Ebolavirus Is Internalized into Host Cells Macropinocytosis in a Viral Glycoprotein-Dependent Manner

1. ConnerSD

SchmidSL

2003 Regulated portals of entry into the cell. Nature 422 37 44

2. SieczkarskiSB

WhittakerGR

2002 Dissecting virus entry via endocytosis. J Gen Virol 83 1535 1545

3. MarshM

HeleniusA

2006 Virus entry: open sesame. Cell 124 729 740

4. MarshM

HeleniusA

1980 Adsorptive endocytosis of Semliki Forest virus. J Mol Biol 142 439 454

5. MatlinKS

ReggioH

HeleniusA

SimonsK

1981 Infectious entry pathway of influenza virus in a canine kidney cell line. J Cell Biol 91 601 613

6. MatlinKS

ReggioH

HeleniusA

SimonsK

1982 Pathway of vesicular stomatitis virus entry leading to infection. J Mol Biol 156 609 631

7. VeigaE

CossartP

2005 Listeria hijacks the clathrin-dependent endocytic machinery to invade mammalian cells. Nat Cell Biol 7 894 900

8. VeigaE

CossartP

2006 The role of clathrin-dependent endocytosis in bacterial internalization. Trends Cell Biol 16 499 504

9. PelkmansL

KartenbeckJ

HeleniusA

2001 Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 3 473 483

10. StuartLM

EzekowitzRA

2005 Phagocytosis: elegant complexity. Immunity 22 539 550

11. AderemA

UnderhillDM

1999 Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17 593 623

12. ClementC

TiwariV

ScanlanPM

Valyi-NagyT

YueBY

2006 A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol 174 1009 1021

13. GhigoE

KartenbeckJ

LienP

PelkmansL

CapoC

2008 Ameobal pathogen mimivirus infects macrophages through phagocytosis. PLoS Pathog 4 e1000087

14. JonesAT

2007 Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. J Cell Mol Med 11 670 684

15. KerrMC

TeasdaleRD

2009 Defining macropinocytosis. Traffic 10 364 371

16. MercerJ

HeleniusA

2009 Virus entry by macropinocytosis. Nat Cell Biol 11 510 520

17. SwansonJA

WattsC

1995 Macropinocytosis. Trends Cell Biol 5 424 428

18. SallustoF

CellaM

DanieliC

LanzavecchiaA

1995 Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 182 389 400

19. NorburyCC

ChambersBJ

PrescottAR

LjunggrenHG

WattsC

1997 Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur J Immunol 27 280 288

20. KryskoDV

DeneckerG

FestjensN

GabrielsS

ParthoensE

2006 Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells. Cell Death Differ 13 2011 2022

21. HaiglerHT

McKannaJA

CohenS

1979 Rapid stimulation of pinocytosis in human carcinoma cells A-431 by epidermal growth factor. J Cell Biol 83 82 90

22. DowrickP

KenworthyP

McCannB

WarnR

1993 Circular ruffle formation and closure lead to macropinocytosis in hepatocyte growth factor/scatter factor-treated cells. Eur J Cell Biol 61 44 53

23. AmyereM

PayrastreB

KrauseU

Van Der SmissenP

VeithenA

2000 Constitutive macropinocytosis in oncogene-transformed fibroblasts depends on sequential permanent activation of phosphoinositide 3-kinase and phospholipase C. Mol Biol Cell 11 3453 3467

24. DharmawardhaneS

SchurmannA

SellsMA

ChernoffJ

SchmidSL

2000 Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell 11 3341 3352

25. KasaharaK

NakayamaY

SatoI

IkedaK

HoshinoM

2007 Role of Src-family kinases in formation and trafficking of macropinosomes. J Cell Physiol 211 220 232

26. MercerJ

HeleniusA

2008 Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320 531 535

27. RidleyAJ

PatersonHF

JohnstonCL

DiekmannD

HallA

1992 The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70 401 410

28. WestMA

PrescottAR

EskelinenEL

RidleyAJ

WattsC

2000 Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol 10 839 848

29. NorburyCC

2006 Drinking a lot is good for dendritic cells. Immunology 117 443 451

30. LiberaliP

KakkonenE

TuracchioG

ValenteC

SpaarA

2008 The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J 27 970 981

31. ArakiN

JohnsonMT

SwansonJA

1996 A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135 1249 1260

32. SwansonJA

2008 Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9 639 649

33. AmstutzB

GastaldelliM

KalinS

ImelliN

BouckeK

2008 Subversion of CtBP1-controlled macropinocytosis by human adenovirus serotype 3. EMBO J 27 956 969

34. RaghuH

Sharma-WaliaN

VeettilMV

SadagopanS

ChandranB

2009 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 83 4895 4911

35. PernetO

PohlC

AinouzeM

KwederH

BucklandR

2009 Nipah virus entry can occur by macropinocytosis. Virology 395 298 311

36. LiuNQ

LossinskyAS

PopikW

LiX

GujuluvaC

2002 Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J Virol 76 6689 6700

37. MarechalV

PrevostMC

PetitC

PerretE

HeardJM

2001 Human immunodeficiency virus type 1 entry into macrophages mediated by macropinocytosis. J Virol 75 11166 11177

38. MeierO

BouckeK

HammerSV

KellerS

StidwillRP

2002 Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 158 1119 1131

39. Wool-LewisRJ

BatesP

1998 Characterization of Ebola virus entry by using pseudotyped viruses: identification of receptor-deficient cell lines. J Virol 72 3155 3160

40. ChanSY

EmpigCJ

WelteFJ

SpeckRF

SchmaljohnA

2001 Folate receptor-alpha is a cofactor for cellular entry by Marburg and Ebola viruses. Cell 106 117 126

41. AlvarezCP

LasalaF

CarrilloJ

MunizO

CorbiAL

2002 C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J Virol 76 6841 6844

42. BaribaudF

DomsRW

PohlmannS

2002 The role of DC-SIGN and DC-SIGNR in HIV and Ebola virus infection: can potential therapeutics block virus transmission and dissemination? Expert Opin Ther Targets 6 423 431

43. JiX

OlingerGG

ArisS

ChenY

GewurzH

2005 Mannose-binding lectin binds to Ebola and Marburg envelope glycoproteins, resulting in blocking of virus interaction with DC-SIGN and complement-mediated virus neutralization. J Gen Virol 86 2535 2542

44. LasalaF

ArceE

OteroJR

RojoJ

DelgadoR

2003 Mannosyl glycodendritic structure inhibits DC-SIGN-mediated Ebola virus infection in cis and in trans. Antimicrob Agents Chemother 47 3970 3972

45. SimmonsG

ReevesJD

GroganCC

VandenbergheLH

BaribaudF

2003 DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305 115 123

46. TakadaA

FujiokaK

TsuijiM

MorikawaA

HigashiN

2004 Human macrophage C-type lectin specific for galactose and N-acetylgalactosamine promotes filovirus entry. J Virol 78 2943 2947

47. TakadaA

WatanabeS

ItoH

OkazakiK

KidaH

2000 Downregulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology 278 20 26

48. ShimojimaM

IkedaY

KawaokaY

2007 The mechanism of Axl-mediated Ebola virus infection. J Infect Dis 196 Suppl 2 S259 263

49. ShimojimaM

TakadaA

EbiharaH

NeumannG

FujiokaK

2006 Tyro3 family-mediated cell entry of Ebola and Marburg viruses. J Virol 80 10109 10116

50. EmpigCJ

GoldsmithMA

2002 Association of the caveola vesicular system with cellular entry by filoviruses. J Virol 76 5266 5270

51. SimmonsG

RennekampAJ

ChaiN

VandenbergheLH

RileyJL

2003 Folate receptor alpha and caveolae are not required for Ebola virus glycoprotein-mediated viral infection. J Virol 77 13433 13438

52. BrindleyMA

HughesL

RuizA

McCrayPBJr

SanchezA

2007 Ebola virus glycoprotein 1: identification of residues important for binding and postbinding events. J Virol 81 7702 7709

53. ChandranK

SullivanNJ

FelborU

WhelanSP

CunninghamJM

2005 Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308 1643 1645

54. KaletskyRL

SimmonsG

BatesP

2007 Proteolysis of the Ebola virus glycoproteins enhances virus binding and infectivity. J Virol 81 13378 13384

55. LeeJE

FuscoML

HessellAJ

OswaldWB

BurtonDR

2008 Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Nature 454 177 182

56. SchornbergK

MatsuyamaS

KabschK

DelosS

BoutonA

2006 Role of endosomal cathepsins in entry mediated by the Ebola virus glycoprotein. J Virol 80 4174 4178

57. BavariS

BosioCM

WiegandE

RuthelG

WillAB

2002 Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J Exp Med 195 593 602

58. YonezawaA

CavroisM

GreeneWC

2005 Studies of ebola virus glycoprotein-mediated entry and fusion by using pseudotyped human immunodeficiency virus type 1 virions: involvement of cytoskeletal proteins and enhancement by tumor necrosis factor alpha. J Virol 79 918 926

59. SanchezA

2007 Analysis of filovirus entry into vero e6 cells, using inhibitors of endocytosis, endosomal acidification, structural integrity, and cathepsin (B and L) activity. J Infect Dis 196 Suppl 2 S251 258

60. BhattacharyyaS

WarfieldKL

RuthelG

BavariS

AmanMJ

Ebola virus uses clathrin-mediated endocytosis as an entry pathway. Virology 401 18 28

61. TakadaA

RobisonC

GotoH

SanchezA

MurtiKG

1997 A system for functional analysis of Ebola virus glycoprotein. Proc Natl Acad Sci U S A 94 14764 14769

62. HalfmannP

KimJH

EbiharaH

NodaT

NeumannG

2008 Generation of biologically contained Ebola viruses. Proc Natl Acad Sci U S A 105 1129 1133

63. KallstromG

WarfieldKL

SwensonDL

MortS

PanchalRG

2005 Analysis of Ebola virus and VLP release using an immunocapture assay. J Virol Methods 127 1 9

64. NodaT

SagaraH

SuzukiE

TakadaA

KidaH

2002 Ebola virus VP40 drives the formation of virus-like filamentous particles along with GP. J Virol 76 4855 4865

65. WatanabeS

WatanabeT

NodaT

TakadaA

FeldmannH

2004 Production of novel ebola virus-like particles from cDNAs: an alternative to ebola virus generation by reverse genetics. J Virol 78 999 1005

66. LicataJM

JohnsonRF

HanZ

HartyRN

2004 Contribution of ebola virus glycoprotein, nucleoprotein, and VP24 to budding of VP40 virus-like particles. J Virol 78 7344 7351

67. SakaiT

OhuchiM

ImaiM

MizunoT

KawasakiK

2006 Dual wavelength imaging allows analysis of membrane fusion of influenza virus inside cells. J Virol 80 2013 2018

68. Le BlancI

LuyetPP

PonsV

FergusonC

EmansN

2005 Endosome-to-cytosol transport of viral nucleocapsids. Nat Cell Biol 7 653 664

69. LakadamyaliM

RustMJ

BabcockHP

ZhuangX

2003 Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 100 9280 9285

70. GaidarovI

SantiniF

WarrenRA

KeenJH

1999 Spatial control of coated-pit dynamics in living cells. Nat Cell Biol 1 1 7

71. MerrifieldCJ

FeldmanME

WanL

AlmersW

2002 Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4 691 698

72. RustMJ

LakadamyaliM

ZhangF

ZhuangX

2004 Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11 567 573

73. TorgersenML

SkrettingG

van DeursB

SandvigK

2001 Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114 3737 3747

74. DammEM

PelkmansL

KartenbeckJ

MezzacasaA

KurzchaliaT

2005 Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J Cell Biol 168 477 488

75. OrthJD

KruegerEW

CaoH

McNivenMA

2002 The large GTPase dynamin regulates actin comet formation and movement in living cells. Proc Natl Acad Sci U S A 99 167 172

76. NewtonAJ

KirchhausenT

MurthyVN

2006 Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc Natl Acad Sci U S A 103 17955 17960

77. KerrMC

LindsayMR

LuetterforstR

HamiltonN

SimpsonF

2006 Visualisation of macropinosome maturation by the recruitment of sorting nexins. J Cell Sci 119 3967 3980

78. LimJP

WangJT

KerrMC

TeasdaleRD

GleesonPA

2008 A role for SNX5 in the regulation of macropinocytosis. BMC Cell Biol 9 58

79. RacoosinEL

SwansonJA

1993 Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 121 1011 1020

80. ChavrierP

PartonRG

HauriHP

SimonsK

ZerialM

1990 Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62 317 329

81. RybinV

UllrichO

RubinoM

AlexandrovK

SimonI

1996 GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature 383 266 269

82. ItoH

WatanabeS

SanchezA

WhittMA

KawaokaY

1999 Mutational analysis of the putative fusion domain of Ebola virus glycoprotein. J Virol 73 8907 8912

83. GiraoH

GeliMI

IdrissiFZ

2008 Actin in the endocytic pathway: from yeast to mammals. FEBS Lett 582 2112 2119

84. WalkerEH

PacoldME

PerisicO

StephensL

HawkinsPT

2000 Structural determinants of phosphoinositide 3-kinase inhibition by wortmannin, LY294002, quercetin, myricetin, and staurosporine. Mol Cell 6 909 919

85. KoivusaloM

WelchC

HayashiH

ScottCC

KimM

Amiloride inhibits macropinocytosis by lowering submembranous pH and preventing Rac1 and Cdc42 signaling. J Cell Biol 188 547 563

86. WestMA

BretscherMS

WattsC

1989 Distinct endocytotic pathways in epidermal growth factor-stimulated human carcinoma A431 cells. J Cell Biol 109 2731 2739

87. SunX

WhittakerGR

2007 Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell Microbiol 9 1672 1682

88. EhrhardtC

MarjukiH

WolffT

NurnbergB

PlanzO

2006 Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell Microbiol 8 1336 1348

89. SubausteMC

Von HerrathM

BenardV

ChamberlainCE

ChuangTH

2000 Rho family proteins modulate rapid apoptosis induced by cytotoxic T lymphocytes and Fas. J Biol Chem 275 9725 9733

90. OmuraS

IwaiY

HiranoA

NakagawaA

AwayaJ

1977 A new alkaloid AM-2282 OF Streptomyces origin. Taxonomy, fermentation, isolation and preliminary characterization. J Antibiot (Tokyo) 30 275 282

91. WestphalM

JungbluthA

HeideckerM

MuhlbauerB

HeizerC

1997 Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 7 176 183

92. FengY

PressB

Wandinger-NessA

1995 Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131 1435 1452

93. SaeedMF

KolokoltsovAA

FreibergAN

HolbrookMR

DaveyRA

2008 Phosphoinositide-3 kinase-Akt pathway controls cellular entry of Ebola virus. PLoS Pathog 4 e1000141

94. OgdenCA

deCathelineauA

HoffmannPR

BrattonD

GhebrehiwetB

2001 C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 194 781 795

95. JackDL

LeeME

TurnerMW

KleinNJ

ReadRC

2005 Mannose-binding lectin enhances phagocytosis and killing of Neisseria meningitidis by human macrophages. J Leukoc Biol 77 328 336

96. QuinnK

BrindleyMA

WellerML

KaludovN

KondratowiczA

2009 Rho GTPases modulate entry of Ebola virus and vesicular stomatitis virus pseudotyped vectors. J Virol 83 10176 10186

97. SinnPL

HickeyMA

StaberPD

DyllaDE

JeffersSA

2003 Lentivirus vectors pseudotyped with filoviral envelope glycoproteins transduce airway epithelia from the apical surface independently of folate receptor alpha. J Virol 77 5902 5910

98. GrimmerS

van DeursB

SandvigK

2002 Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 115 2953 2962

99. KennedyG

SugdenB

2003 EBNA-1, a bifunctional transcriptional activator. Mol Cell Biol 23 6901 6908

100. WeissenhornW

2004 Structure of Viral Protein.

Klenk HDFH

Ebola and Marburg Viruses; molecular and cellular biology Norfolk Horizon Bioscience 27 57

101. Neumann GNT

TakadaA

JasenoskyLD

KawaokaY

2004 Roles of Filoviral Matrix- and Glycoproteins in the Viral life Cycle.

KHaFH

Ebola and Marburg Viruses; molecular and cellular biology Norfolk Horizon Bioscience 230 203

102. ImaiM

SugimotoK

OkazakiK

KidaH

1998 Fusion of influenza virus with the endosomal membrane is inhibited by monoclonal antibodies to defined epitopes on the hemagglutinin. Virus Res 53 129 139

103. MoskowitzHS

YokoyamaCT

RyanTA

2005 Highly cooperative control of endocytosis by clathrin. Mol Biol Cell 16 1769 1776

104. ManninenA

VerkadeP

Le LayS

TorkkoJ

KasperM

2005 Caveolin-1 is not essential for biosynthetic apical membrane transport. Mol Cell Biol 25 10087 10096

105. WilkinsonS

PatersonHF

MarshallCJ

2005 Cdc42-MRCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat Cell Biol 7 255 261

106. ManavathiB

RayalaSK

KumarR

2007 Phosphorylation-dependent regulation of stability and transforming potential of ETS transcriptional factor ESE-1 by p21-activated kinase 1. J Biol Chem 282 19820 19830