Identification of the Protein Glycation Sites in Human Myoglobin As Rapidly Induced by D-Ribose

Overview

Journal Molecules

Publisher MDPI

Specialty Biology

Date 2021 Oct 13

PMID 34641382

Citations 5

Authors

Jing-Jing Liu

Yong You

Shu-Qin Gao

Shuai Tang

Lei Chen

Ge-Bo Wen

Ying-Wu Lin

Affiliations

Soon will be listed here.

Abstract

Protein glycation is an important protein post-translational modification and is one of the main pathogenesis of diabetic angiopathy. Other than glycated hemoglobin, the protein glycation of other globins such as myoglobin (Mb) is less studied. The protein glycation of human Mb with ribose has not been reported, and the glycation sites in the Mb remain unknown. This article reports that d-ribose undergoes rapid protein glycation of human myoglobin (HMb) at lysine residues (K34, K87, K56, and K147) on the protein surface, as identified by ultra-high performance liquid chromatography-mass spectrometry (UHPLC-MS) and electrospray ionization tandem mass spectrometry (ESI-MS/MS). Moreover, glycation by d-ribose at these sites slightly decreased the rate of the met heme (Fe) in reaction with HO to form a ferryl heme (Fe=O). This study provides valuable insight into the protein glycation by d-ribose and provides a foundation for studying the structure and function of glycated heme proteins.

Citing Articles

Anhydrous microwave synthesis as efficient method for obtaining model advanced glycation end-products.

Bronowicka-Szydelko A, Madziarska K, Kuzan A, Lewandowski L, Adamiec-Mroczek J, Pietkiewicz J Front Mol Biosci. 2024; 11:1484196.

PMID: 39606032 PMC: 11599739. DOI: 10.3389/fmolb.2024.1484196.

D-ribose metabolic disorder and diabetes mellitus.

Tai Y, Zhang Z, Liu Z, Li X, Yang Z, Wang Z Mol Biol Rep. 2024; 51(1):220.

PMID: 38281218 PMC: 10822815. DOI: 10.1007/s11033-023-09076-y.

Ribose Intake as Food Integrator: Is It a Really Convenient Practice?.

Moschini R, Balestri F, Cappiello M, Signore G, Mura U, Del-Corso A Biomolecules. 2022; 12(12).

PMID: 36551203 PMC: 9776227. DOI: 10.3390/biom12121775.

Analysis of the Site-Specific Myoglobin Modifications in the Melibiose-Derived Novel Advanced Glycation End-Product.

Gostomska-Pampuch K, Wisniewski J, Sowinski K, Gruszecki W, Gamian A, Staniszewska M Int J Mol Sci. 2022; 23(21).

PMID: 36361822 PMC: 9655033. DOI: 10.3390/ijms232113036.

The potential role of albumin glycation by ribose in diabetes mellitus.

Mou L, Cao X, He T, He R Sci China Life Sci. 2022; 65(12):2552-2555.

PMID: 36251157 DOI: 10.1007/s11427-022-2190-6.

References

Ghazanfari-Sarabi S, Habibi-Rezaei M, Eshraghi-Naeeni R, Moosavi-Movahedi A . Prevention of haemoglobin glycation by acetylsalicylic acid (ASA): A new view on old mechanism. PLoS One. 2019; 14(4):e0214725. PMC: 6464172. DOI: 10.1371/journal.pone.0214725. View

Guariguata L, Whiting D, Hambleton I, Beagley J, Linnenkamp U, Shaw J . Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014; 103(2):137-49. DOI: 10.1016/j.diabres.2013.11.002. View

Wu L, Yuan H, Gao S, You Y, Nie C, Wen G . Regulating the nitrite reductase activity of myoglobin by redesigning the heme active center. Nitric Oxide. 2016; 57:21-29. DOI: 10.1016/j.niox.2016.04.007. View

Nelson D, Kiesow L . Enthalpy of decomposition of hydrogen peroxide by catalase at 25 degrees C (with molar extinction coefficients of H 2 O 2 solutions in the UV). Anal Biochem. 1972; 49(2):474-8. DOI: 10.1016/0003-2697(72)90451-4. View

Li S, Wang J, Xiao Y, Zhang L, Fang J, Yang N . D-ribose: Potential clinical applications in congestive heart failure and diabetes, and its complications (Review). Exp Ther Med. 2021; 21(5):496. PMC: 8005739. DOI: 10.3892/etm.2021.9927. View

Schalkwijk C, Ligtvoet N, Twaalfhoven H, Jager A, Blaauwgeers H, Schlingemann R . Amadori albumin in type 1 diabetic patients: correlation with markers of endothelial function, association with diabetic nephropathy, and localization in retinal capillaries. Diabetes. 1999; 48(12):2446-53. DOI: 10.2337/diabetes.48.12.2446. View

Frolov A, Hoffmann P, Hoffmann R . Fragmentation behavior of glycated peptides derived from D-glucose, D-fructose and D-ribose in tandem mass spectrometry. J Mass Spectrom. 2006; 41(11):1459-69. DOI: 10.1002/jms.1117. View

van Steen S, Schrieks I, Hoekstra J, Lincoff A, Tardif J, Mellbin L . The haemoglobin glycation index as predictor of diabetes-related complications in the AleCardio trial. Eur J Prev Cardiol. 2017; 24(8):858-866. DOI: 10.1177/2047487317692664. View

Gladwin M, Kim-Shapiro D . The functional nitrite reductase activity of the heme-globins. Blood. 2008; 112(7):2636-47. PMC: 2556603. DOI: 10.1182/blood-2008-01-115261. View

10.

Shapiro R, McMANUS M, Zalut C, BUNN H . Sites of nonenzymatic glycosylation of human hemoglobin A. J Biol Chem. 1980; 255(7):3120-7. View

11.

Liu C, Yuan H, Liao F, Wei C, Du K, Gao S . Unique Tyr-heme double cross-links in F43Y/T67R myoglobin: an artificial enzyme with a peroxidase activity comparable to that of native peroxidases. Chem Commun (Camb). 2019; 55(46):6610-6613. DOI: 10.1039/c9cc02714a. View

12.

Adrover M, Marino L, Sanchis P, Pauwels K, Kraan Y, Lebrun P . Mechanistic insights in glycation-induced protein aggregation. Biomacromolecules. 2014; 15(9):3449-62. DOI: 10.1021/bm501077j. View

13.

Schalkwijk C, Stehouwer C, van Hinsbergh V . Fructose-mediated non-enzymatic glycation: sweet coupling or bad modification. Diabetes Metab Res Rev. 2004; 20(5):369-82. DOI: 10.1002/dmrr.488. View

14.

Siddiqui Z, Faisal M, Alatar A, Ahmad S . Prevalence of auto-antibodies against D-ribose-glycated-hemoglobin in diabetes mellitus. Glycobiology. 2019; 29(5):409-418. DOI: 10.1093/glycob/cwz012. View

15.

Bokiej M, Livermore A, Harris A, Onishi A, Sandwick R . Ribose sugars generate internal glycation cross-links in horse heart myoglobin. Biochem Biophys Res Commun. 2011; 407(1):191-6. PMC: 3086664. DOI: 10.1016/j.bbrc.2011.02.138. View

16.

Liu H, Li L, He B, Gao S, Wen G, Lin Y . Neuroglobin is capable of self-oxidation of methionine64 introduced at the heme axial position. Dalton Trans. 2018; 47(32):10847-10852. DOI: 10.1039/c8dt02397b. View

17.

Soboleva A, Schmidt R, Vikhnina M, Grishina T, Frolov A . Maillard Proteomics: Opening New Pages. Int J Mol Sci. 2017; 18(12). PMC: 5751279. DOI: 10.3390/ijms18122677. View

18.

Chen X, Su T, Chen Y, He Y, Liu Y, Xu Y . d-Ribose as a Contributor to Glycated Haemoglobin. EBioMedicine. 2017; 25:143-153. PMC: 5704047. DOI: 10.1016/j.ebiom.2017.10.001. View

19.

Chen Y, Yu L, Wang Y, Wei Y, Xu Y, He T . d-Ribose contributes to the glycation of serum protein. Biochim Biophys Acta Mol Basis Dis. 2019; 1865(9):2285-2292. DOI: 10.1016/j.bbadis.2019.05.005. View

20.

Hori H, Andersson L, Prince R, Pickering I, George G, Sanders 2nd C . Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants. J Biol Chem. 1992; 267(32):22843-52. View