Hop-on hop-off: Importin-α-guided tours to the nucleus in innate immune signaling

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  Wirthmueller, Lennart ^a   Roth, Charlotte ^b   Banfield, Mark J ^a   Wiermer, Marcel ^b  

^a JOHN INNES CENTRE   (United Kingdom)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Arabidopsis; Importin ; Innate immunity; Nuclear protein import; Nucleocytoplasmic transport

Indexed keywords

EID: 84885193216     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00149     Document Type: Review

References (96)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J., and Parker, J. E. (1998). Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 95, 10306-10311.
2. Ausubel, F. M. (2005). Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6, 973-979.
3. Bhattacharjee, S., Lee, L., and Oltmanns, H. (2008). IMPa-4, an Arabidopsis importin-α isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20, 2661-2680.
4. Bhattacharya, A., and Steward, R. (2002). The Drosophila homolog of NTF-2, the nuclear transport factor-2, is essential for immune response. EMBO Rep. 3, 378-383.
5. Borg, M., Brownfield, L., Khatab, H., Sidorova, A., Lingaya, M., and Twell, D. (2011). The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell 23, 534-549.
6. Burch-Smith, T. M., Schiff, M., Caplan, J. L., Tsao, J., Czymmek, K., and Dinesh-Kumar, S. P. (2007). A novel role for the TIR domain in association with pathogen-derived elicitors. PLoS Biol. 5:e68. doi: 10.1371/journal.pbio.0050068
7. Caillaud, M.-C., Piquerez, S. J. M., Fabro, G., Steinbrenner, J., Ishaque, N., Beynon, J., et al. (2012a). Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 69, 252-265.
8. Caillaud, M.-C., Wirthmueller, L., Fabro, G., Piquerez, S. J. M., Asai, S., Ishaque, N., et al. (2012b). Mechanisms of nuclear suppression of host immunity by effectors from the Arabidopsis downy mildew pathogen Hyaloperonospora arabidopsidis (Hpa). Cold Spring Harb. Symp. Quant. Biol. [Epub ahead of print].
9. Caplan, J., Padmanabhan, M., and Dinesh-Kumar, S. P. (2008). Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe 3, 126-135.
10. Cardarelli, F., Bizzarri, R., Serresi, M., Albertazzi, L., and Beltram, F. (2009). Probing nuclear localization signal-importin alpha binding equilibria in living cells. J. Biol. Chem. 284, 36638-36646.
11. Chang, C.-W., Counago, R. L. M., Williams, S. J., Boden, M., and Kobe, B. (2012). Crystal structure of rice importin-α and structural basis of its interaction with plant-specific nuclear localization signals. Plant Cell 24, 5074-5088.
12. Cheng, Y. T., Germain, H., Wiermer, M., Bi, D., Xu, F., Garcia, A. V., et al. (2009). Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21, 2503-2516.
13. Cohen, S., Etingov, I., and Panté, N. (2012). Effect of viral infection on the nuclear envelope and nuclear pore complex. Int. Rev. Cell Mol. Biol. 299, 117-159.
14. Conti, E., Uy, M., and Leighton, L. (1998). Crystallographic analysis of the recognition of a nuclear localization signal by the nuclear import factor karyopherin-α. Cell 94, 193-204.
15. Cressman, D. E., O'Connor, W. J., Greer, S. F., Zhu, X. S., and Ting, J. P. (2001). Mechanisms of nuclear import and export that control the subcellular localization of class II transactivator. J. Immunol. 167, 3626-3634.
16. Deslandes, L., and Rivas, S. (2011). The plant cell nucleus: a true arena for the fight between plants and pathogens. Plant Signal. Behav. 6, 42-48.
17. Deslandes, L., Olivier, J., Peeters, N., Feng, D. X., Khounlotham, M., Boucher, C., et al. (2003). Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100, 8024-8029.
18. Dias, S. M. G., Cerione, R. A., and Wilson, K. F. (2010). Unloading RNAs in the cytoplasm. Nucleus 1, 139-143.
19. Dias, S. M. G., Wilson, K. F., Rojas, K. S., Ambrosio, A. L. B., and Cerione, R. A. (2009). The molecular basis for the regulation of the cap-binding complex by the importins. Nat. Struct. Mol. Biol. 16, 930-937.
20. Fagerlund, R., Kinnunen, L., Köhler, M., Julkunen, I., and Melén, K. (2005). NF-kB is transported into the nucleus by importin a3 and importin a4. J. Biol. Chem. 280, 15942-15951.
21. Fagerlund, R., Melen, K., Kinnunen, L., and Julkunen, I. (2002). Arginine/lysine-rich nuclear localization signals mediate interactions between dimeric STATs and importin α5. J. Biol. Chem. 277, 30072-30078.
22. Feys, B. J., Moisan, L. J., Newman, M. A., and Parker, J. E. (2001). Direct interaction between the Arabidopsisdisease resistance signaling proteins, EDS1 and PAD4. EMBO J. 20, 5400-5411.
23. Feys, B. J., Wiermer, M., Bhat, R. A., Moisan, L. J., Medina-Escobar, N., Neu, C., et al. (2005). ArabidopsisSENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17, 2601-2613.
24. Fontes, M. R., Teh, T., Jans, D., Brinkworth, R. I., and Kobe, B. (2003). Structural basis for the specificity of bipartite nuclear localization sequence binding by importin-alpha. J. Biol. Chem. 278, 27981-27987.
25. Garcia, A. V., Blanvillain-Baufume, S., Huibers, R. P., Wiermer, M., Li, G., Gobbato, E., et al. (2010). Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog. 6:e1000970. doi: 10.1371/journal.ppat.1000970
26. Ge, Q., Nakagawa, T., Wynn, R. M., Chook, Y. M., Miller, B. C., and Uyeda, K. (2011). Importin-alpha protein binding to a nuclear localization signal of carbohydrate response element-binding protein (ChREBP). J. Biol. Chem. 286, 28119-28127.
27. Gelvin, S. B. (2010). Finding a way to the nucleus. Curr. Opin. Microbiol. 13, 53-58.
28. Genoud, T., Schweizer, F., Tscheuschler, A., Debrieux, D., Casal, J. J., Schäfer, E., et al. (2008). FHY1 mediates nuclear import of the light-activated phytochrome A photoreceptor. PLoS Genet. 4:e1000143. doi: 10.1371/journal.pgen.1000143
29. Goldfarb, D. S., Corbett, A. H., Mason, D. A., Harreman, M. T., and Adam, S. A. (2004). Importin α: a multipurpose nuclear-transport receptor. Trends Cell Biol. 14, 505-514.
30. Görlich, D., Henklein, P., Laskey, R. A., and Hartmann, E. (1996a). A 41 amino acid motif in importin-alpha confers binding to importin-beta and hence transit into the nucleus. EMBO J. 15, 1810-1817.
31. Görlich, D., Kraft, R., Kostka, S., Vogel, F., Hartmann, E., Laskey, R. A., et al. (1996b). Importin provides a link between nuclear protein import and U snRNA export. Cell 87, 21-32.
32. He, S., Huang, K., Zhang, X., Yu, X., Huang, P., and An, C. (2011). The LSD1-type zinc finger motifs of Pisum sativaLSD1 are a novel nuclear localization signal and interact with importin alpha. PLoS ONE 6:e22131. doi: 10.1371/journal.pone.0022131
33. Hodel, A. E., Harreman, M. T., Pulliam, K. F., Harben, M. E., Holmes, J. S., Hodel, M. R., et al. (2006). Nuclear localization signal receptor affinity correlates with in vivo localization in Saccharomyces cerevisiae. J. Biol. Chem. 281, 23545-23556.
34. Hodel, M. R., Corbett, A. H., and Hodel, A E. (2001). Dissection of a nuclear localization signal. J. Biol. Chem. 276, 1317-1325.
35. Hruz, T., Laule, O., Szabo, G., Wessendorp, F., Bleuler, S., Oertle, L., et al. (2008). Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv. Bioinformatics 2008, 420747.
36. Hu, J., Wang, F., Yuan, Y., Zhu, X., Wang, Y., Zhang, Y., et al. (2010). Novel importin-alpha family member Kpnα7 is required for normal fertility and fecundity in the mouse. J. Biol. Chem. 285, 33113-33122.
37. Huang, J.-G., Yang, M., Liu, P., Yang, G.-D., Wu, C.-A., and Zheng, C.-C. (2010). Genome-wide profiling of developmental, hormonal or environmental responsiveness of the nucleocytoplasmic transport receptors in Arabidopsis. Gene 451, 38-44.
38. Huang, T. T., Kudo, N., Yoshida, M., and Miyamoto, S. (2000). A nuclear export signal in the N-terminal regulatory domain of IκBα controls cytoplasmic localization of inactive NF-κB/IκBαcomplexes. Proc. Natl. Acad. Sci. U.S.A. 97, 1014-1019.
39. Jiang, C. J., Shoji, K., Matsuki, R., Baba, A., Inagaki, N., Ban, H., et al. (2001). Molecular cloning of a novel importin alpha homologue from rice, by which Constitutive Photomorphogenic 1 (COP1) nuclear localization signal (NLS)-protein is preferentially nuclear imported. J. Biol. Chem. 276, 9322-9329.
40. Johnson, C., Van Antwerp, D., and Hope, T. J. (1999). An N-terminal nuclear export signal is required for the nucleocytoplasmic shuttling of IκBα. EMBO J. 18, 6682-6693.
41. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329.
42. Kaminaka, H., Näke, C., Epple, P., Dittgen, J., Schütze, K., Chaban, C., et al. (2006). bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J. 25, 4400-4411.
43. Kanneganti, T.-D. D., Bai, X., Tsai, C.-W. W., Win, J., Meulia, T., Goodin, M., et al. (2007b). A functional genetic assay for nuclear trafficking in plants. Plant J. 50, 149-158.
44. Kanneganti, T. D., Lamkanfi, M., and Nunez, G. (2007a). Intracellular NOD-like receptors in host defense and disease. Immunity 27, 549-559.
45. Kelley, J. B., Talley, A. M., Spencer, A., Gioeli, D., and Paschal, B. M. (2010). Karyopherin alpha7 (KPNA7), a divergent member of the importin alpha family of nuclear import receptors. BMC Cell Biol. 11:63. doi: 10.1186/1471-2121-11-63
46. Kinkema, M., Fan, W. H., and Dong, X. N. (2000). Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12, 2339-2350.
47. Kobe, B. (1999). Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin alpha. Nat. Struct. Biol. 6, 388-397.
48. Köhler, M., Ansieau, S., Prehn, S., Leutz, A., Haller, H., and Hartmann, E. (1997). Cloning of two novel human importin-α subunits and analysis of the expression pattern of the importin-α protein family. FEBS Lett. 417, 104-108.
49. Köhler, M., Speck, C., Christiansen, M., Bischoff, R., Prehn, S., Haller, H., et al. (1999). Evidence for distinct substrate specificities of importin α family members in nuclear protein import evidence for distinct substrate specificities of importin α family members in nuclear protein import. Mol. Cell Biol. 19, 7782-7791.
50. Kosugi, S., Hasebe, M., Entani, T., Takayama, S., Tomita, M., and Yanagawa, H. (2008). Design of peptide inhibitors for the importin αβ nuclear import pathway by activity-based profiling. Chem. Biol. 15, 940-949.
51. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
52. Lim, C. P., and Cao, X. (2006). Structure, function, and regulation of STAT proteins. Mol. Biosyst. 2, 536-550.
53. Liu, J., and Coaker, G. (2008). Nuclear trafficking during plant innate immunity. Mol. Plant 1, 411-422.
54. Liu, L., McBride, K. M., and Reich, N. C. (2005). STAT3 nuclear import is independent of tyrosine phosphorylation and mediated by importin-α3. Proc. Natl. Acad. Sci. U.S.A. 102, 8150-8155.
55. Lott, K., Bhardwaj, A., Sims, P. J., and Cingolani, G. (2011). A minimal nuclear localization signal (NLS) in human phospholipid scramblase 4 that binds only the minor NLS-binding site of importin alpha1. J. Biol. Chem. 286, 28160-28169.
56. Maekawa, T., Kufer, T. A., and Schulze-Lefert, P. (2011). NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817-826.
57. Malek, S., Chen, Y., Huxford, T., and Ghosh, G. (2001). IkBβ, but not IkBα, functions as a classical cytoplasmic inhibitor of NF-κB dimers by masking both NF-κB nuclear localization sequences in resting cells. J. Biol. Chem. 276, 45225-45235.
58. Marfori, M., Lonhienne, T. G., Forwood, J. K., and Kobe, B. (2012). Structural basis of high-affinity nuclear localization signal interactions with importin-α. Traffic 13, 532-548.
59. Marfori, M., Mynott, A., Ellis, J. J., Mehdi, A. M., Saunders, N. F. W., Curmi, P. M., et al. (2011). Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim. Biophys. Acta 1813, 1562-1577.
60. Matsuura, Y., and Stewart, M. (2004). Structural basis for the assembly of a nuclear export complex. Nature 432, 872-877.
61. Meier, I., and Somers, D. E. (2011). Regulation of nucleocytoplasmic trafficking in plants. Curr. Opin. Plant Biol. 14, 538-546.
62. Meissner, T. B., Li, A., Liu, Y. J., Gagnon, E., and Kobayashi, K. S. (2012). The nucleotide-binding domain of NLRC5 is critical for nuclear import and transactivation activity. Biochem. Biophys. Res. Commun. 418, 786-791.
63. Melén, K., Fagerlund, R., Franke, J., Kohler, M., Kinnunen, L., and Julkunen, I. (2003). Importin alpha nuclear localization signal binding sites for STAT1, STAT2, and influenza A virus nucleoprotein. J. Biol. Chem. 278, 28193-28200.
64. Melén, K., Kinnunen, L., and Julkunen, I. (2001). Arginine/lysine-rich structural element is involved in interferon-induced nuclear import of STATs. J. Biol. Chem. 276, 16447-16455.
65. Merkle, T. (2011). Nucleo-cytoplasmic transport of proteins and RNA in plants. Plant Cell Rep. 30, 153-176.
66. Meyers, B. C., Lee, D. K., Vu, T. H., Tej, S. S., Edberg, S. B., Matvienko, M., et al. (2004). Arabidopsis MPSS. An online resource for quantitative expression analysis 1 [w]. Analysis 135, 801-813.
67. Miyamoto, Y., Imamoto, N., Sekimoto, T., Tachibana, T., Seki, T., Tada, S., et al. (1997). Differential modes of nuclear localization signal (NLS) recognition by three distinct classes of NLS receptors. J. Biol. Chem. 272, 26375-26381.
68. Mou, Z., Fan, W. H., Dong, X. N., and Carolina, N. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
69. Nadler, S. G., Tritschler, D., Haffar, O. K., Blake, J., Bruce, A. G., and Cleaveland, J. S. (1997). Differential expression and sequence-specific interaction of karyopherin alpha with nuclear localization sequences. J. Biol. Chem. 272, 4310-4315.
70. Nürnberger, T., Brunner, F., Kemmerling, B., and Piater, L. (2004). Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198, 249-266.
71. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., et al. (2007). The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 35, D883-D887.
72. Palma, K., Zhang, Y., and Li, X. (2005). An importin alpha homolog, MOS6, plays an important role in plant innate immunity. Curr. Biol. 15, 1129-1135.
73. Park, C. J., and Ronald, P. C. (2012). Cleavage and nuclear localization of the rice XA21 immune receptor. Nat. Commun. 3, 920.
74. Pitzschke, A., and Hirt, H. (2010). New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J. 29, 1021-1032.
75. Quensel, C., Friedrich, B., Sommer, T., Hartmann, E., and Kohler, M. (2004). In vivo analysis of importin α proteins reveals cellular proliferation inhibition and substrate specificity. Mol. Cell. Biol. 24, 10246-10255.
76. Ratan, R., Mason, D. A., Sinnot, B., Goldfarb, D. S., and Fleming, R. J. (2008). Drosophila importin alpha1 performs paralog-specific functions essential for gametogenesis. Genetics 178, 839-850.
77. Ribbeck, K., Lipowsky, G., Kent, H. M., Stewart, M., and Gorlich, D. (1998). NTF2 mediates nuclear import of Ran. EMBO J. 17, 6587-6598.
78. Riddick, G., and Macara, I. G. (2005). A systems analysis of importin-α-β mediated nuclear protein import. J. Cell Biol. 168, 1027-1038.
79. Ronald, P. C., and Beutler, B. (2010). Plant and animal sensors of conserved microbial signatures. Science 330, 1061-1064.
80. Shen, Q. H., and Schulze-Lefert, P. (2007). Rumble in the nuclear jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J. 26, 4293-4301.
81. Shen, Q. H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., et al. (2007). Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315, 1098-1103.
82. Slootweg, E., Roosien, J., Spiridon, L. N., Petrescu, A. J., Tameling, W., Joosten, M., et al. (2010). Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell 22, 4195-4115.
83. Smith, A., Brownawell, A., and Macara, I. G. (1998). Nuclear import of Ran is mediated by the transport factor NTF2. Curr. Biol. 8, 1403-1406.
84. Spilianakis, C., Papamatheakis, J., and Kretsovali, A. (2000). Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes. Mol. Cell. Biol. 20, 8489-8498.
85. Stewart, M. (2007). Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 8, 195-208.
86. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al. (2008). Plant immunity requires conformational charges of NPR1 via S-nitrosylation and thioredoxins. Science 952, 952-956.
87. Tameling, W. I. L., Nooijen, C., Ludwig, N., Boter, M., Slootweg, E., Goverse, A., et al. (2010). RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell 22, 4176-4194.
88. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599.
89. Terry, L. J., Shows, E. B., and Wente, S. R. (2007). Crossing the nuclear envelope: hierarchical regulation of nucleocytoplasmic transport. Science 318, 1412-1416.
90. Timney, B. L., Tetenbaum-Novatt, J., Agate, D. S., Williams, R., Zhang, W., Chait, B. T., et al. (2006). Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J. Cell Biol. 175, 579-593.
91. Tsuji, L., Takumi, T., Imamoto, N., and Yoneda, Y. (1997). Identification of novel homologues of mouse importin α, the α subunit of the nuclear pore-targeting complex, and their tissue-specific expression. FEBS Lett. 416, 30-34.
92. Wiermer, M., Feys, B. J., and Parker, J. E. (2005). Plant immunity: the EDS1 regulatory node. Curr. Opin. Plant Biol. 8, 383-389.
93. Wirthmueller, L., Zhang, Y., Jones, J. D. G., and Parker, J. E. (2007). Nuclear accumulation of the Arabidopsisimmune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr. Biol. 17, 2023-2029.
94. Yano, R., Oakes, M., Yamaghishi, M., Dodd, J. A., and Nomura, M. (1992). Cloning and characterization of SRPI, a suppressor of temperature-sensitive RNA polymerase I mutations, in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 5640-5651.
95. Yasuhara, N., Shibazaki, N., Tanaka, S., Nagai, M., Kamikawa, Y., Oe, S., et al. (2007). Triggering neural differentiation of ES cells by subtype switching of importin-alpha. Nat. Cell Biol. 9, 72-79.
96. Zhu, Y., Qian, W., and Hua, J. (2010). Temperature modulates plant defense responses through NB-LRR proteins. PLoS Pathog. 6:e1000844. doi: 10.1371/journal.ppat.1000844