Tissue dual RNA-seq allows fast discovery of infection-specific functions and riboregulators shaping host-pathogen transcriptomes

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 5, 2017, Pages E791-E800

  Nuss, Aaron M ^a   Beckstette, Michael ^a   Pimenova, Maria ^a   Schmühl, Carina ^a   Opitz, Wiebke ^a   Pisano, Fabio ^a   Heroven, Ann Kathrin ^a   Dersch, Petra ^a  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Host adapted metabolism; Host pathogen interaction; Noncoding RNAs; Tissue dual RNA seq; Yersinia

Indexed keywords

CARBON; METAL ION; TRANSCRIPTOME; MESSENGER RNA; VIRULENCE FACTOR;

ACUTE PHASE RESPONSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BACTERIAL VIRULENCE; BLOOD CLOTTING; CARBON STORAGE; CONFERENCE PAPER; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HOST CELL; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; INFLAMMATION; LYMPHOID TISSUE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TYPE III SECRETION SYSTEM; UPREGULATION; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTION; ANIMAL; BAGG ALBINO MOUSE; FEMALE; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PEYER PATCH; PHYSIOLOGY; SEQUENCE ANALYSIS;

ANIMALS; FEMALE; HOST-PATHOGEN INTERACTIONS; MICE, INBRED BALB C; PEYER'S PATCHES; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME; VIRULENCE FACTORS; YERSINIA PSEUDOTUBERCULOSIS; YERSINIA PSEUDOTUBERCULOSIS INFECTIONS;

EID: 85011277100     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1613405114     Document Type: Article

References (99)

1. Papenfort K, Vogel J (2014) Small RNA functions in carbon metabolism and virulence of enteric pathogens. Front Cell Infect Microbiol 4:91.
2. Oliva G, Sahr T, Buchrieser C (2015) Small RNAs, 5′ UTR elements and RNA-binding proteins in intracellular bacteria: Impact on metabolism and virulence. FEMS Microbiol Rev 39(3):331-349.
3. Heroven AK, Nuss AM, Dersch P (2016) RNA-based mechanisms of virulence control in Enterobacteriaceae. RNA Biol 2016:1-17.
4. Kröger C, et al. (2013) An infection-relevant transcriptomic compendium for Salmonella enterica Serovar Typhimurium. Cell Host Microbe 14(6):683-695.
5. Nuss AM, et al. (2015) Transcriptomic profiling of Yersinia pseudotuberculosis reveals reprogramming of the Crp regulon by temperature and uncovers Crp as a master regulator of small RNAs. PLoS Genet 11(3):e1005087.
6. Koo JT, Alleyne TM, Schiano CA, Jafari N, LathemWW(2011) Global discovery of small RNAs in Yersinia pseudotuberculosis identifies Yersinia-specific small, noncoding RNAs required for virulence. Proc Natl Acad Sci USA 108(37):E709-E717.
7. Srikumar S, et al. (2015) RNA-seq brings new insights to the intra-macrophage transcriptome of Salmonella Typhimurium. PLoS Pathog 11(11):e1005262.
8. Mandlik A, et al. (2011) RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. Cell Host Microbe 10(2):165-174.
9. Wu Z, et al. (2014) The Streptococcus suis transcriptional landscape reveals adaptation mechanisms in pig blood and cerebrospinal fluid. RNA 20(6):882-898.
10. Westermann AJ, Gorski SA, Vogel J (2012) Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10(9):618-630.
11. Westermann AJ, et al. (2016) Dual RNA-seq unveils noncoding RNA functions in hostpathogen interactions. Nature 529(7587):496-501.
12. Baddal B, et al. (2015) Dual RNA-seq of nontypeable haemophilus influenzae and host cell transcriptomes reveals novel insights into host-pathogen cross talk. MBio 6(6): e01765-e15.
13. Rienksma RA, et al. (2015) Comprehensive insights into transcriptional adaptation of intracellularmycobacteria bymicrobe-enriched dual RNA sequencing. BMC Genomics 16:34.
14. Pisano F, et al. (2014) Influence of PhoP and intra-species variations on virulence of Yersinia pseudotuberculosis during the natural oral infection route. PLoS One 9(7): e103541.
15. Carter PB (1975) Animal model of human disease. Yersinia enteritis. Animal model: Oral Yersinia enterocolitica infection of mice. Am J Pathol 81(3):703-706.
16. Dube PH, Handley SA, Lewis J, Miller VL (2004) Protective role of interleukin-6 during Yersinia enterocolitica infection is mediated through the modulation of inflammatory cytokines. Infect Immun 72(6):3561-3570.
17. Dube PH, Revell PA, Chaplin DD, Lorenz RG, Miller VL (2001) A role for IL-1 alpha in inducing pathologic inflammation during bacterial infection. Proc Natl Acad Sci USA 98(19):10880-10885.
18. Locati MD, et al. (2015) Improving small RNA-seq by using a synthetic spike-in set for size-range quality control together with a set for data normalization. Nucleic Acids Res 43(14):e89.
19. Haas BJ, Chin M, Nusbaum C, Birren BW, Livny J (2012) How deep is deep enough for RNA-Seq profiling of bacterial transcriptomes? BMC Genomics 13:734.
20. Ching T, Huang S, Garmire LX (2014) Power analysis and sample size estimation for RNA-Seq differential expression. RNA 20(11):1684-1696.
21. Kim D, et al. (2012) Comparative analysis of regulatory elements between Escherichia coli and Klebsiella pneumoniae by genome-wide transcription start site profiling. PLoS Genet 8(8):e1002867.
22. Kröger C, et al. (2012) The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci USA 109(20):E1277-E1286.
23. Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550.
24. Liu M, et al. (2012) Formylpeptide receptors are critical for rapid neutrophil mobilization in host defense against Listeria monocytogenes. Sci Rep 2:786.
25. Sharma A, Steichen AL, Jondle CN, Mishra BB, Sharma J (2014) Protective role of Mincle in bacterial pneumonia by regulation of neutrophil mediated phagocytosis and extracellular trap formation. J Infect Dis 209(11):1837-1846.
26. Kang MJ, et al. (2015) Role of chitinase 3-like-1 in interleukin-18-induced pulmonary type 1, type 2, and type 17 inflammation; alveolar destruction; and airway fibrosis in the murine lung. Am J Respir Cell Mol Biol 53(6):863-871.
27. Autenrieth IB, Kempf V, Sprinz T, Preger S, Schnell A (1996) Defense mechanisms in Peyer's patches and mesenteric lymph nodes against Yersinia enterocolitica involve integrins and cytokines. Infect Immun 64(4):1357-1368.
28. Matteoli G, et al. (2008) Role of IFN-gamma and IL-6 in a protective immune response to Yersinia enterocolitica in mice. BMC Microbiol 8:153.
29. Comer JE, et al. (2010) Transcriptomic and innate immune responses to Yersinia pestis in the lymph node during bubonic plague. Infect Immun 78(12):5086-5098.
30. Nikoopour E, Bellemore SM, Singh B (2015) IL-22, cell regeneration and autoimmunity. Cytokine 74(1):35-42.
31. Wang Y, et al. (2015) Jagged-1 signaling suppresses the IL-6 and TGF-β treatmentinduced Th17 cell differentiation via the reduction of RORγt/IL-17A/IL-17F/IL-23a/IL-12rb1. Sci Rep 5:8234.
32. Mascanfroni ID, et al. (2013) IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat Immunol 14(10):1054-1063.
33. Dinarello CA (2009) Immunological and inflammatory functions of the interleukin-1 family. Annu Rev Immunol 27:519-550.
34. Cray C, Zaias J, Altman NH (2009) Acute phase response in animals: A review. Comp Med 59(6):517-526.
35. Kanther M, et al. (2014) Commensal microbiota stimulate systemic neutrophil migration through induction of serum amyloid A. Cell Microbiol 16(7):1053-1067.
36. Björkman L, et al. (2008) Serum amyloid A mediates human neutrophil production of reactive oxygen species through a receptor independent of formyl peptide receptor like-1. J Leukoc Biol 83(2):245-253.
37. Ather JL, et al. (2011) Serum amyloid A activates the NLRP3 inflammasome and promotes Th17 allergic asthma in mice. J Immunol 187(1):64-73.
38. Ivanov II, et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139(3):485-498.
39. Vallon R, et al. (2001) Serum amyloid A (apoSAA) expression is up-regulated in rheumatoid arthritis and induces transcription of matrix metalloproteinases. J Immunol 166(4):2801-2807.
40. Hall JA, Grainger JR, Spencer SP, Belkaid Y (2011) The role of retinoic acid in tolerance and immunity. Immunity 35(1):13-22.
41. Derebe MG, et al. (2014) Serum amyloid A is a retinol binding protein that transports retinol during bacterial infection. eLife 3:e03206.
42. van der Poll T, Herwald H (2014) The coagulation system and its function in early immune defense. Thromb Haemost 112(4):640-648.
43. Weiss SJ, Peppin G, Ortiz X, Ragsdale C, Test ST (1985) Oxidative autoactivation of latent collagenase by human neutrophils. Science 227(4688):747-749.
44. Hasty KA, Hibbs MS, Kang AH, Mainardi CL (1986) Secreted forms of human neutrophil collagenase. J Biol Chem 261(12):5645-5650.
45. Cunningham AC, Hasty KA, Enghild JJ, Mast AE (2002) Structural and functional characterization of tissue factor pathway inhibitor following degradation by matrix metalloproteinase-8. Biochem J 367(Pt 2):451-458.
46. Papareddy P, et al. (2012) Tissue factor pathway inhibitor 2 is found in skin and its C-terminal region encodes for antibacterial activity. PLoS One 7(12):e52772.
47. Kasetty G, et al. (2011) The C-terminal sequence of several human serine proteases encodes host defense functions. J Innate Immun 3(5):471-482.
48. Degen JL, Bugge TH, Goguen JD (2007) Fibrin and fibrinolysis in infection and host defense. J Thromb Haemost 5(Suppl 1):24-31.
49. Luo D, et al. (2013) Fibrin facilitates both innate and T cell-mediated defense against Yersinia pestis. J Immunol 190(8):4149-4161.
50. Sodeinde OA, et al. (1992) A surface protease and the invasive character of plague. Science 258(5084):1004-1007.
51. Guinet F, et al. (2015) Dissociation of tissue destruction and bacterial expansion during bubonic plague. PLoS Pathog 11(10):e1005222.
52. Davis KM, Mohammadi S, Isberg RR (2015) Community behavior and spatial regulation within a bacterial microcolony in deep tissue sites serves to protect against host attack. Cell Host Microbe 17(1):21-31.
53. Korhonen TK (2015) Fibrinolytic and procoagulant activities of Yersinia pestis and Salmonella enterica. J Thromb Haemost 13(Suppl 1):S115-S120.
54. Diaz-Ochoa VE, Jellbauer S, Klaus S, Raffatellu M (2014) Transition metal ions at the crossroads of mucosal immunity andmicrobial pathogenesis. Front Cell InfectMicrobiol 4:2.
55. Raffatellu M, et al. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5(5):476-486.
56. Kehl-Fie TE, et al. (2011) Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10(2):158-164.
57. Damo SM, et al. (2013) Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci USA 110(10):3841-3846.
58. Steinbakk M, et al. (1990) Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336(8718):763-765.
59. Flo TH, et al. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432(7019):917-921.
60. Handley SA, Dube PH, Miller VL (2006) Histamine signaling through the H(2) receptor in the Peyer's patch is important for controlling Yersinia enterocolitica infection. Proc Natl Acad Sci USA 103(24):9268-9273.
61. Michelucci A, et al. (2013) Immune-responsive gene 1 protein links metabolism to immunity by catalyzing itaconic acid production. Proc Natl Acad Sci USA 110(19): 7820-7825.
62. Sasikaran J, Ziemski M, Zadora PK, Fleig A, Berg IA (2014) Bacterial itaconate degradation promotes pathogenicity. Nat Chem Biol 10(5):371-377.
63. Handley SA, Miller VL (2007) General and specific host responses to bacterial infection in Peyer's patches: A role for stromelysin-1 (matrix metalloproteinase-3) during Salmonella enterica infection. Mol Microbiol 64(1):94-110.
64. Gericke B, Amiri M, Naim HY (2016) The multiple roles of sucrase-isomaltase in the intestinal physiology. Mol Cell Pediatr 3(1):2.
65. Cornelis GR, et al. (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62(4):1315-1352.
66. Durand EA, Maldonado-Arocho FJ, Castillo C, Walsh RL, Mecsas J (2010) The presence of professional phagocytes dictates the number of host cells targeted for Yop translocation during infection. Cell Microbiol 12(8):1064-1082.
67. Pettersson J, et al. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273(5279):1231-1233.
68. Pinto UM, Pappas KM, Winans SC (2012) The ABCs of plasmid replication and segregation. Nat Rev Microbiol 10(11):755-765.
69. Wang H, et al. (2016) Increased plasmid copy-number is essential for Yersinia T3SS function and virulence. Science 353(6298):492-495.
70. Righetti F, et al. (2016) Temperature-responsive in vitro RNA structurome of Yersinia pseudotuberculosis. Proc Natl Acad Sci USA 113(26):7237-7242.
71. Perry RD, Bobrov AG, Fetherston JD (2015) The role of transition metal transporters for iron, zinc, manganese, and copper in the pathogenesis of Yersinia pestis. Metallomics 7(6):965-978.
72. Soares MP, Weiss G (2015) The Iron age of host-microbe interactions. EMBO Rep 16(11):1482-1500.
73. Gabriel SE, Helmann JD (2009) Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J Bacteriol 191(19):6116-6122.
74. Akanuma G, Nanamiya H, Natori Y, Nomura N, Kawamura F (2006) Liberation of zinccontaining L31 (RpmE) from ribosomes by its paralogous gene product, YtiA, in Bacillus subtilis. J Bacteriol 188(7):2715-2720.
75. Bücker R, Heroven AK, Becker J, Dersch P, Wittmann C (2014) The pyruvate-tricarboxylic acid cycle node: A focal point of virulence control in the enteric pathogen Yersinia pseudotuberculosis. J Biol Chem 289(43):30114-30132.
76. Pradel E, et al. (2014) New insights into how Yersinia pestis adapts to its mammalian host during bubonic plague. PLoS Pathog 10(3):e1004029.
77. Sebbane F, et al. (2006) Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc Natl Acad Sci USA 103(31): 11766-11771.
78. Palace SG, Proulx MK, Lu S, Baker RE, Goguen JD (2014) Genome-wide mutant fitness profiling identifies nutritional requirements for optimal growth of Yersinia pestis in deep tissue. MBio 5(4):e01385-14.
79. Deng Z, et al. (2012) Two sRNA RyhB homologs from Yersinia pestis biovar microtus expressed in vivo have differential Hfq-dependent stability. Res Microbiol 163(6-7):413-418.
80. Deng Z, et al. (2014) Rapid degradation of Hfq-free RyhB in Yersinia pestis by PNPase independent of putative ribonucleolytic complexes. BioMed Res Int 2014:798918.
81. Massé E, Gottesman S (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99(7):4620-4625.
82. Kim JN, Kwon YM (2013) Identification of target transcripts regulated by small RNA RyhB homologs in Salmonella: RyhB-2 regulates motility phenotype. Microbiol Res 168(10):621-629.
83. Horler RS, Vanderpool CK (2009) Homologs of the small RNA SgrS are broadly distributed in enteric bacteria but have diverged in size and sequence. Nucleic Acids Res 37(16):5465-5476.
84. Vanderpool CK, Gottesman S (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54(4):1076-1089.
85. Wadler CS, Vanderpool CK (2007) A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci USA 104(51):20454-20459.
86. Wadler CS, Vanderpool CK (2009) Characterization of homologs of the small RNA SgrS reveals diversity in function. Nucleic Acids Res 37(16):5477-5485.
87. Rice JB, Vanderpool CK (2011) The small RNA SgrS controls sugar-phosphate accumulation by regulating multiple PTS genes. Nucleic Acids Res 39(9):3806-3819.
88. Göpel Y, et al. (2011) Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae. Nucleic Acids Res 39(4):1294-1309.
89. Flamez C, Ricard I, Arafah S, Simonet M, Marceau M (2008) Phenotypic analysis of Yersinia pseudotuberculosis 32777 response regulator mutants: New insights into twocomponent system regulon plasticity in bacteria. Int J Med Microbiol 298(3-4):193-207.
90. Heroven AK, et al. (2012) Crp induces switching of the CsrB and CsrC RNAs in Yersinia pseudotuberculosis and links nutritional status to virulence. Front Cell Infect Microbiol 2:158.
91. Suzuki K, Babitzke P, Kushner SR, Romeo T (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20(18):2605-2617.
92. Heroven AK, Böhme K, Dersch P (2012) The Csr/Rsm system of Yersinia and related pathogens: A post-transcriptional strategy for managing virulence. RNA Biol 9(4):379-391.
93. Vakulskas CA, Potts AH, Babitzke P, Ahmer BM, Romeo T (2015) Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev 79(2):193-224.
94. Avraham R, et al. (2015) Pathogen cell-to-cell variability drives heterogeneity in host immune responses. Cell 162(6):1309-1321.
95. Saliba AE, et al. (2016) Single-cell RNA-seq ties macrophage polarization to growth rate of intracellular Salmonella. Nat Microbiol 2:16206.
96. Böhme K, et al. (2012) Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathog 8(2):e1002518.
97. Monack DM, Mecsas J, Bouley D, Falkow S (1998) Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J Exp Med 188(11): 2127-2137.
98. Heroven AK, Böhme K, Rohde M, Dersch P (2008) A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 68(5):1179-1195.
99. Nicol JW, Helt GA, Blanchard SG, Jr, Raja A, Loraine AE (2009) The Integrated Genome Browser: Free software for distribution and exploration of genome-scale datasets. Bioinformatics 25(20):2730-2731.