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Journal of Virology, January 2002, p. 421-426, Vol. 76, No. 1
0022-538X/01/$04.00+0     DOI: 10.1128/JVI.76.1.421-426.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

Complete Nucleotide Sequence of the Rhesus Lymphocryptovirus: Genetic Validation for an Epstein-Barr Virus Animal Model

Pierre Rivailler,1 Hua Jiang,1 Young-gyu Cho,1 Carol Quink,1 and Fred Wang1*

Department of Medicine, Brigham & Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115

Received 28 June 2001/ Accepted 21 September 2001


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ABSTRACT
 
We sequenced the rhesus lymphocryptovirus (LCV) genome in order to determine its genetic similarity to Epstein-Barr virus (EBV). The rhesus LCV encodes a repertoire identical to that of EBV, with 80 open reading frames, including cellular interleukin-10, bcl-2, and colony-stimulating factor 1 receptor homologues and an equivalent set of viral glycoproteins. The highly conserved rhesus LCV gene repertoire provides a unique animal model for the study of EBV pathogenesis.


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TEXT
 
Epstein-Barr virus (EBV)-related herpesviruses in the same gamma-1, or lymphocryptovirus (LCV), genera are known to naturally infect both Old and New World nonhuman primates, and the biology of these nonhuman LCVs appears indistinguishable from that of EBV (reviewed in reference 35). The potential utility of using Old World LCV as an animal model system was demonstrated by the ability to experimentally infect naive rhesus macaques with rhesus LCVs and reproduce many aspects of acute and persistent EBV infection in humans (20).

Previous studies revealed that Old World LCV genomes are organized in a colinear fashion with EBV and that EBV DNA cross-reacts with viral DNA from simian LCVs (11, 12). Rhesus LCV homologues for most of the EBV latent infection genes have been described (reviewed in reference 35). In virtually every aspect, these rhesus LCV latent infection genes are functionally interchangeable with the EBV genes despite modest degrees of homology (27 to 50% amino acid homology). However, the gene repertoire from the rhesus LCV, or any gamma-1 herpesvirus besides EBV, has not been completely characterized, particularly those genes encoding cellular homologues and viral glycoproteins that are highly relevant for studies in an animal model system. The development of a rhesus LCV genetic system to generate mutant viruses for use in experimental infections and study of molecular pathogenesis in vivo also requires a thorough understanding of the rhesus LCV genome and its sequence as a starting point.

Primary sequence and genome structure of rhesus LCV. Six overlapping cosmid and two plasmid viral DNA clones were isolated from the rhesus LCV-infected B-cell line LCL8664 (Fig. 1A). A shotgun cloning and sequencing strategy was used to derive contiguous sequences from these eight viral DNA clones. The complete rhesus LCV sequence was assembled with a sevenfold average redundancy from 1,500 overlapping sequences of 300 to 800 nucleotides.



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  		FIG. 1. Rhesus LCV genome, ORFs, and homology with EBV ORFs. (A) Overlapping cosmid and plasmid DNA clones used to sequence the rhesus LCV genome. Cosmids were identified from the library by hybridization with the EBV BamHI C (CC1, CD1), BamHI Q (QA15), BamHI L (LV28), BamHI D (DK12), and BamHI A (cos9) DNA fragments. RE1 and TR4 are EcoRI and BamHI fragments, respectively, cloned from Hirt DNA. The nucleotide coordinates for each viral DNA clone are as follows: CD1 (140 to 38,206), CC1 (1,785 to 39,553), QA15 (39,641 to 79,990), LV28 (70,760 to 111,969), DK12 (100,417 to 135,417), Cos9 (116,690 to 157,414), RE1 (156,359 to 166,542), and TR4 (166,175 to 783). An 88-bp gap between the CC1 and QA15 cosmid clones was deduced from four PCR clones amplified from rhesus LCV-infected cell DNA using primers from the CC1 and QA15 sequence. (B) Organization of the rhesus LCV genome. Homologues for the EBV lytic and latent origins of replication (ori-p; 7,511 to 9,357), ori-lyt DL (34,141 to 35,138), ori-lyt DR (138,080 to 139,080), major repeat regions IR1 (12,240 to 29,750), IR2 (33,674 to 34,047), IR3 (89,780 to 90,460), and IR4 (135,263 to 137,761), and terminal repeats (TR; 167,326 to 171,106) are identified in the rhesus LCV genome as shown. (C) Rhesus LCV ORFs and amino acid homology with EBV ORFs. The percent amino acid similarity is shown on the y axis. Latent, immediate-early, early, and late lytic ORFs are in black, dark grey, light grey, and white, respectively. Latent infection genes are identified by name (LMPs, EBERs, EBNAs [E], and BARF0 [A0]). Each lytic infection ORF is identified using the EBV nomenclature for BamHI ORFs. The orientations of the ORFs are shown by the direction of the arrow (i.e., right or left). The EBV BamHI fragment is indicated by the letter within the arrow, and the number of the ORF in the EBV BamHI fragment is given last, e.g., the rhesus LCV BCRF1 homologue is indicated by the rightward C1 arrow with approximately 85% amino acid similarity. (The ECRF4 ORF is the only exception to these abbreviations.) ORFs common to other herpesviruses are shown with a bold outline. The initiator codon for each ORF is positioned accurately, but the ORF size is not drawn to scale.

The rhesus LCV genome contains internal (IR1 to IR4) and terminal repeats (TR) as in EBV (Fig. 1B). The major internal repeat, IR1, contains 5.7 copies of a 3,072-bp motif that is 61.5% homologous to the 3,072-bp BamHI W fragment of the EBV IR1. The rhesus LCV TR consists of a 933-bp motif versus a 538-bp motif in the EBV TR, and there is no significant sequence homology besides a similarly high GC content (75%). Based on 5.7 copies in the major internal repeat and 4 TR copies, the rhesus LCV genome has 171,096 nucleotides (versus 172,231 bp in B95-8 EBV with 11.3 IR1 copies and 4 TR copies), with an overall GC content of 62% (60% for EBV), and 65% overall nucleotide homology with the EBV genome.

ORFs encoded in rhesus LCV. Eighty open reading frames (ORFs) are identified in the rhesus LCV sequence (Fig. 1C, Table 1). Each of the rhesus LCV ORFs has a homologue in EBV, each is located in a similar relative position as in EBV, and every EBV ORF is represented in the rhesus LCV genome. Thus, the rhesus LCV, in contrast to the recently described New World primate marmoset LCV (5), has the same viral gene repertoire as EBV. The average homology among all EBV and rhesus LCV ORFs is 75.6% compared to an average homology of 47.3% between EBV and marmoset LCV ORFs (5). Because of the overall similarity in repertoire and sequence, we have adopted the EBV nomenclature with the prefix rh to identify the rhesus LCV ORFs.


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  		TABLE 1. Rhesus LCV genes and amino acid similarity with EBV ORFsa

Rhesus LCV latent infection genes. Homologues for the rhesus LCV EBV-encoded small RNAs (EBERs), EBNA-LP, two types of EBNA-2, EBNA-1, EBNA-3A, -3B, and -3C, LMP1, LMP2A, and LMP2B have been reported previously (3, 6, 8, 15, 24, 26, 27). The complete rhesus LCV sequence shows that there is also a homologue for the EBV BARF0 open reading frame, with 77% homology, suggesting that the family of EBV BamHI A transcripts expressed during latent infection are also likely to be conserved in the rhesus LCV. The latent infection genes are generally the least well conserved among all rhesus LCV genes (Fig. 1C, Table 1).

Conservation of LCV lytic infection genes. Most of the EBV lytic infection genes have homologues in other herpesviruses due to the conserved mechanisms for herpesvirus replication. These 56 ORFs (24 late, 32 early, and 1 immediate-early lytic infection viral gene product) have an average homology of 82.8% with the rhesus LCV homologues (Fig. 1C, ORFs with bold outline). Fifteen EBV lytic infection ORFs do not have homologues in other herpesviruses, i.e., they are restricted to gamma-1 herpesviruses, and the rhesus LCV homologues for these ORFs have an average homology of 60.3%. These genes have presumably evolved more recently and are generally less well conserved between EBV and rhesus LCV.

ORFs encoding homologues of cellular proteins. Four EBV lytic infection genes are cell gene homologues likely to have been captured because they provide a biologic advantage during EBV infection. These include a viral interleukin-10 (vIL-10; BCRF1), two bcl-2 homologues (BHRF1 and BALF1), and a colony-stimulating factor 1 receptor (CSF-1R) homologue (BARF1) (14, 18, 19, 32). These viral genes are not essential for EBV-induced transformation of B-cell growth and for EBV replication in vitro (7, 18, 33). Rhesus LCV has captured an identical repertoire of cellular homologues. Conservation of these ORFs in the rhesus LCV (73 to 84% homology relative to the EBV proteins) indicates that these cellular homologues provide biologic advantages that are common to both EBV and rhesus LCV infection in their natural hosts.

Viral membrane proteins. Viral membrane proteins are important for cell tropism, as targets for the host immune response, and for pathogenesis of infection in vivo. All 10 EBV ORFs known to encode viral membrane glycoproteins are positionally conserved in the rhesus LCV. Five of these glycoproteins are conserved in all herpesviruses (gB, gH, gL, gM, and gN) and are important for herpesvirus virus assembly, egress, and cell fusion (13, 16, 17, 21). These glycoproteins are well conserved in the rhesus LCV (74 to 90% homology with the EBV glycoproteins). Five glycoproteins are restricted to gammaherpesviruses, and these viral gene products are likely to be important for LCV biology and pathogenesis. Among these, gp350 and gp150 have the lowest degree of homology between EBV and the rhesus LCV, 49.3 and 46.6% homology, respectively. gp350 is the major viral membrane glycoprotein that binds to CR2/CD21 and is a major determinant for EBV’s B-cell tropism (22, 34). gp150 is not essential for EBV replication and infection in vitro (4), suggesting an important role for this glycoprotein during human and rhesus LCV infection in vivo.

The rhesus LCV is only the second completely sequenced genome from the oncogenic LCV genera. The EBV B95-8 strain was the first gamma-1 herpesvirus fully sequenced (2). Portions of several other EBV strains have been sequenced (23, 29). Analysis of an 11-kb DNA sequence from Raji EBV demonstrated that the B95-8 strain is a deletion mutant, missing a duplicated ori-lyt sequence (DR) at the right-hand side of the genome (10, 23, 25). Thus, the rhesus LCV genome is the first complete sequence derived from a prototypical LCV genome.

The identical repertoire of lytic and latent infection genes between EBV and the rhesus LCV demonstrates the close genetic relationship between these two viruses and provides genetic validation that the rhesus LCV is an accurate model for studying EBV pathogenesis. The conservation of a type 1 latency EBNA-1 promoter (28) and the existence of two different rhesus LCV types similar to type 1 and 2 EBV (6) provide further evidence of the biologic and genetic similarities between EBV and the rhesus LCV. Thus, Old World LCVs, such as the rhesus LCV, appear to have evolved very closely in parallel with EBV, whereas New World LCVs, such as the marmoset LCV, appear to have evolved somewhat differently despite the overt biologic similarities (5). Thus, the evolutionary distances between human, Old World, and New World LCVs are similar to the relationships between New World, Old World, and human hosts. Studies in both New and Old World model systems may provide a better understanding of how various viral genes contribute to successful EBV infection and pathogenesis in vivo.

Primates have been touted as important animal model systems for studying human virus infection because of the strong similarities in both the viruses and the natural hosts. To our knowledge, only two other herpesviruses naturally infecting Old World nonhuman primate species have been completely sequenced, rhesus rhadinovirus (RRV) and simian varicella virus (SVV) (1, 9, 30), and both have been proposed as animal models for human herpesvirus infections (31, 36). However, the viral gene repertoire from these two viruses is not identical to their human counterparts, Kaposi’s sarcoma herpesvirus (KSHV) and varicella-zoster virus (VZV). RRV does not encode homologues for the KSHV K3, K5, K7, K8, K8.1, and K12 ORFs (1, 30). In addition, the dihydrofolate reductase (DHFR) homologue is encoded in a different location and the copy numbers of macrophage inflammatory protein and viral interferon regulatory factor homologues are different.

Similarly, the SVV and VZV genomes do not have an identical gene repertoire. SVV does not encode a homologue for the VZV ORF2, a gene with unknown function, and SVV encodes for a novel ORF A that is a truncated form of VZV ORF4 (9). In addition, the average homology of RRV and SVV ORFs with their human herpesvirus counterparts is relatively low, approximately 55%, versus 75% between rhesus LCV and EBV. Thus, the identical gene repertoire and high overall sequence homology make the rhesus LCV a uniquely accurate animal model for studying EBV pathogenesis.


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ACKNOWLEDGMENTS
 
We acknowledge members of the Massachusetts General Hospital DNA Sequencing Core (Harry Orf, Brian Seed, Dan Stetson, and David Levin) and the Brigham & Women’s Hospital Genetics Core (David Beier) for assistance with and performance of high-throughput DNA sequencing. We thank Elliott Kieff for valuable advice.

This work was supported by grants from the U.S. Public Health Service (CA68051) and the American Heart Association.


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FOOTNOTES
 
* Corresponding author. Mailing address: Channing Laboratories, 181 Longwood Ave., Boston, MA 02115. Phone: (617) 525-4258. Fax: (617) 525-4257. E-mail: fwang{at}rics.bwh.harvard.edu. Back


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REFERENCES
 
    1
  1. Alexander, L., L. Denekamp, A. Knapp, M. R. Auerbach, B. Damania, and R. C. Desrosiers. 2000. The primary sequence of rhesus monkey rhadinovirus isolate 26-95: sequence similarities to Kaposi’s sarcoma-associated herpesvirus and rhesus monkey rhadinovirus isolate 17577. J. Virol. 74:3388–3398.[Abstract/Free Full Text]
    2. 2
  2. Baer, R., A. T. Bankier, M. D. Biggin, P. L. Deininger, P. J. Farrell, T. J. Gibson, G. Hatfull, G. S. Hudson, S. C. Satchwell, C. Seguin, et al. 1984. DNA sequence and expression of the B95-8 Epstein-Barr virus genome. Nature 310:207–211.[CrossRef][Medline]
    3. 3
  3. Blake, N. W., A. Moghaddam, P. Rao, A. Kaur, R. Glickman, Y. G. Cho, A. Marchini, T. Haigh, R. P. Johnson, A. B. Rickinson, and F. Wang. 1999. Inhibition of antigen presentation by the glycine/alanine repeat domain is not conserved in simian homologues of Epstein-Barr virus nuclear antigen 1. J. Virol. 73:7381–7389.[Abstract/Free Full Text]
    4. 4
  4. Borza, C. M., and L. M. Hutt-Fletcher. 1998. Epstein-Barr virus recombinant lacking expression of glycoprotein gp150 infects B cells normally but is enhanced for infection of epithelial cells. J. Virol. 72:7577–7582.[Abstract/Free Full Text]
    5. 5
  5. Cho, Y., J. Ramer, P. Rivailler, C. Quink, R. L. Garber, D. R. Beier, and F. Wang. 2001. An Epstein-Barr-related herpesvirus from marmoset lymphomas. Proc. Natl. Acad. Sci. USA 98:1224–1229.[Abstract/Free Full Text]
    6. 6
  6. Cho, Y. G., A. V. Gordadze, P. D. Ling, and F. Wang. 1999. Evolution of two types of rhesus lymphocryptovirus similar to type 1 and type 2 Epstein-Barr virus. J. Virol. 73:9206–9212.[Abstract/Free Full Text]
    7. 7
  7. Cohen, J. I., and K. Lekstrom. 1999. Epstein-Barr virus BARF1 protein is dispensable for B-cell transformation and inhibits alpha interferon secretion from mononuclear cells. J. Virol. 73:7627–7632.[Abstract/Free Full Text]
    8. 8
  8. Franken, M., O. Devergne, M. Rosenzweig, B. Annis, E. Kieff, and F. Wang. 1996. Comparative analysis identifies conserved tumor necrosis factor receptor-associated factor 3 binding sites in the human and simian Epstein-Barr virus oncogene LMP1. J. Virol. 70:7819–7826.[Abstract]
    9. 9
  9. Gray, W. L., B. Starnes, M. W. White, and R. Mahalingam. 2001. The DNA sequence of the simian varicella virus genome. Virology 284:123–130.[CrossRef][Medline]
    10. 10
  10. Hammerschmidt, W., and B. Sugden. 1988. Identification and characterization of oriLyt, a lytic origin of DNA replication of Epstein-Barr virus. Cell 55:427–433.[CrossRef][Medline]
    11. 11
  11. Heller, M., P. Gerber, and E. Kieff. 1982. DNA of herpesvirus pan, a third member of the Epstein-Barr virus-herpesvirus papio group. J. Virol. 41:931–939.[Abstract/Free Full Text]
    12. 12
  12. Heller, M., and E. Kieff. 1981. Colinearity between the DNAs of Epstein-Barr virus and herpesvirus papio. J. Virol. 37:821–826.[Abstract/Free Full Text]
    13. 13
  13. Herrold, R. E., A. Marchini, S. Fruehling, and R. Longnecker. 1996. Glycoprotein 110, the Epstein-Barr virus homolog of herpes simplex virus glycoprotein B, is essential for Epstein-Barr virus replication in vivo. J. Virol. 70:2049–2054.[Abstract]
    14. 14
  14. Hsu, D. H., R. de Waal Malefyt, D. F. Fiorentino, M. N. Dang, P. Vieira, J. de Vries, H. Spits, T. R. Mosmann, and K. W. Moore. 1990. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science 250:830–832.[Abstract/Free Full Text]
    15. 15
  15. Jiang, H., Y. G. Cho, and F. Wang. 2000. Structural, functional, and genetic comparisons of Epstein-Barr virus nuclear antigen 3A, 3B, and 3C homologues encoded by the rhesus lymphocryptovirus. J. Virol. 74:5921–5932.[Abstract/Free Full Text]
    16. 16
  16. Lake, C. M., and L. M. Hutt-Fletcher. 2000. Epstein-barr virus that lacks glycoprotein gN is impaired in assembly and infection. J. Virol. 74:11162–11172.[Abstract/Free Full Text]
    17. 17
  17. Li, Q., S. M. Turk, and L. M. Hutt-Fletcher. 1995. The Epstein-Barr virus (EBV) BZLF2 gene product associates with the gH and gL homologs of EBV and carries an epitope critical to infection of B cells but not of epithelial cells. J. Virol. 69:3987–3994.[Abstract]
    18. 18
  18. Marchini, A., B. Tomkinson, J. I. Cohen, and E. Kieff. 1991. BHRF1, the Epstein-Barr virus gene with homology to Bc12, is dispensable for B-lymphocyte transformation and virus replication. J. Virol. 65:5991–6000.[Abstract/Free Full Text]
    19. 19
  19. Marshall, W. L., C. Yim, E. Gustafson, T. Graf, D. R. Sage, K. Hanify, L. Williams, J. Fingeroth, and R. W. Finberg. 1999. Epstein-Barr virus encodes a novel homolog of the bcl-2 oncogene that inhibits apoptosis and associates with Bax and Bak. J. Virol. 73:5181–5185.[Abstract/Free Full Text]
    20. 20
  20. Moghaddam, A., M. Rosenzweig, D. Lee-Parritz, B. Annis, R. P. Johnson, and F. Wang. 1997. An animal model for acute and persistent Epstein-Barr virus infection. Science 276:2030–2033.[Abstract/Free Full Text]
    21. 21
  21. Molesworth, S. J., C. M. Lake, C. M. Borza, S. M. Turk, and L. M. Hutt-Fletcher. 2000. Epstein-Barr virus gH is essential for penetration of B cells but also plays a role in attachment of virus to epithelial cells. J. Virol. 74:6324–6332.[Abstract/Free Full Text]
    22. 22
  22. Nemerow, G. R., C. Mold, V. K. Schwend, V. Tollefson, and N. R. Cooper. 1987. Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d. J. Virol. 61:1416–1420.[Abstract/Free Full Text]
    23. 23
  23. Parker, B. D., A. Bankier, S. Satchwell, B. Barrell, and P. J. Farrell. 1990. Sequence and transcription of Raji Epstein-Barr virus DNA spanning the B95-8 deletion region. Virology 179:339–346.[CrossRef][Medline]
    24. 24
  24. Peng, R., A. V. Gordadze, E. M. Fuentes Panana, F. Wang, J. Zong, G. S. Hayward, J. Tan, and P. D. Ling. 2000. Sequence and functional analysis of EBNA-LP and EBNA2 proteins from nonhuman primate lymphocryptoviruses. J. Virol. 74:379–389.[Abstract/Free Full Text]
    25. 25
  25. Raab-Traub, N., T. Dambaugh, and E. Kieff. 1980. DNA of Epstein-Barr virus VIII: B95-8, the previous prototype, is an unusual deletion derivative. Cell 22:257–267.[CrossRef][Medline]
    26. 26
  26. Rao, P., H. Jiang, and F. Wang. 2000. Cloning of the rhesus lymphocryptovirus viral capsid antigen and epstein-barr virus-encoded small RNA homologues and use in diagnosis of acute and persistent infections. J. Clin. Microbiol. 38:3219–3225.[Abstract/Free Full Text]
    27. 27
  27. Rivailler, P., C. Quink, and F. Wang. 1999. Strong selective pressure for evolution of an Epstein-Barr virus LMP2B homologue in the rhesus lymphocryptovirus. J. Virol. 73:8867–8872.[Abstract/Free Full Text]
    28. 28
  28. Ruf, I. K., A. Moghaddam, F. Wang, and J. Sample. 1999. Mechanisms that regulate Epstein-Barr virus EBNA-1 gene transcription during restricted latency are conserved among lymphocryptoviruses of Old World primates. J. Virol. 73:1980–1989.[Abstract/Free Full Text]
    29. 29
  29. Sample, J., L. Young, B. Martin, T. Chatman, E. Kieff, and A. Rickinson. 1990. Epstein-Barr virus types 1 and 2 differ in their EBNA-3A, EBNA-3B, and EBNA-3C genes. J. Virol. 64:4084–4092.[Abstract/Free Full Text]
    30. 30
  30. Searles, R. P., E. P. Bergquam, M. K. Axthelm, and S. W. Wong. 1999. Sequence and genomic analysis of a Rhesus macaque rhadinovirus with similarity to Kaposi’s sarcoma-associated herpesvirus/human herpesvirus 8. J. Virol. 73:3040–3053.[Abstract/Free Full Text]
    31. 31
  31. Soike, K. F. 1992. Simian varicella virus infection in African and Asian monkeys: the potential for development of antivirals for animal diseases. Ann. N. Y. Acad. Sci. 653:323–333.[Medline]
    32. 32
  32. Strockbine, L. D., J. I. Cohen, T. Farrah, S. D. Lyman, F. Wagener, R. F. DuBose, R. J. Armitage, and M. K. Spriggs. 1998. The Epstein-Barr virus BARF1 gene encodes a novel, soluble colony-stimulating factor-1 receptor. J. Virol. 72:4015–4021.[Abstract/Free Full Text]
    33. 33
  33. Swaminathan, S., R. Hesselton, J. Sullivan, and E. Kieff. 1993. Epstein-Barr virus recombinants with specifically mutated BCRF1 genes. J. Virol. 67:7406–7413.[Abstract/Free Full Text]
    34. 34
  34. Tanner, J., J. Weis, D. Fearon, Y. Whang, and E. Kieff. 1987. Epstein-Barr virus gp350/220 binding to the B lymphocyte C3d receptor mediates adsorption, capping, and endocytosis. Cell 50:203–213.[CrossRef][Medline]
    35. 35
  35. Wang, F., P. Rivailler, P. Rao, and Y. Cho. 2001. Simian homologues of Epstein-Barr virus. Phil. Trans. R. Soc. Lond. B Biol. Sci. 356:489–497.[Abstract/Free Full Text]
    36. 36
  36. Wong, S. W., E. P. Bergquam, R. M. Swanson, F. W. Lee, S. M. Shiigi, N. A. Avery, J. W. Fanton, and M. K. Axthelm. 1999. Induction of B cell hyperplasia in simian immunodeficiency virus-infected rhesus macaques with the simian homologue of Kaposi’s sarcoma-associated herpesvirus. J. Exp. Med. 190:827–840.[Abstract/Free Full Text]

Journal of Virology, January 2002, p. 421-426, Vol. 76, No. 1
0022-538X/01/$04.00+0     DOI: 10.1128/JVI.76.1.421-426.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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  • Chen, A., Zhao, B., Kieff, E., Aster, J. C., Wang, F. (2006). EBNA-3B- and EBNA-3C-Regulated Cellular Genes in Epstein-Barr Virus-Immortalized Lymphoblastoid Cell Lines.. J. Virol. 80: 10139-10150 [Abstract] [Full Text]  
  • Fogg, M. H., Garry, D., Awad, A., Wang, F., Kaur, A. (2006). The BZLF1 Homolog of an Epstein-Barr-Related {gamma}-Herpesvirus Is a Frequent Target of the CTL Response in Persistently Infected Rhesus Macaques. J. Immunol. 176: 3391-3401 [Abstract] [Full Text]  
  • Fogg, M. H., Kaur, A., Cho, Y.-G., Wang, F. (2005). The CD8+ T-Cell Response to an Epstein-Barr Virus-Related Gammaherpesvirus Infecting Rhesus Macaques Provides Evidence for Immune Evasion by the EBNA-1 Homologue. J. Virol. 79: 12681-12691 [Abstract] [Full Text]  
  • Wu, L., Borza, C. M., Hutt-Fletcher, L. M. (2005). Mutations of Epstein-Barr Virus gH That Are Differentially Able To Support Fusion with B Cells or Epithelial Cells. J. Virol. 79: 10923-10930 [Abstract] [Full Text]  
  • Maruo, S., Johannsen, E., Illanes, D., Cooper, A., Zhao, B., Kieff, E. (2005). Epstein-Barr Virus Nuclear Protein 3A Domains Essential for Growth of Lymphoblasts: Transcriptional Regulation through RBP-J{kappa}/CBF1 Is Critical. J. Virol. 79: 10171-10179 [Abstract] [Full Text]  
  • Fogg, M. H., Carville, A., Cameron, J., Quink, C., Wang, F. (2005). Reduced Prevalence of Epstein-Barr Virus-Related Lymphocryptovirus Infection in Sera from a New World Primate. J. Virol. 79: 10069-10072 [Abstract] [Full Text]  
  • Chiou, S.-H., Chow, K.-C., Yang, C.-H., Chiang, S.-F., Lin, C.-H. (2005). Discovery of Epstein-Barr virus (EBV)-encoded RNA signal and EBV nuclear antigen leader protein DNA sequence in pet dogs. J. Gen. Virol. 86: 899-905 [Abstract] [Full Text]  
  • McGeoch, D. J., Gatherer, D., Dolan, A. (2005). On phylogenetic relationships among major lineages of the Gammaherpesvirinae. J. Gen. Virol. 86: 307-316 [Abstract] [Full Text]  
  • Rivailler, P., Carville, A., Kaur, A., Rao, P., Quink, C., Kutok, J. L., Westmoreland, S., Klumpp, S., Simon, M., Aster, J. C., Wang, F. (2004). Experimental rhesus lymphocryptovirus infection in immunosuppressed macaques: an animal model for Epstein-Barr virus pathogenesis in the immunosuppressed host. Blood 104: 1482-1489 [Abstract] [Full Text]  
  • Kutok, J. L., Klumpp, S., Simon, M., MacKey, J. J., Nguyen, V., Middeldorp, J. M., Aster, J. C., Wang, F. (2004). Molecular Evidence for Rhesus Lymphocryptovirus Infection of Epithelial Cells in Immunosuppressed Rhesus Macaques. J. Virol. 78: 3455-3461 [Abstract] [Full Text]  
  • Ehlers, B., Ochs, A., Leendertz, F., Goltz, M., Boesch, C., Matz-Rensing, K. (2003). Novel Simian Homologues of Epstein-Barr Virus. J. Virol. 77: 10695-10699 [Abstract] [Full Text]  
  • Zhao, B., Dalbies-Tran, R., Jiang, H., Ruf, I. K., Sample, J. T., Wang, F., Sample, C. E. (2003). Transcriptional Regulatory Properties of Epstein-Barr Virus Nuclear Antigen 3C Are Conserved in Simian Lymphocryptoviruses. J. Virol. 77: 5639-5648 [Abstract] [Full Text]  
  • Xue, S.-A., Jones, M. D., Lu, Q.-L., Middeldorp, J. M., Griffin, B. E. (2003). Genetic Diversity: Frameshift Mechanisms Alter Coding of a Gene (Epstein-Barr Virus LF3 Gene) That Contains Multiple 102-Base-Pair Direct Sequence Repeats. Mol. Cell. Biol. 23: 2192-2201 [Abstract] [Full Text]  
  • Rivailler, P., Cho, Y.-g., Wang, F. (2002). Complete Genomic Sequence of an Epstein-Barr Virus-Related Herpesvirus Naturally Infecting a New World Primate: a Defining Point in the Evolution of Oncogenic Lymphocryptoviruses. J. Virol. 76: 12055-12068 [Abstract] [Full Text]  
  • Cuconati, A., White, E. (2002). Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection. Genes Dev. 16: 2465-2478 [Full Text]  
  • Jenson, H. B., Ench, Y., Zhang, Y., Gao, S.-J., Arrand, J. R., Mackett, M. (2002). Characterization of an Epstein-Barr virus-related gammaherpesvirus from common marmoset (Callithrix jacchus). J. Gen. Virol. 83: 1621-1633 [Abstract] [Full Text]  

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