Retinoid X receptor α and retinoids are key regulators in apoptosis of trophoblasts of patients with recurrent miscarriages

Journal of Molecular Endocrinology

Volumn 47, Issue 2, 2011, Pages 145-156

  Pestka, A ^a   Toth, B ^b   Kuhn, C ^a   Hofmann, S ^a   Wiest, I ^a   Wypior, G ^a   Friese, K ^a   Jeschke, U ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALITRETINOIN; PROSTAGLANDIN J2; RETINOID; RETINOID X RECEPTOR ALPHA;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CHORIOCARCINOMA; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FIRST TRIMESTER PREGNANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; PLACENTA; PREGNANCY TERMINATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENT ABORTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROPHOBLAST; WESTERN BLOTTING;

ABORTION, HABITUAL; APOPTOSIS; BLOTTING, WESTERN; CELLS, CULTURED; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; PREGNANCY; RETINOID X RECEPTOR ALPHA; RETINOIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TROPHOBLASTS;

EID: 80054802173     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-11-0002     Document Type: Article

References (50)

1. Abrahams VM, Straszewski-Chavez SL, Guller S & Mor G 2004 First trimester trophoblast cells secrete Fas ligand which induces immune cell apoptosis. Molecular Human Reproduction 10 55-63. (doi:10.1093/molehr/gah006)
2. Ahuja HS, Szanto A, Nagy L & Davies PJ 2003 The retinoid X receptor and its ligands: versatile regulators of metabolic function, cell differentiation and cell death. Journal of Biological Regulators and Homeostatic Agents 17 29-45.
3. Altucci L, Rossin A, Hirsch O, Nebbioso A, Vitoux D, Wilhelm E, Guidez F, De Simone M, Schiavone EM, Grimwade D et al. 2005 Rexinoid-triggered differentiation and tumor-selective apoptosis of acute myeloid leukemia by protein kinase A-mediated desubordination of retinoid X receptor. Cancer Research 65 8754-8765. (doi:10.1158/0008-5472.CAN-04-3569)
4. Arck P, Toth B, Pestka A & Jeschke U 2010 Nuclear receptors of the peroxisome proliferator-activated receptor (PPAR) family in gestational diabetes: from animal models to clinical trials. Biology of Reproduction 83 168-176. (doi:10.1095/biolreprod.110.083550)
5. Boudjelal M, Voorhees JJ & Fisher GJ 2002 Retinoid signaling is attenuated by proteasome-mediated degradation of retinoid receptors in human keratinocyte HaCaT cells. Experimental Cell Research 274 130-137. (doi:10.1006/excr.2001.5450)
6. Desvergne B 2007 RXR: from partnership to leadership in metabolic regulations. Vitamins and Hormones 75 1-32. (doi:10.1016/S0083- 6729(06)75001-4)
7. Desvergne B & Wahli W 1999 Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocrine Reviews 20 649-688. (doi:10.1210/er.20.5.649)
8. Duttaroy AK 2009 Transport of fatty acids across the human placenta: a review. Progress in Lipid Research 48 52-61. (doi:10.1016/j.plipres. 2008.11.001)
9. Forman BM, Tontonoz P, Chen J, Brun RP, Spiegelman BM & Evans RM 1995 15-Deoxy-delta 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR gamma. Cell 83 803-812. (doi:10.1016/0092-8674(95)90193-0)
10. Grune T, Lietz G, Palou A, Ross AC, Stahl W, Tang G, Thurnham D, Yin SA & Biesalski HK 2010 β-Carotene is an important vitamin A source for humans. Journal of Nutrition 140 2268S-2285S. (doi:10. 3945/jn.109.119024)
11. Guibourdenche J, Tarrade A, Laurendeau I, Rochette-Egly C, Chambon P, Vidaud M & Evain-Brion D 2000 Retinoids stimulate leptin synthesis and secretion in human syncytiotrophoblast. Journal of Clinical Endocrinology and Metabolism 85 2550-2555. (doi:10.1210/jc.85.7.2550)
12. Hollung K, Rise CP, Drevon CA & Reseland JE 2004 Tissue-specific regulation of leptin expression and secretion by all-trans retinoic acid. Journal of Cellular Biochemistry 92 307-315. (doi:10.1002/ jcb.20047)
13. Kalter H & Warkany J 1961 Experimental production of congenital malformations in strains of inbred mice by maternal treatment with hypervitaminosis A. American Journal of Pathology 38 1-21.
14. Kastner P, Grondona JM, Mark M, Gansmuller A, LeMeur M, Decimo D, Vonesch JL, Dolle P & Chambon P 1994 Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78 987-1003. (doi:10.1016/0092-8674(94)90274-7)
15. Kastner P, Mark M & Chambon P 1995 Nonsteroid nuclear receptors: what are genetic studies telling us about their role in real life? Cell 83 859-869. (doi:10.1016/0092-8674(95)90202-3)
16. Kauma SW, Huff TF, Hayes N & Nilkaeo A 1999 Placental Fas ligand expression is a mechanism for maternal immune tolerance to the fetus. Journal of Clinical Endocrinology and Metabolism 84 2188-2194. (doi:10.1210/jc.84.6.2188)
17. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Willson TM, Lenhard JM et al. 1997 Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. PNAS 94 4318-4323. (doi:10.1073/pnas.94.9.4318)
18. Krskova-Tybitanclova K, Macejova D, Brtko J, Baculikova M, Krizanova O, &Zorad S, 2008 Short term13-cis-retinoic acidtreatment at therapeutic doses elevates expression of leptin, GLUT4, PPARg and aP2 in rat adipose tissue. Journal of Physiology and Pharmacology 59 731-743.
19. Lammer EJ, Chen DT, Hoar RM, Agnish ND, Benke PJ, Braun JT, Curry CJ, Fernhoff PM, Grix AW Jr, Lott IT et al. 1985 Retinoic acid embryopathy. New England Journal of Medicine 313 837-841. (doi:10.1056/NEJM198510033131401)
20. Lee GS, Kochhar DM & Collins MD 2004 Retinoid-induced limb malformations. Current Pharmaceutical Design 10 2657-2699. (doi:10.2174/1381612043383728)
21. Makrigiannakis A, Zoumakis E, Kalantaridou S, Coutifaris C, Margioris AN, Coukos G, Rice KC, Gravanis A & Chrousos GP 2001 Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nature Immunology 2 1018-1024. (doi:10.1038/ni719)
22. Mangelsdorf DJ & Evans RM 1995 The RXR heterodimers and orphan receptors. Cell 83 841-850. (doi:10.1016/0092-8674(95)90200-7)
23. Mangelsdorf DJ, Borgmeyer U, Heyman RA, Zhou JY, Ong ES, Oro AE, Kakizuka A & Evans RM 1992 Characterization of three RXR genes that mediate the action of 9-cis retinoic acid. Genes and Development 6 329-344. (doi:10.1101/gad.6.3.329)
24. Mark M, Ghyselinck NB & Chambon P 2006 Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annual Review of Pharmacology and Toxicology 46 451-480. (doi:10.1146/annurev.pharmtox.46.120604.141156)
25. Mascrez B, Mark M, Krezel W, Dupe V, LeMeur M, Ghyselinck NB & Chambon P 2001 Differential contributions of AF-1 and AF-2 activities to the developmental functions of RXR alpha. Development 128 2049-2062.
26. McIntyre TM, Pontsler AV, Silva AR, St Hilaire A, Xu Y, Hinshaw JC, Zimmerman GA, Hama K, Aoki J, Arai H et al. 2003 Identification of an intracellular receptor for lysophosphatidic acid (LPA): LPA is a transcellular PPARgamma agonist. PNAS 100 131-136. (doi:10. 1073/pnas.0135855100)
27. Minas V, Jeschke U, Kalantaridou SN, Richter DU, Reimer T, Mylonas I, Friese K & Makrigiannakis A 2007 Abortion is associated with increased expression of FasL in decidual leukocytes and apoptosis of extravillous trophoblasts: a role for CRH and urocortin. Molecular Human Reproduction 13 663-673. (doi:10.1093/molehr/gam054)
28. Nawaz Z, Lonard DM, Dennis AP, Smith CL & O'Malley BW 1999 Proteasome-dependent degradation of the human estrogen receptor. PNAS 96 1858-1862. (doi:10.1073/pnas.96.5.1858)
29. Nomura Y, Nagaya T, Hayashi Y, Kambe F & Seo H 1999 9-Cis-retinoic acid decreases the level of its cognate receptor, retinoid X receptor, through acceleration of the turnover. Biochemical and Biophysical Research Communications 260 729-733. (doi:10.1006/bbrc.1999.0969)
30. Rebourcet R, Mignot TM, Robert B & Ferre F 2004 Endothelin-2 downregulation occurs in parallel with the anti-proliferative effect of dimethylsulfoxide in BeWO human choriocarcinoma cell line. Cellular and Molecular Biology 50 OL701-OL712.
31. Remmele W & Stegner HE 1987 Recommendation for uniform definition of an immunoreactive score (IRS) for immunohistochemical estrogen receptor detection (ER-ICA) in breast cancer tissue. Der Pathologe 8 138-140.
32. Ross SA, McCaffery PJ, Drager UC & De Luca LM 2000 Retinoids in embryonal development. Physiological Reviews 80 1021-1054.
33. Runic R, Lockwood CJ, Ma Y, Dipasquale B & Guller S 1996 Expression of Fas ligand by human cytotrophoblasts: implications in placentation and fetal survival. Journal of Clinical Endocrinology and Metabolism 81 3119-3122. (doi:10.1210/jc.81.8.3119)
34. Sapin V, Dolle P, Hindelang C, Kastner P & Chambon P 1997 Defects of the chorioallantoic placenta in mouse RXRalpha null fetuses. Developmental Biology 191 29-41. (doi:10.1006/dbio.1997.8687)
35. Schaiff WT, Carlson MG, Smith SD, Levy R, Nelson DM & Sadovsky Y 2000 Peroxisome proliferator-activated receptor-gamma modulates differentiation of human trophoblast in a ligand-specific manner. Journal of Clinical Endocrinology and Metabolism 85 3874-3881. (doi:10.1210/jc.85.10.3874)
36. Schopfer FJ, Lin Y, Baker PR, Cui T, Garcia-Barrio M, Zhang J, Chen K, Chen YE & Freeman BA 2005 Nitrolinoleic acid: an endogenous peroxisome proliferator-activated receptor gamma ligand. PNAS 102 2340-2345. (doi:10.1073/pnas.0408384102)
37. Singh RR, Gururaj AE, Vadlamudi RK & Kumar R 2006 9-Cis-retinoic acid up-regulates expression of transcriptional coregulator PELP1, a novel coactivator of the retinoid X receptor alpha pathway. Journal of Biological Chemistry 281 15394-15404. (doi:10.1074/ jbc.M601593200)
38. Sucov HM, Dyson E, Gumeringer CL, Price J, Chien KR & Evans RM 1994 RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes and Development 8 1007-1018. (doi:10.1101/gad.8.9.1007)
39. Szanto A, Narkar V, Shen Q, Uray IP, Davies PJ & Nagy L 2004 Retinoid X receptors: X-ploring their (patho)physiological functions. Cell Death and Differentiation 11 (Suppl 2) S126-S143. (doi:10.1038/ sj.cdd.4401533)
40. Takahashi YI, Smith JE, Winick M & Goodman DS 1975 Vitamin A deficiency and fetal growth and development in the rat. Journal of Nutrition 105 1299-1310.
41. Tarrade A, Schoonjans K, Pavan L, Auwerx J, Rochette-Egly C, Evain-Brion D & Fournier T 2001 PPARgamma/RXRalpha heterodimers control human trophoblast invasion. Journal of Clinical Endocrinology and Metabolism 86 5017-5024. (doi:10.1210/jc.86.10.5017)
42. Taschner S, Koesters C, Platzer B, Jorgl A, Ellmeier W, Benesch T & Strobl H 2007 Down-regulation of RXRalpha expression is essential for neutrophil development from granulocyte/monocyte progenitors. Blood 109 971-979. (doi:10.1182/blood-2006-04-020552)
43. Toth B, Hornung D, Scholz C, Djalali S, Friese K & Jeschke U 2007 Peroxisome proliferator-activated receptors: new players in the field of reproduction. American Journal of Reproductive Immunology 58 289-310. (doi:10.1111/j.1600-0897.2007.00514.x)
44. Toth B, Bastug M, Scholz C, Arck P, Schulze S, Kunze S, Friese K & Jeschke U 2008 Leptin and peroxisome proliferator-activated receptors: impact on normal and disturbed first trimester human pregnancy. Histology and Histopathology 23 1465-1475.
45. Uckan D, Steele A, Cherry, Wang BY, Chamizo W, Koutsonikolis A, Gilbert-Barness E & Good RA 1997 Trophoblasts express Fas ligand: a proposed mechanism for immune privilege in placenta and maternal invasion. Molecular Human Reproduction 3 655-662. (doi:10.1093/molehr/3.8.655)
46. Villarroya F, Giralt M & Iglesias R 1999 Retinoids and adipose tissues: metabolism, cell differentiation and gene expression. International Journal of Obesity and Related Metabolic Disorders 23 1-6. (doi:10.1038/ sj.ijo.0800799)
47. Wilson JG & Warkany J 1948 Malformations in the genito-urinary tract induced by maternal vitamin A deficiency in the rat. American Journal of Anatomy 83 357-407. (doi:10.1002/aja.1000830303)
48. Wilson JG & Barch S 1949 Fetal death and maldevelopment resulting from maternal vitamin A deficiency in the rat. Proceedings of the Society for Experimental Biology and Medicine 72 687-693.
49. Wilson JG, Roth CB & Warkany J 1953 An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. American Journal of Anatomy 92 189-217. (doi:10.1002/aja.1000920202)
50. Zhang XK & Pfahl M 1993 Hetero- and homodimeric receptors in thyroid hormone and vitamin A action. Receptor 3 183-191.