Characterization of the Adenosine Triphosphatase Activity of the Periplasmic Histidine Permease, a Traffic ATPase (ABC Transporter)

Abstract

The superfamily of traffic ATPases (ABC transporters) includes bacterial periplasmic transport systems (permeases) and eukaryotic transporters. The histidine permease ofSalmonella typhimurium is composed of a membrane-bound complex (HisQMP2) containing four subunits, and of a soluble receptor, the histidine-binding protein (HisJ). Transport is energized by ATP. In this article the ATPase activity of HisQMP2 has been characterized, using a novel assay that is independent of transport. The assay uses Mg2+ ions to permeabilize membrane vesicles or proteoliposomes, thus allowing access of ATP to both sides of the bilayer. HisQMP2 displays a low level of intrinsic ATPase activity in the absence of HisJ; unliganded HisJ stimulates the activity and liganded HisJ stimulates to an even higher level. All three levels of activity display positive cooperativity for ATP with a Hill coefficient of 2 and aK0.5 value of 0.6 mm. The activity has been characterized with respect to pH, salt, phospholipids, substrate, and inhibitor specificity. Free histidine has no effect. The activity is inhibited by orthovanadate, but not byN-ethylmaleimide, bafilomycin A1, or ouabain. Several nucleotide analogs, ADP, 5′-adenylyl-β,γ-imidodiphosphate, adenosine 5′-(β,γimino)triphosphate, and adenosine 5′-O-(3-thio)triphosphate, inhibit the activity. Unliganded HisJ does not compete with liganded HisJ for the stimulation of the ATPase activity of HisQMP2. The superfamily of traffic ATPases (ABC transporters) includes bacterial periplasmic transport systems (permeases) and eukaryotic transporters. The histidine permease ofSalmonella typhimurium is composed of a membrane-bound complex (HisQMP2) containing four subunits, and of a soluble receptor, the histidine-binding protein (HisJ). Transport is energized by ATP. In this article the ATPase activity of HisQMP2 has been characterized, using a novel assay that is independent of transport. The assay uses Mg2+ ions to permeabilize membrane vesicles or proteoliposomes, thus allowing access of ATP to both sides of the bilayer. HisQMP2 displays a low level of intrinsic ATPase activity in the absence of HisJ; unliganded HisJ stimulates the activity and liganded HisJ stimulates to an even higher level. All three levels of activity display positive cooperativity for ATP with a Hill coefficient of 2 and aK0.5 value of 0.6 mm. The activity has been characterized with respect to pH, salt, phospholipids, substrate, and inhibitor specificity. Free histidine has no effect. The activity is inhibited by orthovanadate, but not byN-ethylmaleimide, bafilomycin A1, or ouabain. Several nucleotide analogs, ADP, 5′-adenylyl-β,γ-imidodiphosphate, adenosine 5′-(β,γimino)triphosphate, and adenosine 5′-O-(3-thio)triphosphate, inhibit the activity. Unliganded HisJ does not compete with liganded HisJ for the stimulation of the ATPase activity of HisQMP2. The superfamily of traffic ATPases (or ABC transporters) comprises both prokaryotic and eukaryotic transport proteins which share a conserved nucleotide-binding domain (1Ames G.F.-L. Mimura C. Shyamala V. FEMS Microbiol. Rev. 1990; 75: 429-446Crossref Google Scholar, 2Hyde S.C. Emsley P. Hartshorn M.J. Mimmack M.M. Gileadi U. Pearce S.R. Gallagher M.P. Gill D.R. Hubbard R.E. Higgins C.F. Nature. 1990; 346: 362-365Crossref PubMed Scopus (949) Google Scholar). The superfamily includes bacterial periplasmic permeases, the yeast STE6 gene product, the mammalian P-glycoprotein (multidrug resistance protein or MDR), 1The abbreviations used are: MDR, multidrug resistance protein; HisQMP2, HisQ·HisM·HisP, membrane-bound complex of the histidine permease; PLS, proteoliposomes reconstituted from solubilized membrane vesicles, unless specified differently; CF, 5- (and 6)-carboxyfluorescein; PAGE, polyacrylamide gel electrophoresis; PE, phosphatidylethanolamine; AMP-PNP, 5′-adenylyl-β,γ-imidodiphosphate; AMP-PCP, adenosine 5′-(β,γ-imino)triphosphate; ATPγS, adenosine 5′-O-(3-thio)triphosphate; MOPS, 4-morpholinepropanesulfonic acid; BisTris, 2-[bis(2-hydroxyethyl)amino]-2-(hydroxymethyl)-propane-1,3-diol; TNP-ATP, 2′-(3′)-D-(trinitrophenyl)adenosine 5′-triphosphate.1The abbreviations used are: MDR, multidrug resistance protein; HisQMP2, HisQ·HisM·HisP, membrane-bound complex of the histidine permease; PLS, proteoliposomes reconstituted from solubilized membrane vesicles, unless specified differently; CF, 5- (and 6)-carboxyfluorescein; PAGE, polyacrylamide gel electrophoresis; PE, phosphatidylethanolamine; AMP-PNP, 5′-adenylyl-β,γ-imidodiphosphate; AMP-PCP, adenosine 5′-(β,γ-imino)triphosphate; ATPγS, adenosine 5′-O-(3-thio)triphosphate; MOPS, 4-morpholinepropanesulfonic acid; BisTris, 2-[bis(2-hydroxyethyl)amino]-2-(hydroxymethyl)-propane-1,3-diol; TNP-ATP, 2′-(3′)-D-(trinitrophenyl)adenosine 5′-triphosphate. the human cystic fibrosis transmembrane conductance regulator (CFTR), and the mammalian heterodimeric transporter (TAP1/TAP2) involved in antigen processing (3Higgins C.F. Annu. Rev. Cell Biol. 1992; 8: 67-113Crossref PubMed Scopus (3323) Google Scholar, 4Doige C.A. Ames G.F.-L. Annu. Rev. Microbiol. 1993; 47: 291-319Crossref PubMed Scopus (264) Google Scholar). The periplasmic histidine permease in Salmonella typhimurium and the maltose permease in Escherichia coli have been extensively characterized; both are good model systems for this superfamily (5Shyamala V. Baichwal V. Beall E. Ames G.F.-L. J. Biol. Chem. 1991; 266: 18714-18719Abstract Full Text PDF PubMed Google Scholar, 6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, 7Nikaido H. FEBS Lett. 1994; 346: 55-58Crossref PubMed Scopus (64) Google Scholar). The histidine permease is composed of a soluble substrate-binding receptor, HisJ (the periplasmic histidine-binding protein), and a membrane-bound complex, HisQMP2 (8Kerppola R.E. Shyamala V.K. Klebba P. Ames G.F.-L. J. Biol. Chem. 1991; 266: 9857-9865Abstract Full Text PDF PubMed Google Scholar), which contains two integral membrane proteins, HisQ and HisM, and two copies of HisP which carries the ATP-binding motif (9Mimura C.S. Admon A. Hurt K.A. Ames G.F.-L. J. Biol. Chem. 1990; 265: 19535-19542Abstract Full Text PDF PubMed Google Scholar, 10Mimura C.S. Holbrook S.R. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1991; 88: 84-88Crossref PubMed Scopus (139) Google Scholar). ATP hydrolysis provides the energy for the transport process (11Ames G.F.-L. Krulwich T.A. Bacterial Energetics. Academic Press, Inc., New York1990: 225-245Crossref Google Scholar). The histidine permease has been reconstituted into PLS that transport histidine when ATP is trapped internally and HisJ is added externally (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, 12Bishop L. Agbayani R.J. Ambudkar S.V. Maloney P.C. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1989; 86: 6953-6957Crossref PubMed Scopus (125) Google Scholar). As usually assumed in current working models, the liganded receptor sends a signal that initiates ATP hydrolysis and results in subsequent ligand translocation (13Ames G.F.-L. Liu C.E. Joshi A.K. Nikaido K. J. Biol. Chem. 1996; 271: 14264-14270Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar, 14Davidson A.L. Shuman H.A. Nikaido H. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 2360-2364Crossref PubMed Scopus (231) Google Scholar). The characterization of the ATPase activity, which is likely to be common to all members of this superfamily of transporters because of the extensive sequence conservation, is crucial for understanding their mechanism of action. ATP hydrolysis has generally been ascribed to the nucleotide-binding domain. Therefore, several laboratories took the approach of purifying this domain (or component) for the purpose of studying its activity in vitro. MalK, following its solubilization with urea and purification from inclusion bodies, has ATP binding and hydrolyzing activity (15Walter C. Honer K. E. J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar). nucleotide-binding have been by a of and to ATP V. C. E. Microbiol. 1993; 8: PubMed Scopus Google Scholar, A. J. Biol. Chem. 1993; Full Text PDF PubMed Google Scholar). the activity of the in not to stimulation by the soluble the with and and the of the ATPase activity the integral membrane is to the of the membrane-bound In this a of the ATPase activity of the histidine permease reconstituted in PLS, using a novel assay in which the has been to both ATP and the is that HisQMP2 has an intrinsic low level ATPase activity in the absence of The activity is by unliganded HisJ and to a level by liganded the intrinsic and display positive cooperativity for ATP. The of the activity have been The following E. coli which carries the and contains the S. typhimurium the of the A. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus (70) Google which is from by of coli a of in 2 with a to a and in in and in with in the and no from E. and from and in the phospholipids, that the E. a in of a of in 2 a of and to The of by J. Biol. Chem. Full Text PDF PubMed Google Scholar, J. Biol. Chem. Full Text PDF PubMed Google Scholar). vesicles and PLS (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar), from unless specified ATPase in a of membrane vesicles containing or PLS containing and protein and or of PLS reconstituted from HisQMP2, containing and protein and and E. coli added when the assay with membrane vesicles or PLS reconstituted with HisQMP2. HisJ and histidine added the The for in a and the assay by the of ATP with and unless specified the with of The of ATP hydrolysis by the S. PubMed Scopus Google Scholar), using a to of with a using and of and and for both and with the of the gel to A. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus (70) Google Scholar, Nature. PubMed Scopus Google Scholar). by a PubMed Scopus Google using a and the HisJ E. A. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google and the unliganded and liganded by K. Ames G.F.-L. J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar). from the following from and and bafilomycin A1, and AMP-PNP, AMP-PCP, and ATPγS, The soluble receptor HisJ the ATPase activity of HisQMP2 in by a signal the membrane because HisJ is in the and the ATP-binding domain of HisP is in the has been that HisJ and ATP are sides of the PLS, with ATP trapped internally and HisJ added externally L. Agbayani R.J. Ambudkar S.V. Maloney P.C. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1989; 86: 6953-6957Crossref PubMed Scopus (125) Google Scholar), or (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar), the ATPase activity is by liganded The that HisJ the activity when of the PLS is to the that the of HisQMP2 is in PLS in in the and (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). HisP has been to be from the periplasmic of the membrane V. Liu Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1993; PubMed Scopus Google Scholar), is that ATP the domain of this PLS containing HisQMP2 (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google and their ATPase activity when both liganded HisJ and ATP to the of HisJ does not the activity that ATP does not have access to hydrolyzing the ATPase activity, HisJ and ATP be sides of PLS, with trapped in both are ATP is trapped internally and HisJ is added an of is because the ATP is a of ATP be trapped into PLS ATP value PLS an PLS of (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google and an of that not all of the trapped are because PLS be the the (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). HisJ the PLS and ATP externally (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, 14Davidson A.L. Shuman H.A. Nikaido H. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 2360-2364Crossref PubMed Scopus (231) Google several the for the receptor is a of receptor protein is and a of the be in the because or two of receptor be trapped PLS and receptor an of and receptor be trapped and in be to the of the the receptor and the Therefore, a that ATP and HisJ to both sides of PLS is membrane solubilization be a but all inhibited the ATPase activity. Mg2+ an to hydrolysis by PLS of externally added ATP in the of thus that permeabilize using an of PLS be trapped PLS which of its PLS are the be when the a of its into the 1993; PubMed Scopus Google Scholar). that of from PLS, which that PLS have been The is to Mg2+ ions to by the that not have effect. of is not used for PLS because with the ATPase The of protein is not for because results are with not ATP and histidine are by to that this is not to be from PLS by to of the by the of HisJ from PLS and with of using Mg2+ ions are with of or ATP to PLS, no is that are for the to be for the ATPase its be the of is this is an because is to of the of that the is and the is All in this In the of the Mg2+ not this to be for the ATPase activity in PLS in membrane that the of a assay of ATP hydrolysis by The of hydrolysis in the of liganded HisJ is to that the of hydrolysis is to the of PLS added the to protein and to PLS protein and that a of is with PLS reconstituted with HisQMP2 to the of protein a that the of hydrolysis is to protein in this in which the of to protein from to the assay the activity the protein and is not by the The of the Mg2+ the of hydrolysis is in A. Mg2+ is in ATP and in the absence of the hydrolysis is higher when are and In the of liganded the is 2 In both the in activity is to the of ATP to by the The in the of liganded HisJ is to the that both and HisJ to ATP and HisJ the of liganded HisJ is the The in activity in the of is not to from PLS because the activity is the of ATP not that ATP is PLS, PLS are the of the the activity in because of ATP and of is the in PLS (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google be PLS be which ATP for this of Mg2+ by have no effect. ATP hydrolysis of The that be levels of ATPase activity are in and protein in the absence of and in the of HisJ and liganded The low level ATP hydrolysis in the absence of HisJ be to ATPases or to an intrinsic activity of HisQMP2, or a of PLS containing of HisQMP2 in the of of the proteins of for of and the of PLS of the by and using HisP and the of HisQMP2 in PLS the The ATPase activity in PLS in the absence of HisJ in the of ATPases to this activity, PLS from contains no the for and to have a activity all the activity in PLS in the absence of HisJ is to the of an activity intrinsic to HisQMP2 and that of the complex has an intrinsic activity by purifying and into PLS, ATP in the absence of HisJ S. C. E. P. and S. in ATPase activity of HisQMP2. PLS from membrane vesicles from or for of of proteins in PLS from and with of and The gel with but using HisP and ATPase activity of PLS from and in the absence or of liganded The the of the to membrane PLS from for ATP hydrolysis in the or absence of liganded the activity by liganded HisJ is to HisQMP2 to a activity which is by is by its the HisQMP2 in PLS HisQMP2 the an activity of protein activity of protein in the of a of liganded HisJ The stimulation is for HisJ because a of HisJ proteins that are to the ATPase activity. E. A. and with soluble receptor, (the periplasmic C.F. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), be to the ATPase activity. both unliganded and the activity. The of for the level of activity to be and are to for HisJ (13Ames G.F.-L. Liu C.E. Joshi A.K. Nikaido K. J. Biol. Chem. 1996; 271: 14264-14270Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar). HisQMP2 in PLS used to the of HisQMP2 for both for the intrinsic activity and the activity by liganded In both the are with respect to ATP a positive cooperativity ATP-binding in HisQMP2, with Hill two binding in HisQMP2 are for ATP are and 0.6 for the activity by liganded HisJ and for the intrinsic activity. are and for the activity by liganded HisJ and for the intrinsic activity. the that the cooperativity is to the of PLS containing internally trapped liganded HisJ in the of the activity positive cooperativity with a Hill coefficient and of and ATP have been to histidine transport and to to HisP A. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. PubMed Scopus (70) Google Scholar, G.F.-L. Nikaido K. J. J. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar), that HisQMP2 has a for the hydrolysis of and for their in transport. The of hydrolysis of and 2 are in the following ATP of is the that when for the of transport L. Agbayani R.J. Ambudkar S.V. Maloney P.C. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1989; 86: 6953-6957Crossref PubMed Scopus (125) Google Scholar, G.F.-L. Nikaido K. J. J. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar). The ATP ADP, AMP-PNP, AMP-PCP, and ATPγS, inhibit the activity a inhibitor of ATPases J. J. Biol. Chem. Full Text Full Text PDF PubMed Scopus Google and histidine transport E. A. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar), the activity of HisQMP2, to and not of PLS for the assay with has no and of the ATPase activity in PLS in the of liganded HisJ a of nucleotide The value is the of nucleotide which results in the activity in the of 2 The the activity in the of 2 of or is the which in the of 2 ATP. The is the which does not inhibit activity. in and the in the assay not The activity in PLS in the of liganded HisJ a of nucleotide The value is the of nucleotide which results in the activity in the of 2 The the activity in the of 2 is the which in the of 2 ATP. The is the which does not inhibit activity. in and the in the assay not in a has been that the membrane-bound complex of periplasmic carries a substrate-binding (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, C.F. Nikaido K. Ames G.F.-L. Nature. PubMed Scopus Google Scholar, V. Ames G.F.-L. J. Biol. Chem. 1991; 266: Full Text PDF PubMed Google Scholar, Shuman H.A. J. Biol. 1993; PubMed Scopus Google Scholar, Shuman H.A. J. PubMed Google Scholar). The of a in HisQMP2 has been by the of V. Ames G.F.-L. J. Biol. Chem. 1991; 266: Full Text PDF PubMed Google Scholar, Ames G.F.-L. J. 1991; PubMed Google Scholar), the of in transport by histidine trapped PLS (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar), and the of several in HisQ or C.F. Nikaido K. Ames G.F.-L. Nature. PubMed Scopus Google Scholar). The of this be to the histidine from liganded HisJ and a of for or to histidine to HisQMP2 for with The of histidine the of hydrolysis a of histidine in the of a of unliganded HisJ The hydrolysis in with histidine to which the activity histidine has no the ATPase activity results that the substrate-binding HisQMP2 is not involved in HisQMP2 for transport in the of Free to has no the intrinsic activity that histidine in the is to transport in the absence of In the ATPase activity of HisQMP2 by liganded HisJ or the intrinsic is not by is not for activity and higher activity, with The is to that for histidine transport (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). and the activity, with higher The for the activity is and an the for the and for ATP because the for the ATPase of several HisQMP2 is and the for histidine transport is (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar, E. A. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar, A. S. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar). The of the activity of HisQMP2 vesicles used in this low levels of phospholipids, thus by vesicles are by that the activity with the of E. coli phospholipids, a 2 with a to protein of for PE, are with the by is the of of and when in with of the results in an activity higher that in the of E. coli activity in the of activity E. added to the ATPase the The ATPase activity in membrane vesicles and is of the activity in the absence of In the absence of phospholipids, the contains coli which are in the membrane in a added to the ATPase the The ATPase activity in membrane vesicles and is of the activity in the absence of In the absence of phospholipids, the contains coli which are in the membrane that unliganded HisJ with HisQMP2 with an to that of liganded by stimulation of ATPase activity (13Ames G.F.-L. Liu C.E. Joshi A.K. Nikaido K. J. Biol. Chem. 1996; 271: 14264-14270Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar), and of histidine transport E. A. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar). Therefore, that unliganded HisJ compete with liganded HisJ in the stimulation of ATPase activity. that of unliganded HisJ inhibit the of ATP hydrolysis by liganded because the stimulates a level of activity. that the with of unliganded when or histidine are In the absence of histidine the is for the stimulation by unliganded HisJ (13Ames G.F.-L. Liu C.E. Joshi A.K. Nikaido K. J. Biol. Chem. 1996; 271: 14264-14270Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar). In the of histidine a is the HisJ that of which the that are the of the by the liganded and unliganded HisJ the of HisQMP2 is that is no unliganded and liganded HisJ in the stimulation of ATP when the of unliganded HisJ to In this that Mg2+ ions the of of a of to the and of membrane vesicles and and the of into the S. J. 1990; PubMed Scopus Google Scholar). has been ascribed to the of the in the K. 1990; PubMed Scopus Google Scholar). is generally Mg2+ in Mg2+ is in containing S. J. 1990; PubMed Scopus Google Scholar). the results using PLS from E. coli which a of G.F.-L. J. PubMed Google Scholar). that PLS of has been in K. 1990; PubMed Scopus Google Scholar). a PubMed Scopus Google Scholar, A. PubMed Scopus Google Scholar), ATP from PLS not that the has for the is that is to in a which the of Proc. Natl. Acad. Sci. U. S. A. 1996; PubMed Scopus Google Scholar). The of the in the of the membrane-bound ATPases of periplasmic In to the of all ATP-binding and to both ATP and the is likely to the of the is that of the of The of the to the HisJ to a low of trapped to the of the The has is and be used for both membrane vesicles and PLS, thus allowing the activity to be an purification HisQMP2 displays three levels of ATPase activity, the and of the receptor, The activity of HisQMP2 is higher the intrinsic activity. The that the intrinsic activity an by the solubilization and is because HisQMP2 in membrane vesicles displays intrinsic activity. The of HisJ HisQ by of two by a of HisP or by its activity. The of is likely because HisP in the absence of HisQ and has an activity higher the intrinsic activity of HisQMP2, and for that HisQ be the The ATPase activity for PLS is higher of protein L. Agbayani R.J. Ambudkar S.V. Maloney P.C. Ames G.F.-L. Proc. Natl. Acad. Sci. U. S. A. 1989; 86: 6953-6957Crossref PubMed Scopus (125) Google Scholar). The higher hydrolysis is to of with assay systems in which ATP is trapped in with of the higher value the hydrolyzing of HisQMP2 is to the for that have V. Ames G.F.-L. J. Biol. Chem. 1991; 266: Full Text PDF PubMed Google Scholar, of Transport by the of Salmonella typhimurium of Scholar). levels of activity have been for the maltose transport complex from solubilized membrane vesicles in of protein A.L. Shuman H.A. Nikaido H. Proc. Natl. Acad. Sci. U. S. A. 1992; 89: 2360-2364Crossref PubMed Scopus (231) Google Scholar). HisQMP2 ATP with a of of protein which is to to a of in the of liganded PLS transport histidine a of of which be to of the are in the in the transport is an is in the PLS (6Liu C.E. Ames G.F.-L. J. Biol. Chem. 1997; 272: 859-866Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar). Therefore, a of ATP to histidine be to be a transport of has been in the absence of an PLS have the to a transport of in the of an The a of ATP to histidine of which be a of the the and intrinsic display positive cooperativity for an the two HisP the be independent of HisJ The two both or with the binding ATP and the activity. The that the two of HisP with the complex is with that the of soluble HisP is a the two of HisP in HisQMP2 have and no has been is that has the to ATP and binding hydrolysis by the value for HisQMP2 of 0.6 for both the intrinsic and is with the value from in histidine transport A. S. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google and with that for the maltose permease A.L. J. Biol. Chem. 1996; 271: Full Text Full Text PDF PubMed Scopus Google and J. Biol. Chem. 1993; Full Text PDF PubMed Google Scholar, J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar). The that added the activity in membrane vesicles a by the The of activity by several a in to a of in the a in activity which a of is the coli G.F.-L. J. PubMed Google Scholar), its a in and does not in The by an a common with that of traffic ATPases J. Biol. Chem. 1992; Full Text PDF PubMed Google Scholar), V. C. E. Microbiol. 1993; 8: PubMed Scopus Google Scholar), and the maltose permease A.L. J. Biol. Chem. 1996; 271: Full Text Full Text PDF PubMed Scopus Google The of by unliganded HisJ for liganded ATP hydrolysis is be even the unliganded liganded HisJ HisQMP2, has a of a histidine with the complex of ATP be the complex is with the of of histidine the HisJ and the process is The ATPase activity of HisQMP2 with members of the superfamily several be of the intrinsic activity has been for J. PubMed Scopus Google Scholar). with respect to ATP has been for the maltose permease A.L. J. Biol. Chem. 1996; 271: Full Text Full Text PDF PubMed Scopus Google and for the in in The activity is to ATPase in the of HisQMP2 and E. A. Ames G.F.-L. J. Biol. Chem. 1989; Full Text PDF PubMed Google Scholar), the maltose permease A.L. J. Biol. Chem. 1996; 271: Full Text Full Text PDF PubMed Scopus Google Scholar), and J. Biol. Chem. 1993; Full Text PDF PubMed Google Scholar, J. Biol. Chem. 1992; Full Text PDF PubMed Google HisQMP2 and are to is which be soluble of HisP of HisQ and is to for of the and and Nikaido for