Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy

<h2>Background</h2><p dir="ltr">The mechanism of tumor immune escape and progression in colorectal cancer (CRC) is widely investigated in-vitro to help understand and identify agents that might play a crucial role in response to treatment and improve the overall survival...

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التفاصيل البيبلوغرافية
المؤلف الرئيسي: Nassiba Taib (14557385) (author)
مؤلفون آخرون: Maysaloun Merhi (4246147) (author), Varghese Inchakalody (15263530) (author), Sarra Mestiri (14557379) (author), Shereena Hydrose (14442135) (author), Karama Makni-Maalej (15263533) (author), Afsheen Raza (492657) (author), Fairooz Sahir (6595517) (author), Fouad Azizi (11835843) (author), Parveen B. Nizamuddin (14590613) (author), Queenie Fernandes (14557388) (author), Zeenath Safira K. M. Yoosuf (15263536) (author), Salam Almoghrabi (15263539) (author), Lobna Al-Zaidan (14557394) (author), Alaaeldin Shablak (14778097) (author), Shahab Uddin (154400) (author), Cristina Maccalli (2632465) (author), Mohammed Ussama Al Homsi (15263542) (author), Said Dermime (79420) (author)
منشور في: 2023
الموضوعات:
الوسوم: إضافة وسم
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author Nassiba Taib (14557385)
author2 Maysaloun Merhi (4246147)
Varghese Inchakalody (15263530)
Sarra Mestiri (14557379)
Shereena Hydrose (14442135)
Karama Makni-Maalej (15263533)
Afsheen Raza (492657)
Fairooz Sahir (6595517)
Fouad Azizi (11835843)
Parveen B. Nizamuddin (14590613)
Queenie Fernandes (14557388)
Zeenath Safira K. M. Yoosuf (15263536)
Salam Almoghrabi (15263539)
Lobna Al-Zaidan (14557394)
Alaaeldin Shablak (14778097)
Shahab Uddin (154400)
Cristina Maccalli (2632465)
Mohammed Ussama Al Homsi (15263542)
Said Dermime (79420)
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author_facet Nassiba Taib (14557385)
Maysaloun Merhi (4246147)
Varghese Inchakalody (15263530)
Sarra Mestiri (14557379)
Shereena Hydrose (14442135)
Karama Makni-Maalej (15263533)
Afsheen Raza (492657)
Fairooz Sahir (6595517)
Fouad Azizi (11835843)
Parveen B. Nizamuddin (14590613)
Queenie Fernandes (14557388)
Zeenath Safira K. M. Yoosuf (15263536)
Salam Almoghrabi (15263539)
Lobna Al-Zaidan (14557394)
Alaaeldin Shablak (14778097)
Shahab Uddin (154400)
Cristina Maccalli (2632465)
Mohammed Ussama Al Homsi (15263542)
Said Dermime (79420)
author_role author
dc.creator.none.fl_str_mv Nassiba Taib (14557385)
Maysaloun Merhi (4246147)
Varghese Inchakalody (15263530)
Sarra Mestiri (14557379)
Shereena Hydrose (14442135)
Karama Makni-Maalej (15263533)
Afsheen Raza (492657)
Fairooz Sahir (6595517)
Fouad Azizi (11835843)
Parveen B. Nizamuddin (14590613)
Queenie Fernandes (14557388)
Zeenath Safira K. M. Yoosuf (15263536)
Salam Almoghrabi (15263539)
Lobna Al-Zaidan (14557394)
Alaaeldin Shablak (14778097)
Shahab Uddin (154400)
Cristina Maccalli (2632465)
Mohammed Ussama Al Homsi (15263542)
Said Dermime (79420)
dc.date.none.fl_str_mv 2023-03-31T03:00:00Z
dc.identifier.none.fl_str_mv 10.1186/s12967-023-04073-y
dc.relation.none.fl_str_mv https://figshare.com/articles/journal_contribution/Treatment_with_decitabine_induces_the_expression_of_stemness_markers_PD-L1_and_NY-ESO-1_in_colorectal_cancer_potential_for_combined_chemoimmunotherapy/24941844
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
Reproductive medicine
Colorectal cancer
Decitabine
NY-ESO-1
PD-L1
Stemness markers
Chemoresistance
Immune escape
dc.title.none.fl_str_mv Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
dc.type.none.fl_str_mv Text
Journal contribution
info:eu-repo/semantics/publishedVersion
text
contribution to journal
description <h2>Background</h2><p dir="ltr">The mechanism of tumor immune escape and progression in colorectal cancer (CRC) is widely investigated in-vitro to help understand and identify agents that might play a crucial role in response to treatment and improve the overall survival of CRC patients. Several mechanisms of immune escape and tumor progression, including expression of stemness markers, inactivation of immunoregulatory genes by methylation, and epigenetic silencing, have been reported in CRC, indicating the potential of demethylating agents as anti-cancer drugs. Of these, a chemotherapeutic demethylating agent, Decitabine (DAC), has been reported to induce a dual effect on both DNA demethylation and histone changes leading to an increased expression of target biomarkers, thus making it an attractive anti-tumorigenic drug.</p><h2>Methods</h2><p dir="ltr">We compared the effect of DAC in primary 1076 Col and metastatic 1872 Col cell lines isolated and generated from patients’ tumor tissues. Both cell lines were treated with DAC, and the expression of the NY-ESO-1 cancer-testis antigen, the PD-L1 immunoinhibitory marker, and the CD44, Nanog, KLF-4, CD133, MSI-1 stemness markers were analyzed using different molecular and immunological assays.</p><h2>Results</h2><p dir="ltr">DAC treatment significantly upregulated stemness markers in both primary 1076 Col and meta-static 1872 Col cell lines, although a lower effect occurred on the latter: CD44 (7.85 fold; ***p = 0.0001 vs. (4.19 fold; *p = 0.0120), Nanog (4.1 fold; ***p < 0.0001 vs.1.69 fold; ***p = 0.0008), KLF-4 (4.33 fold; ***p < 0.0001 vs.2.48 fold; ***p = 0.0005), CD133 (16.77 fold; ***p = 0.0003 vs.6.36 fold; *p = 0.0166), and MSI-1 (2.33 fold; ***p = 0.0003 vs.2.3 fold; ***p = 0.0004), respectively. Interestingly, in the metastatic 1872 Col cells treated with DAC, the expression of both PD-L1 and NY-ESO-1 was increased tenfold (*p = 0.0128) and fivefold (***p < 0.0001), respectively.</p><h2>Conclusions</h2><p dir="ltr">We conclude that the upregulation of both stemness and immune checkpoint markers by DAC treatment on CRC cells might represent a mechanism of immune evasion. In addition, induction of NY-ESO-1 may represent an immuno-therapeutic option in metastatic CRC patients. Finally, the combination of DAC and anti-PD-1/anti-PD-L1 antibodies treatment should represent a potential therapeutic intervention for this group of patients.</p><p dir="ltr"><br></p><h2>Other Information</h2><p dir="ltr">Published in: Journal of Translational Medicine<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/10.1186/s12967-023-04073-y" target="_blank">https://dx.doi.org/10.1186/s12967-023-04073-y</a></p>
eu_rights_str_mv openAccess
id Manara2_54849e8a3be3e0c5634223c11eb140cf
identifier_str_mv 10.1186/s12967-023-04073-y
network_acronym_str Manara2
network_name_str Manara2
oai_identifier_str oai:figshare.com:article/24941844
publishDate 2023
repository.mail.fl_str_mv
repository.name.fl_str_mv
repository_id_str
rights_invalid_str_mv CC BY 4.0
spelling Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapyNassiba Taib (14557385)Maysaloun Merhi (4246147)Varghese Inchakalody (15263530)Sarra Mestiri (14557379)Shereena Hydrose (14442135)Karama Makni-Maalej (15263533)Afsheen Raza (492657)Fairooz Sahir (6595517)Fouad Azizi (11835843)Parveen B. Nizamuddin (14590613)Queenie Fernandes (14557388)Zeenath Safira K. M. Yoosuf (15263536)Salam Almoghrabi (15263539)Lobna Al-Zaidan (14557394)Alaaeldin Shablak (14778097)Shahab Uddin (154400)Cristina Maccalli (2632465)Mohammed Ussama Al Homsi (15263542)Said Dermime (79420)Biological sciencesBiochemistry and cell biologyBiomedical and clinical sciencesReproductive medicineColorectal cancerDecitabineNY-ESO-1PD-L1Stemness markersChemoresistanceImmune escape<h2>Background</h2><p dir="ltr">The mechanism of tumor immune escape and progression in colorectal cancer (CRC) is widely investigated in-vitro to help understand and identify agents that might play a crucial role in response to treatment and improve the overall survival of CRC patients. Several mechanisms of immune escape and tumor progression, including expression of stemness markers, inactivation of immunoregulatory genes by methylation, and epigenetic silencing, have been reported in CRC, indicating the potential of demethylating agents as anti-cancer drugs. Of these, a chemotherapeutic demethylating agent, Decitabine (DAC), has been reported to induce a dual effect on both DNA demethylation and histone changes leading to an increased expression of target biomarkers, thus making it an attractive anti-tumorigenic drug.</p><h2>Methods</h2><p dir="ltr">We compared the effect of DAC in primary 1076 Col and metastatic 1872 Col cell lines isolated and generated from patients’ tumor tissues. Both cell lines were treated with DAC, and the expression of the NY-ESO-1 cancer-testis antigen, the PD-L1 immunoinhibitory marker, and the CD44, Nanog, KLF-4, CD133, MSI-1 stemness markers were analyzed using different molecular and immunological assays.</p><h2>Results</h2><p dir="ltr">DAC treatment significantly upregulated stemness markers in both primary 1076 Col and meta-static 1872 Col cell lines, although a lower effect occurred on the latter: CD44 (7.85 fold; ***p = 0.0001 vs. (4.19 fold; *p = 0.0120), Nanog (4.1 fold; ***p < 0.0001 vs.1.69 fold; ***p = 0.0008), KLF-4 (4.33 fold; ***p < 0.0001 vs.2.48 fold; ***p = 0.0005), CD133 (16.77 fold; ***p = 0.0003 vs.6.36 fold; *p = 0.0166), and MSI-1 (2.33 fold; ***p = 0.0003 vs.2.3 fold; ***p = 0.0004), respectively. Interestingly, in the metastatic 1872 Col cells treated with DAC, the expression of both PD-L1 and NY-ESO-1 was increased tenfold (*p = 0.0128) and fivefold (***p < 0.0001), respectively.</p><h2>Conclusions</h2><p dir="ltr">We conclude that the upregulation of both stemness and immune checkpoint markers by DAC treatment on CRC cells might represent a mechanism of immune evasion. In addition, induction of NY-ESO-1 may represent an immuno-therapeutic option in metastatic CRC patients. Finally, the combination of DAC and anti-PD-1/anti-PD-L1 antibodies treatment should represent a potential therapeutic intervention for this group of patients.</p><p dir="ltr"><br></p><h2>Other Information</h2><p dir="ltr">Published in: Journal of Translational Medicine<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/10.1186/s12967-023-04073-y" target="_blank">https://dx.doi.org/10.1186/s12967-023-04073-y</a></p>2023-03-31T03:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1186/s12967-023-04073-yhttps://figshare.com/articles/journal_contribution/Treatment_with_decitabine_induces_the_expression_of_stemness_markers_PD-L1_and_NY-ESO-1_in_colorectal_cancer_potential_for_combined_chemoimmunotherapy/24941844CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/249418442023-03-31T03:00:00Z
spellingShingle Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
Nassiba Taib (14557385)
Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Reproductive medicine
Colorectal cancer
Decitabine
NY-ESO-1
PD-L1
Stemness markers
Chemoresistance
Immune escape
status_str publishedVersion
title Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
title_full Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
title_fullStr Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
title_full_unstemmed Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
title_short Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
title_sort Treatment with decitabine induces the expression of stemness markers, PD-L1 and NY-ESO-1 in colorectal cancer: potential for combined chemoimmunotherapy
topic Biological sciences
Biochemistry and cell biology
Biomedical and clinical sciences
Reproductive medicine
Colorectal cancer
Decitabine
NY-ESO-1
PD-L1
Stemness markers
Chemoresistance
Immune escape