SEPTEMBER 2012 • VOLUME 86 • NO. 17

TABLE OF CONTENTS

SPOTLIGHT Articles of Significant Interest Selected from This Issue by the 8919 Editors MINIREVIEW Targeted DNA Mutagenesis for the Cure of Chronic Viral Joshua T. Schiffer, Martine Aubert, 8920–8936 Infections Nicholas D. Weber, Esther Mintzer, Daniel Stone, and Keith R. Jerome STRUCTURE AND ASSEMBLY Cell Culture-Adaptive Mutations Promote Viral Protein-Protein Jieyun Jiang and Guangxiang Luo 8987–8997 Interactions and Morphogenesis of Infectious Hepatitis C Virus

Biochemical Analysis of the Complex between the Tetrameric Janina S. Langner, Nina V. Fuchs, Jan 9079–9087 Export Adapter Protein Rec of HERV-K/HML-2 and the Hoffmann, Alexander Wittmann, Responsive RNA Element RcRE pck30 Bernhard Brutschy, Roswitha Löwer, and Beatrix Suess GENOME REPLICATION AND REGULATION OF VIRAL GENE EXPRESSION Drosophila melanogaster as a Model Organism for Bluetongue Andrew E. Shaw, Eva Veronesi, 9015–9024 Virus Replication and Tropism Guillemette Maurin, Najate Ftaich, Francois Guiguen, Frazer Rixon, Maxime Ratinier, Peter Mertens, Simon Carpenter, Massimo Palmarini, Christophe Terzian, and Frederick Arnaud

Hepatitis D Virus Isolates with Low Replication and Epithelial- Hsuan Hui Shih, I-Jane Sheen, Chien- 9044–9054 Mesenchymal Transition-Inducing Activity Are Associated with Wei Su, Wei-Li Peng, Ling-Hui Lin, Disease Remission and Jaw-Ching Wu Latent HIV-1 Infection Occurs in Multiple Subsets of Lucy A. McNamara, Janani A. Ganesh, 9337–9350 Hematopoietic Progenitor Cells and Is Reversed by NF-␬B and Kathleen L. Collins Activation Cohesins Repress Kaposi’s Sarcoma-Associated Herpesvirus Horng-Shen Chen, Priyankara 9454–9464 Immediate Early Gene Transcription during Latency Wikramasinghe, Louise Showe, and Paul M. Lieberman Adaptive Changes in Alphavirus mRNA Translation Allowed Iván Ventoso 9484–9494 Colonization of Vertebrate Hosts Identification of Novel T Cell Factor 4 (TCF-4) Binding Sites on Lisa J. Henderson, Srinivas D. 9495–9503 the HIV Long Terminal Repeat Which Associate with TCF-4, Narasipura, Vyacheslav Adarichev, ␤-Catenin, and SMAR1 To Repress HIV Transcription Fatah Kashanchi, and Lena Al-Harthi Reverse Genetics Analysis of Poxvirus Intermediate Robin D. Warren, Catherine A. Cotter, 9514–9519 Transcription Factors and Bernard Moss Human Papillomaviruses Recruit Cellular DNA Repair and Kenric A. Gillespie, Kavi P. Mehta, 9520–9526 Homologous Recombination Factors to Viral Replication Laimonis A. Laimins, and Cary A. Centers Moody

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GENETIC DIVERSITY AND EVOLUTION Reevaluation of the Coding Potential and Proteomic Analysis of Daniel Malouli, Ernesto S. Nakayasu, 8959–8973 the BAC-Derived Rhesus Cytomegalovirus Strain 68-1 Kasinath Viswanathan, David G. Camp II, W. L. William Chang, Peter A. Barry, Richard D. Smith, and Klaus Früh Lineage-Specific Differences between Human and Simian Andrés Finzi, Beatriz Pacheco, Shi-Hua 8974–8986 Immunodeficiency Virus Regulation of gp120 Trimer Xiang, Marie Pancera, Alon Association and CD4 Binding Herschhorn, Liping Wang, Xing Zeng, Anik Desormeaux, Peter D. Kwong, and Joseph Sodroski Bats Worldwide Carry Hepatitis E Virus-Related Viruses That Jan Felix Drexler, Annika Seelen, Victor 9134–9147 Form a Putative Novel Genus within the Family Hepeviridae Max Corman, Adriana Fumie Tateno, Veronika Cottontail, Rodrigo Melim Zerbinati, Florian Gloza-Rausch, Stefan M. Klose, Yaw Adu-Sarkodie, Samuel K. Oppong, Elisabeth K. V. Kalko, Andreas Osterman, Andrea Rasche, Alexander Adam, Marcel A. Müller, Rainer G. Ulrich, Eric M. Leroy, Alexander N. Lukashev, and Christian Drosten Diversity and Relationships of Cocirculating Modern Human Sarah M. McDonald, Allison O. 9148–9162 Rotaviruses Revealed Using Large-Scale Comparative Genomics McKell, Christine M. Rippinger, John K. McAllen, Asmik Akopov, Ewen F. Kirkness, Daniel C. Payne, Kathryn M. Edwards, James D. Chappell, and John T. Patton The First Full-Length Endogenous Hepadnaviruses: Wei Liu, Shaokun Pan, Huijuan Yang, 9510–9513 Identification and Analysis Weiya Bai, Zhongliang Shen, Jing Liu, and Youhua Xie VIRUS-CELL INTERACTIONS Large Ribosomal Protein 4 Increases Efficiency of Viral Lisa Green, Brian Houck-Loomis, 8949–8958 Recoding Sequences Andrew Yueh, and Stephen P. Goff A Nuclear Localization Signal in Herpesvirus Protein VP1-2 Is F. Abaitua, M. Hollinshead, M. Bolstad, 8998–9014 Essential for Infection via Capsid Routing to the Nuclear Pore C. M. Crump, and P. O’Hare Detailed Mapping of Determinants within the Porcine Takele Argaw and Carolyn A. Wilson 9096–9104 Endogenous Retrovirus Envelope Surface Unit Identifies Critical Residues for Human Cell Infection within the Proline-Rich Region HMGB1 Protein Binds to Influenza Virus Nucleoprotein and Dorothée Moisy, Sergiy V. Avilov, Yves 9122–9133 Promotes Viral Replication Jacob, Brid M. Laoide, Xingyi Ge, Florence Baudin, Nadia Naffakh, and Jean-Luc Jestin Impact of VP1-Specific Protein Sequence Motifs on Adeno- Ruth Popa-Wagner, Manvi Porwal, 9163–9174 Associated Virus Type 2 Intracellular Trafficking and Nuclear Michael Kann, Matthias Reuss, Marc Entry Weimer, Luise Florin, and Jürgen A. Kleinschmidt The “Bridge” in the Epstein-Barr Virus Alkaline Exonuclease Daniëlle Horst, Wim P. Burmeister, 9175–9187 Protein BGLF5 Contributes to Shutoff Activity during Ingrid G. J. Boer, Daphne van Leeuwen, Productive Infection Marlyse Buisson, Alexander E. Gorbalenya, Emmanuel J. H. J. Wiertz, and Maaike E. Ressing

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Functional Balance of the Hemagglutinin and Neuraminidase Rui Xu, Xueyong Zhu, Ryan McBride, 9221–9232 Activities Accompanies the Emergence of the 2009 H1N1 Corwin M. Nycholat, Wenli Yu, James Influenza Pandemic C. Paulson, and Ian A. Wilson The PDZ1 and PDZ3 Domains of MAGI-1 Regulate the Eight- Abimbola Olayinka Kolawole, Priyanka 9244–9254 Exon Isoform of the Coxsackievirus and Adenovirus Receptor Sharma, Ran Yan, Kyle Joseph Edward Lewis, Zhigang Xu, Heather Ann Hostetler, and Katherine Julie Diane Ashbourne Excoffon Impact on the Endoplasmic Reticulum and Golgi Apparatus of Romain Grangeon, Maxime Agbeci, 9255–9265 Turnip Mosaic Virus Infection Jun Chen, Gilles Grondin, Huanquan Zheng, and Jean-François Laliberté Characterization of the Early Steps of Human Parvovirus B19 Silva Quattrocchi, Nico Ruprecht, 9274–9284 Infection Claudia Bönsch, Sven Bieli, Christoph Zürcher, Klaus Boller, Christoph Kempf, and Carlos Ros Roles of Cell Signaling Pathways in Cell-to-Cell Contact- Asuka Nanbo, Haruna Terada, 9285–9296 Mediated Epstein-Barr Virus Transmission Kunihiro Kachi, Kenzo Takada, and Tadashi Matsuda Foot-and-Mouth Disease Virus 3C Protease Cleaves NEMO To Dang Wang, Liurong Fang, Kui Li, 9311–9322 Impair Innate Immune Signaling Huijuan Zhong, Jinxiu Fan, Chao Ouyang, Huan Zhang, Erzhen Duan, Rui Luo, Zhongming Zhang, Xiangtao Liu, Huanchun Chen, and Shaobo Xiao Inhibition of Human Cytomegalovirus Immediate-Early Gene Jennifer D. Oduro, Ralf Uecker, 9369–9383 Expression by Cyclin A2-Dependent Kinase Activity Christian Hagemeier, and Lüder Wiebusch Proteome-Wide Overexpression of Host Proteins for Muhammad Shah Nawaz-ul-Rehman, 9384–9395 Identification of Factors Affecting Tombusvirus RNA Natalia Martinez-Ochoa, Helene Pascal, Replication: an Inhibitory Role of Protein Kinase C Zsuzsanna Sasvari, Christin Herbst, Kai Xu, Jannine Baker, Monika Sharma, Alan Herbst, and Peter D. Nagy Entry of Hepatitis B Virus into Immortalized Human Primary Hsiu-Chen Huang, Chun-Chi Chen, 9443–9453 Hepatocytes by Clathrin-Dependent Endocytosis Wen-Cheng Chang, Mi-Hua Tao, and Cheng Huang Quantitative Measurement of Human Papillomavirus Type 16 Ziad Sahab, Sawali R. Sudarshan, 9465–9473 E5 Oncoprotein Levels in Epithelial Cell Lines by Mass Xuefeng Liu, YiYu Zhang, Alexander Spectrometry Kirilyuk, Christopher M. Kamonjoh, Vera Simic, Yuhai Dai, Stephen W. Byers, John Doorbar, Frank A. Suprynowicz, and Richard Schlegel Ovine TRIM5␣ Can Restrict Visna/Maedi Virus P. Jáuregui, H. Crespo, I. Glaria, L. 9504–9509 Luján, A. Contreras, S. Rosati, D. de Andrés, B. Amorena, G. J. Towers, and R. Reina A Common Strategy for Host RNA Degradation by Divergent Marta Maria Gaglia, Sergio 9527–9530 Viruses Covarrubias, Wesley Wong, and Britt A. Glaunsinger CELLULAR RESPONSE TO INFECTION Mammalian Innate Resistance to Highly Pathogenic Avian Rahul K. Nelli, Stephen P. Dunham, 9201–9210 Influenza H5N1 Virus Infection Is Mediated through Reduced Suresh V. Kuchipudi, Gavin A. White, Proinflammation and Infectious Virus Release Belinda Baquero-Perez, Pengxiang Chang, Amir Ghaemmaghami, Sharon M. Brookes, Ian H. Brown, and Kin- Chow Chang

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TRANSFORMATION AND ONCOGENESIS Human T-Cell Leukemia Virus Type 1 (HTLV-1) bZIP Factor Hélène Gazon, Isabelle Lemasson, 9070–9078 Requires Cellular Transcription Factor JunD To Upregulate Nicholas Polakowski, Raymond HTLV-1 Antisense Transcription from the 3= Long Terminal Césaire, Masao Matsuoka, Benoit Repeat Barbeau, Jean-Michel Mesnard, and Jean-Marie Peloponese, Jr. HTLV-1 Tax-Induced Rapid Senescence Is Driven by the Yik-Khuan Ho, Huijun Zhi, Dominic 9474–9483 Transcriptional Activity of NF-␬B and Depends on Chronically DeBiaso, Subha Philip, Hsiu-Ming Activated IKK␣ and p65/RelA Shih, and Chou-Zen Giam GENE DELIVERY Safer, Silencing-Resistant Lentiviral Vectors: Optimization of Sean Knight, Fang Zhang, Uta Mueller- 9088–9095 the Ubiquitous Chromatin-Opening Element through Kuller, Marieke Bokhoven, Abhinav Elimination of Aberrant Splicing Gupta, Thomas Broughton, Sha Sha, Michael N. Antoniou, Christian Brendel, Manuel Grez, Adrian J. Thrasher, Mary Collins, and Yasuhiro Takeuchi

The Threefold Protrusions of Adeno-Associated Virus Type 8 Christina Raupp, Matthias Naumer, 9396–9408 Are Involved in Cell Surface Targeting as Well as Oliver J. Müller, Brittney L. Gurda,, Postattachment Processing Mavis Agbandje-McKenna, and Jürgen A. Kleinschmidt VACCINES AND ANTIVIRAL AGENTS Selected Drugs with Reported Secondary Cell-Differentiating Takao Shishido, Frank Wolschendorf, 9055–9069 Capacity Prime Latent HIV-1 Infection for Reactivation Alexandra Duverger, Frederic Wagner, John Kappes, Jennifer Jones, and Olaf Kutsch Increased Antibody Affinity Confers Broad In Vitro Protection Mridula Rani, Meagan Bolles, Eric F. 9113–9121 against Escape Mutants of Severe Acute Respiratory Syndrome Donaldson, Thomas Van Blarcom, Coronavirus Ralph Baric, Brent Iverson, and George Georgiou DNA Prime-Adenovirus Boost Immunization Induces a Anna D. Kosinska, Lena Johrden, Ejuan 9297–9310 Vigorous and Multifunctional T-Cell Response against Zhang, Melanie Fiedler, Anja Mayer, Hepadnaviral Proteins in the Mouse and Woodchuck Model Oliver Wildner, Mengji Lu, and Michael Roggendorf Intracytoplasmic Trapping of Influenza Virus by a Lipophilic Evelien Vanderlinden, Els Vanstreels, 9416–9431 Derivative of Aglycoristocetin Eline Boons, Wouter ter Veer, Anke Huckriede, Dirk Daelemans, Alfons Van Lommel, Erzsébet Ro˝th, Ferenc Sztaricskai, Pa`l Herczegh, and Lieve Naesens PATHOGENESIS AND IMMUNITY CD8؉ T Cells Use TRAIL To Restrict West Nile Virus Bimmi Shrestha, Amelia K. Pinto, 8937–8948 Pathogenesis by Controlling Infection in Neurons Sharone Green, Irene Bosch, and Michael S. Diamond FOXO3 Regulates the CD8 T Cell Response to a Chronic Viral Jeremy A. Sullivan, Eui Ho Kim, Erin 9025–9034 Infection H. Plisch, and M. Suresh Naturally Occurring Swine Influenza A Virus PB1-F2 Jenni N. Weeks-Gorospe, Heather R. 9035–9043 Phenotypes That Contribute to Superinfection with Gram- Hurtig, Amy R. Iverson, Margaret J. Positive Respiratory Pathogens Schuneman, Richard J. Webby, Jonathan A. McCullers, and Victor C. Huber

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Lethal Monkeypox Virus Infection of CAST/EiJ Mice Is Patricia L. Earl, Jeffrey L. Americo, and 9105–9112 Associated with a Deficient Gamma Interferon Response Bernard Moss Live-Attenuated Lentivirus Immunization Modulates Innate Meritxell Genesca`, Zhong-Min Ma, 9188–9200 Immunity and Inflammation while Protecting Rhesus Macaques Yichuan Wang, Basel Assaf, Huma from Vaginal Simian Immunodeficiency Virus Challenge Qureshi, Linda Fritts, Ying Huang, Michael B. McChesney, and Christopher J. Miller Analysis by Single-Gene Reassortment Demonstrates that the Li Qi, A. Sally Davis, Brett W. Jagger, 9211–9220 1918 Influenza Virus Is Functionally Compatible with a Low- Louis M. Schwartzman, Eleca J. Pathogenicity Avian Influenza Virus in Mice Dunham, John C. Kash, and Jeffery K. Taubenberger

A Human CD4؉ T Cell Epitope in the Influenza Virus Jenny Aurielle B. Babon, John Cruz, 9233–9243 Hemagglutinin Is Cross-Reactive to Influenza A Virus Subtypes Francis A. Ennis, Liusong Yin, and and to Influenza B Virus Masanori Terajima Hepatitis B Virus Nucleocapsid but Not Free Core Antigen Yi-Jiun Lin, Hui-Lin Wu, Ding-Shinn 9266–9273 Controls Viral Clearance in Mice Chen, and Pei-Jer Chen Glycosylation of Simian Immunodeficiency Virus Influences Chie Sugimoto, Shinichiro Nakamura, 9323–9336 Immune-Tissue Targeting during Primary Infection, Leading to Shoko I. Hagen, Yasuko Tsunetsugu- Immunodeficiency or Viral Control Yokota, Francois Villinger, Aftab A. Ansari, Yasuo Suzuki, Naoki Yamamoto, Yoshiyuki Nagai, Louis J. Picker, and Kazuyasu Mori Expansion of Polyfunctional HIV-Specific T Cells upon Brenda De Keersmaecker, Sabine D. 9351–9360 Stimulation with mRNA Electroporated Dendritic Cells in the Allard, Patrick Lacor, Rik Schots, Kris Presence of Immunomodulatory Drugs Thielemans, and Joeri L. Aerts Characterization In Vitro and In Vivo of Pandemic (H1N1) 2009 Tokiko Watanabe, Masaki Imai, Shinji 9361–9368 Influenza Viruses Isolated from Patients Watanabe, Kyoko Shinya, Masato Hatta, Chengjun Li, Gabriele Neumann, Makoto Ozawa, Anthony Hanson, Gongxun Zhong, Satoshi Fukuyama, Eiryo Kawakami, Heather A. Simmons, Daniel Schenkman, Kevin Brunner, Saverio V. Capuano III, Jason T. Weinfurter, Anette Kilander, Susanne G. Dudman, M. Suresh, Olav Hungnes, Thomas C. Friedrich, and Yoshihiro Kawaoka STAT4 Regulates Antiviral Gamma Interferon Responses and Alexandra Svensson, Petra Tunbäck, 9409–9415 Recurrent Disease during Herpes Simplex Virus 2 Infection Inger Nordström, Andrey Shestakov, Leonid Padyukov, and Kristina Eriksson

Pathogenic Consequences of Vaginal Infection with CCR5- Madina Shakirzyanova, Lily Tsai, Wuze 9432–9442

Tropic Simian-Human Immunodeficiency Virus SHIVSF162P3N Ren, Agegneu Gettie, James Blanchard, and Cecilia Cheng-Mayer

GENOME ANNOUNCEMENTS Complete Genome Sequences of Novel Canine Noroviruses in Herman Tse, Susanna K. P. Lau, Wan- 9531–9532 Hong Kong Mui Chan, Garnet K. Y. Choi, Patrick C. Y. Woo, and Kwok-Yung Yuen

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Complete Genome Sequence of a Novel Avian-Like H3N2 Swine Shuo Su, Ji-dang Chen, Hai-tao Qi, 9533 Influenza Virus Discovered in Southern China Wan-jun Zhu, Jie-xiong Xie, Zhen Huang, Li-kai Tan, Wen-bao Qi, and Gui-hong Zhang Papilio polyxenes Densovirus Has an Iteravirus-Like Genome Qian Yu, Ann E. Hajek, Max Bergoin, 9534–9535 Organization and Peter Tijssen Complete Genome Sequence of Porcine Circovirus 2b Strain Xin Yang, Fuwang Chen, Yuhang Cao, 9536 CC1 Daxing Pang, Hongsheng Ouyang, and Linzhu Ren Complete Genome Sequence of Pseudomonas aeruginosa Hee-Won Bae, In-Young Chung, Nuri 9537 Siphophage MP1412 Sim, and You-Hee Cho Complete Genome Sequence of Bacteriophage BC-611 Tomohiro Horiuchi, Makiko Sakka, 9538–9539 Specifically Infecting Enterococcus faecalis Strain NP-10011 Atsushi Hayashi, Takashi Shimada, Tetsuya Kimura, and Kazuo Sakka Genome Sequence of Herpes Simplex Virus 1 Strain McKrae Stuart J. Macdonald, Heba H. Mostafa, 9540–9541 Lynda A. Morrison, and David J. Davido

Complete Genome Sequence of an Avian-Like H4N8 Swine Shuo Su, Wen-bao Qi, Ji-dang Chen, 9542 Influenza Virus Discovered in Southern China Nan Cao, Wan-jun Zhu, Li-guo Yuan, Heng Wang, and Gui-hong Zhang Complete Genome Sequence of a Novel Variant Porcine Lu Wenhui, Wei Zhongyan, Zhang 9543 Reproductive and Respiratory Syndrome Virus (PRRSV) Strain: Guanqun, Li Zhili, Ma JingYun, Xie Evidence for Recombination between Vaccine and Wild-Type Qingmei, Sun Baoli, and Bi Yingzuo PRRSV Strains The Genome of Pieris rapae Granulovirus Bao-Qin Zhang, Ruo-Lin Cheng, Xiao- 9544 Feng Wang, and Chuan-Xi Zhang Complete Genome Sequence of a Novel Vitivirus Isolated from Maher Al Rwahnih, Mysore R. 9545 Grapevine Sudarshana, Jerry K. Uyemoto, and Adib Rowhani Characterization and Complete Genome Sequence of Human Heyuan Geng, Lijin Cui, Zhengde Xie, 9546–9547 Coronavirus NL63 Isolated in China Roujian Lu, Li Zhao, and Wenjie Tan Complete Genome Sequence of an Avian-Origin H3N2 Canine Seong-Jun Park, Hyoung-Joon Moon, 9548–9549 Influenza Virus Isolated from Dogs in South Korea Bo-Kyu Kang, Minki Hong, Woonseong Na, Jeong-Ki Kim, Haryoung Poo, Bong-Kyun Park, and Dae-Sub Song Complete Genome Sequencing of a Novel Newcastle Disease Sean C. Courtney, Dejelia Gomez, 9550 Virus Isolate Circulating in Layer Chickens in the Dominican Leonardo Susta, Nichole Hines, Janice Republic C. Pedersen, Patti J. Miller, and Claudio L. Afonso Complete Genome Sequence of a Highly Prevalent Isolate of Yongwen Luo, Jie Zhang, Xianbo Deng, 9551 Porcine Epidemic Diarrhea Virus in South China Yu Ye, Ming Liao, and Huiying Fan Genome Sequence of a Novel Actinophage PIS136 Isolated from Richa Bajpai, Vishal Soni, Lakshmipathi 9552 a Strain of Saccharomonospora sp. Khandrika, Pramod Kumar Jangir, Rakesh Sharma, and Pushpa Agrawal

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Genome Sequence of a Novel Reassortant H3N2 Avian Influenza Jin Tian, Changhui Zhang, Wenbao Qi, 9553–9554 Virus in Southern China Chenggang Xu, Lihong Huang, Huanan Li, and Ming Liao Complete Genome Sequence of a Novel Pararetrovirus Isolated Junping Han, Leslie L. Domier, Anne 9555 from Soybean Dorrance, and Feng Qu

Cover photograph (Copyright © 2012, American Society for Microbiology. All Rights Reserved.): The type member of the genus Chlorovirus (family Phycodnaviridae)isParamecium bursaria chlorella virus 1, which has a 190-nm diameter quasiicosahedral capsid (red) surrounding a large double-stranded DNA genome (yellow) enclosed in an internal membrane (green). The cryo-electron microscopy reconstruction images (courtesy of Xinzheng Zhang and Michael G. Rossmann of Purdue University) show the initial phase of attachment (left) via a spike structure (purple) from the unique vertex. Once bound, the particle will uncoat (right). The virion inner membrane appears to transition from an asymmetric distribution to a more rounded symmetric state as virus entry progresses. The virion proteome complexity, consisting of 148 virus-encoded proteins and one host-encoded protein, is described in the related article. (See related article in August 2012, vol. 86, no. 16, p. 8821.)