Complex Nature of Protein Carbonylation Specificity After Metal-Catalyzed Oxidation

Overview

Journal Pharm Res

Specialties Pharmacology
Pharmacy

Date 2017 Feb 3

PMID 28150167

Citations 7

Authors

Dmitry Kryndushkin

Wells W Wu

Ramesh Venna

Michael A Norcross

Rong-Fong Shen

V Ashutosh Rao

Affiliations

Soon will be listed here.

Abstract

Purpose: Protein carbonylation is an irreversible modification of Lys, Arg, Thr and Pro amino acids under conditions of oxidative stress. Previous studies have reported specific carbonylated residues in purified recombinant albumins, albeit with a lack of agreement between the studies. Currently, structural factors that determine site-specific protein carbonylation are not well understood.

Methods: In this study, we utilized metal-catalyzed oxidizing conditions to generate carbonylation in recombinant human serum albumin (HSA) and granulocyte-colony stimulating factor (G-CSF), two proteins with distinct metal-binding abilities. To estimate predictability of HSA carbonylation sites, the same oxidative reaction was repeated based on the previously reported conditions. For G-CSF, oxidative conditions were gradually adjusted to achieve substantial levels of protein carbonylation. Corresponding accumulation of specific oxidized residues was identified and confirmed with high-resolution mass spectrometry.

Results: Our HSA dataset contained 55 carbonylated residues and showed a significant overlap with the previously published pooled data, indicating a certain level of carbonylation site specificity for albumins. Oxidation of G-CSF under multiple oxidative conditions consistently showed a highly specific carbonylation at position Pro45. We also detected a previously unreported, oxidation-induced cleavage site in G-CSF between His44 and Pro45, which might be attributed to a presence of a potential metal-binding site near residue Pro45.

Conclusions: Our results show distinct patterns of protein carbonylation for HSA and G-CSF. Thus, specificity of protein carbonylation induced by metal-catalyzed oxidation is protein dependent and might be predicted by availability of transition metal binding site(s) within the protein.

Citing Articles

Regulation of Redox Profile and Genomic Instability by Physical Exercise Contributes to Neuroprotection in Mice with Experimental Glioblastoma.

Marqueze L, Costa A, Pedroso G, Vasconcellos F, Pilger B, Kindermann S Antioxidants (Basel). 2023; 12(7).

PMID: 37507883 PMC: 10376052. DOI: 10.3390/antiox12071343.

Effect of the metal ion-induced carbonylation modification of mitochondrial membrane channel protein VDAC on cell vitality, seedling growth and seed aging.

Li Y, Liu C, Qi M, Ye T, Kang Y, Wang Y Front Plant Sci. 2023; 14:1138781.

PMID: 37324694 PMC: 10264620. DOI: 10.3389/fpls.2023.1138781.

Effects of Packaging Materials on Structural and Simulated Digestive Characteristics of Walnut Protein during Accelerated Storage.

Han M, Zhao J, Wu Q, Mao X, Zhang J Foods. 2023; 12(3).

PMID: 36766154 PMC: 9913943. DOI: 10.3390/foods12030620.

Metal-induced oxidative stress and human plasma protein oxidation after SARS-CoV-2 infection.

Aryal B, Tillotson J, Ok K, Stoltzfus A, Michel S, Rao V Sci Rep. 2023; 13(1):2441.

PMID: 36765106 PMC: 9916496. DOI: 10.1038/s41598-023-29119-5.

The Combined Administration of Vitamin C and Copper Induces a Systemic Oxidative Stress and Kidney Injury.

Jiang R, Sui Y, Hong J, Niimi M, Yan Q, Shi Z Biomolecules. 2023; 13(1).

PMID: 36671529 PMC: 9856059. DOI: 10.3390/biom13010143.

References

Sokolowska M, Wszelaka-Rylik M, Poznanski J, Bal W . Spectroscopic and thermodynamic determination of three distinct binding sites for Co(II) ions in human serum albumin. J Inorg Biochem. 2009; 103(7):1005-13. DOI: 10.1016/j.jinorgbio.2009.04.011. View

Hill C, Osslund T, Eisenberg D . The structure of granulocyte-colony-stimulating factor and its relationship to other growth factors. Proc Natl Acad Sci U S A. 1993; 90(11):5167-71. PMC: 46676. DOI: 10.1073/pnas.90.11.5167. View

Guedes S, Vitorino R, Domingues R, Amado F, Domingues P . Oxidation of bovine serum albumin: identification of oxidation products and structural modifications. Rapid Commun Mass Spectrom. 2009; 23(15):2307-15. DOI: 10.1002/rcm.4149. View

Uehara H, Rao V . Metal-mediated protein oxidation: applications of a modified ELISA-based carbonyl detection assay for complex proteins. Pharm Res. 2014; 32(2):691-701. DOI: 10.1007/s11095-014-1496-y. View

Bal W, Sokolowska M, Kurowska E, Faller P . Binding of transition metal ions to albumin: sites, affinities and rates. Biochim Biophys Acta. 2013; 1830(12):5444-55. DOI: 10.1016/j.bbagen.2013.06.018. View

Temple A, Yen T, Gronert S . Identification of specific protein carbonylation sites in model oxidations of human serum albumin. J Am Soc Mass Spectrom. 2006; 17(8):1172-80. DOI: 10.1016/j.jasms.2006.04.030. View

Zhao F, Aced G, Hong J, Milby T, Schoneich C . Metal-catalyzed oxidation of histidine in human growth hormone. Mechanism, isotope effects, and inhibition by a mild denaturing alcohol. J Biol Chem. 1997; 272(14):9019-29. DOI: 10.1074/jbc.272.14.9019. View

Sugio S, Kashima A, Mochizuki S, Noda M, Kobayashi K . Crystal structure of human serum albumin at 2.5 A resolution. Protein Eng. 1999; 12(6):439-46. DOI: 10.1093/protein/12.6.439. View

Bridgewater J, Lim J, Vachet R . Transition metal-peptide binding studied by metal-catalyzed oxidation reactions and mass spectrometry. Anal Chem. 2006; 78(7):2432-8. DOI: 10.1021/ac051983r. View

10.

Xu X, Zhang L, Shen D, Wu H, Liu Q . Oxygen-dependent oxidation of Fe(II) to Fe(III) and interaction of Fe(III) with bovine serum albumin, leading to a hysteretic effect on the fluorescence of bovine serum albumin. J Fluoresc. 2007; 18(1):193-201. DOI: 10.1007/s10895-007-0263-4. View

11.

Majorek K, Porebski P, Dayal A, Zimmerman M, Jablonska K, Stewart A . Structural and immunologic characterization of bovine, horse, and rabbit serum albumins. Mol Immunol. 2012; 52(3-4):174-82. PMC: 3401331. DOI: 10.1016/j.molimm.2012.05.011. View

12.

Torosantucci R, Schoneich C, Jiskoot W . Oxidation of therapeutic proteins and peptides: structural and biological consequences. Pharm Res. 2013; 31(3):541-53. DOI: 10.1007/s11095-013-1199-9. View

13.

Bollineni R, Fedorova M, Hoffmann R . Qualitative and quantitative evaluation of derivatization reagents for different types of protein-bound carbonyl groups. Analyst. 2013; 138(17):5081-8. DOI: 10.1039/c3an00724c. View

14.

Madian A, Regnier F . Proteomic identification of carbonylated proteins and their oxidation sites. J Proteome Res. 2010; 9(8):3766-80. PMC: 3214645. DOI: 10.1021/pr1002609. View

15.

Babor M, Gerzon S, Raveh B, Sobolev V, Edelman M . Prediction of transition metal-binding sites from apo protein structures. Proteins. 2007; 70(1):208-17. DOI: 10.1002/prot.21587. View

16.

Maisonneuve E, Ducret A, Khoueiry P, Lignon S, Longhi S, Talla E . Rules governing selective protein carbonylation. PLoS One. 2009; 4(10):e7269. PMC: 2751825. DOI: 10.1371/journal.pone.0007269. View

17.

Silva A, Hider R . Influence of non-enzymatic post-translation modifications on the ability of human serum albumin to bind iron. Implications for non-transferrin-bound iron speciation. Biochim Biophys Acta. 2009; 1794(10):1449-58. DOI: 10.1016/j.bbapap.2009.06.003. View

18.

Petersen B, Petersen T, Andersen P, Nielsen M, Lundegaard C . A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct Biol. 2009; 9:51. PMC: 2725087. DOI: 10.1186/1472-6807-9-51. View

19.

Zaveckas M, Zvirbliene A, Zvirblis G, Chmieliauskaite V, Bumelis V, Pesliakas H . Effect of surface histidine mutations and their number on the partitioning and refolding of recombinant human granulocyte-colony stimulating factor (Cys17Ser) in aqueous two-phase systems containing chelated metal ions. J Chromatogr B Analyt Technol Biomed Life Sci. 2007; 852(1-2):409-19. DOI: 10.1016/j.jchromb.2007.01.051. View

20.

Kryndushkin D, Rao V . Comparative Effects of Metal-Catalyzed Oxidizing Systems on Carbonylation and Integrity of Therapeutic Proteins. Pharm Res. 2015; 33(2):526-39. DOI: 10.1007/s11095-015-1807-y. View