Current Organoid Culture Systems in Pancreatic Cancer

References

1. Wang F Ma J Racial disparities in clinical features and survival outcomes among patients with pancreatic neuroendocrine tumor: A contemporary SEER database analysis. Oncologie 2022 24 4 865 895 10.32604/oncologie.2022.025447
   [Google Scholar]
2. Siegel R.L. Giaquinto A.N. Jemal A. Cancer statistics, 2024. CA Cancer J. Clin. 2024 74 1 12 49 10.3322/caac.21820 38230766
   [Google Scholar]
3. Abbruzzese J.L. Hess K.R. New option for the initial management of metastatic pancreatic cancer? J. Clin. Oncol. 2014 32 23 2405 2407 10.1200/JCO.2013.54.4155 24982449
   [Google Scholar]
4. Khorana A.A. Mangu P.B. Berlin J. Engebretson A. Hong T.S. Maitra A. Mohile S.G. Mumber M. Schulick R. Shapiro M. Urba S. Zeh H.J. Katz M.H.G. Potentially curable pancreatic cancer: American society of clinical oncology clinical practice guideline. J. Clin. Oncol. 2016 34 21 2541 2556 10.1200/JCO.2016.67.5553 27247221
   [Google Scholar]
5. Kleeff J. Korc M. Apte M. La Vecchia C. Johnson C.D. Biankin A.V. Neale R.E. Tempero M. Tuveson D.A. Hruban R.H. Neoptolemos J.P. Pancreatic cancer. Nat. Rev. Dis. Primers 2016 2 1 16022 10.1038/nrdp.2016.22 27158978
   [Google Scholar]
6. Binnewies M. Roberts E.W. Kersten K. Chan V. Fearon D.F. Merad M. Coussens L.M. Gabrilovich D.I. Ostrand-Rosenberg S. Hedrick C.C. Vonderheide R.H. Pittet M.J. Jain R.K. Zou W. Howcroft T.K. Woodhouse E.C. Weinberg R.A. Krummel M.F. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med. 2018 24 5 541 550 10.1038/s41591‑018‑0014‑x 29686425
   [Google Scholar]
7. Gerlinger M. Rowan A.J. Horswell S. Larkin J. Endesfelder D. Gronroos E. Martinez P. Matthews N. Stewart A. Tarpey P. Varela I. Phillimore B. Begum S. McDonald N.Q. Butler A. Jones D. Raine K. Latimer C. Santos C.R. Nohadani M. Eklund A.C. Spencer-Dene B. Clark G. Pickering L. Stamp G. Gore M. Szallasi Z. Downward J. Futreal P.A. Swanton C. Swanton C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012 366 10 883 892 10.1056/NEJMoa1113205 22397650
   [Google Scholar]
8. Biankin A.V. Waddell N. Kassahn K.S. Gingras M.C. Muthuswamy L.B. Johns A.L. Miller D.K. Wilson P.J. Patch A.M. Wu J. Chang D.K. Cowley M.J. Gardiner B.B. Song S. Harliwong I. Idrisoglu S. Nourse C. Nourbakhsh E. Manning S. Wani S. Gongora M. Pajic M. Scarlett C.J. Gill A.J. Pinho A.V. Rooman I. Anderson M. Holmes O. Leonard C. Taylor D. Wood S. Xu Q. Nones K. Lynn Fink J. Christ A. Bruxner T. Cloonan N. Kolle G. Newell F. Pinese M. Scott Mead R. Humphris J.L. Kaplan W. Jones M.D. Colvin E.K. Nagrial A.M. Humphrey E.S. Chou A. Chin V.T. Chantrill L.A. Mawson A. Samra J.S. Kench J.G. Lovell J.A. Daly R.J. Merrett N.D. Toon C. Epari K. Nguyen N.Q. Barbour A. Zeps N. Kakkar N. Zhao F. Qing Wu Y. Wang M. Muzny D.M. Fisher W.E. Charles Brunicardi F. Hodges S.E. Reid J.G. Drummond J. Chang K. Han Y. Lewis L.R. Dinh H. Buhay C.J. Beck T. Timms L. Sam M. Begley K. Brown A. Pai D. Panchal A. Buchner N. De Borja R. Denroche R.E. Yung C.K. Serra S. Onetto N. Mukhopadhyay D. Tsao M.S. Shaw P.A. Petersen G.M. Gallinger S. Hruban R.H. Maitra A. Iacobuzio-Donahue C.A. Schulick R.D. Wolfgang C.L. Morgan R.A. Lawlor R.T. Capelli P. Corbo V. Scardoni M. Tortora G. Tempero M.A. Mann K.M. Jenkins N.A. Perez-Mancera P.A. Adams D.J. Largaespada D.A. Wessels L.F.A. Rust A.G. Stein L.D. Tuveson D.A. Copeland N.G. Musgrove E.A. Scarpa A. Eshleman J.R. Hudson T.J. Sutherland R.L. Wheeler D.A. Pearson J.V. McPherson J.D. Gibbs R.A. Grimmond S.M. Australian Pancreatic Cancer Genome Initiative Pancreatic cancer genomes reveal aberrations in axon guidance pathway genes. Nature 2012 491 7424 399 405 10.1038/nature11547 23103869
   [Google Scholar]
9. Klemm F. Joyce J.A. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol. 2015 25 4 198 213 10.1016/j.tcb.2014.11.006 25540894
   [Google Scholar]
10. Elyada E. Bolisetty M. Laise P. Flynn W.F. Courtois E.T. Burkhart R.A. Teinor J.A. Belleau P. Biffi G. Lucito M.S. Sivajothi S. Armstrong T.D. Engle D.D. Yu K.H. Hao Y. Wolfgang C.L. Park Y. Preall J. Jaffee E.M. Califano A. Robson P. Tuveson D.A. Cross-species single-cell analysis of pancreatic ductal adenocarcinoma reveals antigen-presenting cancer-associated fibroblasts. Cancer Discov. 2019 9 8 1102 1123 10.1158/2159‑8290.CD‑19‑0094 31197017
    [Google Scholar]
11. Huang H. Wang Z. Zhang Y. Pradhan R.N. Ganguly D. Chandra R. Murimwa G. Wright S. Gu X. Maddipati R. Müller S. Turley S.J. Brekken R.A. Mesothelial cell-derived antigen-presenting cancer-associated fibroblasts induce expansion of regulatory T cells in pancreatic cancer. Cancer Cell 2022 40 6 656 673.e7 35523176
    [Google Scholar]
12. Krishnamurty A.T. Shyer J.A. Thai M. Gandham V. Buechler M.B. Yang Y.A. Pradhan R.N. Wang A.W. Sanchez P.L. Qu Y. Breart B. Chalouni C. Dunlap D. Ziai J. Elstrott J. Zacharias N. Mao W. Rowntree R.K. Sadowsky J. Lewis G.D. Pillow T.H. Nabet B.Y. Banchereau R. Tam L. Caothien R. Bacarro N. Roose-Girma M. Modrusan Z. Mariathasan S. Müller S. Turley S.J. LRRC15+ myofibroblasts dictate the stromal setpoint to suppress tumour immunity. Nature 2022 611 7934 148 154 36171287
    [Google Scholar]
13. McAndrews K.M. Chen Y. Darpolor J.K. Zheng X. Yang S. Carstens J.L. Li B. Wang H. Miyake T. Correa de Sampaio P. Kirtley M.L. Natale M. Wu C.C. Sugimoto H. LeBleu V.S. Kalluri R. Identification of functional heterogeneity of carcinoma-associated fibroblasts with distinct IL6-mediated therapy resistance in pancreatic cancer. Cancer Discov. 2022 12 6 1580 1597 35348629
    [Google Scholar]
14. Ireland L. Santos A. Ahmed M.S. Rainer C. Nielsen S.R. Quaranta V. Weyer-Czernilofsky U. Engle D.D. Perez-Mancera P.A. Coupland S.E. Taktak A. Bogenrieder T. Tuveson D.A. Campbell F. Schmid M.C. Mielgo A. Chemoresistance in pancreatic cancer is driven by stroma-derived insulin-like growth factors. Cancer Res. 2016 76 23 6851 6863 27742686
    [Google Scholar]
15. Hesler R.A. Huang J.J. Starr M.D. Treboschi V.M. Bernanke A.G. Nixon A.B. McCall S.J. White R.R. Blobe G.C. TGF-β-induced stromal CYR61 promotes resistance to gemcitabine in pancreatic ductal adenocarcinoma through downregulation of the nucleoside transporters hENT1 and hCNT3. Carcinogenesis 2016 37 11 1041 1051 10.1093/carcin/bgw093 27604902
    [Google Scholar]
16. Richards K.E. Zeleniak A.E. Fishel M.L. Wu J. Littlepage L.E. Hill R. Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene 2017 36 13 1770 1778 10.1038/onc.2016.353 27669441
    [Google Scholar]
17. Villarroel M.C. Rajeshkumar N.V. Garrido-Laguna I. De Jesus-Acosta A. Jones S. Maitra A. Hruban R.H. Eshleman J.R. Klein A. Laheru D. Donehower R. Hidalgo M. Personalizing cancer treatment in the age of global genomic analyses: PALB2 gene mutations and the response to DNA damaging agents in pancreatic cancer. Mol. Cancer Ther. 2011 10 1 3 8 21135251
    [Google Scholar]
18. Almeqdadi M. Mana M.D. Roper J. Yilmaz Ö.H. Gut organoids: Mini-tissues in culture to study intestinal physiology and disease. Am. J. Physiol. Cell Physiol. 2019 317 3 C405 C419 31216420
    [Google Scholar]
19. Rossi G. Manfrin A. Lutolf M.P. Progress and potential in organoid research. Nat. Rev. Genet. 2018 19 11 671 687 30228295
    [Google Scholar]
20. Friedl P. Locker J. Sahai E. Segall J.E. Classifying collective cancer cell invasion. Nat. Cell Biol. 2012 14 8 777 783 10.1038/ncb2548 22854810
    [Google Scholar]
21. Huang W. Navarro-Serer B. Jeong Y.J. Chianchiano P. Xia L. Luchini C. Veronese N. Dowiak C. Ng T. Trujillo M.A. Huang B. Pflüger M.J. Macgregor-Das A.M. Lionheart G. Jones D. Fujikura K. Nguyen-Ngoc K.V. Neumann N.M. Groot V.P. Hasanain A. van Oosten A.F. Fischer S.E. Gallinger S. Singhi A.D. Zureikat A.H. Brand R.E. Gaida M.M. Heinrich S. Burkhart R.A. He J. Wolfgang C.L. Goggins M.G. Thompson E.D. Roberts N.J. Ewald A.J. Wood L.D. Pattern of invasion in human pancreatic cancer organoids is associated with loss of smad4 and clinical outcome. Cancer Res. 2020 80 13 2804 2817 10.1158/0008‑5472.CAN‑19‑1523 32376602
    [Google Scholar]
22. Boj S.F. Hwang C.I. Baker L.A. Chio I.I.C. Engle D.D. Corbo V. Jager M. Ponz-Sarvise M. Tiriac H. Spector M.S. Gracanin A. Oni T. Yu K.H. van Boxtel R. Huch M. Rivera K.D. Wilson J.P. Feigin M.E. Öhlund D. Handly-Santana A. Ardito-Abraham C.M. Ludwig M. Elyada E. Alagesan B. Biffi G. Yordanov G.N. Delcuze B. Creighton B. Wright K. Park Y. Morsink F.H.M. Molenaar I.Q. Borel Rinkes I.H. Cuppen E. Hao Y. Jin Y. Nijman I.J. Iacobuzio-Donahue C. Leach S.D. Pappin D.J. Hammell M. Klimstra D.S. Basturk O. Hruban R.H. Offerhaus G.J. Vries R.G.J. Clevers H. Tuveson D.A. Organoid models of human and mouse ductal pancreatic cancer. Cell 2015 160 1-2 324 338 10.1016/j.cell.2014.12.021 25557080
    [Google Scholar]
23. Wood L.D. Ewald A.J. Organoids in cancer research: A review for pathologist‐scientists. J. Pathol. 2021 254 4 395 404 10.1002/path.5684 33886125
    [Google Scholar]
24. Xu H. Lyu X. Yi M. Zhao W. Song Y. Wu K. Organoid technology and applications in cancer research. J. Hematol. Oncol. 2018 11 1 116 10.1186/s13045‑018‑0662‑9 30219074
    [Google Scholar]
25. Ren X. Chen W. Yang Q. Li X. Xu L. Patient‐derived cancer organoids for drug screening: Basic technology and clinical application. J. Gastroenterol. Hepatol. 2022 37 8 1446 1454 10.1111/jgh.15930 35771719
    [Google Scholar]
26. Ballard D.H. Boyer C.J. Alexander J.S. Organoids — preclinical models of human disease. N. Engl. J. Med. 2019 380 20 1981 1982 10.1056/NEJMc1903253 31091396
    [Google Scholar]
27. Nakano T. Ando S. Takata N. Kawada M. Muguruma K. Sekiguchi K. Saito K. Yonemura S. Eiraku M. Sasai Y. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012 10 6 771 785 10.1016/j.stem.2012.05.009 22704518
    [Google Scholar]
28. Crespo M. Vilar E. Tsai S.Y. Chang K. Amin S. Srinivasan T. Zhang T. Pipalia N.H. Chen H.J. Witherspoon M. Gordillo M. Xiang J.Z. Maxfield F.R. Lipkin S. Evans T. Chen S. Colonic organoids derived from human induced pluripotent stem cells for modeling colorectal cancer and drug testing. Nat. Med. 2017 23 7 878 884 10.1038/nm.4355 28628110
    [Google Scholar]
29. Tiriac H. Belleau P. Engle D.D. Plenker D. Deschênes A. Somerville T.D.D. Froeling F.E.M. Burkhart R.A. Denroche R.E. Jang G.H. Miyabayashi K. Young C.M. Patel H. Ma M. LaComb J.F. Palmaira R.L.D. Javed A.A. Huynh J.C. Johnson M. Arora K. Robine N. Shah M. Sanghvi R. Goetz A.B. Lowder C.Y. Martello L. Driehuis E. LeComte N. Askan G. Iacobuzio-Donahue C.A. Clevers H. Wood L.D. Hruban R.H. Thompson E. Aguirre A.J. Wolpin B.M. Sasson A. Kim J. Wu M. Bucobo J.C. Allen P. Sejpal D.V. Nealon W. Sullivan J.D. Winter J.M. Gimotty P.A. Grem J.L. DiMaio D.J. Buscaglia J.M. Grandgenett P.M. Brody J.R. Hollingsworth M.A. O’Kane G.M. Notta F. Kim E. Crawford J.M. Devoe C. Ocean A. Wolfgang C.L. Yu K.H. Li E. Vakoc C.R. Hubert B. Fischer S.E. Wilson J.M. Moffitt R. Knox J. Krasnitz A. Gallinger S. Tuveson D.A. Organoid profiling identifies common responders to chemotherapy in pancreatic cancer. Cancer Discov. 2018 8 9 1112 1129 10.1158/2159‑8290.CD‑18‑0349 29853643
    [Google Scholar]
30. Scarpa A. Chang D.K. Nones K. Corbo V. Patch A.M. Bailey P. Lawlor R.T. Johns A.L. Miller D.K. Mafficini A. Rusev B. Scardoni M. Antonello D. Barbi S. Sikora K.O. Cingarlini S. Vicentini C. McKay S. Quinn M.C.J. Bruxner T.J.C. Christ A.N. Harliwong I. Idrisoglu S. McLean S. Nourse C. Nourbakhsh E. Wilson P.J. Anderson M.J. Fink J.L. Newell F. Waddell N. Holmes O. Kazakoff S.H. Leonard C. Wood S. Xu Q. Nagaraj S.H. Amato E. Dalai I. Bersani S. Cataldo I. Dei Tos A.P. Capelli P. Davì M.V. Landoni L. Malpaga A. Miotto M. Whitehall V.L.J. Leggett B.A. Harris J.L. Harris J. Jones M.D. Humphris J. Chantrill L.A. Chin V. Nagrial A.M. Pajic M. Scarlett C.J. Pinho A. Rooman I. Toon C. Wu J. Pinese M. Cowley M. Barbour A. Mawson A. Humphrey E.S. Colvin E.K. Chou A. Lovell J.A. Jamieson N.B. Duthie F. Gingras M.C. Fisher W.E. Dagg R.A. Lau L.M.S. Lee M. Pickett H.A. Reddel R.R. Samra J.S. Kench J.G. Merrett N.D. Epari K. Nguyen N.Q. Zeps N. Falconi M. Simbolo M. Butturini G. Van Buren G. Partelli S. Fassan M. Khanna K.K. Gill A.J. Wheeler D.A. Gibbs R.A. Musgrove E.A. Bassi C. Tortora G. Pederzoli P. Pearson J.V. Waddell N. Biankin A.V. Grimmond S.M. Australian Pancreatic Cancer Genome Initiative Whole-genome landscape of pancreatic neuroendocrine tumours. Nature 2017 543 7643 65 71 10.1038/nature21063 28199314
    [Google Scholar]
31. Fan H. Demirci U. Chen P. Emerging organoid models: Leaping forward in cancer research. J. Hematol. Oncol. 2019 12 1 142 31884964
    [Google Scholar]
32. Balachandran V.P. Beatty G.L. Dougan S.K. Broadening the impact of immunotherapy to pancreatic cancer: Challenges and opportunities. Gastroenterology 2019 156 7 2056 2072 10.1053/j.gastro.2018.12.038 30660727
    [Google Scholar]
33. Simian M. Bissell M.J. Organoids: A historical perspective of thinking in three dimensions. J. Cell Biol. 2017 216 1 31 40 28031422
    [Google Scholar]
34. Gunti S. Hoke A.T.K. Vu K.P. London N.R. Jr Organoid and Spheroid Tumor Models: Techniques and Applications. Cancers 2021 13 4 874 10.3390/cancers13040874 33669619
    [Google Scholar]
35. Sato T. Stange D.E. Ferrante M. Vries R.G. Van Es J.H. Van den Brink S. Van Houdt W.J. Pronk A. Van Gorp J. Siersema P.D. Clevers H. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett’s epithelium. Gastroenterology 2011 141 5 1762 1772 10.1053/j.gastro.2011.07.050 21889923
    [Google Scholar]
36. Marsee A. Roos F.J.M. Verstegen M.M.A. Gehart H. de Koning E. Lemaigre F. Forbes S.J. Peng W.C. Huch M. Takebe T. Vallier L. Clevers H. van der Laan L.J.W. Spee B. Marsee A. Roos F. Verstegen M. Clevers H. Vallier L. Takebe T. Huch M. Peng W.C. Forbes S. Lemaigre F. de Koning E. Gehart H. van der Laan L. Spee B. Boj S. Baptista P. Schneeberger K. Soroka C. Heim M. Nuciforo S. Zaret K. Saito Y. Lutolf M. Cardinale V. Simons B. van IJzendoorn S. Kamiya A. Chikada H. Wang S. Mun S.J. Son M.J. Onder T.T. Boyer J. Sato T. Georgakopoulos N. Meneses A. Broutier L. Boulter L. Grün D. IJzermans J. Artegiani B. van Boxtel R. Kuijk E. Carpino G. Peltz G. Banales J. Man N. Aloia L. LaRusso N. George G. Rimland C. Yeoh G. Grappin-Botton A. Stange D. Prior N. Tirnitz-Parker J.E.E. Andersson E. Braconi C. Hannan N. Lu W-Y. Strom S. Sancho-Bru P. Ogawa S. Corbo V. Lancaster M. Hu H. Fuchs S. Hendriks D. HPB Organoid Consortium Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids. Cell Stem Cell 2021 28 5 816 832 10.1016/j.stem.2021.04.005 33961769
    [Google Scholar]
37. Zhou Q. Melton D.A. Pancreas regeneration. Nature 2018 557 7705 351 358 10.1038/s41586‑018‑0088‑0 29769672
    [Google Scholar]
38. Huch M. Bonfanti P. Boj S.F. Sato T. Loomans C.J.M. van de Wetering M. Sojoodi M. Li V.S.W. Schuijers J. Gracanin A. Ringnalda F. Begthel H. Hamer K. Mulder J. van Es J.H. de Koning E. Vries R.G.J. Heimberg H. Clevers H. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 2013 32 20 2708 2721 10.1038/emboj.2013.204 24045232
    [Google Scholar]
39. Casamitjana J. Espinet E. Rovira M. Pancreatic organoids for regenerative medicine and cancer research. Front. Cell Dev. Biol. 2022 10 886153 10.3389/fcell.2022.886153 35592251
    [Google Scholar]
40. Rezakhani S. Gjorevski N. Lutolf M.P. Extracellular matrix requirements for gastrointestinal organoid cultures. Biomaterials 2021 276 121020 10.1016/j.biomaterials.2021.121020 34280822
    [Google Scholar]
41. Li X. Nadauld L. Ootani A. Corney D.C. Pai R.K. Gevaert O. Cantrell M.A. Rack P.G. Neal J.T. Chan C.W.M. Yeung T. Gong X. Yuan J. Wilhelmy J. Robine S. Attardi L.D. Plevritis S.K. Hung K.E. Chen C.Z. Ji H.P. Kuo C.J. Oncogenic transformation of diverse gastrointestinal tissues in primary organoid culture. Nat. Med. 2014 20 7 769 777 10.1038/nm.3585 24859528
    [Google Scholar]
42. Ito F. Kato K. Yanatori I. Maeda Y. Murohara T. Toyokuni S. Matrigel-based organoid culture of malignant mesothelioma reproduces cisplatin sensitivity through CTR1. BMC Cancer 2023 23 1 487 10.1186/s12885‑023‑10966‑4 37254056
    [Google Scholar]
43. Rigamonti G. Veronesi F. Chiaradia E. Gosten-Heinrich P. Müller A. Brustenga L. de Angelis S. Tognoloni A. De Santo R. Klotz C. Lalle M. Selective activity of Tabebuia avellanedae against Giardia duodenalis infecting organoid-derived human gastrointestinal epithelia. Int. J. Parasitol. Drugs Drug Resist. 2025 27 100583 10.1016/j.ijpddr.2025.100583 39864282
    [Google Scholar]
44. Vlachogiannis G. Hedayat S. Vatsiou A. Jamin Y. Fernández-Mateos J. Khan K. Lampis A. Eason K. Huntingford I. Burke R. Rata M. Koh D.M. Tunariu N. Collins D. Hulkki-Wilson S. Ragulan C. Spiteri I. Moorcraft S.Y. Chau I. Rao S. Watkins D. Fotiadis N. Bali M. Darvish-Damavandi M. Lote H. Eltahir Z. Smyth E.C. Begum R. Clarke P.A. Hahne J.C. Dowsett M. de Bono J. Workman P. Sadanandam A. Fassan M. Sansom O.J. Eccles S. Starling N. Braconi C. Sottoriva A. Robinson S.P. Cunningham D. Valeri N. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science 2018 359 6378 920 926 10.1126/science.aao2774 29472484
    [Google Scholar]
45. Hennig A. Wolf L. Jahnke B. Polster H. Seidlitz T. Werner K. Aust D.E. Hampe J. Distler M. Weitz J. Stange D.E. Welsch T. CFTR expression analysis for subtyping of human pancreatic cancer organoids. Stem Cells Int. 2019 2019 1024614 31191661
    [Google Scholar]
46. Pagliuca F.W. Millman J.R. Gürtler M. Segel M. Van Dervort A. Ryu J.H. Peterson Q.P. Greiner D. Melton D.A. Generation of functional human pancreatic β cells in vitro. Cell 2014 159 2 428 439 10.1016/j.cell.2014.09.040 25303535
    [Google Scholar]
47. Nostro M.C. Sarangi F. Ogawa S. Holtzinger A. Corneo B. Li X. Micallef S.J. Park I.H. Basford C. Wheeler M.B. Daley G.Q. Elefanty A.G. Stanley E.G. Keller G. Stage-specific signaling through TGFβ family members and WNT regulates patterning and pancreatic specification of human pluripotent stem cells. Development 2011 138 5 861 871 10.1242/dev.055236 21270052
    [Google Scholar]
48. Nostro M.C. Sarangi F. Yang C. Holland A. Elefanty A.G. Stanley E.G. Greiner D.L. Keller G. Efficient generation of NKX6-1+ pancreatic progenitors from multiple human pluripotent stem cell lines. Stem Cell Reports 2015 4 4 591 604 10.1016/j.stemcr.2015.02.017 25843049
    [Google Scholar]
49. Huang L. Holtzinger A. Jagan I. BeGora M. Lohse I. Ngai N. Nostro C. Wang R. Muthuswamy L.B. Crawford H.C. Arrowsmith C. Kalloger S.E. Renouf D.J. Connor A.A. Cleary S. Schaeffer D.F. Roehrl M. Tsao M.S. Gallinger S. Keller G. Muthuswamy S.K. Ductal pancreatic cancer modeling and drug screening using human pluripotent stem cell– and patient-derived tumor organoids. Nat. Med. 2015 21 11 1364 1371 10.1038/nm.3973 26501191
    [Google Scholar]
50. Breunig M. Merkle J. Wagner M. Melzer M.K. Barth T.F.E. Engleitner T. Krumm J. Wiedenmann S. Cohrs C.M. Perkhofer L. Jain G. Krüger J. Hermann P.C. Schmid M. Madácsy T. Varga Á. Griger J. Azoitei N. Müller M. Wessely O. Robey P.G. Heller S. Dantes Z. Reichert M. Günes C. Bolenz C. Kuhn F. Maléth J. Speier S. Liebau S. Sipos B. Kuster B. Seufferlein T. Rad R. Meier M. Hohwieler M. Kleger A. Modeling plasticity and dysplasia of pancreatic ductal organoids derived from human pluripotent stem cells. Cell Stem Cell 2021 28 6 1105 1124.e19 10.1016/j.stem.2021.03.005 33915078
    [Google Scholar]
51. Rappaport S.M. Smith M.T. Epidemiology. Environment and disease risks. Science 2010 330 6003 460 461 10.1126/science.1192603 20966241
    [Google Scholar]
52. Komor A.C. Badran A.H. Liu D.R. CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 2017 169 3 559 10.1016/j.cell.2017.04.005 28431253
    [Google Scholar]
53. Clevers H. Modeling development and disease with organoids. Cell 2016 165 7 1586 1597 10.1016/j.cell.2016.05.082 27315476
    [Google Scholar]
54. Lee J. Snyder E.R. Liu Y. Gu X. Wang J. Flowers B.M. Kim Y.J. Park S. Szot G.L. Hruban R.H. Longacre T.A. Kim S.K. Reconstituting development of pancreatic intraepithelial neoplasia from primary human pancreas duct cells. Nat. Commun. 2017 8 1 14686 10.1038/ncomms14686 28272465
    [Google Scholar]
55. Seino T. Kawasaki S. Shimokawa M. Tamagawa H. Toshimitsu K. Fujii M. Ohta Y. Matano M. Nanki K. Kawasaki K. Takahashi S. Sugimoto S. Iwasaki E. Takagi J. Itoi T. Kitago M. Kitagawa Y. Kanai T. Sato T. Human pancreatic tumor organoids reveal loss of stem cell niche factor dependence during disease progression. Cell Stem Cell 2018 22 3 454 467.e6 10.1016/j.stem.2017.12.009 29337182
    [Google Scholar]
56. Go Y.H. Choi W.H. Bae W.J. Jung S.I. Cho C.H. Lee S.A. Park J.S. Ahn J.M. Kim S.W. Lee K.J. Lee D. Yoo J. Modeling pancreatic cancer with patient-derived organoids integrating cancer-associated fibroblasts. Cancers 2022 14 9 2077 10.3390/cancers14092077 35565206
    [Google Scholar]
57. Beelen N.A. Aberle M.R. Bruno V. Olde Damink S.W.M. Bos G.M.J. Rensen S.S. Wieten L. Antibody-dependent cellular cytotoxicity-inducing antibodies enhance the natural killer cell anti-cancer response against patient-derived pancreatic cancer organoids. Front. Immunol. 2023 14 1133796 10.3389/fimmu.2023.1133796 37520563
    [Google Scholar]
58. Schork N.J. Personalized medicine: Time for one-person trials. Nature 2015 520 7549 609 611 10.1038/520609a 25925459
    [Google Scholar]
59. Zhang D Fu S Clinical significance of CA-199 and LINC01197 in pancreatic cancer. Oncologie 2020 22 2 95 105 10.32604/oncologie.2020.012439
    [Google Scholar]
60. Collins D.C. Sundar R. Lim J.S.J. Yap T.A. Towards precision medicine in the clinic: From biomarker discovery to novel therapeutics. Trends Pharmacol. Sci. 2017 38 1 25 40 10.1016/j.tips.2016.10.012 27871777
    [Google Scholar]
61. Kim S. Min S. Choi Y.S. Jo S.H. Jung J.H. Han K. Kim J. An S. Ji Y.W. Kim Y.G. Cho S.W. Tissue extracellular matrix hydrogels as alternatives to Matrigel for culturing gastrointestinal organoids. Nat. Commun. 2022 13 1 1692 10.1038/s41467‑022‑29279‑4 35354790
    [Google Scholar]