Citation: Yue Lu, Ping He, Yuxuan Zhang, Yongwen Ren, Leiliang Zhang. The emerging roles of retromer and sorting nexins in the life cycle of viruses .VIROLOGICA SINICA, 2022, 37(3) : 321-330.  http://dx.doi.org/10.1016/j.virs.2022.04.014

The emerging roles of retromer and sorting nexins in the life cycle of viruses

  • Corresponding author: Leiliang Zhang, armzhang@hotmail.com
  • Received Date: 28 December 2021
    Accepted Date: 12 April 2022
    Available online: 02 May 2022
  • Retromer and sorting nexins (SNXs) transport cargoes from endosomes to the trans-Golgi network or plasma membrane. Recent studies have unveiled the emerging roles for retromer and SNXs in the life cycle of viruses, including members of Coronaviridae, Flaviviridae and Retroviridae. Key components of retromer/SNXs, such as Vps35, Vps26, SNX5 and SNX27, can affect multiple steps of the viral life cycle, including facilitating the entry of viruses into cells, participating in viral replication, and promoting the assembly of virions. Here we present a comprehensive updated review on the interplay between retromer/SNXs and virus, which will shed mechanistic insights into controlling virus infection.

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    1. Al-Saleem, J., Dirksen, W.P., Martinez, M.P., Shkriabai, N., Kvaratskhelia, M., Ratner, L., Green, P.L., 2019. HTLV-1 Tax-1 interacts with SNX27 to regulate cellular localization of the HTLV-1 receptor molecule, GLUT1. PLoS One 14, e0214059.

    2. Amako, Y., Sarkeshik, A., Hotta, H., Yates 3rd, J., Siddiqui, A., 2009. Role of oxysterol binding protein in hepatitis C virus infection. J. Virol. 83, 9237-9246.

    3. Arighi, C.N., Hartnell, L.M., Aguilar, R.C., Haft, C.R., Bonifacino, J.S., 2004. Role of the mammalian retromer in sorting of the cation-independent mannose 6-phosphate receptor. J. Cell Biol. 165, 123-133.

    4. Attar, N., Cullen, P.J., 2010. The retromer complex. Adv. Enzym. Regul. 50, 216-236.

    5. Aydin, I., Villalonga-Planells, R., Greune, L., Bronnimann, M.P., Calton, C.M., Becker, M., Lai, K.Y., Campos, S.K., Schmidt, M.A., Schelhaas, M., 2017. A central region in the minor capsid protein of papillomaviruses facilitates viral genome tethering and membrane penetration for mitotic nuclear entry. PLoS Pathog. 13, e1006308.

    6. Bantel-Schaal, U., Hub, B., Kartenbeck, J., 2002. Endocytosis of adeno-associated virus type 5 leads to accumulation of virus particles in the Golgi compartment. J. Virol. 76, 2340-2349.

    7. Bartuzi, P., Billadeau, D.D., Favier, R., Rong, S., Dekker, D., Fedoseienko, A., Fieten, H., Wijers, M., Levels, J.H., Huijkman, N., Kloosterhuis, N., van der Molen, H., Brufau, G., Groen, A.K., Elliott, A.M., Kuivenhoven, J.A., Plecko, B., Grangl, G., McGaughran, J., Horton, J.D., Burstein, E., Hofker, M.H., van de Sluis, B., 2016. CCC-and WASHmediated endosomal sorting of LDLR is required for normal clearance of circulating LDL. Nat. Commun. 7, 10961.

    8. Bayliss, R., Wheeldon, J., Caucheteux, S.M., Niessen, C.M., Piguet, V., 2020. Identification of host trafficking genes required for HIV-1 virological synapse formation in dendritic cells. J. Virol. 94, e01597-19.

    9. Belenkaya, T.Y., Wu, Y., Tang, X., Zhou, B., Cheng, L., Sharma, Y.V., Yan, D., Selva, E.M., Lin, X., 2008. The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network. Dev. Cell 14, 120-131.

    10. Benfield, C.T.O., Ren, H., Lucas, S.J., Bahsoun, B., Smith, G.L., 2013. Vaccinia virus protein K7 is a virulence factor that alters the acute immune response to infection.J. Gen. Virol. 94, 1647-1657.

    11. Bergant, M., Banks, L., 2013. SNX17 facilitates infection with diverse papillomavirus types. J. Virol. 87, 1270-1273.

    12. Bergant Marusic, M., Ozbun, M.A., Campos, S.K., Myers, M.P., Banks, L., 2012. Human papillomavirus L2 facilitates viral escape from late endosomes via sorting nexin 17.Traffic 13, 455-467.

    13. Berlioz-Torrent, C., Shacklett, B.L., Erdtmann, L., Delamarre, L., Bouchaert, I., Sonigo, P., Dokhelar, M.C., Benarous, R., 1999. Interactions of the cytoplasmic domains of human and simian retroviral transmembrane proteins with components of the clathrin adaptor complexes modulate intracellular and cell surface expression of envelope glycoproteins. J. Virol. 73, 1350-1361.

    14. Bhowmick, S., Chakravarty, C., Sellathamby, S., Lal, S.K., 2017. The influenza A virus matrix protein 2 undergoes retrograde transport from the endoplasmic reticulum into the cytoplasm and bypasses cytoplasmic proteasomal degradation. Arch. Virol. 162, 919-929.

    15. Bianco, A., Reghellin, V., Donnici, L., Fenu, S., Alvarez, R., Baruffa, C., Peri, F., Pagani, M., Abrignani, S., Neddermann, P., De Francesco, R., 2012. Metabolism of phosphatidylinositol 4-kinase IIIalpha-dependent PI4P Is subverted by HCV and is targeted by a 4-anilino quinazoline with antiviral activity. PLoS Pathog. 8, e1002576.

    16. Bonifacino, J.S., Hurley, J.H., 2008. Retromer. Curr. Opin. Cell Biol. 20, 427-436.

    17. Bonifacino, J.S., Rojas, R., 2006. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 7, 568-579.

    18. Borg Distefano, M., Hofstad Haugen, L., Wang, Y., Perdreau-Dahl, H., Kjos, I., Jia, D., Morth, J.P., Neefjes, J., Bakke, O., Progida, C., 2018. TBC1D5 controls the GTPase cycle of Rab7b. J. Cell Sci. 131, jcs216630.

    19. Bronnimann, M.P., Chapman, J.A., Park, C.K., Campos, S.K., 2013. A transmembrane domain and GxxxG motifs within L2 are essential for papillomavirus infection.J. Virol. 87, 464-473.

    20. Bugarcic, A., Zhe, Y., Kerr, M.C., Griffin, J., Collins, B.M., Teasdale, R.D., 2011. Vps26A and Vps26B subunits define distinct retromer complexes. Traffic 12, 1759-1773.

    21. Bujny, M.V., Popoff, V., Johannes, L., Cullen, P.J., 2007. The retromer component sorting nexin-1 is required for efficient retrograde transport of Shiga toxin from early endosome to the trans Golgi network. J. Cell Sci. 120, 2010-2021.

    22. Burd, C., Cullen, P.J., 2014. Retromer:a master conductor of endosome sorting. Cold Spring Harbor Perspect. Biol. 6, a016774.

    23. Byland, R., Vance, P.J., Hoxie, J.A., Marsh, M., 2007. A conserved dileucine motif mediates clathrin and AP-2-dependent endocytosis of the HIV-1 envelope protein.Mol. Biol. Cell 18, 414-425.

    24. Cai, L., Loo, L.S., Atlashkin, V., Hanson, B.J., Hong, W., 2011. Deficiency of sorting nexin 27 (SNX27) leads to growth retardation and elevated levels of N-methyl-D-aspartate receptor 2C (NR2C). Mol. Cell Biol. 31, 1734-1747.

    25. Cardoso, R.S., Tavares, L.A., Jesus, B.L.S., Criado, M.F., de Carvalho, A.N., Souza, J.P., Bedi, S., de Souza, M.M., Silva, M.L., Lanfredi, G.P., Vitti, B.C., Scudero, O.B., Faca, V.M., Ono, A., Ventura, A.M., daSilva, L.L.P., Arruda, E., 2020. Host retromer protein sorting nexin 2 interacts with human respiratory syncytial virus structural proteins and is required for efficient viral production. mBio 11, e01869-20.

    26. Carlton, J., Bujny, M., Peter, B.J., Oorschot, V.M., Rutherford, A., Mellor, H., Klumperman, J., McMahon, H.T., Cullen, P.J., 2004. Sorting nexin-1 mediates tubular endosome-to-TGN transport through coincidence sensing of high-curvature membranes and 3-phosphoinositides. Curr. Biol. 14, 1791-1800.

    27. Cattin-Ortolá, J., Welch, L.G., Maslen, S.L., Papa, G., James, L.C., Munro, S., 2021.Sequences in the cytoplasmic tail of SARS-CoV-2 Spike facilitate expression at the cell surface and syncytia formation. Nat. Commun. 12, 5333.

    28. Chattopadhyay, A., Wang, E., Seymour, R., Weaver, S.C., Rose, J.K., 2013. A chimeric vesiculo/alphavirus is an effective alphavirus vaccine. J. Virol. 87, 395-402.

    29. Checkley, M.A., Luttge, B.G., Freed, E.O., 2011. HIV-1 envelope glycoprotein biosynthesis, trafficking, and incorporation. J. Mol. Biol. 410, 582-608.

    30. Cheung, T.K., Poon, L.L., 2007. Biology of influenza a virus. Ann. N. Y. Acad. Sci. 1102, 1-25.

    31. Choy, R.W., Park, M., Temkin, P., Herring, B.E., Marley, A., Nicoll, R.A., von Zastrow, M., 2014. Retromer mediates a discrete route of local membrane delivery to dendrites.Neuron 82, 55-62.

    32. Cullen, P.J., 2008. Endosomal sorting and signalling:an emerging role for sorting nexins.Nat. Rev. Mol. Cell Biol. 9, 574-582.

    33. Cullen, P.J., Korswagen, H.C., 2011. Sorting nexins provide diversity for retromerdependent trafficking events. Nat. Cell Biol. 14, 29-37.

    34. Daniloski, Z., Jordan, T.X., Wessels, H.H., Hoagland, D.A., Kasela, S., Legut, M., Maniatis, S., Mimitou, E.P., Lu, L., Geller, E., Danziger, O., Rosenberg, B.R., Phatnani, H., Smibert, P., Lappalainen, T., tenOever, B.R., Sanjana, N.E., 2021.Identification of required host factors for SARS-CoV-2 infection in human cells. Cell 184, 92-105.

    35. Das, S., Pellett, P.E., 2011. Spatial relationships between markers for secretory and endosomal machinery in human cytomegalovirus-infected cells versus those in uninfected cells. J. Virol. 85, 5864-5879.

    36. Das, S., Vasanji, A., Pellett, P.E., 2007. Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus. J. Virol. 81, 11861-11869.

    37. Davison, A.J., Eberle, R., Ehlers, B., Hayward, G.S., McGeoch, D.J., Minson, A.C., Pellett, P.E., Roizman, B., Studdert, M.J., Thiry, E., 2009. The order Herpesvirales.Arch. Virol. 154, 171-177.

    38. Day, P.M., Thompson, C.D., Schowalter, R.M., Lowy, D.R., Schiller, J.T., 2013.Identification of a role for the trans-Golgi network in human papillomavirus 16 pseudovirus infection. J. Virol. 87, 3862-3870.

    39. Day, P.M., Weisberg, A.S., Thompson, C.D., Hughes, M.M., Pang, Y.Y., Lowy, D.R., Schiller, J.T., 2019. Human papillomavirus 16 capsids mediate nuclear entry during infection. J. Virol. 93, e00454-19.

    40. DiGiuseppe, S., Luszczek, W., Keiffer, T.R., Bienkowska-Haba, M., Guion, L.G., Sapp, M.J., 2016. Incoming human papillomavirus type 16 genome resides in a vesicular compartment throughout mitosis. Proc. Natl. Acad. Sci. U. S. A. 113, 6289-6294.

    41. Fjorback, A.W., Seaman, M., Gustafsen, C., Mehmedbasic, A., Gokool, S., Wu, C., Militz, D., Schmidt, V., Madsen, P., Nyengaard, J.R., Willnow, T.E., Christensen, E.I., Mobley, W.B., Nykjaer, A., Andersen, O.M., 2012. Retromer binds the FANSHY sorting motif in SorLA to regulate amyloid precursor protein sorting and processing. J. Neurosci. 32, 1467-1480.

    42. Gallon, M., Clairfeuille, T., Steinberg, F., Mas, C., Ghai, R., Sessions, R.B., Teasdale, R.D., Collins, B.M., Cullen, P.J., 2014. A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc. Natl. Acad. Sci. U. S. A. 111, E3604-E3613.

    43. Ganti, K., Massimi, P., Manzo-Merino, J., Tomaic, V., Pim, D., Playford, M.P., Lizano, M., Roberts, S., Kranjec, C., Doorbar, J., Banks, L., 2016a. Interaction of the human papillomavirus E6 oncoprotein with sorting nexin 27 modulates endocytic cargo transport pathways. PLoS Pathog. 12, e1005854.

    44. Ganti, K., Massimi, P., Manzo-Merino, J., Tomaic, V., Pim, D., Playford, M.P., Lizano, M., Roberts, S., Kranjec, C., Doorbar, J., Banks, L., 2016b. Interaction of the human papillomavirus E6 oncoprotein with sorting nexin 27 modulates endocytic cargo transport pathways. PLoS Pathog. 12, e1005854.

    45. Ghai, R., Bugarcic, A., Liu, H., Norwood, S.J., Skeldal, S., Coulson, E.J., Li, S.S., Teasdale, R.D., Collins, B.M., 2013. Structural basis for endosomal trafficking of diverse transmembrane cargos by PX-FERM proteins. Proc. Natl. Acad. Sci. U. S. A. 110, E643-E652.

    46. Goncalves, D.U., Proietti, F.A., Ribas, J.G., Araujo, M.G., Pinheiro, S.R., Guedes, A.C., Carneiro-Proietti, A.B., 2010. Epidemiology, treatment, and prevention of human Tcell leukemia virus type 1-associated diseases. Clin. Microbiol. Rev. 23, 577-589.

    47. Griffin, C.T., Trejo, J., Magnuson, T., 2005. Genetic evidence for a mammalian retromer complex containing sorting nexins 1 and 2. Proc. Natl. Acad. Sci. U. S. A. 102, 15173-15177.

    48. Griffin, L.M., Cicchini, L., Xu, T., Pyeon, D., 2014. Human keratinocyte cultures in the investigation of early steps of human papillomavirus infection. Methods Mol. Biol. 1195, 219-238.

    49. Grimm, D., Kay, M.A., 2003. From virus evolution to vector revolution:use of naturally occurring serotypes of adeno-associated virus (AAV) as novel vectors for human gene therapy. Curr. Gene Ther. 3, 281-304.

    50. Groppelli, E., Len, A.C., Granger, L.A., Jolly, C., 2014. Retromer regulates HIV-1 envelope glycoprotein trafficking and incorporation into virions. PLoS Pathog. 10, e1004518.

    51. Guerra, F., Bucci, C., 2016. Multiple roles of the small GTPase Rab7. Cells 5, 34.

    52. Haft, C.R., de la Luz Sierra, M., Bafford, R., Lesniak, M.A., Barr, V.A., Taylor, S.I., 2000. Human orthologs of yeast vacuolar protein sorting proteins Vps26, 29, and 35:assembly into multimeric complexes. Mol. Biol. Cell 11, 4105-4116.

    53. Harbour, M.E., Breusegem, S.Y., Seaman, M.N., 2012. Recruitment of the endosomal WASH complex is mediated by the extended ‘tail’ of Fam21 binding to the retromer protein Vps35. Biochem. J. 442, 209-220.

    54. Harrison, K., Haga, I.R., Pechenick Jowers, T., Jasim, S., Cintrat, J.C., Gillet, D., SchmittJohn, T., Digard, P., Beard, P.M., 2016. Vaccinia virus uses retromer-independent cellular retrograde transport pathways to facilitate the wrapping of intracellular mature virions during virus morphogenesis. J. Virol. 90, 10120-10132.

    55. Harrison, M.S., Hung, C.S., Liu, T.T., Christiano, R., Walther, T.C., Burd, C.G., 2014. A mechanism for retromer endosomal coat complex assembly with cargo. Proc. Natl. Acad. Sci. U. S. A. 111, 267-272.

    56. Henkel, J.R., Apodaca, G., Altschuler, Y., Hardy, S., Weisz, O.A., 1998. Selective perturbation of apical membrane traffic by expression of influenza M2, an acidactivated ion channel, in polarized madin-darby canine kidney cells. Mol. Biol. Cell 9, 2477-2490.

    57. Hong, Z., Yang, X., Yang, G., Zhang, L., 2014. Hepatitis C virus NS5A competes with PI4KB for binding to ACBD3 in a genotype-dependent manner. Antivir. Res. 107, 50-55.

    58. Hsiao, J.C., Chu, L.W., Lo, Y.T., Lee, S.P., Chen, T.J., Huang, C.Y., Ping, Y.H., Chang, W., 2015. Intracellular transport of vaccinia virus in HeLa cells requires WASH-VPEF/FAM21-Retromer complexes and recycling molecules Rab11 and Rab22. J. Virol. 89, 8365-8382.

    59. Hsu, N.Y., Ilnytska, O., Belov, G., Santiana, M., Chen, Y.H., Takvorian, P.M., Pau, C., van der Schaar, H., Kaushik-Basu, N., Balla, T., Cameron, C.E., Ehrenfeld, E., van Kuppeveld, F.J., Altan-Bonnet, N., 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141, 799-811.

    60. Huang, C.Y., Lu, T.Y., Bair, C.H., Chang, Y.S., Jwo, J.K., Chang, W., 2008. A novel cellular protein, VPEF, facilitates vaccinia virus penetration into HeLa cells through fluid phase endocytosis. J. Virol. 82, 7988-7999.

    61. Jia, D., Gomez, T.S., Billadeau, D.D., Rosen, M.K., 2012. Multiple repeat elements within the FAM21 tail link the WASH actin regulatory complex to the retromer. Mol. Biol.Cell 23, 2352-2361.

    62. Jia, D., Zhang, J.S., Li, F., Wang, J., Deng, Z., White, M.A., Osborne, D.G., PhillipsKrawczak, C., Gomez, T.S., Li, H., Singla, A., Burstein, E., Billadeau, D.D., Rosen, M.K., 2016. Structural and mechanistic insights into regulation of the retromer coat by TBC1d5. Nat. Commun. 7, 13305.

    63. Jimenez-Orgaz, A., Kvainickas, A., Nagele, H., Denner, J., Eimer, S., Dengjel, J., Steinberg, F., 2018. Control of RAB7 activity and localization through the retromerTBC1D5 complex enables RAB7-dependent mitophagy. EMBO J. 37, 235-254.

    64. Johannes, L., Popoff, V., 2008. Tracing the retrograde route in protein trafficking. Cell 135, 1175-1187.

    65. Johnson, J.S., Gentzsch, M., Zhang, L., Ribeiro, C.M., Kantor, B., Kafri, T., Pickles, R.J., Samulski, R.J., 2011. AAV exploits subcellular stress associated with inflammation, endoplasmic reticulum expansion, and misfolded proteins in models of cystic fibrosis.PLoS Pathog. 7, e1002053.

    66. Keiser, N.W., Yan, Z., Zhang, Y., Lei-Butters, D.C., Engelhardt, J.F., 2011. Unique characteristics of AAV1, 2, and 5 viral entry, intracellular trafficking, and nuclear import define transduction efficiency in HeLa cells. Hum. Gene Ther. 22, 1433-1444.

    67. Kerr, M.C., Bennetts, J.S., Simpson, F., Thomas, E.C., Flegg, C., Gleeson, P.A., Wicking, C., Teasdale, R.D., 2005. A novel mammalian retromer component, Vps26B. Traffic 6, 991-1001.

    68. Khan, I., Katikaneni, D.S., Han, Q., Sanchez-Felipe, L., Hanada, K., Ambrose, R.L., Mackenzie, J.M., Konan, K.V., 2014. Modulation of hepatitis C virus genome replication by glycosphingolipids and four-phosphate adaptor protein 2. J. Virol. 88, 12276-12295.

    69. Kingston, D., Chang, H., Ensser, A., Lee, H.R., Lee, J., Lee, S.H., Jung, J.U., Cho, N.H., 2011. Inhibition of retromer activity by herpesvirus saimiri tip leads to CD4 downregulation and efficient T cell transformation. J. Virol. 85, 10627-10638.

    70. Kliche, J., Kuss, H., Ali, M., Ivarsson, Y., 2021. Cytoplasmic short linear motifs in ACE2 and integrin beta3 link SARS-CoV-2 host cell receptors to mediators of endocytosis and autophagy. Sci. Signal. 14, eabf1117.

    71. Kuwahara, T., Inoue, K., D'Agati, V.D., Fujimoto, T., Eguchi, T., Saha, S., Wolozin, B., Iwatsubo, T., Abeliovich, A., 2016. LRRK2 and RAB7L1 coordinately regulate axonal morphology and lysosome integrity in diverse cellular contexts. Sci. Rep. 6, 29945.

    72. Kvainickas, A., Jimenez-Orgaz, A., Nagele, H., Hu, Z., Dengjel, J., Steinberg, F., 2017. Cargo-selective SNX-BAR proteins mediate retromer trimer independent retrograde transport. J. Cell Biol. 216, 3677-3693.

    73. Lee, S., Chang, J., Blackstone, C., 2016. FAM21 directs SNX27-retromer cargoes to the plasma membrane by preventing transport to the Golgi apparatus. Nat. Commun. 7, 10939.

    74. Li, H., Koo, Y., Mao, X., Sifuentes-Dominguez, L., Morris, L.L., Jia, D., Miyata, N., Faulkner, R.A., van Deursen, J.M., Vooijs, M., Billadeau, D.D., van de Sluis, B., Cleaver, O., Burstein, E., 2015. Endosomal sorting of Notch receptors through COMMD9-dependent pathways modulates Notch signaling. J. Cell Biol. 211, 605-617.

    75. Li, H., Yang, X., Yang, G., Hong, Z., Zhou, L., Yin, P., Xiao, Y., Chen, L., Chung, R.T., Zhang, L., 2014. Hepatitis C virus NS5A hijacks ARFGAP1 to maintain a phosphatidylinositol 4-phosphate-enriched microenvironment. J. Virol. 88, 5956-5966.

    76. Li, Y., Zhang, L., Ke, Y., 2017. Cellular interactome analysis of vaccinia virus K7 protein identifies three transport machineries as binding partners for K7. Virus Gene. 53, 814-822.

    77. Lim, Y.S., Hwang, S.B., 2011. Hepatitis C virus NS5A protein interacts with phosphatidylinositol 4-kinase type IIIalpha and regulates viral propagation. J. Biol. Chem. 286, 11290-11298.

    78. Lipovsky, A., Erden, A., Kanaya, E., Zhang, W., Crite, M., Bradfield, C., MacMicking, J., DiMaio, D., Schoggins, J.W., Iwasaki, A., 2017. The cellular endosomal protein stannin inhibits intracellular trafficking of human papillomavirus during virus entry.J. Gen. Virol. 98, 2821-2836.

    79. Lipovsky, A., Popa, A., Pimienta, G., Wyler, M., Bhan, A., Kuruvilla, L., Guie, M.A., Poffenberger, A.C., Nelson, C.D., Atwood, W.J., DiMaio, D., 2013. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proc. Natl. Acad. Sci. U. S. A. 110, 7452-7457.

    80. Liu, T.T., Gomez, T.S., Sackey, B.K., Billadeau, D.D., Burd, C.G., 2012. Rab GTPase regulation of retromer-mediated cargo export during endosome maturation. Mol.Biol. Cell 23, 2505-2515.

    81. Lucas, M., Gershlick, D.C., Vidaurrazaga, A., Rojas, A.L., Bonifacino, J.S., Hierro, A., 2016.Structural mechanism for cargo recognition by the retromer complex. Cell 167, 1623-1635 e1614.

    82. Maschkowitz, G., Gartner, S., Hofmann-Winkler, H., Fickenscher, H., Winkler, M., 2018.Interaction of human cytomegalovirus tegument proteins ppUL35 and ppUL35A with sorting nexin 5 regulates glycoprotein B (gpUL55) localization. J. Virol. 92, e00013-18.

    83. Mercer, J., Helenius, A., 2008. Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320, 531-535.

    84. Muscolino, E., Schmitz, R., Loroch, S., Caragliano, E., Schneider, C., Rizzato, M., Kim, Y.H., Krause, E., Juranić Lisnić, V., Sickmann, A., Reimer, R., Ostermann, E., Brune, W., 2020. Herpesviruses induce aggregation and selective autophagy of host signalling proteins NEMO and RIPK1 as an immune-evasion mechanism. Nat.Microbiol. 5, 331-342.

    85. Nair, H., Brooks, W.A., Katz, M., Roca, A., Berkley, J.A., Madhi, S.A., Simmerman, J.M., Gordon, A., Sato, M., Howie, S., Krishnan, A., Ope, M., Lindblade, K.A., CarosoneLink, P., Lucero, M., Ochieng, W., Kamimoto, L., Dueger, E., Bhat, N., Vong, S., Theodoratou, E., Chittaganpitch, M., Chimah, O., Balmaseda, A., Buchy, P., Harris, E., Evans, V., Katayose, M., Gaur, B., O'Callaghan-Gordo, C., Goswami, D., Arvelo, W., Venter, M., Briese, T., Tokarz, R., Widdowson, M.A., Mounts, A.W., Breiman, R.F., Feikin, D.R., Klugman, K.P., Olsen, S.J., Gessner, B.D., Wright, P.F., Rudan, I., Broor, S., Simoes, E.A., Campbell, H., 2011. Global burden of respiratory infections due to seasonal influenza in young children:a systematic review and meta-analysis.Lancet 378, 1917-1930.

    86. Niu, Y., Zhang, C., Sun, Z., Hong, Z., Li, K., Sun, D., Yang, Y., Tian, C., Gong, W., Liu, J.J., 2013. PtdIns(4)P regulates retromer-motor interaction to facilitate dynein-cargo dissociation at the trans-Golgi network. Nat. Cell Biol. 15, 417-429.

    87. Nonnenmacher, M., Weber, T., 2011. Adeno-associated virus 2 infection requires endocytosis through the CLIC/GEEC pathway. Cell Host Microbe 10, 563-576.

    88. Nonnenmacher, M.E., Cintrat, J.C., Gillet, D., Weber, T., 2015. Syntaxin 5-dependent retrograde transport to the trans-Golgi network is required for adeno-associated virus transduction. J. Virol. 89, 1673-1687.

    89. Pajusola, K., Gruchala, M., Joch, H., Luscher, T.F., Yla-Herttuala, S., Bueler, H., 2002.Cell-type-specific characteristics modulate the transduction efficiency of adenoassociated virus type 2 and restrain infection of endothelial cells. J. Virol. 76, 11530-11540.

    90. Papa, G., Mallery, D.L., Albecka, A., Welch, L.G., Cattin-Ortola, J., Luptak, J., Paul, D., McMahon, H.T., Goodfellow, I.G., Carter, A., Munro, S., James, L.C., 2021. Furin cleavage of SARS-CoV-2 Spike promotes but is not essential for infection and cell-cell fusion. PLoS Pathog. 17, e1009246.

    91. Phillips-Krawczak, C.A., Singla, A., Starokadomskyy, P., Deng, Z., Osborne, D.G., Li, H., Dick, C.J., Gomez, T.S., Koenecke, M., Zhang, J.S., Dai, H., Sifuentes-Dominguez, L.F., Geng, L.N., Kaufmann, S.H., Hein, M.Y., Wallis, M., McGaughran, J., Gecz, J., Sluis, B., Billadeau, D.D., Burstein, E., 2015. COMMD1 is linked to the WASH complex and regulates endosomal trafficking of the copper transporter ATP7A. Mol.Biol. Cell 26, 91-103.

    92. Pim, D., Broniarczyk, J., Bergant, M., Playford, M.P., Banks, L., 2015. A novel PDZ domain interaction mediates the binding between human papillomavirus 16 L2 and sorting nexin 27 and modulates virion trafficking. J. Virol. 89, 10145-10155.

    93. Pim, D., Broniarczyk, J., Siddiqa, A., Massimi, P., Banks, L., 2021. Human papillomavirus 16 L2 recruits both retromer and retriever complexes during retrograde trafficking of the viral genome to the cell nucleus. J. Virol. 95, e02068, 20.

    94. Poiesz, B.J., Ruscetti, F.W., Gazdar, A.F., Bunn, P.A., Minna, J.D., Gallo, R.C., 1980.Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. U. S.A. 77, 7415-7419.

    95. Popa, A., Zhang, W., Harrison, M.S., Goodner, K., Kazakov, T., Goodwin, E.C., Lipovsky, A., Burd, C.G., DiMaio, D., 2015. Direct binding of retromer to human papillomavirus type 16 minor capsid protein L2 mediates endosome exit during viral infection. PLoS Pathog. 11, e1004699.

    96. Popovic, D., Akutsu, M., Novak, I., Harper, J.W., Behrends, C., Dikic, I., 2012. Rab GTPase-activating proteins in autophagy:regulation of endocytic and autophagy pathways by direct binding to human ATG8 modifiers. Mol. Cell Biol. 32, 1733-1744.

    97. Popovic, D., Dikic, I., 2014. TBC1D5 and the AP2 complex regulate ATG9 trafficking and initiation of autophagy. EMBO Rep. 15, 392-401.

    98. Ravussin, A., Brech, A., Tooze, S.A., Stenmark, H., 2021. The phosphatidylinositol 3-phosphate-binding protein SNX4 controls ATG9A recycling and autophagy. J. Cell Sci. 134, jcs250670.

    99. Reiss, S., Rebhan, I., Backes, P., Romero-Brey, I., Erfle, H., Matula, P., Kaderali, L., Poenisch, M., Blankenburg, H., Hiet, M.S., Longerich, T., Diehl, S., Ramirez, F., Balla, T., Rohr, K., Kaul, A., Buhler, S., Pepperkok, R., Lengauer, T., Albrecht, M., Eils, R., Schirmacher, P., Lohmann, V., Bartenschlager, R., 2011. Recruitment and activation of a lipid kinase by hepatitis C virus NS5A is essential for integrity of the membranous replication compartment. Cell Host Microbe 9, 32-45.

    100. Rojas, R., van Vlijmen, T., Mardones, G.A., Prabhu, Y., Rojas, A.L., Mohammed, S., Heck, A.J., Raposo, G., van der Sluijs, P., Bonifacino, J.S., 2008. Regulation of retromer recruitment to endosomes by sequential action of Rab5 and Rab7. J. Cell Biol. 183, 513-526.

    101. Schelhaas, M., Shah, B., Holzer, M., Blattmann, P., Kuhling, L., Day, P.M., Schiller, J.T., Helenius, A., 2012. Entry of human papillomavirus type 16 by actindependent, clathrin-and lipid raft-independent endocytosis. PLoS Pathog. 8, e1002657.

    102. Schroder, M., Baran, M., Bowie, A.G., 2008. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J. 27, 2147-2157.

    103. Schuchman, R., Kilianski, A., Piper, A., Vancini, R., Ribeiro, J.M.C., Sprague, T.R., Nasar, F., Boyd, G., Hernandez, R., Glaros, T., 2018. Comparative characterization of the Sindbis virus proteome from mammalian and invertebrate hosts identifies nsP2 as a component of the virion and sorting nexin 5 as a significant host factor for alphavirus replication. J. Virol. 92, e00694, 18.

    104. Seaman, M.N., 2004. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 165, 111-122.

    105. Seaman, M.N., 2005. Recycle your receptors with retromer. Trends Cell Biol. 15, 68-75.

    106. Seaman, M.N., 2007. Identification of a novel conserved sorting motif required for retromer-mediated endosome-to-TGN retrieval. J. Cell Sci. 120, 2378-2389.

    107. Seaman, M.N., 2012. The retromer complex-endosomal protein recycling and beyond.J. Cell Sci. 125, 4693-4702.

    108. Seaman, M.N., Harbour, M.E., Tattersall, D., Read, E., Bright, N., 2009. Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 122, 2371-2382.

    109. Seaman, M.N., McCaffery, J.M., Emr, S.D., 1998. A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J. Cell Biol. 142, 665-681.

    110. Shepard, C.W., Finelli, L., Alter, M.J., 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5, 558-567.

    111. Shi, H., Rojas, R., Bonifacino, J.S., Hurley, J.H., 2006. The retromer subunit Vps26 has an arrestin fold and binds Vps35 through its C-terminal domain. Nat. Struct. Mol. Biol. 13, 540-548.

    112. Siddiqa, A., Massimi, P., Pim, D., Broniarczyk, J., Banks, L., 2018. Human papillomavirus 16 infection induces VAP-dependent endosomal tubulation. J. Virol. 92, e01514-e01517.

    113. Simonetti, B., Danson, C.M., Heesom, K.J., Cullen, P.J., 2017. Sequence-dependent cargo recognition by SNX-BARs mediates retromer-independent transport of CI-MPR. J. Cell Biol. 216, 3695-3712.

    114. Stroupe, C., 2018. This is the end:regulation of Rab7 nucleotide binding in endolysosomal trafficking and autophagy. Front. Cell Dev. Biol. 6, 129.

    115. Tabuchi, M., Yanatori, I., Kawai, Y., Kishi, F., 2010. Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1.J. Cell Sci. 123, 756-766.

    116. Tai, A.W., Salloum, S., 2011. The role of the phosphatidylinositol 4-kinase PI4KA in hepatitis C virus-induced host membrane rearrangement. PLoS One 6, e26300.

    117. Taubenberger, J.K., Morens, D.M., 2010. Influenza:the once and future pandemic. Publ.Health Rep. 125 (Suppl. 3), 16-26.

    118. Temkin, P., Lauffer, B., Jager, S., Cimermancic, P., Krogan, N.J., von Zastrow, M., 2011. SNX27 mediates retromer tubule entry and endosome-to-plasma membrane trafficking of signalling receptors. Nat. Cell Biol. 13, 715-721.

    119. Van Vliet, K., Mohamed, M.R., Zhang, L., Villa, N.Y., Werden, S.J., Liu, J., McFadden, G., 2009. Poxvirus proteomics and virus-host protein interactions. Microbiol. Mol. Biol.Rev. 73, 730-749.

    120. Wang, H., Perry, J.W., Lauring, A.S., Neddermann, P., De Francesco, R., Tai, A.W., 2014.Oxysterol-binding protein is a phosphatidylinositol 4-kinase effector required for HCV replication membrane integrity and cholesterol trafficking. Gastroenterology 146, 1373-1385 e1371-1311.

    121. Wassmer, T., Attar, N., Bujny, M.V., Oakley, J., Traer, C.J., Cullen, P.J., 2007. A loss-offunction screen reveals SNX5 and SNX6 as potential components of the mammalian retromer. J. Cell Sci. 120, 45-54.

    122. Weinberg, M.S., Nicolson, S., Bhatt, A.P., McLendon, M., Li, C., Samulski, R.J., 2014.Recombinant adeno-associated virus utilizes cell-specific infectious entry mechanisms. J. Virol. 88, 12472-12484.

    123. Wyss, S., Berlioz-Torrent, C., Boge, M., Blot, G., Honing, S., Benarous, R., Thali, M., 2001.The highly conserved C-terminal dileucine motif in the cytosolic domain of the human immunodeficiency virus type 1 envelope glycoprotein is critical for its association with the AP-1 clathrin adaptor[correction of adapter]. J. Virol. 75, 2982-2992.

    124. Xie, J., Heim, E.N., Crite, M., DiMaio, D., 2020. TBC1D5-Catalyzed cycling of Rab7 is required for retromer-mediated human papillomavirus trafficking during virus entry.Cell Rep. 31, 107750.

    125. Xie, J., Zhang, P., Crite, M., Lindsay, C.V., DiMaio, D., 2021. Retromer stabilizes transient membrane insertion of L2 capsid protein during retrograde entry of human papillomavirus. Sci. Adv. 7, eabh4276.

    126. Yamane, D., McGivern, D.R., Masaki, T., Lemon, S.M., 2013. Liver injury and disease pathogenesis in chronic hepatitis C. Curr. Top. Microbiol. Immunol. 369, 263-288.

    127. Yang, B., Jia, Y., Meng, Y., Xue, Y., Liu, K., Li, Y., Liu, S., Li, X., Cui, K., Shang, L., Cheng, T., Zhang, Z., Hou, Y., Yang, X., Yan, H., Duan, L., Tong, Z., Wu, C., Liu, Z., Gao, S., Zhuo, S., Huang, W., Gao, G.F., Qi, J., Shang, G., 2022. SNX27 suppresses SARS-CoV-2 infection by inhibiting viral lysosome/late endosome entry. Proc. Natl.Acad. Sci. U. S. A. 119, e2117576119.

    128. Yin, P., Hong, Z., Yang, X., Chung, R.T., Zhang, L., 2016. A role for retromer in hepatitis C virus replication. Cell. Mol. Life Sci. 73, 869-881.

    129. Yin, P., Hong, Z., Zhang, L., Ke, Y., 2017. Retromer localizes to autophagosomes during HCV replication. Virol. Sin. 32, 245-248.

    130. Yong, X., Zhao, L., Deng, W., Sun, H., Zhou, X., Mao, L., Hu, W., Shen, X., Sun, Q., Billadeau, D.D., Xue, Y., Jia, D., 2020. Mechanism of cargo recognition by retromerlinked SNX-BAR proteins. PLoS Biol. 18, e3000631.

    131. Yoshida, M., Miyoshi, I., Hinuma, Y., 1982. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc.Natl. Acad. Sci. U. S. A. 79, 2031-2035.

    132. Young, J.M., Zine El Abidine, A., Gomez-Martinez, R.A., Ozbun, M.A., 2019. The known and potential intersections of rab-GTPases in human papillomavirus infections. Front.Cell Dev. Biol. 7, 139.

    133. Zhang, P., Monteiro da Silva, G., Deatherage, C., Burd, C., DiMaio, D., 2018. Cellpenetrating peptide mediates intracellular membrane passage of human papillomavirus L2 protein to trigger retrograde trafficking. Cell 174, 1465-1476.

    134. Zhang, P., Moreno, R., Lambert, P.F., DiMaio, D., 2020. Cell-penetrating peptide inhibits retromer-mediated human papillomavirus trafficking during virus entry. Proc. Natl.Acad. Sci. U. S. A. 117, 6121-6128.

    135. Zhang, Q.Y., Tan, M.S., Yu, J.T., Tan, L., 2016. The role of retromer in Alzheimer's disease. Mol. Neurobiol. 53, 4201-4209.

    136. Zhao, L., Zhong, K., Zhao, J., Yong, X., Tong, A., Jia, D., 2021. SARS-CoV-2 spike protein harnesses SNX27-mediated endocytic recycling pathway. Med. Comm. 2, 798-809.

    137. Zhu, Y., Feng, F., Hu, G., Wang, Y., Yu, Y., Zhu, Y., Xu, W., Cai, X., Sun, Z., Han, W., Ye, R., Qu, D., Ding, Q., Huang, X., Chen, H., Xu, W., Xie, Y., Cai, Q., Yuan, Z., Zhang, R., 2021. A genome-wide CRISPR screen identifies host factors that regulate SARS-CoV-2entry. Nat. Commun. 12, 961.

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    The emerging roles of retromer and sorting nexins in the life cycle of viruses

      Corresponding author: Leiliang Zhang, armzhang@hotmail.com
    • a Department of Clinical Laboratory Medicine, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Jinan, 250013, China;

    Abstract: Retromer and sorting nexins (SNXs) transport cargoes from endosomes to the trans-Golgi network or plasma membrane. Recent studies have unveiled the emerging roles for retromer and SNXs in the life cycle of viruses, including members of Coronaviridae, Flaviviridae and Retroviridae. Key components of retromer/SNXs, such as Vps35, Vps26, SNX5 and SNX27, can affect multiple steps of the viral life cycle, including facilitating the entry of viruses into cells, participating in viral replication, and promoting the assembly of virions. Here we present a comprehensive updated review on the interplay between retromer/SNXs and virus, which will shed mechanistic insights into controlling virus infection.

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