DOI QR코드

DOI QR Code

Past, Present, and Future of Brain Organoid Technology

  • Koo, Bonsang (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Choi, Baekgyu (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Park, Hoewon (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST)) ;
  • Yoon, Ki-Jun (Department of Biological Sciences, Korea Advanced Institute of Science and Technology (KAIST))
  • 투고 : 2019.07.21
  • 심사 : 2019.09.23
  • 발행 : 2019.09.30

초록

Brain organoids are an exciting new technology with the potential to significantly change our understanding of the development and disorders of the human brain. With step-by-step differentiation protocols, three-dimensional neural tissues are self-organized from pluripotent stem cells, and recapitulate the major millstones of human brain development in vitro. Recent studies have shown that brain organoids can mimic the spatiotemporal dynamicity of neurogenesis, the formation of regional neural circuitry, and the integration of glial cells into a neural network. This suggests that brain organoids could serve as a representative model system to study the human brain. In this review, we will overview the development of brain organoid technology, its current progress and applications, and future prospects of this technology.

키워드

참고문헌

  1. Bian, S., Repic, M., Guo, Z., Kavirayani, A., Burkard, T., Bagley, J.A., Krauditsch, C., and Knoblich, J.A. (2018). Genetically engineered cerebral organoids model brain tumor formation. Nat. Methods 15, 631-639. https://doi.org/10.1038/s41592-018-0070-7
  2. Birey, F., Andersen, J., Makinson, C.D., Islam, S., Wei, W., Huber, N., Fan, H.C., Metzler, K.R.C., Panagiotakos, G., Thom, N., et al. (2017). Assembly of functionally integrated human forebrain spheroids. Nature 545, 54-59. https://doi.org/10.1038/nature22330
  3. Buchanan, M. (2018). Organoids of intelligence. Nat. Phys. 14, 634. https://doi.org/10.1038/s41567-018-0200-2
  4. Calvet, G., Aguiar, R.S., Melo, A.S.O., Sampaio, S.A., de Filippis, I., Fabri, A., Araujo, E.S.M., de Sequeira, P.C., de Mendonça, M.C.L., de Oliveira, L., et al. (2016). Detection and sequencing of Zika virus from amniotic fluid of fetuses with microcephaly in Brazil: a case study. Lancet Infect. Dis. 16, 653-660. https://doi.org/10.1016/S1473-3099(16)00095-5
  5. Camp, J.G., Badsha, F., Florio, M., Kanton, S., Gerber, T., Wilsch-Brauninger, M., Lewitus, E., Sykes, A., Hevers, W., Lancaster, M., et al. (2015). Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc. Natl. Acad. Sci. U. S. A. 112, 15672-15677. https://doi.org/10.1073/pnas.1520760112
  6. Charras, G. and Yap, A.S. (2018). Tensile forces and mechanotransduction at cell-cell junctions. Curr. Biol. 28, R445-R457. https://doi.org/10.1016/j.cub.2018.02.003
  7. Choi, Y.H. and Kim, J.K. (2019). Dissecting cellular heterogeneity using single-cell RNA sequencing. Mol. Cells 42, 189-199. https://doi.org/10.14348/MOLCELLS.2019.2446
  8. Cugola, F.R., Fernandes, I.R., Russo, F.B., Freitas, B.C., Dias, J.L.M., Guimarães, K.P., Benazzato, C., Almeida, N., Pignatari, G.C., Romero, S., et al. (2016). The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534, 267-271. https://doi.org/10.1038/nature18296
  9. Czerniecki, S.M., Cruz, N.M., Harder, J.L., Menon, R., Annis, J., Otto, E.A., Gulieva, R.E., Islas, L.V., Kim, Y.K., Tran, L.M., et al. (2018). Highthroughput screening enhances kidney organoid differentiation from human pluripotent stem cells and enables automated multidimensional phenotyping. Cell Stem Cell 22, 929-940.e4. https://doi.org/10.1016/j.stem.2018.04.022
  10. Dang, J., Tiwari, S.K., Lichinchi, G., Qin, Y., Patil, V.S., Eroshkin, A.M., and Rana, T.M. (2016). Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell 19, 258-265. https://doi.org/10.1016/j.stem.2016.04.014
  11. Dawson, T.M., Ko, H.S., and Dawson, V.L. (2010). Genetic animal models of Parkinson's disease. Neuron 66, 646-661. https://doi.org/10.1016/j.neuron.2010.04.034
  12. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T., and Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56. https://doi.org/10.1038/nature09941
  13. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., and Sasai, Y. (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532. https://doi.org/10.1016/j.stem.2008.09.002
  14. Gabriel, E., Ramani, A., Karow, U., Gottardo, M., Natarajan, K., Gooi, L.M., Goranci-Buzhala, G., Krut, O., Peters, F., Nikolic, M., et al. (2017). Recent Zika virus isolates induce premature differentiation of neural progenitors in human brain organoids. Cell Stem Cell 20, 397-406.e5. https://doi.org/10.1016/j.stem.2016.12.005
  15. Garcez, P.P., Loiola, E.C., Madeiro da Costa, R., Higa, L.M., Trindade, P., Delvecchio, R., Nascimento, J.M., Brindeiro, R., Tanuri, A., and Rehen, S.K. (2016). Zika virus impairs growth in human neurospheres and brain organoids. Science 352, 816-818. https://doi.org/10.1126/science.aaf6116
  16. Gaspard, N., Bouschet, T., Hourez, R., Dimidschstein, J., Naeije, G., Van den Ameele, J., Espuny-Camacho, I., Herpoel, A., Passante, L., and Schiffmann, S.N. (2008). An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455, 351-357. https://doi.org/10.1038/nature07287
  17. Grebenyuk, S. and Ranga, A. (2019). Engineering organoid vascularization. Front. Bioeng. Biotechnol. 7, 39. https://doi.org/10.3389/fbioe.2019.00039
  18. Heymann, D.L., Hodgson, A., Sall, A.A., Freedman, D.O., Staples, J.E., Althabe, F., Baruah, K., Mahmud, G., Kandun, N., Vasconcelos, P.F., et al. (2016). Zika virus and microcephaly: why is this situation a PHEIC? Lancet 387, 719-721. https://doi.org/10.1016/S0140-6736(16)00320-2
  19. Hockemeyer, D. and Jaenisch, R. (2016). Induced pluripotent stem cells meet genome editing. Cell Stem Cell 18, 573-586. https://doi.org/10.1016/j.stem.2016.04.013
  20. Homem, C.C.F., Repic, M., and Knoblich, J.A. (2015). Proliferation control in neural stem and progenitor cells. Nat. Rev. Neurosci. 16, 647-659. https://doi.org/10.1038/nrn4021
  21. Hubert, C.G., Rivera, M., Spangler, L.C., Wu, Q., Mack, S.C., Prager, B.C., Couce, M., McLendon, R.E., Sloan, A.E., and Rich, J.N. (2016). A threedimensional organoid culture system derived from human glioblastomas recapitulates the hypoxic gradients and cancer stem cell heterogeneity of tumors found in vivo. Cancer Res. 76, 2465-2477. https://doi.org/10.1158/0008-5472.CAN-15-2402
  22. Janssens, S., Schotsaert, M., Karnik, R., Balasubramaniam, V., Dejosez, M., Meissner, A., García-Sastre, A., and Zwaka, T.P. (2018). Zika virus alters DNA methylation of neural genes in an organoid model of the developing human brain. mSystems 3, e00219-e00217.
  23. Jo, J., Xiao, Y., Sun, A.X., Cukuroglu, E., Tran, H.D., Göke, J., Tan, Z.Y., Saw, T.Y., Tan, C.P., Lokman, H., et al. (2016). Midbrain-like organoids from human pluripotent stem cells contain functional dopaminergic and neuromelanin-producing neurons. Cell Stem Cell 19, 248-257. https://doi.org/10.1016/j.stem.2016.07.005
  24. Karzbrun, E., Kshirsagar, A., Cohen, S.R., Hanna, J.H., and Reiner, O. (2018). Human brain organoids on a chip reveal the physics of folding. Nat. Phys. 14, 515-522. https://doi.org/10.1038/s41567-018-0046-7
  25. Karzbrun, E., Reiner, O., Karzbrun, E., and Reiner, O. (2019). Brain organoids-a bottom-up approach for studying human neurodevelopment. Bioengineering (Basel) 6, E9. https://doi.org/10.3390/bioengineering6010009
  26. Kim, H., Park, H.J., Choi, H., Chang, Y., Park, H., Shin, J., Kim, J., Lengner, C.J., Lee, Y.K., and Kim, J. (2019a). Modeling G2019S-LRRK2 sporadic Parkinson's disease in 3D midbrain organoids. Stem Cell Reports 12, 518-531. https://doi.org/10.1016/j.stemcr.2019.01.020
  27. Kim, J., Koo, B.K., and Yoon, K.J. (2019b). Modeling host-virus interactions in viral infectious diseases using stem-cell-derived systems and CRISPR/Cas9 technology. Viruses 11, E124. https://doi.org/10.3390/v11020124
  28. Kopper, O., de Witte, C.J., Lohmussaar, K., Valle-Inclan, J.E., Hami, N., Kester, L., Balgobind, A.V., Korving, J., Proost, N., Begthel, H., et al. (2019). An organoid platform for ovarian cancer captures intra- and interpatient heterogeneity. Nat. Med. 25, 838-849. https://doi.org/10.1038/s41591-019-0422-6
  29. Kriegstein, A.R. and Noctor, S.C. (2004). Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392-399. https://doi.org/10.1016/j.tins.2004.05.001
  30. Lancaster, M.A. and Knoblich, J.A. (2014). Organogenesis in a dish: modeling development and disease using organoid technologies. Science 345, 1247125. https://doi.org/10.1126/science.1247125
  31. Lancaster, M.A., Renner, M., Martin, C.A., Wenzel, D., Bicknell, L.S., Hurles, M.E., Homfray, T., Penninger, J.M., Jackson, A.P., and Knoblich, J.A. (2013). Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379. https://doi.org/10.1038/nature12517
  32. Levitt, P. and Veenstra-VanderWeele, J. (2015). Neurodevelopment and the origins of brain disorders. Neuropsychopharmacology 40, 1-3. https://doi.org/10.1038/npp.2014.237
  33. Li, Y., Muffat, J., Omer, A., Bosch, I., Lancaster, M.A., Sur, M., Gehrke, L., Knoblich, J.A., and Jaenisch, R. (2017). Induction of expansion and folding in human cerebral organoids. Cell Stem Cell 20, 385-396.e3. https://doi.org/10.1016/j.stem.2016.11.017
  34. Lin, Y.T., Seo, J., Gao, F., Feldman, H.M., Wen, H.L., Penney, J., Cam, H.P., Gjoneska, E., Raja, W.K., Cheng, J., et al. (2018). APOE4 causes widespread molecular and cellular alterations associated with Alzheimer's disease phenotypes in human iPSC-derived brain cell types. Neuron 98, 1141-1154.e7. https://doi.org/10.1016/j.neuron.2018.05.008
  35. Linkous, A., Balamatsias, D., Snuderl, M., Pisapia, D., Liston, C., and Correspondence, H.A.F. (2019). Modeling patient-derived glioblastoma with cerebral organoids. Cell Rep. 26, 3203-3211.e5. https://doi.org/10.1016/j.celrep.2019.02.063
  36. Lui, J.H., Hansen, D.V., and Kriegstein, A.R. (2011). Development and evolution of the human neocortex. Cell 146, 18-36. https://doi.org/10.1016/j.cell.2011.06.030
  37. Madhavan, M., Nevin, Z.S., Shick, H.E., Garrison, E., Clarkson-Paredes, C., Karl, M., Clayton, B.L.L., Factor, D.C., Allan, K.C., and Barbar, L. (2018). Induction of myelinating oligodendrocytes in human cortical spheroids. Nat. Methods 15, 700-706. https://doi.org/10.1038/s41592-018-0081-4
  38. Mansour, A.A., Gonçalves, J.T., Bloyd, C.W., Li, H., Fernandes, S., Quang, D., Johnston, S., Parylak, S.L., Jin, X., and Gage, F.H. (2018). An in vivo model of functional and vascularized human brain organoids. Nat. Biotechnol. 36, 432-441. https://doi.org/10.1038/nbt.4127
  39. Mariani, J., Coppola, G., Zhang, P., Abyzov, A., Provini, L., Tomasini, L., Amenduni, M., Szekely, A., Palejev, D., Wilson, M., et al. (2015). FOXG1-dependent dysregulation of GABA/Glutamate neuron differentiation in autism spectrum disorders. Cell 162, 375-390. https://doi.org/10.1016/j.cell.2015.06.034
  40. Martin, G.R. (1981). Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. U. S. A. 78, 7634-7638. https://doi.org/10.1073/pnas.78.12.7634
  41. Marton, R.M., Miura, Y., Sloan, S.A., Li, Q., Revah, O., Levy, R.J., Huguenard, J.R., and Pasca, S.P. (2019). Differentiation and maturation of oligodendrocytes in human three-dimensional neural cultures. Nat. Neurosci. 22, 484-491. https://doi.org/10.1038/s41593-018-0316-9
  42. Mitchell, K.J. (2011). The genetics of neurodevelopmental disease. Curr. Opin. Neurobiol. 21, 197-203. https://doi.org/10.1016/j.conb.2010.08.009
  43. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljsak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodusek, V., et al. (2016). Zika virus associated with microcephaly. N. Engl. J. Med. 374, 951-958. https://doi.org/10.1056/NEJMoa1600651
  44. Muguruma, K., Nishiyama, A., Kawakami, H., Hashimoto, K., and Sasai, Y. (2015). Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep. 10, 537-550. https://doi.org/10.1016/j.celrep.2014.12.051
  45. Murphy, S.V. and Atala, A. (2014). 3D bioprinting of tissues and organs. Nat. Biotechnol. 32, 773-785. https://doi.org/10.1038/nbt.2958
  46. Ogawa, J., Pao, G.M., Shokhirev, M.N., and Verma, I.M. (2018). Glioblastoma model using human cerebral organoids. Cell Rep. 23, 1220-1229. https://doi.org/10.1016/j.celrep.2018.03.105
  47. Oh, Y. and Jang, J. (2019). Directed differentiation of pluripotent stem cells by transcription factors. Mol. Cells 42, 200-209. https://doi.org/10.14348/molcells.2019.2439
  48. Ormel, P.R., Vieira de Sa, R., van Bodegraven, E.J., Karst, H., Harschnitz, O., Sneeboer, M.A.M., Johansen, L.E., van Dijk, R.E., Scheefhals, N., Berdenis van Berlekom, A., et al. (2018). Microglia innately develop within cerebral organoids. Nat. Commun. 9, 4167. https://doi.org/10.1038/s41467-018-06684-2
  49. Park, S.E., Georgescu, A., and Huh, D. (2019). Organoids-on-a-chip. Science 364, 960-965. https://doi.org/10.1126/science.aaw7894
  50. Pasca, A.M., Park, J.Y., Shin, H.W., Qi, Q., Revah, O., Krasnoff, R., O'Hara, R., Willsey, A.J., Palmer, T.D., and Pasca, S.P. (2019). Human 3D cellular model of hypoxic brain injury of prematurity. Nat. Med. 25, 784-791. https://doi.org/10.1038/s41591-019-0436-0
  51. Pasca, A.M., Sloan, S.A., Clarke, L.E., Tian, Y., Makinson, C.D., Huber, N., Kim, C.H., Park, J.Y., O'Rourke, N.A., Nguyen, K.D., et al. (2015). Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat. Methods 12, 671-678. https://doi.org/10.1038/nmeth.3415
  52. Plummer, S., Wallace, S., Ball, G., Lloyd, R., Schiapparelli, P., Quinones-Hinojosa, A., Hartung, T., and Pamies, D. (2019). A human iPSC-derived 3D platform using primary brain cancer cells to study drug development and personalized medicine. Sci. Rep. 9, 1407. https://doi.org/10.1038/s41598-018-38130-0
  53. Qian, X., Jacob, F., Song, M.M., Nguyen, H.N., Song, H., and Ming, G.l. (2018). Generation of human brain region-specific organoids using a miniaturized spinning bioreactor. Nat. Protoc. 13, 565-580. https://doi.org/10.1038/nprot.2017.152
  54. Qian, X., Nguyen, H.N., Song, M.M., Hadiono, C., Ogden, S.C., Hammack, C., Yao, B., Hamersky, G.R., Jacob, F., Zhong, C., et al. (2016). Brain-regionspecific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238-1254. https://doi.org/10.1016/j.cell.2016.04.032
  55. Qian, X., Song, H., and Ming, G.L. (2019). Brain organoids: advances, applications and challenges. Development 146, dev166074.
  56. Quadrato, G., Nguyen, T., Macosko, E.Z., Sherwood, J.L., Min Yang, S., Berger, D.R., Maria, N., Scholvin, J., Goldman, M., Kinney, J.P., et al. (2017). Cell diversity and network dynamics in photosensitive human brain organoids. Nature 545, 48-53. https://doi.org/10.1038/nature22047
  57. Raja, W.K., Mungenast, A.E., Lin, Y.T., Ko, T., Abdurrob, F., Seo, J., and Tsai, L.H. (2016). Self-organizing 3D human neural tissue derived from induced pluripotent stem cells recapitulate Alzheimer's disease phenotypes. PLoS One 11, 1-18.
  58. Raslan, A.A. and Kee, Y. (2013). Tackling neurodegenerative diseases: animal models of Alzheimer's disease and Parkinson's disease. Genes Genom. 35, 425-440. https://doi.org/10.1007/s13258-013-0116-2
  59. Sachs, N., de Ligt, J., Kopper, O., Gogola, E., Bounova, G., Weeber, F., Balgobind, A.V., Wind, K., Gracanin, A., Begthel, H., et al. (2018). A living biobank of breast cancer organoids captures disease heterogeneity. Cell 172, 373-386.e10. https://doi.org/10.1016/j.cell.2017.11.010
  60. Sakaguchi, H., Kadoshima, T., Soen, M., Narii, N., Ishida, Y., Ohgushi, M., Takahashi, J., Eiraku, M., and Sasai, Y. (2015). Generation of functional hippocampal neurons from self-organizing human embryonic stem cellderived dorsomedial telencephalic tissue. Nat. Commun. 6, 8896. https://doi.org/10.1038/ncomms9896
  61. Sato, T., Vries, R.G., Snippert, H.J., van de Wetering, M., Barker, N., Stange, D.E., van Es, J.H., Abo, A., Kujala, P., Peters, P.J., et al. (2009). Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265. https://doi.org/10.1038/nature07935
  62. Schafer, S.T., Paquola, A.C.M., Stern, S., Gosselin, D., Ku, M., Pena, M., Kuret, T.J.M., Liyanage, M., Mansour, A.A., Jaeger, B.N., et al. (2019). Pathological priming causes developmental gene network heterochronicity in autistic subject-derived neurons. Nat. Neurosci. 22, 243-255. https://doi.org/10.1038/s41593-018-0295-x
  63. Shi, Y., Kirwan, P., Smith, J., Robinson, H.P.C., and Livesey, F.J. (2012). Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat. Neurosci. 15, 477-486, S1. https://doi.org/10.1038/nn.3041
  64. Sloan, S.A., Darmanis, S., Huber, N., Khan, T.A., Birey, F., Caneda, C., Reimer, R., Quake, S.R., Barres, B.A., and Paşca, S.P. (2017). Human astrocyte maturation captured in 3D cerebral cortical spheroids derived from pluripotent stem cells. Neuron 95, 779-790.e6. https://doi.org/10.1016/j.neuron.2017.07.035
  65. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872. https://doi.org/10.1016/j.cell.2007.11.019
  66. Takahashi, K. and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676. https://doi.org/10.1016/j.cell.2006.07.024
  67. Tao, Y. and Zhang, S.C. (2016). Neural subtype specification from human pluripotent stem cells. Cell Stem Cell 19, 573-586. https://doi.org/10.1016/j.stem.2016.10.015
  68. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., Waknitz, M.A., Swiergiel, J.J., Marshall, V.S., and Jones, J.M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147. https://doi.org/10.1126/science.282.5391.1145
  69. Trujillo, C.A., Gao, R., Negraes, P.D., Gu, J., Buchanan, J., Preissl, S., Wang, A., Wu, W., Haddad, G.G., Chaim, I.A., et al. (2019). Complex oscillatory waves emerging from cortical organoids model early human brain network development. Cell Stem Cell 25, 1-12. https://doi.org/10.1016/j.stem.2019.06.005
  70. Tung, T.C. and Kü, S.H. (1944). Experimental studies on the development of the pronephric duct in anuran embryos. J. Anat. 78, 52-57.
  71. Valiente, M. and Marin, O. (2010). Neuronal migration mechanisms in development and disease. Curr. Opin. Neurobiol. 20, 68-78. https://doi.org/10.1016/j.conb.2009.12.003
  72. van de Wetering, M., Francies, H.E., Francis, J.M., Bounova, G., Iorio, F., Pronk, A., van Houdt, W., van Gorp, J., Taylor-Weiner, A., Kester, L., et al. (2015). Prospective derivation of a living organoid biobank of colorectal cancer patients. Cell 161, 933-945. https://doi.org/10.1016/j.cell.2015.03.053
  73. Velasco, S., Kedaigle, A.J., Simmons, S.K., Nash, A., Rocha, M., Quadrato, G., Paulsen, B., Nguyen, L., Adiconis, X., Regev, A., et al. (2019). Individual brain organoids reproducibly form cell diversity of the human cerebral cortex. Nature 570, 523-527. https://doi.org/10.1038/s41586-019-1289-x
  74. Vijayavenkataraman, S., Yan, W.C., Lu, W.F., Wang, C.H., and Fuh, J.Y.H. (2018). 3D bioprinting of tissues and organs for regenerative medicine. Adv. Drug Deliv. Rev. 132, 296-332. https://doi.org/10.1016/j.addr.2018.07.004
  75. Wang, P., Mokhtari, R., Pedrosa, E., Kirschenbaum, M., Bayrak, C., Zheng, D., and Lachman, H.M. (2017). CRISPR/Cas9-mediated heterozygous knockout of the autism gene CHD8 and characterization of its transcriptional networks in cerebral organoids derived from iPS cells. Mol. Autism 8, 11. https://doi.org/10.1186/s13229-017-0124-1
  76. Watanabe, M., Buth, J.E., Vishlaghi, N., de la Torre-Ubieta, L., Taxidis, J., Khakh, B.S., Coppola, G., Pearson, C.A., Yamauchi, K., Gong, D., et al. (2017). Self-organized cerebral organoids with human-specific features predict effective drugs to combat Zika virus infection. Cell Rep. 21, 517-532. https://doi.org/10.1016/j.celrep.2017.09.047
  77. Werner, S., Vu, H.T., and Rink, J.C. (2017). Self-organization in development, regeneration and organoids. Curr. Opin. Cell Biol. 44, 102-109. https://doi.org/10.1016/j.ceb.2016.09.002
  78. Wilson, H.V. (1907). On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5, 245-258. https://doi.org/10.1002/jez.1400050204
  79. Wimmer, R.A., Leopoldi, A., Aichinger, M., Wick, N., Hantusch, B., Novatchkova, M., Taubenschmid, J., Hammerle, M., Esk, C., Bagley, J.A., et al. (2019). Human blood vessel organoids as a model of diabetic vasculopathy. Nature 565, 505-510. https://doi.org/10.1038/s41586-018-0858-8
  80. Xia, Y., Sancho-Martinez, I., Nivet, E., Rodriguez Esteban, C., Campistol, J.M., and Izpisua Belmonte, J.C. (2014). The generation of kidney organoids by differentiation of human pluripotent cells to ureteric bud progenitor-like cells. Nat. Protoc. 9, 2693-2704. https://doi.org/10.1038/nprot.2014.182
  81. Xu, M., Lee, E.M., Wen, Z., Cheng, Y., Huang, W.K., Qian, X., Tcw, J., Kouznetsova, J., Ogden, S.C., Hammack, C., et al. (2016). Identification of small-molecule inhibitors of Zika virus infection and induced neural cell death via a drug repurposing screen. Nat. Med. 22, 1101-1107. https://doi.org/10.1038/nm.4184
  82. Yamanaka, S. (2012). Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 10, 678-684. https://doi.org/10.1016/j.stem.2012.05.005
  83. Yan, H.H.N., Siu, H.C., Law, S., Ho, S.L., Yue, S.S.K., Tsui, W.Y., Chan, D., Chan, A.S., Ma, S., Lam, K.O., et al. (2018). A comprehensive human gastric cancer organoid biobank captures tumor subtype heterogeneity and enables therapeutic screening. Cell Stem Cell 23, 882-897.e11. https://doi.org/10.1016/j.stem.2018.09.016
  84. Yin, X., Mead, B.E., Safaee, H., Langer, R., Karp, J.M., and Levy, O. (2016). Engineering stem cell organoids. Cell Stem Cell 18, 25-38. https://doi.org/10.1016/j.stem.2015.12.005
  85. Yoon, K.J., Nguyen, H.N., Ursini, G., Zhang, F., Kim, N.S., Wen, Z., Makri, G., Nauen, D., Shin, J.H., Park, Y., et al. (2014). Modeling a genetic risk for schizophrenia in iPSCs and mice reveals neural stem cell deficits associated with adherens junctions and polarity. Cell Stem Cell 15, 79-91. https://doi.org/10.1016/j.stem.2014.05.003
  86. Yoon, K.J., Ringeling, F.R., Vissers, C., Jacob, F., Pokrass, M., Jimenez-Cyrus, D., Su, Y., Kim, N.S., Zhu, Y., Zheng, L., et al. (2017a). Temporal control of mammalian cortical neurogenesis by m(6)A methylation. Cell 171, 877-889.e17. https://doi.org/10.1016/j.cell.2017.09.003
  87. Yoon, K.J., Song, G., Qian, X., Pan, J., Xu, D., Rho, H.S., Kim, N.S., Habela, C., Zheng, L., Jacob, F., et al. (2017b). Zika-virus-encoded NS2A disrupts mammalian cortical neurogenesis by degrading adherens junction proteins. Cell Stem Cell 21, 349-358.e6. https://doi.org/10.1016/j.stem.2017.07.014
  88. Yoon, S.J., Elahi, L.S., Pasca, A.M., Marton, R.M., Gordon, A., Revah, O., Miura, Y., Walczak, E.M., Holdgate, G.M., Fan, H.C., et al. (2019). Reliability of human cortical organoid generation. Nat. Methods 16, 75-78. https://doi.org/10.1038/s41592-018-0255-0
  89. Yu, J., Vodyanik, M.A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J.L., Tian, S., Nie, J., Jonsdottir, G.A., Ruotti, V., Stewart, R., et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920. https://doi.org/10.1126/science.1151526
  90. Yuan, L., Huang, X.Y., Liu, Z.Y., Zhang, F., Zhu, X.L., Yu, J.Y., Ji, X., Xu, Y.P., Li, G., Li, C., et al. (2017). A single mutation in the prM protein of Zika virus contributes to fetal microcephaly. Science 358, 933-936. https://doi.org/10.1126/science.aam7120
  91. Zhang, S.C., Wernig, M., Duncan, I.D., Brustle, O., and Thomson, J.A. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133. https://doi.org/10.1038/nbt1201-1129
  92. Zhong, X., Gutierrez, C., Xue, T., Hampton, C., Vergara, M.N., Cao, L.H., Peters, A., Park, T.S., Zambidis, E.T., Meyer, J.S., et al. (2014). Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs. Nat. Commun. 5, 4047. https://doi.org/10.1038/ncomms5047
  93. Zhou, T., Tan, L., Cederquist, G.Y., Fan, Y., Hartley, B.J., Mukherjee, S., Tomishima, M., Brennand, K.J., Zhang, Q., Schwartz, R.E., et al. (2017). Highcontent screening in hPSC-neural progenitors identifies drug candidates that inhibit Zika virus infection in fetal-like organoids and adult brain. Cell Stem Cell 21, 274-283.e5. https://doi.org/10.1016/j.stem.2017.06.017
  94. Zwilling, E. (1960). Some aspects of differentiation: disaggregation and reaggregation of early chick embryos. Natl. Cancer Inst. Monogr. 2, 19-39.

피인용 문헌

  1. Brain Organoids as Model Systems for Genetic Neurodevelopmental Disorders vol.8, 2019, https://doi.org/10.3389/fcell.2020.590119
  2. Simplified Brain Organoids for Rapid and Robust Modeling of Brain Disease vol.8, 2019, https://doi.org/10.3389/fcell.2020.594090
  3. Unprecedented Potential for Neural Drug Discovery Based on Self-Organizing hiPSC Platforms vol.25, pp.5, 2019, https://doi.org/10.3390/molecules25051150
  4. Cerebral Organoids: A Model of Brain Development vol.51, pp.4, 2019, https://doi.org/10.1134/s1062360420040074
  5. Genetic and environmental factors of schizophrenia and autism spectrum disorder: insights from twin studies vol.127, pp.11, 2020, https://doi.org/10.1007/s00702-020-02188-w
  6. Recent Advances in Three-Dimensional Stem Cell Culture Systems and Applications vol.2021, 2019, https://doi.org/10.1155/2021/9477332
  7. Electrophysiological Analysis of Brain Organoids: Current Approaches and Advancements vol.14, 2021, https://doi.org/10.3389/fnins.2020.622137
  8. Heterocellular spheroids of the neurovascular blood-brain barrier as a platform for personalized nanoneuromedicine vol.24, pp.3, 2021, https://doi.org/10.1016/j.isci.2021.102183
  9. Role of SHH in Patterning Human Pluripotent Cells towards Ventral Forebrain Fates vol.10, pp.4, 2021, https://doi.org/10.3390/cells10040914
  10. Development of 3D Cerebral Aggregates in the Brain Ventricles of Adult Mice vol.52, pp.3, 2021, https://doi.org/10.1134/s1062360421030061
  11. Experimental Technique to Generate Complex Pressure Cycles in TBI-related In-vitro or Ex-vivo Samples vol.45, pp.6, 2019, https://doi.org/10.1007/s40799-021-00453-5
  12. Development of a quantitative prediction algorithm for target organ-specific similarity of human pluripotent stem cell-derived organoids and cells vol.12, pp.1, 2021, https://doi.org/10.1038/s41467-021-24746-w
  13. Neuron and astrocyte aggregation and sorting in three-dimensional neuronal constructs vol.4, pp.1, 2019, https://doi.org/10.1038/s42003-021-02104-2
  14. Increased connectivity of hiPSC-derived neural networks in multiphase granular hydrogel scaffolds vol.9, 2019, https://doi.org/10.1016/j.bioactmat.2021.07.008