Generation of Human Induced Pluripotent Stem Cells from Extraembryonic Tissues of Fetuses Affected by Monogenic Diseases.
Identifieur interne : 000B81 ( PubMed/Corpus ); précédent : 000B80; suivant : 000B82Generation of Human Induced Pluripotent Stem Cells from Extraembryonic Tissues of Fetuses Affected by Monogenic Diseases.
Auteurs : Paola Spitalieri ; Rosa V. Talarico ; Annalisa Botta ; Michela Murdocca ; Maria Rosaria D'Apice ; Augusto Orlandi ; Emiliano Giardina ; Massimo Santoro ; Francesco Brancati ; Giuseppe Novelli ; Federica SangiuoloSource :
- Cellular reprogramming [ 2152-4998 ] ; 2015.
English descriptors
- KwdEn :
- Animals, Cells, Cultured, Cellular Reprogramming, Chorionic Villi Sampling, Cystic Fibrosis (embryology), Eyelashes (abnormalities), Eyelashes (embryology), Female, Fetus (cytology), Fetus (physiology), Genetic Vectors, Humans, Induced Pluripotent Stem Cells (metabolism), Kruppel-Like Transcription Factors (genetics), Lentivirus (genetics), Lymphedema (embryology), Mice, Muscular Atrophy, Spinal (embryology), Myotonic Dystrophy (embryology), Octamer Transcription Factor-3 (genetics), Pregnancy, Proto-Oncogene Proteins c-myc (genetics), SOXB1 Transcription Factors (genetics), Transgenes, beta-Thalassemia (embryology).
- MESH :
- chemical , genetics : Kruppel-Like Transcription Factors, Octamer Transcription Factor-3, Proto-Oncogene Proteins c-myc, SOXB1 Transcription Factors.
- abnormalities : Eyelashes.
- cytology : Fetus.
- embryology : Cystic Fibrosis, Eyelashes, Lymphedema, Muscular Atrophy, Spinal, Myotonic Dystrophy, beta-Thalassemia.
- genetics : Lentivirus.
- metabolism : Induced Pluripotent Stem Cells.
- physiology : Fetus.
- Animals, Cells, Cultured, Cellular Reprogramming, Chorionic Villi Sampling, Female, Genetic Vectors, Humans, Mice, Pregnancy, Transgenes.
Abstract
The generation of human induced pluripotent stem cells (hiPSCs) derived from an autologous extraembryonic fetal source is an innovative personalized regenerative technology that can transform own-self cells into embryonic stem-like ones. These cells are regarded as a promising candidate for cell-based therapy, as well as an ideal target for disease modeling and drug discovery. Thus, hiPSCs enable researchers to undertake studies for treating diseases or for future applications of in utero therapy. We used a polycistronic lentiviral vector (hSTEMCCA-loxP) encoding OCT4, SOX2, KLF4, and cMYC genes and containing loxP sites, excisible by Cre recombinase, to reprogram patient-specific fetal cells derived from prenatal diagnosis for several genetic disorders, such as myotonic dystrophy type 1 (DM1), β-thalassemia (β-Thal), lymphedema-distichiasis syndrome (LDS), spinal muscular atrophy (SMA), cystic fibrosis (CF), as well as from wild-type (WT) fetal cells. Because cell types tested to create hiPSCs influence both the reprogramming process efficiency and the kinetics, we used chorionic villus (CV) and amniotic fluid (AF) cells, demonstrating how they represent an ideal cell resource for a more efficient generation of hiPSCs. The successful reprogramming of both CV and AF cells into hiPSCs was confirmed by specific morphological, molecular, and immunocytochemical markers and also by their teratogenic potential when inoculated in vivo. We further demonstrated the stability of reprogrammed cells over 10 and more passages and their capability to differentiate into the three embryonic germ layers, as well as into neural cells. These data suggest that hiPSCs-CV/AF can be considered a valid cellular model to accomplish pathogenesis studies and therapeutic applications.
DOI: 10.1089/cell.2015.0003
PubMed: 26474030
Links to Exploration step
pubmed:26474030Le document en format XML
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Talarico</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Botta, Annalisa" sort="Botta, Annalisa" uniqKey="Botta A" first="Annalisa" last="Botta">Annalisa Botta</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Murdocca, Michela" sort="Murdocca, Michela" uniqKey="Murdocca M" first="Michela" last="Murdocca">Michela Murdocca</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="D Apice, Maria Rosaria" sort="D Apice, Maria Rosaria" uniqKey="D Apice M" first="Maria Rosaria" last="D'Apice">Maria Rosaria D'Apice</name><affiliation><nlm:affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Orlandi, Augusto" sort="Orlandi, Augusto" uniqKey="Orlandi A" first="Augusto" last="Orlandi">Augusto Orlandi</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Giardina, Emiliano" sort="Giardina, Emiliano" uniqKey="Giardina E" first="Emiliano" last="Giardina">Emiliano Giardina</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Santoro, Massimo" sort="Santoro, Massimo" uniqKey="Santoro M" first="Massimo" last="Santoro">Massimo Santoro</name><affiliation><nlm:affiliation>4 Don Carlo Gnocchi Foundation, ONLUS , Milan, 20148, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Brancati, Francesco" sort="Brancati, Francesco" uniqKey="Brancati F" first="Francesco" last="Brancati">Francesco Brancati</name><affiliation><nlm:affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Novelli, Giuseppe" sort="Novelli, Giuseppe" uniqKey="Novelli G" first="Giuseppe" last="Novelli">Giuseppe Novelli</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author><author><name sortKey="Sangiuolo, Federica" sort="Sangiuolo, Federica" uniqKey="Sangiuolo F" first="Federica" last="Sangiuolo">Federica Sangiuolo</name><affiliation><nlm:affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</nlm:affiliation></affiliation></author></analytic><series><title level="j">Cellular reprogramming</title><idno type="eISSN">2152-4998</idno><imprint><date when="2015" type="published">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals</term><term>Cells, Cultured</term><term>Cellular Reprogramming</term><term>Chorionic Villi Sampling</term><term>Cystic Fibrosis (embryology)</term><term>Eyelashes (abnormalities)</term><term>Eyelashes (embryology)</term><term>Female</term><term>Fetus (cytology)</term><term>Fetus (physiology)</term><term>Genetic Vectors</term><term>Humans</term><term>Induced Pluripotent Stem Cells (metabolism)</term><term>Kruppel-Like Transcription Factors (genetics)</term><term>Lentivirus (genetics)</term><term>Lymphedema (embryology)</term><term>Mice</term><term>Muscular Atrophy, Spinal (embryology)</term><term>Myotonic Dystrophy (embryology)</term><term>Octamer Transcription Factor-3 (genetics)</term><term>Pregnancy</term><term>Proto-Oncogene Proteins c-myc (genetics)</term><term>SOXB1 Transcription Factors (genetics)</term><term>Transgenes</term><term>beta-Thalassemia (embryology)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Kruppel-Like Transcription Factors</term><term>Octamer Transcription Factor-3</term><term>Proto-Oncogene Proteins c-myc</term><term>SOXB1 Transcription Factors</term></keywords><keywords scheme="MESH" qualifier="abnormalities" xml:lang="en"><term>Eyelashes</term></keywords><keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Fetus</term></keywords><keywords scheme="MESH" qualifier="embryology" xml:lang="en"><term>Cystic Fibrosis</term><term>Eyelashes</term><term>Lymphedema</term><term>Muscular Atrophy, Spinal</term><term>Myotonic Dystrophy</term><term>beta-Thalassemia</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Lentivirus</term></keywords><keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Induced Pluripotent Stem Cells</term></keywords><keywords scheme="MESH" qualifier="physiology" xml:lang="en"><term>Fetus</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Animals</term><term>Cells, Cultured</term><term>Cellular Reprogramming</term><term>Chorionic Villi Sampling</term><term>Female</term><term>Genetic Vectors</term><term>Humans</term><term>Mice</term><term>Pregnancy</term><term>Transgenes</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The generation of human induced pluripotent stem cells (hiPSCs) derived from an autologous extraembryonic fetal source is an innovative personalized regenerative technology that can transform own-self cells into embryonic stem-like ones. These cells are regarded as a promising candidate for cell-based therapy, as well as an ideal target for disease modeling and drug discovery. Thus, hiPSCs enable researchers to undertake studies for treating diseases or for future applications of in utero therapy. We used a polycistronic lentiviral vector (hSTEMCCA-loxP) encoding OCT4, SOX2, KLF4, and cMYC genes and containing loxP sites, excisible by Cre recombinase, to reprogram patient-specific fetal cells derived from prenatal diagnosis for several genetic disorders, such as myotonic dystrophy type 1 (DM1), β-thalassemia (β-Thal), lymphedema-distichiasis syndrome (LDS), spinal muscular atrophy (SMA), cystic fibrosis (CF), as well as from wild-type (WT) fetal cells. Because cell types tested to create hiPSCs influence both the reprogramming process efficiency and the kinetics, we used chorionic villus (CV) and amniotic fluid (AF) cells, demonstrating how they represent an ideal cell resource for a more efficient generation of hiPSCs. The successful reprogramming of both CV and AF cells into hiPSCs was confirmed by specific morphological, molecular, and immunocytochemical markers and also by their teratogenic potential when inoculated in vivo. We further demonstrated the stability of reprogrammed cells over 10 and more passages and their capability to differentiate into the three embryonic germ layers, as well as into neural cells. These data suggest that hiPSCs-CV/AF can be considered a valid cellular model to accomplish pathogenesis studies and therapeutic applications.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26474030</PMID><DateCreated><Year>2015</Year><Month>10</Month><Day>17</Day></DateCreated><DateCompleted><Year>2016</Year><Month>08</Month><Day>15</Day></DateCompleted><DateRevised><Year>2015</Year><Month>10</Month><Day>17</Day></DateRevised><Article PubModel="Print"><Journal><ISSN IssnType="Electronic">2152-4998</ISSN><JournalIssue CitedMedium="Internet"><Volume>17</Volume><Issue>4</Issue><PubDate><Year>2015</Year><Month>Aug</Month></PubDate></JournalIssue><Title>Cellular reprogramming</Title><ISOAbbreviation>Cell Reprogram</ISOAbbreviation></Journal><ArticleTitle>Generation of Human Induced Pluripotent Stem Cells from Extraembryonic Tissues of Fetuses Affected by Monogenic Diseases.</ArticleTitle><Pagination><MedlinePgn>275-87</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1089/cell.2015.0003</ELocationID><Abstract><AbstractText>The generation of human induced pluripotent stem cells (hiPSCs) derived from an autologous extraembryonic fetal source is an innovative personalized regenerative technology that can transform own-self cells into embryonic stem-like ones. These cells are regarded as a promising candidate for cell-based therapy, as well as an ideal target for disease modeling and drug discovery. Thus, hiPSCs enable researchers to undertake studies for treating diseases or for future applications of in utero therapy. We used a polycistronic lentiviral vector (hSTEMCCA-loxP) encoding OCT4, SOX2, KLF4, and cMYC genes and containing loxP sites, excisible by Cre recombinase, to reprogram patient-specific fetal cells derived from prenatal diagnosis for several genetic disorders, such as myotonic dystrophy type 1 (DM1), β-thalassemia (β-Thal), lymphedema-distichiasis syndrome (LDS), spinal muscular atrophy (SMA), cystic fibrosis (CF), as well as from wild-type (WT) fetal cells. Because cell types tested to create hiPSCs influence both the reprogramming process efficiency and the kinetics, we used chorionic villus (CV) and amniotic fluid (AF) cells, demonstrating how they represent an ideal cell resource for a more efficient generation of hiPSCs. The successful reprogramming of both CV and AF cells into hiPSCs was confirmed by specific morphological, molecular, and immunocytochemical markers and also by their teratogenic potential when inoculated in vivo. We further demonstrated the stability of reprogrammed cells over 10 and more passages and their capability to differentiate into the three embryonic germ layers, as well as into neural cells. These data suggest that hiPSCs-CV/AF can be considered a valid cellular model to accomplish pathogenesis studies and therapeutic applications.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Spitalieri</LastName><ForeName>Paola</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Talarico</LastName><ForeName>Rosa V</ForeName><Initials>RV</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Botta</LastName><ForeName>Annalisa</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Murdocca</LastName><ForeName>Michela</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>D'Apice</LastName><ForeName>Maria Rosaria</ForeName><Initials>MR</Initials><AffiliationInfo><Affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Orlandi</LastName><ForeName>Augusto</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Giardina</LastName><ForeName>Emiliano</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>3 Molecular Genetics Laboratory UILDM , Santa Lucia Foundation, Rome, 00142, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Santoro</LastName><ForeName>Massimo</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>4 Don Carlo Gnocchi Foundation, ONLUS , Milan, 20148, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brancati</LastName><ForeName>Francesco</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Novelli</LastName><ForeName>Giuseppe</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sangiuolo</LastName><ForeName>Federica</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>1 Department of Biomedicine and Prevention, Tor Vergata University of Rome , Rome, 00133, Italy .</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>2 Department of Laboratory Medicine, Policlinic of Tor Vergata , Rome, 00133, Italy .</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Cell Reprogram</MedlineTA><NlmUniqueID>101528176</NlmUniqueID><ISSNLinking>2152-4971</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C102583">GKLF protein</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D051741">Kruppel-Like Transcription Factors</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C489427">MYC protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D050814">Octamer Transcription Factor-3</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C494173">POU5F1 protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D016271">Proto-Oncogene Proteins c-myc</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C527782">SOX2 protein, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D055748">SOXB1 Transcription Factors</NameOfSubstance></Chemical></ChemicalList><SupplMeshList><SupplMeshName Type="Disease" UI="C537710">Lymphedema distichiasis syndrome</SupplMeshName></SupplMeshList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D002478" MajorTopicYN="N">Cells, Cultured</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D065150" MajorTopicYN="N">Cellular Reprogramming</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D015193" MajorTopicYN="N">Chorionic Villi Sampling</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D003550" MajorTopicYN="N">Cystic Fibrosis</DescriptorName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005140" MajorTopicYN="N">Eyelashes</DescriptorName><QualifierName UI="Q000002" MajorTopicYN="N">abnormalities</QualifierName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005333" MajorTopicYN="N">Fetus</DescriptorName><QualifierName UI="Q000166" MajorTopicYN="Y">cytology</QualifierName><QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D005822" MajorTopicYN="N">Genetic Vectors</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D057026" MajorTopicYN="N">Induced Pluripotent Stem Cells</DescriptorName><QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051741" MajorTopicYN="N">Kruppel-Like Transcription Factors</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016086" MajorTopicYN="N">Lentivirus</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D008209" MajorTopicYN="N">Lymphedema</DescriptorName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D009134" MajorTopicYN="N">Muscular Atrophy, Spinal</DescriptorName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D009223" MajorTopicYN="N">Myotonic Dystrophy</DescriptorName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D050814" MajorTopicYN="N">Octamer Transcription Factor-3</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D011247" MajorTopicYN="N">Pregnancy</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D016271" MajorTopicYN="N">Proto-Oncogene Proteins c-myc</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D055748" MajorTopicYN="N">SOXB1 Transcription Factors</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D019076" MajorTopicYN="N">Transgenes</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D017086" MajorTopicYN="N">beta-Thalassemia</DescriptorName><QualifierName UI="Q000196" MajorTopicYN="N">embryology</QualifierName></MeshHeading></MeshHeadingList></MedlineCitation><PubmedData><History><PubMedPubDate 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| HfdSelect -Kh $EXPLOR_AREA/Data/PubMed/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a LymphedemaV1
| This area was generated with Dilib version V0.6.31. |  |