Diversity and versatility of phagocytosis: Roles in innate immunity, tissue remodeling, and homeostasis

Frontiers in Cellular and Infection Microbiology

Volumn 7, Issue MAY, 2017, Pages

  Lim, Justin J ^a   Grinstein, Sergio ^a,b,c   Roth, Ziv ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b ST MICHAEL'S HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Macrophage; Neutrophil; Phagocyte; Phagocytosis; Phagosome

Indexed keywords

MEMBRANE PROTEIN; OPSONIN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL DIFFERENTIATION; CELL PHAGOCYTOSIS; CHROMOSOME PAIRING; DENDRITIC CELL; ERYTHROCYTE LIFESPAN; ERYTHROPOIESIS; GLIA CELL; HOMEOSTASIS AND REGULATION; HUMAN; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MICROORGANISM; NERVOUS SYSTEM DEVELOPMENT; NEUTROPHIL; NONHUMAN; PHAGOLYSOSOME; SERTOLI CELL; SPERMATOGENESIS; TISSUE HOMEOSTASIS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; HOMEOSTASIS; IMMUNOLOGY; LYMPHOCYTE; MALE; PHAGOCYTE; PHAGOCYTOSIS; PHAGOSOME; PHYSIOLOGY; PSYCHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; CELL LINE, TUMOR; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; LYMPHOCYTES; MALE; NEUROGENESIS; NEUTROPHILS; PHAGOCYTES; PHAGOCYTOSIS; PHAGOSOMES; SERTOLI CELLS; SIGNAL TRANSDUCTION; SPERMATOGENESIS;

EID: 85027523475     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2017.00191     Document Type: Article

References (128)

1. Aida, Y., and Pabst, M. J. (1990). Priming of neutrophils by lipopolysaccharide for enhanced release of superoxide. Requirement for plasma but not for tumor necrosis factor-alpha. J. Immunol. 145, 3017–3025.
2. Antonelou, M. H., Kriebardis, A. G., and Papassideri, I. S. (2010). Aging and death signalling in mature red cells: from basic science to transfusion practice. Blood Transfus. 8, 39–47. doi: 10.2450/2010.007S
3. Arandjelovic, S., and Ravichandran, K. S. (2015). Phagocytosis of apoptotic cells in homeostasis. Nat. Immunol. 16, 907–917. doi: 10.1038/ni.3253
4. Arese, P., Turrini, F., and Schwarzer, E. (2005). Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell. Physiol. Biochem. 16, 133–146. doi: 10.1159/000089839
5. Awasaki, T., and Ito, K. (2004). Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Curr. Biol. 14, 668–677. doi: 10.1016/j.cub.2004.04.001
6. Barrionuevo, F., Burgos, M., and Jiménez, R. (2011). Origin and function of embryonic Sertoli cells. Biomol. Concepts 2, 537–547. doi: 10.1515/BMC.2011.044
7. Boas, F. E., Forman, L., and Beutler, E. (1998). Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc. Natl. Acad. Sci. U.S.A. 95, 3077–3081. doi: 10.1073/pnas.95.6.3077
8. Braun, S. M. G., and Jessberger, S. (2014). Adult neurogenesis: mechanisms and functional significance. Development 141, 1983–1986. doi: 10.1242/dev.104596
9. Brown, G. C., and Neher, J. J. (2012). Eaten alive! Cell death by primary phagocytosis: “phagoptosis.” Trends Biochem. Sci. 37, 325–332. doi: 10.1016/j.tibs.2012.05.002
10. Butterfield, T. A., Best, T. M., and Merrick, M. A. (2006). The dual roles of neutrophils and macrophages in inflammation: a critical balance between tissue damage and repair. J. Athl. Train. 41, 457–465. doi: 10.1016/S0162-0908(08)79217-1
11. Campbell, F. R. (1968). Nuclear elimination from the normoblast of fetal guinea pig liver as studied with electron microscopy and serial sectioning techniques. Anat. Rec. 160, 539–554. doi: 10.1002/ar.1091600304
12. Canton, J., Khezri, R., Glogauer, M., and Grinstein, S. (2014). Contrasting phagosome pH regulation and maturation in human M1 and M2 macrophages. Mol. Biol. Cell 25, 3330–3341. doi: 10.1091/mbc.E14-05-0967
13. Chanmee, T., Ontong, P., Konno, K., and Itano, N. (2014). Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel). 6, 1670–1690. doi: 10.3390/cancers6031670
14. Chao, M. P., Jaiswal, S., Weissman-Tsukamoto, R., Alizadeh, A. A., Gentles, A. J., Volkmer, J., et al. (2010). Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci. Transl. Med. 2, 63ra94. doi: 10.1126/scitranslmed.3001375
15. Chen, Q., Zhang, X. H.-F., and Massagué, J. (2011). Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20, 538–549. doi: 10.1016/j.ccr.2011.08.025
16. Connor, J., Pak, C. C., and Schroit, A. J. (1994). Exposure of phosphatidylserine in the outer leaflet of human red blood cells: relationship to cell density, cell age, and clearance by mononuclear cells. J. Biol. Chem. 269, 2399–2404.
17. Cox, G., Crossley, J., and Xing, Z. (1995). Macrophage engulfment of apoptotic neutrophils contributes to the resolution of acute pulmonary inflammation in vivo. Am. J. Respir. Cell Mol. Biol. 12, 232–237. doi: 10.1165/ajrcmb.12.2.7865221
18. Crehan, H., Hardy, J., and Pocock, J. (2013). Blockage of CR1 prevents activation of rodent microglia. Neurobiol. Dis. 54, 139–149. doi: 10.1016/j.nbd.2013.02.003
19. Cresswell, P. (1994). Assembly, transport, and function of MHC class II molecules. Annu. Rev. Immunol. 12, 259–293. doi: 10.1146/annurev.iy.12.040194.001355
20. de Back, D. Z., Kostova, E. B., van Kraaij, M., van den Berg, T. K., and van Bruggen, R. (2014). Of macrophages and red blood cells; a complex love story. Front. Physiol. 5:9. doi: 10.3389/fphys.2014.00009
21. Delamarre, L., Pack, M., Chang, H., Mellman, I., and Trombetta, E. S. (2005). Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307, 1630–1634. doi: 10.1126/science.1108003
22. Doherty, J., Logan, M. A., Taademir, O. E., and Freeman, M. R. (2009). Ensheathing glia function as phagocytes in the adult Drosophila brain. J. Neurosci. 29, 4768–4781. doi: 10.1523/JNEUROSCI.5951-08.2009
23. Dzierzak, E., and Philipsen, S. (2013). Erythropoiesis: development and differentiation. Cold Spring Harb. Perspect. Med. 3:a011601. doi: 10.1101/cshperspect.a011601
24. 3 ). J. Immunol. 161, 6250–6257.
25. Faurschou, M., and Borregaard, N. (2003). Neutrophil granules and secretory vesicles in inflammation. Microbes Infect. 5, 1317–1327. doi: 10.1016/j.micinf.2003.09.008
26. Feng, Y., andMao, H. (2012). Expression and preliminary functional analysis of Siglec-F on mouse macrophages. J. Zhejiang Univ. Sci. B 13, 386–394. doi: 10.1631/jzus.B1100218
27. Freeman, S. A., and Grinstein, S. (2014). Phagocytosis: receptors, signal integration, and the cytoskeleton. Immunol. Rev. 262, 193–215. doi: 10.1111/imr.12212
28. Gabillet, J., Millet, A., Pederzoli-Ribeil, M., Tacnet-Delorme, P., Guillevin, L., Mouthon, L., et al. (2012). Proteinase 3, the autoantigen in granulomatosis with polyangiitis, associates with calreticulin on apoptotic neutrophils, impairs macrophage phagocytosis, and promotes inflammation. J. Immunol. 189, 2574–2583. doi: 10.4049/jimmunol.1200600
29. Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., et al. (2005). Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321–334. doi: 10.1016/j.cell.2005.08.032
30. Garrett, W. S., Chen, L. M., Kroschewski, R., Ebersold, M., Turley, S., Trombetta, S., et al. (2000). Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102, 325–334. doi: 10.1016/S0092-8674(00)00038-6
31. Gattegno, L., Saffar, L., and Vaysse, J. (1989). Inhibition by monoclonal anticomplement receptor type 1 on interactions between senescent human red blood cells and monocytic-macrophagic cells. J. Leukoc. Biol. 45, 422–428.
32. Gayen Betal, S., and Setty, B. N. Y. (2008). Phosphatidylserine-positive erythrocytes bind to immobilized and soluble thrombospondin-1 via its heparin-binding domain. Transl. Res. 152, 165–177. doi: 10.1016/j.trsl.2008.07.007
33. Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., et al. (2015). Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518, 547–551. doi: 10.1038/nature13989
34. Gordon, S. (2008). Elie metchnikoff: father of natural immunity. Eur. J. Immunol. 38, 3257–3264. doi: 10.1002/eji.200838855
35. Gordon, S. (2016). Phagocytosis: an Immunobiologic Process. Immunity 44, 463–475. doi: 10.1016/j.immuni.2016.02.026
36. Goswami, S., Sahai, E., Wyckoff, J. B., Cammer, M., Cox, D., Pixley, F. J., et al. (2005). Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 65, 5278–5283. doi: 10.1158/0008-5472.CAN-04-1853
37. Griswold, M. D. (1998). The central role of Sertoli cells in spermatogenesis. Semin. Cell Dev. Biol. 9, 411–416. doi: 10.1006/scdb.1998.0203
38. Guermonprez, P., Valladeau, J., Zitvogel, L., Théry, C., and Amigorena, S. (2002). Antigen presentation and T cell stimulation by dendritic cells. Annu. Rev. Immunol. 20, 621–667. doi: 10.1146/annurev.immunol.20.100301.064828
39. Guilliams, M., Bruhns, P., Saeys, Y., Hammad, H., and Lambrecht, B. N. (2014). The function of Fcγ receptors in dendritic cells and macrophages. Nat. Rev. Immunol. 14, 94–108. doi: 10.1038/nri3582
40. Guilliams, M., De Kleer, I., Henri, S., Post, S., Vanhoutte, L., De Prijck, S., et al. (2013). Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210, 1977–1992. doi: 10.1084/jem.20131199
41. Guth, A. M., Janssen, W. J., Bosio, C. M., Crouch, E. C., Henson, P. M., and Dow, S. W. (2009). Lung environment determines unique phenotype of alveolar macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 296, L936–L946. doi: 10.1152/ajplung.90625.2008
42. Hanna, R. N., Cekic, C., Sag, D., Tacke, R., Thomas, G. D., Nowyhed, H., et al. (2015). Patrolling monocytes control tumor metastasis to the lung. Science 350, 985–990. doi: 10.1126/science.aac9407
43. Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M. B., Leboeuf, M., et al. (2013). Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38, 792–804. doi: 10.1016/j.immuni.2013.04.004
44. Haslett, C. (1992). Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes. Clin. Sci. 83, 639–648. doi: 10.1042/cs0830639
45. Haslett, C., Savill, J. S., Whyte, M. K., Stern, M., Dransfield, I., and Meagher, L. C. (1994). Granulocyte apoptosis and the control of inflammation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 345, 327–333. doi: 10.1098/rstb.1994.0113
46. Hentze, M. W., Muckenthaler, M. U., Galy, B., and Camaschella, C. (2010). Two to tango: regulation of mammalian iron metabolism. Cell 142, 24–38. doi: 10.1016/j.cell.2010.06.028
47. Hernandez, L., Smirnova, T., Kedrin, D., Wyckoff, J., Zhu, L., Stanley, E. R., et al. (2009). The EGF/CSF-1 paracrine invasion loop can be triggered by heregulin beta1 and CXCL12. Cancer Res. 69, 3221–3227. doi: 10.1158/0008-5472.CAN-08-2871
48. Hochreiter-Hufford, A., and Ravichandran, K. S. (2013). Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb. Perspect. Biol. 5:a008748. doi: 10.1101/cshperspect.a008748
49. Hoffmann, J. J. M. L. (2009). Neutrophil CD64 : a diagnostic marker for infection and sepsis. Clin. Chem. Lab. Med. 47, 903–916. doi: 10.1515/cclm.2009.224
50. Huckins, C. (1978). The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anat. Rec. 190, 905–926. doi: 10.1002/ar.1091900410
51. Hussell, T., and Bell, T. J. (2014). Alveolar macrophages: plasticity in a tissue-specific context. Nat. Rev. Immunol. 14, 81–93. doi: 10.1038/nri3600
52. Huttenlocher, P. R., and Dabholkar, A. S. (1997). Regional differences in synaptogenesis in human cerebral cortex. J. Comp. Neurol. 387, 167–178. doi: 10.1002/(sici)1096-9861(19971020)387:2<167::aid-cne1>3.0.co;2-z
53. Ishii, Y., Hashimoto, K., Nomura, A., Sakamoto, T., Uchida, Y., Ohtsuka, M., et al. (1998). Elimination of neutrophils by apoptosis during the resolution of acute pulmonary inflammation in rats. Lung 176, 89–98. doi: 10.1007/PL000 07597
54. Joffre, O. P., Segura, E., Savina, A., and Amigorena, S. (2012). Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12, 557–569. doi: 10.1038/nri3254
55. Kannan, R., Yuan, J., and Low, P. S. (1991). Isolation and partial characterization of antibody- and globin-enriched complexes from membranes of dense human erythrocytes. Biochem. J. 278 (Pt 1), 57–62. doi: 10.1042/bj2780057
56. Kawane, K., Fukuyama, H., Kondoh, G., Takeda, J., Ohsawa, Y., Uchiyama, Y., et al. (2001). Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292, 1546–1549. doi: 10.1126/science.292.5521.1546
57. Kawasaki, Y., Nakagawa, A., Nagaosa, K., Shiratsuchi, A., and Nakanishi, Y. (2002). Phosphatidylserine binding of class B scavenger receptor type I, a phagocytosis receptor of testicular sertoli cells. J. Biol. Chem. 277, 27559–27566. doi: 10.1074/jbc.M202879200
58. Kerscher, B., Willment, J. A., and Brown, G. D. (2013). The Dectin-2 family of C-type lectin-like receptors: an update. Int. Immunol. 25, 271–277. doi: 10.1093/intimm/dxt006
59. Kettenmann, H., Hanisch, U.-K., Noda, M., and Verkhratsky, A. (2011). Physiology of microglia. Physiol. Rev. 91, 461–553. doi: 10.1152/physrev.00011. 2010
60. Khandelwal, S., Van Rooijen, N., and Saxena, R. K. (2007). Reduced expression of CD47 during murine red blood cell (RBC) senescence and its role in RBC clearance from the circulation. Transfusion 47, 1725–1732. doi: 10.1111/j.1537-2995.2007.01348.x
61. Khwaja, A., Carver, J. E., and Linch, D. C. (1992). Interactions of granulocytemacrophage colony-stimulating factor (CSF), granulocyte CSF, and tumor necrosis factor alpha in the priming of the neutrophil respiratory burst. Blood 79, 745–753.
62. Kimura, Y., Inoue, A., Hangai, S., Saijo, S., Negishi, H., Nishio, J., et al. (2016). The innate immune receptor Dectin-2 mediates the phagocytosis of cancer cells by Kupffer cells for the suppression of liver metastasis. Proc. Natl. Acad. Sci. U.S.A. 113, 14097–14102. doi: 10.1073/pnas.1617903113
63. Kinchen, J. M., and Ravichandran, K. S. (2008). Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9, 781–795. doi: 10.1038/nrm2515
64. Knapp, S., Leemans, J. C., Florquin, S., Branger, J., Maris, N. A., Pater, J., et al. (2003). Alveolar macrophages have a protective antiinflammatory role during murine pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 167, 171–179. doi: 10.1164/rccm.200207-698OC
65. Koh, T. J., and DiPietro, L. A. (2011). Inflammation and wound healing: the role of the macrophage. Expert Rev. Mol. Med. 13:e23. doi: 10.1017/S1462399411001943
66. Kolaczkowska, E., and Kubes, P. (2013). Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175. doi: 10.1038/nri3399
67. Korotzer, A. R., Watt, J., Cribbs, D., Tenner, A. J., Burdick, D., Glabe, C., et al. (1995). Cultured rat microglia express C1q and receptor for C1q: implications for amyloid effects on microglia. Exp. Neurol. 134, 214–221. doi: 10.1006/exnr.1995.1051
68. Lee, S. J., Park, S. Y., Jung, M. Y., Bae, S. M., and Kim, I. S. (2011). Mechanism for phosphatidylserine-dependent erythrophagocytosis in mouse liver. Blood 117, 5215–5223. doi: 10.1182/blood-2010-10-313239
69. Levin, R., Grinstein, S., and Canton, J. (2016). The life cycle of phagosomes: formation, maturation, and resolution. Immunol. Rev. 273, 156–179. doi: 10.1111/imr.12439
70. Lin, Z., Schmidt, C. Q., Koutsogiannaki, S., Ricci, P., Risitano, A. M., Lambris, J. D., et al. (2015). Complement C3dg-mediated erythrophagocytosis: implications for paroxysmal nocturnal hemoglobinuria. Blood 126, 891–894. doi: 10.1182/blood-2015-02-625871
71. London, A., Cohen, M., and Schwartz, M. (2013). Microglia and monocyte-derived macrophages: functionally distinct populations that act in concert in CNS plasticity and repair. Front. Cell. Neurosci. 7:34. doi: 10.3389/fncel.2013.00034
72. Low, L. K., and Cheng, H.-J. (2006). Axon pruning: an essential step underlying the developmental plasticity of neuronal connections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1531–1544. doi: 10.1098/rstb.2006.1883
73. Lu, Z., Elliott, M. R., Chen, Y., Walsh, J. T., Klibanov, A. L., Ravichandran, K. S., et al. (2011). Phagocytic activity of neuronal progenitors regulates adult neurogenesis. Nat. Cell Biol. 13, 1076–1083. doi: 10.1038/ncb2299
74. Luo, C., Koyama, R., and Ikegaya, Y. (2016). Microglia engulf viable newborn cells in the epileptic dentate gyrus. Glia 64, 1508–1517. doi: 10.1002/glia.23018
75. Lutz, H. U., Bussolino, F., Flepp, R., Fasler, S., Stammler, P., Kazatchkine, M. D., et al. (1987). Naturally occurring anti-band-3 antibodies and complement together mediate phagocytosis of oxidatively stressed human erythrocytes. Proc. Natl. Acad. Sci. U.S.A. 84, 7368–7372. doi: 10.1073/pnas.84.21.7368
76. Lutz, H. U., Stammler, P., and Fasler, S. (1990). How naturally occurring anti-band 3 antibodies stimulate C3b deposition to senescent and oxidatively stressed red blood cells. Biomed. Biochim. Acta 49, S224–S229.
77. Mallat, M., Marín-Teva, J. L., and Chéret, C. (2005). Phagocytosis in the developing CNS: more than clearing the corpses. Curr. Opin. Neurobiol. 15, 101–107. doi: 10.1016/j.conb.2005.01.006
78. Manwani, D., and Bieker, J. J. (2008). The Erythroblastic island. Curr. Top. Dev. Biol. 82, 23–53. doi: 10.1016/S0070-2153(07)00002-6
79. Mayer-Scholl, A., Averhoff, P., and Zychlinsky, A. (2004). How do neutrophils and pathogens interact? Curr. Opin. Microbiol. 7, 62–66. doi: 10.1016/j.mib.2003.12.004
80. McEvoy, L., Williamson, P., and Schlegel, R. A. (1986). Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc. Natl. Acad. Sci. U.S.A. 83, 3311–3315. doi: 10.1073/pnas.83.10.3311
81. Misharin, A. V., Morales-Nebreda, L., Mutlu, G. M., Budinger, G. R. S., and Perlman, H. (2013). Flow cytometric analysis of macrophages and dendritic cell subsets in the mouse lung. Am. J. Respir. Cell Mol. Biol. 49, 503–510. doi: 10.1165/rcmb.2013-0086MA
82. Mohandas, N., and Prenant, M. (1978). Three-dimensional model of bone marrow. Blood 51, 633–643.
83. Mukherjee, R., Kanti Barman, P., Kumar Thatoi, P., Tripathy, R., Kumar Das, B., and Ravindran, B. (2015). Non-classical monocytes display inflammatory features: validation in sepsis and systemic lupus erythematous. Sci. Rep. 5, 138–186. doi: 10.1038/srep13886
84. Nagl, M., Kacani, L., Müllauer, B., Lemberger, E.-M., Stoiber, H., Sprinzl, G. M., et al. (2002). Phagocytosis and killing of bacteria by professional phagocytes and dendritic cells. Clin. Diagn. Lab. Immunol. 9, 1165–1168. doi: 10.1128/cdli.9.6.1165-1168.2002
85. Nakagawa, A., Shiratsuchi, A., Tsuda, K., and Nakanishi, Y. (2005). In vivo analysis of phagocytosis of apoptotic cells by testicular Sertoli cells. Mol. Reprod. Dev. 71, 166–177. doi: 10.1002/mrd.20278
86. Nakanishi, Y., and Shiratsuchi, A. (2004). Phagocytic removal of apoptotic spermatogenic cells by Sertoli cells: mechanisms and consequences. Biol. Pharm. Bull. 27, 13–16. doi: 10.1248/bpb.27.13
87. Olsson, M., and Oldenborg, P. A. (2008). CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcγ receptor-mediated but not scavenger receptor-mediated recognition by macrophages. Blood 112, 4259–4267. doi: 10.1182/blood-2008-03-143008
88. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456–1458. doi: 10.1126/science.1202529
89. Petanjek, Z., Judas, M., Simic, G., Rasin, M. R., Uylings, H. B. M., Rakic, P., et al. (2011). Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 108, 13281–13286. doi: 10.1073/pnas.1105108108
90. Platt, C. D., Ma, J. K., Chalouni, C., Ebersold, M., Bou-Reslan, H., Carano, R. A. D., et al. (2010). Mature dendritic cells use endocytic receptors to capture and present antigens. Proc. Natl. Acad. Sci. U.S.A. 107, 4287–4292. doi: 10.1073/pnas.0910609107
91. Potter, P. K., Cortes-Hernandez, J., Quartier, P., Botto, M., and Walport, M. J. (2003). Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170, 3223–3232. doi: 10.4049/jimmunol.170.6.3223
92. Prince, L. R., Whyte, M. K., Sabroe, I., and Parker, L. C. (2011). The role of TLRs in neutrophil activation. Curr. Opin. Pharmacol. 11, 397–403. doi: 10.1016/j.coph.2011.06.007
93. Psaila, B., Barkas, N., Iskander, D., Roy, A., Anderson, S., Ashley, N., et al. (2016). Single-cell profiling of human megakaryocyte-erythroid progenitors identifies distinct megakaryocyte and erythroid differentiation pathways. Genome Biol. 17:83. doi: 10.1186/s13059-016-0939-7
94. Qiu, L. B., Dickson, H., Hajibagheri, N., and Crocker, P. R. (1995). Extruded erythroblast nuclei are bound and phagocytosed by a novel macrophage receptor. Blood 85, 1630–1639.
95. Rabinovitch, M. (1995). Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 5, 85–87. doi: 10.1016/S0962-8924(00)88955-2
96. Russell, L. D., Chiarini-Garcia, H., Korsmeyer, S. J., and Knudson, C. M. (2002). Bax-dependent spermatogonia apoptosis is required for testicular development and spermatogenesis. Biol. Reprod. 66, 950–958. doi: 10.1095/biolreprod66.4.950
97. Sambrano, G. R., Parthasarathy, S., and Steinberg, D. (1994). Recognition of oxidatively damaged erythrocytes by a macrophage receptor with specificity for oxidized low density lipoprotein. Proc. Natl. Acad. Sci. U.S.A. 91, 3265–3269. doi: 10.1073/pnas.91.8.3265
98. Sasaki, K., Iwatsuki, H., Suda, M., and Itano, C. (1993a). Cell death and phagocytosis of haematopoietic elements at the onset of haematopoiesis in the mouse spleen: an ultrastructural study. J. Anat. 183(Pt 1), 113–20.
99. Sasaki, K., Iwatsuki, H., Suda, M., and Itano, C. (1993b). Scavenger macrophages and central macrophages of erythroblastic islands in liver hemopoiesis of the fetal and early postnatal mouse: a semithin light-and electron-microscopic study. Acta Anat. (Basel). 147, 75–82. doi: 10.1159/000147485
100. Savill, J., Dransfield, I., Hogg, N., and Haslett, C. (1990). Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 170–173. doi: 10.1038/343170a0
101. Savill, J., Hogg, N., Ren, Y., and Haslett, C. (1992). Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513–1522. doi: 10.1172/JCI116019
102. Savill, J. S., Wyllie, A. H., Henson, J. E., Walport, M. J., Henson, P. M., and Haslett, C. (1989). Macrophage phagocytosis of aging neutrophils in inflammation. Programmed cell death in the neutrophil leads to its recognition by macrophages. J. Clin. Invest. 83, 865–875. doi: 10.1172/JCI113970
103. Savina, A., and Amigorena, S. (2007). Phagocytosis and antigen presentation in dendritic cells. Immunol. Rev. 219, 143–156. doi: 10.1111/j.1600-065X.2007.00552.x
104. Savina, A., Jancic, C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., et al. (2006). NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126, 205–218. doi: 10.1016/j.cell.2006.05.035
105. Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., et al. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691–705. doi: 10.1016/j.neuron.2012.03.026
106. Schraml, B. U., and Reis e Sousa, C. (2015). Defining dendritic cells. Curr. Opin. Immunol. 32, 13–20. doi: 10.1016/j.coi.2014.11.001
107. Segal, A. W., Dorling, J., andCoade, S. (1980). Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes. Biochemical and morphological studies. J. Cell Biol. 85, 42–59. doi: 10.1083/jcb.85.1.42
108. Shaha, C., Tripathi, R., and Mishra, D. P. (2010). Male germ cell apoptosis: regulation and biology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1501–1515. doi: 10.1098/rstb.2009.0124
109. Shaykhiev, R., Krause, A., Salit, J., Strulovici-Barel, Y., Harvey, B.-G., O'Connor, T. P., et al. (2009). Smoking-dependent reprogramming of alveolar macrophage polarization: implication for pathogenesis of chronic obstructive pulmonary disease. J. Immunol. 183, 2867–2883. doi: 10.4049/jimmunol.0900473
110. Shiratsuchi, A., Umeda, M., Ohba, Y., and Nakanishi, Y. (1997). Recognition of phosphatidylserine on the surface of apoptotic spermatogenic cells and subsequent phagocytosis by sertoli cells of the rat. J. Biol. Chem. 272, 2354–2358. doi: 10.1074/jbc.272.4.2354
111. Sierra, A., Encinas, J. M., Deudero, J. J. P., Chancey, J. H., Enikolopov, G., Overstreet-Wadiche, L. S., et al. (2010). Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7, 483–495. doi: 10.1016/j.stem.2010.08.014
112. Skutelsky, E., and Danon, D. (1969). Reduction in surface charge as an explanation of the recognition by macrophages of nuclei expelled from normoblasts. J. Cell Biol. 43, 8–15. doi: 10.1083/jcb.43.1.8
113. Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., et al. (2007). The classical complement cascade mediates CNS synapse elimination. Cell 131, 1164–1178. doi: 10.1016/j.cell.2007.10.036
114. Tang, G., Gudsnuk, K., Kuo, S. H., Cotrina, M. L., Rosoklija, G., Sosunov, A., et al. (2014). Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 83, 1131–1143. doi: 10.1016/j.neuron.2014.07.040
115. Terpstra, V., and van Berkel, T. J. C. (2000). Scavenger receptors on liver Kupffer cells mediate the in vivo uptake of oxidatively damaged red blood cells in mice. Blood 95, 2157–2163. doi: 10.1073/pnas.83.5.1339
116. Theurl, I., Hilgendorf, I., Nairz, M., Tymoszuk, P., Haschka, D., Asshoff, M., et al. (2016). On-demand erythrocyte disposal and iron recycling requires transient macrophages in the liver. Nat. Med. 22, 945–951. doi: 10.1038/nm.4146
117. Tollis, S., Dart, A. E., Tzircotis, G., and Endres, R. G. (2010). The zipper mechanism in phagocytosis: energetic requirements and variability in phagocytic cup shape. BMC Syst. Biol. 4:149. doi: 10.1186/1752-0509-4-149
118. Torre, D., Gennero, L., Baccino, F. M., Speranza, F., Biondi, G., and Pugliese, A. (2002). Impaired macrophage phagocytosis of apoptotic neutrophils in patients with human immunodeficiency virus type 1 infection. Clin. Diagn. Lab. Immunol. 9, 983–986. doi: 10.1128/cdli.9.5.983-986.2002
119. van Kessel, K. P. M., Bestebroer, J., and van Strijp, J. A. G. (2014). Neutrophil-Mediated Phagocytosis of Staphylococcus aureus. Front. Immunol. 5:467. doi: 10.3389/fimmu.2014.00467
120. Vijayan, D., Radford, K. J., Beckhouse, A. G., Ashman, R. B., and Wells, C. A. (2012). Mincle polarizes human monocyte and neutrophil responses to Candida albicans. Immunol. Cell Biol. 90, 889–895. doi: 10.1038/icb.2012.24
121. Visser, C. E., Steenbergen, J. J., Betjes, M. G., Meijer, S., Arisz, L., Hoefsmit, E. C., et al. (1995). Interleukin-8 production by human mesothelial cells after direct stimulation with staphylococci. Infect. Immun. 63, 4206–4209.
122. Wake, H., Moorhouse, A. J., Jinno, S., Kohsaka, S., and Nabekura, J. (2009). Resting microglia directly monitor the functional state of synapses in vivo and determine the fate of ischemic terminals. J. Neurosci. 29, 3974–3980. doi: 10.1523/JNEUROSCI.4363-08.2009
123. Watts, R. J., Schuldiner, O., Perrino, J., Larsen, C., and Luo, L. (2004). Glia engulf degenerating axons during developmental axon pruning. Curr. Biol. 14, 678–684. doi: 10.1016/j.cub.2004.03.035
124. Wynn, T. A., and Vannella, K. M. (2016). Macrophages in tissue repair, regeneration, and fibrosis. Immunity 44, 450–462. doi: 10.1016/j.immuni.2016.02.015
125. Yoshida, H., Kawane, K., Koike, M., Mori, Y., Uchiyama, Y., and Nagata, S. (2005). Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437, 754–758. doi: 10.1038/nature03964
126. Yuan, A., Hsiao, Y.-J, Chen, H.-Y., Chen, H.-W., Ho, C.-C., Chen, Y.-Y., et al. (2015). Opposite effects of M1 and M2 macrophage subtypes on lung cancer progression. Sci. Rep. 5:14273. doi: 10.1038/srep14273
127. Zaynagetdinov, R., Sherrill, T. P., Kendall, P. L., Segal, B. H., Weller, K. P., Tighe, R. M., et al. (2013). Identification of myeloid cell subsets in murine lungs using flow cytometry. Am. J. Respir. Cell Mol. Biol. 49, 180–189. doi: 10.1165/rcmb.2012-0366MA
128. hi CD16+ monocytes phagocytose antibody-opsonised Plasmodium falciparum infected erythrocytes more efficiently than other monocyte subsets, and require CD16 and complement to do so. BMC Med. 13:154. doi: 10.1186/s12916-015-0391-7