Endostatin and irradiation modifies the activity of ADAM10 and neprilysin in breast cancer cells

Aydemir,Esra  Arslan; Şimşek,Ece; Korcum,Aylin  Fidan; Fişkin,Kayahan

doi:10.3892/mmr.2016.5463

Endostatin and irradiation modifies the activity of ADAM10 and neprilysin in breast cancer cells

Authors:
- Esra Arslan Aydemir
- Ece Şimşek
- Aylin Fidan Korcum
- Kayahan Fişkin
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Affiliations: Department of Biology, Science Faculty, Akdeniz University, Antalya 07058, Turkey, Department of Nutrition and Dietetics, Antalya School of Health, Akdeniz University, Antalya 07058, Turkey, Department of Radiation Oncology, School of Medicine, Akdeniz University, Antalya 07058, Turkey
Published online on: July 1, 2016 https://doi.org/10.3892/mmr.2016.5463
Pages: 2343-2351

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Abstract

Angiogenesis, the formation of new blood vessels, is regarded as a key cancer cell property. Endostatin (ES) is a potential antiangiogenic agent and it may be useful when implemented in combination with other cancer therapeutic strategies. The present study investigated the in vitro effects of ES, radiotherapy (RT) or combination therapy (ES + RT) on two important proteases, a disintegrin and metalloproteinase domain‑containing protein 10 (ADAM10) and neprilysin (NEP) in 4T1 mouse breast cancer cells and the more metastatic phenotype of 4THMpc breast cancer cells. 4T1 and 4THMpc cells were treated with recombinant murine ES (4 µg/ml) alone, RT (45 Gy) alone or with ES + RT. ADAM10 enzyme activity was determined using a tumor necrosis factor‑α converting enzyme (α‑secretase) activity assay kit, and NEP enzyme activity was measured with a fluorometric assay based on the generation of free dansyl‑D‑Ala‑Gly from N-dansyl-Ala-Gly-D-nitro-Phe-Gly, the substrate of NEP. Western blotting analysis was performed to determine whether the altered enzyme activity levels of the two cell lines occurred due to changes in expression level. These data indicate that ES independently potentiates the activity of ADAM10 and NEP enzymes in 4T1 and 4THMpc breast cancer cells.

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1	Hanahan D and Folkman J: Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 86:353–364. 1996. View Article : Google Scholar : PubMed/NCBI
2	Pieraccini S, Saladino G, Sironi M, Francescato P, Cattaneo MG, Vicentini LM, Speranza G and Manitto P: A molecular dynamics study of an endostatin-derived peptide with antiangiogenic activity and of its mutants. Chem Phys Lett. 455:311–315. 2008. View Article : Google Scholar
3	Wang Z, Dabrosin C, Yin X, Fuster MM, Arreola A, Rathmell WK, Generali D, Nagaraju GP, El-Rayes B, Ribatti D, et al: Broad targeting of angiogenesis for cancer prevention and therapy. Semi Cancer Biol. 35(Suppl): S224–S243. 2015. View Article : Google Scholar
4	Shimizu K and Oku N: Cancer anti-angiogenic therapy. Biol Pharm Bull. 27:599–605. 2004. View Article : Google Scholar : PubMed/NCBI
5	O'Reilly MS, Boehm T, Shing Y, Fukai N, Vasios G, Lane WS, Flynn E, Birkhead JR, Olsen BR and Folkman J: Endostatin: An endogenous inhibitor of angiogenesis and tumor growth. Cell. 88:277–285. 1997. View Article : Google Scholar : PubMed/NCBI
6	Zatterstrom UK, Felbor U, Fukai N and Olsen BR: Collagen XVIII/endostatin structure and functional role in angiogenesis. Cell Struct Funct. 25:97–101. 2000. View Article : Google Scholar : PubMed/NCBI
7	Dhanabal M, Ramchandran R, Waterman MJ, Lu H, Knebelmann B, Segal M and Sukhatme VP: Endostatin induces endothelial cell apoptosis. J Biol Chem. 274:11721–11726. 1999. View Article : Google Scholar : PubMed/NCBI
8	Rehn M, Veikkkola T, Kukk-Valdre E, Nakamura H, Ilmonen M, Lombardo C, Pihlajaniemi T, Alitalo K and Vuori K: Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA. 98:1024–1029. 2001. View Article : Google Scholar : PubMed/NCBI
9	Kim YM, Hwang S, Kim YM, Pyunn BJ, Kim TY, Lee ST, Gho YS and Kwon YG: Endostatin blocks vascular endthelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J Biol Chem. 277:27872–27879. 2002. View Article : Google Scholar : PubMed/NCBI
10	Hanai J, Dhanabal M, Karumanchi SA, Albanese C, Waterman M, Chan B, Ramchandran R, Pestell R and Sukhatme VP: Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. J Biol Chem. 277:16464–16469. 2002. View Article : Google Scholar : PubMed/NCBI
11	Kim YM, Jang JW, Lee OH, Yeon J, Choi EY, Kim KW, Lee ST and Kwon YG: Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase. Cancer Res. 60:5410–5413. 2000.PubMed/NCBI
12	Lee SJ, Jang JW, Kim YM, Lee HI, Jeon JY, Kwon YG and Lee ST: Endostatin binds to the catalytic domain of matrix metalloproteinase-2. FEBS Lett. 519:147–152. 2002. View Article : Google Scholar : PubMed/NCBI
13	Foda HD and Zucker S: Matrix metalloproteinases in cancer invasion, metastasis and angiogenesis. Drug Discov Today. 6:478–482. 2001. View Article : Google Scholar : PubMed/NCBI
14	Hellström-Lindahl E, Ravid R and Nordberg A: Age-dependent decline of neprilysin in Alzheimer's disease and normal brain: Inverse correlation with A beta levels. Neurobiol Aging. 29:210–221. 2008. View Article : Google Scholar
15	Bunn PA Jr, Helfrich BA, Brenner DG, Chan DC, Dykes DJ, Cohen AJ and Miller YE: Effects of recombinant neutral endopeptidase (EC 3.4.24.11.) on the growth of lung cancer cell lines in vitro and in vivo. Clin Cancer Res. 4:2849–2858. 1998.PubMed/NCBI
16	Usmani BA, Harden B, Maitland NJ and Turner AJ: Differential expression of neutral endopeptidase-24.11 (neprilysin) and endothelin-converting enzyme in human prostate cancer cell lines. Clin Sci (Lond). 103(Suppl 48): 314S–317S. 2002. View Article : Google Scholar
17	Renneberg H, Albrecht M, Kurek R, Krause E, Lottspeich F, Aumüller G and Wilhelm B: Identification and characterization of neutral endopeptidase (EC 3.4.24.11) from human prostasomes-localization in prostatic tissue and cell lines. Prostate. 46:173–183. 2001. View Article : Google Scholar : PubMed/NCBI
18	Albrecht M, Doroszewicz J, Gillen S, Gomes I, Wilhelm B, Stief T and Aumüller G: Proliferation of prostate cancer cells and activity of neutral endopeptidase is regulated by bombesin and IL-Ibeta with IL-1beta acting as a modulator of cellular differentiation. Prostate. 58:82–94. 2004. View Article : Google Scholar
19	Burns DM, Walker B, Gray J and Nelson J: Breast cancer cell associated endopeptidase EC 24.11 modulates proliferative response to bombesin. Br J Cancer. 79:214–220. 1999. View Article : Google Scholar : PubMed/NCBI
20	Seals DF and Courtneidge SA: The ADAMs family of metalloproteinases: Multidomain proteins with multiple functions. Genes Dev. 17:7–30. 2003. View Article : Google Scholar : PubMed/NCBI
21	Van der Vorst EP, Keijbeck AA, de Winther MP and Donners MM: A disintegrin and metalloproteases: Molecular scissors in angiogenesis, inflammation and atherosclerosis. Atherosclerosis. 224:302–308. 2012. View Article : Google Scholar : PubMed/NCBI
22	Mochizuki S and Okada Y: ADAMs in cancer cell proliferation and progression. Cancer Sci. 98:621–628. 2007. View Article : Google Scholar : PubMed/NCBI
23	Erin N, Zhao W, Bylander J, Chase G and Clawson G: Capsaicin induced inactivation of sensory neurons promotes a more aggressive gene expression phenotype in breast cancer cells. Breast Cancer Res Treat. 99:351–364. 2006. View Article : Google Scholar : PubMed/NCBI
24	Sumner SC, Gallagher KS, Davis DG, Covell DG, Jernigan RL and Ferretti JA: Conformational analysis of the tachykinins in solution: Substance P and physalaemin. J Biomol Struct Dyn. 8:687–707. 1990. View Article : Google Scholar : PubMed/NCBI
25	Kurtz MM, Wang R, Clements MK, Cascieria MA, Austin CP, Cunningham BR, Chicchia GG and Liu Q: Identification, localization and receptor characterization of novel mammalian substance P-like peptides. Gene. 296:205–212. 2002. View Article : Google Scholar : PubMed/NCBI
26	Koon HW and Pothoulakis C: Immunomodulatory properties of substance P: The gastrointestinal system as a model. Ann NY Acad Sci. 1088:23–40. 2006. View Article : Google Scholar : PubMed/NCBI
27	Schäffer M, Beiter T, Becker HD and Hunt TK: Neuropeptides: Mediators of inflammation and tissue repair? Arch Surg. 133:1107–1116. 1998. View Article : Google Scholar : PubMed/NCBI
28	Muangman P, Tamura RN, Muffley LA, Isik FF, Scott JR, Xie C, Kegel G, Sullivan SR, Liang Z and Gibran NS: Substance P enhances wound closure in nitric oxide synthase knockout mice. J Surg Res. 153:201–209. 2009. View Article : Google Scholar :
29	Chappa AK, Audus KL and Lunte SM: Characteristics of substance P transport across the blood-brain barrier. Pharm Res. 23:1201–1208. 2006. View Article : Google Scholar : PubMed/NCBI
30	Esteban F, Gonzalez-Moles MA, Castro D, Martin-Jaen Mdel M, Redondo M, Ruiz-Avila I and Muñoz M: Expression of substance P and neurokinin-1-receptor in laryngeal cancer: Linking chronic inflammation to cancer promotion and progression. Histopathology. 54:258–260. 2009. View Article : Google Scholar : PubMed/NCBI
31	Erin N and Ulusoy O: Differentiation of neuronal from non-neuronal substance P. Regul Pept. 152:108–113. 2009. View Article : Google Scholar
32	Arslan Aydemir E, Simsek Oz E, Fidan Korcum A and Fiskin K: Endostatin enhances radioresponse in breast cancer cells via alteration of substance P levels. Oncol Lett. 2:879–886. 2011.
33	Carpenter TC and Stenmark KR: Hypoxia decreases lung neprilysin express and increases pulmonary vascular leak. Am J Physiol Lung Cell Mol Physiol. 281:L941–L948. 2001.PubMed/NCBI
34	Shichiri M and Hirata Y: Antiangiogenesis signals by endostatin. FASEB J. 15:1044–1053. 2001. View Article : Google Scholar : PubMed/NCBI
35	Kranenburga O, Kroon-Batenburgb LM, Reijerkerka A, Wuc YP, Voesta EE and Gebbinka MF: Recombinant endostatin forms amyloid fibrils that bind and are cytotoxic to murine neuroblastoma cells in vitro. FEBS Lett. 539:149–155. 2003. View Article : Google Scholar
36	Dkhissi F, Lu H, Sorıa C, Opolon P, Griscelli F, Liu H, Khattar P, Mishal Z, Perricaudet M and Li H: Endostatin exhibits a direct antitumor effect in addition to its antiangiogenic activity in colon cancer cells. Hum Gene Ther. 14:997–1008. 2003. View Article : Google Scholar : PubMed/NCBI
37	Hanai J, Gloy J, Karumanchi SA, Kale S, Tang J, Hu G, Chan B, Ramchandran R, Jha V, Sukhatme VP and Sokol S: Endostatin is a potential inhibitor of Wnt signaling. J Cell Biol. 158:529–539. 2002. View Article : Google Scholar : PubMed/NCBI
38	Hajitou A, Grignet C, Devy L, Berndt S, Blacher S, Deroanne CF, Bajou K, Fong T, Chiang Y, Foidart JM and Noël A: The antitumoral effect of endostatin and angiostatin is associated with a down-regulation of vascular endothelial growth factor expression in tumor cells. FASEB J. 16:1802–1804. 2002.PubMed/NCBI
39	Verhoef C, de Wilt JH and Verheul HM: Angiogenesis inhibitors: Perspectives for medical, surgical and radiation oncology. Curr Pharma Design. 12:2623–2630. 2006. View Article : Google Scholar
40	Higgins GS, O'Cathail SM, Muschel RJ and McKenna WG: Drug radiotherapy combinations: Review of previous failures and reasons for future optimism. Cancer Treat Rev. 41:105–113. 2015. View Article : Google Scholar : PubMed/NCBI
41	Teicher BA: A systems approach to cancer therapy. (Antioncogenics + standard cytotoxics→mechanism(s) of interaction). Cancer Metastasis Rev. 15:247–272. 1996. View Article : Google Scholar : PubMed/NCBI
42	Zips D, Krause M, Hessel F, Westphal J, Brüchner K, Eicheler W, Dörfler A, Grenman R, Petersen C, Haberey M and Baumann M: Experimental study on different combination schedules of VEGF-receptor inhibitor PTK787/ZK222584 and fractionated irradiation. Anticancer Res. 23:3869–3876. 2003.PubMed/NCBI
43	Kaliski A, Maggiorella L, Cengel KA, Mathe D, Rouffiac V, Opolon P, Lassau N, Bourhis J and Deutsch E: Angiogenesis and tumor growth inhibition by a matrix metalloproteinase inhibitor targeting radiation-induced invasion. Mol Cancer Ther. 4:1717–1728. 2005. View Article : Google Scholar : PubMed/NCBI
44	Dass CR, Tran TM and Choong PF: Angiogenesis Inhibitors and the need for anti-angiogenic therapeutics. J Dent Res. 86:927–936. 2007. View Article : Google Scholar : PubMed/NCBI
45	Luo W, Sharif TR and Sharif M: Substance P-induced mitogenesis in human astrocytoma cells correlates with activation of the mitogen-activated protein kinase signaling pathway. Cancer Res. 56:4983–4991. 1996.PubMed/NCBI
46	Muñoz M, Pérez A, Rosso M, Zamarriego C and Rosso R: Antitumoral action of the neurokinin-1 receptor antagonist L-733 060 on human melanoma cell lines. Melanoma Res. 14:183–188. 2004. View Article : Google Scholar : PubMed/NCBI
47	Walsh DT, Weg VB, Williams TJ and Nourshargh S: Substance P induced inflammatory responses in guinea-pig skin: The effect of specific NK1 receptor antagonists and the role of endogenous mediators. Br J Pharmacol. 114:1343–1350. 1995. View Article : Google Scholar : PubMed/NCBI
48	Musumecia G, Coleman R, Imbesi R, Magro G, Parenti R, Szychlinska MA, Scuderi R, Cinà CS, Castorina S and Castrogiovanni P: ADAM-10 could mediate cleavage of N-cadherin promoting apoptosis in human atherosclerotic lesions leading to vulnerable plaque: A morphological and immunohistochemical study. Acta Histochem. 116:1148–1158. 2014. View Article : Google Scholar
49	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. View Article : Google Scholar
50	Li B, Yu D and Xu Z: Activated protein C inhibits amyloid β production via promoting expression of ADAM-10. Brain Res. 1545:35–44. 2014. View Article : Google Scholar
51	Jones AV, Lambert DW, Speight PM and Whawell SA: ADAM 10 is over expressed in oral squamous cell carcinoma and contributes to invasive behaviour through a functional association with αvβ6 integrin. FEBS Lett. 587:3529–3534. 2013. View Article : Google Scholar : PubMed/NCBI
52	Şimşek E, Aydemir E, Korcum AF and Fişkin K: Thalidomide combined with irradiation alters the activity of two proteases. Mol Med Rep. 11:1535–1541. 2015.
53	von Lueder TG, Atar D and Kruma H: Current role of neprilysin inhibitors in hypertension and heart failure. Pharmacol Ther. 144:41–49. 2014. View Article : Google Scholar : PubMed/NCBI
54	Bayés-Genís A, Barallat J, Galán A, de Antonio M, Domingo M, Zamora E, Urrutia A and Lupón J: Soluble neprilysin is predictive of cardiovascular death and heart failure hospitalization in heart failure patients. J Am Coll Cardiol. 65:657–665. 2015. View Article : Google Scholar : PubMed/NCBI
55	Cohen AJ, Bunn PA, Franklin W, Magill-Solc C, Hartmann C, Helfrich B, Gilman L, Folkvord J, Helm K and Miller YE: Neutral endopeptidase: Variable expression in human lung, inactivation in lung cancer, and modulation of peptide-induced calcium flux. Cancer Res. 56:831–839. 1996.PubMed/NCBI
56	Göhring B, Holzhausen HJ, Meye A, Heynemann H, Rebmann U, Langner J and Riemann D: Endopeptidase 24.11/CD10 is down-regulated in renal cell cancer. Int J Mol Med. 2:409–414. 1998.PubMed/NCBI
57	Sato Y, Itoh F, Hinoda Y, Ohe Y, Nakagawa N, Ueda R, Yachi A and Imai K: Expression of CD10/neutral endopeptidase in normal and malignant tissues of the human stomach and colon. J Gastroenterol. 31:12–17. 1996. View Article : Google Scholar : PubMed/NCBI
58	Dragović T, Deddish PA, Tan F, Weber G and Erdös EG: Increased expression of neprilysin (neutral endopeptidase 24.11) in rat and human hepatocellular carcinomas. Lab Invest. 70:107–113. 1994.
59	Dragovic T, Sekosan M, Becker RP and Erdös EG: Detection of neutral endopeptidase 24.11 (neprilysin) in human hepatocellular carcinomas by immunocytochemistry. Anticancer Res. 17:3233–3238. 1997.PubMed/NCBI
60	Esteban F, Muñoz M, González-Moles MA and Rosso M: A role for substance P in cancer promotion and progression: A mechanism to counteract intracellular death signals following oncogene activation or DNA damage. Cancer Metastasis Rev. 25:137–145. 2006. View Article : Google Scholar : PubMed/NCBI
61	Langdon S, Sethi T, Ritchie A, Muir M, Smyth J and Rozengurt E: Broad spectrum neuropeptide antagonists inhibit the growth of small celllung cancer in vivo. Cancer Res. 52:4554–4557. 1992.PubMed/NCBI
62	Reeve JG and Bleehen NM: D-Arg¹, D-Phe⁵, D-Trp^7,9, Leu¹¹ substance P induces apoptosis in lung cancer cell lines in vitro. Biochem Biophys Res Commun. 199:1313–1319. 1994. View Article : Google Scholar : PubMed/NCBI
63	Seckl MJ, Higgins T, Widmer F and Rozengurt E: D-Arg¹, D-Trp^5,7,9, Leu¹¹ substance P: A novel potent inhibitor of signal transduction and growth in vitro and in vivo in small cell lung cancer cells. Cancer Res. 57:51–54. 1997.PubMed/NCBI
64	Woll PJ and Rozengurt E: D-Arg¹, D-Phe⁵, D-Trp^7,9, Leu¹¹ substance P, a potent bombesin antagonist in murine Swiss 3T3 cells, inhibits the growth of human small cell lung cancer cells in vitro. Proc Natl Acad Sci USA. 85:1859–1863. 1988. View Article : Google Scholar
65	Palma C, Bigioni M, Irrissuto C, Nardelli F, Maggi CA and Manzini S: Anti-tumour activity of tachykinin NK1 receptor antagonists on human glioma U373 MG xenograft. Br J Cancer. 82:480–487. 2000.PubMed/NCBI
66	Gross K, Karagiannides I, Thomou T, Koon HW, Bowe C, Kim H, Giorgadze N, Tchkonia T, Pirtskhalava T, Kirkland JL and Pothoulakis C: Substance P promotes expansion of human mesenteric preadipocytes through proliferative and antiapoptotic pathways. Am J Physiol Gastrointest Liver Physiol. 296:G1012–G1019. 2009. View Article : Google Scholar : PubMed/NCBI