Synthetic Peptides Containing ITIM-Like Domains Block Expression of Inflammatory Mediators and Migration/Invasion of Cancer Cells Through Activation of SHP-1 and PI3K

REFERENCES

• Alvarez-Errico D, Aguilar H, Kitzig F, Brckalo T, Sayos J, Lopez-Botet M. IREM-1 is a novel inhibitory receptor expressed by myeloid cells. Eur J Immunol 2004;34(12):3690–3701.
   PubMed Web of Science ®Google Scholar
• Chung DH, Humphrey MB, Nakamura MC, Ginzinger DG, Seaman WE, Daws MR. CMRF-35-like molecule-1, a novel mouse myeloid receptor, can inhibit osteoclast formation. J Immunol 2003;171(12):6541–6548.
   PubMed Web of Science ®Google Scholar
• Shibuya A, Nakahashi-Oda C, Tahara-Hanaoka S. Regulation of immune responses by the activating and inhibitory myeloid-associate immunoglobuline-like receptors (MAIR) (CD300). Immune Netw 2009;9(2):41–45.
   PubMedGoogle Scholar
• Sui L, Li N, Liu Q, Zhang W, Wan T, Wang B, Luo K, Sun H, Cao X. IgSF13, a novel human inhibitory receptor of the immunoglobulin superfamily, is preferentially expressed in dendritic cells and monocytes. Biochem Biophys Res Commun 2004;319(3):920–928.
   PubMed Web of Science ®Google Scholar
• Izawa K, Kitaura J, Yamanishi Y, Matsuoka T, Kaitani A, Sugiuchi M, Takahashi M, Maehara A, Enomoto Y, Oki T, Takai T, Kitamura T. An activating and inhibitory signal from an inhibitory receptor LMIR3/CLM-1: LMIR3 augments lipopolysaccharide response through association with FcRgamma in mast cells. J Immunol 2009;183(2):925–936.
   PubMed Web of Science ®Google Scholar
• Lee SM, Nam YP, Suk K, Lee WH. IREM-1 inhibits BAFF-mediated inflammatory regulation of THP-1 cells through modulation of the activities of ERK. Clin Exp Immunol 2010;161(3):504–511.
   PubMed Web of Science ®Google Scholar
• Xi H., Katschke KJ, Jr, Helmy KY, Wark PA, Kljavin N, Clark H, Eastham-Anderson J, Shek T, Roose-Girma M, Ghilardi N, van Lookeren Campagne M. Negative regulation of autoimmune demyelination by the inhibitory receptor CLM-1. J Exp Med 2010;207(1):7–16, S11–15.
   PubMed Web of Science ®Google Scholar
• Alvarez-Errico D, Sayos J, Lopez-Botet M. The IREM-1 (CD300f) inhibitory receptor associates with the p85alpha subunit of phosphoinositide 3-kinase. J Immunol 2007;178(2):808–816.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008;454(7203):436–444.
   PubMed Web of Science ®Google Scholar
• Philip M, Rowley DA, Schreiber H. Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 2004;14(6):433–439.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Schioppa T, Porta C, Allavena P, Sica A. Role of tumor-associated macrophages in tumor progression and invasion. Cancer Metast Rev 2006;25(3):315–322.
   PubMed Web of Science ®Google Scholar
• Sica A, Allavena P, Mantovani A. Cancer related inflammation: the macrophage connection. Cancer Lett 2008;267(2):204–215.
   PubMed Web of Science ®Google Scholar
• Clevers H. At the crossroads of inflammation and cancer. Cell 2004;118(6):671–674.
   PubMed Web of Science ®Google Scholar
• Lu H, Ouyang W, Huang C. Inflammation, a key event in cancer development. Mol Cancer Res 2006;4(4):221–233.
   PubMed Web of Science ®Google Scholar
• Lee SM, Kim EJ, Suk K, Lee WH. CD300F blocks both MyD88 and TRIF-mediated TLR signaling through activation of SHP-1. J Immunol 2011;186(11):6296–6303.
   PubMed Web of Science ®Google Scholar
• Lee SM, Kim EJ, Suk K, Lee WH. Stimulation of FasL induces production of pro-inflammatory mediators through activation of mitogen activated protein kinases and nuclear factor-kappaB in THP-1 cells. Inflammation 2012;35(1):1–10.
   PubMed Web of Science ®Google Scholar
• Vives E, Richard JP, Rispal C, Lebleu B. TAT peptide internalization: seeking the mechanism of entry. Curr Protein Pept Sci 2003;4(2):125–132.
   PubMed Web of Science ®Google Scholar
• Kim WJ, Lee WH. LIGHT is expressed in foam cells and involved in destabilization of atherosclerotic plaques through induction of matrix metalloproteinase-9 and IL-8. Immune Netw 2004;4(2):116–122.
   Google Scholar
• Lee WH, Kim SH, Lee Y, Lee BB, Kwon B, Song H, Kwon BS, Park JE. Tumor necrosis factor receptor superfamily 14 is involved in atherogenesis by inducing proinflammatory cytokines and matrix metalloproteinases. Arterioscler Thromb Vasc Biol 2001;21(12):2004–2010.
   PubMed Web of Science ®Google Scholar
• Lee SH, Kim EJ, Suk K, Kim IS, Lee WH. TL1A induces the expression of TGF-beta-inducible gene h3 (betaig-h3) through PKC, PI3K, and ERK in THP-1 cells. Cell Immunol 2010;266(1):61–66.
   PubMed Web of Science ®Google Scholar
• Rosenau C, Emery D, Kaboord B, Qoronfleh MW. Development of a high-throughput plate-based chemiluminescent transcription factor assay. J Biomol Screen 2004;9(4):334–342.
   PubMed Web of Science ®Google Scholar
• Arabaci G, Guo XC, Beebe KD, Coggeshall KM, Pei D. α-Haloacetophenone derivatives as photoreversible covalent inhibitors of protein tyrosine phosphatases. J Am Chem Soc 1999;121:5085–5086.
   Web of Science ®Google Scholar
• Lorenz U. SHP-1 and SHP-2 in T cells: two phosphatases functioning at many levels. Immunol Rev 2009;228(1):342–359.
   PubMedGoogle Scholar
• Fayard E, Xue G, Parcellier A, Bozulic L, Hemmings BA. Protein kinase B (PKB/Akt): a key mediator of the PI3K signaling pathway. Curr Top Microbiol Immunol 2010;346:31–56.
   PubMed Web of Science ®Google Scholar
• Carpenter CL, Auger KR, Chanudhuri M, Yoakim M, Schaffhausen B, Shoelson S, Cantley LC. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J Biol Chem 1993; 268(13):9478–9483.
   PubMed Web of Science ®Google Scholar
• Street A, Macdonald A, Crowder K, Harris M. The hepatitis C virus NS5A protein activates a phosphoinositide 3-kinase-dependent survival signaling cascade. J Biol Chem 2004;279(13):12232–12241.
   PubMed Web of Science ®Google Scholar
• Lee SM, Kim EJ, Suk K, Lee WH. Synthetic peptides containing ITIM-like sequences of IREM-1 inhibit BAFF-mediated regulation of interleukin-8 expression and phagocytosis through SHP-1 and/or PI3K. Immunology 2011;134(2):224–233.
   PubMed Web of Science ®Google Scholar
• Chong ZZ, Maiese K. The Src homology 2 domain tyrosine phosphatases SHP-1 and SHP-2: diversified control of cell growth, inflammation, and injury. Histol Histopathol 2007; 22(11):1251–1267.
   PubMed Web of Science ®Google Scholar
• Christophi GP, Hudson CA, Panos M, Gruber RC, Massa PT. Modulation of macrophage infiltration and inflammatory activity by the phosphatase SHP-1 in virus-induced demyelinating disease. J Virol 2009;83(2):522–539.
   PubMed Web of Science ®Google Scholar
• Christophi GP, Massa PT. Central neuroinvasion and demyelination by inflammatory macrophages after peripheral virus infection is controlled by SHP-1. Viral Immunol 2009;22(6):371–387.
   PubMed Web of Science ®Google Scholar
• Christophi GP, Panos M, Hudson CA, Christophi RL, Gruber RC, Mersich AT, Blystone SD, Jubelt B, Massa PT. Macrophages of multiple sclerosis patients display deficient SHP-1 expression and enhanced inflammatory phenotype. Lab Invest 2009;89(7):742–759.
   PubMed Web of Science ®Google Scholar
• Hardin AO, Meals EA, Yi T, Knapp KM, English BK. SHP-1 inhibits LPS-mediated TNF and iNOS production in murine macrophages. Biochem Bioph Res Commun 2006;342(2):547–555.
   PubMed Web of Science ®Google Scholar
• Guha M, Mackman N. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J Biol Chem 2002;277(35):32124–32132.
   PubMed Web of Science ®Google Scholar
• Strassheim D, Asehnoune K, Park JS, Kim JY, He Q, Richter D, Kuhn K, Mitra S, Abraham E. Phosphoinositide 3-kinase and Akt occupy central roles in inflammatory responses of Toll-like receptor 2-stimulated neutrophils. J Immunol 2004;172(9):5727–5733.
   PubMed Web of Science ®Google Scholar
• Diaz-Guerra MJ, Castrillo A, Martin-Sanz P, Bosca L. Negative regulation by phosphatidylinositol 3-kinase of inducible nitric oxide synthase expression in macrophages. J Immunol 1999;162(10):6184–6190.
   PubMed Web of Science ®Google Scholar
• Li X, Tupper JC, Bannerman DD, Winn RK, Rhodes CJ, Harlan JM. Phosphoinositide 3 kinase mediates Toll-like receptor 4-induced activation of NF-kappa B in endothelial cells. Infect Immun 2003;71(8):4414–4420.
   PubMed Web of Science ®Google Scholar
• Pahan K, Raymond JR, Singh I. Inhibition of phosphatidylinositol 3-kinase induces nitric-oxide synthase in lipopolysaccharide- or cytokine-stimulated C6 glial cells. J Biol Chem 1999;274(11):7528–7536.
   PubMed Web of Science ®Google Scholar
• Aksoy E, Vanden Berghe W, Detienne S, Amraoui Z, Fitzgerald KA, Haegeman G, Goldman M, Willems F. Inhibition of phosphoinositide 3-kinase enhances TRIF-dependent NF-kappa B activation and IFN-beta synthesis downstream of Toll-like receptor 3 and 4. Eur J Immunol 2005;35(7):2200–2209.
   PubMed Web of Science ®Google Scholar
• Bansal K, Kapoor N, Narayana Y, Puzo G, Gilleron M, Balaji KN. PIM2 induced COX-2 and MMP-9 expression in macrophages requires PI3K and Notch1 signaling. PloS One 2009;4(3): e4911.
   PubMed Web of Science ®Google Scholar
• Barber MA, Welch HC. PI3K and RAC signalling in leukocyte and cancer cell migration. Bull Cancer 2006;93(5):E44–E52.
   PubMedGoogle Scholar
• Dagia NM, Agarwal G, Kamath DV, Chetrapal-Kunwar A, Gupte RD, Jadhav MG, Dadarkar SS, Trivedi J, Kulkarni-Almeida AA, Kharas F, A preferential p110alpha/gamma PI3K inhibitor attenuates experimental inflammation by suppressing the production of proinflammatory mediators in a NF-kappaB-dependent manner. Am J Physiol 2010;298(4):C929–941.
   Web of Science ®Google Scholar
• Lee IT, Lee CW, Tung WH, Wang SW, Lin CC, Shu JC, Yang CM. Cooperation of TLR2 with MyD88, PI3K, and Rac1 in lipoteichoic acid-induced cPLA2/COX-2-dependent airway inflammatory responses. Am J Pathol 2010;176(4):1671–1684.
   PubMed Web of Science ®Google Scholar