Nitric oxide triggers enhanced induction of vascular endothelial growth factor expression in cultured keratinocytes (HaCaT) and during cutaneous wound repair

FASEB Journal

Volumn 13, Issue 14, 1999, Pages 2002-2014

  Frank, Stefan ^a   Stallmeyer, Birgit ^a   Kämpfer, Heiko ^a   Kolb, Nicole ^a   Pfeilschifter, Josef ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

Gene expression regulation; Inducible nitric oxide synthase; Skin

Indexed keywords

CYTOKINE; GAMMA INTERFERON; MESSENGER RNA; N(G) METHYLARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN BIOPSY; WOUND HEALING;

ANIMALIA;

EID: 0032721941     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.14.2002     Document Type: Article

References (57)

1. Clark, R. A. F. (1996) Wound repair: overview and general considerations. In The Molecular and Cellular Biology of Wound Repair (Clark, R. A. F., ed) pp. 3-50, Plenum Press, New York and London
2. Moncada, S., Palmer, R. M. J, and Higgs, E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142
3. Nathan, C. (1992) Nitric oxide as a secretory product of mammalian cells. FASEB J. 6, 3051-3064
4. Bredt, D. S., and Snyder, S. H. (1994) Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195
5. Knowles, R. G., and Moncada, S. (1994) Nitric oxide synthases in mammals. Biochem. J. 298, 249-258
6. Nathan, C., and Xie, Q. (1994) Regulation of biosynthesis of nitric oxide. J. Biol. Chem. 269, 13725-13728
7. Kröncke, K. D., Fehsel, H., and Kolb-Bachofen, V. (1995) Inducible nitric oxide synthase and its product nitric oxide, a small molecule with complex biological activities. Biol. Chem. Hoppe Seyler 376, 327-343
8. Back, K. J., Thiel, B. A., Lucas, S., and Stuehr, D. J. (1993) Macrophage nitric oxide synthase subunits. Purification, characterization, and role of prosthetic groups and substrate in regulating their association into a dimeric enzyme. J. Biol. Chem. 268, 21120-21129
9. Klatt, P., Schmidt, K., Uray, G., and Mayer, B. (1993) Multiple catalytic functions of brain nitric oxide synthase. Biochemical characterization, cofactor-requirement, and the role of N omega-hydroxy-L-arginine as an intermediate. J. Biol. Chem. 268, 14781-14787
10. Goldsmith, P. C., Leslie, T. A., Hayes, N. A., Levell, N. J., Dowd, P. M., and Foreman J. C. (1996) Inhibitors of nitric oxide synthase in human skin. J. Invest. Dermatol 106, 113-118
11. Weller, R., Pattullo, S., Smith, L., Golden, M., Ormerod, A., and Benjamin, N. (1996) Nitric oxide is generated on the skin surface by reduction of sweat nitrate. J. Invest. Dermatol. 107, 327-331
12. Romero-Graillet, C., Aberdam, E., Clement, M., Ortonne, J. P., and Balloti, R. (1997) Nitric oxide produced by ultraviolet-irradiated keratinocytes stimulates melanogenesis. J. Clin. Invest. 99, 635-642
13. Yamasaki, K., Edington, H. D. J., McClosky, C., Tzeng, E., Lizonova, A., Kovesdi, I., Steed, D. L., and Billiar, T. R. (1998) Reversal of impaired wound repair in iNOS-deficient mice by topical adenoviral-mediated iNOS gene transfer. J. Clin. Invest. 101, 967-971
14. Frank, S., Madlener, M., Pfeilschifter, J., and Werner, S. (1998) Induction of inducible nitric oxide synthase and its corresponding tetrahydrobiopterin-cofactor-synthesizing enzyme GTP-cyclohydrolase I during cutaneous wound repair. J. Invest. Dermatol. 111, 1058-1064
15. Beck, K. F., Eberhardt, W., Frank, S., Huwiler, A., Messmer, U. K., Mühl, H., and Pfeilschifter, J. (1999) Inducible NO synthase: role in cellular signalling. J. Exp. Biol. 202, 645-653
16. Chin, K., Kurashima, Y., Ogura, T., Tajiri, H., Yoshida, S., and Esumi, H. (1997) Induction of vascular endothelial growth factor by nitric oxide in human glioblastoma and hepatocellular carcinoma cells. Oncogene 15, 437-442
17. Tsurumi, Y., Murohara, T., Krasinski, K., Chen, D., Witzenbichler, B., Kearny, M., Couffinhal, T., and Isner J. M. (1997) Reciprocal relation between VEGF and NO in the regulation of endothelial integrity. Nature Med. 3, 879-886
18. Remick, D. G., and Villarete, L. (1996) Regulation of cytokine gene expression by reactive oxygen and reactive nitrogen intermediates. J. Leukoc. Biol. 59, 471-475
19. Frank, S., Stallmeyer, B., Kämpfer, H., Schaffner, C., and Pfeilschifter, J. (1999) Differential regulation of vascular endothelial growth factor and its receptor fms-like-tyrosine kinase is mediated by nitric oxide in rat renal mesangial cells. Biochem. J. 338, 367-374
20. Houck, K. A., Ferrara, N., Winer, J., Cachianes, G., Li, B., and Leung, D. (1991) The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. 5, 1806-1814
21. Leung, D. W., Cachianes, G., Kuang, W.-J., Goeddel, D. V., and Ferrara, N. (1989) Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309
22. Keck, P. J., Hauser, S., Krivi, G., Sanzo, K., Warren, T., Feder, J., and Connolly, D. T. (1989) Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science 246, 1309-1312
23. Gospodarowicz, D., Abraham, J. A., and Schilling, J. (1989) Isolation and characterization of a vascular endothelial cell mitogen produced by pituitary-derived folliculo stellate cells. Proc. Natl Acad. Sci. USA 86, 7311-7315
24. Connolly, D. T., Heuvelmam, D. M., Nelson, R., Olander, J. V., Eppley, B. L., Delfino, J. J., Siegel, N. R., Leimgruber, R. M., and Feder, J. (1989) Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J. Clin. Invest. 84, 1470-1478
25. Brown, L. F., Van de Water, L., Harvey, V. S., and Dvorak, H. F. (1988) Fibrinogen influx and accumulation of cross-linked fibrin in healing wounds and in tumor stroma. Am. J. Pathol. 130, 455-461
26. Nissen, N. N., Polverini, P. J., Koch, A. E., Volin, M. V., Gamelli, R. L., and DiPietro, L. A. (1998) Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am. J. Pathol. 152, 1445-52
27. Brown, L. F., Yeo, K.-T., Berse, B., Yeo, T.-K., Senger, D. R., Dvorak, H. F., and Van de Water, L. (1992) Expression of vascular permeability factor (vascular endothelial growth factor) by epidermal keratinocytes during wound healing. J. Exp. Med. 176, 1375-1379
28. Frank, S., Hübner, G., Breier, G., Longaker, M. T., Greenhalgh, D. G., and Werner, S. (1995) Regulation of vascular endothelial growth factor expression in cultured keratinocytes. Implications for normal and impaired wound healing. J. Biol. Chem. 270, 12607-12613
29. Coleman, D. L. (1982) Diabetes-obesity syndromes in mice. Diabetes 31, 1-6
30. Moore, W. M., Webber, R. K., Jerome, G. M., Tjoeng, F. S., Misko, T. P., and Currie, M. G. (1994) L-N6-(1-iminoethyl) lysine: a selective inhibitor of inducible nitric oxide synthase. J. Med. Chem. 37, 3886-3888
31. Stenger, S., Thüring, H., Röllinghoff, M., Manning, P., and Bogdan, C. (1995) L-N6-(1-iminoethyl)-lysine potently inhibits inducible nitric oxide synthase and is superior to NG-monomethyl-arginine in vitro and in vivo. Eur. J. Pharmacol. 294, 703-712
32. Diefenbach, A., Schindler, H., Donhauser, N., Lorenz, E., Laskay, T., MacMicking, J., Röllinghoff, M., Gresser, I., and Bogdan, C. (1998) Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 8, 77-87
33. Chomczynski, P., and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159
34. Werner, S., Peters, K. G., Longaker, M. T., Fuller-Pace, F., Banda, M. J., and Williams, L. T. (1992) Large induction of keratinocyte growth factor expression in the dermis during wound healing. Proc. Natl. Acad. Sci. USA 89, 6896-6900
35. Breier, G., Albrecht, U., Sterrer, S., and Risau, W. (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114, 521-532
36. Weindel, K., Marme, D., and Weich, H. A. (1992) AIDS-associated Kaposi's sarcoma cells in culture express vascular endothelial growth factor. Biochem. Biophys. Res. Commun. 183, 1167-1174
37. Boukamp, P., Petrussevska, R. T., Breitkreuz, D., Hornung, J., Markham, A., and Fusenig, N. E. (1988) Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106, 761-771
38. Hart, T. W. (1985) Some observations concerning the S-nitroso and S-phenylsulphonyl derivatives of L-cysteine and glutathione. Tetrahedron Lett. 26, 2013-2016
39. Frank, S., Kolb, N., Werner, E. R., and Pfeilschifter, J. (1998) Coordinated induction of inducible nitric oxide synthase and GTP-cyclohydrolase I is dependent on inflammatory cytokines and interferon-gamma in HaCaT keratinocytes: implications for the model of cutaneous wound repair. J. Invest. Dermatol. 111, 1065-1071
40. Garrido, C., Saule, S., and Gospodarowicz, D. (1993) Transcriptional regulation of vascular endothelial growth factor gene expression in ovarian bovine granulosa cells. Growth Factors 8, 109-117
41. Rubin, J. S., Osada, H., Finch, P. W., Taylor, W. G., Rudikoff, S., and Aaronson, S. A. (1989) Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc. Natl. Acad. Sci. USA 86, 802-806
42. Werner, S., Smola, H., Liao, X., Longaker, M. T., Krieg, T., Hofschneider, P. H., and Williams, L. T. (1994) The function of KGF in morphogenesis of epithelium and reepithelialization of wounds. Science 266, 819-822
43. Reichner, S., Meszaros, A. J., Louis, C. A., Henry, W. L., Mastrofrancesco, B., Martin, B.-A., and Albina, J. E. (1999) Molecular and metabolic evidence for the restricted expression of inducible nitric oxide synthase in healing wounds. Am. J. Pathol. 154, 1097-1104
44. Martin, P. (1997) Wound healing - aiming for perfect skin regeneration. Science 276, 75-81
45. Shimizu, Y., Sakai, M., Umemura, Y., and Ueda, H. (1997) 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, 80-87
46. Rowe, A., Farrell, A. M., and Bunker, C. B. (1997) Constitutive endothelial and inducible nitric oxide synthase in inflammatory dermatoses. Br. J. Dermatol. 136, 18-23
47. Bruch-Gerharz, D., Fehsel, K., Suschek, C., Michel, G., Ruzicka, T., and Kolb-Bachofen, V. (1996) A proinflammatory activity of interleukin 8 in human skin: expression of the inducible nitric oxide synthase in psoriatic lesions and cultured keratinocytes. J. Exp. Med. 184, 2007-2012
48. Sirsjö, A., Karlsson, M., Gidlöf, A., Rollman, O., and Törmä, H. (1996) Increased expression of inducible nitric oxide synthase in psoriatic skin and cytokine-stimulated cultured keratinocytes. Br. J. Dermatol. 134, 643-648
49. Ormerod, A. D., Weller, R., Copeland, P., Benjamin, N., Ralston, S. H., Grabowski, P., and Herriot, R. (1998) Detection of nitric oxide and nitric oxide synthases in psoriasis. Arch. Dermatol Res. 290, 3-8
50. Barbul, A. S., Lazarou, A., Efron, D. T., Wasserkrug, H. L., and Efron, G. (1990) Arginine enhances wound healing and lymphocyte immune responses in humans. Surgery 108, 331-336
51. Kirk, S. J., Hurson, M., Regan, M. C., Holt, D. R., Wasserkrug, H. L., and Barbul, A. (1993) Arginine stimulates wound healing and immune function in elderly human beings. Surgery 114, 155-159
52. Seifter, E., Rettura, G., Barbul, A., and Levenson, S. M. (1978) Arginine: an essential amino acid for injured rats. Surgery 84, 224-230
53. Albina, J. E., Mills, C. D., Henry, W. L., and Caldwell, M. D. (1990) Temporal expression of different pathways of 1-arginine metabolism in healing wounds. J. Immunol. 144, 3877-3880
54. de Vries, C., Escobedo, J. A., Ueno, H., Houck, K., Ferrara, N., and Williams, L. T. (1992) The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science 255, 989-991
55. Detmar, M., Yeo, K. T., Nagy, J. A., Van de Water, L., Brown, L. F., Berse, B., Elicker, B. M., Ledbetter, S., and Dvorak, H. F. (1995) Keratinocyte-derived vascular permeability factor (vascular endothelial growth factor) is a potent mitogen for dermal microvascular endothelial cells. J. Invest. Dermatol 105, 44-50
56. Wong, H. L., and Wahl, S. M. (1989) Tissue repair and fibrosis. In Human Monocytes (Zembala, M., and Asherson, G. L., eds) pp. 383-394, Academic Press, New York
57. Xiong, M., Elson, G., Legarda, D., and Leibovich, S. J. (1998) Production of vascular endothelial growth factor by murine macrophages. Regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am. J. Pathol. 153, 587-598