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Gold nanoparticles biosynthesized by Nocardiopsis dassonvillei NCIM 5124 enhance osteogenesis in gingival mesenchymal stem cells

  • Applied microbial and cell physiology
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Abstract

Gold nanoparticles are widely used for biomedical applications owing to their biocompatibility, ease of functionalization and relatively non-toxic nature. In recent years, biogenic nanoparticles have gained attention as an eco-friendly alternative for a variety of applications. In this report, we have synthesized and characterized gold nanoparticles (AuNPs) from an Actinomycete, Nocardiopsis dassonvillei NCIM 5124. The conditions for biosynthesis were optimized (100 mg/ml of cell biomass, 2.5 mM tetrachloroauric acid (HAuCl4) at 80 °C and incubation time of 25 min) and the nanoparticles were characterized by TEM, SAED, EDS and XRD analysis. The nanoparticles were spherical and ranged in size from 10 to 25 nm. Their interactions with human gingival tissue–derived mesenchymal stem cells (GMSCs) and their potential applications in regenerative medicine were evaluated further. The AuNPs did not display cytotoxicity towards GMSCs when assessed by 3-(4,5-dimethylthiazolyl-2)-2,5-diphenyltetrazolium bromide assay, DNA fragmentation patterns and Annexin V/propidium iodide staining techniques. These AuNPs induced faster cell migration when monitored by the in vitro wound healing assay. The effect of these nanoparticles on osteogenesis of GMSCs was also studied. Based on the results obtained from alkaline phosphatase, Von Kossa staining and Alizarin Red S staining, the AuNPs were seen to positively affect differentiation of GMSCs and enhance mineralization of the synthesized matrix. We therefore conclude that the biogenic, non-toxic AuNPs are of potential relevance for tissue regeneration applications.

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References

  • Ahmed S, Ikram S (2016) Biosynthesis of gold nanoparticles: a green approach. J Photochem Photobiol B 161:141–153

    CAS  PubMed  Google Scholar 

  • Apte M, Girme G, Bankar A, Kumar AR, Zinjarde S (2013) 3, 4-Dihydroxy-L-phenylalanine-derived melanin from Yarrowia lipolytica mediates the synthesis of silver and gold nanostructures. J Nanobiotechnol. https://doi.org/10.1186/1477-3155-11-2

  • Apte M, Chaudhari P, Vaidya A, Kumar AR, Zinjarde S (2016) Application of nanoparticles derived from marine Staphylococcus lentus in sensing dichlorvos and mercury ions. Colloids Surf A Physicochem Eng Asp 501:1–8

    CAS  Google Scholar 

  • Baharara J, Ramezani T, Divsalar A, Mousavi M, Seyedarabi A (2016) Induction of apoptosis by green synthesized gold nanoparticles through activation of caspase-3 and 9 in human cervical cancer cells. Avicenna J Med Biotechnol 8:75–83

    PubMed  PubMed Central  Google Scholar 

  • Bankar A, Joshi B, Kumar AR, Zinjarde S (2010) Banana peel extract mediated synthesis of gold nanoparticles. Colloids Surf B 80:45–50

    CAS  Google Scholar 

  • Behie SW, Bonet B, Zacharia VM, McClung DJ, Traxler MF (2017) Molecules to ecosystems: Actinomycete natural products in situ. Front Microbiol. https://doi.org/10.3389/fmicb.2016.02149

  • Bennur T, Kumar AR, Zinjarde S, Javdekar V (2014) Nocardiopsis species as potential sources of diverse and novel extracellular enzymes. Appl Microbiol Biotechnol 98:9173–9185

    CAS  PubMed  Google Scholar 

  • Bennur T, Kumar AR, Zinjarde S, Javdekar V (2015) Nocardiopsis species: incidence, ecological roles and adaptations. Microbiol Res 174:33–47

    PubMed  Google Scholar 

  • Bennur T, Kumar AR, Zinjarde SS, Javdekar V (2016a) Nocardiopsis species: a potential source of bioactive compounds. J Appl Microbiol 120:1–16

    CAS  PubMed  Google Scholar 

  • Bennur T, Khan Z, Kshirsagar R, Javdekar V, Zinjarde S (2016b) Biogenic gold nanoparticles from the actinomycete Gordonia amarae: application in rapid sensing of copper ions. Sensor Actuat B Chem 233:684–690

    CAS  Google Scholar 

  • Boroumand Moghaddam A, Namvar F, Moniri M, Azizi S, Mohamad R (2015) Nanoparticles biosynthesized by fungi and yeast: a review of their preparation, properties, and medical applications. Molecules 20:16540–16565

    PubMed  PubMed Central  Google Scholar 

  • Chaudhary HS, Soni B, Shrivastava AR, Shrivastava S (2013) Diversity and versatility of actinomycetes and its role in antibiotic production. J Appl Pharm Sci 3:S83–S94

    Google Scholar 

  • Choi SY, Song MS, Ryu PD, Lam ATN, Joo SW, Lee SY (2015) Gold nanoparticles promote osteogenic differentiation in human adipose-derived mesenchymal stem cells through the wnt/β-catenin signaling pathway. Inter J Nanomed. https://doi.org/10.2147/IJN.S78775

  • Chokriwal A, Sharma MM, Singh A (2014) Biological synthesis of nanoparticles using bacteria and their applications. Am J PharmTech Res 4:38–61

    Google Scholar 

  • De Crozals G, Bonnet R, Farre C, Chaix C (2016) Nanoparticles with multiple properties for biomedical applications: a strategic guide. Nano Today 11:435–463

    Google Scholar 

  • Dixit VS, Pant A (2000a) Comparative characterization of two serine endopeptidases from Nocardiopsis sp. NCIM 5124. Biochim Biophys Acta Gen Sub 1523:261–268

    CAS  Google Scholar 

  • Dixit VS, Pant A (2000b) Hydrocarbon degradation and protease production by Nocardiopsis sp. NCIM 5124. Lett Appl Microbiol 30:67–69

    CAS  PubMed  Google Scholar 

  • El Domany EB, Essam TM, Ahmed AE, Farghali AA (2018) Biosynthesis physico-chemical optimization of gold nanoparticles as anti-cancer and synergetic antimicrobial activity using Pleurotus ostreatus fungus. J Appl Pharm Sci 8:119–128

    Google Scholar 

  • Engel López E, Michiardi A, Navarro M, Lacroix DJ, Planell Estany JA (2008) Nanotechnology in regenerative medicine: the materials side. Trends Biotechnol 26:39–47

    Google Scholar 

  • Fan JH, Li WT, Hung WI, Chen CP, Yeh JM (2011) Cytotoxicity and differentiation effects of gold nanoparticles to human bone marrow mesenchymal stem cells. Biomed Eng Appl Basis Commun 23:141–152

    CAS  Google Scholar 

  • Golinska P, Wypij M, Ingle AP, Gupta I, Dahm H, Rai M (2014) Biogenic synthesis of metal nanoparticles from actinomycetes: biomedical applications and cytotoxicity. Appl Microbiol Biotechnol 98:8083–8097

    CAS  PubMed  Google Scholar 

  • Golub EE, Boesze-Battaglia K (2007) The role of alkaline phosphatase in mineralization. Curr Opin Orthop 18:444–448

    Google Scholar 

  • Hamza F, Vaidya A, Apte M, Kumar AR, Zinjarde S (2017) Selenium nanoparticle-enriched biomass of Yarrowia lipolytica enhances growth and survival of Artemia salina. Enzyme Microbial Technol 106:48–54

    CAS  Google Scholar 

  • He W, Elkhooly TA, Liu X, Cavallaro A, Taheri S, Vasilev K, Feng Q (2016) Silver nanoparticle based coatings enhance adipogenesis compared to osteogenesis in human mesenchymal stem cells through oxidative stress. J Mat Chem B 4:1466–1479

    CAS  Google Scholar 

  • He X, Deng H, Hwang HM (2019) The current application of nanotechnology in food and agriculture. J Food Drug Anal 27:1–21

    CAS  PubMed  Google Scholar 

  • Hoemann CD, El-Gabalawy H, McKee MD (2009) In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol Biol 57:318–323

    CAS  PubMed  Google Scholar 

  • Infante A, Rodríguez CI (2018) Osteogenesis and aging: lessons from mesenchymal stem cells. Stem Cell Res Ther 9:1–7. https://doi.org/10.1186/s13287-018-0995-x

    Article  CAS  Google Scholar 

  • Ko WK, Heo DN, Moon HJ, Lee SJ, Bae MS, Lee JB, Sun IC, Jeon HB, Park HK, Kwon IK (2015) The effect of gold nanoparticle size on osteogenic differentiation of adipose-derived stem cells. J Coll Interf Sci 438:68–76

    CAS  Google Scholar 

  • Li X, Xu H, Chen ZS, Chen G (2011) Biosynthesis of nanoparticles by microorganisms and their applications. J Nanomater. https://doi.org/10.1155/2011/270974

  • Li JJ, Kawazoe N, Chen G (2015) Gold nanoparticles with different charge and moiety induce differential cell response on mesenchymal stem cell osteogenesis. Biomaterials 54:226–236

    CAS  PubMed  Google Scholar 

  • Li J, Li JJ, Zhang J, Wang X, Kawazoe N, Chen G (2016) Gold nanoparticle size and shape influence on osteogenesis of mesenchymal stem cells. Nanoscale 8:7992–8007

    CAS  PubMed  Google Scholar 

  • Li J, Chen Y, Yang Y, Kawazoe N, Chen G (2017) Sub-10 nm gold nanoparticles promote adipogenesis and inhibit osteogenesis of mesenchymal stem cells. J Mat Chem B 5:1353–1362

    CAS  Google Scholar 

  • Liang CC, Park AY, Guan JL (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2:329–333

    CAS  PubMed  Google Scholar 

  • Lin L, Chow KL, Leng Y (2009) Study of hydroxyapatite osteoinductivity with an osteogenic differentiation of mesenchymal stem cells. J Biomed Mater Res A 89:326–335

    PubMed  Google Scholar 

  • Luby AO, Ranganathan K, Lynn JV, Nelson NS, Donneys A, Buchman SR (2019) Stem cells for bone regeneration: current state and future directions. J Craniofac Surg. https://doi.org/10.1097/SCS.0000000000005250

  • Manimaran M, Kannabiran K (2017) Actinomycetes-mediated biogenic synthesis of metal and metal oxide nanoparticles: progress and challenges. Lett Appl Microbiol 64:401–408

    CAS  PubMed  Google Scholar 

  • Manivasagan P, Alam MS, Kang KH, Kwak M, Kim SK (2015) Extracellular synthesis of gold bionanoparticles by Nocardiopsis sp. and evaluation of its antimicrobial, antioxidant and cytotoxic activities. Bioprocess Biosyst Eng 38:1167–1177

    CAS  PubMed  Google Scholar 

  • Matassov D, Kagan T, Leblanc J, Sikorska M, Zakeri Z (2004) Measurement of apoptosis by DNA fragmentation. In: Brady HJM (ed) Apoptosis methods and protocols. Methods in molecular biology. Humana Press, Totowa, pp 1–17

    Google Scholar 

  • Mittal AK, Chisti Y, Banerjee UC (2013) Synthesis of metallic nanoparticles using plant extracts. Biotechnol Adv 31:346–356

    CAS  PubMed  Google Scholar 

  • Monti M, Perotti C, Del Fante C, Cervio M, Redi CA (2012) Stem cells: sources and therapies. Biol Res 45:207–214

    PubMed  Google Scholar 

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    CAS  PubMed  Google Scholar 

  • Ovais M, Ahmad I, Khalil AT, Mukherjee S, Javed R, Ayaz M, Raza A, Shinwari ZK (2018) Wound healing applications of biogenic colloidal silver and gold nanoparticles: recent trends and future prospects. Appl Microbiol Biotechnol 102:4305–4318

    CAS  PubMed  Google Scholar 

  • Rani M, Shanker U, Jassal V (2017) Recent strategies for removal and degradation of persistent & toxic organochlorine pesticides using nanoparticles: a review. J Environ Manag 190:208–222

    CAS  Google Scholar 

  • Sett A, Gadewar M, Sharma P, Deka M, Bora U (2016) Green synthesis of gold nanoparticles using aqueous extract of Dillenia indica. Adv Nat Sci Nanosci Nanotechnol. https://doi.org/10.1088/2043-6262/7/2/025005

  • Siddiqi KS, Husen A (2016) Fabrication of metal and metal oxide nanoparticles by algae and their toxic effects. Nanoscale Res Lett 11:363–373

    PubMed  PubMed Central  Google Scholar 

  • Sowani H, Mohite P, Munot H, Shouche Y, Bapat T, Kumar AR, Kulkarni M, Zinjarde S (2016) Green synthesis of gold and silver nanoparticles by an actinomycete Gordonia amicalis HS-11: mechanistic aspects and biological application. Process Biochem 51:374–383

    CAS  Google Scholar 

  • Sridhar S, Venugopal JR, Sridhar R, Ramakrishna S (2015) Cardiogenic differentiation of mesenchymal stem cells with gold nanoparticle loaded functionalized nanofibers. Colloids Surf B 134:346–354

    CAS  Google Scholar 

  • Suzuki H, Toyooka T, Ibuki Y (2007) Simple and easy method to evaluate uptake potential of nanoparticles in mammalian cells using a flow cytometric light scatter analysis. Environ Sci Technol 41:3018–3024

    CAS  PubMed  Google Scholar 

  • Tomar GB, Srivastava RK, Gupta N, Barhanpurkar AP, Pote ST, Jhaveri HM, Mishra GC, Wani MR (2010) Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem Biophys Res Commun 393:377–383

    CAS  PubMed  Google Scholar 

  • Volkova N, Pavlovich O, Fesenko O, Budnyk O, Kovalchuk S, Goltsev A (2017) Studies of the influence of gold nanoparticles on characteristics of mesenchymal stem cells. J Nanomater. https://doi.org/10.1155/2017/6934757

  • Wu W (2017) Inorganic nanomaterials for printed electronics: a review. Nanoscale 9:7342–7372

    CAS  PubMed  Google Scholar 

  • Wu JW, Ng IS (2017) Biofabrication of gold nanoparticles by Shewanella species. Bioresour Bioprocess. https://doi.org/10.1186/s4064

  • Yang X, Li Y, Liu X, Huang Q, He W, Zhang R, Feng Q, Benayahu D (2016) The stimulatory effect of silica nanoparticles on osteogenic differentiation of human mesenchymal stem cells. Biomed Mater. https://doi.org/10.1088/1748-605X/12/1/015001

  • Yang J, Nian F, Guo Z, Bai T, Peng G (2017) Effect of gold nanoparticles with different diameters on rat neural stem and progenitor cells. Nanosci Nanotechnol Lett 9:1491–1496

    Google Scholar 

  • Yi C, Liu D, Fong CC, Zhang J, Yang M (2010) Gold nanoparticles promote osteogenic differentiation of mesenchymal stem cells through p38 MAPK pathway. ACS Nano 4:6439–6448

    CAS  PubMed  Google Scholar 

  • Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Shi S, Le AD (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183:7787–7798

    CAS  PubMed  Google Scholar 

  • Zhang D, Liu D, Zhang J, Fong C, Yang M (2014) Gold nanoparticles stimulate differentiation and mineralization of primary osteoblasts through the ERK/MAPK signaling pathway. Mater Sci Eng C 42:70–77

    Google Scholar 

  • Zhang R, Lee P, Lui VC, Chen Y, Liu X, Lok CN, To M, Yeung KW, Wong KK (2015) Silver nanoparticles promote osteogenesis of mesenchymal stem cells and improve bone fracture healing in osteogenesis mechanism mouse model. Nanomed Nanotechnol Biol Med 11:1949–1959

    CAS  Google Scholar 

  • Zhang Y, Kong N, Zhang Y, Yang W, Yan F (2017) Size-dependent effects of gold nanoparticles on osteogenic differentiation of human periodontal ligament progenitor cells. Theranostics 7:1214–1224

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Zhang Y, Li L, Fu H, Yang W, Yan F (2018) Human β-defensin 3-combined gold nanoparticles for enhancement of osteogenic differentiation of human periodontal ligament cells in inflammatory microenvironments. Int J Nanomedicine 13:555–567

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by funds from University Grants Commission under University with Potential for Excellence, Phase II. TB thanks the Council of Scientific and Industrial Research, New Delhi, India, for Junior and Senior Research Fellowship. GB thanks the Department of Science and Technology INSPIRE, Govt. of India [grant number IFA13 LSBM73] for fellowship and research grant.

Funding

This work was financially supported by funds from the University Grants Commission under University with Potential for Excellence, Phase II. TB received Junior and Senior Research Fellowship from the Council of Scientific and Industrial Research, New Delhi, India. GB received fellowship and research grant from the Department of Science and Technology INSPIRE, Govt. of India [grant number IFA13 LSBM73].

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Authors and Affiliations

  1. Institute of Bioinformatics and Biotechnology, Savitribai Phule Pune University, Pune, Maharashtra, 411007, India

    Tahsin Bennur, Geetanjali B. Tomar & Smita Zinjarde

  2. Department of Biotechnology, Abasaheb Garware College, Pune, Maharashtra, 411004, India

    Vaishali Javdekar

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  1. Tahsin Bennur
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  2. Vaishali Javdekar
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  3. Geetanjali B. Tomar
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Tahsin Bennur. Geetanjali B. Tomar contributed towards cell culture experimentation. Vaishali Javdekar and Smita Zinjarde gave inputs for the nanotechnology component. First manuscript draft was written by Tahsin Bennur. GB and SZ worked on the draft and finalized the contents of the manuscript.

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Correspondence to Geetanjali B. Tomar or Smita Zinjarde.

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The authors declare that they have no conflict of interest.

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All protocols involving gingival stem cells have been approved by the Institutional Ethics Committee of Deenanath Mangeshkar Hospital and Research Centre, Pune, India, and Savitribai Phule Pune University, Pune, India. The gingival tissue samples were collected after obtaining informed consent from the donors.

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Bennur, T., Javdekar, V., Tomar, G.B. et al. Gold nanoparticles biosynthesized by Nocardiopsis dassonvillei NCIM 5124 enhance osteogenesis in gingival mesenchymal stem cells. Appl Microbiol Biotechnol 104, 4081–4092 (2020). https://doi.org/10.1007/s00253-020-10508-z

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  • DOI: https://doi.org/10.1007/s00253-020-10508-z

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