Long Noncoding Competing Endogenous RNA Networks in Age-Associated Cardiovascular Diseases
Identifieur interne : 000631 ( Pmc/Checkpoint ); précédent : 000630; suivant : 000632Long Noncoding Competing Endogenous RNA Networks in Age-Associated Cardiovascular Diseases
Auteurs : Simona Greco [Italie] ; Carlo Gaetano ; Fabio Martelli [Italie]Source :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2019.
Abstract
Cardiovascular diseases (CVDs) are the most serious health problem in the world, displaying high rates of morbidity and mortality. One of the main risk factors for CVDs is age. Indeed, several mechanisms are at play during aging, determining the functional decline of the cardiovascular system. Aging cells and tissues are characterized by diminished autophagy, causing the accumulation of damaged proteins and mitochondria, as well as by increased levels of oxidative stress, apoptosis, senescence and inflammation. These processes can induce a rapid deterioration of cellular quality-control systems. However, the molecular mechanisms of age-associated CVDs are only partially known, hampering the development of novel therapeutic strategies. Evidence has emerged indicating that noncoding RNAs (ncRNAs), such as long ncRNAs (lncRNAs) and micro RNAs (miRNAs), are implicated in most patho-physiological mechanisms. Specifically, lncRNAs can bind miRNAs and act as competing endogenous-RNAs (ceRNAs), therefore modulating the levels of the mRNAs targeted by the sponged miRNA. These complex lncRNA/miRNA/mRNA networks, by regulating autophagy, apoptosis, necrosis, senescence and inflammation, play a crucial role in the development of age-dependent CVDs. In this review, the emerging knowledge on lncRNA/miRNA/mRNA networks will be summarized and the way in which they influence age-related CVDs development will be discussed.
Url:
DOI: 10.3390/ijms20123079
PubMed: 31238513
PubMed Central: 6627372
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Cardiovascular diseases (CVDs) are the most serious health problem in the world, displaying high rates of morbidity and mortality. One of the main risk factors for CVDs is age. Indeed, several mechanisms are at play during aging, determining the functional decline of the cardiovascular system. Aging cells and tissues are characterized by diminished autophagy, causing the accumulation of damaged proteins and mitochondria, as well as by increased levels of oxidative stress, apoptosis, senescence and inflammation. These processes can induce a rapid deterioration of cellular quality-control systems. However, the molecular mechanisms of age-associated CVDs are only partially known, hampering the development of novel therapeutic strategies. Evidence has emerged indicating that noncoding RNAs (ncRNAs), such as long ncRNAs (lncRNAs) and micro RNAs (miRNAs), are implicated in most patho-physiological mechanisms. Specifically, lncRNAs can bind miRNAs and act as competing endogenous-RNAs (ceRNAs), therefore modulating the levels of the mRNAs targeted by the sponged miRNA. These complex lncRNA/miRNA/mRNA networks, by regulating autophagy, apoptosis, necrosis, senescence and inflammation, play a crucial role in the development of age-dependent CVDs. In this review, the emerging knowledge on lncRNA/miRNA/mRNA networks will be summarized and the way in which they influence age-related CVDs development will be discussed.</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">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31238513</article-id>
<article-id pub-id-type="pmc">6627372</article-id>
<article-id pub-id-type="doi">10.3390/ijms20123079</article-id>
<article-id pub-id-type="publisher-id">ijms-20-03079</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Long Noncoding Competing Endogenous RNA Networks in Age-Associated Cardiovascular Diseases</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Greco</surname>
<given-names>Simona</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03079">1</xref>
<xref rid="c1-ijms-20-03079" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gaetano</surname>
<given-names>Carlo</given-names>
</name>
<xref ref-type="aff" rid="af2-ijms-20-03079">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-8624-7738</contrib-id>
<name><surname>Martelli</surname>
<given-names>Fabio</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-03079">1</xref>
<xref rid="c1-ijms-20-03079" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-ijms-20-03079"><label>1</label>
Molecular Cardiology Laboratory, IRCCS Policlinico San Donato, San Donato Milanese, 20097 Milan, Italy</aff>
<aff id="af2-ijms-20-03079"><label>2</label>
Laboratory of Epigenetics, Istituti Clinici Scientifici Maugeri IRCCS, 27100 Pavia, Italy;<email>carlo.gaetano@icsmaugeri.it</email>
</aff>
<author-notes><corresp id="c1-ijms-20-03079"><label>*</label>
Correspondence: <email>simona.greco@grupposandonato.it</email>
(S.G.); <email>fabio.martelli@grupposandonato.it</email>
(F.M.); Tel.: +39-02-2643-7762 (F.M.)</corresp>
</author-notes>
<pub-date pub-type="epub"><day>24</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>6</month>
<year>2019</year>
</pub-date>
<volume>20</volume>
<issue>12</issue>
<elocation-id>3079</elocation-id>
<history><date date-type="received"><day>29</day>
<month>5</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>21</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>Cardiovascular diseases (CVDs) are the most serious health problem in the world, displaying high rates of morbidity and mortality. One of the main risk factors for CVDs is age. Indeed, several mechanisms are at play during aging, determining the functional decline of the cardiovascular system. Aging cells and tissues are characterized by diminished autophagy, causing the accumulation of damaged proteins and mitochondria, as well as by increased levels of oxidative stress, apoptosis, senescence and inflammation. These processes can induce a rapid deterioration of cellular quality-control systems. However, the molecular mechanisms of age-associated CVDs are only partially known, hampering the development of novel therapeutic strategies. Evidence has emerged indicating that noncoding RNAs (ncRNAs), such as long ncRNAs (lncRNAs) and micro RNAs (miRNAs), are implicated in most patho-physiological mechanisms. Specifically, lncRNAs can bind miRNAs and act as competing endogenous-RNAs (ceRNAs), therefore modulating the levels of the mRNAs targeted by the sponged miRNA. These complex lncRNA/miRNA/mRNA networks, by regulating autophagy, apoptosis, necrosis, senescence and inflammation, play a crucial role in the development of age-dependent CVDs. In this review, the emerging knowledge on lncRNA/miRNA/mRNA networks will be summarized and the way in which they influence age-related CVDs development will be discussed.</p>
</abstract>
<kwd-group><kwd>cardiovascular disease</kwd>
<kwd>aging</kwd>
<kwd>microRNA</kwd>
<kwd>long noncoding RNA</kwd>
<kwd>competing endogenous RNA</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="ijms-20-03079-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Cardiovascular function deterioration by ageing. (<bold>A</bold>
) <italic>Vascular function impairment by ageing.</italic>
The loss of aorta distensibility with ageing is associated to: (1) increased collagen deposition; (2) the depletion of elastin; (3) the non-enzymatic glycosylation of collagen, which results in the cross-linking of adjacent proteins; (4) amyloid deposition in the medial layer; (5) migration/proliferation of VSMCs and (6) endothelial hyperplasia. The impaired distensibility is responsible for the development of hypertension and decreased coronary perfusion. (<bold>B</bold>
) <italic>Cardiac function impairment by ageing.</italic>
The ageing process of the cardiac system is characterized by a reduction of both peak cardiac-output and left ventricular (LV) diastolic function, an altered response to catecholamine, an incomplete relaxation during early diastolic filling, and increased myocardial stiffness. These responses are compensated by increased muscle mass that leads to cardiac hypertrophy and LV wall thickening. This compensatory mechanism enhances cardiac output at the beginning, but reduces the cardiac function as hypertrophy increases. Fibroblast activation to myofibroblast, increased apoptosis, collagen deposition and crosslinking, inflammatory cells migration and perivascular fibrosis are frequent histologic findings in the old myocardium.</p>
</caption>
<graphic xlink:href="ijms-20-03079-g001a"></graphic>
<graphic xlink:href="ijms-20-03079-g001b"></graphic>
</fig>
<fig id="ijms-20-03079-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Competitive interactions between lncRNAs, miRNAs and mRNAs. The presence of miRNA response elements (MREs) allows the binding of miRNAs, which results in the inhibition of mRNA expression and/or stability. In addition, lncRNAs acting as ceRNAs harbor MREs and function as “sponges” for the miRNAs, which are sequestered so that the miRNA-RISC is unable to regulate the expression of target mRNAs. Thus, by acting as ceRNAs, lncRNAs are competitors for the binding of miRNA to the mRNA targets.</p>
</caption>
<graphic xlink:href="ijms-20-03079-g002"></graphic>
</fig>
<fig id="ijms-20-03079-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>LncRNA-miRNA-mRNA networks and autophagy. A decrease in autophagic function is a hallmark of ageing. A variety of stimuli, such as hypoxia or ischemia/reperfusion, oxidized lipoproteins (ox-LDL) or treatment with an MTOR pathway agonist (3BDO), can activate the interaction of lncRNA and miRNA, and the specific modulation of direct and/or indirect targets that, in turn, can affect positively or negatively the autophagic process.</p>
</caption>
<graphic xlink:href="ijms-20-03079-g003"></graphic>
</fig>
<fig id="ijms-20-03079-f004" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>LncRNA-miRNA-mRNA networks and inflammation. During ageing, there is an increased accumulation of inflammatory molecules as well as a burst in oxidative stress. A prolonged state of inflammation can be detrimental for cardiovascular tissue and it can predispose to atherogenesis. Indeed, an increase in inflammatory cytokines and chemokines leads to the internalization of oxidized lipoproteins (ox-LDL) with transformation in foam cells, both contributing to tissue injury. The figure summarizes in vitro experiments performed in endothelial cells (ECs), macrophages cells (M∅) and cardiomyocytes (CMs).</p>
</caption>
<graphic xlink:href="ijms-20-03079-g004"></graphic>
</fig>
<fig id="ijms-20-03079-f005" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>LncRNA-miRNA-mRNA networks and senescence. Cellular senescence is associated with the release of a large number of pro-inflammatory cytokines and growth factors. These factors cause an increased burden of tissue inflammation and oxidative stress that contribute to telomere shortening. Moreover, telomere shortening and cellular senescence are involved in aging and in the development of CVDs. The figure shows that the senescence phenotype can be induced by: (1) ageing the endothelial cells by culturing until late passages (p9) (2) stimulating cardiomyocytes (CMs) with D-galactose and (3) treating vascular smooth muscle cells (VSMCs) with high glucose. The lncRNA-miRNA-mRNA networks triggered by these conditions stimulate or inhibit senescence according to the modulated targets.</p>
</caption>
<graphic xlink:href="ijms-20-03079-g005"></graphic>
</fig>
<table-wrap id="ijms-20-03079-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">ijms-20-03079-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>LncRNA/miRNA/mRNA networks and ageing mechanisms involved in cardiovascular diseases.</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">Process</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">lncRNA</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">miRNA</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Prediction Tool</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">miRNA Target (Direct/Indirect)</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Pathology/Condition</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody><tr><td rowspan="8" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Autophagy</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">APF</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-188-3p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RNAhybrid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATG7 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-A/R in mouse CMs <break></break>
-I/R (mouse)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B71-ijms-20-03079" ref-type="bibr">71</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AK088388</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-30a</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miRANDA TargetScan</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Beclin-1 (direct) <break></break>
LC3-II (indirect)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-H/R in mouse CMs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B72-ijms-20-03079" ref-type="bibr">72</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">AK139328</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-204-3p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATG proteins (indirect)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Diabetic mouse <break></break>
-I/R (mouse)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B73-ijms-20-03079" ref-type="bibr">73</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BACE1-AS</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-29/miR-107/miR-124/miR-485/miR-761</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miRANDA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BACE1 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-human DCM <break></break>
-HAOECs <break></break>
-mouse cardiomyocytes</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B51-ijms-20-03079" ref-type="bibr">51</xref>
,<xref rid="B74-ijms-20-03079" ref-type="bibr">74</xref>
,<xref rid="B75-ijms-20-03079" ref-type="bibr">75</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Galont</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-338</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RNAhybrid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATG5 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">A/R cardiomyocytes (mouse)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B76-ijms-20-03079" ref-type="bibr">76</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GAS5</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-26a</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RNAhybrid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATG proteins (indirect)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-ox-LDL stimulation of human ECs <break></break>
-plasma of AS patients</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B77-ijms-20-03079" ref-type="bibr">77</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGFB2-OT1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-4459</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mirbase MicroInspector</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ATG13 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-3BDO stimulation of human ECs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B78-ijms-20-03079" ref-type="bibr">78</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">UCA1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-128</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HSP70 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-I/R (mouse) <break></break>
-H/R in mouse CMs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B79-ijms-20-03079" ref-type="bibr">79</xref>
]</td>
</tr>
<tr><td rowspan="8" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Inflammation</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GAS5</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-26a</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Starbase v2.0 <break></break>
LncBase Predicted v.2 tool</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HMGB1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-PA treated mouse CMs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B80-ijms-20-03079" ref-type="bibr">80</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GAS5</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-221</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IL-1β, TNF-α, MMP-2, MMP-9 (indirect)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Ox/LDL stimulation of THP-1 human cells <break></break>
-Human AS plaques</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B81-ijms-20-03079" ref-type="bibr">81</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H19</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">let-7</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Periostin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Ox/LDL stimulation of human HUVEC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B82-ijms-20-03079" ref-type="bibr">82</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">HOTAIR</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-34a</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miRANDA</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SIRT1 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-STZ mice <break></break>
-high glucose treated rat CMs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B83-ijms-20-03079" ref-type="bibr">83</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MALAT-1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-155</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TargetScan</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">SOCS1 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">- ox-LDL stimulation of human HAOECs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B84-ijms-20-03079" ref-type="bibr">84</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RNCR3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-185-5p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TargetScan</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">KLF-2 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Human aortic lesions <break></break>
-Aorta from apoE<sup>−/−</sup>
mice <break></break>
- ox-LDL stimulation of human EC and VSMCs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B85-ijms-20-03079" ref-type="bibr">85</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">RP5-833A20.1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-382-5p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miRBase, <break></break>
PicTar, <break></break>
TargetScan, <break></break>
RNAhybrid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NFIA (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Ox/Ac-LDL stimulation of THP-1 human cells <break></break>
-Aorta from apoE<sup>−/−</sup>
mice</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B86-ijms-20-03079" ref-type="bibr">86</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TGFB2-OT1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-4459</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MicroInspector</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LARP/CERS1/ NAT8L/ ATG13 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-LPS/ox-LDL stimulation of human ECs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B87-ijms-20-03079" ref-type="bibr">87</xref>
]</td>
</tr>
<tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Senescence</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GAS5</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-223</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miRWalk <break></break>
miRANDA <break></break>
TargetScan <break></break>
microT-CDS</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NAMPT (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Human EPCs (late passages)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B88-ijms-20-03079" ref-type="bibr">88</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H19</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-29b-3p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">cIAP1 (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-D-galactose/H-Post treatment of CMs <break></break>
-I/Post (mouse)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B89-ijms-20-03079" ref-type="bibr">89</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">LncRNA-ES3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-34c-5p</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">BMF</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-high glucose stimulated human aorta VSMCs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B90-ijms-20-03079" ref-type="bibr">90</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MEG3</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">miR-128</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nd</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">GIRDIN (direct)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Coronary artery aged mice <break></break>
-HUVECs (late passages)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B91-ijms-20-03079" ref-type="bibr">91</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Abbreviations: A/R = Anoxia/reperfusion; AS = aortic stenosis; CMs = cardiomyocytes; DCM = dilated cardiomyopathy; ECs = endothelial cells; EPCs = endothelial precursor cells; HAOECs = human aortic endothelial cells; H-Post = hypoxia-postconditioning; H/R = hypoxia/reperfusion; HUVECs = human umbilical endothelial cells; I-Post = ischemia-postconditioning; I/R = Ischemia/reperfusion; LPS = lipopolysaccharide; ox-LDL= oxidized low density lipoprotein; PA = palmitic acid; STZ = streptozotocin; VSMCs = vascular smooth muscle cells; 3BDO = 3-benzyl-5-((2-nitrophenoxy) methyl)-dihydrofuran-2(3H)-one.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Italie</li>
</country>
<region><li>Lombardie</li>
</region>
<settlement><li>Milan</li>
</settlement>
</list>
<tree><noCountry><name sortKey="Gaetano, Carlo" sort="Gaetano, Carlo" uniqKey="Gaetano C" first="Carlo" last="Gaetano">Carlo Gaetano</name>
</noCountry>
<country name="Italie"><region name="Lombardie"><name sortKey="Greco, Simona" sort="Greco, Simona" uniqKey="Greco S" first="Simona" last="Greco">Simona Greco</name>
</region>
<name sortKey="Martelli, Fabio" sort="Martelli, Fabio" uniqKey="Martelli F" first="Fabio" last="Martelli">Fabio Martelli</name>
</country>
</tree>
</affiliations>
</record>
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