HIF-KDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia
The hemochorial placenta develops from the coordinated multi-lineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage remodels uterine spiral arteries, facilitating nutrient flow, failure of which is associated with pathological conditions such as preeclampsia, in...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 113; no. 46; pp. E7212 - E7221 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences
15.11.2016
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| Series | PNAS Plus |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The hemochorial placenta develops from the coordinated multi-lineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage remodels uterine spiral arteries, facilitating nutrient flow, failure of which is associated with pathological conditions such as preeclampsia, intrauterine growth restriction, and preterm birth. Hypoxia plays an instructive role in influencing trophoblast cell differentiation and regulating placental organization. Key downstream hypoxia-activated events were delineated using rat TS cells and tested in vivo, using trophoblast-specific lentiviral gene delivery and genome editing. DNA microarray analyses performed on rat TS cells exposed to ambient or low oxygen and pregnant rats exposed to ambient or hypoxic conditions showed up-regulation of genes characteristic of an invasive/vascular remodeling/inflammatory phenotype. Among the shared up-regulated genes was matrix metallopeptidase 12 (MMP12). To explore the functional importance of MMP12 in trophoblast cell-directed spiral artery remodeling, we generated an Mmp12 mutant rat model using transcription activator-like nucleases-mediated genome editing. Homozygous mutant placentation sites showed decreased hypoxia-dependent endovascular trophoblast invasion and impaired trophoblast-directed spiral artery remodeling. A link was established between hypoxia/HIF and MMP12; however, evidence did not support Mmp12 as a direct target of HIF action. Lysine demethylase 3A (KDM3A) was identified as mediator of hypoxia/HIF regulation of Mmp12. Knockdown of KDM3A in rat TS cells inhibited the expression of a subset of the hypoxia–hypoxia inducible factor (HIF)-dependent transcripts, including Mmp12, altered H3K9 methylation status, and decreased hypoxia-induced trophoblast cell invasion in vitro and in vivo. The hypoxia-HIF-KDM3A-MMP12 regulatory circuit is conserved and facilitates placental adaptations to environmental challenges. |
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| AbstractList | The hemochorial placenta is a dynamic structure endowed with responsibilities controlling the extraction of maternal resources, ensuring fetal development and preserving maternal health. A healthy placenta exhibits plasticity and can adapt to environmental challenges. Such adaptations can be executed through instructive actions on trophoblast stem cells, influencing their abilities to expand and differentiate into specialized cells that accommodate the challenge. Hypoxia, when appropriately timed, promotes invasive trophoblast-directed uterine spiral artery remodeling. Hypoxia activates hypoxia inducible factor-dependent expression of lysine demethylase 3A, modifying the histone landscape on key target genes, including matrix metallopeptidase 12, which acts to facilitate trophoblast invasion and uterine vascular remodeling. Plasticity and adaptations at the maternal–fetal interface safeguard placental development and the healthy progression of pregnancy.
The hemochorial placenta develops from the coordinated multilineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage remodels uterine spiral arteries, facilitating nutrient flow, failure of which is associated with pathological conditions such as preeclampsia, intrauterine growth restriction, and preterm birth. Hypoxia plays an instructive role in influencing trophoblast cell differentiation and regulating placental organization. Key downstream hypoxia-activated events were delineated using rat TS cells and tested in vivo, using trophoblast-specific lentiviral gene delivery and genome editing. DNA microarray analyses performed on rat TS cells exposed to ambient or low oxygen and pregnant rats exposed to ambient or hypoxic conditions showed up-regulation of genes characteristic of an invasive/vascular remodeling/inflammatory phenotype. Among the shared up-regulated genes was matrix metallopeptidase 12 (MMP12). To explore the functional importance of MMP12 in trophoblast cell-directed spiral artery remodeling, we generated an
Mmp12
mutant rat model using transcription activator-like nucleases-mediated genome editing. Homozygous mutant placentation sites showed decreased hypoxia-dependent endovascular trophoblast invasion and impaired trophoblast-directed spiral artery remodeling. A link was established between hypoxia/HIF and MMP12; however, evidence did not support
Mmp12
as a direct target of HIF action. Lysine demethylase 3A (KDM3A) was identified as mediator of hypoxia/HIF regulation of
Mmp12
. Knockdown of KDM3A in rat TS cells inhibited the expression of a subset of the hypoxia–hypoxia inducible factor (HIF)-dependent transcripts, including
Mmp12
, altered H3K9 methylation status, and decreased hypoxia-induced trophoblast cell invasion in vitro and in vivo. The hypoxia-HIF-KDM3A-MMP12 regulatory circuit is conserved and facilitates placental adaptations to environmental challenges. The hemochorial placenta develops from the coordinated multi-lineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage remodels uterine spiral arteries, facilitating nutrient flow, failure of which is associated with pathological conditions such as preeclampsia, intrauterine growth restriction, and preterm birth. Hypoxia plays an instructive role in influencing trophoblast cell differentiation and regulating placental organization. Key downstream hypoxia-activated events were delineated using rat TS cells and tested in vivo, using trophoblast-specific lentiviral gene delivery and genome editing. DNA microarray analyses performed on rat TS cells exposed to ambient or low oxygen and pregnant rats exposed to ambient or hypoxic conditions showed up-regulation of genes characteristic of an invasive/vascular remodeling/inflammatory phenotype. Among the shared up-regulated genes was matrix metallopeptidase 12 (MMP12). To explore the functional importance of MMP12 in trophoblast cell-directed spiral artery remodeling, we generated an Mmp12 mutant rat model using transcription activator-like nucleases-mediated genome editing. Homozygous mutant placentation sites showed decreased hypoxia-dependent endovascular trophoblast invasion and impaired trophoblast-directed spiral artery remodeling. A link was established between hypoxia/HIF and MMP12; however, evidence did not support Mmp12 as a direct target of HIF action. Lysine demethylase 3A (KDM3A) was identified as mediator of hypoxia/HIF regulation of Mmp12. Knockdown of KDM3A in rat TS cells inhibited the expression of a subset of the hypoxia–hypoxia inducible factor (HIF)-dependent transcripts, including Mmp12, altered H3K9 methylation status, and decreased hypoxia-induced trophoblast cell invasion in vitro and in vivo. The hypoxia-HIF-KDM3A-MMP12 regulatory circuit is conserved and facilitates placental adaptations to environmental challenges. The hemochorial placenta develops from the coordinated multilineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage remodels uterine spiral arteries, facilitating nutrient flow, failure of which is associated with pathological conditions such as preeclampsia, intrauterine growth restriction, and preterm birth. Hypoxia plays an instructive role in influencing trophoblast cell differentiation and regulating placental organization. Key downstream hypoxia-activated events were delineated using rat TS cells and tested in vivo, using trophoblast-specific lentiviral gene delivery and genome editing. DNA microarray analyses performed on rat TS cells exposed to ambient or low oxygen and pregnant rats exposed to ambient or hypoxic conditions showed up-regulation of genes characteristic of an invasive/vascular remodeling/inflammatory phenotype. Among the shared up-regulated genes was matrix metallopeptidase 12 (MMP12). To explore the functional importance of MMP12 in trophoblast cell-directed spiral artery remodeling, we generated an Mmp12 mutant rat model using transcription activator-like nucleases-mediated genome editing. Homozygous mutant placentation sites showed decreased hypoxia-dependent endovascular trophoblast invasion and impaired trophoblast-directed spiral artery remodeling. A link was established between hypoxia/HIF and MMP12; however, evidence did not support Mmp12 as a direct target of HIF action. Lysine demethylase 3A (KDM3A) was identified as mediator of hypoxia/HIF regulation of Mmp12 Knockdown of KDM3A in rat TS cells inhibited the expression of a subset of the hypoxia-hypoxia inducible factor (HIF)-dependent transcripts, including Mmp12, altered H3K9 methylation status, and decreased hypoxia-induced trophoblast cell invasion in vitro and in vivo. The hypoxia-HIF-KDM3A-MMP12 regulatory circuit is conserved and facilitates placental adaptations to environmental challenges. |
| Author | Cui, Wei Dhakal, Pramod Rosario, Gracy X. Tachibana, Makoto Scott, Regan L. Rumi, M. A. Karim Soares, Michael J. Mason, Clifford W. Chakraborty, Damayanti Renaud, Stephen J. Krieg, Adam J. |
| Author_xml | – sequence: 1 givenname: Damayanti surname: Chakraborty fullname: Chakraborty, Damayanti organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 2 givenname: Wei surname: Cui fullname: Cui, Wei organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 3 givenname: Gracy X. surname: Rosario fullname: Rosario, Gracy X. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 4 givenname: Regan L. surname: Scott fullname: Scott, Regan L. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 5 givenname: Pramod surname: Dhakal fullname: Dhakal, Pramod organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 6 givenname: Stephen J. surname: Renaud fullname: Renaud, Stephen J. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 7 givenname: Makoto surname: Tachibana fullname: Tachibana, Makoto organization: Department of Enzyme Chemistry, Institute for Enzyme Research, Tokushima University, Tokushima 770-8503, Japan – sequence: 8 givenname: M. A. Karim surname: Rumi fullname: Rumi, M. A. Karim organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 9 givenname: Clifford W. surname: Mason fullname: Mason, Clifford W. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 10 givenname: Adam J. surname: Krieg fullname: Krieg, Adam J. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 – sequence: 11 givenname: Michael J. surname: Soares fullname: Soares, Michael J. organization: Institute for Reproductive Health and Regenerative Medicine, University of Kansas Medical Center, Kansas City, KS 66160 |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27807143$$D View this record in MEDLINE/PubMed |
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| Cites_doi | 10.1016/j.ydbio.2007.12.007 10.1172/JCI6380 10.1242/dev.01923 10.1006/dbio.1997.8758 10.1093/humrep/dem303 10.1016/j.placenta.2008.12.003 10.1210/endo-118-4-1567 10.1016/j.cell.2006.03.027 10.2217/epi.15.24 10.1073/pnas.1109478108 10.1242/dev.00642 10.1101/gad.853700a 10.1128/MCB.00425-06 10.1042/BJ20081238 10.1161/CIRCRESAHA.107.164178 10.1016/S0143-4004(81)80042-2 10.1074/jbc.M110.174045 10.1126/science.282.5396.2072 10.1053/plac.2001.0738 10.1002/dvg.20518 10.1016/S0012-1606(03)00210-0 10.1016/j.devcel.2009.11.008 10.1016/S0955-0674(98)80043-4 10.1073/pnas.94.17.9102 10.1095/biolreprod.102.014977 10.1128/MCB.06643-11 10.1073/pnas.0914507107 10.1210/endo-129-6-2895 10.2353/ajpath.2010.100182 10.1073/pnas.1309561110 10.1128/MCB.00444-09 10.1016/0002-9378(93)90172-F 10.1002/wsbm.69 10.1073/pnas.93.9.3942 10.1113/jphysiol.2006.104968 10.1016/j.placenta.2011.03.013 10.1016/j.placenta.2004.02.011 10.1038/nrg3173 10.1387/ijdb.140083ms 10.1053/plac.2002.0946 10.1126/science.1239864 10.1074/jbc.M804578200 10.1016/j.placenta.2011.11.026 10.1093/molehr/gau089 10.1016/j.cellsig.2011.08.019 10.1016/j.placenta.2009.12.012 10.1016/j.cell.2010.03.015 10.1074/jbc.M901790200 10.1073/pnas.0810067106 10.1016/j.placenta.2008.09.015 10.1016/j.ydbio.2010.12.038 10.1038/ncomms8052 10.1146/annurev-cellbio-100814-125620 10.1017/CBO9780511750847.014 10.1016/j.ydbio.2014.01.015 10.1038/nrm2125 10.1093/nar/gkp425 10.1128/MCB.25.23.10479-10491.2005 10.2144/05385BM05 10.1002/bies.201400141 10.1016/j.placenta.2005.12.006 10.1182/blood-2010-10-314427 |
| ContentType | Journal Article |
| Copyright | Volumes 1–89 and 106–113, copyright as a collective work only; author(s) retains copyright to individual articles Copyright National Academy of Sciences Nov 15, 2016 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 4Present address: Department of Anatomy and Cell Biology, University of Western Ontario, London, ON, Canada N6A 3K7. Edited by R. Michael Roberts, University of Missouri–Columbia, Columbia, MO, and approved October 5, 2016 (received for review July 31, 2016) Author contributions: D.C. and M.J.S. designed research; D.C., W.C., G.X.R., R.L.S., and P.D. performed research; M.T. and C.W.M. contributed new reagents/analytic tools; D.C., S.J.R., M.A.K.R., A.J.K., and M.J.S. analyzed data; and D.C. and M.J.S. wrote the paper. 5Present address: Department of Obstetrics and Gynecology, Oregon Health & Science University, Portland, OR 97239. 2Present address: Department of Veterinary & Animal Sciences, University of Massachusetts, Amherst, MA 01003. 3Present address: Department of Biochemistry, Global Pathways Institute, Mumbai 400066, India. |
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| References | 9256442 - Proc Natl Acad Sci U S A. 1997 Aug 19;94(17 ):9102-7 12620937 - Biol Reprod. 2003 Jul;69(1):1-7 19131105 - Placenta. 2009 Apr;30(4):299-304 18713068 - Biochem J. 2008 Dec 15;416(3):387-94 18199431 - Dev Biol. 2008 Feb 15;314(2):362-75 25948511 - Nat Commun. 2015 May 07;6:7052 9851926 - Science. 1998 Dec 11;282(5396):2072-5 22284666 - Placenta. 2012 Apr;33(4):233-43 16603237 - Cell. 2006 May 5;125(3):483-95 18984585 - J Biol Chem. 2008 Dec 26;283(52):36542-52 23034156 - Biol Reprod. 2012 Dec 13;87(6):134 12744931 - Placenta. 2003 May;24(5):540-8 17905750 - Hum Reprod. 2007 Nov;22(11):2834-41 16469781 - J Physiol. 2006 Apr 1;572(Pt 1):25-30 16966370 - Mol Cell Biol. 2006 Nov;26(22):8336-46 20059947 - Dev Cell. 2009 Dec;17 (6):755-73 12900459 - Development. 2003 Sep;130(18):4439-50 17318226 - Nat Rev Mol Cell Biol. 2007 Mar;8(3):221-33 3512258 - Endocrinology. 1986 Apr;118(4):1567-82 11869088 - Placenta. 2002 Jan;23(1):3-19 25832587 - Epigenomics. 2015 Aug;7(5):791-811 8632994 - Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3942-6 17991879 - Circ Res. 2007 Dec 7;101(12):e115-23 23776237 - Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11109-14 21447827 - Blood. 2011 Jun 9;117(23):e207-17 24485853 - Dev Biol. 2014 Mar 15;387(2):131-41 15987772 - Development. 2005 Aug;132(15):3393-403 20802175 - Am J Pathol. 2010 Oct;177(4):2103-15 25449798 - Bioessays. 2015 Mar;37(3):294-304 10377170 - J Clin Invest. 1999 Jun;103(12):1641-50 15945368 - Biotechniques. 2005 May;38(5):702, 704, 706 25245255 - Mol Hum Reprod. 2015 Jan;21(1):95-104 20479220 - Proc Natl Acad Sci U S A. 2010 Jun 15;107(24):10783-90 20371345 - Cell. 2010 Apr 2;141(1):52-67 26443191 - Annu Rev Cell Dev Biol. 2015;31:523-52 11124810 - Genes Dev. 2000 Dec 15;14(24):3191-203 12885563 - Dev Biol. 2003 Aug 1;260(1):176-90 19491311 - Nucleic Acids Res. 2009 Aug;37(14):4587-602 15451190 - Placenta. 2004 Nov;25(10):763-9 8333462 - Am J Obstet Gynecol. 1993 Jul;169(1):224-9 19386601 - J Biol Chem. 2009 Jun 19;284(25):16767-75 22473383 - Nat Rev Genet. 2012 Apr 03;13(5):343-57 9818178 - Curr Opin Cell Biol. 1998 Oct;10(5):660-6 21900602 - Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16295-300 25023691 - Int J Dev Biol. 2014;58(2-4):247-59 20060584 - Placenta. 2010 Mar;31 Suppl:S93-8 20836033 - Wiley Interdiscip Rev Syst Biol Med. 2010 May-Jun;2(3):336-61 21511332 - Placenta. 2011 Jun;32(6):475-81 21924352 - Cell Signal. 2012 Jan;24(1):35-43 19255431 - Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4260-5 9398442 - Dev Biol. 1997 Nov 15;191(2):297-305 22645302 - Mol Cell Biol. 2012 Aug;32(15):3018-32 21051540 - J Biol Chem. 2011 Jan 7;286(1):450-9 16287860 - Mol Cell Biol. 2005 Dec;25(23):10479-91 19858293 - Mol Cell Biol. 2010 Jan;30(1):344-53 16490251 - Placenta. 2006 Sep-Oct;27(9-10):939-58 24009392 - Science. 2013 Sep 6;341(6150):1106-9 19444902 - Genesis. 2009 Jul;47(7):433-9 1954876 - Endocrinology. 1991 Dec;129(6):2895-906 7010344 - Placenta. 1981 Jan-Mar;2(1):71-91 19027158 - Placenta. 2009 Jan;30(1):15-24 21215265 - Dev Biol. 2011 Mar 1;351(1):110-9 16251750 - Methods Mol Med. 2006;121:295-313 Myatt L (e_1_3_4_12_2) 2006; 572 Georgiades P (e_1_3_4_1_2) 2002; 23 Lockman K (e_1_3_4_64_2) 2007; 101 Rugg-Gunn PJ (e_1_3_4_49_2) 2010; 107 Tal R (e_1_3_4_46_2) 2012; 87 Harris LK (e_1_3_4_2_2) 2010; 31 Schneider MR (e_1_3_4_55_2) 2015; 37 Maltepe E (e_1_3_4_3_2) 2015; 31 Pijnenborg R (e_1_3_4_10_2) 2010 Ain R (e_1_3_4_33_2) 2003; 260 Mole DR (e_1_3_4_37_2) 2009; 284 Solberg H (e_1_3_4_29_2) 2003; 130 Clapcote SJ (e_1_3_4_60_2) 2005; 38 Gnarra JR (e_1_3_4_19_2) 1997; 94 Beyer S (e_1_3_4_40_2) 2008; 283 Desforges M (e_1_3_4_56_2) 2015; 21 Shipley JM (e_1_3_4_35_2) 1996; 93 Cowden Dahl KD (e_1_3_4_22_2) 2005; 25 Pijnenborg R (e_1_3_4_5_2) 2006; 27 Plaks V (e_1_3_4_31_2) 2013; 110 Yamane K (e_1_3_4_51_2) 2006; 125 Founds SA (e_1_3_4_47_2) 2009; 30 Harris LK (e_1_3_4_34_2) 2007; 22 Soares MJ (e_1_3_4_11_2) 2012; 33 Xia X (e_1_3_4_38_2) 2009; 106 Zhou S (e_1_3_4_48_2) 2011; 32 Semenza GL (e_1_3_4_18_2) 2010; 2 Benita Y (e_1_3_4_36_2) 2009; 37 Schödel J (e_1_3_4_39_2) 2011; 117 Greer EL (e_1_3_4_50_2) 2012; 13 Zhou Y (e_1_3_4_16_2) 1993; 169 Kadyrov M (e_1_3_4_13_2) 2003; 24 Pollard PJ (e_1_3_4_41_2) 2008; 416 Kliman HJ (e_1_3_4_61_2) 1986; 118 Rajakumar A (e_1_3_4_45_2) 2004; 25 Tanaka S (e_1_3_4_58_2) 1998; 282 Faria TN (e_1_3_4_59_2) 1991; 129 Pijnenborg R (e_1_3_4_9_2) 1981; 2 Adelman DM (e_1_3_4_21_2) 2000; 14 Caniggia I (e_1_3_4_44_2) 1999; 103 Hancock RL (e_1_3_4_26_2) 2015; 7 Harris LK (e_1_3_4_30_2) 2010; 177 Kozak KR (e_1_3_4_20_2) 1997; 191 Kessenbrock K (e_1_3_4_28_2) 2010; 141 Rosario GX (e_1_3_4_14_2) 2008; 314 Kaufmann P (e_1_3_4_4_2) 2003; 69 Damsky CH (e_1_3_4_7_2) 1998; 10 Asanoma K (e_1_3_4_32_2) 2011; 351 Abe Y (e_1_3_4_53_2) 2015; 6 Maltepe E (e_1_3_4_23_2) 2005; 132 Ain R (e_1_3_4_57_2) 2006; 121 Mimura I (e_1_3_4_43_2) 2012; 32 Rai A (e_1_3_4_8_2) 2014; 387 Lee DS (e_1_3_4_63_2) 2009; 47 Melvin A (e_1_3_4_25_2) 2012; 24 Krieg AJ (e_1_3_4_42_2) 2010; 30 Page-McCaw A (e_1_3_4_27_2) 2007; 8 Chakraborty D (e_1_3_4_15_2) 2011; 108 Dunwoodie SL (e_1_3_4_17_2) 2009; 17 Soares MJ (e_1_3_4_6_2) 2014; 58 Kuroki S (e_1_3_4_62_2) 2013; 341 Takeda K (e_1_3_4_24_2) 2006; 26 Shakya A (e_1_3_4_52_2) 2011; 286 Harris LK (e_1_3_4_54_2) 2009; 30 |
| References_xml | – volume: 314 start-page: 362 year: 2008 ident: e_1_3_4_14_2 article-title: Maternal hypoxia activates endovascular trophoblast cell invasion publication-title: Dev Biol doi: 10.1016/j.ydbio.2007.12.007 contributor: fullname: Rosario GX – volume: 103 start-page: 1641 year: 1999 ident: e_1_3_4_44_2 article-title: Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies publication-title: J Clin Invest doi: 10.1172/JCI6380 contributor: fullname: Caniggia I – volume: 132 start-page: 3393 year: 2005 ident: e_1_3_4_23_2 article-title: Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta publication-title: Development doi: 10.1242/dev.01923 contributor: fullname: Maltepe E – volume: 191 start-page: 297 year: 1997 ident: e_1_3_4_20_2 article-title: ARNT-deficient mice and placental differentiation publication-title: Dev Biol doi: 10.1006/dbio.1997.8758 contributor: fullname: Kozak KR – volume: 22 start-page: 2834 year: 2007 ident: e_1_3_4_34_2 article-title: BeWo cells stimulate smooth muscle cell apoptosis and elastin breakdown in a model of spiral artery transformation publication-title: Hum Reprod doi: 10.1093/humrep/dem303 contributor: fullname: Harris LK – volume: 30 start-page: 299 year: 2009 ident: e_1_3_4_54_2 article-title: Adhesion molecules in human trophoblast: A review. II. extravillous trophoblast publication-title: Placenta doi: 10.1016/j.placenta.2008.12.003 contributor: fullname: Harris LK – volume: 118 start-page: 1567 year: 1986 ident: e_1_3_4_61_2 article-title: Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae publication-title: Endocrinology doi: 10.1210/endo-118-4-1567 contributor: fullname: Kliman HJ – volume: 125 start-page: 483 year: 2006 ident: e_1_3_4_51_2 article-title: JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor publication-title: Cell doi: 10.1016/j.cell.2006.03.027 contributor: fullname: Yamane K – volume: 7 start-page: 791 year: 2015 ident: e_1_3_4_26_2 article-title: Epigenetic regulation by histone demethylases in hypoxia publication-title: Epigenomics doi: 10.2217/epi.15.24 contributor: fullname: Hancock RL – volume: 108 start-page: 16295 year: 2011 ident: e_1_3_4_15_2 article-title: Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1109478108 contributor: fullname: Chakraborty D – volume: 130 start-page: 4439 year: 2003 ident: e_1_3_4_29_2 article-title: A functional overlap of plasminogen and MMPs regulates vascularization during placental development publication-title: Development doi: 10.1242/dev.00642 contributor: fullname: Solberg H – volume: 14 start-page: 3191 year: 2000 ident: e_1_3_4_21_2 article-title: Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses publication-title: Genes Dev doi: 10.1101/gad.853700a contributor: fullname: Adelman DM – volume: 26 start-page: 8336 year: 2006 ident: e_1_3_4_24_2 article-title: Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2 publication-title: Mol Cell Biol doi: 10.1128/MCB.00425-06 contributor: fullname: Takeda K – volume: 416 start-page: 387 year: 2008 ident: e_1_3_4_41_2 article-title: Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha publication-title: Biochem J doi: 10.1042/BJ20081238 contributor: fullname: Pollard PJ – volume: 101 start-page: e115 year: 2007 ident: e_1_3_4_64_2 article-title: The histone demethylase, Jmjd1a, interacts with the myocardin factors to regulate SMC differentiation marker gene expression publication-title: Circ Res doi: 10.1161/CIRCRESAHA.107.164178 contributor: fullname: Lockman K – volume: 2 start-page: 71 year: 1981 ident: e_1_3_4_9_2 article-title: Review article: Trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals publication-title: Placenta doi: 10.1016/S0143-4004(81)80042-2 contributor: fullname: Pijnenborg R – volume: 286 start-page: 450 year: 2011 ident: e_1_3_4_52_2 article-title: Oct1 is a switchable, bipotential stabilizer of repressed and inducible transcriptional states publication-title: J Biol Chem doi: 10.1074/jbc.M110.174045 contributor: fullname: Shakya A – volume: 282 start-page: 2072 year: 1998 ident: e_1_3_4_58_2 article-title: Promotion of trophoblast stem cell proliferation by FGF4 publication-title: Science doi: 10.1126/science.282.5396.2072 contributor: fullname: Tanaka S – volume: 23 start-page: 3 year: 2002 ident: e_1_3_4_1_2 article-title: Comparative developmental anatomy of the murine and human definitive placentae publication-title: Placenta doi: 10.1053/plac.2001.0738 contributor: fullname: Georgiades P – volume: 47 start-page: 433 year: 2009 ident: e_1_3_4_63_2 article-title: In vivo genetic manipulation of the rat trophoblast cell lineage using lentiviral vector delivery publication-title: Genesis doi: 10.1002/dvg.20518 contributor: fullname: Lee DS – volume: 260 start-page: 176 year: 2003 ident: e_1_3_4_33_2 article-title: Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: Novel endocrine phenotype and regulation publication-title: Dev Biol doi: 10.1016/S0012-1606(03)00210-0 contributor: fullname: Ain R – volume: 17 start-page: 755 year: 2009 ident: e_1_3_4_17_2 article-title: The role of hypoxia in development of the Mammalian embryo publication-title: Dev Cell doi: 10.1016/j.devcel.2009.11.008 contributor: fullname: Dunwoodie SL – volume: 10 start-page: 660 year: 1998 ident: e_1_3_4_7_2 article-title: Trophoblast pseudo-vasculogenesis: Faking it with endothelial adhesion receptors publication-title: Curr Opin Cell Biol doi: 10.1016/S0955-0674(98)80043-4 contributor: fullname: Damsky CH – volume: 94 start-page: 9102 year: 1997 ident: e_1_3_4_19_2 article-title: Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.94.17.9102 contributor: fullname: Gnarra JR – volume: 69 start-page: 1 year: 2003 ident: e_1_3_4_4_2 article-title: Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia publication-title: Biol Reprod doi: 10.1095/biolreprod.102.014977 contributor: fullname: Kaufmann P – volume: 32 start-page: 3018 year: 2012 ident: e_1_3_4_43_2 article-title: Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A publication-title: Mol Cell Biol doi: 10.1128/MCB.06643-11 contributor: fullname: Mimura I – volume: 107 start-page: 10783 year: 2010 ident: e_1_3_4_49_2 article-title: Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0914507107 contributor: fullname: Rugg-Gunn PJ – volume: 129 start-page: 2895 year: 1991 ident: e_1_3_4_59_2 article-title: Trophoblast cell differentiation: Establishment, characterization, and modulation of a rat trophoblast cell line expressing members of the placental prolactin family publication-title: Endocrinology doi: 10.1210/endo-129-6-2895 contributor: fullname: Faria TN – volume: 177 start-page: 2103 year: 2010 ident: e_1_3_4_30_2 article-title: Trophoblast- and vascular smooth muscle cell-derived MMP-12 mediates elastolysis during uterine spiral artery remodeling publication-title: Am J Pathol doi: 10.2353/ajpath.2010.100182 contributor: fullname: Harris LK – volume: 110 start-page: 11109 year: 2013 ident: e_1_3_4_31_2 article-title: Matrix metalloproteinase-9 deficiency phenocopies features of preeclampsia and intrauterine growth restriction publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1309561110 contributor: fullname: Plaks V – volume: 30 start-page: 344 year: 2010 ident: e_1_3_4_42_2 article-title: Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth publication-title: Mol Cell Biol doi: 10.1128/MCB.00444-09 contributor: fullname: Krieg AJ – volume: 169 start-page: 224 year: 1993 ident: e_1_3_4_16_2 article-title: Increased depth of trophoblast invasion after chronic constriction of the lower aorta in rhesus monkeys publication-title: Am J Obstet Gynecol doi: 10.1016/0002-9378(93)90172-F contributor: fullname: Zhou Y – volume: 2 start-page: 336 year: 2010 ident: e_1_3_4_18_2 article-title: Oxygen homeostasis publication-title: Wiley Interdiscip Rev Syst Biol Med doi: 10.1002/wsbm.69 contributor: fullname: Semenza GL – volume: 93 start-page: 3942 year: 1996 ident: e_1_3_4_35_2 article-title: Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.93.9.3942 contributor: fullname: Shipley JM – volume: 572 start-page: 25 year: 2006 ident: e_1_3_4_12_2 article-title: Placental adaptive responses and fetal programming publication-title: J Physiol doi: 10.1113/jphysiol.2006.104968 contributor: fullname: Myatt L – volume: 32 start-page: 475 year: 2011 ident: e_1_3_4_48_2 article-title: Oxygen levels that optimize TSC culture are identified by maximizing growth rates and minimizing stress publication-title: Placenta doi: 10.1016/j.placenta.2011.03.013 contributor: fullname: Zhou S – volume: 25 start-page: 763 year: 2004 ident: e_1_3_4_45_2 article-title: Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae publication-title: Placenta doi: 10.1016/j.placenta.2004.02.011 contributor: fullname: Rajakumar A – volume: 13 start-page: 343 year: 2012 ident: e_1_3_4_50_2 article-title: Histone methylation: A dynamic mark in health, disease and inheritance publication-title: Nat Rev Genet doi: 10.1038/nrg3173 contributor: fullname: Greer EL – volume: 58 start-page: 247 year: 2014 ident: e_1_3_4_6_2 article-title: Adaptive mechanisms controlling uterine spiral artery remodeling during the establishment of pregnancy publication-title: Int J Dev Biol doi: 10.1387/ijdb.140083ms contributor: fullname: Soares MJ – volume: 24 start-page: 540 year: 2003 ident: e_1_3_4_13_2 article-title: Pre-eclampsia and maternal anaemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast publication-title: Placenta doi: 10.1053/plac.2002.0946 contributor: fullname: Kadyrov M – volume: 341 start-page: 1106 year: 2013 ident: e_1_3_4_62_2 article-title: Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a publication-title: Science doi: 10.1126/science.1239864 contributor: fullname: Kuroki S – volume: 283 start-page: 36542 year: 2008 ident: e_1_3_4_40_2 article-title: The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF publication-title: J Biol Chem doi: 10.1074/jbc.M804578200 contributor: fullname: Beyer S – volume: 33 start-page: 233 year: 2012 ident: e_1_3_4_11_2 article-title: Rat placentation: An experimental model for investigating the hemochorial maternal-fetal interface publication-title: Placenta doi: 10.1016/j.placenta.2011.11.026 contributor: fullname: Soares MJ – volume: 21 start-page: 95 year: 2015 ident: e_1_3_4_56_2 article-title: Elastin-derived peptides stimulate trophoblast migration and invasion: A positive feedback loop to enhance spiral artery remodelling publication-title: Mol Hum Reprod doi: 10.1093/molehr/gau089 contributor: fullname: Desforges M – volume: 24 start-page: 35 year: 2012 ident: e_1_3_4_25_2 article-title: Chromatin as an oxygen sensor and active player in the hypoxia response publication-title: Cell Signal doi: 10.1016/j.cellsig.2011.08.019 contributor: fullname: Melvin A – volume: 31 start-page: S93 year: 2010 ident: e_1_3_4_2_2 article-title: Review: Trophoblast-vascular cell interactions in early pregnancy: How to remodel a vessel publication-title: Placenta doi: 10.1016/j.placenta.2009.12.012 contributor: fullname: Harris LK – volume: 141 start-page: 52 year: 2010 ident: e_1_3_4_28_2 article-title: Matrix metalloproteinases: Regulators of the tumor microenvironment publication-title: Cell doi: 10.1016/j.cell.2010.03.015 contributor: fullname: Kessenbrock K – volume: 284 start-page: 16767 year: 2009 ident: e_1_3_4_37_2 article-title: Genome-wide association of hypoxia-inducible factor (HIF)-1α and HIF-2α DNA binding with expression profiling of hypoxia-inducible transcripts publication-title: J Biol Chem doi: 10.1074/jbc.M901790200 contributor: fullname: Mole DR – volume: 106 start-page: 4260 year: 2009 ident: e_1_3_4_38_2 article-title: Integrative analysis of HIF binding and transactivation reveals its role in maintaining histone methylation homeostasis publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.0810067106 contributor: fullname: Xia X – volume: 30 start-page: 15 year: 2009 ident: e_1_3_4_47_2 article-title: Altered global gene expression in first trimester placentas of women destined to develop preeclampsia publication-title: Placenta doi: 10.1016/j.placenta.2008.09.015 contributor: fullname: Founds SA – volume: 351 start-page: 110 year: 2011 ident: e_1_3_4_32_2 article-title: FGF4-dependent stem cells derived from rat blastocysts differentiate along the trophoblast lineage publication-title: Dev Biol doi: 10.1016/j.ydbio.2010.12.038 contributor: fullname: Asanoma K – volume: 6 start-page: 7052 year: 2015 ident: e_1_3_4_53_2 article-title: JMJD1A is a signal-sensing scaffold that regulates acute chromatin dynamics via SWI/SNF association for thermogenesis publication-title: Nat Commun doi: 10.1038/ncomms8052 contributor: fullname: Abe Y – volume: 31 start-page: 523 year: 2015 ident: e_1_3_4_3_2 article-title: Placenta: The forgotten organ publication-title: Annu Rev Cell Dev Biol doi: 10.1146/annurev-cellbio-100814-125620 contributor: fullname: Maltepe E – start-page: 127 volume-title: Placental Bed Disorders: Basic Science and Its Translation to Obstetrics year: 2010 ident: e_1_3_4_10_2 doi: 10.1017/CBO9780511750847.014 contributor: fullname: Pijnenborg R – volume: 387 start-page: 131 year: 2014 ident: e_1_3_4_8_2 article-title: Development of the hemochorial maternal vascular spaces in the placenta through endothelial and vasculogenic mimicry publication-title: Dev Biol doi: 10.1016/j.ydbio.2014.01.015 contributor: fullname: Rai A – volume: 8 start-page: 221 year: 2007 ident: e_1_3_4_27_2 article-title: Matrix metalloproteinases and the regulation of tissue remodelling publication-title: Nat Rev Mol Cell Biol doi: 10.1038/nrm2125 contributor: fullname: Page-McCaw A – volume: 121 start-page: 295 year: 2006 ident: e_1_3_4_57_2 article-title: Phenotypic analysis of the rat placenta publication-title: Methods Mol Med contributor: fullname: Ain R – volume: 37 start-page: 4587 year: 2009 ident: e_1_3_4_36_2 article-title: An integrative genomics approach identifies Hypoxia Inducible Factor-1 (HIF-1)-target genes that form the core response to hypoxia publication-title: Nucleic Acids Res doi: 10.1093/nar/gkp425 contributor: fullname: Benita Y – volume: 25 start-page: 10479 year: 2005 ident: e_1_3_4_22_2 article-title: Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation publication-title: Mol Cell Biol doi: 10.1128/MCB.25.23.10479-10491.2005 contributor: fullname: Cowden Dahl KD – volume: 38 start-page: 702 year: 2005 ident: e_1_3_4_60_2 article-title: Simplex PCR assay for sex determination in mice publication-title: Biotechniques doi: 10.2144/05385BM05 contributor: fullname: Clapcote SJ – volume: 87 start-page: 134 year: 2012 ident: e_1_3_4_46_2 article-title: The role of hypoxia and hypoxia-inducible factor-1alpha in preeclampsia pathogenesis publication-title: Biol Reprod contributor: fullname: Tal R – volume: 37 start-page: 294 year: 2015 ident: e_1_3_4_55_2 article-title: E-cadherin’s role in development, tissue homeostasis and disease: Insights from mouse models: Tissue-specific inactivation of the adhesion protein E-cadherin in mice reveals its functions in health and disease publication-title: BioEssays doi: 10.1002/bies.201400141 contributor: fullname: Schneider MR – volume: 27 start-page: 939 year: 2006 ident: e_1_3_4_5_2 article-title: The uterine spiral arteries in human pregnancy: Facts and controversies publication-title: Placenta doi: 10.1016/j.placenta.2005.12.006 contributor: fullname: Pijnenborg R – volume: 117 start-page: e207 year: 2011 ident: e_1_3_4_39_2 article-title: High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq publication-title: Blood doi: 10.1182/blood-2010-10-314427 contributor: fullname: Schödel J |
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| Snippet | The hemochorial placenta develops from the coordinated multi-lineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage... The hemochorial placenta develops from the coordinated multilineage differentiation of trophoblast stem (TS) cells. An invasive trophoblast cell lineage... The hemochorial placenta is a dynamic structure endowed with responsibilities controlling the extraction of maternal resources, ensuring fetal development and... |
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| SubjectTerms | Biological Sciences Genes Genotype & phenotype Hypoxia Mutation Peptides PNAS Plus Stem cells |
| Title | HIF-KDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia |
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