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Cited by 393D Printing in Biomedical ResearchCellular Mechanics and InteractionsPluripotent Stem Cells Research

A 3D bioprinted cortical organoid platform for modeling human brain development

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Cadena, Melissa A., Sing, Anson, Taylor, Kylie, Jin, Linqi, Ning, Liqun, Salar Amoli, Mehdi, Singh, Yamini, Lanjewar, Samantha N. +3 more·2024·Advanced Healthcare Materials
DOI 10.1002/adhm.202401603PMC PMC11518656
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Abstract

The ability to promote three‐dimensional (3D) self‐organization of induced pluripotent stem cells into complex tissue structures called organoids presents new opportunities for the field of developmental biology. Brain organoids have been used to investigate principles of neurodevelopment and neuropsychiatric disorders and serve as a drug screening and discovery platform. However, brain organoid cultures are currently limited by a lacking ability to precisely control their extracellular environment. Here, this work employs 3D bioprinting to generate a high‐throughput, tunable, and reproducible scaffold for controlling organoid development and patterning. Additionally, this approach supports the coculture of organoids and vascular cells in a custom architecture containing interconnected endothelialized channels. Printing fidelity and mechanical assessments confirm that fabricated scaffolds closely match intended design features and exhibit stiffness values reflective of the developing human brain. Using organoid growth, viability, cytoarchitecture, proliferation, and transcriptomic benchmarks, this work finds that organoids cultured within the bioprinted scaffold long‐term are healthy and have expected neuroectodermal differentiation. Lastly, this work confirms that the endothelial cells (ECs) in printed channel structures can migrate toward and infiltrate into the embedded organoids. This work demonstrates a tunable 3D culturing platform that can be used to create more complex and accurate models of human brain development and underlying diseases.

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  • Successful fabrication of stable 3D constructs relies on hydrogels with optimized rheological behavior, structural stability, and physicochemical properties that ensure printability and shape fidelity.

    “However, the successful fabrication of stable 3D constructs relies on hydrogels with optimized rheological behavior, structural stability, and physicochemical properties that ensure printability and shape fidelity [7,8,9].”

    From Montmorillonite-reinforced methacrylated collagen/methacrylated silk fibroin hydrogel-based inks: rheological and physicochemical characterization for bone scaffold applications (2026) · cites this paper as [8]

  • The formulations containing 2.0% and 3.0% MMT exhibited significantly higher shape fidelity than the formulation without MMT, whereas no significant difference was observed between the control and the 1.0% MMT group.

    “Tukey's post hoc test showed that the formulations containing 2.0% and 3.0% MMT exhibited significantly higher shape fidelity than the formulation without MMT, whereas no significant difference was observed between the control and the 1.0% MMT group [8].”

    From Montmorillonite-reinforced methacrylated collagen/methacrylated silk fibroin hydrogel-based inks: rheological and physicochemical characterization for bone scaffold applications (2026) · cites this paper as [8]

    The Results and Printing Fidelity Characterization sections describe the shape fidelity of GelMA scaffolds, but do not report MMT formulations or comparisons among 0%, 1.0%, 2.0%, and 3.0% MMT. Searches for MMT, montmorillonite, and the claimed concentration comparisons found no passage addressing those results. Page numbers were unavailable in our copy. (LLM, conf=0.77)

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  1. [1]M. A. Lancaster, M. Renner, C. A. Martin, D. Wenzel, L. S. Bicknell, M. E. Hurles, T. Homfray, J. M. Penninger, A. P. Jackson, J. A. Knoblich, Nature 2013, 501, 373. 23995685 PMC3817409
  2. [2]S. A. Sloan, S. Darmanis, N. Huber, T. A. Khan, F. Birey, C. Caneda, R. Reimer, S. R. Quake, B. A. Barres, S. P. Paşca, Neuron 2017, 95, 779. 28817799 PMC5890820
  3. [3]S. A. Sloan, J. Andersen, A. M. Pasca, F. Birey, S. P. Pasca, Nat. Protoc. 2018, 13, 2062. 30202107 PMC6597009
  4. [4]X. Qian, H. N. Nguyen, M. M. Song, C. Hadiono, S. C. Ogden, C. Hammack, B. Yao, G. R. Hamersky, F. Jacob, C. Zhong, K. J. Yoon, W. Jeang, L. Lin, Y. Li, J. Thakor, D. A. Berg, C. Zhang, E. Kang, M. Chickering, D. Nauen, C. Y. Ho, Z. Wen, K. M. Christian, P. Y. Shi, B. J. Maher, H. Wu, P. Jin, H. Tang, H. Song, G. L. Ming, Cell 2016, 165, 1238. 27118425 PMC4900885
  5. [5]A. M. Pasca, S. A. Sloan, L. E. Clarke, Y. Tian, C. D. Makinson, N. Huber, C. H. Kim, J. Y. Park, N. A. O'Rourke, K. D. Nguyen, S. J. Smith, J. R. Huguenard, D. H. Geschwind, B. A. Barres, S. P. Pasca, Nat. Methods 2015, 12, 671. 26005811 PMC4489980
  6. [6]M. A. Skylar‐Scott, J. Y. Huang, A. Lu, A. H. M. Ng, T. Duenki, S. Liu, L. L. Nam, S. Damaraju, G. M. Church, J. A. Lewis, Nat. Biomed. Eng. 2022, 6, 449. 35332307 PMC9506705
  7. [7]M. A. Lancaster, J. A. Knoblich, Science 2014, 345, 1247125. 25035496
  8. [8]H. Clevers, Cell 2016, 165, 1586. 27315476
  9. [9]X. Qian, Y. Su, C. D. Adam, A. U. Deutschmann, S. R. Pather, E. M. Goldberg, K. Su, S. Li, L. Lu, F. Jacob, P. T. T. Nguyen, S. Huh, A. Hoke, S. E. Swinford‐Jackson, Z. Wen, X. Gu, R. C. Pierce, H. Wu, L. A. Briand, H. I. Chen, J. A. Wolf, H. Song, G. L. Ming, Cell Stem Cell 2020, 26, 766. 32142682 PMC7366517
  10. [10]F. Birey, J. Andersen, C. D. Makinson, S. Islam, W. Wei, N. Huber, H. C. Fan, K. R. C. Metzler, G. Panagiotakos, N. Thom, N. A. O'Rourke, L. M. Steinmetz, J. A. Bernstein, J. Hallmayer, J. R. Huguenard, S. P. Paşca, Nature 2017, 545, 54. 28445465 PMC5805137
  11. [11]J. Andersen, O. Revah, Y. Miura, N. Thom, N. D. Amin, K. W. Kelley, M. Singh, X. Chen, M. V. Thete, E. M. Walczak, H. Vogel, H. C. Fan, S. P. Paşca, Cell 2020, 183, 1913. 33333020 PMC8711252
  12. [12]G. Y. Cederquist, J. J. Asciolla, J. Tchieu, R. M. Walsh, D. Cornacchia, M. D. Resh, L. Studer, Nat. Biotechnol. 2019, 37, 436. 30936566 PMC6447454
  13. [13]A. Girós, J. Morante, C. Gil‐Sanz, A. Fairén, M. Costell, BMC Dev. Biol. 2007, 7, 29. 17411441 PMC1852307
  14. [14]N. Luo, H. Li, B. Xiang, L. Qiao, J. He, Y. Ji, Y. Liu, S. Li, R. Lu, Y. Li, W. Meng, Y. Wu, H. Xu, X. Mo, Sci. Rep. 2016, 6, 25300. 27143125 PMC4855150
  15. [15]N. Haubst, E. Georges‐Labouesse, A. De Arcangelis, U. Mayer, M. Götz, Development 2006, 133, 3245. 16873583
  16. [16]L. Luckenbill‐Edds, J. L. Carrington, Cell Tissue Res. 1988, 252, 573. 3396055
  17. [17]G. D'Arcangelo, G. G. Miao, S. C. Chen, H. D. Soares, J. I. Morgan, T. Curran, Nature 1995, 374, 719. 7715726
  18. [18]Z. L. Chen, V. Haegeli, H. Yu, S. Strickland, Dev. Biol. 2009, 327, 158. 19118544 PMC2669444
  19. [19]K. R. Long, W. B. Huttner, Front. Cell Neurosci. 2022, 15, 804649. 35140590 PMC8818730
  20. [20]D. Bonneh‐Barkay, C. A. Wiley, Brain Pathol. 2009, 19, 573. 18662234 PMC2742568
  21. [21]G. Potjewyd, S. Moxon, T. Wang, M. Domingos, N. M. Hooper, Trends Biotechnol. 2018, 36, 457. 29422410
  22. [22]J. S. Goldberg, K. K. Hirschi, Regener. Med. 2009, 4, 879. PMC2836203 19903006
  23. [23]M. R. Mancuso, F. Kuhnert, C. J. Kuo, Lymphatic Res. Biol. 2008, 6, 173. PMC2712664 19093790
  24. [24]M. A. Lancaster, J. A. Knoblich, Nat. Protoc. 2014, 9, 2329. 25188634 PMC4160653
  25. [25]J. A. Bagley, D. Reumann, S. Bian, J. Lévi‐Strauss, J. A. Knoblich, Nat. Methods 2017, 14, 743. 28504681 PMC5540177
  26. [26]T. G. Krieger, S. M. Tirier, J. Park, K. Jechow, T. Eisemann, H. Peterziel, P. Angel, R. Eils, C. Conrad, Neuro‐Oncology 2020, 22, 1138. 32297954 PMC7594554
  27. [27]G. Quadrato, T. Nguyen, E. Z. Macosko, J. L. Sherwood, S. Min Yang, D. R. Berger, N. Maria, J. Scholvin, M. Goldman, J. P. Kinney, E. S. Boyden, J. W. Lichtman, Z. M. Williams, S. A. McCarroll, P. Arlotta, Nature 2017, 545, 48. 28445462 PMC5659341
  28. [28]R. Simsa, T. Rothenbücher, H. Gürbüz, N. Ghosheh, J. Emneus, L. Jenndahl, D. L. Kaplan, N. Bergh, A. M. Serrano, P. Fogelstrand, PLoS One 2021, 16, e0245685. 33507989 PMC7842896
  29. [29]D. Sood, K. Chwalek, E. Stuntz, D. Pouli, C. Du, M. Tang‐Schomer, I. Georgakoudi, L. D. Black 3rd, D. L. Kaplan, ACS Biomater. Sci. Eng. 2016, 2, 131. 29034320 PMC5636008
  30. [30]A.‐N. Cho, Y. Jin, Y. An, J. Kim, Y. S. Choi, J. S. Lee, J. Kim, W.‐Y. Choi, D.‐J. Koo, W. Yu, G.‐E. Chang, D.‐Y. Kim, S.‐H. Jo, J. Kim, S.‐Y. Kim, Y.‐G. Kim, J. Y. Kim, N. Choi, E. Cheong, Y.‐J. Kim, H. S. Je, H.‐C. Kang, S.‐W. Cho, Nat. Commun. 2021, 12, 4730. 34354063 PMC8342542
  31. [31]A. R. Cortez, H. M. Poling, N. E. Brown, A. Singh, M. M. Mahe, M. A. Helmrath, Surgery 2018, 164, 643. 30072255 PMC6326178
  32. [32]A. A. Mansour, J. T. Gonçalves, C. W. Bloyd, H. Li, S. Fernandes, D. Quang, S. Johnston, S. L. Parylak, X. Jin, F. H. Gage, Nat. Biotechnol. 2018, 36, 432. 29658944 PMC6331203
  33. [33]Y. Shi, L. Sun, M. Wang, J. Liu, S. Zhong, R. Li, P. Li, L. Guo, A. Fang, R. Chen, W. P. Ge, Q. Wu, X. Wang, PLoS Biol. 2020, 18, e3000705. 32401820 PMC7250475
  34. [34]M. T. Pham, K. M. Pollock, M. D. Rose, W. A. Cary, H. R. Stewart, P. Zhou, J. A. Nolta, B. Waldau, Neuroreport 2018, 29, 588. 29570159 PMC6476536
  35. [35]B. Cakir, Y. Xiang, Y. Tanaka, M. H. Kural, M. Parent, Y. J. Kang, K. Chapeton, B. Patterson, Y. Yuan, C. S. He, M. S. B. Raredon, J. Dengelegi, K. Y. Kim, P. Sun, M. Zhong, S. Lee, P. Patra, F. Hyder, L. E. Niklason, S. H. Lee, Y. S. Yoon, I. H. Park, Nat. Methods 2019, 16, 1169. 31591580 PMC6918722
  36. [36]S. Boccardo, E. Gaudiello, L. Melly, G. Cerino, D. Ricci, I. Martin, F. Eckstein, A. Banfi, A. Marsano, Acta Biomater. 2016, 42, 127. 27469308
  37. [37]S. G. Guerreiro, R. E. Unger, N. Cerqueira, A. Sartoris, M. J. Martins, M. A. Barbosa, R. Soares, P. L. Granja, C. J. Kirkpatrick, J. Cell. Biochem. 2021, 122, 116. 32748513
  38. [38]S. Blatt, V. Burkhardt, P. W. Kämmerer, A. M. Pabst, K. Sagheb, M. Heller, B. Al‐Nawas, E. Schiegnitz, Clin. Oral Investig. 2020, 24, 3425. 32030513
  39. [39]S. V. Murphy, A. Atala, Nat. Biotechnol. 2014, 32, 773. 25093879
  40. [40]D. B. Kolesky, K. A. Homan, M. A. Skylar‐Scott, J. A. Lewis, Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 3179. 26951646 PMC4812707
  41. [41]M. A. Skylar‐Scott, S. G. M. Uzel, L. L. Nam, J. H. Ahrens, R. L. Truby, S. Damaraju, J. A. Lewis, Sci. Adv. 2019, 5, eaaw2459. 31523707 PMC6731072
  42. [42]L. Ning, J. Shim, M. L. Tomov, R. Liu, R. Mehta, A. Mingee, B. Hwang, L. Jin, A. Mantalaris, C. Xu, M. Mahmoudi, K. C. Goldsmith, V. Serpooshan, Adv. Sci. 2022, 9, e2200244. PMC9376856 35644929
  43. [43]M. Cadena, L. Ning, A. King, B. Hwang, L. Jin, V. Serpooshan, S. A. Sloan, Adv. Healthcare Mater. 2021, 10, e2001600. PMC8711131 33200587
  44. [44]D. Lam, H. A. Enright, J. Cadena, S. K. G. Peters, A. P. Sales, J. J. Osburn, D. A. Soscia, K. S. Kulp, E. K. Wheeler, N. O. Fischer, Sci. Rep. 2019, 9, 4159. 30858401 PMC6411890
  45. [45]C. Nicholson, E. Syková, Trends Neurosci. 1998, 21, 207. 9610885
  46. [46]J. W. Fawcett, T. Oohashi, T. Pizzorusso, Nat. Rev. Neurosci. 2019, 20, 451. 31263252
  47. [47]Q. Gu, E. Tomaskovic‐Crook, R. Lozano, Y. Chen, R. M. Kapsa, Q. Zhou, G. G. Wallace, J. M. Crook, Adv. Healthcare Mater. 2016, 5, 1429. 27028356
  48. [48]E. Monferrer, S. Martín‐Vañó, A. Carretero, A. García‐Lizarribar, R. Burgos‐Panadero, S. Navarro, J. Samitier, R. Noguera, Sci. Rep. 2020, 10, 6370. 32286364 PMC7156444
  49. [49]L. D. Vega, D. A. R. Gómez, E. Abelseth, L. Abelseth, V. A. d. Silva, S. M. Willerth, Appl. Sci. 2018, 8, 2414.
  50. [50]Q. Gu, E. Tomaskovic‐Crook, G. G. Wallace, J. M. Crook, Adv. Healthcare Mater. 2017, 6, 1700175. 28544655
  51. [51]D. F. Duarte Campos, A. Bonnin Marquez, C. O'Seanain, H. Fischer, A. Blaeser, M. Vogt, D. Corallo, S. Aveic, Cancers 2019, 11, 180. 30764492 PMC6406373
  52. [52]A. Dravid, A. McCaughey‐Chapman, B. Raos, S. J. O'Carroll, B. Connor, D. Svirskis, Biomed. Mater. 2022, 17, 055001. 35654031
  53. [53]B. A. G. de Melo, E. M. Cruz, T. N. Ribeiro, M. V. Mundim, M. A. Porcionatto, J. Visualized Exp. 2021. 34338675
  54. [54]E. V. Alakpa, A. Bahrd, K. Wiklund, M. Andersson, L. N. Novikov, C. Ljungberg, P. Kelk, Gels 2023, 9, 172. 36975621 PMC10048219
  55. [55]J. P. Jiang, X. Y. Liu, F. Zhao, X. Zhu, X. Y. Li, X. G. Niu, Z. T. Yao, C. Dai, H. Y. Xu, K. Ma, X. Y. Chen, S. Zhang, Neural Regener. Res. 2020, 15, 959. PMC6990792 31719263
  56. [56]C. Chen, M. L. Zhao, R. K. Zhang, G. Lu, C. Y. Zhao, F. Fu, H. T. Sun, S. Zhang, Y. Tu, X. H. Li, J. Biomed. Mater. Res., Part A 2017, 105, 1324. 28120511
  57. [57]X. Li, X. Wang, X. Wang, H. Chen, X. Zhang, L. Zhou, T. Xu, 3 Biotech 2018, 8, 342. PMC6063810 30073127
  58. [58]Z. Wu, Q. Li, S. Xie, X. Shan, Z. Cai, Mater. Sci. Eng., C 2020, 109, 110530. 32228940
  59. [59]M. A. Heinrich, R. Bansal, T. Lammers, Y. S. Zhang, R. Michel Schiffelers, J. Prakash, Adv. Mater. 2019, 31, 1806590. 30702785
  60. [60]X. Zhou, H. Cui, M. Nowicki, S. Miao, S. J. Lee, F. Masood, B. T. Harris, L. G. Zhang, ACS Appl. Mater. Interfaces 2018, 10, 8993. 29461046
  61. [61]J. Chen, D. Huang, L. Wang, J. Hou, H. Zhang, Y. Li, S. Zhong, Y. Wang, Y. Wu, W. Huang, J. Colloid Interface Sci. 2020, 574, 162. 32311538
  62. [62]M. Tang, Q. Xie, R. C. Gimple, Z. Zhong, T. Tam, J. Tian, R. L. Kidwell, Q. Wu, B. C. Prager, Z. Qiu, A. Yu, Z. Zhu, P. Mesci, H. Jing, J. Schimelman, P. Wang, D. Lee, M. H. Lorenzini, D. Dixit, L. Zhao, S. Bhargava, T. E. Miller, X. Wan, J. Tang, B. Sun, B. F. Cravat, A. R. Muotri, S. Chen, J. N. Rich, Cell Res. 2020, 30, 833. 32499560 PMC7608409
  63. [63]H. Shirahama, B. H. Lee, L. P. Tan, N.‐J. Cho, Sci. Rep. 2016, 6, 31036. 27503340 PMC4977492
  64. [64]R. Gauvin, Y.‐C. Chen, J. W. Lee, P. Soman, P. Zorlutuna, J. W. Nichol, H. Bae, S. Chen, A. Khademhosseini, Biomaterials 2012, 33, 3824. 22365811 PMC3766354
  65. [65]J. Tao, J. Zhang, T. Du, X. Xu, X. Deng, S. Chen, J. Liu, Y. Chen, X. Liu, M. Xiong, Y. Luo, H. Cheng, J. Mao, L. Cardon, M. Gou, Y. Wei, Acta Biomater. 2019, 90, 49. 30930306
  66. [66]G. Camci‐Unal, D. Cuttica, N. Annabi, D. Demarchi, A. Khademhosseini, Biomacromolecules 2013, 14, 1085. 23419055 PMC3643200
  67. [67]T. J. Hinton, A. Hudson, K. Pusch, A. Lee, A. W. Feinberg, ACS Biomater. Sci. Eng. 2016, 2, 1781. 27747289 PMC5059754
  68. [68]L. Ning, C. J. Gil, B. Hwang, A. S. Theus, L. Perez, M. L. Tomov, H. Bauser‐Heaton, V. Serpooshan, Appl. Phys. Rev. 2020, 7, 041319. 33425087 PMC7780402
  69. [69]L. Ning, R. Mehta, C. Cao, A. Theus, M. Tomov, N. Zhu, E. R. Weeks, H. Bauser‐Heaton, V. Serpooshan, ACS Appl. Mater. Interfaces 2020, 12, 44563. 32966746
  70. [70]Y. Zheng, G. Wu, L. Chen, Y. Zhang, Y. Luo, Y. Zheng, F. Hu, T. Forouzanfar, H. Lin, B. Liu, Bioact. Mater. 2021, 6, 627. 33005827 PMC7508914
  71. [71]Q. L. Loh, C. Choong, Tissue Eng., Part B 2013, 19, 485. PMC3826579 23672709
  72. [72]H. Yin, M. Zhu, Y. Wang, L. Luo, Q. Ye, B. H. Lee, Front. Soft Matter 2023, 2, 1101680.
  73. [73]A. J. Engler, H. L. Sweeney, D. E. Discher, J. E. Schwarzbauer, Cell 2006, 126, 677. 16923388
  74. [74]G. J. Her, H. C. Wu, M. H. Chen, M. Y. Chen, S. C. Chang, T. W. Wang, Acta Biomater. 2013, 9, 5170. 23079022
  75. [75]T. P. Kraehenbuehl, R. Langer, L. S. Ferreira, Nat. Methods 2011, 8, 731. 21878920
  76. [76]S. Velasco, A. J. Kedaigle, S. K. Simmons, A. Nash, M. Rocha, G. Quadrato, B. Paulsen, L. Nguyen, X. Adiconis, A. Regev, J. Z. Levin, P. Arlotta, Nature 2019, 570, 523. 31168097 PMC6906116
  77. [77]H. Zhisong, D. Leander, F. Jonas Simon, S. Artur, X. L. Katelyn, S. Irena, L. Hsiu‐Chuan, S. Malgorzata, A. Alexander, Q. Giorgia, S. Jieran, P. P. Sergiu, J. G. Camp, T. Fabian, T. Barbara, bioRxiv 2023 2023.10.05.561097.
  78. [78]A. Bhaduri, M. G. Andrews, W. Mancia Leon, D. Jung, D. Shin, D. Allen, D. Jung, G. Schmunk, M. Haeussler, J. Salma, A. A. Pollen, T. J. Nowakowski, A. R. Kriegstein, Nature 2020, 578, 142. 31996853 PMC7433012
  79. [79]D. Simão, M. M. Silva, A. P. Terrasso, F. Arez, M. F. Q. Sousa, N. Z. Mehrjardi, T. Šarić, P. Gomes‐Alves, N. Raimundo, P. M. Alves, C. Brito, Stem Cell Rep. 2018, 11, 552. PMC6094163 30057262
  80. [80]R. Choudhuri, H. T. Zhang, S. Donnini, M. Ziche, R. Bicknell, Cancer Res. 1997, 57, 1814. 9135027
  81. [81]R. N. Munji, A. L. Soung, G. A. Weiner, F. Sohet, B. D. Semple, A. Trivedi, K. Gimlin, M. Kotoda, M. Korai, S. Aydin, A. Batugal, A. C. Cabangcala, P. G. Schupp, M. C. Oldham, T. Hashimoto, L. J. Noble‐Haeusslein, R. Daneman, Nat. Neurosci. 2019, 22, 1892. 31611708 PMC6858546
  82. [82]J. Koffler, W. Zhu, X. Qu, O. Platoshyn, J. N. Dulin, J. Brock, L. Graham, P. Lu, J. Sakamoto, M. Marsala, S. Chen, M. H. Tuszynski, Nat. Med. 2019, 25, 263. 30643285 PMC6559945
  83. [83]L. Zhou, A. C. Wolfes, Y. Li, D. C. W. Chan, H. Ko, F. G. Szele, H. Bayley, Adv. Mater. 2020, 32, 2002183. 32537827
  84. [84]D. Joung, V. Truong, C. C. Neitzke, S. Z. Guo, P. J. Walsh, J. R. Monat, F. Meng, S. H. Park, J. R. Dutton, A. M. Parr, M. C. McAlpine, Adv. Funct. Mater. 2018, 28, 1801850. 32595422 PMC7319181
  85. [85]L. Ning, H. Sun, T. Lelong, R. Guilloteau, N. Zhu, D. J. Schreyer, X. Chen, Biofabrication 2018, 10, 035014. 29911990
  86. [86]K. Franze, P. A. Janmey, J. Guck, Annu. Rev. Biomed. Eng. 2013, 15, 227. 23642242
  87. [87]I. Sack, B. Beierbach, J. Wuerfel, D. Klatt, U. Hamhaber, S. Papazoglou, P. Martus, J. Braun, NeuroImage 2009, 46, 652. 19281851
  88. [88]M. C. Murphy, J. Huston 3rd, C. R. Jack Jr., K. J. Glaser, A. Manduca, J. P. Felmlee, R. L. Ehman, J. Magn. Reson. Imaging 2011, 34, 494. 21751286 PMC3217096
  89. [89]W. B. Pope, L. Mirsadraei, A. Lai, A. Eskin, J. Qiao, H. J. Kim, B. Ellingson, P. L. Nghiemphu, S. Kharbanda, R. H. Soriano, S. F. Nelson, W. Yong, H. S. Phillips, T. F. Cloughesy, Am. J. Neuroradiol. 2012, 33, 1059. 22268080 PMC8013245
  90. [90]S. S. Margulies, K. L. Thibault, J. Biomech. Eng. 2000, 122, 364. 11036559
  91. [91]L. R. Madden, D. J. Mortisen, E. M. Sussman, S. K. Dupras, J. A. Fugate, J. L. Cuy, K. D. Hauch, M. A. Laflamme, C. E. Murry, B. D. Ratner, Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 15211. 20696917 PMC2930533
  92. [92]O. Oliviero, M. Ventre, P. A. Netti, Acta Biomater. 2012, 8, 3294. 22641106
  93. [93]A. Artel, H. Mehdizadeh, Y. C. Chiu, E. M. Brey, A. Cinar, Tissue Eng., Part A 2011, 17, 2133. 21513462
  94. [94]C. M. Murphy, F. J. O'Brien, Cell Adhes. Migr. 2010, 4, 377. PMC2958613 20421733
  95. [95]J. L. Schmidt, D. J. Tweten, A. A. Badachhape, A. J. Reiter, R. J. Okamoto, J. R. Garbow, P. V. Bayly, J. Mech. Behav. Biomed. Mater. 2018, 79, 30. 29253729 PMC5807163
  96. [96]M.‐H. Kim, S. Y. Tan, K. Yamahara, M. Kino‐oka, Acta Biomater. 2023, 170, 376. 37619896
  97. [97]F. Urciuolo, G. Imparato, P. A. Netti, Front. Bioeng. Biotechnol. 2023, 11, 1197075. 37434756 PMC10330728
  98. [98]C. M. Nelson, M. J. Bissell, Annu. Rev. Cell Dev. Biol. 2006, 22, 287. 16824016 PMC2933192
  99. [99]N. D. Leipzig, M. S. Shoichet, Biomaterials 2009, 30, 6867. 19775749
  100. [100]Y. Zhu, X. Li, R. R. R. Janairo, G. Kwong, A. D. Tsou, J. S. Chu, A. Wang, J. Yu, D. A.‐O. X. Wang, S. Li, J. Cell. Physiol. 2019, 234, 7569. 30368818 PMC6995283
  101. [101]Q.‐Y. Zhang, Y.‐Y. Zhang, J. Xie, C.‐X. Li, W.‐Y. Chen, B.‐L. Liu, X.‐a. Wu, S.‐N. Li, B. Huo, L.‐H. Jiang, H.‐C. Zhao, Sci. Rep. 2014, 4, 6215. 25163607 PMC4147369
  102. [102]J. Arulmoli, M. M. Pathak, L. P. McDonnell, J. L. Nourse, F. Tombola, J. C. Earthman, L. A. Flanagan, Sci. Rep. 2015, 5, 8499. 25686615 PMC4330529
  103. [103]E. Tomaskovic‐Crook, S. L. Higginbottom, B. Zhang, J. Bourke, G. G. Wallace, J. M. Crook, Organoids 2023, 2, 20.
  104. [104]A. A.‐O. GhavamiNejad, N. Ashammakhi, X. Y. Wu, A. Khademhosseini, Small 2020, 16, e2002931. 32734720 PMC7754762
  105. [105]D. N. Heo, S. Lee, R. Timsina, X. Qiu, N. J. Castro, L. G. Zhang, Mater. Sci. Eng., C 2019, 99, 582. 30889733
  106. [106]H. Stratesteffen, M. Köpf, F. Kreimendahl, A. Blaeser, S. Jockenhoevel, H. Fischer, Biofabrication 2017, 9, 045002. 28795951
  107. [107]L. Ning, R. Mehta, C. Cao, A. Theus, M. Tomov, N. Zhu, E. R. Weeks, H. Bauser‐Heaton, V. Serpooshan, ACS Appl. Mater. Interfaces 2020, 12, 44563. 32966746
  108. [108]S. Chen, M. L. Tomov, L. Ning, C. J. Gil, B. Hwang, H. D. Bauser‐Heaton, H. Chen, V. Serpooshan, Adv. Biol. 2023, 7, e2300124. 37132122
  109. [109]C. J. Gil, C. J. Evans, L. Li, A. J. Allphin, M. L. Tomov, L. Jin, M. Vargas, B. Hwang, J. Wang, V. Putaturo, G. Kabboul, A. S. Alam, R. K. Nandwani, Y. Wu, A. Sushmit, T. Fulton, M. Shen, J. M. Kaiser, L. Ning, R. Veneziano, N. Willet, G. Wang, H. Drissi, E. R. Weeks, H. D. Bauser‐Heaton, C. T. Badea, R. K. Roeder, V. Serpooshan, Adv. Healthcare Mater. 2023, 12, e2302271. PMC10842604 37709282
  110. [110]L. Ning, J. Shim, M. L. Tomov, R. Liu, R. Mehta, A. Mingee, B. Hwang, L. Jin, A. Mantalaris, C. Xu, M. Mahmoudi, K. C. Goldsmith, V. Serpooshan, Adv. Sci. 2022, 9, e2200244. PMC9376856 35644929
  111. [111]M. L. Tomov, L. Perez, L. Ning, H. Chen, B. Jing, A. Mingee, S. Ibrahim, A. S. Theus, G. Kabboul, K. Do, S. R. Bhamidipati, J. Fischbach, K. McCoy, B. A. Zambrano, J. Zhang, R. Avazmohammadi, A. Mantalaris, B. D. Lindsey, D. Frakes, L. P. Dasi, V. Serpooshan, H. Bauser‐Heaton, Adv. Healthcare Mater. 2021, 10, 2100968. PMC8823098 34369107
  112. [112]W. C. Oliver, G. M. Pharr, J. Mater. Res. 2004, 19, 3.
  113. [113]W. C. Oliver, G. M. Pharr, J. Mater. Res. 2011, 7, 1564.
  114. [114]R. M. Agoglia, D. Sun, F. Birey, S.‐J. Yoon, Y. Miura, K. Sabatini, S. P. Pașca, H. B. Fraser, Nature 2021, 592, 421. 33731928 PMC8719633
  115. [115]A. M. Bolger, M. Lohse, B. Usadel, Bioinformatics 2014, 30, 2114. 24695404 PMC4103590
  116. [116]A. Dobin, C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, T. R. Gingeras, Bioinformatics 2013, 29, 15. 23104886 PMC3530905
  117. [117]Y. Liao, G. K. Smyth, W. Shi, Bioinformatics 2014, 30, 923. 24227677
  118. [118]J. T. Leek, W. E. Johnson, H. S. Parker, A. E. Jaffe, J. D. Storey, Bioinformatics 2012, 28, 882. 22257669 PMC3307112
  119. [119]S. Anders, D. J. McCarthy, Y. Chen, M. Okoniewski, G. K. Smyth, W. Huber, M. D. Robinson, Nat. Protoc. 2013, 8, 1765. 23975260
  120. [120]A. S. F. Berry, C. F. Amorim, C. L. Berry, C. M. Syrett, E. D. English, D. P. Beiting, mBio 2021, 12, e0121421. 34225494 PMC8406131
  121. [121]L. Kolberg, U. Raudvere, I. Kuzmin, P. Adler, J. Vilo, H. Peterson, Nucleic Acids Res. 2023, 51, W207. 37144459 PMC10320099
  122. [122]S. E. Marsh, A. J. Walker, T. Kamath, L. Dissing‐Olesen, T. R. Hammond, T. Y. de Soysa, A. M. H. Young, S. Murphy, A. Abdulraouf, N. Nadaf, C. Dufort, A. C. Walker, L. E. Lucca, V. Kozareva, C. Vanderburg, S. Hong, H. Bulstrode, P. J. Hutchinson, D. J. Gaffney, D. A. Hafler, R. J. M. Franklin, E. Z. Macosko, B. Stevens, Nat. Neurosci. 2022, 25, 306. 35260865 PMC11645269
  123. [123]G. X. Y. Zheng, J. M. Terry, P. Belgrader, P. Ryvkin, Z. W. Bent, R. Wilson, S. B. Ziraldo, T. D. Wheeler, G. P. McDermott, J. Zhu, M. T. Gregory, J. Shuga, L. Montesclaros, J. G. Underwood, D. A. Masquelier, S. Y. Nishimura, M. Schnall‐Levin, P. W. Wyatt, C. M. Hindson, R. Bharadwaj, A. Wong, K. D. Ness, L. W. Beppu, H. J. Deeg, C. McFarland, K. R. Loeb, W. J. Valente, N. G. Ericson, E. A. Stevens, J. P. Radich, et al., Nat. Commun. 2017, 8, 14049. 28091601 PMC5241818
  124. [124]E. Y. Chen, C. M. Tan, Y. Kou, Q. Duan, Z. Wang, G. Vaz Meirelles, N. R. Clark, A. Ma'ayan, BMC Bioinf. 2013, 14, 128. PMC3637064 23586463
  125. [125]Z. Xie, A. Bailey, M. V. Kuleshov, D. J. B. Clarke, J. E. Evangelista, S. L. Jenkins, A. Lachmann, M. L. Wojciechowicz, E. Kropiwnicki, K. M. Jagodnik, M. Jeon, A. Ma'ayan, Curr. Protoc. 2021, 1, e90. 33780170 PMC8152575

Cited by

Sorted by citations

Authors
Cadena, M. A., Sing, A., Taylor, K., Jin, L., Ning, L., Salar Amoli, M., Singh, Y., Lanjewar, S. N., Tomov, M. L., Serpooshan, V., & Sloan, S. A.
Affiliations
  • Georgia Institute of Technology (US)
  • Emory University (US)
  • Cleveland State University (US)
  • Department of Biomedical Engineering Emory University School of Medicine and Georgia Institute of Technology Atlanta GA 30322 USA
Corresponding author
  • Serpooshan, Vahid
  • Sloan, Steven A.
ORCID
Venue
Advanced Healthcare Materials
Publisher
Wiley
Published
2024-06-08
Volume
13
Issue
27
Pages
e2401603-e2401603
ISSN
  • 2192-2640 (ISSN-L)
  • 2192-2659
DOI
10.1002/adhm.202401603
PMC
PMC11518656
OpenAlex
W4399163047
Cited by
39
References
16
Citations by year
2026: 13 · 2025: 22 · 2024: 4
FWCI
4.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Healthcare Materials (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (ECCS‐2025462)
  • National Science Foundation Graduate Research Fellowship Program (1937971)
  • National Institutes of Health (R01MH126195)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Keywords
3D bioprinting, brain organoids, cortical organoids, human brain development, induced pluripotent stem cells, endothelial cell migration, scaffold stiffness, neuroectodermal differentiation, disease modeling
MeSH terms
Brain, Cell Differentiation, Humans, Organoids, Tissue Engineering, Endothelial Cells, Tissue Scaffolds, Induced Pluripotent Stem Cells, Bioprinting, Printing, Three-Dimensional

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