Presynaptically localized cyclic GMP-dependent protein kinase 1 is a key determinant of spinal synaptic potentiation and pain hypersensitivity

PLoS Biology

Volumn 10, Issue 3, 2012, Pages

  Luo, Ceng ^a,b   Gangadharan, Vijayan ^a   Bali, Kiran Kumar ^a   Xie, Rou Gang ^b   Agarwal, Nitin ^a   Kurejova, Martina ^a   Tappe Theodor, Anke ^a   Tegeder, Irmgard ^c   Feil, Susanne ^d   Lewin, Gary ^e   Polgar, Erika ^f   Todd, Andrew J ^f   Schlossmann, Jens ^g,h   Hofmann, Franz ^g   Liu, Da Lu ^b   Hu, San Jue ^b   Feil, Robert ^d   Kuner, Thomas ^a   Kuner, Rohini ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^f UNIVERSITY OF GLASGOW   (United Kingdom)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^h UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR 1; MYOSIN LIGHT CHAIN KINASE; UNCLASSIFIED DRUG; 6 ANILINO 5,8 QUINOLINEQUINONE; 6-ANILINO-5,8-QUINOLINEDIONE; ACTIN BINDING PROTEIN; AMINOQUINOLINE DERIVATIVE; CELL ADHESION MOLECULE; CGMP DEPENDENT PROTEIN KINASE I; CGMP-DEPENDENT PROTEIN KINASE I; GUANYLATE CYCLASE; PHOSPHOPROTEIN; VASODILATOR STIMULATED PHOSPHOPROTEIN; VASODILATOR-STIMULATED PHOSPHOPROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; IN VIVO STUDY; LONG TERM POTENTIATION; MOUSE; NERVE CELL; NERVE CONDUCTION; NERVE ENDING; NEUROTRANSMITTER RELEASE; NOCICEPTION; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PROBABILITY; PROTEIN EXPRESSION; PROTEIN TARGETING; REGULATORY MECHANISM; SPINAL CORD; SPINAL SYNAPTIC POTENTIATION; SYNAPTIC TRANSMISSION; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYME SPECIFICITY; GENE DELETION; GENETICS; METABOLISM; MOUSE MUTANT; NERVE FIBER; NOCICEPTIVE RECEPTOR; PAIN; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPINAL GANGLION;

MUS;

AMINOQUINOLINES; ANIMALS; BEHAVIOR, ANIMAL; CELL ADHESION MOLECULES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GANGLIA, SPINAL; GENE DELETION; GUANYLATE CYCLASE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LONG-TERM POTENTIATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; NERVE FIBERS; NOCICEPTORS; PAIN; PATCH-CLAMP TECHNIQUES; PHOSPHOPROTEINS; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY; SYNAPTIC TRANSMISSION;

EID: 84858984769     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001283     Document Type: Article

References (49)

1. Basbaum A. I, Bautista D. M, Scherrer G, Julius D, (2009) Cellular and molecular mechanisms of pain. Cell 139: 267-284.
2. Sandkuhler J, (2009) Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 89: 707-758.
3. Woolf C. J, Salter M. W, (2000) Neuronal plasticity: increasing the gain in pain. Science 288: 1765-1769.
4. Ikeda H, Heinke B, Ruscheweyh R, Sandkuhler J, (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299: 1237-1240.
5. Ikeda H, Stark J, Fischer H, Wagner M, Drdla R, et al. (2006) Synaptic amplifier of inflammatory pain in the spinal dorsal horn. Science 312: 1659-1662.
6. Klein T, Magerl W, Hopf H. C, Sandkuhler J, Treede R. D, (2004) Perceptual correlates of nociceptive long-term potentiation and long-term depression in humans. J Neurosci 24: 964-971.
7. Sandkuhler J, (2007) Understanding LTP in pain pathways. Mol Pain 3: 9.
8. Hofmann F, Feil R, Kleppisch T, Schlossmann J, (2006) Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 86: 1-23.
9. Kaupp U. B, Seifert R, (2002) Cyclic nucleotide-gated ion channels. Physiol Rev 82: 769-824.
10. Schmidt H, Werner M, Heppenstall P. A, Henning M, More M. I, et al. (2002) cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159: 489-498.
11. Qian Y, Chao D. S, Santillano D. R, Cornwell T. L, Nairn A. C, et al. (1996) cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16: 3130-3138.
12. Feil R, Kleppisch T, (2008) NO/cGMP-dependent modulation of synaptic transmission. Handb Exp Pharmacol pp. 529-560.
13. Feil S, Zimmermann P, Knorn A, Brummer S, Schlossmann J, et al. (2005) Distribution of cGMP-dependent protein kinase type I and its isoforms in the mouse brain and retina. Neuroscience 135: 863-868.
14. Tegeder I, Del Turco D, Schmidtko A, Sausbier M, Feil R, et al. (2004) Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Natl Acad Sci U S A 101: 3253-3257.
15. Wegener J. W, Nawrath H, Wolfsgruber W, Kuhbandner S, Werner C, et al. (2002) cGMP-dependent protein kinase I mediates the negative inotropic effect of cGMP in the murine myocardium. Circ Res 90: 18-20.
16. Agarwal N, Offermanns S, Kuner R, (2004) Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38: 122-129.
17. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin C. E, et al. (2007) Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10: 870-879.
18. Schlossmann J, Ammendola A, Ashman K, Zong X, Huber A, et al. (2000) Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Ibeta. Nature 404: 197-201.
19. Pfeifer A, Klatt P, Massberg S, Ny L, Sausbier M, et al. (1998) Defective smooth muscle regulation in cGMP kinase I-deficient mice. EMBO J 17: 3045-3051.
20. Mantyh P. W, Allen C. J, Ghilardi J. R, Rogers S. D, Mantyh C. R, et al. (1995) Rapid endocytosis of a G protein-coupled receptor: substance P evoked internalization of its receptor in the rat striatum in vivo. Proc Natl Acad Sci U S A 92: 2622-2626.
21. Glass D. B, (1983) Differential responses of cyclic GMP-dependent and cyclic AMP-dependent protein kinases to synthetic peptide inhibitors. Biochem J 213: 159-164.
22. Wexler E. M, Stanton P. K, Nawy S, (1998) Nitric oxide depresses GABAA receptor function via coactivation of cGMP-dependent kinase and phosphodiesterase. J Neurosci 18: 2342-2349.
23. Yang X. F, Miao Y, Ping Y, Wu H. J, Yang X. L, et al. (2011) Melatonin inhibits tetraethylammonium-sensitive potassium channels of rod ON type bipolar cells via MT2 receptors in rat retina. Neuroscience 173: 19-29.
24. Ji R. R, Kohno T, Moore K. A, Woolf C. J, (2003) Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26: 696-705.
25. Voronin L. L, Cherubini E, (2004) 'Deaf, mute and whispering' silent synapses: their role in synaptic plasticity. J Physiol 557: 3-12.
26. Schulz P. E, Cook E. P, Johnston D, (1995) Using paired-pulse facilitation to probe the mechanisms for long-term potentiation (LTP). J Physiol Paris 89: 3-9.
27. Aszodi A, Pfeifer A, Ahmad M, Glauner M, Zhou X. H, et al. (1999) The vasodilator-stimulated phosphoprotein (VASP) is involved in cGMP- and cAMP-mediated inhibition of agonist-induced platelet aggregation, but is dispensable for smooth muscle function. EMBO J 18: 37-48.
28. Surks H. K, Mochizuki N, Kasai Y, Georgescu S. P, Tang K. M, et al. (1999) Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase Ialpha. Science 286: 1583-1587.
29. Komalavilas P, Lincoln T. M, (1994) Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase. J Biol Chem 269: 8701-8707.
30. Wagner L. E 2nd, Li W. H, Yule D. I, (2003) Phosphorylation of type-1 inositol 1,4,5-trisphosphate receptors by cyclic nucleotide-dependent protein kinases: a mutational analysis of the functionally important sites in the S2+ and S2- splice variants. J Biol Chem 278: 45811-45817.
31. Tjolsen A, Berge O. G, Hunskaar S, Rosland J. H, Hole K, (1992) The formalin test: an evaluation of the method. Pain 51: 5-17.
32. Gangadharan V, Wang R, Ulzhofer B, Luo C, Bardoni R, et al. (2011) Peripheral calcium-permeable AMPA receptors regulate chronic inflammatory pain in mice. J Clin Invest 121: 1608-1623.
33. Hartmann B, Ahmadi S, Heppenstall P. A, Lewin G. R, Schott C, et al. (2004) The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 44: 637-650.
34. Wetzel C, Hu J, Riethmacher D, Benckendorff A, Harder L, et al. (2007) A stomatin-domain protein essential for touch sensation in the mouse. Nature 445: 206-209.
35. Meyer R. A, Ringkamp M, Campbell J. N, Raja S. N, (2006) Peripheral mechanism of cutaneous nociception. In: McMahon S. B, Koltzenburg M, editors. Wall and Melzack's Textbook of Pain (Elsevier Churchill Livingstone) pp. 3-34.
36. Sluka K. A, Kalra A, Moore S. A, (2001) Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24: 37-46.
37. Kolhekar R, Meller S. T, Gebhart G. F, (1993) Characterization of the role of spinal N-methyl-D-aspartate receptors in thermal nociception in the rat. Neuroscience 57: 385-395.
38. Schmidtko A, Gao W, Konig P, Heine S, Motterlini R, et al. (2008) cGMP produced by NO-sensitive guanylyl cyclase essentially contributes to inflammatory and neuropathic pain by using targets different from cGMP-dependent protein kinase I. J Neurosci 28: 8568-8576.
39. Maihofner C, Euchenhofer C, Tegeder I, Beck K. F, Pfeilschifter J, et al. (2000) Regulation and immunhistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. Neurosci Lett 290: 71-75.
40. Ruscheweyh R, Goralczyk A, Wunderbaldinger G, Schober A, Sandkuhler J, (2006) Possible sources and sites of action of the nitric oxide involved in synaptic plasticity at spinal lamina I projection neurons. Neuroscience 141: 977-988.
41. Potter L. R, Abbey-Hosch S, Dickey D. M, (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27: 47-72.
42. Schmidt H, Stonkute A, Juttner R, Schaffer S, Buttgereit J, et al. (2007) The receptor guanylyl cyclase Npr2 is essential for sensory axon bifurcation within the spinal cord. J Cell Biol 179: 331-340.
43. Browning D. D, Mc Shane M, Marty C, Ye R. D, (2001) Functional analysis of type 1alpha cGMP-dependent protein kinase using green fluorescent fusion proteins. J Biol Chem 276: 13039-13048.
44. Engelman H. S, MacDermott A. B, (2004) Presynaptic ionotropic receptors and control of transmitter release. Nat Rev Neurosci 5: 135-145.
45. Emptage N. J, Reid C. A, Fine A, (2001) Calcium stores in hippocampal synaptic boutons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron 29: 197-208.
46. Zucker R. S, Regehr W. G, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
47. Ryan T. A, (1999) Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J Neurosci 19: 1317-1323.
48. Tokuoka H, Goda Y, (2006) Myosin light chain kinase is not a regulator of synaptic vesicle trafficking during repetitive exocytosis in cultured hippocampal neurons. J Neurosci 26: 11606-11614.
49. Schweizerhof M, Stosser S, Kurejova M, Njoo C, Gangadharan V, et al. (2009) Hematopoietic colony-stimulating factors mediate tumor-nerve interactions and bone cancer pain. Nat Med 15: 802-807.