Dosage-dependent regulation of cell proliferation and adhesion through dual β2-adrenergic receptor/cAMP signals

FASEB Journal

Volumn 28, Issue 3, 2014, Pages 1342-1354

  Bruzzone, Ariana ^a   Saulière, Aude ^b   Finana, Frédéric ^c   Sénard, Jean Michel ^b,d   Lüthy, Isabel ^a   Galés, Céline ^b  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b University Hospital of Toulouse   (France)

^c INSTITUT DE RECHERCHE PIERRE FABRE   (France)

^d TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

Epac; MCF 10A human breast cell line; PKA; Signaling compartmentalization

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ISOPRENALINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

ARTICLE; BREAST CELL; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; EPAC; MCF-10A HUMAN BREAST CELL LINE; PHYSIOLOGY; PKA; SIGNALING COMPARTMENTALIZATION; TUMOR CELL LINE;

EPAC; MCF-10A HUMAN BREAST CELL LINE; PKA; SIGNALING COMPARTMENTALIZATION;

CELL ADHESION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIC AMP; HUMANS; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION;

EID: 84899559940     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-239285     Document Type: Article

References (63)

1. Daly, C. J., and McGrath, J. C. (2011) Previously unsuspected widespread cellular and tissue distribution of beta-Adrenoceptors and its relevance to drug action. Trends Pharmacol. Sci. 32, 219-226
2. Cheng, X., Ji, Z., Tsalkova, T., and Mei, F. (2008) Epac and PKA: a tale of two intracellular cAMP receptors. Acta Biochim. Biophys. Sin. 40, 651-662
3. Kim, M. O., Lee, Y. J., Park, J. H., Ryu, J. M., Yun, S. P., and Han, H. J. (2012) PKA and cAMP stimulate proliferation of mouse embryonic stem cells by elevating GLUT1 expression mediated by the NF-kappaB and CREB/CBP signaling pathways. Biochim. Biophys. Acta 1820, 1636-1646
4. Toll, L., Jimenez, L., Waleh, N., Jozwiak, K., Woo, A. Y., Xiao, R. P., Bernier, M., and Wainer, I. W. (2011) α2-Adrenergic receptor agonists inhibit the proliferation of 1321N1 astrocytoma cells. J. Pharmacol. Exp. Ther. 336, 524-532
5. Nedvetsky, P. I., Kwon, S. H., Debnath, J., and Mostov, K. E. (2012) Cyclic AMP regulates formation of mammary epithelial acini in vitro. Mol. Biol. Cell 23, 2973-2981
6. Li, D. M., and Feng, Y. M. (2011) Signaling mechanism of cell adhesion molecules in breast cancer metastasis: potential therapeutic targets. Breast Cancer Res. Treat. 128, 7-21
7. Chen, L., Zhang, J. J., and Huang, X. Y. (2008) cAMP inhibits cell migration by interfering with Rac-induced lamellipodium formation. J. Biol. Chem. 283, 13799-13805
8. Grandoch, M., Rose, A., ter Braak, M., Jendrossek, V., Rubben, H., Fischer, J. W., Schmidt, M., and Weber, A. A. (2009) Epac inhibits migration and proliferation of human prostate carcinoma cells. Br. J. Cancer 101, 2038-2042
9. Mantovani, G., Lania, A. G., Bondioni, S., Peverelli, E., Pedroni, C., Ferrero, S., Pellegrini, C., Vicentini, L., Arnaldi, G., Bosari, S., Beck-Peccoz, P., and Spada, A. (2008) Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Exp. Cell Res. 314, 123-130
10. Rivas, M., and Santisteban, P. (2003) TSH-Activated signaling pathways in thyroid tumorigenesis. Mol. Cell. Endocrinol. 213, 31-45
11. Thaker, P. H., Han, L. Y., Kamat, A. A., Arevalo, J. M., Takahashi, R., Lu, C., Jennings, N. B., Armaiz-Pena, G., Bankson, J. A., Ravoori, M., Merritt, W. M., Lin, Y. G., Mangala, L. S., Kim, T. J., Coleman, R. L., Landen, C. N., Li, Y., Felix, E., Sanguino, A. M., Newman, R. A., Lloyd, M., Gershenson, D. M., Kundra, V., Lopez-Berestein, G., Lutgendorf, S. K., Cole, S. W., and Sood, A. K. (2006) Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat. Med. 12, 939-944
12. Armaiz-Pena, G. N., Allen, J. K., Cruz, A., Stone, R. L., Nick, A. M., Lin, Y. G., Han, L. Y., Mangala, L. S., Villares, G. J., Vivas-Mejia, P., Rodriguez-Aguayo, C., Nagaraja, A. S., Gharpure, K. M., Wu, Z., English, R. D., Soman, K. V., Shazhad, M. M., Zigler, M., Deavers, M. T., Zien, A., Soldatos, T. G., Jackson, D. B., Wiktorowicz, J. E., Torres-Lugo, M., Young, T., De Geest, K., Gallick, G. E., Bar-Eli, M., Lopez-Berestein, G., Cole, S. W., Lopez, G. E., Lutgendorf, S. K., and Sood, A. K. (2013) Src activation by beta-Adrenoreceptors is a key switch for tumour metastasis. Nat. Commun. 4, 1403
13. Tagliaferri, P., Katsaros, D., Clair, T., Ally, S., Tortora, G., Neckers, L., Rubalcava, B., Parandoosh, Z., Chang, Y. A., Revankar, G. R., Crabtree, G. W., Robins, R. K., and Cho-Chung, Y. S. (1988) Synergistic inhibition of growth of breast and colon human cancer cell lines by site-selective cyclic AMP analogues. Cancer Res. 48, 1642-1650
14. Tagliaferri, P., Katsaros, D., Clair, T., Neckers, L., Robins, R. K., and Cho-Chung, Y. S. (1988) Reverse transformation of Harvey murine sarcoma virus-Transformed NIH/3T3 cells by site-selective cyclic AMP analogs. J. Biol. Chem. 263, 409-416
15. Tortora, G., Tagliaferri, P., Clair, T., Colamonici, O., Neckers, L. M., Robins, R. K., and Cho-Chung, Y. S. (1988) Site-selective cAMP analogs at micromolar concentrations induce growth arrest and differentiation of acute promyelocytic, chronic myelocytic, and acute lymphocytic human leukemia cell lines. Blood 71, 230-233
16. Rangarajan, S., Enserink, J. M., Kuiperij, H. B., de Rooij, J., Price, L. S., Schwede, F., and Bos, J. L. (2003) Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-Adrenergic receptor. J. Cell Biol. 160, 487-493
17. Eid, A. H. (2012) cAMP induces adhesion of microvascular smooth muscle cells to fibronectin via an Epac-mediated but PKA-independent mechanism. Cell. Physiol. Biochem. 30, 247-258
18. Enserink, J. M., Price, L. S., Methi, T., Mahic, M., Sonnenberg, A., Bos, J. L., and Tasken, K. (2004) The cAMP-Epac-Rap1 pathway regulates cell spreading and cell adhesion to laminin-5 through the alpha3beta1 integrin but not the alpha6beta4 integrin. J. Biol. Chem. 279, 44889-44896
19. Lorenowicz, M. J., van Gils, J., de Boer, M., Hordijk, P. L., and Fernandez-Borja, M. (2006) Epac1-Rap1 signaling regulates monocyte adhesion and chemotaxis. J. Leukoc. Biol. 80, 1542-1552
20. Badino, G. R., Novelli, A., Girardi, C., and Di Carlo, F. (1996) Evidence for functional beta-Adrenoceptor subtypes in CG-5 breast cancer cell. Pharmacol. Res. 33, 255-260
21. Slotkin, T. A., Zhang, J., Dancel, R., Garcia, S. J., Willis, C., and Seidler, F. J. (2000) Beta-Adrenoceptor signaling and its control of cell replication in MDA-MB-231 human breast cancer cells. Breast Cancer Res. Treat. 60, 153-166
22. Vandewalle, B., Revillion, F., and Lefebvre, J. (1990) Functional beta-Adrenergic receptors in breast cancer cells. J. Cancer Res. Clin. Oncol. 116, 303-306
23. Perez, P. C., Bruzzone, A., Sarappa, M., Castillo, L., and Luthy, I. (2012) Involvement of alpha2-And beta2-Adrenoceptors on breast cancer cell proliferation and tumour growth regulation. Br. J. Pharmacol. 166, 721-736
24. Draoui, A., Vandewalle, B., Hornez, L., Revillion, F., and Lefebvre, J. (1991) Beta-Adrenergic receptors in human breast cancer: identification, characterization and correlation with progesterone and estradiol receptors. Anticancer Res. 11, 677-680
25. Powe, D. G., Voss, M. J., Habashy, H. O., Zanker, K. S., Green, A. R., Ellis, I. O., and Entschladen, F. (2011) Alpha-And beta-Adrenergic receptor (AR) protein expression is associated with poor clinical outcome in breast cancer: an immunohistochemical study. Breast Cancer Res. Treat. 130, 457-463
26. Barron, T. I., Sharp, L., and Visvanathan, K. (2012) Betaadrenergic blocking drugs in breast cancer: a perspective review. Ther. Adv. Med. Oncol. 4, 113-125
27. Powe, D. G., Voss, M. J., Zanker, K. S., Habashy, H. O., Green, A. R., Ellis, I. O., and Entschladen, F. (2010) Beta-blocker drug therapy reduces secondary cancer formation in breast cancer and improves cancer specific survival. Oncotarget 1, 628-638
28. Carie, A. E., and Sebti, S. M. (2007) A chemical biology approach identifies a beta-2 adrenergic receptor agonist that causes human tumor regression by blocking the Raf-1/Mek-1/Erk1/2 pathway. Oncogene 26, 3777-3788
29. Sloan, E. K., Priceman, S. J., Cox, B. F., Yu, S., Pimentel, M. A., Tangkanangnukul, V., Arevalo, J. M., Morizono, K., Karanikolas, B. D., Wu, L., Sood, A. K., and Cole, S. W. (2010) The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res. 70, 7042-7052
30. Spina, A., Di Maiolo, F., Esposito, A., Sapio, L., Chiosi, E., Sorvillo, L., and Naviglio, S. (2012) cAMP elevation downregulates beta3 integrin and focal adhesion kinase and inhibits leptin-induced migration of MDA-MB-231 breast cancer cells. Biores. Open Access 1, 324-332
31. Wellner, R. B., He, X. J., Marmary, Y., and Baum, B. J. (1988) Functional beta-Adrenergic receptors in a human mammary cell line (HBL-100). Biochem. Pharmacol. 37, 3035-3037
32. Sauliere, A., Bellot, M., Paris, H., Denis, C., Finana, F., Hansen, J. T., Altie, M. F., Seguelas, M. H., Pathak, A., Hansen, J. L., Senard, J. M., and Gales, C. (2012) Deciphering biased-Agonism complexity reveals a new active AT1 receptor entity. Nat. Chem. Biol. 8, 622-630
33. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-Time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25, 402-408
34. Gilman, A. G. (1970) A protein binding assay for adenosine 3=:5=-cyclic monophosphate. Proc. Natl. Acad. Sci. U. S. A. 67, 305-312
35. Shenoy, S. K., Drake, M. T., Nelson, C. D., Houtz, D. A., Xiao, K., Madabushi, S., Reiter, E., Premont, R. T., Lichtarge, O., and Lefkowitz, R. J. (2006) beta-Arrestin-dependent, G proteinindependent ERK1/2 activation by the beta2 adrenergic receptor. J. Biol. Chem. 281, 1261-1273
36. Gjertsen, B. T., Mellgren, G., Otten, A., Maronde, E., Genieser, H. G., Jastorff, B., Vintermyr, O. K., McKnight, G. S., and Doskeland, S. O. (1995) Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture. Basal cAMP-kinase activity modulates interleukin-1 beta action. J. Biol. Chem. 270, 20599-20607
37. Almahariq, M., Tsalkova, T., Mei, F. C., Chen, H., Zhou, J., Sastry, S. K., Schwede, F., and Cheng, X. (2013) A novel EPAC-specific inhibitor suppresses pancreatic cancer cell migration and invasion. Mol. Pharmacol. 83, 122-128
38. Castellone, M. D., Teramoto, H., Williams, B. O., Druey, K. M., and Gutkind, J. S. (2005) Prostaglandin E2 promotes colon cancer cell growth through a Gs-Axin-beta-catenin signaling axis. Science 310, 1504-1510
39. Hochbaum, D., Tanos, T., Ribeiro-Neto, F., Altschuler, D., and Coso, O. A. (2003) Activation of JNK by Epac is independent of its activity as a Rap guanine nucleotide exchanger. J. Biol. Chem. 278, 33738-33746
40. Ostrom, R. S., and Insel, P. A. (2004) The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br. J. Pharmacol. 143, 235-245
41. Mouat, M. F., Greenspan, P., Byerley, L. O., and Grider, A. (2003) Zinc uptake into MCF-10A cells is inhibited by cholesterol depletion. J. Nutr. Biochem. 14, 74-80
42. Sun, Y., Huang, J., Xiang, Y., Bastepe, M., Juppner, H., Kobilka, B. K., Zhang, J. J., and Huang, X. Y. (2007) Dosage-dependent switch from G protein-coupled to G protein-independent signaling by a GPCR. EMBO J. 26, 53-64
43. Swaminath, G., Xiang, Y., Lee, T. W., Steenhuis, J., Parnot, C., and Kobilka, B. K. (2004) Sequential binding of agonists to the beta2 adrenoceptor. Kinetic evidence for intermediate conformational states. J. Biol. Chem. 279, 686-691
44. Guzzi, F., Zanchetta, D., Cassoni, P., Guzzi, V., Francolini, M., Parenti, M., and Chini, B. (2002) Localization of the human oxytocin receptor in caveolin-1 enriched domains turns the receptor-mediated inhibition of cell growth into a proliferative response. Oncogene 21, 1658-1667
45. Leitinger, B., and Hogg, N. (2002) The involvement of lipid rafts in the regulation of integrin function. J. Cell Sci. 115, 963-972
46. Zocher, M., Zhang, C., Rasmussen, S. G., Kobilka, B. K., and Muller, D. J. (2012) Cholesterol increases kinetic, energetic, and mechanical stability of the human beta2-Adrenergic receptor. Proc. Natl. Acad. Sci. U. S. A. 109, E3463-3472
47. Pontier, S. M., Percherancier, Y., Galandrin, S., Breit, A., Gales, C., and Bouvier, M. (2008) Cholesterol-dependent separation of the beta2-Adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J. Biol. Chem. 283, 24659-24672
48. Xiang, Y., Rybin, V. O., Steinberg, S. F., and Kobilka, B. (2002) Caveolar localization dictates physiologic signaling of beta 2-Adrenoceptors in neonatal cardiac myocytes. J. Biol. Chem. 277, 34280-34286
49. Kassel, K. M., Wyatt, T. A., Panettieri, R. A., Jr., and Toews, M. L. (2008) Inhibition of human airway smooth muscle cell proliferation by beta 2-Adrenergic receptors and cAMP is PKA independent: evidence for EPAC involvement. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L131-138
50. Brock, M., Nickel, A. C., Madziar, B., Blusztajn, J. K., and Berse, B. (2007) Differential regulation of the high affinity choline transporter and the cholinergic locus by cAMP signaling pathways. Brain Res. 1145, 1-10
51. Kiermayer, S., Biondi, R. M., Imig, J., Plotz, G., Haupenthal, J., Zeuzem, S., and Piiper, A. (2005) Epac activation converts cAMP from a proliferative into a differentiation signal in PC12 cells. Mol. Biol. Cell 16, 5639-5648
52. Dodge-Kafka, K. L., Soughayer, J., Pare, G. C., Carlisle Michel, J. J., Langeberg, L. K., Kapiloff, M. S., and Scott, J. D. (2005) The protein kinase A anchoring protein mAKAP coordinates two integrated cAMP effector pathways. Nature 437, 574-578
53. Honegger, K. J., Capuano, P., Winter, C., Bacic, D., Stange, G., Wagner, C. A., Biber, J., Murer, H., and Hernando, N. (2006) Regulation of sodium-proton exchanger isoform 3 (NHE3) by PKA and exchange protein directly activated by cAMP (EPAC). Proc. Natl. Acad. Sci. U. S. A. 103, 803-808
54. Cooper, D. M. (2005) Compartmentalization of adenylate cyclase and cAMP signalling. Biochem. Soc. Trans. 33, 1319-1322
55. Houslay, M. D. (2010) Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem. Sci. 35, 91-100
56. Agarwal, S. R., MacDougall, D. A., Tyser, R., Pugh, S. D., Calaghan, S. C., and Harvey, R. D. (2011) Effects of cholesterol depletion on compartmentalized cAMP responses in adult cardiac myocytes. J. Mol. Cell. Cardiol. 50, 500-509
57. Wu, C. Y., DiJulio, D. H., Jacobson, K. L., McKnight, G. S., and Watson, E. L. (2010) The contribution of AKAP5 in amylase secretion from mouse parotid acini. Am. J. Physiol. Cell Physiol. 298, C1151-C1158
58. De Arcangelis, V., Liu, S., Zhang, D., Soto, D., and Xiang, Y. K. (2010) Equilibrium between adenylyl cyclase and phosphodiesterase patterns adrenergic agonist dose-dependent spatiotemporal cAMP/protein kinase A activities in cardiomyocytes. Mol. Pharmacol. 78, 340-349
59. Zaccolo, M., Cesetti, T., Di Benedetto, G., Mongillo, M., Lissandron, V., Terrin, A., and Zamparo, I. (2005) Imaging the cAMP-dependent signal transduction pathway. Biochem. Soc. Trans. 33, 1323-1326
60. Inderwies, T., Pfaffl, M. W., Meyer, H. H., Blum, J. W., and Bruckmaier, R. M. (2003) Detection and quantification of mRNA expression of alpha-And beta-Adrenergic receptor subtypes in the mammary gland of dairy cows. Domest. Anim. Endocrinol. 24, 123-135
61. Marchetti, B., Fortier, M. A., Poyet, P., Follea, N., Pelletier, G., and Labrie, F. (1990) Beta-Adrenergic receptors in the rat mammary gland during pregnancy and lactation: characterization, distribution, and coupling to adenylate cyclase. Endocrinology 126, 565-574
62. Bos, J. L. (2003) Epac: a new cAMP target and new avenues in cAMP research. Nat. Rev. Mol. Cell Biol. 4, 733-738
63. Enserink, J. M., Christensen, A. E., de Rooij, J., van Triest, M., Schwede, F., Genieser, H. G., Doskeland, S. O., Blank, J. L., and Bos, J. L. (2002) A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK. Nat. Cell Biol. 4, 901-906