Research progress on vascularization of organoids_Journal of Biomedical Engineering

Authors：

SHEN Junyi , OUYANG Zhi , ZHONG Jian , LONG Yicen , SUN Yujia ,  ZENG Ye

Institute of Biomedical Engineering, West China School of Basic Medical Sciences and Forensic Medicine, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

ZENG Ye, Email: ye@scu.edu.cn

Keywords：

Organoids; Stem cells; Blood vessels; Coculture; Endothelial cells

DOI：

10.7507/1001-5515.202211011

Video：

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Abstract Full text Figures/Tables Video References Cited by

Organoids are three-dimensional structures formed by self-organizing growth of cells in vitro, which own many structures and functions similar with those of corresponding in vivo organs. Although the organoid culture technologies are rapidly developed and the original cells are abundant, the organoid cultured by current technologies are rather different with the real organs, which limits their application. The major challenges of organoid cultures are the immature tissue structure and restricted growth, both of which are caused by poor functional vasculature. Therefore, how to develop the vascularization of organoids has become an urgent problem. We presently reviewed the progresses on the original cells of organoids and the current methods to develop organoids vascularization, which provide clues to solve the above-mentioned problems.

Citation： SHEN Junyi, OUYANG Zhi, ZHONG Jian, LONG Yicen, SUN Yujia, ZENG Ye. Research progress on vascularization of organoids. Journal of Biomedical Engineering, 2023, 40(4): 625-631. doi: 10.7507/1001-5515.202211011 Copy

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2.	马亮. 血管化人脑类器官的构建及其功能研究. 哈尔滨: 哈尔滨工业大学, 2020.
3.	Duval K, Grover H, Han L H, et al. Modeling physiological events in 2D vs. 3D cell culture. Physiology (Bethesda), 2017, 32(4): 266-277.
4.	Farcy S, Albert A, Gressens P, et al. Cortical organoids to model microcephaly. Cells, 2022, 11(14): 2135.
5.	Cheaito K, Bahmad H F, Hadadeh O, et al. Establishment and characterization of prostate organoids from treatment-naïve patients with prostate cancer. Oncol Lett, 2022, 23(1): 6.
6.	Blutt S E, Estes M K. Organoid models for infectious disease. Annu Rev Med, 2022, 73: 167-182.
7.	Wimmer R A, Leopoldi A, Aichinger M, et al. Human blood vessel organoids as a model of diabetic vasculopathy. Nature, 2019, 565(7740): 505-510.
8.	Vargas-Valderrama A, Messina A, Mitjavila-Garcia M T, et al. The endothelium, a key actor in organ development and hPSC-derived organoid vascularization. J Biomed Sci, 2020, 27(1): 67.
9.	Rambani K, Vukasinovic J, Glezer A, et al. Culturing thick brain slices: an interstitial 3D microperfusion system for enhanced viability. J Neurosci Methods, 2009, 180(2): 243-254.
10.	Muschler G F, Nakamoto C, Griffith L G. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am, 2004, 86(7): 1541-1558.
11.	Mansour A A, Gonçalves J T, Bloyd C W, et al. An in vivo model of functional and vascularized human brain organoids. Nat Biotechnol, 2018, 36(5): 432-441.
12.	Cakir B, Xiang Y, Tanaka Y, et al. Engineering of human brain organoids with a functional vascular-like system. Nat Methods, 2019, 16(11): 1169-1175.
13.	Zhu X, Zhang B, He Y, et al. Liver organoids: Formation strategies and biomedical applications. Tissue Eng Regen Med, 2021, 18(4): 573-585.
14.	Rossi G, Manfrin A, Lutolf M P. Progress and potential in organoid research. Nat Rev Genet, 2018, 19(11): 671-687.
15.	McCauley H A, Wells J M. Pluripotent stem cell-derived organoids: using principles of developmental biology to grow human tissues in a dish. Development, 2017, 144(6): 958-962.
16.	Pham M T, Pollock K M, Rose M D, et al. Generation of human vascularized brain organoids. Neuroreport, 2018, 29(7): 588-593.
17.	Morizane R, Bonventre J V. Generation of nephron progenitor cells and kidney organoids from human pluripotent stem cells. Nat Protoc, 2017, 12(1): 195-207.
18.	Lee S G, Kim Y J, Son M Y, et al. Generation of human iPSCs derived heart organoids structurally and functionally similar to heart. Biomaterials, 2022, 290: 121860.
19.	McCracken K W, Catá E M, Crawford C M, et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature, 2014, 516(7531): 400-404.
20.	Lee J, Rabbani C C, Gao H, et al. Hair-bearing human skin generated entirely from pluripotent stem cells. Nature, 2020, 582(7812): 399-404.
21.	Eiraku M, Takata N, Ishibashi H, et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature, 2011, 472(7341): 51-56.
22.	Eiraku M, Watanabe K, Matsuo-Takasaki M, et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell, 2008, 3(5): 519-532.
23.	McCracken K W, Howell J C, Wells J M, et al. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat Protoc, 2011, 6(12): 1920-1928.
24.	Takasato M, Er P X, Becroft M, et al. Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat Cell Biol, 2014, 16(1): 118-126.
25.	Yousef Yengej F A, Jansen J, Rookmaaker M B, et al. Kidney organoids and tubuloids. Cells, 2020, 9(6): 1326.
26.	Yan K S, Janda C Y, Chang J, et al. Non-equivalence of Wnt and R-spondin ligands during Lgr5(+) intestinal stem-cell self-renewal. Nature, 2017, 545(7653): 238-242.
27.	Lu A Q, Popova E Y, Barnstable C J. Activin signals through SMAD2/3 to increase photoreceptor precursor yield during embryonic stem cell differentiation. Stem Cell Reports, 2017, 9(3): 838-852.
28.	Wu H, Uchimura K, Donnelly E L, et al. Comparative analysis and refinement of human PSC-derived kidney organoid differentiation with single-cell transcriptomics. Cell Stem Cell, 2018, 23(6): 869-881.
29.	Tuveson D, Clevers H. Cancer modeling meets human organoid technology. Science, 2019, 364(6444): 952-955.
30.	Clevers H. Modeling development and disease with organoids. Cell, 2016, 165(7): 1586-1597.
31.	Sato T, Vries R G, Snippert H J, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 2009, 459(7244): 262-265.
32.	Mohammadi S, Morell-Perez C, Wright C W, et al. Assessing donor-to-donor variability in human intestinal organoid cultures. Stem Cell Reports, 2021, 16(9): 2364-2378.
33.	Calandrini C, Drost J. Generation of human kidney tubuloids from tissue and urine. J Vis Exp, 2021, (170). DOI: 10.3791/62404-v.
34.	Al-Ghadban S, Pursell I A, Diaz Z T, et al. 3D spheroids derived from human lipedema ASCs demonstrated similar adipogenic differentiation potential and ECM remodeling to non-lipedema ASCs in vitro. Int J Mol Sci, 2020, 21(21): 8350.
35.	Huch M, Dorrell C, Boj S F, et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature, 2013, 494(7436): 247-250.
36.	Furuya K, Zheng Y W, Sako D, et al. Enhanced hepatic differentiation in the subpopulation of human amniotic stem cells under 3D multicellular microenvironment. World J Stem Cells, 2019, 11(9): 705-721.
37.	Pleguezuelos-Manzano C, Puschhof J, van den Brink S, et al. Establishment and culture of human intestinal organoids derived from adult stem cells. Curr Protoc Immunol, 2020, 130(1): e106.
38.	Greggio C, De Franceschi F, Figueiredo-Larsen M, et al. Artificial three-dimensional niches deconstruct pancreas development in vitro. Development, 2013, 140(21): 4452-4462.
39.	Fordham R P, Yui S, Hannan N R, et al. Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell, 2013, 13(6): 734-744.
40.	Saito Y, Matsumoto N, Yamanaka S, et al. Beneficial impact of interspecies chimeric renal organoids against a xenogeneic immune response. Front Immunol, 2022, 13: 848433.
41.	Cambuli F, Foletto V, Alaimo A, et al. Intra-epithelial non-canonical Activin A signaling safeguards prostate progenitor quiescence. EMBO Rep, 2022, 23(5): e54049.
42.	Bhang S H, Lee S, Shin J Y, et al. Transplantation of cord blood mesenchymal stem cells as spheroids enhances vascularization. Tissue Eng Part A, 2012, 18(19-20): 2138-2147.
43.	Weiss S, Hennig T, Bock R, et al. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J Cell Physiol, 2010, 223(1): 84-93.
44.	Al-Nbaheen M, Vishnubalaji R, Ali D, et al. Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev Rep, 2013, 9(1): 32-43.
45.	Wang C, Yin S, Cen L, et al. Differentiation of adipose-derived stem cells into contractile smooth muscle cells induced by transforming growth factor-beta1 and bone morphogenetic protein-4. Tissue Eng Part A, 2010, 16(4): 1201-1213.
46.	He Y T, Zhu X L, Li S F, et al. Creating rat hepatocyte organoid as an in vitro model for drug testing. World J Stem Cells, 2020, 12(10): 1184-1195.
47.	Leeman K T, Pessina P, Lee J H, et al. Mesenchymal stem cells increase alveolar differentiation in lung progenitor organoid cultures. Sci Rep, 2019, 9(1): 6479.
48.	Strobel H A, Gerton T, Hoying J B. Vascularized adipocyte organoid m odel using isolated human microvessel fragments. Biofabrication, 2021, 13(3): 035022.
49.	周子墨, 柳达, 陈森相, 等. 3D细胞培养和类器官在骨髓源性间充质干细胞成骨分化中的研究进展. 中国骨质疏松杂志, 2022, 28(9): 1400-1404.
50.	Martini G, Belli V, Napolitano S, et al. Establishment of patient-derived tumor organoids to functionally inform treatment decisions in metastatic colorectal cancer. ESMO Open, 2023, 8(3): 101198.
51.	Dutta D, Heo I, Clevers H. Disease modeling in stem cell-derived 3D organoid systems. Trends Mol Med, 2017, 23(5): 393-410.
52.	Shembrey C, Smith J, Grandin M, et al. Longitudinal monitoring of intra-tumoural heterogeneity using optical barcoding of patient-derived colorectal tumour models. Cancers (Basel), 2022, 14(3): 581.
53.	Bhatia S, Kramer M, Russo S, et al. Patient-derived triple-negative breast cancer organoids provide robust model systems that recapitulate tumor intrinsic characteristics. Cancer Res, 2022, 82(7): 1174-1192.
54.	Hubert C G, Rivera M, Spangler L C, et al. A three-dimensional organoid culture system derived from human glioblastomas recapitulates the hypoxic gradients and cancer stem cell heterogeneity of tumors found in vivo. Cancer Res, 2016, 76(8): 2465-2477.
55.	Tindle C, Fuller M, Fonseca A, et al. Adult stem cell-derived complete lung orga noid models emulate lung disease in COVID-19. Elife, 2021, 10: e66417.
56.	Hallett J M, Ferreira-Gonzalez S, Man T Y, et al. Human biliary epithelial cells from discarded donor livers rescue bile duct structure and function in a mouse model of biliary disease. Cell Stem Cell, 2022, 29(3): 355-371.
57.	Vonk A C, Hasel-Kolossa S C, Lopez G A, et al. Lizard blastema organoid model recapitulates regenerated tail chondrogenesis. J Dev Biol, 2022, 10(1): 12.
58.	Asai A, Aihara E, Watson C, et al. Paracrine signals regulate human liver organoid maturation from induced pluripotent stem cells. Development, 2017, 144(6): 1056-1064.
59.	Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459): 481-484.
60.	Homan K A, Gupta N, Kroll K T, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods, 2019, 16(3): 255-262.
61.	Takahashi Y, Sekine K, Kin T, et al. Self-condensation culture enables vascularization of tissue fragments for efficient therapeutic transplantation. Cell Rep, 2018, 23(6): 1620-1629.
62.	Wimmer R A, Leopoldi A, Aichinger M, et al. Generation of blood vessel organoids from human pluripotent stem cells. Nat Protoc, 2019, 14(11): 3082-3100.
63.	Song J W, Munn L L. Fluid forces control endothelial sprouting. Proc Natl Acad Sci U S A, 2011, 108(37): 15342-15347.
64.	Ibrahim M, Richardson M K. Beyond organoids: In vitro vasculogenesis and angiogenesis using cells from mammals and zebrafish. Reprod Toxicol, 2017, 73: 292-311.
65.	Moya M L, Hsu Y-H, Lee A P, et al. In vitro perfused human capillary networks. Tissue Eng Part C: Methods, 2013, 19(9): 730-737.
66.	Zhang S, Wan Z, Kamm R D. Vascularized organoids on a chip: strategies for engineering organoids with functional vasculature. Lab Chip, 2021, 21(3): 473-488.
67.	Rajasekar S, Lin D S Y, Abdul L, et al. IFlowPlate-A customized 384-well plate for the culture of perfusable vascularized colon organoids. Adv Mater, 2020, 32(46): e2002974.
68.	Lee H N, Choi Y Y, Kim J W, et al. Effect of biochemical and biomechanical factors on vascularization of kidney organoid-on-a-chip. Nano Converg, 2021, 8(1): 35.
69.	Nashimoto Y, Okada R, Hanada S, et al. Vascularized cancer on a chip: The effect of perfusion on growth and drug delivery of tumor spheroid. Biomaterials, 2020, 229: 119547.

1. Lancaster M A, Knoblich J A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science, 2014, 345(6194): 1247125.
2. 马亮. 血管化人脑类器官的构建及其功能研究. 哈尔滨: 哈尔滨工业大学, 2020.
3. Duval K, Grover H, Han L H, et al. Modeling physiological events in 2D vs. 3D cell culture. Physiology (Bethesda), 2017, 32(4): 266-277.
4. Farcy S, Albert A, Gressens P, et al. Cortical organoids to model microcephaly. Cells, 2022, 11(14): 2135.
5. Cheaito K, Bahmad H F, Hadadeh O, et al. Establishment and characterization of prostate organoids from treatment-naïve patients with prostate cancer. Oncol Lett, 2022, 23(1): 6.
6. Blutt S E, Estes M K. Organoid models for infectious disease. Annu Rev Med, 2022, 73: 167-182.
7. Wimmer R A, Leopoldi A, Aichinger M, et al. Human blood vessel organoids as a model of diabetic vasculopathy. Nature, 2019, 565(7740): 505-510.
8. Vargas-Valderrama A, Messina A, Mitjavila-Garcia M T, et al. The endothelium, a key actor in organ development and hPSC-derived organoid vascularization. J Biomed Sci, 2020, 27(1): 67.
9. Rambani K, Vukasinovic J, Glezer A, et al. Culturing thick brain slices: an interstitial 3D microperfusion system for enhanced viability. J Neurosci Methods, 2009, 180(2): 243-254.
10. Muschler G F, Nakamoto C, Griffith L G. Engineering principles of clinical cell-based tissue engineering. J Bone Joint Surg Am, 2004, 86(7): 1541-1558.
11. Mansour A A, Gonçalves J T, Bloyd C W, et al. An in vivo model of functional and vascularized human brain organoids. Nat Biotechnol, 2018, 36(5): 432-441.
12. Cakir B, Xiang Y, Tanaka Y, et al. Engineering of human brain organoids with a functional vascular-like system. Nat Methods, 2019, 16(11): 1169-1175.
13. Zhu X, Zhang B, He Y, et al. Liver organoids: Formation strategies and biomedical applications. Tissue Eng Regen Med, 2021, 18(4): 573-585.
14. Rossi G, Manfrin A, Lutolf M P. Progress and potential in organoid research. Nat Rev Genet, 2018, 19(11): 671-687.
15. McCauley H A, Wells J M. Pluripotent stem cell-derived organoids: using principles of developmental biology to grow human tissues in a dish. Development, 2017, 144(6): 958-962.
16. Pham M T, Pollock K M, Rose M D, et al. Generation of human vascularized brain organoids. Neuroreport, 2018, 29(7): 588-593.
17. Morizane R, Bonventre J V. Generation of nephron progenitor cells and kidney organoids from human pluripotent stem cells. Nat Protoc, 2017, 12(1): 195-207.
18. Lee S G, Kim Y J, Son M Y, et al. Generation of human iPSCs derived heart organoids structurally and functionally similar to heart. Biomaterials, 2022, 290: 121860.
19. McCracken K W, Catá E M, Crawford C M, et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature, 2014, 516(7531): 400-404.
20. Lee J, Rabbani C C, Gao H, et al. Hair-bearing human skin generated entirely from pluripotent stem cells. Nature, 2020, 582(7812): 399-404.
21. Eiraku M, Takata N, Ishibashi H, et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature, 2011, 472(7341): 51-56.
22. Eiraku M, Watanabe K, Matsuo-Takasaki M, et al. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell, 2008, 3(5): 519-532.
23. McCracken K W, Howell J C, Wells J M, et al. Generating human intestinal tissue from pluripotent stem cells in vitro. Nat Protoc, 2011, 6(12): 1920-1928.
24. Takasato M, Er P X, Becroft M, et al. Directing human embryonic stem cell differentiation towards a renal lineage generates a self-organizing kidney. Nat Cell Biol, 2014, 16(1): 118-126.
25. Yousef Yengej F A, Jansen J, Rookmaaker M B, et al. Kidney organoids and tubuloids. Cells, 2020, 9(6): 1326.
26. Yan K S, Janda C Y, Chang J, et al. Non-equivalence of Wnt and R-spondin ligands during Lgr5(+) intestinal stem-cell self-renewal. Nature, 2017, 545(7653): 238-242.
27. Lu A Q, Popova E Y, Barnstable C J. Activin signals through SMAD2/3 to increase photoreceptor precursor yield during embryonic stem cell differentiation. Stem Cell Reports, 2017, 9(3): 838-852.
28. Wu H, Uchimura K, Donnelly E L, et al. Comparative analysis and refinement of human PSC-derived kidney organoid differentiation with single-cell transcriptomics. Cell Stem Cell, 2018, 23(6): 869-881.
29. Tuveson D, Clevers H. Cancer modeling meets human organoid technology. Science, 2019, 364(6444): 952-955.
30. Clevers H. Modeling development and disease with organoids. Cell, 2016, 165(7): 1586-1597.
31. Sato T, Vries R G, Snippert H J, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 2009, 459(7244): 262-265.
32. Mohammadi S, Morell-Perez C, Wright C W, et al. Assessing donor-to-donor variability in human intestinal organoid cultures. Stem Cell Reports, 2021, 16(9): 2364-2378.
33. Calandrini C, Drost J. Generation of human kidney tubuloids from tissue and urine. J Vis Exp, 2021, (170). DOI: 10.3791/62404-v.
34. Al-Ghadban S, Pursell I A, Diaz Z T, et al. 3D spheroids derived from human lipedema ASCs demonstrated similar adipogenic differentiation potential and ECM remodeling to non-lipedema ASCs in vitro. Int J Mol Sci, 2020, 21(21): 8350.
35. Huch M, Dorrell C, Boj S F, et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature, 2013, 494(7436): 247-250.
36. Furuya K, Zheng Y W, Sako D, et al. Enhanced hepatic differentiation in the subpopulation of human amniotic stem cells under 3D multicellular microenvironment. World J Stem Cells, 2019, 11(9): 705-721.
37. Pleguezuelos-Manzano C, Puschhof J, van den Brink S, et al. Establishment and culture of human intestinal organoids derived from adult stem cells. Curr Protoc Immunol, 2020, 130(1): e106.
38. Greggio C, De Franceschi F, Figueiredo-Larsen M, et al. Artificial three-dimensional niches deconstruct pancreas development in vitro. Development, 2013, 140(21): 4452-4462.
39. Fordham R P, Yui S, Hannan N R, et al. Transplantation of expanded fetal intestinal progenitors contributes to colon regeneration after injury. Cell Stem Cell, 2013, 13(6): 734-744.
40. Saito Y, Matsumoto N, Yamanaka S, et al. Beneficial impact of interspecies chimeric renal organoids against a xenogeneic immune response. Front Immunol, 2022, 13: 848433.
41. Cambuli F, Foletto V, Alaimo A, et al. Intra-epithelial non-canonical Activin A signaling safeguards prostate progenitor quiescence. EMBO Rep, 2022, 23(5): e54049.
42. Bhang S H, Lee S, Shin J Y, et al. Transplantation of cord blood mesenchymal stem cells as spheroids enhances vascularization. Tissue Eng Part A, 2012, 18(19-20): 2138-2147.
43. Weiss S, Hennig T, Bock R, et al. Impact of growth factors and PTHrP on early and late chondrogenic differentiation of human mesenchymal stem cells. J Cell Physiol, 2010, 223(1): 84-93.
44. Al-Nbaheen M, Vishnubalaji R, Ali D, et al. Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev Rep, 2013, 9(1): 32-43.
45. Wang C, Yin S, Cen L, et al. Differentiation of adipose-derived stem cells into contractile smooth muscle cells induced by transforming growth factor-beta1 and bone morphogenetic protein-4. Tissue Eng Part A, 2010, 16(4): 1201-1213.
46. He Y T, Zhu X L, Li S F, et al. Creating rat hepatocyte organoid as an in vitro model for drug testing. World J Stem Cells, 2020, 12(10): 1184-1195.
47. Leeman K T, Pessina P, Lee J H, et al. Mesenchymal stem cells increase alveolar differentiation in lung progenitor organoid cultures. Sci Rep, 2019, 9(1): 6479.
48. Strobel H A, Gerton T, Hoying J B. Vascularized adipocyte organoid m odel using isolated human microvessel fragments. Biofabrication, 2021, 13(3): 035022.
49. 周子墨, 柳达, 陈森相, 等. 3D细胞培养和类器官在骨髓源性间充质干细胞成骨分化中的研究进展. 中国骨质疏松杂志, 2022, 28(9): 1400-1404.
50. Martini G, Belli V, Napolitano S, et al. Establishment of patient-derived tumor organoids to functionally inform treatment decisions in metastatic colorectal cancer. ESMO Open, 2023, 8(3): 101198.
51. Dutta D, Heo I, Clevers H. Disease modeling in stem cell-derived 3D organoid systems. Trends Mol Med, 2017, 23(5): 393-410.
52. Shembrey C, Smith J, Grandin M, et al. Longitudinal monitoring of intra-tumoural heterogeneity using optical barcoding of patient-derived colorectal tumour models. Cancers (Basel), 2022, 14(3): 581.
53. Bhatia S, Kramer M, Russo S, et al. Patient-derived triple-negative breast cancer organoids provide robust model systems that recapitulate tumor intrinsic characteristics. Cancer Res, 2022, 82(7): 1174-1192.
54. Hubert C G, Rivera M, Spangler L C, et al. A three-dimensional organoid culture system derived from human glioblastomas recapitulates the hypoxic gradients and cancer stem cell heterogeneity of tumors found in vivo. Cancer Res, 2016, 76(8): 2465-2477.
55. Tindle C, Fuller M, Fonseca A, et al. Adult stem cell-derived complete lung orga noid models emulate lung disease in COVID-19. Elife, 2021, 10: e66417.
56. Hallett J M, Ferreira-Gonzalez S, Man T Y, et al. Human biliary epithelial cells from discarded donor livers rescue bile duct structure and function in a mouse model of biliary disease. Cell Stem Cell, 2022, 29(3): 355-371.
57. Vonk A C, Hasel-Kolossa S C, Lopez G A, et al. Lizard blastema organoid model recapitulates regenerated tail chondrogenesis. J Dev Biol, 2022, 10(1): 12.
58. Asai A, Aihara E, Watson C, et al. Paracrine signals regulate human liver organoid maturation from induced pluripotent stem cells. Development, 2017, 144(6): 1056-1064.
59. Takebe T, Sekine K, Enomura M, et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature, 2013, 499(7459): 481-484.
60. Homan K A, Gupta N, Kroll K T, et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat Methods, 2019, 16(3): 255-262.
61. Takahashi Y, Sekine K, Kin T, et al. Self-condensation culture enables vascularization of tissue fragments for efficient therapeutic transplantation. Cell Rep, 2018, 23(6): 1620-1629.
62. Wimmer R A, Leopoldi A, Aichinger M, et al. Generation of blood vessel organoids from human pluripotent stem cells. Nat Protoc, 2019, 14(11): 3082-3100.
63. Song J W, Munn L L. Fluid forces control endothelial sprouting. Proc Natl Acad Sci U S A, 2011, 108(37): 15342-15347.
64. Ibrahim M, Richardson M K. Beyond organoids: In vitro vasculogenesis and angiogenesis using cells from mammals and zebrafish. Reprod Toxicol, 2017, 73: 292-311.
65. Moya M L, Hsu Y-H, Lee A P, et al. In vitro perfused human capillary networks. Tissue Eng Part C: Methods, 2013, 19(9): 730-737.
66. Zhang S, Wan Z, Kamm R D. Vascularized organoids on a chip: strategies for engineering organoids with functional vasculature. Lab Chip, 2021, 21(3): 473-488.
67. Rajasekar S, Lin D S Y, Abdul L, et al. IFlowPlate-A customized 384-well plate for the culture of perfusable vascularized colon organoids. Adv Mater, 2020, 32(46): e2002974.
68. Lee H N, Choi Y Y, Kim J W, et al. Effect of biochemical and biomechanical factors on vascularization of kidney organoid-on-a-chip. Nano Converg, 2021, 8(1): 35.
69. Nashimoto Y, Okada R, Hanada S, et al. Vascularized cancer on a chip: The effect of perfusion on growth and drug delivery of tumor spheroid. Biomaterials, 2020, 229: 119547.

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