Multifunctional probes play an increasing role even beyond applications in biomedicine. Multifunctionality introduced by the dual types of complementary probes is always attractive because, in this case, functionalized objects inherit the function of both materials. Porous calcium carbonate microparticles are becoming popular carriers of biomolecules and biosensors, as well as imaging enhancers. We demonstrate here a dual function of these carriers by incorporating both magnetic and silver nanoparticles. Magnetic nanoparticles enable movements and displacements by a magnetic field, while silver nanoparticles provide surface-enhanced Raman signal amplification necessary for the detection of biomolecules. Application of such dual-functional carriers is foreseen beyond the applications of biomedicine and theranostics.
REFERENCES
1.
L.
Sercombe
, T.
Veerati
, F.
Moheimani
, S. Y.
Wu
, A. K.
Sood
, and S.
Hua
, “Advances and challenges of liposome assisted drug delivery
,” Front. Pharmacol.
6
, 286
(2015
). 2.
I. M.
Laura
, F.
Dosio
, and L.
Cattel
, “Stealth liposomes: Review of the basic science, rationale and clinical applications, existing and potential
,” Int. J. Nanomedicine
1
, 297
(2015
).3.
4.
C.
Bharti
, U.
Nagaich
, A.
Pal
, and N.
Gulati
, “Mesoporous silica nanoparticles in target drug delivery system: A review
,” Int. J. Pharm. Investig.
5
, 124
–133
(2015
). 5.
R.
Rothon
and C.
DeArmitt
, “Fillers (including fiber reinforcements)
,” in Brydson’s Plastics Materials
, 8th ed., edited by M. Gilbert (Butterworth-Heinemann, 2017), Chap. 8, pp. 169–204
.6.
S. P.
Gopi
, V.
Subramanian
, and K.
Palanisamy
, “Aragonite-calcite-vaterite: A temperature influenced sequential polymorphic transformation of CaCO3 in the presence of DTPA
,” Mater. Res. Bull.
48
, 1906
–1912
(2013
). 7.
J. D.
Rodriguez-Blanco
, S.
Shaw
, and L. G.
Benning
, “The kinetics and mechanisms of amorphous calcium carbonate (ACC) crystallization to calcite, via vaterite
,” Nanoscale
3
(1
), 265
–271
(2011
). 8.
B. V.
Parakhonskiy
, A. M.
Yashchenok
, S.
Donatan
, D. V.
Volodkin
, F.
Tessarolo
, R.
Antolini
, H.
Möhwald
, and A. G.
Skirtach
, “Macromolecule loading into spherical, elliptical, star-like and cubic calcium carbonate carriers
,” Chem. Phys. Chem.
15
, 2817
–2822
(2014
). 9.
D. B.
Trushina
, T. V.
Bukreeva
, M. V.
Kovalchuk
, and M. N.
Antipina
, “CaCO3 vaterite microparticles for biomedical and personal care applications
,” Mater. Sci. Eng. C
45
, 644
–658
(2014
). 10.
S.
Schmidt
and D. V.
Volodkin
, “Microparticulate biomolecules by mild CaCO3 templating
,” J. Mater. Chem. B
1
, 1210
(2013
). 11.
J.-P.
Andreassen
, “Formation mechanism and morphology in precipitation of vaterite-nano-aggregation or crystal growth
,” J. Cryst. Growth
274
, 256
–264
(2005
). 12.
Y. I.
Svenskaya
, H.
Fattah
, O. A.
Inozemtseva
, A. G.
Ivanova
, S. N.
Shtykov
, D. A.
Gorin
, and B. V.
Parakhonskiy
, “Key parameters for size- and shape-controlled synthesis of vaterite particles
,” Cryst. Growth Des.
18
, 331
–337
(2018
). 13.
Y. I.
Svenskaya
, H.
Fattah
, A. M.
Zakharevich
, D. A.
Gorin
, G. B.
Sukhorukov
, and B. V.
Parakhonskiy
, “Ultrasonically assisted fabrication of vaterite submicron-sized carriers
,” Adv. Powder Technol.
27
, 618
–624
(2016
). 14.
B. V.
Parakhonskiy
, A.
Haase
, and R.
Antolini
, “Sub-micrometer vaterite containers: Synthesis, substance loading, and release
,” Angew. Chem. Int. Ed.
51
, 1195
–1197
(2012
). 15.
A. A.
Abalymov
, R. A.
Verkhovskii
, M. V.
Novoselova
, B. V.
Parakhonskiy
, D. A.
Gorin
, A. M.
Yashchenok
, and G. B.
Sukhorukov
, “Live-cell imaging by confocal Raman and fluorescence microscopy recognizes the crystal structure of calcium carbonate particles in HeLa cells
,” Biotechnol. J.
13
, 1800071
(2018
). 16.
Y. I.
Svenskaya
, B. V.
Parakhonskiy
, A.
Haase
, V.
Atkin
, E.
Lukyanets
, D. A.
Gorin
, and R.
Antolini
, “Anticancer drug delivery system based on calcium carbonate particles loaded with a photosensitizer
,” Biophys. Chem.
182
, 11
–15
(2013
). 17.
C.
Muderrisoglu
, M. S.
Saveleva
, A. A.
Abalymov
, L.
Van der Meeren
, A.
Ivanova
, V.
Atkin
, B. V.
Parakhonskiy
, and A. G.
Skirtach
, “Nanostructured biointerfaces based on bioceramic calcium carbonate/hydrogel coatings on titanium with an active enzyme for stimulating osteoblasts growth
,” Adv. Mater. Interfaces
5
, 1800452
(2018
). 18.
M. S.
Saveleva
, A. N.
Ivanov
, M. O.
Kurtukova
, V. S.
Atkin
, A. G.
Ivanova
, G. P.
Lyubun
, A. V.
Martyukova
, E. I.
Cherevko
, A. K.
Sargsyan
, A. S.
Fedonnikov
, I. A.
Norkin
, A. G.
Skirtach
, D. A.
Gorin
, and B. V.
Parakhonskiy
, “Hybrid PCL/CaCO3 scaffolds with capabilities of carrying biologically active molecules: Synthesis, loading and in vivo applications
,” Mater. Sci. Eng. C
85
, 57
–67
(2018
). 19.
Y.
Won
, H. S.
Jang
, D.-W.
Chung
, and L. A.
Stanciu
, “Multifunctional calcium carbonate microparticles: Synthesis and biological applications
,” J. Mater. Chem.
20
, 7728
(2010
). 20.
D. A.
Gorin
, S. A.
Portnov
, O. A.
Inozemtseva
, Z.
Luklinska
, A. M.
Yashchenok
, A. M.
Pavlov
, A. G.
Skirtach
, H.
Möhwald
, and G. B.
Sukhorukov
, “Magnetic/gold nanoparticle functionalized biocompatible microcapsules with sensitivity to laser irradiation
,” Phys. Chem. Chem. Phys.
10
, 6899
–6905
(2008
). 21.
A.
Sergeeva
, R.
Sergeev
, E.
Lengert
, A.
Zakharevich
, B. V.
Parakhonskiy
, D.
Gorin
, S.
Sergeev
, and D.
Volodkin
, “Composite magnetite and protein containing CaCO3 crystals. External manipulation and vaterite → calcite recrystallization-mediated release performance
,” ACS Appl. Mater. Interfaces
7
, 21315
–21325
(2015
). 22.
S. V.
German
, M. V.
Novoselova
, D. N.
Bratashov
, P. A.
Demina
, V. S.
Atkin
, D. V.
Voronin
, B. N.
Khlebtsov
, B. V.
Parakhonskiy
, G. B.
Sukhorukov
, and D. A.
Gorin
, “High-efficiency freezing-induced loading of inorganic nanoparticles and proteins into micron- and submicron-sized porous particles
,” Sci. Rep.
8
, 17763
(2018
). 23.
R.
Kamyshinsky
, I.
Marchenko
, B. V.
Parakhonskiy
, A.
Yashchenok
, Y.
Chesnokov
, A.
Mikhutkin
, D.
Gorin
, A.
Vasiliev
, and T.
Bukreeva
, “Composite materials based on Ag nanoparticles in situ synthesized on the vaterite porous matrices
,” Nanotechnology
30
, 035603
(2019
). 24.
B. V.
Parakhonskiy
, M. F.
Bedard
, T. V.
Bukreeva
, G. B.
Sukhorukov
, H.
Möhwald
, and A. G.
Skirtach
, “Nanoparticles on polyelectrolytes at low concentration: Controlling concentration and size
,” J. Phys. Chem. C
114
, 1996
–2002
(2010
). 25.
R.
Xiong
, S. J.
Soenen
, K.
Braeckmans
, and A. G.
Skirtach
, “Towards theranostic multicompartment microcapsules: In-situ diagnostics and laser-induced treatment
,” Theranostics
3
, 141
–151
(2013
). 26.
I. V.
Vidiasheva
, A. A.
Abalymov
, M. A.
Kurochkin
, O. A.
Mayorova
, M. V.
Lomova
, S. V.
German
, D. N.
Khalenkow
, M. N.
Zharkov
, D. A.
Gorin
, A. G.
Skirtach
, V. V.
Tuchin
, and G. B.
Sukhorukov
, “Transfer of cells with uptaken nanocomposite, magnetite-nanoparticle functionalized capsules with electromagnetic tweezers
,” Biomater. Sci.
6
, 2219
–2229
(2018
). 27.
D. V.
Voronin
, O. A.
Sindeeva
, M. A.
Kurochkin
, O.
Mayorova
, I. V.
Fedosov
, O.
Semyachkina-Glushkovskaya
, D. A.
Gorin
, V. V.
Tuchin
, and G. B.
Sukhorukov
, “In vitro and in vivo visualization and trapping of fluorescent magnetic microcapsules in a bloodstream
,” ACS Appl. Mater. Interfaces
9
, 6885
–6893
(2017
). 28.
A.
Ali
, H.
Zafar
, M.
Zia
, I.
ul Haq
, A. R.
Phull
, J. S.
Ali
, and A.
Hussain
, “Synthesis, characterization, applications, and challenges of iron oxide nanoparticles
,” Nanotechnol. Sci. Appl.
9
, 49
–67
(2016
), PMCID: PMC4998023. 29.
Z. R.
Stephen
, F. M.
Kievit
, and M.
Zhang
, “Magnetite nanoparticles for medical MR imaging
,” Mater. Today
14
, 330
–338
(2012
). 30.
A.
Akbarzadeh
, M.
Samiei
, and S.
Davaran
, “Magnetic nanoparticles : Preparation, physical properties, and applications in biomedicine
,” Nanoscale Res. Lett.
7
, 1
–13
(2012
). 31.
D. L.
Tran
, V. H.
Le
, H. L.
Pham
, T. M. N.
Hoang
, T. Q.
Nguyen
, T. T.
Luong
, P. T.
Ha
, and X. P.
Nguyen
, “Biomedical and environmental applications of magnetic nanoparticles
,” Adv. Nat. Sci. Nanosci. Nanotechnol.
1
, 045013
(2011
). 32.
M. E.
De Sousa
, M. B.
Fernández Van Raap
, P. C.
Rivas
, P.
Mendoza Zélis
, P.
Girardin
, G. A.
Pasquevich
, J. L.
Alessandrini
, D.
Muraca
, and F. H.
Sánchez
, “Stability and relaxation mechanisms of citric acid coated magnetite nanoparticles for magnetic hyperthermia
,” J. Phys. Chem. C
117
, 5436
–5445
(2013
). 33.
M.
Rǎcuciu
, D. E.
Creangǎ
, and A.
Airinei
, “Citric-acid-coated magnetite nanoparticles for biological applications
,” Eur. Phys. J. E
21
, 117
–121
(2006
). 34.
J. J.
Mock
, M.
Barbic
, D. R.
Smith
, D. A.
Schultz
, and S.
Schultz
. “Shape effects in plasmon resonance of individual colloidal silver nanoparticles
,” J. Chem. Phys.
116
(15
), 6755
–6759
(2002
). 35.
S. L.
Smitha
, K. M.
Nissamudeen
, D.
Philip
, and K. G.
Gopchandran
. “Studies on surface plasmon resonance and photoluminescence of silver nanoparticles
,” Spectrochim. Acta: Part A: Mol. Biomol. Spectrosc.
71
(1
), 186
–190
(2008
). 36.
L.
Gharibshahi
, E.
Saion
, E.
Gharibshahi
, A. H.
Shaari
, and K. A.
Matori
, “Structural and optical properties of ag nanoparticles synthesized by thermal treatment method
,” Materials
10
, 402
(2017
). 37.
M.
Gühlke
, S.
Selve
, and J.
Kneippa
, “Magnetic separation and SERS observation of analyte molecules on bifunctional silver/iron oxide composite nanostructures
,” J. Raman Spectrosc.
43
, 1204
–1207
(2012
). 38.
A. M.
Yashchenok
, A.
Masic
, D. A.
Gorin
, B. S.
Shim
, N. A.
Kotov
, P.
Fratzl
, H.
Möhwald
, and A. G.
Skirtach
, “Nanoengineered colloidal probes for Raman-based detection of biomolecules inside living cells
,” Small
9
, 351
–356
(2013
). 39.
D.
Graham
, M.
Moskovits
, and Z.-Q.
Tian
, “SERS—Facts, figures and the future
,” Chem. Soc. Rev.
46
, 3864
–3865
(2017
). 40.
D.
Zopf
, A.
Pittner
, A.
Dathe
, N.
Grosse
, A.
Csáki
, K.
Arstila
, J. J.
Toppari
, W.
Schott
, D.
Dontsov
, G.
Uhlrich
, W.
Fritzsche
, and O.
Stranik
, “Plasmonic nanosensor array for multiplexed DNA-based pathogen detection
,” ACS Sensors
4
, 335
–343
(2019
). 41.
A.
Raza
, S.
Clemmen
, P.
Wuytens
, M.
Muneeb
, M.
Van Daele
, J.
Dendooven
, C.
Detavernier
, A.
Skirtach
, and R.
Baets
, “ALD assisted nanoplasmonic slot waveguide for on-chip enhanced Raman spectroscopy
,” APL Photonics
3
, 116105
(2018
). 42.
D. V.
Volodkin
, N. I.
Larionova
, and G. B.
Sukhorukov
, “Protein encapsulation via porous CaCO3 microparticles templating
,” Biomacromolecules
5
, 1962
–1972
(2004
). 43.
W.
Elmore
, “Ferromagnetic colloid for studying magnetic structures
,” Phys. Rev.
54
, 309
–310
(1938
). 44.
R.
Kamyshinsky
, I.
Marchenko
, and B.
Parakhonskiy
, “The vaterite porous matrices composite materials based on Ag nanoparticles in situ synthesized on the vaterite porous matrices
,” Nanotechnology
30
, 035603
(2019
). 45.
K.
Kneipp
, H.
Kneipp
, and J.
Kneipp
, “Surface-enhanced Raman scattering in local optical fields of silver and gold nanoaggregates from single-molecule Raman spectroscopy to ultrasensitive probing in live cells single-molecule Raman scattering in local
,” Acc. Chem. Res.
39
, 443
–450
(2006
). 46.
J.
Soukupová
, L.
Kvítek
, A.
Panáček
, T.
Nevěčná
, and R.
Zbořil
, “Comprehensive study on surfactant role on silver nanoparticles prepared via modified Tollens process
,” Mater. Chem. Phys.
111
, 77
–81
(2008
). 47.
R.
Dondi
, W.
Su
, G.
Griffith
, G.
Clark
, and G.
Burley
, “Highly size and shape controlled synthesis of silver nanoparticles via a templated Tollens rection
,” Small
8
, 770
–776
(2012
). 48.
Y.
Yin
, Z.
Zhong
, B. D.
Gates
, Z.-Y.
Li
, Y.
Xia
, and S.
Venkateswaran
, “Synthesis and characterization of stable aqueous dispersions of silver nanoparticles through the Tollens process
,” J. Mater. Chem.
12
, 522
–527
(2002
). 49.
T. V.
Bukreeva
, I. V.
Marchenko
, B. B. V.
Parakhonskiy
, Y. V.
Grigor’ev
, and Y. V.
Grigor’ev
, “Formation of silver nanoparticles on shells of polyelectrolyte capsules using silver-mirror reaction
,” Colloid J.
71
, 596
–602
(2009
). 50.
K.
Hering
, D.
Cialla
, K.
Ackermann
, T.
Dörfer
, R.
Möller
, H.
Schneidewind
, R.
Mattheis
, W.
Fritzsche
, P.
Rösch
, and J.
Popp
, “SERS: A versatile tool in chemical and biochemical diagnostics
,” Anal. Bioanal. Chem.
390
, 113
–124
(2008
). 51.
H.
Ko
, S.
Singamaneni
, and V. V.
Tsukruk
, “Nanostructured surfaces and assemblies as SERS media
,” Small
4
, 1576
–1599
(2008
). 52.
C.
Krafft
, M.
Schmitt
, I. W.
Schie
, D.
Cialla-May
, C.
Matthäus
, T.
Bocklitz
, and J.
Popp
, “Label-free molecular imaging of biological cells and tissues by linear and nonlinear Raman spectroscopic approaches
,” Angew. Chemie Int. Ed.
56
, 4392
–4430
(2017
). 53.
M.
Tebbe
, P.
Cherepanov
, E. V.
Skorb
, S. K.
Poznyak
, J. G.
De Abajo
, A.
Fery
, D. V.
Andreeva
, R. A. A.
Puebla
, and N.
Pazos-Perez
, “SERS platforms of plasmonic hydrophobic surfaces for analyte concentration: Hierarchically assembled gold nanorods on anodized aluminum
,” Part. Part. Syst. Charact.
31
, 1134
–1140
(2014
). 54.
N.
Bontempi
, L.
Carletti
, C.
De Angelis
, and I.
Alessandri
, “Plasmon-free SERS detection of environmental CO2 on TiO2 surfaces
,” Nanoscale
8
, 3226
–3231
(2016
). 55.
M. S.
Saveleva
, K.
Eftekhari
, A.
Abalymov
, T. E. L.
Douglas
, D.
Volodkin
, B. V.
Parakhonskiy
, and A. G.
Skirtach
, “Hierarchy of hybrid materials—The place of inorganics-in-organics in it, their composition and applications
,” Front. Chem.
7
, 1
–21
(2019
). 56.
R. V.
Chernozem
, M. A.
Surmeneva
, V.
Atkin
, B.
Krause
, T.
Baumbach
, B. V.
Parakhonskiy
, D.
Khalenkow
, A. G.
Skirtach
, and R. A.
Surmenev
, “Plasmonic hybrid biocomposite as an effective substrate for detection of biomolecules by surface-enhanced Raman spectroscopy
,” Russ. Phys. J.
61
, 1288
–1293
(2018
). 57.
C.
Wu
, E.
Chen
, and J.
Wei
, “Surface enhanced Raman spectroscopy of rhodamine 6G on agglomerates of different-sized silver truncated nanotriangles
,” Colloids Surf. A
506
, 450
–456
(2016
). 58.
M.
Delcea
, H.
Möhwald
, and A. G.
Skirtach
, “Stimuli-responsive LbL capsules and nanoshells for drug delivery
,” Adv. Drug Deliv. Rev.
63
, 730
–747
(2011
). © 2019 Author(s).
2019
Author(s)
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