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Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants

Identifieur interne : 002A28 ( Istex/Corpus ); précédent : 002A27; suivant : 002A29

Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants

Auteurs : Joshua R. Buser ; Jennifer Maire ; Art Riddle ; Xi Gong ; Thuan Nguyen ; Kerst Nelson ; Ning Ling Luo ; Jennifer Ren ; Jaime Struve ; Larry S. Sherman ; Steven P. Miller ; Vann Chau ; Glenda Hendson ; Praveen Ballabh ; Marjorie R. Grafe ; Stephen A. Back

Source :

RBID : ISTEX:14F3C9DB140E18F2C7CA49EB99AF20179071F320

Abstract

The major form of magnetic resonance imaging–defined white matter injury (WMI) comprises diffuse lesions where the burden of small necrotic foci (microscopic necrosis) is poorly defined. We hypothesized that myelination failure associated with diffuse WMI involves an aberrant injury response linked to arrested preoligodendrocyte (preOL) maturation in reactive astrocyte‐rich lesions.

Url:
DOI: 10.1002/ana.22627

Links to Exploration step

ISTEX:14F3C9DB140E18F2C7CA49EB99AF20179071F320

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<p>In the contemporary case series, diffuse WMI was accompanied by a significant reduction in the burden of microscopic necrosis and axonopathy. Diffuse astrogliosis extended into the lesion surround with elevated HA and astrocyte‐expressed CD44. The total population of OL lineage stages was significantly increased in lesions. This increase coincided with significant expansion of the preOL pool.</p>
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<p>Although these data confirm that microscopic necrosis occurs in contemporary cases, the markedly decreased burden supports that it does not contribute substantially to myelination failure. The primary mechanism of myelination failure involves a disrupted cellular response whereby preOLs fail to differentiate in diffuse astrogliotic lesions. PreOL maturation arrest converts chronic WMI to a more immature state related to the burden of astrogliosis. ANN NEUROL 2012;71:93–109</p>
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<p> Additional supporting information can be found in the online version of this article. </p>
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<p>The major form of magnetic resonance imaging–defined white matter injury (WMI) comprises diffuse lesions where the burden of small necrotic foci (microscopic necrosis) is poorly defined. We hypothesized that myelination failure associated with diffuse WMI involves an aberrant injury response linked to arrested preoligodendrocyte (preOL) maturation in reactive astrocyte‐rich lesions.</p>
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<p>A retrospective autopsy series (1983–2000) was selected for cases with diffuse WMI and analyzed relative to prospectively collected contemporary cases (2003–2010). Controls were age‐ and region‐matched to address regional variation in preOL maturation. Successive oligodendrocyte stages were analyzed with lineage‐specific markers. Microscopic necrosis was quantified with microglial markers. Axon injury markers defined the burden of axonopathy. Extracellular matrix remodeling was defined by detection of hyaluronic acid (HA), an inhibitor of preOL maturation, and the HA receptor, CD44.</p>
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<p>In the contemporary case series, diffuse WMI was accompanied by a significant reduction in the burden of microscopic necrosis and axonopathy. Diffuse astrogliosis extended into the lesion surround with elevated HA and astrocyte‐expressed CD44. The total population of OL lineage stages was significantly increased in lesions. This increase coincided with significant expansion of the preOL pool.</p>
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<p>Although these data confirm that microscopic necrosis occurs in contemporary cases, the markedly decreased burden supports that it does not contribute substantially to myelination failure. The primary mechanism of myelination failure involves a disrupted cellular response whereby preOLs fail to differentiate in diffuse astrogliotic lesions. PreOL maturation arrest converts chronic WMI to a more immature state related to the burden of astrogliosis. ANN NEUROL 2012;71:93–109</p>
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<name type="personal">
<namePart type="given">Marjorie R.</namePart>
<namePart type="family">Grafe</namePart>
<namePart type="termsOfAddress">MD, PhD</namePart>
<affiliation>Departments of Public Health and Pathology, Oregon Health and Science University, Portland, OR</affiliation>
<role>
<roleTerm type="text">author</roleTerm>
</role>
</name>
<name type="personal">
<namePart type="given">Stephen A.</namePart>
<namePart type="family">Back</namePart>
<namePart type="termsOfAddress">MD, PhD</namePart>
<affiliation>Departments of Pediatrics, Oregon Health and Science University, Portland, OR</affiliation>
<affiliation>Neurology, Oregon Health and Science University, Portland, OR</affiliation>
<affiliation>Department of Pediatrics, Mail Code L481, Oregon Health and Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239‐3098</affiliation>
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<place>
<placeTerm type="text">Hoboken</placeTerm>
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<dateIssued encoding="w3cdtf">2012-01</dateIssued>
<dateCaptured encoding="w3cdtf">2011-07-07</dateCaptured>
<dateValid encoding="w3cdtf">2011-08-16</dateValid>
<copyrightDate encoding="w3cdtf">2012</copyrightDate>
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<abstract>The major form of magnetic resonance imaging–defined white matter injury (WMI) comprises diffuse lesions where the burden of small necrotic foci (microscopic necrosis) is poorly defined. We hypothesized that myelination failure associated with diffuse WMI involves an aberrant injury response linked to arrested preoligodendrocyte (preOL) maturation in reactive astrocyte‐rich lesions.</abstract>
<abstract>A retrospective autopsy series (1983–2000) was selected for cases with diffuse WMI and analyzed relative to prospectively collected contemporary cases (2003–2010). Controls were age‐ and region‐matched to address regional variation in preOL maturation. Successive oligodendrocyte stages were analyzed with lineage‐specific markers. Microscopic necrosis was quantified with microglial markers. Axon injury markers defined the burden of axonopathy. Extracellular matrix remodeling was defined by detection of hyaluronic acid (HA), an inhibitor of preOL maturation, and the HA receptor, CD44.</abstract>
<abstract>In the contemporary case series, diffuse WMI was accompanied by a significant reduction in the burden of microscopic necrosis and axonopathy. Diffuse astrogliosis extended into the lesion surround with elevated HA and astrocyte‐expressed CD44. The total population of OL lineage stages was significantly increased in lesions. This increase coincided with significant expansion of the preOL pool.</abstract>
<abstract>Although these data confirm that microscopic necrosis occurs in contemporary cases, the markedly decreased burden supports that it does not contribute substantially to myelination failure. The primary mechanism of myelination failure involves a disrupted cellular response whereby preOLs fail to differentiate in diffuse astrogliotic lesions. PreOL maturation arrest converts chronic WMI to a more immature state related to the burden of astrogliosis. ANN NEUROL 2012;71:93–109</abstract>
<note type="funding">NIH</note>
<note type="funding">National Institutes of Neurological Diseases and Stroke - No. 1RO1NS054044; No. R37NS045737‐06S1/06S2; No. 1F30NS066704; </note>
<note type="funding">Bugher Award from the American Heart Association</note>
<note type="funding">March of Dimes Birth Defects Foundation</note>
<note type="funding">Canada Research Chair in Neonatal Neuroscience</note>
<note type="funding">Michael Smith Foundation for Health Research Scholar award</note>
<note type="funding">Canadian Institutes of Health Research Clinician Scientist award</note>
<note type="funding">NIH - No. R01NS071263; </note>
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<title>Annals of Neurology</title>
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<titleInfo type="abbreviated">
<title>Ann Neurol.</title>
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<genre type="journal">journal</genre>
<note type="content"> Additional supporting information can be found in the online version of this article.Supporting Info Item: Supporting Information Figure 1 - Supporting Information Figure 2 - Supporting Information Figure 3 - Supporting Information Figure 4 - Supporting Information Figure 5 - Supporting Information Figure 6 - Supporting Information Figure 7 - Supporting Information Table 1 - </note>
<subject>
<genre>article-category</genre>
<topic>Original Article</topic>
</subject>
<identifier type="ISSN">0364-5134</identifier>
<identifier type="eISSN">1531-8249</identifier>
<identifier type="DOI">10.1002/(ISSN)1531-8249</identifier>
<identifier type="PublisherID">ANA</identifier>
<part>
<date>2012</date>
<detail type="volume">
<caption>vol.</caption>
<number>71</number>
</detail>
<detail type="issue">
<caption>no.</caption>
<number>1</number>
</detail>
<extent unit="pages">
<start>93</start>
<end>109</end>
<total>17</total>
</extent>
</part>
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<identifier type="istex">14F3C9DB140E18F2C7CA49EB99AF20179071F320</identifier>
<identifier type="DOI">10.1002/ana.22627</identifier>
<identifier type="ArticleID">ANA22627</identifier>
<accessCondition type="use and reproduction" contentType="copyright">Copyright © 2011 American Neurological Association</accessCondition>
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