<p>Long Non-Coding Small Nucleolar RNA Host Genes (SNHGs) in Endocrine-Related Cancers</p>

Yuan Qin; Wei Sun; Zhihong Wang; Wenwu Dong; Liang He; Ting Zhang; Hao Zhang

doi:10.2147/OTT.S267140

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Review

Long Non-Coding Small Nucleolar RNA Host Genes (SNHGs) in Endocrine-Related Cancers

Authors Qin Y, Sun W, Wang Z, Dong W , He L, Zhang T, Zhang H

Received 11 June 2020

Accepted for publication 17 July 2020

Published 5 August 2020 Volume 2020:13 Pages 7699—7717

DOI https://doi.org/10.2147/OTT.S267140

Checked for plagiarism Yes

Review by Single anonymous peer review

Peer reviewer comments 2

Editor who approved publication: Dr William C. Cho

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Yuan Qin ,^* Wei Sun ,^* Zhihong Wang, Wenwu Dong, Liang He, Ting Zhang, Hao Zhang

Department of Thyroid Surgery, The First Hospital of China Medical University, Shenyang 110001, Liaoning Province, People’s Republic of China

*These authors contributed equally to this work

Correspondence: Hao Zhang
Department of Thyroid Surgery, The First Hospital of China Medical University, 155 Nanjing Bei Street, Shenyang, Liaoning 110001, People’s Republic of China
Email [email protected]

Abstract: Long non-coding RNAs (lncRNAs) are emerging regulators of a diverse range of biological processes through various mechanisms. Genome-wide association studies of tumor samples have identified several lncRNAs, which act as either oncogenes or tumor suppressors in various types of cancers. Small nucleolar RNAs (snoRNAs) are predominantly found in the nucleolus and function as guide RNAs for the processing of transcription. As the host genes of snoRNAs, lncRNA small nucleolar RNA host genes (SNHGs) have been shown to be abnormally expressed in multiple cancers and can participate in cell proliferation, tumor progression, metastasis, and chemoresistance. Here, we review the biological functions and emerging mechanisms of SNHGs involved in the development and progression of endocrine-related cancers including thyroid cancer, breast cancer, pancreatic cancer, ovarian cancer and prostate cancer.

Keywords: endocrine, cancers, lncRNA, SNHG

Introduction

Long non-coding RNAs (lncRNAs, >200 nucleotides in length) are emerging regulators of gene transcription.¹ The human genome estimated to encode >28,000 lncRNAs,² but only 15,778 lncRNAs are annotated in the current GENECODE version 27.³ Therefore, more lncRNAs are yet to be discovered. Moreover, the known lncRNAs have not been studied in depth.

Accumulating evidence suggests lncRNAs play key roles in the development and progression of several cancers, acting as either oncogenes or tumor suppressors.⁴ LncRNAs can regulate transcription, translation, protein modification, and the formation of RNA-protein or protein-protein complexes, depending on the cellular location.⁵ For example, lncRNAs primarily located in the nucleus are involved in transcriptional regulation and mRNA processing, while cytoplasmic lncRNAs play roles in modulating mRNA translation by competing with proteins or in miRNA-mediated mRNA decoy.^5,6

Small nucleolar RNAs (snoRNAs, 60–300 nucleotides in length) are more well-characterized than lncRNAs and are predominantly found in the nucleolus.⁷ Most snoRNAs function as guide RNAs for the post-transcriptional modification of ribosomal RNAs and some spliceosomal RNAs, with some involved in the nucleolytic processing of the original rRNA transcript.⁸ As shown in Figure 1, the majority of snoRNAs are encoded (hosted) in the introns of protein-coding and non-protein-coding genes, termed small nucleolar RNA host genes (SNHGs).^9–11 Primary RNA transcripts of host genes (including all exons and introns with their snoRNAs) are cut into different exons and introns. Exons are then re-spliced and function in the cytoplasm, while the introns are further processed into snoRNAs and play roles in the nucleolus.

Figure 1 The synthetic pathway of snoRNAs.

Currently, there are 22 members of SNHG family (SNHG1 to SNHG22) that have been shown to regulate proliferation, apoptosis, invasion, and migration in multiple cancers, including endocrine-related cancers (as summarized in Tables 1 and 2). These 22 SNHGs have diverse activities and mechanisms of action. For example, SNHG1 has been shown to promote colorectal cancer cell growth by modulating histone methylation of gene promoters of the Kruppel Like Factor 2 (KLF2, a member of the KLF family, also exerts tumor-suppressive roles) and the cyclin-dependent kinase 4 inhibitor B (CDKN2B, a tumor suppressor).¹² SNHG1 can also act as a sponge for miR-154-5p to upregulate expression of G1/S-specific cyclin-D2 (CCND2, which is involved in cell cycle progression).¹² Meanwhile, SNHG13 serves as a competing endogenous RNA (ceRNA) of miR-34a-5p, leading to the derepression of Jagged 1 (JAG1) expression, which eventually triggers resistance to docetaxel in prostate cancer.¹³

Table 1 Characteristics of SNHG Members

Table 2 SNHG Members in Endocrine-Related Cancers

This review aims to provide an overview on the current understanding of the regulation and function of SNHGs in endocrine-related cancers that arise from the endocrine glands or neuroendocrine tissues, including thyroid cancer, breast cancer, pancreatic cancer, ovarian cancer, and prostate cancer.¹⁴

Thyroid Cancer

Thyroid cancer is the most common malignancy of the endocrine system with enormous heterogeneity in terms of morphological features and prognosis.¹⁵ Although the majority of cases of thyroid cancer tend to be biologically indolent and have an excellent prognosis, some are associated with more aggressive clinical behavior.¹⁶

SNHG1 may act as an oncogene in thyroid cancer by competing with miR-199a-5p and upregulating the expression of its target gene, the transcription factor (TF) SP1. In turn, SP1 targets the promoter region of SNHG1 and promote its transcription, forming a positive feedback loop to promote cancer cell proliferation and invasion.¹⁷ Conversely, low expression of SNHG2, also known as growth arrest specific transcript 5 (GAS5), is associated with poor prognosis of patients with thyroid cancer.¹⁸ Mechanistically, GAS5 acts as a sponge for miR-222-3p, thereby modulating the expression of the phosphatase and tensin homolog (PTEN), leading to PTEN/protein kinase B (AKT) pathway activation and the suppression of thyroid cancer cell proliferation.¹⁹

SNHG7 is also markedly upregulated in thyroid cancer samples, with high SNHG7 expression associated with shorter survival times.²⁰ Indeed, SNHG7 knockdown leads to a suppression of thyroid cancer cell proliferation and migration, and induction of apoptosis via downregulating the acyl-CoA synthetase long chain family member 1 (ACSL1) and the brain-derived neurotrophic factor (BDNF).^21,22 In addition, bioinformatics analysis showed SNHG7 was associated with the processes of “protein translation”, “viral life cycle”, “RNA processing”, “mRNA splicing”, “histone ubiquitination”, “endoplasmic reticulum-to-Golgi vesicle-mediated transport”, “sister chromatid cohesion”, “DNA damage checkpoint regulation”, “translation”, and “the spliceosome”, suggesting further research directions for this lncRNA.²⁰

SNHG12 is also upregulated (by 3.8-fold) in papillary thyroid carcinoma (PTC) tissues compared to normal adjacent tissue samples.²³ High SNHG12 was associated with poorer progression in PTC in terms of tumor node metastasis (TNM) staging and lymph node metastasis (LNM).²⁴ SNHG12 likely acts as a sponge for miR-16-5p, thereby inducing PTC cell proliferation, migration, and invasion, as well as inhibiting apoptosis.²⁵ SNHG12 also promotes the proliferation and migration of PTC cells via the Wnt/β-catenin signaling pathway.²³ Meanwhile, SNHG13, also known as differentiation antagonizing non-protein coding RNA (DANCR), acts as a tumor suppressor in PTC: downregulation of DANCR is associated with more aggressive clinical features of PTC.²⁶ DANCR is also a potential biomarker for PTC diagnosis, showing a sensitivity of 85.29% and a specificity of 66.18%.²⁶

The role of SNHG15 in thyroid cancer remains controversial. SNHG15 is upregulated in human PTC tissues and cell lines compared to controls, and was associated with gender, larger tumor size, LNM, advanced TNM stage, and poorer overall survival (OS).²⁷ Meanwhile, SNHG15 downregulation attenuated cell proliferation, migration, and epithelial–mesenchymal transition (EMT) in PTC cells, as well as inducing apoptosis.²⁷ Mechanistically, SNHG15 acts as a sponge for miR-200a-3p, thereby upregulating the Yes-associated protein 1 (YAP1) signaling pathway.²⁷ Alternatively, another study showed SNHG15 was downregulated in thyroid cancer tissues and cell lines and suppressed tumor progression, indicating SNHG15 may act as a tumor suppressor.²⁸ Moreover, inhibition of SNHG15 by miR-510-5p promoted cell proliferation, migration, and invasion in thyroid cancer.²⁹ These diverse functions of SNHG15 found in different studies may reflect the different subtypes of thyroid cancer; however, further research is required.

Finally, SNHG16, which functions as an endogenous sponge for miR-497, was upregulated in both PTC tissues and cell lines and shown to induce proliferation, migration, and invasion of thyroid cancer cells, while inhibiting apoptosis.³⁰ High expression of SNHG16 was also positively associated with advanced TNM stage and LNM.³⁰

In summary, SNHG1, GAS5, SNHG7, SNHG12, DANCR, SNHG15, and SNHG16 all appear to play essential roles in thyroid cancer; although the function of SNHG15 requires further confirmation.

Breast Cancer

Breast cancer is the most commonly diagnosed cancer worldwide and the leading cause of cancer-related death for women.³¹ Although advances in early detection and cancer therapeutics have led to a decrease in mortality rates, breast cancer remains a significant public health concern. Some classes of breast cancer, such as triple-negative breast cancer (characterized by a lack of expression of the progesterone receptor, estrogen receptor, and Her-2), have a poor prognosis.³² Many lncRNAs have been implicated in breast cancer development in recent years, which may eventually lead to better outcomes for these patients.³³

The downregulation of SNHG1 can suppress the proliferation and invasion of breast cancer cells by regulating miR-382.³⁴ In addition, SNHG1 may inhibit the differentiation of regulatory T cells, promote miR-448 expression, and reduce indoleamine 2,3 dioxygenase (IDO) levels in breast cancer.³⁵ Therefore, SNHG1 may be a useful target in breast cancer treatment.

GAS5 was first reported to be a tumor suppressor in breast cancer in 2009.³⁶ Since then, studies have shown low GAS5 expression is closely related to a more aggressive tumor phenotype, enhanced proliferation, and attenuated apoptosis in breast cancer cells.^37–39 GAS5 can bind to miR-196a-5p, thereby partially alleviating its tumor-promoting effects, including invasion and downstream forkhead box O1 (FOXO1)/phosphatidylinositol 3-kinase (PI3K)/AKT signal pathway activation.³⁷ Notch-1 also promotes breast cancer cell proliferation by downregulating GAS5.⁴⁰ GAS5 can also act as a sponge for miR-23a to promote autophagy via the GAS5-miR-23a-ATG3 axis in breast cancer.³⁸ Moreover, in drug-resistant breast cancer cells, GAS5 overexpression increases chemosensitivity (eg to trastuzumab, imatinib, paclitaxel, cisplatin, among others), especially in triple-negative breast cancer cells.^39,41-46 Another study showed miR-221/222 suppresses GAS5 expression and enhances tumor growth in a mouse model of breast cancer xenografts.⁴⁷ Moreover, lower plasma GAS5 levels were found in patients with a high Ki67 proliferation index before surgery and in those with LNM after surgery.⁴⁸ Finally, bioinformatics analysis showed GAS5 plays a role in “proliferation” and the “cell cycle”, although the molecular mechanisms related to these regulatory pathways are unclear.⁴⁹

There is evidence that lncRNA secreted in exosomes from cancer cells can regulate gene expression and signaling pathways in other niche cells. For example, breast cancer-derived cancer-associated fibroblasts can secrete increased amounts of SNHG3 than healthy breast tissue cells, which in turn promotes the growth of breast cancer cells by regulating miR-330-5p/Pyruvate Kinase M1/M2 (PKM).⁵⁰ SNHG3 can also act as a sponge for miR-384/hepatoma-derived growth factor (HDGF) to drive breast cancer cell proliferation, migration, and invasion.⁵¹

SNHG5 is an oncogene and acts as a sponge for miR-154-5p, reducing its ability to repress proliferating cell nuclear antigen (PCNA), thus promoting breast cancer proliferation, cell cycle progression, and inhibiting apoptosis.⁵² SNHG6 was also found to be highly expressed in breast cancer tissues and cell lines, and is associated with poorer clinicopathologic features.⁵³ Indeed, SNHG6 knockdown inhibits breast cancer cell proliferation, migration, invasion, and G1 cell cycle arrest by acting as a sponge for miR-26a-5p, which regulates expression of the vasodilator-stimulated phosphoprotein (VASP)⁵⁴ and mitogen-activated protein kinase 6 (MAPK6).⁵⁵

The expression of SNHG7 is also upregulated in breast cancer tissues and cells compared to healthy tissues, with high SNHG7 expression strongly related to tumor stage, distant metastasis, LNM, and OS.^56–58 Knocking down SNHG7 inhibited breast cancer cell proliferation, invasion, and EMT.^56–58 Further mechanistic studies revealed SNHG7 could act as a sponge to repress miR-34a,⁵⁷ miR-186,⁵⁸ and miR-381,⁵⁶ thereby activating the Notch-1 pathway and glycolysis in breast cancer. Additionally, c-Myc (a TF) can bind to the SNHG7 promoter and positively regulate its expression in breast cancer.⁵⁹

Increased expression of SNHG12 has been observed in triple-negative breast cancer.⁶⁰ SNHG12 upregulation positively correlated with advanced tumor stage and size, and negatively correlated with OS.⁶⁰ SNHG12 is a direct transcriptional target of c-Myc, and the c-Myc-induced upregulation of SNHG12 enhances the proliferation of breast cancer cells and inhibits apoptosis.⁶⁰ SNHG12 may also promote the migration of breast cancer cells by regulating the expression of matrix metalloproteinase 13 (MMP13).⁶⁰

High DANCR levels can lead to shorter OS in triple-negative breast cancer, by acting as a sponge for miR-216a-5p and thereby promoting the proliferation and invasion of tumor cells.⁶¹ DANCR can mediate protein assembly and modification in triple-negative breast cancer. For example, DANCR can bind to the phosphorylation site of retinoid X receptor alpha (RXRA) and suppresses its interaction with the phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha (PIK3CA) promoter.⁶² This leads to the activation of the P13K/AKT pathway, which in turn, promotes the proliferation and growth of triple-negative breast cancer cells.⁶² DANCR may also participate in the enhancer of zeste homolog 2 (EHZ2)-mediated epigenetic repression of the suppressor of cytokine signaling 3 (SOCS3) in breast cancer cells.⁶³ Sha et al⁶⁴ proposed DANCR knockdown was associated with increased binding of EZH2 to the promoters of CD44 and ABCG2 (two triple-negative breast cancer stem cell markers), and the concomitant reduction of expression of these genes decreased cancer cell proliferation and invasion. Furthermore, nanoparticle-mediated RNAi of DANCR was shown to be an effective therapy for triple-negative breast cancer.⁶⁵

Upregulation of SNHG14 in breast cancer tissues may also promote cancer cell proliferation and invasion.⁶⁶ In particular, SNHG14 upregulates polyadenylate-binding protein 1 (PABPC1) expression by modulating H3K27 acetylation (H3K27ac) in the promoter of PABPC1 gene, resulting in the activation of the nuclear factor E2-related factor 2 (NRF2) signaling pathway, which is involved in cell defense and survival against chemotherapy drugs.⁶⁶ Besides histone methylation, acetylation is another important form of histone modification.

Indeed, exosomal SNHG14 was upregulated in trastuzumab-resistant human epidermal growth factor receptor 2 (HER2) breast cancer cells compared with parental breast cancer cells, and SNHG14 knockdown re-sensitized breast cancer cells to trastuzumab treatment.⁶⁷ These results indicate SNHG14 may be a promising therapeutic target for patients with HER2+ breast cancer. In addition, SNHG14 may enhance breast cancer cell proliferation and invasion by acting as a sponge for miR-193a-3p.⁶⁸

SNHG15 has also been shown to be highly expressed in breast cancer tissues and cell lines and is positively associated with larger tumor size, LNM, advanced TMN stage, and worse survival.^69,70 SNHG15 primarily acts as a sponge for miR-411-5p⁶⁹ and miR-211-3p,⁷⁰ leading to the proliferation, migration, and invasion of breast cancer cells. Additionally, SNHG15 knockdown enhances the cisplatin sensitivity of breast cancer cells by acting as a sponge for miR-381.⁷¹ Moreover, bioinformatics analysis showed SNHG16 might be associated with the prognosis of breast cancer.^72,73 In particular, SNHG16 may interact with miR-30a to regulate the expression of ribonucleoside-diphosphate reductase subunit M2 (RRM2)⁷⁴ and competitively bind miR-98 and the E2F Transcription Factor 5 (E2F5)⁷⁵ to promote the proliferation and invasion of breast cancer cells. Finally, SNHG17⁷⁶ and SNHG20⁷⁷ may also drive breast cancer progression by sponging miR-124-3p and miR-495, respectively.

In general, multiple SNHGs, including SNHG1, GAS5, SNHG3, SNHG5, SNHG6, SNHG7, SNHG12, DANCR, SNHG14, SNHG15, SNHG16 and SNHG20, play a role in breast cancer. Targeting SNHGs, especially the treatment of drug-resistant breast cancer, is the future research direction.

Pancreatic Cancer

Pancreatic cancer is one of the most devastating human tumors, with high invasiveness, early metastasis, lack of specific symptoms, and high mortality. According to the most recent statistical data, the 5-year survival of pancreatic cancer is 9%, which is the lowest among all types of cancers and continues to increase (by 0.3% per year) in men.⁷⁸ The high fatality rate in pancreatic cancer is attributed to late diagnosis and resistance to current therapies. Recent studies demonstrate lncRNAs are critical in the pathogenesis of pancreatic cancer and are therefore potential biomarkers or drug targets.⁷⁹

SNHG1 acts as an oncogene in pancreatic cancer and accelerates cancer cell growth.⁸⁰ In addition, SNHG1 overexpression can promote cyclin D1-mediated pancreatic cancer proliferation by regulating the cell cycle.⁸¹ Meanwhile, SNHG1 downregulation inhibits the proliferation, migration, and invasion of pancreatic cancer cells by suppressing the Notch-1 signaling pathway.⁸⁰ Similarly, SNHG1 downregulation inhibits the PI3K/AKT signaling pathway in pancreatic ductal adenocarcinoma (PDAC).⁸²

By acting as a sponge for miR-32-5p, GAS5 can promote the expression of PTEN and stop the activation of the PI3K/AKT signaling pathway, thereby inhibiting pancreatic cancer cell proliferation and survival.⁸³ GAS5 also inhibits the expression of the oncogene cyclin-dependent kinase 6 (CDK6), although the underlying mechanisms have not been determined.⁸⁴ Studies also show GAS5 reduces the chemoresistance of pancreatic cancer cells by downregulating miR-181c-5p and miR-221.^85,86

SNHG7 is highly expressed in pancreatic cancer tissues and positively correlates with reduced OS. Meanwhile, SNHG7 knockdown suppresses cell proliferation, migration, and invasion of pancreatic cancer cells by modulating the miR-342-3p/inhibitor of DNA binding 4 (ID4) axis.⁸⁷ Zhang et al⁸⁸ showed low expression of SNHG9 in pancreatic cancer tissues and serums, while those with high SNHG9 expression had significantly higher survival rates. This data indicates SNHG9 may be a novel prognostic marker for pancreatic cancer.

High DANCR expression correlates with vascular invasion, advanced T grade, LNM, and advanced TNM stage, and is an independent risk factor for poor OS and progression-free survival (PFS) in PDAC.^89,90 Mechanistically, DANCR acts as an miRNA sponge, affecting the miRNA-33a-5p/Anexelekto (AXL) axis,⁸⁹ the miRNA-33b/MMP16 axis,⁹¹ the miR-135a/NLRP3 axis,⁹² and the miR-214-5p/E2F2 axis⁹⁰ to promote cell proliferation, migration, invasion, and metastasis in pancreatic cancer.

The SNHG14 oncogene also potentiates pancreatic cancer cell proliferation through modulation of annexin A2 (ANXA2) expression by acting as a ceRNA for miR-613.⁹³ It also acts as a sponge for miR-10, thereby enhancing autophagy, which underlies the chemoresistance of PDAC cells to gemcitabine.^94,95 Finally, SNHG15 and SNHG16 are upregulated in pancreatic cancer samples and are associated with progression in pancreatic cancer patients.^96,97 SNHG15 may help repress P15 and KLF2 expression,⁹⁶ while SNHG16 promotes cell proliferation, migration, and invasion of pancreatic cancer by sponging miR-200a-3p⁹⁸ and miR-218-5p.⁹⁷ SNHG16 may also promote pancreatic cancer lipogenesis by directly regulating the miR-195/SREBP2 axis.⁹⁹

In short, many SNHGs have a significant predictive effect on the survival of pancreatic cancer patients, and can be used as a clinical prognostic marker in pancreatic cancer.

Ovarian Carcinoma

Ovarian cancer is the most lethal gynecological cancer in women globally.¹⁰⁰ Despite recent improvements in cytoreductive surgery and chemotherapy, the 5-year survival rate of ovarian cancer is still approximately 40–50% owing to its late diagnosis and the development of chemoresistance.⁷⁸ Therefore, understanding the molecular mechanisms of ovarian carcinogenesis may help improve diagnosis, therapy, and prevention.

Expression of SNHG1 is increased in human epithelial ovarian cancer tissues and cell lines compared to normal healthy tissues, and promotes the proliferation and invasion of ovarian carcinoma cells through the regulation of EMT and the Wnt/β-catenin pathway.^101,102 Meanwhile, GAS5 acts as a tumor suppressor and is expressed in low levels epithelial ovarian cancer samples.^103,104 Indeed, GAS5 expression correlates with prognosis in epithelial ovarian cancer, including International Federation of Gynecology and Obstetrics (FIGO) stage, histological type, OS, and disease-free survival (DFS).^103,104 In terms of its mechanism of action, GAS5 may block CCAAT/enhancer-binding protein beta (CEBPB)-mediated transcription of the growth/differentiation factor 15 (GD15), leading to decreased viability and increased apoptosis of ovarian cancer cells.¹⁰⁵ GAS5 may also suppress the proliferation of ovarian cancer cells by sponging miR-21¹⁰⁶ and miR-196a-5p,¹⁰⁷ which regulate sprouty homolog 2 (SPRY2) and homeobox A5 (HOXA5) expression, respectively. GAS5 is also implicated in inflammasome formation and pyroptosis, but the underlying mechanism is unclear.¹⁰⁸ Finally, GAS5 has been linked to chemoresistance; in particular, GAS5 overexpression control the expression of poly(ADP-ribose) polymerase 1 (PARP1) by recruiting the transcription factor E2F4 to its promoter, which subsequently affects the mitogen-activated protein kinase (MAPK) pathway activity, further enhance the cisplatin sensitivity of ovarian cancer cells.¹⁰⁹

Upregulation of SNHG3 expression is associated with poor prognosis in ovarian cancer (including FIGO stage and LNM) and promotes proliferation and invasion by activating the GSK3β/-catenin signaling pathway.¹¹⁰ Bioinformatics analysis has shown SNHG3 is related to energy metabolism in the “glycolysis”, “Kreb’s cycle”, and “oxidative phosphorylation” pathways, and to “drug resistance”.¹¹¹ Similarly, SNHG5 has been implicated in chemoresistance: paclitaxel-resistant ovarian cancer tissues and cell lines have lower levels of SNHG5, while SNHG5 overexpression can enhance paclitaxel sensitivity (likely by sponging miR-23a).¹¹²

SNHG12 is also upregulated in ovarian cancer tissues and enhances the proliferative and migratory capacity of cells via sponging miR-129 and upregulating expression of SOX4 (a TF).¹¹³ In addition, DANCR levels are higher in ovarian cancer patients with worse tumor stage and accompanied by metastatic loci.¹¹⁴ DANCR binds directly to miR-145 and regulates vascular endothelial growth factor (VEGF) expression.¹¹⁵ Indeed, knockdown of DANCR impairs ovarian tumor growth by inhibiting tumor angiogenesis.¹¹⁵ In addition, DANCR may enhance the proliferation, migration, and invasion capacities of ovarian cancer cells by upregulating expression of the insulin-like growth factor 2 (IGF2)¹¹⁶ and downregulating UPF1 RNA Helicase And ATPase (UPF1) expression.¹¹⁴

Like SNHG12, SNHG14 is highly expressed in ovarian cancer tissues and associated with poorer OS.^117,118 SNHG14 may promote ovarian cancer cell progression by sponging miR-125a-5p¹¹⁷ and miR-219a-5p,¹¹⁸ or directly regulating the expression of DiGeorge syndrome chromosomal region 8 (DGCR8).¹¹⁹ SNHG15 and SNHG16 may also serve as oncogenes in epithelial ovarian cancer. SNHG16 has been shown to promote the proliferation, invasion, and migration of cancer cells via activation of the PI3K/AKT signaling pathway,¹²⁰ while the role of SNHG15 is unclear.¹²¹ SNHG20 is also upregulated in ovarian cancer and is associated with shorter OS.¹²² SNHG20 knockdown suppresses Wnt/β-catenin signaling activity and EMT-associated gene expression, thereby inhibiting ovarian cancer cell proliferation, migration, and invasion.¹²³ Finally, the SNHG22 oncogene may regulate the miR-2467/Gal-1 axis to promote cisplatin- and paclitaxel-resistance of ovarian cancer cells.¹²⁴

In a word, compared with other SNHGs, GAS5 regulates the progression of ovarian cancer through various mechanisms, indicating its key role in the development of ovarian cancer.

Prostate Cancer

Prostate cancer is the most common malignancy in males and accounts for 10% of cancer-related deaths.⁷⁸ Androgen deprivation therapy (ADT) is the standard treatment for patients with biochemical recurrence after primary treatment, or with locally-advanced or metastatic disease. However, the majority of cancers will eventually acquire ADT resistance and progress to castration-resistant prostate cancer (CRPC).¹²⁵ Aberrantly expressed lncRNAs can be indicative of certain stages of prostate cancer progression, and may predict early progression or efficiently sustain tumor‐related signaling pathways. Thus, lncRNAs may be applicable for the diagnosis of prostate cancer, as well as being potential criteria in the choice of therapy and new therapeutic targets of CRPC.¹²⁶

SNHG1 upregulation in prostate cancer correlates with the Gleason score, T stage, and a short biochemical recurrence-free survival time.¹²⁷ SNHG1 may promote prostate cancer cell proliferation by regulating the miR-199a-3p/CDK7 axis¹²⁸ and the miR-377-3p/AKT2 axis.¹²⁹ Conversely, GAS5 levels are reduced in prostate cancer tissues and cell lines.^130–132 Low GAS5 levels are associated with prostate-specific antigen level, Gleason score, and pathological stage.^130–132

Most studies indicate that GAS5 inhibits the proliferation, migration, and invasion of prostate cancer cells, and promotes apoptosis.^130–132 In terms of its mechanism of action, GAS5 may act as a sponge for miR-103, which in turn, inactivates the AKT/mTOR signaling pathway, thus inhibiting prostate cancer cell proliferation.¹³¹ In addition, two single nucleotide polymorphisms (SNPs) located in the chromosomal segment of GAS5 (rs55829688 and rs145204276) can increase GAS5 expression,^133–135 and are associated with improved survival in prostate cancer.¹³³ Patients with prostate cancer and the GAS5 rs145204276 polymorphism are associated with a low risk of pathologic N stage and seminal vesicle invasion.¹³⁵ Furthermore, patients with prostate cancer aged >65 years who carry the GAS5 rs145204276 polymorphism show decreased risk of clinical T stage, pathologic N stage, and lymphovascular invasion.¹³⁵ Differential expression of GAS5 due to these SNPs likely affects the miR-21/programmed cell death 4 (PDCD4)/PTEN axis,¹³³ as well as the miR-1284/AKT¹³³ and miR-1284/high mobility group box 1 (HMGB1)¹³⁴ pathways. In addition, overexpression of miR-145 can upregulate GAS5 expression, although GAS5 overexpression (or silencing) has no effect on miR-145 levels.¹³²

Enhancing GAS5 expression may be particularly useful in androgen-sensitive prostate cancers.¹³⁶ Indeed, mTOR inhibitors enhance GAS5 transcript levels in androgen-sensitive prostate cancer cell lines but have no effect on androgen-independent cell lines (which exhibit low endogenous levels of GAS5).¹³⁶ As further evidence of its tumor-suppressing role, GAS5 is implicated in improving the radiosensitivity of prostate cancer cells. In particular, GAS5 can enhance the α-Solanine-induced radiosensitivity of prostate cancer cells by negatively regulating miR-18a.¹³⁷

Despite available evidence showing that GAS5 acts as a tumor suppressor, some studies report GAS5 may exist as an oncogene in prostate cancer. For example, Zhang and Chen et al.^138,139 found GAS5 expression was higher in prostate cancer tissues than normal healthy tissues in both public databases and human tissue samples. In addition, functional analysis showed GAS5 knockdown inhibited the proliferation and cell cycle progression of prostate cancer cells, while promoting apoptosis.¹³⁸ A bioinformatics analysis also showed high expression of GAS5 correlated with poorer DFS in prostate cancer, and other studies show GAS5 may be involved in regulating translational elongation, protein biosynthesis, transcription, protein translation, and proliferation.^138–140

SP1-mediated upregulation of SNHG4 can facilitate prostate cancer progression via the miR-377/zic family member 5 (ZIC5) axis.¹⁴¹ Similarly, SNHG6 overexpression was associated with shorter DFS in the Cancer Genome Atlas (TCGA) and Taylor datasets, with bioinformatics analysis revealing SNHG6 is associated with “translation”, “nuclear-transcribed mRNA catabolic processes”, “ribosomal RNA processing”, and “mRNA splicing”.¹⁴² SNHG7 is also significantly upregulated in prostate cancer tissue and cell lines,^143,144 and correlates with the Gleason score, bone metastasis, pelvic LNM, TNM stage, and OS.¹⁴⁵ In terms of its mechanism of action, SNHG7 knockdown was found to inhibit proliferation and promote CCND1-induced cell cycle arrest at the G0/G1 phase.¹⁴⁴ SNHG7 can also promote EMT via regulating miR-324-3p and WNT2B, an important protein in the Wnt signaling pathway.¹⁴³ Therefore, targeting the SNHG7/miR-324-p/WNT2B axis may represent a novel therapeutic strategy for prostate cancer treatment.

As SNHG12 acts as an oncogene, it may be a useful predictor of poor prognosis in prostate cancer. Indeed, a study showed SNHG12 acts as a sponge for miR-195 and can activate the Wnt/β-catenin signaling pathway.¹⁴⁶ SNHG12 can also promote cell viability and inhibit apoptosis and autophagy of prostate cancer cells via regulating the expression of the G1/S-specific cyclin-E1 (CCNE1) by sponging miR-195.¹⁴⁷ Bioinformatic analysis revealed higher expression of SNHG12 was enriched in the “P53 signaling pathway”, “cell cycle”, “regulation of cell migration”, “cellular metabolic process”, “gene expression”, and “Notch signaling pathway”, and that SNHG12 may target miR-133b.¹⁴⁸

The oncogene DANCR has also been shown to promote the invasion and migration of prostate cancer cells in vitro and the metastasis of tumor xenografts in nude mice.¹⁴⁹ Mechanistically, DANCR works synergistically with EZH2 to downregulate the expression of the tissue inhibitor of metalloproteinases (TIMP) 2/3.¹⁴⁹ Furthermore, downregulation of DANCR can increase the paclitaxel sensitivity of prostate cancer cells by negatively regulating the expression of miR-135a.¹⁵⁰ In addition, stimulation of the DANCR/miR-34a-5p axis enhanced docetaxel-resistance in prostate cancer via targeting JAG1, which in turn activates the Notch signaling pathway.¹³ Finally, SNHG14,¹⁵¹ SNHG15,¹⁵² and SNHG20¹⁵³ may all act as oncogenes in prostate cancer via targeting miR-613, miR-338-3p, and miR-6516-5p to promote cell proliferation, migration, and invasion.

In conclusion, SNHGs plays an important role in the process and embody diversified treatment strategies in prostate cancer, especially in CRPC.

Conclusion

This review highlights that the abnormal expression of SNHGs is significantly related to poor prognosis (eg TNM stage, LNM, OS, DFS) and function (eg proliferation, invasion, migration, apoptosis, autophagy, and chemoresistance) in multiple endocrine-related cancers. Some SNHGs played similar roles in different tumors. For example, SNHG1, SNHG3, SNHG4, SNHG6, SNHG7, SNHG12, SNHG14, SNHG16, SNHG17, SNHG20 and SNHG22 promotes tumor growth as oncogenes, while GAS5 and SNHG9 played the role of tumor suppressor genes. In addition, SNHG5, DANCR, SNHG15 played a dual role, which have attracted more scholars’ attention. SNHGs could regulate the tumor process via various mechanisms, including direct regulation (promotion or inhibition) (Figure 2A), binding and being activated by TFs, acting as a ceRNA, activating different signaling pathways (Figure 2B), and regulating promoter methylation (Figure 2C) or acetylation of downstream target genes (Figure 2D). Both methylation and acetylation were histone modifications and their mechanisms were similar. The difference between them was that they bound and modified different histones, and then promoted or inhibited the expression of downstream genes. However, the SNHGs described in this review are only just the tip of the iceberg, and further mechanistic will be required as more SNHG family members are uncovered.

Figure 2 Schematic diagram of the functional mechanism of SNHGs. (A) SNHGs can promote or inhibit expression of downstream target genes. (B) Transcription factors (TF) bind to the promoter and activate transcription of SNHGs. SNHGs can then act as competing endogenous RNA sponges to regulate transcription of downstream target genes (ie TF), forming a positive feedback loop. SNHGs regulate promoter methylation (C) or acetylation (D) of downstream target genes and regulate tumor progression.

Abbreviations

ACSL1, acyl-CoA synthetase long chain family member 1; ADT, androgen deprivation therapy; AKT, protein kinase B; ANXA2, annexin A2; AXL, Anexelekto; BDNF, brain-derived neurotrophic factor; CCND1/2, cyclin-D1, cyclin-D2; CCNE1, cyclin-E1; CDK6/7, cyclin-dependent kinase 6, cyclin-dependent kinase 7; CDKN2B, cyclin-dependent kinase 4 inhibitor B; CEBPB, CCAAT/enhancer-binding protein beta; CeRNA, competing endogenous RNA; CRPC, castration-resistant prostate cancer; DANCR, Differentiation antagonizing non-protein coding RNA; DFS, disease-free survival; DGCR8, DiGeorge syndrome chromosomal region 8; E2F5, E2F Transcription Factor 5; EHZ2, enhancer of zeste homolog 2; EMT, epithelial–mesenchymal transition; FIGO, International Federation of Gynecology and Obstetrics; FOXO1, forkhead box O1; GAS5, growth arrest specific transcript 5; GD15, growth/differentiation factor 15; HDGF, hepatoma-derived growth factor; HER2, human epidermal growth factor receptor 2; HMGB1, high mobility group box 1; HOXA5, homeobox A5; IDO, indoleamine 2,3 dioxygenase; IGF2, insulin-like growth factor 2; JAG1, Jagged 1; KLF2, Kruppel Like Factor 2; LncRNA, long non-coding RNA; LNM, lymph node metastasis; MAPK6, mitogen-activated protein kinase 6; MMP13, matrix metalloproteinase 13; NRF2, nuclear factor E2-related factor 2; OS, overall survival; PABPC1, polyadenylate-binding protein 1; PARP1, poly(ADP-ribose) polymerase 1; PCNA, proliferating cell nuclear antigen; PDAC, pancreatic ductal adenocarcinoma; PDCD4, programmed cell death 4; PFS, progression-free survival; PI3K, phosphatidylinositol 3-kinase; PIK3CA, phosphatidylinositol-4,5-bisphosphate 3-kinase catalytic subunit alpha; PKM, pyruvate Kinase M1/M2; PTC, papillary thyroid carcinoma; PTEN, phosphatase and tensin homolog; RRM2, ribonucleoside-diphosphate reductase subunit M2; RXRA, retinoid X receptor alpha; SNHG, small nucleolar RNA host genes; SnoRNA, small nucleolar RNA; SNP, single nucleotide polymorphisms; SOCS3, suppressor of cytokine signaling 3; SPRY2, sprouty homolog 2; TCGA, the Cancer Genome Atlas; TF, transcription Factor; TIMP, tissue inhibitor of metalloproteinases; TNM, tumor node metastasis; UPF1, UPF1 RNA Helicase And ATPase; VASP, vasodilator-stimulated phosphoprotein; VEGF, Vascular endothelial growth factor; YAP1, Yes-associated protein 1; ZIC5, zic family member 5.

Data Sharing Statement

The data supporting the findings of this study are available from the corresponding author upon reasonable request.

the National Natural Science Foundation of China

the China Postdoctoral Science Foundation

the Natural Science Foundation of Liaoning Province This project was funded by the National Natural Science Foundation of China (grant number 81902726), the China Postdoctoral Science Foundation (grant number 2018M641739), and the Natural Science Foundation of Liaoning Province (grant number 20180530090).

Disclosure

The authors report no conflicts of interest for this work.

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