Interactions of Apolipoproteins AI, AII, B and HDL, LDL, VLDL with

Article pubs.acs.org/Langmuir

Interactions of Apolipoproteins AI, AII, B and HDL, LDL, VLDL with Polyurethane and Polyurethane-PEO Surfaces R.M. Cornelius,†,‡ J. Macri,‡ K.M. Cornelius,§ and J.L. Brash*,†,∥ †

Department of Chemical Engineering ‡Department of Pathology & Molecular Medicine §Department of Biology ∥School of Biomedical Engineering McMaster University Hamilton, Ontario Canada S Supporting Information *

ABSTRACT: The lipoproteins (HDL, LDL, VLDL) are important components of blood present in high concentration. Surprisingly, their role in blood-biomaterial interactions has been largely ignored. In previous work apolipoprotein AI (the main protein component of HDL) was identified as a major constituent of protein layers adsorbed from plasma to biomaterials having a wide range of surface properties, and quantitative data on the adsorption of apo AI to a biomedical grade polyurethane were reported. In the present communication quantitative data on the adsorption of apo AI, apo AII and apoB (the latter being a constituent of LDL and VLDL), as well as the lipoprotein particles themselves (HDL, LDL, VLDL), to a biomedical segmented polyurethane (PU) with and without an additive containing poly(ethylene oxide) (material referred to as PEO) are reported. Using radiolabeled apo AI, apo AII, and apoB, adsorption levels on PU from buffer at a protein concentration of 50 μg/mL were found to be 0.34, 0.40, and 0.14 μg/cm2 (12, 23, and 0.25 nmol/cm2) respectively. Adsorption to the PEO surface was 96% of the adsorbed apo AI was eluted under these conditions. In contrast, however, it was found that the elutability of the lipoproteins was much lower, particularly from the PEO material (90% compared to the

Table 1. Adsorption of apo AI, AII, and B from a 50 μg/mL Single Protein Solution, to PU and PEO, Data are Mean ±SD, n≥8 protein

adsorption to PU (μg/cm2)

adsorption to PEO (μg/ cm2)

adsorption to PU (ρmols/ cm2)

adsorption to PEO (ρmols/ cm2)

Apo AI Apo AII Apo B

0.34 ± 0.03 0.40 ± 0.01 0.14 ± 0.01

0.02 ± 0.01 0.01 ± 0.002 0.01 ± 0.004

11.98 ± 1.09 23.20 ± 0.57 0.24 ± 0.02

0.56 ± 0.17 0.34 ± 0.11 0.02 ± 0.01

concentration of 50 μg/mL, a significant quantity (0.14 ± 0.01 μg/cm2) of apo B was adsorbed to the PU surface, and similarly to apo AI and AII, a large reduction in adsorption (>90%), was observed for the PEO surface. Lipoprotein Adsorption from Buffer to PU and PEO. Data on the adsorption of HDL, LDL, and VLDL from buffer solution to the PU and PEO surfaces are shown in Figure 2. The data are in terms of total lipoprotein (TLP) based on the known protein concentration as provided by the supplier and an average protein content by weight of the lipoproteins (Table S2). 12089

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Figure 2. Adsorption of lipoproteins from TBS (single lipoprotein solutions) to (a) PU, (◆) HDL, (■) LDL, (▲)VLDL; (b) PEO, (◇) HDL, (□) LDL, (Δ)VLDL. Lipoprotein concentration, 0.010−2.5 mg/mL; adsorption time, 2 h. Means ± SD, n ≥ 8.

Figure 2(a) shows the data for HDL, LDL, and VLDL adsorption from buffer to the PU. Significant quantities were adsorbed and the trend was similar for all three, that is, increasing

and approaching a quasi-plateau with increasing solution concentration. At a concentration of 1.0 mg/mL, the adsorbed quantities of HDL, LDL, and VLDL were 2.06 ± 0.08, 3.21 ± 12090

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Langmuir 0.01, and 4.23 ± 0.09 μg/cm2 respectively. Although it appears that the adsorbed quantities decrease in the order VLDL > LDL > HDL, it should be pointed out that such comparisons, based on mass, are not useful since the adsorbing species are the lipoprotein particles and the HDL, LDL, and VLDL particles differ in density and very considerably in size. The data for the three types are shown together for convenience. Figure 2(b) shows the data for adsorption of the lipoproteins from buffer to the PEO surface. Somewhat surprisingly, in view of the demonstrated protein resistance of this surface, significant amounts of all three lipoproteins were adsorbed. At a solution concentration of 1.0 mg/mL, the adsorbed quantities of HDL, LDL, and VLDL were 4.21 ± 0.12, 2.58 ± 0.07, and 1.64 ± 0.17 μg/cm2, respectively. The order, HDL > LDL > VLDL, is the inverse of that seen for the PU surface. Again a caveat regarding such comparisons is in order due to the density and size differences among the lipoprotein particles. Comparing adsorption on the two surfaces (Table 2) it is seen that HDL adsorption was higher on the PEO than on the PU whereas LDL and VLDL were lower on the PEO than on the PU. Table 2. Adsorption to PU and PEO (μg/cm2) Compared (Data from Figure 1 for Apolipoproteins; from Figure 2 for Lipoproteins) HDL (1 mg/mL) LDL (1 mg/mL) VLDL (1 mg/mL) apo AI (0.25 mg/mL) apo AII (0.25 mg/mL)

PU

PEO

change PEO vs PU, %

2.06 3.21 4.23 0.43 0.45

4.21 2.58 1.64 0.03 0.015

+104 −20 −61 −93 −97

The adsorbed quantities of the lipoproteins are much higher than typically seen for “simple” proteins and the isotherms do not reach saturation at the highest concentration. This may well reflect multilayer formation, though given the broad distribution of dimensions in lipoprotein populations, the conversion of mass to molar quantities is uncertain and it is thus difficult to confirm multilayering based on mass adsorbed. X-ray Photoelectron Spectroscopy (XPS). Lipoprotein adsorption from single component solutions was also investigated using XPS. Survey spectra of the unmodified PU and PEO surfaces showed signals for carbon, nitrogen, and oxygen as expected (data not shown). Since lipoproteins contain phosphorus, albeit at relatively low levels, phosphorus XPS was explored as a means of checking the unanticipated and substantive adsorption of the lipoproteins to the PEO surface. Phosphorus signals were indeed detected on both surfaces after exposure to the lipoproteins. The data in Table 3 from survey spectra, and the high resolution phosphorus spectra in Figure 3 show that the signals were stronger for PEO than for PU after exposure to HDL. The phosphorus content of the layers estimated from these data is of the order of 0.1 atom %. To give some context, spectra were obtained of relatively thick layers of

Figure 3. High resolution XPS spectra of phosphorus: (a) PU, (b) PEO.

HDL that were deposited on the surfaces by drying down HDL solution. The P content of these layers was found to be on the order of 0.3 atom %. If these layers are considered to be pure HDL from the XPS sampling point of view, then it may be concluded that the phosphorus signal seen in the adsorption experiments represents a substantial uptake of lipoprotein. It was also found by XPS that the nitrogen content of the PEO surface following exposure to HDL increased from 4.22% to 5.81% (Supporting Information Table S4). Taken together, the XPS and labeled lipoprotein experiments indicate that HDL was adsorbed in significant quantity to both the PEO and PU surfaces.

Table 3. XPS Data for HDL Adsorbed to PU and PEO: Phosphorus Content (Atom Percent) At Takeoff Angles of 90 and 20° material

90° takeoff angle

20° takeoff angle

PU PEO

0.09 0.13

0.06 0.12 12091

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Langmuir Immunoblotting. The PU and PEO surfaces were exposed to single component lipoprotein solutions for 2 h at room temperature. The adsorbed proteins were then eluted with SDS and subjected to SDS-PAGE and immunoblotting using antiapolipoprotein antibodies. Figure 4 shows gold-stained SDS-PAGE gels of the three lipoproteins used in this work. The main band in the HDL gel

Figure 5 shows immunoblots of eluates from the surfaces after incubation with single component HDL, LDL, and VLDL solutions. The blots of the HDL eluates are shown in Figure 5 (a) and (b). These were generated using antibodies against apo AI and apo AII respectively, and show that HDL was adsorbed to both surfaces. The adsorbed quantity appears to be greater on the PU than on the PEO surface. This is in contrast to the data from experiments with radiolabeled HDL (Figure 2, Table 2); it should be kept in mind, however, that the blots are based on eluted protein which may not accurately reflect adsorbed protein depending on elutability from a given surface. Figure 5(c) and (d) show blots of LDL eluates using antibodies against apo B and apo E respectively. The blots are positive for these proteins, showing that LDL was adsorbed to both surfaces, again with stronger responses for the PU than for the PEO. Similarly, blots of VLDL eluates using antibodies directed against apo B (Figure 5(e)) and apo E (Figure 5(f)) show that VLDL was adsorbed to both surfaces.

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DISCUSSION Quantitative and qualitative data on the adsorption of apolipoproteins and lipoproteins to a relatively hydrophobic material (water contact angle >100°) and a relatively hydrophilic material (contact angle 60°) are reported in this communication. Significant quantities of apo AI and apo AII were found to adsorb to the hydrophobic polyurethane surface from single component solutions, reaching levels expected for monolayer coverage (∼0.45 μg/cm2). In addition significant quantities of apo B adsorbed to the polyurethane, even at low solution concentration

Figure 4. Gold stained SDS-PAGE gels (10−20% gradient) of HDL, LDL, and VLDL.

corresponds to apo AI (molecular weight 28.2 kDa), which accounts for ∼50% of the mass of the HDL particle. Apo B (550 kDa) is seen in the LDL and VLDL gels (Figure 4).

Figure 5. Immunoblots of eluates from PU (Lanes 1 and 2) and PEO (Lanes 3 and 4) surfaces after exposure to (a) HDL (anti-apo AI antibody); (b) HDL (anti-apo AII antibody); (c) LDL (anti-apo B antibody); (d) LDL (anti-apo E antibody); (e) VLDL (anti-apo B antibody); (f) VLDL (anti-apo E antibody). 12092

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Langmuir (50 μg/mL). The hydrophilic material, containing a PEO additive, adsorbed minimal quantities of apo AI, apo AII, and apo B (90% compared to the PU. The tendency to adsorb to the PEO surface increased with decreasing particle size, that is, VLDL < LDL < HDL. This apparent dependence on size could be related to the more limited ability of the bigger particles to access appropriate binding sites in the surface layers. Differences in surface properties of the particles could also account for the differences in adsorption to PEO. The structure of lipoproteins is complex and is known in some detail, especially that of HDL.45,46 In a general sense the particle surfaces are composed of phospholipid bilayers with embedded apoproteins which solubilize the particles in aqueous systems. Given the differences in the types and relative amounts of protein and lipid among the lipoprotein classes it is likely that there are differences in surface hydrophobicity from class to class (and even within classes); information on such surface properties appears, however, to be lacking. In the XPS data (Figure 3, Table 3) the phosphorus signals provide clear evidence that HDL adsorbed to the PEO as well as to the PU surface. The relative atomic concentrations of 0.09% and 0.13%, respectively, on PU and PEO are in accord with the radiolabeling data showing greater adsorption on the PEO than on the PU. These concentrations may appear low, but should be seen in relation to a value of 0.34% found for a layer of HDL deposited directly on PU from a concentrated solution; it is reasonable to assume that the spectrum of this layer reflects the composition of pure HDL. For the adsorbed layers, the underlying substrate as well as the adsorbed material will be sampled, causing a reduced P content compared to pure HDL.47 The XPS and radiolabeling data are thus in agreement, both indicating extensive interactions of the lipoproteins with the PEO surface. Immunoblots of the proteins eluted from the surfaces after contact with lipoprotein suspensions, on the other hand, suggest that adsorption to the PEO surface is generally less than to the PU (Figure 5); this is true for HDL, LDL, and VLDL. However, it must be kept in mind that the immunoblots represent eluted proteins and that the quantities elutable will be dependent on the properties of the underlying surface. As reported above it was found that elutability of the lipoproteins from the PEO was only about 20%. Therefore, it does not seem valid to draw conclusions regarding adsorbed quantity from these data; they provide qualitative indications only. Taken together, the results of this study suggest that the PEOmodified surface is strongly resistant to apolipoproteins but not to lipoproteins. In support of the latter conclusion, Feng et al. showed that HDL adsorbed significantly to hydrophilic as well as hydrophobic surfaces.32 Also the adsorption of lipoproteins to antifouling polymer surfaces, including surfaces based on poly(oligoethylene glycol) methacrylate (POEGMA), a PEOrelated material, has been reported,48 and investigations of plasma interactions with PEGylated nanoparticles showed that apo B, apo E, apo AI, and apo AII were present in the protein corona adsorbed to the nanoparticles.49 Riedel et al. have recently demonstrated that apo AI, apo B, and apo E are present in the human blood plasma deposits on PEG based surfaces.50 One can speculate that the presence of these proteins on the PEG based surfaces are due, at least in part, to the adsorption of HDL, LDL, and VLDL. The present work focuses on the adsorption of apolipoproteins and lipoproteins from buffer and provides information on a 12093

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fundamental nature. The adsorption of these species from plasma and blood is of more practical interest, for example, for implantable devices such as stents and extracorporeal systems such as hemodialysis. Given that lipoproteins are present in relatively high concentration, it is to be expected that they will be significant components of the layers adsorbed from blood and plasma, and indeed this has been found to be the case in several studies.32,39,41,48,50 Interestingly Gunkel and Huck48 found that lipoproteins adsorb substantially to hydrophilic polymer brushes and are major fouling proteins on these reputedly nonfouling surfaces. Given the findings of the present work, the importance of lipoproteins in cardiovascular disease processes and recent suggestions that HDL “coatings” on surfaces may provide antithrombogenic activity and facilitate endothelial cell attachment,37,51 it is clear that more work to elucidate lipoprotein− surface interactions and to explore lipoprotein-modified surfaces for blood contacting applications is warranted.

SUMMARY AND CONCLUSIONS The interactions of plasma lipoproteins and their protein components, the apolipoproteins, with two polyurethane surfaces have been investigated. One polyurethane was a conventional unmodified material and the other was a blend of the unmodified material with a PEO-containing copolymer. Using radioiodine labeling methods it was shown for the apolipoproteins (apo AI, apo AII, and apo B) that approximate monolayer quantities were adsorbed to the unmodified polyurethane, whereas vanishingly small quantities were adsorbed to the blend surface, thereby confirming the strong protein resistance of the PEO surface. For the lipoproteins (HDL, LDL, and VLDL) significant quantities were adsorbed to both surfaces. X-ray photoelectron spectroscopy data confirmed that the lipoproteins adsorbed significantly to the PEO-containing blend. Immunoblots of the eluted lipoproteins suggested that adsorption to the blend was relatively low and less than on the unmodified polyurethane, however elution of adsorbed material was also less complete on the blend than on the unmodified polyurethane. On the balance of the evidence it is concluded that the PEO surface is resistant to the adsorption of the apolipoproteins but less so (LDL, VLDL) or not at all (HDL) to the lipoproteins themselves. ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.5b02688. Tables S1−S4 (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Phone: (905) 525-9140; fax: (905) 521-1350; e-mail: brashjl@ mcmaster.ca. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS Financial support from the Natural Sciences and Engineering Research Council (NSERC) of Canada is gratefully acknowledged. Helpful discussions with Dr. Bernardo Trigatti are also acknowledged. 12094

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