AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Electrospun poly(vinylidene fluoride-trifluoroethylene)/zinc oxide nanocomposite tissue engineering scaffolds with enhanced cell adhesion and blood vessel formation

Robin Augustine1,2,§( )Pan Dan3,§Alejandro Sosnik1Nandakumar Kalarikkal2,4Nguyen Tran5Brice Vincent6Sabu Thomas2,7Patrick Menu3Didier Rouxel6( )
Laboratory of Pharmaceutical Nanomaterials ScienceDepartment of Materials Science and EngineeringTechnion-Israel Institute of Technology, De-Jur Building, Technion CityHaifa3200003Israel
International and Inter University Centre for Nanoscience and NanotechnologyMahatma Gandhi UniversityKottayamKerala686560India
Ingénierie Moléculaire et Physiopathologie Articulaire UMR 7365 CNRS-Université de Lorraine, Vandoeuvre-lès Nancy F-54500 France
School of Pure and Applied PhysicsMahatma Gandhi UniversityKottayamKerala686560India
School of SurgeryFaculty of MedicineUniversité de Lorraine, Vandoeuvre-lès-Nancy F-54500France
Institut Jean Lamour UMR 7198 CNRS-Université de Lorraine, Vandoeuvre-lès-Nancy F-54500 France
School of Chemical SciencesMahatma Gandhi UniversityKottayamKerala686560India

§ Robin Augustine and Pan Dan contributed equally to this work.

Show Author Information

Graphical Abstract

Abstract

Piezoelectric materials that generate electrical signals in response to mechanical strain can be used in tissue engineering to stimulate cell proliferation. Poly (vinylidene fluoride-trifluoroethylene) (P(VDF-TrFE)), a piezoelectric polymer, is widely used in biomaterial applications. We hypothesized that incorporation of zinc oxide (ZnO)nanoparticles into the P(VDF-TrFE) matrix could promote adhesion, migration, and proliferation of cells, as well as blood vessel formation (angiogenesis). In this study, we fabricated and comprehensively characterized a novel electrospun P(VDF-TrFE)/ZnO nanocomposite tissue engineering scaffold. We analyzed the morphological features of the polymeric matrix by scanning electron microscopy, and utilized Fourier transform infrared spectroscopy, X-ray diffraction, and differential scanning calorimetry to examine changes in the crystalline phases of the copolymer due to addition of the nanoparticles. We detected no or minimal adverse effects of the biomaterials with regard to blood compatibility in vitro, biocompatibility, and cytotoxicity, indicating that P(VDF-TrFE)/ZnO nanocomposite scaffolds are suitable for tissue engineering applications. Interestingly, human mesenchymal stem cells (hMSCs) and human umbilical vein endothelial cells cultured on the nanocomposite scaffolds exhibited higher cell viability, adhesion, and proliferation compared to cells cultured on tissue culture plates or neat P(VDF-TrFE) scaffolds. Nanocomposite scaffolds implanted into rats with or without hMSCs did not elicit immunological responses, as assessed by macroscopic analysis and histology. Importantly, nanocomposite scaffolds promoted angiogenesis, which was increased in scaffolds pre-seeded with hMSCs. Overall, our results highlight the potential of these novel P(VDF-TrFE)/ZnO nanocomposites for use in tissue engineering, due to their biocompatibility and ability to promote cell adhesion and angiogenesis.

Electronic Supplementary Material

Download File(s)
nr-10-10-3358_ESM.pdf (2.5 MB)

References

1

Kuang, R.; Zhang, Z. P.; Jin, X. B.; Hu, J.; Shi, S. T.; Ni, L. X.; Ma, P. X. Nanofibrous spongy microspheres for the delivery of hypoxia-primed human dental pulp stem cells to regenerate vascularized dental pulp. Acta Biomater. 2016, 33, 225–234.

2

Briquez, P. S.; Clegg, L. E.; Martino, M. M.; Gabhann, F. M.; Hubbell, J. A. Design principles for therapeutic angiogenic materials. Nat. Rev. Mater. 2016, 1, 15006.

3

Dondossola, E.; Holzapfel, B. M.; Alexander, S.; Filippini, S.; Hutmacher, D. W.; Friedl, P. Examination of the foreign body response to biomaterials by nonlinear intravital microscopy. Nat. Biomed. Eng. 2016, 1, 0007.

4

McCaig, C. D.; Song, B.; Rajnicek, A. M. Electrical dimensions in cell science. J. Cell Sci. 2009, 122, 4267–4276.

5

McCaig, C. D.; Rajnicek, A. M.; Song, B.; Zhao, M. Controlling cell behavior electrically: Current views and future potential. Physiol. Rev. 2005, 85, 943–978.

6

Weber, N.; Lee, Y. S.; Shanmugasundaram, S.; Jaffe, M.; Arinzeh, T. L. Characterization and in vitro cytocompatibility of piezoelectric electrospun scaffolds. Acta Biomater. 2010, 6, 3550–3556.

7

Hu, Z. J.; Tian, M. W.; Nysten, B.; Jonas, A. M. Regular arrays of highly ordered ferroelectric polymer nanostructures for non-volatile low-voltage memories. Nat. Mater. 2009, 8, 62–67.

8

Huang, S.; Yee, W. A.; Tjiu, W. C.; Liu, Y.; Kotaki, M.; Boey, Y. C. F.; Ma, J.; Liu, T. X.; Lu, X. H. Electrospinning of polyvinylidene difluoride with carbon nanotubes: Synergistic effects of extensional force and interfacial interaction on crystalline structures. Langmuir 2008, 24, 13621–13626.

9

Li, M. Y.; Wondergem, H. J.; Spijkman, M. J.; Asadi, K.; Katsouras, I.; Blom, P. W. M.; De Leeuw, D. M. Revisiting the d-phase of poly(vinylidene fluoride) for solution-processed ferroelectric thin films. Nat. Mater. 2013, 12, 433–438.

10

Liu, Y. W.; Lu, J. F.; Li, H. N.; Wei, J. J.; Li, X. H. Engineering blood vessels through micropatterned co-culture of vascular endothelial and smooth muscle cells on bilayered electrospun fibrous mats with pDNA inoculation. Acta Biomater. 2015, 11, 114–125.

11

Fine, E. G.; Valentini, R. F.; Bellamkonda, R.; Aebischer, P. Improved nerve regeneration through piezoelectric vinylidenefluoride-trifluoroethylene copolymer guidance channels. Biomaterials 1991, 12, 775–780.

12

Lee, Y. S.; Collins, G.; Arinzeh, T. L. Neurite extension of primary neurons on electrospun piezoelectric scaffolds. Acta Biomater. 2011, 7, 3877–3886.

13

Lee, Y. S.; Wu, S.; Arinzeh, T. L.; Bunge, M. B. Enhanced noradrenergic axon regeneration into schwann cell-filled PVDF-TrFE conduits after complete spinal cord transection. Biotechnol. Bioeng. 2017, 114, 444–456.

14

Martins, P. M.; Ribeiro, S.; Ribeiro, C.; Sencadas, V.; Gomes, A. C.; Gama, F. M.; Lanceros-Mé ndez, S. Effect of poling state and morphology of piezoelectric poly(vinylidene fluoride) membranes for skeletal muscle tissue engineering. RSC Adv. 2013, 3, 17938–17944.

15

Hitscherich, P.; Wu, S. L.; Gordan, R.; Xie, L. H.; Arinzeh, T.; Lee, E. J. The effect of PVDF-TrFE scaffolds on stem cell derived cardiovascular cells. Biotechnol. Bioeng. 2016, 113, 1577–1585.

16

Zhu, P.; Weng, Z. Y.; Li, X.; Liu, X. M.; Wu, S. L.; Yeung, K. W. K.; Wang, X. B.; Cui, Z. D.; Yang, X. J.; Chu, P. K. Biomedical applications of functionalized ZnO nanomaterials: From biosensors to bioimaging. Adv. Mater. Interfaces 2016, 3, 1500494.

17

Liao, Q. L.; Zhang, Z.; Zhang, X. H.; Mohr, M.; Zhang, Y.; Fecht, H. J. Flexible piezoelectric nanogenerators based on a fiber/ZnO nanowires/paper hybrid structure for energy harvesting. Nano Res. 2014, 7, 917–928.

18

Kang, Z.; Yan, X. Q.; Zhao, L. Q.; Liao, Q. L.; Zhao, K.; Du, H. W.; Zhang, X. H.; Zhang, X. J.; Zhang, Y. Gold nanoparticle/ZnO nanorod hybrids for enhanced reactive oxygen species generation and photodynamic therapy. Nano Res. 2015, 8, 2004–2014.

19

Yan, Z. Q.; Zhao, A. D.; Liu, X. P.; Ren, J. S.; Qu, X. G. A pH-switched mesoporous nanoreactor for synergetic therapy. Nano Res. 2017, 10, 1651–1661.

20

Augustine, R.; Malik, H. N.; Singhal, D. K.; Mukherjee, A.; Malakar, D.; Kalarikkal, N.; Thomas, S. Electrospun polycaprolactone/ZnO nanocomposite membranes as biomaterials with antibacterial and cell adhesion properties. J. Polym. Res. 2014, 21, 347.

21

Augustine, R.; Dominic, E. A.; Reju, I.; Kaimal, B.; Kalarikkal, N.; Thomas, S. Electrospun polycaprolactone membranes incorporated with ZnO nanoparticles as skin substitutes with enhanced fibroblast proliferation and wound healing. RSC Adv. 2014, 4, 24777–24785.

22

Augustine, R.; Dominic, E. A.; Reju, I.; Kaimal, B.; Kalarikkal, N.; Thomas, S. Investigation of angiogenesis and its mechanism using zinc oxide nanoparticle-loaded electrospun tissue engineering scaffolds. RSC Adv. 2014, 4, 51528–51536.

23

Sirelkhatim, A.; Mahmud, S.; Seeni, A.; Kaus, N. H. M.; Ann, L. C.; Bakhori, S. K. M.; Hasan, H.; Mohamad, D. Review on zinc oxide nanoparticles: Antibacterial activity and toxicity mechanism. Nano-Micro Lett. 2015, 7, 219–242.

24

Saptarshi, S. R.; Duschl, A.; Lopata, A. L. Biological reactivity of zinc oxide nanoparticles with mammalian test systems: An overview. Nanomedicine 2015, 10, 2075–2092.

25

Versiani, M. A.; Abi Rached-Junior, F. J.; Kishen, A.; Pécora J. D.; Silva-Sousa, Y. T.; De Sousa-Neto, M. D. Zinc oxide nanoparticles enhance physicochemical characteristics of Grossman sealer. J. Endod. 2016, 42, 1804–1810.

26

Jiang, L. Y.; Li, Y. B.; Xiong, C. D. Preparation and biological properties of a novel composite scaffold of nano-hydroxyapatite/chitosan/carboxymethyl cellulose for bone tissue engineering. J. Biomed. Sci. 2009, 16, 65.

27

Joshy, K. S.; Sharma, C. P.; Kalarikkal, N.; Sandeep, K.; Thomas, S.; Pothen, L. A. Evaluation of in-vitro cytotoxicity and cellular uptake efficiency of zidovudine-loaded solid lipid nanoparticles modified with Aloe Vera in glioma cells. Mater. Sci. Eng. C 2016, 66, 40–50.

28

El Omar, R.; Xiong, Y.; Dostert, G.; Louis, H.; Gentils, M.; Menu, P.; Stoltz, J. F.; Velot, é.; Decot, V. Immunomodulation of endothelial differentiated mesenchymal stromal cells: Impact on T and NK cells. Immunol. Cell Biol. 2015, 94, 342–356.

29

Choi, Y. Y.; Yun, T. G.; Qaiser, N.; Paik, H.; Roh, H. S.; Hong, J.; Hong, S.; Han, S. M.; No, K. Vertically aligned P(VDF-TrFE) core–shell structures on flexible pillar arrays. Sci. Rep. 2015, 5, 10728.

30

Tashiro, K.; Takano, K.; Kobayashi, M.; Chatani, Y.; Tadokoro, H. Structural study on ferroelectric phase transition of vinylidene fluoride-trifluoroethylene random copolymers. Polymer 1981, 22, 1312–1314.

31

Kim, K. J.; Kim, G. B.; Vanlencia, C. L.; Rabolt, J. F. Curie transition, ferroelectric crystal structure, and ferroelectricity of a VDF/TrFE(75/25) copolymer 1. The effect of the consecutive annealing in the ferroelectric state on curie transition and ferroelectric crystal structure. J. Polym. Sci. Part B Polym. Phys. 1994, 32, 2435–2444.

32

Tashiro, K.; Itoh, Y.; Kobayashi, M.; Tadokoro, H. Polarized Raman spectra and LO-TO splitting of poly (vinylidene fluoride) crystal form I. Macromolecules 1985, 18, 2600–2606.

33

Mattsson, B.; Ericson, H.; Torell, L. M.; Sundholm, F. Micro-Raman investigations of PVDF-based proton-conducting membranes. J. Polym. Sci. Part A Polym. Chem. 1999, 37, 3317–3327.

34

Yee, W. A.; Nguyen, A. C.; Lee, P. S.; Kotaki, M.; Liu, Y.; Tan, B. T.; Mhaisalkar, S.; Lu, X. H. Stress-induced structural changes in electrospun polyvinylidene difluoride nanofibers collected using a modified rotating disk. Polymer 2008, 49, 4196–4203.

35

Mahdi, R. I.; Gan, W. C.; Abd Majid, W. H. Hot plate annealing at a low temperature of a thin ferroelectric P(VDF-TrFE) film with an improved crystalline structure for sensors and actuators. Sensors 2014, 14, 19115–19127.

36

Xu, B.; Choi, J.; Borca, C. N.; Dowben, P. A.; Sorokin, A. V.; Palto, S. P.; Petukhova, N. N.; Yudin, S. G. Comparison of aluminum and sodium doped poly(vinylidene fluoridetrifluoroethylene) copolymers by X-ray photoemission spectroscopy. Appl. Phys. Lett. 2001, 78, 448–450.

37

Nguyen, V. S.; Rouxel, D.; Vincent, B.; Badie, L.; Dos Santos, F. D.; Lamouroux, E.; Fort, Y. Influence of cluster size and surface functionalization of ZnO nanoparticles on the morphology, thermomechanical and piezoelectric properties of P(VDF-TrFE) nanocomposite films. Appl. Surf. Sci. 2013, 279, 204–211.

38

Bharti, V.; Xu, H. S.; Shanthi, G.; Zhang, Q. M.; Liang, K. M. Polarization and structural properties of high-energy electron irradiated poly(vinylidene fluoride-trifluoroethylene) copolymer films. J. Appl. Phys. 2000, 87, 452–461.

39

Oswald, J.; Boxberger, S.; J?rgensen, B.; Feldmann, S.; Ehninger, G.; Bornh? user M.; Werner, C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 2004, 22, 377–384.

40

Lutolf, M. P.; Hubbell, J. A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat. Biotechnol. 2005, 23, 47–55.

41

Place, E. S.; Evans, N. D.; Stevens, M. M. Complexity in biomaterials for tissue engineering. Nat. Mater. 2009, 8, 457–470.

42

Okoshi, T.; Chen, H.; Soldani, G.; Galletti, P. M.; Goddard, M. Microporous small diameter PVDF-TrFE vascular grafts fabricated by a spray phase inversion technique. ASAIO J. 1992, 38, M201–M206.

43

Katsouras, I.; Asadi, K.; Li, M. Y.; Van Driel, T. B.; Kj? r, K. S.; Zhao, D.; Lenz, T.; Gu, Y.; Blom, P. W. M.; Damjanovic, D. et al. The negative piezoelectric effect of the ferroelectric polymer poly(vinylidene fluoride). Nat. Mater. 2016, 15, 78–84.

44

Zhang, X. H.; Zhang, C. G.; Lin, Y. H.; Hu, P. H.; Shen, Y.; Wang, K.; Meng, S.; Chai, Y.; Dai, X. H.; Liu, X. et al. Nanocomposite membranes enhance bone regeneration through restoring physiological electric microenvironment. ACS Nano 2016, 10, 7279–7286.

45

Zhang, D.; Karki, A. B.; Rutman, D.; Young, D. P.; Wang, A.; Cocke, D.; Ho, T. H.; Guo, Z. H. Electrospun polyacrylonitrile nanocomposite fibers reinforced with Fe3O4 nanoparticles: Fabrication and property analysis. Polymer 2009, 50, 4189–4198.

46

Baumgarten, P. K. Electrostatic spinning of acrylic microfibers. J. Colloid Interface Sci. 1971, 36, 71–79.

47

Huttenlocher, A.; Horwitz, A. R. Wound healing with electric potential. N. Engl. J. Med. 2007, 356, 303–304.

48

Hwang, G. T.; Byun, M.; Jeong, C. K.; Lee, K. J. Flexible piezoelectric thin-film energy harvesters and nanosensors for biomedical applications. Adv. Healthc. Mater. 2015, 4, 646–658.

49

Lonjon, A.; Laffont, L.; Demont, P.; Dantras, E.; Lacabanne, C. Structural and electrical properties of gold nanowires/P(VDF-TrFE) nanocomposites. J. Phys. D: Appl. Phys. 2010, 43, 345401.

50

Andrew, J. S.; Clarke, D. R. Effect of electrospinning on the ferroelectric phase content of polyvinylidene difluoride fibers. Langmuir 2008, 24, 670–672.

51

Guo, H. F.; Li, Z. S.; Dong, S. W.; Chen, W. J.; Deng, L.; Wang, Y. F.; Ying, D. J. Piezoelectric PU/PVDF electrospun scaffolds for wound healing applications. Colloids Surf. B: Biointerfaces 2012, 96, 29–36.

52

Augustine, R.; Sarry, F.; Kalarikkal, N.; Thomas, S.; Badie, L.; Rouxel, D. Surface acoustic wave device with reduced insertion loss by electrospinning P(VDF-TrFE)/ZnO nanocomposites. Nano-Micro Lett. 2016, 8, 282–290.

53

Lee, Y. S.; Arinzeh, T. L. The influence of piezoelectric scaffolds on neural differentiation of human neural stem/progenitor cells. Tissue Eng. Part A 2012, 18, 2063–2072.

54

Li, W. J.; Laurencin, C. T.; Caterson, E. J.; Tuan, R. S.; Ko, F. K. Electrospun nanofibrous structure: A novel scaffold for tissue engineering. J. Biomed. Mater. Res. 2002, 60, 613–621.

55

Chhabra, H.; Deshpande, R.; Kanitkar, M.; Jaiswal, A.; Kale, V. P.; Bellare, J. R. A nano zinc oxide doped electrospun scaffold improves wound healing in a rodent model. RSC Adv. 2016, 6, 1428–1439.

56

Augustine, R.; Mathew, A.; Sosnik, A. Metal oxide nanoparticles as versatile therapeutic agents modulating cell signaling pathways: Linking nanotechnology with molecular medicine. Appl. Mater. Today 2017, 7, 91–103.

57

Paszek, E.; Czyz, J.; Wo?nicka, O.; Jakubiak, D.; Wojnarowicz, J.; ?ojkowski, W.; St?pień, E. Zinc oxide nanoparticles impair the integrity of human umbilical vein endothelial cell monolayer in vitro. J. Biomed. Nanotechnol. 2012, 8, 957–967.

58

Hsiao, I. L.; Huang, Y. J. Effects of various physicochemical characteristics on the toxicities of ZnO and TiO2 nanoparticles toward human lung epithelial cells. Sci. Total Environ. 2011, 409, 1219–1228.

59

Nair, S.; Sasidharan, A.; Divya Rani, V. V.; Menon, D.; Nair, S.; Manzoor, K.; Raina, S. Role of size scale of ZnO nanoparticles and microparticles on toxicity toward bacteria and osteoblast cancer cells. J. Mater. Sci. : Mater. Med. 2009, 20, 235.

60

Mironov, V.; Kasyanov, V.; Markwald, R. R. Nanotechnology in vascular tissue engineering: From nanoscaffolding towards rapid vessel biofabrication. Trends Biotechnol. 2008, 26, 338–244.

61

Barui, A. K.; Veeriah, V.; Mukherjee, S.; Manna, J.; Patel, A. K.; Patra, S.; Pal, K.; Murali, S.; Rana, R. K.; Chatterjee, S. et al. Zinc oxide nanoflowers make new blood vessels. Nanoscale 2012, 4, 7861–7869.

62

Todeschi, M. R.; El Backly, R.; Capelli, C.; Daga, A.; Patrone, E.; Introna, M.; Cancedda, R.; Mastrogiacomo, M. Transplanted umbilical cord mesenchymal stem cells modify the in vivo microenvironment enhancing angiogenesis and leading to bone regeneration. Stem Cells Dev. 2015, 24, 1570–1581.

63

Hoffman, A. J.; Carraway, E. R.; Hoffmann, M. R. Photocatalytic production of H2O2 and organic peroxides on quantum-sized semiconductor colloids. Environ. Sci. Technol. 1994, 28, 776–785.

Nano Research
Pages 3358-3376
Cite this article:
Augustine R, Dan P, Sosnik A, et al. Electrospun poly(vinylidene fluoride-trifluoroethylene)/zinc oxide nanocomposite tissue engineering scaffolds with enhanced cell adhesion and blood vessel formation. Nano Research, 2017, 10(10): 3358-3376. https://doi.org/10.1007/s12274-017-1549-8

1079

Views

155

Crossref

N/A

Web of Science

157

Scopus

7

CSCD

Altmetrics

Received: 27 December 2016
Revised: 21 February 2017
Accepted: 23 February 2017
Published: 06 May 2017
© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2017
Return