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.	呂春艷, 廖曼各, 張麗林, 等. 甲狀腺乳頭狀癌頸部淋巴結轉移的臨床評估進展. 腫瘤學雜志, 2018, 24(4): 297-302.
4.	郭靈敏, 馮偉兆, 李林株, 等. 甲狀腺乳頭狀癌組織中 p-Akt 及 VEGF-C 的表達及臨床意義. 中國現代醫生, 2020, 58(26): 12-15, 19.
5.	田文, 郗洪慶. 分化型甲狀腺癌外科診療進展及展望. 中國實用外科雜志, 2020, 40(1): 78-82.
6.	熊雄, 焉正慶, 張愛軍. 長鏈非編碼 RNA CBR3-AS1 在乳腺癌中的表達及其功能. 中國普通外科雜志, 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, 譚望, 楊發才, 等. 長鏈非編碼 RNA POU6F2-AS2 在人胃癌組織中的表達及臨床意義. 中國普外基礎與臨床雜志, 2019, 26(5): 563-567.
9.	賀鈺斌, 朱丹. 鈣化性主動脈瓣疾病發病機制的研究進展. 中國胸心血管外科臨床雜志, 2018, 25(2): 171-176.
10.	何璐, 李彥林, 王國梁, 等. 長鏈非編碼 RNA 在骨關節炎軟骨損傷中的調控作用. 中國修復重建外科雜志, 2020, 34(11): 1486-1491.
11.	張洋, 郭海, 馬莉, 等. 長鏈非編碼 RNA MALAT1 吸附微小 RNA-124 調控 MSCs 成骨分化的實驗研究. 中國修復重建外科雜志, 2020, 34(2): 240-245.
12.	張世杰, 張田利, 童翔, 等. 非編碼 RNA 在肺纖維化中作用機制的研究進展. 華西醫學, 2021, 36(1): 91-96.
13.	侯婉婷, 唐秋琳, 畢鋒. 腎透明細胞癌中 lncRNA 和 miRNA 差異表達及相關 ceRNA 調控網絡的分析研究. 生物醫學工程學雜志, 2019, 36(2): 267-273.
14.	陳舒澤, 于正桐, 王梓鴻, 等. 長鏈非編碼 RNA 中 INK4 基因座中反義非編碼 RNA 在糖尿病視網膜病變中的研究現狀. 中華眼底病雜志, 2020, 36(1): 78-81.
15.	王凡, 李培, 許芳, 等. 特發性肺間質纖維化中長鏈非編碼 RNA 及轉錄因子的生物信息學挖掘. 中國呼吸與危重監護雜志, 2020, 19(6): 554-562.
16.	陳鳳惟, 張成, 董慧, 等. 慢性間歇低氧上調心肌 lncRNA MALAT1 及相關分子的表達. 中國呼吸與危重監護雜志, 2018, 17(4): 377-382.
17.	龍勃, 展昊, 杜恒銳, 等. 長鏈非編碼 RNA 高表達與胃癌預后不良相關性的 Meta 分析. 中國循證醫學雜志, 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.	楊敏, 王昌敏. 甲狀腺乳頭狀癌差異表達 lnc RNA 的篩選與分析. 新疆醫科大學, 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.	金海龍, 張毅, 潘炯. 淋巴結轉移率與甲狀腺乳頭狀癌患者術后復發及預后的相關性. 中國綜合臨床, 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.	張冬雪, 劉欣, 陳振文, 等. 長鏈非編碼 RNA GAS8-AS1 在甲狀腺微小乳頭狀癌中的表達特點及臨床意義分析. 中華內分泌代謝雜志, 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.	劉玲, 錢瀟瀟, 宋斌, 等. lncRNA TCONS-00020455 及 TCONS-00020457 在甲狀腺乳頭狀癌中的表達及意義. 南京醫科大學學報(自然科學版), 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.	宋慧勝, 邱惠思, 吳華振, 等. 特異性蛋白 1 (SP1) 上調 FOXP4-AS1 促進結直腸癌細胞增殖. 中國生物化學與分子生物學報, 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. 呂春艷, 廖曼各, 張麗林, 等. 甲狀腺乳頭狀癌頸部淋巴結轉移的臨床評估進展. 腫瘤學雜志, 2018, 24(4): 297-302.
4. 郭靈敏, 馮偉兆, 李林株, 等. 甲狀腺乳頭狀癌組織中 p-Akt 及 VEGF-C 的表達及臨床意義. 中國現代醫生, 2020, 58(26): 12-15, 19.
5. 田文, 郗洪慶. 分化型甲狀腺癌外科診療進展及展望. 中國實用外科雜志, 2020, 40(1): 78-82.
6. 熊雄, 焉正慶, 張愛軍. 長鏈非編碼 RNA CBR3-AS1 在乳腺癌中的表達及其功能. 中國普通外科雜志, 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, 譚望, 楊發才, 等. 長鏈非編碼 RNA POU6F2-AS2 在人胃癌組織中的表達及臨床意義. 中國普外基礎與臨床雜志, 2019, 26(5): 563-567.
9. 賀鈺斌, 朱丹. 鈣化性主動脈瓣疾病發病機制的研究進展. 中國胸心血管外科臨床雜志, 2018, 25(2): 171-176.
10. 何璐, 李彥林, 王國梁, 等. 長鏈非編碼 RNA 在骨關節炎軟骨損傷中的調控作用. 中國修復重建外科雜志, 2020, 34(11): 1486-1491.
11. 張洋, 郭海, 馬莉, 等. 長鏈非編碼 RNA MALAT1 吸附微小 RNA-124 調控 MSCs 成骨分化的實驗研究. 中國修復重建外科雜志, 2020, 34(2): 240-245.
12. 張世杰, 張田利, 童翔, 等. 非編碼 RNA 在肺纖維化中作用機制的研究進展. 華西醫學, 2021, 36(1): 91-96.
13. 侯婉婷, 唐秋琳, 畢鋒. 腎透明細胞癌中 lncRNA 和 miRNA 差異表達及相關 ceRNA 調控網絡的分析研究. 生物醫學工程學雜志, 2019, 36(2): 267-273.
14. 陳舒澤, 于正桐, 王梓鴻, 等. 長鏈非編碼 RNA 中 INK4 基因座中反義非編碼 RNA 在糖尿病視網膜病變中的研究現狀. 中華眼底病雜志, 2020, 36(1): 78-81.
15. 王凡, 李培, 許芳, 等. 特發性肺間質纖維化中長鏈非編碼 RNA 及轉錄因子的生物信息學挖掘. 中國呼吸與危重監護雜志, 2020, 19(6): 554-562.
16. 陳鳳惟, 張成, 董慧, 等. 慢性間歇低氧上調心肌 lncRNA MALAT1 及相關分子的表達. 中國呼吸與危重監護雜志, 2018, 17(4): 377-382.
17. 龍勃, 展昊, 杜恒銳, 等. 長鏈非編碼 RNA 高表達與胃癌預后不良相關性的 Meta 分析. 中國循證醫學雜志, 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. 楊敏, 王昌敏. 甲狀腺乳頭狀癌差異表達 lnc RNA 的篩選與分析. 新疆醫科大學, 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. 金海龍, 張毅, 潘炯. 淋巴結轉移率與甲狀腺乳頭狀癌患者術后復發及預后的相關性. 中國綜合臨床, 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. 張冬雪, 劉欣, 陳振文, 等. 長鏈非編碼 RNA GAS8-AS1 在甲狀腺微小乳頭狀癌中的表達特點及臨床意義分析. 中華內分泌代謝雜志, 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. 劉玲, 錢瀟瀟, 宋斌, 等. lncRNA TCONS-00020455 及 TCONS-00020457 在甲狀腺乳頭狀癌中的表達及意義. 南京醫科大學學報(自然科學版), 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. 宋慧勝, 邱惠思, 吳華振, 等. 特異性蛋白 1 (SP1) 上調 FOXP4-AS1 促進結直腸癌細胞增殖. 中國生物化學與分子生物學報, 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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