Functional role and underlying mechanisms of neuropilin-1 in proliferation and migration of rat vascular smooth muscle cells_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LIU Yu , ZHANG Hongwei , YANG Peng , HUANG Yao , LU Chen , ZHANG Yu ,  HU Jia

Department of Cardiovascular Surgery, West China Hospital, Sichuan University, Chengdu, 610041, P.R.China;

Corresponding author：

HU Jia, Email: humanjia@msn.com

Keywords：

Neuropilin-1; coronary artery bypass grafting; vein graft failure; vascular smooth muscle cell

DOI：

10.7507/1007-4848.202005091

Video：

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Objective To investigate the role and potential mechanisms of neuropilin-1 (NRP1) in the pathogenesis of vein graft failure.Methods The rat vascular smooth muscle cells (VSMCs) were transfected with NRP1-shRNA adenovirus and negative control adenovirus respectively. Cell counting kit-8, flow cytometry, Transwell and Western blot were used to investigate the effects of inhibition of NRP1 on VSMCs proliferation viability, apoptosis, migration capacity and its downstream signaling pathway protein expression.Results The proliferation and migration of rat VSMCs could be inhibited after down-regulation of NRP1, and the increase of apoptosis was also observed. Moreover, inhibition of NRP1 significantly reduced Akt and NF-κB phosphorylation in rat VSMCs, but had little effect on activation of ERK1/2.Conclusion NRP1 may promote vein graft hyperplastic remodeling by regulating the proliferation and migration of VSMCs through PI3K/Akt and NF-κB pathways, but further animal study is required.

Citation： LIU Yu, ZHANG Hongwei, YANG Peng, HUANG Yao, LU Chen, ZHANG Yu, HU Jia. Functional role and underlying mechanisms of neuropilin-1 in proliferation and migration of rat vascular smooth muscle cells. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2021, 28(7): 849-857. doi: 10.7507/1007-4848.202005091 Copy

1.	胡盛寿, 高润霖, 刘力生, 等. 《中国心血管病报告2018》概要. 中国循环杂志, 2019, 34(3): 209-220.
2.	Solo K, Lavi S, Kabali C, et al. Antithrombotic treatment after coronary artery bypass graft surgery: Systematic review and network meta-analysis. BMJ, 2019, 367: I5476.
3.	Gaudino M, Antoniades C, Benedetto U, et al. Mechanisms, consequences, and prevention of coronary graft failure. Circulation, 2017, 136(18): 1749-1764.
4.	de Vries MR, Simons KH, Jukema JW, et al. Vein graft failure: From pathophysiology to clinical outcomes. Nat Rev Cardiol, 2016, 13(8): 451-470.
5.	Harskamp RE, Lopes RD, Baisden CE, et al. Saphenous vein graft failure after coronary artery bypass surgery: Pathophysiology, management, and future directions. Ann Surg, 2013, 257(5): 824-833.
6.	Owens CD, Gasper WJ, Rahman AS, et al. Vein graft failure. J Vasc Surg, 2015, 61(1): 203-216.
7.	张洪伟, 肖正华, 张尔永, 等. 血管外支架防治自体静脉桥失效的研究进展. 中华实验外科杂志, 2015, 32(11): 2903-2905.
8.	McKavanagh P, Yanagawa B, Zawadowski G, et al. Management and prevention of saphenous vein graft failure: A review. Cardiol Ther, 2017, 6(2): 203-223.
9.	Wang D, Uhrin P, Mocan A, et al. Vascular smooth muscle cell proliferation as a therapeutic target. Part 1: molecular targets and pathways. Biotechnol Adv, 2018, 36(6): 1586-1607.
10.	Uhrin P, Wang D, Mocan A, et al. Vascular smooth muscle cell proliferation as a therapeutic target. Part 2: Natural products inhibiting proliferation. Biotechnol Adv, 2018, 36(6): 1608-1621.
11.	Frismantiene A, Philippova M, Erne P, et al. Smooth muscle cell-driven vascular diseases and molecular mechanisms of VSMC plasticity. Cell Signal, 2018, 52: 48-64.
12.	Pellet-Many C, Frankel P, Evans IM, et al. Neuropilin-1 mediates PDGF stimulation of vascular smooth muscle cell migration and signalling via p130Cas. Biochem J, 2011, 435(3): 609-618.
13.	Pellet-Many C, Mehta V, Fields L, et al. Neuropilins 1 and 2 mediate neointimal hyperplasia and re-endothelialization following arterial injury. Cardiovasc Res, 2015, 108(2): 288-298.
14.	Kofler N, Simons M. The expanding role of neuropilin: Regulation of transforming growth factor-β and platelet-derived growth factor signaling in the vasculature. Curr Opin Hematol, 2016, 23(3): 260-267.
15.	张洪伟, 古君, 张尔永, 等. BMP4在合并糖尿病的冠状动脉旁路移植术患者原位静脉桥病变中的作用. 四川大学学报(医学版), 2016, 47(5): 738-742.
16.	方登峰, 张洪伟, 古君, 等. 骨形态发生蛋白-4在高糖环境下静脉桥增殖重构进程中的作用研究. 四川大学学报(医学版), 2017, 48(5): 710-715.
17.	Raines EW. PDGF and cardiovascular disease. Cytokine Growth Factor Rev, 2004, 15(4): 237-254.
18.	Ouyang L, Zhang K, Chen J, et al. Roles of platelet-derived growth factor in vascular calcification. J Cell Physiol, 2018, 233(4): 2804-2814.
19.	Wang C, Liu Y, He D. Diverse effects of platelet-derived growth factor-BB on cell signaling pathways. Cytokine, 2019, 113: 13-20.
20.	Huang B, Dreyer T, Heidt M, et al. Insulin and local growth factor PDGF induce intimal hyperplasia in bypass graft culture models of saphenous vein and internal mammary artery. Eur J Cardiothorac Surg, 2002, 21(6): 1002-1008.
21.	Lu QB, Wan MY, Wang PY, et al. Chicoric acid prevents PDGF-BB-induced VSMC dedifferentiation, proliferation and migration by suppressing ROS/NFκB/mTOR/P70S6K signaling cascade. Redox Biol, 2018, 14: 656-668.
22.	Dong X, Hu H, Fang Z, et al. CTRP6 inhibits PDGF-BB-induced vascular smooth muscle cell proliferation and migration. Biomed Pharmacother, 2018, 103: 844-850.
23.	Yang J, Zeng P, Yang J, et al. MicroRNA-24 regulates vascular remodeling via inhibiting PDGF-BB pathway in diabetic rat model. Gene, 2018, 659: 67-76.
24.	Ma X, Jiang C, Li Y, et al. Inhibition effect of tacrolimus and platelet-derived growth factor-BB on restenosis after vascular intimal injury. Biomed Pharmacother, 2017, 93: 180-189.
25.	Yelland T, Djordjevic S. Crystal structure of the neuropilin-1 MAM domain: Completing the neuropilin-1 ectodomain picture. Structure, 2016, 24(11): 2008-2015.
26.	Banerjee S, Sengupta K, Dhar K, et al. Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol Carcinog, 2006, 45(11): 871-880.
27.	Li H, Zhao J, Liu B, et al. MicroRNA-320 targeting neuropilin 1 inhibits proliferation and migration of vascular smooth muscle cells and neointimal formation. Int J Med Sci, 2019, 16(1): 106-114.
28.	Banerjee S, Mehta S, Haque I, et al. VEGF-A165 induces human aortic smooth muscle cell migration by activating neuropilin-1-VEGFR1-PI3K axis. Biochemistry, 2008, 47(11): 3345-3351.
29.	Liu W, Parikh AA, Stoeltzing O, et al. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine, 2005, 32(5): 206-212.
30.	Chai S, Yu Y, Li H, et al. Application of medical adhesive inhibits intimal hyperplasia involving the downregulation of ERK1/2 and eNOS levels. Mol Med Rep, 2018, 18(5): 4643-4649.
31.	Li Y, Liu S, Zhang Z, et al. RAGE mediates accelerated diabetic vein graft atherosclerosis induced by combined mechanical stress and AGEs via synergistic ERK activation. PLoS One, 2012, 7(4): e35016.
32.	Bai X, Xi J, Bi Y, et al. TNF-α promotes survival and migration of MSCs under oxidative stress via NF-κB pathway to attenuate intimal hyperplasia in vein grafts. J Cell Mol Med, 2017, 21(9): 2077-2091.
33.	Jia G, Mitra AK, Gangahar DM, et al. Insulin-like growth factor-1 induces phosphorylation of PI3K-Akt/PKB to potentiate proliferation of smooth muscle cells in human saphenous vein. Exp Mol Pathol, 2010, 89(1): 20-26.
34.	Peng CY, Pan SL, Huang YW, et al. Baicalein attenuates intimal hyperplasia after rat carotid balloon injury through arresting cell-cycle progression and inhibiting ERK, Akt, and NF-kappaB activity in vascular smooth-muscle cells. Naunyn Schmiedebergs Arch Pharmacol, 2008, 378(6): 579-588.

1. 胡盛寿, 高润霖, 刘力生, 等. 《中国心血管病报告2018》概要. 中国循环杂志, 2019, 34(3): 209-220.
2. Solo K, Lavi S, Kabali C, et al. Antithrombotic treatment after coronary artery bypass graft surgery: Systematic review and network meta-analysis. BMJ, 2019, 367: I5476.
3. Gaudino M, Antoniades C, Benedetto U, et al. Mechanisms, consequences, and prevention of coronary graft failure. Circulation, 2017, 136(18): 1749-1764.
4. de Vries MR, Simons KH, Jukema JW, et al. Vein graft failure: From pathophysiology to clinical outcomes. Nat Rev Cardiol, 2016, 13(8): 451-470.
5. Harskamp RE, Lopes RD, Baisden CE, et al. Saphenous vein graft failure after coronary artery bypass surgery: Pathophysiology, management, and future directions. Ann Surg, 2013, 257(5): 824-833.
6. Owens CD, Gasper WJ, Rahman AS, et al. Vein graft failure. J Vasc Surg, 2015, 61(1): 203-216.
7. 张洪伟, 肖正华, 张尔永, 等. 血管外支架防治自体静脉桥失效的研究进展. 中华实验外科杂志, 2015, 32(11): 2903-2905.
8. McKavanagh P, Yanagawa B, Zawadowski G, et al. Management and prevention of saphenous vein graft failure: A review. Cardiol Ther, 2017, 6(2): 203-223.
9. Wang D, Uhrin P, Mocan A, et al. Vascular smooth muscle cell proliferation as a therapeutic target. Part 1: molecular targets and pathways. Biotechnol Adv, 2018, 36(6): 1586-1607.
10. Uhrin P, Wang D, Mocan A, et al. Vascular smooth muscle cell proliferation as a therapeutic target. Part 2: Natural products inhibiting proliferation. Biotechnol Adv, 2018, 36(6): 1608-1621.
11. Frismantiene A, Philippova M, Erne P, et al. Smooth muscle cell-driven vascular diseases and molecular mechanisms of VSMC plasticity. Cell Signal, 2018, 52: 48-64.
12. Pellet-Many C, Frankel P, Evans IM, et al. Neuropilin-1 mediates PDGF stimulation of vascular smooth muscle cell migration and signalling via p130Cas. Biochem J, 2011, 435(3): 609-618.
13. Pellet-Many C, Mehta V, Fields L, et al. Neuropilins 1 and 2 mediate neointimal hyperplasia and re-endothelialization following arterial injury. Cardiovasc Res, 2015, 108(2): 288-298.
14. Kofler N, Simons M. The expanding role of neuropilin: Regulation of transforming growth factor-β and platelet-derived growth factor signaling in the vasculature. Curr Opin Hematol, 2016, 23(3): 260-267.
15. 张洪伟, 古君, 张尔永, 等. BMP4在合并糖尿病的冠状动脉旁路移植术患者原位静脉桥病变中的作用. 四川大学学报(医学版), 2016, 47(5): 738-742.
16. 方登峰, 张洪伟, 古君, 等. 骨形态发生蛋白-4在高糖环境下静脉桥增殖重构进程中的作用研究. 四川大学学报(医学版), 2017, 48(5): 710-715.
17. Raines EW. PDGF and cardiovascular disease. Cytokine Growth Factor Rev, 2004, 15(4): 237-254.
18. Ouyang L, Zhang K, Chen J, et al. Roles of platelet-derived growth factor in vascular calcification. J Cell Physiol, 2018, 233(4): 2804-2814.
19. Wang C, Liu Y, He D. Diverse effects of platelet-derived growth factor-BB on cell signaling pathways. Cytokine, 2019, 113: 13-20.
20. Huang B, Dreyer T, Heidt M, et al. Insulin and local growth factor PDGF induce intimal hyperplasia in bypass graft culture models of saphenous vein and internal mammary artery. Eur J Cardiothorac Surg, 2002, 21(6): 1002-1008.
21. Lu QB, Wan MY, Wang PY, et al. Chicoric acid prevents PDGF-BB-induced VSMC dedifferentiation, proliferation and migration by suppressing ROS/NFκB/mTOR/P70S6K signaling cascade. Redox Biol, 2018, 14: 656-668.
22. Dong X, Hu H, Fang Z, et al. CTRP6 inhibits PDGF-BB-induced vascular smooth muscle cell proliferation and migration. Biomed Pharmacother, 2018, 103: 844-850.
23. Yang J, Zeng P, Yang J, et al. MicroRNA-24 regulates vascular remodeling via inhibiting PDGF-BB pathway in diabetic rat model. Gene, 2018, 659: 67-76.
24. Ma X, Jiang C, Li Y, et al. Inhibition effect of tacrolimus and platelet-derived growth factor-BB on restenosis after vascular intimal injury. Biomed Pharmacother, 2017, 93: 180-189.
25. Yelland T, Djordjevic S. Crystal structure of the neuropilin-1 MAM domain: Completing the neuropilin-1 ectodomain picture. Structure, 2016, 24(11): 2008-2015.
26. Banerjee S, Sengupta K, Dhar K, et al. Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol Carcinog, 2006, 45(11): 871-880.
27. Li H, Zhao J, Liu B, et al. MicroRNA-320 targeting neuropilin 1 inhibits proliferation and migration of vascular smooth muscle cells and neointimal formation. Int J Med Sci, 2019, 16(1): 106-114.
28. Banerjee S, Mehta S, Haque I, et al. VEGF-A165 induces human aortic smooth muscle cell migration by activating neuropilin-1-VEGFR1-PI3K axis. Biochemistry, 2008, 47(11): 3345-3351.
29. Liu W, Parikh AA, Stoeltzing O, et al. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine, 2005, 32(5): 206-212.
30. Chai S, Yu Y, Li H, et al. Application of medical adhesive inhibits intimal hyperplasia involving the downregulation of ERK1/2 and eNOS levels. Mol Med Rep, 2018, 18(5): 4643-4649.
31. Li Y, Liu S, Zhang Z, et al. RAGE mediates accelerated diabetic vein graft atherosclerosis induced by combined mechanical stress and AGEs via synergistic ERK activation. PLoS One, 2012, 7(4): e35016.
32. Bai X, Xi J, Bi Y, et al. TNF-α promotes survival and migration of MSCs under oxidative stress via NF-κB pathway to attenuate intimal hyperplasia in vein grafts. J Cell Mol Med, 2017, 21(9): 2077-2091.
33. Jia G, Mitra AK, Gangahar DM, et al. Insulin-like growth factor-1 induces phosphorylation of PI3K-Akt/PKB to potentiate proliferation of smooth muscle cells in human saphenous vein. Exp Mol Pathol, 2010, 89(1): 20-26.
34. Peng CY, Pan SL, Huang YW, et al. Baicalein attenuates intimal hyperplasia after rat carotid balloon injury through arresting cell-cycle progression and inhibiting ERK, Akt, and NF-kappaB activity in vascular smooth-muscle cells. Naunyn Schmiedebergs Arch Pharmacol, 2008, 378(6): 579-588.

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Functional role and underlying mechanisms of neuropilin-1 in proliferation and migration of rat vascular smooth muscle cells

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