Endostatin induces proliferation of oral carcinoma cells but its effect on invasion is modified by the tumor microenvironment

Experimental Cell Research

Volumn 336, Issue 1, 2015, Pages 130-140

  Alahuhta, Ilkka ^a,b   Aikio, Mari ^c   Väyrynen, Otto ^a,b   Nurmenniemi, Sini ^a,b   Suojanen, Juho ^d   Teppo, Susanna ^a,b   Pihlajaniemi, Taina ^c   Heljasvaara, Ritva ^c   Salo, Tuula ^a,b,d,e   Nyberg, Pia ^a,b  

^a UNIVERSITY OF OULU   (Finland)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF OULU   (Finland)

^d UNIVERSITY OF HELSINKI   (Finland)

^e UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Endostatin; Extracellular matrix; Organotypic models; Tongue carcinoma; Tumor invasion

Indexed keywords

ENDOSTATIN; RECOMBINANT ENDOSTATIN; ANGIOGENESIS INHIBITOR;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER SIZE; CARCINOGENESIS; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HISTOLOGY; HSC 3 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TONGUE CARCINOMA; TUMOR INVASION; TUMOR MICROENVIRONMENT; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, SQUAMOUS CELL; CELL MOTION; DRUG EFFECTS; DRUG SCREENING; FEMALE; METABOLISM; MYOMA; NEOVASCULARIZATION, PATHOLOGIC; NUDE MOUSE; PATHOLOGY; TONGUE NEOPLASMS; TUMOR CELL CULTURE; UTERINE NEOPLASMS; VASCULARIZATION;

ANGIOGENESIS INHIBITORS; ANIMALS; APOPTOSIS; CARCINOMA, SQUAMOUS CELL; CELL MOVEMENT; CELL PROLIFERATION; ENDOSTATINS; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; MYOFIBROBLASTS; MYOMA; NEOPLASM INVASIVENESS; NEOVASCULARIZATION, PATHOLOGIC; TONGUE NEOPLASMS; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT; UTERINE NEOPLASMS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84943401145     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.06.012     Document Type: Article

References (47)

1. Hillbertz N.S., Hirsch J.M., Jalouli J., Jalouli M.M., Sand L. Viral and molecular aspects of oral cancer. Anticancer. Res. 2012, 32:4201-4212.
2. Bsoul S.A., Huber M.A., Terezhalmy G.T. Squamous cell carcinoma of the oral tissues: a comprehensive review for oral healthcare providers. J. Contemp. Dent. Pract. 2005, 15:1-16.
3. Vasil'ev Iu.M. Tumor cells and their microenvironment. Vopr. Onkol. 1984, 30:96-103.
4. Nyberg P., Xie L., Kalluri R. Endogenous inhibitors of angiogenesis. Cancer Res. 2005, 65:3967-3979.
5. O'Reilly M.S., Boehm T., Shing Y., Fukai N., Vasios G., Lane W.S., Flynn E., Birkhead J.R., Olsen B.R., Folkman J. Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell 1997, 88:277-285.
6. Folkman J. Antiangiogenesis in cancer therapy-endostatin and its mechanisms of action. Exp. Cell Res. 2006, 312:594-607.
7. Nyberg P., Heikkilä P., Sorsa T., Luostarinen J., Heljasvaara R., Stenman U.H., Pihlajaniemi T., Salo T. Endostatin inhibits human tongue carcinoma cell invasion and intravasation and blocks the activation of matrix metalloprotease-2, -9, and -13. J. Biol. Chem. 2003, 278:22404-22411.
8. Wilson R.F., Morse M.A., Pei P., Renner R.J., Schuller D.E., Robertson F.M., Mallery S.R. Endostatin inhibits migration and invasion of head and neck squamous cell carcinoma cells. Anticancer. Res. 2003, 23:1289-1295.
9. Schmidt A., Addicks K., Bloch W. Opposite effects of endostatin on different endothelial cells. Cancer Biol. Ther. 2004, 3:1162-1166.
10. Brideau G., Mäkinen M.J., Elamaa H., Tu H., Nilsson G., Alitalo K., Pihlajaniemi T., Heljasvaara R. Endostatin overexpression inhibits lymphangiogenesis and lymph node metastasis in mice. Cancer Res. 2007, 67:11528-11535.
11. Celik I., Sürücü O., Dietz C., Heymach J.V., Force J., Höschele I., Becker C.M., Folkman J., Kisker O. Therapeutic efficacy of endostatin exhibits a biphasic dose-response curve. Cancer Res. 2005, 65:11044-11050.
12. Rehn M., Veikkola T., Kukk-Valdre E., Nakamura H., Ilmonen M., Lombardo C., Pihlajaniemi T., Alitalo K., Vuori K. Interaction of endostatin with integrins implicated in angiogenesis. Proc. Natl. Acad. Sci. 2001, 98:1024-1029.
13. Yamaguchi N., Anand-Apte B., Lee M., Sasaki T., Fukai N., Shapiro R., Que I., Lowik C., Timpl R., Olsen B.R. Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J. 1999, 18:4414-4423.
14. Ricard-Blum S., Féraud O., Lortat-Jacob H., Rencurosi A., Fukai N., Dkhissi F., Vittet D., Imberty A., Olsen B.R., van der Rest M. Characterization of endostatin binding to heparin and heparan sulfate by surface plasmon resonance and molecular modeling: role of divalent cations. J. Biol. Chem. 2004, 279:2927-2936.
15. Abdollahi A., Hahnfeldt P., Maercker C., Gröne H.J., Debus J., Ansorge W., Folkman J., Hlatky L., Huber P.E. Endostatin's antiangiogenic signaling network. Mol. Cell 2004, 13:649-663.
16. Lee J.H., Isayeva T., Larson M.R., Sawant A., Cha H.R., Chanda D., Chesnokov I.N., Ponnazhagan S. Endostatin: a novel inhibitor of androgen receptor function in prostate cancer. Proc. Natl. Acad. Sci. 2015, 112:1392-1397.
17. Rong B., Yang S., Li W., Zhang W., Ming Z. Systematic review and meta-analysis of Endostar (rh-endostatin) combined with chemotherapy versus chemotherapy alone for treating advanced non-small cell lung cancer. World J. Surg. Oncol. 2012, 24:170.
18. Tse J.C., Kalluri R. Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment. J. Cell Biochem. 2007, 101:816-829.
19. Moutasim K.A., Nystrom M.L., Thomas G.J. Cell migration and invasion assays. Methods Mol. Biol. 2011, 731:333-343.
20. Nurmenniemi S., Sinikumpu T., Alahuhta I., Salo S., Sutinen M., Santala M., Risteli J., Nyberg P., Salo T. A novel organotypic model mimics the tumor microenvironment. Am. J. Pathol. 2009, 175:1281-1291.
21. Teppo S., Sundquist E., Vered M., Holappa H., Parkkisenniemi J., Rinaldi T., Lehenkari P., Grenman R., Dayan D., Risteli J., Salo T., Nyberg P. The hypoxic tumor microenvironment regulates invasion of aggressive oral carcinoma cells. Exp. Cell Res. 2013, 319:376-389.
22. Vilen S.T., Suojanen J., Salas F., Risteli J., Ylipalosaari M., Itkonen O., Koistinen H., Baumann M., Stenman U.H., Sorsa T., Salo T., Nyberg P. Trypsin-2 enhances carcinoma invasion by processing tight junctions and activating ProMT1-MMP. Cancer Investig. 2012, 30:583-592.
23. Bitu C.C., Kauppila J.H., Bufalino A., Nurmenniemi S., Teppo S., Keinänen M., Vilen S.T., Lehenkari P., Nyberg P., Coletta R.D., Salo T. Cathepsin k is present in invasive oral tongue squamous cell carcinoma in vivo and in vitro. PLoS One 2013, 8:70925.
24. Nyberg P., Salo T., Kalluri R. Tumor microenvironment and angiogenesis. Front. Biosci. 2008, 13:6537-6553.
25. Kylmäniemi M., Oikarinen A., Oikarinen K., Salo T. Effects of dexamethasone and cell proliferation on the expression of matrix metalloproteinases in human mucosal normal and malignant cells. J. Dent. Res. 1996, 75:919-926.
26. Dayan D., Salo T., Salo S., Nyberg P., Nurmenniemi S., Costea D.E., Vered M. Molecular crosstalk between cancer cells and tumor microenvironment components suggests potential targets for new therapeutic approaches in mobile tongue cancer. Cancer Med. 2012, 1:128-140.
27. Saarela J., Ylikärppä R., Rehn M., Purmonen S., Pihlajaniemi T. Complete primary structure of two variant forms of human type XVIII collagen and tissue-specific differences in the expression of the corresponding transcripts. Matrix Biol. 1998, 16:319-328.
28. Aikio M., Alahuhta I., Nurmenniemi S., Suojanen J., Palovuori R., Teppo S., Sorsa T., López-Otín C., Pihlajaniemi T., Salo T., Heljasvaara R., Nyberg P. Arresten, a collagen-derived angiogenesis inhibitor, suppresses invasion of squamous cell carcinoma. PLoS One 2012, 7:51044.
29. Bryne M., Koppang H.S., Lilleng R., Kjaerheim A. Malignancy grading of the deep invasive margins of oral squamous cell carcinomas has high prognostic value. J. Pathol. 1992, 166:375-381.
30. Liby K., Neltner B., Mohamet L., Burd C., Ben-Jonathan N. Endostatin expression by MDA-MB-435 breast cancer cells effectively inhibits tumor growth. Cancer Biol. Ther. 2003, 2:48-52.
31. Weigelt B., Peterse J.L., van't Veer L.J. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 2005, 5:591-602.
32. Velde E.A., Reijerkerk A., Brandsma D., Vogten J.M., Wu Y., Kranenburg O., Voest E.E., Gebbink M., Borel Rinkes I.H. Early endostatin treatment inhibits metastatic seeding of murine colorectal cancer cells in the liver and their adhesion to endothelial cells. Br. J. Cancer 2005, 92:729-735.
33. Sudhakar A., Sugimoto H., Changqing Y., Lively J., Zeisberg M., Kalluri R. Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by alpha v beta 3 and alpha 5 beta 1 integrins. Proc. Natl. Acad. Sci. 2003, 100:4766-4771.
34. Sudhakar A., Nyberg P., Keshamouni V.G., Mannam A.P., Li J., Sugimoto H., Cosgrove D., Kalluri R. Human alpha1 type IV collagen NC1 domain exhibits distinct antiangiogenic activity mediated by alpha1beta1 integrin. J. Clin. Investig. 2005, 115:2801-2810.
35. Karumanchi S.A., Jha V., Ramchandran R., Karihaloo A., Tsiokas L., Chan B., Dhanabal M., Hanai J.I., Venkataraman G., Shriver Z., Keiser N., Kalluri R., Zeng H., Mukhopadhyay D., Chen R.L., Lander A.D., Hagihara K., Yamaguchi Y., Sasisekharan R., Cantley L., Sukhatme V.P. Cell surface glypicans are low-affinity endostatin receptors. Mol. Cell 2001, 7:811-822.
36. Faye C., Chautard E., Olsen B.R., Ricard-Blum S. The first draft of the endostatin interaction network. J. Biol. Chem. 2009, 284:22041-22047.
37. Shi H., Huang Y., Zhou H., Song X., Yuan S., Fu Y., Luo Y. Nucleolin is a receptor that mediates antiangiogenic and antitumor activity of endostatin. Blood 2007, 110:2899-2906.
38. Gaggioli C., Hooper S., Hidalgo-Carcedo C., Grosse R., Marshall J.F., Harrington K., Sahai E. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 2007, 12:1392-1400.
39. Vered M., Allon I., Buchner A., Dayan D. Stromal myofibroblasts and malignant transformation in a 4NQO rat tongue carcinogenesis model. Oral Oncol. 2007, 43:999-1006.
40. Özdemir B.C., Pentcheva-Hoang T., Carstens J.L., Zheng X., Wu C.C., Simpson T.R., Laklai H., Sugimoto H., Kahlert C., Novitskiy S.V., De Jesus-Acosta A., Sharma P., Heidari P., Mahmood U., Chin L., Moses H.L., Weaver V.M., Maitra A., Allison J.P., LeBleu V.S., Kalluri R. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 2014, 25:719-734.
41. Väänänen A., Ylipalosaari M., Parikka M., Kainulainen T., Rehn M., Heljasvaara R., Tjäderhane L., Salo T. Collagen XVIII modulation is altered during progression of oral dysplasia and carcinoma. J. Oral Pathol. Med. 2007, 36:35-42.
42. Kulke M.H., Bergsland E.K., Ryan D.P., Enzinger P.C., Lynch T.J., Zhu A.X., Meyerhardt J.A., Heymach J.V., Fogler W.E., Sidor C., Michelini A., Kinsella K., Venook A.P., Fuchs C.S. Phase II study of recombinant human endostatin in patients with advanced neuroendocrine tumors. J. Clin. Oncol. 2006, 24:3555-3561.
43. Reynolds A.R. Potential relevance of bell-shaped and u-shaped dose-responses for the therapeutic targeting of angiogenesis in cancer. Dose Response 2010, 8:253-284.
44. Tjin Tham Sjin R.M., Naspinski J., Birsner A.E., Li C., Chan R., Lo K.M., Gillies S., Zurakowski D., Folkman J., Samulski J., Javaherian K. Endostatin therapy reveals a U-shaped curve for antitumor activity. Cancer Gene Ther. 2006, 13:619-627.
45. Kisker O., Becker C.M., Prox D., Fannon M., D'Amato R., Flynn E., Fogler W.E., Sim B.K., Allred E.N., Pirie-Shepherd S.R., Folkman J. Continuous administration of endostatin by intraperitoneally implanted osmotic pump improves the efficacy and potency of therapy in a mouse xenograft tumor model. Cancer Res. 2001, 61:7669-7674.
46. Capillo M., Mancuso P., Gobbi A., Monestiroli S., Pruneri G., Dell'Agnola C., Martinelli G., Shultz L., Bertolini F. Continuous infusion of endostatin inhibits differentiation, mobilization, and clonogenic potential of endothelial cell progenitors. Clin. Cancer Res. 2003, 9:377-382.
47. Clamp A.R., Jayson G.C. The clinical potential of antiangiogenic fragments of extracellular matrix proteins. Br. J. Cancer 2005, 93:967-972.