Serologic evidence of gut-driven systemic inflammation in juvenile idiopathic arthritis

Journal of Rheumatology

Volumn 44, Issue 11, 2017, Pages 1624-1631

  Fotis, Lampros ^b   Shaikh, Nurmohammad ^c   Baszis, Kevin W ^a   Samson, Charles M ^c   Lev Tzion, Raffi ^c   French, Anthony R ^a   Tarr, Phillip I ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NOTTINGHAM UNIVERSITY HOSPITALS NHS TRUST   (United Kingdom)

^c SHAARE ZEDEK MEDICAL CENTER   (Israel)

Author keywords

Acute phase proteins 1 acid glycoprotein; Intestinal permeability; Juvenile idiopathic arthritis; Lipopolysaccharide lipopolysaccharide binding protein

Indexed keywords

C REACTIVE PROTEIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; OROSOMUCOID; IMMUNOGLOBULIN G;

ADOLESCENT; ARTICLE; BACTERIAL STRAIN; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; HUMAN; IMMUNE RESPONSE; INFLAMMATORY BOWEL DISEASE; INTESTINE FLORA; JUVENILE RHEUMATOID ARTHRITIS; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PEDIATRICS; PRIORITY JOURNAL; SEROLOGY; BLOOD; IMMUNOLOGY; INFLAMMATION; PRESCHOOL CHILD;

ADOLESCENT; ARTHRITIS, JUVENILE; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; IMMUNOGLOBULIN G; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE;

EID: 85032628883     PISSN: 0315162X     EISSN: 14992752     Source Type: Journal    
DOI: 10.3899/jrheum.161589     Document Type: Article

References (49)

1. Arvonen M, Berntson L, Pokka T, Karttunen TJ, Vähäsalo P, Stoll ML. Gut microbiota-host interactions and juvenile idiopathic arthritis. Pediatr Rheumatol Online J 2016;14:44.
2. Lerner A, Matthias T. Rheumatoid arthritis-celiac disease relationship: joints get that gut feeling. Autoimmun Rev 2015;14:1038-47.
3. Kokkonen J, Arvonen M, Vähäsalo P, Karttunen TJ. Intestinal immune activation in juvenile idiopathic arthritis and connective tissue disease. Scand J Rheumatol 2007;36:386-9.
4. Arvonen M, Ikni L, Augustin M, Karttunen TJ, Vähäsalo P. Increase of duodenal and ileal mucosal cytotoxic lymphocytes in juvenile idiopathic arthritis. Clin Exp Rheumatol 2010;28:128-34.
5. Weber P, Brune T, Ganser G, Zimmer KP. Gastrointestinal symptoms and permeability in patients with juvenile idiopathic arthritis. Clin Exp Rheumatol 2003;21:657-62.
6. Picco P, Gattorno M, Marchese N, Vignola S, Sormani MP, Barabino A, et al. Increased gut permeability in juvenile chronic arthritides. A multivariate analysis of the diagnostic parameters. Clin Exp Rheumatol 2000;18:773-8.
7. Pichler J, Ong C, Shah N, Sebire N, Kiparrissi F, Borrelli O, et al. Histopathological features of gastrointestinal mucosal biopsies in children with juvenile idiopathic arthritis. Pediatr Res 2016; 79:895-901.
8. Berntson L, Hedlund-Treutiger I, Alving K. Anti-inflammatory effect of exclusive enteral nutrition in patients with juvenile idiopathic arthritis. Clin Exp Rheumatol 2016;34:941-5.
9. Tejesvi MV, Arvonen M, Kangas SM, Keskitalo PL, Pirttilä AM, Karttunen TJ, et al. Faecal microbiome in new-onset juvenile idiopathic arthritis. Eur J Clin Microbiol Infect Dis 2016;35:363-70.
10. Aggarwal A, Sarangi AN, Gaur P, Shukla A, Aggarwal R. Gut microbiome in children with enthesitis-related arthritis in a developing country and the effect of probiotic administration. Clin Exp Immunol 2017;187:480-9.
11. Stoll ML, Kumar R, Morrow CD, Lefkowitz EJ, Cui X, Genin A, et al. Altered microbiota associated with abnormal humoral immune responses to commensal organisms in enthesitis-related arthritis. Arthritis Res Ther 2014;16:486.
12. Trent MS, Stead CM, Tran AX, Hankins JV. Diversity of endotoxin and its impact on pathogenesis. J Endotoxin Res 2006;12:205-23.
13. de Punder K, Pruimboom L. Stress induces endotoxemia and low-grade inflammation by increasing barrier permeability. Front Immunol 2015;6:223.
14. Lorenz W, Buhrmann C, Mobasheri A, Lueders C, Shakibaei M. Bacterial lipopolysaccharides form procollagen-endotoxin complexes that trigger cartilage inflammation and degeneration: implications for the development of rheumatoid arthritis. Arthritis Res Ther 2013;15:R111.
15. Gutsmann T, Müller M, Carroll SF, MacKenzie RC, Wiese A, Seydel U. Dual role of lipopolysaccharide (LPS)-binding protein in neutralization of LPS and enhancement of LPS-induced activation of mononuclear cells. Infect Immun 2001;69:6942-50.
16. Berner R, Fürll B, Stelter F, Dröse J, Müller H-P, Schütt C. Elevated levels of lipopolysaccharide-binding protein and soluble CD14 in plasma in neonatal early-onset sepsis. Clin Diagn Lab Immunol 2002;9:440-5.
17. Heumann D, Bas S, Gallay P, Le Roy D, Barras C, Mensi N, et al. Lipopolysaccharide binding protein as a marker of inflammation in synovial fluid of patients with arthritis: correlation with interleukin 6 and C-reactive protein. J Rheumatol 1995;22:1224-9.
18. Hochepied T, Berger FG, Baumann H, Libert C. α1-Acid glycoprotein: an acute phase protein with inflammatory and immunomodulating properties. Cytokine Growth Factor Rev 2003;14:25-34.
19. Moore DF, Rosenfeld MR, Gribbon PM, Winlove CP, Tsai CM. Alpha-1-acid (AAG, orosomucoid) glycoprotein: interaction with bacterial lipopolysaccharide and protection from sepsis. Inflammation 1997;21:69-82.
20. Cylwik B, Chrostek L, Gindzienska-Sieskiewicz E, Sierakowski S, Szmitkowski M. Relationship between serum acute-phase proteins and high disease activity in patients with rheumatoid arthritis. Adv Med Sci 2010;55:80-5.
21. Nielsen OH, Vainer B, Madsen SM, Seidelin JB, Heegaard NH. Established and emerging biological activity markers of inflammatory bowel disease. Am J Gastroenterol 2000;95:359-67.
22. Petty RE, Southwood TR, Baum J, Bhettay E, Glass DN, Manners P, et al. Revision of the proposed classification criteria for juvenile idiopathic arthritis: Durban, 1997. J Rheumatol 1998;25:1991-4.
23. Prakken B, Albani S, Martini A. Juvenile idiopathic arthritis. Lancet 2011;377:2138-49.
24. Chandler WL, Jelacic S, Boster DR, Ciol MA, Williams GD, Watkins SL, et al. Prothrombotic coagulation abnormalities preceding the hemolytic-uremic syndrome. N Engl J Med 2002;346:23-32.
25. Nordal EB, Zak M, Aalto K, Berntson L, Fasth A, Herlin T, et al. Validity and predictive ability of the juvenile arthritis disease activity score based on CRP versus ESR in a Nordic population-based setting. Ann Rheum Dis 2012;71:1122-7.
26. Bilge SS, Vary JC, Dowell SF, Tarr PI. Role of the Escherichia coli O157:H7 O side chain in adherence and analysis of an rfb locus. Infect Immun 1996;64:4795-801.
27. Inzana TJ. Electrophoretic heterogeneity and interstrain variation of the lipopolysaccharide of Haemophilus influenzae. J Infect Dis 1983;148:492-9.
28. Tsai CM, Frasch CE. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 1982;119:115-9.
29. Tyler JW, Cullor JS, Spier SJ, Smith BP. Immunity targeting common core antigens of gram-negative bacteria. J Vet Intern Med 1990;4:17-25.
30. Mielants H, Veys EM, Cuvelier C, De Vos M, Goemaere S, De Clercq L, et al. The evolution of spondyloarthropathies in relation to gut histology. II. Histological aspects. J Rheumatol 1995;22:2273-8.
31. Conti F, Borrelli O, Anania C, Marocchi E, Romeo EF, Paganelli M, et al. Chronic intestinal inflammation and seronegative spondyloarthropathy in children. Dig Liver Dis 2005;37:761-7.
32. Lee EK, Kang SM, Paik DJ, Kim JM, Youn J. Essential roles of Toll-like receptor-4 signaling in arthritis induced by type II collagen antibody and LPS. Int Immunol 2005;17:325-33.
33. Pierer M, Wagner U, Rossol M, Ibrahim S. Toll-like receptor 4 is involved in inflammatory and joint destructive pathways in collagen-induced arthritis in DBA1J mice. PLoS One 2011;6:e23539.
34. Pianta A, Arvikar S, Strle K, Drouin EE, Wang Q, Costello CE, et al. Evidence for immune relevance of Prevotella copri, a gut microbe, in patients with rheumatoid arthritis. Arthritis Rheumatol 2017;69:964-75.
35. Aoki S, Yoshikawa K, Yokoyama T, Nonogaki T, Iwasaki S, Mitsui T, et al. Role of enteric bacteria in the pathogenesis of rheumatoid arthritis: evidence for antibodies to enterobacterial common antigens in rheumatoid sera and synovial fluids. Ann Rheum Dis 1996;55:363-9.
36. Granfors K, Merilahti-Palo R, Luukkainen R, Möttönen T, Lahesmaa R, Probst P, et al. Persistence of Yersinia antigens in peripheral blood cells from patients with Yersinia enterocolitica O:3 infection with or without reactive arthritis. Arthritis Rheum 1998;41:855-62.
37. Olewicz-Gawlik A, Korczowska-Łacka I, Łacki JK, Klama K, Hrycaj P. Fucosylation of serum alpha1-acid glycoprotein in rheumatoid arthritis patients treated with infliximab. Clin Rheumatol 2007;26:1679-84.
38. Haston JL, FitzGerald O, Kane D, Smith KD. The influence of alpha1-acid glycoprotein on collagenase-3 activity in early rheumatoid arthritis. Biomed Chromatogr 2003;17:361-4.
39. De Graaf TW, Van Ommen EC, Van der Stelt ME, Kerstens PJ, Boerbooms AM, Van Dijk W. Effects of low dose methotrexate therapy on the concentration and the glycosylation of alpha 1-acid glycoprotein in the serum of patients with rheumatoid arthritis: a longitudinal study. J Rheumatol 1994;21:2209-16.
40. Hietbrink F, Besselink MG, Renooij W, de Smet MB, Draisma A, van der Hoeven H, et al. Systemic inflammation increases intestinal permeability during experimental human endotoxemia. Shock 2009;32:374-8.
41. Dossus L, Becker S, Achaintre D, Kaaks R, Rinaldi S. Validity of multiplex-based assays for cytokine measurements in serum and plasma from "non-diseased" subjects: Comparison with ELISA. J Immunol Methods 2009;350:125-32.
42. Siev M, Yu X, Prados-Rosales R, Martiniuk FT, Casadevall A, Achkar JM. Correlation between serum and plasma antibody titers to mycobacterial antigens. Clin Vaccine Immunol 2011;18:173-5.
43. Cherpes TL, Meyn LA, Hillier SL. Plasma versus serum for detection of herpes simplex virus type 2-specific immunoglobulin G antibodies with a glycoprotein G2-based enzyme immunoassay. J Clin Microbiol 2003;41:2758-9.
44. Gonzalez-Quintela A, Alonso M, Campos J, Vizcaino L, Loidi L, Gude F. Determinants of serum concentrations of lipopolysaccharide-binding protein (LBP) in the adult population: the role of obesity. PLoS One 2013;8:e54600.
45. Pasternak BA, D'Mello S, Jurickova II, Han X, Willson T, Flick L, et al. Lipopolysaccharide exposure is linked to activation of the acute phase response and growth failure in pediatric Crohn's disease and murine colitis. Inflamm Bowel Dis 2010;16:856-69.
46. Van Erp SJ, Verheul MK, Levarht EW, van der Reijden JJ, van der Heijde D, van Gaalen FA, et al. Short article: Absence of serological rheumatoid arthritis biomarkers in inflammatory bowel disease patients with arthropathies. Eur J Gastroenterol Hepatol 2017;29:345-8.
47. Guo S, Nighot M, Al-Sadi R, Alhmoud T, Nighot P, Ma TY. Lipopolysaccharide regulation of intestinal tight junction permeability is mediated by TLR4 signal transduction pathway activation of FAK and MyD88. J Immunol 2015;195:4999-5010.
48. Lakatos PL, Kiss LS, Palatka K, Altorjay I, Antal-Szalmas P, Palyu E, et al. Serum lipopolysaccharide-binding protein and soluble CD14 are markers of disease activity in patients with Crohn's disease. Inflamm Bowel Dis 2011;17:767-77.
49. Pastor Rojo O, López San Román A, Albéniz Arbizu E, de la Hera Martínez A, Ripoll Sevillano E, Albillos Martínez A. Serum lipopolysaccharide-binding protein in endotoxemic patients with inflammatory bowel disease. Inflamm Bowel Dis 2007;13:269-77.