Cancer Translational Medicine

Original Research | Open Access

Vol.8 (2022) | Issue-2 | Page No: 63-75

DOI: https://doi-ds.org/doilink/06.2022-29697239/A4

Differential Expression of T-box Transcription Factor TBX19 Regulates the Progression of Hepatocellular Carcinoma

Guifang He1, Yanjiao Hu2, Fuguo Dong3, Changchang Liu1, Duo Cai1, Shihai Liu1*

Affiliations  

1. Medical Animal Laboratory, the Affiliated Hospital of Qingdao University, Qingdao, Shandong, China

2. Department of Pathology, the Affiliated Hospital of Qingdao University, Qingdao, Shandong, China

3. Medical Record Management Center, the Affiliated Hospital of Qingdao University, Qingdao, Shandong, China

Corresponding Author

Address for correspondence: Dr. Shihai Liu, Medical Animal Laboratory, the Affiliated Hospital of Qingdao University, No.1677 Wutaishan Road, Changjiang Road District, Qingdao 266400, Shandong, China. E-mail: shliumed@126.com 


Important Dates  

Date of Submission:   24-Jan-2022

Date of Acceptance:   30-May-2022

Date of Publication:   28-Jun-2022

ABSTRACT

Aim: Hepatocellular carcinoma (HCC) is a leading cause of global cancer-related mortality, the prevalence of which is rising annually. HCC patients exhibit poor prognosis due to a lack of predictive biomarkers associated with the early stages of the disease, underlining the need for more research into the molecular drivers of this malignancy in order to better guide its diagnosis and treatment. The T-box (TBX) transcription factor family encodes a series of regulators of tumor cell development. In light of this, we aim to study the impact of TBX19 on the growth of HCC cells.

Methods: Using the UALCAN database, we conducted a series of bioinformatics analyses assessing the prognostic relevance of TBX19 in HCC and the association between the expression of this gene and patients’ clinicopathological findings. In addition, a series of proliferation, and migration assays were performed to assess the relationship between TBX19 and HCC cell malignancy. Furthermore, the effects of TBX19 overexpression on deoxythymidylate kinase (DTYMK) were evaluated through Western blotting and measurements of deoxyribonucleoside triphosphate (dTTP) levels.

Results: Bioinformatics analysis revealed that the TBX19 overexpression was associated with a poor prognosis in HCC patients. Further, a strong correlation between TBX19 overexpression and the overall survival of patients was observed. Functional assays indicated that TBX19 was able to promote HCC cell proliferation and migration while also regulating DTYMK and DTYMK-related dTTP levels.

Conclusions: Overexpression of TBX19 is associated with poor prognosis in HCC patients. Further, exogenous TBX19 expression could promote the in vitro growth of HCC cells, underscoring the promise of TBX19 as a target for future efforts aimed at diagnosing and treating this cancer type.

Keywords: T-box 19, hepatocellular carcinoma, proliferation, migration, deoxyribonucleoside triphosphate


INTRODUCTION

Primary liver cancers are the sixth and third most common causes of cancer and cancer-related mortality in the world, respectively, with only lung cancer and colorectal cancer being responsible for higher rates of patient death.[1] Hepatocellular carcinoma (HCC) accounts for 75%-85% of all liver cancer cases, and an estimated 900,000 cases of primary liver cancer were diagnosed in 2020 with 800,000 corresponding deaths according to the GLOBOCAN 2020 database.[1] Liver cancer cases in China account for approximately 55% of the total global caseload, underscoring the major threat to public health that this tumor type represents.[2] While there have been major breakthroughs in diagnosing and treating HCC, many patients nonetheless exhibit a poor prognosis attributable to the high rates of recurrence and metastasis associated with this cancer.[3] There is thus an urgent need to further explore the molecular mechanisms governing HCC malignancy and progression in an effort to define more reliable diagnostic tests and therapeutic interventions for affected patients.[4],[5],[6],[7]

The T-box (TBX) transcription factor family consists of a range of regulatory proteins that play essential roles in governing early embryogenesis and other stages of development.[8] TBX abnormalities are commonly observed in a range of heritable human diseases, including TBX1, TBX3, TBX5, and TBX22 mutations in patients with DiGeorge syndrome, Ulnar-Mammary syndrome, Holt-Oram syndrome, and cleft palate with ankyloglossia, respectively.[LinkRef 9-900] Several recent studies have additionally highlighted a potential link between specific TBX genes and certain malignancies.[10] For example, the downstream Wnt/β-catenin signaling targets, TBX2 and TBX3, are commonly overexpressed and mutated in breast and ovarian cancer, respectively, in addition to being associated with malignant melanoma, pancreatic cancer and HCC.[11],[12],[13],[14],[15],[16],[17],[18],[19] The TBX19 transcription factor, which harbors a conserved T-box DNA binding motif, is reportedly expressed at elevated levels in colorectal cancer, pituitary corticotroph tumors, and cells bearing KRAS mutations.[20],[21]

Deoxythymidylate kinase (DTYMK), a nuclear deoxythymidylate kinase, catalyzes the process of deoxy-TMP phosphorylation.[22] This enzyme plays a vital role in DNA synthesis in vivo and is a key intermediate enzyme in many pyrimidine analog drug-related pathways.[23] Previous studies have shown that DTYMK is a probable predictive factor of poor prognosis in non-small cell lung cancer (NSCLC) and may be a potential therapeutic target for the disease. Yeh et. al., mentioned that DTYMK might have relevance to the poor prognosis of HCC patients, but its importance has not yet been evaluated.[24]

The specific clinical relevance and functional importance of TBX19 in individual cancers, however, remain to be fully clarified. In this analysis, we found TBX19 to be overexpressed in HCC patient clinical samples, with the knockdown of this gene being sufficient to suppress the proliferative and migratory activity of HCC cells. Moreover, we found TBX19 to regulate DTYMK, which catalyzes the penultimate step in deoxyribonucleoside triphosphate (dTTP) biosynthesis. Together, the results of this study indicate that TBX19 expression can promote the in vitro growth of HCC cells, underscoring the promise of TBX19 as a target for future efforts aimed at diagnosing and treating liver cancer.


MATERIALS AND METHODS

UALCAN database analyses

The Cancer Genome Atlas (TCGA)-based UALCAN (http://ualcan.path.uab.edu) database,[25] constructed using PERL-CGI, javascript, and CSS, enables online mining analyses. Using this database, we were able to assess the expression of TBX19 in both HCC tumors and control tissues, in addition to examining relative expression levels in different stages of HCC. This database was additionally used to examine the relationship between gene expression and patient prognosis.

Cell culture and reagents

The Huh7, HepG2, and SNU387 liver cancer cell lines and the control LX-2 cell line were obtained from Procell (Wuhan, China) and cultured in DMEM (Gibco, USA) supplemented with 10% fetal bovine serum (FBS) in a 5% CO2 incubator. STR identification was used to validate all cell lines.

Western blotting

RIPA buffer (Beyotime Institute of Biotechnology, China) containing PMSF (1 nM; Invitrogen) was used to lyse cells, after which the levels of protein in the collected extracts were measured via BCA assay (Thermo Fisher Scientific Inc., Waltham, MA). Proteins were then separated via 10% SDS-PAGE and transferred to PVDF membranes (Millipore), which were subsequently probed overnight with anti-TBX19 (1:1500, Abcam, MA, USA), anti-DTYMK (1:1000, Abcam), or anti-GAPDH (1:3000, Abcam). Secondary HRP-conjugated anti-rabbit (1:5000) or anti-mouse (1:5000) IgG (Abcam) were then used to detect protein bands, which were imaged with a Bio-Rad ChemiDoc XRS+ system (Hercules, CA, USA).

Real-time quantitative polymerase chain reaction (qPCR)

An RNeasy Mini Kit (Qiagen, Hilden, Germany) was used to isolate total RNA from cells, after which an iScript cDNA synthesis kit (Bio-Rad Laboratories, CA, USA) was used to prepare cDNA. For qPCR analyses, samples were analyzed using Takara SYBR Premix Ex Taq (Tli RNaseH Plus, Japan) and a real-time qPCR instrument (Mode: FTC-3000P, Funglyn Biotech, Toronto, Canada) with the following thermocycler settings: 94°C for 4 min; 40 cycles of 94°C for 20 s, 60°C for 10 s, and 72°C for 20 s. All primers used in this study are compiled in Table 1, with GAPDH serving as a normalization control. Relative gene expression was measured via the 2-ΔΔCt approach.[26]

Cellular transfection

For overexpression studies, full-length TBX19 cDNA was amplified and cloned into the GV141 vector (Genechem, China). TBX19-specific siRNA constructs (siR1, siR2, and siR3) and a negative control construct (siNC) were obtained from GenePharma Co. (Shanghai, China). Cells were plated into 6-well plates and transfected with appropriate constructs using Lipofectamine 3000 (Invitrogen, USA) based on provided directions, as in prior report.[27] All siRNA sequences are compiled in Table 1.

 

Table 1.
Table 1. Sequences of primers for qPCR and siRNA sequence

 

CCK-8 assay

A Cell Counting Kit-8 (CCK-8, Dojindo, MD, USA) was used based on provided directions to monitor cellular proliferation. Briefly, Huh7 or SNU387 cells (2 × 103 cells/well) were added to 96-well plates and cultured for appropriate periods of time, with absorbance at 450 nm (OD450) recorded every 24 h over a 4-day period.

5-Ethynyl-2'-Deoxyuridine (EdU) uptake assay

A BeyoClick EdU Cell Proliferation Kit with Alexa Fluor 555 (Beyotime, China) was utilized based on provided directions to monitor cell proliferation, as in previous reports.[28] Briefly, cells were rinsed two times using phosphate buffered saline (PBS) prior to incubation for 4 h in an EdU working solution (10 μM) at 37°C while protected from light. Cells were then rinsed two additional times with PBS, fixed for 15 min with 4% paraformaldehyde (PFA), permeabilized for 15 min using 0.1% Triton-X100, and rinsed thrice using PBS. DAPI (4',6-diamidino-2-phenylindole, Boster, China) was then employed to counterstain cells for 5 min, after which they were imaged using a fluorescence microscope (Celenas, Nikon, Tokyo, Japan) at 100× magnification. DAPI (blue) and EdU (red) fluorescence respectively corresponded to DNA replication and nuclei.

Colony formation assay

Cells transfected with appropriate siRNAs or overexpression vectors were plated and incubated at 37°C for 6-9 days, after which media was discarded, cells were washed with PBS, and methanol was used to fix colonies for 30 min followed by crystal violet staining and imaging with a Nikon camera.

Transwell assays

Transwell assays were used to assess cellular migration, as in prior reports.[28] Media supplemented with 20% FBS was added to the lower chamber of each well as a chemoattractant. After a 24 h incubation, non-migratory cells were removed with a cotton swab, while the remaining cells were stained with crystal violet prior to imaging. The mean number of cells in 10 (100×) fields of view were counted to quantify migration. All analyses were performed in duplicate for a minimum of three times.

LinkedOmics analysis

The publicly available LinkedOmics platform (http://www.linkedomics.org/login.php) enables analyses of multiomics datasets from 32 tumor types included in the TCGA database.[29] The LinkedOmics LinkFinder module enables users to search for attributes related to a particular attribute of interest, and was used in this report to identify genes that were differentially expressed in a manner correlated with TBX19 expression in the TCGA liver cancer cohort. Spearman’s correlation coefficients and heat maps, scatter plots, or volcano plots were used to analyze the resultant data. Data were additionally ranked, and transcription factor target enrichment analyses were conducted using GSEA. Rank criteria were as follows: false discovery rate (FDR) < 0.05, with 1,000 replicate simulations performed.

Deoxyribonucleoside triphosphate (dTTP) extraction and quantification

In total, 106 cells were treated with 60% chilled methanol to prepare extracts, which were then immersed in a 100°C dry bath for 3 minutes. Samples were then dried under vacuum, as in prior reports,[28] the remaining residues were then suspended in 80 µl of nuclease-free dH2O. The dTTP levels in these samples were then measured as reported previously.[28]

Statistical analysis

Statistical analysis was performed using SPSS 22.0 (SPSS Inc, NY, USA) and GraphPad Prism 5.0.1 (GraphPad Software, NY, USA). Data are means ± SEM from three or more replicate experiments. Data were compared via two-tailed Student’s t-tests, while survival analyses were conducted using the log-rank test. Correlations between TBX19 and DTYMK were analyzed via Spearman’s test. P < 0.05 was the threshold of significance for this study.


RESULTS

Analysis of TBX19 expression in the UALCAN database

We began by using the UALCAN database to assess TBX19 expression in a range of tumor types, revealing differences between tumors and normal tissues. In 24 tumor samples studied, TBX19 was found upregulated in 15 samples and downregulated in 9 samples. TBX19 expression was found to be elevated in BLCA, CHOL, COAD, ESCA, GBM, HNSC, KIRC, KIRP, LIHC, LUAD, LUSC, PCPG, READ, SARC, and STAD relative to normal tissues, with similar upregulation in other tumors [Supplementary Figure 1].

We further used this database to perform subgroup analyses of LIHC cases, including 371 primary tumors and 50 normal tissues, and found that TBX19 mRNA levels were significantly elevated in primary tumors (P < 1×10-12) [Figure 1A]. In addition, TBX19 levels were significantly increased in stage 3 liver cancer as compared to normal tissue or stage 1/2 liver cancer (normal vs. stage 1, P = 5.83×10-12; normal vs. stage 2, P = 3.94×10-14; normal vs. stage 3, P = 2.33×10-15; normal vs. stage 4, P = 4.58 ×10-2) [Figure 1B]. The Kaplan-Meier plotter tool additionally indicated that the overall survival of HCC patients exhibiting high TBX19 expression was significantly lower than that of patients expressing lower levels of this gene (log-rank P <  0.0001) [Figure 1C]. As such, lower levels of TBX19 expression are associated with a better HCC patient prognosis.

 

Figure 1
Figure 1. Association between the expression of TBX19, clinicopathological parameters, and prognostic outcomes in patients with HCC. (A) TBX19 expression in HCC samples from the UALCAN database. (B) TBX19 expression levels in different HCC stages in the UALCAN database. (C) The relationship between TBX19 expression and prognostic outcomes in the KM plotter online database.

 

TBX19 controls HCC cellular migratory and proliferative activity

To determine how TBX19 affects HCC cell malignancy, we examined its expression in a range of HCC cell lines and control LX-2 cells. These analyses revealed that TBX19 expression levels were relatively high and low in SNU387 and Huh7 cells, respectively [Figure 2A]. To test the functional relevance of this gene, we then knocked down the TBX19 expresion in SNU387 cells, while upregulating the same in Huh7 cells, using appropriate constructs. As expected, this approach successfully enabled TBX19 knockdown and overexpression in the respective SNU387 and Huh7 cell lines [Figure 2B-C].

Following TBX19 knockdown, SNU387 cell viability was reduced relative to control cells [Figure 3A], as was further confirmed in an EdU uptake assay [Figure 3B]. The migration of these SNU387 cells was also impaired upon TBX19 silencing [Figure 3C-D]

We further constructed a TBX19 overexpression vector [Supplementary Figure 2A], and assessed the localization of TBX19 [Supplementary Figure 2B]. Then, we evaluated its impact on proliferative and migratory activity following successful transfection [Figure 2B-C]. When TBX19 was overexpressed, Huh7 cell viability was enhanced, as were proliferative and migratory activity [Figure 4A-D], thus confirming the ability of this gene to promote these malignant behaviors in tumor cells.

 

Figure 2.
Figure 2. TBX19 transfection efficiency in HCC cell lines. (A) TBX19 levels were detected via Western blotting in SNU387, LX-2, HepG2, and Huh7 cells. (B) qPCR was used to detect TBX19 expression levels in SNU387 and Huh7 cells. (C) Relative TBX19 levels in SNU387 and Huh7 cells were measured via Western blotting. **P < 0.01 vs. control.

 

Figure 3.
Figure 3. TBX19 downregulation suppresses HCC cell migration and proliferation in vitro. (A) A CCK-8 assay was employed to assess SNU387 cell proliferation following siR3 transfection. (B) Representative fluorescent images of SNU387 cells following EdU staining, with EdU staining (red) being indicative of proliferation and DAPI (blue) corresponding to cellular nuclei. (C) TBX19 knockdown inhibited SNU387 cell colony formation activity. (D) HCC cell migration was assessed via Transwell assay following TBX19 downregulation, with representative results being shown (100×). **P < 0.01 vs. control.

 

Figure 4.
Figure 4. TBX19 upregulation enhances in vitro HCC cellular migration and proliferation. (A) A CCK-8 assay was employed to assess Huh7 cell viability following TBX19 overexpression. (B) TBX19 overexpression promoted Huh7 cell proliferation by EdU staining. (C) TBX19 overexpression promoted Huh7 cell colony formation activity. (D) HCC cell migration was assessed via Transwell assay following TBX19 overexpression, with representative results being shown (100×). **P < 0.01 vs. control.

 

Analysis of TBX19 co-expressed genes in HCC

Next, genes that were co-expressed with TBX19 in HCC tumors were evaluated in an effort to assess patterns of shared genetic risk. In total, 19,922 genes were significantly correlated with TBX19 expression in this oncogenic context, of which 1,731 and 3,585 were respectively positively and negatively correlated with its expression (FDR < 0.01) [Figure 5A]. The top 50 most significantly positively and negatively correlated genes were additionally used to generate heat maps [Supplementary Figure 3]. A GO term enrichment analysis of these TBX19-correlated genes was then conducted, revealing them to be enriched for cellular component terms including nucleus, membrane, and membrane-enclosed lumen, molecular function terms 

including hydrolase activity, nucleic acid binding, ion binding, and protein binding, and biological process terms including response to stimulus, multicellular organismal process, metabolic processes, and biological regulation [Figure 5B]. In a KEGG pathway enrichment analysis, these genes were also enriched in the spliceosome, drug metabolism, tryptophan metabolism, retinol metabolism, and valine, leucine, and isoleucine degradation pathways [Figure 5C]. We elected to focus on DTYMK as a target for further study, as we have previously found it to influence HCC tumor growth and it was more significant than other genes in this context.[28] We subsequently found that TBX19 expression was positively correlated with the expression of DTYMK [Figure 5D]. Overall, these results indicated that TBX19 to play a range of complex regulatory roles in HCC.

 

Figure 5.
Figure 5. LinkedOmics analysis of the intersection between TBX19 co-expressed genes and TBX19-related differentially expressed genes. (A) TBX19 co-expressed genes within HCC tumors were detected via Spearman correlation analyses using LinkedOmics. (B) Genes correlated with TBX19 expression were subjected to a GO term enrichment analysis of associated cellular component (CC), molecular function (MF), and biological process (BP) terms. (C) Genes correlated with TBX19 expression were subjected to a KEGG pathway enrichment analysis. (D) A positive correlation between TBX19 and DTYMK gene expression was observed. Full results are available online.

 

TBX19 regulates DTYMK-related dTTP pyrimidine biosynthesis

The DTYMK enzyme plays an essential role in mediating the synthesis of dTTP in pathways associated with pyrimidine metabolism, and poorly differentiated HCC samples exhibit elevated DTYMK expression and the intratumoral concentrations of dTTP.[24] We additionally found that overexpressing TBX19 in Huh7 cells resulted in an increase in dTTP levels within these cells, whereas TBX19 downregulation in TBX19 overexpressing cells was associated with a reduction in these dTTP levels [Figure 6A-B].

 

Figure 6.
Figure 6. TBX19 promotes DTYMK upregulation and thereby regulates dTTP levels within cells. (A) DTYMK protein expression was assessed within cells following siR3 and/or TBX19 overexpression construct transfection. (B) Relative dTTP levels were measured within cells following siR3 and/or TBX19 overexpression construct transfection. **P < 0.01; Student’s t-tests.


DISCUSSION

There have been major advances in the management and diagnosis of HCC in recent years. However, early diagnosis rates for this cancer remain unsatisfactory despite the more widespread application of ultrasonography, magnetic resonance imaging, computed tomography, and serum α-fetoprotein-based surveillance.[30] In patients diagnosed with HCC, surgical resection remains the primary treatment approach in combination with radiotherapy, chemotherapy, targeted therapies, interventional therapies, and/or traditional Chinese medicinal treatment as appropriate.[31] However, the prognosis of HCC patients remains poor owing to the high rates of tumor recurrence, with an estimated 5-year survival rate of < 20% for affected patients.[32] There is thus an urgent need to identify potential biomarkers with the potential to improve HCC patient prognostic outcomes.

TBX19, formerly referred to as TPIT, is a gene which encodes a member of the TBX transcription factor family encoding a conserved T-box DNA binding domain. In the first step of our study, we used the UALCAN databases to determine the expression level of TBX19 in cancers and normal tissues. The results showed that TBX19 had significantly higher expression in most cancer types. These results indicated that TBX19 indeed promotes oncogenesis and tumor progression in human cancers. Genes in this family regulate gene expression in essential processes including embryonic development, with TBX19 being capable of binding to specific genes via T-box domain interactions.[33],[34] In mice in which TBX19 is knocked out, a near-total loss of proopiomelanocortin-expressing cells is observed, resulting in profound glucocorticoid and adrenocorticotropic hormone deficiencies.[12],[35],[36],[37]

We then focused on the function of differentially expressed TBX19 using GO enrichment analysis and KEGG pathway enrichment analysis. As expected, we found that the functions of these genes are primarily related to the cellular component terms including nucleus, membrane, and membrane-enclosed lumen, molecular function terms including hydrolase activity, nucleic acid binding and so on. In order to replicate all cells including tumor cells, must be capable of synthesizing and replicating DNA. As such, drugs that disrupt nucleoside metabolism and synthesis are frequently employed to treat certain cancers.[38] In the de novo pathway, deoxyuridine-5’-monophosphate is methylated by thymidylate synthetase to produce deoxythymidine-5’-monophosphate (dTMP),[39] whereas in the salvage pathway thymidine kinase instead phosphorylates thymidine to yield dTMP. In turn, dTMP can be phosphorylated in a reaction catalyzed by deoxythymidylate kinase (DTYMK), thereby yielding dTDP, thus unifying the de novo and salvage pathways and providing an essential basis for the synthesis of additional DNA.[40],[41] In prior reports, DTYMK knockdown was shown to inhibit this pathway, resulting in reduced dTDP levels together with dTMP accumulation.[42]

Here, we found TBX19 to be upregulated at the mRNA level in HCC, with the knockdown of this gene suppressing HCC cell growth and malignancy in vitro, whereas its upregulation had the opposite effect. TBX19 thus appears to play a central role in the context of hepatic oncogenesis, although additional work will be necessary to clarify the molecular mechanisms whereby it shapes tumor progression. Moreover, we found TBX19 protein expression to be correlated with the expression of DTYMK, which regulated dTTP production within HCC tumors. As such, this TBX19 may represent a viable clinical target in HCC patients worthy of future study.

However, there are some limitations to our study. Notably, we did not explore the exact underlying molecular mechanisms and relationship between TBX19 and DTYMK in the context of tumorigenesis, and this will therefore need to be a topic for future research.


CONCLUSIONS

In conclusion, these results indicate that TBX19 is overexpressed in HCC tumors and play an important role in the malignancy and progression of this form of cancer. Moreover, we found TBX19 to regulate the expression of DTYMK and associated DTYMK-mediated dTTP production in HCC cells. These findings highlight the HCC effects of TBX19 revealing its potential as a novel therapeutic target for HCC.

 

FINANCIAL SUPPORT AND SPONSORSHIP

This work was supported by the Natural Science Foundations of Shandong Province (No.ZR2021MH022, to Shihai Liu) and the Youth Foundation of Affiliated Hospital of Qingdao University (No.QDFYQN202102025, to Guifang He).

 

CONFLICTS OF INTEREST

There are no conflicts of interest.

 

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.


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SUPPLEMENTARY FIGURES

Supplementary Figure 1.
Supplementary Figure 1. Gene expression profiles for all tumors and paired normal tissue samples included in the UALCAN database.

Supplementary Figure 2.
Supplementary Figure 2. TBX19 vector construct preparation, sequencing, and localization analyses. (A) The constructed TBX19 overexpression vector. (B) Immunofluorescent assessment of TBX19 localization within Huh7 cells (red), with DAPI (blue) being used for nuclear counterstaining.

Supplementary Figure 3.
Supplementary Figure 3. LinkedOmics analysis of the intersection between TBX19 co-expressed genes and TBX19-related differentially expressed genes. (A) The top 50 genes that were positively correlated with the expression of TBX19 within HCC tumors as assessed via LinkedOmics. (B) The top 50 genes that were negatively correlated with the expression of TBX19 within HCC tumors as assessed via LinkedOmics. Green and red respectively correspond to genes negatively and positively correlated with the expression of TBX19.

 

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Panobinostat and Its Combination with 3‑Deazaneplanocin‑A Induce Apoptosis and Inhibit In vitro Tumorigenesis and Metastasis in GOS‑3 Glioblastoma Cell Lines

Javier de la Rosa*, Alejandro Urdiciain*, Juan Jesús Aznar‑Morales, Bárbara Meléndez1,
Juan A. Rey2, Miguel A. Idoate3, Javier S. Castresana


Cancer Stem‑Like Cells Have Cisplatin Resistance and miR‑93 Regulate p21 Expression in Breast Cancer

Akiko Sasaki1, Yuko Tsunoda2, Kanji Furuya3, Hideto Oyamada1, Mayumi Tsuji1, Yuko Udaka1, Masahiro Hosonuma1, Haruna Shirako1, Nana Ichimura1, Yuji Kiuchi1


The Contribution of Hexokinase 2 in Glioma

Hui Liu1, Hongwei Yang2, Xin Wang3, Yanyang Tu1


The Mechanism of BMI1 in Regulating Cancer Stemness Maintenance, Metastasis, Chemo‑ and Radiation Resistance

Xiaoshan Xu, Zhen Wang, Nan Liu, Pengxing Zhang, Hui Liu, Jing Qi, Yanyang Tu


A Multisource Adaptive Magnetic Resonance Image Fusion Technique for Versatile Contrast Magnetic Resonance Imaging

Lei Zhang1,2, Fang‑Fang Yin1,2,3, Brittany Moore1,2, Silu Han1,2, Jing Cai1,2,4


Senescence and Cancer

Sulin Zeng1,2, Wen H. Shen2, Li Liu1


The “Wild”‑type Gastrointestinal Stromal Tumors: Heterogeneity on Molecule Characteristics and Clinical Features

Yanhua Mou1, Quan Wang1, Bin Li1,2


Retreatment with Cabazitaxel in a Long‑Surviving Patient with Castration‑Resistant Prostate Cancer and Visceral Metastasis

Raquel Luque Caro, Carmen Sánchez Toro, Lucia Ochoa Vallejo


Therapy‑Induced Histopathological Changes in Breast Cancers: The Changing Role of Pathology in Breast Cancer Diagnosis and Treatment

Shazima Sheereen1, Flora D. Lobo1, Waseemoddin Patel2, Shamama Sheereen3,
Abhishek Singh Nayyar4, Mubeen Khan5


Glioma Research in the Era of Medical Big Data

Feiyifan Wang1, Christopher J. Pirozzi2, Xuejun Li1


Transarterial Embolization for Hepatocellular Adenomas: Case Report and Literature Review

Jian‑Hong Zhong1,2, Kang Chen1, Bhavesh K. Ahir3, Qi Huang4, Ye Wu4, Cheng‑Cheng Liao1, Rong‑Rong Jia1, Bang‑De Xiang1,2, Le‑Qun Li1,2


Nicotinamide Phosphoribosyltransferase: Biology, Role in Cancer, and Novel Drug Target

Antonio Lucena‑Cacace1,2,3, Amancio Carnero1,2


Enhanced Anticancer Effect by Combination of Proteoglucan and Vitamin K3 on Bladder Cancer Cells

Michael Zhang, Kelvin Zheng, Muhammad Choudhury, John Phillips, Sensuke Konno


Molecular Insights Turning Game for Management of Ependymoma: A Review of Literature

Ajay Sasidharan, Rahul Krishnatry


IDH Gene Mutation in Glioma

Leping Liu1, Xuejun Li1,2


Challenges and Advances in the Management of Pediatric Intracranial Germ Cell Tumors: A Case Report and Literature Review

Gerard Cathal Millen1, Karen A. Manias1,2, Andrew C. Peet1,2, Jenny K. Adamski1


Assessing the Feasibility of Using Deformable Registration for Onboard Multimodality‑Based Target Localization in Radiation Therapy

Ge Ren1,2,3, Yawei Zhang1,2, Lei Ren1,2


Research Advancement in the Tumor Biomarker of Hepatocellular Carcinoma

Qing Du1, Xiaoying Ji2, Guangjing Yin3, Dengxian Wei3, Pengcheng Lin1, Yongchang Lu1,
Yugui Li3, Qiaohong Yang4, Shizhu Liu5, Jinliang Ku5, Wenbin Guan6, Yuanzhi Lu7


Novel Insights into the Role of Bacterial Gut Microbiota in Hepatocellular Carcinoma

Lei Zhang1, Guoyu Qiu2, Xiaohui Xu2, Yufeng Zhou3, Ruiming Chang4


Central Odontogenic Fibroma with Unusual Presenting Symptoms

Aanchal Tandon, Bharadwaj Bordoloi, Safia Siddiqui, Rohit Jaiswal


The Prognostic Role of Lactate in Patients Who Achieved Return of Spontaneous Circulation after Cardiac Arrest: A Systematic Review and Meta‑analysis

Dongni Ren1, Xin Wang2, Yanyang Tu1,2


Inhibitory Effect of Hyaluronidase‑4 in a Rat Spinal Cord Hemisection Model

Xipeng Wang1,2, Mitsuteru Yokoyama2, Ping Liu3


Research and Development of Anticancer Agents under the Guidance of Biomarkers

Xiaohui Xu1, Guoyu Qiu1, Lupeng Ji2, Ruiping Ma3, Zilong Dang4, Ruling Jia1, Bo Zhao1


Idiopathic Hypereosinophilic Syndrome and Disseminated Intravascular Coagulation

Mansoor C. Abdulla


Phosphorylation of BRCA1‑Associated Protein 1 as an Important Mechanism in the Evasion of Tumorigenesis: A Perspective

Guru Prasad Sharma1, Anjali Geethadevi2, Jyotsna Mishra3, G. Anupa4, Kapilesh Jadhav5,
K. S. Vikramdeo6, Deepak Parashar2


Progress in Diagnosis and Treatment of Mixed Adenoneuroendocrine Carcinoma of Biliary‑Pancreatic System

Ge Zengzheng1, Huang-Sheng Ling2, Ming-Feng Li2, Xu Xiaoyan1, Yao Kai1, Xu Tongzhen3,
Ge Zengyu4, Li Zhou5


Surface-Enhanced Raman Spectroscopy to Study the Biological Activity of Anticancer Agent

Guoyu Qiu1, Xiaohui Xu1, Lupeng Ji2, Ruiping Ma3, Zilong Dang4, Huan Yang5


Alzheimer’s Disease Susceptibility Genes in Malignant Breast Tumors

Steven Lehrer1, Peter H. Rheinstein2


OSMCC: An Online Survival Analysis Tool for Merkel Cell Carcinoma

Umair Ali Khan Saddozai1, Qiang Wang1, Xiaoxiao Sun1, Yifang Dang1, JiaJia Lv1,2, Junfang Xin1, Wan Zhu3, Yongqiang Li1, Xinying Ji1, Xiangqian Guo1


Protective Activity of Selenium against 5‑Fluorouracil‑Induced Nephrotoxicity in Rats

Elias Adikwu, Nelson Clemente Ebinyo, Beauty Tokoni Amgbare


Advances on the Components of Fibrinolytic System in Malignant Tumors

Zengzheng Ge1, Xiaoyan Xu1, Zengyu Ge2, Shaopeng Zhou3, Xiulin Li1, Kai Yao1, Lan Deng4


A Patient with Persistent Foot Swelling after Ankle Sprain: B‑Cell Lymphoblastic Lymphoma Mimicking Soft‑tissue Sarcoma

Crystal R. Montgomery‑Goecker1, Andrew A. Martin2, Charles F. Timmons3, Dinesh Rakheja3, Veena Rajaram3, Hung S. Luu3


Coenzyme Q10 and Resveratrol Abrogate Paclitaxel‑Induced Hepatotoxicity in Rats

Elias Adikwu, Nelson Clemente Ebinyo, Loritta Wasini Harris


Progress in Clinical Follow‑up Study of Dendritic Cells Combined with Cytokine‑Induced Killer for Stomach Cancer

Ling Wang1,2, Run Wan1,2, Cong Chen1,2, Ruiliang Su1,2, Yumin Li1,2


Supraclavicular Lymphadenopathy as the Initial Manifestation in Carcinoma of Cervix

Priyanka Priyaarshini1, Tapan Kumar Sahoo2


ABO Typing Error Resolution and Transfusion Support in a Case of an Acute Leukemia Patient Showing Loss of Antigen Expression

Debasish Mishra1, Gopal Krushna Ray1, Smita Mahapatra2, Pankaj Parida2


Protein Disulfide Isomerase A3: A Potential Regulatory Factor of Colon Epithelial Cells

Yang Li1, Zhenfan Huang2, Haiping Jiang3


Clinicopathological Association of p16 and its Impact on Outcome of Chemoradiation in Head‑and‑Neck Squamous Cell Cancer Patients in North‑East India

Srigopal Mohanty1, Yumkhaibam Sobita Devi2, Nithin Raj Daniel3, Dulasi Raman Ponna4,
Ph. Madhubala Devi5, Laishram Jaichand Singh2


Potential Inhibitor for 2019‑Novel Coronaviruses in Drug Development

Xiaohui Xu1, Zilong Dang2, Lei Zhang3, Lingxue Zhuang4, Wutang Jing5, Lupeng Ji6, Guoyu Qiu1


Best‑Match Blood Transfusion in Pediatric Patients with Mixed Autoantibodies

Debasish Mishra1, Dibyajyoti Sahoo1, Smita Mahapatra2, Ashutosh Panigrahi3


Characteristics and Outcome of Patients with Pheochromocytoma

Nadeema Rafiq1, Tauseef Nabi2, Sajad Ahmad Dar3, Shahnawaz Rasool4


Comparison of Histopathological Grading and Staging of Breast Cancer with p53‑Positive and Transforming Growth Factor‑Beta Receptor 2‑Negative Immunohistochemical Marker Expression Cases

Palash Kumar Mandal1, Anindya Adhikari2, Subir Biswas3, Amita Giri4, Arnab Gupta5,
Arindam Bhattacharya6


Chemical Compositions and Antiproliferative Effect of Essential Oil of Asafoetida on MCF7 Human Breast Cancer Cell Line and Female Wistar Rats

Seyyed Majid Bagheri1,2, Davood Javidmehr3, Mohammad Ghaffari1, Ehsan Ghoderti‑Shatori4


Cyclooxygenase‑2 Contributes to Mutant Epidermal Growth Factor Receptor Lung Tumorigenesis by Promoting an Immunosuppressive Environment

Mun Kyoung Kim1, Aidin Iravani2, Matthew K. Topham2,3


Potential role of CircMET as A Novel Diagnostic Biomarker of Papillary Thyroid Cancer

Yan Liu1,2,3,4#, Chen Cui1,2,3,4#, Jidong Liu1,2,3,4, Peng Lin1,2,3,4,Kai Liang1,2,3,4, Peng Su5, Xinguo Hou1,2,3,4, Chuan Wang1,2,3,4, Jinbo Liu1,2,3,4, Bo Chen6, Hong Lai1,2,3,4, Yujing Sun1,2,3,4* and Li Chen 1,2,3,4*


Cuproptosis-related Genes in Glioblastoma as Potential Therapeutic Targets

Zhiyu Xia1,2, Haotian Tian1, Lei Shu1,2, Guozhang Tang3, Zhenyu Han4, Yangchun Hu1*, Xingliang Dai1*


Cancer Diagnosis and Treatments by Porous Inorganic Nanocarriers

Jianfeng Xu1,2, Hanwen Zhang1,2, Xiaohui Song1,2, Yangong Zheng3, Qingning Li1,2,4*


Delayed (20 Years) post-surgical Esophageal Metastasis of Breast Cancer - A Case Report

Bowen Hu1#, Lingyu Du2#, Hongya Xie1, Jun Ma1, Yong Yang1*, Jie Tan2*


Subtyping of Undifferentiated Pleomorphic Sarcoma and Its Clinical Meaning

Umair Ali Khan Saddozai, Zhendong Lu, Fengling Wang, Muhammad Usman Akbar, Saadullah Khattak, Muhammad Badar, Nazeer Hussain Khan, Longxiang Xie, Yongqiang Li, Xinying Ji, Xiangqian Guo


Construction of Glioma Prognosis Model and Exploration of Related Regulatory Mechanism of Model Gene

Suxia Hu, Abdusemer Reyimu, Wubi Zhou, Xiang Wang, Ying Zheng, Xia Chen, Weiqiang Li, Jingjing Dai


ESRP2 as a Non-independent Potential Biomarker-Current Progress in Tumors

Yuting Chen, Yuzhen Rao, Zhiyu Zeng, Jiajie Luo, Chengkuan Zhao, Shuyao Zhang


Resection of Bladder Tumors at the Ureteral Orifice Using a Hook Plasma Electrode: A Case Report

Jun Li, Ziyong Wang, Qilin Wang


Structural Characterization and Bioactivity for Lycium Barbarum Polysaccharides

Jinghua Qi1,2,  Hangping Chen3,Huaqing Lin2,4,Hongyuan Chen1,2,5* and Wen Rui2,3,5,6*


The Role of IL-22 in the Prevention of Inflammatory Bowel Disease and Liver Injury

Xingli Qi1,2, Huaqing Lin2,3, Wen Rui2,3,4,5 and Hongyuan Chen1,2,3


RBM15 and YTHDF3 as Positive Prognostic Predictors in ESCC: A Bioinformatic Analysis Based on The Cancer Genome Atlas (TCGA)

Yulou Luo1, Lan Chen2, Ximing Qu3, Na Yi3, Jihua Ran4, Yan Chen3,5*


Mining and Analysis of Adverse Drug Reaction Signals Induced by Anaplastic Lymphoma Kinase-Tyrosine Kinase Inhibitors Based on the FAERS Database

Xiumin Zhang1,2#, Xinyue Lin1,3#, Siman Su1,3#, Wei He3, Yuying Huang4, Chengkuan Zhao3, Xiaoshan Chen3, Jialin Zhong3, Chong Liu3, Wang Chen3, Chengcheng Xu3, Ping Yang5, Man Zhang5, Yanli Lei5*, Shuyao Zhang1,3*


Advancements in Immunotherapy for Advanced Gastric Cancer

Min Jiang1#, Rui Zheng1#, Ling Shao1, Ning Yao2, Zhengmao Lu1*


Tumor Regression after COVID-19 Infection in Metastatic Adrenocortical Carcinoma Treated with Immune Checkpoint Blockade: A Case Report

Qiaoxin Lin1, Bin Liang1, Yangyang Li2, Ling Tian3*, Dianna Gu1*


Mining and Analysis of Adverse Events of BRAF Inhibitors Based on FDA Reporting System

Silan Peng1,2#, Danling Zheng1,3#, Yanli Lei4#, Wang Chen3, Chengkuan Zhao3, Xinyue Lin1, Xiaoshan Chen3, Wei He3, Li Li3, Qiuzhen Zhang5*, Shuyao Zhang1,3*


Malignant Phyllodes Tumor with Fever, Anemia, Hypoproteinemia: A Rare and Strange Case Report and Literature Review

Zhenghang Li1, Yuxian Wei1*


Construction of Cuproptosis-Related LncRNA Signature as a Prognostic Model Associated with Immune Microenvironment for Clear-Cell Renal Cell Carcinoma

Jiyao Yu1#, Shukai Zhang2#, Qingwen Ran3, Xuemei Li4,5,6*


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