Paleo-immunology: Evidence consistent with insertion of a primordial herpes virus-like element in the origins of acquired immunity

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Dreyfus, David H ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Keren Pharmaceutical   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; DDE RECOMBINASE; RAG1 PROTEIN; RAG2 PROTEIN; RECOMBINASE; RNA INDUCED SILENCING COMPLEX; UNCLASSIFIED DRUG; VIRUS ENZYME; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; RAG 1 PROTEIN; RAG-1 PROTEIN; RAG2 PROTEIN, HUMAN; RIBONUCLEASE H;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; GENE EXPRESSION REGULATION; GENE STRUCTURE; GENETIC RECOMBINATION; HERPES VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOGENETICS; IMMUNOSTIMULATION; INFECTION RESISTANCE; INNATE IMMUNITY; NONHUMAN; PRECAMBRIAN; REGULATORY SEQUENCE; SEA URCHIN; STRUCTURAL HOMOLOGY; TRANSPOSON; VIRUS PARTICLE; B LYMPHOCYTE; CELL LINE; EPSTEIN BARR VIRUS; GENETICS; HERPES SIMPLEX VIRUS; HERPES VIRUS; HUMAN; IMMUNITY; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PALEONTOLOGY; SEQUENCE HOMOLOGY; T LYMPHOCYTE;

ECHINOIDEA; HERPES; HERPESVIRIDAE; VERTEBRATA;

AMINO ACID SEQUENCE; B-LYMPHOCYTES; BASE SEQUENCE; CELL LINE; DNA TRANSPOSABLE ELEMENTS; DNA-BINDING PROTEINS; HERPESVIRIDAE; HERPESVIRUS 4, HUMAN; HOMEODOMAIN PROTEINS; HUMANS; IMMUNITY; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PALEONTOLOGY; RIBONUCLEASE H; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIMPLEXVIRUS; T-LYMPHOCYTES; VDJ RECOMBINASES;

EID: 66749159635     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005778     Document Type: Article

References (69)

1. Tonegawa S (1983) Somatic generation of antibody diversity. Nature 302: 575-581.
2. Dreyfus DH (1992) Evidence suggesting an evolutionary relationship between transposable elements and immune system recombination sequences. Mol Immunol 29: 807-810.
3. Spanopoulou E, Zaitseva F, Wang FH, Santagata S, Baltimore D, et al. (1996) The homeodomain region of Rag-1 reveals the parallel mechanisms of bacterial and V(D)J recombination. Cell 87: 263-276.
4. Jones JM, Gellert M (2004) The taming of a transposon: V(D)J recombination and the immune system. Immunol Rev 200: 233-248.
5. Schatz DG (2004) Antigen receptor genes and the evolution of a recombinase. Semin Immunol 16: 245-256.
6. Kapitonov VV, Jurka J (2005) RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3: e181.
7. Fugmann SD, Messier C, Novack LA, Cameron RA, Rast JP (2006) An ancient evolutionary origin of the Rag1/2 gene locus. Proc Natl Acad Sci U S A 103: 3728-3733.
8. van Gent DC, Mizuuchi K, Gellert M (1996) Similarities between initiation of V(D)J recombination and retroviral integration. Science 271: 1592-1594.
9. Melek M, Jones JM, O'Dea MH, Pais G, Burke TR Jr, et al. (2002) Effect of HIV integrase inhibitors on the RAG1/2 recombinase. Proc Natl Acad Sci U S A 99: 134-137.
10. Hiom K, Melek M, Gellert M (1998) DNA transposition by the RAG1 and RAG2 proteins: a possible source of oncogenic translocations. Cell 94: 463-470.
11. Agrawal A, Eastman QM, Schatz DG (1998) Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system. Nature 394: 744-751.
12. Shih IH, Melek M, Jayaratne ND, Gellert M (2002) Inverse transposition by the RAG1 and RAG2 proteins: role reversal of donor and target DNA. Embo J 21: 6625-6633.
13. Chatterji M, Tsai CL, Schatz DG (2004) New concepts in the regulation of an ancient reaction: transposition by RAG1/RAG2. Immunol Rev 200: 261-271.
14. Brandt VL, Roth DB (2008) G.O.D.'s Holy Grail: discovery of the RAG proteins. J Immunol 180: 3-4.
15. Tsai CL, Schatz DG (2003) Regulation of RAG1/RAG2-mediated transposition by GTP and the C-terminal region of RAG2. Embo J 22: 1922-1930.
16. Swanson PC, Volkmer D, Wang L (2004) Full-length RAG-2, and not full-length RAG-1, specifically suppresses RAG-mediated transposition but not hybrid joint formation or disintegration. J Biol Chem 279: 4034-4044.
17. Dreyfus DH, Kelleher CA, Jones JF, Gelfand EW (1996) Epstein-Barr virus infection of T cells: implications for altered T-lymphocyte activation, repertoire development and autoimmunity. Immunol Rev 152: 89-110.
18. Kuhn-Hallek I, Sage DR, Stein L, Groelle H, Fingeroth JD (1995) Expression of recombination activating genes (RAG-1 and RAG-2) in Epstein-Barr virus-bearing B cells. Blood 85: 1289-1299.
19. Srinivas SK, Sixbey JW (1995) Epstein-Barr virus induction of recombinase-activating genes RAG1 and RAG2. J Virol 69: 8155-8158.
20. Wagner HJ, Scott RS, Buchwald D, Sixbey JW (2004) Peripheral blood lymphocytes express recombination-activating genes 1 and 2 during Epstein-Barr virus-induced infectious mononucleosis. J Infect Dis 190: 979-984.
21. Makhov AM, Taylor DW, Griffith JD (2004) Two-dimensional crystallization of herpes simplex virus type 1 single-stranded DNA-binding protein, ICP8, on a lipid monolayer. Biochim Biophys Acta 1701: 101-108.
22. Mapelli M, Panjikar S, Tucker PA (2005) The crystal structure of the herpes simplex virus 1 ssDNA-binding protein suggests the structural basis for flexible, cooperative single-stranded DNA binding. J Biol Chem 280: 2990-2997.
23. Dreyfus DH (2006) The DDE recombinases: diverse roles in acquired and innate immunity. Ann Allergy Asthma Immunol 97: 567-576; quiz 576-568, 602.
24. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L (2004) Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305: 1434-1437.
25. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, et al. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
26. Dyda F, Hickman AB, Jenkins TM, Engelman A, Craigie R, et al. (1994) Crystal structure of the catalytic domain of HIV-1 integrase: similarity to other polynucleotidyl transferases. Science 266: 1981-1986.
27. Chowdhury SI, Buhk HJ, Ludwig H, Hammerschmidt W (1990) Genomic termini of equine herpesvirus 1. J Virol 64: 873-880.
28. Hammerschmidt W, Sugden B (1990) DNA replication of herpesviruses during the lytic phase of their life-cycles. Mol Biol Med 7: 45-57.
29. Zimmermann J, Hammerschmidt W (1995) Structure and role of the terminal repeats of Epstein-Barr virus in processing and packaging of virion DNA. J Virol 69: 3147-3155.
30. Kolman JL, Kolman CJ, Miller G (1992) Marked variation in the size of genomic plasmids among members of a family of related Epstein-Barr viruses. Proc Natl Acad Sci U S A 89: 7772-7776.
31. Srinivas SK, Sample JT, Sixbey JW (1998) Spontaneous loss of viral episomes accompanying Epstein-Barr virus reactivation in a Burkitt's lymphoma cell line. J Infect Dis 177: 1705-1709.
32. Taylor TJ, Knipe DM (2004) Proteomics of herpes simplex virus replication compartments: association of cellular DNA replication, repair, recombination, and chromatin remodeling proteins with ICP8. J Virol 78: 5856-5866.
33. Delecluse HJ, Hammerschmidt W (2000) The genetic approach to the Epstein-Barr virus: from basic virology to gene therapy. Mol Pathol 53: 270-279.
34. Carey M, Kolman J, Katz DA, Gradoville L, Barberis L, et al. (1992) Transcriptional synergy by the Epstein-Barr virus transactivator ZEBRA. J Virol 66: 4803-4813.
35. Francis AL, Gradoville L, Miller G (1997) Alteration of a single serine in the basic domain of the Epstein-Barr virus ZEBRA protein separates its functions of transcriptional activation and disruption of latency. J Virol 71: 3054-3061.
36. Moody CA, Scott RS, Su T, Sixbey JW (2003) Length of Epstein-Barr virus termini as a determinant of epithelial cell clonal emergence. J Virol 77: 8555-8561.
37. Spain TA, Sun R, Miller G (1997) The locus of Epstein-Barr virus terminal repeat processing is bound with enhanced affinity by Sp1 and Sp3. Virology 237: 137-147.
38. Sun R, Spain TA, Lin SF, Miller G (1997) Sp1 binds to the precise locus of end processing within the terminal repeats of Epstein-Barr virus DNA. J Virol 71: 6136-6143.
39. Paramita DK, Fachiroh J, Artama WT, van Benthem E, Haryana SM, et al. (2007) Native early antigen of Epstein-Barr virus, a promising antigen for diagnosis of nasopharyngeal carcinoma. J Med Virol 79: 1710-1721.
40. Dardari R, Hinderer W, Lang D, Benider A, El Gueddari B, et al. (2001) Antibody responses to recombinant Epstein-Barr virus antigens in nasopharyngeal carcinoma patients: complementary test of ZEBRA protein and early antigens p54 and p138. J Clin Microbiol 39: 3164-3170.
41. Dreyfus DH, Gelfand EW (1999) Comparative analysis of invertebrate Tc6 sequences that resemble the vertebrate V(D)J recombination signal sequences (RSS). Mol Immunol 36: 481-488.
42. Oettinger MA (2004) How to keep V(D)J recombination under control. Immunol Rev 200: 165-181.
43. Reddy YV, Perkins EJ, Ramsden DA (2006) Genomic instability due to V(D)J recombination-associated transposition. Genes Dev 20: 1575-1582.
44. Miller G, El-Guindy A, Countryman J, Ye J, Gradoville L (2007) Lytic cycle switches of oncogenic human gammaherpesviruses(1). Adv Cancer Res 97: 81-109.
45. Feschotte C, Pritham EJ (2007) DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41: 331-368.
46. Feschotte C (2008) Transposable elements and the evolution of regulatory networks. Nat Rev Genet 9: 397-405.
47. Pritham EJ, Putliwala T, Feschotte C (2007) Mavericks, a novel class of giant transposable elements widespread in eukaryotes and related to DNA viruses. Gene 390: 3-17.
48. Hung CH, Liu ST (1999) Characterization of the Epstein-Barr virus BALF2 promoter. J Gen Virol 80(Pt 10): 2747-2750.
49. Menetski JP, Gellert M (1990) V(D)J recombination activity in lymphoid cell lines is increased by agents that elevate cAMP. Proc Natl Acad Sci U S A 87: 9324-9328.
50. Kolman JL, Taylor N, Gradoville L, Countryman J, Miller G (1996) Comparing transcriptional activation and autostimulation by ZEBRA and ZEBRA/c-Fos chimeras. J Virol 70: 1493-1504.
51. Verkoczy L, Ait-Azzouzene D, Skog P, Martensson A, Lang J, et al. (2005) A role for nuclear factor kappa B/rel transcription factors in the regulation of the recombinase activator genes. Immunity 22: 519-531.
52. Verkoczy LK, Martensson AS, Nemazee D (2004) The scope of receptor editing and its association with autoimmunity. Curr Opin Immunol 16: 808-814.
53. Finkel TH, Kubo RT, Cambier JC (1991) T-cell development and transmembrane signaling: changing biological responses through an unchanging receptor. Immunol Today 12: 79-85.
54. Gladow M, Uckert W, Blankenstein T (2004) Dual T cell receptor T cells with two defined specificities mediate tumor suppression via both receptors. Eur J Immunol 34: 1882-1891.
55. Han S, Zheng B, Schatz DG, Spanopoulou E, Kelsoe G (1996) Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 274: 2094-2097.
56. Balmelle N, Zamarreno N, Krangel MS, Hernandez-Munain C (2004) Developmental activation of the TCR alpha enhancer requires functional collaboration among proteins bound inside and outside the core enhancer. J Immunol 173: 5054-5063.
57. Hah C, Kim M, Kim K (2005) Induction of peripheral tolerance in dual TCR T cells: an evidence for non-dominant signaling by one TCR. J Biochem Mol Biol 38: 334-342.
58. de Bruyn Kops A, Knipe DM (1994) Preexisting nuclear architecture defines the intranuclear location of herpesvirus DNA replication structures. J Virol 68: 3512-3526.
59. Chen YM, Knipe DM (1996) A dominant mutant form of the herpes simplex virus ICP8 protein decreases viral late gene transcription. Virology 221: 281-290.
60. Zhou C, Knipe DM (2002) Association of herpes simplex virus type 1 ICP8 and ICP27 proteins with cellular RNA polymerase II holoenzyme. J Virol 76: 5893-5904.
61. Taylor TJ, Knipe DM (2003) C-terminal region of herpes simplex virus ICP8 protein needed for intranuclear localization. Virology 309: 219-231.
62. Uprichard SL, Knipe DM (2003) Conformational changes in the herpes simplex virus ICP8 DNA-binding protein coincident with assembly in viral replication structures. J Virol 77: 7467-7476.
63. Gellert M (2002) V(D)J recombination: RAG proteins, repair factors, and regulation. Annu Rev Biochem 71: 101-132.
64. Jones JM, Gellert M, Yang W (2001) A Ku bridge over broken DNA. Structure 9: 881-884.
65. Lu CP, Posey JE, Roth DB (2008) Understanding how the V(D)J recombinase catalyzes transesterification: distinctions between DNA cleavage and transposition. Nucleic Acids Res 36: 2864-2873.
66. Lu CP, Sandoval H, Brandt VL, Rice PA, Roth DB (2006) Amino acid residues in Rag1 crucial for DNA hairpin formation. Nat Struct Mol Biol 13: 1010-1015.
67. Dreyfus DH, Nagasawa M, Gelfand EW, Ghoda LY (2005) Modulation of p53 activity by IkappaBalpha: evidence suggesting a common phylogeny between NF-kappaB and p53 transcription factors. BMC Immunol 6: 12.
68. Song JJ, Joshua-Tor L (2006) Argonaute and RNA-getting into the groove. Curr Opin Struct Biol 16: 5-11.
69. Dreyfus DH, Jones JF, Gelfand EW (1999) Asymmetric DDE (D35E)-like sequences in the RAG proteins: implications for V(D)J recombination and retroviral pathogenesis. Med Hypotheses 52: 545-549.