Identification and Functional Verification of MicroRNA-16 Family Targeting Intestinal Divalent Metal Transporter 1 (DMT1) in vitro and in vivo

Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1 is poorly understood. In this study, bioinformatic algorithms (TargetScan, PITA, miRanda, and miRDB) were applied to predict, screen, analyze,...

Full description

Saved in:
Bibliographic Details
Published inFrontiers in physiology Vol. 10; p. 819
Main Authors Jiang, Shuxia, Guo, Shihui, Li, Huifang, Ni, Yingdong, Ma, Wenqiang, Zhao, Ruqian
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers Media S.A 27.06.2019
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1 is poorly understood. In this study, bioinformatic algorithms (TargetScan, PITA, miRanda, and miRDB) were applied to predict, screen, analyze, and obtain microRNA-16 family members (miR-16, miR-195, miR-497, and miR-15b) targeting DMT1, seed sequence and their binding sites within DMT1 3' untranslated region (3' UTR) region. As demonstrated by dual-luciferase reporter assays, luciferase activity of DMT1 3' UTR reporter was impaired/enhanced when microRNA-16 family member over-expression plasmid/its inhibitor was transfected to HCT116 cells. Corroboratively, co-transfection of microRNA-16 family member over-expression plasmid and DMT1 3' UTR mutant reporter repressed the luciferase activity in HCT116 cells. In addition, over-expression microRNA-16 family member augmented its expression and diminished DMT1 protein expression in HCT116 cells. Interestingly, tail vein injection of miR-16 assay revealed reduced plasma iron levels, higher miR-16 expression, and lower DMT1 protein expression in the duodenum of mice. Taken together, we provide evidence that microRNA-16 family (miR-16, miR-195, miR-497, and miR-15b) is confirmed to repress intestinal DMT1 expression and , which will give valuable insight into post-transcriptional regulation of DMT1.
AbstractList Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1 is poorly understood. In this study, bioinformatic algorithms (TargetScan, PITA, miRanda, and miRDB) were applied to predict, screen, analyze, and obtain microRNA-16 family members (miR-16, miR-195, miR-497, and miR-15b) targeting DMT1, seed sequence and their binding sites within DMT1 3′ untranslated region (3′ UTR) region. As demonstrated by dual-luciferase reporter assays, luciferase activity of DMT1 3′ UTR reporter was impaired/enhanced when microRNA-16 family member over-expression plasmid/its inhibitor was transfected to HCT116 cells. Corroboratively, co-transfection of microRNA-16 family member over-expression plasmid and DMT1 3′ UTR mutant reporter repressed the luciferase activity in HCT116 cells. In addition, over-expression microRNA-16 family member augmented its expression and diminished DMT1 protein expression in HCT116 cells. Interestingly, tail vein injection of miR-16 assay revealed reduced plasma iron levels, higher miR-16 expression, and lower DMT1 protein expression in the duodenum of mice. Taken together, we provide evidence that microRNA-16 family (miR-16, miR-195, miR-497, and miR-15b) is confirmed to repress intestinal DMT1 expression in vitro and in vivo, which will give valuable insight into post-transcriptional regulation of DMT1.
Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1 is poorly understood. In this study, bioinformatic algorithms (TargetScan, PITA, miRanda, and miRDB) were applied to predict, screen, analyze, and obtain microRNA-16 family members (miR-16, miR-195, miR-497, and miR-15b) targeting DMT1, seed sequence and their binding sites within DMT1 3′ untranslated region (3′ UTR) region. As demonstrated by dual-luciferase reporter assays, luciferase activity of DMT1 3′ UTR reporter was impaired/enhanced when microRNA-16 family member over-expression plasmid/its inhibitor was transfected to HCT116 cells. Corroboratively, co-transfection of microRNA-16 family member over-expression plasmid and DMT1 3′ UTR mutant reporter repressed the luciferase activity in HCT116 cells. In addition, over-expression microRNA-16 family member augmented its expression and diminished DMT1 protein expression in HCT116 cells. Interestingly, tail vein injection of miR-16 assay revealed reduced plasma iron levels, higher miR-16 expression, and lower DMT1 protein expression in the duodenum of mice. Taken together, we provide evidence that microRNA-16 family (miR-16, miR-195, miR-497, and miR-15b) is confirmed to repress intestinal DMT1 expression in vitro and in vivo , which will give valuable insight into post-transcriptional regulation of DMT1.
Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1 is poorly understood. In this study, bioinformatic algorithms (TargetScan, PITA, miRanda, and miRDB) were applied to predict, screen, analyze, and obtain microRNA-16 family members (miR-16, miR-195, miR-497, and miR-15b) targeting DMT1, seed sequence and their binding sites within DMT1 3' untranslated region (3' UTR) region. As demonstrated by dual-luciferase reporter assays, luciferase activity of DMT1 3' UTR reporter was impaired/enhanced when microRNA-16 family member over-expression plasmid/its inhibitor was transfected to HCT116 cells. Corroboratively, co-transfection of microRNA-16 family member over-expression plasmid and DMT1 3' UTR mutant reporter repressed the luciferase activity in HCT116 cells. In addition, over-expression microRNA-16 family member augmented its expression and diminished DMT1 protein expression in HCT116 cells. Interestingly, tail vein injection of miR-16 assay revealed reduced plasma iron levels, higher miR-16 expression, and lower DMT1 protein expression in the duodenum of mice. Taken together, we provide evidence that microRNA-16 family (miR-16, miR-195, miR-497, and miR-15b) is confirmed to repress intestinal DMT1 expression and , which will give valuable insight into post-transcriptional regulation of DMT1.
Author Zhao, Ruqian
Li, Huifang
Ma, Wenqiang
Ni, Yingdong
Jiang, Shuxia
Guo, Shihui
AuthorAffiliation 1 Key Laboratory of Animal Physiology and Biochemistry, College of Veterinary Medicine, Nanjing Agricultural University , Nanjing , China
2 MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University , Nanjing , China
AuthorAffiliation_xml – name: 1 Key Laboratory of Animal Physiology and Biochemistry, College of Veterinary Medicine, Nanjing Agricultural University , Nanjing , China
– name: 2 MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University , Nanjing , China
Author_xml – sequence: 1
  givenname: Shuxia
  surname: Jiang
  fullname: Jiang, Shuxia
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
– sequence: 2
  givenname: Shihui
  surname: Guo
  fullname: Guo, Shihui
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
– sequence: 3
  givenname: Huifang
  surname: Li
  fullname: Li, Huifang
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
– sequence: 4
  givenname: Yingdong
  surname: Ni
  fullname: Ni, Yingdong
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
– sequence: 5
  givenname: Wenqiang
  surname: Ma
  fullname: Ma, Wenqiang
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
– sequence: 6
  givenname: Ruqian
  surname: Zhao
  fullname: Zhao, Ruqian
  organization: MOE Joint International Research Laboratory of Animal Health and Food Safety, Nanjing Agricultural University, Nanjing, China
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31316397$$D View this record in MEDLINE/PubMed
BookMark eNpVkk1vEzEQhi1UREvpnRPysRw2-Gu96wtS1TYQqWklFBA3y-uP1NXGDvYmUv5EfzPOppTWF894Zp6xPe97cBRisAB8xGhCaSu-uPX9Lk8IwmKCUIvFG3CCOWcVYuT30Qv7GJzl_IDKYogghN-BY4op5lQ0J-BxZmwYvPNaDT4GqIKB003Qe0f18JdN_2PRwbnXKf64vagwh1O18v0OLlRa2sGHJZyFweZilborv1V9AcO5HYq7SCrkdUyDTRDD86v5An-GPsCtH1Ice47ONn4Ab53qsz172k_Bz-n14vJ7dXP3bXZ5cVPpmrRD5TgT2nXIalQrwzVxxGjWtp22DWWMd4R1qmksta1xtGHCUdHWXdd0VNcNRfQUzA5cE9WDXCe_Umkno_JyPIhpKVUavO6ttEaLVmFBKGbM1LprWlyjGmMjNDWOF9bXA2u96VYluzw7qf4V9HUk-Hu5jFvJOS7zoQVw_gRI8c-mfKFc-axt36tg4yZLQmohEOfNPhUdUssYck7WPbfBSO5VIUdVyL0q5KiKUvLp5fWeC_5pgP4FNyC3lg
CitedBy_id crossref_primary_10_1142_S2591722620400050
crossref_primary_10_1016_j_ymthe_2021_03_022
crossref_primary_10_1007_s13577_022_00699_0
crossref_primary_10_3390_cells8101135
crossref_primary_10_1155_2020_6062094
crossref_primary_10_3389_fcell_2020_00015
crossref_primary_10_3389_fvets_2021_711576
crossref_primary_10_3390_nu13072331
crossref_primary_10_3390_biology10070653
Cites_doi 10.3389/fnagi.2018.00165
10.3389/fphys.2017.00551
10.1172/jci38499
10.1093/nar/gkj112
10.1073/pnas.0804373105
10.1186/s12885-015-1458-8
10.3324/haematol.2009.020685
10.12659/msm.898574
10.1016/j.biopha.2018.07.105
10.3389/fphys.2018.00355
10.1097/MIB.0b013e31829e71cf
10.1152/ajpgi.2000.278.6.G930
10.1093/nar/gku1104
10.1182/blood-2008-04-150953
10.1038/nbt.1543
10.1038/nrg.2016.20
10.1371/journal.pone.0032754
10.1007/s00109-015-1362-3
10.1007/978-1-4939-2547-6_17
10.1159/000485876
10.1093/nar/gku988
10.1016/j.cell.2009.01.002
10.1053/j.gastro.2017.01.049
10.1371/journal.pgen.1003408
10.1055/s-0043-118910
10.1038/msb.2010.24
10.1073/pnas.0511155103
10.3390/nu9060617
10.1038/ijo.2009.141
10.1182/blood.V93.12.4406
10.1038/onc.2012.214
10.1016/j.cell.2007.04.037
10.1073/pnas.95.3.1148
10.1038/ng2135
10.1186/s40104-017-0204-2
10.1007/s12672-016-0276-z
10.1016/j.cell.2011.07.014
10.1038/ng0897-383
10.1016/j.tcm.2012.05.003
10.1371/journal.pbio.0020363
10.1038/s41467-018-03072-8
10.1016/j.cmet.2016.07.015
10.1016/j.cmet.2008.12.012
10.1016/j.celrep.2013.02.026
10.1016/j.molmed.2014.06.005
10.1002/jcb.26297
10.1186/s12974-016-0753-x
10.3390/ijms140611171
10.1016/s1001-9294(10)60043-0
10.1172/jci24356
10.1016/j.tcb.2015.07.011
10.1016/j.molcel.2016.09.027
10.3892/mmr.2016.6088
10.1016/j.exphem.2008.10.002
10.1667/RR14428.1
10.7554/eLife.29538
10.1101/gr.082701.108
10.1172/jci44883
10.1016/s0014-5793(01)03189-1
10.1186/1758-907x-3-3
ContentType Journal Article
Copyright Copyright © 2019 Jiang, Guo, Li, Ni, Ma and Zhao. 2019 Jiang, Guo, Li, Ni, Ma and Zhao
Copyright_xml – notice: Copyright © 2019 Jiang, Guo, Li, Ni, Ma and Zhao. 2019 Jiang, Guo, Li, Ni, Ma and Zhao
DBID NPM
AAYXX
CITATION
7X8
5PM
DOA
DOI 10.3389/fphys.2019.00819
DatabaseName PubMed
CrossRef
MEDLINE - Academic
PubMed Central (Full Participant titles)
DOAJ Directory of Open Access Journals
DatabaseTitle PubMed
CrossRef
MEDLINE - Academic
DatabaseTitleList

PubMed
Database_xml – sequence: 1
  dbid: DOA
  name: DOAJ Directory of Open Access Journals
  url: https://www.doaj.org/
  sourceTypes: Open Website
– sequence: 2
  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
DeliveryMethod fulltext_linktorsrc
EISSN 1664-042X
EndPage 819
ExternalDocumentID oai_doaj_org_article_edc98a1923144d5cb78150511d9c3df6
10_3389_fphys_2019_00819
31316397
Genre Journal Article
GrantInformation_xml – fundername: National Natural Science Foundation of China
  grantid: 31302053; 31872439
GroupedDBID 53G
5VS
9T4
AAFWJ
AAKDD
ACGFO
ACGFS
ACXDI
ADBBV
ADRAZ
AENEX
AFPKN
ALMA_UNASSIGNED_HOLDINGS
AOIJS
BCNDV
DIK
EMOBN
F5P
GROUPED_DOAJ
GX1
HYE
IAO
IEA
IHR
IHW
IPNFZ
ISR
KQ8
M48
M~E
NPM
O5R
O5S
OK1
PGMZT
RIG
RNS
RPM
AAYXX
CITATION
7X8
5PM
ID FETCH-LOGICAL-c528t-f649cfb0ec05ad6c2f2dc488bce73446b24ba77e3e8df3749f3985bb7b3c57303
IEDL.DBID RPM
ISSN 1664-042X
IngestDate Tue Oct 22 14:54:01 EDT 2024
Tue Sep 17 21:28:42 EDT 2024
Fri Oct 25 09:27:57 EDT 2024
Thu Sep 26 18:26:58 EDT 2024
Sat Sep 28 08:39:28 EDT 2024
IsDoiOpenAccess true
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Keywords functional verification
intestine
regulation
DMT1
microRNA-16 family
Language English
License This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c528t-f649cfb0ec05ad6c2f2dc488bce73446b24ba77e3e8df3749f3985bb7b3c57303
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
Reviewed by: Jinlian Hua, Northwest A&F University, China; Shikha Prasad, Northwestern University, United States
This article was submitted to Gastrointestinal Sciences, a section of the journal Frontiers in Physiology
Edited by: Stephen J. Pandol, Cedars-Sinai Medical Center, United States
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6610423/
PMID 31316397
PQID 2259906673
PQPubID 23479
PageCount 1
ParticipantIDs doaj_primary_oai_doaj_org_article_edc98a1923144d5cb78150511d9c3df6
pubmedcentral_primary_oai_pubmedcentral_nih_gov_6610423
proquest_miscellaneous_2259906673
crossref_primary_10_3389_fphys_2019_00819
pubmed_primary_31316397
PublicationCentury 2000
PublicationDate 2019-06-27
PublicationDateYYYYMMDD 2019-06-27
PublicationDate_xml – month: 06
  year: 2019
  text: 2019-06-27
  day: 27
PublicationDecade 2010
PublicationPlace Switzerland
PublicationPlace_xml – name: Switzerland
PublicationTitle Frontiers in physiology
PublicationTitleAlternate Front Physiol
PublicationYear 2019
Publisher Frontiers Media S.A
Publisher_xml – name: Frontiers Media S.A
References John (B29) 2004; 2
Oates (B40) 2000; 278
Galy (B18) 2013; 3
Lo (B37) 2018; 9
Tilghman (B53) 2012; 7
Wang (B54) 2017; 8
Zhang (B60) 2016; 22
Iwakawa (B28) 2015; 25
Fleming (B15) 1997; 16
Schaar (B47) 2009; 37
Pena-Philippides (B41) 2016; 13
Kertesz (B30) 2007; 39
Fan (B13) 2017; 49
Ameres (B1) 2007; 130
Hayes (B26) 2014; 20
Shah (B48) 2009; 9
Li (B32) 2017; 15
Arvey (B3) 2010; 6
Zhai (B59) 2013; 19
Canonne-Hergaux (B7) 1999; 93
Friedman (B17) 2009; 19
Castoldi (B9) 2011; 121
Andolfo (B2) 2010; 95
Foot (B16) 2008; 112
Clement (B10) 2015; 1296
Guo (B24) 2018; 9
Cummins (B11) 2006; 103
Wong (B57) 2015; 43
Gunshin (B23) 2005; 115
Quek (B42) 2015; 43
Wang (B55) 2016; 186
Canonne-Hergaux (B6) 2000; 96
Caporali (B8) 2011; 21
Wang (B56) 2018; 106
Salazar (B44) 2008; 105
Salmena (B45) 2011; 146
Khan (B31) 2009; 27
Nagata (B39) 2013; 14
Tian (B52) 2017; 6
Zhou (B61) 2017; 44
He (B27) 2017; 152
Lo (B36) 2017; 8
Denzler (B12) 2016; 64
Xue (B58) 2016; 24
Griffiths-Jones (B21) 2006; 34
Liu (B35) 2018; 119
Tian (B50) 2018; 10
Tian (B51) 2017; 8
Gong (B20) 2009; 33
Thomson (B49) 2016; 17
Guo (B25) 2013; 32
Gunshin (B22) 2001; 509
Gong (B19) 2010; 25
Liang (B34) 2015; 15
Sangokoya (B46) 2013; 9
Saito (B43) 2012; 3
Babu (B4) 2016; 94
Li (B33) 2017; 9
Fleming (B14) 1998; 95
Bartel (B5) 2009; 136
Mastrogiannaki (B38) 2009; 119
References_xml – volume: 10
  year: 2018
  ident: B50
  article-title: Lower expression of Ndfip1 is associated with Alzheimer disease pathogenesis through decreasing DMT1 degradation and increasing iron influx.
  publication-title: Front. Aging Neurosci.
  doi: 10.3389/fnagi.2018.00165
  contributor:
    fullname: Tian
– volume: 8
  year: 2017
  ident: B36
  article-title: MicroRNA-146a-5p mediates high glucose-induced endothelial inflammation via targeting interleukin-1 receptor-associated kinase 1 expression.
  publication-title: Front. Physiol.
  doi: 10.3389/fphys.2017.00551
  contributor:
    fullname: Lo
– volume: 119
  start-page: 1159
  year: 2009
  ident: B38
  article-title: HIF-2alpha, but not HIF-1alpha, promotes iron absorption in mice.
  publication-title: J. Clin. Invest.
  doi: 10.1172/jci38499
  contributor:
    fullname: Mastrogiannaki
– volume: 34
  start-page: D140
  year: 2006
  ident: B21
  article-title: MiRBase: microRNA sequences, targets and gene nomenclature.
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkj112
  contributor:
    fullname: Griffiths-Jones
– volume: 105
  start-page: 18578
  year: 2008
  ident: B44
  article-title: Divalent metal transporter 1 (DMT1) contributes to neurodegeneration in animal models of Parkinson’s disease.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0804373105
  contributor:
    fullname: Salazar
– volume: 15
  year: 2015
  ident: B34
  article-title: MiR-16 promotes the apoptosis of human cancer cells by targeting FEAT.
  publication-title: BMC Cancer
  doi: 10.1186/s12885-015-1458-8
  contributor:
    fullname: Liang
– volume: 95
  start-page: 1244
  year: 2010
  ident: B2
  article-title: Regulation of divalent metal transporter 1 (DMT1) non-IRE isoform by the microRNA Let-7d in erythroid cells.
  publication-title: Haematologica
  doi: 10.3324/haematol.2009.020685
  contributor:
    fullname: Andolfo
– volume: 22
  start-page: 4820
  year: 2016
  ident: B60
  article-title: Expression of long non-coding RNA (lncRNA) small nucleolar RNA host gene 1 (SNHG1) exacerbates hepatocellular carcinoma through suppressing miR-195.
  publication-title: Med. Sci. Monit.
  doi: 10.12659/msm.898574
  contributor:
    fullname: Zhang
– volume: 106
  start-page: 1661
  year: 2018
  ident: B56
  article-title: LncRNA SNHG16 reverses the effects of miR-15a/16 on LPS-induced inflammatory pathway.
  publication-title: Biomed. Pharmacother.
  doi: 10.1016/j.biopha.2018.07.105
  contributor:
    fullname: Wang
– volume: 9
  year: 2018
  ident: B37
  article-title: MicroRNA-200a/200b modulate high glucose-induced endothelial inflammation by targeting O-linked N-acetylglucosamine transferase expression.
  publication-title: Front. Physiol.
  doi: 10.3389/fphys.2018.00355
  contributor:
    fullname: Lo
– volume: 19
  start-page: 2295
  year: 2013
  ident: B59
  article-title: miR-106b fine tunes ATG16L1 expression and autophagic activity in intestinal epithelial HCT116 cells.
  publication-title: Inflamm. Bowel. Dis.
  doi: 10.1097/MIB.0b013e31829e71cf
  contributor:
    fullname: Zhai
– volume: 278
  start-page: G930
  year: 2000
  ident: B40
  article-title: Gene expression of divalent metal transporter 1 and transferrin receptor in duodenum of Belgrade rats.
  publication-title: Am. J. Physiol. Gastrointest. Liver Physiol.
  doi: 10.1152/ajpgi.2000.278.6.G930
  contributor:
    fullname: Oates
– volume: 43
  start-page: D146
  year: 2015
  ident: B57
  article-title: MiRDB: an online resource for microRNA target prediction and functional annotations.
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gku1104
  contributor:
    fullname: Wong
– volume: 112
  start-page: 4268
  year: 2008
  ident: B16
  article-title: Regulation of the divalent metal ion transporter DMT1 and iron homeostasis by a ubiquitin-dependent mechanism involving Ndfips and WWP2.
  publication-title: Blood
  doi: 10.1182/blood-2008-04-150953
  contributor:
    fullname: Foot
– volume: 27
  start-page: 549
  year: 2009
  ident: B31
  article-title: Transfection of small RNAs globally perturbs gene regulation by endogenous microRNAs.
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.1543
  contributor:
    fullname: Khan
– volume: 17
  start-page: 272
  year: 2016
  ident: B49
  article-title: Endogenous microRNA sponges: evidence and controversy.
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg.2016.20
  contributor:
    fullname: Thomson
– volume: 7
  year: 2012
  ident: B53
  article-title: Endocrine disruptor regulation of microRNA expression in breast carcinoma cells.
  publication-title: PLoS One
  doi: 10.1371/journal.pone.0032754
  contributor:
    fullname: Tilghman
– volume: 94
  start-page: 347
  year: 2016
  ident: B4
  article-title: MiR-20a regulates expression of the iron exporter ferroportin in lung cancer.
  publication-title: J. Mol. Med.
  doi: 10.1007/s00109-015-1362-3
  contributor:
    fullname: Babu
– volume: 1296
  start-page: 187
  year: 2015
  ident: B10
  article-title: Dual luciferase gene reporter assays to study miRNA function.
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-2547-6_17
  contributor:
    fullname: Clement
– volume: 44
  start-page: 1867
  year: 2017
  ident: B61
  article-title: MicroRNA-195 suppresses the progression of pancreatic cancer by targeting DCLK1.
  publication-title: Cell Physiol. Biochem.
  doi: 10.1159/000485876
  contributor:
    fullname: Zhou
– volume: 43
  start-page: D168
  year: 2015
  ident: B42
  article-title: LncRNAdb v2.0: expanding the reference database for functional long noncoding RNAs.
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gku988
  contributor:
    fullname: Quek
– volume: 136
  start-page: 215
  year: 2009
  ident: B5
  article-title: MicroRNAs: target recognition and regulatory functions.
  publication-title: Cell
  doi: 10.1016/j.cell.2009.01.002
  contributor:
    fullname: Bartel
– volume: 152
  start-page: 1434.e15
  year: 2017
  ident: B27
  article-title: MicroRNA 301A promotes intestinal inflammation and colitis-associated cancer development by inhibiting BTG1.
  publication-title: Gastroenterology
  doi: 10.1053/j.gastro.2017.01.049
  contributor:
    fullname: He
– volume: 9
  year: 2013
  ident: B46
  article-title: Iron-responsive miR-485-3p regulates cellular iron homeostasis by targeting ferroportin.
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1003408
  contributor:
    fullname: Sangokoya
– volume: 49
  start-page: 793
  year: 2017
  ident: B13
  article-title: Effects of zinc alpha2 glycoprotein on lipid metabolism of liver in high-fat diet-induced obese mice.
  publication-title: Horm. Metab. Res.
  doi: 10.1055/s-0043-118910
  contributor:
    fullname: Fan
– volume: 6
  year: 2010
  ident: B3
  article-title: Target mRNA abundance dilutes microRNA and siRNA activity.
  publication-title: Mol. Syst. Biol.
  doi: 10.1038/msb.2010.24
  contributor:
    fullname: Arvey
– volume: 103
  start-page: 3687
  year: 2006
  ident: B11
  article-title: The colorectal microRNAome.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0511155103
  contributor:
    fullname: Cummins
– volume: 9
  year: 2017
  ident: B33
  article-title: Long-term dexamethasone exposure down-regulates hepatic TFR1 and reduces liver iron concentration in rats.
  publication-title: Nutrients
  doi: 10.3390/nu9060617
  contributor:
    fullname: Li
– volume: 33
  start-page: 1023
  year: 2009
  ident: B20
  article-title: Zinc-alpha2-glycoprotein is involved in regulation of body weight through inhibition of lipogenic enzymes in adipose tissue.
  publication-title: Int. J. Obes.
  doi: 10.1038/ijo.2009.141
  contributor:
    fullname: Gong
– volume: 93
  start-page: 4406
  year: 1999
  ident: B7
  article-title: Cellular and subcellular localization of the Nramp2 iron transporter in the intestinal brush border and regulation by dietary iron.
  publication-title: Blood
  doi: 10.1182/blood.V93.12.4406
  contributor:
    fullname: Canonne-Hergaux
– volume: 32
  start-page: 1910
  year: 2013
  ident: B25
  article-title: MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer.
  publication-title: Oncogene
  doi: 10.1038/onc.2012.214
  contributor:
    fullname: Guo
– volume: 130
  start-page: 101
  year: 2007
  ident: B1
  article-title: Molecular basis for target RNA recognition and cleavage by human RISC.
  publication-title: Cell
  doi: 10.1016/j.cell.2007.04.037
  contributor:
    fullname: Ameres
– volume: 95
  start-page: 1148
  year: 1998
  ident: B14
  article-title: Nramp2 is mutated in the anemic Belgrade (b) rat: evidence of a role for Nramp2 in endosomal iron transport.
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.95.3.1148
  contributor:
    fullname: Fleming
– volume: 39
  start-page: 1278
  year: 2007
  ident: B30
  article-title: The role of site accessibility in microRNA target recognition.
  publication-title: Nat. Genet.
  doi: 10.1038/ng2135
  contributor:
    fullname: Kertesz
– volume: 8
  year: 2017
  ident: B51
  article-title: Negative effects of long-term feeding of high-grain diets to lactating goats on milk fat production and composition by regulating gene expression and DNA methylation in the mammary gland.
  publication-title: J. Anim. Sci. Biotechnol.
  doi: 10.1186/s40104-017-0204-2
  contributor:
    fullname: Tian
– volume: 8
  start-page: 49
  year: 2017
  ident: B54
  article-title: MiR-15b inhibits the progression of glioblastoma cells through targeting insulin-like growth factor receptor 1.
  publication-title: Horm Cancer
  doi: 10.1007/s12672-016-0276-z
  contributor:
    fullname: Wang
– volume: 146
  start-page: 353
  year: 2011
  ident: B45
  article-title: A ceRNA hypothesis: the rosetta stone of a hidden RNA language?
  publication-title: Cell
  doi: 10.1016/j.cell.2011.07.014
  contributor:
    fullname: Salmena
– volume: 16
  start-page: 383
  year: 1997
  ident: B15
  article-title: Microcytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene.
  publication-title: Nat. Genet.
  doi: 10.1038/ng0897-383
  contributor:
    fullname: Fleming
– volume: 21
  start-page: 162
  year: 2011
  ident: B8
  article-title: MicroRNA-503 and the extended microRNA-16 family in angiogenesis.
  publication-title: Trends Cardiovasc. Med.
  doi: 10.1016/j.tcm.2012.05.003
  contributor:
    fullname: Caporali
– volume: 2
  year: 2004
  ident: B29
  article-title: Human microRNA targets.
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.0020363
  contributor:
    fullname: John
– volume: 9
  year: 2018
  ident: B24
  article-title: Ultraconserved element uc.372 drives hepatic lipid accumulation by suppressing miR-195/miR4668 maturation.
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-018-03072-8
  contributor:
    fullname: Guo
– volume: 24
  start-page: 447
  year: 2016
  ident: B58
  article-title: Iron uptake via DMT1 integrates cell cycle with JAK-STAT3 signaling to promote colorectal tumorigenesis.
  publication-title: Cell Metab.
  doi: 10.1016/j.cmet.2016.07.015
  contributor:
    fullname: Xue
– volume: 9
  start-page: 152
  year: 2009
  ident: B48
  article-title: Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency.
  publication-title: Cell Metab.
  doi: 10.1016/j.cmet.2008.12.012
  contributor:
    fullname: Shah
– volume: 3
  start-page: 844
  year: 2013
  ident: B18
  article-title: Iron regulatory proteins control a mucosal block to intestinal iron absorption.
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2013.02.026
  contributor:
    fullname: Galy
– volume: 20
  start-page: 460
  year: 2014
  ident: B26
  article-title: MicroRNAs in cancer: biomarkers, functions and therapy.
  publication-title: Trends Mol. Med.
  doi: 10.1016/j.molmed.2014.06.005
  contributor:
    fullname: Hayes
– volume: 119
  start-page: 1368
  year: 2018
  ident: B35
  article-title: Knockdown of long non-coding RNA MALAT1 inhibits growth and motility of human hepatoma cells via modulation of miR-195.
  publication-title: J. Cell. Biochem.
  doi: 10.1002/jcb.26297
  contributor:
    fullname: Liu
– volume: 13
  year: 2016
  ident: B41
  article-title: In vivo inhibition of miR-155 significantly alters post-stroke inflammatory response.
  publication-title: J. Neuroinflam.
  doi: 10.1186/s12974-016-0753-x
  contributor:
    fullname: Pena-Philippides
– volume: 14
  start-page: 11171
  year: 2013
  ident: B39
  article-title: Fluctuation of global gene expression by endogenous miRNA response to the introduction of an exogenous miRNA.
  publication-title: Int. J. Mol. Sci.
  doi: 10.3390/ijms140611171
  contributor:
    fullname: Nagata
– volume: 25
  start-page: 169
  year: 2010
  ident: B19
  article-title: Fatty acid synthase and hormone-sensitive lipase expression in liver are involved in zinc-alpha2-glycoprotein-induced body fat loss in obese mice.
  publication-title: Chin. Med. Sci. J.
  doi: 10.1016/s1001-9294(10)60043-0
  contributor:
    fullname: Gong
– volume: 115
  start-page: 1258
  year: 2005
  ident: B23
  article-title: Slc11a2 is required for intestinal iron absorption and erythropoiesis but dispensable in placenta and liver.
  publication-title: J. Clin. Invest.
  doi: 10.1172/jci24356
  contributor:
    fullname: Gunshin
– volume: 25
  start-page: 651
  year: 2015
  ident: B28
  article-title: The functions of microRNAs: mRNA decay and translational repression.
  publication-title: Trends Cell. Biol.
  doi: 10.1016/j.tcb.2015.07.011
  contributor:
    fullname: Iwakawa
– volume: 64
  start-page: 565
  year: 2016
  ident: B12
  article-title: Impact of microRNA levels, target-site complementarity, and cooperativity on competing endogenous RNA-regulated gene expression.
  publication-title: Mol. Cell.
  doi: 10.1016/j.molcel.2016.09.027
  contributor:
    fullname: Denzler
– volume: 15
  start-page: 833
  year: 2017
  ident: B32
  article-title: Influence of microRNA-34a on proliferation, invasion and metastasis of HCT116 cells.
  publication-title: Mol. Med. Rep.
  doi: 10.3892/mmr.2016.6088
  contributor:
    fullname: Li
– volume: 96
  start-page: 3964
  year: 2000
  ident: B6
  article-title: The Nramp2/DMT1 iron transporter is induced in the duodenum of microcytic anemia mk mice but is not properly targeted to the intestinal brush border.
  publication-title: Blood
  contributor:
    fullname: Canonne-Hergaux
– volume: 37
  start-page: 245
  year: 2009
  ident: B47
  article-title: MiR-320 targets transferrin receptor 1 (CD71) and inhibits cell proliferation.
  publication-title: Exp. Hematol.
  doi: 10.1016/j.exphem.2008.10.002
  contributor:
    fullname: Schaar
– volume: 186
  start-page: 292
  year: 2016
  ident: B55
  article-title: MiR-29a regulates radiosensitivity in human intestinal cells by targeting PTEN gene.
  publication-title: Radiat. Res.
  doi: 10.1667/RR14428.1
  contributor:
    fullname: Wang
– volume: 6
  year: 2017
  ident: B52
  article-title: Stress responsive miR-31 is a major modulator of mouse intestinal stem cells during regeneration and tumorigenesis.
  publication-title: eLife
  doi: 10.7554/eLife.29538
  contributor:
    fullname: Tian
– volume: 19
  start-page: 92
  year: 2009
  ident: B17
  article-title: Most mammalian mRNAs are conserved targets of microRNAs.
  publication-title: Genome Res.
  doi: 10.1101/gr.082701.108
  contributor:
    fullname: Friedman
– volume: 121
  start-page: 1386
  year: 2011
  ident: B9
  article-title: The liver-specific microRNA miR-122 controls systemic iron homeostasis in mice.
  publication-title: J. Clin. Invest.
  doi: 10.1172/jci44883
  contributor:
    fullname: Castoldi
– volume: 509
  start-page: 309
  year: 2001
  ident: B22
  article-title: Iron-dependent regulation of the divalent metal ion transporter.
  publication-title: FEBS Lett.
  doi: 10.1016/s0014-5793(01)03189-1
  contributor:
    fullname: Gunshin
– volume: 3
  year: 2012
  ident: B43
  article-title: Target gene expression levels and competition between transfected and endogenous microRNAs are strong confounding factors in microRNA high-throughput experiments.
  publication-title: Silence
  doi: 10.1186/1758-907x-3-3
  contributor:
    fullname: Saito
SSID ssj0000402001
Score 2.3052363
Snippet Divalent metal transporter 1 (DMT1) is a key transporter of iron uptake and delivering in human and animals. However, post-transcriptional regulation of DMT1...
SourceID doaj
pubmedcentral
proquest
crossref
pubmed
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage 819
SubjectTerms DMT1
functional verification
intestine
microRNA-16 family
Physiology
regulation
SummonAdditionalLinks – databaseName: DOAJ Directory of Open Access Journals
  dbid: DOA
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV07T8MwELYQEwsC8QovGYkBhogkdmJ7BEqFkMqACmKL4pfokqCq5Wfwm7mz29IiJBbGxEls-Tvb39mX7wg5RwovWe5TwyuecsGrVGXOpswym-VWmiyo7Q8eq_tn_vBavi6l-sKYsCgPHDvuylmjZBN4COe2NFpI4DBAE6wyzPootp2pJWcqzMHoFmV5PJcEL0xdedwpwFAu1KeUKKyztA4Fuf7fOObPUMmltae_RTZnpJFex8ZukzXX7pDP-I-tn2260aa1tA-rVNzcoy9gWouyztMBRt49PV6neUVjtgs6DFHgsHZR3BeEsY7v9UZge_BhOnDAy-m3-PmY5vSiNxjml3TU0o_RZNyFOsPFR7dLnvt3w9v7dJZdITVlISepr7gyXmcO4GhsZQpfWAPDWRsnGDiJuuC6EcIxJ61ngivPlCy1FpqZEuYFtkfW2651B4SWUNxwaSQDwIXxSuiGZ4Z5XXqW8SYhl_O-rt-jiEYNzgfiUgdcasSlDrgk5AbBWDyH8tfhBhhFPTOK-i-jSMjZHMoahguegTSt66ZQEbh7KuQ6Tch-hHZRFctZjuecCREroK-0ZbWkHb0FSW5gORhgdPgfjT8iG9gdGI9WiGOyPhlP3Qkwn4k-DUb-BS_oAto
  priority: 102
  providerName: Directory of Open Access Journals
– databaseName: Scholars Portal Open Access Journals
  dbid: M48
  link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1LT9wwELYQvXCpWlEgfSBX4sAeUpLYiZ1DhSjLaoW0e0C71d6i-NVGqhJIF9T-if5mZpzswlZ75Jg4ji1_Hs834_GYkBOk8JLFLtQ84yEXPAvzyJqQGWai2Egd-Wz7k2k2nvPrRbp4Oh7dD-DvraYd3ic1b399-XP39xwE_itanKBvzxw6ATBKC1NPSswB-irhYKdjIF9P9v26jKZSFHd7lVsrbugmn8J_G-_8P3zymT4avSGveyJJLzrk35IdW--Tf925W9c74mhZGzoCzdU5_Oh3mG7rssbRCUbj3Uwvwjij3Q0YdOYjw0GfUfQVgvxjvWEF8xF-TCcWhok-JURvaUxPh5NZPKBVTR-qZdv4Nv3DQ_OOzEdXs8tx2N-4EOo0kcvQZTzXTkUWICpNphOXGA0irrQVDAxHlXBVCmGZlcYxwXPHcpkqJRTTKawV7IDs1k1tjwhNobjkUksGk0BolwtV8kgzp1LHIl4GZLAa6-K2S6xRgEGCuBQelwJxKTwuAfmGYKy_w5TY_kXT_ih6CSsAj1yWnrByblKthASyC3zS5JoZlwXk8wrKAkQI90XK2jb30BCYgLm__zQghx2066ZYzGLc-wyI2AB9oy-bJXX106fpBuaDQUfvX6LzH8geDgfGqCXiI9ldtvf2E7ChpTr2k_wRT7ULOA
  priority: 102
  providerName: Scholars Portal
Title Identification and Functional Verification of MicroRNA-16 Family Targeting Intestinal Divalent Metal Transporter 1 (DMT1) in vitro and in vivo
URI https://www.ncbi.nlm.nih.gov/pubmed/31316397
https://search.proquest.com/docview/2259906673
https://pubmed.ncbi.nlm.nih.gov/PMC6610423
https://doaj.org/article/edc98a1923144d5cb78150511d9c3df6
Volume 10
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1LT9wwEB4Bh4pLBaKlaQG5Ug_lEDaJndg-8lqhSkFVtVTcovjVRoIErRZ-Br-ZsZMsLOLEJVLiOLb8jTMPfx4D_PAmvKCpizUrWMw4K2KZWBNTQ02SGqGTkG2_vCwurtiv6_x6DfJxL0wg7WvVHLU3t0dt8z9wK-9u9WTkiU1-l6eoUzydY7IO6yigL1z08Pv1HlGS9kuS6IDJifNBAs_i8qkpUQNuwgea0tQvaa1oo5C0_y1L8zVh8oUGmm7Bx8F0JMd9F7dhzbY78NjvtHVD6I3UrSFT1FV9iI_8RQFblnWOlJ5_9-fyOE4L0p95QWaBC44ajPjoIM54X--sQQnED5PSonVOnlOgz0lKfp6Vs_SQNC15aBbzLrQZbh66T3A1PZ-dXsTDGQuxzjOxiF3BpHYqsQhKbQqducxonNRKW07RVVQZUzXnllphHOVMOipFrhRXVOc4-PQzbLRda78AybG4ZkILirBz7SRXNUs0dSp3NGF1BIfjWFd3fSqNCl0QD1EVIKo8RFWAKIITD8byPZ8EOzzo5v-qQRQqxEOKOpiojJlcKy7QvEUL0khNjSsi-D5CWeGk8SshdWu7e2wInT4ZTjyNYLeHdtnUKBoR8BXQV_qyWoJyGhJzD3L59d01v8GmHwNPRcv4Hmws5vd2H42ehToIwQK8lkwcBIF_Asz-BU0
link.rule.ids 230,315,730,783,787,867,888,2109,24330,27936,27937,53804,53806
linkProvider National Library of Medicine
linkToHtml http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwEB6VIkEvPMQrPI3EgR6ym8ROnBxLy2qBZoXQturNil8QQZNqle2BH8FvZuwkS7fiAsfESezk--yZsb-MAd44Fz6nsQ0Vy1jIOMvCIjI6pJrqKNa5iny2_XKRzU_Yx7P0bAfS8V8YL9pXsp40P84nTf3NaysvztV01IlNP5eHaFOcnGN6A25if43YlSDdD8AuJoriflESQ7Biat00gdNxueSUaAP34BaNaewWtbbskU_b_zdf87pk8ooNmt2F07H1vfTk-2TdyYn6eS2x4z-_3j24M3il5KAvvg87pnkAv_qfeO0wq0eqRpMZmsF-9pCcInc3Za0lpZP2fVkchHFG-u00yNLLzNE4EjfxiIOJu--oRnLjg0lp0PEnf7Krr0hM3h6Vy3if1A25rLtV6-v0B5ftQziZvV8ezsNh-4ZQpUnehTZjhbIyMoh3pTOV2EQrHC-kMpxiFCoTJivODTW5tpSzwtIiT6XkkqoUBx76CHabtjFPgKRYXLFc5RQZxZUtuKxYpKiVqaURqwLYH0EUF32WDoHRjcNeeOyFw1547AN451DeXOfya_sT7eqrGGAQCHSRV977ZUynSvIcPWd0TnWhqLZZAK9Hjgjsj26RpWpMu8aKMJ4s_GaqATzuObOpauRcAHyLTVtt2S5Bjvic3wMnnv73na_g9nxZHovjD4tPz2DPfQ-neEv4c9jtVmvzAn2rTr70Pek3mrglag
linkToPdf http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Jb5wwFH5qUynKpYu6hK6u1ENzYFhsMBzTTEfpwiiqJlXUC8Jbi9rAaMTk0B_R39xnA9OZqKccwQYD32e_9-yPZ4A31oXPaGR8yVLmM85SPw-18qmiKoxUJkOXbb-Yp6fn7ONFcrG11ZcT7UtRT5pfl5Om_uG0lctLGYw6seCsOEGbYuUcwVKZ4DbcwT4bpluBuhuEbVwURv3CJIZheWDsVIHVctkElWgHD2CfRjSyC1s7Nsml7v-fv3ldNrllh2b34Nv4Br385Odk3YmJ_H0tueONXvE-3B28U3LcV3kAt3TzEP70P_OaYXaPVI0iMzSH_Swi-Yoc3pS1hhRW4vdlfuxHKem31SALJzdHI0nsBCQOKva6aY0kxxuTQmMAQP5lWV-RiLydFovoiNQNuaq7VevadAdX7SM4n71fnJz6wzYOvkzirPNNynJpRKgR90qlMjaxkjhuCKk5xWhUxExUnGuqM2UoZ7mheZYIwQWVCQ5A9DHsNW2jD4EkWFyxTGYUmcWlybmoWCipEYmhIas8OBqBLJd9to4SoxyLf-nwLy3-pcPfg3cW6U09m2fbnWhX38sBihLBzrPKecGMqUQKnqEHjU6qyiVVJvXg9ciTEvulXWypGt2usSGMK3O3qaoHT3rebJoaeecB32HUzrPsliBPXO7vgRdPb3zlK9g_m87Kzx_mn57Bgf0cVvgW8-ew163W-gW6WJ146TrTX7NkJ-o
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=Identification+and+Functional+Verification+of+MicroRNA-16+Family+Targeting+Intestinal+Divalent+Metal+Transporter+1+%28DMT1%29+in+vitro+and+in+vivo&rft.jtitle=Frontiers+in+physiology&rft.au=Shuxia+Jiang&rft.au=Shuxia+Jiang&rft.au=Shihui+Guo&rft.au=Shihui+Guo&rft.date=2019-06-27&rft.pub=Frontiers+Media+S.A&rft.eissn=1664-042X&rft.volume=10&rft_id=info:doi/10.3389%2Ffphys.2019.00819&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_edc98a1923144d5cb78150511d9c3df6
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-042X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-042X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-042X&client=summon