{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T23:03:51Z","timestamp":1768345431070,"version":"3.49.0"},"reference-count":44,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,9,6]],"date-time":"2022-09-06T00:00:00Z","timestamp":1662422400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Fundamental Research Grant Scheme","award":["FP030-2015A"],"award-info":[{"award-number":["FP030-2015A"]}]},{"name":"Fundamental Research Grant Scheme","award":["FP128-2020"],"award-info":[{"award-number":["FP128-2020"]}]},{"name":"Fundamental Research Grant Scheme","award":["GPF012E-2018"],"award-info":[{"award-number":["GPF012E-2018"]}]},{"name":"University Malaya Faculty Research Grant","award":["FP030-2015A"],"award-info":[{"award-number":["FP030-2015A"]}]},{"name":"University Malaya Faculty Research Grant","award":["FP128-2020"],"award-info":[{"award-number":["FP128-2020"]}]},{"name":"University Malaya Faculty Research Grant","award":["GPF012E-2018"],"award-info":[{"award-number":["GPF012E-2018"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: Oral squamous cell carcinoma (OSCC) is the sixth most common malignancy in the world. Transient receptor potential vanilloid 4 (TRPV4) channel has been shown to be involved in angiogenesis in multiple types of tumors. However, not much is known about TRPV4\u2032s involvement in OSCC. Thus, in this study, we investigate the effect of administering a TRPV4 agonist on angiogenesis in OSCC. Materials and Methods: Thirty-six Sprague Dawley (SD) rats were used in this study. 4-nitroquinoline 1-oxide (4NQO) was used to induce OSCC. Cisplatin (an anticancer drug), and GSK1016790A (an agonist for TRPV4) was used in this study. Immunohistochemistry was employed to examine the TRPV4 expression. An RT2 Profiler PCR Array was performed for gene expression analysis of TRPV4, vascular growth factors that correspond directly with angiogenesis, such as angiopoietin (Ang-1 and Ang-2), and tyrosine kinase (Tie-1 and Tie-2) receptors. Tumor vessel maturity was assessed by microvessel density and microvessel-pericyte-coverage index. Results: RT2 profiler PCR array showed significant elevated levels of Ang-1 (2.1-fold change; p &lt; 0.05) and Tie-2 (4.5-fold change; p &lt; 0.05) in OSCC following the administration of a combination of GSK1016790A and cisplatin. Additionally, the combination treatment significantly reduced the microvessel density (p &lt; 0.01) and significantly increased the percentage of microvessels covered with pericytes (p &lt; 0.01) in OSCC. Furthermore, tumor size was significantly reduced (p &lt; 0.05) in rats that received cisplatin alone. The combination treatment also greatly reduced the tumor size; however, the data were not statistically significant. Conclusions: The findings suggest that combining a TRPV4 agonist with cisplatin for treatment of OSCC promote vessels normalization via modulation of Ang-1\/Tie-2 pathway.<\/jats:p>","DOI":"10.3390\/medicina58091229","type":"journal-article","created":{"date-parts":[[2022,9,6]],"date-time":"2022-09-06T22:33:01Z","timestamp":1662503581000},"page":"1229","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Combination Treatment of TRPV4 Agonist with Cisplatin Promotes Vessel Normalization in an Animal Model of Oral Squamous Cell Carcinoma"],"prefix":"10.3390","volume":"58","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2991-8504","authenticated-orcid":false,"given":"Farhana","family":"Yahya","sequence":"first","affiliation":[{"name":"Department of Oral and Craniofacial Sciences, Faculty of Dentistry, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marina","family":"Mohd Bakri","sequence":"additional","affiliation":[{"name":"Department of Oral and Craniofacial Sciences, Faculty of Dentistry, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6621-8737","authenticated-orcid":false,"given":"Mohammad","family":"Hossain","sequence":"additional","affiliation":[{"name":"Department of Oral Physiology, School of Dentistry, Matsumoto Dental University, 1780 Gobara Hirooka, Shiojiri, Nagano 399-0781, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Syarifah","family":"Syed Abdul Rahman","sequence":"additional","affiliation":[{"name":"Department of Oral and Craniofacial Sciences, Faculty of Dentistry, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aied","family":"Mohammed Alabsi","sequence":"additional","affiliation":[{"name":"Department of Oral Biology and Biomedical Sciences, Faculty of Dentistry, MAHSA University, Jenjarom 42610, Malaysia"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6496-7139","authenticated-orcid":false,"given":"Anand","family":"Ramanathan","sequence":"additional","affiliation":[{"name":"Department of Oral and Maxillofacial Clinical Sciences, Universiti Malaya, Kuala Lumpur 50603, Malaysia"},{"name":"Oral Cancer Research and Coordinating Center, Universiti Malaya, Kuala Lumpur 50603, Malaysia"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1007\/s10147-014-0689-z","article-title":"Current status of oral cancer treatment strategies: Surgical treatments for oral squamous cell carcinoma","volume":"19","author":"Omura","year":"2014","journal-title":"Int. J. Clin. Oncol."},{"key":"ref_2","first-page":"1884","article-title":"Essentials of oral cancer","volume":"8","author":"Rivera","year":"2015","journal-title":"Int. J. Clin. Exp. Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1215\/S1152851705000232","article-title":"The role of pericytes in blood-vessel formation and maintenance","volume":"7","author":"Bergers","year":"2005","journal-title":"Neuro. Oncol."},{"key":"ref_4","unstructured":"Bergers, G. (2008). Angiogenesis: An Integrative Approach from Science to Medicine, Springer."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.job.2016.05.003","article-title":"Endothelial cell transplantation in tumors restores normal vasculature, reduces tumor hypoxia, and suppresses tumor outgrowth","volume":"58","author":"Kitahara","year":"2016","journal-title":"J. Oral Biosci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"3967","DOI":"10.1158\/0008-5472.CAN-05-4536","article-title":"Antiangiogenesis and drug delivery to tumors: Bench to bedside and back","volume":"66","author":"Duda","year":"2006","journal-title":"Cancer Res."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"7144","DOI":"10.1158\/0008-5472.CAN-13-1989","article-title":"Benefits of vascular normalization are dose and time dependent\u2014Letter","volume":"73","author":"Huang","year":"2013","journal-title":"Cancer Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"27903","DOI":"10.1038\/srep27903","article-title":"TRPV4 regulates breast cancer cell extravasation, stiffness and actin cortex","volume":"6","author":"Lee","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1248\/bpbreports.3.1_50","article-title":"Involvement of TRPV1 and TRPV4 Channels in Enhancement of Metastatic Ability Induced by \u03b3-Irradiation in Human Lung Cancer A549 Cells","volume":"3","author":"Washiya","year":"2020","journal-title":"BPB Rep."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1038\/s41419-019-1700-4","article-title":"Activation of PTEN by inhibition of TRPV4 suppresses colon cancer development","volume":"10","author":"Liu","year":"2019","journal-title":"Cell Death Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1038\/s41419-020-03181-7","article-title":"Calcium and TRPV4 promote metastasis by regulating cytoskeleton through the RhoA\/ROCK1 pathway in endometrial cancer","volume":"11","author":"Li","year":"2020","journal-title":"Cell Death Dis."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3946","DOI":"10.1038\/s41388-019-0709-6","article-title":"VPAC1 couples with TRPV4 channel to promote calcium-dependent gastric cancer progression via a novel autocrine mechanism","volume":"38","author":"Tang","year":"2019","journal-title":"Oncogene"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.3389\/fimmu.2017.01325","article-title":"Inhibition of pro-inflammatory and anti-apoptotic biomarkers during experimental oral cancer chemoprevention by dietary black raspberries","volume":"8","author":"Oghumu","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"101","DOI":"10.21315\/mjms2017.24.5.11","article-title":"Sample size calculation in animal studies using resource equation approach","volume":"24","author":"Arifin","year":"2017","journal-title":"Malays. J. Med. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1007\/BF00300234","article-title":"Determination of subcutaneous tumor size in athymic (nude) mice","volume":"24","author":"Tomayko","year":"1989","journal-title":"Cancer Chemother. Pharmacol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Wali, R.K., Kunte, D.P., De La Cruz, M., Tiwari, A.K., Brasky, J., Weber, C.R., Wali, R.K., Kunte, D.P., De La Cruz, M., and Tiwari, A.K. (2012). Topical Polyethylene Glycol as a Novel Chemopreventive Agent for Oral Cancer via Targeting of Epidermal Growth Factor Response. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0038047"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1038\/onc.2015.83","article-title":"Activation of mechanosensitive ion channel TRPV4 normalizes tumor vasculature and improves cancer therapy","volume":"35","author":"Adapala","year":"2016","journal-title":"Oncogene"},{"key":"ref_18","first-page":"210","article-title":"Comparison of HSCORE assessment of endometrial \u03b23 integrin subunit expression with digital HSCORE using computerized image analysis (ImageJ)","volume":"35","author":"Fuhrich","year":"2013","journal-title":"Anal. Quant. Cytopathol. Histopathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1159\/000087840","article-title":"Absence of Smooth Muscle Actin-Positive Pericyte Coverage of Tumor Vessels Correlates with Hematogenous Metastasis and Prognosis of Colorectal Cancer Patients","volume":"69","author":"Yonenaga","year":"2005","journal-title":"Oncology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"432","DOI":"10.1124\/jpet.108.139295","article-title":"N-((1S)-1-{[4-((2S)-2-{[(2,4-dichlorophenyl)sulfonyl]amino}-3-hydroxypropanoyl)-1-piperazinyl]carbonyl}-3-methylbutyl)-1-benzothiophene-2- carboxamide (GSK1016790A), a novel and potent transient receptor potential vanilloid 4 channel agonist induces urinary bladder contraction and hyperactivity: Part I [S]","volume":"326","author":"Thorneloe","year":"2008","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1038\/s41374-019-0357-z","article-title":"The TRPV4-AKT axis promotes oral squamous cell carcinoma cell proliferation via CaMKII activation","volume":"100","author":"Fujii","year":"2020","journal-title":"Lab. Investig."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Sakakibara, A., Sakakibara, S., Kusumoto, J., Takeda, D., Hasegawa, T., Akashi, M., Minamikawa, T., Hashikawa, K., Terashi, H., and Komori, T. (2017). Upregulated Expression of Transient Receptor Potential Cation Channel Subfamily V Receptors in Mucosae of Patients with Oral Squamous Cell Carcinoma and Patients with a History of Alcohol Consumption or Smoking. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0169723"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"16106","DOI":"10.1038\/ncomms16106","article-title":"Pericyte-expressed Tie2 controls angiogenesis and vessel maturation","volume":"8","author":"Teichert","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3317","DOI":"10.1242\/dev.01888","article-title":"Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period","volume":"132","author":"Thurston","year":"2005","journal-title":"Development"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"460","DOI":"10.1038\/74725","article-title":"Angiopoietin-1 protects the adult vasculature against plasma leakage","volume":"6","author":"Thurston","year":"2000","journal-title":"Nat. Med."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1016\/S0002-9440(10)62565-5","article-title":"Activation of the Tie2 receptor by angiopoietin-1 enhances tumor vessel maturation and impairs sauamous cell carcinoma growth","volume":"160","author":"Hawighorst","year":"2002","journal-title":"Am. J. Pathol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"a006650","DOI":"10.1101\/cshperspect.a006650","article-title":"The complex role of angiopoietin-2 in the angiopoietin-Tie signaling pathway","volume":"2","author":"Thurston","year":"2012","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1038\/nrd.2016.278","article-title":"Therapeutic targeting of the angiopoietin\u2013TIE pathway","volume":"16","author":"Saharinen","year":"2017","journal-title":"Nat. Rev. Drug Discov."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1126\/science.277.5322.48","article-title":"Signaling vascular morphogenesis and maintenance","volume":"277","author":"Hanahan","year":"1997","journal-title":"Science"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"5356","DOI":"10.1038\/sj.onc.1203035","article-title":"New model of tumor angiogenesis: Dynamic balance between vessel regression and growth mediated by angiopoietins and VEGF","volume":"18","author":"Holash","year":"1999","journal-title":"Oncogene"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1158\/1535-7163.MCT-09-0554","article-title":"A human monoclonal anti-ANG2 antibody leads to broad antitumor activity in combination with VEGF inhibitors and chemotherapy agents in preclinical models","volume":"9","author":"Brown","year":"2010","journal-title":"Mol. Cancer Ther."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2159","DOI":"10.2353\/ajpath.2009.090391","article-title":"Contrasting actions of selective inhibitors of angiopoietin-1 and angiopoietin-2 on the normalization of tumor blood vessels","volume":"175","author":"Hashizume","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2213","DOI":"10.1158\/0008-5472.CAN-09-1977","article-title":"Complementary actions of inhibitors of angiopoietin-2 and VEGF on tumor angiogenesis and growth","volume":"70","author":"Hashizume","year":"2010","journal-title":"Cancer Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1038\/ncb1715","article-title":"Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts","volume":"10","author":"Saharinen","year":"2008","journal-title":"Nat. Cell Biol."},{"key":"ref_35","first-page":"1388","article-title":"Heterogeneity of angiogenesis and blood vessel maturation in human tumors: Implications for antiangiogenic tumor therapies","volume":"60","author":"Eberhard","year":"2000","journal-title":"Cancer Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/pcan.2008.33","article-title":"Pericyte coverage decreases invasion of tumour cells into blood vessels in prostate cancer xenografts","volume":"12","author":"Jennbacken","year":"2009","journal-title":"Prostate Cancer Prostatic Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1172\/JCI25705","article-title":"Pericytes limit tumor cell metastasis","volume":"116","author":"Xian","year":"2006","journal-title":"J. Clin. Investig."},{"key":"ref_38","unstructured":"Mcdonald, D.M. (2008). Angiogenesis: An Integrative Approach from Science to Medicine, Springer."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.oraloncology.2009.04.001","article-title":"Major advances in the knowledge and understanding of the epidemiology, aetiopathogenesis, diagnosis, management and prognosis of oral cancer","volume":"45","author":"Rapidis","year":"2009","journal-title":"Oral Oncol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1016\/j.oraloncology.2009.01.010","article-title":"Current concepts of management in radiotherapy for head and neck squamous-cell cancer","volume":"45","author":"Mazeron","year":"2009","journal-title":"Oral Oncol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"263","DOI":"10.4236\/jct.2012.34037","article-title":"Oral Squamous Cell Carcinoma: Epidemiology, Clinical Presentation and Treatment","volume":"3","author":"Feller","year":"2012","journal-title":"J. Cancer Ther."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/j.ejphar.2014.07.025","article-title":"Cisplatin in cancer therapy: Molecular mechanisms of action","volume":"740","author":"Dasari","year":"2014","journal-title":"Eur. J. Pharmacol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.oraloncology.2008.08.009","article-title":"Seeking alternative biological therapies: The future of targeted molecular treatment","volume":"45","author":"Lorch","year":"2009","journal-title":"Oral Oncol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s12276-018-0202-2","article-title":"Beyond EGFR inhibition: Multilateral combat strategies to stop the progression of head and neck cancer","volume":"51","author":"Byeon","year":"2019","journal-title":"Exp. Mol. Med."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/9\/1229\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:24:02Z","timestamp":1760142242000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/58\/9\/1229"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,6]]},"references-count":44,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["medicina58091229"],"URL":"https:\/\/doi.org\/10.3390\/medicina58091229","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,6]]}}}