PLIC11 drives lung cancer progression through regulating the YY1/PIWIL4 axis
Yuyao Zhu
Department of Pathology, Eastern Hepatobiliary Surgery Hospital, The Second Military Medical University, Shanghai, China
Search for more papers by this authorBing Chen
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorHongyu Pan
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorLei Sun
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Tao Yu
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Correspondence Tao Yu, Department of Oncology, Shanghai Medical College, Fudan University, No. 270, Dongan Rd, Shanghai 200032, China.
Email: [email protected]
Search for more papers by this authorYuyao Zhu
Department of Pathology, Eastern Hepatobiliary Surgery Hospital, The Second Military Medical University, Shanghai, China
Search for more papers by this authorBing Chen
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorHongyu Pan
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorLei Sun
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Tao Yu
Fudan University Shanghai Cancer Center, Shanghai Medical College, Fudan University, Shanghai, China
Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China
Correspondence Tao Yu, Department of Oncology, Shanghai Medical College, Fudan University, No. 270, Dongan Rd, Shanghai 200032, China.
Email: [email protected]
Search for more papers by this authorYuyao Zhu and Bing Chen contributed equally to this study.
Abstract
Lung cancer is the leading cause of cancer related deaths worldwide. Nonsmall cell lung cancers (NSCLC), the most common histological type of lung cancer, are known to be less well characterized. Long noncoding RNAs are a new class of cancer regulators. Here, we aimed to investigate the effect of lncRNA PLIC11 in NSCLC progression. In our study, we found that PLIC11 was upregulated in lung cancer, particularly in metastatic lung cancer tissues. Overexpression of PLIC11 enhanced cell proliferation, migration, and metastasis in vitro and in vivo. Mechanically, PLIC11 could interact with YY1 and promote PIWIL4 expression by transcription activation. Therefore, PLIC11 upregulation is a potential indicator of aggressive lung cancer, Silencing of PLIC11 has great potential therapeutic strategy in NSCLC.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing not applicable to this article as no data sets were generated or analyzed during the current study.
Supporting Information
| Filename | Description |
|---|---|
| mc23496-sup-0001-Supplemental_Information.docx1.2 MB | Supporting information. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Bray 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.
- 2Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018; 68(1): 7-30.
- 3Avasarala SK, Rickman OB. Endobronchial therapies for diagnosis, staging, and treatment of lung cancer. Surg Clin North Am. 2022; 102(3): 393-412.
- 4Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2021. CA Cancer J Clin. 2021; 71(1): 7-33.
- 5Djebali S, Davis CA, Merkel A, et al. Landscape of transcription in human cells. Nature. 2012; 489(7414): 101-108.
- 6Herman AB, Tsitsipatis D, Gorospe M. Integrated lncRNA function upon genomic and epigenomic regulation. Mol Cell. 2022; 82(12): 2252-2266.
- 7Bhat SA, Ahmad SM, Mumtaz PT, et al. Long non-coding RNAs: mechanism of action and functional utility. Non-coding RNA Res. 2016; 1(1): 43-50.
- 8Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discov. 2011; 1(5): 391-407.
- 9Cabili MN, Trapnell C, Goff L, et al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011; 25(18): 1915-1927.
- 10Lee JT. Epigenetic regulation by long noncoding RNAs. Science. 2012; 338(6113): 1435-1439.
- 11Ulitsky I, Bartel DP. lincRNAs: genomics, evolution, and mechanisms. Cell. 2013; 154(1): 26-46.
- 12Ørom UA, Derrien T, Beringer M, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010; 143(1): 46-58.
- 13Luo S, Lu JY, Liu L, et al. Divergent lncRNAs regulate gene expression and lineage differentiation in pluripotent cells. Cell Stem Cell. 2016; 18(5): 637-652.
- 14Dimitrova N, Zamudio JR, Jong RM, et al. LincRNA-p21 activates p21 in cis to promote polycomb target gene expression and to enforce the G1/S checkpoint. Mol Cell. 2014; 54(5): 777-790.
- 15Brown CJ, Ballabio A, Rupert JL, et al. A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome. Nature. 1991; 349(6304): 38-44.
- 16Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013; 152(6): 1308-1323.
- 17Jia D, Yan M, Wang X, et al. Development of a highly metastatic model that reveals a crucial role of fibronectin in lung cancer cell migration and invasion. BMC Cancer. 2010; 10(1): 364.
- 18Llères D, Imaizumi Y, Feil R. Exploring chromatin structural roles of non-coding RNAs at imprinted domains. Biochem Soc Trans. 2021; 49(4): 1867-1879.
- 19Subhramanyam CS, Cao Q, Wang C, Heng ZSL, Zhou Z, Hu Q. Role of PIWI-like 4 in modulating neuronal differentiation from human embryonal carcinoma cells. RNA Biol. 2020; 17(11): 1613-1624.
- 20Wang Z, Liu N, Shi S, Liu S, Lin H. The role of PIWIL4, an argonaute family protein, in breast cancer. J Biol Chem. 2016; 291(20): 10646-10658.
- 21Wang Y, Liu Y, Shen X, et al. The PIWI protein acts as a predictive marker for human gastric cancer. Int J Clin Exp Pathol. 2012; 5(4): 315-325.
- 22Juliano C, Wang J, Lin H. Uniting germline and stem cells: the function of piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet. 2011; 45: 447-469. doi:10.1146/annurev-genet-110410-132541
- 23Lee JH, Schütte D, Wulf G, et al. Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Gen. 2006; 15(2): 201-211.
- 24Su C, Ren ZJ, Wang F, Liu M, Li X, Tang H. PIWIL4 regulates cervical cancer cell line growth and is involved in down-regulating the expression of p14ARF and p53. FEBS Lett. 2012; 586(9): 1356-1362.
- 25Gao XQ, Zhang YH, Liu F, et al. The piRNA CHAPIR regulates cardiac hypertrophy by controlling METTL3-dependent N6-methyladenosine methylation of Parp10 mRNA. Nature Cell Biol. 2020; 22(11): 1319-1331.
- 26Martinez-Ruiz GU, Morales-Sanchez A, Pacheco-Hernandez AF. Roles played by YY1 in embryonic, adult and cancer stem cells. Stem Cell Rev Rep. 2021; 17(5): 1590-1606.
- 27Gordon S, Akopyan G, Garban H, Bonavida B. Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene. 2006; 25(8): 1125-1142.
- 28Deng Z, Cao P, Wan MM, Sui G. Yin Yang 1: a multifaceted protein beyond a transcription factor. Transcription. 2010; 1(2): 81-84.
- 29Shi Y, Lee JS, Galvin KM. Everything you have ever wanted to know about Yin Yang 1. Biochimica et Biophysica Acta (BBA)-Reviews on Cancer. 1997; 1332(2): F49-F66.
- 30Yao YL, Yang WM, Seto E. Regulation of transcription factor YY1 by acetylation and deacetylation. Mol Cell Biol. 2001; 21(17): 5979-5991.
- 31Wai DCC, Shihab M, Low JKK, Mackay JP. The zinc fingers of YY1 bind single-stranded RNA with low sequence specificity. Nucleic Acids Res. 2016; 44(19): gkw590.
- 32Zhang XC, Gu AP, Zheng CY, et al. YY1/LncRNA GAS5 complex aggravates cerebral ischemia/reperfusion injury through enhancing neuronal glycolysis. Neuropharmacology. 2019; 158:107682.
- 33Yang D, Ding J, Wang Y, et al. YY1-PVT1 affects trophoblast invasion and adhesion by regulating mTOR pathway-mediated autophagy. J Cell Physiol. 2020; 235(10): 6637-6646.
- 34Zhou L, Sun K, Zhao Y, et al. Linc-YY1 promotes myogenic differentiation and muscle regeneration through an interaction with the transcription factor YY1. Nat Commun. 2015; 6(1):10026.
