Macrophage complement receptors and pathogen clearance
Open accessAbstract
Phagocytosis, an important mechanism of the host-defence system and a primary function of macrophages, is facilitated by opsonization, a process by which serum components tag pathogens for recognition by neutrophils and macrophages. Complement component C3 is central to opsonization. Its first cleavage product, C3b, forms the multisubunit enzyme, C3bBb, which proteolytically cleaves additional C3 molecules on the pathogen surface. C3b is further degraded to iC3b, C3c and C3dg, products that serve as ligands for selective complement receptors on leukocytes. This receptor-ligand interaction subsequently modulates immune responses or directly targets the pathogen for clearance by phagocytosis. Although a central role for C3 in phagocytosis of certain pathogens is well accepted, the receptors orchestrating the phagocytic response have not been well characterized. The recent structures of C3 and its breakdown products have increased our insights into the molecular basis of complement activation and recognition by their receptors. Here we review the biology of macrophage receptors for C3 fragments and discuss their role in the host response to pathogens.
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In the immune system, C3 is cleaved into an activated form, iC3b, which covalently binds to the surface of cells or debris and targets them for elimination by macrophages via specific phagocytic receptor signaling (e.g., CR3).
“In the immune system, C3 is cleaved into an activated form, iC3b, which covalently binds to the surface of cells or debris and targets them for elimination by macrophages via specific phagocytic receptor signaling (e.g., CR3) (Lambris and Tsokos, 1986; van Lookeren Campagne et al., 2007).”
From Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner (2012) · cites this paper as van Lookeren Campagne et al., 2007
The “Complement C3 opsonization” section says C3 is first cleaved to C3b, which covalently binds a surface; subsequent cleavage of bound C3b produces iC3b. The receptor sections support iC3b recognition and phagocytosis through CR3, but the claim incorrectly presents iC3b as the direct product of C3 cleavage and the form that initially binds covalently. The discussion of cell-debris removal identifies CRIg as a possible receptor, rather than specifically CR3. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAnaphylatoxin C3a and C5a function as chemoattractants for neutrophils, macrophages, astrocytes, and microglia.
“Anaphylatoxin C3a and C5a—downstream products of the complement pathway [211]—function as chemoattractants for neutrophils [212], macrophages [213], astrocytes [214], and microglia [215–217] (Fig. 4B&G).”
From Oligodendrocyte death and myelin loss in the cuprizone model: an updated overview of the intrinsic and extrinsic causes of cuprizone demyelination (2022) · cites this paper as [213]
Citation [213] is attached specifically to macrophages. The ‘Complement C3 opsonization’ section identifies C3a as a product of C3 cleavage, and ‘The role of CR3 and CRIg in complement-mediated phagocytosis’ discusses macrophage receptors and leukocyte trafficking. Neither passage says that C3a or C5a attracts macrophages; searches for C5a, chemotaxis, and anaphylatoxin-mediated recruitment found no such statement. Page numbers were not available in our copy. (LLM, conf=0.75)
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1 retracted
The structure of complement C3b provides insights into complement activation and regulation
Ajees, A. A., Gunasekaran, K., Volanakis, J. E., Narayana, S. V. L., Kotwal, G. J., & Murthy, H. M. K. (2006) · Nature · doi:10.1038/nature05258 · Cited by 70 · see citing works
RetractedWalport, M. J. (2001) · New England Journal of Medicine · doi:10.1056/nejm200104053441406 · Cited by 2,921 · see citing works
Mechanisms of phagocytosis in macrophages
Aderem, A., & Underhill, D. M. (1999) · Annual Review of Immunology · doi:10.1146/annurev.immunol.17.1.593 · Cited by 2,854 · see citing works
Structural Basis of Integrin Regulation and Signaling
Luo, B., Carman, C. V., & Springer, T. A. (2007) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141618 · Cited by 1,662 · see citing works
MACROPHAGE RECEPTORS AND IMMUNE RECOGNITION
Taylor, P. R., Martínez‐Pomares, L., Stacey, M. A., Lin, H.-H., Brown, G. D., & Gordon, S. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115816 · Cited by 1,325 · see citing works
Phagocytosis of Microbes: Complexity in Action
Underhill, D. M., & Ozinsky, A. (2002) · Annual Review of Immunology · doi:10.1146/annurev.immunol.20.103001.114744 · Cited by 1,124 · see citing works
Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases
Caron, E., & Hall, A. (1998) · Science · doi:10.1126/science.282.5394.1717 · Cited by 1,019 · see citing works
ICAM-1 (CD54): a counter-receptor for Mac-1 (CD11b/CD18).
Diamond, M., Staunton, D. E., de Fougerolles, A. R., Stacker, S. A., García‐Aguilar, J., Hibbs, M. L., & Springer, T. A. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.111.6.3129 · Cited by 881 · see citing works
Role of Kupffer cells in host defense and liver disease
Bilzer, M., Roggel, F., & Gerbes, A. L. (2006) · Liver International · doi:10.1111/j.1478-3231.2006.01342.x · Cited by 857 · see citing works
Stuart, L. M., & Ezekowitz, R. A. B. (2005) · Immunity · doi:10.1016/j.immuni.2005.05.002 · Cited by 667 · see citing works
CRIg: A Macrophage Complement Receptor Required for Phagocytosis of Circulating Pathogens
Helmy, K. Y., Katschke, K. J., Gorgani, N. N., Kljavin, N. M., Elliott, J. M., Diehl, L. J., Scales, S. J., Ghilardi, N., & Campagne, M. V. L. (2006) · Cell · doi:10.1016/j.cell.2005.12.039 · Cited by 629 · see citing works
Structures of complement component C3 provide insights into the function and evolution of immunity
Janssen, B. J. C., Huizinga, E. G., Raaijmakers, H. C. A., Roos, A., Daha, M. R., Nilsson‐Ekdahl, K., Nilsson, B., & Gros, P. (2005) · Nature · doi:10.1038/nature04005 · Cited by 542 · see citing works
Ahearn, J. M., Fischer, M. B., Croix, D., Goerg, S., Ma, M., Xia, J., Zhou, X., Howard, R. G., Rothstein, T. L., & Carroll, M. C. (1996) · Immunity · doi:10.1016/s1074-7613(00)80433-1 · Cited by 480 · see citing works
Markedly impaired humoral immune response in mice deficient in complement receptors 1 and 2.
Molina, H. D., Holers, V. M., Li, B., Fung, Y., Mariathasan, S., Goellner, J. J., Strauss‐Schoenberger, J., Karr, R. W., & Chaplin, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3357 · Cited by 465 · see citing works
Structure of C3b reveals conformational changes that underlie complement activity
Janssen, B. J. C., Christodoulidou, A., McCarthy, A. A., Lambris, J. D., & Gros, P. (2006) · Nature · doi:10.1038/nature05172 · Cited by 369 · see citing works
Conlan, J. W., & North, R. J. (1994) · The Journal of Experimental Medicine · doi:10.1084/jem.179.1.259 · Cited by 344 · see citing works
Zhou, M., & Brown, E. J. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.6.1407 · Cited by 324 · see citing works
Self-citationFocal Exocytosis of Vamp3-Containing Vesicles at Sites of Phagosome Formation
Bajno, L., Peng, X., Schreiber, A. D., Moore, H.-P. H., Trimble, W. S., & Grinstein, S. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.149.3.697 · Cited by 319 · see citing works
Membrane Complement Receptors Specific for Bound Fragments of C3
Ross, G. D., & Medof, M. E. (1985) · Advances in immunology · doi:10.1016/s0065-2776(08)60341-7 · Cited by 309 · see citing works
Matsumoto, A. K., Kopicky-Burd, J. A., Carter, R. H., Tuveson, D. A., Tedder, T. F., & Fearon, D. T. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.173.1.55 · Cited by 305 · see citing works
Integrin activation takes shape
Liddington, R., & Ginsberg, M. H. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200206011 · Cited by 303 · see citing works
Benacerraf, B., Sebestyen, M. M., & Schlossman, S. F. (1959) · The Journal of Experimental Medicine · doi:10.1084/jem.110.1.27 · Cited by 275 · see citing works
VSIG4, a B7 family-related protein, is a negative regulator of T cell activation
Vogt, L., Schmitz, N., Kurrer, M. O., Bauer, M., Hinton, H. I., Behnke, S., Gatto, D., Sebbel, P., Beerli, R. R., Sonderegger, I., et al. (2006) · Journal of Clinical Investigation · doi:10.1172/jci25673 · Cited by 273 · see citing works
Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice
Rogers, H. W., & Unanue, E. R. (1993) · Infection and Immunity · doi:10.1128/iai.61.12.5090-5096.1993 · Cited by 271 · see citing works
Xia, Y., Vetvicka, V., Yan, J., Hanikýřová, M., Mayadas, T. N., & Ross, G. D. (1999) · PubMed · Cited by 265 · see citing works
Structure–function relationships of complement receptor type 1
Krych‐Goldberg, M., & Atkinson, J. P. (2001) · Immunological Reviews · doi:10.1034/j.1600-065x.2001.1800110.x · Cited by 259 · see citing works
Structure of C3b in complex with CRIg gives insights into regulation of complement activation
Wiesmann, C., Katschke, K. J., Yin, J., Helmy, K. Y., Steffek, M., Fairbrother, W. J., McCallum, S. A., Embuscado, L., DeForge, L. E., Hass, P. E., et al. (2006) · Nature · doi:10.1038/nature05263 · Cited by 250 · see citing works
Self-citationIdentification of a 145,000 Mr membrane protein as the C3d receptor (CR2) of human B lymphocytes.
Weis, J., Tedder, T. F., & Fearon, D. T. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.3.881 · Cited by 248 · see citing works
Differences in the Mode of Phagocytosis with Fc and C3 Receptors in Macrophages
Kaplan, G. (1977) · Scandinavian Journal of Immunology · doi:10.1111/j.1365-3083.1977.tb02153.x · Cited by 244 · see citing works
Xia, Y., Větvička, V., Yan, J., Hanikýřová, M., Mayadas, T. N., & Ross, G. D. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.4.2281 · Cited by 244 · see citing works
A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis
Cox, D., Lee, D. J., Dale, B. M., Calafat, J., & Greenberg, S. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.2.680 · Cited by 241 · see citing works
Regulation of the Adhesion versus Cytotoxic Functions of the Mac-1/CR3/αMβ2 - lntegrin Glycoprotein
Ross, G. D. (2000) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v20.i3.20 · Cited by 218 · see citing works
Kang, Y., Do, Y., Lee, H., Park, S. H., Cheong, C., Lynch, R. M., Loeffler, J. M., Steinman, R. M., & Park, C. G. (2006) · Cell · doi:10.1016/j.cell.2006.01.046 · Cited by 216 · see citing works
Molina, H. D., Wong, W., Kinoshita, T., Brenner, C., Foley, S., & Holers, V. M. (1992) · The Journal of Experimental Medicine · doi:10.1084/jem.175.1.121 · Cited by 135 · see citing works
Holers, V. M., Kinoshita, T., & Molina, H. D. (1992) · Immunology Today · doi:10.1016/0167-5699(92)90160-9 · Cited by 132 · see citing works
Structural transitions of complement component C3 and its activation products
Nishida, N., Walz, T., & Springer, T. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609791104 · Cited by 129 · see citing works
Aderem, A. A., Wright, S. D., Silverstein, S. C., & Cohn, Z. A. (1985) · The Journal of Experimental Medicine · doi:10.1084/jem.161.3.617 · Cited by 128 · see citing works
Gregory, S., Cousens, L., van Rooijen, N., Döpp, E., Carlos, T., & Wing, E. (2002) · Journal of Immunology · doi:10.4049/jimmunol.168.1.308 · Cited by 126 · see citing works
Secretory vesicles are the intracellular reservoir of complement receptor 1 in human neutrophils.
Sengeløv, H., Kjeldsen, L., Kroeze, W. K., Berger, M., & Borregaard, N. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.2.804 · Cited by 119 · see citing works
Structure of the C3b Binding Site of CR1 (CD35), the Immune Adherence Receptor
Smith, B. O., Mallin, R. L., Krych‐Goldberg, M., Wang, X., Hauhart, R. E., Bromek, K., Uhrı́n, D., Atkinson, J. P., & Barlow, P. N. (2002) · Cell · doi:10.1016/s0092-8674(02)00672-4 · Cited by 112 · see citing works
Škoberne, M., Somersan, S., Almodovar, W., Truong, T., Petrova, K., Henson, P. M., & Bhardwaj, N. (2006) · Blood · doi:10.1182/blood-2005-12-4812 · Cited by 111 · see citing works
Decay Accelerating Activity of Complement Receptor Type 1 (CD35)
Krych‐Goldberg, M., Hauhart, R. E., Subramanian, V. B., Yurcisin, B. M., Crimmins, D. L., Hourcade, D. E., & Atkinson, J. P. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.44.31160 · Cited by 98 · see citing works
Lambris, J. D., Lao, Z., Oglesby, T. J., Atkinson, J. P., Hack, C. E., & Becherer, J. D. (1996) · The Journal of Immunology · doi:10.4049/jimmunol.156.12.4821 · Cited by 97 · see citing works
Protein-tyrosine kinase Syk is required for pathogen engulfment in complement-mediated phagocytosis
Shi, Y., Tohyama, Y., Kadono, T., He, J., Miah, S. M. S., Hazama, R., Tanaka, C., Tohyama, K., & Yamamura, H. (2006) · Blood · doi:10.1182/blood-2005-09-3616 · Cited by 93 · see citing works
Zhang, L., & Plow, E. F. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.30.18211 · Cited by 87 · see citing works
Structural insights into the central complement component C3
Janssen, B. J. C., & Gros, P. (2006) · Molecular Immunology · doi:10.1016/j.molimm.2006.06.017 · Cited by 80 · see citing works
Analysis of C3 Deposition and Degradation on Bacterial Surfaces After Opsonization
Gordon, D., Rice, J., Finlay‐Jones, J. J., McDonald, P. J., & Hostetter, M. K. (1988) · The Journal of Infectious Diseases · doi:10.1093/infdis/157.4.697 · Cited by 80 · see citing works
Emerging Patterns in Complement-Mediated Pathogen Recognition
Roozendaal, R., & Carroll, M. C. (2006) · Cell · doi:10.1016/j.cell.2006.03.018 · Cited by 75 · see citing works
Weisman, H. F., Bartow, T. A., Leppo, M. K., Boyle, M., Marsh, H. C., Carson, G. R., Roux, K., Weisfeldt, M. L., & Fearon, D. T. (1990) · PubMed · Cited by 67 · see citing works
Taniguchi‐Sidle, A., & Isenman, D. E. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.11.5285 · Cited by 63 · see citing works
Clemenza, L., & Isenman, D. E. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.7.3839 · Cited by 63 · see citing works
Carpentier, J. L., Lew, D. P., Paccaud, J. P., Gil, R. B., Iacopetta, B. M., Kazatchkine, M. D., Stendahl, O. I., & Pozzan, T. (1991) · Cell Regulation · doi:10.1091/mbc.2.1.41 · Cited by 55 · see citing works
Balsam, L. B., Liang, T. W., & Parkos, C. A. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.10.5058 · Cited by 52 · see citing works
Hinglais, N., Kazatchkine, M. D., Mandet, C., Appay, M., & Bariety, J. (1989) · PubMed · Cited by 51 · see citing works
Oran, A. E., & Isenman, D. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.8.5120 · Cited by 50 · see citing works
Complement Receptors, Adhesion, and Phagocytosis
Brown, E. J. (2008) · Springer eBooks · doi:10.1007/978-0-387-28669-3_4 · Cited by 50 · see citing works
Self-citationRole of bacterial association with Kupffer cells in occurrence of endogenous systemic bacteremia
Hirakata, Y., Tomono, K., Tateda, K., Matsumoto, T., Furuya, N., SHIMOGUCHI, K., Kaku, M., & Yamaguchi, K. (1991) · Infection and Immunity · doi:10.1128/iai.59.1.289-294.1991 · Cited by 48 · see citing works
Lee, M.-Y., Kim, W.-J., Kang, Y., Jung, Y., Kang, Y. M., Suk, K., Park, J.-E., Choi, E.-M., Choi, B.-K., Kwon, B. S., et al. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0306160 · Cited by 47 · see citing works
Taylor, R. P., Ferguson, P. J., Martin, E. N., Cooke, J., Greene, K. L., Grinspun, K., Guttman, M., & Kuhn, S. (1997) · Clinical Immunology and Immunopathology · doi:10.1006/clin.1996.4286 · Cited by 46 · see citing works
Cloning of Z39Ig, a novel gene with immunoglobulin-like domains located on human chromosome X
Langnaese, K., Colleaux, L., Kloos, D. U., Fontés, M., & Wieacker, P. F. (2000) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(00)00131-7 · Cited by 46 · see citing works
Croizé, J., Arvieux, J., Berche, P., & Colomb, M. G. (1993) · Infection and Immunity · doi:10.1128/iai.61.12.5134-5139.1993 · Cited by 43 · see citing works
Rothman, I. K., Gelfand, J. A., Fauci, A. S., & Frank, M. M. (1975) · The Journal of Immunology · doi:10.4049/jimmunol.115.5.1312 · Cited by 29 · see citing works
Zang, X., & Allison, J. P. (2006) · Journal of Clinical Investigation · doi:10.1172/jci30103 · Cited by 24 · see citing works
Expression and Characterization of the C345C/NTR Domains of Complement Components C3 and C5
Thai, C.-T., & Ogata, R. T. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.12.6565 · Cited by 22 · see citing works
Flagged first, then by citations
2 of the 67 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
PEGylation as a strategy for improving nanoparticle-based drug and gene delivery
Suk, J. S., Xu, Q., Kim, N., Hanes, J., & Ensign, L. M. (2016) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2015.09.012 · Cited by 4,523 · see citing works
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
“In the immune system, C3 is cleaved into anactivated form, iC3b,which covalently binds to the surfaceof cells or debris and targets them for elimination by macrophages via specific phagocytic receptor signaling (e.g., CR3) (Lambris and Tsokos, 1986; van Lookeren Campagne et al., 2007).”
Complement: a key system for immune surveillance and homeostasis
Ricklin, D., Hajishengallis, G., Yang, K., & Lambris, J. D. (2010) · Nature Immunology · doi:10.1038/ni.1923 · Cited by 3,654 · see citing works
Complement and its role in innate and adaptive immune responses
Dunkelberger, J. R., & Song, W.-C. (2010) · Cell Research · doi:10.1038/cr.2009.139 · Cited by 1,932 · see citing works
Nanoparticle Size and Surface Chemistry Determine Serum Protein Adsorption and Macrophage Uptake
Walkey, C. D., Olsen, J. B., Guo, H., Emili, A., & Chan, W. C. W. (2012) · Journal of the American Chemical Society · doi:10.1021/ja2084338 · Cited by 1,926 · see citing works
Microglia emerge as central players in brain disease
Salter, M. W., & Stevens, B. (2017) · Nature Medicine · doi:10.1038/nm.4397 · Cited by 1,767 · see citing works
Complement System Part I – Molecular Mechanisms of Activation and Regulation
Merle, N. S., Church, S. E., Fremeaux-Bacchi, V., & Roumenina, L. T. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00262 · Cited by 1,620 · see citing works
Nanoparticle uptake: The phagocyte problem
Gustafson, H. H., Holt‐Casper, D., Grainger, D. W., & Ghandehari, H. (2015) · Nano Today · doi:10.1016/j.nantod.2015.06.006 · Cited by 1,424 · see citing works
The Complement System: An Unexpected Role in Synaptic Pruning During Development and Disease
Stephan, A. H., Barres, B. A., & Stevens, B. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113810 · Cited by 1,113 · see citing works
The Role of Microglia in the Healthy Brain: Figure 1.
Tremblay, M.-È., Stevens, B., Sierra, A., Wake, H., Bessis, A., & Nimmerjahn, A. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4158-11.2011 · Cited by 992 · see citing works
Signaling pathways involved in ischemic stroke: molecular mechanisms and therapeutic interventions
Qin, C., Yang, S., Chu, Y., Zhang, H., Pang, X., Chen, L., Zhou, L., Chen, M., Tian, D., & Wang, W. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01064-1 · Cited by 971 · see citing works
Heterogeneity of Microglial Activation in the Innate Immune Response in the Brain
Colton, C. A. (2009) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-009-9164-4 · Cited by 871 · see citing works
Phagocytosis: Our Current Understanding of a Universal Biological Process
Uribe-Querol, E., & Rosales, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01066 · Cited by 651 · see citing works
Information processing during phagocytosis
Underhill, D. M., & Goodridge, H. S. (2012) · Nature Reviews Immunology · doi:10.1038/nri3244 · Cited by 616 · see citing works
The “quad‐partite” synapse: Microglia‐synapse interactions in the developing and mature CNS
Schafer, D. P., Lehrman, E. K., & Stevens, B. (2013) · Glia · doi:10.1002/glia.22389 · Cited by 570 · see citing works
The role of saliva in tick feeding
Ivo, M. B. F. (2009) · Frontiers in bioscience · doi:10.2741/3363 · Cited by 581 · see citing works
Materials engineering for immunomodulation
Hubbell, J. A., Thomas, S. N., & Swartz, M. A. (2009) · Nature · doi:10.1038/nature08604 · Cited by 565 · see citing works
Phagosome maturation: going through the acid test
Kinchen, J. M., & Ravichandran, K. S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2515 · Cited by 555 · see citing works
Phagocytosis: A Fundamental Process in Immunity
Rosales, C., & Uribe‐Querol, E. (2017) · BioMed Research International · doi:10.1155/2017/9042851 · Cited by 562 · see citing works
Cellular effectors mediating Th17-dependent clearance of pneumococcal colonization in mice
Zhang, Z., Clarke, T. B., & Weiser, J. N. (2009) · Journal of Clinical Investigation · doi:10.1172/jci36731 · Cited by 453 · see citing works
Cancer immunotherapy targeting the CD47/SIRPα axis
Weiskopf, K. (2017) · European Journal of Cancer · doi:10.1016/j.ejca.2017.02.013 · Cited by 356 · see citing works
Microglia Function in Central Nervous System Development and Plasticity
Schafer, D. P., & Stevens, B. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020545 · Cited by 353 · see citing works
Control of Phagocytosis by Microbial Pathogens
Uribe‐Querol, E., & Rosales, C. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01368 · Cited by 310 · see citing works
Biological Barriers to Therapy with Antisense and siRNA Oligonucleotides
Juliano, R. L., Bauman, J. A., Kang, H. M., & Ming, X. (2009) · Molecular Pharmaceutics · doi:10.1021/mp900093r · Cited by 306 · see citing works
Pierigè, F., Serafini, S., Rossi, L., & Magnani, M. (2007) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2007.08.029 · Cited by 292 · see citing works
Structures of C3b in Complex with Factors B and D Give Insight into Complement Convertase Formation
Forneris, F., Ricklin, D., Wu, J., Τζέκου, Α., Wallace, R. S., Lambris, J. D., & Gros, P. (2010) · Science · doi:10.1126/science.1195821 · Cited by 289 · see citing works
Microglia and the brain: Complementary partners in development and disease
Hammond, T. R., Robinton, D., & Stevens, B. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060509 · Cited by 288 · see citing works
Particulate vaccines: on the quest for optimal delivery and immune response
Temmerman, M. D., Rejman, J., Demeester, J., Irvine, D. J., Gander, B. A., & Smedt, S. C. D. (2011) · Drug Discovery Today · doi:10.1016/j.drudis.2011.04.006 · Cited by 288 · see citing works
Nanoparticle–protein corona complexes govern the biological fates and functions of nanoparticles
Gunawan, C., Lim, M., Marquis, C. P., & Amal, R. (2014) · Journal of Materials Chemistry B · doi:10.1039/c3tb21526a · Cited by 277 · see citing works
Presentation of Phagocytosed Antigens by MHC Class I and II
Mantegazza, A. R., Magalhaes, J. G., Amigorena, S., & Marks, M. S. (2012) · Traffic · doi:10.1111/tra.12026 · Cited by 254 · see citing works
Mishra, M., Byrd, M. S., Sergeant, S., Azad, A. K., Parsek, M. R., McPhail, L. C., Schlesinger, L. S., & Wozniak, D. J. (2011) · Cellular Microbiology · doi:10.1111/j.1462-5822.2011.01704.x · Cited by 245 · see citing works
Zirngibl, M., Assinck, P., Sizov, A., Caprariello, A. V., & Plemel, J. R. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00538-8 · Cited by 233 · see citing works
Microglia function during brain development: New insights from animal models
Bilimoria, P. M., & Stevens, B. (2015) · Brain Research · doi:10.1016/j.brainres.2014.11.032 · Cited by 204 · see citing works
Immune Function and Diversity of Osteoclasts in Normal and Pathological Conditions
Madel, M., Ibáñez, L., Wakkach, A., de Vries, T. J., Teti, A. M., Apparailly, F., & Blin‐Wakkach, C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01408 · Cited by 206 · see citing works
Moalli, F., Doni, A., Deban, L., Zelante, T., Zagarella, S., Bottazzi, B., Romani, L., Mantovani, A., & Garlanda, C. (2010) · Blood · doi:10.1182/blood-2009-12-258376 · Cited by 205 · see citing works
Verschoor, A., Neuenhahn, M., Navarini, A. A., Graef, P., Plaumann, A., Seidlmeier, A., Nieswandt, B., Maßberg, S., Zinkernagel, R. M., Hengartner, H., et al. (2011) · Nature Immunology · doi:10.1038/ni.2140 · Cited by 201 · see citing works
The Role of Complement in Tumor Growth
Pı́o, R., Corrales, L. P., & Lambris, J. D. (2013) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5915-6_11 · Cited by 196 · see citing works
Enolase-1 promotes plasminogen-mediated recruitment of monocytes to the acutely inflamed lung
Wygrecka, M., Marsh, L. M., Morty, R. E., Henneke, I., Günther, A., Lohmeyer, J., Markart, P., & Preissner, K. T. (2009) · Blood · doi:10.1182/blood-2008-08-170837 · Cited by 197 · see citing works
Ståhl, A.-L., Sartz, L., & Karpman, D. (2011) · Blood · doi:10.1182/blood-2010-09-309161 · Cited by 197 · see citing works
Insights into TREM2 biology by network analysis of human brain gene expression data
Forabosco, P., Ramasamy, A., Trabzuni, D., Walker, R., Smith, C., Bras, J., Levine, A. P., Hardy, J., Pocock, J. M., Guerreiro, R., et al. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.05.001 · Cited by 180 · see citing works
Liu, Y., Shen, X. P., Zhang, Y., Zheng, X., Cepeda, C., Wang, Y., Duan, S., & Tong, X. (2023) · Glia · doi:10.1002/glia.24343 · Cited by 190 · see citing works
Complement Is an Essential Component of the Immune Response to Adeno-Associated Virus Vectors
Zaiss, A. K., Cotter, M. J., White, L. R., Clark, S. A., Wong, N. C. W., Holers, V. M., Bartlett, J. S., & Muruve, D. A. (2008) · Journal of Virology · doi:10.1128/jvi.01990-07 · Cited by 177 · see citing works
Evasion of the Immune Response by Trypanosoma cruzi during Acute Infection
Cardoso, M. S., Reis-Cunha, J. L., & Bartholomeu, D. C. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00659 · Cited by 170 · see citing works
Stepien, G., Moros, M., Pérez-Hernández, M., Monge, M., Gutiérrez, L., Fratila, R. M., Heras, M. D. L., Menao, S., Lanzarote, J. J. P., Solans, C., et al. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b18648 · Cited by 159 · see citing works
Broadley, S. P., Plaumann, A., Coletti, R., Lehmann, C., Wanisch, A., Seidlmeier, A., Esser, K., Luo, S., Rämer, P. C., Massberg, S., et al. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.05.023 · Cited by 156 · see citing works
Coustau, C., Gourbal, B., DUVAL, D. T., Yoshino, T. P., Adema, C. M., & Mitta, G. (2015) · Fish & Shellfish Immunology · doi:10.1016/j.fsi.2015.01.036 · Cited by 151 · see citing works
Du, T., Yu, X., Shao, S., Li, T., Xu, S., & Wu, L. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.2c05772 · Cited by 151 · see citing works
Structural basis for complement factor I control and its disease-associated sequence polymorphisms
Roversi, P., Johnson, S., Caesar, J. J. E., McLean, F. E., Leath, K. J., Tsiftsoglou, S. A., Morgan, B. P., Harris, C. L., Sim, R. B., & Lea, S. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102167108 · Cited by 138 · see citing works
Bajic, G., Yatime, L., Sim, R. B., Vorup‐Jensen, T., & Andersen, G. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311261110 · Cited by 135 · see citing works
The Role of Microglial Phagocytosis in Ischemic Stroke
Jia, J., Yang, L., Chen, Y., Zheng, L., Chen, Y., Xu, Y., & Zhang, M. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.790201 · Cited by 136 · see citing works
Obst, K., Yealland, G., Balzus, B., Miceli, E., Dimde, M., Weise, C., Eravci, M., Bodmeier, R. A., Haag, R., Calderón, M., et al. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.7b00158 · Cited by 133 · see citing works
Molecular mechanism of the anti-inflammatory effects of plant essential oils: A systematic review
Zhao, Q., Zhu, L.-Y., Wang, S., Gao, Y., & Jin, F. (2022) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2022.115829 · Cited by 137 · see citing works
Moné, Y., Gourbal, B., DUVAL, D. T., Pasquier, L. D., Kieffer‐Jaquinod, S., & Mitta, G. (2010) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000813 · Cited by 130 · see citing works
Antibody Distance from the Cell Membrane Regulates Antibody Effector Mechanisms
Cleary, K. L. S., Chan, H. T. C., James, S., Glennie, M. J., & Cragg, M. S. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601473 · Cited by 125 · see citing works
Significance of Complement System in Ischemic Stroke: A Comprehensive Review
Ma, Y., Liu, Y., Zhang, Z., & Yang, G. (2019) · Aging and Disease · doi:10.14336/ad.2019.0119 · Cited by 122 · see citing works
Luo, S., Poltermann, S., Kunert, A., Rupp, S., & Zipfel, P. F. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.07.017 · Cited by 122 · see citing works
Advances and applications of nanoparticles in cancer therapy
Huang, X., He, T., Liang, X., Xiang, Z., Liu, C., Zhou, S., Luo, R., Bai, L., Kou, X., Li, X., et al. (2024) · MedComm – Oncology · doi:10.1002/mog2.67 · Cited by 123 · see citing works
The Opportunistic Human Pathogenic FungusAspergillus fumigatusEvades the Host Complement System
Behnsen, J., Hartmann, A., Schmaler-Ripcke, J., Gehrke, A., Brakhage, A. A., & Zipfel, P. F. (2007) · Infection and Immunity · doi:10.1128/iai.01037-07 · Cited by 116 · see citing works
IgGs are made for walking on bacterial and viral surfaces
Preiner, J., Kodera, N., Tang, J., Ebner, A., Brameshuber, M. O., Blaas, D., Gelbmann, N., Gruber, H. J., Ando, T., & Hinterdorfer, P. (2014) · Nature Communications · doi:10.1038/ncomms5394 · Cited by 115 · see citing works
Mitta, G., Adema, C. M., Gourbal, B., Loker, E. S., & Thèron, A. (2011) · Developmental & Comparative Immunology · doi:10.1016/j.dci.2011.09.002 · Cited by 110 · see citing works
Neher, M. D., Weckbach, S., Flierl, M. A., Huber-Lang, M. S., & Stahel, P. F. (2011) · Journal of Biomedical Science · doi:10.1186/1423-0127-18-90 · Cited by 110 · see citing works
Coulton, A., Murai, J., Qian, D., Thakkar, K., Lewis, C. E., & Litchfield, K. (2024) · Nature Communications · doi:10.1038/s41467-024-49885-8 · Cited by 114 · see citing works
Mechanisms of Pathogenic Candida Species to Evade the Host Complement Attack
Singh, D. K., Tóth, R., & Gácser, A. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00094 · Cited by 110 · see citing works
Binnemars‐Postma, K., ten Hoopen, H., Storm, G., & Prakash, J. (2016) · Nanomedicine · doi:10.2217/nnm-2016-0233 · Cited by 103 · see citing works
A visual review of the human pathogen Streptococcus pneumoniae
Engholm, D. H., Kilian, M., Goodsell, D. S., Andersen, E. S., & Kjærgaard, R. S. (2017) · FEMS Microbiology Reviews · doi:10.1093/femsre/fux037 · Cited by 101 · see citing works
Complement activation turnover on surfaces of nanoparticles
Moghimi, S. M., & Simberg, D. (2017) · Nano Today · doi:10.1016/j.nantod.2017.03.001 · Cited by 99 · see citing works
Zou, G., Wang, J., Xu, X., Xu, P., Zhu, L., Yu, Q., Peng, Y., Guo, X., Li, T., & Zhang, X. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00613-5 · Cited by 98 · see citing works
Clay, C. D., Soni, S., Gunn, J. S., & Schlesinger, L. S. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.8.5568 · Cited by 97 · see citing works
Host response toCandida albicansbloodstream infection and sepsis
Duggan, S., Leonhardt, I., Hünniger, K., & Kurzai, O. (2015) · Virulence · doi:10.4161/21505594.2014.988096 · Cited by 97 · see citing works
Crosstalk between platelets and the complement system in immune protection and disease
Langer, H. F., & Verschoor, A. (2013) · Thrombosis and Haemostasis · doi:10.1160/th13-02-0102 · Cited by 91 · see citing works
Targeting complement components C3 and C5 for the retina: Key concepts and lingering questions
Kim, B. J., Mastellos, D. C., Li, Y., Dunaief, J. L., & Lambris, J. D. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100936 · Cited by 91 · see citing works
The Compatibility Between Biomphalaria glabrata Snails and Schistosoma mansoni
Mitta, G., Gourbal, B., Grunau, C., Knight, M., Bridger, J. M., & Thèron, A. (2016) · Advances in Parasitology/Advances in parasitology · doi:10.1016/bs.apar.2016.08.006 · Cited by 87 · see citing works
The Complement System: A Prey of Trypanosoma cruzi
Lidani, K. C. F., Bavia, L., Ambrósio, A. R., & Messias-Reason, I. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00607 · Cited by 83 · see citing works
Immune Evasion of Enterococcus faecalis by an Extracellular Gelatinase That Cleaves C3 and iC3b
Park, S. Y., Shin, Y. P., Kim, C. H., Park, H. J., Seong, Y., Kim, B. S., Seo, S. J., & Lee, I. H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.9.6328 · Cited by 83 · see citing works
Gancz, D., & Fishelson, Z. (2009) · Molecular Immunology · doi:10.1016/j.molimm.2009.05.009 · Cited by 83 · see citing works
Comparative Functional Evolution of Human and Mouse CR1 and CR2,
Jacobson, A. C., & Weis, J. H. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.5.2953 · Cited by 82 · see citing works
Vieira, M. L., de Morais, Z. M., Vasconcellos, S. A., Romero, E. C., & Nascimento, A. L. T. O. (2011) · Microbial Pathogenesis · doi:10.1016/j.micpath.2011.06.008 · Cited by 80 · see citing works
Spatiotemporal Adaptations of Macrophage and Dendritic Cell Development and Function
Roquilly, A., Mintern, J. D., & Villadangos, J. A. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101320-031931 · Cited by 77 · see citing works
Zhu, Q., Zhang, M., Shi, M., Liu, Y., Zhao, Q. C., Wang, W., Zhang, G., Yang, L.-X., Zhi, J., Zhang, L., et al. (2015) · Immunobiology · doi:10.1016/j.imbio.2015.12.003 · Cited by 74 · see citing works
Complement: A primer for the coming therapeutic revolution
Barnum, S. R. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.11.014 · Cited by 72 · see citing works
Role of Macrophage Receptor with Collagenous Structure in Innate Immune Tolerance
Jing, J., Yang, I. V., Hui, L., Patel, J., Evans, C. M., Prikeris, R., Kobzik, L., O’Connor, B. P., & Schwartz, D. A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1202942 · Cited by 69 · see citing works
Acharya, D., Li, X. R. (., Heineman, R. E.-S., & Harrison, R. E. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03049 · Cited by 66 · see citing works
Rheumatic heart disease: A review of the current status of global research activity
Dooley, L., Ahmad, T. B., Pandey, M., Good, M. F., & Kotiw, M. (2020) · Autoimmunity Reviews · doi:10.1016/j.autrev.2020.102740 · Cited by 69 · see citing works
Amarilyo, G., Verbovetski, I., Atallah, M., Grau, A., Wiser, G., Gill, O., Ben‐Neriah, Y., & Mevorach, D. (2009) · European Journal of Immunology · doi:10.1002/eji.200838951 · Cited by 67 · see citing works
Pivotal Advance: Characterization of mouse liver phagocytic B cells in innate immunity
Nakashima, M., Kinoshita, M., Nakashima, H., Habu, Y., Miyazaki, H., Shono, S., Hiroi, S., Shinomiya, N., Nakanishi, K., & Seki, S. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0411214 · Cited by 66 · see citing works
Binding of Soluble Yeast β-Glucan to Human Neutrophils and Monocytes is Complement-Dependent
Bose, N., Chan, A. S. H., Guerrero, F. O., Maristany, C. M., Qiu, X., Walsh, R. M., Ertelt, K. E., Jonas, A. B., Gorden, K. B., Dudney, C., et al. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00230 · Cited by 65 · see citing works
Cellular immune reactions in the lung
Hasenberg, M., Stegemann‐Koniszewski, S., & Gunzer, M. (2012) · Immunological Reviews · doi:10.1111/imr.12020 · Cited by 65 · see citing works
Park, J. H., Jackman, J. A., Ferhan, A. R., Belling, J. N., Mokrzecka, N., Weiss, P. S., & Cho, N. (2020) · ACS Nano · doi:10.1021/acsnano.0c05097 · Cited by 63 · see citing works
The immunobiology of viral arthritides
Suhrbier, A., & Mahalingam, S. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.09.005 · Cited by 62 · see citing works
Hinkle, J. J., Olschowka, J. A., Love, T. M., Williams, J. P., & O’Banion, M. K. (2019) · Scientific Reports · doi:10.1038/s41598-019-55366-6 · Cited by 61 · see citing works
Peterson, S. L., & Anderson, A. J. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.04.028 · Cited by 61 · see citing works
Luo, S., Hoffmann, R., Skerka, C., & Zipfel, P. F. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jis718 · Cited by 61 · see citing works
Old dogs—new tricks: immunoregulatory properties of C3 and C5 cleavage fragments
Verschoor, A., Karsten, C. M., Broadley, S. P., Laumonnier, Y., & Köhl, J. (2016) · Immunological Reviews · doi:10.1111/imr.12473 · Cited by 59 · see citing works
Delivery and Biodistribution of siRNA for Cancer Therapy: Challenges and Future Prospects
Seth, S., Johns, R. E., & Templin, M. V. (2012) · Therapeutic Delivery · doi:10.4155/tde.11.155 · Cited by 58 · see citing works
Streptococcus pneumoniae interactions with the complement system
Gil, E., Noursadeghi, M., & Brown, J. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.929483 · Cited by 57 · see citing works
CCN1 is an opsonin for bacterial clearance and a direct activator of Toll-like receptor signaling
Jun, J.-I., & Lau, L. F. (2020) · Nature Communications · doi:10.1038/s41467-020-15075-5 · Cited by 54 · see citing works
Rosa, T. F. A., Flammersfeld, A., Ngwa, C. J., Kiesow, M. J., Fischer, R., Zipfel, P. F., Skerka, C., & Pradel, G. (2015) · Cellular Microbiology · doi:10.1111/cmi.12535 · Cited by 56 · see citing works
Antibody‐mediated phagocytosis in cancer immunotherapy
Wagoner, C. M. V., Rivera‐Escalera, F., Jaimes‐Delgadillo, N. C., Chu, C. C., Zent, C. S., & Elliott, M. R. (2023) · Immunological Reviews · doi:10.1111/imr.13265 · Cited by 54 · see citing works
Bai, H., Mu, L., Qiu, L., Chen, N., Li, J., Zeng, Q., Yin, X., & Ye, J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232415586 · Cited by 54 · see citing works
Thompson, A., Davies, L. C., Liao, C., da Fonseca, D. M., Griffiths, J. S., Andrews, R., Jones, A. V., Clement, M., Brown, G. D., Humphreys, I. R., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007850 · Cited by 51 · see citing works
- Authors
- van Lookeren Campagne, M., Wiesmann, C., & Brown, E. J.
- Affiliations
- Genentech (US)
- Venue
- Cellular Microbiology
- Publisher
- Hindawi Limited
- Published
- 2007-09
- Volume
- 9
- Issue
- 9
- Pages
- 2095-2102
- ISSN
- 1462-5814 (ISSN-L)
- 1462-5822
- OpenAlex
- W2007658022
- Cited by
- 332
- References
- 67
- Citations by year
- 2026: 9 · 2025: 13 · 2024: 14 · 2023: 23 · 2022: 15 · 2021: 18 · 2020: 27 · 2019: 18 · 2018: 9 · 2017: 25 · 2016: 17 · 2015: 22 · 2014: 20 · 2013: 19 · 2012: 20
- FWCI
- 1.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cellular Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Complement system in diseases
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Immunology and Microbiology › Immunology › Biomarkers in Disease Mechanisms
- Keywords
- complement C3, opsonization, phagocytosis, C3b, iC3b, C3dg, C3c, complement activation, pathogen clearance, host defense, ligand-receptor interactions
- MeSH terms
- Complement Activation, Complement C3, Macrophages, Models, Molecular, Opsonin Proteins, Phagocytosis, Protein Conformation, Receptors, Complement, Protein Isoforms
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