A Review of ULK1-Mediated Autophagy in Drug Resistance of Cancer
Identifieur interne : 000915 ( Pmc/Curation ); précédent : 000914; suivant : 000916A Review of ULK1-Mediated Autophagy in Drug Resistance of Cancer
Auteurs : Li Liu ; Lu Yan ; Ning Liao ; Wan-Qin Wu ; Jun-Ling ShiSource :
- Cancers [ 2072-6694 ] ; 2020.
Abstract
The difficulty of early diagnosis and the development of drug resistance are two major barriers to the successful treatment of cancer. Autophagy plays a crucial role in several cellular functions, and its dysregulation is associated with both tumorigenesis and drug resistance. Unc-51-like kinase 1 (ULK1) is a serine/threonine kinase that participates in the initiation of autophagy. Many studies have indicated that compounds that directly or indirectly target ULK1 could be used for tumor therapy. However, reports of the therapeutic effects of these compounds have come to conflicting conclusions. In this work, we reviewed recent studies related to the effects of ULK1 on the regulation of autophagy and the development of drug resistance in cancers, with the aim of clarifying the mechanistic underpinnings of this therapeutic target.
Url:
DOI: 10.3390/cancers12020352
PubMed: 32033142
PubMed Central: 7073181
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<front><div type="abstract" xml:lang="en"><p>The difficulty of early diagnosis and the development of drug resistance are two major barriers to the successful treatment of cancer. Autophagy plays a crucial role in several cellular functions, and its dysregulation is associated with both tumorigenesis and drug resistance. Unc-51-like kinase 1 (ULK1) is a serine/threonine kinase that participates in the initiation of autophagy. Many studies have indicated that compounds that directly or indirectly target ULK1 could be used for tumor therapy. However, reports of the therapeutic effects of these compounds have come to conflicting conclusions. In this work, we reviewed recent studies related to the effects of ULK1 on the regulation of autophagy and the development of drug resistance in cancers, with the aim of clarifying the mechanistic underpinnings of this therapeutic target.</p>
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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">32033142</article-id>
<article-id pub-id-type="pmc">7073181</article-id>
<article-id pub-id-type="doi">10.3390/cancers12020352</article-id>
<article-id pub-id-type="publisher-id">cancers-12-00352</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>A Review of ULK1-Mediated Autophagy in Drug Resistance of Cancer</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Li</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Yan</surname>
<given-names>Lu</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Liao</surname>
<given-names>Ning</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Wu</surname>
<given-names>Wan-Qin</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Shi</surname>
<given-names>Jun-Ling</given-names>
</name>
<xref rid="c1-cancers-12-00352" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-cancers-12-00352">Key Laboratory for Space Bioscience and Biotechnology, School of Life Sciences, Northwestern Polytechnical University, 127 Youyi West Road, Xi’an 710072, China;<email>liuli3696352@mail.nwpu.edu.cn</email>
(L.L.);<email>1508271153@mail.nwpu.edu.cn</email>
(L.Y.);<email>liaoning@mail.nwpu.edu.cn</email>
(N.L.);<email>wuwanqin@mail.nwpu.edu.cn</email>
(W.-Q.W.)</aff>
<author-notes><corresp id="c1-cancers-12-00352"><label>*</label>
Correspondence: <email>sjlshi2004@nwpu.edu.cn</email>
; Tel./Fax: +86-029-8846-0543</corresp>
</author-notes>
<pub-date pub-type="epub"><day>04</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><month>2</month>
<year>2020</year>
</pub-date>
<volume>12</volume>
<issue>2</issue>
<elocation-id>352</elocation-id>
<history><date date-type="received"><day>05</day>
<month>1</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>31</day>
<month>1</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 by the authors.</copyright-statement>
<copyright-year>2020</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>The difficulty of early diagnosis and the development of drug resistance are two major barriers to the successful treatment of cancer. Autophagy plays a crucial role in several cellular functions, and its dysregulation is associated with both tumorigenesis and drug resistance. Unc-51-like kinase 1 (ULK1) is a serine/threonine kinase that participates in the initiation of autophagy. Many studies have indicated that compounds that directly or indirectly target ULK1 could be used for tumor therapy. However, reports of the therapeutic effects of these compounds have come to conflicting conclusions. In this work, we reviewed recent studies related to the effects of ULK1 on the regulation of autophagy and the development of drug resistance in cancers, with the aim of clarifying the mechanistic underpinnings of this therapeutic target.</p>
</abstract>
<kwd-group><kwd>ULK1</kwd>
<kwd>autophagy</kwd>
<kwd>cancer</kwd>
<kwd>drug resistance</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="cancers-12-00352-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Structure and biological function of ULK1. The domain of ULK1 contains three units including a kinase domain (KD), proline/serine-rich (PS) region, and C-terminal domain (CTD). AMPK and mTORC1 are upstream kinases that regulate ULK1. ATF4 is an activating transcription factor that directly regulates transcription of ULK1.</p>
</caption>
<graphic xlink:href="cancers-12-00352-g001"></graphic>
</fig>
<fig id="cancers-12-00352-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Summary of the relationships between ULK1, autophagy, and cancer.</p>
</caption>
<graphic xlink:href="cancers-12-00352-g002"></graphic>
</fig>
<fig id="cancers-12-00352-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>A summary of how ULK1 is involved in the development of drug resistance in cancer.</p>
</caption>
<graphic xlink:href="cancers-12-00352-g003"></graphic>
</fig>
<table-wrap id="cancers-12-00352-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-12-00352-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Identity of ULK1 in Homo sapiens as compared with its homologues in other model organisms [<xref rid="B28-cancers-12-00352" ref-type="bibr">28</xref>
,<xref rid="B29-cancers-12-00352" ref-type="bibr">29</xref>
,<xref rid="B30-cancers-12-00352" ref-type="bibr">30</xref>
,<xref rid="B31-cancers-12-00352" ref-type="bibr">31</xref>
,<xref rid="B32-cancers-12-00352" ref-type="bibr">32</xref>
,<xref rid="B33-cancers-12-00352" ref-type="bibr">33</xref>
,<xref rid="B34-cancers-12-00352" ref-type="bibr">34</xref>
,<xref rid="B40-cancers-12-00352" ref-type="bibr">40</xref>
].</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">Homologues Name</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Model Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Open Reading Frame (ORF)/Amino Acids</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">N-Terminal Kinase Domain/Residue</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Proline/Serine-Rich (PS)/Residue</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">C-Terminal Domains/Residue</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">ULK1</td>
<td align="center" valign="middle" rowspan="1" colspan="1"><italic>Homo sapiens</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1050</td>
<td align="center" valign="middle" rowspan="1" colspan="1">16–278</td>
<td align="center" valign="middle" rowspan="1" colspan="1">279–832</td>
<td align="center" valign="middle" rowspan="1" colspan="1">833–1050</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">ULK1</td>
<td align="center" valign="middle" rowspan="1" colspan="1"><italic>Mus. musculus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1051</td>
<td align="center" valign="middle" rowspan="1" colspan="1">26–278</td>
<td align="center" valign="middle" rowspan="1" colspan="1">279–828</td>
<td align="center" valign="middle" rowspan="1" colspan="1">829–1051</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">ULK2</td>
<td align="center" valign="middle" rowspan="1" colspan="1"><italic>Homo sapiens</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1036</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9–271</td>
<td align="center" valign="middle" rowspan="1" colspan="1">272–811</td>
<td align="center" valign="middle" rowspan="1" colspan="1">812–1036</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">ATG1</td>
<td align="center" valign="middle" rowspan="1" colspan="1"><italic>S. cerevisiae</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">897</td>
<td align="center" valign="middle" rowspan="1" colspan="1">24–325</td>
<td align="center" valign="middle" rowspan="1" colspan="1">326–740</td>
<td align="center" valign="middle" rowspan="1" colspan="1">741–897</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">UNC-51</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>C. elegans</italic>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">856</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">9–275</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">276–631</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">632–856</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="cancers-12-00352-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-12-00352-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>Induction factors, important autophagy-related proteins, and their relevance to different stages of autophagy in mammalian cells [<xref rid="B73-cancers-12-00352" ref-type="bibr">73</xref>
,<xref rid="B87-cancers-12-00352" ref-type="bibr">87</xref>
,<xref rid="B89-cancers-12-00352" ref-type="bibr">89</xref>
,<xref rid="B91-cancers-12-00352" ref-type="bibr">91</xref>
,<xref rid="B92-cancers-12-00352" ref-type="bibr">92</xref>
,<xref rid="B93-cancers-12-00352" ref-type="bibr">93</xref>
,<xref rid="B94-cancers-12-00352" ref-type="bibr">94</xref>
].</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">Induction Factors</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Autophagy Stages</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Complex</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Core Proteins of the Complex</th>
</tr>
</thead>
<tbody><tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><bold>Intrinsic cellular stress</bold>
: Reactive oxygen species (ROS), damaged organelles, protein aggregates, infected pathogens, AMP/ATP, endoplasmic reticulum stress and hypoxia, etc.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Induction of autophagy</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mTORC1 complex</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AMPK mTOR, RAPTOR, mLST8, PRAS40, DEPTOR, CASTOR1, SLC38A9, GATOR1</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nucleation and expansion of phagophore,<break></break>
Formation of autophagosomes</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK1-FIP200-ATG13complex<break></break>
Beclin-1-VPS15-VPS34-ATG14 l complex</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK1, ULK2, ATG13, ATG101, FIP200<break></break>
ATG9, VPS34, VPS15, BECN1, ATG14L, AMBRA, ATG5, ATG12, ATG16</td>
</tr>
<tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><bold>Extrinsic cellular stress:</bold>
Nutrients (amino acids, glucose, and oxygen), growth factors and drugs, etc.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fusion of autophagosome-lysosome fusion</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipidation complex</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">WIPI1/2, LC3, ATG3, ATG4, ATG7, ATG12, ATG16L, GABARAP</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Degradation of autophagic substrates</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">syntaxin-17, SNARE, VAMP8,<break></break>
SNAP29, RAB7, EPG5, HOPS,<break></break>
PLEKHM1</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="cancers-12-00352-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-12-00352-t003_Table 3</object-id>
<label>Table 3</label>
<caption><p>Small-molecule compounds targeting ULK1/ULK2-mediated autophagy in cancer.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Function</th>
<th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Compound</th>
<th colspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">In Vitro Kinase Assay (nM)</th>
<th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">CellularEC50/IC50 (nM)</th>
<th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Cell Type</th>
<th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Reference</th>
</tr>
<tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK1 IC<sub>50</sub>
</th>
<th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK2 IC<sub>50</sub>
</th>
</tr>
</thead>
<tbody><tr><td rowspan="12" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">ULK1/ULK2<break></break>
inhibitor</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Compound 1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5.3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">13</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B127-cancers-12-00352" ref-type="bibr">127</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Compound2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">67</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">200</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Compound 3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">120</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">360</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BX-795</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">87</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">310</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Compound 6</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">8</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B33-cancers-12-00352" ref-type="bibr">33</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MRT67307</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">45</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">38</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">MEFs</td>
<td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B128-cancers-12-00352" ref-type="bibr">128</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MRT68921</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2.9</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1.1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SBI0206965</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">38</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">212</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">EC50 = 2400</td>
<td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">U2OS cells</td>
<td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B135-cancers-12-00352" ref-type="bibr">135</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK100</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1.6</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2.6</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">EC50 = 83</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ULK101</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">8.3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">30</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">EC50 = 390</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NVP-BEZ235</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colon cancer cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B133-cancers-12-00352" ref-type="bibr">133</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATO -THAL</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">U93, KG-1 cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B134-cancers-12-00352" ref-type="bibr">134</xref>
]</td>
</tr>
<tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">ULK1/ULK2<break></break>
activator</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LYN-1604</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">18.94</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IC50 = 1.66 μM</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MDA-MB-231</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B136-cancers-12-00352" ref-type="bibr">136</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AEC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">150 μg/mL</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HT-29 cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B137-cancers-12-00352" ref-type="bibr">137</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="cancers-12-00352-t004" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-12-00352-t004_Table 4</object-id>
<label>Table 4</label>
<caption><p>Molecular events of ULK1-related cancer drug resistance.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="left" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Drug Resistance Cancer Cell Type</th>
<th align="left" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Event</th>
<th align="left" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Effects on Cancer Drug Resistance</th>
</tr>
</thead>
<tbody><tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Chronic myeloid leukemia (CML) resistance to tyrosine kinase inhibitors</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A mutation in the BCR-ABL protein; IIB02 producing significant cytotoxicity to BCR-ABL mutation cells BIIB021 inducing autophagic cell death by the downregulation of AKT-mTOR pathway and the activation of ULK1</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overcoming drug resistance</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colorectal cancer (CRC) resistance to selective BRAF inhibitors</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A mutation in BRAF protein; BRAF<sup>V600E</sup>
of colorectal cancer (CRC) develops drug resistance to selective BRAF inhibitors is that BRAF inhibitors induce cytoprotective autophagy through AMPK-ULK1 pathway</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibiting autophagy and overcoming drug resistance</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colorectal cancer cell resistance to 5-fluorouracil (5-FU)</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SNHG6 enhances chemoresistance through ULK1-induced autophagy via reducing free miR-26a-5p</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Inhibiting autophagy, SNHG6 knockdown or overexpression of miR-26a-5p, thus overcoming drug resistance</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Colon cancers resistance to KRAS drugs</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Two mitochondrial targeted compound 3-Carboxyl proxyl nitroxide (Mito-CP) and Mito-Metformin cause mitochondrial autophagy of KRAS cells by activating AMPK-ULK1 signaling cascade</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overcoming drug resistance of KRAS mutant cells </td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Non-small cell lung cancer (NSCLC) cells resistance to NK cell-mediated killing</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">The natural product rocaglamide (RocA) inhibited autophagy by targeting to ULK1 and restored the level of NK cell-derived GZMB (granzyme B) in NSCLC cells increasing their susceptibility to NK cell-mediated killing.</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overcoming resistance of NSCLC cells against NK cell-mediated killing</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Breast cancer cell resistance to doxorubicin (DOX), tamoxifen and cisplatin</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mir-489 directly targeting ULK1 and LAPTM4B genes, negatively regulating the expression of ULK1 and LAPTM4B inhibiting autophagy</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overcoming resistance to doxorubicin (DOX), tamoxifen and cisplatin</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NSCLC resistance to crizotinib</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HOTAIR (HOX transcript antisense intergenic RNA) is a high expression in NSCLC and promotes cisplatin resistance in NSCLC</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HOTAIR shRNA transfection overcoming the resistance of A549 cells to crizotinib by inhibiting autophagy activity decreasing the phosphorylation of ULK1</td>
</tr>
<tr><td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cisplatin-resistant NSCLC cells</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SBI0206965, as a selective inhibitor of ULK1 blocks cisplatin-induced autophagy and promotes cell death</td>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Overcoming NSCLC cells resistance to cisplatin</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
</record>
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