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Hsp70 in Fungi: Evolution, Function and Vaccine Candidate

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HSP70 in Human Diseases and Disorders

Part of the book series: Heat Shock Proteins ((HESP,volume 14))

Abstract

In fungal system, Hsp70 protein being highly conserved in nature has played a major role in various stress conditions. Genes encoding for Hsp70 proteins in fungi are highly conserved. Hsp70 protein performs chaperone dependent or independent function, essential for growth and morphogenesis of fungi. Functional distinction of Hsp70 protein conjointly depends on the prevalence of Hsp70 in numerous cellular compartments. Fungal Hsp70 protein is involved in protein aggregation, folding as well as in degradation of nascent polypeptide. Additionally, Hsp70 protein has a vital role in the formation of prions in case of yeasts. Fungi showed expression of hsp70 mRNA during interaction with plant. Also, fungal hsp70 showed expression in human during various infections, and may provide lead as a potential bio-marker for disease conditions. This chapter summarizes our present knowledge on fungal Hsp70 proteins and their role in morphogenesis, stress responses and a potential candidate for vaccine.

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Abbreviations

AmB:

Amphotericin B

CFTR:

cystic fibrosis transmembrane conductance regulator

Hsp:

heat shock protein

kDa:

kilo Dalton

NEF:

nucleotide exchange factor

References

  • Adams, C. C., & Gross, D. S. (1991). The yeast heat shock response is induced by conversion of cells to spheroplasts and by potent transcriptional inhibitors. Journal of Bacteriology, 173, 7429–7435.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Allen, K. D., Wegrzyn, R. D., Chernova, T. A., Müller, S., Newnam, G. P., Winslett, P. A., Wittich, K. B., Wilkinson, K. D., & Chernoff, Y. O. (2005). Hsp70 chaperones as modulators of prion life cycle. Genetics, 169, 1227–1242.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Allendoerfer, R., Maresca, B., & Deepe, G. (1996). Cellular immune responses to recombinant heat shock protein 70 from Histoplasma capsulatum. Infection and Immunity, 64, 4123–4128.

    Google Scholar 

  • Andréasson, C., Rampelt, H., Fiaux, J., Druffel-Augustin, S., & Bukau, B. (2010). The endoplasmic reticulum Grp170 acts as a nucleotide exchange factor of Hsp70 via a mechanism similar to that of the cytosolic Hsp110. The Journal of Biological Chemistry, 285, 12445–12453.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Antelo, J. M., Arce, F., Parajo, M., Rodriguez, P., & Varela, A. (1992). Disproportionation kinetics of NaCl isopropylamine and NaCl isopropylamine. International Journal of Chemical Kinetics, 24, 991–997.

    Google Scholar 

  • Azad, P., Zhou, D., Russo, E., & Haddad, G. G. (2009). Distinct mechanisms underlying tolerance to intermittent and constant hypoxia in Drosophila melanogaster. PLoS One, 4, e5371.

    Google Scholar 

  • Banerjee, D., Martin, N., Nandi, S., Shukla, S., Dominguez, A., Mukhopadhyay, G., & Prasad, R. (2007). A genome-wide steroid response study of the major human fungal pathogen Candida albicans. Mycopathologia, 164, 1–17.

    Google Scholar 

  • Blatzer, M., Blum, G., Jukic, E., Posch, W., Gruber, P., Nagl, M., Binder, U., Maurer, E., Sarg, B., & Lindner, H. (2015). Blocking Hsp70 enhances the efficiency of amphotericin B treatment against resistant Aspergillus terreus strains. Antimicrobial Agents and Chemotherapy, 59, 3778–3788.

    Google Scholar 

  • Boorstein, W. R., Ziegelhoffer, T., & Craig, E. A. (1994). Molecular evolution of the HSP70 multigene family. Journal of Molecular Evolution, 38, 1–17.

    Article  PubMed  CAS  Google Scholar 

  • Brand, A. (2011). Hyphal growth in human fungal pathogens and its role in virulence. International Journal of Microbiology, 2012, 1–11.

    Article  Google Scholar 

  • Brodsky, J. L., Lawrence, J. G., & Caplan, A. J. (1998). Mutations in the cytosolic DnaJ homologue, YDJ1, delay and compromise the efficient translation of heterologous proteins in yeast. Biochemistry, 37, 18045–18055.

    Article  PubMed  CAS  Google Scholar 

  • Bromuro, C., La Valle, R., Sandini, S., Urbani, F., Ausiello, C. M., Morelli, L., Féd’ostiani, C., Romani, L., & Cassone, A. (1998). A 70-kilodalton recombinant heat shock protein of Candida albicans is highly immunogenic and enhances systemic murine candidiasis. Infection and Immunity, 66, 2154–2162.

    Google Scholar 

  • Bukau, B., & Horwich, A. L. (1998). The Hsp70 and Hsp60 chaperone machines. Cell, 92, 351–366.

    Article  PubMed  CAS  Google Scholar 

  • Burnie, J. P., Carter, T. L., Hodgetts, S. J., & Matthews, R. C. (2006). Fungal heat shock proteins in human disease. FEMS Microbiology Reviews, 30, 53–88.

    Article  PubMed  CAS  Google Scholar 

  • Burt, E. T., Daly, R., Hoganson, D., Tsirulnikov, Y., Essmann, M., & Larsen, B. (2003). Isolation and partial characterization of Hsp90 from Candida albicans. Annals of Clinical and Laboratory Science, 33, 86–93.

    Google Scholar 

  • Caddick, M. X., Brownlee, A. G., & Arst, H. N. (1986). Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Molecular & General Genetics, 203, 346–353.

    Google Scholar 

  • Caruso, M., Sacco, M., Medoff, G., & Maresca, B. (1987). Heat shock 70 gene is differentially expressed in Histoplasma capsulatum strains with different levels of thermotolerance and pathogenicity. Molecular Microbiology, 1, 151–158.

    Google Scholar 

  • ÄŒernila, B., ÄŒreÅ¡nar, B., & Breskvar, K. (2003). Molecular characterization of genes encoding cytosolic Hsp70s in the zygomycete fungus Rhizopus nigricans. Cell Stress & Chaperones, 8, 317–328.

    Google Scholar 

  • Chakraborty, B., Ouimet, P., Sreenivasan, G., Curle, C., & Kapoor, M. (1995). Sequence repeat-induced disruption of the major heat-inducible HSP70 gene of Neurospora crassa. Current Genetics, 29, 18–26.

    Google Scholar 

  • Chauhan, N. M., Washe, A. P., & Minota, T. (2016). Fungal infection and aflatoxin contamination in maize collected from Gedeo zone, Ethiopia. SpringerPlus, 5, 753.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheetham, M. E., & Caplan, A. J. (1998). Structure, function and evolution of DnaJ: Conservation and adaptation of chaperone function. Cell Stress & Chaperones, 3, 28.

    Article  CAS  Google Scholar 

  • Chen, Z., Ribeiro, A., Silva, M., Santos, P., Guerra-Guimarães, L., Gouveia, M., Fernandez, D., & Rodrigues, C. (2003). Heat shock-induced susceptibility of green coffee leaves and berries to Colletotrichum gloeosporioides and its association to PR and hsp70 gene expression. Physiological and Molecular Plant Pathology, 63, 181–190.

    Google Scholar 

  • Chun, C. D., Liu, O. W., & Madhani, H. D. (2007). A link between virulence and homeostatic responses to hypoxia during infection by the human fungal pathogen Cryptococcus neoformans. PLoS Pathogens, 3, e22.

    Google Scholar 

  • Cleare, L. G., Miranda, D. Z., & Nosanchuk, J. D. (2017). Heat shock proteins in Histoplasmaand Paracoccidioides. Clinical and Vaccine Immunology, 24, 00221–00217.

    Google Scholar 

  • Clemons, K. V., Shankar, J., & Stevens, D. A. (2010). Mycologic endocrinology. In M. Lyte & P. P. E. Freestone (Eds.), The microbial endocrinology (pp. 269–290). New York: Springer.

    Chapter  Google Scholar 

  • Craig, E. A., & Marszalek, J. (2011). Hsp70 chaperones. In The encyclopedia of life sciences (ELS) (pp. 1–8). Chichester: Wiley.

    Google Scholar 

  • Craig, E. A., Gambill, B. D., & Nelson, R. J. (1993). Heat shock proteins: molecular chaperones of protein biogenesis. Microbiological Reviews, 57, 402–414.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Craig, E., Ziegelhoffer, T., Nelson, J., Laloraya, S., & Halladay, J. (1995). Complex multigene family of functionally distinct Hsp70s of yeast. Cold Spring Harbor Symposia on Quantitative Biology, 60, 441–449.

    Article  PubMed  CAS  Google Scholar 

  • Craig, E. A., Eisenman, H. C., & Hundley, H. A. (2003). Ribosome-tethered molecular chaperones: The first line of defense against protein misfolding? Current Opinion in Microbiology, 6, 157–162.

    Article  PubMed  CAS  Google Scholar 

  • Craig, E., Huang, P., Aron, R., & Andrew, A. (2006). The diverse roles of J-proteins, the obligate Hsp70 co-chaperone. In N. Brend & G. Thomas (Eds.), The reviews of physiology, biochemistry and pharmacology (Vol. 156, pp. 1–21). Berlin/Heidelberg: Springer.

    Google Scholar 

  • Cutler, J. E., Deepe, G. S., Jr., & Klein, B. S. (2007). Advances in combating fungal diseases: Vaccines on the threshold. Nature Reviews. Microbiology, 5, 13.

    Article  PubMed  CAS  Google Scholar 

  • Da Silva, S. P., Borges-Walmsley, M. I., Pereira, I. S., Soares, C. M. A., Walmsley, A. R., & Felipe, M. S. S. (1999). Differential expression of an hsp70 gene during transition from the mycelial to the infective yeast form of the human pathogenic fungus Paracoccidioides brasiliensis. Molecular Microbiology, 31, 1039–1050.

    Google Scholar 

  • Damelin, L., Vokes, S., Whitcutt, J., Damelin, S., & Alexander, J. (2000). Hormesis: A stress response in cells exposed to low levels of heavy metals. Human & Experimental Toxicology, 19, 420–430.

    Article  CAS  Google Scholar 

  • Daugaard, M., Rohde, M., & Jäättelä, M. (2007). The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Letters, 581, 3702–3710.

    Article  CAS  PubMed  Google Scholar 

  • De Arruda Grossklaus, D., Bailão, A. M., Rezende, T. C. V., Borges, C. L., de Oliveira, M. A. P., Parente, J. A., & de Almeida, S. C. M. (2013). Response to oxidative stress in Paracoccidioides yeast cells as determined by proteomic analysis. Microbes and Infection, 15, 347–364.

    Article  PubMed  CAS  Google Scholar 

  • De Castro Georg, R., & Gomes, S. L. (2007). Comparative expression analysis of members of the Hsp70 family in the chytridiomycete Blastocladiella emersonii. Gene, 386, 24–34.

    Google Scholar 

  • Deepe, G. S., Jr., & Gibbons, R. S. (2002). Cellular and molecular regulation of vaccination with heat shock protein 60 from Histoplasma capsulatum. Infection and Immunity, 70, 3759–3767.

    Google Scholar 

  • Dix, N. J. (2012). The mycelium and substrates for growth. In Springer Science & Business Media & J. Dix Neville (Eds.), The fungal ecology (pp. 12–38). Dordrecht: Springer.

    Google Scholar 

  • Easton, D. P., Kaneko, Y., & Subjeck, J. R. (2000). The Hsp110 and Grp170 stress proteins: newly recognized relatives of the Hsp70s. Cell Stress & Chaperones, 5, 276–290.

    Article  CAS  Google Scholar 

  • Eroles, P., Sentandreu, M., Elorza, M. V., & Sentandreu, R. (1995). Cloning of a DNA fragment encoding part of a 70-kDa heat shock protein of Candida albicans. FEMS Microbiology Letters, 128, 95–100.

    Google Scholar 

  • Ferreira-Nozawa, M. S., Silveira, H. C., Ono, C. J., Fachin, A. L., Rossi, A., & Martinez-Rossi, N. M. (2006). The pH signaling transcription factor PacC mediates the growth of Trichophyton rubrum on human nail in vitro. Medical Mycology, 44, 641–645.

    Google Scholar 

  • Fracella, F., Scholle, C., Kallies, A., Häfker, T., Schröder, T., & Rensing, L. (1997). Differential HSC70 expression during asexual development of Neurospora crassa. Microbiology, 143, 3615–3624.

    Google Scholar 

  • Freitas, J. S., Silva, E. M., Leal, J., Gras, D. E., Martinez-Rossi, N. M., Dos Santos, L. D., Palma, M. S., & Rossi, A. (2011). Transcription of the Hsp30, Hsp70, and Hsp90 heat shock protein genes is modulated by the PalA protein in response to acid pH-sensing in the fungus Aspergillus nidulans. Cell Stress & Chaperones, 16, 565–572.

    Google Scholar 

  • Frydman, J. (2001). Folding of newly translated proteins in vivo: the role of molecular chaperones. Annual Review of Biochemistry, 70, 603–647.

    Article  PubMed  CAS  Google Scholar 

  • Galagan, J. E., Henn, M. R., Ma, L.-J., Cuomo, C. A., & Birren, B. (2005). Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Research, 15, 1620–1631.

    Article  PubMed  CAS  Google Scholar 

  • Gautam, P., Shankar, J., Madan, T., Sirdeshmukh, R., Sundaram, C. S., Gade, W. N., Basir, S. F., & Sarma, P. U. (2008). Proteomic and transcriptomic analysis of Aspergillus fumigatus on exposure to amphotericin B. Antimicrobial Agents and Chemotherapy, 52, 4220–4227.

    Google Scholar 

  • Georg, R. C., & Gomes, S. L. (2007). Transcriptome analysis in response to heat shock and cadmium in the aquatic fungus Blastocladiella emersonii. Eukaryotic Cell, 6, 1053–1062.

    Google Scholar 

  • Girvitz, T., Ouimet, P., & Kapoor, M. (2000). Heat shock protein 80 of Neurospora crassa: Sequence analysis of the gene and expression during the asexual phase. Canadian Journal of Microbiology, 46, 981–991.

    Article  PubMed  CAS  Google Scholar 

  • Goldman, G. H., dos Reis Marques, E., Ribeiro, D. C. D., de Souza, B. L. A. N., Quiapin, A. C., Vitorelli, P. M., Savoldi, M., Semighini, C. P., de Oliveira, R. C., & Nunes, L. R. (2003). Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryotic Cell, 2, 34–48.

    Google Scholar 

  • Grant, C. M., & Tuite, M. F. (1994). Mistranslation of human phosphoglycerate kinase in yeast in the presence of paromomycin. Current Genetics, 26, 95–99.

    Article  PubMed  CAS  Google Scholar 

  • Grant, C., Firoozan, M., & Tuite, M. (1989). Mistranslation induces the heat-shock response in the yeast Saccharomyces cerevisiae. Molecular Microbiology, 3, 215–220.

    Article  PubMed  CAS  Google Scholar 

  • Guarro, J., Gené, J., & Stchigel, A. M. (1999). Developments in fungal taxonomy. Clinical Microbiology Reviews, 12, 454–500.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Gupta, R. S., & Singh, B. (1994). Phylogenetic analysis of 70 kD heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus. Current Biology, 4, 1104–1114.

    Article  PubMed  CAS  Google Scholar 

  • Gwynne, D. I., & Brandhorst, B. (1982). Alterations in gene expression during heat shock of Achlya ambisexualis. Journal of Bacteriology, 149, 488–493.

    Google Scholar 

  • Häfker, T., Techel, D., Steier, G., & Rensing, L. (1998). Differential expression of glucose-regulated (grp78) and heat-shock-inducible (hsp70) genes during asexual development of Neurospora crassa. Microbiology, 144, 37–43.

    Google Scholar 

  • Hennessy, F., Cheetham, M. E., Dirr, H. W., & Blatch, G. L. (2000). Analysis of the levels of conservation of the J domain among the various types of DnaJ-like proteins. Cell Stress & Chaperones, 5, 347–358.

    Article  CAS  Google Scholar 

  • Hettema, E. H., Ruigrok, C. C., Koerkamp, M. G., Van, D., Berg, M., Tabak, H. F., Distel, B., & Braakman, I. (1998). The cytosolic DnaJ-like protein djp1p is involved specifically in peroxisomal protein import. The Journal of Cell Biology, 142, 421–434.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Horton, L. E., James, P., Craig, E. A., & Hensold, J. O. (2001). The yeast hsp70 homologue Ssa is required for translation and interacts with Sis1 and Pab1 on translating ribosomes. The Journal of Biological Chemistry, 276, 14426–14433.

    Article  PubMed  CAS  Google Scholar 

  • Jin, C. (2011). Protein glycosylation in Aspergillus fumigatus is essential for cell wall synthesis and serves as a promising model of multicellular eukaryotic development. International Journal of Microbiology, 2012, 654251.

    Google Scholar 

  • Jones, G., Song, Y., Chung, S., & Masison, D. C. (2004). Propagation of Saccharomyces cerevisiae [PSI+] prion is impaired by factors that regulate Hsp70 substrate binding. Molecular and Cellular Biology, 24, 3928–3937.

    Google Scholar 

  • Jung, G., Jones, G., Wegrzyn, R. D., & Masison, D. C. (2000). A role for cytosolic Hsp70 in yeast [PSI+] prion propagation and [PSI+] as a cellular stress. Genetics, 156, 559–570.

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kabani, M., Beckerich, J.-M., & Gaillardin, C. (2000). Sls1p stimulates Sec63p-mediated activation of Kar2p in a conformation-dependent manner in the yeast endoplasmic reticulum. Molecular and Cellular Biology, 20, 6923–6934.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kabani, M., Beckerich, J.-M., & Brodsky, J. L. (2002). Nucleotide exchange factor for the yeast Hsp70 molecular chaperone Ssa1p. Molecular and Cellular Biology, 22, 4677–4689.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kakeya, H., Udono, H., Maesaki, S., Sasaki, E., Kawamura, S., Hossain, M., Yamamoto, Y., Sawai, T., Fukuda, M., & Mitsutake, K. (1999). Heat shock protein 70 (hsp70) as a major target of the antibody response in patients with pulmonary cryptococcosis. Clinical and Experimental Immunology, 115, 485.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kampinga, H. H., & Craig, E. A. (2010). The Hsp70 chaperone machinery: J-proteins as drivers of functional specificity. Nature Reviews. Molecular Cell Biology, 11, 579.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kapoor, M. (1983). A study of the heat-shock response in Neurospora crassa. The International Journal of Biochemistry, 15, 639–649.

    Google Scholar 

  • Kapoor, M., & Lewis, J. (1987). Heat shock induces peroxidase activity in Neurospora crassa and confers tolerance toward oxidative stress. Biochemical and Biophysical Research Communications, 147, 904–910.

    Article  PubMed  CAS  Google Scholar 

  • Kapoor, M., Curle, C., & Runham, C. (1995). The hsp70 gene family of Neurospora crassa: Cloning, sequence analysis, expression, and genetic mapping of the major stress-inducible member. Journal of Bacteriology, 177, 212–221.

    Google Scholar 

  • Kominek, J., Marszalek, J., Neuvéglise, C., Craig, E. A., & Williams, B. L. (2013). The complex evolutionary dynamics of Hsp70s: A genomic and functional perspective. Genome Biology and Evolution, 5, 2460–2477.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kregel, K. C. (2002). Invited review: Heat shock proteins: Modifying factors in physiological stress responses and acquired thermotolerance. Journal of Applied Physiology, 92, 2177–2186.

    Article  PubMed  CAS  Google Scholar 

  • Kummasook, A., Kummasook, A., Pongpom, P., Kummasook, A., Pongpom, P., & Vanittanakom, N. (2007). Cloning, characterization and differential expression of an hsp70 gene from the pathogenic dimorphic fungus, Penicillium marneffei. DNA Sequence, 18, 385–394.

    Google Scholar 

  • Lakshman, D. K., Roberts, D. P., Garrett, W. M., Natarajan, S. S., Darwish, O., Alkharouf, N., Pain, A., Khan, F., Jambhulkar, P. P., & Mitra, A. (2016). Proteomic investigation of Rhizoctonia solani AG 4 identifies secretome and mycelial proteins with roles in plant cell wall degradation and virulence. Journal of Agricultural and Food Chemistry, 64, 3101–3110.

    Google Scholar 

  • Latouche, S., Totel, A., Lacube, P., Bolognini, J., Nevez, G., & Roux, A. (2001). Development of an RT-PCR on the heat shock protein 70 gene for viability detection of Pneumocystis carinii f. sp. hominis in patients with Pneumocystosis and in air sample. Journal of Eukaryotic Microbiology, 48, 176S–177S.

    Google Scholar 

  • Lewis, J., Learmonth, R., & Watson, K. (1995). Induction of heat, freezing and salt tolerance by heat and salt shock in Saccharomyces cerevisiae. Microbiology, 141, 687–694.

    Google Scholar 

  • Li, J., Qian, X., & Sha, B. (2003a). The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure, 11, 1475–1483.

    Article  PubMed  CAS  Google Scholar 

  • Li, X. S., Reddy, M. S., Baev, D., & Edgerton, M. (2003b). Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5. The Journal of Biological Chemistry, 278, 28553–28561.

    Google Scholar 

  • Li, L., Li, Q., Liu, Z., & Wu, H. (2008). Immunological analysis and mass spectrometry identification of the major allergen from Cladosporium cladosporioides. Journal of Hygiene Research, 37, 50–52.

    Google Scholar 

  • Liebman, S. W., & Chernoff, Y. O. (2012). Prions in yeast. Genetics, 191, 1041–1072.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lindquist, S., & Craig, E. (1988). The heat-shock proteins. Annual Review of Genetics, 22, 631–677.

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Ribot, J. L., Alloush, H. M., Masten, B. J., & Chaffin, W. L. (1996). Evidence for presence in the cell wall of Candida albicans of a protein related to the hsp70 family. Infection and Immunity, 64, 3333–3340.

    Google Scholar 

  • Lüders, J., Demand, J., & Höhfeld, J. (2000). The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. The Journal of Biological Chemistry, 275, 4613–4617.

    Article  PubMed  Google Scholar 

  • Mayer, M., & Bukau, B. (2005). Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62, 670.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McEwen, J., Taylor, J., Carter, D., Xu, J., Felipe, M., Vilgalys, R., Mitchell, T., Kasuga, T., White, T., & Bui, T. (2000). Molecular typing of pathogenic fungi. Medical Mycology, 38, 189–197.

    Article  PubMed  CAS  Google Scholar 

  • Molinari, M., Galli, C., Piccaluga, V., Pieren, M., & Paganetti, P. (2002). Sequential assistance of molecular chaperones and transient formation of covalent complexes during protein degradation from the ER. The Journal of Cell Biology, 158, 247–257.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Monteiro, J. P., Clemons, K. V., Mirels, L. F., Coller, J. A., Jr., Wu, T. D., Shankar, J., Lopes, C. R., & Stevens, D. A. (2009). Genomic DNA microarray comparison of gene expression patterns in Paracoccidioides brasiliensis mycelia and yeasts in vitro. Microbiology, 155, 2795–2808.

    Google Scholar 

  • Morano, K. A., Grant, C. M., & Moye-Rowley, W. S. (2012). The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics, 190, 1157–1195.

    Google Scholar 

  • Newbury, J., & Peberdy, J. F. (1996). Characterization of the heat shock response in protoplasts of Aspergillus nidulans. Mycological Research, 100, 1325–1332.

    Google Scholar 

  • Nikolaidis, N., & Nei, M. (2004). Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Molecular Biology and Evolution, 21, 498–505.

    Article  PubMed  CAS  Google Scholar 

  • Odds, F. C., Brown, A. J., & Gow, N. A. (2003). Antifungal agents: Mechanisms of action. Trends in Microbiology, 11, 272–279.

    Article  PubMed  CAS  Google Scholar 

  • Ouimet, P., & Kapoor, M. (1999). Nucleotide binding and hydrolysis properties of Neurospora crassa cytosolic molecular chaperones, Hsp70 and Hsp80, heat-inducible members of the eukaryotic stress-70 and stress-90 families. Biochemistry and Cell Biology, 77, 89–99.

    Google Scholar 

  • Peñalva, M. A., & Arst, H. N. (2002). Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiology and Molecular Biology Reviews, 66, 426–446.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perlman, J., & Feldman, J. F. (1982). Cycloheximide and heat shock induce new polypeptide synthesis in Neurospora crassa. Molecular and Cellular Biology, 2, 1167–1173.

    Google Scholar 

  • Pfund, C., Huang, P., Lopez-Hoyo, N., & Craig, E. A. (2001). Divergent functional properties of the ribosome-associated molecular chaperone Ssb compared with other Hsp70s. Molecular Biology of the Cell, 12, 3773–3782.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plesofsky-Vig, N., & Brambl, R. (1985a). The heat shock response of fungi. Experimental Mycology, 9, 7–94.

    Article  Google Scholar 

  • Plesofsky-Vig, N., & Brambl, R. (1985b). Heat shock response of Neurospora crassa: Protein synthesis and induced thermotolerance. Journal of Bacteriology, 162, 1083–1091.

    Google Scholar 

  • Plesset, J., Palm, C., & McLaughlin, C. (1982). Induction of heat shock proteins and thermotolerance by ethanol in Saccharomyces cerevisiae. Biochemical and Biophysical Research Communications, 108, 1340–1345.

    Google Scholar 

  • Qiu, X.-B., Shao, Y.-M., Miao, S., & Wang, L. (2006). The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cellular and Molecular Life Sciences, 63, 2560–2570.

    Article  PubMed  CAS  Google Scholar 

  • Raitt, D. C., Johnson, A. L., Erkine, A. M., Makino, K., Morgan, B., Gross, D. S., & Johnston, L. H. (2000). The Skn7 response regulator of Saccharomyces cerevisiaeinteracts with Hsf1 in vivo and is required for the induction of heat shock genes by oxidative stress. Molecular Biology of the Cell, 11, 2335–2347.

    Google Scholar 

  • Röhl, A., Wengler, D., Madl, T., Lagleder, S., Tippel, F., Herrmann, M., Hendrix, J., Richter, K., Hack, G., & Schmid, A. B. (2015). Hsp90 regulates the dynamics of its cochaperone Sti1 and the transfer of Hsp70 between modules. Nature Communications, 6, 6655.

    Article  PubMed  CAS  Google Scholar 

  • Roychowdhury, H., & Kapoor, M. (1988). Ethanol and carbon-source starvation enhance the accumulation of HSP80 in Neurospora crassa. Canadian Journal of Microbiology, 34, 162–168.

    Google Scholar 

  • Salzer, H. J. F. (2008). Identification and characterization of heat shock protein 60 and 70 of common environmental fungi of medical interest. MedizinischeUniversität.

    Google Scholar 

  • Sanchez, Y., Parsell, D., Taulien, J., Vogel, J., Craig, E., & Lindquist, S. (1993). Genetic evidence for a functional relationship between Hsp104 and Hsp70. Journal of Bacteriology, 175, 6484–6491.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Satyanarayana, C., Schröder-Köhne, S., Craig, E. A., Schu, P. V., & Horst, M. (2000). Cytosolic Hsp70s are involved in the transport of aminopeptidase 1 from the cytoplasm into the vacuole. FEBS Letters, 470, 232–238.

    Article  PubMed  CAS  Google Scholar 

  • Schmidt, P., Walker, J., Selway, L., Stead, D., Yin, Z., Enjalbert, B., Weig, M., & Brown, A. J. (2008). Proteomic analysis of the pH response in the fungal pathogen Candida glabrata. Proteomics, 8, 534–544.

    Google Scholar 

  • Setiadi, E. R., Doedt, T., Cottier, F., Noffz, C., & Ernst, J. F. (2006). Transcriptional response of Candida albicans to hypoxia: Linkage of oxygen sensing and Efg1p-regulatory networks. Journal of Molecular Biology, 361, 399–411.

    Google Scholar 

  • Shaner, L., Sousa, R., & Morano, K. A. (2006). Characterization of Hsp70 binding and nucleotide exchange by the yeast Hsp110 chaperone Sse1. Biochemistry, 45, 15075–15084.

    Article  PubMed  CAS  Google Scholar 

  • Shankar, J. (2013). An overview of toxins in Aspergillus associated with pathogenesis. International Journal of Life Sciences Biotechnology and Pharma Research, 2, 16–31.

    Google Scholar 

  • Shankar, J., Nigam, S., Saxena, S., Madan, T., & Sarma, P. (2004). Identification and assignment of function to the genes of Aspergillus fumigatus expressed at 37 C. The Journal of Eukaryotic Microbiology, 51, 428–432.

    Google Scholar 

  • Shankar, J., Restrepo, A., Clemons, K. V., & Stevens, D. A. (2011a). Hormones and the resistance of women to paracoccidioidomycosis. Clinical Microbiology Reviews, 24, 296–313.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shankar, J., Wu, T. D., Clemons, K. V., Monteiro, J. P., Mirels, L. F., & Stevens, D. A. (2011b). Influence of 17β-estradiol on gene expression of Paracoccidioides during mycelia-to-yeast transition. PLoS One, 6, e28402.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma, D., & Masison, D. C. (2009). Hsp70 structure, function, regulation and influence on yeast prions. Protein and Peptide Letters, 16, 571–581.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma, D., Martineau, C. N., Le Dall, M.-T., Reidy, M., Masison, D. C., & Kabani, M. (2009a). Function of SSA subfamily of Hsp70 within and across species varies widely in complementing Saccharomyces cerevisiae cell growth and prion propagation. PLoS One, 4, e6644.

    Google Scholar 

  • Sharma, S. K., Christen, P., & Goloubinoff, P. (2009b). Disaggregating chaperones: An unfolding story. Current Protein and Peptide Science, 10, 432–446.

    Article  PubMed  CAS  Google Scholar 

  • Shearer, G., Jr., Birge, C. H., Yuckenberg, P. D., Kobayashi, G. S., & Medoff, G. (1987). Heat-shock proteins induced during the mycelial-to-yeast transitions of strains of Histoplasma capsulatum. Microbiology, 133, 3375–3382.

    Google Scholar 

  • Shen, H. D., Au, L. C., Lin, W. L., Liaw, S. F., Tsai, J. J., & Han, S. H. (1997). Molecular cloning and expression of a Penicillium citrinum allergen with sequence homology and antigenic crossreactivity to a hsp 70 human heat shock protein. Clinical and Experimental Allergy, 27, 682–690.

    Google Scholar 

  • Shen, Y., Meunier, L., & Hendershot, L. M. (2002). Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. The Journal of Biological Chemistry, 277, 15947–15956.

    Article  PubMed  CAS  Google Scholar 

  • Shiber, A., & Ravid, T. (2014). Chaperoning proteins for destruction: Diverse roles of Hsp70 chaperones and their co-chaperones in targeting misfolded proteins to the proteasome. Biomolecules, 4, 704–724.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shiber, A., Breuer, W., Brandeis, M., & Ravid, T. (2013). Ubiquitin conjugation triggers misfolded protein sequestration into quality control foci when Hsp70 chaperone levels are limiting. Molecular Biology of the Cell, 24, 2076–2087.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silva, E. M., Freitas, J. S., Gras, D. E., Squina, F. M., Leal, J., Silveira, H. C., Martinez-Rossi, N. M., & Rossi, A. (2008). Identification of genes differentially expressed in a strain of the mold Aspergillus nidulans carrying a loss-of-function mutation in the palA gene. Canadian Journal of Microbiology, 54, 803–811.

    Article  PubMed  CAS  Google Scholar 

  • Singh, K., Nizam, S., Sinha, M., & Verma, P. K. (2012). Comparative transcriptome analysis of the necrotrophic fungus Ascochyta rabiei during oxidative stress: Insight for fungal survival in the host plant. PLoS One, 7, e33128.

    Google Scholar 

  • Sondermann, H., Ho, A. K., Listenberger, L. L., Siegers, K., Moarefi, I., Wente, S. R., Hartl, F.-U., & Young, J. C. (2002). Prediction of novel Bag-1 homologs based on structure/function analysis identifies Snl1p as an Hsp70 co-chaperone in Saccharomyces cerevisiae. The Journal of Biological Chemistry, 277, 33220–33227.

    Google Scholar 

  • Song, Y., & Masison, D. C. (2005). Independent regulation of Hsp70 and Hsp90 chaperones by Hsp70/Hsp90-organizing protein Sti1 (Hop1). The Journal of Biological Chemistry, 280, 34178–34185.

    Google Scholar 

  • Song, Y., Wu, Y.-x., Jung, G., Tutar, Y., Eisenberg, E., Greene, L. E., & Masison, D. C. (2005). Role for Hsp70 chaperone in Saccharomyces cerevisiae prion seed replication. Eukaryotic Cell, 4, 289–297.

    Google Scholar 

  • Squina, F. M., Leal, J., Cipriano, V. T., Martinez-Rossi, N. M., & Rossi, A. (2010). Transcription of the Neurospora crassa 70-kDa class heat shock protein genes is modulated in response to extracellular pH changes. Cell Stress & Chaperones, 15, 225–231.

    Google Scholar 

  • Stedman, T. T., Butler, D. R., & Buck, G. A. (1998). The HSP70 gene family in Pneumocystis carinii: Molecular and phylogenetic characterization of cytoplasmic members. The Journal of Eukaryotic Microbiology, 45, 589–599.

    Google Scholar 

  • Steel, G. J., Fullerton, D. M., Tyson, J. R., & Stirling, C. J. (2004). Coordinated activation of Hsp70 chaperones. Science, 303, 98–101.

    Article  PubMed  CAS  Google Scholar 

  • Stefani, R. M. P., & Gomes, S. L. (1995). A unique intron-containing hsp70 gene induced by heat shock and during sporulation in the aquatic fungus Blastocladiella emersonii. Gene, 152, 19–26.

    Google Scholar 

  • Tereshina, V. (2005). Thermotolerance in fungi: The role of heat shock proteins and trehalose. Microbiology, 74, 247–257.

    Article  CAS  Google Scholar 

  • Thakur, R., Anand, R., Tiwari, S., Singh, A. P., Tiwary, B. N., & Shankar, J. (2015). Cytokines induce effector T-helper cells during invasive aspergillosis; what we have learned about T-helper cells? Frontiers in Microbiology, 6, 429.

    Article  PubMed  PubMed Central  Google Scholar 

  • Thakur, R., Tiwari, S., & Shankar, J. (2016). Differential expression pattern of heat shock protein genes in toxigenic and atoxigenic isolate of Aspergillus flavus. British Microbiology Research Journal, 14, 1–9.

    Google Scholar 

  • Tibor Roberts, B., Moriyama, H., & Wickner, R. B. (2004). [URE3] prion propagation is abolished by a mutation of the primary cytosolic Hsp70 of budding yeast. Yeast, 21, 107–117.

    Article  PubMed  CAS  Google Scholar 

  • Tilburn, J., Sarkar, S., Widdick, D., Espeso, E., Orejas, M., Mungroo, J., Penalva, M., & Arst, H., Jr. (1995). The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid-and alkaline-expressed genes by ambient pH. The EMBO Journal, 14, 779.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tiwari, S., Thakur, R., & Shankar, J. (2015). Role of heat-shock proteins in cellular function and in the biology of fungi. Biotechnology Research International, 2015, 1–11.

    Article  CAS  Google Scholar 

  • Tiwari, S., Thakur, R., Goel, G., & Shankar, J. (2016). Nano-LC-Q-TOF analysis of proteome revealed germination of Aspergillus flavus Conidia is accompanied by MAPK signalling and cell wall modulation. Mycopathologia, 181, 769–786.

    Google Scholar 

  • Tiwari, S., & Shankar, J. (2018) Integrated proteome and HPLC analysis revealed quercetin-mediated inhibition of aflatoxin B1 biosynthesis in Aspergillus flavus. 3 Biotech 8 (1)

    Google Scholar 

  • Tyson, J. R., & Stirling, C. J. (2000). LHS1 and SIL1 provide a lumenal function that is essential for protein translocation into the endoplasmic reticulum. The EMBO Journal, 19, 6440–6452.

    Google Scholar 

  • Verghese, J., Abrams, J., Wang, Y., & Morano, K. A. (2012). Biology of the heat shock response and protein chaperones: Budding yeast (Saccharomyces cerevisiae) as a model system. Microbiology and Molecular Biology Reviews, 76, 115–158.

    Google Scholar 

  • Wang, L., & Lin, X. (2012). Morphogenesis in fungal pathogenicity: Shape, size, and surface. PLoS Pathogens, 8, e1003027.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang, C., Duan, Z., & Leger, R. J. S. (2008). MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryotic Cell, 7, 302–309.

    Google Scholar 

  • Weitzel, G., Pilatus, U., & Rensing, L. (1985). Similar dose response of heat shock protein synthesis and intracellular pH change in yeast. Experimental Cell Research, 159, 252–256.

    Article  PubMed  CAS  Google Scholar 

  • Werner-Washburne, M., & Craig, E. A. (1989). Expression of members of the Saccharomyces cerevisiae hsp70 multigene family. Genome, 31, 684–689.

    Article  PubMed  CAS  Google Scholar 

  • Werner-Washburne, M., Stone, D. E., & Craig, E. A. (1987). Complex interactions among members of an essential subfamily of hsp70 genes in Saccharomyces cerevisiae. Molecular and Cellular Biology, 7, 2568–2577.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wormley, F. L., Jr. (2011). Potential vaccine strategies for the management of cryptococcal disease. Journal of Invasive Fungal Infection, 5, 65.

    Google Scholar 

  • Xavier, I. J. (1998). Environmental stress response of the Hyphomycetous Entomopathogenic fungi. http://hdl.handle.net/10388/etd-10212004-001033

  • Yi, M., Chi, M.-H., Khang, C. H., Park, S.-Y., Kang, S., Valent, B., & Lee, Y.-H. (2009). The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell, 21, 681–695.

    Google Scholar 

  • Zhu, C., Ai, L., Wang, L., Yin, P., Liu, C., Li, S., & Zeng, H. (2016). De novo transcriptome analysis of Rhizoctonia solani AG1 IA strain early invasion in Zoysia japonica root. Frontiers in Microbiology, 7, 708.

    Google Scholar 

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We are thankful to the Department of Biotechnology and Bioinformatics, Jaypee University of Information Technology, for providing facilities.

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Tiwari, S., Shankar, J. (2018). Hsp70 in Fungi: Evolution, Function and Vaccine Candidate. In: Asea, A., Kaur, P. (eds) HSP70 in Human Diseases and Disorders. Heat Shock Proteins, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-319-89551-2_20

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