Skip to main content

Role for Mechanotransduction in Macrophage and Dendritic Cell Immunobiology

  • Chapter
  • First Online:
Macrophages

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 62))

Abstract

Tissue homeostasis is not only controlled by biochemical signals but also through mechanical forces that act on cells. Yet, while it has long been known that biochemical signals have profound effects on cell biology, the importance of mechanical forces has only been recognized much more recently. The types of mechanical stress that cells experience include stretch, compression, and shear stress, which are mainly induced by the extracellular matrix, cell–cell contacts, and fluid flow. Importantly, macroscale tissue deformation through stretch or compression also affects cellular function.

Immune cells such as macrophages and dendritic cells are present in almost all peripheral tissues, and monocytes populate the vasculature throughout the body. These cells are unique in the sense that they are subject to a large variety of different mechanical environments, and it is therefore not surprising that key immune effector functions are altered by mechanical stimuli. In this chapter, we describe the different types of mechanical signals that cells encounter within the body and review the current knowledge on the role of mechanical signals in regulating macrophage, monocyte, and dendritic cell function.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abagnale G, Steger M, Nguyen VH, Hersch N, Sechi A, Joussen S, Denecke B, Merkel R, Hoffmann B, Dreser A, Schnakenberg U, Gillner A, Wagner W (2015) Surface topography enhances differentiation of mesenchymal stem cells towards osteogenic and adipogenic lineages. Biomaterials 61:316–326. doi:10.1016/j.biomaterials.2015.05.030

    Article  CAS  PubMed  Google Scholar 

  • Acton SE, Farrugia AJ, Astarita JL, Mourao-Sa D, Jenkins RP, Nye E, Hooper S, van Blijswijk J, Rogers NC, Snelgrove KJ, Rosewell I, Moita LF, Stamp G, Turley SJ, Sahai E, Reis e Sousa C (2014) Dendritic cells control fibroblastic reticular network tension and lymph node expansion. Nature 514(7523):498–502. doi:10.1038/nature13814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adamo L, Naveiras O, Wenzel PL, McKinney-Freeman S, Mack PJ, Gracia-Sancho J, Suchy-Dicey A, Yoshimoto M, Lensch MW, Yoder MC, Garcia-Cardena G, Daley GQ (2009) Biomechanical forces promote embryonic haematopoiesis. Nature 459(7250):1131–1135. doi:10.1038/nature08073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adlerz KM, Aranda-Espinoza H, Hayenga HN (2016) Substrate elasticity regulates the behavior of human monocyte-derived macrophages. Eur Biophys J EBJ 45(4):301–309. doi:10.1007/s00249-015-1096-8

    Article  CAS  PubMed  Google Scholar 

  • Akei H, Whitsett JA, Buroker M, Ninomiya T, Tatsumi H, Weaver TE, Ikegami M (2006) Surface tension influences cell shape and phagocytosis in alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 291(4):L572–L579. doi:10.1152/ajplung.00060.2006

    Article  CAS  PubMed  Google Scholar 

  • Anderson JA, Lamichhane S, Mani G (2016) Macrophage responses to 316 L stainless steel and cobalt chromium alloys with different surface topographies. J Biomed Mater Res A 104(11):2658–2672. doi:10.1002/jbm.a.35808

    Article  CAS  PubMed  Google Scholar 

  • Angele P, Yoo JU, Smith C, Mansour J, Jepsen KJ, Nerlich M, Johnstone B (2003) Cyclic hydrostatic pressure enhances the chondrogenic phenotype of human mesenchymal progenitor cells differentiated in vitro. J Orthop Res Off Publ Orthop Res Soc 21(3):451–457. doi:10.1016/S0736-0266(02)00230-9

    Article  CAS  Google Scholar 

  • Arold SP, Bartolak-Suki E, Suki B (2009) Variable stretch pattern enhances surfactant secretion in alveolar type II cells in culture. Am J Physiol Lung Cell Mol Physiol 296(4):L574–L581. doi:10.1152/ajplung.90454.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajaj P, Reddy B Jr, Millet L, Wei C, Zorlutuna P, Bao G, Bashir R (2011) Patterning the differentiation of C2C12 skeletal myoblasts. Integr Biol Quant Biosci Nano Macro 3(9):897–909. doi:10.1039/c1ib00058f

    CAS  Google Scholar 

  • Ball M, Grant DM, Lo WJ, Scotchford CA (2008) The effect of different surface morphology and roughness on osteoblast-like cells. J Biomed Mater Res A 86(3):637–647. doi:10.1002/jbm.a.31652

    Article  PubMed  CAS  Google Scholar 

  • Banerjee I, Carrion K, Serrano R, Dyo J, Sasik R, Lund S, Willems E, Aceves S, Meili R, Mercola M, Chen J, Zambon A, Hardiman G, Doherty TA, Lange S, del Alamo JC, Nigam V (2015) Cyclic stretch of embryonic cardiomyocytes increases proliferation, growth, and expression while repressing Tgf-beta signaling. J Mol Cell Cardiol 79:133–144. doi:10.1016/j.yjmcc.2014.11.003

    Article  CAS  PubMed  Google Scholar 

  • Bartneck M, Schulte VA, Paul NE, Diez M, Lensen MC, Zwadlo-Klarwasser G (2010) Induction of specific macrophage subtypes by defined micro-patterned structures. Acta Biomater 6(10):3864–3872. doi:10.1016/j.actbio.2010.04.025

    Article  CAS  PubMed  Google Scholar 

  • Bartneck M, Heffels KH, Pan Y, Bovi M, Zwadlo-Klarwasser G, Groll J (2012) Inducing healing-like human primary macrophage phenotypes by 3D hydrogel coated nanofibres. Biomaterials 33(16):4136–4146. doi:10.1016/j.biomaterials.2012.02.050

    Article  CAS  PubMed  Google Scholar 

  • Beningo KA, Wang YL (2002) Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J Cell Sci 115(Pt 4):849–856

    CAS  PubMed  Google Scholar 

  • Berry CC, Campbell G, Spadiccino A, Robertson M, Curtis AS (2004) The influence of microscale topography on fibroblast attachment and motility. Biomaterials 25(26):5781–5788. doi:10.1016/j.biomaterials.2004.01.029

    Article  CAS  PubMed  Google Scholar 

  • 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(6):1375–1386. doi:10.1002/jbm.a.34104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boochoon KS, Manarang JC, Davis JT, McDermott AM, Foster WJ (2014) The influence of substrate elastic modulus on retinal pigment epithelial cell phagocytosis. J Biomech 47(12):3237–3240. doi:10.1016/j.jbiomech.2014.06.021

    Article  PubMed  PubMed Central  Google Scholar 

  • Brock A, Chang E, Ho CC, LeDuc P, Jiang X, Whitesides GM, Ingber DE (2003) Geometric determinants of directional cell motility revealed using microcontact printing. Langmuir ACS J Surf Colloids 19(5):1611–1617

    Article  CAS  Google Scholar 

  • Brugnano JL, Panitch A (2014) Matrix stiffness affects endocytic uptake of MK2-inhibitor peptides. PLoS One 9(1):e84821. doi:10.1371/journal.pone.0084821

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Butcher DT, Alliston T, Weaver VM (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9(2):108–122. doi:10.1038/nrc2544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell JJ, Hedrick J, Zlotnik A, Siani MA, Thompson DA, Butcher EC (1998) Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279(5349):381–384

    Article  CAS  PubMed  Google Scholar 

  • 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(3):1151–1159. doi:10.1002/jbm.a.32609

    PubMed  Google Scholar 

  • Castro-Nunez L, Dienava-Verdoold I, Herczenik E, Mertens K, Meijer AB (2012) Shear stress is required for the endocytic uptake of the factor VIII-von Willebrand factor complex by macrophages. J Thromb Haemost JTH 10(9):1929–1937. doi:10.1111/j.1538-7836.2012.04860.x

    Article  CAS  PubMed  Google Scholar 

  • Champion JA, Mitragotri S (2006) Role of target geometry in phagocytosis. Proc Natl Acad Sci USA 103(13):4930–4934. doi:10.1073/pnas.0600997103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang SF, Chang CA, Lee DY, Lee PL, Yeh YM, Yeh CR, Cheng CK, Chien S, Chiu JJ (2008) Tumor cell cycle arrest induced by shear stress: roles of integrins and Smad. Proc Natl Acad Sci USA 105(10):3927–3932. doi:10.1073/pnas.0712353105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang JM, Park IA, Lee SH, Kim WH, Bae MS, Koo HR, Yi A, Kim SJ, Cho N, Moon WK (2013) Stiffness of tumours measured by shear-wave elastography correlated with subtypes of breast cancer. Eur Radiol 23(9):2450–2458. doi:10.1007/s00330-013-2866-2

    Article  PubMed  Google Scholar 

  • Chang YJ, Chen YJ, Huang CW, Fan SC, Huang BM, Chang WT, Tsai YS, Su FC, Wu CC (2016) Cyclic stretch facilitates myogenesis in C2C12 myoblasts and rescues thiazolidinedione-inhibited myotube formation. Front Bioeng Biotechnol 4:27. doi:10.3389/fbioe.2016.00027

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman KE, Sinclair SE, Zhuang D, Hassid A, Desai LP, Waters CM (2005) Cyclic mechanical strain increases reactive oxygen species production in pulmonary epithelial cells. Am J Physiol Lung Cell Mol Physiol 289(5):L834–L841. doi:10.1152/ajplung.00069.2005

    Article  CAS  PubMed  Google Scholar 

  • Chaterji S, Kim P, Choe SH, Tsui JH, Lam CH, Ho DS, Baker AB, Kim DH (2014) Synergistic effects of matrix nanotopography and stiffness on vascular smooth muscle cell function. Tissue Eng A 20(15–16):2115–2126. doi:10.1089/ten.tea.2013.0455

    Article  CAS  Google Scholar 

  • Chaudhuri PK, Pan CQ, Low BC, Lim CT (2016) Topography induces differential sensitivity on cancer cell proliferation via Rho-ROCK-Myosin contractility. Sci Rep 6:19672. doi:10.1038/srep19672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheeniyil A, Evani SJ, Dallo SF, Ramasubramanian AK (2015) Shear stress upregulates IL-1beta secretion by Chlamydia pneumoniae-infected monocytes. Biotechnol Bioeng 112(4):838–842. doi:10.1002/bit.25486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276(5317):1425–1428

    Article  CAS  PubMed  Google Scholar 

  • Chen CS, Alonso JL, Ostuni E, Whitesides GM, Ingber DE (2003) Cell shape provides global control of focal adhesion assembly. Biochem Biophys Res Commun 307(2):355–361

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Xie J, Deng L, Yang L (2014) Substrate stiffness together with soluble factors affects chondrocyte mechanoresponses. ACS Appl Mater Interfaces 6(18):16106–16116. doi:10.1021/am504135b

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Yan Y, Mullner M, Ping Y, Cui J, Kempe K, Cortez-Jugo C, Caruso F (2016) Shape-dependent activation of cytokine secretion by polymer capsules in human monocyte-derived macrophages. Biomacromolecules 17(3):1205–1212. doi:10.1021/acs.biomac.6b00027

    Article  CAS  PubMed  Google Scholar 

  • Choi B, Park KS, Kim JH, Ko KW, Kim JS, Han DK, Lee SH (2016) Stiffness of hydrogels regulates cellular reprogramming efficiency through mesenchymal-to-epithelial transition and stemness markers. Macromol Biosci 16(2):199–206. doi:10.1002/mabi.201500273

    Article  CAS  PubMed  Google Scholar 

  • Chowdhury F, Li Y, Poh YC, Yokohama-Tamaki T, Wang N, Tanaka TS (2010) Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS One 5(12):e15655. doi:10.1371/journal.pone.0015655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cicha I, Goppelt-Struebe M, Yilmaz A, Daniel WG, Garlichs CD (2008) Endothelial dysfunction and monocyte recruitment in cells exposed to non-uniform shear stress. Clin Hemorheol Microcirc 39(1–4):113–119

    CAS  PubMed  Google Scholar 

  • Collison JL, Carlin LM, Eichmann M, Geissmann F, Peakman M (2015) Heterogeneity in the locomotory behavior of human monocyte subsets over human vascular endothelium in vitro. J Immunol 195(3):1162–1170. doi:10.4049/jimmunol.1401806

    Article  CAS  PubMed  Google Scholar 

  • Cox TR, Erler JT (2011) Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis Model Mech 4(2):165–178. doi:10.1242/dmm.004077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Craig DH, Shiratsuchi H, Basson MD (2009) Increased extracellular pressure provides a novel adjuvant stimulus for enhancement of conventional dendritic cell maturation strategies. Biochem Biophys Res Commun 387(1):174–179. doi:10.1016/j.bbrc.2009.07.010

    Article  CAS  PubMed  Google Scholar 

  • David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, Jones DB, Vico L, Guignandon A (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148(5):2553–2562. doi:10.1210/en.2006-1704

    Article  CAS  PubMed  Google Scholar 

  • Deroanne CF, Lapiere CM, Nusgens BV (2001) In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc Res 49(3):647–658

    Article  CAS  PubMed  Google Scholar 

  • Doxzen K, Vedula SR, Leong MC, Hirata H, Gov NS, Kabla AJ, Ladoux B, Lim CT (2013) Guidance of collective cell migration by substrate geometry. Integr Biol Quant Biosci Nano Macro 5(8):1026–1035. doi:10.1039/c3ib40054a

    CAS  Google Scholar 

  • Dreier B, Gasiorowski JZ, Morgan JT, Nealey PF, Russell P, Murphy CJ (2013) Early responses of vascular endothelial cells to topographic cues. Am J Physiol Cell Physiol 305(3):C290–C298. doi:10.1152/ajpcell.00264.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edwards YS, Sutherland LM, Power JH, Nicholas TE, Murray AW (1999) Cyclic stretch induces both apoptosis and secretion in rat alveolar type II cells. FEBS Lett 448(1):127–130

    Article  CAS  PubMed  Google Scholar 

  • Edwards YS, Sutherland LM, Murray AW (2000) NO protects alveolar type II cells from stretch-induced apoptosis. A novel role for macrophages in the lung. Am J Physiol Lung Cell Mol Physiol 279(6):L1236–L1242

    CAS  PubMed  Google Scholar 

  • Ehrlich PJ, Lanyon LE (2002) Mechanical strain and bone cell function: a review. Osteoporos Int 13(9):688–700. doi:10.1007/s001980200095

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg JL, Safi A, Wei X, Espinosa HD, Budinger GS, Takawira D, Hopkinson SB, Jones JC (2011) Substrate stiffness regulates extracellular matrix deposition by alveolar epithelial cells. Res Rep Biol 2011(2):1–12. doi:10.2147/RRB.S13178

    PubMed  PubMed Central  Google Scholar 

  • Elder SH, Goldstein SA, Kimura JH, Soslowsky LJ, Spengler DM (2001) Chondrocyte differentiation is modulated by frequency and duration of cyclic compressive loading. Ann Biomed Eng 29(6):476–482

    Article  CAS  PubMed  Google Scholar 

  • Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166(6):877–887. doi:10.1083/jcb.200405004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689. doi:10.1016/j.cell.2006.06.044

    Article  CAS  PubMed  Google Scholar 

  • Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE (2008) Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 121(Pt 22):3794–3802. doi:10.1242/jcs.029678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eriksson C, Lausmaa J, Nygren H (2001) Interactions between human whole blood and modified TiO2-surfaces: influence of surface topography and oxide thickness on leukocyte adhesion and activation. Biomaterials 22(14):1987–1996

    Article  CAS  PubMed  Google Scholar 

  • Evani SJ, Murthy AK, Mareedu N, Montgomery RK, Arulanandam BP, Ramasubramanian AK (2011) Hydrodynamic regulation of monocyte inflammatory response to an intracellular pathogen. PLoS One 6(1):e14492. doi:10.1371/journal.pone.0014492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evani SJ, Dallo SF, Murthy AK, Ramasubramanian AK (2013) Shear stress enhances chemokine secretion from Chlamydia pneumoniae-infected monocytes. Cell Mol Bioeng 6(3):326–334. doi:10.1007/s12195-013-0291-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evans ND, Minelli C, Gentleman E, LaPointe V, Patankar SN, Kallivretaki M, Chen X, Roberts CJ, Stevens MM (2009) Substrate stiffness affects early differentiation events in embryonic stem cells. Eur Cell Mater 18:1–13. discussion 13–14

    Article  CAS  PubMed  Google Scholar 

  • Fan R, Emery T, Zhang Y, Xia Y, Sun J, Wan J (2016) Circulatory shear flow alters the viability and proliferation of circulating colon cancer cells. Sci Rep 6:27073. doi:10.1038/srep27073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fereol S, Fodil R, Labat B, Galiacy S, Laurent VM, Louis B, Isabey D, Planus E (2006) Sensitivity of alveolar macrophages to substrate mechanical and adhesive properties. Cell Motil Cytoskeleton 63(6):321–340. doi:10.1002/cm.20130

    Article  PubMed  Google Scholar 

  • Fereol S, Fodil R, Laurent VM, Planus E, Louis B, Pelle G, Isabey D (2008) Mechanical and structural assessment of cortical and deep cytoskeleton reveals substrate-dependent alveolar macrophage remodeling. Biomed Mater Eng 18(1 Suppl):S105–S118

    CAS  PubMed  Google Scholar 

  • Flanagan LA, Ju YE, Marg B, Osterfield M, Janmey PA (2002) Neurite branching on deformable substrates. Neuroreport 13(18):2411–2415. doi:10.1097/01.wnr.0000048003.96487.97

    Article  PubMed  PubMed Central  Google Scholar 

  • Frank V, Kaufmann S, Wright R, Horn P, Yoshikawa HY, Wuchter P, Madsen J, Lewis AL, Armes SP, Ho AD, Tanaka M (2016) Frequent mechanical stress suppresses proliferation of mesenchymal stem cells from human bone marrow without loss of multipotency. Sci Rep 6:24264. doi:10.1038/srep24264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galie PA, Nguyen DH, Choi CK, Cohen DM, Janmey PA, Chen CS (2014) Fluid shear stress threshold regulates angiogenic sprouting. Proc Natl Acad Sci USA 111(22):7968–7973. doi:10.1073/pnas.1310842111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galie PA, van Oosten A, Chen CS, Janmey PA (2015) Application of multiple levels of fluid shear stress to endothelial cells plated on polyacrylamide gels. Lab Chip 15(4):1205–1212. doi:10.1039/c4lc01236d

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geblinger D, Addadi L, Geiger B (2010) Nano-topography sensing by osteoclasts. J Cell Sci 123(Pt 9):1503–1510. doi:10.1242/jcs.060954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georges PC, Hui JJ, Gombos Z, McCormick ME, Wang AY, Uemura M, Mick R, Janmey PA, Furth EE, Wells RG (2007) Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 293(6):G1147–G1154. doi:10.1152/ajpgi.00032.2007

    Article  CAS  PubMed  Google Scholar 

  • Ginhoux F, Guilliams M (2016) Tissue-resident macrophage ontogeny and homeostasis. Immunity 44(3):439–449. doi:10.1016/j.immuni.2016.02.024

    Article  CAS  PubMed  Google Scholar 

  • Grodzinsky AJ, Levenston ME, Jin M, Frank EH (2000) Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng 2:691–713. doi:10.1146/annurev.bioeng.2.1.691

    Article  CAS  PubMed  Google Scholar 

  • Grundy TJ, De Leon E, Griffin KR, Stringer BW, Day BW, Fabry B, Cooper-White J, O’Neill GM (2016) Differential response of patient-derived primary glioblastoma cells to environmental stiffness. Sci Rep 6:23353. doi:10.1038/srep23353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guilak F, Cohen DM, Estes BT, Gimble JM, Liedtke W, Chen CS (2009) Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5(1):17–26. doi:10.1016/j.stem.2009.06.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammerschmidt S, Kuhn H, Sack U, Schlenska A, Gessner C, Gillissen A, Wirtz H (2005) Mechanical stretch alters alveolar type II cell mediator release toward a proinflammatory pattern. Am J Respir Cell Mol Biol 33(2):203–210. doi:10.1165/rcmb.2005-0067OC

    Article  CAS  PubMed  Google Scholar 

  • Haniffa M, Bigley V, Collin M (2015) Human mononuclear phagocyte system reunited. Semin Cell Dev Biol 41:59–69. doi:10.1016/j.semcdb.2015.05.004

    Article  CAS  PubMed  Google Scholar 

  • Heo KS, Fujiwara K, Abe J (2014) Shear stress and atherosclerosis. Mol Cells 37(6):435–440. doi:10.14348/molcells.2014.0078

    Google Scholar 

  • Her GJ, Wu HC, Chen MH, Chen MY, Chang SC, Wang TW (2013) Control of three-dimensional substrate stiffness to manipulate mesenchymal stem cell fate toward neuronal or glial lineages. Acta Biomater 9(2):5170–5180. doi:10.1016/j.actbio.2012.10.012

    Article  CAS  PubMed  Google Scholar 

  • Herd H, Daum N, Jones AT, Huwer H, Ghandehari H, Lehr CM (2013) Nanoparticle geometry and surface orientation influence mode of cellular uptake. ACS Nano 7(3):1961–1973. doi:10.1021/nn304439f

    Article  CAS  PubMed  Google Scholar 

  • Hettinger J, Richards DM, Hansson J, Barra MM, Joschko AC, Krijgsveld J, Feuerer M (2013) Origin of monocytes and macrophages in a committed progenitor. Nat Immunol 14(8):821–830. doi:10.1038/ni.2638

    Article  CAS  PubMed  Google Scholar 

  • Hind LE, Dembo M, Hammer DA (2015) Macrophage motility is driven by frontal-towing with a force magnitude dependent on substrate stiffness. Integr Biol Quant Biosci Nano Macro 7(4):447–453. doi:10.1039/c4ib00260a

    CAS  Google Scholar 

  • Hotchkiss KM, Reddy GB, Hyzy SL, Schwartz Z, Boyan BD, Olivares-Navarrete R (2016) Titanium surface characteristics, including topography and wettability, alter macrophage activation. Acta Biomater 31:425–434. doi:10.1016/j.actbio.2015.12.003

    Article  CAS  PubMed  Google Scholar 

  • Hsiong SX, Carampin P, Kong HJ, Lee KY, Mooney DJ (2008) Differentiation stage alters matrix control of stem cells. J Biomed Mater Res A 85(1):145–156. doi:10.1002/jbm.a.31521

    Article  PubMed  Google Scholar 

  • Huang CY, Hagar KL, Frost LE, Sun Y, Cheung HS (2004) Effects of cyclic compressive loading on chondrogenesis of rabbit bone-marrow derived mesenchymal stem cells. Stem Cells 22(3):313–323. doi:10.1634/stemcells.22-3-313

    Article  CAS  PubMed  Google Scholar 

  • Huang C, Ozdemir T, Xu LC, Butler PJ, Siedlecki CA, Brown JL, Zhang S (2016) The role of substrate topography on the cellular uptake of nanoparticles. J Biomed Mater Res B Appl Biomater 104(3):488–495. doi:10.1002/jbm.b.33397

    Article  CAS  PubMed  Google Scholar 

  • Huynh J, Nishimura N, Rana K, Peloquin JM, Califano JP, Montague CR, King MR, Schaffer CB, Reinhart-King CA (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 3(112):112ra122. doi:10.1126/scitranslmed.3002761

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Irwin EF, Saha K, Rosenbluth M, Gamble LJ, Castner DG, Healy KE (2008) Modulus-dependent macrophage adhesion and behavior. J Biomater Sci Polym Ed 19(10):1363–1382. doi:10.1163/156856208786052407

    Article  CAS  PubMed  Google Scholar 

  • Izumi G, Koga K, Nagai M, Urata Y, Takamura M, Harada M, Hirata T, Hirota Y, Ogawa K, Inoue S, Fujii T, Osuga Y (2015) Cyclic stretch augments production of neutrophil chemokines, matrix metalloproteinases, and activin a in human endometrial stromal cells. Am J Reprod Immunol 73(6):501–506. doi:10.1111/aji.12359

    Article  CAS  PubMed  Google Scholar 

  • Jadhav S, Bochner BS, Konstantopoulos K (2001) Hydrodynamic shear regulates the kinetics and receptor specificity of polymorphonuclear leukocyte-colon carcinoma cell adhesive interactions. J Immunol 167(10):5986–5993

    Article  CAS  PubMed  Google Scholar 

  • Jafari B, Ouyang B, Li LF, Hales CA, Quinn DA (2004) Intracellular glutathione in stretch-induced cytokine release from alveolar type-2 like cells. Respirology 9(1):43–53. doi:10.1111/j.1440-1843.2003.00527.x

    Article  PubMed  Google Scholar 

  • Janmey PA, Weitz DA (2004) Dealing with mechanics: mechanisms of force transduction in cells. Trends Biochem Sci 29(7):364–370. doi:10.1016/j.tibs.2004.05.003

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo M, Singh SS, Velankar S, Kumta PN, Banerjee I (2015) Inducing endoderm differentiation by modulating mechanical properties of soft substrates. J Tissue Eng Regen Med 9(1):1–12. doi:10.1002/term.1602

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Zeng Z, Sun D, Ka W, Wen Z (2005) Adhesion of monocyte-derived dendritic cells to human umbilical vein endothelial cells in flow field decreases upon maturation. Clin Hemorheol Microcirc 32(4):261–268

    PubMed  Google Scholar 

  • Jiang J, Woulfe DS, Papoutsakis ET (2014) Shear enhances thrombopoiesis and formation of microparticles that induce megakaryocytic differentiation of stem cells. Blood 124(13):2094–2103. doi:10.1182/blood-2014-01-547927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khatiwala CB, Peyton SR, Putnam AJ (2006) Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. Am J Physiol Cell Physiol 290(6):C1640–C1650. doi:10.1152/ajpcell.00455.2005

    Article  CAS  PubMed  Google Scholar 

  • 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(11):4872–4877. doi:10.1073/pnas.0903269107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim MH, Sawada Y, Taya M, Kino-Oka M (2014) Influence of surface topography on the human epithelial cell response to micropatterned substrates with convex and concave architectures. J Biol Eng 8:13. doi:10.1186/1754-1611-8-13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kou PM, Schwartz Z, Boyan BD, Babensee JE (2011) Dendritic cell responses to surface properties of clinical titanium surfaces. Acta Biomater 7(3):1354–1363. doi:10.1016/j.actbio.2010.10.020

    Article  CAS  PubMed  Google Scholar 

  • Kourouklis AP, Kaylan KB, Underhill GH (2016) Substrate stiffness and matrix composition coordinately control the differentiation of liver progenitor cells. Biomaterials 99:82–94. doi:10.1016/j.biomaterials.2016.05.016

    Article  CAS  PubMed  Google Scholar 

  • Kulangara K, Yang J, Chellappan M, Yang Y, Leong KW (2014) Nanotopography alters nuclear protein expression, proliferation and differentiation of human mesenchymal stem/stromal cells. PLoS One 9(12):e114698. doi:10.1371/journal.pone.0114698

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kushida N, Yamaguchi O, Kawashima Y, Akaihata H, Hata J, Ishibashi K, Aikawa K, Kojima Y (2016) Uni-axial stretch induces actin stress fiber reorganization and activates c-Jun NH2 terminal kinase via RhoA and Rho kinase in human bladder smooth muscle cells. BMC Urol 16:9. doi:10.1186/s12894-016-0127-9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee S, Choi J, Shin S, Im YM, Song J, Kang SS, Nam TH, Webster TJ, Kim SH, Khang D (2011) Analysis on migration and activation of live macrophages on transparent flat and nanostructured titanium. Acta Biomater 7(5):2337–2344. doi:10.1016/j.actbio.2011.01.006

    Article  CAS  PubMed  Google Scholar 

  • Lee HG, Hsu A, Goto H, Nizami S, Lee JH, Cadet ER, Tang P, Shaji R, Chandhanayinyong C, Kweon SH, Oh DS, Tawfeek H, Lee FY (2013) Aggravation of inflammatory response by costimulation with titanium particles and mechanical perturbations in osteoblast- and macrophage-like cells. Am J Physiol Cell Physiol 304(5):C431–C439. doi:10.1152/ajpcell.00202.2012

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Abdeen AA, Huang TH, Kilian KA (2014) Controlling cell geometry on substrates of variable stiffness can tune the degree of osteogenesis in human mesenchymal stem cells. J Mech Behav Biomed Mater 38:209–218. doi:10.1016/j.jmbbm.2014.01.009

    Article  CAS  PubMed  Google Scholar 

  • Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5):891–906. doi:10.1016/j.cell.2009.10.027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lewis JS, Dolgova NV, Chancellor TJ, Acharya AP, Karpiak JV, Lele TP, Keselowsky BG (2013) The effect of cyclic mechanical strain on activation of dendritic cells cultured on adhesive substrates. Biomaterials 34(36):9063–9070. doi:10.1016/j.biomaterials.2013.08.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li F, Sun X, Zhao B, Ma J, Zhang Y, Li S, Li Y, Ma X (2015a) Effects of cyclic tension stress on the apoptosis of osteoclasts in vitro. Exp Ther Med 9(5):1955–1961. doi:10.3892/etm.2015.2338

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Tang QY, Jadhav AD, Narang A, Qian WX, Shi P, Pang SW (2015b) Large-scale topographical screen for investigation of physical neural-guidance cues. Sci Rep 5:8644. doi:10.1038/srep08644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang S, Slattery MJ, Wagner D, Simon SI, Dong C (2008) Hydrodynamic shear rate regulates melanoma-leukocyte aggregation, melanoma adhesion to the endothelium, and subsequent extravasation. Ann Biomed Eng 36(4):661–671. doi:10.1007/s10439-008-9445-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhao F, Gu W, Yang H, Meng Q, Zhang Y, Yang H, Duan Q (2009) The roles of platelet GPIIb/IIIa and alphavbeta3 integrins during HeLa cells adhesion, migration, and invasion to monolayer endothelium under static and dynamic shear flow. J Biomed Biotechnol 2009:829243. doi:10.1155/2009/829243

    PubMed  PubMed Central  Google Scholar 

  • Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschumperlin DJ (2010) Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 190(4):693–706. doi:10.1083/jcb.201004082

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79(1):144–152. doi:10.1016/S0006-3495(00)76279-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu D, Luo C, Zhang C, Li Z, Long M (2014) Differential regulation of morphology and stemness of mouse embryonic stem cells by substrate stiffness and topography. Biomaterials 35(13):3945–3955. doi:10.1016/j.biomaterials.2014.01.066

    Article  CAS  PubMed  Google Scholar 

  • Luff SA, Papoutsakis ET (2016) Megakaryocytic maturation in response to shear flow is mediated by the activator protein 1 (AP-1) transcription factor via mitogen-activated protein kinase (MAPK) mechanotransduction. J Biol Chem 291(15):7831–7843. doi:10.1074/jbc.M115.707174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacKay JL, Hammer DA (2016) Stiff substrates enhance monocytic cell capture through E-selectin but not P-selectin. Integr Biol Quant Biosci Nano Macro 8(1):62–72. doi:10.1039/c5ib00199d

    CAS  Google Scholar 

  • Martinez E, Engel E, Planell JA, Samitier J (2009) Effects of artificial micro- and nano-structured surfaces on cell behaviour. Ann Anat 191(1):126–135. doi:10.1016/j.aanat.2008.05.006

    Article  CAS  PubMed  Google Scholar 

  • Mass E, Ballesteros I, Farlik M, Halbritter F, Gunther P, Crozet L, Jacome-Galarza CE, Handler K, Klughammer J, Kobayashi Y, Gomez-Perdiguero E, Schultze JL, Beyer M, Bock C, Geissmann F (2016) Specification of tissue-resident macrophages during organogenesis. Science 353(6304). doi:10.1126/science.aaf4238

  • Mathaes R, Winter G, Siahaan TJ, Besheer A, Engert J (2015) Influence of particle size, an elongated particle geometry, and adjuvants on dendritic cell activation. Eur J Pharm Biopharm 94:542–549. doi:10.1016/j.ejpb.2015.06.015

    Article  CAS  PubMed  Google Scholar 

  • Matheson LA, Maksym GN, Santerre JP, Labow RS (2006) Cyclic biaxial strain affects U937 macrophage-like morphology and enzymatic activities. J Biomed Mater Res A 76(1):52–62. doi:10.1002/jbm.a.30448

    Article  PubMed  Google Scholar 

  • Mathur AB, Reichert WM, Truskey GA (2007) Flow and high affinity binding affect the elastic modulus of the nucleus, cell body and the stress fibers of endothelial cells. Ann Biomed Eng 35(7):1120–1130. doi:10.1007/s10439-007-9288-8

    Article  PubMed  Google Scholar 

  • Matsuzaki S, Canis M, Pouly JL, Darcha C (2016) Soft matrices inhibit cell proliferation and inactivate the fibrotic phenotype of deep endometriotic stromal cells in vitro. Hum Reprod 31(3):541–553. doi:10.1093/humrep/dev333

    Article  PubMed  Google Scholar 

  • McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6(4):483–495

    Article  CAS  PubMed  Google Scholar 

  • McKee CT, Wood JA, Ly I, Russell P, Murphy CJ (2012) The influence of a biologically relevant substratum topography on human aortic and umbilical vein endothelial cells. Biophys J 102(5):1224–1233. doi:10.1016/j.bpj.2012.01.053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McWhorter FY, Wang T, Nguyen P, Chung T, Liu WF (2013) Modulation of macrophage phenotype by cell shape. Proc Natl Acad Sci USA 110(43):17253–17258. doi:10.1073/pnas.1308887110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messer RL, Mickalonis J, Lewis JB, Omata Y, Davis CM, Brown Y, Wataha JC (2008) Interactions between stainless steel, shear stress, and monocytes. J Biomed Mater Res A 87(1):229–235. doi:10.1002/jbm.a.31730

    Article  PubMed  CAS  Google Scholar 

  • Micholt L, Gartner A, Prodanov D, Braeken D, Dotti CG, Bartic C (2013) Substrate topography determines neuronal polarization and growth in vitro. PLoS One 8(6):e66170. doi:10.1371/journal.pone.0066170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mihic A, Li J, Miyagi Y, Gagliardi M, Li SH, Zu J, Weisel RD, Keller G, Li RK (2014) The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 35(9):2798–2808. doi:10.1016/j.biomaterials.2013.12.052

    Article  CAS  PubMed  Google Scholar 

  • Mita Y, Dobashi K, Nakazawa T, Mori M (2001) Mechanical fluid flow and surfactant-TA influence activation of macrophages. In Vitro Cell Dev Biol Anim 37(5):270–274. doi:10.1007/BF02577542

    Article  CAS  PubMed  Google Scholar 

  • Mohiuddin M, Pan HA, Hung YC, Huang GS (2012) Control of growth and inflammatory response of macrophages and foam cells with nanotopography. Nanoscale Res Lett 7(1):394. doi:10.1186/1556-276X-7-394

    Article  PubMed  PubMed Central  Google Scholar 

  • Morgan JT, Wood JA, Shah NM, Hughbanks ML, Russell P, Barakat AI, Murphy CJ (2012) Integration of basal topographic cues and apical shear stress in vascular endothelial cells. Biomaterials 33(16):4126–4135. doi:10.1016/j.biomaterials.2012.02.047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moura Rosa P, Gopalakrishnan N, Ibrahim H, Haug M, Halaas O (2016) The intercell dynamics of T cells and dendritic cells in a lymph node-on-a-chip flow device. Lab Chip 16(19):3728–3740. doi:10.1039/c6lc00702c

    Article  CAS  PubMed  Google Scholar 

  • Naik SH, Sathe P, Park HY, Metcalf D, Proietto AI, Dakic A, Carotta S, O’Keeffe M, Bahlo M, Papenfuss A, Kwak JY, Wu L, Shortman K (2007) Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat Immunol 8(11):1217–1226. doi:10.1038/ni1522

    Article  CAS  PubMed  Google Scholar 

  • Naujok O, Bandou Y, Shikama Y, Funaki M, Lenzen S (2014) Effect of substrate rigidity in tissue culture on the function of insulin-secreting INS-1E cells. J Tissue Eng Regen Med. doi:10.1002/term.1857

    PubMed  Google Scholar 

  • Ng CP, Helm CL, Swartz MA (2004) Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc Res 68(3):258–264. doi:10.1016/j.mvr.2004.08.002

    Article  PubMed  Google Scholar 

  • Niwa K, Kado T, Sakai J, Karino T (2004) The effects of a shear flow on the uptake of LDL and acetylated LDL by an EC monoculture and an EC-SMC coculture. Ann Biomed Eng 32(4):537–543

    Article  PubMed  Google Scholar 

  • Nomura S, Takano-Yamamoto T (2000) Molecular events caused by mechanical stress in bone. Matrix Biol J Int Soc Matrix Biol 19(2):91–96

    Article  CAS  Google Scholar 

  • North TE, Goessling W, Peeters M, Li P, Ceol C, Lord AM, Weber GJ, Harris J, Cutting CC, Huang P, Dzierzak E, Zon LI (2009) Hematopoietic stem cell development is dependent on blood flow. Cell 137(4):736–748. doi:10.1016/j.cell.2009.04.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okabe Y, Medzhitov R (2016) Tissue biology perspective on macrophages. Nat Immunol 17(1):9–17. doi:10.1038/ni.3320

    Article  CAS  PubMed  Google Scholar 

  • Olivier LA, Yen J, Reichert WM, Truskey GA (1999) Short-term cell/substrate contact dynamics of subconfluent endothelial cells following exposure to laminar flow. Biotechnol Prog 15(1):33–42. doi:10.1021/bp980107e

    Article  CAS  PubMed  Google Scholar 

  • Olsen AL, Bloomer SA, Chan EP, Gaca MD, Georges PC, Sackey B, Uemura M, Janmey PA, Wells RG (2011) Hepatic stellate cells require a stiff environment for myofibroblastic differentiation. Am J Physiol Gastrointest Liver Physiol 301(1):G110–G118. doi:10.1152/ajpgi.00412.2010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onai N, Obata-Onai A, Schmid MA, Ohteki T, Jarrossay D, Manz MG (2007) Identification of clonogenic common Flt3+M-CSFR+ plasmacytoid and conventional dendritic cell progenitors in mouse bone marrow. Nat Immunol 8(11):1207–1216. doi:10.1038/ni1518

    Article  CAS  PubMed  Google Scholar 

  • Oya K, Sakamoto N, Sato M (2013) Hypoxia suppresses stretch-induced elongation and orientation of macrophages. Biomed Mater Eng 23(6):463–471. doi:10.3233/BME-130770

    CAS  PubMed  Google Scholar 

  • Parker KK, Brock AL, Brangwynne C, Mannix RJ, Wang N, Ostuni E, Geisse NA, Adams JC, Whitesides GM, Ingber DE (2002) Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB J Off Publ Fed Am Soc Exp Biol 16(10):1195–1204. doi:10.1096/fj.02-0038com

    CAS  Google Scholar 

  • Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241–254. doi:10.1016/j.ccr.2005.08.010

    Article  CAS  PubMed  Google Scholar 

  • Patel H, Kwon S (2009) Interplay between cytokine-induced and cyclic equibiaxial deformation-induced nitric oxide production and metalloproteases expression in human alveolar epithelial cells. Cell Mol Bioeng 2(4):615–624. doi:10.1007/s12195-009-0092-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel NR, Bole M, Chen C, Hardin CC, Kho AT, Mih J, Deng L, Butler J, Tschumperlin D, Fredberg JJ, Krishnan R, Koziel H (2012) Cell elasticity determines macrophage function. PLoS One 7(9):e41024. doi:10.1371/journal.pone.0041024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pathak JL, Bravenboer N, Luyten FP, Verschueren P, Lems WF, Klein-Nulend J, Bakker AD (2015) Mechanical loading reduces inflammation-induced human osteocyte-to-osteoclast communication. Calcif Tissue Int 97(2):169–178. doi:10.1007/s00223-015-9999-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul NE, Skazik C, Harwardt M, Bartneck M, Denecke B, Klee D, Salber J, Zwadlo-Klarwasser G (2008) Topographical control of human macrophages by a regularly microstructured polyvinylidene fluoride surface. Biomaterials 29(30):4056–4064. doi:10.1016/j.biomaterials.2008.07.010

    Article  CAS  PubMed  Google Scholar 

  • Pelham RJ Jr, Wang Y (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci USA 94(25):13661–13665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng R, Yao X, Ding J (2011) Effect of cell anisotropy on differentiation of stem cells on micropatterned surfaces through the controlled single cell adhesion. Biomaterials 32(32):8048–8057. doi:10.1016/j.biomaterials.2011.07.035

    Article  CAS  PubMed  Google Scholar 

  • Peyton SR, Putnam AJ (2005) Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 204(1):198–209. doi:10.1002/jcp.20274

    Article  CAS  PubMed  Google Scholar 

  • Previtera ML, Sengupta A (2015) Substrate stiffness regulates proinflammatory mediator production through TLR4 activity in macrophages. PLoS One 10(12):e0145813. doi:10.1371/journal.pone.0145813

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Previtera ML, Peterman K, Shah S, Luzuriaga J (2015) Lipid rafts direct macrophage motility in the tissue microenvironment. Ann Biomed Eng 43(4):896–905. doi:10.1007/s10439-014-1142-1

    Article  PubMed  Google Scholar 

  • Pritchard WF, Davies PF, Derafshi Z, Polacek DC, Tsao R, Dull RO, Jones SA, Giddens DP (1995) Effects of wall shear stress and fluid recirculation on the localization of circulating monocytes in a three-dimensional flow model. J Biomech 28(12):1459–1469

    Article  CAS  PubMed  Google Scholar 

  • Pugin J, Dunn I, Jolliet P, Tassaux D, Magnenat JL, Nicod LP, Chevrolet JC (1998) Activation of human macrophages by mechanical ventilation in vitro. Am J Physiol 275(6 Pt 1):L1040–L1050

    CAS  PubMed  Google Scholar 

  • 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 A 70(2):194–205. doi:10.1002/jbm.a.30075

    Article  PubMed  CAS  Google Scholar 

  • Reijnders CM, Bravenboer N, Tromp AM, Blankenstein MA, Lips P (2007) Effect of mechanical loading on insulin-like growth factor-I gene expression in rat tibia. J Endocrinol 192(1):131–140. doi:10.1677/joe.1.06880

    Article  CAS  PubMed  Google Scholar 

  • Saez A, Ghibaudo M, Buguin A, Silberzan P, Ladoux B (2007) Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc Natl Acad Sci USA 104(20):8281–8286. doi:10.1073/pnas.0702259104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saino E, Focarete ML, Gualandi C, Emanuele E, Cornaglia AI, Imbriani M, Visai L (2011) Effect of electrospun fiber diameter and alignment on macrophage activation and secretion of proinflammatory cytokines and chemokines. Biomacromolecules 12(5):1900–1911. doi:10.1021/bm200248h

    Article  CAS  PubMed  Google Scholar 

  • Satpathy AT, Wu X, Albring JC, Murphy KM (2012) Re(de)fining the dendritic cell lineage. Nat Immunol 13(12):1145–1154. doi:10.1038/ni.2467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheraga RG, Abraham S, Niese KA, Southern BD, Grove LM, Hite RD, McDonald C, Hamilton TA, Olman MA (2016) TRPV4 mechanosensitive ion channel regulates lipopolysaccharide-stimulated macrophage phagocytosis. J Immunol 196(1):428–436. doi:10.4049/jimmunol.1501688

    Article  CAS  PubMed  Google Scholar 

  • Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, Benten D, Forbes SJ, Wells RG, Iredale JP (2011) Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53(4):1192–1205. doi:10.1002/hep.24108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scott HA, Quach B, Yang X, Ardekani S, Cabrera AP, Wilson R, Messaoudi-Powers I, Ghosh K (2016) Matrix stiffness exerts biphasic control over monocyte-endothelial adhesion via Rho-mediated ICAM-1 clustering. Integr Biol Quant Biosci Nano Macro 8(8):869–878. doi:10.1039/c6ib00084c

    CAS  Google Scholar 

  • Semler EJ, Lancin PA, Dasgupta A, Moghe PV (2005) Engineering hepatocellular morphogenesis and function via ligand-presenting hydrogels with graded mechanical compliance. Biotechnol Bioeng 89(3):296–307. doi:10.1002/bit.20328

    Article  CAS  PubMed  Google Scholar 

  • Seneviratne AN, Cole JE, Goddard ME, Park I, Mohri Z, Sansom S, Udalova I, Krams R, Monaco C (2015) Low shear stress induces M1 macrophage polarization in murine thin-cap atherosclerotic plaques. J Mol Cell Cardiol 89(Pt B):168–172. doi:10.1016/j.yjmcc.2015.10.034

    Article  CAS  PubMed  Google Scholar 

  • Serbina NV, Jia T, Hohl TM, Pamer EG (2008) Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 26:421–452. doi:10.1146/annurev.immunol.26.021607.090326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shebanova O, Hammer DA (2012) Biochemical and mechanical extracellular matrix properties dictate mammary epithelial cell motility and assembly. Biotechnol J 7(3):397–408. doi:10.1002/biot.201100188

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Dong Y, Duan Y, Jiang X, Chen C, Deng L (2013) Substrate stiffness influences TGF-beta1-induced differentiation of bronchial fibroblasts into myofibroblasts in airway remodeling. Mol Med Rep 7(2):419–424. doi:10.3892/mmr.2012.1213

    CAS  PubMed  Google Scholar 

  • Shiratsuchi H, Basson MD (2004) Extracellular pressure stimulates macrophage phagocytosis by inhibiting a pathway involving FAK and ERK. Am J Physiol Cell Physiol 286(6):C1358–C1366. doi:10.1152/ajpcell.00553.2003

    Article  CAS  PubMed  Google Scholar 

  • Shiratsuchi H, Basson MD (2005) Activation of p38 MAPKalpha by extracellular pressure mediates the stimulation of macrophage phagocytosis by pressure. Am J Physiol Cell Physiol 288(5):C1083–C1093. doi:10.1152/ajpcell.00543.2004

    Article  CAS  PubMed  Google Scholar 

  • Shive MS, Brodbeck WG, Colton E, Anderson JM (2002) Shear stress and material surface effects on adherent human monocyte apoptosis. J Biomed Mater Res 60(1):148–158

    Article  CAS  PubMed  Google Scholar 

  • Siddharthan V, Kim YV, Liu S, Kim KS (2007) Human astrocytes/astrocyte-conditioned medium and shear stress enhance the barrier properties of human brain microvascular endothelial cells. Brain Res 1147:39–50. doi:10.1016/j.brainres.2007.02.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skardal A, Mack D, Atala A, Soker S (2013) Substrate elasticity controls cell proliferation, surface marker expression and motile phenotype in amniotic fluid-derived stem cells. J Mech Behav Biomed Mater 17:307–316. doi:10.1016/j.jmbbm.2012.10.001

    Article  CAS  PubMed  Google Scholar 

  • Soltow QA, Zeanah EH, Lira VA, Criswell DS (2013) Cessation of cyclic stretch induces atrophy of C2C12 myotubes. Biochem Biophys Res Commun 434(2):316–321. doi:10.1016/j.bbrc.2013.03.048

    Article  CAS  PubMed  Google Scholar 

  • Sonam S, Sathe SR, Yim EK, Sheetz MP, Lim CT (2016) Cell contractility arising from topography and shear flow determines human mesenchymal stem cell fate. Sci Rep 6:20415. doi:10.1038/srep20415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song JW, Munn LL (2011) Fluid forces control endothelial sprouting. Proc Natl Acad Sci USA 108(37):15342–15347. doi:10.1073/pnas.1105316108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanton MM, Parrillo A, Thomas GM, McGimpsey WG, Wen Q, Bellin RM, Lambert CR (2015) Fibroblast extracellular matrix and adhesion on microtextured polydimethylsiloxane scaffolds. J Biomed Mater Res B Appl Biomater 103(4):861–869. doi:10.1002/jbm.b.33244

    Article  PubMed  CAS  Google Scholar 

  • Sun SJ, Yu WQ, Zhang YL, Jiang XQ, Zhang FQ (2013) Effects of TiO2 nanotube layers on RAW 264.7 macrophage behaviour and bone morphogenetic protein-2 expression. Cell Prolif 46(6):685–694. doi:10.1111/cpr.12072

    Article  CAS  PubMed  Google Scholar 

  • Takebe J, Champagne CM, Offenbacher S, Ishibashi K, Cooper LF (2003) Titanium surface topography alters cell shape and modulates bone morphogenetic protein 2 expression in the J774A.1 macrophage cell line. J Biomed Mater Res A 64(2):207–216. doi:10.1002/jbm.a.10275

    Article  CAS  PubMed  Google Scholar 

  • 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(30):5170–5177. doi:10.1016/j.biomaterials.2006.05.002

    Article  CAS  PubMed  Google Scholar 

  • Tan LH, Sykes PH, Alkaisi MM, Evans JJ (2015) The characteristics of Ishikawa endometrial cancer cells are modified by substrate topography with cell-like features and the polymer surface. Int J Nanomedicine 10:4883–4895. doi:10.2147/IJN.S86336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tang X, Kuhlenschmidt TB, Zhou J, Bell P, Wang F, Kuhlenschmidt MS, Saif TA (2010) Mechanical force affects expression of an in vitro metastasis-like phenotype in HCT-8 cells. Biophys J 99(8):2460–2469. doi:10.1016/j.bpj.2010.08.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tee SY, Fu J, Chen CS, Janmey PA (2011) Cell shape and substrate rigidity both regulate cell stiffness. Biophys J 100(5):L25–L27. doi:10.1016/j.bpj.2010.12.3744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teo BK, Goh SH, Kustandi TS, Loh WW, Low HY, Yim EK (2011) The effect of micro and nanotopography on endocytosis in drug and gene delivery systems. Biomaterials 32(36):9866–9875. doi:10.1016/j.biomaterials.2011.08.088

    Article  CAS  PubMed  Google Scholar 

  • Terraciano V, Hwang N, Moroni L, Park HB, Zhang Z, Mizrahi J, Seliktar D, Elisseeff J (2007) Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 25(11):2730–2738. doi:10.1634/stemcells.2007-0228

    Article  CAS  PubMed  Google Scholar 

  • Thery M, Pepin A, Dressaire E, Chen Y, Bornens M (2006) Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil Cytoskeleton 63(6):341–355. doi:10.1002/cm.20126

    Article  CAS  PubMed  Google Scholar 

  • Thomas G, Tacke R, Hedrick CC, Hanna RN (2015) Nonclassical patrolling monocyte function in the vasculature. Arterioscler Thromb Vasc Biol 35(6):1306–1316. doi:10.1161/ATVBAHA.114.304650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian Y, Gawlak G, O’Donnell JJ 3rd, Mambetsariev I, Birukova AA (2016) Modulation of endothelial inflammation by low and high magnitude cyclic stretch. PLoS One 11(4):e0153387. doi:10.1371/journal.pone.0153387

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsubota Y, Frey JM, Raines EW (2014) Novel ex vivo culture method for human monocytes uses shear flow to prevent total loss of transendothelial diapedesis function. J Leukoc Biol 95(1):191–195. doi:10.1189/jlb.0513272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ueno N, Harker KS, Clarke EV, McWhorter FY, Liu WF, Tenner AJ, Lodoen MB (2014) Real-time imaging of Toxoplasma-infected human monocytes under fluidic shear stress reveals rapid translocation of intracellular parasites across endothelial barriers. Cell Microbiol 16(4):580–595. doi:10.1111/cmi.12239

    Article  CAS  PubMed  Google Scholar 

  • Vaine CA, Patel MK, Zhu J, Lee E, Finberg RW, Hayward RC, Kurt-Jones EA (2013) Tuning innate immune activation by surface texturing of polymer microparticles: the role of shape in inflammasome activation. J Immunol 190(7):3525–3532. doi:10.4049/jimmunol.1200492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van den Dries K, van Helden SF, te Riet J, Diez-Ahedo R, Manzo C, Oud MM, van Leeuwen FN, Brock R, Garcia-Parajo MF, Cambi A, Figdor CG (2012) Geometry sensing by dendritic cells dictates spatial organization and PGE(2)-induced dissolution of podosomes. Cell Mol Life Sci CMLS 69(11):1889–1901. doi:10.1007/s00018-011-0908-y

    Article  PubMed  CAS  Google Scholar 

  • Wang HB, Dembo M, Wang YL (2000) Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol 279(5):C1345–C1350

    CAS  PubMed  Google Scholar 

  • Wang Y, Wang G, Luo X, Qiu J, Tang C (2012) Substrate stiffness regulates the proliferation, migration, and differentiation of epidermal cells. Burns 38(3):414–420. doi:10.1016/j.burns.2011.09.002

    Article  PubMed  Google Scholar 

  • Wang C, Baker BM, Chen CS, Schwartz MA (2013a) Endothelial cell sensing of flow direction. Arterioscler Thromb Vasc Biol 33(9):2130–2136. doi:10.1161/ATVBAHA.113.301826

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Yu X, Cao Q, Wang Y, Zheng G, Tan TK, Zhao H, Zhao Y, Wang Y, Harris D (2013b) Characterization of murine macrophages from bone marrow, spleen and peritoneum. BMC Immunol 14:6. doi:10.1186/1471-2172-14-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang P, Chen SH, Hung WC, Paul C, Zhu F, Guan PP, Huso DL, Kontrogianni-Konstantopoulos A, Konstantopoulos K (2015) Fluid shear promotes chondrosarcoma cell invasion by activating matrix metalloproteinase 12 via IGF-2 and VEGF signaling pathways. Oncogene 34(35):4558–4569. doi:10.1038/onc.2014.397

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Luu TU, Chen A, Khine M, Liu WF (2016) Topographical modulation of macrophage phenotype by shrink-film multi-scale wrinkles. Biomater Sci 4(6):948–952. doi:10.1039/c6bm00224b

    Article  CAS  PubMed  Google Scholar 

  • Wanjare M, Agarwal N, Gerecht S (2015) Biomechanical strain induces elastin and collagen production in human pluripotent stem cell-derived vascular smooth muscle cells. Am J Physiol Cell Physiol 309(4):C271–C281. doi:10.1152/ajpcell.00366.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wehner S, Buchholz BM, Schuchtrup S, Rocke A, Schaefer N, Lysson M, Hirner A, Kalff JC (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(5):G1187–G1197. doi:10.1152/ajpgi.00452.2009

    Article  CAS  PubMed  Google Scholar 

  • Wilkins JR, Pike DB, Gibson CC, Kubota A, Shiu YT (2014) Differential effects of cyclic stretch on bFGF- and VEGF-induced sprouting angiogenesis. Biotechnol Prog 30(4):879–888. doi:10.1002/btpr.1883

    Article  CAS  PubMed  Google Scholar 

  • Winer JP, Janmey PA, McCormick ME, Funaki M (2009) Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng A 15(1):147–154. doi:10.1089/ten.tea.2007.0388

    Article  CAS  Google Scholar 

  • Witkowska-Zimny M, Walenko K, Walkiewicz AE, Pojda Z, Przybylski J, Lewandowska-Szumiel M (2012) Effect of substrate stiffness on differentiation of umbilical cord stem cells. Acta Biochim Pol 59(2):261–264

    CAS  PubMed  Google Scholar 

  • Witkowska-Zimny M, Walenko K, Wrobel E, Mrowka P, Mikulska A, Przybylski J (2013) Effect of substrate stiffness on the osteogenic differentiation of bone marrow stem cells and bone-derived cells. Cell Biol Int 37(6):608–616. doi:10.1002/cbin.10078

    Article  CAS  PubMed  Google Scholar 

  • Wojciak-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(2):426–435. doi:10.1006/excr.1996.0098

    Article  CAS  PubMed  Google Scholar 

  • Wu CC, Li YS, Haga JH, Kaunas R, Chiu JJ, Su FC, Usami S, Chien S (2007) Directional shear flow and Rho activation prevent the endothelial cell apoptosis induced by micropatterned anisotropic geometry. Proc Natl Acad Sci USA 104(4):1254–1259. doi:10.1073/pnas.0609806104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu J, Yan Z, Schwartz DE, Yu J, Malik AB, Hu G (2013) Activation of NLRP3 inflammasome in alveolar macrophages contributes to mechanical stretch-induced lung inflammation and injury. J Immunol 190(7):3590–3599. doi:10.4049/jimmunol.1200860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wyss HM, Henderson JM, Byfield FJ, Bruggeman LA, Ding Y, Huang C, Suh JH, Franke T, Mele E, Pollak MR, Miner JH, Janmey PA, Weitz DA, Miller RT (2011) Biophysical properties of normal and diseased renal glomeruli. Am J Physiol Cell Physiol 300(3):C397–C405. doi:10.1152/ajpcell.00438.2010

    Article  CAS  PubMed  Google Scholar 

  • Xie J, Zhang Q, Zhu T, Zhang Y, Liu B, Xu J, Zhao H (2014) Substrate stiffness-regulated matrix metalloproteinase output in myocardial cells and cardiac fibroblasts: implications for myocardial fibrosis. Acta Biomater 10(6):2463–2472. doi:10.1016/j.actbio.2014.01.031

    Article  CAS  PubMed  Google Scholar 

  • Yanez-Soto B, Liliensiek SJ, Gasiorowski JZ, Murphy CJ, Nealey PF (2013) The influence of substrate topography on the migration of corneal epithelial wound borders. Biomaterials 34(37):9244–9251. doi:10.1016/j.biomaterials.2013.08.042

    Article  CAS  PubMed  Google Scholar 

  • 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. Development 126(13):3027–3033

    CAS  PubMed  Google Scholar 

  • Yang JH, Sakamoto H, Xu EC, Lee RT (2000) Biomechanical regulation of human monocyte/macrophage molecular function. Am J Pathol 156(5):1797–1804. doi:10.1016/S0002-9440(10)65051-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang K, Jung H, Lee HR, Lee JS, Kim SR, Song KY, Cheong E, Bang J, Im SG, Cho SW (2014) Multiscale, hierarchically patterned topography for directing human neural stem cells into functional neurons. ACS Nano 8(8):7809–7822. doi:10.1021/nn501182f

    Article  CAS  PubMed  Google Scholar 

  • Yang C, DelRio FW, Ma H, Killaars AR, Basta LP, Kyburz KA, Anseth KS (2016) Spatially patterned matrix elasticity directs stem cell fate. Proc Natl Acad Sci USA 113(31):E4439–E4445. doi:10.1073/pnas.1609731113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yerrapureddy A, Tobias J, Margulies SS (2010) Cyclic stretch magnitude and duration affect rat alveolar epithelial gene expression. Cell Physiol Biochem Int J Exp Cell Physiol Biochem Pharmacol 25(1):113–122. doi:10.1159/000272056

    Article  CAS  Google Scholar 

  • Yeung T, Georges PC, Flanagan LA, Marg B, Ortiz M, Funaki M, Zahir N, Ming W, Weaver V, Janmey PA (2005) Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil Cytoskeleton 60(1):24–34. doi:10.1002/cm.20041

    Article  PubMed  Google Scholar 

  • Yun JK, Anderson JM, Ziats NP (1999) Cyclic strain effects on human monocyte interactions with endothelial cells and extracellular matrix proteins. Tissue Eng 5(1):67–77. doi:10.1089/ten.1999.5.67

    Article  CAS  PubMed  Google Scholar 

  • Zhao F, Li L, Guan L, Yang H, Wu C, Liu Y (2014) Roles for GP IIb/IIIa and alphavbeta3 integrins in MDA-MB-231 cell invasion and shear flow-induced cancer cell mechanotransduction. Cancer Lett 344(1):62–73. doi:10.1016/j.canlet.2013.10.019

    Article  CAS  PubMed  Google Scholar 

  • Zustiak S, Nossal R, Sackett DL (2014) Multiwell stiffness assay for the study of cell responsiveness to cytotoxic drugs. Biotechnol Bioeng 111(2):396–403. doi:10.1002/bit.25097

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alessandra Cambi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Mennens, S.F.B., van den Dries, K., Cambi, A. (2017). Role for Mechanotransduction in Macrophage and Dendritic Cell Immunobiology. In: Kloc, M. (eds) Macrophages. Results and Problems in Cell Differentiation, vol 62. Springer, Cham. https://doi.org/10.1007/978-3-319-54090-0_9

Download citation

Publish with us

Policies and ethics