Organoids and organoid extracellular vesicles-based disease treatment strategies.

Publisher: BioMed Central Country of Publication: England NLM ID: 101152208 Publication Model: Electronic Cited Medium: Internet ISSN: 1477-3155 (Electronic) Linking ISSN: 14773155 NLM ISO Abbreviation: J Nanobiotechnology Subsets: MEDLINE

Original Publication: London : BioMed Central, 2003-

Organoids*/metabolism ; Extracellular Vesicles*/metabolism; Humans ; Animals ; Stem Cells/cytology ; Drug Delivery Systems/methods

Organoids are "mini-organs" that self-organize and differentiate from stem cells under in vitro 3D culture conditions, mimicking the spatial structure and function of tissues in vivo. Extracellular vesicles (EVs) are nanoscale phospholipid bilayer vesicles secreted by living cells, rich in bioactive molecules, with excellent biocompatibility and low immunogenicity. Compared to EVs, organoid-derived EVs (OEVs) exhibit higher yield and enhanced biological functions. Organoids possess stem cell characteristics, and OEVs are capable of delivering active substances, making both highly promising for medical applications. In this review, we provide an overview of the fundamental biological principles of organoids and OEVs, and discuss their current applications in disease treatment. We then focus on the differences between OEVs and traditional EVs. Subsequently, we present methods for the engineering modification of OEVs. Finally, we critically summarize the advantages and challenges of organoids and OEVs. In conclusion, we believe that a deeper understanding of organoids and OEVs will provide innovative solutions to complex diseases.
(© 2024. The Author(s).)

Front Cell Dev Biol. 2022 Jan 03;9:787118. (PMID: 35047499)
Blood. 2012 Jan 19;119(3):756-66. (PMID: 22031862)
Trends Cell Biol. 2017 Mar;27(3):172-188. (PMID: 27979573)
Trends Cell Biol. 2008 Oct;18(10):505-16. (PMID: 18774294)
Cell Stem Cell. 2023 Jan 5;30(1):10-19. (PMID: 36608674)
Nat Chem Biol. 2022 Mar;18(3):244-255. (PMID: 35058646)
Biosens Bioelectron. 2021 Dec 15;194:113589. (PMID: 34543824)
Crit Care Med. 2003 Jan;31(1 Suppl):S1-6. (PMID: 12544970)
Arch Med Sci. 2018 Jun;14(4):910-919. (PMID: 30002710)
Biomaterials. 2024 Jun;307:122522. (PMID: 38428092)
Cell Rep Med. 2023 Jan 17;4(1):100881. (PMID: 36603578)
J Extracell Vesicles. 2022 Jun;11(6):e12235. (PMID: 35716062)
Front Cell Dev Biol. 2021 Dec 23;9:761807. (PMID: 35004672)
Cell. 2015 Jan 15;160(1-2):299-312. (PMID: 25533785)
J Control Release. 2023 Dec;364:46-60. (PMID: 37866404)
Nat Methods. 2015 Jul;12(7):671-8. (PMID: 26005811)
Adv Sci (Weinh). 2018 Jan 30;5(4):1700611. (PMID: 29721412)
J Extracell Vesicles. 2020 Apr 21;9(1):1748931. (PMID: 32373289)
Bioconjug Chem. 2014 Oct 15;25(10):1777-84. (PMID: 25220352)
Nat Med. 2017 Jan;23(1):49-59. (PMID: 27869805)
Research (Wash D C). 2023;6:0089. (PMID: 36996343)
Nat Mater. 2021 Feb;20(2):145-155. (PMID: 33199860)
Exp Mol Med. 2019 Mar 15;51(3):1-12. (PMID: 30872574)
Acta Biomater. 2019 Nov;99:247-257. (PMID: 31539656)
Adv Mater. 2021 Nov;33(45):e2007949. (PMID: 34561899)
Adv Mater. 2017 Apr;29(13):. (PMID: 28165174)
Nat Rev Neurosci. 2017 Oct;18(10):573-584. (PMID: 28878372)
ACS Nano. 2019 Feb 26;13(2):1499-1510. (PMID: 30677286)
Tumour Biol. 2017 Feb;39(2):1010428317691182. (PMID: 28231725)
Plant Physiol. 2017 Jan;173(1):728-741. (PMID: 27837092)
J Extracell Vesicles. 2016 May 17;5:30829. (PMID: 27193612)
Biomed Pharmacother. 2023 May;161:114557. (PMID: 36963364)
J Extracell Vesicles. 2021 Dec;10(14):e12182. (PMID: 34953156)
J Control Release. 2022 Aug;348:723-744. (PMID: 35718214)
J Nanobiotechnology. 2023 Apr 27;21(1):137. (PMID: 37106449)
Nano Lett. 2019 May 8;19(5):3040-3048. (PMID: 30968694)
Cell Stem Cell. 2020 May 7;26(5):766-781.e9. (PMID: 32142682)
Nat Biomed Eng. 2020 Sep;4(9):863-874. (PMID: 32514094)
Nat Neurosci. 2007 Oct;10(10):1294-9. (PMID: 17828256)
J Control Release. 2012 Dec 10;164(2):183-6. (PMID: 22446384)
Nat Protoc. 2021 Feb;16(2):579-602. (PMID: 33328611)
Cell Stem Cell. 2018 Dec 6;23(6):869-881.e8. (PMID: 30449713)
Gastroenterology. 2011 Nov;141(5):1762-72. (PMID: 21889923)
Bioact Mater. 2023 Jan 20;25:29-41. (PMID: 37056252)
Stem Cell Res Ther. 2022 Aug 19;13(1):425. (PMID: 35986305)
Cell. 2016 Jun 16;165(7):1586-1597. (PMID: 27315476)
Nat Protoc. 2019 Jun;14(6):1884-1925. (PMID: 31110298)
Brain Res. 1990 Jul 16;523(1):78-86. (PMID: 2207692)
Prog Retin Eye Res. 2020 Mar;75:100779. (PMID: 31494256)
Nat Med. 2021 Jan;27(1):125-135. (PMID: 33432170)
Pharm Res. 2023 Apr;40(4):801-816. (PMID: 36002615)
Neurochem Int. 2017 Dec;111:69-81. (PMID: 27539657)
Nat Rev Gastroenterol Hepatol. 2017 Nov;14(11):688. (PMID: 29018274)
Nat Biotechnol. 2011 Apr;29(4):341-5. (PMID: 21423189)
Cell Metab. 2019 Aug 6;30(2):374-384.e6. (PMID: 31155493)
Trends Pharmacol Sci. 2022 Jul;43(7):569-581. (PMID: 35504760)
Science. 2021 Feb 19;371(6531):839-846. (PMID: 33602855)
Biomark Res. 2022 Aug 7;10(1):57. (PMID: 35933395)
Dev Cell. 2017 Jan 9;40(1):95-103. (PMID: 28041903)
Biomater Adv. 2022 Feb;133:112647. (PMID: 35067434)
Mol Cancer Res. 2019 Feb;17(2):337-347. (PMID: 30487244)
Sci Adv. 2023 Apr 5;9(14):eabo7868. (PMID: 37018403)
Signal Transduct Target Ther. 2022 Mar 10;7(1):78. (PMID: 35273164)
ACS Nano. 2018 Jul 24;12(7):6830-6842. (PMID: 29975503)
Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20284-9. (PMID: 24277810)
Cell Stem Cell. 2023 Feb 2;30(2):137-152.e7. (PMID: 36736289)
ACS Nano. 2022 Jan 25;16(1):771-782. (PMID: 34979087)
ACS Appl Mater Interfaces. 2016 Mar 23;8(11):6790-5. (PMID: 26954538)
Sci China Life Sci. 2021 Oct;64(10):1661-1676. (PMID: 33521856)
Biomaterials. 2022 Sep;288:121741. (PMID: 36031458)
J Hematol Oncol. 2022 Jul 21;15(1):99. (PMID: 35864538)
Bioact Mater. 2022 May 27;20:166-178. (PMID: 35663338)
EBioMedicine. 2022 Mar;77:103914. (PMID: 35278743)
Adv Sci (Weinh). 2021 Oct;8(19):e2101437. (PMID: 34382379)
Theranostics. 2022 Sep 11;12(15):6576-6594. (PMID: 36185613)
Theranostics. 2018 Jan 1;8(1):237-255. (PMID: 29290805)
J Extracell Vesicles. 2024 Jan;13(1):e12401. (PMID: 38151470)
Commun Biol. 2020 Mar 13;3(1):116. (PMID: 32170210)
J Extracell Vesicles. 2024 Apr;13(4):e12429. (PMID: 38576241)
Bone Res. 2021 Mar 17;9(1):20. (PMID: 33731688)
Protein Cell. 2016 Feb;7(2):100-13. (PMID: 26399619)
Adv Sci (Weinh). 2018 Dec 20;6(4):1800948. (PMID: 30828519)
Nat Rev Mol Cell Biol. 2018 Apr;19(4):213-228. (PMID: 29339798)
Nat Biotechnol. 2023 Jun;41(6):824-831. (PMID: 36702898)
Am J Physiol Cell Physiol. 2020 Jul 1;319(1):C151-C165. (PMID: 32459504)
Gastroenterology. 2021 Feb;160(3):831-846.e10. (PMID: 33039464)
Annu Rev Pathol. 2020 Jan 24;15:211-234. (PMID: 31550983)
J Control Release. 2022 Jul;347:533-543. (PMID: 35597405)
Signal Transduct Target Ther. 2021 Feb 11;6(1):59. (PMID: 33568623)
Adv Mater. 2024 Jul;36(30):e2309875. (PMID: 38642033)
Bioscience. 2015 Aug 1;65(8):783-797. (PMID: 26955082)
Bioact Mater. 2021 Dec 17;14:169-181. (PMID: 35310361)
Aging Dis. 2021 Sep 1;12(6):1438-1450. (PMID: 34527420)
Invest Ophthalmol Vis Sci. 2002 Mar;43(3):864-9. (PMID: 11867609)
Biochim Biophys Acta. 2014 Jan;1841(1):108-20. (PMID: 24140720)
Nat Cell Biol. 2007 Jun;9(6):654-9. (PMID: 17486113)
Neuron. 1995 Oct;15(4):805-19. (PMID: 7576630)
Cell. 2016 May 19;165(5):1238-1254. (PMID: 27118425)
Stem Cells Transl Med. 2019 Aug;8(8):775-784. (PMID: 31037833)
Bioact Mater. 2023 Jun 01;28:273-283. (PMID: 37303851)
Adv Healthc Mater. 2023 Jul;12(18):e2203361. (PMID: 36881547)
Bioact Mater. 2022 Nov 11;23:156-169. (PMID: 36406248)
Bioact Mater. 2022 Nov 14;23:206-222. (PMID: 36439082)
Cell Commun Signal. 2022 May 23;20(1):69. (PMID: 35606749)
Nat Rev Cancer. 2018 Jul;18(7):407-418. (PMID: 29692415)
Science. 2014 Jul 18;345(6194):1247125. (PMID: 25035496)
Nat Rev Mol Cell Biol. 2020 Oct;21(10):571-584. (PMID: 32636524)
Alzheimers Dement. 2023 Nov;19(11):4828-4840. (PMID: 37023079)
ACS Sens. 2021 Apr 23;6(4):1418-1429. (PMID: 33755415)
Bioact Mater. 2021 Sep 17;10:207-221. (PMID: 34901540)
Sci Rep. 2021 Oct 26;11(1):21128. (PMID: 34702879)
J Extracell Vesicles. 2015 May 14;4:27066. (PMID: 25979354)
Small. 2020 Jan;16(3):e1906273. (PMID: 31840420)
Nat Commun. 2019 Mar 14;10(1):1205. (PMID: 30872578)
Small. 2022 Jan;18(1):e2104229. (PMID: 34791802)
Mucosal Immunol. 2021 Jul;14(4):887-898. (PMID: 33854193)
J Control Release. 2015 Dec 10;219:396-405. (PMID: 26241750)
Nat Med. 2017 Aug;23(8):954-963. (PMID: 28671689)
J Am Coll Cardiol. 2021 Mar 2;77(8):1073-1088. (PMID: 33632482)
J Extracell Vesicles. 2021 Sep;10(11):e12145. (PMID: 34514732)
Nat Rev Genet. 2018 Nov;19(11):671-687. (PMID: 30228295)
Nat Cell Biol. 2019 Jan;21(1):9-17. (PMID: 30602770)
Digestion. 2023;104(1):24-29. (PMID: 36353779)
Cancer Lett. 2023 May 28;562:216180. (PMID: 37061121)
Nat Protoc. 2023 May;18(5):1462-1487. (PMID: 36914899)
Retrovirology. 2021 Feb 23;18(1):6. (PMID: 33622348)
J Extracell Vesicles. 2014 Nov 13;3:24722. (PMID: 25398455)
J Head Trauma Rehabil. 1999 Dec;14(6):602-15. (PMID: 10671706)
J Hematol Oncol. 2023 Apr 8;16(1):36. (PMID: 37031172)
Adv Healthc Mater. 2023 Jul;12(18):e2203131. (PMID: 36854163)
Cell Stem Cell. 2018 Jul 05;23(1):25-30. (PMID: 29681514)
Nat Biotechnol. 2021 Jan;39(1):13-17. (PMID: 33384458)
Mil Med Res. 2022 Nov 19;9(1):65. (PMID: 36401295)
Chem Rev. 2018 Feb 28;118(4):1917-1950. (PMID: 29384376)
Theranostics. 2021 Jan 1;11(1):397-409. (PMID: 33391482)
Drug Discov Today. 2022 Apr;27(4):1062-1076. (PMID: 34954328)
Nat Commun. 2015 Apr 01;6:6716. (PMID: 25828099)
Bioact Mater. 2021 Nov 03;13:300-311. (PMID: 35224310)
J Extracell Vesicles. 2018 Jan 21;7(1):1422674. (PMID: 29410778)
Cells. 2022 Oct 30;11(21):. (PMID: 36359825)
Prog Retin Eye Res. 2021 Nov;85:100970. (PMID: 33930561)
Nat Immunol. 2002 Dec;3(12):1156-62. (PMID: 12426563)
Bioact Mater. 2022 Feb 16;18:151-163. (PMID: 35387159)
Nat Med. 2012 Mar 11;18(4):618-23. (PMID: 22406745)
Sci Transl Med. 2019 May 15;11(492):. (PMID: 31092696)
Immunity. 2017 Apr 18;46(4):649-659. (PMID: 28410991)
Bioact Mater. 2022 Feb 05;18:15-25. (PMID: 35387160)
Nat Commun. 2015 Oct 23;6:8715. (PMID: 26493500)
Nature. 2016 Aug 11;536(7615):238. (PMID: 27120161)
Signal Transduct Target Ther. 2022 Sep 27;7(1):336. (PMID: 36167824)
Bioact Mater. 2021 Oct 26;12:327-339. (PMID: 35128180)
J Neurosci. 2005 Nov 2;25(44):10167-79. (PMID: 16267224)
J Leukoc Biol. 2011 Oct;90(4):751-9. (PMID: 21724807)

82230071 National Natural Science Foundation of China; 92249303 Integrated Project of Major Research Plan of National Natural Science Foundation of China; 23141900600 Shanghai Committee of Science and Technology Laboratory Animal Research Project; BK20241808 Jiangsu Province Natural Science Foundation project

Keywords: Disease treatment; Engineering modification; Extracellular vesicles; Organoids; Organoids extracellular vesicles

Date Created: 20241107 Date Completed: 20241107 Latest Revision: 20241109

20241112

PMC11542470

10.1186/s12951-024-02917-3

39506799