Caenorhabditis elegans mom-4 is required for the activation of the p38 MAPK signaling pathway in the response to Pseudomonas aeruginosa infection

Ajing Xu1,3, Guojun Shi3,4, Feng Liu3,4, Baoxue Ge2,3()

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Protein Cell ›› 2013, Vol. 4 ›› Issue (1) : 53-61. DOI: 10.1007/s13238-012-2080-z
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Caenorhabditis elegans mom-4 is required for the activation of the p38 MAPK signaling pathway in the response to Pseudomonas aeruginosa infection

  • Ajing Xu1,3, Guojun Shi3,4, Feng Liu3,4, Baoxue Ge2,3()
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Abstract

The p38 mitogen-activated protein kinase (MAPK) plays an evolutionarily conserved role in the cellular response to microbial infection and environmental stress. Activation of p38 is mediated through phosphorylation by upstream MAPKK, which in turn is activated by MAPKKK. In the Caenorhabditis elegans, the p38 MAPK (also called PMK-1) signaling pathway has been shown to be required in its resistance to bacterial infection. However, how different upstream MAP2Ks and MAP3Ks specifically contribute to the activation of PMK-1 in response to bacterial infection still is not clearly understood. By using double-stranded RNA-mediated interference (RNAi) and genetic mutants of C. elegans, we demonstrate that C. elegans MOM-4, a mammalian TAK1 homolog, is required for the resistance of C. elegans to a P. aeruginosa infection. We have also found that the MKK-4 of C. elegans is required for P. aeruginosa resistance, but not through the regulation of DLK-1. In summary, our results indicate that different upstream MAPKKKs or MAPKKs regulate the activation of PMK-1 in response to P. aeruginosa.

Keywords

C. elegans / MAPK / innate immunity / p38 / P. aeruginosa PA-14 / MOM-4

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Ajing Xu, Guojun Shi, Feng Liu, Baoxue Ge. Caenorhabditis elegans mom-4 is required for the activation of the p38 MAPK signaling pathway in the response to Pseudomonas aeruginosa infection. Prot Cell, 2013, 4(1): 53‒61 https://doi.org/10.1007/s13238-012-2080-z

References

[1] Berman, K., McKay, J., Avery, L., and Cobb, M. (2001). Isolation and characterization of pmk-(1-3): three p38 homologs in Caenorhabditis elegans. Mol Cell Biol Res Commun 4, 337-344 .10.1006/mcbr.2001.0300
[2] Brancho, D., Tanaka, N., Jaeschke, A., Ventura, J.J., Kelkar, N., Tanaka, Y., Kyuuma, M., Takeshita, T., Flavell, R.A., and Davis R .J. (2003). Mechanism of p38 MAP kinase activation in vivo. Genes Dev 17, 1969-1978 .10.1101/gad.1107303
[3] Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94 .
[4] Byrd, D.T., Kawasaki, M., Walcoff, M., Hisamoto, N., Matsumoto, K., and Jin, Y. (2001). UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32, 787-800 .10.1016/S0896-6273(01)00532-3
[5] Chiariello, M., Marinissen M.J., and Gutkind J.S. (2000). Multiple mitogen-activated protein kinase signaling pathways connect the cot oncoprotein to the c-jun promoter and to cellular transformation. Mol Cell Biol 20, 1747-1758 .10.1128/MCB.20.5.1747-1758.2000
[6] Cobb, M.H., Boulton T.G., and Robbins D.J. (1991). Extracellular signal-regulated kinases: ERKs in progress. Cell Regul 2, 965-978 .
[7] Deacon, K. and Blank J.L. (1999). MEK kinase 3 directly activates MKK6 and MKK7, specific activators of the p38 and c-Jun NH2-terminal kinases. J Biol Chem. 274( 23), 16604-16610 .10.1074/jbc.274.23.16604
[8] Deak, M., Clifton, A.D., Lucocq, L.M., and Alessi, D.R. (1998). Mitogen- and stress-activated protein kinase-1 (MSK1) is directly activated by MAPK and SAPK2/p38, and may mediate activation of CREB. EMBO J 17, 4426-4441 .10.1093/emboj/17.15.4426
[9] Delaney, J.R. and Mlodzik, M., (2006). TGF-beta activated kinase-1: new insights into the diverse roles of TAK1 in development and immunity. Cell Cycle 5, 2852-2825 .10.4161/cc.5.24.3558
[10] Dérijard, B., Hibi, M., Wu, I.H., Barrett, T., Su, B., Deng, T., Karin, M., and Davis, R.J. (1994). JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76, 1025-1037 .10.1016/0092-8674(94)90380-8
[11] Fukunaga, R. and Hunter T. (1997). MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 16, 1921-1933 .10.1093/emboj/16.8.1921
[12] Han, J., Lee, J.D., Bibbs, L., and Ulevitch, R.J. (1994). A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265, 808-811 .10.1126/science.7914033
[13] Han, J., Jiang, Y., Li, Z., Kravchenko, V.V., and Ulevitch, R.J. (1997). Activation of the transcription factor MEF2C by the MAP kinase p38 in inflammation. Nature 386, 296-299 .10.1038/386296a0
[14] Herskowitz, I. (1995). MAP kinase pathways in yeast: for mating and more. Cell 80, 187-197 .10.1016/0092-8674(95)90402-6
[15] Ichijo, H., Nishida, E., Irie, K., ten Dijke, P., Saitoh, M., Moriguchi, T., Takagi, M., and Matsumoto, K. (1997). Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275, 90-94 .10.1126/science.275.5296.90
[16] Iordanov, M., Bender, K., Ade, T., Schmid, W., Sachsenmaier, C., Engel, K., Gaestel, M., Rahmsdorf, H.J., and Herrlich, P. (1997). CREB is activated by UVC through a p38/HOG-1-dependent protein kinase. EMBO J 16, 1009-1022 .10.1093/emboj/16.5.1009
[17] Kajino-Sakamoto, R., Inagaki, M., Lippert, E., Akira, S., Robine, S., Matsumoto, K., Jobin, C., and Ninomiya-Tsuji, J. (2008). Enterocyte- derived TAK1 signaling prevents epithelium apoptosis and the development of ileitis and colitis. J Immunol 181, 1143-1152 .
[18] Kamath, R.S., Fraser, A.G., Dong, Y., Poulin, G., Sohrmann, M., Welchman, D.P., Zipperlen, P., and Ahringer, J. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237 .10.1038/nature01278
[19] Kawasaki, M., Hisamoto, N., Iino, Y., Yamamoto, M., Ninomiya-Tsuji, J., and Matsumoto, K. (1999). A Caenorhabditis elegans JNK signal transduction pathway regulates coordinated movement via type-D GABAergic motor neurons. EMBO J 18, 3604-3615 .10.1093/emboj/18.13.3604
[20] Kim, D.H. and Ausubel F.M. (2005). Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans. Curr Opin Immunol 17, 4-10 .10.1016/j.coi.2004.11.007
[21] Kim, D.H., Feinbaum, R., Alloing, G., Emerson, F.E., Garsin, D.A., Inoue, H., Tanaka-Hino, M., Hisamoto, N., Matsumoto, K., Tan, M.W., et al. (2002). A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623-626 .10.1126/science.1073759
[22] Koga, M., Zwaal, R., Guan, K.L., Avery, L., and Ohshima, Y. (2000). A Caenorhabditis elegans MAP kinase kinase, MEK-1, is involved in stress responses. EMBO J 19, 5148-5156 .10.1093/emboj/19.19.5148
[23] Kyriakis, J.M. and Avruch, J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81, 807-869 .
[24] Kyriakis, J.M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E.A., Ahmad, M.F., Avruch, J., and Woodgett, J.R. (1994). The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369, 156-160 .10.1038/369156a0
[25] Lee, J.C., Laydon, J.T., McDonnell, P.C., Gallagher, T.F., Kumar, S., Green, D., McNulty, D., Blumenthal, M.J., Heys, J.R., and Landvatter, S.W. (1994). A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372, 739-746 .10.1038/372739a0
[26] Lu, G., Kang, Y.J., Han, J., Herschman, H.R., Stefani, E., and Wang, Y. (2006). TAB-1 modulates intracellular localization of p38 MAP kinase and downstream signaling. J Biol Chem 281, 6087-6095 .10.1074/jbc.M507610200
[27] Nakata, K., Abrams, B., Grill, B., Goncharov, A., Huang, X., Chisholm, A.D., and Jin, Y. (2005). Regulation of a DLK-1 and p38 MAP kinase pathway by the ubiquitin ligase RPM-1 is required for presynaptic development. Cell 120, 407-420 .10.1016/j.cell.2004.12.017
[28] New, L., Jiang, Y., Zhao, M., Liu, K., Zhu, W., Flood, L.J., Kato, Y., Parry, G.C., and Han, J. (1998). PRAK, a novel protein kinase regulated by the p38 MAP kinase. EMBO J 17, 3372-3384 .10.1093/emboj/17.12.3372
[29] Ninomiya-Tsuji, J., Kishimoto, K., Hiyama, A., Inoue, J., Cao, Z., and Matsumoto, K. (1999). The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway. Nature 398, 252-256 .10.1038/18465
[30] Pierrat, B., Correia, J.S., Mary, J.L., Tomás-Zuber, M., and Lesslauer, W. (1998). RSK-B, a novel ribosomal S6 kinase family member, is a CREB kinase under dominant control of p38alpha mitogen- activated protein kinase (p38alphaMAPK). J Biol Chem. 273, 29661-29671 .10.1074/jbc.273.45.29661
[31] Plowman, G.D., Sudarsanam, S., Bingham, J., Whyte, D., and Hunter, T. (1999). The protein kinases of Caenorhabditis elegans: a model for signal transduction in multicellular organisms. Proc Natl Acad Sci U S A 96, 13603-13610 .10.1073/pnas.96.24.13603
[32] Raingeaud, J., Whitmarsh, A.J., Barrett, T., Derijard, B, and Davis, R.J. (1996). MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol 16, 1247-1255 .
[33] Sagasti, A., Hisamoto, N., Hyodo, J., Tanaka-Hino, M., Matsumoto, K., and Bargmann, C.I. (2001). The CaMKII UNC-43 activates the MAPKKK NSY-1 to execute a lateral signaling decision required for asymmetric olfactory neuron fates. Cell 105, 221-232 .10.1016/S0092-8674(01)00313-0
[34] Sakaguchi, A., Matsumoto K., and Hisamoto N. (2004). Roles of MAP kinase cascades in Caenorhabditis elegans. J Biochem (Tokyo) 136, 7-11 .10.1093/jb/mvh097
[35] Schaeffer, H.J. and Weber M.J. (1999). Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol Cell Biol 19, 2435-2444 .
[36] Shapira, M., Hamlim, B., Rong, J.M., Chen, K., Ronen, M., and Tan, M.W. (2006). A conserved role for a GATA transcription factor in regulating epithelial innate immune responses. Proc Natl Acad Sci U S A 103, 14086-14091 .10.1073/pnas.0603424103
[37] Shivers, R.P., Pagano, D.J., Kooistra, T., Richardson, C.E., Reddy, K.C., Whitney, J.K., Kamanzi, O., Matsumoto, K., Hisamoto, N., and Kim, D.H. (2010). Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans. PLoS Genet 6, e100089210.1371/journal.pgen.1000892
[38] Stokoe, D., Campbell, D.G., Nakielny, S., Hidaka, H., Leevers, S.J., Marshall, C., and Cohen, P. (1992). MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J 11, 3985-3994 .
[39] Symons, A., Beinke S., and Ley S.C. (2006). MAP kinase kinase kinases and innate immunity. Trends Immunol 27, 40-48 .10.1016/j.it.2005.11.007
[40] Tan, M.W., Rahme, L.G., Sternberg, J.A., Tompkins, R.G., and Ausubel, F.M. (1999). Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96, 2408-2413 .10.1073/pnas.96.5.2408
[41] Tanaka, N., Kamanaka, M., Enslen, H., Dong, C., Wysk, M., Davis, R.J., and Flavell, R.A. (2002). Differential involvement of p38 mitogen- activated protein kinase kinases MKK3 and MKK6 in T-cell apoptosis. EMBO Rep 3, 785-791 .10.1093/embo-reports/kvf153
[42] Tibbles, L.A., Ing, Y.L., Kiefer, F., Chan, J., Iscove, N., Woodgett, J.R., and Lassam, N.J. (1996). MLK-3 activates the SAPK/JNK and p38/RK pathways via SEK1 and MKK3/6. EMBO J 15, 7026-7035 .
[43] Timmons, L., Court D.L., and Fire A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112 .10.1016/S0378-1119(00)00579-5
[44] Troemel, E.R., Chu, S.W., Reinke, V., Lee, S.S., Ausubel, F.M., Kim, D.H. (2006). p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2, 1725-1739 .10.1371/journal.pgen.0020183
[45] Wan, Y.Y., Chi, H., Xie, M., Schneider, M.D., and Flavell, R.A. (2006). The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat Immunol 7, 851-858 .10.1038/ni1355
[46] Wang, X.Z. and Ron D. (1996). Stress-induced phosphorylation and activation of the transcription factor CHOP (GADD153) by p38 MAP Kinase. Science 272, 1347-1349 .10.1126/science.272.5266.1347
[47] Waskiewicz, A.J. and Cooper J.A. (1995). Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol 7, 798-805 .10.1016/0955-0674(95)80063-8
[48] Waskiewicz, A.J., Flynn, A., Proud, C.G., and Cooper, J.A. (1997). Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16, 1909-1920 .10.1093/emboj/16.8.1909
[49] Whitmarsh, A.J., Yang, S.H., Su, M.S., Sharrocks, A.D., and Davis, R.J. (1997). Role of p38 and JNK mitogen-activated protein kinases in the activation of ternary complex factors. Mol Cell Biol 17, 2360-2371 .
[50] Widmann, C., Gibson, S., Jarpe, M.B., and Johnson, G.L. (1999). Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79, 143-180 .
[51] Wolff, S., Ma, H., Burch, D., Maciel, G.A., Hunter, T., and Dillin, A. (2006). SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 124, 1039-1053 .10.1016/j.cell.2005.12.042
[52] Wysk, M., Yang, D.D., Lu, H.T., Flavell, R.A., and Davis, R.J. (1999). Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for tumor necrosis factor-induced cytokine expression. Proc Natl Acad Sci U S A 96, 3763-3768 .10.1073/pnas.96.7.3763
[53] Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E., and Matsumoto, K. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270, 2008-2011 .10.1126/science.270.5244.2008
[54] Zhuang, Z.H., Sun, L., Kong, L., Hu, J.H., Yu, M.C., Reinach, P., Zang, J.W., and Ge, B.X. (2006). Regulation of Drosophila p38 activation by specific MAP2 kinase and MAP3 kinase in response to different stimuli. Cell Signal 18, 441-448 .10.1016/j.cellsig.2005.05.013
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