Impact of CRISPR immunity on the emergence and virulence of bacterial pathogens

Current Opinion in Microbiology

Volumn 17, Issue 1, 2014, Pages 82-90

  Hatoum Aslan, Asma ^a   Marraffini, Luciano A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL IMMUNITY; BACTERIAL VIRULENCE; CRISPR CAS SYSTEM; ENTEROCOCCUS; FRANCISELLA; NONHUMAN; PATHOGENESIS; PSEUDOMONAS; REVIEW; STAPHYLOCOCCUS; STREPTOCOCCUS GROUP A; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; CRISPR-CAS SYSTEMS; HUMANS; MICE;

EID: 84891113073     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.12.001     Document Type: Review

References (70)

1. Brussow H., Hendrix R.W. Phage genomics: small is beautiful. Cell 2002, 108:13-16.
2. Labrie S.J., Samson J.E., Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010, 8:317-327.
3. Terns M.P., Terns R.M. CRISPR-based adaptive immune systems. Curr Opin Microbiol 2011, 14:321-327.
4. Deveau H., Garneau J.E., Moineau S. CRISPR/Cas system and its role in phage-bacteria interactions. Annu Rev Microbiol 2010, 64:475-493.
5. Westra E.R., Swarts D.C., Staals R.H., Jore M.M., Brouns S.J., van der Oost J. The CRISPRs, they are a-changin': how prokaryotes generate adaptive immunity. Annu Rev Genet 2012, 46:311-339.
6. Barrangou R., Fremaux C., Deveau H., Richards M., Boyaval P., Moineau S., Romero D.A., Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
7. Datsenko K.A., Pougach K., Tikhonov A., Wanner B.L., Severinov K., Semenova E. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 2012, 3:945.
8. Swarts D.C., Mosterd C., van Passel M.W., Brouns S.J. CRISPR interference directs strand specific spacer acquisition. PLoS ONE 2012, 7:e35888.
9. Yosef I., Goren M.G., Qimron U. Proteins and DNA elements essential for the CRISPR adaptation process in Escherichia coli. Nucleic Acids Res 2012, 40:5569-5576.
10. Brodt A., Lurie-Weinberger M.N., Gophna U. CRISPR loci reveal networks of gene exchange in archaea. Biol Direct 2011, 6:65.
11. Stern A., Keren L., Wurtzel O., Amitai G., Sorek R. Self-targeting by CRISPR: gene regulation or autoimmunity?. Trends Genet 2010, 26:335-340.
12. Marraffini L.A., Sontheimer E.J. CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 2010, 11:181-190.
13. Brouns S.J., Jore M.M., Lundgren M., Westra E.R., Slijkhuis R.J., Snijders A.P., Dickman M.J., Makarova K.S., Koonin E.V., van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008, 321:960-964.
14. Carte J., Wang R., Li H., Terns R.M., Terns M.P. Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 2008, 22:3489-3496.
15. Deltcheva E., Chylinski K., Sharma C.M., Gonzales K., Chao Y., Pirzada Z.A., Eckert M.R., Vogel J., Charpentier E. CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 2011, 471:602-607.
16. Hatoum-Aslan A., Maniv I., Marraffini L.A. Mature clustered, regularly interspaced, short palindromic repeats RNA (crRNA) length is measured by a ruler mechanism anchored at the precursor processing site. Proc Natl Acad Sci U S A 2011, 108:21218-21222.
17. Haurwitz R.E., Jinek M., Wiedenheft B., Zhou K., Doudna J.A. Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 2010, 329:1355-1358.
18. Garneau J.E., Dupuis M.E., Villion M., Romero D.A., Barrangou R., Boyaval P., Fremaux C., Horvath P., Magadan A.H., Moineau S. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 2010, 468:67-71.
19. Hale C.R., Zhao P., Olson S., Duff M.O., Graveley B.R., Wells L., Terns R.M., Terns M.P. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 2009, 139:945-956.
20. Westra E.R., van Erp P.B., Kunne T., Wong S.P., Staals R.H., Seegers C.L., Bollen S., Jore M.M., Semenova E., Severinov K., et al. CRISPR immunity relies on the consecutive binding and degradation of negatively supercoiled invader DNA by Cascade and Cas3. Mol Cell 2012, 46:595-605.
21. Chylinski K., Le Rhun A., Charpentier E. The tracrRNA and Cas9 families of type II CRISPR-Cas immunity systems. RNA Biol 2013, 10:726-737.
22. 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 2011, 6:38.
23. Makarova K.S., Haft D.H., Barrangou R., Brouns S.J., Charpentier E., Horvath P., Moineau S., Mojica F.J., Wolf Y.I., Yakunin A.F., et al. Evolution and classification of the CRISPR-Cas systems. Nat Rev Microbiol 2011, 9:467-477.
24. Koonin E.V., Makarova K.S. CRISPR-Cas: evolution of an RNA-based adaptive immunity system in prokaryotes. RNA Biol 2013, 10:679-686.
25. Hale C., Kleppe K., Terns R.M., Terns M.P. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 2008, 14:2572-2579.
26. Marraffini L.A., Sontheimer E.J. CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 2008, 322:1843-1845.
27. Hatoum-Aslan A., Samai P., Maniv I., Jiang W., Marraffini L.A. A ruler protein in a complex for antiviral defense determines the length of small interfering CRISPR RNAs. J Biol Chem 2013, 288:27888-27897.
28. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
29. Grissa I., Vergnaud G., Pourcel C. The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinform 2007, 8:172.
30. Furuya E.Y., Lowy F.D. Antimicrobial-resistant bacteria in the community setting. Nat Rev Microbiol 2006, 4:36-45.
31. Weigel L.M., Clewell D.B., Gill S.R., Clark N.C., McDougal L.K., Flannagan S.E., Kolonay J.F., Shetty J., Killgore G.E., Tenover F.C. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 2003, 302:1569-1571.
32. Gill S.R., Fouts D.E., Archer G.L., Mongodin E.F., Deboy R.T., Ravel J., Paulsen I.T., Kolonay J.F., Brinkac L., Beanan M., et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 2005, 187:2426-2438.
33. Jiang W., Maniv I., Arain F., Wang Y., Levin B.R., Marraffini L.A. Dealing with the evolutionary downside of CRISPR immunity: bacteria and beneficial plasmids. PLoS Genet 2013, 9:e1003844.
34. Baba T., Bae T., Schneewind O., Takeuchi F., Hiramatsu K. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 2008, 190:300-310.
35. Diep B.A., Gill S.R., Chang R.F., Phan T.H., Chen J.H., Davidson M.G., Lin F., Lin J., Carleton H.A., Mongodin E.F., et al. Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 2006, 367:731-739.
36. Griffith F. The significance of pneumococcal types. J Hyg 1928, 27:113-159.
37. Avery O.T., Macleod C.M., McCarty M. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from Pneumococcus type III. J Exp Med 1944, 79:137-158.
38. Croucher N.J., Harris S.R., Fraser C., Quail M.A., Burton J., van der Linden M., McGee L., von Gottberg A., Song J.H., Ko K.S., et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011, 331:430-434.
39. Bikard D., Hatoum-Aslan A., Mucida D., Marraffini L.A. CRISPR interference can prevent natural transformation and virulence acquisition during in vivo bacterial infection. Cell Host Microbe 2012, 12:177-186.
40. Top J., Willems R., Bonten M. Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen. FEMS Immunol Med Microbiol 2008, 52:297-308.
41. Isnard C., Malbruny B., Leclercq R., Cattoir V. Genetic basis for in vitro and in vivo resistance to lincosamides, streptogramins a, and pleuromutilins (LSAP phenotype) in Enterococcus faecium. Antimicrob Agents Chemother 2013, 57:4463-4469.
42. Palmer K.L., Gilmore M.S. Multidrug-resistant enterococci lack CRISPR-cas. mBio 2010, 1. e00227-00210.
43. Paulsen I.T., Banerjei L., Myers G.S., Nelson K.E., Seshadri R., Read T.D., Fouts D.E., Eisen J.A., Gill S.R., Heidelberg J.F., et al. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 2003, 299:2071-2074.
44. Shankar N., Baghdayan A.S., Gilmore M.S. Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 2002, 417:746-750.
45. Burley K.M., Sedgley C.M. CRISPR-Cas, a prokaryotic adaptive immune system, in endodontic, oral, and multidrug-resistant hospital-acquired Enterococcus faecalis. J Endod 2012, 38:1511-1515.
46. Bisno A.L. Group A streptococcal infections and acute rheumatic fever. N Engl J Med 1991, 325:783-793.
47. Beres S.B., Musser J.M. Contribution of exogenous genetic elements to the group A Streptococcus metagenome. PLoS ONE 2007, 2:e800.
48. Banks D.J., Beres S.B., Musser J.M. The fundamental contribution of phages to GAS evolution, genome diversification and strain emergence. Trends Microbiol 2002, 10:515-521.
49. Nozawa T., Furukawa N., Aikawa C., Watanabe T., Haobam B., Kurokawa K., Maruyama F., Nakagawa I. CRISPR inhibition of prophage acquisition in Streptococcus pyogenes. PLoS ONE 2011, 6:e19543.
50. Mah T.F., Pitts B., Pellock B., Walker G.C., Stewart P.S., O'Toole G.A. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003, 426:306-310.
51. Cady K.C., White A.S., Hammond J.H., Abendroth M.D., Karthikeyan R.S., Lalitha P., Zegans M.E., O'Toole G.A. Prevalence, conservation and functional analysis of Yersinia and Escherichia CRISPR regions in clinical Pseudomonas aeruginosa isolates. Microbiology 2011, 157:430-437.
52. Cady K.C., Bondy-Denomy J., Heussler G.E., Davidson A.R., O'Toole G.A. The CRISPR/Cas adaptive immune system of Pseudomonas aeruginosa mediates resistance to naturally occurring and engineered phages. J Bacteriol 2012, 194:5728-5738.
53. Zegans M.E., Wagner J.C., Cady K.C., Murphy D.M., Hammond J.H., O'Toole G.A. Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J Bacteriol 2009, 191:210-219.
54. Cady K.C., O'Toole G.A. Non-identity-mediated CRISPR-bacteriophage interaction mediated via the Csy and Cas3 proteins. J Bacteriol 2011, 193:3433-3445.
55. Dennis D.T., Inglesby T.V., Henderson D.A., Bartlett J.G., Ascher M.S., Eitzen E., Fine A.D., Friedlander A.M., Hauer J., Layton M., et al. Tularemia as a biological weapon: medical and public health management. JAMA 2001, 285:2763-2773.
56. Schunder E., Rydzewski K., Grunow R., Heuner K. First indication for a functional CRISPR/Cas system in Francisella tularensis. Int J Med Microbiol 2013, 303:51-60.
57. Sampson T.R., Saroj S.D., Llewellyn A.C., Tzeng Y.L., Weiss D.S. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 2013, 497:254-257.
58. Sampson T.R., Saroj S.D., Llewellyn A.C., Tzeng Y.L., Weiss D.S. Corrigendum: a CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 2013, 501:262.
59. Louwen R., Horst-Kreft D., de Boer A.G., van der Graaf L., de Knegt G., Hamersma M., Heikema A.P., Timms A.R., Jacobs B.C., Wagenaar J.A., et al. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barre syndrome. Eur J Clin Microbiol Infect Dis 2013, 32:207-226.
60. Gunderson F.F., Cianciotto N.P. The CRISPR-associated gene cas2 of Legionella pneumophila is required for intracellular infection of amoebae. mBio 2013, 4. e00074-00013.
61. Ferretti J.J., McShan W.M., Ajdic D., Savic D.J., Savic G., Lyon K., Primeaux C., Sezate S., Suvorov A.N., Kenton S., et al. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 2001, 98:4658-4663.
62. Beres S.B., Richter E.W., Nagiec M.J., Sumby P., Porcella S.F., DeLeo F.R., Musser J.M. Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc Natl Acad Sci U S A 2006, 103:7059-7064.
63. McShan W.M., Ferretti J.J., Karasawa T., Suvorov A.N., Lin S., Qin B., Jia H., Kenton S., Najar F., Wu H., et al. Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 2008, 190:7773-7785.
64. Sumby P., Porcella S.F., Madrigal A.G., Barbian K.D., Virtaneva K., Ricklefs S.M., Sturdevant D.E., Graham M.R., Vuopio-Varkila J., Hoe N.P., et al. Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 2005, 192:771-782.
65. Green N.M., Zhang S., Porcella S.F., Nagiec M.J., Barbian K.D., Beres S.B., LeFebvre R.B., Musser J.M. Genome sequence of a serotype M28 strain of group a streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 2005, 192:760-770.
66. Beres S.B., Sylva G.L., Barbian K.D., Lei B., Hoff J.S., Mammarella N.D., Liu M.Y., Smoot J.C., Porcella S.F., Parkins L.D., et al. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 2002, 99:10078-10083.
67. Nakagawa I., Kurokawa K., Yamashita A., Nakata M., Tomiyasu Y., Okahashi N., Kawabata S., Yamazaki K., Shiba T., Yasunaga T., et al. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res 2003, 13:1042-1055.
68. Holden M.T., Scott A., Cherevach I., Chillingworth T., Churcher C., Cronin A., Dowd L., Feltwell T., Hamlin N., Holroyd S., et al. Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain manfredo. J Bacteriol 2007, 189:1473-1477.
69. Banks D.J., Porcella S.F., Barbian K.D., Beres S.B., Philips L.E., Voyich J.M., DeLeo F.R., Martin J.M., Somerville G.A., Musser J.M. Progress toward characterization of the group A Streptococcus metagenome: complete genome sequence of a macrolide-resistant serotype M6 strain. J Infect Dis 2004, 190:727-738.
70. Smoot J.C., Barbian K.D., Van Gompel J.J., Smoot L.M., Chaussee M.S., Sylva G.L., Sturdevant D.E., Ricklefs S.M., Porcella S.F., Parkins L.D., et al. Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci U S A 2002, 99:4668-4673.