514
Views
15
CrossRef citations to date
0
Altmetric
Review Article

4-Hydroxy-2-nonenal, a lipid peroxidation product, as a biomarker in diabetes and its complications: challenges and opportunities

, , , , , , & ORCID Icon show all
Pages 510-524 | Received 30 Sep 2020, Accepted 15 Dec 2020, Published online: 07 Jan 2021

References

  • Petrie JR, Guzik TJ, Touyz RM. Diabetes, hypertension, and cardiovascular disease: clinical insights and vascular mechanisms. Can J Cardiol. 2018;34(5):575–584.
  • Gianazza E, Brioschi M, Fernandez AM, et al. Lipoxidation in cardiovascular diseases. Redox Biol. 2019;23:101119.
  • Vistoli G, De Maddis D, Cipak A, et al. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res. 2013;47(Suppl 1):3–27.
  • Ito F, Sono Y, Ito T. Measurement and clinical significance of lipid peroxidation as a biomarker of oxidative stress: oxidative stress in diabetes, atherosclerosis, and chronic inflammation. Antioxidants (Basel). 2019;8(3):72.
  • Dator RP, Solivio MJ, Villalta PW, et al. Bioanalytical and mass spectrometric methods for aldehyde profiling in biological fluids. Toxics. 2019;7(2):32.
  • Tsikas D. Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: analytical and biological challenges. Anal Biochem. 2017;524:13–30.
  • Hall SE, Aitken RJ, Nixon B, et al. Electrophilic aldehyde products of lipid peroxidation selectively adduct to heat shock protein 90 and arylsulfatase A in stallion spermatozoa. Biol Reprod. 2017;96(1):107–121.
  • Griendling KK, Touyz RM, Zweier JL, et al. Measurement of reactive oxygen species, reactive nitrogen species, and redox-dependent signaling in the cardiovascular system: a scientific statement from the American Heart Association. Circ Res. 2016;119(5):e39–e75.
  • Semchyshyn HM. Reactive carbonyl species in vivo: generation and dual biological effects. Sci World J. 2014;2014:417842.
  • Singh M, Kapoor A, Bhatnagar A. Oxidative and reductive metabolism of lipid-peroxidation derived carbonyls. Chem Biol Interact. 2015;234:261–273.
  • Ayala A, Munoz MF, Arguelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438.
  • Centers for Disease Control and Prevention. National Diabetes Statistics Report. Atlanta (GA): Centers for Disease Control and Prevention, U.S. Dept of Health and Human Services; 2020.
  • Boyle JP, Honeycutt AA, Narayan KM, et al. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U.S. Diabetes Care. 2001;24(11):1936–1940.
  • American Diabetes Association. 2. Classification and diagnosis of diabetes: standards of medical care in diabetes-2020. Diabetes Care. 2020;43(Suppl 1):S14–S31.
  • Barrett EJ, Liu Z, Khamaisi M, et al. Diabetic microvascular disease: an endocrine society scientific statement. J Clin Endocrinol Metab. 2017;102(12):4343–4410.
  • Leon BM, Maddox TM. Diabetes and cardiovascular disease: epidemiology, biological mechanisms, treatment recommendations and future research. World J Diabetes. 2015;6(13):1246–1258.
  • Pechlivani N, Ajjan RA. Thrombosis and vascular inflammation in diabetes: mechanisms and potential therapeutic targets. Front Cardiovasc Med. 2018;5(1):1.
  • Takeshima K, Ariyasu H, Ishibashi T, et al. Myotonic dystrophy type 1 with diabetes mellitus, mixed hypogonadism and adrenal insufficiency. Endocrinol Diabetes Metab Case Rep. 2018;2018:17–0143.
  • Li X, Gao Y, Xu H, et al. Diabetes mellitus is a significant risk factor for the development of liver cirrhosis in chronic hepatitis C patients. Sci Rep. 2017;7(1):9087.
  • Alicic RZ, Rooney MT, Tuttle KR. Diabetic kidney disease: challenges, progress, and possibilities. Clin J Am Soc Nephrol. 2017;12(12):2032–2045.
  • Gheith O, Farouk N, Nampoory N, et al. Diabetic kidney disease: world wide difference of prevalence and risk factors. J Nephropharmacol. 2016;5(1):49–56.
  • Sayin N, Kara N, Pekel G. Ocular complications of diabetes mellitus. World J Diabetes. 2015;6(1):92–108.
  • Roy B. Biomolecular basis of the role of diabetes mellitus in osteoporosis and bone fractures. World J Diabetes. 2013;4(4):101–113.
  • Selvarajah D, Wilkinson ID, Davies J, et al. Central nervous system involvement in diabetic neuropathy. Curr Diab Rep. 2011;11(4):310–322.
  • Pizzino G, Irrera N, Cucinotta M, et al. Oxidative stress: harms and benefits for human health. Oxid Med Cell Longev. 2017;2017:8416763.
  • Tangvarasittichai S. Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. 2015;6(3):456–480.
  • Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res. 2010;107(9):1058–1070.
  • Jaganjac M, Tirosh O, Cohen G, et al. Reactive aldehydes-second messengers of free radicals in diabetes mellitus. Free Radic Res. 2013;47(Suppl 1):39–48.
  • Pradeep AR, Agarwal E, Bajaj P, et al. 4-Hydroxy-2-nonenal, an oxidative stress marker in crevicular fluid and serum in type 2 diabetes with chronic periodontitis. Contemp Clin Dent. 2013;4(3):281–285.
  • Zhao Y, Song W, Wang Z, et al. Resveratrol attenuates testicular apoptosis in type 1 diabetic mice: role of Akt-mediated Nrf2 activation and p62-dependent Keap1 degradation. Redox Biol. 2018;14:609–617.
  • Knaś M, Maciejczyk M, Daniszewska I, et al. Oxidative damage to the salivary glands of rats with streptozotocin-induced diabetes-temporal study: oxidative stress and diabetic salivary glands. J Diabetes Res. 2016;2016:4583742.
  • Toyokuni S, Yamada S, Kashima M, et al. Serum 4-hydroxy-2-nonenal-modified albumin is elevated in patients with type 2 diabetes mellitus. Antioxid Redox Signal. 2000;2(4):681–685.
  • Calabrese V, Mancuso C, Sapienza M, et al. Oxidative stress and cellular stress response in diabetic nephropathy. Cell Stress Chaper. 2007;12(4):299–306.
  • Jaganjac M, Almuraikhy S, Al-Khelaifi F, et al. Combined metformin and insulin treatment reverses metabolically impaired omental adipogenesis and accumulation of 4-hydroxynonenal in obese diabetic patients. Redox Biol. 2017;12:483–490.
  • Miao X, Wang Y, Sun J, et al. Zinc protects against diabetes-induced pathogenic changes in the aorta: roles of metallothionein and nuclear factor (erythroid-derived 2)-like 2. Cardiovasc Diabetol. 2013;12:54.
  • Shvedova AA, Kisin ER, Yanamala N, et al. Gender differences in murine pulmonary responses elicited by cellulose nanocrystals. Part Fibre Toxicol. 2016;13(1):28.
  • Gomez-Perez Y, Amengual-Cladera E, Catala-Niell A, et al. Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats. Cell Physiol Biochem. 2008;22(5–6):539–548.
  • Bloomer SA, Wellen KE, Henderson GC. Sexual dimorphism in the hepatic protein response to a moderate trans fat diet in senescence-accelerated mice. Lipids Health Dis. 2017;16(1):243.
  • Ihara Y, Toyokuni S, Uchida K, et al. Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes. 1999;48(4):927–932.
  • Altura BM, Carella A, Gebrewold A, et al. Why there is an increased risk of cardiac failure, widening of pulse pressure and hemorrhagic stroke in type 2 diabetics over age 60: roles of unrecognized hypomagnesemia and epigenetics coupled with increased levels of ceramides, cytokines, ROS, 4-HNE and platelet activating factor. J Clin Case Stud. 2020;5(2):10.
  • Zhao MX, Zhou B, Ling L, et al. Salusin-β contributes to oxidative stress and inflammation in diabetic cardiomyopathy. Cell Death Dis. 2017;8(3):e2690.
  • Liu M, Verma N, Peng X, et al. Hyperamylinemia increases IL-1β synthesis in the heart via peroxidative sarcolemmal injury. Diabetes. 2016;65(9):2772–2783.
  • Csala M, Kardon T, Legeza B, et al. On the role of 4-hydroxynonenal in health and disease. Biochim Biophys Acta. 2015;1852(5):826–838.
  • Mali VR, Ning R, Chen J, et al. Impairment of aldehyde dehydrogenase-2 by 4-hydroxy-2-nonenal adduct formation and cardiomyocyte hypertrophy in mice fed a high-fat diet and injected with low-dose streptozotocin. Exp Biol Med (Maywood). 2014;239(5):610–618.
  • Deshpande M, Mali VR, Pan G, et al. Increased 4-hydroxy-2-nonenal-induced proteasome dysfunction is correlated with cardiac damage in streptozotocin-injected rats with isoproterenol infusion. Cell Biochem Funct. 2016;34(5):334–342.
  • Mali VR, Pan G, Deshpande M, et al. Cardiac mitochondrial respiratory dysfunction and tissue damage in chronic hyperglycemia correlate with reduced aldehyde dehydrogenase-2 activity. PLoS One. 2016;11(10):e0163158.
  • Pan G, Deshpande M, Pang H, et al. Precision medicine approach: empagliflozin for diabetic cardiomyopathy in mice with aldehyde dehydrogenase (ALDH) 2*2 mutation, a specific genetic mutation in millions of East Asians. Eur J Pharmacol. 2018;839:76–81.
  • Obrosova IG, Drel VR, Pacher P, et al. Oxidative-nitrosative stress and poly(ADP-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: the relation is revisited. Diabetes. 2005;54(12):3435–3441.
  • Akude E, Zherebitskaya E, Roy Chowdhury SK, et al. 4-Hydroxy-2-nonenal induces mitochondrial dysfunction and aberrant axonal outgrowth in adult sensory neurons that mimics features of diabetic neuropathy. Neurotox Res. 2010;17(1):28–38.
  • Zhang C, Lu X, Tan Y, et al. Diabetes-induced hepatic pathogenic damage, inflammation, oxidative stress, and insulin resistance was exacerbated in zinc deficient mouse model. PLoS One. 2012;7(12):e49257.
  • Barman S, Srinivasan K. Attenuation of oxidative stress and cardioprotective effects of zinc supplementation in experimental diabetic rats. Br J Nutr. 2017;117(3):335–350.
  • Bacevic M, Brkovic B, Albert A, et al. Does oxidative stress play a role in altered characteristics of diabetic bone? A systematic review. Calcif Tissue Int. 2017;101(6):553–563.
  • Li X, Sun X, Zhang X, et al. Enhanced oxidative damage and Nrf2 downregulation contribute to the aggravation of periodontitis by diabetes mellitus. Oxid Med Cell Longev. 2018;2018:1–11.
  • Kubota K, Nakano M, Kobayashi E, et al. An enriched environment prevents diabetes-induced cognitive impairment in rats by enhancing exosomal miR-146a secretion from endogenous bone marrow-derived mesenchymal stem cells. PLoS One. 2018;13(9):e0204252.
  • Wyatt LH, Ferrance RJ. The musculoskeletal effects of diabetes mellitus. J Can Chiropr Assoc. 2006;50(1):43–50.
  • Ingram KH, Hill H, Moellering DR, et al. Skeletal muscle lipid peroxidation and insulin resistance in humans. J Clin Endocrinol Metab. 2012;97(7):E1182–E1186.
  • Aragno M, Mastrocola R, Catalano MG, et al. Oxidative stress impairs skeletal muscle repair in diabetic rats. Diabetes. 2004;53(4):1082–1088.
  • Ali TK, Matragoon S, Pillai BA, et al. Peroxynitrite mediates retinal neurodegeneration by inhibiting nerve growth factor survival signaling in experimental and human diabetes. Diabetes. 2008;57(4):889–898.
  • Shu XS, Zhu H, Huang X, et al. Loss of beta-catenin via activated GSK3beta causes diabetic retinal neurodegeneration by instigating a vicious cycle of oxidative stress-driven mitochondrial impairment. Aging (Albany NY) 2020;12(13):13437–13462.
  • Al-Maskari AY, Al-Maskari MY, Al-Sudairy S. Oral manifestations and complications of diabetes mellitus: a review. Sultan Qaboos Univ Med J. 2011;11(2):179–186.
  • Korytar P, Sivonova M, Maruniakova A, et al. Influence of 2,5-dihydroxybenzylidene aminoguanidine on lipid oxidative damage and on antioxidant levels in model diabetes mellitus. Pharmazie. 2003;58(10):733–737.
  • Chevolleau S, Noguer-Meireles MH, Jouanin I, et al. Development and validation of an ultra high performance liquid chromatography-electrospray tandem mass spectrometry method using selective derivatisation, for the quantification of two reactive aldehydes produced by lipid peroxidation, HNE (4-hydroxy-2(E)-nonenal) and HHE (4-hydroxy-2(E)-hexenal) in faecal water. J Chromatogr B Anal Technol Biomed Life Sci. 2018;1083:171–179.
  • Chung FL, Nath RG, Ocando J, et al. Deoxyguanosine adducts of t-4-hydroxy-2-nonenal are endogenous DNA lesions in rodents and humans: detection and potential sources. Cancer Res. 2000;60(6):1507–1511.
  • Grimsrud PA, Picklo MJ, Sr., Griffin TJ, et al. Carbonylation of adipose proteins in obesity and insulin resistance: identification of adipocyte fatty acid-binding protein as a cellular target of 4-hydroxynonenal. Mol Cell Proteomics. 2007;6(4):624–637.
  • Zelzer S, Mangge H, Oberreither R, et al. Oxidative stress: determination of 4-hydroxy-2-nonenal by gas chromatography/mass spectrometry in human and rat plasma. Free Radic Res. 2015;49(10):1233–1238.
  • Asselin C, Bouchard B, Tardif JC, et al. Circulating 4-hydroxynonenal-protein thioether adducts assessed by gas chromatography-mass spectrometry are increased with disease progression and aging in spontaneously hypertensive rats. Free Radic Biol Med. 2006;41(1):97–105.
  • Kim Y, Kim D, Hwang J, et al. Determination of 4-hydroxynonenal in rat plasma by gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom. 2002;16(12):1238–1242.
  • Orioli M, Aldini G, Benfatto MC, et al. HNE Michael adducts to histidine and histidine-containing peptides as biomarkers of lipid-derived carbonyl stress in urines: LC-MS/MS profiling in Zucker obese rats. Anal Chem. 2007;79(23):9174–9184.
  • Warnke MM, Wanigasekara E, Singhal SS, et al. The determination of glutathione-4-hydroxynonenal (GSHNE), E-4-hydroxynonenal (HNE), and E-1-hydroxynon-2-en-4-one (HNO) in mouse liver tissue by LC-ESI-MS. Anal Bioanal Chem. 2008;392(7–8):1325–1333.
  • Weber D, Milkovic L, Bennett SJ, et al. Measurement of HNE-protein adducts in human plasma and serum by ELISA-Comparison of two primary antibodies. Redox Biol. 2013;1:226–233.
  • Xiao TL, Shoeb M, Ansari NH. Metabolism and detoxification of the lipid derived aldehyde, 4-Hydroxynonenal in diabetic cataractogenesis in rat. Zhonghua Yan Ke Za Zhi. 2009;45(3):248–253.
  • Carini M, Aldini G, Facino RM. Mass spectrometry for detection of 4-hydroxy-trans-2-nonenal (HNE) adducts with peptides and proteins. Mass Spectrom Rev. 2004;23(4):281–305.
  • Isom AL, Barnes S, Wilson L, et al. Modification of cytochrome c by 4-hydroxy- 2-nonenal: evidence for histidine, lysine, and arginine-aldehyde adducts. J Am Soc Mass Spectrom. 2004;15(8):1136–1147.
  • Valle A, Catalan V, Rodriguez A, et al. Identification of liver proteins altered by type 2 diabetes mellitus in obese subjects. Liver Int. 2012;32(6):951–961.
  • Siddiqui MA, Kashyap M, Khanna V, et al. Metabolism of 4-hydroxy trans 2-nonenal (HNE) in cultured pc-12 cells. ANS. 2008;15(3):60–68.
  • Pan G, Deshpande M, Pang H, et al. 4-Hydroxy-2-nonenal attenuates 8-oxoguanine DNA glycosylase 1 activity. J Cell Biochem. 2020;121(12):4887–4897.
  • Spickett CM. The lipid peroxidation product 4-hydroxy-2-nonenal: advances in chemistry and analysis. Redox Biol. 2013;1:145–152.
  • Sima A, Stancu C, Starodub O, et al. Immunodetection of modified lipoproteins in plasma and arterial walls of patients with coronary heart disease. Rom J Intern Med. 1997;35(1–4):29–38.
  • Nanto H, Yokoi Y, Mukai T, et al. Novel gas sensor using polymer-film-coated quartz resonator for environmental monitoring. Mater Sci Eng C. 2000;12(1–2):43–48.
  • Yang P, Lau C, Liang JY, et al. Zeolite-based cataluminescence sensor for the selective detection of acetaldehyde. Luminescence. 2007;22(5):473–479.
  • Xiaoan Cao ZZ, Zhang X. A novel gaseous acetaldehyde sensor utilizing cataluminescence on nanosized BaCO3. Sens Actuators B. 2004;99(1):6.
  • Bicanic D, Persijn S, Taylor A, et al. Detection of ethanol and acetaldehyde released from cabbage seeds of different quality: laser photoacoustic spectroscopy versus FTIR and headspace gas chromatography. Rev Sci Instrum. 2003;74(1):4.
  • Ohata HO, Otsuka M, Ohmori S. Determination of acetaldehyde in biological samples by gas chromatography with electron-capture detection. J Chromatogr B Biomed Sci Appl. 1997;693(2):9.
  • Li Z, Jacobus LK, Wuelfing WP, et al. Detection and quantification of low-molecular-weight aldehydes in pharmaceutical excipients by headspace gas chromatography. J Chromatogr A. 2006;1104(1–2):1–10.
  • Jacquinot Pweh A, Hauser C, Müller P, et al. Amperometric detection of gaseous ethanol and acetaldehyde at low concentrations on an Au–Nafion electrode. Analyst. 1999;124(6):7.
  • Avramescu AN, Noguer T, Avramescu M, et al. Screen-printed biosensors for the control of wine quality based on lactate and acetaldehyde determination. Anal Chim Acta. 2002;458(1):11.
  • Mitsubayashi KM, Matsunaga H, Nishio G, et al. Bio-sniffer sticks for breath analysis after drinking. Sens Actuators B Chem. 2005;108(1):5.
  • Titoiu AM, Lapauw M, Necula-Petrareanu G, et al. Carbon nanofiber and meldola blue based electrochemical sensor for NADH: application to the detection of benzaldehyde. Electroanalysis. 2018;30(11):2676–2688.
  • Enache TA, Matei E, Diculescu VC. Electrochemical sensor for carbonyl groups in oxidized proteins. Anal Chem. 2019;91(3):1920–1927.
  • Shereema RM, Nambiar SR, Shankar SS, et al. CeO2–MWCNT nanocomposite based electrochemical sensor for acetaldehyde. Anal Methods. 2015;7(12):7.
  • Toniolo R, Dossi N, Bortolomeazzi R, et al. Volatile aldehydes sensing in headspace using a room temperature ionic liquid-modified electrochemical microprobe. Talanta. 2019;197:522–529.
  • Zhang YZ, Cai M, Chen Z, et al. A novel electrochemical sensor for formaldehyde based on palladium nanowire arrays electrode in alkaline media. Electrochim Acta. 2012;68(6):172–177.
  • Safavi AM, Maleki N, Farjami F, et al. Electrocatalytic oxidation of formaldehyde on palladium nanoparticles electrodeposited on carbon ionic liquid composite electrode. J Electroanal Chem. 2009;626(1):5.
  • Raoof J-BH, Ojani R, Aghajani S. Fabrication of bimetallic Cu/Pd particles modified carbon nanotube paste electrode and its use towards formaldehyde electrooxidation. J Mol Liq. 2015;204(6):106–111.
  • Yan R-W, Jin B-K. Study of the electrochemical oxidation mechanism of formaldehyde on gold electrode in alkaline solution. Chin Chem Lett. 2013;24(2):159–162.
  • Chi X, Tang Y, Zeng X. Electrode reactions coupled with chemical reactions of oxygen, water and acetaldehyde in an ionic liquid: new approaches for sensing volatile organic compounds. Electrochim Acta. 2016;216:171–180.
  • Reinheckel T, Noack H, Lorenz S, et al. Comparison of protein oxidation and aldehyde formation during oxidative stress in isolated mitochondria. Free Radic Res. 1998;29(4):297–305.
  • Kinter M. Analytical technologies for lipid oxidation products analysis. J Chromatogr B Biomed Sci Appl. 1995;671(1):14.
  • Esterbauer HS, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med. 1991;11(1):81–128.
  • Poli DG, Corradi M, Acampa M, et al. Determination of aldehydes in exhaled breath of patients with lung cancer by means of on-fiber-derivatisation SPME–GC/MS. J Chromatogr B. 2010;878(27):2643–2651.
  • Obermeier J, Trefz P, Wex K, et al. Electrochemical sensor system for breath analysis of aldehydes, CO and NO. J Breath Res. 2015;9(1):016008.
  • Leung LWH, Weaver MJ. Influence of adsorbed carbon monoxide on electrocatalytic oxidation of simple organic molecules at platinum and palladium electrodes in acidic solution: a survey using real-time FTIR spectroscopy. Langmuir. 1990;6(2):323–333.
  • Liu N, Xu Z, Morrin A, et al. Low fouling strategies for electrochemical biosensors targeting disease biomarkers. Anal Methods. 2019;11(6):702–711.
  • Hanssen BL, Siraj S, Wong DKY. Recent strategies to minimise fouling in electrochemical detection systems. Rev Anal Chem. 2016;35(1):1–28.
  • Peng H, Yu Q, Wang S, et al. Molecular design strategies for electrochemical behavior of aromatic carbonyl compounds in organic and aqueous electrolytes. Adv Sci (Weinh). 2019;6(17):1900431.
  • Bondue CJ, Koper MTM. Electrochemical reduction of the carbonyl functional group: the importance of adsorption geometry, molecular structure, and electrode surface structure. J Am Chem Soc. 2019;141(30):12071–12078.
  • Vidal N, Cavaille JP, Graziani F, et al. High throughput assay for evaluation of reactive carbonyl scavenging capacity. Redox Biol. 2014;2:590–598.
  • Ju J, Liu X, Yu JJ, et al. Electrochemistry at bimetallic Pd/Au thin film surfaces for selective detection of reactive oxygen species and reactive nitrogen species. Anal Chem. 2020;92(9):6538–6547.
  • Lyberopoulou A, Efstathopoulos EP, Gazouli M. Nanotechnology-based rapid diagnostic tests. In: Saxena SK, editor. Proof and Concepts in Rapid Diagnostic Tests and Technologies. Rijeka: IntechOpen; 2016. p. 91–105.
  • Augustyniak E, Adam A, Wojdyla K, et al. Validation of protein carbonyl measurement: a multi-centre study. Redox Biol. 2015;4:149–157.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.