Transcutaneous carbon dioxide suppresses epithelial-mesenchymal transition in oral squamous cell carcinoma

International Journal of Oncology

Volumn 48, Issue 4, 2016, Pages 1493-1498

  Iwata, Eiji ^a   Hasegawa, Takumi ^a   Takeda, Daisuke ^a   Ueha, Takeshi ^a   Kawamoto, Teruya ^a   Akisue, Toshihiro ^b   Sakai, Yoshitada ^a   Komori, Takahide ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KOBE UNIVERSITY   (Japan)

Author keywords

epithelial mesenchymal transition; hypoxia; metastatic potential; oral squamous cell carcinoma; transcutaneous CO2

Indexed keywords

CARBON DIOXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NERVE CELL ADHESION MOLECULE; OXYGEN; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; VIMENTIN; HIF1A PROTEIN, HUMAN; TUMOR PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS POTENTIAL; MIDDLE AGED; MOUSE; MOUTH SQUAMOUS CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; BIOSYNTHESIS; CARCINOMA, SQUAMOUS CELL; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; MOUTH NEOPLASMS; PATHOLOGY; PROGNOSIS; TUMOR CELL LINE;

ANIMALS; CARBON DIOXIDE; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MOUTH NEOPLASMS; NEOPLASM PROTEINS; PROGNOSIS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84958951272     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2016.3380     Document Type: Article

References (55)

1. Warnakulasuriya S. Global epidemiology of oral, and oropharyngeal cancer. Oral Oncol. 45: 309-316, 2009.
2. Kume K, Haraguchi M, Hijioka H, Ishida T, Miyawaki A, Nakamura N, and Ozawa M. The transcription factor Snail enhanced the degradation of E-cadherin, and desmoglein 2 in oral squamous cell carcinoma cells. Biochem Biophys Res Commun. 430: 889-894, 2013.
3. Sasahira T, Kirita T, Yamamoto K, Ueda N, Kurihara M, Matsushima S, Bhawal UK, Bosserhoff AK, and Kuniyasu H. Transport, and Golgi organisation protein 1 is a novel tumour progressive factor in oral squamous cell carcinoma. Eur J Cancer. 50: 2142-2151, 2014.
4. Thiery JP, and Sleeman JP. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol. 7: 131-142, 2006.
5. Savagner P. Leaving the neighborhood: Molecular mechanisms involved during epithelial-mesenchymal transition. BioEssays. 23: 912-923, 2001.
6. Voulgari A, and Pintzas A. Epithelial-mesenchymal transition in cancer metastasis: Mechanisms, markers, and strategies to overcome drug resistance in the clinic. Biochim Biophys Acta 1796: 75-90, 2009.
7. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, Donowitz M, Tsichlis PN, and Larue L. The protein kinase Akt induces epithelial mesenchymal transition, and promotes enhanced motility, and invasiveness of squamous cell carcinoma lines. Cancer Res. 63: 2172-2178, 2003.
8. Ikenouchi J, Matsuda M, Furuse M, and Tsukita S. Regulation of tight junctions during the epithelium-mesenchyme transition: Direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci. 116: 1959-1967, 2003.
9. da Silva SD, Morand GB, Alobaid FA, Hier MP, Mlynarek AM, Alaoui-Jamali MA, and Kowalski LP. Epithelial-mesenchymal transition (EMT) markers have prognostic impact in multiple primary oral squamous cell carcinoma. Clin Exp Metastasis. 32: 55-63, 2015.
10. Fan CC, Wang TY, Cheng YA, Jiang SS, Cheng CW, Lee AY, and Kao TY. Expression of E-cadherin, Twist and p53, and their prognostic value in patients with oral squamous cell carcinoma. J Cancer Res Clin Oncol. 139: 1735-1744, 2013.
11. Faleiro-Rodrigues C, Macedo-Pinto I, Pereira D, and Lopes CS. Prognostic value of E-cadherin immunoexpression in patients with primary ovarian carcinomas. Ann Oncol. 15: 1535-1542, 2004.
12. Zhou YN, Xu CP, Han B, Li M, Qiao L, Fang DC, and Yang JM. Expression of E-cadherin, and beta-catenin in gastric carcinoma, and its correlation with the clinicopathological features, and patient survival. World J Gastroenterol. 8: 987-993, 2002.
13. Richmond PJ, Karayiannakis AJ, Nagafuchi A, Kaisary AV, and Pignatelli M. Aberrant E-cadherin, and alpha-catenin expression in prostate cancer: Correlation with patient survival. Cancer Res. 57: 3189-3193, 1997.
14. Bondi J, Bukholm G, Nesland JM, Bakka A, and Bukholm IR. An increase in the number of adhesion proteins with altered expression is associated with an increased risk of cancer death for colon carcinoma patients. Int J Colorectal Dis. 21: 231-237, 2006.
15. Tseng RC, Lee SH, Hsu HS, Chen BH, Tsai WC, Tzao C, and Wang YC. SLIT2 attenuation during lung cancer progression deregulates beta-catenin, and E-cadherin, and associates with poor prognosis. Cancer Res. 70: 543-551, 2010.
16. Li YY, Zhou CX, and Gao Y. Snail regulates the motility of oral cancer cells via RhoA/Cdc42/p-ERM pathway. Biochem Biophys Res Commun. 452: 490-496, 2014.
17. Wushou A, Pan HY, Liu W, Tian Z, Wang LZ, Shali S, and Zhang ZY. Correlation of increased twist with lymph node metastasis in patients with oral squamous cell carcinoma. J Oral Maxillofac Surg. 70: 1473-1479, 2012.
18. Zhao D, Tang XF, Yang K, Liu JY, and Ma XR. Over-expression of integrin-linked kinase correlates with aberrant expression of Snail, E-cadherin, and N-cadherin in oral squamous cell carcinoma: Implications in tumor progression, and metastasis. Clin Exp Metastasis. 29: 957-969, 2012.
19. Zhou J, Tao D, Xu Q, Gao Z, and Tang D. Expression of E-cadherin, and vimentin in oral squamous cell carcinoma. Int J Clin Exp Pathol. 8: 3150-3154, 2015.
20. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, and Vaupel P. Association between tumor hypoxia, and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 56: 4509-4515, 1996.
21. Jing SW, Wang YD, Chen LQ, Sang MX, Zheng MM, Sun GG, Liu Q, Cheng YJ, and Yang CR. Hypoxia suppresses E-cadherin, and enhances matrix metalloproteinase-2 expression favoring esophageal carcinoma migration, and invasion via hypoxia inducible factor-1 alpha activation. Dis Esophagus. 26: 75-83, 2013.
22. Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, and Semenza GL. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A and ZFHX1B. Cancer Res. 66: 2725-2731, 2006.
23. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, Iyer N, LaRusch J, Pak B, Taghavi P, et al. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res. 63: 1138-1143, 2003.
24. Lv L, Yuan J, Huang T, Zhang C, Zhu Z, Wang L, Jiang G, and Zeng F. Stabilization of Snail by HIF-1a, and TNF-A is required for hypoxia-induced invasion in prostate cancer PC3 cells. Mol Biol Rep. 41: 4573-4582, 2014.
25. Wang F, Chang M, Shi Y, Jiang L, Zhao J, Hai L, Sharen G, and Du H. Down-regulation of hypoxia-inducible factor-1 suppresses malignant biological behavior of triple-negative breast cancer cells. Int J Clin Exp Med. 7: 3933-3940, 2014.
26. Wang N, Dong CR, Jiang R, Tang C, Yang L, Jiang QF, Chen GG, and Liu ZM. Overexpression of HIF-1a, metallothionein, and SLUG is associated with high TNM stage, and lymph node metastasis in papillary thyroid carcinoma. Int J Clin Exp Pathol. 7: 322-330, 2013.
27. Takeda D, Hasegawa T, Ueha T, Imai Y, Sakakibara A, Minoda M, Kawamoto T, Minamikawa T, Shibuya Y, Akisue T, et al. Transcutaneous carbon dioxide induces mitochondrial apoptosis, and suppresses metastasis of oral squamous cell carcinoma in vivo. PLoS One. 9: e100530, 2014.
28. Matsui T, Ota T, Ueda Y, Tanino M, and Odashima S. Isolation of a highly metastatic cell line to lymph node in human oral squamous cell carcinoma by orthotopic implantation in nude mice. Oral Oncol. 34: 253-256, 1998.
29. Okada Y, Akisue T, Hara H, Kishimoto K, Kawamoto T, Imabori M, Kishimoto S, Fukase N, Onishi Y, and Kurosaka M. The effect of bevacizumab on tumour growth of malignant fibrous histiocytoma in an animal model. Anticancer Res. 30: 3391-3395, 2010.
30. Jordan RC, and Daley T. Oral squamous cell carcinoma: new in sights. J Can Dent Assoc. 63: 517-518, 521-525, 1997.
31. Christiansen JJ, and Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion, and metastasis. Cancer Res. 66: 8319-8326, 2006.
32. Smith A, Teknos TN, and Pan Q. Epithelial to mesenchymal transition in head, and neck squamous cell carcinoma. Oral Oncol. 49: 287-292, 2013.
33. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, and Nieto MA. Epithelial-mesenchymal transitions: The importance of changing cell state in development, and disease. J Clin Invest. 119: 1438-1449, 2009.
34. Thiery JP, Acloque H, Huang RY, and Nieto MA. Epithelialmesenchymal transitions in development, and disease. Cell. 139: 871-890, 2009.
35. Huber MA, Kraut N, and Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 17: 548-558, 2005.
36. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, and Johnson KR. Cadherin switching. J Cell Sci. 121: 727-735, 2008.
37. Peinado H, Olmeda D, and Cano A. Snail, Zeb, and bHLH factors in tumour progression: An alliance against the epithelial phenotype?. Nat Rev Cancer. 7: 415-428, 2007.
38. Peinado H, Portillo F, and Cano A. Transcriptional regulation of cadherins during development, and carcinogenesis. Int J Dev Biol. 48: 365-375, 2004.
39. Mattijssen V, Peters HM, Schalkwijk L, Manni JJ, van 't Hof-Grootenboer B, de Mulder PH, and Ruiter DJ. E-cadherin expression in head, and neck squamous-cell carcinoma is associated with clinical outcome. Int J Cancer. 55: 580-585, 1993.
40. Thomas PA, Kirschmann DA, Cerhan JR, Folberg R, Seftor EA, Sellers TA, and Hendrix MJ. Association between keratin, and vimentin expression, malignant phenotype and survival in postmenopausal breast cancer patients. Clin Cancer Res. 5: 2698-2703, 1999.
41. Yokoyama K, Kamata N, Hayashi E, Hoteiya T, Ueda N, Fujimoto R, and Nagayama M. Reverse correlation of E-cadherin, and snail expression in oral squamous cell carcinoma cells in vitro. Oral Oncol. 37: 65-71, 2001.
42. Tang CH, and Tsai CC. CCL2 increases MMP-9 expression, and cell motility in human chondrosarcoma cells via the Ras/Raf/ MEK/ERK/NF-?B signaling pathway. Biochem Pharmacol. 83: 335-344, 2012.
43. Barrallo-Gimeno A, and Nieto MA. Evolutionary history of the Snail/Scratch superfamily. Trends Genet. 25: 248-252, 2009.
44. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 3: 155-166, 2002.
45. Parent AE, Newkirk KM, and Kusewitt DF. Slug (Snai2) expression during skin, and hair follicle development. J Invest Dermatol. 130: 1737-1739, 2010.
46. Murray SA, Oram KF, and Gridley T. Multiple functions of Snail family genes during palate development in mice. Development. 134: 1789-1797, 2007.
47. Li G, Satyamoorthy K, and Herlyn M. N-cadherin-mediated intercellular interactions promote survival, and migration of melanoma cells. Cancer Res. 61: 3819-3825, 2001.
48. Vuoriluoto K, Haugen H, Kiviluoto S, Mpindi JP, Nevo J, Gjerdrum C, Tiron C, Lorens JB, and Ivaska J. Vimentin regulates EMT induction by Slug, and oncogenic H-Ras, and migration by governing Axl expression in breast cancer. Oncogene. 30: 1436-1448, 2011.
49. Hashimoto T, Soeno Y, Maeda G, Taya Y, Aoba T, Nasu M, Kawashiri S, and Imai K. Progression of oral squamous cell carcinoma accompanied with reduced E-cadherin expression but not cadherin switch. PLoS One. 7: e47899, 2012.
50. Mandal M, Myers JN, Lippman SM, Johnson FM, Williams MD, Rayala S, Ohshiro K, Rosenthal DI, Weber RS, Gallick GE, et al. Epithelial to mesenchymal transition in head, and neck squamous carcinoma: Association of Src activation with E-cadherin downregulation, vimentin expression and aggressive tumor features. Cancer. 112: 2088-2100, 2008.
51. Zhang S, Zhou X, Wang B, Zhang K, Liu S, Yue K, Zhang L, and Wang X. Loss of VHL expression contributes to epithelialmesenchymal transition in oral squamous cell carcinoma. Oral Oncol. 50: 809-817, 2014.
52. Teppo S, Sundquist E, Vered M, Holappa H, Parkkisenniemi J, Rinaldi T, Lehenkari P, Grenman R, Dayan D, Risteli J, et al. The hypoxic tumor microenvironment regulates invasion of aggressive oral carcinoma cells. Exp Cell Res. 319: 376-389, 2013.
53. Wu XY, Fu ZX, and Wang XH. Effect of hypoxia-inducible factor 1-A on Survivin in colorectal cancer. Mol Med Rep. 3: 409-415, 2010.
54. Zhang Q, Zhang ZF, Rao JY, Sato JD, Brown J, Messadi DV, and Le AD. Treatment with siRNA, and antisense oligonucleotides targeted to HIF-1alpha induced apoptosis in human tongue squamous cell carcinomas. Int J Cancer. 111: 849-857, 2004.
55. Sakai Y, Miwa M, Oe K, Ueha T, Koh A, Niikura T, Iwakura T, Lee SY, Tanaka M, and Kurosaka M. A novel system for transcutaneous application of carbon dioxide causing an 'artificial Bohr effect' in the human body. PLoS One. 6: e24137, 2011.