7:e333502012. View Article : Google Scholar : PubMed/NCBI
11.	Milla ME, Leesnitzer MA, Moss ML, et al: Specific sequence elements are required for the expression of functional tumor necrosis factor-alpha-converting enzyme (TACE). J Biol Chem. 274:30563–30570. 1999. View Article : Google Scholar
12.	Lorenzen I, Trad A and Grötzinger J: Multimerisation of A disintegrin and metalloprotease protein-17 (ADAM17) is mediated by its EGF-like domain. Biochem Biophys Res Commun. 415:330–336. 2011. View Article : Google Scholar : PubMed/NCBI
13.	Reddy P, Slack JL, Davis R, et al: Functional analysis of the domain structure of tumor necrosis factor-alpha converting enzyme. J Biol Chem. 275:14608–14614. 2000. View Article : Google Scholar : PubMed/NCBI
14.	Tape CJ, Willems SH, Dombernowsky SL, et al: Cross-domain inhibition of TACE ectodomain. Proc Natl Acad Sci USA. 108:5578–5583. 2011. View Article : Google Scholar : PubMed/NCBI
15.	Lorenzen I, Lokau J, Düsterhöft S, et al: The membrane-proximal domain of A Disintegrin and Metalloprotease 17 (ADAM17) is responsible for recognition of the interleukin-6 receptor and interleukin-1 receptor II. FEBS Lett. 586:1093–1100. 2012. View Article : Google Scholar : PubMed/NCBI
16.	Smith KM, Gaultier A, Cousin H, Alfandari D, White JM and DeSimone DW: The cysteine-rich domain regulates ADAM protease function in vivo. J Cell Biol. 159:893–902. 2002. View Article : Google Scholar : PubMed/NCBI
17.	Soond SM, Everson B, Riches DW and Murphy G: ERK-mediated phosphorylation of Thr735 in TNFalpha-converting enzyme and its potential role in TACE protein trafficking. J Cell Sci. 118:2371–2380. 2005. View Article : Google Scholar : PubMed/NCBI
18.	Edwards DR, Handsley MM and Pennington CJ: The ADAM metalloproteinases. Mol Aspects Med. 29:258–289. 2008. View Article : Google Scholar
19.	Kommaddi RP, Thomas R, Ceni C, Daigneault K and Barker PA: Trk-dependent ADAM17 activation facilitates neurotrophin survival signaling. FASEB J. 25:2061–2070. 2011. View Article : Google Scholar : PubMed/NCBI
20.	McGowan PM, McKiernan E, Bolster F, et al: ADAM-17 predicts adverse outcome in patients with breast cancer. Ann Oncol. 19:1075–1081. 2008. View Article : Google Scholar : PubMed/NCBI
21.	McGowan PM, Ryan BM, Hill AD, McDermott E, O'Higgins N and Duffy MJ: ADAM-17 expression in breast cancer correlates with variables of tumor progression. Clin Cancer Res. 13:2335–2343. 2007. View Article : Google Scholar : PubMed/NCBI
22.	Tanaka Y, Miyamoto S, Suzuki SO, et al: Clinical significance of heparin-binding epidermal growth factor-like growth factor and a disintegrin and metalloprotease 17 expression in human ovarian cancer. Clin Cancer Res. 11:4783–4792. 2005. View Article : Google Scholar : PubMed/NCBI
23.	Rosso O, Piazza T, Bongarzone I, et al: The ALCAM shedding by the metalloprotease ADAM17/TACE is involved in motility of ovarian carcinoma cells. Mol Cancer Res. 5:1246–1253. 2007. View Article : Google Scholar : PubMed/NCBI
24.	Blanchot-Jossic F, Jarry A, Masson D, et al: Up-regulated expression of ADAM17 in human colon carcinoma: co-expression with EGFR in neoplastic and endothelial cells. J Pathol. 207:156–163. 2005. View Article : Google Scholar : PubMed/NCBI
25.	Dijkstra A, Postma DS, Noordhoek JA, et al: Expression of ADAMs (‘a disintegrin and metalloprotease’) in the human lung. Virchows Arch. 454:441–449. 2009.
26.	Badoual C, Bouchaud G, Agueznay Nel H, et al: The soluble alpha chain of interleukin-15 receptor: a proinflammatory molecule associated with tumor progression in head and neck cancer. Cancer Res. 68:3907–3914. 2008. View Article : Google Scholar : PubMed/NCBI
27.	Zheng X, Jiang F, Katakowski M, Zhang ZG, Lu QE and Chopp M: ADAM17 promotes breast cancer cell malignant phenotype through EGFR-PI3K-AKT activation. Cancer Biol Ther. 8:1045–1054. 2009. View Article : Google Scholar : PubMed/NCBI
28.	Trad A, Hedemann N, Shomali M, Pawlak V, Grotzinger J and Lorenzen I: Development of sandwich ELISA for detection and quantification of human and murine a disintegrin and metalloproteinase 17. J Immunol Methods. 371:91–96. 2011. View Article : Google Scholar : PubMed/NCBI
29.	Trad A, Hansen HP, Shomali M, et al: ADAM17-overexpressing breast cancer cells selectively targeted by antibody-toxin conjugates. Cancer Immunol Immunother. Sep 1–2012, (Epub ahead of print).
30.	Yamamoto K, Trad A, Baumgart A, et al: A novel bispecific single-chain antibody for ADAM17 and CD3 induces T-cell-mediated lysis of prostate cancer cells. Biochem J. 445:135–144. 2012. View Article : Google Scholar : PubMed/NCBI
31.	Zigrino P, Nischt R and Mauch C: The disintegrin-like and cysteine-rich domains of ADAM-9 mediate interactions between melanoma cells and fibroblasts. J Biol Chem. 286:6801–6807. 2011. View Article : Google Scholar : PubMed/NCBI
32.	Chalaris A, Rabe B, Paliga K, et al: Apoptosis is a natural stimulus of IL6R shedding and contributes to the proinflammatory trans-signaling function of neutrophils. Blood. 110:1748–1755. 2007. View Article : Google Scholar : PubMed/NCBI
33.	Jovic M, Naslavsky N, Rapaport D, Horowitz M and Caplan S: EHD1 regulates beta1 integrin endosomal transport: effects on focal adhesions, cell spreading and migration. J Cell Sci. 120:802–814. 2007. View Article : Google Scholar : PubMed/NCBI
34.	Chalaris A, Adam N, Sina C, et al: Critical role of the disintegrin metalloprotease ADAM17 for intestinal inflammation and regeneration in mice. J Exp Med. 207:1617–1624. 2010. View Article : Google Scholar : PubMed/NCBI
35.	Baumgart A, Seidl S, Vlachou P, et al: ADAM17 regulates epidermal growth factor receptor expression through the activation of Notch1 in non-small cell lung cancer. Cancer Res. 70:5368–5378. 2010. View Article : Google Scholar : PubMed/NCBI
36.	Sternlicht MD and Sunnarborg SW: The ADAM17-amphiregulin-EGFR axis in mammary development and cancer. J Mammary Gland Biol Neoplasia. 13:181–194. 2008. View Article : Google Scholar : PubMed/NCBI
37.	Kuramochi H, Nakajima G, Kaneko Y, et al: Amphiregulin and Epiregulin mRNA expression in primary colorectal cancer and corresponding liver metastases. BMC Cancer. 12:882012. View Article : Google Scholar : PubMed/NCBI
38.	Toquet C, Colson A, Jarry A, et al: ADAM15 to alpha5beta1 integrin switch in colon carcinoma cells: A late event in cancer progression associated with tumor dedifferentiation and poor prognosis. Int J Cancer. 130:278–287. 2012. View Article : Google Scholar : PubMed/NCBI
39.	Lucas N and Day ML: The role of the disintegrin metalloproteinase ADAM15 in prostate cancer progression. J Cell Biochem. 106:967–974. 2009. View Article : Google Scholar : PubMed/NCBI
40.	Desiderio UV, Zhu X and Evans JP: ADAM2 interactions with mouse eggs and cell lines expressing alpha4/alpha9 (ITGA4/ITGA9) integrins: implications for integrin-based adhesion and fertilization. PLoS One. 5:e137442010. View Article : Google Scholar : PubMed/NCBI
41.	Kornfeld JW, Meder S, Wohlberg M, et al: Overexpression of TACE and TIMP3 mRNA in head and neck cancer: association with tumour development and progression. Br J Cancer. 104:138–145. 2011. View Article : Google Scholar : PubMed/NCBI
42.	Gooz M: ADAM-17: the enzyme that does it all. Crit Rev Biochem Mol Biol. 45:146–169. 2010. View Article : Google Scholar : PubMed/NCBI
43.	Zheng X, Jiang F, Katakowski M, Lu Y and Chopp M: ADAM17 promotes glioma cell malignant phenotype. Mol Carcinog. 51:150–164. 2012. View Article : Google Scholar : PubMed/NCBI