Cell motility in models of wounded human skin is improved by Gap27 despite raised glucose, insulin and IGFBP-5

Experimental Cell Research

Volumn 319, Issue 4, 2013, Pages 390-401

  Wright, Catherine S ^a   Berends, Rebecca F ^a   Flint, David J ^b   Martin, Patricia E M ^a  

^a GLASGOW CALEDONIAN UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

Author keywords

Connexin; IGF; Keratinocyte; Peptide; Skin; Wound

Indexed keywords

CONNEXIN 43; GLUCOSE; INSULIN; MESSENGER RNA; SOMATOMEDIN BINDING PROTEIN 5; SOMATOMEDIN C; GAP 27 PEPTIDE; GAP JUNCTION PROTEIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL STIMULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SKIN INJURY; WOUND CLOSURE; CELL CULTURE; CELL MOTION; CULTURE TECHNIQUE; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; EVALUATION; FUNCTIONS OF THE SKIN AND ITS APPENDAGES; NEWBORN; OSMOLARITY; PHYSIOLOGY; THEORETICAL MODEL; UPREGULATION; VALIDATION STUDY; WOUND HEALING;

CELL CULTURE TECHNIQUES; CELL MIGRATION ASSAYS; CELL MOVEMENT; CELLS, CULTURED; CONNEXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUCOSE; HUMANS; INFANT, NEWBORN; INSULIN; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; KERATINOCYTES; MODELS, THEORETICAL; OSMOLAR CONCENTRATION; SKIN PHYSIOLOGICAL PHENOMENA; UP-REGULATION; WOUND HEALING;

MLCS; MLOWN;

EID: 84875523960     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.12.013     Document Type: Article

References (63)

1. Kretz M., Euwens C., Hombach S., Eckardt D., Teubner B., Traub O., Willecke K., Ott T. Altered connexin expression and wound healing in the epidermis of connexin-deficient mice. J. Cell. Sci. 2003, 116:3443-3452.
2. Brandner J.M., Houdek P., Husing B., Kaiser C., Moll I. Connexins 26, 30, and 43: differences among spontaneous, chronic, and accelerated human wound healing. J. Invest. Dermatol 2004, 122:1310-1320.
3. Di W.L., Rugg E.L., Leigh I.M., Kelsell D.P. Multiple epidermal connexins are expressed in different keratinocyte subpopulations including connexin 31. J. Invest. Dermatol 2001, 117:958-964.
4. Evans W.H., Martin P.E. Gap junctions: structure and function (Review). Mol. Membr. Biol. 2002, 19:121-136.
5. Elias L.A., Wang D.D., Kriegstein A.R. Gap junction adhesion is necessary for radial migration in the neocortex. Nature 2007, 448:901-907.
6. Machtaler S., Dang-Lawson M., Choi K., Jang C., Naus C.C., Matsuuchi L. The gap junction protein Cx43 regulates B-lymphocyte spreading and adhesion. J. Cell. Sci. 2011, 124:2611-2621.
7. Qiu C., Coutinho P., Frank S., Franke S., Law L.Y., Martin P., Green C.R., Becker D.L. Targeting connexin43 expression accelerates the rate of wound repair. Curr. Biol. 2003, 13:1697-1703.
8. Mori R., Power K.T., Wang C.M., Martin P., Becker D.L. Acute downregulation of connexin43 at wound sites leads to a reduced inflammatory response, enhanced keratinocyte proliferation and wound fibroblast migration. J. Cell. Sci. 2006, 119:5193-5203.
9. Wang C.M., Lincoln J., Cook J.E., Becker D.L. Abnormal connexin expression underlies delayed wound healing in diabetic skin. Diabetes 2007, 56:2809-2817.
10. Wright C.S., van Steensel M.A., Hodgins M.B., Martin P.E. Connexin mimetic peptides improve cell migration rates of human epidermal keratinocytes and dermal fibroblasts in vitro. Wound Repair Regen. 2009, 17:240-249.
11. Pollok S., Pfeiffer A.C., Lobmann R., Wright C.S., Moll I., Martin P.E., Brandner J.M. Connexin 43 mimetic peptide Gap27 reveals potential differences in the role of Cx43 in wound repair between diabetic and non-diabetic cells. J. Cell. Mol. Med. 2011, 15:861-873.
12. Evans W.H., Boitano S. Connexin mimetic peptides: specific inhibitors of gap-junctional intercellular communication. Biochem. Soc. Trans. 2001, 29:606-612.
13. Leybaert L., Braet K., Vandamme W., Cabooter L., Martin P.E., Evans W.H. Connexin channels, connexin mimetic peptides and ATP release. Cell. Commun. Adhes. 2003, 10:251-257.
14. Werner S., Grose R. Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 2003, 83:835-870.
15. Rudman S.M., Philpott M.P., Thomas G.A., Kealey T. The role of IGF-I in human skin and its appendages: morphogen as well as mitogen?. J. Invest. Dermatol 1997, 109:770-777.
16. Todorovic V., Pesko P., Micev M., Bjelovic M., Budec M., Micic M., Brasanac D., Ilic-Stojanovic O. Insulin-like growth factor-I in wound healing of rat skin. Regul. Pept. 2008, 150:7-13.
17. Brown D.L., Kane C.D., Chernausek S.D., Greenhalgh D.G. Differential expression and localization of insulin-like growth factors I and II in cutaneous wounds of diabetic and nondiabetic mice. Am. J. Pathol. 1997, 151:715-724.
18. Semenova E., Koegel H., Hasse S., Klatte J.E., Slonimsky E., Bilbao D., Paus R., Werner S., Rosenthal N. Overexpression of mIGF-1 in keratinocytes improves wound healing and accelerates hair follicle formation and cycling in mice. Am. J. Pathol 2008, 173:1295-1310.
19. Hirsch T., Spielmann M., Velander P., Zuhaili B., Bleiziffer O., Fossum M., Steinstraesser L., Yao F., Eriksson E. Insulin-like growth factor-1 gene therapy and cell transplantation in diabetic wounds. J. Gene. Med. 2008, 10:1247-1252.
20. Beattie J., Allan G.J., Lochrie J.D., Flint D.J. Insulin-like growth factor-binding protein-5 (IGFBP-5): a critical member of the IGF axis. Biochem. J. 2006, 395:1-19.
21. Park I.S., Kiyomoto H., Alvarez F., Xu Y.C., Abboud H.E., Abboud S.L. Preferential expression of insulin-like growth factor binding proteins-1, -3, and -5 during early diabetic renal hypertrophy in rats. Am. J. Kidney. Dis. 1998, 32:1000-1010.
22. Bergman P.B., Moravski C.J., Edmondson S.R., Russo V.C., Bach L.A., Wilkinson-Berka J.L., Werther G.A. Expression of the IGF system in normal and diabetic transgenic (mRen-2)27 rat eye. Invest. Ophthalmol. Vis. Sci. 2005, 46:2708-2715.
23. Schaeffer V., Hansen K.M., Morris D.R., Abrass C.K. Reductions in laminin beta2 mRNA translation are responsible for impaired IGFBP-5-mediated mesangial cell migration in the presence of high glucose. Am. J. Physiol. Renal Physiol. 2010, 298:F314-322.
24. Pilewski J.M., Liu L., Henry A.C., Knauer A.V., Feghali-Bostwick C.A. Insulin-like growth factor binding proteins 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am. J. Pathol 2005, 166:399-407.
25. Yasuoka H., Jukic D.M., Zhou Z., Choi A.M., Feghali-Bostwick C.A. Insulin-like growth factor binding protein 5 induces skin fibrosis: A novel murine model for dermal fibrosis. Arthritis Rheum. 2006, 54:3001-3010.
26. Sorrell A.M., Shand J.H., Tonner E., Gamberoni M., Accorsi P.A., Beattie J., Allan G.J., Flint D.J. Insulin-like growth factor-binding protein-5 activates plasminogen by interaction with tissue plasminogen activator, independently of its ability to bind to plasminogen activator inhibitor-1, insulin-like growth factor-I, or heparin. J. Biol. Chem. 2006, 281:10883-10889.
27. Griffith T.M. Endothelium-dependent smooth muscle hyperpolarization: do gap junctions provide a unifying hypothesis?. Br. J. Pharmacol. 2004, 141:881-903.
28. Spravchikov N., Sizyakov G., Gartsbein M., Accili D., Tennenbaum T., Wertheimer E. Glucose effects on skin keratinocytes: implications for diabetes skin complications. Diabetes 2001, 50:1627-1635.
29. Bagdade J.D., Bierman E.L., Porte D. The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects. J. Clin. Invest. 1967, 46:1549-1557.
30. Easton J.A., Petersen J.S., Martin P.E. The anti-arrhythmic peptide AAP10 remodels Cx43 and Cx40 expression and function. Naunyn Schmiedebergs Arch. Pharmacol. 2009, 380:11-24.
31. Rivedal E., Leithe E. Connexin43 synthesis, phosphorylation, and degradation in regulation of transient inhibition of gap junction intercellular communication by the phorbol ester TPA in rat liver epithelial cells. Exp. Cell. Res. 2005, 302:143-152.
32. Boutinaud M., Shand J.H., Park M.A., Phillips K., Beattie J., Flint D.J., Allan G.J. A quantitative RT-PCR study of the mRNA expression profile of the IGF axis during mammary gland development. J. Mol. Endocrinol 2004, 33:195-207.
33. Martin P.E., Wall C., Griffith T.M. Effects of connexin-mimetic peptides on gap junction functionality and connexin expression in cultured vascular cells. Br. J. Pharmacol 2005, 144:617-627.
34. Wright C.S., Pollok S., Flint D.J., Brandner J.M., Martin P.E. The connexin mimetic peptide Gap27 increases human dermal fibroblast migration in hyperglycemic and hyperinsulinemic conditions in vitro. J. Cell. Physiol. 2012, 227:77-87.
35. Presland R.B., Dale B.A. Epithelial structural proteins of the skin and oral cavity: function in health and disease. Crit. Rev. Oral Biol. Med. 2000, 11:383-408.
36. Easton J.A., Donnelly S., Kamps M.A., Steijlen P.M., Martin P.E., Tadini G., Janssens R., Happle R., van Geel M., van Steensel M.A. Porokeratotic eccrine nevus may be caused by somatic connexin26 mutations. J. Invest. Dermatol. 2012, 132:2184-2191.
37. Donnelly S., English G., De Zwart-Storm E.A., Lang S., Van Steensel M.A., Martin P.E. Differential susceptibility of Cx26 mutations associated with epidermal dysplasias to peptidoglycan derived from Staphylococcus aureus and Staphylococcus epidermidis. Exp. Dermatol. 2012, 21:592-598.
38. Kandyba E.E., Hodgins M.B., Martin P.E. A murine living skin equivalent amenable to live-cell imaging: analysis of the roles of connexins in the epidermis. J. Invest. Dermatol. 2008, 128:1039-1049.
39. Blakytny R., Jude E. The molecular biology of chronic wounds and delayed healing in diabetes. Diabet. Med. 2006, 23:594-608.
40. Solan J.L., Lampe P.D. Connexin43 phosphorylation: structural changes and biological effects. Biochem. J. 2009, 419:261-272.
41. Lan C.C., Wu C.S., Kuo H.Y., Huang S.M., Chen G.S. Hyperglycaemic conditions hamper keratinocyte locomotion via sequential inhibition of distinct pathways: new insights on poor wound closure in patients with diabetes. Br. J. Dermatol. 2009, 160:1206-1214.
42. Thomas K., Kiwit M., Kerner W. Glucose concentration in human subcutaneous adipose tissue: comparison between forearm and abdomen. Exp. Clin. Endocrinol. Diabetes 1998, 106:465-469.
43. Schairer C., Hill D., Sturgeon S.R., Fears T., Pollak M., Mies C., Ziegler R.G., Hoover R.N., Sherman M.E. Serum concentrations of IGF-I, IGFBP-3 and c-peptide and risk of hyperplasia and cancer of the breast in postmenopausal women. Int. J. Cancer 2004, 108:773-779.
44. Hyde C., Hollier B., Anderson A., Harkin D., Upton Z. Insulin-like growth factors (IGF) and IGF-binding proteins bound to vitronectin enhance keratinocyte protein synthesis and migration. J. Invest. Dermatol. 2004, 122:1198-1206.
45. Kilani R.T., Guilbert L., Lin X., Ghahary A. Keratinocyte conditioned medium abrogates the modulatory effects of IGF-1 and TGF-beta1 on collagenase expression in dermal fibroblasts. Wound Repair Regen. 2007, 15:236-244.
46. Ko J.A., Yanai R., Morishige N., Takezawa T., Nishida T. Upregulation of connexin43 expression in corneal fibroblasts by corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 2009, 50:2054-2060.
47. Lin D., Boyle D.L., Takemoto D.J. IGF-I-induced phosphorylation of connexin 43 by PKCgamma: regulation of gap junctions in rabbit lens epithelial cells. Invest. Ophthalmol. Vis. Sci. 2003, 44:1160-1168.
48. Hatakeyama N., Kojima T., Iba K., Murata M., Thi M.M., Spray D.C., Osanai M., Chiba H., Ishiai S., Yamashita T., Sawada N. IGF-I regulates tight-junction protein claudin-1 during differentiation of osteoblast-like MC3T3-E1 cells via a MAP-kinase pathway. Cell. Tissue Res. 2008, 334:243-254.
49. Jia G., Mitra A.K., Cheng G., Gangahar D.M., Agrawal D.K., IGF-1 Angiotensin regulate connexin43 expression via ERK and p38 signaling pathways in vascular smooth muscle cells of coronary artery bypass conduits. J. Surg. Res. 2007, 142:137-142.
50. Aberg N.D., Blomstrand F., Aberg M.A., Bjorklund U., Carlsson B., Carlsson-Skwirut C., Bang P., Ronnback L., Eriksson P.S. Insulin-like growth factor-I increases astrocyte intercellular gap junctional communication and connexin43 expression in vitro. J. Neurosci. Res. 2003, 74:12-22.
51. Bradshaw S.L., Naus C.C., Zhu D., Kidder G.M., D'Ercole A.J., Han V.K Alterations in the synthesis of insulin-like growth factor binding proteins and insulin-like growth factors in rat C6 glioma cells transfected with a gap junction connexin43 cDNA. Regul. Pept. 1993, 48:99-112.
52. Sureshbabu A., Okajima H., Yamanaka D., Tonner E., Shastri S., Maycock J., Szymanowska M., Shand J., Takahashi S., Beattie J., Allan G., Flint D. IGFBP5 induces cell adhesion, increases cell survival and inhibits cell migration in MCF-7 human breast cancer cells. J. Cell. Sci. 2012, 125:1693-1705.
53. Yasuoka H., Zhou Z., Pilewski J.M., Oury T.D., Choi A.M., Feghali-Bostwick C.A. Insulin-like growth factor-binding protein-5 induces pulmonary fibrosis and triggers mononuclear cellular infiltration. Am. J. Pathol. 2006, 169:1633-1642.
54. Desplantez T., Verma V., Leybaert L., Evans W.H., Weingart R. Gap26, a connexin mimetic peptide, inhibits currents carried by connexin43 hemichannels and gap junction channels. Pharmacol. Res. 2012, 65:546-552.
55. Prochnow N., Dermietzel R. Connexons and cell adhesion: a romantic phase. Histochem. Cell. Biol. 2008, 130:71-77.
56. Cotrina M.L., Lin J.H., Nedergaard M. Adhesive properties of connexin hemichannels. Glia 2008, 56:1791-1798.
57. Palatinus J.A., Rhett J.M., Gourdie R.G. Enhanced PKCepsilon mediated phosphorylation of connexin43 at serine 368 by a carboxyl-terminal mimetic peptide is dependent on injury. Channels (Austin) 2011, 5.
58. Ghatnekar G.S., O'Quinn M.P., Jourdan L.J., Gurjarpadhye A.A., Draughn R.L., Gourdie R.G. Connexin43 carboxyl-terminal peptides reduce scar progenitor and promote regenerative healing following skin wounding. Regen. Med. 2009, 4:205-223.
59. Srinivas M. Pharmacology of Connexin Channels. Connexins: A Guide 2009, 207-224. Humanna Press, New York. H. Harris, D. Locke (Eds.).
60. Wang J., Ma M., Locovei S., Keane R.W., Dahl G. Modulation of membrane channel currents by gap junction protein mimetic peptides: size matters. Am. J. Physiol Cell Physiol. 2007, 293:C1112-1119.
61. Bruzzone R., Barbe M.T., Jakob N.J., Monyer H. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J. Neurochem. 2005, 92:1033-1043.
62. Robertson J., Lang S., Lambert P.A., Martin P.E. Peptidoglycan derived from Staphylococcus epidermidis induces Connexin43 hemichannel activity with consequences on the innate immune response in endothelial cells. Biochem. J. 2010, 432:133-143.
63. Wang N., De Bock M., Antoons G., Gadicherla A.K., Bol M., Decrock E., Evans W.H., Sipido K.R., Bukauskas F.F., Leybaert L. Connexin mimetic peptides inhibit Cx43 hemichannel opening triggered by voltage and intracellular Ca(2+) elevation. Basic. Res. Cardiol. 2012, 107:304.