Intrinsic Resistance to EGFR-Tyrosine Kinase Inhibitors in EGFR-Mutant Non-Small Cell Lung Cancer: Differences and Similarities with Acquired Resistance
Identifieur interne : 000890 ( Pmc/Curation ); précédent : 000889; suivant : 000891Intrinsic Resistance to EGFR-Tyrosine Kinase Inhibitors in EGFR-Mutant Non-Small Cell Lung Cancer: Differences and Similarities with Acquired Resistance
Auteurs : Eric Santoni-Rugiu [Danemark] ; Linea C. Melchior [Danemark] ; Edyta M. Urbanska [Danemark] ; Jan N. Jakobsen [Danemark] ; Karin De Stricker [Danemark] ; Morten Grauslund [Suède] ; Jens B. S Rensen [Danemark]Source :
- Cancers [ 2072-6694 ] ; 2019.
Abstract
Activating mutations in the
Url:
DOI: 10.3390/cancers11070923
PubMed: 31266248
PubMed Central: 6678669
Links toward previous steps (curation, corpus...)
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PMC:6678669Le document en format XML
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-Mutant Non-Small Cell Lung Cancer: Differences and Similarities with Acquired Resistance</title>
<author><name sortKey="Santoni Rugiu, Eric" sort="Santoni Rugiu, Eric" uniqKey="Santoni Rugiu E" first="Eric" last="Santoni-Rugiu">Eric Santoni-Rugiu</name>
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<author><name sortKey="Melchior, Linea C" sort="Melchior, Linea C" uniqKey="Melchior L" first="Linea C." last="Melchior">Linea C. Melchior</name>
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<author><name sortKey="De Stricker, Karin" sort="De Stricker, Karin" uniqKey="De Stricker K" first="Karin" last="De Stricker">Karin De Stricker</name>
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<author><name sortKey="Grauslund, Morten" sort="Grauslund, Morten" uniqKey="Grauslund M" first="Morten" last="Grauslund">Morten Grauslund</name>
<affiliation wicri:level="1"><nlm:aff id="af4-cancers-11-00923">Department of Clinical Genetics and Pathology, Skåne University Hospital, SE-221 85 Lund, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Department of Clinical Genetics and Pathology, Skåne University Hospital, SE-221 85 Lund</wicri:regionArea>
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<author><name sortKey="S Rensen, Jens B" sort="S Rensen, Jens B" uniqKey="S Rensen J" first="Jens B." last="S Rensen">Jens B. S Rensen</name>
<affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00923">Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Intrinsic Resistance to EGFR-Tyrosine Kinase Inhibitors in <italic>EGFR</italic>
-Mutant Non-Small Cell Lung Cancer: Differences and Similarities with Acquired Resistance</title>
<author><name sortKey="Santoni Rugiu, Eric" sort="Santoni Rugiu, Eric" uniqKey="Santoni Rugiu E" first="Eric" last="Santoni-Rugiu">Eric Santoni-Rugiu</name>
<affiliation wicri:level="1"><nlm:aff id="af1-cancers-11-00923">Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Melchior, Linea C" sort="Melchior, Linea C" uniqKey="Melchior L" first="Linea C." last="Melchior">Linea C. Melchior</name>
<affiliation wicri:level="1"><nlm:aff id="af1-cancers-11-00923">Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Urbanska, Edyta M" sort="Urbanska, Edyta M" uniqKey="Urbanska E" first="Edyta M." last="Urbanska">Edyta M. Urbanska</name>
<affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00923">Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Jakobsen, Jan N" sort="Jakobsen, Jan N" uniqKey="Jakobsen J" first="Jan N." last="Jakobsen">Jan N. Jakobsen</name>
<affiliation wicri:level="1"><nlm:aff id="af3-cancers-11-00923">Department of Oncology and Palliative Units, Zealand University Hospital, DK-4700 Næstved, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Oncology and Palliative Units, Zealand University Hospital, DK-4700 Næstved</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="De Stricker, Karin" sort="De Stricker, Karin" uniqKey="De Stricker K" first="Karin" last="De Stricker">Karin De Stricker</name>
<affiliation wicri:level="1"><nlm:aff id="af1-cancers-11-00923">Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Grauslund, Morten" sort="Grauslund, Morten" uniqKey="Grauslund M" first="Morten" last="Grauslund">Morten Grauslund</name>
<affiliation wicri:level="1"><nlm:aff id="af4-cancers-11-00923">Department of Clinical Genetics and Pathology, Skåne University Hospital, SE-221 85 Lund, Sweden</nlm:aff>
<country xml:lang="fr">Suède</country>
<wicri:regionArea>Department of Clinical Genetics and Pathology, Skåne University Hospital, SE-221 85 Lund</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="S Rensen, Jens B" sort="S Rensen, Jens B" uniqKey="S Rensen J" first="Jens B." last="S Rensen">Jens B. S Rensen</name>
<affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00923">Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</nlm:aff>
<country xml:lang="fr">Danemark</country>
<wicri:regionArea>Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Cancers</title>
<idno type="eISSN">2072-6694</idno>
<imprint><date when="2019">2019</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p>Activating mutations in the <italic>epidermal growth factor</italic>
<italic>receptor</italic>
gene occur as early cancer-driving clonal events in a subset of patients with non-small cell lung cancer (NSCLC) and result in increased sensitivity to EGFR-tyrosine-kinase-inhibitors (EGFR-TKIs). Despite very frequent and often prolonged clinical response to EGFR-TKIs, virtually all advanced <italic>EGFR</italic>
-mutated (<italic>EGFR</italic>
M+) NSCLCs inevitably acquire resistance mechanisms and progress at some point during treatment. Additionally, 20–30% of patients do not respond or respond for a very short time (<3 months) because of intrinsic resistance. While several mechanisms of acquired EGFR-TKI-resistance have been determined by analyzing tumor specimens obtained at disease progression, the factors causing intrinsic TKI-resistance are less understood. However, recent comprehensive molecular-pathological profiling of advanced <italic>EGFR</italic>
M+ NSCLC at baseline has illustrated the co-existence of multiple genetic, phenotypic, and functional mechanisms that may contribute to tumor progression and cause intrinsic TKI-resistance. Several of these mechanisms have been further corroborated by preclinical experiments. Intrinsic resistance can be caused by mechanisms inherent in <italic>EGFR</italic>
or by <italic>EGFR</italic>
-independent processes, including genetic, phenotypic or functional tumor changes. This comprehensive review describes the identified mechanisms connected with intrinsic EGFR-TKI-resistance and differences and similarities with acquired resistance and among clinically implemented EGFR-TKIs of different generations. Additionally, the review highlights the need for extensive pre-treatment molecular profiling of advanced NSCLC for identifying inherently TKI-resistant cases and designing potential combinatorial targeted strategies to treat them.</p>
</div>
</front>
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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">Cancers (Basel)</journal-id>
<journal-id journal-id-type="iso-abbrev">Cancers (Basel)</journal-id>
<journal-id journal-id-type="publisher-id">cancers</journal-id>
<journal-title-group><journal-title>Cancers</journal-title>
</journal-title-group>
<issn pub-type="epub">2072-6694</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31266248</article-id>
<article-id pub-id-type="pmc">6678669</article-id>
<article-id pub-id-type="doi">10.3390/cancers11070923</article-id>
<article-id pub-id-type="publisher-id">cancers-11-00923</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Intrinsic Resistance to EGFR-Tyrosine Kinase Inhibitors in <italic>EGFR</italic>
-Mutant Non-Small Cell Lung Cancer: Differences and Similarities with Acquired Resistance</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-2283-3535</contrib-id>
<name><surname>Santoni-Rugiu</surname>
<given-names>Eric</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-00923">1</xref>
<xref rid="c1-cancers-11-00923" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Melchior</surname>
<given-names>Linea C.</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-00923">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Urbanska</surname>
<given-names>Edyta M.</given-names>
</name>
<xref ref-type="aff" rid="af2-cancers-11-00923">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jakobsen</surname>
<given-names>Jan N.</given-names>
</name>
<xref ref-type="aff" rid="af3-cancers-11-00923">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Stricker</surname>
<given-names>Karin</given-names>
</name>
<xref ref-type="aff" rid="af1-cancers-11-00923">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Grauslund</surname>
<given-names>Morten</given-names>
</name>
<xref ref-type="aff" rid="af4-cancers-11-00923">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sørensen</surname>
<given-names>Jens B.</given-names>
</name>
<xref ref-type="aff" rid="af2-cancers-11-00923">2</xref>
</contrib>
</contrib-group>
<aff id="af1-cancers-11-00923"><label>1</label>
Department of Pathology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</aff>
<aff id="af2-cancers-11-00923"><label>2</label>
Department of Oncology, Rigshospitalet, Copenhagen University Hospital, DK-2100 Copenhagen, Denmark</aff>
<aff id="af3-cancers-11-00923"><label>3</label>
Department of Oncology and Palliative Units, Zealand University Hospital, DK-4700 Næstved, Denmark</aff>
<aff id="af4-cancers-11-00923"><label>4</label>
Department of Clinical Genetics and Pathology, Skåne University Hospital, SE-221 85 Lund, Sweden</aff>
<author-notes><corresp id="c1-cancers-11-00923"><label>*</label>
Correspondence: <email>eric.santoni-rugiu.02@regionh.dk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>01</day>
<month>7</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>7</month>
<year>2019</year>
</pub-date>
<volume>11</volume>
<issue>7</issue>
<elocation-id>923</elocation-id>
<history><date date-type="received"><day>19</day>
<month>4</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>25</day>
<month>6</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>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 (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>Activating mutations in the <italic>epidermal growth factor</italic>
<italic>receptor</italic>
gene occur as early cancer-driving clonal events in a subset of patients with non-small cell lung cancer (NSCLC) and result in increased sensitivity to EGFR-tyrosine-kinase-inhibitors (EGFR-TKIs). Despite very frequent and often prolonged clinical response to EGFR-TKIs, virtually all advanced <italic>EGFR</italic>
-mutated (<italic>EGFR</italic>
M+) NSCLCs inevitably acquire resistance mechanisms and progress at some point during treatment. Additionally, 20–30% of patients do not respond or respond for a very short time (<3 months) because of intrinsic resistance. While several mechanisms of acquired EGFR-TKI-resistance have been determined by analyzing tumor specimens obtained at disease progression, the factors causing intrinsic TKI-resistance are less understood. However, recent comprehensive molecular-pathological profiling of advanced <italic>EGFR</italic>
M+ NSCLC at baseline has illustrated the co-existence of multiple genetic, phenotypic, and functional mechanisms that may contribute to tumor progression and cause intrinsic TKI-resistance. Several of these mechanisms have been further corroborated by preclinical experiments. Intrinsic resistance can be caused by mechanisms inherent in <italic>EGFR</italic>
or by <italic>EGFR</italic>
-independent processes, including genetic, phenotypic or functional tumor changes. This comprehensive review describes the identified mechanisms connected with intrinsic EGFR-TKI-resistance and differences and similarities with acquired resistance and among clinically implemented EGFR-TKIs of different generations. Additionally, the review highlights the need for extensive pre-treatment molecular profiling of advanced NSCLC for identifying inherently TKI-resistant cases and designing potential combinatorial targeted strategies to treat them.</p>
</abstract>
<kwd-group><kwd>EGFR-mutated non-small cell lung cancer</kwd>
<kwd>EGFR-TKI</kwd>
<kwd>intrinsic resistance</kwd>
<kwd>resistance mechanisms</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="cancers-11-00923-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Summary of main molecular mechanisms of intrinsic resistance to EGFR-tyrosine-kinase-inhibitors (EGFR-TKIs) in <italic>EGFR</italic>
-mutated (<italic>EGFR</italic>
M+) non-small cell lung cancer (NSCLC). Given the clonal genetic heterogeneity of NSCLC, innate genetic alterations capable of impairing the response and causing intrinsic resistance to TKIs may be present in pre-existing clones before treatment (de novo alterations) or may be very rapidly induced in surviving cancer cells as immediate adaptive response or tolerance to the targeted therapy. If the relative allelic frequency of one or several (polyclonal resistance) of these pre-existing/immediately induced alterations is sufficient to very rapidly counteract the effect of TKIs (conventionally within the first 3 months after TKI-treatment initiation), tumor cells will continue to proliferate and survive, and intrinsic TKI-resistance will ensue. The EGFR-dependent resistance mechanisms are represented by amplification (<bold>Ampl</bold>
) and/or specific somatic or germline mutations (<bold>Mut</bold>
) of the <italic>EGFR</italic>
-gene. Some of these mutations cause resistance to EGFR-TKIs of all three generations, while others are sensitive to 2G or 3G TKIs, as indicated (* = EGFR-mutants resistant to 1G/2G EGFR-TKIs, but sensitive to 3G TKIs, the most common being <bold>T790M</bold>
indicated in bold; ** = EGFR-mutants resistant to 1G EGFR-TKIs, but sensitive to afatinib). Among the uncommon <italic>EGFR</italic>
-mutations G719X and insertions in exon 19 (Exon 19ins) are indicated in brackets, because despite being less sensitive than common EGFR-mutants, they may show some response to 1G TKIs. Instead, most of the EGFR-independent resistance mechanisms are shared by EGFR-TKIs of all three generations and include the activation of by-pass pathways via amplification (<bold>Ampl</bold>
), mutation (<bold>Mut</bold>
) or fusion (<bold>Fus</bold>
) of alternative parallel receptor tyrosine kinase- (RTK)-genes such as <italic>Mesenchymal-Epithelial Transition</italic>
(<italic>MET), Anaplastic Lymphoma Kinase (ALK)</italic>
, non-EGFR <italic>Erythroblastic Oncogene B</italic>
(<italic>ERBB)</italic>
-family-members, <italic>Fibroblast Growth Factor Receptor</italic>
genes (<italic>FGFR</italic>
s) (written in bold), and possibly <italic>REarranged during Transfection</italic>
(<italic>RET</italic>
) and <italic>Neurotrophic Tyrosine Receptor Kinase (NTRK)</italic>
(not in bold). Activation of parallel RTKs can also be induced by overexpression of hepatocyte growth factor (HGF) that binds the MET-receptor or Heregulin (Hrg) that binds ERBB2. Alternative downstream by-pass mechanisms of resistance are represented by mutations, fusions, or deletion (<bold>Del</bold>
) of members of the RAS-RAF-MEK-MAPK and PI3K-AKT-PTEN-mTOR pathways or inactivation of <italic>TP53</italic>
and/or <italic>retinoblastoma 1 (RB1)</italic>
tumor-suppressor genes via mutation/deletion/epigenetic mechanism (<bold>Epigen</bold>
) or indirectly by gene-amplification of the p53-inhibitor Mouse Double Minute 2 homolog (MDM2) and mutation/amplification of genes encoding cyclins and cyclin-dependent kinases (CDKs). Additional by-pass mechanisms are activation (<bold>Act</bold>
) of the NF-κB transcription factor by different pathways or impairment of TKI-induced apoptosis by loss of the pro-apoptotic <italic>BIM</italic>
-gene expression due to genetic polymorphism (<bold>Polym</bold>
) or transcriptional downregulation (<bold>Downreg</bold>
). Putative mechanisms of intrinsic (and acquired) resistance to all three generations’ TKIs that await further clinical validation are phenotypic changes, such as epithelial-mesenchymal transition (EMT), transformation to small-cell lung cancer (SCLC) or squamous cell carcinomas (SqCC), and potential functional changes reducing TKI efficacy, like rapidly increased autophagic activity, drug-efflux or intracellular drug-sequestration in cancer cells. Some evidence for NSCLC cases with pre-existing, inherently TKI-resistant cells due to upregulation (Upreg; in brackets) of the EMT-inducing RTK AXL has also been provided. RTKs are in light blue, intracellular downstream oncoproteins in white boxes, tumor suppressors in yellow symbols.</p>
</caption>
<graphic xlink:href="cancers-11-00923-g001"></graphic>
</fig>
<table-wrap id="cancers-11-00923-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-00923-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p><italic>EGFR</italic>
-mutations associated with reduced response or primary resistance to EGFR-TKIs in NSCLC.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Somatic Mutation (Amino Acid Position)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Exon </th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Effect on EGFR-TKIs</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Other Features</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">G719X<break></break>
S768I<break></break>
L861Q</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">18<break></break>
20<break></break>
21</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Reduced response to 1G TKIs in pts. & preclinical models.<break></break>
Sensitive to afatinib.<break></break>
Osimertinib less effective in pts. or cell lines with these mutants than in those with classic EGFR-mutants, regardless of presence of T790M co-mutation. </td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Significantly less sensitive than L858R & exon 19dels but do show some response to 1G TKIs.<break></break>
Can co-occur together or with sensitizing mutations, especially L858R.<break></break>
The rare variant L861P reported co-existing with L858R in pts. not responding to 1G EGFR-TKIs.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B54-cancers-11-00923" ref-type="bibr">54</xref>
,<xref rid="B76-cancers-11-00923" ref-type="bibr">76</xref>
,<xref rid="B81-cancers-11-00923" ref-type="bibr">81</xref>
,<xref rid="B83-cancers-11-00923" ref-type="bibr">83</xref>
,<xref rid="B87-cancers-11-00923" ref-type="bibr">87</xref>
,<xref rid="B89-cancers-11-00923" ref-type="bibr">89</xref>
,<xref rid="B90-cancers-11-00923" ref-type="bibr">90</xref>
,<xref rid="B92-cancers-11-00923" ref-type="bibr">92</xref>
,<xref rid="B94-cancers-11-00923" ref-type="bibr">94</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">L747P</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">19</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Intrinsic resistance to EGFR-TKIs of all three generations</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Very rare, resistance mechanism unclear.<break></break>
The variant L747S occasionally reported both as secondary TKI-resistant mutant in the setting of acquired TKI-resistance and as de novo mutation in cases with co-existing L858R not responding to 1G EGFR-TKIs.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B54-cancers-11-00923" ref-type="bibr">54</xref>
,<xref rid="B57-cancers-11-00923" ref-type="bibr">57</xref>
,<xref rid="B58-cancers-11-00923" ref-type="bibr">58</xref>
,<xref rid="B86-cancers-11-00923" ref-type="bibr">86</xref>
,<xref rid="B99-cancers-11-00923" ref-type="bibr">99</xref>
,<xref rid="B101-cancers-11-00923" ref-type="bibr">101</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Exon 19 insertions</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">19</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Unclear (very rare, require further investigations) </td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Some epidemiological evidence for lower TKI-sensitivity than common EGFR-mutations.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B51-cancers-11-00923" ref-type="bibr">51</xref>
,<xref rid="B97-cancers-11-00923" ref-type="bibr">97</xref>
,<xref rid="B98-cancers-11-00923" ref-type="bibr">98</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Exon 20 insertions</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">20</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Poor response to 1G/2G TKIs; in vitro appear responsive to osimertinib & single cases were reported sensitive to osimertinib. </td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A763_Y764insFQEA is an exception, as structurally resembles L858R & is sensitive to TKIs.<break></break>
In preclinical models, exon 20ins responded to cetuximab + afatinib or osimertinib.<break></break>
Cases responding to afatinib + cetuximab have been reported.<break></break>
Promising results in vitro and in vivo from new selective TKIs targeting EGFR and ERBB2 exon 20 insertions, such as poziotinib, TAS6417, and TAK-788.<break></break>
Heat shock protein 90 inhibitors also potentially active against NSCLC cells with EGFR exon 20ins.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B83-cancers-11-00923" ref-type="bibr">83</xref>
,<xref rid="B86-cancers-11-00923" ref-type="bibr">86</xref>
,<xref rid="B87-cancers-11-00923" ref-type="bibr">87</xref>
,<xref rid="B103-cancers-11-00923" ref-type="bibr">103</xref>
,<xref rid="B104-cancers-11-00923" ref-type="bibr">104</xref>
,<xref rid="B106-cancers-11-00923" ref-type="bibr">106</xref>
,<xref rid="B108-cancers-11-00923" ref-type="bibr">108</xref>
,<xref rid="B110-cancers-11-00923" ref-type="bibr">110</xref>
,<xref rid="B112-cancers-11-00923" ref-type="bibr">112</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">T790M</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">20</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Resistant to 1G/2G TKIs, sensitive to 3G TKIs.</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Present as de novo mutation, either alone or with a common sensitizing mutation such as L858R.<break></break>
Amplification of T790M-positive EGFR may provide further TKI-resistance.<break></break>
High relative abundance of T790M predicts poor response to 1G/2G TKIs but may predict better response to 3G TKIs. </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B51-cancers-11-00923" ref-type="bibr">51</xref>
,<xref rid="B54-cancers-11-00923" ref-type="bibr">54</xref>
,<xref rid="B57-cancers-11-00923" ref-type="bibr">57</xref>
,<xref rid="B61-cancers-11-00923" ref-type="bibr">61</xref>
,<xref rid="B62-cancers-11-00923" ref-type="bibr">62</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Germline T790M</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">20</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Resistant to 1G/2G TKIs, sensitive to 3G TKIs.</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Predominantly in females, non-smokers with a secondary somatic EGFR-mutation. </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B115-cancers-11-00923" ref-type="bibr">115</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Germline V843I</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">21</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Resistant to 1G/2G TKIs, possibly sensitive to 3G TKIs.</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">As T790M sterically hinders TKI-binding to EGFR.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B113-cancers-11-00923" ref-type="bibr">113</xref>
,<xref rid="B114-cancers-11-00923" ref-type="bibr">114</xref>
,<xref rid="B115-cancers-11-00923" ref-type="bibr">115</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
</record>
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