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PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
This study confirmed circAPP as a gene modifier of miR-6838-5p.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
miR-6838-5p is involved in a series of biological processes in cancer.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
miR-6838-5p is downregulated in osteosarcoma, and induction of miR-6838-5p suppresses tumor metastasis.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
In addition, miR-6838-5p is also involved in myocardial ischemia-reperfusion injury and cerebral hemorrhage injury.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Here, this study implied that miR-6838-5p was lowly expressed in both GIST, and suppression of miR-838-5p mitigated the effect of silencing circAPP.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
This study further showed that, mechanistically, CDV3 was a target of miR-6838-5p.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
CDV3 was documented as an unidentified gene in breast cancer in 1999 and it is overexpressed in hepatocellular carcinoma.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
This study also observed the abundance of CDV3 in GIST, and inhibition of CDV3 impaired circAPP restoration-mediated influences on GIST cell proliferation and the Warburg effect.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Although this study has partially elucidated the function of circAPP in GIST, further research is required in order to develop effective GIST treatments.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
On the one hand, due to the insufficient sample size, the correlation of circAPP with pathological T-staging and poor prognosis of GIST patients has not been established.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
On the other hand, the expression of most circRNAs is significantly correlated with GIST tumor size, mitotic number, and malignant degree by constructing circDNA expression profiles, and does not correlate with tumor site, but no experiments have been performed to verify this idea.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The exact role of this still needs to be further explored, and the molecular expression of the circAPP/miR-6838-5p/CDV3 axis and whether its mechanism is affected by differences in primary sites is a direction for our future in-depth research.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Despite its important role, miR-6838-5p is not the only target regulated by circAPP.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Whether other miRNAs are involved in circAPP affecting Warburg effect of GIST and the related specific mechanism still needs to be further explored.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
This study demonstrates that a novel circRNA, circAPP, is upregulated in GIST tissues and cells and that upregulating circAPP expression promotes the Warburg effect by targeting the miR-6838-5p/CDV3 axis, which is of great significance for the malignant proliferation and metastasis of GIST.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The results provide important data support for the future clinical treatment of GIST and the development of targeted drugs.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The datasets used and/or analyzed during the present study are available from the corresponding author upon reasonable request.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Written informed consent for publication was obtained from all participants.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
All subjects were approved by the Affiliated Hospital of Inner Mongolia Minzu University (n° 201211Y62).
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Written informed consent was obtained from each subject.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The animal experiments were complied with the ARRIVE guidelines and performed in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The experiments were approved by the Institutional Animal Care and Use Committee of the Affiliated Hospital of Inner Mongolia Minzu University (n° 201306YT2).
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
GeTu ZhaoRi and ChunJuan Wang designed the research study.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
XianJing Zeng and JinHua Yuan performed the research.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
GeTu ZhaoRi and XianJing Zeng provided help and advice.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
ChunJuan Wang and JinHua Yuan analyzed the data.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
GeTu ZhaoRi and ChunJuan Wang wrote the manuscript.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
JinHua Yuan reviewed and edited the manuscript.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
All authors contributed to editorial changes in the manuscript.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
All authors read and approved the final manuscript.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
Not applicable.
PMC11269792
CircRNA amyloid precursor protein by competitive adsorption of microRNA-6838-5p mediates CDV3 expression to enhance malignant behavior and Warburg effect in Gastrointestinal Stromal Tumor
The authors declare no conflicts of interest.
PMC10669128
Preclinical Models of Visceral Sarcomas
Visceral sarcomas are a rare malignant subgroup of soft tissue sarcomas (STSs).
PMC10669128
Preclinical Models of Visceral Sarcomas
STSs, accounting for 1% of all adult tumors, are derived from mesenchymal tissues and exhibit a wide heterogeneity.
PMC10669128
Preclinical Models of Visceral Sarcomas
Their rarity and the high number of histotypes hinder the understanding of tumor development mechanisms and negatively influence clinical outcomes and treatment approaches.
PMC10669128
Preclinical Models of Visceral Sarcomas
Although some STSs (~20%) have identifiable genetic markers, as specific mutations or translocations, most are characterized by complex genomic profiles.
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, identification of new therapeutic targets and development of personalized therapies are urgent clinical needs.
PMC10669128
Preclinical Models of Visceral Sarcomas
Although cell lines are useful for preclinical investigations, more reliable preclinical models are required to develop and test new potential therapies.
PMC10669128
Preclinical Models of Visceral Sarcomas
Here, we provide an overview of the available in vitro and in vivo models of visceral sarcomas, whose gene signatures are still not well characterized, to highlight current challenges and provide insights for future studies.
PMC10669128
Preclinical Models of Visceral Sarcomas
Visceral sarcomas are rare malignancies belonging to soft tissue sarcomas (STSs).
PMC10669128
Preclinical Models of Visceral Sarcomas
STSs are aggressive tumors which arise from the malignant transformation of mesenchymal cells and comprise very heterogeneous entities, accounting for ~1% of all adult human malignancies .
PMC10669128
Preclinical Models of Visceral Sarcomas
Visceral sarcomas mainly occur in adults and include several histotypes, including liposarcoma (LPS) and angiosarcoma (AS), as well as some leiomyosarcomas (LMSs) and undifferentiated pleomorphic sarcomas (UPSs).
PMC10669128
Preclinical Models of Visceral Sarcomas
The most common type of visceral sarcoma is the gastrointestinal stromal tumor (GIST), which arises from the muscle wall of the digestive tract .
PMC10669128
Preclinical Models of Visceral Sarcomas
All these neoplasms are believed to derive from the transformation of a common multipotent cell of origin, which can differentiate into specific lineages .
PMC10669128
Preclinical Models of Visceral Sarcomas
The precise mechanisms associated with sarcoma development remain to be clarified because of the rarity of the disease and the large number of subtypes .
PMC10669128
Preclinical Models of Visceral Sarcomas
Indeed, STSs comprise over 70 different histotypes, each characterized by a distinct morphology and molecular aberrations, which usually correspond to a specific clinical course and to specific therapeutic approaches .
PMC10669128
Preclinical Models of Visceral Sarcomas
Only a small percentage of tumors (~20%) displays distinct diagnostic markers: recurrent genetic alterations, such as specific mutations (e.g., KIT activating mutation in gastrointestinal stromal tumors) and chromosomal translocations (observed in approximately 20% of STSs), or complex genomic profiles and mutated tumor suppressor genes, including TP53 and retinoblastoma 1 (RB1) .
PMC10669128
Preclinical Models of Visceral Sarcomas
However, the majority of STSs have nonspecific genetic alteration with a complex karyotype .
PMC10669128
Preclinical Models of Visceral Sarcomas
Despite their heterogeneity, the first-line treatment for most sarcoma subtypes is still limited to traditional surgery, with or without adjuvant or neoadjuvant radiotherapy, and represents the most common treatment for localized sarcomas.
PMC10669128
Preclinical Models of Visceral Sarcomas
Unfortunately, most patients develop metastasis, which is treated with chemotherapy, principally doxorubicin and ifosfamide, two main active agents reaching a response rate higher than 20% in advanced STSs .
PMC10669128
Preclinical Models of Visceral Sarcomas
Nonetheless, the high degree of heterogeneity combined with the poor knowledge of tumor molecular drivers limits treatment efficacy, especially in the case of unresectable, recurrent, or metastatic disease.
PMC10669128
Preclinical Models of Visceral Sarcomas
Moreover, due to the prevalence of many molecular aberrations within specific sarcomas, few STSs are therapeutically targeted with a 5-year survival rate of ~50% and <10% for localized and metastatic STSs, respectively .
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, the identification of new genomic and molecular therapeutic targets and preclinical testing of personalized therapies remain urgent unmet medical needs, especially for visceral sarcomas.
PMC10669128
Preclinical Models of Visceral Sarcomas
However, this requires the development of reliable and predictive tumor models to test only the most promising therapies in clinical trials.
PMC10669128
Preclinical Models of Visceral Sarcomas
To date, the most used preclinical models in the field include genetically engineered or transgenic mice, xenografts, and PDXs (patient-derived xenografts) .
PMC10669128
Preclinical Models of Visceral Sarcomas
However, these models present significant limitations, including high management costs, lengthy experimental processes, and the variable adherence of the animal model to human pathology.
PMC10669128
Preclinical Models of Visceral Sarcomas
In this regard, given the rarity of visceral sarcomas, several studies focus on the most common STSs, mainly skeletal sarcomas.
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, in this review, we aim to provide an overview of the current in vitro and in vivo models developed for visceral sarcomas, to highlight related challenges and offer insights for forthcoming research.
PMC10669128
Preclinical Models of Visceral Sarcomas
Historically, cell models have been the primary research tool for the study of STSs, providing valuable insights into sarcoma biology, such as tumor progression and metastasis.
PMC10669128
Preclinical Models of Visceral Sarcomas
Nonetheless, cancer cell lines present several limitations.
PMC10669128
Preclinical Models of Visceral Sarcomas
For instance, prolonged cell culture can determine the onset of secondary genetic changes, including copy number variations and transcriptomic drifts, or specific clone selection, leading to biased results.
PMC10669128
Preclinical Models of Visceral Sarcomas
Additionally, the research findings suggest that tumor cell lines are more similar to one other than to the original clinical samples, which explains their limited utility.
PMC10669128
Preclinical Models of Visceral Sarcomas
In fact, the in vitro and in vivo drug response of certain cell lines was not frequently recapitulated in numerous clinical trials .
PMC10669128
Preclinical Models of Visceral Sarcomas
Many sarcoma cell lines have been established over the years.
PMC10669128
Preclinical Models of Visceral Sarcomas
However, several histological subtypes are largely underrepresented and only a few well-characterized cell lines are publicly available; moreover, many of them are not fully representative of the corresponding tumor tissue .
PMC10669128
Preclinical Models of Visceral Sarcomas
Hattori and colleagues investigated the current status of the reported sarcoma cell lines, observing that only 139 out of 819 sarcoma cell lines, named according to the WHO classification, have been deposited into public cell banks.
PMC10669128
Preclinical Models of Visceral Sarcomas
They also observed that among the 189 histotypes listed in the WHO classification, only 45 have corresponding cell lines .
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, an increased number of cell lines representing numerous sarcoma histological subtypes is necessary to effectively understand the complexity of the disease and enhance the utility of tumor cell cultures in cancer research.
PMC10669128
Preclinical Models of Visceral Sarcomas
Table 1 shows some examples of the available human cell lines derived from different sarcomas.
PMC10669128
Preclinical Models of Visceral Sarcomas
In vitro studies with these cell lines have been fundamental in sarcoma research, mainly for drug screening, but also for a better comprehension of the mechanisms behind tumor progression and metastasis .
PMC10669128
Preclinical Models of Visceral Sarcomas
An excellent example of successful translational research is represented by the human GIST cell lines widely employed to predict the role of c-KIT signaling and to evaluate the efficiency of imatinib (IM) as a new targeted therapy.
PMC10669128
Preclinical Models of Visceral Sarcomas
Different KIT mutations affect the apoptotic signal transduction caused by imatinib in GISTs, as observed by Noma and colleagues in the GIST-T1 and the GIST882 lines, carrying activating mutant KIT.
PMC10669128
Preclinical Models of Visceral Sarcomas
However, development of imatinib resistance is frequent, and understanding the underlying mechanisms of this event is crucial to establish new treatment strategies .
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, alternative approaches have been proposed, such as the inhibition of KIT-dependent signaling pathways or their indirect inhibition by using HSP90 inhibitors (HSP90i).
PMC10669128
Preclinical Models of Visceral Sarcomas
Preclinical studies on tumor cell lines have extensively investigated small-molecule HSP90i, which appears to be a promising strategy to overcome imatinib resistance .
PMC10669128
Preclinical Models of Visceral Sarcomas
Some inhibitors are currently undergoing phase II/III clinical trials in cancer patients, either as standalone treatments or in combination with traditional chemotherapy .
PMC10669128
Preclinical Models of Visceral Sarcomas
The effects of new classes of anti-cancer agents involved in epigenetic and non-epigenetic regulation, alone or in combination with other anti-cancer therapies, are widely investigated in tumor cell lines .
PMC10669128
Preclinical Models of Visceral Sarcomas
In this regard, Mühlenberg’s group observed that the histone deacetylase (HDAC) inhibitors (HDACi) SAHA and panobinostat (LBH589) hinder cell growth in KIT-positive (GIST-T1, GIST822, and GIST48) but not in KIT-negative cells (GIST62, GIST48B, and GIST522).
PMC10669128
Preclinical Models of Visceral Sarcomas
This proves that HDACi primarily act by targeting the oncogenic KIT and exert their strong antiproliferative and proapoptotic effects in both IM-sensitive and IM-resistant GISTs.
PMC10669128
Preclinical Models of Visceral Sarcomas
The authors also provided preclinical evidence of the disease-specific impact of HDACi on KIT-positive GISTs, which has the potential to be translated into therapeutic activity .
PMC10669128
Preclinical Models of Visceral Sarcomas
To overcome IM resistance in GIST patients, other drugs have been tested over the years, such as sorafenib, which displays clinical activity against TKI-resistant GISTs.
PMC10669128
Preclinical Models of Visceral Sarcomas
Heinrich and colleagues tested this compound in a panel of KIT- and PDGFRA-mutant kinases expressed by the transient transfection of the reference cell lines (GIST-T1/829 and IM-resistant GIST-T1).
PMC10669128
Preclinical Models of Visceral Sarcomas
Sorafenib showed a good IC50 potency against all IM-resistant mutations, except those involving KIT codon 816 and PDGFRA codon 842 .
PMC10669128
Preclinical Models of Visceral Sarcomas
Among the available liposarcoma cell lines, LPS141 cells are valid candidates to test new anti-cancer drugs, while T449 and T778 are more suitable to study tumor progression and recurrence, as demonstrated by Stratford‘s team.
PMC10669128
Preclinical Models of Visceral Sarcomas
A correlation between high proliferation rate and in vivo tumor-forming ability was also observed .
PMC10669128
Preclinical Models of Visceral Sarcomas
Simultaneously, cell lines derived from dedifferentiated liposarcomas carrying 12q13-15 region amplification (including MDM2 and CDK4 genes) represent an excellent preclinical model for the study of well-differentiated (WDLPS) and dedifferentiated (DDLPS) liposarcoma development and proliferation.
PMC10669128
Preclinical Models of Visceral Sarcomas
The p53 significance in both cancer development and therapy response has aroused interest in terms of the p53–MDM2 interaction as a possible target for small-molecule therapy over the years .
PMC10669128
Preclinical Models of Visceral Sarcomas
MDM2 inhibition results in antitumor activity and increased apoptosis, as demonstrated by Müller and colleagues in an in vitro study conducted on WDLPS (T449 and T778) and DDLPS (FU-DDLS-1) TP53 wild-type and MDM2 amplified cell lines, indicating a potential link between treatment response and the mutational status of these genes .
PMC10669128
Preclinical Models of Visceral Sarcomas
Unfortunately, for some visceral sarcoma subtypes, very few cellular models are available, as in the case of AS .
PMC10669128
Preclinical Models of Visceral Sarcomas
Krump-Konvalinkova and Bittinger were able to establish the human endothelial AS-M cell line from a cutaneous angiosarcoma.
PMC10669128
Preclinical Models of Visceral Sarcomas
These cells displayed endothelial characteristics, as CD31 expression, and might be considered a suitable model to investigate human endothelial cells .
PMC10669128
Preclinical Models of Visceral Sarcomas
Several studies have also been conducted to develop three-dimensional culture systems for sarcomas, with the aim of better resembling the surrounding extracellular matrix and overcoming the disadvantages of two-dimensional cell cultures.
PMC10669128
Preclinical Models of Visceral Sarcomas
Maintaining cells in a 2D culture results in morphological changes, leading to altered gene and protein expression and different cell behavior compared to the original tissue.
PMC10669128
Preclinical Models of Visceral Sarcomas
3D cellular models can overcome these limitations since the architecture of the original tissue and the native cell-cell and cell–extracellular matrix interactions are preserved .
PMC10669128
Preclinical Models of Visceral Sarcomas
3D cultures are also valuable tools for studying the microenvironment’s influence on cells within a tumor and their response to drug treatment .
PMC10669128
Preclinical Models of Visceral Sarcomas
However, inducing sarcoma cell proliferation in a 3D culture system is more challenging than in a 2D culture.
PMC10669128
Preclinical Models of Visceral Sarcomas
This can be explained by the impact of the microenvironment on sarcoma cell proliferation, including angiogenic capability, and by the presence of distinct cell–matrix adhesion molecules in 3D and 2D models .
PMC10669128
Preclinical Models of Visceral Sarcomas
As previously discussed, cells of a specific sarcoma subtype can differentiate into multiple lineages in vitro in the presence of certain inducing factors.
PMC10669128
Preclinical Models of Visceral Sarcomas
Thus, it is clear that not only the cell of origin but also the tumor microenvironment plays a crucial role in determining the final tumor phenotype .