Journal of Surgical Research
Volume 153, Issue 2 , Pages 201-209 , 15 May 2009

Substance P Enhances Wound Closure in Nitric Oxide Synthase Knockout Mice

Received 9 January 2008

References 

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

PII: S0022-4804(08)00272-2

doi: 10.1016/j.jss.2008.03.051

Journal of Surgical Research
Volume 153, Issue 2 , Pages 201-209 , 15 May 2009

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