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An insight into the associations between microRNA expression and mitochondrial functions in cancer cell and cancer stem cell

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Abstract

The self-renew ability of cancer stem cells (CSCs) continues to challenge our determination for accomplishing cancer therapy breakthrough. Ineffectiveness of current cancer therapies to eradicate CSCs has contributed to chemoresistance and tumor recurrence. Yet, the discoveries of highly effective therapies have not been thoroughly developed. Further insights into cancer metabolomics and gene-regulated mechanisms of mitochondria in CSCs can expedite the development of novel anticancer drugs. In cancer cells, the metabolism is reprogrammed from oxidative phosphorylation (OXPHOS) to glycolysis. This alteration allows the cancer cell to receive continuous energy supplies and avoid apoptosis. The pyruvate obtained from glycolysis produces acetyl-coenzyme A (Acetyl-CoA) via oxidative decarboxylation and enters the tricarboxylic acid cycle for adenosine triphosphate generation. Mitochondrial calcium ion (Ca2+) uptake is responsible for mitochondrial physiology regulation, and reduced uptake of Ca2+  inhibits apoptosis and enhances cell survival in cancer. There have been many discoveries of mitochondria-associated microRNAs (miRNAs) stimulating the metabolic alterations in mitochondria via gene regulation which promote cancer cell survival. These miRNAs are also found in CSCs where they regulate genes and activate different mechanisms to destroy the mitochondria and enhance CSCs survival. By targeting the miRNAs that induced mitochondrial destruction, the mitochondrial functions can be restored; thus, it triggers CSCs apoptosis and completely eliminates the CSCs. In general, this review article aims to address the associations between miRNAs with mitochondrial activities in cancer cells and cancer stem cells that support cancer cell survival and self-renewal.

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Abbreviations

Acetyl-CoA:

Acetyl-coenzyme A

ACL:

ATP-citrate lyase

ATP:

 Adenosine triphosphate

CSCs:

Cancer stem cells

EMT:

Epithelial-to-mesenchymal transition

lncRNA:

Long non-coding RNA

MAMs:

Mitochondria-associated membranes

MCU:

Mitochondrial Ca2+ uniporter

miRNAs:

microRNAs

OXPHOS:

Oxidative phosphorylation

ROS:

Reactive oxygen species

SCC:

Squamous cell carcinoma

TCA:

Tricarboxylic acid

References

  1. Osellame LD, Blacker TS, Duchen MR (2012) Cellular and molecular mechanisms of mitochondrial function. Best Pract Res Clin Endocrinol Metab 26:711–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular Biology of the cell, 4th edn. Garland Science, The Mitochondrion, New York

    Google Scholar 

  3. Kühlbrandt W (2015) Structure and function of mitochondrial membrane protein complexes. BMC Biol 13:1–11

    Article  Google Scholar 

  4. Friedman JR, Nunnari J (2014) Mitochondrial form and function. Nature 505:335–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Brand MD, Orr AL, Perevoshchikova IV, Quinlan CL (2013) The role of mitochondrial function and cellular bioenergetics in ageing and disease. Br J Dermatol 169:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. De Giusti CJ, Roman B, Das S (2018) The influence of microRNAs on mitochondrial calcium. Front Physiol 9:1–10

    Google Scholar 

  7. Lin MT, Beal MF (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443:787–795

    Article  CAS  PubMed  Google Scholar 

  8. Hotamisligil GS (2006) Inflammation and metabolic disorders. Nature 444:860–867

    Article  CAS  PubMed  Google Scholar 

  9. Luchsinger JA, Gustafson DR (2009) Adiposity, type 2 diabetes, and Alzheimer’s disease. J Alzheimers Dis 16:693–704

    Article  PubMed  PubMed Central  Google Scholar 

  10. O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol 9:1–12

    Google Scholar 

  11. Borralho PM, Rodrigues CMP, Steer CJ (2015) MicroRNAs in mitochondria: an unexplored niche. In: Novák J (ed) Olejníčková V. MicroRNA: Basic science. Springer, Switzerland, pp 79–100

    Google Scholar 

  12. Srinivasan H, Das S (2015) Mitochondrial miRNA (MitomiR): a new player in cardiovascular health. Can J Physiol Pharmacol 93:855–861

    Article  CAS  PubMed  Google Scholar 

  13. Herst PM, Rowe MR, Carson GM, Berridge MV (2017) Functional mitochondria in health and disease. Front Endocrinol 8:296

    Article  Google Scholar 

  14. Reznik E, Miller ML, Şenbabaoğlu Y, Riaz N, Sarungbam J, Tickoo SK, Al-Ahmadie HA, Lee W, Seshan VE, Hakimi AA, Sander C (2016) Mitochondrial DNA copy number variation across human cancers. Elife 5:1–20

    Article  Google Scholar 

  15. Li J, Condello S, Thomes-Pepin J, Ma X, Xia Y, Hurley TD, Matei D, Cheng JX (2017) Lipid desaturation is a metabolic marker and therapeutic target of ovarian cancer stem cells. Cell Stem Cell 20:303–314e5

    Article  CAS  PubMed  Google Scholar 

  16. Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J (2005) The origin of the cancer stem cell: current controversies and new insights. Perspectives 5:899–904

    CAS  Google Scholar 

  17. Suvà M, Rheinbay E, Gillespie SM, Patel AP, Wakimoto H, Rabkin SD, Riggi N, Chi AS, Cahill DP, Nahed BV, Curry WT, Martuza RL, Rivera MN, Rossetti N, Kasif S, Beik S, Kadri S, Tirosh I, Wortman I, Shalek AK, Rozenblatt-Rosen O, Regev A, Louis DN, Bernstein BE (2014) Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 157:580–594

    Article  PubMed  PubMed Central  Google Scholar 

  18. Yeung KT, Yang J (2017) Epithelial-mesenchymal transition in tumor metastasis. Mol Oncol 11:28–39

    Article  PubMed  Google Scholar 

  19. Tabassum N, Verma V, Kumar M, Kumar A, Singh B (2018) Nanomedicine in cancer stem cell therapy: from fringe to forefront. Cell Tissue Res 374:427–438

    Article  PubMed  Google Scholar 

  20. Vakifahmetoglu-Norberg H, Ouchida AT, Norberg E (2017) The role of mitochondria in metabolism and cell death. Biochem Biophys Res Commun 482:426–431

    Article  CAS  PubMed  Google Scholar 

  21. Wallace DC (2012) Mitochondria and cancer. Nat Rev Cancer 12:685–698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Zhang J, Duan H, Feng Z, Han X, Gu C (2020) Acetyle-CoA synthetase 3 promotes bladder cancer cell growth under metabolic stress. Oncogenesis 9:46

    Article  PubMed  PubMed Central  Google Scholar 

  23. Pustylnikov S, Costabile F, Beghi S, Facciabene A (2018) Targeting mitochondria in cancer: current concepts and immunotherapy approaches. Transl Res 202:35–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gao T, Zhang X, Zhao J, Zhou F, Wang Y, Zhao Z, Xing J, Chen B, Li J, Liu S (2020) SIK2 promotes reprogramming of glucose metabolism through PI3K/AKT/HIF-1α pathway and Drp1-mediated mitochondrial fission in ovarian cancer. Cancer Lett 469:89–101

    Article  CAS  PubMed  Google Scholar 

  25. Jones RG, Thompson CB (2009) Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev 23:537–548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. García-Rostán G, Costa AM, Pereira-Castro I, Salvatore G, Hernandez R, Hermsem MJA, Herrero A, Fusco A, Cameselle-Teijeiro J, Santoro M (2005) Mutation of the PIK3CA gene in anaplastic thyroid cancer. Cancer Res 65:10199–10207

    Article  PubMed  Google Scholar 

  27. Okano JI, Snyder L, Rustgi AK (2003) Genetic alterations in esophageal cancer. Methods Mol Biol 222:131–145

    CAS  PubMed  Google Scholar 

  28. Yan S, Liu G, Pei C, Chen W, Li P, Wang Q, Jin X, Zhu J, Wang M, Liu X (2015) Inhibition of NADPH oxidase protects against metastasis of human lung cancer by decreasing microRNA-21. Anticancer Drug 26:388–398

    Article  CAS  Google Scholar 

  29. Wallace DC, Fan W, Procaccio V (2010) Mitochondrial energetics and therapeutics. Annu Rev Pathol 5:297–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wallace DC, Fan W (2010) Energetics, epigenetics, mitochondrial genetics. Mitochondrion 10:12–31

    Article  CAS  PubMed  Google Scholar 

  31. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry. 5th edition. New York: W H Freeman; Chapter 17, The Citric Acid Cycle. Available from: https://www.ncbi.nlm.nih.gov/books/NBK21163/

  32. Yoshii Y, Furukawa T, Saga T, Fujibayashi Y (2015) Acetate/acetyl-CoA metabolism associated with cancer fatty acid synthesis: overview and application. Cancer Lett 356:211–216

    Article  CAS  PubMed  Google Scholar 

  33. Hatzivassiliou G, Zhao F, Bauer DE, Andreadis C, Shaw AN, Dhanak D, Hingorani SR, Tuveson DA, Thompson CB (2005) ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 8:311–321

    Article  CAS  PubMed  Google Scholar 

  34. Kamphorst JJ, Chung MK, Fan J, Rabinowitz JD (2014) Quantitative analysis of acetyl-CoA production in hypoxic cancer cells reveals substantial contribution from acetate. Cancer & Metabolism 2:1–8

    Article  Google Scholar 

  35. Carrer A, Trefely S, Zhao S, Campbell SL, Norgard RJ, Schultz KC, Sidoli S, Parris JLD, Affronti HC, Sivanand S, Egolf S, Sela Y, Trizzino M, Gardini A, Garcia BA, Snyder NW, Stanger BZ, Wellen KE (2019) Acetyl-CoA metabolism supports multistep pancreatic tumorigenesis. Cancer Discov 9:416–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Ding S, Tang S, Wang M, Wu D, Guo H (2017) Acyl-CoA synthetase 5 promotes the growth and invasion of colorectal cancer cells. Can J Gastroenterol Hepatol 2017:1–14

    Article  Google Scholar 

  37. Graier WF, Malli R (2017) Mitochondrial calcium: a crucial hub for cancer cell metabolism? Transl Cancer Res 6:S1124–S1127

    Article  Google Scholar 

  38. Gueguinou M, Crottès D, Chantôme A, Rapetti-Mauss R, Potier-Cartereau M, Clarysse L, Girault A, Fourbon Y, Jézéquel P, Guérin-Charbonnel C, Fromont G, Martin P, Pellissier B, Schiappa R, Chamorey E, Mignen O, Uguen A, Borgese F, Vandier C, Soriani O (2017) The SigmaR1 chaperone drives breast and colorectal cancer cell migration by tuning SK3-dependent Ca2 + homeostasis. Oncogene 36:3640–3647

    Article  CAS  PubMed  Google Scholar 

  39. Liu Y, Jin M, Wang Y, Zhu J, Tan R, Zhao J, Ji X, Jin C, Jia Y, Ren T, Xing J (2020) MCU-induced mitochondrial calcium uptake promotes mitochondrial biogenesis and colorectal cancer growth. Signal Transduct Target Ther 5:59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Perocchi F, Gohil VM, Girgis HS, Bao XR, McCombs JE, Palmer AE, Mootha VK (2010) MICU1 encodes a mitochondrial EF hand protein required for Ca2 + uptake. Nature 467:291–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chakraborty PK, Mustafi SB, Xiong X, Dwivedi SKD, Nesin V, Saha S, Zhang M, Dhanasekaran D, Jayaraman M, Mannel R, Moore K, McMeekin S, Yang D, Zuna R, Ding K, Tsiokas L, Bhattacharya R, Mukherjee P (2017) MICU1 drives glycolysis and chemoresistance in ovarian cancer. Nat Commun 8:1–16

    Article  Google Scholar 

  42. Barrey E, Saint-Auret G, Bonnamy B, Damas D, Boyer O, Gidrol X (2011) Pre-microRNA and mature microRNA in human mitochondria. PLoS ONE 6:e20220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Saini SK, Kalaiarasan P, Singh RK, Manvati S, Bamezai RNK (2018) MicroRNA (hsa-miR-19b-2-5p) targets key mitochondrial biogenesis genes-a bioinformatics analysis. Mitochondrion 43:30–36

    Article  CAS  PubMed  Google Scholar 

  44. Jiang S, Zhang LF, Zhang HW, Hu S, Lu MH, Liang S, Li B, Li Y, Li D, Wang ED, Liu MF (2012) A novel miR-155/miR-143 cascade controls glycolysis by regulating hexokinase 2 in breast cancer cells. EMBO J 31:1985–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Peschiaroli A, Giacobbe A, Formosa A, Markert EK, Bongiorno-Borbone L, Levine AJ, Candi E, D’Alessandro A, Zolla L, Finazzi Agrò A, Melino G (2013) MiR-143 regulates hexokinase 2 expression in cancer cells. Oncogene 32:797–802

    Article  CAS  PubMed  Google Scholar 

  46. Fan S, Tian T, Chen W, Lv X, Lei X, Zhang H, Sun S, Cai L, Pan G, He L, Ou Z, Lin X, Wang X, Perez MF, Tu Z, Ferrone S, Tannous BA, Li J (2019) Mitochondrial miRNA determines chemoresistance by reprogramming metabolism and regulating mitochondrial transcription. Cancer Res 79:1069–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kao YY, Chou CH, Yeh LY, Chen YF, Chang KW, Liu CJ, Fan CCY, Lin SC (2019) MicroRNA miR-31 targets SIRT3 to disrupt mitochondrial activity and increase oxidative stress in oral carcinoma. Cancer Lett 456:40–48

    Article  CAS  PubMed  Google Scholar 

  48. Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, Tang LH, Levine AJ, Feng Z (2010) Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell 38:689–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Le MTN, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B (2009) MicroRNA-125b is a novel negative regulator of p53. Genes Dev 23:862–876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Birks DK, Barton VN, Donson AM, Handler MH, Vibhakar R, Foreman NK (2011) Survey of MicroRNA expression in pediatric brain tumors. Pediatr Blood Cancer 56:211–216

    Article  PubMed  Google Scholar 

  51. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, Cavazzini L, Volinia S, Alder H, Ruco LP, Baldassarre G, Croce CM, Vecchione A (2008) E2F1-regulated microRNAs impair TGFβ-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13:272–286

    Article  CAS  PubMed  Google Scholar 

  52. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, Rameh L, Loda M, Pandolfi PP (2010) Identification of the miR-106b∼25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal 3:ra29

    Article  PubMed  PubMed Central  Google Scholar 

  53. Wu T, Hu H, Zhang T, Jiang L, Li X, Liu S, Zheng C, Yan G, Chen W, Ning Y, Li Y, Lu Z (2019) MiR-25 promotes cell proliferation, migration, and invasion of non-small-cell lung cancer by targeting the LATS2/YAP signaling pathway. Oxid Med Cell Longev 2019:1–14

    Article  Google Scholar 

  54. Feng S, Pan W, Jin Y, Zheng J (2014) MiR-25 promotes ovarian cancer proliferation and motility by targeting LATS2. Tumor Biol 35:12339–12344

    Article  CAS  Google Scholar 

  55. Marchi S, Lupini L, Patergnani S, Rimessi A, Missiroli S, Bonora M, Bononi A, Corrà F, Giorgi C, De Marchi E, Poletti F, Gafà R, Lanza G, Negrini M, Rizzuto R, Pinton P (2013) Downregulation of the mitochondrial calcium uniporter by cancer-related miR-25. Curr Biol 23:58–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Penna E, Orso F, Cimino D, Tenaglia E, Lembo A, Quaglino E, Poliseno L, Haimovic A, Osella-Abate S, De Pittá C, Pinatel E, Stadler MB, Provero P, Bernengo MG, Osman I, Taverna D (2011) MicroRNA-214 contributes to melanoma tumour progression through suppression of TFAP2C. EMBO J 30:1990–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Wang JM, Ju BH, Pan CJ, Gu Y, Li MQ, Sun L, Xu YY, Yin LR (2017) MiR-214 inhibits cell migration, invasion and promotes the drug sensitivity in human cervical cancer by targeting FOXM1. Am J Transl Res 9:3541–3557

    PubMed  PubMed Central  Google Scholar 

  58. Wu K, Ma J, Zhan Y, Liu K, Ye Z, Chen J, Xu K, Huang H, He Y (2018) Down-regulation of MicroRNA-214 contributed to the enhanced mitochondrial transcription factor A and inhibited proliferation of colorectal cancer cells. Cell Physiol Biochem 49:545–554

    Article  CAS  PubMed  Google Scholar 

  59. Luan T, Fu S, Huang L, Zuo Y, Ding M, Li N, Chen J, Wang H, Wang J (2018) MicroRNA-98 promotes drug resistance and regulates mitochondrial dynamics by targeting LASS2 in bladder cancer cells. Exp Cell Res 373:188–197

    Article  CAS  PubMed  Google Scholar 

  60. Zhang Y, Yang Y, Liu R, Meng Y, Tian G, Cao Q (2019) Downregulation of microRNA-425-5p suppresses cervical cancer tumorigenesis by targeting AIFM1. Exp Ther Med 17:4032–4038

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CYJ, Sasaki T, Elia AJ, Cheng HYM, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zúñiga-Pflücker JC, Kroemer G, Penninger JM (2001) Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature 410:549–554

    Article  CAS  PubMed  Google Scholar 

  62. Wu MJ, Chen YS, Kim MR, Chang CC, Gampala S, Zhang Y, Wang Y, Chang CY, Yang JY, Chang CJ (2019) Epithelial-mesenchymal transition directs stem cell polarity via regulation of mitofusin. Cell Metabol 29:993–1002e6

    Article  CAS  Google Scholar 

  63. Lee SY, Ju MK, Jeon HM, Lee YJ, Kim CH, Park HG, Han SI, Kang HS (2018) Oncogenic metabolism acts as a prerequisite step for induction of cancer metastasis and cancer stem cell phenotype. Oxid Med Cell Longev 2018:1–28

    Google Scholar 

  64. Luan L, Zhao Y, Xu Z, Jiang G, Zhang X, Fan C, Liu D, Zhao H, Xu K, Wang M, Yu X, Wang E (2014) Diversin increases the proliferation and invasion ability of non-small-cell lung cancer cells via JNK pathway. Cancer Lett 344:232–238

    Article  CAS  PubMed  Google Scholar 

  65. Lu YC, Chang JT, Liao CT, Kang CJ, Huang SF, Chen IH, Huang CC, Huang YC, Chen WH, Tsai CY, Wang HM, Yen TC, You GR, Chiang CH, Cheng AJ (2014) OncomiR-196 promotes an invasive phenotype in oral cancer through the NME4-JNK-TIMP1-MMP signaling pathway. Mol Cancer 13:1–14

    Article  Google Scholar 

  66. An BC, Jung NK, Park CY, Oh IJ, Choi YD, Park JI, Lee SW (2016) Epigenetic and glucocorticoid receptor-mediated regulation of glutathione peroxidase 3 in lung cancer cells. Mol Cells 39:631–638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Liu Q, Bai W, Huang F, Tang J, Lin X (2019) Downregulation of microRNA-196a inhibits stem cell self-renewal ability and stemness in non-small-cell lung cancer through upregulating GPX3 expression. Int J Biochem Cell Biol 115:105571

    Article  CAS  PubMed  Google Scholar 

  68. Pan Y, Shu X, Sun L, Yu L, Sun L, Zhihua Y, Ran Y (2017) MiR-196a-5p modulates gastric cancer stem cell characteristics by targeting Smad4. Int J Oncol 50:1965–1976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Xourafas D, Mizuno T, Cloyd JM (2019) The impact of somatic SMAD4 mutations in colorectal liver metastases. Chin Clin Oncol 8:6–11

    Article  Google Scholar 

  70. Lin LH, Chang KW, Cheng HW, Liu CJ (2019) SMAD4 somatic mutations in head and neck carcinoma are associated with tumor progression. Front Oncol 9:1–12

    Article  Google Scholar 

  71. Wang Z, Li Y, Zhan S, Zhang L, Zhang S, Tang Q, Li M, Tan Z, Liu S, Xing X (2019) SMAD4 Y353C promotes the progression of PDAC. BMC Cancer 19:1–12

    Article  Google Scholar 

  72. Shi Y, Massagué J (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113:685–700

    Article  CAS  PubMed  Google Scholar 

  73. Massagué J (2012) TGFβ signalling in context. Nat Rev Mol Cell Biol 13:616–630

    Article  PubMed  PubMed Central  Google Scholar 

  74. Braun T, Bober E, Singh S, Agarwal DP, Goedde HW (1987) Evidence for a signal peptide at the amino-terminal end of human mitochondrial aldehyde dehydrogenase. FEBS Lett 215:233–236

    Article  CAS  PubMed  Google Scholar 

  75. Vasillou V, Pappa A, Estey T (2004) Role of human aldehyde dehydrogenases in endobiotic and xenobiotic metabolism. Drug Metab Rev 36:279–299

    Article  Google Scholar 

  76. Singh S, Brocker C, Koppaka V, Ying C, Jackson B, Matsumoto A, Thompson DC, Vasiliou V (2014) Aldehyde dehydrogenases in cellular responses to oxidative/electrophilic stress. Free Radic Biol Med 1:89–101

    Google Scholar 

  77. Viswanathan V, Damle S, Zhang T, Opdenaker L, Modarai S, Accerbi M, Schmidt S, Green P, Galileo D, Palazzo J, Fields J, Haghighat S, Rigoutsos I, Gonye G, Boman BM (2017) An miRNA expression signature for the human colonic stem cell niche distinguishes malignant from normal epithelia. Cancer Res 77:3778–3790

    Article  CAS  PubMed  Google Scholar 

  78. De Lau W, Barker N, Low TY, Koo BK, Li VSW, Teunissen H, Kujala P, Haegebarth A, Peters PJ, Van De Wetering M, Stange DE, Van Es J, Guardavaccaro D, Schasfoort RBM, Mohri Y, Nishimori K, Mohammed S, Heck AJR, Clevers H (2011) Lgr5 homologues associate with wnt receptors and mediate R-spondin signalling. Nature 476:293–297

    Article  CAS  PubMed  Google Scholar 

  79. Gao P, Tchernyshyov I, Chang TC, Lee YS, Kita K, Ochi T, Zeller KI, De Marzo AM, Van EJE, 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 

  80. Wang W, Li Y, Liu N, Gao Y, Li L (2017) MiR-23b controls ALDH1A1 expression in cervical cancer stem cells. BMC Cancer 17:1–6

    Article  Google Scholar 

  81. Wu Q, Yang Z, Wang F, Hu S, Yang L, Shi Y, Fan D (2013) MiR-19b/20a/92a regulates the self-renewal and proliferation of gastric cancer stem cell. J Cell Sci 126:4220–4229

    CAS  PubMed  Google Scholar 

  82. Zhu J, Wang S, Chen Y, Li X, Jiang Y, Yang X, Li Y, Wang X, Meng Y, Zhu M, Ma X, Huang C, Wu R, Xie C, Geng S, Wu J, Zhong C, Han H (2017) miR-19 targeting of GSK3β mediates sulforaphane suppression of lung cancer stem cells. J Nutr Biochem 44:80–91

    Article  CAS  PubMed  Google Scholar 

  83. Zheng H, Saito H, Masuda S, Yang X, Takano Y (2007) Phosphorylated GSK3β-ser9 and EGFR are good prognostic factors for lung carcinomas. Anticancer Res 27:3561–3569

    PubMed  Google Scholar 

  84. Liu W, Huang YJ, Liu C, Yang YY, Liu H, Cui JG, Cheng Y, Gao F, Cai JM, Li BL (2014) Inhibition of TBK1 attenuates radiation-induced epithelial-mesenchymal transition of A549 human lung cancer cells via activation of GSK-3β and repression of ZEB1. Lab Invest 94:362–370

    Article  CAS  PubMed  Google Scholar 

  85. Zhao D, Chen Y, Chen S, Zheng C, Hu J, Luo S (2017) MiR-19a regulates the cell growth and apoptosis of osteosarcoma stem cells by targeting PTEN. Tumor Biol 39:1–10

    Article  Google Scholar 

  86. Blanco-Aparicio C, Renner O, Leal JFM, Carnero A (2007) PTEN, more than the AKT pathway. Carcinogenesis 28:1379–1386

    Article  CAS  PubMed  Google Scholar 

  87. Zhu K, Wang Y, Liu L, Li S, Yu W (2020) Long non-coding RNA MBNL1-AS1 regulates proliferation, migration, and invasion of cancer stem cells in colon cancer by interacting with MYL9 via sponging microRNA-412-3p. Clin Res Hepatol Gastroenterol 44:101–114

    Article  CAS  PubMed  Google Scholar 

  88. Huang YQ, Han ZD, Liang YX, Lin ZY, Ling XH, Fu X, Cai C, Bi XC, Dai QS, Chen JH, He HC, Chen YR, Jiang FN, Zhong WD (2014) Decreased expression of myosin light chain MYL9 in stroma predicts malignant progression and poor biochemical recurrence-free survival in prostate cancer. Med Oncol 31:1–9

    Article  Google Scholar 

  89. Wang JH, Zhang L, Huang ST, Xu J, Zhou Y, Yu XJ, Luo RZ, Wen ZS, Jia WH, Zheng M (2017) Expression and prognostic significance of MYL9 in esophageal squamous cell carcinoma. PLoS ONE 12:1–13

    Google Scholar 

  90. Xu W, Zhang Z, Zou K, Cheng Y, Yang M, Chen H, Wang H, Zhao J, Chen P, He L, Chen X, Geng L, Gong S (2017) MiR-1 suppresses tumor cell proliferation in colorectal cancer by inhibition of Smad3-mediated tumor glycolysis. Cell Death Dis 8:e2761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Liu C, Zhang S, Wang Q, Zhang X (2017) Tumor suppressor miR-1 inhibits tumor growth and metastasis by simultaneously targeting multiple genes. Oncotarget 8:42043–42060

    Article  PubMed  PubMed Central  Google Scholar 

  92. Childs G, Fazzari M, Kung G, Kawachi N, Brandwein-Gensler M, McLemore M, Chen Q, Burk RD, Smith RV, Prystowsky MB, Belbin TJ, Schlecht NF (2009) Low-level expression of microRNAs let-7d and miR-205 are prognostic markers of head and neck squamous cell carcinoma. Am J Pathol 174:736–745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Lee SS, Cheah YK (2019) The interplay between microRNAs and cellular components of tumour microenvironment (TME) on non-small-cell lung cancer (NSCLC) progression. J Immunol Res 2019:1–12

    CAS  Google Scholar 

  94. Zhang S, Liu C, Zhang X (2019) Mitochondrial damage mediated by miR-1 overexpression in cancer stem cells. Mol Ther Nucleic Acids 18:938–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Fan T, Wang W, Zhang B, Xu Y, Chen L, Pan S, Hu H, Geng Q (2016) Regulatorymechanisms of microRNAs in lung cancer stem cells. SpringerPlus 5:1762

    Article  PubMed  PubMed Central  Google Scholar 

  96. Cho WCS, Chow ASC, Au JSK (2011) MiR-145 inhibits cell proliferation of human lung adenocarcinoma by targeting EGFR and NUDT1. RNA Biol 8:125–131

    Article  CAS  PubMed  Google Scholar 

  97. Yin R, Zhang S, Wu Y, Fan X, Jiang F, Zhang Z, Feng D, Guo X, Xu L (2011) microRNA-145 suppresses lung adenocarcinoma-initiating cell proliferation by targeting OCT4. Oncol Rep 25:1747–1754

    CAS  PubMed  Google Scholar 

  98. Jia Y, Liu H, Zhuang Q, Xu S, Yang Z, Li J, Lou J, Zhang W (2012) Tumorigenicity of cancer stem-like cells derived from hepatocarcinoma is regulated by microRNA-145. Oncol Rep 27:1865–1872

    CAS  PubMed  Google Scholar 

  99. Bonifacio LN, Jarstfer MB (2010) MiRNA profile associated with replicative senescence, extended cell culture, and ectopic telomerase expression in human foreskin fibroblasts. PLoS ONE 5:1–8

    Article  Google Scholar 

  100. Karatas OF, Suer I, Yuceturk B, Yilmaz M, Hajiyev Y, Creighton CJ, Ittmann M, Ozen M (2016) The role of miR-145 in stem cell characteristics of human laryngeal squamous cell carcinoma Hep-2 cells. Tumor Biol 37:4183–4192

    Article  CAS  Google Scholar 

  101. Yu Y, Nangia-Makker P, Farhana L, Rajendra SG, Levi E, Majumdar APN (2015) miR-21 and miR-145 cooperation in regulation of colon cancer stem cells. Mol Cancer 14:98

    Article  PubMed  PubMed Central  Google Scholar 

  102. Yu RMC, Cheah YK (2017) The roles of miRNAs in human breast cancer and canine mammary tumor. Appl Cancer Res 37:1–11

    Article  CAS  Google Scholar 

  103. Wong JS, Cheah YK (2020) Potential miRNAs for miRNA-based therapeutics in breast cancer. Non-coding RNA 6:29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Jeong JY, Kang H, Kim TH, Kim G, Heo JH, Kwon AY, Kim S, Jung SG, An HJ (2017) MicroRNA-136 inhibits cancer stem cell activity and enhances the anti-tumor effect of paclitaxel against chemoresistant ovarian cancer cells by targeting Notch3. Cancer Lett 386:168–178

    Article  CAS  PubMed  Google Scholar 

  105. Takebea N, Nguyen D, Yang SX (2014) Targeting notch signaling pathway in cancer: clinical development advances and challenges. Pharmacol Ther 141:140–149

    Article  Google Scholar 

  106. Venkatesh V, Nataraj R, Thangaraj GS, Karthikeyan M, Gnanasekaran A, Kaginelli SB, Kuppanna G, Kallappa CG, Basalingappa KM (2018) Targeting notch signalling pathway of cancer stem cells. Stem Cell Investig 5:5

    Article  PubMed  PubMed Central  Google Scholar 

  107. Zhang Q, Lu C, Fang T, Wang Y, Hu W, Qiao J, Liu B, Liu J, Chen N, Li M, Zhu R (2015) Notch3 functions as a regulator of cell self-renewal by interacting with the β-catenin pathway in hepatocellular carcinoma. Oncotarget 6:3669–3679

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was funded by Fundamental Research Grant Scheme (04-01-20-2285FR) and Universiti Putra Malaysia Research University Grant Scheme (GP-IPS/2022/9724000).

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Correspondence to Yoke Kqueen Cheah.

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Tan, W.L., Subha, S.T., Mohtarrudin, N. et al. An insight into the associations between microRNA expression and mitochondrial functions in cancer cell and cancer stem cell. Mol Biol Rep 50, 5395–5405 (2023). https://doi.org/10.1007/s11033-023-08421-5

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