Advertisement

Inflammation

, Volume 38, Issue 1, pp 224–244 | Cite as

Differential Induction of Inflammatory Cytokines and Reactive Oxygen Species in Murine Peritoneal Macrophages and Resident Fresh Bone Marrow Cells by Acute Staphylococcus aureus Infection: Contribution of Toll-Like Receptor 2 (TLR2)

  • Ajeya Nandi
  • Somrita Dey
  • Julie Biswas
  • Pooja Jaiswal
  • Shamreen Naaz
  • Tamima Yasmin
  • Biswadev Bishayi
Article

Abstract

Among the known Toll-like receptors (TLRs), Toll-like receptor 2 (TLR2) is a key sensor for detecting Staphylococcus aureus invasion. But the function of TLR2 during S. aureus infection in different cell populations is unclear. Two different cell subtypes were chosen to study the interaction of S. aureus with TLR2 because macrophages are extremely different from one compartment to another and their capacity to respond to live bacteria or bacterial products differs from one site to another. The contribution of TLR2 to the host innate response against acute live S. aureus infection and heat-killed S. aureus (HKSA) using anti-TLR2 antibody in murine peritoneal macrophages and resident fresh bone marrow cells has been investigated here. TLR2 blocking before infection induces the release of interleukin (IL)-10 by macrophages thereby inhibiting excessive production of oxidants by activating antioxidant enzymes. TLR2-blocked peritoneal macrophages showed impaired release of tumor necrosis factor-alpha (TNF-α), interferon-gamma (IFN-γ) and IL-6 in response to both live and heat-killed S. aureus infection except bone marrow cells. TLR2-mediated free radical production and killing of S. aureus were modulated by TLR2 blocking in peritoneal macrophages and resident bone marrow cells. This study supported that S. aureus persists in resident bone marrow cells in a state of quiescence.

KEY WORDS

antioxidant enzymes bone marrow cells intracellular survival murine peritoneal macrophages Staphylococcus aureus Swiss albino mice Toll-like receptor 2 

Abbreviations

CPCSEA

Committee for the Purpose of Control and Supervision of Experiments on Animal

EDTA

Ethylenediaminetetraacetic acid

FBMCs

Fresh bone marrow cells

FBS

Fetal bovine serum

HBSS

Hank’s balanced salt solution

iNOS

Inducible nitric oxide synthase

NaNO3

Sodium nitrate

NaOH

Sodium hydroxide

NaCl

Sodium chloride

PAMP

Pathogen-associated molecular pattern

TLR2

Toll-like receptor 2

TLRs

Toll-like receptors

Notes

ACKNOWLEDGMENTS

This work was supported/funded by the Department of Science and Technology (DST), Science and Engineering Research Board (SERB), Ministry of Science and Technology, Government of India, New Delhi, India [Grant Number: SR/SO/HS/0013/2012, dated 21 May 2013 to Biswadev Bishayi]. The author (BB) is indebted to the Department of Science and Technology, Government of India for providing the instruments procured under the DST-PURSE programme to the Department of Physiology, University of Calcutta. The Department of Science and Technology, Government of India is also thanked for providing the DST-INSPIRE fellowship to Mrs. Ajeya Nandi [Grant Number: DST INSPIRE FELLOWSHIP/2013/1118, dated 23 June 2014]. The authors remained thankful to Dr Debajit Bhowmick, Ph.D., CU BD COE Manager, of the Centre for Research in Nanoscience and Nanotechnology, Acharya Prafulla Chandra Roy Siksha Prangan affiliated to the University of Calcutta, JD-2, Sector III, Salt Lake, Kolkata 700098, West Bengal, India for performing the flow cytometry.

Conflict of Interest

All authors declared that they have no conflict of interest. They also state that they do not have a direct financial relation with the commercial identities mentioned in this manuscript that might lead to a conflict of interest.

REFERENCES

  1. 1.
    Lowy, F.D. 1998. Staphylococcus aureus infections. New England Journal of Medicine 339: 520–532.CrossRefPubMedGoogle Scholar
  2. 2.
    Garzoni, C., and W.L. Kelley. 2009. Staphylococcus aureus: new evidence for intracellular persistence. Trends in Microbiology 17: 59–65.CrossRefPubMedGoogle Scholar
  3. 3.
    Cohen, J. 2002. The immunopathogenesis of sepsis. Nature 420: 885–891.CrossRefPubMedGoogle Scholar
  4. 4.
    Bronner, S., H. Monteil, and G. Prévost. 2004. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiology Reviews 28: 183–200.CrossRefPubMedGoogle Scholar
  5. 5.
    Wang, J.E., P.F. Jørgensen, M. Almlöf, C. Thiemermann, S.J. Foster, A.O. Aasen, and R. Solberg. 2000. Peptidoglycan and lipoteichoic acid from Staphylococcus aureus induce tumor necrosis factor alpha, interleukin 6 (IL-6), and IL-10 production in both T cells and monocytes in a human whole blood model. Infection and Immunity 68: 3965–3970.CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    Müller-Anstett, M.A., P. Müller, T. Albrecht, M. Nega, J. Wagener, Q. Gao, S. Kaesler, M. Schaller, T. Biedermann, and F. Götz. 2010. Staphylococcal peptidoglycan co-localizes with Nod2 and TLR2 and activates innate immune response via both receptors in primary murine keratinocytes. PloS One 5: e13153.CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Mattsson, E., R. Heying, J.S. van de Gevel, T. Hartung, and H. Beekhuizen. 2008. Staphylococcal peptidoglycan initiates an inflammatory response and procoagulant activity in human vascular endothelial cells: a comparison with highly purified lipoteichoic acid and TSST-1. FEMS Immunology and Medical Microbiology 52: 110–117.CrossRefPubMedGoogle Scholar
  8. 8.
    Gillrie, M.R., L. Zbytnuik, E. McAvoy, R. Kapadia, K. Lee, C.C.M. Waterhouse, S.P. Davis, D.A. Muruve, P. Kubes, and M. Ho. 2010. Divergent roles of Toll-like receptor 2 in response to lipoteichoic acid and Staphylococcus aureus in vivo. European Journal of Immunology 40: 1639–1650.CrossRefPubMedGoogle Scholar
  9. 9.
    Fournier, B., and D.J. Philpott. 2005. Recognition of Staphylococcus aureus by the innate immune system. Clinical Microbiology Reviews 18: 521–540.CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Kubica, M., K. Guzik, J. Koziel, M. Zarebski, W. Richter, B. Gajkowska, A. Golda, A.M. Gudowska, K. Brix, L. Shaw, T. Foster, and J. Potempa. 2008. A potential new pathway for Staphylococcus aureus dissemination: the silent survival of S. aureus phagocytosed by human monocyte-derived macrophages. PloS One 3: e1409.CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Von Köckritz-Blickwede, M., M. Rohde, S. Oehmcke, L.S. Miller, A.L. Cheung, H. Herwald, S. Foster, and E. Medina. 2008. Immunological mechanisms underlying the genetic predisposition to severe Staphylococcus aureus infection in the mouse model. American Journal of Pathology 173: 1657–1668.CrossRefGoogle Scholar
  12. 12.
    Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783–801.CrossRefPubMedGoogle Scholar
  13. 13.
    Hoebe, K., P. Georgel, S. Rutschmann, X. Du, S. Mudd, K. Crozat, S. Sovath, L. Shamel, T. Hartung, U. Zähringer, and B. Beutler. 2005. CD36 is a sensor of diacylglycerides. Nature 433: 523–527.CrossRefPubMedGoogle Scholar
  14. 14.
    Silva, M.T. 2011. Macrophage phagocytosis of neutrophils at inflammatory/infectious foci: a cooperative mechanism in the control of infection and infectious inflammation. Journal of Leukocyte Biology 89: 675–683.CrossRefPubMedGoogle Scholar
  15. 15.
    Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805–820.CrossRefPubMedGoogle Scholar
  16. 16.
    Takeuchi, O., K. Hoshino, T. Kawai, H. Sanjo, T. Ogawa, H. Takada, K. Takeda, and S. Akira. 1999. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11: 443–451.CrossRefPubMedGoogle Scholar
  17. 17.
    Knuefermann, P., Y. Sakata, J.S. Baker, C.H. Huang, K. Sekiguchi, H.S. Hardarson, O. Takeuchi, S. Akira, and J.G. Vallejo. 2004. Toll-like receptor 2 mediates Staphylococcus aureus-induced myocardial dysfunction and cytokine production in the heart. Circulation 110: 3693–3698.CrossRefPubMedGoogle Scholar
  18. 18.
    Spiller, S., G. Elson, R. Ferstl, S. Dreher, T. Mueller, M. Freudenberg, B. Daubeuf, H. Wagner, and C.J. Kirschning. 2008. TLR-4 induced IFN-γ production increases TLR-2 sensitivity and drives Gram negative sepsis in mice. Journal of Experimental Medicine 205: 1747–1754.CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    Netea, M.G., J.W.M. Van der Meer, and B.J. Kullberg. 2004. Toll-like receptors as an escape mechanism from the host defense. Trends in Microbiology 12: 484–488.CrossRefPubMedGoogle Scholar
  20. 20.
    Arko-Mensah, J., E. Julian, M. Singh, and C. Fernández. 2007. TLR2 but not TLR4 signalling is critically involved in the inhibition of IFN-γ induced killing of Mycobacteria by murine macrophages. Scandinavian Journal of Immunology 65: 148–157.CrossRefPubMedGoogle Scholar
  21. 21.
    Watanabe, I., M. Ichiki, A. Shiratsuchi, and Y. Nakanishi. 2007. TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. Journal of Immunology 178: 4917–4925.CrossRefGoogle Scholar
  22. 22.
    Singh, A., D. Rost, N. Tvardovskaia, A. Roggenkamp, A. Wiedemann, C.J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits toll-like receptor 2 and CD14 for interleukin 10 mediated immunosuppression. Journal of Experimental Medicine 196: 1017–1024.CrossRefGoogle Scholar
  23. 23.
    Strunk, T., P. Richmond, A. Prosser, K. Simmer, O. Levy, D. Burgner, and A. Currie. 2011. Method of bacterial killing differentially affects the human innate immune response to Staphylococcus epidermidis. Innate Immunity 17: 508–516.CrossRefPubMedGoogle Scholar
  24. 24.
    Dong, C., H. Sexton, A. Gertrudes, T. Akama, S. Martin, C. Virtucio, C.W. Chen, X. Fan, A. Wu, W. Bu, L. Liu, L. Feng, K. Jarnagin, and Y.R. Freund. 2013. Inhibition of Toll-like receptor-mediated inflammation in vitro and in vivo by a novel benzoxaborole. Journal of Pharmacology and Experimental Therapeutics 344: 436–446.CrossRefPubMedGoogle Scholar
  25. 25.
    Kondo, T., T. Kawai, and S. Akira. 2012. Dissecting negative regulation of Toll-like receptor signaling. Trends in Microbiology 33: 450–460.Google Scholar
  26. 26.
    Takeuchi, O., K. Hoshino, and S. Akira. 2000. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. Journal of Immunology 165: 5392–5396.CrossRefGoogle Scholar
  27. 27.
    Shin, J.E., Y.S. Kim, J.E. Oh, B.M. Min, and Y. Choi. 2010. Treponema denticola suppresses expression of human beta defensin-3 in gingival epithelial cells through inhibition of the toll-like receptor 2 axis. Infection and Immunity 78: 672–679.CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Das, D., and B. Bishayi. 2009. Staphylococcal catalase protects intracellularly survived bacteria by destroying H2O2 produced by the murine peritoneal macrophages. Microbial Pathogenesis 47: 57–67.CrossRefPubMedGoogle Scholar
  29. 29.
    Paul-Clark, M.J., S.K. McMaster, and R. Sorrentino. 2009. Toll-like receptor 2 is essential for sensing of oxidants during inflammation. American Journal of Respiratory and Critical Care Medicine 179: 299–306.CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    Sorci, G., and B. Faivre. 2009. Inflammation and oxidative stress in vertebrate host-parasite system. Philosophical Transactions of the Royal Society B 364: 71–83.CrossRefGoogle Scholar
  31. 31.
    West, A.P., I.E. Brodsky, C. Rahner, D.K. Woo, H. Erdjument-Bromage, P. Tempst, M.C. Walsh, Y. Choi, S. Gerald, G.S. Shadel, and S. Ghosh. 2011. TLR signalling augments macrophage bactericidal activity through mitochondrial ROS. Nature 272: 476–482.CrossRefGoogle Scholar
  32. 32.
    Martínez-Pulgarín, S., G. Dominguez-Bernal, J.A. Orden, and R. de la Fuente. 2009. Simultaneous lack of catalase and beta-toxin in Staphylococcus aureus leads to increased intracellular survival in macrophages and epithelial cells and to attenuated virulence in murine and ovine models. Microbiology 155: 1505–1515.CrossRefPubMedGoogle Scholar
  33. 33.
    Mal, P., S. Dutta, D. Bandyopadhyay, K. Dutta, A. Basu, and B. Bishayi. 2012. Gentamicin in combination with ascorbic acid regulates the severity of Staphylococcus aureus infection-induced septic arthritis in mice. Scandinavian Journal of Immunology 76: 528–540.CrossRefPubMedGoogle Scholar
  34. 34.
    Mathias, S., J.J. Naja, F. Ferracin, and R. Landmann. 2011. T and B cells are not required for clearing Staphylococcus aureus in systemic infection despite a strong TLR2–MyD88-dependent T cell activation. Journal of Immunology 186: 443–452.CrossRefGoogle Scholar
  35. 35.
    Marim, F.M., T.N. Silveira, D.S. Lima Jr., and D.S. Zamboni. 2010. A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PloS One 5: e15263.CrossRefPubMedCentralPubMedGoogle Scholar
  36. 36.
    Das, D., and B. Bishayi. 2010. Contribution of catalase and superoxide dismutase to the intracellular survival of clinical isolates of Staphylococcus aureus in murine macrophages. Indian Journal of Microbiology 50: 375–384.CrossRefPubMedCentralPubMedGoogle Scholar
  37. 37.
    Lancioni, C.L., Q. Li, J.J. Thomas, X.D. Ding, B. Thiel, M.G. Drage, N.D. Pecora, A.G. Ziady, S. Shank, C.V. Harding, W.H. Boom, and R.E. Rojas. 2011. Mycobacterium tuberculosis lipoproteins directly regulate human memory CD4+ T cell activation via Toll-like receptors 1 and 2. Infection and Immunity 79: 663–673.CrossRefPubMedCentralPubMedGoogle Scholar
  38. 38.
    Swisher, J.F.A., N. Burton, S.M. Bacot, S.N. Vogel, and G.M. Feldman. 2010. Annexin A2 tetramer activates human and murine macrophages through TLR4. Blood 115: 549–558.CrossRefPubMedCentralPubMedGoogle Scholar
  39. 39.
    Gebbia, J.A., J.L. Coleman, and J.L. Benach. 2004. Selective induction of matrix metalloproteinases by Borrelia burgdorferi via Toll-like receptors 2 in monocyte. Journal of Infectious Diseases 189: 113–119.CrossRefPubMedGoogle Scholar
  40. 40.
    Sen, R., D. Das, and B. Bishayi. 2010. Staphylococcal catalase regulates its virulence and induces arthritis in catalase deficient mice. Indian Journal of Physiology and Pharmacology 53: 307–317.Google Scholar
  41. 41.
    Leigh, P.C.J., R. van Furth, and T.L. van Zwet. 1986. In vitro determination of phagocytosis and intracellular killing by polymorphonuclear and mononuclear phagocytes. In Handbook of experimental Immunology, ed. D.M. Weir, 46.1–46.26. Oxford: Blackwell Scientific.Google Scholar
  42. 42.
    Absolom, D.R. 1986. Basic methods for the study of phagocytosis. Methods Enzymology 132: 95–180.CrossRefGoogle Scholar
  43. 43.
    Bae, Yun Soo, Jee Hyun Lee, Soo Ho. Choi, Sunah Kim, Felicidad Almazan, Joseph L. Witztum, and Yury I. Miller. 2009. Macrophages generate reactive oxygen species in response to minimally oxidized low density lipoprotein: Toll like receptor 4 and spleen tyrosine kinase dependent activation of NADPH oxidase-2. Circulation Research 104: 210–218.CrossRefPubMedCentralPubMedGoogle Scholar
  44. 44.
    Nandi, D., M.K. Mishra, A. Basu, and B. Bishayi. 2010. Protective effects of interleukin-6 in lipopolysaccharide (LPS)-induced experimental endotoxemia is linked to alteration in hepatic anti-oxidant enzymes and endogenous cytokines. Immunobiology 215: 443–451.CrossRefPubMedGoogle Scholar
  45. 45.
    Mal, P., D. Ghosh, D. Bandyopadhyay, K. Dutta, and B. Bishayi. 2012. Ampicillin alone and in combination with riboflavin modulates Staphylococcus aureus infection induced septic arthritis in mice. Indian Journal of Experimental Biology 50: 677–689.PubMedGoogle Scholar
  46. 46.
    Bishayi, B., D. Bandyopadhyay, A. Majhi, and R. Adhikary. 2014. Possible role of Toll like receptor-2 (TLR-2) in the intracellular survival of Staphylococcus aureus in murine peritoneal macrophages: involvement of cytokines and anti-oxidant enzymes. Scandinavian Journal of Immunology 80: 127–143.CrossRefPubMedGoogle Scholar
  47. 47.
    Miller, R.A., and B.E. Britigan. 1997. Role of oxidants in microbial pathophysiology. Clinical Microbiology Reviews 10: 1–18.PubMedCentralPubMedGoogle Scholar
  48. 48.
    Philippart, F., C. Fitting, and J.M. Cavaillon. 2012. Lung microenvironment contributes to the resistance of alveolar macrophages to develop tolerance to endotoxin. Critical Care Medicine 40: 2987–2996.CrossRefPubMedGoogle Scholar
  49. 49.
    Gautier, E.L., T. Shay, J. Miller, M. Greter, C. Jakubzick, S. Ivanov, J. Helft, A. Chow, K.G. Elpek, S. Gordonov, A.R. Mazloom, A. Ma’ayan, W.J. Chua, T.H. Hansen, S.J. Turley, M. Merad, and G.J. Randolph. 2012. Gene expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nature Immunology 13: 1118–1128.CrossRefPubMedCentralPubMedGoogle Scholar
  50. 50.
    Michelsen, K.S., A. Aicher, M. Mohaupt, T. Hartung, S. Dimmeler, C.J. Kirschning, and R.R. Schumann. 2001. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS): peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. Journal of Biological Chemistry 276: 25680–25686.CrossRefPubMedGoogle Scholar
  51. 51.
    Schwandner, R., R. Dziarski, H. Wesche, M. Rothe, and C.J. Kirschning. 1999. Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll like receptor 2. Journal of Biological Chemistry 274: 17406–17409.CrossRefPubMedGoogle Scholar
  52. 52.
    Dziarski, R., and D. Gupta. 2005. Staphylococcus aureus peptidoglycan is a Toll-like receptor 2 activator: a reevaluation. Infection and Immunity 73: 5212–5216.CrossRefPubMedCentralPubMedGoogle Scholar
  53. 53.
    Mae, M., M. Iyori, M. Yasuda, H.M. Shamsul, H. Kataoka, K. Kiura, A. Hasebe, Y. Totsuka, and K. Shibata. 2007. The diacylated lipopeptide FSL-1 enhances phagocytosis of bacteria by macrophages through a Toll-like receptor 2-mediated signaling pathway. FEMS Immunology and Medical Microbiology 49: 398–409.CrossRefPubMedGoogle Scholar
  54. 54.
    Jann, N.J., M. Schmaler, F. Ferracin, and R. Landmann. 2011. TLR2 enhances NADPH oxidase activity and killing of Staphylococcus aureus by PMN. Immunology Letters 135: 17–23.CrossRefPubMedGoogle Scholar
  55. 55.
    Stuart, L.M., J. Deng, J.M. Silver, K. Takahashi, A.A. Tseng, E.J. Hennessy, R.A.B.. Ezekowitz, and K.J. Moore. 2005. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. Journal of Cell Biology 170: 477–485.Google Scholar
  56. 56.
    Yimin, M. Kohanawa, Z. Songji, M. Ozaki, S. Haga, G. Nan, Y. Kuge, and N. Tamaki. 2013. Contribution of Toll-like receptor 2 to the innate response against Staphylococcus aureus infection in mice. PloS One 9: e74287.CrossRefGoogle Scholar
  57. 57.
    Rigby, K.M., and F.R. DeLeo. 2012. Neutrophils in innate host defense against Staphylococcus aureus infections. Seminars in Immunopathology 34: 237–259.CrossRefPubMedCentralPubMedGoogle Scholar
  58. 58.
    Heumann, D., C. Barras, A. Severin, M.P. Glauser, and A. Tomasz. 1994. Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infection and Immunity 62: 2715–2721.PubMedCentralPubMedGoogle Scholar
  59. 59.
    Timmerman, C.P., E. Mattsson, L. Martinez-Martinez, L. De Graaf, J.A. Van Strijp, H.A. Verbrugh, J. Verhoef, and A. Fleer. 1993. Induction of release of tumor necrosis factor from human monocytes by staphylococci and staphylococcal peptidoglycans. Infection and Immunity 61: 4167–4172.PubMedCentralPubMedGoogle Scholar
  60. 60.
    Wakabayashi, G., J.A. Gelfand, W.K. Jung, R.J. Connolly, J.F. Burke, and C.A. Dinarello. 1991. Staphylococcus epidermidis induces complement activation, tumor necrosis factor and interleukin-1, a shock-like state and tissue injury in rabbits without endotoxemia. Comparison to Escherichia coli. Journal of Clinical Investigation 87: 1925–1935.CrossRefPubMedCentralPubMedGoogle Scholar
  61. 61.
    Jiang, W., B. Li, X. Zheng, X. Liu, Y. Cen, J. Li, X. Pan, H. Cao, J. Zheng, and H. Zhou. 2011. Artesunate in combination with oxacillin protect sepsis model mice challenged with lethal live methicillin-resistant Staphylococcus aureus (MRSA) via its inhibition on proinflammatory cytokines release and enhancement on antibacterial activity of oxacillin. International Immunopharmacology 11: 1065–1073.CrossRefPubMedGoogle Scholar
  62. 62.
    Frodermann, V., T.A. Chau, S. Sayedyahossein, J.M. Toth, D.E. Heinrichs, and J. Madrenas. 2011. A modulatory interleukin-10 response to staphylococcal peptidoglycan prevents Th1/Th17 adaptive immunity to Staphylococcus aureus. Journal of Infectious Diseases 204: 253–262.CrossRefPubMedGoogle Scholar
  63. 63.
    Manicassamy, S., and B. Pulendran. 2009. Modulation of adaptive immunity with Toll-like receptors. Seminars in Immunology 21: 185–193.CrossRefPubMedCentralPubMedGoogle Scholar
  64. 64.
    Deshmukh, H.S., J.B. Hamburger, S.H. Ahn, D.G. McCafferty, S.R. Yang, G. Vance, and Fowler Jr. 2009. Critical role of NOD2 in regulating the immune response to Staphylococcus aureus. Infection and Immunity 77: 1376–1382.CrossRefPubMedCentralPubMedGoogle Scholar
  65. 65.
    Schindler, H., M.B. Lutz, M. Röllinghoff, and C. Bogdan. 2001. The production of IFN-γ by IL-12/IL-18-activated macrophages requires STAT4 signaling and is inhibited by IL-4. Journal of Immunology 166: 3075–3082.CrossRefGoogle Scholar
  66. 66.
    Presky, D.H., H. Yang, L.J. Minetti, A.O. Chua, N. Nabavi, C.Y. Wu, M.K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two beta-type cytokine receptor subunits. Proceedings of the National Academy of Sciences of the United States of America 93: 14002–14007.CrossRefPubMedCentralPubMedGoogle Scholar
  67. 67.
    Torres, D., M. Barrier, F. Bihl, V.J.F. Quesniaux, I. Maillet, S. Akira, B. Ryffel, and F. Erard. 2004. Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infection and Immunity 72: 2131–2139.CrossRefPubMedCentralPubMedGoogle Scholar
  68. 68.
    Conroy, H., N.A. Marshall, and K.H. Mills. 2008. TLR ligand suppression or enhancement of Treg cells? A double-edged sword in immunity to tumors. Oncogene 27: 168–180.CrossRefPubMedGoogle Scholar
  69. 69.
    Henderson, B., and S.P. Nair. 2003. Hard labour: bacterial infection of the skeleton. Trends in Microbiology 11: 570–577.CrossRefPubMedGoogle Scholar
  70. 70.
    Ellington, J.K., S.S. Reilly, W.K. Ramp, M.S. Smeltzer, J.F. Kellam, and M.C. Hudson. 1999. Mechanisms of Staphylococcus aureus invasion of cultured osteoblasts. Microbial Pathogenesis 26: 317–323.CrossRefPubMedGoogle Scholar
  71. 71.
    Hudson, M.C., W.K. Ramp, N.C. Nicholson, A.S. Williams, and M.T. Nousiainen. 1995. Internalization of Staphylococcus aureus by cultured osteoblasts. Microbial Pathogenesis 19: 409–419.CrossRefPubMedGoogle Scholar
  72. 72.
    Jevon, M., C. Guo, B. Ma, N. Mordan, S.P. Nair, M. Harris, B. Henderson, G. Bentley, and S. Meghji. 1999. Mechanisms of internalization of Staphylococcus aureus by cultured human osteoblasts. Infection and Immunity 67: 2677–2681.PubMedCentralPubMedGoogle Scholar
  73. 73.
    Khalil, H., R.J. Williams, G. Stenbeck, B. Henderson, S. Meghji, and S.P. Nair. 2007. Invasion of bone cells by Staphylococcus epidermidis. Microbes and Infection 9: 460–465.CrossRefPubMedGoogle Scholar
  74. 74.
    Reilly, S.S., M.C. Hudson, J.F. Kellam, and W.K. Ramp. 2000. In vivo internalization of Staphylococcus aureus by embryonic chick osteoblasts. Bone 26: 63–70.CrossRefPubMedGoogle Scholar
  75. 75.
    Kwan, T.S., M. Padrines, S. Theoleyre, D. Heymann, and Y. Fortun. 2004. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Reviews 15: 49–60.CrossRefGoogle Scholar
  76. 76.
    Mundy, G.R. 1991. Inflammatory mediators and the destruction of bone. Journal of Periodontal Research 26: 213–217.CrossRefPubMedGoogle Scholar
  77. 77.
    Pfeilschifter, J., C. Chenu, A. Bird, G.R. Mundy, and G.D. Roodman. 1989. Interleukin-1 and tumor necrosis factor stimulate the formation of human osteoclast-like cells in vitro. Journal of Bone and Mineral Research 4: 113–118.CrossRefPubMedGoogle Scholar
  78. 78.
    Tokukoda, Y., S. Takata, H. Kaji, R. Kitazawa, T. Sugimoto, and K. Chihara. 2001. Interleukin-1beta stimulates transendothelial mobilization of human peripheral blood mononuclear cells with a potential to differentiate into osteoclasts in the presence of osteoblasts. Journal of Endocrinology 48: 443–452.Google Scholar
  79. 79.
    Ishimi, Y., C. Miyaura, C.H. Jin, T. Akatsu, E. Abe, Y. Nakamura, A. Yamaguchi, S. Yoshiki, T. Matsuda, and T. Hirano. 1990. IL-6 is produced by osteoblasts and induces bone resorption. Journal of Immunology 145: 3297–3303.Google Scholar
  80. 80.
    Kotake, S., K. Sato, K.J. Kim, N. Takahashi, N. Udagawa, I. Nakamura, A. Yamaguchi, T. Kishimoto, T. Suda, and S. Kashiwazaki. 1996. Interleukin-6 and soluble interleukin-6 receptors in the synovial fluids from rheumatoid arthritis patients are responsible for osteoclast-like cell formation. Journal of Bone and Mineral Research 11: 88–95.CrossRefPubMedGoogle Scholar
  81. 81.
    Meghji, S., S.J. Crean, P.A. Hill, M. Sheikh, S.P. Nair, K. Heron, B. Henderson, E.B. Mawer, and M. Harris. 1998. Surface-associated protein from Staphylococcus aureus stimulates osteoclastogenesis: possible role in S. aureus-induced bone pathology. British Journal of Rheumatology 37: 1095–1101.CrossRefPubMedGoogle Scholar
  82. 82.
    Nair, S., Y. Song, S. Meghji, K. Reddi, M. Harris, A. Ross, S. Poole, M. Wilson, and B. Henderson. 1995. Surface-associated proteins from Staphylococcus aureus demonstrate potent bone resorbing activity. Journal of Bone and Mineral Research 10: 726–734.CrossRefPubMedGoogle Scholar
  83. 83.
    Yokoyama, R., S. Itoh, G. Kamoshida, T. Takii, S. Fujii, T. Tsuji, and K. Onozakia. 2012. Staphylococcal superantigen-like protein 3 binds to the Toll-like receptor 2 extracellular domain and inhibits cytokine production induced by Staphylococcus aureus, cell wall component, or lipopeptides in murine macrophages. Infection and Immunity 80: 2816–2825.CrossRefPubMedCentralPubMedGoogle Scholar
  84. 84.
    Wright, J.A., and S.P. Nair. 2010. Interaction of staphylococci with bone. International Journal of Medical Microbiology 300: 193–204.CrossRefPubMedCentralPubMedGoogle Scholar
  85. 85.
    Bosse, M.J., H.E. Gruber, and W.K. Ramp. 2005. Internalization of bacteria by osteoblasts in a patient with recurrent, long-term osteomyelitis: a case report. Journal of Bone and Joint Surgery 87: 1343–1347.CrossRefPubMedGoogle Scholar
  86. 86.
    Hamza, T., M. Dietz, D. Pham, N. Clovis, S. Danley, and B. Li. 2013. Intracellular Staphylococcus aureus alone causes infection in vivo. European Cells and Materials 25: 341–350.PubMedCentralPubMedGoogle Scholar
  87. 87.
    Facecchia, K., L.A. Fochesato, S.D. Ray, S.J. Stohs, and S. Pandey. 2011. Oxidative toxicity in neurodegenerative diseases: role of mitochondrial dysfunction and therapeutic strategies. Journal of Toxicology :Article ID 683728. doi: 10.1155/2011/683728
  88. 88.
    Hampton, M.B., A.J. Kettle, and C.C. Winterbourn. 1998. Inside the neutrophil phagosome: oxidants, myeloperoxidase and bacterial killing. Blood 92: 3007–3017.PubMedGoogle Scholar
  89. 89.
    Stor, Z.G., L.A. Tartaglia, S.B. Farr, and B.N. Ames. 1990. Bacterial defense against oxidative stress. Trends in Genetics 6: 363–368.CrossRefGoogle Scholar
  90. 90.
    Bogdan, C., M. Rollinghoff, and A. Diefenach. 2000. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion Immunology 12: 64–76.CrossRefGoogle Scholar
  91. 91.
    Komuro, I., N. Keicho, A. Iwamoto, and K.S. Akagawa. 2001. Human alveolar macrophages and granulocyte macrophages colony stimulating factor-induced monocyte derived macrophages are resistant to H2O2 via their high basal and inducible levels of catalase activity. Journal of Biological Chemistry 276: 24360–24364.CrossRefPubMedGoogle Scholar
  92. 92.
    Tripp, C.S., S.F. Wolf, and E.R. Unanue. 1993. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proceedings of the National Academy of Sciences of the United States of America 90: 3725–3729.CrossRefPubMedCentralPubMedGoogle Scholar
  93. 93.
    Bishayi, B., D. Bandyopadhyay, A. Majhi, and R. Adhikary. 2014. Expression of CXCR1 (interleukin-8 receptor) in murine macrophages after Staphylococcus aureus infection and its possible implication on intracellular survival correlating with cytokines and bacterial anti-oxidant enzymes. Inflammation. doi: 10.1007/s10753-014-9991-1.Google Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Ajeya Nandi
    • 1
  • Somrita Dey
    • 1
  • Julie Biswas
    • 1
  • Pooja Jaiswal
    • 1
  • Shamreen Naaz
    • 1
  • Tamima Yasmin
    • 1
  • Biswadev Bishayi
    • 1
  1. 1.Department of Physiology, Immunology LaboratoryUniversity of Calcutta, University Colleges of Science and TechnologyCalcuttaIndia

Personalised recommendations