Analysis of anticancer effect of endostatin on oral squamous cell carcinoma based on results of experimental studies
Keywords:
endostatin, oral squamous cell carcinoma, neoangiogenesis, metastasis
Abstract
The main reason for cancer-associated mortality in patients with oral squamous cell carcinoma is metastatic spread to regional lymph nodes. It is known that the processes of malignant growth and metastasis are highly dependent on blood supply to the primary cancerous focus. The development of malignancy is accompanied by failure of the normally well-balanced system of angiogenesis regulation with prevalence of proangiogenic factors over inhibitors. Therefore, the use of angiogenic inhibitors is a pathophysiologically justified method aimed at suppression of cancer progression. This review presents reports of experimental studies on the role of endostatin, a natural inhibitor of angiogenesis, in processes of tumour shrinkage in squamous cell carcinoma of the maxillofacial region. The authors analysed pathogenic mechanisms of the anticancer effects exhibited by endostatin in preclinical models of oral malignancy. Endostatin can be regarded as a potential antitumor agent for the treatment of oral squamous cell carcinoma.
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References
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31. Hanai J., Dhanabal M., Karumanchi S.A., Albanese C., Waterman M., Chan B. et al. Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. J Biol Chem. 2002; 277(19): 16464-9. doi: 10.1074/jbc.M112274200.
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38. Szafarowski T., Sierdzinski J., Szczepanski M.J., Whiteside T.L., Ludwig N., Krzeski A. Microvessel density in head and neck squamous cell carcinoma. Eur Arch Otorhinolaryngol. 2018; 275(7): 1845-51. doi: 10.1007/s00405-018-4996-2.
39. Mardani M., Tadbir A.A., Ranjbar M.A., Khademi B., Fattahi M.J., Rahbar A. Serum Endostatin Levels in Oral Squamous Cell Carcinoma. Iran J Otorhinolaryngol. 2018; 30(98): 125-30.
40. Nikitakis N.G., Rivera H., Lopes M.A., Siavash H., Reynolds M.A., Ord R.A. at al. Immunohistochemical expression of angiogenesis-related markers in oral squamous cell carcinomas with multiple metastatic lymph nodes. Am J Clin Pathol. 2003; 119(4): 574-86. doi: 10.1309/JD3D-HGCD-GAUN-1R0J.
41. Adhim Z., Lin X., Huang W., Morishita N., Nakamura T., Yasui H. et al. E10A, an adenovirus-carrying endostatin gene, dramatically increased the tumor drug concentration of metronomic chemotherapy with low-dose cisplatin in a xenograft mouse model for head and neck squamous-cell carcinoma. Cancer Gene Ther. 2012; 19(2): 144-52. doi: 10.1038/cgt.2011.79.
42. Wilson R.F., Morse M.A., Pei P., Renner R.J., Schuller D.E., Robertson F.M. et al. Endostatin inhibits migration and invasion of head and neck squamous cell carcinoma cells. Anticancer Res. 2003; 23(2B): 1289-95.
43. Sarode G.S., Sarode S.C., Patil A., Anand R., Patil S.G., Rao R.S. et al. Inflammation and Oral Cancer: An Update Review on Targeted Therapies. J Contemp Dent Pract. 2015; 16(7): 595-602.
44. Nyberg P., Heikkilä P., Sorsa T., Luostarinen J., Heljasvaara R., Stenman U.H. et al. 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(25): 22404-11. doi: 10.1074/jbc.M210325200.
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47. Hebert C., Siavash H., Norris K., Nikitakis N.G., Sauk J.J. Endostatin inhibits nitric oxide and diminishes VEGF and collagen XVIII in squamous carcinoma cells. Int J Cancer. 2005. 114(2): 195-201. doi: 10.1002/ijc.20692.
48. Fukumoto S., Morifuji M., Katakura Y., Ohishi M., Nakamura S. Endostatin inhibits lymph node metastasis by a down-regulation of the vascular endothelial growth factor C expression in tumor cells. Clin Exp Metastasis. 2005; 22(1): 31-8. doi: 10.1007/s10585-005-3973-5.
49. Alahuhta I., Aikio M., Väyrynen O., Nurmenniemi S., Suojanen J., Teppo S. et al. Endostatin induces proliferation of oral carcinoma cells but its effect on invasion is modified by the tumor microenvironment. Exp Cell Res. 2015; 336(1): 130-40. doi: 10.1016/j.yexcr.2015.06.012.
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3. Argiris A., Karamouzis M.V., Raben D., Ferris R.L. Head and neck cancer. Lancet. 2008; 371(9625): 1695-709. doi: 10.1016/S0140-6736(08)60728-X.
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6. Ferris R.L., Xi L., Seethala R.R., Chan J., Desai S., Hoch B., Gooding W. et al. Intraoperative qRT-PCR for detection of lymph node metastasis in head and neck cancer. Clin Cancer Res. 2011; 17(7): 1858-66. doi: 10.1158/1078-0432.CCR-10-3110.
7. Blasco MA, Svider PF, Raza SN, Jacobs JR, Folbe AJ, Saraf P, Eloy JA, Baredes S, Fribley AM. Systemic therapy for head and neck squamous cell carcinoma: Historical perspectives and recent breakthroughs. Laryngoscope. 2017; 127(11): 2565-9. doi: 10.1002/lary.26629.
8. Xing Y., Zhang J., Lin H., Gold K.A., Sturgis E.M., Garden A.S. et al. Relation between the level of lymph node metastasis and survival in locally advanced head and neck squamous cell carcinoma. Cancer. 2016; 122(4): 534-45. doi: 10.1002/cncr.29780.
9. Murakami R., Nakayama H., Semba A., Hiraki A., Nagata M., Kawahara K. et al. Prognostic impact of the level of nodal involvement: Retrospective analysis of patients with advanced oral squamous cell carcinoma. Br J Oral Maxillofac Surg. 2017; 55(1): 50-5. doi: 10.1016/j.bjoms.2016.08.026.
10. Chen C.C., Lin J.C., Chen K.W. Lymph node ratio as a prognostic factor in head and neck cancer patients. Radiat Oncol. 2015; 10: 181. doi: 10.1186/s13014-015-0490-9.
11. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol. 2002; 29(6 Suppl 16): 15-8. Doi: 10.1053/sonc.2002.37263.
12. Folkman J. Tumor angiogenesis. Adv Cancer Res. 1985; 43: 175-203.
13. Folkman J., Kalluri R. Cancer without disease. Nature. 2004; 427(6977): 787. doi: 10.1038/427787a.
14. Jayson G.C., Kerbel R., Ellis L.M., Harris A.L. Antiangiogenic therapy in oncology: current status and future directions. The Lancet. 2016; 388(10043): 518-29. doi: 10.1016/S0140-6736(15)01088-0.
15. Kyzas P.A., Stefanou D., Batistatou A., Agnantis N.J. Prognostic significance of VEGF immunohistochemical expression and tumor angiogenesis in head and neck squamous cell carcinoma. J Cancer Res Clin Oncol. 2005; 131(9): 624-630. doi: 10.1007/s00432-005-0003-6.
16. Seki S., Fujiwara M., Matsuura M., Fujita S., Ikeda H., Asahina I. et al. Prediction of outcome of patients with oral squamous cell carcinoma using vascular invasion and the strongly positive expression of vascular endothelial growth factors. Oral Oncol. 2011; 47(7): 588-93. doi: 10.1016/j.oraloncology.2011.04.013.
17. de Oliveira M.V.M., Gomes É.P.P., Pereira C.S., de Souza L.R., Barros L.O., Mendes D.C. et al. Prognostic value of microvessel density and p53 expression on the locoregional metastasis and survival of the patients with head and neck squamous cell carcinoma. Appl Immunohistochem Mol Morphol. 2013; 21(5): 444-51. doi: 10.1097/PAI.0b013e3182773125.
18. Yamamoto C., Yuasa K., Okamura K., Shiraishi T., Miwa K. Vascularity as assessed by Doppler intraoral ultrasound around the invasion front of tongue cancer is a predictor of pathological grade of malignancy and cervical lymph node metastasis. Dentomaxillofac Radiol. 2016; 45(3): 20150372. doi: 10.1259/dmfr.20150372.
19. Yadav L., Puri N., Rastogi V., Satpute P., Sharma V. Tumour angiogenesis and angiogenic inhibitors: a review. J Clin Diagn Res. 2015; 9(6): XE01- XE05. doi: 10.7860/JCDR/2015/12016.6135.
20. Denaro, N., Russi E.G., Colantonio, I., Adamo, V., Merlano, M.C. The role of antiangiogenic agents in the treatment of head and neck cancer. Oncology. 2012; 83(2): 108-16. doi: 10.1159/000339542.
21. Folkman J. Antiangiogenesis in cancer therapy - endostatin and its mechanisms of action. Exp Cell Res. 2006; 312(5): 594-607. doi: 10.1016/j.yexcr.2005.11.015.
22. Huang X., Wong M.K., Zhao Q., Zhu Z., Wang K.Z., Huang N. et al. Soluble recombinant endostatin purified from Escherichia coli: antiangiogenic activity and antitumor effect. Cancer Res. 2001; 61(2): 478-81.
23. Jin X., Bookstein R., Wills K., Avanzini J., Tsai V., LaFace D. et al. Evaluation of endostatin antiangiogenesis gene therapy in vitro and in vivo. Cancer Gene Ther. 2001; 8(12): 982-9. doi: 10.1038/sj.cgt.7700396.
24. Abdollahi A., Hahnfeldt P., Maercker C., Gröne H.J., Debus J., Ansorge W. et al. Endostatin's antiangiogenic signaling network. Mol Cell. 2004; 13(5): 649-63.
25. Cui R., Ohashi R., Takahashi F., Yoshioka M., Tominaga S., Sasaki S. et. Signal transduction mediated by endostatin directly modulates cellular function of lung cancer cells in vitro. Cancer Sci. 2007; 98(6): 830-7. doi: 10.1111/j.1349-7006.2007.00459.x.
26. Yokoyama Y., Ramakrishnan S. Binding of endostatin to human ovarian cancer cells inhibits cell attachment. Int J Cancer. 2007; 121(11): 2402-9. doi: 10.1002/ijc.22935.
27. Dkhissi F., Lu H., Soria C., Opolon P., Griscelli F., Liu H. et al. Endostatin exhibits a direct antitumor effect in addition to its antiangiogenic activity in colon cancer cells. Hum Gene Ther. 2003; 14(10): 997-1008. doi: 10.1089/104303403766682250.
28. Jia Y., Liu M., Huang W., Wang Z., He Y., Wu J. et al. Recombinant human endostatin endostar inhibits tumor growth and metastasis in a mouse xenograft model of colon cancer. Pathol Oncol Res. 2012; 18(2): 315-23. doi: 10.1007/s12253-011-9447-y.
29. Lee J.H., Isayeva T., Larson M.R., Sawant A., Cha H.R., Chanda D. et al. Endostatin: A novel inhibitor of androgen receptor function in prostate cancer. Proc Natl Acad Sci USA. 2015; 112(5): 1392-7. doi: 10.1073/pnas.1417660112.
30. Dhanabal M., Ramchandran R., Waterman M.J., Lu H., Knebelmann B., Segal M. et al. Endostatin induces endothelial cell apoptosis. J Biol Chem. 1999; 274(17): 11721-6.
31. Hanai J., Dhanabal M., Karumanchi S.A., Albanese C., Waterman M., Chan B. et al. Endostatin causes G1 arrest of endothelial cells through inhibition of cyclin D1. J Biol Chem. 2002; 277(19): 16464-9. doi: 10.1074/jbc.M112274200.
32. Rehn M., Veikkola T., Kukk-Valdre E., Nakamura H., Ilmonen M., Lombardo C.R. et al. Interaction of endostatin with integrins implicated in angiogenesis. Proc Natl Acad Sci USA. 2001; 98(3): 1024-9. doi: 10.1073/pnas.031564998.
33. Wickström S.A., Alitalo K., Keski-Oja J. Endostatin associates with integrin α5β1 and caveolin-1, and activates Src via a tyrosyl phosphatase-dependent pathway in human endothelial cells. Cancer Res. 2002; 62(19): 5580-9.
34. Sudhakar A., Sugimoto H., Yang C., Lively J., Zeisberg M., Kalluri R. Human tumstatin and human endostatin exhibit distinct antiangiogenic activities mediated by αvβ3 and α5β1 integrins. Proc Natl Acad Sci USA. 2003; 100(8): 4766-71. doi: 10.1073/pnas.0730882100.
35. Peng F., Xu Z., Wang J., Chen Y., Li Q., Zuo Y. et al. Recombinant human endostatin normalizes tumor vasculature and enhances radiation response in xenografted human nasopharyngeal carcinoma models. PloS one. 2012; 7(4): e34646. doi: 10.1371/journal.pone.0034646.
36. Walia A., Yang J.F., Huang Y.H., Rosenblatt M.I., Chang J.H., Azar D.T. Endostatin's emerging roles in angiogenesis, lymphangiogenesis, disease, and clinical applications. Biochim Biophys Acta. 2015; 1850(12): 2422-38. doi: 10.1016/j.bbagen.2015.09.007.
37. Jung S., Sielker S., Purcz N., Sproll C., Acil Y., Kleinheinz J. Analysis of angiogenic markers in oral squamous cell carcinoma-gene and protein expression. Head Face Med. 2015; 11: 19. doi: 10.1186/s13005-015-0076-7.
38. Szafarowski T., Sierdzinski J., Szczepanski M.J., Whiteside T.L., Ludwig N., Krzeski A. Microvessel density in head and neck squamous cell carcinoma. Eur Arch Otorhinolaryngol. 2018; 275(7): 1845-51. doi: 10.1007/s00405-018-4996-2.
39. Mardani M., Tadbir A.A., Ranjbar M.A., Khademi B., Fattahi M.J., Rahbar A. Serum Endostatin Levels in Oral Squamous Cell Carcinoma. Iran J Otorhinolaryngol. 2018; 30(98): 125-30.
40. Nikitakis N.G., Rivera H., Lopes M.A., Siavash H., Reynolds M.A., Ord R.A. at al. Immunohistochemical expression of angiogenesis-related markers in oral squamous cell carcinomas with multiple metastatic lymph nodes. Am J Clin Pathol. 2003; 119(4): 574-86. doi: 10.1309/JD3D-HGCD-GAUN-1R0J.
41. Adhim Z., Lin X., Huang W., Morishita N., Nakamura T., Yasui H. et al. E10A, an adenovirus-carrying endostatin gene, dramatically increased the tumor drug concentration of metronomic chemotherapy with low-dose cisplatin in a xenograft mouse model for head and neck squamous-cell carcinoma. Cancer Gene Ther. 2012; 19(2): 144-52. doi: 10.1038/cgt.2011.79.
42. Wilson R.F., Morse M.A., Pei P., Renner R.J., Schuller D.E., Robertson F.M. et al. Endostatin inhibits migration and invasion of head and neck squamous cell carcinoma cells. Anticancer Res. 2003; 23(2B): 1289-95.
43. Sarode G.S., Sarode S.C., Patil A., Anand R., Patil S.G., Rao R.S. et al. Inflammation and Oral Cancer: An Update Review on Targeted Therapies. J Contemp Dent Pract. 2015; 16(7): 595-602.
44. Nyberg P., Heikkilä P., Sorsa T., Luostarinen J., Heljasvaara R., Stenman U.H. et al. 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(25): 22404-11. doi: 10.1074/jbc.M210325200.
45. Kondakova I.V., Klisho E.V., Savenkova O.V., Shishkin D.A., Choynzonov E.L. Pathogenic significance of the matrix metalloproteinase system in squamous cell head and neck cancer. Siberian Journal of Oncology. 2011; 1(43): 29-33. (in Russian)
46. Katayama A., Bandoh N., Kishibe K., Takahara M., Ogino T., Nonaka S. et al. Expressions of matrix metalloproteinases in early-stage oral squamous cell carcinoma as predictive indicators for tumor metastases and prognosis. Clin Cancer Res. 2004; 10(2): 634-40.
47. Hebert C., Siavash H., Norris K., Nikitakis N.G., Sauk J.J. Endostatin inhibits nitric oxide and diminishes VEGF and collagen XVIII in squamous carcinoma cells. Int J Cancer. 2005. 114(2): 195-201. doi: 10.1002/ijc.20692.
48. Fukumoto S., Morifuji M., Katakura Y., Ohishi M., Nakamura S. Endostatin inhibits lymph node metastasis by a down-regulation of the vascular endothelial growth factor C expression in tumor cells. Clin Exp Metastasis. 2005; 22(1): 31-8. doi: 10.1007/s10585-005-3973-5.
49. Alahuhta I., Aikio M., Väyrynen O., Nurmenniemi S., Suojanen J., Teppo S. et al. Endostatin induces proliferation of oral carcinoma cells but its effect on invasion is modified by the tumor microenvironment. Exp Cell Res. 2015; 336(1): 130-40. doi: 10.1016/j.yexcr.2015.06.012.
Published
2020-11-26
How to Cite
Tuguzbaeva G., Pavlov V., Enikeev D. Analysis of anticancer effect of endostatin on oral squamous cell carcinoma based on results of experimental studies // Patologicheskaya Fiziologiya i Eksperimental’naya Terapiya (Pathological physiology and experimental therapy). 2020. VOL. 64. № 4. PP. 134–139.
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Section
Reviews
