The C-termini of the baculovirus per os infectivity factors 1 and 2 mediate ODV oral infectivity by facilitating the binding of PIF0 and PIF8 to the core of the entry complex
Oral infection of caterpillars by baculoviruses is initiated by occlusion-derived virus particles (ODVs) that infect midgut epithelium cells. The ODV envelope therefore contains at least ten different proteins, which are called per os infectivity factors (PIFs). Nine of these PIFs form the so-called ODV entry complex that consists of a stable core formed by PIF1, 2, 3 and 4, to which the other PIFs [PIF0, 6, 7, 8 and 9 (ac108)] bind with lower affinity. PIF1 and 2 are not only essential for complex formation, but also mediate ODV-binding to the epithelial brush border, probably via the C-termini. To study the involvement of these PIFs during midgut infection in greater detail, we assessed the oral infectivity and the ability to form the complex of a series of PIF1 and PIF2 C-terminal truncation mutants of Autographa californica multiple nucleopolyhedrovirus (AcMNPV), which were constructed in this study. Limited truncation of either PIF1 or 2 already severely impaired the ODV oral infectivity, but did not affect the formation of the core complex. However, the entry complex as a whole was not assembled in these mutants as PIF0 and 8 failed to bind to the core. This suggests that the interactions between the core and the loosely associated PIFs are important for the ODV infectivity and that complex formation complicates the determination of the exact roles of PIF1 and 2 during midgut infection. We also showed that the presence of PIF0, 6 and the ZF-domain of PIF8 are crucial for complex formation.
FaulknerP,
KuzioJ,
WilliamsGV,
WilsonJA.
Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo
. J Gen Virol1997; 78 (Pt 12:3091–3100 [View Article][PubMed]
KikhnoI,
GutiérrezS,
CroizierL,
CroizierG,
FerberML.
Characterization of pif, a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol2002; 83:3013–3022 [View Article][PubMed]
PijlmanGP,
PruijssersAJP,
VlakJM.
Identification of pif-2, a third conserved baculovirus gene required for per os infection of insects. J Gen Virol2003; 84:2041–2049 [View Article][PubMed]
OhkawaT,
WashburnJO,
SitaparaR,
SidE,
VolkmanLE.
Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of PIF genes Ac119 and Ac022 but not by Ac115. J Virol2005; 79:15258–15264 [View Article][PubMed]
SparksWO,
HarrisonRL,
BonningBC.
Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. Virology2011; 409:69–76 [View Article][PubMed]
NieY,
FangM,
ErlandsonMA,
TheilmannDA.
Analysis of the Autographa californica multiple nucleopolyhedrovirus overlapping gene pair lef3 and ac68 reveals that AC68 is a per os infectivity factor and that LEF3 is critical, but not essential, for virus replication. J Virol2012; 86:3985–3994 [View Article][PubMed]
ZhuS,
WangW,
WangY,
YuanM,
YangK.
The baculovirus core gene ac83 is required for nucleocapsid assembly and per os infectivity of Autographa californica nucleopolyhedrovirus. J Virol2013; 87:10573–10586 [View Article][PubMed]
JavedMA,
BiswasS,
WillisLG,
HarrisS,
PritchardC et al. Acmnpv AC83 is a PIF protein required for ODV and bv nucleocapsid assembly as well as assembly of the PIF complex in ODV envelopes. J Virol2016; 91:02115–02116
LiuJ,
ZhuL,
ZhangS,
DengZ,
HuangZ et al. The Autographa californica multiple nucleopolyhedrovirus ac110 gene encodes a new per os infectivity factor. Virus Res2016; 221:30–37 [View Article][PubMed]
BoogaardB,
EversF,
van LentJWM,
van OersMM.
The baculovirus Ac108 protein is a per os infectivity factor and a component of the ODV entry complex. J Gen Virol2019; 100:669–678 [View Article][PubMed]
Haas-StapletonEJ,
WashburnJO,
VolkmanLE.
P74 mediates specific binding of Autographa californica Mnucleopolyhedrovirus occlusion-derived virus to primary cellular targets in the midgut epithelia of Heliothis virescens larvae. J Virol2004; 78:6786–6791 [View Article][PubMed]
MuJ,
van LentJWM,
SmaggheG,
WangY,
ChenX et al. Live imaging of baculovirus infection of midgut epithelium cells: a functional assay of per os infectivity factors. J Gen Virol2014; 95:2531–2539 [View Article][PubMed]
PengK,
van OersMM,
HuZ,
van LentJWM,
VlakJM.
Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. J Virol2010; 84:9497–9504 [View Article][PubMed]
PengK,
van LentJWM,
BoerenS,
FangM,
TheilmannDA et al. Characterization of novel components of the baculovirus per os infectivity factor complex. J Virol2012; 86:4981–4988 [View Article][PubMed]
BoogaardB,
van LentJWM,
TheilmannDA,
ErlandsonMA,
van OersMM.
Baculoviruses require an intact ODV entry-complex to resist proteolytic degradation of per os infectivity factors by co-occluded proteases from the larval host. J Gen Virol2017; 98:3101–3110 [View Article][PubMed]
Haas-StapletonEJ,
WashburnJO,
VolkmanLE.
Spodoptera frugiperda resistance to oral infection by Autographa californica multiple nucleopolyhedrovirus linked to aberrant occlusion-derived virus binding in the midgut. J Gen Virol2005; 86:1349–1355 [View Article][PubMed]
PengK,
WuM,
DengF,
SongJ,
DongC et al. Identification of protein-protein interactions of the occlusion-derived virus-associated proteins of Helicoverpa armigera nucleopolyhedrovirus. J Gen Virol2010; 91:659–670 [View Article][PubMed]
ZhengQ,
ShenY,
KonX,
ZhangJ,
FengM et al. Protein-protein interactions of the baculovirus per os infectivity factors (PIFs) in the PIF complex. J Gen Virol2017; 98:853–861 [View Article][PubMed]
DongZ-Q,
ZhangJ,
ChenX-M,
HeQ,
CaoM-Y et al. Bombyx mori nucleopolyhedrovirus ORF79 is a per os infectivity factor associated with the PIF complex. Virus Res2014; 184:62–70 [View Article][PubMed]
SongJ,
WangR,
DengF,
WangH,
HuZ.
Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol2008; 89:2331–2338 [View Article][PubMed]
HarrisonRL,
SparksWO,
BonningBC.
Autographa californica multiple nucleopolyhedrovirus ODV-E56 envelope protein is required for oral infectivity and can be substituted functionally by Rachiplusia ou multiple nucleopolyhedrovirus ODV-E56. J Gen Virol2010; 91:1173–1182 [View Article][PubMed]
SparksWO,
RohlfingA,
BonningBC.
A peptide with similarity to baculovirus ODV-E66 binds the gut epithelium of Heliothis virescens and impedes infection with Autographa californica multiple nucleopolyhedrovirus. J Gen Virol2011; 92:1051–1060 [View Article][PubMed]
LiS,
LiL,
ZhaoH,
LiuW.
Disruption of Autographa californica multiple nucleopolyhedrovirus ac111 results in reduced per os infectivity in a host-dependent manner. Viruses2018; 10:527 [View Article]
LapointeR,
PophamHJR,
StraschilU,
GouldingD,
O'ReillyDR et al. Characterization of two Autographa californica nucleopolyhedrovirus proteins, Ac145 and Ac150, which affect oral infectivity in a host-dependent manner. J Virol2004; 78:6439–6448 [View Article][PubMed]
ZhangJ-H,
OhkawaT,
WashburnJO,
VolkmanLE.
Effects of Ac150 on virulence and pathogenesis of Autographa californica multiple nucleopolyhedrovirus in noctuid hosts. J Gen Virol2005; 86:1619–1627 [View Article][PubMed]
The C-termini of the baculovirus per os infectivity factors 1 and 2 mediate ODV oral infectivity by facilitating the binding of PIF0 and PIF8 to the core of the entry complex