Entrance and survival of Brucella pinnipedialis hooded seal strain in human macrophages and epithelial cells

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Larsen, Anett K ^a,b   Nymo, Ingebjørg H ^a,b   Briquemont, Benjamin ^c   Sørensen, Karen K ^d   Godfroid, Jacques ^a,b  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b Fram Centre   (Norway)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE;

ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BRUCELLA; BRUCELLA PINNIPEDIALIS; CELL COMPARTMENTALIZATION; CELL DEATH; CELL STRAIN; CELL STRAIN HELA S3; CELL STRAIN J774A.1; CELL STRAIN RAW264.7; CELL STRAIN THP 1; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; INTERNALIZATION; LIPID RAFT; LYSOSOME; MACROPHAGE; MICROBIAL ACTIVITY; MOUSE; NONHUMAN; PHAGOCYTE; SEAL;

ANIMALS; BRUCELLA; CELL LINE; EPITHELIAL CELLS; GENTAMICINS; HUMANS; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; SEALS, EARLESS; ZOONOSES;

EID: 84893205506     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084861     Document Type: Article

References (64)

1. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV (2006) The new global map of human brucellosis. Lancet Infect Dis 6: 91-99. doi:10.1016/S1473-3099(06)70382-6. PubMed: 16439329. (Pubitemid 43138907)
2. Corbel MJ, Brinley-Morgan WJ (1984) Genus Brucella. In: NR KriegJG Hold. Bergey Manual of Systematic. Journal of Bacteriology, Vol 1. Baltimore /London: Williams and Wilkins. pp. 377-388.
3. Foster G, Osterman BS, Godfroid J, Jacques I, Cloeckaert A (2007) Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred hosts. Int J Syst Evol Microbiol 57: 2688-2693. doi:10.1099/ijs.0.65269-0. PubMed: 17978241. (Pubitemid 350187441)
4. Scholz HC, Hubalek Z, Sedlácek I, Vergnaud G, Tomaso H et al. (2008) Brucella microti sp. nov., isolated from the common vole Microtus arvalis. Int J Syst Evol Microbiol 58: 375-382. doi:10.1099/ijs.0.65356-0. PubMed: 18218934. (Pubitemid 351298409)
5. Scholz HC, Nöckler K, Göllner C, Bahn P, Vergnaud G et al. (2010) Brucella inopinata sp. nov., isolated from a breast implant infection. Int J Syst Evol Microbiol 60: 801-808. doi:10.1099/ijs.0.011148-0. PubMed: 19661515.
6. Godfroid J, Scholz HC, Barbier T, Nicolas C, Wattiau P et al. (2011) Brucellosis at the animal/ecosystem/human interface at the beginning of the 21st century. Prev Vet Med 102: 118-131. doi:10.1016/j.prevetmed.2011.04.007. PubMed: 21571380.
7. Ewalt DR, Payeur JB, Martin BM, Cummins DR, Miller WG (1994) Characteristics of a Brucella species from a bottlenose dolphin (Tursiops truncatus). J Vet Diagn Invest 6: 448-452. doi: 10.1177/104063879400600408. PubMed: 7858024.
8. Ross HM, Foster G, Reid RJ, Jahans KL, MacMillan AP (1994) Brucella species infection in sea-mammals. Vet Rec 134: 359. doi:10.1136/vr.134.14.359-b. PubMed: 8017020.
9. Nymo IH, Tryland M, Godfroid J (2011) A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Vet Res 42: 93. doi: 10.1186/1297-9716-42-93. PubMed: 21819589.
10. Foster G, MacMillan AP, Godfroid J, Howie F, Ross HM et al. (2002) A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland. Vet Microbiol 90: 563-580. doi: 10.1016/S0378-1135(02) 00236-5. PubMed: 12414172. (Pubitemid 35279903)
11. Bingham J, Taylor TK, Swingler JE, Meehan G, Middleton DJ et al. (2008) Infection trials in pigs with a human isolate of Brucella (isolate 02/611 'marine mammal type'). N Z Vet J 56: 10-14. doi: 10.1080/00480169.2008.36798. PubMed: 18322554. (Pubitemid 351440026)
12. Perrett LL, Brew SD, Stack JA, MacMillan AP, Bashiruddin JB (2004) Experimental assessment of the pathogenicity of Brucella strains from marine mammals for pregnant sheep. Small Ruminant Res 51: 221-228. doi:10.1016/S0921- 4488(03)00233-5. (Pubitemid 38214901)
13. Rhyan JC, Gidlewski T, Ewalt DR, Hennager SG, Lambourne DM et al. (2001) Seroconversion and abortion in cattle experimentally infected with Brucella sp. isolated from a Pacific harbor seal (Phoca vitulina richardsi). J Vet Diagn Invest 13: 379-382. doi: 10.1177/104063870101300502. PubMed: 11580057. (Pubitemid 33646043)
14. Brew SD, Perrett LL, Stack JA, MacMillan AP, Staunton NJ (1999) Human exposure to Brucella recovered from a sea mammal. Vet Rec 144: 483. PubMed: 10358880. (Pubitemid 29197021)
15. McDonald WL, Jamaludin R, Mackereth G, Hansen M, Humphrey S et al. (2006) Characterization of a Brucella sp. strain as a marine-mammal type despite isolation from a patient with spinal osteomyelitis in New Zealand. J Clin Microbiol 44: 4363-4370. doi:10.1128/JCM.00680-06. PubMed: 17035490. (Pubitemid 44937065)
16. Sohn AH, Probert WS, Glaser CA, Gupta N, Bollen AW et al. (2003) Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerg Infect Dis 9: 485-488. doi: 10.3201/eid0904.020576. PubMed: 12702232. (Pubitemid 37070418)
17. Whatmore AM, Dawson CE, Groussaud P, Koylass MS, King AC et al. (2008) Marine mammal Brucella genotype associated with zoonotic infection. Emerg Infect Dis 14: 517-518. doi:10.3201/eid1403.070829. PubMed: 18325282. (Pubitemid 351451414)
18. El-Tras WF, Tayel AA, Eltholth MM, Guitian J (2010) Brucella infection in fresh water fish: Evidence for natural infection of Nile catfish, Clarias gariepinus, with Brucella melitensis. Vet Microbiol 141: 321-325. doi: 10.1016/j.vetmic.2009.09.017. PubMed: 19880265.
19. Perrett LL, Dawson CE, Davison N, Quinney S (2004) Brucella infection of lungworms from a harbour porpoise. Vet Rec 154: 800. PubMed: 15233465. (Pubitemid 38877723)
20. Garner MM, Lambourn DM, Jeffries SJ, Hall PB, Rhyan JC et al. (1997) Evidence of Brucella infection in Parafilaroides lungworms in a Pacific harbor seal (Phoca vitulina richardsi). J Vet Diagn Invest 9: 298-303. doi:10.1177/104063879700900311. PubMed: 9249169. (Pubitemid 127689703)
21. Liautard JP, Gross A, Dornand J, Köhler S (1996) Interactions between professional phagocytes and Brucella spp. Microbiologia 12: 197-206. PubMed: 8767704.
22. Pizarro-Cerdá J, Méresse S, Parton RG, van der Goot G, Sola-Landa A et al. (1998) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66: 5711-5724. PubMed: 9826346. (Pubitemid 28531826)
23. von Bargen K, Gorvel JP, Salcedo SP (2012) Internal affairs: investigating the Brucella intracellular lifestyle. FEMS Microbiol Rev 36: 533-562. doi:10.1111/j.1574-6976.2012.00334.x. PubMed: 22373010.
24. Maquart M, Zygmunt MS, Cloeckaert A (2009) Marine mammal Brucella isolates with different genomic characteristics display a differential response when infecting human macrophages in culture. Microbes Infect 11: 361-366. doi:10.1016/j.micinf.2008.12.012. PubMed: 19397885.
25. Tryland M, Kleivane L, Alfredsson A, Kjeld M, Arnason A et al. (1999) Evidence of Brucella infection in marine mammals in the North Atlantic Ocean. Vet Rec 144: 588-592. doi:10.1136/vr.144.21.588. PubMed: 10378290. (Pubitemid 129545025)
26. Tryland M, Sørensen KK, Godfroid J (2005) Prevalence of Brucella pinnipediae in healthy hooded seals (Cystophora cristata) from the North Atlantic Ocean and ringed seals (Phoca hispida) from Svalbard. Vet Microbiol 105: 103-111. doi:10.1016/j.vetmic.2004.11.001. PubMed: 15627521. (Pubitemid 41373288)
27. ICES (2006) Report of the ICES/NAFO working group on harp and hooded seals (WGHARP), 12-16 June, Copenhagen, Denmark. Lund S, Anthony B, editors. pp 1-28. International Council for the Exploration of the Sea (ICES) website. Available: http://www.ices.dk/sites/pub/PublicationReports/ICES-AnnualReport/ 2006AnnualReport-LR.pdf. Accessed 2013 Aug 15
28. Roop RM, Gaines JM, Anderson ES, Caswell CC, Martin DW (2009) Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol 198: 221-238. doi:10.1007/s00430-009-0123-8. PubMed: 19830453.
29. Larsen AK, Nymo IH, Boysen P, Tryland M, Godfroid J (2013) Entry and elimination of marine mammal Brucella spp. by hooded seal (Cystophora cristata) alveolar macrophages in vitro. PLOS ONE 8(7): e70186. doi:10.1371/journal.pone. 0070186. PubMed: 23936159.
30. Nymo IH, Tryland M, Frie AK, Haug T, Foster G et al. (2013) Age-dependent prevalence of anti-Brucella antibodies in hooded seals (Cystophora cristata). DAO. doi:10.3354/dao02659. Available: http://www.int-res.com/prepress/d02659. html. Accessed 2013 October 24
31. Lambourn DM, Garner M, Ewalt D, Raverty S, Sidor I et al. (2013) Brucella pinnipedialis infections in Pacific harbor seals (Phoca vitulina richardsi) from Washington State, USA. J Wildl Dis 49: 802-815. doi: 10.7589/2012-05-137.
32. Bohlin J, Snipen L, Cloeckaert A, Lagesen K, Ussery D et al. (2010) Genomic comparisons of Brucella spp. and closely related bacteria using base compositional and proteome based methods. BMC Evol Biol 10: 249. doi:10.1186/1471-2148-10-249. PubMed: 20707916.
33. Alton GG, Jones LM, Pietz DE (1975) Laboratory techniques in brucellosis. Monogr Ser World Health Organ: 1-163. PubMed: 812265.
34. OIE World Organization for Animal Health (2013) Bovine Brucellosis. Office International des Epizooties, Paris, France. World Organization for Animal Health website. Available: http://www.oie.int/manual-of-diagnostic-tests- and-vaccines-for-terrestrial-animals/. Accessed 2013 Aug 15
35. Cloeckaert A, Grayon M, Grepinet O (2000) An IS711 element downstream of the bp26 gene is a specific marker of Brucella spp. isolated from marine mammals. Clin Diagn Lab Immunol 7: 835-839. PubMed: 10973465.
36. Le Flèche P, Jacques I, Grayon M, Al Dahouk S, Bouchon P et al. (2006) Evaluation and selection of tandem repeat loci for a Brucella MLVA typing assay. BMC Microbiol 6: 9. doi:10.1186/1471-2180-6-9. PubMed: 16469109.
37. Maquart M, Le FP, Foster G, Tryland M, Ramisse F et al. (2009) MLVA-16 typing of 295 marine mammal Brucella isolates from different animal and geographic origins identifies 7 major groups within Brucella ceti and Brucella pinnipedialis. BMC Microbiol 9: 145. doi: 10.1186/1471-2180-9-145. PubMed: 19619320.
38. Tsuchiya S, Kobayashi Y, Goto Y, Okumura H, Nakae S et al. (1982) Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester. Cancer Res 42: 1530-1536. PubMed: 6949641. (Pubitemid 12148801)
39. Slot JW, Geuze HJ (2007) Cryosectioning and immunolabeling. Nat Protoc 2: 2480-2491. doi:10.1038/nprot.2007.365. PubMed: 17947990.
40. Martín-Martín AI, Vizcaíno N, Fernández-Lago L (2010) Cholesterol, ganglioside GM1 and class A scavenger receptor contribute to infection by Brucella ovis and Brucella canis in murine macrophages. Microbes Infect 12: 246-251. doi:10.1016/j.micinf.2009.12.008. PubMed: 20083220.
41. Fang FC, Vazquez-Torres A (2002) Nitric oxide production by human macrophages: there's NO doubt about it. Am J Physiol-Lung C 202: L941-L943. (Pubitemid 34654609)
42. Baucheron S, Grayon M, Zygmunt MS, Cloeckaert A (2002) Lipopolysaccharide heterogeneity in Brucella strains isolated from marine mammals. Res Microbiol 153: 277-280. doi:10.1016/S0923-2508(02)01317-7. PubMed: 12160318. (Pubitemid 34626785)
43. Jahans KL, Foster G, Broughton ES (1997) The characterisation of Brucella strains isolated from marine mammals. Vet Microbiol 57: 373-382. doi:10.1016/S0378-1135(97)00118-1. PubMed: 9444074. (Pubitemid 27515865)
44. Kim S, Watarai M, Suzuki H, Makino S, Kodama T et al. (2004) Lipid raft microdomains mediate class A scavenger receptor-dependent infection of Brucella abortus. Microb Pathog 37: 11-19. doi:10.1016/j.micpath.2004.04.002. PubMed: 15194155. (Pubitemid 38759614)
45. Naroeni A, Porte F (2002) Role of cholesterol and the ganglioside GM(1) in entry and short-term survival of Brucella suis in murine macrophages. Infect Immun 70: 1640-1644. doi:10.1128/IAI.70.3.1640-1644.2002. PubMed: 11854258. (Pubitemid 34163449)
46. Watarai M, Makino S, Fujii Y, Okamoto K, Shirahata T (2002) Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol 4: 341-355. doi:10.1046/j.1462-5822.2002.00195.x. PubMed: 12067319. (Pubitemid 34727538)
47. Pei J, Turse JE, Ficht TA (2008) Evidence of Brucella abortus OPS dictating uptake and restricting NF-kappaB activation in murine macrophages. Microbes Infect 10: 582-590. doi:10.1016/j.micinf.2008.01.005. PubMed: 18457975.
48. Porte F, Naroeni A, Ouahrani-Bettache S, Liautard JP (2003) Role of the Brucella suis lipopolysaccharide O antigen in phagosomal genesis and in inhibition of phagosome-lysosome fusion in murine macrophages. Infect Immun 71: 1481-1490. doi:10.1128/IAI.71.3.1481-1490.2003. PubMed: 12595466. (Pubitemid 36254335)
49. Jiménez de Bagüés MP, Terraza A, Gross A, Dornand J (2004) Different responses of macrophages to smooth and rough Brucella spp.: relationship to virulence. Infect Immun 72: 2429-2433. doi: 10.1128/IAI.72.4. 2429-2433.2004. PubMed: 15039375. (Pubitemid 38419966)
50. Pei J, Ficht TA (2004) Brucella abortus rough mutants are cytopathic for macrophages in culture. Infect Immun 72: 440-450. doi:10.1128/IAI.72.1.440-450. 2004. PubMed: 14688125. (Pubitemid 38018205)
51. Cloeckaert A, Weynants V, Godfroid J, Verger JM, Grayon M et al. (1998) O-Polysaccharide epitopic heterogeneity at the surface of Brucella spp. studied by enzyme-linked immunosorbent assay and flow cytometry. Clin Diagn Lab Immunol 5: 862-870. PubMed: 9801349. (Pubitemid 28519266)
52. Zaccheus MV, Ali T, Cloeckaert A, Zygmunt MS, Weintraub A, et al. (2013) The epitopic and structural characterization of Brucella suis biovar 2 O-polysaccharide demonstrates the existence of a new Mnegative C-negative smooth Brucella serovar. PLOS ONE 8: e53941. doi: 10.1371/journal.pone.0053941.
53. Rittig MG, Kaufmann A, Robins A, Shaw B, Sprenger H et al. (2003) Smooth and rough lipopolysaccharide phenotypes of Brucella induce different intracellular trafficking and cytokine/chemokine release in human monocytes. J Leukoc Biol 74: 1045-1055. doi:10.1189/jlb.0103015. PubMed: 12960272. (Pubitemid 38040326)
54. Fernandez-Prada CM, Zelazowska EB, Nikolich M, Hadfield TL, Roop RM et al. (2003) Interactions between Brucella melitensis and human phagocytes: bacterial surface O-Polysaccharide inhibits phagocytosis, bacterial killing, and subsequent host cell apoptosis. Infect Immun 71: 2110-2119. doi:10.1128/IAI.71.4.2110-2119.2003. PubMed: 12654833. (Pubitemid 36368746)
55. Atluri VL, Xavier MN, de Jong MF, den Hartigh AB, Tsolis RE (2011) Interactions of the human pathogenic Brucella species with their hosts. Annu Rev Microbiol 65: 523-541. doi:10.1146/annurev-micro-090110-102905. PubMed: 21939378.
56. Starr T, Child R, Wehrly TD, Hansen B, Hwang S et al. (2012) Selective subversion of autophagy complexes facilitates completion of the Brucella intracellular cycle. Cell Host Microbe 11: 33-45. doi:10.1016/j.chom.2011.12. 002. PubMed: 22264511.
57. Köhler S, Michaux-Charachon S, Porte F, Ramuz M, Liautard JP (2003) What is the nature of the replicative niche of a stealthy bug named Brucella? Trends Microbiol 11: 215-219. doi:10.1016/S0966-842X(03)00078-7. PubMed: 12781524.
58. Pizarro-Cerdá J, Moreno E, Sanguedolce V, Mege JL, Gorvel JP (1998) Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments. Infect Immun 66: 2387-2392. PubMed: 9573138. (Pubitemid 28194151)
59. Pizarro-Cerdá J, Moreno E, Gorvel JP (2000) Invasion and intracellular trafficking of Brucella abortus in nonphagocytic cells. Microbes Infect 2: 829-835. doi:10.1016/S1286-4579(00)90368-X. PubMed: 10955964. (Pubitemid 30451225)
60. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH (2010) The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PLOS ONE 5: e8668. doi:10.1371/journal. pone.0008668. PubMed: 20084270.
61. Schwende H, Fitzke E, Ambs P, Dieter P (1996) Differences in the state of differentiation of THP-1 cells induced by phorbol ester and 1,25-dihydroxyvitamin D3. J Leukoc Biol 59: 555-561. PubMed: 8613704. (Pubitemid 26156616)
62. Brubaker M, Berner MD, Butler J, Bradley M (2010) Brucellosis: Understanding an important Arctic infectious disease. Center for Climate and Health, Alaska Native Tribal Health Consortium, CCH Bulletin: 5. Alaska Native Tribal Health Consortium webpage. Available: http://www.anthc.org/chs/ces/ climate/upload/CCH-Bulletin-No-5-Brucellosis-Understanding-an-Important-Arctic- Infectious-Disease-4.pdf. Accessed 2013 Aug 15
63. Chan J, Baxter C, Wenman WM (1989) Brucellosis in an inuit child, probably related to caribou meat consumption. Scand J Infect Dis 21: 337-338. doi:10.3109/00365548909035706. PubMed: 2569231. (Pubitemid 19163196)
64. Young EJ (1983) Human Brucellosis. Review of Infectious Diseases 5: 821-842. doi:10.1093/clinids/5.5.821.