Collagen-based silver nanoparticles for biological applications: synthesis and characterization

Journal of Nanobiotechnology

José Ribeiro dos Santos Júnior²  Durcilene Silva⁴  José Roberto SA Leite⁴  Carla Eiras⁶  Selma AS Kuckelhaus¹  José Raimundo Corrêa⁷  Yvonne P Mascarenhas⁸  Ana C Mafud⁸  Antonio C Tedesco⁵  Graciely Gomides Gobo⁵  Fernando Lucas Primo⁵  Adriany Amorin⁴  Patrick V Quelemes⁴  Vinicius S Cardoso³ 

[1] Area of Morphology, Faculty of Medicine, University of Brasília, Brasília 70910900, DF, Brazil;Department of Chemistry, Campus Teresina, Federal University of Piauí, Teresina, 64049-550, Piauí, Brazil;Physiotherapy Department, Campus Parnaíba, Federal University of Piauí, Av. São Sebastião 2819, Parnaíba, 64202-020, Piauí, Brazil;Research Center in Biodiversity and Biotechnology (Biotec), Campus Parnaíba, Federal University of Piauí, Av São Sebastian 2819, Parnaíba, 64202-020, Piauí, Brazil;Departamento de Química, Laboratório de Fotobiologia e Fotomedicina, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 14040-901, Ribeirão Preto, SP, Brazil;Interdisciplinary Laboratory for Advanced Materials (LIMAV), Federal University of Piauí, Teresina, 64049-550, PI, Brazil;Laboratory of Microscopy, Institute of Biology, University of Brasília, Brasília, 70910900, DF, Brazil;Institute of Physics of São Carlos (IFSC), University of São Paulo (USP), São Carlos, 13566-590, SP, Brazil

关键词: Cell viability;    Antimicrobial activity;    Collagen;    Silver nanoparticles;   

Others  :  1146156
DOI  :  10.1186/s12951-014-0036-6

 received in 2014-07-01, accepted in 2014-09-04,  发布年份 2014

【 摘 要 】

Background

Type I collagen is an abundant natural polymer with several applications in medicine as matrix to regenerate tissues. Silver nanoparticles is an important nanotechnology material with many utilities in some areas such as medicine, biology and chemistry. The present study focused on the synthesis of silver nanoparticles (AgNPs) stabilized with type I collagen (AgNPcol) to build a nanomaterial with biological utility. Three formulations of AgNPcol were physicochemical characterized, antibacterial activity in vitro and cell viability assays were analyzed. AgNPcol was characterized by means of the following: ultraviolet¿visible spectroscopy, dynamic light scattering analysis, Fourier transform infrared spectroscopy, atomic absorption analysis, transmission electron microscopy and of X-ray diffraction analysis.

Results

All AgNPcol showed spherical and positive zeta potential. The AgNPcol at a molar ratio of 1:6 showed better characteristics, smaller hydrodynamic diameter (64.34?±?16.05) and polydispersity index (0.40?±?0.05), and higher absorbance and silver reduction efficiency (0.645 mM), when compared with the particles prepared in other mixing ratios. Furthermore, these particles showed antimicrobial activity against both Staphylococcus aureus and Escherichia coli and no toxicity to the cells at the examined concentrations.

Conclusions

The resulted particles exhibited favorable characteristics, including the spherical shape, diameter between 64.34 nm and 81.76 nm, positive zeta potential, antibacterial activity, and non-toxicity to the tested cells (OSCC).

【 授权许可】

   
2014 Cardoso et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Dornelles C, Costa S: Estudo comparativo da dissolução de três diferentes marcas de colágeno utilizadas em técnicas cirúrgicas otológicas. Rev Bras Otorrinolaringol 2003, 69:744-751.
• [2]Tonhi E, Plepis AMG: Obtenção e caracterização de blendas colágeno-quitosana. Qim nova 2002, 25:943-948.
• [3]Lin YC, Tan FJ, Marra KG, Jan SS, Liu DC: Synthesis and characterization of collagen/hyaluronan/chitosan composite sponges for potential biomedical applications. Acta Biomater 2009, 5:2591-2600.
• [4]Wang XH, Li DP, Wang WJ, Feng QL, Cui FZ, Xu YX, Song XH, Van der Werf M: Crosslinked collagen/chitosan matrix for artificial livers. Biomaterials 2003, 24:3213-3220.
• [5]Nehrer S, Breinan HA, Ramappa A, Young G, Shortkroff S, Louie LK, Sledge CB, Yannas IV, Spector M: Matrix collagen type and pore size influence behaviour of seeded canine chondrocytes. Biomaterials 1997, 18:769-776.
• [6]Nishikawa AK, Taira T, Yoshizato K: In vitro maturation of collagen fibrils modulates spreading, DNA synthesis, and collagenolysis of epidermal cells and fibroblasts. Exp Cell Res 1987, 171:164-177.
• [7]Heimbach D, Luterman A, Burke J, Cram A, Herndon D, Hunt J, Jordan M, McManus W, Solem L, Warden G, Zawacki B: Artificial dermis for major burns. Ann Surg 1988, 208:313-320.
• [8]De Vries HJC, Middelkoop E, Mekkes JR, Dutrieux RP, Wildevuur CHR, Westerhof W: Dermal regeneration in native noncross-linked collagen sponges with diferent extracellular matrix molecules. Wound Repair Regen 1994, 2:37-47.
• [9]Nevins M, Kirkerhead C, Nevins M, Wozney JA, Palmer R: Bone formation in the goat maxillary sinus induced by absorbable collagen sponge implants impregnated with recombinant human bone morphogenetic protein-2. Int J Periodont Restorative Dent 1996, 16:9-19.
• [10]Stone KR, Steadman JR, Rodkey WG, Li ST: Regeneration of a meniscal cartilage with use of a collagen scaffold: analysis of preliminary data. J Bone Jt Surg 1997, 79A:1770-1777.
• [11]Speer DP, Chvapil M, Volz RG, Holmes MD: Enhancement of healing in osteochondral defects by collagen sponge implants. Clin Orthop Relat Res 1979, 144:326-335.
• [12]Natsume T, Ike O, Okada T, Takimoto N, Shimizu Y, Ikada Y: Porous collagen sponge for esophageal replacement. J Biomed Mater Res 1993, 27:867-875.
• [13]Narotam PK, Van Dellen JR, Bhoola KD: A clinicopathological study of collagen sponge as a dural graft in neurosurgery. J Neurosurg 1995, 82:406-412.
• [14]Van-Wachem PB, Van-Luyn MJA, Costa MLP: Myoblast seeding in a collagen matrix evaluated in vitro. J Biomed Mater Res 1996, 30:353-360.
• [15]Ding T, Lu WW, Zheng Y, Li ZY, Pan HB, Luo Z: Rapid repair of rat sciatic nerve injury using a nanosilver-embedded collagen scaffold coated with laminin and fibronectin. Regen Med 2011, 6:437-447.
• [16]Matsuda K, Suzuki S, Isshiki N, Yoshioka K, Okada T, Ikada Y: Influence of glycosaminoglycans on the collagen sponge component of a bilayer artificial skin. Biomaterials 1990, 11:351-355.
• [17]Srivastava S, Gorham SD, French DA, Shivas AA, Courtney JM: In vivo evaluation and comparison of collagen, acetylated collagen and collagen/glycosaminoglycan composite films and sponges as candidate biomaterials. Biomaterials 1990, 11:155-161.
• [18]Liu W, Deng C, McLaughlin CR, Fagerholm P, Lagali NS, Heyne B, Scaiano JC, Watsky MA, Kato Y, Munger R, Shinozaki N, Li F, Griffith M: Collagen-phosphorylcholine interpenetrating network hydrogels as corneal substitutes. Biomaterials 2009, 30:1551-1559.
• [19]Fagerholm P, Lagali NS, Merrett K, Jackson WB, Munger R, Liu Y, Polarek JW, Söderqvist M, Griffith M: A biosynthetic alternative to human donor tissue for inducing corneal regeneration: 24-month follow-up of a phase 1 clinical study. Sci Transl Med 2010, 2:46ra61.
• [20]Perng CK, Wang YJ, Tsi CH, Ma H: In vivo angiogenesis effect of porous collagen scaffold with hyaluronic acid oligosaccharides. J Surg Res 2011, 168:9-15.
• [21]Bakare RA, Bhan C, Raghavan D: Synthesis and characterization of collagen grafted Poly(hydroxybutyrate-valerate) (PHBV) scaffold for loading of bovine serum albumin capped silver (Ag/BSA) nanoparticles in the potential use of tissue engineering application. Biomacromolecules 2014, 15:423-435.
• [22]Jithendra P, Rajam AM, Kalaivani T, Mandal AB, Rose C: Preparation and characterization of aloe vera blended collagen-chitosan composite scaffold for tissue engineering applications. ACS Appl Mater Interfaces 2013, 5:7291-7298.
• [23]Hackenberg S, Scherzed A, Kessler M, Hummel S, Technau A, Froelich K, Ginzkey C, Koehler C, Hagen R, Kleinsasser N: Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol Lett 2011, 201:27-33.
• [24]Shang L, Wang Y, Huang L, Dong S: Preparation of DNA-silver nanohybrids in multilayer nanoreactors by in situ electrochemical reduction, characterization, and application. Langmuir 2007, 23:7738-7744.
• [25]Dipankar C, Murugan S: The green synthesis, characterization and evaluation of the biological activities of silver nanoparticles synthesized from Iresine herbstii leaf aqueous extracts. Colloids Surf B 2012, 98:112-119.
• [26]Neto EAB, Ribeiro C, Zucolotto V: Síntese de nanopartículas de prata para aplicação na sanitização de embalagens. [http://www.clickciencia.ufscar.br/portal/edicao19/Artigo.pdf] webciteEmbrapa 2008. http://www.clickciencia.ufscar.br/portal/edicao19/Artigo.pdf
• [27]Wong KKY, Liu X: Silver nanoparticles-the real ¿silver bullet¿ in clinical medicine? Med Chem Commun 2010, 1:125-131.
• [28]Chaloupka K, Malam Y, Seifalian AM: Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol 2010, 28:580-588.
• [29]Ahamed M, Alsalhi MS, Siddiqui MKJ: Silver nanoparticle applications and human health. Clin Chim Acta 2010, 411:1841-1848.
• [30]Lok C, Ho C, Chen R, He Q, Yu W, Sun H, Tam PK, Chiu J, Che C: Proteomic analysis of the mode of antibacterial action of silver research articles. J Proteome Res 2006, 5:916-924.
• [31]Shahverdi AR, Fakhimi A, Shahverdi HR, Minaian S: Synthesis and effect of silver nanoparticles on the antibacterial activity of different antibiotics against Staphylococcus aureus and Escherichia coli. Nanomedicine 2007, 3:168-171.
• [32]Panácek A, Kvítek L, Prucek R, Kolá? M, Vece?ová R, Pizúrová N, Sharma VK, Nev?cná TJ, Zbo?il R: Silver colloid nanoparticles: synthesis, characterization, and their antibacterial activity. J Phys Chem B 2006, 110:16248-16253.
• [33]Gnanadhas DP, Ben Thomas M, Thomas R, Raichur AM, Chakravortty D: Interaction of silver nanoparticles with serum proteins affects their antimicrobial activity in vivo. Antimicrob Agents Chemother 2013, 57:4945-4955.
• [34]Pal S, Tak YK, Song JM: Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl Environ Microbiol 2007, 73:1712-1720.
• [35]Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramírez JT, Yacaman MJ: The bactericidal effect of silver nanoparticles. Nanotechnology 2005, 16:2346-2353.
• [36]Kwan KHL, Liu X, To MKT, Yeung KWK, Ho C, Wong KKY: Modulation of collagen alignment by silver nanoparticles results in better mechanical properties in wound healing. Nanomedicine 2011, 7:497-504.
• [37]Alarcon EI, Udekwu K, Skog M, Pacioni NL, Stamplecoskie KG, González-Béjar M, Polisetti N, Wickham A, Richter-Dahlfors A, Griffith M, Scaiano JC: The biocompatibility and antibacterial properties of collagen-stabilized, photochemically prepared silver nanoparticles. Biomaterials 2012, 33:4947-4956.
• [38]Sun Y, Wang L, Sun L, Guo C, Yang T, Liu Z, Xu F, Li Z: Fabrication, characterization, and application in surface-enhanced Raman spectrum of assembled type-I collagen-silver nanoparticle multilayered films. J Chem Phys 2008, 128:074704.
• [39]Zhang Z, Wu Y: Investigation of the NaBH4-induced aggregation of Au nanoparticles. Langmuir 2010, 26:9214-9223.
• [40]Li Y, Douglas EP: Effects of various salts on structural polymorphism of reconstituted type I collagen fibrils. Colloids Surf B 2013, 112:42-50.
• [41]Sano S, Kato K, Ikada Y: Introduction of functional groups onto the surface of polyethylene for protein immobilization. Biomaterials 1993, 14:817-822.
• [42]Desai V, Kowshik M: Synthesis and characterization of fumaric acid functionalized AgCl/titania nanocomposite with enhanced antibacterial activity. J Nanosci Nanotechnol 2013, 13:2826-2834.
• [43]Prasad RY, McGee JK, Killius MG, Suarez DA, Blackman CF, DeMarini DM, Simmons SO: Investigating oxidative stress and inflammatory responses elicited by silver nanoparticles using high-throughput reporter genes in HepG2 cells: effect of size, surface coating, and intracellular uptake. Toxicol In Vitro 2013, 27:2013-2021.
• [44]Stevanovi? M, Bra?ko I, Milenkovi? M, Filipovi? N, Nuni? J, Filipi? M, Uskokovi? DP: Multifunctional PLGA particles containing poly(l-glutamic acid)-capped silver nanoparticles and ascorbic acid with simultaneous antioxidative and prolonged antimicrobial activity. Acta Biomater 2014, 10:151-162.
• [45]Hebeish A, El-Rafie MH, El-Sheikh MA, Seleem AA, El-Naggar ME: Antimicrobial wound dressing and anti-inflammatory efficacy of silver nanoparticles. Int J Biol Macromol 2014, 65:509-515.
• [46]Silva T, Pokhrel LR, Dubey B, Tolaymat TM, Maier KJ, Liu X: Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: comparison between general linear model-predicted and observed toxicity. Sci Total Environ 2014, 468¿469:968-976.
• [47]Kim JS, Kuk E, Yu KN, Kim JH, Park SJ, Lee HJ, Kim SH, Park YK, Park YH, Hwang CY, Kim YK, Lee YS, Jeong DH, Cho MH: Antimicrobial effects of silver nanoparticles. Nanomedicine 2007, 3:95-101.
• [48]Hamouda T, Baker JR: Antimicrobial mechanism of action of surfactant lipid preparations in enteric Gram-negative bacilli. J Appl Microbiol 2000, 89:397-403.
• [49]Shang L, Nienhaus K, Nienhaus GU: Engineered nanoparticles interacting with cells: size matters. J Nanobiotechnol 2014, 12:5. BioMed Central Full Text
• [50]Baker C, Pradhan A, Parkstis L, Pochan DJ, Shah SI: Synthesis and antibacterial properties of silver nanoparticles. J Nanosci Nanotechnol 2005, 5(2):244-249.
• [51]Saptarshi SR, Duschl A, Lopata AL: Interaction of nanoparticles with proteins: relation to bio-reactivity of the nanoparticle. J Nanobiotechnol 2013, 11:26. BioMed Central Full Text
• [52]Gao X, Gu G, Hu Z, Guo Y, Fu X, Song J: A simple method for preparation of silver dendrites. Colloids Surfaces A Physicochem Eng Asp 2005, 254:57-61.
• [53]Sileikait? A, Prosy?evas I, Pui¿o J, Juraitis A, Guobien? A: Analysis of silver nanoparticles produced by chemical reduction of silver salt solution. Mater Sci (Medziagotyra) 2006, 12(4):287-291.
• [54]Yamamoto SY, Ujiwara KF, Atarai HW: Surface-enhanced Raman scattering from oleate-stabilized silver colloids at a liquid/liquid interface. Anal Sci 2004, 20(September):1347-1352.
• [55]Zaheer K, Shaeel AA, Abdullah YO, Ziya AK, Abdulrahman AOA: Shape-directing role of cetyltrimethylammonium bromide in the preparation of silver nanoparticles. J Colloid Interface Sci 2012, 367:101-108.
• [56]Lara HH, Garza-Treviño EN, Ixtepan-Turrent L, Singh DK: Silver nanoparticles are broad-spectrum bactericidal and virucidal compounds. J Nanobiotechnol 2011, 9:30. BioMed Central Full Text
• [57]Kato H, Nakamura A, Takahashi K, Kinugasa S: Accurate size and size-distribution determination of polystyrene latex nanoparticles in aqueous medium using dynamic light scattering and asymmetrical flow field flow fractionation with multi-angle light scattering. Nanomaterials 2012, 2:15-30.
• [58]Gurunathan S, Han JW, Eppakayala V, Jeyaraj M, Kim JH: Cytotoxicity of biologically synthesized silver nanoparticles in MDA-MB-231 human breast cancer cells. Biomed Res Int 2013, 2013:535796.
• [59]Prokopovich P, Leech R, Carmalt CJ, Parkin IP, Perni S: A novel bone cement impregnated with silver ¿ tiopronin nanoparticles: its antimicrobial, cytotoxic, and mechanical properties. Int J Nanomed 2013, 8:2227-2237.
• [60]PEAK Fitting Module. Northampton: OriginLab Corporation, One Roundhouse Plaza; 2002.
• [61][http:/ / antimicrobianos.com.ar/ ATB/ wp-content/ uploads/ 2012/ 11/ 03-CLSI-M07-A9-2012.pdf] webcite CLSI-Clinical Laboratory Standards Institute: Methods for Dilution Antimicrobial Susceptibility Test for Bacteria that Grow Aerobically. Available online: (accessed on 18 September 2013).
• [62]Quelemes PV, Araruna FB, de Faria BEF, Kuckelhaus SAS, da Silva DA, Mendonça RZ, Eiras C, Soares MJS, Leite JRSA: Development and antibacterial activity of cashew gum-based silver nanoparticles. Int J Mol Sci 2013, 14:4969-4981.
• [63]Guzman M, Dille J, Godet S: Synthesis and antibacterial activity of silver nanoparticles against gram-positive and gram-negative bacteria. Nanomedicine 2012, 8:37-45.
• [64]Falqueiro AM, Siqueira-Moura MP, Jardim DR, Primo FL, Morais PC, Mosiniewicz-Szablewska E, Suchocki P, Tedesco AC: In vitro cytotoxicity of Selol-loaded magnetic nanocapsules against neoplastic cell lines under AC magnetic field activation. J Appl Phys 2012, 111:07B335.