1932

Abstract

In addition to their early-recognized functions in host defense and the clearance of apoptotic cell debris, macrophages play vital roles in tissue development, homeostasis, and repair. If misregulated, they steer the progression of many inflammatory diseases. Much progress has been made in understanding the mechanisms underlying macrophage signaling, transcriptomics, and proteomics, under physiological and pathological conditions. Yet, the detailed mechanisms that tune circulating monocytes/macrophages and tissue-resident macrophage polarization, differentiation, specification, and their functional plasticity remain elusive. We review how physical factors affect macrophage phenotype and function, including how they hunt for particles and pathogens, as well as the implications for phagocytosis, autophagy, and polarization from proinflammatory to prohealing phenotype. We further discuss how this knowledge can be harnessed in regenerative medicine and for the design of new drugs and immune-modulatory drug delivery systems, biomaterials, and tissue scaffolds.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-bioeng-062117-121224
2019-06-04
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/bioeng/21/1/annurev-bioeng-062117-121224.html?itemId=/content/journals/10.1146/annurev-bioeng-062117-121224&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Odegaard JI, Chawla A. 2011. Alternative macrophage activation and metabolism. Annu. Rev. Pathol. Mech. Dis. 6:275–97
    [Google Scholar]
  2. 2.
    Ritz T, Krenkel O, Tacke F 2017. Dynamic plasticity of macrophage functions in diseased liver. Cell Immunol 330:175–82
    [Google Scholar]
  3. 3.
    Van den Bossche J, Saraber DL 2018. Metabolic regulation of macrophages in tissues. Cell Immunol 330:54–59
    [Google Scholar]
  4. 4.
    Okabe Y, Medzhitov R. 2016. Tissue biology perspective on macrophages. Nat. Immunol. 17:9–17
    [Google Scholar]
  5. 5.
    Wynn TA, Vannella KM. 2016. Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44:450–62
    [Google Scholar]
  6. 6.
    Franceschi C, Bonafe M, Valensin S, Olivieri F, De Luca M et al. 2000. Inflamm-aging. An evolutionary perspective on immunosenescence. Ann. N. Y. Acad. Sci. 908:244–54
    [Google Scholar]
  7. 7.
    Franceschi C, Garagnani P, Parini P, Giuliani C, Santoro A 2018. Inflammaging: a new immune-metabolic viewpoint for age-related diseases. Nat. Rev. Endocrinol. 14:576–90
    [Google Scholar]
  8. 8.
    Prattichizzo F, Bonafe M, Olivieri F, Franceschi C 2016. Senescence associated macrophages and “macroph-aging”: Are they pieces of the same puzzle. ? Aging 8:3159–60
    [Google Scholar]
  9. 9.
    McGrath KE, Frame JM, Palis J 2015. Early hematopoiesis and macrophage development. Semin. Immunol. 27:379–87
    [Google Scholar]
  10. 10.
    Ginhoux F, Guilliams M. 2016. Tissue-resident macrophage ontogeny and homeostasis. Immunity 44:439–49
    [Google Scholar]
  11. 11.
    Kurotaki D, Sasaki H, Tamura T 2017. Transcriptional control of monocyte and macrophage development. Int. Immunol. 29:97–107
    [Google Scholar]
  12. 12.
    Hoeffel G, Ginhoux F. 2018. Fetal monocytes and the origins of tissue-resident macrophages. Cell Immunol 330:5–15
    [Google Scholar]
  13. 13.
    Mass E. 2018. Delineating the origins, developmental programs and homeostatic functions of tissue-resident macrophages. Int. Immunol. 30:493–501
    [Google Scholar]
  14. 14.
    Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8:958–69
    [Google Scholar]
  15. 15.
    Murray PJ. 2017. Macrophage polarization. Annu. Rev. Physiol. 79:541–66
    [Google Scholar]
  16. 16.
    Jacob SS, Sudhakaran PR. 2002. Molecular mechanism involved in matrix dependent upregulation of matrix metalloproteinases in monocyte/macrophage. J. Biochem. Mol. Biol. Biophys. 6:335–40
    [Google Scholar]
  17. 17.
    DiNapoli MR, Calderon CL, Lopez DM 1997. Phosphatidyl serine is involved in the reduced rate of transcription of the inducible nitric oxide synthase gene in macrophages from tumor-bearing mice. J. Immunol. 158:1810–17
    [Google Scholar]
  18. 18.
    Roberts AW, Lee BL, Deguine J, John S, Shlomchik MJ, Barton GM 2017. Tissue-resident macrophages are locally programmed for silent clearance of apoptotic cells. Immunity 47:913–27
    [Google Scholar]
  19. 19.
    Guilliams M, Scott CL. 2017. Does niche competition determine the origin of tissue-resident macrophages?. Nat. Rev. Immunol. 17:451–60
    [Google Scholar]
  20. 20.
    Soncin I, Sheng J, Chen Q, Foo S, Duan K et al. 2018. The tumour microenvironment creates a niche for the self-renewal of tumour-promoting macrophages in colon adenoma. Nat. Commun. 9:582
    [Google Scholar]
  21. 21.
    Lawrence T, Natoli G. 2011. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 11:750–61
    [Google Scholar]
  22. 22.
    Wang N, Liang H, Zen K 2014. Molecular mechanisms that influence the macrophage M1-M2 polarization balance. Front. Immunol. 5:614
    [Google Scholar]
  23. 23.
    Martinez FO, Gordon S. 2014. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 6:13
    [Google Scholar]
  24. 24.
    Schlundt C, El Khassawna T, Serra A, Dienelt A, Wendler S et al. 2018. Macrophages in bone fracture healing: their essential role in endochondral ossification. Bone 106:78–89
    [Google Scholar]
  25. 25.
    Smith TD, Tse MJ, Read EL, Liu WF 2016. Regulation of macrophage polarization and plasticity by complex activation signals. Integr. Biol. 8:946–55
    [Google Scholar]
  26. 26.
    Le TT, Karmouty-Quintana H, Melicoff E, Le TT, Weng T et al. 2014. Blockade of IL-6 trans signaling attenuates pulmonary fibrosis. J. Immunol. 193:3755–68
    [Google Scholar]
  27. 27.
    Egeblad M, Littlepage LE, Werb Z 2005. The fibroblastic coconspirator in cancer progression. Cold Spring Harb. Symp. Quant. Biol. 70:383–88
    [Google Scholar]
  28. 28.
    Taddei ML, Cavallini L, Comito G, Giannoni E, Folini M et al. 2014. Senescent stroma promotes prostate cancer progression: the role of miR-210. Mol. Oncol. 8:1729–46
    [Google Scholar]
  29. 29.
    Vannella KM, Wynn TA. 2017. Mechanisms of organ injury and repair by macrophages. Annu. Rev. Physiol. 79:593–617
    [Google Scholar]
  30. 30.
    Julier Z, Park AJ, Briquez PS, Martino MM 2017. Promoting tissue regeneration by modulating the immune system. Acta Biomater 53:13–28
    [Google Scholar]
  31. 31.
    Ogle ME, Segar CE, Sridhar S, Botchwey EA 2016. Monocytes and macrophages in tissue repair: implications for immunoregenerative biomaterial design. Exp. Biol. Med. 241:1084–97
    [Google Scholar]
  32. 32.
    Smith TD, Nagalla RR, Chen EY, Liu WF 2017. Harnessing macrophage plasticity for tissue regeneration. Adv. Drug Deliv. Rev. 114:193–205
    [Google Scholar]
  33. 33.
    Zhou D, Yang K, Chen L, Zhang W, Xu Z et al. 2017. Promising landscape for regulating macrophage polarization: epigenetic viewpoint. Oncotarget 8:57683–706
    [Google Scholar]
  34. 34.
    Neele AE, Van den Bossche J, Hoeksema MA, de Winther MP 2015. Epigenetic pathways in macrophages emerge as novel targets in atherosclerosis. Eur. J. Pharmacol. 763:79–89
    [Google Scholar]
  35. 35.
    Vergadi E, Ieronymaki E, Lyroni K, Vaporidi K, Tsatsanis C 2017. Akt signaling pathway in macrophage activation and M1/M2 polarization. J. Immunol. 198:1006–14
    [Google Scholar]
  36. 36.
    Barrett JP, Minogue AM, Falvey A, Lynch MA 2015. Involvement of IGF-1 and Akt in M1/M2 activation state in bone marrow–derived macrophages. Exp. Cell Res. 335:258–68
    [Google Scholar]
  37. 37.
    Wang H, Lafdil F, Kong X, Gao B 2011. Signal transducer and activator of transcription 3 in liver diseases: a novel therapeutic target. Int. J. Biol. Sci. 7:536–50
    [Google Scholar]
  38. 38.
    Zhao J, Yu H, Liu Y, Gibson SA, Yan Z et al. 2016. Protective effect of suppressing STAT3 activity in LPS-induced acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 311:L868–80
    [Google Scholar]
  39. 39.
    Ye J, Guo R, Shi Y, Qi F, Guo C, Yang L 2016. miR-155 regulated inflammation response by the SOCS1-STAT3-PDCD4 axis in atherogenesis. Mediat. Inflamm. 2016:8060182
    [Google Scholar]
  40. 40.
    Sica A, Bronte V. 2007. Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Investig. 117:1155–66
    [Google Scholar]
  41. 41.
    Szade A, Grochot-Przeczek A, Florczyk U, Jozkowicz A, Dulak J 2015. Cellular and molecular mechanisms of inflammation-induced angiogenesis. IUBMB Life 67:145–59
    [Google Scholar]
  42. 42.
    Takeda N, O'Dea EL, Doedens A, Kim JW, Weidemann A et al. 2010. Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasis. Genes Dev 24:491–501
    [Google Scholar]
  43. 43.
    Davis MJ, Tsang TM, Qiu Y, Dayrit JK, Freij JB et al. 2013. Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection. mBio 4:e00264–13
    [Google Scholar]
  44. 44.
    Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P 2017. Tumour-associated macrophages as treatment targets in oncology. Nat. Rev. Clin. Oncol. 14:399–416
    [Google Scholar]
  45. 45.
    Essandoh K, Li Y, Huo J, Fan GC 2016. MiRNA-mediated macrophage polarization and its potential role in the regulation of inflammatory response. Shock 46:122–31
    [Google Scholar]
  46. 46.
    Lu X. 2017. The role of exosomes and exosome-derived microRNAs in atherosclerosis. Curr. Pharm. Des. 23:6182–93
    [Google Scholar]
  47. 47.
    Wallner S, Schroder C, Leitao E, Berulava T, Haak C et al. 2016. Epigenetic dynamics of monocyte-to-macrophage differentiation. Epigenetics Chromatin 9:33
    [Google Scholar]
  48. 48.
    Iskratsch T, Wolfenson H, Sheetz MP 2014. Appreciating force and shape—the rise of mechanotransduction in cell biology. Nat. Rev. Mol. Cell Biol. 15:825–33
    [Google Scholar]
  49. 49.
    Dingal PC, Discher DE. 2014. Systems mechanobiology: Tension-inhibited protein turnover is sufficient to physically control gene circuits. Biophys. J. 107:2734–43
    [Google Scholar]
  50. 50.
    Wang N, Tytell JD, Ingber DE 2009. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10:75–82
    [Google Scholar]
  51. 51.
    Uhler C, Shivashankar GV. 2017. Regulation of genome organization and gene expression by nuclear mechanotransduction. Nat. Rev. Mol. Cell Biol. 18:717–27
    [Google Scholar]
  52. 52.
    Szczesny SE, Mauck RL. 2017. The nuclear option: evidence implicating the cell nucleus in mechanotransduction. J. Biomech. Eng. 139:BIO–16-1276
    [Google Scholar]
  53. 53.
    Ladoux B, Mege RM. 2017. Mechanobiology of collective cell behaviours. Nat. Rev. Mol. Cell Biol. 18:743–57
    [Google Scholar]
  54. 54.
    Panciera T, Azzolin L, Cordenonsi M, Piccolo S 2017. Mechanobiology of YAP and TAZ in physiology and disease. Nat. Rev. Mol. Cell Biol. 18:758–70
    [Google Scholar]
  55. 55.
    Hu X, Margadant FM, Yao M, Sheetz MP 2017. Molecular stretching modulates mechanosensing pathways. Protein Sci 26:1337–51
    [Google Scholar]
  56. 56.
    Elosegui-Artola A, Trepat X, Roca-Cusachs P 2018. Control of mechanotransduction by molecular clutch dynamics. Trends Cell Biol 28:356–67
    [Google Scholar]
  57. 57.
    Vogel V. 2018. Unraveling the mechanobiology of extracellular matrix. Annu. Rev. Physiol. 80:353–87
    [Google Scholar]
  58. 58.
    Schoen I, Pruitt BL, Vogel V 2013. The yin-yang in rigidity sensing: how forces and mechanical properties regulate the cellular response to materials. Annu. Rev. Mater. Res. 43:589–618
    [Google Scholar]
  59. 59.
    Discher DE, Smith L, Cho S, Colasurdo M, Garcia AJ, Safran S 2017. Matrix mechanosensing: from scaling concepts in ’omics data to mechanisms in the nucleus, regeneration, and cancer. Annu. Rev. Biophys. 46:295–315
    [Google Scholar]
  60. 60.
    Ihalainen TO, Aires L, Herzog FA, Schwartlander R, Moeller J, Vogel V 2015. Differential basal-to-apical accessibility of lamin A/C epitopes in the nuclear lamina regulated by changes in cytoskeletal tension. Nat. Mater. 14:1252–61
    [Google Scholar]
  61. 61.
    Schoen I, Aires L, Ries J, Vogel V 2017. Nanoscale invaginations of the nuclear envelope: shedding new light on wormholes with elusive function. Nucleus 8:506–14
    [Google Scholar]
  62. 62.
    Jain N, Iyer KV, Kumar A, Shivashankar GV 2013. Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. PNAS 110:11349–54
    [Google Scholar]
  63. 63.
    Roy B, Venkatachalapathy S, Ratna P, Wang Y, Jokhun DS et al. 2018. Laterally confined growth of cells induces nuclear reprogramming in the absence of exogenous biochemical factors. PNAS 115:E4741–50
    [Google Scholar]
  64. 64.
    Xia Z, Triffitt JT. 2006. A review on macrophage responses to biomaterials. Biomed. Mater. 1:R1–9
    [Google Scholar]
  65. 65.
    Patel NR, Bole M, Chen C, Hardin CC, Kho AT et al. 2012. Cell elasticity determines macrophage function. PLOS ONE 7:e41024
    [Google Scholar]
  66. 66.
    Blakney AK, Swartzlander MD, Bryant SJ 2012. 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 100:1375–86
    [Google Scholar]
  67. 67.
    Sussman EM, Halpin MC, Muster J, Moon RT, Ratner BD 2014. Porous implants modulate healing and induce shifts in local macrophage polarization in the foreign body reaction. Ann. Biomed. Eng. 42:1508–16
    [Google Scholar]
  68. 68.
    Hind LE, Dembo M, Hammer DA 2015. Macrophage motility is driven by frontal-towing with a force magnitude dependent on substrate stiffness. Integr. Biol. 7:447–53
    [Google Scholar]
  69. 69.
    Sosale NG, Rouhiparkouhi T, Bradshaw AM, Dimova R, Lipowsky R, Discher DE 2015. Cell rigidity and shape override CD47's “self”-signaling in phagocytosis by hyperactivating myosin II. Blood 125:542–52
    [Google Scholar]
  70. 70.
    Adlerz KM, Aranda-Espinoza H, Hayenga HN 2016. Substrate elasticity regulates the behavior of human monocyte-derived macrophages. Eur. Biophys. J. 45:301–9
    [Google Scholar]
  71. 71.
    Chen S, Jones JA, Xu Y, Low HY, Anderson JM, Leong KW 2010. Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31:3479–91
    [Google Scholar]
  72. 72.
    Guilliams M, Scott CL. 2017. Does niche competition determine the origin of tissue-resident macrophages?. Nat. Rev. Immunol. 17:451–60
    [Google Scholar]
  73. 73.
    McWhorter FY, Davis CT, Liu WF 2015. Physical and mechanical regulation of macrophage phenotype and function. Cell Mol. Life Sci. 72:1303–16
    [Google Scholar]
  74. 74.
    Luu TU, Gott SC, Woo BW, Rao MP, Liu WF 2015. Micro- and nanopatterned topographical cues for regulating macrophage cell shape and phenotype. ACS Appl. Mater. Interfaces 7:28665–72
    [Google Scholar]
  75. 75.
    Ratner BD. 2016. A pore way to heal and regenerate: 21st century thinking on biocompatibility. Regen. Biomater. 3:107–10
    [Google Scholar]
  76. 76.
    Jain N, Vogel V. 2018. Spatial confinment downsizes the pro-inflammatory response of macrophages. Nat. Mater. 17:1134–44
    [Google Scholar]
  77. 77.
    Trappmann B, Gautrot JE, Connelly JT, Strange DG, Li Y et al. 2012. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11:642–49
    [Google Scholar]
  78. 78.
    Vining KH, Mooney DJ. 2017. Mechanical forces direct stem cell behaviour in development and regeneration. Nat. Rev. Mol. Cell Biol. 18:728–42
    [Google Scholar]
  79. 79.
    Chaudhuri O, Gu L, Klumpers D, Darnell M, Bencherif SA et al. 2016. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat. Mater. 15:326–34
    [Google Scholar]
  80. 80.
    Baker BM, Trappmann B, Wang WY, Sakar MS, Kim IL et al. 2015. Cell-mediated fibre recruitment drives extracellular matrix mechanosensing in engineered fibrillar microenvironments. Nat. Mater. 14:1262–68
    [Google Scholar]
  81. 81.
    Gong Z, Szczesny SE, Caliari SR, Charrier EE, Chaudhuri O et al. 2018. Matching material and cellular timescales maximizes cell spreading on viscoelastic substrates. PNAS 115:E2686–95
    [Google Scholar]
  82. 82.
    Baneyx G, Baugh L, Vogel V 2001. Coexisting conformations of fibronectin in cell culture imaged using fluorescence resonance energy transfer. PNAS 98:14464–68
    [Google Scholar]
  83. 83.
    Jansen LE, Amer LD, Chen EY, Nguyen TV, Saleh LS et al. 2018. Zwitterionic PEG-PC hydrogels modulate the foreign body response in a modulus-dependent manner. Biomacromolecules 19:2880–88
    [Google Scholar]
  84. 84.
    Liu Y, Kao WJ. 2002. Human macrophage adhesion on fibronectin: the role of substratum and intracellular signalling kinases. Cell Signal 14:145–52
    [Google Scholar]
  85. 85.
    Miyazaki H, Hayashi K. 2001. Effects of cyclic strain on the morphology and phagocytosis of macrophages. Biomed. Mater. Eng. 11:301–9
    [Google Scholar]
  86. 86.
    Schief WR, Antia M, Discher BM, Hall SB, Vogel V 2003. Liquid-crystalline collapse of pulmonary surfactant monolayers. Biophys. J. 84:3792–806
    [Google Scholar]
  87. 87.
    Akei H, Whitsett JA, Buroker M, Ninomiya T, Tatsumi H et al. 2006. Surface tension influences cell shape and phagocytosis in alveolar macrophages. Am. J. Physiol. Lung Cell Mol. Physiol. 291:L572–79
    [Google Scholar]
  88. 88.
    Cho MR, Thatte HS, Lee RC, Golan DE 2000. Integrin-dependent human macrophage migration induced by oscillatory electrical stimulation. Ann. Biomed. Eng. 28:234–43
    [Google Scholar]
  89. 89.
    Hoare JI, Rajnicek AM, McCaig CD, Barker RN, Wilson HM 2016. Electric fields are novel determinants of human macrophage functions. J. Leukoc. Biol. 99:1141–51
    [Google Scholar]
  90. 90.
    Ross CL, Harrison BS. 2013. Effect of time-varied magnetic field on inflammatory response in macrophage cell line RAW 264.7. Electromagn. Biol. Med. 32:59–69
    [Google Scholar]
  91. 91.
    Schuerle S, Avalos Vizcarra I, Moeller J, Sakar MS, Özkale B et al. 2017. Robotically controlled microprey to resolve initial attack modes preceding phagocytosis. Sci. Robot. 2:eaah6094
    [Google Scholar]
  92. 92.
    Wosik J, Chen W, Qin K, Ghobrial RM, Kubiak JZ, Kloc M 2018. Magnetic field changes macrophage phenotype. Biophys. J. 114:2001–13
    [Google Scholar]
  93. 93.
    Luster AD, Alon R, von Andrian UH 2005. Immune cell migration in inflammation: present and future therapeutic targets. Nat. Immunol. 6:1182–90
    [Google Scholar]
  94. 94.
    Bischof RJ, Zafiropoulos D, Hamilton JA, Campbell IK 2000. Exacerbation of acute inflammatory arthritis by the colony-stimulating factors CSF-1 and granulocyte macrophage (GM)-CSF: evidence of macrophage infiltration and local proliferation. Clin. Exp. Immunol. 119:361–67
    [Google Scholar]
  95. 95.
    Hynes RO. 2009. The extracellular matrix: not just pretty fibrils. Science 326:1216–19
    [Google Scholar]
  96. 96.
    Barros-Becker F, Lam PY, Fisher R, Huttenlocher A 2017. Live imaging reveals distinct modes of neutrophil and macrophage migration within interstitial tissues. J. Cell Sci. 130:3801–8
    [Google Scholar]
  97. 97.
    Murphy DA, Courtneidge SA. 2011. The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat. Rev. Mol. Cell Biol. 12:413–26
    [Google Scholar]
  98. 98.
    Zaidel-Bar R, Cohen M, Addadi L, Geiger B 2004. Hierarchical assembly of cell–matrix adhesion complexes. Biochem. Soc. Trans. 32:416–20
    [Google Scholar]
  99. 99.
    Collin O, Na S, Chowdhury F, Hong M, Shin ME et al. 2008. Self-organized podosomes are dynamic mechanosensors. Curr. Biol. 18:1288–94
    [Google Scholar]
  100. 100.
    Linder S, Wiesner C. 2016. Feel the force: podosomes in mechanosensing. Exp. Cell Res. 343:67–72
    [Google Scholar]
  101. 101.
    Block MR, Badowski C, Millon-Fremillon A, Bouvard D, Bouin AP et al. 2008. Podosome-type adhesions and focal adhesions, so alike yet so different. Eur. J. Cell Biol. 87:491–506
    [Google Scholar]
  102. 102.
    Cougoule C, Van Goethem E, Le Cabec V, Lafouresse F, Dupré L et al. 2012. Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and to migrate in 3D environments. Eur. J. Cell Biol. 91:938–49
    [Google Scholar]
  103. 103.
    Khandani A, Eng E, Jongstra-Bilen J, Schreiber AD, Douda D et al. 2007. Microtubules regulate PI-3K activity and recruitment to the phagocytic cup during Fcγ receptor–mediated phagocytosis in nonelicited macrophages. J. Leukoc. Biol. 82:417–28
    [Google Scholar]
  104. 104.
    Ghrebi S, Hamilton DW, Douglas Waterfield J, Brunette DM 2013. The effect of surface topography on cell shape and early ERK1/2 signaling in macrophages; linkage with FAK and Src. J. Biomed. Mater. Res. A 101:2118–28
    [Google Scholar]
  105. 105.
    Labernadie A, Bouissou A, Delobelle P, Balor S, Voituriez R et al. 2014. Protrusion force microscopy reveals oscillatory force generation and mechanosensing activity of human macrophage podosomes. Nat. Commun. 5:5343
    [Google Scholar]
  106. 106.
    Van Goethem E, Guiet R, Balor S, Charriere GM, Poincloux R et al. 2011. Macrophage podosomes go 3D. Eur. J. Cell Biol. 90:224–36
    [Google Scholar]
  107. 107.
    Akisaka T, Yoshida H, Suzuki R, Takama K 2008. Adhesion structures and their cytoskeleton-membrane interactions at podosomes of osteoclasts in culture. Cell Tissue Res 331:625–41
    [Google Scholar]
  108. 108.
    Luxenburg C, Geblinger D, Klein E, Anderson K, Hanein D et al. 2007. The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLOS ONE 2:e179
    [Google Scholar]
  109. 109.
    Mersich AT, Miller MR, Chkourko H, Blystone SD 2010. The formin FRL1 (FMNL1) is an essential component of macrophage podosomes. Cytoskeleton 67:573–85
    [Google Scholar]
  110. 110.
    Panzer L, Trube L, Klose M, Joosten B, Slotman J et al. 2016. The formins FHOD1 and INF2 regulate inter- and intra-structural contractility of podosomes. J. Cell Sci. 129:298–313
    [Google Scholar]
  111. 111.
    Bhuwania R, Cornfine S, Fang Z, Kruger M, Luna EJ, Linder S 2012. Supervillin couples myosin-dependent contractility to podosomes and enables their turnover. J. Cell Sci. 125:2300–14
    [Google Scholar]
  112. 112.
    Van Audenhove I, Debeuf N, Boucherie C, Gettemans J 2015. Fascin actin bundling controls podosome turnover and disassembly while cortactin is involved in podosome assembly by its SH3 domain in THP-1 macrophages and dendritic cells. Biochim. Biophys. Acta 1853:940–52
    [Google Scholar]
  113. 113.
    Dovas A, Gevrey JC, Grossi A, Park H, Abou-Kheir W, Cox D 2009. Regulation of podosome dynamics by WASp phosphorylation: implication in matrix degradation and chemotaxis in macrophages. J. Cell Sci. 122:3873–82
    [Google Scholar]
  114. 114.
    Champion JA, Mitragotri S. 2009. Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res. 26:244–49
    [Google Scholar]
  115. 115.
    Sheng Y, Liu C, Yuan Y, Tao X, Yang F et al. 2009. Long-circulating polymeric nanoparticles bearing a combinatorial coating of PEG and water-soluble chitosan. Biomaterials 30:2340–48
    [Google Scholar]
  116. 116.
    Akilbekova D, Philiph R, Graham A, Bratlie KM 2015. Macrophage reprogramming: influence of latex beads with various functional groups on macrophage phenotype and phagocytic uptake in vitro. J. Biomed. Mater. Res. A 103:262–68
    [Google Scholar]
  117. 117.
    Chen X, Yan Y, Mullner M, Ping Y, Cui J et al. 2016. Shape-dependent activation of cytokine secretion by polymer capsules in human monocyte-derived macrophages. Biomacromolecules 17:1205–12
    [Google Scholar]
  118. 118.
    Moeller J, Lühmann T, Chabria M, Hall H, Vogel V 2013. Macrophages lift off surface-bound bacteria using a filopodium–lamellipodium hook-and-shovel mechanism. Sci. Rep. 3:2884
    [Google Scholar]
  119. 119.
    Jones GE. 2000. Cellular signaling in macrophage migration and chemotaxis. J. Leukoc. Biol. 68:593–602
    [Google Scholar]
  120. 120.
    Constantin G, Laudanna C. 2010. Leukocyte chemotaxis: from lysosomes to motility. Nat. Immunol. 11:463–64
    [Google Scholar]
  121. 121.
    Swaney KF, Huang C-H, Devreotes PN 2010. Eukaryotic chemotaxis: a network of signaling pathways controls motility, directional sensing, and polarity. Annu. Rev. Biophys. 39:265–89
    [Google Scholar]
  122. 122.
    Zhang B, Ma Y, Guo H, Sun B, Niu R et al. 2009. Akt2 is required for macrophage chemotaxis. Eur. J. Immunol. 39:894–901
    [Google Scholar]
  123. 123.
    Xuan W, Qu Q, Zheng B, Xiong S, Fan GH 2015. The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J. Leukoc. Biol. 97:61–69
    [Google Scholar]
  124. 124.
    Stachelek SJ, Finley MJ, Alferiev IS, Wang F, Tsai RK et al. 2011. The effect of CD47 modified polymer surfaces on inflammatory cell attachment and activation. Biomaterials 32:4317–26
    [Google Scholar]
  125. 125.
    Sosale NG, Spinler KR, Alvey C, Discher DE 2015. Macrophage engulfment of a cell or nanoparticle is regulated by unavoidable opsonization, a species-specific ‘marker of self’ CD47, and target physical properties. Curr. Opin. Immunol. 35:107–12
    [Google Scholar]
  126. 126.
    Kress H, Stelzer EH, Holzer D, Buss F, Griffiths G, Rohrbach A 2007. Filopodia act as phagocytic tentacles and pull with discrete steps and a load-dependent velocity. PNAS 104:11633–38
    [Google Scholar]
  127. 127.
    Vonna L, Wiedemann A, Aepfelbacher M, Sackmann E 2007. Micromechanics of filopodia mediated capture of pathogens by macrophages. Eur. Biophys. J. 36:145–51
    [Google Scholar]
  128. 128.
    Thomas WE, Trintchina E, Forero M, Vogel V, Sokurenko EV 2002. Bacterial adhesion to target cells enhanced by shear force. Cell 109:913–23
    [Google Scholar]
  129. 129.
    Forero M, Yakovenko O, Sokurenko EV, Thomas WE, Vogel V 2006. Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds. PLOS Biol 4:e298
    [Google Scholar]
  130. 130.
    Mizushima N, Levine B, Cuervo AM, Klionsky DJ 2008. Autophagy fights disease through cellular self-digestion. Nature 451:1069–75
    [Google Scholar]
  131. 131.
    Doshi N, Mitragotri S. 2010. Macrophages recognize size and shape of their targets. PLOS ONE 5:e10051
    [Google Scholar]
  132. 132.
    Beningo KA, Wang Y-L. 2002. Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J. Cell Sci. 115:849–56
    [Google Scholar]
  133. 133.
    Anselmo AC, Zhang M, Kumar S, Vogus DR, Menegatti S et al. 2015. Elasticity of nanoparticles influences their blood circulation, phagocytosis, endocytosis and targeting. ACS Nano 9:3169–77
    [Google Scholar]
  134. 134.
    Garapaty A, Champion JA. 2017. Tunable particles alter macrophage uptake based on combinatorial effects of physical properties. Bioeng. Transl. Med. 2:92–101
    [Google Scholar]
  135. 135.
    Palomba R, Palange AL, Rizzuti IF, Ferreira M, Cervadoro A et al. 2018. Modulating phagocytic cell sequestration by tailoring nanoconstruct softness. ACS Nano 12:1433–44
    [Google Scholar]
  136. 136.
    Champion JA, Mitragotri S. 2006. Role of target geometry in phagocytosis. PNAS 103:4930–34
    [Google Scholar]
  137. 137.
    Moeller J, Lühmann T, Hall H, Vogel V 2012. The race to the pole: how high-aspect ratio shape and heterogeneous environments limit phagocytosis of filamentous Escherichia coli bacteria by macrophages. Nano Lett 12:2901–5
    [Google Scholar]
  138. 138.
    Swanson JA, Johnson MT, Beningo K, Post P, Mooseker M, Araki N 1999. A contractile activity that closes phagosomes in macrophages. J. Cell Sci. 112:307–16
    [Google Scholar]
  139. 139.
    Porta C, Rimoldi M, Raes G, Brys L, Ghezzi P et al. 2009. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor κB. PNAS 106:14978–83
    [Google Scholar]
  140. 140.
    Mao Y, Finnemann SC. 2015. Regulation of phagocytosis by Rho GTPases. Small GTPases 6:89–99
    [Google Scholar]
  141. 141.
    Irmscher M, de Jong AM, Kress H, Prins MW 2013. A method for time-resolved measurements of the mechanics of phagocytic cups. J. R. Soc. Interface 10:20121048
    [Google Scholar]
  142. 142.
    Brandt DT, Marion S, Griffiths G, Watanabe T, Kaibuchi K, Grosse R 2007. Dia1 and IQGAP1 interact in cell migration and phagocytic cup formation. J. Cell Biol. 178:193–200
    [Google Scholar]
  143. 143.
    Merkel TJ, Jones SW, Herlihy KP, Kersey FR, Shields AR et al. 2011. Using mechanobiological mimicry of red blood cells to extend circulation times of hydrogel microparticles. PNAS 108:586–91
    [Google Scholar]
  144. 144.
    Albright JM, Dunn RC, Shults JA, Boe DM, Afshar M, Kovacs EJ 2016. Advanced age alters monocyte and macrophage responses. Antioxid Redox Signal 25:805–15
    [Google Scholar]
  145. 145.
    Justice SS, Hunstad DA, Cegelski L, Hultgren SJ 2008. Morphological plasticity as a bacterial survival strategy. Nat. Rev. Microbiol. 6:162–68
    [Google Scholar]
  146. 146.
    Justice SS, Hunstad DA, Seed PC, Hultgren SJ 2006. Filamentation by Escherichia coli subverts innate defenses during urinary tract infection. PNAS 103:19884–89
    [Google Scholar]
  147. 147.
    Bos J, Zhang Q, Vyawahare S, Rogers E, Rosenberg SM, Austin RH 2015. Emergence of antibiotic resistance from multinucleated bacterial filaments. PNAS 112:178–83
    [Google Scholar]
  148. 148.
    Prashar A, Bhatia S, Gigliozzi D, Martin T, Duncan C et al. 2013. Filamentous morphology of bacteria delays the timing of phagosome morphogenesis in macrophages. J. Cell Biol. 203:1081–97
    [Google Scholar]
  149. 149.
    Upadhyay S, Mittal E, Philips JA 2018. Tuberculosis and the art of macrophage manipulation. Pathog. Dis. 76:fty037
    [Google Scholar]
  150. 150.
    Avalos Vizcarra I, Hosseini V, Kollmannsberger P, Meier S, Weber SS et al. 2016. How type 1 fimbriae help Escherichia coli to evade extracellular antibiotics. Sci. Rep. 6:18109
    [Google Scholar]
  151. 151.
    McWhorter FY, Wang T, Nguyen P, Chung T, Liu WF 2013. Modulation of macrophage phenotype by cell shape. PNAS 110:17253–58
    [Google Scholar]
  152. 152.
    Das Gupta K, Shakespear MR, Iyer A, Fairlie DP, Sweet MJ 2016. Histone deacetylases in monocyte/macrophage development, activation and metabolism: refining HDAC targets for inflammatory and infectious diseases. Clin. Transl. Immunol. 5:e62
    [Google Scholar]
  153. 153.
    Kapellos TS, Iqbal AJ. 2016. Epigenetic control of macrophage polarisation and soluble mediator gene expression during inflammation. Mediat. Inflamm. 2016:6591703
    [Google Scholar]
  154. 154.
    Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M et al. 2011. Histone deacetylase inhibitors impair innate immune responses to Toll-like receptor agonists and to infection. Blood 117:1205–17
    [Google Scholar]
  155. 155.
    Raza S, Barnett MW, Barnett-Itzhaki Z, Amit I, Hume DA, Freeman TC 2014. Analysis of the transcriptional networks underpinning the activation of murine macrophages by inflammatory mediators. J. Leukoc. Biol. 96:167–83
    [Google Scholar]
  156. 156.
    Medzhitov R, Horng T. 2009. Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9:692–703
    [Google Scholar]
  157. 157.
    Shinji H, Akagawa KS, Yoshida T 1993. Cytochalasin D inhibits lipopolysaccharide-induced tumor necrosis factor production in macrophages. J. Leukoc. Biol. 54:336–42
    [Google Scholar]
  158. 158.
    Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E, Treisman R 2009. Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 11:257–68
    [Google Scholar]
  159. 159.
    Janmey PA, Wells RG, Assoian RK, McCulloch CA 2013. From tissue mechanics to transcription factors. Differentiation 86:112–20
    [Google Scholar]
  160. 160.
    Ravasi T, Wells CA, Hume DA 2007. Systems biology of transcription control in macrophages. BioEssays 29:1215–26
    [Google Scholar]
  161. 161.
    Kim MY, Kim JH, Cho JY 2014. Cytochalasin B modulates macrophage-mediated inflammatory responses. Biomol. Ther. 22:295–300
    [Google Scholar]
  162. 162.
    Eswarappa SM, Pareek V, Chakravortty D 2008. Role of actin cytoskeleton in LPS-induced NF-κB activation and nitric oxide production in murine macrophages. Innate Immun 14:309–18
    [Google Scholar]
  163. 163.
    Azevedo E, Oliveira LT, Castro Lima AK, Terra R, Dutra PM, Salerno VP 2012. Interactions between Leishmania braziliensis and macrophages are dependent on the cytoskeleton and myosin VA. J. Parasitol. Res. 2012:275436
    [Google Scholar]
  164. 164.
    Nogales E. 2000. Structural insights into microtubule function. Annu. Rev. Biochem. 69:277–302
    [Google Scholar]
  165. 165.
    Allen LA, Aderem A. 1996. Mechanisms of phagocytosis. Curr. Opin. Immunol. 8:36–40
    [Google Scholar]
  166. 166.
    Binker MG, Zhao DY, Pang SJ, Harrison RE 2007. Cytoplasmic linker protein 170 enhances spreading and phagocytosis in activated macrophages by stabilizing microtubules. J. Immunol. 179:3780–91
    [Google Scholar]
  167. 167.
    Kirikae T, Kirikae F, Oghiso Y, Nakano M 1996. Microtubule-disrupting agents inhibit nitric oxide production in murine peritoneal macrophages stimulated with lipopolysaccharide or paclitaxel (Taxol). Infect. Immun. 64:3379–84
    [Google Scholar]
  168. 168.
    Hanania R, Sun HS, Xu K, Pustylnik S, Jeganathan S, Harrison RE 2012. Classically activated macrophages use stable microtubules for matrix metalloproteinase 9 (MMP-9) secretion. J. Biol. Chem. 287:8468–83
    [Google Scholar]
  169. 169.
    Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677–86
    [Google Scholar]
  170. 170.
    Roszer T. 2015. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediat. Inflamm. 2015:816460
    [Google Scholar]
  171. 171.
    Martinez FO, Helming L, Gordon S 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27:451–83
    [Google Scholar]
  172. 172.
    Okamoto T, Takagi Y, Kawamoto E, Park EJ, Usuda H et al. 2018. Reduced substrate stiffness promotes M2-like macrophage activation and enhances peroxisome proliferator–activated receptor γ expression. Exp. Cell Res. 367:264–73
    [Google Scholar]
  173. 173.
    Chinetti-Gbaguidi G, Baron M, Bouhlel MA, Vanhoutte J, Copin C et al. 2011. Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARγ and LXRα pathways. Circ. Res. 108:985–95
    [Google Scholar]
  174. 174.
    Stoger JL, Gijbels MJ, van der Velden S, Manca M, van der Loos CM et al. 2012. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 225:461–68
    [Google Scholar]
  175. 175.
    Wang J, Meng F, Song W, Jin J, Ma Q et al. 2018. Nanostructured titanium regulates osseointegration via influencing macrophage polarization in the osteogenic environment. Int. J. Nanomed. 13:4029–43
    [Google Scholar]
  176. 176.
    Almeida CR, Serra T, Oliveira MI, Planell JA, Barbosa MA, Navarro M 2014. Impact of 3-D printed PLA- and chitosan-based scaffolds on human monocyte/macrophage responses: unraveling the effect of 3-D structures on inflammation. Acta Biomater 10:613–22
    [Google Scholar]
  177. 177.
    Malheiro V, Lehner F, Dinca V, Hoffmann P, Maniura-Weber K 2016. Convex and concave micro-structured silicone controls the shape, but not the polarization state of human macrophages. Biomater. Sci. 4:1562–73
    [Google Scholar]
  178. 178.
    Li R, Serrano JC, Xing H, Lee TA, Azizgolshani H et al. 2018. Interstitial flow promotes macrophage polarization toward an M2 phenotype. Mol. Biol. Cell 29:1927–40
    [Google Scholar]
  179. 179.
    Barth KA, Waterfield JD, Brunette DM 2013. The effect of surface roughness on RAW 264.7 macrophage phenotype. J. Biomed. Mater. Res. A 101:2679–88
    [Google Scholar]
  180. 180.
    Kao CT, Huang TH, Fang HY, Chen YW, Chien CF et al. 2016. Tensile force on human macrophage cells promotes osteoclastogenesis through receptor activator of nuclear factor κB ligand induction. J. Bone Miner. Metab. 34:406–16
    [Google Scholar]
  181. 181.
    Dou C, Cao Z, Yang B, Ding N, Hou T et al. 2016. Changing expression profiles of lncRNAs, mRNAs, circRNAs and miRNAs during osteoclastogenesis. Sci. Rep. 6:21499
    [Google Scholar]
  182. 182.
    Guo LJ, Liao L, Yang L, Li Y, Jiang TJ 2014. MiR-125a TNF receptor–associated factor 6 to inhibit osteoclastogenesis. Exp. Cell Res. 321:142–52
    [Google Scholar]
  183. 183.
    Redlich K, Smolen JS. 2012. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nat. Rev. Drug Discov. 11:234–50
    [Google Scholar]
  184. 184.
    Lampiasi N, Russo R, Zito F 2016. The alternative faces of macrophage generate osteoclasts. Biomed. Res. Int. 2016:9089610
    [Google Scholar]
  185. 185.
    Abdelmagid SM, Barbe MF, Safadi FF 2015. Role of inflammation in the aging bones. Life Sci 123:25–34
    [Google Scholar]
  186. 186.
    Zhao H, Zhang J, Shao H, Liu J, Jin M et al. 2017. miRNA-340 inhibits osteoclast differentiation via repression of MITF. Biosci. Rep. 37:BSR20170203
    [Google Scholar]
  187. 187.
    He D, Kou X, Yang R, Liu D, Wang X et al. 2015. M1-like macrophage polarization promotes orthodontic tooth movement. J. Dent. Res. 94:1286–94
    [Google Scholar]
  188. 188.
    Kanzaki H, Shinohara F, Itohiya-Kasuya K, Ishikawa M, Nakamura Y 2015. Nrf2 activation attenuates both orthodontic tooth movement and relapse. J. Dent. Res. 94:787–94
    [Google Scholar]
  189. 189.
    Hayakawa T, Yoshimura Y, Kikuiri T, Matsuno M, Hasegawa T et al. 2015. Optimal compressive force accelerates osteoclastogenesis in RAW 264.7 cells. Mol. Med. Rep. 12:5879–85
    [Google Scholar]
  190. 190.
    Jin Z, Wei W, Dechow PC, Wan Y 2013. HDAC7 inhibits osteoclastogenesis by reversing RANKL-triggered β-catenin switch. Mol. Endocrinol. 27:325–35
    [Google Scholar]
  191. 191.
    Onuora S. 2015. Bone: targeting epigenetic regulation of osteoclastogenesis to prevent bone loss. Nat. Rev. Rheumatol. 11:195
    [Google Scholar]
  192. 192.
    Lee D, Heo DN, Kim HJ, Ko WK, Lee SJ et al. 2016. Inhibition of osteoclast differentiation and bone resorption by bisphosphonate-conjugated gold nanoparticles. Sci. Rep. 6:27336
    [Google Scholar]
  193. 193.
    Dou C, Li N, Ding N, Liu C, Yang X et al. 2016. HDAC2 regulates FoxO1 during RANKL-induced osteoclastogenesis. Am. J. Physiol. Cell Physiol. 310:C780–87
    [Google Scholar]
  194. 194.
    Varol C, Mildner A, Jung S 2015. Macrophages: development and tissue specialization. Annu. Rev. Immunol. 33:643–75
    [Google Scholar]
  195. 195.
    T'Jonck W, Guilliams M, Bonnardel J 2018. Niche signals and transcription factors involved in tissue-resident macrophage development. Cell Immunol 330:43–53
    [Google Scholar]
  196. 196.
    Carver W, Goldsmith EC. 2013. Regulation of tissue fibrosis by the biomechanical environment. Biomed. Res. Int. 2013:101979
    [Google Scholar]
  197. 197.
    O'Connor JW, Gomez EW. 2014. Biomechanics of TGFβ-induced epithelial–mesenchymal transition: implications for fibrosis and cancer. Clin. Transl. Med. 3:23
    [Google Scholar]
  198. 198.
    Przybyla L, Muncie JM, Weaver VM 2016. Mechanical control of epithelial-to-mesenchymal transitions in development and cancer. Annu. Rev. Cell Dev. Biol. 32:527–54
    [Google Scholar]
  199. 199.
    Lee HS, Stachelek SJ, Tomczyk N, Finley MJ, Composto RJ, Eckmann DM 2013. Correlating macrophage morphology and cytokine production resulting from biomaterial contact. J. Biomed. Mater. Res. A 101:203–12
    [Google Scholar]
  200. 200.
    Gruber E, Heyward C, Cameron J, Leifer C 2018. Toll-like receptor signaling in macrophages is regulated by extracellular substrate stiffness and Rho-associated coiled-coil kinase (ROCK1/2). Int. Immunol. 30:267–78
    [Google Scholar]
  201. 201.
    Burkhardt MA, Waser J, Milleret V, Gerber I, Emmert MY et al. 2016. Synergistic interactions of blood-borne immune cells, fibroblasts and extracellular matrix drive repair in an in vitro peri-implant wound healing model. Sci. Rep. 6:21071
    [Google Scholar]
  202. 202.
    Burkhardt MA, Gerber I, Moshfegh C, Lucas MS, Waser J et al. 2017. Clot-entrapped blood cells in synergy with human mesenchymal stem cells create a pro-angiogenic healing response. Biomater. Sci. 5:2009–23
    [Google Scholar]
  203. 203.
    Han CZ, Juncadella IJ, Kinchen JM, Buckley MW, Klibanov AL et al. 2016. Macrophages redirect phagocytosis by non-professional phagocytes and influence inflammation. Nature 539:570–74
    [Google Scholar]
  204. 204.
    Godwin JW, Pinto AR, Rosenthal NA 2017. Chasing the recipe for a pro-regenerative immune system. Semin. Cell Dev. Biol. 61:71–79
    [Google Scholar]
  205. 205.
    Gerri C, Marin-Juez R, Marass M, Marks A, Maischein HM, Stainier DYR 2017. Hif-1α regulates macrophage–endothelial interactions during blood vessel development in zebrafish. Nat. Commun. 8:15492
    [Google Scholar]
/content/journals/10.1146/annurev-bioeng-062117-121224
Loading
/content/journals/10.1146/annurev-bioeng-062117-121224
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error