Fasciola hepatica Fatty Acid Binding Protein Inhibits TLR4 Activation and Suppresses the Inflammatory Cytokines Induced by Lipopolysaccharide In Vitro and In Vivo
Open accessAbstract
TLR4, the innate immunity receptor for bacterial endotoxins, plays a pivotal role in the induction of inflammatory responses. There is a need to develop molecules that block either activation through TLR4 or the downstream signaling pathways to inhibit the storm of inflammation typically elicited by bacterial LPS, which is a major cause of the high mortality associated with bacterial sepsis. We report in this article that a single i.p. injection of 15 μg fatty acid binding protein from Fasciola hepatica (Fh12) 1 h before exposure to LPS suppressed significantly the expression of serum inflammatory cytokines in a model of septic shock using C57BL/6 mice. Because macrophages are a good source of IL-12p70 and TNF-α, and are critical in driving adaptive immunity, we investigated the effect of Fh12 on the function of mouse bone marrow–derived macrophages (bmMΦs). Although Fh12 alone did not induce cytokine expression, it significantly suppressed the expression of IL-12, TNF-α, IL-6, and IL-1β cytokines, as well as inducible NO synthase–2 in bmMΦs, and also impaired the phagocytic capacity of bmMΦs. Fh12 had a limited effect on the expression of inflammatory cytokines induced in response to other TLR ligands. One mechanism used by Fh12 to exert its anti-inflammatory effect is binding to the CD14 coreceptor. Moreover, it suppresses phosphorylation of ERK, p38, and JNK. The potent anti-inflammatory properties of Fh12 demonstrated in this study open doors to further studies directed at exploring the potential of this molecule as a new class of drug against septic shock or other inflammatory diseases.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Fh12 and Fh15 suppress responses of CD14-deficient cells.
“The Fh12 and Fh15 proteins also suppress responses of CD14-deficient cells”
From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Martin et al., 2015
The Results section on CD14-knockout macrophages (page unavailable) reports that Fh12 suppressed IL1β expression in response to HKLM, supporting one limited instance of the claim. It did not suppress the measured responses to LPS or IL12p35 in response to HKLM. The cited passages provide no finding for Fh15, so the claim overgeneralizes the Fh12 result and does not establish the Fh15 result. (LLM, conf=0.88)
Experimental — accuracy not yet measuredFh12 and Fh15 bind to the TLR4 cofactor CD14 and reduce its expression, mediating suppression of TLR4 responses.
“They bind to the TLR4 cofactor CD14 and reduce its expression, mediating suppression of TLR4 responses.”
From Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules (2018) · cites this paper as Martin et al., 2015
The Results sections on CD14 interaction and TLR4 pathway components report that Fh12 binds CD14 and reduces its expression. The Discussion proposes CD14 as a likely route for blocking LPS–TLR4 responses, rather than establishing it as the sole mechanism. The passages address Fh12, not Fh15, so they do not support extending the claim to both proteins. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Interleukin-10 and the Interleukin-10 Receptor
Moore, K. W., de Waal Malefyt, R., Coffman, R. L., & O'Garra, A. (2001) · Annual Review of Immunology · doi:10.1146/annurev.immunol.19.1.683 · Cited by 6,737 · see citing works
Protein structure prediction on the Web: a case study using the Phyre server
Kelley, L. A., & Sternberg, M. J. E. (2009) · Nature Protocols · doi:10.1038/nprot.2009.2 · Cited by 4,154 · see citing works
Interleukin-12 and the regulation of innate resistance and adaptive immunity
Trinchieri, G. (2003) · Nature reviews. Immunology · doi:10.1038/nri1001 · Cited by 3,933 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Cua, D. J., Sherlock, J., Chen, Y., Murphy, C. A., Joyce, B., Seymour, B., Lucian, L., To, W., Kwan, S., Churakova, T., et al. (2003) · Nature · doi:10.1038/nature01355 · Cited by 2,906 · see citing works
THE INTERLEUKIN-12/INTERLEUKIN-12-RECEPTOR SYSTEM: Role in Normal and Pathologic Immune Responses
Gately, M. K., Renzetti, L. M., Magram, J., STERN, A. S., Adorini, L., Gubler, U., & Presky, D. H. (1998) · Annual Review of Immunology · doi:10.1146/annurev.immunol.16.1.495 · Cited by 1,231 · see citing works
Horror Autoinflammaticus: The Molecular Pathophysiology of Autoinflammatory Disease
Masters, S. L., Simon, A., Aksentijevich, I. A., & Kastner, D. L. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141627 · Cited by 1,063 · see citing works
Interleukin 15: biology and relevance to human disease
Fehniger, T. A., & Caligiuri, M. A. (2001) · Blood · doi:10.1182/blood.v97.1.14 · Cited by 976 · see citing works
Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists
Kanzler, H., Barrat, F. J., Hessel, E. M., & Coffman, R. L. (2007) · Nature Medicine · doi:10.1038/nm1589 · Cited by 869 · see citing works
Helminth parasites – masters of regulation
Maizels, R. M., Balic, A., Gomez‐Escobar, N., Nair, M. G., Taylor, M. D., & Allen, J. E. (2004) · Immunological Reviews · doi:10.1111/j.0105-2896.2004.00191.x · Cited by 866 · see citing works
ClusPro: an automated docking and discrimination method for the prediction of protein complexes
Comeau, S. R., GATCHELL, D. W., Vajda, S., & Camacho, C. J. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg371 · Cited by 857 · see citing works
Diversity and dialogue in immunity to helminths
Allen, J. E., & Maizels, R. M. (2011) · Nature reviews. Immunology · doi:10.1038/nri2992 · Cited by 831 · see citing works
ClusPro: a fully automated algorithm for protein-protein docking
Comeau, S. R., GATCHELL, D. W., Vajda, S., & Camacho, C. J. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh354 · Cited by 826 · see citing works
Shi, Y., Liu, C. H., Roberts, A. I., Das, J., Xu, G., Ren, G., Zhang, Y., Zhang, L., Yuan, Z., Tan, H. S., et al. (2006) · Cell Research · doi:10.1038/sj.cr.7310017 · Cited by 550 · see citing works
Mouse interleukin‐12 (IL‐12) p40 homodimer: a potent IL‐12 antagonist
Gillessen, S., Carvajal, D. M., Ling, P., et al. (1995) · European Journal of Immunology · doi:10.1002/eji.1830250133 · Cited by 436 · see citing works
Epidemiology of fascioliasis in human endemic areas
Mas‐Coma, S. (2005) · Journal of Helminthology · doi:10.1079/joh2005296 · Cited by 385 · see citing works
MAP kinase activation in macrophages
Rao, K. M. K. (2001) · Journal of Leukocyte Biology · doi:10.1189/jlb.69.1.3 · Cited by 371 · see citing works
Immunomodulation by helminth parasites: Defining mechanisms and mediators
McSorley, H. J., Hewitson, J. P., & Maizels, R. M. (2013) · International Journal for Parasitology · doi:10.1016/j.ijpara.2012.11.011 · Cited by 319 · see citing works
The interleukin‐12 subunit p40 specifically inhibits effects of the interleukin‐12 heterodimer
Mattner, F., Fischer, S., Guckes, S., et al. (1993) · European Journal of Immunology · doi:10.1002/eji.1830230923 · Cited by 283 · see citing works
Robinson, M. W., Menon, R., Donnelly, S., et al. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900045-mcp200 · Cited by 272 · see citing works
Protection from lethal Gram-negative bacterial sepsis by targeting Toll-like receptor 4
Roger, T., Froidevaux, C., Roy, D. L., Reymond, M. K., Chanson, A.-L., Mauri, D., Burns, K., Riederer, B. M., Akira, S., & Calandra, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808146106 · Cited by 267 · see citing works
Donnelly, S., O’Neill, S. M., Sekiya, M., Mulcahy, G. M., & Dalton, J. P. (2004) · Infection and Immunity · doi:10.1128/iai.73.1.166-173.2005 · Cited by 265 · see citing works
TLR4 as the Mammalian Endotoxin Sensor
Beutler, B. (2002) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-59430-4_7 · Cited by 240 · see citing works
Goodridge, H. S., Marshall, F. A., Else, K. J., Houston, K. M., EGAN, C. A., Al‐Riyami, L., Liew, F.-Y., Harnett, W., & Harnett, M. M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.1.284 · Cited by 239 · see citing works
Helminth Antigens Modulate TLR-Initiated Dendritic Cell Activation
Kane, C. M., Cervi, L., Sun, J., McKee, A. S., Masek, K. S., Shapira, S. D., Hunter, C. A., & Pearce, E. J. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.12.7454 · Cited by 229 · see citing works
Donnelly, S., Stack, C. M., O’Neill, S. M., Sayed, A. A., Williams, D. L., & Dalton, J. P. (2008) · The FASEB Journal · doi:10.1096/fj.08-106278 · Cited by 227 · see citing works
Jarvius, M., Paulsson, J., Weibrecht, I., Leuchowius, K., Andersson, A., Wählby, C., Gullberg, M. T., Botling, J., Sjöblom, T., Markova, B., et al. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700166-mcp200 · Cited by 225 · see citing works
Fasciola hepaticaSuppresses a Protective Th1 Response againstBordetella pertussis
Brady, M. T., O’Neill, S. M., Dalton, J. P., & Mills, K. H. G. (1999) · Infection and Immunity · doi:10.1128/iai.67.10.5372-5378.1999 · Cited by 216 · see citing works
Butcher, B. A., Kim, L., Johnson, P. F., & Denkers, E. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.4.2193 · Cited by 215 · see citing works
Fasciola hepatica infection downregulates Th1 responses in mice
O’Neill, S. M., Brady, M. T., Callanan, J. J., Mulcahy, G. M., Joyce, P. D., Mills, K. H. G., & Dalton, J. P. (2000) · Parasite Immunology · doi:10.1046/j.1365-3024.2000.00290.x · Cited by 208 · see citing works
Role of CD14 in Cellular Recognition of Bacterial Lipopolysaccharides
Kitchens, R. L. (1999) · KARGER eBooks · doi:10.1159/000058750 · Cited by 197 · see citing works
Catalytic Properties of Lipopolysaccharide (LPS) Binding Protein
Yu, B., & Wright, S. D. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.8.4100 · Cited by 195 · see citing works
McManus, D. P., & Dalton, J. P. (2006) · Parasitology · doi:10.1017/s0031182006001806 · Cited by 187 · see citing works
Functions of the tegument of schistosomes: Clues from the proteome and lipidome
van Hellemond, J. J., Retra, K., Brouwers, J. F. H. M., et al. (2006) · International Journal for Parasitology · doi:10.1016/j.ijpara.2006.01.007 · Cited by 186 · see citing works
Proteomic analysis of Fasciola hepatica excretory-secretory products
Jefferies, J. R., Campbell, A. M., van Rossum, A. J., Barrett, J., & Brophy, P. M. (2001) · PROTEOMICS · doi:10.1002/1615-9861(200109)1:9 · Cited by 171 · see citing works
Beutler, B., Du, X., & Poltorak, A. N. (2001) · Journal of Endotoxin Research · doi:10.1177/09680519010070040901 · Cited by 167 · see citing works
Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists
Peri, F., & Piazza, M. (2011) · Biotechnology Advances · doi:10.1016/j.biotechadv.2011.05.014 · Cited by 162 · see citing works
Morphew, R. M., Wright, H. A., LaCourse, E. J., et al. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600375-mcp200 · Cited by 150 · see citing works
TLR2 & Co: a critical analysis of the complex interactions between TLR2 and coreceptors
van Bergenhenegouwen, J., Plantinga, T. S., Joosten, L. A. B., Netea, M. G., Folkerts, G., Kraneveld, A. D., Garssen, J., & Vos, A. P. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.0113003 · Cited by 143 · see citing works
Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3
Donnelly, S., O’Neill, S. M., Stack, C. M., Robinson, M. W., Turnbull, L., Whitchurch, C., & Dalton, J. P. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.060368 · Cited by 140 · see citing works
Flynn, R. J., Mannion, C., Golden, O., Haçarız, O., & Mulcahy, G. M. (2006) · Infection and Immunity · doi:10.1128/iai.01445-06 · Cited by 131 · see citing works
Dowling, D. J., Hamilton, C. M., Donnelly, S., LaCourse, E. J., Brophy, P. M., Dalton, J. P., & O’Neill, S. M. (2009) · Infection and Immunity · doi:10.1128/iai.00573-09 · Cited by 131 · see citing works
Everts, B., Smits, H. H., Hokke, C. H., & Yazdanbakhsh, M. (2010) · European Journal of Immunology · doi:10.1002/eji.200940109 · Cited by 119 · see citing works
Exploring the Fasciola hepatica tegument proteome
Wilson, R. A., Wright, J. M., Castro‐Borges, W., Parker-Manuel, S. J., Dowle, A., Ashton, P. D., Young, N. D., Gasser, R. B., & Spithill, T. W. (2011) · International Journal for Parasitology · doi:10.1016/j.ijpara.2011.08.003 · Cited by 119 · see citing works
Improving animal and human health through understanding liver fluke immunology
Piedrafita, D. M., Spithill, T. W., Smith, R. E., et al. (2010) · Parasite Immunology · doi:10.1111/j.1365-3024.2010.01223.x · Cited by 115 · see citing works
TheFasciola hepaticaTegumental Antigen Suppresses Dendritic Cell Maturation and Function
Hamilton, C. M., Dowling, D. J., Loscher, C. E., et al. (2009) · Infection and Immunity · doi:10.1128/iai.00919-08 · Cited by 114 · see citing works
Overexpression of interleukin-12 and T helper 1 predominance in lupus nephritis
Tucci, M., Lombardi, L., Richards, H., et al. (2008) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2008.03758.x · Cited by 113 · see citing works
Kelley, S. L., Lukk, T., Nair, S. K., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1202446 · Cited by 110 · see citing works
Robinson, M. W., & Connolly, B. (2005) · PROTEOMICS · doi:10.1002/pmic.200402057 · Cited by 107 · see citing works
O’Neill, S. M., Mills, K. H. G., & Dalton, J. P. (2001) · Parasite Immunology · doi:10.1046/j.1365-3024.2001.00411.x · Cited by 105 · see citing works
Soluble CD14-Mediated Cellular Responses to Lipopolysaccharide
Tapping, R. I., & Tobias, P. S. (1999) · KARGER eBooks · doi:10.1159/000058751 · Cited by 100 · see citing works
Chitohexaose Activates Macrophages by Alternate Pathway through TLR4 and Blocks Endotoxemia
Panda, S. K., Kumar, S., Tupperwar, N., Vaidya, T., George, A., Rath, S., Bal, V., & Ravindran, B. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002717 · Cited by 94 · see citing works
van Riet, E., Everts, B., Retra, K., Phylipsen, M., van Hellemond, J. J., Tielens, A. G. M., van der Kleij, D., Hartgers, F. C., & Yazdanbakhsh, M. (2009) · BMC Immunology · doi:10.1186/1471-2172-10-9 · Cited by 93 · see citing works
Inhibition of TLR3 and TLR4 function and expression in human dendritic cells by helminth parasites
Semnani, R. T., Venugopal, P. G., Leifer, C. A., Mostböck, S., Sabzevari, H., & Nutman, T. B. (2008) · Blood · doi:10.1182/blood-2008-04-149856 · Cited by 92 · see citing works
Increasing the efficiency of SAGE adaptor ligation bydirected ligation chemistry
So, A. P. (2004) · Nucleic Acids Research · doi:10.1093/nar/gnh082 · Cited by 90 · see citing works
Cai, X., Li, M., Vrana, J. A., & Schaller, M. D. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.7.2857-2868.2006 · Cited by 85 · see citing works
Human Schistosomiasis Is Associated with Endotoxemia and Toll-Like Receptor 2- and 4-Bearing B Cells
Onguru, D., Liang, Y., Griffith, Q., Nikolajczyk, B. S., Mwinzi, P. N. M., & Ganley-Leal, L. M. (2011) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2011.10-0397 · Cited by 74 · see citing works
CD14 Employs Hydrophilic Regions to “Capture” Lipopolysaccharides
Cunningham, M., Shapiro, R. A., Seachord, C. L., et al. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.6.3255 · Cited by 73 · see citing works
Potential role for excretory–secretory forms of glutathione-S-transferase (GST) in Fasciola hepatica
Cervi, L., ROSSI, G., & Masih, D. T. (1999) · Parasitology · doi:10.1017/s003118209900517x · Cited by 73 · see citing works
Fasciola hepatica Fatty Acid Binding Protein Induces the Alternative Activation of Human Macrophages
Figueroa-Santiago, O., & Espino, A. M. (2014) · Infection and Immunity · doi:10.1128/iai.02541-14 · Cited by 67 · see citing works
Self-citationPiazza, M., Rossini, C., Fiorentina, S. D., Pozzi, C., Comelli, F., Bettoni, I., Fusi, P. A., Costa, B., & Peri, F. (2009) · Journal of Medicinal Chemistry · doi:10.1021/jm801333m · Cited by 66 · see citing works
Martínez‐Fernández, A. R., Nogal‐Ruiz, J. J., López‐Abán, J., Ramajo, V., Oleaga, A., Manga-González, Y., Hillyer, G. V., & Muro, A. (2004) · Veterinary Parasitology · doi:10.1016/j.vetpar.2004.07.023 · Cited by 64 · see citing works
Flynn, R. J., & Mulcahy, G. M. (2007) · Infection and Immunity · doi:10.1128/iai.00732-07 · Cited by 60 · see citing works
Proximity ligation: A specific and versatile tool for the proteomic era
Söderberg, O., Leuchowius, K.-J., Kamali-Moghaddam, M., Jarvius, M., Gustafsdottir, S., Schallmeiner, E., Gullberg, M., Jarvius, J., & Landegren, U. (2007) · Genetic Engineering · doi:10.1007/978-0-387-34504-8_5 · Cited by 59 · see citing works
Alternative activation of ruminant macrophages by Fasciola hepatica
Flynn, R. J., Irwin, J. A., Olivier, M., Sekiya, M., Dalton, J. P., & Mulcahy, G. M. (2007) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2007.07.003 · Cited by 58 · see citing works
Fasciola hepatica Tegumental Coat Impairs Mast Cells’ Ability To Drive Th1 Immune Responses
Vukman, K. V., Adams, P. N., Metz, M., Maurer, M., & O’Neill, S. M. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1203011 · Cited by 56 · see citing works
Shuto, T., Kato, K., Mori, Y., Viriyakosol, S., Oba, M., Furuta, T., Okiyoneda, T., Arima, H., Suico, M. A., & Kai, H. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.10.102 · Cited by 55 · see citing works
Haçarız, O., Sayers, G., & Baykal, A. T. (2012) · Journal of Proteome Research · doi:10.1021/pr300015p · Cited by 50 · see citing works
López‐Abán, J., Casanueva, P., Nogal‐Ruiz, J. J., Arias, M., Morrondo, P., Díez-Baños, P., Hillyer, G. V., Martínez‐Fernández, A. R., & Muro, A. (2007) · Veterinary Parasitology · doi:10.1016/j.vetpar.2006.12.017 · Cited by 44 · see citing works
Verbon, A., Meijers, J. C. M., Spek, C. A., et al. (2002) · The Journal of Infectious Diseases · doi:10.1086/346043 · Cited by 44 · see citing works
Distribution of 28.5kDa antigen in the tegument of adult Fasciola gigantica
Anuracpreeda, P., Wanichanon, C., Chaithirayanon, K., et al. (2006) · Acta Tropica · doi:10.1016/j.actatropica.2006.09.006 · Cited by 40 · see citing works
Anuracpreeda, P., Wanichanon, C., Chawengkirtikul, R., et al. (2009) · Experimental Parasitology · doi:10.1016/j.exppara.2009.08.014 · Cited by 38 · see citing works
Vukman, K. V., Adams, P. N., & O’Neill, S. M. (2013) · Parasite Immunology · doi:10.1111/pim.12033 · Cited by 36 · see citing works
Morales, A., & Espino, A. M. (2012) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00487-12 · Cited by 36 · see citing works
Self-citationMendes, R. E., Zafra, R., Pérez-Écija, R. A., et al. (2010) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02762010000500017 · Cited by 33 · see citing works
Simpson, P. B., Mistry, M. S., Maki, R. A., et al. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.7.3333 · Cited by 32 · see citing works
Asai, Y., Hashimoto, M., & Ogawa, T. (2003) · European Journal of Immunology · doi:10.1002/eji.200324219 · Cited by 29 · see citing works
Wenzel, J., Held, C., Palmisano, R., et al. (2011) · Frontiers in Physiology · doi:10.3389/fphys.2011.00071 · Cited by 25 · see citing works
Gaudier, J. F., Cabán-Hernández, K., Osuna, A., et al. (2012) · Clinical and Vaccine Immunology · doi:10.1128/cvi.05501-11 · Cited by 25 · see citing works
Self-citationFirst Demonstration of the Role of TNF in the Pathogenesis of Disease
Vilček, J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.1.5 · Cited by 25 · see citing works
Vaccine strategies against schistosomiasis
Capron, A., Dessaint, J., Capron, M., et al. (1992) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02761992000900001 · Cited by 24 · see citing works
Anuracpreeda, P., Wanichanon, C., & Sobhon, P. (2009) · Experimental Parasitology · doi:10.1016/j.exppara.2009.03.007 · Cited by 23 · see citing works
Espino, A. M., & Hillyer, G. V. (2001) · Journal of Parasitology · doi:10.1645/0022-3395(2001)087[0426:iofami]2.0.co;2 · Cited by 21 · see citing works
Self-citationThe tegument of Schistosoma mansoni: genes, antigens and the host-parasite relationship
Xavier, E. M., Lucena‐Silva, N., Werkhäuser, R. P., et al. (1998) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02761998000700011 · Cited by 11 · see citing works
Brazilian dengue virus type 1 replication in mosquito cell cultures
Barth, O. M., & Schatzmayr, H. G. (1992) · Memórias do Instituto Oswaldo Cruz · doi:10.1590/s0074-02761992000100001 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Modulation of Host Immunity by Helminths: The Expanding Repertoire of Parasite Effector Molecules
Maizels, R. M., Smits, H. H., & McSorley, H. J. (2018) · Immunity · doi:10.1016/j.immuni.2018.10.016 · Cited by 435 · see citing works
Ramos-Benítez, M. J., Ruiz-Jiménez, C., Aguayo, V., & Espino, A. M. (2017) · Scientific Reports · doi:10.1038/s41598-017-05735-w · Cited by 41 · see citing works
Self-citation
- Authors
- Martin, I., Cabán-Hernández, K., Figueroa-Santiago, O., & Espino, A. M.
- Affiliations
- University of Puerto Rico, Medical Sciences Campus (PR)
- Corresponding author
- Espino, Ana M
- ORCID
- Espino, Ana M
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-04
- Volume
- 194
- Issue
- 8
- Pages
- 3924-3936
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC4390499
- OpenAlex
- W2121445620
- Cited by
- 95
- References
- 86
- Citations by year
- 2026: 6 · 2025: 8 · 2024: 5 · 2023: 5 · 2022: 8 · 2021: 9 · 2020: 13 · 2019: 11 · 2018: 5 · 2017: 15 · 2016: 7 · 2015: 3
- FWCI
- 4.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of General Medical Sciences (P20GM103642, R25GM061838)
- National Institute of Allergy and Infectious Diseases (SC1AI096108)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Health Sciences › Medicine › Epidemiology › Sepsis Diagnosis and Treatment
- Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
- Keywords
- Fasciola hepatica, fatty acid binding protein, TLR4, lipopolysaccharide, septic shock, anti-inflammatory activity, macrophages, inflammatory cytokines, ERK1/2 phosphorylation, MAPK signaling, phagocytosis, innate immunity
- MeSH terms
- Animals, Bone Marrow Cells, Fasciola hepatica, Female, Inflammation, Lipopolysaccharides, Macrophages, Phosphorylation, Shock, Septic, Helminth Proteins, Cytokines, Mice, Knockout, Lipopolysaccharide Receptors, Extracellular Signal-Regulated MAP Kinases, Fatty Acid-Binding Proteins, Toll-Like Receptor 4, Mice, Nitric Oxide Synthase Type II
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
