Association between PVT1 expression and digestive system tumors: a systematic review_Chinese Journal of Evidence-Based Medicine

Authors：

YANG Kang ^1,2 , CAO Wei ² , LI Jiale ³ ,  CHEN Bo ²

1. Department of General Surgery, the Fourth Affiliated Hospital of Anhui Medical University, Hefei 230011, P.R.China;
2. Department of General Surgery, the First Affiliated Hospital of Anhui Medical University, Hefei 230022, P.R.China;
3. Department of Emergency Medicine, The Second Affiliated Hospital of Anhui Medical University, Hefei 230601, P.R.China;

Corresponding author：

CHEN Bo, Email: chenbo@ahmu.edu.cn

Keywords：

PVT1; Digestive system tumor; Prognosis; Systematic review; Meta-analysis; Case-control study

DOI：

10.7507/1672-2531.202104091

Video：

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Objective To systematically review the association between PVT1 expression and digestive system tumors (DST). Methods PubMed, EMbase, Web of Science, The Cochrane Library, CBM, and CNKI databases were electronically searched to collect case-control studies on the correlation between PVT1 expression and DST from inception to June 2021. Two reviewers independently screened literature, extracted data, and assessed the risk of bias of included studies. Meta-analysis was then performed by using Stata 16.0 software. Results A total of 34 case-control studies involving 3 882 DST patients were included. The results of meta-analysis showed that the high expression of PVT1 was significantly associated with tumor size (>5 cm), differentiation degree (poor), T stage (T₃-T₄), lymph node metastasis (N⁺), distant metastasis (M⁺), and clinical stages (Ⅲ-Ⅳ) of DST; however, it was not associated with gender, age and venous invasion. In addition, the high expression of PVT1 in DST tissues was significantly correlated with the low rates of 1, 3 and 5-year overall survival and poor prognosis (HR=1.96, 95%CI 1.70 to 2.26, P<0.000 1). Subgroup analysis showed that the high expression of PVT1 was significantly associated with poor prognosis of gastric cancer, colorectal cancer, pancreatic cancer and liver cancer.Conclusions Current evidence shows that the high expression of PVT1 is correlated with the clinic pathological features (tumor size >5 cm, poor differentiation, T₃-T₄ stage, lymph node metastasis, distant metastasis, and clinical stage Ⅲ-Ⅳ) and indicates poor prognosis in most patients with DST (gastric cancer, colorectal cancer, pancreatic cancer, liver cancer).

Citation： YANG Kang, CAO Wei, LI Jiale, CHEN Bo. Association between PVT1 expression and digestive system tumors: a systematic review. Chinese Journal of Evidence-Based Medicine, 2021, 21(10): 1133-1140. doi: 10.7507/1672-2531.202104091 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Feng RM, Zong YN, Cao SM, et al. Current cancer situation in China: good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond), 2019, 39(1): 22.
3.	Maule M, Merletti F. Cancer transition and priorities for cancer control. Lancet Oncol, 2012, 13(8): 745-746.
4.	Cui M, You L, Ren X, et al. Long non-coding RNA PVT1 and cancer. Biochem Biophys Res Commun, 2016, 471(1): 10-14.
5.	Guo K, Yao J, Yu Q, et al. The expression pattern of long non-coding RNA PVT1 in tumor tissues and in extracellular vesicles of colorectal cancer correlates with cancer progression. Tumour Biol, 2017, 39(4): 1010428317699122.
6.	Wu BQ, Jiang Y, Zhu F, et al. Long noncoding RNA PVT1 promotes EMT and cell proliferation and migration through downregulating p21 in pancreatic cancer cells. Technol Cancer Res Treat, 2017, 16(6): 819-827.
7.	Guan Y, Kuo WL, Stilwell JL, et al. Amplification of PVT1 contributes to the pathophysiology of ovarian and breast cancer. Clin Cancer Res, 2007, 13(19): 5745-5755.
8.	Huang T, Liu HW, Chen JQ, et al. The long noncoding RNA PVT1 functions as a competing endogenous RNA by sponging miR-186 in gastric cancer. Biomed Pharmacother, 2017, 88: 302-308.
9.	Huang C, Liu S, Wang H, et al. LncRNA PVT1 overexpression is a poor prognostic biomarker and regulates migration and invasion in small cell lung cancer. Am J Transl Res, 2016, 8(11): 5025-5034.
10.	Chen S, Zhou L, Wang Y. ALKBH5-mediated m6A demethylation of lncRNA PVT1 plays an oncogenic role in osteosarcoma. Cancer Cell Int, 2020, 20: 34.
11.	Wang L, Xiao B, Yu T, et al. lncRNA PVT1 promotes the migration of gastric cancer by functioning as ceRNA of miR-30a and regulating Snail. J Cell Physiol, 2021, 236(1): 536-548.
12.	Li B, Guo LH, Ban ZQ, et al. Upregulation of lncRNA plasmacytoma variant translocation 1 predicts poor prognosis in patients with muscle-invasive bladder cancer. Medicine (Baltimore), 2020, 99(28): e21059.
13.	Han Y, Li F, Xie J, et al. PVT1 Mediates cell proliferation, apoptosis and radioresistance in nasopharyngeal carcinoma through regulating miR-515-5p/PIK3CA axis. Cancer Manag Res, 2020, 12: 10077-10090.
14.	Yu X, Zhao J, He Y. Long non-coding RNA PVT1 functions as an oncogene in human colon cancer through miR-30d-5p/RUNX2 axis. J BUON, 2018, 23(1): 48-54.
15.	Takahashi Y, Sawada G, Kurashige J, et al. Amplification of PVT-1 is involved in poor prognosis via apoptosis inhibition in colorectal cancers. Br J Cancer, 2014, 110(1): 164-171.
16.	Li Q, Dai Y, Wang F, et al. Differentially expressed long non-coding RNAs and the prognostic potential in colorectal cancer. Neoplasma, 2016, 63(6): 977-983.
17.	Tong D, Zou E, Bai L, et al. IRF-1 mediated long non-coding RNA PVT1-214 promotes oxaliplatin resistance of colorectal cancer via miR-128 inhibition. J BUON, 2020, 25(5): 2205-2214.
18.	Liu F, Wu R, Guan L, et al. Knockdown of PVT1 suppresses colorectal cancer progression by regulating MiR-106b-5p/FJX1 axis. Cancer Manag Res, 2020, 12: 8773-8785.
19.	Wu H, Wei M, Jiang X, et al. lncRNA PVT1 promotes tumorigenesis of colorectal cancer by stabilizing miR-16-5p and interacting with the VEGFA/VEGFR1/AKT axis. Mol Ther Nucleic Acids, 2020, 20: 438-450.
20.	Fan H, Zhu JH, Yao XQ. Long non-coding RNA PVT1 as a novel potential biomarker for predicting the prognosis of colorectal cancer. Int J Biol Markers, 2018, 33(4): 415-422.
21.	He F, Song Z, Chen H, et al. Long noncoding RNA PVT1-214 promotes proliferation and invasion of colorectal cancer by stabilizing Lin28 and interacting with miR-128. Oncogene, 2019, 38(2): 164-179.
22.	Pan X, Cheng R, Zhu X, et al. Prognostic significance and diagnostic value of overexpressed lncRNA PVT1 in colorectal cancer. Clin Lab, 2019, 65(12).
23.	Ping G, Xiong W, Zhang L, et al. Silencing long noncoding RNA PVT1 inhibits tumorigenesis and cisplatin resistance of colorectal cancer. Am J Transl Res, 2018, 10(1): 138-149.
24.	Shigeyasu K, Toden S, Ozawa T, et al. The PVT1 lncRNA is a novel epigenetic enhancer of MYC, and a promising risk-stratification biomarker in colorectal cancer. Mol Cancer, 2020, 19(1): 155.
25.	任晓阳. 长链非编码 RNA PVT1 和 NEAT1 在食管鳞状细胞癌中的表达及意义. 青岛: 青岛大学, 2017.
26.	Li PD, Hu JL, Ma C, et al. Upregulation of the long non-coding RNA PVT1 promotes esophageal squamous cell carcinoma progression by acting as a molecular sponge of miR-203 and LASP1. Oncotarget, 2017, 8(21): 34164-34176.
27.	Zheng X, Hu H, Li S. High expression of lncRNA PVT1 promotes invasion by inducing epithelial-to-mesenchymal transition in esophageal cancer. Oncol Lett, 2016, 12(4): 2357-2362.
28.	Xu Y, Li Y, Jin J, et al. LncRNA PVT1 up-regulation is a poor prognosticator and serves as a therapeutic target in esophageal adenocarcinoma. Mol Cancer, 2019, 18(1): 141.
29.	Huang C, Yu W, Wang Q, et al. Increased expression of the lncRNA PVT1 is associated with poor prognosis in pancreatic cancer patients. Minerva Med, 2015, 106(3): 143-149.
30.	Huang F, Chen W, Peng J, et al. LncRNA PVT1 triggers cyto-protective autophagy and promotes pancreatic ductal adenocarcinoma development via the miR-20a-5p/ULK1 axis. Mol Cancer, 2018, 17(1): 98.
31.	Yuan CL, Li H, Zhu L, et al. Aberrant expression of long noncoding RNA PVT1 and its diagnostic and prognostic significance in patients with gastric cancer. Neoplasma, 2016, 63(3): 442-449.
32.	Ding J, Li D, Gong M, et al. Expression and clinical significance of the long non-coding RNA PVT1 in human gastric cancer. Onco Targets Ther, 2014, 7: 1625-1630.
33.	Li Y, Song S, Pizzi MP, et al. LncRNA PVT1 is a poor prognosticator and can be targeted by PVT1 antisense oligos in gastric adenocarcinoma. Cancers (Basel), 2020, 12(10): 2995.
34.	Zhao J, Du P, Cui P, et al. LncRNA PVT1 promotes angiogenesis via activating the STAT3/VEGFA axis in gastric cancer. Oncogene, 2018, 37(30): 4094-4109.
35.	Kong R, Zhang EB, Yin DD, et al. Long noncoding RNA PVT1 indicates a poor prognosis of gastric cancer and promotes cell proliferation through epigenetically regulating p15 and p16. Mol Cancer, 2015, 14: 82.
36.	Niu J, Song X, Zhang X. Regulation of lncRNA PVT1 on miR-125 in metastasis of gastric cancer cells. Oncol Lett, 2020, 19(2): 1261-1266.
37.	Luo Z, Cao P. Long noncoding RNA PVT1 promotes hepatoblastoma cell proliferation through activating STAT3. Cancer Manag Res, 2019, 11: 8517-8527.
38.	Gou X, Zhao X, Wang Z. Long noncoding RNA PVT1 promotes hepatocellular carcinoma progression through regulating miR-214. Cancer Biomark, 2017, 20(4): 511-519.
39.	Lan T, Yan X, Li Z, et al. Long non-coding RNA PVT1 serves as a competing endogenous RNA for miR-186-5p to promote the tumorigenesis and metastasis of hepatocellular carcinoma. Tumour Biol, 2017, 39(6): 1010428317705338.
40.	Wang F, Yuan JH, Wang SB, et al. Oncofetal long noncoding RNA PVT1 promotes proliferation and stem cell-like property of hepatocellular carcinoma cells by stabilizing NOP2. Hepatology, 2014, 60(4): 1278-1290.
41.	陈昌娜, 于红刚. 长链非编码RNA PVT1在肝癌组织中的表达与临床意义. 现代生物医学进展, 2019, 19(16): 3110-3114.
42.	Ding C, Yang Z, Lv Z, et al. Long non-coding RNA PVT1 is associated with tumor progression and predicts recurrence in hepatocellular carcinoma patients. Oncol Lett, 2015, 9(2): 955-963.
43.	Guo J, Hao C, Wang C, et al. Long noncoding RNA PVT1 modulates hepatocellular carcinoma cell proliferation and apoptosis by recruiting EZH2. Cancer Cell Int, 2018, 18: 98.
44.	Yang L, Peng X, Jin H, et al. Long non-coding RNA PVT1 promotes autophagy as ceRNA to target ATG3 by sponging microRNA-365 in hepatocellular carcinoma. Gene, 2019, 697: 94-102.
45.	吴大平, 吴焕良, 郑文宏, 等. 长链非编码 RNA PVT1 和 miR-30 d-5 p 在肝内胆管癌组织中的表达及其与预后相关性分析. 现代肿瘤医学, 2020, 28(16): 2833-2837.
46.	Xu MD, Wang Y, Weng W, et al. A positive feedback loop of lncRNA- PVT1 and FOXM1 facilitates gastric cancer growth and invasion. Clin Cancer Res, 2017, 23(8): 2071-2080.
47.	Guo K, Yao J, Yu Q, et al. The expression pattern of long non-coding RNA PVT1 in tumor tissues and in extracellular vesicles of colorectal cancer correlates with cancer progression. Tumour Biol, 2017, 39(4): 1010428317699122.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Feng RM, Zong YN, Cao SM, et al. Current cancer situation in China: good or bad news from the 2018 global cancer statistics? Cancer Commun (Lond), 2019, 39(1): 22.
3. Maule M, Merletti F. Cancer transition and priorities for cancer control. Lancet Oncol, 2012, 13(8): 745-746.
4. Cui M, You L, Ren X, et al. Long non-coding RNA PVT1 and cancer. Biochem Biophys Res Commun, 2016, 471(1): 10-14.
5. Guo K, Yao J, Yu Q, et al. The expression pattern of long non-coding RNA PVT1 in tumor tissues and in extracellular vesicles of colorectal cancer correlates with cancer progression. Tumour Biol, 2017, 39(4): 1010428317699122.
6. Wu BQ, Jiang Y, Zhu F, et al. Long noncoding RNA PVT1 promotes EMT and cell proliferation and migration through downregulating p21 in pancreatic cancer cells. Technol Cancer Res Treat, 2017, 16(6): 819-827.
7. Guan Y, Kuo WL, Stilwell JL, et al. Amplification of PVT1 contributes to the pathophysiology of ovarian and breast cancer. Clin Cancer Res, 2007, 13(19): 5745-5755.
8. Huang T, Liu HW, Chen JQ, et al. The long noncoding RNA PVT1 functions as a competing endogenous RNA by sponging miR-186 in gastric cancer. Biomed Pharmacother, 2017, 88: 302-308.
9. Huang C, Liu S, Wang H, et al. LncRNA PVT1 overexpression is a poor prognostic biomarker and regulates migration and invasion in small cell lung cancer. Am J Transl Res, 2016, 8(11): 5025-5034.
10. Chen S, Zhou L, Wang Y. ALKBH5-mediated m6A demethylation of lncRNA PVT1 plays an oncogenic role in osteosarcoma. Cancer Cell Int, 2020, 20: 34.
11. Wang L, Xiao B, Yu T, et al. lncRNA PVT1 promotes the migration of gastric cancer by functioning as ceRNA of miR-30a and regulating Snail. J Cell Physiol, 2021, 236(1): 536-548.
12. Li B, Guo LH, Ban ZQ, et al. Upregulation of lncRNA plasmacytoma variant translocation 1 predicts poor prognosis in patients with muscle-invasive bladder cancer. Medicine (Baltimore), 2020, 99(28): e21059.
13. Han Y, Li F, Xie J, et al. PVT1 Mediates cell proliferation, apoptosis and radioresistance in nasopharyngeal carcinoma through regulating miR-515-5p/PIK3CA axis. Cancer Manag Res, 2020, 12: 10077-10090.
14. Yu X, Zhao J, He Y. Long non-coding RNA PVT1 functions as an oncogene in human colon cancer through miR-30d-5p/RUNX2 axis. J BUON, 2018, 23(1): 48-54.
15. Takahashi Y, Sawada G, Kurashige J, et al. Amplification of PVT-1 is involved in poor prognosis via apoptosis inhibition in colorectal cancers. Br J Cancer, 2014, 110(1): 164-171.
16. Li Q, Dai Y, Wang F, et al. Differentially expressed long non-coding RNAs and the prognostic potential in colorectal cancer. Neoplasma, 2016, 63(6): 977-983.
17. Tong D, Zou E, Bai L, et al. IRF-1 mediated long non-coding RNA PVT1-214 promotes oxaliplatin resistance of colorectal cancer via miR-128 inhibition. J BUON, 2020, 25(5): 2205-2214.
18. Liu F, Wu R, Guan L, et al. Knockdown of PVT1 suppresses colorectal cancer progression by regulating MiR-106b-5p/FJX1 axis. Cancer Manag Res, 2020, 12: 8773-8785.
19. Wu H, Wei M, Jiang X, et al. lncRNA PVT1 promotes tumorigenesis of colorectal cancer by stabilizing miR-16-5p and interacting with the VEGFA/VEGFR1/AKT axis. Mol Ther Nucleic Acids, 2020, 20: 438-450.
20. Fan H, Zhu JH, Yao XQ. Long non-coding RNA PVT1 as a novel potential biomarker for predicting the prognosis of colorectal cancer. Int J Biol Markers, 2018, 33(4): 415-422.
21. He F, Song Z, Chen H, et al. Long noncoding RNA PVT1-214 promotes proliferation and invasion of colorectal cancer by stabilizing Lin28 and interacting with miR-128. Oncogene, 2019, 38(2): 164-179.
22. Pan X, Cheng R, Zhu X, et al. Prognostic significance and diagnostic value of overexpressed lncRNA PVT1 in colorectal cancer. Clin Lab, 2019, 65(12).
23. Ping G, Xiong W, Zhang L, et al. Silencing long noncoding RNA PVT1 inhibits tumorigenesis and cisplatin resistance of colorectal cancer. Am J Transl Res, 2018, 10(1): 138-149.
24. Shigeyasu K, Toden S, Ozawa T, et al. The PVT1 lncRNA is a novel epigenetic enhancer of MYC, and a promising risk-stratification biomarker in colorectal cancer. Mol Cancer, 2020, 19(1): 155.
25. 任晓阳. 长链非编码 RNA PVT1 和 NEAT1 在食管鳞状细胞癌中的表达及意义. 青岛: 青岛大学, 2017.
26. Li PD, Hu JL, Ma C, et al. Upregulation of the long non-coding RNA PVT1 promotes esophageal squamous cell carcinoma progression by acting as a molecular sponge of miR-203 and LASP1. Oncotarget, 2017, 8(21): 34164-34176.
27. Zheng X, Hu H, Li S. High expression of lncRNA PVT1 promotes invasion by inducing epithelial-to-mesenchymal transition in esophageal cancer. Oncol Lett, 2016, 12(4): 2357-2362.
28. Xu Y, Li Y, Jin J, et al. LncRNA PVT1 up-regulation is a poor prognosticator and serves as a therapeutic target in esophageal adenocarcinoma. Mol Cancer, 2019, 18(1): 141.
29. Huang C, Yu W, Wang Q, et al. Increased expression of the lncRNA PVT1 is associated with poor prognosis in pancreatic cancer patients. Minerva Med, 2015, 106(3): 143-149.
30. Huang F, Chen W, Peng J, et al. LncRNA PVT1 triggers cyto-protective autophagy and promotes pancreatic ductal adenocarcinoma development via the miR-20a-5p/ULK1 axis. Mol Cancer, 2018, 17(1): 98.
31. Yuan CL, Li H, Zhu L, et al. Aberrant expression of long noncoding RNA PVT1 and its diagnostic and prognostic significance in patients with gastric cancer. Neoplasma, 2016, 63(3): 442-449.
32. Ding J, Li D, Gong M, et al. Expression and clinical significance of the long non-coding RNA PVT1 in human gastric cancer. Onco Targets Ther, 2014, 7: 1625-1630.
33. Li Y, Song S, Pizzi MP, et al. LncRNA PVT1 is a poor prognosticator and can be targeted by PVT1 antisense oligos in gastric adenocarcinoma. Cancers (Basel), 2020, 12(10): 2995.
34. Zhao J, Du P, Cui P, et al. LncRNA PVT1 promotes angiogenesis via activating the STAT3/VEGFA axis in gastric cancer. Oncogene, 2018, 37(30): 4094-4109.
35. Kong R, Zhang EB, Yin DD, et al. Long noncoding RNA PVT1 indicates a poor prognosis of gastric cancer and promotes cell proliferation through epigenetically regulating p15 and p16. Mol Cancer, 2015, 14: 82.
36. Niu J, Song X, Zhang X. Regulation of lncRNA PVT1 on miR-125 in metastasis of gastric cancer cells. Oncol Lett, 2020, 19(2): 1261-1266.
37. Luo Z, Cao P. Long noncoding RNA PVT1 promotes hepatoblastoma cell proliferation through activating STAT3. Cancer Manag Res, 2019, 11: 8517-8527.
38. Gou X, Zhao X, Wang Z. Long noncoding RNA PVT1 promotes hepatocellular carcinoma progression through regulating miR-214. Cancer Biomark, 2017, 20(4): 511-519.
39. Lan T, Yan X, Li Z, et al. Long non-coding RNA PVT1 serves as a competing endogenous RNA for miR-186-5p to promote the tumorigenesis and metastasis of hepatocellular carcinoma. Tumour Biol, 2017, 39(6): 1010428317705338.
40. Wang F, Yuan JH, Wang SB, et al. Oncofetal long noncoding RNA PVT1 promotes proliferation and stem cell-like property of hepatocellular carcinoma cells by stabilizing NOP2. Hepatology, 2014, 60(4): 1278-1290.
41. 陈昌娜, 于红刚. 长链非编码RNA PVT1在肝癌组织中的表达与临床意义. 现代生物医学进展, 2019, 19(16): 3110-3114.
42. Ding C, Yang Z, Lv Z, et al. Long non-coding RNA PVT1 is associated with tumor progression and predicts recurrence in hepatocellular carcinoma patients. Oncol Lett, 2015, 9(2): 955-963.
43. Guo J, Hao C, Wang C, et al. Long noncoding RNA PVT1 modulates hepatocellular carcinoma cell proliferation and apoptosis by recruiting EZH2. Cancer Cell Int, 2018, 18: 98.
44. Yang L, Peng X, Jin H, et al. Long non-coding RNA PVT1 promotes autophagy as ceRNA to target ATG3 by sponging microRNA-365 in hepatocellular carcinoma. Gene, 2019, 697: 94-102.
45. 吴大平, 吴焕良, 郑文宏, 等. 长链非编码 RNA PVT1 和 miR-30 d-5 p 在肝内胆管癌组织中的表达及其与预后相关性分析. 现代肿瘤医学, 2020, 28(16): 2833-2837.
46. Xu MD, Wang Y, Weng W, et al. A positive feedback loop of lncRNA- PVT1 and FOXM1 facilitates gastric cancer growth and invasion. Clin Cancer Res, 2017, 23(8): 2071-2080.
47. Guo K, Yao J, Yu Q, et al. The expression pattern of long non-coding RNA PVT1 in tumor tissues and in extracellular vesicles of colorectal cancer correlates with cancer progression. Tumour Biol, 2017, 39(4): 1010428317699122.

Chinese Journal of Evidence-Based Medicine

Association between PVT1 expression and digestive system tumors: a systematic review

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