한국발생생물학회지:발생과생식 (Development and Reproduction)

  • 제27권2호
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  • Pages.57-65
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  • 2023
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  • 2465-9525(pISSN)
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  • 2465-9541(eISSN)
한국발생생물학회 (The Korean Society of Developmental Biology)
권호 표지
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Kidney Organoid Derived from Human Pluripotent and Adult Stem Cells for Disease Modeling

  • Hyun Mi Kang (Korea Research Institute of Bioscience and Biotechnology (KRIBB))
  • 투고 : 2023.02.28
  • 심사 : 2023.05.26
  • 발행 : 2023.06.30
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⟨ 이전 논문 다음 논문 ⟩

초록

Kidney disease affects a significant portion of the global population, yet effective therapies are lacking despite advancements in identifying genetic causes. This limitation can be attributed to the absence of adequate in vitro models that accurately mimic human kidney disease, hindering targeted therapeutic development. However, the emergence of human induced pluripotent stem cells (PSCs) and the development of organoids using them have opened up a way to model kidney development and disease in humans, as well as validate the effects of new drugs. To fully leverage their capabilities in these fields, it is crucial for kidney organoids to closely resemble the structure and functionality of adult human kidneys. In this review, we aim to discuss the potential of using human PSCs or adult kidney stem cell-derived kidney organoids to model genetic kidney disease and renal cancer.

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과제정보

This research was supported by the Korea Research Institute of Bioscience and Biotechnology (KRIBB) Research Initiative Program (KGM4722122), and the National Research Foundation of Korea funded by the Ministry of Science and ICT (NRF2019R1C1C1006822).

참고문헌

  1. Al-Bataineh MM, Kinlough CL, Poland PA, Pastor-Soler NM, Sutton TA, Mang HE, Bastacky SI, Gendler SJ, Madsen CS, Singh S, Monga SP, Hughey RP (2016) Muc1 enhances the β-catenin protective pathway during ischemia-reperfusion injury. Am J Physiol Renal Physiol 310:F569-F579. https://doi.org/10.1152/ajprenal.00520.2015
  2. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M, Danenberg E, van den Brink S, Korving J, Abo A, Peters PJ, Wright N, Poulsom R, Clevers H (2010) Lgr5+ve stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6:25-36. https://doi.org/10.1016/j.stem.2009.11.013
  3. Bingham C, Ellard S, Van't Hoff WG, Anne Simmonds H, Marinaki AM, Badman MK, Winocour PH, Stride A, Lockwood CR, Nicholls AJ, Owen KR, Spyer G, Pearson ER, Hattersley AT (2003) Atypical familial juvenile hyperuricemic nephropathy associated with a hepatocyte nuclear factor-1β gene mutation. Kidney Int 63:1645-1651. https://doi.org/10.1046/j.1523-1755.2003.00903.x
  4. Boj SF, Hwang CI, Baker LA, Chio IIC, Engle DD, Corbo V, et al. (2015) Organoid models of human and mouse ductal pancreatic cancer. Cell 160:324-338. https://doi.org/10.1016/j.cell.2014.12.021
  5. Calandrini C, Schutgens F, Oka R, Margaritis T, Candelli T, Mathijsen L, et al. (2020) An organoid biobank for childhood kidney cancers that captures disease and tissue heterogeneity. Nat Commun 11:1310.
  6. Capowski EE, Samimi K, Mayerl SJ, Joseph Phillips M, Pinilla I, Howden SE, Saha J, Jansen AD, Edwards KL, Jager LD, Barlow K, Valiauga R, Erlichman Z, Hagstrom A, Sinha D, Sluch VM, Chamling X, Zack DJ, Skala MC, Gamm DM (2019) Reproducibility and staging of 3D human retinal organoids across multiple pluripotent stem cell lines. Development 146:dev171686.
  7. Chen YW, Huang SX, de Carvalho ALRT, Ho SH, Islam MN, Volpi S, Notarangelo LD, Ciancanelli M, Casanova JL, Bhattacharya J, Liang AF, Palermo LM, Porotto M, Moscona A, Snoeck HW (2017) A three-dimensional model of human lung development and disease from pluripotent stem cells. Nat Cell Biol 19:542-549. https://doi.org/10.1038/ncb3510
  8. Clevers H (2016) Modeling development and disease with organoids. Cell 165:1586-1597. https://doi.org/10.1016/j.cell.2016.05.082
  9. Coffinier C, Barra J, Babinet C, Yaniv M (1999) Expression of the vHNF1/HNF1β homeoprotein gene during mouse organogenesis. Mech Dev 89:211-213. https://doi.org/10.1016/S0925-4773(99)00221-X
  10. Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS (2007) Prevalence of chronic kidney disease in the United States. J Am Med Assoc 298:2038-2047. https://doi.org/10.1001/jama.298.17.2038
  11. Creighton CJ, Morgan M, Gunaratne PH, Wheeler DA, Gibbs RA, Robertson AG, et al. (2013) Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499:43-49. https://doi.org/10.1038/nature12222
  12. Cruz NM, Song X, Czerniecki SM, Gulieva RE, Churchill AJ, Kim YK, Winston K, Tran LM, Diaz MA, Fu H, Finn LS, Pei Y, Himmelfarb J, Freedman BS (2017) Organoid cystogenesis reveals a critical role of microenvironment in human polycystic kidney disease. Nat Mater 16:1112-1119. https://doi.org/10.1038/nmat4994
  13. Davis CF, Ricketts CJ, Wang M, Yang L, Cherniack AD, Shen H, et al. (2014) The somatic genomic landscape of chromophobe renal cell carcinoma. Cancer Cell 26:319-330. https://doi.org/10.1016/j.ccr.2014.07.014
  14. Decramer S, Parant O, Beaufils S, Clauin S, Guillou C, Kessler S, Aziza J, Bandin F, Schanstra JP, Bellanne-Chantelot C (2007) Anomalies of the TCF2 gene are the main cause of fetal bilateral hyperechogenic kidneys. J Am Soc Nephrol 18:923-933. https://doi.org/10.1681/ASN.2006091057
  15. Doyonnas R, Kershaw DB, Duhme C, Merkens H, Chelliah S, Graf T, McNagny KM (2001) Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exp Med 194:13-28. https://doi.org/10.1084/jem.194.1.13
  16. Dvela-Levitt M, Kost-Alimova M, Emani M, Kohnert E, Thompson R, Sidhom EH, et al. (2019) Small molecule targets TMED9 and promotes lysosomal degradation to reverse proteinopathy. Cell 178:521-535.E23. https://doi.org/10.1016/j.cell.2019.07.002
  17. Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, Nishiyama A, Muguruma K, 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
  18. Eneanya ND, Wenger JB, Waite K, Crittenden S, Hazar DB, Volandes A, Temel JS, Thadhani R, Paasche-Orlow MK (2016) Racial disparities in end-of-life communication and preferences among chronic kidney disease patients. Am J Nephrol 44:46-53. https://doi.org/10.1159/000447097
  19. Fatehullah A, Tan SH, Barker N (2016) Organoids as an in vitro model of human development and disease. Nat Cell Biol 18:246-254. https://doi.org/10.1038/ncb3312
  20. Fitzgerald HC, Dhakal P, Behura SK, Schust DJ, Spencer TE (2019) Self-renewing endometrial epithelial organoids of the human uterus. Proc Natl Acad Sci USA 116:23132-23142. https://doi.org/10.1073/pnas.1915389116
  21. Freedman BS, Brooks CR, Lam AQ, Fu H, Morizane R, Agrawal V, et al. (2015) Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nat Commun 6:8715.
  22. Gahl WA, Thoene JG, Schneider JA (2002) Cystinosis. N Engl J Med 347:111-121. https://doi.org/10.1056/NEJMra020552
  23. Gibier JB, Hemon B, Fanchon M, Gaudelot K, Pottier N, Ringot B, Van Seuningen I, Glowacki F, Cauffiez C, Blum D, Copin MC, Perrais M, Gnemmi V (2017) Dual role of MUC1 mucin in kidney ischemia-reperfusion injury: Nephroprotector in early phase, but pro-fibrotic in late phase. Biochim Biophys Acta Mol Basis Dis 1863:1336-1349. https://doi.org/10.1016/j.bbadis.2017.03.023
  24. Grassi L, Alfonsi R, Francescangeli F, Signore M, De Angelis ML, Addario A, et al. (2019) Organoids as a new model for improving regenerative medicine and cancer personalized therapy in renal diseases. Cell Death Dis 10:201.
  25. Gresh L, Fischer E, Reimann A, Tanguy M, Garbay S, Shao X, Hiesberger T, Fiette L, Igarashi P, Yaniv M, Pontoglio M (2004) A transcriptional network in polycystic kidney disease. EMBO J 23:1657-1668. https://doi.org/10.1038/sj.emboj.7600160
  26. Hale LJ, Howden SE, Phipson B, Lonsdale A, Er PX, Ghobrial I, Hosawi S, Wilson S, Lawlor KT, Khan S, Oshlack A, Quinlan C, Lennon R, Little MH (2018) 3D organoid-derived human glomeruli for personalised podocyte disease modelling and drug screening. Nat Commun 9:5167.
  27. Harris PC, Torres VE (2014) Genetic mechanisms and signaling pathways in autosomal dominant polycystic kidney disease. J Clin Invest 124:2315-2324. https://doi.org/10.1172/JCI72272
  28. Hohwieler M, Illing A, Hermann PC, Mayer T, Stockmann M, Perkhofer L, et al. (2017) Human pluripotent stem cell-derived acinar/ductal organoids generate human pancreas upon orthotopic transplantation and allow disease modelling. Gut 66:473-486. https://doi.org/10.1136/gutjnl-2016-312423
  29. Hollywood JA, Przepiorski A, D'souza RF, Sreebhavan S, Wolvetang EJ, Harrison PT, Davidson AJ, Holm TM (2020) Use of human induced pluripotent stem cells and kidney organoids to develop a cysteamine/mTOR inhibition combination therapy for cystinosis. J Am Soc Nephrol 31:962-982. https://doi.org/10.1681/ASN.2019070712
  30. Hsieh JJ, Purdue MP, Signoretti S, Swanton C, Albiges L, Schmidinger M, Heng DY, Larkin J, Ficarra V (2017) Renal cell carcinoma. Nat Rev Dis Primers 3:17009.
  31. Hu H, Gehart H, Artegiani B, Lopez-Iglesias C, Dekkers F, Basak O, et al. (2018) Long-term expansion of functional mouse and human hepatocytes as 3D organoids. Cell 175:1591-1606. E19. https://doi.org/10.1016/j.cell.2018.11.013
  32. Hwang JW, Desterke C, Feraud O, Richard S, Ferlicot S, Verkarre V, Patard JJ, Loisel-Duwattez J, Foudi A, Griscelli F, Bennaceur-Griscelli A, Turhan AG (2019) iPSC-derived embryoid bodies as models of c-Met-mutated hereditary papillary renal cell carcinoma. Int J Mol Sci 20:4867.
  33. Kang HG, Lee M, Lee KB, Hughes M, Kwon BS, Lee S, McNagny KM, Ahn YH, Ko JM, Ha IS, Choi M, Cheong HI (2017) Loss of podocalyxin causes a novel syndromic type of congenital nephrotic syndrome. Exp Mol Med 49:e414.
  34. Karthaus WR, Iaquinta PJ, Drost J, Gracanin A, van Boxtel R, Wongvipat J, Dowling CM, Gao D, Begthel H, Sachs N, Vries RGJ, Cuppen E, Chen Y, Sawyers CL, Clevers HC (2014) Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell 159:163-175. https://doi.org/10.1016/j.cell.2014.08.017
  35. Kim YK, Refaeli I, Brooks CR, Jing P, Gulieva RE, Hughes MR, Cruz NM, Liu Y, Churchill AJ, Wang Y, Fu H, Pippin JW, Lin LY, Shankland SJ, Wayne Vogl A, McNagny KM, Freedman BS (2017) Gene-edited human kidney organoids reveal mechanisms of disease in podocyte development. Stem Cells 35:2366-2378. https://doi.org/10.1002/stem.2707
  36. Kirby A, Gnirke A, Jaffe DB, Baresova V, Pochet N, Blumenstiel B, et al. (2013) Mutations causing medullary cystic kidney disease type 1 lie in a large VNTR in MUC1 missed by massively parallel sequencing. Nat Genet 45:299-303. https://doi.org/10.1038/ng.2543
  37. Kuraoka S, Tanigawa S, Taguchi A, Hotta A, Nakazato H, Osafune K, Kobayashi A, Nishinakamura R (2020) PKD1-dependent renal cystogenesis in human induced pluripotent stem cell-derived ureteric bud/collecting duct organoids. J Am Soc Nephrol 31:2355-2371. https://doi.org/10.1681/ASN.2020030378
  38. Kurmann AA, Serra M, Hawkins F, Rankin SA, Mori M, Astapova I, Ullas S, Lin S, Bilodeau M, Rossant J, Jean JC, Ikonomou L, Deterding RR, Shannon JM, Zorn AM, Hollenberg AN, Kotton DN (2015) Regeneration of thyroid function by transplantation of differentiated pluripotent stem cells. Cell Stem Cell 17:527-542. https://doi.org/10.1016/j.stem.2015.09.004
  39. Lasagni L, Lazzeri E, Shankland SJ, Anders HJ, Romagnani P (2013) Podocyte mitosis: A catastrophe. Curr Mol Med 13:13-23. https://doi.org/10.2174/156652413804486250
  40. Li Z, Xu H, Yu L, Wang J, Meng Q, Mei H, Cai Z, Chen W, Huang W (2022) Patient-derived renal cell carcinoma organoids for personalized cancer therapy. Clin Transl Med 12:e970.
  41. Low JH, Li P, Chew EGY, Zhou B, Suzuki K, Zhang T, Lian MM, Liu M, Aizawa E, Rodriguez Esteban C, Yong KSM, Chen Q, Campistol JM, Fang M, Khor CC, Foo JN, Izpisua Belmonte JC, Xia Y (2019) Generation of human PSC-derived kidney organoids with patterned nephron segments and a de novo vascular network. Cell Stem Cell 25:373-387.E9. https://doi.org/10.1016/j.stem.2019.06.009
  42. Mae SI, Ryosaka M, Sakamoto S, Matsuse K, Nozaki A, Igami M, Kabai R, Watanabe A, Osafune K (2020) Expansion of human iPSC-derived ureteric bud organoids with repeated branching potential. Cell Rep 32:107963.
  43. Marston Linehan W, Spellman PT, Ricketts CJ, Creighton CJ, Fei SS, Davis C, et al. (2016) Comprehensive molecular characterization of papillary renal-cell carcinoma. N Engl J Med 374:135-145. https://doi.org/10.1056/NEJMoa1505917
  44. Nakanishi K, Sweeney WE Jr, Zerres K, Guay-Woodford LM, Avner ED (2000) Proximal tubular cysts in fetal human autosomal recessive polycystic kidney disease. J Am Soc Nephrol 11:760-763. https://doi.org/10.1681/ASN.V114760
  45. Ogawa M, Ogawa S, Bear CE, Ahmadi S, Chin S, Li B, Grompe M, Keller G, Kamath BM, Ghanekar A (2015) Directed differentiation of cholangiocytes from human pluripotent stem cells. Nat Biotechnol 33:853-861. https://doi.org/10.1038/nbt.3294
  46. Przepiorski A, Sander V, Tran T, Hollywood JA, Sorrenson B, Shih JH, Wolvetang EJ, McMahon AP, Holm TM, Davidson AJ (2018) A simple bioreactor-based method to generate kidney organoids from pluripotent stem cells. Stem Cell Rep 11:470-484. https://doi.org/10.1016/j.stemcr.2018.06.018
  47. Sachs N, de Ligt J, Kopper O, Gogola E, Bounova G, Weeber F, 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
  48. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H (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
  49. Schell C, Wanner N, Huber TB (2014) Glomerular development - shaping the multi-cellular filtration unit. Semin Cell Dev Biol 36:39-49. https://doi.org/10.1016/j.semcdb.2014.07.016
  50. Schutgens F, Rookmaaker MB, Margaritis T, Rios A, Ammerlaan C, Jansen J, et al. (2019) Tubuloids derived from human adult kidney and urine for personalized disease modeling. Nat Biotechnol 37:303-313. https://doi.org/10.1038/s41587-019-0048-8
  51. Sharmin S, Taguchi A, Kaku Y, Yoshimura Y, Ohmori T, Sakuma T, Mukoyama M, Yamamoto T, Kurihara H, Nishinakamura R (2016) Human induced pluripotent stem cell-derived podocytes mature into vascularized glomeruli upon experimental transplantation. J Am Soc Nephrol 27:1778-1791. https://doi.org/10.1681/ASN.2015010096
  52. Shimizu T, Mae SI, Araoka T, Okita K, Hotta A, Yamagata K, Osafune K (2020) A novel ADPKD model using kidney organoids derived from disease-specific human iPSCs. Biochem Biophys Res Commun 529:1186-1194. https://doi.org/10.1016/j.bbrc.2020.06.141
  53. Takasato M, Er PX, Chiu HS, Maier B, Baillie GJ, Ferguson C, Parton RG, Wolvetang EJ, Roost MS, Chuva de Sousa Lopes SM, Little MH (2015) Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 536:238.
  54. Tanigawa S, Islam M, Sharmin S, Naganuma H, Yoshimura Y, Haque F, Era T, Nakazato H, Nakanishi K, Sakuma T, Yamamoto T, Kurihara H, Taguchi A, Nishinakamura R (2018) Organoids from nephrotic disease-derived iPSCs identify impaired NEPHRIN localization and slit diaphragm formation in kidney podocytes. Stem Cell Reports 11:727-740. https://doi.org/10.1016/j.stemcr.2018.08.003
  55. Torres VE, Harris PC, Pirson Y (2007) Autosomal dominant polycystic kidney disease. Lancet 369:1287-1301. https://doi.org/10.1016/S0140-6736(07)60601-1
  56. Tsai YH, Nattiv R, Dedhia PH, Nagy MS, Chin AM, Thomson M, Klein OD, Spence JR (2017) In vitro patterning of pluripotent stem cell-derived intestine recapitulates in vivo human development. Development 144:1045-1055.
  57. Ulinski T, Lescure S, Beaufils S, Guigonis V, Decramer S, Morin D, Clauin S, Deschenes G, Bouissou F, Bensman A, Bellanne-Chantelot C (2006) Renal phenotypes related to hepatocyte nuclear factor-1β (TCF2) mutations in a pediatric cohort. J Am Soc Nephrol 17:497-503. https://doi.org/10.1681/ASN.2005101040