Genetic Analysis of Protein Translocation

  • Thomas J. SilhavyEmail author
  • Angela M. Mitchell


Cells in all domains of life must translocate newly synthesized proteins both across membranes and into membranes. In eukaryotes, proteins are translocated into the lumen of the ER or the ER membrane. In prokaryotes, proteins are translocated into the cytoplasmic membrane or through the membrane into the periplasm for Gram-negative bacteria or the extracellular space for Gram-positive bacteria. Much of what we know about protein translocation was learned through genetic selections and screens utilizing lacZ gene fusions in Escherichia coli. This review covers the basic principles of protein translocation and how they were discovered and developed. In particular, we discuss how lacZ gene fusions and the phenotypes conferred were exploited to identify the genes involved in protein translocation and provide insights into their mechanisms of action. These approaches, which allowed the elucidation of processes that are conserved throughout the domains of life, illustrate the power of seemingly simple experiments.


Gene fusion Protein translocation Sec Protein secretion Prl mutant 



Funding was provided by National Institute of General Medical Sciences (Grant No. R35GM118024).


  1. 1.
    Bladen HA, Mergenhagen SE (1964) Ultrastructure of Veillonella and morphological correlation of an outer membrane with particles associated with endotoxic activity. J Bacteriol 88:1482–1492PubMedPubMedCentralGoogle Scholar
  2. 2.
    Mitchell P (1961) Approaches to the analysis of specific membrane transport. In: Goodwin TW OL (ed) Biological structure and function. Academic Press, New York, pp 581–603Google Scholar
  3. 3.
    Glauert AM, Thornley MJ (1969) The topography of the bacterial cell wall. Annu Rev Microbiol 23:159–198. CrossRefPubMedGoogle Scholar
  4. 4.
    Miura T, Mizushima S (1968) Separation by density gradient centrifugation of two types of membranes from spheroplast membrane of Escherichia coli K12. Biochim Biophys Acta 150(1):159–161CrossRefPubMedGoogle Scholar
  5. 5.
    Schnaitman CA (1970) Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J Bacteriol 104(2):890–901PubMedPubMedCentralGoogle Scholar
  6. 6.
    Osborn MJ, Gander JE, Parisi E, Carson J (1972) Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247(12):3962–3972PubMedGoogle Scholar
  7. 7.
    Heppel LA (1967) Selective release of enzymes from bacteria. Science 156(3781):1451–1455CrossRefPubMedGoogle Scholar
  8. 8.
    Silhavy TJ, Kahne D, Walker S (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2(5):a000414. CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Palade G (1975) Intracellular aspects of the process of protein synthesis. Science 189(4200):347–358CrossRefPubMedGoogle Scholar
  10. 10.
    Blobel GaS DD (1971) Ribosome-membrane interaction in eukaryotic cells. In: Manson LA (ed) Biomembranes. Plenum Press, New York, pp 193–195CrossRefGoogle Scholar
  11. 11.
    Milstein C, Brownlee GG, Harrison TM, Mathews MB (1972) A possible precursor of immunoglobulin light chains. Nat New Biol 239(91):117–120CrossRefPubMedGoogle Scholar
  12. 12.
    Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J Cell Biol 67(3):852–862CrossRefPubMedGoogle Scholar
  13. 13.
    Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67(3):835–851CrossRefPubMedGoogle Scholar
  14. 14.
    Inouye H, Beckwith J (1977) Synthesis and processing of an Escherichia coli alkaline phosphatase precursor in vitro. Proc Natl Acad Sci USA 74(4):1440–1444CrossRefPubMedGoogle Scholar
  15. 15.
    Hazelbauer GL (1975) Role of the receptor for bacteriophage lambda in the functioning of the maltose chemoreceptor of Escherichia coli. J Bacteriol 124(1):119–126PubMedPubMedCentralGoogle Scholar
  16. 16.
    Szmelcman S, Hofnung M (1975) Maltose transport in Escherichia coli K-12: involvement of the bacteriophage lambda receptor. J Bacteriol 124(1):112–118PubMedPubMedCentralGoogle Scholar
  17. 17.
    Randall-Hazelbauer L, Schwartz M (1973) Isolation of the bacteriophage lambda receptor from Escherichia coli. J Bacteriol 116(3):1436–1446PubMedPubMedCentralGoogle Scholar
  18. 18.
    Payne JW, Gilvarg C (1968) Size restriction on peptide utilization in Escherichia coli. J Biol Chem 243(23):6291–6299PubMedGoogle Scholar
  19. 19.
    Ferenci T, Boos W (1980) The role of the Escherichia coli lambda receptor in the transport of maltose and maltodextrins. J Supramol Struct 13(1):101–116. CrossRefPubMedGoogle Scholar
  20. 20.
    Emr SD, Schwartz M, Silhavy TJ (1978) Mutations altering the cellular localization of the phage lambda receptor, an Escherichia coli outer membrane protein. Proc Natl Acad Sci USA 75(12):5802–5806CrossRefPubMedGoogle Scholar
  21. 21.
    Driessen AJ, Nouwen N (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667. CrossRefPubMedGoogle Scholar
  22. 22.
    Brundage L, Hendrick JP, Schiebel E, Driessen AJ, Wickner W (1990) The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation. Cell 62(4):649–657CrossRefPubMedGoogle Scholar
  23. 23.
    Nishiyama K, Hanada M, Tokuda H (1994) Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature. EMBO J 13(14):3272–3277CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Schulze RJ, Komar J, Botte M, Allen WJ, Whitehouse S, Gold VA, Lycklama ANJA, Huard K, Berger I, Schaffitzel C, Collinson I (2014) Membrane protein insertion and proton-motive-force-dependent secretion through the bacterial holo-translocon SecYEG-SecDF-YajC-YidC. Proc Natl Acad Sci USA 111(13):4844–4849. CrossRefPubMedGoogle Scholar
  25. 25.
    Tsukazaki T, Mori H, Echizen Y, Ishitani R, Fukai S, Tanaka T, Perederina A, Vassylyev DG, Kohno T, Maturana AD, Ito K, Nureki O (2011) Structure and function of a membrane component SecDF that enhances protein export. Nature 474(7350):235–238. CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Kuhn A, Kiefer D (2017) Membrane protein insertase YidC in bacteria and archaea. Mol Microbiol 103(4):590–594. CrossRefPubMedGoogle Scholar
  27. 27.
    Crane JM, Randall LL (2017) The Sec System: protein export in Escherichia coli. EcoSal Plus. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Collier DN, Bankaitis VA, Weiss JB, Bassford PJ Jr (1988) The antifolding activity of SecB promotes the export of the E. coli maltose-binding protein. Cell 53(2):273–283CrossRefPubMedGoogle Scholar
  29. 29.
    Ulbrandt ND, Newitt JA, Bernstein HD (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88(2):187–196CrossRefPubMedGoogle Scholar
  30. 30.
    Fekkes P, van der Does C, Driessen AJ (1997) The molecular chaperone SecB is released from the carboxy-terminus of SecA during initiation of precursor protein translocation. EMBO J 16(20):6105–6113. CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Dalbey RE, Wickner W (1985) Leader peptidase catalyzes the release of exported proteins from the outer surface of the Escherichia coli plasma membrane. J Biol Chem 260(29):15925–15931PubMedGoogle Scholar
  32. 32.
    Yamagata H, Taguchi N, Daishima K, Mizushima S (1983) Genetic characterization of a gene for prolipoprotein signal peptidase in Escherichia coli. Mol Gen Genet: MGG 192(1–2):10–14CrossRefPubMedGoogle Scholar
  33. 33.
    Inouye S, Franceschini T, Sato M, Itakura K, Inouye M (1983) Prolipoprotein signal peptidase of Escherichia coli requires a cysteine residue at the cleavage site. EMBO J 2(1):87–91CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bernstein HD, Poritz MA, Strub K, Hoben PJ, Brenner S, Walter P (1989) Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature 340(6233):482–486. CrossRefPubMedGoogle Scholar
  35. 35.
    Benzer S, Champe SP (1962) A change from nonsense to sense in the genetic code. Proc Natl Acad Sci USA 48:1114–1121CrossRefPubMedGoogle Scholar
  36. 36.
    Crick FH, Barnett L, Brenner S, Watts-Tobin RJ (1961) General nature of the genetic code for proteins. Nature 192:1227–1232CrossRefPubMedGoogle Scholar
  37. 37.
    Jacob F, Ullmann A, Monod J (1965) Deletions fusionnant loperon lactose Et Un Operon Purine Chez Escherichia Coli. J Mol Biol 13 (3):704–704&. CrossRefGoogle Scholar
  38. 38.
    Beckwith JR, Signer ER, Epstein W (1966) Transposition of the Lac region of E. coli. Cold Spring Harb Symp Quant Biol 31:393–401CrossRefPubMedGoogle Scholar
  39. 39.
    Casadaban MJ (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104(3):541–555CrossRefPubMedGoogle Scholar
  40. 40.
    Schwartz M (1987) The maltose regulon. In: Neidhard FC (ed) Escherichia coli and Salmonella typhimurium: cellular and molecular biology, vol 2. American Society for Microbiology, Washington DC, pp 1482–1502Google Scholar
  41. 41.
    Kellermann O, Szmelcman S (1974) Active transport of maltose in Escherichia coli K12. Eur J Biochem 47(1):139–149. doiCrossRefPubMedGoogle Scholar
  42. 42.
    Shuman HA, Silhavy TJ (1981) Identification of the malK gene product. A peripheral membrane component of the Escherichia coli maltose transport system. J Biol Chem 256(2):560–562PubMedGoogle Scholar
  43. 43.
    Shuman HA, Silhavy TJ, Beckwith JR (1980) Labeling of proteins with beta-galactosidase by gene fusion. Identification of a cytoplasmic membrane component of the Escherichia coli maltose transport system. J Biol Chem 255(1):168–174PubMedGoogle Scholar
  44. 44.
    Dassa E, Hofnung M (1985) Sequence of gene malG in E. coli K12: homologies between integral membrane components from binding protein-dependent transport systems. EMBO J 4(9):2287–2293CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Cole ST, Raibaud O (1986) The nucleotide sequence of the malT gene encoding the positive regulator of the Escherichia coli maltose regulon. Gene 42(2):201–208CrossRefPubMedGoogle Scholar
  46. 46.
    Silhavy TJ, Shuman HA, Beckwith J, Schwartz M (1977) Use of gene fusions to study outer membrane protein localization in Escherichia coli. Proc Natl Acad Sci USA 74(12):5411–5415CrossRefPubMedGoogle Scholar
  47. 47.
    Bassford P, Beckwith J (1979) Escherichia coli mutants accumulating the precursor of a secreted protein in the cytoplasm. Nature 277(5697):538–541CrossRefPubMedGoogle Scholar
  48. 48.
    Davidson AL, Shuman HA, Nikaido H (1992) Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci USA 89(6):2360–2364CrossRefPubMedGoogle Scholar
  49. 49.
    Schwartz M, Hofnung M (1967) La maltodextrine phosphorylase d’ Escherichia coli. Eur J Biochem 2(2):132–145. doiCrossRefPubMedGoogle Scholar
  50. 50.
    Hatfield D, Hofnung M, Schwartz M (1969) Genetic analysis of the maltose A region in Escherichia coli. J Bacteriol 98(2):559–567PubMedPubMedCentralGoogle Scholar
  51. 51.
    Silhavy TJ, Casadaban MJ, Shuman HA, Beckwith JR (1976) Conversion of beta-galactosidase to a membrane-bound state by gene fusion. Proc Natl Acad Sci USA 73(10):3423–3427CrossRefPubMedGoogle Scholar
  52. 52.
    Froshauer S, Green GN, Boyd D, McGovern K, Beckwith J (1988) Genetic analysis of the membrane insertion and topology of MalF, a cytoplasmic membrane protein of Escherichia coli. J Mol Biol 200(3):501–511CrossRefPubMedGoogle Scholar
  53. 53.
    Oliver DB, Beckwith J (1981) E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25(3):765–772CrossRefPubMedGoogle Scholar
  54. 54.
    Bassford PJ Jr, Silhavy TJ, Beckwith JR (1979) Use of gene fusion to study secretion of maltose-binding protein into Escherichia coli periplasm. J Bacteriol 139(1):19–31PubMedPubMedCentralGoogle Scholar
  55. 55.
    Dwyer RS, Malinverni JC, Boyd D, Beckwith J, Silhavy TJ (2014) Folding LacZ in the periplasm of Escherichia coli. J Bacteriol 196(18):3343–3350. CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    van Stelten J, Silva F, Belin D, Silhavy TJ (2009) Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325(5941):753–756. CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Takahashi N, Gruber CC, Yang JH, Liu X, Braff D, Yashaswini CN, Bhubhanil S, Furuta Y, Andreescu S, Collins JJ, Walker GC (2017) Lethality of MalE-LacZ hybrid protein shares mechanistic attributes with oxidative component of antibiotic lethality. Proc Natl Acad Sci USA. CrossRefPubMedGoogle Scholar
  58. 58.
    Manoil C, Beckwith J (1986) A genetic approach to analyzing membrane protein topology. Science 233(4771):1403–1408CrossRefPubMedGoogle Scholar
  59. 59.
    Bardwell JC, McGovern K, Beckwith J (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67(3):581–589CrossRefPubMedGoogle Scholar
  60. 60.
    Bowers CW, Lau F, Silhavy TJ (2003) Secretion of LamB-LacZ by the signal recognition particle pathway of Escherichia coli. J Bacteriol 185(19):5697–5705CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Emr SD, Hedgpeth J, Clement JM, Silhavy TJ, Hofnung M (1980) Sequence analysis of mutations that prevent export of lambda receptor, an Escherichia coli outer membrane protein. Nature 285(5760):82–85CrossRefPubMedGoogle Scholar
  62. 62.
    Bedouelle H, Bassford PJ Jr, Fowler AV, Zabin I, Beckwith J, Hofnung M (1980) Mutations which alter the function of the signal sequence of the maltose binding protein of Escherichia coli. Nature 285(5760):78–81CrossRefPubMedGoogle Scholar
  63. 63.
    Jarvik J, Botstein D (1975) Conditional-lethal mutations that suppress genetic defects in morphogenesis by altering structural proteins. Proc Natl Acad Sci USA 72(7):2738–2742CrossRefPubMedGoogle Scholar
  64. 64.
    Li M, Moyle H, Susskind MM (1994) Target of the transcriptional activation function of phage lambdacI protein. Science 263(5143):75–77CrossRefPubMedGoogle Scholar
  65. 65.
    Nickels BE, Dove SL, Murakami KS, Darst SA, Hochschild A (2002) Protein-protein and protein-DNA interactions of sigma70 region 4 involved in transcription activation by lambdacI. J Mol Biol 324(1):17–34CrossRefPubMedGoogle Scholar
  66. 66.
    Misra R, Benson SA (1989) A novel mutation, cog, which results in production of a new porin protein (OmpG) of Escherichia coli K-12. J Bacteriol 171(8):4105–4111CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Misra R, Benson SA (1988) Isolation and characterization of OmpC porin mutants with altered pore properties. J Bacteriol 170(2):528–533CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Sampson BA, Misra R, Benson SA (1989) Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability. Genetics 122(3):491–501PubMedPubMedCentralGoogle Scholar
  69. 69.
    Shuman HA, Beckwith J (1979) Escherichia coli K-12 mutants that allow transport of maltose via the beta-galactoside transport system. J Bacteriol 137(1):365–373PubMedPubMedCentralGoogle Scholar
  70. 70.
    Emr SD, Hanley-Way S, Silhavy TJ (1981) Suppressor mutations that restore export of a protein with a defective signal sequence. Cell 23(1):79–88CrossRefPubMedGoogle Scholar
  71. 71.
    Shultz J, Silhavy TJ, Berman ML, Fiil N, Emr SD (1982) A previously unidentified gene in the spc operon of Escherichia coli K12 specifies a component of the protein export machinery. Cell 31(1):227–235CrossRefPubMedGoogle Scholar
  72. 72.
    Ito K, Wittekind M, Nomura M, Shiba K, Yura T, Miura A, Nashimoto H (1983) A temperature-sensitive mutant of E. coli exhibiting slow processing of exported proteins. Cell 32(3):789–797CrossRefPubMedGoogle Scholar
  73. 73.
    Post LE, Arfsten AE, Davis GR, Nomura M (1980) DNA sequence of the promoter region for the alpha ribosomal protein operon in Escherichia coli. J Biol Chem 255(10):4653–4659PubMedGoogle Scholar
  74. 74.
    Fikes JD, Bassford PJ Jr (1989) Novel secA alleles improve export of maltose-binding protein synthesized with a defective signal peptide. J Bacteriol 171(1):402–409CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Stader J, Gansheroff LJ, Silhavy TJ (1989) New suppressors of signal-sequence mutations, prlG, are linked tightly to the secE gene of Escherichia coli. Genes Dev 3(7):1045–1052CrossRefPubMedGoogle Scholar
  76. 76.
    Schatz PJ, Riggs PD, Jacq A, Fath MJ, Beckwith J (1989) The secE gene encodes an integral membrane protein required for protein export in Escherichia coli. Genes Dev 3(7):1035–1044CrossRefPubMedGoogle Scholar
  77. 77.
    Bost S, Belin D (1997) prl mutations in the Escherichia coli secG gene. J Biol Chem 272(7):4087–4093CrossRefPubMedGoogle Scholar
  78. 78.
    Derman AI, Puziss JW, Bassford PJ Jr, Beckwith J (1993) A signal sequence is not required for protein export in prlA mutants of Escherichia coli. EMBO J 12(3):879–888CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Flower AM, Doebele RC, Silhavy TJ (1994) PrlA and PrlG suppressors reduce the requirement for signal sequence recognition. J Bacteriol 176(18):5607–5614CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Osborne RS, Silhavy TJ (1993) PrlA suppressor mutations cluster in regions corresponding to three distinct topological domains. EMBO J 12(9):3391–3398CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Flower AM, Osborne RS, Silhavy TJ (1995) The allele-specific synthetic lethality of prlA-prlG double mutants predicts interactive domains of SecY and SecE. EMBO J 14(5):884–893CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Harris CR, Silhavy TJ (1999) Mapping an interface of SecY (PrlA) and SecE (PrlG) by using synthetic phenotypes and in vivo cross-linking. J Bacteriol 181(11):3438–3444PubMedPubMedCentralGoogle Scholar
  83. 83.
    van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a protein-conducting channel. Nature 427(6969):36–44. CrossRefPubMedGoogle Scholar
  84. 84.
    Corey Robin A, Allen William J, Komar J, Masiulis S, Menzies S, Robson A, Collinson I (2016) Unlocking the bacterial SecY translocon. Structure 24(4):518–527. CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Smith MA, Clemons WM Jr, DeMars CJ, Flower AM (2005) Modeling the effects of prl mutations on the Escherichia coli SecY complex. J Bacteriol 187(18):6454–6465. CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Huie JL, Silhavy TJ (1995) Suppression of signal sequence defects and azide resistance in Escherichia coli commonly result from the same mutations in secA. J Bacteriol 177(12):3518–3526CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Lederberg J (1950) The selection of genetic recombinations with bacterial growth inhibitors. J Bacteriol 59(2):211–215PubMedPubMedCentralGoogle Scholar
  88. 88.
    Schmidt M, Ding H, Ramamurthy V, Mukerji I, Oliver D (2000) Nucleotide binding activity of SecA homodimer is conformationally regulated by temperature and altered by prlD and azi mutations. J Biol Chem 275(20):15440–15448. CrossRefPubMedGoogle Scholar
  89. 89.
    Oliver DB, Beckwith J (1982) Identification of a new gene (secA) and gene product involved in the secretion of envelope proteins in Escherichia coli. J Bacteriol 150(2):686–691PubMedPubMedCentralGoogle Scholar
  90. 90.
    Kumamoto CA, Beckwith J (1983) Mutations in a new gene, secB, cause defective protein localization in Escherichia coli. J Bacteriol 154(1):253–260PubMedPubMedCentralGoogle Scholar
  91. 91.
    Gardel C, Benson S, Hunt J, Michaelis S, Beckwith J (1987) secD, a new gene involved in protein export in Escherichia coli. J Bacteriol 169(3):1286–1290CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Oliver DB, Beckwith J (1982) Regulation of a membrane component required for protein secretion in Escherichia coli. Cell 30(1):311–319CrossRefPubMedGoogle Scholar
  93. 93.
    Nakatogawa H, Murakami A, Ito K (2004) Control of SecA and SecM translation by protein secretion. Curr Opin Microbiol 7(2):145–150. CrossRefPubMedGoogle Scholar
  94. 94.
    Riggs PD, Derman AI, Beckwith J (1988) A mutation affecting the regulation of a secA-lacZ fusion defines a new sec gene. Genetics 118(4):571–579PubMedPubMedCentralGoogle Scholar
  95. 95.
    Schatz PJ, Bieker KL, Ottemann KM, Silhavy TJ, Beckwith J (1991) One of three transmembrane stretches is sufficient for the functioning of the SecE protein, a membrane component of the E. coli secretion machinery. EMBO J 10(7):1749–1757CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Walter P, Blobel G (1982) Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature 299(5885):691–698CrossRefPubMedGoogle Scholar
  97. 97.
    Romisch K, Webb J, Herz J, Prehn S, Frank R, Vingron M, Dobberstein B (1989) Homology of 54K protein of signal-recognition particle, docking protein and two E. coli proteins with putative GTP-binding domains. Nature 340(6233):478–482. CrossRefPubMedGoogle Scholar
  98. 98.
    Hann BC, Poritz MA, Walter P (1989) 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 109(6 Pt 2):3223–3230CrossRefPubMedGoogle Scholar
  99. 99.
    Ribes V, Romisch K, Giner A, Dobberstein B, Tollervey D (1990) E. coli 4.5S RNA is part of a ribonucleoprotein particle that has properties related to signal recognition particle. Cell 63(3):591–600CrossRefPubMedGoogle Scholar
  100. 100.
    Poritz MA, Bernstein HD, Strub K, Zopf D, Wilhelm H, Walter P (1990) An E. coli ribonucleoprotein containing 4.5S RNA resembles mammalian signal recognition particle. Science 250(4984):1111–1117CrossRefPubMedGoogle Scholar
  101. 101.
    Phillips GJ, Silhavy TJ (1992) The E. coli ffh gene is necessary for viability and efficient protein export. Nature 359(6397):744–746. CrossRefPubMedGoogle Scholar
  102. 102.
    Brown S, Fournier MJ (1984) The 4.5 S RNA gene of Escherichia coli is essential for cell growth. J Mol Biol 178(3):533–550CrossRefPubMedGoogle Scholar
  103. 103.
    Brown S (1991) 4.5S RNA: does form predict function? New Biol 3(5):430–438PubMedGoogle Scholar
  104. 104.
    Tian H, Boyd D, Beckwith J (2000) A mutant hunt for defects in membrane protein assembly yields mutations affecting the bacterial signal recognition particle and Sec machinery. Proc Natl Acad Sci USA 97(9):4730–4735. CrossRefPubMedGoogle Scholar
  105. 105.
    Blobel G (2000) Protein targeting (Nobel lecture). ChemBioChem 1(2):86–102CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Molecular BiologyPrinceton UniversityPrincetonUSA

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