Systems biology analysis of gene expression during in vivo Mycobacterium avium paratuberculosis enteric colonization reveals role for immune tolerance

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Khare, Sangeeta ^a,f   Lawhon, Sara D ^a   Drake, Kenneth L ^b   Nunes, Jairo E S ^a   Figueiredo, Josely F ^a   Rossetti, Carlos A ^a   Gull, Tamara ^a   Everts, Robin E ^c,e   Lewin, Harris A ^c   Galindo, Cristi L ^d   Garner, Harold R ^d   Adams, Leslie Garry ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b Seralogix Limited Liability Company   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e SEQUENOM INC   (United States)

^f NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; CYTOKINE; CYTOKINE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; DNA HYBRIDIZATION; ENDOCYTOSIS; ENTERITIS; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; ILEUM; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INTESTINE MUCOSA PERMEABILITY; MALE; MICROARRAY ANALYSIS; MICROBIAL ACTIVITY; MYCOBACTERIOSIS; MYCOBACTERIUM PARATUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEYER PATCH; PREDICTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; T LYMPHOCYTE; TISSUE SECTION;

ADAPTIVE IMMUNITY; ANIMALS; BAYES THEOREM; CATTLE; GENE EXPRESSION PROFILING; HELA CELLS; HUMANS; IMMUNE TOLERANCE; INTESTINAL MUCOSA; MALE; MYCOBACTERIUM AVIUM SUBSP. PARATUBERCULOSIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEYER'S PATCHES; SYSTEMS BIOLOGY; TIME FACTORS;

EID: 84865100072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042127     Document Type: Article

References (91)

1. Hines ME 2nd, Stabel JR, Sweeney RW, Griffin F, Talaat AM, et al. (2007) Experimental challenge models for Johne's disease: A review and proposed international guidelines. Vet Microbiol 122: 197-222.
2. Khare S, Nunes JS, Figueiredo JF, Lawhon SD, Rossetti CA, et al. (2009) Early phase morphological lesions and transcriptional responses of bovine ileum infected with Mycobacterium avium subsp. paratuberculosis. Vet Pathol 46: 717-728.
3. Momotani E, Whipple DL, Thiermann AB, Cheville NF, (1988) Role of M cells and macrophages in the entrance of Mycobacterium paratuberculosis into domes of ileal Peyer's patches in calves. Vet Pathol 25: 131-137.
4. Larsen AB, Merkal RS, Cutlip RC, (1975) Age of cattle as related to resistance to infection with Mycobacterium paratuberculosis. Am J Vet Res 36: 255-257.
5. Waters WR, Miller JM, Palmer MV, Stabel JR, Jones DE, et al. (2003) Early induction of humoral and cellular immune responses during experimental Mycobacterium avium subsp. paratuberculosis infection of calves. Infect Immun 71: 5130-5138.
6. Bendixen PH, (1977) Application of the direct leukocyte-migration agarose test in cattle from a Mycobacterium paratuberculosis-infected herd. Am J Vet Res 38: 2027-2028.
7. Weiss DJ, Evanson OA, Souza CD, (2006) Mucosal immune response in cattle with subclinical Johne's disease. Vet Pathol 43: 127-135.
8. Crawford GC, Ziccardi MH, Gonzales BJ, Woods LM, Fischer JK, et al. (2006) Mycobacterium avium subspecies paratuberculosis and Mycobacterium avium subsp. avium infections in a tule elk (Cervus elaphus nannodes) herd. J Wildl Dis 42: 715-723.
9. Murphy JT, Sommer S, Kabara EA, Verman N, Kuelbs MA, et al. (2006) Gene expression profiling of monocyte-derived macrophages following infection with Mycobacterium avium subspecies avium and Mycobacterium avium subspecies paratuberculosis. Physiol Genomics 28: 67-75.
10. Souza CD, Evanson OA, Weiss DJ, (2007) Role of the mitogen-activated protein kinase pathway in the differential response of bovine monocytes to Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. Microbes Infect 9: 1545-1552.
11. Weiss DJ, Souza CD, Evanson OA, Sanders M, Rutherford M, (2008) Bovine monocyte TLR2 receptors differentially regulate the intracellular fate of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. J Leukoc Biol 83: 48-55.
12. Souza CD, Evanson OA, Weiss DJ, (2006) Mitogen activated protein kinase p38 pathway is an important component of the anti-inflammatory response in Mycobacterium avium subsp. paratuberculosis-infected bovine monocytes. Microb Pathog 41: 59-66.
13. United States Department of Agriculture, Animal and Plant Health Inspection Service web site. Available: http://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_Johnes.pdf. Accessed 2012 July 25. Johne's Disease on U.S. Dairies, 1991-2007, (info sheet, 4p, 4/08).
14. Pierce ES, (2009) Possible transmission of Mycobacterium avium subspecies paratuberculosis through potable water: lessons from an urban cluster of Crohn's disease. Gut Pathog 1: 17.
15. Chamberlin WM, Naser SA, (2006) Integrating theories of the etiology of Crohn's disease. On the etiology of Crohn's disease: questioning the hypotheses. Med Sci Monit 12: RA27-33.
16. Lidar M, Langevitz P, Shoenfeld Y, (2009) The role of infection in inflammatory bowel disease: initiation, exacerbation and protection. Isr Med Assoc J 11: 558-563.
17. Pineton de Chambrun G, Colombel JF, Poulain D, Darfeuille-Michaud A, (2008) Pathogenic agents in inflammatory bowel diseases. Curr Opin Gastroenterol 24: 440-447.
18. Sartor RB, (2003) Targeting enteric bacteria in treatment of inflammatory bowel diseases: why, how, and when. Curr Opin Gastroenterol 19: 358-365.
19. Sartor RB, (2005) Does Mycobacterium avium subspecies paratuberculosis cause Crohn's disease? Gut 54: 896-898.
20. Knosel T, Schewe C, Petersen N, Dietel M, Petersen I, (2009) Prevalence of infectious pathogens in Crohn's disease. Pathol Res Pract 205: 223-230.
21. Waddell LA, Rajic A, Sargeant J, Harris J, Amezcua R, et al. (2008) The zoonotic potential of Mycobacterium avium spp. paratuberculosis: a systematic review. Can J Public Health 99: 145-155.
22. Kirkwood CD, Wagner J, Boniface K, Vaughan J, Michalski WP, et al. (2009) Mycobacterium avium subspecies paratuberculosis in children with early-onset Crohn's disease. Inflamm Bowel Dis 15: 1643-1655.
23. Khare S, Ficht TA, Santos RL, Romano J, Ficht AR, et al. (2004) Rapid and sensitive detection of Mycobacterium avium subsp. paratuberculosis in bovine milk and feces by a combination of immunomagnetic bead separation-conventional PCR and real-time PCR. J Clin Microbiol 42: 1075-1081.
24. Lawhon SD, Khare S, Rossetti CA, Everts RE, Galindo CL, et al. (2011) Role of SPI-1 Secreted Effectors in Acute Bovine Response to Salmonella enterica Serovar Typhimurium: A Systems Biology Analysis Approach. PLoS ONE pp. e26869.
25. Rossetti CA, Galindo CL, Everts RE, Lewin HA, Garner HR, et al. (2011) Comparative analysis of the early transcriptome of Brucella abortus-infected monocyte-derived macrophages from cattle naturally resistant or susceptible to brucellosis. Res Vet Sci 91: 40-51.
26. Loor JJ, Everts RE, Bionaz M, Dann HM, Morin DE, et al. (2007) Nutrition-induced ketosis alters metabolic and signaling gene networks in liver of periparturient dairy cows. Physiol Genomics 32: 105-116.
27. Everts RE, Band MR, Liu ZL, Kumar CG, Liu L, et al. (2005) A 7872 cDNA microarray and its use in bovine functional genomics. Vet Immunol Immunopathol 105: 235-245.
28. Adams LG, Khare S, Lawhon SD, Rossetti CA, Lewin HA, et al. (2011) Multi-comparative systems biology analysis reveals time-course biosignatures of in vivo bovine pathway responses to B.melitensis, S.enterica Typhimurium and M.avium paratuberculosis. BMC Proc 5 Suppl 4: S6.
29. Baldi P, Long AD, (2001) A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17: 509-519.
30. Long AD, Mangalam HJ, Chan BY, Tolleri L, Hatfield GW, et al. (2001) Improved statistical inference from DNA microarray data using analysis of variance and a Bayesian statistical framework. Analysis of global gene expression in Escherichia coli K12. J Biol Chem 276: 19937-19944.
31. Plattner BL, Chiang YW, Roth JA, Platt R, Huffman E, et al. (2011) Direct inoculation of Mycobacterium avium subspecies Paratuberculosis into ileocecal Peyer's patches results in colonization of the intestine in a calf model. Vet Pathol 48: 584-592.
32. Bermudez LE, Petrofsky M, Sommer S, Barletta RG, (2010) Peyer's patch-deficient mice demonstrate that Mycobacterium avium subsp. paratuberculosis translocates across the mucosal barrier via both M cells and enterocytes but has inefficient dissemination. Infect Immun 78: 3570-3577.
33. Smythies LE, Sellers M, Clements RH, Mosteller-Barnum M, Meng G, et al. (2005) Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115: 66-75.
34. Fooksman DR, Vardhana S, Vasiliver-Shamis G, Liese J, Michael L Dustin, (2011) Functional Anatomy of T Cell Activation and Synapse Formation. Annual Review of Immunology.
35. Kim M, Ogawa M, Fujita Y, Yoshikawa Y, Nagai T, et al. (2009) Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. CNature 459: 578-582.
36. Secott TE, Lin TL, Wu CC, (2004) Mycobacterium avium subsp. paratuberculosis fibronectin attachment protein facilitates M-cell targeting and invasion through a fibronectin bridge with host integrins. Infect Immun 72: 3724-3732.
37. Taupin D, Podolsky DK, (2003) Trefoil factors: initiators of mucosal healing. Nat Rev Mol Cell Biol 4: 721-732.
38. Meena LS, Rajin, (2010) Survival mechanisms of pathogenic Mycobacterium tuberculosis H37Rv. The FEBS Journal 277: 2416-2427.
39. Kusner DJ, Hall CF, Schlesinger LS, (1996) Activation of phospholipase D is tightly coupled to the phagocytosis of Mycobacterium tuberculosis or opsonized zymosan by human macrophage. J Exp Med 184: 585-595.
40. Rosales C (2005) Molecular Mechanisms of Phagocytosis: Landes Biosciences and Springer. 164 p.
41. Goldfine H, Wadsworth SJ, Johnston NC, (2000) Activation of Host Phospholipases C and D in Macrophages after Infection with Listeria monocytogenes. Infect Immun 68: 5735-41.
42. Russell DG, Cardona P-J, Kim M-J, Allain S, Altare F, (2009) Foamy macrophages and the progression of the human TB granuloma. Nat Immunol 10: 943-948.
43. Russell DG, VanderVen BC, Lee W, Abramovitch RB, Kim M, et al. (2010) Mycobacterium tuberculosis wears what it eats. Cell Host Microbe 8: 68-76.
44. Sharbati J, Lewin A, Kutz-Lohroff B, Kamal E, Einspanier R, et al. (2011) Integrated MicroRNA-mRNA-Analysis of Human Monocyte Derived Macrophages upon Mycobacterium avium subsp. hominissuis Infection. PLoS ONE 6: e20258.
45. Fratti RA, Chua J, Vergne I, Deretic V, (2003) Mycobacterium tuberculosis glycosylated phosphatidylinositol causes phagosome maturation arrest. PNAS 100: 5437-42.
46. Armstrong JA, Hart PD, (1971) Response of cultured macrophages to mycobacterium tuberculosis with observation on fusion of lysosomes with phagosomes. J Exp Med 143: 713-740.
47. Clemens DL, Horwitz MA, (1995) Characterization of the Mycobacterium tuberculosis phagosome and evidence that phagosomal maturation is inhibited. J Exp Med 181: 257-270.
48. Crowle AJ, Dahl R, Ross E, May MH, (1991) Evidence that vesicles containing living, virulent Mycobacterium tuberculosis or Mycobacterium avium in cultured human macrophages are not acidic. Infect Immun 59: 1823-1831.
49. Man SM, Kaakoush NO, Mitchell HM, (2011) The role of bacteria and pattern-recognition receptors in Crohn's disease. Nat Rev Gastroenterol Hepatol 8: 152-168.
50. Ferwerda G, Kullberg BJ, Jong DJd, Girardin SE, Langenberg DML, et al. (2007) Mycobacterium paratuberculosis is recognized by Toll-like receptors and NOD2. Journal of Leukocyte Biology 82: 1011-8.
51. Pai RK, Pennini ME, Tobian AAR, Canaday DH, Boom WH, et al. (2004) Prolonged Toll-Like Receptor Signaling by Mycobacterium tuberculosis and Its 19-Kilodalton Lipoprotein Inhibits Gamma Genes in Macrophages Interferon-Induced Regulation of Selected Genes in Macrophages. Infect Immun 72: 6603-14.
52. Baum J, Pinder M, Conway DJ, (2003) Erythrocyte Invasion Phenotypes of Plasmodium falciparum in the Gambia. Infect Immun 71: 1856-63.
53. McKenna HJ, Stocking KL, Miller RE, Brasel K, Smedt TD, et al. (2009) Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95: 3489-3497.
54. Sommer S, Pudrith CB, Colvin CJ, Coussens PM, (2009) Mycobacterium avium subspecies paratuberculosis suppresses expression of IL-12p40 and iNOS genes induced by signalling through CD40 in bovine monocyte-derived macrophages. Vet Immunol Immunopathol 128: 44-52.
55. Young LS, Eliopoulos AG, Gallagher NJ, Dawson CW, (1998) CD40 and epithelial cells: across the great divide. Immunol Today 19: 502-506.
56. Legler DF, Loetscher M, Roos RS, Clark-Lewis I, Baggiolini M, et al. (1998) B Cell-attracting Chemokine 1, a Human CXC Chemokine Expressed in Lymphoid Tissues, Selectively Attracts B Lymphocytes via BLR1/CXCR5. J Exp Med 187: 655-660.
57. Tiffany HL, Lautens LL, Gao J-L, Pease J, Locati M, et al. (1997) Identification of CCR8: A Human Monocyte and Thymus Receptor for the CC Chemokine I-309. J Exp Med 186: 165-170.
58. Greenwell-Wild T, Vázquez N, Sim D, Schito M, Chatterjee D, et al. (2002) Mycobacterium avium Infection and Modulation of Human Macrophage Gene Expression. The Journal of Immunology 169: 6286-6297.
59. Tilg H, Moschen AR, (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature Reviews Immunology 6: 772-783.
60. van Leeuwen IM, Mirams GR, Walter A, Fletcher A, Murray P, et al. (2009) An integrative computational model for intestinal tissue renewal. Cell Prolif 42: 617-636.
61. Missler M, Fernandez-Chacon R, Sudhof TC, (1998) The making of neurexins. J Neurochem 71: 1339-1347.
62. Missler M, Hammer RE, Sudhof TC, (1998) Neurexophilin binding to alpha-neurexins. A single LNS domain functions as an independently folding ligand-binding unit. J Biol Chem 273: 34716-34723.
63. Missler M, Sudhof TC, (1998) Neurexophilins form a conserved family of neuropeptide-like glycoproteins. J Neurosci 18: 3630-3638.
64. Barthalay Y, Hipeau-Jacquotte R, de la Escalera S, Jimenez F, Piovant M, (1990) Drosophila neurotactin mediates heterophilic cell adhesion. Embo J 9: 3603-3609.
65. Furness J, (2008) The enteric nervous system: normal functions and enteric neuropathies. Neurogastroenterol Motil 20 Suppl 1: 32-38.
66. Scanu AM, Bull TJ, Cannas S, Sanderson JD, Sechi LA, et al. (2007) Mycobacterium avium subspecies paratuberculosis infection in cases of irritable bowel syndrome and comparison with Crohn's disease and Johne's disease: common neural and immune pathogenicities. J Clin Microbiol 45: 3883-3890.
67. Sechi LA, Ruehl A, Ahmed N, Usai D, Paccagnini D, et al. (2007) Mycobacterium avium subspecies paratuberculosis infects and multiplies in enteric glial cells. World J Gastroenterol 13: 5731-5735.
68. Buergelt CD, Hall C, McEntee K, Duncan JR, (1978) Pathological evaluation of paratuberculosis in naturally infected cattle. Vet Pathol 15: 196-207.
69. Gwozdz JM, Thompson KG, Manktelow BW, (2001) Lymphocytic neuritis of the ileum in sheep with naturally acquired and experimental paratuberculosis. J Comp Pathol 124: 317-320.
70. Courtemanche C, Elson-Schwab I, Mashiyama ST, Kerry N, Ames BN, (2004) Folate deficiency inhibits the proliferation of primary human CD8+ T lymphocytes in vitro. J Immunol 173: 3186-3192.
71. Krajinovic M, (2004) MTHFD1 gene: role in disease susceptibility and pharmacogenetics. J Immunol 173: 3186-3192.
72. Nyhan WL, (2005) Disorders of purine and pyrimidine metabolism. Mol Genet Metab 86: 25-33.
73. Shi L, Chowdhury SM, Smallwood HS, Yoon H, Mottaz-Brewer HM, et al. (2009) Proteomic Investigation of the Time Course Responses of RAW 264.7 Macrophages to Infection with Salmonella enterica. Infect Immun 77: 3227-3233.
74. Lin JE, Snook AE, Li P, Stoecker BA, Kim GW, et al. (2012) GUCY2C Opposes Systemic Genotoxic Tumorigenesis by Regulating AKT-Dependent Intestinal Barrier Integrity. PLoS One 7: e31686.
75. Hwang I-Y, Park C, Harrision K, Huang N-N, Kehrl JH, (2011) Variations in Gnai2 and Rgs1 Expression Affect Chemokine Receptor Signaling and the Organization of Secondary Lymphoid Organs. Genes Immun 11: 384-396.
76. Olsen I, Boysen P, Kulberg S, Hope JC, Jungersen G, et al. (2005) Bovine NK cells can produce gamma interferon in response to the secreted mycobacterial proteins ESAT-6 and MPP14 but not in response to MPB70. Infect Immun 73: 5628-5635.
77. Singh UP, Singh R, Singh S, Karls RK, Quinn FD, et al. (2008) CXCL10+ T cells and NK cells assist in the recruitment and activation of CXCR3+ and CXCL11+ leukocytes during Mycobacteria-enhanced colitis. BMC Immunol 9: 25-32.
78. Boyce JA, (2003) Mast cells: beyond IgE. J Allergy Clin Immunol 111: 24-32.
79. Alzuherri HMLD, Clarke CJ, (1997) Altered intestinal macrophage phenotype in ovine paratuberculosis. Res Vet Sci 63: 139-143.
80. Berger STGF, (2006) A comparison of ovine monocyte-derived macrophage function following infection with Mycobacterium avium ssp. avium and Mycobacterium avium ssp. paratuberculosis. Immunol Cell Biol 84: 349-356.
81. Ferwerda GKB, de Jong DJ, Girardin SE, Langenberg DM, van Crevel R, et al. (2007) Mycobacterium paratuberculosis is recognized by Toll-like receptors and NOD2. J Leukoc Biol 82: 1011-1018.
82. Lei LHJ, (2007) Limited phenotypic and functional maturation of bovine monocyte-derived dendritic cells following Mycobacterium avium subspecies paratuberculosis infection in vitro. Vet Immunol Immunopathol 120: 177-186.
83. Purdie ACPK, Begg DJ, de Silva K, Whittington RJ, (2012) Expression of genes associated with the antigen presentation and processing pathway are consistently regulated in early Mycobacterium avium subsp. paratuberculosis infection. Comp Immunol Microbiol Infect Dis 35: 151-162.
84. Ruiz-Larrañaga OMC, Iriondo M, Garrido JM, Molina E, Vazquez P, et al. (2011) Genetic variation of toll-like receptor genes and infection by Mycobacterium avium ssp. paratuberculosis in Holstein-Friesian cattle. J Dairy Sci pp. 3635-3641.
85. Taylor DLZL, Begg DJ, de Silva K, Whittington RJ, (2008) Toll-like receptor genes are differentially expressed at the sites of infection during the progression of Johne's disease in outbred sheep. Vet Immunol Immunopathol 124: 132-151.
86. Weiss DJEO, McClenahan DJ, Abrahamsen MS, Walcheck BK, (2001) Regulation of expression of major histocompatibility antigens by bovine macrophages infected with Mycobacterium avium subsp. paratuberculosis or Mycobacterium avium subsp. avium. Infect Immun 96: 1002-1008.
87. Berger ST, Griffin FT, (2006) A comparison of ovine monocyte-derived macrophage function following infection with Mycobacterium avium ssp. avium and Mycobacterium avium ssp. paratuberculosis. Immunol Cell Biol 84: 349-356.
88. Weiss DJ, Evanson OA, McClenahan DJ, Abrahamsen MS, Walcheck BK, (2001) Regulation of expression of major histocompatibility antigens by bovine macrophages infected with Mycobacterium avium subsp. paratuberculosis or Mycobacterium avium subsp. avium. Infect Immun 69: 1002-1008.
89. Weiss DJ, Souza CD, (2008) Review paper: modulation of mononuclear phagocyte function by Mycobacterium avium subsp. paratuberculosis. Vet Pathol 45: 829-841.
90. Chalupsky K, Cai H, (2005) Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci U S A 102: 9056-9061.
91. Polymeros D, Bogdanos DP, Day R, Arioli D, Vergani D, et al. (2006) Does cross-reactivity between mycobacterium avium paratuberculosis and human intestinal antigens characterize Crohn's disease? Gastroenterology 131: 85-96.