Altered Regulation of ELAVL1/HuR in HLA-B27-Expressing U937 Monocytic Cells

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Sahlberg, Anna S ^a,b   Ruuska, Marja ^a,b   Granfors, Kaisa ^b   Penttinen, Markus A ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

EMBRYONIC LETHAL ABNORMAL VISION L1 PROTEIN; GLUTAMIC ACID; HLA B27 ANTIGEN; HU ANTIGEN; HUMAN ANTIGEN R; INTERLEUKIN 10; LIPOPOLYSACCHARIDE; PROTEIN KINASE R; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; MONOCYTE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN STRUCTURE; REGULATORY MECHANISM; SALMONELLOSIS;

GENE EXPRESSION; GLUTAMIC ACID; HLA-B27 ANTIGEN; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; IMIDAZOLES; INTERLEUKIN-10; MONOCYTES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; SALMONELLA; TUMOR NECROSIS FACTOR-ALPHA; U937 CELLS;

EID: 84880672279     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070377     Document Type: Article

References (46)

1. Ruuska M, Sahlberg AS, Colbert RA, Granfors K, Penttinen MA, (2012) Enhanced phosphorylation of STAT-1 is dependent on double-stranded RNA-dependent protein kinase signaling in HLA-B27-expressing U937 monocytic cells. Arthritis Rheum 64: 772-777.
2. Sahlberg AS, Penttinen MA, Heiskanen KM, Colbert RA, Sistonen L, et al. (2007) Evidence that the p38 MAP kinase pathway is dysregulated in HLA-B27-expressing human monocytic cells: correlation with HLA-B27 misfolding. Arthritis Rheum 56: 2652-2662.
3. Sahlberg AS, Ruuska M, Colbert RA, Granfors K, Penttinen MA, (2012) Altered PKR Signalling and C/ EBPβ Expression is Associated with HLA-B27 Expression in Monocytic Cells. Scandinavian Journal of Immunology 75: 184-192.
4. Gaston JS, Cox C, Granfors K, (1999) Clinical and experimental evidence for persistent Yersinia infection in reactive arthritis. Arthritis Rheum 42: 2239-2242.
5. Granfors K, Jalkanen S, Lindberg AA, Maki-Ikola O, von Essen R, et al. (1990) Salmonella lipopolysaccharide in synovial cells from patients with reactive arthritis. Lancet 335: 685-688.
6. Granfors K, Jalkanen S, von Essen R, Lahesmaa-Rantala R, Isomaki O, et al. (1989) Yersinia antigens in synovial-fluid cells from patients with reactive arthritis. N Engl J Med 320: 216-221.
7. Granfors K, Merilahti-Palo R, Luukkainen R, Mottonen T, Lahesmaa R, et al. (1998) Persistence of Yersinia antigens in peripheral blood cells from patients with Yersinia enterocolitica O:3 infection with or without reactive arthritis. Arthritis Rheum 41: 855-862.
8. Ge S, He Q, Granfors K, (2012) HLA-B27 Modulates Intracellular Growth of Salmonella Pathogenicity Island 2 Mutants and Production of Cytokines in Infected Monocytic U937 Cells. PLoS One 7: e34093.
9. Colbert RA, (2004) The immunobiology of HLA-B27: variations on a theme. Curr Mol Med 4: 21-30.
10. Khan MA, (2002) Update on spondyloarthropathies. Ann Intern Med 136: 896-907.
11. Dangoria NS, DeLay ML, Kingsbury DJ, Mear JP, Uchanska-Ziegler B, et al. (2002) HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation (dimerization) in the endoplasmic reticulum. J Biol Chem 277: 23459-23468.
12. Mear JP, Schreiber KL, Munz C, Zhu X, Stevanovic S, et al. (1999) Misfolding of HLA-B27 as a result of its B pocket suggests a novel mechanism for its role in susceptibility to spondyloarthropathies. J Immunol 163: 6665-6670.
13. Hinman MN, Lou H, (2008) Diverse molecular functions of Hu proteins. Cell Mol Life Sci 65: 3168-3181.
14. von Roretz C, Di Marco S, Mazroui R, Gallouzi IE, (2011) Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip Rev RNA 2: 336-347.
15. Rhee WJ, Ni CW, Zheng Z, Chang K, Jo H, et al. (2010) HuR regulates the expression of stress-sensitive genes and mediates inflammatory response in human umbilical vein endothelial cells. Proc Natl Acad Sci U S A 107: 6858-6863.
16. Dean JL, Wait R, Mahtani KR, Sully G, Clark AR, et al. (2001) The 3' untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol Cell Biol 21: 721-730.
17. Katsanou V, Papadaki O, Milatos S, Blackshear PJ, Anderson P, et al. (2005) HuR as a negative posttranscriptional modulator in inflammation. Mol Cell 19: 777-789.
18. Bergalet J, Fawal M, Lopez C, Desjobert C, Lamant L, et al. (2011) HuR-mediated control of C/EBPbeta mRNA stability and translation in ALK-positive anaplastic large cell lymphomas. Mol Cancer Res 9: 485-496.
19. Eberhardt W, Doller A, Akool el S, Pfeilschifter J, (2007) Modulation of mRNA stability as a novel therapeutic approach. Pharmacol Ther 114: 56-73.
20. Lin WN, Lin CC, Cheng HY, Yang CM, (2011) Regulation of COX-2 and cPLA(2) gene expression by LPS through the RNA-binding protein HuR: involvement of NADPH oxidase, ROS and MAPKs. Br J Pharmacol 163: 1691-1706.
21. Mazroui R, Di Marco S, Clair E, von Roretz C, Tenenbaum SA, et al. (2008) Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. J Cell Biol 180: 113-127.
22. Cherry J, Jones H, Karschner VA, Pekala PH, (2008) Post-transcriptional control of CCAAT/enhancer-binding protein beta (C/EBPbeta) expression: formation of a nuclear HuR-C/EBPbeta mRNA complex determines the amount of message reaching the cytosol. J Biol Chem 283: 30812-30820.
23. von Roretz C, Gallouzi IE, (2010) Protein kinase RNA/FADD/caspase-8 pathway mediates the proapoptotic activity of the RNA-binding protein human antigen R (HuR). J Biol Chem 285: 16806-16813.
24. Sundstrom C, Nilsson K, (1976) Establishment and characterization of a human histiocytic lymphoma cell line (U-937). Int J Cancer 17: 565-577.
25. Taurog JD, Lowen L, Forman J, Hammer RE, (1988) HLA-B27 in inbred and non-inbred transgenic mice. Cell surface expression and recognition as an alloantigen in the absence of human beta 2-microglobulin. J Immunol 141: 4020-4023.
26. Penttinen MA, Heiskanen KM, Mohapatra R, DeLay ML, Colbert RA, et al. (2004) Enhanced intracellular replication of Salmonella enteritidis in HLA-B27-expressing human monocytic cells: dependency on glutamic acid at position 45 in the B pocket of HLA-B27. Arthritis Rheum 50: 2255-2263.
27. Laitio P, Virtala M, Salmi M, Pelliniemi LJ, Yu DT, et al. (1997) HLA-B27 modulates intracellular survival of Salmonella enteritidis in human monocytic cells. Eur J Immunol 27: 1331-1338.
28. Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, et al. (2009) p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29: 4341-4351.
29. Pargellis C, Tong L, Churchill L, Cirillo PF, Gilmore T, et al. (2002) Inhibition of p38 MAP kinase by utilizing a novel allosteric binding site. Nat Struct Biol 9: 268-272.
30. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, et al. (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408: 297-315.
31. Cabanski M, Steinmüller M, Marsh LM, Surdziel E, Seeger W, et al. (2008) PKR regulates TLR2/TLR4-dependent signaling in murine alveolar macrophages. Am J Respir Cell Mol Biol 38: 26-31.
32. Gorina R, Font-Nieves M, Márquez-Kisinousky L, Santalucia T, Planas AM, (2011) Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFκB signaling, MAPK, and Jak1/Stat1 pathways. Glia 59: 242-255.
33. Bennett RL, Blalock WL, Abtahi DM, Pan Y, Moyer SA, et al. (2006) RAX, the PKR activator, sensitizes cells to inflammatory cytokines, serum withdrawal, chemotherapy, and viral infection. Blood 108: 821-829.
34. Kontoyiannis D, Kotlyarov A, Carballo E, Alexopoulou L, Blackshear PJ, et al. (2001) Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J 20: 3760-3770.
35. Dobreva ZG, Miteva LD, Stanilova SA, (2009) The inhibition of JNK and p38 MAPKs downregulates IL-10 and differentially affects c-Jun gene expression in human monocytes. Immunopharmacol Immunotoxicol 31: 195-201.
36. Cheung BK, Lee DC, Li JC, Lau YL, Lau AS, (2005) A role for double-stranded RNA-activated protein kinase PKR in Mycobacterium-induced cytokine expression. J Immunol 175: 7218-7225.
37. Ekman P, Saarinen M, He Q, Gripenberg-Lerche C, Gronberg A, et al. (2002) HLA-B27-transfected (Salmonella permissive) and HLA-A2-transfected (Salmonella nonpermissive) human monocytic U937 cells differ in their production of cytokines. Infect Immun 70: 1609-1614.
38. Maki-Ikola O, Granfors K, (1992) Salmonella-triggered reactive arthritis. Lancet 339: 1096-1098.
39. Ge S, Danino V, He Q, Hinton JC, Granfors K, (2010) Microarray analysis of response of Salmonella during infection of HLA-B27- transfected human macrophage-like U937 cells. BMC Genomics 11: 456.
40. Farooq F, Balabanian S, Liu X, Holcik M, MacKenzie A, (2009) p38 Mitogen-activated protein kinase stabilizes SMN mRNA through RNA binding protein HuR. Hum Mol Genet 18: 4035-4045.
41. Krishnamurthy P, Rajasingh J, Lambers E, Qin G, Losordo DW, et al. (2009) IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR. Circ Res 104: e9-18.
42. Rajasingh J, Bord E, Luedemann C, Asai J, Hamada H, et al. (2006) IL-10-induced TNF-alpha mRNA destabilization is mediated via IL-10 suppression of p38 MAP kinase activation and inhibition of HuR expression. Faseb J 20: 2112-2114.
43. Tanaka T, Akira S, Yoshida K, Umemoto M, Yoneda Y, et al. (1995) Targeted disruption of the NF-IL6 gene discloses its essential role in bacteria killing and tumor cytotoxicity by macrophages. Cell 80: 353-361.
44. Abdelmohsen K, Lal A, Kim HH, Gorospe M, (2007) Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6: 1288-1292.
45. von Roretz C, Gallouzi IE Protein kinase RNA/FADD/caspase-8 pathway mediates the proapoptotic activity of the RNA-binding protein human antigen R (HuR). J Biol Chem 285: 16806-16813.
46. Hsu LC, Park JM, Zhang K, Luo JL, Maeda S, et al. (2004) The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428: 341-345.