Inhibiting spinal neuron-astrocytic activation correlates with synergistic analgesia of dexmedetomidine and ropivacaine

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Wu, Huang Hui ^a   Yin, Jun Bin ^b   Zhang, Ting ^b   Cui, Yuan Yuan ^b   Dong, Yu Lin ^b   Chen, Guo Zhong ^a   Wang, Wen ^b  

^a FUZHOU GENERAL HOSPITAL   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; DEXMEDETOMIDINE; FREUND ADJUVANT; GLIAL FIBRILLARY ACIDIC PROTEIN; ROPIVACAINE; AMIDE;

ANALGESIA; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CHRONIC PAIN; CONTROLLED STUDY; DOWN REGULATION; DRUG POTENTIATION; IMMUNOHISTOCHEMISTRY; INFLAMMATORY PAIN; MALE; NONHUMAN; RAT; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; THERMAL STIMULATION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; INTRASPINAL DRUG ADMINISTRATION; NERVE CELL; PROCEDURES; SPRAGUE DAWLEY RAT;

AMIDES; ANALGESIA; ANIMALS; ASTROCYTES; CHRONIC PAIN; DEXMEDETOMIDINE; DRUG SYNERGISM; FREUND'S ADJUVANT; GLIAL FIBRILLARY ACIDIC PROTEIN; INJECTIONS, SPINAL; MALE; NEURONS; RATS, SPRAGUE-DAWLEY; SPINAL CORD DORSAL HORN;

EID: 84899096633     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092374     Document Type: Article

References (66)

1. Jones L, Othman M, Dowswell T, Alfirevic Z, Gates S, et al. (2012) Pain management for women in labour: an overview of systematic reviews. Cochrane database of systematic reviews 3: CD009234.
2. Simmons SW, Taghizadeh N, Dennis AT, Hughes D, Cyna AM (2012) Combined spinal-epidural versus epidural analgesia in labour. Cochrane database of systematic reviews 10: CD003401.
3. Nishimori M, Low JH, Zheng H, Ballantyne JC (2012) Epidural pain relief versus systemic opioid-based pain relief for abdominal aortic surgery. Cochrane database of systematic reviews 7: CD005059.
4. Gandhi K, Baratta JL, Heitz JW, Schwenk ES, Vaghari B, et al. (2012) Acute pain management in the postanesthesia care unit. Anesthesiology clinics 30: e1-15.
5. Dadure C, Capdevila X (2012) Peripheral catheter techniques. Paediatric anaesthesia 22: 93-101.
6. Goldman JA (1958) A rare toxic effect of local anaesthesia with lignocaine; a case report. British journal of anaesthesia 30: 377-379.
7. Perrott DH (2008) Anesthesia outside the operating room in the office-based setting. Current opinion in anaesthesiology 21: 480-485.
8. Harsten A, Kehlet H, Toksvig-Larsen S (2013) Recovery after total intravenous general anaesthesia or spinal anaesthesia for total knee arthroplasty: a randomized trial. British journal of anaesthesia.
9. Zhong Z, Qulian G, Yuan Z, Wangyuan Z, Zhihua S (2009) Repeated intrathecal administration of ropivacaine causes neurotoxicity in rats. Anaesthesia and intensive care 37: 929-936.
10. Sun ZH, Xu XP, Song ZB, Zhang Z, Wang N, et al. (2012) Repeated intrathecal administration of ropivacaine causes neurotoxicity in rats. Anaesthesia and intensive care 40: 825-831.
11. Sun Z, Liu H, Guo Q, Xu X, Zhang Z, et al. (2012) In vivo and in vitro evidence of the neurotoxic effects of ropivacaine: the role of the Akt signaling pathway. Molecular medicine reports 6: 1455-1459.
12. Ihmsen H, Saari TI (2012) [Dexmedetomidine. Pharmacokinetics and pharmacodynamics]. Der Anaesthesist 61: 1059-1066.
13. Stone LS, Broberger C, Vulchanova L, Wilcox GL, Hokfelt T, et al. (1998) Differential distribution of alpha2A and alpha2C adrenergic receptor immuno-reactivity in the rat spinal cord. The Journal of neuroscience : the official journal of the Society for Neuroscience 18: 5928-5937.
14. Mori K, Ozaki E, Zhang B, Yang L, Yokoyama A, et al. (2002) Effects of norepinephrine on rat cultured microglial cells that express alpha1, alpha2, beta1 and beta2 adrenergic receptors. Neuropharmacology 43: 1026-1034. (Pubitemid 35341238)
15. Toda S, Sakai A, Ikeda Y, Sakamoto A, Suzuki H (2011) A local anesthetic, ropivacaine, suppresses activated microglia via a nerve growth factor-dependent mechanism and astrocytes via a nerve growth factor-independent mechanism in neuropathic pain. Molecular pain 7: 2.
16. Chichorro JG, Lorenzetti BB, Zampronio AR (2004) Involvement of bradykinin, cytokines, sympathetic amines and prostaglandins in formalin-induced orofacial nociception in rats. British journal of pharmacology 141: 1175-1184. (Pubitemid 38582255)
17. Scholz J, Woolf CJ (2007) The neuropathic pain triad: neurons, immune cells and glia. Nature neuroscience 10: 1361-1368. (Pubitemid 350014681)
18. Li X, Eisenach JC (2001) alpha2A-adrenoceptor stimulation reduces capsaicin-induced glutamate release from spinal cord synaptosomes. The Journal of pharmacology and experimental therapeutics 299: 939-944. (Pubitemid 33104963)
19. Mei X, Wang W, Wang W, Li Y, Zhang H, et al. (2009) Inhibiting astrocytic activation: a novel analgesic mechanism of ketamine at the spinal level? Journal of neurochemistry 109: 1691-1700.
20. Mei XP, Wang W, Wang W, Zhu C, Chen L, et al. (2010) Combining ketamine with astrocytic inhibitor as a potential analgesic strategy for neuropathic pain ketamine, astrocytic inhibitor and pain. Molecular pain 6: 50.
21. Mei XP, Zhang H, Wang W, Wei YY, Zhai MZ, et al. (2011) Inhibition of spinal astrocytic c-Jun N-terminal kinase (JNK) activation correlates with the analgesic effects of ketamine in neuropathic pain. Journal of neuroinflammation 8: 6.
22. Mei XP, Zhou Y, Wang W, Tang J, Wang W, et al. (2011) Ketamine depresses toll-like receptor 3 signaling in spinal microglia in a rat model of neuropathic pain. Neuro-Signals 19: 44-53.
23. Wang W, Wang W, Mei X, Huang J, Wei Y, et al. (2009) Crosstalk between spinal astrocytes and neurons in nerve injury-induced neuropathic pain. PloS one 4: e6973.
24. Wang W, Wang W, Wang Y, Huang J, Wu S, et al. (2008) Temporal changes of astrocyte activation and glutamate transporter-1 expression in the spinal cord after spinal nerve ligation-induced neuropathic pain. Anatomical record 291: 513-518. (Pubitemid 351644525)
25. Liu L, Ji F, Liang J, He H, Fu Y, et al. (2012) Inhibition by dexmedetomidine of the activation of spinal dorsal horn glias and the intracellular ERK signaling pathway induced by nerve injury. Brain research 1427: 1-9.
26. Xu B, Zhang WS, Yang JL, Lu N, Deng XM, et al. (2010) Evidence for suppression of spinal glial activation by dexmedetomidine in a rat model of monoarthritis. Clinical and experimental pharmacology & physiology 37: e158-166.
27. Bourgoin S, Pohl M, Mauborgne A, Benoliel JJ, Collin E, et al. (1993) Monoaminergic control of the release of calcitonin gene-related peptide- and substance P-like materials from rat spinal cord slices. Neuropharmacology 32: 633-640. (Pubitemid 23180108)
28. Holz GGt, Kream RM, Spiegel A, Dunlap K (1989) G proteins couple alpha-adrenergic and GABAb receptors to inhibition of peptide secretion from peripheral sensory neurons. The Journal of neuroscience : the official journal of the Society for Neuroscience 9: 657-666.
29. Zimmermann M (1983) Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16: 109-110.
30. Kimura M, Saito S, Obata H (2012) Dexmedetomidine decreases hyperalgesia in neuropathic pain by increasing acetylcholine in the spinal cord. Neuroscience letters 529: 70-74.
31. Zhang H, Zhou F, Li C, Kong M, Liu H, et al. (2013) Molecular mechanisms underlying the analgesic property of intrathecal dexmedetomidine and its neurotoxicity evaluation: an in vivo and in vitro experimental study. PloS one 8: e55556.
32. Guo BL, Sui BD, Wang XY, Wei YY, Huang J, et al. (2013) Significant changes in mitochondrial distribution in different pain models of mice. Mitochondrion 13: 292-297.
33. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88.
34. Zhuang ZY, Gerner P, Woolf CJ, Ji RR (2005) ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 114: 149-159. (Pubitemid 40279096)
35. Tallarida RJ (2001) Drug synergism: its detection and applications. The Journal of pharmacology and experimental therapeutics 298: 865-872.
36. Sun YH, Dong YL, Wang YT, Zhao GL, Lu GJ, et al. (2013) Synergistic Analgesia of Duloxetine and Celecoxib in the Mouse Formalin Test: A Combination Analysis. PloS one 8: e76603.
37. Bai L, Wang W, Dong YL, Wang W, Huang J, et al. (2012) Attenuation of mouse somatic and emotional inflammatory pain by hydralazine through scavenging acrolein and inhibiting neuronal activation. Pain physician 15: 311-326.
38. Liang L, Tao B, Fan L, Yaster M, Zhang Y, et al. (2013) mTOR and its downstream pathway are activated in the dorsal root ganglion and spinal cord after peripheral inflammation, but not after nerve injury. Brain research 1513: 17-25.
39. Yaster M, Guan X, Petralia RS, Rothstein JD, Lu W, et al. (2011) Effect of inhibition of spinal cord glutamate transporters on inflammatory pain induced by formalin and complete Freund's adjuvant. Anesthesiology 114: 412-423.
40. Katsura H, Obata K, Miyoshi K, Kondo T, Yamanaka H, et al. (2008) Transforming growth factor-activated kinase 1 induced in spinal astrocytes contributes to mechanical hypersensitivity after nerve injury. Glia 56: 723-733.
41. Zhuang ZY, Wen YR, Zhang DR, Borsello T, Bonny C, et al. (2006) A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. The Journal of neuroscience : the official journal of the Society for Neuroscience 26: 3551-3560.
42. Wirkner K, Gunther A, Weber M, Guzman SJ, Krause T, et al. (2007) Modulation of NMDA receptor current in layer V pyramidal neurons of the rat prefrontal cortex by P2Y receptor activation. Cerebral cortex 17: 621-631.
43. Jourdain P, Bergersen LH, Bhaukaurally K, Bezzi P, Santello M, et al. (2007) Glutamate exocytosis from astrocytes controls synaptic strength. Nature neuroscience 10: 331-339.
44. Oka M, Wada M, Wu Q, Yamamoto A, Fujita T (2006) Functional expression of metabotropic GABAB receptors in primary cultures of astrocytes from rat cerebral cortex. Biochemical and biophysical research communications 341: 874-881. (Pubitemid 43177570)
45. Thorlin T, Eriksson PS, Persson PA, Aberg ND, Hansson E, et al. (1998) Delta-opioid receptors on astroglial cells in primary culture: mobilization of intracellular free calcium via a pertussis sensitive G protein. Neuropharmacology 37: 299-311. (Pubitemid 28282635)
46. Guo W, Wang H, Watanabe M, Shimizu K, Zou S, et al. (2007) Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain. The Journal of neuroscience : the official journal of the Society for Neuroscience 27: 6006-6018.
47. Suter MR, Wen YR, Decosterd I, Ji RR (2007) Do glial cells control pain? Neuron glia biology 3: 255-268. (Pubitemid 351594231)
48. Watkins LR, Milligan ED, Maier SF (2001) Glial activation: a driving force for pathological pain. Trends in neurosciences 24: 450-455. (Pubitemid 32695356)
49. Werdehausen R, Fazeli S, Braun S, Hermanns H, Essmann F, et al. (2009) Apoptosis induction by different local anaesthetics in a neuroblastoma cell line. British journal of anaesthesia 103: 711-718.
50. Sites BD, Taenzer AH, Herrick MD, Gilloon C, Antonakakis J, et al. (2012) Incidence of local anesthetic systemic toxicity and postoperative neurologic symptoms associated with 12,668 ultrasound-guided nerve blocks: an analysis from a prospective clinical registry. Regional anesthesia and pain medicine 37: 478-482.
51. Yan M, Dai H, Ding T, Dai A, Zhang F, et al. (2011) Effects of dexmedetomidine on the release of glial cell line-derived neurotrophic factor from rat astrocyte cells. Neurochemistry international 58: 549-557.
52. Bruzzone A, Pinero CP, Castillo LF, Sarappa MG, Rojas P, et al. (2008) Alpha2-adrenoceptor action on cell proliferation and mammary tumour growth in mice. British journal of pharmacology 155: 494-504.
53. Sanders RD, Sun P, Patel S, Li M, Maze M, et al. (2010) Dexmedetomidine provides cortical neuroprotection: impact on anaesthetic-induced neuroapoptosis in the rat developing brain. Acta anaesthesiologica Scandinavica 54: 710-716.
54. Grosu I, Lavand'homme P (2010) Use of dexmedetomidine for pain control. F1000 medicine reports 2: 90.
55. Huang R, Hertz L (2000) Receptor subtype and dose dependence of dexmedetomidine-induced accumulation of [14C]glutamine in astrocytes suggests glial involvement in its hypnotic-sedative and anesthetic-sparing effects. Brain research 873: 297-301. (Pubitemid 30619056)
56. Li SS, Zhang WS, Yang JL, Xiong YC, Zhang YQ, et al. (2013) Involvement of protein kinase B/Akt in analgesic effect of dexmedetomidine on neuropathic pain. CNS neuroscience & therapeutics 19: 364-366.
57. Yuan X, Wu J, Wang Q, Xu M (2013) The antinociceptive effect of systemic administration of a combination of low-dose tramadol and dexmedetomidine in a rat model of bone cancer pain. European journal of anaesthesiology.
58. Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 22: 659-661.
59. Abbott FV, Grimes RW, Melzack R (1984) Single nerve capsaicin: effects on pain and morphine analgesia in the formalin and foot-flick tests. Brain research 295: 77-84. (Pubitemid 14155857)
60. Gupta R, Verma R, Bogra J, Kohli M, Raman R, et al. (2011) A Comparative study of intrathecal dexmedetomidine and fentanyl as adjuvants to Bupivacaine. Journal of anaesthesiology, clinical pharmacology 27: 339-343.
61. Gupta R, Bogra J, Verma R, Kohli M, Kushwaha JK, et al. (2011) Dexmedetomidine as an intrathecal adjuvant for postoperative analgesia. Indian journal of anaesthesia 55: 347-351.
62. Solanki SL, Bharti N, Batra YK, Jain A, Kumar P, et al. (2013) The analgesic effect of intrathecal dexmedetomidine or clonidine, with bupivacaine, in trauma patients undergoing lower limb surgery: a randomised, double-blind study. Anaesthesia and intensive care 41: 51-56.
63. Mohamed AA, Fares KM, Mohamed SA (2012) Efficacy of intrathecally administered dexmedetomidine versus dexmedetomidine with fentanyl in patients undergoing major abdominal cancer surgery. Pain physician 15: 339-348.
64. Shukla D, Verma A, Agarwal A, Pandey HD, Tyagi C (2011) Comparative study of intrathecal dexmedetomidine with intrathecal magnesium sulfate used as adjuvants to bupivacaine. Journal of anaesthesiology, clinical pharmacology 27: 495-499.
65. Al-Mustafa MM, Abu-Halaweh SA, Aloweidi AS, Murshidi MM, Ammari BA, et al. (2009) Effect of dexmedetomidine added to spinal bupivacaine for urological procedures. Saudi medical journal 30: 365-370.
66. Kanazi GE, Aouad MT, Jabbour-Khoury SI, Al Jazzar MD, Alameddine MM, et al. (2006) Effect of low-dose dexmedetomidine or clonidine on the characteristics of bupivacaine spinal block. Acta anaesthesiologica Scandinavica 50: 222-227. (Pubitemid 43340856)