Inflammatory monocyte response due to altered wall shear stress in an isolated femoral artery model
Main Article Content
Keywords
arteriogenesis, femoral artery, inflammation, monocyte, wall shear stress
Abstract
Arteriogenesis (collateral formation) is accompanied by a pro-inflammatory state that may be related to the wall shear stress (WSS) within the neo-collateral vessels. Examining the pro-inflammatory component in situ or in vivo is complex. In an ex vivo mouse femoral artery perfusion model, we examined the effect of wall shear stress on pro-arteriogenic inflammatory markers and monocyte adhesion. In a femoral artery model with defined pulsatile flow, WSS was controlled (at physiological stress, 1.4×, and 2× physiological stress) during a 24 h perfusion before gene expression levels and monocyte adhesion were assessed. Significant upregulation of expression was found for the cytokine TNFα, adhesion molecule ICAM-1, growth factor TGFβ, and the transcription factor Egr-1 at varying levels of increased WSS compared to physiological control. Further, trends toward upregulation were found for FGF-2, the cytokine MCP-1 and adhesion molecules VCAM-1 and P-selectin with increased WSS. Finally, monocytes adhesion increased in response to increased WSS. We have developed a murine femoral artery model for studying changes in WSS ex vivo and show that the artery responds by upregulating inflammatory cytokines, adhesion molecules and growth factors consistent with previous in vivo findings.
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References
1. Cross MJ, Claesson-Welsh L (2001) FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends in Pharmacological Sciences 22: 201-207.
2. Liu J, Wang Y, Akamatsu Y, Lee CC, Stetler RA, et al. (2014) Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog Neurobiol 115: 138-156.
3. Buschmann I, Heil M, Jost M, Schaper W (2003) Influence of inflammatory cytokines on arteriogenesis. Microcirculation 10: 371-379.
4. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W (2006) Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 10: 45-55.
5. Grundmann S, Piek JJ, Pasterkamp G, Hoefer IE (2007) Arteriogenesis: basic mechanisms and therapeutic stimulation. European journal of clinical investigation 37: 755-766.
6. Sheikh I, Tchekanov G, Krum D, Hare J, Djelmami-Hani M, et al. (2005) Effect of electrical stimulation on arteriogenesis and angiogenesis after bilateral femoral artery excision in the rabbit hind-limb ischemia model. Vasc Endovascular Surg 39: 257-265.
7. Troidl C, Jung G, Troidl K, Hoffmann J, Mollmann H, et al. (2013) The temporal and spatial distribution of macrophage subpopulations during arteriogenesis. Curr Vasc Pharmacol 11: 5-12.
8. Schaper W (2009) Collateral circulation: past and present. Basic Res Cardiol 104: 5-21.
9. Shireman PK (2007) The chemokine system in arteriogenesis and hind limb ischemia. J Vasc Surg 45 Suppl A: A48-56.
10. Heil M, Schaper W (2004) Influence of Mechanical, Cellular, and Molecular Factors on Collateral Artery Growth (Arteriogenesis). Circulation Research 95: 449-458.
11. Rubenstein D, Dong H, Goldgraben S, El-Gendi H, Gouma P-I, et al. (2007) Bioassay Chamber for Angiogenesis with Perfused Explanted Arteries and Electrospun Scaffolding. Microcirculation: Taylor & Francis Ltd. pp. 723-737.
12. Koller A, Sun D, Kaley G (1993) Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circulation Research 72: 1276-1284.
13. Yamawaki H, Lehoux S, Berk BC (2003) Chronic Physiological Shear Stress Inhibits Tumor Necrosis Factor–Induced Proinflammatory Responses in Rabbit Aorta Perfused Ex Vivo. Circulation 108: 1619-1625.
14. Myers PR, Zhong Q, Jones JJ, Tanner MA, Adams HR, et al. (1995) Release of EDRF and NO in ex vivo perfused aorta: inhibition by in vivo E. coli endotoxemia. American Journal of Physiology - Heart and Circulatory Physiology 268: H955-H961.
15. Dickinson H, Moritz K, Wintour EM, Walker DW, Kett MM (2007) A comparative study of renal function in the desert-adapted spiny mouse and the laboratory-adapted C57BL/6 mouse: response to dietary salt load. American Journal of Physiology - Renal Physiology 293: F1093-F1098.
16. Huo Y, Guo X, Kassab GS (2008) The flow field along the entire length of mouse aorta and primary branches. Annals of Biomedical Engineering 36: 685-699.
17. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25: 402-408.
18. Laurindo F, Pedro M de A, Barbeiro H, Pileggi F, Carvalho M, et al. (1994) Vascular free radical release. Ex vivo and in vivo evidence for a flow- dependent endothelial mechanism. Circulation Research 74: 700-709.
19. Zeerleder S, Mauron T, Lämmle B, Wuillemin WA (2002) Effect of low-molecular weight dextran sulfate on coagulation and platelet function tests. Thrombosis Research 105: 441-446.
20. Hoefer IE, Grundmann S, van Royen N, Voskuil M, Schirmer SH, et al. (2005) Leukocyte subpopulations and arteriogenesis: Specific role of monocytes, lymphocytes and granulocytes. Atherosclerosis 181: 285-293.
21. Rouleau L, Rossi J, Leask R (2010) Concentration and Time Effects of Dextran Exposure on Endothelial Cell Viability, Attachment, and Inflammatory Marker Expression In Vitro. Annals of Biomedical Engineering 38: 1451-1462.
22. Dougherty FC, Donovan FM, Jr., Townsley MI (2003) Harmonic analysis of perfusion pumps. J Biomech Eng 125: 814-822.
23. Schaper W, Ito WD (1996) Molecular Mechanisms of Coronary Collateral Vessel Growth. Circ Res 79: 911-919.
24. Pagel JI, Ziegelhoeffer T, Heil M, Fischer S, Fernandez B, et al. (2012) Role of early growth response 1 in arteriogenesis: impact on vascular cell proliferation and leukocyte recruitment in vivo. Thromb Haemost 107: 562-574.
25. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
26. Sarateanu CS, Retuerto MA, Beckmann JT, McGregor L, Carbray J, et al. (2006) An Egr-1 master switch for arteriogenesis: Studies in Egr-1 homozygous negative and wild-type animals. The Journal of thoracic and cardiovascular surgery 131: 138-145.
27. Alexander GC, Vines JB, Hwang P, Kim T, Kim JA, et al. (2016) Novel Multifunctional Nanomatrix Reduces Inflammation in Dynamic Conditions in Vitro and Dilates Arteries ex Vivo. ACS Appl Mater Interfaces 8: 5178-5187.
2. Liu J, Wang Y, Akamatsu Y, Lee CC, Stetler RA, et al. (2014) Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog Neurobiol 115: 138-156.
3. Buschmann I, Heil M, Jost M, Schaper W (2003) Influence of inflammatory cytokines on arteriogenesis. Microcirculation 10: 371-379.
4. Heil M, Eitenmuller I, Schmitz-Rixen T, Schaper W (2006) Arteriogenesis versus angiogenesis: similarities and differences. J Cell Mol Med 10: 45-55.
5. Grundmann S, Piek JJ, Pasterkamp G, Hoefer IE (2007) Arteriogenesis: basic mechanisms and therapeutic stimulation. European journal of clinical investigation 37: 755-766.
6. Sheikh I, Tchekanov G, Krum D, Hare J, Djelmami-Hani M, et al. (2005) Effect of electrical stimulation on arteriogenesis and angiogenesis after bilateral femoral artery excision in the rabbit hind-limb ischemia model. Vasc Endovascular Surg 39: 257-265.
7. Troidl C, Jung G, Troidl K, Hoffmann J, Mollmann H, et al. (2013) The temporal and spatial distribution of macrophage subpopulations during arteriogenesis. Curr Vasc Pharmacol 11: 5-12.
8. Schaper W (2009) Collateral circulation: past and present. Basic Res Cardiol 104: 5-21.
9. Shireman PK (2007) The chemokine system in arteriogenesis and hind limb ischemia. J Vasc Surg 45 Suppl A: A48-56.
10. Heil M, Schaper W (2004) Influence of Mechanical, Cellular, and Molecular Factors on Collateral Artery Growth (Arteriogenesis). Circulation Research 95: 449-458.
11. Rubenstein D, Dong H, Goldgraben S, El-Gendi H, Gouma P-I, et al. (2007) Bioassay Chamber for Angiogenesis with Perfused Explanted Arteries and Electrospun Scaffolding. Microcirculation: Taylor & Francis Ltd. pp. 723-737.
12. Koller A, Sun D, Kaley G (1993) Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circulation Research 72: 1276-1284.
13. Yamawaki H, Lehoux S, Berk BC (2003) Chronic Physiological Shear Stress Inhibits Tumor Necrosis Factor–Induced Proinflammatory Responses in Rabbit Aorta Perfused Ex Vivo. Circulation 108: 1619-1625.
14. Myers PR, Zhong Q, Jones JJ, Tanner MA, Adams HR, et al. (1995) Release of EDRF and NO in ex vivo perfused aorta: inhibition by in vivo E. coli endotoxemia. American Journal of Physiology - Heart and Circulatory Physiology 268: H955-H961.
15. Dickinson H, Moritz K, Wintour EM, Walker DW, Kett MM (2007) A comparative study of renal function in the desert-adapted spiny mouse and the laboratory-adapted C57BL/6 mouse: response to dietary salt load. American Journal of Physiology - Renal Physiology 293: F1093-F1098.
16. Huo Y, Guo X, Kassab GS (2008) The flow field along the entire length of mouse aorta and primary branches. Annals of Biomedical Engineering 36: 685-699.
17. Livak KJ, Schmittgen TD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25: 402-408.
18. Laurindo F, Pedro M de A, Barbeiro H, Pileggi F, Carvalho M, et al. (1994) Vascular free radical release. Ex vivo and in vivo evidence for a flow- dependent endothelial mechanism. Circulation Research 74: 700-709.
19. Zeerleder S, Mauron T, Lämmle B, Wuillemin WA (2002) Effect of low-molecular weight dextran sulfate on coagulation and platelet function tests. Thrombosis Research 105: 441-446.
20. Hoefer IE, Grundmann S, van Royen N, Voskuil M, Schirmer SH, et al. (2005) Leukocyte subpopulations and arteriogenesis: Specific role of monocytes, lymphocytes and granulocytes. Atherosclerosis 181: 285-293.
21. Rouleau L, Rossi J, Leask R (2010) Concentration and Time Effects of Dextran Exposure on Endothelial Cell Viability, Attachment, and Inflammatory Marker Expression In Vitro. Annals of Biomedical Engineering 38: 1451-1462.
22. Dougherty FC, Donovan FM, Jr., Townsley MI (2003) Harmonic analysis of perfusion pumps. J Biomech Eng 125: 814-822.
23. Schaper W, Ito WD (1996) Molecular Mechanisms of Coronary Collateral Vessel Growth. Circ Res 79: 911-919.
24. Pagel JI, Ziegelhoeffer T, Heil M, Fischer S, Fernandez B, et al. (2012) Role of early growth response 1 in arteriogenesis: impact on vascular cell proliferation and leukocyte recruitment in vivo. Thromb Haemost 107: 562-574.
25. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7: 678-689.
26. Sarateanu CS, Retuerto MA, Beckmann JT, McGregor L, Carbray J, et al. (2006) An Egr-1 master switch for arteriogenesis: Studies in Egr-1 homozygous negative and wild-type animals. The Journal of thoracic and cardiovascular surgery 131: 138-145.
27. Alexander GC, Vines JB, Hwang P, Kim T, Kim JA, et al. (2016) Novel Multifunctional Nanomatrix Reduces Inflammation in Dynamic Conditions in Vitro and Dilates Arteries ex Vivo. ACS Appl Mater Interfaces 8: 5178-5187.
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Published
Feb 20, 2019
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Kadam AA, Gersch RP, Rosengart TK, Frame MD. Inflammatory monocyte response due to altered wall shear stress in an isolated femoral artery model. J Biol Methods [Internet]. 2019 Feb. 20 [cited 2024 Apr. 24];6(1):e109. Available from: https://jbmethods.org/index.php/jbm/article/view/274
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