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C/D box small nucleolar RNA SNORD104 promotes endometrial cancer by regulating the 2'-O-methylation of PARP1

Bingfeng Lu¹, Xi Chen¹, Xin Liu¹

¹Department of Obstetrics and Gynecology, Department of Gynecologic Oncology Research Office, Guangdong Provincial Key Laboratory for Major Obstetric Diseases, The Third Affiliated Hospital of Guangzhou Medical University, No. 63 Duobao Raod, Liwan District, Guangzhou, 510150, Guangdong, People's Republic of China.

Journal of Translational Medicine

|December 24, 2022

Abstract

Background:

Small nucleolar RNAs (snoRNAs) are dysregulated in many cancers, although their exact role in tumor genesis and progression remains unclear.

Methods:

The expression profiles of snoRNAs in endometrial cancer (EC) tissues were analyzed using data from The Cancer Genome Atlas, and SNORD104 was identified as an upregulated snoRNA in EC. The tumorigenic role of SNORD104 in EC was established in CCK8, colony formation, EdU, apoptosis, Transwell, and in vivo xenograft experiments. The molecular mechanisms of SNORD104 were analyzed by RNA immunoprecipitation (RIP), Nm-seq, RTL-P assay, RNA stability assay, qRT-PCR, and western blotting.

Results:

Antisense oligonucleotide (ASO)-mediated knockdown of SNORD104 in Ishikawa cells significantly inhibited their proliferation, colony formation ability, migration, and invasion in vitro and increased apoptosis. On the other hand, overexpression of SNORD104 promoted EC growth in vivo and in vitro. RIP assay showed that SNORD104 binds to the 2'-O-methyltransferase fibrillarin (FBL), and according to the results of Nm-seq and RTL-P assay, SNORD104 upregulated PARP1 (encoding poly (ADP-ribose) polymerase 1) 2'-O-methylation. The binding of FBL to PARP1 mRNA was also verified by RIP assay. Furthermore, SNORD104 expression was positively correlated with PARP1 expression in EC tissues. In the presence of actinomycin D, SNORD104 increased the stability of PARP1 mRNA and promoted its nuclear localization. Finally, silencing FBL or PARP1 in the HEC1B cells overexpressing SNORD104 inhibited their proliferative and clonal capacities and increased apoptosis rates.

Conclusions:

SNORD104 enhances PARP1 mRNA stability and translation in the EC cells by upregulating 2'-O-methylation and promotes tumor growth.

Insights

Small nucleolar RNA SNORD104 promotes endometrial cancer growth by increasing PARP1 mRNA stability and translation. Silencing SNORD104 inhibits tumor progression and increases apoptosis, revealing a potential therapeutic target.

Area of Science:

Oncology
Molecular Biology
RNA Biology

Background:

Small nucleolar RNAs (snoRNAs) are implicated in various cancers, but their specific roles in tumor development are not fully understood.
Endometrial cancer (EC) exhibits dysregulated snoRNA expression, necessitating investigation into individual snoRNA functions.

Purpose of the Study:

To investigate the role of SNORD104 in endometrial cancer pathogenesis.
To elucidate the molecular mechanisms by which SNORD104 influences EC progression.

Main Methods:

Analysis of The Cancer Genome Atlas (TCGA) data for snoRNA expression profiles in EC.
In vitro and in vivo experiments assessing the functional impact of SNORD104 on EC cells (proliferation, migration, invasion, apoptosis).
Molecular mechanism studies including RNA immunoprecipitation (RIP), Nm-seq, RNA stability assays, and correlation analyses.

Main Results:

SNORD104 was identified as significantly upregulated in EC tissues.
SNORD104 knockdown inhibited EC cell proliferation, migration, and invasion, while promoting apoptosis.
SNORD104 was found to bind Fibrillarin (FBL) and upregulate 2'-O-methylation of PARP1 mRNA, enhancing its stability and promoting EC growth.

Conclusions:

SNORD104 promotes endometrial cancer progression by enhancing PARP1 mRNA stability and translation through 2'-O-methylation.
SNORD104 represents a potential therapeutic target for endometrial cancer treatment.

Read full analysis

Keywords:

2ʹ-O-methylation Endometrial cancer Fibrillarin PARP1 SNORD104

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