Unboxing the network among long non-coding RNAs and TGF-β signaling in cancer

Keywords: Cancer, epigenetics, non-coding RNA, signal transduction, transforming growth factor-β

Abstract

Deeper analysis of molecular mechanisms arising in tumor cells is an unmet need to provide new diagnostic and therapeutic strategies to prevent and treat tumors. The transforming growth factor β (TGF-β) signaling has been steadily featured in tumor biology and linked to poor prognosis of cancer patients. One pro-tumorigenic mechanism induced by TGF-β is the epithelial-to-mesenchymal transition (EMT), which can initiate cancer dissemination, enrich the tumor stem cell population, and increase chemoresistance. TGF-β signals via SMAD proteins, ubiquitin ligases, and protein kinases and modulates the expression of protein-coding and non-coding RNA genes, including those encoding larger than 500 nt transcripts, defined as long non-coding RNAs (lncRNAs). Several reports have shown lncRNAs regulating malignant phenotypes by directly affecting epigenetic processes, transcription, and post-transcriptional regulation. Thus, this review aims to update and summarize the impact of TGF-β signaling on the expression of lncRNAs and the function of such lncRNAs as regulators of TGF-β signaling, and how these networks might impact specific hallmarks of cancer.

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References

1. Li P, Elowitz MB. Communication codes in developmental signaling pathways. Development. 2019;146(12):dev170977. doi: 10.1242/dev.170977

2. Massagué J, Sheppard D. TGF-b signaling in health and disease. Cell. 2023;186(19):4007–37. doi: 10.1016/j.cell.2023.07.036

3. Morikawa M, Koinuma D, Miyazono K, Heldin C-H. Genome-wide mechanisms of Smad binding. Oncogene. 2013;32(13):1609–15. doi: 10.1038/onc.2012.191

4. Papoutsoglou P, Moustakas A. Long non-coding RNAs and TGF-b signaling in cancer. Cancer Sci. 2020;111(8):2672–81. doi: 10.1111/cas.14509

5. Morikawa M, Derynck R, Miyazono K. TGF-b and the TGF-b family: context-dependent roles in cell and tissue physiology. Cold Spring Harb Perspect Biol. 2016;8(5):a021873. doi: 10.1101/cshperspect.a021873

6. Tsubakihara Y, Moustakas A. Epithelial-mesenchymal transition and metastasis under the control of transforming growth factor b. Int J Mol Sci. 2018;19(11):3672. doi: 10.3390/ijms19113672

7. Bellomo C, Caja L, Moustakas A. Transforming growth factor b as regulator of cancer stemness and metastasis. Br J Cancer. 2016;115(7):761–9. doi: 10.1038/bjc.2016.255

8. Mattick JS, Amaral PP, Carninci P, Carpenter S, Chang HY, Chen LL, et al. Long non-coding RNAs: definitions, functions, challenges and recommendations. Nat Rev Mol Cell Biol. 2023;24(6):430–47. doi: 10.1038/s41580-022-00566-8

9. Frankish A, Diekhans M, Jungreis I, Lagarde J, Loveland JE, Mudge JM, et al. Gencode 2021. Nucleic Acids Res. 2021;49(D1):D916–23. doi: 10.1093/nar/gkaa1087

10. Huang JZ, Chen M, Chen D, Gao XC, Zhu S, Huang H, et al. A peptide encoded by a putative lncRNA HOXB-AS3 suppresses colon cancer growth. Mol Cell. 2017;68(1):171–84.e6. doi: 10.1016/j.molcel.2017.09.015

11. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. doi: 10.3322/caac.21708

12. Sideris N, Dama P, Bayraktar S, Stiff T, Castellano L. LncRNAs in breast cancer: a link to future approaches. Cancer Gene Ther. 2022;29(12):1866–77. doi: 10.1038/s41417-022-00487-w

13. Yuan JH, Yang F, Wang F, Ma JZ, Guo YJ, Tao QF, et al. A long noncoding RNA activated by TGF-b promotes the invasion-metastasis cascade in hepatocellular carcinoma. Cancer Cell. 2014;25(5):666–81. doi: 10.1016/j.ccr.2014.03.010

14. Xiao H, Zhang F, Zou Y, Li J, Liu Y, Huang W. The function and mechanism of long non-coding RNA-ATB in cancers. Front Physiol. 2018;9:321. doi: 10.3389/fphys.2018.00321

15. El-Ashmawy NE, Hussien FZ, El-Feky OA, Hamouda SM, Al-Ashmawy GM. Serum LncRNA-ATB and FAM83H-AS1 as diagnostic/prognostic non-invasive biomarkers for breast cancer. Life Sci. 2020;259:118193. doi: 10.1016/j.lfs.2020.118193

16. Chen HY, Chan SJ, Liu X, Wei AC, Jian RI, Huang KW, et al. Long noncoding RNA Smyca coactivates TGF-b/Smad and Myc pathways to drive tumor progression. J Hematol Oncol. 2022;15(1):85. doi: 10.1186/s13045-022-01306-3

17. Ni K, Huang Z, Zhu Y, Xue D, Jin Q, Zhang C, et al. The lncRNA ADAMTS9-AS2 regulates RPL22 to modulate TNBC progression via controlling the TGF-b signaling pathway. Front Oncol. 2021;11:654472. doi: 10.3389/fonc.2021.654472

18. Zheng BH, He ZX, Zhang J, Ma JJ, Zhang HW, Zhu W, et al. The biological function of TUSC7/miR-1224-3p axis in triple-negative breast cancer. Cancer Manag Res. 2021;13:5763–74. doi: 10.2147/CMAR.S305865

19. Zhang Y, O’Leary MN, Peri S, Wang M, Zha J, Melov S, et al. Ribosomal proteins Rpl22 and Rpl22l1 control morphogenesis by regulating pre-mRNA splicing. Cell Rep. 2017;18(2):545–56. doi: 10.1016/j.celrep.2016.12.034

20. Mitobe Y, Ikeda K, Sato W, Kodama Y, Naito M, Gotoh N, et al. Proliferation-associated long noncoding RNA, TMPO-AS1, is a potential therapeutic target for triple-negative breast cancer. Cancer Sci. 2020;111(7):2440–50. doi: 10.1111/cas.14498

21. Wo L, Zhang B, You X, Hu Y, Gu Z, Zhang M, et al. Up-regulation of LncRNA UCA1 by TGF-b promotes doxorubicin resistance in breast cancer cells. Immunopharmacol Immunotoxicol. 2022;44(4):492–9. doi: 10.1080/08923973.2022.2054428

22. Fan C, Gonzalez-Prieto R, Kuipers TB, Vertegaal ACO, van Veelen PA, Mei H, et al. The lncRNA LETS1 promotes TGF-b-induced EMT and cancer cell migration by transcriptionally activating a TbR1-stabilizing mechanism. Sci Signal. 2023;16(790):eadf1947. doi: 10.1126/scisignal.adf1947

23. Zhou F, Drabsch Y, Dekker TJ, de Vinuesa AG, Li Y, Hawinkels LJ, et al. Nuclear receptor NR4A1 promotes breast cancer invasion and metastasis by activating TGF-b signalling. Nat Commun. 2014;5:3388. doi: 10.1038/ncomms4388

24. Guo B, Wu S, Zhu X, Zhang L, Deng J, Li F, et al. Micropeptide CIP2A-BP encoded by LINC00665 inhibits triple-negative breast cancer progression. EMBO J. 2020;39(1):e102190. doi: 10.15252/embj.2019102190

25. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394–424. doi: 10.3322/caac.21492

26. Chen M, Lei N, Tian W, Li Y, Chang L. Recent advances of non-coding RNAs in ovarian cancer prognosis and therapeutics. Ther Adv Med Oncol. 2022;14:17588359221118010. doi: 10.1177/17588359221118010

27. Lin H, Xu X, Chen K, Fu Z, Wang S, Chen Y, et al. LncRNA CASC15, MiR-23b cluster and SMAD3 form a novel positive feedback loop to promote epithelial-mesenchymal transition and metastasis in ovarian cancer. Int J Biol Sci. 2022;18(5):1989–2002. doi: 10.7150/ijbs.67486

28. Tan X, Shao Y, Teng Y, Liu S, Li W, Xue L, et al. The cancer-testis long non-coding RNA PCAT6 facilitates the malignant phenotype of ovarian cancer by sponging miR-143-3p. Front Cell Dev Biol. 2021;9:593677. doi: 10.3389/fcell.2021.593677

29. Huang FT, Peng JF, Cheng WJ, Zhuang YY, Wang LY, Li CQ, et al. MiR-143 Targeting TAK1 attenuates pancreatic ductal adenocarcinoma progression via MAPK and NF-kB pathway in vitro. Dig Dis Sci 2017; 62(4): 944–57. doi: 10.1007/s10620-017-4472-7

30. Wu Y, Gu W, Han X, Jin Z. LncRNA PVT1 promotes the progression of ovarian cancer by activating TGF-b pathway via miR-148a-3p/AGO1 axis. J Cell Mol Med. 2021;25(17):8229–43. doi: 10.1111/jcmm.16700

31. Li Y, Zhao Z, Sun D, Li Y. Novel long noncoding RNA LINC02323 promotes cell growth and migration of ovarian cancer via TGF-b receptor 1 by miR-1343-3p. J Clin Lab Anal. 2021;35(2):e23651. doi: 10.1002/jcla.23651

32. Zhang X, Du L, Han J, Li X, Wang H, Zheng G, et al. Novel long non-coding RNA LINC02323 promotes epithelial-mesenchymal transition and metastasis via sponging miR-1343-3p in lung adenocarcinoma. Thorac Cancer. 2020;11(9):2506–16. doi: 10.1111/1759-7714.13562

33. Rodrigues-Junior DM, Tsirigoti C, Lim SK, Heldin C-H, Moustakas A. Extracellular vesicles and transforming growth factor b signaling in cancer. Front Cell Dev Biol. 2022;10:849938. doi: 10.3389/fcell.2022.849938

34. Yuan D, Guo T, Zhu D, Ge H, Zhao Y, Huang A, et al. Exosomal lncRNA ATB derived from ovarian cancer cells promotes angiogenesis via regulating miR-204-3p/TGFbR2 axis. Cancer Manag Res. 2022;14:327–37. doi: 10.2147/CMAR.S330368

35. Shetty A, Venkatesh T, Kabbekodu SP, Tsutsumi R, Suresh PS. LncRNA-miRNA-mRNA regulatory axes in endometrial cancer: a comprehensive overview. Arch Gynecol Obstet. 2022;306(5):1431–47. doi: 10.1007/s00404-022-06423-5

36. Ma J, Kong FF, Yang D, Yang H, Wang C, Cong R, et al. lncRNA MIR210HG promotes the progression of endometrial cancer by sponging miR-337-3p/137 via the HMGA2-TGF-b/Wnt pathway. Mol Ther Nucleic Acids. 2021;24:905–22. doi: 10.1016/j.omtn.2021.04.011

37. Iyer NG, Tan DS, Tan VK, Wang W, Hwang J, Tan NC, et al. Randomized trial comparing surgery and adjuvant radiotherapy versus concurrent chemoradiotherapy in patients with advanced, nonmetastatic squamous cell carcinoma of the head and neck: 10-year update and subset analysis. Cancer. 2015;121(10):1599–607. doi: 10.1002/cncr.29251

38. Wang Y, Wang S, Ren Y, Zhou X. The role of lncRNA crosstalk in leading cancer metastasis of head and neck squamous cell carcinoma. Front Oncol. 2020;10:561833. doi: 10.3389/fonc.2020.561833

39. Wu J, Chen Z, Zhang L, Cao J, Li X, Gong Z, et al. Knockdown of LINC01116 inhibits cell migration and invasion in head and neck squamous cell carcinoma through epithelial-mesenchymal transition pathway. J Cell Biochem. 2020;121(1):867–75. doi: 10.1002/jcb.29331

40. Shen H, Sun B, Yang Y, Cai X, Bi L, Deng L, et al. MIR4435-2HG regulates cancer cell behaviors in oral squamous cell carcinoma cell growth by upregulating TGF-b1. Odontology. 2020;108(4):553–9. doi: 10.1007/s10266-020-00488-x

41. Zhou B, Zhou Y, Liu Y, Zhang H, Mao H, Peng M, et al. Association of CASC18/miR-20a-3p/TGFB2 ceRNA axis with occult lymph node metastasis in tongue squamous cell carcinoma. Mol Med. 2021;27(1):85. doi: 10.1186/s10020-021-00345-9

42. Li Y, Tang B, Lyu K, Yue H, Wei F, Xu Y, et al. Low expression of lncRNA SBF2-AS1 regulates the miR-302b-3p/TGFBR2 axis, promoting metastasis in laryngeal cancer. Mol Carcinog. 2022;61(1):45–58. doi: 10.1002/mc.23358

43. Pang X, Tang YL, Liang XH. Transforming growth factor-b signaling in head and neck squamous cell carcinoma: insights into cellular responses. Oncol Lett. 2018;16(4):4799–806. doi: 10.3892/ol.2018.9319

44. Yang J, Feng E, Ren Y, Qiu S, Zhao L, Li X. Long non-coding (lnc)RNA profiling and the role of a key regulator lnc-PNRC2-1 in the transforming growth factor-b1-induced epithelial-mesenchymal transition of CNE1 nasopharyngeal carcinoma cells. J Int Med Res. 2021;49(3):300060521996515. doi: 10.1177/0300060521996515

45. Du M, Hu X, Jiang X, Yin L, Chen J, Wen J, et al. LncRNA EPB41L4A-AS2 represses nasopharyngeal carcinoma metastasis by binding to YBX1 in the nucleus and sponging MiR-107 in the cytoplasm. Int J Biol Sci. 2021;17(8):1963–78. doi: 10.7150/ijbs.55557

46. Papoutsoglou P, Rodrigues-Junior DM, Morén A, Bergman A, Pontén F, Coulouarn C, et al. The noncoding MIR100HG RNA enhances the autocrine function of transforming growth factor b signaling. Oncogene. 2021;40(21):3748–65. doi: 10.1038/s41388-021-01803-8

47. Zhu L, Liu Y, Tang H, Wang P. FOXP3 activated-LINC01232 accelerates the stemness of non-small cell lung carcinoma by activating TGF-b signaling pathway and recruiting IGF2BP2 to stabilize TGFBR1. Exp Cell Res. 2022;413(2):113024. doi: 10.1016/j.yexcr.2022.113024

48. Li C, Li Z, Yi H, Liu Z. IncRNA Linc00511 upregulation elevates TGFBR1 and participates in the postoperative distant recurrence of non-small-cell lung cancer by targeting miR-98-5p. Crit Rev Eukaryot Gene Expr. 2022;32(5):1–10. doi: 10.1615/CritRevEukaryotGeneExpr.2022039498

49. Shi J, Li J, Yang S, Hu X, Chen J, Feng J, et al. LncRNA SNHG3 is activated by E2F1 and promotes proliferation and migration of non-small-cell lung cancer cells through activating TGF-b pathway and IL-6/JAK2/STAT3 pathway. J Cell Physiol. 2020;235(3):2891–900. doi: 10.1002/jcp.29194

50. Yang M, He X, Huang X, Wang J, He Y, Wei L. LncRNA MIR4435-2HG-mediated upregulation of TGF-b1 promotes migration and proliferation of nonsmall cell lung cancer cells. Environ Toxicol. 2020;35(5):582–90. doi: 10.1002/tox.22893

51. Kawasaki N, Miwa T, Hokari S, Sakurai T, Ohmori K, Miyauchi K, et al. Long noncoding RNA NORAD regulates transforming growth factor-b signaling and epithelial-to-mesenchymal transition-like phenotype. Cancer Sci. 2018;109(7):2211–20. doi: 10.1111/cas.13626

52. Yao J, Lu X, Wang Y, Li J, Ni B. Long noncoding RNAs AC026904.1 is essential for TGF-b-induced migration and epithelial-mesenchymal transition through functioning as an enhancer of slug in lung cancer cells. Environ Toxicol. 2020;35(9):942–51. doi: 10.1002/tox.22930

53. Sarkar A, Rahaman A, Biswas I, Mukherjee G, Chatterjee S, Bhattacharjee S, et al. TGFb mediated LINC00273 upregulation sponges mir200a-3p and promotes invasion and metastasis by activating ZEB1. J Cell Physiol. 2020;235(10):7159–72. doi: 10.1002/jcp.29614

54. Wu D, Deng S, Li L, Liu T, Zhang T, Li J, et al. TGF-b1-mediated exosomal lnc-MMP2-2 increases blood-brain barrier permeability via the miRNA-1207-5p/EPB41L5 axis to promote non-small cell lung cancer brain metastasis. Cell Death Dis. 2021;12(8):721. doi: 10.1038/s41419-021-04004-z

55. Xu L, Liu W, Li T, Hu Y, Wang Y, Huang L, et al. Long non-coding RNA SMASR inhibits the EMT by negatively regulating TGF-b/Smad signaling pathway in lung cancer. Oncogene. 2021;40(20):3578–92. doi: 10.1038/s41388-021-01760-2

56. Fan C, Wang Q, Kuipers TB, Cats D, Iyengar PV, Hagenaars SC, et al. LncRNA LITATS1 suppresses TGF-b-induced EMT and cancer cell plasticity by potentiating TbRI degradation. EMBO J. 2023;42(10):e112806. doi: 10.15252/embj.2022112806

57. Papoutsoglou P, Tsubakihara Y, Caja L, Morén A, Pallis P, Ameur A, et al. The TGFB2-AS1 lncRNA regulates TGF-b signaling by modulating corepressor activity. Cell Rep. 2019;28(12):3182–98.e11. doi: 10.1016/j.celrep.2019.08.028

58. Zhou C, Wang D, Li J, Wang Q, Wo L, Zhang X, et al. TGFB2-AS1 inhibits triple-negative breast cancer progression via interaction with SMARCA4 and regulating its targets TGFB2 and SOX2. Proc Natl Acad Sci U S A. 2022;119(39):e2117988119. doi: 10.1073/pnas.2117988119

59. Gong R, Jiang Y. Non-coding RNAs in pancreatic ductal adenocarcinoma. Front Oncol. 2020;10:309. doi: 10.3389/fonc.2020.00309

60. Ko CC, Hsieh YY, Yang PM. Long on-coding RNA MIR31HG promotes the transforming growth factor b-induced epithelial-mesenchymal transition in pancreatic ductal adenocarcinoma cells. Int J Mol Sci. 2022;23(12):6559. doi: 10.3390/ijms23126559

61. Sun J, Zhang Y. LncRNA XIST enhanced TGF-b2 expression by targeting miR-141-3p to promote pancreatic cancer cells invasion. Biosci Rep. 2019;39(7):BSR20190332. doi: 10.1042/BSR20190332

62. Takahashi K, Ota Y, Kogure T, Suzuki Y, Iwamoto H, Yamakita K, et al. Circulating extracellular vesicle-encapsulated HULC is a potential biomarker for human pancreatic cancer. Cancer Sci. 2020;111(1):98–111. doi: 10.1111/cas.14232

63. Dorn A, Glass M, Neu CT, Heydel B, Huttelmaier S, Gutschner T, et al. LINC00261 is differentially expressed in pancreatic cancer subtypes and regulates a pro-epithelial cell identity. Cancers (Basel). 2020;12(5):1227. doi: 10.3390/cancers12051227

64. Tang Y, Shu G, Yuan X, Jing N, Song J. FOXA2 functions as a suppressor of tumor metastasis by inhibition of epithelial-to-mesenchymal transition in human lung cancers. Cell Res. 2011;21(2):316–26. doi: 10.1038/cr.2010.126

65. Huang Z, Zhou JK, Peng Y, He W, Huang C. The role of long noncoding RNAs in hepatocellular carcinoma. Mol Cancer. 2020;19(1):77. doi: 10.1186/s12943-020-01188-4

66. Han M, Liao Z, Liu F, Chen X, Zhang B. Modulation of the TGF-b signaling pathway by long noncoding RNA in hepatocellular carcinoma. Biomark Res. 2020;8(1):70. doi: 10.1186/s40364-020-00252-x

67. Wang Y, Yang L, Dong X, Yang X, Zhang X, Liu Z, et al. Overexpression of NNT-AS1 activates TGF-b signaling to decrease tumor CD4 lymphocyte infiltration in hepatocellular carcinoma. Biomed Res Int. 2020;2020:8216541. doi: 10.1155/2020/8216541

68. Lou J, Yan W, Li QY, Zhu AK, Tan BQ, Dong R, et al. LncRNA MEG8 plays an oncogenic role in hepatocellular carcinoma progression through miR-367-3p/14-3-3z/TGFbR1 axis. Neoplasma. 2021;68(2):273–82. doi: 10.4149/neo_2020_200730N785

69. Lu J, Guo H, Treekitkarnmongkol W, Li P, Zhang J, Shi B, et al. 14-3-3z Cooperates with ErbB2 to promote ductal carcinoma in situ progression to invasive breast cancer by inducing epithelial-mesenchymal transition. Cancer Cell. 2009;16(3):195–207. doi: 10.1016/j.ccr.2009.08.010

70. Wu YH, Yu B, Chen WX, Ai X, Zhang W, Dong W, et al. Downregulation of lncRNA SBF2-AS1 inhibits hepatocellular carcinoma proliferation and migration by regulating the miR-361-5p/TGF-b1 signaling pathway. Aging (Albany NY). 2021;13(15):19260–71. doi: 10.18632/aging.203248

71. Chen Z, Xiang L, Li L, Ou H, Fang Y, Xu Y, et al. TGF-b1 induced deficiency of linc00261 promotes epithelial-mesenchymal-transition and stemness of hepatocellular carcinoma via modulating SMAD3. J Transl Med. 2022;20(1):75. doi: 10.1186/s12967-022-03276-z

72. Ghafouri-Fard S, Hussen BM, Gharebaghi A, Eghtedarian R, Taheri M. LncRNA signature in colorectal cancer. Pathol Res Pract. 2021;222:153432. doi: 10.1016/j.prp.2021.153432

73. Gao Z, Zhou H, Wang Y, Chen J, Ou Y. Regulatory effects of lncRNA ATB targeting miR-200c on proliferation and apoptosis of colorectal cancer cells. J Cell Biochem. 2020;121(1):332–43. doi: 10.1002/jcb.29180

74. Liu X, Wang C. Long non-coding RNA ATB is associated with metastases and promotes cell invasion in colorectal cancer via sponging miR-141-3p. Exp Ther Med. 2020;20(6):261. doi: 10.3892/etm.2020.9391

75. Yang X, Tao H, Wang C, Chen W, Hua F, Qian H. lncRNA-ATB promotes stemness maintenance in colorectal cancer by regulating transcriptional activity of the b-catenin pathway. Exp Ther Med. 2020;19(4):3097–103. doi: 10.3892/etm.2020.8558

76. Shen X, Hu X, Mao J, Wu Y, Liu H, Shen J, et al. The long noncoding RNA TUG1 is required for TGF-b/TWIST1/EMT-mediated metastasis in colorectal cancer cells. Cell Death Dis. 2020;11(1):65. doi: 10.1038/s41419-020-2254-1

77. Javanmard AR, Dokanehiifard S, Bohlooli M, Soltani BM. LOC646329 long non-coding RNA sponges miR-29b-1 and regulates TGFb signaling in colorectal cancer. J Cancer Res Clin Oncol. 2020;146(5):1205–15. doi: 10.1007/s00432-020-03145-6

78. Li Q, Yue W, Li M, Jiang Z, Hou Z, Liu W, et al. Downregulating long non-coding RNAs CTBP1-AS2 inhibits colorectal cancer development by modulating the miR-93-5p/TGF-b/SMAD2/3 pathway. Front Oncol. 2021;11:626620. doi: 10.3389/fonc.2021.626620

79. Wu N, Jiang M, Liu H, Chu Y, Wang D, Cao J, et al. LINC00941 promotes CRC metastasis through preventing SMAD4 protein degradation and activating the TGF-b/SMAD2/3 signaling pathway. Cell Death Differ. 2021;28(1):219–32. doi: 10.1038/s41418-020-0596-y

80. Huang Y, Luo Y, Ou W, Wang Y, Dong D, Peng X, et al. Exosomal lncRNA SNHG10 derived from colorectal cancer cells suppresses natural killer cell cytotoxicity by upregulating INHBC. Cancer Cell Int. 2021;21(1):528. doi: 10.1186/s12935-021-02221-2

81. Li Y, Li G, Guo X, Yao H, Wang G, Li C. Non-coding RNA in bladder cancer. Cancer Lett. 2020;485:38–44. doi: 10.1016/j.canlet.2020.04.023

82. Zhang Z, Ao P, Han H, Zhang Q, Chen Y, Han J, et al. LncRNA PLAC2 upregulates miR-663 to downregulate TGF-b1 and suppress bladder cancer cell migration and invasion. BMC Urol. 2020;20(1):94. doi: 10.1186/s12894-020-00663-w

83. Zhuang C, Liu Y, Fu S, Yuan C, Luo J, Huang X, et al. Silencing of lncRNA MIR497HG via CRISPR/Cas13d induces bladder cancer progression through promoting the crosstalk between Hippo/Yap and TGF-b/Smad signaling. Front Mol Biosci. 2020;7:616768. doi: 10.3389/fmolb.2020.616768

84. Huang CS, Tsai CH, Yu CP, Wu YS, Yee MF, Ho JY, et al. Long noncoding RNA LINC02470 sponges MicroRNA-143-3p and enhances SMAD3-mediated epithelial-to-mesenchymal transition to promote the aggressive properties of bladder cancer. Cancers (Basel). 2022;14(4):968. doi: 10.3390/cancers14040968

85. Zhang Z, Chen F, Zhan H, Chen L, Deng Q, Xiong T, et al. lncRNA CASC9 sponges miR7583p to promote proliferation and EMT in bladder cancer by upregulating TGFb2. Oncol Rep. 2021;45(1):265–77. doi: 10.3892/or.2020.7852

86. Shi H, Xie J, Wang K, Li W, Yin L, Wang G, et al. LINC01451 drives epithelial-mesenchymal transition and progression in bladder cancer cells via LIN28/TGF-b/Smad pathway. Cell Signal. 2021;81:109932. doi: 10.1016/j.cellsig.2021.109932

87. Guan Z, Song Y, Ma J, Li F, Zhao X, Liang G, et al. Altered expression of lncRNA NCK1-AS1 distinguished patients with prostate cancer from those with benign prostatic hyperplasia. Oncol Lett. 2019;18(6):6379–84. doi: 10.3892/ol.2019.11039

88. Lang C, Dai Y, Wu Z, Yang Q, He S, Zhang X, et al. SMAD3/SP1 complex-mediated constitutive active loop between lncRNA PCAT7 and TGF-b signaling promotes prostate cancer bone metastasis. Mol Oncol. 2020;14(4):808–28. doi: 10.1002/1878-0261.12634

89. Xi X, Hu Z, Wu Q, Hu K, Cao Z, Zhou J, et al. High expression of small nucleolar RNA host gene 3 predicts poor prognosis and promotes bone metastasis in prostate cancer by activating transforming growth factor-b signaling. Bioengineered. 2022;13(1):1895–907. doi: 10.1080/21655979.2021.2020393

90. Weng W, Liu C, Li G, Ruan Q, Li H, Lin N, et al. Long non-coding RNA SNHG16 functions as a tumor activator by sponging miR3733p to regulate the TGFbR2/SMAD pathway in prostate cancer. Mol Med Rep. 2021;24(6):843. doi: 10.3892/mmr.2021.12483

91. Deng H, Zhu B, Dong Z, Jiang H, Zhao X, Wu S. miR-214-5p targeted by LncRNA DANCR mediates TGF-b signaling pathway to accelerate proliferation, migration and inhibit apoptosis of prostate cancer cells. Am J Transl Res. 2021;13(4):2224–40.

92. Gélabert C, Papoutsoglou P, Golàn I, Ahlström E, Ameur A, Heldin C-H, et al. The long non-coding RNA LINC00707 interacts with Smad proteins to regulate TGFb signaling and cancer cell invasion. Cell Commun Signal. 2023;21(1):271. doi: 10.1186/s12964-023-01273-3

93. DeSouza PA, Qu X, Chen H, Patel B, Maher CA, Kim AH. Long, noncoding RNA dysregulation in glioblastoma. Cancers (Basel). 2021;13(7):1604. doi: 10.3390/cancers13071604

94. Shree B, Tripathi S, Sharma V. Transforming growth factor-B-regulated LncRNA-MUF promotes invasion by modulating the miR-34a snail1 axis in glioblastoma multiforme. Front Oncol. 2021;11:788755. doi: 10.3389/fonc.2021.788755

95. Hegi ME, Liu L, Herman JG, Stupp R, Wick W, Weller M, et al. Correlation of O6-methylguanine methyltransferase (MGMT) promoter methylation with clinical outcomes in glioblastoma and clinical strategies to modulate MGMT activity. J Clin Oncol. 2008;26(25):4189–99. doi: 10.1200/JCO.2007.11.5964

96. Nie E, Jin X, Miao F, Yu T, Zhi T, Shi Z, et al. TGF-b1 modulates temozolomide resistance in glioblastoma via altered microRNA processing and elevated MGMT. Neuro Oncol. 2021;23(3):435–46. doi: 10.1093/neuonc/noaa198

97. Xu H, Zhang B, Yang Y, Li Z, Zhao P, Wu W, et al. LncRNA MIR4435-2HG potentiates the proliferation and invasion of glioblastoma cells via modulating miR-1224-5p/TGFBR2 axis. J Cell Mol Med. 2020;24(11):6362–72. doi: 10.1111/jcmm.15280

98. Wang H, Li H, Jiang Q, Dong X, Li S, Cheng S, et al. HOTAIRM1 Promotes Malignant progression of transformed fibroblasts in glioma stem-like cells remodeled microenvironment via regulating miR-133b-3p/TGFb axis. Front Oncol. 2021;11:603128. doi: 10.3389/fonc.2021.603128

99. Li Y, Liu G, Li X, Dong H, Xiao W, Lu S. Long non-coding RNA SBF2-AS1 promotes hepatocellular carcinoma progression through regulation of miR-140-5p-TGFBR1 pathway. Biochem Biophys Res Commun. 2018;503(4):2826–32. doi: 10.1016/j.bbrc.2018.08.047
Published
2024-03-27
How to Cite
Rodrigues-Junior D. M., & Moustakas A. (2024). Unboxing the network among long non-coding RNAs and TGF-β signaling in cancer. Upsala Journal of Medical Sciences, 129(S1), e10614. https://doi.org/10.48101/ujms.v129.10614