Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)

3′-phosphoadenosine 5′-phosphosulfate (PAPS) is synthesized by PAPS synthase (PAPSS) in two steps. In the first step ATP sulfurylase (ATPS) transfers sulfate group onto adenylyl moiety of ATP to form adenosine 5′-phosphosulfate (APS) and PPi. APS-kinase (APSK) then transfers the gamma-phosphoryl fro...

Full description

Saved in:
Bibliographic Details
Main Authors: K.V. Venkatachalam, Dhiraj Sinha, Chris Soha, Rudi H. Ettrich
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Biochemistry and Biophysics Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2405580824002565
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850072000112885760
author K.V. Venkatachalam
Dhiraj Sinha
Chris Soha
Rudi H. Ettrich
author_facet K.V. Venkatachalam
Dhiraj Sinha
Chris Soha
Rudi H. Ettrich
author_sort K.V. Venkatachalam
collection DOAJ
description 3′-phosphoadenosine 5′-phosphosulfate (PAPS) is synthesized by PAPS synthase (PAPSS) in two steps. In the first step ATP sulfurylase (ATPS) transfers sulfate group onto adenylyl moiety of ATP to form adenosine 5′-phosphosulfate (APS) and PPi. APS-kinase (APSK) then transfers the gamma-phosphoryl from ATP onto 3′-OH of APS to form PAPS and ADP. Mutations of histidine's (H425/H428) of hPAPSS isoform1 knocked out ATPS and not APSK. In silico ATP binding and molecular dynamics experiments exhibited an unfavorable binding energy for mutant enzymes. Thus, requirements of H425NGH428 motif for ATPS is established. The N426 residue in various organisms is substituted with R. We mutated hPAPSS1 with basic residue K. The N426 to K426 (N–K) mutant exhibited slightly lower Km (3.7 mM) and higher Vmax (3X) for ATP compared to wildtype (WT, Km 4.3 mM). The Km for sulfate for N–K mutant was nearly same as WT but the Vmax was ∼4X higher for N–K. The catalytic efficiency (Vmax/Km) of N–K was ∼3 fold higher than WT. The full length hPAPSS1 evinced bimodal response against ATP, a paradigm that was deduced to be a trait of PAPSS that requires 2 mol of ATP/PAPS formed. This bimodal kinetics with ATP was lost when the N-terminal APSK was deleted from the C-terminal ATPS domain. The C-terminal domain contained ATPS activity, exhibited Km of 2.2 mM for ATP and Km of 0.53 mM for Sulfate and much higher catalytic efficiency compared to full length hPAPSS1. Thus, fused ATPS-APSK must be structurally and kinetically different than individual domains influenced by inter-domain residues.
format Article
id doaj-art-2e73bd9e02524fac96427b567aec46dd
institution DOAJ
issn 2405-5808
language English
publishDate 2025-03-01
publisher Elsevier
record_format Article
series Biochemistry and Biophysics Reports
spelling doaj-art-2e73bd9e02524fac96427b567aec46dd2025-08-20T02:47:10ZengElsevierBiochemistry and Biophysics Reports2405-58082025-03-014110189210.1016/j.bbrep.2024.101892Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)K.V. Venkatachalam0Dhiraj Sinha1Chris Soha2Rudi H. Ettrich3College of Allopathic Medicine, USA; Health Professions Division, Nova Southeastern University, Ft. Lauderdale, FL, 33328, USA; Corresponding author. College of Allopathic Medicine, USA.Department of Radiation Oncology, UT Southwestern Medical Center, Dallas, TX, 75390, USAHealth Professions Division, Nova Southeastern University, Ft. Lauderdale, FL, 33328, USACollege of Biomedical Sciences, Larkin University, Miami, FL, 33169, USA; Department of Cellular Biology & Pharmacology, Herbert Wertheim College of Medicine, Florida International University, Miami, FL, 33174, USA3′-phosphoadenosine 5′-phosphosulfate (PAPS) is synthesized by PAPS synthase (PAPSS) in two steps. In the first step ATP sulfurylase (ATPS) transfers sulfate group onto adenylyl moiety of ATP to form adenosine 5′-phosphosulfate (APS) and PPi. APS-kinase (APSK) then transfers the gamma-phosphoryl from ATP onto 3′-OH of APS to form PAPS and ADP. Mutations of histidine's (H425/H428) of hPAPSS isoform1 knocked out ATPS and not APSK. In silico ATP binding and molecular dynamics experiments exhibited an unfavorable binding energy for mutant enzymes. Thus, requirements of H425NGH428 motif for ATPS is established. The N426 residue in various organisms is substituted with R. We mutated hPAPSS1 with basic residue K. The N426 to K426 (N–K) mutant exhibited slightly lower Km (3.7 mM) and higher Vmax (3X) for ATP compared to wildtype (WT, Km 4.3 mM). The Km for sulfate for N–K mutant was nearly same as WT but the Vmax was ∼4X higher for N–K. The catalytic efficiency (Vmax/Km) of N–K was ∼3 fold higher than WT. The full length hPAPSS1 evinced bimodal response against ATP, a paradigm that was deduced to be a trait of PAPSS that requires 2 mol of ATP/PAPS formed. This bimodal kinetics with ATP was lost when the N-terminal APSK was deleted from the C-terminal ATPS domain. The C-terminal domain contained ATPS activity, exhibited Km of 2.2 mM for ATP and Km of 0.53 mM for Sulfate and much higher catalytic efficiency compared to full length hPAPSS1. Thus, fused ATPS-APSK must be structurally and kinetically different than individual domains influenced by inter-domain residues.http://www.sciencedirect.com/science/article/pii/S2405580824002565
spellingShingle K.V. Venkatachalam
Dhiraj Sinha
Chris Soha
Rudi H. Ettrich
Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
Biochemistry and Biophysics Reports
title Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
title_full Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
title_fullStr Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
title_full_unstemmed Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
title_short Structure/function of ATP sulfurylase domain of human 3′-phosphoadenosine 5′-phosphosulfate synthase (hPAPSS)
title_sort structure function of atp sulfurylase domain of human 3 phosphoadenosine 5 phosphosulfate synthase hpapss
url http://www.sciencedirect.com/science/article/pii/S2405580824002565
work_keys_str_mv AT kvvenkatachalam structurefunctionofatpsulfurylasedomainofhuman3phosphoadenosine5phosphosulfatesynthasehpapss
AT dhirajsinha structurefunctionofatpsulfurylasedomainofhuman3phosphoadenosine5phosphosulfatesynthasehpapss
AT chrissoha structurefunctionofatpsulfurylasedomainofhuman3phosphoadenosine5phosphosulfatesynthasehpapss
AT rudihettrich structurefunctionofatpsulfurylasedomainofhuman3phosphoadenosine5phosphosulfatesynthasehpapss