Biological effect of licochalcone C on the regulation of PI3K/Akt/eNOS and NF-κB/iNOS/NO signaling pathways in H9c2 cells in response to LPS stimulation

International Journal of Molecular Sciences

Volumn 18, Issue 4, 2017, Pages

  Franceschelli, Sara ^a   Pesce, Mirko ^a   Ferrone, Alessio ^a   Gatta, Daniela Maria Pia ^a   Patruno, Antonia ^a   De Lutiis, Maria Anna ^a   Quiles, José Luis ^b   Grilli, Alfredo ^a   Felaco, Mario ^a   Speranza, Lorenza ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b UNIVERSITY OF GRANADA   (Spain)

Author keywords

Adhesion molecule; Akt; Cardiomyocytes; Inflammation; Licochalcone C; Nitric oxide; Nuclear factor B

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ANTIINFLAMMATORY AGENT; ENDOTHELIAL NITRIC OXIDE SYNTHASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; LICOCHALCONE C; LIPOPOLYSACCHARIDE; NITRITE; PHOSPHATIDYLINOSITOL 3 KINASE; PLANT MEDICINAL PRODUCT; PROTEIN KINASE B; PROTEIN TRANSLOCASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; CHALCONE DERIVATIVE; NITRIC OXIDE;

ANIMAL CELL; ARTICLE; CARDIAC MUSCLE CELL; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; GENE TRANSLOCATION; HEART DISEASE; HOMEOSTASIS; MTT ASSAY; NITROBLUE TETRAZOLIUM TEST; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; METABOLISM;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; CHALCONES; INTERCELLULAR ADHESION MOLECULE-1; LIPOPOLYSACCHARIDES; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION;

EID: 85016161063     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms18040690     Document Type: Article

References (47)

1. Perner, A.; Rhodes, A.; Venkatesh, B.; Angus, D.C.; Martin-Loeches, I.; Preiser, J.C.; Vincent, J.L.; Marshall, J.; Reinhart, K.; Joannidis, M.; et al. Sepsis: Frontiers in supportive care, organi-sation and research. Intensive Care Med. 2017, 43, 496–508. [PubMed]
2. Speranza, L.; Franceschelli, S.; Riccioni, G. The biological effects of ivabradine in cardiovascular disease. Molecules 2012, 17, 4924–4235. [PubMed]
3. Patruno, A.; Franceschelli, S.; Pesce, M.; Maccallini, C.; Fantacuzzi, M.; Speranza, L.; Ferrone, A.; de Lutiis, M.A.; Ricciotti, E.; Amoroso, R.; et al. Novel aminobenzyl-acetamidine deriva-tive modulate the differential regulation of NOSs in LPS induced inflammatory response: Role of PI3K/Akt pathway. Biochim. Biophys. Acta 2012, 1820, 2095–2104. [CrossRef] [PubMed]
4. Gao, M.; Wang, X.; Zhang, X.; Ha, T.; Ma, H.; Liu, L.; Kalbfleisch, J.H.; Gao, X.; Kao, R.L.; Wil-liams, D.L.; et al. Attenuation of Cardiac Dysfunction in polymicrobial sepsis by microRNA-146a is mediated via targeting of IRAK1 and TRAF6 expression. J. Immunol. 2015, 195, 672–682. [CrossRef] [PubMed]
5. Fenton, K.E.; Parker, M.M. Cardiac function and dysfunction in sepsis. Clin. Chest Med. 2016, 37, 289–298. [CrossRef] [PubMed]
6. Pesce, M.; Ferrone, A.; Rizzuto, A.; Tatangelo, R.; Iezzi, I.; Ladu, S.; Franceschelli, S.; Speranza, L.; Patruno, A.; Felaco, M.; et al. The SHP-1 expression is associated with cytokines and psy-chopathological status in unmedicated first episode schizophrenia patients. Brain Behav. Immun. 2014, 41, 251–260. [CrossRef] [PubMed]
7. Kim, Y.W.; Baek, S.H.; Lee, S.H.; Kim, T.H.; Kim, S.Y. Fucoidan, a sulfated polysaccharide, inhibits osteoclast differentiation and function by modulating RANKL signaling. Int. J. Mol. Sci. 2014, 15, 18840–18855. [CrossRef] [PubMed]
8. Zhang, H.; Qin, G.; Liang, G.; Li, J.; Chiu, I.; Barrington, R.A.; Liu, D. Suppression of complement regulatory protein C1 inhibitor in vascular endothelial activation by inhibiting vascular cell adhesion molecule-1 action. Biochem. Biophys. Res. Commun. 2007, 358, 1120–1127. [CrossRef] [PubMed]
9. Lv, X.; Wang, H. Pathophysiology of sepsis-induced myocardial dysfunction. Mil. Med. Res. 2016, 27. [CrossRef] [PubMed]
10. Cobb, J.P. Nitric oxide synthase inhibition as therapy for sepsis: A decade of promise. Surg. Infect. 2001, 2, 93–100. [CrossRef] [PubMed]
11. Prauchner, C.A. Oxidative stress in sepsis: Pathophysiological implications justifying antioxidant co-therapy. Burns 2016. [CrossRef] [PubMed]
12. Amalakuhan, B.; Habib, S.A.; Mangat, M.; Reyes, L.F.; Rodriguez, A.H.; Hinojosa, C.A.; Soni, N.J.; Gilley, R.P.; Bustamante, C.A.; Anzueto, A.; et al. Endothelial adhesion molecules and multiple organ failure in patients with severe sepsis. Cytokine 2016, 88, 267–273. [CrossRef] [PubMed]
13. Ha, T.; Hua, F.; Grant, D.; Xia, Y.; Ma, J.; Gao, X.; Kelley, J.; Williams, D.L.; Kalbfleisch, J.; Browder, I.W.; et al. Glucan phosphate attenuates cardiac dysfunction and inhibits car-diac MIF expression and apoptosis in septic mice. Am. J. Physiol. Heart Circ. Physiol. 2006, 291, H1910–H1918. [CrossRef]
14. You, W.; Min, X.; Zhang, X.; Qian, B.; Pang, S.; Ding, Z.; Li, C.; Gao, X.; Di, R.; Cheng, Y.; et al. Cardiac-specific expression of heat shock protein 27 attenuated endotoxin-induced cardiac dysfunction and mortality in mice through a PI3K/Akt-dependent mechanism. Shock 2009, 32, 108–117. [CrossRef] [PubMed]
15. Thomas, K.W.; Monick, M.M.; Stabler, J.M.; Yarovinsky, T.; Carter, A. B.; Hunninghake, G. W. Respiratory syncytial virus inhibits apoptosis and induces NF-κB activity through a phos-phatidylinositol 3-kinase-dependent pathway. J. Biol. Chem. 2002, 277, 492–501. [CrossRef] [PubMed]
16. Arbibe, L.; Mira, J.P.; Teusch, N.; Kline, L.; Guha, M.; Mackman, N.; Godowski, P.J.; Ulevitch, R.J.; Knaus, U.G. Toll-like receptor 2-mediated NF-κB activation requires a Rac1-dependent pathway. Nat. Immunol. 2000, 1, 533–540. [CrossRef] [PubMed]
17. Madrid, L.V.; Mayo, M.W.; Reuther, J.Y.; Baldwin, A.S., Jr. Akt stimulates the transactivation potential of the RelA/p65 Subunit of NF-κB through utilization of the IκB kinase and activation of the mitogen-activated protein kinase p38. J. Biol. Chem. 2001, 276, 18934–18940. [CrossRef] [PubMed]
18. Pahan, K.; Raymond, J.R.; Singh, I. Inhibition of phosphatidylinositol 3-kinase induces nitric-oxide synthase in lipopolysaccharide- or cytokine-stimulated C6 glial cells. J. Biol. Chem. 1999, 274, 7528–7536. [CrossRef] [PubMed]
19. Speranza, L.; Franceschelli, S.; Pesce, M.; Menghini, L.; Patruno, A.; Vinciguerra, I.; de Lutiis, M.A.; Felaco, M.; Felaco, P.; Grilli, A. Anti-inflammatory properties of the plant Verbascum mallophorum. J. Biol. Regul. Homeost. Agents 2009, 23, 189–195. [PubMed]
20. Salvamani, S.; Gunasekaran, B.; Shaharuddin, N.A.; Ahmad, S.A.; Shukor, M.Y. Antiartherosclerotic effects of plant flavonoids. BioMed Res. Int. 2014, 2014. [CrossRef] [PubMed]
21. Khurana, S.; Venkataraman, K.; Hollingsworth, A.; Piche, M.; Tai, T.C. Polyphenols: Benefits to the cardiovascular system in health and in aging. Nutrients 2013, 5, 3779–3827. [PubMed]
22. Song, N.R.; Kim, J.E.; Park, J.S.; Kim, J.R.; Kang, H.; Lee, E.; Kang, Y.G.; Son, J.E.; Seo, S.G.; Heo, Y.S.; et al. Licochalcone A, a polyphenol present in licorice, suppresses UV-induced COX-2 expression by targeting PI3K, MEK1, and B-Raf. Int. J. Mol. Sci. 2015, 16, 4453–4470. [CrossRef] [PubMed]
23. Katsori, A.M.; Hadjipavlou-Litina, D. Recent progress in therapeutic applications of chalcones. Expert Opin. Ther. Pat. 2011, 21, 1575–1596. [CrossRef] [PubMed]
24. Franceschelli, S.; Pesce, M.; Vinciguerra, I.; Ferrone, A.; Riccioni, G.; Patruno, A.; Grilli, A.; Felaco, M.; Speranza, L. Licocalchone-C extracted from Glycyrrhiza glabra inhibits lipopolysaccharide-interferon-γ inflammation by improving antioxidant conditions and regulating inducible nitric oxide synthase expression. Molecules 2011, 16, 5720–5734. [CrossRef] [PubMed]
25. Zhou, M.; Liu, L.; Wang, W.; Han, J.; Ren, H.; Zheng, Q.; Wang, D. Role of Licochalcone C in cardioprotection against ischemia/reperfusion injury of isolated rat heart via antioxidant, anti-inflammatory, and anti-apoptotic activities. Life Sci. 2015, 132, 27–33. [CrossRef] [PubMed]
26. Egom, E.E.; Mohamed, T.M.; Mamas, M.A.; Shi, Y.; Liu, W.; Chirico, D.; Stringer, S.E.; Ke, Y.; Shaheen, M.; Wang, T.; et al. Activation of Pak1/Akt/eNOS signaling following sphingosine-1-phosphate release as part of a mechanism protecting cardiomyocytes against ischemic cell injury. Am. J. Physiol. Heart Circ. Physiol. 2011, 301, H1487–H1495. [CrossRef] [PubMed]
27. Frazier, W.J.; Xue, J.; Luce, W.A.; Liu, Y. MAPK signaling drives inflammation in LPS-stimulated cardiomyocytes: The route of crosstalk to G-protein-coupled receptors. PLoS ONE 2012, 7. [CrossRef] [PubMed]
28. Franceschelli, S.; Ferrone, A.; Pesce, M.; Riccioni, G.; Speranza, L. Biological functional relevance of asymmetric dimethylarginine (ADMA) in cardiovascular disease. Int. J. Mol. Sci. 2013, 14, 24412–24421. [CrossRef] [PubMed]
29. − production. PLoS ONE 2014, 9. [CrossRef] [PubMed]
30. Lin, C.Y.; Lee, C.H.; Chang, Y.W.; Wang, H.M.; Chen, C.Y.; Chen, Y.H. Pheophytin a inhibits inflammation via suppression of LPS-induced nitric oxide synthase-2, prostaglandin E2, and inter-leukin-1β of macrophages. Int. J. Mol. Sci. 2014, 15, 22819–22834. [CrossRef] [PubMed]
31. Franceschelli, S.; Pesce, M.; Ferrone, A.; Patruno, A.; Pasqualone, L.; Carlucci, G.; Ferrone, V.; Carlucci, M.; de Lutiis, M.A.; Grilli, A.; et al. A novel biological role of α-mangostin in modulating inflammatory response through the activation of SIRT-1 signaling pathway. J. Cell. Physiol. 2016, 231, 2439–2451. [CrossRef] [PubMed]
32. Speranza, L.; Franceschelli, S.; Pesce, M.; Reale, M.; Menghini, L.; Vinciguerra, I.; de Lutiis, M.A.; Felaco, M.; Grilli, A. Antiinflammatory effects in THP-1 cells treated with verbascoside. Phytother. Res. 2010, 24, 1398–1404. [CrossRef] [PubMed]
33. Wang, S.G.; Xu, Y.; Xie, H.; Wang, W.; Chen, X.H. Astragaloside IV prevents lipopolysaccha-ride-induced injury in H9C2 cardiomyocytes. Chin. J. Nat. Med. 2015, 13, 127–132. [PubMed]
34. Ha, T.; Hu, Y.; Liu, L.; Lu, C.; McMullen, J.R.; Kelley, J.; Kao, R.L.; Williams, D.L.; Gao, X.; Li, C. TLR2 ligands induce cardioprotection against ischaemia/reperfusion injury through a PI3K/Akt-dependent mechanism. Cardiovasc. Res. 2010, 87, 694–703. [CrossRef] [PubMed]
35. Zhang, W.J.; Wei, H.; Hagen, T.; Frei, B. α-lipoic acid attenuates LPS-induced inflammatory responses by activating the phosphoinositide 3-kinase/Akt signaling pathway. Proc. Natl. Acad. Sci. USA 2007, 104, 4077–4082. [CrossRef] [PubMed]
36. Patruno, A.; Pesce, M.; Grilli, A.; Speranza, L.; Franceschelli, S.; de Lutiis, M.A.; Vianale, G.; Costantini, E.; Amerio, P.; Muraro, R.; et al. mTOR Activation by PI3K/Akt and ERK Signaling in Short ELF-EMF Exposed Human Keratinocytes. PLoS ONE 2015, 10. [CrossRef] [PubMed]
37. Li, Q.; Shen, L.; Wang, Z.; Jiang, H.P.; Liu, L.X. Tanshinone IIA protects against myocardial ischemia reperfusion injury by activating the PI3K/Akt/mTOR signaling pathway. Biomed. Pharmacother. 2016, 84, 106–114. [CrossRef] [PubMed]
38. Wu, Y.; Xia, Z.Y.; Meng, Q.T.; Zhu, J.; Lei, S.; Xu, J.; Dou, J. Shen-Fu injection preconditioning inhibits myocardial ischemia-reperfusion injury in diabetic rats: Activation of eNOS via the PI3K/Akt pathway. J. Biomed. Biotechnol. 2010, 2011. [CrossRef] [PubMed]
39. Ni, L.; Li, T.; Liu, B.; Song, X.; Yang, G.; Wang, L.; Miao, S.; Liu, C. The Protective Effect of Bcl-xl Overexpression against Oxidative Stress-Induced Vascular Endothelial Cell Injury and the Role of the Akt/eNOS Pathway. Int. J. Mol. Sci. 2013, 14, 22149–22162. [CrossRef] [PubMed]
40. Hoesel, B.; Schmid, J.A. The complexity of NF-κB signaling in inflammation and cancer. Mol. Cancer 2013, 2. [CrossRef] [PubMed]
41. Jaakkola, K.; Jalkanen, S.; Kaunismäki, K.; Vänttinen, E.; Saukko, P.; Alanen, K.; Kallajoki, M.; Voipio-Pulkki, L.M.; Salmi, M. Vascular adhesion protein-1, intercellular adhesion molecule-1 and P-selectin mediate leukocyte binding to ischemic heart in humans. J. Am. Coll. Cardiol. 2000, 36, 122–129. [CrossRef]
42. Franceschelli, S.; Gatta, D.M.; Pesce, M.; Ferrone, A.; Patruno, A.; de Lutiis, M.A.; Grilli, A.; Felaco, M.; Croce, F.; Speranza, L. New approach in translational medicine: Effects of electro-lyzed reduced water (ERW) on NF-κB/iNOS pathway in U937 cell line under altered redox state. Int. J. Mol. Sci. 2016, 17. [CrossRef] [PubMed]
43. Patruno, A.; Fornasari, E.; di Stefano, A.; Cerasa, L.S.; Marinelli, L.; Baldassarre, L.; Sozio, P.; Turkez, H.; Franceschelli, S.; Ferrone, A.; et al. Synthesis of a novel cyclic prodrug of S-allyl-glutathione able to attenuate LPS-induced ROS production through the inhibition of MAPK pathways in U937 cells. Mol. Pharm. 2015, 12, 66–74. [CrossRef] [PubMed]
44. Speranza, L.; Pesce, M.; Franceschelli, S.; Bucciarelli, T.; Gallina, S.; Riccioni, G.; Patruno, A.; Felaco, M. The biological evaluation of ADMA/SDMA and eNOS in patients with ACHF. Front. Biosci. 2013, 5, 551–557. [CrossRef]
45. Conti, P.; Reale, M.; Barbacane, R.C.; Felaco, M.; Grilli, A.; Theoharides, T.C. Mast cell recruitment after subcutaneous injection of RANTES in the sole of the rat paw. Br. J. Haematol. 1998, 103, 798–803. [CrossRef]
46. Speranza, L.; Franceschelli, S.; Pesce, M.; Vinciguerra, I.; de Lutiis, M.A.; Grilli, A.; Felaco, M.; Patruno, A. Phosphodiesterase type-5 inhibitor and oxidative stress. Int. J. Immunopathol. Pharmacol. 2008, 21, 879–889. [CrossRef]
47. Hevel, J.M.; Marletta, M.A. Nitric oxide synthase assays. Methods Enzymol. 1994, 233, 250–258. [PubMed]