Translational Surgery

Review | Open Access

Vol.6 (2022) | Issue-1 | Page No: 1-8

Peroxisome Proliferator-Activated Receptor-γ Agonists as New Targets of Lung Cancer Therapy

Shixiong Wei1*

Affiliations  

1. Department of Cardiothoracic Surgery, The First Bethune Hospital of Jilin University, Changchun, 130000, Jilin Province, China.

* Corresponding Author

Address for Correspondance: Dr.Shixiong Wei, The First Bethune Hospital of Jilin University, Changchun, No.1 Xinmin Road, Chaoyang District, Changchun, 130000, Jilin Province, China, email: wei_shixiong@163.com, Ph: +8613269330000


Important Dates  

Date of Submission:   07-Jan-2022

Date of Acceptance:   28-Feb-2022

Date of Publication:   30-Mar-2022

ABSTRACT

Lung cancer is one of the main causes of cancer-related deaths. Clinically, most patients are diagnosed at the advanced stage of the disease, hence often confront poor prognosis. Therefore, it is crucial to develop new prevention and treatment methods. Peroxisome Proliferator-Activated Receptors (PPARs) are a class of nuclear transcription factors activated by ligands, belonging to the type II nuclear hormone receptor superfamily. PPAR-γ is known to promote differentiation, antiproliferation, and apoptosis in adipocyte maturation and lipid homeostasis. However, more and more evidences show that it also plays an important role in tumor inhibition. The secretion of certain metalloproteinases and extracellular matrix proteins, which may induce angiogenesis in the tumor matrix microenvironment, are regulated by PPAR-γ and thus can inhibit the development and metastasis of malignant tumors such as lung cancer. This article reviews the relevant literature, and summarizes the research progress of PPAR-γ agonists used alone or in combination with standard chemotherapy as new therapies for lung cancer.


1. INTRODUCTION

Lung cancer accounts for about 25% of cancer-related deaths every year and can be classified into small cell lung cancer (SCLC) and Non-small cell lung cancer (NSCLC) according to their pathological manifestations. NSCLC comprising of adenocarcinoma, squamous cell carcinoma, and large cell carcinoma accounts for 85% of all lung cancers, while the remaining 15% is SCLC.[1],[2] Genetic mutation, poor diet, and air pollution are currently known risk factors for lung cancer, and chronic lung inflammation and infection have been demonstrated to play a role in the process.[3] Although medical technology has evolved significantly in the past 30 years, the overall 5-year survival rate of lung cancer patients is still less than 18%, which is mainly due to the fact that more than half of the patients are in the advanced stage at diagnosis.[4] Therefore, there is an urgent need for surgeons to follow new preventive, diagnostic, and therapeutic strategies to improve the clinical outcomes of patients with lung cancer.

Initially, cells acquire the ability to dedifferentiate or escape terminal differentiation, proliferate in an unrestricted manner and resist apoptosis, which in turn enables them to produce tumors. Therefore, interventions that reverse these processes have become one of the main research areas in cancer treatment. Studies have shown that activation of nuclear hormone receptors can produce therapeutic effects on several common tumors. In addition, agonists of estrogen receptor-β, retinoic acid receptor-α, and Retinoid X receptor (RXR) have also been shown to have pre-differentiation, anti-proliferation, and/or pro-apoptotic effects in a variety of cancers.[5] Peroxisome proliferator-activated receptors (PPARs), another type of nuclear hormone receptor, have long been recognized for their role in the regulation of lipid and glucose metabolism. However, recent studies have shown that the mechanism by which PPAR target genes are activated or inhibited by transcription also plays an important role in cell differentiation, proliferation, survival, and apoptosis-related carcinogenesis.[6],[7] PARs in the human body widely exist in a variety of cells. They are broadly 

divided into three types; PPAR-α, PPAR-β/δ, and PPAR-γ, with each group differing in structure and function, as well as the expression of the site and pattern.[5],[7] Compared with the former two, PPAR-γ has a more active role in lung cancer tissues, so its research value as a tumor suppressor is also higher.[8] 

 

Figure 1
Figure 1. Molecular regulatory mechanisms of PPARγ.
 

 

Based on the variations in promoter sequence and splicing method, the mRNA of PPAR-γ can be divided into four subtypes: PPAR-γ1, PPAR-γ2, PPAR-γ3, and PPAR-γ4. PPAR-γ1 is the most important subtype of PPAR-γ, which is widely distributed in adipose tissues, the heart, pancreas, gastrointestinal tract, kidney, and skeletal muscle. The molecular structure of PPAR-γ2 is 30 amino acids longer than that of PPAR-γ1, and it is mainly expressed in adipose tissues, which exert multiple effects on human metabolism, insulin sensitization, and inflammatory response. PPAR-γ3 is expressed in adipocytes, macrophages, and colonic epithelial cells, while the tissue distribution of PPAR-γ4 is currently unclear.[7]

Previous studies have shown that PPAR-γ is widely present in tumor tissues of patients with SCLC and NSCLC.[9] However, due to some modification mechanism of the functional domain or the lack of suitable ligands, this receptor is inactive in lung cancer cells. In fact, studies have shown that the loss of PPAR-γ function in vivo may be related to the metastasis of colorectal cancer.[10] Immunohistochemical study of 147 primary NSCLC tumor specimens confirmed that the expression of PPAR-γ was related to the histological type and pathological grade of tumor specimens. Also, its expression in well-differentiated adenocarcinoma was much higher than that in poorly differentiated adenocarcinoma or squamous cell carcinoma, which provided a theoretical foundation to study the role of PPAR-γ in the treatment of lung cancer patients.[11]

It has been established that PPAR-γ ligands are both naturally occurring and artificially synthesized; the former includes saturated fatty acids, unsaturated fatty acids, and eicosane derivatives, such as 15-deoxy-δ 12, 14-prostaglandin J2 (15D-pgj2) and nitrated fatty acids such as nitrated linoleic acid and nitrated oleic acid, while the latter is a synthetic compound represented by thiazolidinediones (TZDs), such as Pioglitazone, Rosiglitazone, and Troglitazone.[8] At present, it is believed that these agonists can activate the PPAR-γ pathway through a variety of pathways, including direct binding to PPAR-γ ligand, binding to heat shock protein 72, and then binding to a ligand. However, the mainstream view is that the ligand first activates PPAR-γ by regulating the phosphorylation of tyrosine residues in kinases -1,2 by extracellular signals and the phosphorylation of mitogen-activated protein kinase (MAPK). It forms heterodimers (PPAR: RXR) with the corpus luteum X receptor and binds to specific peroxisome proliferator-response elements in the promoter region of the target gene, thereby activating the transcriptional activity of PPAR-γ.[12] A large number of evidence have shown that PPAR-γ agonists have an anti-tumor effect, which can limit their proliferation, growth, and progression, and induce their differentiation and apoptosis.[13] Therefore, PPAR-γ is worthy of investigation as a new approach to the treatment of lung cancer.


2. MULTIPLE EFFECTS OF PPAR-γ IN LUNG CANCER

Multiple molecular mechanisms play role in the anti-tumor process of PPAR-γ activation, which not only affects cancer cells themselves but also affects the microenvironment of tumor cells, such as surrounding immune system cells, fibroblasts, fat cells, blood, and lymphatic system, etc. Studies have shown that apart from cellular components, PPAR-γ can even affect non-cellular components of the tumor microenvironment, such as growth factors, cytokines, chemokines, extracellular matrix (ECM), etc. PPAR-γ plays a key role in all stages of tumor genesis and development by directly acting on tumor cells and indirectly acting on the tumor cell microenvironment (Figure 2).[13] Up to now, studies have shown that PPAR-γ can regulate the differentiation, proliferation, apoptosis, and metastasis of cancer cells after activation, and finally form a microenvironment that is not conducive to tumor growth and development, and can inhibit tumor development and metastasis.

 

Figure 2
Figure 2. PPARγ’s role in pulmonary inflammation.

 

2.1. Role of PPAR-γ agonist in tumorigenesis

2.1.1. Regulatory effect of PPAR-γ agonist on tumor cells

PPAR-γ is an important regulator of cell differentiation and a key factor that represents the antitumor potential of the human body. As mentioned above, cells often dedifferentiate or escape terminal differentiation during carcinogenesis, so the expression of protein markers related to cell differentiation in cancer cells is usually down-regulated. Actin-binding protein (Gelsolin), one of such markers, is low in expression in many cancers, including lung cancer, and up-regulated after induction of differentiation in vitro. The PPAR-γ activation of Ciglitazone and 15d-PGJ2 in multiple non-small cell lung cancer cell lines enhanced the expression of gelsolin, Mad, and p21, suggesting that it promoted the differentiation process of cancer cells while also reducing the expression of lineage-specific markers associated with lung progenitor cells, such as mucin 1 (MUC1) and surfactant protein -A (SP-A). Moreover, the researchers also observed that the treatment with Ciglitazone could promote the morphological changes of cancer cells, and the treated cells were closer to differentiated and mature cells.[14] Another study further explored this finding, which proved that such PPAR-γ agonists can induce the differentiation of NSCLC cells of A549 and NCI-H23, with the continuous activation of extracellular signal-regulated kinase 1/2 (ERK1/2), which has been proved to be able to induce cell differentiation.[15] Other studies have shown that PPAR-γ activation can also induce adenocarcinoma cells to transform into polar mature differentiation phenotype.[16] These studies have proved the anti-tumor and pre-differentiation effects of PPAR-γ activator in lung cancer.

The activation of PPAR-γ can also inhibit abnormal cell proliferation and tumor growth, and promote tumor cell apoptosis. A variety of PPAR-γ ligands have shown this anti-tumor effect in a variety of lung cancer cell lines as well as in mouse lung cancer models, and interestingly, researchers observed that there may be a variety of mechanisms that depend on cell type specifically responsible for these anti-proliferative and pro-apoptotic effects of PPAR-γ agonists. Troglitazone can inhibit the growth and induce the apoptosis of SQ-5 NSCLC cells in a PPAR-γ-dependent manner by stimulating the transcription factor GADD153, which is involved in the pro-apoptotic process.[17] Similarly, Ciglitazone and 15d-PGJ2 inhibit cell proliferation and promote the apoptosis of SCLC cells of H345 and H2081 and NSCLC cells of H1838 and H2106. The researchers found that the potential mechanisms that play a role in this process are up-regulation of p21 expression and down-regulation of cyclin D1 expression.[18] Troglitazone is also capable of inhibiting NSCLC cell proliferation in H1838, H1792, and A549 through PPAR-γ mediated inhibition of phosphoinositide 3-kinase (PI3K)/Akt signal pathway, stimulating that expression of deleted phosphatase and tensin homologues on chromosome 10 (PTEN). In addition, the aggregation of G0/G1 phase cells and the reduction in the number of S-phase cells can also demonstrate that Troglitazone can exert antiproliferative effects by inducing the blockade of G0/G1 cells in multiple NSCLC cell lines.[19] In A549 cells, cell cycle arrest is caused by decreased expression of two G1 phase regulators, cyclins D, and E. Although the apoptotic pathway is not affected in A549 cells, Troglitazone-mediated growth inhibition is the result of increased caspases-3 and caspases-9-dependent apoptosis in NSCLC cells of NCI-H23.[20] Through studying the signaling pathways of these apoptotic processes, people found that the expression levels of B-cell lymphoma -2 (Bcl-2) and Bcl-w were decreased, while the continuous activation of ERK1/2 and p38 led to the decreased expression of stress-activated protein kinase (SAPK)/c-jun N-terminal kinase (JNK).[21] Finally, nonsteroidal anti-inflammatory drugs, as another type of PPAR-γ ligand, have also been shown to inhibit non-anchored growth in NSCLC and SCLC cells. Natural and synthetic PPAR-γ ligands, as well as PPAR overexpression studies, yielded similar results.[22]

The above studies are supported by the results of animal studies. Troglitazone and Pioglitazone as well as Sulindac sulfide significantly reduced the primary tumor growth of NSCLC cells in A549 in a xenogenic mouse model.[23] Moreover, in the research using a mouse model of spontaneous lung adenocarcinoma, the treatment with Troglitazone or Pioglitazone can significantly delay the disease progression. This ability to inhibit tumors from proliferation to metastasis is the result of inhibited cell proliferation.[24] Therefore, the pro-differentiation, anti-proliferation, and pro-apoptosis functions generated after the activation of PPAR-γ will make PPAR-γ agonists become drugs with the potential to treat lung cancer.

2.1.2. Regulatory effect of PPAR-γ agonist on tumor microenvironment

Neovascularization is a pathological process necessary for cancer cells to successfully produce primary and metastatic lesions. Neovascularization allows tumor growth beyond the limits imposed by passive oxygen and nutrient diffusion at the primary and secondary sites and promotes metastasis by providing access for cancer cells to enter the circulation. Under normal circumstances, the angiogenic process is affected by both angiogenic and antiangiogenic factors, however, the upregulation of angiogenic factors during tumorigenesis leads to persistent abnormal angiogenesis. Unlike normal blood vessels, these tumor-associated blood vessels are highly permeable, further promoting the local diffusion and distant metastasis of cancer cells.[25]

Vascular endothelial growth factor (VEGF) is currently recognized as a potent angiogenic factor,[1] and in addition, includes members of the CXC chemokine family containing ELR motifs such as interleukin-8 (IL- 8, CXCL8), epithelial neutrophil-activating protein 78 (ena-78, CXCL5), growth regulated oncogene-α (growth regulated oncogene-α, growth-α, CXCL1) all of which have been proved to be capable of induce angiogenesis by stimulating the chemotaxis of endothelial cells that form new blood vessels.[26] Rosiglitazone reduces the tumor burden in mice by reducing the secretion of VEGF and inhibiting angiogenesis in Lewis lung cancer (LLC) cells, while Troglitazone and Pioglitazone inhibit the neoangiogenesis in mouse xenogenic cancer cell transplantation model by inhibiting the secretion of ELR-positive CXC chemokines by A549 cells and the migration of endothelial cells.[27] The activation of PPAR-γ, which is highly expressed in tumor endothelial cells, not only affects angiogenesis by inhibiting angiogenic factors but also blocks angiogenesis by directly inhibiting endothelial cell growth.[28] In addition, 15d- PGJ2 has been proved to induce caspase-dependent apoptosis in endothelial cells, and its antiangiogenic effect is worthy of further investigation.[29]

Stromal cells, led by myofibroblasts, are the main sources of cytokines, growth factors, matrix metalloproteinases (MMP), and ECM proteins in the tumor microenvironment, providing important assistance in the growth and metastasis of tumors. The transforming growth factor-β (TGF-β) signaling pathway has the function of inducing fibroblast differentiation into myofibroblasts, while 15d- PGJ2, Troglitazone, Ciglitazone, and Rosiglitazone have been demonstrated to inhibit TGF-β-stimulated differentiation of primary human lung fibroblasts into myofibroblasts, which is also true in IMR-90 human fetal lung fibroblasts.[30],[31] In addition, TGF-β-induced fibronectin expression was also inhibited by the PPAR-γ agonist pioglitazone, which has replicated in PPAR-γ ligand BRL49653, 15d- PGJ2, or Troglitazone-treated H1838 NSCLC cells.[32],[33] Studies have shown that the abnormal increase of some ECM components, including fibronectin and type Ⅰ collagen, will trigger the remodeling of the tumor microenvironment and eventually lead to the generation and development of cancer.[34] Therefore, PPAR-γ agonists do have significant anti-tumor effects and have a positive impact on the tumor microenvironment, which can further support their role and value in the treatment of lung cancer.

2.2. Effect of PPAR-γ agonist on tumor metastasis 

The effect of PPAR-γ on lung cancer is not just limited to the regulation of the formation and development of primary tumors. More and more evidences show that PPAR-γ can inhibit tumor metastasis after activation. In a study using a mouse xenogenic tumor cell transplantation model, the researchers found that the A549 cancer cell line transplanted to the dorsal side of the mouse was significantly inhibited after the application of Troglitazone or Pioglitazone. Another study has shown that metastases are detected in the lungs of animals treated with PPAR-γ agonists in a smaller and smaller number than those treated with placebo.[35] Similarly, a study using a rat model of in situ lung cancer showed that PPAR-γ overexpression was able to block the metastasis of tumor cells from one lung to the opposite lung or mediastinum by weakening the invasion ability of cancer cells, and the rats overexpressing PPAR-γ also survived for a longer period of time than the control rats.[36] Similar results were obtained in the mouse xenogeneic tumor cell transplantation model by implanting the LLC cell line into the subcutaneous area of the back of the mouse: Treatment with Rosiglitazone almost completely blocked the lung metastasis, thus retaining normal structure on most of the lung tissue, while the lung tissue of the control mice was full of metastatic cancer cells. Moreover, the researcher also observed the presence of LLC cells in the pulmonary vessels of mice treated with Rosiglitazone, but no LLC cells were detected in the lung parenchyma. These findings suggested that Rosiglitazone was able to inhibit the metastasis of tumor cells by preventing cancer cells from escaping into the circulation.[37]

Several other MMP experiments have also demonstrated the significant inhibitory effect of PPAR-γ agonists on tumor metastasis: matrix metalloproteinases are key regulators of extracellular matrix remodeling and destruction, and the expression of certain MMPs is related to the metastatic potential of tumors in mouse models and often to the poor prognosis of human patients with different types of cancer. In contrast, Rosiglitazone significantly reduced the activity of NCI-H157 and H1299 non-small cell lung cancer cells and the expression level of MMP-2,[14] and Rosiglitazone enhanced the activity of MMP tissue inhibitors, which substantially reduced the proteolytic activity of MMP.[38] Therefore, the inhibition of MMP also supports PPAR-γ-mediated antitumor effects.

The process of primary tumor metastasis is often accompanied by changes in the expression of some cell adhesion molecules. Naturally, E-cadherin connects epithelial cells together by secreting intercellular attachment molecules to maintain cells in a stable state. In tumor tissues, E-cadherin expression is often down-regulated, while adhesion molecules related to enhanced cell migration, such as N-cadherin, are usually up-regulated. Subsequently, intercellular adhesion loss, morphological changes, secretion of proteolytic enzymes, and anti-apoptosis appear. The activation of this process by tumor cells finally promotes their own diffusion and metastasis.[39]

TGF-β signaling pathway can drive and regulate a group of transcription factors including Snail, Slug, Twist, and zinc finger structure (ZEB1/2), and studies have shown that their expression in malignant tumors like lung cancer was abnormally increased, which has been proved to be related to the metastatic potential of advanced tumors and poor prognosis.[40] TGF-β could induce the formation of EMT in A549 cells, which was characterized by a gradual evolution from cuboidal epithelium to flat mesenchyme with loss of intercellular adhesion, as well as altered cadherin expression, which indicates enhanced tumor invasion and metastatic potential.[41] Troglitazone and Rosiglitazone could block TGF-β-induced EMT production, inhibit down-regulation of E-cadherin expression and up-regulation of N-cadherin and other mesenchymal cell markers. Furthermore, the researchers attempted to reverse the TGF-β-induced EMT production process using Troglitazone and Rosiglitazone and found that by inhibiting the transcriptional activity of SMAD3, a downstream component of TGF-β signal, both PPAR-γ agonists could maintain intercellular adhesion, inhibit the migration and invasion of tumor cells, and reduce the secretion of MMP-2 and MMP-9, further demonstrating the anti-tumor invasion and metastatic potential of PPAR-γ agonists.[13]

Clinical data showed that cancers diagnosed with local infiltration and distant metastasis are a strong predictor of poor prognosis. More than half of patients with lung cancer have distant metastasis at the time of diagnosis.[1] However, PPAR-γ agonists can not only inhibit the development of primary tumors but also inhibit their ability of infiltration and metastasis, which makes them have a broad prospect for treating lung cancer.


3. PPAR-γ AGONISTS COMBINED WITH CONVENTIONAL THERAPY IN LUNG CANCER TREATMENT

The potential value of PPAR-γ agonists in the treatment of lung cancer has not only been verified by a large number of experimental studies but also have been documented clinically. A multi-center study retrospectively analyzed 87,678 male patients with diabetes, of which, 11,289 patients used TZD while the remaining 76,389 patients did not use TZD. The study found that the probability of a subsequent diagnosis of lung cancer in the TZD group was decreased by 33%.[42] However, because of the study’s special population, it remains to be further explored for their application to the general population. One clinical trial (NCT00780234) targeting the general population is currently underway to evaluate the role of Pioglitazone in the prevention of lung cancer.

PPAR-γ agonists not only have a therapeutic effect on lung cancer when used alone but also show a good synergistic effect when used in combination with traditional chemotherapy drugs. Researchers combined PPAR-γ ligands such as Rosiglitazone and GW1929 with platinum drugs commonly used for the treatment of lung cancer such as cisplatin and carboplatin, and the results showed that they synergistically could inhibit the growth of NSCLC cell line. This effect was also evident in xenograft lung cancer models and spontaneous colon cancer models, with absence of additional toxicity to test animals. The mechanism of this synergistic effect is the activation of PPAR-γ which reduces the expression of metallothionein, thus protecting cells from platinum toxicity.[43] Another study using the PPAR-γ agonist Troglitazone and Pioglitazone in combination with the chemotherapeutic drugs cisplatin and paclitaxel has also obtained similar results in vivo.[44] In addition to traditional cytotoxic chemotherapy, specific molecular targeted therapy for tumorigenesis has attracted more and more attention from clinicians in recent years. PPAR-γ agonists also have synergistic effects with this new type of therapeutic agent. Rosiglitazone could enhance the anti-proliferative effect of epidermal growth factor receptor inhibitor gefitinib on A549 cells. The 3-hydroxy -3-methylglutaryl-CoA reductase (HMG-CoA reductase) inhibitor in combination with Troglitazone and lovastatin, inhibits the growth of CL1-0 lung adenocarcinoma cells significantly compared with the inhibitor alone.[45],[46]


4. CONCLUSION

Through the review of a large number of experimental data combined with clinical retrospective analysis data, it is clear that PPAR-γ has a good prospect as a new target of anticancer drugs. PPAR-γ agonists not only have a curative effect when used alone but also show a synergistic effect when used in combination with standard chemotherapy. All these have indicated that PPAR-γ agonist, in combination with other therapies that have been applied or are still in clinical trials, represents a novel and attractive therapeutic method for lung cancer. Researchers should continue to design multi-center randomized controlled clinical trials to verify the efficacy and safety of PPAR-γ agonists in the treatment of lung cancer.

 

FUNDING: N/A

 

CONFLICTS OF INTEREST:

The author confirms that there are no potential conflicts of interest.


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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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