Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion

Kristin L. Reigle, Gloria Di Lullo, Kevin Turner, Jerold A. Last, Inna Chervoneva, David E. Birk, James L. Funderburgh, Elizabeth Elrod, Markus W. Germann, Charles Surber, Ralph D. Sanderson, James D San Antonio

Research output: Contribution to journalArticle

32 Citations (Scopus)

Abstract

Non-enzymatic glycation of type I collagen occurs in aging and diabetes, and may affect collagen solubility, charge, polymerization, and intermolecular interactions. Proteoglycans1 (PGs) bind type I collagen and are proposed to regulate fibril assembly, function, and cell-collagen interactions. Moreover, on the collagen fibril a keratan sulfate (KS) PG binding region overlaps with preferred collagen glycation sites. Thus, we examined the effect of collagen modified by simple glycation on PG-collagen interactions. By affinity coelectrophoresis (ACE), we found reduced affinities of heparin and KSPGs for glycated but not normal collagen, whereas the dermatan sulfate (DS)PGs decorin and biglycan bound similarly to both, and that the affinity of heparin for normal collagen decreased with increasing pH. Circular dichroism (CD) spectroscopy revealed normal and glycated collagens to assume triple helical conformations, but heparin addition caused precipitation and decreased triple helical content - effects that were more marked with glycated collagen. A spectrophotometric assay revealed slower polymerization of glycated collagen. However, ultrastructural analyses indicated that fibrils assembled from normal and glycated collagen exhibited normal periodicity, and had similar structures and comparable diameter distributions. B-cells expressing the cell surface heparan sulfate PG syndecan-1 adhered well to normal but not glycated collagen, and endothelial cell migration was delayed on glycated collagen. We speculate that glycation diminishes the electrostatic interactions between type I collagen and PGs, and may interfere with core protein-collagen associations for KSPGs but not DSPGs. Therefore in vivo, collagen glycation may weaken PG-collagen interactions, thereby disrupting matrix integrity and cell-collagen interactions, adhesion, and migration.

Original languageEnglish (US)
Pages (from-to)1684-1698
Number of pages15
JournalJournal of Cellular Biochemistry
Volume104
Issue number5
DOIs
StatePublished - Aug 1 2008
Externally publishedYes

Fingerprint

Cell adhesion
Proteoglycans
Collagen Type I
Cell Adhesion
Collagen
Heparin
Cell Communication
Polymerization
Syndecan-1
Biglycan
Decorin
Keratan Sulfate
Circular dichroism spectroscopy
Dermatan Sulfate
Heparitin Sulfate
Endothelial cells
Periodicity
Medical problems
Circular Dichroism
Coulomb interactions

Keywords

  • Aging
  • Diabetes
  • Endothelial cells
  • Extracellular matrix
  • Glycation
  • Proteoglycan
  • Type I collagen

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology

Cite this

Reigle, K. L., Di Lullo, G., Turner, K., Last, J. A., Chervoneva, I., Birk, D. E., ... Antonio, J. D. S. (2008). Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion. Journal of Cellular Biochemistry, 104(5), 1684-1698. https://doi.org/10.1002/jcb.21735

Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion. / Reigle, Kristin L.; Di Lullo, Gloria; Turner, Kevin; Last, Jerold A.; Chervoneva, Inna; Birk, David E.; Funderburgh, James L.; Elrod, Elizabeth; Germann, Markus W.; Surber, Charles; Sanderson, Ralph D.; Antonio, James D San.

In: Journal of Cellular Biochemistry, Vol. 104, No. 5, 01.08.2008, p. 1684-1698.

Research output: Contribution to journalArticle

Reigle, KL, Di Lullo, G, Turner, K, Last, JA, Chervoneva, I, Birk, DE, Funderburgh, JL, Elrod, E, Germann, MW, Surber, C, Sanderson, RD & Antonio, JDS 2008, 'Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion', Journal of Cellular Biochemistry, vol. 104, no. 5, pp. 1684-1698. https://doi.org/10.1002/jcb.21735
Reigle, Kristin L. ; Di Lullo, Gloria ; Turner, Kevin ; Last, Jerold A. ; Chervoneva, Inna ; Birk, David E. ; Funderburgh, James L. ; Elrod, Elizabeth ; Germann, Markus W. ; Surber, Charles ; Sanderson, Ralph D. ; Antonio, James D San. / Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion. In: Journal of Cellular Biochemistry. 2008 ; Vol. 104, No. 5. pp. 1684-1698.
@article{5c621e7755bd454581b90fd97dd91114,
title = "Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion",
abstract = "Non-enzymatic glycation of type I collagen occurs in aging and diabetes, and may affect collagen solubility, charge, polymerization, and intermolecular interactions. Proteoglycans1 (PGs) bind type I collagen and are proposed to regulate fibril assembly, function, and cell-collagen interactions. Moreover, on the collagen fibril a keratan sulfate (KS) PG binding region overlaps with preferred collagen glycation sites. Thus, we examined the effect of collagen modified by simple glycation on PG-collagen interactions. By affinity coelectrophoresis (ACE), we found reduced affinities of heparin and KSPGs for glycated but not normal collagen, whereas the dermatan sulfate (DS)PGs decorin and biglycan bound similarly to both, and that the affinity of heparin for normal collagen decreased with increasing pH. Circular dichroism (CD) spectroscopy revealed normal and glycated collagens to assume triple helical conformations, but heparin addition caused precipitation and decreased triple helical content - effects that were more marked with glycated collagen. A spectrophotometric assay revealed slower polymerization of glycated collagen. However, ultrastructural analyses indicated that fibrils assembled from normal and glycated collagen exhibited normal periodicity, and had similar structures and comparable diameter distributions. B-cells expressing the cell surface heparan sulfate PG syndecan-1 adhered well to normal but not glycated collagen, and endothelial cell migration was delayed on glycated collagen. We speculate that glycation diminishes the electrostatic interactions between type I collagen and PGs, and may interfere with core protein-collagen associations for KSPGs but not DSPGs. Therefore in vivo, collagen glycation may weaken PG-collagen interactions, thereby disrupting matrix integrity and cell-collagen interactions, adhesion, and migration.",
keywords = "Aging, Diabetes, Endothelial cells, Extracellular matrix, Glycation, Proteoglycan, Type I collagen",
author = "Reigle, {Kristin L.} and {Di Lullo}, Gloria and Kevin Turner and Last, {Jerold A.} and Inna Chervoneva and Birk, {David E.} and Funderburgh, {James L.} and Elizabeth Elrod and Germann, {Markus W.} and Charles Surber and Sanderson, {Ralph D.} and Antonio, {James D San}",
year = "2008",
month = "8",
day = "1",
doi = "10.1002/jcb.21735",
language = "English (US)",
volume = "104",
pages = "1684--1698",
journal = "Journal of Cellular Biochemistry",
issn = "0730-2312",
publisher = "Wiley-Liss Inc.",
number = "5",

}

TY - JOUR

T1 - Non-enzymatic glycation of type I collagen diminishes collagen-proteoglycan binding and weakens cell adhesion

AU - Reigle, Kristin L.

AU - Di Lullo, Gloria

AU - Turner, Kevin

AU - Last, Jerold A.

AU - Chervoneva, Inna

AU - Birk, David E.

AU - Funderburgh, James L.

AU - Elrod, Elizabeth

AU - Germann, Markus W.

AU - Surber, Charles

AU - Sanderson, Ralph D.

AU - Antonio, James D San

PY - 2008/8/1

Y1 - 2008/8/1

N2 - Non-enzymatic glycation of type I collagen occurs in aging and diabetes, and may affect collagen solubility, charge, polymerization, and intermolecular interactions. Proteoglycans1 (PGs) bind type I collagen and are proposed to regulate fibril assembly, function, and cell-collagen interactions. Moreover, on the collagen fibril a keratan sulfate (KS) PG binding region overlaps with preferred collagen glycation sites. Thus, we examined the effect of collagen modified by simple glycation on PG-collagen interactions. By affinity coelectrophoresis (ACE), we found reduced affinities of heparin and KSPGs for glycated but not normal collagen, whereas the dermatan sulfate (DS)PGs decorin and biglycan bound similarly to both, and that the affinity of heparin for normal collagen decreased with increasing pH. Circular dichroism (CD) spectroscopy revealed normal and glycated collagens to assume triple helical conformations, but heparin addition caused precipitation and decreased triple helical content - effects that were more marked with glycated collagen. A spectrophotometric assay revealed slower polymerization of glycated collagen. However, ultrastructural analyses indicated that fibrils assembled from normal and glycated collagen exhibited normal periodicity, and had similar structures and comparable diameter distributions. B-cells expressing the cell surface heparan sulfate PG syndecan-1 adhered well to normal but not glycated collagen, and endothelial cell migration was delayed on glycated collagen. We speculate that glycation diminishes the electrostatic interactions between type I collagen and PGs, and may interfere with core protein-collagen associations for KSPGs but not DSPGs. Therefore in vivo, collagen glycation may weaken PG-collagen interactions, thereby disrupting matrix integrity and cell-collagen interactions, adhesion, and migration.

AB - Non-enzymatic glycation of type I collagen occurs in aging and diabetes, and may affect collagen solubility, charge, polymerization, and intermolecular interactions. Proteoglycans1 (PGs) bind type I collagen and are proposed to regulate fibril assembly, function, and cell-collagen interactions. Moreover, on the collagen fibril a keratan sulfate (KS) PG binding region overlaps with preferred collagen glycation sites. Thus, we examined the effect of collagen modified by simple glycation on PG-collagen interactions. By affinity coelectrophoresis (ACE), we found reduced affinities of heparin and KSPGs for glycated but not normal collagen, whereas the dermatan sulfate (DS)PGs decorin and biglycan bound similarly to both, and that the affinity of heparin for normal collagen decreased with increasing pH. Circular dichroism (CD) spectroscopy revealed normal and glycated collagens to assume triple helical conformations, but heparin addition caused precipitation and decreased triple helical content - effects that were more marked with glycated collagen. A spectrophotometric assay revealed slower polymerization of glycated collagen. However, ultrastructural analyses indicated that fibrils assembled from normal and glycated collagen exhibited normal periodicity, and had similar structures and comparable diameter distributions. B-cells expressing the cell surface heparan sulfate PG syndecan-1 adhered well to normal but not glycated collagen, and endothelial cell migration was delayed on glycated collagen. We speculate that glycation diminishes the electrostatic interactions between type I collagen and PGs, and may interfere with core protein-collagen associations for KSPGs but not DSPGs. Therefore in vivo, collagen glycation may weaken PG-collagen interactions, thereby disrupting matrix integrity and cell-collagen interactions, adhesion, and migration.

KW - Aging

KW - Diabetes

KW - Endothelial cells

KW - Extracellular matrix

KW - Glycation

KW - Proteoglycan

KW - Type I collagen

UR - http://www.scopus.com/inward/record.url?scp=50249101041&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=50249101041&partnerID=8YFLogxK

U2 - 10.1002/jcb.21735

DO - 10.1002/jcb.21735

M3 - Article

C2 - 18348167

AN - SCOPUS:50249101041

VL - 104

SP - 1684

EP - 1698

JO - Journal of Cellular Biochemistry

JF - Journal of Cellular Biochemistry

SN - 0730-2312

IS - 5

ER -