Barrier protective effects of piperlonguminine in LPS-induced inflammation in vitro and in vivo

Food and Chemical Toxicology

Volumn 58, Issue , 2013, Pages 149-157

  Lee, Wonhwa ^a,b   Yoo, Hayoung ^a   Kim, Jeong Ah ^a   Lee, Sangkyu ^a   Jee, Jun Goo ^a   Lee, Min Young ^a   Lee, You Mie ^a   Bae, Jong Sup ^a,b  

^a Kyungpook National University   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

Author keywords

Barrier integrity; Endothelium; Inflammation; Lipopolysaccharide; Piperlonguminine

Indexed keywords

ANTIINFLAMMATORY AGENT; CELL ADHESION MOLECULE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; PIPERLONGUMININE; PLANT EXTRACT; RUTOSIDE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BARRIER PROTECTIVE EFFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG ISOLATION; DRUG PENETRATION; DRUG STRUCTURE; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE ACTIVATION; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; MALE; MONOCYTE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SEPSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULITIS;

BARRIER INTEGRITY; ENDOTHELIUM; INFLAMMATION; LIPOPOLYSACCHARIDE; PIPERLONGUMININE;

ANIMALS; CAPILLARY PERMEABILITY; CELLS, CULTURED; DIOXOLANES; ENDOTHELIUM, VASCULAR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INFLAMMATION; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84877792694     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2013.04.027     Document Type: Article

References (56)

1. Ajmone-Cat M.A., De Simone R., Nicolini A., Minghetti L. Effects of phosphatidylserine on p38 mitogen activated protein kinase, cyclic AMP responding element binding protein and nuclear factor-kappaB activation in resting and activated microglial cells. J. Neurochem. 2003, 84:413-416.
2. Akeson A.L., Woods C.W. A fluorometric assay for the quantitation of cell adherence to endothelial cells. J. Immunol. Methods 1993, 163:181-185.
3. Bae J.S. Role of high mobility group box 1 in inflammatory disease: focus on sepsis. Arch Pharm Res 2012, 35:1511-1523.
4. Bae J.W., Bae J.S. Barrier protective effects of lycopene in human endothelial cells. Inflamm. Res. 2011, 60:751-758.
5. Bae J.S., Rezaie A.R. Protease activated receptor 1 (PAR-1) activation by thrombin is protective in human pulmonary artery endothelial cells if endothelial protein C receptor is occupied by its natural ligand. Thromb. Haemost. 2008, 100:101-109.
6. Bae J.S., Rezaie A.R. Activated protein C inhibits high mobility group box 1 signaling in endothelial cells. Blood 2011, 118:3952-3959.
7. Bae J.S., Lee W., Rezaie A.R. Polyphosphate elicits proinflammatory responses that are counteracted by activated protein C in both cellular and animal models. J. Thromb. Haemost. 2012.
8. Berman R.S., Frew J.D., Martin W. Endotoxin-induced arterial endothelial barrier dysfunction assessed by an in vitro model. Br. J. Pharmacol. 1993, 110:1282-1284.
9. Beynon H.L., Haskard D.O., Davies K.A., Haroutunian R., Walport M.J. Combinations of low concentrations of cytokines and acute agonists synergize in increasing the permeability of endothelial monolayers. Clin. Exp. Immunol. 1993, 91:314-319.
10. Bhatia M., He M., Zhang H., Moochhala S. Sepsis as a model of SIRS. Front Biosci. 2009, 14:4703-4711.
11. Bierhaus A., Chen J., Liliensiek B., Nawroth P.P. LPS and cytokine-activated endothelium. Semin. Thromb. Hemost. 2000, 26:571-587.
12. Borbiev T., Verin A.D., Birukova A., Liu F., Crow M.T., Garcia J.G. Role of CaM kinase II and ERK activation in thrombin-induced endothelial cell barrier dysfunction. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 285:L43-L54.
13. Chatterjee A., Dutta C.P. Alkaloids of Piper longum Linn. I. Structure and synthesis of piperlongumine and piperlonguminine. Tetrahedron 1967, 23:1769-1781.
14. Che W., Lerner-Marmarosh N., Huang Q., Osawa M., Ohta S., Yoshizumi M., Glassman M., Lee J.D., Yan C., Berk B.C., Abe J. Insulin-like growth factor-1 enhances inflammatory responses in endothelial cells: role of Gab1 and MEKK3 in TNF-alpha-induced c-Jun and NF-kappaB activation and adhesion molecule expression. Circ. Res. 2002, 90:1222-1230.
15. Cohen J. The immunopathogenesis of sepsis. Nature 2002, 420:885-891.
16. Covert M.W., Leung T.H., Gaston J.E., Baltimore D. Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 2005, 309:1854-1857.
17. Desai S.J., Prabhu B.R., Mulchandani N.B. Aristolactams and 4,5-dioxoaporphines from Piper longum. Phytochemistry 1988, 27:1511-1515.
18. Dudek S.M., Garcia J.G. Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 2001, 91:1487-1500.
19. Frenette P.S., Wagner D.D. Adhesion molecules - Part 1. N. Engl. J. Med. 1996, 334:1526-1529.
20. Frenette P.S., Wagner D.D. Adhesion molecules - Part II: blood vessels and blood cells. N. Engl. J. Med. 1996, 335:43-45.
21. Frijns C.J., Kappelle L.J. Inflammatory cell adhesion molecules in ischemic cerebrovascular disease. Stroke 2002, 33:2115-2122.
22. Ghosh S., May M.J., Kopp E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 1998, 16:225-260.
23. Goldblum S.E., Ding X., Brann T.W., Campbell-Washington J. Bacterial lipopolysaccharide induces actin reorganization, intercellular gap formation, and endothelial barrier dysfunction in pulmonary vascular endothelial cells: concurrent F-actin depolymerization and new actin synthesis. J. Cell. Physiol. 1993, 157:13-23.
24. Guha M., Mackman N. LPS induction of gene expression in human monocytes. Cell. Signal. 2001, 13:85-94.
25. Hawiger J. Innate immunity and inflammation: a transcriptional paradigm. Immunol. Res. 2001, 23:99-109.
26. Huang H., Morgan C.M., Asolkar R.N., Koivunen M.E., Marrone P.G. Phytotoxicity of sarmentine isolated from long pepper (Piper longum) fruit. J. Agric. Food Chem. 2010, 58:9994-10000.
27. Javaid K., Rahman A., Anwar K.N., Frey R.S., Minshall R.D., Malik A.B. Tumor necrosis factor-alpha induces early-onset endothelial adhesivity by protein kinase Czeta-dependent activation of intercellular adhesion molecule-1. Circ. Res. 2003, 92:1089-1097.
28. Jeon K.I., Xu X., Aizawa T., Lim J.H., Jono H., Kwon D.S., Abe J., Berk B.C., Li J.D., Yan C. Vinpocetine inhibits NF-kappaB-dependent inflammation via an IKK-dependent but PDE-independent mechanism. Proc. Natl. Acad. Sci. USA 2010, 107:9795-9800.
29. Jin Z., Borjihan G., Zhao R., Sun Z., Hammond G.B., Uryu T. Antihyperlipidemic compounds from the fruit of Piper longum L. Phytother. Res. 2009, 23:1194-1196.
30. Kim T.H., Bae J.S. Ecklonia cava extracts inhibit lipopolysaccharide induced inflammatory responses in human endothelial cells. Food Chem. Toxicol. 2010, 48:1682-1687.
31. Kim I., Moon S.O., Kim S.H., Kim H.J., Koh Y.S., Koh G.Y. Vascular endothelial growth factor expression of intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), and E-selectin through nuclear factor-kappa B activation in endothelial cells. J. Biol. Chem. 2001, 276:7614-7620.
32. Kim K.S., Kim J.A., Eom S.Y., Lee S.H., Min K.R., Kim Y. Inhibitory effect of piperlonguminine on melanin production in melanoma B16 cell line by downregulation of tyrosinase expression. Pigment Cell Res. 2006, 19:90-98.
33. Kim T.H., Ku S.K., Bae J.S. Inhibitory effects of kaempferol-3-O-sophoroside on HMGB1-mediated proinflammatory responses. Food Chem. Toxicol. 2011, 50:1118-1123.
34. Komarova, Y.A., Mehta, D., Malik, A.B., 2007. Dual regulation of endothelial junctional permeability. Sci STKE 2007, re8.
35. Lee J.D., Huh J.E., Jeon G., Yang H.R., Woo H.S., Choi D.Y., Park D.S. Flavonol-rich RVHxR from Rhus verniciflua Stokes and its major compound fisetin inhibits inflammation-related cytokines and angiogenic factor in rheumatoid arthritic fibroblast-like synovial cells and in vivo models. Int. Immunopharmacol. 2009, 9:268-276.
36. Lee W., Ku S.K., Bae J.S. Barrier protective effects of rutin in LPS-induced inflammation in vitro and in vivo. Food Chem. Toxicol. 2012, 50:3048-3055.
37. Lin W.N., Luo S.F., Wu C.B., Lin C.C., Yang C.M. Lipopolysaccharide induces VCAM-1 expression and neutrophil adhesion to human tracheal smooth muscle cells: involvement of Src/EGFR/PI3-K/Akt pathway. Toxicol. Appl. Pharmacol. 2008, 228:256-268.
38. Lockyer J.M., Colladay J.S., Alperin-Lea W.L., Hammond T., Buda A.J. Inhibition of nuclear factor-kappaB-mediated adhesion molecule expression in human endothelial cells. Circ. Res. 1998, 82:314-320.
39. Manoj P., Soniya E.V., Banerjee N.S., Ravichandran P. Recent studies on well-known spice, Piper longum Linn. Nat. Prod. Radiance 2004, 3:222-227.
40. Marcus B.C., Wyble C.W., Hynes K.L., Gewertz B.L. Cytokine-induced increases in endothelial permeability occur after adhesion molecule expression. Surgery 1996, 120:411-416. discussion 416-417.
41. Marui N., Offermann M.K., Swerlick R., Kunsch C., Rosen C.A., Ahmad M., Alexander R.W., Medford R.M. Vascular cell adhesion molecule-1 (VCAM-1) gene transcription and expression are regulated through an antioxidant-sensitive mechanism in human vascular endothelial cells. J. Clin. Invest. 1993, 92:1866-1874.
42. Mittelstadt P.R., Salvador J.M., Fornace A.J., Ashwell J.D. Activating p38 MAPK: new tricks for an old kinase. Cell Cycle 2005, 4:1189-1192.
43. Osmond R.I., Sheehan A., Borowicz R., Barnett E., Harvey G., Turner C., Brown A., Crouch M.F., Dyer A.R. GPCR screening via ERK 1/2: a novel platform for screening G protein-coupled receptors. J. Biomol. Screen. 2005, 10:730-737.
44. Park B.S., Son D.J., Choi W.S., Takeoka G.R., Han S.O., Kim T.W., Lee S.E. Antiplatelet activities of newly synthesized derivatives of piperlongumine. Phytother. Res. 2008, 22:1195-1199.
45. Parmar V.S., Jain S.C., Bisht K.S., Jain R., Taneja P., Jha A., Tyagi O.D., Prasad A.K., Wengel J., Olsen C.E., Boll P.M. Phytochemistry of the genus Piper. Phytochemistry 1997, 46:597-673.
46. Rao G.V., Rao K.S., Mukhopadhyay T., Madhavi M.S.L. Alkamides and their biological activity from Piper longum Linn. J. Pharm. Res. 2012, 5:165-168.
47. Rose B.A., Force T., Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol. Rev. 2010, 90:1507-1546.
48. Ruiz-Torres M.P., Perez-Rivero G., Rodriguez-Puyol M., Rodriguez-Puyol D., Diez-Marques M.L. The leukocyte-endothelial cell interactions are modulated by extracellular matrix proteins. Cell. Physiol. Biochem. 2006, 17:221-232.
49. Sedgwick J.B., Menon I., Gern J.E., Busse W.W. Effects of inflammatory cytokines on the permeability of human lung microvascular endothelial cell monolayers and differential eosinophil transmigration. J. Allergy Clin. Immunol. 2002, 110:752-756.
50. Sluiter W., Pietersma A., Lamers J.M., Koster J.F. Leukocyte adhesion molecules on the vascular endothelium: their role in the pathogenesis of cardiovascular disease and the mechanisms underlying their expression. J. Cardiovasc. Pharmacol. 1993, 22(Suppl 4):S37-S44.
51. Ulbrich H., Eriksson E.E., Lindbom L. Leukocyte and endothelial cell adhesion molecules as targets for therapeutic interventions in inflammatory disease. Trends Pharmacol. Sci. 2003, 24:640-647.
52. Wadgaonkar R., Linz-McGillem L., Zaiman A.L., Garcia J.G. Endothelial cell myosin light chain kinase (MLCK) regulates TNFalpha-induced NFkappaB activity. J. Cell. Biochem. 2005, 94:351-364.
53. Walton K.L., Holt L., Sartor R.B. Lipopolysaccharide activates innate immune responses in murine intestinal myofibroblasts through multiple signaling pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296:G601-G611.
54. Wang X., Feuerstein G.Z., Gu J.L., Lysko P.G., Yue T.L. Interleukin-1 beta induces expression of adhesion molecules in human vascular smooth muscle cells and enhances adhesion of leukocytes to smooth muscle cells. Atherosclerosis 1995, 115:89-98.
55. Wung B.S., Ni C.W., Wang D.L. ICAM-1 induction by TNFalpha and IL-6 is mediated by distinct pathways via Rac in endothelial cells. J. Biomed. Sci. 2005, 12:91-101.
56. Yamagami H., Yamagami S., Inoki T., Amano S., Miyata K. The effects of proinflammatory cytokines on cytokine-chemokine gene expression profiles in the human corneal endothelium. Invest. Ophthalmol. Vis. Sci. 2003, 44:514-520.