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Chapter 2 Materials and Methods

2.10. Western blot analysis

Following the separation of proteins by SDS–PAGE, the gel was electrically transfer to a

nitrocellulose-membrane attached with a 3MM filter paper pre-soaked in a transfer buffer

containing 48 mM Tris–HCl, 39 mM glycine, 0.037% SDS (w/v), and 20% methanol (v/v),

pH 8.3. The rest of the procedures for immunoblot was similar to that described previously

[9,10].

RESULTS

In our previous studies, we have described mAb and hemoglobin affinity-column

methods for the purification of human Hp [10,11]. Although these two methods, using PBS

(pH11) as an eluent, were simple; the average Hp recovery was lower than 50% and an

additional chromatographic step was need to remove the contaminated apoA-I. To improve

the recovery and the purity of isolated Hp in the present report, the following steps described

below were conducted.

3.1. Evaluation of dissociation of bound Hp from immobilized mAb

To optimize the elution conditions for the yield of Hp while isolating, we evaluated the

Hp and mAb interaction on an ELISA plate to mimic the Hp binding on mAb affinity column.

Various modified eluting buffers including PBS (pH 11), 4 M urea-PBS (pH 11), and 0.1%

SDS-PBS (pH 11) were studied. Fig. 2 demonstrates that the dissociation of bound Hp from

mAb was not completed using PBS, pH 11. However, the bound Hp was completely

dissociated when using the same PBS buffer containing 0.1% SDS. Buffer containing 4M

urea was only partially effective. The data suggest that SDS with pH 11 could be a useful

reagent for eluting the bound Hp.

3.2 Effect of the concentration of SDS-PBS, pH 11, on the dissociation of bound Hp from

immobilized mAb

To optimize the concentration of SDS capable of dissociating Hp from immobilized mAb,

serial diluted SDS was used for the assay. Fig. 3 shows that the SDS concentrations greater

than 0.08% completely dissociated Hp from the mAb. Since the mAb was immobilized on

the plate as a capture, it is worth mentioning that SDS at 0-2.5% did not cause the dissociation

of immobilized mAb from the plate (data not shown).

3.3. Initial purification of Hp1-1, 2-1, and 2-2 on immunoaffinity chromatography

Fig. 4 shows the optimal conditions for the recovery of Hp phenotypes from the column.

Overall, the Hp yield using SDS-PBS, pH 11 as an eluant was two times higher than that

using PBS, pH 11 (a conventional method) or SDS-PBS, pH 7.4. Interestingly, eluting

buffer of SDS with pH 7.4 delayed the Hp retention time. One of the explanations is that

antibody-antigen interaction is mostly ionic dependent; SDS at neutral pH slowly alters the

conformation of antigen or antibody via a protein-SDS micelle formation [15]. Further

conformational change is induced at high pH resulting in the dissociation of antigen-antibody

complex. Thereby, elution of Hp by SDS combined with pH 11 resulted in high recovery of

Hp 1-1 (71%), 2-1 (68%), and 2-2 (85%) from the column (Table. 1). Nonetheless, the

isolated Hp appeared to contaminate some apoA-I (Fig. 4D).

3.4. Removal of apoA-I contamination

ApoA-I is a major apolipoprotein residued in HDL [16]. It has been known for some

time, apoA-I is a major contaminant in isolated Hp using variety of the methods [9,10]. To

minimize the apoA-I contamination, we evaluated the HDL and Hp interaction on an ELISA

plate immobilized with Hp. Fig. 5A reveals that apoA-I was able to bind Hp, but bound

apoA-I was dissociated from Hp at SDS (pH 7.4) concentrations greater than 0.025%. In the

next experiment, we mimicked the above condition directly on the affinity column. By

SDS-PAGE, concentrations between 0.02 and 0.04% of SDS could wash bound apoA-I away

from the column, but higher concentrations of SDS (≧0.06%) removed both apoA-I and Hp

from the immobilized mAb (Fig. 5B). Likewise, 0.04% SDS-PBS (pH 11) also removed

apoA-I and Hp (data not shown). The data indicate apoA-I can be selectively removed using

0.04% SDS-PBS, pH 7.4, prior to a final elution of Hp.

3.5. Final affinity purification of bound Hp via pre-wash with 0.04% SDS-PBS, pH 7.4

Finally, we used 0.04% SDS as a pre-wash for the removal of bound apoA-I from Hp

over the affinity column. Fig. 6 shows a typical chromatographic profile for the plasma of

Hp 1-1, 2-1, or 2-2. Following a flow through of plasma and washes with a PBS, pH 7.4, the

column was then pre-washed with 0.04% SDS-PBS, pH 7.4 to remove bound apoA-I as well

as other non-specifically bound proteins as fraction 1 (F1). Next, 0.1% SDS–PBS, pH 11

was used to elute bound Hp from mAb as fraction 2 (F2). Fig. 6 exhibits that pre-wash

fraction (F1) had most of apoA-I contaminant as identified by a SDS-PAGE and confirmed by

a Western blot analysis. The homogeneity of final isolated Hp was about 97% (Fig. 6, F2

fraction). The final recovery of isolated Hp 1-1, 2-1, and 2-2 was approximately of 56, 55,

and 71%, respectively (Table 1).

3.6. Analysis of hemoglobin-binding property of isolated Hp 1-1, 2-1, and 2-2

Fig. 7 reveals that final isolated Hp possessed the ability to form complex with Hb using

a 7% native PAGE analysis. Each phenotype formed complex with Hb as a monomer (Hp

1-1) and polymers (Hp 2-1 and 2-2), while Hp 2-1 shared one completely identical monomer

to Hp 1-1.

DISCUSSION

Clinically, Hp phenotypes are found to be related to several inflammatory diseases. For

examples, polymeric form of Hp 2-1 or 2-2 is associated with the complications of myocardial

infarction [17], kidney failure [18], and diabetics [19]. In a prospective study, human

subjects with Hp 2-2 are at a 5-fold increased risk for the development of CAD as compared

to those with Hp 1-1 [20]. The risk in heterozygous Hp 2-1 participates is intermediate [20].

Low levels of Hp are also found among HIV-1 seropositive patients with Hp 2-2 [21]. Due

to the difficult purification procedures for each Hp phenotype, the relationship between the

Hp levels and its affected diseases are rarely reported. One of the most difficulties is to

isolate Hp 2-1 and 2-2 because of their heterogeneity with polymeric molecular forms (Fig. 1).

On the other hand, it is essential to study the structural and functional relationship among the

Hp phenotypes. Previously, Rademacher et al. [22] utilize the chicken

hemoglobin–Sepharose affinity column to isolate human Hp; the harsh-elution condition (8M

urea) causes the dissociation of a hemoglobin subunit from the Sepharose matrix.

Meanwhile, human apoA-I appears to be another major contaminant. Travis et al. [23]

employ Sephadex G-200 gel filtration, but the purified Hp is accompanied with large amounts

of IgM and a-2 macroglobulin. Morimatsu et al. [24] provide a modified method using

HPLC with anion-exchange, Sephacryl S-300, TSK Phenyl-5PW, and TSK DEAE-5PW

columns together; the procedures however are time-consuming and the yield is relatively low.

In our previous studies, we utilized hemoglobin or Hp mAb (prepared against Hp

β-chain;clone 8B1-3A) affinity column to isolate three phenotypes of Hp [10,11]. Both

methods showed that there was a contamination of apoA-I, when eluting Hp by PBS, pH 11.

To remove contaminated apoA-I, a re-chromatography on an HPLC Sephorose-12

gel-filtration was required [11]. For this reason, one major focus of this report was attempt

to minimize the contamination of apoA-I. To test the possibility that plasma HDL (apoA-I

containing lipoprotein) may directly bind to Hp, we immobilized purified Hp on an ELISA

plate followed by the addition of excess amount of HDL to saturate its interaction with Hp, if

any. Most interestingly, we found that HDL could bind Hp (Fig. 5), although the binding

affinity between HDL and Hp was not readily known. Such binding is not non-specific,

since Hp can inhibit the apoA-I-dependent lecithin:cholesterol acyl transferase (LCAT)

activity in vitro [25], which plays a role in the reverse cholesterol transport [26]. The data

suggest that HDL is associated with Hp in plasma, at least in part. Fortunately, the binding

affinity seemed to be differentially lower than that of Hp-mAb. It was why 0.04% SDS-PBS

(pH 7.4) only removed apoA-I from Hp, but not Hp from immobilized mAb (Fig. 5). But,

SDS concentrations ≧ 0.06% or 0.04% SDS-PBS at pH 11 should be avoid for pre-wash as

Hp could come off the column. In an early study [9], we proposed to use HDL depleted

plasma (a bottom fraction obtained by ultracentrifugation at KBr d.1.21 g/ml) for Hp

purification, assuming the contamination of plasma apoA-I could be eliminated. This

experiment was conducted in the present study. The isolated Hp still contained some apoA-I,

but not as much as that of whole plasma (data not shown). Therefore, the use of

HDL-deficient plasma for Hp purification may not be considered in the future.

SDS is used more often than any other detergent as an excellent denaturing or unfolding

reagent [15,27]. It breaks mostly the quaternary and tertiary protein-protien interaction

[28,29]. As such, at low SDS concentration (0.04%), pH 7.4, it dissociates the apoA-I from

Hp. While at 0.1% of SDS, pH 11, it elutes bound Hp from the immobilized mAb over the

affinity column. However, one concern is that SDS may alter the conformation of isolated

Hp. Biswas and Das reported that α-Crystallin was able to refold to native structure after

unfolding by SDS [29]. To address whether isolated Hp could refold closely to its native

conformation, we monitored the structure of Hp 1-1 using a circular dichroic

spectrophotometer. We found SDS-eluted Hp being slightly more disordered than that of Hp

eluted without using SDS. Following extensive dialysis in 4 l PBS with three changes, the

disordered structure, however, refolded to the original alpha-helical content (about 30% helix)

as that values previously reported [11] (data not shown). Furthermore, we have shown that

the formation of Hp-Hb complex is dependent on the overall conformation of Hp [8]. In the

present study, the purified Hp following a dialysis could form complex with Hb (Fig. 7),

suggesting that Hp have refolded to native form. Nevertheless, the purified Hp also retained

its immunochemical property as determined by Western blot and ELISA (data not shown).

Taking together, the present method using SDS as an eluant has certain advantages.

First, Hp can be purified in a predictable way by passing it through the immobilized mAb.

Second, the bound apoA-I (or other non-specially bound proteins) is selectively removed prior

to final elution of Hp. Third, the technique allows isolation of the polymeric form of Hp 2-1

and 2-2 (Fig. 7) unlike standard methods which may significantly lose part of them. Some

standard methods which rely on different molecular masses or charges can distribute the

component to different fractions. Fourth, the simple technique can be used for analytical

purpose, for example, for the determination of polymeric forms of Hp that may be of

important for the investigation of metabolism in pathological cases. Because SDS is used in

the elution buffers, it is worth mentioning that a large volume of PBS (300 ml), pH 7.4, is

required for the regeneration of the column, which is time consuming and considered to be

one disadvantage of the present method.

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Fig. 1. Schematic drawing of molecular arrangement in huamn Hp phenotypes. Hp 1-1

possesses only the basic dimer (α1-β)2. While Hp 2-1 is comprised of many structures, a

dimer (α1-β)2, a trimer (α-β)3, and other linear polymers. Here, α represents both α1 and α2

chains. Hp 2-2 is comprised of a trimer (α2-β)3 and other cyclic polymers. Each α1, α2,

or β is 83, 142, or 245 amino acids in length, respectively. α2 is similar to α1, differing only

by an additional insertion of a repeat identical to 3/4 of α1. Due to the extra Cys-74 in α2,

Hp 2-1 and 2-2 form complicated polymers.

Fig. 2. Evaluation of dissociation of bound Hp from immobilized mAb at various elution

conditions. To determine a simple and optional condition that is able to elute the Hp from

immobilized mAb, Hp mAb was first immobilized on an ELISA plate followed by incubating

50 μg of purified Hp 2-1 in 50 μl PBS. After washing, bound Hp was then treated with

various eluting buffers. (A) Total binding of Hp without eluting reagents; (B) PBS, pH 11;

(C) 4 M urea-PBS, pH 11; (D) 0.1% SDS-PBS, pH 11. Binding of Hp was determined using

goat anti-Hp followed by HRP conjugated anti-goat IgG for final development of

chromogenicity. Each value represents a mean of triplicates ± SD.

Fig. 3. Effect of SDS concentrations (pH 11) on the dissociation of bound Hp from

immobilized mAb. The remaining Hp was determined similar to that described in Fig. 2.

Each point represents a mean of triplicates ± SD. Typical deviation is shown in the first

three doses.

Fig. 4. Elution profile of bound Hp from immobilized mAb on immunoaffinity column

(A-C) and contamination of apoA-I in isolated Hp (D). (A-C) One ml of human plasma

was applied onto the immunoaffinity column and washed with a PBS, pH 7.4. The bound

Hp was subsequently eluted with a 0.1% SDS-PBS, pH 11 and with a 0.1% SDS-PBS, pH 7.4.

The overall data suggests that the eluting buffer containing 0.1% SDS at pH 11 results in high

yield for Hp purification. (D) Analysis of isolated Hp by a 15% SDS-PAGE containing 1%

2-mercaptoethanol. It reveals that isolated Hp contaminates apoA-I.

Fig. 5. Binding of HDL with Hp and its dissociation by SDS. (A) Hp was first

immobilized on an ELISA plate followed by incubating 50 μg of purified HDL in 50 μl PBS.

After washing with PBS, the bound HDL dissociated from Hp by treating with SDS in a

dose-dependent fasion. Binding levels of HDL were determined using goat anti-apoA-I

followed by HRP conjugated anti-goat IgG similar to that described in Fig. 2. The data

suggests that Hp associated apoA-I can be eliminated in the presence of SDS. (B) Eluant

from affinity column, eluted with 0.02%, 0.04% and 0.06% SDS-PBS, pH 7.4, was analyzed

by SDS-PAGE in the presence of reducing reagent. It suggests to avoid of using 0.06% SDS

for apoA-I removal.

Fig. 6. Final purification of human Hp 1-1 (A), 2-1 (B), and 2-2 (C) from immunoaffinity column pre-washed with 0.04% SDS-PBS, pH 7.4. (A-C) Initially, 1 ml of human plasma was passed through the column with PBS, pH 7.4 and washed with the same buffer. The bound Hp was then pre-washed with 40 ml of 0.04% SDS-PBS, pH 7.4 to remove Hp associated apoA-I (F1). Finally, Hp was eluted from immobilized mAb by 0.1% SDS-PBS, pH 11 (F2). (D) Analysis of F1 and F2 on 15% SDS-PAGE containing 1%

2-mercaptoethanol and F1 on Western blot (F1'). The α and β subunits corresponding to each Hp phenotype are shown.

Fig. 7. Analysis of hemoglobin-binding property of isolated Hp 1-1, 2-1, and 2-2 (A) and

Hp 1-1, 2-1, and 2-2 from human plasma (B) on 7% native-PAGE. Briefly, each isolated

Hp (5 μg) or each plasma (6 μl) was incubated with hemoglobin (Hb) (5 μg) at room

temperature for 30 min. Following electrophoresis, the gel was stained directly by a freshly

prepared DAB solution containing 0.05% H2O2 as a developer for the endogenous peroxidase

activity of hemoglobin.

INTRODUCTION

Porcine Hp is an acute phase protein with a molecular weight approximate 120 kDa [1-3].

It possesses an electrophoretic mobility and quaternary structure similar to human Hp 1-1

being a homodimer (αβ)2 that is linked by disulfide bridges [3, 4]. Due to its homogeneity,

porcine Hp can be purified by a one-step HPLC gel-filtration chromatography established in

our laboratory [5].

Functions of Hp have been proposed comprehensively; one of the major functions is to

scavenge and complex with plasma free hemoglobin (Hb) that possesses an oxidative toxicity

via iron-containing hemes [6, 7]. The Hp-Hb complex is then metabolized through a

cycteine-rich receptor (CD163) on macrophage [8]. It has the bacteriostasis ability by

attenuating iron necessary for bacteria growth [9, 10]. Hp has also been proved to be an

extremely potent antioxidant which directly inhibits Cu(Ⅱ) induced low density lipoprotein

oxidation and reduces cell oxidative stress [11].

The plasma concentration of porcine Hp increases significantly during infection,

inflammation, and tissue damage [12, 13]. Pigs with lameness, tail biting or diarrhea show a

high level of Hp [14]. Natural infections of pigs with porcine reproductive and respiratory

syndrome virus (PRRS) [15], or with Actinobacillus pleuropneumoniae [13], Mycoplasma

hyorhinis [16] and Toxoplasma gondii [17] bacteria resulted in a significant elevation of their Hp levels. The protein level has therefore been used to identify both clinical and subclinical

diseases [1, 18] as well as to monitor the health status in pig production [14].

Human plasma Hp is classified as three phenotypes: 1-1, 2-1, and 2-2 (Fig. 1) [11, 19].

Hp 1-1 is a molecule of homodimer or (αβ)2, whereas 2-1 is comprised of multiple forms

including homodimer, trimer, tetramer, and other linear polymers. Hp 2-2, on the other hand,

consists of trimer, tetramer, and other cyclic polymers. In non-human mammalians, both

dimeric and polymeric forms of Hp exist. Thus far, polymeric forms analogous to human

polymeric Hp are found only in ruminant families of Artiodactyla order [20]. TLY minipigs

classified as Sus scrofa are aborigine in Taiwan with ears smaller than the other breeds. The

body weight of TLY is usually lower than 25 kg during the first six months of age as

compared with 80 kg of other domestic pigs [21]. Due to its low body weight and conserved

population, TLY minipigs have been used as an experimental animal [21]. In the present

study, we phenotyped the Hp of TLY minipigs. While phenotyping, we noticed that many

of them possessed very low plasma levels of Hp. The cDNA nucleotide sequence of TLY

Hp was also conducted to study whether there was a gene defect. It is of interest to observe

that there is no direct relationship between the putative amino-acid sequence of Hp and its

levels. Their amino-acid sequences are almost completely identical to that of domestic pigs

(except Val-65ÆLeu-65). Finally, a noncompetitive ELISA was employed to determine

their plasma Hp levels. In average, the mean Hp levels of TLY (0.21 ± 0.25 mg/ml) were

significantly lower (4X) than that of domestics (0.78 ± 0.45 mg/ml) (p<0.001). Among

which, 25% of TLY revealed a level lower than 0.05 mg/ml. The present study may provide

a reference value for the future use of TLY as an animal model for inflammatory,

cardiovascular, and infectious disease studies.

MATERIALS and METHODS

2.1. Materials

Purified porcine Hb and rat polyclonal antibodies against porcine Hp were prepared

according to the methods previously described [5, 22]. Goat anti-rat IgG was purchased

from Chemicon (Temecula, CA). Sepharose-12 HR column was obtained from Pharmacia

(Uppsala, Sweden). Total RNA extraction kit was purchased from Geneaid (Taipei, Taiwan).

All other chemicals were purchased from Sigma-Aldrich (St. Louis, MO) without any further

purification. The buffers used in this report were all filtered through a 0.45-μm filter before

use (Millipore, MA, USA).

2.2. Preparation of plasma samples

Forty-three TLY minipigs (23 sows and 20 boars) aged from 1 to 2 years were raised in

Taitung Animal Propagation. Thirty-five domestics (12 Durac, 15 Landrace, and 8 Yorkshire)

aged 6-8 months used in this study were from Animal Technology Institute, Taiwan. All of

these pigs were reared in a natural lighting environment. Management and medical

treatment were conducted according to the instruction established by National Science

Council of Taiwan. Pigs were vaccinated against swineenzooticpneumonia, hog cholera,

pseudorabies, atrophic rhinitis, foot and mouth disease, and Actinobacilluspleuropneumoniae.

All selected animals were free of adverse signs of disease after a clinical examination in the

herd. Blood samples were collected via jugular puncture using a 25-gauge needle and added

into the tubes containing 0.1% ethylenediaminetetraacetic acid (EDTA). Plasma was

obtained by a centrifugation at 2,000 g for 20 min and stored at -20℃ until analysis.

2.3. Phenotyping of Hp

A 7% native-polyacrylamide gel electrophoresis (native-PAGE) was conducted

according to the Laemmli’s method with the use of 5% polyacrylamide (w/v) as a stacking gel

[23]. Eight μl of plasma was incubated with 16 μg of porcine or human Hb for 30 min at

room temperature and subsequently mixed with a loading buffer [12 mM Tris–HCl, pH 6.8,

5% glycerol (v/v), 2.88 mM of 2-mercaptoethanol, and 0.02% bromphenol blue (w/v)] in a

final volume of 15 μl. Following the electrophoresis, the gel was briefly washed and then

immersed in freshly prepared 3,3’-diaminobendidine (DAB) solution (0.125 g of DAB

dissolved in 0.5 ml DMSO with the addition of 30 ml deionized H2O containing 0.05% H2O2)

with gently shaking to develop the pattern of Hp-Hb complex.

2.4. Western blot

Following the separation of proteins by SDS–PAGE, the gel was electrically transferred

to a nitrocellulose-membrane attached with a 3MM filter paper presoaked in a transfer buffer

containing 48 mMTris–HCl, 39 mM glycine, 0.037% SDS (w/v) and 20% methanol (v/v), pH

8.3. The rest of the procedures for Western blot were similar to that described previously [5,

24]. Rat polyclonal antibody against β chain of porcine Hp was used for the determination

24]. Rat polyclonal antibody against β chain of porcine Hp was used for the determination

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