Skip to main content

Advertisement

SpringerLink
Log in

3D Cell Culturing and Possibilities for Myometrial Tissue Engineering

  • Reproductive Tissue Engineering
  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Research insights into uterine function and the mechanisms of labour have been hindered by the lack of suitable animal and cellular models. The use of traditional culturing methods limits the exploration of complex uterine functions, such as cell interactions, connectivity and contractile behaviour, as it fails to mimic the three-dimensional (3D) nature of uterine cell interactions in vivo. Animal models are an option, however, use of these models is constrained by ethical considerations as well as translational limitations to humans. Evidence indicates that these limitations can be overcome by using 3D culture systems, or 3D Bioprinters, to model the in vivo cytological architecture of the tissue in an in vitro environment. 3D cultured or 3D printed cells can be used to form an artificial tissue. This artificial tissue can not only be used as an appropriate model in which to study cellular function and organisation, but could also be used for regenerative medicine purposes including organ or tissue transplantation, organ donation and obstetric care. The current review describes recent developments in cell culture that can facilitate the development of myometrial 3D structures and tissue engineering applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Adissu, H. A., E. K. Asem, and S. A. Lelievre. Three-dimensional cell culture to model epithelia in the female reproductive system. Reprod. Sci. 14:11–19, 2007.

    Article  PubMed  Google Scholar 

  2. Almany, L., and D. Seliktar. Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures. Biomaterials 26:2467–2477, 2005.

    Article  CAS  PubMed  Google Scholar 

  3. Astashkina, A., B. Mann, and D. W. Grainger. A critical evaluation of in vitro cell culture models for high-throughput drug screening and toxicity. Pharmacol. Ther. 134:82–106, 2012.

    Article  CAS  PubMed  Google Scholar 

  4. Bajpai, V. K., P. Mistriotis, Y. H. Loh, G. Q. Daley, and S. T. Andreadis. Functional vascular smooth muscle cells derived from human induced pluripotent stem cells via mesenchymal stem cell intermediates. Cardiovasc. Res. 96:391–400, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Boretti, M. I., and K. J. Gooch. Effect of extracellular matrix and 3D morphogenesis on islet hormone gene expression by Ngn3-infected mouse pancreatic ductal epithelial cells. Tissue Eng. A 14:1927–1937, 2008.

    Article  CAS  Google Scholar 

  6. Bursztyn, L., O. Eytan, A. J. Jaffa, and D. Elad. Mathematical model of excitation-contraction in a uterine smooth muscle cell. Am. J. Physiol. Cell Physiol. 292:C1816–C1829, 2007.

    Article  CAS  PubMed  Google Scholar 

  7. Castillejo, M., E. Rebollar, M. Oujja, M. Sanz, A. Selimis, M. Sigletou, S. Psycharakis, A. Ranella, and C. Fotakis. Fabrication of porous biopolymer substrates for cell growth by UV laser: The role of pulse duration. Appl. Surf. Sci. 258:8919–8927, 2012.

    Article  CAS  Google Scholar 

  8. Chamley-Campbell, J., G. R. Campbell, and R. Ross. The smooth muscle cell in culture. Physiol. Rev. 59:1–61, 1979.

    CAS  PubMed  Google Scholar 

  9. Charwat, V., K. Schütze, W. Holnthoner, A. Lavrentieva, R. Gangnus, P. Hofbauer, C. Hoffmann, B. Angres, and C. Kasper. Potential and limitations of microscopy and Raman spectroscopy for live-cell analysis of 3D cell cultures. J. Biotechnol. 205:70–81, 2015.

    Article  CAS  PubMed  Google Scholar 

  10. Condon, J., S. Yin, B. Mayhew, R. A. Word, W. E. Wright, J. W. Shay, and W. E. Rainey. Telomerase immortalization of human myometrial cells. Biol. Reprod. 67(2):506–514, 2002.

    Article  CAS  PubMed  Google Scholar 

  11. Dainiak, M. B., I. N. Savina, I. Musolino, A. Kumar, B. Mattiasson, and I. Y. Galaev. Biomimetic macroporous hydrogel scaffolds in a high-throughput screening format for cell-based assays. Biotechnol. Prog. 24:1373–1383, 2008.

    Article  CAS  PubMed  Google Scholar 

  12. Dallot, E., M. Pouchelet, N. Gouhier, D. Cabrol, F. Ferre, and M. Breuiller-Fouche. Contraction of cultured human uterine smooth muscle cells after stimulation with endothelin-1. Biol. Reprod. 68:937–942, 2003.

    Article  CAS  PubMed  Google Scholar 

  13. Dhiman, H. K., A. R. Ray, and A. K. Panda. Three-dimensional chitosan scaffold-based MCF-7 cell culture for the determination of the cytotoxicity of tamoxifen. Biomaterials 26:979–986, 2005.

    Article  CAS  PubMed  Google Scholar 

  14. Drover, J. W., and R. F. Casper. Initiation of parturition in humans. Can. Med. Assoc. J. 128:387–392, 1983.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Elliott, N. T., and F. Yuan. A review of three-dimensional in vitro tissue models for drug discovery and transport studies. J. Pharm. Sci. 100:59–74, 2011.

    Article  CAS  PubMed  Google Scholar 

  16. El-Sherbiny, I. M., and M. H. Yacoub. Hydrogel scaffolds for tissue engineering: Progress and challenges. Global Cardiol. Sci. Pract. 2013:38, 2013.

    Article  Google Scholar 

  17. Equils, O., P. Nambiar, C. J. Hobel, R. Smith, C. F. Simmons, and S. Vali. A computer simulation of progesterone and Cox2 inhibitor treatment for preterm labor. PLoS ONE 5:e8502, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fitzgibbon, J., J. J. Morrison, T. J. Smith, and M. O’Brien. Modulation of human uterine smooth muscle cell collagen contractility by thrombin, Y-27632, TNF alpha and indomethacin. Reprod. Biol. Endocrinol. 7:2, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Fleischer, S., J. Miller, H. Hurowitz, A. Shapira, and T. Dvir. Effect of fiber diameter on the assembly of functional 3D cardiac patches. Nanotechnology 26(29):291002, 2015.

    Article  PubMed  Google Scholar 

  20. Foty, R. A simple hanging drop cell culture protocol for generation of 3D spheroids. J. Vis. Exp. 51:2720, 2011.

    Google Scholar 

  21. Gong, P. Y., W. Zheng, D. Xiao, and X. Y. Jiang. Microscale methods to assemble mammalian cells into tissue-like structures. Sci. China Life Sci. 55:862–871, 2012.

    Article  CAS  PubMed  Google Scholar 

  22. Graf, B. W., and S. A. Boppart. Imaging and analysis of three-dimensional cell culture models. Methods Mol. Biol. 591:211–227, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Grefte, S., S. Vullinghs, A. M. Kuijpers-Jagtman, R. Torensma, and J. W. Von den Hoff. Matrigel, but not collagen I, maintains the differentiation capacity of muscle derived cells in vitro. Biomed. Mater. 7:055004, 2012.

    Article  CAS  PubMed  Google Scholar 

  24. Grima, R. Directed cell migration in the presence of obstacles. Theor. Biol. Med. Model. 4:2, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Harris, L. J., H. Abdollahi, P. Zhang, S. McIlhenny, T. N. Tulenko, and P. J. DiMuzio. Differentiation of adult stem cells into smooth muscle for vascular tissue engineering. J. Surg. Res. 168:306–314, 2011.

    Article  CAS  PubMed  Google Scholar 

  26. Hellström, M., R. R. El-Akouri, C. Sihlbom, B. M. Olsson, J. Lengqvist, H. Bäckdahl, B. R. Johansson, M. Olausson, S. Sumitran-Holgersson, and M. Brännström. Towards the development of a bioengineered uterus: Comparison of different protocols for rat uterus decellularization. Acta Biomater. 10:5034–5042, 2014.

    Article  PubMed  Google Scholar 

  27. Hellström, M., J. M. Moreno-Moya, S. Bandstein, E. Bom, R. R. Akouri, K. Miyazaki, T. Maruyama, and M. Brännström. Bioengineered uterine tissue supports pregnancy in a rat model. Fertil. Steril. 106(2):487–496, 2016.

    Article  PubMed  Google Scholar 

  28. Holmes, T. C., S. de Lacalle, X. Su, G. Liu, A. Rich, and S. Zhang. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proc. Natl Acad. Sci. USA 97:6728–6733, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Hsieh, W.-C., and J.-J. Liau. Cell culture and characterization of cross-linked poly(vinyl alcohol)-g-starch 3D scaffold for tissue engineering. Carbohydr. Polym. 98:574–580, 2013.

    Article  CAS  PubMed  Google Scholar 

  30. Huh, D., G. A. Hamilton, and D. E. Ingber. From 3D cell culture to organs-on-chips. Trends Cell Biol. 21:745–754, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ikonen, L., E. Kerkelä, G. Metselaar, M. C. A. Stuart, M. R. de Jong, and K. Aalto-Setälä. 2D and 3D self-assembling nanofiber hydrogels for cardiomyocyte culture. BioMed. Res. Int. 2013. doi:10.1155/2013/285678.

    PubMed  Google Scholar 

  32. Kakade, S., and G. Mani. A comparative study of the effects of vitamin C, sirolimus, and paclitaxel on the growth of endothelial and smooth muscle cells for cardiovascular medical device applications. Drug Des. Dev. Ther. 7:529–544, 2013.

    CAS  Google Scholar 

  33. Heidari Kani, M., R. Smith, T. Butler, C. Chan, and R. Young. Glass wool as a model scaffold for 3D culture of uterine smooth muscle cells. Front. Bioeng. Biotechnol. Conference Abstract: 10th World Biomaterials Congress. 2016. doi:10.3389/conf.FBIOE.2016.01.02608.

  34. Khait, L., C. J. Hodonsky, and R. K. Birla. Variable optimization for the formation of three-dimensional self-organized heart muscle. Vitro Cell. Dev. Biol. 45:592–601, 2009.

    Article  Google Scholar 

  35. Khetan, S., and J. Burdick. Cellular encapsulation in 3D hydrogels for tissue engineering. J. Vis. Exp. 2009. doi:10.3791/1590.

    PubMed  PubMed Central  Google Scholar 

  36. Khoshfetrat, Pakazad S. A. Savov, A. Van De Stolpe and R. Dekker. A novel stretchable micro-electrode array (SMEA) design for directional stretching of cells. J. Micromech. Microeng. 24(3):034003, 2014.

    Article  Google Scholar 

  37. Kucukgul, C., B. Ozler, H. E. Karakas, D. Gozuacik, and B. Koc. 3D hybrid bioprinting of macrovascular structures. Procedia Eng. 59:183–192, 2013.

    Article  Google Scholar 

  38. Kuo, C. W., D. Y. Chueh, and P. Chen. Investigation of size-dependent cell adhesion on nanostructured interfaces. J. Nanobiotechnol. 12:54, 2014.

    Article  Google Scholar 

  39. Lawrence, B. J., and S. V. Madihally. Cell colonization in degradable 3D porous matrices. Cell Adhens. Migr. 2:9–16, 2008.

    Article  Google Scholar 

  40. Lee, H. J., E. R. Norwitz, and J. Shaw. Contemporary management of fibroids in pregnancy. Rev. Obstet. Gynecol. 3:20–27, 2010.

    PubMed  PubMed Central  Google Scholar 

  41. Lee, V., G. Singh, J. P. Trasatti, C. Bjornsson, X. Xu, T. N. Tran, S. S. Yoo, G. Dai, and P. Karande. Design and fabrication of human skin by three-dimensional bioprinting. Tissue Eng. C Methods 20:473–484, 2014.

    Article  CAS  Google Scholar 

  42. Lee, J. B., S. H. Son, M. C. Park, T. H. Kim, M. G. Kim, S. D. Yoo, and S. Kim. A novel in vitro permeability assay using three-dimensional cell culture system. J. Biotechnol. 205:93–100, 2015.

    Article  CAS  PubMed  Google Scholar 

  43. Lee, D. W., S. H. Yi, S. H. Jeong, B. Ku, J. Kim, and M.-Y. Lee. Plastic pillar inserts for three-dimensional (3D) cell cultures in 96-well plates. Sens. Actuators B 177:78–85, 2013.

    Article  CAS  Google Scholar 

  44. Lei, K. F., M. H. Wu, C. W. Hsu, and Y. D. Chen. Real-time and non-invasive impedimetric monitoring of cell proliferation and chemosensitivity in a perfusion 3D cell culture microfluidic chip. Biosens. Bioelectron. 51:16–21, 2013.

    Article  PubMed  Google Scholar 

  45. Li, Z., and Z. Cui. Three-dimensional perfused cell culture. Biotechnol. Adv. 32:243–254, 2014.

    Article  CAS  PubMed  Google Scholar 

  46. Liu, J. Y., H. F. Peng, and S. T. Andreadis. Contractile smooth muscle cells derived from hair-follicle stem cells. Cardiovasc. Res. 79:24–33, 2008.

    Article  CAS  PubMed  Google Scholar 

  47. Lovitt, C. J., T. B. Shelper, and V. M. Avery. Advanced cell culture techniques for cancer drug discovery. Biology 3:345–367, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Masuda, S., and T. Shimizu. Three-dimensional cardiac tissue fabrication based on cell sheet technology. Adv. Drug Deliv. Rev. 96:103–109, 2016.

    Article  CAS  PubMed  Google Scholar 

  49. Mironov, V., T. Boland, T. Trusk, G. Forgacs, and R. R. Markwald. Organ printing: computer-aided jet-based 3D tissue engineering. Trends Biotechnol. 21:157–161, 2003.

    Article  CAS  PubMed  Google Scholar 

  50. Mironov, V., V. Kasyanov, and R. R. Markwald. Organ printing: from bioprinter to organ biofabrication line. Curr. Opin. Biotechnol. 22:667–673, 2011.

    Article  CAS  PubMed  Google Scholar 

  51. Mironov, V., N. Reis, and B. Derby. Review: bioprinting: a beginning. Tissue Eng. 12:631–634, 2006.

    Article  PubMed  Google Scholar 

  52. Mitchell, B. F., and M. J. Taggart. Are animal models relevant to key aspects of human parturition? Am. J. Physiol. 297:R525–R545, 2009.

    CAS  Google Scholar 

  53. Miyazaki, K., and T. Maruyama. Partial regeneration and reconstruction of the rat uterus through recellularization of a decellularized uterine matrix. Biomaterials 35:8791–8800, 2014.

    Article  CAS  PubMed  Google Scholar 

  54. Monga, M., C. Y. Ku, K. Dodge, and B. M. Sanborn. Oxytocin-stimulated responses in a pregnant human immortalized myometrial cell line. Biol. Reprod. 55:427–432, 1996.

    Article  CAS  PubMed  Google Scholar 

  55. Negishi, J., S. Funamoto, T. Kimura, K. Nam, T. Higami, and A. Kishida. Effect of treatment temperature on collagen structures of the decellularized carotid artery using high hydrostatic pressure. J. Artif. Organs 14:223–231, 2011.

    Article  CAS  PubMed  Google Scholar 

  56. Norotte, C., F. S. Marga, L. E. Niklason, and G. Forgacs. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30:5910–5917, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ong, S.-M., C. Zhang, Y.-C. Toh, S. H. Kim, H. L. Foo, C. H. Tan, D. van Noort, S. Park, and H. Yu. A gel-free 3D microfluidic cell culture system. Biomaterials 29:3237–3244, 2008.

    Article  CAS  PubMed  Google Scholar 

  58. Palumbo, F. S., G. Pitarresi, C. Fiorica, S. Rigogliuso, G. Ghersi, and G. Giammona. Chemical hydrogels based on a hyaluronic acid-graft-α-elastin derivative as potential scaffolds for tissue engineering. Mater. Sci. Eng. C 33:2541–2549, 2013.

    Article  CAS  Google Scholar 

  59. Park, W. S., S. C. Heo, E. S. Jeon, D. H. Hong, Y. K. Son, J. H. Ko, H. K. Kim, S. Y. Lee, J. H. Kim, and J. Han. Functional expression of smooth muscle-specific ion channels in TGF-β1-treated human adipose-derived mesenchymal stem cells. Am. J. Physiol. 305:C377–C391, 2013.

    Article  CAS  Google Scholar 

  60. Pati, F., J.-H. Shim, J.-S. Lee, and D.-W. Cho. 3D printing of cell-laden constructs for heterogeneous tissue regeneration. Manuf. Lett. 1:49–53, 2013.

    Article  CAS  Google Scholar 

  61. Rampichová, M., J. Chvojka, M. Buzgo, E. Prosecká, P. Mikeš, L. Vysloužilová, D. Tvrdík, P. Kochová, T. Gregor, D. Lukáš, and E. Amler. Elastic three-dimensional poly (ε-caprolactone) nanofibre scaffold enhances migration, proliferation and osteogenic differentiation of mesenchymal stem cells. Cell Prolif. 46:23–37, 2013.

    Article  PubMed  Google Scholar 

  62. Ravi, M., V. Paramesh, S. R. Kaviya, E. Anuradha, and F. D. Paul Solomon. 3D cell culture systems: Advantages and applications. J. Cell. Physiol. 230:16–26, 2015.

    Article  CAS  PubMed  Google Scholar 

  63. Schindler, M., A. Nur-E-Kamal, I. Ahmed, J. Kamal, H. Y. Liu, N. Amor, A. S. Ponery, D. P. Crockett, T. H. Grafe, H. Y. Chung, T. Weik, E. Jones, and S. Meiners. Living in three dimensions: 3D nanostructured environments for cell culture and regenerative medicine. Cell Biochem. Biophys. 45:215–227, 2006.

    Article  CAS  PubMed  Google Scholar 

  64. Shamir, E. R., and A. J. Ewald. Three-dimensional organotypic culture: experimental models of mammalian biology and disease. Nat. Rev. Mol. Cell Biol. 15:647–664, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Shay, J. W., and W. E. Wright. Use of telomerase to create bioengineered tissues. Ann. N. Y. Acad. Sci. 479–491:2005, 1057.

    Google Scholar 

  66. Shrestha, K. R., Y. H. Park, Y. S. Choi, I. G. Kim, S. Piao, A. R. Jung, S. H. Jeon, S. H. Oh, J. H. Lee, and J. Y. Lee. Bladder reconstruction using stem cells seeded on multilayered scaffolds in a mucosa preserving partial cystectomy model. Tissue Eng. Regener. Med. 12:427–434, 2015.

    Article  CAS  Google Scholar 

  67. Shynlova, O., P. Tsui, S. Jaffer, and S. J. Lye. Integration of endocrine and mechanical signals in the regulation of myometrial functions during pregnancy and labour. Eur. J. Obstet. Gynecol. Reprod. Biol. 144(Supplement 1):S2–S10, 2009.

    Article  CAS  PubMed  Google Scholar 

  68. Simon, K. A., K. M. Park, B. Mosadegh, A. B. Subramaniam, A. D. Mazzeo, P. M. Ngo, and G. M. Whitesides. Polymer-based mesh as supports for multi-layered 3D cell culture and assays. Biomaterials 35:259–268, 2014.

    Article  CAS  PubMed  Google Scholar 

  69. Sims, S. M., E. E. Daniel, and R. E. Garfield. Improved electrical coupling in uterine smooth muscle is associated with increased numbers of gap junctions at parturition. J. Gen. Physiol. 80:353–375, 1982.

    Article  CAS  PubMed  Google Scholar 

  70. Sokolowski, P., F. Saison, W. Giles, S. McGrath, D. Smith, J. Smith, and R. Smith. Human uterine wall tension trajectories and the onset of parturition. PLoS ONE 5:e11037, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Stile, R. A., W. R. Burghardt, and K. E. Healy. Synthesis and characterization of injectable poly(N-isopropylacrylamide)-based hydrogels that support tissue formation in vitro. Macromolecules 32:7370–7379, 1999.

    Article  CAS  Google Scholar 

  72. Stratmann, A. T., D. Fecher, G. Wangorsch, C. Göttlich, T. Walles, H. Walles, T. Dandekar, G. Dandekar, and S. L. Nietzer. Establishment of a human 3D lung cancer model based on a biological tissue matrix combined with a Boolean in silico model. Mol. Oncol. 8:351–365, 2014.

    Article  CAS  PubMed  Google Scholar 

  73. Sullivan, D. C., S. H. Mirmalek-Sani, D. B. Deegan, P. M. Baptista, T. Aboushwareb, A. Atala, and J. J. Yoo. Decellularization methods of porcine kidneys for whole organ engineering using a high-throughput system. Biomaterials 33:7756–7764, 2012.

    Article  CAS  PubMed  Google Scholar 

  74. Sylvain, C., F. Jean-Christophe, G. Bertrand, P. Benjamin, B. Reine, R. Murielle, L. Eric, D. Bernard, A. Joëlle, and G. Fabien. Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication 3:025001, 2011.

    Article  Google Scholar 

  75. Taggart, M. J., A. Blanks, S. Kharche, A. Holden, B. Wang, and H. Zhang. Towards understanding the myometrial physiome: approaches for the construction of a virtual physiological uterus. BMC Pregnancy Childbirth 7(Suppl 1):S3, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  76. Tamayol, A., M. Akbari, N. Annabi, A. Paul, A. Khademhosseini, and D. Juncker. Fiber-based tissue engineering: Progress, challenges, and opportunities. Biotechnol. Adv. 31:669–687, 2013.

    Article  CAS  PubMed  Google Scholar 

  77. Tan, Y., D. J. Richards, T. C. Trusk, R. P. Visconti, M. J. Yost, M. S. Kindy, C. J. Drake, W. S. Argraves, R. R. Markwald, and Y. Mei. 3D printing facilitated scaffold-free tissue unit fabrication. Biofabrication 6:024111, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Topman, G., N. Shoham, O. Sharabani-Yosef, F. H. Lin, and A. Gefen. A new technique for studying directional cell migration in a hydrogel-based three-dimensional matrix for tissue engineering model systems. Micron 51:9–12, 2013.

    Article  CAS  PubMed  Google Scholar 

  79. Turnbull, A. C. Myometrial contractility in pregnancy and its regulation. Proc R. Soc. Med. 64:1015–1017, 1971.

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Turner, W. S., N. Sandhu, and K. E. McCloskey. Tissue engineering: Construction of a multicellular 3D scaffold for the delivery of layered cell sheets. J. Visualized Exp. 92:e51044–e51044, 2014.

    Google Scholar 

  81. Wang, Z., Y. Cui, J. Wang, X. Yang, Y. Wu, K. Wang, X. Gao, D. Li, Y. Li, X. L. Zheng, Y. Zhu, D. Kong, and Q. Zhao. The effect of thick fibers and large pores of electrospun poly(ε-caprolactone) vascular grafts on macrophage polarization and arterial regeneration. Biomaterials 35:5700–5710, 2014.

    Article  CAS  PubMed  Google Scholar 

  82. Wang, L., L. Liu, X. Li, N. Magome, K. Agladze, and Y. Chen. Multi-electrode monitoring of guided excitation in patterned cardiomyocytes. Microelectron. Eng. 111:267–271, 2013.

    Article  CAS  Google Scholar 

  83. Wozniak, M. A., and P. J. Keely. Use of three-dimensional collagen gels to study mechanotransduction in T47D breast epithelial cells. Biol. Proced. Online 7:144–161, 2005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Xiao, Q., G. Wang, Z. Luo, and Q. Xu. The mechanism of stem cell differentiation into smooth muscle cells. Thromb. Haemost. 104:440–448, 2010.

    Article  CAS  PubMed  Google Scholar 

  85. Xu, T., H. Kincaid, A. Atala, and J. J. Yoo. High-throughput production of single-cell microparticles using an inkjet printing technology. Trans. ASME Ser. B 130:210171–210175, 2008.

    Google Scholar 

  86. Xu, T., J. I. Rodriguez-Devora, D. Reyna-Soriano, M. Bhuyan, L. Zhu, K. Wang, and Y. Yuan. Chapter 6 - Principles of Bioprinting Technology. In: Regenerative medicine applications in organ transplantation, edited by G. Orlando, J. Lerut, S. Soker, and R. J. Stratta. Boston: Academic Press, 2014, pp. 67–79.

    Chapter  Google Scholar 

  87. Yamamoto, M., N. Kawashima, N. Takashino, Y. Koizumi, K. Takimoto, N. Suzuki, M. Saito, and H. Suda. Three-dimensional spheroid culture promotes odonto/osteoblastic differentiation of dental pulp cells. Arch. Oral Biol. 59:310–317, 2014.

    Article  CAS  PubMed  Google Scholar 

  88. Yan, P., C. Xia, C. Duan, S. Li, and Z. Mei. Biological characteristics of foam cell formation in smooth muscle cells derived from Bone Marrow stem cells. Int. J. Biol. Sci. 7:937–946, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Yoshii, Y., A. Waki, K. Yoshida, A. Kakezuka, M. Kobayashi, H. Namiki, Y. Kuroda, Y. Kiyono, H. Yoshii, T. Furukawa, T. Asai, H. Okazawa, J. G. Gelovani, and Y. Fujibayashi. The use of nanoimprinted scaffolds as 3D culture models to facilitate spontaneous tumor cell migration and well-regulated spheroid formation. Biomaterials 32:6052–6058, 2011.

    Article  CAS  PubMed  Google Scholar 

  90. Young, R. C. Myocytes, myometrium, and uterine contractions. Ann. N. Y. Acad. Sci. 1101:72–84, 2007.

    Article  CAS  PubMed  Google Scholar 

  91. Young, R. C., R. Schumann, and P. Zhang. Three-dimensional culture of human uterine smooth muscle myocytes on a resorbable scaffolding. Tissue Eng. 9:451–459, 2003.

    Article  CAS  PubMed  Google Scholar 

  92. Yu, C., Z. Zhu, L. Wang, Q. Wang, N. Bao, and H. Gu. A new disposable electrode for electrochemical study of leukemia K562 cells and anticancer drug sensitivity test. Biosens. Bioelectron. 53:142–147, 2014.

    Article  CAS  PubMed  Google Scholar 

  93. Zhang, S., F. Gelain, and X. Zhao. Designer self-assembling peptide nanofiber scaffolds for 3D tissue cell cultures. Semin. Cancer Biol. 15:413–420, 2005.

    Article  PubMed  Google Scholar 

  94. Zhao, X., L. Liu, J. Wang, Y. Xu, W. Zhang, G. Khang, and X. Wang. In vitro vascularization of a combined system based on a 3D printing technique. J Tissue Eng Regen Med. 2014. doi:10.1002/term.1863.

    Google Scholar 

  95. Zhao, Z. K., H. L. Yu, F. Xiao, S. W. Li, W. B. Liao, and K. L. Zhao. Muscle-derived stem cells differentiate into functional smooth muscle cells for ureter tissue engineering: An experimental study. Biotechnol. Bioprocess Eng. 17:456–464, 2012.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was conducted with the support of an Australian NHMRC grant to Roger Smith (G1200367).

Conflict of Interest

No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript.

Author information

Authors and Affiliations

  1. Mothers and Babies Research Centre, School of Medicine and Public Health, Faculty of Health and Medicine, University of Newcastle, Callaghan, NSW, 2308, Australia

    Minoo Heidari Kani, Eng-Cheng Chan, Roger C. Young, Trent Butler, Roger Smith & Jonathan W. Paul

  2. Hunter Medical Research Institute, 1 Kookaburra Circuit, New Lambton Heights, NSW, 2305, Australia

    Minoo Heidari Kani, Eng-Cheng Chan, Trent Butler, Roger Smith & Jonathan W. Paul

  3. Priority Research Centre of Reproductive Science, University of Newcastle, Callaghan, NSW, 2308, Australia

    Minoo Heidari Kani, Eng-Cheng Chan, Trent Butler, Roger Smith & Jonathan W. Paul

  4. John Hunter Hospital, New Lambton Heights, NSW, 2305, Australia

    Roger Smith

Authors
  1. Minoo Heidari Kani
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eng-Cheng Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roger C. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Trent Butler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roger Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jonathan W. Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Minoo Heidari Kani.

Additional information

Associate Editor Christiani Amorim oversaw the review of this article.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heidari Kani, M., Chan, EC., Young, R.C. et al. 3D Cell Culturing and Possibilities for Myometrial Tissue Engineering. Ann Biomed Eng 45, 1746–1757 (2017). https://doi.org/10.1007/s10439-016-1749-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-016-1749-5

Keywords

Search

Navigation