ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Venugopal PG, Nutman TB, Semnani RT, 2009. Activation and regulation of toll-like receptors (TLRs) by helminth parasites. Immunol Res 43: 252–263.
-
2.
Layland LE, Rad R, Wagner H, da Costa CU, 2007. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur J Immunol 37: 2174–2184.
-
3.
Aksoy E, Zouain CS, Vanhoutte F, Fontaine J, Pavelka N, Thieblemont N, Willems F, Ricciardi-Castagnoli P, Goldman M, Capron M, Ryffel B, Trottein F, 2005. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280: 277–283.
-
4.
Thomas PG, Carter MR, Da'dara AA, DeSimone TM, Harn DA, 2005. A helminth glycan induces APC maturation via alternative NF-kappa B activation independent of I kappa B alpha degradation. J Immunol 175: 2082–2090.
-
5.
Marshall FA, Pearce EJ, 2008. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J Immunol 181: 7562–7570.
-
6.
van Liempt E, van Vliet SJ, Engering A, Garcia Vallejo JJ, Bank CM, Sanchez-Hernandez M, van Kooyk Y, van Die I, 2007. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol Immunol 44: 2605–2615.
-
7.
Jenkins SJ, Hewitson JP, Ferret-Bernard S, Mountford AP, 2005. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol 17: 1409–1418.
-
8.
Kane CM, Cervi L, Sun J, McKee AS, Masek KS, Shapira S, Hunter CA, Pearce EJ, 2004. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 173: 7454–7461.
-
9.
Brannstrom K, Sellin ME, Holmfeldt P, Brattsand M, Gullberg M, 2009. The Schistosoma mansoni protein Sm16/SmSLP/SmSPO-1 assembles into a nine-subunit oligomer with potential to inhibit Toll-like receptor signaling. Infect Immun 77: 1144–1154.
-
10.
van Riet E, Everts B, Retra K, Phylipsen M, van Hellemond JJ, Tielens AG, van der Kleij D, Hartgers FC, Yazdanbakhsh M, 2009. Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol 10: 9.
-
11.
Everts B, Adegnika AA, Kruize YC, Smits HH, Kremsner PG, Yazdanbakhsh M, 2010. Functional impairment of human myeloid dendritic cells during Schistosoma haematobium infection. PLoS Negl Trop Dis 4: e667.
-
12.
Aoki K, 1978. A study of endotoxemia in ulcerative colitis and Crohn's disease. II. Experimental study. Acta Med Okayama 32: 207–216.
-
13.
Pastor Rojo O, Lopez San Roman A, Albeniz Arbizu E, de la Hera Martinez A, Ripoll Sevillano E, Albillos Martinez A, 2007. Serum lipopolysaccharide-binding protein in endotoxemic patients with inflammatory bowel disease. Inflamm Bowel Dis 13: 269–277.
-
14.
Douek D, 2007. HIV disease progression: immune activation, microbes, and a leaky gut. Top HIV Med 15: 114–117.
-
15.
Sandek A, Rauchhaus M, Anker SD, von Haehling S, 2008. The emerging role of the gut in chronic heart failure. Curr Opin Clin Nutr Metab Care 11: 632–639.
-
16.
Karanja DM, Hightower AW, Colley DG, Mwinzi PN, Galil K, Andove J, Secor WE, 2002. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 360: 592–596.
-
17.
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R, 2009. Bacterial community variation in human body habitats across space and time. Science 326: 1694–1697.
-
18.
Kim JH, Kim SJ, Lee IS, Lee MS, Uematsu S, Akira S, Oh KI, 2009. Bacterial endotoxin induces the release of high mobility group box 1 via the IFN-beta signaling pathway. J Immunol 182: 2458–2466.
-
19.
Noronha AM, Liang Y, Hetzel JT, Hasturk H, Kantarci A, Stucchi A, Zhang Y, Nikolajczyk BS, Farraye FA, Ganley-Leal LM, 2009. Hyperactivated B cells in human inflammatory bowel disease. J Leukoc Biol 86: 1007–1016.
-
20.
Jagannathan M, Hasturk H, Liang Y, Shin H, Hetzel JT, Kantarci A, Rubin D, McDonnell ME, Van Dyke TE, Ganley-Leal LM, Nikolajczyk BS, 2009. TLR cross-talk specifically regulates cytokine production by B cells from chronic inflammatory disease patients. J Immunol 183: 7461–7470.
-
21.
Shin H, Zhang Y, Jagannathan M, Hasturk H, Kantarci A, Liu H, Van Dyke TE, Ganley-Leal LM, Nikolajczyk BS, 2009. B cells from periodontal disease patients express surface Toll-like receptor 4. J Leukoc Biol 85: 648–655.
-
22.
McDonnell M, Liang Y, Noronha A, Coukos J, Kasper DL, Farraye FA, Ganley-Leal LM, 2011. Systemic toll-like receptor ligands modify B-cell responses in human inflammatory bowel disease. Inflamm Bowel Dis 17: 298–307.
-
23.
Coats SR, Reife RA, Bainbridge BW, Pham TT, Darveau RP, 2003. Porphyromonas gingivalis lipopolysaccharide antagonizes Escherichia coli lipopolysaccharide at toll-like receptor 4 in human endothelial cells. Infect Immun 71: 6799–6807.
-
24.
Mwinzi PN, Ganley-Leal L, Black CL, Secor WE, Karanja DM, Colley DG, 2009. Circulating CD23+ B cell subset correlates with the development of resistance to Schistosoma mansoni reinfection in occupationally exposed adults who have undergone multiple treatments. J Infect Dis 199: 272–279.
-
25.
Casey LC, Balk RA, Bone RC, 1993. Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Ann Intern Med 119: 771–778.
-
26.
Pedras-Vasconcelos JA, Brunet LR, Pearce EJ, 2001. Profound effect of the absence of IL-4 on T cell responses during infection with Schistosoma mansoni. J Leukoc Biol 70: 737–744.
-
27.
Pisetsky DS, Erlandsson-Harris H, Andersson U, 2008. High-mobility group box protein 1 (HMGB1): an alarmin mediating the pathogenesis of rheumatic disease. Arthritis Res Ther 10: 209.
-
28.
Devaraj S, Dasu MR, Park SH, Jialal I, 2009. Increased levels of ligands of Toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia 52: 1665–1668.
-
29.
Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ, 2007. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8: 487–496.
-
30.
Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, Nakasato M, Lu Y, Hangai S, Koshiba R, Savitsky D, Ronfani L, Akira S, Bianchi ME, Honda K, Tamura T, Kodama T, Taniguchi T, 2009. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462: 99–103.
-
31.
Kane CM, Jung E, Pearce EJ, 2008. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect Immun 76: 5754–5759.
-
32.
Gioannini TL, Teghanemt A, Zhang D, Prohinar P, Levis EN, Munford RS, Weiss JP, 2007. Endotoxin-binding proteins modulate the susceptibility of bacterial endotoxin to deacylation by acyloxyacyl hydrolase. J Biol Chem 282: 7877–7884.
-
33.
van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, Espevik T, de Jong EC, Kapsenberg ML, Golenbock DT, Tielens AG, Yazdanbakhsh M, 2002. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J Biol Chem 277: 48122–48129.
-
34.
Donnelly S, O'Neill SM, Stack CM, Robinson MW, Turnbull L, Whitchurch C, Dalton JP, 2010. Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3. J Biol Chem 285: 3383–3392.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 671 | 458 | 13 |
| Full Text Views | 563 | 29 | 10 |
| PDF Downloads | 109 | 16 | 0 |
Human Schistosomiasis Is Associated with Endotoxemia and Toll-Like Receptor 2- and 4-Bearing B Cells
Daniel Onguru
Daniel Onguru
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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YanMei Liang
YanMei Liang
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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Qyana Griffith
Qyana Griffith
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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Barbara Nikolajczyk
Barbara Nikolajczyk
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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Pauline Mwinzi
Pauline Mwinzi
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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Lisa Ganley-Leal
Lisa Ganley-Leal
Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisian, Kenya; Section of Infectious Diseases, Department of Medicine, Boston University School of Medicine, Boston, Massachusetts; Department of Microbiology, Boston University School of Medicine, Boston, Massachusetts
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Schistosomiasis is caused by parasitic trematodes. Individuals can accumulate hundreds of intravascular worms, which secrete a myriad of antigenic molecules into the bloodstream. Some of these molecules suppress immunity to microbial Toll-like receptor (TLR) ligands, such as lipopolysaccharides, which may increase host susceptibility to coinfecting pathogens. We show that schistosomiasis is associated with extremely high levels of endotoxemia as well as high mobility group 1, an endogenous inflammatory TLR ligand, in the absence of other coinfected pathogens. Circulating B cells express surface TLR2 and TLR4, reflecting systemic exposure to microbial ligands. Bacterial translocation may occur with schistosomal egg movement from the vascular to the gut and other routes, such as the skin during infection. Our report suggests that immunosuppressive schistosome antigens may have evolved to curb inflammatory responses to the high antigenic burden of translocated bacteria products and endogenous TLR ligands that arise during parasite exposure and inflammation.
Author Notes
Financial support: This study was supported with funding from National Institute of Allergy and Infectious Diseases Grant A1074843 (to L.G.-L.) and Wellcome Trust Grant 08360 (to P.M.).
Authors' addresses: Daniel Onguru and Pauline Mwiniz, Vector Biology and Control Research Centre, Kenya Medical Research Institute, Kisumu, Kenya, E-mails: danonguru@yahoo.com and pmwinzi@kisian.mimcom.net. YanMei Liang, Qyana Griffith, and Lisa Ganley-Leal, Division of Infectious Diseases, Boston University School of Medicine, Boston, MA, E-mails: yanmei.liang@bmc.org, qyana@bu.edu, and Lisa.GanleyLeal@bmc.org. Barbara Nikolajczyk, Department of Microbiology, Boston University School of Medicine, Boston, MA, E-mail: bnikol@bu.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Venugopal PG, Nutman TB, Semnani RT, 2009. Activation and regulation of toll-like receptors (TLRs) by helminth parasites. Immunol Res 43: 252–263.
-
2.
Layland LE, Rad R, Wagner H, da Costa CU, 2007. Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2. Eur J Immunol 37: 2174–2184.
-
3.
Aksoy E, Zouain CS, Vanhoutte F, Fontaine J, Pavelka N, Thieblemont N, Willems F, Ricciardi-Castagnoli P, Goldman M, Capron M, Ryffel B, Trottein F, 2005. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J Biol Chem 280: 277–283.
-
4.
Thomas PG, Carter MR, Da'dara AA, DeSimone TM, Harn DA, 2005. A helminth glycan induces APC maturation via alternative NF-kappa B activation independent of I kappa B alpha degradation. J Immunol 175: 2082–2090.
-
5.
Marshall FA, Pearce EJ, 2008. Uncoupling of induced protein processing from maturation in dendritic cells exposed to a highly antigenic preparation from a helminth parasite. J Immunol 181: 7562–7570.
-
6.
van Liempt E, van Vliet SJ, Engering A, Garcia Vallejo JJ, Bank CM, Sanchez-Hernandez M, van Kooyk Y, van Die I, 2007. Schistosoma mansoni soluble egg antigens are internalized by human dendritic cells through multiple C-type lectins and suppress TLR-induced dendritic cell activation. Mol Immunol 44: 2605–2615.
-
7.
Jenkins SJ, Hewitson JP, Ferret-Bernard S, Mountford AP, 2005. Schistosome larvae stimulate macrophage cytokine production through TLR4-dependent and -independent pathways. Int Immunol 17: 1409–1418.
-
8.
Kane CM, Cervi L, Sun J, McKee AS, Masek KS, Shapira S, Hunter CA, Pearce EJ, 2004. Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 173: 7454–7461.
-
9.
Brannstrom K, Sellin ME, Holmfeldt P, Brattsand M, Gullberg M, 2009. The Schistosoma mansoni protein Sm16/SmSLP/SmSPO-1 assembles into a nine-subunit oligomer with potential to inhibit Toll-like receptor signaling. Infect Immun 77: 1144–1154.
-
10.
van Riet E, Everts B, Retra K, Phylipsen M, van Hellemond JJ, Tielens AG, van der Kleij D, Hartgers FC, Yazdanbakhsh M, 2009. Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol 10: 9.
-
11.
Everts B, Adegnika AA, Kruize YC, Smits HH, Kremsner PG, Yazdanbakhsh M, 2010. Functional impairment of human myeloid dendritic cells during Schistosoma haematobium infection. PLoS Negl Trop Dis 4: e667.
-
12.
Aoki K, 1978. A study of endotoxemia in ulcerative colitis and Crohn's disease. II. Experimental study. Acta Med Okayama 32: 207–216.
-
13.
Pastor Rojo O, Lopez San Roman A, Albeniz Arbizu E, de la Hera Martinez A, Ripoll Sevillano E, Albillos Martinez A, 2007. Serum lipopolysaccharide-binding protein in endotoxemic patients with inflammatory bowel disease. Inflamm Bowel Dis 13: 269–277.
-
14.
Douek D, 2007. HIV disease progression: immune activation, microbes, and a leaky gut. Top HIV Med 15: 114–117.
-
15.
Sandek A, Rauchhaus M, Anker SD, von Haehling S, 2008. The emerging role of the gut in chronic heart failure. Curr Opin Clin Nutr Metab Care 11: 632–639.
-
16.
Karanja DM, Hightower AW, Colley DG, Mwinzi PN, Galil K, Andove J, Secor WE, 2002. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 360: 592–596.
-
17.
Costello EK, Lauber CL, Hamady M, Fierer N, Gordon JI, Knight R, 2009. Bacterial community variation in human body habitats across space and time. Science 326: 1694–1697.
-
18.
Kim JH, Kim SJ, Lee IS, Lee MS, Uematsu S, Akira S, Oh KI, 2009. Bacterial endotoxin induces the release of high mobility group box 1 via the IFN-beta signaling pathway. J Immunol 182: 2458–2466.
-
19.
Noronha AM, Liang Y, Hetzel JT, Hasturk H, Kantarci A, Stucchi A, Zhang Y, Nikolajczyk BS, Farraye FA, Ganley-Leal LM, 2009. Hyperactivated B cells in human inflammatory bowel disease. J Leukoc Biol 86: 1007–1016.
-
20.
Jagannathan M, Hasturk H, Liang Y, Shin H, Hetzel JT, Kantarci A, Rubin D, McDonnell ME, Van Dyke TE, Ganley-Leal LM, Nikolajczyk BS, 2009. TLR cross-talk specifically regulates cytokine production by B cells from chronic inflammatory disease patients. J Immunol 183: 7461–7470.
-
21.
Shin H, Zhang Y, Jagannathan M, Hasturk H, Kantarci A, Liu H, Van Dyke TE, Ganley-Leal LM, Nikolajczyk BS, 2009. B cells from periodontal disease patients express surface Toll-like receptor 4. J Leukoc Biol 85: 648–655.
-
22.
McDonnell M, Liang Y, Noronha A, Coukos J, Kasper DL, Farraye FA, Ganley-Leal LM, 2011. Systemic toll-like receptor ligands modify B-cell responses in human inflammatory bowel disease. Inflamm Bowel Dis 17: 298–307.
-
23.
Coats SR, Reife RA, Bainbridge BW, Pham TT, Darveau RP, 2003. Porphyromonas gingivalis lipopolysaccharide antagonizes Escherichia coli lipopolysaccharide at toll-like receptor 4 in human endothelial cells. Infect Immun 71: 6799–6807.
-
24.
Mwinzi PN, Ganley-Leal L, Black CL, Secor WE, Karanja DM, Colley DG, 2009. Circulating CD23+ B cell subset correlates with the development of resistance to Schistosoma mansoni reinfection in occupationally exposed adults who have undergone multiple treatments. J Infect Dis 199: 272–279.
-
25.
Casey LC, Balk RA, Bone RC, 1993. Plasma cytokine and endotoxin levels correlate with survival in patients with the sepsis syndrome. Ann Intern Med 119: 771–778.
-
26.
Pedras-Vasconcelos JA, Brunet LR, Pearce EJ, 2001. Profound effect of the absence of IL-4 on T cell responses during infection with Schistosoma mansoni. J Leukoc Biol 70: 737–744.
-
27.
Pisetsky DS, Erlandsson-Harris H, Andersson U, 2008. High-mobility group box protein 1 (HMGB1): an alarmin mediating the pathogenesis of rheumatic disease. Arthritis Res Ther 10: 209.
-
28.
Devaraj S, Dasu MR, Park SH, Jialal I, 2009. Increased levels of ligands of Toll-like receptors 2 and 4 in type 1 diabetes. Diabetologia 52: 1665–1668.
-
29.
Tian J, Avalos AM, Mao SY, Chen B, Senthil K, Wu H, Parroche P, Drabic S, Golenbock D, Sirois C, Hua J, An LL, Audoly L, La Rosa G, Bierhaus A, Naworth P, Marshak-Rothstein A, Crow MK, Fitzgerald KA, Latz E, Kiener PA, Coyle AJ, 2007. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8: 487–496.
-
30.
Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, Nakasato M, Lu Y, Hangai S, Koshiba R, Savitsky D, Ronfani L, Akira S, Bianchi ME, Honda K, Tamura T, Kodama T, Taniguchi T, 2009. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature 462: 99–103.
-
31.
Kane CM, Jung E, Pearce EJ, 2008. Schistosoma mansoni egg antigen-mediated modulation of Toll-like receptor (TLR)-induced activation occurs independently of TLR2, TLR4, and MyD88. Infect Immun 76: 5754–5759.
-
32.
Gioannini TL, Teghanemt A, Zhang D, Prohinar P, Levis EN, Munford RS, Weiss JP, 2007. Endotoxin-binding proteins modulate the susceptibility of bacterial endotoxin to deacylation by acyloxyacyl hydrolase. J Biol Chem 282: 7877–7884.
-
33.
van der Kleij D, Latz E, Brouwers JF, Kruize YC, Schmitz M, Kurt-Jones EA, Espevik T, de Jong EC, Kapsenberg ML, Golenbock DT, Tielens AG, Yazdanbakhsh M, 2002. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J Biol Chem 277: 48122–48129.
-
34.
Donnelly S, O'Neill SM, Stack CM, Robinson MW, Turnbull L, Whitchurch C, Dalton JP, 2010. Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3. J Biol Chem 285: 3383–3392.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 671 | 458 | 13 |
| Full Text Views | 563 | 29 | 10 |
| PDF Downloads | 109 | 16 | 0 |