Novosti
Khirurgii

 This journal is
indexed in Scopus
journal cover
android icon Android Applicaion

Year 2019 Vol. 27 No 1

REVIEWS

R.E. KALININ, I.A. SUCHKOV, A.S. PSHENNIKOV, S.A. VINOGRADOV

MARKERS OF ARTERIOVENOUS DIFFERENTIATION OF ENDOTHELIAL CELLS AND THEIR INFLUENCE ON ADAPTATION OF AUTOVENOUS CONDUITS IN MAIN ARTERIES RECONSTRUCTIVE SURGERY

Ryazan State Medical University, Ryazan,
The Russian Federation

Revascularization of the occluded arterial segments is currently the main treatment method in patients with critical limb ischemia. Discussions regarding the choice of the best conduit for the reconstructive procedures on the femoro-popliteal-tibial segments have been continuing over the last five decades. Autovenous conduits using the great saphenous vein remain the golden standard in vascular reconstructive surgery. However, up to 50% of autovenous transplants lose patency within 5 years. Reaction of venous conduit to arterial circulation and its morphofunctional changes are not fully described in present-day medical literature. Markers of embryonic arteriovenous differentiation of endothelial cells determining the faith of both arteries and veins have gained popularity within past years. Ephrin-B2 is specifically expressed in arterial endothelium while Eph-B4 is expressed in venous endothelial cells. Arterialization of the autovenous conduit is characterized by the loss of the venous marker Eph-B4 without obtaining the arterial marker Ephrin-B2, which is accompanied by the negative morphological remodeling of the venous wall, i.e. its thickening. Eph-B4 in venous endothelium interacts with a number of molecules including eNOS, caveolin and others, thus regulating the process of adaptation. Further studies of the adaptation of venous conduits to arterial circulation may help improve our understanding of this process and results of the autovenous reconstructive procedures.

Keywords: endothelium, autovenous bypass, arterialization of the venous conduit, adaptation of the autovenous conduit, atherosclerosis, endothelial dysfunction, eph-B4, ephrin-B2
p. 91-100 of the original issue
References
  1. Gavrilenko AV, Kotov AE, Kalinin VD, Krotovskiy MA. Modern techniques of vascular surgery in the treatment of the chronic lower limbs ischemia. Annaly Khirurgiia. 2016;21(1-2):26-31. doi: 10.18821/1560-9502-2016-21-1-26-31 (in Russ.)
  2. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-society consensus for the management of peripheral arterial disease (TASC II). J Vasc Surg. 2007 Jan;45(Suppl S):S5-67. doi: 10.1016/j.jvs.2006.12.037
  3. Natsional’nye rekomendatsii po vedeniiu patsientov s zabolevaniiami arterii nizhnikh konechnostei. Moscow, RF; 2013. 68 p. http://www.angiolsurgery.org/recommendations/2013/recommendations_LLA.pdf (in Russ.)
  4. Belov YuV, Vinokurov IA. The concept of surgical treatment of critical limb ischemia. Kardiologia i Serguch-Sosud Khirurgiia. 2015;8(5):9-13. doi: 10.17116/kardio2015859-13 (in Russ.)
  5. Isaji T, Hashimoto T, Yamamoto K, Santana JM, Yatsula B, Hu H, Bai H, Jianming G, Kudze T, Nishibe T, Dardik A. Improving the outcome of vein grafts: should vascular surgeons turn veins into arteries? Ann Vasc Dis. 2017 Mar 24;10(1):8-16. doi: 10.3400/avd.ra.17-00008
  6. Muto A, Model L, Ziegler K, Eghbalieh, Dardik A. Mechanisms of vein graft adaptation to the arterial circulation – insights into the neointimal algorithm and management strategies. Circ J. 2010;74(8):1501-12. doi: 10.1253/circj.cj-10-0495
  7. Kalinin RE, Suchkov IA, Mnikhovich MV, Kaktursky LV, Levitin AV, Isakov SA. Peculiarities of morphological imaging at the sites of vascular anastomosis at different periods of time fol-lowing lower extremity arterial reconstructive surgery. Morfol Vedomosti. 2013;(1):21-27. https://elibrary.ru/item.asp?id=21396754 (in Russ.)
  8. Owens CD. Adaptive changes in autogenous vein grafts for arterial reconstruction: clinical implications. J Vasc Surg. 2010 Mar;51(3):736-46. doi: 10.1016/j.jvs.2009.07.102
  9. Ambler GK, Twine CP. Graft type for femoro-popliteal bypass surgery. Cochrane Database Syst Rev. 2018 Feb;11(2):CD001487. doi: 10.1002/14651858.CD001487.pub3
  10. Ziegler KR, Muto A, Eghbalieh SD, Dardik A. Basic data related to surgical infrainguinal revascularization procedures: a twenty year update. Ann Vasc Surg. 2011 Apr;25(3):413-22. doi: 10.1016/j.avsg.2010.10.010
  11. Park C, Kim TM, Malik AB. Transcriptional regulation of endothelial cell and vascular development. Circ Res. 2013 May 10;112(10):1380-400. doi: 10.1161/CIRCRESAHA.113.301078
  12. Wang HU, Chen ZF, Anderson DJ. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 1998 May 29;93(5):741-53. doi: 10.1016/s0092-8674(00)81436-1
  13. Simons M, Eichmann A. Molecular controls of arterial morphogenesis. Circ Res. 2015 May 8;116(10):1712-24. doi: 10.1161/CIRCRESAHA.116.302953
  14. Fancher TT, Muto A, Fitzgerald TN, Magri D, Gortler D, Nishibe T, Dardik A. Control of blood vessel identity: from embryo to adult. Ann Vasc Dis. 2008;1(1):28-34. Published online 2008 Feb 15.doi: 10.3400/avd.AVDrev0701
  15. dela Paz NG, D’Amore PA.. Arterial versus venous endothelial cells. Cell Tissue Res. 2009 Jan;335(1):5-16. doi: 10.1007/s00441-008-0706-5.
  16. Kanaya K, Ii M, Okazaki T, Nakamura T, Horii-Komatsu M, Alev C, Akimaru H, Kawamoto A, Akashi H,Tanaka H, Asahi M, Asahara T. Sonic Hedgehog signaling regulates vascular differentiation and function in human CD34 positive cells: vasculogenic CD34(+) cells with Sonic Hedgehog. Stem Cell Res. 2015 Mar;14(2):165-76. doi: 10.1016/j.scr.2015.01.003
  17. Eichmann A, Simons M. VEGF signaling inside vascular endothelial cells and beyond. Curr Opin Cell Biol. 2012 Apr;24(2):188-93. doi: 10.1016/j.ceb.2012.02.002
  18. Simons M, Gordon E, Claesson-Welsh L. Mechanisms and regulation of endothelial VEGF receptor signalling. Nat Rev Mol Cell Biol. 2016;17(10):611-25. doi: 10.1038/nrm.2016.87
  19. Yang C, Guo Y, Jadlowiec CC, Li X, Lv W, Model LS, Collins MJ, Kondo Y, Muto A, Shu C, Dardik A. Vascular endothelial growth factor-A Inhibits Ephb4 and stimulates delta-like ligand 4 expression in adult endothelial cells. J Surg Res. 2013 Jul;183(1):478-86. doi: 10.1016/j.jss.2013.01.009
  20. Benedito R, Hellström M. Notch as a hub for signaling in angiogenesis. Exp Cell Res. 2013 May 15;319(9):1281-88. doi: 10.1016/j.yexcr.2013.01.010
  21. Kondo Y, Muto A, Kudo FA, Model L, Eghbalieh S, Chowdhary P, Dardik A. Age-related Notch-4 quiescence is associated with altered wall remodeling during vein graft adaptation. J Surg Res. 2011 Nov;171(1):e149-60. doi: 10.1016/j.jss.2011.06.036
  22. You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature. 2005;435(7038):98-104. doi: 10.1038/nature03511
  23. Qin J, Tsai SY, Tsai MJ. The critical roles of COUP-TFII in tumor progression and metastasis. Cell Biosci. 2014;4(1):58. doi: 10.1186/2045-3701-4-58
  24. Salvucci O, Tosato G. Essential roles of EphB receptors and EphrinB ligands in endothelial cell function and angiogenesis. Adv Cancer Res. 2012;114:21-57. doi: 10.1016/B978-0-12-386503-8.00002-8
  25. Park I, Lee HS. EphB/ephrinB signaling in cell adhesion and migration. Mol Cells. 2015 Jan 31;38(1):14-19. doi: 10.14348/molcells.2015.2116
  26. Klein R. Eph/ephrin signalling during development. Development. 2012 Nov;139(22):4105-9. doi: 10.1242/dev.074997
  27. Yamanashi Y, Tezuka T, Yokoyama K. Activation of receptor protein-tyrosine kinases from the cytoplasmic compartment. J Biochem. 2012 Apr;151(4):353-9. doi: 10.1093/jb/mvs013
  28. Pitulescu ME, Adams RH. Regulation of signaling interactions and receptor endocytosis in growing blood vessels. Cell Adh Migr. 2014;8(4):366-77. doi: 10.4161/19336918.2014.970010
  29. Xiao Z, Carrasco R, Kinneer K, Sabol D, Jallal B, Coats S, Tice DA. EphB4 promotes or suppresses Ras/MEK/ERK pathway in a context-dependent manner: implications for EphB4 as a cancer target. Cancer Biol Ther. 2012 Jun;13(8):630-37. doi: 10.4161/cbt.20080
  30. Salgia R, Kulkarni P, Gill PS. EphB4: A promising target for upper aerodigestive malignancies. Biochim Biophys Acta. 2018 Apr;1869(2):128-37. doi: 10.1016/j.bbcan.2018.01.003
  31. Hashimoto T, Tsuneki M, Foster TR, Santana JM, Bai H, Wang M, Hu H, Hanisch JJ, Dardik A, Membrane-mediated regulation of vascular identity. Birth Defects Res C Embryo Today. 2016 Mar;108(1):65-84. doi: 10.1002/bdrc.21123
  32. Kudo FA, Muto A, Maloney SP, Pimiento JM, Bergaya S, Fitzgerald TN, Westvik TS, Frattini JC, Breuer CK, Cha CH, Nishibe T, Tellides G, Sessa WC, Dardik A. Venous identity is lost but arterial identity is not gained during vein graft adaptation. Arterioscler Thromb Vasc Biol. 2007;27(7):1562-71. doi: 10.1161/ATVBAHA.107.143032
  33. Muto A, Yi T, Harrison KD, Dávalos A, Fancher TT, Ziegler KR, Feigel A, Kondo Y, Nishibe T, Sessa WC, Dardik A. Eph-B4 prevents venous adaptive remodeling in the adult arterial environment. J Exp Med. 2011 Mar 14;208(3):561-75. doi: 10.1084/jem.20101854
  34. Model LS, Hall MR, Wong DJ, Muto A, Kondo Y, Ziegler KR, Feigel A, Quint C, Niklason L, Dardik A. Arterial shear stress reduces eph-b4 expression in adult human veins. Yale J Biol Med. 2014 Sep;87(3):359-71. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4144290
  35. Berard X, Déglise S, Alonso F, Saucy F, Meda P, Bordenave L, Corpataux JM, Haefliger JA. Role of hemodynamic forces in the ex vivo arterialization of human saphenous veins. J Vasc Surg. 2013 May;57(5):1371-82. doi: 10.1016/j.jvs.2012.09.041
  36. Wong DJ, Lu DY, Protack CD, Kuwahara G, Bai H, Sadaghianloo N, Tellides G, Dardik A. Ephrin type-B receptor 4 activation reduces neointimal hyperplasia in human saphenous vein in vitro. J Vasc Surg. 2016 Mar;63(3):795-804. doi: 10.1016/j.jvs.2014.09.036
  37. Ivanov AN, Bugaeva IO, Kurtukova MO. Structural characteristics of human and other mammalian endothelial cells. Tsitologiia. 2016;58(9):657-65. http://www.tsitologiya.cytspb.rssi.ru/58_9/ivanov1.pdf (in Russ.)
  38. Rivera M, Muto A, Feigel A, Kondo Y, Dardik A. Venous and arterial identity: a role for caveolae? Vascular. 2009 Jun;17(1):S10-14. doi: 10.2310/6670.2008.00088
  39. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest. 2006 May 1;116(5):1284-91. doi: 10.1172/jci27100
  40. Jadlowiec CC, Feigel A, Yang C, Feinstein AJ, Kim ST, Collins MJ, Kondo Y, Muto A, Dardik A. Reduced adult endothelial cell EphB4 function promotes venous remodeling. Am J Physiol Cell Physiol. 2013 Apr 1;304(7):C627-35. doi: 10.1152/ajpcell.00333.2012
  41. Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J. 2012 Apr;33(7):829-37, 837a-837d. doi: 10.1093/eurheartj/ehr304
  42. Onan B, Erkanli K, Onan IS, Ersoy B, Canillioglu YE, Senturk GE, Hurdag C, Yeniterzi M. The impact of vessel clamps on endothelial integrity and function of saphenous vein grafts. Ann Vasc Surg. 2014 Jul;28(5):1113-22. doi: 10.1016/j.avsg.2014.01.020
  43. Kalinin RE, Suchkov IA, Pshennikov AS. Correction of endothelial dysfunction as a component in treatment for atherosclerosis obliterans of lower-limb arteries. Angiologiia i Sosud Khirurgiia. 2014;20(3):17-22. http://www.angiolsurgery.org/magazine/2014/3/2.htm (in Russ.)
  44. Sugimoto M, Yamanouchi D, Komori K. Therapeutic approach against intimal hyperplasia of vein grafts through endothelial nitric oxide synthase/nitric oxide (eNOS/NO) and the Rho/Rho-kinase pathway. Surg Today. 2009;39(6):459-65. doi: 10.1007/s00595-008-3912-6
  45. Chen Z, Bakhshi FR, Shajahan AN, Sharma T, Mao M, Trane A, Bernatchez P, van Nieuw Amerongen GP, Bonini MG, Skidgel RA, Malik AB, Minshall RD. Nitric oxide-dependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/caveolin-1 binding and eNOS inhibition. Mol Biol Cell. 2012 Apr;23(7):1388-98. doi: 10.1091/mbc.E11-09-0811
    46 Bernatchez P, Sharma A, Bauer PM, Marin E, Sessa WC. A noninhibitory mutant of the caveolin-1 scaffolding domain enhances eNOS-derived NO synthesis and vasodilation in mice. J Clin Invest. 2011 Sep;121(9):3747-55. doi: 10.1172/JCI44778
  46. Wang M, Collins MJ, Foster TR, Bai H, Hashimoto T, Santana JM, Shu C, Dardik A. Eph-B4 mediates vein graft adaptation by regulation of endothelial nitric oxide synthase. J Vasc Surg. 2017 Jan;65(1):179-89. doi: 10.1016/j.jvs.2015.11.041
  47. Kalinin RE, Pshennikov AS, Suchkov IA. Reperfusion injury of tissues in lower limb arterial reconstructive surgery. Novosti Khirurgiia. 2015;23(3):348-52. doi: 10.18484/2305-0047.2015.3.348 (in Russ.)
Address for correspondence:
390026, The Russian Federation,
Ryazan, Vysokovoltnaya Str.,9,
Ryazan State Medical University,
Department of Cardiovascular, Endovascular,
Operative Surgery and Topographic Anatomy.
Tel. +7 910 900-95-23,
e-mail: pshennikov1610@rambler.ru,
Alexander S. Pshennikov
Information about the authors:
Kalinin Roman E., MD, Professor, Rector, Head of the Department of Cardiovascular, Endovascular, Operative Surgery and Topographic Anatomy, Ryazan State Medical University, Ryazan, Russian Federation.
http://orcid.org/0000-0002-0817-9573
Suchkov Igor A., MD, Associate Professor, Vice-Rector for Research and Innovative Development, Professor of the Department of Cardiovascular, Endovascular, Operative Surgery and Topographic Anatomy, Ryazan State Medical University, Ryazan, Russian Federation.
http://orcid.org/0000-0002-1292-5452
Pshennikov Alexander S., PhD, Associate Professor, Dean of the Medical Faculty, Associate Professor of the Department of Cardiovascular, Endovascular, Operative Surgery and Topographic Anatomy, Ryazan State Medical University, Ryazan, Russian Federation. http://orcid.org/0000-0002-1687-332X
Vinogradov Sergey A., Clinical Intern of the Department of Cardiovascular, Endovascular, Operative Surgery and Topographic Anatomy, Ryazan State Medical University, Ryazan, Russian Federation.
http://orcid.org/0000-0001-8547-4798
Contacts | ©Vitebsk State Medical University, 2007-2023