The Length of Vesicular Stomatitis Virus Particles Dictates a Need for Actin Assembly during Clathrin-Dependent Endocytosis
Microbial pathogens exploit the clathrin endocytic machinery to enter host cells. Vesicular stomatitis virus (VSV), an enveloped virus with bullet-shaped virions that measure 70×200 nm, enters cells by clathrin-dependent endocytosis. We showed previously that VSV particles exceed the capacity of typical clathrin-coated vesicles and instead enter through endocytic carriers that acquire a partial clathrin coat and require local actin filament assembly to complete vesicle budding and internalization. To understand why the actin system is required for VSV uptake, we compared the internalization mechanisms of VSV and its shorter (75 nm long) defective interfering particle, DI-T. By imaging the uptake of individual particles into live cells, we found that, as with parental virions, DI-T enters via the clathrin endocytic pathway. Unlike VSV, DI-T internalization occurs through complete clathrin-coated vesicles and does not require actin polymerization. Since VSV and DI-T particles display similar surface densities of the same attachment glycoprotein, we conclude that the physical properties of the particle dictate whether a virus-containing clathrin pit engages the actin system. We suggest that the elongated shape of a VSV particle prevents full enclosure by the clathrin coat and that stalling of coat assembly triggers recruitment of the actin machinery to finish the internalization process. Since some enveloped viruses have pleomorphic particle shapes and sizes, our work suggests that they may use altered modes of endocytic uptake. More generally, our findings show the importance of cargo geometry for specifying cellular entry modes, even when the receptor recognition properties of a ligand are maintained.
Vyšlo v časopise:
The Length of Vesicular Stomatitis Virus Particles Dictates a Need for Actin Assembly during Clathrin-Dependent Endocytosis. PLoS Pathog 6(9): e32767. doi:10.1371/journal.ppat.1001127
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1001127
Souhrn
Microbial pathogens exploit the clathrin endocytic machinery to enter host cells. Vesicular stomatitis virus (VSV), an enveloped virus with bullet-shaped virions that measure 70×200 nm, enters cells by clathrin-dependent endocytosis. We showed previously that VSV particles exceed the capacity of typical clathrin-coated vesicles and instead enter through endocytic carriers that acquire a partial clathrin coat and require local actin filament assembly to complete vesicle budding and internalization. To understand why the actin system is required for VSV uptake, we compared the internalization mechanisms of VSV and its shorter (75 nm long) defective interfering particle, DI-T. By imaging the uptake of individual particles into live cells, we found that, as with parental virions, DI-T enters via the clathrin endocytic pathway. Unlike VSV, DI-T internalization occurs through complete clathrin-coated vesicles and does not require actin polymerization. Since VSV and DI-T particles display similar surface densities of the same attachment glycoprotein, we conclude that the physical properties of the particle dictate whether a virus-containing clathrin pit engages the actin system. We suggest that the elongated shape of a VSV particle prevents full enclosure by the clathrin coat and that stalling of coat assembly triggers recruitment of the actin machinery to finish the internalization process. Since some enveloped viruses have pleomorphic particle shapes and sizes, our work suggests that they may use altered modes of endocytic uptake. More generally, our findings show the importance of cargo geometry for specifying cellular entry modes, even when the receptor recognition properties of a ligand are maintained.
Zdroje
1. ConnerSD
SchmidSL
2003 Regulated portals of entry into the cell. Nature 422 37 44
2. KirchhausenT
2000 Clathrin. Annu Rev Biochem 69 699 727
3. KirchhausenT
2009 Imaging endocytic clathrin structures in living cells. Trends Cell Biol 19 596 605
4. OwenDJ
EvansPR
1998 A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 282 1327 1332
5. HoningS
RicottaD
KraussM
SpateK
SpolaoreB
2005 Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol Cell 18 519 531
6. DamkeH
BabaT
WarnockDE
SchmidSL
1994 Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 127 915 934
7. LeeDW
ZhaoX
ZhangF
EisenbergE
GreeneLE
2005 Depletion of GAK/auxilin 2 inhibits receptor-mediated endocytosis and recruitment of both clathrin and clathrin adaptors. J Cell Sci 118 4311 4321
8. MassolRH
BollW
GriffinAM
KirchhausenT
2006 A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc Natl Acad Sci U S A 103 10265 10270
9. EhrlichM
BollW
Van OijenA
HariharanR
ChandranK
2004 Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118 591 605
10. LoerkeD
MettlenM
YararD
JaqamanK
JaqamanH
2009 Cargo and dynamin regulate clathrin-coated pit maturation. PLoS Biol 7 e57
11. HanoverJA
BeguinotL
WillinghamMC
PastanIH
1985 Transit of receptors for epidermal growth factor and transferrin through clathrin-coated pits. Analysis of the kinetics of receptor entry. J Biol Chem 260 15938 15945
12. AndersonRG
BrownMS
GoldsteinJL
1977 Role of the coated endocytic vesicle in the uptake of receptor-bound low density lipoprotein in human fibroblasts. Cell 10 351 364
13. van der SchaarHM
RustMJ
ChenC
van der Ende-MetselaarH
WilschutJ
2008 Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathog 4 e1000244
14. RustMJ
LakadamyaliM
ZhangF
ZhuangX
2004 Assembly of endocytic machinery around individual influenza viruses during viral entry. Nat Struct Mol Biol 11 567 573
15. CuretonDK
MassolRH
SaffarianS
KirchhausenTL
WhelanSP
2009 Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5 e1000394
16. VeigaE
GuttmanJA
BonazziM
BoucrotE
Toledo-AranaA
2007 Invasive and adherent bacterial pathogens co-Opt host clathrin for infection. Cell Host Microbe 2 340 351
17. SimpsonRW
HauserRE
DalesS
1969 Viropexis of vesicular stomatitis virus by L cells. Virology 37 285 290
18. HarrisA
CardoneG
WinklerDC
HeymannJB
BrecherM
2006 Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci U S A 103 19123 19127
19. MeierE
HarmisonGG
KeeneJD
SchubertM
1984 Sites of copy choice replication involved in generation of vesicular stomatitis virus defective-interfering particle RNAs. J Virol 51 515 521
20. HuangAS
WagnerRR
1966 Defective T particles of vesicular stomatitis virus. II. Biologic role in homologous interference. Virology 30 173 181
21. PengG
TsaoJ
ScheinS
GreenTJ
LuoM
2010 Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327 689 693
22. HuangAS
GreenawaltJW
WagnerRR
1966 Defective T particles of vesicular stomatitis virus. I. Preparation, morphology, and some biologic properties. Virology 30 161 172
23. WagnerRR
SchnaitmanTA
SnyderRM
1969 Structural proteins of vesicular stomatitis viruses. J Virol 3 395 403
24. PattnaikAK
BallLA
LeGroneAW
WertzGW
1992 Infectious defective interfering particles of VSV from transcripts of a cDNA clone. Cell 69 1011 1020
25. WhelanSP
BallLA
BarrJN
WertzGT
1995 Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci U S A 92 8388 8392
26. SaffarianS
CocucciE
KirchhausenT
2009 Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol 7 e1000191
27. UrunoT
LiuJ
ZhangP
FanY
EgileC
2001 Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat Cell Biol 3 259 266
28. McNivenMA
KimL
KruegerEW
OrthJD
CaoH
2000 Regulated interactions between dynamin and the actin-binding protein cortactin modulate cell shape. J Cell Biol 151 187 198
29. MerrifieldCJ
PerraisD
ZenisekD
2005 Coupling between clathrin-coated-pit invagination, cortactin recruitment, and membrane scission observed in live cells. Cell 121 593 606
30. CoueM
BrennerSL
SpectorI
KornED
1987 Inhibition of actin polymerization by latrunculin A. FEBS Lett 213 316 318
31. CoyneCB
BergelsonJM
2006 Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124 119 131
32. CoyneCB
KimKS
BergelsonJM
2007 Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. Embo J 26 4016 4028
33. KaksonenM
ToretCP
DrubinDG
2006 Harnessing actin dynamics for clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 7 404 414
34. KaksonenM
SunY
DrubinDG
2003 A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115 475 487
35. IdrissiFZ
GrotschH
Fernandez-GolbanoIM
Presciatto-BaschongC
RiezmanH
2008 Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. J Cell Biol 180 1219 1232
36. HeuserJ
1980 Three-dimensional visualization of coated vesicle formation in fibroblasts. J Cell Biol 84 560 583
37. GottliebTA
IvanovIE
AdesnikM
SabatiniDD
1993 Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120 695 710
38. Da CostaSR
SouE
XieJ
YarberFA
OkamotoCT
2003 Impairing actin filament or syndapin functions promotes accumulation of clathrin-coated vesicles at the apical plasma membrane of acinar epithelial cells. Mol Biol Cell 14 4397 4413
39. ShupliakovO
BloomO
GustafssonJS
KjaerulffO
LowP
2002 Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton. Proc Natl Acad Sci U S A 99 14476 14481
40. BourneJ
MorganJR
PieriboneVA
2006 Actin polymerization regulates clathrin coat maturation during early stages of synaptic vesicle recycling at lamprey synapses. J Comp Neurol 497 600 609
41. BoucrotE
SaffarianS
MassolR
KirchhausenT
EhrlichM
2006 Role of lipids and actin in the formation of clathrin-coated pits. Exp Cell Res 312 4036 4048
42. QualmannB
RoosJ
DiGregorioPJ
KellyRB
1999 Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell 10 501 513
43. SouletF
YararD
LeonardM
SchmidSL
2005 SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol Biol Cell 16 2058 2067
44. YararD
Waterman-StorerCM
SchmidSL
2007 SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev Cell 13 43 56
45. RingstadN
NemotoY
De CamilliP
1997 The SH3p4/Sh3p8/SH3p13 protein family: binding partners for synaptojanin and dynamin via a Grb2-like Src homology 3 domain. Proc Natl Acad Sci U S A 94 8569 8574
46. OtsukiM
ItohT
TakenawaT
2003 Neural Wiskott-Aldrich syndrome protein is recruited to rafts and associates with endophilin A in response to epidermal growth factor. J Biol Chem 278 6461 6469
47. DawsonJC
LeggJA
MacheskyLM
2006 Bar domain proteins: a role in tubulation, scission and actin assembly in clathrin-mediated endocytosis. Trends Cell Biol 16 493 498
48. RobertsPC
CompansRW
1998 Host cell dependence of viral morphology. Proc Natl Acad Sci U S A 95 5746 5751
49. RobertsPC
LambRA
CompansRW
1998 The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240 127 137
50. NeumanBW
AdairBD
BurnsJW
MilliganRA
BuchmeierMJ
2005 Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J Virol 79 3822 3830
51. MurphyFA
WebbPA
JohnsonKM
WhitfieldSG
ChappellWA
1970 Arenoviruses in Vero cells: ultrastructural studies. J Virol 6 507 518
52. RojekJM
SanchezAB
NguyenNT
de la TorreJC
KunzS
2008 Different mechanisms of cell entry by human-pathogenic Old World and New World arenaviruses. J Virol 82 7677 7687
53. ChandranK
SullivanNJ
FelborU
WhelanSP
CunninghamJM
2005 Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308 1643 1645
54. NegreteOA
LevroneyEL
AguilarHC
Bertolotti-CiarletA
NazarianR
2005 EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 436 401 405
55. ClementeR
de la TorreJC
2009 Cell entry of Borna disease virus follows a clathrin-mediated endocytosis pathway that requires Rab5 and microtubules. J Virol 83 10406 10416
56. BhattacharyyaS
WarfieldKL
RuthelG
BavariS
AmanMJ
2010 Ebola virus uses clathrin-mediated endocytosis as an entry pathway. Virology 401 18 28
57. Le ClaincheC
PaulyBS
ZhangCX
Engqvist-GoldsteinAE
CunninghamK
2007 A Hip1R-cortactin complex negatively regulates actin assembly associated with endocytosis. Embo J 26 1199 1210
58. KaksonenM
PengHB
RauvalaH
2000 Association of cortactin with dynamic actin in lamellipodia and on endosomal vesicles. J Cell Sci 113 Pt 24 4421 4426
59. MaupinP
PollardTD
1983 Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. J Cell Biol 96 51 62
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2010 Číslo 9
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- Structure of the Extracellular Portion of CD46 Provides Insights into Its Interactions with Complement Proteins and Pathogens
- The Length of Vesicular Stomatitis Virus Particles Dictates a Need for Actin Assembly during Clathrin-Dependent Endocytosis
- Inhibition of TIR Domain Signaling by TcpC: MyD88-Dependent and Independent Effects on Virulence
- Cellular Entry of Ebola Virus Involves Uptake by a Macropinocytosis-Like Mechanism and Subsequent Trafficking through Early and Late Endosomes