Activated protein C stimulates proliferation, migration and wound closure, inhibits apoptosis and upregulates MMP-2 activity in cultured human keratinocytes

Experimental Cell Research

Volumn 299, Issue 1, 2004, Pages 119-127

  Xue, Meilang ^a   Thompson, Patrick ^a   Kelso, Ian ^a   Jackson, Chris ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Activated protein C; Apoptosis; Keratinocyte; Matrix metalloproteinase; Migration; Proliferation; Wound healing

Indexed keywords

ACTIVATED PROTEIN C; GELATINASE A; GELATINASE B; ILOMASTAT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MATRIX METALLOPROTEINASE INHIBITOR;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; KERATINOCYTE; NEWBORN; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STATISTICAL SIGNIFICANCE; UPREGULATION; WOUND CLOSURE;

EID: 4043156336     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2004.05.015     Document Type: Article

References (52)

1. Esmon C.T. The anticoagulant and anti-inflammatory roles of the protein C anticoagulant pathway. J. Autoimmun. 15:2000;113-116
2. Esmon C.T. The normal role of activated protein C in maintaining homeostasis and its relevance to critical illness. Crit. Care. 5(Suppl. 2):2001;S7-S12
3. Murakami K., Okajima K., Uchiba M., Johno M., Nakagaki T., Okabe H., Takatsuki K. Activated protein C prevents LPS-induced pulmonary vascular injury by inhibiting cytokine production. Am. J. Physiol. 272:1997;L197-L202
4. Uchiba M., Okajima K., Murakami K., Johno M., Okabe H., Takatsuki K. Effect of human urinary thrombomodulin on endotoxin-induced intravascular coagulation and pulmonary vascular injury in rats. Am. J. Hematol. 54:1997;118-123
5. Yuksel M., Okajima K., Uchiba M., Horiuchi S., Okabe H. Activated protein C inhibits lipopolysaccharide-induced tumor necrosis factor-alpha production by inhibiting activation of both nuclear factor-kappa B and activator protein-1 in human monocytes. Thromb. Haemostasis. 88:2002;267-273
6. Joyce D.E., Grinnell B.W. Recombinant human activated protein C attenuates the inflammatory response in endothelium and monocytes by modulating nuclear factor-kappaB. Crit. Care Med. 30:2002;S288-S293
7. Joyce D.E., Gelbert L., Ciaccia A., DeHoff B., Grinnell B.W. Gene expression profile of antithrombotic protein C defines new mechanisms modulating inflammation and apoptosis. J. Biol. Chem. 276:2001;11199-11203
8. Cheng T., Liu D., Griffin J.H., Fernandez J.A., Castellino F., Rosen E.D., Fukudome K., Zlokovic B.V. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat. Med. 9:2003;338-342
9. Nguyen M., Arkell J., Jackson C.J. Activated protein C directly activates human endothelial gelatinase A. J. Biol. Chem. 275:2000;9095-9098
10. Ravanti L., Kahari V.M. Matrix metalloproteinases in wound repair (review). Int. J. Mol. Med. 6:2000;391-407
11. Bikle D.D., Ng D., Tu C.L., Oda Y., Xie Z. Calcium- and vitamin D-regulated keratinocyte differentiation. Mol. Cell. Endocrinol. 177:2001;161-171
12. Dransfield D.T., Griner R.D., Ray S., Keskintepe M., Bollag W.B. 8-Cl-adenosine induces growth arrest without differentiation of primary mouse epidermal keratinocytes. J. Invest. Dermatol. 117:2001;1588-1593
13. Norris D.A., Ryan S.B., Kissinger R.M., Fritz K.A., Boyce S.T. Systematic comparison of antibody-mediated mechanisms of keratinocyte lysis in vitro. J. Immunol. 135:1985;1073-1079
14. Orlidge A., D'Amore P.A. Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J. Cell Biol. 105:1987;1455-1462
15. Herron G.S., Banda M.J., Clark E.J., Gavrilovic J., Werb Z. Secretion of metalloproteinases by stimulated capillary endothelial cells: II. Expression of collagenase and stromelysin activities is regulated by endogenous inhibitors. J. Biol. Chem. 261:1986;2814-2818
16. Ketabchi A., MacRobert A., Speight P.M., Bennett J.H. Induction of apoptotic cell death by photodynamic therapy in human keratinocytes. Arch. Oral Biol. 43:1998;143-149
17. Makela M., Larjava H., Pirila E., Maisi P., Salo T., Sorsa T., Uitto V.J. Matrix metalloproteinase 2 (gelatinase A) is related to migration of keratinocytes. Exp. Cell Res. 251:1999;67-78
18. Thomas G.J., Poomsawat S., Lewis M.P., Hart I.R., Speight P.M., Marshall J.F. alpha v beta 6 Integrin upregulates matrix metalloproteinase 9 and promotes migration of normal oral keratinocytes. J. Invest. Dermatol. 116:2001;898-904
19. Tuschil A., Lam C., Haslberger A., Lindley I. Interleukin-8 stimulates calcium transients and promotes epidermal cell proliferation. J. Invest. Dermatol. 99:1992;294-298
20. Grossman R.M., Krueger J., Yourish D., Granelli-Piperno A., Murphy D.P., May L.T., Kupper T.S., Sehgal P.B., Gottlieb A.B. Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc. Natl. Acad. Sci. U. S. A. 86:1989;6367-6371
21. Hennings H., Michael D., Cheng C., Steinert P., Holbrook K., Yuspa S.H. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell. 19:1980;245-254
22. Broad T.E., Ham R.G. Growth and adipose differentiation of sheep preadipocyte fibroblasts in serum-free medium. Eur. J. Biochem. 135:1983;33-39
23. Valyi-Nagy I.T., Murphy G.F., Mancianti M.L., Whitaker D., Herlyn M. Phenotypes and interactions of human melanocytes and keratinocytes in an epidermal reconstruction model. Lab. Invest. 62:1990;314-324
24. Hamuro M., Polan J., Natarajan M., Mohan S. High glucose induced nuclear factor kappa B mediated inhibition of endothelial cell migration. Atherosclerosis. 162:2002;277-287
25. Kucharczak J., Simmons M.J., Fan Y., Gelinas C. To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene. 22:2003;8961-8982
26. Jacinto A., Martinez-Arias A., Martin P. Mechanisms of epithelial fusion and repair. Nat. Cell Biol. 3:2001;E117-E123
27. Garlick J.A., Taichman L.B. Fate of human keratinocytes during reepithelialization in an organotypic culture model. Lab. Invest. 70:1994;916-924
28. Lavker R.M., Matoltsy A.G. Substructure of keratohyalin granules of the epidermis as revealed by high resolution electron microscopy. J. Ultrastruct. Res. 35:1971;575-581
29. Kirchberg K., Lange T.S., Klein E.C., Jungtaubl H., Heinen G., Meyer-Ingold W., Scharffetter-Kochanek K. Induction of beta 1 integrin synthesis by recombinant platelet-derived growth factor (PDGF-AB) correlates with an enhanced migratory response of human dermal fibroblasts to various extracellular matrix proteins. Exp. Cell Res. 220:1995;29-35
30. Brown R.A., Sethi K.K., Gwanmesia I., Raemdonck D., Eastwood M., Mudera V. Enhanced fibroblast contraction of 3D collagen lattices and integrin expression by TGF-beta1 and -beta3: mechanoregulatory growth factors? Exp. Cell Res. 274:2002;310-322
31. Esmon C.T., Xu J., Gu J.M., Qu D., Laszik Z., Ferrell G., Stearns-Kurosawa D.J., Kurosawa S., Taylor F.B. Jr., Esmon N.L. Endothelial protein C receptor. Thromb. Haemostasis. 82:1999;251-258
32. Riewald M., Petrovan R.J., Donner A., Mueller B.M., Ruf W. Activation of endothelial cell protease activated receptor 1 by the protein C pathway. Science. 296:2002;1880-1882
33. Feistritzer C., Sturn D.H., Kaneider N.C., Djanani A., Wiedermann C.J. Endothelial protein C receptor-dependent inhibition of human eosinophil chemotaxis by protein C. J. Allergy Clin. Immunol. 112:2003;375-381
34. Salo T., Makela M., Kylmaniemi M., Autio-Harmainen H., Larjava H. Expression of matrix metalloproteinase-2 and -9 during early human wound healing. Lab. Invest. 70:1994;176-182
35. Peled Z.M., Phelps E.D., Updike D.L., Chang J., Krummel T.M., Howard E.W., Longaker M.T. Matrix metalloproteinases and the ontogeny of scarless repair: the other side of the wound healing balance. Plast. Reconstr. Surg. 110:2002;801-811
36. Soo C., Shaw W.W., Zhang X., Longaker M.T., Howard E.W., Ting K. Differential expression of matrix metalloproteinases and their tissue-derived inhibitors in cutaneous wound repair. Plast. Reconstr. Surg. 105:2000;638-647
37. Roman E., Wilhelmi I., Colomina J., Villar J., Cilleruelo M.L., Nebreda V., Del Alamo M., Sanchez-Fauquier A. Acute viral gastroenteritis: proportion and clinical relevance of multiple infections in Spanish children. J. Med. Microbiol. 52:2003;435-440
38. Kahari V.M., Saarialho-Kere U. Matrix metalloproteinases in skin. Exp. Dermatol. 6:1997;199-213
39. Martin P. Wound healing - Aiming for perfect skin regeneration. Science. 276:1997;75-81
40. Charvat S., Chignol M.C., Souchier C., Le Griel C., Schmitt D., Serres M. Cell migration and MMP-9 secretion are increased by epidermal growth factor in HaCaT-ras transfected cells. Exp. Dermatol. 7:1998;184-190
41. Makela M., Sorsa T., Uitto V.J., Salo T., Teronen O., Larjava H. The effects of chemically modified tetracyclines (CMTs) on human keratinocyte proliferation and migration. Adv. Dent. Res. 12:1998;131-135
42. McQuibban G.A., Gong J.H., Wong J.P., Wallace J.L., Clark-Lewis I., Overall C.M. Matrix metalloproteinase processing of monocyte chemoattractant proteins generates CC chemokine receptor antagonists with anti-inflammatory properties in vivo. Blood. 100:2002;1160-1167
43. Hooper W.C., Phillips D.J., Renshaw M.A., Evatt B.L., Benson J.M. The up-regulation of IL-6 and IL-8 in human endothelial cells by activated protein C. J. Immunol. 161:1998;2567-2573
44. Schmidt-Supprian M., Murphy C., While B., Lawler M., Kapurniotu A., Voelter W., Smith O., Bernhagen J. Activated protein C inhibits tumor necrosis factor and macrophage migration inhibitory factor production in monocytes. Eur. Cytokine Network. 11:2000;407-413
45. Kono T., Tanii T., Furukawa M., Mizuno N., Taniguchi S., Ishii M., Hamada T. Effects of human recombinant tumor necrosis factor-alpha (TNF-alpha) on the proliferative potential of human keratinocytes cultured in serum-free medium. J. Dermatol. 17:1990;409-413
46. Cho A., Reidy M.A. Matrix metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ. Res. 91:2002;845-851
47. Amendt C., Mann A., Schirmacher P., Blessing M. Resistance of keratinocytes to TGF{beta}-mediated growth restriction and apoptosis induction accelerates re-epithelialization in skin wounds. J. Cell Sci. 115:2002;2189-2198
48. Li L., Kruszewski F.H., Punnonen K., Tucker R.W., Yuspa S.H., Hennings H. Strontium induces murine keratinocyte differentiation in vitro in the presence of serum and calcium. J. Cell. Physiol. 154:1993;643-653
49. Menon G.K., Grayson S., Elias P.M. Ionic calcium reservoirs in mammalian epidermis: ultrastructural localization by ion-capture cytochemistry. J. Invest. Dermatol. 84:1985;508-512
50. Leigh I.M., Purkis P.E., Whitehead P., Lane E.B. Monospecific monoclonal antibodies to keratin 1 carboxy terminal (synthetic peptide) and to keratin 10 as markers of epidermal differentiation. Br. J. Dermatol. 129:1993;110-119
51. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326(Pt. 1):1997;1-16
52. Mosnier L.O., Griffin J.H. Inhibition of staurosporine-induced apoptosis of endothelial cells by activated protein C requires protease-activated receptor-1 and endothelial cell protein C receptor. Biochem. J. 373:2003;65-70