Morphine-induced early delays in wound closure: Involvement of sensory neuropeptides and modification of neurokinin receptor expression

Biochemical Pharmacology

Volumn 77, Issue 11, 2009, Pages 1747-1755

  Rook, Jerri M ^a   Hasan, Wohaib ^a   McCarson, Kenneth E ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Macrophage; Myofibroblast; Neurokinin A; Primary afferent neuron; Skin; Substance P

Indexed keywords

CAPSAICIN; MORPHINE; MORPHINE SULFATE; NEUROKININ 1 RECEPTOR; NEUROKININ 2 RECEPTOR; NEUROKININ A; NEUROPEPTIDE; OPIATE; TACHYKININ RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MACROPHAGE ACTIVATION; MALE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; RAT; WOUND CLOSURE; WOUND HEALING IMPAIRMENT;

ANIMALS; CAPSAICIN; GENE EXPRESSION REGULATION; MALE; MORPHINE; NEUROKININ A; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; RECEPTORS, NEUROKININ-2; SUBSTANCE P; WOUND HEALING; WOUNDS AND INJURIES;

EID: 64249140130     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2009.03.003     Document Type: Article

References (75)

1. Stein C. Peripheral mechanisms of opioid analgesia. Anesth Analg 76 (1993) 182-191
2. Stein C., Comisel K., Haimerl E., Yassouridis A., Lehrberger K., Herz A., et al. Analgesic effect of intraarticular morphine after arthroscopic knee surgery. N Engl J Med 325 (1991) 1123-1126
3. Ho S.T., Wang T.J., Tang J.S., Liaw W.J., and Ho C.M. Pain relief after arthroscopic knee surgery: intravenous morphine, epidural morphine, and intra-articular morphine. Clin J Pain 16 (2000) 105-109
4. Likar R., Schafer M., Paulak F., Sittl R., Pipam W., Schalk H., et al. Intraarticular morphine analgesia in chronic pain patients with osteoarthritis. Anesth Analg 84 (1997) 1313-1317
5. Stein A., Yassouridis A., Szopko C., Helmke K., and Stein C. Intraarticular morphine versus dexamethasone in chronic arthritis. Pain 83 (1999) 525-532
6. Cerchietti L.C., Navigante A.H., Bonomi M.R., Zaderajko M.A., Menendez P.R., Pogany C.E., et al. Effect of topical morphine for mucositis-associated pain following concomitant chemoradiotherapy for head and neck carcinoma. Cancer 95 (2002) 2230-2236
7. Flock P. Pilot study to determine the effectiveness of diamorphine gel to control pressure ulcer pain. J Pain Symptom Manage 25 (2003) 547-554
8. Long T.D., Cathers T.A., Twillman R., O'Donnell T., Garrigues N., and Jones T. Morphine-infused silver sulfadiazine (MISS) cream for burn analgesia: a pilot study. J Burn Care Rehabil 22 (2001) 118-123
9. Watterson G., Howard R., and Goldman A. Peripheral opioids in inflammatory pain. Arch Dis Child 89 (2004) 679-681
10. Zeppetella G., Paul J., and Ribeiro M.D. Analgesic efficacy of morphine applied topically to painful ulcers. J Pain Symptom Manage 25 (2003) 555-558
11. Jin S., Lei L., Wang Y., Da D., and Zhao Z. Endomorphin-1 reduces carrageenan-induced fos expression in the rat spinal dorsal horn. Neuropeptides 33 (1999) 281-284
12. Khalil Z., Sanderson K., Modig M., and Nyberg F. Modulation of peripheral inflammation by locally administered endomorphin-1. Inflamm Res 48 (1999) 550-556
13. 2+ currents, but spares a sustained current. Neuron 6 (1991) 13-20
14. Aimone L.D., and Yaksh T.L. Opioid modulation of capsaicin-evoked release of substance P from rat spinal cord in vivo. Peptides 10 (1989) 1127-1131
15. Delgado A.V., McManus A.T., and Chambers J.P. Exogenous administration of Substance P enhances wound healing in a novel skin-injury model. Exp Biol Med (Maywood) 230 (2005) 271-280
16. Engin C. Effects of calcitonin gene-related peptide on wound contraction in denervated and normal rat skin: a preliminary report. Plast Reconstr Surg 101 (1998) 1887-1890
17. Kjartansson J., and Dalsgaard C.J. Calcitonin gene-related peptide increases survival of a musculocutaneous critical flap in the rat. Eur J Pharmacol 142 (1987) 355-358
18. Khalil Z., and Helme R. Sensory peptides as neuromodulators of wound healing in aged rats. J Gerontol A Biol Sci Med Sci 51 (1996) B354-B361
19. Kjartansson J., Dalsgaard C.J., and Jonsson C.E. Decreased survival of experimental critical flaps in rats after sensory denervation with capsaicin. Plast Reconstr Surg 79 (1987) 218-221
20. Peskar B.M., Lambrecht N., Stroff T., Respondek M., and Muller K.M. Functional ablation of sensory neurons impairs healing of acute gastric mucosal damage in rats. Digest Dis Sci 40 (1995) 2460-2464
21. Smith P.G., and Liu M. Impaired cutaneous wound healing after sensory denervation in developing rats: effects on cell proliferation and apoptosis. Cell Tissue Res 307 (2002) 281-291
22. Eglezos A., Andrews P.V., Boyd R.L., and Helme R.D. Modulation of the immune response by tachykinins. Immunol Cell Biol 69 Pt 4 (1991) 285-294
23. Eglezos A., Helme R.D., Dandie G.W., Andrews P.V., and Boyd R.L. Substance P-mediated modulation of the primary antibody response. Adv Exp Med Biol 237 (1988) 499-503
24. Khalil Z., and Helme R.D. Serotonin modulates substance P-induced plasma extravasation and vasodilatation in rat skin by an action through capsaicin-sensitive primary afferent nerves. Brain Res 527 (1990) 292-298
25. Khalil Z., and Helme R.D. Sequence of events in substance P-mediated plasma extravasation in rat skin. Brain Res 500 (1989) 256-262
26. Nilsson J., von Euler A.M., and Dalsgaard C.J. Stimulation of connective tissue cell growth by substance P and substance K. Nature 315 (1985) 61-63
27. Rameshwar P., Poddar A., Zhu G., and Gascon P. Receptor induction regulates the synergistic effects of substance P with IL-1 and platelet-derived growth factor on the proliferation of bone marrow fibroblasts. J Immunol 158 (1997) 3417-3424
28. Ziche M., Morbidelli L., Pacini M., Dolara P., and Maggi C.A. NK1-receptors mediate the proliferative response of human fibroblasts to tachykinins. Br J Pharmacol 100 (1990) 11-14
29. Ziche M., Morbidelli L., Pacini M., Geppetti P., Alessandri G., Maggi C.A., and Substance. P stimulates neovascularization in vivo and proliferation of cultured endothelial cells. Microvasc Res 40 (1990) 264-278
30. Tanaka T., Danno K., Ikai K., and Imamura S. Effects of substance P and substance K on the growth of cultured keratinocytes. J Invest Dermatol 90 (1988) 399-401
31. Mussap C.J., Geraghty D.P., and Burcher E. Tachykinin receptors: a radioligand binding perspective. J Neurochem 60 (1993) 1987-2009
32. Regoli D., Boudon A., and Fauchere J.L. Receptors and antagonists for substance P and related peptides. Pharmacol Rev 46 (1994) 551-599
33. Ansel J.C., Kaynard A.H., Armstrong C.A., Olerud J., Bunnett N., and Payan D. Skin-nervous system interactions. J Invest Dermatol 106 (1996) 198-204
34. Bowden J.J., Baluk P., Lefevre P.M., Vigna S.R., and McDonald D.M. Substance P (NK1) receptor immunoreactivity on endothelial cells of the rat tracheal mucosa. Am J Physiol 270 (1996) L404-L414
35. Ho W.Z., Lai J.P., Zhu X.H., Uvaydova M., and Douglas S.D. Human monocytes and macrophages express substance P and neurokinin-1 receptor. J Immunol 159 (1997) 5654-5660
36. Krause J.E., Takeda Y., and Hershey A.D. Structure, functions, and mechanisms of substance P receptor action. J Invest Dermatol 98 (1992) 2S-7S
37. Lai J.P., Douglas S.D., and Ho W.Z. Human lymphocytes express substance P and its receptor. J Neuroimmunol 86 (1998) 80-86
38. Qian B.F., Zhou G.Q., Hammarstrom M.L., and Danielsson A. Both substance P and its receptor are expressed in mouse intestinal T lymphocytes. Neuroendocrinology 73 (2001) 358-368
39. Haley K.J., Sunday M.E., Osathanondh R., Du J., Vathanaprida C., Karpitsky V.V., et al. Developmental expression of neurokinin A and functional neurokinin-2 receptors in lung. Am J Physiol Lung Cell Mol Physiol 280 (2001) L1348-L1358
40. Song I.S., Bunnett N.W., Olerud J.E., Harten B., Steinhoff M., Brown J.R., et al. Substance P induction of murine keratinocyte PAM 212 interleukin 1 production is mediated by the neurokinin 2 receptor (NK-2R). Exp Dermatol 9 (2000) 42-52
41. Rook J.M., and McCarson K.E. Delay of cutaneous wound closure by morphine via local blockade of peripheral tachykinin release. Biochem Pharmacol 74 (2007) 752-757
42. Schmassmann A., Waser B., Flogerzi B., and Reubi J.C. Expression of functional neurokinin-1 receptors in regenerative glands during gastric wound healing in rodents. Gastroenterology 126 (2004) 784-795
43. Cao T., Grant A.D., Gerard N.P., and Brain S.D. Lack of a significant effect of deletion of the tachykinin neurokinin-1 receptor on wound healing in mouse skin. Neuroscience 108 (2001) 695-700
44. Chen C., Farooqui M., and Gupta K. Morphine stimulates vascular endothelial growth factor-like signaling in mouse retinal endothelial cells. Curr Neurovasc Res 3 (2006) 171-180
45. Farooqui M., Li Y., Rogers T., Poonawala T., Griffin R.J., Song C.W., et al. COX-2 inhibitor celecoxib prevents chronic morphine-induced promotion of angiogenesis, tumour growth, metastasis and mortality, without compromising analgesia. Br J Cancer 97 (2007) 1523-1531
46. Gupta K., Kshirsagar S., Chang L., Schwartz R., Law P.Y., Yee D., et al. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res 62 (2002) 4491-4498
47. Singleton P.A., Lingen M.W., Fekete M.J., Garcia J.G., and Moss J. Methylnaltrexone inhibits opiate and VEGF-induced angiogenesis: role of receptor transactivation. Microvasc Res 72 (2006) 3-11
48. Dai X., Cui S.G., Wang T., Liu Q., Song H.J., and Wang R. Endogenous opioid peptides, endomorphin-1 and -2 and deltorphin I, stimulate angiogenesis in the CAM assay. Eur J Pharmacol 579 (2008) 269-275
49. Poonawala T., Levay-Young B.K., Hebbel R.P., and Gupta K. Opioids heal ischemic wounds in the rat. Wound Repair Regen 13 (2005) 165-174
50. Bigliardi-Qi M., Gaveriaux-Ruff C., Zhou H., Hell C., Bady P., Rufli T., et al. Deletion of delta-opioid receptor in mice alters skin differentiation and delays wound healing. Differentiation 74 (2006) 174-185
51. Lei Y.H., and Rogers D.F. Effects and interactions of opioids on plasma exudation induced by cigarette smoke in guinea pig bronchi. Am J Physiol 276 (1999) 391-397
52. Romero A., and Planas E. Anti-exudative effects of opioid receptor agonists in a rat model of carrageenan-induced acute inflammation of the paw. Eur J Pharmacol 511 (2005) 207-217
53. Twillman R.K., Long T.D., Cathers T.A., and Mueller D.W. Treatment of painful skin ulcers with topical opioids. J Pain Symptom Manage 17 (1999) 288-292
54. Rook J.M., Hasan W., and McCarson K.E. Temporal effects of topical morphine application on cutaneous wound healing. Anesthesiology 109 (2008) 130-136
55. Liu M., Warn J.D., Fan Q., and Smith P.G. Relationships between nerves and myofibroblasts during cutaneous wound healing in the developing rat. Cell Tissue Res 297 (1999) 423-433
56. Zhou L., Zhang Q., Stein C., and Schafer M. Contribution of opioid receptors on primary afferent versus sympathetic neurons to peripheral opioid analgesia. J Pharmacol Exp Ther 286 (1998) 1000-1006
57. Lauria G., Cornblath D.R., Johansson O., McArthur J.C., Mellgren S.I., Nolano M., et al. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur J Neurol 12 (2005) 747-758
58. Lynn B. Capsaicin: actions on nociceptive C-fibres and therapeutic potential. Pain 41 (1990) 61-69
59. Holzer P. Capsaicin: cellular targets, mechanisms of action, and selectivity for thin sensory neurons. Pharmacol Rev 43 (1991) 143-201
60. Zhang Q., Schaffer M., Elde R., and Stein C. Effects of neurotoxins and hindpaw inflammation on opioid receptor immunoreactivities in dorsal root ganglia. Neuroscience 85 (1998) 281-291
61. Schicho R., Skofitsch G., and Donnerer J. Regenerative effect of human recombinant NGF on capsaicin-lesioned sensory neurons in the adult rat. Brain Res 815 (1999) 60-69
62. Schaffer M., Beiter T., Becker H.D., and Hunt T.K. Neuropeptides: mediators of inflammation and tissue repair?. Arch Surg 133 (1998) 1107-1116
63. Levine J.D., Fields H.L., and Basbaum A.I. Peptides and the primary afferent nociceptor. J Neurosci 13 (1993) 2273-2286
64. DiPietro L.A. Wound healing: the role of the macrophage and other immune cells. Shock 4 (1995) 233-240
65. Leibovich S.J., and Ross R. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol 78 (1975) 71-100
66. Dinda A., Gitman M., and Singhal P.C. Immunomodulatory effect of morphine: therapeutic implications. Expert Opin Drug Saf 4 (2005) 669-675
67. Lam C.F., Chang P.J., Huang Y.S., Sung Y.H., Huang C.C., Lin M.W., et al. Prolonged use of high-dose morphine impairs angiogenesis and mobilization of endothelial progenitor cells in mice. Anesth Analg 107 (2008) 686-692
68. Diegelmann R.F., Schuller-Levis G., Cohen I.K., and Kaplan A.M. Identification of a low molecular weight, macrophage-derived chemotactic factor for fibroblasts. Clin Immunol Immunopathol 41 (1986) 331-341
69. Gharaee-Kermani M., Denholm E.M., and Phan S.H. Costimulation of fibroblast collagen and transforming growth factor beta1 gene expression by monocyte chemoattractant protein-1 via specific receptors. J Biol Chem 271 (1996) 17779-17784
70. Yamamoto T., Eckes B., Mauch C., Hartmann K., and Krieg T. Monocyte chemoattractant protein-1 enhances gene expression and synthesis of matrix metalloproteinase-1 in human fibroblasts by an autocrine IL-1 alpha loop. J Immunol 164 (2000) 6174-6179
71. Baum C.L., and Arpey C.J. Normal cutaneous wound healing: clinical correlation with cellular and molecular events. Dermatol Surg 31 (2005) 674-686
72. Werner S., and Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 83 (2003) 835-870
73. Gabbiani G. The biology of the myofibroblast. Kidney Int 41 (1992) 530-532
74. Gabbiani G., Ryan G.B., and Majne G. Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction. Experientia 27 (1971) 549-550
75. Goetzl E.J., Banda M.J., and Leppert D. Matrix metalloproteinases in immunity. J Immunol 156 (1996) 1-4