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Review

PPAR-γ signaling pathway in placental development and function: A potential therapeutic target in the treatment of gestational diseases

, & , MD PhD
Pages 1049-1063 | Published online: 12 Jul 2008

Bibliography

  • Schaiff WT, Barak Y, Sadovsky Y. The pleiotropic function of PPARγ in the placenta. Mol Cell Endocrinol 2006;249:10-5
  • Froment P, Gizard F, Defever D, et al. Peroxisome proliferator-activated receptors in reproductive tissues: from gametogenesis to parturition. J Endocrinol 2006;189:199-209
  • Cross JC, Anson-Cartwright L, Scott IC. Transcription factors underlying the development and endocrine functions of the placenta. Recent Prog Horm Res 2002;57:221-34
  • Burton GJ, Jauniaux E, Charnock-Jones DS. Human early placental development: potential roles of the endometrial glands. Placenta 2007;28:S64-9
  • Nadra K, Anghel SI, Joye E, et al. Differentiation of trophoblast giant cells and their metabolic functions are dependent on peroxisome proliferator-activated receptor β/δ. Mol Cell Biol 2006;26:3266-81
  • Kingdom J, Huppertz B, Seaward G, Kaufmann P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol 2000;92:35-43
  • Tarrade A, Schoonjans K, Guibourdenche J, et al. PPARγ/RXRα heterodimers are involved in human CGβ synthesis and human trophoblast differentiation. Endocrinology 2001;142:4504-14
  • Desvergne B, Wahli W. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev 1999;20:649-88
  • Berger J, Moller DE. The mechanisms of action of PPARs. Ann Rev Med 2002;53:409-35
  • Nolte RT, Wisely GB, Westin S, et al. Ligand binding and co-activator assembly of the peroxisome proliferators activated receptor-γ. Nature 1998;395:137-43
  • Gearing KL, Gottlicher M, Teboul M, et al. Interaction of the peroxisome proliferator-activated receptor and retinoid X receptor. Proc Natl Acad Sci USA 1993;90:1440-4
  • Feige JN, Gelman L, Michalik L, et al. From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. Progr Lipid Res 2006;45:120-59
  • Feinstein DL, Spangolo A, Akar C, et al. Receptor-independent actions of PPAR thiazolidinedione agonists: is a mitochondrial function the key? Biochem Pharm 2005;70:177-88
  • Tolon RM, Castillo AI, Aranda A. Activation of the prolactin protein gene by peroxisome proliferator-activated receptor-α appears to be DNA binding-independent. J Biol Chem 1998;273:26652-61
  • Wilson TM, Brown PJ, Strenbach DD, Henke BR. The PPARs: from orphan receptors to drug discovery. J Med Chem 2000;43:527-50
  • Schopfer FJ, Lin Y, Baker PR, et al. Nitrolinoleic acid: An endogenous peroxisome proliferator-activated receptor γ ligand. Proc Natl Acad Sci USA 2005;102:2340-5
  • Lehmann JM, Moore LB, Smith-Oliver TA, et al. An antidiabetic Thiazolidinedione is a high affinity ligand for peroxisome-proliferator-activated receptor γ (PPARγ). J Biol Chem 1995;270:12953-6
  • Theocharis S, Margeli A, Kouraklis G. Peroxisome proliferator activated receptor-gamma ligands as potent antineoplastic agents. Curr Med Chem Anticancer Agents 2003;3:239-51
  • Theocharis S, Margeli A, Vielh P, Kouraklis G. Peroxisome proliferator-activated receptor-γ ligands as cell-cycle modulators. Cancer Treat Rev 2004;30:545-54
  • Giaginis C, Margeli A, Theocharis S. Peroxisome proliferator activated receptor-γ ligands as investigational modulators of angiogenesis. Expert Opin Investig Drugs 2007;16:1561-72
  • Giaginis C, Tsantili-Kakoulidou A, Theocharis S. Peroxisome proliferator activated receptor-γ ligands as bone turnover modulators. Expert Opin Investig Drugs 2007;16:195-207
  • Hamerman D. Osteoporosis and atheroslerosis: biological linkages and the emergence of dual-purpose therapies. Q J Med 2005;98:467-84
  • Tenenbaum A, Motro M, Fisman EZ. Dual and pan-peroxisome proliferator-activated receptors (PPAR) co-agonism: the bezafibrate lessons. Cardiovasc Diabetol 2005;4:14. Published online 16 September 2005, doi:10.1186/1475-2840-4-14
  • Michalik L, Desvergne B, Dreyer C, et al. PPAR expression and function during vertebrate development. Int J Dev Biol 2002;46:105-14
  • Wang Q, Fujii H, Knipp GT. Expression of PPAR and RXR isoforms in the developing rat and human term placentas. Placenta 2002;23:661-71
  • Barak Y, Nelson MC, Ong ES, et al. PPARγ is required for placental, cardiac, and adipose tissue development. Mol Cell 1999;4:585-95
  • Barak Y, Liao D, He W, et al. Effects of peroxisome proliferator-activated receptor δ on placentation, adiposity, and colorectal cancer. Proc Natl Acad Sci USA 2002;99:303-8
  • Kubota N, Terauchi Y, Miki H, et al. PPARγ mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 1999;4:597-609
  • Asami-Miyagishi R, Iseki S, Usui M, et al. Expression and function of PPARγ in rat placental development. Biochem Biophys Res Commun 2004;315:497-501
  • Schaiff WT, Knapp FF JR, Barak Y, et al. Ligand-activated peroxisome proliferator activated receptor γ alters placental morphology and placental fatty acid uptake in mice. Endocrinology 2007;148:3625-34
  • Xu Y, Cook TJ, Knipp GT. Effects of di-(2-ethylhexyl)-phthalate (DEHP) and its metabolites on fatty acid homeostasis regulating proteins in rat placental HRP-1 trophoblast cells. Toxicol Sci 2005;84:287-300
  • Shalom-Barak T, Nicholas JM, Wang Y, et al. Peroxisome proliferator-activated receptor γ controls Muc1 transcription in trophoblasts. Mol Cell Biol 2004;24:10661-9
  • Hewitt DP, Mark PJ, Waddell BJ. Placental expression of peroxisome proliferator-activated receptors in rat pregnancy and the effect of increased glucocorticoid exposure. Biol Reprod 2006;74:23-8
  • Miles JR, Farin CE, Rodriguez KF, et al. Effects of embryo culture on angiogenesis and morphometry of bovine placentas during early gestation. Biol Reprod 2005;73:663-71
  • Langdown ML, Sugden MC. Enhanced placental GLUT1 and GLUT3 expression in dexamethasone-induced fetal growth retardation. Mol Cell Endocrinol 2001;185:109-17
  • Crawford SE, Qi C, Misra P, et al. Defects of the heart, eye and megakaryocytes in peroxisome proliferator activator receptor-binding protein (PBP) null embryos implicate GATA family of transcription factors. J Biol Chem 2002;277:3585-92
  • Antonson P, Schuster GU, Wang L, et al. Inactivation of the nuclear receptor coactivator RAP250 in mice results in placental vascular dysfunction. Mol Cell Biol 2003;23:1260-8
  • Zhu Y-J, Crawford SE, Stellmach V, et al. Coactivator PRIP, the peroxisome proliferator-activated receptor-interacting protein, is a modulator of placental, cardiac, hepatic, and embryonic development. J Biol Chem 2003;278:1986-90
  • Fournier T, Handschuh K, Tsatsaris V, Evain-Brion D. Involvement of PPARγ in human trophoblast invasion. Placenta Trophoblast Res 2007;21:S76-81
  • Fournier T, Tsatsaris V, Handschuh K, Evain-Brion D. PPARs and the placenta. Placenta 2007;28:65-76
  • Schaiff WT, Carlson MG, Smith SD, et al. Peroxisome proliferator-activated receptor-γ modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab 2000;85:3874-81
  • Wang LH, Yang XY, Zhang X, et al. Transcriptional inactivation of STAT3 by PPARγ suppresses IL-6-responsive multiple myeloma cells. Immunity 2004;20:205-18
  • Waite LL, Person EC, Zhou Y, et al. Placental peroxisome proliferator-activated receptor-γ is up-regulated by pregnancy serum. J Clin Endocrinol Metab 2000;85:3808-14
  • Capparuccia L, Marzioni D, Giordano A, et al. PPARγ expression in normal human placenta, hydatidiform mole and choriocarcinoma. Mol Hum Reprod 2002;8:574-9
  • Tarrade A, Schoonjans K, Pavan L, et al. PPARγ/RXRα heterodimers control human trophoblast invasion. J Clin Endocrinol Metab 2001;86:5017-24
  • Marvin KW, Eykholt RL, Keelan JA, et al. The 15-deoxy-Δ12,14-prostaglandin J2 receptor, peroxisome proliferator activated receptor-γ (PPARγ) is expressed in human gestational tissues and is functionally active in JEG3 choriocarcinoma cells. Placenta 2000;21:436-40
  • Fournier T, Pavan L, Tarrade A, et al. The role of PPAR-γ/RXR-α heterodimers in the regulation of human trophoblast invasion. Ann NY Acad Sci 2002;973:26-30
  • Pavan L, Tarrade A, Hermouet A, et al. Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPARγ in cell invasion process. Carcinogenesis 2003;24:1325-36
  • Schaiff WT, Bildirici I, Cheong M, et al. Peroxisome proliferator-activated receptior-γ and retinoid X receptor signaling regulate fatty acid uptake by primary human placental trophoblasts. J Clin Endocrinol Metab 2005;90:4267-75
  • Schild RL, Sonnenberg-Hirche CM, Schaiff WTB, et al. The kinase p38 regulates peroxisome proliferator activated receptor-γ in human trophoblasts. Placenta 2006;27:191-9
  • Dunn-Albanese LR, Ackerman WE 4TH, Xie Y, et al. Reciprocal expression of peroxisome proliferator-activated receptor γ and cyclooxygenase-2 in human term parturition. Am J Obstet Gynecol 2004;190:809-16
  • Daoud G, Simoneau L, Masse A, et al. Expression of cFABP and PPAR in trophoblast cells: effect of PPAR ligands on linoleic acid uptake and differentiation. Biochim Biophys Acta 2005;1687:181-94
  • Schild RL, Schaiff WT, Carlson MG, et al. The activity of PPARγ in primary human trophoblasts is enhanced by oxidized lipids. J Clin Endocrinol Metab 2002;87:1105-10
  • Handschuh K, Guibourdenche J, Tsatsaris V, et al. Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor-gamma. Endocrinology 2007;148:5011-9
  • Lappas M, Rice GE. Phospholipase A2 isozymes in pregnancy and parturition. Prostaglandins Leukot Essent Fatty Acids 2004;70:87-100
  • Lappas M, Permezel M, Georgiou HM, Rice GE. Regulation of proinflammatory cytokines in human gestational tissues by peroxisome proliferator-activated receptor-γ: effect of 15-deoxy-Δ(12,14)-PGJ(2) and troglitazone. J Clin Endocrinol Metab 2002;87:4667-72
  • Xu Y, Wang Q, Cook TJ, Knipp GT. Effect of placental fatty acid metabolism and regulation by peroxisome proliferator activated receptor on pregnancy and fetal outcomes. J Pharm Sci 2007;96:2582-606
  • Lappas M, Permezel M, Rice GE. Leptin and adiponectin stimulate the release of proinflammatory cytokines and prostaglandins from human placenta and maternal adipose tissue via nuclear factor-κB, peroxisomal proliferator-activated receptor-γ and extracellularly regulated kinase 1/2. Endocrinology 2005;146:3334-42
  • Lappas M, Permezel M, Rice GE. 15-Deoxy-δ(12,14)-prostaglandin J(2) and troglitazone regulation of the release of phospholipid metabolites, inflammatory cytokines and proteases from human gestational tissues. Placenta 2006;27:1060-72
  • Lappas M, Permezel M, Holdsworth SJ, et al. Antiinflammatory effects of the cyclopentenone isoprostane 15-A(2)-IsoP in human gestational tissues. Free Radic Biol Med 2007;42:1791-6
  • Berry EB, Eykholt R, Helliwell RJ, et al. Peroxisome proliferator-activated receptor isoform expression changes in human gestational tissues with labor at term. Mol Pharmacol 2003;64:1586-90
  • Handschuh K, Guibourdenche J, Guesnon M, et al. Modulation of PAPP-A expression by PPARγ in human first trimester trophoblast. Placenta 2006;27:S127-34
  • Lain KY, Catalano PM. Metabolic changes in pregnancy. Clin Obstet Gynecol 2007;50:938-48
  • Barnes-Powell LL. Infants of diabetic mothers: the effects of hyperglycemia on the fetus and neonate. Neonatal Netw 2007;26:283-90
  • Jawerbaum A, Capobianco E, Pustovrh C, et al. Influence of peroxisome proliferator-activated receptor γ activation by its endogenous ligand 15-deoxy δ12,14 prostaglandin J2 on nitric oxide production in term placental tissues from diabetic women. Mol Hum Reprod 2004;10:671-6
  • Meirhaeghe A, Amouyel P. Impact of genetic variation of PPARγ in humans. Mol Genet Metabol 2004;83:93-102
  • Meirhaeghe A, Boreham CA, Murray LJ, et al. A possible role for the PPARG Pro12Ala polymorphism in preterm birth. Diabetes 2007;56:494-8
  • Deeb SS, Fajas L, Nemoto M, et al. A Pro12Ala substitution in PPAR2 associated with decreased receptor activity, lower body mass index and improved insulin sensitivity. Nat Genet 1998;20:159-61
  • Suwaki N, Masuyama H, Masumoto A, et al. Expression and potential role of peroxisome proliferator-activated receptor γ in the placenta of diabetic pregnancy. Placenta 2007;28:315-23
  • Capobianco E, Jawerbaum A, Romanini MC, et al. 15-Deoxy-Δ12,14-prostaglandin J2 and peroxisome proliferator-activated receptor γ (PPARγ) levels in term placental tissues from control and diabetic rats: modulatory effects of a PPARγ agonist on nitridergic and lipid placental metabolism. Reprod Fertil Dev 2005;17:423-33
  • Holmes HJ, Casey BM, Bawdon RE. Placental transfer of rosiglitazone in the ex vivo human perfusion model. Am J Obstet Gynecol 2006;195:1715-9
  • Chan LY, Yeung JH, Lau TK. Placental transfer of rosiglitazone in the first trimester of human pregnancy. Fertil Steril 2005;83:955-8
  • Yaris F, Yaris E, Kadioglu M, et al. Normal pregnancy outcome following inadvertent exposure to rosiglitazone, gliclazide, and atorvastatin in a diabetic and hypertensive woman. Reprod Toxicol 2004;18:619-21
  • Kalyoncu NI, Yaris F, Ulku C, et al. A case of rosiglitazone exposure in the second trimester of pregnancy. Reprod Toxicol 2005;19:563-4
  • Cho H, Tai HH. Inhibition of NAD+-dependent 15-hydroxyprostaglandin dehydrogenase (15-PGDH) by cyclooxygenase inhibitors and chemopreventive agents. Prostaglandins Leukot Essent Fatty Acids 2002;67:461-5
  • Rodie VA, Young A, Jordan F, et al. Human placental peroxisome proliferator-activated receptor δ and γ expression in healthy pregnancy and in preeclampsia and intrauterine growth restriction. J Soc Gynecol Investig 2005;12:320-9
  • Waite LL, Louie RE, Taylor RN. Circulating activators of peroxisome proliferator-activated receptors are reduced in preeclamptic pregnancy. J Clin Endocrinol Metab 2005;90:620-6
  • Toth B, Hornung D, Scholz C, et al. Peroxisome proliferator-activated receptors: New players in the field of reproduction. Am J Reprod Immunol 2007;58:289-310
  • Giordano FJ, Johnson RS. Angiogenesis: the role of the microenvironment in flipping the switch. Curr Opin Genet Dev 2001;11:35-40
  • Hickey MM, Simon MC. Regulation of angiogenesis by hypoxia and hypoxia-inducible factors. Curr Top Dev Biol 2006;76:217-57
  • Liao D, Johnson RS. Hypoxia: a ket regulator of angiogenesis in cancer. Cancer Met Rev 2007;26:281-90
  • Jensen RL, Ragel BT, Whang K, Gillespie D. Inhibition of hypoxia inducible factor-1α (HIF-1-α) decrease vascular endothelial growth factor (VEGF) secretion and tumor growth in malignant gliomas. J Neurooncol 2006;78:233-47
  • Morris JM, Gopaul NK, Endresen MJ, et al. Circulating markers of oxidative stress are raised in normal pregnancy and pre-eclampsia. Br J Obstet Gynaecol 1998;105:1195-9
  • Li R, Chase M, Jung SK, et al. Hypoxic stress in diabetic pregnancy contributes to impaired embryo gene expression and defective development by inducing oxidative stress. Am J Physiol Endocrinol Metab 2005;289:E591-9
  • Rosario GX, Konno T, Soares MJ. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 2008;314:362-75
  • Alsat E, Wyplosz P, Malassine A, et al. Hypoxia impairs cell fusion and differentiation process in human cytotrophoblast, in vitro. J Cell Physiol 1996;168:346-53
  • Jiang B, Kamat A, Mendelson CR. Hypoxia prevents induction of aromatase expression in human trophoblast cells in culture: potential inhibitory role of the hypoxia-inducible transcription factor Mash-2 (mammalian achaete-scute homologous protein-2). Mol Endocrinol 2000;14:1661-73
  • Jiang B, Mendelson CR. USF1 and USF2 mediate inhibition of human trophoblast differentiation and CYP19 gene expression by Mash-2 and hypoxia. Mol Cell Biol 2003;23:6117-28
  • Nisbet RE, Sutliff RL, Hartl CM. The role of peroxisome proliferator-activated receptors in pulmonary vascular diseases. PPAR Res 2007;2007:18797. Published online 30 April 2007, doi:10.1155/2007/18797
  • Crossno JT Jr, Garat CV, Reusch JE, et al. Rosiglitazone attenuates hypoxia-induced pulmonary arterial remodeling. Am J Physiol Lung Cell Mol Physiol 2007;292:L885-97
  • Diamond MP, Saed G. Modulation of the expression of peroxisome proliferators-activated receptors in human fibroblasts. Fertil Steril 2007;87:706-9
  • Li X, Kimura H, Hirota K, et al. Hypoxia reduces the expression and anti-inflammatory effects of peroxisome proliferator-activated receptor-γ in human proximal renal tubular cells. Nephrol Dial Transplant 2007;22:1041-51
  • Kim EH, Surh YJ. 15-deoxy-Δ12,14-prostaglandin J2 as a potential endogenous regulator of redox-sensitive transcription factors. Biochem Pharmacol 2006;72:1516-28
  • Lee KS, Kim SR, Park SJ, et al. Peroxisome proliferator activated receptor-γ modulates reactive oxygen species generation and activation of nuclear factor-κB and hypoxia-inducible factor 1α in allergic airway disease of mice. J Allergy Clin Immunol 2006;118:120-7
  • Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. Regulation of human-placental development by oxygen tension. Science 1997;277:1669-72
  • Desmarais JA, Lopes FL, Zhang H, et al. The peroxisome proliferator-activated receptor gamma regulates trophoblast cell differentiation in mink (Mustela vison). Biol Reprod 2007;77:829-39
  • Elchalal U, Humphrey RG, Smith SD, et al. Troglitazone attenuates hypoxia-induced injury in cultured term human trophoblasts. Am J Obstet Gynecol 2004;191:2154-9
  • Vähäkangas K, Myllynen P. Experimental methods to study human transplacental exposure to genotoxic agents. Mutat Res 2006;608:129-35
  • Myllynen P, Pasanen M, Pelkonen O. Human placenta: a human organ for developmental toxicology research and biomonitoring. Placenta 2005;26:361-71
  • Myren M, Mose T, Mathiensen L, Knudsen LE. The human placenta-An alternative for studying foetal exposure. Toxicol In vitro 2007;21:1332-40
  • Feig DS, Briggs GG, Koren G. Oral antidiabetic agents in pregnancy and lactation: a paradigm shift? Ann Pharmacother 2007;41:1174-80
  • Wieser F, Waite L, Depoix C, Taylor RN. PPAR action in human placental development and pregnancy and its complications. PPAR Res 2008;2008:527048
  • Martinez N, Capobianco E, White V, et al. PPARα activation regulates lipid metabolism in the feto-placental unit from diabetic rats. Reproduction 2008; In press. Published online 16 April 2008, doi:10.1530/REP-08-0028
  • Wang H, Xie H, Sun X, et al. Stage-specific integration of maternal and embryonic peroxisome proliferator-activated receptor δ signaling is critical to pregnancy success. J Biol Chem 2007;282:37770-82

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