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References

  1. Pierce GF. 1990. Macrophages: important physiologic and pathologic sources of polypeptide growth factors. Am. J. Respir. Cell Mol. Biol. 2: 233-234.
    Pubmed CrossRef
  2. Jiang WY, Jeon BH, Kim YC, Lee SH, Sohn DH, Seo GS. 2013. PF2401-SF, standardized fraction of Salvia miltiorrhiza shows anti-inflammatory activity in macrophages and acute arthritis in vivo. Int. Immunopharmacol. 16: 160-164.
    Pubmed CrossRef
  3. Werner F, Jain MK, Feinberg MW, Sibinga NE, Pellacani A, Wiesel P, et al. 2000. Transforming growth factor-beta 1 inhibition of macrophage activation is mediated via Smad3. J. Biol. Chem. 275: 36653-36658.
    Pubmed CrossRef
  4. O’Farrell AM, Liu Y, Moore KW, Mui AL. 1998. IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and -independent pathways. EMBO J. 17: 1006-1018.
    Pubmed PMC CrossRef
  5. Sato K, Fujimoto K, Koyama T, Shichiri M. 2010. Release of salusin-beta from human monocytes/macrophages. Regul. Pept. 162: 68-72.
    Pubmed CrossRef
  6. Sun W, Tadmori I, Yang L, Delgado M, Ganea D. 2000. Vasoactive intestinal peptide (VIP) inhibits TGF-beta1 production in murine macrophages. J. Neuroimmunol. 107:88-99.
    CrossRef
  7. Yang LX, Liu H, Guo RW, Ye J, Wang XM, Qi F, et al. 2010. Angiotensin II induces EMMPRIN expression in THP-1 macrophages via the NF-kappa B pathway. Regul. Pept. 163:88-95.
    Pubmed CrossRef
  8. Suzuki E, Umezawa K. 2006. Inhibition of macrophage activation and phagocytosis by a novel NF-kappa B inhibitor, dehydroxymethylepoxyquinomicin. Biomed. Pharmacother. 60: 578-586.
    Pubmed CrossRef
  9. Kim JB, Han AR, Park EY, Kim JY, Cho W, Lee J, et al. 2007. Inhibition of LPS-induced iNOS, COX-2 and cytokines expression by poncirin through the NF-kappa B inactivation in RAW 264.7 macrophage cells. Biol. Pharm. Bull. 30: 23452351.
    CrossRef
  10. Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, et al. 1999. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann. Rheum. Dis. 58: 691-697.
    Pubmed PMC CrossRef
  11. Cunnane G, FitzGerald O, Hummel KM, Youssef PP, Gay RE, Gay S, Bresnihan B. 2001. Synovial tissue protease gene expression and joint erosions in early rheumatoid arthritis. Arthritis Rheum. 44: 1744-1753.
    CrossRef
  12. Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, et al. 1997. Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum. 40: 217-225.
    Pubmed CrossRef
  13. Hansson GK. 2005. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 352: 1685-1695.
    Pubmed CrossRef
  14. Hansson GK, Libby P. 2006. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6:508-519.
    Pubmed CrossRef
  15. Tripathi S, Bruch D, Kittur DS. 2008. Ginger extract inhibits LPS induced macrophage activation and function. BMC Complement. Altern. Med. 8: 1.
    Pubmed PMC CrossRef
  16. Hwang JS, Lee J, Kim YJ, Bang HS, Yun EY, Kim SR, et al. 2009. Isolation and characterization of a defensin-like peptide (coprisin) from the dung beetle, Copris tripartitus. Int. J. Pept. 2009: 136284.
    Pubmed PMC CrossRef
  17. Nam HJ, Oh AR, Nam ST, Kang JK, Chang JS, Kim DH, et al. 2012. The insect peptide CopA3 inhibits lipopolysaccharideinduced macrophage activation. J. Pept. Sci. 18: 650-656.
    Pubmed CrossRef
  18. Kang JK, Hwang JS, Nam HJ, Ahn KJ, Seok H, Kim SK, et al. 2011. The insect peptide coprisin prevents Clostridium difficile-mediated acute inflammation and mucosal damage through selective antimicrobial activity. Antimicrob. Agents Chemother. 55: 4850-4857.
    Pubmed PMC CrossRef
  19. Kim DH, Hwang JS, Lee IH, Nam ST, Hong J, Zhang P, et al. 2015. The insect peptide CopA3 increases colonic epithelial cell proliferation and mucosal barrier function to prevent inflammatory responses in the gut. J. Biol. Chem. 291: 32093223.
  20. Zhang F, Lau SS, Monks TJ. 2011. The cytoprotective effect of N-acetyl-L-cysteine against ROS-induced cytotoxicity is independent of its ability to enhance glutathione synthesis. Toxicol. Sci. 120: 87-97.
    Pubmed PMC CrossRef
  21. Hung LC, Lin CC, Hung SK, Wu BC, Jan MD, Liou SH, Fu SL. 2007. A synthetic analog of alpha-galactosylceramide induces macrophage activation via the TLR4-signaling pathways. Biochem. Pharmacol. 73: 1957-1970.
    Pubmed CrossRef
  22. Onishi J, Roy MK, Juneja LR, Watanabe Y, Tamai Y. 2008. A lactoferrin-derived peptide with cationic residues concentrated in a region of its helical structure induces necrotic cell death in a leukemic cell line (HL-60). J. Pept. Sci. 14: 1032-1038.
    Pubmed CrossRef
  23. Yajima A, Narita N, Narita M. 2008. Recently identified a novel neuropeptide manserin colocalize with the TUNELpositive cells i n the top villi o f the r at d uodenum. J. Pept. Sci. 14: 773-776.
    Pubmed CrossRef
  24. Grunfeld C, Marshall M, Shigenaga JK, Moser AH, Tobias P, Feingold KR. 1999. Lipoproteins inhibit macrophage activation by lipoteichoic acid. J. Lipid Res. 40: 245-252.
    Pubmed
  25. Lee SH, Park DW, Park SC, Park YK, Hong SY, Kim JR, et al. 2009. Calcium-independent phospholipase A2beta-Akt signaling is involved in lipopolysaccharide-induced NADPH oxidase 1 expression and foam cell formation. J. Immunol. 183: 7497-7504.
    Pubmed CrossRef
  26. Kovarik P, Stoiber D, Novy M, Decker T. 1998. Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J. 17: 3660-3668.
    Pubmed PMC CrossRef
  27. Wu C, Zhao W, Zhang X, Chen X. 2015. Neocryptotanshinone inhibits lipopolysaccharide-induced inflammation in RAW264.7 macrophages by suppression of NF-kappa B and iNOS signaling pathways. Acta Pharm. Sin. B 5: 323-329.
    Pubmed PMC CrossRef
  28. Kim YJ, Kim ES, Lee JE, Park WY, Kwon JS, Park KS, et al. 2011. Is cervical cancer a risk factor for colorectal neoplasia? Prevalence of colorectal adenoma in Korean patients with cervical cancer. Hepatogastroenterology 58: 1177-1181.
    Pubmed CrossRef
  29. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN. 2005. LPS induces CD40 gene expression through the activation of NF-kappa B and STAT-1alpha in macrophages and microglia. Blood 106: 3114-3122.
    Pubmed PMC CrossRef
  30. Rhee SH, Jones BW, Toshchakov V, Vogel SN, Fenton MJ. 2003. Toll-like receptors 2 and 4 activate STAT1 serine phosphorylation by distinct mechanisms in macrophages. J. Biol. Chem. 278: 22506-22512.
    Pubmed CrossRef
  31. Hsu HY, Wen MH. 2002. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J. Biol. Chem. 277: 22131-22139.
    Pubmed CrossRef
  32. Luu K, Greenhill CJ, Majoros A, Decker T, Jenkins BJ, Mansell A. 2014. STAT1 plays a role in TLR signal transduction and inflammatory responses. Immunol. Cell Biol. 92: 761-769.
    Pubmed CrossRef
  33. Ohmori Y, Hamilton TA. 2001. Requirement for STAT1 in LPS-induced gene expression in macrophages. J. Leukoc. Biol. 69: 598-604.
    Pubmed
  34. Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y. 2006. Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl. Environ. Microbiol. 72: 6854-6858.
    Pubmed PMC CrossRef
  35. Karin M, Ben-Neriah Y. 2000. Phosphorylation meets ubiquitination: the control of NF-kappa B activity. Annu. Rev. Immunol 18: 621-663.
    Pubmed CrossRef
  36. Chien HY, Lu CS, Chuang KH, Kao PH, Wu YL. 2015. Attenuation of LPS-induced cyclooxygenase-2 and inducible NO synthase expression by lysophosphatidic acid in macrophages. Innate Immun. 21: 635-646.
    Pubmed CrossRef
  37. Youn GS, Lee KW, Choi SY, Park J. 2016. Overexpression of HDAC6 induces pro-inflammatory responses by regulating ROS-MAPK-NF-kappa B/AP-1 signaling pathways in macrophages. Free Radic. Biol. Med. 97: 14-23.
    Pubmed CrossRef
  38. Akira S, Takeda K. 2004. Toll-like receptor signaling. Nat. Rev. Immunol. 4: 499-511.
    Pubmed CrossRef
  39. Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, Kaisho T, et al. 2002. Essential role for TIRAP in activation of the signaling cascade shared by TLR2 and TLR4. Nature 420: 324-329.
    Pubmed CrossRef
  40. Kamezaki K, Shimoda K, Numata A, Matsuda T, Nakayama K, Harada M. 2004. The role o f Tyk2, S tat1 and S tat4 in LPSinduced endotoxin signals. Int. Immunol. 16: 1173-1179.
    Pubmed CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(2): 350-356

Published online February 28, 2017 https://doi.org/10.4014/jmb.1607.07065

Copyright © The Korean Society for Microbiology and Biotechnology.

An Analog of the Antimicrobial Peptide CopA5 Inhibits Lipopolysaccharide-Induced Macrophage Activation

I Na Yoon 1, Ji Hong 1, Peng Zhang 1, Jae Sam Hwang 2 and Ho Kim 1*

1Divison of Life Science and Chemistry, College of Natural Science, Daejin University, Pocheon 11159, Republic of Korea, 2Department of Agricultural Biology, National Academy of Agricultural Science, RDA, Wanju 55365, Republic of Korea

Received: July 28, 2016; Accepted: October 11, 2016

Abstract

We previously reported that the CopA3 peptide (LLCIALRKK, D-form) originally isolated
from the Korean dung beetle has antimicrobial and immunosuppressive effects. However, the
high cost of producing the synthetic peptide, especially the D-form, has limited the
development of CopA3 for therapeutic purposes. Here, we investigated whether the CopA3
deletion derivative, CopA5, which is composed of only five amino acids (LLCIA) and has the
L-form structure, could inhibit the lipopolysaccharide (LPS)-induced activation of
macrophages. Peritoneal exudate macrophages (PEM) were isolated from mice and exposed to
LPS in the presence or absence of CopA5, and biomarkers of macrophage activation were
measured. Our results revealed that LPS-induced nitric oxide (NO) production, tumor
necrosis factor (TNF)-α secretion, and phagocytic activity of PEM were significantly inhibited
by CopA5 treatment. Similar to CopA3, the structurally modified CopA5 peptide had no cell
toxicity (as assessed by measurement of cell viability loss and apoptosis) in PEM. Moreover,
the LPS-induced upregulation of the activating phosphorylation of signal transducer and
activator of transcription 1 (STAT1) was markedly inhibited by CopA5 treatment. These
results suggest that, similar to CopA3, CopA5 inhibits macrophage activation by inhibiting
STAT1 phosphorylation and blocking the release of NO and TNF-α. CopA5 may therefore
prove therapeutically useful in the realm of immune suppression.

Keywords: Antimicrobial peptide, lipopolysaccharide, macrophages, immunosuppressive agent, signal transduction, STAT1

References

  1. Pierce GF. 1990. Macrophages: important physiologic and pathologic sources of polypeptide growth factors. Am. J. Respir. Cell Mol. Biol. 2: 233-234.
    Pubmed CrossRef
  2. Jiang WY, Jeon BH, Kim YC, Lee SH, Sohn DH, Seo GS. 2013. PF2401-SF, standardized fraction of Salvia miltiorrhiza shows anti-inflammatory activity in macrophages and acute arthritis in vivo. Int. Immunopharmacol. 16: 160-164.
    Pubmed CrossRef
  3. Werner F, Jain MK, Feinberg MW, Sibinga NE, Pellacani A, Wiesel P, et al. 2000. Transforming growth factor-beta 1 inhibition of macrophage activation is mediated via Smad3. J. Biol. Chem. 275: 36653-36658.
    Pubmed CrossRef
  4. O’Farrell AM, Liu Y, Moore KW, Mui AL. 1998. IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: evidence for Stat3-dependent and -independent pathways. EMBO J. 17: 1006-1018.
    Pubmed KoreaMed CrossRef
  5. Sato K, Fujimoto K, Koyama T, Shichiri M. 2010. Release of salusin-beta from human monocytes/macrophages. Regul. Pept. 162: 68-72.
    Pubmed CrossRef
  6. Sun W, Tadmori I, Yang L, Delgado M, Ganea D. 2000. Vasoactive intestinal peptide (VIP) inhibits TGF-beta1 production in murine macrophages. J. Neuroimmunol. 107:88-99.
    CrossRef
  7. Yang LX, Liu H, Guo RW, Ye J, Wang XM, Qi F, et al. 2010. Angiotensin II induces EMMPRIN expression in THP-1 macrophages via the NF-kappa B pathway. Regul. Pept. 163:88-95.
    Pubmed CrossRef
  8. Suzuki E, Umezawa K. 2006. Inhibition of macrophage activation and phagocytosis by a novel NF-kappa B inhibitor, dehydroxymethylepoxyquinomicin. Biomed. Pharmacother. 60: 578-586.
    Pubmed CrossRef
  9. Kim JB, Han AR, Park EY, Kim JY, Cho W, Lee J, et al. 2007. Inhibition of LPS-induced iNOS, COX-2 and cytokines expression by poncirin through the NF-kappa B inactivation in RAW 264.7 macrophage cells. Biol. Pharm. Bull. 30: 23452351.
    CrossRef
  10. Konttinen YT, Ainola M, Valleala H, Ma J, Ida H, Mandelin J, et al. 1999. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann. Rheum. Dis. 58: 691-697.
    Pubmed KoreaMed CrossRef
  11. Cunnane G, FitzGerald O, Hummel KM, Youssef PP, Gay RE, Gay S, Bresnihan B. 2001. Synovial tissue protease gene expression and joint erosions in early rheumatoid arthritis. Arthritis Rheum. 44: 1744-1753.
    CrossRef
  12. Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, et al. 1997. Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum. 40: 217-225.
    Pubmed CrossRef
  13. Hansson GK. 2005. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 352: 1685-1695.
    Pubmed CrossRef
  14. Hansson GK, Libby P. 2006. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6:508-519.
    Pubmed CrossRef
  15. Tripathi S, Bruch D, Kittur DS. 2008. Ginger extract inhibits LPS induced macrophage activation and function. BMC Complement. Altern. Med. 8: 1.
    Pubmed KoreaMed CrossRef
  16. Hwang JS, Lee J, Kim YJ, Bang HS, Yun EY, Kim SR, et al. 2009. Isolation and characterization of a defensin-like peptide (coprisin) from the dung beetle, Copris tripartitus. Int. J. Pept. 2009: 136284.
    Pubmed KoreaMed CrossRef
  17. Nam HJ, Oh AR, Nam ST, Kang JK, Chang JS, Kim DH, et al. 2012. The insect peptide CopA3 inhibits lipopolysaccharideinduced macrophage activation. J. Pept. Sci. 18: 650-656.
    Pubmed CrossRef
  18. Kang JK, Hwang JS, Nam HJ, Ahn KJ, Seok H, Kim SK, et al. 2011. The insect peptide coprisin prevents Clostridium difficile-mediated acute inflammation and mucosal damage through selective antimicrobial activity. Antimicrob. Agents Chemother. 55: 4850-4857.
    Pubmed KoreaMed CrossRef
  19. Kim DH, Hwang JS, Lee IH, Nam ST, Hong J, Zhang P, et al. 2015. The insect peptide CopA3 increases colonic epithelial cell proliferation and mucosal barrier function to prevent inflammatory responses in the gut. J. Biol. Chem. 291: 32093223.
  20. Zhang F, Lau SS, Monks TJ. 2011. The cytoprotective effect of N-acetyl-L-cysteine against ROS-induced cytotoxicity is independent of its ability to enhance glutathione synthesis. Toxicol. Sci. 120: 87-97.
    Pubmed KoreaMed CrossRef
  21. Hung LC, Lin CC, Hung SK, Wu BC, Jan MD, Liou SH, Fu SL. 2007. A synthetic analog of alpha-galactosylceramide induces macrophage activation via the TLR4-signaling pathways. Biochem. Pharmacol. 73: 1957-1970.
    Pubmed CrossRef
  22. Onishi J, Roy MK, Juneja LR, Watanabe Y, Tamai Y. 2008. A lactoferrin-derived peptide with cationic residues concentrated in a region of its helical structure induces necrotic cell death in a leukemic cell line (HL-60). J. Pept. Sci. 14: 1032-1038.
    Pubmed CrossRef
  23. Yajima A, Narita N, Narita M. 2008. Recently identified a novel neuropeptide manserin colocalize with the TUNELpositive cells i n the top villi o f the r at d uodenum. J. Pept. Sci. 14: 773-776.
    Pubmed CrossRef
  24. Grunfeld C, Marshall M, Shigenaga JK, Moser AH, Tobias P, Feingold KR. 1999. Lipoproteins inhibit macrophage activation by lipoteichoic acid. J. Lipid Res. 40: 245-252.
    Pubmed
  25. Lee SH, Park DW, Park SC, Park YK, Hong SY, Kim JR, et al. 2009. Calcium-independent phospholipase A2beta-Akt signaling is involved in lipopolysaccharide-induced NADPH oxidase 1 expression and foam cell formation. J. Immunol. 183: 7497-7504.
    Pubmed CrossRef
  26. Kovarik P, Stoiber D, Novy M, Decker T. 1998. Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. EMBO J. 17: 3660-3668.
    Pubmed KoreaMed CrossRef
  27. Wu C, Zhao W, Zhang X, Chen X. 2015. Neocryptotanshinone inhibits lipopolysaccharide-induced inflammation in RAW264.7 macrophages by suppression of NF-kappa B and iNOS signaling pathways. Acta Pharm. Sin. B 5: 323-329.
    Pubmed KoreaMed CrossRef
  28. Kim YJ, Kim ES, Lee JE, Park WY, Kwon JS, Park KS, et al. 2011. Is cervical cancer a risk factor for colorectal neoplasia? Prevalence of colorectal adenoma in Korean patients with cervical cancer. Hepatogastroenterology 58: 1177-1181.
    Pubmed CrossRef
  29. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN. 2005. LPS induces CD40 gene expression through the activation of NF-kappa B and STAT-1alpha in macrophages and microglia. Blood 106: 3114-3122.
    Pubmed KoreaMed CrossRef
  30. Rhee SH, Jones BW, Toshchakov V, Vogel SN, Fenton MJ. 2003. Toll-like receptors 2 and 4 activate STAT1 serine phosphorylation by distinct mechanisms in macrophages. J. Biol. Chem. 278: 22506-22512.
    Pubmed CrossRef
  31. Hsu HY, Wen MH. 2002. Lipopolysaccharide-mediated reactive oxygen species and signal transduction in the regulation of interleukin-1 gene expression. J. Biol. Chem. 277: 22131-22139.
    Pubmed CrossRef
  32. Luu K, Greenhill CJ, Majoros A, Decker T, Jenkins BJ, Mansell A. 2014. STAT1 plays a role in TLR signal transduction and inflammatory responses. Immunol. Cell Biol. 92: 761-769.
    Pubmed CrossRef
  33. Ohmori Y, Hamilton TA. 2001. Requirement for STAT1 in LPS-induced gene expression in macrophages. J. Leukoc. Biol. 69: 598-604.
    Pubmed
  34. Kawasaki S, Mimura T, Satoh T, Takeda K, Niimura Y. 2006. Response of the microaerophilic Bifidobacterium species, B. boum and B. thermophilum, to oxygen. Appl. Environ. Microbiol. 72: 6854-6858.
    Pubmed KoreaMed CrossRef
  35. Karin M, Ben-Neriah Y. 2000. Phosphorylation meets ubiquitination: the control of NF-kappa B activity. Annu. Rev. Immunol 18: 621-663.
    Pubmed CrossRef
  36. Chien HY, Lu CS, Chuang KH, Kao PH, Wu YL. 2015. Attenuation of LPS-induced cyclooxygenase-2 and inducible NO synthase expression by lysophosphatidic acid in macrophages. Innate Immun. 21: 635-646.
    Pubmed CrossRef
  37. Youn GS, Lee KW, Choi SY, Park J. 2016. Overexpression of HDAC6 induces pro-inflammatory responses by regulating ROS-MAPK-NF-kappa B/AP-1 signaling pathways in macrophages. Free Radic. Biol. Med. 97: 14-23.
    Pubmed CrossRef
  38. Akira S, Takeda K. 2004. Toll-like receptor signaling. Nat. Rev. Immunol. 4: 499-511.
    Pubmed CrossRef
  39. Yamamoto M, Sato S, Hemmi H, Sanjo H, Uematsu S, Kaisho T, et al. 2002. Essential role for TIRAP in activation of the signaling cascade shared by TLR2 and TLR4. Nature 420: 324-329.
    Pubmed CrossRef
  40. Kamezaki K, Shimoda K, Numata A, Matsuda T, Nakayama K, Harada M. 2004. The role o f Tyk2, S tat1 and S tat4 in LPSinduced endotoxin signals. Int. Immunol. 16: 1173-1179.
    Pubmed CrossRef