Lactate dehydrogenase A negatively regulated by miRNAs promotes aerobic glycolysis and is increased in colorectal cancer

Oncotarget

Volumn 6, Issue 23, 2015, Pages 19456-19468

  Wang, Jian ^a   Wang, Hui ^b   Liu, Aifen ^c   Fang, Changge ^d   Hao, Jianguo ^e   Wang, Zhenghui ^f  

^a Tianjin Hospital   (China)

^b Tianjin Public Security Hospital   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d Advanced Personalized Diagnostics LLC   (United States)

^e Taiyuan Central Hospital   (China)

^f Logistics University   (China)

Author keywords

3'untranslated region; Colorectal cancer; Lactate dehydrogenase A; miRNA; Warburg effect

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUCOSE; LACTATE DEHYDROGENASE; LACTATE DEHYDROGENASE A; MICRORNA; MICRORNA 34A; MICRORNA 34C; MICRORNA 369P; MICRORNA 374A; MICRORNA 4524A; UNCLASSIFIED DRUG; 3' UNTRANSLATED REGION; ISOENZYME; LACTATE DEHYDROGENASE 5; LACTIC ACID;

3' UNTRANSLATED REGION; ANAEROBIC GLYCOLYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; CANCER GROWTH; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENERGY METABOLISM; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME LOCALIZATION; FEMALE; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE OVEREXPRESSION; GLUCOSE TRANSPORT; GROWTH RATE; HUMAN; HUMAN TISSUE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; SEQUENCE ANALYSIS; ANIMAL; CELL PROLIFERATION; COLORECTAL TUMOR; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; GLYCOLYSIS; HCT 116 CELL LINE; HT-29 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTOR; TUMOR VOLUME; UPREGULATION;

3' UNTRANSLATED REGIONS; ADENOSINE TRIPHOSPHATE; ANIMALS; BINDING SITES; CELL PROLIFERATION; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; GLYCOLYSIS; HCT116 CELLS; HT29 CELLS; HUMANS; ISOENZYMES; L-LACTATE DEHYDROGENASE; LACTIC ACID; MICE, NUDE; MICRORNAS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR BURDEN; UP-REGULATION;

EID: 84939248200     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3318     Document Type: Article

References (42)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA: a cancer journal for clinicians. 2013; 63:11-30.
2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA: a cancer journal for clinicians. 2011; 61:69-90.
3. Davies JM, Goldberg RM. (2011). Treatment of metastatic colorectal cancer. Seminars in oncology: Elsevier. 2011; pp. 552-560.
4. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis?. Nature Reviews Cancer. 2004; 4:891-899.
5. Kim JW, Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer research. 2006; 66:8927-8930.
6. Dang CV, Le A, Gao P. MYC-induced cancer cell energy metabolism and therapeutic opportunities. Clinical cancer research: an official journal of the American Association for Cancer Research. 2009; 15:6479-6483.
7. Kaelin WG, Jr., Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell. 2008; 30:393-402.
8. Tennant DA, Durán RV, Gottlieb E. Targeting metabolic transformation for cancer therapy. Nature Reviews Cancer. 2010; 10:267-277.
9. Kambe T, Tada J, Chikuma M, Masuda S, Nagao M, Tsuchiya T, Ratcliffe PJ, Sasaki R. Embryonal carcinoma P19 cells produce erythropoietin constitutively but express lactate dehydrogenase in an oxygen-dependent manner. Blood. 1998; 91:1185-1195.
10. Luo W, Semenza GL. Pyruvate kinase M regulates glucose metabolism by functioning as a coactivator for hypoxia-inducible factor 1 in cancer cells. Oncotarget. 2011; 2:551.
11. Chung F-Z, Tsujibo H, Bhattacharyya U, Sharief FS, Li S. Genomic organization of human lactate dehydrogenase-A gene. Biochem J. 1985; 231:537-541.
12. Shi M, Cui J, Du J, Wei D, Jia Z, Zhang J, Zhu Z, Gao Y, Xie K. A novel KLF4/LDHA signaling pathway regulates aerobic glycolysis in and progression of pancreatic cancer. Clin Cancer Res. 2014; 20:4370-4380.
13. Mirebeau-Prunier D, Le Pennec S, Jacques C, Fontaine JF, Gueguen N, Boutet-Bouzamondo N, Donnart A, Malthiery Y, Savagner F. Estrogen-related receptor alpha modulates lactate dehydrogenase activity in thyroid tumors. PloS one. 2013; 8:e58683.
14. Zhao D, Zou SW, Liu Y, Zhou X, Mo Y, Wang P, Xu YH, Dong B, Xiong Y, Lei QY, Guan KL. Lysine-5 acetylation negatively regulates lactate dehydrogenase A and is decreased in pancreatic cancer. Cancer Cell. 2013; 23:464-476.
15. Yang Y, Su D, Zhao L, Zhang D, Xu J, Wan J, Fan S, Chen M. Different effects of LDH-A inhibition by oxamate in non-small cell lung cancer cells. Oncotarget. 2014.
16. Cui J, Shi M, Xie D, Wei D, Jia Z, Zheng S, Gao Y, Huang S, Xie K. FOXM1 promotes the warburg effect and pancreatic cancer progression via transactivation of LDHA expression. Clin Cancer Res. 2014; 20:2595-2606.
17. Rong Y, Wu W, Ni X, Kuang T, Jin D, Wang D, Lou W. Lactate dehydrogenase A is overexpressed in pancreatic cancer and promotes the growth of pancreatic cancer cells. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2013; 34:1523-1530.
18. Girgis H, Masui O, White NM, Scorilas A, Rotondo F, Seivwright A, Gabril M, Filter ER, Girgis AH, Bjarnason GA. Lactate Dehydrogenase A is a potential prognostic marker in clear cell renal cell carcinoma. Molecular Cancer. 2014; 13:101.
19. Yao F, Zhao T, Zhong C, Zhu J, Zhao H. LDHA is necessary for the tumorigenicity of esophageal squamous cell carcinoma. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2013; 34:25-31.
20. Cai Z, Zhao J-S, Li J-J, Peng D-N, Wang X-Y, Chen T-L, Qiu Y-P, Chen P-P, Li W-J, Xu L-Y. A combined proteomics and metabolomics profiling of gastric cardia cancer reveals characteristic dysregulations in glucose metabolism. Molecular&Cellular Proteomics. 2010; 9:2617-2628.
21. White N, Masui O, DeSouza LV, Krakovska O, Metias S, Romaschin AD, Honey RJ, Stewart R, Pace K, Lee J. Quantitative proteomic analysis reveals potential diagnostic markers and pathways involved in pathogenesis of renal cell carcinoma. Oncotarget. 2014; 5:506-518.
22. Qing G, Skuli N, Mayes PA, Pawel B, Martinez D, Maris JM, Simon MC. Combinatorial regulation of neuroblastoma tumor progression by N-Myc and hypoxia inducible factor HIF-1alpha. Cancer Res. 2010; 70:10351-10361.
23. Shim H, Dolde C, Lewis BC, Wu C-S, Dang G, Jungmann RA, Dalla-Favera R, Dang CV. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proceedings of the National Academy of Sciences. 1997; 94:6658-6663.
24. Zhao D, Xiong Y. LDH-A acetylation: implication in cancer. Oncotarget. 2013; 4:802.
25. Kaller M, Liffers S-T, Oeljeklaus S, Kuhlmann K, Röh S, Hoffmann R, Warscheid B, Hermeking H. Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Molecular&Cellular Proteomics. 2011; 10:M111-010462.
26. Pullen TJ, da Silva Xavier G, Kelsey G, Rutter GA. miR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Molecular and cellular biology. 2011; 31:3182-3194.
27. Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ. 2010; 17:193-199.
28. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D'Andrea A, Vidigal JA, Maughan WP, Ogrodowski P, Ventura A. Intact p53-dependent responses in miR-34-deficient mice. PLoS genetics. 2012; 8:e1002797.
29. Siemens H, Jackstadt R, Kaller M, Hermeking H. Repression of c-Kit by p53 is mediated by miR-3 and is associated with reduced chemoresistance, migration and stemness. Oncotarget. 2013; 4:1399.
30. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, Arking DE, Beer MA, Maitra A, Mendell JT. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell. 2007; 26:745-752.
31. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell. 2011; 144:646-674.
32. Bui T, Thompson CB. Cancer's sweet tooth. Cancer cell. 2006; 9:419-420.
33. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. science. 2009; 324:1029-1033.
34. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, Li XY, Kang SE, Cha SY, Ryu JK, Na JM, Park C, Kim K, Lee S, Gumbiner BM, Yook JI, Weiss SJ. p53 and microRNA-3 are suppressors of canonical Wnt signaling. Sci Signal. 2011; 4:ra71.
35. Bu P, Chen KY, Chen JH, Wang L, Walters J, Shin YJ, Goerger JP, Sun J, Witherspoon M, Rakhilin N, Li J, Yang H, Milsom J, Lee S, Zipfel W, Jin MM, et al. A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell. 2013; 12:602-615.
36. Liu C, Kelnar K, Liu B, Chen X, Calhoun-Davis T, Li H, Patrawala L, Yan H, Jeter C, Honorio S, Wiggins JF, Bader AG, Fagin R, Brown D, Tang DG. The microRNA miR-34a inhibits prostate cancer stem cells and metastasis by directly repressing CD44. Nat Med. 2011; 17:211-215.
37. Krzeszinski JY, Wei W, Huynh H, Jin Z, Wang X, Chang TC, Xie XJ, He L, Mangala LS, Lopez-Berestein G, Sood AK, Mendell JT, Wan Y. miR-34a blocks osteoporosis and bone metastasis by inhibiting osteoclastogenesis and Tgif2. Nature. 2014; 512:431-435.
38. Arcaroli JJ, Quackenbush KS, Powell RW, Pitts TM, Spreafico A, Varella-Garcia M, Bemis L, Tan AC, Reinemann JM, Touban BM, Dasari A, Eckhardt SG, Messersmith WA. Common PIK3CA Mutants and a Novel 3' UTR Mutation Are Associated with Increased Sensitivity to Saracatinib. Clinical Cancer Research. 2012; 18:2704-2714.
39. Wang W, Sun J, Li F, Li R, Gu Y, Liu C, Yang P, Zhu M, Chen L, Tian W, Zhou H, Mao Y, Zhang L, Jiang J, Wu C, Hua D, et al. A frequent somatic mutation in CD274 3'-UTR leads to protein over-expression in gastric cancer by disrupting miR-570 binding. Hum Mutat. 2012; 33:480-484.
40. Simon D, Laloo B, Barillot M, Barnetche T, Blanchard C, Rooryck C, Marche M, Burgelin I, Coupry I, Chassaing N, Gilbert-Dussardier B, Lacombe D, Grosset C, Arveiler B. A mutation in the 3'-UTR of the HDAC6 gene abolishing the post-transcriptional regulation mediated by hsa-miR-433 is linked to a new form of dominant X-linked chondrodysplasia. Hum Mol Genet. 2010; 19:2015-2027.
41. Yatsenko AS, Marrone AK, Shcherbata HR. miRNA-based buffering of the cobblestone-lissencephaly-associated extra-cellular matrix receptor dystroglycan via its alternative 3'-UTR. Nat Commun. 2014; 5:4906.
42. Dini Modigliani S, Morlando M, Errichelli L, Sabatelli M, Bozzoni I. An ALS-associated mutation in the FUS 3'-UTR disrupts a microRNA-FUS regulatory circuitry. Nat Commun. 2014; 5:4335.