The influence of the size and aspect ratio of anisotropic, porous CaCO 3 particles on their uptake by cells

Journal of Nanobiotechnology

Andre G Skirtach⁴  Wolfgang J Parak¹  Helmuth Möhwald³  Joanna Rejman¹  Susana Carregal-Romero¹  Alexey Yashchenok³  Mikhail V Zyuzin¹  Bogdan Parakhonskiy² 

[1] Fachbereich Physik, Philipps University of Marburg, Marburg, Germany;Institute of Nanostructures and Biosystems, Saratov State University, Saratov, Russia;Department of Interfaces, Max-Planck Institute of Colloids and Interfaces, Potsdam, Germany;Department of Molecular Biotechnology, Ghent University, Ghent, Belgium

关键词: Internalisation;    Cells;    Uptake;    Anisotropic;    Calcium carbonate;   

Others  :  1224843
DOI  :  10.1186/s12951-015-0111-7

 received in 2015-04-16, accepted in 2015-07-28,  发布年份 2015

【 摘 要 】

Background

Recent reports highlighting the role of particle geometry have suggested that anisotropy can affect the rate and the pathway of particle uptake by cells. Therefore, we investigate the internalization by cells of porous calcium carbonate particles with different shapes and anisotropies.

Results

We report here on a new method of the synthesis of polyelectrolyte coated calcium carbonate particles whose geometry was controlled by varying the mixing speed and time, pH value of the reaction solution, and ratio of the interacting salts used for particle formation. Uptake of spherical, cuboidal, ellipsoidal (with two different sizes) polyelectrolyte coated calcium carbonate particles was studied in cervical carcinoma cells. Quantitative data were obtained from the analysis of confocal laser scanning microscopy images.

Conclusions

Our results indicate that the number of internalized calcium carbonate particles depends on the aspect ratio of the particle, whereby elongated particles (higher aspect ratio) are internalized with a higher frequency than more spherical particles (lower aspect ratio). The total volume of internalized particles scales with the volume of the individual particles, in case equal amount of particles were added per cell.

【 授权许可】

   
2015 Parakhonskiy et al.

【 图 表 】

Fig.1.

Fig.2.

Fig.3.

Fig.4.

Fig.5.

【 参考文献 】

• [1]Chithrani BD, Ghazani AA, Chan WCW. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006; 6:662-668.
• [2]Lerch S, Dass M, Musyanovych A, Landfester K, Mailaender V. Polymeric nanoparticles of different sizes overcome the cell membrane barrier. Eur J Pharm Biopharm. 2013; 84:265-274.
• [3]Bhaskar S, Pollock KM, Yoshida M, Lahann J. Towards designer microparticles: simultaneous control of anisotropy, shape, and size. Small. 2010; 6:404-411.
• [4]Daum N, Tscheka C, Neumeyer A, Schneider M. Novel approaches for drug delivery systems in nanomedicine: effects of particle design and shape. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2012; 4:52-65.
• [5]Shimoni O, Yan Y, Wang YJ, Caruso F. Shape-dependent cellular processing of polyelectrolyte capsules. ACS Nano. 2013; 7:522-530.
• [6]Meng H, Yang S, Li ZX, Xia T, Chen J, Ji ZX et al.. Aspect ratio determines the quantity of mesoporous silica nanoparticle uptake by a small GTPase-dependent macropinocytosis mechanism. ACS Nano. 2011; 5:4434-4447.
• [7]Holt B, Lam R, Meldrum FC, Stoyanov SD, Paunov VN. Anisotropic nano-papier mache microcapsules. Soft Matter. 2007; 3:188-190.
• [8]Huhn D, Kantner K, Geidel C, Brandholt S, De Cock I, Soenen SJH et al.. Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano. 2013; 7:3253-3263.
• [9]Javier AM, Kreft O, Alberola AP, Kirchner C, Zebli B, Susha AS et al.. Combined atomic force microscopy and optical microscopy measurements as a method to investigate particle uptake by cells. Small. 2006; 2:394-400.
• [10]Wattendorf U, Kreft O, Textor M, Sukhorukov GB, Merkle HP. Stable stealth function for hollow polyelectrolyte microcapsules through a poly(ethylene glycol) grafted polyelectrolyte adlayer. Biomacromolecules. 2008; 9:100-108.
• [11]Jiang XE, Dausend J, Hafner M, Musyanovych A, Rocker C, Landfester K, Mailander V et al.. Specific effects of surface amines on polystyrene nanoparticles in their interactions with mesenchymal stem cells. Biomacromolecules. 2010; 11:748-753.
• [12]He CB, Hu YP, Yin LC, Tang C, Yin CH. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials. 2010; 31:3657-3666.
• [13]Delehanty JB, Blanco-Canosa JB, Bradburne CE, Susumu K, Stewart MH, Prasuhn DE et al.. Site-specific cellular delivery of quantum dots with chemoselectively-assembled modular peptides. Chem Commun. 2013; 49:7878-7880.
• [14]Parakhonskiy BV, Foss C, Carletti E, Fedel M, Haase A, Motta A et al.. Tailored intracellular delivery via a crystal phase transition in 400 nm vaterite particles. Biomater Sci. 2013; 1:1273-1281.
• [15]Tang R, Moyano DF, Subramani C, Yan B, Jeoung E, Tonga GY et al.. Rapid coating of surfaces with functionalized nanoparticles for regulation of cell behavior. Adv Mater. 2014; 26:3310-3314.
• [16]Caballero-Diaz E, Pfeiffer C, Kastl L, Rivera-Gil P, Simonet B, Valcarcel M et al.. the toxicity of silver nanoparticles depends on their uptake by cells and thus on their surface chemistry. Part Part Syst Charact. 2013; 30:1079-1085.
• [17]Bedard MF, Munoz-Javier A, Mueller R, del Pino P, Fery A, Parak WJ et al.. On the mechanical stability of polymeric microcontainers functionalized with nanoparticles. Soft Matter. 2009; 5:148-155.
• [18]Hartmann R, Weidenbach M, Neubauer M, Fery A, Parak WJ. Stiffness-dependent in vitro uptake and lysosomal acidification of colloidal particles. Angew Chem Int Ed. 2015; 54:1365-1368.
• [19]Kim CS, Le NDB, Xing YQ, Yan B, Tonga GY, Kim C et al.. The role of surface functionality in nanoparticle exocytosis. Adv Healthc Mater. 2014; 3:1200-1202.
• [20]Wang B, Zhang YY, Mao ZW, Gao CY. Cellular uptake of covalent poly(allylamine hydrochloride) microcapsules and its influences on cell functions. Macromol Biosci. 2012; 12:1534-1545.
• [21]Doshi N, Mitragotri S. Macrophages recognize size and shape of their targets. PLoS One. 2010; 5:e10051.
• [22]Leclerc L, Boudard D, Pourchez J, Forest V, Marmuse L, Louis C et al.. Quantitative cellular uptake of double fluorescent core-shelled model submicronic particles. J Nanopart Res. 2012; 14:1221.
• [23]Simone EA, Dziubla TD, Muzykantov VR. Polymeric carriers: role of geometry in drug delivery. Expert Opin Drug Deliv. 2008; 5:1283-1300.
• [24]De Jong WH, Hagens WI, Krystek P, Burger MC, Sips A, Geertsma RE. Particle size-dependent organ distribution of gold nanoparticles after intravenous administration. Biomaterials. 2008; 29:1912-1919.
• [25]Sonavane G, Tomoda K, Makino K. Biodistribution of colloidal gold nanoparticles after intravenous administration: effect of particle size. Colloids Surf B Biointerfaces. 2008; 66:274-280.
• [26]Lankveld DPK, Oomen AG, Krystek P, Neigh A, Troost-de Jong A, Noorlander CW et al.. The kinetics of the tissue distribution of silver nanoparticles of different sizes. Biomaterials. 2010; 31:8350-8361.
• [27]Velev OD, Gupta S. Materials fabricated by micro- and nanoparticle assembly—the challenging path from science to engineering. Adv Mater. 2009; 21:1897-1905.
• [28]Rivera-Gil P, De Aberasturi DJ, Wulf V, Pelaz B, Del Pino P, Zhao YY et al.. The challenge to relate the physicochemical properties of colloidal nanoparticles to their cytotoxicity. Acc Chem Res. 2013; 46:743-749.
• [29]Yan Y, Gause KT, Kamphuis MMJ, Ang CS, O’Brien-Simpson NM, Lenzo JC et al.. Differential roles of the protein corona in the cellular uptake of nanoporous polymer particles by monocyte and macrophage cell lines. ACS Nano. 2013; 7:10960-10970.
• [30]Hutter E, Boridy S, Labrecque S, Lalancette-Hebert M, Kriz J, Winnik FM et al.. microglial response to gold nanoparticles. ACS Nano. 2010; 4:2595-2606.
• [31]Liu SB, Wei L, Hao L, Fang N, Chang MW, Xu R et al.. Sharper and faster “nano darts” kill more bacteria: a study of antibacterial activity of individually dispersed pristine single-walled carbon nanotube. ACS Nano. 2009; 3:3891-3902.
• [32]Kastl L, Sasse D, Wulf V, Hartmann R, Mircheski J, Ranke C et al.. Multiple internalization pathways of polyelectrolyte multilayer capsules into mammalian cells. ACS Nano. 2013; 7:6605-6618.
• [33]Yoo JW, Doshi N, Mitragotri S. Endocytosis and intracellular distribution of PLGA particles in endothelial cells: effect of particle geometry. Macromol Rapid Commun. 2010; 31:142-148.
• [34]Herd H, Daum N, Jones AT, Huwer H, Ghandehari H, Lehr CM. Nanoparticle geometry and surface orientation influence mode of cellular uptake. ACS Nano. 2013; 7:1961-1973.
• [35]Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc Natl Acad Sci USA. 2006; 103:4930-4934.
• [36]Decuzzi P, Ferrari M. The receptor-mediated endocytosis of nonspherical particles. Biophys J. 2008; 94:3790-3797.
• [37]Gilbert JB, O’Brien JS, Suresh HS, Cohen RE, Rubner MF. Orientation-specific attachment of polymeric microtubes on cell surfaces. Adv Mater. 2013; 25:5948-5952.
• [38]Florez L, Herrmann C, Cramer JM, Hauser CP, Koynov K, Landfester K et al.. How shape influences uptake: interactions of anisotropic polymer nanoparticles and human mesenchymal stem cells. Small. 2012; 8:2222-2230.
• [39]Swiston AJ, Gilbert JB, Irvine DJ, Cohen RE, Rubner MF. Freely suspended cellular “backpacks” lead to cell aggregate self-assembly. Biomacromolecules. 2010; 11:1826-1832.
• [40]Gratton SEA, Ropp PA, Pohlhaus PD, Luft JC, Madden VJ, Napier ME et al.. The effect of particle design on cellular internalization pathways. Proc Natl Acad Sci USA. 2008; 105:11613-11618.
• [41]Geng Y, Dalhaimer P, Cai SS, Tsai R, Tewari M, Minko T et al.. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat Nanotechnol. 2007; 2:249-255.
• [42]Kolhar P, Anselmo AC, Gupta V, Pant K, Prabhakarpandian B, Ruoslahti E et al.. Using shape effects to target antibody-coated nanoparticles to lung and brain endothelium. Proc Natl Acad Sci USA. 2013; 110:10753-10758.
• [43]Agarwal R, Singh V, Jurney P, Shi L, Sreenivasan SV, Roy K. Mammalian cells preferentially internalize hydrogel nanodiscs over nanorods and use shape-specific uptake mechanisms. Proc Natl Acad Sci USA. 2013; 110:17247-17252.
• [44]Glotzer SC, Solomon MJ. Anisotropy of building blocks and their assembly into complex structures. Nat Mater. 2007; 6:557-562.
• [45]Pawar AB, Kretzschmar I. Fabrication, assembly, and application of patchy particles. Macromol Rapid Commun. 2010; 31:150-168.
• [46]Kohler D, Madaboosi N, Delcea M, Schmidt S, De Geest BG, Volodkin DV et al.. Patchiness of embedded particles and film stiffness control through concentration of gold nanoparticles. Adv Mater. 2012; 24:1095-1100.
• [47]Sharp EL, Al-Shehri H, Horozov TS, Stoyanov SD, Paunov VN. Adsorption of shape-anisotropic and porous particles at the air-water and the decane-water interface studied by the gel trapping technique. Rsc Adv. 2014; 4:2205-2213.
• [48]Volodkin D. CaCO3 templated micro-beads and -capsules for bioapplications. Adv Colloid Interface Sci. 2014; 207:306-324.
• [49]Trushina DB, Bukreeva TV, Kovalchuk MV, Antipina MN. CaCO3 vaterite microparticles for biomedical and personal care applications. Mater Sci Eng, C. 2014; 45:644-658.
• [50]Parakhonskiy BV, Yashchenok AM, Donatan S, Volodkin DV, Tessarolo F, Antolini R et al.. Macromolecule loading into spherical, elliptical, star-like and cubic calcium carbonate carriers. ChemPhysChem. 2014; 15:2817-2822.
• [51]Ariga K, Lvov YM, Kawakami K, Ji QM, Hill JP. Layer-by-layer self-assembled shells for drug delivery. Adv Drug Deliv Rev. 2011; 63:762-771.
• [52]Becker AL, Johnston APR, Caruso F. Layer-by-layer-assembled capsules and films for therapeutic delivery. Small. 2010; 6:1836-1852.
• [53]Rivera Gil P, del Mercato LL, del-Pino P, Munoz-Javier A, Parak WJ. Nanoparticle-modified polyelectrolyte capsules. Nano Today. 2008; 3:12-21.
• [54]Skirtach AG, Yashchenok AM, Mohwald H. Encapsulation, release and applications of LbL polyelectrolyte multilayer capsules. Chem Commun. 2011; 47:12736-12746.
• [55]Vergaro V, Scarlino F, Bellomo C, Rinaldi R, Vergara D, Maffia M et al.. Drug-loaded polyelectrolyte microcapsules for sustained targeting of cancer cells. Adv Drug Deliv Rev. 2011; 63:847-863.
• [56]Parakhonskiy BV, Yashchenok AM, Konrad M, Skirtach AG. Colloidal micro- and nano-particles as templates for polyelectrolyte multilayer capsules. Adv Colloid Interface Sci. 2014; 207:253-264.
• [57]Sukhorukov GB, Rogach AL, Zebli B, Liedl T, Skirtach AG, Kohler K et al.. Nanoengineered polymer capsules: tools for detection, controlled delivery, and site-specific manipulation. Small. 2005; 1:194-200.
• [58]De Koker S, De Geest BG, Cuvelier C, Ferdinande L, Deckers W, Hennink WE et al.. In vivo cellular uptake, degradation, and biocompatibility of polyelectrolyte microcapsules. Adv Funct Mater. 2007; 17:3754-3763.
• [59]Javier AM, Kreft O, Semmling M, Kempter S, Skirtach AG, Bruns OT et al.. Uptake of colloidal polyelectrolyte-coated particles and polyelectrolyte multilayer capsules by living cells. Adv Mater. 2008; 20:4281-4287.
• [60]Cortez C, Tomaskovic-Crook E, Johnston APR, Radt B, Cody SH, Scott AM et al.. Targeting and uptake of multilayered particles to colorectal cancer cells. Adv Mater. 2006; 18:1998.
• [61]del Mercato LL, Ferraro MM, Baldassarre F, Mancarella S, Greco V, Rinaldi R et al.. Biological applications of LbL multilayer capsules: from drug delivery to sensing. Adv Colloid Interface Sci. 2014; 207:139-154.
• [62]Yashchenok AM, Borisova D, Parakhonskiy BV, Masic A, Pinchasik BE, Mohwald H et al.. Nanoplasmonic smooth silica versus porous calcium carbonate bead biosensors for detection of biomarkers. Ann Phys. 2012; 524:723-732.
• [63]Yashchenok AM, Delcea M, Videnova K, Jares-Erijman EA, Jovin TM, Konrad M et al.. Enzyme reaction in the pores of CaCO3 particles upon ultrasound disruption of attached substrate-filled liposomes. Angew Chem Int Ed. 2010; 49:8116-8120.
• [64]Islan GA, Cacicedo ML, Bosio VE, Castro GR. Development and characterization of new enzymatic modified hybrid calcium carbonate microparticles to obtain nano-architectured surfaces for enhanced drug loading. J Colloid Interface Sci. 2015; 439:76-87.
• [65]del Mercato LL, Abbasi AZ, Ochs M, Parak WJ. Multiplexed sensing of ions with barcoded polyelectrolyte capsules. ACS Nano. 2011; 5:9668-9674.
• [66]Sukhorukov GB, Volodkin DV, Gunther AM, Petrov AI, Shenoy DB, Mohwald H. Porous calcium carbonate microparticles as templates for encapsulation of bioactive compounds. J Mater Chem. 2004; 14:2073-2081.
• [67]Rivera-Gil P, De Koker S, De Geest BG, Parak WJ. Intracellular processing of proteins mediated by biodegradable polyelectrolyte capsules. Nano Lett. 2009; 9:4398-4402.
• [68]Sami H, Maparu AK, Kumar A, Sivakumar S. Generic delivery of payload of nanoparticles intracellularly via hybrid polymer capsules for bioimaging applications. PLoS One. 2012; 7:e36195.
• [69]Yashchenok A, Parakhonskiy B, Donatan S, Kohler D, Skirtach A, Mohwald H. Polyelectrolyte multilayer microcapsules templated on spherical, elliptical and square calcium carbonate particles. J Mater Chem B. 2013; 1:1223-1228.
• [70]Sato K, Seno M, Anzai JI. Release of insulin from calcium carbonate microspheres with and without layer-by-layer thin coatings. Polymers. 2014; 6:2157-2165.
• [71]Palankar R, Pinchasik BE, Schmidt S, De Geest BG, Fery A, Mohwald H et al.. Mechanical strength and intracellular uptake of CaCO3-templated LbL capsules composed of biodegradable polyelectrolytes: the influence of the number of layers. J Mater Chem B. 2013; 1:1175-1181.
• [72]Reibetanz U, Schonberg M, Rathmann S, Strehlow V, Gose M, Lessig J. Inhibition of human neutrophil elastase by alpha(1)-antitrypsin functionalized colloidal microcarriers. ACS Nano. 2012; 6:6325-6336.
• [73]Wuytens P, Parakhonskiy B, Yashchenok A, Winterhalter M, Skirtach A. Pharmacological aspects of release from microcapsules—from polymeric multilayers to lipid membranes. Curr Opin Pharmacol. 2014; 18:129-140.
• [74]Ye CH, Combs ZA, Calabrese R, Dai HQ, Kaplan DL, Tsukruk VV. Robust microcapsules with controlled permeability from silk fibroin reinforced with graphene oxide. Small. 2014; 10:5087-5097.
• [75]Parakhonskiy BV, Haase A, Antolini R. Sub-micrometer vaterite containers: synthesis, substance loading, and release. Angew Chem Int Ed. 2012; 51:1195-1197.
• [76]Tai CY, Chen FB. Polymorphism of CaCO3 precipitated in a constant-composition environment. AIChE J. 1998; 44:1790-1798.
• [77]Svenskaya Y, Parakhonskiy B, Haase A, Atkin V, Lukyanets E, Gorin D et al.. Anticancer drug delivery system based on calcium carbonate particles loaded with a photosensitizer. Biophys Chem. 2013; 182:11-15.
• [78]Sawada K. The mechanisms of crystallization and transformation of calcium carbonates. Pure Appl Chem. 1997; 69:921-928.
• [79]Kozlovskaya V, Chen J, Tedjo C, Liang X, Campos-Gomez J, Oh JW et al.. pH-responsive hydrogel cubes for release of doxorubicin in cancer cells. J Mater Chem B. 2014; 2:2494-2507.
• [80]Lattuada M, Hatton TA. Synthesis, properties and applications of Janus nanoparticles. Nano Today. 2011; 6:286-308.
• [81]Sacanna S, Pine DJ. Shape-anisotropic colloids: building blocks for complex assemblies. Curr Opin Colloid Interface Sci. 2011; 16:96-105.
• [82]Walther A, Muller AHE. Janus particles: synthesis, self-assembly, physical properties, and applications. Chem Rev. 2013; 113:5194-5261.
• [83]Lee KJ, Yoon J, Lahann J. Recent advances with anisotropic particles. Curr Opin Colloid Interface Sci. 2011; 16:195-202.
• [84]Shields CW, Zhu S, Yang Y, Bharti B, Liu J, Yellen BB et al.. Field-directed assembly of patchy anisotropic microparticles with defined shape. Soft Matter. 2013; 9:9219-9229.
• [85]Shchepelina O, Kozlovskaya V, Kharlampieva E, Mao WB, Alexeev A, Tsukruk VV. Anisotropic micro- and nano-capsules. Macromol Rapid Commun. 2010; 31:2041-2046.
• [86]Shchepelina O, Kozlovskaya V, Singamaneni S, Kharlampieva E, Tsukruk VV. Replication of anisotropic dispersed particulates and complex continuous templates. J Mater Chem. 2010; 20:6587-6603.
• [87]Delcea M, Madaboosi N, Yashchenok AM, Subedi P, Volodkin DV, De Geest BG et al.. Anisotropic multicompartment micro- and nano-capsules produced via embedding into biocompatible PLL/HA films. Chem Commun. 2011; 47:2098-2100.
• [88]Lisunova M, Dorokhin A, Holland N, Shevchenko VV, Tsukruk VV. Assembly of the anisotropic microcapsules in aqueous dispersions. Soft Matter. 2013; 9:3651-3660.
• [89]Alexeev A, Uspal WE, Balazs AC. Harnessing Janus nanoparticles to create controllable pores in membranes. ACS Nano. 2008; 2:1117-1122.
• [90]Palankar R, Pinchasik BE, Khlebtsov BN, Kolesnikova TA, Mohwald H, Winterhalter M et al.. Nanoplasmonically-induced defects in lipid membrane monitored by ion current: transient nanopores versus membrane rupture. Nano Lett. 2014; 14:4273-4279.
• [91]Hosta-Rigau L, Shimoni O, Stadler B, Caruso F. Advanced subcompartmentalized microreactors: polymer hydrogel carriers encapsulating polymer capsules and liposomes. Small. 2013; 9:3573-3583.
• [92]Delcea M, Yashchenok A, Videnova K, Kreft O, Mohwald H, Skirtach AG. Multicompartmental micro- and nanocapsules: hierarchy and applications in biosciences. Macromol Biosci. 2010; 10:465-474.
• [93]Musyanovych A, Landfester K. Polymer micro- and nanocapsules as biological carriers with multifunctional properties. Macromol Biosci. 2014; 14:458-477.