Carnosine enhances diabetic wound healing in the db/db mouse model of type 2 diabetes

Amino Acids

Volumn 43, Issue 1, 2012, Pages 127-134

  Ansurudeen, Ishrath ^a   Sunkari, Vivekananda Gupta ^a   Grünler, Jacob ^a   Peters, Verena ^b   Schmitt, Claus Peter ^b   Catrina, Sergiu Bogdan ^a   Brismar, Kerstin ^a   Forsberg, Elisabete Alcantara ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Centre for Pediatric and Adolescent Medicine   (Germany)

Author keywords

Carnosine; db db mice; Diabetic wound healing; Human dermal fibroblast; Human dermal microvascular endothelial cells

Indexed keywords

CARNOSINE; GLUCOSE; GROWTH FACTOR; HISTAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE GENE; DRUG BLOOD LEVEL; DRUG EFFECT; GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN FIBROBLAST; SYNTHESIS; WOUND; WOUND HEALING;

ANIMALS; CARNOSINE; CELL LINE; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; RANDOM ALLOCATION; SKIN; WOUND HEALING;

MUS;

EID: 84862765718     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-012-1269-z     Document Type: Article

References (41)

1. C Agarwal Z Britton D Alaseirlis Y Li J Wang 2006 Healing and normal fibroblasts exhibit differential proliferation, collagen production, α-SMA expression, and contraction Ann Biomed Eng 34 4 653 659 10.1007/s10439-006- 9090-z 16568347 10.1007/s10439-006-9090-z
2. Bradbury P, Rae K (1996) Connective tissues and stains. In: Bancroft JD, Stevens A (eds) Theory and practice of histological techniques, 4th edition. Churchill Livingstone, New York, pp 113-137
3. S Barrientos O Stojadinovic MS Golinko H Brem M Tomic-Canic 2008 Perspective article: growth factors and cytokines in wound healing Wound Repair Regen 16 5 585 601 10.1111/j.1524-475X.2008.00410.x 19128254 10.1111/j.1524-475X.2008.00410.x
4. F Bhora B Dunkin S Batzri H Aly B Bass A Sidawy J Harmon 1995 Effect of growth factors on cell proliferation and epithelialization in human skin J Surg Res 59 236 244 7543631 10.1006/jsre.1995.1160 1:CAS:528:DyaK2MXnvFSmsr0%3D
5. M Bitar 1997 Insulin-like growth factor-1 reverses diabetes-induced wound healing impairment in rats Horm Metab Res 29 383 386 9288575 10.1055/s-2007-979060 1:CAS:528:DyaK2sXlsFGrur4%3D (Pubitemid 27362062)
6. M Bitar Z Labbad 1996 Transforming growth factor-beta and insulin-like growth factor-I in relation to diabetes-induced impairment of wound healing J Surg Res 61 113 119 8769952 10.1006/jsre.1996.0090 1:CAS:528:DyaK28Xhslyls7c%3D (Pubitemid 26066038)
7. IR Botusan VG Sunkari O Savu AI Catrina J Grünler S Lindberg T Pereira S Ylä-Herttuala L Poellinger K Brismar S-B Catrina 2008 Stabilization of HIF-1α is critical to improve wound healing in diabetic mice Proc Natl Acad Sci 105 49 19426 19431 19057015 10.1073/pnas.0805230105 1:CAS:528:DC%2BD1cXhsFamu7vK
8. S Catrina K Okamoto T Pereira K Brismar L Poellinger 2004 Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function Diabetes 53 3226 3232 15561954 10.2337/diabetes.53.12.3226 1:CAS:528: DC%2BD2cXhtVOls7bN (Pubitemid 39564499)
9. D Ceradini A Kulkarni M Callaghan O Tepper N Bastidas M Kleinman J Capla R Galiano J Levine G Gurtner 2004 Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 Nat Med 10 858 864 15235597 10.1038/nm1075 1:CAS:528:DC%2BD2cXmtFWrtr0%3D (Pubitemid 39070860)
10. CH Cho HK Sung KT Kim HG Cheon GT Oh HJ Hong OJ Yoo GY Koh 2006 COMP-angiopoietin-1 promotes wound healing through enhanced angiogenesis, lymphangiogenesis, and blood flow in a diabetic mouse model Proc Natl Acad Sci USA 103 13 4946 4951 16543381 10.1073/pnas.0506352103 1:CAS:528: DC%2BD28XjsVGls7g%3D
11. S Cuzzocrea T Genovese M Failla G Vecchio M Fruciano E Mazzon R Di Paola C Muià C La Rosa N Crimi E Rizzarelli C Vancheri 2007 Protective effect of orally administered carnosine on bleomycin-induced lung injury Am J Physiol Lung Cell Mol Physiol 292 5 L1095 L1104 17220373 10.1152/ajplung.00283.2006 1:CAS:528:DC%2BD2sXls1yhs7s%3D (Pubitemid 47086285)
12. T Fedorova M Macletsova A Kulikov M Stepanova A Boldyrev 2006 Carnosine protects from the oxidative stress induced by prenatal hypoxia Dokl Biol Sci 408 207 210 16909979 10.1134/S001249660603001X 1:STN:280:DC%2BD28vosFyrtA%3D%3D (Pubitemid 43988324)
13. D Fitzpatrick H Fisher 1982 Carnosine, histidine, and wound healing Surgery 91 56 60 7054908 1:STN:280:DyaL387gvVagsA%3D%3D (Pubitemid 12212550)
14. AA Fouad MA-A El-Rehany HK Maghraby 2007 The hepatoprotective effect of carnosine against ischemia/reperfusion liver injury in rats Eur J Pharmacol 572 1 61 68 17610873 10.1016/j.ejphar.2007.06.010 1:CAS:528:DC%2BD2sXhtVCitrfO (Pubitemid 47374680)
15. H Galkowska U Wojewodzka W Olszewski 2006 Chemokines, cytokines, and growth factors in keratinocytes and dermal endothelial cells in the margin of chronic diabetic foot ulcers Wound Repair Regen 14 558 565 17014667 10.1111/j.1743-6109.2006.00155.x (Pubitemid 44470072)
16. M Grant J Jerdan T Merimee 1987 Insulin-like growth factor-I modulates endothelial cell chemotaxis J Clin Endocrinol Metab 65 370 371 3597713 10.1210/jcem-65-2-370 1:CAS:528:DyaL2sXkvFSrt7s%3D (Pubitemid 17103028)
17. DG Greenhalgh 2003 Wound healing and diabetes mellitus Clin Plast Surg 30 37 45 12636214 10.1016/S0094-1298(02)00066-4 (Pubitemid 36288299)
18. Y Guney U Turkcu A Hicsonmez M Andrieu H Guney A Bilgihan C Kurtman 2006 Carnosine may reduce lung injury caused by radiation therapy Med Hypotheses 66 957 959 16406688 10.1016/j.mehy.2005.11.023 1:CAS:528:DC%2BD28XhtlGgu70%3D (Pubitemid 43207655)
19. S Guo LA DiPietro 2010 Factors affecting wound healing J Dent Res 89 3 219 229 20139336 10.1177/0022034509359125 1:CAS:528:DC%2BC3cXjtFOnsLc%3D
20. Khanna S, Biswas S, Shang Y, Collard E, Azad A, Kauh C, Bhasker V, Gordillo G, Sen C, Roy S (2010) Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 5(3):e9539
21. M Kucia J Ratajczak M Ratajczak 2005 Bone marrow as a source of circulating CXCR4 + tissue-committed stem cells Biol Cell 97 133 146 15656779 10.1042/BC20040069 1:CAS:528:DC%2BD2MXhtlSrtb4%3D (Pubitemid 40298268)
22. ML Lamers MES Almeida M Vicente-Manzanares AF Horwitz MF Santos 2011 High glucose-mediated oxidative stress impairs cell migration PLoS One 6 8 e22865 21826213 10.1371/journal.pone.0022865 1:CAS:528:DC%2BC3MXhtFWitLrK
23. K Nagai T Suda K Kawasaki S Mathuura 1986 Action of carnosine and beta-alanine on wound healing Surgery 100 815 821 3095942 1:STN:280: DyaL2s%2Fktlaksw%3D%3D (Pubitemid 17193026)
24. M Peppa P Stavroulakis SA Raptis 2009 Advanced glycoxidation products and impaired diabetic wound healing Wound Repair Regen 17 4 461 472 19614910 10.1111/j.1524-475X.2009.00518.x
25. Peters V, Schmitt C, Zschocke J, Gross M-L, Brismar K, Forsberg E (2011) Carnosine treatment largely prevents alterations of renal carnosine metabolism in diabetic mice. Amino Acids. doi: 10.1007/s00726-011-1046-4
26. P Quinn A Boldyrev V Formazuyk 1992 Carnosine: its properties, functions and potential therapeutic applications Mol Aspects Med 13 379 444 9765790 10.1016/0098-2997(92)90006-L 1:CAS:528:DyaK3sXksVSju70%3D (Pubitemid 23152963)
27. Reddy VP, Garrett MR, Perry G, Smith MA (2005) Carnosine: a versatile antioxidant and antiglycating agent. Sci Aging Knowl Environ (18):pe12
28. E Riedl H Koeppel F Pfister V Peters S Sauerhoefer P Sternik P Brinkkoetter H Zentgraf G Navis RH Henning J Van Den Born SJL Bakker B Janssen FJ van der Woude BA Yard 2010 N-Glycosylation of carnosinase influences protein secretion and enzyme activity Diabetes 59 8 1984 1990 20460427 10.2337/db09-0868 1:CAS:528:DC%2BC3cXhtVOlsbvE
29. PR Roberts KW Black JT Santamauro GP Zaloga 1998 Dietary peptides improve wound healing following surgery Nutrition 14 3 266 269 10.1016/s0899-9007(97) 00468-1 9583369 10.1016/S0899-9007(97)00468-1 1:CAS:528:DyaK1cXivFahu7k%3D (Pubitemid 28185920)
30. J Schönherr 2002 Analysis of products of animal origin in feeds by determination of carnosine and related dipeptides by high-performance liquid chromatography J Agric Food Chem 50 1945 1950 11902938 10.1021/jf0112116 (Pubitemid 34259993)
31. S Schreml RM Szeimies L Prantl S Karrer M Landthaler P Babilas 2010 Oxygen in acute and chronic wound healing Br J Dermatol 163 2 257 268 20394633 10.1111/j.1365-2133.2010.09804.x 1:STN:280:DC%2BC3cjgslWktQ%3D%3D
32. G Schultz J Davidson R Kirsner P Bornstein I Herman 2011 Dynamic reciprocity in the wound microenvironment Wound Repair Regen 19 134 148 21362080 10.1111/j.1524-475X.2011.00673.x
33. GL Semenza 2006 Regulation of physiological responses to continuous and intermittent hypoxia by hypoxia-inducible factor 1 Exp Physiol 91 5 803 806 10.1113/expphysiol.2006.033498 16740642 10.1113/expphysiol.2006.033498 1:CAS:528:DC%2BD28XhtFSisrvF (Pubitemid 44266576)
34. CK Sen 2009 Wound healing essentials: let there be oxygen Wound Repair Regen 17 1 1 18 19152646 10.1111/j.1524-475X.2008.00436.x
35. V Skulachev 1978 Membrane-linked energy buffering as the biological function of N +/K + gradient FEBS Lett 87 171 179 344066 10.1016/0014-5793(78) 80326-3 1:CAS:528:DyaE1cXhvVCkt74%3D (Pubitemid 8280814)
36. A Soneja M Drews T Malinski 2005 Role of nitric oxide, nitroxidative and oxidative stress in wound healing Pharmacol Rep 57 108 119 16415491
37. AA Tandara TA Mustoe 2004 Oxygen in wound healing-more than a nutrient World J Surg 28 3 294 300 14961188 10.1007/s00268-003-7400-2 (Pubitemid 38375532)
38. R Tsuboi C Shi C Sato G Cox H Ogawa 1995 Co-administration of insulin-like growth factor (IGF)-I and IGF-binding protein-1 stimulates wound healing in animal models J Invest Dermatol 104 199 203 7530269 10.1111/1523-1747.ep12612755 1:CAS:528:DyaK2MXktVejtr4%3D
39. AM Vincent JW Russell P Low EL Feldman 2004 Oxidative stress in the pathogenesis of diabetic neuropathy Endocr Rev 25 4 612 628 15294884 10.1210/er.2003-0019 1:CAS:528:DC%2BD2cXns1Ght78%3D (Pubitemid 39096072)
40. M Vizioli O Almeida 1978 Effects of carnosine on the development of rat sponge-induced granulation. I. General morphology and glycosaminoglycans histophotometr Cell Mol Biol Incl Cyto Enzymol 23 267 273 737675 1:CAS:528:DyaE1MXhvVSrtb0%3D (Pubitemid 9085432)
41. M Vizioli G Blumen O Almeida C Munhoz 1983 Effects of carnosine on the development of rat sponge-induced granulation tissue. II. Histoautoradiographic observations on collagen biosynthesis Cell Mol Biol Incl Cyto Enzymol 29 1 9 1:CAS:528:DyaL3sXks1ChtLg%3D (Pubitemid 13066227)