Spatiotemporal regulation of cAMP signaling controls the human trophoblast fusion

Frontiers in Pharmacology

Volumn 6, Issue SEP, 2015, Pages

  Gerbaud, Pascale ^a,b   Taskén, Kjetil ^c,d   Pidoux, Guillaume ^a,b,e  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF OSLO   (Norway)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

AKAPs; CAMP; Phosphatases; Phosphodiesterases; Placenta; Protein kinase A; Trophoblast fusion

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; CYCLIC AMP PHOSPHODIESTERASE; ISOENZYME; MESSENGER RNA; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN SERINE THREONINE KINASE;

ARTICLE; CELL FUSION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ANALYSIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; PROTEIN LOCALIZATION; PROTEIN TARGETING; REGULATORY MECHANISM; SPATIOTEMPORAL REGULATION; TROPHOBLAST; TROPHOBLAST FUSION;

EID: 85053361346     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2015.00202     Document Type: Article

References (80)

1. Baillie, G. S., Scott, J. D., and Houslay, M. D. (2005). Compartmentalisation of phosphodiesterases and protein kinase A: opposites attract. FEBS Lett. 579, 3264-3270. doi: 10.1016/j.febslet.2005.03.089
2. Benirschke, K., and Kaufmann, P. (2000). Pathology of the Human Placenta. New-York, NY: Springer-Verlag.
3. Bernatchez, R., Belkacemi, L., Rassart, E., Daoud, G., Simoneau, L., and Lafond, J. (2003). Differential expression of membrane and soluble adenylyl cyclase isoforms in cytotrophoblast cells and syncytiotrophoblasts of human placenta. Placenta 24, 648-657. doi: 10.1016/S0143-4004(03)00060-2
4. Bos, J. L. (2006). Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 31, 680-686. doi: 10.1016/j.tibs.2006.10.002
5. Burgers, P. P., Ma, Y., Margarucci, L., Mackey, M., Van Der Heyden, M. A., Ellisman, M., et al. (2012). A small novel A-kinase anchoring protein (AKAP) that localizes specifically protein kinase A-regulatory subunit I (PKA-RI) to the plasma membrane. J. Biol. Chem. 287, 43789-43797. doi: 10.1074/jbc.M112.395970
6. Carr, D. W., Stofko-Hahn, R. E., Fraser, I. D., Bishop, S. M., Acott, T. S., Brennan, R. G., et al. (1991). Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J. Biol. Chem. 266, 14188-14192.
7. Chang, C. W., Chang, G. D., and Chen, H. (2011). A novel cyclic AMP/Epac1/CaMKI signaling cascade promotes GCM1 desumoylation and placental cell fusion. Mol. Cell. Biol. 31, 3820-3831. doi: 10.1128/MCB.05582-11
8. Charrasse, S., Comunale, F., Fortier, M., Portales-Casamar, E., Debant, A., and Gauthier-Rouviere, C. (2007). M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion. Mol. Biol. Cell 18, 1734-1743. doi: 10.1091/mbc.E06-08-0766
9. Chen, C. P., Chen, L. F., Yang, S. R., Chen, C. Y., Ko, C. C., Chang, G. D., et al. (2008). Functional characterization of the human placental fusogenic membrane protein syncytin 2. Biol. Reprod. 79, 815-823. doi: 10.1095/biolreprod.108.069765
10. Chen, H., and Cheong, M. L. (2011). "Syncytins: molecular aspects," in Cell Fusions: Regulation and Control, ed. L. G. Larsson (Amsterdam: Springer), 117-137.
11. Coghlan, V. M., Perrino, B. A., Howard, M., Langeberg, L. K., Hicks, J. B., Gallatin, W. M., et al. (1995). Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267, 108-111. doi: 10.1126/science.7528941
12. Colledge, M., and Scott, J. D. (1999). AKAPs: from structure to function. Trends Cell Biol. 9, 216-221. doi: 10.1016/S0962-8924(99)01558-5
13. Conti, A., Fabbrini, F., D'agostino, P., Negri, R., Greco, D., Genesio, R., et al. (2007). Altered expression of mitochondrial and extracellular matrix genes in the heart of human fetuses with chromosome 21 trisomy. BMC Genomics 8:268. doi: 10.1186/1471-2164-8-268
14. Coutifaris, C., Kao, L., Sehdev, H., Chin, U., Babalola, G., Blaschuk, O., et al. (1991). E-cadherin expression during the differentiation of human trophoblasts. Development 113, 767-777.
15. Dahl, E., Winterhager, E., Traub, O., and Willecke, K. (1995). Expression of gap junction genes, connexin40 and connexin43, during fetal mouse development. Anat. Embryol. (Berl) 191, 267-278. doi: 10.1007/BF00187825
16. de Rooij, J., Zwartkruis, F. J., Verheijen, M. H., Cool, R. H., Nijman, S. M., Wittinghofer, A., et al. (1998). Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474-477. doi: 10.1038/24884
17. Delidaki, M., Gu, M., Hein, A., Vatish, M., and Grammatopoulos, D. K. (2011). Interplay of cAMP and MAPK pathways in hCG secretion and fusogenic gene expression in a trophoblast cell line. Mol. Cell. Endocrinol. 332, 213-220. doi: 10.1016/j.mce.2010.10.013
18. Dell'Acqua, M. L., and Scott, J. D. (1997). Protein kinase A anchoring. J. Biol. Chem. 272, 12881-12884. doi: 10.1074/jbc.272.20.12881
19. Dimitrov, D. S., Broder, C. C., Berger, E. A., and Blumenthal, R. (1993). Calcium ions are required for cell fusion mediated by the CD4-human immunodeficiency virus type 1 envelope glycoprotein interaction. J. Virol. 67, 1647-1652.
20. Diviani, D., and Scott, J. D. (2001). AKAP signaling complexes at the cytoskeleton. J. Cell Sci. 114, 1431-1437.
21. Dodge, K., and Scott, J. D. (2000). AKAP79 and the evolution of the AKAP model. FEBS Lett. 476, 58-61. doi: 10.1016/S0014-5793(00)01671-9
22. Dunk, C. E., Gellhaus, A., Drewlo, S., Baczyk, D., Potgens, A. J., Winterhager, E., et al. (2012). The molecular role of connexin 43 in human trophoblast cell fusion. Biol. Rep. 86:115. doi: 10.1095/biolreprod.111.096925
23. Eaton, B., and Contractor, S. (1993). "In vitro assessment of trophoblast receptors and placental transport mechanisms," in The Human Placenta, eds C. W. Redman, I. L. Sargent, and P. M. Starkey (London: Blackwell Scientific Publication), 471-503.
24. Feliciello, A., Gottesman, M. E., and Avvedimento, E. V. (2001). The biological functions of A-kinase anchor proteins. J. Mol. Biol. 308, 99-114. doi: 10.1006/jmbi.2001.4585
25. Ferre, F., Breuiller, M., and Cedard, L. (1975). Human placental cAMP phosphodiesterase activity kinetic properties and sensitivity to some drugs and hormones. FEBS Lett. 52, 295-299. doi: 10.1016/0014-5793(75)80829-5
26. Fraser, I. D., Tavalin, S. J., Lester, L. B., Langeberg, L. K., Westphal, A. M., Dean, R. A., et al. (1998). A novel lipid-anchored A-kinase Anchoring Protein facilitates cAMP-responsive membrane events. EMBO J. 17, 2261-2272. doi: 10.1093/emboj/17.8.2261
27. Frendo, J.-L., Cronier, L., Bertin, G., Guibourdenche, J., Vidaud, M., Evain-Brion, D., et al. (2003). Involvement of connexin 43 in human trophoblast cell fusion and differentiation. J. Cell Sci. 116, 3413-3421. doi: 10.1242/jcs.00648
28. Gerbaud, P., and Pidoux, G. (2015). Review: an overview of molecular events occurring in human trophoblast fusion. Placenta 36(Suppl. 1), S35-S42. doi: 10.1016/j.placenta.2014.12.015
29. Gloerich, M., and Bos, J. L. (2010). Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 50, 355-375. doi: 10.1146/annurev.pharmtox.010909.105714
30. Gomez-Concha, C., Flores-Herrera, O., Olvera-Sanchez, S., Espinosa-Garcia, M. T., and Martinez, F. (2011). Progesterone synthesis by human placental mitochondria is sensitive to PKA inhibition by H89. Int. J. Biochem. Cell Biol. 43, 1402-1411. doi: 10.1016/j.biocel.2011.06.005
31. Hausken, Z. E., Coghlan, V. M., and Scott, J. D. (1998). Overlay, ligand blotting, and band-shift techniques to study kinase anchoring. Methods Mol. Biol. 88, 47-64.
32. Huang, L. J., Durick, K., Weiner, J. A., Chun, J., and Taylor, S. S. (1997a). D-AKAP2, a novel protein kinase A anchoring protein with a putative RGS domain. Proc. Natl. Acad. Sci. U.S.A. 94, 11184-11189. doi: 10.1073/pnas.94.21.11184
33. Huang, L. J., Durick, K., Weiner, J. A., Chun, J., and Taylor, S. S. (1997b). Identification of a novel protein kinase A anchoring protein that binds both type I and type II regulatory subunits. J. Biol. Chem. 272, 8057-8064. doi: 10.1074/jbc.272.12.8057
34. Huppertz, B., and Kingdom, J. C. (2004). Apoptosis in the trophoblast-role of apoptosis in placental morphogenesis. J. Soc. Gynecol. Investig. 11, 353-362. doi: 10.1016/j.jsgi.2004.06.002
35. Ilvesaro, J., Vaananen, K., and Tuukkanen, J. (2000). Bone-resorbing osteoclasts contain gap-junctional connexin-43. J. Bone Miner. Res. 15, 919-926. doi: 10.1359/jbmr.2000.15.5.919
36. Kaupp, U. B., and Seifert, R. (2002). Cyclic nucleotide-gated ion channels. Physiol. Rev. 82, 769-824.
37. Kawasaki, H., Springett, G. M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M., et al. (1998). A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275-2279. doi: 10.1126/science.282.5397.2275
38. Keryer, G., Alsat, E., Taskén, K., and Evain Brion, D. (1998a). Role of cyclic AMP-dependant protein kinases in human villous cytotrophoblast differentiation. Placenta 19(Suppl. 2), S295-S314. doi: 10.1016/S0143-4004(98)80050-7
39. Keryer, G., Alsat, E., Tasken, K., and Evain-Brion, D. (1998b). Cyclic AMP-dependent protein kinases and human trophoblast cell differentiation in vitro. J. Cell Sci. 111, 995-1004.
40. Klarenbeek, J. B., Goedhart, J., Hink, M. A., Gadella, T. W., and Jalink, K. (2011). A mTurquoise-based cAMP sensor for both FLIM and ratiometric read-out has improved dynamic range. PLoS ONE 6:e19170. doi: 10.1371/journal.pone.0019170
41. Kliman, H., Nestler, J., Sermasi, E., Sanger, J., and Strauss, J. F. III. (1986). Purification, characterization, and in vitro differenciation of cytotrophoblasts from human term placentae. Endocrinology 118, 1567-1582. doi: 10.1210/endo-118-4-1567
42. Knerr, I., Schubert, S. W., Wich, C., Amann, K., Aigner, T., Vogler, T., et al. (2005). Stimulation of GCMa and syncytin via cAMP mediated PKA signaling in human trophoblastic cells under normoxic and hypoxic conditions. FEBS Lett. 579, 3991-3998. doi: 10.1016/j.febslet.2005.06.029
43. Li, H., Degenhardt, B., Tobin, D., Yao, Z. X., Tasken, K., and Papadopoulos, V. (2001). Identification, localization, and function in steroidogenesis of PAP7: a peripheral-type benzodiazepine receptor-and PKA (RIalpha)-associated protein. Mol. Endocrinol. 15, 2211-2228. doi: 10.1210/me.15.12.2211
44. Lin, J. W., Wyszynski, M., Madhavan, R., Sealock, R., Kim, J. U., and Sheng, M. (1998). Yotiao, a novel protein of neuromuscular junction and brain that interacts with specific splice variants of NMDA receptor subunit NR1. J. Neurosci. 18, 2017-2027.
45. Liu, J., Matyakhina, L., Han, Z., Sandrini, F., Bei, T., Stratakis, C. A., et al. (2003). Molecular cloning, chromosomal localization of human peripheral-type benzodiazepine receptor and PKA regulatory subunit type 1A (PRKAR1A)-associated protein PAP7, and studies in PRKAR1A mutant cells and tissues. FASEB J. 17, 1189-1191.
46. Lu, X., and Kang, Y. (2009). Cell fusion as a hidden force in tumor progression. Cancer Res. 69, 8536-8539. doi: 10.1158/0008-5472.CAN-09-2159
47. Lugnier, C. (2006). Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol. Ther. 109, 366-398. doi: 10.1016/j.pharmthera.2005.07.003
48. Lygren, B., Carlson, C. R., Santamaria, K., Lissandron, V., Mcsorley, T., Litzenberg, J., et al. (2007). AKAP complex regulates Ca2+ re-uptake into heart sarcoplasmic reticulum. EMBO Rep. 8, 1061-1067. doi: 10.1038/sj.embor.7401081
49. Matsubara, S., Tamada, T., and Saito, T. (1987). Ultracytochemical localizations of adenylate cyclase, guanylate cyclase and cyclic 3',5'-nucleotide phosphodiesterase activity on the trophoblast in the human placenta. Direct histochemical evidence. Histochemistry 87, 505-509.
50. Mbalaviele, G., Chen, H., Boyce, B. F., Mundy, G. R., and Yoneda, T. (1995). The role of cadherin in the generation of multinucleated osteoclasts from mononuclear precursors in murine marrow. J. Clin. Invest. 95, 2757-2765. doi: 10.1172/JCI117979
51. Means, C. K., Lygren, B., Langeberg, L. K., Jain, A., Dixon, R. E., Vega, A. L., et al. (2011). An entirely specific type I A-kinase anchoring protein that can sequester two molecules of protein kinase A at mitochondria. Proc. Natl. Acad. Sci. U.S.A. 108, E1227-E1235. doi: 10.1073/pnas.1107182108
52. Meuris, S., Polliotti, B., Robyn, C., and Lebrun, P. (1994). Ca2+ entry through L-Type voltage semsitive Ca2+ channels stimulates the release of human chorionic gonadotrophin and placental lactogen by placental explants. Biochim. Biophys. Acta 1220, 101-106. doi: 10.1016/0167-4889(94)90124-4
53. Midgley, A., Pierce, G., Denau, G., and Gosling, J. (1963). Morphogenesis of syncytiotrophoblast in vivo: an autoradiographic demonstration. Science 141, 350-351. doi: 10.1126/science.141.3578.349
54. Nakamura, T., and Gold, G. H. (1987). A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325, 442-444. doi: 10.1038/325442a0
55. Ogren, L., and Talamentes, F. (1994). "The placenta as an endocrine organ: polypeptides," in Physiology of Reproduction, eds E. Knobil and J. Neill (New-York, NY: Raven Press), 875-945.
56. Oren-Suissa, M., and Podbilewicz, B. (2007). Cell fusion during development. Trends Cell Biol. 17, 537-546. doi: 10.1016/j.tcb.2007.09.004
57. Pérot, P., Montgiraud, C., Lavillette, D., and Mallet, F. (2011). "A comparative portrait of retroviral fusogens and syncytins," in Cell Fusions: Regulation and Control, ed. L. I. Larsson (Amsterdam: Springer), 63-115.
58. Pidoux, G., Gerbaud, P., Dompierre, J., Lygren, B., Solstad, T., Evain-Brion, D., et al. (2014). A PKA-ezrin-connexin 43 signaling complex controls gap junction communication and thereby trophoblast cell fusion. J. Cell Sci. 127, 4172-4185. doi: 10.1242/jcs.149609
59. Pidoux, G., Gerbaud, P., Gnidehou, S., Grynberg, M., Geneau, G., Guibourdenche, J., et al. (2010). ZO-1 is involved in trophoblastic cells differentiation in human placenta. Am. J. Physiol. Cell Physiol. 298, C1517-C1526. doi: 10.1152/ajpcell.00484.2008
60. Pidoux, G., Gerbaud, P., Marpeau, O., Guibourdenche, J., Ferreira, F., Badet, J., et al. (2007a). Human placental development is impaired by abnormal human chorionic gonadotropin signaling in trisomy 21 pregnancies. Endocrinology 148, 5403-5413. doi: 10.1210/en.2007-0589
61. Pidoux, G., Gerbaud, P., Tsatsaris, V., Marpeau, O., Ferreira, F., Meduri, G., et al. (2007b). Biochemical characterization and modulation of LH/CG-receptor during human trophoblast differentiation. J. Cell. Physiol. 212, 26-35. doi: 10.1002/jcp.20995
62. Pidoux, G., and Tasken, K. (2010). Specificity and spatial dynamics of PKA signaling organized by A kinase anchoring proteins. J. Mol. Endocrinol. 44, 271-284. doi: 10.1677/JME-10-0010
63. Polito, M., Klarenbeek, J., Jalink, K., Paupardin-Tritsch, D., Vincent, P., and Castro, L. R. (2013). The NO/cGMP pathway inhibits transient cAMP signals through the activation of PDE2 in striatal neurons. Front. Cell Neurosci. 7:211. doi: 10.3389/fncel.2013.00211
64. Rote, N. S. (2005). Intercellular fusion of BeWo. Placenta 26, 686.
65. Sato, K., and Ryan, K. J. (1971). Adenyl cyclase in the human placenta. Biochim. Biophys. Acta 244, 618-624. doi: 10.1016/0304-4165(71)90079-1
66. Schillace, R. V., and Scott, J. D. (1999). Association of the type 1 protein phosphatase PP1 with the A-kinase anchoring protein AKAP220. Curr. Biol. 9, 321-324. doi: 10.1016/S0960-9822(99)80141-9
67. Scott, J. D., and Pawson, T. (2009). Cell signaling in space and time: where proteins come together and when they're apart. Science 326, 1220-1224. doi: 10.1126/science.1175668
68. Shi, Q., Lei, Z., Rao, C., and Lin, J. (1993). Novel role of human chorionic gonadotropin in differentiation of human cytotrophoblasts. Endocrinology 132, 1387-1395. doi: 10.1210/endo.132.3.7679981
69. Tasken, K., and Aandahl, E. M. (2004). Localized effects of cAMP mediated by distinct routes of protein kinase A. Physiol. Rev. 84, 137-167. doi: 10.1152/physrev.00021.2003
70. Tasken, K., Andersson, K. B., Skalhegg, B. S., Tasken, K. A., Hansson, V., Jahnsen, T., et al. (1993). Reciprocal regulation of mRNA and protein for subunits of cAMP-dependent protein kinase (RI alpha and C alpha) by cAMP in a neoplastic B cell line (Reh). J. Biol. Chem. 268, 23483-23489.
71. Tasken, K. A., Collas, P., Kemmner, W. A., Witczak, O., Conti, M., and Tasken, K. (2001). Phosphodiesterase 4D and protein kinase a type II constitute a signaling unit in the centrosomal area. J. Biol. Chem. 276, 21999-22002. doi: 10.1074/jbc.C000911200
72. Trotter, K. W., Fraser, I. D., Scott, G. K., Stutts, M. J., Scott, J. D., and Milgram, S. L. (1999). Alternative splicing regulates the subcellular localization of A-kinase anchoring protein 18 isoforms. J. Cell Biol. 147, 1481-1492. doi: 10.1083/jcb.147.7.1481
73. Ul Hussain, M. (2014). "Transcriptional regulation of the connexin gene," in Connexins: The Gap Junction Proteins, ed. M. Ul Hussain (New Delhi: Springer), 17-23.
74. Wakelam, M. (1985). The fusion of myoblasts. Biochem. J. 15, 1-12. doi: 10.1042/bj2280001
75. Walsh, D. A., Perkins, J. P., and Krebs, E. G. (1968). An adenosine 3',5'-monophosphate-dependant protein kinase from rabbit skeletal muscle. J. Biol. Chem. 243, 3763-3765.
76. Weedon-Fekjær, M. S., and Taskén, K. (2012). Spatiotemporal dynam of hCG/cAMP signaling and regulation of placental function. Placenta 33(Suppl.), S87-S91. doi: 10.1016/j.placenta.2011.11.003
77. Xiong, L. M., Lebon, T. R., and Fujita-Yamaguchi, Y. (1990). Characterization of human placental cytosolic adenosine 3',5'-monophosphate phosphodiesterase by inhibitors and insulin treatment. Endocrinology 126, 2102-2109. doi: 10.1210/endo-126-4-2102
78. Yoshie, M., Kaneyama, K., Kusama, K., Higuma, C., Nishi, H., Isaka, K., et al. (2010). Possible role of the exchange protein directly activated by cyclic AMP (Epac) in the cyclic AMP-dependent functional differentiation and syncytialization of human placental BeWo cells. Hum. Reprod. 25, 2229-2238. doi: 10.1093/humrep/deq190
79. Zaccolo, M., and Pozzan, T. (2002). Discrete microdomains with high concentration of cAMP in stimulated rat neonatal cardiac myocytes. Science 295, 1711-1715. doi: 10.1126/science.1069982
80. Zambonin Zallone, A., Teti, A., and Primavera, M. (1984). Monocytes from circulating blood fuse in vitro with purified osteoclasts in primary culture. J. Cell Sci. 66, 335-342.