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Cardiovascular Research 2000 47(2):306-313; doi:10.1016/S0008-6363(00)00105-X
© 2000 by European Society of Cardiology
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Copyright © 2000, European Society of Cardiology

Increased glycoxidation and lipoperoxidation in the collagen of the myocardium in hemodialysis patients

Jing Meng, Noriyuki Sakata and Shigeo Takebayashi*

The Second Department of Pathology, Fukuoka University Medical School, 45-1, 7-chome Nanakuma, Jonan-ku, Fukuoka 814-0180, Japan

* Corresponding author. Tel.: +81-92-801-1011, ext. 3285; fax: +81-92-863-8383 mengji{at}fukuoka-u.ac.jp

Received 22 September 1999; accepted 11 April 2000


   Abstract
Top
 Abstract
1 Introduction
 2 Subjects and methods
 3 Results
 4 Discussion
 References
 
Objective: The purpose of this study was to examine the glycoxidation and lipoperoxidation products in the collagen of the myocardium in hemodialysis (HD) patients and age-matched control subjects. Methods: Cardiac samples from 15 autopsied subjects (HD, n=6; control, n=9) were sequentially extracted with 0.9% NaCl and collagenase to obtain two fractions [soluble fraction (SF) and collagenase soluble fraction (CSF)]. The glycoxidation and lipoperoxidation products of these two fractions were measured by pentosidine-linked fluorescence ({lambda}ex, 335; {lambda}em, 385) and malondialdehyde (MDA)-linked fluorescence ({lambda}ex, 390; {lambda}em, 460), respectively. Results: Both pentosidine- and MDA-linked fluorescence were found to have significantly increased more in the collagenase soluble fraction (CSF) extracted form the anterior and posterior wall in HD patients than in the controls (P<0.05, control, n=9 vs. HD, n=6). Interestingly, the level of the lipid peroxides strongly correlated with that of the glycoxidation product in CSF (both P<0.0001 for the anterior and posterior wall). In contrast, in SF, which did not contain matrix collagen, neither significant difference nor correlation in the levels of pentosidine- and MDA-linked fluorescence was observed in these two groups. Conclusion: the present study provides the first biochemical evidence for an increase in glycoxidation and a close link between glycoxidation and lipoperoxidation in the collagen of the myocardium in hemodialysis patients. These findings suggest that these two spontaneous chemical reactions in the collagen matrix of myocardium may synergistically contribute to cardiac damage in hemodialysis patients.

KEYWORDS Enzymes (kinetics); Extracellular matrix; Fibrosis; Heart failure


   1 Introduction
Top
 Abstract
 1 Introduction
2 Subjects and methods
 3 Results
 4 Discussion
 References
 
The nonenzymatic reaction of reducing sugars such as glucose with proteins leads to the formation of advanced glycation end products by means of a biochemical process called the Maillard reaction [1]. Another spontaneous reaction of proteins is oxidation in vivo. Both nonenzymatic glycation and oxidation have been implicated in the pathogenesis of diabetic or non-diabetic complications [2–5]. Furthermore, a close relationship between nonenzymatic glycation and oxidation has been proposed and the resulting hypothesis suggests that the term ‘glycoxidation’ be used [2]. Glycoxidation reactions lead to the formation of permanent, irreversible chemical modifications and crosslinks in protein [2,6]. Carboxymethyllysine (CML) [6,7] and pentosidine [8,9] are two glycoxidation products.

An increase in oxidative stress has been reported in a uremic state [10–12]. In particular, increases in lipid peroxides, such as MDA and HNE, have been well documented in patients with CRF [13,14]. On the other hand, recent studies have demonstrated a marked increase in glycoxidation products, such as pentosidine, in plasma proteins [15], β2-microglobulin, amyloid fibrils [16], and skin collagen [17,18] in uremic patients. However, so far no information is available on the glycoxidation in the collagen matrix of the heart in uremic patients. We believe that such information is important due to an increase in cardiac damage in uremic patients.

The purpose of this study is to examine pentosidine, one of the glycoxidation products, in the collagen of the myocardium in uremic patients undergoing hemodialysis. Furthermore, since oxidative stress is a common base for glycoxidation and lipoperoxidation, it is reasonable to assume that some relationship might exist between lipoperoxidation and glycoxidation, and this hypothesis is also investigated in the present study.

Formation and clearance are two of the basic factors known to influence the tissue level of glycoxidation products, especially in patients with end-stage renal disease. Two fractions were extracted to reflect these two basic factors in this study. A structural collagen-binding fraction representing in situ formation was extracted by collagenase and was referred to as the collagenase soluble fraction (CSF). The other fraction was a soluble fraction (SF) representing clearance because this fraction was soluble and could be transferred and balanced freely between the myocardium and circulation.


   2 Subjects and methods
Top
 Abstract
 1 Introduction
 2 Subjects and methods
3 Results
 4 Discussion
 References
 
2.1 Subjects
Cardiac samples were obtained from 15 autopsied subjects, including 6 non-diabetic hemodialysis patients (HD), and 9 non-diabetic individuals without end-stage renal disease as a control group. The clinical characteristics of these subjects are shown in Table 1. The normal renal function was defined as a serum creatinine concentration of <1.5 mg/dl. End-stage renal disease in the nondiabetic HD patients was attributed to glomerulonephritis in two patients, rheumatoid arthritis in two and hypertension in two patients. The HD patients underwent dialysis [median duration of hemodialysis: 8.0 (0.6–15) years] on a conventional hemodialyzer. The investigation conforms with the principles outlined in the Declaration of Helsinki.


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  		Table 1 Profile of the subjects examined in this studya

 
2.2 Reagents
Bacterial collagenase (Type VII) was purchased from the Sigma (St. Louis, MO, USA). All other chemicals and reagents used were of analytical reagent grade.

2.3 Tissue preparation for the biochemical analysis
The heart was cut in a series of rings from the apex to base. The left anterior descending branch (LAD) of the coronary artery was inspected to exclude evident occlusion and myocardial infarction. The rings were put on a plate. The anterior wall was defined as the wall on the same side as the LAD, and the posterior wall, on the opposite of the anterior wall. The samples were collected from the anterior free wall (AFW) and the posterior wall of the left ventricle, the area of the anterior/posterior wall between the elongation line of the septum on the inner side and the parallel line drawn from the outermost point of the left ventricular lumen on the outer side (Fig. 1). After washing with phosphate-buffered saline, the samples were stored at –40°C until use. The preparation method of the samples for the biochemical analysis was as described by Charney et al. [19] with minor modifications.


Figure 1
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  		Fig. 1 Flow diagram for the fractionation of (1) SF and (2) CSF. Final insoluble precipitate was about 15% of 5 mg dry fiber. AFW, anterior free wall; LV, left ventricle; RV, right ventricle; NMWL, nominal molecular weight limit. Buffer A: 10 mM Tris HCl buffer (pH 7.4) containing 4 mM EDTA, 0.1 mM phenylmethylsulfonyl fluoride, 1 mM N-ethylmaleimide and 0.1 µg/ml pepstatin A. Buffer B: HEPES buffer (pH 7.4) containing 0.1 M CaCl2.

 
The samples were trimmed of the innermost and outermost 1 mm of tissue. The segments from the rings of each heart were pooled. A 2-g amount of the pooled wet sample were used to extract a SF and a CSF as described in the flow diagram (Fig. 1). In addition, 0.5 g of wet weight sample was used to analyze the total collagen content in terms of original tissue (Fig. 1). The SFs and CSFs were used to determine the amounts of pentosidine- and MDA-linked fluorescence. In addition, hydroxyproline and protein contents were determined for the CSFs and SFs, respectively.

2.4 Biochemical analysis
The CSF was assayed to determine the content of hydroxyproline. The determination of the collagen content was based on the assumption that hydroxyproline constitutes 14% of collagen. Hydroxyproline in the two fractions was measured according to the method of Stegemann and Stalder [20]. Briefly, 50 µl of the sample was acid-hydrolyzed in 1 ml of 6 M HCl at 110°C for 24 h. After the hydrochloric acid had evaporated, 4-hydroxyproline was measured with a spectrophotometer (Shimadzu, Kyoto, Japan). In addition, 0.5 g of wet weight sample of original heart tissue was placed in capped tubes to which 2 ml of 6 M HCl was added. The capped tubes were incubated at 110°C for 24 h. The resultant hydrolysates were analyzed for hydroxyproline as described above.

The protein concentrations in the SF were measured with a bicinchoninic acid protein assay kit (Pierce, Rockford, IL, USA) using human albumin as a standard protein according to the manufacturer's instructions.

The pentosidine and MDA-linked fluorescence [21] in the SFs and CSFs were measured at wavelengths of 335/385 and 390/460 nm (excitation/emission), respectively, using a spectrofluorophotometer (Shimadzu, Kyoto, Japan). The fluorescence values in SF, and CSF were corrected with those of the blanks containing the same concentration of NaCl and collagenase, respectively. Three replicate samples from each tissue pool were analyzed with one run each day on 3 consecutive days. The intra- and inter-assay CVs for pentosidine-linked fluorescence were 0.5–1.9 and 1.6–7.6%, respectively. The intra- and inter-assay CVs for MDA-linked fluorescence were 0.6–2.2 and 1.8–7.9%, respectively. The CSF data were expressed as arbitrary units per mg of collagen (AU/mg collagen). The SF was a non-collagen fraction which contained soluble extracts. Contaminated collagen in SF was excluded by ultrafiltration (NMWL 100x103; collagen: about 130x103). Because samples of SF contained no detectable collagen but still showed pentosidine and MDA-linked fluorescence, pentosidine and MDA in this fraction is associated with soluble protein. Therefore, the levels of pentosidine and MDA-linked fluorescence in SF were expressed as AU/mg protein.

2.5 Statistical analysis
All numerical data were expressed as the median with range. The significance of the differences between the two groups was analyzed by a non-parametric test (Mann–Whitney test). Probability values of <0.05 were considered significant.


   3 Results
Top
 Abstract
 1 Introduction
 2 Subjects and methods
 3 Results
4 Discussion
 References
 
The contents of collagen in the CSF extracted from 5 mg of fiber and total collagen in terms of 2 g wet weight of original myocardial tissue were demonstrated in Table 2. There was no significant difference in these parameters between the two groups although the total collagen in HD group tended to increase (Table 2).


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  		Table 2 Collagen contents in the CSF and original myocardial tissuea

 
As shown in Fig. 2, the levels of pentosidine-linked (a) and MDA-linked (b) fluorescence of CSF extracted from the anterior wall were significantly higher in the HD patients than in the control group. The levels of pentosidine-linked fluorescence were 42.91 (12.08–89.16) and 87.11 (55.47–155.34) (AU/mg collagen) for control and HD groups, respectively (medians with range, P<0.05 between control and HD). The level of the MDA-linked fluorescence also significantly increased in the HD patients. The fluorescence levels of MDA were 42.17 (7.87–78.58) and 86.36 (30.40–128.38) (AU/mg collagen) for control and HD groups, respectively (P<0.05 between control and HD). Interestingly, a strong correlation was observed between the level of the pentosidine-linked and MDA-linked fluorescence in the CSF (n=15, r=0.988, P<0.0001) (Fig. 2c).


Figure 2
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  		Fig. 2 Levels of pentosidine (a) and MDA-linked fluorescence (b) of CSF extracted from the anterior wall of the heart. The data were expressed as median with range. Box plots show median, 25th, and 75th centiles as the box, 10th and 90th centiles, plus outliers. *, P<0.05, between the controls (C) and the HD patients (HD). The pentosidine-linked fluorescence strongly correlated with the MDA-linked fluorescence (c). bullet, HD; {circ}, control; see Sections 2 and 3 for details.

 
A similar change of the oxidative products in HD patients was also present in CSF extracted from the posterior wall (Fig. 3). The levels of pentosidine-linked (a) and MDA-linked (b) fluorescence of CSF extracted from the posterior wall were significantly higher in the HD patients than in the control group. The pentosidine-lined fluorescence was 63.65 (13.55–124.23) and 105.29 (49.58–182.39) (AU/mg collagen) for control and HD groups, respectively (medians with range, P<0.05 between control and HD). The fluorescence levels of MDA were 51.73 (11.61–95.28) and 92.85 (42.59–145.30) (AU/mg collagen) for control and HD groups, respectively (P<0.05 between control and HD). A strong correlation was observed between the level of the pentosidine-linked and MDA-linked fluorescence in the CSF (n=15, r=0.989, P<0.0001) (Fig. 3c).


Figure 3
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  		Fig. 3 Levels of pentosidine (a) and MDA-linked fluorescence (b) of CSF extracted from the posterior wall of the heart. The data are expressed as median with range. Box plots show median, 25th, and 75th centiles as the box, 10th and 90th centiles, plus outliers. *, P<0.05, between the controls (C) and the HD patients (HD). The pentosidine-linked fluorescence strongly correlated with the MDA-linked fluorescence (c). bullet, HD; {circ}, control; see Sections 2 and 3 for details.

 
In contrast, the levels of pentosidine/MDA-linked fluorescence of SF were not significantly different in the two groups (Figs. 4 and 5Go). In SF from the anterior wall, the pentosidine-linked fluorescence was 1.98 (0.74–8.51) and 1.97 (1.56–5.85) (AU/mg protein) for control and HD groups, respectively (median with range, Fig. 4a). The MDA-linked fluorescence was 2.33 (1.80–6.25) and 3.27 (1.66–5.83) (AU/mg protein) for control and HD groups, respectively (median with range, Fig. 4b). Similarly, in SF from the posterior wall, the pentosidine-linked fluorescence was 3.80 (2.99–7.92) and 3.85 (2.92–5.91) (AU/mg protein) for control and HD groups, respectively (Fig. 5a). The MDA-linked fluorescence was 3.40 (2.76–8.00) and 4.37 (3.06–6.22) (AU/mg protein) for control and HD groups, respectively (Fig. 5b). In addition, no correlation was seen between the level of pentosidine-linked fluorescence and the MDA-linked fluorescence in the SF.


Figure 4
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  		Fig. 4 Levels of pentosidine (a) and MDA-linked fluorescence (b) of SF extracted from the anterior wall of the heart. The data were expressed as median with range. Box plots show median, 25th, and 75th centiles as the box, 10th and 90th centiles, plus outliers. C, control; HD, hemodialysis patients.

 

Figure 5
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  		Fig. 5 Levels of pentosidine (a) and MDA-linked fluorescence (b) of SF extracted from the posterior wall of the heart. Data are expressed as median with range. Box plots show median, 25th, and 75th centiles as the box, 10th and 90th centiles, plus outliers. C, control; HD, hemodialysis patients.

 

   4 Discussion
Top
 Abstract
 1 Introduction
 2 Subjects and methods
 3 Results
 4 Discussion
References
 
The focus of the present study was collagen-binding pentosidine and MDA, products of oxidative stress. The samples were taken and examined within 2–4 h postmortem since oxidation occurs rapidly, especially lipoperoxidation. As observed in our preliminary experiment using dermal samples from living subjects stored at 4°C, MDA-linked fluorescence did not significantly change during the preparation of samples [18]. Although lipoperoxidation is a rapid process and free MDA is very active, collagen-binding MDA, which produces fluorescence, could nevertheless remain stable for a short period of time. In addition, there were two reasons for us to choose an aliquot of collagen fiber, other than the total collagen as the target of the study. First, we believed that it was the insoluble collagen fiber, and not the soluble collagen, which contributes most to cardiac damages such as increased stiffness and lower compliance. Second, we thought that the biochemical change in collagen quality as observed in the present study was probably more important than a simple increase in collagen quantity in terms of cardiac damage as observed in the present study (Table 1, lower ejection fraction in HD patients).

We chose the anterior free wall of the left ventricle of the heart because a histological specimen was taken from this region as a routine procedure since the anterior free wall has a higher incidence of myocardial infarction. Myocardial infarction could be routinely excluded microscopically from the histological sections. It is important to rule out myocardial infarction because it could induce heterogeneity in collagen, including a mixture of newly synthesized and aged collagen. This heterogeneity will affect the pentosidine levels after normalization with the collagen contents because the pentosidine levels in the newly synthesized and aged collagen are different. In addition, the posterior wall of the left ventricle was also assayed to investigate if there was a difference of the oxidative products in different areas of the heart.

The levels of pentosidine-linked fluorescence in the CSF extracted from the anterior wall increased significantly more in hemodialysis patients than in the controls (Fig. 2a). Because pentosidine is inactive, its binding to matrix collagen is strong evidence of in situ formation. In the CSF, the level of MDA-linked fluorescence was also significantly higher in hemodialysis patients than that in the controls (Fig. 2b). A strong correlation was observed between the pentosidine and MDA levels (Fig. 2c). Similar changes were present in other region of the heart, the posterior wall (Fig. 3a–c). These data suggest that some common factor(s) might exist for the accelerated formation of the oxidative products in hemodialysis patients. Recently, carbonyl compounds have been proposed to be responsible for increased glycoxidation in patients with chronic renal failure [22]. The common factor could be an increased carbonyl stress since both MDA and pentosidine are products derived from carbonyl compounds [22]. However, the carbonyl compounds responsible remain to be identified. Another possible common factor for the accelerated generation of the oxidative products is probably the reactive oxygen species (ROS) released from the Maillard reaction. According to the original hypothesis proposed by Hodge [23], the central molecule responsible for the advanced Maillard reaction is the Amadori product. In the pathway of Amadori product degradation, H2O2 can be generated via both 1,2-and 2,3-enolization and the oxidation of the enolate anion [24]. Superoxidative products can also be formed in the pathway of Amadori product formation [24,25]. Therefore, carbonyl compounds and ROS may be responsible for the increased glycoxidation and peroxidation in the collagen matrix of the myocardium in hemodialysis patients.

In contrast, no significant difference in pentosidine and MDA levels in the SF, the non-collagen fraction (collagen was excluded by ultrafiltration, Fig. 1), was observed between the control and HD patients (Figs. 4 and 5Go). Since pentosidine and MDA in SF exist as a soluble form in the tissue specimens, MDA and pentosidine in SF could be interchanged between the tissue and circulation in vivo. The levels of these oxidative products in SF were thus largely influenced by renal or hemodialytic clearance. It seems that pentosidine and MDA in SF could be excreted by hemodialysis at least in part.

The MDA and pentosidine levels in two regions of the heart, the anterior and posterior wall, were examined in this study. The levels of MDA and pentosidine-linked fluorescence were not significant different in these regions (Figs. 2 and 3Go). Both glycoxidation and lipoperoxidation are spontaneous and non-enzymatic reactions. It seems that these two oxidative reactions occurred in an ‘indiscriminate’ way and caused nonselective damage in the extracellular matrix of the heart in HD patients. Cardiac failure is one of the major complications of HD patients, now accounting for between 40 and 50% of all deaths in this cohort [26]. Both glycoxidation and lipoperoxidation have been shown to cause alterations in the chemical structures and functions of collagen fibers, including cross-linking, rigidity and insolubility [5,27,28]. In this study, HD patients showed increases in the levels of collagen-linked pentosidine and MDA (Fig. 2). As a result, glycoxidative and lipoperoxidative modifications may cause structural and functional damages in the collagen matrix of the myocardium, which may be one of the mechanisms responsible for cardiac complications in HD patients.

In summary, the present study provides the first biochemical evidence for a close link between glycoxidation and lipoperoxidation in the collagen matrix of myocardium in HD patients. These findings suggest that these two spontaneous chemical reactions may synergistically contribute to cardiac damage in HD patients.

Time for primary review 21 days.


   Acknowledgements
 
This study was supported by Grant-in-Aid for Encouragement of Young Scientists (10770089) from the Ministry of Education, Science, Sports and Culture of Japan.


   References
Top
 Abstract
 1 Introduction
 2 Subjects and methods
 3 Results
 4 Discussion
 References
 

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