Surface topography and free energy regulate osteogenesis of stem cells: effects of shape-controlled gold nanoparticles

doi:10.12336/biomatertransl.2021.02.006

Biomaterials Translational ›› 2021, Vol. 2 ›› Issue (2): 165-173.doi: 10.12336/biomatertransl.2021.02.006

• RESEARCH ARTICLE • Previous Articles

Surface topography and free energy regulate osteogenesis of stem cells: effects of shape-controlled gold nanoparticles

Kamolrat Metavarayuth, Esteban Villarreal, Hui Wang, Qian Wang^*()

Department of Chemistry and Biochemistry, University of South Carolina, Columbia, SC, USA

Received:2021-04-05 Revised:2021-06-07 Accepted:2021-06-09 Online:2021-06-28 Published:2021-06-28
Contact: Qian Wang E-mail:Wang263@mailbox.sc.edu

Abstract

Abstract:

The surface free energy of a biomaterial plays an important role in the early stages of cell-biomaterial interactions, profoundly influencing protein adsorption, interfacial water accessibility, and cell attachment on the biomaterial surface. Although multiple approaches have been developed to engineer the surface free energy of biomaterials, systematically tuning their surface free energy without altering other physicochemical properties remains challenging. In this study, we constructed an array of chemically-equivalent surfaces with comparable apparent roughness through assembly of gold nanoparticles adopting various geometrically-distinct shapes but all capped with the same surface ligand, (1-hexadecyl)trimethylammonium chloride, on cell culture substrates. We found that bone marrow stem cells exhibited distinct osteogenic differentiation behaviours when interacting with different types of substrates comprising shape-controlled gold nanoparticles. Our results reveal that bone marrow stem cells are capable of sensing differences in the nanoscale topographical features, which underscores the role of the surface free energy of nanostructured biomaterials in regulating cell responses. The study was approved by Institutional Animal Care and Use Committee, School of Medicine, University of South Carolina.

Key words: biomaterials, gold nanoparticles, osteogenesis, stem cells, surface free energy

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Figures/Tables 7

Table 1 The composition of growth solution mixture and HAuCl4 addition rate for each AuNP

AuNP	L-ascorbic acid	Au seed	0.1 M (1-hexadecyl)trimethylammonium chloride	0.5 mM HAuCl₄ (2 mL) addition rate
Quasi-spherical nanoparticles	0.01 M, 130 μL	10 μL	2 mL	2 mL/h using a syringe pump
Nanotrioctahedra	0.1 M, 100 μL	10 μL	2 mL	1 shot injection (stir simultaneously)
Porous nanoparticles	0.1 M, 10 μL	10 μL	2 mL	1 shot injection (no stir)
Concave nanocube particles	0.1 M, 130 μL	10 μL	2 mL	2 mL/h using a syringe pump

Figure 1. Seed-mediated synthesis of AuNPs with different shapes. Seed particles were first prepared by reduction of Au3+ in a strong reducing agent as the first step. Then the Au3+ growth solution was reduced in weak reducing agent and surfactant to Au+ which was kinetically controlled to grow on seed particles from the first step into gold nanoparticles with different shapes. Slower reduction rates produced AuNPs that were more stable or had lower surface energies such as quasi-nanospheres enclosed by {111} and {100} facets, while faster reaction rates produced high index faceting Au QSNPs with higher surface energies, such as TOH, PNPs, and CCNPs.31, 32 AuNPs: gold nanoparticles; CCNPs: concave nanocube particles; PNPs: porous nanoparticles; QSNPs: quasi-spherical nanoparticles; TOH: nanotrioctahedra.

Figure 2. Characterisation of different-shaped AuNPs. (A) Transmission electron microscopic images of different-shaped AuNPs. The images show that AuNPs were similar in size and monodisperse in term of shape. Scale bar: 100 nm. (B) Particle size analysis of images obtained by transmission electron microscopy. AuNPs: gold nanoparticles; CCNPs: concave nanocube particles; PNPs: porous nanoparticles; QSNPs: quasi-spherical nanoparticles; TOH: nanotrioctahedra. (C) Size distribution of the different-shaped AuNPs analysed by dynamic light scattering. The results of dynamic light scattering showed a monodisperse peak of each shape of AuNPs with similar diameter, approximately 90 nm. (D) Optical extinction spectra of AuNPs reflecting differences in localised surface plasmon resonance.

Figure 3. AuNP-coated substrate analysis. (A) AuNPs were deposited onto ‘piranha’-treated glass cover-slips by electrostatic interaction between positively-charged quaternary amine function groups on AuNP ligands and negatively-charged ‘piranha’-treated glass cover-slips. (B) Atomic force microscopic images show the different shapes of AuNP-coated substrates. The AuNP-coated glass cover-slips exhibited similar coverage of AuNPs on the substrate which was approximately 40﹣50%. (C) Root mean square (Ra) roughness from data collected from atomic force microscopic images. The Ra result revealed no significant difference in microscale roughness among QSNP-, TOH-, and PNP-coated substrates. CCNP-coated substrates showed significantly higher roughness compared to the other surfaces. Data are expressed as mean ± SD. *P < 0.05 based on one-way analysis of variance. AuNPs: gold nanoparticles; CCNPs: concave nanocube particles; CTAC: (1-hexadecyl)trimethylammonium chloride; PNPs: porous nanoparticles; QSNPs: quasi-spherical nanoparticles; TOH: nanotrioctahedra.

Figure 4. AuNP-coated substrate characterisation by contact angle measurement and QCM measurement. (A) AuNP-coated surfaces exhibit higher contact angles compared to an uncoated glass surface. QSNP is the most hydrophilic AuNP-coated surface, followed by gold sputtered surface, TOH-, CCNP-, and PNP-coated substrates respectively. (B) Frequency shifts measured by QCM after incubation of the AuNP-coated QCM probe with cell culture medium. Gold sputtered quartz probe was used as control. Data are expressed as mean (± SD). **P ≤ 0.01 based on one-way analysis of variance. AuNPs: gold nanoparticles; CCNPs: concave nanocube particles; PNPs: porous nanoparticles; QCM: quartz crystal microbalance; QSNPs: quasi-spherical nanoparticles; TOH: nanotrioctahedra.

Figure 5. Cytochemical analysis of the osteogenic differentiation process of rat bone marrow stem cells on control glass, gold-sputtered substrates, and gold nanoparticle-coated substrates at day 2 after incubated in osteogenic media. (A) Alkaline phosphatase activity of cells cultured on different substrates. (B) Optical density at 548 nm of solubilised Alizarin red S staining normalised to cell number indicates the relative deposited calcium quantity at day 5. The mineralisation of cells on QSNP and TOH substrates was significantly higher than that of control glass, gold-sputtered, PNP and CCNP substrates. Data are expressed as mean ± SD (n = 3). *P < 0.05 (one-way analysis of variance followed by multiple comparisons). CCNPs: concave nanocube particles; PNPs: porous nanoparticles; QSNPs: quasi-spherical nanoparticles; TOH: nanotrioctahedra.

Figure 6. Micrographic images of bone marrow stem cells stained with lizarin red S staining of each sample at day 5. Cells on QSNP and TOH substrates are obviously stained for calcium deposition, as illustrated by the deep red colour for calcium of large cell nodules, whereas much weaker staining was observed on gold-sputtered and PNP-coated substrates. The Alizarin red S staining confirms calcium mineralisation of cells on the two substrates. Notably, cells on CCNP substrate only formed small nodules that were also stained with Alizarin red S. Scale bar: 200 μm. CCNP: concave nanocube particle; PNP: porous nanoparticle; QSNP: quasi-spherical nanoparticle; TOH: nanotrioctahedra.

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Surface topography and free energy regulate osteogenesis of stem cells: effects of shape-controlled gold nanoparticles

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