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Annals of Biomedical Engineering

, Volume 47, Issue 11, pp 2213–2231 | Cite as

Mechano-Immunomodulation: Mechanoresponsive Changes in Macrophage Activity and Polarization

  • Sarah Adams
  • Leah M. Wuescher
  • Randall Worth
  • Eda Yildirim-AyanEmail author
Article

Abstract

In recent years, biomaterial- and scaffold-based immunomodulation strategies were implemented in tissue regeneration efforts for manipulating macrophage polarization (a.k.a. phenotype or lineage commitment, or differentiation). Yet, most of our understanding of macrophage phenotype commitment and phagocytic capacity is limited to how physical cues (extracellular matrix stiffness, roughness, and topography) and soluble chemical cues (cytokines and chemokines released from the scaffold) influence macrophage polarization. In the context of immune response–tissue interaction, the mechanical cues experienced by the residing cells within the tissue also play a critical role in macrophage polarization and inflammatory response. However, there is no compiled study discussing the effect of the dynamic mechanical environment around the tissues on macrophage polarization and the innate immune response. The aim of this comprehensive review paper is 2-fold; (a) to highlight the importance of mechanical cues on macrophage lineage commitment and function and (b) to summarize the important studies dedicated to understand how macrophage polarization changes with different mechanical loading modalities. For the first time, this review paper compiles and compartmentalizes the studies investigating the role of dynamic mechanical loading with various modalities, amplitude, and frequency on macrophage differentiation. A deeper understanding of macrophage phenotype in mechanically dominant tissues (i.e. musculoskeletal tissues, lung tissues, and cardiovascular tissues) provides mechanistic insights into the design of mechano-immunomodulatory tissue scaffold for tissue regeneration.

Keywords

Macrophages Polarization Immunomodulation Mechanical strain Mechanotransduction Tissue engineering Mechanoimmunomodulation Anti-inflammatory Pro-inflammatory Phagocytic activity 

Notes

Acknowledgments

This study was supported in part by National Institutes of Health, National Heart, Lung, and Blood Institute (HL122401 to RGW).

References

  1. 1.
    Alpers, C. E., K. L. Hudkins, P. Pritzl, and R. J. Johnson. Mechanisms of clearance of immune complexes from peritubular capillaries in the rat. Am. J. Pathol. 139(4):855–867, 1991; (Epub 1991/10/01).PubMedPubMedCentralGoogle Scholar
  2. 2.
    Arazi, A., and A. U. Neumann. Modeling immune complex-mediated autoimmune inflammation. J. Theor. Biol. 267(3):426–436, 2010.  https://doi.org/10.1016/j.jtbi.2010.08.033; (Epub 2010/09/14).CrossRefPubMedGoogle Scholar
  3. 3.
    Badylak, S. F., J. E. Valentin, A. K. Ravindra, G. P. McCabe, and A. M. Stewart-Akers. Macrophage phenotype as a determinant of biologic scaffold remodeling. Tissue Eng. A 14(11):1835–1842, 2008.CrossRefGoogle Scholar
  4. 4.
    Ballotta, V., A. Driessen-Mol, C. V. Bouten, and F. P. Baaijens. Strain-dependent modulation of macrophage polarization within scaffolds. Biomaterials 35(18):4919–4928, 2014.  https://doi.org/10.1016/j.biomaterials.2014.03.002.CrossRefPubMedGoogle Scholar
  5. 5.
    Barcelli, U., R. Rademacher, Y. M. Ooi, and B. S. Ooi. Modification of glomerular immune complex deposition in mice by activation of the reticuloendothelial system. J. Clin. Investig. 67(1):20–27, 1981.  https://doi.org/10.1172/jci110013; (Epub 1981/01/01).CrossRefPubMedGoogle Scholar
  6. 6.
    Bartneck, M., K. H. Heffels, Y. Pan, M. Bovi, G. Zwadlo-Klarwasser, and J. Groll. Inducing healing-like human primary macrophage phenotypes by 3D hydrogel coated nanofibres. Biomaterials 33(16):4136–4146, 2012.  https://doi.org/10.1016/j.biomaterials.2012.02.050; (Epub 2012/03/16).CrossRefPubMedGoogle Scholar
  7. 7.
    Bentzon, J. F., and E. Falk. Atherosclerotic lesions in mouse and man: is it the same disease? Curr. Opin. Lipidol. 21(5):434–440, 2010.  https://doi.org/10.1097/mol.0b013e32833ded6a; (Epub 2010/08/05).CrossRefPubMedGoogle Scholar
  8. 8.
    Blakney, A. K., M. D. Swartzlander, and S. J. Bryant. The effects of substrate stiffness on the in vitro activation of macrophages and in vivo host response to poly(ethylene glycol)-based hydrogels. J. Biomed. Mater. Res. A 100(6):1375–1386, 2012.  https://doi.org/10.1002/jbm.a.34104.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Boyle, J. J. Heme and haemoglobin direct macrophage Mhem phenotype and counter foam cell formation in areas of intraplaque haemorrhage. Curr. Opin. Lipidol. 23(5):453–461, 2012.  https://doi.org/10.1097/mol.0b013e328356b145.CrossRefPubMedGoogle Scholar
  10. 10.
    Broughton, II, G., J. E. Janis, and C. E. Attinger. The basic science of wound healing. Plast. Reconstr. Surg. 117(7 Suppl):12S–34S, 2006.  https://doi.org/10.1097/01.prs.0000225430.42531.c2.CrossRefPubMedGoogle Scholar
  11. 11.
    Brown, B. N., B. M. Sicari, and S. F. Badylak. Rethinking regenerative medicine: a macrophage-centered approach. Front. Immunol. 5:510, 2014.  https://doi.org/10.3389/fimmu.2014.00510.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Bryckaert, M., J. P. Rosa, C. V. Denis, and P. J. Lenting. Of von Willebrand factor and platelets. Cell Mol. Life Sci. 72(2):307–326, 2015.  https://doi.org/10.1007/s00018-014-1743-8; (Epub 2014/10/10).CrossRefPubMedGoogle Scholar
  13. 13.
    Castro-Nunez, L., I. Dienava-Verdoold, E. Herczenik, K. Mertens, and A. B. Meijer. Shear stress is required for the endocytic uptake of the factor VIII–von Willebrand factor complex by macrophages. J. Thromb. Haemost. 10(9):1929–1937, 2012.  https://doi.org/10.1111/j.1538-7836.2012.04860.x; (Epub 2012/07/21).CrossRefPubMedGoogle Scholar
  14. 14.
    Cheng, C., D. Tempel, R. van Haperen, A. van der Baan, F. Grosveld, M. J. Daemen, R. Krams, and R. de Crom. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113(23):2744–2753, 2006.  https://doi.org/10.1161/circulationaha.105.590018.CrossRefPubMedGoogle Scholar
  15. 15.
    Cikes, M., G. R. Sutherland, L. J. Anderson, and B. H. Bijnens. The role of echocardiographic deformation imaging in hypertrophic myopathies. Nat. Rev. Cardiol. 7(7):384–396, 2010.CrossRefGoogle Scholar
  16. 16.
    De Wilde, D., B. Trachet, G. R. 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.  https://doi.org/10.1007/s10439-015-1540-z; (Epub 2015/12/24).CrossRefPubMedGoogle Scholar
  17. 17.
    Denis, C. V., and P. J. Lenting. vWF clearance: it’s glycomplicated. Blood 131(8):842–843, 2018.  https://doi.org/10.1182/blood-2018-01-824904; (Epub 2018/02/24).CrossRefPubMedGoogle Scholar
  18. 18.
    Dhawan, S. S., R. P. Avati Nanjundappa, J. R. Branch, W. R. Taylor, A. A. Quyyumi, H. Jo, M. C. McDaniel, J. Suo, D. Giddens, and H. Samady. Shear stress and plaque development. Expert Rev. Cardiovasc. Ther. 8(4):545–556, 2010.  https://doi.org/10.1586/erc.10.28; (Epub 2010/04/20).CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Dziki, J. L., R. M. Giglio, B. M. Sicari, D. S. Wang, R. M. Gandhi, R. Londono, C. L. Dearth, and S. F. Badylak. The effect of mechanical loading upon extracellular matrix bioscaffold-mediated skeletal muscle remodeling. Tissue Eng. A 24(1–2):34–46, 2018.  https://doi.org/10.1089/ten.tea.2017.0011.CrossRefGoogle Scholar
  20. 20.
    Edwards, J. P., X. Zhang, K. A. Frauwirth, and D. M. Mosser. Biochemical and functional characterization of three activated macrophage populations. J. Leukoc. Biol. 80(6):1298–1307, 2006.  https://doi.org/10.1189/jlb.0406249.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Elsaadany, M., M. Harris, and E. Yildirim-Ayan. Design and validation of equiaxial mechanical strain platform, EQUicycler, for 3D tissue engineered constructs. Biomed. Res. Int. 2017.  https://doi.org/10.1155/2017/3609703; (Epub 2017/02/09).CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Evans, B. J., D. O. Haskard, G. Sempowksi, and R. C. Landis. Evolution of the macrophage CD163 phenotype and cytokine profiles in a human model of resolving inflammation. Int. J. Inflamm. 2013:780502, 2013.  https://doi.org/10.1155/2013/780502.CrossRefGoogle Scholar
  23. 23.
    Ferrante, C. J., and S. J. Leibovich. Regulation of macrophage polarization and wound healing. Adv Wound Care (New Rochelle) 1(1):10–16, 2012.  https://doi.org/10.1089/wound.2011.0307.CrossRefGoogle Scholar
  24. 24.
    Ferrier, G. M., A. McEvoy, C. E. Evans, and J. G. Andrew. The effect of cyclic pressure on human monocyte-derived macrophages in vitro. J. Bone Jt Surg. Br. Vol. 82(5):755–759, 2000.CrossRefGoogle Scholar
  25. 25.
    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. 2017.  https://doi.org/10.1002/adhm.201600967.CrossRefPubMedGoogle Scholar
  26. 26.
    Fujishiro, T., T. Nishikawa, N. Shibanuma, T. Akisue, S. Takikawa, T. Yamamoto, S. Yoshiya, and M. Kurosaka. Effect of cyclic mechanical stretch and titanium particles on prostaglandin E2 production by human macrophages in vitro. J. Biomed. Mater. Res. A 68(3):531–536, 2004.  https://doi.org/10.1002/jbm.a.20098.CrossRefPubMedGoogle Scholar
  27. 27.
    Fukunaga, T., K. Kubo, Y. Kawakami, S. Fukashiro, H. Kanehisa, and C. N. Maganaris. In vivo behaviour of human muscle tendon during walking. Proc. Biol. Sci. 268(1464):229–233, 2001.  https://doi.org/10.1098/rspb.2000.1361.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Garash, R., A. Bajpai, B. M. Marcinkiewicz, and K. L. Spiller. Drug delivery strategies to control macrophages for tissue repair and regeneration. Exp. Biol. Med. (Maywood) 241(10):1054–1063, 2016.  https://doi.org/10.1177/1535370216649444.CrossRefGoogle Scholar
  29. 29.
    Garg, K., N. A. Pullen, C. A. Oskeritzian, J. J. Ryan, and G. L. Bowlin. Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds. Biomaterials 34:4439, 2013.CrossRefGoogle Scholar
  30. 30.
    Genet, M., L. C. Lee, R. Nguyen, H. Haraldsson, G. Acevedo-Bolton, Z. H. Zhang, L. Ge, K. Ordovas, S. Kozerke, and J. M. Guccione. Distribution of normal human left ventricular myofiber stress at end diastole and end systole: a target for in silico design of heart failure treatments. J. Appl. Physiol. 117(2):142–152, 2014.  https://doi.org/10.1152/japplphysiol.00255.2014.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Gonzalez, M. L., and F. J. Waxman. Relationship between complement activation and renal deposition of immune complexes made with IgG2a monoclonal antibodies. Clin. Immunol. 100(3):362–371, 2001.  https://doi.org/10.1006/clim.2001.5077; (Epub 2001/08/22).CrossRefPubMedGoogle Scholar
  32. 32.
    Gundra, U. M., N. M. Girgis, D. Ruckerl, S. Jenkins, L. N. Ward, Z. D. Kurtz, K. E. Wiens, M. S. Tang, U. Basu-Roy, A. Mansukhani, J. E. Allen, and P. Loke. Alternatively activated macrophages derived from monocytes and tissue macrophages are phenotypically and functionally distinct. Blood 123(20):e110–e122, 2014.  https://doi.org/10.1182/blood-2013-08-520619.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Hansen, P., J. Bojsen-Moller, P. Aagaard, M. Kjaer, and S. P. Magnusson. Mechanical properties of the human patellar tendon, in vivo. Clin. Biomech. (Bristol Avon) 21(1):54–58, 2006.  https://doi.org/10.1016/j.clinbiomech.2005.07.008.CrossRefGoogle Scholar
  34. 34.
    Harwani, S. C. Macrophages under pressure: the role of macrophage polarization in hypertension. Transl. Res. 191:45–63, 2018.  https://doi.org/10.1016/j.trsl.2017.10.011.CrossRefPubMedGoogle Scholar
  35. 35.
    Heo, K. S., K. Fujiwara, and J. Abe. Shear stress and atherosclerosis. Mol. Cells 37(6):435–440, 2014.  https://doi.org/10.14348/molcells.2014.0078; (Epub 2014/05/02).CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Hesketh, M., K. B. Sahin, Z. E. West, and R. Z. Murray. Macrophage phenotypes regulate scar formation and chronic wound healing. Int. J. Mol. Sci. 2017.  https://doi.org/10.3390/ijms18071545.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Hong, J. E., Y. C. Kye, S. M. Park, I. S. Cheon, H. Chu, B. C. Park, Y. M. Park, J. Chang, J. H. Cho, M. K. Song, S. H. Han, and C. H. Yun. Alveolar macrophages treated with Bacillus subtilis spore protect mice infected with respiratory syncytial virus A2. Front. Microbiol. 10:447, 2019.  https://doi.org/10.3389/fmicb.2019.00447; (Epub 2019/04/02).CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Hotchkiss, K. M., G. B. Reddy, S. L. Hyzy, Z. Schwartz, B. D. Boyan, and R. Olivares-Navarrete. Titanium surface characteristics, including topography and wettability, alter macrophage activation. Acta Biomater. 31:425–434, 2016.  https://doi.org/10.1016/j.actbio.2015.12.003.CrossRefPubMedGoogle Scholar
  39. 39.
    Hwang, J., A. Saha, Y. C. Boo, G. P. Sorescu, J. S. McNally, S. M. Holland, S. Dikalov, D. P. Giddens, K. K. Griendling, D. G. Harrison, and H. Jo. Oscillatory shear stress stimulates endothelial production of O2 from p47 phox-dependent NAD(P)H oxidases, leading to monocyte adhesion. J. Biol. Chem. 278(47):47291–47298, 2003.  https://doi.org/10.1074/jbc.m305150200; (Epub 2003/09/06).CrossRefPubMedGoogle Scholar
  40. 40.
    Ingersoll, M. A., R. Spanbroek, C. Lottaz, E. L. Gautier, M. Frankenberger, R. Hoffmann, R. Lang, M. Haniffa, M. Collin, F. Tacke, A. J. Habenicht, L. Ziegler-Heitbrock, and G. J. Randolph. Comparison of gene expression profiles between human and mouse monocyte subsets. Blood 115(3):e10–e19, 2010.  https://doi.org/10.1182/blood-2009-07-235028; (Epub 2009/12/08).CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Johnson, G. A., D. M. Tramaglini, R. E. Levine, K. Ohno, N. Y. Choi, and S. L. Woo. Tensile and viscoelastic properties of human patellar tendon. J. Orthop. Res. 12(6):796–803, 1994.  https://doi.org/10.1002/jor.1100120607.CrossRefPubMedGoogle Scholar
  42. 42.
    Jung, S. H., A. Saxena, K. Kaur, E. Fletcher, V. Ponemone, J. M. Nottingham, J. A. Sheppe, M. Petroni, J. Greene, K. Graves, M. S. Baliga, and R. Fayad. The role of adipose tissue-associated macrophages and T lymphocytes in the pathogenesis of inflammatory bowel disease. Cytokine 61(2):459–468, 2013.  https://doi.org/10.1016/j.cyto.2012.11.021; (Epub 2012/12/19).CrossRefPubMedGoogle Scholar
  43. 43.
    Kongsgaard, M., C. H. Nielsen, S. Hegnsvad, P. Aagaard, and S. P. Magnusson. Mechanical properties of the human Achilles tendon, in vivo. Clin. Biomech. (Bristol Avon) 26(7):772–777, 2011.  https://doi.org/10.1016/j.clinbiomech.2011.02.011.CrossRefGoogle Scholar
  44. 44.
    Kratochvill, F., G. Neale, J. M. Haverkamp, L. A. Van de Velde, A. M. Smith, D. Kawauchi, J. McEvoy, M. F. Roussel, M. A. Dyer, J. E. Qualls, and P. J. Murray. TNF counterbalances the emergence of M2 tumor macrophages. Cell Rep. 12(11):1902–1914, 2015.  https://doi.org/10.1016/j.celrep.2015.08.033.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Krzyszczyk, P., R. Schloss, A. Palmer, and F. Berthiaume. The role of macrophages in acute and chronic wound healing and interventions to promote pro-wound healing phenotypes. Front. Physiol. 9:419, 2018.  https://doi.org/10.3389/fphys.2018.00419.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Ku, D. N., D. P. Giddens, C. K. Zarins, and S. Glagov. Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5(3):293–302, 1985; (Epub 1985/05/01).CrossRefGoogle Scholar
  47. 47.
    Kwak, B. R., M. Back, M. L. Bochaton-Piallat, G. Caligiuri, M. J. Daemen, P. F. Davies, I. E. Hoefer, P. Holvoet, H. Jo, R. Krams, S. Lehoux, C. Monaco, S. Steffens, R. Virmani, C. Weber, J. J. Wentzel, and P. C. Evans. Biomechanical factors in atherosclerosis: mechanisms and clinical implications. Eur. Heart J. 35(43):3013–3020, 20a–20d, 2014.  https://doi.org/10.1093/eurheartj/ehu353 (Epub 2014/09/19).CrossRefGoogle Scholar
  48. 48.
    Lang, R., D. Patel, J. J. Morris, R. L. Rutschman, and P. J. Murray. Shaping gene expression in activated and resting primary macrophages by IL-10. J. Immunol. 169(5):2253–2263, 2002.  https://doi.org/10.4049/jimmunol.169.5.2253.CrossRefPubMedGoogle Scholar
  49. 49.
    Lehoux, S., and A. Tedgui. Cellular mechanics and gene expression in blood vessels. J. Biomech. 36(5):631–643, 2003; (Epub 2003/04/16).CrossRefGoogle Scholar
  50. 50.
    Li, J., Y. Li, B. Gao, C. Qin, Y. He, F. Xu, H. Yang, and M. Lin. Engineering mechanical microenvironment of macrophage and its biomedical applications. Nanomedicine (Lond.) 2018.  https://doi.org/10.2217/nnm-2017-0324.CrossRefGoogle Scholar
  51. 51.
    Libby, P., P. M. Ridker, and G. K. Hansson. Progress and challenges in translating the biology of atherosclerosis. Nature 473(7347):317–325, 2011.  https://doi.org/10.1038/nature10146; (Epub 2011/05/20).CrossRefPubMedGoogle Scholar
  52. 52.
    Luu, T. U., S. C. Gott, B. W. Woo, M. P. Rao, and W. F. Liu. Micro- and nanopatterned topographical cues for regulating macrophage cell shape and phenotype. ACS Appl. Mater. Interfaces 7(51):28665–28672, 2015.  https://doi.org/10.1021/acsami.5b10589.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Maganaris, C. N., and J. P. Paul. In vivo human tendon mechanical properties. J Physiol. 521(Pt 1):307–313, 1999.CrossRefGoogle Scholar
  54. 54.
    Malissen, B., S. Tamoutounour, and S. Henri. The origins and functions of dendritic cells and macrophages in the skin. Nat. Rev. Immunol. 14(6):417–428, 2014.  https://doi.org/10.1038/nri3683.CrossRefPubMedGoogle Scholar
  55. 55.
    Martinez, F. O., and S. Gordon. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6(13.10):12703, 2014.Google Scholar
  56. 56.
    Matheson, L. A., N. J. Fairbank, G. N. Maksym, J. Paul Santerre, and R. S. Labow. Characterization of the Flexcell Uniflex cyclic strain culture system with U937 macrophage-like cells. Biomaterials 27(2):226–233, 2006.  https://doi.org/10.1016/j.biomaterials.2005.05.070.CrossRefPubMedGoogle Scholar
  57. 57.
    Matheson, L. A., G. N. Maksym, J. P. Santerre, and R. S. Labow. Cyclic biaxial strain affects U937 macrophage-like morphology and enzymatic activities. J. Biomed. Mater. Res. A 76(1):52–62, 2006.  https://doi.org/10.1002/jbm.a.30448; (Epub 2005/10/15).CrossRefPubMedGoogle Scholar
  58. 58.
    Matheson, L. A., G. N. Maksym, J. P. Santerre, and R. S. Labow. The functional response of U937 macrophage-like cells is modulated by extracellular matrix proteins and mechanical strain. Biochem. Cell Biol. 84(5):763–773, 2006.  https://doi.org/10.1139/o06-093.CrossRefPubMedGoogle Scholar
  59. 59.
    Matsumoto, T., P. Delafontaine, K. J. Schnetzer, B. C. Tong, and R. M. Nerem. Effect of uniaxial, cyclic stretch on the morphology of monocytes/macrophages in culture. J. Biomech. Eng. 118(3):420–422, 1996; (Epub 1996/08/01).CrossRefGoogle Scholar
  60. 60.
    Mattana, J., R. T. Sankaran, and P. C. Singhal. Repetitive mechanical strain suppresses macrophage uptake of immunoglobulin G complexes and enhances cyclic adenosine monophosphate synthesis. Am. J. Pathol. 147(2):529–540, 1995.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Mattana, J., R. T. Sankaran, and P. C. Singhal. Increased applied pressure enhances the uptake of IgG complexes by macrophages. Pathobiology 64(1):40–45, 1996.  https://doi.org/10.1159/000164004.CrossRefPubMedGoogle Scholar
  62. 62.
    Matthews, J. B., W. Mitchell, M. H. Stone, J. Fisher, and E. Ingham. A novel three-dimensional tissue equivalent model to study the combined effects of cyclic mechanical strain and wear particles on the osteolytic potential of primary human macrophages in vitro. Proc. Inst. Mech. Eng. H 215(5):479–486, 2001.  https://doi.org/10.1243/0954411011536073.CrossRefPubMedGoogle Scholar
  63. 63.
    McEvoy, A., M. Jeyam, G. Ferrier, C. E. Evans, and J. G. Andrew. Synergistic effect of particles and cyclic pressure on cytokine production in human monocyte/macrophages: proposed role in periprosthetic osteolysis. Bone 30(1):171–177, 2002.CrossRefGoogle Scholar
  64. 64.
    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.  https://doi.org/10.1073/pnas.1308887110.CrossRefPubMedGoogle Scholar
  65. 65.
    Mestas, J., and C. C. Hughes. Of mice and not men: differences between mouse and human immunology. J. Immunol. (Baltim. Md 1950) 172(5):2731–2738, 2004.  https://doi.org/10.4049/jimmunol.172.5.2731; (Epub 2004/02/24).CrossRefGoogle Scholar
  66. 66.
    Miles, S. A., S. M. Conrad, R. G. Alves, S. M. Jeronimo, and D. M. Mosser. A role for IgG immune complexes during infection with the intracellular pathogen Leishmania. J. Exp. Med. 201(5):747–754, 2005.  https://doi.org/10.1084/jem.20041470; (Epub 2005/03/09).CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Minardi, S., B. Corradetti, F. Taraballi, J. H. Byun, F. Cabrera, X. Liu, M. Ferrari, B. K. Weiner, and E. Tasciotti. IL-4 release from a biomimetic scaffold for the temporally controlled modulation of macrophage response. Ann. Biomed. Eng. 44(6):2008–2019, 2016.  https://doi.org/10.1007/s10439-016-1580-z.CrossRefPubMedGoogle Scholar
  68. 68.
    Minutti, C. M., J. A. Knipper, J. E. Allen, and D. M. Zaiss. Tissue-specific contribution of macrophages to wound healing. Semin. Cell Dev. Biol. 61:3–11, 2017.  https://doi.org/10.1016/j.semcdb.2016.08.006.CrossRefPubMedGoogle Scholar
  69. 69.
    Miyazaki, H., and K. Hayashi. Effects of cyclic strain on the morphology and phagocytosis of macrophages. Biomed. Mater. Eng. 11(4):301–309, 2001.PubMedGoogle Scholar
  70. 70.
    Moreno, P. R., E. Falk, I. F. Palacios, J. B. Newell, V. Fuster, and J. T. Fallon. Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture. Circulation 90(2):775–778, 1994; (Epub 1994/08/01).CrossRefGoogle Scholar
  71. 71.
    Mourgeon, E., N. Isowa, S. Keshavjee, X. Zhang, A. S. Slutsky, and M. Liu. Mechanical stretch stimulates macrophage inflammatory protein-2 secretion from fetal rat lung cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 279(4):L699–L706, 2000.  https://doi.org/10.1152/ajplung.2000.279.4.l699; (Epub 2000/09/23).CrossRefPubMedGoogle Scholar
  72. 72.
    Munder, M., K. Eichmann, and M. Modolell. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J. Immunol. 160(11):5347–5354, 1998.PubMedGoogle Scholar
  73. 73.
    Munder, M., K. Eichmann, J. M. Moran, F. Centeno, G. Soler, and M. Modolell. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163(7):3771–3777, 1999.PubMedGoogle Scholar
  74. 74.
    Murray, P. J. Macrophage polarization. Annu. Rev. Physiol. 79:541–566, 2017.  https://doi.org/10.1146/annurev-physiol-022516-034339.CrossRefPubMedGoogle Scholar
  75. 75.
    Ogle, M. E., C. E. Segar, S. Sridhar, and E. A. Botchwey. Monocytes and macrophages in tissue repair: implications for immunoregenerative biomaterial design. Exp. Biol. Med. (Maywood) 241(10):1084–1097, 2016.  https://doi.org/10.1177/1535370216650293.CrossRefGoogle Scholar
  76. 76.
    Ohki, R., K. Yamamoto, H. Mano, R. T. Lee, U. Ikeda, and K. Shimada. Identification of mechanically induced genes in human monocytic cells by DNA microarrays. J. Hypertens. 20(4):685–691, 2002.CrossRefGoogle Scholar
  77. 77.
    Olivon, V. C., R. A. Fraga-Silva, D. Segers, C. Demougeot, A. M. de Oliveira, S. S. Savergnini, A. Berthelot, R. de Crom, R. Krams, N. Stergiopulos, and R. F. da Silva. Arginase inhibition prevents the low shear stress-induced development of vulnerable atherosclerotic plaques in ApoE−/− mice. Atherosclerosis 227(2):236–243, 2013.  https://doi.org/10.1016/j.atherosclerosis.2012.12.014; (Epub 2013/02/09).CrossRefPubMedGoogle Scholar
  78. 78.
    Pugin, J., I. Dunn, P. Jolliet, D. Tassaux, J. L. Magnenat, L. P. Nicod, and J. C. Chevrolet. Activation of human macrophages by mechanical ventilation in vitro. Am. J. Physiol. 275(6 Pt 1):L1040–L1050, 1998.PubMedGoogle Scholar
  79. 79.
    Purdue, P. E. Alternative macrophage activation in periprosthetic osteolysis. Autoimmunity 41(3):212–217, 2008.  https://doi.org/10.1080/08916930701694626.CrossRefPubMedGoogle Scholar
  80. 80.
    Raes, G., R. Van den Bergh, P. De Baetselier, G. H. Ghassabeh, C. Scotton, M. Locati, A. Mantovani, and S. Sozzani. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J. Immunol. (Baltim. Md 1950) 174(11):6561; author reply -2, 2005.  https://doi.org/10.4049/jimmunol.174.11.6561 (Epub 2005/05/21).CrossRefGoogle Scholar
  81. 81.
    Rao, A. J., E. Gibon, T. Ma, Z. Yao, R. L. Smith, and S. B. Goodman. Revision joint replacement, wear particles, and macrophage polarization. Acta Biomater. 8(7):2815–2823, 2012.  https://doi.org/10.1016/j.actbio.2012.03.042.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Rojko, J. L., M. G. Evans, S. A. Price, B. Han, G. Waine, M. DeWitte, J. Haynes, B. Freimark, P. Martin, J. T. Raymond, W. Evering, M. C. Rebelatto, E. Schenck, and C. Horvath. Formation, clearance, deposition, pathogenicity, and identification of biopharmaceutical-related immune complexes: review and case studies. Toxicol. Pathol. 42(4):725–764, 2014.  https://doi.org/10.1177/0192623314526475; (Epub 2014/04/08).CrossRefPubMedGoogle Scholar
  83. 83.
    Rosenson-Schloss, R. S., J. L. Vitolo, and P. V. Moghe. Flow-mediated cell stress induction in adherent leukocytes is accompanied by modulation of morphology and phagocytic function. Med. Biol. Eng. Comput. 37(2):257–263, 1999.CrossRefGoogle Scholar
  84. 84.
    Roszer, T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediat. Inflamm. 2015:816460, 2015.  https://doi.org/10.1155/2015/816460.CrossRefGoogle Scholar
  85. 85.
    Santerre, J. P., R. S. Labow, and E. L. Boynton. The role of the macrophage in periprosthetic bone loss. Can. J. Surg. 43(3):173–179, 2000.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Schache, A. G., T. W. Dorn, P. D. Blanch, N. A. Brown, and M. G. Pandy. Mechanics of the human hamstring muscles during sprinting. Med. Sci. Sports Exerc. 44(4):647–658, 2012.  https://doi.org/10.1249/mss.0b013e318236a3d2.CrossRefPubMedGoogle Scholar
  87. 87.
    Schaffer, J. L., M. Rizen, G. J. L’Italien, A. Benbrahim, J. Megerman, L. C. Gerstenfeld, and M. L. Gray. Device for the application of a dynamic biaxially uniform and isotropic strain to a flexible cell culture membrane. J. Orthop. Res. 12(5):709–719, 1994.  https://doi.org/10.1002/jor.1100120514.CrossRefPubMedGoogle Scholar
  88. 88.
    Schleicher, U., K. Paduch, A. Debus, S. Obermeyer, T. Konig, J. C. Kling, E. Ribechini, D. Dudziak, D. Mougiakakos, P. J. Murray, R. Ostuni, H. Korner, and C. Bogdan. TNF-mediated restriction of arginase 1 expression in myeloid cells triggers Type 2 NO synthase activity at the site of infection. Cell Rep. 15(5):1062–1075, 2016.  https://doi.org/10.1016/j.celrep.2016.04.001.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Schneemann, M., and G. Schoeden. Macrophage biology and immunology: man is not a mouse. J. Leukoc. Biol. 81(3):579, 2007.  https://doi.org/10.1189/jlb.1106702; (Epub 2007/03/01).CrossRefPubMedGoogle Scholar
  90. 90.
    Schneemann, M., and G. Schoedon. Species differences in macrophage NO production are important. Nat. Immunol. 3(2):102, 2002.  https://doi.org/10.1038/ni0202-102a; (Epub 2002/01/29).CrossRefPubMedGoogle Scholar
  91. 91.
    Seifert, R., M. T. Kuhlmann, S. Eligehausen, F. Kiefer, S. Hermann, and M. Schafers. Molecular imaging of MMP activity discriminates unstable from stable plaque phenotypes in shear-stress induced murine atherosclerosis. PLoS ONE 13(10):e0204305, 2018.  https://doi.org/10.1371/journal.pone.0204305; (Epub 2018/10/12).CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Seneviratne, A. N., J. E. Cole, M. E. Goddard, Z. Mohri, R. Krams, and C. Monaco. Macrophage polarisation in shear stress modulated atherosclerotic plaque vulnerability. Atherosclerosis 225(2):E2-E, 2012.CrossRefGoogle Scholar
  93. 93.
    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.  https://doi.org/10.1016/j.yjmcc.2015.10.034.CrossRefPubMedGoogle Scholar
  94. 94.
    Seneviratne, A., M. Hulsmans, P. Holvoet, and C. Monaco. Biomechanical factors and macrophages in plaque stability. Cardiovasc. Res. 99(2):284–293, 2013.  https://doi.org/10.1093/cvr/cvt097; (Epub 2013/05/21).CrossRefPubMedGoogle Scholar
  95. 95.
    Seo, J., J. Y. Shin, J. Leijten, O. Jeon, A. B. Ozturk, J. Rouwkema, Y. C. Li, S. R. Shin, H. Hajiali, E. Alsberg, and A. Khademhosseini. Interconnectable dynamic compression bioreactors for combinatorial screening of cell mechanobiology in three dimensions. ACS Appl. Mater. Interfaces 10(16):13293–13303, 2018.CrossRefGoogle Scholar
  96. 96.
    Singhal, P. C., P. Sagar, S. Gupta, M. Arya, M. Gupta, A. Prasad, R. Loona, P. Sharma, and J. Mattana. Pressure modulates monocyte migration. Am. J. Hypertens. 10(11):1297–1301, 1997.CrossRefGoogle Scholar
  97. 97.
    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.  https://doi.org/10.1016/j.biomaterials.2014.02.012.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Spiller, K. L., E. A. Wrona, S. Romero-Torres, I. Pallotta, P. L. Graney, C. E. Witherel, L. M. Panicker, R. A. Feldman, A. M. Urbanska, L. Santambrogio, G. Vunjak-Novakovic, and D. O. Freytes. Differential gene expression in human, murine, and cell line-derived macrophages upon polarization. Exp. Cell Res. 347(1):1–13, 2016.  https://doi.org/10.1016/j.yexcr.2015.10.017.CrossRefPubMedGoogle Scholar
  99. 99.
    Sridharan, R., A. R. Cameron, D. J. Kelly, C. J. Kearney, and F. J. O’Brien. Biomaterial based modulation of macrophage polarization: a review and suggested design principles. Mater. Today 18(6):313–325, 2015.CrossRefGoogle Scholar
  100. 100.
    Stankevich, G. A., A. Gudima, V. D. Filimonov, H. Kluter, E. M. Mamontova, S. I. Tverdokhlebov, and J. Kzhyshkowska. Surface modification of biomaterials based on high-molecular polylactic acid and their effect on inflammatory reactions of primary human monocyte-derived macrophage: perspective of personalized therapy. Mater. Sci. Eng. C 51:117, 2015.CrossRefGoogle Scholar
  101. 101.
    Stone, P. H., A. U. Coskun, S. Kinlay, M. E. Clark, M. Sonka, A. Wahle, O. J. Ilegbusi, Y. Yeghiazarians, J. J. Popma, J. Orav, R. E. Kuntz, and C. L. Feldman. Effect of endothelial shear stress on the progression of coronary artery disease, vascular remodeling, and in-stent restenosis in humans: in vivo 6-month follow-up study. Circulation 108(4):438–444, 2003.  https://doi.org/10.1161/01.cir.0000080882.35274.ad; (Epub 2003/07/16).CrossRefPubMedGoogle Scholar
  102. 102.
    Subramanian, G., M. Elsaadany, C. Bialorucki, and E. Yildirim-Ayan. Creating homogenous strain distribution within 3D cell-encapsulated constructs using a simple and cost-effective uniaxial tensile bioreactor: design and validation study. Biotechnol. Bioeng. 114(8):1878–1887, 2017.  https://doi.org/10.1002/bit.26304; (Epub 2017/04/21).CrossRefPubMedGoogle Scholar
  103. 103.
    Svensson, R. B., P. Hansen, T. Hassenkam, B. T. Haraldsson, P. Aagaard, V. Kovanen, M. Krogsgaard, M. Kjaer, and S. P. Magnusson. Mechanical properties of human patellar tendon at the hierarchical levels of tendon and fibril. J. Appl. Physiol. (1985) 112(3):419–426, 2012.  https://doi.org/10.1152/japplphysiol.01172.2011.CrossRefGoogle Scholar
  104. 104.
    Taraballi, F., B. Corradetti, S. Minardi, S. Powel, F. Cabrera, J. L. Van Eps, B. K. Weiner, and E. Tasciotti. Biomimetic collagenous scaffold to tune inflammation by targeting macrophages. J. Tissue Eng. 7:2041731415624667, 2016.  https://doi.org/10.1177/2041731415624667.CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Trumbull, A., G. Subramanian, and E. Yildirim-Ayan. Mechanoresponsive musculoskeletal tissue differentiation of adipose-derived stem cells. Biomed. Eng. Online 15:43, 2016.  https://doi.org/10.1186/s12938-016-0150-9; (Epub 2016/04/23).CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    van der Vis, H., P. Aspenberg, R. de Kleine, W. Tigchelaar, and C. J. van Noorden. Short periods of oscillating fluid pressure directed at a titanium–bone interface in rabbits lead to bone lysis. Acta orthop. Scand. 69(1):5–10, 1998.CrossRefGoogle Scholar
  107. 107.
    van der Wal, A. C., A. E. Becker, C. M. van der Loos, and P. K. Das. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 89(1):36–44, 1994; (Epub 1994/01/01).CrossRefGoogle Scholar
  108. 108.
    Vishwakarma, A., N. S. Bhise, M. B. Evangelista, J. Rouwkema, M. R. Dokmeci, A. M. Ghaemmaghami, N. E. Vrana, and A. Khademhosseini. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends Biotechnol. 34(6):470–482, 2016.  https://doi.org/10.1016/j.tibtech.2016.03.009.CrossRefPubMedGoogle Scholar
  109. 109.
    Wehner, S., B. M. Buchholz, S. Schuchtrup, A. Rocke, N. Schaefer, M. Lysson, A. Hirner, and J. C. Kalff. Mechanical strain and TLR4 synergistically induce cell-specific inflammatory gene expression in intestinal smooth muscle cells and peritoneal macrophages. Am. J. Physiol. Gastrointest. Liver Physiol. 299(5):G1187–G1197, 2010.  https://doi.org/10.1152/ajpgi.00452.2009.CrossRefPubMedGoogle Scholar
  110. 110.
    Wren, T. A., S. A. Yerby, G. S. Beaupre, and D. R. Carter. Mechanical properties of the human Achilles tendon. Clin. Biomech. (Bristol Avon) 16(3):245–251, 2001; (Epub 2001/03/10).CrossRefGoogle Scholar
  111. 111.
    Xu, X. Y., C. Guo, Y. X. Yan, Y. Guo, R. X. Li, M. Song, and X. Z. Zhang. Differential effects of mechanical strain on osteoclastogenesis and osteoclast-related gene expression in RAW264.7 cells. Mol. Med. Rep. 6(2):409–415, 2012.  https://doi.org/10.3892/mmr.2012.908.CrossRefPubMedGoogle Scholar
  112. 112.
    Yamamoto, K., U. Ikeda, and K. Shimada. Role of mechanical stress in monocytes/macrophages: implications for atherosclerosis. Curr. Vasc. Pharmacol. 1(3):315–319, 2003; (Epub 2004/08/24).CrossRefGoogle Scholar
  113. 113.
    Yanagida, H., H. Yanase, K. M. Sanders, and S. M. Ward. Intestinal surgical resection disrupts electrical rhythmicity, neural responses, and interstitial cell networks. Gastroenterology 127(6):1748–1759, 2004; (Epub 2004/12/04).CrossRefGoogle Scholar
  114. 114.
    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.  https://doi.org/10.1016/s0002-9440(10)65051-1.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Biomedical Engineering Society 2019

Authors and Affiliations

  • Sarah Adams
    • 1
  • Leah M. Wuescher
    • 2
  • Randall Worth
    • 2
  • Eda Yildirim-Ayan
    • 1
    • 3
    Email author
  1. 1.Department of Bioengineering, College of EngineeringUniversity of ToledoToledoUSA
  2. 2.Department of Medical Microbiology and ImmunologyUniversity of Toledo College of Medicine and Life SciencesToledoUSA
  3. 3.Department of Orthopaedic SurgeryUniversity of Toledo Medical CenterToledoUSA

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