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

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 phen...

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Main Authors: Sana Khurshid Baba, Sadaf Khursheed Baba, Rashid Mir, Imadeldin Elfaki, Naseh Algehainy, Mohammad Fahad Ullah, Jameel Barnawi, Faisal H. Altemani, Mohammad Alanazi, Syed Khalid Mustafa, Tariq Masoodi, Ammira S. Alshabeeb Akil, Ajaz A. Bhat, Muzafar A. Macha
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-06-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2023.1164301/full
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author Sana Khurshid Baba
Sadaf Khursheed Baba
Rashid Mir
Imadeldin Elfaki
Naseh Algehainy
Mohammad Fahad Ullah
Jameel Barnawi
Faisal H. Altemani
Mohammad Alanazi
Syed Khalid Mustafa
Tariq Masoodi
Ammira S. Alshabeeb Akil
Ajaz A. Bhat
Muzafar A. Macha
author_facet Sana Khurshid Baba
Sadaf Khursheed Baba
Rashid Mir
Imadeldin Elfaki
Naseh Algehainy
Mohammad Fahad Ullah
Jameel Barnawi
Faisal H. Altemani
Mohammad Alanazi
Syed Khalid Mustafa
Tariq Masoodi
Ammira S. Alshabeeb Akil
Ajaz A. Bhat
Muzafar A. Macha
author_sort Sana Khurshid Baba
collection DOAJ
description 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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spelling doaj.art-a3cb5b0205474c5fb2c9fec15c4c380d2023-06-13T13:44:21ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2023-06-011110.3389/fcell.2023.11643011164301Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic interventionSana Khurshid Baba0Sadaf Khursheed Baba1Rashid Mir2Imadeldin Elfaki3Naseh Algehainy4Mohammad Fahad Ullah5Jameel Barnawi6Faisal H. Altemani7Mohammad Alanazi8Syed Khalid Mustafa9Tariq Masoodi10Ammira S. Alshabeeb Akil11Ajaz A. Bhat12Muzafar A. Macha13Watson-Crick Centre for Molecular Medicine, Islamic University of Science and Technology, Awantipora, Kashmir, IndiaDepartment of Microbiology, Sher-I-Kashmir Institute of Medical Science (SKIMS), Soura, Kashmir, IndiaDepartment of Medical Lab Technology, Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Biochemistry, Faculty of Science, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Medical Lab Technology, Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Medical Lab Technology, Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Medical Lab Technology, Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Medical Lab Technology, Prince Fahd Bin Sultan Research Chair Faculty of Applied Medical Sciences, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Biochemistry, Faculty of Science, University of Tabuk, Tabuk, Saudi ArabiaDepartment of Chemistry, Faculty of Science, University of Tabuk, Tabuk, Saudi ArabiaHuman Immunology Department, Research Branch, Sidra Medicine, Doha, QatarDepartment of Human Genetics-Precision Medicine in Diabetes, Obesity, and Cancer Program, Sidra Medicine, Doha, QatarDepartment of Human Genetics-Precision Medicine in Diabetes, Obesity, and Cancer Program, Sidra Medicine, Doha, QatarWatson-Crick Centre for Molecular Medicine, Islamic University of Science and Technology, Awantipora, Kashmir, IndiaCancer 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.https://www.frontiersin.org/articles/10.3389/fcell.2023.1164301/fullcancermetastasislong non-coding RNAstumor microenvironmentanoikis resistancemetabolic reprogramming
spellingShingle Sana Khurshid Baba
Sadaf Khursheed Baba
Rashid Mir
Imadeldin Elfaki
Naseh Algehainy
Mohammad Fahad Ullah
Jameel Barnawi
Faisal H. Altemani
Mohammad Alanazi
Syed Khalid Mustafa
Tariq Masoodi
Ammira S. Alshabeeb Akil
Ajaz A. Bhat
Muzafar A. Macha
Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
Frontiers in Cell and Developmental Biology
cancer
metastasis
long non-coding RNAs
tumor microenvironment
anoikis resistance
metabolic reprogramming
title Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
title_full Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
title_fullStr Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
title_full_unstemmed Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
title_short Long non-coding RNAs modulate tumor microenvironment to promote metastasis: novel avenue for therapeutic intervention
title_sort long non coding rnas modulate tumor microenvironment to promote metastasis novel avenue for therapeutic intervention
topic cancer
metastasis
long non-coding RNAs
tumor microenvironment
anoikis resistance
metabolic reprogramming
url https://www.frontiersin.org/articles/10.3389/fcell.2023.1164301/full
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