Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention

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Abstract

Cancer is a devastating disease and the primary cause of morbidity and mortality worldwide, with cancer metastasis responsible for 90% of cancer-related deaths. Cancer metastasis is a multistep process characterized by spreading of cancer cells from the primary tumor and acquiring molecular and phenotypic changes that enable them to expand and colonize in distant organs. Despite recent advancements, the underlying molecular mechanism(s) of cancer metastasis is limited and requires further exploration. In addition to genetic alterations, epigenetic changes have been demonstrated to play an important role in the development of cancer metastasis. Long non-coding RNAs (lncRNAs) are considered one of the most critical epigenetic regulators. By regulating signaling pathways and acting as decoys, guides, and scaffolds, they modulate key molecules in every step of cancer metastasis such as dissemination of carcinoma cells, intravascular transit, and metastatic colonization. Gaining a good knowledge of the detailed molecular basis underlying lncRNAs regulating cancer metastasis may provide previously unknown therapeutic and diagnostic lncRNAs for patients with metastatic disease. In this review, we concentrate on the molecular mechanisms underlying lncRNAs in the regulation of cancer metastasis, the cross-talk with metabolic reprogramming, modulating cancer cell anoikis resistance, influencing metastatic microenvironment, and the interaction with pre-metastatic niche formation. In addition, we also discuss the clinical utility and therapeutic potential of lncRNAs for cancer treatment. Finally, we also represent areas for future research in this rapidly developing field.

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Most cited references 294

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Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Hyuna Sung, Jacques Ferlay, Rebecca Siegel … (2021)

This article provides an update on the global cancer burden using the GLOBOCAN 2020 estimates of cancer incidence and mortality produced by the International Agency for Research on Cancer. Worldwide, an estimated 19.3 million new cancer cases (18.1 million excluding nonmelanoma skin cancer) and almost 10.0 million cancer deaths (9.9 million excluding nonmelanoma skin cancer) occurred in 2020. Female breast cancer has surpassed lung cancer as the most commonly diagnosed cancer, with an estimated 2.3 million new cases (11.7%), followed by lung (11.4%), colorectal (10.0 %), prostate (7.3%), and stomach (5.6%) cancers. Lung cancer remained the leading cause of cancer death, with an estimated 1.8 million deaths (18%), followed by colorectal (9.4%), liver (8.3%), stomach (7.7%), and female breast (6.9%) cancers. Overall incidence was from 2-fold to 3-fold higher in transitioned versus transitioning countries for both sexes, whereas mortality varied <2-fold for men and little for women. Death rates for female breast and cervical cancers, however, were considerably higher in transitioning versus transitioned countries (15.0 vs 12.8 per 100,000 and 12.4 vs 5.2 per 100,000, respectively). The global cancer burden is expected to be 28.4 million cases in 2040, a 47% rise from 2020, with a larger increase in transitioning (64% to 95%) versus transitioned (32% to 56%) countries due to demographic changes, although this may be further exacerbated by increasing risk factors associated with globalization and a growing economy. Efforts to build a sustainable infrastructure for the dissemination of cancer prevention measures and provision of cancer care in transitioning countries is critical for global cancer control.

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Hallmarks of Cancer: The Next Generation

Douglas Hanahan, Robert A. Weinberg (2011)

The hallmarks of cancer comprise six biological capabilities acquired during the multistep development of human tumors. The hallmarks constitute an organizing principle for rationalizing the complexities of neoplastic disease. They include sustaining proliferative signaling, evading growth suppressors, resisting cell death, enabling replicative immortality, inducing angiogenesis, and activating invasion and metastasis. Underlying these hallmarks are genome instability, which generates the genetic diversity that expedites their acquisition, and inflammation, which fosters multiple hallmark functions. Conceptual progress in the last decade has added two emerging hallmarks of potential generality to this list-reprogramming of energy metabolism and evading immune destruction. In addition to cancer cells, tumors exhibit another dimension of complexity: they contain a repertoire of recruited, ostensibly normal cells that contribute to the acquisition of hallmark traits by creating the "tumor microenvironment." Recognition of the widespread applicability of these concepts will increasingly affect the development of new means to treat human cancer. Copyright © 2011 Elsevier Inc. All rights reserved.

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Understanding the Warburg effect: the metabolic requirements of cell proliferation.

Craig B Thompson, Matthew Vander Heiden, Lewis Cantley (2009)

In contrast to normal differentiated cells, which rely primarily on mitochondrial oxidative phosphorylation to generate the energy needed for cellular processes, most cancer cells instead rely on aerobic glycolysis, a phenomenon termed "the Warburg effect." Aerobic glycolysis is an inefficient way to generate adenosine 5'-triphosphate (ATP), however, and the advantage it confers to cancer cells has been unclear. Here we propose that the metabolism of cancer cells, and indeed all proliferating cells, is adapted to facilitate the uptake and incorporation of nutrients into the biomass (e.g., nucleotides, amino acids, and lipids) needed to produce a new cell. Supporting this idea are recent studies showing that (i) several signaling pathways implicated in cell proliferation also regulate metabolic pathways that incorporate nutrients into biomass; and that (ii) certain cancer-associated mutations enable cancer cells to acquire and metabolize nutrients in a manner conducive to proliferation rather than efficient ATP production. A better understanding of the mechanistic links between cellular metabolism and growth control may ultimately lead to better treatments for human cancer.

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Author and article information

Contributors

Sana Khurshid Baba: URI : https://loop.frontiersin.org/people/2310215/overview

Rashid Mir: URI : https://loop.frontiersin.org/people/1449620/overview

Mohammad Fahad Ullah: URI : https://loop.frontiersin.org/people/1002786/overview

Faisal H. Altemani: URI : https://loop.frontiersin.org/people/2206402/overview

Tariq Masoodi: URI : https://loop.frontiersin.org/people/1725510/overview

Ajaz A. Bhat: URI : https://loop.frontiersin.org/people/537745/overview

Muzafar A. Macha: URI : https://loop.frontiersin.org/people/954838/overview

Journal

Journal ID (nlm-ta): Front Cell Dev Biol

Journal ID (iso-abbrev): Front Cell Dev Biol

Journal ID (publisher-id): Front. Cell Dev. Biol.

Title: Frontiers in Cell and Developmental Biology

Publisher: Frontiers Media S.A.

ISSN (Electronic): 2296-634X

Publication date (Electronic): 13 June 2023

Publication date Collection: 2023

Volume: 11

Electronic Location Identifier: 1164301

Affiliations

[1] ¹ Watson-Crick Centre for Molecular Medicine , Islamic University of Science and Technology , Awantipora, Kashmir, India

[2] ² Department of Microbiology , Sher-I-Kashmir Institute of Medical Science (SKIMS) , Soura, Kashmir, India

[3] ³ Department of Medical Lab Technology , Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences , University of Tabuk , Tabuk, Saudi Arabia

[4] ⁴ Department of Biochemistry , Faculty of Science , University of Tabuk , Tabuk, Saudi Arabia

[5] ⁵ Department of Chemistry , Faculty of Science , University of Tabuk , Tabuk, Saudi Arabia

[6] ⁶ Human Immunology Department , Research Branch , Sidra Medicine , Doha, Qatar

[7] ⁷ Department of Human Genetics-Precision Medicine in Diabetes, Obesity, and Cancer Program , Sidra Medicine , Doha, Qatar

Author notes

Edited by: Samikshan Dutta, University of Nebraska Medical Center, United States

Reviewed by: Shailendra Kumar Maurya, University of Nebraska Medical Center, United States

Erika Zambalde, State University of Campinas, Brazil

*Correspondence: Muzafar A. Macha, muzafar.macha@ 123456iust.ac.in , muzafar.aiiims@ 123456gmail.com

Article

Publisher ID: 1164301

DOI: 10.3389/fcell.2023.1164301

PMC ID: 10299194

PubMed ID: 37384249

SO-VID: 4b59e267-a897-4e46-bd0d-592b344049a7

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

History

Date received : 12 February 2023

Date accepted : 22 May 2023

Funding

Funded by: Department of Biotechnology, Ministry of Science and Technology, India , doi 10.13039/501100001407;

Funded by: Science and Engineering Research Board , doi 10.13039/501100001843;

This study was supported by the Ramalingaswami Re-entry Fellowship (Grant number: D.O. NO.BT/HRD/35/02/2006) from the Department of Biotechnology, Govt. of India, New Delhi, and Core Research Grant (CRG/2021/003805) from the Science and Engineering Research Board (SERB), Govt. of India, New Delhi, to MM. Promotion of University Research and Scientific Excellence (SR/PURSE/2022/121) grant from the Department of Biotechnology, Govt. of India, New Delhi to the Islamic University of Science and Technology (IUST), Awantipora, Kashmir.

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section-at-acceptance Cancer Cell Biology

Keywords: cancer,metastasis,long non-coding rnas,tumor microenvironment,anoikis resistance,metabolic reprogramming,immune modulation

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Keywords: cancer, metastasis, long non-coding rnas, tumor microenvironment, anoikis resistance, metabolic reprogramming, immune modulation

Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention

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Karger: Oncology

Most cited references 294

Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries

Hallmarks of Cancer: The Next Generation

Understanding the Warburg effect: the metabolic requirements of cell proliferation.

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