Intrathecal grafting of porcine chromaffin cells reduces formalin-evoked c-Fos expression in the rat spinal cord

Cell Transplantation

Volumn 14, Issue 6, 2005, Pages 353-365

  Sol, J C ^a   Li, R Y ^a   Sallerin, B ^a   Jozan, S ^a   Zhou, H ^a   Lauwers Cances, V ^a   Tortosa, F ^a   Chaynes, P ^a   Mascott, C ^a   Bastide, R ^a   Lazorthes, Y ^a  

^a UNIVERSITÉ PAUL SABATIER   (France)

Author keywords

c Fos; Cell therapy; Intrathecal transplantation; Pain; Xenograft

Indexed keywords

CATECHOLAMINE; FORMALDEHYDE; GROWTH FACTOR; OPIATE; PROTEIN C FOS;

ADRENAL GLAND; ANALGESIA; ANIMAL CELL; ANTINOCICEPTION; ARTICLE; CATECHOLAMINE RELEASE; CHROMAFFIN CELL; CONTROLLED STUDY; COW; EVALUATION; GRAFT DYSFUNCTION; IMMUNOREACTIVITY; IN VIVO STUDY; MALE; NONHUMAN; ONCOGENE C FOS; PAIN ASSESSMENT; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPINAL CORD; SPINAL CORD DORSAL HORN; SUBARACHNOID SPACE; SWINE; XENOGRAFT;

ANIMALIA; BOVINAE; RODENTIA; SUIDAE;

EID: 24944519226     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/000000005783982963     Document Type: Article

References (67)

1. Abbadie, C.; Besson, J. M. C-fos expression in rat lumbar spinal cord during the development of adjuvant-induced arthritis. Neuroscience 48:985-993; 1992.
2. Abbadie, C.; Besson, J. M. Fos-like immunoreactivity in the rat superficial dorsal horn induced by formalin injection in the forepaw: Effects of dorsal rhizotomies. Brain Res. 578:17-25; 1992.
3. Abbadie, C.; Honore, P.; Besson, J. M. Intense cold stimulation of the rat hindpaw induces c-fos expression in rat lumbar spinal cord neurons by noxious heat stimulation. Eur. J. Pharmacol. 258:215-227; 1994.
4. Abbadie, C.; Lombard, M. C.; Morain, F.; Besson, J. M. Fos-like immunoreactivity in the rat spinal cord induced by formalin injection in the forelimb to gauge possible plasticity of primary afferent fibers following partial deafferentation. Restor. Neurol. Neurosci. 6:195-207; 1994.
5. Abbadie, C.; Taylor, B. K.; Peterson, M. A.; Basbaum, A. I. Differential contribution of the two phases of the formalin test to the pattern of c-fos expression in the rat spinal cord: Studies with remifentanil and lidocaine. Pain 69:101-110; 1997.
6. Bader, M. F.; Ciesielski-Treska, J.; Thierse, D.; Hesketh, J. E.; Aunis, D. Immunocytochemical study of microtubules in chromaffin cells in culture and evidence that tubulin is not an integral protein of the chromaffin granule membrane. J. Neurochem. 37:917-933; 1981.
7. Bes, J. C.; Tkaczuk, J.; Czech, K. A.; Tafani, M.; Bastide, R.; Caratero, C.; Pappas, G. D.; Lazorthes, Y. One-year chromaffin cell allograft survival in cancer patients with chronic pain: Morphological and functional evidence. Cell Transplant. 7:227-238; 1998.
8. Besson, J. M.; Chaouch, A. Peripheral and spinal mechanisms of nociception. Physiol. Rev. 67:67-186; 1987.
9. Borie, D. C.; Cramer, D. V.; Phan-Thanh, L.; Vaillant, J. C.; Bequet, J. L.; Makowka, L.; Hannoun, L. Microbiological hazards related to xenotransplantation of porcine organs into man. Infect. Control Hosp. Epidemiol. 19: 355-365; 1998.
10. Brewer, K. L.; Yezierski, R. P. Effects of adrenal medullary transplants on pain-related behaviors following excitotoxic spinal cord injury. Brain Res. 798:83-92; 1998.
11. Bullitt, E. Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. Neurol. 296:517-530; 1990.
12. Bullitt, E. Somatotopy of spinal nociceptive processing. J. Comp. Neurol. 312:279-290; 1991.
13. Bullitt, E.; Lee, C. L.; Light, A. R.; Willcockson, H. The effect of stimulus duration on noxious-stimulus induced c-fos expression in the rodent spinal cord. Brain Res. 580: 172-179; 1992.
14. Buritova, J.; Fletcher, D.; Honore, P.; Besson, J. M. Effects of local anaesthetics on carrageenan-evoked inflammatory nociceptive processing in the rat. Br. J. Anaesth. 77:645-652; 1996.
15. Clive, P.; Scobie, L.; Quinn, G. Porcine endogenous retrovirus-advances, issues and solutions. Xenotransplantation 9:373-375; 2002.
16. Czech, K. A.; Sagen, J. Update on cellular transplantation into the CNS as a novel therapy for chronic pain. Prog. Neurobiol. 46:507-529; 1995.
17. Decosterd, I.; Buchser, E.; Gilliard, N.; Saydoff, J.; Zurn, A. D.; Aebischer, P. Intrathecal implants of bovine chromaffin cells alleviate mechanical allodynia in a rat model of neuropathic pain. Pain 76:159-166; 1998.
18. Dubuisson, D.; Dennis, S. G. The formalin test: A quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4: 161-174; 1977.
19. Duplan, H.; Bes, J. C.; Tafani, M.; Sallerin, B.; Sagen, J.; Ohayon, E.; Lazorthes, Y.; Tkaczuk, J. Adrenal medullary explants as an efficient tool for pain control: Adhesive biomolecular components are involved in graft function ex vivo. Exp. Neurol. 163:331-347; 2000.
20. Elliott, K. J.; Brodsky, M.; Hynansky, A. D.; Foley, K. M.; Inturrisi, C. E. Dextromethorphan suppresses both formalin-induced nociceptive behavior and the formalin-induced increase in spinal cord c-fos mRNA. Pain 61:401-409; 1995.
21. Fitzgerald, M. C-fos and the changing face of pain. Trends Neurosci. 13:439-440; 1990.
22. Ginzburg, R.; Seltzer, Z. Subarachnoid spinal cord transplantation of adrenal medulla suppresses chronic neuropathic pain behavior in rats. Brain Res. 523:147-150; 1990.
23. Goddard, M. J.; Forewaker, J. E.; Wallwork, J. Xenotransplantation-2000. J. Clin. Pathol. 53:44-48; 2000.
24. Gogas, K. R.; Levine, J. D.; Basbaum, A. I. Differential contribution of descending controls to the antinociceptive actions of kappa and mu opioids: An analysis of formalin-evoked c-fos expression. J. Pharmacol. Exp. Ther. 276: 801-809; 1996.
25. Gogas, K. R.; Presley, R. W.; Levine, J. D.; Basbaum, A. I. The antinociceptive action of supraspinal opioids results from an increase in descending inhibitory control: Correlation of nociceptive behavior and c-fos expression. Neuroscience 42:617-628; 1991.
26. Gulwadi, A. G.; Hoane, M. R.; Saydoff, J. A.; Frydel, B. R.; Lindner, M. D. No detectable analgesic effects in the formalin test even with one million bovine adrenal chromaffin cells. Pain 99:263-271; 2002.
27. Hains, B. C.; Chastain, K. M.; Everhart, A. W.; McAdoo, D. J.; Hulsebosch, C. E. Transplants of adrenal medullary chromaffin cells reduce forelimb and hindlimb allodynia in a rodent model of chronic central pain after spinal cord hemisection injury. Exp. Neurol. 164:426-437; 2000.
28. Hama, A. T.; Sagen, J. Alleviation of neuropathic pain symptoms by xenogeneic chromaffin cell grafts in the spinal subarachnoid space. Brain Res. 651:183-193; 1994.
29. Hama, A. T.; Sagen, J. Reduced pain-related behavior by adrenal medullary transplants in rats with experimental painful peripheral neuropathy. Pain 52:223-231; 1993.
30. Hammond, D. L.; Wang, H.; Nakashima, N.; Basbaum, A. I. Differential effects of intrathecally administered delta and mu opioid receptor agonists on formalin-evoked nociception and on the expression of fos-like immunoreactivity in the spinal cord of rat. J. Pharmacol. Exp. Ther. 284:378-387; 1998.
31. Harris, J. A. Using c-fos as a neural marker of pain. Brain Res. Bull. 45:1-8; 1998.
32. Honore, P.; Buritova, J.; Besson, J. M. Intraplantar morphine depresses spinal c-Fos expression induced by carrageenin inflammation but not by noxious heat. Br. J. Pharmacol. 118:671-680; 1996.
33. Hunt, S. P.; Pini, L. A.; Evan, G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634; 1987.
34. Kaneko, M.; Mestre, C.; Sanchez, E. H.; Hammond, D. L. Intrathecally administerd gabapentin inhibits formalin-evoked nociception and the expression of fos-like immunoreactivity in the spinal cord of rat. J. Pharmacol. Exp. Ther. 292:743-751; 2000.
35. Lazorthes, Y.; Bes, J. C.; Sagen, J.; Tafani, M.; Tkaczuk, J.; Sallerin, B.; Nahri, I.; Verdie, J. C.; Ohayon, E.; Caratero, C. Transplantation of human chromaffin cells for control of intractable cancer pain. Acta Neurochir. Suppl. (Wien) 64:97-100; 1995.
36. Lazorthes, Y.; Sagen, J.; Sallerin, B.; Tkaczuk, J.; Duplan, H.; Sol, J. C.; Tafani, M.; Bes, J. C. Human chromaffin cell graft into the CSF for cancer pain management: A prospective phase II clinical study. Pain 87:19-32; 2000.
37. Lima, D.; Avelino, A.; Coimbra, A. Differential activation of c-fos in spinal neurons by distinct classes of noxious stimuli. Neuroreport 4:747-750; 1993.
38. Lindner, M. D.; Francis, J. M.; McDermott, P. E.; Bell, W. J.; Blaney, T. J.; Sherman, S. S.; Saydoff, J. A. Numerous adrenal chromaffin cell preparations fail to produce analgesic effects in the formalin test or in tests of acute pain even with nicotine stimulation. Pain 88:177-188; 2000.
39. Lindner, M. D.; Francis, J. M.; Saydoff, J. A. Intrathecal polymer-encapsulated bovine adrenal chromaffin cells fail to produce analgesic effects in the hotplate and formalin test. Exp. Neurol. 165:370-383; 2000.
40. Lindner, M. D.; Frydel, B. R.; Francis, J. M.; Cain, C. K. Analgesic effects of adrenal chromaffin allografts: contingent on special procedures or due to experimenter bias? J. Pain 4:64-73; 2003.
41. Menetrey, D.; Gannon, A.; Levine, J. D.; Basbaum, A. I. Expression of c-fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation. J. Comp. Neurol. 285:177-195; 1989.
42. Molander, C.; Grant, G. Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat. Neuroscience 19:297-312; 1986.
43. Molander, C.; Xu, Q.; Grant, G. The cytoarchitectonic organization of the spinal cord in the rat: I. The lower thoracic and lumbosacral cord. J. Comp. Neurol. 230:133-141; 1984.
44. Munglani, R.; Hunt, S. P. Molecular biology of pain. Br. J. Anaesth. 75:186-192; 1995.
45. Onions, D.; Cooper, D. K.; Alexander, T. J.; Brown, C.; Claasen, E.; Forewaker, J. E.; Harris, D. L.; Mahy, B. W.; Minor, P. D.; Osterhaus, A. D.; Pastoret, P. P.; Yamanouchi, K. An approach to the control of disease transmission in pig to human xenotransplantation. Xenotransplantation 7:143-155; 2000.
46. Ortega, J. D.; Sagen, J.; Pappas, G. D. Short-term immunosuppression enhances long-term survival of bovine chromaffin cell xenografts in rat CNS. Cell Transplant. 1: 33-41; 1992.
47. Ortega-Alvaro, A.; Gibert-Rahola, J.; Mellado-Fernandez, M. L.; Chover, A. J.; Mico, J. A. The effects of different monoaminergic antidepressants on the analgesia induced by spinal cord adrenal medullary transplants in the formalin test in rats. Anesth. Analg. 84:816-820; 1997.
48. Pappas, G. D.; Lazorthes, Y.; Bes, J. C.; Tafani, M.; Winnie, A. P. Relief of intractable cancer pain by human chromaffin cell transplants: experience at two medical centers. Neurol. Res. 19:71-77; 1997.
49. Pertovaara, A.; Bravo, R.; Herdegen, T. Induction and suppression of immediate-early genes in the rat brain by a selective alpha-2-adrenoreceptor agonist and antagonist following noxious peripheral stimulation. Neuroscience 54:117-126; 1993.
50. Presley, R.; Menetrey, D.; Levine, J. D.; Basbaum, A. I. Systemic morphine suppresses noxious stimulus-evoked Fos protein-like immunoreactivity in the rat spinal cord. J. Neurosci. 10:323-335; 1990.
51. Rexed, B. The cytoarchitectonic organisation of the spinal cord in the cat. J. Comp. Neurol. 96:415-495; 1952.
52. Sagen, J. Cellular transplantation for intractable pain. Adv. Pharmacol. 42:579-582; 1998.
53. Sagen, J.; Pappas, G. D.; Perlow, M. J. Adrenal medullary tissue transplants in the rat spinal cord reduce pain sensitivity. Brain Res. 384:189-194; 1986.
54. Sagen, J.; Pappas, G. D.; Pollard, H. B. Analgesia induced by isolated bovine chromaffin cells implanted in rat spinal cord. Proc. Natl. Acad. Sci. USA 83:7522-7526; 1986.
55. Sagen, J.; Wang, H. Adrenal medullary grafts suppress c-fos induction in spinal neurons of arthritic rats. Neurosci. Lett. 192:181-184; 1995.
56. Sagen, J.; Wang, H.; Pappas, G. D. Adrenal medullary implants in the rat spinal cord reduce nociception in a chronic pain model. Pain 42:69-79; 1990.
57. Siegan, J. B.; Herzberg, U.; Frydel, B. R.; Sagen, J. Adrenal medullary transplants reduce formalin-evoked c-fos expression in the rat spinal cord. Brain Res. 944:174-183; 2002.
58. Siegan, J. B.; Sagen, J. Attenuation of formalin pain responses in the rat by adrenal medullary transplants in the spinal subarachnoid space. Pain 70:279-285; 1997.
59. Sol, J. C.; Sallerin, B.; Larrue, S.; Li, R.; Jozan, S.; Tortosa, F.; Mascott, C.; Carraoue, F.; Tafani, M.; Lazorthes, Y. Intrathecal xenogeneic chromaffin cell grafts reduce nociceptive behavior in a rodent tonic pain model. Exp. Neurol. 186:198-211; 2004.
60. Vaquero, J.; Arias, A.; Oya, S.; Zurita, M. Chromaffin allografts into arachnoid of spinal cord reduce basal pain responses in rats. Neuroreport 2:149-151; 1991.
61. Watson, G. S.; Sufka, K. J.; Coderre, T. J. Optimal scoring strategies and weights for the formalin test in rats. Pain 70:53-58; 1997.
62. Winnie, A. P.; Pappas, G. D.; Das Gupta, T. K.; Wang, H.; Ortega, J. D.; Sagen, J. Subarachnoid adrenal medullary transplants for terminal cancer pain. A report of preliminary studies. Anesthesiology 79:644-653; 1993.
63. Yadid, G.; Zangen, A.; Herzberg, U.; Nakash, R.; Sagen, J. Alterations in endogenous brain beta-endorphin release by adrenal medullary transplants in the spinal cord. Neuropsychopharmacology 23:709-716; 2000.
64. Yeomans, D. C.; Lu, Y.; Pappas, G. D. Conditional analgesia from spinally transplanted adrenal chromaffin cells. Pain 95:191-194; 2002.
65. Yu, W.; Hao, J. X.; Xu, X. J.; Saydoff, J.; Haegerstrand, A.; Hokfelt, T.; Wiesenfeld-Hallin, Z. Long-term alleviation of allodynia-like behaviors by intrathecal implantation of bovine chromaffin cells in rats with spinal cord injury. Pain 74:115-122; 1998.
66. Yu, W.; Hao, J. X.; Xu, X. J.; Saydoff, J.; Haegerstrand, A.; Wiesenfeld-Hallin, Z. Immunoisolating encapsulation of intrathecally implanted bovine chromaffin cells prolongs their survival and produces anti-allodynic effects in spinally injured rats. Eur. J. Pain 2:143-151; 1998.
67. Zimmerman, M. Ethical guidelines for investigators of experimental pain in conscious animals. Pain 16:109-110; 1983.