Abstract
The ability to investigate substances at the molecular level has boosted the search for materials with outstanding properties for use in medicine. The application of these novel materials has generated the new research field of nanobiotechnology, which plays a central role in disease diagnosis, drug design and delivery, and implants. In this review, we provide an overview of the use of metallic and metal oxide nanoparticles, carbon-nanotubes, liposomes, and nanopatterned flat surfaces for specific biomedical applications. The chemical and physical properties of the surface of these materials allow their use in diagnosis, biosensing and bioimaging devices, drug delivery systems, and bone substitute implants. The toxicology of these particles is also discussed in the light of a new field referred to as nanotoxicology that studies the surface effects emerging from nanostructured materials.
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Abukabda AB, Stapleton PA, Nurkiewicz TR (2016) Metal nanomaterial toxicity variations within the vascular system. Curr Environ Health Rep 3:379–391. doi:10.1007/s40572-016-0112-1
Akbarzadeh A, Rezaei-sadabady R, Davaran S et al (2013) Liposome : classification, preparation, and applications. Nanoscale Res Lett 8:1. doi:10.1186/1556-276X-8-102
Albrektsson T, Brånemark P, Hansson H, Lindström J (1981) Osseointegrated titanium implants: requirements for ensuring a long-lasting, direct bone-to-implant anchorage in man. Acta Orthop 52:155–170. doi:10.3109/17453678108991776
Alt V, Bechert T, Steinrücke P et al (2004) An in vitro assessment of the antibacterial properties and cytotoxicity of nanoparticulate silver bone cement. Biomaterials 25:4383–4391. doi:10.1016/j.biomaterials.2003.10.078
Anselme K (2000) Osteoblast adhesion on biomaterials. Biomaterials 21:667–681. doi:10.1016/S0142-9612(99)00242-2
Anselme K, Bigerelle M, Noel B et al (2000) Qualitative and quantitative study of human osteoblast adhesion on materials with various surface roughnesses. J Biomed Mater Res 49:155–166. doi:10.1002/(SICI)1097-4636(200002)49:2<155::AID-JBM2>3.0.CO;2-J
Arima Y, Iwata H (2007) Effect of wettability and surface functional groups on protein adsorption and cell adhesion using well-defined mixed self-assembled monolayers. Biomaterials 28:3074–82. doi:10.1016/j.biomaterials.2007.03.013
Bangham AD, Horne RW (1964) Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J Mol Biol 8:660–668. doi:10.1016/S0022-2836(64)80115-7
Barbosa SC, Cilli EM, Dias LG et al (2011) Labaditin, a cyclic peptide with rich biotechnological potential: preliminary toxicological studies and structural changes in water and lipid membrane environment. Amino Acids 40:135–144. doi:10.1007/s00726-010-0648-6
Benech RO, Kheadr EE, Lacroix C et al (2002) Antibacterial activities of nisin Z encapsulated in liposomes or produced in situ by mixed culture during cheddar cheese ripening antibacterial activities of nisin Z encapsulated in liposomes or produced in situ by mixed culture during cheddar cheese ripe. Appl Environ Microbiol 68:5607–5619. doi:10.1128/AEM.68.8.3683
Berg JM, Eriksson LGT, Claesson PM, Borve KGN (1994) Three-component langmuir-blodgett films with a controllable degree of polarity. Langmuir 10:1225–1234. doi:10.1021/la00016a041
Bhattacharya R, Mukherjee P (2008) Biological properties of “naked” metal nanoparticles. Adv Drug Deliv Rev 60:1289–1306. doi:10.1016/j.addr.2008.03.013
Bilia AR, Guccione C, Isacchi B et al (2014) Essential oils loaded in nanosystems: a developing strategy for a successful therapeutic approach. Evid Based Complement Alternat Med. doi:10.1155/2014/651593
Bolean M, Simão AMS, Favarin BZ et al (2010) The effect of cholesterol on the reconstitution of alkaline phosphatase into liposomes. Biophys Chem 152:74–79. doi:10.1016/j.bpc.2010.08.002
Bolean M, Simão A, Favarin B (2011) Thermodynamic properties and characterization of proteoliposomes rich in microdomains carrying alkaline phosphatase. Biophys Chem 158:111–118. doi:10.1016/j.bpc.2011.05.019
Bolean M, Simão AMS, Kiffer-Moreira T et al (2015) Proteoliposomes with the ability to transport Ca2+ into the vesicles and hydrolyze phosphosubstrates on their surface. Arch Biochem Biophys 584:79–89. doi:10.1016/j.abb.2015.08.018
Bolfarini GC, Siqueira-Moura MP, Demets GJF et al (2012) In vitro evaluation of combined hyperthermia and photodynamic effects using magnetoliposomes loaded with cucurbituril zinc phthalocyanine complex on melanoma. J Photochem Photobiol B 115:1–4. doi:10.1016/j.jphotobiol.2012.05.009
Boyan BD, Dean DD, Lohmann CH, et al. (2001) The titanium–bone cell interface in vitro: the role of the surface in promoting osteointegration. In: Brunette DM, Tengvall P, Textor M, Thomsen P (eds) Titanium in medicine. Springer, Berlin, Heidelberg, pp 561–585
Brammer KS, Frandsen CJ, Jin S (2012) TiO2 nanotubes for bone regeneration. Trends Biotechnol 30:315–322. doi:10.1016/j.tibtech.2012.02.005
Brett PM, Harle J, Salih V et al (2004) Roughness response genes in osteoblasts. Bone 35:124–33. doi:10.1016/j.bone.2004.03.009
Brunetti V, Maiorano G, Rizzello L et al (2010) Neurons sense nanoscale roughness with nanometer sensitivity. Proc Natl Acad Sci USA 107:6264–6269. doi:10.1073/pnas.0914456107
Camolezi FL, Daghastanli KRP, Magalhães PP et al (2002) Construction of an alkaline phosphatase-liposome system: a tool for biomineralization study. Int J Biochem Cell Biol 34:1091–1101. doi:10.1016/S1357-2725(02)00029-8
Carlson C, Hussain SM, Schrand AM et al (2008) Unique cellular interaction of silver nanoparticles : size-dependent generation of reactive oxygen species unique cellular interaction of silver nanoparticles : size-dependent generation of reactive. J Phys Chem B 112:13608–13619. doi:10.1021/jp712087m
Caseli L, Nobre TM, Ramos AP et al (2015) The role of langmuir monolayers to understand biological events. ACS Symp Ser 1215:65–88. doi:10.1021/bk-2015-1215.ch004
Castner DG, Ratner BD (2002) Biomedical surface science: foundations to frontiers. Surface Sci 500(1–3):28–60
Cedervall T, Lynch I, Lindman S et al (2007) Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci USA 104:2050–2055. doi:10.1073/pnas.0608582104
Chaloupka K, Malam Y, Seifalian AM (2010) Nanosilver as a new generation of nanoproduct in biomedical applications. Trends Biotechnol 28:580–588. doi:10.1016/j.tibtech.2010.07.006
Chen X, Schluesener HJ (2008) Nanosilver: a nanoproduct in medical application. Toxicol Lett 176:1–12. doi:10.1016/j.toxlet.2007.10.004
Chen Z, Kang L, Wang Z et al (2014) Recent progress in the research of biomaterials regulating cell behavior. RSC Adv 4:63807–63816. doi:10.1039/C4RA05534A
Ciancaglini P, Simão AMS, Bolean M et al (2012) Proteoliposomes in nanobiotechnology. Biophys Rev 4:67–81. doi:10.1007/s12551-011-0065-4
Costa N, Maquis PM (1998) Biomimetic processing of calcium phosphate coating. Med Eng Phys 20:602–606
Costa DO, Allo BA, Klassen R et al (2012) Control of surface topography in biomimetic calcium phosphate coatings. Langmuir 28:3871–3880. doi:10.1021/la203224a
Cruz MAE, Ramos AP (2016) Bioactive CaCO3/poly(acrylic acid)/chitosan hybrid coatings deposited on titanium. Surf Coat Technol 294:145–152. doi:10.1016/j.surfcoat.2016.03.084
Cruz MAE, Ruiz GCM, Faria AN et al (2016) Calcium carbonate hybrid coating promotes the formation of biomimetic hydroxyapatite on titanium surfaces. Appl Surf Sci 370:459–468. doi:10.1016/j.apsusc.2015.12.250
Cüneyt Tas A (2000) Synthesis of biomimetic Ca-hydroxyapatite powders at 37°C in synthetic body fluids. Biomaterials 21:1429–1438. doi:10.1016/S0142-9612(00)00019-3
Daghastanli KRP, Ferreira RB, Thedei G et al (2004) Lipid composition-dependent incorporation of multiple membrane proteins into liposomes. Colloids Surf B Biointerfaces 36:127–137. doi:10.1016/j.colsurfb.2004.03.015
De Lima SH, Lopes ML, Maggio B, Ciancaglini P (2005) Na, K-ATPase reconstituted in liposomes: Effects of lipid composition on hydrolytic activity and enzyme orientation. Colloids Surf B Biointerfaces 41:239–248. doi:10.1016/j.colsurfb.2004.12.013
de Souza ID, Cruz MAE, de Faria AN et al (2014a) Formation of carbonated hydroxyapatite films on metallic surfaces using dihexadecyl phosphate-LB film as template. Colloids Surf B Biointerfaces 118C:31–40. doi:10.1016/j.colsurfb.2014.03.029
de Souza ID, Cruz MAE, de Faria AN et al (2014b) Formation of carbonated hydroxyapatite films on metallic surfaces using dihexadecyl phosphate-LB film as template. Colloids Surf B Biointerfaces 118:31–40. doi:10.1016/j.colsurfb.2014.03.029
Decher G, Hong JD, Schmitt J (1992) Buildup of ultrathin multilayer films by a self-assembly process : III.Consecutively alternating adsorption of anionic and cationic polyelectrolytes on charged surfaces. Thin Solid Films 210–211:831–835
Decher G, Eckle M, Schmitt J, Struth B (1998) Layer-by-layer assembled multicomposite films. Curr Opin Colloid Interface Sci 3:32–39. doi:10.1016/S1359-0294(98)80039-3
Deng Z, Mortimer G, Schiller T (2009) Differential plasma protein binding to metal oxide nanoparticles. Nanotechnology 20:455101. doi:10.1088/0957-4484/20/45/455101
Dhawan A, Sharma V, Parmar D (2009) Nanomaterials: a challenge for toxicologists. Nanotoxicology 3:1–9. doi:10.1080/17435390802578595
Dong Y, Yang J, Zhang J, Zhang X (2016) Nano-delivery vehicles/adjuvants for DNA vaccination against HIV. J Nanosci Nanotechnol 16:2126–2133. doi:10.1166/jnn.2016.10947
Ehrlich H (2010) Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev 52:661–699. doi:10.1080/00206811003679521
Elkhodiry MA, Momah CC, Suwaidi SR et al (2016) Synergistic nanomedicine: passive, active, and ultrasound-triggered drug delivery in cancer treatment. J Nanosci Nanotechnol 16:1–18. doi:10.1166/jnn.2016.11124
Elsaesser A, Howard CV (2012) Toxicology of nanoparticles. Adv Drug Deliv Rev 64:129–137. doi:10.1016/j.addr.2011.09.001
Fadeel B, Garcia-Bennett AE (2010) Better safe than sorry: understanding the toxicological properties of inorganic nanoparticles manufactured for biomedical applications. Adv Drug Deliv Rev 62:362–374. doi:10.1016/j.addr.2009.11.008
Faraji AH, Wipf P (2009) Nanoparticles in cellular drug delivery. Bioorg Med Chem 17:2950–2962. doi:10.1016/j.bmc.2009.02.043
Faria PEP, Felipucci DNB, Simioni AR et al (2015) Effects of photodynamic process (PDP) in implant osseointegration: a histologic and histometric study in dogs. Clin Implant Dent Relat Res 17:879–890. doi:10.1111/cid.12204
Faucheux N, Schweiss R, Lützow K et al (2004) Self-assembled monolayers with different terminating groups as model substrates for cell adhesion studies. Biomaterials 25:2721–2730. doi:10.1016/j.biomaterials.2003.09.069
Fei Yin Z, Wu L, Gui Yang H, Hua Su Y (2013) Recent progress in biomedical applications of titanium dioxide. Phys Chem Chem Phys 15:4844. doi:10.1039/c3cp43938k
Feng B, Weng J, Yang BC et al (2003) Characterization of surface oxide films on titanium and adhesion of osteoblast. Biomaterials 24:4663–4670. doi:10.1016/S0142-9612(03)00366-1
Ferris DM, Moodie GD, Dimond PM et al (1999) RGD-coated titanium implants stimulate increased bone formation in vivo. Biomaterials 20:2323–2331
Fricain JC, Bareille R, Ulysse F et al (1998) Evaluation of proliferation and protein expression of human bone marrow cells cultured on coral crystallized in the aragonite of calcite form. J Biomed Mater Res 42:96–102. doi:10.1002/(SICI)1097-4636(199810)42:1<96::AID-JBM12>3.0.CO;2-M
Fujihara K, Kotaki M, Ramakrishna S (2005) Guided bone regeneration membrane made of polycaprolactone/calcium carbonate composite nano-fibers. Biomaterials 26:4139–4147. doi:10.1016/j.biomaterials.2004.09.014
Gao W, Thamphiwatana S, Angsantikul P, Zhang L (2014) Nanoparticle approaches against bacterial infections. Wiley Interdiscip Rev Nanomedicine Nanobiotechnol 6:532–547. doi:10.1002/wnan.1282
Ghalandarlaki N, Alizadeh AM, Ashkani-Esfahani S (2014) Nanotechnology-applied curcumin for different diseases therapy. Biomed Res Int 2014:394264. doi:10.1155/2014/394264
Guidelli EJ, Ramos AP, Zaniquelli MED, Baffa O (2011) Green synthesis of colloidal silver nanoparticles using natural rubber latex extracted from hevea brasiliensis. Spectrochim Acta A Mol Biomol Spectrosc 82:140–145. doi:10.1016/j.saa.2011.07.024
Guidelli EJ, Ramos AP, Zaniquelli MED et al (2012) Synthesis and characterization of silver/alanine nanocomposites for radiation detection in medical applications: the influence of particle size on the detection properties. Nanoscale 4:2884–2893. doi:10.1039/c2nr30090g
Guidelli ÉJ, Kinoshita A, Ramos AP, Baffa O (2013) Silver nanoparticles delivery system based on natural rubber latex membranes. J Nanoparticle Res 15:1536. doi:10.1007/s11051-013-1536-2
Guidelli EJ, Ramos AP, Baffa O (2016) Silver nanoparticle films for metal enhanced luminescence: toward development of plasmonic radiation detectors for medical applications. Sensors Actuators B Chem 224:248–255. doi:10.1016/j.snb.2015.10.024
Gupta AK, Gupta M (2005) Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 26:3995–4021. doi:10.1016/j.biomaterials.2004.10.012
Gupta AK, Naregalkar RR, Vaidya VD, Gupta M (2007) Recent advances on surface engineering of magnetic iron oxide nanoparticles and their biomedical applications. Nanomedicine 2:23–39. doi:10.2217/17435889.2.1.23
Han YJ, Aizenberg J (2003) Face-selective nucleation of calcite on self-assembled monolayers of alkanethiols: effect of the parity of the alkyl chain. Angew Chem Int Ed 42:3668–3670. doi:10.1002/anie.200351655
Hanawa T (2011) A comprehensive review of techniques for biofunctionalization of titanium. J Periodontal Implant Sci 41:263–272. doi:10.5051/jpis.2011.41.6.263
Hartono D, Qin WJ, Yang KL, Yung LYL (2009) Imaging the disruption of phospholipid monolayer by protein-coated nanoparticles using ordering transitions of liquid crystals. Biomaterials 30:843–849. doi:10.1016/j.biomaterials.2008.10.037
He J, Zhou W, Zhou X et al (2008) The anatase phase of nanotopography titania plays an important role on osteoblast cell morphology and proliferation. J Mater Sci Mater Med 19:3465–3472. doi:10.1007/s10856-008-3505-3
Hendesi H, Barbe MF, Safadi FF et al (2015) Integrin mediated adhesion of osteoblasts to connective tissue growth factor (CTGF/CCN2) induces cytoskeleton reorganization and cell differentiation. PLoS One 10:1–20. doi:10.1371/journal.pone.0115325
Hong H, Shi J, Yang Y et al (2011) Cancer-targeted optical imaging with fluorescent zinc oxide nanowires. Nano Lett 11:3744–3750. doi:10.1021/nl201782m
Hotchkiss KM, Reddy GB, Hyzy SL et al (2016) Titanium surface characteristics, including topography and wettability, alter macrophage activation. Acta Biomater 31:425–434. doi:10.1016/j.actbio.2015.12.003
Ierardi DF, Pizauro JM, Ciancaglini P (2002) Erythrocyte ghost cell-alkaline phosphatase: construction and characterization of a vesicular system for use in biomineralization studies. Biochim Biophys Acta Biomembr 1567:183–192. doi:10.1016/S0005-2736(02)00615-6
Jalota S, Bhaduri S, Tas A (2007) Osteoblast proliferation on neat and apatite-like calcium phosphate-coated titanium foam scaffolds. Mater Sci Eng C 27:432–440. doi:10.1016/j.msec.2006.05.052
Jayaraman M, Meyer U, Bühner M et al (2004) Influence of titanium surfaces on attachment of osteoblast-like cells in vitro. Biomaterials 25:625–631. doi:10.1016/S0142-9612(03)00571-4
Jiang J, Oberdörster G, Elder A et al (2008) Does nanoparticle activity depend upon size and crystal phase? Nanotoxicology 2:33–42. doi:10.1080/17435390701882478
Jin HE, Jang J, Chung J et al (2015) Biomimetic self-templated hierarchical structures of collagen-like peptide amphiphiles. Nano Lett 15:7138–7145. doi:10.1021/acs.nanolett.5b03313
Karmali PP, Simberg D (2011) Interactions of nanoparticles with plasma proteins: implication on clearance and toxicity of drug delivery systems. Expert Opin Drug Deliv 8:343–357. doi:10.1517/17425247.2011.554818
Kasemo B (2002) Biological surface science. Surf Sci 500:656–677. doi:10.1016/S0039-6028(01)01809-X
Khang D, Choi J, Im Y-M et al (2012) Role of subnano-, nano- and submicron-surface features on osteoblast differentiation of bone marrow mesenchymal stem cells. Biomaterials 33:5997–6007. doi:10.1016/j.biomaterials.2012.05.005
Kilpadi KL, Chang PL, Bellis SL (2001) Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. J Biomed Mater Res 57:258–267. doi:10.1002/1097-4636(200111)57:2<258::AID-JBM1166>3.0.CO;2-R
Kim JS, Yoon T-J, Yu KN et al (2005) Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol Sci 89:338–347. doi:10.1093/toxsci/kfj027
Klymov A, Prodanov L, Lamers E et al (2013) Understanding the role of nano-topography on the surface of a bone-implant. Biomater Sci 1:135–151. doi:10.1039/C2BM00032F
Koch FP, Weng D, Krämer S et al (2010) Osseointegration of one-piece zirconia implants compared with a titanium implant of identical design: a histomorphometric study in the dog. Clin Oral Implants Res 21:350–356. doi:10.1111/j.1600-0501.2009.01832.x
Kokubo T, Takadama H (2006) How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27:2907–2915. doi:10.1016/j.biomaterials.2006.01.017
Kokubo T, Kushitani H, Sakka S et al (1990) Solutions able to reproduce in vivo surface-structure changes in bioactive glass-ceramic A-W3. J Biomed Mater Res 24:721–734. doi:10.1002/jbm.820240607
Kroll A, Pillukat MH, Hahn D, Schnekenburger J (2009) Current in vitro methods in nanoparticle risk assessment: limitations and challenges. Eur J Pharm Biopharm 72:370–377. doi:10.1016/j.ejpb.2008.08.009
Krug HF, Wick P (2011) Nanotoxicology: an interdisciplinary challenge. Angew Chem Int Ed 50:1260–1278. doi:10.1002/anie.201001037
Kubota S, Johkura K, Asanuma K et al (2004) Titanium oxide nanotubes for bone regeneration. J Mater Sci Mater Med 15:1031–1035. doi:10.1023/B:JMSM.0000042689.78768.77
Kuna JJ, Voïtchovsky K, Singh C et al (2009) The effect of nanometre-scale structure on interfacial energy. Nat Mater 8:837–842. doi:10.1038/nmat2534
Kunzmann A, Andersson B, Thurnherr T et al (2011) Toxicology of engineered nanomaterials: focus on biocompatibility, biodistribution and biodegradation. Biochim Biophys Acta Gen Subj 1810:361–373. doi:10.1016/j.bbagen.2010.04.007
Kwok DY, Neumann AW (1999) Contact angle measurement and contact angle interpretation. Adv Colloid Interface Sci 81:167–249. doi:10.1016/S0001-8686(98)00087-6
Lampin M, Warocquier-Clérout LC et al (1997) Correlation between substratum roughness and wettability, cell adhesion, and cell migration. J Biomed Mater Res 36:99–108
Le Guéhennec L, Soueidan A, Layrolle P, Amouriq Y (2007) Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater 23:844–854. doi:10.1016/j.dental.2006.06.025
Liao H, Nehl CL, Hafner JH (2006) Biomedical applications of plasmon resonant metal nanoparticles. Nanomedicine (London) 1:201–208. doi:10.2217/17435889.1.2.201
Lim JY, Taylor AF, Li Z et al (2005) Integrin expression and osteopontin regulation in human fetal osteoblastic cells mediated by substratum surface characteristics. Tissue Eng 11:19–29. doi:10.1089/ten.2005.11.19
Liu D, Yang F, Xiong F, Gu N (2016a) The smart drug delivery system and its clinical potential. Theranostics 6:1306–1323. doi:10.7150/thno.14858
Liu H, Zhang J, Chen X et al (2016b) Application of iron oxide nanoparticles in glioma imaging and therapy: from bench to bedside. Nanoscale 8:7808–7826. doi:10.1039/c6nr00147e
Liu T-Y, Liao H-C, Lin C-C et al (2006) Biofunctional ZnO nanorod arrays grown on flexible substrates. Langmuir 22:5804–5809. doi:10.1021/la052363o
Liu Y, Chen C (2015) Role of nanotechnology in HIV/AIDS vaccine development. Adv Drug Deliv Rev 103:76–89. doi:10.1016/j.addr.2016.02.010
Longo JPF, Leal SC, Simioni AR et al (2012) Photodynamic therapy disinfection of carious tissue mediated by aluminum-chloride-phthalocyanine entrapped in cationic liposomes: an in vitro and clinical study. Lasers Med Sci 27:575–584. doi:10.1007/s10103-011-0962-6
Lopez E, Vidal B, Berland S et al (1992) Demonstration of the capacity of nacre to induce bone formation by human osteoblasts maintained in vitro. Tissue Cell 24:667–679. doi:10.1016/0040-8166(92)90037-8
Lundqvist M, Stigler J, Cedervall T et al (2011) The evolution of the protein corona arouns nanoparticles: a test study. ACS Nano 5:7503–7509
Lvov Y, Ariga K, Ichinose I, Kunitake T (1995) Assembly of multicomponent protein films by means of electrostatic layer-by-layer adsorption. J Am Chem Soc 117:6117–6123. doi:10.1021/ja00127a026
Lynch I, Dawson KA (2008) The key role of protein-nanoparticle interactions in nanomedicine and. Nano Today 3:40–47
Madni MA, Sarfraz M, Rehman M et al (2014) Liposomal drug delivery: a versatile platform for challenging clinical applications. J Pharm Pharm Sci 17:401–426
Mahmoudi M, Hofmann H, Rothen-Rutishauser B, Petri-Fink A (2012) Assessing the in vitro and in vivo toxicity of superparamagnetic iron oxide nanoparticles. Chem Rev 112:2323–2338. doi:10.1021/cr2002596
Martin JY, Schwartz Z, Hummert TW et al (1995) Effect of titanium surface roughness on proliferation, differentiation, and protein synthesis of human osteoblast-like cells (MG63). J Biomed Mater Res 29:389–401. doi:10.1002/jbm.820290314
McNamara LE, McMurray RJ, Biggs MJP et al (2010) Nanotopographical control of stem cell differentiation. J Tissue Eng 2010:120623. doi:10.4061/2010/120623
Menzies KL, Jones L (2010) The impact of contact angle on the biocompatibility of biomaterials. Optom Vis Sci 87:387–399. doi:10.1097/OPX.0b013e3181da863e
Moyano DF, Rotello VM (2011) Nano meets biology: structure and function at the nanoparticle interface. Langmuir 27:10376–10385. doi:10.1021/la2004535
Nogueira LFB, Maniglia BC, Pereira LS et al (2016) Formation of carrageenan-CaCO3 bioactive membranes. Mater Sci Eng C 58:1–6. doi:10.1016/j.msec.2015.08.021
Nowack B, Bucheli TD (2007) Occurrence, behavior and effects of nanoparticles in the environment. Environ Pollut 150:5–22. doi:10.1016/j.envpol.2007.06.006
Oberdörster G (2010) Safety assessment for nanotechnology and nanomedicine: concepts of nanotoxicology. J Intern Med 267:89–105. doi:10.1111/j.1365-2796.2009.02187.x
Oh J, Feldman MD, Kim J et al (2006) Detection of magnetic nanoparticles in tissue using magneto-motive ultrasound. Nanotechnology 17:4183–4190. doi:10.1088/0957-4484/17/16/031
Olszta MJ, Cheng X, Jee SS et al (2007) Bone structure and formation: a new perspective. Mater Sci Eng R Rep 58:77–116. doi:10.1016/j.mser.2007.05.001
Özkurt Z, Kazazoğlu E (2011) Zirconia dental implants: a literature review. J Oral Implantol 37:367–376. doi:10.1563/AAID-JOI-D-09-00079
Pantarotto D, Briand J-P, Prato M, Bianco A (2004a) Translocation of bioactive peptides across cell membranes by carbon nanotubes. Chem Commun (Camb) 1:16–17. doi:10.1039/b311254c
Pantarotto D, Singh R, McCarthy D et al (2004b) Functionalized carbon nanotubes for plasmid DNA gene delivery. Angew Chem Int Ed 43:5242–5246. doi:10.1002/anie.200460437
Pastorin G, Wu W, Wieckowski S et al (2006) Double functionalization of carbon nanotubes for multimodal drug delivery. Chem Commun (Camb) 1:1182–1184. doi:10.1039/b516309a
Pastorino L, Dellacasa E, Scaglione S et al (2014) Oriented collagen nanocoatings for tissue engineering. Colloids Surf B: Biointerfaces 114:372–378. doi:10.1016/j.colsurfb.2013.10.026
Piattelli A, Podda G, Scarano A (1997) Clinical and histological results in alveolar ridge enlargement using coralline calcium carbonate. Biomaterials 18:623–627. doi:10.1016/S0142-9612(96)00158-5
Prato M, Kostarelos K, Bianco A (2008) Functionalized carbon nanotubes in drug design and discovery. Acc Chem Res 41:60–68
Puleo DA, Nanci A (1999) Understanding and controlling the bone–implant interface. Biomaterials 20:2311–2321
Quéré D (2008) Wetting and roughness. Annu Rev Mater Res 38:71–99. doi:10.1146/annurev.matsci.38.060407.132434
Rack HJ, Qazi JI (2006) Titanium alloys for biomedical applications. Mater Sci Eng C 26:1269–1277. doi:10.1016/j.msec.2005.08.032
Rammelt S, Illert T, Bierbaum S et al (2006) Coating of titanium implants with collagen, RGD peptide and chondroitin sulfate. Biomaterials 27:5561–5571. doi:10.1016/j.biomaterials.2006.06.034
Ramos AP, Nobre TM, Montoro LA, Zaniquelli MED (2008) Calcium carbonate particle growth depending on coupling among adjacent layers in hybrid LB/LbL films. J Phys Chem B 112:14648–54. doi:10.1021/jp8023793
Ramos AP, Espimpolo DM, Zaniquelli MED (2012) Influence of the type of phospholipid head and of the conformation of the polyelectrolyte on the growth of calcium carbonate thin films on LB/LbL matrices. Colloids Surf B: Biointerfaces 95:178–185. doi:10.1016/j.colsurfb.2012.02.040
Ravi-Kumar MN (2000) Nano and microparticles as controlled drug delivery devices. J Pharm Pharm Sci 3:234–258
Reimhult E (2015) Nanoparticle-triggered release from lipid membrane vesicles. New Biotechnol 32:665–672. doi:10.1016/j.nbt.2014.12.002
Riehle MO, Dalby MJ, Johnstone H et al (2003) Cell behaviour of rat calvaria bone cells on surfaces with random nanometric features. Mater Sci Eng C 23:337–340. doi:10.1016/S0928-4931(02)00282-5
Rigos CF, Nobre TM, Zaniquelli MED et al (2008) The association of Na, K-ATPase subunits studied by circular dichroism, surface tension and dilatational elasticity. J Colloid Interface Sci 325:478–484. doi:10.1016/j.jcis.2008.06.011
Rosales-Leal JI, Rodríguez-Valverde MA, Mazzaglia G et al (2010) Effect of roughness, wettability and morphology of engineered titanium surfaces on osteoblast-like cell adhesion. Colloids Surf A Physicochem Eng Asp 365:222–229. doi:10.1016/j.colsurfa.2009.12.017
Saji VS, Choe HC, Young KWK (2010) Nanotechnology in biomedical applications—a review. Int J Nano Biomater 3:119–139
Santos LER, Colhone MC, Daghastanli KRP et al (2009) Lipid microspheres loaded with antigenic membrane proteins of the leishmania amazonensis as a potential biotechnology application. J Colloid Interface Sci 340:112–118. doi:10.1016/j.jcis.2009.08.025
Sato M, Slamovich EB, Webster TJ (2005) Enhanced osteoblast adhesion on hydrothermally treated hydroxyapatite/titania/poly(lactide-co-glycolide) sol–gel titanium coatings. Biomaterials 26:1349–1357. doi:10.1016/j.biomaterials.2004.04.044
Schmidt RC, Healy KE (2009) Controlling biological interfaces on the nanometer length scale. Biomed Mater Res A 90:1252–1261. doi:10.1002/jbm.a.32501
Sharma P, Mehra NK, Jain K, Jain N (2016) Biomedical applications of carbon nanotubes: a critical review. Curr Drug Deliv 13:796–817
Shehata T, Ogawara K, Higaki K, Kimura T (2008) Prolongation of residence time of liposome by surface-modification with mixture of hydrophilic polymers. Int J Pharm 359:272–279. doi:10.1016/j.ijpharm.2008.04.004
Simão AMS, Yadav MC, Ciancaglini P, Millán JL (2010a) Proteoliposomes as matrix vesicles’ biomimetics to study the initiation of skeletal mineralization. Braz J Med Biol Res 43:234–241. doi:10.1590/S0100-879X2010007500008
Simão AMS, Yadav MC, Narisawa S et al (2010b) Proteoliposomes harboring alkaline phosphatase and nucleotide pyrophosphatase as matrix vesicle biomimetics. J Biol Chem 285:7598–7609. doi:10.1074/jbc.M109.079830
Simão AMS, Bolean M, Cury TAC et al (2015) Liposomal systems as carriers for bioactive compounds. Biophys Rev 7:391–397. doi:10.1007/s12551-015-0180-8
Surmenev RA (2011) A review of plasma-assisted methods for calcium phosphate-based coatings fabrication. Surf Coat Technol 206:2035–2056. doi:10.1016/j.surfcoat.2011.11.002
Surmenev RA, Surmeneva MA, Ivanova AA (2014) Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis: a review. Acta Biomater 10:557–579. doi:10.1016/j.actbio.2013.10.036
Tan AW, Pingguan-Murphy B, Ahmad R, Akbar SA (2012) Review of titania nanotubes: fabrication and cellular response. Ceram Int 38:4421–4435. doi:10.1016/j.ceramint.2012.03.002
Tanahashi M, Matsuda T (1997) Surface functional group dependence on apatite formation on self-assembled monolayers in a simulated body fluid. J Biomed Mater Res 34:305–315. doi:10.1002/(SICI)1097-4636(19970305)34:3<305::AID-JBM5>3.0.CO;2-O
Tas AC (2014) The use of physiological solutions or media in calcium phosphate synthesis and processing. Acta Biomater 10:1771–1792. doi:10.1016/j.actbio.2013.12.047
Tian J, Wong KKY, Ho CM et al (2007) Topical delivery of silver nanoparticles promotes wound healing. ChemMedChem 2:129–136. doi:10.1002/cmdc.200600171
Tirrell M, Kokkoli E, Biesalski M (2002) The role of surface science in bioengineered materials. Surf Sci 500:61–83. doi:10.1016/S0039-6028(01)01548-5
Tovani CB, Zancanela DC, Faria AN et al (2016) Bio-inspired synthesis of hybrid tube-like structures based on CaCO 3 and type I-collagen. RSC Adv 6:90509–90515. doi:10.1039/C6RA18984A
Verma A, Stellacci F (2010) Effect of surface properties on nanoparticle-cell interactions. Small 6:12–21. doi:10.1002/smll.200901158
Vogler EA (1998) Structure and reactivity of water at biomaterial surfaces. Adv Colloid Interface Sci 74:69–117. doi:10.1016/S0001-8686(97)00040-7
Walsh D, Furuzono T, Tanaka J (2001) Preparation of porous composite implant materials by in situ polymerization of porous apatite containing ɛ-caprolactone or methyl methacrylate. Biomaterials 22:1205–1212. doi:10.1016/S0142-9612(00)00268-4
Wang HF, Huff TB, Zweifel DA et al (2005) In vitro and in vivo two-photon luminescence imaging of single gold nanorods. Proc Natl Acad Sci USA 102:15752–15756. doi:10.1073/pnas.0504892102
Webster TJ, Ejiofor JU (2004) Increased osteoblast adhesion on nanophase metals: Ti, Ti6Al4V, and CoCrMo. Biomaterials 25:4731–4939. doi:10.1016/j.biomaterials.2003.12.002
Webster TJ, Ergun C, Doremus RH et al (2000) Specific proteins mediate enhanced osteoblast adhesion on nanophase ceramics. J Biomed Mater Res 51:475–483
Wei G, Ma PX (2004) Structure and properties of nano-hydroxyapatite/polymer composite scaffolds for bone tissue engineering. Biomaterials 25:4749–4757. doi:10.1016/j.biomaterials.2003.12.005
Wennerberg A, Albrektsson T (2009) Effects of titanium surface topography on bone integration: a systematic review. Clin Oral Implants Res 20[Suppl 4]:172–184. doi:10.1111/j.1600-0501.2009.01775.x
Wennerberg A, Hallgren C, Johansson C, Danelli S (1998) A histomorphometric evaluation of screw-shaped implants each prepared with two surface roughnesses. Clin Oral Implants Res 9:11–19. doi:10.1034/j.1600-0501.1998.090102.x
Williams KA, Veenhuizen PTM, de la Torre BG, Ramon Eritja CD (2002) Carbon nanotubes with DNA recognition. Nature 420:761
Xia Z, Yu X, Wei M (2012) Biomimetic collagen/apatite coating formation on Ti6Al4V substrates. J Biomed Mater Res B Appl Biomater 100:871–881. doi:10.1002/jbm.b.31970
Xiao F-X, Pagliaro M, Xu Y-J, Liu B (2016) Layer-by-layer assembly of versatile nanoarchitectures with diverse dimensionality: a new perspective for rational construction of multilayer assemblies. Chem Soc Rev 45:3088–3121. doi:10.1039/C5CS00781J
Xu Z, Liang G, Jin L et al (2014) Synthesis of sodium caseinate–calcium carbonate microspheres and their mineralization to bone-like apatite. J Cryst Growth 395:116–122. doi:10.1016/j.jcrysgro.2014.03.023
Yang W, Thordarson P, Gooding JJ et al (2007) Carbon nanotubes for biological and biomedical applications. Nanotechnology 18:1. doi:10.1088/0957-4484/18/41/412001
Yang Y, Kim K, Ong J (2005) A review on calcium phosphate coatings produced using a sputtering process? An alternative to plasma spraying. Biomaterials 26:327–337. doi:10.1016/j.biomaterials.2004.02.029
Yim EKF, Darling EM, Kulangara K et al (2010) Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 31:1299–1306. doi:10.1016/j.biomaterials.2009.10.037
Yoneda JS, Rigos CF, Ciancaglini P (2013) Addition of subunit l, K+ ions, and lipid restores the thermal stability of solubilized Na, K-ATPase. Arch Biochem Biophys 530:93–100. doi:10.1016/j.abb.2009.01.015
Yoneda JS, Rigos CF, De Lourenço TFA et al (2014) Na, K-ATPase reconstituted in ternary liposome: The presence of cholesterol affects protein activity and thermal stability. Arch Biochem Biophys 564:136–141. doi:10.1016/j.abb.2014.09.015
Yoon I-K, Hwang J-Y, Jang W-C et al (2014) Natural bone-like biomimetic surface modification of titanium. Appl Surf Sci 301:401–409. doi:10.1016/j.apsusc.2014.02.090
Yukna RA, Yukna CN (1998) A 5-year follow-up of 16 patients treated with coralline calcium carbonate (Biocoraltm) bone replacement grafts in infrabony defects. J Clin Periodontol 25:1036–1040. doi:10.1111/j.1600-051X.1998.tb02410.x
Zancanela DC, de Faria AN, Simão AMS et al (2016) Multi and single walled carbon nanotubes: effects on cell responses and biomineralization of osteoblasts culture. J Mater Sci Mater Med 27:1–10
Zanello LP, Zhao B, Hu H, Haddon RC (2006) Bone cell proliferation on carbon nanotubes. Nano Lett 6:562–7. doi:10.1021/nl051861e
Zhang Y, Jin R, Zhang L, Liu M (2004) Growth of CaCO3 in the templated Langmuir?Blodgett film of a bolaamphiphilic diacid. New J Chem 28:614. doi:10.1039/b314136e
Zhao HY, Xu XX, Zhang JX et al (2010) Carbon nanotube-hydroxyapatite-hemoglobin nanocomposites with high bioelectrocatalytic activity. Bioelectrochemistry 78:124–129. doi:10.1016/j.bioelechem.2009.08.009
Zucolotto V, Daghastanli KRP, Hayasaka CO et al (2007) Using capacitance measurements as the detection method in antigen containing layer by layer films for biosensing. Anal Chem 79:2163–2167. doi:10.1021/ac0616153
Acknowledgements
The authors thank the São Paulo Research Foundation (FAPESP—grant 2013/12615-0, 2014/11941-3, 2014/24249-0, 2012/20946-3 and 2015/08774-0) and the National Council of Technological and Scientific Development (CNPq- grant 44283412014-4) for financial support. Camila B. Tovani and Marcos A. E. Cruz thank FAPESP for the PhD and MSc scholarships, respectively. Ana P. Ramos and Pietro Ciancaglini are CNPq researchers.
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Ana P. Ramos declares that she has no conflicts of interest. Marcos A.E. Cruz declares that he has no conflicts of interest. Camila B. Tovani declares that she has no conflicts of interest. Pietro Ciancaglini declares that he has no conflicts of interest.
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Ramos, A.P., Cruz, M.A.E., Tovani, C.B. et al. Biomedical applications of nanotechnology. Biophys Rev 9, 79–89 (2017). https://doi.org/10.1007/s12551-016-0246-2
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DOI: https://doi.org/10.1007/s12551-016-0246-2