Substance P Enhances Wound Closure in Nitric Oxide Synthase Knockout Mice

Journal of Surgical Research

Volumn 153, Issue 2, 2009, Pages 201-209

  Muangman, Pornprom ^a   Tamura, Richard N ^a   Muffley, Lara A ^a   Isik, F Frank ^a   Scott, Jeffrey R ^a   Xie, Chengyu ^a   Kegel, Gary ^a   Sullivan, Stephen R ^a   Liang, Zhi ^a   Gibran, Nicole S ^a  

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

Author keywords

eNOS; flow cytometry; image analysis; inflammation; iNOS; neuropeptide; nNOS; NOS; response to injury; SP; wound healing

Indexed keywords

INDUCIBLE NITRIC OXIDE SYNTHASE; SODIUM CHLORIDE; SUBSTANCE P;

ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; ENDOTHELIUM CELL; EPITHELIZATION; FLOW CYTOMETRY; GENE DELETION; HEALING; INFLAMMATION; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; WOUND CLOSURE;

ANIMALS; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SKIN; SOFT TISSUE INJURIES; SUBSTANCE P; TIME FACTORS; WOUND HEALING;

EID: 64849099962     PISSN: 00224804     EISSN: 10958673     Source Type: Journal    
DOI: 10.1016/j.jss.2008.03.051     Document Type: Article

References (57)

1. Ansel J.C., Armstrong C.A., Song I., et al. Interactions of the skin and nervous system. J Investig Dermatol Symp Proc 2 (1997) 23
2. Lu B., Figini M., Emanueli C., et al. The control of microvascular permeability and blood pressure by neutral endopeptidase. Nat Med 3 (1997) 904
3. Foreman J.C. The skin as an organ for the study of the pharmacology of neuropeptides. Skin Pharmacol 1 (1988) 77
4. Baraniuk J.N., Kowalski M.L., and Kaliner M.A. Relationships between permeable vessels, nerves, and mast cells in rat cutaneous neurogenic inflammation. J Appl Physiol 68 (1990) 2305
5. Holzer P. Neurogenic vasodilatation and plasma leakage in the skin. Gen Pharmacol 30 (1998) 5
6. Hughes S.R., Williams T.J., and Brain S.D. Evidence that endogenous nitric oxide modulates oedema formation induced by substance P. Eur J Pharmacol 191 (1990) 481
7. Chancellor F.-C., Zhu G.F., Kage R., et al. Substance P and stress-induced changes in macrophages. Ann NY Acad Sci 771 (1995) 472
8. Ansel J.C., Brown J.R., Payan D.G., et al. Substance P selectively activates TNF-α gene expression in murine mast cells. J Immunol 150 (1993) 4478
9. Matis W.L., Lavker R.M., and Murphy G.F. Substance P induces the expression of an endothelial-leukocyte adhesion molecule by microvascular endothelium. J Invest Dermatol 94 (1990) 492
10. Nakagawa N., Iwamoto I., and Yoshida S. Effect of substance P on the expression of an adhesion molecule ICAM-1 in human vascular endothelial cells. Regul Pept 46 (1993) 223
11. Quinlan K.L., Song I.S., Naik S.M., et al. VCAM-1 expression on human dermal microvascular endothelial cells is directly and specifically up-regulated by substance P. J Immunol 162 (1999) 1656
12. Nakagawa N., Sano H., and Iwamoto I. Substance P induces the expression of intercellular adhesion molecule-1 on vascular endothelial cells and enhances neutrophil transendothelial migration. Peptides 16 (1995) 721
13. Parenti A., Amerini S., Ledda F., et al. The tachykinin NK1 receptor mediates the migration-promoting effect of substance P on human skin fibroblasts in culture. Naunyn-Schmiedebergs Arch Pharmacol 353 (1996) 475
14. Ziche M., Morbidelli L., Pacini M., et al. Substance P stimulates neovascularization in vivo and proliferation of cultured endothelial cells. Microvasc Res 40 (1990) 264
15. Ziche M., Morbidelli L., Geppetti P., et al. Substance P induces migration of capillary endothelial cells: A novel NK-1 selective receptor mediated activity. Life Sci 48 (1991) PL7
16. Furchgott R.F., Cherry P.D., Zawadzki J.V., et al. Endothelial cells as mediators of vasodilation of arteries. J Cardiovasc Pharmacol Suppl 2 (1984) S336
17. Furchgott R.F. The 1996 Albert Lasker Medical Research Awards. The discovery of endothelium-derived relaxing factor and its importance in the identification of nitric oxide. JAMA 276 (1996) 1186
18. Ignarro L.J., Buga G.M., Wood K.S., et al. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84 (1987) 9265
19. Fleming I., and Busse R. NO: The primary EDRF. J Mol Cell Cardiol 31 (1999) 5
20. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: Structure, function, and inhibition. Biochem J 357 (2001) 593
21. Ignarro L.J., Byrns R.E., Buga G.M., et al. Mechanisms of endothelium-dependent vascular smooth muscle relaxation elicited by bradykinin and VIP. Am J Physiol 253 (1987) H1074
22. Forstermann U., and Kleinert H. Nitric oxide synthase: Expression and expressional control of the three isoforms. Naunyn Schmiedebergs Arch Pharmacol 352 (1995) 351
23. Bull H.A., Hothersall J., Chowdhury N., et al. Neuropeptides induce release of nitric oxide from human dermal microvascular endothelial cells. J Investig Dermatol 106 (1996) 655
24. Jeon H.K., Jung N.P., Choi I.H., et al. Substance P augments nitric oxide production and gene expression in murine macrophages. Immunopharmacology 41 (1999) 219
25. Frank S., Kampfer H., Wetzler C., et al. Nitric oxide drives skin repair: Novel functions of an established mediator. Kidney Int 61 (2002) 882
26. Witte M.B., and Barbul A. Role of nitric oxide in wound repair. Am J Surg 183 (2002) 406
27. Akcay M.N., Ozcan O., Gundogdu C., et al. Effect of nitric oxide synthase inhibitor on experimentally induced burn wounds. J Trauma 49 (2000) 327
28. Schwentker A., Vodovotz Y., Weller R., et al. Nitric oxide and wound repair: Role of cytokines?. Nitric Oxide 7 (2002) 1
29. Arnhold S., Fassbender A., Klinz F.J., et al. NOS-II is involved in early differentiation of murine cortical, retinal, and ES cell-derived neurons-an immunocytochemical and functional approach. Int J Dev Neurosci 20 (2002) 83
30. Keilhoff G., Fansa H., and Wolf G. Neuronal nitric oxide synthase is the dominant nitric oxide supplier for the survival of dorsal root ganglia after peripheral nerve axotomy. J Chem Neuroanat 24 (2002) 181
31. Keilhoff G., Wolf G., and Fansa H. NOS-mediated differences in peripheral nerve graft revascularization and regeneration. Neuroreport 13 (2002) 1463
32. Ziche M., and Morbidelli L. Nitric oxide and angiogenesis. J Neurooncol 50 (2000) 139
33. Xiong Q., Shi Q., Le X., et al. Regulation of interleukin-8 expression by nitric oxide in human pancreatic adenocarcinoma. J Interferon Cytokine Res 21 (2001) 529
34. Shimizu Y., Sakai M., Umemura Y., et al. Immunohistochemical localization of nitric oxide synthase in normal human skin: Expression of endothelial-type and inducible-type nitric oxide synthase in keratinocytes. J Dermatol 24 (1997) 80
35. Bruch-Gerharz D., Ruzicka T., and Kolb-Bachofen V. Nitric oxide in human skin: Current status and future prospects. J Invest Dermatol 110 (1998) 1
36. Abd-El-Aleem S.A., Ferguson M.W., Appleton I., et al. Expression of nitric oxide synthase isoforms and arginase in normal human skin and chronic venous leg ulcers. J Pathol 191 (2000) 434
37. Wang R., Ghahary A., Shen Y.J., et al. Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J Invest Dermatol 106 (1996) 419
38. Carter E.A., Derojas-Walker T., Tamir S., et al. Nitric oxide production is intensely and persistently increased in tissue by thermal injury. Biochem J 304 (1994) 201
39. Paulsen S.M., Wurster S.H., and Nanney L.B. Expression of inducible nitric oxide synthase in human burn wounds. Wound Repair Regen 6 (1998) 142
40. Lee P.C., Salyapongse A.N., Bragdon G.A., et al. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am J Physiol 277 (1999) H1600
41. Lee R.H., Efron D., Tantry U., et al. Nitric oxide in the healing wound: A time-course study. J Surg Res 101 (2001) 104
42. Schaffer M.R., Tantry U., Thornton F.J., et al. Inhibition of nitric oxide synthesis in wounds: Pharmacology and effect on accumulation of collagen in wounds in mice. Eur J Surg 165 (1999) 262
43. Gibran N.S., Jang Y.C., Isik F.F., et al. Diminished neuropeptide levels contribute to the impaired cutaneous healing response associated with diabetes mellitus. J Surg Res 108 (2002) 122
44. Spenny M.L., Muangman P., Sullivan S.R., et al. Neutral endopeptidase inhibition in diabetic wound repair. Wound Repair Regen 10 (2002) 295
45. Muangman P., Muffley L.A., Anthony J.P., et al. Nerve growth factor accelerates wound healing in diabetic mice. Wound Repair Regen 12 (2004) 44
46. Ismail J.A., Poppa V., Kemper L.E., et al. Immunohistologic labeling of murine endothelium. Cardiovasc Pathol 12 (2003) 82
47. Johnson W.D., Lang C.M., and Johnson M.T. Fixatives and methods of fixation in selected tissues of the laboratory rat. Clin Toxicol 12 (1978) 583
48. Wilson L., Fathke C., and Isik F. Tissue dispersion and flow cytometry for the cellular analysis of wound healing. Biotechniques 32 (2002) 548
49. Underwood R.A., Gibran N.S., Muffley L.A., et al. Color subtractive-computer-assisted image analysis for quantification of cutaneous nerves in a diabetic mouse model. J Histochem Cytochem 49 (2001) 1285
50. Erin N., and Clawson G.A. Parameters affecting substance P measurement in heart, lung, and skin. Biotechniques 37 (2004) 232
51. Hosoi J., Murphy G., Egan C., et al. Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide. Nature 363 (1993) 159
52. Ansel J.C., Kaynard A.H., Armstrong C.A., et al. Skin-nervous system interactions. J Investig Dermat 106 (1996) 198
53. Leibovich S.J., and Ross R. The role of the macrophage in wound repair. Am J Pathol 78 (1975) 71
54. Dimmeler S., Dernbach E., and Zeiher A.M. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration. FEBS Lett 477 (2000) 258
55. Tsou R., Fathke C., Wilson L., et al. Retroviral delivery of dominant-negative vascular endothelial growth factor receptor type 2 to murine wounds inhibits wound angiogenesis. Wound Repair Regen 10 (2002) 222
56. Poluha W., Schonhoff C.M., Harrington K.S., et al. A novel, nerve growth factor-activated pathway involving nitric oxide, p53, and p21WAF1 regulates neuronal differentiation of PC12 cells. J Biol Chem 272 (1997) 24002
57. Thippeswamy T., and Morris R. The roles of nitric oxide in dorsal root ganglion neurons. Ann NY Acad Sci 962 (2002) 103