Dynamics of virus-receptor interactions in virus binding, signaling, and endocytosis

Viruses

Volumn 7, Issue 6, 2015, Pages 2794-2815

  Boulant, Steeve ^a,b   Stanifer, Megan ^a,b   Lozach, Pierre Yves ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Binding; Endocytosis; Signalization; Single particle tracking; Uptake; Virus receptor

Indexed keywords

BETA1 INTEGRIN; CD150 ANTIGEN; CD209 ANTIGEN; CD51 ANTIGEN; CLATHRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GANGLIOSIDE GM1; JUNCTIONAL ADHESION MOLECULE A; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; TRANSFERRIN RECEPTOR; VERY LATE ACTIVATION ANTIGEN 2; VIRUS RECEPTOR; VITRONECTIN RECEPTOR;

ENDOCYTOSIS; ENTEROVIRUS; ENTEROVIRUS B; FELINE PANLEUKOPENIA VIRUS; HUMAN HERPESVIRUS 8; HUMAN PAPILLOMAVIRUS TYPE 16; INFLUENZA VIRUS A; INTERNALIZATION; MURINE POLYOMAVIRUS; NONHUMAN; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INFECTION; METABOLISM;

ENDOCYTOSIS; RECEPTORS, VIRUS; SIGNAL TRANSDUCTION; VIRUS ATTACHMENT; VIRUS INTERNALIZATION;

EID: 84930932695     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7062747     Document Type: Review

References (112)

1. Backovic, M.; Rey, F.A. Virus entry: Old viruses, new receptors. Curr. Opin. Virol. 2012, 2, 4-13.
2. Carette, J.E.; Guimaraes, C.P.; Varadarajan, M.; Park, A.S.; Wuethrich, I.; Godarova, A.; Kotecki, M.; Cochran, B.H.; Spooner, E.; Ploegh, H.L.; et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 2009, 326, 1231-1235.
3. Carette, J.E.; Raaben, M.; Wong, A.C.; Herbert, A.S.; Obernosterer, G.; Mulherkar, N.; Kuehne, A.I.; Kranzusch, P.J.; Griffin, A.M.; Ruthel, G.; et al. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477, 340-343.
4. Jae, L.T.; Raaben, M.; Herbert, A.S.; Kuehne, A.I.; Wirchnianski, A.S.; Soh, T.K.; Stubbs, S.H.; Janssen, H.; Damme, M.; Saftig, P.; et al. Virus entry. Lassa virus entry requires a trigger-induced receptor switch. Science 2014, 344, 1506-1510.
5. Greber, U.F. Signaling in viral entry. Cell. Mol. Life Sci. 2002, 59, 608-626.
6. Schiffner, T.; Sattentau, Q.J.; Duncan, C.J. Cell-to-cell spread of HIV-1 and evasion of neutralizing antibodies. Vaccine 2013, 31, 5789-5797.
7. Ehrlich, M.; Boll, W.; van Oijen, A.; Hariharan, R.; Chandran, K.; Nibert, M.L.; Kirchhausen, T. Endocytosis by random initiation and stabilization of Clathrin-Coated Pits. Cell 2004, 118, 591-605.
8. Boulant, S.; Stanifer, M.; Kural, C.; Cureton, D.K.; Massol, R.; Nibert, M.L.; Kirchhausen, T. Similar uptake but different trafficking and escape routes of reovirus virions and infectious subvirion particles imaged in polarized Madin-Darby canine kidney cells. Mol. Biol. Cell 2013, 24, 1196-1207.
9. Lozach, P.Y.; Kuhbacher, A.; Meier, R.; Mancini, R.; Bitto, D.; Bouloy, M.; Helenius, A. DC-SIGN as a receptor for phleboviruses. Cell Host Microbe 2011, 10, 75-88.
10. Stehle, T.; Harrison, S.C. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: Implications for assembly and receptor binding. EMBO J. 1997, 16, 5139–5148.
11. Reiter, D.M.; Frierson, J.M.; Halvorson, E.E.; Kobayashi, T.; Dermody, T.S.; Stehle, T. Crystal structure of reovirus attachment protein sigma1 in complex with sialylated oligosaccharides. PLoS Pathogens 2011, 7, e1002166.
12. Gibbons, M.M.; Chou, T.; D’Orsogna, M.R. Diffusion-dependent mechanisms of receptor engagement and viral entry. J. Phys. Chem. B 2010, 114, 15403-15412.
13. Stencel-Baerenwald, J.E.; Reiss, K.; Reiter, D.M.; Stehle, T.; Dermody, T.S. The sweet spot: Defining virus-sialic acid interactions. Nat. Rev. Microbiol. 2014, 12, 739-749.
14. Grove, J.; Marsh, M. The cell biology of receptor-mediated virus entry. J. Cell Biol. 2011, 195, 1071-1082.
15. Neu, U.; Stehle, T.; Atwood, W.J. The Polyomaviridae: Contributions of virus structure to our understanding of virus receptors and infectious entry. Virology 2009, 384, 389–399.
16. Mercer, J.; Schelhaas, M.; Helenius, A. Virus entry by endocytosis. Annu. Rev. Biochem. 2010, 79, 803-833.
17. Stewart, P.L.; Nemerow, G.R. Cell integrins: Commonly used receptors for diverse viral pathogens. Trends Microbiol. 2007, 15, 500-507.
18. Cureton, D.K.; Harbison, C.E.; Cocucci, E.; Parrish, C.R.; Kirchhausen, T. Limited transferrin receptor clustering allows rapid diffusion of canine parvovirus into clathrin endocytic structures. J. Virol. 2012, 86, 5330-5340.
19. Lehmann, M.J. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol. 2005, 170, 317–325.
20. Singer, S.J. A fluid lipid-globular protein mosaic model of membrane structure. Ann. N. Y. Acad. Sci. 1972, 195, 16–23.
21. Ryan, T.A.; Myers, J.; Holowka, D.; Baird, B.; Webb, W.W. Molecular crowding on the cell surface. Science 1988, 239, 61-64.
22. Kusumi, A.; Koyama-Honda, I.; Suzuki, K. Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 2004, 5, 213-230.
23. Kusumi, A.; Sako, Y.; Yamamoto, M. Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys. J. 1993, 65, 2021-2040.
24. Di Rienzo, C.; Gratton, E.; Beltram, F.; Cardarelli, F. Fast spatiotemporal correlation spectroscopy to determine protein lateral diffusion laws in live cell membranes. Proc. Natl. Acad. Sci. USA 2013, 110, 12307-12312.
25. Cureton, D.K.; Massol, R.H.; Saffarian, S.; Kirchhausen, T.L.; Whelan, S.P. Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog. 2009, 5, e1000394.
26. Maginnis, M.S.; Forrest, J.C.; Kopecky-Bromberg, S.A.; Dickeson, S.K.; Santoro, S.A.; Zutter, M.M.; Nemerow, G.R.; Bergelson, J.M.; Dermody, T.S. B1 integrin mediates internalization of mammalian reovirus. J. Virol. 2006, 80, 2760-2770.
27. Barton, E.S.; Forrest, J.C.; Connolly, J.L.; Chappell, J.D.; Liu, Y.; Schnell, F.J.; Nusrat, A.; Parkos, C.A.; Dermody, T.S. Junction adhesion molecule is a receptor for reovirus. Cell 2001, 104, 441-451.
28. Cera, M.R.; Fabbri, M.; Molendini, C.; Corada, M.; Orsenigo, F.; Rehberg, M.; Reichel, C.A.; Krombach, F.; Pardi, R.; Dejana, E. JAM-A promotes neutrophil chemotaxis by controlling integrin internalization and recycling. J. Cell Sci. 2009, 122, 268-277.
29. Rust, M.J.; Lakadamyali, M.; Zhang, F.; Zhuang, X. Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat. Struct. Mol. Biol. 2004, 11, 567-573.
30. Ewers, H.; Smith, A.E.; Sbalzarini, I.F.; Lilie, H.; Koumoutsakos, P.; Helenius, A. Single-particle tracking of murine polyoma virus-like particles on live cells and artificial membranes. Proc. Natl. Acad. Sci. USA 2005, 102, 15110-15115.
31. Hammond, A.T.; Heberle, F.A.; Baumgart, T.; Holowka, D.; Baird, B.; Feigenson, G.W. Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc. Natl. Acad. Sci. USA 2005, 102, 6320-6325.
32. Ewers, H.; Romer, W.; Smith, A.E.; Bacia, K.; Dmitrieff, S.; Chai, W.; Mancini, R.; Kartenbeck, J.; Chambon, V.; Berland, L.; et al. GM1 structure determines SV40-induced membrane invagination and infection. Nat. Cell Biol. 2010, 12, 11-18, S1-S12.
33. Van der Schaar, H.M.; Rust, M.J.; Chen, C.; van der Ende-Metselaar, H.; Wilschut, J.; Zhuang, X.; Smit, J.M. Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog. 2008, 4, e1000244.
34. Helenius, A.; Kartenbeck, J.; Simons, K.; Fries, E. On the entry of Semliki forest virus into BHK-21 cells. J. Cell Biol. 1980, 84, 404-420.
35. Smith, A.E.; Helenius, A. How viruses enter animal cells. Science 2004, 304, 237-242.
36. Schelhaas, M.; Ewers, H.; Rajamaki, M.L.; Day, P.M.; Schiller, J.T.; Helenius, A. Human papillomavirus type 16 entry: Retrograde cell surface transport along actin-rich protrusions. PLoS Pathog. 2008, 4, e1000148.
37. Hofmann, H.; Li, X.; Zhang, X.; Liu, W.; Kuhl, A.; Kaup, F.; Soldan, S.S.; Gonzalez-Scarano, F.; Weber, F.; He, Y.; et al. Severe fever with thrombocytopenia virus glycoproteins are targeted by neutralizing antibodies and can use DC-SIGN as a receptor for pH-dependent entry into human and animal cell lines. J. Virol. 2013, 87, 4384-4394.
38. Neumann, A.K.; Thompson, N.L.; Jacobson, K. Distribution and lateral mobility of DC-SIGN on immature dendritic cells—Implications for pathogen uptake. J. Cell Sci. 2008, 121, 634-643.
39. Coyne, C.B.; Bergelson, J.M. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 2006, 124, 119-131.
40. Burckhardt, C.J.; Suomalainen, M.; Schoenenberger, P.; Boucke, K.; Hemmi, S.; Greber, U.F. Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure. Cell Host Microbe 2011, 10, 105-117.
41. Wiethoff, C.M.; Wodrich, H.; Gerace, L.; Nemerow, G.R. Adenovirus protein VI mediates membrane disruption following capsid disassembly. J. Virol. 2005, 79, 1992-2000.
42. Tsai, B.; Gilbert, J.M.; Stehle, T.; Lencer, W.; Benjamin, T.L.; Rapoport, T.A. Gangliosides are receptors for murine polyoma virus and SV40. EMBO J. 2003, 22, 4346-4355.
43. Chen, Y.; Norkin, L.C. Extracellular simian virus 40 transmits a signal that promotes virus enclosure within caveolae. Exp. Cell Res. 1999, 246, 83-90.
44. Stang, E.; Kartenbeck, J.; Parton, R.G. Major histocompatibility complex class I molecules mediate association of SV40 with caveolae. Mol. Biol. Cell 1997, 8, 47-57.
45. Pelkmans, L.; Puntener, D.; Helenius, A. Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 2002, 296, 535-539.
46. Damm, E.M.; Pelkmans, L.; Kartenbeck, J.; Mezzacasa, A.; Kurzchalia, T.; Helenius, A. Clathrin- and caveolin-1-independent endocytosis: Entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 2005, 168, 477-488.
47. Norkin, L.C. Caveolae in the uptake and targeting of infectious agents and secreted toxins. Adv. Drug Deliv. Rev. 2001, 49, 301-315.
48. Pelkmans, L.; Fava, E.; Grabner, H.; Hannus, M.; Habermann, B.; Krausz, E.; Zerial, M. Genome-wide analysis of human kinases in clathrin- and caveolae/raft-mediated endocytosis. Nature 2005, 436, 78-86.
49. Nemerow, G.R. Cell receptors involved in adenovirus entry. Virology 2000, 274, 1-4.
50. Meier, O.; Boucke, K.; Hammer, S.V.; Keller, S.; Stidwill, R.P.; Hemmi, S.; Greber, U.F. Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J. Cell Biol. 2002, 158, 1119-1131.
51. Li, E.; Stupack, D.; Bokoch, G.M.; Nemerow, G.R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 1998, 72, 8806-8812.
52. Boulant, S.; Kural, C.; Zeeh, J.C.; Ubelmann, F.; Kirchhausen, T. Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 2011, 13, 1124-1131.
53. Saffarian, S.; Cocucci, E.; Kirchhausen, T. Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol. 2009, 7, e1000191.
54. Jokinen, J.; White, D.J.; Salmela, M.; Huhtala, M.; Kapyla, J.; Sipila, K.; Puranen, J.S.; Nissinen, L.; Kankaanpaa, P.; Marjomaki, V.;et al. Molecular mechanism of α2β1 integrin interaction with human echovirus 1. EMBO J. 2010, 29, 196-208.
55. Zheng, K.; Kitazato, K.; Wang, Y. Viruses exploit the function of epidermal growth factor receptor. Rev. Med. Virol. 2014, 24, 274-286.
56. Wang, X.; Huang, D.Y.; Huong, S.M.; Huang, E.S. Integrin αvβ3 is a coreceptor for human cytomegalovirus. Nat. Med. 2005, 11, 515-521.
57. Zheng, K.; Xiang, Y.; Wang, X.; Wang, Q.; Zhong, M.; Wang, S.; Wang, X.; Fan, J.; Kitazato, K.; Wang, Y. Epidermal growth factor receptor-PI3K signaling controls cofilin activity to facilitate herpes simplex virus 1 entry into neuronal cells. MBio 2014, 5, e00958-13.
58. Dawson, C.W.; Tramountanis, G.; Eliopoulos, A.G.; Young, L.S. Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodeling. J. Biol. Chem. 2003, 278, 3694-3704.
59. Kung, C.P.; Meckes, D.G., Jr.; Raab-Traub, N. Epstein-Barr virus LMP1 activates EGFR, STAT3, and ERK through effects on PKCdelta. J. Virol. 2011, 85, 4399-4408.
60. Eierhoff, T.; Hrincius, E.R.; Rescher, U.; Ludwig, S.; Ehrhardt, C. The epidermal growth factor receptor (EGFR) promotes uptake of influenza A viruses (IAV) into host cells. PLoS Pathog. 2010, 6, e1001099.
61. Zona, L.; Lupberger, J.; Sidahmed-Adrar, N.; Thumann, C.; Harris, H.J.; Barnes, A.; Florentin, J.; Tawar, R.G.; Xiao, F.; Turek, M.;et al. HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 2013, 13, 302-313.
62. Douam, F.; Lavillette, D.; Cosset, F.L. The mechanism of HCV entry into host cells. Prog. Mol. Biol. Transl. Sci. 2015, 129, 63-107.
63. Schelhaas, M.; Shah, B.; Holzer, M.; Blattmann, P.; Kuhling, L.; Day, P.M.; Schiller, J.T.; Helenius, A. Entry of human papillomavirus type 16 by actin-dependent, clathrin- and lipid raft-independent endocytosis. PLoS Pathog. 2012, 8, e1002657.
64. Surviladze, Z.; Sterk, R.T.; DeHaro, S.A.; Ozbun, M.A. Cellular entry of human papillomavirus type 16 involves activation of the phosphatidylinositol 3-kinase/Akt/mTOR pathway and inhibition of autophagy. J. Virol. 2013, 87, 2508-2517.
65. Krzyzaniak, M.A.; Zumstein, M.T.; Gerez, J.A.; Picotti, P.; Helenius, A. Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the F protein. PLoS Pathog. 2013, 9, e1003309.
66. Sanchez, E.G.; Quintas, A.; Perez-Nunez, D.; Nogal, M.; Barroso, S.; Carrascosa, A.L.; Revilla, Y. African swine fever virus uses macropinocytosis to enter host cells. PLoS Pathog. 2012, 8, e1002754.
67. Chandran, B. Early events in Kaposi’s sarcoma-associated herpesvirus infection of target cells. J. Virol. 2010, 84, 2188-2199.
68. Akula, S.M.; Pramod, N.P.; Wang, F.Z.; Chandran, B. Integrin α3β1 (CD49c/29) is a cellular receptor for Kaposi’s sarcoma-associated herpesvirus (KSHV/HHV-8) entry into the target cells. Cell 2002, 108, 407-419.
69. Garrigues, H.J.; Rubinchikova, Y.E.; Dipersio, C.M.; Rose, T.M. Integrin αVβ3 Binds to the RGD motif of glycoprotein B of Kaposi’s sarcoma-associated herpesvirus and functions as an RGD-dependent entry receptor. J. Virol. 2008, 82, 1570-1580.
70. Wang, F.Z.; Akula, S.M.; Sharma-Walia, N.; Zeng, L.; Chandran, B. Human herpesvirus 8 envelope glycoprotein B mediates cell adhesion via its RGD sequence. J. Virol. 2003, 77, 3131-3147.
71. Veettil, M.V.; Sharma-Walia, N.; Sadagopan, S.; Raghu, H.; Sivakumar, R.; Naranatt, P.P.; Chandran, B. RhoA-GTPase facilitates entry of Kaposi’s sarcoma-associated herpesvirus into adherent target cells in a Src-dependent manner. J. Virol. 2006, 80, 11432-11446.
72. Naranatt, P.P.; Akula, S.M.; Zien, C.A.; Krishnan, H.H.; Chandran, B. Kaposi’s sarcoma-associated herpesvirus induces the phosphatidylinositol 3-kinase-PKC-zeta-MEK-ERK signaling pathway in target cells early during infection: Implications for infectivity. J. Virol. 2003, 77, 1524-1539.
73. Naranatt, P.P.; Krishnan, H.H.; Smith, M.S.; Chandran, B. Kaposi’s sarcoma-associated herpesvirus modulates microtubule dynamics via RhoA-GTP-diaphanous 2 signaling and utilizes the dynein motors to deliver its DNA to the nucleus. J. Virol. 2005, 79, 1191-1206.
74. Raghu, H.; Sharma-Walia, N.; Veettil, M.V.; Sadagopan, S.; Caballero, A.; Sivakumar, R.; Varga, L.; Bottero, V.; Chandran, B. Lipid rafts of primary endothelial cells are essential for Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8-induced phosphatidylinositol 3-kinase and RhoA-GTPases critical for microtubule dynamics and nuclear delivery of viral DNA but dispensable for binding and entry. J. Virol. 2007, 81, 7941-7959.
75. Krishnan, H.H.; Sharma-Walia, N.; Streblow, D.N.; Naranatt, P.P.; Chandran, B. Focal adhesion kinase is critical for entry of Kaposi’s sarcoma-associated herpesvirus into target cells. J. Virol. 2006, 80, 1167-1180.
76. Sharma-Walia, N.; Naranatt, P.P.; Krishnan, H.H.; Zeng, L.; Chandran, B. Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8 envelope glycoprotein gB induces the integrin-dependent focal adhesion kinase-Src-phosphatidylinositol 3-kinase-rho GTPase signal pathways and cytoskeletal rearrangements. J. Virol. 2004, 78, 4207-4223.
77. Pan, H.; Xie, J.; Ye, F.; Gao, S.J. Modulation of Kaposi’s sarcoma-associated herpesvirus infection and replication by MEK/ERK, JNK, and p38 multiple mitogen-activated protein kinase pathways during primary infection. J. Virol. 2006, 80, 5371-5382.
78. Sharma-Walia, N.; Krishnan, H.H.; Naranatt, P.P.; Zeng, L.; Smith, M.S.; Chandran, B. ERK1/2 and MEK1/2 induced by Kaposi’s sarcoma-associated herpesvirus (human herpesvirus 8) early during infection of target cells are essential for expression of viral genes and for establishment of infection. J. Virol. 2005, 79, 10308-10329.
79. Greene, W.; Gao, S.J. Actin dynamics regulate multiple endosomal steps during Kaposi’s sarcoma-associated herpesvirus entry and trafficking in endothelial cells. PLoS Pathog. 2009, 5, e1000512.
80. Raghu, H.; Sharma-Walia, N.; Veettil, M.V.; Sadagopan, S.; Chandran, B. Kaposi’s sarcoma-associated herpesvirus utilizes an actin polymerization-dependent macropinocytic pathway to enter human dermal microvascular endothelial and human umbilical vein endothelial cells. J. Virol. 2009, 83, 4895-4911.
81. Mercer, J.; Helenius, A. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320, 531-535.
82. Stiefel, P.; Schmidt, F.I.; Dorig, P.; Behr, P.; Zambelli, T.; Vorholt, J.A.; Mercer, J. Cooperative vaccinia infection demonstrated at the single-cell level using FluidFM. Nano Lett. 2012, 12, 4219-4227.
83. Schmidt, F.I.; Bleck, C.K.; Mercer, J. Poxvirus host cell entry. Curr. Opin. Virol. 2012, 2, 20-27.
84. Traub, L.M.; Bonifacino, J.S. Cargo recognition in clathrin-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 2013, 5.
85. Collawn, J.F.; Stangel, M.; Kuhn, L.A.; Esekogwu, V.; Jing, S.Q.; Trowbridge, I.S.; Tainer, J.A. Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 1990, 63, 1061-1072.
86. Chen, W.J.; Goldstein, J.L.; Brown, M.S. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 1990, 265, 3116-3123.
87. Letourneur, F.; Klausner, R.D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 1992, 69, 1143-1157.
88. Ohno, H.; Aguilar, R.C.; Yeh, D.; Taura, D.; Saito, T.; Bonifacino, J.S. The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 1998, 273, 25915-25921.
89. Pitcher, C.; Honing, S.; Fingerhut, A.; Bowers, K.; Marsh, M. Cluster of differentiation antigen 4 (CD4) endocytosis and adaptor complex binding require activation of the CD4 endocytosis signal by serine phosphorylation. Mol. Biol. Cell 1999, 10, 677-691.
90. Rohrer, J.; Schweizer, A.; Russell, D.; Kornfeld, S. The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J. Cell Biol. 1996, 132, 565-576.
91. Shiratori, T.; Miyatake, S.; Ohno, H.; Nakaseko, C.; Isono, K.; Bonifacino, J.S.; Saito, T. Tyrosine phosphorylation controls internalization of CTLA-4 by regulating its interaction with clathrin-associated adaptor complex AP-2. Immunity 1997, 6, 583-589.
92. Pryor, P.R.; Jackson, L.; Gray, S.R.; Edeling, M.A.; Thompson, A.; Sanderson, C.M.; Evans, P.R.; Owen, D.J.; Luzio, J.P. Molecular basis for the sorting of the SNARE VAMP7 into endocytic clathrin-coated vesicles by the ArfGAP Hrb. Cell 2008, 134, 817-827.
93. Miller, S.E.; Sahlender, D.A.; Graham, S.C.; Honing, S.; Robinson, M.S.; Peden, A.A.; Owen, D.J. The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 2011, 147, 1118-1131.
94. Ferguson, S.S.; Downey, W.E., 3rd; Colapietro, A.M.; Barak, L.S.; Menard, L.; Caron, M.G. Role of β-arrestin in mediating agonist-promoted G protein-coupled receptor internalization. Science 1996, 271, 363-366.
95. Hicke, L.; Riezman, H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 1996, 84, 277-287.
96. Svajger, U.; Anderluh, M.; Jeras, M.; Obermajer, N. C-type lectin DC-SIGN: An adhesion, signaling and antigen-uptake molecule that guides dendritic cells in immunity. Cell. Signal. 2010, 22, 1397-1405.
97. Gringhuis, S.I.; den Dunnen, J.; Litjens, M.; van der Vlist, M.; Geijtenbeek, T.B. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat. Immunol. 2009, 10, 1081-1088.
98. Gringhuis, S.I.; den Dunnen, J.; Litjens, M.; van Het Hof, B.; van Kooyk, Y.; Geijtenbeek, T.B. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-κB. Immunity 2007, 26, 605-616.
99. Braulke, T.; Bonifacino, J.S. Sorting of lysosomal proteins. Biochim. Biophys. Acta 2009, 1793, 605-614.
100. Lozach, P.Y.; Burleigh, L.; Staropoli, I.; Navarro-Sanchez, E.; Harriague, J.; Virelizier, J.L.; Rey, F.A.; Despres, P.; Arenzana-Seisdedos, F.; Amara, A. Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J. Biol. Chem. 2005, 280, 23698-23708.
101. Goncalves, A.R.; Moraz, M.L.; Pasquato, A.; Helenius, A.; Lozach, P.Y.; Kunz, S. Role of DC-SIGN in Lassa virus entry into human dendritic cells. J. Virol. 2013, 87, 11504-11515.
102. Azad, A.K.; Torrelles, J.B.; Schlesinger, L.S. Mutation in the DC-SIGN cytoplasmic triacidic cluster motif markedly attenuates receptor activity for phagocytosis and endocytosis of mannose-containing ligands by human myeloid cells. J. Leukoc. Biol. 2008, 84, 1594-1603.
103. De Witte, L.; de Vries, R.D.; van der Vlist, M.; Yuksel, S.; Litjens, M.; de Swart, R.L.; Geijtenbeek, T.B. DC-SIGN and CD150 have distinct roles in transmission of measles virus from dendritic cells to T-lymphocytes. PLoS Pathog. 2008, 4, e1000049.
104. Maginnis, M.S.; Mainou, B.A.; Derdowski, A.; Johnson, E.M.; Zent, R.; Dermody, T.S. NPXY motifs in the β1 integrin cytoplasmic tail are required for functional reovirus entry. J. Virol. 2008, 82, 3181-3191.
105. Salinas, S.; Zussy, C.; Loustalot, F.; Henaff, D.; Menendez, G.; Morton, P.E.; Parsons, M.; Schiavo, G.; Kremer, E.J. Disruption of the coxsackievirus and adenovirus receptor-homodimeric interaction triggers lipid microdomain- and dynamin-dependent endocytosis and lysosomal targeting. J. Biol. Chem. 2014, 289, 680-695.
106. Tomas, A.; Futter, C.E.; Eden, E.R. EGF receptor trafficking: Consequences for signaling and cancer. Trends Cell Biol. 2014, 24, 26-34.
107. Schelhaas, M. Come in and take your coat off—How host cells provide endocytosis for virus entry. Cell Microbiol. 2010, 12, 1378-1388.
108. Ewers, H.; Helenius, A. Lipid-mediated endocytosis. Cold Spring Harb. Perspect. Biol. 2011, 3.
109. Aigal, S.; Claudinon, J.; Romer, W. Plasma membrane reorganization: A glycolipid gateway for microbes. Biochim. Biophys. Acta 2015, 1853, 858-871.
110. Rydell, G.E.; Svensson, L.; Larson, G.; Johannes, L.; Romer, W. Human GII.4 norovirus VLP induces membrane invaginations on giant unilamellar vesicles containing secretor gene dependent α1,2-fucosylated glycosphingolipids. Biochim. Biophys. Acta 2013, 1828, 1840-1845.
111. Kagan, J.C.; Medzhitov, R. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 2006, 125, 943-955.
112. Kagan, J.C.; Su, T.; Horng, T.; Chow, A.; Akira, S.; Medzhitov, R. TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 2008, 9, 361-368.