Identification of Protein Targets of -Nitroso-Coenzyme A-Mediated -Nitrosation Using Chemoproteomics

Overview

Journal ACS Chem Biol

Publisher American Chemical Society

Specialties Biochemistry
Biology

Date 2023 Dec 30

PMID 38159293

Authors

Julia A Falco

Sarah L Wynia-Smith

James McCoy

Brian C Smith

Eranthie Weerapana

Affiliations

Soon will be listed here.

Abstract

-Nitrosation is a cysteine post-translational modification fundamental to cellular signaling. This modification regulates protein function in numerous biological processes in the nervous, cardiovascular, and immune systems. Small molecule or protein nitrosothiols act as mediators of NO signaling by transferring the NO group (formally NO) to a free thiol on a target protein through a transnitrosation reaction. The protein targets of specific transnitrosating agents and the extent and functional effects of -nitrosation on these target proteins have been poorly characterized. -nitroso-coenzyme A (CoA-SNO) was recently identified as a mediator of endogenous -nitrosation. Here, we identified direct protein targets of CoA-SNO-mediated transnitrosation using a competitive chemical-proteomic approach that quantified the extent of modification on 789 cysteine residues in response to CoA-SNO. A subset of cysteines displayed high susceptibility to modification by CoA-SNO, including previously uncharacterized sites of -nitrosation. We further validated and functionally characterized the functional effects of -nitrosation on the protein targets phosphofructokinase (platelet type), ATP citrate synthase, and ornithine aminotransferase.

References

Stomberski C, Hess D, Stamler J . Protein S-Nitrosylation: Determinants of Specificity and Enzymatic Regulation of S-Nitrosothiol-Based Signaling. Antioxid Redox Signal. 2017; 30(10):1331-1351. PMC: 6391618. DOI: 10.1089/ars.2017.7403. View

Nakamura T, Lipton S . Emerging role of protein-protein transnitrosylation in cell signaling pathways. Antioxid Redox Signal. 2012; 18(3):239-49. PMC: 3518546. DOI: 10.1089/ars.2012.4703. View

Lee S, Kim C, Lee K, Ahn J . S-nitrosylation of B23/nucleophosmin by GAPDH protects cells from the SIAH1-GAPDH death cascade. J Cell Biol. 2012; 199(1):65-76. PMC: 3461512. DOI: 10.1083/jcb.201205015. View

Greco T, Hodara R, Parastatidis I, Heijnen H, Dennehy M, Liebler D . Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells. Proc Natl Acad Sci U S A. 2006; 103(19):7420-5. PMC: 1464354. DOI: 10.1073/pnas.0600729103. View

Zhou Y, Wynia-Smith S, Couvertier S, Kalous K, Marletta M, Smith B . Chemoproteomic Strategy to Quantitatively Monitor Transnitrosation Uncovers Functionally Relevant S-Nitrosation Sites on Cathepsin D and HADH2. Cell Chem Biol. 2016; 23(6):727-37. PMC: 4920707. DOI: 10.1016/j.chembiol.2016.05.008. View

Anand P, Hausladen A, Wang Y, Zhang G, Stomberski C, Brunengraber H . Identification of S-nitroso-CoA reductases that regulate protein S-nitrosylation. Proc Natl Acad Sci U S A. 2014; 111(52):18572-7. PMC: 4284529. DOI: 10.1073/pnas.1417816112. View

Martinez M, Andriantsitohaina R . Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid Redox Signal. 2008; 11(3):669-702. DOI: 10.1089/ars.2007.1993. View

Stricker N, Christopherson K, Yi B, Schatz P, Raab R, Dawes G . PDZ domain of neuronal nitric oxide synthase recognizes novel C-terminal peptide sequences. Nat Biotechnol. 1997; 15(4):336-42. DOI: 10.1038/nbt0497-336. View

Marin-Hernandez A, Gallardo-Perez J, Ralph S, Rodriguez-Enriquez S, Moreno-Sanchez R . HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem. 2009; 9(9):1084-101. DOI: 10.2174/138955709788922610. View

10.

Halliday K, Sillerud L . Differentiation of human tumors from nonmalignant tissue by natural-abundance 13C NMR spectroscopy. Magn Reson Med. 1988; 7(4):384-411. DOI: 10.1002/mrm.1910070403. View

11.

Perissinotti L, Turjanski A, Estrin D, Doctorovich F . Transnitrosation of nitrosothiols: characterization of an elusive intermediate. J Am Chem Soc. 2005; 127(2):486-7. DOI: 10.1021/ja044056v. View

12.

Chen Y, Lu C, Su M, Huang K, Ching W, Yang H . dbSNO 2.0: a resource for exploring structural environment, functional and disease association and regulatory network of protein S-nitrosylation. Nucleic Acids Res. 2014; 43(Database issue):D503-11. PMC: 4383970. DOI: 10.1093/nar/gku1176. View

13.

Li C, Feng J, Wu Y, Zhang G . Cerebral ischemia-reperfusion induces GAPDH S-nitrosylation and nuclear translocation. Biochemistry (Mosc). 2012; 77(6):671-8. DOI: 10.1134/S0006297912060156. View

14.

Migita T, Narita T, Nomura K, Miyagi E, Inazuka F, Matsuura M . ATP citrate lyase: activation and therapeutic implications in non-small cell lung cancer. Cancer Res. 2008; 68(20):8547-54. DOI: 10.1158/0008-5472.CAN-08-1235. View

15.

Wei Z, Oh J, Flavell R, Crawford J . LACC1 bridges NOS2 and polyamine metabolism in inflammatory macrophages. Nature. 2022; 609(7926):348-353. PMC: 9813773. DOI: 10.1038/s41586-022-05111-3. View

16.

Kloos M, Bruser A, Kirchberger J, Schoneberg T, Strater N . Crystal structure of human platelet phosphofructokinase-1 locked in an activated conformation. Biochem J. 2015; 469(3):421-32. DOI: 10.1042/BJ20150251. View

17.

Turyn J, Schlichtholz B, Dettlaff-Pokora A, Presler M, Goyke E, Matuszewski M . Increased activity of glycerol 3-phosphate dehydrogenase and other lipogenic enzymes in human bladder cancer. Horm Metab Res. 2003; 35(10):565-9. DOI: 10.1055/s-2003-43500. View

18.

Zhao S, Tang X, Miao Z, Chen Y, Cao J, Song T . Hsp90 S-nitrosylation at Cys521, as a conformational switch, modulates cycling of Hsp90-AHA1-CDC37 chaperone machine to aggravate atherosclerosis. Redox Biol. 2022; 52:102290. PMC: 8942817. DOI: 10.1016/j.redox.2022.102290. View

19.

Inadomi C, Murata H, Ihara Y, Goto S, Urata Y, Yodoi J . Overexpression of glutaredoxin protects cardiomyocytes against nitric oxide-induced apoptosis with suppressing the S-nitrosylation of proteins and nuclear translocation of GAPDH. Biochem Biophys Res Commun. 2012; 425(3):656-61. DOI: 10.1016/j.bbrc.2012.07.118. View

20.

Calabrese V, Cornelius C, Rizzarelli E, Owen J, Dinkova-Kostova A, Butterfield D . Nitric oxide in cell survival: a janus molecule. Antioxid Redox Signal. 2009; 11(11):2717-39. DOI: 10.1089/ars.2009.2721. View