An immunocompromised murine model of chronic Bartonella infection

American Journal of Pathology

Volumn 176, Issue 6, 2010, Pages 2753-2763

  Chiaraviglio, Lucius ^a   Duong, Scott ^a   Brown, Daniel A ^a   Birtles, Richard J ^b   Kirby, James E ^a  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BARTONELLA; BARTONELLA TAYLORII; BARTONELLOSIS; CELL AGGREGATION; CELL DIVISION; CELL TYPE; CONTROLLED STUDY; DISEASE SEVERITY; ENDOTHELIUM CELL; HOST PARASITE INTERACTION; IMMUNE RESPONSE; MOUSE; MURINAE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CAT; CAT SCRATCH DISEASE; DISEASE MODEL; HUMAN; IMMUNOCOMPROMISED PATIENT; IMMUNOLOGY; KIDNEY; LIVER; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; SCID MOUSE; SPLEEN; TRENCH FEVER; VETERINARY;

ANIMALS; BARTONELLA; BARTONELLA INFECTIONS; CAT-SCRATCH DISEASE; CATS; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOCOMPROMISED HOST; KIDNEY; LIVER; MICE; MICE, SCID; SPLEEN; TRENCH FEVER;

EID: 77953219736     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090862     Document Type: Article

References (57)

1. Breitschwerdt EB, Kordick DL: Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin Microbiol Rev 2000, 13:428-438
2. Maggi RG, Raverty SA, Lester SJ, Huff DG, Haulena M, Ford SL, Nielsen O, Robinson JH, Breitschwerdt EB: Bartonella henselae in captive and hunter-harvested beluga (Delphinapterus leucas). J Wildl Dis 2008, 44:871-877
3. Fournier PE, Taylor C, Rolain JM, Barrassi L, Smith G, Raoult D: Bartonella australis sp. nov. from kangaroos, Australia. Emerg Infect Dis 2007, 13:1961-1962
4. Concannon R, Wynn-Owen K, Simpson VR, Birtles RJ: Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology 2005, 131:489-496
5. Telfer S, Begon M, Bennett M, Bown KJ, Burthe S, Lambin X, Telford G, Birtles R: Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics. Parasitology 2007, 134:413-425
6. Dehio C, Lanz C, Pohl R, Behrens P, Bermond D, Piemont Y, Pelz K, Sander A: Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int J Syst Evol Microbiol 2001, 51:1557-1565
7. Valentine KH, Harms CA, Cadenas MB, Birkenheuer AJ, Marr HS, Braun-McNeill J, Maggi RG, Breitschwerdt EB: Bartonella DNA in loggerhead sea turtles. Emerg Infect Dis 2007, 13:949-950
8. Bai Y, Kosoy MY, Ray C, Brinkerhoff RJ, Collinge SK: Temporal and spatial patterns of Bartonella infection in black-tailed prairie dogs (Cynomys ludovicianus). Microb Ecol 2008, 56:373-382
9. Mediannikov O, Ivanov L, Zdanovskaya N, Vysochina N, Fournier PE, Tarasevich I, Raoult D: Molecular screening of Bartonella species in rodents from the Russian Far East. Ann N Y Acad Sci 2005, 1063:308-311
10. Matsumoto K, Berrada ZL, Klinger E, Goethert HK, Telford SR 3rd: Molecular detection of Bartonella schoenbuchensis from ectoparasites of deer in Massachusetts, Vector Borne Zoonotic Dis 2008, 8:549-554
11. Cherry NA, Maggi RG, Cannedy AL, Breitschwerdt EB: PCR detection of Bartonella bovis and Bartonella henselae in the blood of beef cattle. Vet Microbiol 2009, 135:308-312
12. Anderson BE, Neuman MA: Bartonella spp. as emerging human pathogens. Clin Microbiol Rev 1997, 10:203-219
13. Sander A, Posselt M, Oberle K, Bredt W: Seroprevalence of antibodies to Bartonella henselae in patients with cat scratch disease and in healthy controls: evaluation and comparison of two commercial serological tests. Clin Diagn Lab Immunol 1998, 5:486-490
14. Iralu J, Bai Y, Crook L, Tempest B, Simpson G, Mckenzie T, Koster F: Rodent-associated Bartonella febrile illness, Southwestern United States. Emerg Infect Dis 2006, 12:1081-1086
15. Recavarren S, Lumbreras H: Pathogenesis of the verruga of Carrion's disease. Ultrastructural studies. Am J Pathol 1972, 66:461-470
16. Perkocha LA, Geaghan SM, Yen TS, Nishimura SL, Chan SP, Garcia-Kennedy R, Honda G, Stoloff AC, Klein HZ, Goldman RL: Clinical and pathological features of bacillary peliosis hepatis in association with human immunodeficiency virus infection. N Engl J Med 1990, 323:1581-1586
17. Conley T, Slater L, Hamilton K: Rochalimaea species stimulate human endothelial cell proliferation and migration in vitro. J Lab Clin Med 1994, 124:521-528
18. Dehio C: Recent progress in understanding Bartonella-induced vascular proliferation. Curr Opin Microbiol 2003, 6:61-65
19. Kempf VA, Volkmann B, Schaller M, Sander CA, Alitalo K, Riess T, Autenrieth IB: Evidence of a leading role for VEGF in Bartonella henselae-induced endothelial cell proliferations. Cell Microbiol 2001, 3:623-632
20. Kirby JE, Nekorchuk DM: Bartonella-associated endothelial proliferation depends on inhibition of apoptosis. Proc Natl Acad Sci U S A 2002, 99:4656-4661
21. Kirby JE: In vitro model of Bartonella henselae-induced angiogenesis. Infect Immun 2004, 72:7315-7317
22. Regnath T, Mielke ME, Arvand M, Hahn H: Murine model of Bartonella henselae infection in the immunocompetent host. Infect Immun 1998, 66:5534-5536
23. Velho PS, Moraes AM, Cintra ML, Giglioli R, Goncalves SA, Shlessarenko N, Camargo ME: Baccilary angiomatosis: negative results using normal Balb/c and Balb/c nude mice. Braz J Infect Dis 1998, 2:300-303
24. Koesling J, Aebischer T, Falch C, Schulein R, Dehio C: Cutting edge: antibody-mediated cessation of hemotropic infection by the intraerythrocytic mouse pathogen Bartonella grahamii. J Immunol 2001, 167:11-14
25. Kitchell BE, Fan TM, Kordick D, Breitschwerdt EB, Wollenberg G, Lichtensteiger CA: Peliosis hepatis in a dog infected with Bartonella henselae. J Am Vet Med Assoc 2000, 216:519-523
26. Maeno N, Oda H, Yoshiie K, Wahid MR, Fujimura T, Matayoshi S: Live Bartonella henselae enhances endothelial cell proliferation without direct contact. Microb Pathog 1999, 27:419-427
27. Cockerell CJ, LeBoit PE: Bacillary angiomatosis: a newly characterized, pseudoneoplastic, infectious, cutaneous vascular disorder. J Am Acad Dermatol 1990, 22:501-512
28. Chomel BB, Kasten RW, Sykes JE, Boulouis HJ, Breitschwerdt EB: Clinical impact of persistent Bartonella bacteremia in humans and animals 2003, 990:267-278
29. Meininger GR, Nadasdy T, Hruban RH, Bollinger RC, Baughman KL, Hare JM: Chronic active myocarditis following acute Bartonella henselae infection (cat scratch disease). Am J Surg Pathol 2001, 25:1211-1214
30. Breitschwerdt EB, Maggi RG: Comparative medical features of canine and human bartonellosis. Clinical Microbiology and Infection 2009, 15:106-107
31. Maman E, Bickels J, Ephros M, Paran D, Comaneshter D, Metzkor-Cotter E, Avidor B, Varon-Graidy M, Wientroub S, Giladi M: Musculoskeletal manifestations of cat scratch disease. Clin Infect Dis 2007, 45:1535-1540
32. Birtles RJ, Hazel SM, Bennett M, Bown K, Raoult D, Begon M: Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect 2001, 126:323-329
33. Birtles RJ, Harrison TG, Saunders NA, Molyneux DH: Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov. Bartonella peromysci comb nov, and three new species, Bartonella grahamii sp nov, Bartonella taylorii sp nov, and Bartonella doshiae sp nov. Int J Syst Bacteriol 1995, 45:1-8
34. Kyme P, Dillon B, Iredell J: Phase variation in Bartonella henselae. Microbiology 2003, 149:621-629
35. Gilmore RD Jr, Bellville TM, Sviat SL, Frace M: The Bartonella vinsonii subsp. arupensis immunodominant surface antigen BrpA gene. Encoding a 382-kilodalton protein composed of repetitive sequences, is a member of a multigene family conserved among bartonella species. Infect Immun 2005, 73:3128-3136
36. Riess T, Andersson S, Lupas A, Schaller M, Schafer A, Kyme P, Martin J, Walzlein JH, Ehehalt U, Lindroos H, Schirle M, Nordheim A, Autenrieth IB, Kempf VA: Bartonella adhesin A mediates a proangiogenic host cell response. J Exp Med 2004, 200:1267-1278
37. Batterman HJ, Peek JA, Loutit JS, Falkow S, Tompkins LS: Bartonella henselae and Bartonella quintana adherence to and entry in cultured human epithelial cells. Infect Immun 1995, 63:4553-4556
38. Warren K, Goldstein E, Hung VS, Koehler JE, Richardson W: Use of retinal biopsy to diagnose Bartonella (formerly Rochalimaea) henselae retinitis in an HIV-infected patient. Arch Ophthalmol 1998, 116:937-940
39. Bender E, Silver FH, Hayashi K, Trelstad RL: Type I collagen segment long spacing banding patterns. Evidence that the alpha 2 chain is in the reference or A position. J Biol Chem 1982, 257:9653-9657
40. Ortolani F, Marchini M: Cartilage type II collagen fibrils show distinctive negative-staining band patterns differences between type II and type I unfixed or glutaraldehyde-fixed collagen fibrils. J Electron Microsc (Tokyo) 1995, 44:365-375
41. Slater LN, Pitha JV, Herrera L, Hughson MD, Min KW, Reed JA: Rochalimaea henselae infection in acquired immunodeficiency syndrome causing inflammatory disease without angiomatosis or peliosis. Demonstration by immunocytochemistry and corroboration by DNA amplification. Arch Pathol Lab Med 1994, 118:33-38
42. Lynch AS, Robertson GT: Bacterial and fungal biofilm infections. Annu Rev Med 2008, 59:415-428
43. Slater LN, Welch DF, Min KW: Rochalimaea henselae causes bacillary angiomatosis and peliosis hepatis. Arch Intern Med 1992, 152:602-606
44. Karem KL, Paddock CD, Regnery RL: Bartonella henselae. B quintana, and B bacilliformis: historical pathogens of emerging significance. Microbes Infect 2000, 2:1193-1205
45. Borczuk AC, Niedt G, Sablay LB, Kress Y, Mannion CM, Factor SM, Tanaka KE: Fibrous long-spacing collagen in bacillary angiomatosis. Ultrastruct Pathol 1998, 22:127-133
46. Cockerell CJ, Tierno PM, Friedman-Kien AE, Kim KS: Clinical, histologic, microbiologic, and biochemical characterization of the causative agent of bacillary (epithelioid) angiomatosis: a rickettsial illness with features of bartonellosis. J Invest Dermatol 1991, 97:812-817
47. Arias-Stella J, Lieberman PH, Erlandson RA, Arias-Stella JJ: Histology, immunohistochemistry, and ultrastructure of the verruga in Carrion's Disease. Am J Surg Pathol 1986, 10:595-610
48. Dabo SM, Confer AW, Saliki JT, Anderson BE: Binding of Bartonella henselae to extracellular molecules: identification of potential adhesins. Microbial Pathogenesis 2006, 41:10-20
49. Kaiser PO, Riess T, Wagner CL, Linke D, Lupas AN, Schwarz H, Raddatz G, Schafer A, Kempf VA: The head of Bartonella adhesin A is crucial for host cell interaction of Bartonella henselae. Cell Microbiol 2008, 10:2223-2234
50. Zhang P, Chomel BB, Schau MK, Goo JS, Droz S, Kelminson KL, George SS, Lerche NW, Koehler JE: A family of variably expressed outer-membrane proteins (Vomp) mediates adhesion and autoaggregation in Bartonella quintana. Proc Natl Acad Sci U S A 2004, 101:13630-13635
51. LeBoit PE, Berger TG, Egbert BM, Beckstead JH, Yen TS, Stoler MH: Bacillary angiomatosis. The histopathology and differential diagnosis of a pseudoneoplastic infection in patients with human immunodeficiency virus disease. Am J Surg Pathol 1989, 13: 909-920
52. Bhutto AM, Nonaka S, Hashiguchi Y, Gomez EA: Histopathological and electron microscopical features of skin lesions in a patient with bartonellosis (verruga peruana). J Dermatol 1994, 21:178-184
53. Dehio C, Meyer M, Berger J, Schwarz H, Lanz C: Interaction of Bartonella henselae with endothelial cells results in bacterial aggregation on the cell surface and the subsequent engulfment and internalisation of the bacterial aggregate by a unique structure, the invasome. J Cell Sci 1997, 110:2141-2154
54. Kempf VA, Schaller M, Behrendt S, Volkmann B, Aepfelbacher M, Cakman I, Autenrieth IB: Interaction of Bartonella henselae with endothelial cells results in rapid bacterial rRNA synthesis and replication. Cell Microbiol 2000, 2:431-441
55. Mandle T, Einsele H, Schaller M, Neumann D, Vogel W, Autenrieth IB, Kempf VA: Infection of human CD34+ progenitor cells with Bartonella henselae results in intraerythrocytic presence of B. henselae. Blood 2005, 106:1215-1222
56. Salvatore P, Casamassimi A, Sommese L, Fiorito C, Ciccodicola A, Rossiello R, Avallone B, Grimaldi V, Costa V, Rienzo M, Colicchio R, Williams-Ignarro S, Pagliarulo C, Prudente ME, Abbondanza C, Lamberti F, Baroni A, Buommino E, Farzati B, Tufano MA, Ignarro LJ, Napoli C: Detrimental effects of Bartonella henselae are counteracted by L-arginine and nitric oxide in human endothelial progenitor cells, Proc Natl Acad Sci U S A 2008, 105:9427-9432
57. Seubert A, Schulein R, Dehio C: Bacterial persistence within erythrocytes: a unique pathogenic strategy of Bartonella spp. Int J Med Microbiol 2002, 291:555-560