Home LiteratureArticle Details
PMID: 18003793 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Detectable serum flagellin and lipopolysaccharide and upregulated anti-flagellin and lipopolysaccharide immunoglobulins in human short bowel syndrome.

Ziegler TR, Luo M, Estívariz CF, Moore DA, Sitaraman SV, Hao L, Bazargan N, Klapproth JM, Tian J, Galloway JR, Leader LM, Jones DP, Gewirtz AT

Abstract

Gut barrier dysfunction may occur in short bowel syndrome (SBS). We hypothesized that systemic exposure to flagellin and lipopolysaccharide (LPS) in SBS might regulate specific immune responses. We analyzed serial serum samples obtained from parenteral nutrition (PN)-dependent patients with SBS versus non-SBS control serum. Serum from 23 adult SBS patients was obtained at baseline and 4, 8, 12, 16, 20, and 24 wk in a trial of modified diet with or without growth hormone. Control serum was obtained from 48 healthy adults and 37 adults requiring PN during critical illness. Serum flagellin was detected by an ELISA recognizing an array of gram-negative flagellins, and LPS was detected by limulus assay. Serum flagellin- and LPS-specific immunoglobulin levels (IgM, IgA, and IgG) were determined by ELISA. Serum flagellin and LPS were undetectable in control subjects. In contrast, serum flagellin, LPS, or both were detected in 14 SBS patients (61%) during one or more time points [flagellin alone, 5/23 (22%); LPS alone, 6/23 (26%); or flagellin + LPS, 3/23 (13%)]. Flagellin-specific serum IgM, IgA, and IgG levels were markedly increased in SBS patients compared with both control populations and remained elevated during the 6-mo study period. LPS-specific IgA was significantly higher in SBS patients compared with healthy controls; LPS-specific IgM, IgA, and IgG levels each decreased over time in association with PN weaning. We conclude that adults with PN-dependent SBS are systemically exposed to flagellin and LPS, presumably from the gut lumen. This likely regulates innate and adaptive immune responses to these specific bacterial products.

MeSH Terms
Adult Aged Antibodies, Bacterial/blood Antibody Specificity Female Flagellin/blood,immunology Humans Immunoglobulin A/blood Immunoglobulin G/blood Immunoglobulin M/blood Lipopolysaccharides/blood,immunology Male Middle Aged Short Bowel Syndrome/immunology Up-Regulation
Chemicals
Antibodies, Bacterial Immunoglobulin A Immunoglobulin G Immunoglobulin M Lipopolysaccharides Flagellin
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Ziegler Thomas R
General Clinical Research Center, Emory University Hospital, 1364 Clifton Road, Atlanta, GA 30322, USA. tzieg01@emory.edu
Luo Menghua
Estívariz Concepción F
Moore Daniel A
Sitaraman Shanthi V
Hao Li
Bazargan Niloofar
Klapproth Jan-Michael
Tian Junqiang
Galloway John R
Leader Lorraine M
Jones Dean P
Gewirtz Andrew T
References (37)
37 references, click to expand
  1. Home parenteral nutrition in Denmark in the period from 1996 to 2001.
    Scand J Gastroenterol. 2006 Apr;41(4):401-7 PMID: 16635907
  2. New developments in the diagnosis of bloodstream infections.
    Lancet Infect Dis. 2004 Dec;4(12):751-60 PMID: 15567125
  3. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms.
    J Immunol. 2003 Dec 1;171(11):6164-72 PMID: 14634132
  4. Flag in the crossroads: flagellin modulates innate and adaptive immunity.
    Curr Opin Gastroenterol. 2006 Jan;22(1):8-12 PMID: 16319670
  5. Parenteral glutamine increases serum heat shock protein 70 in critically ill patients.
    Intensive Care Med. 2005 Aug;31(8):1079-86 PMID: 15973519
  6. Comparison of inflammation, organ damage, and oxidant stress induced by Salmonella enterica serovar Muenchen flagellin and serovar Enteritidis lipopolysaccharide.
    Infect Immun. 2002 Jan;70(1):192-8 PMID: 11748182
  7. Remaining small bowel length: association with catheter sepsis in patients receiving home total parenteral nutrition: evidence of bacterial translocation.
    World J Surg. 2000 Dec;24(12):1537-41 PMID: 11193720
  8. Microbiology of bacterial translocation in humans.
    Gut. 1998 Jan;42(1):29-35 PMID: 9505882
  9. Intestinal absorption and permeability in paediatric short-bowel syndrome: a pilot study.
    J Pediatr Gastroenterol Nutr. 1999 Nov;29(5):588-93 PMID: 10554128
  10. Inflammatory mediators and immune function are altered in home parenteral nutrition patients.
    Nutrition. 2006 Feb;22(2):97-103 PMID: 16459221
  11. A single dose of endotoxin increases intestinal permeability in healthy humans.
    Arch Surg. 1988 Dec;123(12):1459-64 PMID: 3142442
  12. Increased intestinal permeability associated with infection in burn patients.
    Arch Surg. 1988 Nov;123(11):1313-9 PMID: 3140766
  13. Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease.
    Am J Physiol Gastrointest Liver Physiol. 2006 Jun;290(6):G1157-63 PMID: 16439468
  14. Enhancing bowel adaptation in short bowel syndrome.
    Curr Gastroenterol Rep. 2002 Aug;4(4):338-47 PMID: 12149180
  15. Inflammatory mediators in patients receiving long-term home parenteral nutrition.
    Dig Dis Sci. 2001 Nov;46(11):2484-9 PMID: 11713958
  16. Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn's disease.
    Gastroenterology. 2005 Jun;128(7):2020-8 PMID: 15940634
  17. Growth hormone favorably affects bone turnover and bone mineral density in patients with short bowel syndrome undergoing intestinal rehabilitation.
    JPEN J Parenter Enteral Nutr. 2006 Nov-Dec;30(6):480-6 PMID: 17047171
  18. Catheter-related infections associated with home parenteral nutrition and predictive factors for the need for catheter removal in their treatment.
    JPEN J Parenter Enteral Nutr. 1994 Jul-Aug;18(4):297-302 PMID: 7933434
  19. Humoral immune response to flagellin requires T cells and activation of innate immunity.
    J Immunol. 2006 Sep 1;177(5):2810-8 PMID: 16920916
  20. Alterations in intestinal barrier function do not predispose to translocation of enteric bacteria in gastroenterologic patients.
    Nutrition. 1998 Apr;14(4):358-62 PMID: 9591307
  21. Microbial translocation in neonates and infants receiving long-term parenteral nutrition.
    Arch Surg. 1996 Feb;131(2):176-9 PMID: 8611075
  22. Elevated flagellin-specific immunoglobulins in Crohn's disease.
    Am J Physiol Gastrointest Liver Physiol. 2005 Feb;288(2):G403-6 PMID: 15388489
  23. Bacterial flagellin is a dominant antigen in Crohn disease.
    J Clin Invest. 2004 May;113(9):1296-306 PMID: 15124021
  24. Gut origin of sepsis: a prospective study investigating associations between bacterial translocation, gastric microflora, and septic morbidity.
    Gut. 1999 Aug;45(2):223-8 PMID: 10403734
  25. Surgical manipulation of the large intestine increases bacterial translocation in patients undergoing elective colorectal surgery.
    Colorectal Dis. 2006 Sep;8(7):596-600 PMID: 16919113
  26. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression.
    J Immunol. 2001 Aug 15;167(4):1882-5 PMID: 11489966
  27. Surgical stress shifts the intestinal Escherichia coli population to that of a more adherent phenotype: role in barrier regulation.
    Surgery. 2001 Jul;130(1):65-73 PMID: 11436014
  28. Trophic and cytoprotective nutrition for intestinal adaptation, mucosal repair, and barrier function.
    Annu Rev Nutr. 2003;23:229-61 PMID: 12626687
  29. Influence of bacterial overgrowth and intestinal inflammation on duration of parenteral nutrition in children with short bowel syndrome.
    J Pediatr. 1997 Sep;131(3):356-61 PMID: 9329409
  30. Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: I kappa B alpha degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction.
    J Immunol. 2001 Jan 15;166(2):1248-60 PMID: 11145708
  31. The process of microbial translocation.
    Ann Surg. 1990 Oct;212(4):496-510; discussion 511-2 PMID: 2222015
  32. Incidence of catheter-associated gram-negative bacteremia in children with short bowel syndrome.
    J Clin Microbiol. 1989 Jun;27(6):1317-9 PMID: 2666441
  33. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response.
    J Clin Invest. 2001 Jan;107(1):99-109 PMID: 11134185
  34. Recurrent sepsis in home parenteral nutrition patients: an analysis of risk factors.
    JPEN J Parenter Enteral Nutr. 1994 May-Jun;18(3):256-63 PMID: 8065002
  35. Treatment strategies for small bowel bacterial overgrowth in short bowel syndrome.
    J Pediatr Gastroenterol Nutr. 1998 Aug;27(2):155-60 PMID: 9702645
  36. Lipopolysaccharide endotoxemia reduces cell proliferation and decreases enterocyte apopotosis during intestinal adaptation in a rat model of short-bowel syndrome.
    Pediatr Surg Int. 2002 Oct;18(7):615-9 PMID: 12471477
  37. Bacterial adaptation in patients with short bowel and colon in continuity.
    Gastroenterology. 1995 Nov;109(5):1446-53 PMID: 7557124
Article Info
Journal
American journal of physiology. Regulatory, integrative and comparative physiology
Abbr.
Am J Physiol Regul Integr Comp Physiol
ISSN
0363-6119
Published
2008-02-00
Epub
2007-00-14
Pages
R402-10
Language
English
Region
United States
NLM ID
100901230
PMCID
PMC3064750
Subset
IM
Grants
NIDDK NIH HHS · R01 DK 061417 · United States
NIDDK NIH HHS · K24 DK096574 · United States
NIDDK NIH HHS · R01 DK061417 · United States
NCRR NIH HHS · K24 RR023356-03 · United States
NCRR NIH HHS · M01 RR000039 · United States
NCRR NIH HHS · M01 RR 00039 · United States
NIDDK NIH HHS · R01 DK055850 · United States
NIDDK NIH HHS · R24 DK 064399 · United States
NCRR NIH HHS · K24 RR023356 · United States
NCRR NIH HHS · UL1 RR025008 · United States
NIDDK NIH HHS · R01 DK 55850 · United States
NIDDK NIH HHS · R01 DK055850-05 · United States
NIDDK NIH HHS · R03 DK067123-02 · United States
NIDDK NIH HHS · K08 DK002802 · United States
NCATS NIH HHS · UL1 TR000454 · United States
NIDDK NIH HHS · R24 DK064399 · United States
NIDDK NIH HHS · R03 DK067123 · United States
NCRR NIH HHS · UL1 RR025008-01 · United States
NIDDK NIH HHS · R01 DK 002802 · 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