Exosomal lncRNA SNHG10 derived from colorectal cancer cells suppresses natural killer cell cytotoxicity by upregulating INHBC

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Abstract

Background

Exosome-mediated crosstalk between cancer cells and immune cells contributes to tumor growth. In this study, we investigated the mechanism underlying the exosome-mediated immune escape of colorectal cancer (CRC) cells from natural killer (NK) cells via the transfer of long noncoding RNAs (lncRNAs).

Methods

An epithelial–mesenchymal transition (EMT) model of SW480 cells was established by transforming growth factor beta (TGF-β), followed by the assessment of the effect of EMT-derived exosomes (EMT-exo) on the functions of NK cells. RNA sequencing was performed to identify exosomal lncRNAs and target genes. The function of exosomal lncRNAs in tumor growth was further verified in vivo.

Results

EMT-exo suppressed the proliferation, cytotoxicity, IFN-γ production, and perforin-1 and granzyme B secretion of NK cells. RNA sequencing revealed that SNHG10 expression was upregulated in EMT-exo compared with that in non-EMT-exo. Moreover, SNHG10 expression was upregulated in tumor tissues in CRC, which was associated with poor prognosis. Overexpression of SNHG10 in exosomes (oe-lnc-SNHG10 exo) significantly suppressed the viability and cytotoxicity of NK cells. Transcriptome sequencing of NK cells revealed that the expression levels of 114 genes were upregulated in the oe-lnc-SNHG10 exo group, including inhibin subunit beta C ( INHBC), which was involved in the TGF-β signaling pathway. Si-INHBC treatment abrogated the effect of oe-lnc-SNHG10 exo on NK cells. oe-lnc-SNHG10 exo induced tumor growth and upregulated INHBC expression in mice and downregulated the expression of perforin, granzyme B, and NK1.1 in tumor tissues.

Conclusions

The CRC cell-derived exosomal lncRNA SNHG10 suppresses the function of NK cells by upregulating INHBC expression. This study provides evidence that exosomal lncRNAs contribute to immune escape by inducing NK cell inhibition and proposes a potential treatment strategy for CRC.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12935-021-02221-2.

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Most cited references 31

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Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries

Ahmedin Jemal, Lindsey A Torre, Rebecca Siegel … (2018)

This article provides a status report on the global burden of cancer worldwide using the GLOBOCAN 2018 estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer, with a focus on geographic variability across 20 world regions. There will be an estimated 18.1 million new cancer cases (17.0 million excluding nonmelanoma skin cancer) and 9.6 million cancer deaths (9.5 million excluding nonmelanoma skin cancer) in 2018. In both sexes combined, lung cancer is the most commonly diagnosed cancer (11.6% of the total cases) and the leading cause of cancer death (18.4% of the total cancer deaths), closely followed by female breast cancer (11.6%), prostate cancer (7.1%), and colorectal cancer (6.1%) for incidence and colorectal cancer (9.2%), stomach cancer (8.2%), and liver cancer (8.2%) for mortality. Lung cancer is the most frequent cancer and the leading cause of cancer death among males, followed by prostate and colorectal cancer (for incidence) and liver and stomach cancer (for mortality). Among females, breast cancer is the most commonly diagnosed cancer and the leading cause of cancer death, followed by colorectal and lung cancer (for incidence), and vice versa (for mortality); cervical cancer ranks fourth for both incidence and mortality. The most frequently diagnosed cancer and the leading cause of cancer death, however, substantially vary across countries and within each country depending on the degree of economic development and associated social and life style factors. It is noteworthy that high-quality cancer registry data, the basis for planning and implementing evidence-based cancer control programs, are not available in most low- and middle-income countries. The Global Initiative for Cancer Registry Development is an international partnership that supports better estimation, as well as the collection and use of local data, to prioritize and evaluate national cancer control efforts. CA: A Cancer Journal for Clinicians 2018;0:1-31. © 2018 American Cancer Society.

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Natural killer cells and other innate lymphoid cells in cancer

Eric Vivier, Pierre-Yves Dumas, Margaux Vienne … (2018)

Immuno-oncology is an emerging field that has revolutionized cancer treatment. Most immunomodulatory strategies focus on enhancing T cell responses, but there has been a recent surge of interest in harnessing the relatively underexplored natural killer (NK) cell compartment for therapeutic interventions. NK cells show cytotoxic activity against diverse tumour cell types, and some of the clinical approaches originally developed to increase T cell cytotoxicity may also activate NK cells. Moreover, increasing numbers of studies have identified novel methods for increasing NK cell antitumour immunity and expanding NK cell populations ex vivo, thereby paving the way for a new generation of anticancer immunotherapies. The role of other innate lymphoid cells (group 1 innate lymphoid cell (ILC1), ILC2 and ILC3 subsets) in tumours is also being actively explored. This Review provides an overview of the field and summarizes current immunotherapeutic approaches for solid tumours and haematological malignancies.

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Cancer incidence and mortality in China, 2014.

Wanqing Chen, Kexin Sun, Rongshou Zheng … (2018)

National Central Cancer Registry of China (NCCRC) updated nationwide cancer statistics using population-based cancer registry data in 2014 collected from all available cancer registries.

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Author and article information

Contributors

Yiwen Huang: wymanhuang@qq.com

Yanbo Luo: wct66@163.com

Wentao Ou: Owt320@sina.com

Yuanyuan Wang: 315347857@qq.com

Dong Dong: 61408754@qq.com

Xiaowen Peng: 77294565@qq.com

Yuqi Luo:

ORCID: http://orcid.org/0000-0002-4236-4449

eyluoyuqi@scut.edu.cn

Journal

Journal ID (nlm-ta): Cancer Cell Int

Journal ID (iso-abbrev): Cancer Cell Int

Title: Cancer Cell International

Publisher: BioMed Central (London )

ISSN (Electronic): 1475-2867

Publication date (Electronic): 12 October 2021

Publication date PMC-release: 12 October 2021

Publication date Collection: 2021

Volume: 21

Electronic Location Identifier: 528

Affiliations

[1 ]GRID grid.413432.3, ISNI 0000 0004 1798 5993, Department of Emergency, Nansha Hospital, Guangzhou First People’s Hospital, School of Medicine, , Southern China University of Technology, ; Guangzhou, Guangdong China

[2 ]Department of Gastrointestinal and Hepatobiliary Surgery, Shenzhen Longhua District Central Hospital, No. 187, Guanlan Road, Longhua District, Shenzhen, 518110 Guangdong Province China

[3 ]GRID grid.413432.3, ISNI 0000 0004 1798 5993, Department of General Surgery, Nansha Hospital, Guangzhou First People’s Hospital, School of Medicine, , Southern China University of Technology, ; Guangzhou, Guangdong China

[4 ]GRID grid.413432.3, ISNI 0000 0004 1798 5993, Department of Neurology, Nansha Hospital, Guangzhou First People’s Hospital, School of Medicine, , Southern China University of Technology, ; Guangzhou, Guangdong China

[5 ]GRID grid.413432.3, ISNI 0000 0004 1798 5993, Department of Laboratory Medicine, Guangzhou First People’s Hospital, School of Medicine, , Nansha Hospital, Southern China University of Technology, ; Guangzhou, Guangdong China

Author information

Yuqi Luo http://orcid.org/0000-0002-4236-4449

Article

Publisher ID: 2221

DOI: 10.1186/s12935-021-02221-2

PMC ID: 8507338

PubMed ID: 34641864

SO-VID: bbc19249-1013-468a-8a40-5e5fd05313db

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 15 July 2021

Date accepted : 23 September 2021

Funding

Funded by: Fundamental Research Funds for the Central Universities, South China University of Technology

Award ID: 2018MS021

Award Recipient : Yuqi Luo

Funded by: guangzhou medical and health research project

Award ID: 2018A11042

Award ID: 20201A010005

Award Recipient : Wentao Ou

Custom metadata

ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: colorectal cancer,exosomal lncrna,epithelial–mesenchymal transition,immune escape,natural killer cells

Data availability:

ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: colorectal cancer, exosomal lncrna, epithelial–mesenchymal transition, immune escape, natural killer cells

Exosomal lncRNA SNHG10 derived from colorectal cancer cells suppresses natural killer cell cytotoxicity by upregulating INHBC

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Abstract

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Supplementary Information

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Karger: Oncology

Most cited references 31

Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries

Natural killer cells and other innate lymphoid cells in cancer

Cancer incidence and mortality in China, 2014.

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