Ligand-activated peroxisome proliferator activated receptor γ alters placental morphology and placental fatty acid uptake in mice

Endocrinology

Volumn 148, Issue 8, 2007, Pages 3625-3634

  Schaiff, W Timothy ^a   Knapp Jr , F F ^b   Barak, Yaacov ^c   Biron Shental, Tal ^a   Nelson, D Michael ^a   Sadovsky, Yoel ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

15 (4 IODOPHENYL)PENTADECANOIC ACID; ADIPOPHILIN; FATTY ACID; FATTY ACID DERIVATIVE; FATTY ACID TRANSPORTER; FATTY ACID TRANSPORTER PROTEIN 1; FATTY ACID TRANSPORTER PROTEIN 2; FATTY ACID TRANSPORTER PROTEIN 3; FATTY ACID TRANSPORTER PROTEIN 4; FATTY ACID TRANSPORTER PROTEIN 6; MYOCARDIAL LIPID DROPLET PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; ROSIGLITAZONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; FATTY ACID TRANSPORT; FEMALE; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTA; PREGNANCY; PRIORITY JOURNAL; RECOMMENDED DRUG DOSE; TROPHOBLAST; WILD TYPE;

ANIMALS; FATTY ACIDS; FEMALE; FETAL WEIGHT; GENOTYPE; HYPOGLYCEMIC AGENTS; IODINE RADIOISOTOPES; IODOBENZENES; LIGANDS; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; PLACENTA; PPAR GAMMA; PREGNANCY; THIAZOLIDINEDIONES;

EID: 34547121969     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-0211     Document Type: Article

References (60)

1. Haggarty P 2004 Effect of placental function on fatty acid requirements during pregnancy. Eur J Clin Nutr 58:1559-1570
2. Crawford M 2000 Placental delivery of arachidonic and docosahexaenoic acids: implications for the lipid nutrition of preterm infants. Am J Clin Nutr 71(Suppl 1):275S-284S
3. Larque E, Demmelmair H, Berger B, Hasbargen U, Koletzko B 2003 In vivo investigation of the placental transfer of (13)C-labeled fatty acids in humans. J Lipid Res 44:49-55
4. Schaiff WT, Barak Y, Sadovsky Y 2006 The pleiotropic function of PPARγ in the placenta. Mol Cell Endocrinol 249:10-15
5. Fournier T, Tsatsaris V, Handschuh K, Evain-Brion D 2007 PPARs and the placenta. Placenta 28:65-76
6. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM 1999 PPARγ is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585-595
7. Kubota N, Terauchi Y, Miki H, Tamemoto H, Yamauchi T, Komeda K, Satoh S, Nakano R, Ishii C, Sugiyama T, Eto K, Tsubamoto Y, Okuno A, Murakami K, Sekihara H, Hasegawa G, Naito M, Toyoshima Y, Tanaka S, Shiota K, Kitamura T, Fujita T, Ezaki O, Aizawa S, Nagai R, Tobe K, Kimura S, Kadowaki T 1999 PPARγ mediates high-fat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 4:597-609
8. Schaiff WT, Bildirici I, Cheong M, Chern PL, Nelson DM, Sadovsky Y 2005 Peroxisome proliferator-activated receptor-γ and retinoid X receptor signaling regulate fatty acid uptake by primary human placental trophoblasts. J Clin Endocrinol Metab 90:4267-4275
9. Bildirici I, Roh CR, Schaiff WT, Lewkowski BM, Nelson DM, Sadovsky Y 2003 The lipid droplet-associated protein adipophilin is expressed in human trophoblasts and is regulated by peroxisomal proliferator-activated receptor-γ/retinoid X receptor. J Clin Endocrinol Metab 88:6056-6062
10. Miura S, Gan JW, Brzostowski J, Parisi MJ, Schultz CJ, Londos C, Oliver B, Kimmel AR 2002 Functional conservation for lipid storage droplet association among Perilipin, ADRP, and TIP47 (PAT)-related proteins in mammals, Drosophila, and Dictyostelium. J Biol Chem 277:32253-32257
11. Shen Q, Cline GW, Shulman GI, Leibowitz MD, Davies PJ 2004 Effects of rexinoids on glucose transport and insulin-mediated signaling in skeletal muscles of diabetic (db/db) mice. J Biol Chem 279:19721-19731
12. Kast-Woelbern HR, Dana SL, Cesario RM, Sun L, de Grandpre LY, Brooks ME, Osburn DL, Reifel-Miller A, Klausing K, Leibowitz MD 2004 Rosiglitazone induction of Insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor γ and sterol regulatory element-binding protein in the regulation of adipogenesis. J Biol Chem 279:23908-23915
13. Lytle C, Tod TJ, Vo KT, Lee JW, Atkinson RD, Straus DS 2005 The peroxisome proliferator-activated receptor γ ligand rosiglitazone delays the onset of inflammatory bowel disease in mice with interleukin 10 deficiency. Inflamm Bowel Dis 11:231-243
14. Lecka-Czernik B, Ackert-Bicknell C, Adamo ML, Marmolejos V, Churchill GA, Shockley KR, Reid IR, Grey A, Rosen CJ 2007 Activation of peroxisome proliferator-activated receptor γ (PPARγ) by rosiglitazone suppresses components of the insulin-like growth factor regulatory system in vitro and in vivo. Endocrinology 148:903-911
15. Ghose R, Mulder J, von Furstenberg RJ, Thevananther S, Kuipers F, Karpen SJ 2007 Rosiglitazone attenuates suppression of RXRα-dependent gene expression in inflamed liver. J Hepatol 46:115-123
16. Baddeley AJ, Gundersen HJ, Cruz-Orive LM 1986 Estimation of surface area from vertical sections. J Microsc 142:259-276
17. Coan PM, Ferguson-Smith AC, Burton GJ 2004 Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod 70:1806-1813
18. Backhed F, Crawford PA, O'Donnell D, Gordon JI 2007 Postnatal lymphatic partitioning from the blood vasculature in the small intestine requires fasting-induced adipose factor. Proc Natl Acad Sci USA 104:606-611
19. T method. Methods 25:402-408
20. Wang X, Seed B 2003 A PCR primer bank for quantitative gene expression analysis. Nucleic Acids Res 31:e154
21. Ameen C, Edvardsson U, Ljungberg A, Asp L, Akerblad P, Tuneld A, Olofsson SO, Linden D, Oscarsson J 2005 Activation of peroxisome proliferator-activated receptor alpha increases the expression and activity of microsomal triglyceride transfer protein in the liver. J Biol Chem 280:1224-1229
22. Knapp Jr FF, Goodman MM, Callahan AP, Kirsch G 1986 Radioiodinated 15-(p-iodophenyl)-3,3-dimethylpentadecanoic acid: a useful new agent to evaluate myocardial fatty acid uptake. J Nucl Med 27:521-531
23. Goodman MM, Kirsch G, Knapp Jr FF 1984 Synthesis and evaluation of radioiodinated terminal p-iodophenyl-substituted α- and β-methyl-branched fatty acids. J Med Chem 27:390-397
24. Mokler FT, Lin Q, Luo H, McPherson DW, Beets AL, Bockisch A, Kropp J, Knapp Jr FF 1999 Dual-label studies with [125I]-3(R)/[131I]-3(S)-BMIPP show similar metabolism in rat tissues. J Nucl Med 40:1918-1927
25. Schaiff WT, Carlson MG, Smith SD, Levy R, Nelson DM, Sadovsky Y 2000 Peroxisome proliferator-activated receptor-γ modulates differentiation of human trophoblast in a ligand-specific manner. J Clin Endocrinol Metab 85:3874-3881
26. Antonson P, Schuster GU, Wang L, Rozell B, Holter E, Flodby P, Treuter E, Holmgren L, Gustafsson JA 2003 Inactivation of the nuclear receptor coactivator RAP250 in mice results in placental vascular dysfunction. Mol Cell Biol 23:1260-1268
27. Calzonetti T, Stevenson L, Rossant J 1995 A novel regulatory region is required for trophoblast-specific transcription in transgenic mice. Dev Biol 171:615-626
28. Lescisin KR, Varmuza S, Rossant J 1988 Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev 2:1639-1646
29. Guillemot F, Nagy A, Auerbach A, Rossant J, Joyner AL 1994 Essential role of Mash-2 in extraembryonic development. Nature 371:333-336
30. Tanaka M, Gertsenstein M, Rossant J, Nagy A 1997 Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev Biol 190:55-65
31. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, Pearce JJ, Barton SC, Surani MA, Ryan K, Nehls MC, Wilson V, Evans MJ 2000 Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404:95-99
32. Wu L, de Bruin A, Saavedra HI, Starovic M, Trimboli A, Yang Y, Opavska J, Wilson P, Thompson JC, Ostrowski MC, Rosol TJ, Woollett LA, Weinstein M, Cross JC, Robinson ML, Leone G 2003 Extra-embryonic function of Rb is essential for embryonic development and viability. Nature 421:942-947
33. Li Y, Lemaire P, Behringer RR 1997 Esx1, a novel X chromosome-linked homeobox gene expressed in mouse extraembryonic tissues and male germ cells. Dev Biol 188:85-95
34. Li Y, Behringer RR 1998 Esx1 is an X-chromosome-imprinted regulator of placental development and fetal growth. Nat Genet 20:309-311
35. Kip2 regulates the proper development of labyrinthine and spongiotrophoblasts. Mol Hum Reprod 6:1019-1025
36. KIP2 in the control of tissue growth and development. Genes Dev 12:3162-3167
37. Shalom-Barak T, Nicholas JM, Wang Y, Zhang X, Ong ES, Young TH, Gendler SJ, Evans RM, Barak Y 2004 Peroxisome proliferator-activated receptor γ controls Muc1 transcription in trophoblasts. Mol Cell Biol 24:10661-10669
38. Scherer PE, Bickel PE, Kotler M, Lodish HF 1998 Cloning of cell-specific secreted and surface proteins by subtractive antibody screening. Nat Biotechnol 16:581-586
39. Yamaguchi T, Matsushita S, Motojima K, Hirose F, Osumi T 2006 MLDP, a novel PAT family protein localized to lipid droplets and enriched in the heart, is regulated by peroxisome proliferator-activated receptor α. J Biol Chem 281:14232-14240
40. Wolins NE, Quaynor BK, Skinner JR, Tzekov A, Croce MA, Gropler MC, Varma V, Yao-Borengasser A, Rasouli N, Kern PA, Finck BN, Bickel PE 2006 OXPAT/PAT-1 is a PPAR-induced lipid droplet protein that promotes fatty acid utilization. Diabetes 55:3418-3428
41. Wolins NE, Brasaemle DL, Bickel PE 2006 A proposed model of fat packaging by exchangeable lipid droplet proteins. FEBS Lett 580:5484-5491
42. Dalen KT, Dahl T, Holter E, Arntsen B, Londos C, Sztalryd C, Nebb HI 2007 LSDP5 is a PAT protein specifically expressed in fatty acid oxidizing tissues. Biochim Biophys Acta 1771:210-227
43. Campbell FM, Bush PG, Veerkamp JH, Dutta-Roy AK 1998 Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta. Placenta 19:409-415
44. Dutta-Roy AK 2000 Cellular uptake of long-chain fatty acids: role of membrane-associated fatty-acid-binding/transport proteins. Cell Mol Life Sci 57:1360-1372
45. Haggarty P 2002 Placental regulation of fatty acid delivery and its effect on fetal growth-a review. Placenta 23(Suppl A):S28-S38
46. Terasawa Y, Cases SJ, Wong JS, Jamil H, Jothi S, Traber MG, Packer L, Gordon DA, Hamilton RL, Farese Jr RV 1999 Apolipoprotein B-related gene expression and ultrastructural characteristics of lipoprotein secretion in mouse yolk sac during embryonic development. J Lipid Res 40:1967-1977
47. Hainline BE, Kahlenbeck DJ, Grant J, Strauss AW 1993 Tissue specific and developmental expression of rat long-and medium-chain acyl-CoA dehydrogenases. Biochim Biophys Acta 1216:460-468
48. Gilde AJ, van der Lee KA, Willemsen PH, Chinetti G, van der Leij FR, van der Vusse GJ, Staels B, van Bilsen M 2003 Peroxisome proliferator-activated receptor (PPAR) α and PPARβ/d, but not PPARγ, modulate the expression of genes involved in cardiac lipid metabolism. Circ Res 92:518-524
49. Coburn CT, Knapp Jr FF, Febbraio M, Beets AL, Silverstein RL, Abumrad NA 2000 Defective uptake and utilization of long chain fatty acids in muscle and adipose tissues of CD36 knockout mice. J Biol Chem 275:32523-32529
50. Hajri T, Ibrahimi A, Coburn CT, Knapp Jr FF, Kurtz T, Pravenec M, Abumrad NA 2001 Defective fatty acid uptake in the spontaneously hypertensive rat is a primary determinant of altered glucose metabolism, hyperinsulinemia, and myocardial hypertrophy. J Biol Chem 276:23661-23666
51. Buhman KK, Smith SJ, Stone SJ, Repa JJ, Wong JS, Knapp Jr FF, Burri BJ, Hamilton RL, Abumrad NA, Farese Jr RV 2002 DGAT1 is not essential for intestinal triacylglycerol absorption or chylomicron synthesis. J Biol Chem 277:25474-25479
52. Klinkner DB, Lim HJ, Strawn Jr EY, Oldham KT, Sander TL 2006 An in vivo murine model of rosiglitazone use in pregnancy. Fertil Steril 86(Suppl 4):1074-1079
53. Sevillano J, Lopez-Perez IC, Herrera E, Del Pilar Ramos M, Bocos C 2005 Englitazone administration to late pregnant rats produces delayed body growth and insulin resistance in their fetuses and neonates. Biochem J 389:913-918
54. Asami-Miyagishi R, Iseki S, Usui M, Uchida K, Kubo H, Morita I 2004 Expression and function of PPARγ in rat placental development. Biochem Biophys Res Commun 315:497-501
55. Dalen KT, Schoonjans K, Ulven SM, Weedon-Fekjaer MS, Bentzen TG, Koutnikova H, Auwerx J, Nebb HI 2004 Adipose tissue expression of the lipid droplet-associating proteins S3-12 and perilipin is controlled by peroxisome proliferator-activated receptor-g. Diabetes 53:1243-1252
56. Schaffer JE, Lodish HF 1994 Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427-436
57. Milger K, Herrmann T, Becker C, Gotthardt D, Zickwolf J, Ehehalt R, Watkins PA, Stremmel W, Fullekrug J 2006 Cellular uptake of fatty acids driven by the ER-localized acyl-CoA synthetase FATP4. J Cell Sci 119:4678-4688
58. Stahl A, Hirsch DJ, Gimeno RE, Punreddy S, Ge P, Watson N, Patel S, Kotler M, Raimondi A, Tartaglia LA, Lodish HF 1999 Identification of the major intestinal fatty acid transport protein. Mol Cell 4:299-308
59. Lobo S, Wiczer BM, Smith AJ, Hall AM, Bernlohr DA 2007 Fatty acid metabolism in adipocytes: functional analysis of fatty acid transport proteins 1 and 4. J Lipid Res 48:609-620
60. Gordon DA, Jamil H 2000 Progress towards understanding the role of microsomal triglyceride transfer protein in apolipoprotein-B lipoprotein assembly. Biochim Biophys Acta 1486:72-83