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Targeting the warburg effect:A revisited perspective from molecular mechanisms to traditional and innovative therapeutic strategies in cancer

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Acta Pharmaceutica Sinica B 2024年第3期14卷 953-1008页

作者： Minru Liao Dahong Yao Lifeng Wu Chaodan Luo Zhiwen Wang Jin Zhang Bo Liu Department of Biotherapy Cancer Center and State Key Laboratory of BiotherapyWest China HospitalSichuan UniversityChengdu 610041China School of Pharmaceutical Sciences Shenzhen Technology UniversityShenzhen 518118China School of Pharmacy Shenzhen University Medical SchoolShenzhen UniversityShenzhen 518055China Department of Psychology University of Southern CaliforniaLos AngelesCA 90089USA

Cancer reprogramming is an important facilitator of cancer development and survival,with tumor cells exhibiting a preference for aerobic glycolysis beyond oxidative phosphorylation,even under sufficient oxygen supply *** metabolic alteration,known as the warburg effect,serves as a significant indicator of malignant tumor *** warburg effect primarily impacts cancer occurrence by influencing the aerobic glycolysis pathway in cancer *** enzymes involved in this process include glucose transporters(GLUTs),HKs,PFKs,LDHs,and ***,the expression of transcriptional regulatory factors and proteins,such as FOXM1,p53,NF-κB,HIF1a,and c-Myc,can also influence cancer ***,lncRNAs,miRNAs,and circular RNAs play a vital role in directly regulating the warburg ***,gene mutations,tumor microenvironment remodeling,and immune system interactions are closely associated with the warburg ***,the development of drugs targeting the warburg effect has exhibited promising potential in tumor *** comprehensive review presents novel directions and approaches for the early diagnosis and treatment of cancer patients by conducting in-depth research and summarizing the bright prospects of targeting the warburg effect in cancer.

关键词： warburg effect Cancer Regulatory factor LncRNAs miRNAs Traditional Chinese medicine Small-molecule drug Drug resistance

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warburg effect mimicking inborn errors of metabolism in childhood hematologic malignancies:A case-based systematic review

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World Journal of Clinical Pediatrics 2023年第5期12卷 350-358页

作者： Khanittha Permtawee Maliwan Tengsujaritkul Chane Choed-Amphai Supapitch Chanthong Kanittha Mankhemthong Lalita Sathitsamitphong Rungrote Natesirinilkul Pimlak Charoenkwan Department of Pediatrics Faculty of MedicineChiang Mai UniversityChiang Mai 50200Thailand Department of Pediatrics Nakornping HospitalChiang Mai 50180Thailand

BACKGROUND Type B lactic acidosis and hypoglycemia can occur in various pediatric *** young children with a history of fasting preceding these metabolic derangements,inborn errors of metabolism should be primarily ***,the warburg effect,a rare metabolic complication,can also manifest in children with hematologic *** a few reports of this condition in children have been published in the *** To identify the clinical course,treatment strategies,and outcomes of childhood hematologic malignancies with type B lactic *** We performed a comprehensive search of the PubMed,Scopus,and Cochrane databases without any time restriction but limited to English language *** databases were last accessed on July 1st,*** A total of 20 publications were included in the analysis,all of which were case reports or case *** higher quality evidence was *** children with hematologic malignancies and warburg effect,there were 14 cases of acute lymphoblastic leukemia and 6 cases of non-Hodgkin’s lymphoma including our illustrative *** acidosis occurred in 55%of newly diagnosed cases and 45%of relapsed *** mean age was 10.3±4.5 years,and 80%of cases were *** mean serum lactate was 16.9±12.6 mmol/L,and 43.8%of the cases had concomitant *** acidosis initially subsided in 80%of patients receiving chemotherapy compared to 60%in the contrast *** mortality rate of newly diagnosed cases was 45.5%,while the relapsed cases represented a 100%mortality *** 8 patients reported before 2001 died from disease-related ***,patients described in reports published between 2003 and 2023 had a 54.5%rate of complete *** This complication has historically led to fatal outcome;however,patients who received chemotherapy showed a more favorable ***,it is crucial to promptly initiate specific treatment in this context.

关键词： warburg effect Lactic acidosis type B Inborn errors of metabolism Leukemia Lymphoma Children

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NUDT5 promotes the growth,metastasis,and warburg effect of IDH wild-type glioblastoma multiforme cells by upregulating TRIM47

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Asian Pacific Journal of Tropical Biomedicine 2024年第2期14卷 82-92页

作者： Zi-Fa Zhang Shu-Ming Liu Neurosurgery Department Shanxi Bethune HospitalTaiyuanShanxi Province030022China Shanxi Academy of Medical Sciences TaiyuanShanxi province030022China Emergency Department Taiyuan People’s HospitalTaiyuanShanxi Province030021China

Objective:To explore the regulatory mechanism of NUDT5 in glioblastoma multiforme(GBM).Methods:GEPIA database was used to predict the expressions of NUDT5 and tripartite motif family proteins 47(TRIM47)in GBM ***-qPCR and Western blot analyses were performed to examine NUDT5 expression in GBM ***-229 cell proliferation,migration as well as invasion were estimated by CCK-8,colony formation,wound healing,and Transwell assays following interference with *** assay,L-lactic acid kit,glucose detection kit,and ATP detection kit were applied for the detection of glycolysis-related ***-immunoprecipitation experiment was carried out to verify the relationship between NUDT5 and ***:GEPIA database showed that NUDT5 expression was significantly increased in GBM *** the expression of NUDT5 in GBM cells significantly suppressed the viability,proliferation,invasion,migration,and glycolysis of GBM ***,TRIM47 was highly expressed in GBM cells and interacted with *** of TRIM47 partially reversed the inhibitory effect of NUDT5 downregulation on the proliferation,metastasis,and glycolysis of GBM ***:NUDT5 promotes the growth,metastasis,and warburg effect of GBM cells by upregulating *** NUDT5 and TRIM47 can be used as targets for GMB treatment.

关键词： Glioblastoma multiforme NUDT5 TRIM47 Growth Metastasis warburg effect

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Novel miR-490-3p/hnRNPA1-b/PKM2 axis mediates the warburg effect and proliferation of colon cancer cells via the PI3K/AKT pathway

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World Journal of Gastrointestinal Oncology 2024年第5期16卷 2038-2059页

作者： Xiang-Hui Wan Guo-Bing Jin Qun Yang Ji-Long Hu Zhi-Liang Liu Jun Rao Can Wen Peng-Ling Li Xi-Mei Yang Bo Huang Xiao-Zhong Wang Jiangxi Medical College Nanchang UniversityNanchang 330029Jiangxi ProvinceChina Department of Clinical Laboratory Jiangxi Cancer HospitalNanchang 330029Jiangxi ProvinceChina Jiangxi Key Laboratory of Translational Research for Cancer Jiangxi Cancer HospitalNanchang 330029Jiangxi ProvinceChina Department of Abdominal Surgery Jiangxi Cancer HospitalNanchang 330029Jiangxi ProvinceChina Department of Pathology Jiangxi Cancer HospitalNanchang 330029Jiangxi ProvinceChina Science and Education Section Jiangxi Cancer HospitalNanchang 330029Jiangxi ProvinceChina Department of Clinical Laboratory Jiangxi Children’s HospitalNanchang 330006Jiangxi ProvinceChina Department of Clinical Laboratory The Second Affiliated Hospital of Nanchang UniversityNanchang 330006Jiangxi ProvinceChina Jiangxi Province Key Laboratory of Laboratory Medicine The Second Affiliated Hospital of Nanchang UniversityNanchang 330006Jiangxi ProvinceChina

BACKGROUND Heterogeneous ribonucleoprotein A1(hnRNPA1)has been reported to enhance the warburg effect and promote colon cancer(CC)cell proliferation,but the role and mechanism of the miR-490-3p/hnRNPA1-b/PKM2 axis in CC have not yet been *** To investigate the role and mechanism of a novel miR-490-3p/hnRNPA1-b/PKM2 axis in enhancing the warburg effect and promoting CC cell proliferation through the PI3K/AKT *** Paraffin-embedded pathological sections from 220 CC patients were collected and subjected to immunohistochemical analysis to determine the expression of *** relationship between the expression values and the clinicopathological features of the patients was *** in mRNA expression were analyzed using quantitative real-time polymerase chain reaction,while differences in protein expression were analyzed using western *** proliferation was evaluated using the cell counting kit-8 and 5-ethynyl-2’-deoxyuridine assays,and cell cycle and apoptosis were detected using flow cytometric *** targeted binding of miR-490-3p to hnRNPA1-b was validated using a dual luciferase reporter *** warburg effect was evaluated by glucose uptake and lactic acid production *** The expression of hnRNPA1-b was significantly increased in CC tissues and cells compared to normal controls(Pwarburg effect through the PI3K/AKT pathway,thereby promoting proliferation of HCT116 and SW620 ***,the proliferation of HCT116 and SW620 cells was inhibited when miR-490-3p targeted and bound to hnRNPA1-b,effectively blocking the warburg ***

关键词： Heterogeneous ribonucleoprotein A1-b MiR-490-3p Colon cancer Alternative splicing warburg effect

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Oncogenic lncRNA LINC00973 promotes warburg effect by enhancing LDHA enzyme activity

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Science Bulletin 2021年第13期66卷 1330-1341,M0004页

作者： Huili Wang Kequan Lin Lin Zhu Shaojun Zhang Le Li Yilie Liao Baichao Zhang Ming Yang Xinde Liu Lu Li Shasha Li Liuqing Yang Haiyan Wang Qianyu Wang Haitao Li Suneng Fu Xiaorong Zhang Peng JiangQiangfeng Cliff Zhang Jing Cheng Dong Wang School of Medicine Tsinghua UniversityBeijing 100084China School of Life Sciences Tsinghua UniversityBeijing 100084China Institute of Biophysics Chinese Academy of SciencesBeijing 100101China National Engineering Research Center for Beijing Biochip Technology Beijing 102206China Center for Precision Medicine West China HospitalSichuan UniversityChengdu 610041China School of Basic Medical Sciences Chengdu University of Traditional Chinese MedicineChengdu 611137China State Key Laboratory of Southwestern Chinese Medicine Resources Chengdu University of Traditional Chinese MedicineChengdu 611137China

Aerobic glycolysis,also known as the warburg effect,is a hallmark of cancer and essential for metabolism in malignancies,but its regulation and modulation in cancer cells remain poorly ***,using large-scale functional screening,we identified a tumor-associated and broadly expressed oncogenic long noncoding RNA ***,knocking down LINC00973 significantly inhibits the proliferation of multiple types of cancer cells and reduces tumor growth in ***,LINC00973 directly binds to lactate dehydrogenase A(LDHA),an essential glycolytic enzyme,and enhances its enzymatic activity,thereby promoting ***,high expression of LINC00973 is significantly associated with poor prognosis in many types of human *** work demonstrates that LINC00973 modulates cancer-specific regulation of the warburg effect,and may represent a potential target for broad-acting anti-cancer therapies.

关键词： LINC00973 LDHA warburg effect Cancer metabolism Biomarker

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Fundamentals of the warburg effect in Cancer

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Journal of Nutritional Oncology 2019年第3期4卷 108-114页

作者： Pi Xian Zhang Ya Qi Xing Yong Dong Niu Department of Biochemistry and Molecular Biology Shantou University Medical CollegeShantouGuangdong 515041China Department of Pharmacology Shantou University Medical CollegeShantouGuangdong 515041China

As the fundamental energy unit of most cells,the ATP generated from glucose is vital to maintain biological processes such as the synthesis of proteins and nucleic ***,a common feature of cancer cells is an altered metabolism with increased glucose uptake and the fermentation of glucose to lactate even in the presence of normal *** phenomenon is known as the‘warburg effect’(now termed aerobic glycolysis).One simple explanation for this effect is that it permits cells to more easily produce energy to support rapid *** can also help to meet the biosynthetic requirements for pyruvate as a major building *** a well-known metabolic hallmark of cancer cells,the role of the warburg effect in oncology is a newly-emerging area of growing *** this perspective,we provide some new understanding of these mechanisms based on recent progress in research on cancer *** better understanding of these mechanisms will support the development of new therapeutic strategies that take into account tumor nutrition and energy metabolism.

关键词： warburg effect Cancer Glycolysis ATP Lactate

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OTUB2 stabilizes U2AF2 to promote the warburg effect and tumorigenesis via the AKT/mTOR signaling pathway in non-small cell lung cancer

OTUB2 stabilizes U2AF2 to promote the Warburg effect and tum...

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第十五届中国实验动物科学年会

作者： Jing Li Dongdong Cheng Miaoxin Zhu Huajian Yu Zhen Pan Lei Liu Qin Geng Hongyu Pan Mingxia Yan Ming Yao State Key Laboratory of Oncogenes and Related Genes Shanghai Cancer InstituteRenji HospitalShanghai Jiao Tong University School of Medicine Department of Orthopedics Shanghai Jiao Tong University Affiliated Sixth People's Hospital

Increasing evidence has confirmed that deubiquitinating enzymes play an important role in lung cancer *** the current study,we investigated the expression profile of deubiquitinating enzymes in non-small cell lung cancer(NSCLC) tissues and identified OTUB2 as an upregulated deubiquitinating *** role of OTUB2 in NSCLC is ***:Quantitative,real-time PCR and Western blot were used to detect OTUB2 and U2 AF2 expression in NSCLC *** correlations between OTUB2 and U2 AF2 expression and clinicopathologic features were then *** used In vitro Cell Counting Kit-8(CCK-8),colony formation,and trans-well invasion assays to investigate the function of OTUB2 and U2 AF2 in *** regulation of glycolysis by OTUB2 and U2 AF2 was assessed by determining the extracellular acid ratio,glucose consumption,and lactate *** mechanism of OTUB2 was explored through co-immunoprecipitation and mass spectrometry analyses.A xenograft model was also used to study the tumorigenesis role of OTUB2 In ***:OTUB2 expression was significantly upregulated in primary NSCLC tissues and greatly associated with metastasis,advanced tumor stages,poor survival,and *** NSCLC cell lines,OTUB2 promoted cell growth,colony formation,migration,and invasive *** investigations showed that OTUB2 stimulated the warburg effect and induced the activation of the serine/threonine kinase/mechanistic target of rapamycin kinase(AKT/mTOR) pathway in different NSCLC *** importantly,OTUB2 promoted NSCLC progression,which was largely dependent on the direct binding to and deubiquitination of U2 AF2,at least in NSCLC cells.U2 AF2 expression was also significantly upregulated in primary NSCLC tissues and dramatically associated with metastasis,advanced tumor stages,poor survival,and ***,a positive correlation between the protein expression of OTUB2 and U2 AF2 in NSCLC tissues was *** vivo experiments

关键词： deubiquitinating enzyme OTUB2 NSCLC warburg effect U2AF2

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The down-regulation of apoptosis inducing factor 1 by hypoxia and its implication in the warburg effect of cancer energy metabolism

The down-regulation of apoptosis inducing factor 1 by hypoxi...

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中国病理生理学会受体、肿瘤和免疫专业委员会联合学术会议

作者： Li-Shun Wang,Shao-Ming Shen,Yun Yu,Guo-Qiang Chen Department of Pathophysiology,Key Laboratory of Cell Differentiation and Apoptosis of National Ministry of Education,Ruijin Hospital,Shanghai Jiao-Tong University School of Medicine

Hypoxia is one of the most important characteristics of cancer *** an anti-hypoxia adaptive response,more than 50%of the ATP production in cancer cells relies on glycolysis, as compared to only 10%in normal *** abnormal status of energy metabolism is called"warburg effect".Recently,the research in the"Cell"journal reported that the down-regulation of apoptosis-inducing factor(AIF ) turned ATP production to glycolysis by suppressing the oxygen consuming in mitochondrial energy metabolism,which is similar to the warburg effect in cancer ***,we found that hypoxia could induce the down-regulation of AIF in various cancer cell *** we found that hypoxia-inducible factor 1 alpha(HIF-1α) mediates the down-regulation of AIF after hypoxia treatment by suppressing the transcription of AIF via direct binding to the hypoxia responsive element(HRE) on the promoter region of AIF *** speculated that the down-regulation of AIF under hypoxia may contribute to the"warburg effect"in cancer cells.

关键词： warburg effect hypoxia AIF HIF-1α cancer

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Oncogenic lncRNA TURBOR promotes warburg effect by enhancing LDHA enzyme activity

Oncogenic lncRNA TURBOR promotes Warburg effect by enhancing...

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中国生物化学与分子生物学会2019年全国学术会议暨学会成立四十周年

作者： Huili Wang Kequan Lin Lin Zhu Shaojun Zhang Le Li Yilie Liao Baichao Zhang Ming Yang Xinde Liu Lu Li Shasha Li Haitao Li Peng Jiang Qiangfeng Cliff Zhang Dong Wang School of Medicine Tsinghua University School of Life Sciences Tsinghua University Center of Synthetic & Systems Biology Tsinghua University National Collaborative Innovation Center for Biotherapy Tsinghua University School of Basic Medical Sciences Chengdu University of Traditional Chinese Medicine

Aerobic glycolysis, also known as the warburg effect, is a hallmark of cancer and essential for malignancies, but its regulation and modulation in cancer cells remain poorly understood. Here, by large-scale functional screening, we identified a tumorassociated and broadly expressed oncogenic long noncoding RNA TURBOR, which is highly expressed in multiple types of human cancers. Notably, knocking down TURBOR significantly inhibits the proliferation of multiple types of cancer cells and reduces tumor growth in vivo. Mechanistically, TURBOR directly binds to lactate dehydrogenase A(LDHA), an essential glycolysis-associated enzyme, and enhances its enzymatic activity, thereby promoting glycolysis. Clinically, high expression of TURBOR is significantly associated with poor prognosis in many types of human cancers. Together, our results identified a new long noncoding RNA(lncRNA) that modulated a cancer-specific regulation mechanism for the warburg effect and suggested a potential target against one of cancer’s vulnerabilities for developing broad-acting anti-cancer therapies.

关键词： Long noncoding RNA warburg effect Tumor proliferation

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O-GlcNAcylation destabilizes the active tetrameric PKM2 to promote the warburg effect

O-GlcNAcylation destabilizes the active tetrameric PKM2 to p...

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中国生物化学与分子生物学会第十二届全国会员代表大会暨2018年全国学术会议

作者： Yang Wang Jia Liu Xin Jin Dapeng Zhang Dongxue Li Fengqi Hao Yunpeng Feng Shan Gu Fanlin Meng Miaomiao Tian Yi Zheng Ling Xin Xinbo Zhang Xue Han L.Aravind Min Wei Key Laboratory of Molecular Epigenetics of the Ministry of Education (MOE) Northeast Normal University Department of Biology and Program of Bioinformatics and Computational Biology Saint Louis University National Center for Biotechnology Information National Library of MedicineNational Institutes of Health

The warburg effect,characterized by increased glucose uptake and lactate production,is a well-known universal across cancer-and other ***2,a splice isoform of the pyruvate kinase(PK) specifically expressed in these cells,serves as a major regulator of this metabolic reprogramming with an adjustable activity subjected to numerous allosteric effectors and posttranslational *** we have identified a novel posttranslational modification on PKM2,O-GlcNAcylation,which specifically targets Thr and Ser,residues of the region encoded by the alternatively spliced exon 10 in cancer *** show that PKM2 O-GlcNAcylation is upregulated in various types of human tumor cells and patient tumor *** modification destabilized the active tetrameric PKM2,reduced PK activity and led to nuclear translocation of *** also observed that the modification is associated with an increased glucose consumption and lactate production,and enhanced level of lipid and DNA synthesis,indicating that O-GlcNAcylation promotes the warburg *** vivo experiments showed that blocking PKM2 O-GlcNAcylation attenuated tumor ***,we demonstrate that O-GlcNAcylation is a new regulatory mechanism for PKM2 in cancer cells and serves as a bridge between PKM2 and metabolic reprogramming typical of the warburg effect.

关键词： PKM2 O-GlcNAcylation warburg effect cancer metabolism

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