Skip to main content

Macrophages: First Innate Immune Responders to Nanomaterials

  • Chapter
  • First Online:
Interaction of Nanomaterials with the Immune System

Part of the book series: Molecular and Integrative Toxicology ((MOLECUL))

Abstract

Macrophages are professional phagocytes that play key roles in immune surveillance and host defense against a variety of external stimuli, including engineered nanomaterials (ENMs). Physicochemical characteristics of ENMs such as size, shape, and surface charge are factors that determine macrophage recognition and uptake through various endocytotic mechanisms. Moreover, toll-like receptors (TLRs) and scavenger receptors (SRs) on the surface of macrophages facilitate binding, uptake, and intracellular signaling in response to specific types of ENMs. Biocorona formation further modulates the interaction of ENMs with cell-surface receptors. The immune response of macrophages to ENMs, including inflammasome activation and alternative polarization, plays important roles in immune-mediated diseases such as fibrosis, asthma, and cancer.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Arredouani MS, Palecanda A, Koziel H, Huang YC, Imrich A, Sulahian TH, Ning YY, Yang Z, Pikkarainen T, Sankala M, Vargas SO, Takeya M, Tryggvason K, Kobzik L. MARCO is the major binding receptor for unopsonized particles and bacteria on human alveolar macrophages. J Immunol. 2005;175(9):6058–64.

    Article  CAS  PubMed  Google Scholar 

  • Bartneck M, Ritz T, Keul HA, Wambach M, Bornemann J, Gbureck U, Ehling J, Lammers T, Heymann F, Gassler N, Lüdde T, Trautwein C, Groll J, Tacke F. Peptide-functionalized gold nanorods increase liver injury in hepatitis. ACS Nano. 2012;6(10):8767–77.

    Article  CAS  PubMed  Google Scholar 

  • Bianchi MG, Allegri M, Costa AL, et al. Titanium dioxide nanoparticles enhance macrophage activation by LPS through a TLR4-dependent intracellular pathway. Toxicol Res (Camb). 2015;4:385–98.

    Article  CAS  Google Scholar 

  • Biondo C, Mancuso G, Midiri A, Signorino G, Domina M, Lanza Cariccio V, Venza M, Venza I, Teti G, Beninati C. Essential role of interleukin-1 signaling in host defenses against group B streptococcus. MBio. 2014;5(5):e01428–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boraschi D, Italiani P, Palomba R, Decuzzi P, Duschl A, Fadeel B, Moghimi SM. Nanoparticles and innate immunity: new perspectives on host defence. Semin Immunol. 2017;34:33–51.

    Article  CAS  PubMed  Google Scholar 

  • Brown MS, Goldstein JL. Receptor-mediated endocytosis: insights from the lipoprotein receptor system. Proc Natl Acad Sci U S A. 1979;76(7):3330–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calkins CM, Bensard DD, Shames BD, Pulido EJ, Abraham E, Fernandez N, Meng X, Dinarello CA, McIntyre RC Jr. IL-1 regulates in vivo C-X-C chemokine induction and neutrophil sequestration following endotoxemia. J Endotoxin Res. 2002;8(1):59–67.

    CAS  PubMed  Google Scholar 

  • Canton J, Neculai D, Grinstein S. Scavenger receptors in homeostasis and immunity. Nat Rev Immunol. 2013;13(9):621–34.

    Article  CAS  PubMed  Google Scholar 

  • Chan TK, Tan WSD, Peh HY, Wong WSF. Aeroallergens induce reactive oxygen species production and DNA damage and dampen antioxidant responses in bronchial epithelial cells. J Immunol. 2017;199:39–47.

    Article  CAS  PubMed  Google Scholar 

  • Cornwell WD, Kim V, Fan X, Vega ME, Ramsey FV, Criner GJ, Rogers TJ. Activation and polarization of circulating monocytes in severe chronic obstructive pulmonary disease. BMC Pulm Med. 2018;18(1):101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies LC, Rice CM, McVicar DW, Weiss JM. Diversity and environmental adaptation of phagocytic cell metabolism. Journal of Leukocyte Biology. 2018;105(1):37–48

    Google Scholar 

  • Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, Alexander A. Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci. 2006;92(1):5–22.

    Article  CAS  PubMed  Google Scholar 

  • Duke KS, Bonner JC. Mechanisms of carbon nanotube-induced pulmonary fibrosis: a physicochemical characteristic perspective. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2018;10(3):e1498.

    PubMed  Google Scholar 

  • Elomaa O, Kangas M, Sahlberg C, Tuukkanen J, Sormunen R, Liakka A, Thesleff I, Kraal G, Tryggvason K. Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell. 1995;80(4):603–9.

    Article  CAS  PubMed  Google Scholar 

  • Feiner-Gracia N, Beck M, Pujals S, Tosi S, Mandal T, Buske C, Linden M, Albertazzi L. Super-resolution microscopy unveils dynamic heterogeneities in nanoparticle protein corona. Small. 2017;13(41):1701631.

    Article  CAS  Google Scholar 

  • Fleischer CC, Payne CK. Nanoparticle–cell interactions: molecular structure of the protein corona and cellular outcomes. Acc Chem Res. 2014a;47(8):2651–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleischer CC, Payne CK. Secondary structure of corona proteins determines the cell surface receptors used by nanoparticles. J Phys Chem B. 2014b;118(49):14017–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabehart K, Correll KA, Loader JE, White CW, Dakhama A. The lung response to ozone is determined by age and is partially dependent on Toll-like receptor 4. Respir Res. 2015;16:117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao N, Zhang Q, Mu Q, Bai Y, Li L, Zhou H, Butch ER, Powell TB, Snyder SE, Jiang G, Yan B. Steering carbon nanotubes to scavenger receptor recognition by nanotube surface chemistry modification partially alleviates NFκB activation and reduces its immunotoxicity. ACS Nano. 2011;5(6):4581–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garapaty A, Champion JA. Tunable particles alter macrophage uptake based on combinatorial effects of physical properties. Bioeng Transl Med. 2017;2(1):92–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giovanni M, Yue J, Zhang L, Xie J, Ong CN, Leong DT. Pro-inflammatory responses of RAW264.7 macrophages when treated with ultralow concentrations of silver, titanium dioxide, and zinc oxide nanoparticles. J Hazard Mater. 2015;297:146–52.

    Article  CAS  PubMed  Google Scholar 

  • Girtsman TA, Beamer CA, Wu N, Buford M, Holian A. IL-1R signaling is critical for regulation of multi-walled carbon nanotubes-induced acute lung inflammation in C57Bl/6 mice. Nanotoxicology. 2014;8(1):17–27.

    Article  CAS  PubMed  Google Scholar 

  • Glista-Baker EE, Taylor AJ, Sayers BC, Thompson EA, Bonner JC. Nickel nanoparticles enhance platelet-derived growth factor-induced chemokine expression by mesothelial cells via prolonged mitogen-activated protein kinase activation. Am J Respir Cell Mol Biol. 2012;47(4):552–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity. 2010;32(5):593–604.

    Article  CAS  PubMed  Google Scholar 

  • Gough PJ, Gordon S. The role of scavenger receptors in the innate immune system. Microbes Infect. 2000;2(3):305–11.

    Article  CAS  PubMed  Google Scholar 

  • Gwinn MR, Vallyathan V. Respiratory burst: role in signal transduction in alveolar macrophages. J Toxicol Environ Health B Crit Rev. 2006;9(1):27–39.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton RF, de Villiers WJS, Holian A. Class A type II scavenger receptor mediates silica-induced apoptosis in Chinese hamster ovary cell line. Toxicol Appl Pharmacol. 2000;162(2):100–6.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton RF Jr, Thakur SA, Mayfair JK, Holian A. MARCO mediates silica uptake and toxicity in alveolar macrophages from C57BL/6 mice. J Biol Chem. 2006;281(45):34218–26.

    Article  CAS  PubMed  Google Scholar 

  • Heit B, Kim H, Cosío G, Castaño D, Collins R, Lowell CA, Kain KC, Trimble WS, Grinstein S. Multimolecular signaling complexes enable Syk-mediated signaling of CD36 internalization. Dev Cell. 2013;24(4):372–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirano S, Fujitani Y, Furuyama A, Kanno S. Macrophage receptor with collagenous structure (MARCO) is a dynamic adhesive molecule that enhances uptake of carbon nanotubes by CHO-K1 cells. Toxicol Appl Pharmacol. 2012;259(1):96–103.

    Article  CAS  PubMed  Google Scholar 

  • Holian A, Scheule RK. Alveolar macrophage biology. Hosp Pract (Off Ed). 1990;25(12):53–62.

    Article  CAS  Google Scholar 

  • Huang C, Sun M, Yang Y, Wang F, Ma X, Li J, Wang Y, Ding Q, Ying H, Song H, Wu Y, Jiang Y, Jia X, Ba Q, Wang H. Titanium dioxide nanoparticles prime a specific activation state of macrophages. Nanotoxicology. 2017;11(6):737–50.

    PubMed  Google Scholar 

  • Hussell T, Bell TJ. Alveolar macrophages: plasticity in a tissue-specific context. Nat Rev Immunol. 2014;14(2):81–93.

    Article  CAS  PubMed  Google Scholar 

  • Janssen WJ, Barthel L, Muldrow A, Oberley-Deegan RE, Kearns MT, Jakubzick C, Henson PM. Fas determines differential fates of resident and recruited macrophages during resolution of acute lung injury. Am J Respir Crit Care Med. 2011;184(5):547–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jayaram DT, Runa S, Kemp ML, Payne CK. Nanoparticle-induced oxidation of corona proteins initiates an oxidative stress response in cells. Nanoscale. 2017;9(22):7595–601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanno S, Furuyama A, Hirano S. A murine scavenger receptor MARCO recognizes polystyrene nanoparticles. Toxicol Sci. 2007;97(2):398–406.

    Article  CAS  PubMed  Google Scholar 

  • Kedmi R, Ben-Arie N, Peer D. The systemic toxicity of positively charged lipid nanoparticles and the role of Toll-like receptor 4 in immune activation. Biomaterials. 2010;31(26):6867–75.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn DA, Vanhecke D, Michen B, Blank F, Gehr P, Petri-Fink A, Rothen-Rutishauser B. Different endocytotic uptake mechanisms for nanoparticles in epithelial cells and macrophages. Beilstein J Nanotechnol. 2014;5:1625–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzmich NN, Sivak KV, Chubarev VN, Porozov YB, Savateeva-Lyubimova TN, Peri F. TLR4 Signaling pathway modulators as potential therapeutics in inflammation and sepsis. Vaccines (Basel). 2017;5(4):34.

    Article  CAS  Google Scholar 

  • Lee JK, Sayers BC, Chun KS, Lao HC, Shipley-Phillips JK, Bonner JC, Langenbach R. Multi-walled carbon nanotubes induce COX-2 and iNOS expression via MAP kinase-dependent and -independent mechanisms in mouse RAW264.7 macrophages. Part Fibre Toxicol. 2012;9:14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Light WG, Wei ET. Surface charge and asbestos toxicity. Nature. 1977;265(5594):537–9.

    Article  CAS  PubMed  Google Scholar 

  • Lonez C, Irvine KL, Pizzuto M, et al. Critical residues involved in Toll-like receptor 4 activation by cationic lipid nanocarriers are not located at the lipopolysaccharide-binding interface. Cell Mol Life Sci. 2015;72(20):3971–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lunov O, Zablotskii V, Syrovets T, Röcker C, Tron K, Nienhaus GU, Simmet T. Modeling receptor-mediated endocytosis of polymer-functionalized iron oxide nanoparticles by human macrophages. Biomaterials. 2011;32(2):547–55.

    Article  CAS  PubMed  Google Scholar 

  • Ma J, Liu R, Wang X, Liu Q, Chen Y, Valle RP, Zuo YY, Xia T, Liu S. Crucial role of lateral size for graphene oxide in activating macrophages and stimulating pro-inflammatory responses in cells and animals. ACS Nano. 2015;9(10):10498–515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma J, Li R, Qu G, et al. Carbon nanotubes stimulate synovial inflammation through inducing systemic pro-inflammatory cytokines. Nanoscale. 2016;8:18070–86.

    Article  CAS  PubMed  Google Scholar 

  • Mangum JB, Turpin EA, Antao-Menezes A, Cesta MF, Bermudez E, Bonner JC. Single-walled carbon nanotube (SWCNT)-induced interstitial fibrosis in the lungs of rats is associated with increased levels of PDGF mRNA and the formation of unique intercellular carbon structures that bridge alveolar macrophages in situ. Part Fibre Toxicol. 2006;3:15.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci. 2008;13:453–61.

    Article  CAS  PubMed  Google Scholar 

  • Martinon F, Mayor A, Tschopp J. The inflammasomes: guardians of the body. Annu Rev Immunol. 2009;27:229–65.

    Article  CAS  PubMed  Google Scholar 

  • Maus UA, Janzen S, Wall G, Srivastava M, Blackwell TS, Christman JW, Seeger W, Welte T, Lohmeyer J. Resident alveolar macrophages are replaced by recruited monocytes in response to endotoxin-induced lung inflammation. Am J Respir Cell Mol Biol. 2006;35(2):227–35.

    Article  CAS  PubMed  Google Scholar 

  • Meunier E, Coste A, Olagnier D, et al. Double-walled carbon nanotubes trigger IL-1β release in human monocytes through Nlrp3 inflammasome activation. Nanomedicine. 2012;8(6):987–95.

    Article  CAS  PubMed  Google Scholar 

  • Melgert BN, ten Hacken NH, Rutgers B, Timens W, Postma DS, Hylkema MN. More alternative activation of macrophages in lungs of asthmatic patients. Journal of Allergy and Clinical Immunology. 2011;127(3):831–833

    Google Scholar 

  • Miao X, Leng X, Zhang Q. The current state of nanoparticle-induced macrophage polarization and reprogramming research. Int J Mol Sci. 2017;18(2):pii: E336.

    Article  CAS  Google Scholar 

  • Miller SI, Ernst RK, Bader MW. LPS, TLR4 and infectious disease diversity. Nat Rev Microbiol. 2005;3:36–46.

    Article  CAS  PubMed  Google Scholar 

  • Miller LS, Pietras EM, Uricchio LH, Hirano K, Rao S, Lin H, O’Connell RM, Iwakura Y, Cheung AL, Cheng G, Modlin RL. Inflammasome-mediated production of IL-1beta is required for neutrophil recruitment against Staphylococcus aureus in vivo. J Immunol. 2007;179(10):6933–42.

    Article  CAS  PubMed  Google Scholar 

  • Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal. 2014;20(7):1126–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Bombelli FB, Dawson KA. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc. 2011;133(8):2525–34.

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee SP, Bondarenko O, Kohonen P, et al. Macrophage sensing of single-walled carbon nanotubes via Toll-like receptors. Sci Rep. 2018;8:1115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy JE, Tedbury PR, Homer-Vanniasinkam S, Walker JH, Ponnambalam S. Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis. 2005;182(1):1–15.

    Article  CAS  PubMed  Google Scholar 

  • Murthy S, Larson-Casey JL, Ryan AJ, He C, Kobzik L, Carter AB. Alternative activation of macrophages and pulmonary fibrosis are modulated by scavenger receptor, macrophage receptor with collagenous structure. FASEB J. 2015;29(8):3527–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oberdörster G, Ferin J, Gelein R, Soderholm SC, Finkelstein J. Role of the alveolar macrophage in lung injury: studies with ultrafine particles. Environ Health Perspect. 1992;97:193–9.

    PubMed  PubMed Central  Google Scholar 

  • Oberdörster G, Ferin J, Lehnert BE. Correlation between particle size, in vivo particle persistence, and lung injury. Environ Health Perspect. 1994;102(Suppl 5):173–9.

    PubMed  PubMed Central  Google Scholar 

  • Oblak A, Pohar J, Jerala R. MD-2 determinants of nickel and cobalt-mediated activation of human TLR4. PLoS One. 2015;10(3):e0120583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palomäki J, Välimäki E, Sund J, Vippola M, Clausen PA, Jensen KA, Savolainen K, Matikainen S, Alenius H. Long, needle-like carbon nanotubes and asbestos activate the NLRP3 inflammasome through a similar mechanism. ACS Nano. 2011;5(9):6861–70.

    Article  CAS  PubMed  Google Scholar 

  • Pampaloni F, Florin EL. Microtubule architecture: inspiration for novel carbon nanotube-based biomimetic materials. Trends Biotechnol. 2008;26(6):302–10.

    Article  CAS  PubMed  Google Scholar 

  • Patra A, Ding T, Engudar G, Wang Y, Dykas MM, Liedberg B, Kah JC, Venkatesan T, Drum CL. Component-specific analysis of plasma protein corona formation on gold nanoparticles using multiplexed surface plasmon resonance. Small. 2016;12(9):1174–82.

    Article  CAS  PubMed  Google Scholar 

  • Paul D, Achouri S, Yoon YZ, Herre J, Bryant CE, Cicuta P. Phagocytosis dynamics depends on target shape. Biophys J. 2013;105(5):1143–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrarca C, Clemente E, Amato V, Pedata P, Sabbioni E, Bernardini G, Iavicoli I, Cortese S, Niu Q, Otsuki T, Paganelli R, Di Gioacchino M. Engineered metal based nanoparticles and innate immunity. Clin Mol Allergy. 2015;13:13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pluddemann A, Neyen C, Gordon S. Macrophage scavenger receptors and host-derived ligands. Methods. 2007;43(3):207–17.

    Article  CAS  PubMed  Google Scholar 

  • Pluddemann A, Mukhopadhyay S, Sankala M, Savino S, Pizza M, Rappuoli R, Tryggvason K, Gordon S. SR-A, MARCO and TLRs differentially recognise selected surface proteins from Neisseria meningitidis: an example of fine specificity in microbial ligand recognition by innate immune receptors. J Innate Immun. 2009;1(2):153–63.

    Article  CAS  PubMed  Google Scholar 

  • Potnis PA, Dutta DK, Wood SC. Toll-like receptor 4 signaling pathway mediates proinflammatory immune response to cobalt-alloy particles. Cell Immunol. 2013;282:53–65.

    Article  CAS  PubMed  Google Scholar 

  • Raghavan B, Martin SF, Esser PR, Goebeler M, Schmidt M. Metal allergens nickel and cobalt facilitate TLR4 homodimerization independently of MD2. EMBO Rep. 2012;13(12):1109–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raynal I, Prigent P, Peyramaure S, Najid A, Rebuzzi C, Corot C. Macrophage endocytosis of superparamagnetic iron oxide nanoparticles: mechanisms and comparison of ferumoxides and ferumoxtran-10. Investig Radiol. 2004;39(1):56–63.

    Article  CAS  Google Scholar 

  • Resnick D, Freedman NJ, Xu S, Krieger M. Secreted extracellular domains of macrophage scavenger receptors form elongated trimers which specifically bind crocidolite asbestos. J Biol Chem. 1993;268(5):3538–45.

    CAS  PubMed  Google Scholar 

  • Runa S, Hussey M, Payne CK. Nanoparticle-cell interactions: relevance for public health. J Phys Chem B. 2018;122(3):1009–16.

    Article  CAS  PubMed  Google Scholar 

  • Ryman-Rasmussen JP, Cesta MF, Brody AR, Shipley-Phillips JK, Everitt JI, Tewksbury EW, Moss OR, Wong BA, Dodd DE, Andersen ME, Bonner JC. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat Nanotechnol. 2009;4(11):747–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samet JM, Tal TL. Toxicological disruption of signaling homeostasis: tyrosine phosphatases as targets. Annu Rev Pharmacol Toxicol. 2010;50:215–35.

    Article  CAS  PubMed  Google Scholar 

  • Sargent LM, Shvedova AA, Hubbs AF, Salisbury JL, Benkovic SA, Kashon ML, et al. Induction of aneuploidy by single-walled carbon nanotubes. Environ Mol Mutagen. 2009;50(8):708–17.

    Article  CAS  PubMed  Google Scholar 

  • Sayan M, Mossman BT. The NLRP3 inflammasome in pathogenic particle and fibre-associated lung inflammation and diseases. Part Fibre Toxicol. 2016;13(1):51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt M, Goebeler M. Nickel allergies: paying the Toll for innate immunity. J Mol Med. 2011;89:961–70.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt M, Raghavan B, Müller V, Vogl T. Crucial role for human Toll-like receptor 4 in the development of contact allergy to nickel. Nat Immunol. 2010;11:814–9.

    Article  CAS  PubMed  Google Scholar 

  • Shannahan JH, Fritz KS, Raghavendra AJ, Podila R, Persaud I, Brown JM. Formation of a protein corona on silver nanoparticles mediates cellular toxicity via scavenger receptors. Toxicol Sci. 2015;143(1):136–46.

    Article  CAS  PubMed  Google Scholar 

  • Shaykhiev R, Krause A, Salit J, Strulovici-Barel Y, Harvey BG, O’Connor TP, Crystal RG. Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J Immunol. 2009;183(4):2867–83.

    Article  CAS  PubMed  Google Scholar 

  • Shipkowski KA, Taylor AJ, Thompson EA, Glista-Baker EE, Sayers BC, Messenger ZJ, Bauer RN, Jaspers I, Bonner JC. An allergic lung microenvironment suppresses carbon nanotube-induced inflammasome activation via STAT6-dependent inhibition of caspase-1. PLoS One. 2015;10(6):e0128888.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shvedova AA, Fabisiak JP, Kisin ER, Murray AR, Roberts JR, Tyurina YY, Antonini JM, Feng WH, Kommineni C, Reynolds J, Barchowsky A, Castranova V, Kagan VE. Sequential exposure to carbon nanotubes and bacteria enhances pulmonary inflammation. Am J Respir Cell Mol Biol. 2008;38(5):579–90.

    Article  CAS  PubMed  Google Scholar 

  • Singh RP, Ramarao P. Cellular uptake, intracellular trafficking and cytotoxicity of silver nanoparticles. Toxicol Lett. 2012;213(2):249–59.

    Article  CAS  PubMed  Google Scholar 

  • Sosale NG, Spinler KR, Alvey C, Discher DE. 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. 2015;35:107–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strowig T, Henao-Mejia J, Elinav E, et al. Inflammasomes in health and disease. Nature. 2012;481(7381):278–86.

    Article  CAS  PubMed  Google Scholar 

  • Sun B, Wang X, Ji Z, Wang M, Liao YP, Chang CH, Li R, Zhang H, Nel AE, Xia T. NADPH oxidase-dependent NLRP3 inflammasome activation and its important role in lung fibrosis by multiwalled carbon nanotubes. Small. 2015;11(17):2087–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thakur SA, Hamilton RF Jr, Holian A. Role of scavenger receptor a family in lung inflammation from exposure to environmental particles. J Immunotoxicol. 2008;5(2):151–7.

    Article  CAS  PubMed  Google Scholar 

  • Thakur SA, Hamilton R, Pikkarainen T, Holian A. Differential binding of inorganic particles to MARCO. Toxicological Sciences. Toxicol Sci. 2009;107(1):238–246

    Google Scholar 

  • Thomas DC. The phagocyte respiratory burst: historical perspectives and recent advances. Immunol Lett. 2017;192:88–96.

    Article  CAS  PubMed  Google Scholar 

  • Thompson EA, Sayers BC, Glista-Baker EE, Sipkowski KA, Taylor AJ, Bonner JC. Innate immune responses to nanoparticle exposure in the lung. J Environ Immunol Toxicol. 2014;1(3):150–6.

    PubMed  PubMed Central  Google Scholar 

  • Tsugita M, Morimoto N, Tashiro M, Kinoshita K, Nakayama M. SR-B1 is a silica receptor that mediates canonical inflammasome activation. Cell Rep. 2017;18(5):1298–311.

    Article  CAS  PubMed  Google Scholar 

  • Turabekova M, Rasulev B, Theodore M, Jackman J, Leszcynska D, Leszczynski J. Immunotoxicity of nanoparticles: computational study suggests that CNTs and C60 fullerenes might be recognized as pathogens by Toll-like receptors. Nanoscale. 2014;6:3488.

    Article  CAS  PubMed  Google Scholar 

  • van der Laan LJ, Döpp EA, Haworth R, Pikkarainen T, Kangas M, Elomaa O, Dijkstra CD, Gordon S, Tryggvason K, Kraal G. Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J Immunol. 1999;162(2):939–47.

    PubMed  Google Scholar 

  • Walling BE, Kuang Z, Hao Y, Estrada D, Wood JD, Lian F, Miller LA, Shah AB, Jeffries JL, Haasch RT, Lyding JW, Pop E, Lau GW. Helical carbon nanotubes enhance the early immune response and inhibit macrophage-mediated phagocytosis of Pseudomonas aeruginosa. PLoS One. 2013;8(11):e80283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Tassiulas I, Park-Min KH, Reid AC, Gil-Henn H, Schlessinger J, Baron R, Zhang JJ, Ivashkiv LB. ‘Tuning’ of type I interferon-induced Jak-STAT1 signaling by calcium-dependent kinases in macrophages. Nat Immunol. 2008;9(2):186–93.

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Guo J, Chen T, Nie H, Wang H, Zang J, Cui X, Jia G. Multi-walled carbon nanotubes induce apoptosis via mitochondrial pathway and scavenger receptor. Toxicol In Vitro. 2012;26(6):799–806.

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Ren T, Xiao C, Li H, Wu T. Nickel promotes the invasive potential of human lung cancer cells via TLR4/MyD88 signaling. Toxicology. 2011;285:25–30.

    Article  CAS  PubMed  Google Scholar 

  • Yang RB, Mark MR, Gray A, et al. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signaling. Nature. 1998;395:284–8.

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Ha T, Liu L, Wang X, Gao M, Kelley J, Kao R, Williams D, Li C. Scavenger receptor A (SR-A) is required for LPS-induced TLR4 mediated NF-κB activation in macrophages. Biochim Biophys Acta. 2012;1823(7):1192–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zani IA, Stephen SL, Mughal NA, Russell D, Homer-Vanniasinkam S, Wheatcroft SB, Ponnambalam S. Scavenger receptor structure and function in health and disease. Cell. 2015;4(2):178–201.

    Article  CAS  Google Scholar 

  • Zong G, Zhu Y, Zhang Y, Wang Y, Bai H, Yang Q, Ben J, Zhang H, Li X, Zhu X, Chen Q. SR-A1 suppresses colon inflammation and tumorigenesis through negative regulation of NF-κB signaling. Biochem Pharmacol. 2018;154:335–43.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James C. Bonner .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

You, D.J., Lee, H.Y., Bonner, J.C. (2020). Macrophages: First Innate Immune Responders to Nanomaterials. In: Bonner, J., Brown, J. (eds) Interaction of Nanomaterials with the Immune System. Molecular and Integrative Toxicology. Springer, Cham. https://doi.org/10.1007/978-3-030-33962-3_2

Download citation

Publish with us

Policies and ethics