In-vivo detection of binary PKA network interactions upon activation of endogenous GPCRs

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Röck, Ruth ^a   Bachmann, Verena ^a   Bhang, Hyo Eun C ^b,d   Malleshaiah, Mohan ^c,e   Raffeiner, Philipp ^a   Mayrhofer, Johanna E ^a   Tschaikner, Philipp M ^a   Bister, Klaus ^a   Aanstad, Pia ^a   Pomper, Martin G ^b   Michnick, Stephen W ^c   Stefan, Eduard ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; PROTEIN BINDING;

ANIMAL; DRUG SCREENING; EMBRYOLOGY; GENETIC PROCEDURES; HEK293 CELL LINE; HUMAN; METABOLISM; MOUSE; NONMAMMALIAN EMBRYO; OSTEOSARCOMA; PROTEIN ANALYSIS; REPORTER GENE; SACCHAROMYCES CEREVISIAE; TUMOR CELL LINE; ZEBRA FISH;

ANIMALS; BIOSENSING TECHNIQUES; CELL LINE, TUMOR; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EMBRYO, NONMAMMALIAN; GENES, REPORTER; HEK293 CELLS; HUMANS; MICE; OSTEOSARCOMA; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECEPTORS, G-PROTEIN-COUPLED; SACCHAROMYCES CEREVISIAE; XENOGRAFT MODEL ANTITUMOR ASSAYS; ZEBRAFISH;

EID: 84932617822     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11133     Document Type: Article

References (69)

1. Scott, J. D. & Pawson, T. Cell signaling in space and time: where proteins come together and when they're apart. Science 326, 1220-4 (2009).
2. Good, M. C., Zalatan, J. G. & Lim, W. A. Scaffold proteins: hubs for controlling the flow of cellular information. Science 332, 680-6 (2011).
3. Rajakulendran, T., Sahmi, M., Lefrancois, M., Sicheri, F. & Therrien, M. A dimerization-dependent mechanism drives RAF catalytic activation. Nature 461, 542-5 (2009).
4. Stephen, A. G., Esposito, D., Bagni, R. K. & McCormick, F. Dragging ras back in the ring. Cancer Cell 25, 272-81 (2014).
5. Heidorn, S. J. et al. Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140, 209-21 (2010).
6. Hynes, N. E. & MacDonald, G. ErbB receptors and signaling pathways in cancer. Curr Opin Cell Biol 21, 177-84 (2009).
7. Cheung, J. et al. Structural insights into mis-regulation of protein kinase A in human tumors. Proc Natl Acad Sci U S A 112, 1374-9 (2015).
8. Scott, J. D., Dessauer, C. W. & Tasken, K. Creating order from chaos: cellular regulation by kinase anchoring. Annu Rev Pharmacol Toxicol 53, 187-210 (2013).
9. Pierce, K. L., Premont, R. T. & Lefkowitz, R. J. Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3, 639-50 (2002).
10. Lappano, R. & Maggiolini, M. G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10, 47-60 (2011).
11. O'Hayre, M. et al. The emerging mutational landscape of G proteins and G-protein-coupled receptors in cancer. Nat Rev Cancer 13, 412-24 (2013).
12. Taylor, S. S., Ilouz, R., Zhang, P. & Kornev, A. P. Assembly of allosteric macromolecular switches: lessons from PKA. Nat Rev Mol Cell Biol 13, 646-58 (2012).
13. Dalton, G. D. & Dewey, W. L. Protein kinase inhibitor peptide (PKI): a family of endogenous neuropeptides that modulate neuronal cAMP-dependent protein kinase function. Neuropeptides 40, 23-34 (2006).
14. Walsh, D. A., Ashby, C. D., Gonzalez, C., Calkins, D. & Fischer, E. H. Krebs EG: Purification and characterization of a protein inhibitor of adenosine 3',5'-monophosphate-dependent protein kinases. J Biol Chem 246, 1977-85 (1971).
15. Scott, J. D., Fischer, E. H., Demaille, J. G. & Krebs, E. G. Identification of an inhibitory region of the heat-stable protein inhibitor of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA 82, 4379-83 (1985).
16. Stratakis, C. A. cAMP/PKA signaling defects in tumors: genetics and tissue-specific pluripotential cell-derived lesions in human and mouse. Mol Cell Endocrinol 371, 208-20 (2013).
17. Beuschlein, F. et al. Constitutive activation of PKA catalytic subunit in adrenal Cushing's syndrome. N Engl J Med 370, 1019-28 (2014).
18. Goh, G. et al. Recurrent activating mutation in PRKACA in cortisol-producing adrenal tumors. Nat Genet 46, 613-7 (2014).
19. Sato, Y. et al. Recurrent somatic mutations underlie corticotropin-independent Cushing's syndrome. Science 344, 917-20 (2014).
20. Espiard, S., Ragazzon, B. & Bertherat, J. Protein kinase a alterations in adrenocortical tumors. Horm Metab Res 46, 869-75 (2014).
21. Calebiro, D. et al. PKA catalytic subunit mutations in adrenocortical Cushing's adenoma impair association with the regulatory subunit. Nat Commun 5, 5680 (2014).
22. Di Dalmazi, G. et al. Novel somatic mutations in the catalytic subunit of the protein kinase A as a cause of adrenal Cushing's syndrome: a European multicentric study. J Clin Endocrinol Metab 99, E2093-100 (2014).
23. Cao, Y. et al. Activating hotspot L205R mutation in PRKACA and adrenal Cushing's syndrome. Science 344, 913-7 (2014).
24. Honeyman, J. N. et al. Detection of a recurrent DNAJB1-PRKACA chimeric transcript in fibrolamellar hepatocellular carcinoma. Science 343, 1010-4 (2014).
25. Ivanov, A. A., Khuri, F. R. & Fu, H. Targeting protein-protein interactions as an anticancer strategy. Trends Pharmacol Sci 34, 393-400 (2013).
26. Zhang, J., Yang, P. L. & Gray, N. S. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 9, 28-39 (2009).
27. De, A., Jasani, A., Arora, R. & Gambhir, S. S. Evolution of BRET Biosensors from Live Cell to Tissue-Scale Imaging. Front Endocrinol (Lausanne) 4, 131 (2013).
28. Audet, M., Lagace, M., Silversides, D. W. & Bouvier, M. Protein-protein interactions monitored in cells from transgenic mice using bioluminescence resonance energy transfer. FASEB J 24, 2829-38 (2010).
29. Johnsson, A. K. et al. The Rac-FRET Mouse Reveals Tight Spatiotemporal Control of Rac Activity in Primary Cells and Tissues. Cell Rep 6, 1153-64 (2014).
30. Calebiro, D. et al. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7, e1000172 (2009).
31. Luker, K. E. et al. In vivo imaging of ligand receptor binding with Gaussia luciferase complementation. Nat Med 18, 172-7 (2012).
32. Luker, K. E. et al. Kinetics of regulated protein-protein interactions revealed with firefly luciferase complementation imaging in cells and living animals. Proc Natl Acad Sci USA 101, 12288-93 (2004).
33. Stefan, E. et al. Quantification of dynamic protein complexes using Renilla luciferase fragment complementation applied to protein kinase A activities in vivo. Proc Natl Acad Sci USA 104, 16916-21 (2007).
34. Chan, C. T. et al. Discovery and validation of small-molecule heat-shock protein 90 inhibitors through multimodality molecular imaging in living subjects. Proc Natl Acad Sci USA 109, E2476-85 (2012).
35. Michnick, S. W., Ear, P. H., Manderson, E. N., Remy, I. & Stefan, E. Universal strategies in research and drug discovery based on protein-fragment complementation assays. Nat Rev Drug Discov 6, 569-82 (2007).
36. Houslay, M. D. Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem Sci 35, 91-100 (2009).
37. Lefkowitz, R. J. Seven transmembrane receptors: something old, something new. Acta Physiol (Oxf) 190, 9-19 (2007).
38. Daaka, Y., Luttrell, L. M. & Lefkowitz, R. J. Switching of the coupling of the beta2-adrenergic receptor to different G proteins by protein kinase A. Nature 390, 88-91 (1997).
39. Thaker, P. H. et al. Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma. Nat Med 12, 939-44 (2006).
40. Wong, W. & Scott, J. D. AKAP signalling complexes: focal points in space and time. Nat Rev Mol Cell Biol 5, 959-70 (2004).
41. Zhang, J., Hupfeld, C., Taylor, S., Olefsky, J. & Tsien, R. Y. Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes. Nature 437, 569-73 (2005).
42. Friedman, J., Babu, B. & Clark, R. B. Beta(2)-adrenergic receptor lacking the cyclic AMP-dependent protein kinase consensus sites fully activates extracellular signal-regulated kinase 1/2 in human embryonic kidney 293 cells: lack of evidence for G(s)/G(i) switching. Mol Pharmacol 62, 1094-102 (2002).
43. Bhang, H. E., Gabrielson, K. L., Laterra, J., Fisher, P. B. & Pomper, M. G. Tumor-specific imaging through progression elevated gene-3 promoter-driven gene expression. Nat Med 17, 123-9 (2011).
44. Griffioen, G. & Thevelein, J. M. Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet 41, 199-207 (2002).
45. Stefan, E. et al. PKA regulatory subunits mediate synergy among conserved G-protein-coupled receptor cascades. Nat Commun 2, 598 (2011).
46. Manderson, E. N., Malleshaiah, M. & Michnick, S. W. A novel genetic screen implicates Elm1 in the inactivation of the yeast transcription factor SBF. PLoS One 3, e1500 (2008).
47. Malleshaiah, M. K., Shahrezaei, V., Swain, P. S. & Michnick, S. W. The scaffold protein Ste5 directly controls a switch-like mating decision in yeast. Nature 465, 101-5 (2010).
48. Harris, B. Z., Hillier, B. J. & Lim, W. A. Energetic determinants of internal motifrecognition by PDZ domains. Biochemistry 40, 5921-30 (2001).
49. White, R., Rose, K. & Zon, L. Zebrafish cancer: the state of the art and the path forward. Nat Rev Cancer 13, 624-36 (2013).
50. Gibert, Y., Trengove, M. C. & Ward, A. C. Zebrafish as a genetic model in pre-clinical drug testing and screening. Curr Med Chem 20, 2458-66 (2013).
51. Das, B.C., McCormick, L., Thapa, P., Karki, R. & Evans, T. Use of zebrafish in chemical biology and drug discovery. Future Med Chem 5, 2103-16 (2013).
52. Chakraborty, C., Hsu, C.H., Wen, Z.H., Lin, C.S. & Agoramoorthy, G. Zebrafish: a complete animal model for in vivo drug discovery and development. Curr Drug Metab 10, 116-24 (2009).
53. Briscoe, J. & Therond, P. P. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat Rev Mol Cell Biol 14, 416-29 (2013).
54. Clevers, H. & Nusse, R. Wnt/beta-catenin signaling and disease. Cell 149, 1192-205 (2012).
55. Stuckemann, T. et al. Zebrafish Cxcr4a determines the proliferative response to Hedgehog signalling. Development 139, 2711-20 (2012).
56. Lappano, R. & Maggiolini, M. G protein-coupled receptors: novel targets for drug discovery in cancer. Nat Rev Drug Discov 10, 47-60 (2011).
57. MacDonald, M. L. et al. Identifying off-target effects and hidden phenotypes of drugs in human cells. Nat Chem Biol 2, 329-37 (2006).
58. Alvarez-Curto, E., Pediani, J. D. & Milligan, G. Applications of fluorescence and bioluminescence resonance energy transfer to drug discovery at G protein coupled receptors. Anal Bioanal Chem 398, 167-80 (2010).
59. Lohse, M. J., Nuber, S. & Hoffmann, C. Fluorescence/bioluminescence resonance energy transfer techniques to study G-proteincoupled receptor activation and signaling. Pharmacol Rev 64, 299-336 (2012).
60. Marullo, S. & Bouvier, M. Resonance energy transfer approaches in molecular pharmacology and beyond. Trends Pharmacol Sci 28, 362-5 (2007).
61. Bachmann, V. A. et al. Reciprocal regulation of PKA and Rac signaling. Proc Natl Acad Sci USA 110, 8531-6 (2013).
62. Lignitto, L. et al. Proteolysis of MOB1 by the ubiquitin ligase praja2 attenuates Hippo signalling and supports glioblastoma growth. Nat Commun 4, 1822 (2013).
63. Lignitto, L. et al. Control of PKA stability and signalling by the RING ligase praja2. Nat Cell Biol 13, 412-22 (2011).
64. Bachmann, V. A., Bister, K. & Stefan, E. Interplay of PKA and Rac: Fine-tuning of Rac localization and signaling. Small GTPases 4, 247-51 (2013).
65. Skoumbourdis, A. P. et al. Exploration and optimization of substituted triazolothiadiazines and triazolopyridazines as PDE4 inhibitors. Bioorg Med Chem Lett 19, 3686-92 (2009).
66. Hart, J. R. et al. Inhibitor of MYC identified in a Krohnke pyridine library. Proc Natl Acad Sci USA 111, 12556-61 (2014).
67. Raffeiner, P. et al. In vivo quantification and perturbation of Myc-Max interactions and the impact on oncogenic potential. Oncotarget 5, 8869-78 (2014).
68. Filteau, M. et al. Systematic identification of signal integration by protein kinase A. Proc Natl Acad Sci USA 112, 4501-6 (2015).
69. Day, R. N., Walder, J. A. & Maurer, R. A. A protein kinase inhibitor gene reduces both basal and multihormone-stimulated prolactin gene transcription. J Biol Chem 264, 431-6 (1989).