Jumonji domain containing protein 6 is decreased in human preeclamptic placentas and regulates sFLT-1 splice variant production

Biology of Reproduction

Volumn 94, Issue 3, 2016, Pages

  Palmer, Kirsten R ^a   Tong, Stephen ^a   Tuohey, Laura ^a   Cannon, Ping ^a   Ye, Louie ^a   Hannan, Natalie J ^a   Brownfoot, Fiona C ^a   Illanes, Sebastián E ^b   Kaitu'u Lino, Tu'uhevaha J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSIDAD DE LOS ANDES   (Chile)

Author keywords

Hypoxia; JMJD6; Placenta; Preeclampsia; Pregnancy; sFLT 1

Indexed keywords

JUMONJI DOMAIN CONTAINING PROTEIN 6; MESSENGER RNA; PROTEIN; SMALL INTERFERING RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 1; FLT1 PROTEIN, HUMAN; HISTONE DEMETHYLASE; ISOPROTEIN; JMJD6 PROTEIN, HUMAN; OXYGEN; SPLICING FACTOR U2AF; U2AF2 PROTEIN, HUMAN; SOLUBLE FMS LIKE TYROSINE KINASE 1;

ADULT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; FEMALE; GENE FUNCTION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROXYLATION; HYPOXIA; OXYGEN SENSING; PATHOPHYSIOLOGY; PLACENTA; PREECLAMPSIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RNA SPLICING; TROPHOBLAST; UPREGULATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PREGNANCY; ASIAN; BIRTH WEIGHT; CAUCASIAN; DIASTOLIC BLOOD PRESSURE; ETHNICITY; GESTATIONAL AGE; MATERNAL AGE; PREMATURITY; PRIMIPARA; PROTEIN PROTEIN INTERACTION; PROTEIN SPLICING; SYSTOLIC BLOOD PRESSURE;

DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; OXYGEN; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; PROTEIN ISOFORMS; SPLICING FACTOR U2AF; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

EID: 85007448643     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.115.134460     Document Type: Article

References (24)

1. World Health Report: Making Every Mother and Child Count. World Health Organization, 2005. http://www.who.int/whr/2005/en/. Accessed 29 November 2015.
2. Maynard S, Min, JY, Merchan, J, Lim, KH, Li, J, Mondal, S, Libermann, TA, Morgan, JP, Sellke, FW, Stillman, IE, Epstein, FH, Sukhatme, VP, Ananth Karumanchi S. Excess placental soluble fms-like tyrosine kinase 1 (sFlt-1) may contribute to endothelial dysfunction, hypertension, and proteinuria in pre-eclampsia. J Clin Investig 2003; 111:649-658.
3. Nevo O, Soleymanlou N, Wu Y, Xu J, Kingdom J, Many A, Zamudio S, Caniggia I. Increased expression of sFlt-1 in in vivo and in vitro models of human placental hypoxia is mediated by HIF-1. Am J Physiol Regul Integr Comp Physiol 2006; 291:R1085-R1093.
4. Kendall RL, Thomas KA. Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc Natl Acad Sci U S A 1993; 90:10705-10709.
5. He Y, Smith SK, Day KA, Clark DE, Licence DR, Charnock-Jones DS. Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol Endocrinol 1999; 13:537-545.
6. Sela S, Itin A, Natanson-Yaron S, Greenfield C, Goldman-Wohl D, Yagel Keshet EA. Novel human-specific soluble vascular endothelial growth factor receptor 1: cell type-specific splicing and implications to vascular endothelial growth factor homeostasis and preeclampsia. Circ Res 2008; 102:1566-1574.
7. Thomas CP, Andrews JI, Raikwar NS, Kelley EA, Herse F, Dechend R, Golos TG, Liu KZ. A recently evolved novel trophoblast-enriched secreted form of fms-like tyrosine kinase-1 variant is up-regulated in hypoxia and preeclampsia. J Clin Endocrinol Metab 2009; 94:2524-2530.
8. Jebbink J, Keijser R, Veenboer G, van der Post J, Ris-Stalpers C, Afink G. Expression of placental FLT1 transcript variants relates to both gestational hypertensive disease and fetal growth. Hypertension 2011; 58:70-76.
9. Boeckel JN, Guarani V, Koyanagi M, Roexe T, Lengeling A, Schermuly RT, Gellert P, Braun T, Zeiher A, Dimmeler S. Jumonji domaincontaining protein 6 (Jmjd6) is required for angiogenic sprouting and regulates splicing of VEGF-receptor 1. Proc Natl Acad Sci U S A 2011; 108:3276-3281.
10. The American College of Obstetricians and Gynecologists; Task Force on Hypertension in Pregnancy. Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists Task Force on Hypertension in Pregnancy. Obstet Gynecol 2013; 122:1122-1131.
11. Kaitu'u-Lino TJ, Tong S, Beard S, Hastie R, Tuohey L, Brownfoot F, Onda K, Hannan NJ. Characterization of protocols for primary trophoblast purification, optimized for functional investigation of sFlt-1 and soluble endoglin. Pregnancy Hypertens 2014; 4:287-295.
12. Palmer KR, Kaitu'u-Lino TJ, Hastie R, Hannan NJ, Ye L, Binder N, Cannon P, Tuohey L, Johns TG, Shub A, Tong S. Placental-specific sFLT- 1 e15a protein is increased in preeclampsia, antagonizes vascular endothelial growth factor signaling, and has antiangiogenic activity. Hypertension 2015; 66:1251-1259.
13. Rajakumar A, Cerdeira AS, Rana S, Zsengeller Z, Edmunds L, Jeyabalan A, Hubel CA, Stillman IE, Parikh SM, Karumanchi SA. Transcriptionally active syncytial aggregates in the maternal circulation may contribute to circulating soluble fms-like tyrosine kinase 1 in preeclampsia. Hypertension 2012; 59:256-264.
14. Alahari S, Post M, Caniggia I. Jumonji domain containing protein 6: a novel oxygen sensor in the human placenta. Endocrinology 2015; 156: 3012-3025.
15. Webby CJ, Wolf A, Gromak N, Dreger M, Kramer H, Kessler B, Nielsen ML, Schmitz C, Butler DS, Yates JR III, Delahunty CM, Hahn P, et al. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science 2009; 325:90-93.
16. Loenarz C, Schofield CJ. Expanding chemical biology of 2-oxoglutarate oxygenases. Nat Chem Biol 2008; 4:152-156.
17. Pollard PJ, Loenarz C, Mole DR, McDonough MA, Gleadle JM, Schofield CJ, Ratcliffe PJ. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha. Biochem J 2008; 416:387-394.
18. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y. Histone demethylation by a family of JmjC domaincontaining proteins. Nature 2006; 439:811-816.
19. Miller RK, Genbacev O, Turner MA, Aplin JD, Caniggia I, Huppertz B. Human placental explants in culture: approaches and assessments. Placenta 2005; 26:439-448.
20. Ahmad S, Ahmed A. Elevated placental soluble vascular endothelial growth factor receptor-1 inhibits angiogenesis in preeclampsia. Circ Res 2004; 95:884-891.
21. Gu Y, Lewis DF, Wang Y. Placental productions and expressions of soluble endoglin, soluble fms-like tyrosine kinase receptor-1, and placental growth factor in normal and preeclamptic pregnancies. J Clin Endocrinol Metab 2008; 93:260-266.
22. Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, Momoeda M, Kozuma S, Taketani Y. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004; 145:4838-4845.
23. Rajakumar A, Brandon HM, Daftary A, Ness R, Conrad KP. Evidence for the functional activity of hypoxia-inducible transcription factors overexpressed in preeclamptic placentae. Placenta 2004; 25:763-769.
24. Tal R, Shaish A, Barshack I, Polak-Charcon S, Afek A, Volkov A, Feldman B, Avivi C, Harats D. Effects of hypoxia-inducible factor-1a overexpression in pregnant mice. Possible implications for preeclampsia and intrauterine growth restriction. Am J Pathol 2010 177:2950-2962.