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Vesicular Transport of Progeny Parvovirus Particles through ER and Golgi Regulates Maturation and Cytolysis

DOI: 10.1371/journal.ppat.1003605

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Abstract:

Progeny particles of non-enveloped lytic parvoviruses were previously shown to be actively transported to the cell periphery through vesicles in a gelsolin-dependent manner. This process involves rearrangement and destruction of actin filaments, while microtubules become protected throughout the infection. Here the focus is on the intracellular egress pathway, as well as its impact on the properties and release of progeny virions. By colocalization with cellular marker proteins and specific modulation of the pathways through over-expression of variant effector genes transduced by recombinant adeno-associated virus vectors, we show that progeny PV particles become engulfed into COPII-vesicles in the endoplasmic reticulum (ER) and are transported through the Golgi to the plasma membrane. Besides known factors like sar1, sec24, rab1, the ERM family proteins, radixin and moesin play (an) essential role(s) in the formation/loading and targeting of virus-containing COPII-vesicles. These proteins also contribute to the transport through ER and Golgi of the well described analogue of cellular proteins, the secreted Gaussia luciferase in absence of virus infection. It is therefore likely that radixin and moesin also serve for a more general function in cellular exocytosis. Finally, parvovirus egress via ER and Golgi appears to be necessary for virions to gain full infectivity through post-assembly modifications (e.g. phosphorylation). While not being absolutely required for cytolysis and progeny virus release, vesicular transport of parvoviruses through ER and Golgi significantly accelerates these processes pointing to a regulatory role of this transport pathway.

 References

[1]  Mackenzie JM, Westaway EG (2001) Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J Virol 75: 10787–10799. doi: 10.1128/jvi.75.22.10787-10799.2001
[2]  Coller KE, Heaton NS, Berger KL, Cooper JD, Saunders JL, et al. (2012) Molecular determinants and dynamics of hepatitis C virus secretion. PLoS Pathog 8: e1002466. doi: 10.1371/journal.ppat.1002466
[3]  Mettenleiter TC (2002) Herpesvirus assembly and egress. J Virol 76: 1537–1547. doi: 10.1128/jvi.76.4.1537-1547.2002
[4]  Krijnse-Locker J, Ericsson M, Rottier PJ, Griffiths G (1994) Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. J Cell Biol 124: 55–70. doi: 10.1083/jcb.124.1.55
[5]  Tandon R, Mocarski ES (2012) Viral and host control of cytomegalovirus maturation. Trends Microbiol 20: 392–401. doi: 10.1016/j.tim.2012.04.008
[6]  Lambert C, Doring T, Prange R (2007) Hepatitis B virus maturation is sensitive to functional inhibition of ESCRT-III, Vps4, and gamma 2-adaptin. J Virol 81: 9050–9060. doi: 10.1128/jvi.00479-07
[7]  Rowe RK, Suszko JW, Pekosz A (2008) Roles for the recycling endosome, Rab8, and Rab11 in hantavirus release from epithelial cells. Virology 382: 239–249. doi: 10.1016/j.virol.2008.09.021
[8]  Salanueva IJ, Carrascosa JL, Risco C (1999) Structural maturation of the transmissible gastroenteritis coronavirus. J Virol 73: 7952–7964.
[9]  Salanueva IJ, Novoa RR, Cabezas P, Lopez-Iglesias C, Carrascosa JL, et al. (2003) Polymorphism and structural maturation of bunyamwera virus in Golgi and post-Golgi compartments. J Virol 77: 1368–1381. doi: 10.1128/jvi.77.2.1368-1381.2003
[10]  Lopez T, Camacho M, Zayas M, Najera R, Sanchez R, et al. (2005) Silencing the morphogenesis of rotavirus. J Virol 79: 184–192. doi: 10.1128/jvi.79.1.184-192.2005
[11]  Johnson DC, Baines JD (2011) Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9: 382–394. doi: 10.1038/nrmicro2559
[12]  Chen J, Lee KH, Steinhauer DA, Stevens DJ, Skehel JJ, et al. (1998) Structure of the hemagglutinin precursor cleavage site, a determinant of influenza pathogenicity and the origin of the labile conformation. Cell 95: 409–417. doi: 10.1016/s0092-8674(00)81771-7
[13]  Horimoto T, Nakayama K, Smeekens SP, Kawaoka Y (1994) Proprotein-processing endoproteases PC6 and furin both activate hemagglutinin of virulent avian influenza viruses. J Virol 68: 6074–6078.
[14]  Stein BS, Engleman EG (1990) Intracellular processing of the gp160 HIV-1 envelope precursor. Endoproteolytic cleavage occurs in a cis or medial compartment of the Golgi complex. J Biol Chem 265: 2640–2649.
[15]  Tattersall P (1972) Replication of the parvovirus MVM. I. Dependence of virus multiplication and plaque formation on cell growth. J Virol 10: 586–590.
[16]  Cotmore SF, Tattersall P (1987) The autonomously replicating parvoviruses of vertebrates. Adv Virus Res 33: 91–174. doi: 10.1016/s0065-3527(08)60317-6
[17]  Daeffler L, Horlein R, Rommelaere J, Nuesch JP (2003) Modulation of minute virus of mice cytotoxic activities through site-directed mutagenesis within the NS coding region. J Virol 77: 12466–12478. doi: 10.1128/jvi.77.23.12466-12478.2003
[18]  Clayson ET, Brando LV, Compans RW (1989) Release of simian virus 40 virions from epithelial cells is polarized and occurs without cell lysis. J Virol 63: 2278–2288.
[19]  Inal JM, Jorfi S (2013) Coxsackievirus B transmission and possible new roles for extracellular vesicles. Biochem Soc Trans 41: 299–302. doi: 10.1042/bst20120272
[20]  Bar S, Daeffler L, Rommelaere J, Nuesch JP (2008) Vesicular egress of non-enveloped lytic parvoviruses depends on gelsolin functioning. PLoS Pathog 4: e1000126. doi: 10.1371/journal.ppat.1000126
[21]  Pfeffer S, Aivazian D (2004) Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 5: 886–896. doi: 10.1038/nrm1500
[22]  Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91: 119–149. doi: 10.1152/physrev.00059.2009
[23]  Wendeler MW, Paccaud JP, Hauri HP (2007) Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep 8: 258–264. doi: 10.1038/sj.embor.7400893
[24]  Bonifacino JS, Glick BS (2004) The mechanisms of vesicle budding and fusion. Cell 116: 153–166. doi: 10.1016/s0092-8674(03)01079-1
[25]  Kuehn MJ, Herrmann JM, Schekman R (1998) COPII-cargo interactions direct protein sorting into ER-derived transport vesicles. Nature 391: 187–190.
[26]  Dancourt J, Barlowe C (2010) Protein sorting receptors in the early secretory pathway. Annu Rev Biochem 79: 777–802. doi: 10.1146/annurev-biochem-061608-091319
[27]  Yang Z, Li H, Chai Z, Fullerton MJ, Cao Y, et al. (2001) Dynamin II regulates hormone secretion in neuroendocrine cells. J Biol Chem 276: 4251–4260. doi: 10.1074/jbc.m006371200
[28]  Anitei M, Hoflack B (2012) Bridging membrane and cytoskeleton dynamics in the secretory and endocytic pathways. Nat Cell Biol 14: 11–19. doi: 10.1038/ncb2409
[29]  Fromme JC, Orci L, Schekman R (2008) Coordination of COPII vesicle trafficking by Sec23. Trends Cell Biol 18: 330–336. doi: 10.1016/j.tcb.2008.04.006
[30]  Gurkan C, Stagg SM, Lapointe P, Balch WE (2006) The COPII cage: unifying principles of vesicle coat assembly. Nat Rev Mol Cell Biol 7: 727–738. doi: 10.1038/nrm2025
[31]  Schmoranzer J, Goulian M, Axelrod D, Simon SM (2000) Imaging constitutive exocytosis with total internal reflection fluorescence microscopy. J Cell Biol 149: 23–32. doi: 10.1083/jcb.149.1.23
[32]  Toomre D, Steyer JA, Keller P, Almers W, Simons K (2000) Fusion of constitutive membrane traffic with the cell surface observed by evanescent wave microscopy. J Cell Biol 149: 33–40. doi: 10.1083/jcb.149.1.33
[33]  Nuesch JP, Lachmann S, Rommelaere J (2005) Selective alterations of the host cell architecture upon infection with parvovirus minute virus of mice. Virology 331: 159–174. doi: 10.1016/j.virol.2004.10.019
[34]  Nuesch JP, Lacroix J, Marchini A, Rommelaere J (2012) Molecular pathways: rodent parvoviruses–mechanisms of oncolysis and prospects for clinical cancer treatment. Clin Cancer Res 18: 3516–3523. doi: 10.1158/1078-0432.ccr-11-2325
[35]  Nuesch JP (2006) Regulation of non-structural protein functions by differential synthesis, modifications and trafficking. In: Kerr JR CS, Bloom ME, Linden RM, Parrish CR editor. Parvoviruses. London: Edward Arnold Ltd. pp. 275–290.
[36]  Nuesch JP, Rommelaere J (2006) NS1 interaction with CKII alpha: novel protein complex mediating parvovirus-induced cytotoxicity. J Virol 80: 4729–4739. doi: 10.1128/jvi.80.10.4729-4739.2006
[37]  Nuesch JP, Rommelaere J (2007) A viral adaptor protein modulating casein kinase II activity induces cytopathic effects in permissive cells. Proc Natl Acad Sci U S A 104: 12482–12487. doi: 10.1073/pnas.0705533104
[38]  Nuesch JP, Bar S, Lachmann S, Rommelaere J (2009) Ezrin-radixin-moesin family proteins are involved in parvovirus replication and spreading. J Virol 83: 5854–5863. doi: 10.1128/jvi.00039-09
[39]  Lachmann S, Bar S, Rommelaere J, Nuesch JP (2008) Parvovirus interference with intracellular signalling: mechanism of PKCeta activation in MVM-infected A9 fibroblasts. Cell Microbiol 10: 755–769. doi: 10.1111/j.1462-5822.2007.01082.x
[40]  Tsukita S, Yonemura S (1997) ERM proteins: head-to-tail regulation of actin-plasma membrane interaction. Trends Biochem Sci 22: 53–58. doi: 10.1016/s0968-0004(96)10071-2
[41]  Di Piazza M, Mader C, Geletneky K, Herrero YCM, Weber E, et al. (2007) Cytosolic activation of cathepsins mediates parvovirus H-1-induced killing of cisplatin and TRAIL-resistant glioma cells. J Virol 81: 4186–4198. doi: 10.1128/jvi.02601-06
[42]  Nuoffer C, Davidson HW, Matteson J, Meinkoth J, Balch WE (1994) A GDP-bound of rab1 inhibits protein export from the endoplasmic reticulum and transport between Golgi compartments. J Cell Biol 125: 225–237. doi: 10.1083/jcb.125.2.225
[43]  Moritz OL, Tam BM, Hurd LL, Peranen J, Deretic D, et al. (2001) Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol Biol Cell 12: 2341–2351. doi: 10.1091/mbc.12.8.2341
[44]  Chen W, Feng Y, Chen D, Wandinger-Ness A (1998) Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9: 3241–3257. doi: 10.1091/mbc.9.11.3241
[45]  Badr CE, Hewett JW, Breakefield XO, Tannous BA (2007) A highly sensitive assay for monitoring the secretory pathway and ER stress. PLoS One 2: e571. doi: 10.1371/journal.pone.0000571
[46]  Barroso-Gonzalez J, Machado JD, Garcia-Exposito L, Valenzuela-Fernandez A (2009) Moesin regulates the trafficking of nascent clathrin-coated vesicles. J Biol Chem 284: 2419–2434. doi: 10.1074/jbc.m805311200
[47]  Krieg J, Hunter T (1992) Identification of the two major epidermal growth factor-induced tyrosine phosphorylation sites in the microvillar core protein ezrin. J Biol Chem 267: 19258–19265.
[48]  Kestler J, Neeb B, Struyf S, Van Damme J, Cotmore SF, et al. (1999) cis requirements for the efficient production of recombinant DNA vectors based on autonomous parvoviruses. Hum Gene Ther 10: 1619–1632. doi: 10.1089/10430349950017626
[49]  Corbau R, Salom N, Rommelaere J, Nuesch JP (1999) Phosphorylation of the viral nonstructural protein NS1 during MVMp infection of A9 cells. Virology 259: 402–415. doi: 10.1006/viro.1999.9786
[50]  Zhong L, Li B, Jayandharan G, Mah CS, Govindasamy L, et al. (2008) Tyrosine-phosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology 381: 194–202. doi: 10.1016/j.virol.2008.08.027
[51]  Richards AL, Jackson WT (2012) Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog 8: e1003046. doi: 10.1371/journal.ppat.1003046
[52]  Pornillos O, Alam SL, Rich RL, Myszka DG, Davis DR, et al. (2002) Structure and functional interactions of the Tsg101 UEV domain. EMBO J 21: 2397–2406. doi: 10.1093/emboj/21.10.2397
[53]  Pornillos O, Higginson DS, Stray KM, Fisher RD, Garrus JE, et al. (2003) HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J Cell Biol 162: 425–434. doi: 10.1083/jcb.200302138
[54]  Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, et al. (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55–65. doi: 10.1016/s0092-8674(01)00506-2
[55]  Katzmann DJ, Babst M, Emr SD (2001) Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106: 145–155. doi: 10.1016/s0092-8674(01)00434-2
[56]  Morita E, Sundquist WI (2004) Retrovirus budding. Annu Rev Cell Dev Biol 20: 395–425. doi: 10.1146/annurev.cellbio.20.010403.102350
[57]  Demirov DG, Freed EO (2004) Retrovirus budding. Virus Res 106: 87–102. doi: 10.1016/j.virusres.2004.08.007
[58]  Akasaki K, Michihara A, Fujiwara Y, Mibuka K, Tsuji H (1996) Biosynthetic transport of a major lysosome-associated membrane glycoprotein 2, lamp-2: a significant fraction of newly synthesized lamp-2 is delivered to lysosomes by way of early endosomes. J Biochem 120: 1088–1094. doi: 10.1093/oxfordjournals.jbchem.a021526
[59]  Hristov G, Kramer M, Li J, El-Andaloussi N, Mora R, et al. (2010) Through its nonstructural protein NS1, parvovirus H-1 induces apoptosis via accumulation of reactive oxygen species. J Virol 84: 5909–5922. doi: 10.1128/jvi.01797-09
[60]  Geletneky K, Huesing J, Rommelaere J, Schlehofer JR, Dahm M, et al. (2012) Phase I/IIa study of intratumoral/intracerebral or intravenous/intracerebral administration of Parvovirus H-1 (ParvOryx) in patients with progressive primary or recurrent glioblastoma multiforme: ParvOryx01 protocol. BMC Cancer 12: 99. doi: 10.1186/1471-2407-12-99
[61]  Grekova SP, Rommelaere J, Raykov Z (2012) Parvoviruses-tools to fine-tune anticancer immune responses. Oncoimmunology 1: 1417–1419. doi: 10.4161/onci.21097
[62]  Grekova S, Aprahamian M, Giese N, Schmitt S, Giese T, et al. (2011) Immune cells participate in the oncosuppressive activity of parvovirus H-1PV and are activated as a result of their abortive infection with this agent. Cancer Biol Ther 10: 1280–1289. doi: 10.4161/cbt.10.12.13455
[63]  Eichwald V, Daeffler L, Klein M, Rommelaere J, Salome N (2002) The NS2 proteins of parvovirus minute virus of mice are required for efficient nuclear egress of progeny virions in mouse cells. J Virol 76: 10307–10319. doi: 10.1128/jvi.76.20.10307-10319.2002
[64]  Lachmann S, Rommeleare J, Nuesch JP (2003) Novel PKCeta is required to activate replicative functions of the major nonstructural protein NS1 of minute virus of mice. J Virol 77: 8048–8060. doi: 10.1128/jvi.77.14.8048-8060.2003
[65]  Kruger L, Eskerski H, Dinsart C, Cornelis J, Rommelaere J, et al. (2008) Augmented transgene expression in transformed cells using a parvoviral hybrid vector. Cancer Gene Ther 15: 252–267. doi: 10.1038/sj.cgt.7701113
[66]  Kuck D, Lau T, Leuchs B, Kern A, Muller M, et al. (2006) Intranasal vaccination with recombinant adeno-associated virus type 5 against human papillomavirus type 16 L1. J Virol 80: 2621–2630. doi: 10.1128/jvi.80.6.2621-2630.2006
[67]  Fullekrug J, Sonnichsen B, Wunsch U, Arseven K, Nguyen Van P, et al. (1994) CaBP1, a calcium binding protein of the thioredoxin family, is a resident KDEL protein of the ER and not of the intermediate compartment. J Cell Sci 107 ((Pt 10)) 2719–2727.
[68]  Nuesch JP, Corbau R, Tattersall P, Rommelaere J (1998) Biochemical activities of minute virus of mice nonstructural protein NS1 are modulated In vitro by the phosphorylation state of the polypeptide. J Virol 72: 8002–8012.

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