Laser microdissection coupled with RNA-seq analysis of porcine enterocytes infected with an obligate intracellular pathogen (Lawsonia intracellularis)

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Vannucci, Fabio A ^a   Foster, Douglas N ^b   Gebhart, Connie J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Lawsonia intracellularis; Microdissection; Obligate intracellular; Proliferative enteropathy; RNA seq

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; COPPER; COPPER UPTAKE TRANSPORTER; COPPER ZINC SUPEROXIDE DISMUTASE; RHO FACTOR; RUBREDOXIN; RUBRERYTHRIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL MATURATION; CELL MEMBRANE TRANSPORT; CELL METABOLISM; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOPLASM; DESULFOVIBRIONACEAE INFECTION; ENTEROPATHY; GENE EXPRESSION; GENETIC ASSOCIATION; HOST PATHOGEN INTERACTION; INTESTINE CELL; LASER MICRODISSECTION; LAWSONIA; LAWSONIA INTRACELLULARIS; NONHUMAN; NUTRIENT UPTAKE; OPERON; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN SYNTHESIS; RNA SEQUENCE; TRANSCRIPTION INITIATION;

ANIMALS; APOPTOSIS; CELL CYCLE; ELECTROLYTES; ENTEROCYTES; HOST-PATHOGEN INTERACTIONS; INTRACELLULAR SPACE; LASER CAPTURE MICRODISSECTION; LAWSONIA BACTERIA; SEQUENCE ANALYSIS, RNA; SWINE; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); EQUIDAE; LAWSONIA INTRACELLULARIS; PRIMATES; SUIDAE; SUS;

EID: 84879248703     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-421     Document Type: Article

References (63)

1. Lax AJ, Thomas W. How bacteria could cause cancer: one step at a time. Trends Microbiol 2002, 10(6):293-299. 10.1016/S0966-842X(02)02360-0, 12088666.
2. Ikeno T, Ota H, Sugiyama A, Ishida K, Katsuyama T, Genta RM, Kawasaki S. Helicobacter pylori-induced chronic active gastritis, intestinal metaplasia, and gastric ulcer in Mongolian gerbils. Am J Pathol 1999, 154(3):951-960. 10.1016/S0002-9440(10)65343-6, 1866409, 10079274.
3. Baik SC, Youn HS, Chung MH, Lee WK, Cho MJ, Ko GH, Park CK, Kasai H, Rhee KH. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res 1996, 56(6):1279-1282.
4. Luperchio SA, Schauer DB. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect 2001, 3(4):333-340. 10.1016/S1286-4579(01)01387-9, 11334751.
5. Smith DG, Lawson GH. Lawsonia intracellularis: getting inside the pathogenesis of proliferative enteropathy. Vet Microbiol 2001, 82(4):331-345. 10.1016/S0378-1135(01)00397-2, 11506927.
6. Sellin JH, Wang Y, Singh P, Umar S. beta-Catenin stabilization imparts crypt progenitor phenotype to hyperproliferating colonic epithelia. Exp Cell Res 2009, 315(1):97-109. 10.1016/j.yexcr.2008.10.019, 2868370, 18996369.
7. McOrist S, Gebhart CJ, Bosworth BT. Evaluation of porcine ileum models of enterocyte infection by Lawsonia intracellularis. Can J Vet Res 2006, 70(2):155-159. 1410719, 16639950.
8. Gebhart CJ, Guedes RMC. Lawsonia intracellularis. Pathogenesis of bacterial infections in animals 2010, 503-509. Fourth edn. Ames, Iowa, USA: Blackwell Publishing, Gyles CL, Prescott JF, Songer JG, Thoen CO.
9. Lawson GH, Gebhart CJ. Proliferative enteropathy. J Comp Pathol 2000, 122(2-3):77-100.
10. Cooper DM, Swanson DL, Barns SM, Gebhart CJ. Comparison of the 16S ribosomal DNA sequences from the intracellular agents of proliferative enteritis in a hamster, deer, and ostrich with the sequence of a porcine isolate of Lawsonia intracellularis. Int J Syst Bacteriol 1997, 47(3):635-639. 10.1099/00207713-47-3-635, 9226893.
11. Pusterla N, Mapes S, Rejmanek D, Gebhart C. Detection of Lawsonia intracellularis by real-time PCR in the feces of free-living animals from equine farms with documented occurrence of equine proliferative enteropathy. J Wildl Dis 2008, 44(4):992-998.
12. Klein EC, Gebhart CJ, Duhamel GE. Fatal outbreaks of proliferative enteritis caused by Lawsonia intracellularis in young colony-raised rhesus macaques. J Med Primatol 1999, 28(1):11-18. 10.1111/j.1600-0684.1999.tb00084.x, 10372536.
13. Lavoie JP, Drolet R. Equine proliferative enteropathy: an emerging disease of foals. Equine Vet Educ 2009, 21(4):183-185.
14. Lawson GH, McOrist S, Jasni S, Mackie RA. Intracellular bacteria of porcine proliferative enteropathy: cultivation and maintenance in vitro. J Clin Microbiol 1993, 31(5):1136-1142. 262892, 8501214.
15. Biester HE, Schwarte LH. Intestinal adenoma in swine. Am J Pathol 1931, 7(2):175-185.176. 2062611, 19969959.
16. McOrist S, Jasni S, Mackie RA, Berschneider HM, Rowland AC, Lawson GH. Entry of the bacterium ileal symbiont intracellularis into cultured enterocytes and its subsequent release. Res Vet Sci 1995, 59(3):255-260. 10.1016/0034-5288(95)90013-6, 8588102.
17. Guedes RM, Gebhart CJ. Comparison of intestinal mucosa homogenate and pure culture of the homologous Lawsonia intracellularis isolate in reproducing proliferative enteropathy in swine. Vet Microbiol 2003, 93(2):159-166. 10.1016/S0378-1135(03)00013-0, 12637004.
18. Vannucci FA, Wattanaphansak S, Gebhart CJ. An alternative method for cultivation of lawsonia intracellularis. J Clin Microbiol 2012, 50(3):1070-1072. 10.1128/JCM.05976-11, 3295169, 22219308.
19. Guedes RM, Gebhart CJ. Onset and duration of fecal shedding, cell-mediated and humoral immune responses in pigs after challenge with a pathogenic isolate or attenuated vaccine strain of Lawsonia intracellularis. Vet Microbiol 2003, 91(2-3):135-145.
20. Vannucci FA, Beckler D, Pusterla N. Mapes SM 2012, Gebhart CJ: Attenuation of virulence of Lawsonia intracellularis after in vitro passages and its effects on the experimental reproduction of porcine proliferative enteropathy. Vet Microbiol.
21. Mikulowska-Mennis A, Taylor TB, Vishnu P, Michie SA, Raja R, Horner N, Kunitake ST. High-quality RNA from cells isolated by laser capture microdissection. Biotechniques 2002, 33(1):176-179.
22. Schafer KA. The cell cycle: a review. Vet Pathol 1998, 35(6):461-478. 10.1177/030098589803500601, 9823588.
23. Pruitt K, Der CJ. Ras and Rho regulation of the cell cycle and oncogenesis. Cancer Lett 2001, 171(1):1-10. 10.1016/S0304-3835(01)00528-6, 11485822.
24. Coleman ML, Marshall CJ, Olson MF. RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat Rev Mol Cell Biol 2004, 5(5):355-366.
25. Harris DS, Slot JW, Geuze HJ, James DE. Polarized distribution of glucose transporter isoforms in Caco-2 cells. Proc Natl Acad Sci U S A 1992, 89(16):7556-7560. 10.1073/pnas.89.16.7556, 49749, 1502167.
26. Boyer S, Sharp PA, Debnam ES, Baldwin SA, Srai SK. Streptozotocin diabetes and the expression of GLUT1 at the brush border and basolateral membranes of intestinal enterocytes. FEBS Lett 1996, 396(2-3):218-222.
27. Lumppio HL, Shenvi NV, Summers AO, Voordouw G, Kurtz DM. Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris: a novel oxidative stress protection system. J Bacteriol 2001, 183(1):101-108. 10.1128/JB.183.1.101-108.2001, 94855, 11114906.
28. Westermann AJ, Gorski SA, Vogel J. Dual RNA-seq of pathogen and host. Nat Rev Microbiol 2012, 10(9):618-630. 10.1038/nrmicro2852, 22890146.
29. McOrist S, Roberts L, Jasni S, Rowland AC, Lawson GH, Gebhart CJ, Bosworth B. Developed and resolving lesions in porcine proliferative enteropathy: possible pathogenetic mechanisms. J Comp Pathol 1996, 115(1):35-45. 10.1016/S0021-9975(96)80026-0, 8878750.
30. Oh YS, Lee JB, McOrist S. Microarray analysis of differential expression of cell cycle and cell differentiation genes in cells infected with Lawsonia intracellularis. Vet J 2010, 184(3):340-345. 10.1016/j.tvjl.2009.03.018, 19362500.
31. Jacobson M, Andersson M, Lindberg R, Fossum C, Jensen-Waern M. Microarray and cytokine analyses of field cases of pigs with diarrhoea. Vet Microbiol 2011, 153:307-314. 10.1016/j.vetmic.2011.06.003, 21741782.
32. Freeman TC, Ivens A, Baillie JK, Beraldi D, Barnett MW, Dorward D, Downing A, Fairbairn L, Kapetanovic R, Raza S, et al. A gene expression atlas of the domestic pig. BMC Biol 2012, 10:90. 10.1186/1741-7007-10-90, 23153189.
33. Rowland AC, Lawson GH. Intestinal adenomatosis in the pig: immunofluorescent and electron microscopic studies. Res Vet Sci 1974, 17(3):323-330.
34. Navare AT, Sova P, Purdy DE, Weiss JM, Wolf-Yadlin A, Korth MJ, Chang ST, Proll SC, Jahan TA, Krasnoselsky AL, et al. Quantitative proteomic analysis of HIV-1 infected CD4+ T cells reveals an early host response in important biological pathways: protein synthesis, cell proliferation, and T-cell activation. Virology 2012, 429(1):37-46. 10.1016/j.virol.2012.03.026, 3358407, 22542004.
35. Oswald E, Nougayrède JP, Taieb F, Sugai M. Bacterial toxins that modulate host cell-cycle progression. Curr Opin Microbiol 2005, 8(1):83-91. 10.1016/j.mib.2004.12.011, 15694861.
36. Nougayrède JP, Taieb F, De Rycke J, Oswald E. Cyclomodulins: bacterial effectors that modulate the eukaryotic cell cycle. Trends Microbiol 2005, 13(3):103-110. 10.1016/j.tim.2005.01.002, 15737728.
37. Lemonnier M, Landraud L, Lemichez E. Rho GTPase-activating bacterial toxins: from bacterial virulence regulation to eukaryotic cell biology. FEMS Microbiol Rev 2007, 31(5):515-534. 10.1111/j.1574-6976.2007.00078.x, 17680807.
38. Mulvey MA, Lopez-Boado YS, Wilson CL, Roth R, Parks WC, Heuser J, Hultgren SJ. Induction and evasion of host defenses by type 1-piliated uropathogenic Escherichia coli. Science 1998, 282(5393):1494-1497.
39. Boutrup T. Studies of the pathogenesis of porcine proliferative enteropathy caused by Lawsonia intracellularis 2008, Copenhagen, Denmark: University of Copenhagen.
40. Moeser AJ, Blikslager AT. Mechanisms of porcine diarrheal disease. J Am Vet Med Assoc 2007, 231(1):56-67. 10.2460/javma.231.1.56, 17605665.
41. Vannucci FA, Borges EL, de Oliveira JS, Guedes RM. Intestinal absorption and histomorphometry of Syrian hamsters (Mesocricetus auratus) experimentally infected with Lawsonia intracellularis. Vet Microbiol 2010, 145(3-4):286-291.
42. Sharp PA. Ctr1 and its role in body copper homeostasis. Int J Biochem Cell Biol 2003, 35(3):288-291. 10.1016/S1357-2725(02)00134-6, 12531240.
43. Festa RA, Thiele DJ. Copper at the front line of the host-pathogen battle. PLoS Pathog 2012, 8(9):e1002887. 10.1371/journal.ppat.1002887, 3447745, 23028306.
44. Schmitz-Esser S, Linka N, Collingro A, Beier CL, Neuhaus HE, Wagner M, Horn M. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J Bacteriol 2004, 186(3):683-691. 10.1128/JB.186.3.683-691.2004, 321502, 14729693.
45. Schmitz-Esser S, Haferkamp I, Knab S, Penz T, Ast M, Kohl C, Wagner M, Horn M. Lawsonia intracellularis contains a gene encoding a functional rickettsia-like ATP/ADP translocase for host exploitation. J Bacteriol 2008, 190(17):5746-5752. 10.1128/JB.00391-08, 2519521, 18606736.
46. Perry A, Lambert P. Propionibacterium acnes: infection beyond the skin. Expert Rev Anti Infect Ther 2011, 9(12):1149-1156. 10.1586/eri.11.137, 22114965.
47. McOrist S, Jasni S, Mackie RA, MacIntyre N, Neef N, Lawson GH. Reproduction of porcine proliferative enteropathy with pure cultures of ileal symbiont intracellularis. Infect Immun 1993, 61(10):4286-4292. 281156, 8406817.
48. Nikolaus T, Deiwick J, Rappl C, Freeman JA, Schröder W, Miller SI, Hensel M. SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J Bacteriol 2001, 183(20):6036-6045. 10.1128/JB.183.20.6036-6045.2001, 99683, 11567004.
49. Guedes RM, Gebhart CJ, Deen J, Winkelman NL. Validation of an immunoperoxidase monolayer assay as a serologic test for porcine proliferative enteropathy. J Vet Diagn Invest 2002, 14(6):528-530. 10.1177/104063870201400618, 12423042.
50. Vannucci FA, Pusterla N, Mapes SM, Gebhart C. Evidence of host adaptation in Lawsonia intracellularis infections. Vet Res 2012, 43(1):53. 10.1186/1297-9716-43-53, 3443049, 22715937.
51. Brown AL, Smith DW. Improved RNA preservation for immunolabeling and laser microdissection. RNA 2009, 15(12):2364-2374. 10.1261/rna.1733509, 2779672, 19850907.
52. Guedes RM, Gebhart CJ. Preparation and characterization of polyclonal and monoclonal antibodies against Lawsonia intracellularis. J Vet Diagn Invest 2003, 15(5):438-446. 10.1177/104063870301500506, 14535543.
53. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 2005, 15(10):1451-1455. 10.1101/gr.4086505, 1240089, 16169926.
54. Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, Team G. Manipulation of FASTQ data with Galaxy. Bioinformatics 2010, 26(14):1783-1785. 10.1093/bioinformatics/btq281, 2894519, 20562416.
55. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998, 8(3):175-185. 10.1101/gr.8.3.175, 9521921.
56. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
57. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012, 7(3):562-578. 10.1038/nprot.2012.016, 3334321, 22383036.
58. Segata N, Waldron L, Ballarini A, Narasimhan V, Jousson O, Huttenhower C. Metagenomic microbial community profiling using unique clade-specific marker genes. Nat Methods 2012, 9(8):811-814. 10.1038/nmeth.2066, 3443552, 22688413.
59. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B 1995, 57(1):289-300.
60. Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009, 4(3):363-371. 10.1038/nprot.2009.2, 19247286.
61. Wass MN, Sternberg MJ. ConFunc-functional annotation in the twilight zone. Bioinformatics 2008, 24(6):798-806. 10.1093/bioinformatics/btn037, 18263643.
62. Bookout AL, Cummins CL, Mangelsdorf DJ, Pesola JM, Kramer MF. High-throughput real-time quantitative reverse transcription PCR. Curr Protoc Mol Biol 2006, 15:15-18.
63. Vannucci FA, Foster DN, Gebhart CJ. Comparative transcriptional analysis of homologous pathogenic and non-pathogenic lawsonia intracellularis isolates in infected porcine cells. PLoS One 2012, 7(10):e46708. 10.1371/journal.pone.0046708, 3463550, 23056413.