Skip to main content
SpringerLink
Log in

L-4F Inhibits Lipopolysaccharide-Mediated Activation of Primary Human Neutrophils

  • Published:
Inflammation Aims and scope Submit manuscript

Abstract

Human apolipoprotein A-I (apoA-I) mimetic L-4F inhibits acute inflammation in endotoxemic animals. Since neutrophils play a crucial role in septic inflammation, we examined the effects of L-4F, compared to apoA-I, on lipopolysaccharide (LPS)-mediated activation of human neutrophils. We performed bioassays in human blood, isolated human neutrophils (incubated in 50 % donor plasma), and isolated human leukocytes (incubated in 5 and 50 % plasma) in vitro. In whole blood, both L-4F and apoA-I inhibited LPS-mediated elevation of TNF-α and IL-6. In LPS-stimulated neutrophils, L-4F and apoA-I (40 μg/ml) also decreased myeloperoxidase and TNF-α levels; however, L-4F tended to be superior in inhibiting LPS-mediated increase in IL-6 levels, membrane lipid rafts abundance and CD11b expression. In parallel experiments, when TNF-α and IL-8, instead of LPS, was used for cell stimulation, L-4F and/or apoA-I revealed only limited efficacy. In LPS-stimulated leukocytes, L-4F was as effective as apoA-I in reducing superoxide formation in 50 % donor plasma, and more effective in 5 % donor plasma (P < 0.05). Limulus ambocyte lysate (LAL) and surface plasmon resonance assays showed that L-4F neutralizes LAL endotoxin activity more effectively than apoA-I (P < 0.05) likely due to avid binding to LPS. We conclude that (1) direct binding/neutralization of LPS is a major mechanism of L-4F in vitro; (2) while L-4F has similar efficacy to apoA-I in anti-endotoxin effects in whole blood, it demonstrates superior efficacy to apoA-I in aqueous solutions and fluids with limited plasma components. This study rationalizes the utility of L-4F in the treatment of inflammation that is mediated by endotoxin-activated neutrophils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

REFERENCES

  1. Mantovani, A., M.A. Cassatella, C. Costantini, and S. Jaillon. 2011. Neutrophils in the activation and regulation of innate and adaptive immunity. Nature Reviews Immunology 11(8): 519–531.

    Article  PubMed  CAS  Google Scholar 

  2. Brown, K.A., S.D. Brain, J.D. Pearson, J.D. Edgeworth, S.M. Lewis, and D.F. Treacher. 2006. Neutrophils in development of multiple organ failure in sepsis. Lancet 368(9530): 157–169.

    Article  PubMed  CAS  Google Scholar 

  3. Davies, M.J. 2011. Myeloperoxidase-derived oxidation: mechanisms of biological damage and its prevention. Journal of Clinical Biochemistry and Nutrition 48(1): 8–19.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  4. Munford, R.S. 2006. Severe sepsis and septic shock: the role of Gram-negative bacteremia. Annual Review of Pathology 1: 467–496.

    Article  PubMed  CAS  Google Scholar 

  5. Pasterkamp, G., J.K. Van Keulen, and D.P. De Kleijn. 2004. Role of toll-like receptor 4 in the initiation and progression of atherosclerotic disease. European Journal of Clinical Investigation 34(5): 328–334.

    Article  PubMed  CAS  Google Scholar 

  6. Zhou, X., X.P. Gao, J. Fan, Q. Liu, K.N. Anwar, R.S. Frey, and A.B. Malik. 2005. LPS activation of toll-like receptor 4 signals CD11b/CD18 expression in neutrophils. American Journal of Physiology - Lung Cellular and Molecular Physiology 288(4): L655–662.

    Article  PubMed  CAS  Google Scholar 

  7. Sorci-Thomas, M.G., and M.J. Thomas. 2012. High density lipoprotein biogenesis, cholesterol efflux, and immune cell function. Arteriosclerosis, Thrombosis, and Vascular Biology 32(11): 2561–2565.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  8. Barter, P.J., S. Nicholls, K.A. Rye, G.M. Anantharamaiah, M. Navab, and A.M. Fogelman. 2004. Antiinflammatory properties of HDL. Circulation Research 95(8): 764–772.

    Article  PubMed  CAS  Google Scholar 

  9. Blackburn Jr., W.D., J.G. Dohlman, Y.V. Venkatachalapathi, D.J. Pillion, W.J. Koopman, J.P. Segrest, and G.M. Anantharamaiah. 1991. Apolipoprotein A-I decreases neutrophil degranulation and superoxide production. The Journal of Lipid Research 32(12): 1911–1918.

    CAS  Google Scholar 

  10. Liao, X.L., B. Lou, J. Ma, and M.P. Wu. 2005. Neutrophils activation can be diminished by apolipoprotein A-I. Life Sciences 77(3): 325–335.

    Article  PubMed  CAS  Google Scholar 

  11. Murphy, A.J., K.J. Woollard, A. Suhartoyo, R.A. Stirzaker, J. Shaw, D. Sviridov, and J.P. Chin-Dusting. 2011. Neutrophil activation is attenuated by high-density lipoprotein and apolipoprotein A-I in in vitro and in vivo models of inflammation. Arteriosclerosis, Thrombosis, and Vascular Biology 31(6): 1333–1341.

    Article  PubMed  CAS  Google Scholar 

  12. Levine, D.M., T.S. Parker, T.M. Donnelly, A. Walsh, and A.L. Rubin. 1993. In vivo protection against endotoxin by plasma high density lipoprotein. Proceedings of the National Academy of Sciences of the United States of America 90(24): 12040–12044.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  13. Yan, Y.J., Y. Li, B. Lou, and M.P. Wu. 2006. Beneficial effects of ApoA-I on LPS-induced acute lung injury and endotoxemia in mice. Life Sciences 79(2): 210–215.

    Article  PubMed  CAS  Google Scholar 

  14. Shah, P.K., J. Nilsson, S. Kaul, M.C. Fishbein, H. Ageland, A. Hamsten, J. Johansson, F. Karpe, and B. Cercek. 1998. Effects of recombinant apolipoprotein A-I (Milano) on aortic atherosclerosis in apolipoprotein E-deficient mice. Circulation 97(8): 780–785.

    Article  PubMed  CAS  Google Scholar 

  15. Pajkrt, D., J.E. Doran, F. Koster, P.G. Lerch, B. Arnet, T. van der Poll, J.W. ten Cate, and S.J. van Deventer. 1996. Antiinflammatory effects of reconstituted high-density lipoprotein during human endotoxemia. The Journal of Experimental Medicine 184(5): 1601–1608.

    Article  PubMed  CAS  Google Scholar 

  16. Nissen, S.E., T. Tsunoda, E.M. Tuzcu, P. Schoenhagen, C.J. Cooper, M. Yasin, G.M. Eaton, M.A. Lauer, W.S. Sheldon, C.L. Grines, S. Halpern, T. Crowe, J.C. Blankenship, and R. Kerensky. 2003. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA 290(17): 2292–2300.

    Article  PubMed  CAS  Google Scholar 

  17. Kitchens, R.L., P.A. Thompson, S. Viriyakosol, G.E. O’Keefe, and R.S. Munford. 2001. Plasma CD14 decreases monocyte responses to LPS by transferring cell-bound LPS to plasma lipoproteins. The Journal of Clinical Investigation 108(3): 485–493.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  18. Remaley, A.T., M. Amar, and D. Sviridov. 2008. HDL-replacement therapy: mechanism of action, types of agents and potential clinical indications. Expert Review of Cardiovascular Therapy 6(9): 1203–1215.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  19. Garber, D.W., G. Datta, M. Chaddha, M.N. Palgunachari, S.Y. Hama, M. Navab, A.M. Fogelman, J.P. Segrest, and G.M. Anantharamaiah. 2001. A new synthetic class A amphipathic peptide analogue protects mice from diet-induced atherosclerosis. The Journal of Lipid Research 42(4): 545–552.

    CAS  Google Scholar 

  20. Navab, M., G.M. Anantharamaiah, S.T. Reddy, S. Hama, G. Hough, V.R. Grijalva, N. Yu, B.J. Ansell, G. Datta, D.W. Garber, and A.M. Fogelman. 2005. Apolipoprotein A-I mimetic peptides. Arteriosclerosis, Thrombosis, and Vascular Biology 25(7): 1325–1331.

    Article  PubMed  CAS  Google Scholar 

  21. Gupta, H., L. Dai, G. Datta, D.W. Garber, H. Grenett, Y. Li, V. Mishra, M.N. Palgunachari, S. Handattu, S.H. Gianturco, W.A. Bradley, G.M. Anantharamaiah, and C.R. White. 2005. Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein AI mimetic peptide. Circulation Research 97(3): 236–243.

    Article  PubMed  CAS  Google Scholar 

  22. Zhang, Z., G. Datta, Y. Zhang, A.P. Miller, P. Mochon, Y.F. Chen, J. Chatham, G.M. Anantharamaiah, and C.R. White. 2009. Apolipoprotein A-I mimetic peptide treatment inhibits inflammatory responses and improves survival in septic rats. American Journal of Physiology - Heart and Circulatory Physiology 297(2): H866–873.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  23. Kwon, W.Y., G.J. Suh, K.S. Kim, Y.H. Kwak, and K. Kim. 2012. 4F, apolipoprotein AI mimetic peptide, attenuates acute lung injury and improves survival in endotoxemic rats. Journal Trauma Acute Care Surgery 72(6): 1576–1583.

    Article  CAS  Google Scholar 

  24. Sharifov, O.F., X. Xu, A. Gaggar, W.E. Grizzle, V.K. Mishra, J. Honavar, S.H. Litovsky, M.N. Palgunachari, C.R. White, G.M. Anantharamaiah, and H. Gupta. 2013. Anti-inflammatory mechanisms of apolipoprotein a-I mimetic peptide in acute respiratory distress syndrome secondary to sepsis. PLoS One 8(5): e64486.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  25. Madenspacher, J.H., K.M. Azzam, W. Gong, K.M. Gowdy, M.P. Vitek, D.T. Laskowitz, A.T. Remaley, J.M. Wang, and M.B. Fessler. 2012. Apolipoproteins and apolipoprotein mimetic peptides modulate phagocyte trafficking through chemotactic activity. The Journal of Biological Chemistry 287(52): 43730–43740.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  26. Datta, G., M. Chaddha, S. Hama, M. Navab, A.M. Fogelman, D.W. Garber, V.K. Mishra, R.M. Epand, R.F. Epand, S. Lund-Katz, M.C. Phillips, J.P. Segrest, and G.M. Anantharamaiah. 2001. Effects of increasing hydrophobicity on the physical–chemical and biological properties of a class A amphipathic helical peptide. Journal of Lipid Research 42(7): 1096–1104.

    PubMed  CAS  Google Scholar 

  27. Anantharamaiah, G.M., and D.W. Garber. 1996. Chromatographic methods for quantitation of apolipoprotein A-I. Methods in Enzymology 263: 267–282.

    Article  PubMed  CAS  Google Scholar 

  28. Smythies, L.E., C.R. White, A. Maheshwari, M.N. Palgunachari, G.M. Anantharamaiah, M. Chaddha, A.R. Kurundkar, and G. Datta. 2010. Apolipoprotein A-I mimetic 4F alters the function of human monocyte-derived macrophages. American Journal of Physiology - Cellular Physiology 298(6): C1538–1548.

    Article  CAS  Google Scholar 

  29. White, C.R., L.E. Smythies, D.K. Crossman, M.N. Palgunachari, G.M. Anantharamaiah, and G. Datta. 2012. Regulation of pattern recognition receptors by the apolipoprotein A-I mimetic peptide 4F. Arteriosclerosis, Thrombosis, and Vascular Biology 32(11): 2631–2639.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  30. Xu, X., P.L. Jackson, S. Tanner, M.T. Hardison, M. Abdul Roda, J.E. Blalock, and A. Gaggar. 2011. A self-propagating matrix metalloprotease-9 (MMP-9) dependent cycle of chronic neutrophilic inflammation. PLoS One 6(1): e15781.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  31. Iovine, N.M., P. Elsbach, and J. Weiss. 1997. An opsonic function of the neutrophil bactericidal/permeability-increasing protein depends on both its N- and C-terminal domains. Proceedings of the National Academy of Sciences of the United States of America 94(20): 10973–10978.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  32. Sharifov, O.F., G. Nayyar, V.V. Ternovoy, V.K. Mishra, S.H. Litovsky, M.N. Palgunachari, D.W. Garber, G.M. Anantharamaiah, and H. Gupta. 2013. Cationic peptide mR18L with lipid lowering properties inhibits LPS-induced systemic and liver inflammation in rats. Biochemical and Biophysical Research Communications 436(4): 705–710.

    Article  PubMed  CAS  Google Scholar 

  33. Lehmann, V., M.A. Freudenberg, and C. Galanos. 1987. Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and d-galactosamine-treated mice. The Journal of Experimental Medicine 165(3): 657–663.

    Article  PubMed  CAS  Google Scholar 

  34. Nowak, M., G.C. Gaines, J. Rosenberg, R. Minter, F.R. Bahjat, J. Rectenwald, S.L. MacKay, C.K. Edwards 3rd, and L.L. Moldawer. 2000. LPS-induced liver injury in D-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 278(5): R1202–1209.

    PubMed  CAS  Google Scholar 

  35. Lundahl, J., S.H. Jacobson, and J.M. Paulsson. 2012. IL-8 from local subcutaneous wounds regulates CD11b activation. Scandinavian Journal of Immunology 75(4): 419–425.

    Article  PubMed  CAS  Google Scholar 

  36. Olsson, S., and R. Sundler. 2006. The role of lipid rafts in LPS-induced signaling in a macrophage cell line. Molecular Immunology 43(6): 607–612.

    Article  PubMed  CAS  Google Scholar 

  37. Van Lenten, B.J., A.C. Wagner, C.L. Jung, P. Ruchala, A.J. Waring, R.I. Lehrer, A.D. Watson, S. Hama, M. Navab, G.M. Anantharamaiah, and A.M. Fogelman. 2008. Anti-inflammatory apoA-I-mimetic peptides bind oxidized lipids with much higher affinity than human apoA-I. The Journal of Lipid Research 49(11): 2302–2311.

    Article  Google Scholar 

  38. Malle, E., G. Marsche, J. Arnhold, and M.J. Davies. 2006. Modification of low-density lipoprotein by myeloperoxidase-derived oxidants and reagent hypochlorous acid. Biochimica et Biophysica Acta 1761(4): 392–415.

    Article  PubMed  CAS  Google Scholar 

  39. Carr, A.C., and B. Frei. 2002. Human neutrophils oxidize low-density lipoprotein by a hypochlorous acid-dependent mechanism: the role of vitamin C. Biological Chemistry 383(3–4): 627–636.

    PubMed  CAS  Google Scholar 

  40. Memon, R.A., I. Staprans, M. Noor, W.M. Holleran, Y. Uchida, A.H. Moser, K.R. Feingold, and C. Grunfeld. 2000. Infection and inflammation induce LDL oxidation in vivo. Arteriosclerosis, Thrombosis, and Vascular Biology 20(6): 1536–1542.

    Article  PubMed  CAS  Google Scholar 

  41. Nayyar, G., V.K. Mishra, S.P. Handattu, M.N. Palgunachari, R. Shin, D.T. McPherson, C.C. Deivanayagam, D.W. Garber, J.P. Segrest, and G.M. Anantharamaiah. 2012. Sidedness of interfacial arginine residues and anti-atherogenicity of apolipoprotein A-I mimetic peptides. The Journal of Lipid Research 53(5): 849–858.

    Article  CAS  Google Scholar 

  42. Aviram, M., M. Rosenblat, C.L. Bisgaier, R.S. Newton, S.L. Primo-Parmo, and B.N. La Du. 1998. Paraoxonase inhibits high-density lipoprotein oxidation and preserves its functions. A possible peroxidative role for paraoxonase. Journal of Clinic Investment 101(8): 1581–1590.

    Article  CAS  Google Scholar 

  43. Moren, X., S. Deakin, M.L. Liu, M.R. Taskinen, and R.W. James. 2008. HDL subfraction distribution of paraoxonase-1 and its relevance to enzyme activity and resistance to oxidative stress. The Journal of Lipid Research 49(6): 1246–1253.

    Article  CAS  Google Scholar 

  44. Undurti, A., Y. Huang, J.A. Lupica, J.D. Smith, J.A. DiDonato, and S.L. Hazen. 2009. Modification of high density lipoprotein by myeloperoxidase generates a pro-inflammatory particle. The Journal of Biological Chemistry 284(45): 30825–30835.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. White, C.R., G. Datta, A.K. Buck, M. Chaddha, G. Reddy, L. Wilson, M.N. Palgunachari, M. Abbasi, and G.M. Anantharamaiah. 2012. Preservation of biological function despite oxidative modification of the apolipoprotein A-I mimetic peptide 4F. The Journal of Lipid Research 53(8): 1576–1587.

    Article  CAS  Google Scholar 

  46. Lau, D., H. Mollnau, J.P. Eiserich, B.A. Freeman, A. Daiber, U.M. Gehling, J. Brummer, V. Rudolph, T. Munzel, T. Heitzer, T. Meinertz, and S. Baldus. 2005. Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proceedings of the National Academy of Sciences of the United States of America 102(2): 431–436.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  47. El Kebir, D., L. Jozsef, W. Pan, and J.G. Filep. 2008. Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation. Circulation Research 103(4): 352–359.

    Article  PubMed  Google Scholar 

  48. Dai, L., G. Datta, Z. Zhang, H. Gupta, R. Patel, J. Honavar, S. Modi, J.M. Wyss, M. Palgunachari, G.M. Anantharamaiah, and C.R. White. 2010. The apolipoprotein A-I mimetic peptide 4F prevents defects in vascular function in endotoxemic rats. The Journal of Lipid Research 51(9): 2695–2705.

    Article  CAS  Google Scholar 

  49. Yu, B., and S.D. Wright. 1996. Catalytic properties of lipopolysaccharide (LPS) binding protein. Transfer of LPS to soluble CD14. The Journal of Biological Chemistry 271(8): 4100–4105.

    Article  PubMed  CAS  Google Scholar 

  50. Wurfel, M.M., S.T. Kunitake, H. Lichenstein, J.P. Kane, and S.D. Wright. 1994. Lipopolysaccharide (LPS)-binding protein is carried on lipoproteins and acts as a cofactor in the neutralization of LPS. The Journal of Experimental Medicine 180(3): 1025–1035.

    Article  PubMed  CAS  Google Scholar 

  51. McDonald, M.C., P. Dhadly, G.W. Cockerill, S. Cuzzocrea, H. Mota-Filipe, C.J. Hinds, N.E. Miller, and C. Thiemermann. 2003. Reconstituted high-density lipoprotein attenuates organ injury and adhesion molecule expression in a rodent model of endotoxic shock. Shock 20(6): 551–557.

    Article  PubMed  CAS  Google Scholar 

  52. Baetta, R., and A. Corsini. 2010. Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis 210(1): 1–13.

    Article  PubMed  CAS  Google Scholar 

  53. Soehnlein, O. 2012. Multiple roles for neutrophils in atherosclerosis. Circulation Research 110(6): 875–888.

    Article  PubMed  CAS  Google Scholar 

  54. Wiedermann, C.J., S. Kiechl, S. Dunzendorfer, P. Schratzberger, G. Egger, F. Oberhollenzer, and J. Willeit. 1999. Association of endotoxemia with carotid atherosclerosis and cardiovascular disease: prospective results from the Bruneck study. Journal of the American College of Cardiology 34(7): 1975–1981.

    Article  PubMed  CAS  Google Scholar 

  55. Bloedon, L.T., R. Dunbar, D. Duffy, P. Pinell-Salles, R. Norris, B.J. DeGroot, R. Movva, M. Navab, A.M. Fogelman, and D.J. Rader. 2008. Safety, pharmacokinetics, and pharmacodynamics of oral apoA-I mimetic peptide D-4F in high-risk cardiovascular patients. The Journal of Lipid Research 49(6): 1344–1352.

    Article  CAS  Google Scholar 

  56. Watson, C.E., N. Weissbach, L. Kjems, S. Ayalasomayajula, Y. Zhang, I. Chang, M. Navab, S. Hama, G. Hough, S.T. Reddy, D. Soffer, D.J. Rader, A.M. Fogelman, and A. Schecter. 2011. Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function. The Journal of Lipid Research 52(2): 361–373.

    Article  CAS  Google Scholar 

  57. Navab, M., S.T. Reddy, G.M. Anantharamaiah, S. Imaizumi, G. Hough, S. Hama, and A.M. Fogelman. 2011. Intestine may be a major site of action for the apoA-I mimetic peptide 4F whether administered subcutaneously or orally. The Journal of Lipid Research 52(6): 1200–1210.

    Article  CAS  Google Scholar 

  58. Meriwether, D., S. Imaizumi, V. Grijalva, G. Hough, L. Vakili, G.M. Anantharamaiah, R. Farias-Eisner, M. Navab, A.M. Fogelman, S.T. Reddy, and I. Shechter. 2011. Enhancement by LDL of transfer of L-4F and oxidized lipids to HDL in C57BL/6 J mice and human plasma. The Journal of Lipid Research 52(10): 1795–1809.

    Article  CAS  Google Scholar 

  59. Navab, M., S.T. Reddy, G.M. Anantharamaiah, G. Hough, G.M. Buga, J. Danciger, and A.M. Fogelman. 2012. D-4F-mediated reduction in metabolites of arachidonic and linoleic acids in the small intestine is associated with decreased inflammation in low-density lipoprotein receptor-null mice. The Journal of Lipid Research 53(3): 437–445.

    Article  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

SPR experiments and data analysis was performed in Multidisciplinary Molecular Interaction Core (MMIC) facility (NIH Grant 1S10RR026935). This work was supported by NIH grants NHLBI K08HL085282 (H.G.), R01 HL102371 (A.G.), 5R01GM 082952 (C.R.W.), NHLBI HL 34343 (G.M.A.).

Dr. G.M. Anantharamaiah, who is inventor of the peptide L-4F and co-investigator, is a principal in Bruin Pharma, a start-up biotech company.

Author information

Authors and Affiliations

  1. Department of Medicine, University of Alabama at Birmingham, BDB-101, 1808 7th Avenue South, Birmingham, AL, 35294-0012, USA

    Oleg F. Sharifov, Xin Xu, Amit Gaggar, Edlue M. Tabengwa, C. Roger White, Mayakonda N. Palgunachari, G. M. Anantharamaiah & Himanshu Gupta

  2. VA Medical Center, Birmingham, AL, 35294, USA

    Amit Gaggar & Himanshu Gupta

  3. Department of Biochemistry and Molecular Genetics, University of Alabama at Birmingham, Birmingham, AL, 35294-0012, USA

    G. M. Anantharamaiah

Authors
  1. Oleg F. Sharifov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amit Gaggar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edlue M. Tabengwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Roger White
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mayakonda N. Palgunachari
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. M. Anantharamaiah
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Himanshu Gupta
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Himanshu Gupta.

ELECTRONIC SUPPLEMENTARY MATERIAL

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sharifov, O.F., Xu, X., Gaggar, A. et al. L-4F Inhibits Lipopolysaccharide-Mediated Activation of Primary Human Neutrophils. Inflammation 37, 1401–1412 (2014). https://doi.org/10.1007/s10753-014-9864-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10753-014-9864-7

KEY WORDS

Search

Navigation