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A comparative study of the adhesion of biosynthesized gold and conjugated gold/prodigiosin nanoparticles to triple negative breast cancer cells

  • Engineering and Nano-engineering Approaches for Medical Devices
  • Original Research
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Abstract

This paper explores the adhesion of biosynthesized gold nanoparticles (AuNPs) and gold (Au) nanoparticle/prodigiosin (PG) drug nanoparticles to breast cancer cells (MDA-MB-231 cells). The AuNPs were synthesized in a record time (less than 30 s) from Nauclea latifolia leaf extracts, while the PG was produced via bacterial synthesis with Serratia marcescens sp. The size distributions and shapes of the resulting AuNPs were characterized using transmission electron microscopy (TEM), while the resulting hydrodynamic diameters and polydispersity indices were studied using dynamic light scattering (DLS). Atomic Force Microscopy (AFM) was used to study the adhesion between the synthesized gold nanoparticles (AuNPs)/LHRH-conjugated AuNPs and triple negative breast cancer cells (MDA-MB-231 cells), as well as the adhesion between LHRH-conjugated AuNP/PG drug and MDA-MB-231 breast cancer cells. The adhesion forces between LHRH-conjugated AuNPs and breast cancer cells are shown to be five times greater than those between AuNPs and normal breast cells. The increase in adhesion is shown to be due to the over-expression of LHRH receptors on the surfaces of MDA-MB-231 breast cancer cells, which was revealed by confocal immuno-fluorescence microscopy. The implications of the results are then discussed for the selective and specific targeting and treatment of triple negative breast cancer.

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References

  1. Jennings T, Strouse G. Past, present and future of gold nanoparticles. Adv Exp Med Biol. 2007;620:34–47.

    Article  Google Scholar 

  2. Holiday R. Use of gold in medicine and surgery. UK: Biomedical Scientist (The Official Gazette of the Institute of Biomedical science; 2008. p. 962–3.

    Google Scholar 

  3. Dykman LA, Khlebtsov NG. Gold nanoparticles in biology and medicine: recent advances and prospects. Acta Nat. 2011;3(2):34–55.

    Google Scholar 

  4. Chen PO, Mwakwari SC, Oyelere AK. Gold nanoparticles: from nanomedicine to nanosensing. Nanotechnol, Sci Appl. 2008;1:45–66.

    Article  Google Scholar 

  5. Canizal G, Ascencio JA, Gardea-Torresday J, Jose-Yacaman M. Multiple twinned gold nanorods grown by bio-reduction techniques. J Nanopart Res. 2001;3:475–81.

    Article  Google Scholar 

  6. Zhou Y, Yu SH, Cui XP, Wang CY, Chen ZY. Formation of silver nanowires by a novel solid- liquid phase arc discharge method. Chem Mater. 1999;11:545–6.

    Article  Google Scholar 

  7. Sun Y, Mayers B, Herricks T, Xia Y. Polyol synthesis of uniform silver nanowires: a plausible growth mechanism and the supporting evidence. Nano Lett. 2003;3:955–60.

    Article  Google Scholar 

  8. Mouxing F, Qingbiao L, Daohua S, Yinghua L, Ning H, Xu D, Huixuan W, Jiale H. Rapid preparation process of silver nanoparticles by bioreduction and their characterizations. chin. J Chem Eng. 2006;14(1):114–7.

    Google Scholar 

  9. Selvakannan PR, Mandal S, Pasricha R, Adyanthaya SD, Sastry M. One-step synthesis of hydrophobized gold nanoparticles of controllable size by the reduction of aqueous chloroaurate ions by hexadecylaniline at the liquid-liquid interface. Chem Commun. 2002;13:1334–5.

    Article  Google Scholar 

  10. Okitsu K, Yue A, Tanabe S, Matsumoto H, Yobiko Y. Formation of colloidal gold nanoparticles in an ultrasonic field: control of rate of gold (III) reduction and size of formed gold particles. Langmuir. 2001;17(25):7717–20.

    Article  Google Scholar 

  11. Singh A, Jain D, Upadhyay MK, Khandelwal N, Verma HN. Green synthesis of silver nanoparticles using Argemone mexicana leaf extract and evaluation of their antimicrobial activities. Dig J Nanomater Biostruct. 2010;5(2):483–9.

    Google Scholar 

  12. Leela A, Vivekanandan M. Tapping the unexploited plant resources for the synthesis of silver nanoparticles. Afr J Biotechnol. 2008;7(17):3162–5.

    Google Scholar 

  13. Balaprasad A. Biosynthesis of Gold Nanoparticles (Green-Gold) Using Leaf Extract of Terminalia Catappa. E-J Chem. 2010;7(4):1334–9.

    Article  Google Scholar 

  14. Gericke M, Pinches A. Microbial production of gold nanoparticles. Gold Bull. 2006;39(1):22–8.

    Article  Google Scholar 

  15. Sanghi R, Verma P, Puri S. Enzymatic formation of gold nanoparticles using Phanerochaete Chrysosporium. Adv Chem Eng Sci. 2011;1(3):154–62.

    Article  Google Scholar 

  16. Sun Y, Xia Y. Shape-controlled synthesis of gold and silver nanoparticles. Science. 2002;298(5601):2176–9.

    Article  Google Scholar 

  17. Nair B, Pradeep T. Coalescence of nanoclusters and formation of submicron crystallites assisted by Lactobacillus Strains. Cryst Growth Des. 2002;2:293.

    Article  Google Scholar 

  18. Chatterjee DK, Diagardjane P, Krishnan S. Nanoparticle-mediated hyperthermia in cancer therapy. Ther Deliv. 2011;2(8):1001–14.

    Article  Google Scholar 

  19. Mafune F, Kohno J, Takeda Y. Full physical preparation of size-selected gold nanoparticles in solution: laser ablation and laser-induced size control. J Phys Chem B. 2002;106(31):7575–7.

    Article  Google Scholar 

  20. Cho K, Wang X, Nie S, Chen ZG, Dong MS. Therapeuticnanoparticles for drug delivery in cancer. Clin Cancer Res. 2008;14(5):1310–6.

    Article  Google Scholar 

  21. Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR, Khan MI, Parischa R, Ajayakumar PV, Alam M, Kumar R, Sastry M. Fungus mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: A novel biological approach to nanoparticle synthesis. Nano Lett. 2001;1:515–9.

    Article  Google Scholar 

  22. Ahmad A, Senapati S, Khan MI, Kumar, Sastry M. Extracellular biosynthesis of monodisperse fold nanoparticles by a novel extremophilic actinomycete thermonospora sp. Langmuir. 2003;19:3550–3.

    Article  Google Scholar 

  23. Stephen JR, Maenaughton SJ. Developments in terrestrial bacterial remediation of metals. Curr Opin Biotechnol. 1999;10:230–5.

    Article  Google Scholar 

  24. Sastry M, Ahmad A, Khan MI, Kumar R. Biosynthesis of metal nanoparticles using fungi and actinomycete. Curr Sci. 2003;85:162–70.

    Google Scholar 

  25. Huang J, Li Q, Sun D, Lu Y, Su Y, Yang X, Wang H, Wang Y, Shao W, He N, Hong J, Chen C. Biosynthesis of silver and gold nanoparticles by novel sundried Cinnamomum canphora leaf. Nanotechnology. 2007;18(10):105104–15.

    Article  Google Scholar 

  26. Kasthuri J, Kathiravan K, Rajendiran N. Phyllanthin-assisted biosynthesis of silver and gold nanoparticles: a novel biological approach. J Nanopart Res. 2009;11(5):1075–85.

    Article  Google Scholar 

  27. Dozie-Nwachukwu SO, Etuk-Udo G, Obayemi JD, Anuku N, Odusanya OS, Malatesta K, Chi C, Soboyejo WO. Biosynthesis of gold nanoparticles from Nauclea latifolia leaves. Adv Mater Res. 2016;1132:36–50.

    Article  Google Scholar 

  28. Pellegrino T, Kudera S, Liedl T, Muñoz Javier A, Manna L, Parak WJ. On the development of colloidal nanoparticles towards multifunctional structures and their possible use for biological applications. Small. 2005;1:48–63.

    Article  Google Scholar 

  29. Shankar SS, Ahmad A, Pasrichaa R, Sastry M. Bioreduction of chloroaurate ions by geranium leaves and its endophytic fungus yields gold nanoparticles of different shapes. J Mater Chem. 2003;13:1822–6.

    Article  Google Scholar 

  30. Ankamwar B, Chaudhary M, Sastry M. Gold nanotriangles biologically synthesized using tamarind leaf extract and potential application in vapor sensing. Synth React Inorg Metal-Org Nano- Metal Chem. 2005;35:19–26.

    Article  Google Scholar 

  31. Huang J, Li Q, Sun D, Lu Y, Su Y, Yang X. Biosynthesis of silver and gold nanoparticles by novel sundried Cinnamomum camphora leaf. Nanotechnology. 2007;18:105104–14.

    Article  Google Scholar 

  32. Shankar SS, Rai A, Ahmad A, Sastry M. Controlling the optical properties of lemongrass extract synthesized gold nanotriangles and potential application in infrared-absorbing optical coatings. Chem Mater. 2005;17:566–72.

    Article  Google Scholar 

  33. Ankamwar B, Damle C, Ahmad A, Sastry M. Biosynthesis of gold and silver nanoparticles using Emblica officinalis fruit extract, their phase transfer and transmetallation in an organic solution. J Nanosci Nanotechnol. 2005;5:1665–71.

    Article  Google Scholar 

  34. Shankar SS, Rai A, Ahmad A, Sastry M. Rapid synthesis of Au, Ag and bimetallic Au core–Ag shell nanoparticles using neem (Azadirachta indica) leaf broth. J Colloid Interf Sci. 2004;275:496–502.

    Article  Google Scholar 

  35. Chandran SP, Chaudhary M, Pasricha R, Ahmad A, Sastry M. Synthesis of gold nanotriangles and silver nanoparticles using Aloe vera plant extract. Biotechnol Prog. 2006;22:577–83.

    Article  Google Scholar 

  36. Umadevi M, Sampath Kumar KP, Bhowmik D, Duraive S. Traditionally used anticancer herbs in India. J Med Plants Stud. 2013;1(3):56–74.

    Google Scholar 

  37. Paul J, Gnanam RM, Jayadeepa R, Arul L. Anti-cancer activity on Graviola, an exciting medicinal plant extract vs various cancer cell lines and a detailed computational study on its potent anti-cancerous leads. Curr Top Med Chem. 2013;13(14):1666–73.

    Article  Google Scholar 

  38. Akpanabiatu MI, Umoh IB, Eyong EU, Udoh FV. Influence of Nauclea latifolia leaf extracts on some hepatic enzymes of rats fed on coconut oil and non-coconut oil meals. Pharm Biol. 2005;43(2):153–7.

    Article  Google Scholar 

  39. Brandenburg KS, Shakeri-Zadeh A, Mansoori GA. Folate-conjugated gold nanoparticlesfor cancer nanotechnology applications. Nanotechnology. 2011;3:404–7.

    Google Scholar 

  40. Gao T, Hong H, Sun J. Applications of gold nanoparticles in cancer nanotechnology. Nanotechnol, Sci Appl. 2008;1:17–32.

    Article  Google Scholar 

  41. Chatterjee DK, Diagaradjane P, Krishnan S. Nanoparticle-mediated hyperthermia in cancer therapy. Ther Deliv. 2011;2(8):1001–14.

    Article  Google Scholar 

  42. Jain S, Hirst DG, O’Sullivan JM. Gold nanoparticles as novel agents for cancer therapy. Br J Radiol. 2012;85(1010):101–13.

    Article  Google Scholar 

  43. Hampp E, Botah R, Odusanya SO, Anuku N, Malatesta K, Soboyejo WO. Biosynthesis and adhesion of gold nanoparticles for breast cancer detection and treatment. J Mater Res. 2012;27(22):2891.

    Article  Google Scholar 

  44. Meng J, Paetzell E, Bogorad A, Soboyejo WO. Adhesion between peptides/antibodies and breast cancer cells. J Appl Phys. 2010;107:114301.

    Article  Google Scholar 

  45. Oni Y, Hao K, Dozie-Nwachukwu S, Obayemi JD, Odusanya OS, Anuku N, Soboyejo WO. Gold nanoparticles for cancer detection and treatment: the role of adhesion. J Appl Phys. 2014;115:084305.

    Article  Google Scholar 

  46. Gates RS, Osborn WA, Pratt JR. Experimental determination of mode correction factors for thermal method spring constant calibration of AFM cantilevers using laser Doppler vibrometry. Nanotechnology. 2013;24(25):255706.

    Article  Google Scholar 

  47. Dupres V, Menozzi FD, Locht C, Clare BH, Abbott NL, Cuenot S, Bompard C, Raze D, Dufrene YF. Nanoscale mapping and functional analysis of individual adhesins on living bacteria. Nat Methods. 2005;2:515–20.

    Article  Google Scholar 

  48. Wojcikiewicz EP, Zhang X, Moy V. Force and compliance measurements on living cells using atomic force microscopy (AFM). Biol Proced. 2004;6:1–9.

    Article  Google Scholar 

  49. Li F, Redick SD, Erickson HP, Moy VT. Force measurements of the α5β1 Integrin–Fibronectin interaction. Biophys J. 2003;84:1252–62.

    Article  Google Scholar 

  50. Shiao-Wen T, Jiunn-Woei TL, Fu-Yin H, Yi-Yun C, Mei-Jhih L, Ming-His Y. Surface-modified gold nanoparticles with folic acid as optical probes for cellular imaging. Sensors. 2008;8:6660–73.

    Article  Google Scholar 

  51. Obayemi JD, Danyuo Y, Dozie-Nwachukwu S, Odusanya OS, Anuku N, Malatesta K, Yu W, Uhrich KE, Soboyejo O. PLGA-based microparticles loaded with bacterial-synthesized prodigiosin for anticancer drug release: Effects of particle size on drug release kinetics and cell viability. Mater Sci Eng C. 2016;66:51–65.

    Article  Google Scholar 

  52. Kamble KD, Hiwarale VD. “Prodigiosin production from Serratia marcescens strains obtained from farm soil”. Int J Environ Sci. 2012;3(1):631–8.

    Google Scholar 

  53. Butt H, Cappella B, Kappl M. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep. 2005;59:1–152.

    Article  Google Scholar 

  54. Santner E, Stegemann B. Adhesion measurements by AFM – a gateway to the basics of friction. Accessed from: www.academia.edu/7351106/Adhesion_measurements_by_AFM_a_gateway_to_the_basics_of_friction on 30th March, 2016.

  55. Bhushan B, (Ed.). Handbook of Micro/Nanotribology. 2nd ed. Boca Raton: CRC press; 1999.

    Google Scholar 

  56. Burnham NA, Colton RJ, Pollock HM. Interpretation of force curves in force microscopy. Nanotechnology. 1993;4:64–80.

    Article  Google Scholar 

  57. Cappella B, Dietler G. Force-distance curves by atomic force microscopy. Surf Sci Rep. 1999;34(1-3):1–104.

    Article  Google Scholar 

  58. Rogošić M, Mencer HJ, Gomzi Z. Polydispersity index and molecular weight distributions of polymers. Eur Polym J. 1996;32(11):1337–44.

    Article  Google Scholar 

  59. Takae S, AkiyamaY, Otsuka H, Nakamura T, Nagasaki Y, Kataoka K. Ligand density effect on biorecognition by PEGylated gold nanoparticles: regulated interaction of RCA120 lectin with lactose installed to the distal end of tethered PEG N strands on gold surface. Biomacromolecules. 2005;6(2):818–24.

    Article  Google Scholar 

  60. Hall JB, Dobrovolskaia MA, Patri AK, McNeil SE. Characterization of nanoparticles for therapeutics. Nanomedicine. 2007;2(6):789–803.

    Article  Google Scholar 

  61. Arnida A, Janát-Amsbury MM, Ray A, Peterson CM, Ghandehari H. Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophages. Eur J Pharm Biopharm. 2011;77:417–23.

    Article  Google Scholar 

  62. Obayemi JD, Dozie-Nwachukwu S, Danyuo Y, Odusanya OS, Anuku N, Malatesta K, Soboyejo WO. Biosynthesis and the conjugation of magnetite nanoparticles with Luteinizing hormone releasing hormone (LHRH). J Mater Sci Eng C. 2015;46:482–96.

    Article  Google Scholar 

  63. Xiaohua Huanga, Mostafa A. El-Sayeda. Gold nanoparticles: Optical properties and implementations in cancer diagnosis and photothermal therapy. J Adv Res. 2010;1(1):13–28.

    Article  Google Scholar 

  64. Boham AB, Kocipai AA.: Flavonoids and condensed tannins from leaves of Hawaiian Vaccinium vaticulation and V. calycinium. Pac Sci. 1994;48:458–63.

  65. Madhavi RB. Dighe VV.Synthesis of gold nano particles using Putranjiva roxburghii wall. Leaves extract. Int J Drug Discov Herbal Res. 2012;2(1):275–8.

    Google Scholar 

  66. Kundu A, Layek RK, Kujla Nandi AK. : Highly fluorescent graphene oxide-poly (vinyl alcohol) hybrid: an effective material for specific Au3+ ion sensors. ACS Appl Mater Interface. 2012;4(10):5576–82.

    Article  Google Scholar 

  67. Lim J, Yeap SP, Che HX, Low SC. Characterization of magnetic nanoparticle by dynamic light scattering. Nanoscale Res Lett. 2013;8:381.

    Article  Google Scholar 

  68. Ohnesorge F, Binnig G. True atomic resolution by atomic force microscopy through repulsive and attractive forces. Science. 1993;260(5113):1451–6.

    Article  Google Scholar 

  69. Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett. 1986;56(9):930–3.

    Article  Google Scholar 

  70. Martin Y, Williams CC, Wickramasinghe HK. Atomic force microscope-force mapping and profiling on a sub 100-Å scale. J Appl Phys. 1987;61(10):4723–9.

    Article  Google Scholar 

  71. Zhou J, Leuschner C, Kumar C, Hormes JF, Soboyejo WO. Sub-cellular accumulation of magnetic nanoparticles in breast tumors and metastases. Biomaterials. 2006;27(9):2001–8.

    Article  Google Scholar 

  72. Zhou J, Leuschner C, Kumar C, Hormes J, Soboyejo WOA. TEM study of functionalized nanoparticles targeting breast cancer cells in mice. Mater Sci Eng C. 2006;26:1451–5.

    Article  Google Scholar 

  73. Leuschner C, Kumar CSSR, Hansel W, Zhou J, Soboyejo WO, Hormes J. LHRH-Conjugated magnetic iron oxide nanoparticles for detection of breast cancer metasteses. Breast Cancer Res Treat. 2006;99:163–76.

    Article  Google Scholar 

  74. Meng J, Fana J, Galiana G, Branca RT, Clasen PL, Ma, S, Zhou J, Leuschner C, Kumar CSSR., Hormes J, Otiti, T, Beye AC, Harmer MP, Kiely CJ, Warren W, Haataja MP, Soboyejo WO. LHRH-functionalized superparamagnetic iron oxide nanoparticles for breast cancer targeting and contrast enhancement in MRI. Mater Sci Eng C. 2009; 29: 1467-79.

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Acknowledgements

The research was supported by the SHESTCO-AUST-Princeton World Bank STEP-B Program, the World Bank African Centers of Excellence Program, Pan African Materials Institute (PAMI) the African Capacity Building Foundation (ACBF), the African Development Bank (ADB) and the Princeton University Old Schools Innovation Fund for their financial support. The authors are also grateful to Ms. Jingjie Hu, Ms. Cathy Chi, Ms. Vanessa Ozonwanne and Mr. Gerald Poirier of Princeton University, for all their assistance in DLS and TEM measurements.

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Authors and Affiliations

  1. Department of Materials Science and Engineering, African University of Science and Technology (AUST) Abuja-Nigeria, Abuja, Nigeria

    S. O. Dozie-Nwachukwu, J. D. Obayemi, Y. Danyuo, O. S. Odusanya & W. O. Soboyejo

  2. Biotechnology Advanced Research Center, Sheda Science and Technology Complex (SHESTCO) P.M.B 186, Garki, Abuja, Nigeria

    S. O. Dozie-Nwachukwu & O. S. Odusanya

  3. Department of Mechanical and Aerospace Engineering, Olden Street, Princeton, NJ, 08544, USA

    J. D. Obayemi & W. O. Soboyejo

  4. Department of Materials Science and Engineering, Kwara State University, Malete, Nigeria

    Y. Danyuo

  5. Princeton Institute of Science and Technology of Materials (PRISM), Bowen Hall, 70 Prospect Street, Princeton, NJ, 08544, USA

    N. Anuku, K. Malatesta & W. O. Soboyejo

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  1. S. O. Dozie-Nwachukwu
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  2. J. D. Obayemi
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  4. N. Anuku
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  5. O. S. Odusanya
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  7. W. O. Soboyejo
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Dozie-Nwachukwu, S.O., Obayemi, J.D., Danyuo, Y. et al. A comparative study of the adhesion of biosynthesized gold and conjugated gold/prodigiosin nanoparticles to triple negative breast cancer cells. J Mater Sci: Mater Med 28, 143 (2017). https://doi.org/10.1007/s10856-017-5943-2

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