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http://dx.doi.org/10.5423/PPJ.RW.08.2015.0150

Heat Shock Proteins: A Review of the Molecular Chaperones for Plant Immunity  

Park, Chang-Jin (Department of Plant Biotechnology and PERI, Sejong University)
Seo, Young-Su (Department of Microbiology, Pusan National University)
Publication Information
The Plant Pathology Journal / v.31, no.4, 2015 , pp. 323-333 More about this Journal
Abstract
As sessile organisms, plants are exposed to persistently changing stresses and have to be able to interpret and respond to them. The stresses, drought, salinity, chemicals, cold and hot temperatures, and various pathogen attacks have interconnected effects on plants, resulting in the disruption of protein homeostasis. Maintenance of proteins in their functional native conformations and preventing aggregation of non-native proteins are important for cell survival under stress. Heat shock proteins (HSPs) functioning as molecular chaperones are the key components responsible for protein folding, assembly, translocation, and degradation under stress conditions and in many normal cellular processes. Plants respond to pathogen invasion using two different innate immune responses mediated by pattern recognition receptors (PRRs) or resistance (R) proteins. HSPs play an indispensable role as molecular chaperones in the quality control of plasma membrane-resident PRRs and intracellular R proteins against potential invaders. Here, we specifically discuss the functional involvement of cytosolic and endoplasmic reticulum (ER) HSPs/chaperones in plant immunity to obtain an integrated understanding of the immune responses in plant cells.
Keywords
chaperones; heat shock proteins; plant immunity;
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1 Anderson, S. L., Shen, T., Lou J, Xing, L., Blachere, N. E., Srivastava, P. K. and Rubin, B. Y. 1994. The endoplasmic reticular heat shock protein gp96 is transcriptionally upregulated in interferon-treated cells. J. Exp. Med. 180:1565-1569.   DOI
2 Bao, F., Huang, X., Zhu, C., Zhang, X., Li, X. and Yang, S. 2014. Arabidopsis HSP90 protein modulates RPP4-mediated temperature-dependent cell death and defense responses. New Phytol. 202:1320-1334.   DOI
3 Bhattarai, K. K., Li, Q., Liu, Y., Dinesh-Kumar, S. P. and Kaloshian, I. 2007. The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol. 144:312-323.   DOI
4 Boevink, P. and Oparka, K. J. 2005. Virus-host interactions during movement processes. Plant Physiol. 138:1815-1821.   DOI
5 Bosl, B., Grimminger, V. and Walter, S. 2006. The molecular chaperone Hsp104--a molecular machine for protein disaggregation. J. Struct. Biol. 156:139-148.   DOI
6 Boston, R. S., Viitanen, P. V. and Vierling, E. 1996. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32:191-222.   DOI
7 Boter, M., Amigues, B., Peart, J., Breuer, C., Kadota, Y., Casais, C., Moore, G., Kleanthous, C., Ochsenbein, F., Shirasu, K. and Guerois, R. 2007. Structural and functional analysis of SGT1 reveals that its interaction with HSP90 is required for the accumulation of Rx, an R protein involved in plant immunity. Plant Cell 19:3791-3804.   DOI
8 Breiman, A. 2014. Plant Hsp90 and its co-chaperones. Curr. Protein Pept. Sci. 15:232-244.   DOI
9 Cai, B., Tomida, A., Mikami, K., Nagata, K. and Tsuruo, T. 1998. Down-regulation of epidermal growth factor receptor-signaling pathway by binding of GRP78/BiP to the receptor under glucose-starved stress conditions. J. Cell. Physiol. 177:282-288.   DOI
10 Carvalho, H. H., Silva, P. A., Mendes, G. C., Brustolini, O. J., Pimenta, M. R., Gouveia, B. C., Valente, M. A., Ramos, H. J., Soares-Ramos, J. R. and Fontes, E. P. 2014. The endoplasmic reticulum binding protein BiP displays dual function in modulating cell death events. Plant Physiol. 164:654-670.   DOI
11 Catlett, M. G. and Kaplan, K. B. 2006. Sgt1p is a unique co-chaperone that acts as a client adaptor to link Hsp90 to Skp1p. J. Biol. Chem. 281:33739-33748.   DOI
12 Chisholm, S. T., Coaker, G., Day, B. and Staskawicz, B. J. 2006. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803-814.   DOI
13 Chen, L., Hamada, S., Fujiwara, M., Zhu, T., Thao, N. P., Wong, H. L., Krishna, P., Ueda, T., Kaku, H., Shibuya, N., Kawasaki, T. and Shimamoto, K. 2010. The Hop/Sti1-Hsp90 chaperone complex facilitates the maturation and transport of a PAMP receptor in rice innate immunity. Cell Host Microbe 7:185-196.   DOI
14 Chen, W., Syldath, U., Bellmann, K., Burkart, V. and Kolb, H. 1999. Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J. Immunol. 162:3212-3219.
15 Chen, Z., Zhou, T., Wu, X., Hong, Y., Fan, Z. and Li, H. 2008. Influence of cytoplasmic heat shock protein 70 on viral infection of Nicotiana benthamiana. Mol. Plant Pathol. 9:809-817.   DOI
16 Dodds, P. N. and Rathjen, J. P. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548.
17 Eichmann, R. and Schafer, P. 2012. The endoplasmic reticulum in plant immunity and cell death. Front. Plant Sci. 3:200.
18 Fleck, M. W. 2006. Glutamate receptors and endoplasmic reticulum quality control: looking beneath the surface. Neuroscientist 12:232-244.   DOI
19 Fukuda, S., Sumii, M., Masuda, Y., Takahashi, M., Koike, N., Teishima, J., Yasumoto, H., Itamoto, T., Asahara, T., Dohi, K. and Kamiya, K. 2001. Murine and human SDF2L1 is an endoplasmic reticulum stress-inducible gene and encodes a new member of the Pmt/rt protein family. Biochem. Biophys. Res. Commun. 280:407-414.   DOI
20 Gorovits, R., Moshe, A., Ghanim, M. and Czosnek, H. 2013. Recruitment of the host plant heat shock protein 70 by Tomato yellow leaf curl virus coat protein is required for virus infection. PLoS One 8:e70280.   DOI
21 Guo, B. and Li, Z. 2014. Endoplasmic reticulum stress in hepatic steatosis and inflammatory bowel diseases. Front. Genet. 5:242.
22 Guo, F. and Snapp, E. L. 2013. ERdj3 regulates BiP occupancy in living cells. J. Cell Sci. 126:1429-1439.   DOI
23 Gupta, D. and Tuteja, N. 2011. Chaperones and foldases in endoplasmic reticulum stress signaling in plants. Plant Signal Behav. 6:232-236.   DOI
24 Gupta, S. C., Sharma, A., Mishra, M., Mishra, R. K. and Chowdhuri, D. K. 2010. Heat shock proteins in toxicology: how close and how far? Life Sci. 86:377-384.   DOI
25 Hafren, A., Hofius, D., Ronnholm, G., Sonnewald, U. and Makinen, K. 2010. HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant cell 22:523-535.   DOI
26 Haweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S. and von Schaewen, A. 2010. Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285:4629-4636.   DOI
27 Hofius, D., Maier, A. T., Dietrich, C., Jungkunz, I., Bornke, F., Maiss, E. and Sonnewald, U. 2007. Capsid protein-mediated recruitment of host DnaJ-like proteins is required for Potato virus Y infection in tobacco plants. J. Virol. 81:11870-11880.   DOI
28 Hong, S. W. and Vierling, E. 2001. Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J. 27:25-35.   DOI
29 Hubert, D. A., He, Y., McNulty, B. C., Tornero, P. and Dangl, J. L. 2009. Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc. Natl. Acad. Sci. USA 106:9556-9563.   DOI
30 Hong, Z., Jin, H., Tzfira, T. and Li, J. 2008. Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:3418-3429.   DOI
31 Hubert, D. A., Tornero, P., Belkhadir, Y., Krishna, P., Takahashi, A., Shirasu, K. and Dangl, J. L. 2003. Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J. 22:5679-5689.   DOI
32 Huttner, S. and Strasser, R. 2012. Endoplasmic reticulum-associated degradation of glycoproteins in plants. Front. Plant Sci. 3:67.
33 Jin, H., Yan, Z., Nam, K. H. and Li, J. 2007. Allele-specific suppression of a defective brassinosteroid receptor reveals a physiological role of UGGT in ER quality control. Mol. Cell 26:821-830.   DOI
34 Kadota, Y. and Shirasu, K. 2012. The HSP90 complex of plants. Biochim. Biophys. Acta 1823:689-697.   DOI
35 Kampinga, H. H. and Craig, E. A. 2010. The HSP70 chaperone machinery: J proteins as drivers of functional specificity. Nat. Rev. 11:579-592.   DOI
36 Kanzaki, H., Saitoh, H., Ito, A., Fujisawa, S., Kamoun, S., Katou, S., Yoshioka, H. and Terauchi, R. 2003. Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4:383-391.   DOI
37 Kawai, T. and Akira, S. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11:373-384.   DOI
38 Kleizen, B. and Braakman, I. 2004. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 16:343-349.   DOI
39 Kim, H. J., Hwang, N. R. and Lee, K. J. 2007. Heat shock responses for understanding diseases of protein denaturation. Mol. Cells 23:123-131.
40 Kim, N. H. and Hwang, B. K. 2015. Pepper heat shock protein 70a interacts with the type III effector AvrBsT and triggers plant cell death and immunity. Plant Physiol. 167:307-322.   DOI
41 Kotak, S., Larkindale, J., Lee, U., von Koskull-Doring, P., Vierling, E. and Scharf, K. D. 2007. Complexity of the heat stress response in plants. Curr. Opin. Plant Biol. 10:310-316.   DOI
42 Lee, A. S. 2001. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 26:504-510.   DOI
43 Li, J., Zhao-Hui, C., Batoux, M., Nekrasov, V., Roux, M., Chinchilla, D., Zipfel, C. and Jones, J. D. 2009. Specific ER quality control components required for biogenesis of the plant innate immune receptor EFR. Proc. Natl. Acad. Sci. USA 106:15973-15978.   DOI
44 Li, Z., Menoret, A. and Srivastava, P. 2002. Roles of heat-shock proteins in antigen presentation and cross-presentation. Curr. Opin. Immunol. 14:45-51.   DOI
45 Liberek, K., Lewandowska, A. and Zietkiewicz, S. 2008. Chaperones in control of protein disaggregation. EMBO J. 27:328-335.   DOI
46 Liebrand, T. W., Smit, P., Abd-El-Haliem, A., de Jonge, R., Cordewener, J. H., America, A. H., Sklenar, J., Jones, A. M., Robatzek, S., Thomma, B. P., Tameling, W. I. and Joosten, M. H. 2012. Endoplasmic reticulum-quality control chaperones facilitate the biogenesis of Cf receptor-like proteins involved in pathogen resistance of tomato. Plant Physiol. 159:1819-1833.   DOI
47 Liu, B. 2014. Heat Shock Protein gp96 as an Immune Chaperone of Inflammation and Cancer. Aust. J. Clin. Immunol. 1:1014.
48 Lin, M. Y., Chai, K. H., Ko, S. S., Kuang, L. Y., Lur, H. S. and Charng, Y. Y. 2014. A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol. 164:2045-2053.   DOI
49 Lindquist, S. 1986. The heat-shock response. Annu. Rev. Biochem. 55:1151-1191.   DOI
50 Lindquist, S. and Craig, E. A. 1988. The heat-shock proteins. Annu. Rev. Genet. 22:631-677.   DOI
51 Liu, B. and Li, Z. 2008. Endoplasmic reticulum HSP90b1 (gp96, grp94) optimizes B-cell function via chaperoning integrin and TLR but not immunoglobulin. Blood 112:1223-1230.   DOI
52 Liu, E. S. and Lee, A. S. 1991. Common sets of nuclear factors binding to the conserved promoter sequence motif of two coordinately regulated ER protein genes, GRP78 and GRP94. Nucleic Acids Res. 19:5425-5431.   DOI
53 Liu, J. X. and Howell, S. H. 2010. Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22:2930-2942.   DOI
54 Liu, J. Z. and Whitham, S. A. 2013. Overexpression of a soybean nuclear localized type-III DnaJ domain-containing HSP40 reveals its roles in cell death and disease resistance. Plant J. 74:110-121.   DOI
55 Liu, Y., Burch-Smith, T., Schiff, M., Feng, S. and Dinesh-Kumar, S. P. 2004. Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 279:2101-2108.   DOI
56 Matsumiya, T., Imaizumi, T., Yoshida, H., Satoh, K., Topham, M. K. and Stafforini, D. M. 2009. The levels of retinoic acidinducible gene I are regulated by heat shock protein 90-alpha. J. Immunol. 182:2717-2725.   DOI
57 Lu, R., Malcuit, I., Moffett, P., Ruiz, M. T., Peart, J., Wu, A. J., Rathjen, J. P., Bendahmane, A., Day, L. and Baulcombe, D. C. 2003. High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J. 22:5690-5699.   DOI
58 Lu, X., Tintor, N., Mentzel, T., Kombrink, E., Boller, T., Robatzek, S., Schulze-Lefert, P. and Saijo, Y. 2009. Uncoupling of sustained MAMP receptor signaling from early outputs in an Arabidopsis endoplasmic reticulum glucosidase II allele. Proc. Natl. Acad. Sci. USA 106:22522-22527.   DOI
59 Maimbo, M., Ohnishi, K., Hikichi, Y., Yoshioka, H. and Kiba, A. 2007. Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum. Plant Physiol. 145:1588-1599.   DOI
60 Meunier, L., Usherwood, Y. K., Chung, K. T. and Hendershot, L. M. 2002. A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins. Mol. Biol. Cell 13:4456-4469.   DOI
61 Molinari, M. and Helenius, A. 2000. Chaperone selection during glycoprotein translocation into the endoplasmic reticulum. Science 288:331-333.   DOI
62 Monaghan, J. and Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15:349-357.   DOI
63 Ohashi, K., Burkart, V., Flohe, S. and Kolb, H. 2000. Cutting edge: heat shock protein 60 is a putative endogenous ligand of the toll-like receptor-4 complex. J. Immunol. 164:558-561.   DOI
64 Moreno, A. A., Mukhtar, M. S., Blanco, F., Boatwright, J. L., Moreno, I., Jordan, M. R., Chen, Y., Brandizzi, F., Dong, X., Orellana, A. and Pajerowska-Mukhtar, K. M. 2012. IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One 7:e31944.   DOI
65 Nekrasov, V., Li, J., Batoux, M., Roux, M., Chu, Z. H., Lacombe, S., Rougon, A., Bittel, P., Kiss-Papp, M., Chinchilla, D., van Esse, H. P., Jorda, L., Schwessinger, B., Nicaise, V., Thomma, B. P., Molina, A., Jones, J. D. and Zipfel, C. 2009. Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J. 28:3428-3438.   DOI
66 Nguyen, N., Francoeur, N., Chartrand, V., Klarskov, K., Guillemette, G. and Boulay, G. 2009. Insulin promotes the association of heat shock protein 90 with the inositol 1,4,5-trisphosphate receptor to dampen its $Ca^{2+}$ release activity. Endocrinology 150:2190-2196.   DOI
67 Ohta, M. and Takaiwa, F. 2014. Emerging features of ER resident J-proteins in plants. Plant Signal Behav. 9:e28194.   DOI
68 Park, C. J., Bart, R., Chern, M., Canlas, P. E., Bai, W. and Ronald, P. C. 2010. Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One 5(2):e9262.   DOI
69 Park, C. J., Sharma, R., Lefebvre, B., Canlas, P. E. and Ronald, P. C. 2013. The endoplasmic reticulum-quality control component SDF2 is essential for XA21-mediated immunity in rice. Plant Sci. 210:53-60.   DOI
70 Park, C. J., Song, M. Y., Kim, C. Y., Jeon, J. S. and Ronald, P. C. 2014. Rice BiP3 regulates immunity mediated by the PRRs XA3 and XA21 but not immunity mediated by the NB-LRR protein, Pi5. Biochem. Biophys. Res. Commun. 448:70-75.   DOI
71 Qiu, X. B., Shao, Y. M., Miao, S. and Wang, L. 2006. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol. Life Sci. 63:2560-2570.   DOI
72 Queitsch, C., Hong, S. W., Vierling, E. and Lindquist, S. 2000. Heat shock protein 101 plays a crucial role in thermotolerance in Arabidopsis. Plant Cell 12:479-492.   DOI
73 Queitsch, C., Sangster, T. A. and Lindquist, S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417:618-624.   DOI
74 Ramakrishnan, M., Tugizov, S., Pereira, L. and Lee, A. S. 1995. Conformation-defective herpes simplex virus 1 glycoprotein B activates the promoter of the grp94 gene that codes for the 94-kD stress protein in the endoplasmic reticulum. DNA Cell Biol. 14:373-384.   DOI
75 Ritossa, F. 1962. A new puffing pattern induced by temperature shock and DNP in drosophila. Experientia 18:571-573.   DOI
76 Rug, M. and Maier, A. G. 2011. The heat shock protein 40 family of the malaria parasite Plasmodium falciparum. IUBMB Life 63:1081-1086.   DOI
77 Saijo, Y. 2010. ER quality control of immune receptors and regulators in plants. Cell. Microbiol. 12:716-724.   DOI
78 Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Haweker, H., Dong, X., Robatzek, S. and Schulze-Lefert, P. 2009. Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28:3439-3449.   DOI
79 Sangster, T. A. and Queitsch, C. 2005. The HSP90 chaperone complex, an emerging force in plant development and phenotypic plasticity. Curr. Opin. Plant Biol. 8:86-92.   DOI
80 Sangster, T. A., Bahrami, A., Wilczek, A., Watanabe, E., Schellenberg, K., McLellan, C., Kelley, A., Kong, S. W., Queitsch, C. and Lindquist, S. 2007. Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2:e648.   DOI
81 Schott, A., Ravaud, S., Keller, S., Radzimanowski, J., Viotti, C., Hillmer, S., Sinning, I. and Strahl, S. 2010. Arabidopsis stromal-derived Factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum. J. Biol. Chem. 285:18113-18121.   DOI
82 Seo, Y. S., Lee, S. K., Song, M. Y., Suh, J. P., Hahn, T. R., Ronald, P. and Jeon, J. S. 2008. The HSP90-SGT1-RAR1 molecular chaperone complex: A core modulator in plant immunity. J. Plant Biol. 51:1-10.   DOI
83 Shafikova, T. N., Omelichkina, Y. V., Soldatenko, A. S., Enikeev, A. G., Kopytina, T. V., Rusaleva, T. M. and Volkova, O. D. 2013. Tobacco cell cultures transformed by the hsp101 gene exhibit an increased resistance to Clavibacter michiganensis ssp. sepedonicus. Doklady Biol. Sci. 450:165-167.   DOI
84 Shen, Y. and Hendershot, L. M. 2005. ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP's interactions with unfolded substrates. Mol. Biol. Cell 16:40-50.   DOI
85 Shirasu, K. 2009. The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu. Rev. Plant Biol. 60:139-164.   DOI
86 Shirasu, K. and Schulze-Lefert, P. 2003. Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci. 8:252-258.   DOI
87 Soellick, T., Uhrig, J. F., Bucher, G. L., Kellmann, J. W. and Schreier, P. H. 2000. The movement protein NSm of Tomato spotted wilt tospovirus (TSWV): RNA binding, interaction with the TSWV N protein, and identification of interacting plant proteins. Proc. Natl. Acad. Sci. USA 97:2373-2378.   DOI
88 Shiu, R. P., Pouyssegur, J. and Pastan, I. 1977. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc. Natl. Acad. Sci. USA 74:3840-3844.   DOI
89 Simons, G., Groenendijk, J., Wijbrandi, J., Reijans, M., Groenen, J., Diergaarde, P., Van der Lee, T., Bleeker, M., Onstenk, J., de Both, M., Haring, M., Mes, J., Cornelissen, B., Zabeau, M. and Vos, P. 1998. Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055-1068.   DOI
90 Sitia, R. and Braakman, I. 2003. Quality control in the endoplasmic reticulum protein factory. Nature 426:891-894.   DOI
91 Takahashi, A., Casais, C., Ichimura, K. and Shirasu, K. 2003. HSP90 interacts with RAR1 and SGT1 and is essential for RPS2-mediated disease resistance in Arabidopsis. Proc. Natl. Acad. Sci. USA 100:11777-11782.   DOI
92 Te, J., Jia, L., Rogers, J., Miller, A. and Hartson, S. D. 2007. Novel subunits of the mammalian Hsp90 signal transduction chaperone. J. Proteome Res. 6:1963-1973.   DOI
93 Tsan, M. F. and Gao, B. 2009. Heat shock proteins and immune system. J. Leukoc. Biol. 85:905-910.   DOI
94 Vabulas, R. M., Ahmad-Nejad, P., da Costa, C., Miethke, T., Kirschning, C. J., Hacker, H. and Wagner, H. 2001. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276:31332-31339.   DOI
95 Vandenberghe, W., Nicoll, R. A. and Bredt, D. S. 2005. Interaction with the unfolded protein response reveals a role for stargazin in biosynthetic AMPA receptor transport. J. Neurosci. 25:1095-1102.   DOI
96 van Eden, W., Spiering, R., Broere, F. and van der Zee, R. 2012. A case of mistaken identity: HSPs are no DAMPs but DAMPERs. Cell Stress and Chaperones 17:281-292.   DOI
97 van Montfort, R. L., Basha, E., Friedrich, K. L., Slingsby, C. and Vierling, E. 2001. Crystal structure and assembly of a eukaryotic small heat shock protein. Nat. Struct. Biol. 8:1025-1030.   DOI
98 Van Ooijen, G., Lukasik, E., Van Den Burg, H. A., Vossen, J. H., Cornelissen, B. J. and Takken, F. L. 2010. The small heat shock protein 20 RSI2 interacts with and is required for stability and function of tomato resistance protein I-2. Plant J. 63:563-572.   DOI
99 Verchot, J. 2012. Cellular chaperones and folding enzymes are vital contributors to membrane bound replication and movement complexes during plant RNA virus infection. Front. Plant Sci. 3:275.
100 Vierling, E. 1991. The Roles of Heat Shock Proteins in Plants. Annu. Rev. Plant Physiol. & Plant Mol. Biol. 42:579-620.   DOI
101 Vitale, A. and Boston, R. S. 2008. Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 9:1581-1588.   DOI
102 Wallin, R. P., Lundqvist, A., More, S. H., von Bonin, A., Kiessling, R. and Ljunggren, H. G. 2002. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23:130-135.   DOI
103 Wang, D., Weaver, N. D, Kesarwani, M. and Dong, X. 2005. Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036-1040.   DOI
104 Xu, G., Li, S., Xie, K., Zhang, Q., Wang, Y., Tang, Y., Liu, D., Hong, Y., He, C. and Liu, Y. 2012a. Plant ERD2-like proteins function as endoplasmic reticulum luminal protein receptors and participate in programmed cell death during innate immunity. Plant J. 72:57-69.   DOI
105 Wang, W., Vinocur, B., Shoseyov, O. and Altman, A. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 9:244-252.   DOI
106 Whitley, D., Goldberg, S. P. and Jordan, W. D. 1999. Heat shock proteins: a review of the molecular chaperones. J. Vasc. Sur. 29:748-751.   DOI
107 Williams, J. H. and Ireland, H. E. 2008. Sensing danger--Hsp72 and HMGB1 as candidate signals. J. Leukoc. Biol. 83:489-492.   DOI
108 Xu, Z. S., Li, Z. Y., Chen, Y., Chen, M., Li, L. C. and Ma, Y. Z. 2012b. Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int. J. Mol. Sci. 13:15706-15723.   DOI
109 Yang, Y., Liu, B., Dai, J., Srivastava, P. K., Zammit, D. J., Lefrancois, L. and Li, Z. 2007. Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 26:215-226.   DOI
110 Ye, C., Dickman, M. B., Whitham, S. A., Payton, M. and Verchot, J. 2011. The unfolded protein response is triggered by a plant viral movement protein. Plant Physiol. 156:741-755.   DOI
111 Zhang, Y., Dorey, S., Swiderski, M. and Jones, J. D. 2004. Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J. 40:213-224.   DOI