Skip to main content

Advertisement

SpringerLink
Log in

The strict regulation of HIF-1α by non-coding RNAs: new insight towards proliferation, metastasis, and therapeutic resistance strategies

  • Published:
Cancer and Metastasis Reviews Aims and scope Submit manuscript

Abstract

The hypoxic environment is prominently witnessed in most solid tumors and is associated with the promotion of cell proliferation, epithelial-mesenchymal transition (EMT), angiogenesis, metabolic reprogramming, therapeutic resistance, and metastasis of tumor cells. All the effects are mediated by the expression of a transcription factor hypoxia-inducible factor-1α (HIF-1α). HIF-1α transcriptionally modulates the expression of genes responsible for all the aforementioned functions. The stability of HIF-1α is regulated by many proteins and non-coding RNAs (ncRNAs). In this article, we have critically discussed the crucial role of ncRNAs [such as microRNAs (miRNAs), long non-coding RNAs (lncRNAs), circular RNAs (circRNAs), Piwi-interacting RNAs (piRNAs), and transfer RNA (tRNA)-derived small RNAs (tsRNAs)] in the regulation of stability and expression of HIF-1α. We have comprehensively discussed the molecular mechanisms and relationship of HIF-1α with each type of ncRNA in either promotion or repression of human cancers and therapeutic resistance. We have also elaborated on ncRNAs that are in clinical examination for the treatment of cancers. Overall, the majority of aspects concerning the relationship between HIF-1α and ncRNAs have been discussed in this article.

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
Fig. 5

Similar content being viewed by others

References

  1. Sin, S. Q., Mohan, C. D., Goh, R. M. W.-J., You, M., Nayak, S. C., Chen, L., et al. (2022). Hypoxia signaling in hepatocellular carcinoma: Challenges and therapeutic opportunities. Cancer and Metastasis Reviews. https://doi.org/10.1007/s10555-022-10071-1

  2. Vaupel, P., & Harrison, L. (2004). Tumor Hypoxia: Causative Factors, Compensatory Mechanisms, and Cellular Response. The Oncologist, 9(S5), 4–9. https://doi.org/10.1634/theoncologist.9-90005-4

    Article  PubMed  Google Scholar 

  3. Semenza, G. L. (2000). Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Critical Reviews in Biochemistry and Molecular Biology, 35(2), 71–103. https://doi.org/10.1080/10409230091169186

    Article  CAS  PubMed  Google Scholar 

  4. Muz, B., de la Puente, P., Azab, F., & Azab, A. K. (2015). The role of hypoxia in cancer progression, angiogenesis, metastasis, and resistance to therapy. Hypoxia (Auckl), 3, 83–92. https://doi.org/10.2147/hp.s93413

    Article  PubMed  Google Scholar 

  5. Vaupel, P., Thews, O., & Hoeckel, M. (2001). Treatment resistance of solid tumors: role of hypoxia and anemia. Medical Oncology, 18(4), 243–259. https://doi.org/10.1385/mo:18:4:243

    Article  CAS  PubMed  Google Scholar 

  6. Erler, J. T., Cawthorne, C. J., Williams, K. J., Koritzinsky, M., Wouters, B. G., Wilson, C., et al. (2004). Hypoxia-Mediated Down-Regulation of Bid and Bax in Tumors Occurs via Hypoxia-Inducible Factor 1-Dependent and -Independent Mechanisms and Contributes to Drug Resistance. Molecular and Cellular Biology, 24(7), 2875–2889. https://doi.org/10.1128/MCB.24.7.2875-2889.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Pennacchietti, S., Michieli, P., Galluzzo, M., Mazzone, M., Giordano, S., & Comoglio, P. M. (2003). Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell, 3(4), 347–361. https://doi.org/10.1016/S1535-6108(03)00085-0

    Article  PubMed  Google Scholar 

  8. Graham, A. M., & Presnell, J. S. (2017). Hypoxia Inducible Factor (HIF) transcription factor family expansion, diversification, divergence and selection in eukaryotes. PLoS One, 12(6), e0179545. https://doi.org/10.1371/journal.pone.0179545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Palazon, A., Goldrath, A. W., Nizet, V., & Johnson, R. S. (2014). HIF transcription factors, inflammation, and immunity. Immunity, 41(4), 518–528. https://doi.org/10.1016/j.immuni.2014.09.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cavadas, M. A. S., Nguyen, L. K., & Cheong, A. (2013). Hypoxia-inducible factor (HIF) network: insights from mathematical models. Cell Communication and Signaling: CCS, 11(1), 42. https://doi.org/10.1186/1478-811X-11-42

    Article  PubMed  PubMed Central  Google Scholar 

  11. McNeill, L. A., Hewitson, K. S., Claridge, T. D., Seibel, J. F., Horsfall, L. E., & Schofield, C. J. (2002). Hypoxia-inducible factor asparaginyl hydroxylase (FIH-1) catalyses hydroxylation at the β-carbon of asparagine-803. Biochemical Journal, 367(3), 571–575.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lando, D., Peet, D. J., Whelan, D. A., Gorman, J. J., & Whitelaw, M. L. (2002). Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science, 295(5556), 858–861.

    Article  CAS  PubMed  Google Scholar 

  13. Mahon, P. C., Hirota, K., & Semenza, G. L. (2001). FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes & Development, 15(20), 2675–2686.

    Article  CAS  Google Scholar 

  14. Hashimoto, T., & Shibasaki, F. (2015). Hypoxia-Inducible Factor as an Angiogenic Master Switch. Frontiers in Pediatrics, 3. https://doi.org/10.3389/fped.2015.00033

  15. Cheng, L., Yu, H., Yan, N., Lai, K., & Xiang, M. (2017). Hypoxia-Inducible Factor-1α Target Genes Contribute to Retinal Neuroprotection. Frontiers in Cellular Neuroscience, 11. https://doi.org/10.3389/fncel.2017.00020

  16. Wang, X., Du, Z. W., Xu, T. M., Wang, X. J., Li, W., Gao, J. L., et al. (2021). HIF-1α Is a Rational Target for Future Ovarian Cancer Therapies. Frontiers in Oncology, 11, 785111. https://doi.org/10.3389/fonc.2021.785111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Korbecki, J., Simińska, D., Gąssowska-Dobrowolska, M., Listos, J., Gutowska, I., Chlubek, D., et al. (2021). Chronic and Cycling Hypoxia: Drivers of Cancer Chronic Inflammation through HIF-1 and NF-κB Activation: A Review of the Molecular Mechanisms. International Journal of Molecular Sciences, 22(19). https://doi.org/10.3390/ijms221910701

  18. Tan, P., Wang, M., Zhong, A., Wang, Y., Du, J., Wang, J., et al. (2021). SRT1720 inhibits the growth of bladder cancer in organoids and murine models through the SIRT1-HIF axis. Oncogene, 40(42), 6081–6092. https://doi.org/10.1038/s41388-021-01999-9

    Article  CAS  PubMed  Google Scholar 

  19. Nelson, J. K., Thin, M. Z., Evan, T., Howell, S., Wu, M., Almeida, B., et al. (2022). USP25 promotes pathological HIF-1-driven metabolic reprogramming and is a potential therapeutic target in pancreatic cancer. Nature Communications, 13(1), 2070. https://doi.org/10.1038/s41467-022-29684-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bian, Y., Yin, G., Wang, G., Liu, T., Liang, L., Yang, X., et al. (2022). Degradation of HIF-1α induced by curcumol blocks glutaminolysis and inhibits epithelial-mesenchymal transition and invasion in colorectal cancer cells. Cell Biology and Toxicology. https://doi.org/10.1007/s10565-021-09681-2

  21. Kishore, C., & Karunagaran, D. (2022). Non-coding RNAs as emerging regulators and biomarkers in colorectal cancer. Molecular and Cellular Biochemistry, 477(6), 1817–1828. https://doi.org/10.1007/s11010-022-04412-5

    Article  CAS  PubMed  Google Scholar 

  22. Ashrafizadeh, M., Mohan, C. D., Rangappa, S., Zarrabi, A., Hushmandi, K., Kumar, A. P., et al. (2023). Noncoding RNAs as regulators of STAT3 pathway in gastrointestinal cancers: Roles in cancer progression and therapeutic response. Medicinal Research Reviews. https://doi.org/10.1002/med.21950

  23. Uchino, K., Ochiya, T., & Takeshita, F. (2013). RNAi therapeutics and applications of microRNAs in cancer treatment. Japanese Journal of Clinical Oncology, 43(6), 596–607. https://doi.org/10.1093/jjco/hyt052

    Article  PubMed  Google Scholar 

  24. Wang, Z., Rao, D. D., Senzer, N., & Nemunaitis, J. (2011). RNA interference and cancer therapy. Pharmaceutical Research, 28(12), 2983–2995. https://doi.org/10.1007/s11095-011-0604-5

    Article  CAS  PubMed  Google Scholar 

  25. O'Brien, J., Hayder, H., Zayed, Y., & Peng, C. (2018). Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation. Frontiers in Endocrinology, 9. https://doi.org/10.3389/fendo.2018.00402

  26. Tay, Y., Zhang, J., Thomson, A. M., Lim, B., & Rigoutsos, I. (2008). MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature, 455(7216), 1124–1128. https://doi.org/10.1038/nature07299

    Article  CAS  PubMed  Google Scholar 

  27. Vasudevan, S., Tong, Y., & Steitz, J. A. (2007). Switching from repression to activation: microRNAs can up-regulate translation. Science, 318(5858), 1931–1934. https://doi.org/10.1126/science.1149460

    Article  CAS  PubMed  Google Scholar 

  28. Ørom, U. A., Nielsen, F. C., & Lund, A. H. (2008). MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Molecular Cell, 30(4), 460–471. https://doi.org/10.1016/j.molcel.2008.05.001

    Article  CAS  PubMed  Google Scholar 

  29. Henke, J. I., Goergen, D., Zheng, J., Song, Y., Schüttler, C. G., Fehr, C., et al. (2008). microRNA-122 stimulates translation of hepatitis C virus RNA. The EMBO Journal, 27(24), 3300–3310. https://doi.org/10.1038/emboj.2008.244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Filipowicz, W., Bhattacharyya, S. N., & Sonenberg, N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nature Reviews Genetics, 9(2), 102–114.

    Article  CAS  PubMed  Google Scholar 

  31. Huang, S., Tan, X., Huang, Z., Chen, Z., Lin, P., & Fu, S. W. (2018). microRNA biomarkers in colorectal cancer liver metastasis. Journal of Cancer, 9(21), 3867–3873. https://doi.org/10.7150/jca.28588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zhang, L.-F., Jiang, S., & Liu, M.-F. (2017). MicroRNA regulation and analytical methods in cancer cell metabolism. Cellular and Molecular Life Sciences, 74(16), 2929–2941. https://doi.org/10.1007/s00018-017-2508-y

    Article  CAS  PubMed  Google Scholar 

  33. Syed, S. N., Frank, A. C., Raue, R., & Brüne, B. (2019). MicroRNA-A Tumor Trojan Horse for Tumor-Associated Macrophages. Cells, 8(12). https://doi.org/10.3390/cells8121482

  34. Mirzaei, S., Zarrabi, A., Hashemi, F., Zabolian, A., Saleki, H., Ranjbar, A., et al. (2021). Regulation of Nuclear Factor-KappaB (NF-κB) signaling pathway by non-coding RNAs in cancer: Inhibiting or promoting carcinogenesis? Cancer Letters, 509, 63–80. https://doi.org/10.1016/j.canlet.2021.03.025

    Article  CAS  PubMed  Google Scholar 

  35. Ashrafizadeh, M., Hushmandi, K., Hashemi, M., Akbari, M. E., Kubatka, P., Raei, M., et al. (2020). Role of microRNA/Epithelial-to-Mesenchymal Transition Axis in the Metastasis of Bladder. Cancer., 10(8), 1159.

    CAS  Google Scholar 

  36. Ashrafizadeh, M., Zarrabi, A., Hushmandi, K., Hashemi, F., Moghadam, E. R., Owrang, M., et al. (2021). Lung cancer cells and their sensitivity/resistance to cisplatin chemotherapy: Role of microRNAs and upstream mediators. Cellular Signalling, 78, 109871. https://doi.org/10.1016/j.cellsig.2020.109871

    Article  CAS  PubMed  Google Scholar 

  37. Dutta, M., Das, B., Mohapatra, D., Behera, P., Senapati, S., & Roychowdhury, A. (2022). MicroRNA-217 modulates pancreatic cancer progression via targeting ATAD2. Life Sciences, 301, 120592. https://doi.org/10.1016/j.lfs.2022.120592

    Article  CAS  PubMed  Google Scholar 

  38. Kong, P., Zhu, X., Geng, Q., Xia, L., Sun, X., Chen, Y., et al. (2017). The microRNA-423-3p-Bim Axis Promotes Cancer Progression and Activates Oncogenic Autophagy in Gastric Cancer. Molecular Therapy, 25(4), 1027–1037. https://doi.org/10.1016/j.ymthe.2017.01.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Quinn, J. J., & Chang, H. Y. (2016). Unique features of long non-coding RNA biogenesis and function. Nature Reviews Genetics, 17(1), 47–62. https://doi.org/10.1038/nrg.2015.10

    Article  CAS  PubMed  Google Scholar 

  40. Wooten, S., & Smith, K. N. (2022). Long non-coding RNA OIP5-AS1 (Cyrano): A context-specific regulator of normal and disease processes. Clinical and Translational Medicine, 12(1), e706. https://doi.org/10.1002/ctm2.706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Yang, G., Lu, X., & Yuan, L. (2014). LncRNA: a link between RNA and cancer. Biochimica et Biophysica Acta, 1839(11), 1097–1109. https://doi.org/10.1016/j.bbagrm.2014.08.012

    Article  CAS  PubMed  Google Scholar 

  42. Hashemi, M., Hajimazdarany, S., Mohan, C. D., Mohammadi, M., Rezaei, S., Olyaee, Y., et al. (2022). Long non-coding RNA/epithelial-mesenchymal transition axis in human cancers: Tumorigenesis, chemoresistance, and radioresistance. Pharmacological Research, 186, 106535. https://doi.org/10.1016/j.phrs.2022.106535

    Article  CAS  PubMed  Google Scholar 

  43. Mohan, C. D., Rangappa, S., Nayak, S. C., Sethi, G., & Rangappa, K. S. (2021). Paradoxical functions of long noncoding RNAs in modulating STAT3 signaling pathway in hepatocellular carcinoma. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer, 1876(1), 188574. https://doi.org/10.1016/j.bbcan.2021.188574

    Article  CAS  PubMed  Google Scholar 

  44. Wen, A., Luo, L., Du, C., & Luo, X. (2021). Long non-coding RNA miR155HG silencing restrains ovarian cancer progression by targeting the microRNA-155-5p/tyrosinase-related protein 1 axis. Experimental and Therapeutic Medicine, 22(5), 1237. https://doi.org/10.3892/etm.2021.10672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mo, C., Wu, J., Sui, J., Deng, Y., Li, M., Cao, Z., et al. (2022). Long non-coding RNA LINC01793 as a potential diagnostic biomarker of hepatitis B virus-related hepatocellular carcinoma. Clinical Biochemistry. https://doi.org/10.1016/j.clinbiochem.2022.06.006

  46. Liang, M., Zhu, B., Wang, M., & Jin, J. (2022). Knockdown of long non-coding RNA DDX11-AS1 inhibits the proliferation, migration and paclitaxel resistance of breast cancer cells by upregulating microRNA-497 expression. Molecular Medicine Reports, 25(4). https://doi.org/10.3892/mmr.2022.12639

  47. Wang, W., Zhang, Z., Li, Y., Gu, A., Wang, Y., Cai, Y., et al. (2022). Down-regulated long non-coding RNA LHFPL3 antisense RNA 1 inhibits the radiotherapy resistance of nasopharyngeal carcinoma via modulating microRNA-143-5p/homeobox A6 axis. Bioengineered, 13(3), 5421–5433. https://doi.org/10.1080/21655979.2021.2024386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Rong, D., Sun, H., Li, Z., Liu, S., Dong, C., Fu, K., et al. (2017). An emerging function of circRNA-miRNAs-mRNA axis in human diseases. Oncotarget, 8(42), 73271–73281. https://doi.org/10.18632/oncotarget.19154

    Article  PubMed  PubMed Central  Google Scholar 

  49. Nigro, J. M., Cho, K. R., Fearon, E. R., Kern, S. E., Ruppert, J. M., Oliner, J. D., et al. (1991). Scrambled exons. Cell, 64(3), 607–613. https://doi.org/10.1016/0092-8674(91)90244-s

    Article  CAS  PubMed  Google Scholar 

  50. Sanger, H. L., Klotz, G., Riesner, D., Gross, H. J., & Kleinschmidt, A. K. (1976). Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proceedings of the National Academy of Sciences of the United States of America, 73(11), 3852–3856. https://doi.org/10.1073/pnas.73.11.3852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kolakofsky, D. (1976). Isolation and characterization of Sendai virus DI-RNAs. Cell, 8(4), 547–555. https://doi.org/10.1016/0092-8674(76)90223-3

    Article  CAS  PubMed  Google Scholar 

  52. Zhou, G. R., Huang, D. P., Sun, Z. F., & Zhang, X. F. (2020). Characteristics and prognostic significance of circRNA-100876 in patients with colorectal cancer. European Review for Medical and Pharmacological Sciences, 24(22), 11587–11593. https://doi.org/10.26355/eurrev_202011_23801

    Article  PubMed  Google Scholar 

  53. Ishola, A. A., Chien, C. S., Yang, Y. P., Chien, Y., Yarmishyn, A. A., Tsai, P. H., et al. (2022). Oncogenic circRNA C190 Promotes Non-Small Cell Lung Cancer via Modulation of the EGFR/ERK Pathway. Cancer Research, 82(1), 75–89. https://doi.org/10.1158/0008-5472.Can-21-1473

    Article  CAS  PubMed  Google Scholar 

  54. Cai, A., Hu, Y., Zhou, Z., Qi, Q., Wu, Y., Dong, P., et al. (2022). PIWI-Interacting RNAs (piRNAs): Promising Applications as Emerging Biomarkers for Digestive System Cancer. Frontiers in Molecular Biosciences, 9. https://doi.org/10.3389/fmolb.2022.848105

  55. Xiao, Y., & Ke, A. (2016). PIWI Takes a Giant Step. Cell, 167(2), 310–312. https://doi.org/10.1016/j.cell.2016.09.043

    Article  CAS  PubMed  Google Scholar 

  56. Ozata, D. M., Gainetdinov, I., Zoch, A., O’Carroll, D., & Zamore, P. D. (2019). PIWI-interacting RNAs: small RNAs with big functions. Nature Reviews Genetics, 20(2), 89–108. https://doi.org/10.1038/s41576-018-0073-3

    Article  CAS  PubMed  Google Scholar 

  57. Tan, L., Mai, D., Zhang, B., Jiang, X., Zhang, J., Bai, R., et al. (2019). PIWI-interacting RNA-36712 restrains breast cancer progression and chemoresistance by interaction with SEPW1 pseudogene SEPW1P RNA. Molecular Cancer, 18(1), 9. https://doi.org/10.1186/s12943-019-0940-3

    Article  PubMed  PubMed Central  Google Scholar 

  58. Cheng, J., Guo, J. M., Xiao, B. X., Miao, Y., Jiang, Z., Zhou, H., et al. (2011). piRNA, the new non-coding RNA, is aberrantly expressed in human cancer cells. Clinica Chimica Acta, 412(17-18), 1621–1625. https://doi.org/10.1016/j.cca.2011.05.015

    Article  CAS  Google Scholar 

  59. Di Fazio, A., & Gullerova, M. (2023). An old friend with a new face: tRNA-derived small RNAs with big regulatory potential in cancer biology. British Journal of Cancer, 128(9), 1625–1635. https://doi.org/10.1038/s41416-023-02191-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wen, J.-T., Huang, Z.-H., Li, Q.-H., Chen, X., Qin, H.-L., & Zhao, Y. (2021). Research progress on the tsRNA classification, function, and application in gynecological malignant tumors. Cell Death Discovery, 7(1), 388. https://doi.org/10.1038/s41420-021-00789-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Li, X., Liu, X., Zhao, D., Cui, W., Wu, Y., Zhang, C., et al. (2021). tRNA-derived small RNAs: novel regulators of cancer hallmarks and targets of clinical application. Cell Death Discovery, 7(1), 249. https://doi.org/10.1038/s41420-021-00647-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ivanov, P., Emara, M. M., Villen, J., Gygi, S. P., & Anderson, P. (2011). Angiogenin-induced tRNA fragments inhibit translation initiation. Molecular Cell, 43(4), 613–623. https://doi.org/10.1016/j.molcel.2011.06.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Haussecker, D., Huang, Y., Lau, A., Parameswaran, P., Fire, A. Z., & Kay, M. A. (2010). Human tRNA-derived small RNAs in the global regulation of RNA silencing. Rna, 16(4), 673–695. https://doi.org/10.1261/rna.2000810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Goodarzi, H., Liu, X., Nguyen, H. C., Zhang, S., Fish, L., & Tavazoie, S. F. (2015). Endogenous tRNA-Derived Fragments Suppress Breast Cancer Progression via YBX1 Displacement. Cell, 161(4), 790–802. https://doi.org/10.1016/j.cell.2015.02.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Saikia, M., Jobava, R., Parisien, M., Putnam, A., Krokowski, D., Gao, X. H., et al. (2014). Angiogenin-cleaved tRNA halves interact with cytochrome c, protecting cells from apoptosis during osmotic stress. Molecular and Cellular Biology, 34(13), 2450–2463. https://doi.org/10.1128/mcb.00136-14

    Article  PubMed  PubMed Central  Google Scholar 

  66. Shao, Y., Sun, Q., Liu, X., Wang, P., Wu, R., & Ma, Z. (2017). tRF-Leu-CAG promotes cell proliferation and cell cycle in non-small cell lung cancer. Chemical Biology & Drug Design, 90(5), 730–738. https://doi.org/10.1111/cbdd.12994

    Article  CAS  Google Scholar 

  67. Luan, N., Chen, Y., Li, Q., Mu, Y., Zhou, Q., Ye, X., et al. (2021). TRF-20-M0NK5Y93 suppresses the metastasis of colon cancer cells by impairing the epithelial-to-mesenchymal transition through targeting Claudin-1. American Journal of Translational Research, 13(1), 124–142.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. He, C., Wang, L., Zhang, J., & Xu, H. (2017). Hypoxia-inducible microRNA-224 promotes the cell growth, migration and invasion by directly targeting RASSF8 in gastric cancer. Molecular Cancer, 16(1), 35. https://doi.org/10.1186/s12943-017-0603-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhu, G., Zhou, L., Liu, H., Shan, Y., & Zhang, X. (2018). MicroRNA-224 Promotes Pancreatic Cancer Cell Proliferation and Migration by Targeting the TXNIP-Mediated HIF1α Pathway. Cellular Physiology and Biochemistry, 48(4), 1735–1746. https://doi.org/10.1159/000492309

    Article  CAS  PubMed  Google Scholar 

  70. Xia, M., Wei, J., & Tong, K. (2016). MiR-224 promotes proliferation and migration of gastric cancer cells through targeting PAK4. Pharmazie, 71(8), 460–464. https://doi.org/10.1691/ph.2016.6580

    Article  CAS  PubMed  Google Scholar 

  71. Zhang, Y., Li, C. F., Ma, L. J., Ding, M., & Zhang, B. (2016). MicroRNA-224 aggrevates tumor growth and progression by targeting mTOR in gastric cancer. International Journal of Oncology, 49(3), 1068–1080. https://doi.org/10.3892/ijo.2016.3581

    Article  CAS  PubMed  Google Scholar 

  72. Li, Y., Zhao, L., Qi, Y., & Yang, X. (2019). MicroRNA-214 upregulates HIF-1α and VEGF by targeting ING4 in lung cancer cells. Molecular Medicine Reports, 19(6), 4935–4945. https://doi.org/10.3892/mmr.2019.10170

    Article  CAS  PubMed  Google Scholar 

  73. Ji, Z., Wang, X., Liu, Y., Zhong, M., Sun, J., & Shang, J. (2022). MicroRNA-574-3p Regulates HIF-α Isoforms Promoting Gastric Cancer Epithelial-Mesenchymal Transition via Targeting CUL2. Digestive Diseases and Sciences, 67(8), 3714–3724. https://doi.org/10.1007/s10620-021-07263-0

    Article  CAS  PubMed  Google Scholar 

  74. Xia, X., Wang, S., Ni, B., Xing, S., Cao, H., Zhang, Z., et al. (2020). Hypoxic gastric cancer-derived exosomes promote progression and metastasis via MiR-301a-3p/PHD3/HIF-1α positive feedback loop. Oncogene, 39(39), 6231–6244. https://doi.org/10.1038/s41388-020-01425-6

    Article  CAS  PubMed  Google Scholar 

  75. Kelly, T. J., Souza, A. L., Clish, C. B., & Puigserver, P. (2011). A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like. Molecular and Cellular Biology, 31(13), 2696–2706. https://doi.org/10.1128/mcb.01242-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Du, Y., Wei, N., Ma, R., Jiang, S., & Song, D. (2020). A miR-210-3p regulon that controls the Warburg effect by modulating HIF-1α and p53 activity in triple-negative breast cancer. Cell Death & Disease, 11(9), 731. https://doi.org/10.1038/s41419-020-02952-6

    Article  CAS  Google Scholar 

  77. DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G., Thompson, C. B. J. C., & m. (2008). The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metabolism, 7(1), 11–20.

    Article  CAS  PubMed  Google Scholar 

  78. Hanahan, D., & Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell, 144(5), 646–674.

    Article  CAS  PubMed  Google Scholar 

  79. Hsu, P. P., & Sabatini, D. M. J. C. (2008). Cancer cell metabolism: Warburg and beyond., 134(5), 703–707.

    CAS  Google Scholar 

  80. Vander Heiden, M. G., Cantley, L. C., Thompson, C. B. J., & s. (2009). Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science, 324(5930), 1029–1033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. DeBerardinis, R. J., & Chandel, N. S. (2016). Fundamentals of cancer metabolism. Science Advances, 2(5), e1600200. https://doi.org/10.1126/sciadv.1600200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Lee, N., & Kim, D. (2016). Cancer metabolism: fueling more than just growth. Molecules and Cells, 39(12), 847.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Pavlova, N. N., Thompson, C. B. J. C., & m. (2016). The emerging hallmarks of cancer metabolism. Cell Metabolism, 23(1), 27–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Zhang, S., Zhang, R., Xu, R., Shang, J., He, H., & Yang, Q. (2020). MicroRNA-574-5p in gastric cancer cells promotes angiogenesis by targeting protein tyrosine phosphatase non-receptor type 3 (PTPN3). Gene, 733, 144383. https://doi.org/10.1016/j.gene.2020.144383

    Article  CAS  PubMed  Google Scholar 

  85. Seok, J. K., Lee, S. H., Kim, M. J., & Lee, Y. M. (2014). MicroRNA-382 induced by HIF-1α is an angiogenic miR targeting the tumor suppressor phosphatase and tensin homolog. Nucleic Acids Research, 42(12), 8062–8072. https://doi.org/10.1093/nar/gku515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Qiu, H., Chen, F., & Chen, M. (2019). MicroRNA-138 negatively regulates the hypoxia-inducible factor 1α to suppress melanoma growth and metastasis. Biol Open, 8(8). https://doi.org/10.1242/bio.042937

  87. Wu, F., Huang, W., & Wang, X. (2015). microRNA-18a regulates gastric carcinoma cell apoptosis and invasion by suppressing hypoxia-inducible factor-1α expression. Experimental and Therapeutic Medicine, 10(2), 717–722. https://doi.org/10.3892/etm.2015.2546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Shi, J., Wang, H., Feng, W., Huang, S., An, J., Qiu, Y., et al. (2020). MicroRNA-130a targeting hypoxia-inducible factor 1 alpha suppresses cell metastasis and Warburg effect of NSCLC cells under hypoxia. Life Sciences, 255, 117826. https://doi.org/10.1016/j.lfs.2020.117826

    Article  CAS  PubMed  Google Scholar 

  89. Choi, J. Y., Seok, H. J., Kim, R. K., Choi, M. Y., Lee, S. J., & Bae, I. H. (2021). miR-519d-3p suppresses tumorigenicity and metastasis by inhibiting Bcl-w and HIF-1α in NSCLC. Mol Ther Oncolytics, 22, 368–379. https://doi.org/10.1016/j.omto.2021.06.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Hu, Q., Liu, F., Yan, T., Wu, M., Ye, M., Shi, G., et al. (2019). MicroRNA-576-3p inhibits the migration and proangiogenic abilities of hypoxia-treated glioma cells through hypoxia-inducible factor-1α. International Journal of Molecular Medicine, 43(6), 2387–2397. https://doi.org/10.3892/ijmm.2019.4157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Cheng, C. W., Chen, P. M., Hsieh, Y. H., Weng, C. C., Chang, C. W., Yao, C. C., et al. (2015). Foxo3a-mediated overexpression of microRNA-622 suppresses tumor metastasis by repressing hypoxia-inducible factor-1α in ERK-responsive lung cancer. Oncotarget, 6(42), 44222–44238. https://doi.org/10.18632/oncotarget.5826

    Article  PubMed  PubMed Central  Google Scholar 

  92. Ang, H. L., Mohan, C. D., Shanmugam, M. K., Leong, H. C., Makvandi, P., Rangappa, K. S., et al. (2023). Mechanism of epithelial-mesenchymal transition in cancer and its regulation by natural compounds. Medicinal Research Reviews, 43(4), 1141–1200. https://doi.org/10.1002/med.21948

    Article  CAS  PubMed  Google Scholar 

  93. Huang, X., Liu, F., Jiang, Z., Guan, H., & Jia, Q. (2020). CREB1 Suppresses Transcription of microRNA-186 to Promote Growth, Invasion and Epithelial-Mesenchymal Transition of Gastric Cancer Cells Through the KRT8/HIF-1α Axis. Cancer Management and Research, 12, 9097–9111. https://doi.org/10.2147/cmar.S265187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Peng, D., Wu, T., Wang, J., Huang, J., Zheng, L., Wang, P., et al. (2022). microRNA-671-5p reduces tumorigenicity of ovarian cancer via suppressing HDAC5 and HIF-1α expression. Chemico-Biological Interactions, 355, 109780. https://doi.org/10.1016/j.cbi.2021.109780

    Article  CAS  PubMed  Google Scholar 

  95. Hu, S., Cao, P., Kong, K., Han, P., Deng, Y., Li, F., et al. (2021). MicroRNA-449a delays lung cancer development through inhibiting KDM3A/HIF-1α axis. Journal of Translational Medicine, 19(1), 224. https://doi.org/10.1186/s12967-021-02881-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Li, X., Li, H., Zhang, R., Liu, J., & Liu, J. (2015). MicroRNA-449a inhibits proliferation and induces apoptosis by directly repressing E2F3 in gastric cancer. Cellular Physiology and Biochemistry, 35(5), 2033–2042. https://doi.org/10.1159/000374010

    Article  CAS  PubMed  Google Scholar 

  97. Xu, B., Zhang, X., Wang, S., & Shi, B. (2018). MiR-449a suppresses cell migration and invasion by targeting PLAGL2 in breast cancer. Pathology, Research and Practice, 214(5), 790–795. https://doi.org/10.1016/j.prp.2017.12.012

    Article  CAS  PubMed  Google Scholar 

  98. Wang, L., Zhao, Y., Xiong, W., Ye, W., Zhao, W., & Hua, Y. (2019). MicroRNA-449a Is Downregulated in Cervical Cancer and Inhibits Proliferation, Migration, and Invasion. Oncol Res Treat, 42(11), 564–571. https://doi.org/10.1159/000502122

    Article  CAS  PubMed  Google Scholar 

  99. Wu, X., Han, Y., Liu, F., & Ruan, L. (2020). Downregulations of miR-449a and miR-145-5p Act as Prognostic Biomarkers for Endometrial Cancer. Journal of Computational Biology, 27(5), 834–844. https://doi.org/10.1089/cmb.2019.0215

    Article  CAS  PubMed  Google Scholar 

  100. Yogev, O., Henderson, S., Hayes, M. J., Marelli, S. S., Ofir-Birin, Y., Regev-Rudzki, N., et al. (2017). Herpesviruses shape tumour microenvironment through exosomal transfer of viral microRNAs. PLoS Pathogens, 13(8), e1006524. https://doi.org/10.1371/journal.ppat.1006524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Pucci, F., & Pittet, M. J. (2013). Molecular pathways: tumor-derived microvesicles and their interactions with immune cells in vivo. Clinical Cancer Research, 19(10), 2598–2604. https://doi.org/10.1158/1078-0432.Ccr-12-0962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. King, H. W., Michael, M. Z., & Gleadle, J. M. (2012). Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer, 12, 421. https://doi.org/10.1186/1471-2407-12-421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Kucharzewska, P., Christianson, H. C., Welch, J. E., Svensson, K. J., Fredlund, E., Ringnér, M., et al. (2013). Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proceedings of the National Academy of Sciences of the United States of America, 110(18), 7312–7317. https://doi.org/10.1073/pnas.1220998110

    Article  PubMed  PubMed Central  Google Scholar 

  104. Li, S., Yi, M., Dong, B., Jiao, Y., Luo, S., & Wu, K. (2020). The roles of exosomes in cancer drug resistance and its therapeutic application. Clinical and Translational Medicine, 10(8), e257. https://doi.org/10.1002/ctm2.257

    Article  PubMed  PubMed Central  Google Scholar 

  105. Zhu, X., Shen, H., Yin, X., Yang, M., Wei, H., Chen, Q., et al. (2019). Macrophages derived exosomes deliver miR-223 to epithelial ovarian cancer cells to elicit a chemoresistant phenotype. Journal of Experimental & Clinical Cancer Research, 38(1), 81. https://doi.org/10.1186/s13046-019-1095-1

    Article  Google Scholar 

  106. Xu, K., Zhan, Y., Yuan, Z., Qiu, Y., Wang, H., Fan, G., et al. (2019). Hypoxia Induces Drug Resistance in Colorectal Cancer through the HIF-1α/miR-338-5p/IL-6 Feedback Loop. Molecular Therapy, 27(10), 1810–1824. https://doi.org/10.1016/j.ymthe.2019.05.017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Mohan, C. D., Rangappa, S., Preetham, H. D., Chandra Nayaka, S., Gupta, V. K., Basappa, S., et al. (2022). Targeting STAT3 signaling pathway in cancer by agents derived from Mother Nature. Seminars in Cancer Biology, 80, 157–182. https://doi.org/10.1016/j.semcancer.2020.03.016

    Article  CAS  PubMed  Google Scholar 

  108. Keerthy, H. K., Garg, M., Mohan, C. D., Madan, V., Kanojia, D., Shobith, R., et al. (2014). Synthesis and Characterization of Novel 2-Amino-Chromene-Nitriles that Target Bcl-2 in Acute Myeloid Leukemia Cell Lines. PLoS One, 9(9), e107118. https://doi.org/10.1371/journal.pone.0107118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Anusha, S., Mohan, C. D., Ananda, H., Baburajeev, C. P., Rangappa, S., Mathai, J., et al. (2016). Adamantyl-tethered-biphenylic compounds induce apoptosis in cancer cells by targeting Bcl homologs. Bioorganic & Medicinal Chemistry Letters, 26(3), 1056–1060. https://doi.org/10.1016/j.bmcl.2015.12.026

    Article  CAS  Google Scholar 

  110. Mohan, C. D., Kim, C., Siveen, K. S., Manu, K. A., Rangappa, S., Chinnathambi, A., et al. (2021). Crocetin imparts antiproliferative activity via inhibiting STAT3 signaling in hepatocellular carcinoma. IUBMB Life, 73(11), 1348–1362. https://doi.org/10.1002/iub.2555

    Article  CAS  PubMed  Google Scholar 

  111. Liu, H., Chen, C., Zeng, J., Zhao, Z., & Hu, Q. (2021). MicroRNA-210-3p is transcriptionally upregulated by hypoxia induction and thus promoting EMT and chemoresistance in glioma cells. PLoS One, 16(7), e0253522. https://doi.org/10.1371/journal.pone.0253522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Ge, X., Liu, X., Lin, F., Li, P., Liu, K., Geng, R., et al. (2016). MicroRNA-421 regulated by HIF-1α promotes metastasis, inhibits apoptosis, and induces cisplatin resistance by targeting E-cadherin and caspase-3 in gastric cancer. Oncotarget, 7(17), 24466–24482. https://doi.org/10.18632/oncotarget.8228

    Article  PubMed  PubMed Central  Google Scholar 

  113. Koo, T., Cho, B. J., Kim, D. H., Park, J. M., Choi, E. J., Kim, H. H., et al. (2017). MicroRNA-200c increases radiosensitivity of human cancer cells with activated EGFR-associated signaling. Oncotarget, 8(39), 65457–65468. https://doi.org/10.18632/oncotarget.18924

    Article  PubMed  PubMed Central  Google Scholar 

  114. Byun, Y., Choi, Y. C., Jeong, Y., Lee, G., Yoon, S., Jeong, Y., et al. (2019). MiR-200c downregulates HIF-1α and inhibits migration of lung cancer cells. Cellular & Molecular Biology Letters, 24, 28. https://doi.org/10.1186/s11658-019-0152-2

    Article  CAS  Google Scholar 

  115. Xu, Z., Zhu, C., Chen, C., Zong, Y., Feng, H., Liu, D., et al. (2018). CCL19 suppresses angiogenesis through promoting miR-206 and inhibiting Met/ERK/Elk-1/HIF-1α/VEGF-A pathway in colorectal cancer. Cell Death & Disease, 9(10), 974. https://doi.org/10.1038/s41419-018-1010-2

    Article  CAS  Google Scholar 

  116. Xu, F., Hu, Y., Gao, J., Wang, J., Xie, Y., Sun, F., et al. (2022). HIF-1α/Malat1/miR-141 Axis Activates Autophagy to Increase Proliferation, Migration, and Invasion in Triple-negative Breast Cancer. Current Cancer Drug Targets. https://doi.org/10.2174/1568009623666221228104833

  117. Zhang, Y., Yan, J., Wang, L., Dai, H., Li, N., Hu, W., et al. (2017). HIF-1α Promotes Breast Cancer Cell MCF-7 Proliferation and Invasion Through Regulating miR-210. Cancer Biotherapy & Radiopharmaceuticals, 32(8), 297–301. https://doi.org/10.1089/cbr.2017.2270

    Article  CAS  Google Scholar 

  118. He, M., Zhan, M., Chen, W., Xu, S., Long, M., Shen, H., et al. (2017). MiR-143-5p Deficiency Triggers EMT and Metastasis by Targeting HIF-1α in Gallbladder Cancer. Cellular Physiology and Biochemistry, 42(5), 2078–2092. https://doi.org/10.1159/000479903

    Article  CAS  PubMed  Google Scholar 

  119. Zhang, C., Tian, W., Meng, L., Qu, L., & Shou, C. (2016). PRL-3 promotes gastric cancer migration and invasion through a NF-κB-HIF-1α-miR-210 axis. Journal of Molecular Medicine (Berlin, Germany), 94(4), 401–415. https://doi.org/10.1007/s00109-015-1350-7

    Article  CAS  PubMed  Google Scholar 

  120. Lv, D., Shen, T., Yao, J., Yang, Q., Xiang, Y., & Ma, Z. (2021). HIF-1α Induces HECTD2 Up-Regulation and Aggravates the Malignant Progression of Renal Cell Cancer via Repressing miR-320a. Frontiers in Cell and Development Biology, 9, 775642. https://doi.org/10.3389/fcell.2021.775642

    Article  Google Scholar 

  121. Zhou, B., Lei, J. H., Wang, Q., Qu, T. F., Cha, L. C., Zhan, H. X., et al. (2022). Cancer-associated fibroblast-secreted miR-421 promotes pancreatic cancer by regulating the SIRT3/H3K9Ac/HIF-1α axis. The Kaohsiung Journal of Medical Sciences, 38(11), 1080–1092. https://doi.org/10.1002/kjm2.12590

    Article  CAS  PubMed  Google Scholar 

  122. Lu, Y., Ji, N., Wei, W., Sun, W., Gong, X., & Wang, X. (2017). MiR-142 modulates human pancreatic cancer proliferation and invasion by targeting hypoxia-inducible factor 1 (HIF-1α) in the tumor microenvironments. Biol Open, 6(2), 252–259. https://doi.org/10.1242/bio.021774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Chiang, C. H., Chu, P. Y., Hou, M. F., & Hung, W. C. (2016). MiR-182 promotes proliferation and invasion and elevates the HIF-1α-VEGF-A axis in breast cancer cells by targeting FBXW7. American Journal of Cancer Research, 6(8), 1785–1798.

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Jin, F., Yang, R., Wei, Y., Wang, D., Zhu, Y., Wang, X., et al. (2019). HIF-1α-induced miR-23a∼27a∼24 cluster promotes colorectal cancer progression via reprogramming metabolism. Cancer Letters, 440-441, 211–222. https://doi.org/10.1016/j.canlet.2018.10.025

    Article  CAS  PubMed  Google Scholar 

  125. Ma, C. N., Wo, L. L., Wang, D. F., Zhou, C. X., Li, J. C., Zhang, X., et al. (2021). Hypoxia activated long non-coding RNA HABON regulates the growth and proliferation of hepatocarcinoma cells by binding to and antagonizing HIF-1 alpha. RNA Biology, 18(11), 1791–1806. https://doi.org/10.1080/15476286.2020.1871215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Chen, F., Chen, J., Yang, L., Liu, J., Zhang, X., Zhang, Y., et al. (2019). Extracellular vesicle-packaged HIF-1α-stabilizing lncRNA from tumour-associated macrophages regulates aerobic glycolysis of breast cancer cells. Nature Cell Biology, 21(4), 498–510. https://doi.org/10.1038/s41556-019-0299-0

    Article  CAS  PubMed  Google Scholar 

  127. Hua, Q., Mi, B., Xu, F., Wen, J., Zhao, L., Liu, J., et al. (2020). Hypoxia-induced lncRNA-AC020978 promotes proliferation and glycolytic metabolism of non-small cell lung cancer by regulating PKM2/HIF-1α axis. Theranostics, 10(11), 4762–4778. https://doi.org/10.7150/thno.43839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Xu, L., Huan, L., Guo, T., Wu, Y., Liu, Y., Wang, Q., et al. (2020). LncRNA SNHG11 facilitates tumor metastasis by interacting with and stabilizing HIF-1α. Oncogene, 39(46), 7005–7018. https://doi.org/10.1038/s41388-020-01512-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Liu, P., Huang, H., Qi, X., Bian, C., Cheng, M., Liu, L., et al. (2021). Hypoxia-Induced LncRNA-MIR210HG Promotes Cancer Progression By Inhibiting HIF-1α Degradation in Ovarian Cancer. Frontiers in Oncology, 11, 701488. https://doi.org/10.3389/fonc.2021.701488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Mineo, M., Ricklefs, F., Rooj, A. K., Lyons, S. M., Ivanov, P., Ansari, K. I., et al. (2016). The Long Non-coding RNA HIF1A-AS2 Facilitates the Maintenance of Mesenchymal Glioblastoma Stem-like Cells in Hypoxic Niches. Cell Reports, 15(11), 2500–2509. https://doi.org/10.1016/j.celrep.2016.05.018

    Article  CAS  PubMed  Google Scholar 

  131. Tong, J., Xu, X., Zhang, Z., Ma, C., Xiang, R., Liu, J., et al. (2020). Hypoxia-induced long non-coding RNA DARS-AS1 regulates RBM39 stability to promote myeloma malignancy. Haematologica, 105(6), 1630–1640. https://doi.org/10.3324/haematol.2019.218289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Qian, Y., Wang, R., Wei, W., Wang, M., & Wang, S. (2021). Resveratrol reverses the cadmium-promoted migration, invasion, and epithelial-mesenchymal transition procession by regulating the expression of ZEB1. Human & Experimental Toxicology, 40(12_suppl), S331–s338. https://doi.org/10.1177/09603271211041678

    Article  CAS  Google Scholar 

  133. Kalinkova, L., Nikolaieva, N., Smolkova, B., Ciernikova, S., Kajo, K., Bella, V., et al. (2021). miR-205-5p Downregulation and ZEB1 Upregulation Characterize the Disseminated Tumor Cells in Patients with Invasive Ductal Breast Cancer. International Journal of Molecular Sciences, 23(1). https://doi.org/10.3390/ijms23010103

  134. Deng, S. J., Chen, H. Y., Ye, Z., Deng, S. C., Zhu, S., Zeng, Z., et al. (2018). Hypoxia-induced LncRNA-BX111 promotes metastasis and progression of pancreatic cancer through regulating ZEB1 transcription. Oncogene, 37(44), 5811–5828. https://doi.org/10.1038/s41388-018-0382-1

    Article  CAS  PubMed  Google Scholar 

  135. Zhang, J., Jin, H. Y., Wu, Y., Zheng, Z. C., Guo, S., Wang, Y., et al. (2019). Hypoxia-induced LncRNA PCGEM1 promotes invasion and metastasis of gastric cancer through regulating SNAI1. Clinical and Translational Oncology, 21(9), 1142–1151. https://doi.org/10.1007/s12094-019-02035-9

    Article  CAS  PubMed  Google Scholar 

  136. Li, L., Wang, M., Mei, Z., Cao, W., Yang, Y., Wang, Y., et al. (2017). lncRNAs HIF1A-AS2 facilitates the up-regulation of HIF-1α by sponging to miR-153-3p, whereby promoting angiogenesis in HUVECs in hypoxia. Biomedicine & Pharmacotherapy, 96, 165–172. https://doi.org/10.1016/j.biopha.2017.09.113

    Article  CAS  Google Scholar 

  137. Barth, D. A., Prinz, F., Teppan, J., Jonas, K., Klec, C., & Pichler, M. (2020). Long-noncoding RNA (lncRNA) in the regulation of hypoxia-inducible factor (HIF) in cancer. Non-coding RNA, 6(3), 27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Kanamori, A., Matsubara, D., Saitoh, Y., Fukui, Y., Gotoh, N., Kaneko, S., et al. (2020). Mint3 depletion restricts tumor malignancy of pancreatic cancer cells by decreasing SKP2 expression via HIF-1. Oncogene, 39(39), 6218–6230. https://doi.org/10.1038/s41388-020-01423-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Liu, M., Zhong, J., Zeng, Z., Huang, K., Ye, Z., Deng, S., et al. (2019). Hypoxia-induced feedback of HIF-1α and lncRNA-CF129 contributes to pancreatic cancer progression through stabilization of p53 protein. Theranostics, 9(16), 4795–4810. https://doi.org/10.7150/thno.30988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Wang, X., Li, L., Zhao, K., Lin, Q., Li, H., Xue, X., et al. (2020). A novel LncRNA HITT forms a regulatory loop with HIF-1α to modulate angiogenesis and tumor growth. Cell Death and Differentiation, 27(4), 1431–1446. https://doi.org/10.1038/s41418-019-0449-8

    Article  CAS  PubMed  Google Scholar 

  141. Kim, K. H., & Roberts, C. W. (2016). Targeting EZH2 in cancer. Nature Medicine, 22(2), 128–134. https://doi.org/10.1038/nm.4036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Sun, Y. W., Chen, Y. F., Li, J., Huo, Y. M., Liu, D. J., Hua, R., et al. (2014). A novel long non-coding RNA ENST00000480739 suppresses tumour cell invasion by regulating OS-9 and HIF-1α in pancreatic ductal adenocarcinoma. British Journal of Cancer, 111(11), 2131–2141. https://doi.org/10.1038/bjc.2014.520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Zhang, W., Yuan, W., Song, J., Wang, S., & Gu, X. (2018). LncRNA CPS1-IT1 suppresses EMT and metastasis of colorectal cancer by inhibiting hypoxia-induced autophagy through inactivation of HIF-1α. Biochimie, 144, 21–27. https://doi.org/10.1016/j.biochi.2017.10.002

    Article  CAS  PubMed  Google Scholar 

  144. Wang, G., Dong, Y., Liu, H., Ji, N., Cao, J., Liu, A., et al. (2022). Long noncoding RNA (lncRNA) metallothionein 1 J, pseudogene (MT1JP) is downregulated in triple-negative breast cancer and upregulates microRNA-138 (miR-138) to downregulate hypoxia-inducible factor-1α (HIF-1α). Bioengineered, 13(5), 13718–13727. https://doi.org/10.1080/21655979.2022.2077906

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Li, W., Han, S., Hu, P., Chen, D., Zeng, Z., Hu, Y., et al. (2021). LncRNA ZNFTR functions as an inhibitor in pancreatic cancer by modulating ATF3/ZNF24/VEGFA pathway. Cell Death & Disease, 12(9), 830. https://doi.org/10.1038/s41419-021-04119-3

    Article  CAS  Google Scholar 

  146. Zhu, Y., Wu, F., Gui, W., Zhang, N., Matro, E., Zhu, L., et al. (2021). A positive feedback regulatory loop involving the lncRNA PVT1 and HIF-1α in pancreatic cancer. Journal of Molecular Cell Biology, 13(9), 676–689. https://doi.org/10.1093/jmcb/mjab042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Liu, Y.-F., Luo, D., Li, X., Li, Z.-Q., Yu, X., & Zhu, H.-W. (2021). PVT1 Knockdown Inhibits Autophagy and Improves Gemcitabine Sensitivity by Regulating the MiR-143/HIF-1α/VMP1 Axis in Pancreatic Cancer. Pancreas, 50(2), 227–234. https://doi.org/10.1097/mpa.0000000000001747

    Article  CAS  PubMed  Google Scholar 

  148. Zhang, L., Wu, H., Zhang, Y., Xiao, X., Chu, F., & Zhang, L. (2022). Induction of lncRNA NORAD accounts for hypoxia-induced chemoresistance and vasculogenic mimicry in colorectal cancer by sponging the miR-495-3p/ hypoxia-inducible factor-1α (HIF-1α). Bioengineered, 13(1), 950–962. https://doi.org/10.1080/21655979.2021.2015530

    Article  CAS  PubMed  Google Scholar 

  149. Jin, L., Ma, X., Zhang, N., Zhang, Q., Chen, X., Zhang, Z., et al. (2021). Targeting Oncogenic miR-181a-2-3p Inhibits Growth and Suppresses Cisplatin Resistance of Gastric Cancer. Cancer Management and Research, 13, 8599–8609. https://doi.org/10.2147/cmar.S332713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Qiao, X. L., Zhong, Z. L., Dong, Y., & Gao, F. (2020). LncRNA HMGA1P4 promotes cisplatin-resistance in gastric cancer. European Review for Medical and Pharmacological Sciences, 24(17), 8830–8836. https://doi.org/10.26355/eurrev_202009_22822

    Article  PubMed  Google Scholar 

  151. Xu, Y. D., Shang, J., Li, M., & Zhang, Y. Y. (2019). LncRNA DANCR accelerates the development of multidrug resistance of gastric cancer. European Review for Medical and Pharmacological Sciences, 23(7), 2794–2802. https://doi.org/10.26355/eurrev_201904_17554

    Article  PubMed  Google Scholar 

  152. Zhang, X. W., Bu, P., Liu, L., Zhang, X. Z., & Li, J. (2015). Overexpression of long non-coding RNA PVT1 in gastric cancer cells promotes the development of multidrug resistance. Biochemical and Biophysical Research Communications, 462(3), 227–232. https://doi.org/10.1016/j.bbrc.2015.04.121

    Article  CAS  PubMed  Google Scholar 

  153. Yu, Z., Wang, Y., Deng, J., Liu, D., Zhang, L., Shao, H., et al. (2021). Long non-coding RNA COL4A2-AS1 facilitates cell proliferation and glycolysis of colorectal cancer cells via miR-20b-5p/hypoxia inducible factor 1 alpha subunit axis. Bioengineered, 12(1), 6251–6263. https://doi.org/10.1080/21655979.2021.1969833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Zhang, H., Yao, B., Tang, S., & Chen, Y. (2019). LINK-A Long Non-Coding RNA (lncRNA) Participates in Metastasis of Ovarian Carcinoma and Upregulates Hypoxia-Inducible Factor 1 (HIF1α). Medical Science Monitor, 25, 2221–2227. https://doi.org/10.12659/msm.913609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Liu, D., & Li, H. (2019). Long non-coding RNA GEHT1 promoted the proliferation of ovarian cancer cells via modulating the protein stability of HIF1α. Bioscience Reports, 39(5). https://doi.org/10.1042/bsr20181650

  156. Zhang, T., Wang, F., Liao, Y., Yuan, L., & Zhang, B. (2019). LncRNA AWPPH promotes the invasion and migration of glioma cells through the upregulation of HIF1α. Oncology Letters, 18(6), 6781–6786. https://doi.org/10.3892/ol.2019.11018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Lin, Z., Song, J., Gao, Y., Huang, S., Dou, R., Zhong, P., et al. (2022). Hypoxia-induced HIF-1α/lncRNA-PMAN inhibits ferroptosis by promoting the cytoplasmic translocation of ELAVL1 in peritoneal dissemination from gastric cancer. Redox Biology, 52, 102312. https://doi.org/10.1016/j.redox.2022.102312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Wang, Y., Chen, W., Lian, J., Zhang, H., Yu, B., Zhang, M., et al. (2020). The lncRNA PVT1 regulates nasopharyngeal carcinoma cell proliferation via activating the KAT2A acetyltransferase and stabilizing HIF-1α. Cell Death and Differentiation, 27(2), 695–710. https://doi.org/10.1038/s41418-019-0381-y

    Article  CAS  PubMed  Google Scholar 

  159. Jin, Y., Zhang, Z., Yu, Q., Zeng, Z., Song, H., Huang, X., et al. (2021). Positive Reciprocal Feedback of lncRNA ZEB1-AS1 and HIF-1α Contributes to Hypoxia-Promoted Tumorigenesis and Metastasis of Pancreatic Cancer. Frontiers in Oncology, 11, 761979. https://doi.org/10.3389/fonc.2021.761979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Wu, F., Gao, H., Liu, K., Gao, B., Ren, H., Li, Z., et al. (2019). The lncRNA ZEB2-AS1 is upregulated in gastric cancer and affects cell proliferation and invasion via miR-143-5p/HIF-1α axis. Oncotargets and Therapy, 12, 657–667. https://doi.org/10.2147/ott.S175521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Li, L., Ma, Y., Maerkeya, K., Reyanguly, D., & Han, L. (2021). LncRNA OIP5-AS1 Regulates the Warburg Effect Through miR-124-5p/IDH2/HIF-1α Pathway in Cervical Cancer. Frontiers in Cell and Development Biology, 9, 655018. https://doi.org/10.3389/fcell.2021.655018

    Article  Google Scholar 

  162. Zhang, J., Du, C., Zhang, L., Wang, Y., Zhang, Y., & Li, J. (2022). LncRNA LINC00649 promotes the growth and metastasis of triple-negative breast cancer by maintaining the stability of HIF-1α through the NF90/NF45 complex. Cell Cycle, 21(10), 1034–1047. https://doi.org/10.1080/15384101.2022.2040283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Yang, B., Jia, L., Ren, H., Jin, C., Ren, Q., Zhang, H., et al. (2020). LncRNA DLX6-AS1 increases the expression of HIF-1α and promotes the malignant phenotypes of nasopharyngeal carcinoma cells via targeting MiR-199a-5p. Molecular Genetics & Genomic Medicine, 8(1), e1017. https://doi.org/10.1002/mgg3.1017

    Article  Google Scholar 

  164. Peng, X., Yan, J., & Cheng, F. (2020). LncRNA TMPO-AS1 up-regulates the expression of HIF-1α and promotes the malignant phenotypes of retinoblastoma cells via sponging miR-199a-5p. Pathology, Research and Practice, 216(4), 152853. https://doi.org/10.1016/j.prp.2020.152853

    Article  CAS  PubMed  Google Scholar 

  165. Zeng, Z., Xu, F. Y., Zheng, H., Cheng, P., Chen, Q. Y., Ye, Z., et al. (2019). LncRNA-MTA2TR functions as a promoter in pancreatic cancer via driving deacetylation-dependent accumulation of HIF-1α. Theranostics, 9(18), 5298–5314. https://doi.org/10.7150/thno.34559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Sun, S., Xia, C., & Xu, Y. (2020). HIF-1α induced lncRNA LINC00511 accelerates the colorectal cancer proliferation through positive feedback loop. Biomedicine & Pharmacotherapy, 125, 110014. https://doi.org/10.1016/j.biopha.2020.110014

    Article  CAS  Google Scholar 

  167. Dong, L., Cao, X., Luo, Y., Zhang, G., & Zhang, D. (2020). A Positive Feedback Loop of lncRNA DSCR8/miR-98-5p/STAT3/HIF-1α Plays a Role in the Progression of Ovarian Cancer. Frontiers in Oncology, 10, 1713. https://doi.org/10.3389/fonc.2020.01713

    Article  PubMed  PubMed Central  Google Scholar 

  168. Zhu, Y., Tong, Y., Wu, J., Liu, Y., & Zhao, M. (2019). Knockdown of LncRNA GHET1 suppresses prostate cancer cell proliferation by inhibiting HIF-1α/Notch-1 signaling pathway via KLF2. Biofactors, 45(3), 364–373. https://doi.org/10.1002/biof.1486

    Article  CAS  PubMed  Google Scholar 

  169. Li, X., Deng, S. J., Zhu, S., Jin, Y., Cui, S. P., Chen, J. Y., et al. (2016). Hypoxia-induced lncRNA-NUTF2P3-001 contributes to tumorigenesis of pancreatic cancer by derepressing the miR-3923/KRAS pathway. Oncotarget, 7(5), 6000–6014. https://doi.org/10.18632/oncotarget.6830

    Article  PubMed  PubMed Central  Google Scholar 

  170. Chen, Z., Hu, Z., Sui, Q., Huang, Y., Zhao, M., Li, M., et al. (2022). LncRNA FAM83A-AS1 facilitates tumor proliferation and the migration via the HIF-1α/ glycolysis axis in lung adenocarcinoma. International Journal of Biological Sciences, 18(2), 522–535. https://doi.org/10.7150/ijbs.67556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Zhou, C., Huang, C., Wang, J., Huang, H., Li, J., Xie, Q., et al. (2017). LncRNA MEG3 downregulation mediated by DNMT3b contributes to nickel malignant transformation of human bronchial epithelial cells via modulating PHLPP1 transcription and HIF-1α translation. Oncogene, 36(27), 3878–3889. https://doi.org/10.1038/onc.2017.14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Jiang, P., Hao, S., Xie, L., Xiang, G., Hu, W., Wu, Q., et al. (2021). LncRNA NEAT1 contributes to the acquisition of a tumor like-phenotype induced by PM 2.5 in lung bronchial epithelial cells via HIF-1α activation. Environmental Science and Pollution Research International, 28(32), 43382–43393. https://doi.org/10.1007/s11356-021-13735-7

    Article  CAS  PubMed  Google Scholar 

  173. Wang, C., Han, C., Zhang, Y., & Liu, F. (2018). LncRNA PVT1 regulate expression of HIF1α via functioning as ceRNA for miR-199a-5p in non-small cell lung cancer under hypoxia. Molecular Medicine Reports, 17(1), 1105–1110. https://doi.org/10.3892/mmr.2017.7962

    Article  CAS  PubMed  Google Scholar 

  174. Meng, F., Luo, X., Li, C., & Wang, G. (2022). LncRNA LINC00525 activates HIF-1α through miR-338-3p / UBE2Q1 / β-catenin axis to regulate the Warburg effect in colorectal cancer. Bioengineered, 13(2), 2554–2567. https://doi.org/10.1080/21655979.2021.2018538

    Article  CAS  PubMed  Google Scholar 

  175. Zhang, W., Wang, J., Chai, R., Zhong, G., Zhang, C., Cao, W., et al. (2018). Hypoxia-regulated lncRNA CRPAT4 promotes cell migration via regulating AVL9 in clear cell renal cell carcinomas. Oncotargets and Therapy, 11, 4537–4545. https://doi.org/10.2147/ott.S169155

    Article  PubMed  PubMed Central  Google Scholar 

  176. Piao, H. Y., Liu, Y., Kang, Y., Wang, Y., Meng, X. Y., Yang, D., et al. (2022). Hypoxia associated lncRNA HYPAL promotes proliferation of gastric cancer as ceRNA by sponging miR-431-5p to upregulate CDK14. Gastric Cancer, 25(1), 44–63. https://doi.org/10.1007/s10120-021-01213-5

    Article  CAS  PubMed  Google Scholar 

  177. Zhou, L., Jiang, J., Huang, Z., Jin, P., Peng, L., Luo, M., et al. (2022). Hypoxia-induced lncRNA STEAP3-AS1 activates Wnt/β-catenin signaling to promote colorectal cancer progression by preventing m(6)A-mediated degradation of STEAP3 mRNA. Molecular Cancer, 21(1), 168. https://doi.org/10.1186/s12943-022-01638-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Wang, L., Li, B., Bo, X., Yi, X., Xiao, X., & Zheng, Q. (2022). Hypoxia-induced LncRNA DACT3-AS1 upregulates PKM2 to promote metastasis in hepatocellular carcinoma through the HDAC2/FOXA3 pathway. Experimental & Molecular Medicine, 54(6), 848–860. https://doi.org/10.1038/s12276-022-00767-3

    Article  CAS  Google Scholar 

  179. Jin, Y., Xie, H., Duan, L., Zhao, D., Ding, J., & Jiang, G. (2019). Long Non-Coding RNA CASC9 And HIF-1α Form A Positive Feedback Loop To Facilitate Cell Proliferation And Metastasis In Lung Cancer. Oncotargets and Therapy, 12, 9017–9027. https://doi.org/10.2147/ott.S226078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Ma, H. N., Chen, H. J., Liu, J. Q., & Li, W. T. (2022). Long non-coding RNA DLEU1 promotes malignancy of breast cancer by acting as an indispensable coactivator for HIF-1α-induced transcription of CKAP2. Cell Death & Disease, 13(7), 625. https://doi.org/10.1038/s41419-022-04880-z

    Article  CAS  Google Scholar 

  181. Liu, H., Wan, J., Feng, Q., Li, J., Liu, J., & Cui, S. (2022). Long non-coding RNA SOS1-IT1 promotes endometrial cancer progression by regulating hypoxia signaling pathway. J Cell Commun Signal, 16(2), 253–270. https://doi.org/10.1007/s12079-021-00651-1

    Article  CAS  PubMed  Google Scholar 

  182. Zhang, Y., Ma, H., & Chen, C. (2021). Long non-coding RNA PCED1B-AS1 promotes pancreatic ductal adenocarcinoma progression by regulating the miR-411-3p/HIF-1α axis. Oncology Reports, 46(1). https://doi.org/10.3892/or.2021.8085

  183. Wang, S., You, H., & Yu, S. (2020). Long non-coding RNA HOXA-AS2 promotes the expression levels of hypoxia-inducible factor-1α and programmed death-ligand 1, and regulates nasopharyngeal carcinoma progression via miR-519. Oncology Letters, 20(5), 245. https://doi.org/10.3892/ol.2020.12107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Zhao, R., Sun, F., Bei, X., Wang, X., Zhu, Y., Jiang, C., et al. (2017). Upregulation of the long non-coding RNA FALEC promotes proliferation and migration of prostate cancer cell lines and predicts prognosis of PCa patients. Prostate, 77(10), 1107–1117. https://doi.org/10.1002/pros.23367

    Article  CAS  PubMed  Google Scholar 

  185. Liu, L., Zhao, X., Zou, H., Bai, R., Yang, K., & Tian, Z. (2016). Hypoxia Promotes Gastric Cancer Malignancy Partly through the HIF-1α Dependent Transcriptional Activation of the Long Non-coding RNA GAPLINC. Frontiers in Physiology, 7, 420. https://doi.org/10.3389/fphys.2016.00420

    Article  PubMed  PubMed Central  Google Scholar 

  186. Liu, J., Liu, H., Zeng, Q., Xu, P., Liu, M., & Yang, N. (2020). Circular RNA circ-MAT2B facilitates glycolysis and growth of gastric cancer through regulating the miR-515-5p/HIF-1α axis. Cancer Cell International, 20, 171. https://doi.org/10.1186/s12935-020-01256-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Zhao, J. P., & Chen, L. L. (2020). Circular RNA MAT2B Induces Colorectal Cancer Proliferation via Sponging miR-610, Resulting in an Increased E2F1 Expression. Cancer Management and Research, 12, 7107–7116. https://doi.org/10.2147/cmar.S251180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Wang, H., Feng, L., Cheng, D., Zheng, Y., Xie, Y., & Fu, B. (2021). Circular RNA MAT2B promotes migration, invasion and epithelial-mesenchymal transition of non-small cell lung cancer cells by sponging miR-431. Cell Cycle, 20(16), 1617–1627. https://doi.org/10.1080/15384101.2021.1956106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Liu, A., & Xu, J. (2021). Circ_03955 promotes pancreatic cancer tumorigenesis and Warburg effect by targeting the miR-3662/HIF-1α axis. Clinical & Translational Oncology, 23(9), 1905–1914. https://doi.org/10.1007/s12094-021-02599-5

    Article  CAS  Google Scholar 

  190. Liu, Z., Zhou, Y., Liang, G., Ling, Y., Tan, W., Tan, L., et al. (2019). Circular RNA hsa_circ_001783 regulates breast cancer progression via sponging miR-200c-3p. Cell Death & Disease, 10(2), 55. https://doi.org/10.1038/s41419-018-1287-1

    Article  CAS  Google Scholar 

  191. Dong, L., Zhang, L., Liu, H., Xie, M., Gao, J., Zhou, X., et al. (2020). Circ_0007331 knock-down suppresses the progression of endometriosis via miR-200c-3p/HiF-1α axis. Journal of Cellular and Molecular Medicine, 24(21), 12656–12666. https://doi.org/10.1111/jcmm.15833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Jiang, Y., Ji, X., Liu, K., Shi, Y., Wang, C., Li, Y., et al. (2020). Exosomal miR-200c-3p negatively regulates the migraion and invasion of lipopolysaccharide (LPS)-stimulated colorectal cancer (CRC). BMC Mol Cell Biol, 21(1), 48. https://doi.org/10.1186/s12860-020-00291-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Anastasiadou, E., Messina, E., Sanavia, T., Mundo, L., Farinella, F., Lazzi, S., et al. (2021). MiR-200c-3p Contrasts PD-L1 Induction by Combinatorial Therapies and Slows Proliferation of Epithelial Ovarian Cancer through Downregulation of β-Catenin and c-Myc. Cells, 10(3). https://doi.org/10.3390/cells10030519

  194. Cao, L., Wang, M., Dong, Y., Xu, B., Chen, J., Ding, Y., et al. (2020). Circular RNA circRNF20 promotes breast cancer tumorigenesis and Warburg effect through miR-487a/HIF-1α/HK2. Cell Death & Disease, 11(2), 145. https://doi.org/10.1038/s41419-020-2336-0

    Article  CAS  Google Scholar 

  195. Zhai, Z., Fu, Q., Liu, C., Zhang, X., Jia, P., Xia, P., et al. (2019). Emerging Roles Of hsa-circ-0046600 Targeting The miR-640/HIF-1α Signalling Pathway In The Progression Of HCC. Oncotargets and Therapy, 12, 9291–9302. https://doi.org/10.2147/ott.S229514

    Article  PubMed  PubMed Central  Google Scholar 

  196. Liu, J., Liu, Y., Zhang, Y., Zheng, J., Wang, S., & Cao, G. (2022). Circular RNA hsa_circ_0004543 Aggravates Cervical Cancer Development by Sponging MicroRNA hsa-miR-217 to Upregulate Hypoxia-Inducible Factor. Journal of Oncology, 2022, 4031403. https://doi.org/10.1155/2022/4031403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Chi, Y., Luo, Q., Song, Y., Yang, F., Wang, Y., Jin, M., et al. (2019). Circular RNA circPIP5K1A promotes non-small cell lung cancer proliferation and metastasis through miR-600/HIF-1α regulation. Journal of Cellular Biochemistry, 120(11), 19019–19030. https://doi.org/10.1002/jcb.29225

    Article  CAS  PubMed  Google Scholar 

  198. Qian, W., Huang, T., & Feng, W. (2020). Circular RNA HIPK3 Promotes EMT of Cervical Cancer Through Sponging miR-338-3p to Up-Regulate HIF-1α. Cancer Management and Research, 12, 177–187. https://doi.org/10.2147/cmar.s232235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Chen, L.-Y., Wang, L., Ren, Y.-X., Pang, Z., Liu, Y., Sun, X.-D., et al. (2020). The circular RNA circ-ERBIN promotes growth and metastasis of colorectal cancer by miR-125a-5p and miR-138-5p/4EBP-1 mediated cap-independent HIF-1α translation. Molecular Cancer, 19(1), 164. https://doi.org/10.1186/s12943-020-01272-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Xu, G., Li, M., Wu, J., Qin, C., Tao, Y., & He, H. (2020). Circular RNA circNRIP1 Sponges microRNA-138-5p to Maintain Hypoxia-Induced Resistance to 5-Fluorouracil Through HIF-1α-Dependent Glucose Metabolism in Gastric Carcinoma. Cancer Management and Research, 12, 2789–2802. https://doi.org/10.2147/cmar.s246272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Zeng, Z., Zhao, Y., Chen, Q., Zhu, S., Niu, Y., Ye, Z., et al. (2021). Hypoxic exosomal HIF-1α-stabilizing circZNF91 promotes chemoresistance of normoxic pancreatic cancer cells via enhancing glycolysis. Oncogene, 40(36), 5505–5517. https://doi.org/10.1038/s41388-021-01960-w

    Article  CAS  PubMed  Google Scholar 

  202. Joo, H. Y., Yun, M., Jeong, J., Park, E. R., Shin, H. J., Woo, S. R., et al. (2015). SIRT1 deacetylates and stabilizes hypoxia-inducible factor-1α (HIF-1α) via direct interactions during hypoxia. Biochemical and Biophysical Research Communications, 462(4), 294–300. https://doi.org/10.1016/j.bbrc.2015.04.119

    Article  CAS  PubMed  Google Scholar 

  203. Shangguan, H., Feng, H., Lv, D., Wang, J., Tian, T., & Wang, X. (2020). Circular RNA circSLC25A16 contributes to the glycolysis of non-small-cell lung cancer through epigenetic modification. Cell Death & Disease, 11(6), 437. https://doi.org/10.1038/s41419-020-2635-5

    Article  CAS  Google Scholar 

  204. Zhou, P., Xie, W., Huang, H. L., Huang, R. Q., Tian, C., Zhu, H. B., et al. (2020). circRNA_100859 functions as an oncogene in colon cancer by sponging the miR-217-HIF-1α pathway. Aging, 12(13), 13338–13353. https://doi.org/10.18632/aging.103438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  205. Feng, J., Yang, M., Wei, Q., Song, F., Zhang, Y., Wang, X., et al. (2020). Novel evidence for oncogenic piRNA-823 as a promising prognostic biomarker and a potential therapeutic target in colorectal cancer. Journal of Cellular and Molecular Medicine, 24(16), 9028–9040. https://doi.org/10.1111/jcmm.15537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Tao, E.-W., Wang, H.-L., Cheng, W. Y., Liu, Q.-Q., Chen, Y.-X., & Gao, Q.-Y. (2021). A specific tRNA half, 5’tiRNA-His-GTG, responds to hypoxia via the HIF1α/ANG axis and promotes colorectal cancer progression by regulating LATS2. Journal of Experimental & Clinical Cancer Research, 40(1), 67. https://doi.org/10.1186/s13046-021-01836-7

    Article  CAS  Google Scholar 

  207. Hong, D. S., Kang, Y.-K., Borad, M., Sachdev, J., Ejadi, S., Lim, H. Y., et al. (2020). Phase 1 study of MRX34, a liposomal miR-34a mimic, in patients with advanced solid tumours. British Journal of Cancer, 122(11), 1630–1637. https://doi.org/10.1038/s41416-020-0802-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Anastasiadou, E., Seto, A. G., Beatty, X., Hermreck, M., Gilles, M.-E., Stroopinsky, D., et al. (2021). Cobomarsen, an Oligonucleotide Inhibitor of miR-155, Slows DLBCL Tumor Cell Growth In Vitro and In Vivo. Clinical Cancer Research, 27(4), 1139–1149. https://doi.org/10.1158/1078-0432.ccr-20-3139

    Article  CAS  PubMed  Google Scholar 

  209. Reid, G., Pel, M. E., Kirschner, M. B., Cheng, Y. Y., Mugridge, N., Weiss, J., et al. (2013). Restoring expression of miR-16: a novel approach to therapy for malignant pleural mesothelioma. Annals of Oncology, 24(12), 3128–3135. https://doi.org/10.1093/annonc/mdt412

    Article  CAS  PubMed  Google Scholar 

  210. Ronnen, E. A., Kondagunta, G. V., Ishill, N., Sweeney, S. M., Deluca, J. K., Schwartz, L., et al. (2006). A phase II trial of 17-(Allylamino)-17-demethoxygeldanamycin in patients with papillary and clear cell renal cell carcinoma. Investigational New Drugs, 24(6), 543–546. https://doi.org/10.1007/s10637-006-9208-z

    Article  CAS  PubMed  Google Scholar 

  211. Yong, L., Tang, S., Yu, H., Zhang, H., Zhang, Y., Wan, Y., et al. (2022). The role of hypoxia-inducible factor-1 alpha in multidrug-resistant breast cancer. Frontiers in Oncology, 12, 964934. https://doi.org/10.3389/fonc.2022.964934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

K.S.R. thank the Council of Scientific & Industrial Research (New Delhi, India) and the Indian Science Congress Association (Kolkata, India) for providing the emeritus scientist and Asutosh Mookerjee fellowship, respectively.

Author information

Author notes

  1. Chakrabhavi Dhananjaya Mohan

    Present address: FEST Division, CSIR-Indian Institute of Toxicology Research, Vishvigyan Bhawan, 31, Mahatma Gandhi Marg, Lucknow, Uttar Pradesh, 226 001, India

Authors and Affiliations

  1. Department of Pharmacy, Al-Mustaqbal University College, Hilla, Babylon, 51001, Iraq

    Sabrean Farhan Jawad

  2. National Institute of Laser Enhanced Sciences, University of Cairo, Giza, 12613, Egypt

    Farag M. A. Altalbawy

  3. Department of Chemistry, University College of Duba, University of Tabuk, Tabuk, Saudi Arabia

    Farag M. A. Altalbawy

  4. College of Pharmacy, Ahl Al Bayt University, Kerbala, Iraq

    Radhwan M. Hussein

  5. College of Medical Technology, Medical Lab Techniques, Al-Farahidi University, Baghdad, Iraq

    Ali Abdulhussain Fadhil

  6. Department of Medical Laboratories Technology, Al-Nisour University College, Baghdad, Iraq

    Mohammed Abed Jawad

  7. Medical Laboratory Technology Department, College of Medical Technology, The Islamic University, Najaf, Iraq

    Rahman S. Zabibah

  8. Department of Dentistry, AlNoor University College, Nineveh, Iraq

    Tasneem Younus Taraki

  9. Department of Studies in Molecular Biology, University of Mysore, Manasagangotri, Mysore, 570006, India

    Chakrabhavi Dhananjaya Mohan

  10. Institution of Excellence, Vijnana Bhavan, University of Mysore, Manasagangotri, Mysore, 570006, India

    Kanchugarakoppal S. Rangappa

Authors
  1. Sabrean Farhan Jawad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farag M. A. Altalbawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Radhwan M. Hussein
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ali Abdulhussain Fadhil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammed Abed Jawad
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rahman S. Zabibah
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tasneem Younus Taraki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chakrabhavi Dhananjaya Mohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kanchugarakoppal S. Rangappa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chakrabhavi Dhananjaya Mohan or Kanchugarakoppal S. Rangappa.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jawad, S.F., Altalbawy, F.M.A., Hussein, R.M. et al. The strict regulation of HIF-1α by non-coding RNAs: new insight towards proliferation, metastasis, and therapeutic resistance strategies. Cancer Metastasis Rev 43, 5–27 (2024). https://doi.org/10.1007/s10555-023-10129-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10555-023-10129-8

Keywords

Search

Navigation