Expression levels and DNA methylation profiles of the growth gene SHOX in cartilage tissues and chondrocytes
All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based transcriptome analysis of the cartilage tissues of four adults and chondrocytes of 12 children showed that the median expression levels of SHOX , a g...
Saved in:
Published in | Scientific reports Vol. 14; no. 1; p. 8069 |
---|---|
Main Authors | , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
London
Nature Publishing Group UK
05.04.2024
Nature Publishing Group Nature Portfolio |
Subjects | |
Online Access | Get full text |
Cover
Loading…
Abstract | All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based transcriptome analysis of the cartilage tissues of four adults and chondrocytes of 12 children showed that the median expression levels of
SHOX
, a growth gene in the pseudoautosomal region (PAR), were higher in male samples than in female samples. Male-dominant
SHOX
expression was confirmed by quantitative RT-PCR for 36 cartilage samples. Reduced representation bisulfite sequencing of four cartilage samples revealed sex-biased DNA methylation in the
SHOX
-flanking regions, and pyrosequencing of 22 cartilage samples confirmed male-dominant DNA methylation at the CpG sites in the
SHOX
upstream region and exon 6a. DNA methylation indexes of these regions were positively correlated with
SHOX
expression levels. These results, together with prior findings that PAR genes often exhibit male-dominant expression, imply that the relatively low
SHOX
expression in female cartilage tissues reflects the partial spread of X chromosome inactivation into PAR. Altogether, this study provides the first indication that sex differences in height are ascribed, at least in part, to the sex-dependent epigenetic regulation of
SHOX
. Our findings deserve further validation. |
---|---|
AbstractList | All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based transcriptome analysis of the cartilage tissues of four adults and chondrocytes of 12 children showed that the median expression levels of SHOX, a growth gene in the pseudoautosomal region (PAR), were higher in male samples than in female samples. Male-dominant SHOX expression was confirmed by quantitative RT-PCR for 36 cartilage samples. Reduced representation bisulfite sequencing of four cartilage samples revealed sex-biased DNA methylation in the SHOX-flanking regions, and pyrosequencing of 22 cartilage samples confirmed male-dominant DNA methylation at the CpG sites in the SHOX upstream region and exon 6a. DNA methylation indexes of these regions were positively correlated with SHOX expression levels. These results, together with prior findings that PAR genes often exhibit male-dominant expression, imply that the relatively low SHOX expression in female cartilage tissues reflects the partial spread of X chromosome inactivation into PAR. Altogether, this study provides the first indication that sex differences in height are ascribed, at least in part, to the sex-dependent epigenetic regulation of SHOX. Our findings deserve further validation. All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based transcriptome analysis of the cartilage tissues of four adults and chondrocytes of 12 children showed that the median expression levels of SHOX , a growth gene in the pseudoautosomal region (PAR), were higher in male samples than in female samples. Male-dominant SHOX expression was confirmed by quantitative RT-PCR for 36 cartilage samples. Reduced representation bisulfite sequencing of four cartilage samples revealed sex-biased DNA methylation in the SHOX -flanking regions, and pyrosequencing of 22 cartilage samples confirmed male-dominant DNA methylation at the CpG sites in the SHOX upstream region and exon 6a. DNA methylation indexes of these regions were positively correlated with SHOX expression levels. These results, together with prior findings that PAR genes often exhibit male-dominant expression, imply that the relatively low SHOX expression in female cartilage tissues reflects the partial spread of X chromosome inactivation into PAR. Altogether, this study provides the first indication that sex differences in height are ascribed, at least in part, to the sex-dependent epigenetic regulation of SHOX . Our findings deserve further validation. Abstract All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based transcriptome analysis of the cartilage tissues of four adults and chondrocytes of 12 children showed that the median expression levels of SHOX, a growth gene in the pseudoautosomal region (PAR), were higher in male samples than in female samples. Male-dominant SHOX expression was confirmed by quantitative RT-PCR for 36 cartilage samples. Reduced representation bisulfite sequencing of four cartilage samples revealed sex-biased DNA methylation in the SHOX-flanking regions, and pyrosequencing of 22 cartilage samples confirmed male-dominant DNA methylation at the CpG sites in the SHOX upstream region and exon 6a. DNA methylation indexes of these regions were positively correlated with SHOX expression levels. These results, together with prior findings that PAR genes often exhibit male-dominant expression, imply that the relatively low SHOX expression in female cartilage tissues reflects the partial spread of X chromosome inactivation into PAR. Altogether, this study provides the first indication that sex differences in height are ascribed, at least in part, to the sex-dependent epigenetic regulation of SHOX. Our findings deserve further validation. |
ArticleNumber | 8069 |
Author | Umezawa, Akihiro Inaba, Naoto Fukami, Maki Ishiwata, Keisuke Seki, Atsuhito Matsumoto, Kenji Ogata, Tsutomu Katoh-Fukui, Yuko Naiki, Yasuhiro Okamura, Kohji Nakabayashi, Kazuhiko Nasu, Michiyo Michigami, Toshimi Tatsusmi, Kuniko Takeda, Kazue Nakamura, Akie Kagami, Masayo Hattori, Atsushi |
Author_xml | – sequence: 1 givenname: Atsushi surname: Hattori fullname: Hattori, Atsushi organization: Department of Molecular Endocrinology, National Research Institute for Child Health and Development, Division of Diversity Research, National Research Institute for Child Health and Development – sequence: 2 givenname: Atsuhito surname: Seki fullname: Seki, Atsuhito organization: Department of Orthopaedic Surgery, National Medical Center for Children and Mothers – sequence: 3 givenname: Naoto surname: Inaba fullname: Inaba, Naoto organization: Department of Orthopaedic Surgery, National Medical Center for Children and Mothers – sequence: 4 givenname: Kazuhiko surname: Nakabayashi fullname: Nakabayashi, Kazuhiko organization: Department of Maternal-Fetal Biology, National Research Institute for Child Health and Development – sequence: 5 givenname: Kazue surname: Takeda fullname: Takeda, Kazue organization: Department of Allergy and Clinical Immunology, National Research Institute for Child Health and Development – sequence: 6 givenname: Kuniko surname: Tatsusmi fullname: Tatsusmi, Kuniko organization: Center for Regenerative Medicine, National Research Institute for Child Health and Development – sequence: 7 givenname: Yasuhiro surname: Naiki fullname: Naiki, Yasuhiro organization: Division of Endocrinology and Metabolism, National Medical Center for Children and Mothers – sequence: 8 givenname: Akie surname: Nakamura fullname: Nakamura, Akie organization: Department of Molecular Endocrinology, National Research Institute for Child Health and Development – sequence: 9 givenname: Keisuke surname: Ishiwata fullname: Ishiwata, Keisuke organization: Department of Maternal-Fetal Biology, National Research Institute for Child Health and Development – sequence: 10 givenname: Kenji surname: Matsumoto fullname: Matsumoto, Kenji organization: Department of Allergy and Clinical Immunology, National Research Institute for Child Health and Development – sequence: 11 givenname: Michiyo surname: Nasu fullname: Nasu, Michiyo organization: Center for Regenerative Medicine, National Research Institute for Child Health and Development – sequence: 12 givenname: Kohji surname: Okamura fullname: Okamura, Kohji organization: Department of Systems BioMedicine, National Research Institute for Child Health and Development – sequence: 13 givenname: Toshimi surname: Michigami fullname: Michigami, Toshimi organization: Department of Bone and Mineral Research, Research Institute, Osaka Women’s and Children’s Hospital, Osaka Prefectural Hospital Organization – sequence: 14 givenname: Yuko surname: Katoh-Fukui fullname: Katoh-Fukui, Yuko organization: Department of Molecular Endocrinology, National Research Institute for Child Health and Development – sequence: 15 givenname: Akihiro surname: Umezawa fullname: Umezawa, Akihiro organization: Center for Regenerative Medicine, National Research Institute for Child Health and Development – sequence: 16 givenname: Tsutomu surname: Ogata fullname: Ogata, Tsutomu organization: Department of Pediatrics, Hamamatsu University School of Medicine, Department of Pediatrics, Hamamatsu Medical Center – sequence: 17 givenname: Masayo surname: Kagami fullname: Kagami, Masayo organization: Department of Molecular Endocrinology, National Research Institute for Child Health and Development – sequence: 18 givenname: Maki surname: Fukami fullname: Fukami, Maki email: fukami-m@ncchd.go.jp organization: Department of Molecular Endocrinology, National Research Institute for Child Health and Development, Division of Diversity Research, National Research Institute for Child Health and Development |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38580675$$D View this record in MEDLINE/PubMed |
BookMark | eNp9kU1v1DAQhi1UREvpH-CALHHhEnD8kdjHqi20UkUPgMTN8sdkNyuvvdhZYP89TlMK4oAvtmeeeT3j9zk6iikCQi9b8rYlTL4rvBVKNoTyRkjBSKOeoBNKuGgoo_Tor_MxOitlQ-oSVPFWPUPHTApJul6coHD1c5ehlDFFHOA7hIJN9Pjy4znewrQ-BDPNqV1Owxig4DTgaQ14ldOPaY1XEAF_ur77iseIncnTGMwK8DSWsodFya1T9Dm5wwTlBXo6mFDg7GE_RV_eX32-uG5u7z7cXJzfNo6zbmokF8IIwhyn3ApqO6aGXlmuSGv9wIWRjlJnuKtxYZW1nhrWuUF4W6-MsVN0s-j6ZDZ6l8etyQedzKjvAymv9NyrC6AZaZWnFLznnjvpLXDTC9I533MvLVStN4tW_YJvdahJb8fiIAQTIe1LFWC1TSb7tqKv_0E3aZ9jnXSmWN8xSlSl6EK5nErJMDw22BI9W6sXa3W1Vt9bq-eiVw_Se7sF_1jy28gKsAUoNRVXkP-8_R_ZXwuWsG0 |
Cites_doi | 10.1042/EBC20180062 10.1210/er.2016-1036 10.1002/jcp.24882 10.1371/journal.pone.0018115 10.1186/gb-2012-13-10-r87 10.1186/gb-2012-13-10-r92 10.1038/nbt.1533 10.1210/jcem.84.12.6289 10.1038/ng0597-54 10.1186/s12885-018-4221-0 10.1038/nature24265 10.1093/bioinformatics/btr167 10.1016/j.tig.2016.03.007 10.1093/nar/gki901 10.1007/BF00205079 10.1155/2016/6437658 10.1515/JPEM.2003.16.7.987 10.1126/science.aaw7317 10.1126/science.1136352 10.1093/hmg/ddu564 |
ContentType | Journal Article |
Copyright | The Author(s) 2024 2024. The Author(s). The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
Copyright_xml | – notice: The Author(s) 2024 – notice: 2024. The Author(s). – notice: The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
DBID | C6C CGR CUY CVF ECM EIF NPM AAYXX CITATION 3V. 7X7 7XB 88A 88E 88I 8FE 8FH 8FI 8FJ 8FK ABUWG AFKRA AZQEC BBNVY BENPR BHPHI CCPQU DWQXO FYUFA GHDGH GNUQQ HCIFZ K9. LK8 M0S M1P M2P M7P PIMPY PQEST PQQKQ PQUKI Q9U 7X8 DOA |
DOI | 10.1038/s41598-024-58530-9 |
DatabaseName | Springer Nature OA Free Journals Medline MEDLINE MEDLINE (Ovid) MEDLINE MEDLINE PubMed CrossRef ProQuest Central (Corporate) Health & Medical Collection ProQuest Central (purchase pre-March 2016) Biology Database (Alumni Edition) Medical Database (Alumni Edition) Science Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Collection Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest Central ProQuest Central Essentials Biological Science Collection ProQuest Central Natural Science Collection ProQuest One Community College ProQuest Central Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) Biological Sciences Health & Medical Collection (Alumni Edition) PML(ProQuest Medical Library) Science Database (ProQuest) Biological Science Database Publicly Available Content Database ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Academic ProQuest One Academic UKI Edition ProQuest Central Basic MEDLINE - Academic Directory of Open Access Journals |
DatabaseTitle | MEDLINE Medline Complete MEDLINE with Full Text PubMed MEDLINE (Ovid) CrossRef Publicly Available Content Database ProQuest Central Student ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest Natural Science Collection ProQuest Biology Journals (Alumni Edition) ProQuest Central Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Biological Science Collection ProQuest Medical Library (Alumni) ProQuest Science Journals (Alumni Edition) ProQuest Biological Science Collection ProQuest Central Basic ProQuest Science Journals ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest Central (Alumni) MEDLINE - Academic |
DatabaseTitleList | MEDLINE - Academic Publicly Available Content Database CrossRef MEDLINE |
Database_xml | – sequence: 1 dbid: C6C name: Springer Nature OA Free Journals url: http://www.springeropen.com/ sourceTypes: Publisher – sequence: 2 dbid: DOA name: Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 3 dbid: NPM name: PubMed url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed sourceTypes: Index Database – sequence: 4 dbid: EIF name: MEDLINE url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search sourceTypes: Index Database – sequence: 5 dbid: BENPR name: ProQuest Central url: https://www.proquest.com/central sourceTypes: Aggregation Database |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Biology |
EISSN | 2045-2322 |
EndPage | 8069 |
ExternalDocumentID | oai_doaj_org_article_3019d22edd4d4c8dbe4a7506cd74d8be 10_1038_s41598_024_58530_9 38580675 |
Genre | Journal Article |
GrantInformation_xml | – fundername: National Center for Child Health and Development funderid: http://dx.doi.org/10.13039/100007786 – fundername: The Takeda Science Foundation – fundername: The Japan Endocrine Society – fundername: Japan Society for the Promotion of Science,Japan grantid: 22K15932 – fundername: The Canon Foundation |
GroupedDBID | 0R~ 3V. 4.4 53G 5VS 7X7 88A 88E 88I 8FE 8FH 8FI 8FJ AAFWJ AAJSJ AAKDD ABDBF ABUWG ACGFS ACSMW ADBBV ADRAZ AENEX AFKRA AJTQC ALIPV ALMA_UNASSIGNED_HOLDINGS AOIJS AZQEC BAWUL BBNVY BCNDV BENPR BHPHI BPHCQ BVXVI C6C CCPQU DIK DWQXO EBD EBLON EBS ESX FYUFA GNUQQ GROUPED_DOAJ GX1 HCIFZ HH5 HMCUK HYE KQ8 LK8 M0L M1P M2P M7P M~E NAO OK1 PIMPY PQQKQ PROAC PSQYO RIG RNT RNTTT RPM SNYQT UKHRP CGR CUY CVF ECM EIF NPM AAYXX CITATION 7XB 8FK K9. M48 PQEST PQUKI Q9U 7X8 |
ID | FETCH-LOGICAL-c436t-8455a503c424b52b639f79b4901bdf45a8c22ca4c39f5b9bbd2a36cf5db5b9333 |
IEDL.DBID | 7X7 |
ISSN | 2045-2322 |
IngestDate | Tue Oct 22 15:14:35 EDT 2024 Fri Dec 06 00:10:46 EST 2024 Fri Nov 08 20:47:12 EST 2024 Fri Dec 06 05:10:38 EST 2024 Sat Nov 02 12:28:56 EDT 2024 Fri Oct 11 20:56:24 EDT 2024 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Issue | 1 |
Language | English |
License | 2024. The Author(s). |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c436t-8455a503c424b52b639f79b4901bdf45a8c22ca4c39f5b9bbd2a36cf5db5b9333 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
OpenAccessLink | https://www.proquest.com/docview/3033763209?pq-origsite=%requestingapplication% |
PMID | 38580675 |
PQID | 3033763209 |
PQPubID | 2041939 |
PageCount | 1 |
ParticipantIDs | doaj_primary_oai_doaj_org_article_3019d22edd4d4c8dbe4a7506cd74d8be proquest_miscellaneous_3034243871 proquest_journals_3033763209 crossref_primary_10_1038_s41598_024_58530_9 pubmed_primary_38580675 springer_journals_10_1038_s41598_024_58530_9 |
PublicationCentury | 2000 |
PublicationDate | 2024-04-05 |
PublicationDateYYYYMMDD | 2024-04-05 |
PublicationDate_xml | – month: 04 year: 2024 text: 2024-04-05 day: 05 |
PublicationDecade | 2020 |
PublicationPlace | London |
PublicationPlace_xml | – name: London – name: England |
PublicationTitle | Scientific reports |
PublicationTitleAbbrev | Sci Rep |
PublicationTitleAlternate | Sci Rep |
PublicationYear | 2024 |
Publisher | Nature Publishing Group UK Nature Publishing Group Nature Portfolio |
Publisher_xml | – name: Nature Publishing Group UK – name: Nature Publishing Group – name: Nature Portfolio |
References | Rao (CR3) 1997; 16 Munns (CR10) 2003; 16 Balaton, Brown (CR6) 2016; 32 Marchini, Ogata, Rappold (CR4) 2016; 37 Cotton (CR8) 2015; 24 Sun, Bernstein (CR13) 2019; 63 Kosho (CR5) 1999; 84 Matsushita (CR18) 2018; 18 Tukiainen (CR7) 2017; 550 Ball (CR12) 2009; 27 Nasu, Takayama, Umezawa (CR16) 2016; 2016 Boyle (CR17) 2012; 13 Ogata, Matsuo (CR1) 1993; 91 Naqvi (CR2) 2019; 365 Krueger, Andrews (CR19) 2011; 27 Akalin (CR20) 2012; 13 Nasu, Takayama, Umezawa (CR15) 2015; 230 Hellman, Chess (CR11) 2007; 315 Meissner (CR9) 2005; 33 Durand (CR14) 2011; 6 S Naqvi (58530_CR2) 2019; 365 A Hellman (58530_CR11) 2007; 315 MP Ball (58530_CR12) 2009; 27 C Durand (58530_CR14) 2011; 6 A Akalin (58530_CR20) 2012; 13 AM Cotton (58530_CR8) 2015; 24 P Boyle (58530_CR17) 2012; 13 T Kosho (58530_CR5) 1999; 84 T Tukiainen (58530_CR7) 2017; 550 CFJ Munns (58530_CR10) 2003; 16 E Rao (58530_CR3) 1997; 16 BP Balaton (58530_CR6) 2016; 32 T Ogata (58530_CR1) 1993; 91 A Meissner (58530_CR9) 2005; 33 Z Sun (58530_CR13) 2019; 63 J Matsushita (58530_CR18) 2018; 18 M Nasu (58530_CR16) 2016; 2016 A Marchini (58530_CR4) 2016; 37 M Nasu (58530_CR15) 2015; 230 F Krueger (58530_CR19) 2011; 27 |
References_xml | – volume: 63 start-page: 59 year: 2019 end-page: 74 ident: CR13 article-title: Histone variant macroH2A: From chromatin deposition to molecular function publication-title: Essays Biochem. doi: 10.1042/EBC20180062 contributor: fullname: Bernstein – volume: 37 start-page: 417 year: 2016 end-page: 448 ident: CR4 article-title: A track record on SHOX: From basic research to complex models and therapy publication-title: Endocr. Rev. doi: 10.1210/er.2016-1036 contributor: fullname: Rappold – volume: 230 start-page: 1376 year: 2015 end-page: 1388 ident: CR15 article-title: Endochondral ossification model system: Designed cell fate of human epiphyseal chondrocytes during long-term implantation publication-title: J. Cell. Physiol. doi: 10.1002/jcp.24882 contributor: fullname: Umezawa – volume: 6 start-page: e18115 year: 2011 ident: CR14 article-title: Alternative splicing and nonsense-mediated RNA decay contribute to the regulation of SHOX expression publication-title: PLoS ONE doi: 10.1371/journal.pone.0018115 contributor: fullname: Durand – volume: 13 start-page: R87 year: 2012 ident: CR20 article-title: methylKit: A comprehensive R package for the analysis of genome-wide DNA methylation profiles publication-title: Genome Biol. doi: 10.1186/gb-2012-13-10-r87 contributor: fullname: Akalin – volume: 13 start-page: R92 year: 2012 ident: CR17 article-title: Gel-free multiplexed reduced representation bisulfite sequencing for large-scale DNA methylation profiling publication-title: Genome Biol. doi: 10.1186/gb-2012-13-10-r92 contributor: fullname: Boyle – volume: 27 start-page: 361 year: 2009 end-page: 368 ident: CR12 article-title: Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells publication-title: Nat. Biotechnol. doi: 10.1038/nbt.1533 contributor: fullname: Ball – volume: 84 start-page: 4613 year: 1999 end-page: 4621 ident: CR5 article-title: Skeletal features and growth patterns in 14 patients with haploinsufficiency of SHOX: Implications for the development of Turner syndrome publication-title: J. Clin. Endocrinol. Metab. doi: 10.1210/jcem.84.12.6289 contributor: fullname: Kosho – volume: 16 start-page: 54 year: 1997 end-page: 63 ident: CR3 article-title: Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome publication-title: Nat. Genet. doi: 10.1038/ng0597-54 contributor: fullname: Rao – volume: 18 start-page: 317 year: 2018 ident: CR18 article-title: The DNA methylation profile of liver tumors in C3H mice and identification of differentially methylated regions involved in the regulation of tumorigenic genes publication-title: BMC Cancer doi: 10.1186/s12885-018-4221-0 contributor: fullname: Matsushita – volume: 550 start-page: 244 year: 2017 end-page: 248 ident: CR7 article-title: Landscape of X chromosome inactivation across human tissues publication-title: Nature doi: 10.1038/nature24265 contributor: fullname: Tukiainen – volume: 27 start-page: 1571 year: 2011 end-page: 1572 ident: CR19 article-title: Bismark: A flexible aligner and methylation caller for Bisulfite-Seq applications publication-title: Bioinformatics doi: 10.1093/bioinformatics/btr167 contributor: fullname: Andrews – volume: 32 start-page: 348 year: 2016 end-page: 359 ident: CR6 article-title: Escape artists of the X chromosome publication-title: Trends Genet. doi: 10.1016/j.tig.2016.03.007 contributor: fullname: Brown – volume: 33 start-page: 5868 year: 2005 end-page: 5877 ident: CR9 article-title: Reduced representation bisulfite sequencing for comparative high-resolution DNA methylation analysis publication-title: Nucleic Acids Research doi: 10.1093/nar/gki901 contributor: fullname: Meissner – volume: 91 start-page: 551 year: 1993 end-page: 562 ident: CR1 article-title: Sex chromosome aberrations and stature: Deduction of the principal factors involved in the determination of adult height publication-title: Hum. Genet. doi: 10.1007/BF00205079 contributor: fullname: Matsuo – volume: 2016 start-page: 1 year: 2016 end-page: 13 ident: CR16 article-title: Efficiency of human epiphyseal chondrocytes with differential replication numbers for cellular therapy products publication-title: Biomed. Res. Int. doi: 10.1155/2016/6437658 contributor: fullname: Umezawa – volume: 16 start-page: 987 year: 2003 end-page: 996 ident: CR10 article-title: Familial growth and skeletal features associated with SHOX haploinsufficiency publication-title: J. Pediatr. Endocrinol. Metab. doi: 10.1515/JPEM.2003.16.7.987 contributor: fullname: Munns – volume: 365 start-page: eaaw7317 year: 2019 ident: CR2 article-title: Conservation, acquisition, and functional impact of sex-biased gene expression in mammals publication-title: Science doi: 10.1126/science.aaw7317 contributor: fullname: Naqvi – volume: 315 start-page: 1141 year: 2007 end-page: 1143 ident: CR11 article-title: Gene body-specific methylation on the active X chromosome publication-title: Science doi: 10.1126/science.1136352 contributor: fullname: Chess – volume: 24 start-page: 1528 year: 2015 end-page: 1539 ident: CR8 article-title: Landscape of DNA methylation on the X chromosome reflects CpG density, functional chromatin state and X-chromosome inactivation publication-title: Hum. Mol. Genet. doi: 10.1093/hmg/ddu564 contributor: fullname: Cotton – volume: 13 start-page: R92 year: 2012 ident: 58530_CR17 publication-title: Genome Biol. doi: 10.1186/gb-2012-13-10-r92 contributor: fullname: P Boyle – volume: 32 start-page: 348 year: 2016 ident: 58530_CR6 publication-title: Trends Genet. doi: 10.1016/j.tig.2016.03.007 contributor: fullname: BP Balaton – volume: 16 start-page: 54 year: 1997 ident: 58530_CR3 publication-title: Nat. Genet. doi: 10.1038/ng0597-54 contributor: fullname: E Rao – volume: 315 start-page: 1141 year: 2007 ident: 58530_CR11 publication-title: Science doi: 10.1126/science.1136352 contributor: fullname: A Hellman – volume: 37 start-page: 417 year: 2016 ident: 58530_CR4 publication-title: Endocr. Rev. doi: 10.1210/er.2016-1036 contributor: fullname: A Marchini – volume: 91 start-page: 551 year: 1993 ident: 58530_CR1 publication-title: Hum. Genet. doi: 10.1007/BF00205079 contributor: fullname: T Ogata – volume: 365 start-page: eaaw7317 year: 2019 ident: 58530_CR2 publication-title: Science doi: 10.1126/science.aaw7317 contributor: fullname: S Naqvi – volume: 6 start-page: e18115 year: 2011 ident: 58530_CR14 publication-title: PLoS ONE doi: 10.1371/journal.pone.0018115 contributor: fullname: C Durand – volume: 18 start-page: 317 year: 2018 ident: 58530_CR18 publication-title: BMC Cancer doi: 10.1186/s12885-018-4221-0 contributor: fullname: J Matsushita – volume: 27 start-page: 361 year: 2009 ident: 58530_CR12 publication-title: Nat. Biotechnol. doi: 10.1038/nbt.1533 contributor: fullname: MP Ball – volume: 33 start-page: 5868 year: 2005 ident: 58530_CR9 publication-title: Nucleic Acids Research doi: 10.1093/nar/gki901 contributor: fullname: A Meissner – volume: 230 start-page: 1376 year: 2015 ident: 58530_CR15 publication-title: J. Cell. Physiol. doi: 10.1002/jcp.24882 contributor: fullname: M Nasu – volume: 84 start-page: 4613 year: 1999 ident: 58530_CR5 publication-title: J. Clin. Endocrinol. Metab. doi: 10.1210/jcem.84.12.6289 contributor: fullname: T Kosho – volume: 550 start-page: 244 year: 2017 ident: 58530_CR7 publication-title: Nature doi: 10.1038/nature24265 contributor: fullname: T Tukiainen – volume: 2016 start-page: 1 year: 2016 ident: 58530_CR16 publication-title: Biomed. Res. Int. doi: 10.1155/2016/6437658 contributor: fullname: M Nasu – volume: 16 start-page: 987 year: 2003 ident: 58530_CR10 publication-title: J. Pediatr. Endocrinol. Metab. doi: 10.1515/JPEM.2003.16.7.987 contributor: fullname: CFJ Munns – volume: 13 start-page: R87 year: 2012 ident: 58530_CR20 publication-title: Genome Biol. doi: 10.1186/gb-2012-13-10-r87 contributor: fullname: A Akalin – volume: 24 start-page: 1528 year: 2015 ident: 58530_CR8 publication-title: Hum. Mol. Genet. doi: 10.1093/hmg/ddu564 contributor: fullname: AM Cotton – volume: 63 start-page: 59 year: 2019 ident: 58530_CR13 publication-title: Essays Biochem. doi: 10.1042/EBC20180062 contributor: fullname: Z Sun – volume: 27 start-page: 1571 year: 2011 ident: 58530_CR19 publication-title: Bioinformatics doi: 10.1093/bioinformatics/btr167 contributor: fullname: F Krueger |
SSID | ssj0000529419 |
Score | 2.4692543 |
Snippet | All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based... Abstract All attempts to identify male-specific growth genes in humans have failed. This study aimed to clarify why men are taller than women. Microarray-based... |
SourceID | doaj proquest crossref pubmed springer |
SourceType | Open Website Aggregation Database Index Database Publisher |
StartPage | 8069 |
SubjectTerms | 631/136/2442 631/208/176/1988 631/208/199 692/308/2056 Adult Bisulfite Cartilage Cartilage - metabolism Child Chondrocytes Chondrocytes - metabolism CpG islands Deoxyribonucleic acid DNA DNA Methylation DNA microarrays Epigenesis, Genetic Epigenetics Female Females Genes Homeodomain Proteins - genetics Humanities and Social Sciences Humans Inactivation Male multidisciplinary Science Science (multidisciplinary) Sex differences Short Stature Homeobox Protein - genetics Transcriptomes X-chromosome inactivation |
SummonAdditionalLinks | – databaseName: Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV3daxQxEA-lUOiLaK262kqEvmnoNpnsJo-1thyC9UEL9xbyqcKxJ94WvP_eSbJ3VlR88XGz2d1kZpL5zc5khpAT1HEpJRUZok_LAA0M5nSwrFNJ-66Pfevz_453193sBt7O5fxOqa8cE1bTA1fCnaIA6sB5DAECeBVcBItarvOhh6BcLLtvy-8YUzWrN9dwpqdTMq1QpyvUVPk0GQeGCFm0TP-iiUrC_j-hzN88pEXxXN0n9ybESM_rSB-QnTgckL1aQ3L9kCwuv0-xrANd5AigFbVDoG-uz2muDr2usW50qs29ostEEfPRT2h-j58pik-kH2bv5_TLQH2mxgI3GDoWdtQ34f6Ykxr4NYLSQ3JzdfnxYsamEgrMg-hGpkBKK1vhgYOT3CEeSb12gCjAhQTSKs-5t-CxXTrtXOBWdD7J4PBSCPGI7A7LIT4htNfSyzOba1ZZUKjGAhpbNqQIEY2ivm_Iyw05zdeaKcMUD7dQphLfIPFNIb7RDXmdKb7tmbNclwbkvZl4b_7F-4YcbfhlpqW3wodE3jR5i994sb2NiyZ7QuwQl7elDxJEoLHYkMeVz9uRZE9pNqMa8mrD-J8v__uEnv6PCT0j-zxLaI4Mkkdkd_x2G48R9IzueZHvHybQ_QA priority: 102 providerName: Directory of Open Access Journals – databaseName: Springer Nature OA Free Journals dbid: C6C link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwlV1Lj9QwDLZgERIXxJvCgoLEDSJmE6dNj8uwqxESywFWmluUJ6w06iCmKzH_HrvtDFqxHDg2zaO1nfhznNgAr0nHlVJsloQ-vUQyMGRok5e1LW2sm9zMIu93fDqrF-f4cWmWU5gcvgtzxX-v7bsNKRi-BKZQErDVM9nehFukgxuW5nk93--nsMcKj9rpXsz1Ta_oniFE_3W48i-f6KBqTu_B3QkjiuORqffhRu4ewO0xa-T2IaxOfk2nVzux4jM_G-G7JD6cHQvOB70dT7eJKRv3RqyLIJQnvpHB3X8XJDBZfFl8XoqLTkQWnBUtKaIfGDD2RCsihzGIW4Khj-D89OTrfCGnpAkyoq57adEYb2Y6osJgVCAEUpo2IOn9kAoab6NS0WOkchPaEJLyuo7FpECPWuvHcNCtu_wURNOaaI48Z6nyaElxJTKvfCoZM5lBTVPBmx053Y8xNoYbfNraupH4jojvBuK7toL3TPF9TY5rPRQQu900TRwtNzSKyilhwmhTyOgJ09QxNZhsyBUc7vjlpsm2oUaal0k1ozFe7V_TNGHfh-_y-nKoQwTRZB5W8GTk8_5L2DfKhlMFb3eM_9P5v3_o2f9Vfw53FMsin_oxh3DQ_7zMLwjQ9OHlIMm_AW-F7E4 priority: 102 providerName: Springer Nature |
Title | Expression levels and DNA methylation profiles of the growth gene SHOX in cartilage tissues and chondrocytes |
URI | https://link.springer.com/article/10.1038/s41598-024-58530-9 https://www.ncbi.nlm.nih.gov/pubmed/38580675 https://www.proquest.com/docview/3033763209 https://search.proquest.com/docview/3034243871 https://doaj.org/article/3019d22edd4d4c8dbe4a7506cd74d8be |
Volume | 14 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Zb9QwEB5BKyReEOUMtCsj8QZWsz5yPKF22WqFxIKASvtm-UqLtEpKk0rsv2fseLdCHI9OLCeZGc98c8QD8BptXNM0laeIPjUV6GBQUztNi6qpbVH6Mrch3vFxWSzOxYeVXKWAW5_KKrc6MSpq19kQIz9GVRv2Asvrd1c_aOgaFbKrqYXGXdifMjTlKM_lqtzFWEIWS0zr9K9MzqvjHu1V-KeMCYo4mee0_s0exWP7_4Y1_8iTRvNz9hAeJNxITkZGH8Ad3z6Ce2Mnyc1jWM9_porWlqxDHVBPdOvI--UJCT2iN2PFG0kdunvSNQSRH7lAJ3y4JChEnnxdfFqR7y2xQZjWqGbIEJkyroRaMhxtYDcITZ_A-dn822xBUyMFagUvBloJKbXMuRVMGMkMopKmrI1ALGBcI6SuLGNWC4vXpamNcUzzwjbSGRxyzp_CXtu1_jmQspZWTnXoXKVFhcbMoculXeOFR9eoLDN4syWnuhrPy1Axz80rNRJfIfFVJL6qMzgNFN_NDGddxwvd9YVKW0ehCsKnMO-ccMJWznihEecU1pXCVcZncLjll0obsFe34pLBq91t3DohH6Jb393EOUgQji5jBs9GPu_eJORLgzOVwdst428X__cHvfj_u7yE-yzIXqj8kYewN1zf-CMENYOZRMmdwP7pfPn5C45mxWwSAwS_AKSZ9qw |
link.rule.ids | 314,780,784,864,2102,12056,21388,27924,27925,31719,31720,33744,33745,41120,42189,43310,43805,51576,73745,74302 |
linkProvider | ProQuest |
linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3db9QwDLfgJgQviM9RGBAk3iBa1yT9eEIb3HTAdiDYpHuL8tWBdGrH2kncf4_d5m5CfDy2jdLUduyfY9cGeIk2rq7rMnBEn4ZLdDC4rbzheVlXLi9CkTo67zie57NT-WGhFvHArYtplWudOChq3zo6I99FVUt7IUurN-c_OHWNouhqbKFxHbaocrqawNbBdP75y-aUheJYcq-Kf8ukotzt0GLRX2WZ5IiURcqr3yzSULj_b2jzj0jpYIAO78DtiBzZ_sjqu3AtNPfgxthLcnUfltOfMae1YUvKBOqYaTx7N99n1CV6Nea8sdiju2NtzRD7sTN0w_tvDMUosK-zTwv2vWGOxGmJiob1A1vGmVBPUnEDt0Jw-gBOD6cnb2c8tlLgToq856VUyqhUOJlJqzKLuKQuKisRDVhfS2VKl2XOSIf3la2s9ZkRuauVt3gphHgIk6ZtwiNgRaWc2jPUu8rIEs2ZR6fL-DrIgM5RUSTwak1OfT5WzNBDpFuUeiS-RuLrgfi6SuCAKL4ZSdWuhxvtxZmOm0ejEsK3ZMF76aUrvQ3SINLJnS-kL21IYGfNLx23YKevBCaBF5vHuHkoImKa0F4OY5AgAp3GBLZHPm9WQhFTcqcSeL1m_NXk__6gx_9fy3O4OTs5PtJH7-cfn8CtjOSQ8oDUDkz6i8vwFCFOb59FOf4FRRn3lg |
linkToPdf | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV1Zb9QwEB7BViBeEDeBAkbiDaxNfeR4Qi3d1XItFVBp3yyfpdIqabupxP57xol3K8TxGMdynJnxzDeesQfgFdq4EELlKaJPTQU6GNTUTtOiCrUtSl_mNu53fJ4Xs2PxYSEXKf9pldIqNzqxV9SutXGPfIyqNq4FltfjkNIijg6nb8_OaawgFSOtqZzGddhBq5izEewcTOZHX7c7LjGmJfbqdHIm59V4hdYrnjBjgiJq5jmtf7NO_SX-f0Oef0RNe2M0vQO3E4ok-wPb78I139yDG0NdyfV9WE5-pvzWhixjVtCK6MaRw_k-iRWj10P-G0n1ulekDQRxIDlBl7z7QVCkPPk2-7Igpw2xUbSWqHRI17NoGAl1ZrzowK4RqD6A4-nk-7sZTWUVqBW86GglpNQy51YwYSQziFFCWRuByMC4IKSuLGNWC4vt0tTGOKZ5YYN0Bh855w9h1LSNfwykrKWVezrWsdKiQtPm0AHTLnjh0VEqywxeb8ipzobbM1Qf9eaVGoivkPiqJ76qMziIFN_2jDdf9w3txYlKC0mhQsKvMO-ccMJWznihEfUU1pXCVcZnsLvhl0rLcaWuhCeDl9vXuJBidEQ3vr3s-yBBODqQGTwa-LydSYyeRtcqgzcbxl8N_u8fevL_ubyAmyjC6tP7-cencItFMYwpQXIXRt3FpX-GaKczz5MY_wLqFPvD |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Expression+levels+and+DNA+methylation+profiles+of+the+growth+gene+SHOX+in+cartilage+tissues+and+chondrocytes&rft.jtitle=Scientific+reports&rft.au=Hattori%2C+Atsushi&rft.au=Seki%2C+Atsuhito&rft.au=Inaba%2C+Naoto&rft.au=Nakabayashi%2C+Kazuhiko&rft.date=2024-04-05&rft.pub=Nature+Publishing+Group&rft.eissn=2045-2322&rft.volume=14&rft.issue=1&rft.spage=8069&rft_id=info:doi/10.1038%2Fs41598-024-58530-9&rft.externalDBID=HAS_PDF_LINK |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2045-2322&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2045-2322&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2045-2322&client=summon |