Investigating the chaperone properties of a novel heat shock protein, Hsp70.c, from trypanosoma brucei

Journal of Parasitology Research

Volumn 2014, Issue , 2014, Pages

  Burger, Adélle ^a   Ludewig, Michael H ^a   Boshoff, Aileen ^a  

^a RHODES UNIVERSITY   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CHAPERONE; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; MALATE DEHYDROGENASE; PROTEIN TBHSP70.C; PROTOZOAL PROTEIN; THIOSULFATE SULFURTRANSFERASE; TRYPANOSOMA BRUCEI J PROTEIN 2; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; HEAT STRESS; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; TRYPANOSOMA BRUCEI; UPREGULATION;

EID: 84897001801     PISSN: 20900023     EISSN: 20900031     Source Type: Journal    
DOI: 10.1155/2014/172582     Document Type: Article

References (65)

1. Brodsky J. L., McCracken A. A., ER protein quality control and proteasome-mediated protein degradation. Seminars in Cell and Developmental Biology 1999 10 5 507 513 2-s2.0-0033208984 10.1006/scdb.1999.0321 (Pubitemid 129513236)
2. Hamman B. D., Hendershot L. M., Johnson A. E., BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell 1998 92 6 747 758 2-s2.0-0032549767 10.1016/S0092-8674(00)81403-8 (Pubitemid 28155314)
3. Eggers D. K., Welch W. J., Hansen W. J., Complexes between nascent polypeptides and their molecular chaperones in the cytosol of mammalian cells. Molecular Biology of the Cell 1997 8 8 1559 1573 2-s2.0-0030928059 (Pubitemid 27385576)
4. Zylicz M., Ang D., Liberek K., Georgopoulos C., Initiation of DNA replication with purified host- and bacteriophage-encoded proteins: the role of the dnaK, dnaJ and grpE heat shock proteins. EMBO Journal 1989 8 5 1601 1608 2-s2.0-0024316732 (Pubitemid 19274387)
5. Daugaard M., Rohde M., Jäättelä M., The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Letters 2007 581 19 3702 3710 2-s2.0-34447528828 10.1016/j.febslet.2007.05. 039 (Pubitemid 47081009)
6. Slepenkov S. V., Witt S. N., The unfolding story of the Escherichia coli Hsp70 DnaK: is DnaK a holdase or an unfoldase? Molecular Microbiology 2002 45 5 1197 1206 2-s2.0-0036049850 10.1046/j.1365-2958.2002.03093.x (Pubitemid 35015345)
7. Flaherty K. M., DeLuca-Flaherty C., McKay D. B., Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 1990 346 6285 623 628 2-s2.0-0025100372 10.1038/346623a0 (Pubitemid 20266393)
8. Wang T.-F., Chang J.-H., Wang C., Identification of the peptide binding domain of hsc70. 18-kilodalton fragment located immediately after ATPase domain is sufficient for high affinity binding. Journal of Biological Chemistry 1993 268 35 26049 26051 2-s2.0-0027433805 (Pubitemid 23361661)
9. McCarty J. S., Buchberger A., Reinstein J., Bukau B., The role of ATP in the functional cycle of the DnaK chaperone system. Journal of Molecular Biology 1995 249 1 126 137 2-s2.0-0029013908 10.1006/jmbi.1995.0284
10. Brodsky J. L., Bracher A., Blatch G. L., Nucleotide exchange factors for Hsp70 molecular chaperones. Networking of Chaperones By Co-Chaperones 2007 New York, NY, USA Landes Bioscience, Austin, Tex, USA; Springer Science Business Media 26 37
11. Scheufler C., Brinker A., Bourenkov G., Pegoraro S., Moroder L., Bartunik H., Hartl F. U., Moarefi I., Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 2000 101 2 199 210 2-s2.0-0034646511 10.1016/S0092-8674(00)80830-2 (Pubitemid 32004747)
12. Li J., Wu Y., Qian X., Sha B., Crystal structure of yeast Sis1 peptide-binding fragment and Hsp70 Ssa1 C-terminal complex. Biochemical Journal 2006 398 3 353 360 2-s2.0-33748743974 10.1042/BJ20060618 (Pubitemid 44453379)
13. Demand J., Lüders J., Höhfeld J., The carboxy-terminal domain of Hsc70 provides binding sites for a distinct set of chaperone cofactors. Molecular and Cellular Biology 1998 18 4 2023 2028 2-s2.0-2642689664 (Pubitemid 28152651)
14. Genevaux P., Wawrzynow A., Zylicz M., Georgopoulos C., Kelley W. L., DjlA is a third DnaK co-chaperone of Escherichia coli, and DjlA- mediated induction of colanic acid capsule requires DjlA-DnaK interaction. Journal of Biological Chemistry 2001 276 11 7906 7912 2-s2.0-0035896599 10.1074/jbc.M003855200
15. Wittung-Stafshede P., Guidry J., Horne B. E., Landry S. J., The J-domain of Hsp40 couples ATP hydrolysis to substrate capture in Hsp70. Biochemistry 2003 42 17 4937 4944 2-s2.0-0038523841 10.1021/bi027333o (Pubitemid 36532046)
16. Li J., Qian X., Sha B., The crystal structure of the yeast Hsp40 Ydj1 complexed with its peptide substrate. Structure 2003 11 12 1475 1483 2-s2.0-0345299781 10.1016/j.str.2003.10.012 (Pubitemid 37510348)
17. Hu J., Wu Y., Li J., Qian X., Fu Z., Sha B., The crystal structure of the putative peptide-binding fragment from the human Hsp40 protein Hdj1. BMC Structural Biology 2008 8, article 3 2-s2.0-40049097090 10.1186/1472-6807-8-3 (Pubitemid 351322903)
18. Cyr D. M., Langer T., Douglas M. G., DnaJ-like proteins: molecular chaperones and specific regulators of Hsp70. Trends in Biochemical Sciences 1994 19 4 176 181 2-s2.0-0028353336 10.1016/0968-0004(94)90281-X (Pubitemid 24115434)
19. Johnson J. L., Craig E. A., An essential role for the substrate-binding region of Hsp40s in Saccharomyces cerevisiae. Journal of Cell Biology 2001 152 4 851 856 2-s2.0-0035911158 10.1083/jcb.152.4.851 (Pubitemid 34280169)
20. Sha B., Lee S., Cyr D. M., The crystal structure of the peptide-binding fragment from the yeast Hsp40 protein Sis1. Structure 2000 8 8 799 807 2-s2.0-0034662746 10.1016/S0969-2126(00)00170-2
21. Wu Y., Li J., Jin Z., Fu Z., Sha B., The crystal structure of the C-terminal fragment of yeast Hsp40 Ydj1 reveals novel dimerization motif for Hsp40. Journal of Molecular Biology 2005 346 4 1005 1011 2-s2.0-13444274413 10.1016/j.jmb.2004.12.040 (Pubitemid 40215525)
22. Hennessy F., Nicoll W. S., Zimmermann R., Cheetham M. E., Blatch G. L., Not all J domains are created equal: implications for the specificity of Hsp40-Hsp70 interactions. Protein Science 2005 14 7 1697 1709 2-s2.0-22344447035 10.1110/ps.051406805 (Pubitemid 41001413)
23. Manful T., Mulindwa J., Frank F. M., Clayton C. E., Matovu E., A search for Trypanosoma brucei rhodesiense diagnostic antigens by proteomic screening and targeted cloning. PLoS ONE 2010 5 3 2-s2.0-77949798151 10.1371/journal.pone. 0009630 e9630
24. Vickerman K., Developmental cycles and biology of pathogenic trypanosomes. British Medical Bulletin 1985 41 2 105 114 2-s2.0-0021877040 (Pubitemid 15059394)
25. Delespaux V., de Koning H. P., Drugs and drug resistance in African trypanosomiasis. Drug Resistance Updates 2007 10 1-2 30 50 2-s2.0-33847092850 10.1016/j.drup.2007.02.004 (Pubitemid 46636383)
26. Evans C. G., Chang L., Gestwicki J. E., Heat shock protein 70 (Hsp70) as an emerging drug target. Journal of Medicinal Chemistry 2010 53 12 4585 4602 2-s2.0-77953734857 10.1021/jm100054f
27. Bhagat L., Singh V. P., Dawra R. K., Saluja A. K., Sodium arsenite induces heat shock protein 70 expression and protects against secretagogue-induced trypsinogen and NF- B activation. Journal of Cellular Physiology 2008 215 1 37 46 2-s2.0-39149109341 10.1002/jcp.21286 (Pubitemid 351363189)
28. Bao X.-Q., Liu G.-T., Induction of overexpression of the 27- and 70-kDa heat shock proteins by bicyclol attenuates concanavalin A-induced liver injury through suppression of nuclear factor- B in mice. Molecular Pharmacology 2009 75 5 1180 1188 2-s2.0-66049162280 10.1124/mol.108.053280
29. Banumathy G., Singh V., Pavithra S. R., Tatu U., Heat shock protein 90 function is essential for Plasmodium falciparum growth in human erythrocytes. Journal of Biological Chemistry 2003 278 20 18336 18345 2-s2.0-0038381514 10.1074/jbc.M211309200 (Pubitemid 36799454)
30. Pallavi R., Acharya P., Chandran S., Daily J. P., Tatu U., Chaperone expression profiles correlate with distinct physiological states of Plasmodium falciparum in malaria patients. Malaria Journal 2010 9 1, article 236 2-s2.0-77955682353 10.1186/1475-2875-9-236
31. Krautz G. M., Peterson J. D., Godsel L. M., Krettli A. U., Engman D. M., Human antibody responses to Trypanosoma cruzi 70-kD heat-shock proteins. American Journal of Tropical Medicine and Hygiene 1998 58 2 137 143 2-s2.0-0031930633 (Pubitemid 28096216)
32. Planelles L., Thomas M. C., Alonso C., López M. C., DNA immunization with Trypanosoma cruzi HSP70 fused to the KMP11 protein elicits a cytotoxic and humoral immune response against the antigen and leads to protection. Infection and Immunity 2001 69 10 6558 6563 2-s2.0-0034824676 10.1128/IAI.69.10.6558-6563.2001 (Pubitemid 32885228)
33. Arif A. A., Gao L., Davis C. D., Helm D. S., Antibody response to heat shock proteins and histopathology in mice infected with Trypanosoma cruzi and maintained at elevated temperature. Journal of Parasitology 1999 85 6 1089 1099 2-s2.0-0033404358 (Pubitemid 30041276)
34. Edkins A. L., Ludewig M. H., Blatch G. L., A Trypanosoma cruzi heat shock protein 40 is able to stimulate the adenosine triphosphate hydrolysis activity of heat shock protein 70 and can substitute for a yeast heat shock protein 40. International Journal of Biochemistry and Cell Biology 2004 36 8 1585 1598 2-s2.0-2442513446 10.1016/j.biocel.2004.01.016 (Pubitemid 38625837)
35. Folgueira C., Requena J. M., A postgenomic view of the heat shock proteins in kinetoplastids. FEMS Microbiology Reviews 2007 31 4 359 377 2-s2.0-34250351297 10.1111/j.1574-6976.2007.00069.x (Pubitemid 46920247)
36. Louw C. A., Ludewig M. H., Mayer J., Blatch G. L., The Hsp70 chaperones of the Tritryps are characterized by unusual features and novel members. Parasitology International 2010 59 4 497 505 2-s2.0-77958456516 10.1016/j.parint.2010.08.008
37. Louw C. A., Ludewig M. H., Blatch G. L., Overproduction, purification and characterisation of Tbj1, a novel Type III Hsp40 from Trypanosoma brucei, the African sleeping sickness parasite. Protein Expression and Purification 2010 69 2 168 177 2-s2.0-70449524433 10.1016/j.pep.2009.09.023
38. Alsford S., Turner D. J., Obado S. O., Sanchez-Flores A., Glover L., Berriman M., Hertz-Fowler C., Horn D., High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Research 2011 21 6 915 924 2-s2.0-79955602637 10.1101/gr.115089.110
39. Ludewig M. H., Burger A., Boshoff A., Horn D., Blatch G. L., Trypanosoma brucei J protein 2 is a stress inducible and essential Hsp40. International Journal for Parasitology. In press
40. Aslett M., Aurrecoechea C., Berriman M., Brestelli J., Brunk B. P., Carrington M., Depledge D. P., Fischer S., Gajria B., Gao X., Gardner M. J., Gingle A., Grant G., Harb O. S., Heiges M., Hertz-Fowler C., Houston R., Innamorato F., Iodice J., Kissinger J. C., Kraemer E., Li W., Logan F. J., Miller J. A., Mitra S., Myler P. J., Nayak V., Pennington C., Phan I., Pinney D. F., Ramasamy G., Rogers M. B., Roos D. S., Ross C., Sivam D., Smith D. F., Srinivasamoorthy G., Stoeckert C. J. J., Subramanian S., Thibodeau R., Tivey A., Treatman C., Velarde G., Wang H., TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Research 2009 38 1 D457 D462 2-s2.0-75549088870 10.1093/nar/gkp851
41. Hertz-Fowler C., Peacock C. S., Wood V., Aslett M., Kerhornou A., Mooney P., Tivey A., Berriman M., Hall N., Rutherford K., Parkhill J., Ivens A. C., Rajandream M.-A., Barrell B., GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Research 2004 32 D339 D343 2-s2.0-9144264843 (Pubitemid 38081672)
42. Sayers E. W., Barrett T., Benson D. A., Bryant S. H., Canese K., Chetvernin V., Church D. M., Dicuccio M., Edgar R., Federhen S., Feolo M., Geer L. Y., Helmberg W., Kapustin Y., Landsman D., Lipman D. J., Madden T. L., Maglott D. R., Miller V., Mizrachi L., Ostell J., Pruitt K. D., Schuler G. D., Sequeira E., Sherry S. T., Shumway M., Sirotkin K., Souvorov A., Starchenko G., Tatusova T. A., Wagner L., Yaschenko E., Ye J., Database resources of the national center for biotechnology information. Nucleic Acids Research 2011 37 9 3124 3139 2-s2.0-66249127600
43. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011 28 10 2731 2739 2-s2.0-79957613599 10.1093/molbev/msr121
44. Edgar R. C., MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 2004 32 5 1792 1797 2-s2.0-3042666256 10.1093/nar/gkh340 (Pubitemid 38832724)
45. Allan R. K., Mok D., Ward B. K., Ratajczak T., Modulation of chaperone function and cochaperone interaction by novobiocin in the C-terminal domain of Hsp90: evidence that coumarin antibiotics disrupt Hsp90 dimerization. Journal of Biological Chemistry 2006 281 11 7161 7171 2-s2.0-33646371009 10.1074/jbc.M512406200 (Pubitemid 43847481)
46. Botha M., Pesce E.-R., Blatch G. L., The Hsp40 proteins of Plasmodium falciparum and other apicomplexa: regulating chaperone power in the parasite and the host. International Journal of Biochemistry and Cell Biology 2007 39 10 1781 1803 2-s2.0-34548232285 10.1016/j.biocel.2007.02.011 (Pubitemid 47321340)
47. Chifflet S., Torriglia A., Chiesa R., Tolosa S., A method for the determination of inorganic phosphate in the presence of labile organic phosphate and high concentrations of protein: application to lens ATPase. Analytical Biochemistry 1988 168 1 1 4 2-s2.0-0023874147 (Pubitemid 18088291)
48. Goloubinoff P., Mogk A., Ben Zvi A. P., Tomoyasu T., Bukau B., Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proceedings of the National Academy of Sciences of the United States of America 1999 96 24 13732 13737 2-s2.0-0033598703 10.1073/pnas.96.24.13732
49. Basha E., Lee G. J., Demeler B., Vierling E., Chaperone activity of cytosolic small heat shock proteins from wheat. European Journal of Biochemistry 2004 271 8 1426 1436 2-s2.0-2142768810 10.1111/j.1432-1033.2004.04033.x (Pubitemid 38553549)
50. Cockburn I. L., Pesce E.-R., Pryzborski J. M., Davies-Coleman M. T., Clark P. G. K., Keyzers R. A., Stephens L. L., Blatch G. L., Screening for small molecule modulators of Hsp70 chaperone activity using protein aggregation suppression assays: inhibition of the plasmodial chaperone PfHsp70-1. Biological Chemistry 2011 392 5 431 438 2-s2.0-79953855334 10.1515/BC.2011.040
51. Botha M., Chiang A. N., Needham P. B., Stephens L. L., Hoppe H. C., Külzer S., Przyborski J. M., Lingelbach K., Wipf P., Brodsky J. L., Shonhai A., Blatch G. L., Plasmodium falciparum encodes a single cytosolic type i Hsp40 that functionally interacts with Hsp70 and is upregulated by heat shock. Cell Stress and Chaperones 2011 16 4 389 401 2-s2.0-79956289943 10.1007/s12192-010- 0250-6
52. Shonhai A., Botha M., De Beer T. A. P., Boshoff A., Blatch G. L., Structure-function study of a Plasmodium falciparum Hsp70 using three dimensional modelling and in vitro analyses. Protein and Peptide Letters 2008 15 10 1117 1125 2-s2.0-54249123736 10.2174/092986608786071067
53. Shonhai A., Boshoff A., Blatch G. L., The structural and functional diversity of Hsp70 proteins from Plasmodium falciparum. Protein Science 2007 16 9 1803 1818 2-s2.0-34548461255 10.1110/ps.072918107 (Pubitemid 47367104)
54. Silberg J. J., Hoff K. G., Vickery L. E., The Hsc66-Hsc20 chaperone system in Escherichia coli: chaperone activity and interactions with the DnaK-DnaJ-GrpE system. Journal of Bacteriology 1998 180 24 6617 6624 2-s2.0-0032414399 (Pubitemid 29006076)
55. Young J. C., Schneider C., Hartl F. U., In vitro evidence that hsp90 contains two independent chaperone sites. FEBS Letters 1997 418 1-2 139 143 2-s2.0-0030862486 10.1016/S0014-5793(97)01363-X (Pubitemid 27514433)
56. Xu L., Hasin N., Shen M., He J., Xue Y., Zhou X., Perrett S., Song Y., Jones G. W., Using steered molecular dynamics to predict and assess Hsp70 substrate-binding domain mutants that alter prion propogation. PLOS Computational Biology 2013 9 e1002896
57. Young J. C., Hoogenraad N. J., Hartl F. U., Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 2003 112 1 41 50 2-s2.0-0037428164 10.1016/S0092-8674(02)01250-3 (Pubitemid 36106417)
58. Young J. C., Agashe V. R., Siegers K., Hartl F. U., Pathways of chaperone-mediated protein folding in the cytosol. Nature Reviews Molecular Cell Biology 2004 5 10 781 791 2-s2.0-5044239107 10.1038/nrm1492 (Pubitemid 39336272)
59. Panda M., Gorovits B. M., Horowitz P. M., Productive and nonproductive intermediates in the folding of denatured rhodanese. Journal of Biological Chemistry 2000 275 1 63 70 2-s2.0-0034614370 10.1074/jbc.275.1.63 (Pubitemid 30038953)
60. Ramya T. N. C., Surolia N., Surolia A., 15-Deoxyspergualin modulates Plasmodium falciparum heat shock protein function. Biochemical and Biophysical Research Communications 2006 348 2 585 592 2-s2.0-33746926300 10.1016/j.bbrc.2006.07.082 (Pubitemid 44188604)
61. Caplan A. J., Tsai J., Casey P. J., Douglas M. G., Farnesylation of YDJ1p is required for function at elevated growth temperatures in Saccharomyces cerevisiae. Journal of Biological Chemistry 1992 267 26 18890 18895 2-s2.0-0026686468
62. Fewell S. W., Smith C. M., Lyon M. A., Dumitrescu T. P., Wipf P., Day B. W., Brodsky J. L., Small molecule modulators of endogenous and co-chaperone-stimulated Hsp70 ATPase activity. Journal of Biological Chemistry 2004 279 49 51131 51140 2-s2.0-10944263745 10.1074/jbc.M404857200 (Pubitemid 40017855)
63. Laufen T., Mayer M. P., Beisel C., Klostermeier D., Mogk A., Reinstein J., Bukau B., Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. Proceedings of the National Academy of Sciences of the United States of America 1999 96 10 5452 5457 2-s2.0-0033545978 10.1073/pnas.96.10.5452 (Pubitemid 29234638)
64. Pérez-Morales D., Lanz-Mendoza H., Hurtado G., Martínez-Espinosa R., Espinoza B., Proteomic analysis of Trypanosoma cruzi epimastigotes subjected to heat shock. Journal of Biomedicine and Biotechnology 2012 2012 9 2-s2.0-84856377513 10.1155/2012/902803 902803
65. Requena J. M., Jimenez-Ruiz A., Soto M., Assiego R., Santaren J. F., Lopez M. C., Patarroyo M. E., Alonso C., Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Molecular and Biochemical Parasitology 1992 53 1-2 201 212 2-s2.0-0026645312 10.1016/0166-6851(92)90022-C