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PMID: 8367477 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme.

Pancholi V, Fischetti VA

Abstract

We recently identified an enzymatically active glyceraldehyde-3-phosphate dehydrogenase (EC 1.2.1.12; GAPDH) as a major protein on the surface of group A streptococci (SDH), which exhibits multiple binding activity to various mammalian proteins. We now report that the SDH molecule also functions as an ADP-ribosylating enzyme, which, in the presence of NAD, is auto-ADP-ribosylated. In a crude cell wall extract of group A streptococci, SDH is the only protein that is ADP-ribosylated. SDH found in the streptococcal cytoplasmic fraction could not be ADP-ribosylated in the presence of NAD. Treatment of ADP-ribosylated SDH with the cytoplasmic fraction removed the ADP-ribose from SDH, suggesting the presence of an ADP-ribosyl hydrolase in the cytoplasmic compartment. The covalent linkage of ADP-ribose to SDH was stable to neutral hydroxylamine, sensitive to HgCl2, and inhibitable by free cysteine, indicating that the modification was at a cysteine residue of SDH. In addition to its auto-ADP-ribosylation activity, purified SDH or streptococcal cell wall extracts were able to transfer the ADP-ribose moiety of NAD specifically to free cysteine, resulting in a true thioglycosidic linkage. Treatment of purified SDH or the crude cell wall extract with sodium nitroprusside, which spontaneously generates nitric oxide, was found to stimulate the ADP-ribosylation of SDH in a time-dependent manner. ADP-ribosylation and nitric oxide treatment inhibited the GAPDH activity of SDH. Since ADP-ribosylation and nitric oxide are involved in signal transduction events, the ADP-ribosylating activity of SDH may enable communication between host and parasite during infection by group A streptococci.

MeSH Terms
Adenosine Diphosphate Ribose/metabolism Antibodies Blotting, Western Cytosol/enzymology Electrophoresis, Polyacrylamide Gel Glyceraldehyde-3-Phosphate Dehydrogenases/isolation & purification,metabolism Membrane Proteins/isolation & purification,metabolism NAD/metabolism Peptide Fragments/isolation & purification Streptococcus pyogenes/enzymology Subcellular Fractions/enzymology Substrate Specificity
Chemicals
Antibodies Membrane Proteins Peptide Fragments NAD Adenosine Diphosphate Ribose Glyceraldehyde-3-Phosphate Dehydrogenases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Pancholi V
Laboratory of Bacterial Pathogenesis and Immunology, Rockefeller University, New York, NY 10021.
Fischetti V A
References (29)
29 references, click to expand
  1. Nonidentical alkylation sites in rabbit muscle glyceraldehyde-3-phosphate dehydrogenase.
    Biochemistry. 1975 Mar 25;14(6):1146-52 PMID: 1168066
  2. Modification of plasma membrane protein cysteine residues by ADP-ribose in vivo.
    J Biol Chem. 1990 Jul 5;265(19):10825-8 PMID: 2113525
  3. Nitroprusside stimulates the cysteine-specific mono(ADP-ribosylation) of glyceraldehyde-3-phosphate dehydrogenase from human erythrocytes.
    FEBS Lett. 1992 Mar 23;300(1):9-12 PMID: 1547895
  4. Molecular and immunological characterization of ADP-ribosylarginine hydrolases.
    J Biol Chem. 1992 May 25;267(15):10481-8 PMID: 1375222
  5. Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor.
    J Bacteriol. 1992 Aug;174(16):5204-10 PMID: 1322883
  6. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity.
    J Exp Med. 1992 Aug 1;176(2):415-26 PMID: 1500854
  7. Nitric oxide causes ADP-ribosylation and inhibition of glyceraldehyde-3-phosphate dehydrogenase.
    J Biol Chem. 1992 Aug 25;267(24):16771-4 PMID: 1512218
  8. Nitric oxide as a secretory product of mammalian cells.
    FASEB J. 1992 Sep;6(12):3051-64 PMID: 1381691
  9. Nitric oxide stimulates auto-ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9382-5 PMID: 1409644
  10. Amino acid-specific ADP-ribosylation: structural characterization and chemical differentiation of ADP-ribose-cysteine adducts formed nonenzymatically and in a pertussis toxin-catalyzed reaction.
    Biochemistry. 1992 Dec 1;31(47):11881-7 PMID: 1445918
  11. Characterization of a nitric-oxide-catalysed ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase.
    Eur J Biochem. 1992 Nov 15;210(1):305-10 PMID: 1446679
  12. Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation.
    J Biol Chem. 1992 Dec 15;267(35):24929-32 PMID: 1281150
  13. Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase.
    Science. 1993 Jan 15;259(5093):365-8 PMID: 8420004
  14. The relationship between cell growth, macromolecular synthesis and poly ADP-ribose polymerase in lymphoid cells.
    Exp Cell Res. 1974 Jan;83(1):63-72 PMID: 4360096
  15. Amino acid-specific ADP-ribosylation. Identification of an arginine-dependent ADP-ribosyltransferase in rat liver.
    J Biol Chem. 1981 Aug 10;256(15):7830-3 PMID: 6267027
  16. Covalent modification of the iron protein of nitrogenase from Rhodospirillum rubrum by adenosine diphosphoribosylation of a specific arginine residue.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3173-7 PMID: 3923473
  17. ADP-ribosylation.
    Annu Rev Biochem. 1985;54:73-100 PMID: 3927821
  18. Pertussis toxin-catalyzed ADP-ribosylation of transducin. Cysteine 347 is the ADP-ribose acceptor site.
    J Biol Chem. 1985 Nov 25;260(27):14428-30 PMID: 3863818
  19. Identification of the 37-kDa protein displaying a variable interaction with the erythroid cell membrane as glyceraldehyde-3-phosphate dehydrogenase.
    J Biol Chem. 1987 Jan 15;262(2):649-53 PMID: 3027061
  20. ADP-ribosylation of guanyl nucleotide-binding regulatory proteins by bacterial toxins.
    Adv Enzymol Relat Areas Mol Biol. 1988;61:303-79 PMID: 3128060
  21. Eukaryotic mono(ADP-ribosyl)transferase that ADP-ribosylates GTP-binding regulatory Gi protein.
    J Biol Chem. 1988 Apr 15;263(11):5485-9 PMID: 3128540
  22. Isolation and characterization of the cell-associated region of group A streptococcal M6 protein.
    J Bacteriol. 1988 Jun;170(6):2618-24 PMID: 2453502
  23. Activation of a cytosolic ADP-ribosyltransferase by nitric oxide-generating agents.
    J Biol Chem. 1989 May 25;264(15):8455-8 PMID: 2542278
  24. Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose 1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli.
    Mol Microbiol. 1989 Jun;3(6):723-32 PMID: 2546007
  25. The major parasite surface antigen associated with human resistance to schistosomiasis is a 37-kD glyceraldehyde-3P-dehydrogenase.
    J Exp Med. 1989 Dec 1;170(6):2065-80 PMID: 2584935
  26. Identification of an endogenous membrane anchor-cleaving enzyme for group A streptococcal M protein. Its implication for the attachment of surface proteins in gram-positive bacteria.
    J Exp Med. 1989 Dec 1;170(6):2119-33 PMID: 2531195
  27. Identification in human erythrocytes of mono(ADP-ribosyl) protein hydrolase that cleaves a mono(ADP-ribosyl) Gi linkage.
    FEBS Lett. 1990 Feb 26;261(2):381-4 PMID: 2107103
  28. Properties of a novel nitric oxide-stimulated ADP-ribosyltransferase.
    Arch Biochem Biophys. 1990 Jun;279(2):286-90 PMID: 2112369
  29. The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship.
    Eur J Biochem. 1991 Jun 1;198(2):421-8 PMID: 2040303
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1993-09-01
Pages
8154-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC47307
Subset
IM
Grants
NIAID NIH HHS · AI11822 · United States
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