Influenza virus assembly and budding.
Influenza A virus causes seasonal epidemics, sporadic pandemics and is a significant global health burden. Influenza virus is an enveloped virus that contains a segmented negative strand RNA genome. Assembly and budding of progeny influenza virions is a complex, multi-step process that occurs in lipid raft domains on the apical membrane of infected cells. The viral proteins hemagglutinin (HA) and neuraminidase (NA) are targeted to lipid rafts, causing the coalescence and enlargement of the raft domains. This clustering of HA and NA may cause a deformation of the membrane and the initiation of the virus budding event. M1 is then thought to bind to the cytoplasmic tails of HA and NA where it can then polymerize and form the interior structure of the emerging virion. M1, bound to the cytoplasmic tails of HA and NA, additionally serves as a docking site for the recruitment of the viral RNPs and may mediate the recruitment of M2 to the site of virus budding. M2 initially stabilizes the site of budding, possibly enabling the polymerization of the matrix protein and the formation of filamentous virions. Subsequently, M2 is able to alter membrane curvature at the neck of the budding virus, causing membrane scission and the release of the progeny virion. This review investigates the latest research on influenza virus budding in an attempt to provide a step-by-step analysis of the assembly and budding processes for influenza viruses.
Department of Molecular Biosciences, Northwestern University, Evanston, IL 60208-3500, USA.
Jeremy S
JS
Rossman
Robert A
RA
Lamb
D006389:Hemagglutinins, Viral / Q000378:metabolism; D006801:Humans; D009980:Influenza A virus / Q000502:physiology*; D009439:Neuraminidase / Q000378:metabolism; D019590:Nucleocapsid Proteins; D055503:Protein Multimerization; D016601:RNA-Binding Proteins / Q000378:metabolism; D014758:Viral Core Proteins / Q000378:metabolism; D014763:Viral Matrix Proteins / Q000378:metabolism; D014764:Viral Proteins / Q000378:metabolism; D019065:Virus Assembly; D057074:Virus Release; D000086082:Viroporin Proteins
D006389:Hemagglutinins, Viral; D009439:Neuraminidase; D019590:Nucleocapsid Proteins; D016601:RNA-Binding Proteins; D014758:Viral Core Proteins; D014763:Viral Matrix Proteins; D014764:Viral Proteins; C488936:M1 protein, Influenza A virus; C488937:M2 protein, Influenza A virus; D000086082:Viroporin Proteins; C048842:NP protein, Influenza A virus; C458881:hemagglutinin fusogenic peptide, influenza virus; C487630:NA protein, influenza A virus
J Gen Virol. 2010 Sep;91(Pt 9):2322-30
20505010
Biochem Soc Trans. 2009 Feb;37(Pt 1):195-9
19143630
Cell. 1992 Feb 7;68(3):533-44
1531449
J Virol. 1986 Dec;60(3):994-1001
3783822
Virus Res. 2004 Feb;99(2):115-9
14749176
Nature. 2008 Jan 31;451(7178):591-5
18235503
J Gen Virol. 2005 May;86(Pt 5):1447-1454
15831957
J Virol. 2007 Jul;81(13):7111-23
17475660
J Gen Virol. 2003 Mar;84(Pt 3):517-527
12604801
Virology. 1998 Jan 5;240(1):127-37
9448697
J Virol. 2002 Oct;76(20):10455-64
12239322
J Virol. 2001 Jul;75(13):6154-65
11390617
J Virol. 2010 May;84(10):5078-88
20219914
J Exp Med. 1956 Aug 1;104(2):171-82
13345962
Nature. 2000 Apr 27;404(6781):945, 947
10801110
FEBS Lett. 2007 May 22;581(11):2089-97
17434167
Nature. 2009 Jun 18;459(7249):931-9
19525932
J Virol. 2000 Dec;74(24):11538-47
11090151
J Virol. 2005 Jan;79(2):1262-70
15613353
Proc Natl Acad Sci U S A. 1989 Feb;86(3):1061-5
2915973
Biochem J. 2008 Sep 1;414(2):e1-2
18687059
Nature. 2009 Aug 20;460(7258):1021-5
19672242
Virology. 1963 Nov;21:342-52
14081358
Virology. 1961 Apr;13:548-50
13693269
J Virol. 2010 May;84(9):4673-81
20181696
Virology. 1995 Oct 1;212(2):411-21
7571410
J Virol. 2000 May;74(10):4634-44
10775599
PLoS Pathog. 2010 Sep 23;6(9):e1001121
20886108
Arch Biochem Biophys. 2009 Jun 15;486(2):150-4
19514132
Nature. 1992 Jul 9;358(6382):110-1
1377366
Virus Res. 2010 Oct;153(1):58-63
20621136
J Gen Virol. 1991 Jun;72 ( Pt 6):1301-8
1710647
J Biol Chem. 2006 Apr 7;281(14):8997-9000
16407184
Biochemistry. 2008 Sep 23;47(38):9934-6
18754675
J Gen Virol. 2007 Aug;88(Pt 8):2280-2290
17622633
Virology. 1996 Nov 15;225(2):255-66
8918911
Arch Gesamte Virusforsch. 1957;7(5):413-28
13521957
Nat Struct Mol Biol. 2004 Jun;11(6):567-73
15122347
Proc Natl Acad Sci U S A. 1997 Oct 14;94(21):11301-6
9326604
Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15143-8
14630951
J Exp Med. 1960 Nov 1;112:945-52
13693270
J Virol. 1988 Aug;62(8):2762-72
2455818
J Virol. 2010 Sep;84(17):8765-76
20573832
Nature. 2009 Mar 12;458(7235):172-7
19234443
Virology. 2000 Apr 10;269(2):325-34
10753711
J Virol. 2000 Sep;74(18):8709-19
10954572
J Virol. 2006 Aug;80(16):8178-89
16873274
Traffic. 2002 Oct;3(10):705-9
12230468
EMBO J. 1997 Sep 15;16(18):5501-8
9312009
Virology. 2009 Aug 1;390(2):268-78
19524996
PLoS Pathog. 2010 Sep 09;6(9):e1001099
20844577
Virology. 1991 Jul;183(1):32-43
2053285
Jpn J Infect Dis. 2010 Jan;63(1):67-71
20093768
Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):7827-30
10393906
Biopolymers. 1995;37(5):319-38
7632881
Eur Biophys J. 2005 Feb;34(1):52-66
15221235
J Virol. 2003 Jun;77(12):7078-92
12768027
Nature. 2010 Apr 8;464(7290):864-9
20305637
J Gen Microbiol. 1958 Aug;19(1):23-39
13575751
Curr Biol. 2009 Jan 27;19(2):95-107
19150238
J Virol. 1992 Sep;66(9):5542-52
1501289
Arch Virol. 2005 Sep;150(9):1783-96
15959836
J Virol. 2009 Jun;83(12):6257-68
19357161
Adv Virus Res. 2005;64:383-416
16139601
Nat Struct Biol. 1997 Mar;4(3):239-44
9164466
Virology. 2001 Oct 10;289(1):34-44
11601915
Cell. 1992 May 1;69(3):517-28
1374685
J Virol. 2007 Nov;81(22):12169-78
17855515
J Virol. 2004 May;78(10):5258-69
15113907
J Gen Virol. 1994 Jan;75 ( Pt 1):37-42
8113738
Int J Biochem Cell Biol. 2007;39(10):1765-70
17276129
PLoS Pathog. 2008 Nov;4(11):e1000209
19023411
Cell Host Microbe. 2007 Aug 16;2(2):96-105
18005724
Cell. 1985 Mar;40(3):627-33
3882238
Virology. 2001 Jan 20;279(2):439-46
11162800
Virus Res. 2009 Aug;143(2):147-61
19481124
Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9
11413487
Cell. 2010 Sep 17;142(6):902-13
20850012
J Virol. 2008 Oct;82(20):10059-70
18701586
EMBO J. 1997 Mar 17;16(6):1236-47
9135140
J Virol. 2005 Mar;79(6):3595-605
15731254
Virology. 2010 Sep 30;405(2):530-8
20655564
Cell. 1992 May 15;69(4):577-8
1375129
J Virol. 2000 Aug;74(16):7250-60
10906179
Lancet. 1949 Apr 9;1(6554):602
18124993
Virology. 1991 Feb;180(2):617-24
1989386
J Virol. 1985 Nov;56(2):502-11
3840537
Nature. 2006 Jan 26;439(7075):490-2
16437116
Science. 2010 Jan 1;327(5961):46-50
20044567
Virology. 2008 Mar 15;372(2):221-32
18063004
Virology. 2005 Nov 25;342(2):215-27
16249012
PLoS Pathog. 2010 Sep 16;6(9):e1001110
20862315
J Virol. 2006 Mar;80(5):2291-308
16474136
Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):10209-14
18621683
Protein Sci. 2003 Nov;12(11):2597-605
14573870
J Exp Med. 1960 Mar 1;111:387-406
13755924
J Virol. 2010 Dec;84(23):12445-9
20881046
J Virol. 2006 Jun;80(11):5233-40
16699003
Nature. 1981 Oct 22;293(5834):620-5
6270568
J Virol. 2010 Jun;84(12):5848-59
20357086
Virology. 2004 Mar 30;321(1):144-53
15033573
Proc Natl Acad Sci U S A. 2010 Jun 8;107(23):10685-90
20498070
J Virol. 1996 Dec;70(12):8391-401
8970960
Virol J. 2010 May 26;7:108
20504340
Histol Histopathol. 2009 Sep;24(9):1171-80
19609864
Nature. 1997 Jun 5;387(6633):569-72
9177342
Nucleic Acids Res. 1989 Nov 11;17(21):8569-80
2479906
JAMA. 2003 Jan 8;289(2):179-86
12517228
Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14610-7
14561897
Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11263-8
15280537
J Virol. 2005 Nov;79(21):13673-84
16227287