Elevated circulation levels of an antiangiogenic serpin in patients with diabetic microvascular complications impair wound healing through suppression of Wnt signaling

Journal of Investigative Dermatology

Volumn 134, Issue 6, 2014, Pages 1725-1734

  McBride, Jeffrey D ^a,b   Jenkins, Alicia J ^b,c   Liu, Xiaochen ^a,b   Zhang, Bin ^a   Lee, Kyungwon ^a,b   Berry, William L ^a   Janknecht, Ralf ^a   Griffin, Courtney T ^a,d   Aston, Christopher E ^a   Lyons, Timothy J ^b   Tomasek, James J ^a   Ma, Jian Xing ^a,b  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA HEALTH SCIENCES CENTER   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; BETA CATENIN; CREATININE; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; HEMOGLOBIN A1C; KALLIKREIN; KALLISTATIN; LITHIUM CHLORIDE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MESSENGER RNA; SERINE PROTEINASE INHIBITOR; T CELL FACTOR PROTEIN; TISSUE KALLIKREIN; UNCLASSIFIED DRUG; VASCULOTROPIN A; WNT PROTEIN; LITHIUM; WNT3A PROTEIN;

ALBUMIN BLOOD LEVEL; AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY COMPLIANCE; ARTICLE; BLOOD VESSEL REACTIVITY; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; CORRELATION ANALYSIS; CREATININE BLOOD LEVEL; DERMAL MICROVASCULAR ENDOTHELIAL CELL; DERMIS; DISEASE EXACERBATION; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HAIR FOLLICLE; HAIR GROWTH; HEPG2 CELL LINE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEWBORN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PHENOTYPE; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SKIN BLOOD FLOW; SKIN INJURY; SKIN STRUCTURE; SKINFOLD THICKNESS; TRANSGENIC MOUSE; WNT SIGNALING PATHWAY; WOUND CLOSURE; WOUND HEALING; WOUND HEALING IMPAIRMENT; CELL PROLIFERATION; DIABETIC MICROANGIOPATHY; DIABETIC PATIENT; ENDOTHELIUM; ENZYME INHIBITION; GENE OVEREXPRESSION; HEMODYNAMICS; HYPEREMIA; MICROVASCULAR ENDOTHELIAL CELL; PRIORITY JOURNAL;

ADULT; ANIMALS; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; FEMALE; GENE EXPRESSION REGULATION; GENES, REPORTER; GLYCOGEN SYNTHASE KINASE 3; HAIR FOLLICLE; HUMANS; LITHIUM; MALE; MICE; MICE, TRANSGENIC; MICROCIRCULATION; MIDDLE AGED; NEOVASCULARIZATION, PATHOLOGIC; SERPINS; SKIN; TRANSCRIPTION, GENETIC; WNT SIGNALING PATHWAY; WOUND HEALING;

EID: 84900875019     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.40     Document Type: Article

References (50)

1. Barcelos LS, Duplaa C, Krankel N et al. (2009) Human CD133+ progenitor cells promote the healing of diabetic ischemic ulcers by paracrine stimulation of angiogenesis and activation of Wnt signaling. Circ Res 104:1095-102
2. Chao J, Schmaier A, Chen LM et al. (1996) Kallistatin, a novel human tissue kallikrein inhibitor: levels in body fluids, blood cells, and tissues in health and disease. J Lab Clin Med 127:612-20
3. Chao J, Tillman DM, Wang MY et al. (1986) Identification of a new tissuekallikrein-binding protein. Biochem J 239:325-31
4. Chen J, Stahl A, Krah NM et al. (2011) Wnt signaling mediates pathological vascular growth in proliferative retinopathy. Circulation 124:1871-81
5. Chen VC, Chao L, Pimenta DC et al. (2001) Identification of a major heparinbinding site in kallistatin. J Biol Chem 276:1276-84
6. Chen Y, Hu Y, Zhou T et al. (2009) Activation of the Wnt pathway plays a pathogenic role in diabetic retinopathy in humans and animal models. Am J Pathol 175:2676-85
7. Curtis CD, Griffin CT (2012) The chromatin-remodeling enzymes BRG1 and CHD4 antagonistically regulate vascular Wnt signaling. Mol Cell Biol 32:1312-20
8. DasGupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126:4557-68
9. Dawson DW, Volpert OV, Gillis P et al. (1999) Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285:245-8
10. Dejana E (2010) The role of wnt signaling in physiological and pathological angiogenesis. Circ Res 107:943-52
11. Enshell-Seijffers D, Lindon C, Kashiwagi M et al. (2010) Beta-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev Cell 18:633-42
12. Fathke C, Wilson L, Shah K et al. (2006) Wnt signaling induces epithelial differentiation during cutaneous wound healing. BMC Cell Biol 7:4
13. Festa E, Fretz J, Berry R et al. (2011) Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146:761-71
14. George SJ (2008) Wnt pathway: a new role in regulation of inflammation. Arterioscler Throm Vasc Biol 28:400-2
15. Goettig P, Magdolen V, Brandstetter H (2010) Natural and synthetic inhibitors of kallikrein-related peptidases (KLKs). Biochimie 92:1546-67
16. Griffin CT, Curtis CD, Davis RB et al. (2011) The chromatin-remodeling enzyme BRG1 modulates vascular Wnt signaling at two levels. Proc Natl Acad Sci USA 108:2282-7
17. Guo S, Arai K, Stins MF et al. (2009) Lithium upregulates vascular endothelial growth factor in brain endothelial cells and astrocytes. Stroke 40:652-5
18. He TC, Sparks AB, Rago C et al. (1998) Identification of c-MYC as a target of the APC pathway. Science 281:1509-12
19. Hoyt RE (2004) Peripheral arterial disease in people with diabetes: response to consensus statement. Diab Care 27:2095
20. Irving JA, Pike RN, Lesk AM et al. (2000) Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 10:1845-64
21. Ito M, Yang Z, Andl T et al. (2007) Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447:316-20
22. Jenkins AJ, McBride JD, Januszewski AS et al. (2010) Increased serum kallistatin levels in type 1 diabetes patients with vascular complications. J Angiogenes Res 2:19
23. Kaga S, Zhan L, Altaf E et al. (2006) Glycogen synthase kinase-3beta/betacatenin promotes angiogenic and anti-apoptotic signaling through the induction of VEGF, Bcl-2 and survivin expression in rat ischemic preconditioned myocardium. J Mol Cell Cardiol 40:138-47
24. Kostler E, Porst H, Wollina U (2005) Cutaneous manifestations of metabolic diseases: uncommon presentations. Clin Dermatol 23:457-64
25. Liu X, Zhang B, McBride JD et al. (2013) Antiangiogenic and antineuroinflammatory effects of kallistatin through interactions with the canonical wnt pathway. Diabetes 62:4228-38
26. MacDonald BT, Tamai K, He X (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17:9-26
27. Margolis DJ, Malay DS, Hoffstad OJ et al. (2011) Prevalence of Diabetes, Diabetic Foot Ulcer, and Lower Extremity Amputation Among Medicare Beneficiaries, 2006 to 2008: Data Points #1. In: Data Points Publication Series: Rockville, MD
28. Masckauchan TN, Kitajewski J (2006) Wnt/frizzled signaling in the vasculature: new angiogenic factors in sight. Physiology (Bethesda) 21:181-8
29. McMahon GA, Petitclerc E, Stefansson S et al. (2001) Plasminogen activator inhibitor-1 regulates tumor growth and angiogenesis. J Biol Chem 276:33964-8
30. Miao RQ, Agata J, Chao L et al. (2002) Kallistatin is a new inhibitor of angiogenesis and tumor growth. Blood 100:3245-52
31. Monteiro-Soares M, Boyko EJ, Ribeiro J et al. (2012) Predictive factors for diabetic foot ulceration: a systematic review. Diab Metab Res Rev 28:574-600
32. Nissen NN, Polverini PJ, Koch AE et al. (1998) Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 152:1445-52
33. Parmalee NL, Kitajewski J (2008) Wnt signaling in angiogenesis. Curr Drug Targets 9:558-64
34. Petrofsky J, Prowse M, Lohman E (2008) The influence of ageing and diabetes on skin and subcutaneous fat thickness in different regions of the body. J Appl Res 8:55-61
35. Petrofsky JS, Bains GS, Prowse M et al. (2009) The influence of age and diabetes on the skin blood flow response to local pressure. Med Sci Monit 15:CR325-31
36. Phng LK, Potente M, Leslie JD et al. (2009) Nrarp coordinates endothelial Notch and Wnt signaling to control vessel density in angiogenesis. Dev Cell 16:70-82
37. Rajamani K, Colman PG, Li LP et al. (2009) Effect of fenofibrate on amputation events in people with type 2 diabetes mellitus (FIELD study): a prespecified analysis of a randomised controlled trial. Lancet 373:1780-8
38. Schmidt B, Horsley V (2012) Unravelling hair follicle-adipocyte communication. Exp Dermatol 21:827-30
39. Sick S, Reinker S, Timmer J et al. (2006) WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314:1447-50
40. Tseng CH (2006) Prevalence of lower-extremity amputation among patients with diabetes mellitus: is height a factor? CMAJ 174:319-23
41. Tur E, Yosipovitch G, Bar-On Y (1991) Skin reactive hyperemia in diabetic patients. A study by laser Doppler flowmetry. Diab Care 14:958-62
42. Wang J, Takeuchi T, Tanaka S et al. (1999) A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J Clin Invest 103:27-37
43. Whyte JL, Smith AA, Helms JA (2012) Wnt signaling and injury repair. Cold Spring Harb Perspect Biol 4:a008078
44. Whyte JL, Smith AA, Liu B et al. (2013) Augmenting endogenous wnt signaling improves skin wound healing. PloS One 8:e76883
45. Wolf WC, Harley RA, Sluce D et al. (1999) Localization and expression of tissue kallikrein and kallistatin in human blood vessels. J Histochem Cytochem 47:221-8
46. Wu X, Shen QT, Oristian DS et al. (2011) Skin stem cells orchestrate directional migration by regulating microtubule-ACF7 connections through GSK3beta. Cell 144:341-52
47. Xiong W, Tang CQ, Zhou GX et al. (1992) In vivo catabolism of human kallikrein-binding protein and its complex with tissue kallikrein. J Lab Clin Med 119:514-21
48. Zerlin M, Julius MA, Kitajewski J (2008) Wnt/Frizzled signaling in angiogenesis. Angiogenesis 11:63-9
49. Zhang B, Ma JX (2010) Wnt pathway antagonists and angiogenesis. Protein Cell 1:898-906
50. Zhang X, Gaspard JP, Chung DC (2001) Regulation of vascular endothelial growth factor by the Wnt and K-ras pathways in colonic neoplasia. Cancer Res 61:6050-4