The role of hypoxia-inducible factorin the syndrome of chronic lower limb ischemia and influence of diabetes mellitus on process of angiogenesis
https://doi.org/10.24884/1682-6655-2017-16-3-4-9
Abstract
In this review, we pay attention to the role of the hypoxia-inducible factor (HIF) in the development of response of the organism to hypoxia. Special attention is given to the regulation of the cell responses to hypoxia in chronic peripheral artery disease in patients with diabetes mellitus (DM). Cells can survive by activation of a transcription of genes, involved in angiogenesis, glucose metabolism and cell proliferation. Artificial rising of concentration and activity of HIF stimulates an angiogenesis and improves ulcers healing of the lower extremities. The data of the literature are provided on the possible methods of increasing HIF concentration in tissues, which could be a new way to stimulate wound healing in the patients with DM.
About the Authors
M. N. Kudykin
Federal State Budgetary Institution «Privolzhsky Federal Research Medical Centre»
Russian Federation
Russian Federation
V. V. Beschastnov
State budget health agency Nizhny Novgorod region «City Clinical Hospital No. 30, Moscow district of Nizhny Novgorod»
Russian Federation
Russian Federation
R. A. Deryabin
Federal State Budgetary Institution «Privolzhsky Federal Research Medical Centre»
Russian Federation
Russian Federation
G. E. Sheiko
Federal State Budgetary Institution «Privolzhsky Federal Research Medical Centre»
Russian Federation
Russian Federation
L. M. Celousova
Federal State Budgetary Institution «Privolzhsky Federal Research Medical Centre»
Russian Federation
Russian Federation
A. N. Belova
Federal State Budgetary Institution «Privolzhsky Federal Research Medical Centre»
Russian Federation
Russian Federation
References
1. Левченкова О. С. Нейропротективное действие антиоксидантов и умеренной гипоксии в режиме комбинированного прекондиционирования при ишемии головного мозга / О. С. Левченкова, В. Е. Новиков, Э. А. Парфенов, К. Н. Кулагин // Бюллетень эксперимент. биол. и мед. 2016. Т. 162. № 8. С. 173-177. doi: 10.1007/s10517-016-3578-9.
2. Лукьянова Л. Д., Кирова Ю. И., Сукоян Г. В. Сигнальные механизмы адаптации к гипоксии и их роль в системной регуляции // Биолог. мембраны. 2012. Т. 29. № 4. С. 238-252.
3. Серебровская Т. В. Гипоксия-индуцибельный фактор: роль в патофизиологии дыхания // Украин. пульмонол. журн. 2005. № 3. С. 77-81.
4. Aalaa M., Malazy O. T., Sanjari M. et al. Nurses' role in diabetic foot prevention and care. // J. Diabetes Metab. Disord. 2012. Vol. 11. P. 24. doi: 10.1186/2251-6581-11-24.
5. Alavi A., Sibbald R. G., Mayer D. et al. Diabetic foot ulcers: Part II. Management // J. Am. Acad. Dermatol. 2014. Vol. 70. № 1. P. 21.e1-2124. doi: 10.1016/j.jaad.2013.07.048.
6. Bakri F. G., Allan A. H., Khader Y. S. et al. Prevalence of Diabetic Foot Ulcer and its Associated Risk Factors among Diabetic Patients in Jordan // J. Med. J. 2012. Vol. 46. № 2. P. 118-125.
7. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis // Nature Medicine. 2000. Vol. 6. № 4. P. 389-395. doi: 10.1038/7465.
8. Catrina S. B., Okamoto K., Pereira T. et al. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function // Diabetes. 2004. Vol. 53. № 12. P. 3226-3232.
9. Ceradini D. J., Kulkarni A. R., Callaghan M. J. et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1 // Nat Med. 2004. Vol. 10 № 8. P. 858-864. doi: 10.1038/nm1075.
10. Conway E. M., Collen D., Carmeliet P. Molecular mechanisms of blood vessel growth // Cardiovascular Research. 2001. Vol. 49. № 3. P. 507-521. doi: 10.1016/s0008-6363(00)00281-9.
11. Eliceiri B. P., Paul R., Schwartzberg P. L. et al. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability // Molecular Cell. 1999. Vol. 4. № 6. P. 915-924. doi: 10.1016/s1097-2765(00)80221-x.
12. Gao W., Ferguson G., Connell P. et al. High glucose concentrations alter hypoxia-induced control of vascular smooth muscle cell growth via a HIF-1alpha-dependent pathway // J. Mol. Cell. Cardiol. 2007. Vol. 42. P. 609-619. doi: W.1016/j.yjmcc.2006.12.006.
13. Jiang B. H. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension / B. N. Jiang, G. L. Semenza, C. Bauer, H. H. Marti // Am. J. Physiol. 1996. Vol. 271. P. 1172-1180.
14. Kaelin W. G., Ratcliffe P. J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway // Molecular Cell. 2008. Vol. 30. № 4. P. 393-402. doi: 10.1016/j. molcel.2008.04.009.
15. Kelly B. D., Hackett S. F., Hirota K. et al. Cell type specific regulation ofangiogenic growth factor gene expression and induction of angiogenesis in nonischemic tissue by a constitutively active form of hypoxia-inducible factor 1 // Circ. Res. 2003. Vol. 93. № 11. P. 1074-1081. doi: 10.1161/01.RES.0000102937.50486.1B.
16. Lando D., Gorman J. J., Whitelaw M. L. et al. Oxygen-dependent regulation of hypoxiainducible factors by prolyl and asparaginyl hydroxylation // Eur. J. Biochem. 2003. Vol. 270. № 5. P. 781-790. doi: 10.1046/j.1432-1033.2003.03445.x.
17. Leone S., Pascale R., Vitale M. et al. Epidemiology of diabetic foot // Infez. Med. 2012. Vol. 20. Suppl. 1. P. 8-13.
18. Li J., Post M., Volk R. et al. PR39, a peptide regulator of angiogenesis // Nature Medicine. 2000. Vol. 61. P. 49-55. doi: 10.1038/71527.
19. Lindahl P. Endothelial-perivascular cell signaling in vascular development: lessons from knockout mice / P. Lindahl, M. Hellstrom, M. Kalen, C. Betsholtz // Current Opinion in Lipidology. 1998. Vol. 9. № 5. P. 407-411. doi: 10.1097/00041433-199810000-00004.
20. Maisonpierre P. C., Suri C., Jones P. F. et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis // Science. 1997. Vol. 277. № 5322. P. 55-60. doi: 10.1126/science.277.5322.55.
21. Manalo D. J., Rowan A., Lavoie T. et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1 // Blood. 2005 Jan. Vol. 105. № 2. P. 659-669. doi: 10.1182/blood-2004-07-2958.
22. Milkiewicz M., Pugh C. W., Egginton S. Inhibition of endogenous HIF inactivation induces angiogenesis in ischaemic skeletal muscles of mice // J. of Physiology. 2004. Vol. 560. № 1. P. 21-26. doi: 10.1113/jphysiol.2004.069757.
23. Mima A. Incretin-Based Therapy for Prevention of Diabetic Vascular Complications // J. of Diabetes Research. 2016. Vol. 2016. P. 1-12. doi: 10.1155/2016/1379274.
24. Nather A., Bee C. S., Huak C. Y. et al. Epidemiology of diabetic foot problems and predictive factors for limb loss // J. Diabetes Complications. 2008. Vol. 22. P. 77-82. doi: 10.1016/j.jdiacomp.2007.04.004.
25. Niemi H., Honkonen K., Korpisalo P. et al. HIF-1a and HIF-2a induce angiogenesis and improve muscle energy recovery // Eur. J. of Clinical Investigation. 2014. Vol. 44. № 10. P. 989-999. doi: 10.1111/eci.12333.
26. Patel T. H., Kimura H., Weiss C. R. et al. Constitutively active HIF-1 a improves perfusion and arterial remodeling in an endovascular model of limb ischemia // Cardiovascular Research. 2005. Vol. 68. № 1. P. 144-154. doi: 10.1016/j.cardiores.2005.05.002.
27. Podar K., Anderson K. C. The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications // Blood. 2005. Vol. 105 P. 1383-1395. doi: 10.1182/blood-2004-07-2909.
28. Potente M., Gerhardt H., Carmeliet P. Basic and therapeutic aspects of angiogenesis // Cell. 2011. Vol. 146. № 6. P. 873-887. doi: 10.1016/j.cell.2011.08.039.
29. Richard J. L., Schuldiner S. Epidemiology of diabetic foot problems // Rev. Med. Interne. 2008. Vol. 29. Suppl. 2. P. S222-S230. doi: 10.1016/S0248-8663(08)73949-3.
30. Ruthenborg R. J., Ban J., Wazir A. et al. Regulation of Wound Healing and Fibrosis by Hypoxia and Hypoxia-Inducible Factor-1 // Mol. Cells. 2014. Vol. 37. № 9. P. 637-643. doi: 10.14348/molcells.2014.0150.
31. Schofield C. J., Zhang Z. Structural and mechanistic studies on 2-oxoglutarate-dependent oxygenases and related enzymes // Current Opinion in Structural Biology. 1999. Vol. 9. № 6. P. 722-731. doi: 10.1016/S0959-440X(99)00036-6.
32. Semenza G. L. Hypoxia-inducible factors in physiology and medicine // Cell. 2012. Vol. 148. № 3. P. 399-408. doi: 10.1016/j.cell.2012.01.021.
33. Semenza G. L. O2 regulated gene expression: transcriptional control of cardiorespiratory physiology by HIF1 // J. Appl. Physiol. 2004. Vol. 96. № 3. P. 1173-1177. doi:10.1152/japplphysiol.00770.2003.
34. Semenza G. L., Wang G. L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation // Mol. Cell. Biol. 1992. Vol. 12. № 12. P. 5447-5454.
35. Skuli N., Liu L., Runge A. et al. Endothelial deletion of hypoxia-inducible factor-2a (HIF-2a) alters vascular function and tumor angiogenesis // Blood. 2009. Vol. 114. № 2. P. 469-477. doi: 10.1182/blood-2008-12-193581.
36. Thangarajah H., Vial I. H., Grogan R. H. et al. HIF-1alpha dysfunction in diabetes // Cell. Cycle. 2010. Vol. 9. № 1. P. 75-79. doi: 10.4161/cc.9.1.10371.
37. Thurston G., Rudge J. S., Ioffe E. et al. Angiopoietin-1 protects the adult vasculature against plasma leakage // Nature Medicine. 2000. Vol. 6. № 4. P. 460-463. doi: 10.1038/74725.
38. Wang K., Zheng J. Signaling regulation of fetoplacental angiogenesis // J. Endo. 2012. Vol. 212. P. 243-255. doi: 10.1530/JOE-11-0296. Epub 2011 Nov 21.
39. Ziegler D. Painful diabetic neuropathy: treatment and future aspects //Diabetes Metab. Res. Rev. 2008. Vol. 24. № 1. P. 52-57. doi: 10.1002/dmrr.817.
40. Zhang X., Yan X., Cheng L. et al. Wound healing improvement with PHD-2 silencedfibroblasts in diabetic mice //PLoS One. 2013. Vol. 8. № 12. P. 845-848. doi: 10.1371/journal.pone.0084548.eCollection2013.
41. Zimna A., Kurpisz M. Hypoxia-Inducible Factor-1 in Physiological and Pathophysiological Angiogenesis: Applications and Therapies // Biomed. Res. Int. 2015. Vol. 2015. Article ID. 549412. doi: 10.1155/2015/549412.
Review
For citations:
Kudykin M.N., Beschastnov V.V., Deryabin R.A., Sheiko G.E., Celousova L.M., Belova A.N. The role of hypoxia-inducible factorin the syndrome of chronic lower limb ischemia and influence of diabetes mellitus on process of angiogenesis. Regional blood circulation and microcirculation. 2017;16(3):4-9. (In Russ.) https://doi.org/10.24884/1682-6655-2017-16-3-4-9
Views:
1447
Email this article 
