Pain modulators regulate the dynamics of PKA-RII phosphorylation in subgroups of sensory neurons

Journal of Cell Science

Volumn 127, Issue 1, 2014, Pages 216-229

  Isensee, Joerg ^a,b   Diskar, Mandy ^c   Waldherr, Steffen ^d   Buschow, René ^a,b,e   Hasenauer, Jan ^f,g   Prinz, Anke ^c   Allgöwer, Frank ^f   Herberg, Friedrich W ^c   Hucho, Tim ^a,b  

^a UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c UNIVERSITY OF KASSEL   (Germany)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

^f UNIVERSITY OF STUTTGART   (Germany)

^g INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

Camp response element binding protein; Nociception; Protein kinase A; RII phosphorylation; Sensitization

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CAPSAICIN; CYCLIC AMP DEPENDENT PROTEIN KINASE REGULATORY SUBUNIT IIBETA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ISOLECTIN B4; PHOSPHOPROTEIN PHOSPHATASE 2A; PROSTAGLANDIN E2; SODIUM CHANNEL NAV1.8; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MALE; MEDIATOR; NERVE CELL CULTURE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SENSORY NERVE CELL;

CAMP RESPONSE ELEMENT-BINDING PROTEIN; NOCICEPTION; PROTEIN KINASE A; RII PHOSPHORYLATION; SENSITIZATION;

ANIMALS; BIOLOGICAL MARKERS; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM; CAPSAICIN; COLFORSIN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIIBETA SUBUNIT; CYCLIC AMP-DEPENDENT PROTEIN KINASE TYPE I; CYCLOSPORINE; DINOPROSTONE; GENE EXPRESSION REGULATION; MALE; NAV1.8 VOLTAGE-GATED SODIUM CHANNEL; NOCICEPTION; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PHOSPHATASE 2; RATS; RATS, SPRAGUE-DAWLEY; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; TRPV CATION CHANNELS;

EID: 84891374752     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.136580     Document Type: Article

References (52)

1. Amieux, P. S., Cummings, D. E., Motamed, K., Brandon, E. P., Wailes, L. A., Le, K., Idzerda, R. L. and McKnight, G. S. (1997). Compensatory regulation of RIalpha protein levels in protein kinase A mutant mice. J. Biol. Chem. 272, 3993-3998
2. Amieux, P. S., Howe, D. G., Knickerbocker, H., Lee, D. C., Su, T., Laszlo, G. S., Idzerda, R. L. and Mcknight, G. S. (2002). Increased basal cAMP-dependent protein kinase activity inhibits the formation of mesoderm-derived structures in the developing mouse embryo. J. Biol. Chem. 277, 27294-27304
3. Basbaum, A. I., Bautista, D. M., Scherrer, G. and Julius, D. (2009). Cellular and molecular mechanisms of pain. Cell 139, 267-284
4. Belmonte, C. and Viana, F. (2008). Molecular and cellular limits to somatosensory specificity. Mol. Pain 4, 14
5. Bhave, G., Zhu, W., Wang, H., Brasier, D. J., Oxford, G. S. and Gereau, R. W., 4th (2002). cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35, 721-731
6. Boettcher, A. J., Wu, J., Kim, C., Yang, J., Bruystens, J., Cheung, N., Pennypacker, J. K., Blumenthal, D. A., Kornev, A. P. and Taylor, S. S. (2011) Realizing the allosteric potential of the tetrameric protein kinase A RIa holoenzyme. Structure 19, 265-276
7. Brandon, E. P., Logue, S. F., Adams, M. R., Qi, M., Sullivan, S. P., Matsumoto, A. M., Dorsa, D. M., Wehner, J. M., McKnight, G. S. and Idzerda, R. L. (1998) Defective motor behavior and neural gene expression in RIIβeta-protein kinase A mutant mice. J. Neurosci. 18, 3639-3649
8. Cadd, G. and McKnight, G. S. (1989). Distinct patterns of cAMP-dependent protein kinase gene expression in mouse brain. Neuron 3, 71-79
9. Choi, S. C. and Wette, R. (1969). Maximum likelihood estimation of the parameters of the gamma distribution and their bias. Technometrics 11, 683-690
10. Cummings, D. E., Brandon, E. P., Planas, J. V., Motamed, K., Idzerda, R. L and McKnight, G. S. (1996). Genetically lean mice result from targeted disruption of the RII beta subunit of protein kinase A. Nature 382, 622-626
11. Diskar, M., Zenn, H. M., Kaupisch, A., Prinz, A. and Herberg, F. W. (2007) Molecular basis for isoform-specific autoregulation of protein kinase A. Cell Signal. 19, 2024-2034
12. England, S., Bevan, S. and Docherty, R. J. (1996). PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J. Physiol. 495, 429-440
13. Fischer, Q. S., Beaver, C. J., Yang, Y., Rao, Y., Jakobsdottir, K. B., Storm, D R., McKnight, G. S. and Daw, N. W. (2004). Requirement for the RIIβeta isoform of PKA, but not calcium-stimulated adenylyl cyclase, in visual cortical plasticity. J. Neurosci. 24, 9049-9058
14. Fitzgerald, E. M., Okuse, K., Wood, J. N., Dolphin, A. C. and Moss, S. J. (1999) cAMP-dependent phosphorylation of the tetrodotoxin-resistant voltage-dependent sodium channel SNS. J. Physiol. 516, 433-446
15. Friedman, N., Cai, L. and Xie, X. S. (2006). Linking stochastic dynamics to population distribution: an analytical framework of gene expression. Phys. Rev Lett. 97, 168302
16. Georgi, B., Costa, I. G. and Schliep, A. (2010). PyMix-the python mixture package-a tool for clustering of heterogeneous biological data. BMC Bioinformatics 11, 9
17. Huang, Y. Y., Kandel, E. R., Varshavsky, L., Brandon, E. P., Qi, M., Idzerda, RL., McKnight, G. S. and Bourtchouladze, R. (1995). A genetic test of the effects of mutations in PKA on mossy fiber LTP and its relation to spatial and contextual learning. Cell 83, 1211-1222
18. Hucho, T. and Levine, J. D. (2007). Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 55, 365-376
19. Inan, M., Lu, H. C., Albright, M. J., She, W. C. and Crair, M. C. (2006). Barrel map development relies on protein kinase A regulatory subunit II beta-mediated cAMP signaling. J. Neurosci. 26, 4338-4349
20. Jeske, N. A., Diogenes, A., Ruparel, N. B., Fehrenbacher, J. C., Henry, M., Akopian, A. N. and Hargreaves, K. M. (2008). A-kinase anchoring protein mediates TRPV1 thermal hyperalgesia through PKA phosphorylation of TRPV1 Pain 138, 604-616
21. Ji, R. R., Kohno, T., Moore, K. A. and Woolf, C. J. (2003). Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26, 696-705
22. Kim, C., Cheng, C. Y., Saldanha, S. A. and Taylor, S. S. (2007). PKA-I holoenzyme structure reveals a mechanism for cAMP-dependent activation Cell 130, 1032-1043
23. Kim, H. Y., Lee, K. Y., Lu, Y., Wang, J., Cui, L., Kim, S. J., Chung, J. M. and Chung, K. (2011). Mitochondrial Ca(2+) uptake is essential for synaptic plasticity in pain. J. Neurosci. 31, 12982-12991
24. Koch, K. R. (2010). Parameter Estimation and Hypothesis Testing in Linear Models. Berlin: Springer-Verlag
25. Malmberg, A. B., Brandon, E. P., Idzerda, R. L., Liu, H., McKnight, G. S. and Basbaum, A. I. (1997). Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J. Neurosci. 17, 7462-7470
26. Manni, S., Mauban, J. H., Ward, C. W. and Bond, M. (2008). Phosphorylation of the cAMP-dependent protein kinase (PKA) regulatory subunit modulates PKAAKAP interaction, substrate phosphorylation, and calcium signaling in cardiac cells. J. Biol. Chem. 283, 24145-24154
27. Martin, B. R., Deerinck, T. J., Ellisman, M. H., Taylor, S. S. and Tsien, R. Y (2007). Isoform-specific PKA dynamics revealed by dye-triggered aggregation and DAKAP1alpha-mediated localization in living cells. Chem. Biol. 14, 1031-1042
28. Moriyama, T., Higashi, T., Togashi, K., Iida, T., Segi, E., Sugimoto, Y., Tominaga, T., Narumiya, S. and Tominaga, M. (2005). Sensitization of TRPV1 by EP1 and IP reveals peripheral nociceptive mechanism of prostaglandins Mol. Pain 1, 3
29. Murata, T., Ushikubi, F., Matsuoka, T., Hirata, M., Yamasaki, A., Sugimoto, Y., Ichikawa, A., Aze, Y., Tanaka, T., Yoshida, N. et al. (1997). Altered pain perception and inflammatory response in mice lacking prostacyclin receptor Nature 388, 678-682
30. Oliveria, S. F., Dell'Acqua, M. L. and Sather, W. A. (2007). AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 55, 261-275
31. Pidoux, G. and Taskén, K. (2010). Specificity and spatial dynamics of protein kinase A signaling organized by A-kinase-anchoring proteins. J. Mol Endocrinol. 44, 271-284
32. Pierre, S., Eschenhagen, T., Geisslinger, G. and Scholich, K. (2009). Capturing adenylyl cyclases as potential drug targets. Nat. Rev. Drug Discov. 8, 321-335
33. Prinz, A., Diskar, M., Erlbruch, A. and Herberg, F. W. (2006a). Novel, isotypespecific sensors for protein kinase A subunit interaction based on bioluminescence resonance energy transfer (BRET). Cell. Signal. 18, 1616-1625
34. Prinz, A., Diskar, M. and Herberg, F. W. (2006b). Application of bioluminescence resonance energy transfer (BRET) for biomolecular interaction studies ChemBioChem 7, 1007-1012
35. Pulichino, A. M., Rowland, S., Wu, T., Clark, P., Xu, D., Mathieu, M. C., Riendeau, D. and Audoly, L. P. (2006). Prostacyclin antagonism reduces pain and inflammation in rodent models of hyperalgesia and chronic arthritis J. Pharmacol. Exp. Ther. 319, 1043-1050
36. Rangel-Aldao, R. and Rosen, O. M. (1976). Dissociation and reassociation of the phosphorylated and nonphosphorylated forms of adenosine 39:59-monophosphate-dependent protein kinase from bovine cardiac muscle. J. Biol Chem. 251, 3375-3380
37. Rangel-Aldao, R., Kupiec, J. W. and Rosen, O. M. (1979). Resolution of the phosphorylated and dephosphorylated cAMP-binding proteins of bovine cardiac muscle by affinity labeling and two-dimensional electrophoresis. J. Biol. Chem 254, 2499-2508
38. Rao, Y., Fischer, Q. S., Yang, Y., McKnight, G. S., LaRue, A. and Daw, N. W (2004). Reduced ocular dominance plasticity and long-term potentiation in the developing visual cortex of protein kinase A RII alpha mutant mice. Eur. J Neurosci. 20, 837-842
39. Rathee, P. K., Distler, C., Obreja, O., Neuhuber, W., Wang, G. K., Wang, S. Y., Nau, C. and Kress, M. (2002). PKA/AKAP/VR-1 module: A common link of Gsmediated signaling to thermal hyperalgesia. J. Neurosci. 22, 4740-4745
40. Reinold, H., Ahmadi, S., Depner, U. B., Layh, B., Heindl, C., Hamza, M., Pahl, A., Brune, K., Narumiya, S., Müller, U. et al. (2005). Spinal inflammatory hyperalgesia is mediated by prostaglandin E receptors of the EP2 subtype J. Clin. Invest. 115, 673-679
41. Roederer, M. (2002). Compensation in flow cytometry. Curr. Protoc. Cytom. 22, 1.14.1-1.14.20
42. Schnizler, K., Shutov, L. P., Van Kanegan, M. J., Merrill, M. A., Nichols, B., McKnight, G. S., Strack, S., Hell, J. W. and Usachev, Y. M. (2008). Protein kinase A anchoring via AKAP150 is essential for TRPV1 modulation by forskolin and prostaglandin E2 in mouse sensory neurons. J. Neurosci. 28, 4904-4917
43. Taylor, S. S., Buechler, J. A. and Yonemoto, W. (1990). cAMP-dependent protein kinase: framework for a diverse family of regulatory enzymes. Annu Rev. Biochem. 59, 971-1005
44. Taylor, S. S., Ilouz, R., Zhang, P. and Kornev, A. P. (2012). Assembly of allosteric macromolecular switches: lessons from PKA. Nat. Rev. Mol. Cell Biol. 13, 646-658
45. Thiele, T. E., Willis, B., Stadler, J., Reynolds, J. G., Bernstein, I. L. and McKnight, G. S. (2000). High ethanol consumption and low sensitivity to ethanol-induced sedation in protein kinase A-mutant mice. J. Neurosci. 20, RC75
46. Vigil, D., Blumenthal, D. K., Taylor, S. S. and Trewhella, J. (2006). Solution scattering reveals large differences in the global structures of type II protein kinase A isoforms. J. Mol. Biol. 357, 880-889
47. Wang, C., Li, G. W. and Huang, L. Y. (2007). Prostaglandin E2 potentiation of P2X3 receptor mediated currents in dorsal root ganglion neurons. Mol. Pain 3, 22
48. Wu, J., Brown, S. H., von Daake, S. and Taylor, S. S. (2007). PKA type IIalpha holoenzyme reveals a combinatorial strategy for isoform diversity. Science 318, 274-279
49. Zhang, J., Hupfeld, C. J., Taylor, S. S., Olefsky, J. M. and Tsien, R. Y. (2005) Insulin disrupts beta-adrenergic signalling to protein kinase A in adipocytes Nature 437, 569-573
50. Zhang, X., Li, L. and McNaughton, P. A. (2008). Proinflammatory mediators modulate the heat-activated ion channel TRPV1 via the scaffolding protein AKAP79/150. Neuron 59, 450-461
51. Zhang, P., Smith-Nguyen, E. V., Keshwani, M. M., Deal, M. S., Kornev, A. P and Taylor, S. S. (2012). Structure and allostery of the PKA RIIβ tetrameric holoenzyme. Science 335, 712-716
52. Zimmermann, B., Chiorini, J. A., Ma, Y., Kotin, R. M. and Herberg, F. W. (1999) PrKX is a novel catalytic subunit of the cAMP-dependent protein kinase regulated by the regulatory subunit type I. J. Biol. Chem. 274, 5370-5378