Relative quantitative analysis of human plasma <em>O</em>‑sulfotyrosine using HPLC‑MS/MS in linear negative ion mode

Dai,Daopeng; Ruan,Zhanwei; Han,Hui; Zhu,Jinzhou; Zhang,Ruiyan

doi:10.3892/wasj.2021.95

Relative quantitative analysis of human plasma O‑sulfotyrosine using HPLC‑MS/MS in linear negative ion mode

Authors:
- Daopeng Dai
- Zhanwei Ruan
- Hui Han
- Jinzhou Zhu
- Ruiyan Zhang
View Affiliations

Affiliations: Department of Vascular and Cardiology, Ruijin Hospital, Shanghai Jiaotong University School of Medicine, Shanghai 200025, P.R. China, Department of Emergency, The Third Affiliated Hospital to Wenzhou Medical University, Wenzhou, Zhejiang 325200, P.R. China
Published online on: March 11, 2021 https://doi.org/10.3892/wasj.2021.95
Article Number: 24
Copyright: © Dai et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Sulfation has been recognized as a key post‑translational modification in regulating various cellular processes. By contrast, the development of detection methods for protein sulfation is hindered due to the lack of available immune antibodies and lability of this modification. Recently, the serum level of O‑sulfotyrosine was reported to be associated with a decline in renal function, indicating a potential diagnostic value of the O‑sulfotyrosine concentration for certain diseases. The present study describes a sensitive and reproducible method for the relative quantitative analysis of human plasma O‑sulfotyrosine using high performance liquid chromatography (HPLC)‑tandem mass spectrometry (MS/MS) in a linear negative ion mode. The increase in plasma O‑sulfotyrosine levels in patients with chronic kidney disease was confirmed. This method is sensitive and reproducible with a low extraction effect, good intraday precision and inter‑day repeatability. A significantly increased plasma O‑sulfotyrosine concentration was confirmed in patients with chronic kidney disease compared to the healthy controls. Thus, determining the O‑sulfotyrosine concentration in plasma may be an easy method which can reflect the sulfation level in vivo under physical and pathological conditions.

View Figures

View References

1	Bettelheim FR: Tyrosine-O-sulfate in a peptide from fibrinogen. J Am Chem Soc. 76:2838–2839. 1954.
2	Huttner WB: Sulphation of tyrosine residues-a widespread modification of proteins. Nature. 299:273–276. 1982.PubMed/NCBI View Article : Google Scholar
3	Huttner WB: Tyrosine sulfation and the secretory pathway. Annu Rev Physiol. 50:363–376. 1988.PubMed/NCBI View Article : Google Scholar
4	Hsu W, Rosenquist GL, Ansari AA and Gershwin ME: Autoimmunity and tyrosine sulfation. Autoimmun Rev. 4:429–435. 2005.PubMed/NCBI View Article : Google Scholar
5	Pouyani T and Seed B: PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell. 83:333–343. 1995.PubMed/NCBI View Article : Google Scholar
6	Bundgaard JR, Vuust J and Rehfeld JF: Tyrosine O-sulfation promotes proteolytic processing of progastrin. EMBO J. 14:3073–3079. 1995.PubMed/NCBI
7	Friederich E, Fritz HJ and Huttner WB: Inhibition of tyrosine sulfation in the trans-Golgi retards the transport of a constitutively secreted protein to the cell surface. J Cell Biol. 107:1655–1667. 1988.PubMed/NCBI View Article : Google Scholar
8	Leung AW, Backstrom I and Bally MB: Sulfonation, an underexploited area: From skeletal development to infectious diseases and cancer. Oncotarget. 7:55811–55827. 2016.PubMed/NCBI View Article : Google Scholar
9	Nishimura Y, Wakita T and Shimizu H: Tyrosine sulfation of the amino terminus of PSGL-1 is critical for enterovirus 71 infection. PLoS Pathog. 6(e1001174)2010.PubMed/NCBI View Article : Google Scholar
10	Koltsova E and Ley K: Tyrosine sulfation of leukocyte adhesion molecules and chemokine receptors promotes atherosclerosis. Arterioscler Thromb Vasc Biol. 29:1709–1711. 2009.PubMed/NCBI View Article : Google Scholar
11	Huttner WB: Determination and occurrence of tyrosine O-sulfate in proteins. Methods Enzymol. 107:200–223. 1984.PubMed/NCBI View Article : Google Scholar
12	Yu Y, Hoffhines AJ, Moore KL and Leary JA: Determination of the sites of tyrosine O-sulfation in peptides and proteins. Nat Methods. 4:583–588. 2007.PubMed/NCBI View Article : Google Scholar
13	Monigatti F, Gasteiger E, Bairoch A and Jung E: The Sulfinator: Predicting tyrosine sulfation sites in protein sequences. Bioinformatics. 18:769–770. 2002.PubMed/NCBI View Article : Google Scholar
14	Hoffhines AJ, Damoc E, Bridges KG, Leary JA and Moore KL: Detection and purification of tyrosine-sulfated proteins using a novel anti-sulfotyrosine monoclonal antibody. J Biol Chem. 281:37877–37887. 2006.PubMed/NCBI View Article : Google Scholar
15	Kehoe JW, Velappan N, Walbolt M, Rasmussen J, King D, Lou J, Knopp K, Pavlik P, Marks JD, Bertozzi CR, et al: Using phage display to select antibodies recognizing post-translational modifications independently of sequence context. Mol Cell Proteomics. 5:2350–2363. 2006.PubMed/NCBI View Article : Google Scholar
16	Rodgers SD, Camphausen RT and Hammer DA: Tyrosine sulfation enhances but is not required for PSGL-1 rolling adhesion on P-selectin. Biophys J. 81:2001–2009. 2001.PubMed/NCBI View Article : Google Scholar
17	Yagami T, Kitagawa K, Aida C, Fujiwara H and Futaki S: Stabilization of a tyrosine O-sulfate residue by a cationic functional group: Formation of a conjugate acid-base pair. J Pept Res. 56:239–249. 2000.PubMed/NCBI View Article : Google Scholar
18	Balsved D, Bundgaard JR and Sen JW: Stability of tyrosine sulfate in acidic solutions. Anal Biochem. 363:70–76. 2007.PubMed/NCBI View Article : Google Scholar
19	Niewczas MA, Mathew AV, Croall S, Byun J, Major M, Sabisetti VS, Smiles A, Bonventre JV, Pennathur S and Krolewski AS: Circulating modified metabolites and a risk of ESRD in patients with type 1 diabetes and chronic kidney disease. Diabetes Care. 40:383–390. 2017.PubMed/NCBI View Article : Google Scholar
20	Vanholder R, Hoefliger N, De Smet R, Ringoir S and Vogeleere P: Extraction of protein bound ligands from azotemic sera: Comparison of 12 deproteinization methods. Kidney Int. 41:1707–1712. 1992.PubMed/NCBI View Article : Google Scholar
21	Robinson MR, Moore KL and Brodbelt JS: Direct identification of tyrosine sulfation by using ultraviolet photodissociation mass spectrometry. J Am Soc Mass Spectrom. 25:1461–1471. 2014.PubMed/NCBI View Article : Google Scholar
22	Tallan HH, Bella ST, Stein WH and Moore S: Tyrosine-O-sulfate as a constituent of normal human urine. J Biol Chem. 217:703–708. 1955.PubMed/NCBI
23	Phillips LS and Kopple JD: Circulating somatomedin activity and sulfate levels in adults with normal and impaired kidney function. Metabolism. 30:1091–1095. 1981.PubMed/NCBI View Article : Google Scholar
24	Freeman RM and Richards CJ: Studies on sulfate in end-stage renal disease. Kidney Int. 15:167–175. 1979.PubMed/NCBI View Article : Google Scholar
25	Mulder GJ and Scholtens E: The availability of inorganic sulphate in blood for sulphate conjugation of drugs in rat liver in vivo. (35S)Sulphate incorporation into harmol sulphate. Biochem J. 172:247–251. 1978.PubMed/NCBI View Article : Google Scholar