Migration of keratinocytes is impaired on glycated collagen I
Corresponding Author
Keisuke Morita MD
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Keisuke Morita, MD, Department of Dermatology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashiku, Fukuoka 812-8582, Japan. Email: [email protected].Search for more papers by this authorKazunori Urabe
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorYoichi Moroi
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorTetsuya Koga
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorRyuji Nagai
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorSeiko Horiuchi
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorMasutaka Furue
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorCorresponding Author
Keisuke Morita MD
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Keisuke Morita, MD, Department of Dermatology, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashiku, Fukuoka 812-8582, Japan. Email: [email protected].Search for more papers by this authorKazunori Urabe
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorYoichi Moroi
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorTetsuya Koga
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorRyuji Nagai
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorSeiko Horiuchi
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorMasutaka Furue
From the Department of Dermatology a , Graduate School of Medical Sciences, Kyushu University; Department of Dermatology b , Fukuoka Red Cross Hospital, Fukuoka; and Department of Biochemistry c , Kumamoto University School of Medicine, Kumamoto, Japan.
Search for more papers by this authorAbstract
Advanced glycation end products are the chemical modification of proteins induced by sugars in a hyperglycemic condition. Extracellular matrix proteins are prominent targets of nonenzymatic glycation because of their slow turnover rates. The aim of this study was to investigate the influence of nonenzymatic glycation of type I collagen on the migration of keratinocytes. The migration of keratinocytes was dramatically promoted on native type I collagen-coated dishes compared with that on uncoated dishes. When type I collagen was glycated with glycolaldehyde, large amounts of advanced glycation end products were produced; the glycated collagen I-coated dishes did not promote the migration of keratinocytes. Glycated collagen I did not affect the proliferative capacity of keratinocytes. However, the adhesion of keratinocytes to glycated collagen I was profoundly diminished in a glycation intensity-dependent manner. α2β1 integrin is responsible for the migration and adhesion of keratinocytes to type I collagen. Pretreatment with glycated collagen I did not affect the expression level or functional activity of α2β1 integrin on keratinocytes. These findings suggest that in the presence of glycated collagen I, keratinocytes lose their adhesive and migratory abilities. As the glycation did not modify the α2β1 integrin on keratinocytes, it is suggested that glycation may diminish the binding capacity of type I collagen.
References
- 1 Kumar S, Ashe HA, Parnell LN, Fernando DJ, Tsigos C, Young RJ, Ward JD, Boulton AJ. The prevalence of foot ulceration and its correlates in type 2 diabetic patients: a population-based study. Diabet Med 1994; 11: 480–4.
- 2 Neil HA, Thompson AV, Thorogood M, Fowler GH, Mann JI. Diabetes in the elderly: the Oxford Community Diabetes Study. Diabet Med 1989; 6: 608–13.
- 3 Walters DP, Gatling W, Mullee MA, Hill RD. The distribution and severity of diabetic foot disease: a community study with comparison to a non-diabetic group. Diabet Med 1992; 9: 354–8.
- 4 Ferringer T, Miller F 3rd. Cutaneous manifestations of diabetes mellitus. Dermatol Clin 2002; 20: 483–92.
- 5 Huntley AC. The cutaneous manifestations of diabetes mellitus. J Am Acad Dermatol 1982; 7: 427–55.
- 6 Shen S, Wertheimer E, Sampson SR, Tennenbaum T. Characterization of glucose transport system in keratinocytes. insulin and IGF-1 differentially affect specific transporters. J Invest Dermatol 2000; 115: 949–54.DOI: 10.1046/j.1523-1747.2000.00161.x
- 7 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: 1627–35.
- 8 Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR, Baynes JW. Accumulation of Maillard reaction products in skin collagen in diabetes and aging. J Clin Invest 1993; 91: 2463–9.
- 9 Sensi M, Morano S, Sagratella E, Castaldo P, Morelli S, Vetri M, Caltabiano V, Purrello F, Andreani D, Vecci E, Di Mario U. Advanced glycation end product levels in eye lenses, aorta, and tail tendon in transplanted diabetic inbred Lewis rats. Transplantation 2001; 72: 1370–5.DOI: 10.1097/00007890-200110270-00006
- 10 Singh R, Barden A, Mori T, Beilin L. Advanced glycation end-products: a review. Diabetologia 2001; 44: 129–46.DOI: 10.1007/s001250051591
- 11 Tarsio JF, Wigness B, Rhode TD, Rupp WM, Buchwald H, Furcht LT. Nonenzymatic glycation of fibronectin and alterations in the molecular association of cell matrix and basement membrane components in diabetes mellitus. Diabetes 1985; 34: 477–84.
- 12 Lyons TJ, Bailie KE, Dyer DG, Dunn JA, Baynes JW. Decrease in skin collagen glycation with improved glycemic control in patients with insulin-dependent diabetes mellitus. J Clin Invest 1991; 87: 1910–5.
- 13 McCance DR, Dyer DG, Dunn JA, Bailie KE, Thorpe SR, Baynes JW, Lyons TJ. Maillard reaction products and their relation to complications in insulin-dependent diabetes mellitus. J Clin Invest 1993; 91: 2470–8.
- 14 Monnier VM, Bautista O, Kenny D, Sell DR, Fogarty J, Dahms W, Cleary PA, Lachin J, Genuth S. Skin collagen glycation, glycoxidation, and crosslinking are lower in subjects with long-term intensive versus conventional therapy of type 1 diabetes: relevance of glycated collagen products versus HbA1c as markers of diabetic complications. DCCT skin collagen ancillary study group. Diabetes control and complications trial. Diabetes 1999; 48: 870–80.
- 15 Paul RG, Bailey AJ. Glycation of collagen. the basis of its central role in the late complications of ageing and diabetes. Int J Biochem Cell Biol 1996; 28: 1297–310.DOI: 10.1016/S1357-2725(96)00079-9
- 16 Reiser KM. Nonenzymatic glycation of collagen in aging and diabetes. Proc Soc Exp Biol Medical 1998; 218: 23–37.
- 17 Salmela PI, Oikarinen AI, Ukkola O, Karjalainen A, Linnaluoto M, Puukka R, Ryhanen L. Improved metabolic control in patients with non-insulin-dependent diabetes mellitus is associated with a slower accumulation of glycation products in collagen. Eur J Clin Invest 1995; 25: 494–500.
- 18 Vishwanath V, Frank KE, Elmets CA, Dauchot PJ, Monnier VM. Glycation of skin collagen in type I diabetes mellitus. Correlation with long-term complications. Diabetes 1986; 35: 916–21.
- 19 O'Toole EA. Extracellular matrix and keratinocyte migration. Clin Exp Dermatol 2001; 26: 525–30.DOI: 10.1046/j.1365-2230.2001.00891.x
- 20 Horiuchi S, Araki N, Morino Y. Immunochemical approach to characterize advanced glycation end products of the Maillard reaction. Evidence for the presence of a common structure. J Biol Chem 1991; 266: 7329–32.
- 21 Nagai R, Matsumoto K, Ling X, Suzuki H, Araki T, Horiuchi S. Glycolaldehyde, a reactive intermediate for advanced glycation end products, plays an important role in the generation of an active ligand for the macrophage scavenger receptor. Diabetes 2000; 49: 1714–23.
- 22 Glomb MA, Monnier VM. Mechanism of protein modification by glyoxal and glycolaldehyde, reactive intermediates of the Maillard reaction. J Biol Chem 1995; 270: 10017–26.DOI: 10.1074/jbc.270.17.10017
- 23 Knight CG, Morton LF, Onley DJ, Peachey AR, Messent AJ, Smethurst PA, Tuckwell DS, Farndale RW, Barnes MJ. Identification in collagen type I of an integrin alpha2 beta1-binding site containing an essential GER sequence. J Biol Chem 1998; 273: 33287–94.DOI: 10.1074/jbc.273.50.33287
- 24 Reiser KM, Amigable MA, Last JA. Nonenzymatic glycation of type I collagen. The effects of aging on preferential glycation sites. J Biol Chem 1992; 267: 24207–16.
- 25 Herman WH. Clinical evidence: glycaemic control in diabetes. BMJ 1999; 319: 104–6.
- 26 Wertheimer E, Spravchikov N, Trebicz M, Gartsbein M, Accili D, Avinoah I, Nofeh-Moses S, Sizyakov G, Tennenbaum T. The regulation of skin proliferation and differentiation in the IR null mouse: implications for skin complications of diabetes. Endocrinology 2001; 142: 1234–41.DOI: 10.1210/en.142.3.1234
- 27
Blakytny R,
Jude EB,
Martin Gibson J,
Boulton AJ,
Ferguson MW.
Lack of insulin-like growth factor 1 (IGF1) in the basal keratinocyte layer of diabetic skin and diabetic foot ulcers.
J Pathol
2000; 190: 589–94.
10.1002/(SICI)1096-9896(200004)190:5<589::AID-PATH553>3.0.CO;2-T CAS PubMed Web of Science® Google Scholar
- 28 Aukhil I. Biology of wound healing. Periodontology 2000, 2000; 22: 44–50.DOI: 10.1034/j.1600-0757.2000.2220104.x
- 29 Martin P. Wound healing—aiming for perfect skin regeneration. Science 1997; 276: 75–81.DOI: 10.1126/science.276.5309.75
- 30 Paul RG, Bailey AJ. The effect of advanced glycation end-product formation upon cell–matrix interactions. Int J Biochem Cell Biol 1999; 31: 653–60.DOI: 10.1016/S1357-2725(99)00023-0
- 31 Gilcrease MZ, Hoover RL. Human monocyte interactions with non-enzymatically glycated collagen. Diabetologia 1992; 35: 160–4.DOI: 10.1007/BF00402549
- 32 Monboisse JC, Rittie L, Lamfarraj H, Garnotel R, Gillery P. In vitro glycoxidation alters the interactions between collagens and human polymorphonuclear leucocytes. Biochem J 2000; 350 Part 3: 777–83.DOI: 10.1042/0264-6021:3500777
- 33 Ivanov GI, Chaushev TA, Dakovska LN, Kyurkchiev SD. Increased adhesion of lymphoid cells to glycated proteins. Int J Biochem Cell Biol 1999; 31: 797–804.DOI: 10.1016/S1357-2725(99)00025-4
- 34 Kim JP, Zhang K, Kramer RH, Schall TJ, Woodley DT. Integrin receptors and RGD sequences in human keratinocyte migration: unique anti-migratory function of alpha 3 beta 1 epiligrin receptor. J Invest Dermatol 1992; 98: 764–70.DOI: 10.1111/1523-1747.ep12499947
- 35 Knight CG, Morton LF, Peachey AR, Tuckwell DS, Farndale RW, Barnes MJ. The collagen-binding A-domains of integrins alpha (1) beta (1) and alpha (2) beta (1) recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 2000; 275: 35–40.DOI: 10.1074/jbc.275.1.35
- 36 Kramer RZ, Bella J, Mayville P, Brodsky B, Berman HM. Sequence dependent conformational variations of collagen triple-helical structure. Nat Struct Biol 1999; 6: 454–7.
- 37 Xu Y, Gurusiddappa S, Rich RL, Owens RT, Keene DR, Mayne R, Hook A, Hook M. Multiple binding sites in collagen type I for the integrins alpha1beta1 and alpha2beta1. J Biol Chem 2000; 275: 38981–9.DOI: 10.1074/jbc.M007668200
- 38 Fujimori E. Cross-linking and fluorescence changes of collagen by glycation and oxidation. Biochim Biophys Acta 1989; 998: 105–10.
- 39 Chen JR, Takahashi M, Kushida K, Suzuki M, Suzuki K, Horiuchi K, Nagano A. Direct detection of crosslinks of collagen and elastin in the hydrolysates of human yellow ligament using single-column high performance liquid chromatography. Anal Biochem 2000; 278: 99–105.
- 40 Sajithlal GB, Chithra P, Chandrakasan G. Advanced glycation end products induce crosslinking of collagen in vitro. Biochim Biophys Acta 1998; 1407: 215–24.
- 41 Kuzuya M, Asai T, Kanda S, Maeda K, Cheng XW, Iguchi A. Glycation cross-links inhibit matrix metalloproteinase-2 activation in vascular smooth muscle cells cultured on collagen lattice. Diabetologia 2001; 44: 433–6.DOI: 10.1007/s001250051640
- 42 Sims TJ, Rasmussen LM, Oxlund H, Bailey AJ. The role of glycation cross-links in diabetic vascular stiffening. Diabetologia 1996; 39: 946–51.
- 43 Tanaka S, Avigad G, Brodsky B, Eikenberry EF. Glycation induces expansion of the molecular packing of collagen. J Mol Biol 1988; 203: 495–505.DOI: 10.1016/0022-2836(88)90015-0
- 44 Kim BM, Eichler J, Reiser KM, Rubenchik AM, Da Silva LB. Collagen structure and nonlinear susceptibility: effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity. Lasers Surg Med 2000; 27: 329–35.DOI: 10.1002/1096-9101(2000)27:4<329::AID-LSM5>3.0.CO;2-C
Citing Literature
