Physical and mechanical regulation of macrophage phenotype and function

Cellular and Molecular Life Sciences

Volumn 72, Issue 7, 2015, Pages 1303-1316

  McWhorter, Frances Y ^a,b   Davis, Chase T ^a,b   Liu, Wendy F ^a,b  

^a University of California at Irvine   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Macrophages; Mechanotransduction; Microenvironment; Phenotype; Polarization

Indexed keywords

BETA1 INTEGRIN; CD11B ANTIGEN; CD18 ANTIGEN; COLONY STIMULATING FACTOR 1; FOCAL ADHESION KINASE; GAMMA INTERFERON; HERMES ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; PROTEIN CDC42; RAC1 PROTEIN; RAC2 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SCAVENGER RECEPTOR A;

CELL ADHESION; CELL SHAPE; CELL SPREADING; HOMEOSTASIS; HUMAN; INFLAMMATION; MACROPHAGE; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MACROPHAGE MIGRATION; MECHANOTRANSDUCTION; NONHUMAN; POLARIZATION; REVIEW; RIGIDITY; TENSION; TISSUE HOMEOSTASIS; YOUNG MODULUS; ATHEROSCLEROSIS; BIOLOGICAL MODEL; CYTOLOGY; MECHANICAL STRESS; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY; STIMULATION; TUMOR MICROENVIRONMENT;

ATHEROSCLEROSIS; CELL SHAPE; CELLULAR MICROENVIRONMENT; HUMANS; MACROPHAGES; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; NEOPLASMS; PHYSICAL STIMULATION; STRESS, MECHANICAL;

EID: 84930921838     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1796-8     Document Type: Review

References (103)

1. Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496:445-455
2. Sieweke MH, Allen JE (2013) Beyond stem cells: self-renewal of differentiated macrophages. Science 342:1242974
3. Guilliams M et al (2014) Dendritic cells, monocytes and macrophages: a unified nomenclature based on ontogeny. Nat Rev Immunol 14:1-8. doi: 10.1038/nri3712
4. Murray PJ et al (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41:14-20
5. Mosser DM, Edwards JP (2008) Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8:958-969
6. Gautier EL et al (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13:1118-1128
7. Mantovani A et al (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25:677-686
8. Jetten N et al (2014) Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 17:109-118
9. Lumeng CN, DelProposto JB, Westcott DJ, Saltiel AR (2008) Phenotypic switching of adipose tissue macrophages with obesity is generated by spatiotemporal differences in macrophage subtypes. Diabetes 57:3239-3246
10. Biswas SK, Mantovani A (2010) Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11:889-896
11. Fujiu K, Wang J, Nagai R (2014) Cardioprotective function of cardiac macrophages. Cardiovasc Res 102:232-239
12. Van Amerongen MJ, Harmsen MC, van Rooijen N, Petersen AH, van Luyn MJA (2007) Macrophage depletion impairs wound healing and increases left ventricular remodeling after myocardial injury in mice. Am J Pathol 170:818-829
13. Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Cancer Res 66:605-612
14. Cornelissen R et al (2014) Ratio of intratumoral macrophage phenotypes is a prognostic factor in epithelioid malignant pleural mesothelioma. PLoS One 9:e106742
15. Novak ML, Koh TJ (2013) Phenotypic transitions of macrophages orchestrate tissue repair. Am J Pathol 183:1352-1363
16. Sica A et al (2008) Macrophage polarization in tumour progression. Semin Cancer Biol 18:349-355
17. Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF (2009) Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials 30:1482-1491
18. Brown BN et al (2012) Macrophage phenotype as a predictor of constructive remodeling following the implantation of biologically derived surgical mesh materials. Acta Biomater 8:978-987
19. Rich A, Harris AK (1981) Anomalous preferences of cultured macrophages for hydrophobic and roughened substrata. J Cell Sci 50:1-7
20. Refai AK, Textor M, Brunette DM, Waterfield JD (2004) Effect of titanium surface topography on macrophage activation and secretion of proinflammatory cytokines and chemokines. J Biomed Mater Res Part A 70:194-205
21. Tan KS, Qian L, Rosado R, Flood PM, Cooper LF (2006) The role of titanium surface topography on J774A.1 macrophage inflammatory cytokines and nitric oxide production. Biomaterials 27:5170-5177
22. Lee S et al (2011) Analysis on migration and activation of live macrophages on transparent flat and nanostructured titanium. Acta Biomater 7:2337-2344
23. Wójciakâ-Stothard B, Madeja Z, Korohoda W, Curtis A, Wilkinson C (1995) Activation of macrophage-like cells by multiple grooved substrata. Topographical control of cell behaviour. Cell Biol Int 19:485
24. Wójciak-Stothard B, Curtis A, Monaghan W, MacDonald K, Wilkinson C (1996) Guidance and activation of murine macrophages by nanometric scale topography. Exp Cell Res 223:426-435
25. Chen S et al (2010) Characterization of topographical effects on macrophage behavior in a foreign body response model. Biomaterials 31:3479-3491
26. Saino E et al (2011) Effect of electrospun fiber diameter and alignment on macrophage activation and secretion of proinflammatory cytokines and chemokines. Biomacromolecules 12:1900-1911
27. Garg K, Pullen NA, Oskeritzian CA, Ryan JJ, Bowlin GL (2013) Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds. Biomaterials 34:4439-4451
28. Cao H, McHugh K, Chew SY, Anderson JM (2010) The topographical effect of electrospun nanofibrous scaffolds on the in vivo and in vitro foreign body reaction. J Biomed Mater Res A 93:1151-1159
29. Sanders JE, Bale SD, Neumann T (2002) Tissue response to microfibers of different polymers: polyester, polyethylene, polylactic acid, and polyurethane. J Biomed Mater Res 62:222-227
30. Baker BM, Chen CS (2012) Deconstructing the third dimension - how 3D culture microenvironments alter cellular cues. J Cell Sci 125:3015-3024
31. Bartneck M et al (2012) Inducing healing-like human primary macrophage phenotypes by 3D hydrogel coated nanofibres. Biomaterials 33:4136-4146
32. Brown E et al (2003) Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 9:796-800
33. Guiet R et al (2011) The process of macrophage migration promotes matrix metalloproteinase-independent invasion by tumor cells. J Immunol 187:3806-3814
34. Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le Cabec V (2010) Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol 184:1049-1061
35. Liu M, Post M (2000) Invited review: mechanochemical signal transduction in the fetal lung. J Appl Physiol 89:2078-2084
36. Klein-Nulend J, Bacabac RG, Mullender MG (2005) Mechanobiology of bone tissue. Pathol Biol (Paris) 53:576-580
37. Kurata K et al (2001) Mechanical strain effect on bone-resorbing activity and messenger RNA expressions of marker enzymes in isolated osteoclast culture. J Bone Miner Res 16:722-730
38. Pugin J et al (1998) Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol 275:L1040-L1050
39. Wehner S et al (2010) 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:G1187-G1197
40. Yang JH, Sakamoto H, Xu EC, Lee RT (2000) Biomechanical regulation of human monocyte/macrophage molecular function. Am J Pathol 156:1797-1804
41. Ballotta V, Driessen-Mol A, Bouten CVC, Baaijens FPT (2014) Strain-dependent modulation of macrophage polarization within scaffolds. Biomaterials 35:4919-4928
42. Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144-152
43. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677-689
44. Paszek MJ et al (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241-254
45. Huynh J et al (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 3:112ra122
46. 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 100:1375-1386
47. Nemir S, Hayenga HN, West JL (2010) PEGDA hydrogels with patterned elasticity: novel tools for the study of cell response to substrate rigidity. Biotechnol Bioeng 105:636-644
48. Irwin EF et al (2008) Modulus-dependent macrophage adhesion and behavior. J Biomater Sci Polym Ed 19:1363-1382
49. Patel NR et al (2012) Cell elasticity determines macrophage function. PLoS One 7:e41024
50. Folkman J, Moscona A (1978) Role of cell shape in growth control. Nature 273:345-349
51. Matheson LA, Fairbank NJ, Maksym GN (2006) Characterization of the Flexcell Uniflex cyclic strain culture system with U937 macrophage-like cells. Biomaterials 27:226-233
52. Féréol S et al (2006) Sensitivity of alveolar macrophages to substrate mechanical and adhesive properties. Cell Motil Cytoskeleton 63:321-340
53. McWhorter FY, Wang T, Nguyen P, Chung T, Liu WF (2013) Modulation of macrophage phenotype by cell shape. Proc Natl Acad Sci USA 110:17253-17258
54. Wheeler AP et al (2006) Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J Cell Sci 119:2749-2757
55. Hanisch U-K, Kettenmann H (2007) Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci 10:1387-1394
56. Neubrand VE et al (2014) Mesenchymal stem cells induce the ramification of microglia via the small RhoGTPases Cdc42 and Rac1. Glia 62(12):1932-1942. doi: 10.1002/glia.22714
57. Chen CS (1997) Geometric control of cell life and death. Science 276:1425-1428
58. Yang Y, Relan NK, Przywara DA, Schuger L (1999) Embryonic mesenchymal cells share the potential for smooth muscle differentiation: myogenesis is controlled by the cell's shape. Dev Cambridge Engl 126:3027-3033
59. Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 107:4872-4877
60. Li F, Li B, Wang Q-M, Wang JH-C (2008) Cell shape regulates collagen type I expression in human tendon fibroblasts. Cell Motil Cytoskeleton 65:332-341
61. Thakar RG et al (2009) Cell-shape regulation of smooth muscle cell proliferation. Biophys J 96:3423-3432
62. Alford PW, Nesmith AP, Seywerd JN, Grosberg A, Parker KK (2011) Vascular smooth muscle contractility depends on cell shape. Integr Biol (Camb) 3:1063-1070
63. Lee H-S et al (2013) Correlating macrophage morphology and cytokine production resulting from biomaterial contact. J Biomed Mater Res A 101:203-212
64. Vereyken EJF et al (2011) Classically and alternatively activated bone marrow derived macrophages differ in cytoskeletal functions and migration towards specific CNS cell types. J Neuroinflammation 8:58
65. Block MR et al (2008) Podosome-type adhesions and focal adhesions, so alike yet so different. Eur J Cell Biol 87:491-506
66. Leporatti S et al (2006) Elasticity and adhesion of resting and lipopolysaccharide-stimulated macrophages. FEBS Lett 580:450-454
67. Pi J (2014) Detection of lipopolysaccharide induced inflammatory responses in RAW264.7 macrophages using atomic force microscope. Micron 65:1-9. doi: 10.1016/j.micron.2014.03.012
68. Féréol S et al (2008) Mechanical and structural assessment of cortical and deep cytoskeleton reveals substrate-dependent alveolar macrophage remodeling. Biomed Mater Eng 18:S105-S118
69. Tee SY, Fu J, Chen CS, Janmey PA (2011) Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100
70. Friedl P, Weigelin B (2008) Interstitial leukocyte migration and immune function. Nat Immunol 9:960-969
71. Gowen BB, Borg TK (2000) Ghaffar, a & Mayer, E. P. Selective adhesion of macrophages to denatured forms of type I collagen is mediated by scavenger receptors. Matrix Biol 19:61-71
72. El Khoury J et al (1994) Macrophages adhere to glucose-modified basement membrane collagen IV via their scavenger receptors. J Biol Chem 269:10197-10200
73. Santiago-García J, Kodama T, Pitas RE (2003) The class A scavenger receptor binds to proteoglycans and mediates adhesion of macrophages to the extracellular matrix. J Biol Chem 278:6942-6946
74. Kirkham PA, Spooner G, Ffoulkes-Jones C, Calvez R (2003) Cigarette smoke triggers macrophage adhesion and activation: role of lipid peroxidation products and scavenger receptor. Free Radic Biol Med 35:697-710
75. Duong LT, Rodan GA (2000) Pyk2 is an adhesion kinase in macrophages, localized in podosomes and activated by B2-integrin ligation. Cell Motil Cytoskeleton 47:174-188
76. Pfaff M, Jurdic P (2001) Podosomes in osteoclast-like cells: structural analysis and cooperative roles of paxillin, proline-rich tyrosine kinase 2 (Pyk2) and integrin alphaVbeta3. J Cell Sci 114:2775-2786
77. 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 101:2118-2128
78. Collin O et al (2008) Self-organized podosomes are dynamic mechanosensors. Curr Biol 18:1288-1294
79. Van Goethem E et al (2011) Macrophage podosomes go 3D. Eur J Cell Biol 90:224-236
80. Berton G, Lowell C (1999) Integrin signalling in neutrophils and macrophages. Cell Signal 11:621-635
81. Zaveri TD, Lewis JS, Dolgova NV, Clare-Salzler MJ, Keselowsky BG (2014) Integrin-directed modulation of macrophage responses to biomaterials. Biomaterials 35:3504-3515
82. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514
83. Aepfelbacher M, Essler M, Huber E, Czech A, Weber PC (1996) Rho is a negative regulator of human monocyte spreading. J Immunol 157:5070-5075
84. Allen WE, Jones GE, Pollard JW, Ridley AJ (1997) Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J Cell Sci 110(Pt 6):707-720
85. Ory S, Brazier H, Pawlak G, Blangy A (2008) Rho GTPases in osteoclasts: orchestrators of podosome arrangement. Eur J Cell Biol 87:469-477
86. Hoppe AD, Swanson JA (2004) Cdc42, Rac1, and Rac2 display distinct patterns of activation during phagocytosis. Mol Biol Cell 15:3509-3519
87. Joshi S, Singh A, Zulcic M, Bao L, Messer K (2014) Rac2 controls tumor growth, metastasis and M1-M2 macrophage differentiation in vivo. PLoS One 9(4):e95893
88. Wheeler AR, Smith SD, Ridley AJ (2006) CSF-1 and PI 3-kinase regulate podosome distribution and assembly in macrophages. Cell Motil Cytoskeleton 63:132-140
89. Cougoule C 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 91:938-949
90. Pradip D, Peng X, Durden DL (2003) Rac2 specificity in macrophage integrin signaling: potential role for Syk kinase. J Biol Chem 278:41661-41669
91. Mestas J, Hughes CCW (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172:2731-2738
92. Raes G et al (2002) Differential expression of FIZZ1 and Ym1 in alternatively versus classically activated macrophages. J Leukoc Biol 71:597-602
93. Raes G et al (2005) Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J Immunol 174:6561-6562
94. Okamura Y et al (2001) The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 276:10229-10233
95. Smiley ST, King JA, Hancock WW (2001) Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 167:2887-2894
96. Newman SL, Tucci MA (1990) Regulation of human monocyte/macrophage function by extracellular matrix by activation of complement receptors and enhancement of fc receptor function monocyte/mrb bactericidal assay. J Clin Invest 86:703-714
97. Huang E, Wells CA (2014) The ground state of innate immune responsiveness is determined at the interface of genetic, epigenetic, and environmental influences. J Immunol 193:13-19
98. Waterfield JD, Ali TA, Nahid F, Kusano K, Brunette DM (2010) The effect of surface topography on early NFκB signaling in macrophages. J Biomed Mater Res A 95:837-847
99. Wu J et al (2013) Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol 190:3590-3599
100. Martin D, Bootcov M, Campell T, French P, Breit S (1995) Human macrophages contain a stretch-sensitive potassium channel that is activated by adherence and cytokines. J Membr Biol 315:305-315
101. Ishii M et al (2009) Epigenetic regulation of the alternatively activated macrophage phenotype. Blood 114:3244-3254
102. Jetten N et al (2014) Wound administration of m2-polarized macrophages does not improve murine cutaneous healing responses. PLoS One 9:e102994
103. Mirza R, DiPietro LA, Koh TJ (2009) Selective and specific macrophage ablation is detrimental to wound healing in mice. Am J Pathol 175:2454-2462