Host mTORC1 signaling regulates andes virus replication

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 912-922

  McNulty, Shannon ^a,b   Flint, Mike ^a   Nichol, Stuart T ^a   Spiropoulou, Christina F ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b BERRY COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CC1 779; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; PROTEIN P70; TEMSIROLIMUS; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN; VIRUS PROTEIN;

ANDES VIRUS; ANTIVIRAL ACTIVITY; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; HANTAVIRUS; HANTAVIRUS INFECTION; HUMAN; HUMAN CELL; MICROVASCULAR ENDOTHELIAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; TUBEROUS SCLEROSIS; UPREGULATION; VIRUS INHIBITION; VIRUS NEUTRALIZATION; VIRUS PATHOGENESIS; VIRUS RELEASE; VIRUS REPLICATION;

ANTIVIRAL AGENTS; CELLS, CULTURED; GENE KNOCKDOWN TECHNIQUES; HANTAVIRUS; HUMANS; MULTIPROTEIN COMPLEXES; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; VIRUS REPLICATION;

ANDES VIRUS; HANTAVIRUS; MAMMALIA;

EID: 84871987961     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02415-12     Document Type: Article

References (71)

1. Bi Z, Formenty PB, Roth CE. 2008. Hantavirus infection: a review and global update. J. Infect. Dev. Ctries. 2:3-23.
2. Luan VD, Yoshimatsu K, Endo R, Taruishi M, Huong VT, Dat DT, Tien PC, Shimizu K, Koma T, Yasuda SP, Nhi L, Huong VT, Arikawa J. 2012. Studies on hantavirus infection in small mammals captured in Southern and Central Highland area of Vietnam. J. Vet. Med. Sci. 74: 1155-1162.
3. Nichol ST, Spiropoulou CF, Morzunov S, Rollin PE, Ksiazek TG, Feldmann H, Sanchez A, Childs J, Zaki S, Peters CJ. 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262:914-917.
4. Zeier M, Handermann M, Bahr U, Rensch B, Muller S, Kehm R, Muranyi W, Darai G. 2005. New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention: a review. Virus Genes 30:157-180.
5. Zhang Y, Yuan J, Yang X, Zhou J, Yang W, Peng C, Zhang HL, Shi Z. 2011. A novel hantavirus detected in Yunnan red-backed vole (Eothenomys miletus) in China. J. Gen. Virol. 92:1454-1457.
6. Schmaljohn CN, Nichol ST. 2007. Bunyaviridae, p 1741-1789. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
7. Macneil A, Nichol ST, Spiropoulou CF. 2011. Hantavirus pulmonary syndrome. Virus Res. 162:138-147.
8. da Rosa Elkhoury M, da Silva Mendes W, Waldman EA, Dias JP, Carmo EH, Fernando da Costa Vasconcelos P. 2012. Hantavirus pulmonary syndrome: prognostic factors for death in reported cases in Brazil. Trans. R. Soc. Trop. Med. Hyg. 106:298-302.
9. MacNeil A, Ksiazek TG, Rollin PE. 2011. Hantavirus pulmonary syndrome, United States, 1993-2009. Emerg. Infect. Dis. 17:1195-1201.
10. Martinez VP, Bellomo CM, Cacace ML, Suarez P, Bogni L, Padula PJ. 2010. Hantavirus pulmonary syndrome in Argentina, 1995-2008. Emerg. Infect. Dis. 16:1853-1860.
11. Dietl CA, Wernly JA, Pett SB, Yassin SF, Sterling JP, Dragan R, Milligan K, Crowley MR. 2008. Extracorporeal membrane oxygenation support improves survival of patients with severe hantavirus cardiopulmonary syndrome. J. Thorac. Cardiovasc. Surg. 135:579-584.
12. Wernly JA, Dietl CA, Tabe CE, Pett SB, Crandall C, Milligan K, Crowley MR. 2011. Extracorporeal membrane oxygenation support improves survival of patients with hantavirus cardiopulmonary syndrome refractory to medical treatment. Eur. J. Cardiothorac. Surg. 40:1334-1340.
13. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER. 2008. Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J. Virol. 82:5797-5806.
14. Gorbunova E, Gavrilovskaya IN, Mackow ER. 2010. Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cells. J. Virol. 84:7405-7411.
15. Gorbunova EE, Gavrilovskaya IN, Pepini T, Mackow ER. 2011. VEGFR2 and Src kinase inhibitors suppress Andes virus-induced endothelial cell permeability. J. Virol. 85:2296-2303.
16. Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF. 2010. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J. Virol. 84:11227-11234.
17. Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, Rollin PE, Ksiazek TG, Nichol ST, Mahy BWJ, Peters CJ. 1995. Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am. J. Pathol. 146:552-579.
18. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, Kang CY, Kolakofsky D. 1995. The 5' ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J. Virol. 69:5754-5762.
19. Hutchinson KL, Peters CJ, Nichol ST. 1996. Sin Nombre virus mRNA synthesis. Virology 224:139-149.
20. Reguera J, Weber F, Cusack S. 2010. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, es- sential for viral cap-dependent transcription. PLoS Pathog. 6:e1001101. doi:10.1371/journal.ppat.1001101.
21. 7G cap- and RNA-binding sites. J. Biol. Chem. 285: 11357-11368.
22. Cheng E, Haque A, Rimmer MA, Hussein IT, Sheema S, Little A, Mir MA. 2011. Characterization of the interaction between hantavirus nucleocapsid protein (N) and ribosomal protein S19 (RPS19). J. Biol. Chem. 286:11814-11824.
23. Haque A, Mir MA. 2010. Interaction of hantavirus nucleocapsid protein with ribosomal protein S19. J. Virol. 84:12450-12453.
24. Mir MA, Panganiban AT. 2008. A protein that replaces the entire cellular eIF4F complex. EMBO J. 27:3129-3139.
25. Magnuson B, Ekim B, Fingar DC. 2012. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem. J. 441:1-21.
26. Sengupta S, Peterson TR, Sabatini DM. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol. Cell 40:310-322.
27. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN. 2004. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 6:1122-1128.
28. Oh WJ, Jacinto E. 2011. mTOR complex 2 signaling and functions. Cell Cycle 10:2305-2316.
29. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument- Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptorindependent pathway that regulates the cytoskeleton. Curr. Biol. 14: 1296-1302.
30. Dan HC, Sun M, Yang L, Feldman RI, Sui XM, Ou CC, Nellist M, Yeung RS, Halley DJ, Nicosia SV, Pledger WJ, Cheng JQ. 2002. Phosphatidylinositol 3-kinase/Akt pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J. Biol. Chem. 277: 35364-35370.
31. Hayashi AA, Proud CG. 2007. The rapid activation of protein synthesis by growth hormone requires signaling through mTOR. Am. J. Physiol. Endocrinol. Metab. 292:E1647-E1655.
32. Inoki K, Li Y, Zhu T, Wu J, Guan KL. 2002. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 4:648-657.
33. Manning BD, Tee AR, Logsdon MN, Blenis J, Cantley LC. 2002. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/Akt pathway. Mol. Cell 10:151-162.
34. Garami A, Zwartkruis FJ, Nobukuni T, Joaquin M, Roccio M, Stocker H, Kozma SC, Hafen E, Bos JL, Thomas G. 2003. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2. Mol. Cell 11:1457-1466.
35. Inoki K, Li Y, Xu T, Guan KL. 2003. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17:1829-1834.
36. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141:290-303.
37. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar- Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496-1501.
38. Hsu PP, Kang SA, Rameseder J, Zhang Y, Ottina KA, Lim D, Peterson TR, Choi Y, Gray NS, Yaffe MB, Marto JA, Sabatini DM. 2011. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1- mediated inhibition of growth factor signaling. Science 332:1317-1322.
39. Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villen J, Kubica N, Hoffman GR, Cantley LC, Gygi SP, Blenis J. 2011. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332:1322-1326.
40. Price DJ, Grove JR, Calvo V, Avruch J, Bierer BE. 1992. Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science 257:973-977.
41. Rosner M, Hengstschlager M. 2011. Nucleocytoplasmic localization of p70 S6K1, but not of its isoforms p85 and p31, is regulated by TSC2/ mTOR. Oncogene 30:4509-4522.
42. von Manteuffel SR, Dennis PB, Pullen N, Gingras AC, Sonenberg N, Thomas G. 1997. The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70S6K. Mol. Cell. Biol. 17:5426-5436.
43. Jefferies HB, Reinhard C, Kozma SC, Thomas G. 1994. Rapamycin selectively represses translation of the "polypyrimidine tract"mRNAfamily. Proc. Natl. Acad. Sci. U. S. A. 91:4441-4445.
44. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM. 2012. A unifying model for mTORC1-mediated regulation ofmRNA translation. Nature 485:109-113.
45. Flint M, Logvinoff C, Rice CM, McKeating JA. 2004. Characterization of infectious retroviral pseudotype particles bearing hepatitis C virus glycoproteins. J. Virol. 78:6875-6882.
46. Spiropoulou CF, Goldsmith CS, Shoemaker TR, Peters CJ, Compans RW. 2003. Sin Nombre virus glycoprotein trafficking. Virology 308:48-63.
47. Hussein IT, Cheng E, Ganaie SS, Werle MJ, Sheema S, Haque A, Mir MA. 2012. Autophagic clearance of Sin Nombre hantavirus glycoprotein Gn promotes virus replication in cells. J. Virol. 86:7520-7529.
48. MacGurn JA, Hsu PC, Smolka MB, Emr SD. 2011. TORC1 regulates endocytosis via Npr1-mediated phosphoinhibition of a ubiquitin ligase adaptor. Cell 147:1104-1117.
49. Meyuhas O, Dreazen A. 2009. Ribosomal protein S6 kinase from TOP mRNAs to cell size. Prog. Mol. Biol. Transl. Sci. 90:109-153.
50. Clippinger AJ, Maguire TG, Alwine JC. 2011. Human cytomegalovirus infection maintains mTOR activity and its perinuclear localization during amino acid deprivation. J. Virol. 85:9369-9376.
51. Peng L, Liang D, Tong W, Li J, Yuan Z. 2010. Hepatitis C virus NS5A activates the mammalian target of rapamycin (mTOR) pathway, contributing to cell survival by disrupting the interaction between FK506-binding protein 38 (FKBP38) and mTOR. J. Biol. Chem. 285:20870-20881.
52. Tomasoni R, Mondino A. 2011. The tuberous sclerosis complex: balancing proliferation and survival. Biochem. Soc. Trans. 39:466-471.
53. Budde K, Gaedeke J. 2012. Tuberous sclerosis complex-associated angiomyolipomas: focus on mTOR inhibition. Am. J. Kidney Dis. 59:276-283.
54. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL. 1994. A mammalian protein targeted by G1-arresting rapamycin- receptor complex. Nature 369:756-758.
55. Sabatini DM, Erdjument-Bromage H, Lui M, Tempst P, Snyder SH. 1994. RAFT1: a mammalian protein that binds to FKBP12 in a rapamycindependent fashion and is homologous to yeast TORs. Cell 78:35-43.
56. Lippincott-Schwartz J, Fambrough DM. 1987. Cycling of the integral membrane glycoprotein, LEP100, between plasma membrane and lysosomes: kinetic and morphological analysis. Cell 49:669-677.
57. Bose SK, Shrivastava S, Meyer K, Ray RB, Ray R. 2012. Hepatitis C virus activates the mTOR/S6K1 signaling pathway in inhibiting IRS-1 function for insulin resistance. J. Virol. 86:6315-6322.
58. Buchkovich NJ, Yu Y, Zampieri CA, Alwine JC. 2008. The TORrid affairs of viruses: effects of mammalian DNA viruses on the PI3K-AktmTOR signalling pathway. Nat. Rev. Microbiol. 6:266-275.
59. Joubert PE, Werneke SW, de la Calle C, Guivel-Benhassine F, Giodini A, Peduto L, Levine B, Schwartz O, Lenschow DJ, Albert ML. 2012. Chikungunya virus-induced autophagy delays caspase-dependent cell death. J. Exp. Med. 209:1029-1047.
60. Shuda M, Kwun HJ, Feng H, Chang Y, Moore PS. 2011. Human Merkel cell polyomavirus small T antigen is an oncoprotein targeting the 4E-BP1 translation regulator. J. Clin. Invest. 121:3623-3634.
61. Zaborowska I, Walsh D. 2009. PI3K signaling regulates rapamycininsensitive translation initiation complex formation in vaccinia virusinfected cells. J. Virol. 83:3988-3992.
62. Peterson TR, Sengupta SS, Harris TE, Carmack AE, Kang SA, Balderas E, Guertin DA, Madden KL, Carpenter AE, Finck BN, Sabatini DM. 2011.mTORcomplex 1 regulates lipin 1 localization to control the SREBP pathway. Cell 146:408-420.
63. Settembre C, Zoncu R, Medina DL, Vetrini F, Erdin S, Erdin S, Huynh T, Ferron M, Karsenty G, Vellard MC, Facchinetti V, Sabatini DM, Ballabio A. 2012. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 31:1095-1108.
64. Neshat MS, Mellinghoff IK, Tran C, Stiles B, Thomas G, Petersen R, Frost P, Gibbons JJ, Wu H, Sawyers CL. 2001. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl. Acad. Sci. U. S. A. 98:10314-10319.
65. Shor B, Zhang WG, Toral-Barza L, Lucas J, Abraham RT, Gibbons JJ, Yu K. 2008. A new pharmacologic action of CCI-779 involves FKBP12- independent inhibition of mTOR kinase activity and profound repression of global protein synthesis. Cancer Res. 68:2934-2943.
66. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J. Biol. Chem. 284:8023-8032.
67. Yu K, Toral-Barza L, Discafani C, Zhang WG, Skotnicki J, Frost P, Gibbons JJ. 2001. mTOR, a novel target in breast cancer: the effect of CCI-779, an mTOR inhibitor, in preclinical models of breast cancer. Endocr. Relat. Cancer 8:249-258.
68. Thomas GV, Tran C, Mellinghoff IK, Welsbie DS, Chan E, Fueger B, Czernin J, Sawyers CL. 2006. Hypoxia-inducible factor determines sensitivity to inhibitors of mTOR in kidney cancer. Nat. Med. 12:122-127.
69. Mohankumar V, Dhanushkodi NR, Raju R. 2011. Sindbis virus replication, is insensitive to rapamycin and torin1, and suppresses Akt/mTOR pathway late during infection in HEK cells. Biochem. Biophys. Res. Commun. 406:262-267.
70. Gavrilovskaya IN, Gorbunova EE, Mackow ER. 2012. Andes virus infection of lymphatic endothelial cells causes giant cell and enhanced permeability responses that are rapamycin and vascular endothelial growth factor C sensitive. J. Virol. 86:8765-8772.
71. Zoncu R, Bar-Peled L, Efeyan A, Wang S, Sancak Y, Sabatini DM. 2011. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase. Science 334: 678-683.