Home LiteratureArticle Details
PMID: 11402005 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Salmonella-induced cell death is not required for enteritis in calves.

Infection and immunity ·Vol. 69 ·No. 7 ·2001-07-00 ·Pages 4610-7

Santos RL, Tsolis RM, Zhang S, Ficht TA, Bäumler AJ, Adams LG

Abstract

Salmonella enterica serovar Typhimurium causes cell death in bovine monocyte-derived and murine macrophages in vitro by a sipB-dependent mechanism. During this process, SipB binds and activates caspase-1, which in turn activates the proinflammatory cytokine interleukin-1beta through cleavage. We used bovine ileal ligated loops to address the role of serovar Typhimurium-induced cell death in induction of fluid accumulation and inflammation in this diarrhea model. Twelve perinatal calves had 6- to 9-cm loops prepared in the terminal ileum. They were divided into three groups: one group received an intralumen injection of Luria-Bertani broth as a control in 12 loops. The other two groups (four calves each) were inoculated with 0.75 x 10(9) CFU of either wild-type serovar Typhimurium (strain IR715) or a sopB mutant per loop in 12 loops. Hematoxylin and eosin-stained sections were scored for inflammation, and terminal deoxynucleotidyltransferase-mediated dUTP-biotin nick end labeling (TUNEL)-positive cells were detected in situ. Fluid accumulation began at 3 h postinfection (PI). Inflammation was detected in all infected loops at 1 h PI. The area of TUNEL-labeled cells in the wild-type infected loops was significantly higher than that of the controls at 12 h PI, when a severe inflammatory response and tissue damage had already developed. The sopB mutant induced the same amount of TUNEL-positive cells as the wild type, but it was attenuated for induction of fluid secretion and inflammation. Our results indicate that serovar Typhimurium-induced cell death is not required to trigger an early inflammatory response and fluid accumulation in the ileum.

MeSH Terms
Animals Apoptosis/immunology Bacterial Proteins/genetics,immunology Cattle Diarrhea/immunology Disease Models, Animal Enteritis/immunology Male Mutagenesis Salmonella Infections/immunology Salmonella typhimurium/immunology
Chemicals
Bacterial Proteins SopB protein, Bacteria SopB protein, Salmonella
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Santos R L
Department of Veterinary Pathobiology, College of Veterinary Medicine, Texas A&M University, College Station, Texas 77843, USA.
Tsolis R M
Zhang S
Ficht T A
Bäumler A J
Adams L G
References (34)
34 references, click to expand
  1. Salmonella spp. are cytotoxic for cultured macrophages.
    Mol Microbiol. 1996 Sep;21(5):1101-15 PMID: 8885278
  2. Intracellular survival of Brucella abortus, Mycobacterium bovis BCG, Salmonella dublin, and Salmonella typhimurium in macrophages from cattle genetically resistant to Brucella abortus.
    Vet Immunol Immunopathol. 1996 Mar;50(1-2):55-65 PMID: 9157686
  3. In vivo apoptosis in Shigella flexneri infections.
    Infect Immun. 1996 Dec;64(12):5357-65 PMID: 8945588
  4. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo.
    J Exp Med. 1997 Aug 18;186(4):569-80 PMID: 9254655
  5. The early dynamic response of the calf ileal epithelium to Salmonella typhimurium.
    Vet Pathol. 1997 Sep;34(5):369-86 PMID: 9381648
  6. A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa.
    Mol Microbiol. 1997 Sep;25(5):903-12 PMID: 9364916
  7. Identification of a novel Salmonella invasion locus homologous to Shigella ipgDE.
    J Bacteriol. 1998 Apr;180(7):1793-802 PMID: 9537377
  8. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells.
    J Immunol. 1997 Dec 1;159(11):5550-9 PMID: 9548496
  9. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB.
    J Biol Chem. 1998 Dec 4;273(49):32895-900 PMID: 9830039
  10. Salmonella SirA is a global regulator of genes mediating enteropathogenesis.
    Mol Microbiol. 1999 Feb;31(3):971-82 PMID: 10048039
  11. Interaction of Salmonella with host cells through the centisome 63 type III secretion system.
    Curr Opin Microbiol. 1999 Feb;2(1):46-50 PMID: 10047557
  12. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1.
    Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2396-401 PMID: 10051653
  13. Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes.
    J Bacteriol. 1999 Jun;181(11):3433-7 PMID: 10348855
  14. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves.
    Infect Immun. 1999 Sep;67(9):4879-85 PMID: 10456944
  15. SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase.
    Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14057-9 PMID: 9826652
  16. Of mice, calves, and men. Comparison of the mouse typhoid model with other Salmonella infections.
    Adv Exp Med Biol. 1999;473:261-74 PMID: 10659367
  17. Salmonella-induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells.
    J Exp Med. 2000 Feb 21;191(4):613-24 PMID: 10684853
  18. Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis.
    Infect Immun. 2000 Jun;68(6):3744-7 PMID: 10816540
  19. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model.
    J Exp Med. 2000 Jul 17;192(2):249-58 PMID: 10899911
  20. Striking a balance: modulation of the actin cytoskeleton by Salmonella.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):8754-61 PMID: 10922031
  21. Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype typhimurium.
    Infect Immun. 2000 Oct;68(10):5702-9 PMID: 10992474
  22. Salmonella induces macrophage death by caspase-1-dependent necrosis.
    Mol Microbiol. 2000 Oct;38(1):31-40 PMID: 11029688
  23. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD.
    J Biol Chem. 2000 Dec 1;275(48):37718-24 PMID: 10978351
  24. Salmonella enterica serovar typhimurium induces cell death in bovine monocyte-derived macrophages by early sipB-dependent and delayed sipB-independent mechanisms.
    Infect Immun. 2001 Apr;69(4):2293-301 PMID: 11254586
  25. The rectal biopsy appearances in Salmonella colitis.
    Histopathology. 1978 Mar;2(2):117-31 PMID: 669591
  26. Pathology of salmonella colitis.
    Am J Surg Pathol. 1979 Dec;3(6):483-90 PMID: 534385
  27. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells.
    Science. 1989 Feb 24;243(4894 Pt 1):1059-62 PMID: 2646710
  28. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation.
    J Cell Biol. 1992 Nov;119(3):493-501 PMID: 1400587
  29. Ethanolamine utilization in Salmonella typhimurium: nucleotide sequence, protein expression, and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster.
    J Bacteriol. 1995 Mar;177(5):1357-66 PMID: 7868611
  30. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells.
    J Bacteriol. 1995 Jul;177(14):3965-71 PMID: 7608068
  31. Macrophage killing is an essential virulence mechanism of Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4197-201 PMID: 8633040
  32. Salmonella typhimurium secreted invasion determinants are homologous to Shigella Ipa proteins.
    Mol Microbiol. 1995 Nov;18(3):479-90 PMID: 8748032
  33. Salmonella typhimurium invasion induces apoptosis in infected macrophages.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9833-8 PMID: 8790417
  34. Apoptosis of monocytes and prolonged survival of granulocytes as a result of phagocytosis of bacteria.
    Infect Immun. 1996 Oct;64(10):4242-8 PMID: 8926095
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2001-07-00
Pages
4610-7
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC98538
Subset
IM
Grants
PHS HHS · 1 RO1 A144170 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com