Cholesteryl Hemisuccinate Monolayers Efficiently ... - ACS Publications

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Cholesteryl hemisuccinate monolayers efficiently control calcium phosphate nucleation and growth Doreen Hentrich, Gerald Brezesinski, Christian Kübel, Michael Bruns, and Andreas Taubert Cryst. Growth Des., Just Accepted Manuscript • DOI: 10.1021/acs.cgd.7b00753 • Publication Date (Web): 29 Sep 2017 Downloaded from http://pubs.acs.org on October 11, 2017

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Crystal Growth & Design

Cholesteryl

hemisuccinate

monolayers

efficiently

control

calcium phosphate nucleation and growth Doreen Hentrich 1, Gerald Brezesinski 2, Christian Kübel 3, Michael Bruns 4 and Andreas Taubert 1,* 1

Institute of Chemistry, University of Potsdam, D-14476 Potsdam, Germany

2

Max Planck Institute of Colloids and Interfaces, D-14476 Potsdam, Germany

3

Institute of Nanotechnology (INT) and Karlsruhe Nano Micro Facility (KNMF), Karlsruhe Institute of Technology (KIT), D-76344 Eggenstein-Leopoldshafen

4

Institute of Applied Materilas (IAM) and Karlsruhe Nano Micro Facility (KNMF), Karlsruhe Institute of Technology (KIT), D-76344 Eggenstein-Leopoldshafen

* Author to whom correspondence should be addressed: E-Mail: [email protected], Tel.: +49-331-977-5773; Fax: +49-331-977-5055; web: www.taubert-lab.net

Abstract: The article describes the phase behavior of cholesteryl hemisuccinate at the air-liquid interface and its effect on calcium phosphate (CP) mineralization. The amphiphile forms stable monolayers with phase transitions at the air-liquid interface from a gas to a tilted liquidcondensed (TLC) and finally to an untilted liquid-condensed (ULC) phase. CP mineralization beneath these monolayers leads to crumpled CP layers made from individual plates. The main crystal phase is octacalcium phosphate (OCP) along with a minor fraction of hydroxyapatite (HAP), as confirmed by X-ray photoelectron spectroscopy, energy dispersive X-ray spectroscopy, bright field transmission electron microscopy, and electron diffraction.

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Keywords: biomineralization; calcium phosphate; amphiphile monolayer; air-liquid interface; cholesteryl derivate, cholesteryl hemisuccinate.

1. Introduction Nature combines soft organic scaffolds with hard inorganic deposits such as CaCO3 (CC), SiO2, or calcium phosphate (CP) to generate hybrid materials with properties such as high mechanical strength.1–5 Although some biological strategies for biomaterial formation are known, the transfer of these principles to the laboratory or to a large-scale process is still a challenge.6–10 CP is of particular interest to humans because it is the inorganic component of human bones and teeth; on the other hand, the mineralization of calcium minerals also causes diseases like stone formation, arteriosclerosis, dental calculus, etc.11 The common principle of all processes, wanted or unwanted, is that they involve a balance between mineral precipitation or crystallization and


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dissolution. A better understanding of CP nucleation, growth, and dissolution is therefore instrumental to design artificial bones or teeth and to treat diseases like arteriosclerosis. So far CP mineralization in the laboratory was predominantly studied in bulk solution,12–20 which is surprising because biological mineralization often occurs at interfaces.21,22 Monolayers at the air-liquid interface are therefore good models to study crystal nucleation and growth. Low molecular weight amphiphiles and amphiphilic block copolymers were therefore used to investigate the formation of inorganics at the air-liquid interface,13,23–36 including CP.37–44 Although the work on interface-controlled CP mineralization is still quite limited, several publications have shown an impressive diversity in the CP deposits, depending on the interface chemistry and specific mineralization conditions.8,12,37–40,43,44 Casse et al. used poly(n-butyl acrylate)– block–poly(acrylic acid) (PnBuA-PAA) monolayers as mineralization template and observed the most efficient mineralization at high pH, where the polymer is deprotonated and the monolayer thus is highly charged.37 Generally, there are more studies on negatively charged additives.39,40,45 This is likely due to the fact that proteins associated with CP biomineralization are rather acidic and research has therefore concentrated on emulating the effects of these proteins with anionic polymers.5,46 Only a few studies address the effects of polycations on CP mineralization at the air-liquid interface. These studies confirm a strong influence of the surface charge on mineral formation.38,43,44 Besides polymeric amphiphiles, lower molecular weight amphiphiles have also been studied for CP mineralization.39,40,45 Moreover, we have previously shown that cholesteryl-based dendritic amphiphiles are efficient growth modulators for CP formation.47 The current study focuses on the effects of a related, but non-dendritic, cholesteryl hemisuccinate amphiphile monolayer for CP mineralization. The reason for choosing this particular amphiphile is that it enables the direct comparison of the role of a dendritic hydrophilic head group with a single carboxylate on CP mineralization while not changing the hydrophobic block. ACS Paragon Plus Environment


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2. Results 2.1. Phase behavior of the amphiphile at the air-liquid interface Cholesteryl hemisuccinate (CHOL-HEM) contains a hydrophobic cholesteryl unit and a hemisuccinate unit with a free carboxylic acid as the hydrophilic segment (scheme 1).

Scheme 1. The CHOL-HEM amphiphile. Mw = 486.73 g/mol.

Figure 1 shows the pressure-area (π-A) isotherms recorded at 10, 20, and 30 °C. The isotherms exhibit a kink between 17.5 and 20.5 mN/m, which is caused by a change in compressibility. The isotherm is similar to that of a liquid-condensed (LC) phase in equilibrium with a gas phase already at 0 mN/m.48–59 The first-order phase transition between the gas and liquid condensed phase is finished at a mean molecular area (MMA) of about 50 Å2 at all temperatures. A further compression leads to a strong increase in the surface pressure indicating the existence of a LC phase. On further compression a kink (second-order phase transition) appears. This kink may indicate a transition from a tilted (TLC) to a untilted liquid-condensed (ULC) phase.60,61 The slope above the kink is steeper than below indicating a lower compressibility in the ULC phase. This is similar to monolayers of long-chain fatty acids which are more compressible in the tilted state.61 Table 1 shows ACS Paragon Plus Environment

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that the kink shifts to lower surface pressures and higher MMAs with increasing temperature. Once the phase transition to the ULC phase is complete, the MMA remains almost constant (even if the film is compressed further) until the film collapses. The film collapse shifts to higher MMAs with increasing temperature (table 1).

ULC

TLC

Figure 1. π-A isotherms of the amphiphile at the air-liquid interface at 10, 20 and 30 °C.

Table 1. Position of the kink (second-order transition from the TLC to the ULC phase) and film collapse at 10, 20, and 30 °C. For each temperature, at least two isotherms were recorded. The isotherms obtained at the same experimental condition overlay perfectly. The lateral pressure is determined with an uncertainty of ± 0.1 mN/m and the MMA with ± 3%. Temperature [°C]

10

20

30

Kink position: MMA [Å2]

36.5

38.1

39.0

Kink position: surface pressure [mN/m]

20.5

19.9

17.5

2

Collapse: MMA [Å ]

33.3

35.4

36.3

Collapse: surface pressure [mN/m]

43.4

40.1

38.0

To evaluate the film stability three successive compression/expansion curves were recorded on pure water at 10 and 20 °C. All compression/expansion experiments were performed up to 15 mN/m



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(TLC phase) or to 35 mN/m (ULC phase), figure 2. At both temperatures, a strong hysteresis is visible in the isotherms. Hysteresis indices (HI1N)62 show that the re-expansion from the TLC phase leads to a less pronounced hysteresis than the expansion from the ULC phase at both temperatures, table 1. The shift between the first and the third compression/expansion cycle (HI13) is much smaller for the expansion from 15 mN/m than for the expansion from 35 mN/m. At 10 °C, HI13 determined for the expansion from the TLC phase (15 mN/m) is ca. 1.8 times smaller than HI13 determined for samples compressed to the ULC phase (35 mN/m). Similarly, at 20 °C, HI13 determined for the expansion from the TLC phase (15 mN/m) is ca. 1.7 times smaller than HI13 determined for samples compressed to the ULC phase (35 mN/m). Moreover, the compression/expansion cycles at 10 °C show a much more pronounced hysteresis than at 20 °C.

Figure 2. Compression/expansion curves of the amphiphile (a) at 10 °C and (b) at 20 °C.


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Table 2. Hysteresis indices for continuous compression/expansion cycles to a surface pressure of 15 mN/m (TLC phase) and 35 mN/m (ULC phase) (HI1N = (A1-AN)/A1). A1, A2, and A3 are the average areas per molecule in the 1st, 2nd, and 3rd compression/expansion cycle. T

π

1. cycle 2

2. cycle 2

3. cycle 2

Hysteresis index

Hysteresis index

[°C]

[mN/m]

A1 [Å ]

A2 [Å ]

A3 [Å ]

HI12

HI13

10

15

39.2

38.1

36.9

0.028

0.059

35

33.6

31.7

30.0

0.057

0.107

15

42.0

41.4

40.4

0.014

0.038

35

36.8

35.5

34.3

0.035

0.068

20

In contrast to the temperature, the subphase pH only weakly affects the behavior of the amphiphile (figure 3). Between pH 5 and 10, gas and liquid-condensed phases coexist at ca. 0 mN/m. The plateau of the first-order phase transition terminates at around 50 Å² between pH 5 and 10. A further film compression leads to a TLC and finally ULC phase as described above.48– 59

The film collapse shifts to higher surface pressures with increasing pH: from 43 mN/m (pH 5)

to 45 mN/m (pH 10). On pure water, the film collapses at 40 mN/m.

Figure 3. π-A isotherms of the amphiphile on water (pH 5.5) and on subphases with different pH at 20 °C. ACS Paragon Plus Environment


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We have previously used calcium concentrations of 2, 20, and 200 mM for CP mineralization.47 The reason for using higher concentrations than in other studies43–45 is the higher amount of CP available for further analysis. As a result, it is necessary to evaluate the behavior of the amphiphile on calcium-containing subphases, figure 4. All isotherms again show a gas – TLC phase transition, which shifts to lower MMAs with increasing calcium concentration. The coexistence region of the gas and TLC phase on pure water shifts to higher MMAs and terminates at 51 Å². At a calcium concentration of 2 mM the plateau ends at an MMA of 46 Å², at 20 mM at 45 Å², and at 200 mM at 44 Å². After completion of the phase transition, the surface pressure strongly increases. With further film compression again a TLC – ULC phase transition appears (kink), which shifts to lower surface pressures with increasing calcium concentration. At a calcium concentration of 2 mM the film collapses at an MMA of 34 Å² and a surface pressure of 44 mN/m. At a calcium concentration of 20 mM, the collapse takes place at an MMA of 34 Å² and a surface pressure of 45 mN/m. Finally, at 200 mM, the film collapses at 34 Å² and 47 mN/m.


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Figure 4. π-A isotherms of CHOL-HEM at the air-liquid interface at 20 °C on water and aqueous calcium nitrate solutions (2, 20, and 200 mM). Mineralization experiments (see below) were all conducted at 30 mN/m (dashed line), where all monolayers show an identical behavior on the calcium nitrate solutions.

Infrared reflection absorption spectroscopy (IRRAS) was performed to elucidate the origin of the kink (spectra not shown). A band at 1724 cm-1 can be assigned to a C=O stretching vibration of the ester in the cholesteryl hemisuccinate, a band at 1585 cm-1 is caused by the C=C stretching vibration, and the bands between 2360-2340 cm-1 stem from CO2 fluctuations.63 Two bands at 2938 and 2850 cm-1 are caused by the symmetrical and antisymmetrical CH2 stretching vibrations, which is somewhat higher than found in the literature.64 The OH stretching vibration is observed between 3700-3000 cm-1 and is proportional to the effective film thickness.45,65,66 A plot of the amplitude vs. surface pressure (figure 5) shows that the amplitude continuously increases up to a surface pressure of 20 mN/m (the kink in the isotherm). Thereafter, the amplitude is almost constant indicating a constant film thickness.



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Figure 5. Amplitude of the OH stretching vibration vs. surface pressure at 20 °C. The blue lines are a guide for the eye to demonstrate the increasing film thickness in the TLC phase and the constant film thickness in the ULC phase. The intersection of the two lines corresponds to the second-order phase transition from the TLC to the ULC phase at 20 °C (figure 1).

2.2. Calcium phosphate mineralization The subphase pH is one of the key parameters to control the formation of CP.8,12 As a result, the pH during the mineralization was recorded for reactions performed in solutions with calcium concentrations of 2 and 20 mM. Figure 6 shows that the pH of the subphase is between 5.6 and 6.1 in subphases with 2 mM calcium. After injection of the phosphate component (pH 8.0), the subphase pH increases to 7.8 during the first ca. 20 min. Then, the pH slowly decreases to 7.5 after ca. 120 min, somewhat more rapidly to 7.3, and finally to 7.0. The pH curves obtained at a calcium concentration of 20 mM are different. Initially, the pH is between 5.4 and 5.6. Upon injection of the phosphate component, the pH increases to 6.5 within 10


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min. Subsequently, the pH decreases to 5.9 in two broad steps after 24 and 35 min. Finally, the pH slightly decreases to 5.8.

Figure 6. pH evolution during CP mineralization. “0” is the point of phosphate injection. The pH of the subphase before injection was recorded for about 10 min. Every 10th data point is shown and data are averages from three repeats with the corresponding standard deviation.

Further insight into the mineralization was obtained from IRRAS, figure 7. For both calcium concentrations (2 and 20 mM), an increase in the P-O stretching vibration at 1018 cm-1 can be observed with increasing mineralization time (figure 7c). At a calcium concentration of 2 mM, the first signal at 1018 cm-1 is visible after ca. 148 min. Until 172 min the amplitude is constant and then steadily increases until the end of the reaction at 302 min. The spectra recorded during mineralization on 20 mM subphases show a first phosphate band after ca. 40 min, which is followed by a slight increase within the next 36 min. This initial, rather weak increase is followed by a strong increase in band intensity between 76 and ca. 120 min. Finally, the intensity levels off and remains constant until the end of the reaction. Moreover, besides the band at 1018 cm-1, the spectra of samples grown on the 20 mM subphases show two additional bands at 960 and 1126 cm-1. These bands appear after 88 min, which



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roughly coincides with the beginning of the steepest increase in the signal intensity of the band at 1018 cm-1. The two new bands are also associated with CP formation. The band at 1126 cm-1 can be assigned to a triply degenerate antisymmetric ν3 (O-P-O) stretching vibration in PO43- and the band at 960 cm-1 to a symmetric ν1 (O-P-O) stretching vibration in PO43-.67,68 Due to the nature of the IRRAS experiment, the spectra are only recorded from a small area (a few mm2). Nevertheless, all data show that the intensity of the P-O stretching vibration increases for both calcium concentrations over the course of the mineral formation reaction and thus prove the association of the phosphate ions with the monolayer followed by the formation of CP.


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Figure 7. IRRA spectra recorded during mineralization at calcium concentrations of (a) 2 and (b) 20 mM. Panel (b) shows the region between 800 and 1400 cm-1 to illustrate the growth of the P-O stretching vibration band. Panel (c) shows the amplitudes of the same band vs. mineralization time.

After 3, 4, and 5 h of mineralization, the films were transferred to Si wafers for X-ray photoelectron spectroscopy (XPS) and atomic force microscopy (AFM), and to copper grids for transmission electron microscopy (TEM). Generally, samples grown at 2 mM are somewhat stiffer and thus easier to transfer than the samples grown at 20 mM. Moreover, the samples grown at 2 mM show wrinkles and reflect the light more strongly than samples grown at 20 mM. Figure 8 shows representative AFM images of all samples. After a mineralization time of 3 h at a concentration of 2 mM dense crumpled thin layers are visible. The same features are observed after 4 h, but they are less aggregated. The same general morphology is also present after 5 h with again densely aggregated layers. The surface roughness is around 69 nm after 3 h, ca. 113 nm after 4 h, and around 32 nm after 5 h. In contrast to the densely mineralized samples with their rather large features formed at calcium concentrations of 2 mM, AFM images of the samples grown at 20 mM show small particles with rather large empty spaces between individual particles or aggregates. The objects are quite different from the morphologies observed via electron microscopy (figures 8 and 9 below). This is likely due to difficulties with film transfer of the samples grown on 20 mM subphases because these films are much softer than the films grown at 2 mM. Some of the features observed in the AFM could therefore result from sample disruption during film transfer. The fact that the images obtained after 4 h are quite different from the other images suggests that there are lateral inhomogeneities in the film during mineralization. Brewster angle microscopy (BAM) could in principle show these inhomogeneities but the films do not show BAM contrast. As a result, a comment on the presence or absence of such inhomogeneities is not possible. ACS Paragon Plus Environment


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Figure 8. AFM images of CP films obtained after 3, 4 and 5 h of mineralization.

Scanning transmission electron microscopy (STEM, Figure 9) confirms the morphology observed by AFM (figure 8). STEM images of samples mineralized at calcium concentrations of 2 mM for 3 and 5 h show crumpled thin layers consisting of individual plates closely resembling the features observed in AFM. The features observed after 3 h are smaller than those observed after 5 h. At higher calcium concentrations of 20 mM the crumpled thin layers appear more densely stacked. However, it may again be possible that the material morphologies are affected by film transfer.


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Figure 9. STEM images of samples mineralized at calcium concentrations of 2 and 20 mM for 3 and 5 h. Note the different magnification for the sample grown at 20 mM and 5 h.



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Figure 10 shows bright field transmission electron microscopy (BF TEM) images and selected area electron diffraction (SAED) patterns of some materials. The images mostly show plates that sometimes stand upright; these plates exhibit 2-6 lattice fringes with distances of 1.7-1.8 nm. They can be attributed to the {100} lattice planes in octacalcium phosphate (OCP, ICSD 27050). The SAED patterns show that the crumpled thin layers (figure 10c) exhibit strong reflections at 3.91, 3.43, 2.84, 2.33, 2.24, 2.06, 1.05, and 1.72 Å (figure 10d). Most of these reflections can be assigned to OCP (ICSD 27050) with a preferential orientation close to [110]. Possibly there is also a small fraction of HAP in these samples as the diffraction pattern is very similar to previous data.47


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Figure 10. (a) Bright field TEM image and (b) enlarged view of OCP plates standing upright. (c) Defocused area of the crumpled layers and (d) corresponding SAED pattern. Results obtained from the other products are essentially identical.

Some samples could be investigated using energy dispersive X-ray spectroscopy (EDXS, figure 11). In all cases where EDX spectra were obtained, an identical Ca/P ratio of ca. 1.33 is found. Typically, this ratio is associated with OCP,69 consistent with SAED and BF TEM.

Figure 11. Average Ca/P ratios and standard deviation from EDXS measurements. Samples mineralized at 20 mM and 5 h do not show EDX spectra of a quality that can be analyzed. The gray shaded area and the colored lines represent the Ca/P ratios of ACP, HAP, OCP, and DCPD.69

Figure 12 shows the Ca 2p and P 2p XP spectra obtained from samples mineralized at calcium concentrations of 2 and 20 mM during 5 h. The spectra show again that the transfer is better for films obtained at lower calcium concentrations because the signal-to-noise ratio in the corresponding XP spectra is much better. Consequently, only spectra obtained with samples mineralized at 2 mM can be analyzed quantitatively for both the calcium and the phosphate content.



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The binding energies obtained from the XP spectra of the materials formed at a calcium concentration of 2 mM are 347.4 eV for Ca 2p3/2 and 133.1 eV for P 2p3/2. These values confirm the presence of CP.45,70 This observation applies to all samples grown with a subphase concentration of 2 mM. For the samples mineralized over 5 h the Ca/P ratio is 1.32. The Ca 2p XP spectra obtained from samples mineralized at a calcium concentration of 20 mM are difficult to analyze for the following reasons: (1) the spectra are noisy, (2) the phosphorus content is very low, (3) the P 2p region overlaps with a strong Si plasmon.45 Nevertheless, the successful mineralization even at higher calcium concentrations is proven by the non-disturbed Ca 2p peak. Four additional components could be determined in the C 1s spectral region at 285.0 eV (C-H), 286.5 eV (C-O), 287.6 eV (C=O), and at 289.0 eV (COO). These signals prove the presence of the amphiphile in the film.71

Figure 12. Ca 2p (left) and P 2p (right) XP spectra of films mineralized at calcium concentrations of 2 mM (top) and 20 mM (bottom).


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2.3. Discussion The amphiphile used in the current study forms stable monomolecular films at the air-liquidinterface and on subphases with different calcium concentrations (figure 1-4). Unlike an earlier example,47 the phase behavior of the amphiphile is only very weakly affected by temperature. The fact that the coexistence region at nearly zero pressure is not temperature-dependent indicates that directly after spreading a liquid-condensed phase is present. This liquid-condensed phase coexists with a gas phase. The transition pressures of re-sublimation processes are usually not temperature-dependent. This behavior has been reported several times for other amphiphiles.48–59,72 IRRAS data confirm that the kink in the isotherms is caused by the phase transition from the TLC to the ULC phase. Below the kink, the film thickness increases because the tilted hydrophobic block of the individual amphiphile molecules is increasingly erected with further film compression. After the kink, the hydrophobic blocks of the amphiphile molecules are upright and the film thickness does not change anymore upon compression. Such TLC-ULC phase transitions have been described before,54,73–77 for example for ethylene glycol mono-n-alkyl ethers77 and for fatty acids.54 Similar to pentadecanoic acid,54 CHOL-HEM shows a shift in the kink to higher MMAs and lower surface pressures with increasing temperature. This is caused by an increasing mobility and chain flexibility of the molecules with rising temperature enabling the molecules to undergo the TLCULC phase transition more easily. The film collapse shows the same behavior and shifts to higher MMAs and lower surface pressures with increasing temperatures. A further explanation for the decreasing film stability with increasing temperature may be found in the increasing dehydration of the hydrophilic head group with increasing temperature.78,79 The dehydration of the head group leads to a higher overall hydrophobicity, which in turn leads to a less stable monolayer due to less contact of the amphiphiles with the subphase. As stated in the results section, the pH of the subphase only has a minor influence on the phase behavior of the amphiphile. This is consistent with data on dipalmitoylphosphatidic acid (DPPA);72 in ACS Paragon Plus Environment


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DPPA attractive van der Waals interactions between the alkyl chains and hydrogen bonds between the phosphate head groups lead to highly ordered phases at room temperature. Therefore, at high MMAs a gas and a liquid-condensed phase coexist in DPPA and in CHOL-HEM. Similarly, Zhang et al.72 did not observe a difference in the phase behavior below a subphase pH of 10 and showed that DPPA is mainly neutral with only a few deprotonated head groups. There are thus two competing interactions: (1) repulsive forces between charged head groups and (2) attractive hydrogen bonds. With rising pH, the repulsive forces between the head groups increase, the molecules are in less close contact, and consequently, the kinks in the isotherm should shift to higher MMAs. However, as protonated and deprotonated groups still coexist, hydrogen bonds still exist as well. Consequently, the existence of attractive hydrogen bonds should lead to a shift to lower MMAs. Below pH 10, the two effects cancel one another and the resulting isotherms are almost identical. Similar to the results by Zhang et al.72 the neutral species, which exhibits significant hydrogen bonding, probably dominates as well, especially at lower pH. The strong hydrogen bonding leads to a dense molecular packing within the monolayer. With increasing deprotonation by increasing pH, a higher number of negative charges is introduced in the monolayer, which initially may favor the formation of additional hydrogen bonds. Only at pH 10 or higher, electrostatic repulsion between the carboxylate groups dominates and destabilizes the films. Consistent with literature, we presume that the pH at the interface is lower than in the subphase. For example, the pH of a stearic acid monolayer is four pH units lower that of the bulk solution.80 This observation further supports our observations that up to a pH of 9, the film behavior is essentially identical. A rise of the collapse pressure with increasing pH is therefore probably caused by a higher number of deprotonated species. To counteract the rising repulsive forces more energy is necessary for compression; this finally leads to the observed higher collapse pressure with increasing pH. In contrast to the subphase pH, the calcium concentration affects the phase behavior of the amphiphile. This has already been observed for amphiphiles like phospholipids72,81–85 and fatty ACS Paragon Plus Environment

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acids52,56,59,86. For example, Tang et al.59 analyzed the influence of Ca2+ at concentrations of 0.1 and 0.3 M on the phase behavior of palmitic acid by vibrational sum frequency generation spectroscopy (VSFG). At 0.1 M Ca2+ the predominant binding is between two COO- groups and one Ca2+. The bridging complex converts to a certain extent into a bidentate chelate complex (1 Ca2+:1 COO-). At 0.3 M Ca2+ only the 2:1 bridging complex (2 Ca2+: 1 COO-) exists, independent of the time given for structural reorganization (figure 13).

Figure 13. Presumed formation of different calcium complexes at the air-liquid interface. (a) Formation of a bidentate chelate and (b) of a bridging complex. R-COO stands for carboxyl group and M for metal ion (for example Ca2+), adapated from ref.59

In contrast to the results by Tang et al., the current study shows no evidence of a disappearing TLC-to-ULC phase transition. The phase transition pressure decreases with increasing calcium concentration up to 0.2 M. The MMA in the ULC phase is clearly smaller on calcium-containing subphases than on water but increasing calcium concentrations do not lead to a disappearance of the phase transition. Presumably, even higher calcium concentrations are necessary to achieve this. However, as one of the goals of the current study was the investigation of CP mineralization at suitable conditions, we did not study this phenomenon further. As discussed so far, the shifts observed in the isotherms and the film stabilities depend on a multitude of (often counteracting) effects such as electrostatic repulsion and complex formation at the interface. On one hand, the deprotonated carboxylic acid groups of the amphiphile can form complexes with Ca2+, yielding a denser packing of the amphiphiles.59 Hydrogen bonding between individual ACS Paragon Plus Environment


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amphiphiles may further enhance this effect. As a result, the corresponding phase transitions shift to lower MMAs. With increasing calcium concentrations, the ionic strength and the number of deprotonated carboxyl groups increase. This means that the attractive interactions via calcium complexation and the corresponding bridging effects become stronger. At a calcium concentration of 2 mM probably not all carboxyl groups are deprotonated and the degree of bridging is lower than that at higher calcium concentrations. It would be further conceivable that with increasing calcium concentration also deprotonated carboxyl groups form bridges over a greater distance and not only between adjacent carboxyl groups. This would result in a smaller MMA with increasing calcium concentration. Such a bridge formation improves the film stability and shifts the collapse to higher surface pressures. In conclusion, the higher the degree of bridging, the more stable the film and the higher the collapse pressure. Finally, the compression/expansion curves (figure 2) show much lower hysteresis at higher temperatures. Probably, the reason for the more pronounced hysteresis at lower temperatures is the lower thermal motion of the molecules. At higher temperatures, the more mobile molecules can respond more quickly and reorganize faster than at lower temperatures. The hysteresis for the expansion of the ULC phase is more pronounced than the hysteresis for the expansion of the TLC phase. It is therefore difficult to transfer the film from the ULC back to the TLC phase. Likely, there are two reasons for this behavior: (1) strong attractive van der Waals forces in the ULC phase, (2) an additional delay in the reorganization because at higher compression the monolayer must undergo a ULC-TLC phase transition during film expansion. Indeed, there are several examples showing that the surface pressure to which the monolayers are compressed is important for the observation of such a hysteris.57,87 The occurrence of the hysteresis can also be explained by a small material loss either by dissolution of some amphiphile molecules in the subphase or the formation of small 3D crystals87–89 (although there is no evidence in the BAM experiments for


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crystallization). Finally, intermolecular hydrogen bonding during film compression has also been held responsible for hysteresis.90–92 Hydrogen bonding could also explain our observations, because hydrogen bonds are more pronounced at lower than at higher temperatures and therefore the hysteresis at lower temperatures is more pronounced. The hydrogen bonds lead to a bridging of the molecules, which in turn may not have enough time to reorganize during the expansion.90 Possibly, the reorganization of the film during expansion is much slower than the movement of the barriers such that the system is not in equilibrium.89 To induce a local crystal nucleation at the surface, the monolayer must be enriched in calcium and phosphate ions. IRRAS measurements confirm the presence of phosphate ions beneath the monolayer in all experiments; the phosphate concentration at the interface is lower when less phosphate is added (figure 7). The increase of the P-O band intensity suggests that initially phosphate adsorbs to the monolayer and then crystal nucleation and growth occurs. The non-linearity in these data indicates that this is a complex multistep process where phosphate enrichment, formation of the first precipitates, and transformation to the final products strongly overlap. The crystals (figure 8, figure 9, figure 10) are large plates, which aggregate to form crumpled thin layers. Such a morphology is not uncommon, but mostly, these morphologies were obtained from bulk solution and not at the interface.16,18,45,93,94 There are only two examples where these crumpled sheets were observed at the interface.45,47 Consistent with these two studies the main crystal phase obtained in the current study is OCP (figure 10, figure 11, figure 12). Moreover, pH measurements indicate that OCP formation proceeds via several steps because during the formation of ACP, OCP, and HAP protons are released. These proton release steps lead to a decreasing solution pH when a new mineral phase precipitates. Such a process was also observed by Mekmene et al.95 who used the same calcium and phosphate concentration (20 mM) as in the current study. They observed two steps in the pH curve, similar to the current data (Figure 6) and explained ACS Paragon Plus Environment


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this behavior with the formation and dissolution of several intermediates during mineralization. In addition, decreasing saturation of the solution caused by the shift of the equilibrium of the phosphate species from PO43- to HPO42- and finally to H2PO4- with decreasing pH was held responsible by the same authors for this effect. Finally, the same study showed that the pH decreases much more strongly and shifts to lower reaction times and lower pH values with increasing Ca/P ratio in the reaction mixture. A similar multistep process was observed by Ofir et al.93 Such a multistep growth model also matches the current data. The differences in the position of the steps stem from different factors. First, the mineralization in the current study was performed in a trough and thus the mixing by the magnetic stirrer in the dipping well was less effective than, for example, in a beaker. Second, local concentration differences exist in the current system because we used a 3 M (NH4)2HPO4 solution to achieve the final phosphate concentration. Additionally, the airliquid interface is saturated with an amphiphile monolayer rather than with dissolved amphiphiles. The first step in the pH curves is likely due the precipitation of a thermodynamically less stable species like ACP or DCPD. The second step indicates the formation and growth of OCP and thus the dissolution of the first ACP or DCPD species, equations 1 and 2. During OCP formation twice as many protons are released compared to ACP formation. Accordingly, the first step in the pH curve is less pronounced than the second step. After OCP formation, the pH stays almost constant, indicating that OCP does not transform further, e.g. to HAP. This observation is supported by SAED, HRTEM, EDXS and XPS, (figure 10, figure 11, figure 12).

Formation of ACP:

eq. (1)

Formation of OCP:

eq. (2)


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Indeed, the formation of HAP can proceed over several intermediates depending on the reaction conditions. Typically, the first precursor is ACP, which transforms to DCPD or OCP and finally to HAP.12,18,96,97 According to Ostwald,31,98 HAP formation is expected but apparently the monolayer shows a strong enough interaction with the growing minerals to inhibit the OCP-HAP transition. This is consistent with literature showing that polyelectrolytes can inhibit the hydrolysis from OCP to HAP.99–103 Poly(L-glutamate) (PGlu) inhibits the hydrolysis from OCP to HAP much better than poly(L-aspartate) (PAsp); presumably, this hydrolysis proceeds via a layer-to-layer mechanism by splitting to smaller crystals.104 According to the authors of this study, the polyelectrolytes preferentially adsorb to the hydrated layer of the OCP crystal in a [110] orientation; this prevents the splitting of the OCP crystals along the c-axis and thus the hydrolysis from OCP to HAP. PGlu also stabilizes the OCP crystals much better than PAsp because of the additional methylene group. Similar effects have been shown for poly(acrylic acids) of different molecular weights.101 A similar mechanism can also be postulated for the amphiphile used in the current study; possibly, it can adsorb on the OCP [110] crystal face and prevents the hydrolysis to HAP. As pointed out by one of the referees, the CHOL-HEM monolayer should only block one of the faces and the hydrolysis from OCP to HAP could still proceed via the other, free surfaces of the OCP crystals. There is, however, evidence that only one free surface may not be sufficient and that a successful hydrolysis would need to start from two sides of the crystals.105 As a result, the current data appear to support this earlier observation104 and suggest that even partial stabilization of one of the crystal faces may be sufficient to suppress the OCP-HAP phase transition. A previous study using an amphiphile with the same hydrophobic cholesteryl block but with a Newkome type dendron as the hydrophilic segment shows that the control over the mineralization process is similar.47 However, there are two significant differences between the two studies: (1) the current amphiphile appears to be more efficient at preventing the OCP-HAP transformation and (2) the order in the CP deposits found here appears to be lower. For example, HRTEM (figure 10) shows that ACS Paragon Plus Environment


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in the previous study rather extended areas with a high degree of crystallinity formed, while the current study only finds very small regions with a correlated crystallography. This suggests that while the current amphiphile is better at stabilizing the OCP phase, the amphiphile used previously favors the formation of extended crystalline regions with the same crystallographic orientation. We currently assign the better stabilization in the current case to the fact that the number of carboxylate groups per nm2 (and possibly the order in the monolayer) is higher than in the previous case. As a result, similar to a model presented by Bigi and colleagues99–104 there are more functional groups that can efficiently pack and inhibit OCP hydrolysis. In contrast, the earlier amphiphile may better adjust to the growth of HAP and thus favor the formation of extended mineral layers with identical crystallographic orientation.

3. Conclusions Cholesteryl amphiphiles are good models for the investigation of CP mineralization at the soft air-liquid interface.47 The current study expands the platform of cholesteryl-based amphiphiles and demonstrates that both the behavior of the monolayer at the air-liquid interface and the CP mineralization depend on the details of a rather delicate interplay between multiple factors such as (i) charge of the amphiphiles, (ii) the ability of the amphiphiles to form hydrogen bonds, (iii) the presence or absence of metal cations, (iv), the ability of the amphiphiles to complex metal ions and (v) the details of the geometry of the hydrophilic head group.

Acknowledgments. We thank Dr. A. Kopyshev for AFM measurements, ChemAxon LLC for a free license of MarvinSketch v5.12, and the Karlsruhe Micro- and Nano Facility for instrument time (Grant No. 2015-014-007830). Funding by the University of Potsdam, the Max Planck Institute of Colloids and Interfaces, and the Federal Ministry for Economic Affairs and Energy is gratefully acknowledged. ACS Paragon Plus Environment

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Electronic Supporting Information available. Full experimental section is available online at www.XXXXXXX References and Notes (1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11) (12) (13) (14) (15) (16) (17) (18) (19) (20) (21) (22) (23) (24) (25)

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For Table of Contents Use Only

Cholesteryl

hemisuccinate

monolayers

efficiently

control

calcium phosphate nucleation and growth Doreen Hentrich 1, Gerald Brezesinski 2, Christian Kübel 3, Michael Bruns 4 and Andreas Taubert 1,*


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Cholesteryl hemisuccinate monolayers at the water-air interface are efficient tools for controlling the mineralization of calcium phosphate from aqueous solution.


Cholesteryl Hemisuccinate Monolayers Efficiently ... - ACS Publications

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