Stimulation of deep somatic tissue with capsaicin produces long-lasting mechanical allodynia and heat hypoalgesia that depends on early activation of the cAMP pathway

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5687-5693

  Sluka, K A ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Adenylate cyclase; Analgesia; Joint; Muscle; Pain; Protein kinase A

Indexed keywords

8 BROMO CYCLIC AMP; ADENYLATE CYCLASE; CAPSAICIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; HEAT; HYPERALGESIA; HYPOALGESIA; INFLAMMATION; JOINT; MALE; MECHANICAL STIMULATION; MUSCLE; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; SKIN; SPINAL ANESTHESIA; SPINAL CORD;

EID: 0036662902     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05687.2002     Document Type: Article

References (59)

1. Anderson LE, Seybold VS (2000) Phosphorylated cAMP response element binding protein increases in neurokinin-1 receptor-immunoreactive neurons in rat spinal cord in response to formalin-induced nociception. Neurosci Lett 283:29-32.
2. Blackstone C, Murphy TH, Moss SJ, Baraban JM, Huganir RL (1995) Cyclic AMP and synaptic activity dependent phosphorylation of AMPA preferring glutamate receptors. J Neurosci 14:7585-7593.
3. Cerne R, Jiang M, Randic M (1992) Cyclic adenosine 3′5′monophosphate potentiates excitatory amino acid and synaptic responses of rat spinal dorsal horn neurons. Brain Res 596:111-123.
4. Cerne R, Rusin KI, Randic M (1993) Enhancement of the N-methyl-D-aspartate response in spinal dorsal horn neurons by cAMP-dependent protein kinase. Neurosci Lett 161:124-128.
5. Coderre TJ, Van Empel I (1994) The utility of excitatory amino acid (EAA) antagonists as analgesic agents. I. Comparison of the antinociceptive activity of various classes of EAA antagonists in mechanical, thermal, and chemical nociceptive tests. Pain 59:345-352.
6. Craig AD, Hepplemann B, Schaible H-G (1988) The projection of the medial and posterior articular nerves of the cat's knee to the spinal cord. J Comp Neurol 276:279-288.
7. 2+/calmodulin as well as cAMP-dependent protein kinase. Proc Natl Acad Sci USA 88:5061-5065.
8. Desser RK, Himmelhoch SR, Evans WH, Januska M, Mage M, Shelton E (1972) Heterophil and eosinophil peroxidase. Arch Biochem Biophys 148:452-465.
9. Dolan S, Nolan AM (2001) Biphasic modulation of nociceptive processing by the cyclic AMP-protein kinase A signalling pathway in sheep spinal cord. Neurosci Lett 309:157-160.
10. Dougherty PM, Willis WD, Lenz FA (1998) Transient inhibition of responses to thermal stimuli of spinal sensory tract neurons in monkeys during sensitization by intradermal capsaicin. Pain 77:129-136.
11. Gopalkrishnan P, Sluka KA (2000) Effect of varying frequency, intensity and pulse duration of TENS on primary hyperalgesia in inflamed rats. Arch Phys Med Rehabil 81:984-990.
12. Greene EC (1963) Anatomy of the Rat, Vol XXVII. New York: Hafner.
13. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new, sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
14. Hell JW, Yokoyama CT, Breeze LJ, Chavkin C, Catterall WA (1995) Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP dependent protein kinase in hippocampal neurons. EMBO J 14:3036-3044.
15. Ji RR, Rupp F (1997) Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: Relationship to c-fos induction. J Neurosci 17:1776-1785.
16. Ji RR, Brenner GJ, Schmoll R, Baba H, Woolf CJ (2000) Phosphorylation of transcription factor CREB in nociceptive neurons after noxious stimulation. Proceedings of the Ninth World Congress on Pain 16:1776-1785.
17. Kellgren JH (1938) Observations on referred pain arising from muscle. Clin Sci 3:175-190.
18. Lamotte RH, Shain CN, Simone DA, Tsai EFP (1991) Neurogenic hyperalgesia: Psychophysical studies of underlying mechanisms. J Neurophysiol 66:190-211.
19. Liu L, Oortgiesen M, Li L, Simon SA (2001) Capsaicin inhibits activation of voltage-gated sodium currents in capsaicin-sensitive trigeminal ganglion neurons. J Neurophysiol 85:745-758.
20. Ma W, Quirion R (2001) Increased phosphorylation of cyclic AMP response element-binding protein (CREB) in the superficial dorsal horn neurons following partial sciatic nerve ligation. Pain 93:295-301.
21. Malmberg AB, Brandon EP, Idzerda RL, Liu H, McKnight GS, Basbaum AI (1997a) 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.
22. Malmberg AB, Chen C, Tonegawa S, Basbaum AI (1997b) Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 278:279-283.
23. Marchettini P, Cline M, Ochoa J (1990) Innervation territories for touch and pain afferents of single fascicles of the human ulnar nerve. Brain 113:1491-1500.
24. Marchettini P, Simone DA, Caputi G, Ochoa JL (1996) Pain from excitation of identified muscle nociceptors in humans. Brain Res 75:109-116.
25. Mense S (1993) Nociception from skeletal muscle in relation to clinical muscle pain. Pain 54:241-289.
26. Mense S, Craig AD (1988) Spinal and supraspinal terminations of primary afferent fibers from the gastrocnemius-soleus muscle in the cat. Neuroscience 26:1023-1035.
27. Messersmith DJ, Kim DJ, Gu J, Dubner R, Iadarola MJ (1996) c-Jun activation of the DYNCRE3 site in the prodynorphin promoter. Brain Res Mol Brain Res 40:15-21.
28. O'Brien C, Woolf CJ, Fitzgerald M, Lindsay RM, Molander C (1989) Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience 32:493-502.
29. Ochoa J, Torebjork E (1983) Sensations by intraneuronal microstimulation of single mechanoreceptor units innervating the human hand. J Physiol (Lond) 73:633-654.
30. Ochoa J, Torebjork E (1989) Sensations evoked by intraneural microstimulation of C nociceptor fibres in human skin nerves. J Physiol (Lond) 415:583-599.
31. Ohtori S, Takahashi K, Chiba T, Takahashi Y, Yamagata M, Sameda H, Moriya H (2000) Fos expression in the rat brain and spinal cord evoked by noxious stimulation to low back muscle and skin. Spine 25:2425-2430.
32. Plenderleith MB, Snow PJ (1993) The plant lectin Bandeiraea simplicifolia I-B4 identifies a subpopulation of small diameter primary sensory neurones which innervate the skin in the rat. Neurosci Lett 159:17-20.
33. Pogatzki EM, Zahn PK, Brennan TJ (2000) Effect of pretreatment with intrathecal excitatory amino acid receptor antagonists on the development of pain behavior caused by plantar incision. Anesthesiology 93:489-496.
34. Raja SN, Campbell JN, Meyer RA (1984) Evidence for different mechanisms of primary and secondary hyperalgesia following heat injury to the glaborous skin. Brain 107:1179-1188.
35. Recio MC, Giner RM, Uriburu L, Manez S, Cerda M, DelaFuents JR, Rios JL (2000) In vivo activity of pseudoguaianolide sesquiterpene lactones in acute and chronic inflammation. Life Sci 66:2509-2518.
36. Reifen R, Nur T, Matas Z, Halpern Z (2001) Lycopene supplementation attenuates the inflammatory status of colitis in a rat model. Int J Vitam Nutr Res 71:347-351.
37. Schaible H-G, Grubb BD (1993) Afferent and spinal mechanisms of joint pain. Pain 55:5-54.
38. Shaywitz AJ, Greenberg ME (1999) CREB: A stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 68:821-861.
39. Simone DA, Baumann TK, Lamotte RH (1989) Dose dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 38:99-107.
40. Simone DA, Sorkin LS, Oh U, Chung JM, Owens C, Lamotte RH, Willis WD (1991) Neurogenic hyperalgesia: Central neural correlates in responses of spinothalamic tract neurons. J Neurophysiol 66:228-246.
41. Simone DA, Marchettini P, Caputi G, Ochoa JL (1994) Identification of muscle afferents subserving sensation of deep pain in humans. J Neurophysiol 72:883-889.
42. Sluka KA (1997) The role of the cyclic AMP transduction cascade in mechanical allodynia and hyperalgesia induced by intradermal injection of capsaicin in rats. Br J Pharmacol 122:1165-1173.
43. Sluka KA (2000) Development and time course of secondary heat and mechanical hyperalgesia following capsaicin or carrageenan injection of muscle, joint or skin. Soc Neurosci Abstr 26:2192.
44. Sluka KA, Willis WD (1997) The effects of G-protein and protein kinase inhibitors on the behavioral responses of rats to intradermal injection of capsaicin. Pain 71:165-178.
45. Sluka KA, Willis WD (1998) Increased release of excitatory amino acids following intradermal injection of capsaicin is reduced by a protein kinase G inhibitor. Brain Res 798:281-286.
46. Sluka KA, Rees H, Chen PS, Tsuruoka M, Willis WD (1997) Inhibitors of G-proteins and protein kinases reduce the sensitization of spinothalamic tract neurons following intradermal injection of capsaicin in the primate. Exp Brain Res 115:15-24.
47. Sluka KA, Christy MR, Peterson WL, Rudd SL, Troy SM (1999) Reduction of pain-related behaviors with either cold or heat treatment in an animal model of acute arthritis. Arch Phys Med Rehab 80:313-317.
48. Sluka KA, Kalra A, Moore SA (2001) Unilateral intramuscular injections of acidic saline produce a bilateral, long-lasting hyperalgesia. Muscle Nerve 24:37-46.
49. Storkson RV, Kjorsvik A, Tjolsen A, Hole K (1996) Lumbar catheterization of the spinal subarachnoid space in the rat. J Neurosci Methods 65:167-172.
50. Svensson P, Beydoun A, Morrow TJ, Casey KL (1997) Human intramuscular and cutaneous pain: Psychophysical comparisons. Exp Brain Res 114:390-392.
51. Sweatt JD (1999) Toward a molecular explanation for long-term potentiation. Learn Mem 6:399-416.
52. Vazquez SI, Vazquez A, Pena DO (2000) Different hippocampal activity profiles for PKA and PKC in spatial discrimination learning. Behav Neurosci 114:1109-1118.
53. Wall PD, Woolf CJ (1984) Muscle but not cutaneous C-afferent input produces prolonged increases in the excitability of the flexion reflex in the rat. J Physiol (Lond) 356:443-458.
54. Willis WD, Coggeshall RE (1991) Sensory Mechanisms of the Spinal Cord. New York: Plenum.
55. Witting N, Svensson P, Gottrup H, Arendt-Nielsen L, Jensen TS (2000) Intramuscular and intradermal injection of capsaicin: A comparison of local and referred pain. Pain 84:407-412.
56. Wong ST, Athos J, Figueroa XA, Pineda VV, Schaefer ML, Chavkin CC, Muglia LJ, Storm DR (1999) Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP. Neuron 23:787-798.
57. Xia Z, Storm DR (1997) Calmodulin-regulated adenylyl cyclases and neuromodulation. Curr Opin Neurobiol 7:391-396.
58. Zahn PK, Brennan TJ (1998) Lack of effect of intrathecally administered N-methyl-D-aspartate receptor antagonists in a rat model of postoperative pain. Anesthesiology 88:143-156.
59. Zou X, Lin Q, Willis WD (2000) Enhanced phosphorylation of NMDA receptor 1 subunits in spinal cord dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats. J Neurosci 20:6989-6997.