Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture

Biomaterials

Volumn 124, Issue , 2017, Pages 106-115

  Zhu, Wei ^a   Qu, Xin ^a   Zhu, Jie ^b   Ma, Xuanyi ^c   Patel, Sherrina ^b   Liu, Justin ^b   Wang, Pengrui ^b   Lai, Cheuk Sun Edwin ^a   Gou, Maling ^d   Xu, Yang ^e   Zhang, Kang ^b   Chen, Shaochen ^a,b,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d SICHUAN UNIVERSITY   (China)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

3D bioprinting; Biomaterials; Complex microarchitecture; Tissue engineering; Vasculature

Indexed keywords

3D PRINTERS; BIOMATERIALS; BLOOD VESSELS; CELLS; COMPLEX NETWORKS; COMPUTER ARCHITECTURE; CYTOLOGY; ENDOTHELIAL CELLS; HISTOLOGY; TISSUE ENGINEERING;

BIOPRINTING; MICRO ARCHITECTURES; MULTIPLE CELL TYPES; PROGRESSIVE FORMATIONS; SACRIFICIAL MATERIAL; THREEDIMENSIONAL (3-D); VASCULARIZED TISSUES; VASCULATURE;

TISSUE;

BIOMATERIAL;

ANASTOMOSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOPRINTING; CELL COMPOSITION; CELL ENCAPSULATION; CELL SURVIVAL; CELLS BY BODY ANATOMY; CONTROLLED STUDY; ENDOTHELIUM CELL; ERYTHROCYTE; HUMAN; HUMAN CELL; HYDROGEL; IN VITRO STUDY; IN VIVO STUDY; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; THREE DIMENSIONAL PRINTING; TISSUE ENGINEERING; ANGIOGENESIS; BIOARTIFICIAL ORGAN; CELL CULTURE; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MICROVASCULATURE; PHYSIOLOGY; PROCEDURES;

BIOARTIFICIAL ORGANS; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; MICROVESSELS; NEOVASCULARIZATION, PHYSIOLOGIC; PRINTING, THREE-DIMENSIONAL; TISSUE ENGINEERING;

EID: 85012036974     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2017.01.042     Document Type: Article

References (42)

1. [1] Miller, J.S., Stevens, K.R., Yang, M.T., Baker, B.M., Nguyen, D.-H.T., Cohen, D.M., Toro, E., Chen, A.A., Galie, P.A., Yu, X., Chaturvedi, R., Bhatia, S.N., Chen, C.S., Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11 (2012), 768–774, 10.1038/nmat3357.
2. [2] Baranski, J.D., Chaturvedi, R.R., Stevens, K.R., Eyckmans, J., Carvalho, B., Solorzano, R.D., Yang, M.T., Miller, J.S., Bhatia, S.N., Chen, C.S., Geometric control of vascular networks to enhance engineered tissue integration and function. Proc. Natl. Acad. Sci. 110 (2013), 7586–7591, 10.1073/pnas.1217796110.
3. [3] Kolesky, D.B., Truby, R.L., Gladman, A.S., Busbee, T.A., Homan, K.A., Lewis, J.A., 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater 26 (2014), 3124–3130, 10.1002/adma.201305506.
4. [4] Lee, K.Y., Peters, M.C., Anderson, K.W., Mooney, D.J., Controlled growth factor release from synthetic extracellular matrices. Nature 408 (2000), 998–1000, 10.1038/35050141.
5. [5] Fischbach, C., Mooney, D.J., Polymers for pro- and anti-angiogenic therapy. Biomaterials 28 (2007), 2069–2076, 10.1016/j.biomaterials.2006.12.029.
6. [6] Richardson, T.P., Peters, M.C., Ennett, a B., Mooney, D.J., Polymeric system for dual growth factor delivery. Nat. Biotechnol. 19 (2001), 1029–1034, 10.1038/nbt1101-1029.
7. [7] Chen, X., Aledia, A.S., Ghajar, C.M., Griffith, C.K., Putnam, A.J., Hughes, C.C.W., George, S.C., Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng. Part A 15 (2009), 1363–1371, 10.1089/ten.tea.2008.0314.
8. [8] Sahota, P.S., Burn, J.L., Brown, N.J., MacNeil, S., Approaches to improve angiogenesis in tissue-engineered skin. Wound Repair Regen. 12 (2004), 635–642, 10.1111/j.1067-1927.2004.12608.x.
9. [9] Levenberg, S., Rouwkema, J., Macdonald, M., Garfein, E.S., Kohane, D.S., Darland, D.C., Marini, R., van Blitterswijk, C. a, Mulligan, R.C., D'Amore, P. a, Langer, R., Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23 (2005), 879–884, 10.1038/nbt1109.
10. [10] Caspi, O., Lesman, A., Basevitch, Y., Gepstein, A., Arbel, G., Huber, I., Habib, M., Gepstein, L., Levenberg, S., Tissue engineering of vascularized cardiac muscle from human embryonic stem cells. Circ. Res. 100 (2007), 263–272, 10.1161/01.RES.0000257776.05673.ff.
11. [11] Koike, N., Fukumura, D., Gralla, O., Au, P., Schechner, J.S., Jain, R.K., Tissue engineering: creation of long-lasting blood vessels. Nature 428 (2004), 138–139, 10.1038/428138a.
12. [12] Zhang, B., Montgomery, M., Chamberlain, M.D., Ogawa, S., Korolj, A., Pahnke, A., Wells, L.A., Massé, S., Kim, J., Reis, L., Momen, A., Nunes, S.S., Wheeler, A.R., Nanthakumar, K., Keller, G., Sefton, M.V., Radisic, M., Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater 1 (2016), 1–42, 10.1038/nmat4570.
13. [13] Bertassoni, L.E., Cecconi, M., Manoharan, V., Nikkhah, M., Hjortnaes, J., Cristino, A.L., Barabaschi, G., Demarchi, D., Dokmeci, M.R., Yang, Y., Khademhosseini, A., Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab. Chip 14 (2014), 2202–2211, 10.1039/c4lc00030g.
14. [14] Kolesky, D.B., Homan, K.A., Skylar-Scott, M.A., Lewis, J.A., Three-dimensional bioprinting of thick vascularized tissues. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 3179–3184, 10.1073/pnas.1521342113.
15. [15] Jia, W., Gungor-Ozkerim, P.S., Zhang, Y.S., Yue, K., Zhu, K., Liu, W., Pi, Q., Byambaa, B., Dokmeci, M.R., Shin, S.R., Khademhosseini, A., Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomaterials 106 (2016), 58–68, 10.1016/j.biomaterials.2016.07.038.
16. [16] Zhang, Y.S., Arneri, A., Bersini, S., Shin, S.R., Zhu, K., Goli-Malekabadi, Z., Aleman, J., Colosi, C., Busignani, F., Dell'Erba, V., Bishop, C., Shupe, T., Demarchi, D., Moretti, M., Rasponi, M., Dokmeci, M.R., Atala, A., Khademhosseini, A., Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials 110 (2016), 45–59, 10.1016/j.biomaterials.2016.09.003.
17. [17] Chan, V., Zorlutuna, P., Jeong, J.H., Kong, H., Bashir, R., Three-dimensional photopatterning of hydrogels using stereolithography for long-term cell encapsulation. Lab. Chip, 10, 2010, 2062, 10.1039/c004285d.
18. [18] Zhang, a P., Qu, X., Soman, P., Hribar, K.C., Lee, J.W., Chen, S., He, S., Rapid fabrication of complex 3D extracellular microenvironments by dynamic optical projection stereolithography. Adv. Mater 24 (2012), 4266–4270, 10.1002/adma.201202024.
19. [19] Tumbleston, J.R., Shirvanyants, D., Ermoshkin, N., Janusziewicz, R., Johnson, A.R., Kelly, D., Chen, K., Pinschmidt, R., Rolland, J.P., Ermoshkin, A., Samulski, E.T., DeSimone, J.M., Continuous liquid interface production of 3D objects. Science (80-. ) 347 (2015), 1349–1352, 10.1126/science.aaa2397.
20. [20] Suri, S., Han, L.-H., Zhang, W., Singh, A., Chen, S., Schmidt, C.E., Solid freeform fabrication of designer scaffolds of hyaluronic acid for nerve tissue engineering. Biomed. Microdevices 13 (2011), 983–993, 10.1007/s10544-011-9568-9.
21. [21] Gou, M., Qu, X., Zhu, W., Xiang, M., Yang, J., Zhang, K., Wei, Y., Chen, S., Bio-inspired detoxification using 3D-printed hydrogel nanocomposites. Nat. Commun., 5, 2014, 3774, 10.1038/ncomms4774.
22. [22] Zhu, W., Li, J., Leong, Y.J., Rozen, I., Qu, X., Dong, R., Wu, Z., Gao, W., Chung, P.H., Wang, J., Chen, S., 3D-Printed artificial microfish. Adv. Mater 27 (2015), 4411–4417, 10.1002/adma.201501372.
23. [23] Ma, X., Qu, X., Zhu, W., Li, Y.-S., Yuan, S., Zhang, H., Liu, J., Wang, P., Lai, C.S.E., Zanella, F., Feng, G.-S., Sheikh, F., Chien, S., Chen, S., Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc. Natl. Acad. Sci. 113 (2016), 2206–2211, 10.1073/pnas.1524510113.
24. [24] Leach, J.B., Bivens, K.A., Patrick, C.W., Schmidt, C.E., Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol. Bioeng. 82 (2003), 578–589, 10.1002/bit.10605.
25. [25] Nichol, J.W., Koshy, S.T., Bae, H., Hwang, C.M., Yamanlar, S., Khademhosseini, A., Cell-laden microengineered gelatin methacrylate hydrogels. Biomaterials 31 (2010), 5536–5544, 10.1016/j.biomaterials.2010.03.064.
26. [26] Fairbanks, B.D., Schwartz, M.P., Bowman, C.N., Anseth, K.S., Photoinitiated polymerization of PEG-diacrylate with lithium phenyl-2,4,6-trimethylbenzoylphosphinate: polymerization rate and cytocompatibility. Biomaterials 30 (2009), 6702–6707, 10.1016/j.biomaterials.2009.08.055.
27. [27] Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682, 10.1038/nmeth.2019.
28. [28] Burdick, J.A., Prestwich, G.D., Hyaluronic acid hydrogels for biomedical applications. Adv. Mater 23 (2011), H41–H56, 10.1002/adma.201003963.
29. [29] Burdick, J. a, Chung, C., Jia, X., Randolph, M. a, Langer, R., Controlled degradation and mechanical behavior of photopolymerized hyaluronic acid networks. Biomacromolecules 6 (2005), 386–391, 10.1021/bm049508a.
30. [30] Baier Leach, J., Bivens, K. a, Patrick, C.W., Schmidt, C.E., Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds. Biotechnol. Bioeng. 82 (2003), 578–589, 10.1002/bit.10605.
31. [311] Hribar, K.C., Choi, Y.S., Ondeck, M., Engler, A.J., Chen, S., Digital plasmonic patterning for localized tuning of hydrogel stiffness. Adv. Funct. Mater 24 (2014), 4922–4926, 10.1002/adfm.201400274.
32. [32] Choi, Y.S., Vincent, L.G., Lee, A.R., Kretchmer, K.C., Chirasatitsin, S., Dobke, M.K., Engler, A.J., The alignment and fusion assembly of adipose-derived stem cells on mechanically patterned matrices. Biomaterials 33 (2012), 6943–6951, 10.1016/j.biomaterials.2012.06.057.
33. [33] Vincent, L.G., Choi, Y.S., Alonso-Latorre, B., del Álamo, J.C., Engler, A.J., Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength. Biotechnol. J. 8 (2013), 472–484, 10.1002/biot.201200205.
34. [34] Isenberg, B.C., DiMilla, P.A., Walker, M., Kim, S., Wong, J.Y., Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97 (2009), 1313–1322, 10.1016/j.bpj.2009.06.021.
35. [35] Murphy, S.V., Atala, A., 3D bioprinting of tissues and organs. Nat. Biotechnol. 32 (2014), 773–785, 10.1038/nbt.2958.
36. [36] Chang, R., Nam, J., Sun, W., Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng. Part A 14 (2008), 41–48, 10.1089/ten.a.2007.0004.
37. [37] Smith, C.M., Christian, J.J., Warren, W.L., Williams, S.K., Characterizing environmental factors that impact the viability of tissue-engineered constructs fabricated by a direct-write bioassembly tool. Tissue Eng. 13 (2007), 373–383, 10.1089/ten.2007.13.ft-338.
38. [38] Aguado, B.A., Mulyasasmita, W., Su, J., Lampe, K.J., Heilshorn, S.C., Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers. Tissue Eng. Part A 18 (2012), 806–815, 10.1089/ten.tea.2011.0391.
39. [39] Debbage, P.L., Sölder, E., Seidl, S., Hutzler, P., Hugl, B., Öfner, D., Kreczy, A., Intravital lectin perfusion analysis of vascular permeability in human micro- and macro- blood vessels. Histochem. Cell Biol. 116 (2001), 349–359, 10.1007/s004180100328.
40. [40] Debbage, P.L., Griebel, J., Ried, M., Gneiting, T., DeVries, A., Hutzler, P., Lectin intravital perfusion studies in tumor-bearing mice: micrometer-resolution, wide-area mapping of microvascular labeling, distinguishing efficiently and inefficiently perfused microregions in the tumor. J. Histochem. Cytochem 46 (1998), 627–639, 10.1177/002215549804600508.
41. [41] Rouwkema, J., Rivron, N.C., van Blitterswijk, C.A., Vascularization in tissue engineering. Trends Biotechnol. 26 (2008), 434–441, 10.1016/j.tibtech.2008.04.009.
42. [42] Novosel, E.C., Kleinhans, C., Kluger, P.J., Vascularization is the key challenge in tissue engineering. Adv. Drug Deliv. Rev. 63 (2011), 300–311, 10.1016/j.addr.2011.03.004.