Macropinocytosis in Phagocyte Function and Immunity.
Antigen presentation
Cross-presentation
Dendritic cell
Endocytosis
Innate immunity
Macrophage
Macropinocytosis
Microbe-associated molecular pattern (MAMP)
Pattern recognition receptor (PRR)
Phagocyte
Pinocytosis
Journal
Sub-cellular biochemistry
ISSN: 0306-0225
Titre abrégé: Subcell Biochem
Pays: United States
ID NLM: 0316571
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
5
4
2022
pubmed:
6
4
2022
medline:
7
4
2022
Statut:
ppublish
Résumé
Phagocytes play critical roles in the maintenance of organismal homeostasis and immunity. Central to their role is their ability to take up and process exogenous material via the related processes of phagocytosis and macropinocytosis. The mechanisms and functions underlying macropinocytosis have remained severely understudied relative to phagocytosis. In recent years, however, there has been a renaissance in macropinocytosis research. Phagocytes can engage in various forms of macropinocytosis including an "induced" form and a "constitutive" form. This chapter, however, will focus on constitutive macropinocytosis and its role in the maintenance of immunity. Functions previously attributed to macropinocytosis, including antigen presentation and immune surveillance, will be revisited in light of recent revelations and emerging concepts will be highlighted.
Identifiants
pubmed: 35378705
doi: 10.1007/978-3-030-94004-1_6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
103-116Informations de copyright
© 2022. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Areschoug T, Gordon S (2009) Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell Microbiol 11:1160–1169. https://doi.org/10.1111/j.1462-5822.2009.01326.x
doi: 10.1111/j.1462-5822.2009.01326.x
pubmed: 19388903
Bielig H, Rompikuntal PK, Dongre M et al (2011) NOD-like receptor activation by outer membrane vesicles from vibrio cholerae non-O1 non-O139 strains is modulated by the quorum-sensing regulator HapR. Infect Immun 79:1418–1427. https://doi.org/10.1128/IAI.00754-10
doi: 10.1128/IAI.00754-10
pubmed: 21263023
pmcid: 3067550
Brubaker SW, Bonham KS, Zanoni I, Kagan JC (2015) Innate immune pattern recognition: a cell biological perspective. Annu Rev Immunol 33:257–290. https://doi.org/10.1146/annurev-immunol-032414-112240
doi: 10.1146/annurev-immunol-032414-112240
pubmed: 25581309
pmcid: 5146691
Burgdorf S, Lukacs-Kornek V, Kurts C (2006) The mannose receptor mediates uptake of soluble but not of cell-associated antigen for cross-presentation. J Immunol 176:6770–6776. https://doi.org/10.4049/jimmunol.176.11.6770
doi: 10.4049/jimmunol.176.11.6770
pubmed: 16709836
Calmette J, Bertrand M, Vétillard M et al (2016) Glucocorticoid-induced leucine zipper protein controls macropinocytosis in dendritic cells. J Immunol 197:4247–4256. https://doi.org/10.4049/jimmunol.1600561
doi: 10.4049/jimmunol.1600561
pubmed: 27793999
Cañas M-A, Fábrega M-J, Giménez R et al (2018) Outer membrane vesicles from probiotic and commensal Escherichia coli activate NOD1-mediated immune responses in intestinal epithelial cells. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.00498
Canton J (2018) Macropinocytosis: new insights into its underappreciated role in innate immune cell surveillance. Front Immunol 9. https://doi.org/10.3389/fimmu.2018.02286
Canton J, Neculai D, Grinstein S (2013) Scavenger receptors in homeostasis and immunity. Nat Rev Immunol 13:621–634. https://doi.org/10.1038/nri3515
doi: 10.1038/nri3515
pubmed: 23928573
Canton J, Schlam D, Breuer C et al (2016) Calcium-sensing receptors signal constitutive macropinocytosis and facilitate the uptake of NOD2 ligands in macrophages. Nat Commun 7:1–12. https://doi.org/10.1038/ncomms11284
doi: 10.1038/ncomms11284
Champion JA, Walker A, Mitragotri S (2008) Role of particle size in phagocytosis of polymeric microspheres. Pharm Res 25:1815–1821. https://doi.org/10.1007/s11095-008-9562-y
doi: 10.1007/s11095-008-9562-y
pubmed: 18373181
pmcid: 2793372
Charpentier JC, Chen D, Lapinski PE et al (2020) Macropinocytosis drives T cell growth by sustaining the activation of mTORC1. Nat Commun 11:1–9. https://doi.org/10.1038/s41467-019-13997-3
doi: 10.1038/s41467-019-13997-3
Chaturvedi A, Pierce SK (2009) How location governs toll-like receptor signaling. Traffic 10:621–628. https://doi.org/10.1111/j.1600-0854.2009.00899.x
doi: 10.1111/j.1600-0854.2009.00899.x
pubmed: 19302269
pmcid: 2741634
Chefalo PJ, Grandea AG, Kaer LV, Harding CV (2003) Tapasin−/− and TAP1−/− macrophages are deficient in vacuolar alternate class I MHC (MHC-I) processing due to decreased MHC-I stability at phagolysosomal pH. J Immunol 170:5825–5833. https://doi.org/10.4049/jimmunol.170.12.5825
doi: 10.4049/jimmunol.170.12.5825
pubmed: 12794107
Clayton EL, Cousin MA (2009) The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J Neurochem 111:901–914. https://doi.org/10.1111/j.1471-4159.2009.06384.x
doi: 10.1111/j.1471-4159.2009.06384.x
pubmed: 19765184
pmcid: 2871311
Conigrave AD (2016) The calcium-sensing receptor and the parathyroid: past, present, future. Front Physiol 7. https://doi.org/10.3389/fphys.2016.00563
de la Rosa DA, Canessa CM, Fyfe GK, Zhang P (2000) Structure and regulation of amiloride-sensitive sodium channels. Annu Rev Physiol 62:573–594. https://doi.org/10.1146/annurev.physiol.62.1.573
doi: 10.1146/annurev.physiol.62.1.573
De Vito P (2006) The sodium/hydrogen exchanger: a possible mediator of immunity. Cell Immunol 240:69–85. https://doi.org/10.1016/j.cellimm.2006.07.001
doi: 10.1016/j.cellimm.2006.07.001
pubmed: 16930575
Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. https://doi.org/10.1146/annurev.biochem.78.081307.110540
doi: 10.1146/annurev.biochem.78.081307.110540
pubmed: 19317650
Donaldson JG (2019) Macropinosome formation, maturation and membrane recycling: lessons from clathrin-independent endosomal membrane systems. Philos Trans R Soc B Biol Sci 374:20180148. https://doi.org/10.1098/rstb.2018.0148
doi: 10.1098/rstb.2018.0148
Doodnauth SA, Grinstein S, Maxson ME (2019) Constitutive and stimulated macropinocytosis in macrophages: roles in immunity and in the pathogenesis of atherosclerosis. Philos Trans R Soc B Biol Sci 374:20180147. https://doi.org/10.1098/rstb.2018.0147
doi: 10.1098/rstb.2018.0147
East L, Isacke CM (2002) The mannose receptor family. Biochim Biophys Acta (BBA) – General Subjects 1572:364–386. https://doi.org/10.1016/S0304-4165(02)00319-7
doi: 10.1016/S0304-4165(02)00319-7
Freeman SA, Uderhardt S, Saric A et al (2020) Lipid-gated monovalent ion fluxes regulate endocytic traffic and support immune surveillance. Science 367:301–305. https://doi.org/10.1126/science.aaw9544
doi: 10.1126/science.aaw9544
pubmed: 31806695
Garrett WS, Chen L-M, Kroschewski R et al (2000) Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102:325–334. https://doi.org/10.1016/S0092-8674(00)00038-6
doi: 10.1016/S0092-8674(00)00038-6
pubmed: 10975523
Guidi R, Levi L, Rouf SF et al (2013) Salmonella enterica delivers its genotoxin through outer membrane vesicles secreted from infected cells. Cell Microbiol 15:2034–2050. https://doi.org/10.1111/cmi.12172
doi: 10.1111/cmi.12172
pubmed: 23869968
Hackstein H, Steinschulte C, Fiedel S et al (2007) Sanglifehrin A blocks key dendritic cell functions in vivo and promotes long-term allograft survival together with low-dose CsA. Am J Transplant 7:789–798. https://doi.org/10.1111/j.1600-6143.2006.01729.x
doi: 10.1111/j.1600-6143.2006.01729.x
pubmed: 17391124
Hackstein H, Taner T, Logar AJ, Thomson AW (2002) Rapamycin inhibits macropinocytosis and mannose receptor–mediated endocytosis by bone marrow–derived dendritic cells. Blood 100:1084–1087. https://doi.org/10.1182/blood.V100.3.1084
doi: 10.1182/blood.V100.3.1084
pubmed: 12130531
Ira T, Jon WK, Jan B (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis. Circulation 116:1832–1844. https://doi.org/10.1161/CIRCULATIONAHA.106.676890
doi: 10.1161/CIRCULATIONAHA.106.676890
Koivusalo M, Welch C, Hayashi H et al (2010) Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 188:547–563. https://doi.org/10.1083/jcb.200908086
doi: 10.1083/jcb.200908086
pubmed: 20156964
pmcid: 2828922
Lee G-S, Subramanian N, Kim AI et al (2012) The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca 2+ and cAMP. Nature 492:123–127. https://doi.org/10.1038/nature11588
doi: 10.1038/nature11588
pubmed: 23143333
pmcid: 4175565
Lee J, Tattoli I, Wojtal KA et al (2009) pH-dependent internalization of muramyl peptides from early endosomes enables Nod1 and Nod2 signaling. J Biol Chem 284:23818–23829. https://doi.org/10.1074/jbc.M109.033670
doi: 10.1074/jbc.M109.033670
pubmed: 19570976
pmcid: 2749154
Leonard JN, Ghirlando R, Askins J et al (2008) The TLR3 signaling complex forms by cooperative receptor dimerization. PNAS 105:258–263. https://doi.org/10.1073/pnas.0710779105
doi: 10.1073/pnas.0710779105
pubmed: 18172197
pmcid: 2224197
Lewis WH (1937) Pinocytosis by malignant cells. Am J Cancer 29:666–679. https://doi.org/10.1158/ajc.1937.666
doi: 10.1158/ajc.1937.666
Lim JP, Teasdale RD, Gleeson PA (2012) SNX5 is essential for efficient macropinocytosis and antigen processing in primary macrophages. Biology Open 1:904–914. https://doi.org/10.1242/bio.20122204
doi: 10.1242/bio.20122204
pubmed: 23213485
pmcid: 3507233
Marques PE, Grinstein S, Freeman SA (2017) SnapShot: macropinocytosis. Cell 169:766–766.e1. https://doi.org/10.1016/j.cell.2017.04.031
doi: 10.1016/j.cell.2017.04.031
pubmed: 28475901
Masereel B, Pochet L, Laeckmann D (2003) An overview of inhibitors of Na+/H+ exchanger. Eur J Med Chem 38:547–554. https://doi.org/10.1016/S0223-5234(03)00100-4
doi: 10.1016/S0223-5234(03)00100-4
pubmed: 12832126
Moreau HD, Blanch-Mercader C, Attia R et al (2019) Macropinocytosis overcomes directional bias in dendritic cells due to hydraulic resistance and facilitates space exploration. Dev Cell 49:171–188.e5. https://doi.org/10.1016/j.devcel.2019.03.024
doi: 10.1016/j.devcel.2019.03.024
pubmed: 30982662
Nakamura N, Lill JR, Phung Q et al (2014) Endosomes are specialized platforms for bacterial sensing and NOD2 signalling. Nature 509:240–244. https://doi.org/10.1038/nature13133
doi: 10.1038/nature13133
pubmed: 24695226
Norbury CC, Chambers BJ, Prescott AR et al (1997) Constitutive macropinocytosis allows TAP-dependent major histocompatibility compex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 27:280–288. https://doi.org/10.1002/eji.1830270141
doi: 10.1002/eji.1830270141
pubmed: 9022030
Olszak IT, Poznansky MC, Evans RH et al (2000) Extracellular calcium elicits a chemokinetic response from monocytes in vitro and in vivo. J Clin Invest 105:1299–1305. https://doi.org/10.1172/JCI9799
doi: 10.1172/JCI9799
pubmed: 10792005
pmcid: 315448
Orlowski J, Grinstein S (2011) Na+/H+ exchangers. In: Comprehensive physiology. American Cancer Society, pp 2083–2100
doi: 10.1002/cphy.c110020
Prentice-Mott HV, Chang C-H, Mahadevan L et al (2013) Biased migration of confined neutrophil-like cells in asymmetric hydraulic environments. Proc Natl Acad Sci U S A 110:21006–21011. https://doi.org/10.1073/pnas.1317441110
doi: 10.1073/pnas.1317441110
pubmed: 24324148
pmcid: 3876268
Racoosin EL, Swanson JA (1993) Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 121:1011–1020. https://doi.org/10.1083/jcb.121.5.1011
doi: 10.1083/jcb.121.5.1011
pubmed: 8099075
Redka DS, Gütschow M, Grinstein S, Canton J (2018) Differential ability of proinflammatory and anti-inflammatory macrophages to perform macropinocytosis. MBoC 29:53–65. https://doi.org/10.1091/mbc.E17-06-0419
doi: 10.1091/mbc.E17-06-0419
pubmed: 29093026
pmcid: 5746066
Roier S, Zingl FG, Cakar F et al (2016) A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria. Nat Commun 7:1–13. https://doi.org/10.1038/ncomms10515
doi: 10.1038/ncomms10515
Rosales-Reyes R, Pérez-López A, Sánchez-Gómez C et al (2012) Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival. Microb Pathog 52:367–374. https://doi.org/10.1016/j.micpath.2012.03.007
doi: 10.1016/j.micpath.2012.03.007
pubmed: 22475626
Sallusto F, Cella M, Danieli C, Lanzavecchia A (1995) Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 182:389–400. https://doi.org/10.1084/jem.182.2.389
doi: 10.1084/jem.182.2.389
pubmed: 7629501
Sarkar K, Kruhlak MJ, Erlandsen SL, Shaw S (2005) Selective inhibition by rottlerin of macropinocytosis in monocyte-derived dendritic cells. Immunology 116:513–524. https://doi.org/10.1111/j.1365-2567.2005.02253.x
doi: 10.1111/j.1365-2567.2005.02253.x
pubmed: 16313365
pmcid: 1802442
Schlam D, Bagshaw RD, Freeman SA et al (2015) Phosphoinositide 3-kinase enables phagocytosis of large particles by terminating actin assembly through Rac/Cdc42 GTPase-activating proteins. Nat Commun 6:1–12. https://doi.org/10.1038/ncomms9623
doi: 10.1038/ncomms9623
Schlam D, Canton J (2016) Every day I’m rufflin’: calcium sensing and actin dynamics in the growth factor-independent membrane ruffling of professional phagocytes. Small GTPases 8:65–70. https://doi.org/10.1080/21541248.2016.1197873
doi: 10.1080/21541248.2016.1197873
pubmed: 27267709
pmcid: 5464118
Singla B, Ghoshal P, Lin H et al (2018) PKCδ-mediated Nox2 activation promotes fluid-phase pinocytosis of antigens by immature dendritic cells. Front Immunol 9. https://doi.org/10.3389/fimmu.2018.00537
Sorvillo N, Pos W, van den Berg LM et al (2012) The macrophage mannose receptor promotes uptake of ADAMTS13 by dendritic cells. Blood 119:3828–3835. https://doi.org/10.1182/blood-2011-09-377754
doi: 10.1182/blood-2011-09-377754
pubmed: 22289891
Steinman RM, Brodie SE, Cohn ZA (1976) Membrane flow during pinocytosis. A stereologic analysis. J Cell Biol 68:665–687. https://doi.org/10.1083/jcb.68.3.665
doi: 10.1083/jcb.68.3.665
pubmed: 1030706
Swanson JA, King JS (2019) The breadth of macropinocytosis research. Philos Trans R Soc B Biol Sci 374:20180146. https://doi.org/10.1098/rstb.2018.0146
doi: 10.1098/rstb.2018.0146
Uderhardt S, Martins AJ, Tsang JS et al (2019) Resident macrophages cloak tissue microlesions to prevent neutrophil-driven inflammatory damage. Cell 177:541–555.e17. https://doi.org/10.1016/j.cell.2019.02.028
doi: 10.1016/j.cell.2019.02.028
pubmed: 30955887
pmcid: 6474841
Vanaja SK, Russo AJ, Behl B et al (2016) Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell 165:1106–1119. https://doi.org/10.1016/j.cell.2016.04.015
doi: 10.1016/j.cell.2016.04.015
pubmed: 27156449
pmcid: 4874922
von Delwig A, Hilkens CM, Altmann DM et al (2006) Inhibition of macropinocytosis blocks antigen presentation of type II collagen in vitro and in vivoin HLA-DR1 transgenic mice. Arthritis Res Therapy 8:R93. https://doi.org/10.1186/ar1964
doi: 10.1186/ar1964
West MA, Prescott AR, Eskelinen E-L et al (2000) Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 10:839–848. https://doi.org/10.1016/S0960-9822(00)00595-9
doi: 10.1016/S0960-9822(00)00595-9
pubmed: 10899002
West MA, Wallin RPA, Matthews SP et al (2004) Enhanced dendritic cell antigen capture via toll-like receptor-induced actin remodeling. Science 305:1153–1157. https://doi.org/10.1126/science.1099153
doi: 10.1126/science.1099153
pubmed: 15326355
Yoshida S, Pacitto R, Sesi C et al (2018) Dorsal ruffles enhance activation of Akt by growth factors. J Cell Sci 131. https://doi.org/10.1242/jcs.220517
Zindel J, Kubes P (2020) DAMPs, PAMPs, and LAMPs in immunity and sterile inflammation. Annu Rev Pathol: Mechanisms Disease 15:493–518. https://doi.org/10.1146/annurev-pathmechdis-012419-032847
doi: 10.1146/annurev-pathmechdis-012419-032847