Skip to main content

Advertisement

SpringerLink
Log in

Long non-coding RNAs involved in cancer metabolic reprogramming

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Metabolic reprogramming has now been accepted as a hallmark of cancer. Compared to normal cells, cancer cells exhibit different metabolic features, including increased glucose uptake, aerobic glycolysis, enhanced glutamine uptake and glutaminolysis, altered lipid metabolism, and so on. Cancer metabolic reprogramming, which supports excessive cell proliferation and growth, has been widely regulated by activation of oncogenes or loss of tumor suppressors. Here, we review that long non-coding RNAs (lncRNAs) can affect cancer metabolism by mutual regulation with oncogenes or tumor suppressors. Additionally, the interaction of lncRNAs with crucial transcription factors, metabolic enzymes or microRNAs can also effectively modulate the processes of cancer metabolism. LncRNAs-derived metabolism reprogramming allows cancer cells to maintain deregulated proliferation and withstand hostile microenvironment such as energy stress. Understanding the functions of lncRNAs in cancer metabolic reprogramming that contributes to carcinogenesis and cancer development may help to develop novel and effective strategies for cancer diagnosis, prognosis and treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674

    Article  CAS  PubMed  Google Scholar 

  2. Li Z, Zhang H (2016) Reprogramming of glucose, fatty acid and amino acid metabolism for cancer progression. Cell Mol Life Sci (CMLS) 73:377–392

    Article  CAS  Google Scholar 

  3. Daye D, Wellen KE (2012) Metabolic reprogramming in cancer: unraveling the role of glutamine in tumorigenesis. Semin Cell Dev Biol 23:362–369

    Article  CAS  PubMed  Google Scholar 

  4. Beloribi-Djefaflia S, Vasseur S, Guillaumond F (2016) Lipid metabolic reprogramming in cancer cells. Oncogenesis 5:e189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. de Bari L, Atlante A (2018) Including the mitochondrial metabolism of l-lactate in cancer metabolic reprogramming. Cell Mol Life Sci (CMLS) 75:2763–2776

    Article  CAS  Google Scholar 

  6. Mishra P, Tang W, Putluri V, Dorsey TH, Jin F, Wang F, Zhu D, Amable L, Deng T, Zhang S, Killian JK, Wang Y, Minas TZ, Yfantis HG, Lee DH, Sreekumar A, Bustin M, Liu W, Putluri N, Ambs S (2018) ADHFE1 is a breast cancer oncogene and induces metabolic reprogramming. J Clin Investig 128:323–340

    Article  PubMed  Google Scholar 

  7. Yan W, Wu X, Zhou W, Fong MY, Cao M, Liu J, Liu X, Chen CH, Fadare O, Pizzo DP, Wu J, Liu L, Liu X, Chin AR, Ren X, Chen Y, Locasale JW, Wang SE (2018) Cancer-cell-secreted exosomal miR-105 promotes tumour growth through the MYC-dependent metabolic reprogramming of stromal cells. Nat Cell Biol 20:597–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Faubert B, Vincent EE, Griss T, Samborska B, Izreig S, Svensson RU, Mamer OA, Avizonis D, Shackelford DB, Shaw RJ, Jones RG (2014) Loss of the tumor suppressor LKB1 promotes metabolic reprogramming of cancer cells via HIF-1alpha. Proc Natl Acad Sci USA 111:2554–2559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Zhou G, Wang J, Zhao M, Xie TX, Tanaka N, Sano D, Patel AA, Ward AM, Sandulache VC, Jasser SA, Skinner HD, Fitzgerald AL, Osman AA, Wei Y, Xia X, Songyang Z, Mills GB, Hung MC, Caulin C, Liang J, Myers JN (2014) Gain-of-function mutant p53 promotes cell growth and cancer cell metabolism via inhibition of AMPK activation. Mol Cell 54:960–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Schito L, Rey S (2018) Cell-autonomous metabolic reprogramming in hypoxia. Trends Cell Biol 28:128–142

    Article  CAS  PubMed  Google Scholar 

  11. Cassim S, Raymond VA, Dehbidi-Assadzadeh L, Lapierre P, Bilodeau M (2018) Metabolic reprogramming enables hepatocarcinoma cells to efficiently adapt and survive to a nutrient-restricted microenvironment. Cell Cycle 1:1–14

    Google Scholar 

  12. Liu F, Ma F, Wang Y, Hao L, Zeng H, Jia C, Wang Y, Liu P, Ong IM, Li B, Chen G, Jiang J, Gong S, Li L, Xu W (2017) PKM2 methylation by CARM1 activates aerobic glycolysis to promote tumorigenesis. Nat Cell Biol 19:1358–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bu P, Chen KY, Xiang K, Johnson C, Crown SB, Rakhilin N, Ai Y, Wang L, Xi R, Astapova I, Han Y, Li J, Barth BB, Lu M, Gao Z, Mines R, Zhang L, Herman M, Hsu D, Zhang GF, Shen X (2018) Aldolase B-mediated fructose metabolism drives metabolic reprogramming of colon cancer liver metastasis. Cell Metab 27(1249–1262):e1244

    Google Scholar 

  14. Schmitt AM, Chang HY (2016) Long noncoding RNAs in cancer pathways. Cancer Cell 29:452–463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Quinn JJ, Chang HY (2016) Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet 17:47–62

    Article  CAS  PubMed  Google Scholar 

  16. Uszczynska-Ratajczak B, Lagarde J, Frankish A, Guigo R, Johnson R (2018) Towards a complete map of the human long non-coding RNA transcriptome. Nat Rev Genet 19:535–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ransohoff JD, Wei Y, Khavari PA (2018) The functions and unique features of long intergenic non-coding RNA. Nat Rev Mol Cell Biol 19:143–157

    Article  CAS  PubMed  Google Scholar 

  18. Chen S, Wu DD, Sang XB, Wang LL, Zong ZH, Sun KX, Liu BL, Zhao Y (2017) The lncRNA HULC functions as an oncogene by targeting ATG7 and ITGB1 in epithelial ovarian carcinoma. Cell Death Dis 8:e3118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Keckesova Z, Donaher JL, De Cock J, Freinkman E, Lingrell S, Bachovchin DA, Bierie B, Tischler V, Noske A, Okondo MC, Reinhardt F, Thiru P, Golub TR, Vance JE, Weinberg RA (2017) LACTB is a tumour suppressor that modulates lipid metabolism and cell state. Nature 543:681–686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Tomasetti M, Amati M, Santarelli L, Neuzil J (2016) MicroRNA in metabolic re-programming and their role in tumorigenesis. Int J Mol Sci 17:754

    Article  CAS  PubMed Central  Google Scholar 

  21. Zhang LF, Jiang S, Liu MF (2017) MicroRNA regulation and analytical methods in cancer cell metabolism. Cell Mol Life Sci 74:2929–2941

    Article  CAS  PubMed  Google Scholar 

  22. Yue M, Jiang J, Gao P, Liu H, Qing G (2017) Oncogenic MYC activates a feedforward regulatory loop promoting essential amino acid metabolism and tumorigenesis. Cell Rep 21:3819–3832

    Article  CAS  PubMed  Google Scholar 

  23. Goetzman ES, Prochownik EV (2018) The role for Myc in coordinating glycolysis, oxidative phosphorylation, glutaminolysis, and fatty acid metabolism in normal and neoplastic tissues. Front Endocrinol 9:129

    Article  Google Scholar 

  24. Sim J, Cowburn AS, Palazon A, Madhu B, Tyrakis PA, Macias D, Bargiela DM, Pietsch S, Gralla M, Evans CE, Kittipassorn T, Chey YCJ, Branco CM, Rundqvist H, Peet DJ, Johnson RS (2018) The factor inhibiting HIF asparaginyl hydroxylase regulates oxidative metabolism and accelerates metabolic adaptation to hypoxia. Cell Metab 27(898–913):e897

    Google Scholar 

  25. Zhang HS, Du GY, Zhang ZG, Zhou Z, Sun HL, Yu XY, Shi YT, Xiong DN, Li H, Huang YH (2018) NRF2 facilitates breast cancer cell growth via HIF1a-mediated metabolic reprogramming. Int J Biochem Cell Biol 95:85–92

    Article  CAS  PubMed  Google Scholar 

  26. Gnanapradeepan K, Basu S, Barnoud T, Budina-Kolomets A, Kung CP, Murphy ME (2018) The p53 tumor suppressor in the control of metabolism and ferroptosis. Front Endocrinol 9:124

    Article  Google Scholar 

  27. Herzig S, Shaw RJ (2018) AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19:121–135

    Article  CAS  PubMed  Google Scholar 

  28. Kim JW, Zeller KI, Wang Y, Jegga AG, Aronow BJ, O’Donnell KA, Dang CV (2004) Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol Cell Biol 24:5923–5936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Mikawa T, Lleonart ME, Takaori-Kondo A, Inagaki N, Yokode M, Kondoh H (2015) Dysregulated glycolysis as an oncogenic event. Cell Mol Life Sci (CMLS) 72:1881–189231

    Article  CAS  Google Scholar 

  30. Wise DR, DeBerardinis RJ, Mancuso A, Sayed N, Zhang XY, Pfeiffer HK, Nissim I, Daikhin E, Yudkoff M, McMahon SB, Thompson CB (2008) Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 105:18782–18787

    Article  PubMed  PubMed Central  Google Scholar 

  31. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van Eyk JE, Mendell JT, Dang CV (2009) c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458:762–765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Eberlin LS, Gabay M, Fan AC, Gouw AM, Tibshirani RJ, Felsher DW, Zare RN (2014) Alteration of the lipid profile in lymphomas induced by MYC overexpression. Proc Natl Acad Sci USA 111:10450–10455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Edmunds LR, Sharma L, Kang A, Lu J, Vockley J, Basu S, Uppala R, Goetzman ES, Beck ME, Scott D, Prochownik EV (2014) c-Myc programs fatty acid metabolism and dictates acetyl-CoA abundance and fate. J Biol Chem 289:25382–25392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Mannava S, Grachtchouk V, Wheeler LJ, Im M, Zhuang D, Slavina EG, Mathews CK, Shewach DS, Nikiforov MA (2008) Direct role of nucleotide metabolism in C-MYC-dependent proliferation of melanoma cells. Cell Cycle 7:2392–2400

    Article  CAS  PubMed  Google Scholar 

  35. Sun L, Song L, Wan Q, Wu G, Li X, Wang Y, Wang J, Liu Z, Zhong X, He X, Shen S, Pan X, Li A, Wang Y, Gao P, Tang H, Zhang H (2015) cMyc-mediated activation of serine biosynthesis pathway is critical for cancer progression under nutrient deprivation conditions. Cell Res 25:429–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Greasley PJ, Bonnard C, Amati B (2000) Myc induces the nucleolin and BN51 genes: possible implications in ribosome biogenesis. Nucleic Acids Res 28:446–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Li F, Wang Y, Zeller KI, Potter JJ, Wonsey DR, O’Donnell KA, Kim JW, Yustein JT, Lee LA, Dang CV (2005) Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Mol Cell Biol 25:6225–6234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Stine ZE, Walton ZE, Altman BJ, Hsieh AL, Dang CV (2015) MYC, metabolism, and cancer. Cancer Discov 5:1024–1039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Schwartzenberg-Bar-Yoseph F, Armoni M, Karnieli E (2004) The tumor suppressor p53 down-regulates glucose transporters GLUT1 and GLUT4 gene expression. Can Res 64:2627–2633

    Article  CAS  Google Scholar 

  40. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, Gottlieb E, Vousden KH (2006) TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126:107–120

    Article  CAS  PubMed  Google Scholar 

  41. Berkers CR, Maddocks OD, Cheung EC, Mor I, Vousden KH (2013) Metabolic regulation by p53 family members. Cell Metab 18:617–633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Assaily W, Rubinger DA, Wheaton K, Lin Y, Ma W, Xuan W, Brown-Endres L, Tsuchihara K, Mak TW, Benchimol S (2011) ROS-mediated p53 induction of Lpin1 regulates fatty acid oxidation in response to nutritional stress. Mol Cell 44:491–501

    Article  CAS  PubMed  Google Scholar 

  43. Suzuki S, Tanaka T, Poyurovsky MV, Nagano H, Mayama T, Ohkubo S, Lokshin M, Hosokawa H, Nakayama T, Suzuki Y, Sugano S, Sato E, Nagao T, Yokote K, Tatsuno I, Prives C (2010) Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Proc Natl Acad Sci USA 107:7461–7466

    Article  PubMed  PubMed Central  Google Scholar 

  44. Matoba S, Kang JG, Patino WD, Wragg A, Boehm M, Gavrilova O, Hurley PJ, Bunz F, Hwang PM (2006) p53 regulates mitochondrial respiration. Science 312:1650–1653

    Article  CAS  PubMed  Google Scholar 

  45. Lin SC, Hardie DG (2018) AMPK: sensing glucose as well as cellular energy status. Cell Metab 27:299–313

    Article  CAS  PubMed  Google Scholar 

  46. Hung CL, Wang LY, Yu YL, Chen HW, Srivastava S, Petrovics G, Kung HJ (2014) A long noncoding RNA connects c-Myc to tumor metabolism. Proc Natl Acad Sci USA 111:18697–18702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Petrovics G, Zhang W, Makarem M, Street JP, Connelly R, Sun L, Sesterhenn IA, Srikantan V, Moul JW, Srivastava S (2004) Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 23:605–611

    Article  CAS  PubMed  Google Scholar 

  48. Ellis BC, Graham LD, Molloy PL (2014) CRNDE, a long non-coding RNA responsive to insulin/IGF signaling, regulates genes involved in central metabolism. Biochem Biophys Acta 1843:372–386

    Article  CAS  PubMed  Google Scholar 

  49. Guil S, Soler M, Portela A, Carrere J, Fonalleras E, Gomez A, Villanueva A, Esteller M (2012) Intronic RNAs mediate EZH2 regulation of epigenetic targets. Nat Struct Mol Biol 19:664–670

    Article  CAS  PubMed  Google Scholar 

  50. Hay N (2016) Reprogramming glucose metabolism in cancer: can it be exploited for cancer therapy? Nat Rev Cancer 16:635–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wei S, Fan Q, Yang L, Zhang X, Ma Y, Zong Z, Hua X, Su D, Sun H, Li H, Liu Z (2017) Promotion of glycolysis by HOTAIR through GLUT1 upregulation via mTOR signaling. Oncol Rep 38:1902–1908

    Article  CAS  PubMed  Google Scholar 

  52. Song J, Wu X, Liu F, Li M, Sun Y, Wang Y, Wang C, Zhu K, Jia X, Wang B, Ma X (2017) Long non-coding RNA PVT1 promotes glycolysis and tumor progression by regulating miR-497/HK2 axis in osteosarcoma. Biochem Biophys Res Commun 490:217–224

    Article  CAS  PubMed  Google Scholar 

  53. Li Z, Li X, Wu S, Xue M, Chen W (2014) Long non-coding RNA UCA1 promotes glycolysis by upregulating hexokinase 2 through the mTOR-STAT3/microRNA143 pathway. Cancer Sci 105:951–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yang F, Zhang H, Mei Y, Wu M (2014) Reciprocal regulation of HIF-1alpha and lincRNA-p21 modulates the Warburg effect. Mol Cell 53:88–100

    Article  CAS  PubMed  Google Scholar 

  55. Rupaimoole R, Lee J, Haemmerle M, Ling H, Previs RA, Pradeep S, Wu SY, Ivan C, Ferracin M, Dennison JB, Millward NMZ, Nagaraja AS, Gharpure KM, McGuire M, Sam N, Armaiz-Pena GN, Sadaoui NC, Rodriguez-Aguayo C, Calin GA, Drapkin RI, Kovacs J, Mills GB, Zhang W, Lopez-Berestein G, Bhattacharya PK, Sood AK (2015) Long noncoding RNA ceruloplasmin promotes cancer growth by altering glycolysis. Cell Rep 13:2395–2402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Zhao L, Ji G, Le X, Wang C, Xu L, Feng M, Zhang Y, Yang H, Xuan Y, Yang Y, Lei L, Yang Q, Lau WB, Lau B, Chen Y, Deng X, Yao S, Yi T, Zhao X, Wei Y, Zhou S (2017) Long noncoding RNA LINC00092 acts in cancer-associated fibroblasts to drive glycolysis and progression of ovarian cancer. Can Res 77:1369–1382

    Article  CAS  Google Scholar 

  57. Yang B, Zhang L, Cao Y, Chen S, Cao J, Wu D, Chen J, Xiong H, Pan Z, Qiu F, Chen J, Ling X, Yan M, Huang S, Zhou S, Li T, Yang L, Huang Y, Lu J (2017) Overexpression of lncRNA IGFBP4-1 reprograms energy metabolism to promote lung cancer progression. Mol Cancer 16:154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Altman BJ, Stine ZE, Dang CV (2016) From Krebs to clinic: glutamine metabolism to cancer therapy. Nat Rev Cancer 16:619–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Yang L, Venneti S, Nagrath D (2017) Glutaminolysis: a hallmark of cancer metabolism. Annu Rev Biomed Eng 19:163–194

    Article  CAS  PubMed  Google Scholar 

  60. Li HJ, Li X, Pang H, Pan JJ, Xie XJ, Chen W (2015) Long non-coding RNA UCA1 promotes glutamine metabolism by targeting miR-16 in human bladder cancer. Jpn J Clin Oncol 45:1055–1063

    Article  CAS  PubMed  Google Scholar 

  61. Ge Y, Yan X, Jin Y, Yang X, Yu X, Zhou L, Han S, Yuan Q, Yang M (2015) MiRNA-192 (corrected) and miRNA-204 directly suppress lncRNA HOTTIP and interrupt GLS1-mediated glutaminolysis in hepatocellular carcinoma. PLoS Genet 11:e1005726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Redis RS, Vela LE, Lu W, Ferreira de Oliveira J, Ivan C, Rodriguez-Aguayo C, Adamoski D, Pasculli B, Taguchi A, Chen Y, Fernandez AF, Valledor L, Van Roosbroeck K, Chang S, Shah M, Kinnebrew G, Han L, Atlasi Y, Cheung LH, Huang GY, Monroig P, Ramirez MS, Catela Ivkovic T, Van L, Ling H, Gafa R, Kapitanovic S, Lanza G, Bankson JA, Huang P, Lai SY, Bast RC, Rosenblum MG, Radovich M, Ivan M, Bartholomeusz G, Liang H, Fraga MF, Widger WR, Hanash S, Berindan-Neagoe I, Lopez-Berestein G, Ambrosio ALB, Gomes Dias SM, Calin GA (2016) Allele-specific reprogramming of cancer metabolism by the long non-coding RNA CCAT2. Mol Cell 61:520–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Tomlinson I, Webb E, Carvajal-Carmona L, Broderick P, Kemp Z, Spain S, Penegar S, Chandler I, Gorman M, Wood W, Barclay E, Lubbe S, Martin L, Sellick G, Jaeger E, Hubner R, Wild R, Rowan A, Fielding S, Howarth K, Consortium C, Silver A, Atkin W, Muir K, Logan R, Kerr D, Johnstone E, Sieber O, Gray R, Thomas H, Peto J, Cazier JB, Houlston R (2007) A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21. Nature Genet 39:984–988

    Article  CAS  PubMed  Google Scholar 

  64. Beloribi-Djefaflia S, Vasseur S, Guillaumond F (2016) Lipid metabolic reprogramming in cancer cells. Oncogenesis 5:e189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Long J, Zhang CJ, Zhu N, Du K, Yin YF, Tan X, Liao DF, Qin L (2018) Lipid metabolism and carcinogenesis, cancer development. Am J Cancer Res 8:778–791

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Yan S, Yang XF, Liu HL, Fu N, Ouyang Y, Qing K (2015) Long-chain acyl-CoA synthetase in fatty acid metabolism involved in liver and other diseases: an update. World J Gastroenterol 21:3492–3498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Panzitt K, Tschernatsch MM, Guelly C, Moustafa T, Stradner M, Strohmaier HM, Buck CR, Denk H, Schroeder R, Trauner M, Zatloukal K (2007) Characterization of HULC, a novel gene with striking up-regulation in hepatocellular carcinoma, as noncoding RNA. Gastroenterology 132:330–342

    Article  CAS  PubMed  Google Scholar 

  68. Cui M, Xiao Z, Wang Y, Zheng M, Song T, Cai X, Sun B, Ye L, Zhang X (2015) Long noncoding RNA HULC modulates abnormal lipid metabolism in hepatoma cells through an miR-9-mediated RXRA signaling pathway. Can Res 75:846–857

    Article  CAS  Google Scholar 

  69. Christensen LL, True K, Hamilton MP, Nielsen MM, Damas ND, Damgaard CK, Ongen H, Dermitzakis E, Bramsen JB, Pedersen JS, Lund AH, Vang S, Stribolt K, Madsen MR, Laurberg S, McGuire SE, Orntoft TF, Andersen CL (2016) SNHG16 is regulated by the Wnt pathway in colorectal cancer and affects genes involved in lipid metabolism. Mol Oncol 10:1266–1282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Shang C, Wang W, Liao Y, Chen Y, Liu T, Du Q, Huang J, Liang Y, Liu J, Zhao Y, Guo L, Hu Z, Yao S (2018) LNMICC promotes nodal metastasis of cervical cancer by reprogramming fatty acid metabolism. Can Res 78:877–890

    Article  CAS  Google Scholar 

  71. Pavlova NN, Thompson CB (2016) The emerging hallmarks of cancer metabolism. Cell Metab 23:27–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Jeon SM, Chandel NS, Hay N (2012) AMPK regulates NADPH homeostasis to promote tumour cell survival during energy stress. Nature 485:661–665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Qian X, Li X, Tan L, Lee JH, Xia Y, Cai Q, Zheng Y, Wang H, Lorenzi PL, Lu Z (2018) Conversion of PRPS hexamer to monomer by AMPK-mediated phosphorylation inhibits nucleotide synthesis in response to energy stress. Cancer Discov 8:94–107

    Article  CAS  PubMed  Google Scholar 

  74. Bezawork-Geleta A, Wen H, Dong L, Yan B, Vider J, Boukalova S, Krobova L, Vanova K, Zobalova R, Sobol M, Hozak P, Novais SM, Caisova V, Abaffy P, Naraine R, Pang Y, Zaw T, Zhang P, Sindelka R, Kubista M, Zuryn S, Molloy MP, Berridge MV, Pacak K, Rohlena J, Park S, Neuzil J (2018) Alternative assembly of respiratory complex II connects energy stress to metabolic checkpoints. Nat Commun 9:2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, DePinho RA, Cantley LC (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101:3329–3335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Kim LC, Cook RS, Chen J (2017) mTORC1 and mTORC2 in cancer and the tumor microenvironment. Oncogene 36:2191–2201

    Article  CAS  PubMed  Google Scholar 

  77. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, Asara JM, Fitzpatrick J, Dillin A, Viollet B, Kundu M, Hansen M, Shaw RJ (2011) Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 331:456–461

    Article  CAS  PubMed  Google Scholar 

  78. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Liu X, Xiao ZD, Han L, Zhang J, Lee SW, Wang W, Lee H, Zhuang L, Chen J, Lin HK, Wang J, Liang H, Gan B (2016) LncRNA NBR2 engages a metabolic checkpoint by regulating AMPK under energy stress. Nat Cell Biol 18:431–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Xiao ZD, Han L, Lee H, Zhuang L, Zhang Y, Baddour J, Nagrath D, Wood CG, Gu J, Wu X, Liang H, Gan B (2017) Energy stress-induced lncRNA FILNC1 represses c-Myc-mediated energy metabolism and inhibits renal tumor development. Nat Commun 8:783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Khan MR, Xiang S, Song Z, Wu M (2017) The p53-inducible long noncoding RNA TRINGS protects cancer cells from necrosis under glucose starvation. EMBO J 36:3483–3500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Sanchez JF, Sniderhan LF, Williamson AL, Fan S, Chakraborty-Sett S, Maggirwar SB (2003) Glycogen synthase kinase 3beta-mediated apoptosis of primary cortical astrocytes involves inhibition of nuclear factor kappaB signaling. Mol Cell Biol 23:4649–4662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Liu F, Ma F, Wang Y, Hao L, Zeng H, Jia C, Wang Y, Liu P, Ong IM, Li B, Chen G, Jiang J, Gong S, Li L, Xu W (2017) PKM2 methylation by CARM1 activates aerobic glycolysis to promote tumorigenesis. Nat Cell Biol 19:1358–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ji X, Qian J, Rahman SMJ, Siska PJ, Zou Y, Harris BK, Hoeksema MD, Trenary IA, Heidi C, Eisenberg R, Rathmell JC, Young JD, Massion PP (2018) xCT (SLC7A11)-mediated metabolic reprogramming promotes non-small cell lung cancer progression. Oncogene 37:5007–5019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Fujiwara N, Nakagawa H, Enooku K, Kudo Y, Hayata Y, Nakatsuka T, Tanaka Y, Tateishi R, Hikiba Y, Misumi K, Tanaka M, Hayashi A, Shibahara J, Fukayama M, Arita J, Hasegawa K, Hirschfield H, Hoshida Y, Hirata Y, Otsuka M, Tateishi K, Koike K (2018) CPT2 downregulation adapts HCC to lipid-rich environment and promotes carcinogenesis via acylcarnitine accumulation in obesity. Gut 67:1493–1504

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (81772552, 81572714, 81372215) and the Fundamental Research Funds for the Central Universities of China (531107051117, 531107051157).

Author information

Authors and Affiliations

  1. State Key Laboratory of Chemo/Biosensing and Chemometrics, College of Biology, Hunan University, Changsha, 410082, Hunan, China

    Hui Liu, Junyun Luo, Siyu Luan, Chongsheng He & Zhaoyong Li

Authors
  1. Hui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junyun Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Siyu Luan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chongsheng He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhaoyong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhaoyong Li.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Luo, J., Luan, S. et al. Long non-coding RNAs involved in cancer metabolic reprogramming. Cell. Mol. Life Sci. 76, 495–504 (2019). https://doi.org/10.1007/s00018-018-2946-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-018-2946-1

Keywords

Search

Navigation