PRMT1 promotes the proliferation and metastasis of gastric cancer cells by recruiting MLXIP for the transcriptional activation of the β-catenin pathway

Feng Wang; Shitong Chen; Shihan Peng; Xujun Zhou; Houyi Tang; Hanghua Liang; Xi Zhong; He Yang; Xiaoxue Ke; MuHan Lü; Hongjuan Cui

doi:10.1016/j.gendis.2023.02.006

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PRMT1 promotes the proliferation and metastasis of gastric cancer cells by recruiting MLXIP for the transcriptional activation of the β-catenin pathway

Full-length article | 更新时间：2024-02-04

- PRMT1 promotes the proliferation and metastasis of gastric cancer cells by recruiting MLXIP for the transcriptional activation of the β-catenin pathway
- Genes & Diseases Vol. 1, Issue 6, Pages: 2622-2638(2023)
- 作者机构：
  
  1. State Key Laboratory of Silkworm Genome Biology, Southwest University,Chongqing,China,400716
  2. Cancer Center, Medical Research Institute, Southwest University,Chongqing,China,400716
  3. Department of Gastroenterology, The Affiliated Hospital of Southwest Medical University, 25 Taiping Street, Jiangyang District,Sichuan,Luzhou,China,646000
  4. Jinfeng Laboratory,Chongqing,China,401329
- 作者简介：
- 基金信息：
- DOI：10.1016/j.gendis.2023.02.006
  CLC：
- Published：2023，
  
  Published Online：1 November 2023，
扫描看全文
Feng Wang, Shitong Chen, Shihan Peng, et al. PRMT1 promotes the proliferation and metastasis of gastric cancer cells by recruiting MLXIP for the transcriptional activation of the β-catenin pathway. [J]. Genes & Diseases 1(6):2622-2638(2023)
DOI：

Feng Wang, Shitong Chen, Shihan Peng, et al. PRMT1 promotes the proliferation and metastasis of gastric cancer cells by recruiting MLXIP for the transcriptional activation of the β-catenin pathway. [J]. Genes & Diseases 1(6):2622-2638(2023) DOI： 10.1016/j.gendis.2023.02.006.

摘要

Abstract

Protein arginine methyltransferase 1 (PRMT1)

a type I PRMT

is overexpressed in gastric cancer (GC) cells. To elucidate the function of PRMT1 in GC

PRMT1 expression in HGC-27 and MKN-45 cells was knocked down by short hairpin RNA (shRNA) or inhibited by PRMT1 inhibitors (AMI-1 or DCLX069)

which resulted in inhibition of GC cell proliferation

migration

invasion

and tumorigenesis

in vitro

and

in vivo

. MLX-interacting protein (MLXIP) and Kinectin 1 (KTN1) were identified as PRMT1-binding proteins. PRMT1 recruited MLXIP to the promoter of β-catenin

which induced β-catenin transcription and activated the β-catenin signaling pathway

promoting GC cell migration and metastasis. Furthermore

KTN1 inhibited the K48-linked ubiquitination of PRMT1 by decreasing the interaction between TRIM48 and PRMT1. Collectively

our findings reveal a mechanism by which PRMT1 promotes cell proliferation and metastasis mediated by the β-catenin signaling pathway.

关键词

Keywords

β-catenin signaling pathwayGastric cancerPRMT1Transcriptional regulationUbiquitination

references

1 S. Choi, S. Park, H. Kim, et al.Gastric cancer: mechanisms, biomarkers, and therapeutic approaches Biomedicines, 10 (3) (2022), p. 543

2 E.C. Smyth, M. Nilsson, H.I. Grabsch, et al.Gastric cancer Lancet, 396 (10251) (2020), pp. 635-648

3 M. Yaghoobi, J. McNabb-Baltar, R. Bijarchi, et al.What is the quantitative risk of gastric cancer in the first-degree relatives of patients? A meta-analysis World J Gastroenterol, 23 (13) (2017), pp. 2435-2442

4 M. HatakeyamaMalignant Helicobacter pylori-associated diseases: gastric cancer and MALT lymphoma Adv Exp Med Biol, 1149 (2019), pp. 135-149

5 I.J. Majewski, I. Kluijt, A. Cats, et al.An α-E-catenin (CTNNA1) mutation in hereditary diffuse gastric cancer J Pathol, 229 (4) (2013), pp. 621-629

6 T. Akiyama, C. Sudo, H. Ogawara, et al.The product of the human c-erbB-2 gene: a 185-kilodalton glycoprotein with tyrosine kinase activity Science, 232 (4758) (1986), pp. 1644-1646

7 E. Van Cutsem, X. Sagaert, B. Topal, et al.Gastric cancer Lancet, 388 (10060) (2016), pp. 2654-2664

8 B.M. Lorton, D. ShechterCellular consequences of arginine methylation Cell Mol Life Sci, 76 (15) (2019), pp. 2933-2956

9 R.S. Blanc, S. RichardArginine methylation: the coming of age Mol Cell, 65 (1) (2017), pp. 8-24

10 M.T. Bedford, S.G. ClarkeProtein arginine methylation in mammals: who, what, and why Mol Cell, 33 (1) (2009), pp. 1-13

11 H. Kim, Z.A. RonaiPRMT5 function and targeting in cancer Cell Stress, 4 (8) (2020), pp. 199-215

12 J. Jarrold, C.C. DaviesPRMTs and arginine methylation: cancer's best-kept secret? Trends Mol Med, 25 (11) (2019), pp. 993-1009

13 F. Wang, J. Zhang, H. Tang, et al.Nup54-induced CARM1 nuclear importation promotes gastric cancer cell proliferation and tumorigenesis through transcriptional activation and methylation of Notch 2 Oncogene, 41 (2) (2022), pp. 246-259

14 W. An, J. Kim, R.G. RoederOrdered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53 Cell, 117 (6) (2004), pp. 735-748

15 L.M. Liu, Q. Tang, X. Hu, et al.Arginine methyltransferase PRMT1 regulates p53 activity in breast cancer Life, 11 (8) (2021), p. 789

16 O. Jackson-Weaver, N. Ungvijanpunya, Y. Yuan, et al.PRMT1-p53 pathway controls epicardial EMT and invasion Cell Rep, 31 (10) (2020), Article 107739

17 Z. Li, D. Wang, J. Lu, et al.Methylation of EZH2 by PRMT1 regulates its stability and promotes breast cancer metastasis Cell Death Differ, 27 (12) (2020), pp. 3226-3242

18 L. Zhang, N.T. Tran, H. Su, et al.Cross-talk between PRMT1-mediated methylation and ubiquitylation on RBM15 controls RNA splicing Elife, 4 (2015), Article e07938

19 X.K. Yin, Y.L. Wang, F. Wang, et al.PRMT1 enhances oncogenic arginine methylation of NONO in colorectal cancer Oncogene, 40 (7) (2021), pp. 1375-1389

20 B. Yao, T. Gui, X. Zeng, et al.PRMT1-mediated H4R3me2a recruits SMARCA4 to promote colorectal cancer progression by enhancing EGFR signaling Genome Med, 13 (1) (2021), p. 58

21 F. Wang, D. Zhang, J. Mao, et al.Morusin inhibits cell proliferation and tumor growth by down-regulating c-Myc in human gastric cancer Oncotarget, 8 (34) (2017), pp. 57187-57200

22 B. Altan, T. Yokobori, M. Ide, et al.Nuclear PRMT1 expression is associated with poor prognosis and chemosensitivity in gastric cancer patients Gastric Cancer, 19 (3) (2016), pp. 789-797

23 Y. Zhang, D. Wang, M. Zhang, et al.Protein arginine methyltransferase 1 coordinates the epithelial-mesenchymal transition/proliferation dichotomy in gastric cancer cells Exp Cell Res, 362 (1) (2018), pp. 43-50

24 S. Suresh, S. Huard, A. Brisson, et al.PRMT1 regulates EGFR and Wnt signaling pathways and is a promising target for combinatorial treatment of breast cancer Cancers, 14 (2) (2022), p. 306

25 Y. Yang, M.T. BedfordProtein arginine methyltransferases and cancer Nat Rev Cancer, 13 (1) (2013), pp. 37-50

26 Q. Zhao, G. Rank, Y.T. Tan, et al.PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing Nat Struct Mol Biol, 16 (3) (2009), pp. 304-311

27 Y. Hirata, K. Katagiri, K. Nagaoka, et al.TRIM48 promotes ASK1 activation and cell death through ubiquitination-dependent degradation of the ASK1-negative regulator PRMT1 Cell Rep, 21 (9) (2017), pp. 2447-2457

28 T. Huang, Y. Yang, X. Song, et al.PRMT6 methylation of RCC1 regulates mitosis, tumorigenicity, and radiation response of glioblastoma stem cells Mol Cell, 81 (6) (2021), pp. 1276-1291 e9

29 S.J. Hernandez, D.M. Dolivo, T. DominkoPRMT8 demonstrates variant-specific expression in cancer cells and correlates with patient survival in breast, ovarian and gastric cancer Oncol Lett, 13 (3) (2017), pp. 1983-1989

30 X. He, Y. Zhu, Y.C. Lin, et al.PRMT1-mediated FLT3 arginine methylation promotes maintenance of FLT3-ITD+ acute myeloid leukemia Blood, 134 (6) (2019), pp. 548-560

31 Z. Li, D. Wang, W. Wang, et al.Macrophages-stimulated PRMT1-mediated EZH2 methylation promotes breast cancer metastasis Biochem Biophys Res Commun, 533 (4) (2020), pp. 679-684

32 C. Song, T. Chen, L. He, et al.PRMT1 promotes pancreatic cancer growth and predicts poor prognosis Cell Oncol, 43 (1) (2020), pp. 51-62

33 D. Hanahan, R.A. WeinbergHallmarks of cancer: the next generation Cell, 144 (5) (2011), pp. 646-674

34 X. Cheng, X. Xu, D. Chen, et al.Therapeutic potential of targeting the Wnt/β-catenin signaling pathway in colorectal cancer Biomed Pharmacother, 110 (2019), pp. 473-481

35 A. Gajos-Michniewicz, M. CzyzWNT signaling in melanoma Int J Mol Sci, 21 (14) (2020), p. 4852

36 C.Y. Wei, M.X. Zhu, Y.W. Yang, et al.Downregulation of RNF128 activates Wnt/β-catenin signaling to induce cellular EMT and stemness via CD44 and CTTN ubiquitination in melanoma J Hematol Oncol, 12 (1) (2019), p. 21

37 J. Xue, Y. Chen, Y. Wu, et al.Tumour suppressor TRIM33 targets nuclear β-catenin degradation Nat Commun, 6 (2015), p. 6156

38 M. Ranes, M. Zaleska, S. Sakalas, et al.Reconstitution of the destruction complex defines roles of AXIN polymers and APC in β-catenin capture, phosphorylation, and ubiquitylation Mol Cell, 81 (16) (2021), pp. 3246-3261 e11

39 P. Richards, S. Ourabah, J. Montagne, et al.MondoA/ChREBP: the usual suspects of transcriptional glucose sensing; Implication in pathophysiology Metabolism, 70 (2017), pp. 133-151

40 N. Mejhert, L. Kuruvilla, K.R. Gabriel, et al.Partitioning of MLX-family transcription factors to lipid droplets regulates metabolic gene expression Mol Cell, 77 (6) (2020), pp. 1251-1264 e9

41 Y. Lu, Y. Li, Q. Liu, et al.MondoA-thioredoxin-interacting protein axis maintains regulatory T-cell identity and function in colorectal cancer microenvironment Gastroenterology, 161 (2) (2021), pp. 575-591 e16

42 B.R. Wilde, D.E. AyerInteractions between Myc and MondoA transcription factors in metabolism and tumourigenesis Br J Cancer, 113 (11) (2015), pp. 1529-1533

43 P.A. Carroll, D. Diolaiti, L. McFerrin, et al.Deregulated Myc requires MondoA/Mlx for metabolic reprogramming and tumorigenesis Cancer Cell, 27 (2) (2015), pp. 271-285

44 J. Pan, N.X. Chao, Y.Y. Zhang, et al.Upregulating KTN1 promotes hepatocellular carcinoma progression J Cancer, 12 (16) (2021), pp. 4791-4809

45 L. Gao, S. Chen, M. Hong, et al.Kinectin 1 promotes the growth of triple-negative breast cancer via directly co-activating NF-kappaB/p65 and enhancing its transcriptional activity Signal Transduct Targeted Ther, 6 (1) (2021), p. 250

46 J. Ma, S. Ma, Y. Zhang, et al.Kinectin1 depletion promotes EGFR degradation via the ubiquitin-proteosome system in cutaneous squamous cell carcinoma Cell Death Dis, 12 (11) (2021), p. 995

47 Y. Zhang, L. Gao, S. Ma, et al.MALAT1-KTN1-EGFR regulatory axis promotes the development of cutaneous squamous cell carcinoma Cell Death Differ, 26 (10) (2019), pp. 2061-2073

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