Regulation of placental leptin expression by cyclic adenosine 5′-monophosphate involves cross talk between protein kinase A and mitogen-activated protein kinase signaling pathways

Endocrinology

Volumn 151, Issue 8, 2010, Pages 3738-3751

  Maymó, Julieta L ^a   Pérez, Antonio Pérez ^b   Dueñas, José L ^b   Calvo, Juan Carlos ^a,c   Sánchez Margalet, Víctor ^b   Varone, Cecilia L ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b HOSPITAL UNIVERSITARIO VIRGEN MACARENA   (Spain)

^c INST DE BIOL Y MED EXPERIMENTAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ADENYLATE CYCLASE; BUCLADESINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LEPTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME INHIBITION; EXPLANT; GENE ACTIVITY; HORMONE RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; PHYSIOLOGICAL PROCESS; PLACENTA; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; TROPHOBLAST; UPREGULATION; WESTERN BLOTTING;

EID: 77954891467     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0064     Document Type: Article

References (93)

1. Denker HW 1993 Implantation: a cell biological paradox. J Exp Zool 266:541-558
2. Aplin JD 2000 The cell biological basis of human implantation. Baillieres Best Pract Res Clin Obstet Gynaecol 14:757-764
3. Achache H, Revel A 2006 Endometrial receptivity markers, the journey to successful embryo implantation. Hum Reprod Update 12: 731-746
4. Evain-Brion D, Malassine A 2003 Human placenta as an endocrine organ. Growth Horm IGF Res 13(Suppl A):S34-S37
5. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM 1994 Positional cloning of the mouse obese gene and its human homologue. Nature 372:425-432
6. Houseknecht KL, Portocarrero CP 1998 Leptin and its receptors: regulators of whole-body energy homeostasis. Domest Anim Endocrinol 15:457-475
7. Sagawa N, Yura S, Itoh H, Mise H, Kakui K, Korita D, Takemura M, Nuamah MA, Ogawa Y, Masuzaki H, Nakao K, Fujii S 2002 Role of leptin in pregnancy-a review. Placenta 23(Suppl A):S80-S86
8. Reitman ML, Bi S, Marcus-Samuels B, Gavrilova O 2001 Leptin and its role in pregnancy and fetal development-an overview. Biochem Soc Trans 29:68-72
9. Henson MC, Castracane VD 2006 Leptin in pregnancy: an update. Biol Reprod 74:218-229
10. Cervero A, Horcajadas JA, Domínguez F, Pellicer A, Simón C 2005 Leptin system in embryo development and implantation: a protein in search of a function. Reprod Biomed Online 10:217-223
11. Goïot H, Laigneau JP, Devaud H, Sobhani I, Bado A 2005 Similarities and differences in the transcriptional regulation of the leptin gene promoter in gastric and adipose cells. FEBS Lett 579:1911-1916
12. Masuzaki H, Ogawa Y, Sagawa N, Hosoda K, Matsumoto T, Mise H, Nishimura H, Yoshimasa Y, Tanaka I, Mori T, Nakao K 1997 Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nat Med 3:1029-1033
13. Señarís R, Garcia-Caballero T, Casabiell X, Gallego R, Castro R, Considine RV, Dieguez C, Casanueva FF 1997 Synthesis of leptin in human placenta. Endocrinology 138:4501-4504
14. Coya R, Martul P, Algorta J, Aniel-Quiroga MA, Busturia MA, Señarís R 2006 Effect of leptin on the regulation of placental hormone secretion in cultured human placental cells. Gynecol Endocrinol 22:620-626 (Pubitemid 44915728)
15. Castellucci M, De Matteis R, Meisser A, Cancello R, Monsurrò V, Islami D, Sarzani R, Marzioni D, Cinti S, Bischof P 2000 Leptin modulates extracellular matrix molecules and metalloproteinases: possible implications for trophoblast invasion. Mol Hum Reprod 6:951-958
16. Magariños MP, Sánchez-Margalet V, Kotler M, Calvo JC, Varone CL 2007 Leptin promotes cell proliferation and survival of trophoblastic cells. Biol Reprod 76:203-210 (Pubitemid 46219334)
17. Pérez-Pérez A, Maymó J, Dueñas JL, Goberna R, Calvo JC, Varone C, Sánchez-Margalet V 2008 Leptin prevents apoptosis of trophoblastic cells by activation of MAPK pathway. Arch Biochem Biophys 477:390-395
18. Pérez-Pérez A, Maymó J, Gambino Y, Dueñas JL, Goberna R, Varone C, Sánchez-Margalet V 2009 Leptin stimulates protein synthesis-activating translation machinery in human trophoblastic cells. Biol Reprod 81:826-832
19. Butte NF, Hopkinson JM, Nicolson MA 1997 Leptin in human reproduction: serum leptin levels in pregnant and lactating women. J Clin Endocrinol Metab 82:585-589 (Pubitemid 27068634)
20. Caprio M, Fabbrini E, Isidori AM, Aversa A, Fabbri A 2001 Leptin in reproduction. Trends Endocrinol Metab 12:65-72
21. Bajoria R, Sooranna SR, Ward BS, Chatterjee R 2002 Prospective function of placental leptin at maternal-fetal interface. Placenta 23: 103-115 (Pubitemid 41110510)
22. Maymó JL, Pérez Pérez A, Sánchez-Margalet V, Dueñas JL, Calvo JC, Varone CL 2009 Up-regulation of placental leptin by human chorionic gonadotropin. Endocrinology 150:304-313
23. Feinman MA, Kliman HJ, Caltabiano S, Strauss 3rd JF 1986 8-Bromo-3′,5′-adenosine monophosphate stimulates the endocrine activity of human cytotrophoblasts in culture. J Clin Endocrinol Metab 63:1211-1217 (Pubitemid 17173063)
24. Slieker LJ, Sloop KW, Surface PL, Kriauciunas A, La Quier F, Manetta J, Bue-Valleskey J, Stephens TW 1996 Regulation of expression of ob mRNA and protein by glucocorticoids and cAMP. J Biol Chem 271:5301-5304 (Pubitemid 26083858)
25. Szkudelski T, Nowicka E, Szkudelska K 2005 Leptin secretion and protein kinase A activity. Physiol Res 54:79-85 (Pubitemid 40363657)
26. Coya R, Gualillo O, Pineda J, García MC, Busturia MA, Aniel-Quiroga A, Martul P, Señarís RM 2001 Effect of cyclic 3′,5′-adenosine monophosphate, glucocorticoids, and insulin on leptin messenger RNA levels and leptin secretion in cultured human trophoblast. Biol Reprod 65:814-819
27. Yura S, Sagawa N, Ogawa Y, Masuzaki H, Mise H, Matsumoto T, Ebihara K, Fujii S, Nakao K 1998 Augmentation of leptin synthesis and secretion through activation of protein kinases A and C in cultured human trophoblastic cells. J Clin Endocrinol Metab 83:3609-3614 (Pubitemid 28500898)
28. Renstrom E, Eliasson L, Rorsman P 1997 Protein kinase A-dependent and -independent stimulation of exocytosis by cAMP in mouse pancreatic B-cells. J Physiol 502(Pt 1):105-118 (Pubitemid 27322979)
29. Cass LA, Summers SA, Prendergast GV, Backer JM, Birnbaum MJ, Meinkoth JL 1999 Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol Cell Biol 19:5882-5891
30. Staples KJ, Bergmann M, Tomita K, Houslay MD, McPhee I, Barnes PJ, Giembycz MA, Newton R 2001 Adenosine 3′,5′-cyclic monophosphate (cAMP)-dependent inhibition of IL-5 from human T lymphocytes is not mediated by the cAMP-dependent protein kinase A. J Immunol 167:2074-2080
31. Strauss 3rd JF, Kido S, Sayegh R, Sakuragi N, Gåfvels ME 1992 The cAMP signalling system and human trophoblast function. Placenta 13:389-403
32. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
33. Bi S, Gavrilova O, Gong DW, Mason MM, Reitman M 1997 Identification of a placental enhancer for the human leptin gene. J Biol Chem 272:30583-30588 (Pubitemid 27512274)
34. Mellon PL, Clegg CH, Correll LA, McKnight GS 1989 Regulation of transcription by cyclic AMP-dependent protein kinase. Proc Natl Acad Sci USA 86:4887-4891 (Pubitemid 19182204)
35. Clegg CH, Abrahamsen MS, Degen JL, Morris DR, McKnight GS 1992 Cyclic AMP-dependent protein kinase controls basal gene activity and steroidogenesis in Y1 adrenal tumor cells. Biochemistry 31:3720-3726
36. Gonzalez GA, Montminy MR 1989 Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680
37. Caüzac M, Czuba D, Girard J, Hauguel-de Mouzon S 2003 Transduction of leptin growth signals in placental cells is independent of JAK-STAT activation. Placenta 24:378-384 (Pubitemid 37184757)
38. Vossler MR, Yao H, York RD, Pan MG, Rim CS, Stork PJ 1997 cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. Cell 89:73-82 (Pubitemid 27180587)
39. Grewal SS, Horgan AM, York RD, Withers GS, Banker GA, Stork PJ 2000 Neuronal calcium activates a Rap1 and B-Raf signaling pathway via the cyclic adenosine monophosphate-dependent protein kinase. J Biol Chem 275:3722-3728
40. Buscà R, Abbe P, Mantoux F, Aberdam E, Peyssonnaux C, Eychène A, Ortonne JP, Ballotti R 2000 Ras mediates the cAMP-dependent activation of extracellular signal-regulated kinases (ERKs) in melanocytes. EMBO J 19:2900-2910 (Pubitemid 30386762)
41. Sevetson BR, Kong X, Lawrence Jr JC 1993 Increasing cAMP attenuates activation of mitogen-activated protein kinase. Proc Natl Acad Sci USA 90:10305-10309 (Pubitemid 23328301)
42. Osinski MT, Schrör K 2000 Inhibition of platelet-derived growth factor-induced mitogenesis by phosphodiesterase 3 inhibitors: role of protein kinase A in vascular smooth muscle cell mitogenesis. Biochem Pharmacol 60:381-387 (Pubitemid 30336635)
43. Vitiello D, Patrizio P 2007 Implantation and early embryonic development: implications for pregnancy. Semin Perinatol 31:204-207 (Pubitemid 47348101)
44. Hardie L, Trayhurn P, Abramovich D, Fowler P 1997 Circulating leptin in women: a longitudinal study in the menstrual cycle and during pregnancy. Clin Endocrinol 47:101-106 (Pubitemid 27313995)
45. Henson MC, Swan KF, O'Neil JS 1998 Expression of placental leptin and leptin receptor transcripts in early pregnancy and at term. Obstet Gynecol 92:1020-1028 (Pubitemid 28536123)
46. Henson MC, Castracane VD 2000 Leptin in pregnancy. Biol Reprod 63:1219-1228
47. Henson MC, Castracane VD 2002 Leptin: roles and regulation in primate pregnancy. Semin Reprod Med 20:113-122
48. Henson MC, Castracane VD 2006 Leptin in pregnancy: an update. Biol Reprod 74:218-229
49. Domali E, Messinis IE 2002 Leptin in pregnancy. J Matern Fetal Neonatal Med 12:222-230
50. Hauguel-de Mouzon S, Lepercq J 2001 Placental leptin and pregnancy pathologies. Gynecol Obstet Fertil 29:534-537
51. Zygmunt M, Hahn D, Münstedt K, Bischof P, Lang U 1998 Invasion of cytotrophoblastic JEG-3 cells is stimulated by hCG in vitro. Placenta 19:587-593 (Pubitemid 28528846)
52. Standley PR, Standley CA 2002 Identification of a functional Na+/ Mg2+ exchanger in human trophoblast cells. Am J Hypertens 15: 565-570
53. Rebut-Bonneton C, Segond N, Demignon J, Porquet D, Evain-Brion D1992 Effects of calcitonin on human trophoblastic cells in culture: absence of autocrine control. Mol Cell Endocrinol 85:65-71
54. Trayhurn P, Duncan JS, Rayner DV, Hardie LJ 1996 Rapid inhibition of ob gene expression and circulating leptin levels in lean mice by the β3-adrenoceptor agonists BRL 35135A and ZD2079. Biochem Biophys Res Commun 228:605-610
55. Szkudelski T 2007 Intracellular mediators in regulation of leptin secretion from adipocytes. Physiol Res 56:503-512
56. Monjo M, Pujol E, Roca P 2005 α2- To β3-adrenoceptor switch in 3T3-L1 preadipocytes and adipocytes: modulation by testosterone, 17β-estradiol, and progesterone. Am J Physiol Endocrinol Metab 289:E145-E150
57. Popovic V, Casanueva FF 2002 Leptin, nutrition and reproduction: new insights. Hormones 1:204-217
58. Ambrosini G, Nath AK, Sierra-Honigmann MR, Flores-Riveros J 2002 Transcriptional activation of the human leptin gene in response to hypoxia. Involvement of hypoxia-inducible factor 1. J Biol Chem 277:34601-34609
59. Gong DW, Bi S, Pratley RE, Weintraub BD 1996 Genomic structure and promoter analysis of the human obese gene. J Biol Chem 271: 3971-3974
60. He Y, Chen H, Quon MJ, Reitman M 1995 The mouse obese gene. Genomic organization, promoter activity, and activation by CCAAT/ enhancer-binding protein α. J Biol Chem 270:28887-28891
61. Isse N, Ogawa Y, Tamura N, Masuzaki H, Mori K, Okazaki T, Satoh N, Shigemoto M, Yoshimasa Y, Nishi S, Hosoda K, Inazawa J, Nakao K 1995 Structural organization and chromosomal assignment of the human obese gene. J Biol Chem 270:27728-27733
62. Houge G, Vintermyr OK, Døskeland SO 1990 The expression of cAMP-dependent protein kinase subunits in primary rat hepatocyte cultures. Cyclic AMP down-regulates its own effector system by decreasing the amount of catalytic subunit and increasing the mRNAs for the inhibitory (R) subunits of cAMP-dependent protein kinase. Mol Endocrinol 4:481-488
63. Li AW, Morash B, Hollenberg AN, Ur E, Wilkinson M, Murphy PR 2001 Transcriptional regulation of the leptin gene promoter in rat GH3pituitary and C6 glioma cells. Mol Cell Endocrinol 176:57-65
64. Morash B, Johnstone J, Leopold C, Li A, Murphy P, Ur E, Wilkinson M2000 The regulation of leptin gene expression in the C6 glioblastoma cell line. Mol Cell Endocrinol 165:97-105
65. O'Neil JS, Green AE, Edwards DE, Swan KF, Gimpel T, Castracane VD, Henson MC 2001 Regulation of leptin and leptin receptor in baboon pregnancy: effects of advancing gestation and fetectomy. J Clin Endocrinol Metab 86:2518-2524
66. Ebihara K, Ogawa Y, Isse N, Mori K, Tamura N, Masuzaki H, Kohno K, Yura S, Hosoda K, Sagawa N, Nakao K 1997 Identification of the human leptin 5́-flanking sequences involved in the trophoblast-specific transcription. Biochem Biophys Res Commun 241:658-663
67. Bayatti N, Zschocke J, Behl C 2003 Brain region-specific neuro-protective action and signaling of corticotropin-releasing hormone in primary neurons. Endocrinology 144:4051-4060
68. Adler GK, Smas CM, Fiandaca M, Frim DM, Majzoub JA 1990 Regulated expression of thehumancorticotropin releasing hormone gene by cyclic AMP. Mol Cell Endocrinol 70:165-174
69. Pende M, Fisher TL, Simpson PB, Russell JT, Blenis J, Gallo V 1997 Neurotransmitter- and growth factor-induced cAMP response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ribosomal S6 kinase pathway. J Neurosci 17:1291-1301
70. Van LP 1993 Phorbolester stimulates the activity of human corticotropin-releasing hormone gene promoter via 3′,5′-cyclic adenosine monophosphate response element in transiently transfected chicken macrophages. Endocrinology 132:30-34
71. Scatena CD, Adler S 1996 Trans-acting factors dictate the species-specific placental expression of corticotropin-releasing factor genes in choriocarcinoma cell lines. Endocrinology 137:3000-3008
72. Pertseva MN, Shpakov AO 2002 Conservatism of the insulin signal system in the evolution of vertebrate and invertebrate animals. Zh Evol Biokhim Fiziol 38:430-441
73. Pertseva MN 2005 Involvement of adenylyl cyclase signaling mechanism in insulin and IGF-I coregulation of fundamental cell processes. Ann NY Acad Sci 1040:429-430
74. Lepercq J, Cauzac M, Lahlou N, Timsit J, Girard J, Auwerx J, Hauguel-de Mouzon S 1998 Overexpression of placental leptin in diabetic pregnancy: a critical role for insulin. Diabetes 47:847-850
75. Wabitsch M, Jensen PB, Blum WF, Christoffersen CT, Englaro P, Heinze E, Rascher W, Teller W, Tornqvist H, Hauner H 1996 Insulin and cortisol promote leptin production in cultured human fat cells. Diabetes 45:1435-1438
76. Bradley RL, Cheatham B 1999 Regulation of ob gene expression and leptin secretion by insulin and dexamethasone in rat adipocytes. Diabetes 48:272-278
77. Miller SG, De Vos P, Guerre-Millo M, Wong K, Hermann T, Staels B, Briggs MR, Auwerx J 1996 The adipocyte specific transcription factor C/EBPα modulates human ob gene expression. Proc Natl Acad Sci USA 93:5507-5511
78. Martinez-deMena R, Obregón MJ 2005 Insulin increases the adrenergic stimulation of 5́ deiodinase activity and mRNA expression in rat brown adipocytes; role of MAPK and PI3K. J Mol Endocrinol 34:139-151 (Pubitemid 40305556)
79. Hei YJ 1998 Recent progress in insulin signal transduction. J Pharmacol Toxicol Methods 40:123-135
80. Hoeffler JP, Meyer TE, Yun Y, Jameson JL, Habener JF 1988 Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science 242:1430-1433 (Pubitemid 19008071)
81. Mukherjee A, Park-Sarge OK, Mayo KE 1996 Gonadotropins induce rapid phosphorylation of the 3́,5́-cyclic adenosine monophosphate response element binding protein in ovarian granulosa cells. Endocrinology 137:3234-3245 (Pubitemid 26250169)
82. Chijiwa T, Mishima A, Hagiwara M, Sano M, Hayashi K, Inoue T, Naito K, Toshioka T, Hidaka H 1990 Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5- isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J Biol Chem 265:5267-5272
83. Fitzgerald JS, Busch S, Wengenmayer T, Foerster K, de la Motte T, Poehlmann TG, Markert UR 2005 Signal transduction in trophoblast invasion. Chem Immunol Allergy 88:181-199
84. Hatano N, Mori Y, Oh-hora M, Kosugi A, Fujikawa T, Nakai N, Niwa H, Miyazaki J, Hamaoka T, Ogata M 2003 Essential role for ERK2 mitogen-activated protein kinase in placental development. Genes Cells 8:847-856
85. Gerits N, Kostenko S, Shiryaev A, Johannessen M, Moens U 2008 Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell Signal 20:1592-1607
86. Houslay MD 2006 A RSK(y) relationship with promiscuous PKA. Sci STKE 2006:pe32
87. Houslay MD, Kolch W 2000 Cell-type specific integration of crosstalk between extracellular signal-regulated kinase and cAMP signaling. Mol Pharmacol 58:659-668
88. Stork PJ, Schmitt JM 2002 Crosstalk between cAMP and MAP kinase signaling in the regulation of cell proliferation. Trends Cell Biol 12:258-266 (Pubitemid 34634174)
89. Bornfeldt KE, Krebs EG 1999 Crosstalk between protein kinase A and growth factor receptor signaling pathways in arterial smooth muscle. Cell Signal 11:465-477
90. Shaywitz AJ, Greenberg ME 1999 CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861
91. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, Housman DE, Graybiel AM 1998 A family of cAMP-binding proteins that directly activate Rap1. Science 282:2275-2279 (Pubitemid 29004080)
92. Lange-Carter CA, Pleiman CM, Gardner AM, Blumer KJ, Johnson GL 1993 A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf. Science 260:315-319
93. Kolch W 2000 Meaningful relationships: the regulation of the Ras/ Raf/MEK/ERK pathway by protein interactions. Biochem J 351 (Pt 2):289-305