Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner

<p dir="ltr">Colorectal cancer (CRC) is the fourth most common cancer type globally. Investigating the signaling pathways that maintain cancer cell phenotype can identify new biomarkers for targeted therapy. Aberrant transforming growth factor-β (TGFβ) signaling has been implicated i...

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التفاصيل البيبلوغرافية
المؤلف الرئيسي: Mona Elsafadi (18614905) (author)
مؤلفون آخرون: Muthurangan Manikandan (6002243) (author), Sami Almalki (18949444) (author), Amer Mahmood (284424) (author), Tasneem Shinwari (18614908) (author), Radhakrishnan Vishnubalaji (3563306) (author), Mohammad Mobarak (18949447) (author), Musaad Alfayez (3571736) (author), Abdullah Aldahmash (3563300) (author), Moustapha Kassem (101848) (author), Nehad M. Alajez (7397276) (author)
منشور في: 2020
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_version_ 1864513511865974784
author Mona Elsafadi (18614905)
author2 Muthurangan Manikandan (6002243)
Sami Almalki (18949444)
Amer Mahmood (284424)
Tasneem Shinwari (18614908)
Radhakrishnan Vishnubalaji (3563306)
Mohammad Mobarak (18949447)
Musaad Alfayez (3571736)
Abdullah Aldahmash (3563300)
Moustapha Kassem (101848)
Nehad M. Alajez (7397276)
author2_role author
author
author
author
author
author
author
author
author
author
author_facet Mona Elsafadi (18614905)
Muthurangan Manikandan (6002243)
Sami Almalki (18949444)
Amer Mahmood (284424)
Tasneem Shinwari (18614908)
Radhakrishnan Vishnubalaji (3563306)
Mohammad Mobarak (18949447)
Musaad Alfayez (3571736)
Abdullah Aldahmash (3563300)
Moustapha Kassem (101848)
Nehad M. Alajez (7397276)
author_role author
dc.creator.none.fl_str_mv Mona Elsafadi (18614905)
Muthurangan Manikandan (6002243)
Sami Almalki (18949444)
Amer Mahmood (284424)
Tasneem Shinwari (18614908)
Radhakrishnan Vishnubalaji (3563306)
Mohammad Mobarak (18949447)
Musaad Alfayez (3571736)
Abdullah Aldahmash (3563300)
Moustapha Kassem (101848)
Nehad M. Alajez (7397276)
dc.date.none.fl_str_mv 2020-05-11T09:00:00Z
dc.identifier.none.fl_str_mv 10.1038/s41419-020-2529-6
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Transgelin_is_a_poor_prognostic_factor_associated_with_advanced_colorectal_cancer_CRC_stage_promoting_tumor_growth_and_migration_in_a_TGF_-dependent_manner/26144095
dc.rights.none.fl_str_mv CC BY 4.0
info:eu-repo/semantics/openAccess
dc.subject.none.fl_str_mv Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Colorectal cancer (CRC)
Transforming growth factor-β (TGFβ)
TAGLN (Transgelin)
Prognostic marker
Biomarker
Tumor progression
Angiogenesis
dc.title.none.fl_str_mv Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <p dir="ltr">Colorectal cancer (CRC) is the fourth most common cancer type globally. Investigating the signaling pathways that maintain cancer cell phenotype can identify new biomarkers for targeted therapy. Aberrant transforming growth factor-β (TGFβ) signaling has been implicated in CRC progression, however, the exact mechanism by which TGFβ exerts its function is still being unraveled. Herein, we investigated TAGLN expression, prognostic value, and its regulation by TGFβ in CRC. While TAGLN was generally found to be downregulated in CRC, elevated expression of TAGLN was associated with advanced CRC stage and predicted poor overall survival (hazard ratio (HR) = 1.8, log-rank test P-value = 0.014) and disease-free survival (HR = 1.6, log-rank test P-value = 0.046), hence implicating TAGLN as poor prognostic factor in CRC. Forced expression of TAGLN was associated with enhanced CRC cell proliferation, clonogenic growth, cell migration and in vivo tumor formation in immunocompromised mice, while targeted depletion of TAGLN exhibited opposing biological effects. Global gene expression profiling of TAGLN-overexpressing or TAGLN-deficient CRC cell lines revealed deregulation of multiple cancer-related genes and signaling pathways. Transmission electron microscopy (TEM) revealed ultrastructural changes due to loss of TAGLN, including disruption of actin cytoskeleton organization and aberrant actin filament distribution. Hierarchical clustering, principle component, and ingenuity pathway analyses revealed distinct molecular profile associated with TAGLNhigh CRC patients with remarkable activation of a number of mechanistic networks, including SMARCA4, TGFβ1, and P38 MAPK. The P38 MAPK was the top predicted upstream regulator network promoting cell movement through regulation of several intermediate molecules, including TGFβ1. Concordantly, functional categories associated with cellular movement and angiogenesis were also enriched in TAGLNhigh CRC, supporting a model for the molecular mechanisms linking TGFβ-induced upregulation of TAGLN and CRC tumor progression and suggesting TAGLN as potential prognostic marker associated with advanced CRC pathological stage.</p><h2>Other Information</h2><p dir="ltr">Published in: Cell Death & Disease<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41419-020-2529-6" target="_blank">https://dx.doi.org/10.1038/s41419-020-2529-6</a></p>
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identifier_str_mv 10.1038/s41419-020-2529-6
network_acronym_str Manara2
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oai_identifier_str oai:figshare.com:article/26144095
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spelling Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent mannerMona Elsafadi (18614905)Muthurangan Manikandan (6002243)Sami Almalki (18949444)Amer Mahmood (284424)Tasneem Shinwari (18614908)Radhakrishnan Vishnubalaji (3563306)Mohammad Mobarak (18949447)Musaad Alfayez (3571736)Abdullah Aldahmash (3563300)Moustapha Kassem (101848)Nehad M. Alajez (7397276)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesOncology and carcinogenesisColorectal cancer (CRC)Transforming growth factor-β (TGFβ)TAGLN (Transgelin)Prognostic markerBiomarkerTumor progressionAngiogenesis<p dir="ltr">Colorectal cancer (CRC) is the fourth most common cancer type globally. Investigating the signaling pathways that maintain cancer cell phenotype can identify new biomarkers for targeted therapy. Aberrant transforming growth factor-β (TGFβ) signaling has been implicated in CRC progression, however, the exact mechanism by which TGFβ exerts its function is still being unraveled. Herein, we investigated TAGLN expression, prognostic value, and its regulation by TGFβ in CRC. While TAGLN was generally found to be downregulated in CRC, elevated expression of TAGLN was associated with advanced CRC stage and predicted poor overall survival (hazard ratio (HR) = 1.8, log-rank test P-value = 0.014) and disease-free survival (HR = 1.6, log-rank test P-value = 0.046), hence implicating TAGLN as poor prognostic factor in CRC. Forced expression of TAGLN was associated with enhanced CRC cell proliferation, clonogenic growth, cell migration and in vivo tumor formation in immunocompromised mice, while targeted depletion of TAGLN exhibited opposing biological effects. Global gene expression profiling of TAGLN-overexpressing or TAGLN-deficient CRC cell lines revealed deregulation of multiple cancer-related genes and signaling pathways. Transmission electron microscopy (TEM) revealed ultrastructural changes due to loss of TAGLN, including disruption of actin cytoskeleton organization and aberrant actin filament distribution. Hierarchical clustering, principle component, and ingenuity pathway analyses revealed distinct molecular profile associated with TAGLNhigh CRC patients with remarkable activation of a number of mechanistic networks, including SMARCA4, TGFβ1, and P38 MAPK. The P38 MAPK was the top predicted upstream regulator network promoting cell movement through regulation of several intermediate molecules, including TGFβ1. Concordantly, functional categories associated with cellular movement and angiogenesis were also enriched in TAGLNhigh CRC, supporting a model for the molecular mechanisms linking TGFβ-induced upregulation of TAGLN and CRC tumor progression and suggesting TAGLN as potential prognostic marker associated with advanced CRC pathological stage.</p><h2>Other Information</h2><p dir="ltr">Published in: Cell Death & Disease<br>License: <a href="https://creativecommons.org/licenses/by/4.0" target="_blank">https://creativecommons.org/licenses/by/4.0</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1038/s41419-020-2529-6" target="_blank">https://dx.doi.org/10.1038/s41419-020-2529-6</a></p>2020-05-11T09:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1038/s41419-020-2529-6https://figshare.com/articles/journal_contribution/Transgelin_is_a_poor_prognostic_factor_associated_with_advanced_colorectal_cancer_CRC_stage_promoting_tumor_growth_and_migration_in_a_TGF_-dependent_manner/26144095CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/261440952020-05-11T09:00:00Z
spellingShingle Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
Mona Elsafadi (18614905)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Colorectal cancer (CRC)
Transforming growth factor-β (TGFβ)
TAGLN (Transgelin)
Prognostic marker
Biomarker
Tumor progression
Angiogenesis
status_str publishedVersion
title Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
title_full Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
title_fullStr Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
title_full_unstemmed Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
title_short Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
title_sort Transgelin is a poor prognostic factor associated with advanced colorectal cancer (CRC) stage promoting tumor growth and migration in a TGFβ-dependent manner
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Oncology and carcinogenesis
Colorectal cancer (CRC)
Transforming growth factor-β (TGFβ)
TAGLN (Transgelin)
Prognostic marker
Biomarker
Tumor progression
Angiogenesis