Role of Epac and protein kinase A in thyrotropin-induced gene expression in primary thyrocytes

Experimental Cell Research

Volumn 318, Issue 5, 2012, Pages 444-452

  van Staveren, Wilma C G ^a   Beeckman, Sandrine ^a   Tomás, Gil ^a   Dom, Geneviève ^a   Hébrant, Aline ^a   Delys, Laurent ^a   Vliem, Marjolein J ^b   Trésallet, Christophe ^c   Andry, Guy ^d   Franc, Brigitte ^e   Libert, Frédérick ^a   Dumont, Jacques E ^a   Maenhaut, Carine ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d JULES BORDET INSTITUTE   (Belgium)

^e LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

Author keywords

Cancer; Epac; Microarrays; Rap; RapGAP; Thyroid

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DERIVATIVE; FORSKOLIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; MESSENGER RNA; PROTEIN SERINE THREONINE KINASE; RAP PROTEIN; THYROTROPIN;

ARTICLE; CARCINOGENESIS; CELL CULTURE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROARRAY ANALYSIS; PRIORITY JOURNAL; THYROID CANCER; THYROID CELL;

EID: 84857052586     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.12.022     Document Type: Article

References (59)

1. Gloerich M., Bos J.L. Epac: defining a new mechanism for cAMP action. Annu. Rev. Pharmacol. Toxicol. 2010, 50:355-375.
2. Cooper D.M. Regulation and organization of adenylyl cyclases and cAMP. Biochem. J. 2003, 375:517-529.
3. de Rooij J., Zwartkruis F.J., Verheijen M.H., Cool R.H., Nijman S.M., Wittinghofer A., Bos J.L. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
4. Pannekoek W.J., Kooistra M.R., Zwartkruis F.J., Bos J.L. Cell-cell junction formation: the role of Rap1 and Rap1 guanine nucleotide exchange factors. Biochim. Biophys. Acta 2009, 1788:790-796.
5. Bos J.L., Rehmann H., Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007, 129:865-877.
6. Kawasaki H., Springett G.M., Mochizuki N., Toki S., Nakaya M., Matsuda M., Housman D.E., Graybiel A.M. A family of cAMP-binding proteins that directly activate Rap1. Science 1998, 282:2275-2279.
7. Dremier S., Milenkovic M., Blancquaert S., Dumont J.E., Doskeland S.O., Maenhaut C., Roger P.P. Cyclic adenosine 3',5'-monophosphate (cAMP)-dependent protein kinases, but not exchange proteins directly activated by cAMP (Epac), mediate thyrotropin/cAMP-dependent regulation of thyroid cells. Endocrinology 2007, 148:4612-4622.
8. Enserink J.M., Christensen A.E., de Rooij J., van Triest M., Schwede F., Genieser H.G., Doskeland S.O., Blank J.L., Bos J.L. A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 2002, 4:901-906.
9. Vuchak L.A., Tsygankova O.M., Prendergast G.V., Meinkoth J.L. Protein kinase A and B-Raf mediate extracellular signal-regulated kinase activation by thyrotropin. Mol. Pharmacol. 2009, 76:1123-1129.
10. Dumont J.E., Lamy F., Roger P., Maenhaut C. Physiological and pathological regulation of thyroid cell proliferation and differentiation by thyrotropin and other factors. Physiol. Rev. 1992, 72:667-697.
11. Dremier S., Coulonval K., Perpete S., Vandeput F., Fortemaison N., Van Keymeulen A., Deleu S., Ledent C., Clement S., Schurmans S., Dumont J.E., Lamy F., Roger P.P., Maenhaut C. The role of cyclic AMP and its effect on protein kinase A in the mitogenic action of thyrotropin on the thyroid cell. Ann. N. Y. Acad. Sci. 2002, 968:106-121.
12. van Staveren W.C.G., Weiss Solis D., Delys L., Venet D., Cappello M., Andry G., Dumont J.E., Libert F., Detours V., Maenhaut C. Gene expression in human thyrocytes and autonomous adenomas reveals suppression of negative feedbacks in tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:413-418.
13. Roger P., Taton M., Van Sande J., Dumont J.E. Mitogenic effects of thyrotropin and adenosine 3',5'-monophosphate in differentiated normal human thyroid cells in vitro. J. Clin. Endocrinol. Metab. 1988, 66:1158-1165.
14. M. Van Triest, J. de Rooij, J.L. Bos, Measurement of GTP-bound Ras-like GTPases by activation-specific probes, Methods Enzymol. 333 (2001) 343-348.
15. Simon R., Lam A., Li M.C., Ngan M., Menenzes S., Zhao Y. Analysis of gene expression data using BRB-array tools. Cancer Inform. 2007, 3:11-17.
16. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y., Gentry J., Hornik K., Hothorn T., Huber W., Iacus S., Irizarry R., Leisch F., Li C., Maechler M., Rossini A.J., Sawitzki G., Smith C., Smyth G., Tierney L., Yang J.Y., Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5:R80.
17. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5116-5121.
18. Reich M., Liefeld T., Gould J., Lerner J., Tamayo P., Mesirov J.P. GenePattern 2.0. Nat. Genet. 2006, 38:500-501.
19. R Development Core Team R: A Language and Environment for Statistical Computing 2010, R Foundation for Statistical Computing, Vienna, Austria, URL. http://www.R-project.org.
20. Dumont J.E., Dremier S., Pirson I., Maenhaut C. Cross signaling, cell specificity, and physiology. Am. J. Physiol. Cell Physiol. 2002, 283:C2-C28.
21. Song Y., Massart C., Chico-Galdo V., Jin L., De Maertelaer V., Decoster C., Dumont J.E., Van Sande J. Species specific thyroid signal transduction: conserved physiology, divergent mechanisms. Mol. Cell. Endocrinol. 2010, 319:56-62.
22. Hochbaum D., Tanos T., Ribeiro-Neto F., Altschuler D., Coso O.A. Activation of JNK by Epac is independent of its activity as a rap guanine nucleotide exchanger. J. Biol. Chem. 2003, 278:33738-33746.
23. Bartz F., Kern L., Erz D., Zhu M., Gilbert D., Meinhof T., Wirkner U., Erfle H., Muckenthaler M., Pepperkok R., Runz H. Identification of cholesterol-regulating genes by targeted RNAi screening. Cell Metab. 2009, 10:63-75.
24. Takekawa M., Itoh F., Hinoda Y., Arimura Y., Toyota M., Sekiya M., Adachi M., Imai K., Yachi A. Cloning and characterization of a human cDNA encoding a novel putative cytoplasmic protein-tyrosine-phosphatase. Biochem. Biophys. Res. Commun. 1992, 189:1223-1230.
25. Wright G.J., Jones M., Puklavec M.J., Brown M.H., Barclay A.N. The unusual distribution of the neuronal/lymphoid cell surface CD200 (OX2) glycoprotein is conserved in humans. Immunology 2001, 102:173-179.
26. Holz G.G., Chepurny O.G., Schwede F. Epac-selective cAMP analogs: new tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell. Signal. 2008, 20:10-20.
27. Fuld S., Borland G., Yarwood S.J. Elevation of cyclic AMP in Jurkat T-cells provokes distinct transcriptional responses through the protein kinase A (PKA) and exchange protein activated by cyclic AMP (EPAC) pathways. Exp. Cell Res. 2005, 309:161-173.
28. Poppe H., Rybalkin S.D., Rehmann H., Hinds T.R., Tang X.B., Christensen A.E., Schwede F., Genieser H.G., Bos J.L., Doskeland S.O., Beavo J.A., Butt E. Cyclic nucleotide analogs as probes of signaling pathways. Nat. Methods 2008, 5:277-278.
29. Breckler M., Berthouze M., Laurent A.C., Crozatier B., Morel E., Lezoualc'h F. Rap-linked cAMP signaling Epac proteins: compartmentation, functioning and disease implications. Cell. Signal. 2011, 23:1257-1266.
30. Raaijmakers J.H., Bos J.L. Specificity in Ras and Rap signaling. J. Biol. Chem. 2009, 284:10995-10999.
31. Holz G.G., Kang G., Harbeck M., Roe M.W., Chepurny O.G. Cell physiology of cAMP sensor Epac. J. Physiol. Lond. 2006, 577:5-15.
32. Kooistra M.R.H., Dube N., Bos J.L. Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 2007, 120:17-22.
33. Chepurny O.G., Kelley G.G., Dzhura I., Leech C.A., Roe M.W., Dzhura E., Li X.Q., Schwede F., Genieser H.G., Holz G.G. PKA-dependent potentiation of glucose-stimulated insulin secretion by Epac activator 8-pCPT-2'-O-Me-cAMP-AM in human islets of Langerhans. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E622-E633.
34. Ribeiro-Neto F., Leon A., Urbani-Brocard J., Lou L.G., Nyska A., Altschuler D.L. cAMP-dependent oncogenic action of Rap1b in the thyroid gland. J. Biol. Chem. 2004, 279:46868-46875.
35. Baljinnyam E., De Lorenzo M.S., Xie L.H., Iwatsubo M., Chen S., Goydos J.S., Nowycky M.C., Iwatsubo K. Exchange protein directly activated by cyclic AMP increases melanoma cell migration by a Ca2+-dependent mechanism. Cancer Res. 2010, 70:5607-5617.
36. Baljinnyam E., Iwatsubo K., Kurotani R., Wang X., Ulucan C., Iwatsubo M., Lagunoff D., Ishikawa Y. Epac increases melanoma cell migration by a heparan sulfate-related mechanism. Am. J. Physiol. Cell Physiol. 2009, 297:C802-C813.
37. Harper K., Arsenault D., Boulay-Jean S., Lauzier A., Lucien F., Dubois C.M. Autotaxin promotes cancer invasion via the lysophosphatidic acid receptor 4: participation of the cyclic AMP/EPAC/Rac1 signaling pathway in invadopodia formation. Cancer Res. 2010, 70:4634-4643.
38. Hochbaum D., Hong K., Barila G., Ribeiro-Neto F., Altschuler D.L. Epac, in synergy with cAMP-dependent protein kinase (PKA), is required for cAMP-mediated mitogenesis. J. Biol. Chem. 2008, 283:4464-4468.
39. Smallridge R.C., Marlow L.A., Copland J.A. Anaplastic thyroid cancer: molecular pathogenesis and emerging therapies. Endocr. Relat. Cancer 2009, 16:17-44.
40. Kondo T., Ezzat S., Asa S.L. Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat. Rev. Cancer 2006, 6:292-306.
41. Ros P., Rossi D.L., Acebron A., Santisteban P. Thyroid-specific gene expression in the multi-step process of thyroid carcinogenesis. Biochimie 1999, 81:389-396.
42. Brabant G., Maenhaut C., Kohrle J., Scheumann G., Dralle H., Hoang-Vu C., Hesch R.D., von zur M.A., Vassart G., Dumont J.E. Human thyrotropin receptor gene: expression in thyroid tumors and correlation to markers of thyroid differentiation and dedifferentiation. Mol. Cell. Endocrinol. 1991, 82:R7-R12.
43. Vanvooren V., Allgeier A., Nguyen M., Massart C., Parma J., Dumont J.E., Van Sande J. Mutation analysis of the Epac-Rap1 signaling pathway in cold thyroid follicular adenomas. Eur. J. Endocrinol. 2001, 144:605-610.
44. Matsuse M., Mitsutake N., Rogounovitch T., Saenko V., Nakazawa Y., Rumyantsev P., Lushnikov E., Suzuki K., Yamashita S. Mutation analysis of RAP1 gene in papillary thyroid carcinomas. Endocr. J. 2009, 56:161-164.
45. Wu C., Orozco C., Boyer J., Leglise M., Goodale J., Batalov S., Hodge C.L., Haase J., Janes J., Huss J.W., Su A.I. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10:R130.
46. Berglund L., Bjorling E., Oksvold P., Fagerberg L., Asplund A., Szigyarto C.A., Persson A., Ottosson J., Wernerus H., Nilsson P., Lundberg E., Sivertsson A., Navani S., Wester K., Kampf C., Hober S., Ponten F., Uhlen M. A genecentric Human Protein Atlas for expression profiles based on antibodies. Mol. Cell Proteomics 2008, 7:2019-2027.
47. Bigler D., Gioeli D., Conaway M.R., Weber M.J., Theodorescu D. Rap2 regulates androgen sensitivity in human prostate cancer cells. Prostate 2007, 67:1590-1599.
48. Liu Y., Sun W., Zhang K., Zheng H., Ma Y., Lin D., Zhang X., Feng L., Lei W., Zhang Z., Guo S., Han N., Tong W., Feng X., Gao Y., Cheng S. Identification of genes differentially expressed in human primary lung squamous cell carcinoma. Lung Cancer 2007, 56:307-317.
49. McLeod S.J., Li A.H., Lee R.L., Burgess A.E., Gold M.R. The Rap GTPases regulate B cell migration toward the chemokine stromal cell-derived factor-1 (CXCL12): potential role for Rap2 in promoting B cell migration. J. Immunol. 2002, 169:1365-1371.
50. Gutmann D.H., Saporito-Irwin S., DeClue J.E., Wienecke R., Guha A. Alterations in the rap1 signaling pathway are common in human gliomas. Oncogene 1997, 15:1611-1616.
51. Chevillard S., Ugolin N., Vielh P., Ory K., Levalois C., Elliott D., Clayman G.L., El Naggar A.K. Gene expression profiling of differentiated thyroid neoplasms: diagnostic and clinical implications. Clin. Cancer Res. 2004, 10:6586-6597.
52. Zhang L., Chenwei L., Mahmood R., van Golen K., Greenson J., Li G., D'Silva N.J., Li X., Burant C.F., Logsdon C.D., Simeone D.M. Identification of a putative tumor suppressor gene Rap1GAP in pancreatic cancer. Cancer Res. 2006, 66:898-906.
53. Zheng H., Gao L., Feng Y., Yuan L., Zhao H., Cornelius L.A. Down-regulation of Rap1GAP via promoter hypermethylation promotes melanoma cell proliferation, survival, and migration. Cancer Res. 2009, 69:449-457.
54. Tsygankova O.M., Feshchenko E., Klein P.S., Meinkoth J.L. Thyroid-stimulating hormone/cAMP and glycogen synthase kinase 3beta elicit opposing effects on Rap1GAP stability. J. Biol. Chem. 2004, 279:5501-5507.
55. Tsygankova O.M., Prendergast G.V., Puttaswamy K., Wang Y., Feldman M.D., Wang H., Brose M.S., Meinkoth J.L. Downregulation of Rap1GAP contributes to Ras transformation. Mol. Cell. Biol. 2007, 27:6647-6658.
56. Nellore A., Paziana K., Ma C., Tsygankova O.M., Wang Y., Puttaswamy K., Iqbal A.U., Franks S.R., Lv Y., Troxel A.B., Feldman M.D., Meinkoth J.L., Brose M.S. Loss of Rap1GAP in papillary thyroid cancer. J. Clin. Endocrinol. Metab. 2009, 94:1026-1032.
57. Zuo H., Gandhi M., Edreira M.M., Hochbaum D., Nimgaonkar V.L., Zhang P., Dipaola J., Evdokimova V., Altschuler D.L., Nikiforov Y.E. Downregulation of Rap1GAP through epigenetic silencing and loss of heterozygosity promotes invasion and progression of thyroid tumors. Cancer Res. 2010, 70:1389-1397.
58. Park Y.G., Zhao X., Lesueur F., Lowy D.R., Lancaster M., Pharoah P., Qian X., Hunter K.W. Sipa1 is a candidate for underlying the metastasis efficiency modifier locus Mtes1. Nat. Genet. 2005, 37:1055-1062.
59. Tsukamoto N., Hattori M., Yang H., Bos J.L., Minato N. Rap1 GTPase-activating protein SPA-1 negatively regulates cell adhesion. J. Biol. Chem. 1999, 274:18463-18469.