Shear Stress Induces a Time-Dependent Inflammatory Response in Human Monocyte-Derived Macrophages.
Inflammation
Macrophage
Mechanoregulation
Polarization
Shear stress
Journal
Annals of biomedical engineering
ISSN: 1573-9686
Titre abrégé: Ann Biomed Eng
Pays: United States
ID NLM: 0361512
Informations de publication
Date de publication:
17 Sep 2024
17 Sep 2024
Historique:
received:
24
10
2023
accepted:
10
05
2024
medline:
18
9
2024
pubmed:
18
9
2024
entrez:
17
9
2024
Statut:
aheadofprint
Résumé
Macrophages are innate immune cells that are known for their extreme plasticity, enabling diverse phenotypes that lie on a continuum. In a simplified model, they switch between pro-inflammatory (M1) and anti-inflammatory (M2) phenotypes depending on surrounding microenvironmental cues, which have been implicated in disease outcomes. Although considerable research has been focused on macrophage response to biochemical cues and mechanical signals, there is a scarcity of knowledge surrounding their behavior in response to shear stress. In this study, we applied varying magnitudes of shear stress on human monocyte-derived macrophages (MDMs) using a cone-and-plate viscometer and evaluated changes in morphology, gene expression, protein expression, and cytokine secretion over time. MDMs exposed to shear stress exhibited a rounder morphology compared to statically-cultured controls. RT-qPCR results showed significant upregulation of TNF-α, and analysis of cytokine release revealed increased secretion of IL-8, IL-18, fractalkine, and other chemokines. The upregulation of pro-inflammatory factors was evident with both increasing magnitudes of shear and time. Taken together, these results indicate that prolonged shear exposure induced a pro-inflammatory phenotype in human MDMs. These findings have implications for medical technology development, such as in situ vascular graft design wherein macrophages are exposed to shear and have been shown to affect graft resorption, and in delineating disease pathophysiology, for example to further illuminate the role of macrophages in atherosclerosis where shear is directly related to disease outcome.
Identifiants
pubmed: 39289258
doi: 10.1007/s10439-024-03546-5
pii: 10.1007/s10439-024-03546-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Foundation for the National Institutes of Health
ID : RO1 HL140305
Organisme : Foundation for the National Institutes of Health
ID : RO1 HL140305
Organisme : National Science Foundation
ID : Graduate Research Fellowship Program
Organisme : American Heart Association
ID : 20UFEL35260054
Informations de copyright
© 2024. The Author(s) under exclusive licence to Biomedical Engineering Society.
Références
Xue, J., S. V. Schmidt, J. Sander, A. Draffehn, W. Krebs, I. Quester, D. De Nardo, T. D. Gohel, M. Emde, L. Schmidleithner, H. Ganesan, A. Nino-Castro, M. R. Mallmann, L. Labzin, H. Theis, M. Kraut, M. Beyer, E. Latz, T. C. Freeman, T. Ulas, and J. L. Schultze. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity. 40(2):274–288, 2014.
pubmed: 24530056
pmcid: 3991396
doi: 10.1016/j.immuni.2014.01.006
Chavez-Galan, L., M. L. Olleros, D. Vesin, and I. Garcia. Much more than M1 and M2 macrophages, there are also CD169(+) and TCR(+) macrophages. Front. Immunol. 6:263, 2015.
pubmed: 26074923
pmcid: 4443739
Orecchioni, M., Y. Ghosheh, A. B. Pramod, and K. Ley. Macrophage polarization: different gene signatures in M1(LPS+) vs. classically and M2(LPS-) vs. alternatively activated macrophages. Front. Immunol. 10:1084, 2019.
pubmed: 31178859
pmcid: 6543837
doi: 10.3389/fimmu.2019.01084
Smith, T. D., M. J. Tse, E. L. Read, and W. F. Liu. Regulation of macrophage polarization and plasticity by complex activation signals. Integr. Biol. (Camb.). 8(9):946–955, 2016.
pubmed: 27492191
doi: 10.1039/c6ib00105j
Spiller, K. L., R. R. Anfang, K. J. Spiller, J. Ng, K. R. Nakazawa, J. W. Daulton, and G. Vunjak-Novakovic. The role of macrophage phenotype in vascularization of tissue engineering scaffolds. Biomaterials. 35(15):4477–4488, 2014.
pubmed: 24589361
pmcid: 4000280
doi: 10.1016/j.biomaterials.2014.02.012
Lin, P., H. H. Ji, Y. J. Li, and S. D. Guo. Macrophage plasticity and atherosclerosis therapy. Front. Mol. Biosci. 8:679797, 2021.
pubmed: 34026849
pmcid: 8138136
doi: 10.3389/fmolb.2021.679797
Lutgens, E., M. Gijbels, M. Smook, P. Heeringa, P. Gotwals, V. E. Koteliansky, and M. J. Daemen. Transforming growth factor-beta mediates balance between inflammation and fibrosis during plaque progression. Arterioscler. Thromb. Vasc. Biol. 22(6):975–982, 2002.
pubmed: 12067907
doi: 10.1161/01.ATV.0000019729.39500.2F
McWhorter, F. Y., T. Wang, P. Nguyen, T. Chung, and W. F. Liu. Modulation of macrophage phenotype by cell shape. Proc. Natl. Acad. Sci. USA. 110(43):17253–17258, 2013.
pubmed: 24101477
pmcid: 3808615
doi: 10.1073/pnas.1308887110
Heinrich, F., A. Lehmbecker, B. B. Raddatz, K. Kegler, A. Tipold, V. M. Stein, A. Kalkuhl, U. Deschl, W. Baumgartner, R. Ulrich, and I. Spitzbarth. Morphologic, phenotypic, and transcriptomic characterization of classically and alternatively activated canine blood-derived macrophages in vitro. PLoS One.12(8):e0183572, 2017.
pubmed: 28817687
pmcid: 5560737
doi: 10.1371/journal.pone.0183572
Gruber, E. J., and C. A. Leifer. Molecular regulation of TLR signaling in health and disease: mechano-regulation of macrophages and TLR signaling. Innate Immun. 26(1):15–25, 2020.
pubmed: 31955624
pmcid: 6974875
doi: 10.1177/1753425919838322
Gruber, E., C. Heyward, J. Cameron, and C. Leifer. Toll-like receptor signaling in macrophages is regulated by extracellular substrate stiffness and Rho-associated coiled-coil kinase (ROCK1/2). Int. Immunol. 30(6):267–278, 2018.
pubmed: 29800294
pmcid: 5967458
doi: 10.1093/intimm/dxy027
Friedemann, M., L. Kalbitzer, S. Franz, S. Moeller, M. Schnabelrauch, J. C. Simon, T. Pompe, and K. Franke. Instructing human macrophage polarization by stiffness and glycosaminoglycan functionalization in 3D collagen networks. Adv. Healthc. Mater. 6(7):1600967, 2017.
doi: 10.1002/adhm.201600967
Evers, T. M. J., V. Sheikhhassani, H. Tang, M. C. Haks, T. H. M. Ottenhoff, and A. Mashaghi. Single-cell mechanical characterization of human macrophages. Adv. NanoBiomed. Res. 2(7):2100133, 2022.
doi: 10.1002/anbr.202100133
Jain, N., and V. Vogel. Spatial confinement downsizes the inflammatory response of macrophages. Nat. Mater. 17(12):1134–1144, 2018.
pubmed: 30349032
pmcid: 6615903
doi: 10.1038/s41563-018-0190-6
Yang, J. H., H. Sakamoto, E. C. Xu, and R. T. Lee. Biomechanical regulation of human monocyte/macrophage molecular function. Am. J. Pathol. 156(5):1797–1804, 2000.
pubmed: 10793091
pmcid: 1876939
doi: 10.1016/S0002-9440(10)65051-1
Maruyama, K., E. Nemoto, and S. Yamada. Mechanical regulation of macrophage function - cyclic tensile force inhibits NLRP3 inflammasome-dependent IL-1beta secretion in murine macrophages. Inflamm. Regen. 39:3, 2019.
pubmed: 30774738
pmcid: 6367847
doi: 10.1186/s41232-019-0092-2
Seneviratne, A. N., J. E. Cole, M. E. Goddard, I. Park, Z. Mohri, S. Sansom, I. Udalova, R. Krams, and C. Monaco. Low shear stress induces M1 macrophage polarization in murine thin-cap atherosclerotic plaques. J. Mol. Cell. Cardiol. 89(Pt B):168–172, 2015.
pubmed: 26523517
doi: 10.1016/j.yjmcc.2015.10.034
De Wilde, D., B. Trachet, G. R. Y. De Meyer, and P. Segers. Shear stress metrics and their relation to atherosclerosis: an in vivo follow-up study in atherosclerotic mice. Ann. Biomed. Eng. 44(8):2327–2338, 2016.
pubmed: 26695938
doi: 10.1007/s10439-015-1540-z
Seneviratne, A., M. Hulsmans, P. Holvoet, and C. Monaco. Biomechanical factors and macrophages in plaque stability. Cardiovasc. Res. 99(2):284–293, 2013.
pubmed: 23687352
doi: 10.1093/cvr/cvt097
Heo, K. S., K. Fujiwara, and J. Abe. Shear stress and atherosclerosis. Mol. Cells. 37(6):435–440, 2014.
pubmed: 24781409
pmcid: 4086336
doi: 10.14348/molcells.2014.0078
Masse, D. D., J. A. Shar, K. N. Brown, S. G. Keswani, K. J. Grande-Allen, and P. Sucosky. Discrete subaortic stenosis: perspective roadmap to a complex disease. Front. Cardiovasc. Med. 5:122, 2018.
pubmed: 30320123
pmcid: 6166095
doi: 10.3389/fcvm.2018.00122
Butany, J., P. Vaideeswar, and T. E. David. Discrete subaortic membranes in adults–a clinicopathological analysis. Cardiovasc. Pathol. 18(4):236–242, 2009.
pubmed: 18823798
doi: 10.1016/j.carpath.2008.06.013
Jui, E., K. L. Singampalli, K. Shani, Y. Ning, J. P. Connell, R. K. Birla, P. L. Bollyky, C. A. Caldarone, S. G. Keswani, and K. J. Grande-Allen. The immune and inflammatory basis of acquired pediatric cardiac disease. Front. Cardiovasc. Med.8:701224, 2021.
pubmed: 34386532
pmcid: 8353076
doi: 10.3389/fcvm.2021.701224
Smits, A. I., V. Ballotta, A. Driessen-Mol, C. V. Bouten, and F. P. Baaijens. Shear flow affects selective monocyte recruitment into MCP-1-loaded scaffolds. J. Cell. Mol. Med. 18(11):2176–2188, 2014.
pubmed: 25103256
pmcid: 4224552
doi: 10.1111/jcmm.12330
van Haaften, E. E., T. B. Wissing, N. A. Kurniawan, A. Smits, and C. V. C. Bouten. Human in vitro model mimicking material-driven vascular regeneration reveals how cyclic stretch and shear stress differentially modulate inflammation and matrix deposition. Adv. Biosyst.4(6):e1900249, 2020.
pubmed: 32390338
doi: 10.1002/adbi.201900249
Wissing, T. B., E. E. van Haaften, S. E. Koch, B. D. Ippel, N. A. Kurniawan, C. V. C. Bouten, and A. Smits. Hemodynamic loads distinctively impact the secretory profile of biomaterial-activated macrophages—implications for in situ vascular tissue engineering. Biomater. Sci. 8(1):132–147, 2019.
pubmed: 31709425
doi: 10.1039/C9BM01005J
Barral, M., I. El-Sanharawi, A. Dohan, M. Sebuhyan, A. Guedon, A. Delarue, A. Boutigny, N. Mohamedi, B. Magnan, S. Kemel, C. Ketfi, N. Kubis, A. Bisdorff-Bresson, M. Pocard, and P. Bonnin. Blood flow and shear stress allow monitoring of progression and prognosis of tumor diseases. Front Physiol.12:693052, 2021.
pubmed: 34413786
pmcid: 8369886
doi: 10.3389/fphys.2021.693052
Samady, H., P. Eshtehardi, M. C. McDaniel, J. Suo, S. S. Dhawan, C. Maynard, L. H. Timmins, A. A. Quyyumi, and D. P. Giddens. Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation. 124(7):779–788, 2011.
pubmed: 21788584
doi: 10.1161/CIRCULATIONAHA.111.021824
Heo, K. S., H. Lee, P. Nigro, T. Thomas, N. T. Le, E. Chang, C. McClain, C. A. Reinhart-King, M. R. King, B. C. Berk, K. Fujiwara, C. H. Woo, and J. Abe. PKCzeta mediates disturbed flow-induced endothelial apoptosis via p53 SUMOylation. J. Cell. Biol. 193(5):867–884, 2011.
pubmed: 21624955
pmcid: 3105539
doi: 10.1083/jcb.201010051
Reinhart-King, C. A., K. Fujiwara, and B. C. Berk. Physiologic stress-mediated signaling in the endothelium. Methods Enzymol. 443:25–44, 2008.
pubmed: 18772009
doi: 10.1016/S0076-6879(08)02002-8
Jo, H., H. Song, and A. Mowbray. Role of NADPH oxidases in disturbed flow- and BMP4- induced inflammation and atherosclerosis. Antioxid. Redox Signal. 8(9–10):1609–1619, 2006.
pubmed: 16987015
doi: 10.1089/ars.2006.8.1609
Zhang, C., M. Yang, and A. C. Ericsson. Function of macrophages in disease: current understanding on molecular mechanisms. Front. Immunol.12:620510, 2021.
pubmed: 33763066
pmcid: 7982479
doi: 10.3389/fimmu.2021.620510
Ardura, J. A., G. Rackov, E. Izquierdo, V. Alonso, A. R. Gortazar, and M. M. Escribese. Targeting macrophages: friends or foes in disease? Front. Pharmacol. 10:1255, 2019.
pubmed: 31708781
pmcid: 6819424
doi: 10.3389/fphar.2019.01255
Singampalli, K. L., E. Jui, K. Shani, Y. Ning, J. P. Connell, R. K. Birla, P. L. Bollyky, C. A. Caldarone, S. G. Keswani, and K. J. Grande-Allen. Congenital heart disease: an immunological perspective. Front. Cardiovasc. Med.8:701375, 2021.
pubmed: 34434978
pmcid: 8380780
doi: 10.3389/fcvm.2021.701375
Tomlinson, G. S., H. Booth, S. J. Petit, E. Potton, G. J. Towers, R. F. Miller, B. M. Chain, and M. Noursadeghi. Adherent human alveolar macrophages exhibit a transient pro-inflammatory profile that confounds responses to innate immune stimulation. PLoS One.7(6):e40348, 2012.
pubmed: 22768282
pmcid: 3386998
doi: 10.1371/journal.pone.0040348
Chamberlain, L. M., D. Holt-Casper, M. Gonzalez-Juarrero, and D. W. Grainger. Extended culture of macrophages from different sources and maturation results in a common M2 phenotype. J. Biomed. Mater. Res. A. 103(9):2864–2874, 2015.
pubmed: 25684281
pmcid: 4520783
doi: 10.1002/jbm.a.35415
Tokunaga, R., W. Zhang, M. Naseem, A. Puccini, M. D. Berger, S. Soni, M. McSkane, H. Baba, and H. J. Lenz. CXCL9, CXCL10, CXCL11/CXCR3 axis for immune activation—a target for novel cancer therapy. Cancer Treat. Rev. 63:40–47, 2018.
pubmed: 29207310
doi: 10.1016/j.ctrv.2017.11.007
Bickel, M. The role of interleukin-8 in inflammation and mechanisms of regulation. J. Periodontol. 64(5 Suppl):456–460, 1993.
pubmed: 8315568
Szentes, V., M. Gazdag, I. Szokodi, and C. A. Dezsi. The role of CXCR3 and associated chemokines in the development of atherosclerosis and during myocardial infarction. Front. Immunol. 9:1932, 2018.
pubmed: 30210493
pmcid: 6119714
doi: 10.3389/fimmu.2018.01932
Singh, S., D. Anshita, and V. Ravichandiran. MCP-1: function, regulation, and involvement in disease. Int. Immunopharmacol.101(Pt B):107598, 2021.
pubmed: 34233864
pmcid: 8135227
doi: 10.1016/j.intimp.2021.107598
Opdenakker, G., G. Froyen, P. Fiten, P. Proost, and J. Van Damme. Human monocyte chemotactic protein-3 (MCP-3): molecular cloning of the cDNA and comparison with other chemokines. Biochem. Biophys. Res. Commun. 191(2):535–542, 1993.
pubmed: 8461011
doi: 10.1006/bbrc.1993.1251
Mikolajczyk, T. P., R. Nosalski, P. Szczepaniak, K. Budzyn, G. Osmenda, D. Skiba, A. Sagan, J. Wu, A. Vinh, P. J. Marvar, B. Guzik, J. Podolec, G. Drummond, H. E. Lob, D. G. Harrison, and T. J. Guzik. Role of chemokine RANTES in the regulation of perivascular inflammation, T-cell accumulation, and vascular dysfunction in hypertension. FASEB J. 30(5):1987–1999, 2016.
pubmed: 26873938
pmcid: 4836375
doi: 10.1096/fj.201500088R
Mattes, J., and P. S. Foster. Regulation of eosinophil migration and Th2 cell function by IL-5 and eotaxin. Curr. Drug Targets Inflamm. Allergy. 2(2):169–174, 2003.
pubmed: 14561170
doi: 10.2174/1568010033484214
White, G. E., and D. R. Greaves. Fractalkine: a survivor’s guide: chemokines as antiapoptotic mediators. Arterioscler. Thromb. Vasc. Biol. 32(3):589–594, 2012.
pubmed: 22247260
doi: 10.1161/ATVBAHA.111.237412
Sindhu, S., N. Akhter, A. Wilson, R. Thomas, H. Arefanian, A. A. Madhoun, F. Al-Mulla, and R. Ahmad. MIP-1alpha expression induced by co-stimulation of human monocytic cells with palmitate and TNF-alpha involves the TLR4-IRF3 pathway and is amplified by oxidative stress. Cells. 9(8):1799, 2020.
pubmed: 32751118
pmcid: 7465096
doi: 10.3390/cells9081799
Sherry, B., M. Espinoza, K. R. Manogue, and A. Cerami. Induction of the chemokine beta peptides, MIP-1 alpha and MIP-1 beta, by lipopolysaccharide is differentially regulated by immunomodulatory cytokines gamma-IFN, IL-10, IL-4, and TGF-beta. Mol. Med. 4(10):648–657, 1998.
pubmed: 9848081
pmcid: 2230258
doi: 10.1007/BF03401925
Krettek, A., G. Ostergren-Lunden, G. Fager, C. Rosmond, G. Bondjers, and F. Lustig. Expression of PDGF receptors and ligand-induced migration of partially differentiated human monocyte-derived macrophages. Influence of IFN-gamma and TGF-beta. Atherosclerosis. 156(2):267–275, 2001.
pubmed: 11395022
doi: 10.1016/S0021-9150(00)00644-4
Wu, W. K., O. P. Llewellyn, D. O. Bates, L. B. Nicholson, and A. D. Dick. IL-10 regulation of macrophage VEGF production is dependent on macrophage polarisation and hypoxia. Immunobiology. 215(9–10):796–803, 2010.
pubmed: 20692534
doi: 10.1016/j.imbio.2010.05.025
Apostolakis, S., K. Vogiatzi, V. Amanatidou, and D. A. Spandidos. Interleukin 8 and cardiovascular disease. Cardiovasc. Res. 84(3):353–360, 2009.
pubmed: 19617600
doi: 10.1093/cvr/cvp241
Zernecke, A., and C. Weber. Chemokines in the vascular inflammatory response of atherosclerosis. Cardiovasc. Res. 86(2):192–201, 2010.
pubmed: 20007309
doi: 10.1093/cvr/cvp391
Voloshyna, I., M. J. Littlefield, and A. B. Reiss. Atherosclerosis and interferon-gamma: new insights and therapeutic targets. Trends Cardiovasc. Med. 24(1):45–51, 2014.
pubmed: 23916809
doi: 10.1016/j.tcm.2013.06.003
Branen, L., L. Hovgaard, M. Nitulescu, E. Bengtsson, J. Nilsson, and S. Jovinge. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 24(11):2137–2142, 2004.
pubmed: 15345516
doi: 10.1161/01.ATV.0000143933.20616.1b
Partida, R. A., P. Libby, F. Crea, and I. K. Jang. Plaque erosion: a new in vivo diagnosis and a potential major shift in the management of patients with acute coronary syndromes. Eur. Heart J. 39(22):2070–2076, 2018.
pubmed: 29329384
pmcid: 5991215
doi: 10.1093/eurheartj/ehx786
Quillard, T., H. A. Araujo, G. Franck, E. Shvartz, G. Sukhova, and P. Libby. TLR2 and neutrophils potentiate endothelial stress, apoptosis and detachment: implications for superficial erosion. Eur. Heart J. 36(22):1394–1404, 2015.
pubmed: 25755115
pmcid: 4458287
doi: 10.1093/eurheartj/ehv044
Gimbrone, M. A., Jr., and G. Garcia-Cardena. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ. Res. 118(4):620–636, 2016.
pubmed: 26892962
pmcid: 4762052
doi: 10.1161/CIRCRESAHA.115.306301
Son, H., H. S. Choi, S. E. Baek, Y. H. Kim, J. Hur, J. H. Han, J. H. Moon, G. S. Lee, S. G. Park, C. H. Woo, S. K. Eo, S. Yoon, B. S. Kim, D. Lee, and K. Kim. Shear stress induces monocyte/macrophage-mediated inflammation by upregulating cell-surface expression of heat shock proteins. Biomed. Pharmacother.161:114566, 2023.
pubmed: 36963359
doi: 10.1016/j.biopha.2023.114566
Luo, X., Y. Lv, X. Bai, J. Qi, X. Weng, S. Liu, X. Bao, H. Jia, and B. Yu. Plaque erosion: a distinctive pathological mechanism of acute coronary syndrome. Front. Cardiovasc. Med.8:711453, 2021.
pubmed: 34651023
pmcid: 8505887
doi: 10.3389/fcvm.2021.711453
Chandran, S., J. Watkins, A. Abdul-Aziz, M. Shafat, P. A. Calvert, K. M. Bowles, M. D. Flather, S. A. Rushworth, and A. D. Ryding. Inflammatory differences in plaque erosion and rupture in patients with ST-segment elevation myocardial infarction. J. Am. Heart Assoc. 6(5):e005868, 2017.
pubmed: 28468787
pmcid: 5524113
doi: 10.1161/JAHA.117.005868
Wang, L., Z. Huang, W. Huang, X. Chen, P. Shan, P. Zhong, Z. Khan, J. Wang, Q. Fang, G. Liang, and Y. Wang. Inhibition of epidermal growth factor receptor attenuates atherosclerosis via decreasing inflammation and oxidative stress. Sci. Rep. 8:45917, 2017.
pubmed: 28374780
doi: 10.1038/srep45917
Zeboudj, L., A. Giraud, L. Guyonnet, Y. Zhang, L. Laurans, B. Esposito, J. Vilar, A. Chipont, N. Papac-Milicevic, C. J. Binder, A. Tedgui, Z. Mallat, P. L. Tharaux, and H. Ait-Oufella. Selective EGFR (epidermal growth factor receptor) deletion in myeloid cells limits atherosclerosis-brief report. Arterioscler. Thromb. Vasc. Biol. 38(1):114–119, 2018.
pubmed: 29191921
doi: 10.1161/ATVBAHA.117.309927
Nath, S., M. Pigula, A. P. Khan, W. Hanna, M. K. Ruhi, F. M. Dehkordy, K. Pushpavanam, K. Rege, K. Moore, Y. Tsujita, C. Conrad, F. Inci, M. G. D. Carmen, W. Franco, J. P. Celli, U. Demirci, T. Hasan, H. C. Huang, and I. Rizvi. Flow-induced shear stress confers resistance to carboplatin in an adherent three-dimensional model for ovarian cancer: a role for EGFR-targeted photoimmunotherapy informed by physical stress. J. Clin. Med. 9(4):924, 2020.
pubmed: 32231055
pmcid: 7230263
doi: 10.3390/jcm9040924
Chen, B., R. T. Bronson, L. D. Klaman, T. G. Hampton, J. F. Wang, P. J. Green, T. Magnuson, P. S. Douglas, J. P. Morgan, and B. G. Neel. Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nat. Genet. 24(3):296–299, 2000.
pubmed: 10700187
doi: 10.1038/73528
Barrick, C. J., R. B. Roberts, M. Rojas, N. M. Rajamannan, C. B. Suitt, K. D. O’Brien, S. S. Smyth, and D. W. Threadgill. Reduced EGFR causes abnormal valvular differentiation leading to calcific aortic stenosis and left ventricular hypertrophy in C57BL/6J but not 129S1/SvImJ mice. Am. J. Physiol. Heart Circ. Physiol. 297(1):H65-75, 2009.
pubmed: 19448146
pmcid: 2711734
doi: 10.1152/ajpheart.00866.2008
Linglart, L., and B. D. Gelb. Congenital heart defects in Noonan syndrome: diagnosis, management, and treatment. Am. J. Med. Genet. C. 184(1):73–80, 2020.
doi: 10.1002/ajmg.c.31765
Krenz, M., K. E. Yutzey, and J. Robbins. Noonan syndrome mutation Q79R in Shp2 increases proliferation of valve primordia mesenchymal cells via extracellular signal-regulated kinase 1/2 signaling. Circ. Res. 97(8):813–820, 2005.
pubmed: 16166557
pmcid: 1388074
doi: 10.1161/01.RES.0000186194.06514.b0
Blume, C., X. Kraus, S. Heene, S. Loewner, N. Stanislawski, F. Cholewa, and H. Blume. Vascular implants—new aspects for in situ tissue engineering. Eng. Life Sci. 22(3–4):344–360, 2022.
pubmed: 35382534
pmcid: 8961049
doi: 10.1002/elsc.202100100
Wissing, T. B., V. Bonito, E. E. van Haaften, M. van Doeselaar, M. Brugmans, H. M. Janssen, C. V. C. Bouten, and A. Smits. Macrophage-driven biomaterial degradation depends on scaffold microarchitecture. Front. Bioeng. Biotechnol. 7:87, 2019.
pubmed: 31080796
pmcid: 6497794
doi: 10.3389/fbioe.2019.00087
Tang, D., S. Chen, D. Hou, J. Gao, L. Jiang, J. Shi, Q. Liang, D. Kong, and S. Wang. Regulation of macrophage polarization and promotion of endothelialization by NO generating and PEG-YIGSR modified vascular graft. Mater. Sci. Eng. C. 84:1–11, 2018.
doi: 10.1016/j.msec.2017.11.005
Zhu, A. S., T. Mustafa, J. P. Connell, and K. J. Grande-Allen. Tumor necrosis factor alpha and interleukin 1 beta suppress myofibroblast activation via nuclear factor kappa B signaling in 3D-cultured mitral valve interstitial cells. Acta Biomater. 127:159–168, 2021.
pubmed: 33831572
pmcid: 10349650
doi: 10.1016/j.actbio.2021.03.075
Shi, Q., L. Cheng, Z. Liu, K. Hu, J. Ran, D. Ge, and J. Fu. The p38 MAPK inhibitor SB203580 differentially modulates LPS-induced interleukin 6 expression in macrophages. Cent. Eur. J. Immunol. 40(3):276–282, 2015.
pubmed: 26648769
pmcid: 4655375
doi: 10.5114/ceji.2015.54586
Evers, T. M. J., L. J. Holt, S. Alberti, and A. Mashaghi. Reciprocal regulation of cellular mechanics and metabolism. Nat. Metab. 3(4):456–468, 2021.
pubmed: 33875882
pmcid: 8863344
doi: 10.1038/s42255-021-00384-w
Cai, X., K. C. Wang, and Z. Meng. Mechanoregulation of YAP and TAZ in cellular homeostasis and disease progression. Front. Cell. Dev. Biol.9:673599, 2021.
pubmed: 34109179
pmcid: 8182050
doi: 10.3389/fcell.2021.673599
Mia, M. M., D. M. Cibi, S. A. B. A. Ghani, W. Song, N. Tee, S. Ghosh, J. Mao, E. N. Olson, and M. K. Singh. YAP/TAZ deficiency reprograms macrophage phenotype and improves infarct healing and cardiac function after myocardial infarction. PLoS Biol. 18(12):e3000941, 2020.
pubmed: 33264286
pmcid: 7735680
doi: 10.1371/journal.pbio.3000941