Emerging zoonotic viruses: New lessons on receptor and entry mechanisms

Current Opinion in Virology

Volumn 1, Issue 1, 2011, Pages 27-34

  Gerlier, Denis ^a,b  

^a UNIVERSITÉ DE LYON   (France)

^b University Lyon i   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR; EPHRIN B2; EPHRIN B3; P21 ACTIVATED KINASE 1; RAB PROTEIN; RAB7 PROTEIN; RAC1 PROTEIN;

ARTICLE; BAT; EBOLA VIRUS; FILOVIRUS; GENETIC VARIABILITY; HENDRA VIRUS; HENIPAVIRUS; LETHALITY; MARBURG VIRUS; MOLECULAR MECHANICS; NIPAH VIRUS; NONHUMAN; PINOCYTOSIS; RECEPTOR BINDING; RESERVOIR; RNA VIRUS; SARS CORONAVIRUS; VIRUS ENTRY; VIRUS NUCLEOCAPSID;

EID: 79960443826     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2011.05.014     Document Type: Article

References (96)

1. Snowden FM: Emerging and reemerging diseases: a historical perspective. Immunol Rev 2008, 225:9-26.
2. Morens DM, Folkers GK, Fauci AS: Emerging infections: a •• perpetual challenge. Lancet Infect Dis 2008, 8:710-719. An historical overview that allows easy understanding of the "emerging infection" concept.
3. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P: Global trends in emerging infectious diseases. Nature 2008, 451:990-993. (Pubitemid 351301726)
4. Kuba K, Imai Y, Ohto-Nakanishi T, Penninger JM: Trilogy of ace2: •• a peptidase in the renin-angiotensin system, a sars receptor, and a partner for amino acid transporters. Pharmacol Ther 2010, 128:119-128. A review describing known physiological functions of ACE2 that allow the understanding of its key role in the severe lung injury induced by SARS-CoV.
5. Jia HP, Look DC, Tan P, Shi L, Hickey M, Gakhar L, Chappell MC, Wohlford-Lenane C, McCray PB Jr: Ectodomain shedding of angiotensin converting enzyme 2 in human airway epithelia. Am J Physiol Lung Cell Mol Physiol 2009, 297:L84-96.
6. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, Yang P, Sarao R, Wada T, Leong-Poi H, Crackower MA et al.: Angiotensinconverting enzyme 2 protects from severe acute lung failure. Nature 2005, 436:112-116. (Pubitemid 40966195)
7. Oudit GY, Herzenberg AM, Kassiri Z, Wong D, Reich H, Khokha R, Crackower MA, Backx PH, Penninger JM, Scholey JW: Loss of angiotensin-converting enzyme-2 leads to the late development of angiotensin ii-dependent glomerulosclerosis. Am J Pathol 2006, 168:1808-1820. (Pubitemid 43825302)
8. Crackower MA, Sarao R, Oudit GY, Yagil C, Kozieradzki I, Scanga SE, Oliveira-dos-Santos AJ, da Costa J, Zhang L, Pei Y, Scholey J et al.: Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature 2002, 417:822-828. (Pubitemid 34670323)
9. Chen Y, Chan VS, Zheng B, Chan KY, Xu X, To LY, Huang FP, Khoo US, Lin CL: A novel subset of putative stem/progenitor cd34+oct-4+ cells is the major target for sars coronavirus in human lung. J Exp Med 2007, 204:2529-2536. (Pubitemid 350044778)
10. Shulla A, Heald-Sargent T, Subramanya G, Zhao J, Perlman S, • Gallagher T: A transmembrane serine protease is linked to the severe acute respiratory syndrome coronavirus receptor and activates virus entry. J Virol 2011, 85:873-882. These three convergent and complementary papers describe the TMPRSS2 ectoprotease as a partner of ACE2 receptor responsible for both activation of SARS-CoV S protein allowing virus entry and shedding of ACE2 ectodomain.
11. •]
12. bull;]
13. Vaarala MH, Porvari KS, Kellokumpu S, Kyllonen AP, Vihko PT: Expression of transmembrane serine protease TMPRSS2 in mouse and human tissues. J Pathol 2001, 193:134-140. (Pubitemid 32051123)
14. Hamming I, Timens W, Bulthuis ML, Lely AT, Navis GJ, van Goor H: Tissue distribution of ace2 protein, the functional receptor for sars coronavirus. A first step in understanding sars pathogenesis. J Pathol 2004, 203:631-637. (Pubitemid 38714099)
15. Li F, Li W, Farzan M, Harrison SC: Structure of sars coronavirus •• spike receptor-binding domain complexed with receptor. Science 2005, 309:1864-1868. The solved structure illuminates the viral spike binding site on ACE2 receptor. (Pubitemid 41325098)
16. Belouzard S, Chu VC, Whittaker GR: Activation of the sars coronavirus spike protein via sequential proteolytic cleavage at two distinct sites. Proc Natl Acad Sci USA 2009, 106:5871-5876.
17. Roche S, Albertini AA, Lepault J, Bressanelli S, Gaudin Y: Structures of vesicular stomatitis virus glycoprotein: membrane fusion revisited. Cell Mol Life Sci 2008, 65:1716-1728.
18. Kam YW, Okumura Y, Kido H, Ng LF, Bruzzone R, Altmeyer R: Cleavage of the sars coronavirus spike glycoprotein by airway proteases enhances virus entry into human bronchial epithelial cells in vitro. PLoS ONE 2009, 4:e7870.
19. Haga S, Yamamoto N, Nakai-Murakami C, Osawa Y, Tokunaga K, Sata T, Sasazuki T, Ishizaka Y: Modulation of tnf-alphaconverting enzyme by the spike protein of sars-cov and ace2 induces tnf-alpha production and facilitates viral entry. Proc Natl Acad Sci USA 2008, 105:7809-7814. (Pubitemid 351872720)
20. Glowacka I, Bertram S, Herzog P, Pfefferle S, Steffen I, Muench MO, Simmons G, Hofmann H, Kuri T, Weber F, Eichler J et al.: Differential downregulation of ace2 by the spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus nl63. J Virol 2010, 84:1198-1205.
21. Kuba K, Imai Y, Rao S, Gao H, Guo F, Guan B, Huan Y, Yang P, Zhang Y, Deng W, Bao L et al.: A crucial role of angiotensin converting enzyme 2 (ace2) in sars coronavirus-induced lung injury. Nat Med 2005, 11:875-879. (Pubitemid 41161120)
22. Li W, Zhang C, Sui J, Kuhn JH, Moore MJ, Luo S, Wong SK, •• Huang IC, Xu K, Vasilieva N, Murakami A et al.: Receptor and viral determinants of sars-coronavirus adaptation to human ace2 EMBO J 2005, 24:1634-1643. The solved structure illuminates the viral spike binding site on ACE2 receptor. (Pubitemid 40646452)
23. Li W, Wong SK, Li F, Kuhn JH, Huang IC, Choe H, Farzan M: Animal origins of the severe acute respiratory syndrome coronavirus: insight from ace2-s-protein interactions. J Virol 2006, 80:4211-4219.
24. Li F: Structural analysis of major species barriers between humans and palm civets for severe acute respiratory syndrome coronavirus infections. J Virol 2008, 82:6984-6991. (Pubitemid 351977719)
25. Graham RL, Baric RS: Recombination, reservoirs, and the modular spike: Mechanisms of coronavirus cross-species transmission. J Virol 2010, 84:3134-3146.
26. Hou Y, Peng C, Yu M, Li Y, Han Z, Li F, Wang LF, Shi Z: Angiotensin-converting enzyme 2 (ace2) proteins of different bat species confer variable susceptibility to sars-cov entry. Arch Virol 2010, 155:1563-1569.
27. Yu M, Tachedjian M, Crameri G, Shi Z, Wang LF: Identification of key amino acid residues required for horseshoe bat angiotensin-i converting enzyme 2 to function as a receptor for severe acute respiratory syndrome coronavirus. J Gen Virol 2010, 91:1708-1712.
28. Diederich S, Moll M, Klenk HD, Maisner A: The nipah virus fusion protein is cleaved within the endosomal compartment. J Biol Chem 2005, 280:29899-29903. (Pubitemid 41177067)
29. Pager CT, Craft WW Jr, Patch J, Dutch RE: A mature and fusogenic form of the nipah virus fusion protein requires proteolytic processing by cathepsin l. Virology 2006, 346:251-257. (Pubitemid 43357869)
30. Bowden TA, Crispin M, Harvey DJ, Jones EY, Stuart DI: Dimeric architecture of the hendra virus attachment glycoprotein: evidence for a conserved mode of assembly. J Virol 2010, 84:6208-6217.
31. Bowden TA, Crispin M, Harvey DJ, Aricescu AR, Grimes JM, Jones EY, Stuart DI: Crystal structure and carbohydrate analysis of nipah virus attachment glycoprotein: a template for antiviral and vaccine design. J Virol 2008, 82:11628-11636.
32. Lee B: Envelope-receptor interactions in nipah virus pathobiology. Ann N YAcad Sci 2007, 1102:51-65. (Pubitemid 47084909)
33. Pitulescu ME, Adams RH: Eph/ephrin molecules-a hub for • signaling and endocytosis. Genes Dev 2010, 24:2480-2492. Complete review to understand the role of Eph/ephrin molecules in cellcell communication and homeostasis.
34. Shin D, Garcia-Cardena G, Hayashi S, Gerety S, Asahara T, Stavrakis G, Isner J, Folkman J, Gimbrone MA Jr, Anderson DJ: Expression of ephrinb2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev Biol 2001, 230:139-150. (Pubitemid 32171413)
35. Negrete OA, Chu D, Aguilar HC, Lee B: Single amino acid changes in the nipah and hendra virus attachment glycoproteins distinguish ephrinb2 from ephrinb3 usage. J Virol 2007, 81:10804-10814. (Pubitemid 47463353)
36. Bowden TA, Aricescu AR, Gilbert RJ, Grimes JM, Jones EY, •• Stuart DI: Structural basis of nipah and hendra virus attachment to their cell-surface receptor ephrin-b2. Nat Struct Mol Biol 2008, 15:567-572. Crystal structure of Henipavirus G proteins with ephrinB2 receptor showing the central role of the G-H loop of ephrinB2 in the interface and location of the binding site on the edge of the top side of the globular head of G proteins. (Pubitemid 351799140)
37. Hashiguchi T, Ose T, Kubota M, Maita N, Kamishikiryo J, Maenaka K, Yanagi Y: Structure of the measles virus hemagglutinin bound to its cellular receptor slam. Nat Struct Mol Biol 2011, 18:135-141.
38. Qin H, Noberini R, Huan X, Shi J, Pasquale EB, Song J: Structural characterization of the epha4-ephrin-b2 complex reveals new features enabling eph-ephrin binding promiscuity. J Biol Chem 2010, 285:644-654.
39. Himanen JP, Saha N, Nikolov DB: Cell-cell signaling via eph receptors and ephrins. Curr Opin Cell Biol 2007, 19:534-542. (Pubitemid 350016850)
40. Negrete OA, Wolf MC, Aguilar HC, Enterlein S, Wang W, • Muhlberger E, Su SV, Bertolotti-Ciarlet A, Flick R, Lee B: Two key residues in ephrinb3 are critical for its use as an alternative receptor for nipah virus. PLoS Pathog 2006, 2:e7. By mutagenesis of two amino acid that differ between ephrinB1 and ephrinB3 within the G-H loop and using binding and virus entry assays, the molecular basis of ephrinB2/B3 exclusive usage as henipavirus receptor was established.
41. Tanimura N, Imada T, Kashiwazaki Y, Sharifah SH: Distribution of viral antigens and development of lesions in chicken embryos inoculated with nipah virus. J Comp Pathol 2006, 135:74-82. (Pubitemid 44417992)
42. Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, Lam SK, Ksiazek TG, Rollin PE, Zaki SR, Shieh W, Goldsmith CS et al.: Nipah virus: a recently emergent deadly paramyxovirus. Science 2000, 288:1432-1435. (Pubitemid 30366331)
43. Middleton DJ, Westbury HA, Morrissy CJ, van der Heide BM, Russell GM, Braun MA, Hyatt AD: Experimental nipah virus infection in pigs and cats. J Comp Pathol 2002, 126:124-136.
44. Mungall BA, Middleton D, Crameri G, Halpin K, Bingham J, Eaton BT, Broder CC: Vertical transmission and fetal replication of nipah virus in an experimentally infected cat. J Infect Dis 2007, 196:812-816. (Pubitemid 47378929)
45. Wong KT, Shieh WJ, Kumar S, Norain K, Abdullah W, Guarner J, Goldsmith CS, Chua KB, Lam SK, Tan CT, Goh KJ et al.: Nipah virus infection: pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am J Pathol 2002, 161:2153-2167. (Pubitemid 35434861)
46. *ephrinb2 proteinprotein interaction and receptor specificity. J Biol Chem 2006, 281:28185-28192. (Pubitemid 44414532)
47. Himanen JP, Rajashankar KR, Lackmann M, Cowan CA, Henkemeyer M, Nikolov DB: Crystal structure of an eph receptor-ephrin complex. Nature 2001, 414:933-938. (Pubitemid 34024747)
48. Bossart KN, Tachedjian M, McEachern JA, Crameri G, Zhu Z, Dimitrov DS, Broder CC, Wang LF: Functional studies of hostspecific ephrin-b ligands as henipavirus receptors. Virology 2008, 372:357-371. (Pubitemid 351284563)
49. Bossart KN, Zhu Z, Middleton D, Klippel J, Crameri G, Bingham J, • McEachern JA, Green D, Hancock TJ, Chan YP, Hickey AC et al.: A neutralizing human monoclonal antibody protects against lethal disease in a new ferret model of acute nipah virus infection. PLoS Pathog 2009, 5:e1000642. Demonstration of receptor binding site on NiV G protein as potent target for neutralizing antibody.
50. Mungall BA, Middleton D, Crameri G, Bingham J, Halpin K, Russell G, Green D, McEachern J, Pritchard LI, Eaton BT, Wang LF et al.: Feline model of acute nipah virus infection and protection with a soluble glycoprotein-based subunit vaccine. J Virol 2006, 80:12293-12302. (Pubitemid 44904379)
51. Aguilar HC, Aspericueta V, Robinson LR, Aanensen KE, Lee B: A quantitative and kinetic fusion protein-triggering assay can discern distinct steps in the nipah virus membrane fusion cascade. J Virol 2010, 84:8033-8041.
52. Pernet O, Pohl C, Ainouze M, Kweder H, Buckland R: Nipah virus •• entry can occur by macropinocytosis. Virology 2009, 395:298-311. The use of chemical inhibitors and molecular tools strongly supports macropinocytosis as a major pH independent entry pathway for NiV with a key role for ephrinB2 cytosolic tail although G/F complex can mediate fusion at the cell surface.
53. Porotto M, Orefice G, Yokoyama CC, Mungall BA, Realubit R, Sganga ML, Aljofan M, Whitt M, Glickman F, Moscona A: Simulating henipavirus multicycle replication in a screening assay leads to identification of a promising candidate for therapy. J Virol 2009, 83:5148-5155.
54. Cowan CA, Henkemeyer M: The sh2/sh3 adaptor grb4 transduces b-ephrin reverse signals. Nature 2001, 413:174-179. (Pubitemid 32867879)
55. Bruckner K, Pasquale EB, Klein R: Tyrosine phosphorylation of transmembrane ligands for eph receptors. Science 1997, 275:1640-1643. (Pubitemid 27120539)
56. Mercer J, Helenius A: Virus entry by macropinocytosis. Nat Cell • Biol 2009, 11:510-520. A useful review describing the molecular machinery of macropinocytosis and defining molecular criteria required for validating the use of this entry pathway by viruses.
57. Mercer J, Helenius A: Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 2008, 320:531-535. (Pubitemid 351590666)
58. Meier O, Boucke K, Hammer SV, Keller S, Stidwill RP, Hemmi S, Greber UF: Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 2002, 158:1119-1131.
59. Amstutz B, Gastaldelli M, Kalin S, Imelli N, Boucke K, Wandeler E, Mercer J, Hemmi S, Greber UF: Subversion of ctbp1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J 2008, 27:956-969. (Pubitemid 351508148)
60. Hammarfjord O, Wallin RP: Dendritic cell function at low physiological temperature. J Leukoc Biol 2010, 88:747-756.
61. Zhu MX, Ma J, Parrington J, Galione A, Evans AM: Tpcs: endolysosomal channels for ca2+ mobilization from acidic organelles triggered by naadp. FEBS Lett 2010, 584:1966-1974.
62. Helenius A, Kielian M, Wellsteed J, Mellman I, Rudnick G: Effects of monovalent cations on semliki forest virus entry into bhk-21 cells. J Biol Chem 1985, 260:5691-5697. (Pubitemid 15001130)
63. Spielhofer P, Bachi T, Fehr T, Christiansen G, Cattaneo R, Kaelin K, Billeter MA, Naim HY: Chimeric measles viruses with a foreign envelope. J Virol 1998, 72:2150-2159. (Pubitemid 28100771)
64. Frecha C, Costa C, Negre D, Gauthier E, Russell SJ, Cosset FL, Verhoeyen E: Stable transduction of quiescent t cells without induction of cycle progression by a novel lentiviral vector pseudotyped with measles virus glycoproteins. Blood 2008, 112:4843-4852.
65. Funke S, Schneider IC, Glaser S, Muhlebach MD, Moritz T, Cattaneo R, Cichutek K, Buchholz CJ: Pseudotyping lentiviral vectors with the wild-type measles virus glycoproteins improves titer and selectivity. Gene Ther 2009, 16:700-705.
66. Feldmann H, Geisbert TW: Ebola haemorrhagic fever. Lancet 2011, 377:849-862.
67. Volchkov VE, Feldmann H, Volchkova VA, Klenk HD: Processing of the ebola virus glycoprotein by the proprotein convertase furin. Proc Natl Acad Sci USA 1998, 95:5762-5767.
68. Wool-Lewis RJ, Bates P: Endoproteolytic processing of the ebola virus envelope glycoprotein: cleavage is not required for function. J Virol 1999, 73:1419-1426. (Pubitemid 29036797)
69. Powlesland AS, Fisch T, Taylor ME, Smith DF, Tissot B, Dell A, Pohlmann S, Drickamer K: A novel mechanism for lsectin binding to ebola virus surface glycoprotein through truncated glycans. J Biol Chem 2008, 283:593-602.
70. Matsuno K, Kishida N, Usami K, Igarashi M, Yoshida R, Nakayama E, Shimojima M, Feldmann H, Irimura T, Kawaoka Y, Takada A: Different potential of c-type lectin-mediated entry between marburg virus strains. J Virol 2010, 84:5140-5147.
71. Gramberg T, Hofmann H, Moller P, Lalor PF, Marzi A, Geier M, Krumbiegel M, Winkler T, Kirchhoff F, Adams DH, Becker S et al.: Lsectin interacts with filovirus glycoproteins and the spike protein of sars coronavirus. Virology 2005, 340:224-236. (Pubitemid 41317496)
72. Gramberg T, Soilleux E, Fisch T, Lalor PF, Hofmann H, Wheeldon S, Cotterill A, Wegele A, Winkler T, Adams DH, Pohlmann S: Interactions of lsectin and dc-sign/dc-signr with viral ligands: differential ph dependence, internalization and virion binding. Virology 2008, 373:189-201.
73. Francica JR, Varela-Rohena A, Medvec A, Plesa G, Riley JL, Bates P: Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog 2010:6.
74. Reynard O, Borowiak M, Volchkova VA, Delpeut S, Mateo M, Volchkov VE: Ebolavirus glycoprotein gp masks both its own epitopes and the presence of cellular surface proteins. J Virol 2009, 83:9596-9601.
75. Takada A, Watanabe S, Ito H, Okazaki K, Kida H, Kawaoka Y: Downregulation of beta1 integrins by ebola virus glycoprotein: implication for virus entry.2000, 278:20-26.
76. Dube D, Brecher MB, Delos SE, Rose SC, Park EW, Schornberg KL, Kuhn JH, White JM: The primed ebolavirus glycoprotein (19-kilodalton gp1, 2): sequence and residues critical for host cell binding. J Virol 2009, 83:2883-2891. Soluble GP and mutagenesis rationally designed from prefusion GP 3D structure allowed the detailed delineation of the RBR of EboV GP1.
77. Takada A, Robison C, Goto H, Sanchez A, Murti KG, Whitt MA, Kawaoka Y: A system for functional analysis of ebola virus glycoprotein. Proc Natl Acad Sci USA 1997, 94:14764-14769. (Pubitemid 28041448)
78. Dube D, Schornberg KL, Shoemaker CJ, Delos SE, Stantchev TS, • Clouse KA, Broder CC, White JM: Cell adhesion-dependent membrane trafficking of a binding partner for the ebolavirus glycoprotein is a determinant of viral entry. Proc Natl Acad Sci USA 2010, 107:16637-16642. These two papers demonstrate the intracellular pool of RBR binding protein of EboV that can be exported to the cell surface upon cell adhesion including in lymphocyte, which are refractory to EboV infection probably because they poorly able to prime GP.
79. •] (Pubitemid 351977741)
80. Kuhn JH, Radoshitzky SR, Guth AC, Warfield KL, Li W, Vincent MJ, Towner JS, Nichol ST, Bavari S, Choe H, Aman MJ et al.: Conserved receptor-binding domains of lake victoria marburgvirus and zaire ebolavirus bind a common receptor. J Biol Chem 2006, 281:15951-15958. (Pubitemid 43848488)
81. Brindley MA, Hughes L, Ruiz A, McCray PB Jr, Sanchez A, •• Sanders DA, Maury W: Ebola virus glycoprotein 1: identification of residues important for binding and postbinding events. J Virol 2007, 81:7702-7709. A systematic mutagenesis study that has allowed the delineation of key residues of EboV RBR within GP1. (Pubitemid 47047855)
82. Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, •• Saphire EO: Structure of the ebola virus glycoprotein bound to an antibody from a human survivor. Nature 2008, 454:177-182. A first structure of prefusion EboV GP1-GP2 heterodimer showing the mucin-like domain covering the RBR site and location of GP2 at the basis of the GP1 chalice fold. (Pubitemid 351969896)
83. Kaletsky RL, Simmons G, Bates P: Proteolysis of the ebola virus glycoproteins enhances virus binding and infectivity. J Virol 2007, 81:13378-13384. (Pubitemid 350247834)
84. Schornberg K, Matsuyama S, Kabsch K, Delos S, Bouton A, •• White J: Role of endosomal cathepsins in entry mediated by the ebola virus glycoprotein. J Virol 2006, 80:4174-4178. First demonstration for a two-step activation of EboV GP occurring in the endosomal pathway using chemical inhibitors, RNA silencing, and biochemical cleavage by cathepsins.
85. Nanbo A, Imai M, Watanabe S, Noda T, Takahashi K, Neumann G, •• Halfmann P, Kawaoka Y: Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner. PLoS Pathog 2010, 6:e1001121. Using Ebolavirus like particles made of GP and VP40, a close mimic of the filamentous EboV, infectious EboV and dedicated molecular tools and chemical inhibitors, entry by macropinocytosis was demonstrated by these two papers.
86. ••]
87. Quinn K, Brindley MA, Weller ML, Kaludov N, Kondratowicz A, Hunt CL, Sinn PL, McCray PB Jr, Stein CS, Davidson BL, Flick R et al.: Rho gtpases modulate entry of ebola virus and vesicular stomatitis virus pseudotyped vectors. J Virol 2009, 83:10176-10186.
88. Liberali P, Kakkonen E, Turacchio G, Valente C, Spaar A, Perinetti G, Bockmann RA, Corda D, Colanzi A, Marjomaki V, Luini A: The closure of pak1-dependent macropinosomes requires the phosphorylation of ctbp1/bars. EMBO J 2008, 27:970-981. (Pubitemid 351508162)
89. Kalin S, Amstutz B, Gastaldelli M, Wolfrum N, Boucke K, Havenga M, DiGennaro F, Liska N, Hemmi S, Greber UF: Macropinocytotic uptake and infection of human epithelial cells with species b2 adenovirus type 35. J Virol 2010, 84:5336-5350.
90. Norbury CC, Chambers BJ, Prescott AR, Ljunggren HG, Watts C: Constitutive macropinocytosis allows tap-dependent major histocompatibility complex class i presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 1997, 27:280-288. (Pubitemid 27046089)
91. Norbury CC, Hewlett LJ, Prescott AR, Shastri N, Watts C: Class i mhc presentation of exogenous soluble antigen via macropinocytosis in bone marrow macrophages. Immunity 1995, 3:783-791. (Pubitemid 26091151)
92. Hunt CL, Kolokoltsov AA, Davey RA, Maury W: The tyro3 receptor kinase axl enhances macropinocytosis of zaire ebolavirus. J Virol 2011, 85:334-347.
93. Morizono K, Xie Y, Olafsen T, Lee B, Dasgupta A, Wu AM, Chen IS: The soluble serum protein gas6 bridges virion envelope phosphatidylserine to the tam receptor tyrosine kinase axl to mediate viral entry. Cell Host Microbe 2011, 9:286-298.
94. Saeed MF, Kolokoltsov AA, Freiberg AN, Holbrook MR, Davey RA: Phosphoinositide-3 kinase-akt pathway controls cellular entry of ebola virus. PLoS Pathog 2008, 4:e1000141.
95. Schelhaas M: Come in and take your coat off-how host cells provide endocytosis for virus entry. Cell Microbiol 2010, 12:1378-1388.
96. Chandran K, Sullivan NJ, Felbor U, Whelan SP, Cunningham JM: Endosomal proteolysis of the ebola virus glycoprotein is necessary for infection. Science 2005, 308:1643-1645. (Pubitemid 40807517)