PKC -IRAK1 axis regulates oxidized LDL-induced IL-1 production in monocytes

Journal of Lipid Research

Volumn 55, Issue 7, 2014, Pages 1226-1244

  Tiwari, Rajiv Lochan ^a   Singh, Vishal ^a   Singh, Ankita ^a   Rana, Minakshi ^a   Verma, Anupam ^b   Kothari, Nikhil ^c   Kohli, Monica ^c   Bogra, Jaishri ^d   Dikshit, Madhu ^a   Barthwal, Manoj Kumar ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

^b SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

^c Department of Anaesthesia ^*  (India)

^d KING GEORGE'S MEDICAL UNIVERSITY   (India)

Author keywords

Infl ammation; Interleukin 1 receptor associated kinase; Oxidized low density lipoprotein; Protein kinase C 8

Indexed keywords

CD36 ANTIGEN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; JANUS KINASE 1; MESSENGER RNA; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN KINASE C DELTA; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TRANSCRIPTION FACTOR AP 1; 12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; ACETOPHENONE DERIVATIVE; ACETYLCYSTEINE; BENZOFURAN DERIVATIVE; BENZOPYRAN DERIVATIVE; CARBAZOLE DERIVATIVE; CATION; DIPHENYLIODONIUM SALT; IL1B PROTEIN, HUMAN; INDOLE DERIVATIVE; IRAK1 PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN; PRKCD PROTEIN, HUMAN; REACTIVE OXYGEN METABOLITE; RO 31-8220; ROTTLERIN; TASHINONE IIA; TOLL LIKE RECEPTOR;

ADULT; ARTICLE; BLOOD LEVEL; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; MALE; MOLECULAR PATHOLOGY; MONOCYTE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCORING SYSTEM; SIGNAL TRANSDUCTION; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; AGONISTS; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; THP-1 CELL LINE;

ACETOPHENONES; ACETYLCYSTEINE; ADULT; BENZOFURANS; BENZOPYRANS; CARBAZOLES; FEMALE; HUMANS; INDOLES; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-1BETA; LIPOPROTEINS, LDL; MALE; MIDDLE AGED; MONOCYTES; ONIUM COMPOUNDS; PROTEIN KINASE C-DELTA; REACTIVE OXYGEN SPECIES; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; THP-1 CELLS; TOLL-LIKE RECEPTORS;

EID: 84904004538     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M045658     Document Type: Article

References (60)

1. Tsimikas, S., E. S. Brilakis, E. R. Miller, J. P. McConnell, R. J. Lennon, K. S. Kornman, J. L. Witztum, and P. B. Berger. 2005. Oxidized phospholipids, Lp(a) lipoprotein, and coronary artery disease. N. Engl. J. Med. 353: 46-57.
2. Tsimikas, S., and Y. I. Miller. 2011. Oxidative modifi cation of lipoproteins: mechanisms, role in infl ammation and potential clinical applications in cardiovascular disease. Curr. Pharm. Des. 17: 27-37.
3. Chávez-Sánchez, L., K. Chávez-Rueda, M. V. Legorreta-Haquet, E. Zenteno, Y. Ledesma-Soto, E. Montoya-Díaz, E. Tesoro-Cruz, A. Madrid-Miller, and F. Blanco-Favela. 2010. The activation of CD14, TLR4, and TLR2 by mmLDL induces IL-1beta, IL-6, and IL-10 secretion in human monocytes and macrophages. Lipids Health Dis. 9: 117.
4. Pasini, A. F., M. Anselmi, U. Garbin, E. Franchi, C. Stranieri, M. C. Nava, V. Boccioletti, C. Vassanelli, and L. Cominacini. 2007. Enhanced levels of oxidized low-density lipoprotein prime monocytes to cytokine overproduction via upregulation of CD14 and tolllike receptor 4 in unstable angina. Arterioscler. Thromb. Vasc. Biol. 27: 1991-1997.
5. Norris, A. L., J. Steinberger, L. M. Steffen, A. M. Metzig, S. J. Schwarzenberg, and A. S. Kelly. 2011. Circulating oxidized LDL and infl ammation in extreme pediatric obesity. Obesity (Silver Spring). 19: 1415-1419.
6. Stewart, C. R., L. M. Stuart, K. Wilkinson, J. M. van Gils, J. Deng, A. Halle, K. J. Rayner, L. Boyer, R. Zhong, W. A. Frazier, et al. 2010. CD36 ligands promote sterile infl ammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11: 155-161.
7. Jiang, Y., M. Wang, K. Huang, Z. Zhang, N. Shao, Y. Zhang, W. Wang, and S. Wang. 2012. Oxidized low-density lipoprotein induces secretion of interleukin-1-by macrophages via reactive oxygen species-dependent NLRP3 infl ammasome activation. Biochem. Biophys. Res. Commun. 425: 121-126.
8. Chen, G. Y., and G. Nunez. 2010. Sterile infl ammation: sensing and reacting to damage. Nat. Rev. Immunol. 10: 826-837.
9. Hoque, R., A. F. Malik, F. Gorelick, and W. Z. Mehal. 2012. Sterile infl ammatory response in acute pancreatitis. Pancreas. 41: 353-357.
10. Rider, P., Y. Carmi, O. Guttman, A. Braiman, I. Cohen, E. Voronov, M. R. White, C. A. Dinarello, and R. N. Apte. 2011. IL-1-and IL-1-recruit different myeloid cells and promote different stages of sterile infl ammation. J. Immunol. 187: 4835-4843.
11. Yamasaki, K., J. Muto, K. R. Taylor, A. L. Cogen, D. Audish, J. Bertin, E. P. Grant, A. J. Coyle, A. Misaghi, H. M. Hoffman, et al. 2009. NLRP3/cryopyrin is necessary for interleukin-1beta (IL-1beta) release in response to hyaluronan, an endogenous trigger of infl ammation in response to injury. J. Biol. Chem. 284: 12762-12771.
12. Manson, J., C. Thiemermann, and K. Brohi. 2012. Trauma alarmins as activators of damage-induced infl ammation. Br. J. Surg. 99 ( Suppl 1 ): 12-20.
13. Medzhitov, R. 2008. Origin and physiological roles of infl ammation. Nature. 454: 428-435.
14. Hei, Z., X. Chi, N. Cheng, G. Luo, and S. Li. 2010. Upregulation of TLR2/4 expression in mononuclear cells in postoperative systemic infl ammatory response syndrome after liver transplantation. Mediators Infl amm. 2010: 519-589.
15. Poole, J. A., T. A. Wyatt, S. G. Von Essen, J. Hervert, C. Parks, T. Mathisen, and D. J. Romberger. 2007. Repeat organic dust exposure-induced monocyte infl ammation is associated with protein kinase C activity. J. Allergy Clin. Immunol. 120: 366-373.
16. Steinberg, S. F. 2004. Distinctive activation mechanisms and functions for protein kinase Cdelta. Biochem. J. 384: 449-459.
17. Tiwari, R. L., V. Singh, A. Singh, and M. K. Barthwal. 2011. IL-1Rassociated kinase-1 mediates protein kinase C-induced IL-1-production in monocytes. J. Immunol. 187: 2632-2645.
18. Kontny, E., M. Kurowska, K. Szczepanska, and W. Maslinski. 2000. Rottlerin, a PKC isozyme-selective inhibitor, affects signaling events and cytokine production in human monocytes. J. Leukoc. Biol. 67: 249-258.
19. Kilpatrick, L. E., S. W. Standage, H. Li, N. R. Raj, H. M. Korchak, M. R. Wolfson, and C. S. Deutschman. 2011. Protection against sepsisinduced lung injury by selective inhibition of protein kinase C-(-PKC). J. Leukoc. Biol. 89: 3-10.
20. Lee, M. C., S. C. Wei, J. J. Tsai-Wu, C. H. Wu, and P. N. Tsao. 2008. Novel PKC signaling is required for LPS-induced soluble Flt-1 expression in macrophages. J. Leukoc. Biol. 84: 835-841.
21. Dasu, M. R., S. Devaraj, L. Zhao, D. H. Hwang, and I. Jialal. 2008. High glucose induces toll-like receptor expression in human monocytes: mechanism of activation. Diabetes. 57: 3090-3098.
22. Shukla, A., K. M. Lounsbury, T. F. Barrett, J. Gell, M. Rincon, K. J. Butnor, D. J. Taatjes, G. S. Davis, P. Vacek, K. I. Nakayama, et al. 2007. Asbestos-induced peribronchiolar cell proliferation and cytokine production are attenuated in lungs of protein kinase C-delta knockout mice. Am. J. Pathol. 170: 140-151.
23. Kobayashi, K., L. D. Hernandez, J. E. Galan, C. A. Janeway, Jr., R. Medzhitov, and R. A. Flavell. 2002. IRAK-M is a negative regulator of Toll-like receptor signaling. Cell. 110: 191-202.
24. Suzuki, N., S. Suzuki, G. S. Duncan, D. G. Millar, T. Wada, C. Mirtsos, H. Takada, A. Wakeham, A. Itie, S. Li, et al. 2002. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature. 416: 750-756.
25. Janssens, S., and R. Beyaert. 2003. Functional diversity and regulation of different interleukin-1 receptor-associated kinase (IRAK) family members. Mol. Cell. 11: 293-302.
26. Ho, K. M. 2007. Combining sequential organ failure assessment (SOFA) score with acute physiology and chronic health evaluation (APACHE) II score to predict hospital mortality of critically ill patients. Anaesth. Intensive Care. 35: 515-521.
27. Kothari, N., R. S. Keshari, J. Bogra, M. Kohli, H. Abbas, A. Malik, M. Dikshit, and M. K. Barthwal. 2011. Increased myeloperoxidase enzyme activity in plasma is an indicator of infl ammation and onset of sepsis. J. Crit. Care. 26: 435. e1-435. e7.
28. Behnes, M., M. Brueckmann, V. Liebe, C. Liebetrau, S. Lang, C. Putensen, M. Borggrefe, and U. Hoffmann. 2008. Levels of oxidized low-density lipoproteins are increased in patients with severe sepsis. J. Crit. Care. 23: 537-541.
29. Repnik, U., M. Knezevic, and M. Jeras. 2003. Simple and cost-effective isolation of monocytes from buffy coats. J. Immunol. Methods. 278: 283-292.
30. Chen, K., W. Li, J. Major, S. O. Rahaman, M. Febbraio, and R. L. Silverstein. 2011. Vav guanine nucleotide exchange factors link hyperlipidemia and a prothrombotic state. Blood. 117: 5744-5750.
31. Schumaker, V. N., and D. L. Puppione. 1986. Sequential fl otation ultracentrifugation. Methods Enzymol. 128: 155-170.
32. Han, C. Y., and Y. K. Pak. 1999. Oxidation-dependent effects of oxidized LDL: proliferation or cell death. Exp. Mol. Med. 31: 165-173.
33. Chen, C. H., W. Jiang, D. P. Via, S. Luo, T. R. Li, Y. T. Lee, and P. D. Henry. 2000. Oxidized low-density lipoproteins inhibit endothelial cell proliferation by suppressing basic fi broblast growth factor expression. Circulation. 101: 171-177.
34. Garcia-Calvo, M., E. P. Peterson, B. Leiting, R. Ruel, D. W. Nicholson, and N. A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273: 32608-32613.
35. Walker, R. J., and J. J. Steinle. 2007. Role of beta-adrenergic receptors in infl ammatory marker expression in M̈ller cells. Invest. Ophthalmol. Vis. Sci. 48: 5276-5281.
36. Shanmugam, N., M. A. Reddy, M. Guha, and R. Natarajan. 2003. High glucose-induced expression of proinfl ammatory cytokine and chemokine genes in monocytic cells. Diabetes. 52: 1256-1264.
37. Wong, M. L., and J. F. Medrano. 2005. Real-time PCR for mRNA quantitation. Biotechniques. 39: 75-85.
38. Namgaladze, D., A. Kollas, and B. Brune. 2008. Oxidized LDL attenuates apoptosis in monocytic cells by activating ERK signaling. J. Lipid Res. 49: 58-65.
39. Flannery, S., and A. G. Bowie. 2010. The interleukin-1 receptorassociated kinases: critical regulators of innate immune signalling. Biochem. Pharmacol. 80: 1981-1991.
40. Li, X., M. Commane, Z. Jiang, and G. R. Stark. 2001. IL-1-induced NFkappa B and c-Jun N-terminal kinase (JNK) activation diverge at IL-1 receptor-associated kinase (IRAK). Proc. Natl. Acad. Sci. USA. 98: 4461-4465.
41. Vicca, S., Z. A. Massy, C. Hennequin, D. Rihane, T. B. Drueke, and B. Lacour. 2003. Apoptotic pathways involved in U937 cells exposed to LDL oxidized by hypochlorous acid. Free Radic. Biol. Med. 35: 603-615.
42. Reid, V. C., S. J. Hardwick, and M. J. Mitchinson. 1993. Fragmentation of DNA in P388D1 macrophages exposed to oxidised low-density lipoprotein. FEBS Lett. 332: 218-220.
43. Nguyen, H. A., M. V. Rajaram, D. A. Meyer, and L. S. Schlesinger. 2012. Pulmonary surfactant protein A and surfactant lipids upregulate IRAK-M, a negative regulator of TLR-mediated infl ammation in human macrophages. Am. J. Physiol. Lung Cell. Mol. Physiol. 303: L608-L616.
44. Netea, M. G., F. L. van de Veerdonk, B. J. Kullberg, J. W. Van der Meer, and L. A. Joosten. 2008. The role of NLRs and TLRs in the activation of the infl ammasome. Expert Opin. Biol. Ther. 8: 1867-1872.
45. Duewell, P., H. Kono, K. J. Rayner, C. M. Sirois, G. Vladimer, F. G. Bauernfeind, G. S. Abela, L. Franchi, G. Nunez, M. Schnurr, et al. 2010. NLRP3 infl ammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 464: 1357-1361.
46. Liu, W., Y. Yin, Z. Zhou, M. He, and Y. Dai. 2014. OxLDL-induced IL-1beta secretion promoting foam cells formation was mainly viaCD36 mediated ROS production leading to NLRP3 infl ammasome activation. Infl amm. Res. 63: 33-43.
47. Serkkola, E., and M. Hurme. 1993. Synergism between proteinkinase C and cAMP-dependent pathways in the expression of the interleukin-1 beta gene is mediated via the activator-protein-1 (AP-1) enhancer activity. Eur. J. Biochem. 213: 243-249.
48. Rosenzweig, T., S. Aga-Mizrachi, A. Bak, and S. R. Sampson. 2004. Src tyrosine kinase regulates insulin-induced activation of protein kinase C (PKC) delta in skeletal muscle. Cell. Signal. 16: 1299-1308.
49. Xue, Z. H., C. Q. Zhao, G. L. Chua, S. W. Tan, X. Y. Tang, S. C. Wong, and S. M. Tan. 2010. Integrin alphaMbeta2 clustering triggers phosphorylation and activation of protein kinase C delta that regulates transcription factor Foxp1 expression in monocytes. J. Immunol. 184: 3697-3709.
50. Rahaman, S. O., D. J. Lennon, M. Febbraio, E. A. Podrez, S. L. Hazen, and R. L. Silverstein. 2006. A CD36-dependent signaling cascade is necessary for macrophage foam cell formation. Cell Metab. 4: 211-221.
51. Loegering, D. J., and M. R. Lennartz. 2011. Protein kinase C and toll-like receptor signaling. Enzyme Res. 2011: 537821.
52. Platten, M., K. Eitel, J. Wischhusen, J. Dichgans, and M. Weller. 2003. Involvement of protein kinase Cdelta and extracellular signal-regulated kinase-2 in the suppression of microglial inducible nitric oxide synthase expression by N-[3,4-dimethoxycinnamoyl]-anthranilic acid (tranilast). Biochem. Pharmacol. 66: 1263-1270.
53. Lin, C. S., F. Y. Lin, L. J. Ho, C. S. Tsai, S. M. Cheng, W. L. Wu, C. Y. Huang, C. H. Lian, S. P. Yang, and J. H. Lai. 2012. PKC-signalling regulates SR-A and CD36 expression and foam cell formation. Cardiovasc. Res. 95: 346-355.
54. Triantafi lou, M., F. G. Gamper, R. M. Haston, M. A. Mouratis, S. Morath, T. Hartung, and K. Triantafi lou. 2006. Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281: 31002-31011.
55. Xu, X. H., P. K. Shah, E. Faure, O. Equils, L. Thomas, M. C. Fishbein, D. Luthringer, X. P. Xu, T. B. Rajavashisth, J. Yano, et al. 2001. Toll-like receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circulation. 104: 3103-3108.
56. Bhaskar, S., V. Shalini, and A. Helen. 2011. Quercetin regulates oxidized LDL induced infl ammatory changes in human PBMCs by modulating the TLR-NF-B signaling pathway. Immunobiology. 216: 367-373.
57. Puente Navazo, M. D., L. Daviet, E. Ninio, and J. L. McGregor. 1996. Identifi cation on human CD36 of a domain (155-183) implicated in binding oxidized low-density lipoproteins (Ox-LDL). Arterioscler. Thromb. Vasc. Biol. 16: 1033-1039.
58. Janabi, M., S. Yamashita, K. Hirano, N. Sakai, H. Hiraoka, K. Matsumoto, Z. Zhang, S. Nozaki, and Y. Matsuzawa. 2000. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinfl ammatory genes are defective in monocyte-derived macrophages from CD36-defi cient patients. Arterioscler. Thromb. Vasc. Biol. 20: 1953-1960.
59. Chávez-Sánchez, L., A. Madrid-Miller, K. Chávez-Rueda, M. V. Legorreta-Haquet, E. Tesoro-Cruz, and F. Blanco-Favela. 2010. Activation of TLR2 and TLR4 by minimally modifi ed low-density lipoprotein in human macrophages and monocytes triggers the infl ammatory response. Hum. Immunol. 71: 737-744.
60. Bae, Y. S., J. H. Lee, S. H. Choi, S. Kim, F. Almazan, J. L. Witztum, and Y. I. Miller. 2009. Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein: tolllike receptor 4-and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circ. Res. 104: 210-218.