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. 1993 Nov;4(11):1145–1159. doi: 10.1091/mbc.4.11.1145

Genetic interactions between KAR2 and SEC63, encoding eukaryotic homologues of DnaK and DnaJ in the endoplasmic reticulum.

M A Scidmore 1, H H Okamura 1, M D Rose 1
PMCID: PMC275750  PMID: 8305736

Abstract

KAR2 encodes the yeast homologue of mammalian BiP, the endoplasmic reticulum (ER) resident member of the HSP70 family. Kar2p has been shown to be required for the translocation of proteins across the ER membrane as well as nuclear fusion. Sec63, an ER integral membrane protein that shares homology with the Escherichia coli DnaJ protein, is also required for translocation. In this paper we describe several specific genetic interactions between these two proteins, Kar2p and Sec63p. First, temperature-sensitive mutations in KAR2 and SEC63 form synthetic lethal combinations. Second, dominant mutations in KAR2 are allele-specific suppressors for the temperature-sensitive growth and translocation defect of sec63-1. Third, the sec63-1, unlike other translocation defective mutations, results in the induction of KAR2 mRNA levels. Taken together, these genetic interactions suggest that Kar2p and Sec63p interact in vivo in a manner similar to that of the E. coli HSP70, DnaK, and DnaJ. We propose that the interaction between these two proteins is critical to their function in protein translocation.

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  1. Adams A. E., Botstein D., Drubin D. G. A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science. 1989 Jan 13;243(4888):231–233. doi: 10.1126/science.2643162. [DOI] [PubMed] [Google Scholar]
  2. Alfano C., McMacken R. Ordered assembly of nucleoprotein structures at the bacteriophage lambda replication origin during the initiation of DNA replication. J Biol Chem. 1989 Jun 25;264(18):10699–10708. [PubMed] [Google Scholar]
  3. Amaya Y., Nakano A., Ito K., Mori M. Isolation of a yeast gene, SRH1, that encodes a homologue of the 54K subunit of mammalian signal recognition particle. J Biochem. 1990 Mar;107(3):457–463. doi: 10.1093/oxfordjournals.jbchem.a123067. [DOI] [PubMed] [Google Scholar]
  4. Atencio D. P., Yaffe M. P. MAS5, a yeast homolog of DnaJ involved in mitochondrial protein import. Mol Cell Biol. 1992 Jan;12(1):283–291. doi: 10.1128/mcb.12.1.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blumberg H., Silver P. A. A homologue of the bacterial heat-shock gene DnaJ that alters protein sorting in yeast. Nature. 1991 Feb 14;349(6310):627–630. doi: 10.1038/349627a0. [DOI] [PubMed] [Google Scholar]
  6. Boeke J. D., LaCroute F., Fink G. R. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet. 1984;197(2):345–346. doi: 10.1007/BF00330984. [DOI] [PubMed] [Google Scholar]
  7. Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Caplan A. J., Cyr D. M., Douglas M. G. YDJ1p facilitates polypeptide translocation across different intracellular membranes by a conserved mechanism. Cell. 1992 Dec 24;71(7):1143–1155. doi: 10.1016/s0092-8674(05)80063-7. [DOI] [PubMed] [Google Scholar]
  9. Caplan A. J., Douglas M. G. Characterization of YDJ1: a yeast homologue of the bacterial dnaJ protein. J Cell Biol. 1991 Aug;114(4):609–621. doi: 10.1083/jcb.114.4.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chappell T. G., Konforti B. B., Schmid S. L., Rothman J. E. The ATPase core of a clathrin uncoating protein. J Biol Chem. 1987 Jan 15;262(2):746–751. [PubMed] [Google Scholar]
  11. Chirico W. J., Waters M. G., Blobel G. 70K heat shock related proteins stimulate protein translocation into microsomes. Nature. 1988 Apr 28;332(6167):805–810. doi: 10.1038/332805a0. [DOI] [PubMed] [Google Scholar]
  12. Cleves A. E., Bankaitis V. A. Secretory pathway function in Saccharomyces cerevisiae. Adv Microb Physiol. 1992;33:73–144. doi: 10.1016/s0065-2911(08)60216-7. [DOI] [PubMed] [Google Scholar]
  13. Copeland C. S., Doms R. W., Bolzau E. M., Webster R. G., Helenius A. Assembly of influenza hemagglutinin trimers and its role in intracellular transport. J Cell Biol. 1986 Oct;103(4):1179–1191. doi: 10.1083/jcb.103.4.1179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Craig E. A. The heat shock response. CRC Crit Rev Biochem. 1985;18(3):239–280. doi: 10.3109/10409238509085135. [DOI] [PubMed] [Google Scholar]
  15. Cyr D. M., Lu X., Douglas M. G. Regulation of Hsp70 function by a eukaryotic DnaJ homolog. J Biol Chem. 1992 Oct 15;267(29):20927–20931. [PubMed] [Google Scholar]
  16. Deshaies R. J., Koch B. D., Werner-Washburne M., Craig E. A., Schekman R. A subfamily of stress proteins facilitates translocation of secretory and mitochondrial precursor polypeptides. Nature. 1988 Apr 28;332(6167):800–805. doi: 10.1038/332800a0. [DOI] [PubMed] [Google Scholar]
  17. Deshaies R. J., Sanders S. L., Feldheim D. A., Schekman R. Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature. 1991 Feb 28;349(6312):806–808. doi: 10.1038/349806a0. [DOI] [PubMed] [Google Scholar]
  18. Deshaies R. J., Schekman R. A yeast mutant defective at an early stage in import of secretory protein precursors into the endoplasmic reticulum. J Cell Biol. 1987 Aug;105(2):633–645. doi: 10.1083/jcb.105.2.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Deshaies R. J., Schekman R. SEC62 encodes a putative membrane protein required for protein translocation into the yeast endoplasmic reticulum. J Cell Biol. 1989 Dec;109(6 Pt 1):2653–2664. doi: 10.1083/jcb.109.6.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Deshaies R. J., Schekman R. Structural and functional dissection of Sec62p, a membrane-bound component of the yeast endoplasmic reticulum protein import machinery. Mol Cell Biol. 1990 Nov;10(11):6024–6035. doi: 10.1128/mcb.10.11.6024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Dorner A. J., Bole D. G., Kaufman R. J. The relationship of N-linked glycosylation and heavy chain-binding protein association with the secretion of glycoproteins. J Cell Biol. 1987 Dec;105(6 Pt 1):2665–2674. doi: 10.1083/jcb.105.6.2665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Feldheim D., Rothblatt J., Schekman R. Topology and functional domains of Sec63p, an endoplasmic reticulum membrane protein required for secretory protein translocation. Mol Cell Biol. 1992 Jul;12(7):3288–3296. doi: 10.1128/mcb.12.7.3288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Felici F., Cesareni G., Hughes J. M. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol Cell Biol. 1989 Aug;9(8):3260–3268. doi: 10.1128/mcb.9.8.3260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Flajnik M. F., Canel C., Kramer J., Kasahara M. Which came first, MHC class I or class II? Immunogenetics. 1991;33(5-6):295–300. doi: 10.1007/BF00216688. [DOI] [PubMed] [Google Scholar]
  25. Gething M. J., McCammon K., Sambrook J. Expression of wild-type and mutant forms of influenza hemagglutinin: the role of folding in intracellular transport. Cell. 1986 Sep 12;46(6):939–950. doi: 10.1016/0092-8674(86)90076-0. [DOI] [PubMed] [Google Scholar]
  26. Gething M. J., Sambrook J. Protein folding in the cell. Nature. 1992 Jan 2;355(6355):33–45. doi: 10.1038/355033a0. [DOI] [PubMed] [Google Scholar]
  27. Haas I. G., Wabl M. Immunoglobulin heavy chain binding protein. Nature. 1983 Nov 24;306(5941):387–389. doi: 10.1038/306387a0. [DOI] [PubMed] [Google Scholar]
  28. Hann B. C., Poritz M. A., Walter P. Saccharomyces cerevisiae and Schizosaccharomyces pombe contain a homologue to the 54-kD subunit of the signal recognition particle that in S. cerevisiae is essential for growth. J Cell Biol. 1989 Dec;109(6 Pt 2):3223–3230. doi: 10.1083/jcb.109.6.3223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Hann B. C., Stirling C. J., Walter P. SEC65 gene product is a subunit of the yeast signal recognition particle required for its integrity. Nature. 1992 Apr 9;356(6369):532–533. doi: 10.1038/356532a0. [DOI] [PubMed] [Google Scholar]
  30. Hann B. C., Walter P. The signal recognition particle in S. cerevisiae. Cell. 1991 Oct 4;67(1):131–144. doi: 10.1016/0092-8674(91)90577-l. [DOI] [PubMed] [Google Scholar]
  31. Hansen W., Garcia P. D., Walter P. In vitro protein translocation across the yeast endoplasmic reticulum: ATP-dependent posttranslational translocation of the prepro-alpha-factor. Cell. 1986 May 9;45(3):397–406. doi: 10.1016/0092-8674(86)90325-9. [DOI] [PubMed] [Google Scholar]
  32. Hemmings B. A., Zubenko G. S., Hasilik A., Jones E. W. Mutant defective in processing of an enzyme located in the lysosome-like vacuole of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1981 Jan;78(1):435–439. doi: 10.1073/pnas.78.1.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hendershot L., Bole D., Köhler G., Kearney J. F. Assembly and secretion of heavy chains that do not associate posttranslationally with immunoglobulin heavy chain-binding protein. J Cell Biol. 1987 Mar;104(3):761–767. doi: 10.1083/jcb.104.3.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hoffman C. S., Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 1987;57(2-3):267–272. doi: 10.1016/0378-1119(87)90131-4. [DOI] [PubMed] [Google Scholar]
  35. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  36. Huffaker T. C., Hoyt M. A., Botstein D. Genetic analysis of the yeast cytoskeleton. Annu Rev Genet. 1987;21:259–284. doi: 10.1146/annurev.ge.21.120187.001355. [DOI] [PubMed] [Google Scholar]
  37. Hurtley S. M., Bole D. G., Hoover-Litty H., Helenius A., Copeland C. S. Interactions of misfolded influenza virus hemagglutinin with binding protein (BiP). J Cell Biol. 1989 Jun;108(6):2117–2126. doi: 10.1083/jcb.108.6.2117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kassenbrock C. K., Garcia P. D., Walter P., Kelly R. B. Heavy-chain binding protein recognizes aberrant polypeptides translocated in vitro. Nature. 1988 May 5;333(6168):90–93. doi: 10.1038/333090a0. [DOI] [PubMed] [Google Scholar]
  40. Kohno K., Normington K., Sambrook J., Gething M. J., Mori K. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol. 1993 Feb;13(2):877–890. doi: 10.1128/mcb.13.2.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kozutsumi Y., Segal M., Normington K., Gething M. J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 1988 Mar 31;332(6163):462–464. doi: 10.1038/332462a0. [DOI] [PubMed] [Google Scholar]
  42. Liberek K., Georgopoulos C., Zylicz M. Role of the Escherichia coli DnaK and DnaJ heat shock proteins in the initiation of bacteriophage lambda DNA replication. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6632–6636. doi: 10.1073/pnas.85.18.6632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Liberek K., Marszalek J., Ang D., Georgopoulos C., Zylicz M. Escherichia coli DnaJ and GrpE heat shock proteins jointly stimulate ATPase activity of DnaK. Proc Natl Acad Sci U S A. 1991 Apr 1;88(7):2874–2878. doi: 10.1073/pnas.88.7.2874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Luke M. M., Sutton A., Arndt K. T. Characterization of SIS1, a Saccharomyces cerevisiae homologue of bacterial dnaJ proteins. J Cell Biol. 1991 Aug;114(4):623–638. doi: 10.1083/jcb.114.4.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Morrison S. L., Scharff M. D. Heavy chain-producing variants of a mouse myeloma cell line. J Immunol. 1975 Feb;114(2 Pt 1):655–659. [PubMed] [Google Scholar]
  46. Munro S., Pelham H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. doi: 10.1016/0092-8674(86)90746-4. [DOI] [PubMed] [Google Scholar]
  47. Müsch A., Wiedmann M., Rapoport T. A. Yeast Sec proteins interact with polypeptides traversing the endoplasmic reticulum membrane. Cell. 1992 Apr 17;69(2):343–352. doi: 10.1016/0092-8674(92)90414-8. [DOI] [PubMed] [Google Scholar]
  48. Nelson M. K., Kurihara T., Silver P. A. Extragenic suppressors of mutations in the cytoplasmic C terminus of SEC63 define five genes in Saccharomyces cerevisiae. Genetics. 1993 May;134(1):159–173. doi: 10.1093/genetics/134.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Normington K., Kohno K., Kozutsumi Y., Gething M. J., Sambrook J. S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell. 1989 Jun 30;57(7):1223–1236. doi: 10.1016/0092-8674(89)90059-7. [DOI] [PubMed] [Google Scholar]
  50. Ogg S. C., Poritz M. A., Walter P. Signal recognition particle receptor is important for cell growth and protein secretion in Saccharomyces cerevisiae. Mol Biol Cell. 1992 Aug;3(8):895–911. doi: 10.1091/mbc.3.8.895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
  52. Phillips G. J., Silhavy T. J. Heat-shock proteins DnaK and GroEL facilitate export of LacZ hybrid proteins in E. coli. Nature. 1990 Apr 26;344(6269):882–884. doi: 10.1038/344882a0. [DOI] [PubMed] [Google Scholar]
  53. Polaina J., Conde J. Genes involved in the control of nuclear fusion during the sexual cycle of Saccharomyces cerevisiae. Mol Gen Genet. 1982;186(2):253–258. doi: 10.1007/BF00331858. [DOI] [PubMed] [Google Scholar]
  54. Pouysségur J., Shiu R. P., Pastan I. Induction of two transformation-sensitive membrane polypeptides in normal fibroblasts by a block in glycoprotein synthesis or glucose deprivation. Cell. 1977 Aug;11(4):941–947. doi: 10.1016/0092-8674(77)90305-1. [DOI] [PubMed] [Google Scholar]
  55. Rapoport T. A. Transport of proteins across the endoplasmic reticulum membrane. Science. 1992 Nov 6;258(5084):931–936. doi: 10.1126/science.1332192. [DOI] [PubMed] [Google Scholar]
  56. Rippmann F., Taylor W. R., Rothbard J. B., Green N. M. A hypothetical model for the peptide binding domain of hsp70 based on the peptide binding domain of HLA. EMBO J. 1991 May;10(5):1053–1059. doi: 10.1002/j.1460-2075.1991.tb08044.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Rose M. D., Misra L. M., Vogel J. P. KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell. 1989 Jun 30;57(7):1211–1221. doi: 10.1016/0092-8674(89)90058-5. [DOI] [PubMed] [Google Scholar]
  58. Rothblatt J. A., Deshaies R. J., Sanders S. L., Daum G., Schekman R. Multiple genes are required for proper insertion of secretory proteins into the endoplasmic reticulum in yeast. J Cell Biol. 1989 Dec;109(6 Pt 1):2641–2652. doi: 10.1083/jcb.109.6.2641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rothblatt J. A., Meyer D. I. Secretion in yeast: translocation and glycosylation of prepro-alpha-factor in vitro can occur via an ATP-dependent post-translational mechanism. EMBO J. 1986 May;5(5):1031–1036. doi: 10.1002/j.1460-2075.1986.tb04318.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Sadler I., Chiang A., Kurihara T., Rothblatt J., Way J., Silver P. A yeast gene important for protein assembly into the endoplasmic reticulum and the nucleus has homology to DnaJ, an Escherichia coli heat shock protein. J Cell Biol. 1989 Dec;109(6 Pt 1):2665–2675. doi: 10.1083/jcb.109.6.2665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Salminen A., Novick P. J. A ras-like protein is required for a post-Golgi event in yeast secretion. Cell. 1987 May 22;49(4):527–538. doi: 10.1016/0092-8674(87)90455-7. [DOI] [PubMed] [Google Scholar]
  62. Sanders S. L., Schekman R. Polypeptide translocation across the endoplasmic reticulum membrane. J Biol Chem. 1992 Jul 15;267(20):13791–13794. [PubMed] [Google Scholar]
  63. Sanders S. L., Whitfield K. M., Vogel J. P., Rose M. D., Schekman R. W. Sec61p and BiP directly facilitate polypeptide translocation into the ER. Cell. 1992 Apr 17;69(2):353–365. doi: 10.1016/0092-8674(92)90415-9. [DOI] [PubMed] [Google Scholar]
  64. Sharma S., Rodgers L., Brandsma J., Gething M. J., Sambrook J. SV40 T antigen and the exocytotic pathway. EMBO J. 1985 Jun;4(6):1479–1489. doi: 10.1002/j.1460-2075.1985.tb03806.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Shiu R. P., Pouyssegur J., Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteinsin Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3840–3844. doi: 10.1073/pnas.74.9.3840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Stevens T., Esmon B., Schekman R. Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell. 1982 Sep;30(2):439–448. doi: 10.1016/0092-8674(82)90241-0. [DOI] [PubMed] [Google Scholar]
  67. Stirling C. J., Hewitt E. W. The S. cerevisiae SEC65 gene encodes a component of yeast signal recognition particle with homology to human SRP19. Nature. 1992 Apr 9;356(6369):534–537. doi: 10.1038/356534a0. [DOI] [PubMed] [Google Scholar]
  68. Stirling C. J., Rothblatt J., Hosobuchi M., Deshaies R., Schekman R. Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum. Mol Biol Cell. 1992 Feb;3(2):129–142. doi: 10.1091/mbc.3.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Tilly K., Yarmolinsky M. Participation of Escherichia coli heat shock proteins DnaJ, DnaK, and GrpE in P1 plasmid replication. J Bacteriol. 1989 Nov;171(11):6025–6029. doi: 10.1128/jb.171.11.6025-6029.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Tokunaga M., Kawamura A., Kohno K. Purification and characterization of BiP/Kar2 protein from Saccharomyces cerevisiae. J Biol Chem. 1992 Sep 5;267(25):17553–17559. [PubMed] [Google Scholar]
  71. Toyn J., Hibbs A. R., Sanz P., Crowe J., Meyer D. I. In vivo and in vitro analysis of ptl1, a yeast ts mutant with a membrane-associated defect in protein translocation. EMBO J. 1988 Dec 20;7(13):4347–4353. doi: 10.1002/j.1460-2075.1988.tb03333.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Vogel J. P., Misra L. M., Rose M. D. Loss of BiP/GRP78 function blocks translocation of secretory proteins in yeast. J Cell Biol. 1990 Jun;110(6):1885–1895. doi: 10.1083/jcb.110.6.1885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Waters M. G., Blobel G. Secretory protein translocation in a yeast cell-free system can occur posttranslationally and requires ATP hydrolysis. J Cell Biol. 1986 May;102(5):1543–1550. doi: 10.1083/jcb.102.5.1543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Welch W. J., Feramisco J. R. Rapid purification of mammalian 70,000-dalton stress proteins: affinity of the proteins for nucleotides. Mol Cell Biol. 1985 Jun;5(6):1229–1237. doi: 10.1128/mcb.5.6.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Wickner S. H. Three Escherichia coli heat shock proteins are required for P1 plasmid DNA replication: formation of an active complex between E. coli DnaJ protein and the P1 initiator protein. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2690–2694. doi: 10.1073/pnas.87.7.2690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wild J., Altman E., Yura T., Gross C. A. DnaK and DnaJ heat shock proteins participate in protein export in Escherichia coli. Genes Dev. 1992 Jul;6(7):1165–1172. doi: 10.1101/gad.6.7.1165. [DOI] [PubMed] [Google Scholar]
  77. Zylicz M., LeBowitz J. H., McMacken R., Georgopoulos C. The dnaK protein of Escherichia coli possesses an ATPase and autophosphorylating activity and is essential in an in vitro DNA replication system. Proc Natl Acad Sci U S A. 1983 Nov;80(21):6431–6435. doi: 10.1073/pnas.80.21.6431. [DOI] [PMC free article] [PubMed] [Google Scholar]

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