Evolution of adaptive immunity from transposable elements combined with innate immune systems

Nature Reviews Genetics

Volumn 16, Issue 3, 2015, Pages 184-192

  Koonin, Eugene V ^a   Krupovic, Mart ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA FRAGMENT; RECOMBINASE; CASB PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; IMMUNOGLOBULIN; TRANSPOSON;

ADAPTIVE IMMUNITY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; EVOLUTION; GENETIC RECOMBINATION; GENOME; IMMUNOGLOBULIN GENE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; REVIEW; TRANSPOSON; VERTEBRATE; ANIMAL; ARCHAEON; BACTERIA; GENETICS; HUMAN; IMMUNOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; VDJ RECOMBINATION;

ANIMALIA; PROKARYOTA; VERTEBRATA;

ADAPTIVE IMMUNITY; ANIMALS; ARCHAEA; BACTERIA; BASE SEQUENCE; BIOLOGICAL EVOLUTION; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI PROTEINS; HUMANS; IMMUNITY, INNATE; IMMUNOGLOBULINS; MOLECULAR SEQUENCE DATA; V(D)J RECOMBINATION;

EID: 84923640664     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3859     Document Type: Review

References (108)

1. Huda, A. & Jordan, I. K. Epigenetic regulation of mammalian genomes by transposable elements. Ann. NY Acad. Sci. 1178, 276-284 (2009).
2. Lopez-Flores, I. & Garrido-Ramos, M. A. The repetitive DNA content of eukaryotic genomes. Genome Dyn. 7, 1-28 (2012).
3. Defraia, C. & Slotkin, R. K. Analysis of retrotransposon activity in plants. Methods Mol. Biol. 1112, 195-210 (2014).
4. Cortez, D., Forterre, P. & Gribaldo, S. A hidden reservoir of integrative elements is the major source of recently acquired foreign genes and ORFans in archaeal and bacterial genomes. Genome Biol. 10, R65 (2009).
5. Makarova, K. S. et al. Dark matter in archaeal genomes: a rich source of novel mobile elements, defense systems and secretory complexes. Extremophiles 18, 877-893 (2014).
6. Casjens, S. Prophages and bacterial genomics: what have we learned so far Mol. Microbiol. 49, 277-300 (2003).
7. Busby, B., Kristensen, D. M. & Koonin, E. V. Contribution of phage-derived genomic islands to the virulence of facultative bacterial pathogens. Environ. Microbiol. 15, 307-312 (2013).
8. Wicker, T. et al. A unified classification system for eukaryotic transposable elements. Nature Rev. Genet. 8, 973-982 (2007).
9. Kapitonov, V. V. & Jurka, J. A universal classification of eukaryotic transposable elements implemented in Repbase. Nature Rev. Genet. 9, 411-412 (2008).
10. Jurka, J., Kapitonov, V. V., Kohany, O. & Jurka, M. V. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genomics Hum Genet 8, 241-259 (2007).
11. Curcio, M. J. & Derbyshire, K. M. The outs and ins of transposition: from mu to kangaroo. Nature Rev. Mol. Cell Biol. 4, 865-877 (2003).
12. Chandler, M. et al. Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nature Rev. Microbiol. 11, 525-538 (2013).
13. Ilyina, T. V. & Koonin, E. V. Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res. 20, 3279-3285 (1992).
14. Krupovic, M. Networks of evolutionary interactions underlying the polyphyletic origin of ssDNA viruses. Curr Opin Virol 3, 578-586 (2013).
15. Goodwin, T. J. & Poulter, R. T. A new group of tyrosine recombinase-encoding retrotransposons. Mol. Biol. Evol. 21, 746-759 (2004).
16. Boocock, M. R. & Rice, P. A. A proposed mechanism for IS607-family serine transposases. Mob. DNA 4, 24 (2013).
17. Weichenrieder, O., Repanas, K. & Perrakis, A. Crystal structure of the targeting endonuclease of the human LINE-1 retrotransposon. Structure 12, 975-986 (2004).
18. Aswad, A. & Katzourakis, A. Paleovirology and virally derived immunity. Trends Ecol. Evol. 27, 627-636 (2012).
19. Feschotte, C. & Gilbert, C. Endogenous viruses: insights into viral evolution and impact on host biology. Nature Rev. Genet. 13, 283-296 (2012).
20. Duggal, N. K. & Emerman, M. Evolutionary conflicts between viruses and restriction factors shape immunity. Nature Rev. Immunol. 12, 687-695 (2012).
21. Forterre, P. & Prangishvili, D. The major role of viruses in cellular evolution: facts and hypotheses. Curr Opin Virol 3, 558-565 (2013).
22. Koonin, E. V. & Dolja, V. V. A virocentric perspective on the evolution of life. Curr Opin Virol 3, 546-557 (2013).
23. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nature Rev. Microbiol. 8, 317-327 (2010).
24. Seed, K. D., Lazinski, D. W., Calderwood, S. B. & Camilli, A. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494, 489-491 (2013).
25. Boehm, T. Evolution of vertebrate immunity. Curr. Biol. 22, R722-732 (2012).
26. Rimer, J., Cohen, I. R. & Friedman, N. Do all creatures possess an acquired immune system of some sort Bioessays 36, 273-281 (2014).
27. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006).
28. Makarova, K. S., Grishin, N. V., Shabalina, S. A., Wolf, Y. I. & Koonin, E. V. A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol. Direct 1, 7 (2006).
29. Makarova, K. S., Wolf, Y. I. & Koonin, E. V. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res. 41, 4360-4377 (2013).
30. Hur, J. K., Olovnikov, I. & Aravin, A. A. Prokaryotic Argonautes defend genomes against invasive DNA. Trends Biochem. Sci. 39, 257-259 (2014).
31. Swarts, D. C. et al. The evolutionary journey of Argonaute proteins. Nature Struct. Mol. Biol. 21, 743-753 (2014).
32. Makarova, K. S. et al. Evolution and classification of the CRISPR-Cas systems. Nature Rev. Microbiol. 9, 467-477 (2011).
33. van der Oost, J., Jore, M. M., Westra, E. R., Lundgren, M. & Brouns, S. J. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34, 401-407 (2009).
34. Wiedenheft, B., Sternberg, S. H. & Doudna, J. A. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482, 331-338 (2012).
35. Sorek, R., Lawrence, C. M. & Wiedenheft, B. CRISPR-mediated adaptive immune systems in bacteria and archaea. Annu. Rev. Biochem. 82, 237-266 (2013).
36. Barrangou, R. & Marraffini, L. A. CRISPR-Cas systems: prokaryotes upgrade to adaptive immunity. Mol. Cell 54, 234-244 (2014).
37. Manica, A. & Schleper, C. CRISPR-mediated defense mechanisms in the hyperthermophilic archaeal genus Sulfolobus. RNA Biol 10, 671-678 (2013).
38. van der Oost, J., Westra, E. R., Jackson, R. N. & Wiedenheft, B. Unravelling the structural and mechanistic basis of CRISPR-Cas systems. Nature Rev. Microbiol. 12, 479-492 (2014).
39. Weinberger, A. D. et al. Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput. Biol. 8, e1002475 (2012).
40. Koonin, E. V. & Wolf, Y. I. Is evolution Darwinian or/and Lamarckian Biol. Direct 4, 42 (2009).
41. Wang, X. H. et al. RNA interference directs innate immunity against viruses in adult Drosophila. Science 312, 452-454 (2006).
42. Shabalina, S. A. & Koonin, E. V. Origins and evolution of eukaryotic RNA interference. Trends Ecol. Evol. 23, 578-587 (2008).
43. Carthew, R. W. & Sontheimer, E. J. Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655 (2009).
44. Zhou, R. & Rana, T. M. RNA-based mechanisms regulating host-virus interactions. Immunol. Rev. 253, 97-111 (2013).
45. Medzhitov, R. Approaching the asymptote: 20 years later. Immunity 30, 766-775 (2009).
46. Kawai, T. & Akira, S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nature Immunol. 11, 373-384 (2010).
47. Malmgaard, L. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24, 439-454 (2004).
48. Le Page, C., Genin, P., Baines, M. G. & Hiscott, J. Interferon activation and innate immunity. Rev Immunogenet 2, 374-386 (2000).
49. Cooper, M. D. & Alder, M. N. The evolution of adaptive immune systems. Cell 124, 815-822 (2006).
50. Boehm, T. Design principles of adaptive immune systems. Nature Rev. Immunol. 11, 307-317 (2011).
51. Davis, M. M. The evolutionary and structural 'logic' of antigen receptor diversity. Semin. Immunol. 16, 239-243 (2004).
52. Cannon, J. P., Haire, R. N., Rast, J. P. & Litman, G. W. The phylogenetic origins of the antigen-binding receptors and somatic diversification mechanisms. Immunol. Rev. 200, 12-22 (2004).
53. Market, E. & Papavasiliou, F. N. V(D)J recombination and the evolution of the adaptive immune system. PLoS Biol. 1, e16 (2003).
54. Jung, D. & Alt, F. W. Unraveling V(D)J recombination; insights into gene regulation. Cell 116, 299-311 (2004).
55. Fugmann, S. D. The origins of the Rag genes-from transposition to V(D)J recombination. Semin. Immunol. 22, 10-16 (2010).
56. Kapitonov, V. V. & Jurka, J. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol. 3, e181 (2005).
57. Krupovic, M., Makarova, K. S., Forterre, P., Prangishvili, D. & Koonin, E. V. Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol. 12, 36 (2014).
58. Nunez, J. K. et al. Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nature Struct. Mol. Biol. 21, 528-534 (2014).
59. Wiedenheft, B. et al. Structural basis for DNase activity of a conserved protein implicated in CRISPR-mediated genome defense. Structure 17, 904-912 (2009).
60. Makarova, K. S., Aravind, L., Wolf, Y. I. & Koonin, E. V. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6, 38 (2011).
61. Makarova, K. S., Wolf, Y. I. & Koonin, E. V. The basic building blocks and evolution of CRISPR-Cas systems. Biochem. Soc. Trans. 41, 1392-1400 (2013).
62. Brouns, S. J. et al. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321, 960-964 (2008).
63. Rouillon, C. et al. Structure of the CRISPR interference complex CSM reveals key similarities with cascade. Mol. Cell 52, 124-134 (2013).
64. Anantharaman, V., Koonin, E. V. & Aravind, L. Comparative genomics and evolution of proteins involved in RNA metabolism. Nucleic Acids Res. 30, 1427-1464 (2002).
65. Anantharaman, V., Aravind, L. & Koonin, E. V. Emergence of diverse biochemical activities in evolutionarily conserved structural scaffolds of proteins. Curr Opin Chem Biol 7, 12-20 (2003).
66. Clery, A., Blatter, M. & Allain, F. H. RNA recognition motifs: boring Not quite. Curr Opin Struct Biol 18, 290-298 (2008).
67. Koonin, E. V. & Makarova, K. S. CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol. 10, 679-686 (2013).
68. Makarova, K. S., Wolf, Y. I., van der Oost, J. & Koonin, E. V. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4, 29 (2009).
69. Olovnikov, I., Chan, K., Sachidanandam, R., Newman, D. K. & Aravin, A. A. Bacterial Argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51, 594-605 (2013).
70. Swarts, D. C. et al. DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507, 258-261 (2014).
71. Beloglazova, N. et al. A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J. Biol. Chem. 283, 20361-20371 (2008).
72. Han, D. & Krauss, G. Characterization of the endonuclease SSO2001 from Sulfolobus solfataricus P2. FEBS Lett. 583, 771-776 (2009).
73. Makarova, K. S., Anantharaman, V., Aravind, L. & Koonin, E. V. Live virus-free or die: coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes. Biol. Direct 7, 40 (2012).
74. Kwon, A. R. et al. Structural and biochemical characterization of HP0315 from Helicobacter pylori as a VapD protein with an endoribonuclease activity. Nucleic Acids Res. 40, 4216-4228 (2012).
75. Unterholzner, S. J., Poppenberger, B. & Rozhon, W. Toxin-antitoxin systems: biology, identification, and application. Mob. Genet. Elements 3, e26219 (2013).
76. Krupovic, M., Gonnet, M., Hania, W. B., Forterre, P. & Erauso, G. Insights into dynamics of mobile genetic elements in hyperthermophilic environments from five new Thermococcus plasmids. PLoS ONE 8, e49044 (2013).
77. Kunin, V., Sorek, R. & Hugenholtz, P. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol. 8, R61 (2007).
78. Datsenko, K. A. et al. Molecular memory of prior infections activates the CRISPR-Cas adaptive bacterial immunity system. Nature Commun. 3, 945 (2012).
79. Yosef, I., Goren, M. G. & Qimron, U. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res. 40, 5569-5576 (2012).
80. Chylinski, K., Le Rhun, A. & Charpentier, E. The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol. 10, 726-737 (2013).
81. Chylinski, K., Makarova, K. S., Charpentier, E. & Koonin, E. V. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res. 42, 6091-6105 (2014).
82. Bao, W. & Jurka, J. Homologues of bacterial TnpB-IS605 are widespread in diverse eukaryotic transposable elements. Mob DNA 4, 12 (2013).
83. Kim, H. & Kim, J. S. A guide to genome engineering with programmable nucleases. Nature Rev. Genet. 15, 321-334 (2014).
84. Tonegawa, S. Somatic generation of antibody diversity. Nature 302, 575-581 (1983).
85. Papavasiliou, F. N. & Schatz, D. G. Somatic hypermutation of immunoglobulin genes: merging mechanisms for genetic diversity. Cell 109, S35-S44 (2002).
86. Oettinger, M. A., Schatz, D. G., Gorka, C. & Baltimore, D. RAG-1 and RAG-2, adjacent genes that synergistically activate V(D)J recombination. Science 248, 1517-1523 (1990).
87. Swanson, P. C. The bounty of RAGs: recombination signal complexes and reaction outcomes. Immunol. Rev. 200, 90-114 (2004).
88. Panchin, Y. & Moroz, L. L. Molluscan mobile elements similar to the vertebrate recombination-activating genes. Biochem. Biophys. Res. Commun. 369, 818-823 (2008).
89. Sakano, H., Huppi, K., Heinrich, G. & Tonegawa, S. Sequences at the somatic recombination sites of immunoglobulin light-chain genes. Nature 280, 288-294 (1979).
90. Thompson, C. B. New insights into V(D)J recombination and its role in the evolution of the immune system. Immunity 3, 531-539 (1995).
91. Roth, D. B. & Craig, N. L. VDJ recombination: a transposase goes to work. Cell 94, 411-414 (1998).
92. Schatz, D. G. Antigen receptor genes and the evolution of a recombinase. Semin. Immunol. 16, 245-256 (2004).
93. Du Pasquier, L. Speculations on the origin of the vertebrate immune system. Immunol. Lett. 92, 3-9 (2004).
94. Du Pasquier, L. Innate immunity in early chordates and the appearance of adaptive immunity. C. R. Biol. 327, 591-601 (2004).
95. Fugmann, S. D., Messier, C., Novack, L. A., Cameron, R. A. & Rast, J. P. An ancient evolutionary origin of the Rag1/2 gene locus. Proc. Natl Acad. Sci. USA 103, 3728-3733 (2006).
96. Hemmrich, G., Miller, D. J. & Bosch, T. C. The evolution of immunity: a low-life perspective. Trends Immunol. 28, 449-454 (2007).
97. Bowen, N. J. & Jordan, I. K. Transposable elements and the evolution of eukaryotic complexity. Curr. Issues Mol. Biol. 4, 65-76 (2002).
98. Kazazian, H. H. Jr. Mobile elements: drivers of genome evolution. Science 303, 1626-1632 (2004).
99. Jordan, I. K., Rogozin, I. B., Glazko, G. V. & Koonin, E. V. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 19, 68-72 (2003).
100. Conley, A. B., Piriyapongsa, J. & Jordan, I. K. Retroviral promoters in the human genome. Bioinformatics 24, 1563-1567 (2008).
101. Jurka, J. Conserved eukaryotic transposable elements and the evolution of gene regulation. Cell. Mol. Life Sci. 65, 201-204 (2008).
102. Nakamura, T. M. & Cech, T. R. Reversing time: origin of telomerase. Cell 92, 587-590 (1998).
103. Gladyshev, E. A. & Arkhipova, I. R. A widespread class of reverse transcriptase-related cellular genes. Proc. Natl Acad. Sci. USA 108, 20311-20316 (2011).
104. Pardue, M. L. & De Baryshe, P. G. Retrotransposons provide an evolutionarily robust non-telomerase mechanism to maintain telomeres. Annu. Rev. Genet. 37, 485-511 (2003).
105. Kapitonov, V. V. & Jurka, J. Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biol. 23, 311-324 (2004).
106. Sinzelle, L. et al. Transposition of a reconstructed Harbinger element in human cells and functional homology with two transposon-derived cellular genes. Proc. Natl Acad. Sci. USA 105, 4715-4720 (2008).
107. Mali, P. et al. RNA-guided human genome engineering via Cas9. Science 339, 823-826 (2013).
108. Sternberg, S. H., Redding, S., Jinek, M., Greene, E. C. & Doudna, J. A. DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507, 62-67 (2014).