Systems biology of cisplatin resistance: past, present and future
Identifieur interne : 000029 ( Pmc/Curation ); précédent : 000028; suivant : 000030Systems biology of cisplatin resistance: past, present and future
Auteurs : L. Galluzzi [France] ; I. Vitale [Italie] ; J. Michels [France] ; C. Brenner [France] ; G. Szabadkai [Royaume-Uni, Italie] ; A. Harel-Bellan [France] ; M. Castedo [France] ; G. Kroemer [France]Source :
- Cell Death & Disease [ 2041-4889 ] ; 2014.
Abstract
The platinum derivative
Url:
DOI: 10.1038/cddis.2013.428
PubMed: 24874729
PubMed Central: 4047912
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<front><div type="abstract" xml:lang="en"><p>The platinum derivative <italic>cis</italic>
-diamminedichloroplatinum(II), best known as cisplatin, is currently employed for the clinical management of patients affected by testicular, ovarian, head and neck, colorectal, bladder and lung cancers. For a long time, the antineoplastic effects of cisplatin have been fully ascribed to its ability to generate unrepairable DNA lesions, hence inducing either a permanent proliferative arrest known as cellular senescence or the mitochondrial pathway of apoptosis. Accumulating evidence now suggests that the cytostatic and cytotoxic activity of cisplatin involves both a nuclear and a cytoplasmic component. Despite the unresolved issues regarding its mechanism of action, the administration of cisplatin is generally associated with high rates of clinical responses. However, in the vast majority of cases, malignant cells exposed to cisplatin activate a multipronged adaptive response that renders them less susceptible to the antiproliferative and cytotoxic effects of the drug, and eventually resume proliferation. Thus, a large fraction of cisplatin-treated patients is destined to experience therapeutic failure and tumor recurrence. Throughout the last four decades great efforts have been devoted to the characterization of the molecular mechanisms whereby neoplastic cells progressively lose their sensitivity to cisplatin. The advent of high-content and high-throughput screening technologies has accelerated the discovery of cell-intrinsic and cell-extrinsic pathways that may be targeted to prevent or reverse cisplatin resistance in cancer patients. Still, the multifactorial and redundant nature of this phenomenon poses a significant barrier against the identification of effective chemosensitization strategies. Here, we discuss recent systems biology studies aimed at deconvoluting the complex circuitries that underpin cisplatin resistance, and how their findings might drive the development of rational approaches to tackle this clinically relevant problem.</p>
</div>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Cell Death Dis</journal-id>
<journal-id journal-id-type="iso-abbrev">Cell Death Dis</journal-id>
<journal-title-group><journal-title>Cell Death & Disease</journal-title>
</journal-title-group>
<issn pub-type="epub">2041-4889</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">24874729</article-id>
<article-id pub-id-type="pmc">4047912</article-id>
<article-id pub-id-type="pii">cddis2013428</article-id>
<article-id pub-id-type="doi">10.1038/cddis.2013.428</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Systems biology of cisplatin resistance: past, present and future</article-title>
<alt-title alt-title-type="running">Systematic approaches to tackle CDDP resistance</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Galluzzi</surname>
<given-names>L</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="author-notes" rid="note1"><sup>16</sup>
</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vitale</surname>
<given-names>I</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
<xref ref-type="aff" rid="aff5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Michels</surname>
<given-names>J</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="aff" rid="aff6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Brenner</surname>
<given-names>C</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
<xref ref-type="aff" rid="aff8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Szabadkai</surname>
<given-names>G</given-names>
</name>
<xref ref-type="aff" rid="aff9">9</xref>
<xref ref-type="aff" rid="aff10">10</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Harel-Bellan</surname>
<given-names>A</given-names>
</name>
<xref ref-type="aff" rid="aff11">11</xref>
<xref ref-type="aff" rid="aff12">12</xref>
<xref ref-type="aff" rid="aff13">13</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Castedo</surname>
<given-names>M</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="aff" rid="aff6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kroemer</surname>
<given-names>G</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="aff" rid="aff6">6</xref>
<xref ref-type="aff" rid="aff14">14</xref>
<xref ref-type="aff" rid="aff15">15</xref>
<xref ref-type="author-notes" rid="note1"><sup>16</sup>
</xref>
<xref ref-type="corresp" rid="caf2">*</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Gustave Roussy</institution>
, Villejuif,<country>France</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>Université Paris Descartes/Paris V, Sorbonne Paris Cité</institution>
, Paris,<country>France</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>Equipe 11 labellisée par la Ligue Nationale contre le Cancer, Centre de Recherche des Cordeliers</institution>
, Paris,<country>France</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Regina Elena National Cancer Institute</institution>
, Rome,<country>Italy</country>
</aff>
<aff id="aff5"><label>5</label>
<institution>National Institute of Health</institution>
, Rome,<country>Italy</country>
</aff>
<aff id="aff6"><label>6</label>
<institution>INSERM, U848</institution>
, Villejuif,<country>France</country>
</aff>
<aff id="aff7"><label>7</label>
<institution>INSERM, UMRS 769; LabEx LERMIT</institution>
, Châtenay Malabry,<country>France</country>
</aff>
<aff id="aff8"><label>8</label>
<institution>Faculté de Pharmacie, Université de Paris Sud/Paris XI</institution>
, Châtenay Malabry,<country>France</country>
</aff>
<aff id="aff9"><label>9</label>
<institution>Department of Cell and Developmental Biology, Consortium for Mitochondrial Research, University College London</institution>
, London,<country>UK</country>
</aff>
<aff id="aff10"><label>10</label>
<institution>Department of Biomedical Sciences, Università Degli Studi di Padova</institution>
, Padova,<country>Italy</country>
</aff>
<aff id="aff11"><label>11</label>
<institution>Laboratoire Epigenetique et Cancer, Université de Paris Sud/Paris XI</institution>
, Gif-Sur-Yvette,<country>France</country>
</aff>
<aff id="aff12"><label>12</label>
<institution>CNRS, FRE3377</institution>
, Gif-Sur-Yvette,<country>France</country>
</aff>
<aff id="aff13"><label>13</label>
<institution>Commissariat à l'Energie Atomique (CEA)</institution>
, Saclay,<country>France</country>
</aff>
<aff id="aff14"><label>14</label>
<institution>Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP</institution>
, Paris,<country>France</country>
</aff>
<aff id="aff15"><label>15</label>
<institution>Metabolomics and Cell Biology Platforms, Gustave Roussy</institution>
, Villejuif,<country>France</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Université Paris Descartes/Paris V, INSERM, U848, Gustave Roussy</institution>
, PR1, 39, rue Camille Desmoulins, Villejuif F-94805, <country>France</country>
. Tel: +33 1 4211 4516; Fax: 33 1 4211 6665; E-mail: <email>deadoc@vodafone.it</email>
</corresp>
<corresp id="caf2"><label>*</label>
<institution>INSERM, U848, Gustave Roussy, PR1, 39, rue Camille Desmoulins</institution>
, Villejuif F-94805, <country>France</country>
. Tel: +33 1 4211 6046; Fax: +33 1 4211 6047; E-mail: <email>kroemer@orange.fr</email>
</corresp>
<fn fn-type="present-address" id="note1"><label>16</label>
<p>Share senior co-authorship.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>05</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="epub"><day>29</day>
<month>05</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>5</month>
<year>2014</year>
</pub-date>
<volume>5</volume>
<issue>5</issue>
<fpage>e1257</fpage>
<lpage></lpage>
<history><date date-type="received"><day>02</day>
<month>09</month>
<year>2013</year>
</date>
<date date-type="rev-recd"><day>23</day>
<month>09</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>26</day>
<month>09</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2014 Macmillan Publishers Limited</copyright-statement>
<copyright-year>2014</copyright-year>
<copyright-holder>Macmillan Publishers Limited</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/">http://creativecommons.org/licenses/by-nc-nd/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>The platinum derivative <italic>cis</italic>
-diamminedichloroplatinum(II), best known as cisplatin, is currently employed for the clinical management of patients affected by testicular, ovarian, head and neck, colorectal, bladder and lung cancers. For a long time, the antineoplastic effects of cisplatin have been fully ascribed to its ability to generate unrepairable DNA lesions, hence inducing either a permanent proliferative arrest known as cellular senescence or the mitochondrial pathway of apoptosis. Accumulating evidence now suggests that the cytostatic and cytotoxic activity of cisplatin involves both a nuclear and a cytoplasmic component. Despite the unresolved issues regarding its mechanism of action, the administration of cisplatin is generally associated with high rates of clinical responses. However, in the vast majority of cases, malignant cells exposed to cisplatin activate a multipronged adaptive response that renders them less susceptible to the antiproliferative and cytotoxic effects of the drug, and eventually resume proliferation. Thus, a large fraction of cisplatin-treated patients is destined to experience therapeutic failure and tumor recurrence. Throughout the last four decades great efforts have been devoted to the characterization of the molecular mechanisms whereby neoplastic cells progressively lose their sensitivity to cisplatin. The advent of high-content and high-throughput screening technologies has accelerated the discovery of cell-intrinsic and cell-extrinsic pathways that may be targeted to prevent or reverse cisplatin resistance in cancer patients. Still, the multifactorial and redundant nature of this phenomenon poses a significant barrier against the identification of effective chemosensitization strategies. Here, we discuss recent systems biology studies aimed at deconvoluting the complex circuitries that underpin cisplatin resistance, and how their findings might drive the development of rational approaches to tackle this clinically relevant problem.</p>
</abstract>
<kwd-group><kwd>BCL-2</kwd>
<kwd>carboplatin</kwd>
<kwd>CTR1</kwd>
<kwd>DNA damage response</kwd>
<kwd>oxaliplatin</kwd>
<kwd>p53</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Mode of action of cisplatin. As a result of the reduced cytoplasmic concentration of chloride ions, intracellular cisplatin (CDDP) is rapidly ‘aquated', hence acquiring a pronounced electrophilic reactivity. Aquated CDDP binds with high affinity to nuclear DNA, in particular to nucleophilic N7 sites on purines, thereby promoting the activation of the DNA damage response. In addition, CDDP can physically interact with several cytoplasmic nucleophiles, including mitochondrial DNA (mtDNA) as well as multiple mitochondrial and extramitochondrial proteins, hence (i) favoring the establishment of oxidative and reticular stress; (ii) eliciting a signal transduction cascade that involves the pro-apoptotic BCL-2 family members BAK1 and BAX, as well as voltage-dependent anion channel 1 (VDAC1) and (iii) activating the cytoplasmic pool of p53. The relative contribution of these nuclear and cytoplasmic modules to the cytostatic/cytotoxic activity of CDDP remains to be precisely elucidated and may exhibit an elevated degree of context dependency. Asterisks tag the primary consequences of CDDP reactivity. ER, endoplasmic reticulum; MOMP, mitochondrial outer membrane permeabilization</p>
</caption>
<graphic xlink:href="cddis2013428f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Molecular mechanisms of cisplatin resistance. Malignant cells can lose their sensitivity to the cytostatic/cytotoxic activity of cisplatin (CDDP) as a result of a wide panel of genetic or epigenetic defects. These alterations can (i) affect processes that precede the actual binding of CDDP to its targets (pre-target resistance); (ii) potentiate the ability of cells to repair the molecular damage caused by CDDP (on-target resistance); (iii) impair the transmission of signals that normally relay such a CDDP-induced damage to cell senescence or apoptosis (post-target resistance) or (iv) stimulate the delivery of pro-survival signals that antagonize CDDP cytotoxicity although they are normally not elicited by this drug (off-target resistance). Of note, CDDP resistance is generally multifactorial, that is, it relies on the activation of several, non-overlapping mechanisms that concur to limit the cytostatic/cytotoxic effects of CDDP at multiple levels. At least in part, this explains why efficient strategies to increase the sensitivity of human neoplasms to CDDP are still lacking in spite of a prolonged and intense wave of investigation. ATP7B, ATPase, Cu<sup>2+</sup>
transporting, <italic>β</italic>
polypeptide; CTR1, copper transporter 1; MRP2, multidrug resistance-associated protein 2; UPR, unfolded protein response. CDDP aquation is depicted in red</p>
</caption>
<graphic xlink:href="cddis2013428f2"></graphic>
</fig>
</floats-group>
</pmc>
</record>
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