Cited by 24Phagocytosis and Immune RegulationImmunotherapy and Immune ResponsesImmune Response and Inflammation

Efferocytosis in dendritic cells: an overlooked immunoregulatory process

Open access
Ma, Yanyan, Jiang, Tangxing, Zhu, Xun, Xu, Yizhou, Wan, Ke, Zhang, Tingxuan, Xie, Miaorong·2024·Frontiers in Immunology

Abstract

Efferocytosis, the process of engulfing and removing apoptotic cells, plays an essential role in preserving tissue health and averting undue inflammation. While macrophages are primarily known for this task, dendritic cells (DCs) also play a significant role. This review delves into the unique contributions of various DC subsets to efferocytosis, highlighting the distinctions in how DCs and macrophages recognize and handle apoptotic cells. It further explores how efferocytosis influences DC maturation, thereby affecting immune tolerance. This underscores the pivotal role of DCs in orchestrating immune responses and sustaining immune equilibrium, providing new insights into their function in immune regulation.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fimmu.2024.1415573

Cites

22 of 22 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Efferocytosis is seen as a major hurdle to using antigen presenting cells in cell-based therapies.

    “It is seen as a major hurdle to using antigen presenting cells in cell-based therapies (61–64).”

    From Cholesterol efflux protein, ABCA1, supports anticancer functions of myeloid immune cells (2026) · cites this paper as [61]

    The section on DC maturation and function describes using apoptotic cells to activate antitumor T-cell responses as a promising cancer-vaccine approach. The section on antigen cross-presentation likewise presents DC efferocytosis as informing new immunotherapies and vaccines, rather than as a major hurdle to APC-based therapies. Page numbers are unavailable in our copy. (LLM, conf=0.78)

    Checked by a reasoning model — may be wrong.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

1 retracted

Flagged first, then by citations

Research works printed but not linked: 273

  1. [1]Schneider K Arandjelovic S. Apoptotic cell clearance components in inflammatory arthritis. Immunol Rev. (2023) 319: 142–50. doi: 10.1111/imr.13256 PMC10615714 37507355 · DOI
  2. [2]Qiu H Shao Z Wen X Liu Z Chen Z Qu D. Efferocytosis: An accomplice of cancer immune escape. BioMed Pharmacother. (2023) 167: 115540. doi: 10.1016/j.biopha.2023.115540 37741255 · DOI
  3. [3]Zhang M Wei J Sun Y He C Ma S Pan X. The efferocytosis process in aging: Supporting evidence, mechanisms, and therapeutic prospects for age-related diseases. J Adv Res. (2024). doi: 10.1016/j.jare.2024.03.008 38499245 · DOI
  4. [4]Belabed M Mauvais FX Maschalidi S Kurowska M Goudin N Huang JD. Kinesin-1 regulates antigen cross-presentation through the scission of tubulations from early endosomes in dendritic cells. Nat Commun. (2020) 11: 1817. doi: 10.1038/s41467-020-15692-0 32286311 PMC7156633 · DOI
  5. [5]Koga MM Engel A Pigni M Lavanchy C Stevanin M Laversenne V. IL10- and IL35-secreting mutuDC lines act in cooperation to inhibit memory T cell activation through LAG-3 expression. Front Immunol. (2021) 12: 607315. doi: 10.3389/fimmu.2021.607315 33679743 PMC7925845 · DOI
  6. [6]Bianconi E Piovesan A Facchin F Beraudi A Casadei R Frabetti F. An estimation of the number of cells in the human body. Ann Hum Biol. (2013) 40: 463–71. doi: 10.3109/03014460.2013.807878 23829164 · DOI · Paper page
  7. [7]Henson PM Hume DA. Apoptotic cell removal in development and tissue homeostasis. Trends Immunol. (2006) 27: 244–50. doi: 10.1016/j.it.2006.03.005 16584921 · DOI
  8. [8]Vandivier RW Henson PM Douglas IS. Burying the dead: the impact of failed apoptotic cell removal (efferocytosis) on chronic inflammatory lung disease. Chest. (2006) 129: 1673–82. doi: 10.1378/chest.129.6.1673 16778289 · DOI
  9. [9]Rieu Q Bougouin A Zagar Y Chatagnon J Hamieh A Enderlin J. Pleiotropic roles of scavenger receptors in circadian retinal phagocytosis: A new function for lysosomal SR-B2/LIMP-2 at the RPE cell surface. Int J Mol Sci. (2022) 23: 3445–63. doi: 10.3390/ijms23073445 PMC8998831 35408805 · DOI
  10. [10]Savill J Fadok V. Corpse clearance defines the meaning of cell death. Nature. (2000) 407: 784–8. doi: 10.1038/35037722 11048729 · DOI
  11. [11]Flemming A. Sepsis: DAMPening inflammation. Nat Rev Drug Discovery. (2011) 10: 416. doi: 10.1038/nrd3468 21629291 · DOI
  12. [12]Ogden CA deCathelineau A Hoffmann PR Bratton D Ghebrehiwet B Fadok VA. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med. (2001) 194: 781–95. doi: 10.1084/jem.194.6.781 PMC2195958 11560994 · DOI
  13. [13]Hoffmann PR deCathelineau AM Ogden CA Leverrier Y Bratton DL Daleke DL. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol. (2001) 155: 649–59. doi: 10.1083/jcb.200108080 PMC2198875 11706053 · DOI
  14. [14]Aderem A Underhill DM. Mechanisms of phagocytosis in macrophages. Annu Rev Immunol. (1999) 17: 593– 623. doi: 10.1146/annurev.immunol.17.1.593 10358769 · DOI · Paper page
  15. [15]Gude DR Alvarez SE Paugh SW Mitra P Yu J Griffiths R. Apoptosis induces expression of sphingosine kinase 1 to release sphingosine-1-phosphate as a "come-and-get-me" signal. FASEB J. (2008) 22: 2629–38. doi: 10.1096/fj.08-107169 PMC2493451 18362204 · DOI
  16. [16]Truman LA Ford CA Pasikowska M Pound JD Wilkinson SJ Dumitriu IE. CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis. Blood. (2008) 112: 5026–36. doi: 10.1182/blood-2008-06-162404 18799722 · DOI · Paper page
  17. [18]Doran AC Yurdagul A Jr. Tabas I. Efferocytosis in health and disease. Nat Rev Immunol. (2020) 20: 254–67. doi: 10.1038/s41577-019-0240-6 PMC7667664 31822793 · DOI · Paper page
  18. [19]Gardai SJ Bratton DL Ogden CA Henson PM. Recognition ligands on apoptotic cells: a perspective. J Leukoc Biol. (2006) 79: 896– 903. doi: 10.1189/jlb.1005550 16641135 · DOI
  19. [20]Oldenborg PA Zheleznyak A Fang YF Lagenaur CF Gresham HD Lindberg FP. Role of CD47 as a marker of self on red blood cells. Science. (2000) 288: 2051–4. doi: 10.1126/science.288.5473.2051 10856220 · DOI
  20. [21]Barkal AA Brewer RE Markovic M Kowarsky M Barkal SA Zaro BW. CD24 signalling through macrophage Siglec-10 is a target for cancer immunotherapy. Nature. (2019) 572: 392–6. doi: 10.1038/s41586-019-1456-0 PMC6697206 31367043 · DOI
  21. [23]Elward K Griffiths M Mizuno M Harris CL Neal JW Morgan BP. CD46 plays a key role in tailoring innate immune recognition of apoptotic and necrotic cells. J Biol Chem. (2005) 280: 36342–54. doi: 10.1074/jbc.M506579200 16087667 · DOI
  22. [24]Barkal AA Weiskopf K Kao KS Gordon SR Rosental B Yiu YY. Engagement of MHC class I by the inhibitory receptor LILRB1 suppresses macrophages and is a target of cancer immunotherapy. Nat Immunol. (2018) 19: 76– 84. doi: 10.1038/s41590-017-0004-z 29180808 PMC5832354 · DOI
  23. [25]He M Kubo H Morimoto K Fujino N Suzuki T Takahasi T. Receptor for advanced glycation end products binds to phosphatidylserine and assists in the clearance of apoptotic cells. EMBO Rep. (2011) 12: 358–64. doi: 10.1038/embor.2011.28 PMC3077249 21399623 · DOI
  24. [26]Greenberg ME Sun M Zhang R Febbraio M Silverstein R Hazen SL. Oxidized phosphatidylserine-CD36 interactions play an essential role in macrophage-dependent phagocytosis of apoptotic cells. J Exp Med. (2006) 203: 2613–25. doi: 10.1084/jem.20060370 PMC2118161 17101731 · DOI · Paper page
  25. [27]Vago JP Amaral FA van de Loo FAJ. Resolving inflammation by TAM receptor activation. Pharmacol Ther. (2021) 227: 107893. doi: 10.1016/j.pharmthera.2021.107893 33992683 · DOI
  26. [28]Kourtzelis I Li X Mitroulis I Grosser D Kajikawa T Wang B. DEL-1 promotes macrophage efferocytosis and clearance of inflammation. Nat Immunol. (2019) 20: 40–9. doi: 10.1038/s41590-018-0249-1 PMC6291356 30455459 · DOI
  27. [29]Albert ML Kim JI Birge RB. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat Cell Biol. (2000) 2: 899– 905. doi: 10.1038/35046549 11146654 · DOI
  28. [30]Wu Y Singh S Georgescu MM Birge RB. A role for Mer tyrosine kinase in alphavbeta5 integrin-mediated phagocytosis of apoptotic cells. J Cell Sci. (2005) 118: 539–53. doi: 10.1242/jcs.01632 15673687 · DOI
  29. [31]Akakura S Singh S Spataro M Akakura R Kim JI Albert ML. The opsonin MFG-E8 is a ligand for the alphavbeta5 integrin and triggers DOCK180-dependent Rac1 activation for the phagocytosis of apoptotic cells. Exp Cell Res. (2004) 292: 403–16. doi: 10.1016/j.yexcr.2003.09.011 14697347 · DOI
  30. [32]Park D Tosello-Trampont AC Elliott MR Lu M Haney LB Ma Z. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature. (2007) 450: 430–4. doi: 10.1038/nature06329 17960134 · DOI
  31. [33]Tao H Yancey PG Babaev VR Blakemore JL Zhang Y Ding L. Macrophage SR-BI mediates efferocytosis via Src/PI3K/Rac1 signaling and reduces atherosclerotic lesion necrosis. J Lipid Res. (2015) 56: 1449–60. doi: 10.1194/jlr.M056689 PMC4513986 26059978 · DOI · Paper page
  32. [34]Park SY Kang KB Thapa N Kim SY Lee SJ Kim IS. Requirement of adaptor protein GULP during stabilin-2-mediated cell corpse engulfment. J Biol Chem. (2008) 283: 10593–600. doi: 10.1074/jbc.M709105200 18230608 · DOI
  33. [35]Hochreiter-Hufford A Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol. (2013) 5: a008748. doi: 10.1101/cshperspect.a008748 23284042 PMC3579390 · DOI · Paper page
  34. [36]Nakaya M Tanaka M Okabe Y Hanayama R Nagata S. Opposite effects of rho family GTPases on engulfment of apoptotic cells by macrophages. J Biol Chem. (2006) 281: 8836–42. doi: 10.1074/jbc.M510972200 16439364 · DOI
  35. [37]Leverrier Y Ridley AJ. Requirement for Rho GTPases and PI 3-kinases during apoptotic cell phagocytosis by macrophages. Curr Biol. (2001) 11: 195–9. doi: 10.1016/S0960-9822(01)00047-1 11231156 · DOI
  36. [38]Tosello-Trampont AC Kinchen JM Brugnera E Haney LB Hengartner MO Ravichandran KS. Identification of two signaling submodules within the CrkII/ELMO/Dock180 pathway regulating engulfment of apoptotic cells. Cell Death Differ. (2007) 14: 963–72. doi: 10.1038/sj.cdd.4402094 17304244 · DOI
  37. [39]Gumienny TL Brugnera E Tosello-Trampont AC Kinchen JM Haney LB Nishiwaki K. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell. (2001) 107: 27– 41. doi: 10.1016/S0092-8674(01)00520-7 11595183 · DOI · Paper page
  38. [41]Grimsley CM Kinchen JM Tosello-Trampont AC Brugnera E Haney LB Lu M. Dock180 and ELMO1 proteins cooperate to promote evolutionarily conserved Rac-dependent cell migration. J Biol Chem. (2004) 279: 6087–97. doi: 10.1074/jbc.M307087200 14638695 · DOI · Paper page
  39. [42]Chen Z Borek D Padrick SB Gomez TS Metlagel Z Ismail AM. Structure and control of the actin regulatory WAVE complex. Nature. (2010) 468: 533–8. doi: 10.1038/nature09623 PMC3085272 21107423 · DOI · Paper page
  40. [43]Ding B Yang S Schaks M Liu Y Brown AJ Rottner K. Structures reveal a key mechanism of WAVE regulatory complex activation by Rac1 GTPase. Nat Commun. (2022) 13: 5444. doi: 10.1038/s41467-022-33174-3 36114192 PMC9481577 · DOI · Paper page
  41. [44]Heasman SJ Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. (2008) 9: 690– 701. doi: 10.1038/nrm2476 18719708 · DOI · Paper page
  42. [45]Evans IR Ghai PA Urbancic V Tan KL Wood W. SCAR/WAVE-mediated processing of engulfed apoptotic corpses is essential for effective macrophage migration in Drosophila. Cell Death Differ. (2013) 20: 709–20. doi: 10.1038/cdd.2012.166 PMC3619236 23328632 · DOI
  43. [46]Kim SY Kim S Bae DJ Park SY Lee GY Park GM. Coordinated balance of Rac1 and RhoA plays key roles in determining phagocytic appetite. PloS One. (2017) 12: e0174603. doi: 10.1371/journal.pone.0174603 28376111 PMC5380344 · DOI
  44. [47]Riento K Ridley AJ. Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol. (2003) 4: 446–56. doi: 10.1038/nrm1128 12778124 · DOI · Paper page
  45. [48]Erwig LP Gordon S Walsh GM Rees AJ. Previous uptake of apoptotic neutrophils or ligation of integrin receptors downmodulates the ability of macrophages to ingest apoptotic neutrophils. Blood. (1999) 93: 1406–12. doi: 10.1182/blood.V93.4.1406 9949185 · DOI
  46. [49]Tosello-Trampont AC Nakada-Tsukui K Ravichandran KS. Engulfment of apoptotic cells is negatively regulated by Rho-mediated signaling. J Biol Chem. (2003) 278: 49911–9. doi: 10.1074/jbc.M306079200 14514696 · DOI
  47. [50]Lou Y Han M Liu H Niu Y Liang Y Guo J. Essential roles of S100A10 in Toll-like receptor signaling and immunity to infection. Cell Mol Immunol. (2020) 17: 1053–62. doi: 10.1038/s41423-019-0278-1 PMC7608084 31467414 · DOI
  48. [51]Bonfim-Melo A Ferreira ER Mortara RA. Rac1/WAVE2 and Cdc42/N-WASP participation in actin-dependent host cell invasion by extracellular amastigotes of Trypanosoma cruzi. Front Microbiol. (2018) 9: 360. doi: 10.3389/fmicb.2018.00360 29541069 PMC5835522 · DOI
  49. [52]Ho HY Rohatgi R Lebensohn AM Le M Li J Gygi SP. Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex. Cell. (2004) 118: 203–16. doi: 10.1016/j.cell.2004.06.027 15260990 · DOI
  50. [53]Jubrail J Africano-Gomez K Herit F Mularski A Bourdoncle P Oberg L. Arpin is critical for phagocytosis in macrophages and is targeted by human rhinovirus. EMBO Rep. (2020) 21: e47963. doi: 10.15252/embr.201947963 31721415 PMC6945061 · DOI
  51. [54]Rohatgi R Ma L Miki H Lopez M Kirchhausen T Takenawa T. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell. (1999) 97: 221–31. doi: 10.1016/S0092-8674(00)80732-1 10219243 · DOI
  52. [55]Caron E Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science. (1998) 282: 1717–21. doi: 10.1126/science.282.5394.1717 9831565 · DOI · Paper page
  53. [56]Leverrier Y Lorenzi R Blundell MP Brickell P Kinnon C Ridley AJ. Cutting edge: the Wiskott-Aldrich syndrome protein is required for efficient phagocytosis of apoptotic cells. J Immunol. (2001) 166: 4831–4. doi: 10.4049/jimmunol.166.8.4831 11290758 · DOI
  54. [57]Yin C Heit B. Cellular responses to the efferocytosis of apoptotic cells. Front Immunol. (2021) 12: 631714. doi: 10.3389/fimmu.2021.631714 33959122 PMC8093429 · DOI
  55. [58]Kitano M Nakaya M Nakamura T Nagata S Matsuda M. Imaging of Rab5 activity identifies essential regulators for phagosome maturation. Nature. (2008) 453: 241–5. doi: 10.1038/nature06857 18385674 · DOI
  56. [60]Kinchen JM Ravichandran KS. Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells. Nature. (2010) 464: 778–82. doi: 10.1038/nature08853 PMC2901565 20305638 · DOI
  57. [61]Yu X Lu N Zhou Z. Phagocytic receptor CED-1 initiates a signaling pathway for degrading engulfed apoptotic cells. PloS Biol. (2008) 6: e61. doi: 10.1371/journal.pbio.0060061 18351800 PMC2267821 · DOI
  58. [62]Harrison RE Bucci C Vieira OV Schroer TA Grinstein S. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol. (2003) 23: 6494–506. doi: 10.1128/MCB.23.18.6494-6506.2003 PMC193691 12944476 · DOI
  59. [63]Johansson M Lehto M Tanhuanpaa K Cover TL Olkkonen VM. The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol Biol Cell. (2005) 16: 5480–92. doi: 10.1091/mbc.e05-03-0189 PMC1289395 16176980 · DOI
  60. [64]Rink J Ghigo E Kalaidzidis Y Zerial M. Rab conversion as a mechanism of progression from early to late endosomes. Cell. (2005) 122: 735–49. doi: 10.1016/j.cell.2005.06.043 16143105 · DOI
  61. [65]Balderhaar HJ Ungermann C. CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J Cell Sci. (2013) 126: 1307–16. doi: 10.1242/jcs.107805 23645161 · DOI
  62. [66]Miller HE Larson CL Heinzen RA. Actin polymerization in the endosomal pathway, but not on the Coxiella-containing vacuole, is essential for pathogen growth. PloS Pathog. (2018) 14: e1007005. doi: 10.1371/journal.ppat.1007005 29668757 PMC5927470 · DOI
  63. [67]Wu Z Thiyagarajan S O'Shaughnessy B Karatekin E. Regulation of exocytotic fusion pores by SNARE protein transmembrane domains. Front Mol Neurosci. (2017) 10: 315. doi: 10.3389/fnmol.2017.00315 29066949 PMC5641348 · DOI
  64. [68]Lennon-Dumenil AM Bakker AH Maehr R Fiebiger E Overkleeft HS Rosemblatt M. Analysis of protease activity in live antigen-presenting cells shows regulation of the phagosomal proteolytic contents during dendritic cell activation. J Exp Med. (2002) 196: 529–40. doi: 10.1084/jem.20020327 PMC2196045 12186844 · DOI
  65. [69]Backer JM. The intricate regulation and complex functions of the Class III phosphoinositide 3-kinase Vps34. Biochem J. (2016) 473: 2251–71. doi: 10.1042/BCJ20160170 27470591 · DOI
  66. [71]Yin C Argintaru D Heit B. Rab17 mediates intermixing of phagocytosed apoptotic cells with recycling endosomes. Small GTPases. (2019) 10: 218–26. doi: 10.1080/21541248.2017.1308852 PMC6548298 28471261 · DOI
  67. [72]Yin C Kim Y Argintaru D Heit B. Rab17 mediates differential antigen sorting following efferocytosis and phagocytosis. Cell Death Dis. (2016) 7: e2529. doi: 10.1038/cddis.2016.431 28005073 PMC5261003 · DOI
  68. [74]Yurdagul A Jr. Metabolic consequences of efferocytosis and its impact on atherosclerosis. Immunometabolism. (2021) 3: e210017-1–22. doi: 10.20900/immunometab20210017 PMC8081385 33927896 · DOI
  69. [75]Mukundan L Odegaard JI Morel CR Heredia JE Mwangi JW Ricardo-Gonzalez RR. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat Med. (2009) 15: 1266–72. doi: 10.1038/nm.2048 PMC2783696 19838202 · DOI · Paper page
  70. [76]Yoon YS Kim SY Kim MJ Lim JH Cho MS Kang JL. PPARgamma activation following apoptotic cell instillation promotes resolution of lung inflammation and fibrosis via regulation of efferocytosis and proresolving cytokines. Mucosal Immunol. (2015) 8: 1031–46. doi: 10.1038/mi.2014.130 PMC4762910 25586556 · DOI · Paper page
  71. [77]Mota AC Dominguez M Weigert A Snodgrass RG Namgaladze D Brune B. Lysosome-dependent LXR and PPARdelta activation upon efferocytosis in human macrophages. Front Immunol. (2021) 12: 637778. doi: 10.3389/fimmu.2021.637778 34025647 PMC8137840 · DOI
  72. [78]Bosteels V Marechal S De Nolf C Rennen S Maelfait J Tavernier SJ. LXR signaling controls homeostatic dendritic cell maturation. Sci Immunol. (2023) 8: eadd3955. doi: 10.1126/sciimmunol.add3955 37172103 · DOI
  73. [79]Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. (2007) 8: 917–29. doi: 10.1038/nrm2272 17912264 · DOI
  74. [80]Jefferies KC Cipriano DJ Forgac M. Function, structure and regulation of the vacuolar (H+)-ATPases. Arch Biochem Biophys. (2008) 476: 33– 42. doi: 10.1016/j.abb.2008.03.025 18406336 PMC2543942 · DOI
  75. [81]Ablasser A Chen ZJ. cGAS in action: Expanding roles in immunity and inflammation. Science. (2019) 363: 3621–9. doi: 10.1126/science.aat8657 30846571 · DOI · Paper page
  76. [82]Liebold I Al Jawazneh A Casar C Lanzloth C Leyk S Hamley M. Apoptotic cell identity induces distinct functional responses to IL-4 in efferocytic macrophages. Science. (2024) 384: eabo7027. doi: 10.1126/science.abo7027 38574142 · DOI · Paper page
  77. [83]Ohteki T Kawamura S Onai N. Commitment to dendritic cells and monocytes. Int Immunol. (2021) 33: 815–9. doi: 10.1093/intimm/dxab031 34134136 · DOI
  78. [84]Gardner A de Mingo Pulido A Ruffell B. Dendritic cells and their role in immunotherapy. Front Immunol. (2020) 11: 924. doi: 10.3389/fimmu.2020.00924 32508825 PMC7253577 · DOI
  79. [85]Anderson DA 3rd Dutertre CA Ginhoux F Murphy KM. Genetic models of human and mouse dendritic cell development and function. Nat Rev Immunol. (2021) 21: 101–15. doi: 10.1038/s41577-020-00413-x PMC10955724 32908299 · DOI
  80. [86]Bagadia P Huang X Liu TT Durai V Grajales-Reyes GE Nitschke M. An Nfil3-Zeb2-Id2 pathway imposes Irf8 enhancer switching during cDC1 development. Nat Immunol. (2019) 20: 1174–85. doi: 10.1038/s41590-019-0449-3 PMC6707889 31406377 · DOI
  81. [87]Albert ML Sauter B Bhardwaj N. Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature. (1998) 392: 86–9. doi: 10.1038/32183 9510252 · DOI
  82. [88]Schnorrer P Behrens GM Wilson NS Pooley JL Smith CM El-Sukkari D. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U.S.A. (2006) 103: 10729–34. doi: 10.1073/pnas.0601956103 PMC1502299 16807294 · DOI
  83. [89]Albert ML Pearce SF Francisco LM Sauter B Roy P Silverstein RL. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med. (1998) 188: 1359–68. doi: 10.1084/jem.188.7.1359 PMC2212488 9763615 · DOI · Paper page
  84. [90]Yrlid U Wick MJ. Salmonella-induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells. J Exp Med. (2000) 191: 613–24. doi: 10.1084/jem.191.4.613 PMC2195841 10684853 · DOI
  85. [91]Subklewe M Paludan C Tsang ML Mahnke K Steinman RM Munz C. Dendritic cells cross-present latency gene products from Epstein-Barr virus-transformed B cells and expand tumor-reactive CD8(+) killer T cells. J Exp Med. (2001) 193: 405–11. doi: 10.1084/jem.193.3.405 PMC2195925 11157061 · DOI
  86. [92]Motta I Andre F Lim A Tartaglia J Cox WI Zitvogel L. Cross-presentation by dendritic cells of tumor antigen expressed in apoptotic recombinant canarypox virus-infected dendritic cells. J Immunol. (2001) 167: 1795–802. doi: 10.4049/jimmunol.167.3.1795 11466405 · DOI
  87. [93]Iyoda T Shimoyama S Liu K Omatsu Y Akiyama Y Maeda Y. The CD8+ dendritic cell subset selectively endocytoses dying cells in culture and in vivo. J Exp Med. (2002) 195: 1289–302. doi: 10.1084/jem.20020161 PMC2193756 12021309 · DOI
  88. [94]Gu FF Zhang K Ma LL Liu YY Li C Hu Y. The superior ability of human BDCA3(+) (CD141(+)) dendritic cells (DCs) to cross-present antigens derived from necrotic lung cancer cells. Front Immunol. (2020) 11: 1267. doi: 10.3389/fimmu.2020.01267 32655564 PMC7325999 · DOI
  89. [95]Dudziak D Kamphorst AO Heidkamp GF Buchholz VR Trumpfheller C Yamazaki S. Differential antigen processing by dendritic cell subsets in vivo. Science. (2007) 315: 107–11. doi: 10.1126/science.1136080 17204652 · DOI
  90. [96]Wakabayashi A Shimizu M Shinya E Takahashi H. HMGB1 released from intestinal epithelia damaged by cholera toxin adjuvant contributes to activation of mucosal dendritic cells and induction of intestinal cytotoxic T lymphocytes and IgA. Cell Death Dis. (2018) 9: 631. doi: 10.1038/s41419-018-0665-z 29795370 PMC5967345 · DOI
  91. [97]Bandyopadhyay A Fine RL Demento S Bockenstedt LK Fahmy TM. The impact of nanoparticle ligand density on dendritic-cell targeted vaccines. Biomaterials. (2011) 32: 3094–105. doi: 10.1016/j.biomaterials.2010.12.054 PMC4570971 21262534 · DOI · Paper page
  92. [98]Vremec D Pooley J Hochrein H Wu L Shortman K. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J Immunol. (2000) 164: 2978–86. doi: 10.4049/jimmunol.164.6.2978 10706685 · DOI
  93. [99]Niezold T Storcksdieck Genannt Bonsmann M Maaske A Temchura V Heinecke V Hannaman D. DNA vaccines encoding DEC205-targeted antigens: immunity or tolerance? Immunology. (2015) 145: 519–33. doi: 10.1111/imm.12467 PMC4515132 25819746 · DOI
  94. [100]Qiu CH Miyake Y Kaise H Kitamura H Ohara O Tanaka M. Novel subset of CD8alpha+ dendritic cells localized in the marginal zone is responsible for tolerance to cell-associated antigens. J Immunol. (2009) 182: 4127–36. doi: 10.4049/jimmunol.0803364 19299710 · DOI
  95. [101]Oh DS Lee HK. Autophagy protein ATG5 regulates CD36 expression and anti-tumor MHC class II antigen presentation in dendritic cells. Autophagy. (2019) 15: 2091–106. doi: 10.1080/15548627.2019.1596493 PMC6844530 30900506 · DOI
  96. [102]del Rio ML Bernhardt G Rodriguez-Barbosa JI Forster R. Development and functional specialization of CD103+ dendritic cells. Immunol Rev. (2010) 234: 268–81. doi: 10.1111/j.0105-2896.2009.00874.x 20193025 · DOI
  97. [103]Cabeza-Cabrerizo M Cardoso A Minutti CM Pereira da Costa M Reis e Sousa C. Dendritic cells revisited. Annu Rev Immunol. (2021) 39: 131–66. doi: 10.1146/annurev-immunol-061020-053707 33481643 · DOI · Paper page
  98. [104]Hildner K Edelson BT Purtha WE Diamond M Matsushita H Kohyama M. Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science. (2008) 322: 1097–100. doi: 10.1126/science.1164206 PMC2756611 19008445 · DOI · Paper page
  99. [105]Edelson BT Kc W Juang R Kohyama M Benoit LA Klekotka PA. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med. (2010) 207: 823–36. doi: 10.1084/jem.20091627 PMC2856032 20351058 · DOI
  100. [106]Jakubzick C Helft J Kaplan TJ Randolph GJ. Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus particulate antigen. J Immunol Methods. (2008) 337: 121–31. doi: 10.1016/j.jim.2008.07.005 PMC3537501 18662693 · DOI
  101. [107]Vermaelen K Pauwels R. Accurate and simple discrimination of mouse pulmonary dendritic cell and macrophage populations by flow cytometry: methodology and new insights. Cytometry A. (2004) 61: 170–77. doi: 10.1002/cyto.a.20064 15382026 · DOI
  102. [108]Sung SS Fu SM Rose CE Jr. Gaskin F Ju ST Beaty SR. A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol. (2006) 176: 2161–72. doi: 10.4049/jimmunol.176.4.2161 16455972 · DOI
  103. [109]del Rio ML Rodriguez-Barbosa JI Kremmer E Forster R. CD103- and CD103+ bronchial lymph node dendritic cells are specialized in presenting and cross-presenting innocuous antigen to CD4+ and CD8+ T cells. J Immunol. (2007) 178: 6861–6. doi: 10.4049/jimmunol.178.11.6861 17513734 · DOI
  104. [110]GeurtsvanKessel CH Lambrecht BN. Division of labor between dendritic cell subsets of the lung. Mucosal Immunol. (2008) 1: 442–50. doi: 10.1038/mi.2008.39 19079211 · DOI
  105. [111]Belz GT Bedoui S Kupresanin F Carbone FR Heath WR. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat Immunol. (2007) 8: 1060–6. doi: 10.1038/ni1505 17767161 · DOI
  106. [112]GeurtsvanKessel CH Willart MA van Rijt LS Muskens F Kool M Baas C. Clearance of influenza virus from the lung depends on migratory langerin+CD11b- but not plasmacytoid dendritic cells. J Exp Med. (2008) 205: 1621–34. doi: 10.1084/jem.20071365 PMC2442640 18591406 · DOI
  107. [113]Kim TS Braciale TJ. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PloS One. (2009) 4: e4204. doi: 10.1371/journal.pone.0004204 19145246 PMC2615220 · DOI
  108. [114]Bedoui S Whitney PG Waithman J Eidsmo L Wakim L Caminschi I. Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells. Nat Immunol. (2009) 10: 488–95. doi: 10.1038/ni.1724 19349986 · DOI
  109. [115]Desch AN Randolph GJ Murphy K Gautier EL Kedl RM Lahoud MH. CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med. (2011) 208: 1789–97. doi: 10.1084/jem.20110538 PMC3171085 21859845 · DOI
  110. [116]Silva-Sanchez A Meza-Perez S Liu M Stone SL Flores-Romo L Ubil E. Activation of regulatory dendritic cells by Mertk coincides with a temporal wave of apoptosis in neonatal lungs. Sci Immunol. (2023) 8: eadc9081. doi: 10.1126/sciimmunol.adc9081 37327322 PMC10351240 · DOI
  111. [118]Kelsall B. Recent progress in understanding the phenotype and function of intestinal dendritic cells and macrophages. Mucosal Immunol. (2008) 1: 460–9. doi: 10.1038/mi.2008.61 PMC4780321 19079213 · DOI
  112. [119]Sawai CM Sisirak V Ghosh HS Hou EZ Ceribelli M Staudt LM. Transcription factor Runx2 controls the development and migration of plasmacytoid dendritic cells. J Exp Med. (2013) 210: 2151–9. doi: 10.1084/jem.20130443 PMC3804932 24101375 · DOI · Paper page
  113. [121]Bonnefoy F Perruche S Couturier M Sedrati A Sun Y Tiberghien P. Plasmacytoid dendritic cells play a major role in apoptotic leukocyte-induced immune modulation. J Immunol. (2011) 186: 5696–705. doi: 10.4049/jimmunol.1001523 21460208 · DOI
  114. [122]Wu Y Tibrewal N Birge RB. Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. (2006) 16: 189–97. doi: 10.1016/j.tcb.2006.02.003 16529932 · DOI
  115. [123]Kobayashi N Karisola P Pena-Cruz V Dorfman DM Jinushi M Umetsu SE. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity. (2007) 27: 927–40. doi: 10.1016/j.immuni.2007.11.011 PMC2757006 18082433 · DOI
  116. [124]Nakayama M Akiba H Takeda K Kojima Y Hashiguchi M Azuma M. Tim-3 mediates phagocytosis of apoptotic cells and cross-presentation. Blood. (2009) 113: 3821–30. doi: 10.1182/blood-2008-10-185884 19224762 · DOI
  117. [126]Kuroiwa M Yamaguchi SI Kato Y Hori A Toyoura S Nakahara M. Tim4, a macrophage receptor for apoptotic cells, binds polystyrene microplastics via aromatic-aromatic interactions. Sci Total Environ. (2023) 875: 162586. doi: 10.1016/j.scitotenv.2023.162586 36871719 · DOI
  118. [127]Seitz HM Camenisch TD Lemke G Earp HS Matsushima GK. Macrophages and dendritic cells use different Axl/Mertk/Tyro3 receptors in clearance of apoptotic cells. J Immunol. (2007) 178: 5635–42. doi: 10.4049/jimmunol.178.9.5635 17442946 · DOI
  119. [128]Myers KV Amend SR Pienta KJ. Targeting Tyro3, Axl and MerTK (TAM receptors): implications for macrophages in the tumor microenvironment. Mol Cancer. (2019) 18: 94. doi: 10.1186/s12943-019-1022-2 31088471 PMC6515593 · DOI
  120. [129]Guttenberg MA Vose AT Birukova A Lewars K Cumming RI Albright MC. Tissue-resident alveolar macrophages reduce ozone-induced inflammation via MerTK mediated efferocytosis. Am J Respir Cell Mol Biol. (2024). doi: 10.1165/rcmb.2023-0390OC PMC11160417 38386777 · DOI
  121. [130]Rigoni TS Vellozo NS Guimaraes-Pinto K Cabral-Piccin M Fabiano-Coelho L Matos-Silva TC. Axl receptor induces efferocytosis, dampens M1 macrophage responses and promotes heart pathology in Trypanosoma cruzi infection. Commun Biol. (2022) 5: 1421. doi: 10.1038/s42003-022-04401-w 36581764 PMC9800583 · DOI
  122. [131]Verbovetski I Bychkov H Trahtemberg U Shapira I Hareuveni M Ben-Tal O. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J Exp Med. (2002) 196: 1553–61. doi: 10.1084/jem.20020263 PMC2196062 12486098 · DOI
  123. [132]Rubartelli A Poggi A Zocchi MR. The selective engulfment of apoptotic bodies by dendritic cells is mediated by the alpha(v)beta3 integrin and requires intracellular and extracellular calcium. Eur J Immunol. (1997) 27: 1893–900. doi: 10.1002/eji.1830270812 9295024 · DOI
  124. [133]Mevorach D Mascarenhas JO Gershov D Elkon KB. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med. (1998) 188: 2313–20. doi: 10.1084/jem.188.12.2313 PMC2212421 9858517 · DOI
  125. [134]Belz GT Vremec D Febbraio M Corcoran L Shortman K Carbone FR. CD36 is differentially expressed by CD8+ splenic dendritic cells but is not required for cross-presentation in vivo. J Immunol. (2002) 168: 6066–70. doi: 10.4049/jimmunol.168.12.6066 12055215 · DOI
  126. [135]Canavati C Siam A Labes S Trabelsi N Regev E Parnasa E. Pathogenic variants of scavenger receptor CD36 lead to decreased efferocytosis and predispose to myocarditis following vaccination with Pfizer-bioNTech BNT162b2 against coronavirus infection (COVID-19). Circulation. (2024) 149: 270–3. doi: 10.1161/CIRCULATIONAHA.123.064884 38227712 · DOI
  127. [136]Wicker-Planquart C Dufour S Tacnet-Delorme P Bally I Delneste Y Frachet P. Molecular and cellular interactions of scavenger receptor SR-F1 with complement C1q provide insights into its role in the clearance of apoptotic cells. Front Immunol. (2020) 11: 544. doi: 10.3389/fimmu.2020.00544 32296440 PMC7137648 · DOI
  128. [137]Zhang Z Jiang Y Zhou Z Huang J Chen S Zhou W. Scavenger receptor A1 attenuates aortic dissection via promoting efferocytosis in macrophages. Biochem Pharmacol. (2019) 168: 392– 403. doi: 10.1016/j.bcp.2019.07.027 31381873 · DOI
  129. [138]Lee HN Tian L Bouladoux N Davis J Quinones M Belkaid Y. Dendritic cells expressing immunoreceptor CD300f are critical for controlling chronic gut inflammation. J Clin Invest. (2017) 127: 1905–17. doi: 10.1172/JCI89531 PMC5409274 28414292 · DOI
  130. [139]Murakami Y Tian L Voss OH Margulies DH Krzewski K Coligan JE. CD300b regulates the phagocytosis of apoptotic cells via phosphatidylserine recognition. Cell Death Differ. (2014) 21: 1746–57. doi: 10.1038/cdd.2014.86 PMC4211373 25034781 · DOI
  131. [140]Simhadri VR Andersen JF Calvo E Choi SC Coligan JE Borrego F. Human CD300a binds to phosphatidylethanolamine and phosphatidylserine, and modulates the phagocytosis of dead cells. Blood. (2012) 119: 2799–809. doi: 10.1182/blood-2011-08-372425 PMC3327458 22302738 · DOI
  132. [141]Kim S Park SY Kim SY Bae DJ Pyo JH Hong M. Cross talk between engulfment receptors stabilin-2 and integrin alphavbeta5 orchestrates engulfment of phosphatidylserine-exposed erythrocytes. Mol Cell Biol. (2012) 32: 2698–708. doi: 10.1128/MCB.06743-11 PMC3416206 22566688 · DOI
  133. [142]Lee W Park SY Yoo Y Kim SY Kim JE Kim SW. Macrophagic stabilin-1 restored disruption of vascular integrity caused by sepsis. Thromb Haemost. (2018) 118: 1776–89. doi: 10.1055/s-0038-1669477 30235477 · DOI
  134. [143]Mirtschink P Chavakis T. Stabilin-1-mediated efferocytosis protects against vascular leakage in sepsis: A novel therapeutic approach? Thromb Haemost. (2018) 118: 1852–3. doi: 10.1055/s-0038-1673688 30312979 · DOI
  135. [144]Park SY Jung MY Kim HJ Lee SJ Kim SY Lee BH. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. (2008) 15: 192– 201. doi: 10.1038/sj.cdd.4402242 17962816 · DOI
  136. [145]Subramanian M Hayes CD Thome JJ Thorp E Matsushima GK Herz J. An AXL/LRP-1/RANBP9 complex mediates DC efferocytosis and antigen cross-presentation in vivo. J Clin Invest. (2014) 124: 1296–308. doi: 10.1172/JCI72051 PMC3934164 24509082 · DOI
  137. [146]Brophy ML Dong Y Tao H Yancey PG Song K Zhang K. Myeloid-specific deletion of epsins 1 and 2 reduces atherosclerosis by preventing LRP-1 downregulation. Circ Res. (2019) 124: e6– e19. doi: 10.1161/CIRCRESAHA.118.313028 30595089 PMC6375743 · DOI
  138. [147]Mueller PA Kojima Y Huynh KT Maldonado RA Ye J Tavori H. Macrophage LRP1 (Low-density lipoprotein receptor-related protein 1) is required for the effect of CD47 blockade on efferocytosis and atherogenesis-brief report. Arterioscler Thromb Vasc Biol. (2022) 42: e1–9. doi: 10.1161/ATVBAHA.121.316854 PMC8702482 34758632 · DOI
  139. [149]Davis K Banerjee S Friggeri A Bell C Abraham E Zerfaoui M. Poly(ADP-ribosyl)ation of high mobility group box 1 (HMGB1) protein enhances inhibition of efferocytosis. Mol Med. (2012) 18: 359–69. doi: 10.2119/molmed.2011.00203 PMC3356430 22204001 · DOI
  140. [150]Li K Chen G Luo H Li J Liu A Yang C. MRP8/14 mediates macrophage efferocytosis through RAGE and Gas6/MFG-E8, and induces polarization via TLR4-dependent pathway. J Cell Physiol. (2021) 236: 1375–90. doi: 10.1002/jcp.29944 33128793 · DOI
  141. [151]Mahida RY Lax S Bassford CR Scott A Parekh D Hardy RS. Impaired alveolar macrophage 11beta-hydroxysteroid dehydrogenase type 1 reductase activity contributes to increased pulmonary inflammation and mortality in sepsis-related ARDS. Front Immunol. (2023) 14: 1159831. doi: 10.3389/fimmu.2023.1159831 37180160 PMC10172463 · DOI
  142. [152]Das S Sarkar A Ryan KA Fox S Berger AH Juncadella IJ. Brain angiogenesis inhibitor 1 is expressed by gastric phagocytes during infection with Helicobacter pylori and mediates the recognition and engulfment of human apoptotic gastric epithelial cells. FASEB J. (2014) 28: 2214–24. doi: 10.1096/fj.13-243238 PMC3986834 24509909 · DOI
  143. [153]Rothlin CV Ghosh S Zuniga EI Oldstone MB Lemke G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell. (2007) 131: 1124–36. doi: 10.1016/j.cell.2007.10.034 18083102 · DOI · Paper page
  144. [154]Chan PY Carrera Silva EA De Kouchkovsky D Joannas LD Hao L Hu D. The TAM family receptor tyrosine kinase TYRO3 is a negative regulator of type 2 immunity. Science. (2016) 352: 99– 103. doi: 10.1126/science.aaf1358 27034374 PMC4935984 · DOI
  145. [155]Tang J Jin Y Jia F Lv T Manaenko A Zhang LF. Gas6 promotes microglia efferocytosis and suppresses inflammation through activating Axl/Rac1 signaling in subarachnoid hemorrhage mice. Transl Stroke Res. (2023) 14: 955–69. doi: 10.1007/s12975-022-01099-0 36324028 · DOI
  146. [156]Zhu C Anderson AC Schubart A Xiong H Imitola J Khoury SJ. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol. (2005) 6: 1245–52. doi: 10.1038/ni1271 16286920 · DOI · Paper page
  147. [157]Rodriguez-Manzanet R DeKruyff R Kuchroo VK Umetsu DT. The costimulatory role of TIM molecules. Immunol Rev. (2009) 229: 259–70. doi: 10.1111/j.1600-065X.2009.00772.x PMC3217781 19426227 · DOI
  148. [158]de Mingo Pulido A Hanggi K Celias DP Gardner A Li J Batista-Bittencourt B. The inhibitory receptor TIM-3 limits activation of the cGAS-STING pathway in intra-tumoral dendritic cells by suppressing extracellular DNA uptake. Immunity. (2021) 54: 1154– 67.e7. doi: 10.1016/j.immuni.2021.04.019 33979578 PMC8192496 · DOI
  149. [159]Park D Hochreiter-Hufford A Ravichandran KS. The phosphatidylserine receptor TIM-4 does not mediate direct signaling. Curr Biol. (2009) 19: 346–51. doi: 10.1016/j.cub.2009.01.042 19217291 · DOI
  150. [161]Jorge AM Lao T Kim R Licciardi S El Khoury J Luster AD. SCARF1-induced efferocytosis plays an immunomodulatory role in humans, and autoantibodies targeting SCARF1 are produced in patients with systemic lupus erythematosus. J Immunol. (2022) 208: 955–67. doi: 10.4049/jimmunol.2100532 PMC8852219 35082161 · DOI
  151. [162]Ramirez-Ortiz ZG Pendergraft WF 3rd Prasad A Byrne MH Iram T Blanchette CJ. The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat Immunol. (2013) 14: 917–26. doi: 10.1038/ni.2670 PMC3752698 23892722 · DOI
  152. [163]Tian L Choi SC Lee HN Murakami Y Qi CF Sengottuvelu M. Enhanced efferocytosis by dendritic cells underlies memory T-cell expansion and susceptibility to autoimmune disease in CD300f-deficient mice. Cell Death Differ. (2016) 23: 1086–96. doi: 10.1038/cdd.2015.161 PMC4987725 26768664 · DOI
  153. [164]Mantegazza AR Magalhaes JG Amigorena S Marks MS. Presentation of phagocytosed antigens by MHC class I and II. Traffic. (2013) 14: 135–52. doi: 10.1111/tra.12026 PMC3538944 23127154 · DOI
  154. [165]Albert ML. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol. (2004) 4: 223–31. doi: 10.1038/nri11308 15039759 · DOI
  155. [166]Kovacsovics-Bankowski M Clark K Benacerraf B Rock KL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci U.S.A. (1993) 90: 4942–6. doi: 10.1073/pnas.90.11.4942 PMC46629 8506338 · DOI
  156. [167]Bosnjak L Miranda-Saksena M Koelle DM Boadle RA Jones CA Cunningham AL. Herpes simplex virus infection of human dendritic cells induces apoptosis and allows cross-presentation via uninfected dendritic cells. J Immunol. (2005) 174: 2220–7. doi: 10.4049/jimmunol.174.4.2220 15699155 · DOI
  157. [168]Blachere NE Darnell RB Albert ML. Apoptotic cells deliver processed antigen to dendritic cells for cross-presentation. PloS Biol. (2005) 3: e185. doi: 10.1371/journal.pbio.0030185 15839733 PMC1084338 · DOI
  158. [169]Segura E Villadangos JA. A modular and combinatorial view of the antigen cross-presentation pathway in dendritic cells. Traffic. (2011) 12: 1677–85. doi: 10.1111/j.1600-0854.2011.01254.x 21777358 · DOI
  159. [170]Cruz FM Colbert JD Merino E Kriegsman BA Rock KL. The biology and underlying mechanisms of cross-presentation of exogenous antigens on MHC-I molecules. Annu Rev Immunol. (2017) 35: 149–76. doi: 10.1146/annurev-immunol-041015-055254 PMC5508990 28125356 · DOI
  160. [171]Gros M Amigorena S. Regulation of antigen export to the cytosol during cross-presentation. Front Immunol. (2019) 10: 41. doi: 10.3389/fimmu.2019.00041 30745902 PMC6360170 · DOI
  161. [172]Colbert JD Cruz FM Rock KL. Cross-presentation of exogenous antigens on MHC I molecules. Curr Opin Immunol. (2020) 64: 1– 8. doi: 10.1016/j.coi.2019.12.005 31927332 PMC7343603 · DOI · Paper page
  162. [173]Rodriguez A Regnault A Kleijmeer M Ricciardi-Castagnoli P Amigorena S. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat Cell Biol. (1999) 1: 362–8. doi: 10.1038/14058 10559964 · DOI
  163. [174]Grotzke JE Cresswell P. Are ERAD components involved in cross-presentation? Mol Immunol. (2015) 68: 112–5. doi: 10.1016/j.molimm.2015.05.002 26005101 · DOI
  164. [175]Delamarre L Pack M Chang H Mellman I Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science. (2005) 307: 1630–4. doi: 10.1126/science.1108003 15761154 · DOI
  165. [176]Erwig LP McPhilips KA Wynes MW Ivetic A Ridley AJ Henson PM. Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrin-radixin-moesin (ERM) proteins. Proc Natl Acad Sci U.S.A. (2006) 103: 12825–30. doi: 10.1073/pnas.0605331103 PMC1568932 16908865 · DOI
  166. [177]Canton J Blees H Henry CM Buck MD Schulz O Rogers NC. The receptor DNGR-1 signals for phagosomal rupture to promote cross-presentation of dead-cell-associated antigens. Nat Immunol. (2021) 22: 140–53. doi: 10.1038/s41590-020-00824-x PMC7116638 33349708 · DOI
  167. [178]Abdolmaleki F Farahani N Gheibi Hayat SM Pirro M Bianconi V Barreto GE. The role of efferocytosis in autoimmune diseases. Front Immunol. (2018) 9: 1645. doi: 10.3389/fimmu.2018.01645 30083153 PMC6064952 · DOI
  168. [179]Cruz FM Colbert JD Rock KL. The GTPase Rab39a promotes phagosome maturation into MHC-I antigen-presenting compartments. EMBO J. (2020) 39: e102020. doi: 10.15252/embj.2019102020 31821587 PMC6960445 · DOI
  169. [180]Tzelepis F Verway M Daoud J Gillard J Hassani-Ardakani K Dunn J. Annexin1 regulates DC efferocytosis and cross-presentation during Mycobacterium tuberculosis infection. J Clin Invest. (2015) 125: 752–68. doi: 10.1172/JCI77014 PMC4319406 25562320 · DOI
  170. [181]Arrode G Boccaccio C Lule J Allart S Moinard N Abastado JP. Incoming human cytomegalovirus pp65 (UL83) contained in apoptotic infected fibroblasts is cross-presented to CD8(+) T cells by dendritic cells. J Virol. (2000) 74: 10018–24. doi: 10.1128/JVI.74.21.10018-10024.2000 PMC102040 11024130 · DOI
  171. [182]Larsson M Fonteneau JF Lirvall M Haslett P Lifson JD Bhardwaj N. Activation of HIV-1 specific CD4 and CD8 T cells by human dendritic cells: roles for cross-presentation and non-infectious HIV-1 virus. AIDS. (2002) 16: 1319–29. doi: 10.1097/00002030-200207050-00003 12131208 · DOI
  172. [183]Larsson M Fonteneau JF Somersan S Sanders C Bickham K Thomas EK. Efficiency of cross presentation of vaccinia virus-derived antigens by human dendritic cells. Eur J Immunol. (2001) 31: 3432–42. doi: 10.1002/(ISSN)1521-4141 11745362 · DOI
  173. [185]Wang Z Li G Dou S Zhang Y Liu Y Zhang J. Tim-3 promotes listeria monocytogenes immune evasion by suppressing major histocompatibility complex class I. J Infect Dis. (2020) 221: 830–40. doi: 10.1093/infdis/jiz512 31586389 · DOI
  174. [186]Oikawa T Kamimura Y Akiba H Yagita H Okumura K Takahashi H. Preferential involvement of Tim-3 in the regulation of hepatic CD8+ T cells in murine acute graft-versus-host disease. J Immunol. (2006) 177: 4281–7. doi: 10.4049/jimmunol.177.7.4281 16982862 · DOI
  175. [187]Winau F Weber S Sad S de Diego J Hoops SL Breiden B. Apoptotic vesicles crossprime CD8 T cells and protect against tuberculosis. Immunity. (2006) 24: 105–17. doi: 10.1016/j.immuni.2005.12.001 16413927 · DOI · Paper page
  176. [188]Behar SM Divangahi M Remold HG. Evasion of innate immunity by Mycobacterium tuberculosis: is death an exit strategy? Nat Rev Microbiol. (2010) 8: 668–74. doi: 10.1038/nrmicro2387 PMC3221965 20676146 · DOI
  177. [189]Divangahi M Chen M Gan H Desjardins D Hickman TT Lee DM. Mycobacterium tuberculosis evades macrophage defenses by inhibiting plasma membrane repair. Nat Immunol. (2009) 10: 899– 906. doi: 10.1038/ni.1758 19561612 PMC2730354 · DOI
  178. [190]Behar SM Martin CJ Nunes-Alves C Divangahi M Remold HG. Lipids, apoptosis, and cross-presentation: links in the chain of host defense against Mycobacterium tuberculosis. Microbes Infect. (2011) 13: 749–56. doi: 10.1016/j.micinf.2011.03.002 PMC3130819 21458584 · DOI
  179. [191]Divangahi M Desjardins D Nunes-Alves C Remold HG Behar SM. Eicosanoid pathways regulate adaptive immunity to Mycobacterium tuberculosis. Nat Immunol. (2010) 11: 751–8. doi: 10.1038/ni.1904 PMC3150169 20622882 · DOI
  180. [192]Heath WR Belz GT Behrens GM Smith CM Forehan SP Parish IA. Cross-presentation, dendritic cell subsets, and the generation of immunity to cellular antigens. Immunol Rev. (2004) 199: 9– 26. doi: 10.1111/j.0105-2896.2004.00142.x 15233723 · DOI
  181. [193]Kurts C Kosaka H Carbone FR Miller JF Heath WR. Class I-restricted cross-presentation of exogenous self-antigens leads to deletion of autoreactive CD8(+) T cells. J Exp Med. (1997) 186: 239–45. doi: 10.1084/jem.186.2.239 PMC2198972 9221753 · DOI
  182. [194]Liu K Iyoda T Saternus M Kimura Y Inaba K Steinman RM. Immune tolerance after delivery of dying cells to dendritic cells in situ. J Exp Med. (2002) 196: 1091–7. doi: 10.1084/jem.20021215 PMC2194037 12391020 · DOI
  183. [195]Redmond WL Sherman LA. Peripheral tolerance of CD8 T lymphocytes. Immunity. (2005) 22: 275–84. doi: 10.1016/j.immuni.2005.01.010 15780985 · DOI
  184. [196]Luckashenak N Schroeder S Endt K Schmidt D Mahnke K Bachmann MF. Constitutive crosspresentation of tissue antigens by dendritic cells controls CD8+ T cell tolerance in vivo. Immunity. (2008) 28: 521–32. doi: 10.1016/j.immuni.2008.02.018 18387832 · DOI
  185. [197]Guo L Shen S Rowley JW Tolley ND Jia W Manne BK. Platelet MHC class I mediates CD8+ T-cell suppression during sepsis. Blood. (2021) 138: 401–16. doi: 10.1182/blood.2020008958 PMC8343546 33895821 · DOI
  186. [198]Kawai T Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. (2010) 11: 373–84. doi: 10.1038/ni.1863 20404851 · DOI · Paper page
  187. [199]Krispin A Bledi Y Atallah M Trahtemberg U Verbovetski I Nahari E. Apoptotic cell thrombospondin-1 and heparin-binding domain lead to dendritic-cell phagocytic and tolerizing states. Blood. (2006) 108: 3580–9. doi: 10.1182/blood-2006-03-013334 16882710 · DOI
  188. [200]Pujol-Autonell I Ampudia RM Planas R Marin-Gallen S Carrascal J Sanchez A. Efferocytosis promotes suppressive effects on dendritic cells through prostaglandin E2 production in the context of autoimmunity. PloS One. (2013) 8: e63296. doi: 10.1371/journal.pone.0063296 23691013 PMC3654963 · DOI
  189. [201]Stuart LM Lucas M Simpson C Lamb J Savill J Lacy-Hulbert A. Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol. (2002) 168: 1627–35. doi: 10.4049/jimmunol.168.4.1627 11823490 · DOI
  190. [202]Feng H Zeng Y Whitesell L Katsanis E. Stressed apoptotic tumor cells express heat shock proteins and elicit tumor-specific immunity. Blood. (2001) 97: 3505–12. doi: 10.1182/blood.V97.11.3505 11369644 · DOI
  191. [203]Chen Z Moyana T Saxena A Warrington R Jia Z Xiang J. Efficient antitumor immunity derived from maturation of dendritic cells that had phagocytosed apoptotic/necrotic tumor cells. Int J Cancer. (2001) 93: 539–48. doi: 10.1002/(ISSN)1097-0215 11477558 · DOI
  192. [204]Penteado LA Dejani NN Verdan FF Orlando AB Nino VE Dias FN. Distinctive role of efferocytosis in dendritic cell maturation and migration in sterile or infectious conditions. Immunology. (2017) 151: 304–13. doi: 10.1111/imm.12731 PMC5461093 28267881 · DOI
  193. [206]Rodriguez-Fernandez S Pujol-Autonell I Brianso F Perna-Barrull D Cano-Sarabia M Garcia-Jimeno S. Phosphatidylserine-liposomes promote tolerogenic features on dendritic cells in human type 1 diabetes by apoptotic mimicry. Front Immunol. (2018) 9: 253. doi: 10.3389/fimmu.2018.00253 29491866 PMC5817077 · DOI
  194. [207]Sreeramkumar V Fresno M Cuesta N. Prostaglandin E2 and T cells: friends or foes? Immunol Cell Biol. (2012) 90: 579–86. doi: 10.1038/icb.2011.75 PMC3389798 21946663 · DOI
  195. [208]Valdez PA Vithayathil PJ Janelsins BM Shaffer AL Williamson PR Datta SK. Prostaglandin E2 suppresses antifungal immunity by inhibiting interferon regulatory factor 4 function and interleukin-17 expression in T cells. Immunity. (2012) 36: 668–79. doi: 10.1016/j.immuni.2012.02.013 PMC3334441 22464170 · DOI
  196. [209]Gorchs L Fernandez Moro C Bankhead P Kern KP Sadeak I Meng Q. Human pancreatic carcinoma-associated fibroblasts promote expression of co-inhibitory markers on CD4(+) and CD8(+) T-cells. Front Immunol. (2019) 10: 847. doi: 10.3389/fimmu.2019.00847 31068935 PMC6491453 · DOI
  197. [210]Boniface K Bak-Jensen KS Li Y Blumenschein WM McGeachy MJ McClanahan TK. Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling. J Exp Med. (2009) 206: 535–48. doi: 10.1084/jem.20082293 PMC2699124 19273625 · DOI
  198. [212]Amarilyo G Verbovetski I Atallah M Grau A Wiser G Gil O. iC3b-opsonized apoptotic cells mediate a distinct anti-inflammatory response and transcriptional NF-kappaB-dependent blockade. Eur J Immunol. (2010) 40: 699– 709. doi: 10.1002/eji.200838951 20039295 · DOI
  199. [213]Sohn JH Bora PS Suk HJ Molina H Kaplan HJ Bora NS. Tolerance is dependent on complement C3 fragment iC3b binding to antigen-presenting cells. Nat Med. (2003) 9: 206–12. doi: 10.1038/nm814 PMC1821085 12514742 · DOI
  200. [214]Ohl L Mohaupt M Czeloth N Hintzen G Kiafard Z Zwirner J. CCR7 governs skin dendritic cell migration under inflammatory and steady-state conditions. Immunity. (2004) 21: 279–88. doi: 10.1016/j.immuni.2004.06.014 15308107 · DOI · Paper page

200 of 273 shown

Cited by

Sorted by citations

Authors
Ma, Y., Jiang, T., Zhu, X., Xu, Y., Wan, K., Zhang, T., & Xie, M.
Affiliations
  • Capital Medical University (CN)
  • Shandong University (CN)
Corresponding author
Xie, Miaorong
Venue
Frontiers in Immunology
Published
2024-05-21
Volume
15
Pages
1415573-1415573
ISSN
1664-3224 (ISSN-L)
OpenAlex
W4398174391
Cited by
24
References
22
Citations by year
2026: 11 · 2025: 12 · 2024: 1
FWCI
1.06
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
General Hospital of People’s Liberation Army
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords
efferocytosis, dendritic cells, dendritic cell maturation, immune tolerance, macrophages, immune regulation, inflammation, dendritic cell subsets
MeSH terms
Efferocytosis, Animals, Dendritic Cells, Humans, Immune Tolerance, Macrophages, Phagocytosis, Apoptosis

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review