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Elevated Microrna-145 Inhibits the Development of Oral Squamous Cell Carcinoma Through Inactivating ERK/MAPK Signaling Pathway by Down-Regulating

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Elevated Microrna-145 Inhibits the Development of Oral Squamous Cell Carcinoma Through Inactivating ERK/MAPK Signaling Pathway by Down-Regulating Bioscience Reports (2019) 39 BSR20182214 https://doi.org/10.1042/BSR20182214 Research Article Elevated microRNA-145 inhibits the development of oral squamous cell carcinoma through inactivating ERK/MAPK signaling pathway by down-regulating HOXA1 Downloaded from http://portlandpress.com/bioscirep/article-pdf/39/6/BSR20182214/846268/bsr-2018-2214.pdf by guest on 01 October 2021 Junhai Ding1,*, Dubin Sun2,* and Pengfeng Xie3 1Department of Stomatology, Affiliated Hospital of Jining Medical University, Jining 272100, P.R. China; 2Department of Stomatology, Zoucheng People’s Hospital, Zoucheng 273500, P.R. China; 3Special Functions Section, Jinan Stomatological Hospital, Jinan 250001, P.R. China Correspondence: Pengfeng Xie ([email protected]) Background: Oral cancer is one of the most frequent solid cancers worldwide, and oral squamous cell carcinoma (OSCC) constitutes approximately 90% of oral cancers. The dis- covery of reliable prognostic indicators would be a potential strategy for OSCC treatment. In the present study, we aim to explore the underlying mechanism by which microRNA-145 (miR-145) affected OSCC. Methods: Forty-eight patients diagnosed with OSCC were en- rolled to obtain the OSCC tissues and adjacent normal tissues. The targeting relationship between miR-145 and Homeobox A1 (HOXA1) was verified. In order to assess the effects of miR-145 in OSCC and the detailed regulatory mechanism, the SCC-9 cell line was adopted, in which expression of miR-145 and HOXA1 were altered by transfection. Then, a series of in vitro and in vivo experiments were performed to evaluate the cell viability, migration, in- vasion, and tumor growth. Results: miR-145 was poorly expressed and HOXA1 was highly expressed in OSCC. HOXA1 was verified as a target of miR-145 to mediate the activation of the extracellular signal-regulated kinase/mitogen activated protein kinase (ERK/MAPK) sig- naling pathway. In the circumstance of miR-145 elevation or HOXA1 depletion, the SCC-9 cell line manifested with inhibited cell viability, invasion, and migration in vitro, coupled with reduced tumor growth in vivo, with a decreased expression of ERK/MAPK signaling pathway-related genes/proteins. Conclusion: These findings suggested that miR-145 can inhibit HOXA1 to inactivate the ERK/MAPK signaling pathway, thereby suppressing OSCC cell proliferation, migration, and invasion to further inhibit the development of OSCC, high- lighting a novel therapeutic target for the OSCC treatment. Background *These authors are regarded as Oral squamous cell carcinoma (OSCC) is one of the most common malignancies all over the world and co-first authors. accounts for over 90% of cancers in the oral cavity [1]. Among all the patients with OSCC, approximately Received: 28 November 2018 60% of them suffer from local tumor recurrence and 15–25% of them will develop metastasis [2]. Owing to Revised: 19 April 2019 the lack of understanding of the etiopathogenesis, the survival rate of patients with OSCC in recent 5 years Accepted: 08 May 2019 is disappointing, which is less than 50% [3]. OSCC is known as a complex genetic disorder, and previous studies have demonstrated that several dysregulated genes had connection to the growth of OSCC, but the Accepted Manuscript Online: 28 May 2019 molecular mechanism of OSCC remains to be determined [4,5]. Thereby, new diagnostic and therapeutic Version of Record published: approaches to OSCC may be discovered through a better understanding of the molecular mechanisms, 25 June 2019 which would ultimately contribute to a higher survival rate [6]. © 2019 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution 1 License 4.0 (CC BY). Bioscience Reports (2019) 39 BSR20182214 https://doi.org/10.1042/BSR20182214 Accumulation of multiple genetic and epigenetic alterations is attributed to the progression of oral carcinogenesis, with an activation of oncogenes and an inhibition of suppressor genes [7]. MicroRNAs (miRNAs), are a class of small non-coding RNAs, that can negatively take control of gene function via binding to complementary sequences in the 3 untranslated region (UTR) of mRNAs through translational mechanism [8]. Evidence has shown that miRNAs have an impact on the development and progression of OSCC [9]. MicroRNA-145 (miR-145), a major tumor suppressor, which has been proved to express at a low level in diverse epithelial tumors, including lung and breast cancers [10]. In these cancers, miRNAs were found to exert a role through the regulation of Homeobox A1 (HOXA1) [11,12]. HOXA1, an important member of HOXA family, was found to be highly expressed in several malignant tissues and closely associated with tumor progression and poor prognosis [13]. For instance, HOXA1 was a mammary epithelial oncogene in breast cancer and the oncogenic transformation of immortalized human mammary epithelial cells to aggressive in vivo carcinoma was caused by adequate expression of HOXA1 [14]. The extracellular signal-regulated kinase/mitogen activated protein kinase (ERK/MAPK) signaling pathway has the ability to regulate multiple biologi- Downloaded from http://portlandpress.com/bioscirep/article-pdf/39/6/BSR20182214/846268/bsr-2018-2214.pdf by guest on 01 October 2021 cal processes, such as cell growth, apoptosis, proliferation and invasion [15]. Evidence has indicated that miRNAs can exert an anti-angiogenic effect through regulating expression and activity of the MAPK/ERK signaling pathway [16]. Consistently, in our study, in order to find a therapeutic target for the treatment of OSCC, we proposed a hypothe- sis that miR-145 could hinder OSCC cell invasion and migration and suppress tumor growth through regulation of HOXA1 and the ERK/MAPK signaling pathway. Materials and methods Study subjects From August 2012 to December 2016, 48 resected specimens pathologically confirmed as OSCC were collected from Jinan Stomatological Hospital, among which, 21 cases were highly differentiated, 20 cases were moderately differenti- ated and 7 cases were poorly differentiated or undifferentiated. The patients consisted of 26 males and 22 females with the mean age of 57.5 years (range from 26 to 79 years). There were 15 patients with lymph node metastasis (LNM) and 33 patients without LNM. According to the 2002 TNM classification of International Union Against Cancer (UICC) of oral cancer and oropharyngeal cancer, patients were categorized as 27 cases at stage Ia/Ib and 21 cases at stage IIa/IIb [17]. None of the patients received chemoradiotherapy or other related treatment before the operation. The study was approved by the Institutional Review Board of Jinan Stomatological Hospital (Number 201207003) and written informed consents were obtained from all patients. Cell culture The tongue squamous cell carcinoma SCC-9 cell lines (CRL-1629, ATCC Manassas, VA, U.S.A.) were cultured in Dulbecco’s modified Eagle’s medium/nutrient mixture F12 (DMEM/F12) (Gibco Island, NY, U.S.A.) containing 10% fetal bovine serum (FBS). When cell confluence reached 80–90% (% refers to g:ml), single cell suspension was ob- tained by adding trypsin (Gibco Island, NY, U.S.A.). Then cells were centrifuged at 1500 rpm and washed two times with phosphate buffered solution (PBS; pH = 7.4; 0.27 g KH2PO4; 1.42 g Na2HPO4;8gNaCl,and0.2gKCl;1l PBS was fully dissolved using 800 ml deionized water and added with concentrated hydrochloric acid until the pH reached 7.4 and the final volume of PBS was 1 l). Cells were then resuspended with the addition of 200 μlPBS.The platewasaddedwith100μl anti-human CD44 (Cell Signaling Technology, Danvers, MA, U.S.A., a cell-surface glyco- protein involved in cell–cell interactions, cell adhesion and migration) and cultured for 45 min. After being washed with PBS two times, 200 μl PBS was added to resuspend cells. After CD44 immunofluorescent labeling, cells were categorized using the flow cytometer (FACSCanto II, BD Biosciences San Jose, CA, U.S.A.) and CD44+ tumor cells were recollected for cryopreservation or culture for subsequent experiments. Based on experimental data, cells can also be seeded into culture flasks or Petri dishes with different number of wells. Cell transfection and grouping Cells were allocated into the blank group (without any transfection), the miR-145 mimic group (cells transfected with miR-145 mimics; miR-145 mimic refers to the endogenous miRNAs simulating the organism and is chemically synthesized and could enhance the function of the endogenous miRNAs; it is transfected using the same method as the ordinary nucleic acid), the mimic-negative control (NC) group (cells transfected with NC sequence for miR-145 mimics), the miR-145 inhibitor group (cells transfected with miR-145 inhibitors, chemically modified inhibitors to the specific target miRNA), the inhibitor-NC group (cells transfected with NC sequence for miR-145 inhibitors), the siHOXA1 group (cells transfected with siRNA against HOXA1) and the miR-145 inhibitor + siHOXA1 group (cells transfected with combination of miR-145 inhibitors and siRNA against HOXA1; HOXA1 siRNA was transfected 2 © 2019 The Author(s). This is an open access article published by Portland Press Limited on behalf of the Biochemical Society and distributed under the Creative Commons Attribution License 4.0 (CC BY). Bioscience Reports (2019) 39 BSR20182214 https://doi.org/10.1042/BSR20182214 Table 1 Primer sequences for RT-qPCR Genes Primer sequences miR-145 F: 5-GTCCAGTTTTCCCAGGAATC-3 R: 5-AGAACAGTATTTCCAGGAAT-3 U6 F: 5-CTCGCTTCGGCAGCACA-3 R: 5-AACGCTTCACGAATTTGCGT-3 HOXA1 F: 5-ACCCCTCGGACCATAGGATTAC-3 R: 5-AAGGCGCACTGAAGTTCTGTG-3 ERK F: 5-GGAAGCATTATCTTGACCAG-3 R: 5-CTCTTGTGTGCGTTGAATGT-3 β-actin F: 5-CCAACCGCGAGAAGATGA-3 R: 5-CCAGAGGCGTACAGGGATAG-3 Downloaded from http://portlandpress.com/bioscirep/article-pdf/39/6/BSR20182214/846268/bsr-2018-2214.pdf by guest on 01 October 2021 Abbreviations: F, forward; R, reverse; U6, U6 small nuclear RNA. using the same method as the transfection of nucleic acid: transfection reagent and HOXA1 siRNA were mixed and added to the culture dishes).
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