Progress in regulation of long non-coding RNA on malignant biological behavior of gallbladder cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YANG Facai ¹ ,  LI Jingdong ¹ ,  QIU Yinghe ²

1. Department of Hepatobiliary Surgery, Affiliated Hospital of North Sichuan Medical College; Hepatobiliary Research Institute of North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;
2. Department of Biliary Surgery, The Third Affiliated Hospital of Naval Military Medical University, Shanghai 200438, P. R. China;

Corresponding author：

LI Jingdong, Email: lijingdong358@126.com; QIU Yinghe, Email: qiuyinghe@aliyun.com

Keywords：

long non-coding RNA; gallbladder cancer; carcinogenesis; anti-cancer effect; chemoresistance; biomarker

DOI：

10.7507/1007-9424.202004091

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of long non-coding RNA (lncRNA) in the regulation of malignant biological behavior of gallbladder cancer so as to provide references for its related research.Method The relevant literatures about studies of lncRNA in gallbladder cancer in recent years were reviewed.Results The recent studies had shown that 19 lncRNAs associated with gallbladder cancer had played the important roles in regulating tumor cell proliferation, migration, invasion, apoptosis, “sponge” miRNAs, chemoresistance, and tumor metastasis. Among them, most lncRNAs tended to have carcinogenic properties, only a few had anticarcinogenic effect. Although the research suggested the mechanism and role of lncRNA to promote or inhibit the occurrence and development of gallbladder cancer, the current research on its mechanism was still limited. In addition, some lncRNAs were found to be specifically expressed in the serum of patients with gallbladder cancer, so which were expected to become biomarkers for tumor diagnosis and prognosis.Conclusions lncRNAs associated with gallbladder cancer have carcinogenic or anticarcinogenic effect, or chemoresistance. They play potential roles in diagnosis, prognosis, and (or) treatment of tumors, but molecular mechanisms of their effects are still limited.

Citation： YANG Facai, LI Jingdong, QIU Yinghe. Progress in regulation of long non-coding RNA on malignant biological behavior of gallbladder cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(11): 1436-1443. doi: 10.7507/1007-9424.202004091 Copy

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2.	Mishra SK, Kumari N, Krishnani N. Molecular pathogenesis of gallbladder cancer: An update. Mutat Res, 2019, 816-818: 111674.
3.	Montalvo-Jave EE, Rahnemai-Azar AA, Papaconstantinou D, et al. Molecular pathways and potential biomarkers in gallbladder cancer: a comprehensive review. Surg Oncol, 2019, 31: 83-89.
4.	Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature, 2012, 489(7414): 101-108.
5.	Costa FF. Non-coding RNAs: new players in eukaryotic biology. Gene, 2005, 357(2): 83-94.
6.	Zhang G, Lan Y, Xie A, et al. Comprehensive analysis of long noncoding RNA (lncRNA)-chromatin interactions reveals lncRNA functions dependent on binding diverse regulatory elements. J Biol Chem, 2019, 294(43): 15613-15622.
7.	Hon CC, Ramilowski JA, Harshbarger J, et al. An atlas of human long non-coding RNAs with accurate 5′ ends. Nature, 2017, 543(7644): 199-204.
8.	Bekric D, Neureiter D, Ritter M, et al. Long non-coding rnas in biliary tract cancer—an up-to-date review. J Clin Med, 2020, 9(4): 1200.
9.	Zhong Y, Wu XC, Li QP, et al. Long noncoding RNAs as potential biomarkers and therapeutic targets in gallbladder cancer: a systematic review and meta-analysis. Cancer Cell Int, 2019, 19: 169.
10.	Zhou Y, Zhang X, Klibanski A. MEG3 noncoding RNA: A tumor suppressor. J Mol Endocrinol, 2012, 48(3): R45-R53.
11.	Su W, Xie W, Shang Q, et al. The long noncoding RNA MEG3 is downregulated and inversely associated with VEGF levels in osteoarthritis. Biomed Res Int, 2015, 2015: 356893.
12.	Liu B, Shen ED, Liao MM, et al. Expression and mechanisms of long non-coding RNA genes MEG3 and ANRIL in gallbladder cancer. Tumour Biol, 2016, 37(7): 9875-9886.
13.	Jin LY, Cai Q, Wang SH, et al. Long noncoding RNA MEG3 regulates LATS2 by promoting the ubiquitination of EZH2 and inhibits proliferation and invasion in gallbladder cancer. Cell Death Dis, 2018, 9(10): 1017.
14.	Ma MZ, Kong X, Weng MZ, et al. Long non-coding RNA-LET is a positive prognostic factor and exhibits tumor-suppressive activity in gallbladder cancer. Mol Carcinog, 2015, 54(11): 1397-1406.
15.	Shen XH, Qi P, Du X. Long non-coding RNAs in cancer invasion and metastasis. Mod Pathol, 2015, 28(1): 4-13.
16.	Ma MZ, Zhang Y, Weng MZ, et al. Long noncoding RNA GCASPC, a target of miR-17-3p, negatively regulates pyruvate carboxylase-dependent cell proliferation in gallbladder cancer. Cancer Res, 2016, 76(18): 5361-5371.
17.	Wang SH, Wu XC, Zhang MD, et al. Long noncoding RNA H19 contributes to gallbladder cancer cell proliferation by modulated miR-194-5p targeting AKT2. Tumour Biol, 2016, 37(7): 9721-9730.
18.	Wang SH, Ma F, Tang ZH, et al. Long non-coding RNA H19 regulates FOXM1 expression by competitively binding endogenous miR-342-3p in gallbladder cancer. J Exp Clin Cancer Res, 2016, 35(1): 160.
19.	Wang SH, Wu XC, Zhang MD, et al. Upregulation of H19 indicates a poor prognosis in gallbladder carcinoma and promotes epithelial-mesenchymal transition. Am J Cancer Res, 2015, 6(1): 15-26.
20.	Wang SH, Zhang WJ, Wu XC, et al. The lncRNA MALAT1 functions as a competing endogenous RNA to regulate MCL-1 expression by sponging miR-363-3p in gallbladder cancer. J Cell Mol Med, 2016, 20(12): 2299-2308.
21.	Wang SH, Zhang WJ, Wu XC, et al. Long non-coding RNA Malat1 promotes gallbladder cancer development by acting as a molecular sponge to regulate miR-206. Oncotarget, 2016, 7(25): 37857-37867.
22.	Lin N, Yao ZC, Xu MX, et al. Long noncoding RNA MALAT1 potentiates growth and inhibits senescence by antagonizing ABI3BP in gallbladder cancer cells. J Exp Clin Cancer Res, 2019, 38(1): 244.
23.	Ma MZ, Li CX, Zhang Y, et al. Long non-coding RNA HOTAIR, a c-Myc activated driver of malignancy, negatively regulates miRNA-130a in gallbladder cancer. Mol Cancer, 2014, 13: 156.
24.	Ma MZ, Chu BF, Zhang Y, et al. Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218-5p. Cell Death Dis, 2015, 6(1): e1583.
25.	Tu YG, Gao XC, Li G, et al. MicroRNA-218 inhibits glioma invasion, migration, proliferation, and cancer stem-like cell self-renewal by targeting the polycomb group gene Bmi1. Cancer Res, 2013, 73(19): 6046-6055.
26.	Cai Q, Wang ZQ, Wang SH, et al. Upregulation of long non-coding RNA LINC00152 by SP1 contributes to gallbladder cancer cell growth and tumor metastasis via PI3K/AKT pathway. Am J Transl Res, 2016, 8(10): 4068-4081.
27.	Cai Q, Wang ZQ, Wang SH, et al. Long non-coding RNA LINC00152 promotes gallbladder cancer metastasis and epithelial-mesenchymal transition by regulating HIF-1α via miR-138. Open Biol, 2017, 7(1): 160247.
28.	Wang SH, Yang Y, Wu XC, et al. Long non-coding RNA MINCR promotes gallbladder cancer progression through stimulating EZH2 expression. Cancer Lett, 2016, 380(1): 122-133.
29.	Ma F, Wang SH, Cai Q, et al. Overexpression of lncRNA AFAP1-AS1 predicts poor prognosis and promotes cells proliferation and invasion in gallbladder cancer. Biomed Pharmacother, 2016, 84: 1249-1255.
30.	Cai Q, Jin L, Wang S, et al. Long non-coding RNA UCA1 promotes gallbladder cancer progression by epigenetically repressing p21 and E-cadherin expression. Oncotarget, 2017, 8(29): 47957-47968.
31.	Chen JN, Yu Y, Li H, et al. Long non-coding RNA PVT1 promotes tumor progression by regulating the miR-143/HK2 axis in gallbladder cancer. Mol Cancer, 2019, 18(1): 33.
32.	Wu XS, Wang F, Li HF, et al. LncRNA-PAGBC acts as a microRNA sponge and promotes gallbladder tumorigenesis. EMBO Rep, 2017, 18(10): 1837-1853.
33.	Wu XC, Wang SH, Ou HH, et al. The NmrA-like family domain containing 1 pseudogene Loc344887 is amplified in gallbladder cancer and promotes epithelial-mesenchymal transition. Chem Biol Drug Des, 2017, 90(3): 456-463.
34.	Wang SH, Zhang MD, Wu XC, et al. Overexpression of lncRNA-ROR predicts a poor outcome in gallbladder cancer patients and promotes the tumor cells proliferation, migration, and invasion. Tumour Biol, 2016, 37(9): 12867-12875.
35.	Yang L, Gao QX, Wu XX, et al. Long noncoding RNA HEGBC promotes tumorigenesis and metastasis of gallbladder cancer via forming a positive feedback loop with IL-11/STAT3 signaling pathway. J Exp Clin Cancer Res, 2018, 37(1): 186.
36.	Yang F, Tang Z, Duan A, et al. Long noncoding RNA NEAT1 upregulates survivin and facilitates gallbladder cancer progression by sponging microRNA-335. Onco Targets Ther, 2020, 13: 2357-2367.
37.	Cai Q, Wang SH, Jin LY, et al. Long non-coding RNA GBCDRlnc1 induces chemoresistance of gallbladder cancer cells by activating autophagy. Mol Cancer, 2019, 18(1): 82.
38.	da Rocha ST, Edwards CA, Ito M, et al. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet, 2008, 24(6): 306-316.
39.	Yang F, Huo XS, Yuan SX, et al. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell, 2013, 49(6): 1083-1096.
40.	Lin J, Chen Z, Wu S, et al. An NF90/long noncoding RNA-LET/miR-548k feedback amplification loop controls esophageal squamous cell carcinoma progression. J Cancer, 2019, 10(21): 5139-5152.
41.	Ye Z, Duan JC, Wang LH, et al. LncRNA-LET inhibits cell growth of clear cell renal cell carcinoma by regulating miR-373-3p. Cancer Cell Int, 2019, 19: 311.
42.	Zhou CX, Wang X, Yang N, et al. LncRNA LET function as a tumor suppressor in breast cancer development. Eur Rev Med Pharmacol Sci, 2018, 22(18): 6002-6007.
43.	Liu X, Zhao Y, Li Y, et al. Quantitative assessment of lncRNA H19 polymorphisms and cancer risk: a meta-analysis based on 48 166 subjects. Artif Cells Nanomed Biotechnol, 2020, 48(1): 15-27.
44.	Raveh E, Matouk IJ, Gilon M, et al. The H19 long non-coding RNA in cancer initiation, progression and metastasis—a proposed unifying theory. Mol Cancer, 2015, 14: 184.
45.	Wilusz JE, Freier SM, Spector DL. 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell, 2008, 135(5): 919-932.
46.	Li ZX, Zhu QN, Zhang HB, et al. MALAT1: a potential biomarker in cancer. Cancer Manag Res, 2018, 10: 6757-6768.
47.	Sun KK, Hu PP, Xu F. Prognostic significance of long non-coding RNA MALAT1 for predicting the recurrence and metastasis of gallbladder cancer and its effect on cell proliferation, migration, invasion, and apoptosis. J Cell Biochem, 2018, 119(4): 3099-3110.
48.	He S, Liu SP, Zhu H., et al The sequence, structure and evolutionary features of HOTAIR in mammals. BMC Evol Biol, 2011, 11: 102.
49.	Xiang JF, Yin QF, Chen T, et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res, 2014, 24(5): 513-531.
50.	Dai K, Quan J, Yan F, et al. lncRNAs as potential molecular biomarkers in the clinicopathology and prognosis of cholangiocarcinoma: a systematic review and meta-analysis. Onco Targets Ther, 2019, 12: 1905-1915.
51.	Pasmant E, Laurendeau I, Héron D, et al. Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res, 2007, 67(8): 3963-3969.
52.	Xu J, Guo J, Jiang Y, et al. Improved characterization of the relationship between long intergenic non-coding RNA Linc00152 and the occurrence and development of malignancies. Cancer Med, 2019, 8(10): 4722-4731.
53.	Doose G, Haake A, Bernhart SH, et al. MINCR Is a MYC-induced lncRNA able to modulate MYC's transcriptional network in burkitt lymphoma cells. Proc Natl Acad Sci USA, 2015, 112(38): E5261-5270.
54.	Jin XL, Lian JR, Guan YH. Overexpression of long non-coding RNA MINCR contributes to progressive clinicopathological features and poor prognosis of human hepatocellular carcinoma. Eur Rev Med Pharmacol Sci, 2018, 22(23): 8197-8202.
55.	Wang J, Ding M, Zhu H, et al. Up-regulation of long noncoding RNA MINCR promotes non-small cell of lung cancer growth by negatively regulating miR-126/SLC7A5 axis. Biochem Biophys Res Commun, 2019, 508(3): 780-784.
56.	Lyu Q, Jin L, Yang X, et al. LncRNA MINCR activates Wnt/β-catenin signals to promote cell proliferation and migration in oral squamous cell carcinoma. Pathol Res Pract, 2019, 215(5): 924-930.
57.	Zhang F, Li J, Xiao H, et al. AFAP1-AS1: A novel oncogenic long non-coding RNA in human cancers. Cell Prolif, 2018, 51(1): e12397.
58.	Ji D, Zhong X, Jiang X, et al. The role of long non-coding RNA AFAP1-AS1 in human malignant tumors. Pathol Res Pract, 2018, 214(10): 1524-1531.
59.	Wang XS, Zhang Z, Wang HC, et al. Rapid identification of UCA1 as a very sensitive and specific unique marker for human bladder carcinoma. Clin Cancer Res, 2006, 12(16): 4851-4858.
60.	Ghafouri-Fard S, Omrani MD, Taheri M. Long noncoding RNA PVT1: a highly dysregulated gene in malignancy. J Cell Physiol, 2020, 235(2): 818-835.
61.	Clemson CM, Hutchinson JN, Sara SA, et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell, 2009, 33(6): 717-726.
62.	Souquere S, Beauclair G, Harper F, et al. Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol Biol Cell, 2010, 21(22): 4020-4027.
63.	Fox AH, Nakagawa S, Hirose T, et al. Paraspeckles: where long noncoding RNA meets phase separation. Trends Biochem Sci, 2018, 43(2): 124-135.
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71.	Wang FW, Cao CH, Han K, et al. APC-activated long noncoding RNA inhibits colorectal carcinoma pathogenesis through reduction of exosome production. J Clin Invest, 2019, 129(2): 727-743.

1. Cherkassky L, D’Angelica M. Gallbladder cancer: managing the incidental diagnosis. Surg Oncol Clin N Am, 2019, 28(4): 619-630.
2. Mishra SK, Kumari N, Krishnani N. Molecular pathogenesis of gallbladder cancer: An update. Mutat Res, 2019, 816-818: 111674.
3. Montalvo-Jave EE, Rahnemai-Azar AA, Papaconstantinou D, et al. Molecular pathways and potential biomarkers in gallbladder cancer: a comprehensive review. Surg Oncol, 2019, 31: 83-89.
4. Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature, 2012, 489(7414): 101-108.
5. Costa FF. Non-coding RNAs: new players in eukaryotic biology. Gene, 2005, 357(2): 83-94.
6. Zhang G, Lan Y, Xie A, et al. Comprehensive analysis of long noncoding RNA (lncRNA)-chromatin interactions reveals lncRNA functions dependent on binding diverse regulatory elements. J Biol Chem, 2019, 294(43): 15613-15622.
7. Hon CC, Ramilowski JA, Harshbarger J, et al. An atlas of human long non-coding RNAs with accurate 5′ ends. Nature, 2017, 543(7644): 199-204.
8. Bekric D, Neureiter D, Ritter M, et al. Long non-coding rnas in biliary tract cancer—an up-to-date review. J Clin Med, 2020, 9(4): 1200.
9. Zhong Y, Wu XC, Li QP, et al. Long noncoding RNAs as potential biomarkers and therapeutic targets in gallbladder cancer: a systematic review and meta-analysis. Cancer Cell Int, 2019, 19: 169.
10. Zhou Y, Zhang X, Klibanski A. MEG3 noncoding RNA: A tumor suppressor. J Mol Endocrinol, 2012, 48(3): R45-R53.
11. Su W, Xie W, Shang Q, et al. The long noncoding RNA MEG3 is downregulated and inversely associated with VEGF levels in osteoarthritis. Biomed Res Int, 2015, 2015: 356893.
12. Liu B, Shen ED, Liao MM, et al. Expression and mechanisms of long non-coding RNA genes MEG3 and ANRIL in gallbladder cancer. Tumour Biol, 2016, 37(7): 9875-9886.
13. Jin LY, Cai Q, Wang SH, et al. Long noncoding RNA MEG3 regulates LATS2 by promoting the ubiquitination of EZH2 and inhibits proliferation and invasion in gallbladder cancer. Cell Death Dis, 2018, 9(10): 1017.
14. Ma MZ, Kong X, Weng MZ, et al. Long non-coding RNA-LET is a positive prognostic factor and exhibits tumor-suppressive activity in gallbladder cancer. Mol Carcinog, 2015, 54(11): 1397-1406.
15. Shen XH, Qi P, Du X. Long non-coding RNAs in cancer invasion and metastasis. Mod Pathol, 2015, 28(1): 4-13.
16. Ma MZ, Zhang Y, Weng MZ, et al. Long noncoding RNA GCASPC, a target of miR-17-3p, negatively regulates pyruvate carboxylase-dependent cell proliferation in gallbladder cancer. Cancer Res, 2016, 76(18): 5361-5371.
17. Wang SH, Wu XC, Zhang MD, et al. Long noncoding RNA H19 contributes to gallbladder cancer cell proliferation by modulated miR-194-5p targeting AKT2. Tumour Biol, 2016, 37(7): 9721-9730.
18. Wang SH, Ma F, Tang ZH, et al. Long non-coding RNA H19 regulates FOXM1 expression by competitively binding endogenous miR-342-3p in gallbladder cancer. J Exp Clin Cancer Res, 2016, 35(1): 160.
19. Wang SH, Wu XC, Zhang MD, et al. Upregulation of H19 indicates a poor prognosis in gallbladder carcinoma and promotes epithelial-mesenchymal transition. Am J Cancer Res, 2015, 6(1): 15-26.
20. Wang SH, Zhang WJ, Wu XC, et al. The lncRNA MALAT1 functions as a competing endogenous RNA to regulate MCL-1 expression by sponging miR-363-3p in gallbladder cancer. J Cell Mol Med, 2016, 20(12): 2299-2308.
21. Wang SH, Zhang WJ, Wu XC, et al. Long non-coding RNA Malat1 promotes gallbladder cancer development by acting as a molecular sponge to regulate miR-206. Oncotarget, 2016, 7(25): 37857-37867.
22. Lin N, Yao ZC, Xu MX, et al. Long noncoding RNA MALAT1 potentiates growth and inhibits senescence by antagonizing ABI3BP in gallbladder cancer cells. J Exp Clin Cancer Res, 2019, 38(1): 244.
23. Ma MZ, Li CX, Zhang Y, et al. Long non-coding RNA HOTAIR, a c-Myc activated driver of malignancy, negatively regulates miRNA-130a in gallbladder cancer. Mol Cancer, 2014, 13: 156.
24. Ma MZ, Chu BF, Zhang Y, et al. Long non-coding RNA CCAT1 promotes gallbladder cancer development via negative modulation of miRNA-218-5p. Cell Death Dis, 2015, 6(1): e1583.
25. Tu YG, Gao XC, Li G, et al. MicroRNA-218 inhibits glioma invasion, migration, proliferation, and cancer stem-like cell self-renewal by targeting the polycomb group gene Bmi1. Cancer Res, 2013, 73(19): 6046-6055.
26. Cai Q, Wang ZQ, Wang SH, et al. Upregulation of long non-coding RNA LINC00152 by SP1 contributes to gallbladder cancer cell growth and tumor metastasis via PI3K/AKT pathway. Am J Transl Res, 2016, 8(10): 4068-4081.
27. Cai Q, Wang ZQ, Wang SH, et al. Long non-coding RNA LINC00152 promotes gallbladder cancer metastasis and epithelial-mesenchymal transition by regulating HIF-1α via miR-138. Open Biol, 2017, 7(1): 160247.
28. Wang SH, Yang Y, Wu XC, et al. Long non-coding RNA MINCR promotes gallbladder cancer progression through stimulating EZH2 expression. Cancer Lett, 2016, 380(1): 122-133.
29. Ma F, Wang SH, Cai Q, et al. Overexpression of lncRNA AFAP1-AS1 predicts poor prognosis and promotes cells proliferation and invasion in gallbladder cancer. Biomed Pharmacother, 2016, 84: 1249-1255.
30. Cai Q, Jin L, Wang S, et al. Long non-coding RNA UCA1 promotes gallbladder cancer progression by epigenetically repressing p21 and E-cadherin expression. Oncotarget, 2017, 8(29): 47957-47968.
31. Chen JN, Yu Y, Li H, et al. Long non-coding RNA PVT1 promotes tumor progression by regulating the miR-143/HK2 axis in gallbladder cancer. Mol Cancer, 2019, 18(1): 33.
32. Wu XS, Wang F, Li HF, et al. LncRNA-PAGBC acts as a microRNA sponge and promotes gallbladder tumorigenesis. EMBO Rep, 2017, 18(10): 1837-1853.
33. Wu XC, Wang SH, Ou HH, et al. The NmrA-like family domain containing 1 pseudogene Loc344887 is amplified in gallbladder cancer and promotes epithelial-mesenchymal transition. Chem Biol Drug Des, 2017, 90(3): 456-463.
34. Wang SH, Zhang MD, Wu XC, et al. Overexpression of lncRNA-ROR predicts a poor outcome in gallbladder cancer patients and promotes the tumor cells proliferation, migration, and invasion. Tumour Biol, 2016, 37(9): 12867-12875.
35. Yang L, Gao QX, Wu XX, et al. Long noncoding RNA HEGBC promotes tumorigenesis and metastasis of gallbladder cancer via forming a positive feedback loop with IL-11/STAT3 signaling pathway. J Exp Clin Cancer Res, 2018, 37(1): 186.
36. Yang F, Tang Z, Duan A, et al. Long noncoding RNA NEAT1 upregulates survivin and facilitates gallbladder cancer progression by sponging microRNA-335. Onco Targets Ther, 2020, 13: 2357-2367.
37. Cai Q, Wang SH, Jin LY, et al. Long non-coding RNA GBCDRlnc1 induces chemoresistance of gallbladder cancer cells by activating autophagy. Mol Cancer, 2019, 18(1): 82.
38. da Rocha ST, Edwards CA, Ito M, et al. Genomic imprinting at the mammalian Dlk1-Dio3 domain. Trends Genet, 2008, 24(6): 306-316.
39. Yang F, Huo XS, Yuan SX, et al. Repression of the long noncoding RNA-LET by histone deacetylase 3 contributes to hypoxia-mediated metastasis. Mol Cell, 2013, 49(6): 1083-1096.
40. Lin J, Chen Z, Wu S, et al. An NF90/long noncoding RNA-LET/miR-548k feedback amplification loop controls esophageal squamous cell carcinoma progression. J Cancer, 2019, 10(21): 5139-5152.
41. Ye Z, Duan JC, Wang LH, et al. LncRNA-LET inhibits cell growth of clear cell renal cell carcinoma by regulating miR-373-3p. Cancer Cell Int, 2019, 19: 311.
42. Zhou CX, Wang X, Yang N, et al. LncRNA LET function as a tumor suppressor in breast cancer development. Eur Rev Med Pharmacol Sci, 2018, 22(18): 6002-6007.
43. Liu X, Zhao Y, Li Y, et al. Quantitative assessment of lncRNA H19 polymorphisms and cancer risk: a meta-analysis based on 48 166 subjects. Artif Cells Nanomed Biotechnol, 2020, 48(1): 15-27.
44. Raveh E, Matouk IJ, Gilon M, et al. The H19 long non-coding RNA in cancer initiation, progression and metastasis—a proposed unifying theory. Mol Cancer, 2015, 14: 184.
45. Wilusz JE, Freier SM, Spector DL. 3' end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA. Cell, 2008, 135(5): 919-932.
46. Li ZX, Zhu QN, Zhang HB, et al. MALAT1: a potential biomarker in cancer. Cancer Manag Res, 2018, 10: 6757-6768.
47. Sun KK, Hu PP, Xu F. Prognostic significance of long non-coding RNA MALAT1 for predicting the recurrence and metastasis of gallbladder cancer and its effect on cell proliferation, migration, invasion, and apoptosis. J Cell Biochem, 2018, 119(4): 3099-3110.
48. He S, Liu SP, Zhu H., et al The sequence, structure and evolutionary features of HOTAIR in mammals. BMC Evol Biol, 2011, 11: 102.
49. Xiang JF, Yin QF, Chen T, et al. Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res, 2014, 24(5): 513-531.
50. Dai K, Quan J, Yan F, et al. lncRNAs as potential molecular biomarkers in the clinicopathology and prognosis of cholangiocarcinoma: a systematic review and meta-analysis. Onco Targets Ther, 2019, 12: 1905-1915.
51. Pasmant E, Laurendeau I, Héron D, et al. Characterization of a germ-line deletion, including the entire INK4/ARF locus, in a melanoma-neural system tumor family: identification of ANRIL, an antisense noncoding RNA whose expression coclusters with ARF. Cancer Res, 2007, 67(8): 3963-3969.
52. Xu J, Guo J, Jiang Y, et al. Improved characterization of the relationship between long intergenic non-coding RNA Linc00152 and the occurrence and development of malignancies. Cancer Med, 2019, 8(10): 4722-4731.
53. Doose G, Haake A, Bernhart SH, et al. MINCR Is a MYC-induced lncRNA able to modulate MYC's transcriptional network in burkitt lymphoma cells. Proc Natl Acad Sci USA, 2015, 112(38): E5261-5270.
54. Jin XL, Lian JR, Guan YH. Overexpression of long non-coding RNA MINCR contributes to progressive clinicopathological features and poor prognosis of human hepatocellular carcinoma. Eur Rev Med Pharmacol Sci, 2018, 22(23): 8197-8202.
55. Wang J, Ding M, Zhu H, et al. Up-regulation of long noncoding RNA MINCR promotes non-small cell of lung cancer growth by negatively regulating miR-126/SLC7A5 axis. Biochem Biophys Res Commun, 2019, 508(3): 780-784.
56. Lyu Q, Jin L, Yang X, et al. LncRNA MINCR activates Wnt/β-catenin signals to promote cell proliferation and migration in oral squamous cell carcinoma. Pathol Res Pract, 2019, 215(5): 924-930.
57. Zhang F, Li J, Xiao H, et al. AFAP1-AS1: A novel oncogenic long non-coding RNA in human cancers. Cell Prolif, 2018, 51(1): e12397.
58. Ji D, Zhong X, Jiang X, et al. The role of long non-coding RNA AFAP1-AS1 in human malignant tumors. Pathol Res Pract, 2018, 214(10): 1524-1531.
59. Wang XS, Zhang Z, Wang HC, et al. Rapid identification of UCA1 as a very sensitive and specific unique marker for human bladder carcinoma. Clin Cancer Res, 2006, 12(16): 4851-4858.
60. Ghafouri-Fard S, Omrani MD, Taheri M. Long noncoding RNA PVT1: a highly dysregulated gene in malignancy. J Cell Physiol, 2020, 235(2): 818-835.
61. Clemson CM, Hutchinson JN, Sara SA, et al. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol Cell, 2009, 33(6): 717-726.
62. Souquere S, Beauclair G, Harper F, et al. Highly ordered spatial organization of the structural long noncoding NEAT1 RNAs within paraspeckle nuclear bodies. Mol Biol Cell, 2010, 21(22): 4020-4027.
63. Fox AH, Nakagawa S, Hirose T, et al. Paraspeckles: where long noncoding RNA meets phase separation. Trends Biochem Sci, 2018, 43(2): 124-135.
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