ADP ribosylation factor 1 plays an essential role in the replication of a plant RNA virus

Journal of Virology

Volumn 87, Issue 1, 2013, Pages 163-176

  Hyodo, Kiwamu ^a   Mine, Akira ^a,c   Taniguchi, Takako ^b   Kaido, Masanori ^a   Mise, Kazuyuki ^a   Taniguchi, Hisaaki ^b   Okuno, Tetsuro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; BREFELDIN A; COAT PROTEIN COMPLEX I; PROTEIN P27; RNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE ANALYSIS; GOLGI COMPLEX; IN VITRO STUDY; INHIBITION KINETICS; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTOPLAST; RED CLOVER NECROTIC MOSAIC VIRUS; RNA REPLICATION; STRUCTURE ANALYSIS; VIRUS ASSEMBLY; VIRUS INDUCTION; VIRUS MORPHOLOGY; VIRUS REPLICATION;

ADP-RIBOSYLATION FACTOR 1; ARABIDOPSIS; CENTRIFUGATION; ENDOPLASMIC RETICULUM; FLUORESCENCE; HOST-PATHOGEN INTERACTIONS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; TOBACCO; TOMBUSVIRIDAE; VIRAL PROTEINS; VIRUS REPLICATION;

EUKARYOTA; RED CLOVER NECROTIC MOSAIC VIRUS; RNA VIRUSES;

EID: 84871961724     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02383-12     Document Type: Article

References (92)

1. Berger KL, Cooper JD, Heaton NS, Yoon R, Oakland TE, Jordan TX, Mateu G, Grakoui A, Randall G. 2009. Roles for endocytic trafficking and phosphatidylinositol 4-kinase III alpha in hepatitis C virus replication. Proc. Natl. Acad. Sci. U.S.A. 106:7577-7582.
2. Cherry S, Doukas T, Armknecht S, Whelan S, Wang H, Sarnow P, Perrimon N. 2005. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev. 19:445- 452.
3. Cherry S, Kunte A, Wang H, Coyne C, Rawson RB, Perrimon N. 2006. COPI activity coupled with fatty acid biosynthesis is required for viral replication. PLoS Pathog. 2:e102. doi:10.1371/journal.ppat.0020102.
4. Gancarz BL, Hao L, He Q, Newton MA, Ahlquist P. 2011. Systematic identification of novel, essential host genes affecting bromovirus RNA replication. PLoS One 6:e23988. doi:10.1371/journal.pone.0023988.
5. Jiang Y, Serviene E, Gal J, Panavas T, Nagy PD. 2006. Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. J. Virol. 80:7394 -7404.
6. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, Ahlquist P. 2003. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. U.S.A. 100:15764 -15769.
7. Li Z, Pogany J, Panavas T, Xu K, Esposito AM, Kinzy TG, Nagy PD. 2009. Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication co-factor. Virology 385:245-260.
8. Panavas T, Serviene E, Brasher J, Nagy PD. 2005. Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc. Natl. Acad. Sci. U.S.A. 102:7326 -7331.
9. Reiss S, Rebhan I, Backes P, Romero-Brey I, Erfle H, Matula P, Kaderali L, Poenisch M, Blankenburg H, Hiet MS, Longerich T, Diehl S, Ramirez F, Balla T, Rohr K, Kaul A, Bühler 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.
10. Serva S, Nagy PD. 2006. Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J. Virol. 80:2162-2169.
11. Shah Nawaz-ul-Rehman M, Martinez-Ochoa N, Pascal H, Sasvari Z, Herbst C, Xu K, Baker J, Sharma M, Herbst A, Nagy PD. 2012. Proteome-wide overexpression of host proteins for identification of factors affecting tombusvirus RNA replication: an inhibitory role of protein kinase C. J. Virol. 86:9384 -9395.
12. Tai AW, Benita Y, Peng LF, Kim SS, Sakamoto N, Xavier RJ, Chung RT. 2009. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5:298 -307.
13. Zhu J, Gopinath K, Murali A, Yi G, Hayward SD, Zhu H, Kao C. 2007. RNA-binding proteins that inhibit RNA virus infection. Proc. Natl. Acad. Sci. U.S.A. 104:3129 -3134.
14. Nagy PD, Pogany J. 2012. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 10:137-149.
15. den Boon JA, Ahlquist P. 2010. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 64:241-256.
16. den Boon JA, Diaz A, Ahlquist P. 2010. Cytoplasmic viral replication complexes. Cell Host Microbe 8:77- 85.
17. Laliberté JF, Sanfaçon H. 2010. Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 48:69 -91.
18. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-374.
19. Barajas D, Jiang Y, Nagy PD. 2009. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog. 5:e1000705. doi:10.1371/journal.ppat.1000705.
20. Barajas D, Nagy PD. 2010. Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 397:358 -368.
21. Reyes FC, Buono R, Otegui MS. 2011. Plant endosomal trafficking pathways. Curr. Opin. Plant Biol. 14:666-673.
22. Diaz A, Wang X, Ahlquist P. 2010. Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc. Natl. Acad. Sci. U.S.A. 107:16291-16296.
23. Hsu NY, Ilnytska O, Belov G, Santiana M, Chen YH, Takvorian PM, Pau C, van der Schaar H, Kaushik-Basu N, Balla T, Cameron CE, Ehrenfeld E, van Kuppeveld FJ, Altan-Bonnet N. 2010. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication. Cell 141:799-811.
24. Tai AW, Salloum S. 2011. The role of the phosphatidylinositol 4-kinase PI4KA in hepatitis C virus-induced host membrane rearrangement. PLoS One 6:e26300. doi:10.1371/journal.pone.0026300.
25. Xiong Z, Kim KH, Kendall TL, Lommel SA. 1993. Synthesis of the putative red clover necrotic mosaic virus RNA polymerase by ribosomal frameshifting in vitro. Virology 193:213-221.
26. Xiong Z, Lommel SA. 1989. The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1. Virology 171:543-554.
27. Kaido M, Tsuno Y, Mise K, Okuno T. 2009. Endoplasmic reticulum targeting of the Red clover necrotic mosaic virus movement protein is associated with the replication of viral RNA1 but not that of RNA2. Virology 395:232-242.
28. Xiong Z, Kim KH, Giesman-Cookmeyer D, Lommel SA. 1993. The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 192:27-32.
29. Mine A, Takeda A, Taniguchi T, Taniguchi H, Kaido M, Mise K, Okuno T. 2010. Identification and characterization of the 480-kilodalton template- specific RNA-dependent RNA polymerase complex of red clover necrotic mosaic virus. J. Virol. 84:6070-6081.
30. Kusumanegara K, Mine A, Hyodo K, Kaido M, Mise K, Okuno T. 2012. Identification of domains in p27 auxiliary replicase protein essential for its association with the endoplasmic reticulum membranes in Red clover necrotic mosaic virus. Virology 433:131-141.
31. Turner KA, Sit TL, Callaway AS, Allen NS, Lommel SA. 2004. Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 320:276 -290.
32. Mine A, Hyodo K, Tajima Y, Kusumanegara K, Taniguchi T, Kaido M, Mise K, Taniguchi H, Okuno T. 2012. Differential roles of Hsp70 and Hsp90 in the assembly of the replicase complex of a positive-strand RNA plant virus. J. Virol. 86:12091-12104.
33. D'Souza-Schorey C, Chavrier P. 2006. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7:347-358.
34. Memon AR. 2004. The role of ADP-ribosylation factor and SAR1 in vesicular trafficking in plants. Biochim. Biophys. Acta 1664:9 -30.
35. Nebenführ A, Ritzenthaler C, Robinson DG. 2002. Brefeldin A: deciphering an enigmatic inhibitor of secretion. Plant Physiol. 130:1102-1108.
36. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G. 2003. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219 -230.
37. Teh OK, Moore I. 2007. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493- 496.
38. Mossessova E, Corpina RA, Goldberg J. 2003. Crystal structure of ARF1*Sec7 complexed with Brefeldin A and its implications for the guanine nucleotide exchange mechanism. Mol. Cell 12:1403-1411.
39. Belov GA, Altan-Bonnet N, Kovtunovych G, Jackson CL, Lippincott-Schwartz J, Ehrenfeld E. 2007. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA. J. Virol. 81:558 -567.
40. Belov GA, Feng Q, Nikovics K, Jackson CL, Ehrenfeld E. 2008. A critical role of a cellular membrane traffic protein in poliovirus RNA replication. PLoS Pathog. 4:e1000216. doi:10.1371/journal.ppat.1000216.
41. Belov GA, Kovtunovych G, Jackson CL, Ehrenfeld E. 2010. Poliovirus replication requires the N terminus but not the catalytic Sec7 domain of ArfGEF GBF1. Cell Microbiol. 12:1463-1479.
42. Cuconati A, Molla A, Wimmer E. 1998. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus. J. Virol. 72:6456-6464.
43. Goueslain L, Alsaleh K, Horellou P, Roingeard P, Descamps V, Duverlie G, Ciczora Y, Wychowski C, Dubuisson J, Rouillé Y. 2010. Identification of GBF1 as a cellular factor required for hepatitis C virus RNA replication. J. Virol. 84:773-787.
44. Lanke KH, van der Schaar HM, Belov GA, Feng Q, Duijsings D, Jackson CL, Ehrenfeld E, van Kuppeveld FJ. 2009. GBF1, a guanine nucleotide exchange factor for Arf, is crucial for coxsackievirus B3RNAreplication. J. Virol. 83:11940 -11949.
45. Matto M, Sklan EH, David N, Melamed-Book N, Casanova JE, Glenn JS, Aroeti B. 2011. Role for ADP ribosylation factor 1 in the regulation of hepatitis C virus replication. J. Virol. 85:946 -956.
46. Verheije MH, Raaben M, Mari M, Te Lintelo EG, Reggiori F, van Kuppeveld FJ, Rottier PJ, de Haan CA. 2008. Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation. PLoS Pathog. 4:e1000088. doi:10.1371/journal.ppat.1000088.
47. Verchot J. 2011. Wrapping membranes around plant virus infection. Curr. Opin. Virol. 1:388 -395.
48. Takeda A, Tsukuda M, Mizumoto H, Okamoto K, Kaido M, Mise K, Okuno T. 2005. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 24:3147-3157.
49. Xiong ZG, Lommel SA. 1991. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 182:388 -392.
50. Janda M, French R, Ahlquist P. 1987. High efficiency T7 polymerase synthesis of infectious RNA from cloned brome mosaic virus cDNA and effects of 5= extensions on transcript infectivity. Virology 158:259 -262.
51. Kaido M, Funatsu N, Tsuno Y, Mise K, Okuno T. 2011. Viral cell-to-cell movement requires formation of cortical punctate structures containing Red clover necrotic mosaic virus movement protein. Virology 413:205- 215.
52. Hyodo K, Mine A, Iwakawa HO, Kaido M, Mise K, Okuno T. 2011. Identification of amino acids in auxiliary replicase protein p27 critical for its RNA-binding activity and the assembly of the replicase complex in Red clover necrotic mosaic virus. Virology 413:300 -309.
53. Sarawaneeyaruk S, Iwakawa HO, Mizumoto H, Murakami H, Kaido M, Mise K, Okuno T. 2009. Host-dependent roles of the viral 5= untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3= UTR of Red clover necrotic mosaic virus RNA1. Virology 391:107-118.
54. Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T. 2003. Capindependent translational enhancement by the 3= untranslated region of red clover necrotic mosaic virus RNA1. J. Virol. 77:12113-12121.
55. Coemans B, Takahashi Y, Berberich T, Ito A, Kanzaki H, Matsumura H, Saitoh H, Tsuda S, Kamoun S, Sági L, Swennen R, Terauchi R. 2008. High-throughput in planta expression screening identifies an ADPribosylation factor (ARF1) involved in non-host resistance and R genemediated resistance. Mol. Plant Pathol. 9:25-36.
56. Ratcliff F, Martin-Hernandez AM, Baulcombe DC. 2001. Technical advance. Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J. 25:237-245.
57. Mine A, Hyodo K, Takeda A, Kaido M, Mise K, Okuno T. 2010. Interactions between p27 and p88 replicase proteins of Red clover necrotic mosaic virus play an essential role in viral RNA replication and suppression of RNA silencing via the 480-kDa viral replicase complex assembly. Virology 407:213-224.
58. Takeuchi M, Ueda T, Sato K, Abe H, Nagata T, Nakano A. 2000. A dominant negative mutant of Sar1 GTPase inhibits protein transport from the endoplasmic reticulum to the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 23:517-525.
59. Carette JE, Stuiver M, Van Lent J, Wellink J, Van Kammen A. 2000. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J. Virol. 74:6556-6563.
60. Taniguchi T, Kido S, Yamauchi E, Abe M, Matsumoto T, Taniguchi H. 2010. Induction of endosomal/lysosomal pathways in differentiating osteoblasts as revealed by combined proteomic and transcriptomic analyses. FEBS Lett. 584:3969 -3974.
61. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
62. Komoda K, Naito S, Ishikawa M. 2004. Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc. Natl. Acad. Sci. U.S.A. 101:1863-1867.
63. Cui X, Wei T, Chowda-Reddy RV, Sun G, Wang A. 2010. The Tobacco etch virus P3 protein forms mobile inclusions via the early secretory pathway and traffics along actin microfilaments. Virology 397:56-63.
64. Lee MH, Min MK, Lee YJ, Jin JB, Shin DH, Kim DH, Lee KH, Hwang I. 2002. ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiol. 129:1507-1520.
65. Stefano G, Renna L, Chatre L, Hanton SL, Moreau P, Hawes C, Brandizzi F. 2006. In tobacco leaf epidermal cells, the integrity of protein export from the endoplasmic reticulum and of ER export sites depends on active COPI machinery. Plant J. 46:95-110.
66. Takeuchi M, Ueda T, Yahara N, Nakano A. 2002. Arf1 GTPase plays roles in the protein traffic between the endoplasmic reticulum and the Golgi apparatus in tobacco and Arabidopsis cultured cells. Plant J. 31: 499-515.
67. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C. 1998. Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J. 15:441- 447.
68. Nebenführ A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA. 1999. Stop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system. Plant Physiol. 121: 1127-1142.
69. Saint-Jore CM, Evins J, Batoko H, Brandizzi F, Moore I, Hawes C. 2002. Redistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks. Plant J. 29:661- 678.
70. Xu J, Scheres B. 2005. Dissection of Arabidopsis ADP-ribosylation factor 1 function in epidermal cell polarity. Plant Cell 17:525-536.
71. Iwakawa HO, Tajima Y, Taniguchi T, Kaido M, Mise K, Tomari Y, Taniguchi H, Okuno T. 2012. Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral RNA by binding to the 3= untranslated region. J. Virol. 86:7836 -7849.
72. Pucadyil TJ, Schmid SL. 2009. Conserved functions of membrane active GTPases in coated vesicle formation. Science 325:1217-1220.
73. daSilva LL, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, Brandizzi F. 2004. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16:1753- 1771.
74. Marti L, Fornaciari S, Renna L, Stefano G, Brandizzi F. 2010. COPIImediated traffic in plants. Trends Plant Sci. 15:522-528.
75. Yang YD, Elamawi R, Bubeck J, Pepperkok R, Ritzenthaler C, Robinson DG. 2005. Dynamics of COPII vesicles and the Golgi apparatus in cultured Nicotiana tabacum BY-2 cells provides evidence for transient association of Golgi stacks with endoplasmic reticulum exit sites. Plant Cell 17:1513-1531.
76. Hanton SL, Chatre L, Matheson LA, Rossi M, Held MA, Brandizzi F. 2008. Plant Sar1 isoforms with near-identical protein sequences exhibit different localisations and effects on secretion. Plant Mol. Biol. 67:283- 294.
77. Donaldson JG, Jackson CL. 2011. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12:362-375.
78. Altan-Bonnet N, Balla T. 2012. Phosphatidylinositol 4-kinases: hostages harnessed to build panviral replication platforms. Trends Biochem. Sci. 37:293-302.
79. Brown HA, Gutowski S, Moomaw CR, Slaughter C, Sternweis PC. 1993. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity. Cell 75:1137-1144.
80. Beck R, Sun Z, Adolf F, Rutz C, Bassler J, Wild K, Sinning I, Hurt E, Brügger B, Bëthune J, Wieland F. 2008. Membrane curvature induced by Arf1-GTP is essential for vesicle formation. Proc. Natl. Acad. Sci. U.S.A. 105:11731-11736.
81. Krauss M, Jia JY, Roux A, Beck R, Wieland FT, De Camilli P, Haucke V. 2008. Arf1-GTP-induced tubule formation suggests a function of Arf family proteins in curvature acquisition at sites of vesicle budding. J. Biol. Chem. 283:27717-27723.
82. Oostra M, te Lintelo EG, Deijs M, Verheije MH, Rottier PJ, de Haan CA. 2007. Localization and membrane topology of coronavirus nonstructural protein 4: involvement of the early secretory pathway in replication. J. Virol. 81:12323-12336.
83. Trahey M, Oh HS, Cameron CE, Hay JC. 2012. Poliovirus infection transiently increases COPII vesicle budding. J. Virol. 86:9675-9682.
84. Grangeon R, Agbeci M, Chen J, Grondin G, Zheng H, Laliberté JF. 2012. Impact on the endoplasmic reticulum and Golgi apparatus of turnip mosaic virus infection. J. Virol. 86:9255-9265.
85. Tilsner J, Linnik O, Wright KM, Bell K, Roberts AG, Lacomme C, Santa Cruz S, Oparka KJ. 2012. The TGB1 movement protein of Potato virus X reorganizes actin and endomembranes into the X-body, a viral replication factory. Plant Physiol. 158:1359 -1370.
86. Teterina NL, Pinto Y, Weaver JD, Jensen KS, Ehrenfeld E. 2011. Analysis of poliovirus protein 3A interactions with viral and cellular proteins in infected cells. J. Virol. 85:4284-4296.
87. Irurzun A, Perez L, Carrasco L. 1992. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A. Virology 191:166 -175.
88. Sasaki J, Ishikawa K, Arita M, Taniguchi K. 2012. ACBD3-mediated recruitment of PI4KB to picornavirus RNA replication sites. EMBO J. 31:754 -766.
89. Genovés A, Navarro JA, Pallás V. 2010. The intra- and intercellular movement of Melon necrotic spot virus (MNSV) depends on an active secretory pathway. Mol. Plant Microbe Interact. 23:263-272.
90. Ritzenthaler C, Laporte C, Gaire F, Dunoyer P, Schmitt C, Duval S, Piéquet A, Loudes AM, Rohfritsch O, Stussi-Garaud C, Pfeiffer P. 2002. Grapevine fanleaf virus replication occurs on endoplasmic reticulumderived membranes. J. Virol. 76:8808-8819.
91. Serviene E, Jiang Y, Cheng CP, Baker J, Nagy PD. 2006. Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J. Virol. 80:1231-1241.
92. Harries PA, Schoelz JE, Nelson RS. 2010. Intracellular transport of viruses and their components: utilizing the cytoskeleton and membrane highways. Mol. Plant Microbe Interact. 23:1381-1393.