Author's personal copy
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J.,
1990. Basic local alignmentsearch tool. J. Mol. Biol. 215 (3),
403–410.
Ambros, V., Bartel, B., Bartel, D.P., Burge, C.B., Carrington,
J.C., Chen, X., Dreyfuss, G.,Eddy, S.R., Griffiths-Jones, S.,
Marshall, M., Matzke, M., Ruvkun, G., Tuschl, T., 2003.A uniform
system for microRNA annotation. RNA 9 (3), 277–279.
Bartel, D.P., 2004. MicroRNAs: genomics, biogenesis, mechanism,
and function. Cell 116(2), 281–297.
Barth, S., Pfuhl, T., Mamiani, A., Ehses, C., Roemer, K.,
Kremmer, E., Jaker, C., Hock, J.,Meister, G., Grasser, F.A., 2008.
Epstein–Barr virus-encoded microRNA miR-BART2down-regulates the
viral DNA polymerase BALF5. Nucleic Acids Res. 36 (2),666–675.
Bennasser, Y., Le, S.Y., Yeung, M.L., Jeang, K.T., 2004. HIV-1
encoded candidate micro-RNAs and their cellular targets.
Retrovirology 1, 43.
Bideshi, D.K., Renault, S., Stasiak, K., Federici, B.A., Bigot,
Y., 2003. Phylogenetic analysisand possible function of bro-like
genes, a multigene family widespread amonglarge double-stranded DNA
viruses of invertebrates and bacteria. J. Gen. Virol. 84(Pt 9),
2531–2544.
Brennecke, J., Hipfner, D.R., Stark, A., Russell, R.B., Cohen,
S.M., 2003. bantam encodes adevelopmentally regulated microRNA that
controls cell proliferation and regulatesthe proapoptotic gene hid
in Drosophila. Cell 113 (1), 25–36.
Bulet, P., Stocklin, R., Menin, L., 2004. Anti-microbial
peptides: from invertebrates tovertebrates. Immunol. Rev. 198,
169–184.
Cai, X., Lu, S., Zhang, Z., Gonzalez, C.M., Damania, B., Cullen,
B.R., 2005. Kaposi's sarcoma-associated herpesvirus expresses an
array of viral microRNAs in latently infectedcells. Proc. Natl.
Acad. Sci. U. S. A. 102 (15), 5570–5575.
Cai, X., Schafer, A., Lu, S., Bilello, J.P., Desrosiers, R.C.,
Edwards, R., Raab-Traub, N., Cullen,B.R., 2006. Epstein–Barr virus
microRNAs are evolutionarily conserved anddifferentially expressed.
PLoS Pathog. 2 (3), e23.
Cerenius, L., Soderhall, K., 2004. The
prophenoloxidase-activating system in inverte-brates. Immunol. Rev.
198, 116–126.
Chen, C., Ridzon, D.A., Broomer, A.J., Zhou, Z., Lee, D.H.,
Nguyen, J.T., Barbisin, M., Xu, N.L., Mahuvakar, V.R., Andersen,
M.R., Lao, K.Q., Livak, K.J., Guegler, K.J., 2005. Real-time
quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Res.
33 (20),e179.
Didiano, D., Hobert, O., 2006. Perfect seed pairing is not a
generally reliable predictor formiRNA-target interactions. Nat.
Struct. Mol. Biol. 13 (9), 849–851.
Eleftherianos, I., Gokcen, F., Felfoldi, G., Millichap, P.J.,
Trenczek, T.E., Ffrench-Constant,R.H., Reynolds, S.E., 2007. The
immunoglobulin family protein Hemolin mediatescellular immune
responses to bacteria in the insectManduca sexta. Cell. Microbiol.
9(5), 1137–1147.
Enright, A.J., John, B., Gaul, U., Tuschl, T., Sander, C.,
Marks, D.S., 2003. MicroRNA targetsin Drosophila. Genome Biol. 5
(1), R1.
Eveland, A.L., McCarty, D.R., Koch, K.E., 2008. Transcript
profiling by 3′-untranslatedregion sequencing resolves expression
of gene families. Plant Physiol. 146 (1),32–44.
Forman, J.J., Legesse-Miller, A., Coller, H.A., 2008. A search
for conserved sequences incoding regions reveals that the let-7
microRNA targets Dicer within its codingsequence. Proc. Natl. Acad.
Sci. U. S. A. 105 (39), 14879–14884.
Fu, H.J., Zhu, J., Yang, M., Zhang, Z.Y., Tie, Y., Jiang, H.,
Sun, Z.X., Zheng, X.F., 2006. A novelmethod to monitor the
expression of microRNAs. Mol. Biotechnol. 32 (3), 197–204.
Goodman, D., Ollikainen, N., Sholley, C., 2007. Baculovirus
phylogeny based on genomerearrangements. In: Tesler, G., Durand, D.
(Eds.), Comparative Genomics.International Workshop, RECOMB-CG
2007, San Diego, CA, USA, pp. 69–82.
Gottwein, E., Mukherjee, N., Sachse, C., Frenzel, C., Majoros,
W.H., Chi, J.T., Braich, R.,Manoharan, M., Soutschek, J., Ohler,
U., Cullen, B.R., 2007. A viral microRNAfunctions as an orthologue
of cellular miR-155. Nature 450 (7172), 1096–1099.
Griffiths-Jones, S., 2004. The microRNA Registry. Nucleic Acids
Res. 32 (Database issue),D109–11.
Grishok, A., Pasquinelli, A.E., Conte, D., Li, N., Parrish, S.,
Ha, I., Baillie, D.L., Fire, A.,Ruvkun, G., Mello, C.C., 2001.
Genes and mechanisms related to RNA interferenceregulate expression
of the small temporal RNAs that control C. elegansdevelopmental
timing. Cell 106 (1), 23–34.
Gupta, A., Gartner, J.J., Sethupathy, P., Hatzigeorgiou, A.G.,
Fraser, N.W., 2006. Anti-apoptotic function of a microRNA encoded
by the HSV-1 latency-associatedtranscript. Nature 442 (7098),
82–85.
Herniou, E.A., Luque, T., Chen, X., Vlak, J.M., Winstanley, D.,
Cory, J.S., O'Reilly, D.R., 2001.Use of whole genome sequence data
to infer baculovirus phylogeny. J. Virol. 75(17), 8117–8126.
Herniou, E.A., Olszewski, J.A., Cory, J.S., O'Reilly, D.R.,
2003. The genome sequence andevolution of baculoviruses. Annu. Rev.
Entomol. 48, 211–234.
Herniou, E.A., Olszewski, J.A., O'Reilly, D.R., Cory, J.S.,
2004. Ancient coevolution ofbaculoviruses and their insect hosts.
J. Virol. 78 (7), 3244–3251.
Hultmark, D., Steiner, H., Rasmuson, T., Boman, H.G., 1980.
Insect immunity. Purificationand properties of three inducible
bactericidal proteins from hemolymph ofimmunized pupae of
Hyalophora cecropia. Eur. J. Biochem. 106 (1), 7–16.
Humphreys, D.T., Westman, B.J., Martin, D.I., Preiss, T., 2005.
MicroRNAs controltranslation initiation by inhibiting eukaryotic
initiation factor 4E/cap and poly(A)tail function. Proc. Natl.
Acad. Sci. U. S. A. 102 (47), 16961–16966.
Hussain, M., Taft, R.J., Asgari, S., 2008. An insect
virus-encoded microRNA regulates viralreplication. J. Virol. 82
(18), 9164–9170.
Hutvagner, G., McLachlan, J., Pasquinelli, A.E., Balint, E.,
Tuschl, T., Zamore, P.D., 2001. Acellular function for the
RNA-interference enzyme Dicer in the maturation of thelet-7 small
temporal RNA. Science 293 (5531), 834–838.
Jakob, N.J., Muller, K., Bahr, U., Darai, G., 2001. Analysis of
the first complete DNAsequence of an invertebrate iridovirus:
coding strategy of the genome of Chiloiridescent virus. Virology
286 (1), 182–196.
Kang, W., Kurihara, M., Matsumoto, S., 2006. The BRO proteins of
Bombyx morinucleopolyhedrovirus are nucleocytoplasmic shuttling
proteins that utilize theCRM1-mediated nuclear export pathway.
Virology 350 (1), 184–191.
Ketting, R.F., Fischer, S.E., Bernstein, E., Sijen, T., Hannon,
G.J., Plasterk, R.H., 2001. Dicerfunctions in RNA interference and
in synthesis of small RNA involved indevelopmental timing in C.
elegans. Genes Dev. 15 (20), 2654–2659.
Krek, A., Grun, D., Poy, M.N., Wolf, R., Rosenberg, L., Epstein,
E.J., MacMenamin, P., daPiedade, I., Gunsalus, K.C., Stoffel, M.,
Rajewsky, N., 2005. Combinatorial microRNAtarget predictions. Nat.
Genet. 37 (5), 495–500.
Lau, N.C., Lim, L.P., Weinstein, E.G., Bartel, D.P., 2001. An
abundant class of tiny RNAswith probable regulatory roles in
Caenorhabditis elegans. Science 294 (5543),858–862.
Lee, R.C., Feinbaum, R.L., Ambros, V., 1993. The C. elegans
heterochronic gene lin-4 encodessmall RNAs with antisense
complementarity to lin-14. Cell 75 (5), 843–854.
Lee, Y., Jeon, K., Lee, J.T., Kim, S., Kim, V.N., 2002. MicroRNA
maturation: stepwiseprocessing and subcellular localization. EMBO
J. 21 (17), 4663–4670.
Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J.,
Provost, P., Radmark, O., Kim, S.,Kim, V.N., 2003. The nuclear
RNase III Drosha initiates microRNA processing. Nature425 (6956),
415–419.
Lewis, B.P., Burge, C.B., Bartel, D.P., 2005. Conserved seed
pairing, often flanked byadenosines, indicates that thousands of
human genes are microRNA targets. Cell120 (1), 15–20.
Lim, L.P., Glasner, M.E., Yekta, S., Burge, C.B., Bartel, D.P.,
2003. Vertebrate microRNAgenes. Science 299 (5612), 1540.
Lin, S.Y., Johnson, S.M., Abraham, M., Vella, M.C., Pasquinelli,
A., Gamberi, C., Gottlieb, E.,Slack, F.J., 2003. The C. elegans
hunchback homolog, hbl-1, controls temporalpatterning and is a
probable microRNA target. Dev. Cell 4 (5), 639–650.
Liu, C.G., Calin, G.A., Meloon, B., Gamliel, N., Sevignani, C.,
Ferracin, M., Dumitru, C.D.,Shimizu, M., Zupo, S., Dono, M., Alder,
H., Bullrich, F., Negrini, M., Croce, C.M., 2004.An oligonucleotide
microchip for genome-wide microRNA profiling in human andmouse
tissues. Proc. Natl. Acad. Sci. U. S. A. 101 (26), 9740–9744.
Lytle, J.R., Yario, T.A., Steitz, J.A., 2007. Target mRNAs are
repressed as efficiently bymicroRNA-binding sites in the 5′ UTR as
in the 3′ UTR. Proc. Natl. Acad. Sci. U. S. A.104 (23),
9667–9672.
Margulies, M., Egholm, M., Altman, W.E., Attiya, S., Bader,
J.S., Bemben, L.A., Berka, J.,Braverman, M.S., Chen, Y.J., Chen,
Z., Dewell, S.B., Du, L., Fierro, J.M., Gomes, X.V.,Godwin, B.C.,
He, W., Helgesen, S., Ho, C.H., Irzyk, G.P., Jando, S.C., Alenquer,
M.L.,Jarvie, T.P., Jirage, K.B., Kim, J.B., Knight, J.R., Lanza,
J.R., Leamon, J.H., Lefkowitz, S.M.,Lei, M., Li, J., Lohman, K.L.,
Lu, H., Makhijani, V.B., McDade, K.E., McKenna, M.P.,Myers, E.W.,
Nickerson, E., Nobile, J.R., Plant, R., Puc, B.P., Ronan, M.T.,
Roth, G.T.,Sarkis, G.J., Simons, J.F., Simpson, J.W., Srinivasan,
M., Tartaro, K.R., Tomasz, A., Vogt,K.A., Volkmer, G.A., Wang,
S.H., Wang, Y., Weiner, M.P., Yu, P., Begley, R.F., Rothberg,J.M.,
2005. Genome sequencing in microfabricated high-density picolitre
reactors.Nature 437 (7057), 376–380.
Murphy, E., Vanicek, J., Robins, H., Shenk, T., Levine, A.J.,
2008. Suppression ofimmediate-early viral gene expression by
herpesvirus-coded microRNAs: implica-tions for latency. Proc. Natl.
Acad. Sci. U. S. A. 105 (14), 5453–5458.
Nielsen, A.F., Gloggnitzer, J., Martinez, J., 2009. MicroRNAs
cross the line: the battle formRNA stability enters the coding
sequence. Mol. Cell 35 (2), 139–140.
Pfeffer, S., Zavolan, M., Grasser, F.A., Chien, M., Russo, J.J.,
Ju, J., John, B., Enright, A.J.,Marks, D., Sander, C., Tuschl, T.,
2004. Identification of virus-encoded microRNAs.Science 304 (5671),
734–736.
Pfeffer, S., Sewer, A., Lagos-Quintana, M., Sheridan, R.,
Sander, C., Grasser, F.A., van Dyk,L.F., Ho, C.K., Shuman, S.,
Chien, M., Russo, J.J., Ju, J., Randall, G., Lindenbach, B.D.,Rice,
C.M., Simon, V., Ho, D.D., Zavolan, M., Tuschl, T., 2005.
Identification ofmicroRNAs of the herpesvirus family. Nat. Methods
2 (4), 269–276.
Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E.,
Bettinger, J.C., Rougvie, A.E.,Horvitz, H.R., Ruvkun, G., 2000. The
21-nucleotide let-7 RNA regulates develop-mental timing in
Caenorhabditis elegans. Nature 403 (6772), 901–906.
Ro, S., Park, C., Jin, J., Sanders, K.M., Yan, W., 2006. A
PCR-based method for detectionand quantification of small RNAs.
Biochem. Biophys. Res. Commun. 351 (3),756–763.
Rohrmann, G.F., 2008. Baculovirus Molecular Biology. National
Library of Medicine(US), NCBI, Bethesda (MD).
Samols, M.A., Skalsky, R.L., Maldonado, A.M., Riva, A., Lopez,
M.C., Baker, H.V., Renne, R.,2007. Identification of cellular genes
targeted by KSHV-encoded microRNAs. PLoSPathog. 3 (5), e65.
Satoh, D., Horii, A., Ochiai, M., Ashida, M., 1999.
Prophenoloxidase-activating enzyme ofthe silkworm, Bombyx mori.
Purification, characterization, and cDNA cloning. J. Biol.Chem. 274
(11), 7441–7453.
Schwarz, D.S., Tomari, Y., Zamore, P.D., 2004. The RNA-induced
silencing complex is aMg2+-dependent endonuclease. Curr. Biol. 14
(9), 787–791.
Singh, J., Nagaraju, J., 2008. In silico prediction and
characterization of microRNAs fromred flour beetle (Tribolium
castaneum). Insect Mol. Biol. 17 (4), 427–436.
Skalsky, R.L., Samols, M.A., Plaisance, K.B., Boss, I.W., Riva,
A., Lopez, M.C., Baker, H.V.,Renne, R., 2007. Kaposi's
sarcoma-associated herpesvirus encodes an ortholog ofmiR-155. J.
Virol. 81 (23), 12836–12845.
Smith, T.F., Waterman, M.S., 1981. Identification of
commonmolecular subsequences. J.Mol. Biol. 147 (1), 195–197.
Stark, A., Kheradpour, P., Parts, L., Brennecke, J., Hodges, E.,
Hannon, G.J., Kellis, M.,2007a. Systematic discovery and
characterization of fly microRNAs using 12Drosophila genomes.
Genome Res. 17 (12), 1865–1879.
Stark, A., Lin, M.F., Kheradpour, P., Pedersen, J.S., Parts, L.,
Carlson, J.W., Crosby, M.A.,Rasmussen, M.D., Roy, S., Deoras, A.N.,
Ruby, J.G., Brennecke, J., Hodges, E., Hinrichs,A.S., Caspi, A.,
Paten, B., Park, S.W., Han, M.V., Maeder, M.L., Polansky, B.J.,
Robson, B.E., Aerts, S., van Helden, J., Hassan, B., Gilbert, D.G.,
Eastman, D.A., Rice, M., Weir, M.,
127J. Singh et al. / Virology 407 (2010) 120–128
Author's personal copy
Hahn, M.W., Park, Y., Dewey, C.N., Pachter, L., Kent, W.J.,
Haussler, D., Lai, E.C.,Bartel, D.P., Hannon, G.J., Kaufman, T.C.,
Eisen, M.B., Clark, A.G., Smith, D., Celniker,S.E., Gelbart, W.M.,
Kellis, M., 2007b. Discovery of functional elements in 12Drosophila
genomes using evolutionary signatures. Nature 450 (7167),
219–232.
Sullivan, C.S., Ganem, D., 2005a. MicroRNAs and viral infection.
Mol. Cell 20 (1), 3–7.Sullivan, C.S., Ganem, D., 2005b. A
virus-encoded inhibitor that blocks RNA interference
in mammalian cells. J. Virol. 79 (12), 7371–7379.Tabara, H.,
Yigit, E., Siomi, H., Mello, C.C., 2002. The dsRNA binding protein
RDE-4
interacts with RDE-1, DCR-1, and a DExH-box helicase to direct
RNAi in C. elegans.Cell 109 (7), 861–871.
Takemoto, Y., Mitsuhashi, W., Murakami, R., Konishi, H.,
Miyamoto, K., 2008. The N-terminal region of an entomopoxvirus
fusolin is essential for the enhancement ofperoral infection,
whereas the C-terminal region is eliminated in digestive juice.
J.Virol. 82 (24), 12406–12415.
Tang, S., Bertke, A.S., Patel, A.,Wang, K., Cohen, J.I., Krause,
P.R., 2008. Anacutely and latentlyexpressed herpes simplex virus 2
viralmicroRNA inhibits expression of ICP34.5, a viralneurovirulence
factor. Proc. Natl. Acad. Sci. U. S. A. 105 (31), 10931–10936.
Terenius, O., 2008. Hemolin-A lepidopteran anti-viral defense
factor? Dev. Comp.Immunol. 32 (4), 311–316.
Triboulet, R., Mari, B., Lin, Y.L., Chable-Bessia, C.,
Bennasser, Y., Lebrigand, K., Cardinaud,B., Maurin, T., Barbry, P.,
Baillat, V., Reynes, J., Corbeau, P., Jeang, K.T., Benkirane,
M.,2007. Suppression of microRNA-silencing pathway by HIV-1 during
virusreplication. Science 315 (5818), 1579–1582.
Umbach, J.L., Kramer, M.F., Jurak, I., Karnowski, H.W., Coen,
D.M., Cullen, B.R., 2008.MicroRNAs expressed by herpes simplex
virus 1 during latent infection regulateviral mRNAs. Nature 454
(7205), 780–783.
Varkonyi-Gasic, E., Wu, R., Wood, M., Walton, E.F., Hellens,
R.P., 2007. Protocol: a highlysensitive RT-PCR method for detection
and quantification of microRNAs. PlantMethods 3, 12.
Walz, N., Christalla, T., Tessmer, U., Grundhoff, A., 2009. A
global analysis ofevolutionary conservation among known and
predicted gammaherpesvirusmicroRNAs. J. Virol. 84 (2), 716–728.
Wuchty, S., Fontana, W., Hofacker, I.L., Schuster, P., 1999.
Complete suboptimal foldingof RNA and the stability of secondary
structures. Biopolymers 49 (2), 145–165.
Yamakawa, M., Tanaka, H., 1999. Immune proteins and their gene
expression in thesilkworm, Bombyx mori. Dev. Comp. Immunol. 23
(4–5), 281–289.
Yan, X., Mouillet, J.F., Ou, Q., Sadovsky, Y., 2003. A novel
domain within the DEAD-boxprotein DP103 is essential for
transcriptional repression and helicase activity. Mol.Cell. Biol.
23 (1), 414–423.
Yi, R., Qin, Y., Macara, I.G., Cullen, B.R., 2003. Exportin-5
mediates the nuclear export ofpre-microRNAs and short hairpin RNAs.
Genes Dev. 17 (24), 3011–3016.
Yu, X., Zhou, Q., Li, S.C., Luo, Q., Cai, Y., Lin, W.C., Chen,
H., Yang, Y., Hu, S., Yu, J., 2008. Thesilkworm (Bombyx mori)
microRNAs and their expressions in multiple develop-mental stages.
PLoS One 3 (8), e2997.
Zuker, M., Stiegler, P., 1981. Optimal computer folding of large
RNA sequences usingthermodynamics and auxiliary information.
Nucleic Acids Res. 9 (1), 133–148.
128 J. Singh et al. / Virology 407 (2010) 120–128