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PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
To date, no studies have associated lncRNA treatment to altered expression of KIT gene and mutations in GIST, despite the fact that some lncRNAs that have been shown to regulate KIT expression in GIST and are associated with imatinib resistance .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
For example, miRNA sponges is a kind of artificial transcripts that contains multiple miRNA binding sites to trap and sequester it .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Although this tool can simultaneously inhibit miR-221/miR-222 in tumour cells such as breast cancer cells and recently a PhaseI study of the frst-in-class locked nucleic acid (LNA) miR-221 selective inhibitor shows good safety and SD + PR in refractory advanced cancer patients .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The above suggests promising therapeutic ability in targeting ncRNA and thereby modulating KIT expression warranted future investigation.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
And intriguingly, use of an aptamer-based method for KIT expression targeted detection of GIST was successfully executed in vitro and in vivo, and intracellular delivery of TKIs to signaling terrace via anti-KIT DNA aptamer or modified RNA aptamers to inhibit the activity of KIT kinase, heralding a novel avenue in GIST treatment .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
LMTK3 increases KIT expression via the speedup of translation rate of KIT transcripts.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
LMTK3 knockdown not only directly decreases KIT protein translation, but also inhibit the expression of PKC and KIT phosphorylation, indicating LMTK3 as a druggable target.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Mutated KIT protein is usually detained within intracellular organelle and chemical inhibition for intracellular transport to Golgi or specific organelles-targeting TKIs by chemical modifications seems a promising therapeutic strategy .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Intracellular delivery of TKIs to signaling terrace via anti-KIT DNA aptamer or modified RNA aptamers to inhibit the activity of KIT kinase, heralding a novel avenue in GIST treatment .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Homoharringtonine (HHT) is a first-in-class inhibitor of protein biosynthesis and is FDA-approved for the treatment of chronic myeloid leukemia (CML) that is resistance to at least two lines of treatment with TKIs.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
In vivo and in vitro experiment, HHT showed significant anti-proliferation and apoptosis-induction with a notable reduction of KIT protein and subsequent decrease of KIT activation and downstream signaling, while KIT mRNA levels were slightly affected .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Bortezomib is a dipeptide boronic acid inhibitor of the 20S proteasome.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
It synergistically augmentes the efficacy of TKIs in multiple myeloma and mantle cell lymphoma.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Bortezomib can bind to Cbl, an E3 ubiquitin-protein ligase, destabilizing the c-KIT-Hsp90Β-Apaf-1 complex and releasing Apaf-1; then KIT was unleashed from the complex, and be internalized and degraded in the cytoplasm of GIST cells.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Treatment with bortezomib can enhance dasatinib-induced apoptosis in GIST T1 cells and increase the inhibition effect of IM on cell proliferation and invasion in GIST 882 cells.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
HSP (heat-shock protein) is a multi-protein chaperone, acting as a key mediator for the correct folding, intracellular disposition, and proteolytic turnover of the proteins which are responsible for cell growth and survival.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The fundamental chaperoning role of HSPs is subverted, especially heat-shock protein of 90 KD (HSP 90), leading to the maintenance of mutant proteins with its gain-of-function of protecting cancer cells from onco-stress .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
HSP 90 inhibitors, IPI-504 and AT13387 can decrease the KIT protein level, showing obvious antitumor activity in GIST as a single agent, and they are more potent when in combination with IM or sunitinib .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
HSP90AA1, one of the client proteins of HSP90, is a major chaperone protein for KIT oncoprotein with a protective role from its degradation in GIST.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Other HSP90 inhibitors, including 7-allylamino-17- demethoxygeldanamycin (17-AAG) and IPI-493, also exhibit the inhibition effect in cell growth due to the degradation of mutant KIT protein via both proteasome- and autophagy-dependent pathways .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Novel HSP90 inhibitors, NVP-AUY922 and TAS-116, can downregulate both total and phosphorylated KIT proteins, and mTOR inhibitors can enhance the inhibitory role of NVP-AUY922 in GIST cells [205–207].
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Intriguingly, the HDAC inhibitors (HDACi), SAHA and LBH589 can epigenetically attenuate the activity of HSP90 by its acetylating on HSP90 gene, with the resultant degradation of KIT protein.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
In vitro and vivo experiments, HDAC inhibitors presented with a synergistic effect in the IM-treated GIST cells .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Although there are many drugs directly targeting HSP 90 on its co-factors, challenges remain in clinical translation for its endurable toxicity .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Genome-wide functional screening identifies CDC37 as a crucial HSP90-cofactor for KIT oncogenic expression in gastrointestinal stromal tumors .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
PBOX-15, a novel microtubule-targeting agent (MTA) reduced CKII expression, an enzyme which regulates the expression of CDC37, which downregulate KIT expression via CDC37-HSP90 mediated KIT degradation .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
These findings indicate the potential of PBOX-15 to improve the apoptotic response of IM in GIST cells and provide a more effective treatment option for GIST patients.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Targeting the Hh pathway can reduce KIT mRNA and re-enhance the sensitivity of GIST cells to TKIs in in vivo experiments.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
GI1/2 inhibitor, arsenic trioxide, decreases KIT expression and reduces cell viability by significantly increasing the bonding of GLI3 to the KIT promoter, demonstrating efficacy in the Imatinib-sensitive and Imatinib-resistant GIST cells .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The p55PIK specific inhibitor, TAT-N24, can abrogate the resistance of GIST cells to Imatinib and dramatically down-regulated KIT expression and enhanced the Imatinib effectiveness in an NF-κB -dependent manner as validated in the PDX tissue from IM-resistance-GIST patients.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Inhibitors of the PI3K pathway have already made significant contributions to GIST, with the dual PI3K/mTOR inhibitor voxtalisib, the pan-PI3K inhibitor pilaralisib, and the PI3K-restricted inhibitor alpelisib all reducing GIST cell proliferation .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The emerging PI3K or P55PIK inhibitors, including Copanlisib, showed high efficacy and low toxicity in IM-resistant GIST .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
KIT and FGFR3 have a direct interaction in GIST cells, and BGJ398, a selective FGFR1-4 inhibitor, can re-sensitize GIST to IM in in vitro and in vivo experiments .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
With the combination of BGJ398 and sunitinib, SDH-GIST patients may get better outcomes .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Nintedanib, first approved by FDA for idiopathic pulmonary fibrosis, overcame not only resistance induced by KIT mutations, but also ERK-reactivation-mediated resistance induced by FGF upregulation .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The combination of FGFR inhibitor PD173074 and IM showed highly synergistic effect in IM-resistant GIST cells .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The phase Ib study of BGJ398 and imatinib in the treatment of IM-refractory advanced GIST showed that the primary endpoint was achieved in which approximately 25% (3/12) of patients sustained stable disease for more than 32 weeks .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
That suggests that FGF inhibitors like BGJ398 might be a promising treatment strategy combination with TKIs after imatinib resistance.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Different genotypes of KIT mutations are associated with diversified responses to specific TKIs.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Primary mutations often appear in KIT Exon 9 and 11, and the latter is more sensitive to Imatinib with better progression-free survival (PFS), and median overall survival (OS).
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
However, IM showed almost ineffective for secondary KIT mutations including exon 13, 14 and exon 17, 18 .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
In the setting of second and beyond, sunitinib had better inhibitory effect on KIT mutants with exon 9 or 11/13 or 14 double mutations than IM, but regorafenib, dasatinib, nilotinib and sorafenib was largely effective to inhibit the phosphorylation of KIT with secondary exon 17 mutation [217–219].
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
In animal model, compared to control mice with a single V558Δ Kit mutation, mice with a double V558Δ; V653A Kit mutation had increased tumor oncogenesis and associated KIT-dependent STAT activation, while cabozantinib was more effective in overcoming resistance than sunitinib.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
In vitro, V654A mutation encoded by KIT exon 13 was intermediately sensitive to anlotinib.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Moreover, anlotinib was able to partly suppress the activation loop mutation D820A from exon 17 while another activation loop mutation N822K, also from exon 17, was resistant to anlotinib .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
BLU-263 (avapritinib), targeting KIT D816V, is currently being evaluated in the phase 2/3 HARBOR study of patients with ISM .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Recently, PLX-9486 (Bezuclastinib), an active-state TK inhibitor with activity against mutations in KIT exons 9, 11, 17, and 18, including D816V, has several clinical trials and shows great clinical benefit with an acceptable safety profile either using alone or in combination with other TKIs .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Collectively, continued KIT-dependency is a typical characteristic of GIST, and complete tumor eradication of non-operable GIST may require a powerful inhibition of the KIT pathway, which is potentially attained by targeting both the tyrosine kinase and the abnormal overexpression of KIT protein.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Currently, seven drugs targeting KIT mutations have already been approved by the FDA for the treatment of advanced-stage GIST (imatinib, sunitinib, regorafenib, ripretinib, avapritinib, larotrectinib and entrectinib), all of which are TKIs .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Although these agents can be very effective for treating certain GIST subtypes, challenges remain and novel therapeutic approaches are needed .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
GIST is inherently resistant to radiotherapy and cytotoxic drug , albeit some end-stage cases with GIST treated by radiotherapy can achieved palliative pain-relief [226–228].
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Immunotherapy is a promising hotspot in the treatment of tumors , but the efficacy cannot be determined in the existing cases of GIST .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Efforts continue to be made in immunotherapy as well as radiation therapy for GIST [232–235].
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
It has been speculated that special regulation network exclusively in KIT-driven GIST, on the gene coding, epigenetic modification, and protein level.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Available evidence that the decrease of KIT expression via HSP90- chaperone protein for the reversal of IM resistance has become a realistic possibility in clinical application .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
This fact further improves KIT value not only as a diagnosis marker, but also could be a predictive marker for the therapeutic treatments targeting KIT expression.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Thus, the development of standardized approaches to measure KIT expression in different molecule level or various cellular organelles will make it possible.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The emerging molecules which were unravelled recently such as FOFX1, ETV1, which have potentially sculpted the innate link of GIST and its derivation ICC.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Because ETV1 also regulates the expression of ICC gene signatures and is crucial for ICC cell survival, as well as its upstream FOFX1 do .
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
So deeply exploring the key gene expression and regulation process of ICC lineage-specific differentiation or the compelling molecules impact its physical function such as gut motility, may offer the possibility of novel promising targets.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Additionally, these KIT auto-regulation positive loop mediated by the components of the PI3K or MAPK signal pathways strengthened the interest in the conjoined inhibition of these two pathways as potential therapeutic strategy, thus support the continuous endeavor for the development of novel drugs in this field in the setting of IM-resistant GIST, although how to decrease the toxicity of these combination is a key unanswered question.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The crosstalk between various RTK is the common phenomenon in cell body, this KIT in GIST is not an exception.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Evidence chains range from basic research to pre- or early-phase clinical trials consolidated the knowledge that FGF/FGFR signal pathway is a vital target for KIT–mutated GIST via multifaceted mechanism including decreased KIT expression, expected for large-size random clinical trial to confirm and propel FGFR-targeted therapy in GIST patients in the future.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Taken together, there is no doubt that KIT oncoprotein remains a therapeutic target for novel drug or drug-repurpose because the heterogeneous mutations within KIT oncogene generated for the reactivation of KIT signal cascade, contributing to the disease progression in most cases after the failure of IM and even multiple-lines of TKIs.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Current research is evaluating the agents target the high level of KIT expression, either alone or in combination with imatinib or other TKIs, aiming to circumvent the high rate of resistance.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
However, several research questions remain unanswered including (Fig. 4) (Table 3):what is the relationship between KIT activation and KIT upregulation, the rate-limiting processes for abnormal KIT expression in GIST,if the underlying mechanism of KIT expression is exclusive to GIST, but not in WT KIT,imatinib treatment induces the change of tumor microenvironment (TME) , if it in turn affected the expression of KIT gene,upon the IM treatment, c-KIT oncoprotein was substantially up-regulated, which was considered as a protective mechanism for GIST cells, if these from the release of negative feedback, such as sprouty homolog 4 (SPRY4) ,the protein of KIT mutants usually mislocated within intracellular organelles, such as golgi apparatus, how to detect them used for the guidelines of drugs targeting KIT expression?Fig.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
4Perspective of KIT in GIST.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
KIT expression and its downstream activation pathway regulation mechanism needs to be taken seriously as its mechanism is not fully explained.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
KIT mutations are the main culprit responsible for the development of GIST and the primary/secondary resistance of imatinib.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The epigenetic modification of KIT mutation and the study of new mutations’ targets are worthy of further study.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Further treatment options may consider combining TKIs with other drugs that target KIT and their signaling pathway to achieve better efficacy and address drug use in resistant patientsTable 3Clinical trials of the drugs targeting KIT expression in GISTDrugCategoryCombinationPhaseStatusSponsor locationNCT NumberEntacaponeFTO demethylation inhibitorImatinib1Active, not recruitingChina04006769BBI503BRD4/2TerminatedCanada02232620BBI503BRD4/1CompletedUS02354898BIIB021HSP90 inhibitor/2CompletedUS00618319IPI-504HSP90 inhibitor/1CompletedUS00276302PimitespibHSP90 inhibitorImatinib1RecruitingJapan05245968AT13387HSP90 inhibitorImatinib2CompletedUS01294202GanetespibHSP90 inhibitor/2CompletedUS01039519AUY922HSP90 inhibitor/2UnknownTaiwan, China01389583AUY922HSP90 inhibitor/2CompletedUS01404650IPI-504HSP90 inhibitor/3TerminatedUS00688766BKM120PI3K inhibitorImatinib1CompletedUS01468688BYL719PI3Kα inhibitorImatinib1CompletedUS01735968CopanlisibPI3K inhibitorBAY18953441Not recruitingUS05010096PerifosineAKT inhibitorImatinib2CompletedUS00455559PerifosineAKT inhibitorSunitinib1CompletedCanada00399152RAD001(Everolimus)mTOR inhibitorImatinib1/2CompletedUS01275222RAD001(Everolimus)mTOR inhibitor//Available/03493152TemsirolimusmTOR inhibitor//RecruitingGermany00700258RAD001(Everolimus)mTOR inhibitor/2CompletedGermany00767819MEK162 (Binimetinib)MEK inhibitorRipretinib1/2WithdrawnUS05080621MEK162(Binimetinib)MEK inhibitorPexidartinib1CompletedUS03158103MEK162(Binimetinib)MEK inhibitorImatinib1/2Active, not recruitingUS01991379MEK162(Binimetinib)MEK inhibitorRipretinib1/2WithdrawnUnknown05080621TrametinibMEK inhibitorPazopanib2WithdrawnUS02342600Selumetinib(AZD6244)MEK inhibitor/2WithdrawnUS03109301SorafenibRaf inhibitor/2CompletedKorea01091207Sorafenib TosylateRaf inhibitor/2Active, not recruitingUS00265798THE-630Pan-KIT inhibitor/1/2RecruitingUS05160168LinsitinibIGF-1R inhibitor/2CompletedUS01560260BGJ398Pan-FGFR inhibitorImatinib1bCompletedUS02257541VismodegibHedgehog inhibitor/1/2CompletedUS01154452Arsenic trioxideGI1/2/1CompletedUS00124605Arsenic trioxideGI1/2/1CompletedUS00003630XL820GLIPR1 inhibitor/2CompletedUS00570635VorinostatHDACI/2CompletedGermany00918489LBH589HDACI/2CompletedFrance01136499SelinexorSelective inhibitor of Nuclear ExportImatinib1/2RecruitingSpain04138381BLU-263KIT Exon17 D816V/2/3RecruitingUS04910685BezuclastinibKIT exons 9, 11, 17, and 18, including D816V/2RecruitingUS04996875BezuclastinibKIT exons 9, 11, 17, and 18, including D816V/2/3RecruitingUS05186753BezuclastinibKIT exons 9, 11, 17, and 18, including D816VPexidartinib/ Sunitinib1b/2aCompletedUS02401815 what is the relationship between KIT activation and KIT upregulation, the rate-limiting processes for abnormal KIT expression in GIST, if the underlying mechanism of KIT expression is exclusive to GIST, but not in WT KIT, imatinib treatment induces the change of tumor microenvironment (TME) , if it in turn affected the expression of KIT gene, upon the IM treatment, c-KIT oncoprotein was substantially up-regulated, which was considered as a protective mechanism for GIST cells, if these from the release of negative feedback, such as sprouty homolog 4 (SPRY4) , the protein of KIT mutants usually mislocated within intracellular organelles, such as golgi apparatus, how to detect them used for the guidelines of drugs targeting KIT expression?
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Perspective of KIT in GIST.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
KIT expression and its downstream activation pathway regulation mechanism needs to be taken seriously as its mechanism is not fully explained.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
KIT mutations are the main culprit responsible for the development of GIST and the primary/secondary resistance of imatinib.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
The epigenetic modification of KIT mutation and the study of new mutations’ targets are worthy of further study.
PMC10898159
KIT mutations and expression: current knowledge and new insights for overcoming IM resistance in GIST
Further treatment options may consider combining TKIs with other drugs that target KIT and their signaling pathway to achieve better efficacy and address drug use in resistant patients Clinical trials of the drugs targeting KIT expression in GIST RAD001 (Everolimus) RAD001 (Everolimus) RAD001 (Everolimus) MEK162 (Binimetinib) MEK162 (Binimetinib) MEK162 (Binimetinib) Selumetinib (AZD6244)
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Gastrointestinal stromal tumors (GIST) are the most common mesenchymal tumors of the gastrointestinal tract, primarily driven by KIT or PDGFRA mutations.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Programmed cell death (PCD), including apoptosis, autophagy, and ferroptosis, plays a crucial role in GIST pathogenesis, progression, and treatment response.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Non-coding RNAs (ncRNAs) have emerged as key regulators of PCD pathways, influencing GIST proliferation, metastasis, and drug resistance, particularly in response to tyrosine kinase inhibitors (TKIs) such as imatinib.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Apoptosis suppression is strongly associated with poor prognosis, while autophagy contributes to tumor dormancy and TKI resistance.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Ferroptosis, a novel iron-dependent cell death pathway, represents a promising therapeutic target.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Recent evidence suggests that ncRNAs modulate these PCD pathways through interactions with key molecular regulators such as miR-494, miR-30a, and lncRNAs, which affect signaling networks including PI3K/AKT, MAPK, and mTOR.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Furthermore, ncRNAs have mediated secondary resistance to imatinib by promoting autophagic flux and altering ferroptosis sensitivity.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Understanding the molecular interplay between ncRNAs and PCD in GIST provides novel insights into disease mechanisms and offers potential therapeutic strategies to overcome drug resistance.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Targeting ncRNA-mediated regulation of apoptosis, autophagy, and ferroptosis may enhance treatment efficacy and improve patient outcomes.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Future research should focus on elucidating the mechanistic roles of ncRNAs in PCD pathways to develop innovative diagnostic and therapeutic approaches for GIST.Gastrointestinal stromal tumors (GIST) are the most common sarcomas of the gastrointestinal tract, originating from interstitial cells of Cajal (ICC) [1–3].
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Despite this, GIST is still considered a rare disease.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Its incidence varies across regions and periods, with registry data generally reporting an annual incidence exceeding 12 cases per million .
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
While GIST has a low global incidence, significant regional differences have been observed.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
For instance, in North America and parts of Europe, the annual incidence can reach 20–30 cases per million , whereas in some Asian countries, the reported incidence is lower, ranging from 5 to 10 cases per million .
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
These differences highlight the significant impact of racial and geographical factors on GIST incidence.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
The primary driver mutations in GIST occur in the KIT (60–70%) and PDGFRA (10–15%) genes .
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Approximately 15% of GIST cases lack KIT or PDGFRA mutations but exhibit other genetic alterations, such as mutations in succinate dehydrogenase (SDH) subunits (A, B, C, or D), BRAF, KRAS, NF1, or FGFR1.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Some cases also show overexpression of IGF1R [10–12].
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
SDH deficiency promotes the accumulation of succinate, which activates signaling pathways such as PI3K/Akt, MAPK, and mTOR, thereby enhancing GIST cell proliferation, survival, and migration.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
Activation of these abnormal pathways increases tumor invasiveness and is closely associated with malignancy and poor patient prognosis (Fig. 1).
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
KIT and PDGFRA encode receptor tyrosine kinases, and their driver mutations dysregulate and activate several downstream pathways, including MEK-MAPK, PI3K-AKT, and JAK-STAT [13–15].Fig.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
1Tumor Metabolism and Apoptosis Inhibition Mechanisms Driven by SDH Deficiency (Created by BioRender).
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
This figure illustrates the key molecular mechanisms underlying GIST associated with SDH deficiency, observed in approximately 15% of GIST cases.
PMC12065685
Regulatory roles of non-coding RNAs in programmed cell death pathways and drug resistance in gastrointestinal stromal tumors
The accumulation of succinate and fumarate affects the PHD and HIF signaling pathways, subsequently activating the MAPK pathway.