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Annals of Clinical & Laboratory Science 33:11-17 (2003)
© 2003 Association of Clinical Scientists

Oxidized Immunoglobulin G in Patients with End-Stage Renal Disease Treated by Hemodialysis

Shahid Ahmed, Nora Gibbons and Joseph Mattana
Department of Medicine, Long Island Jewish Medical Center, New Hyde Park, New York, (Long Island Campus for the Albert Einstein College of Medicine, Bronx, New York)

Address correspondence to Joseph Mattana, M.D., Division of Kidney Diseases and Hypertension, Room 228, Long Island Jewish Medical Center, New Hyde Park, NY 11040, USA; tel 718 470-7360; fax 718 470-6849; e-mail mattana{at}lij.edu.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
Patients with end-stage renal disease treated by hemodialysis have enhanced oxidative stress that may result in oxidation of IgG and resultant functional changes. In this study, Western blot analysis was used to assess the oxidized protein content of IgG samples purified from plasma of 8 controls and 11 patients on hemodialysis. In certain experiments, oxidized IgG was digested with papain and Western blot analysis was performed to identify oxidized Fc fragments. Compared to plasma IgG from controls, the IgG from hemodialysis patients had greater oxidized protein content, evidenced by more intense antibody binding to both the heavy and light chains. Western blot analysis of papain digests of oxidized IgG samples that were reprobed with an anti-Fc fragment antibody showed oxidative modification of the Fc fragment. These results suggest that patients with end-stage renal disease treated by hemodialysis have increased oxidized IgG in their plasma, including the Fc portion. Further studies are needed to see if this is due to enhanced production and/or decreased clearance of oxidized IgG.

(received 2 March 2002; accepted 25 August 2002)

Keywords: oxidative stress, immunoglobulin G, end-stage renal disease, hemodialysis


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
Uremia is characterized by abnormalities in both the specific and nonspecific components of the immune system [1]. Many studies confirm impairments in chemotaxis of polymorphonuclear leukocytes as well as in their phagocytosis, bactericidal activity, and metabolic functions [2,3]. There is also clinical evidence for defects in lymphocyte and monocyte function in patients with end-stage renal disease, such as delayed cutaneous hypersensitivity to common antigens and diminished host response to immunization with hepatitis B, influenza, and pneumococcal vaccines [4]. Plasma levels of different classes of immunoglobulins are usually in the normal range in these patients, but specific antibody responses are significantly depressed and it is unclear whether this impaired response is intrinsic to B cells or is linked to abnormal T cell and B cell interaction [1–4].

Increased predisposition to infection as well as to malignancy and accelerated atherosclerosis in patients with end-stage renal disease might be associated in part with the increased oxidative stress to which these patients appear prone. Patients with end-stage renal disease suffer increased oxidative stress that is manifested in part by increased circulating levels of oxidized lipids [5–11]. The increased susceptibility of lipids to oxidation in patients with end-stage renal disease may play a role in accelerated atherogenesis [7–10]. Likewise, oxidative modification of nucleotides can result in mutations and possibly malignant transformation of cells [12,13].

Proteins, like lipids and DNA, are also important substrates for biological oxidation [14]. It seems likely that, just as for lipids, oxidized proteins are not simply epiphenomena of oxidative reactions, but they may contribute to the pathophysiology of disease due to changes of their structure and function [15–19]. Increased protein oxidation has been demonstrated in normal human aging, in disorders characterized by accelerated aging, and in inflammatory diseases like rheumatoid arthritis and inflammatory bowel disease, although the pathophysiologic consequences of protein oxidation are not fully understood [14–19].

It is becoming recognized that protein oxidation may also be enhanced in end-stage renal disease patients. Witko-Sarsat et al [20–22] demonstrated oxidized plasma proteins in uremic plasma using size-exclusion chromatography. Odetti et al [23] measured oxidized proteins in plasma of end-stage renal disease patients by assaying the protein carbonyl content; they found it increased in the patients compared to normal controls, suggesting that protein oxidation is enhanced in hemodialysis patients. Shacter et al [24] showed that plasma proteins, including IgG, are susceptible to oxidation in vitro using a metal-catalyzed oxidation system. We reported that in vitro oxidation of IgG impairs its ability to bind to macrophage Fc receptors [25].

The goals of the present study were to identify oxidized IgG in patients with end-stage renal disease on hemodialysis and to determine specifically if the Fc fragment is susceptible to oxidation.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Acknowledgements
 References
 
Purification of IgG from patients with end-stage renal disease and controls.  The study was approved by the hospital’s Institutional Review Board for Human Experimentation; informed consent was obtained from all participants. Eleven patients and 8 healthy controls were studied.

The patients were all non-diabetic and were being dialyzed 3x/wk using cellulose acetate membrane dialyzers. The patients’ regimens all included a daily multivitamin tablet, plus folic acid (1 mg/day), ferrous sulfate (325 mg, 3x/day), and dietary restriction of sodium and potassium intake (each <=2 g/day). None of the patients had received an iv iron preparation, which might theoretically enhance oxygen radical generation, during the month before the study; none of the patients had ingested nutritional supplements, such as high-dose antioxidant vitamins, or any oral minerals, except ferrous sulfate.

None of the patients had received exogenous immunoglobulin infusions and none was being treated with antibiotics nor gave any evidence of infection at the time of the study.

For the hemodialysis patients, blood samples (5 ml) were drawn aseptically into EDTA-containing tubes from a port on the arterial circuit. For the control subjects, blood samples (5 ml) were drawn aseptically by venipuncture. The samples were centrifuged (2000 rpm, 4°C, 10 min) and the plasma was removed.

IgG was purified from plasma by use of an affinity column (Econo-Pac Serum IgG Purification Kit, Bio-Rad Laboratories, USA), according to the manufacturer’s instructions. The loading buffer, a 0.02 M solution of K2HPO4, was prepared with distilled, deionized water and filtered through a Sterifil D-HA (0.45 µm) filter unit. The pH was adjusted to 8.0 ± 0.2 with 10 N KOH or 6 N HCl and the buffer was stored at 4°C. The regeneration buffer was 1.5 M sodium thiocyanate solution prepared with the loading buffer. This buffer was also filtered through a Sterifil D-HA unit and stored at 4°C. The desalting column (Bio-Rad Laboratories), prepared according to the manufacturer’s instructions, was equilibrated with one bed-volume of loading buffer. Three ml of plasma was added to the column and the eluate was discarded. Four ml of loading buffer was added and the desalted plasma eluate was collected. Unless IgG purification was performed immediately, the desalted plasma eluate was stored at -70°C. The desalting column was washed with one bed-volume of distilled, deionized water that contained 0.02% sodium azide; the column was stored at 4°C.

The affinity column (DEAE-Affi-Gel Blue, Bio-Rad) was prepared according to the manufacturer’s instructions and equilibrated with 1.5 bed-volume of loading buffer. Desalted plasma (2.5 ml) was added to the column and the eluate was discarded. Loading buffer (20 ml) was added to the column and eluate fractions (2.5 ml) were collected. The affinity column was regenerated with one bed-volume of regeneration buffer, washed with 1.5 bed-volume of loading buffer containing 0.025% sodium azide, and stored at 4°C. A 30 µl aliquot of each fraction was analyzed by 10% SDS PAGE; protein levels of fractions were assayed by Bradford’s method [26], using a reagent kit (Bio-Rad Laboratories).

Western blot analysis.  Protein oxidation results in the formation of carbonyl groups that can be labeled with 2,4-dinitrophenylhydrazine (DNPH) to form stable protein hydrazones [16] for which highly specific antibodies are available. Western blot analysis of IgG, isolated as described above, was performed by a modification of the method of Shacter et al [24], as previously used by us to examine IgG oxidized in vitro [25].

For Western blot analysis, samples were dissolved in 6% SDS, mixed with an equal volume of 10 mM DNPH, and incubated for 15 min at room temperature. The samples were then incubated with 7.5 ml of neutralization solution (OxyBlot,TM Oncor Corp., Gaithersburg, MD) and an equal volume of 2x-concentrated sample buffer was added. Sample aliquots (1.5 µg protein content), as well as a solution of oxidized protein molecular mass markers (Intergen Company, Purchase, NY), were loaded onto 4–15% acrylamide gradient gels and analyzed by SDS-PAGE under reducing conditions (by adding 2-mercaptoethanol to the sample mixture to achieve a final concentration of 0.74 M).

After separation by SDS-PAGE, the proteins were electrophoretically transferred to nitrocellulose membrane, soaked in PBS-T solution (phosphate buffered saline, pH 7.2, containing 0.05% Tween 20), and incubated on a rocker with blocking buffer (PBS-T containing 1% bovine serum albumin). The membrane was then incubated for 1 hr with the primary antibody (1:150 dilution), which was a rabbit antibody that specifically recognizes DNPH bound to oxidized protein (Oncor Corp.). This antibody does not bind to free DNPH [4].

The membrane was rinsed twice with PBS-T and then incubated with PBS-T, once for 15 min, and twice for 5 min. The membrane was then incubated with secondary antibody (1:300 dilution), which was an HRP-conjugated goat anti-rabbit IgG, for 1 hr at room temperature. The membrane was then rinsed and incubated with PBS-T in the same fashion as was done following the incubation with primary antibody. This was followed by incubation with ECL chemiluminescent reagent (Amersham Corp., Amersham, UK). Autoradiographs were prepared using Kodak "X-OMAT" autoradiographic film.

Measurement of IgG protein carbonyl content.  IgG samples from controls and hemodialysis patients were precipitated in 10% trichloroacetic acid (TCA) at 4°C. The samples were centrifuged and the precipitates resuspended in 10 mM DNPH in 2N HCl. In parallel, the samples were also incubated with 2N HCl without DNPH. In all experiments, the incubations with DNPH or HCl alone were carried out at room temperature for 30 min with vortexing every 10 min. Proteins were precipitated in TCA, centrifuged, and the supernatants were discarded. Samples were extracted 3x with 1 ml ethanol-ethylacetate (1:1, v/v). The precipitates were redissolved in 6 M guanidine solution in 20 mM potassium phosphate that was adjusted to pH 2.3 with 0.05% trifluoroacetic acid. Any insoluble material was removed by centrifuging. Absorbance of the samples was measured by spectrophotometry at 374 nm.

The difference in absorbance between the DNPH-treated samples and the samples treated in parallel with HCl alone (without DNPH) was used to calculate the carbonyl content, using the molar absorption coefficient of 22,000 M-1cm-1 for aliphatic hydrazones [16]. Protein contents of the samples were determined by the Bradford method [26]. Carbonyl contents of the samples were expressed as nmol carbonyl/mg protein.

Western blot analysis of papain digests and reprobing with anti-Fc fragment antibody.  To identify more specifically the oxidized portions of the IgG molecule, purified IgG samples from patients with end-stage renal disease and healthy controls were subjected to digestion with papain. Papain cleaves the IgG molecule into Fab and Fc fragments that are joined by disulfide bonds. Under reducing conditions, the bonds separate to yield heavy chain fragments, Fc fragments, and light chains. In brief, each sample of IgG was diluted to 3 mg/ml in 100 mM sodium acetate, pH 5.5. To 1 ml of this solution, 50 µl of 1 M cysteine and 50 µl of 20 mM EDTA were added. Thirty µg of papain were added and the sample was incubated at 37°C for 4 hr. Iodoacetamide was added to a final concentration of 75 mM and the sample was incubated for 30 min at room temperature. Each sample was then subjected to Western blot analysis using an antibody to DNPH-labeled oxidized protein, as described above, with 12% acrylamide gels to achieve an adequate separation based on the predicted fragment sizes. In other experiments, the membranes were stripped and reprobed with an antibody to the Fc portion of human IgG (polyclonal goat anti-human IgG Fc antibody, Axell, 1:4000 dilution) and autoradiographs were generated and compared to identify oxidized Fc fragments.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Acknowledgements
 References
 
Western blot analysis of purified IgG from hemodialysis patients and controls.  Fig. 1Go shows representative Western blots for DNPH-labeled oxidized protein of purified IgG from 11 hemodialysis patients (H) and 8 controls (C), run under reducing conditions. As this figure illustrates, for the hemodialysis patients, there appeared to be increased antibody binding to bands that correspond to the heavy and light chains of IgG. These results suggest that the oxidized IgG content is increased in the plasma of hemodialysis patients and that both the heavy and light chains are susceptible to oxidation in vivo.



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  		Fig 1. Western blot analysis of IgG purified from hemodialysis patients (H) and controls (C). Plasma was obtained from 11 hemodialysis patients and 8 controls and IgG was purified (see Methods). The purified IgG was subjected to Western blot analysis using an antibody to DNPH-labeled carbonyl groups on oxidized proteins. The 4 autoradiographs shown include all of the patients and controls in the study; the antibody binding to the IgG samples from hemodialysis patients appears to be greater, compared to the IgG samples from controls.

 
Carbonyl content of IgG.  To obtain a quantitative assessment of IgG oxidation, we carried out carbonyl analysis. When the IgG samples from 11 hemodialysis patients and 8 control subjects were analyzed, the carbonyl content was found to be greater in IgG from hemodialysis patients. The carbonyl content of IgG from hemodialysis patients was 2.06 (SD ± 0.3) nmol/mg protein, versus 1.2 (SD ± 0.03) nmol carbonyl/mg protein in IgG from controls (p <0.05). These results indicate that there is more oxidized IgG in plasma of patients on hemodialysis, compared to controls.

Western blot analysis of papain-digested IgG and reprobing with Fc fragment antibody.  Fig. 2Go illustrates the typical results of a Western blot analysis for oxidized protein in IgG samples from 3 hemodialysis patients (H) and 1 control subject (C). The IgG samples (H,C) were digested with papain, except for an undigested IgG sample from a hemodialysis patient (U). These experiments were carried out under reducing conditions. In Fig. 2Go, in the first lane (ie, undigested IgG), there are 2 bands that correspond to the heavy and light chains of IgG. To the right are the papain-digested IgG samples from hemodialysis patients (H) and a control (C). Two bands with prominent antibody binding to DNPH-labeled carbonyl groups correspond to Fc fragments and light chains. These bands are more prominent in the samples from hemodialysis patients (H), compared to the control (C).



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  		Fig 2. Western blot of purified IgG with/without papain digestion, probed with antibody to DNPH-labeled oxidized proteins. Undigested IgG from a hemodialysis patient (U) was run along with papain-digested IgG from 3 hemodialysis patients (H) and a control (C). Under reducing conditions, nondigested IgG has heavy and light chains. In papain-digested IgG, bands corresponding to Fc fragments and light chains are prominent for hemodialysis patients and less so for the control. Faint bands of undigested heavy chains are seen, derived from some undigested IgG. In papain-digested IgG, the lower band corresponds to light chains in undigested IgG; the upper band corresponds to oxidized Fc fragments.

 
As shown in Fig. 2Go, the light chain band in the undigested IgG lanes corresponds to the lower band in the papain digest lanes, consistent with this representing light chains, while the band above it represents oxidized Fc fragments. To confirm that the upper band represents oxidized Fc fragments, membranes were stripped and reprobed with an antibody to the Fc portion of IgG. Fig. 3Go demonstrates that the upper band in the papain digest lanes represents the Fc portion of IgG.



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  		Fig 3. Purified IgG samples from patients with end-stage renal disease on hemodialysis and healthy controls were digested with papain and analyzed by Western blotting for DNPH-labeled oxidized protein (left panel). Blots were then stripped and reprobed with an antibody to the Fc portion of human IgG (1:4000) (right panel). Representative autoradiographs from the same blot are shown in order to demonstrate that the upper of the two bands corresponds to Fc fragments. H: IgG from hemodialysis patients; C: IgG from controls.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Acknowledgements
 References
 
In this study we found that plasma IgG of end-stage renal disease patients has increased content of oxidized protein. Using Western blot analysis, it was evident that both the heavy and light chains of IgG were oxidized, as well as the Fc portion of IgG using papain digestion. IgG is the predominant antibody in the secondary immune response and constitutes an important defense against bacteria and viruses. The variable region of IgG is responsible for antigen recognition and binding, whereas the constant region is responsible for various biological functions such as complement activation and binding to cell surface receptors. IgG binding takes place via interaction of the Fc receptors of phagocytic cells with the Fc portion of the IgG heavy chains. The interaction of antigen with antibody, the uptake of immune complexes by phagocytic cells, and the subsequent killing of foreign organisms by generation of free radicals are important mechanisms in the response to infection. Biochemical modification of IgG molecules may alter their interaction with antigens as well as their ability to bind to phagocytic cells [27,28]. The Fc portion may be a particularly susceptible region of the IgG molecule for oxidative modification. Binding to Fc receptors on phagocytic cells might expose the Fc portion to substantial amounts of oxygen radicals, although this is speculative. Papain digestion of IgG revealed that Fc and Fab fragments were both prone to oxidative modification. However, only the light chain portion of Fab fragments showed susceptibility to oxidation.

In a previous study, we oxidized IgG in vitro using an FeCl3/EDTA/ascorbate metal-catalyzed oxidation system [25]. In that study, papain digestion of oxidized IgG under reducing conditions yielded an additional band that represented IgG heavy chain fragments, along with light chains and the Fc portion of IgG. This difference suggests the possibility that in vitro oxidation under our experimental conditions diffusely involves the whole IgG molecule, causing both light chains and heavy chain fragments of the Fab portion to be equally oxidized. In comparison, IgG bound to an oxygen radical-generating cell, such as a macrophage, may have regions that are more or less exposed to oxygen radicals. Consequently, this may lead to a different in vivo pattern of IgG oxidation, compared to that observed in vitro. Since we did not reprobe papain digests for Fab, we cannot exclude the possibility that Fab carbonyl was enhanced as well. If so, this could have potential implications for antigen binding.

It should be emphasized that, while this study suggests that levels of oxidized IgG may be increased in end-stage renal disease patients on hemodialysis, this study does not delineate the pathophysiological mechanism. Enhanced generation of oxidized IgG might be the principal cause, although impaired clearance of oxidized IgG is also plausible. Further studies are required to determine this.

In summary, plasma samples from patients with end-stage renal disease who were being treated by hemodialysis appear to have an increased content of oxidized IgG, which may reflect its enhanced production via oxidative stress and/or its diminished clearance. The increased oxidation of IgG appears to include oxidative modification of the Fc portion of the molecule; this change may potentially contribute to some of the immunologic abnormalities that occur in these patients.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
References
 
This work was supported by a Beginning Grant-in-Aid from the American Heart Association Heritage Affiliate and by a Faculty Research Award from the Long Island Jewish Medical Center, which is the Long Island Campus for the Albert Einstein College of Medicine, Bronx, NY.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 

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