E3 ubiquitin ligase NKLAM ubiquitinates STAT1 and positively regulates STAT1-mediated transcriptional activity

Cellular Signalling

Volumn 28, Issue 12, 2016, Pages 1833-1841

  Lawrence, Donald W ^a   Kornbluth, Jacki ^a,b  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA St Louis Healthcare System   (United States)

Author keywords

Innate immunity; Interferon gamma; Macrophage; NKLAM; STAT1; Ubiquitination

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; JANUS KINASE 1; JANUS KINASE 2; NATURAL KILLER LYTIC ASSOCIATED MOLECULE; STAT1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; DNA; INTERFERON RECEPTOR; JAK1 PROTEIN, MOUSE; LYSINE; MEMBRANE PROTEIN; NK LYTIC-ASSOCIATED MOLECULE; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOPRECIPITATION; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; BIOLOGICAL MODEL; BONE MARROW CELL; C57BL MOUSE; CYTOLOGY; DRUG EFFECTS; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; RAW 264.7 CELL LINE;

ANIMALS; BONE MARROW CELLS; DNA; HEK293 CELLS; HUMANS; INTERFERON-GAMMA; JANUS KINASE 1; LYSINE; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN BINDING; RAW 264.7 CELLS; RECEPTORS, INTERFERON; STAT1 TRANSCRIPTION FACTOR; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 84985946897     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2016.08.014     Document Type: Article

References (43)

1. [1] Kozlowski, M., Schorey, J., Portis, T., Grigoriev, V., Kornbluth, J., NK lytic-associated molecule: a novel gene selectively expressed in cells with cytolytic function. J. Immunol. 163:4 (1999), 1775–1785.
2. [2] Portis, T., Anderson, J., Esposito, A., Kornbluth, J., Gene structure of human and mouse NKLAM, a gene associated with cellular cytotoxicity. Immunogenetics 51:7 (2000), 546–555.
3. [3] Fortier, J.M., Kornbluth, J., NK lytic-associated molecule, involved in NK cytotoxic function, is an E3 ligase. J. Immunol. 176:11 (2006), 6454–6463.
4. [4] Lawrence, D.W., Kornbluth, J., E3 ubiquitin ligase NKLAM is a macrophage phagosome protein and plays a role in bacterial killing. Cell. Immunol. 279:1 (2012), 46–52.
5. [5] Hoover, R.G., Gullickson, G., Kornbluth, J., Impaired NK cytolytic activity and enhanced tumor growth in NK lytic-associated molecule-deficient mice. J. Immunol. 183:11 (2009), 6913–6921.
6. [6] Hoover, R.G., Gullickson, G., Kornbluth, J., Natural killer lytic-associated molecule plays a role in controlling tumor dissemination and metastasis. Front. Immunol., 3, 2012, 393.
7. [7] Cookson, M.R., The biochemistry of Parkinson's disease. Annu. Rev. Biochem. 74 (2005), 29–52.
8. [8] Dawson, T.M., Dawson, V.L., Molecular pathways of neurodegeneration in Parkinson's disease. Science 302:5646 (2003), 819–822.
9. [9] Sone, J., Niwa, J., Kawai, K., Ishigaki, S., Yamada, S., Adachi, H., Katsuno, M., Tanaka, F., Doyu, M., Sobue, G., Dorfin ameliorates phenotypes in a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci. Res. 88:1 (2010), 123–135.
10. [10] Ali, S., Vollaard, A.M., Widjaja, S., Surjadi, C., van de Vosse, E., van Dissel, J.T., PARK2/PACRG polymorphisms and susceptibility to typhoid and paratyphoid fever. Clin. Exp. Immunol. 144:3 (2006), 425–431.
11. [11] Malhotra, D., Darvishi, K., Lohra, M., Kumar, H., Grover, C., Sood, S., Reddy, B.S., Bamezai, R.N., Association study of major risk single nucleotide polymorphisms in the common regulatory region of PARK2 and PACRG genes with leprosy in an Indian population. Eur. J. Hum. Genet. 14:4 (2006), 438–442.
12. [12] Manzanillo, P.S., Ayres, J.S., Watson, R.O., Collins, A.C., Souza, G., Rae, C.S., Schneider, D.S., Nakamura, K., Shiloh, M.U., Cox, J.S., The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501:7468 (2013), 512–516.
13. [13] Mira, M.T., Alcais, A., Nguyen, V.T., Moraes, M.O., Di Flumeri, C., Vu, H.T., Mai, C.P., Nguyen, T.H., Nguyen, N.B., Pham, X.K., Sarno, E.N., Alter, A., Montpetit, A., Moraes, M.E., Moraes, J.R., Dore, C., Gallant, C.J., Lepage, P., Verner, A., Van De Vosse, E., Hudson, T.J., Abel, L., Schurr, E., Susceptibility to leprosy is associated with PARK2 and PACRG. Nature 427:6975 (2004), 636–640.
14. [14] Lim, C.P., Cao, X., Structure, function, and regulation of STAT proteins. Mol. BioSyst. 2:11 (2006), 536–550.
15. [15] Reich, N.C., STATs get their move on. Jak-Stat, 2(4), 2013, e27080.
16. [16] Kim, T.K., Maniatis, T., Regulation of interferon-gamma-activated STAT1 by the ubiquitin-proteasome pathway. Science 273:5282 (1996), 1717–1719.
17. [17] Tanaka, T., Soriano, M.A., Grusby, M.J., SLIM is a nuclear ubiquitin E3 ligase that negatively regulates STAT signaling. Immunity 22:6 (2005), 729–736.
18. [18] Yuan, C., Qi, J., Zhao, X., Gao, C., Smurf1 protein negatively regulates interferon-gamma signaling through promoting STAT1 protein ubiquitination and degradation. J. Biol. Chem. 287:21 (2012), 17006–17015.
19. [19] Garcin, D., Marq, J.B., Strahle, L., le Mercier, P., Kolakofsky, D., All four Sendai Virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295:2 (2002), 256–265.
20. [20] Leidner, J., Palkowitsch, L., Marienfeld, U., Fischer, D., Marienfeld, R., Identification of lysine residues critical for the transcriptional activity and polyubiquitination of the NF-kappaB family member RelB. Biochem. J. 416:1 (2008), 117–127.
21. [21] van der Horst, A., de Vries-Smits, A.M., Brenkman, A.B., van Triest, M.H., van den Broek, N., Colland, F., Maurice, M.M., Burgering, B.M., FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol. 8:10 (2006), 1064–1073.
22. [22] Brooks, B., Briggs, D.M., Eastmond, N.C., Fernig, D.G., Coleman, J.W., Presentation of IFN-gamma to nitric oxide-producing cells: a novel function for mast cells. J. Immunol. 164:2 (2000), 573–579.
23. [23] Gao, J., Morrison, D.C., Parmely, T.J., Russell, S.W., Murphy, W.J., An interferon-gamma-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-gamma and lipopolysaccharide. J. Biol. Chem. 272:2 (1997), 1226–1230.
24. [24] Irie-Sasaki, J., Sasaki, T., Matsumoto, W., Opavsky, A., Cheng, M., Welstead, G., Griffiths, E., Krawczyk, C., Richardson, C.D., Aitken, K., Iscove, N., Koretzky, G., Johnson, P., Liu, P., Rothstein, D.M., Penninger, J.M., CD45 is a JAK phosphatase and negatively regulates cytokine receptor signalling. Nature 409:6818 (2001), 349–354.
25. [25] Xu, D., Qu, C.K., Protein tyrosine phosphatases in the JAK/STAT pathway. Front. Biosci. 13 (2008), 4925–4932.
26. [26] van den Broek, M.F., Muller, U., Huang, S., Aguet, M., Zinkernagel, R.M., Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 69:8 (1995), 4792–4796.
27. [27] Lawrence, D.W., Gullickson, G., Kornbluth, J., E3 ubiquitin ligase NKLAM positively regulates macrophage inducible nitric oxide synthase expression. Immunobiology 220:1 (2015), 83–92.
28. [28] Ramana, C.V., Gil, M.P., Han, Y., Ransohoff, R.M., Schreiber, R.D., Stark, G.R., Stat1-independent regulation of gene expression in response to IFN-gamma. Proc. Natl. Acad. Sci. U. S. A. 98:12 (2001), 6674–6679.
29. [29] Pine, R., Canova, A., Schindler, C., Tyrosine phosphorylated p91 binds to a single element in the ISGF2/IRF-1 promoter to mediate induction by IFN alpha and IFN gamma, and is likely to autoregulate the p91 gene. EMBO J. 13:1 (1994), 158–167.
30. [30] Liu, J., Guan, X., Ma, X., Interferon regulatory factor 1 is an essential and direct transcriptional activator for interferon {gamma}-induced RANTES/CCl5 expression in macrophages. J. Biol. Chem. 280:26 (2005), 24347–24355.
31. [31] Liu, L., Okada, S., Kong, X.F., Kreins, A.Y., Cypowyj, S., Abhyankar, A., Toubiana, J., Itan, Y., Audry, M., Nitschke, P., Masson, C., Toth, B., Flatot, J., Migaud, M., Chrabieh, M., Kochetkov, T., Bolze, A., Borghesi, A., Toulon, A., Hiller, J., Eyerich, S., Eyerich, K., Gulacsy, V., Chernyshova, L., Chernyshov, V., Bondarenko, A., Grimaldo, R.M., Blancas-Galicia, L., Beas, I.M., Roesler, J., Magdorf, K., Engelhard, D., Thumerelle, C., Burgel, P.R., Hoernes, M., Drexel, B., Seger, R., Kusuma, T., Jansson, A.F., Sawalle-Belohradsky, J., Belohradsky, B., Jouanguy, E., Bustamante, J., Bue, M., Karin, N., Wildbaum, G., Bodemer, C., Lortholary, O., Fischer, A., Blanche, S., Al-Muhsen, S., Reichenbach, J., Kobayashi, M., Rosales, F.E., Lozano, C.T., Kilic, S.S., Oleastro, M., Etzioni, A., Traidl-Hoffmann, C., Renner, E.D., Abel, L., Picard, C., Marodi, L., Boisson-Dupuis, S., Puel, A., Casanova, J.L., Gain-of-function human STAT1 mutations impair IL-17 immunity and underlie chronic mucocutaneous candidiasis. J. Exp. Med. 208:8 (2011), 1635–1648.
32. [32] Duran, A., Rodriguez, A., Martin, P., Serrano, M., Flores, J.M., Leitges, M., Diaz-Meco, M.T., Moscat, J., Crosstalk between PKCzeta and the IL4/Stat6 pathway during T-cell-mediated hepatitis. EMBO J. 23:23 (2004), 4595–4605.
33. [33] Vitour, D., Doceul, V., Ruscanu, S., Chauveau, E., Schwartz-Cornil, I., Zientara, S., Induction and control of the type I interferon pathway by Bluetongue virus. Virus Res. 182 (2014), 59–70.
34. [34] Bohmer, F.D., Friedrich, K., Protein tyrosine phosphatases as wardens of STAT signaling. Jak-Stat, 3(1), 2014, e28087.
35. [35] Yang, C.Y., Chiu, L.L., Tan, T.H., TRAF2-mediated Lys63-linked ubiquitination of DUSP14/MKP6 is essential for its phosphatase activity. Cell. Signal. 28:1 (2016), 145–151.
36. [36] Yang, W.L., Zhang, X., Lin, H.K., Emerging role of Lys-63 ubiquitination in protein kinase and phosphatase activation and cancer development. Oncogene 29:32 (2010), 4493–4503.
37. [37] You, M., Yu, D.H., Feng, G.S., Shp-2 tyrosine phosphatase functions as a negative regulator of the interferon-stimulated Jak/STAT pathway. Mol. Cell. Biol. 19:3 (1999), 2416–2424.
38. [38] Li, Q., Means, R., Lang, S., Jung, J.U., Downregulation of gamma interferon receptor 1 by Kaposi's sarcoma-associated herpesvirus K3 and K5. J. Virol. 81:5 (2007), 2117–2127.
39. [39] Dumoutier, L., de Meester, C., Tavernier, J., Renauld, J.C., New activation modus of STAT3: a tyrosine-less region of the interleukin-22 receptor recruits STAT3 by interacting with its coiled-coil domain. J. Biol. Chem. 284:39 (2009), 26377–26384.
40. [40] Olayioye, M.A., Beuvink, I., Horsch, K., Daly, J.M., Hynes, N.E., ErbB receptor-induced activation of stat transcription factors is mediated by Src tyrosine kinases. J. Biol. Chem. 274:24 (1999), 17209–17218.
41. [41] Adhikary, S., Marinoni, F., Hock, A., Hulleman, E., Popov, N., Beier, R., Bernard, S., Quarto, M., Capra, M., Goettig, S., Kogel, U., Scheffner, M., Helin, K., Eilers, M., The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123:3 (2005), 409–421.
42. [42] Huntelmann, B., Staab, J., Herrmann-Lingen, C., Meyer, T., A conserved motif in the linker domain of STAT1 transcription factor is required for both recognition and release from high-affinity DNA-binding sites. PLoS One, 9(5), 2014, e97633.
43. [43] Ahmed, C.M., Johnson, H.M., IFN-gamma and its receptor subunit IFNGR1 are recruited to the IFN-gamma-activated sequence element at the promoter site of IFN-gamma-activated genes: evidence of transactivational activity in IFNGR1. J. Immunol. 177:1 (2006), 315–321.