Positively charged lysine at the N‐terminus of the signal peptide of the <i>Escherichia coli</i> alkaline phosphatase provides the secretion efficiency and is involved in the interaction with anionic phospholipids

Nesmeyanova, M. A.; Karamyshev, A. L.; Karamysheva, Zemphyra N; Kalinin, Andrey E.; Ksenzenko, V. N.; Kajava, Andrey V.

doi:10.1016/s0014-5793(97)00052-5

Cited by 63 publications

(32 citation statements)

References 24 publications

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“…Most transported proteins contain an amino-terminal region, termed the signal peptide (SP), which directs and facilitates membrane transport of the nascent protein and, then, in most cases is cleaved off, releasing the mature protein. The basic structural characteristics of SPs are highly conserved with three regions important for function: a positively charged amino terminus, a hydrophobic core, and a hydrophilic carboxyl terminus (1)(2)(3). Although natural variation in SPs has been described for proteins from a variety of species, an adaptive benefit of the mutations is unlikely or is poorly understood (4)(5)(6)(7)(8)(9).…”

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confidence: 99%

Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli

Ronald¹,

Yakovenko

Yazvenko³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Signal peptides (SPs) are critical for protein transport across cellular membranes, have a highly conserved structure, and are cleaved from the mature protein upon translocation. Here, we report that naturally occurring mutations in the SP of the adhesive, tipassociated subunit of type 1 fimbriae (FimH) are positively selected in uropathogenic Escherichia coli. On the one hand, these mutations have a detrimental effect, with reduced FimH transport across the inner membrane, fewer FimH and fimbriae expressed on the bacterial surface, and decreased bacterial adhesion under flow conditions. On the other hand, the fimbriae expressed by the mutants are significantly longer on average, with many fimbriae able to stretch to >20 m in length. More surprisingly, the SP mutant bacteria display an increased ability to resist detachment from the surface upon a switch from high to low flow. This functional effect of longer fimbriae highlights the importance of the nonadhesive fimbrial rod for adhesive function. Also, whereas bacterial adhesion to bladder epithelial cells was preserved in most mutants, binding to and killing by human neutrophils was decreased, providing an additional reason the SP mutations are relatively common among uropathogenic strains. Thus, this study demonstrates how mutations in an SP, while decreasing transport function and not affecting the final structure of the translocated protein, can lead to functional gains of the extracellular organelles that incorporate the protein and overall adaptive changes in the organism's fitness.bacterial pathogenesis ͉ fimbrial morphology ͉ protein transport ͉ shear force

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confidence: 99%

Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli

Ronald¹,

Yakovenko

Yazvenko³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…To systematically study the effect on translocation of positively charged residues placed at different distances from a signal sequence, we analyzed mutants derived from the E. coli alkaline phosphatase (PhoA). The secretion of this protein is well studied and is typical for Sec-dependent proteins of gram-negative bacteria (18,25,35,37). The mature alkaline phosphatase has 0 net charge in the region of the first 14 or 15 residues and Ϫ1 net charge in the 16-to 18-residue regions.…”

Section: Statistical Analysis Of Net Charge Distributionmentioning

confidence: 99%

“…The signal sequence contains information for interaction with protein components of the secretory machinery (for reviews, see references 15 and 42), membrane phospholipids (12,20,37), and signal peptidase (9,25). A signal peptide is not, however, sufficient to mediate the export of any attached polypeptide.…”

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confidence: 99%

“…It was also suggested that net positive or neutral charge difference between the N-and C-terminal regions of the signal peptide may be required for protein secretion (51). Further mutational analysis has shown that this N-C charge imbalance may not be obligatory for translocation of proteins across the cytoplasmic membrane of bacteria (5,37,43). Several experimental works suggested that the charge-sensitive mature sequence critical for protein export in bacteria may be extended to 15 (47), 20 (27), and even 30 residues (1).…”

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confidence: 99%

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The Net Charge of the First 18 Residues of the Mature Sequence Affects Protein Translocation across the Cytoplasmic Membrane of Gram-Negative Bacteria

et al. 2000

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This statistical study shows that in proteins of gram-negative bacteria exported by the Sec-dependent pathway, the first 14 to 18 residues of the mature sequences have the highest deviation between the observed and expected net charge distributions. Moreover, almost all sequences have either neutral or negative net charge in this region. This rule is restricted to gram-negative bacteria, since neither eukaryotic nor grampositive bacterial exported proteins have this charge bias. Subsequent experiments performed with a series of Escherichia coli alkaline phosphatase mutants confirmed that this charge bias is associated with protein translocation across the cytoplasmic membrane. Two consecutive basic residues inhibit translocation effectively when placed within the first 14 residues of the mature protein but not when placed in positions 19 and 20. The sensitivity to arginine partially reappeared again 30 residues away from the signal sequence. These data provide new insight into the mechanism of protein export in gram-negative bacteria and lead to practical recommendations for successful secretion of hybrid proteins.

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“…As components of the cytoplasmic membrane, they not only form the barrier of permeability for many substances but also, being a microenvironment for many proteins and possessing metabolic and structural dynamicity, phospholipids are involved in many transmembrane processes [9][10][11][12][13]. In particular, anionic phospholipids (APL) provide optimal conditions for the functioning of protein components of secretory machinery and participate in secretion initiation through interaction with the signal peptide [14][15][16]. Zwitter-ionic phospholipid, phosphatidylethanolamine (PE), is engaged in translocation through formation of non-bilayer structures [17,18].…”

Section: Introductionmentioning

confidence: 99%

The change in membrane phospholipid composition influences protein secretion and cell envelope biogenesis in Escherichia coli

et al. 2007

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Secretion of periplasmic alkaline phosphatase (PhoA) encoded by the gene constituent of plasmids and the peculiar properties of cell envelope biogenesis in Escherichia coli strains with controlled synthesis of individual membrane phospholipids have been studied. Alkaline phosphatase secretion across the cytoplasmic membrane declines, while secretion into the culture medium intensifies under changed metabolism. The composition of anionic membrane phospholipids changes due to inactivation of the pgsA gene or regulation of its expression by environmental factor, as well as in the absence of the pssA gene which is responsible for the synthesis of the precursor for zwitter-ionic phospholipidphosphatidylethanolamine. This correlates with intensified secretion of exopolysaccharides and lower content of lipopolysaccharide and lipoprotein which are responsible for barrier properties of the outer membrane. The results suggest a possible coupling of protein secretion with biogenesis of cell envelope components at a level of phospholipid metabolism.

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Positively charged lysine at the N‐terminus of the signal peptide of the Escherichia coli alkaline phosphatase provides the secretion efficiency and is involved in the interaction with anionic phospholipids

Cited by 63 publications

References 24 publications

Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli

Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli

The Net Charge of the First 18 Residues of the Mature Sequence Affects Protein Translocation across the Cytoplasmic Membrane of Gram-Negative Bacteria

The change in membrane phospholipid composition influences protein secretion and cell envelope biogenesis in Escherichia coli

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