Honey Targets Ribosome Biogenesis Components to Suppress the Growth of Human Pancreatic Cancer Cells
Pancreatic cancer (PanCa) is one of the deadliest cancers, with limited therapeutic response. Various molecular oncogenic events, including dysregulation of ribosome biogenesis, are linked to the induction, progression, and metastasis of PanCa. Thus, the discovery of new therapies suppressing these...
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| Veröffentlicht in: | Cancers 2024-10, Vol.16 (19), p.3431 |
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| creator | Bangash, Aun Ali Alvi, Sahir Sultan Bangash, Muhammad Ali Ahsan, Haider Khan, Shiza Shareef, Rida Villanueva, Georgina Bansal, Divyam Ahmad, Mudassier Kim, Dae Joon Chauhan, Subhash C Hafeez, Bilal Bin |
| description | Pancreatic cancer (PanCa) is one of the deadliest cancers, with limited therapeutic response. Various molecular oncogenic events, including dysregulation of ribosome biogenesis, are linked to the induction, progression, and metastasis of PanCa. Thus, the discovery of new therapies suppressing these oncogenic events and ribosome biogenesis could be a novel therapeutic approach for the prevention and treatment of PanCa. The current study was designed to investigate the anti-cancer effect of honey against PanCa. Our results indicated that honey markedly inhibited the growth and invasive characteristics of pancreatic cancer cells by suppressing the mRNA expression and protein levels of key components of ribosome biogenesis, including RNA Pol-I subunits (RPA194 and RPA135) along with its transcriptional regulators, i.e., UBTF and c-Myc. Honey also induced nucleolar stress in PanCa cells by reducing the expression of various nucleolar proteins (NCL, FBL, and NPM). Honey-mediated regulation on ribosome biogenesis components and nucleolar organization-associated proteins significantly arrested the cell cycle in the G2M phase and induced apoptosis in PanCa cells. These results, for the first time, demonstrated that honey, being a natural remedy, has the potential to induce apoptosis and inhibit the growth and metastatic phenotypes of PanCa by targeting ribosome biogenesis. |
| doi_str_mv | 10.3390/cancers16193431 |
| format | Article |
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Various molecular oncogenic events, including dysregulation of ribosome biogenesis, are linked to the induction, progression, and metastasis of PanCa. Thus, the discovery of new therapies suppressing these oncogenic events and ribosome biogenesis could be a novel therapeutic approach for the prevention and treatment of PanCa. The current study was designed to investigate the anti-cancer effect of honey against PanCa. Our results indicated that honey markedly inhibited the growth and invasive characteristics of pancreatic cancer cells by suppressing the mRNA expression and protein levels of key components of ribosome biogenesis, including RNA Pol-I subunits (RPA194 and RPA135) along with its transcriptional regulators, i.e., UBTF and c-Myc. Honey also induced nucleolar stress in PanCa cells by reducing the expression of various nucleolar proteins (NCL, FBL, and NPM). Honey-mediated regulation on ribosome biogenesis components and nucleolar organization-associated proteins significantly arrested the cell cycle in the G2M phase and induced apoptosis in PanCa cells. These results, for the first time, demonstrated that honey, being a natural remedy, has the potential to induce apoptosis and inhibit the growth and metastatic phenotypes of PanCa by targeting ribosome biogenesis.</description><identifier>ISSN: 2072-6694</identifier><identifier>EISSN: 2072-6694</identifier><identifier>DOI: 10.3390/cancers16193431</identifier><identifier>PMID: 39410048</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Antibiotics ; Apoptosis ; Biosynthesis ; c-Myc protein ; Cancer cells ; Care and treatment ; Cell cycle ; Cell organelles ; Cyclin-dependent kinases ; Development and progression ; Diabetes ; Formation ; Gene expression ; Growth ; Health aspects ; Honey ; Immunotherapy ; Invasiveness ; Kinases ; Medical prognosis ; Metabolites ; Metastases ; Molecular modelling ; Mutation ; Myc protein ; Nucleoli ; Oxidative stress ; Pancreatic cancer ; Phenotypes ; Proteins ; Radiation therapy ; Ribonucleic acid ; Ribosomes ; RNA ; Testing ; Toxicity ; Transcription factors ; Yeast</subject><ispartof>Cancers, 2024-10, Vol.16 (19), p.3431</ispartof><rights>COPYRIGHT 2024 MDPI AG</rights><rights>2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 by the authors. 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c373t-70a4563ec5c8a2a653b0039953ed5d3db20f2f2dc1dea6ac2148b91332cb86833</cites><orcidid>0000-0002-5650-748X ; 0009-0000-7361-1337 ; 0009-0000-4739-1721 ; 0009-0002-3757-9629 ; 0009-0008-4555-0766 ; 0000-0002-7977-9955</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11475701/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11475701/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,886,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39410048$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bangash, Aun Ali</creatorcontrib><creatorcontrib>Alvi, Sahir Sultan</creatorcontrib><creatorcontrib>Bangash, Muhammad Ali</creatorcontrib><creatorcontrib>Ahsan, Haider</creatorcontrib><creatorcontrib>Khan, Shiza</creatorcontrib><creatorcontrib>Shareef, Rida</creatorcontrib><creatorcontrib>Villanueva, Georgina</creatorcontrib><creatorcontrib>Bansal, Divyam</creatorcontrib><creatorcontrib>Ahmad, Mudassier</creatorcontrib><creatorcontrib>Kim, Dae Joon</creatorcontrib><creatorcontrib>Chauhan, Subhash C</creatorcontrib><creatorcontrib>Hafeez, Bilal Bin</creatorcontrib><title>Honey Targets Ribosome Biogenesis Components to Suppress the Growth of Human Pancreatic Cancer Cells</title><title>Cancers</title><addtitle>Cancers (Basel)</addtitle><description>Pancreatic cancer (PanCa) is one of the deadliest cancers, with limited therapeutic response. Various molecular oncogenic events, including dysregulation of ribosome biogenesis, are linked to the induction, progression, and metastasis of PanCa. Thus, the discovery of new therapies suppressing these oncogenic events and ribosome biogenesis could be a novel therapeutic approach for the prevention and treatment of PanCa. The current study was designed to investigate the anti-cancer effect of honey against PanCa. Our results indicated that honey markedly inhibited the growth and invasive characteristics of pancreatic cancer cells by suppressing the mRNA expression and protein levels of key components of ribosome biogenesis, including RNA Pol-I subunits (RPA194 and RPA135) along with its transcriptional regulators, i.e., UBTF and c-Myc. Honey also induced nucleolar stress in PanCa cells by reducing the expression of various nucleolar proteins (NCL, FBL, and NPM). Honey-mediated regulation on ribosome biogenesis components and nucleolar organization-associated proteins significantly arrested the cell cycle in the G2M phase and induced apoptosis in PanCa cells. These results, for the first time, demonstrated that honey, being a natural remedy, has the potential to induce apoptosis and inhibit the growth and metastatic phenotypes of PanCa by targeting ribosome biogenesis.</description><subject>Antibiotics</subject><subject>Apoptosis</subject><subject>Biosynthesis</subject><subject>c-Myc protein</subject><subject>Cancer cells</subject><subject>Care and treatment</subject><subject>Cell cycle</subject><subject>Cell organelles</subject><subject>Cyclin-dependent kinases</subject><subject>Development and progression</subject><subject>Diabetes</subject><subject>Formation</subject><subject>Gene expression</subject><subject>Growth</subject><subject>Health aspects</subject><subject>Honey</subject><subject>Immunotherapy</subject><subject>Invasiveness</subject><subject>Kinases</subject><subject>Medical prognosis</subject><subject>Metabolites</subject><subject>Metastases</subject><subject>Molecular modelling</subject><subject>Mutation</subject><subject>Myc protein</subject><subject>Nucleoli</subject><subject>Oxidative stress</subject><subject>Pancreatic cancer</subject><subject>Phenotypes</subject><subject>Proteins</subject><subject>Radiation therapy</subject><subject>Ribonucleic acid</subject><subject>Ribosomes</subject><subject>RNA</subject><subject>Testing</subject><subject>Toxicity</subject><subject>Transcription factors</subject><subject>Yeast</subject><issn>2072-6694</issn><issn>2072-6694</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNptUsFu1DAQtRCIVqVnbsgSFy7b2p7ETk6oRKWLVAnUlrPlOJNdV4kd7ATUv6-XllVbYR888rx5895oCHnP2QlAzU6t8RZj4pLXUAB_RQ4FU2IlZV28fhIfkOOUblk-AFxJ9ZYcQF1wxorqkHTr4PGO3pi4wTnRK9eGFEakX1zYoMfkEm3COGWQz-k50OtlmiKmHG-RXsTwZ97S0NP1MhpPf2RFEc3sLG3-iqMNDkN6R970Zkh4_PgekZ9fz2-a9ery-8W35uxyZUHBvFLMFKUEtKWtjDCyhDZrrusSsCs76FrBetGLzvIOjTRW8KJqaw4gbFvJCuCIfH7gnZZ2xM5mzdEMeopuNPFOB-P084x3W70JvzXnhSoV45nh0yNDDL8WTLMeXbLZg_EYlqSBc8WUEiAy9OML6G1Yos_-dihZqgKymT1qYwbUzvchN7Y7Un1WcSF5drzjOvkPKt8OR2fz8HuX_58VnD4U2BhSitjvTXKmd8uhXyxHrvjwdDZ7_L9VgHtgPbVY</recordid><startdate>20241009</startdate><enddate>20241009</enddate><creator>Bangash, Aun Ali</creator><creator>Alvi, Sahir Sultan</creator><creator>Bangash, Muhammad Ali</creator><creator>Ahsan, Haider</creator><creator>Khan, Shiza</creator><creator>Shareef, Rida</creator><creator>Villanueva, Georgina</creator><creator>Bansal, Divyam</creator><creator>Ahmad, Mudassier</creator><creator>Kim, Dae Joon</creator><creator>Chauhan, Subhash C</creator><creator>Hafeez, Bilal Bin</creator><general>MDPI AG</general><general>MDPI</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7T5</scope><scope>7TO</scope><scope>7XB</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>COVID</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-5650-748X</orcidid><orcidid>https://orcid.org/0009-0000-7361-1337</orcidid><orcidid>https://orcid.org/0009-0000-4739-1721</orcidid><orcidid>https://orcid.org/0009-0002-3757-9629</orcidid><orcidid>https://orcid.org/0009-0008-4555-0766</orcidid><orcidid>https://orcid.org/0000-0002-7977-9955</orcidid></search><sort><creationdate>20241009</creationdate><title>Honey Targets Ribosome Biogenesis Components to Suppress the Growth of Human Pancreatic Cancer Cells</title><author>Bangash, Aun Ali ; 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Various molecular oncogenic events, including dysregulation of ribosome biogenesis, are linked to the induction, progression, and metastasis of PanCa. Thus, the discovery of new therapies suppressing these oncogenic events and ribosome biogenesis could be a novel therapeutic approach for the prevention and treatment of PanCa. The current study was designed to investigate the anti-cancer effect of honey against PanCa. Our results indicated that honey markedly inhibited the growth and invasive characteristics of pancreatic cancer cells by suppressing the mRNA expression and protein levels of key components of ribosome biogenesis, including RNA Pol-I subunits (RPA194 and RPA135) along with its transcriptional regulators, i.e., UBTF and c-Myc. Honey also induced nucleolar stress in PanCa cells by reducing the expression of various nucleolar proteins (NCL, FBL, and NPM). Honey-mediated regulation on ribosome biogenesis components and nucleolar organization-associated proteins significantly arrested the cell cycle in the G2M phase and induced apoptosis in PanCa cells. These results, for the first time, demonstrated that honey, being a natural remedy, has the potential to induce apoptosis and inhibit the growth and metastatic phenotypes of PanCa by targeting ribosome biogenesis.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>39410048</pmid><doi>10.3390/cancers16193431</doi><orcidid>https://orcid.org/0000-0002-5650-748X</orcidid><orcidid>https://orcid.org/0009-0000-7361-1337</orcidid><orcidid>https://orcid.org/0009-0000-4739-1721</orcidid><orcidid>https://orcid.org/0009-0002-3757-9629</orcidid><orcidid>https://orcid.org/0009-0008-4555-0766</orcidid><orcidid>https://orcid.org/0000-0002-7977-9955</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; MDPI - Multidisciplinary Digital Publishing Institute; PubMed Central |
| subjects | Antibiotics Apoptosis Biosynthesis c-Myc protein Cancer cells Care and treatment Cell cycle Cell organelles Cyclin-dependent kinases Development and progression Diabetes Formation Gene expression Growth Health aspects Honey Immunotherapy Invasiveness Kinases Medical prognosis Metabolites Metastases Molecular modelling Mutation Myc protein Nucleoli Oxidative stress Pancreatic cancer Phenotypes Proteins Radiation therapy Ribonucleic acid Ribosomes RNA Testing Toxicity Transcription factors Yeast |
| title | Honey Targets Ribosome Biogenesis Components to Suppress the Growth of Human Pancreatic Cancer Cells |
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