Cell Communication and Signaling

Table 1 Mechanisms used by several virus types to release from the host cells

From: Exosomal transmission of viruses, a two-edged biological sword

Type of virus	Family	Intracellular transfer	Hijacking mechanism	Releasing mechanisms	Reference
Enveloped DNA viruses
Epstein-Barr Virus	Herpesviridae	ESCRT-dependent and ESCRT-independent pathways	TSG101, CD63, Syntenin‑1, Alix, and lipid rafts	Late endosomes	[195, 196, 238]
Kaposi's sarcoma-associated herpesvirus	Herpesviridae	ESCRT-dependent and ESCRT-independent pathways	Viral LMP1	Late endosomes	[182, 239]
Human Herpes virus-6	Herpesviridae	ESCRT-independent pathway	CD63 and viral gB	Late endosomes	[172]
Human Cytomegalovirus	Herpesviridae	ESCRT-independent, Vamp3-dependent pathways	VAMP3, viral pUL71 and UL99	Late endosomes	[197, 240]
Herpes simplex virus 1	Herpesviridae	ESCRT-dependent pathway	ESCRT-III	Microvesicular budding, Autophagosome-mediated exit without lysis, Late endosomes	[241, 242]
Non-enveloped DNA viruses
Adenoviruses 2 and 5	Adenoviridae	ESCRT-independent pathway	Exosomal CD46, Lamp2c	Late endosomes, Microvesicular budding	[181, 243, 244]
Hepatitis B virus	Hepadnavirideae	ESCRT-dependent pathway	α-taxilin, viral LHBs, TSG101, 2-adaptin, Nedd4	Late endosomes, Microvesicular budding	[245]
Enveloped RNA viruses
Japanese encephalitis virus	Flaviviridae	ESCRT-dependent pathway	viral NS3, TSG101	Late endosomes	[246, 247]
Yellow fever virus	Flaviviridae	ESCRT-dependent pathway	Viral NS3 protein, Alix	Late endosomes	[248, 249]
Dengue virus	Flaviviridae	ESCRT-dependent pathway	Viral NS3, Alix, viral protein E, Tsp29Fb	Late endosomes	[186, 187, 249, 250]
West Nile virus	Flaviviridae	ESCRT-dependent pathway	Viral NS3, Alix and ESCRT	Late endosomes	[249]
Zika virus	Flaviviridae	ESCRT-dependent pathway	Viral NS3 protein interacts with Alix	Late endosomes	[249, 251]
Tick-borne encephalitis	Flaviviridae	ESCRT-dependent pathway	ND	Late endosomes	[249]
Hepatitis C Virus	Flaviviridae	ESCRT-dependent pathway	Viral NS2 and NS5A proteins, Ago2, HSP90, and CD81	Late endosomes	[252,253,254]
Human immunodeficiency virus-1	Retroviridiae	ESCRT-dependent pathway	Viral Nef, Alix, viral Gag, and Syntenin	Late endosomes	[161, 191, 255, 256]
Equine Infectious Anemia Virus	Retroviridiae	ESCRT-dependent pathway	Viral Gag, Alix	Late endosomes TGN is the assembly site	[257]
Feline immunodeficiency virus	Retroviridiae	ESCRT-dependent pathway	Viral Gag, and Alix	Microvesicular budding	[258, 259]
Human immunodeficiency virus-2	Retroviridiae	ESCRT-dependent pathway	Viral Nef, Alix and viral Gag, and TSG-101	Late endosomes, Microvesicular budding	[260, 261]
Mouse Mammary Tumor Virus	Retroviridiae	ESCRT-dependent pathway	Viral Gag and NEDD4	ND	[262]
Murine Leukemia Virus	Retroviridiae	ESCRT-dependent pathway	Viral Gag and WWP1	Late endosomes, Microvesicular budding	[260, 263, 264]
Porcine endogenous retrovirus	Retroviridiae	ESCRT-dependent pathway	Viral Gag, and WWP2	Late endosomes	[265]
Prototypic foamy viruses	Retroviridiae	ESCRT-dependent pathway	Viral Gag, TSG-101, and PPPI	Late endosomes, Microvesicular budding, trans-Golgi network	[266, 267]
Mason–Pfizer monkey virus	Retroviridiae	ESCRT-dependent pathway	Viral Gag, TSG-101 and NEDD4	Microvesicular budding	[268, 269]
Human T cell leukemia virus type 1	Retroviridiae	ESCRT-dependent pathway	Viral Gag, TSG-101 and NEDD4	Late endosomes	[260, 270]
Human endogenous retrovirus-K	Retroviridiae	ESCRT-dependent pathway	Viral Gag, TSG-101	Late endosomes	[271, 272]
Rous sarcoma virus	Retroviridiae	ESCRT-dependent pathway	Gag, NEDD4 and Alix	Late endosomes	[273, 274]
Respiratory syncytial virus	Pneumoviridae	ESCRT-independent pathway	ND	Late endosomes	[46]
Human Pegivirus, GB virus C	Flaviviridae	ESCRT-dependent pathway	hnRNPA2B1 protein	Late endosomes	[275, 276]
Ebola virus	Flaviviridae	ESCRT-dependent pathway	Viral VP40, TSG-101, NEDD4, and VP24	Late endosomes, Microvesicular budding	[277, 278]
Marburg virus	Flaviviridae	ESCRT-dependent pathway	TSG-101, Viral VP40 and NEDD4	Microvesicular budding	[279,280,281]
Lassa fever virus	Arenaviridae	ESCRT-dependent pathway	Z protein and TSG-101	Microvesicular budding	[282, 283]
Rabies Virus	Rhabdoviridae	ESCRT-dependent pathway	Viral M protein, ESCRTI, Alix, ESCRT III and VPS4	Microvesicular budding	[284, 285]
Vesicular stomatitis virus	Rhabdoviridae	ESCRT-dependent pathway	Viral M protein, TSG-101, and NEDD4	Microvesicular budding	[286]
Parainfluenza virus 5	Paramyxoviridae	ESCRT-dependent pathway	Viral M protein, and VPS4 ATPase	Microvesicular budding	[287]
Parainfluenza virus 3	Paramyxoviridae	ESCRT-dependent pathway	Viral M protein	Microvesicular budding	[288]
Newcastle disease	Paramyxoviridae	ESCRT-dependent pathway	Viral M protein and VPS4 ATPase	Microvesicular budding	[289]
Mumps virus	Paramyxoviridae	ESCRT-dependent pathway	Viral M protein and VPS4 ATPase	Microvesicular budding	[290]
Hepatitis E virus	Hepeviridae	ESCRT-dependent pathway	Viral pORF3, and TSG-101	Late endosomes	[291, 292]
Non-enveloped RNA viruses
Hepatitis A virus	Picornaviridae	ESCRT-dependent pathway	Viral VP2, Alix and VPS4B	Late endosomes	[166, 293]
Coxsackievirus B	Picornaviridae	ESCRT-dependent pathway	LC3	Microvesicular budding, Autophagosome-mediated exit without lysis and	[294]
Poliovirus	Picornaviridae	ESCRT-dependent and independent pathways	Alix	Microvesicular budding, Autophagosome-mediated exit without lysis and	[165]
Enterovirus 71	Picornaviridae	ESCRT-dependent pathway	ND	Late endosomes	[295,296,297]
Reovirus	Reoviridae	ESCRT-dependent pathway	Rab5, Viral capsid protein P2	Late endosomes, modified lysosomal organelle act as transporter virions to the plasma membrane	[184, 298]
Rotavirus	Reoviridae	Probably ESCRT-dependent pathway	Probably VP4 interacts with lipid Rafts	Microvesicular budding	[150]
Norovirus	Caliciviridae	Probably ESCRT-dependent pathway	Viral VP1, Phosphatidylserine lipid	Late endosomes	[174]

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