Filarial antigens mediate apoptosis of human monocytes through toll-like receptor 4

Journal of Infectious Diseases

Volumn 210, Issue 7, 2014, Pages 1133-1144

  Mohapatra, Alok Das ^a,c   Panda, Santosh Kumar ^a,d   Pradhan, Anjan Kumar ^a   Prusty, Birendra Kumar ^a   Satapathy, Ashok Kumar ^b   Ravindran, Balachandran ^a  

^a INSTITUTE OF LIFE SCIENCES   (India)

^b REGIONAL MEDICAL RESEARCH CENTRE ICMR   (India)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

Apoptosis; Filariasis; Immunosuppression; Monocytes; TLR4

Indexed keywords

BRUGIA PAHANGI ANTIGEN; CARBOXYFLUORESCEIN DIACETATE SUCCINIMIDYL ESTER; CASPASE 3; PARASITE ANTIGEN; PHYTOHEMAGGLUTININ; THYMIDINE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; TLR4 PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MACROPHAGE; BRUGIA PAHANGI; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; FILARIASIS; FLOW CYTOMETRY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MONOCYTE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMA; PRIORITY JOURNAL; T LYMPHOCYTE; TUNEL ASSAY; WUCHERERIA BANCROFTI; ANIMAL; CELL PROLIFERATION; COHORT ANALYSIS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; ANTIGENS, HELMINTH; APOPTOSIS; BRUGIA PAHANGI; CELL PROLIFERATION; COHORT STUDIES; FILARIASIS; FLOW CYTOMETRY; HUMANS; IMMUNE TOLERANCE; MONOCYTES; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4; WUCHERERIA BANCROFTI;

EID: 84922393361     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu208     Document Type: Article

References (48)

1. Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003;3:733-44.
2. Anthony RM, Rutitzky LI, Urban JF Jr, Stadecker MJ, Gause WC. Protective immune mechanisms in helminth infection. Nat Rev Immunol 2007;7:975-87.
3. Ravindran B, Satapathy AK, Sahoo PK, Mohanty MC. Protective immunity in human lymphatic filariasis: problems and prospects. Med Microbiol Immunol 2003;192:41-6.
4. Smith P, Walsh CM, Mangan NE, et al. Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. J Immunol 2004;173:1240-8.
5. King CL, Mahanty S, Kumaraswami V, et al. Cytokine control of parasitespecific anergy inhumanlymphaticfilariasis. Preferential inductionof a regulatory T helper type 2 lymphocyte subset. J Clin Invest 1993;92:1667-73.
6. Sasisekhar B, Aparna M, Augustin DJ, et al. Diminished monocyte function in microfilaremic patients with lymphatic filariasis and its relationship to altered lymphoproliferative responses. Infect Immun 2005;73:3385-93.
7. Semnani RT, Liu AY, Sabzevari H, et al. Brugia malayi microfilariae induce cell death in human dendritic cells, inhibit their ability to make IL-12 and IL-10, and reduce their capacity to activate CD4+ T cells. J Immunol 2003;171:1950-60.
8. Dai WJ, Gottstein B. Nitric oxide-mediated immunosuppression following murine Echinococcus multilocularis infection. Immunol 1999;97:107-16.
9. Jenson JS, O'Connor R, Osborne J, Devaney E. Infection with Brugia microfilariae induces apoptosis of CD4 (+) T lymphocytes: a mechanism of immune unresponsiveness in filariasis. Euro J Immunol 2002;32:858-67.
10. O'Connor RA, Devaney E. Nitric oxide limits the expansion of antigenspecific T cells in mice infected with the microfilariae of Brugia pahangi. Infect Immun 2002;70:5997-6004.
11. Babu S, Blauvelt CP, Nutman TB. Filarial parasites induce NK cell activation, type 1 and type 2 cytokine secretion, and subsequent apoptotic cell death. J Immunol 2007;179:2445-56.
12. Cros J, Cagnard N, Woollard K, et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010;33:375-86.
13. Mahanty S, Mollis SN, Ravichandran M, et al. High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J Infect Dis 1996;173:769-73.
14. Semnani RT, Keiser PB, Coulibaly YI, et al. Filaria-induced monocyte dysfunction and its reversal following treatment. Infect Immun 2006;74:4409-17.
15. Panda SK, Kumar S, Tupperwar NC, et al. Chitohexaose activates macrophages by alternate pathway through TLR4 and blocks endotoxemia. PLoS Pathog 2012;8:e1002717.
16. Poltorak A, He X, Smirnova I, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998;282:2085-8.
17. Loke P, MacDonald AS, Robb A, Maizels RM, Allen JE. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur J Immunol 2000;30:2669-78.
18. Whelan M, Harnett MM, Houston KM, Patel V, Harnett W, Rigley KP. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J Immunol 2000;164:6453-60.
19. Semnani RT, Venugopal PG, Mahapatra L, et al. Induction of TRAIL- and TNF-alpha-dependent apoptosis in human monocyte-derived dendritic cells by microfilariae of Brugia malayi. J Immunol 2008;181:7081-9.
20. Semnani RT, Sabzevari H, Iyer R, Nutman TB. Filarial antigens impair the function of human dendritic cells during differentiation. Infect Immun 2001;69:5813-22.
21. Nichols JE, Niles JA, Roberts NJ Jr. Human lymphocyte apoptosis after exposure to influenza A virus. J Virol 2001;75:5921-9.
22. Genini D, Sheeter D, Rought S, et al. HIV induces lymphocyte apoptosis by a p53-initiated, mitochondrial-mediated mechanism. FASEB J 2001;15:5-6.
23. Kemp K, Bruunsgaard H, Skinhoj P, Klarlund Pedersen B. Pneumococcal infections in humans are associated with increased apoptosis and trafficking of type 1 cytokine-producing T cells. Infect Immun 2002;70:5019-25.
24. Illera VA, Perandones CE, Stunz LL, Mower DA Jr, Ashman RF. Apoptosis in splenic B lymphocytes. Regulation by protein kinase C and IL-4. J Immunol 1993;151:2965-73.
25. Lundy SK, Lerman SP, Boros DL. Soluble egg antigen-stimulated T helper lymphocyte apoptosis and evidence for cell death mediated by FasL (+) T and B cells during murine Schistosoma mansoni infection. Infect Immun 2001;69:271-80.
26. Ribeiro-Gomes FL, Silva MT, Dosreis GA. Neutrophils, apoptosis and phagocytic clearance: an innate sequence of cellular responses regulating intramacrophagic parasite infections. Parasitol 2006;132(suppl):S61-8.
27. Gobert AP, Cheng Y, Wang JY, et al. Helicobacter pylori induces macrophage apoptosis by activation of arginase II. J Immun 2002;168:4692-700.
28. Ciaramella A, Cavone A, Santucci MB, et al. Induction of apoptosis and release of interleukin-1 beta by cell wall-associated 19-kDa lipoprotein during the course of mycobacterial infection. J Infect Dis 2004;190:1167-76.
29. Zychlinsky A, Thirumalai K, Arondel J, Cantey JR, Aliprantis AO, Sansonetti PJ. In vivo apoptosis in Shigella flexneri infections. Infect Immun 1996;64:5357-65.
30. Krishnamoorthy B, Renner W, Balakrishnan A. Apoptosis induced by filarial parasitic sheath protein in HEp 2 cell lines blocked by ectopic expression of bcl 2. Cell Biol Int 1998;22:483-92.
31. Melendez AJ, Harnett MM, Pushparaj PN, et al. Inhibition of Fc epsilon RI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nat Med 2007;13:1375-81.
32. Babu S, Blauvelt CP, Kumaraswami V, Nutman TB. Diminished expression and function of TLR in lymphatic filariasis: a novel mechanism of immune dysregulation. J Immunol 2005;175:1170-6.
33. Zarember KA, Godowski PJ. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 2002;168:554-61.
34. Ganley-Leal LM, Liang Y, Jagannathan-Bogdan M, Farraye FA, Nikolajczyk BS. Differential regulation of TLR4 expression in human B cells and monocytes. Mol Immunol 2010;48:82-8.
35. Rasooly R, Schuster GU, Gregg JP, Xiao JH, Chandraratna RA, Stephensen CB. Retinoid x receptor agonists increase bcl2a1 expression and decrease apoptosis of naive T lymphocytes. J Immunol 2005;175:7916-29.
36. Watson RW, Rotstein OD, Parodo J, Bitar R, Marshall JC. The IL-1 beta-converting enzyme (caspase-1) inhibits apoptosis of inflammatory neutrophils through activation of IL-1 beta. J Immunol 1998;161:957-62.
37. Rogers PM, Beale PJ, Al-Moundhri M, et al. Overexpression of BclXL in a human ovarian carcinoma cell line: paradoxic effects on chemosensitivity in vitro versus in vivo. Int J Cancer 2002;97:858-63.
38. Belge KU, Dayyani F, Horelt A, et al. The proinflammatory CD14+CD16+DR++ monocytes are a major source of TNF. J Immunol 2002;168:3536-42.
39. Abeles RD, McPhail MJ, Sowter D, et al. CD14, CD16 and HLA-DR reliably identifies human monocytes and their subsets in the context of pathologically reduced HLA-DR expression by CD14 (hi)/CD16 (neg) monocytes: expansion of CD14 (hi)/CD16 (pos) and contraction of CD14 (lo)/CD16 (pos) monocytes in acute liver failure. Cytometry A 2012;81:823-34.
40. Zhao C, Tan YC, Wong WC, et al. The CD14+/lowCD16+ monocyte subset is more susceptible to spontaneous and oxidant-induced apoptosis than the CD14+ CD16-subset. Cell Death Dis 2010;1:e95.
41. Ancuta P, Liu KY, Misra V, et al. Transcriptional profiling reveals developmental relationship and distinct biological functions of CD16+ and CD16-monocyte subsets. BMC Genomics 2009;10:403.
42. Zawada AM, Rogacev KS, Rotter B, et al. SuperSAGE evidence for CD14++ CD16+ monocytes as a third monocyte subset. Blood 2011;118:e50-61.
43. Wei S, Marches F, Borvak J, et al. Toxoplasma gondii-infected human myeloid dendritic cells induce T-lymphocyte dysfunction and contactdependent apoptosis. Infect Immun 2002;70:1750-60.
44. Antoine-Moussiaux N, Cornet A, Cornet F, Glineur S, Dermine M, Desmecht D. A non-cytosolic protein of Trypanosoma evansi induces CD45-dependent lymphocyte death. PLoS One 2009;4:e5728.
45. Semnani RT, Law M, Kubofcik J, Nutman TB. Filaria-induced immune evasion: suppression by the infective stage of Brugia malayi at the earliest host-parasite interface. J Immunol 2004;172:6229-38.
46. Fujiwara RT, Cancado GG, Freitas PA, et al. Necator americanus infection: a possible cause of altered dendritic cell differentiation and eosinophil profile in chronically infected individuals. PLoS Negl Trop Dis 2009;3:e399.
47. Schierack P, Lucius R, Sonnenburg B, Schilling K, Hartmann S. Parasitespecific immunomodulatory functions of filarial cystatin. Infect Immun 2003;71:2422-9.
48. Kamalakannan V, Kirthika S, Haripriya KI, Babu S, Narayanan RB. Wolbachia heat shock protein 60 induces pro-inflammatory cytokines and apoptosis in monocytes in vitro. Microbes Infect 2012;14:610-8.