Cancer Translational Medicine

Review | Open Access

Vol.8 (2022) | Issue-2 | Page No: 45-53

DOI: https://doi-ds.org/doilink/06.2022-48274352/A2

Lung Cancer Tumor Microenvironment: An Update on Recent Advances in Research

Guangda Yuan1, Bowen Hu1, Yong Yang1*

Affiliations  

1. Department of Thoracic Surgery, The Affiliated Suzhou Hospital of Nanjing Medical University, Suzhou Municipal Hospital, Suzhou, Jiangsu, China

Corresponding Author

Address for correspondence: Dr. Yong Yang, Department of Thoracic Surgery, The Affiliated Suzhou Hospital of Nanjing Medical University, Suzhou Municipal Hospital, No.16 Baita West Road, Gusu District, Suzhou 215000, Jiangsu, China. E-mail: 337914338@qq.com


Important Dates  

Date of Submission:   11-Mar-2022

Date of Acceptance:   27-Apr-2022

Date of Publication:   28-Jun-2022

ABSTRACT

Lung cancer has become one of the most predominant malignant tumors worldwide in recent years, and the incidence and mortality rate of lung cancer in China is also rising year after year. According to the authoritative statistics released by the National Cancer Center in 2019, the incidence and mortality rate of lung cancer ranked first among malignant tumors. It is therefore increasingly important to strengthen the treatment and research on lung cancer. In recent years, several studies have found that the tumor microenvironment (TME) has an important role in cancer progression and treatment. TME is even more important in the functions played by malignant tumor infiltration, immune escape, and immune tolerance. Therefore, the aim of this paper is to summarize the role of immune infiltrating cells, hypoxic environment, exosomes, and extracellular matrix (ECM) in the lung cancer tumor microenvironment and to discuss the progress in treatment of lung cancer and its relationship with TME in lung cancer.


INTRODUCTION

Tumor microenvironment (TME) was first proposed by Whiteside and Ioannides, defining it as the local biological microenvironment in which tumorigenesis and development occur, including components such as immune cells, and stromal cells, and their secretory factors, vascular endothelial cells and extracellular matrix (ECM).[1],[2] TME plays an important function in malignant infiltration, immune escape, and immunologic tolerance. [3] Precise and safe immunotherapy based on specific characteristics of the TME is currently the focus of attention in antitumor technology. While the TME characteristics of different individuals, as the main cause of immunotherapy tolerance, have yet to be explored in terms of the exact target population and relevant combination therapy regimens in order to optimize the existing immunotherapy paradigm. Four main types of immune cells have been identified in TME: tumor-infiltrating lymphocytes (TILs), dendritic cells (DCs), myeloid-derived suppressor cells (MDSCs), and tumor-associated macrophages (TAMs). [4]


IMMUNE INFILTRATING CELLS IN THE TUMOR MICROENVIRONMENT OF LUNG CANCER

The role of TILs in the microenvironment of non-small cell lung cancer (NSCLC)

TILs are heterogeneous populations of lymphocytes induced by tumor antigens and found mainly in the tumor stroma, consisting of two major cell subsets; CD8+ T cells and CD4+ T cells. [5] In the different microenvironments of NSCLC, the proportion of CD8+ T cells and CD4+ T cells differed greatly, with varying degrees of decreased CD4+ T, increased CD8+ T, and decreased CD4+ T/CD8+ T in alveolar lavage fluid of NSCLC patients. [6]

In the NSCLC microenvironment, CD8+ T cells can play both a tumor-promoting role by promoting cancer cell proliferation as well as a tumor-suppressive role by accelerating apoptosis of cancer cells. Cytotoxic T lymphocytes (CTL) are the activated state of CD8+ T cells, which effectively mediate anti-tumor immune responses by recognizing tumor-associated antigen (TAA) on Human leukocyte antigen(HLA), and thus exert a direct killing effect. [7] It has been shown that the number of CD8+ T cells in the NSCLC microenvironment has a statistically significant effect on the prognosis of patients with stage I-III NSCLC. And, more the CD8+ T cells, lower the TNM stage and better the prognosis. [LinkRef 8] Related studies suggest that the number of CD8+ T cells in the tumor microenvironment of NSCLC patients is positively correlated with progression-free survival (PFS) and overall survival (OS) of patients.[9] However, when the receptors on the surface of CD8+ T cells bind to certain cytokines in the NSCLC microenvironment, the patient's cellular immune function is greatly diminished, and the tumor continues to progress and deteriorate. [10] However, receptors such as cytotoxic T lymphocyte-associated antigen-4 (CTLA-4) and programmed cell death protein 1 (PD-1) on the surface of CD8+ T cells can prevent CD4+ T cells from inhibiting tumor progression and stimulate immune tolerance, further contributing to the proliferation of lung cancer. [11]

In the NSCLC microenvironment, CD4+ T cells are mainly divided into Th1 cells, Th2 cells, Th17 cells, and Treg cells. CD4+ T cells have antigen-recognizing TCR (T-cell receptor) on their surface, which binds to specific sites of MHC class II molecules and participates in signal transduction processes.[12] Immune function of NSCLC patients is affected by unstable components of CD4+ T cells.[13] Based on cell phenotype CD4+ T cells in the NSCLC microenvironment are divided into two categories; Th1 cells and Th2 cells, which are generally in a dynamic balance initially.[14] However, an imbalance in the Th1/Th2 cell ratio increases the risk of lung cancer progression.[14] Th1 cells release cytokines such as Tumor Necrosis Factor-α (TNF-α), interferon-γ(IFN-γ), and interleukin-2(IL-2) after activation, which inhibit tumor progression by participating in cellular immunity, inhibiting tumor neovascularization, and inducing apoptosis of tumor cells. Th2 cells are activated and release cytokines such as interleukin-4(IL-4), interleukin-5 (IL-5), and interleukin-10 (IL-10), which promote tumor growth through the intervention of humoral immunity.[15],[16] The results showed that the number of Th1 cells and the ratio of Th1/Th2 cells in the lung cancer microenvironment of NSCLC patients were lower than those in the healthy population group. Further, the corresponding number of Th2 cells is also found to be higher. When Th2 cells were significantly increased, the Th1/Th2 cell ratio was diminished that contributing to immune evasion of lung cancer cells, leading to tumor progression.[17] In addition, lung cancer cells secrete a variety of cytokines that hinder the anti-tumor immune process and accelerate the recurrence and metastasis of NSCLC lung cancer.[14] Meanwhile, Th17 cells secrete interleukin-17A (IL-17A), interleukin-17F (IL-17F), and IFN-γ, which mainly play a tumor-suppressive role in the NSCLC tumor microenvironment, and there is a correlation between the number of Th17 cells and the overall survival of tumor patients.[15],[16] CD4+CD25+ T cells, also known as Treg cells, suppress the activation of T lymphocytes by secreting cytokines such as IL-4, IL-10 and transforming growth factor-β (TGF-β) to regulate the immune function of tumor patients and promote the proliferation of lung cancer cells.[17] Treg cells can protect tumor cells from immune surveillance and enhance tumor cell proliferation by secreting IL-10. IL-10 is significantly elevated in the tumor microenvironment of NSCLC lung cancer patients, and the balance of Th17 and Treg cell ratio can also affect tumor progression.[18]

The role of tumor-infiltrating B lymphocytes in the microenvironment of NSCLC

B lymphocytes play an important role in humoral and cellular immunity.[19] Infiltrating B lymphocytes in the tumor microenvironment of NSCLC have a role in inhibiting lung cancer progression and are therefore closely related to the prognosis of lung cancer patients. B lymphocytes mediate inhibition of tumor growth mainly through antibody-dependent cytotoxicity. Tumor-infiltrating B lymphocytes secrete immunoglobulins and present tumor-associated antigens to CD4+ T cells, which in turn activate CD4+ T cells to produce tumor growth inhibition and ultimately achieve anti-tumor immune response through the activation of CD8+ T cells in the NSCLC tumor microenvironment.[20] And the high level of expression of these cells suggested a significant increase in disease-free survival. In addition, a particularly important finding is that Bregs (Regulatory B cells) secrete cytokines such as TNF-β, IL-10, and IL-35 in the NSCLC tumor microenvironment to suppress the immune function of patients, while tumor-evoked Bregs protect tumor cells from clearance by effector cells and subsequently promote the proliferation of lung cancer cells.[21] Breg cells are mainly involved in immunosuppressive processes and play a role in promoting the development of lung cancer.

The role of NK cells in the tumor microenvironment of NSCLC

Natural killer cells (NK cells) are mainly found in the peripheral blood and spleen and are the body's first line of defense against tumor cells. The inhibition of tumor infiltration mediated by infiltrating NK cells is closely related to the extent of tumor progression. One study found that NK cell-deficient mice, whose immune response against tumor cells is suppressed, are more susceptible to lung cancer and have rapid tumor growth and progression.[22] In the NSCLC tumor microenvironment, NK cells have a clear anti-tumor role.[23] On one hand, NK cells rapidly produce granzyme and perforin after activation to kill tumor cells directly without major histocompatibility complex (MHC) restriction or prior sensitization, and on the other hand, NK cells induce tumor cell apoptosis by expressing TNF family members such as Fas Ligand (FasL) and tumor necrosis factor-alpha-related apoptosis-inducing ligand (TRAIL) and also can release numerous immunoreactive cytokines such as TNF-α and IFN-γ to kill tumor cells. The study suggests that in the tumor microenvironment of NSCLC, the activation of NK cells blocks tumor immune escape and thus brings a good prognosis.[24]

The role of dendritic cells in the tumor microenvironment of NSCLC

Dendritic cells play an important role in the induction of antagonistic NSCLC immune response.[25] Dendritic cells are also a key link in the initiation and regulation of the immune response. In the tumor microenvironment, dendritic cells are involved in recognizing tumor-associated antigens and presenting them to effector T cells, which in turn kill tumor cells. Subsequently, a large number of effector T cells are recruited to transfer to the tumor microenvironment and eventually inhibit neovascularization within the tumor. It should be further noted that the combination of DC cells with cytokine-induced killer cells (CIK cells) can enhance the anti-tumor effect. Dendritic cell-cytokine-induced killer cells (DC-CIK) combined with chemotherapy can improve PFS in postoperative patients with stage I - III NSCLC, which not only can reduce the adverse effects caused by radiotherapy, but also can improve the quality of life of patients.[26],[27] The mechanism of this cellular immunotherapy is to induce the generation of a large number of DC cells that bind to the corresponding tumor-associated antigens and stimulate the proliferation of CIK cells, thereby increasing the function of killing cancer cells and achieving an effector cell immune response.[28]

The role of myeloid-derived suppressor cells (MDSCs) in the tumor microenvironment of NSCLC

MDSCs are composed of stem cells, macrophages, granulocytes, and dendritic cell precursors.[29] MDSCs inhibit T cell proliferation and promote T cell apoptosis through the production of inducible nitric oxide synthase (iNOS), arginase-1, and reactive oxygen species (ROS) while inhibiting the activation of effector T cells by antigen-presenting cells and weakening the anti-tumor function of T cells. MDSCs can also induce Treg cells through the release of cytokines such as TNF-β and IL-10, which in turn suppress the immune function of NSCLC patients and finally promote the further development of NSCLC.[30] It has been shown that elevated expression of MDSCs is closely related to higher TNM stage, poor prognosis, and recurrent metastasis in NSCLC patients. Because, MDSCs can inhibit the anti-tumor activity of T cells and NK cells, and stimulate Treg cells to function, leading to tumor progression. Hence their number can be used as an important indicator to detect the immune function of NSCLC patients.[31] Considering the negative immunomodulatory effect of MDSCs, reducing their number and inducing their differentiation and maturation could improve the therapeutic effect of NSCLC.[32]

The role of macrophages in the tumor microenvironment of NSCLC

It was found that the type and number of macrophages in the tumor microenvironment of NSCLC could provide relatively reliable evidence for the early diagnosis and prognosis of tumors. Macrophages are generally classified into two types, M1 macrophages, and M2 macrophages. M1 type is a classically activated macrophage, which can further exert pro-inflammatory and anti-tumor functions by recruiting TNF, and IFN-γ, and inducing Th1 immune response through elevated expression of IL-12, IL-23, and other inflammation-related factors. The alternatively activated macrophage (M2-type) is induced by cytokines such as IL-4 and IL-13 and can secrete chemokines such as IL-10, which in turn promote Th2 type immune responses. In addition, M2-type macrophages are also involved in the regulation of important physiological processes such as angiogenesis, cell growth, and immunosuppression.[33] Macrophages in the NSCLC microenvironment are dominated by M2-type macrophages, which may promote tumor cell growth and metastasis by inducing upregulation of the expression of vascular endothelial growth factor-C (VEGF-C) and its specific receptor vascular endothelial growth factor receptor 3 (VEGFR3).[34] In addition, it can generate some functional enzymes to adjust the growth and metabolism of the tumor microenvironment and effectively participate in tumor metastasis.[35] M2 type macrophages also secrete cytokines such as IL-10 that inhibit the immune response, which in turn reduces the expression of cytokines such as IL-1, IL-12, and TNF-α thereby further promoting tumor growth.[36] It has also been found that NSCLC cells can recruit M2-type macrophages by expressing vascular endothelial growth factor (VEGF).[37] A recent study also suggested that an increase in the number of CD163+ M2 macrophages is an independent risk factor for NSCLC progression, and gauging its count can determine the progression of NSCLC.[38]

The role of mast cells in the tumor microenvironment of NSCLC

Mast cells are shown to promote the growth and metastasis of NSCLC tumors by promoting tumor blood vessel formation and secreting various growth factors and related hormones.[39] Mast cells within tumors are shown to play a key role in the stromal cells of NSCLC cancer nests and affect the prognosis of NSCLC.[40] Mast cells have two phenotypes, both of which have the potential to improve NSCLC prognosis. In addition, mast cells can promote massive proliferation of mast cells by secreting TNF-α while promoting the proliferation of T lymphocytes. The two promoting effects synergistically exert anti-tumor effects.[41]

In addition to immune infiltrating cells, the tumor microenvironment has other components that precisely regulate the important aspects of NSCLC development, progression, and metastasis. The mechanisms of action of various immune infiltrating cells in the tumor microenvironment of lung cancer can be seen in Table 1.

 

Table 1.
Table 1. Mechanism of action of various immune infiltrating cells in the tumor microenvironment of lung cancer and the corresponding citation numbers


OTHER COMPONENTS IN THE TUMOR MICROENVIRONMENT OF LUNG CANCER

Substances produced by anoxic environments

Due to the abnormal and rapid growth of tumor cells in lung cancer and the consequent increase in cellular oxygen consumption, the formation of a hypoxic microenvironment in the tumor tissue is highly likely to occur. It has now been found that the hypoxia inducible factor-1α (HIF-1α) controls tumor angiogenesis.[42] However, it has also been found that HIF-1α binds to HIF-1β under the combined stimulation of hypoxia and growth factors, which promotes the transcription of downstream genes such as vascular endothelial growth factor (VEGF), angiopoietin-2 (Ang-2) and other important factors, thereby adapting tissue cells to the hypoxic environment. HIF-1α activates the transcription and energy metabolism of downstream angiogenesis-related factors (VEGF, Ang-2), which is directly related to the prognosis of NSCLC, affecting the efficacy of radiotherapy and chemotherapy as well as the long-term prognosis of lung cancer.[43] In addition, under hypoxic conditions, the main metabolic form of tumor cells is the anaerobic glycolytic mode. Acidic substances such as lactic acid produced by glycolysis get discharged intracellularly by the proton pump of tumor cells in the form of hydrogen ions, which aggravates the local acidification state of TME, and this adverse condition is not conducive to the survival of immunocidal cells, which eventually leads to the proliferation of lung cancer cells.[44]

Exosomes

Exosomes are tiny vesicles, approximately 30 ~ 100 nm in diameter, that can be secreted by most cells.[45] Exosomes are mainly derived from intracellular lysosomal particles forming multivesicular body (MVB), which are released into the extracellular matrix after fusion of the MVB outer membrane with the cell membrane under specific physiological conditions. Exosomes can be found in a variety of body fluids such as blood, urine, saliva, and emulsions. Exosomes contain biological macromolecules such as proteins, lipids, and nucleic acids such as mRNA, miRNA, lncRNA, etc.[46],[47] Exosomes play an important function in intercellular communication due to their specific components. It both influences the development of malignancy and further regulates the process of tumor invasion and metastasis by recoding NSCLC target cell genes.[48] For example, exosomes secreted by NSCLC cells expressing PD-L1 reduce T-lymphocyte activity through the PD-1/PD-L1 signaling pathway, promoting NSCLC tumor growth and acting as an immune escape for tumor cells.[49] In addition, it was reported that miR-619-5p, an exosome secreted by NSCLC cells, is the most effective inducer of angiogenesis and can promote angiogenesis by inhibiting the expression of the oncogene RCAN1.4, which in turn promotes the growth and proliferation of NSCLC cells.[50] Turunen SP et. al., also found that exosomes secreted by lung adenocarcinoma cells can activate macrophages and increase the levels of matrix metalloproteinase-2 (MMP-2) and matrix metalloproteinase-9 (MMP-9), thus promoting the invasion and metastasis of lung adenocarcinoma cells.[51] In conclusion, exosomes can be used not only as biomarkers for the early diagnosis of NSCLC but also as biomarkers for predicting the therapeutic effects of NSCLC. Based on these studies, further research on the role and mechanism of exosomes in the growth and metastasis of NSCLC can provide new avenues for clinical diagnosis and treatment studies of NSCLC.

Extracellular matrix

The interaction of NSCLC tumor cells with the extracellular matrix influences tumor infiltration and metastasis. The extracellular matrix includes (1) collagen protein; (2) structural glycoprotein, such as fibronectin (FN) and laminin (LN); (3) elastin; (4) proteoglycan, etc. On one hand, the extracellular matrix (ECM) provides a scaffold, and barrier for the growth of tumor cells, weakening the attack of drugs and the immune system on tumor cells; on the other hand, tumor-associated desmocyte secrete growth factors or cytokines, which in turn induce tumor cells to initiate anti-tumor apoptotic pathways and DNA repair, thus enhancing the resistance of tumors to radiotherapy.[52],[53] Acosta et al. also found that basement membrane FN and mesenchymal FN were reduced or not detected when NSCLC malignant tumors were infiltrating and growing or even metastasizing. The result of reduced FN results in a decreased ability of cancer cells to adhere to the matrix, easy separation, and metastasis. The follow-up results showed that the loss of LN, FN and basement membrane type IV collagen around the cancer nests was closely related to the survival rate of NSCLC patients.[54] Therefore, the detection of LN, FN, and the degree of loss of basement membrane type IV collagen around the cancerous nest can be used as one of the indicators to determine the prognosis of patients after surgery.

The mechanisms of action of other substances in the tumor microenvironment of lung cancer and the summary of reference numbers can be found in Table 2.

 

Table 2.
Table 2. Mechanism of action of other substances in the tumor microenvironment of lung cancer and reference numbers


CURRENT USE OF TUMOR MICROENVIRONMENT IN LUNG CANCER TREATMENT

TME can provide raw materials and barriers for the growth of tumor cells and generate immune areas, which in turn provide the necessary conditions for tumor development and progression. In summary, TME has the following three important roles: (1) providing the necessary environment for tumor growth; (2) attenuating the effects of antitumor drugs; and (3) local immune response in an immunosuppressed state, which helps tumor cells evade immune surveillance.[55] In the early stage of tumor growth, an inflammatory microenvironment is formed due to the recruitment and activation of immune cells and related stromal components by tumor cells, thus suppressing the tumor. However, after experiencing persistent tumor antigen stimulation and immune activation responses, the microenvironment is unable to function normally because the relevant effector cells are in a depleted state.[56] One study found that the immune microenvironment in NSCLC is predictive of prognosis after surgery.[57] This suggests that tumor treatment and progression are closely related to the tumor microenvironment. Tubin S. et. al., found that treatment of advanced NSCLC can be improved by sparing the immune microenvironment around the tumor, further demonstrating the significance of studying the tumor microenvironment for tumor treatment.[58] Some investigators retrospectively analyzed the pathological specimens and relevant clinical data of 59 patients, confirmed of primary lung cancer and admitted to hospital between 2013-2015, and performed multifactorial analysis by COX regression. Disease-free survival (DFS) was found to be significantly longer in immune-exclude tumor patients than in immune-inflamed tumor and immune-desert tumor patients; tertiary lymphoid structures (TLSs), immunophenotyping (immune-desert tumor), and later T-stage were independent risk factors for DFS in lung cancer patients. Close attention to the tumor immune microenvironment (tertiary lymphoid structure and immunophenotyping) is of great value in predicting the prognosis of primary lung cancer.[59]


CONCLUSION

TME is a complex and variable environment that provides a place for tumor cells to grow and develop. various components in TME are closely related to the occurrence and metastasis of tumor cells. TME is a dynamic site in constant change, where some inflammatory factors can promote tumor cell proliferation and metastasis by promoting vascular and lymphatic vessel production or inhibiting immune cells' own functions, while other inflammatory factors can inhibit tumor cell growth by enhancing the activity of immune cells. Theoretically, the components of TME do not undergo mutations and genetic abnormalities like tumor cells, and therefore targeted therapies for TME are promising. A better understanding of the interactions between TME and tumor cells is essential for finding and developing new therapeutic approaches. Therefore, it is necessary to study the mechanisms by which multiple components of TME jointly affect tumor cells, which can help improve the diagnosis, treatment, and prognosis of lung cancer and increase the survival rate of lung cancer patients.

In conclusion, studying the count and proportion of immune cells in the microenvironment of lung cancer and their role in tumor development can provide an important reference for early diagnosis, prognosis judgment, and target selection of lung cancer. Of course, some of these problems still need to be solved, and the interaction network of various immune cells and the role of different cytokines on different immune cells still need to be further studied, which will also open a new chapter for lung cancer immunotherapy.

 

FINANCIAL SUPPORT AND SPONSORSHIP

This study was supported by a grant from Suzhou Science and Technology Bureau: Innovation in medical and health science and technology (No. SKJY2021116, to Yong Yang).

 

CONFLICTS OF INTEREST

There are no conflicts of interest.

 

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Not applicable.


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Yasuka Azuma1,2, Masako Mizuno‑Kamiya3, Eiji Takayama1, Harumi Kawaki1, Toshihiro Inagaki4, Eiichi Chihara2, Yasunori Muramatsu5, Nobuo Kondoh1


“Eating” Cancer Cells by Blocking CD47 Signaling: Cancer Therapy by Targeting the Innate Immune Checkpoint

Yi‑Rong Xiang, Li Liu


Glycosylation is Involved in Malignant Properties of Cancer Cells

Kazunori Hamamura1, Koichi Furukawa2


Biomarkers in Molecular Epidemiology Study of Oral Squamous Cell Carcinoma in the Era of Precision Medicine

Qing‑Hao Zhu1*, Qing‑Chao Shang1*, Zhi‑Hao Hu1*, Yuan Liu2, Bo Li1, Bo Wang1, An‑Hui Wang1


I‑Kappa‑B Kinase‑epsilon Activates Nuclear Factor‑kappa B and STAT5B and Supports Glioblastoma Growth but Amlexanox Shows Little Therapeutic Potential in These Tumors

Nadège Dubois1, Sharon Berendsen2, Aurélie Henry1,2, Minh Nguyen1, Vincent Bours1,
Pierre Alain Robe1,2


Suppressive Effect of Mesenchymal Stromal Cells on Interferon‑g‑Producing Capability of Spleen Cells was Specifically Enhanced through Humoral Mediator(s) from Mouse Oral Squamous Cell Carcinoma Sq‑1979 Cells In Vitro

Toshihiro Inagaki1,2, Masako Mizuno‑Kamiya3, Eiji Takayama1, Harumi Kawaki1, Eiichi Chihara4, Yasunori Muramatsu5, Shinichiro Sumitomo5, Nobuo Kondoh1


An Interplay Between MicroRNA and SOX4 in the Regulation of Epithelial–Mesenchymal Transition and Cancer Progression

Anjali Geethadevi1, Ansul Sharma2, Manish Kumar Sharma3, Deepak Parashar1


MicroRNAs Differentially Expressed in Prostate Cancer of African‑American and European‑American Men

Ernest K. Amankwah


The Role of Reactive Oxygen Species in Screening Anticancer Agents

Xiaohui Xu1, Zilong Dang2, Taoli Sun3, Shengping Zhang1, Hongyan Zhang1


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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