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Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect

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Resumo:Advanced urothelial bladder cancer (UBC) patients are tagged by a dismal prognosis and high mortality rates, mostly due to their poor response to standard-of-care platinum-based therapy. Mediators of chemoresistance are not fully elucidated. This work aimed to study the metabolic profile of advanced UBC, in the context of cisplatin resistance. Three isogenic pairs of parental cell lines (T24, HT1376 and KU1919) and the matching cisplatin-resistant (R) sublines were used. A set of functional assays was used to perform a metabolic screening on the cells. In comparison to the parental sublines, a tendency was observed towards an exacerbated glycolytic metabolism in the cisplatin-resistant T24 and HT1376 cells; this glycolytic phenotype was particularly evident for the HT1376/HT1376R pair, for which the cisplatin resistance ratio was higher. HT1376R cells showed decreased basal respiration and oxygen consumption associated with ATP production; in accordance, the extracellular acidification rate was also higher in the resistant subline. Glycolytic rate assay confirmed that these cells presented higher basal glycolysis, with an increase in proton efflux. While the results of real-time metabolomics seem to substantiate the manifestation of the Warburg phenotype in HT1376R cells, a shift towards distinct metabolic pathways involving lactate uptake, lipid biosynthesis and glutamate metabolism occurred with time. On the other hand, KU1919R cells seem to engage in a metabolic rewiring, recovering their preference for oxidative phosphorylation. In conclusion, cisplatin-resistant UBC cells seem to display deep metabolic alterations surpassing the Warburg effect, which likely depend on the molecular signature of each cell line.
Autores principais:Afonso, Julieta Alexandra Pereira
Outros Autores:Matos, Ana Catarina Barbosa; Silvestre, Ricardo Jorge Leal; Pereira-Vieira, Joana; Gonçalves, Samuel Martins; Mendes-Alves, Camille; Parpot, Pier; Pinto, Joana; Carapito, Ângela; Guedes de Pinho, Paula; Santos, Lúcio; Longatto-Filho, Adhemar; Baltazar, Fátima
Assunto:Urothelial bladder cancer Cisplatin resistance Warburg effect Glucose Lactate Lipid metabolism Glutamate
Ano:2024
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso aberto
Instituição associada:Universidade do Minho
Idioma:inglês
Origem:RepositóriUM - Universidade do Minho
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author Afonso, Julieta Alexandra Pereira
author2 Matos, Ana Catarina Barbosa
Silvestre, Ricardo Jorge Leal
Pereira-Vieira, Joana
Gonçalves, Samuel Martins
Mendes-Alves, Camille
Parpot, Pier
Pinto, Joana
Carapito, Ângela
Guedes de Pinho, Paula
Santos, Lúcio
Longatto-Filho, Adhemar
Baltazar, Fátima
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author_facet Afonso, Julieta Alexandra Pereira
Matos, Ana Catarina Barbosa
Silvestre, Ricardo Jorge Leal
Pereira-Vieira, Joana
Gonçalves, Samuel Martins
Mendes-Alves, Camille
Parpot, Pier
Pinto, Joana
Carapito, Ângela
Guedes de Pinho, Paula
Santos, Lúcio
Longatto-Filho, Adhemar
Baltazar, Fátima
author_role author
contributor_name_str_mv Universidade do Minho
country_str PT
creators_json_txt [{\"Person.name\":\"Afonso, Julieta Alexandra Pereira\"},{\"Person.name\":\"Matos, Ana Catarina Barbosa\"},{\"Person.name\":\"Silvestre, Ricardo Jorge Leal\"},{\"Person.name\":\"Pereira-Vieira, Joana\"},{\"Person.name\":\"Gonçalves, Samuel Martins\"},{\"Person.name\":\"Mendes-Alves, Camille\"},{\"Person.name\":\"Parpot, Pier\"},{\"Person.name\":\"Pinto, Joana\"},{\"Person.name\":\"Carapito, Ângela\"},{\"Person.name\":\"Guedes de Pinho, Paula\"},{\"Person.name\":\"Santos, Lúcio\"},{\"Person.name\":\"Longatto-Filho, Adhemar\"},{\"Person.name\":\"Baltazar, Fátima\"}]
datacite.contributors.contributor.contributorName.fl_str_mv Universidade do Minho
datacite.creators.creator.creatorName.fl_str_mv Afonso, Julieta Alexandra Pereira
Matos, Ana Catarina Barbosa
Silvestre, Ricardo Jorge Leal
Pereira-Vieira, Joana
Gonçalves, Samuel Martins
Mendes-Alves, Camille
Parpot, Pier
Pinto, Joana
Carapito, Ângela
Guedes de Pinho, Paula
Santos, Lúcio
Longatto-Filho, Adhemar
Baltazar, Fátima
datacite.date.Accepted.fl_str_mv 2024-04-05T00:00:00Z
datacite.date.available.fl_str_mv 2024-05-31T14:16:02Z
datacite.date.embargoed.fl_str_mv 2024-05-31T14:16:02Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_abf2
datacite.subjects.subject.fl_str_mv Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
datacite.titles.title.fl_str_mv Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
dc.contributor.none.fl_str_mv Universidade do Minho
dc.creator.none.fl_str_mv Afonso, Julieta Alexandra Pereira
Matos, Ana Catarina Barbosa
Silvestre, Ricardo Jorge Leal
Pereira-Vieira, Joana
Gonçalves, Samuel Martins
Mendes-Alves, Camille
Parpot, Pier
Pinto, Joana
Carapito, Ângela
Guedes de Pinho, Paula
Santos, Lúcio
Longatto-Filho, Adhemar
Baltazar, Fátima
dc.date.Accepted.fl_str_mv 2024-04-05T00:00:00Z
dc.date.available.fl_str_mv 2024-05-31T14:16:02Z
dc.date.embargoed.fl_str_mv 2024-05-31T14:16:02Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv https://hdl.handle.net/1822/91633
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute (MDPI)
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.subject.none.fl_str_mv Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
dc.title.fl_str_mv Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Advanced urothelial bladder cancer (UBC) patients are tagged by a dismal prognosis and high mortality rates, mostly due to their poor response to standard-of-care platinum-based therapy. Mediators of chemoresistance are not fully elucidated. This work aimed to study the metabolic profile of advanced UBC, in the context of cisplatin resistance. Three isogenic pairs of parental cell lines (T24, HT1376 and KU1919) and the matching cisplatin-resistant (R) sublines were used. A set of functional assays was used to perform a metabolic screening on the cells. In comparison to the parental sublines, a tendency was observed towards an exacerbated glycolytic metabolism in the cisplatin-resistant T24 and HT1376 cells; this glycolytic phenotype was particularly evident for the HT1376/HT1376R pair, for which the cisplatin resistance ratio was higher. HT1376R cells showed decreased basal respiration and oxygen consumption associated with ATP production; in accordance, the extracellular acidification rate was also higher in the resistant subline. Glycolytic rate assay confirmed that these cells presented higher basal glycolysis, with an increase in proton efflux. While the results of real-time metabolomics seem to substantiate the manifestation of the Warburg phenotype in HT1376R cells, a shift towards distinct metabolic pathways involving lactate uptake, lipid biosynthesis and glutamate metabolism occurred with time. On the other hand, KU1919R cells seem to engage in a metabolic rewiring, recovering their preference for oxidative phosphorylation. In conclusion, cisplatin-resistant UBC cells seem to display deep metabolic alterations surpassing the Warburg effect, which likely depend on the molecular signature of each cell line.
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eu_rights_str_mv openAccess
format article
fulltext.url.fl_str_mv https://repositorium.uminho.pt/bitstreams/ff0558b7-a5b2-4700-bfb4-df43fe419be6/download
id rum_e4e2b5a52e29b0578d050e2f98c4cd12
identifier.url.fl_str_mv https://hdl.handle.net/1822/91633
instacron_str repositorium
institution Universidade do Minho
instname_str Universidade do Minho
language eng
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network_name_str RepositóriUM - Universidade do Minho
oai_identifier_str oai:repositorium.uminho.pt:1822/91633
organization_str_mv urn:organizationAcronym:repositorium
person_str_mv Afonso, Julieta Alexandra Pereira
Matos, Ana Catarina Barbosa
Silvestre, Ricardo Jorge Leal
Pereira-Vieira, Joana
Gonçalves, Samuel Martins
Mendes-Alves, Camille
Parpot, Pier
Pinto, Joana
Carapito, Ângela
Guedes de Pinho, Paula
Santos, Lúcio
Longatto-Filho, Adhemar
Baltazar, Fátima
publishDate 2024
publisher.none.fl_str_mv Multidisciplinary Digital Publishing Institute (MDPI)
reponame_str RepositóriUM - Universidade do Minho
repository_id_str urn:repositoryAcronym:rum
service_str_mv urn:repositoryAcronym:rum
spelling engMultidisciplinary Digital Publishing Institute (MDPI)porAdvanced urothelial bladder cancer (UBC) patients are tagged by a dismal prognosis and high mortality rates, mostly due to their poor response to standard-of-care platinum-based therapy. Mediators of chemoresistance are not fully elucidated. This work aimed to study the metabolic profile of advanced UBC, in the context of cisplatin resistance. Three isogenic pairs of parental cell lines (T24, HT1376 and KU1919) and the matching cisplatin-resistant (R) sublines were used. A set of functional assays was used to perform a metabolic screening on the cells. In comparison to the parental sublines, a tendency was observed towards an exacerbated glycolytic metabolism in the cisplatin-resistant T24 and HT1376 cells; this glycolytic phenotype was particularly evident for the HT1376/HT1376R pair, for which the cisplatin resistance ratio was higher. HT1376R cells showed decreased basal respiration and oxygen consumption associated with ATP production; in accordance, the extracellular acidification rate was also higher in the resistant subline. Glycolytic rate assay confirmed that these cells presented higher basal glycolysis, with an increase in proton efflux. While the results of real-time metabolomics seem to substantiate the manifestation of the Warburg phenotype in HT1376R cells, a shift towards distinct metabolic pathways involving lactate uptake, lipid biosynthesis and glutamate metabolism occurred with time. On the other hand, KU1919R cells seem to engage in a metabolic rewiring, recovering their preference for oxidative phosphorylation. In conclusion, cisplatin-resistant UBC cells seem to display deep metabolic alterations surpassing the Warburg effect, which likely depend on the molecular signature of each cell line.application/pdfporCisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effectAfonso, Julieta Alexandra PereiraMatos, Ana Catarina BarbosaSilvestre, Ricardo Jorge LealPereira-Vieira, JoanaGonçalves, Samuel MartinsMendes-Alves, CamilleParpot, PierPinto, JoanaCarapito, ÂngelaGuedes de Pinho, PaulaSantos, LúcioLongatto-Filho, AdhemarBaltazar, FátimaHostingInstitutionOrganizationalUniversidade do Minhoe-mailmailto:repositorium@usdb.uminho.ptrepositorium@usdb.uminho.ptISSNIsPartOf2072-6694DOIIsPartOf10.3390/cancers160714182024-05-31T14:16:02Z2024-04-052024-05-14T19:15:58Z2024-04-05T00:00:00ZHandlehttps://hdl.handle.net/1822/91633http://purl.org/coar/access_right/c_abf2open accessUrothelial bladder cancerCisplatin resistanceWarburg effectGlucoseLactateLipid metabolismGlutamate5543109 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal articlehttp://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://repositorium.uminho.pt/bitstreams/ff0558b7-a5b2-4700-bfb4-df43fe419be6/download
spellingShingle Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
Afonso, Julieta Alexandra Pereira
Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
status SINGLETON
subject.fl_str_mv Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
title Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
title_full Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
title_fullStr Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
title_full_unstemmed Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
title_short Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
title_sort Cisplatin-resistant urothelial bladder cancer cells undergo metabolic reprogramming beyond the Warburg effect
topic Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
topic_facet Urothelial bladder cancer
Cisplatin resistance
Warburg effect
Glucose
Lactate
Lipid metabolism
Glutamate
url https://hdl.handle.net/1822/91633
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