Regulation of Intrinsic Axon Growth Ability at Retinal Ganglion Cell Growth Cones
Identifieur interne : 000765 ( Pmc/Checkpoint ); précédent : 000764; suivant : 000766Regulation of Intrinsic Axon Growth Ability at Retinal Ganglion Cell Growth Cones
Auteurs : Michael B. Steketee [États-Unis] ; Carly Oboudiyat [États-Unis] ; Richard Daneman [États-Unis] ; Ephraim Trakhtenberg [États-Unis] ; Philip Lamoureux [États-Unis] ; Jessica E. Weinstein [États-Unis] ; Steve Heidemann [États-Unis] ; Ben A. Barres [États-Unis] ; Jeffrey L. Goldberg [États-Unis]Source :
- Investigative Ophthalmology & Visual Science [ 0146-0404 ] ; 2014.
Abstract
Mammalian central nervous system neurons fail to regenerate after injury or disease, in part due to a progressive loss in intrinsic axon growth ability after birth. Whether lost axon growth ability is due to limited growth resources or to changes in the axonal growth cone is unknown.
Static and time-lapse images of purified retinal ganglion cells (RGCs) were analyzed for axon growth rate and growth cone morphology and dynamics without treatment and after manipulating Kruppel-like transcription factor (KLF) expression or applying mechanical tension.
Retinal ganglion cells undergo a developmental switch in growth cone dynamics that mirrors the decline in postnatal axon growth rates, with increased filopodial adhesion and decreased lamellar protrusion area in postnatal axonal growth cones. Moreover, expressing growth-suppressive KLF4 or growth-enhancing KLF6 transcription factors elicits similar changes in postnatal growth cones that correlate with axon growth rates. Postnatal RGC axon growth rate is not limited by an inability to achieve axon growth rates similar to embryonic RGCs; indeed, postnatal axons support elongation rates up to 100-fold faster than postnatal axonal growth rates. Rather, the intrinsic capacity for rapid axon growth is due to both growth cone pausing and retraction, as well as to a slightly decreased ability to achieve rapid instantaneous rates of forward progression. Finally, we observed that RGC axon and dendrite growth are regulated independently in vitro.
Together, these data support the hypothesis that intrinsic axon growth rate is regulated by an axon-specific growth program that differentially regulates growth cone motility.
Url:
DOI: 10.1167/iovs.14-13882
PubMed: 24906860
PubMed Central: 4102390
Affiliations:
- États-Unis
- Californie, Floride, Michigan, Pennsylvanie
- East Lansing, Pittsburgh
- Université d'État du Michigan, Université de Pittsburgh
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Steketee</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2">Department of Ophthalmology and McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Ophthalmology and McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Oboudiyat, Carly" sort="Oboudiyat, Carly" uniqKey="Oboudiyat C" first="Carly" last="Oboudiyat">Carly Oboudiyat</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Daneman, Richard" sort="Daneman, Richard" uniqKey="Daneman R" first="Richard" last="Daneman">Richard Daneman</name><affiliation wicri:level="2"><nlm:aff id="aff3">Department of Neurobiology, Stanford University School of Medicine, Stanford, California, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Neurobiology, Stanford University School of Medicine, Stanford, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Trakhtenberg, Ephraim" sort="Trakhtenberg, Ephraim" uniqKey="Trakhtenberg E" first="Ephraim" last="Trakhtenberg">Ephraim Trakhtenberg</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Lamoureux, Philip" sort="Lamoureux, Philip" uniqKey="Lamoureux P" first="Philip" last="Lamoureux">Philip Lamoureux</name><affiliation wicri:level="4"><nlm:aff id="aff4">Department of Physiology, Michigan State University, East Lansing, Michigan, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology, Michigan State University, East Lansing, Michigan</wicri:regionArea><placeName><region type="state">Michigan</region><settlement type="city">East Lansing</settlement></placeName><orgName type="university">Université d'État du Michigan</orgName></affiliation></author><author><name sortKey="Weinstein, Jessica E" sort="Weinstein, Jessica E" uniqKey="Weinstein J" first="Jessica E." last="Weinstein">Jessica E. 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Steketee</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff2">Department of Ophthalmology and McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Ophthalmology and McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">Pittsburgh</settlement></placeName><orgName type="university">Université de Pittsburgh</orgName></affiliation></author><author><name sortKey="Oboudiyat, Carly" sort="Oboudiyat, Carly" uniqKey="Oboudiyat C" first="Carly" last="Oboudiyat">Carly Oboudiyat</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Daneman, Richard" sort="Daneman, Richard" uniqKey="Daneman R" first="Richard" last="Daneman">Richard Daneman</name><affiliation wicri:level="2"><nlm:aff id="aff3">Department of Neurobiology, Stanford University School of Medicine, Stanford, California, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Neurobiology, Stanford University School of Medicine, Stanford, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Trakhtenberg, Ephraim" sort="Trakhtenberg, Ephraim" uniqKey="Trakhtenberg E" first="Ephraim" last="Trakhtenberg">Ephraim Trakhtenberg</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Lamoureux, Philip" sort="Lamoureux, Philip" uniqKey="Lamoureux P" first="Philip" last="Lamoureux">Philip Lamoureux</name><affiliation wicri:level="4"><nlm:aff id="aff4">Department of Physiology, Michigan State University, East Lansing, Michigan, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology, Michigan State University, East Lansing, Michigan</wicri:regionArea><placeName><region type="state">Michigan</region><settlement type="city">East Lansing</settlement></placeName><orgName type="university">Université d'État du Michigan</orgName></affiliation></author><author><name sortKey="Weinstein, Jessica E" sort="Weinstein, Jessica E" uniqKey="Weinstein J" first="Jessica E." last="Weinstein">Jessica E. Weinstein</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation></author><author><name sortKey="Heidemann, Steve" sort="Heidemann, Steve" uniqKey="Heidemann S" first="Steve" last="Heidemann">Steve Heidemann</name><affiliation wicri:level="4"><nlm:aff id="aff4">Department of Physiology, Michigan State University, East Lansing, Michigan, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Physiology, Michigan State University, East Lansing, Michigan</wicri:regionArea><placeName><region type="state">Michigan</region><settlement type="city">East Lansing</settlement></placeName><orgName type="university">Université d'État du Michigan</orgName></affiliation></author><author><name sortKey="Barres, Ben A" sort="Barres, Ben A" uniqKey="Barres B" first="Ben A." last="Barres">Ben A. Barres</name><affiliation wicri:level="2"><nlm:aff id="aff3">Department of Neurobiology, Stanford University School of Medicine, Stanford, California, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Neurobiology, Stanford University School of Medicine, Stanford, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Goldberg, Jeffrey L" sort="Goldberg, Jeffrey L" uniqKey="Goldberg J" first="Jeffrey L." last="Goldberg">Jeffrey L. Goldberg</name><affiliation wicri:level="2"><nlm:aff id="aff1">Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida</wicri:regionArea><placeName><region type="state">Floride</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff5">Department of Ophthalmology, Shiley Eye Center, University of California San Diego, San Diego, California, United States</nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Ophthalmology, Shiley Eye Center, University of California San Diego, San Diego, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">Investigative Ophthalmology & Visual Science</title><idno type="ISSN">0146-0404</idno><idno type="eISSN">1552-5783</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec id="st1"><title>Purpose.</title><p>Mammalian central nervous system neurons fail to regenerate after injury or disease, in part due to a progressive loss in intrinsic axon growth ability after birth. Whether lost axon growth ability is due to limited growth resources or to changes in the axonal growth cone is unknown.</p></sec><sec id="st2"><title>Methods.</title><p>Static and time-lapse images of purified retinal ganglion cells (RGCs) were analyzed for axon growth rate and growth cone morphology and dynamics without treatment and after manipulating Kruppel-like transcription factor (KLF) expression or applying mechanical tension.</p></sec><sec id="st3"><title>Results.</title><p>Retinal ganglion cells undergo a developmental switch in growth cone dynamics that mirrors the decline in postnatal axon growth rates, with increased filopodial adhesion and decreased lamellar protrusion area in postnatal axonal growth cones. Moreover, expressing growth-suppressive KLF4 or growth-enhancing KLF6 transcription factors elicits similar changes in postnatal growth cones that correlate with axon growth rates. Postnatal RGC axon growth rate is not limited by an inability to achieve axon growth rates similar to embryonic RGCs; indeed, postnatal axons support elongation rates up to 100-fold faster than postnatal axonal growth rates. Rather, the intrinsic capacity for rapid axon growth is due to both growth cone pausing and retraction, as well as to a slightly decreased ability to achieve rapid instantaneous rates of forward progression. Finally, we observed that RGC axon and dendrite growth are regulated independently in vitro.</p></sec><sec id="st4"><title>Conclusions.</title><p>Together, these data support the hypothesis that intrinsic axon growth rate is regulated by an axon-specific growth program that differentially regulates growth cone motility.</p></sec></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Invest Ophthalmol Vis Sci</journal-id><journal-id journal-id-type="iso-abbrev">Invest. Ophthalmol. Vis. Sci</journal-id><journal-id journal-id-type="hwp">iovs</journal-id><journal-id journal-id-type="pmc">iovs</journal-id><journal-id journal-id-type="publisher-id">IOVS</journal-id><journal-title-group><journal-title>Investigative Ophthalmology & Visual Science</journal-title></journal-title-group><issn pub-type="ppub">0146-0404</issn><issn pub-type="epub">1552-5783</issn><publisher><publisher-name>The Association for Research in Vision and Ophthalmology</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24906860</article-id><article-id pub-id-type="pmc">4102390</article-id><article-id pub-id-type="doi">10.1167/iovs.14-13882</article-id><article-id pub-id-type="sici">iovs-55-06-23</article-id><article-id pub-id-type="other">IOVS-14-13882</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject><subj-group><subject>Retinal Cell Biology</subject></subj-group></subj-group></article-categories><title-group><article-title>Regulation of Intrinsic Axon Growth Ability at Retinal Ganglion Cell Growth Cones</article-title><alt-title alt-title-type="runhead">Intrinsic Growth Is Regulated at the Growth Cone</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Steketee</surname><given-names>Michael B.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Oboudiyat</surname><given-names>Carly</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Daneman</surname><given-names>Richard</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Trakhtenberg</surname><given-names>Ephraim</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lamoureux</surname><given-names>Philip</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Weinstein</surname><given-names>Jessica E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Heidemann</surname><given-names>Steve</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Barres</surname><given-names>Ben A.</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Goldberg</surname><given-names>Jeffrey L.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label>Bascom Palmer Eye Institute and Interdisciplinary Stem Cell Institute, University of Miami Miller School of Medicine, Miami, Florida, United States</aff><aff id="aff2"><label>2</label>Department of Ophthalmology and McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, United States</aff><aff id="aff3"><label>3</label>Department of Neurobiology, Stanford University School of Medicine, Stanford, California, United States</aff><aff id="aff4"><label>4</label>Department of Physiology, Michigan State University, East Lansing, Michigan, United States</aff><aff id="aff5"><label>5</label>Department of Ophthalmology, Shiley Eye Center, University of California San Diego, San Diego, California, United States</aff><author-notes><corresp id="cor1">Correspondence: Jeffrey L. Goldberg, Shiley Eye Center, UC San Diego, 9415 Campus Point Drive, La Jolla, CA 92093, USA; <email>JLGoldberg@ucsd.edu</email>.</corresp></author-notes><pub-date pub-type="epub"><day>17</day><month>7</month><year>2014</year></pub-date><pub-date pub-type="ppub"><month>7</month><year>2014</year></pub-date><volume>55</volume><issue>7</issue><fpage>4369</fpage><lpage>4377</lpage><history><date date-type="received"><day>8</day><month>1</month><year>2014</year></date><date date-type="accepted"><day>25</day><month>5</month><year>2014</year></date></history><permissions><copyright-statement>Copyright 2014 The Association for Research in Vision and Ophthalmology, Inc.</copyright-statement><copyright-year>2014</copyright-year></permissions><abstract><sec id="st1"><title>Purpose.</title><p>Mammalian central nervous system neurons fail to regenerate after injury or disease, in part due to a progressive loss in intrinsic axon growth ability after birth. Whether lost axon growth ability is due to limited growth resources or to changes in the axonal growth cone is unknown.</p></sec><sec id="st2"><title>Methods.</title><p>Static and time-lapse images of purified retinal ganglion cells (RGCs) were analyzed for axon growth rate and growth cone morphology and dynamics without treatment and after manipulating Kruppel-like transcription factor (KLF) expression or applying mechanical tension.</p></sec><sec id="st3"><title>Results.</title><p>Retinal ganglion cells undergo a developmental switch in growth cone dynamics that mirrors the decline in postnatal axon growth rates, with increased filopodial adhesion and decreased lamellar protrusion area in postnatal axonal growth cones. Moreover, expressing growth-suppressive KLF4 or growth-enhancing KLF6 transcription factors elicits similar changes in postnatal growth cones that correlate with axon growth rates. Postnatal RGC axon growth rate is not limited by an inability to achieve axon growth rates similar to embryonic RGCs; indeed, postnatal axons support elongation rates up to 100-fold faster than postnatal axonal growth rates. Rather, the intrinsic capacity for rapid axon growth is due to both growth cone pausing and retraction, as well as to a slightly decreased ability to achieve rapid instantaneous rates of forward progression. Finally, we observed that RGC axon and dendrite growth are regulated independently in vitro.</p></sec><sec id="st4"><title>Conclusions.</title><p>Together, these data support the hypothesis that intrinsic axon growth rate is regulated by an axon-specific growth program that differentially regulates growth cone motility.</p></sec></abstract><abstract abstract-type="precis"><p>These data support the hypothesis that retinal ganglion cells' intrinsic axon growth rate is regulated by an axon-specific growth program that differentially regulates specific protrusive dynamics at the growth cone.</p></abstract><kwd-group><title>Keywords</title><kwd>axon</kwd><kwd>regeneration</kwd><kwd>CNS</kwd><kwd>growth cone</kwd><kwd>filopodia</kwd><kwd>lamellipodia</kwd><kwd>KLF</kwd></kwd-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li><li>Floride</li><li>Michigan</li><li>Pennsylvanie</li></region><settlement><li>East Lansing</li><li>Pittsburgh</li></settlement><orgName><li>Université d'État du Michigan</li><li>Université de Pittsburgh</li></orgName></list><tree><country name="États-Unis"><region name="Floride"><name sortKey="Steketee, Michael B" sort="Steketee, Michael B" uniqKey="Steketee M" first="Michael B." last="Steketee">Michael B. Steketee</name></region><name sortKey="Barres, Ben A" sort="Barres, Ben A" uniqKey="Barres B" first="Ben A." last="Barres">Ben A. Barres</name><name sortKey="Daneman, Richard" sort="Daneman, Richard" uniqKey="Daneman R" first="Richard" last="Daneman">Richard Daneman</name><name sortKey="Goldberg, Jeffrey L" sort="Goldberg, Jeffrey L" uniqKey="Goldberg J" first="Jeffrey L." last="Goldberg">Jeffrey L. Goldberg</name><name sortKey="Goldberg, Jeffrey L" sort="Goldberg, Jeffrey L" uniqKey="Goldberg J" first="Jeffrey L." last="Goldberg">Jeffrey L. Goldberg</name><name sortKey="Heidemann, Steve" sort="Heidemann, Steve" uniqKey="Heidemann S" first="Steve" last="Heidemann">Steve Heidemann</name><name sortKey="Lamoureux, Philip" sort="Lamoureux, Philip" uniqKey="Lamoureux P" first="Philip" last="Lamoureux">Philip Lamoureux</name><name sortKey="Oboudiyat, Carly" sort="Oboudiyat, Carly" uniqKey="Oboudiyat C" first="Carly" last="Oboudiyat">Carly Oboudiyat</name><name sortKey="Steketee, Michael B" sort="Steketee, Michael B" uniqKey="Steketee M" first="Michael B." last="Steketee">Michael B. Steketee</name><name sortKey="Trakhtenberg, Ephraim" sort="Trakhtenberg, Ephraim" uniqKey="Trakhtenberg E" first="Ephraim" last="Trakhtenberg">Ephraim Trakhtenberg</name><name sortKey="Weinstein, Jessica E" sort="Weinstein, Jessica E" uniqKey="Weinstein J" first="Jessica E." last="Weinstein">Jessica E. Weinstein</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Checkpoint/RBID.i -Sk "pubmed:24906860" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Checkpoint/biblio.hfd \
| NlmPubMed2Wicri -a PittsburghV1
| This area was generated with Dilib version V0.6.38. |  |