Behavioral and anatomical characterization of the bilateral sciatic nerve chronic constriction (bCCI) injury: Correlation of anatomic changes and responses to cold stimuli

Molecular Pain

Volumn 6, Issue , 2010, Pages

  Datta, Sukdeb ^a,b   Chatterjee, Koel ^b   Kline IV, Robert H ^b   Wiley, Ronald G ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETONE; CHOLECYSTOKININ; MU OPIATE RECEPTOR; NEUROKININ 1 RECEPTOR; NEUROPEPTIDE Y; PEROXIDASE; SUBSTANCE P; ANALGESIC AGENT; BIOLOGICAL MARKER;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; COLD SENSITIVITY; COLD STRESS; CONTROLLED STUDY; EXPERIMENTAL TEST; FEMALE; FOLLOW UP; IMMUNOHISTOCHEMISTRY; MECHANICAL PROBE; MECHANICAL STIMULATION; NERVE INJURY; NERVE LIGATION; NEUROANATOMY; NEUROPATHIC PAIN; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT; SCIATIC NERVE; SPINAL CORD DORSAL HORN; WITHDRAWAL REFLEX; ANIMAL; CHRONIC DISEASE; COLD; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; HEMISPHERIC DOMINANCE; HYPERALGESIA; LIGATION; METABOLISM; METHODOLOGY; PAIN ASSESSMENT; PAIN THRESHOLD; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PHYSIOLOGY; POSTERIOR HORN CELL; PREDICTION AND FORECASTING; REFLEX; SCIATIC NEUROPATHY; SPRAGUE DAWLEY RAT;

ACETONE; ANALGESICS; ANIMALS; BIOLOGICAL MARKERS; CHOLECYSTOKININ; CHRONIC DISEASE; COLD TEMPERATURE; DISEASE MODELS, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; LIGATION; NEUROPEPTIDE Y; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVOUS SYSTEM DISEASES; POSTERIOR HORN CELLS; PREDICTIVE VALUE OF TESTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; RECEPTORS, OPIOID, MU; REFLEX; SCIATIC NEUROPATHY;

EID: 77349110489     PISSN: 17448069     EISSN: None     Source Type: Journal    
DOI: 10.1186/1744-8069-6-7     Document Type: Article

References (76)

1. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107. 10.1016/0304-3959(88)90209-6, 2837713.
2. Hansson P. Difficulties in stratifying neuropathic pain by mechanisms. Eur J Pain 2003, 7:353-7. 10.1016/S1090-3801(03)00051-X, 12821406.
3. Blackburn-Munro G. Pain-like behaviours in animals - how human are they?. Trends Pharmacol Sci 2004, 25:299-305. 10.1016/j.tips.2004.04.008, 15165744.
4. Jorum E, Warncke T, Stubhaug A. Cold allodynia and hyperalgesia in neuropathic pain: the effect of N-methyl-D-aspartate (NMDA) receptor antagonist ketamine--a double-blind, cross-over comparison with alfentanil and placebo. Pain 2003, 101:229-35. 10.1016/S0304-3959(02)00122-7, 12583865.
5. Gottrup H, Andersen J, Arendt-Nielsen L, Jensen TS. Psychophysical examination in patients with post-mastectomy pain. Pain 2000, 87:275-84. 10.1016/S0304-3959(00)00291-8, 10963907.
6. Vierck CJ, Acosta-Rua AJ, Johnson RD. Bilateral chronic constriction of the sciatic nerve: a model of long-term cold hyperalgesia. J Pain 2005, 6:507-17. 10.1016/j.jpain.2005.03.003, 16084465.
7. DeLeo JA, Rutkowski MD. Gender differences in rat neuropathic pain sensitivity is dependent on strain. Neurosci Lett 2000, 282:197-9. 10.1016/S0304-3940(00)00880-6, 10717425.
8. Lee DH, Chung K, Chung JM. Strain differences in adrenergic sensitivity of neuropathic pain behaviors in an experimental rat model. Neuroreport 1997, 8:3453-6.
9. Xu XJ, Plesan A, Yu W, Hao JX, Wiesenfeld-Hallin Z. Possible impact of genetic differences on the development of neuropathic pain-like behaviors after unilateral sciatic nerve ischemic injury in rats. Pain 2001, 89:135-45. 10.1016/S0304-3959(00)00356-0, 11166469.
10. Shir Y, Zeltser R, Vatine JJ, Carmi G, Belfer I, Zangen A, Overstreet D, Raber P, Seltzer Z. Correlation of intact sensibility and neuropathic pain-related behaviors in eight inbred and outbred rat strains and selection lines. Pain 2001, 90:75-82. 10.1016/S0304-3959(00)00388-2, 11166972.
11. Shir Y, Seltzer Z. Heat hyperalgesia following partial sciatic ligation in rats: interacting nature and nurture. Neuroreport 2001, 12:809-13. 10.1097/00001756-200103260-00038, 11277588.
12. Vendruscolo LF, Pamplona FA, Takahashi RN. Strain and sex differences in the expression of nociceptive behavior and stress-induced analgesia in rats. Brain Res 2004, 1030:277-83. 10.1016/j.brainres.2004.10.016, 15571676.
13. Benoliel R, Eliav E, Tal M. Strain-dependent modification of neuropathic pain behaviour in the rat hindpaw by a priming painful trigeminal nerve injury. Pain 2002, 97:203-12. 10.1016/S0304-3959(01)00428-6, 12044617.
14. Stiller CO, Cui JG, O'Connor WT, Brodin E, Meyerson BA, Linderoth B. Release of gamma-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 1996, 39:367-74. discussion 74-5, 10.1097/00006123-199608000-00026, 8832675.
15. Kajander KC, Wakisaka S, Bennett GJ. Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat. Neurosci Lett 1992, 138:225-8. 10.1016/0304-3940(92)90920-3, 1319012.
16. Cameron AA, Cliffer KD, Dougherty PM, Garrison CJ, Willis WD, Carlton SM. Time course of degenerative and regenerative changes in the dorsal horn in a rat model of peripheral neuropathy. J Comp Neurol 1997, 379:428-42. 10.1002/(SICI)1096-9861(19970317)379:3<428::AID-CNE8>3.0.CO;2-5, 9067834.
17. Xu XJ, Puke MJ, Verge VM, Wiesenfeld-Hallin Z, Hughes J, Hokfelt T. Up-regulation of cholecystokinin in primary sensory neurons is associated with morphine insensitivity in experimental neuropathic pain in the rat. Neurosci Lett 1993, 152:129-32. 10.1016/0304-3940(93)90500-K, 8515864.
18. Ossipov MH, Lopez Y, Nichols ML, Bian D, Porreca F. Inhibition by spinal morphine of the tail-flick response is attenuated in rats with nerve ligation injury. Neurosci Lett 1995, 199:83-6. 10.1016/0304-3940(95)12026-Z, 8584249.
19. Bian D, Nichols ML, Ossipov MH, Lai J, Porreca F. Characterization of the antiallodynic efficacy of morphine in a model of neuropathic pain in rats. Neuroreport 1995, 6:1981-4. 10.1097/00001756-199510010-00007, 8580422.
20. Porreca F, Tang QB, Bian D, Riedl M, Elde R, Lai J. Spinal opioid mu receptor expression in lumbar spinal cord of rats following nerve injury. Brain Res 1998, 795:197-203. 10.1016/S0006-8993(98)00292-3, 9622629.
21. Zhang X, Bao L, Xu ZQ, Kopp J, Arvidsson U, Elde R, Hokfelt T. Localization of neuropeptide Y Y1 receptors in the rat nervous system with special reference to somatic receptors on small dorsal root ganglion neurons. Proc Natl Acad Sci USA 1994, 91:1738-42.
22. Xu IS, Hao JX, Xu XJ, Hokfelt T, Wiesenfeld-Hallin Z. The effect of intrathecal selective agonists of Y1 and Y2 neuropeptide Y receptors on the flexor reflex in normal and axotomized rats. Brain Res 1999, 833:251-7. 10.1016/S0006-8993(99)01551-6, 10375701.
23. Xu XJ, Hao JX, Hokfelt T, Wiesenfeld-Hallin Z. The effects of intrathecal neuropeptide Y on the spinal nociceptive flexor reflex in rats with intact sciatic nerves and after peripheral axotomy. Neuroscience 1994, 63:817-26. 10.1016/0306-4522(94)90526-6, 7534884.
24. White DM. Intrathecal neuropeptide Y exacerbates nerve injury-induced mechanical hyperalgesia. Brain Res 1997, 750:141-6. 10.1016/S0006-8993(96)01340-6, 9098538.
25. Taiwo OB, Taylor BK. Antihyperalgesic effects of intrathecal neuropeptide Y during inflammation are mediated by Y1 receptors. Pain 2002, 96:353-63. 10.1016/S0304-3959(01)00481-X, 11973010.
26. Hua XY, Boublik JH, Spicer MA, Rivier JE, Brown MR, Yaksh TL. The antinociceptive effects of spinally administered neuropeptide Y in the rat: systematic studies on structure-activity relationship. J Pharmacol Exp Ther 1991, 258:243-8.
27. Gibbs J, Flores CM, Hargreaves KM. Neuropeptide Y inhibits capsaicin-sensitive nociceptors via a Y1-receptor-mediated mechanism. Neuroscience 2004, 125:703-9. 10.1016/j.neuroscience.2004.01.044, 15099684.
28. Gibbs JL, Flores CM, Hargreaves KM. Attenuation of capsaicin-evoked mechanical allodynia by peripheral neuropeptide Y Y1 receptors. Pain 2006, 124:167-74. 10.1016/j.pain.2006.04.013, 16714086.
29. Broqua P, Wettstein JG, Rocher MN, Gauthier-Martin B, Riviere PJ, Junien JL, Dahl SG. Antinociceptive effects of neuropeptide Y and related peptides in mice. Brain Res 1996, 724:25-32. 10.1016/0006-8993(96)00262-4, 8816252.
30. Naveilhan P, Hassani H, Lucas G, Blakeman KH, Hao JX, Xu XJ, Wiesenfeld-Hallin Z, Thoren P, Ernfors P. Reduced antinociception and plasma extravasation in mice lacking a neuropeptide Y receptor. Nature 2001, 409:513-7. 10.1038/35054063, 11206547.
31. Doyle CA, Hunt SP. A role for spinal lamina I neurokinin-1-positive neurons in cold thermoreception in the rat. Neuroscience 1999, 91:723-32. 10.1016/S0306-4522(98)00623-X, 10366028.
32. Kim KJ, Yoon YW, Chung JM. Comparison of three rodent neuropathic pain models. Exp Brain Res 1997, 113:200-6. 10.1007/BF02450318, 9063706.
33. Kupers RC, Nuytten D, De Castro-Costa M, Gybels JM. A time course analysis of the changes in spontaneous and evoked behaviour in a rat model of neuropathic pain. Pain 1992, 50:101-11. 10.1016/0304-3959(92)90117-T, 1325048.
34. Goff JR, Burkey AR, Goff DJ, Jasmin L. Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behaviour. Neuroscience 1998, 82:559-74. 10.1016/S0306-4522(97)00298-4, 9466461.
35. Desmeules JA, Kayser V, Weil-Fuggaza J, Bertrand A, Guilbaud G. Influence of the sympathetic nervous system in the development of abnormal pain-related behaviours in a rat model of neuropathic pain. Neuroscience 1995, 67:941-51. 10.1016/0306-4522(95)00098-4, 7675215.
36. Lee BH, Yoon YW, Chung K, Chung JM. Comparison of sympathetic sprouting in sensory ganglia in three animal models of neuropathic pain. Exp Brain Res 1998, 120:432-8. 10.1007/s002210050416, 9655228.
37. Perrot S, Attal N, Ardid D, Guilbaud G. Are mechanical and cold allodynia in mononeuropathic and arthritic rats relieved by systemic treatment with calcitonin or guanethidine?. Pain 1993, 52:41-7. 10.1016/0304-3959(93)90111-2, 8383311.
38. Lanteri-Minet M, Desmeules JA, Menetrey D. Opposite effects of axon damage on heat shock proteins (hsp 70) and ubiquitin contents in motor neurons of neuropathic rats. Neurosci Lett 1993, 153:49-52. 10.1016/0304-3940(93)90074-U, 7685508.
39. Guilbaud G, Gautron M, Jazat F, Ratinahirana H, Hassig R, Hauw JJ. Time course of degeneration and regeneration of myelinated nerve fibres following chronic loose ligatures of the rat sciatic nerve: can nerve lesions be linked to the abnormal pain-related behaviours?. Pain 1993, 53:147-58. 10.1016/0304-3959(93)90074-Y, 8393169.
40. Filliatreau G, Attal N, Hassig R, Guilbaud G, Desmeules J, DiGiamberardino L. Time-course of nociceptive disorders induced by chronic loose ligatures of the rat sciatic nerve and changes of the acetylcholinesterase transport along the ligated nerve. Pain 1994, 59:405-13. 10.1016/0304-3959(94)90027-2, 7708415.
41. Rushmer DS, Dunbar DC, Russell CJ, Windus SL. Automatic postural responses in the cat: responses of distal hindlimb muscles to paired vertical perturbations of stance. Exp Brain Res 1987, 68:477-90. 10.1007/BF00249792, 3691720.
42. Steinmetz JE, Cervenka J, Dobson J, Romano AG, Patterson MM. Central and peripheral influences on retention of postural asymmetry in rats. J Comp Physiol Psychol 1982, 96:4-11. 10.1037/h0077865, 7056899.
43. Vierck C. Animal models of pain. 2008, 175-86. Wall and Melzack's Textbook of Pain Elsevier, McMahon S, Kottzenburg M.
44. Wahren LK, Torebjork E. Quantitative sensory tests in patients with neuralgia 11 to 25 years after injury. Pain 1992, 48:237-44. 10.1016/0304-3959(92)90063-H, 1589241.
45. Woolf CJ. Long term alterations in the excitability of the flexion reflex produced by peripheral tissue injury in the chronic decerebrate rat. Pain 1984, 18:325-43. 10.1016/0304-3959(84)90045-9, 6728499.
46. Kauppila T, Kontinen VK, Pertovaara A. Influence of spinalization on spinal withdrawal reflex responses varies depending on the submodality of the test stimulus and the experimental pathophysiological condition in the rat. Brain Res 1998, 797:234-42. 10.1016/S0006-8993(98)00379-5, 9666138.
47. Vierck CJ, Acosta-Rua A, Nelligan R, Tester N, Mauderli A. Low dose systemic morphine attenuates operant escape but facilitates innate reflex responses to thermal stimulation. J Pain 2002, 3:309-19. 10.1054/jpai.2002.125186, 14622755.
48. Vierck CJ, Light A. Assessment of pain sensitivity in dermatomes caudal to the spinal cord injury in rats. Spinal cord injury pain: Assessment mechanisms, management 2002, 137-53. Seattle: IASP press, Yezierski R, Burchiel K.
49. King CD, Devine DP, Vierck CJ, Rodgers J, Yezierski RP. Differential effects of stress on escape and reflex responses to nociceptive thermal stimuli in the rat. Brain Res 2003, 987:214-22. 10.1016/S0006-8993(03)03339-0, 14499966.
50. Vierck CJ, Kline RH, Wiley RG. Intrathecal substance p-saporin attenuates operant escape from nociceptive thermal stimuli. Neuroscience 2003, 119:223-32. 10.1016/S0306-4522(03)00125-8, 12763083.
51. Jabakhanji R, Foss JM, Berra HH, Centeno MV, Apkarian AV, Chialvo DR. Inflammatory and neuropathic pain animals exhibit distinct responses to innocuous thermal and motoric challenges. Mol Pain 2006, 2:1. 10.1186/1744-8069-2-1, 1351167, 16393346.
52. Polgar E, Hughes DI, Riddell JS, Maxwell DJ, Puskar Z, Todd AJ. Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 2003, 104:229-39. 10.1016/S0304-3959(03)00011-3, 12855333.
53. Polgar E, Gray S, Riddell JS, Todd AJ. Lack of evidence for significant neuronal loss in laminae I-III of the spinal dorsal horn of the rat in the chronic constriction injury model. Pain 2004, 111:144-50. 10.1016/j.pain.2004.06.011, 15327818.
54. Zhang X, Dagerlind A, Elde RP, Castel MN, Broberger C, Wiesenfeld-Hallin Z, Hokfelt T. Marked increase in cholecystokinin B receptor messenger RNA levels in rat dorsal root ganglia after peripheral axotomy. Neuroscience 1993, 57:227-33. 10.1016/0306-4522(93)90057-M, 8115034.
55. Zhang X, Bao L, Shi TJ, Ju G, Elde R, Hokfelt T. Down-regulation of mu-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 1998, 82:223-40. 10.1016/S0306-4522(97)00240-6, 9483516.
56. Zhang X, de Araujo Lucas G, Elde R, Wiesenfeld-Hallin Z, Hokfelt T. Effect of morphine on cholecystokinin and mu-opioid receptor-like immunoreactivities in rat spinal dorsal horn neurons after peripheral axotomy and inflammation. Neuroscience 2000, 95:197-207. 10.1016/S0306-4522(99)00419-4, 10619476.
57. McCleane GJ. A phase 1 study of the cholecystokinin (CCK) B antagonist L-365, 260 in human subjects taking morphine for intractable non-cancer pain. Neurosci Lett 2002, 332:210-2. 10.1016/S0304-3940(02)00934-5, 12399016.
58. McCleane GJ. The cholecystokinin antagonist proglumide has an analgesic effect in chronic pancreatitis. Pancreas 2000, 21:324-5. 10.1097/00006676-200010000-00016, 11039479.
59. McCleane GJ. The cholecystokinin antagonist proglumide enhances the analgesic efficacy of morphine in humans with chronic benign pain. Anesth Analg 1998, 87:1117-20. 10.1097/00000539-199811000-00025, 9806692.
60. McCleane G. Cholecystokinin antagonists can they augment opioid-derived analgesia?. J Opioid Manag 2005, 1:273-9.
61. McCleane G. Cholecystokinin antagonists a new way to improve the analgesia from old analgesics?. Curr Pharm Des 2004, 10:303-14. 10.2174/1381612043386419, 14754389.
62. Besse D, Lombard MC, Perrot S, Besson JM. Regulation of opioid binding sites in the superficial dorsal horn of the rat spinal cord following loose ligation of the sciatic nerve: comparison with sciatic nerve section and lumbar dorsal rhizotomy. Neuroscience 1992, 50:921-33. 10.1016/0306-4522(92)90215-N, 1333063.
63. Smith PA, Moran TD, Abdulla F, Tumber KK, Taylor BK. Spinal mechanisms of NPY analgesia. Peptides 2007, 28:464-74. 10.1016/j.peptides.2006.09.029, 17194506.
64. Ma W, Bisby MA. Partial sciatic nerve ligation induced more dramatic increase of neuropeptide Y immunoreactive axonal fibers in the gracile nucleus of middle-aged rats than in young adult rats. J Neurosci Res 2000, 60:520-30. 10.1002/(SICI)1097-4547(20000515)60:4<520::AID-JNR11>3.0.CO;2-D, 10797555.
65. Munglani R, Harrison SM, Smith GD, Bountra C, Birch PJ, Elliot PJ, Hunt SP. Neuropeptide changes persist in spinal cord despite resolving hyperalgesia in a rat model of mononeuropathy. Brain Res 1996, 743:102-8. 10.1016/S0006-8993(96)01026-8, 9017236.
66. Intondi AB, Dahlgren MN, Eilers MA, Taylor BK. Intrathecal neuropeptide Y reduces behavioral and molecular markers of inflammatory or neuropathic pain. Pain 2008, 137:352-65. 10.1016/j.pain.2007.09.016, 2556181, 17976913.
67. Doyle CA, Hunt SP. Substance Preceptor (neurokinin-1)-expressing neurons in lamina I of the spinal cord encode for the intensity of noxious stimulation: a c-Fos study in rat. Neuroscience 1999, 89:17-28. 10.1016/S0306-4522(98)00276-0, 10051214.
68. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Wiley RG, Simone DA. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance Preceptor. Science 1997, 278:275-9. 10.1126/science.278.5336.275, 9323204.
69. Nichols ML, Allen BJ, Rogers SD, Ghilardi JR, Honore P, Luger NM, Finke MP, Li J, Lappi DA, Simone DA, Mantyh PW. Transmission of chronic nociception by spinal neurons expressing the substance Preceptor. Science 1999, 286:1558-61. 10.1126/science.286.5444.1558, 10567262.
70. Wiley RG. Substance Preceptor-expressing dorsal horn neurons: lessons from the targeted cytotoxin substance P-saporin. Pain 2008, 136:7-10. 10.1016/j.pain.2008.03.010, 18372112.
71. Sommer C, Lalonde A, Heckman HM, Rodriguez M, Myers RR. Quantitative neuropathology of a focal nerve injury causing hyperalgesia. J Neuropathol Exp Neurol 1995, 54:635-43. 10.1097/00005072-199509000-00004, 7666051.
72. Cui JG, Holmin S, Mathiesen T, Meyerson BA, Linderoth B. Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy. Pain 2000, 88:239-48. 10.1016/S0304-3959(00)00331-6, 11068111.
73. George A, Marziniak M, Schafers M, Toyka KV, Sommer C. Thalidomide treatment in chronic constrictive neuropathy decreases endoneurial tumor necrosis factor-alpha, increases interleukin-10 and has long-term effects on spinal cord dorsal horn met-enkephalin. Pain 2000, 88:267-75. 10.1016/S0304-3959(00)00333-X, 11068114.
74. Wiley RG, Kline R. Neuropeptide Y receptor-expressing dorsal horn neurons: role in nocifensive reflex responses to heat and formalin. Neuroscience 2009, 161:139-47. 10.1016/j.neuroscience.2008.12.017, 19138726.
75. Kline R, Wiley RG. Spinal mu-opioid receptor-expressing dorsal horn neurons: role in nociception and morphine antinociception. J Neurosci 2008, 28:904-13. 10.1523/JNEUROSCI.4452-07.2008, 18216198.
76. Wiley RG, Kline R, Vierck CJ. Anti-nociceptive effects of selectively destroying substance Preceptor-expressing dorsal horn neurons using [Sar9,Met(O2)11]-substance P-saporin: behavioral and anatomical analyses. Neuroscience 2007, 146:1333-45. 10.1016/j.neuroscience.2007.01.066, 17418497.