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-Herpesvirus Infection Is Established in Activated B Cells, Dendritic Cells, and Macrophages1
,,,§,§,§
Departments of
*
Immunology and
Virology and Molecular Biology, and
Program in Viral Oncogenesis and Tumor Immunology, St. Jude Children’s Research Hospital, Memphis, TN 38105; and
§
Department of Pathology, University of Tennessee, Memphis, TN 38163
Intranasal infection of mice with the murine 
-herpesvirus MHV-68
results in an acute lytic infection in the lung, followed by the
establishment of lifelong latency. Development of an infectious
mononucleosis-like syndrome correlates with the establishment of
latency and is characterized by splenomegaly and the appearance of
activated CD8+ T cells in the peripheral blood.
Interestingly, a large population of activated CD8+ T cells
in the peripheral blood expresses the Vß4+ element in
their TCR. In this report we show that MHV-68 latency in the spleen
after intranasal infection is harbored in three APC types: B cells,
macrophages, and dendritic cells. Surprisingly, since latency has not
previously been described in dendritic cells, these cells harbored the
highest frequency of latent virus. Among B cells, latency was
preferentially associated with activated B cells expressing the
phenotype of germinal center B cells, thus formally linking the
previously reported association of latency gene expression and germinal
centers to germinal center B cells. Germinal center formation, however,
was not required for the establishment of latency. Significantly,
although three cell types were latently infected, the ability to
stimulate Vß4+CD8+ T cell hybridomas was
limited to latently infected, activated B cells.
This article has been cited by other articles:
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J. S. May, J. Walker, S. Colaco, and P. G. Stevenson The Murine Gammaherpesvirus 68 ORF27 Gene Product Contributes to Intercellular Viral Spread J. Virol., April 15, 2005; 79(8): 5059 - 5068. [Abstract] [Full Text] [PDF]
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D. O. Willer and S. H. Speck Establishment and Maintenance of Long-Term Murine Gammaherpesvirus 68 Latency in B Cells in the Absence of CD40 J. Virol., March 1, 2005; 79(5): 2891 - 2899. [Abstract] [Full Text] [PDF]
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J. Herskowitz, M. A. Jacoby, and S. H. Speck The Murine Gammaherpesvirus 68 M2 Gene Is Required for Efficient Reactivation from Latently Infected B Cells J. Virol., February 15, 2005; 79(4): 2261 - 2273. [Abstract] [Full Text] [PDF]
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D. C. Braaten, R. L. Sparks-Thissen, S. Kreher, S. H. Speck, and H. W. Virgin IV An Optimized CD8+ T-Cell Response Controls Productive and Latent Gammaherpesvirus Infection J. Virol., February 15, 2005; 79(4): 2573 - 2583. [Abstract] [Full Text] [PDF]
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B. D. de Lima, J. S. May, S. Marques, J. P. Simas, and P. G. Stevenson Murine gammaherpesvirus 68 bcl-2 homologue contributes to latency establishment in vivo J. Gen. Virol., January 1, 2005; 86(1): 31 - 40. [Abstract] [Full Text] [PDF]
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F. B. Lopes, S. Colaco, J. S. May, and P. G. Stevenson Characterization of Murine Gammaherpesvirus 68 Glycoprotein B J. Virol., December 1, 2004; 78(23): 13370 - 13375. [Abstract] [Full Text] [PDF]
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X. Liang, Y. C. Shin, R. E. Means, and J. U. Jung Inhibition of Interferon-Mediated Antiviral Activity by Murine Gammaherpesvirus 68 Latency-Associated M2 Protein J. Virol., November 15, 2004; 78(22): 12416 - 12427. [Abstract] [Full Text] [PDF]
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J. Loh, D. A. Thomas, P. A. Revell, T. J. Ley, and H. W. Virgin IV Granzymes and Caspase 3 Play Important Roles in Control of Gammaherpesvirus Latency J. Virol., November 15, 2004; 78(22): 12519 - 12528. [Abstract] [Full Text] [PDF]
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J. P. Stewart, O. J. Silvia, I. M. D. Atkin, D. J. Hughes, B. Ebrahimi, and H. Adler In Vivo Function of a Gammaherpesvirus Virion Glycoprotein: Influence on B-Cell Infection and Mononucleosis J. Virol., October 1, 2004; 78(19): 10449 - 10459. [Abstract] [Full Text] [PDF]
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H. Deng, J. T. Chu, N.-H. Park, and R. Sun Identification of cis Sequences Required for Lytic DNA Replication and Packaging of Murine Gammaherpesvirus 68 J. Virol., September 1, 2004; 78(17): 9123 - 9131. [Abstract] [Full Text] [PDF]
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T. M. Rickabaugh, H. J. Brown, D. Martinez-Guzman, T.-T. Wu, L. Tong, F. Yu, S. Cole, and R. Sun Generation of a Latency-Deficient Gammaherpesvirus That Is Protective against Secondary Infection J. Virol., September 1, 2004; 78(17): 9215 - 9223. [Abstract] [Full Text] [PDF]
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J. Douglas, B. Dutia, S. Rhind, J. P. Stewart, and S. J. Talbot Expression in a Recombinant Murid Herpesvirus 4 Reveals the In Vivo Transforming Potential of the K1 Open Reading Frame of Kaposi's Sarcoma-Associated Herpesvirus J. Virol., August 15, 2004; 78(16): 8878 - 8884. [Abstract] [Full Text] [PDF]
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J. J. Obar, S. G. Crist, E. K. Leung, and E. J. Usherwood IL-15-Independent Proliferative Renewal of Memory CD8+ T Cells in Latent Gammaherpesvirus Infection J. Immunol., August 15, 2004; 173(4): 2705 - 2714. [Abstract] [Full Text] [PDF]
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R. L. Sparks-Thissen, D. C. Braaten, S. Kreher, S. H. Speck, and H. W. Virgin IV An Optimized CD4 T-Cell Response Can Control Productive and Latent Gammaherpesvirus Infection J. Virol., July 1, 2004; 78(13): 6827 - 6835. [Abstract] [Full Text] [PDF]
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J. S. McClellan, S. A. Tibbetts, S. Gangappa, K. A. Brett, and H. W. Virgin IV Critical Role of CD4 T Cells in an Antibody-Independent Mechanism of Vaccination against Gammaherpesvirus Latency J. Virol., July 1, 2004; 78(13): 6836 - 6845. [Abstract] [Full Text] [PDF]
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B. M. Dutia, D. J. Roy, B. Ebrahimi, B. Gangadharan, S. Efstathiou, J. P. Stewart, and A. A. Nash Identification of a region of the virus genome involved in murine gammaherpesvirus 68-induced splenic pathology J. Gen. Virol., June 1, 2004; 85(6): 1393 - 1400. [Abstract] [Full Text] [PDF]
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D. Verzijl, C. P. Fitzsimons, M. van Dijk, J. P. Stewart, H. Timmerman, M. J. Smit, and R. Leurs Differential Activation of Murine Herpesvirus 68- and Kaposi's Sarcoma-Associated Herpesvirus-Encoded ORF74 G Protein-Coupled Receptors by Human and Murine Chemokines J. Virol., April 1, 2004; 78(7): 3343 - 3351. [Abstract] [Full Text] [PDF]
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E. Flano, C. L. Hardy, I.-J. Kim, C. Frankling, M. A. Coppola, P. Nguyen, D. L. Woodland, and M. A. Blackman T Cell Reactivity during Infectious Mononucleosis and Persistent Gammaherpesvirus Infection in Mice J. Immunol., March 1, 2004; 172(5): 3078 - 3085. [Abstract] [Full Text] [PDF]
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A. C. Townsley, B. M. Dutia, and A. A. Nash The M4 Gene of Murine Gammaherpesvirus Modulates Productive and Latent Infection In Vivo J. Virol., January 15, 2004; 78(2): 758 - 767. [Abstract] [Full Text] [PDF]
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J. J. Obar, S. G. Crist, D. C. Gondek, and E. J. Usherwood Different Functional Capacities of Latent and Lytic Antigen-Specific CD8 T Cells in Murine Gammaherpesvirus Infection J. Immunol., January 15, 2004; 172(2): 1213 - 1219. [Abstract] [Full Text] [PDF]
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J. S. May, H. M. Coleman, B. Smillie, S. Efstathiou, and P. G. Stevenson Forced lytic replication impairs host colonization by a latency-deficient mutant of murine gammaherpesvirus-68 J. Gen. Virol., January 1, 2004; 85(1): 137 - 146. [Abstract] [Full Text] [PDF]
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S. F. Elsawa and K. L. Bost Murine {gamma}-Herpesvirus-68-Induced IL-12 Contributes to the Control of Latent Viral Burden, but Also Contributes to Viral-Mediated Leukocytosis J. Immunol., January 1, 2004; 172(1): 516 - 524. [Abstract] [Full Text] [PDF]
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E. Bortz, J. P. Whitelegge, Q. Jia, Z. H. Zhou, J. P. Stewart, T.-T. Wu, and R. Sun Identification of Proteins Associated with Murine Gammaherpesvirus 68 Virions J. Virol., December 15, 2003; 77(24): 13425 - 13432. [Abstract] [Full Text] [PDF]
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P. Fowler, S. Marques, J. P. Simas, and S. Efstathiou ORF73 of murine herpesvirus-68 is critical for the establishment and maintenance of latency J. Gen. Virol., December 1, 2003; 84(12): 3405 - 3416. [Abstract] [Full Text] [PDF]
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N. J. Moorman, D. O. Willer, and S. H. Speck The Gammaherpesvirus 68 Latency-Associated Nuclear Antigen Homolog Is Critical for the Establishment of Splenic Latency J. Virol., October 1, 2003; 77(19): 10295 - 10303. [Abstract] [Full Text] [PDF]
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D. Martinez-Guzman, T. Rickabaugh, T.-T. Wu, H. Brown, S. Cole, M. J. Song, L. Tong, and R. Sun Transcription Program of Murine Gammaherpesvirus 68 J. Virol., October 1, 2003; 77(19): 10488 - 10503. [Abstract] [Full Text] [PDF]
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A. I. Macrae, E. J. Usherwood, S. M. Husain, E. Flano, I.-J. Kim, D. L. Woodland, A. A. Nash, M. A. Blackman, J. T. Sample, and J. P. Stewart Murid Herpesvirus 4 Strain 68 M2 Protein Is a B-Cell-Associated Antigen Important for Latency but Not Lymphocytosis J. Virol., September 1, 2003; 77(17): 9700 - 9709. [Abstract] [Full Text] [PDF]
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D. O. Willer and S. H. Speck Long-Term Latent Murine Gammaherpesvirus 68 Infection Is Preferentially Found within the Surface Immunoglobulin D-Negative Subset of Splenic B Cells In Vivo J. Virol., August 1, 2003; 77(15): 8310 - 8321. [Abstract] [Full Text] [PDF]
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I.-J. Kim, E. Flano, D. L. Woodland, F. E. Lund, T. D. Randall, and M. A. Blackman Maintenance of Long Term {gamma}-Herpesvirus B Cell Latency Is Dependent on CD40-Mediated Development of Memory B Cells J. Immunol., July 15, 2003; 171(2): 886 - 892. [Abstract] [Full Text] [PDF]
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S. Marques, S. Efstathiou, K. G. Smith, M. Haury, and J. P. Simas Selective Gene Expression of Latent Murine Gammaherpesvirus 68 in B Lymphocytes J. Virol., July 1, 2003; 77(13): 7308 - 7318. [Abstract] [Full Text] [PDF]
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I. V. Pavlova, H. W. Virgin IV, and S. H. Speck Disruption of Gammaherpesvirus 68 Gene 50 Demonstrates that Rta Is Essential for Virus Replication J. Virol., May 15, 2003; 77(10): 5731 - 5739. [Abstract] [Full Text] [PDF]
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L. F. van Dyk, H. W. Virgin IV, and S. H. Speck Maintenance of Gammaherpesvirus Latency Requires Viral Cyclin in the Absence of B Lymphocytes J. Virol., May 1, 2003; 77(9): 5118 - 5126. [Abstract] [Full Text] [PDF]
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E. Flano, I.-J. Kim, J. Moore, D. L. Woodland, and M. A. Blackman Differential {gamma}-Herpesvirus Distribution in Distinct Anatomical Locations and Cell Subsets During Persistent Infection in Mice J. Immunol., April 1, 2003; 170(7): 3828 - 3834. [Abstract] [Full Text] [PDF]
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S. F. Elsawa, W. Taylor, C. C. Petty, I. Marriott, J. V. Weinstock, and K. L. Bost Reduced CTL Response and Increased Viral Burden in Substance P Receptor-Deficient Mice Infected with Murine {gamma}-Herpesvirus 68 J. Immunol., March 1, 2003; 170(5): 2605 - 2612. [Abstract] [Full Text] [PDF]
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H. M. Coleman, B. d. Lima, V. Morton, and P. G. Stevenson Murine Gammaherpesvirus 68 Lacking Thymidine Kinase Shows Severe Attenuation of Lytic Cycle Replication In Vivo but Still Establishes Latency J. Virol., February 15, 2003; 77(4): 2410 - 2417. [Abstract] [Full Text] [PDF]
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K. Blasdell, C. McCracken, A. Morris, A. A. Nash, M. Begon, M. Bennett, and J. P. Stewart The wood mouse is a natural host for Murid herpesvirus 4 J. Gen. Virol., January 1, 2003; 84(1): 111 - 113. [Abstract] [Full Text] [PDF]
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K. K. Jensen, S.-C. Chen, R. W. Hipkin, M. T. Wiekowski, M. A. Schwarz, C.-C. Chou, J. P. Simas, A. Alcami, and S. A. Lira Disruption of CCL21-Induced Chemotaxis In Vitro and In Vivo by M3, a Chemokine-Binding Protein Encoded by Murine Gammaherpesvirus 68 J. Virol., December 6, 2002; 77(1): 624 - 630. [Abstract] [Full Text] [PDF]
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 E. Flano, I.-J. Kim, D. L. Woodland, and M. A. Blackman {gamma}-Herpesvirus Latency Is Preferentially Maintained in Splenic Germinal Center and Memory B Cells J. Exp. Med., November 18, 2002; 196(10): 1363 - 1372. [Abstract] [Full Text] [PDF]
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S. Gangappa, S. B. Kapadia, S. H. Speck, and H. W. Virgin IV Antibody to a Lytic Cycle Viral Protein Decreases Gammaherpesvirus Latency in B-Cell-Deficient Mice J. Virol., October 17, 2002; 76(22): 11460 - 11468. [Abstract] [Full Text] [PDF]
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B. T. Seet and G. McFadden Viral chemokine-binding proteins J. Leukoc. Biol., July 1, 2002; 72(1): 24 - 34. [Abstract] [Full Text] [PDF]
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S. A. Tibbetts, L. F. van Dyk, S. H. Speck, and H. W. Virgin IV Immune Control of the Number and Reactivation Phenotype of Cells Latently Infected with a Gammaherpesvirus J. Virol., June 14, 2002; 76(14): 7125 - 7132. [Abstract] [Full Text] [PDF]
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E. T. Clambey, H. W. Virgin IV, and S. H. Speck Characterization of a Spontaneous 9.5-Kilobase-Deletion Mutant of Murine Gammaherpesvirus 68 Reveals Tissue-Specific Genetic Requirements for Latency J. Virol., June 5, 2002; 76(13): 6532 - 6544. [Abstract] [Full Text] [PDF]
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I.-J. Kim, E. Flano, D. L. Woodland, and M. A. Blackman Antibody-Mediated Control of Persistent {gamma}-Herpesvirus Infection J. Immunol., April 15, 2002; 168(8): 3958 - 3964. [Abstract] [Full Text] [PDF]
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S. Vacheron, S. A. Luther, and H. Acha-Orbea Preferential Infection of Immature Dendritic Cells and B Cells by Mouse Mammary Tumor Virus J. Immunol., April 1, 2002; 168(7): 3470 - 3476. [Abstract] [Full Text] [PDF]
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H. Liu, S. Andreansky, G. Diaz, T. Hogg, and P. C. Doherty Reduced Functional Capacity of CD8+ T Cells Expanded by Post-Exposure Vaccination of {gamma}-Herpesvirus-Infected CD4-Deficient Mice J. Immunol., April 1, 2002; 168(7): 3477 - 3483. [Abstract] [Full Text] [PDF]
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M. A. Jacoby, H. W. Virgin IV, and S. H. Speck Disruption of the M2 Gene of Murine Gammaherpesvirus 68 Alters Splenic Latency following Intranasal, but Not Intraperitoneal, Inoculation J. Virol., February 15, 2002; 76(4): 1790 - 1801. [Abstract] [Full Text] [PDF]
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C. M. Payne, C. J. Heggie, D. G. Brownstein, J. P. Stewart, and J. P. Quinn Role of Tachykinins in the Host Response to Murine Gammaherpesvirus Infection J. Virol., November 1, 2001; 75(21): 10467 - 10471. [Abstract] [Full Text] [PDF]
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A. Bridgeman, P. G. Stevenson, J. P. Simas, and S. Efstathiou A Secreted Chemokine Binding Protein Encoded by Murine Gammaherpesvirus-68 Is Necessary for the Establishment of a Normal Latent Load J. Exp. Med., August 6, 2001; 194(3): 301 - 312. [Abstract] [Full Text] [PDF]
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H. Adler, M. Messerle, and U. H. Koszinowski Virus Reconstituted from Infectious Bacterial Artificial Chromosome (BAC)-Cloned Murine Gammaherpesvirus 68 Acquires Wild-Type Properties In Vivo Only after Excision of BAC Vector Sequences J. Virol., June 15, 2001; 75(12): 5692 - 5696. [Abstract] [Full Text]
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R. Rochford, M. L. Lutzke, R. S. Alfinito, A. Clavo, and R. D. Cardin Kinetics of Murine Gammaherpesvirus 68 Gene Expression following Infection of Murine Cells in Culture and in Mice J. Virol., June 1, 2001; 75(11): 4955 - 4963. [Abstract] [Full Text]
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A. I. Macrae, B. M. Dutia, S. Milligan, D. G. Brownstein, D. J. Allen, J. Mistrikova, A. J. Davison, A. A. Nash, and J. P. Stewart Analysis of a Novel Strain of Murine Gammaherpesvirus Reveals a Genomic Locus Important for Acute Pathogenesis J. Virol., June 1, 2001; 75(11): 5315 - 5327. [Abstract] [Full Text]
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M. N. Wakeling, D. J. Roy, A. A. Nash, and J. P. Stewart Characterization of the murine gammaherpesvirus 68 ORF74 product: a novel oncogenic G protein-coupled receptor J. Gen. Virol., May 1, 2001; 82(5): 1187 - 1197. [Abstract] [Full Text]
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E. J. Usherwood, D. J. Roy, K. Ward, S. L. Surman, B. M. Dutia, M. A. Blackman, J. P. Stewart, and D. L. Woodland Control of Gammaherpesvirus Latency by Latent Antigen-specific CD8+ T Cells J. Exp. Med., September 25, 2000; 192(7): 943 - 952. [Abstract] [Full Text] [PDF]
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 S. R. Sarawar, B. J. Lee, S. K. Reiter, and S. P. Schoenberger Stimulation via CD40 can substitute for CD4 T cell function in preventing reactivation of a latent herpesvirus PNAS, May 22, 2001; 98(11): 6325 - 6329. [Abstract] [Full Text] [PDF]
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S. Gangappa, L. F. van Dyk, T. J. Jewett, S. H. Speck, and H. W. Virgin IV Identification of the In Vivo Role of a Viral bcl-2 J. Exp. Med., April 1, 2002; 195(7): 931 - 940. [Abstract] [Full Text] [PDF]
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