{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,5]],"date-time":"2026-10-05T02:05:58Z","timestamp":1791165958772,"version":"4.1.0"},"reference-count":21,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"5922","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Science"],"published-print":{"date-parts":[[2009,3,27]]},"abstract":"<jats:p>In the early stages of viral infection, outcomes depend on a race between expansion of infection and the immune response generated to contain it. We combined in situ tetramer staining with in situ hybridization to visualize, map, and quantify relationships between immune effector cells and their targets in tissues. In simian immunodeficiency virus infections in macaques and lymphocytic choriomeningitis virus infections in mice, the magnitude and timing of the establishment of an excess of effector cells versus targets were found to correlate with the extent of control and the infection outcome (i.e., control and clearance versus partial or poor control and persistent infection). This method highlights the importance of the location, timing, and magnitude of the immune response needed for a vaccine to be effective against agents of persistent infection, such as HIV-1.<\/jats:p>","DOI":"10.1126\/science.1168676","type":"journal-article","created":{"date-parts":[[2009,3,26]],"date-time":"2009-03-26T18:18:40Z","timestamp":1238091520000},"page":"1726-1729","source":"Crossref","is-referenced-by-count":166,"title":["Visualizing Antigen-Specific and Infected Cells in Situ Predicts Outcomes in Early Viral Infection"],"prefix":"10.1126","volume":"323","author":[{"given":"Qingsheng","family":"Li","sequence":"first","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pamela J.","family":"Skinner","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sang-Jun","family":"Ha","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lijie","family":"Duan","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teresa L.","family":"Mattila","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron","family":"Hage","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cara","family":"White","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel L.","family":"Barber","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leigh","family":"O'Mara","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter J.","family":"Southern","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cavan S.","family":"Reilly","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"John V.","family":"Carlis","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher J.","family":"Miller","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rafi","family":"Ahmed","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashley T.","family":"Haase","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Medical School, University of Minnesota, Minneapolis, MN 55455, USA."},{"name":"Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, MN55108, USA."},{"name":"Emory Vaccine Center, Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, GA 30322, USA."},{"name":"Immunobiology Section, National Institute of Allergy and Infectious Diseases, Bethesda, MD 20892, USA."},{"name":"Division of Biostatistics, School of Public Health, University of Minnesota, Minneapolis, MN 55455, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_3_1_2_2","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1126\/science.280.5361.227","volume":"280","year":"1998","unstructured":"P. C. Doherty, Science280, 227 (1998).","journal-title":"Science"},{"key":"e_1_3_1_3_2","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.68.7.4650-4655.1994"},{"key":"e_1_3_1_4_2","doi-asserted-by":"crossref","first-page":"5127","DOI":"10.4049\/jimmunol.162.9.5127","volume":"162","year":"1999","unstructured":"M. J. Kurodaet al., J. Immunol.162, 5127 (1999).","journal-title":"J. Immunol."},{"key":"e_1_3_1_5_2","doi-asserted-by":"crossref","first-page":"10096","DOI":"10.1128\/JVI.78.18.10096-10103.2004","volume":"78","year":"2004","unstructured":"M. P. Davenport, R. M. Ribeiro, A. S. Perelson, J. Virol.78, 10096 (2004).","journal-title":"J. Virol."},{"key":"e_1_3_1_6_2","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1038\/nri1706","volume":"5","year":"2005","unstructured":"A. T. Haase, Nat. Rev. Immunol.5, 783 (2005).","journal-title":"Nat. Rev. Immunol."},{"key":"e_1_3_1_7_2","doi-asserted-by":"publisher","DOI":"10.1038\/nm0703-847"},{"key":"e_1_3_1_8_2","doi-asserted-by":"crossref","first-page":"9228","DOI":"10.1128\/JVI.79.14.9228-9235.2005","volume":"79","year":"2005","unstructured":"M. R. Reynoldset al., J. Virol.79, 9228 (2005).","journal-title":"J. Virol."},{"key":"e_1_3_1_9_2","doi-asserted-by":"crossref","first-page":"1148","DOI":"10.1038\/nature03513","volume":"434","year":"2005","unstructured":"Q. Liet al., Nature434, 1148 (2005).","journal-title":"Nature"},{"key":"e_1_3_1_10_2","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1038\/nature03501","volume":"434","year":"2005","unstructured":"J. J. Mattapallilet al., Nature434, 1093 (2005).","journal-title":"Nature"},{"key":"e_1_3_1_11_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.280.5362.427"},{"key":"e_1_3_1_12_2","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1084\/jem.160.2.521","volume":"160","year":"1984","unstructured":"R. Ahmed, A. Salmi, L. D. Butler, J. M. Chiller, M. B. Oldstone, J. Exp. Med.160, 521 (1984).","journal-title":"J. Exp. Med."},{"key":"e_1_3_1_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/JVI.77.8.4911-4927.2003"},{"key":"e_1_3_1_14_2","unstructured":"See supporting material on Science Online."},{"key":"e_1_3_1_15_2","doi-asserted-by":"crossref","first-page":"613","DOI":"10.4049\/jimmunol.165.2.613","volume":"165","year":"2000","unstructured":"P. J. Skinner, M. A. Daniels, C. S. Schmidt, S. C. Jameson, A. T. Haase, J. Immunol.165, 613 (2000).","journal-title":"J. Immunol."},{"key":"e_1_3_1_16_2","doi-asserted-by":"crossref","first-page":"9217","DOI":"10.1128\/JVI.79.14.9217-9227.2005","volume":"79","year":"2005","unstructured":"C. J. Milleret al., J. Virol.79, 9217 (2005).","journal-title":"J. Virol."},{"key":"e_1_3_1_17_2","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1128\/JVI.76.2.875-884.2002","volume":"76","year":"2002","unstructured":"B. R. Motheet al., J. Virol.76, 875 (2002).","journal-title":"J. Virol."},{"key":"e_1_3_1_18_2","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1038\/nature04444","volume":"439","year":"2006","unstructured":"D. L. Barberet al., Nature439, 682 (2006).","journal-title":"Nature"},{"key":"e_1_3_1_19_2","doi-asserted-by":"crossref","first-page":"7340","DOI":"10.1128\/jvi.67.12.7340-7349.1993","volume":"67","year":"1993","unstructured":"M. Matloubian, S. R. Kolhekar, T. Somasundaram, R. Ahmed, J. Virol.67, 7340 (1993).","journal-title":"J. Virol."},{"key":"e_1_3_1_20_2","doi-asserted-by":"crossref","first-page":"1043","DOI":"10.1084\/jem.172.4.1043","volume":"172","year":"1990","unstructured":"M. Matloubian, T. Somasundaram, S. R. Kolhekar, R. Selvakumar, R. Ahmed, J. Exp. Med.172, 1043 (1990).","journal-title":"J. Exp. Med."},{"key":"e_1_3_1_21_2","doi-asserted-by":"crossref","first-page":"15430","DOI":"10.1073\/pnas.0702579104","volume":"104","year":"2007","unstructured":"S. N. Muelleret al., Proc. Natl. Acad. Sci. U.S.A.104, 15430 (2007).","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"e_1_3_1_22_2","unstructured":"We thank the Immunology Core Laboratory and Primate Services Unit of the California National Primate Research Center (CNPRC); D. Lu T. Rourke R. Dizon and B. Vang for technical assistance; J. Sedgewick for assistance in setting up the confocal microscope to capture images of silver grains; D. Masopust for helpful discussion; and C. O'Neill and T. Leonard for help in preparing the manuscript and figures. Supported in part by NIH research grants AI48484 (A.T.H.) AI20048 (R.A.) and AI066314 (C.J.M.); National Center for Research Resources grant RR00169 (CNPRC University of California Davis); and a gift from the James B. Pendleton Charitable Trust (C.J.M.)."}],"container-title":["Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/science.1168676","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,10]],"date-time":"2024-01-10T03:44:12Z","timestamp":1704858252000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/science.1168676"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,3,27]]},"references-count":21,"journal-issue":{"issue":"5922","published-print":{"date-parts":[[2009,3,27]]}},"alternative-id":["10.1126\/science.1168676"],"URL":"https:\/\/doi.org\/10.1126\/science.1168676","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1159878.622527","asserted-by":"object"},{"id-type":"doi","id":"10.3410\/f.1159878.621307","asserted-by":"object"}]},"ISSN":["0036-8075","1095-9203"],"issn-type":[{"value":"0036-8075","type":"print"},{"value":"1095-9203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,3,27]]}}}