Abstract
We have previously shown that increased nonenzymatic glycosylation occurs in peripheral nervous tissue of diabetic humans and animals, primarily on the PO-protein of peripheral nerve myelin. The pathophysiologic mechanism by which this biochemical alteration leads to myelin breakdown and removal is not as yet understood. In the present study we show that advanced glycosylation end-product (AGE) adducts that form during long-term exposure of peripheral nerve myelin proteins to glucose in vitro and in vivo markedly alter the way in which myelin interacts with elicited macrophages. In this interaction, macrophages appear to specifically recognize AGEs on myelin, since AGE-BSA competes nearly as effectively as AGE-myelin, while neither unmodified BSA nor unmodified myelin compete. The failure of yeast mannan to interfere with macrophage recognition of AGE-myelin suggests that the mannose/fucose receptor does not mediate this process. Recognition of AGE-protein by macrophages is associated with endocytosis, as demonstrated by resistance of cell-associated radioactivity to removal by trypsin action, and by low temperature inhibition of ligand accumulation in the cellular fraction. 125I-labeled myelin that had been incubated in vitro with 50 mM glucose for 8 wk reached a steady state accumulation within thioglycolate-elicited macrophages that was five times greater than that of myelin incubated without glucose. Similarly, myelin isolated from rats having diabetes for 1.5-2.0 years duration had a steady state level that was 9 times greater than that of myelin from young rats, and 3.5 times greater than that of myelin from age-matched controls. In contrast, myelin isolated from rats having diabetes for 4-5 wk had the same degree of accumulation observed with myelin of age-matched normal rats. These data suggest that the amount of increased nonenzymatic glycosylation observed in the myelin of short-term diabetic rats had not yet resulted in the significant accumulation of AGE-myelin present both in vitro and in the long-term diabetic rats. The disappearance of acid-insoluble radioactivity from within the cells and the appearance of acid-soluble radioactivity released into the medium were very similar for the two groups, suggesting that the striking difference in accumulation seen between normal myelin and AGE-myelin is due primarily to increased uptake. Formation of irreversible AGE-adducts on myelin appears to promote the recognition and uptake of the modified myelin by macrophages. This interaction between AGE-myelin and macrophages may initiate or contribute to the segmental demyelination associated with diabetes and the normal aging of peripheral nerve.
MeSH Terms
Aging
Animals
Diabetes Mellitus, Experimental/metabolism,physiopathology
Diabetic Neuropathies/metabolism,physiopathology
Female
Glucose/pharmacology
In Vitro Techniques
Kinetics
Macrophage Activation
Macrophages/metabolism
Mice
Mice, Inbred Strains
Myelin Proteins/metabolism
Rats
Rats, Inbred Strains
Chemicals
Myelin Proteins
Glucose
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Vlassara H
Brownlee M
Cerami A
References (24)
24 references, click to expand
-
Metabolism of peripheral nerve myelin in experimental diabetes.
J Clin Invest. 1975 May;55(5):1049-56
PMID: 123535
-
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem. 1976 May 7;72:248-54
PMID: 942051
-
Structure of carbohydrate of hemoglobin AIc.
J Biol Chem. 1977 May 10;252(9):2992-7
PMID: 853040
-
Nonenzymatic glycosylation of hemoglobin.
J Biol Chem. 1977 May 10;252(9):2998-3002
PMID: 856810
-
Protein and cell membrane iodinations with a sparingly soluble chloroamide, 1,3,4,6-tetrachloro-3a,6a-diphrenylglycoluril.
Biochem Biophys Res Commun. 1978 Feb 28;80(4):849-57
PMID: 637870
-
Degradation of basic protein in myelin by neutral proteases secreted by stimulated macrophages: a possible mechanism of inflammatory demyelination.
Proc Natl Acad Sci U S A. 1978 Mar;75(3):1554-8
PMID: 148651
-
Activation of mononuclear phagocytes: fact, fancy, and future.
J Immunol. 1978 Sep;121(3):813-6
PMID: 357655
-
Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition.
Proc Natl Acad Sci U S A. 1979 Jan;76(1):333-7
PMID: 218198
-
Nonenzymatic glucosylation of rat albumin. Studies in vitro and in vivo.
J Biol Chem. 1979 Oct 10;254(19):9394-400
PMID: 489542
-
Malondialdehyde alteration of low density lipoproteins leads to cholesteryl ester accumulation in human monocyte-macrophages.
Proc Natl Acad Sci U S A. 1980 Apr;77(4):2214-8
PMID: 6769124
-
Measurement of glycosylated amino acids and peptides from urine of diabetic patients using affinity chromatography.
Diabetes. 1980 Dec;29(12):1044-7
PMID: 6777222
-
The scavenger cell pathway for lipoprotein degradation: specificity of the binding site that mediates the uptake of negatively-charged LDL by macrophages.
J Supramol Struct. 1980;13(1):67-81
PMID: 6255257
-
Nonenzymatic browning in vivo: possible process for aging of long-lived proteins.
Science. 1981 Jan 30;211(4481):491-3
PMID: 6779377
-
The metabolism of native and malondialdehyde-altered low density lipoproteins by human monocyte-macrophages.
J Lipid Res. 1981 Jan;22(1):63-71
PMID: 6260883
-
Degradation of the P0, P1, and Pr proteins in peripheral nervous system myelin by plasmin: implications regarding the role of macrophages in demyelinating diseases.
J Neurochem. 1981 Apr;36(4):1506-14
PMID: 6167674
-
The biochemistry of the complications of diabetes mellitus.
Annu Rev Biochem. 1981;50:385-432
PMID: 6168237
-
Nonenzymatic glycosylation of human hemoglobin at multiple sites.
Metabolism. 1979 Apr;28(4 Suppl 1):427-30
PMID: 122295
-
Nonenzymatic glycosylation of peripheral nerve protein in diabetes mellitus.
Proc Natl Acad Sci U S A. 1981 Aug;78(8):5190-2
PMID: 6946466
-
Specificity of receptor-mediated recognition of malondialdehyde-modified low density lipoproteins.
Proc Natl Acad Sci U S A. 1982 Mar;79(6):1712-6
PMID: 6281781
-
Complement activation by isolated myelin: activation of the classical pathway in the absence of myelin-specific antibodies.
Proc Natl Acad Sci U S A. 1982 May;79(10):3290-4
PMID: 6954480
-
Receptors for maleylated proteins regulate secretion of neutral proteases by murine macrophages.
Science. 1982 Nov 5;218(4572):574-6
PMID: 6289443
-
Nonenzymatic glucosylation of low-density lipoprotein alters its biologic activity.
Diabetes. 1982 Apr;31(4 Pt 1):283-91
PMID: 6818075
-
Excessive nonenzymatic glycosylation of peripheral and central nervous system myelin components in diabetic rats.
Diabetes. 1983 Jul;32(7):670-4
PMID: 6862112
-
Covalent attachment of soluble proteins by nonenzymatically glycosylated collagen. Role in the in situ formation of immune complexes.
J Exp Med. 1983 Nov 1;158(5):1739-44
PMID: 6415211