Attenuation of massive cytokine response to the staphylococcal enterotoxin B superantigen by the innate immunomodulatory protein lactoferrin

Clinical and Experimental Immunology

Volumn 157, Issue 1, 2009, Pages 60-70

  Hayworth, J L ^b   Kasper, K J ^b   Leon Ponte, M ^b   Herfst, C A ^b   Yue, D ^b   Brintnell, W C ^b   Mazzuca, D M ^b   Heinrichs, D E ^b   Cairns, E ^b   Madrenas, J ^b,c   Hoskin, D W ^e   McCormick, J K ^b,d   Haeryfar, S M M ^a,b,d  

^a WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

^d LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^e DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Cytokine; Lactoferrin; Staphylococcal enterotoxin B; Superantigen

Indexed keywords

BOVINE LACTOFERRIN; CYTOKINE; HLA DR4 ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; LACTOFERRIN; STAPHYLOCOCCUS ENTEROTOXIN B; SUPERANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERICIDAL ACTIVITY; BACTERIOSTASIS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG EFFECT; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IRON BINDING CAPACITY; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAPHYLOCOCCUS INFECTION; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPROTEINS; CATTLE; CELL PROLIFERATION; ENTEROTOXINS; FEMALE; FLOW CYTOMETRY; HLA-DR4 ANTIGEN; HUMANS; INTERLEUKIN-2; JURKAT CELLS; LACTOFERRIN; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SERUM ALBUMIN; STAPHYLOCOCCAL INFECTIONS; SUPERANTIGENS; T-LYMPHOCYTES; TRANSFERRIN;

EID: 66849129513     PISSN: 00099104     EISSN: 13652249     Source Type: Journal    
DOI: 10.1111/j.1365-2249.2009.03963.x     Document Type: Article

References (51)

1. Llewelyn M, Cohen J. Superantigens: microbial agents that corrupt immunity. Lancet Infect Dis 2002 2 : 156 62.
2. McCormick JK, Yarwood JM, Schlievert PM. Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 2001 55 : 77 104. (Pubitemid 32978101)
3. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 2000 13 : 16 34, table. (Pubitemid 30039341)
4. Ferry T, Thomas D, Perpoint T et al. Analysis of superantigenic toxin Vbeta T-cell signatures produced during cases of staphylococcal toxic shock syndrome and septic shock. Clin Microbiol Infect 2008 14 : 546 54.
5. Fey PD, Said-Salim B, Rupp ME et al. Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2003 47 : 196 203. (Pubitemid 36070364)
6. Bergdoll MS. Immunization of rhesus monkeys with enterotoxoid B. J Infect Dis 1966 116 : 191 6.
7. Hamad AR, Herman A, Marrack P, Kappler JW. Monoclonal antibodies defining functional sites on the toxin superantigen staphylococcal enterotoxin B. J Exp Med 1994 180 : 615 21.
8. Boles JW, Pitt ML, LeClaire RD et al. Generation of protective immunity by inactivated recombinant staphylococcal enterotoxin B vaccine in nonhuman primates and identification of correlates of immunity. Clin Immunol 2003 108 : 51 9.
9. Woody MA, Krakauer T, Stiles BG. Staphylococcal enterotoxin B mutants (N23K and F44S): biological effects and vaccine potential in a mouse model. Vaccine 1997 15 : 133 9.
10. Stiles BG, Garza AR, Ulrich RG, Boles JW. Mucosal vaccination with recombinantly attenuated staphylococcal enterotoxin B and protection in a murine model. Infect Immun 2001 69 : 2031 6.
11. Coffman JD, Zhu J, Roach JM, Bavari S, Ulrich RG, Giardina SL. Production and purification of a recombinant Staphylococcal enterotoxin B vaccine candidate expressed in Escherichia coli. Protein Expr Purif 2002 24 : 302 12.
12. Buonpane RA, Churchill HR, Moza B et al. Neutralization of staphylococcal enterotoxin B by soluble, high-affinity receptor antagonists. Nat Med 2007 13 : 725 9.
13. Yang X, Buonpane RA, Moza B et al. Neutralization of multiple staphylococcal superantigens by a single-chain protein consisting of affinity-matured, variable domain repeats. J Infect Dis 2008 198 : 344 8.
14. Lonnerdal B, Iyer S. Lactoferrin: molecular structure and biological function. Annu Rev Nutr 1995 15 : 93 110.
15. Tomita M, Wakabayashi H, Shin K, Yamauchi K, Yaeshima T, Iwatsuki K. Twenty-five years of research on bovine lactoferrin applications. Biochimie 2009 91 : 52 7.
16. Bullen JJ, Rogers HJ, Leigh L. Iron-binding proteins in milk and resistance to Escherichia coli infection in infants. BMJ 1972 1 : 69 75.
17. Ellison RT III., Giehl TJ. Killing of Gram-negative bacteria by lactoferrin and lysozyme. J Clin Invest 1991 88 : 1080 91.
18. Machnicki M, Zimecki M, Zagulski T. Lactoferrin regulates the release of tumour necrosis factor alpha and interleukin 6 in vivo. Int J Exp Pathol 1993 74 : 433 9.
19. Lee WJ, Farmer JL, Hilty M, Kim YB. The protective effects of lactoferrin feeding against endotoxin lethal shock in germfree piglets. Infect Immun 1998 66 : 1421 6.
20. Talukder MJ, Harada E. Bovine lactoferrin protects lipopolysaccharide- induced diarrhea modulating nitric oxide and prostaglandin E2 in mice. Can J Physiol Pharmacol 2007 85 : 200 8.
21. Dohler JR, Nebermann L. Bovine colostrum in oral treatment of enterogenic endotoxaemia in rats. Crit Care 2002 6 : 536 9.
22. Bhimani RS, Vendrov Y, Furmanski P. Influence of lactoferrin feeding and injection against systemic staphylococcal infections in mice. J Appl Microbiol 1999 86 : 135 44.
23. Conneely OM. Antiinflammatory activities of lactoferrin. J Am Coll Nutr 2001 20 : 389S 95S.
24. Ito K, Bian HJ, Molina M et al. HLA-DR4-IE chimeric class II transgenic, murine class II-deficient mice are susceptible to experimental allergic encephalomyelitis. J Exp Med 1996 183 : 2635 44.
25. Weiss A, Stobo JD. Requirement for the coexpression of T3 and the T cell antigen receptor on a malignant human T cell line. J Exp Med 1984 160 : 1284 99.
26. Ohashi PS, Mak TW, Van den EP et al. Reconstitution of an active surface T3/T-cell antigen receptor by DNA transfer. Nature 1985 316 : 606 9.
27. Hodtsev AS, Choi Y, Spanopoulou E, Posnett DN. Mycoplasma superantigen is a CDR3-dependent ligand for the T cell antigen receptor. J Exp Med 1998 187 : 319 27.
28. Strathdee CA, McLeod MR, Hall JR. Efficient control of tetracycline-responsive gene expression from an autoregulated bi-directional expression vector. Gene 1999 229 : 21 9.
29. Gorga JC, Horejsi V, Johnson DR, Raghupathy R, Strominger JL. Purification and characterization of class II histocompatibility antigens from a homozygous human B cell line. J Biol Chem 1987 262 : 16087 94.
30. Kovats S, Nepom GT, Coleman M, Nepom B, Kwok WW, Blum JS. Deficient antigen-presenting cell function in multiple genetic complementation groups of type II bare lymphocyte syndrome. J Clin Invest 1995 96 : 217 23.
31. Chau TA, McCully ML, Brintnell W et al. Toll-like receptor 2 ligands on the staphylococcal cell wall downregulate superantigen-induced T cell activation and prevent toxic shock syndrome. Nat Med 2009 (in press).
32. Leder L, Llera A, Lavoie PM et al. A mutational analysis of the binding of staphylococcal enterotoxins B and C3 to the T cell receptor beta chain and major histocompatibility complex class II. J Exp Med 1998 187 : 823 33.
33. Stohl W, Xu D, Zang S et al. In vivo staphylococcal superantigen-driven polyclonal Ig responses in mice: dependence upon CD4(+) cells and human MHC class II. Int Immunol 2001 13 : 1291 300.
34. DaSilva L, Welcher BC, Ulrich RG, Aman MJ, David CS, Bavari S. Humanlike immune response of human leukocyte antigen-DR3 transgenic mice to staphylococcal enterotoxins: a novel model for superantigen vaccines. J Infect Dis 2002 185 : 1754 60.
35. Nooh MM, El-Gengehi N, Kansal R, David CS, Kotb M. HLA transgenic mice provide evidence for a direct and dominant role of HLA class II variation in modulating the severity of streptococcal sepsis. J Immunol 2007 178 : 3076 83.
36. Ettinger R, Panka DJ, Wang JK, Stanger BZ, Ju ST, Marshak-Rothstein A. Fas ligand-mediated cytotoxicity is directly responsible for apoptosis of normal CD4+ T cells responding to a bacterial superantigen. J Immunol 1995 154 : 4302 8.
37. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995 155 : 1151 64.
38. Huebers HA, Finch CA. The physiology of transferrin and transferrin receptors. Physiol Rev 1987 67 : 520 82.
39. Bellamy W, Takase M, Wakabayashi H, Kawase K, Tomita M. Antibacterial spectrum of lactoferricin B, a potent bactericidal peptide derived from the N-terminal region of bovine lactoferrin. J Appl Bacteriol 1992 73 : 472 9.
40. Mader JS, Smyth D, Marshall J, Hoskin DW. Bovine lactoferricin inhibits basic fibroblast growth factor- and vascular endothelial growth factor165-induced angiogenesis by competing for heparin-like binding sites on endothelial cells. Am J Pathol 2006 169 : 1753 66.
41. Kuwata H, Yip TT, Tomita M, Hutchens TW. Direct evidence of the generation in human stomach of an antimicrobial peptide domain (lactoferricin) from ingested lactoferrin. Biochim Biophys Acta 1998 1429 : 129 41.
42. Fleischer B, Necker A, Leget C, Malissen B, Romagne F. Reactivity of mouse T-cell hybridomas expressing human Vbeta gene segments with staphylococcal and streptococcal superantigens. Infect Immun 1996 64 : 987 94.
43. Ou LS, Goleva E, Hall C, Leung DY. T regulatory cells in atopic dermatitis and subversion of their activity by superantigens. J Allergy Clin Immunol 2004 113 : 756 63.
44. Hwang SA, Kruzel ML, Actor JK. Influence of bovine lactoferrin on expression of presentation molecules on BCG-infected bone marrow derived macrophages. Biochimie 2009 91 : 76 85.
45. Spadaro M, Caorsi C, Ceruti P et al. Lactoferrin, a major defense protein of innate immunity, is a novel maturation factor for human dendritic cells. FASEB J 2008 22 : 2747 57.
46. de la RG, Yang D, Tewary P, Varadhachary A, Oppenheim JJ. Lactoferrin acts as an alarmin to promote the recruitment and activation of APCs and antigen-specific immune responses. J Immunol 2008 180 : 6868 76.
47. Hopkins PA, Fraser JD, Pridmore AC, Russell HH, Read RC, Sriskandan S. Superantigen recognition by HLA class II on monocytes up-regulates Toll-like receptor 4 and enhances proinflammatory responses to endotoxin. Blood 2005 105 : 3655 62.
48. Kansal RG, Aziz RK, Kotb M. Modulation of expression of superantigens by human transferrin and lactoferrin: a novel mechanism in host-Streptococcus interactions. J Infect Dis 2005 191 : 2121 9.
49. Lopez-Exposito I, Pellegrini A, Amigo L, Recio I. Synergistic effect between different milk-derived peptides and proteins. J Dairy Sci 2008 91 : 2184 9.
50. Tanaka T, Morita H, Yoo YC, Kim WS, Kumura H, Shimazaki K. Detection of bovine lactoferrin binding protein on Jurkat human lymphoblastic T cell line. J Vet Med Sci 2004 66 : 865 9.
51. Mazurier J, Legrand D, Hu WL, Montreuil J, Spik G. Expression of human lactotransferrin receptors in phytohemagglutinin-stimulated human peripheral blood lymphocytes. Isolation of the receptors by antiligand-affinity chromatography. Eur J Biochem 1989 179 : 481 7.