Staphylococcus aureus Infection in Humanized Mice: A New Model to Study Pathogenicity Associated with Human Immune Response

Journal of Infectious Diseases

Volumn 212, Issue 3, 2015, Pages 435-444

  Knop, Janin ^a   Hanses, Frank ^a   Leist, Teresa ^a   Archin, Nancie M ^c   Buchholz, Stefan ^a   Gläsner, Joachim ^b   Gessner, André ^b   Wege, Anja K ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

caspase 3; fas receptor; humanized mice (HM); Staphylococcus aureus; T cell apoptosis

Indexed keywords

FAS ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; CASPASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL INVASION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE RESPONSE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECIES DIFFERENCE; STAPHYLOCOCCUS INFECTION; SURVIVAL; SURVIVAL RATE; T LYMPHOCYTE; WEIGHT REDUCTION; WILD TYPE; ANIMAL; B LYMPHOCYTE; CELL CULTURE; DISEASE MODEL; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; STAPHYLOCOCCUS AUREUS; TRANSGENIC MOUSE; VIRULENCE;

ANIMALS; ANTIGENS, CD95; APOPTOSIS; B-LYMPHOCYTES; CASPASE 3; CELLS, CULTURED; DISEASE MODELS, ANIMAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, TRANSGENIC; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; T-LYMPHOCYTES; VIRULENCE;

EID: 84939534435     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv073     Document Type: Article

References (50)

1. Fowler VG Jr, Miro JM, Hoen B, et al. Staphylococcus aureus endocarditis: A consequence of medical progress. JAMA 2005; 293:3012-21.
2. Duerden BI. MRSA: why have we got it and can we do anything about it? Eye (Lond) 2012; 26:218-21.
3. Wertheim HF, Melles DC, Vos MC, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 2005; 5:751-62.
4. Schaumburg F, Köck R, Mellmann A, et al. Population dynamics among methicillin-resistant Staphylococcus aureus isolates in Germany during a 6-year period. J Clin Microbiol 2012; 50:3186-92.
5. BubeckWardenburg J, Bae T, Otto M, Deleo FR, Schneewind O. Poring over pores: Alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 2007; 13:1405-6.
6. Heilbronner S, Hanses F, Monk IR, Speziale P, Foster TJ. Sortase A promotes virulence in experimental Staphylococcus lugdunensis endocarditis. Microbiology 2013; 159:2141-52.
7. Thammavongsa V, Missiakas DM, Schneewind O. Staphylococcus aureus degrades neutrophil extracellular traps to promote immune cell death. Science 2013; 342:863-6.
8. de Haas CJ, Veldkamp KE, Peschel A, et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 2004; 199:687-95.
9. Athanasopoulos AN, Economopoulou M, Orlova VV, et al. The extracellular adherence protein (Eap) of Staphylococcus aureus inhibits wound healing by interfering with host defense and repair mechanisms. Blood 2006; 107:2720-7.
10. Mestas J, Hughes CC. Of mice and not men: Differences between mouse and human immunology. J Immunol 2004; 172:2731-8.
11. Schneemann M, Schoedon G. Species differences in macrophage NO production are important. Nat Immunol 2002; 3:102.
12. Piper RD, Cook DJ, Bone RC, et al. Introducing critical appraisal to studies of animal models investigating novel therapies in sepsis. Crit Care Med 1996; 24:2059-70.
13. Redl H, Bahrami S, Schlag G, Traber DL. Clinical detection of LPS and animal models of endotoxemia. Immunobiology 1993; 187:330-45.
14. Warren HS. Mouse models to study sepsis syndrome in humans. J Leukoc Biol 2009; 86:199-201.
15. Löffler B, Hussain M, Grundmeier M, et al. Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog 2010; 6:e1000715.
16. Cassidy P, Harshman S. Studies on the binding of staphylococcal 125Ilabeled alpha-toxin to rabbit erythrocytes. Biochemistry 1976; 15:2348-55.
17. Verkaik NJ, van Wamel WJ, van Belkum A. Immunotherapeutic Approaches Against Staphylococcus aureus. Immunotherapy 2011; 3: 1063-73.
18. Proctor RA. Challenges for a universal Staphylococcus aureus vaccine. Clin Infect Dis 2012; 54:1179-86.
19. Fowler VG, Allen KB, Moreira ED, et al. Effect of an investigational vaccine for preventing Staphylococcus aureus infections after cardiothoracic surgery: A randomized trial. JAMA 2013; 309:1368-78.
20. Rittirsch D, Hoesel LM, Ward PA. The disconnect between animal models of sepsis and human sepsis. J Leukoc Biol 2007; 81:137-43.
21. Michie HR. The value of animal models in the development of new drugs for the treatment of sepsis syndrome. J Antimicrob Chemother 1998; 41:47-9.
22. Riedemann NC, Guo RF,Ward PA. Novel strategies for the treatment of sepsis. Nat Med 2003; 9:517-24.
23. Seok J, Warren HS, Cuenca AG, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci USA 2013; 110:3507-12.
24. Ishikawa F, Yasukawa M, Lyons B, et al. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 2005; 106:1565-73.
25. Ernst W, Zimara N, Hanses F, Männel DN, Seelbach-Göbel B, Wege AK. Humanized mice, a new model to study the influence of drug treatment on neonatal sepsis. Infect Immun 2013; 81:1520-31.
26. Strommenger B, Kettlitz C, Weniger T, Harmsen D, Friedrich AW, Witte W. Assignment of Staphylococcus isolates to groups by spa typing, SmaI macrorestriction analysis, and multilocus sequence typing. J Clin Microbiol 2006; 44:2533-40.
27. Shultz LD, Ishikawa F, Greiner DL. Humanized mice in translational biomedical research. Nat Rev Immunol 2007; 7:118-30.
28. Wege AK, Florian C, Ernst W, et al. Leishmania major infection in humanized mice induces systemic infection and provokes a nonprotective human immune response. PLoS Negl Trop Dis 2012; 6:e1741.
29. Brehm MA, Jouvet N, Greiner DL, Shultz LD. Humanized mice for the study of infectious diseases. Curr Opin Immunol 2013; 25:428-35.
30. Bone RC. Sir Isaac Newton, sepsis, SIRS, and CARS. Crit Care Med 1996; 24:1125-8.
31. Renno T, Attinger A, Locatelli S, Bakker T, Vacheron S, MacDonald HR. Cutting edge: Apoptosis of superantigen-activated T cells occurs preferentially after a discrete number of cell divisions in vivo. J Immunol 1999; 162:6312-5.
32. McKallip RJ, Do Y, Fisher MT, Robertson JL, Nagarkatti PS, Nagarkatti M. Role of CD44 in activation-induced cell death: CD44-deficient mice exhibit enhanced T cell response to conventional and superantigens. Int Immunol 2002; 14:1015-26.
33. Krammer PH, Arnold R, Lavrik IN. Life and death in peripheral T cells. Nat Rev Immunol 2007; 7:532-42.
34. Oberholzer C, Oberholzer A, Clare-Salzler M, Moldawer LL. Apoptosis in sepsis: A new target for therapeutic exploration. FASEB J 2001; 15: 879-92.
35. Hotchkiss RS, Swanson PE, Freeman BD, et al. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit Care Med 1999; 27:1230-51.
36. Hotchkiss RS, Tinsley KW, Swanson PE, et al. Sepsis-induced apoptosis causes progressive profound depletion of B and CD4+ T lymphocytes in humans. J Immunol 2001; 166:6952-63.
37. Papathanassoglou ED, Moynihan JA, McDermott MP, Ackerman MH. Expression of Fas (CD95) and Fas ligand on peripheral blood mononuclear cells in critical illness and association with multiorgan dysfunction severity and survival. Crit Care Med 2001; 29:709-18.
38. CheadleWG, Pemberton RM, Robinson D, Livingston DH, Rodriguez JL, Polk HC Jr. Lymphocyte subset responses to trauma and sepsis. J Trauma 1993; 35:844-9.
39. Unsinger J, McDonough JS, Shultz LD, Ferguson TA, Hotchkiss RS. Sepsis-induced human lymphocyte apoptosis and cytokine production in "humanized" mice. J Leukoc Biol 2009; 86:219-27.
40. Zhang J, Xu X, Liu Y. Activation-Induced Cell Death in T Cells and Autoimmunity. Cell Mol Immunol 2004; 1:186-92.
41. Chang KC, Unsinger J, Davis CG, et al. Multiple triggers of cell death in sepsis: death receptor and mitochondrial-mediated apoptosis. FASEB J 2007; 21:708-19.
42. Kotzin BL, Leung DY, Kappler J, Marrack P. Superantigens and their potential role in human disease. Adv Immunol 1993; 54:99-166.
43. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 2000; 13:16-34.
44. Niebuhr M, Gathmann M, Scharonow H, et al. Staphylococcal alphatoxin is a strong inducer of interleukin-17 in humans. Infect Immun 2011; 79:1615-22.
45. Nygaard TK, Pallister KB, DuMont AL, et al. Alpha-toxin induces programmed cell death of human T cells, B cells, and monocytes during USA300 infection. PLoS One 2012; 7:e36532.
46. Bantel H, Sinha B, Domschke W, Peters G, Schulze-Osthoff K, Jänicke RU. alpha-Toxin is a mediator of Staphylococcus aureus-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J Cell Biol 2001; 155:637-48.
47. Panacek EA, Marshall JC, Albertson TE, et al. Monoclonal Anti-TNF: A Randomized Controlled Sepsis Study Investigators. Efficacy and safety of the monoclonal anti-tumor necrosis factor antibody F(ab')2 fragment afelimomab in patients with severe sepsis and elevated interleukin-6 levels. Crit Care Med 2004; 32:2173-82.
48. Llewelyn M, Sriskandan S, Peakman M, et al. HLA class II polymorphisms determine responses to bacterial superantigens. J Immunol 2004; 172:1719-26.
49. Kappler J, Kotzin B, Herron L, et al. V beta-specific stimulation of human T cells by staphylococcal toxins. Science 1989; 244:811-3.
50. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J Exp Med 2002; 195:59-70.