Phosphohistidyl Active Sites in Polyphosphate Kinase of Escherichia Coli

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1996 Dec 10

PMID 8962061

Citations 28

Authors

K D Kumble

K Ahn

A Kornberg

Affiliations

Soon will be listed here.

Abstract

In the synthesis of inorganic polyphosphate (polyP) from ATP by polyphosphate kinase (PPK; EC 2.7.4.1) of Escherichia coli, an N-P-linked phosphoenzyme was previously identified as the intermediate. The phosphate is presumed to be linked to N3 of the histidine residue because of its chemical stabilities and its resemblance to other enzymes known to contain N3-phosphohistidine. Tryptic digests of [32P]PPK contain a predominant 32P-labeled peptide that includes His-441. Of the 16 histidine residues in PPK of E. coli, 4 are conserved among several bacterial species. Mutagenesis of these 4 histidines shows that two (His-430 and His-598) are unaffected in function when mutated to glutamine, whereas two others (His-441 and His-460) mutated to glutamine or alanine fail to be phosphorylated, show no enzymatic activities, and fail to support polyP accumulation in cells bearing these mutant enzymes.

Citing Articles

Polyphosphate-kinase-1 dependent polyphosphate hyperaccumulation for acclimation to nutrient loss in the cyanobacterium, sp. PCC 6803.

Sato N, Endo M, Nishi H, Fujiwara S, Tsuzuki M Front Plant Sci. 2024; 15:1441626.

PMID: 39145186 PMC: 11322815. DOI: 10.3389/fpls.2024.1441626.

C-terminal Poly-histidine Tags Alter Escherichia coli Polyphosphate Kinase Activity and Susceptibility to Inhibition.

Bowlin M, Lieber A, Long A, Gray M J Mol Biol. 2024; 436(16):168651.

PMID: 38866092 PMC: 11297678. DOI: 10.1016/j.jmb.2024.168651.

Comparative genomics hints at dispensability of multiple essential genes in two Escherichia coli L-form strains.

Liu Y, Zhang Y, Kang C, Tian D, Lu H, Xu B Biosci Rep. 2023; 43(10).

PMID: 37819245 PMC: 10600066. DOI: 10.1042/BSR20231227.

Make or break: the thermodynamic equilibrium of polyphosphate kinase-catalysed reactions.

Keppler M, Moser S, Jessen H, Held C, Andexer J Beilstein J Org Chem. 2022; 18:1278-1288.

PMID: 36225726 PMC: 9520863. DOI: 10.3762/bjoc.18.134.

Ddp1 Cooperates with Ppx1 to Counter a Stress Response Initiated by Nonvacuolar Polyphosphate.

McCarthy L, Abramchuk I, Wafy G, Denoncourt A, Lavallee-Adam M, Downey M mBio. 2022; 13(4):e0039022.

PMID: 35862758 PMC: 9426566. DOI: 10.1128/mbio.00390-22.

References

Hess J, Bourret R, Simon M . Histidine phosphorylation and phosphoryl group transfer in bacterial chemotaxis. Nature. 1988; 336(6195):139-43. DOI: 10.1038/336139a0. View

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

Akiyama M, Crooke E, Kornberg A . The polyphosphate kinase gene of Escherichia coli. Isolation and sequence of the ppk gene and membrane location of the protein. J Biol Chem. 1992; 267(31):22556-61. View

Wei Y, Matthews H . Identification of phosphohistidine in proteins and purification of protein-histidine kinases. Methods Enzymol. 1991; 200:388-414. DOI: 10.1016/0076-6879(91)00156-q. View

Weigel N, Kukuruzinska M, Nakazawa A, Waygood E, Roseman S . Sugar transport by the bacterial phosphotransferase system. Phosphoryl transfer reactions catalyzed by enzyme I of Salmonella typhimurium. J Biol Chem. 1982; 257(23):14477-91. View

Wylie D, Stock A, Wong C, Stock J . Sensory transduction in bacterial chemotaxis involves phosphotransfer between Che proteins. Biochem Biophys Res Commun. 1988; 151(2):891-6. DOI: 10.1016/s0006-291x(88)80365-6. View

Anthony R, SPECTOR L . Phosphorylated acetate kinase. Its isolation and reactivity. J Biol Chem. 1972; 247(7):2120-5. View

Kato J, Yamamoto T, Yamada K, Ohtake H . Cloning, sequence and characterization of the polyphosphate kinase-encoding gene (ppk) of Klebsiella aerogenes. Gene. 1993; 137(2):237-42. DOI: 10.1016/0378-1119(93)90013-s. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

10.

Ahn K, Kornberg A . Polyphosphate kinase from Escherichia coli. Purification and demonstration of a phosphoenzyme intermediate. J Biol Chem. 1990; 265(20):11734-9. View

11.

Janknecht R, De Martynoff G, Lou J, Hipskind R, Nordheim A, Stunnenberg H . Rapid and efficient purification of native histidine-tagged protein expressed by recombinant vaccinia virus. Proc Natl Acad Sci U S A. 1991; 88(20):8972-6. PMC: 52633. DOI: 10.1073/pnas.88.20.8972. View

12.

Pilkis S, Walderhaug M, Murray K, Beth A, Venkataramu S, Pilkis J . 6-phosphofructo-2-kinase/fructose 2,6-bisphosphatase from rat liver. J Biol Chem. 1983; 258(10):6135-41. View

13.

Kulaev I . Biochemistry of inorganic polyphosphates. Rev Physiol Biochem Pharmacol. 1975; 73:131-58. DOI: 10.1007/BFb0034661. View

14.

Kornberg A, Kornberg S, Simms E . Metaphosphate synthesis by an enzyme from Escherichia coli. Biochim Biophys Acta. 1956; 20(1):215-27. DOI: 10.1016/0006-3002(56)90280-3. View

15.

Keasling J, BERTSCH L, Kornberg A . Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc Natl Acad Sci U S A. 1993; 90(15):7029-33. PMC: 47069. DOI: 10.1073/pnas.90.15.7029. View

16.

Messing J . New M13 vectors for cloning. Methods Enzymol. 1983; 101:20-78. DOI: 10.1016/0076-6879(83)01005-8. View

17.

Niederwieser A . [6] Thin-layer chromatography of amino acids and derivatives. Methods Enzymol. 2012; 25:60-99. DOI: 10.1016/S0076-6879(72)25008-X. View

18.

Kumble K, Kornberg A . Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem. 1995; 270(11):5818-22. DOI: 10.1074/jbc.270.11.5818. View

19.

Crooke E, Akiyama M, Rao N, Kornberg A . Genetically altered levels of inorganic polyphosphate in Escherichia coli. J Biol Chem. 1994; 269(9):6290-5. View

20.

Tinsley C, Gotschlich E . Cloning and characterization of the meningococcal polyphosphate kinase gene: production of polyphosphate synthesis mutants. Infect Immun. 1995; 63(5):1624-30. PMC: 173201. DOI: 10.1128/iai.63.5.1624-1630.1995. View