Hypoxia and trophoblast differentiation: A key role for PPARγ

Stem Cells and Development

Volumn 22, Issue 21, 2013, Pages 2815-2824

  Tache, Veronique ^a   Ciric, Aleksandar ^b   Moretto Zita, Matteo ^b   Li, Yingchun ^b   Peng, Julia ^b   Maltepe, Emin ^c   Milstone, David S ^d   Parast, Mana M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELLULAR PARAMETERS; CONTROLLED STUDY; ENZYME INDUCTION; HYPOXIA; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OXYGEN TENSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TROPHOBLAST; WILD TYPE;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL HYPOXIA; CELLS, CULTURED; CYCLOHEXIMIDE; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE; MICE, KNOCKOUT; PPAR GAMMA; PRE-ECLAMPSIA; PREGNANCY; PROTEIN SYNTHESIS INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS; TROPHOBLASTS;

EID: 84885712621     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0596     Document Type: Article

References (40)

1. Huppertz B, G Burton, JC Cross and JC Kingdom. (2006). Placental morphology: frommolecule tomother-a dedication to Peter Kaufmann-a review. Placenta 27 SUPPL. A:S3-S8.
2. Red-Horse K, Y Zhou, O Genbacev, A Prakobphol, R Foulk, M McMaster and SJ Fisher. (2004). Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest 114:744-754.
3. Maltepe E, AI Bakardjiev and SJ Fisher. (2010). The placenta: Transcriptional, epigenetic, and physiological integration during development. J Clin Invest 120:1016-1025.
4. Burton GJ, AW Woods, E Jauniaux and JC Kingdom. (2009). Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta 30:473-482.
5. McMaster MT, Y Zhou and SJ Fisher. (2004). Abnormal placentation and the syndrome of preeclampsia. Semin Nephrol 24:540-547.
6. Barak Y, Y Sadovsky and T Shalom-Barak. (2008). PPAR signaling in placental development and function. PPAR Res 2008:142082.
7. Barak Y, MC Nelson, ES Ong, YZ Jones, P Ruiz-Lozano, KR Chien, A Koder and RM Evans. (1999). PPARg is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585-595.
8. Kubota N, Y Terauchi, H Miki, H Tamemoto, T Yamauchi, K Komeda, S Satoh, R Nakano, C Ishii, et al. (1999). PPARg mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 4:597-609.
9. Parast MM, H Yu, A Ciric, MW Salata, V Davis and DS Milstone. (2009). PPARg regulates trophoblast proliferation and promotes labyrinthine trilineage differentiation. PLoS One 4:e8055.8.
10. Anson-Cartwright L, K Dawson, D Holmyard, SJ Fisher, RA Lazzarini and JC Cross. (2000). The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat Genet 25:311-314.
11. Schreiber J, E Riethmacher-Sonnenberg, D Riethmacher, EE Tuerk, J Enderich, MR Bosl and M Wegner. (2000). Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol Cell Biol 20:2466-2474.
12. Mohyeldin A, T Garzon-Muvdi and A Quinones-Hinojosa. (2010). Oxygen in stem cell biology: A crintical component of the stem cell niche. Cell Stem Cell 7:150-161.
13. Suda T, K Takubo and GL Semenza. (2011). Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell 9:298-310.
14. De Filippis L and D Delia. (2011). Hypoxia in the regulation of neural stem cells. Cell Mol Life Sci 68:2831-2844.
15. Das R, H Jahr, GJ van Osch and E Farrell. (2010). The role of hypoxia in bone marrow-derived mesenchymal stem cells: Considerations for regenerative medicine approaches. Tissue Eng Part B Rev 16:159-168.
16. Genbacev O, R Joslin, CH Damsky, BM Polliotti and SJ Fisher. (1996). Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest 97:540-550.
17. Genbacev O, Y Zhou, JW Ludlow and SJ Fisher. (1997). Regulation of human placental development by oxygen tension. Science 277:1669-1672.
18. Yun Z, HL Maecker, RS Johnson and AJ Giaccia. (2002). Inhibition of PPARg2 gene expression by the HIF-1- regulated gene DEC1/Stra13: A mechanism for regulation of adipogenesis by hypoxia. Dev Cell 2:331-341.
19. Adelman DM, M Gertsenstein, A Nagy, MC Simon and E Maltepe. (2000). Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 14:3191-3203.
20. Cowden Dahl KD, BH Fryer, FA Mack, V Compernolle, E Maltepe, DM Adelman, P Carmeliet and MC Simon. (2005). Hypoxia-inducible factors 1alpha and 2alpha regulate trophoblast differentiation. Mol Cell Biol 25:10479-10491.
21. Fryer BH and MC Simon. (2006). Hypoxia, HIF and the placenta. Cell Cycle 5:495-498.
22. Maltepe E, GW Krampitz, KM Okazaki, K Red-Horse, W Mak, MC Simon and SJ Fisher. (2005). Hypoxia-inducible factor-dependent histone deacetylase activity determines stem cell fate in the placenta. Development 132:3393-3403.
23. Tanaka S, T Kunath, AK Hadjantonakis, A Nagy and J Rossant. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282:2072-2075.
24. Livak KJ and TD Schmittgen. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2- DDC T method. Methods 25:402-408.
25. Minamide LS and JR Bamburg. (1990). A filter paper dyebinding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal Biochem 190:66-70.
26. Kim MS, HJ Kwon, YM Lee, JH Baek, JE Jang, SW Lee, EJ Moon, HS Kim, SK Lee, et al. (2001). Histone deacetylases induce angiogenesis by negative regulation of tumor suppressor genes. Nat Med 7:437-443.
27. Mie Lee Y, SH Kim, HS Kim, M Jin Son, H Nakajima, H Jeong Kwon and KW Kim. (2003). Inhibition of hypoxiainduced angiogenesis by FK228, a specific histone deacetylase inhibitor, via suppression of HIF-1alpha activity. Biochem Biophys Res Commun 300:241-246.
28. Van den Beucken T, M Koritzinsky and BG Wouters. (2006). Translational control of gene expression during hypoxia. Cancer Biol Ther 5:749-755.
29. Picard F, M Kurtev, N Chung, A Topark-Ngarm, T Senawong, RM de Oliveira, M Leid, MW McBurney and L Guarente. (2004). Sirt1 promotes fat mobilization in white adipocytes by repressing PPARg. Nature 429:771-776.
30. Chen B, DM Nelson and Y Sadovsky. (2006). N-Myc downregulated gene 1 modulates the response of term human trophoblasts to hypoxic injury. J Biol Chem 281:2764-2772.
31. Schubert SW, N Lamoureux, K Kilian, L Klein-Hitpass and S Hashemolhosseini. (2008). Identification of integrin-alpha4, Rb1, and syncytin A as murine placental target genes of the transcription factor GCMa/Gcm1. J Biol Chem 283:5460-5465.
32. Simmons DG, DR Natale, V Begay, M Hughes, A Leutz and JC Cross. (2008). Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth. Development 135:2083-2091.
33. Kao LC, S Caltabiano, S Wu, JF Strauss and HJ Kliman. (1988). The human villous cytotrophoblast: Interactions with extracellular matrix proteins, endocrine function, and cytoplasmic differentiation in the absence of syncytium formation. Dev Biol 130:693-702.
34. Rodie VA, A Young, F Jordan, N Sattar, IA Greer and DJ Freeman. (2005). Human placental peroxisome proliferatoractivated receptor delta and gamma expression in healthy pregnancy and in preeclampsia and intrauterine growth restriction. J Soc Gynecol Investig 12:320-329.
35. Holdsworth-Carson SJ, R Lim, A Mitton, C Whitehead, GE Rice, M Permezel and M Lappas. (2010). Peroxisome proliferator- activated receptors are altered in pathologies of the human placenta: gestational diabetes mellitus, intrauterine growth restriction and preeclampsia. Placenta 31:222-229.
36. Drewlo S, M Czikk, D Baczyk, S Lye and J Kingdom. (2011). Glial cell missing-1 mediates over-expression of tissue inhibitor of metalloproteinase-4 in severe pre-eclamptic placental villi. Hum Reprod 26:1025-1034.
37. Bainbridge SA, A Minhas, KJ Whiteley, D Qu, JG Sled, JC Kingdom and SL Adamson. (2012). Effects of reduced Gcm1 expression on trophoblast morphology, fetoplacental vascularity, and pregnancy outcomes in mice. Hypertension 59:732-739.
38. McCarthy FP, S Drewlo, FA English, J Kingdom, EJ Johns, LC Kenny and SK Walsh. (2011). Evidence implicating peroxisome proliferator-activator receptor-g in the pathogenesis of preeclampsia. Hypertension 58:882-887.
39. Fournier T, J Guibourdenche, K Handschuh, V Tsatsaris, B Rauwel, C Davrinche and D Evain-Brion. (2011). PPARg and human trophoblast differentiation. J Reprod Immunol 90:41-49.
40. Schaiff WT, FF Knapp Jr, Y Barak, T Biron-Shental, DM Nelson and Y Sadovsky. (2007). Ligand-activated peroxisome proliferator activated receptor gamma alters placental morphology and placental fatty acid uptake in mice. Endocrinology 148:3625-3634. Development