Skip to main content
Download PDF

Arylated gold nanoparticles have no effect on the adipogenic differentiation of MG-63 cells nor regulate any key signaling pathway during the differentiation

BMC Research Notes volume 14, Article number: 192 (2021) Cite this article

Abstract

Objective

MG-63 cells that have osteoblastic and adipogenic differentiation potential were evaluated for internalization, and adipogenic differentiation in the presence and absence of the covalently functionalized aryl gold nanoparticles (AuNPs-C6H4-4-COOH).

Results

Inductively coupled plasma, flow cytometry and confocal microscopy analyses confirmed that gold nanoparticles were easily internalized by MG-63 cells. The MG-63 cells were differentiated into adipocytes without gold-aryl nanoparticles and with the gold-aryl nanoparticles at 5 µM concentration in both induction and maintenance media. The lipid content assay and the relative expressions of PPAR-γ, ADR1, GLUT1 and GLUT4 genes showed no significant variation with and without the gold nanoparticles treatment. Differential phosphorylation levels of 43 kinases phosphorylation sites were evaluated using the human phospho-kinase array to assess the effect of the gold nanoparticles on the signaling pathways during the differentiation. No kinase phosphorylation site was differentially phosphorylated with two or more folds after the nanoparticles treatment after the first day as well as at the end of MG-63 cells differentiation. The gold-aryl nanoparticles do not affect MG-63 cells differentiation into adipocytes neither do they affect any key signaling pathway. These properties make these gold nanoparticles suitable for future drug delivery and medical applications.

Introduction

MG-63 cells are osteosarcoma cells but they have the same differentiation potential as Mesenchymal Stem cells (MSCs). They are the cancer form of osteoblasts. By differentiation, these sarcoma cells regain the early state of MSCs characteristics and for that reason, they may be differentiated into cells of mesodermal origin such as osteoblasts and adipocytes [1, 2]. Studies have shown that MG-63 cells may be differentiated into adipocytes [3, 4].

Recently, we synthesized robust covalently functionalized gold nanoparticles attached through aryl carbon with the structure AuNPs-C6H4-4-COOH (abbreviated as AuNPs-COOH) by the reduction of aryldiazonium-AuCl4 salts [5]. These gold-aryl nanoparticles are robust under different pH conditions. They have shown outstanding biocompatibility. Besides, they are not prone to aggregation under several physiological conditions. Another important fact related to this interesting class of gold nanoparticles is the ability to modify the organic shell to synthesize highly water-soluble bioconjugates which can maintain small sizes in solution [6, 7]. They have shown outstanding biocompatibility and unique applications in DNA stabilization, Bovine Serum Albumin (BSA) delivery, cellular uptake, lysozyme bioconjugation for antibiotic-resistant bacteria and insulin defibrillation [6, 7]. Furthermore, our recent study also shows that these aryl-gold nanoparticles having various protein coats are easily uptaken by MG-63 cells [8]. Unlike the gold nanoparticles that are reported to have citrate shells, gold-aryl nanoparticles have aryl functional groups covalently linked through carbon to the gold core and highly water dispersible which make them ideal for cellular uptake study [5]. A few classes of nanoparticles have been evaluated in stem cells differentiation such as silica nanoparticles and magnetic iron nanoparticles [9, 10]. Size, shell and type may affect the route of stem cells differentiation [9,10,11,12]. Hence, nanoparticles have great therapeutic potential for regenerative medicine [13, 14]

The effect of gold nanoparticles on Mesenchymal Stem Cells (MSCs) differentiation has been reported; however, only one study reported their effect on osteoblastic differentiation of MG-63 cells [15]. Conjugated gold nanoparticles also affect cellular proliferation and differentiation. Since our gold-aryl nanoparticles are unique, we aim to assess the effect of gold-aryl nanoparticles on the adipogenic differentiation of MG-63 cells. Two signaling pathways, mitogen-activated protein (MAP) kinase and p38 kinase, were reported to be regulated by gold nanoparticles during osteoblastic and adipogenic differentiation of MSCs [16, 17]. Our study has focused on screening the regulation of various signaling pathways that may be regulated due to the presence of our unique gold-aryl nanoparticles. A human phospho-kinase array was used to assess the effects of the gold-aryl nanoparticles on the phosphorylation levels of 43 kinases phosphorylation sites. These 43 sites consists of kinases or their protein substrates and they are the components of several key signaling pathways and we aimed to find out which pathways are modulated by the uptake of the gold-aryl nanoparticles by MG-63 cells [18]. To the best of our knowledge, this is the first study that screens several signaling pathways in the presence of covalently functionalized gold nanoparticles during the adipogenic differentiation of MG-63 cells. Any gold nanoparticles that do not affect the cellular processes such as signaling pathways can be used for drug delivery and lineage tracing experiments during embryonic development. However, prior to the application of these aryl-gold nanoparticles in biomedicine, further research is needed to unravel the effects of these nanoparticles in other human cells.

Main text

Methods

Nanoparticles synthesis

The gold nanoparticles were synthesised as previously reported [5]. Briefly, [HOOC-4-C6H4N≡N]AuCl4 (0.031 g, 0.064 mmol) was dissolved in 30 mL of DI water and (0.270 mL, 0.135 mmol) of 9-borabicyclo(3.3.1)nonane (9-BBN) was added dropwise to the salt solution. The reaction was vigorously stirred for 2 h. The nanoparticles formed were purified using a 30 cm length of dialysis tubing cellulose membrane of 25 mm width and AuNPs-COOH stock solution was stored in the refrigerator. 1 mL of AuNPs stock solution was centrifuged at 12,000 g. The nanoparticles pellets were washed with PBS and resuspended in 1 ml of PBS before their use in the differentiation.

Internalization of the aryl gold nanoparticles by MG-63 Cells

Some nanoparticles were tagged with FITC [8]. Afterwards, MG-63 cells were treated with the tagged gold nanoparticles for 24 h. Flow cytometry and confocal microscopy methods were used to confirm the uptakes of the nanoparticles [8].

MG-63 cells were treated with gold-aryl nanoparticles with 5, 10, 20 and 40 µM concentrations for 24 h. Afterwards, the nanoparticles were removed, and the cells were lysed to assess the gold concentration by Inductively coupled plasma spectroscopy (ICP).

MG-63 cell differentiation into adipocytes

To assess the effects of the nanoparticles, the protocol for the differentiation was slightly modified from our previous studies [2, 19]. Briefly, adipogenic differentiation was induced by induction medium I (DMI) containing a combination of 0.5 µM/mL of 3-isobutyl-1-methylxanthine (IBMX) and 0.1 µM/mL Indomethacin, 1 µM/mL insulin (INS), 0.25 µM/mL dexamethasone, 0.1 µM/mL Indomethacin with 5 µM/mL of the gold-aryl nanoparticles in the treated group and without gold-aryl nanoparticles in the control group. After 48 h, the media were changed to differentiation maintenance media II (DMII) containing 1 µg/mL insulin (INS) with 5 µM/mL gold-aryl nanoparticles in the treated group and without nanoparticles in the control group for 48 h. This two-steps adipogenic differentiation protocol was repeated for 3 cycles with a total of 12 days. The derived adipocytes were stained with Oil Red O and Nile Red [19].

Lipid content quantification

Lipid quantification was calculated from the three replicas of treated and control adipocytes [19]. Briefly, Oil Red O stain was eluted with 500 µL of 100% isopropanol at room temperature. Then, 100 μL of the samples were quantified by ELISA at 500 nm absorbance (O.D.) for treated and control adipocytes.

Gene expression study via RT-PCR

Real-time gene expression was performed [19] to assess the effects of the nanoparticles on adipogenic regulatory genes. The primers sequences for the genes are given in the additional file 1. Qiagen rotor gene thermal cycle was used to perform real-time PCR using Go Taq qPCR Master Mix. The results were analyzed using Qiagen rotor gene qPCR software and delta-delta Ct calculation method [20].

Proteome profiler human phospho-kinase array

Adipocytes cells at the end of differentiation as well as cells after 24 h of differentiation with and without the treatment of nanoparticles were subjected to lysis buffer provided by the manufacturer of the array kit (ARY003B, Minneapolis, MN 55413, USA) [21, 22]. Protein concentrations were calculated using Bio-Rad DC Protein Assay kit following manufacturer instructions. A solution of 2.0 mL of diluted cell lysate was incubated on the array overnight at 2–8 °C, followed by washing with Phosphate-buffered saline (PBS) buffer to remove extra proteins. A 1.0 mL of diluted Detection Antibody Cocktail A and B, for part A and B membranes, were incubated for 2 h at room temperature followed by three times washing to remove unbound and extra antibodies on the membrane. One mL of diluted Streptavidin- HRP was added into each well containing membrane for 30 min. Enhanced chemiluminescent detection of the protein blots was photographed using the Bio-Rad Gel Doc system. Quantification and analysis were performed with ImageJ 1.52a software.

Statistical analysis

All experiments were performed in triplicates and results expressed as the means ± standard deviation of the independent triplicate assays. Statistical significance was analyzed using two-tailed T-test considering significance at p-value < 0.05.

Results and discussion

Assessing the internalization of gold nanoparticles

To assess the uptake of gold-aryl nanoparticles by MG-63 cells, the cells were treated with 5, 10, 20 and 40 μM concentrations for 24 h. As the treatment concentration increased, so was the concentration of Au detected per mL of the cell lysate (Fig. 1a).

Fig. 1
figure 1

a ICP Spectroscopy of the gold-aryl nanoparticles. As the treatment concentration of the nanoparticles increases so does the concentrations of gold per mL of the lysate indicating the MG-63 cells uptake the gold-aryl nanoparticles. b Confocal image of a representative MG-63 showing the internalization of FITC-conjugated nanoparticles. Nucleus is stained with DPI. c Representative histograms of FITC-conjugated gold-aryl nanoparticles internalized by MG-63 cells. d The treated cells had high emission and percentage of cells that internalized the gold nanoparticles

Full size image

Gold-aryl nanoparticles were also conjugated with FITC and then they were dissolved in PBS with 5 μM concentration. Confocal microscopy and flow cytometry results indicate that FITC conjugated gold nanoparticles were easily internalized by MG-63 cells (Figs. 1b, c, d). The treated cells had higher fluorescence emission and the confocal microscope images show the gold-aryl nanoparticles accumulated inside MG-63 cells.

Evaluation of the differentiation of MG-63 cells into adipocytes with and without the presence of aryl-gold nanoparticles

The nanoparticles at 5 μM concentration were present in both induction and maintenance media of the three cycles. Differentiation was also carried out without nanoparticles (control). Figure 2a displays representative images of the differentiation. The differentiation was evaluated by lipid content assay which shows that adipogenesis was not affected by the presence of the gold-aryl nanoparticles (Fig. 2b). Differentiation was also carried out with the gold nanoparticles conjugated with FITC to observe and confirm the presence of nanoparticles during the entire differentiation process (Fig. 2c).

Fig. 2
figure 2

a Representative image of MG-63 cells, adipocytes differentiated with and without the gold nanoparticles treatment. b Lipid content assay of three biological replica of differentiation of MG-63 into adipocytes. The lipid assay shows no significant difference between treated and control samples. c Representative images of adipocytes differentiated with and without nanoparticles treatment. Nuclei were stained with DAPI. Adipocytes were stained with Nile red staining. Confocal images of the adipocytes differentiated with and without FITC-conjugated gold nanoparticles. d Real-time PCR of the 5 adipogenic markers. There was no statistically significant variation in the relative expression of these markers in the presence of gold nanoparticles

Full size image

We also evaluated the adipogenic differentiation of MG-63 by the relative expression of specific markers: PPAR-γ, ADR1, GLUT1 and GLUT4 (Fig. 2d). There was no statistically significant differential regulation among these markers in the presence of gold nanoparticles nor was any significant variation in the lipid content.

Evaluation of phosphorylation level of the 43 kinases phosphorylation sites in the presence and absence of aryl-gold nanoparticles

The differential phosphorylation level was studied for different kinases or their protein substrates which are the components of the key signaling pathways. We analyzed the phosphorylation levels of these 43 kinases phosphorylation sites; some of them are in the kinases and other are on their protein substrates. The analysis was carried out by using the phospho-kinase array during the adipogenic differentiation. In this array, selected antibodies against specific phosphoproteins (sites of kinases) were spotted on nitrocellulose [23, 24]. After cells lysates were incubated on the array, a mixture of biotinylated antibodies against the phosphoproteins were applied followed by Streptavidin conjugated with horseradish peroxidase. The array analysis shows that gold-aryl nanoparticles did not regulate any of the major signaling pathways at the two-point interval, 24 h and after 12 days, during the differentiation as the phosphorylation level of none of the sites varied for two or more folds (Fig. 3). The two-fold changes were considered significant variation [25, 26].

Fig. 3
figure 3

a and b Phospho-protein array was performed on lysate after 24 h treatment with gold nanoparticles compared with control (b) during the first day of differentiation. c and d: Phospho-protein array was performed on lysate after end of the differentiation in the presence and absence of gold nanoparticles (d). No phosphorylation site was differentially phosphorylated two or more folds

Full size image

It can be concluded that no kinase or their protein substrates were differentially phosphorylated with the presence of gold nanoparticles. We considered the upregulation and down regulation with two or more folds as significant. Any difference in phosphorylation level is due to the change in chemical and biological environment induced by the addition of gold nanoparticles. This in turn determines the behavior of cells. Analysis of phosphorylation levels of the 43 kinases or their substrates at the end of differentiation indicates that no kinase or their phosphorylation of substrates was differentially regulated at the end of differentiation.

Nanoparticles that regulate signaling pathways will affect cellular behavior and will affect their physiology and biochemistry [27]. Our gold nanoparticles do not have any effects on the cellular signaling pathways and can be used as drug delivery vehicle to cells. Based on this study, these unique gold nanoparticles have great therapeutic application in the treatment of Osteosarcoma and future work should be focused to unravel this application [28]. Furthermore, these gold-aryl nanoparticles may also be used in lineage tracing experiments during animal development.

Conclusions

The present study indicated that gold-aryl nanoparticles do not affect the adipogenic differentiation of MG-63 cells. Furthermore, no key signaling pathway was affected by the uptake of the nanoparticles by MG-63 cells, providing a support that they may be ideal for drug delivery and tracing experiment during development. Hence, these gold-aryl nanoparticles can potentially be useful for drug delivery in Osteosarcoma patients, as they do not affect the cellular processes in these cancer cells. The cancerous cells can be potentially targeted with gold nanoparticles conjugated with drugs that would kill cancer cells. Further studies should also be done to assess the effects of these nanoparticles in MSC differentiation as well as the osteoblastic differentiation of the MG-63 cells. To use these specific nanoparticles for wider medical applications, further research is warranted to unravel the effects of these nanoparticles on other human cells.

Limitation of the study

The study did not evaluate the effects of aryl-gold nanoparticles on the differentiation of MG-63 cells into osteoblasts.

Availability of data and materials

All data generated and analyzed during this study will be freely available to any scientist wishing to use them for non-commercial purposes upon reasonable request from the corresponding authors.

Abbreviations

MSC:

Mesenchymal stem cells

RT-PCR:

Real Time quantitative PCR

References

  1. Niu M, Feng X, Zhou L. The role of the ERK1/2 pathway in simvastatin-loaded nanomicelles and simvastatin in regulating the osteogenic effect in MG63 cells. Int J Nanomedicine. 2018;13:8165–78.

    Article  CAS  Google Scholar 

  2. El-Serafi AT, Sandeep D, Abdallah S, Lozansson Y, Hamad M, Khan AA. Paradoxical effects of the epigenetic modifiers 5-aza-deoxycytidine and suberoylanilide hydroxamic acid on adipogenesis. Differentiation. 2019;106:1–8.

    Article  CAS  Google Scholar 

  3. Qiu N, Zhou H, Xiao Z. Downregulation of PKD1 by shRNA results in defective osteogenic differentiation via cAMP/PKA pathway in human MG-63 cells. J Cell Biochem. 2012;113(3):967–76.

    Article  CAS  Google Scholar 

  4. Wang W, Zhang X, Zheng J, Yang J. High glucose stimulates adipogenic and inhibits osteogenic differentiation in MG-63 cells through cAMP/protein kinase A/extracellular signal-regulated kinase pathway. Mol Cell Biochem. 2010;338(1–2):115–22.

    Article  CAS  Google Scholar 

  5. Ahmad AAL, Panicker S, Chehimi MM, Monge M, Lopez-de-Luzuriaga JM, Mohamed AA, Bruce AE, Bruce MRM. Synthesis of water-soluble gold–aryl nanoparticles with distinct catalytic performance in the reduction of the environmental pollutant 4-nitrophenol. Catal Sci Technol. 2019;9:6059–71.

    Article  CAS  Google Scholar 

  6. Ahmady IM, Hameed MK, Almehdi AM, Arooj M, Workie B, Sahle-Demessie E, Han C, Mohamed AA. Green and cytocompatible carboxyl modified gold-lysozyme nanoantibacterial for combating multidrug-resistant superbugs. Biomater Sci. 2019;7:5016–26.

    Article  CAS  Google Scholar 

  7. Enciso AE, Doni G, Nifosì R, Palazzesi F, Gonzalez R, Ellsworth AA, Coffer JL, Walker AV, Pavan GM, Mohamed AA, Simanek EE. Facile synthesis of stable, water soluble, dendron-coated gold nanoparticles. Nanoscale. 2017;9(9):3128–32.

    Article  CAS  Google Scholar 

  8. Hameed M, Panicker S, Abdallah SH, Khan AA, Han C, Chehimi MM, Mohamed AA. Protein-coated aryl modified gold nanoparticles for cellular uptake study by osteosarcoma cancer cells. Langamiur. 2020;33:11765–75.

    Article  Google Scholar 

  9. Yang X, Liu X, Li Y, Huang Q, He W, Zhang R, Feng Q, Benayahu D. The negative effect of silica nanoparticles on adipogenic differentiation of human mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl. 2017;81:341–8.

    Article  CAS  Google Scholar 

  10. Yao D, Liu N, Mo B. Assessment of proliferation, migration and differentiation potentials of bone marrow mesenchymal stem cells labeling with silica-coated and amine-modified superparamagnetic iron oxide nanoparticles. Cytotechnology. 2020;72:513–25.

    Article  CAS  Google Scholar 

  11. Au K, Liao S, Lee Y, Lai W, Ng K, Chan Y, Yip M, Ho C, Wu EX, Li RA, Siu C, Tse H. Effects of iron oxide nanoparticles on cardiac differentiation of embryonic stem cells. Biochem Biophys Res Commun. 2009;379:898–903.

    Article  CAS  Google Scholar 

  12. Au K, Liao S, Lee Y, Lai W, Ng K, Chan Y, Yip M, Ho C, Wu EX, Li RA, Siu C, Tse H. Effects of iron oxide nanoparticles on cardiac differentiation of embryonic stem cells. Biochem Biophys Res Commun. 2009;379(4):898–903.

    Article  CAS  Google Scholar 

  13. Dreaden EC, Alkilany AM, Huang X, Murphy CJ, El-Sayed MA. The golden age: gold nanoparticles for biomedicine. Chem Soc Rev. 2012;41:2740–79.

    Article  CAS  Google Scholar 

  14. Dreaden EC, Austin LA, Mackey MA, El-Sayed MA. Size matters: gold nanoparticles in targeted cancer drug delivery. Ther Deliv. 2012;3:457–78.

    Article  CAS  Google Scholar 

  15. Tsai SW, Liaw JW, Kao YC, Huang MY, Lee CY, Rau LR, Huang CY, Wei KC, Ye TC. Internalized gold nanoparticles do not affect the osteogenesis and apoptosis of MG63 osteoblast-like cells: a quantitative, in vitro study. PLoS ONE. 2013;8(10):e76545.

    Article  CAS  Google Scholar 

  16. Zhang D, Liu D, Zhang J, Fong C, Yang M. Gold nanoparticles stimulate differentiation and mineralization of primary osteoblasts through the ERK/MAPK signaling pathway. Mater Sci Eng C Mater Biol Appl. 2014;42:70–7.

    Article  Google Scholar 

  17. Yi C, Liu D, Fong CC, Zhang J, Yang M. Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano. 2010;4(11):6439–48.

    Article  CAS  Google Scholar 

  18. Neradil J, Kyr M, Polaskova K, Kren L, Macigova P, Skoda J, Sterba J, Veselska R. Phospho-protein arrays as effective tools for screening possible targets for kinase inhibitors and their use in precision pediatric oncology. Front Oncol. 2019;20(9):930.

    Article  Google Scholar 

  19. Fayyad AM, Khan AA, Abdallah SH, Alomran SS, Bajou K, Khattak MNK. Rosiglitazone enhances browning adipocytes in association with MAPK and PI3-K pathways during the differentiation of telomerase-transformed mesenchymal stromal cells into adipocytes. Int J Mol Sci. 2019;20(7):1618.

    Article  CAS  Google Scholar 

  20. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–8.

    Article  CAS  Google Scholar 

  21. Jo MJ, Jeong S, Yun HK, Kim DY, Kim BR, Kim JL, et al. Genipin induces mitochondrial dysfunction and apoptosis via downregulation of Stat3/mcl-1 pathway in gastric cancer. BMC Cancer. 2019;19(1):739.

    Article  Google Scholar 

  22. AlGhalbana FM, Khan AA, Khattak MNK. Comparative anticancer activities of Ficus carica and Ficus salicifolia latex in MDA-MB-231 cells. Saudi J Biol Sci. 2021. https://0-doi-org.brum.beds.ac.uk/10.1016/j.sjbs.2021.02.061.

    Article  Google Scholar 

  23. Zhang J, Liu XH, Li C, Wu X, Chen Y, Li W, Li X, Gong F, Tang Q, Jiang D. SNCG promotes the progression and metastasis of high-grade serous ovarian cancer via targeting the PI3K/AKT signaling pathway. J Exp Clin Cancer Res. 2020;39(1):79.

    Article  CAS  Google Scholar 

  24. Kim JH, Kim WS, Park C. Interleukin-6 mediates resistance to PI3K-pathway-targeted therapy in lymphoma. BMC Cancer. 2019;19(1):936.

    Article  Google Scholar 

  25. Marcantonio M, Trost M, Courcelles M, Desjardins M, Thibault P. Combined enzymatic and data mining approaches for comprehensive phosphoproteome analyses: application to cell signaling events of interferon-gamma-stimulated macrophages. Mol Cell Proteomics. 2008;7(4):645–60.

    Article  CAS  Google Scholar 

  26. Cirulli C, Coccetti P, Alberghina L, Tripodi F. A surface-activated chemical ionization approach allows quantitative phosphorylation analysis of the cyclin-dependent kinase inhibitor Sic1 phosphorylated on Ser201. Rapid Commun Mass Spectrom. 2012;26(13):1527–32.

    Article  CAS  Google Scholar 

  27. Adjei IM, Sharma B, Labhasetwar V. Nanoparticles: cellular uptake and cytotoxicity. Adv Exp Med Biol. 2014;811:73–91.

    Article  Google Scholar 

  28. Barani M, Mukhtar M, Rahdar A, Sargazi S, Pandey S, Kang M. Recent advances in nanotechnology-based diagnosis and treatments of human osteosarcoma. Biosensors. 2021;11(2):55.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Not applicable

Funding

AAK acknowledges funding from the College of Graduate Studies at University of Sharjah and the Competitive Research Project Grant support of grant number 1602145036-P from the University of Sharjah. AAM acknowledges the University of Sharjah support of SEED grant (VC-GRC-SR-83–2015), competitive grants (160–2142-029-P and 150–2142-017-P), Organometallic Research Group grant (RISE-046–2016) and Functionalized Nanomaterials Synthesis Lab grant (151–0039).

Author information

Authors and Affiliations

  1. Department of Applied Biology, College of Sciences, University of Sharjah, Sharjah, 27272, UAE

    Muhammad Abdulwahab, Amir Ali Khan & Muhammad Nasir Khan Khattak

  2. Human Genetics and Stem Cells Research Group, Research Institute of Sciences and Engineering, University of Sharjah, Sharjah, 27272, UAE

    Amir Ali Khan, Sallam Hasan Abdallah & Muhammad Nasir Khan Khattak

  3. Department of Chemistry, Delaware State University, 1200 North DuPont Highway, Dover, DE, 19901, USA

    Bizuneh Workie

  4. Univ Paris Est Creteil, CNRS, ICMPE, UMR7182, 94320, Thiais, France

    Mohamed Mehdi Chehimi

  5. Department of Chemistry, College of Sciences, University of Sharjah, Sharjah, 27272, UAE

    Ahmed Ali Mohamed

Authors
  1. Muhammad Abdulwahab
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amir Ali Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sallam Hasan Abdallah
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Nasir Khan Khattak
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bizuneh Workie
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mohamed Mehdi Chehimi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ahmed Ali Mohamed
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, MA, AAK, BW, MMC AAM; methodology and investigation, MA, AAK, SHA, MNKK and AAM; validation, MA, AAK, SHA, AAM, SHA, MNKK and AAM; formal analysis, MA, AAK and AAM; resources, MA, AAK and AAM; writing—original draft preparation, MA, AAK, and AAM; writing—review and editing, MA, AAK, SHA, MNKK, BW, MMC and AAM; funding acquisition; AAK, and AAM. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Amir Ali Khan or Ahmed Ali Mohamed.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1

: Table S1. qPCR primer sequences of the marker genes.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abdulwahab, M., Khan, A.A., Abdallah, S.H. et al. Arylated gold nanoparticles have no effect on the adipogenic differentiation of MG-63 cells nor regulate any key signaling pathway during the differentiation. BMC Res Notes 14, 192 (2021). https://0-doi-org.brum.beds.ac.uk/10.1186/s13104-021-05594-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/s13104-021-05594-9

Keywords

BMC Research Notes

ISSN: 1756-0500

Contact us