Expression of long non-coding RNA FoxP4-AS1 in papillary thyroid carcinoma and its relationship with lymph node metastasis_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

TANG Rui ¹ , YANG Huifang ¹ , GAO Qingjun ² , LUO Xue ^1,2 , CHEN Xinghong ¹ ,  ZHAO Daiwei ³

1. Clinical Medicine College of Cuizhou Medical University, Guiyang 550004, P. R. China;
2. Department of Thyroid Surgery, Affiliated Hospital of Guizhou Medical University, Guiyang 550004, P. R. China;
3. Department of General Surgery, The Sencond Affiliated Hospital of Guizhou Medical University, Kaili, Guizhou 556000, P. R. China;

Corresponding author：

ZHAO Daiwei, Email: zhaodw@hotmail.com

Keywords：

papillary thyroid carcinoma; long non-coding RNA; FoxP4-AS1; lymph node metastasis; risk prediction

DOI：

10.7507/1007-9424.202101002

Video：

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Objective To investigate relationship of long non-coding RNA FoxP4-AS1 expression with lymph node metastasis (LNM) of papillary thyroid carcinoma (PTC).Methods Real time fluorescent quantitative polymerase chain reaction was used to detect the expression level of FoxP4-AS1 in 52 cases of PTC tissues and corresponding adjacent tissues, PTC cells (TPC-1, B-CPAP, K1), and normal thyroid follicular epithelial cells (Nthy-ori3-1). Univariate and multivariate analysis were used to identify the influencing factors of LNM in PTC. Receiver operating characteristic (ROC) curve was drawn to evaluate the predictive value of influencing factors of LNM in PTC.Results The expression level of FoxP4-AS1 in the PTC tissues was significantly decreased as compared with the corresponding adjacent tissues (t=7.898, P<0.001), which in the different cells had statistical difference (F=29.866, P<0.001): expression levels in the TPC-1 and K1 cells were lower than Nthy-ori3-1 cells (P<0.05) and in the B-CPAP cells and Nthy-ori3-1 cells had no statistical difference (P>0.05) by multiple comparisons. Univariate analysis showed that the extraglandular invasion (χ²=4.205, P=0.040)and low expression of FoxP4-AS1 (χ²=7.144, P=0.008) were the influencing factors of LNM in PTC. Binary logistic regression analysis showed that extraglandular invasion [OR=9.455, 95%CI (1.120, 79.835), P=0.039] and low expression ofFoxP4-AS1[OR=5.437, 95%CI (1.488, 19.873), P=0.010] were risk factors for LNM of PTC. The area under the ROC curve ofFoxP4-AS1,extraglandular invasion alone, and combination of the two were 0.679, 0.656, and 0.785, respectively.Conclusions FoxP4-AS1 is down-regulated in PTC. Low level of FoxP4-AS1 is a risk factor for LNM of PTC. Combined detection of expression level of FoxP4-AS1 and extraglandular invasion has a high predictive value for LNM of PTC.

Citation： TANG Rui, YANG Huifang, GAO Qingjun, LUO Xue, CHEN Xinghong, ZHAO Daiwei. Expression of long non-coding RNA FoxP4-AS1 in papillary thyroid carcinoma and its relationship with lymph node metastasis. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(5): 566-570. doi: 10.7507/1007-9424.202101002 Copy

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2.	La Vecchia C, Malvezzi M, Bosetti C, et al. Thyroid cancer mortality and incidence: a global overview. Int J Cancer, 2015, 136(9): 2187-2195.
3.	吕春艳, 廖曼各, 张丽林, 等. 甲状腺乳头状癌颈部淋巴结转移的临床评估进展. 肿瘤学杂志, 2018, 24(4): 297-302.
4.	郭灵敏, 冯伟兆, 李林株, 等. 甲状腺乳头状癌组织中 p-Akt 及 VEGF-C 的表达及临床意义. 中国现代医生, 2020, 58(26): 12-15, 19.
5.	田文, 郗洪庆. 分化型甲状腺癌外科诊疗进展及展望. 中国实用外科杂志, 2020, 40(1): 78-82.
6.	熊雄, 焉正庆, 张爱军. 长链非编码 RNA CBR3-AS1 在乳腺癌中的表达及其功能. 中国普通外科杂志, 2019, 28(11): 1379-1385.
7.	Niu X, Yang B, Liu F, et al. LncRNA HOXA11-AS promotes OSCC progression by sponging miR-98-5p to upregulate YBX2 expression. Biomed Pharmacother, 2020, 121: 109623.
8.	姚林, 谭望, 杨发才, 等. 长链非编码 RNA POU6F2-AS2 在人胃癌组织中的表达及临床意义. 中国普外基础与临床杂志, 2019, 26(5): 563-567.
9.	贺钰斌, 朱丹. 钙化性主动脉瓣疾病发病机制的研究进展. 中国胸心血管外科临床杂志, 2018, 25(2): 171-176.
10.	何璐, 李彦林, 王国梁, 等. 长链非编码 RNA 在骨关节炎软骨损伤中的调控作用. 中国修复重建外科杂志, 2020, 34(11): 1486-1491.
11.	张洋, 郭海, 马莉, 等. 长链非编码 RNA MALAT1 吸附微小 RNA-124 调控 MSCs 成骨分化的实验研究. 中国修复重建外科杂志, 2020, 34(2): 240-245.
12.	张世杰, 张田利, 童翔, 等. 非编码 RNA 在肺纤维化中作用机制的研究进展. 华西医学, 2021, 36(1): 91-96.
13.	侯婉婷, 唐秋琳, 毕锋. 肾透明细胞癌中 lncRNA 和 miRNA 差异表达及相关 ceRNA 调控网络的分析研究. 生物医学工程学杂志, 2019, 36(2): 267-273.
14.	陈舒泽, 于正桐, 王梓鸿, 等. 长链非编码 RNA 中 INK4 基因座中反义非编码 RNA 在糖尿病视网膜病变中的研究现状. 中华眼底病杂志, 2020, 36(1): 78-81.
15.	王凡, 李培, 许芳, 等. 特发性肺间质纤维化中长链非编码 RNA 及转录因子的生物信息学挖掘. 中国呼吸与危重监护杂志, 2020, 19(6): 554-562.
16.	陈凤惟, 张成, 董慧, 等. 慢性间歇低氧上调心肌 lncRNA MALAT1 及相关分子的表达. 中国呼吸与危重监护杂志, 2018, 17(4): 377-382.
17.	龙勃, 展昊, 杜恒锐, 等. 长链非编码 RNA 高表达与胃癌预后不良相关性的 Meta 分析. 中国循证医学杂志, 2018, 18(3): 286-293.
18.	Li J, Lian Y, Yan C, et al. Long non-coding RNA FOXP4-AS1 is an unfavourable prognostic factor and regulates proliferation and apoptosis in colorectal cancer. Cell Prolif, 2017, 50(1): e12312.
19.	Wang D, Bai T, Chen G, et al. Upregulation of long non-coding RNA FOXP4-AS1 and its regulatory network in hepatocellular carcinoma. Onco Targets Ther, 2019, 12: 7025-7038.
20.	Bhaijee F, Nikiforov YE. Molecular analysis of thyroid tumors. Endocr Pathol, 2011, 22(3): 126-133.
21.	杨敏, 王昌敏. 甲状腺乳头状癌差异表达 lnc RNA 的筛选与分析. 新疆医科大学, 2020: 4-5.
22.	Zhang CL, Geng CH, Jian JJ, et al. Correlations of ultrasound and pathological features of thyroid carcinoma with TC-1 mRNA and protein expression. Eur Rev Med Pharmacol Sci, 2019, 23(8): 3440-3446.
23.	金海龙, 张毅, 潘炯. 淋巴结转移率与甲状腺乳头状癌患者术后复发及预后的相关性. 中国综合临床, 2019, 35(1): 14-17.
24.	Lopez-Pajares V. Long non-coding RNA regulation of gene expression during differentiation. Pflugers Arch, 2016, 468(6): 971-981.
25.	Serghiou S, Kyriakopoulou A, Ioannidis JP. Long noncoding RNAs as novel predictors of survival in human cancer: a systematic review and meta-analysis. Mol Cancer, 2016, 15(1): 50-63.
26.	Aune TM, Spurlock CF. Long non-coding RNAs in innate and adaptive immunity. Virus Res, 2016, 212: 146-160.
27.	Yoon JH, Kim J, Gorospe M. Long noncoding RNA turnover. Biochimie, 2015, 117: 15-21.
28.	张冬雪, 刘欣, 陈振文, 等. 长链非编码 RNA GAS8-AS1 在甲状腺微小乳头状癌中的表达特点及临床意义分析. 中华内分泌代谢杂志, 2017, 33(8): 687-692.
29.	Zhang J, Du Y, Zhang X, et al. Downregulation of BANCR promotes aggressiveness in papillary thyroid cancer via the MAPK and PI3K pathways. J Cancer, 2018, 9(7): 1318-1328.
30.	刘玲, 钱潇潇, 宋斌, 等. lncRNA TCONS-00020455 及 TCONS-00020457 在甲状腺乳头状癌中的表达及意义. 南京医科大学学报(自然科学版), 2019, 39(3): 332-337.
31.	Gao H, Sun X, Wang H, et al. Long noncoding RNA SNHG22 increases ZEB1 expression via competitive binding with microRNA-429 to promote the malignant development of papillary thyroid cancer. Cell Cycle, 2020, 19(10): 1186-1199.
32.	Yang L, Ge D, Chen X, et al. FOXP4-AS1 participates in the development and progression of osteosarcoma by downregulating LATS1 via binding to LSD1 and EZH2. Biochem Biophys Res Commun, 2018, 502(4): 493-500.
33.	Chen RY, Ju Q, Feng LM, et al. The carcinogenic complex lncRNA FOXP4-AS1/EZH2/LSD1 accelerates proliferation, migration and invasion of gastric cancer. Eur Rev Med Pharmacol Sci, 2019, 23(19): 8371-8376.
34.	Wu XC, Xiao Y, Zhou Y, et al. LncRNA FOXP4-AS1 is activated by PAX5 and promotes the growth of prostate cancer by sequestering miR-3184-5p to upregulate FOXP4. Cell Death Dis, 2019, 10(7): 472.
35.	Zhao J, Yang T, Li L. LncRNA FOXP4-AS1 is involved in cervical cancer progression via regulating miR-136-5p/CBX4 axis. Onco Targets Ther, 2020, 13: 2347-2355.
36.	宋慧胜, 邱惠思, 吴华振, 等. 特异性蛋白 1 (SP1) 上调 FOXP4-AS1 促进结直肠癌细胞增殖. 中国生物化学与分子生物学报, 2019, 35(3): 304-309.
37.	Li Y, Li T, Yang Y, et al. YY1-induced upregulation of FOXP4-AS1 and FOXP4 promote the proliferation of esophageal squamous cell carcinoma cells. Cell Biol Int, 2020, 44(7): 1447-1457.
38.	Liu XG, Xu H, Chen M, et al. Identify potential clinical significance of long noncoding RNA forkhead box P4 antisense RNA 1 in patients with early stage pancreatic ductal adenocarcinoma. Cancer Med, 2020, 9(6): 2062-2076.
39.	Zhong LK, Zhou J, He X, et al. Long non-coding RNA FOXP4-AS1 acts as an adverse prognostic factor and regulates proliferation and apoptosis in nasopharyngeal carcinoma. Eur Rev Med Pharmacol Sci, 2020, 24(15): 8008-8016.

1. Kitahara CM, Sosa JA. The changing incidence of thyroid cancer. Nat Rev Endocrinol, 2016, 12(11): 646-653.
2. La Vecchia C, Malvezzi M, Bosetti C, et al. Thyroid cancer mortality and incidence: a global overview. Int J Cancer, 2015, 136(9): 2187-2195.
3. 吕春艳, 廖曼各, 张丽林, 等. 甲状腺乳头状癌颈部淋巴结转移的临床评估进展. 肿瘤学杂志, 2018, 24(4): 297-302.
4. 郭灵敏, 冯伟兆, 李林株, 等. 甲状腺乳头状癌组织中 p-Akt 及 VEGF-C 的表达及临床意义. 中国现代医生, 2020, 58(26): 12-15, 19.
5. 田文, 郗洪庆. 分化型甲状腺癌外科诊疗进展及展望. 中国实用外科杂志, 2020, 40(1): 78-82.
6. 熊雄, 焉正庆, 张爱军. 长链非编码 RNA CBR3-AS1 在乳腺癌中的表达及其功能. 中国普通外科杂志, 2019, 28(11): 1379-1385.
7. Niu X, Yang B, Liu F, et al. LncRNA HOXA11-AS promotes OSCC progression by sponging miR-98-5p to upregulate YBX2 expression. Biomed Pharmacother, 2020, 121: 109623.
8. 姚林, 谭望, 杨发才, 等. 长链非编码 RNA POU6F2-AS2 在人胃癌组织中的表达及临床意义. 中国普外基础与临床杂志, 2019, 26(5): 563-567.
9. 贺钰斌, 朱丹. 钙化性主动脉瓣疾病发病机制的研究进展. 中国胸心血管外科临床杂志, 2018, 25(2): 171-176.
10. 何璐, 李彦林, 王国梁, 等. 长链非编码 RNA 在骨关节炎软骨损伤中的调控作用. 中国修复重建外科杂志, 2020, 34(11): 1486-1491.
11. 张洋, 郭海, 马莉, 等. 长链非编码 RNA MALAT1 吸附微小 RNA-124 调控 MSCs 成骨分化的实验研究. 中国修复重建外科杂志, 2020, 34(2): 240-245.
12. 张世杰, 张田利, 童翔, 等. 非编码 RNA 在肺纤维化中作用机制的研究进展. 华西医学, 2021, 36(1): 91-96.
13. 侯婉婷, 唐秋琳, 毕锋. 肾透明细胞癌中 lncRNA 和 miRNA 差异表达及相关 ceRNA 调控网络的分析研究. 生物医学工程学杂志, 2019, 36(2): 267-273.
14. 陈舒泽, 于正桐, 王梓鸿, 等. 长链非编码 RNA 中 INK4 基因座中反义非编码 RNA 在糖尿病视网膜病变中的研究现状. 中华眼底病杂志, 2020, 36(1): 78-81.
15. 王凡, 李培, 许芳, 等. 特发性肺间质纤维化中长链非编码 RNA 及转录因子的生物信息学挖掘. 中国呼吸与危重监护杂志, 2020, 19(6): 554-562.
16. 陈凤惟, 张成, 董慧, 等. 慢性间歇低氧上调心肌 lncRNA MALAT1 及相关分子的表达. 中国呼吸与危重监护杂志, 2018, 17(4): 377-382.
17. 龙勃, 展昊, 杜恒锐, 等. 长链非编码 RNA 高表达与胃癌预后不良相关性的 Meta 分析. 中国循证医学杂志, 2018, 18(3): 286-293.
18. Li J, Lian Y, Yan C, et al. Long non-coding RNA FOXP4-AS1 is an unfavourable prognostic factor and regulates proliferation and apoptosis in colorectal cancer. Cell Prolif, 2017, 50(1): e12312.
19. Wang D, Bai T, Chen G, et al. Upregulation of long non-coding RNA FOXP4-AS1 and its regulatory network in hepatocellular carcinoma. Onco Targets Ther, 2019, 12: 7025-7038.
20. Bhaijee F, Nikiforov YE. Molecular analysis of thyroid tumors. Endocr Pathol, 2011, 22(3): 126-133.
21. 杨敏, 王昌敏. 甲状腺乳头状癌差异表达 lnc RNA 的筛选与分析. 新疆医科大学, 2020: 4-5.
22. Zhang CL, Geng CH, Jian JJ, et al. Correlations of ultrasound and pathological features of thyroid carcinoma with TC-1 mRNA and protein expression. Eur Rev Med Pharmacol Sci, 2019, 23(8): 3440-3446.
23. 金海龙, 张毅, 潘炯. 淋巴结转移率与甲状腺乳头状癌患者术后复发及预后的相关性. 中国综合临床, 2019, 35(1): 14-17.
24. Lopez-Pajares V. Long non-coding RNA regulation of gene expression during differentiation. Pflugers Arch, 2016, 468(6): 971-981.
25. Serghiou S, Kyriakopoulou A, Ioannidis JP. Long noncoding RNAs as novel predictors of survival in human cancer: a systematic review and meta-analysis. Mol Cancer, 2016, 15(1): 50-63.
26. Aune TM, Spurlock CF. Long non-coding RNAs in innate and adaptive immunity. Virus Res, 2016, 212: 146-160.
27. Yoon JH, Kim J, Gorospe M. Long noncoding RNA turnover. Biochimie, 2015, 117: 15-21.
28. 张冬雪, 刘欣, 陈振文, 等. 长链非编码 RNA GAS8-AS1 在甲状腺微小乳头状癌中的表达特点及临床意义分析. 中华内分泌代谢杂志, 2017, 33(8): 687-692.
29. Zhang J, Du Y, Zhang X, et al. Downregulation of BANCR promotes aggressiveness in papillary thyroid cancer via the MAPK and PI3K pathways. J Cancer, 2018, 9(7): 1318-1328.
30. 刘玲, 钱潇潇, 宋斌, 等. lncRNA TCONS-00020455 及 TCONS-00020457 在甲状腺乳头状癌中的表达及意义. 南京医科大学学报(自然科学版), 2019, 39(3): 332-337.
31. Gao H, Sun X, Wang H, et al. Long noncoding RNA SNHG22 increases ZEB1 expression via competitive binding with microRNA-429 to promote the malignant development of papillary thyroid cancer. Cell Cycle, 2020, 19(10): 1186-1199.
32. Yang L, Ge D, Chen X, et al. FOXP4-AS1 participates in the development and progression of osteosarcoma by downregulating LATS1 via binding to LSD1 and EZH2. Biochem Biophys Res Commun, 2018, 502(4): 493-500.
33. Chen RY, Ju Q, Feng LM, et al. The carcinogenic complex lncRNA FOXP4-AS1/EZH2/LSD1 accelerates proliferation, migration and invasion of gastric cancer. Eur Rev Med Pharmacol Sci, 2019, 23(19): 8371-8376.
34. Wu XC, Xiao Y, Zhou Y, et al. LncRNA FOXP4-AS1 is activated by PAX5 and promotes the growth of prostate cancer by sequestering miR-3184-5p to upregulate FOXP4. Cell Death Dis, 2019, 10(7): 472.
35. Zhao J, Yang T, Li L. LncRNA FOXP4-AS1 is involved in cervical cancer progression via regulating miR-136-5p/CBX4 axis. Onco Targets Ther, 2020, 13: 2347-2355.
36. 宋慧胜, 邱惠思, 吴华振, 等. 特异性蛋白 1 (SP1) 上调 FOXP4-AS1 促进结直肠癌细胞增殖. 中国生物化学与分子生物学报, 2019, 35(3): 304-309.
37. Li Y, Li T, Yang Y, et al. YY1-induced upregulation of FOXP4-AS1 and FOXP4 promote the proliferation of esophageal squamous cell carcinoma cells. Cell Biol Int, 2020, 44(7): 1447-1457.
38. Liu XG, Xu H, Chen M, et al. Identify potential clinical significance of long noncoding RNA forkhead box P4 antisense RNA 1 in patients with early stage pancreatic ductal adenocarcinoma. Cancer Med, 2020, 9(6): 2062-2076.
39. Zhong LK, Zhou J, He X, et al. Long non-coding RNA FOXP4-AS1 acts as an adverse prognostic factor and regulates proliferation and apoptosis in nasopharyngeal carcinoma. Eur Rev Med Pharmacol Sci, 2020, 24(15): 8008-8016.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Expression of long non-coding RNA FoxP4-AS1 in papillary thyroid carcinoma and its relationship with lymph node metastasis

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