Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

Role of MicroRNAs in the Warburg Effect and Mitochondrial Metabolism in Cancer

  • Jin, Li-Hui (Center for Translational Medicine, The First Affiliated Hospital, School of Medicine, Xi'an Jiaotong University) ;
  • Wei, Chen (Clinical Laboratory, The First Affiliated Hospital, School of Medicine, Xi'an Jiaotong University)
  • Published : 2014.09.15
Download PDF
⟨ Previous Next ⟩

Abstract

Metabolism lies at the heart of cell biology. The metabolism of cancer cells is significantly different from that of their normal counterparts during tumorigenesis and progression. Elevated glucose metabolism is one of the hallmarks of cancer cells, even under aerobic conditions. The Warburg effect not only allows cancer cells to meet their high energy demands and supply biological materials for anabolic processes including nucleotide and lipid synthesis, but it also minimizes reactive oxygen species production in mitochondria, thereby providing a growth advantage for tumors. Indeed, the mitochondria also play a more essential role in tumor development. As information about the numorous microRNAs has emerged, the importance of metabolic phenotypes mediated by microRNAs in cancer is being increasingly emphasized. However, the consequences of dysregulation of Warburg effect and mitochondrial metabolism modulated by microRNAs in tumor initiation and progression are still largely unclear.

Keywords

References

  1. Ahmad A, Aboukameel A, Kong D, et al (2011). Phosphoglucose isomerase/autocrine motility factor mediates epithelialmesenchymal transition regulated by miR-200 in breast cancer cells. Cancer Res, 71, 3400-9. https://doi.org/10.1158/0008-5472.CAN-10-0965
  2. Anaya-Ruiz M, Bandala C, Perez-Santos JL (2013). MiR-485 acts as a tumor suppressor by inhibiting cell growth and migration in breast carcinoma T47D cells. Asian Pac J Cancer Prev, 14, 3757-60. https://doi.org/10.7314/APJCP.2013.14.6.3757
  3. Anaya-Ruiz M, Cebada J, Delgado-Lopez G, et al (2013). MiR-153 silencing induces apoptosis in the MDA-MB-231 breast cancer cell line. Asian Pac J Cancer Prev, 14, 2983-6. https://doi.org/10.7314/APJCP.2013.14.5.2983
  4. Bienertova-Vasku J, Sana J, Slaby O (2013). The role of microRNAs in mitochondria in cancer. Cancer Lett, 336, 1-7. https://doi.org/10.1016/j.canlet.2013.05.001
  5. Calin GA, Cimmino A, Fabbri M, et al (2008). MiR-15a and miR-16-1 cluster functions in human leukemia. Proc Natl Acad Sci USA, 105, 5166-71. https://doi.org/10.1073/pnas.0800121105
  6. Chen YH, Heneidi S, Lee JM, et al (2013). MiRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes, 62, 2278-86. https://doi.org/10.2337/db12-0963
  7. Chow TF, Mankaruos M, Scorilas A, et al (2010). The miR-17-92 cluster is over expressed in and has an oncogenic effect on renal cell carcinoma. J Urol, 183, 743-51. https://doi.org/10.1016/j.juro.2009.09.086
  8. Croce CM (2009). Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet, 10, 704-14. https://doi.org/10.1038/nrg2634
  9. Das S, Ferlito M, Kent OA, et al(2012). Nuclear miRNA regulates the mitochondrial genome in the heart. Circ Res, 110, 1596-603. https://doi.org/10.1161/CIRCRESAHA.112.267732
  10. Ebi H, Sato T, Sugito N, et al (2009). Counterbalance between RB inactivation and miR-17-92 overexpression in reactive oxygen species and DNA damage induction in lung cancers. Oncogene, 28, 3371-9. https://doi.org/10.1038/onc.2009.201
  11. Eichner LJ, Perry MC, Dufour CR, et al (2010). MiR-378(*) mediates metabolic shift in breast cancer cells via the PGC-1beta/ERRgamma transcriptional pathway. Cell Metab, 12, 352-61. https://doi.org/10.1016/j.cmet.2010.09.002
  12. Fang R, Xiao T, Fang Z, et al (2012). MicroRNA-143 (miR-143) regulates cancer glycolysis via targeting hexokinase 2 gene. J Biol Chem, 287, 23227-35. https://doi.org/10.1074/jbc.M112.373084
  13. Fei X, Qi M, Wu B, et al (2012). MicroRNA-195-5p suppresses glucose uptake and proliferation of human bladder cancer T24 cells by regulating GLUT3 expression. FEBS Lett, 586, 392-7. https://doi.org/10.1016/j.febslet.2012.01.006
  14. Gao P, Tchernyshyov I, Chang TC, et al (2009). c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature, 458, 762-5. https://doi.org/10.1038/nature07823
  15. Garzon R, Calin GA, Croce CM (2009). MicroRNAs in Cancer. Annu Rev Med, 60, 167-79. https://doi.org/10.1146/annurev.med.59.053006.104707
  16. Gatenby RA, Gillies RJ (2004). Why do cancers have high aerobic glycolysis? Nat Rev Cancer, 4, 891-9. https://doi.org/10.1038/nrc1478
  17. Gigli I, Maizon DO (2013). MicroRNAs and the mammary gland: A new understanding of gene expression. Genet Mol Biol, 36, 465-74. https://doi.org/10.1590/S1415-47572013005000040
  18. Hatziapostolou M, Polytarchou C, Iliopoulos D(2013). miRNAs link metabolic reprogramming to oncogenesis. Trends Endocrinol Metab, 24, 361-73. https://doi.org/10.1016/j.tem.2013.03.002
  19. Horie T, Ono K, Nishi H, et al (2009). MicroRNA-133 regulates the expression of GLUT4 by targeting KLF15 and is involved in metabolic control in cardiac myocytes. Biochem Biophys Res Commun, 389, 315-20. https://doi.org/10.1016/j.bbrc.2009.08.136
  20. Hsu PP, Sabatini DM (2008). Cancer cell metabolism: Warburg and beyond. Cell, 134, 703-7. https://doi.org/10.1016/j.cell.2008.08.021
  21. Ichimi T, Enokida H, Okuno Y, et al (2009). Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer Suppl, 125, 345-52. https://doi.org/10.1002/ijc.24390
  22. Iorio MV, Croce CM (2012). MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol Med, 4, 143-59. https://doi.org/10.1002/emmm.201100209
  23. Jackson AL, Bartz SR, Schelter J, et al (2003). Expression profiling reveals off-target gene regulation by RNAi. Nat Biotechnol, 21, 635-7. https://doi.org/10.1038/nbt831
  24. Jiang S, Zhang LF, Zhang HW, et al (2012). A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J, 31, 1985-98. https://doi.org/10.1038/emboj.2012.45
  25. Kefas B, Comeau, L, Erdle N, et al (2010). Pyruvate kinase M2 is a target of the tumor-suppressive microRNA-326 and regulates the survival of glioma cells. Neuro Oncol, 12, 1102-12. https://doi.org/10.1093/neuonc/noq080
  26. Kinoshita T, Nohata N, Yoshino H, et al (2012). Tumor suppressive microRNA-375 regulates lactate dehydrogenase B in maxillary sinus squamous cell carcinoma. Int J Oncol, 40, 185-93.
  27. Latronico MV, Condorelli G (2012). The might of microRNA in mitochondria. Circ Res, 110, 1540-2. https://doi.org/10.1161/CIRCRESAHA.112.271312
  28. Li J, Donath S, Li Y, et al (2010). MiR-30 regulates mitochondrial fission through targeting p53 and the dynamin-related protein-1 pathway. PLoS Genet, 6, e1000795. https://doi.org/10.1371/journal.pgen.1000795
  29. Li J, Xu ZW, Wang KH, et al (2013). Networks of MicroRNAs and genes in retinoblastomas. APJCP, 14, 6631-6.
  30. Li P, Jiao J, Gao G,et al (2012). Control of mitochondrial activity by miRNAs. J Cell Biochem, 113, 1104-10. https://doi.org/10.1002/jcb.24004
  31. Li SZ, Hu YY, Zhao J, et al (2014). MicroRNA-34a induces apoptosis in the human glioma cell line, A172, through enhanced ROS production and NOX2 expression. Biochem Biophys Res Commun, 444, 6-12. https://doi.org/10.1016/j.bbrc.2013.12.136
  32. Li W, Wang J, Chen QD, et al (2013). Insulin promotes glucose consumption via regulation of miR-99a/mTOR/PKM2 pathway. PloS one, 8, e64924. https://doi.org/10.1371/journal.pone.0064924
  33. Lu H. Buchan RJ, Cook SA (2010). MicroRNA-223 regulates Glut4 expression and cardiomyocyte glucose metabolism. Cardiovasc Res, 86, 410-20. https://doi.org/10.1093/cvr/cvq010
  34. Lunt SY, Vander Heiden MG (2011). Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol, 27, 441-4. https://doi.org/10.1146/annurev-cellbio-092910-154237
  35. Macheda ML, Rogers S, Best JD (2005). Molecular and cellular regulation of glucose transporter (GLUT) proteins in cancer. J Cell Physiol, 202, 654-62. https://doi.org/10.1002/jcp.20166
  36. Ma L, Weinberg RA (2008). Micromanagers of malignancy: role of microRNAs in regulating metastasis.Trends Genet, 24, 448-56. https://doi.org/10.1016/j.tig.2008.06.004
  37. Mateescu B, Batista L, Cardon M, et al (2011). MiR-141 and miR-200a act on ovarian tumorigenesis by controlling oxidative stress response. Nat Med, 17, 1627-35. https://doi.org/10.1038/nm.2512
  38. Pullen TJ, Silva Xavier G, Kelsey G, et al(2011). MiR-29a and miR-29b contribute to pancreatic beta-cell-specific silencing of monocarboxylate transporter 1 (Mct1). Mol Cell Biol, 31, 3182-94. https://doi.org/10.1128/MCB.01433-10
  39. Qi B , Yao WJ, Zhao BS, et al (2003). Involvement of microRNA-198 overexpression in the poor prognosis of esophageal cancer. APJCP, 14, 5073-6.
  40. Rengaraj D, Park TS, Lee SI, et al (2013). Regulation of glucose phosphate isomerase by the 3'UTR-specific miRNAs miR-302b and miR-17-5p in chicken primordial germ cells. Biol Reprod, 89, 33. https://doi.org/10.1095/biolreprod.112.105692
  41. Rottiers V, Naar AM (2012). MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol, 13, 239-50. https://doi.org/10.1038/nrm3313
  42. Shea CM, Tzertzinis G (2010). Controlled expression of functional miR-122 with a ligand inducible expression system. BMC Biotechnol, 10, 76. https://doi.org/10.1186/1472-6750-10-76
  43. Shi Q, Gibson GE (2011). Up-regulation of the mitochondrial malate dehydrogenase by oxidative stress is mediated by miR-743a. J Neurochem, 118, 440-8. https://doi.org/10.1111/j.1471-4159.2011.07333.x
  44. Sikand K, Singh J, Ebron JS, et al (2012). Housekeeping gene selection advisory: glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and beta-actin are targets of miR-644a. PloS one, 7, e47510. https://doi.org/10.1371/journal.pone.0047510
  45. Singh PK, Brand RE, Mehla K (2012). MicroRNAs in pancreatic cancer metabolism. Nat Rev Gastroenterol Hepatol, 9, 334-44. https://doi.org/10.1038/nrgastro.2012.63
  46. Srivastava SK, Bhardwaj A, Singh S, et al (2011). MicroRNA-150 directly targets MUC4 and suppresses growth and malignant behavior of pancreatic cancer cells. Carcinogenesis, 32, 1832-9. https://doi.org/10.1093/carcin/bgr223
  47. Sun Q, Chen X, Ma J, et al (2011). Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci USA, 108, 4129-34. https://doi.org/10.1073/pnas.1014769108
  48. Sun Y, Zhao X, Zhou Y, et al (2012). MiR-124, miR-137 and miR-340 regulate colorectal cancer growth via inhibition of the Warburg effect. Oncol Rep, 28, 1346-52.
  49. Tanaka H, Sasayama T, Tanaka K, et al (2013). MicroRNA-183 upregulates HIF-1alpha by targeting isocitrate dehydrogenase 2 (IDH2) in glioma cells. J Neurooncol, 111, 273-83. https://doi.org/10.1007/s11060-012-1027-9
  50. Tomasetti M, Neuzil J, Dong L (2014). MicroRNAs as regulators of mitochondrial function: role in cancer suppression. Biochim Biophys Acta, 1840, 1441-53. https://doi.org/10.1016/j.bbagen.2013.09.002
  51. Trajkovski M, Hausser J, Soutschek J, et al (2011). MicroRNAs 103 and 107 regulate insulin sensitivity. Nature, 474, 649-53. https://doi.org/10.1038/nature10112
  52. Venkataraman S, Alimova I, Fan R, et al (2010). MicroRNA 128a increases intracellular ROS level by targeting Bmi-1 and inhibits medulloblastoma cancer cell growth by promoting senescence. PloS one, 5, e10748. https://doi.org/10.1371/journal.pone.0010748
  53. Vohwinkel CU, Lecuona E, Sun H, et al (2011). Elevated CO(2) levels cause mitochondrial dysfunction and impair cell proliferation. J Biol Chem, 286, 37067-76. https://doi.org/10.1074/jbc.M111.290056
  54. Volinia S, Croce CM (2013). Prognostic microRNA/mRNA signature from the integrated analysis of patients with invasive breast cancer. Proc Natl Acad Sci U S A, 110, 7413-7. https://doi.org/10.1073/pnas.1304977110
  55. Wang JX, Jiao JQ, Li Q, et al (2011). MiR-499 regulates mitochondrial dynamics by targeting calcineurin and dynamin-related protein-1. Nat Med, 17, 71-8. https://doi.org/10.1038/nm.2282
  56. Wang K, Long B, Jiao JQ, et al (2012). MiR-484 regulates mitochondrial network through targeting Fis1. Nat Commun, 3, 781. https://doi.org/10.1038/ncomms1770
  57. Wilfred BR, Wang WX, Nelson PT (2007). Energizing miRNA research: a review of the role of miRNAs in lipid metabolism, with a prediction that miR-103/107 regulates human metabolic pathways. Mol Genet Metab, 91, 209-17. https://doi.org/10.1016/j.ymgme.2007.03.011
  58. Wise DR, DeBerardinis RJ, Mancuso A, et al (2008). Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA, 105, 18782-7. https://doi.org/10.1073/pnas.0810199105
  59. Wong TS, Liu XB., Chung-Wai HoA, et al (2008). Identification of pyruvate kinase type M2 as potential oncoprotein in squamous cell carcinoma of tongue through microRNA profiling. Int J Cancer Suppl, 123, 251-7. https://doi.org/10.1002/ijc.23583
  60. Yamasaki T, Seki N, Yoshino H, et al (2013). Tumor-suppressive microRNA-1291 directly regulates glucose transporter 1 in renal cell carcinoma. Cancer Sci, 104, 1411-9. https://doi.org/10.1111/cas.12240
  61. You JS, Jones PA (2012). Cancer genetics and epigenetics: two sides of the same coin? Cancer Cell, 22, 9-20 https://doi.org/10.1016/j.ccr.2012.06.008
  62. Zhang X, Ng W L, Wang P, et al (2012). MicroRNA-21 modulates the levels of reactive oxygen species by targeting SOD3 and TNFalpha. Cancer Res, 72, 4707-13. https://doi.org/10.1158/0008-5472.CAN-12-0639
  63. Zhao H, Guan J, Lee HM, et al (2010). Up-regulated pancreatic tissue microRNA-375 associates with human type 2 diabetes through beta-cell deficit and islet amyloid deposition. Pancreas, 39, 843-6. https://doi.org/10.1097/MPA.0b013e3181d12613
  64. Zhou Q, Souba WW, Croce CM, et al (2010). MicroRNA-29a regulates intestinal membrane permeability in patients with irritable bowel syndrome. Gut, 59, 775-84. https://doi.org/10.1136/gut.2009.181834

Cited by

  1. 2-deoxy-D-Glucose Synergizes with Doxorubicin or L-Buthionine Sulfoximine to Reduce Adhesion and Migration of Breast Cancer Cells vol.16, pp.8, 2015, https://doi.org/10.7314/APJCP.2015.16.8.3213
  2. Expression Levels of Warburg-Effect Related microRNAs Correlate with each Other and that of Histone Deacetylase Enzymes in Adult Hematological Malignancies with Emphasis on Acute Myeloid Leukemia vol.23, pp.1, 2017, https://doi.org/10.1007/s12253-016-0151-9
  3. Oridonin induces autophagy via inhibition of glucose metabolism in p53-mutated colorectal cancer cells vol.8, pp.2, 2017, https://doi.org/10.1038/cddis.2017.35
  4. Long non-coding RNAs in cancer metabolism vol.38, pp.10, 2016, https://doi.org/10.1002/bies.201600110