Diabetes/Metabolism Research and Reviews

Volume 29, Issue 1 pp. 66-76

Research Article

Advanced glycated albumin isolated from poorly controlled type 1 diabetes mellitus patients alters macrophage gene expression impairing ABCA-1-mediated reverse cholesterol transport

Adriana Machado-Lima,

Adriana Machado-Lima

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Rodrigo T. Iborra,

Rodrigo T. Iborra

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Raphael S. Pinto,

Raphael S. Pinto

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Camila H. Sartori,

Camila H. Sartori

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Erika R. Oliveira,

Erika R. Oliveira

Cellular and Molecular Endocrinology Laboratory (LIM 25), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Edna R. Nakandakare,

Edna R. Nakandakare

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

José T. Stefano,

José T. Stefano

Gastroenterology Laboratory (LIM 7), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Daniel Giannella-Neto,

Daniel Giannella-Neto

Gastroenterology Laboratory (LIM 7), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Maria Lucia C. Corrêa-Giannella,

Maria Lucia C. Corrêa-Giannella

Cellular and Molecular Endocrinology Laboratory (LIM 25), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Marisa Passarelli,

Corresponding Author

Marisa Passarelli

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Marisa Passarelli, Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Av. Dr. Arnaldo 455, Room 3305, CEP 01246-000 Sao Paulo, Brazil.

E-mail: [email protected]

Search for more papers by this author

Adriana Machado-Lima,

Adriana Machado-Lima

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Rodrigo T. Iborra,

Rodrigo T. Iborra

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Raphael S. Pinto,

Raphael S. Pinto

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Camila H. Sartori,

Camila H. Sartori

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Erika R. Oliveira,

Erika R. Oliveira

Cellular and Molecular Endocrinology Laboratory (LIM 25), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Edna R. Nakandakare,

Edna R. Nakandakare

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

José T. Stefano,

José T. Stefano

Gastroenterology Laboratory (LIM 7), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Daniel Giannella-Neto,

Daniel Giannella-Neto

Gastroenterology Laboratory (LIM 7), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Maria Lucia C. Corrêa-Giannella,

Maria Lucia C. Corrêa-Giannella

Cellular and Molecular Endocrinology Laboratory (LIM 25), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Search for more papers by this author

Marisa Passarelli,

Corresponding Author

Marisa Passarelli

Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Sao Paulo, Brazil

Marisa Passarelli, Lipids Laboratory (LIM 10), Faculty of Medical Sciences, University of Sao Paulo, Av. Dr. Arnaldo 455, Room 3305, CEP 01246-000 Sao Paulo, Brazil.

E-mail: [email protected]

Search for more papers by this author

First published: 26 September 2012

https://doi.org/10.1002/dmrr.2362

Citations: 32

Share a link

Email
Wechat
Bluesky

Abstract

Background

We evaluated the effects of albumin isolated from control individuals and from patients with poorly controlled type 1 diabetes mellitus on macrophage gene expression and on reverse cholesterol transport.

Methods

Serum albumin was purified from control subjects (n = 12) and from patients with poorly controlled type 1 diabetes mellitus (n = 13). ¹⁴C-cholesterol-labelled J774 macrophages treated with albumin were employed to measure cholesterol efflux mediated by apo A-I, HDL₃ or HDL₂, the intracellular lipid accumulation and the cellular ABCA-1 protein content. Agilent arrays (44000 probes) were used to analyse gene expression. Several differentially expressed genes were validated by real-time reverse transcription-PCR using TaqMan Two Step RT-PCR.

Results

Levels of glycation-modified and (carboxymethyl)lysine-modified albumin were higher in diabetic patients than in control subjects. Apo A-I-mediated and HDL₂-mediated cellular cholesterol efflux were impaired in macrophages treated with albumin from diabetic patients in comparison with control albumin-treated cells, which was attributed to the reduction in ABCA-1 protein content. Even in the presence of cholesterol acceptors, a higher level of intracellular lipid was observed in macrophages exposed to albumin from diabetic individuals in comparison with the control. The reduction in ABCA-1 content was associated with enhanced expression of stearoyl CoA desaturase 1 and decreased expression of janus kinase 2, which were induced by albumin from patients with type 1 diabetes mellitus.

Conclusions

(Carboxymethyl)lysine-modified albumin isolated from poorly controlled type 1 diabetic patients impairs ABCA-1-mediated reverse cholesterol transport and elicits intracellular lipid accumulation, possibly contributing to atherosclerosis. Copyright © 2012 John Wiley & Sons, Ltd.

References

1 Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications (DCCT/EDIC) Study Research Group, Nathan DM, Cleary PA, et al. Intensive diabetes treatment and cardiovascular disease in patients with type 1 diabetes. N Engl J Med 2005; 353(25): 2643–2653.
10.1056/NEJMoa052187
PubMed Google Scholar
2 Kumeda Y, Inaba M, Shoji S, et al. Significant correlation of glycated albumin, but not glycated haemoglobin, with arterial stiffening in haemodialysis patients with type 2 diabetes. Clin Endocrinol (Oxf) 2008; 69(4): 556–561.
10.1111/j.1365-2265.2008.03202.x
CAS PubMed Web of Science® Google Scholar
3 Peppa M, Raptis SA. Advanced glycation end products and cardiovascular disease. Curr Diabetes Rev 2008; 4(2): 92–100.
10.2174/157339908784220732
CAS PubMed Google Scholar
4 Masumi AI, Otokozawa S, Schaefer EJ, et al. Glycated albumin and direct low density lipoprotein cholesterol levels in type 2 diabetes mellitus. Clin Chim Acta 2009; 406(1-2): 71–74.
10.1016/j.cca.2009.05.015
CAS PubMed Web of Science® Google Scholar
5 Pu LJ, Lu L, Shen WF, et al. Increased serum glycated albumin level is associated with the presence and severity of coronary artery disease in type 2 diabetic patients. Circ J 2007; 71(7): 1067–1073.
10.1253/circj.71.1067
CAS PubMed Google Scholar
6 Ahmed MU, Thorpe SR, Baynes JW. Identification of N epsilon-carboxymethyllysine as a degradation product of fructoselysine in glycated protein. J Biol Chem 1986; 261(11): 4889–4894.
CAS PubMed Web of Science® Google Scholar
7 Vlassara H, Palace MR. Diabetes and advanced glycation endproducts. J Intern Med 2002; 251(2): 87–101.
10.1046/j.1365-2796.2002.00932.x
CAS PubMed Web of Science® Google Scholar
8 Baidoshvili A, Niessen HW, Stooker W, et al. N(omega)-(carboxymethyl)lysine depositions in human aortic heart valves: similarities with atherosclerotic blood vessels. Atherosclerosis 2004; 174(2): 287–292.
10.1016/j.atherosclerosis.2004.02.012
CAS PubMed Web of Science® Google Scholar
9 Yeh CH, Sturgis L, Haidacher J, et al. Requirement for p38 and p44/p42 mitogen-activated protein kinases in RAGE-mediated nuclear factor-kappaB transcriptional activation and cytokine secretion. Diabetes 2001; 50(6): 1495–1504.
10.2337/diabetes.50.6.1495
CAS PubMed Web of Science® Google Scholar
10 Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 2006; 114(6): 597–605.
10.1161/CIRCULATIONAHA.106.621854
CAS PubMed Web of Science® Google Scholar
11 Ywashima Y, Eto M, Hata A, et al. Advanced glycation end products-induced gene expression of scavenger receptors in cultured human monocyte-derived macrophages. Biochem Biophys Res Commun 2000; 277: 368–380.
10.1006/bbrc.2000.3685
CAS PubMed Web of Science® Google Scholar
12 Horiuchi S, Unno Y, Usui H, et al. Pathological roles of advanced glycation end product receptors SR-A and CD36. Ann N Y Acad Sci 2005; 1043: 671–675.
10.1196/annals.1333.076
CAS PubMed Web of Science® Google Scholar
13 Ohkawara E, Nohara Y, Kanno Y, et al. Fructosamine assay using albumin extracted from serum. Biol Pharm Bull 2002; 25(9): 1121–1124.
10.1248/bpb.25.1121
CAS PubMed Web of Science® Google Scholar
14 Basu SK, Goldstein JL, Anderson GW, Brown MS. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc Natl Acad Sci USA 1976; 73(9): 3178–3182.
10.1073/pnas.73.9.3178
CAS PubMed Web of Science® Google Scholar
15 Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265–275.
10.1016/S0021-9258(19)52451-6
CAS PubMed Web of Science® Google Scholar
16 Machado AP, Pinto RS, Moyses ZP, Nakandakare ER, Quintao EC, Passarelli M. Aminoguanidine and metformin prevent the reduced rate of HDL-mediated cell cholesterol efflux induced by formation of advanced glycation end products. Int J Biochem Cell Biol 2006; 38(3): 392–403.
10.1016/j.biocel.2005.09.016
CAS PubMed Web of Science® Google Scholar
17 Bustin SA, Mueller R. Real-time reverse transcription PCR (qRT-PCR) and its potential use in clinical diagnosis. Clin Sci (Lond) 2005; 109(4): 365–379.
10.1042/CS20050086
CAS PubMed Google Scholar
18 Kubista M, Andrade JM, Bengtsson M, et al. The real-time polymerase chain reaction. Mol Aspects Med 2006; 27(2-3): 95–125.
10.1016/j.mam.2005.12.007
CAS PubMed Google Scholar
19 Terpstra AH, Nicolosi RJ, Herbert PN. In vitro incorporation of radiolabeled cholesteryl esters into high and low density lipoproteins. J Lipid Res 1989; 30(11): 1663–1671.
CAS PubMed Web of Science® Google Scholar
20 Chiang KH, Huang PH, Huang SS, Wu TC, Chen JW, Lin SJ. Plasma levels of soluble receptor for advanced glycation end products are associated with endothelial function and predict cardiovascular events in nondiabetic patients. Coron Artery Dis 2009; 20(4): 267–273.
10.1097/MCA.0b013e32832c459c
PubMed Web of Science® Google Scholar
21 Baumann M, Richart T, Sollinger D, et al. Association between carotid diameter and the advanced glycation endproduct N-epsilon-carboxymethyllysine (CML). Cardiovasc Diabetol 2009; 8: 45.
10.1186/1475-2840-8-45
CAS PubMed Web of Science® Google Scholar
22 Wang X, Collins HL, Ranalletta M, et al. Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J Clin Invest 2007; 117(8): 2216–2224.
10.1172/JCI32057
CAS PubMed Web of Science® Google Scholar
23 Tarr PT, Tarling EJ, Bojanic DD, Edwards PA, Baldán A. Emerging new paradigms for ABCG transporters. Biochim Biophys Acta 2009; 1791(7): 584–593.
10.1016/j.bbalip.2009.01.007
CAS PubMed Web of Science® Google Scholar
24 Serfaty-Lacrosniere C, Civeira F, Lanzberg A, et al. Homozygous Tangier disease and cardiovascular disease. Atherosclerosis 1994; 107: 85–98.
10.1016/0021-9150(94)90144-9
CAS PubMed Web of Science® Google Scholar
25 Passarelli M, Tang C, Mcdonald TO, et al. Advanced glycation end product precursors impair ABCA1-dependent cholesterol removal from cells. Diabetes 2005; 54(7): 2198–2205.
10.2337/diabetes.54.7.2198
CAS PubMed Web of Science® Google Scholar
26 de Souza Pinto R, Castilho G, Paim BA, et al. Inhibition of macrophage oxidative stress prevents the reduction of ABCA-1 transporter induced by advanced glycated albumin. Lipids 2012; 47(5): 443–450.
10.1007/s11745-011-3647-9
CAS PubMed Web of Science® Google Scholar
27 Castilho G, Okuda LS, Pinto RS, et al. ER stress is associated with reduced ABCA-1 protein levels in macrophages treated with advanced glycated albumin – reversal by a chemical chaperone. Int J Biochem Cell Biol 2012; 44(7): 1078–1086.
10.1016/j.biocel.2012.03.016
CAS PubMed Web of Science® Google Scholar
28 Iborra RT, Machado-Lima A, Castilho G, et al. Advanced glycation in macrophages induces intracellular accumulation of 7-ketocholesterol and total sterols by decreasing the expression of ABCA-1 and ABCG-1. Lipids Health Dis 2011; 29(10): 172.
10.1186/1476-511X-10-172
CAS Web of Science® Google Scholar
29 Sun Y, Hao M, Luo Y, et al. Stearoyl-CoA desaturase inhibits ATP-binding cassette transporter A1-mediated cholesterol efflux and modulates membrane domain structure. J Biol Chem 2003; 278(8): 5813–5820.
10.1074/jbc.M208687200
CAS PubMed Web of Science® Google Scholar
30 Wang Y, Kurdi-Haidar B, Oram JF. LXR-mediated activation of macrophage stearoyl-CoA desaturase generates unsaturated fatty acids that destabilize ABCA1. J Lipid Res 2004; 45(5): 972–980.
10.1194/jlr.M400011-JLR200
CAS PubMed Web of Science® Google Scholar
31 Tang C, Vaughan AM, Oram JF. Janus kinase 2 modulates the apolipoprotein interactions with ABCA1 required for removing cellular cholesterol. J Biol Chem 2004; 279(9): 7622–7628.
10.1074/jbc.M312571200
CAS PubMed Web of Science® Google Scholar
32 Passarelli M, Catanozi S, Nakandakare ER, et al. Plasma lipoproteins from patients with poorly controlled diabetes mellitus and “in vitro” glycation of lipoproteins enhance the transfer rate of cholesteryl ester from HDL to apo-B-containing lipoproteins. Diabetologia 1997; 40(9): 1085–1093.
10.1007/s001250050791
CAS PubMed Web of Science® Google Scholar
33 Ohgami N, Nagai R, Miyazaki A, et al. Scavenger receptor class B type I-mediated reverse cholesterol transport is inhibited by advanced glycation end products. J Biol Chem 2001; 276: 13348–13355.
10.1074/jbc.M011613200
CAS PubMed Web of Science® Google Scholar
34 Sayre LM, Sha W, Xu G, et al. Immunochemical evidence supporting 2-pentylpyrrole formation on proteins exposed to 4-hydroxy-2-nonenal. Chem Res Toxicol 1996; 9(7): 1194–1201.
10.1021/tx960094j
CAS PubMed Web of Science® Google Scholar
35 Xu G, Liu Y, Kansal MM, Sayre LM. Rapid cross-linking of proteins by 4-ketoaldehydes and 4-hydroxy-2-alkenals does not arise from the lysine-derived monoalkylpyrroles. Chem Res Toxicol 1999; 12(9): 855–861.
10.1021/tx990056a
CAS PubMed Web of Science® Google Scholar
36 Morris MA, Preddy L. Glycosylation accelerates albumin degradation in normal and diabetic dogs. Biochem Med Metab Biol 1986; 35(3): 267–270.
10.1016/0885-4505(86)90082-4
CAS PubMed Web of Science® Google Scholar
37 Layton GJ, Jerums G. Effect of glycation of albumin on its renal clearance in normal and diabetic rats. Kidney Int 1988; 33(3): 673–676.
10.1038/ki.1988.52
CAS PubMed Web of Science® Google Scholar
38 Kallner A. Elimination of ¹⁴C-glycated albumin from serum of rabbit. Scand J Clin Lab Invest 1990; 50(7): 763–768.
10.3109/00365519009091070
CAS PubMed Web of Science® Google Scholar
39 Nerlich AG, Schleicher ED. N(epsilon)-(carboxymethyl)lysine in atherosclerotic vascular lesions as a marker for local oxidative stress. Atherosclerosis 1999; 144(1): 41–47.
10.1016/S0021-9150(99)00038-6
CAS PubMed Web of Science® Google Scholar

Citing Literature

Volume29, Issue1

January 2013

Pages 66-76

Advanced glycated albumin isolated from poorly controlled type 1 diabetes mellitus patients alters macrophage gene expression impairing ABCA-1-mediated reverse cholesterol transport

Abstract

Background

Methods

Results

Conclusions

References

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Advanced glycated albumin isolated from poorly controlled type 1 diabetes mellitus patients alters macrophage gene expression impairing ABCA-1-mediated reverse cholesterol transport

Abstract

Background

Methods

Results

Conclusions

References

Citing Literature

References

Related

Information