Human embryonic lung epithelial tips are multipotent progenitors that can be expanded in vitro as long-term self-renewing organoids

eLife

Volumn 6, Issue , 2017, Pages

  Nikolić, Marko Z ^a   Caritg, Oriol ^a   Jeng, Quitz ^a   Johnson, Jo Anne ^a   Sun, Dawei ^a   Howell, Kate J ^b,c   Brady, Jane L ^a   Laresgoiti, Usua ^a   Allen, George ^a   Butler, Richard ^a   Zilbauer, Matthias ^b   Giangreco, Adam ^d,f   Rawlins, Emma L ^a,b,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c EUROPEAN BIOINFORMATICS INSTITUTE   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e University of Cambridge   (United Kingdom)

^f Technology Partnership   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; CYTOPLASM; DIFFERENTIATION; EMBRYO; FETUS LUNG; GENE EXPRESSION; IN VITRO STUDY; LUNG DEVELOPMENT; LUNG EPITHELIUM; MORPHOLOGY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; SIGNAL TRANSDUCTION; ANIMAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; LUNG; ORGANOID; PHYSIOLOGY; RESPIRATORY MUCOSA; STEM CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; LUNG; MICE; ORGANOIDS; RESPIRATORY MUCOSA; STEM CELLS;

EID: 85029219467     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.26575     Document Type: Article

References (74)

1. Al Alam D, El Agha E, Sakurai R, Kheirollahi V, Moiseenko A, Danopoulos S, Shrestha A, Schmoldt C, Quantius J, Herold S, Chao CM, Tiozzo C, De Langhe S, Plikus MV, Thornton M, Grubbs B, Minoo P, Rehan VK, Bellusci S. 2015. Evidence for the involvement of fibroblast growth factor 10 in lipofibroblast formation during embryonic lung development. Development 142:4139-4150. doi: 10.1242/dev.109173
2. Alanis DM, Chang DR, Akiyama H, Krasnow MA, Chen J. 2014. Two nested developmental waves demarcate a compartment boundary in the mouse lung. Nature Communications 5:3923. doi: 10.1038/ncomms4923
3. Alescio T, Cassini A. 1962. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. Journal of Experimental Zoology 150:83-94. doi: 10.1002/jez.1401500202
4. Barkauskas CE, Cronce MJ, Rackley CR, Bowie EJ, Keene DR, Stripp BR, Randell SH, Noble PW, Hogan BL. 2013. Type 2 alveolar cells are stem cells in adult lung. Journal of Clinical Investigation 123:3025-3036. doi: 10.1172/JCI68782
5. Bellusci S, Henderson R, Winnier G, Oikawa T, Hogan BL. 1996. Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development 122:1693-1702.
6. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BL. 1997. Involvement of sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 124:53-63.
7. Benlhabib H, Guo W, Pierce BM, Mendelson CR. 2015. The miR-200 family and its targets regulate type II cell differentiation in human fetal lung. Journal of Biological Chemistry 290:22409-22422. doi: 10.1074/jbc.M114.636068
8. Bernstein BE, Stamatoyannopoulos JA, Costello JF, Ren B, Milosavljevic A, Meissner A, Kellis M, Marra MA, Beaudet AL, Ecker JR, Farnham PJ, Hirst M, Lander ES, Mikkelsen TS, Thomson JA. 2010. The NIH roadmap epigenomics mapping consortium. Nature Biotechnology 28:1045-1048. doi: 10.1038/nbt1010-1045
9. Breiteneder-Geleff S, Soleiman A, Kowalski H, Horvat R, Amann G, Kriehuber E, Diem K, Weninger W, Tschachler E, Alitalo K, Kerjaschki D. 1999. Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. The American Journal of Pathology 154:385-394. doi: 10.1016/S0002-9440(10)65285-6
10. Burri PH. 1984. Fetal and postnatal development of the lung. Annual Review of Physiology 46:617-628. doi: 10.1146/annurev.ph.46.030184.003153
11. Chang DR, Martinez Alanis D, Miller RK, Ji H, Akiyama H, McCrea PD, Chen J. 2013. Lung epithelial branching program antagonizes alveolar differentiation. PNAS 110:18042-18051. doi: 10.1073/pnas.1311760110
12. Dekkers JF, Wiegerinck CL, de Jonge HR, Bronsveld I, Janssens HM, de Winter-de Groot KM, Brandsma AM, de Jong NW, Bijvelds MJ, Scholte BJ, Nieuwenhuis EE, van den Brink S, Clevers H, van der Ent CK, Middendorp S, Beekman JM. 2013. A functional CFTR assay using primary cystic fibrosis intestinal organoids. Nature Medicine 19:939-945. doi: 10.1038/nm.3201
13. Desai TJ, Brownfield DG, Krasnow MA. 2014. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 507:190-194. doi: 10.1038/nature12930
14. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S, et al. 2011. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biology 9:e1000582. doi: 10.1371/journal.pbio.1000582
15. Dobbs LG, Gonzalez RF, Allen L, Froh DK. 1999. HTI56, an integral membrane protein specific to human alveolar type I cells. Journal of Histochemistry and Cytochemistry 47:129-137. doi: 10.1177/002215549904700202
16. Dye BR, Miller AJ, Spence JR. 2016. How to grow a lung: applying principles of developmental biology to generate lung lineages from human pluripotent stem cells. Current Pathobiology Reports 4:47-57. doi: 10.1007/s40139-016-0102-x
17. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U, Tenge VR, Neill FH, Blutt SE, Zeng XL, Qu L, Kou B, Opekun AR, Burrin D, Graham DY, Ramani S, Atmar RL, Estes MK. 2016. Replication of human noroviruses in stem cell-derived human enteroids. Science 353:1387-1393. doi: 10.1126/science.aaf5211
18. Farr A, Nelson A, Hosier S. 1992. Characterization of an antigenic determinant preferentially expressed by type I epithelial cells in the murine Thymus. Journal of Histochemistry and Cytochemistry 40:651-664. doi: 10.1177/40.5.1374092
19. Feng L, Wang J, Cao B, Zhang Y, Wu B, Di X, Jiang W, An N, Lu D, Gao S, Zhao Y, Chen Z, Mao Y, Gao Y, Zhou D, Jen J, Liu X, Zhang Y, Li X, Zhang K, et al. 2014. Gene expression profiling in human lung development: an abundant resource for lung adenocarcinoma prognosis. PLoS One 9:e105639. doi: 10.1371/journal.pone.0105639
20. Fujii M, Matano M, Nanki K, Sato T. 2015. Efficient genetic engineering of human intestinal organoids using electroporation. Nature Protocols 10:1474-1485. doi: 10.1038/nprot.2015.088
21. Gonzales LW, Gonzalez R, Barrette AM, Wang P, Dobbs L, Ballard PL. 2015. Expression of Carcinoembryonic Cell adhesion molecule 6 and alveolar epithelial cell markers in lungs of human infants with chronic lungdisease. Journal of Histochemistry and Cytochemistry 63:908-921. doi: 10.1369/0022155415603768
22. Gonzalez AM, Hill DJ, Logan A, Maher PA, Baird A. 1996. Distribution of fibroblast growth factor (FGF)-2 and FGF receptor-1 messenger RNA expression and protein presence in the mid-trimester human fetus. Pediatric Research 39:375-385. doi: 10.1203/00006450-199603000-00001
23. Gonzalez RF, Allen L, Gonzales L, Ballard PL, Dobbs LG. 2010. HTII-280, a biomarker specific to the apical plasma membrane of human lung alveolar type II cells. Journal of Histochemistry and Cytochemistry 58:891-901. doi: 10.1369/jhc.2010.956433
24. Guha A, Vasconcelos M, Cai Y, Yoneda M, Hinds A, Qian J, Li G, Dickel L, Johnson JE, Kimura S, Guo J, McMahon J, McMahon AP, Cardoso WV. 2012. Neuroepithelial body microenvironment is a niche for a distinct subset of Clara-like precursors in the developing airways. PNAS 109:12592-12597. doi: 10.1073/pnas.1204710109
25. Haitchi HM, Bassett DJ, Bucchieri F, Gao X, Powell RM, Hanley NA, Wilson DI, Holgate ST, Davies DE. 2009. Induction of a disintegrin and metalloprotease 33 during embryonic lung development and the influence of IL-13 or maternal allergy. Journal of Allergy and Clinical Immunology 124597:590e591-597. doi: 10.1016/j.jaci.2009.06.026
26. Herriges JC, Yi L, Hines EA, Harvey JF, Xu G, Gray PA, Ma Q, Sun X. 2012. Genome-scale study of transcription factor expression in the branching mouse lung. Developmental Dynamics 241:1432-1453. doi: 10.1002/dvdy.23823
27. Hrycaj SM, Dye BR, Baker NC, Larsen BM, Burke AC, Spence JR, Wellik DM. 2015. Hox5 genes regulate the Wnt2/2b-Bmp4-signaling axis during lung development. Cell Reports 12:903-912. doi: 10.1016/j.celrep.2015.07.02
28. Huang da W, Sherman BT, Lempicki RA. 2009a. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Research 37:1-13. doi: 10.1093/nar/gkn923
29. Huang daW, Sherman BT, Lempicki RA. 2009b. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols 4:44-57. doi: 10.1038/nprot.2008.211
30. Huch M, Dorrell C, Boj SF, van Es JH, Li VS, van de Wetering M, Sato T, Hamer K, Sasaki N, Finegold MJ, Haft A, Vries RG, Grompe M, Clevers H. 2013a. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 494:247-250. doi: 10.1038/nature11826
31. Huch M, Bonfanti P, Boj SF, Sato T, Loomans CJ, van de Wetering M, Sojoodi M, Li VS, Schuijers J, Gracanin A, Ringnalda F, Begthel H, Hamer K, Mulder J, van Es JH, de Koning E, Vries RG, Heimberg H, Clevers H, Fau BP, et al. 2013b. Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin Axis. The EMBO Journal 32:2708-2721. doi: 10.1038/emboj.2013.204
32. Huch M, Gehart H, van Boxtel R, Hamer K, Blokzijl F, Verstegen MM, Ellis E, van Wenum M, Fuchs SA, de Ligt J, van de Wetering M, Sasaki N, Boers SJ, Kemperman H, de Jonge J, Ijzermans JN, Nieuwenhuis EE, Hoekstra R, Strom S, Vries RR, et al. 2015. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 160:299-312. doi: 10.1016/j.cell.2014.11.050
33. Huch M, Koo BK. 2015. Modeling mouse and human development using organoid cultures. Development 142: 3113-3125. doi: 10.1242/dev.118570
34. Ishikawa F, Yasukawa M, Lyons B, Yoshida S, Miyamoto T, Yoshimoto G, Watanabe T, Akashi K, Shultz LD, Harada M. 2005. Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 106:1565-1573. doi: 10.1182/blood-2005-02-0516
35. Ito T, Udaka N, Yazawa T, Okudela K, Hayashi H, Sudo T, Guillemot F, Kageyama R, Kitamura H. 2000. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 127:3913-3921
36. Jain R, Barkauskas CE, Takeda N, Bowie EJ, Aghajanian H, Wang Q, Padmanabhan A, Manderfield LJ, Gupta M, Li D, Li L, Trivedi CM, Hogan BL, Epstein JA. 2015. Plasticity of hopx(+) type I alveolar cells to regenerate type II cells in the lung. Nature Communications 6:6727. doi: 10.1038/ncomms7727
37. Jia S, Wildner H, Birchmeier C. 2015. Insm1 controls the differentiation of pulmonary neuroendocrine cells by repressing Hes1. Developmental Biology 408:90-98. doi: 10.1016/j.ydbio.2015.10.009
38. Kho AT, Bhattacharya S, Tantisira KG, Carey VJ, Gaedigk R, Leeder JS, Kohane IS, Weiss ST, Mariani TJ. 2010. Transcriptomic analysis of human lung development. American Journal of Respiratory and Critical Care Medicine 181:54-63. doi: 10.1164/rccm.200907-1063OC
39. Kho AT, Chhabra D, Sharma S, Qiu W, Carey VJ, Gaedigk R, Vyhlidal CA, Leeder JS, Tantisira KG, Weiss ST. 2016. Age, Sexual Dimorphism, and disease associations in the developing human fetal lung transcriptome. American Journal of Respiratory Cell and Molecular Biology 54:814-821. doi: 10.1165/rcmb.2015-0326OC
40. Khoor A, Gray ME, Hull WM, Whitsett JA, Stahlman MT. 1993. Developmental expression of SP-A and SP-A mRNA in the proximal and distal respiratory epithelium in the human fetus and newborn. Journal of Histochemistry and Cytochemistry 41:1311-1319. doi: 10.1177/41.9.8354874
41. Khoor A, Stahlman MT, Gray ME, Whitsett JA. 1994. Temporal-spatial distribution of SP-B and SP-C proteins and mRNAs in developing respiratory epithelium of human lung. Journal of Histochemistry and Cytochemistry 42: 1187-1199. doi: 10.1177/42.9.8064126
42. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14:R36. doi: 10.1186/gb-2013-14-4-r36
43. Lan MS, Breslin MB. 2009. Structure, expression, and biological function of INSM1 transcription factor in neuroendocrine differentiation. The FASEB Journal 23:2024-2033. doi: 10.1096/fj.08-125971
44. Laresgoiti U, Nikolic´ MZ, Rao C, Brady JL, Richardson RV, Batchen EJ, Chapman KE, Rawlins EL. 2016. Lung epithelial tip progenitors integrate glucocorticoid- and STAT3-mediated signals to control progeny fate. Development 143:3686-3699. doi: 10.1242/dev.134023
45. Lazzaro D, Price M, de Felice M, Di Lauro R. 1991. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093-1104.
46. Liebler JM, Marconett CN, Juul N, Wang H, Liu Y, Flodby P, Laird-Offringa IA, Minoo P, Zhou B. 2016. Combinations of differentiation markers distinguish subpopulations of alveolar epithelial cells in adult lung. American Journal of Physiology - Lung Cellular and Molecular Physiology 310:L114-L120. doi: 10.1152/ajplung.00337.2015
47. Mahoney JE, Mori M, Szymaniak AD, Varelas X, Cardoso WV. 2014. The hippo pathway effector yap controls patterning and differentiation of airway epithelial progenitors. Developmental Cell 30:137-150. doi: 10.1016/j.devcel.2014.06.003
48. Merkle FT, Eggan K. 2013. Modeling human disease with pluripotent stem cells: from genome association to function. Cell Stem Cell 12:656-668. doi: 10.1016/j.stem.2013.05.016
49. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007. A global double-fluorescent cre reporter mouse. Genesis 45:593-605. doi: 10.1002/dvg.20335
50. Okubo T, Knoepfler PS, Eisenman RN, Hogan BL. 2005. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development 132:1363-1374. doi: 10.1242/dev.01678
51. Oulton M, Martin TR, Faulkner GT, Stinson D, Johnson JP. 1980. Developmental study of a lamellar body fraction isolated from human amniotic fluid. Pediatric Research 14:722-728. doi: 10.1203/00006450-198005000-00004
52. Plopper CG, Nishio SJ, Alley JL, Kass P, Hyde DM. 1992. The role of the nonciliated bronchiolar epithelial (Clara) cell as the progenitor cell during bronchiolar epithelial differentiation in the perinatal rabbit lung. American Journal of Respiratory Cell and Molecular Biology 7:606-613. doi: 10.1165/ajrcmb/7.6.606
53. Rackley CR, Stripp BR. 2012. Building and maintaining the epithelium of the lung. Journal of Clinical Investigation 122:2724-2730. doi: 10.1172/JCI60519
54. Rajatapiti P, de Rooij JD, Beurskens LW, Keijzer R, Tibboel D, Rottier RJ, de Krijger RR. 2010. Effect of oxygen on the expression of hypoxia-inducible factors in human fetal lung explants. Neonatology 97:346-354. doi: 10.1159/000261018
55. Rawlins EL, Clark CP, Xue Y, Hogan BL. 2009. The Id2+ distal tip lung epithelium contains individual multipotent embryonic progenitor cells. Development 136:3741-3745. doi: 10.1242/dev.037317
56. Risso D, Ngai J, Speed TP, Dudoit S. 2014. Normalization of RNA-seq data using factor analysis of control genes or samples. Nature Biotechnology 32:896-902. doi: 10.1038/nbt.2931
57. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. doi: 10.1093/bioinformatics/btp616
58. Rock JR, Onaitis MW, Rawlins EL, Lu Y, Clark CP, Xue Y, Randell SH, Hogan BL. 2009. Basal cells as stem cells of the mouse trachea and human airway epithelium. PNAS 106:12771-12775. doi: 10.1073/pnas.0906850106
59. Rockich BE, Hrycaj SM, Shih HP, Nagy MS, Ferguson MA, Kopp JL, Sander M, Wellik DM, Spence JR. 2013. Sox9 plays multiple roles in the lung epithelium during branching morphogenesis. PNAS 110:E4456-E4464. doi: 10.1073/pnas.1311847110
60. 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. doi: 10.1038/nature07935
61. Sheridan JM, Taoudi S, Medvinsky A, Blackburn CC. 2009. A novel method for the generation of reaggregated organotypic cultures that permits juxtaposition of defined cell populations. Genesis 47:346-351. doi: 10.1002/dvg.20505
62. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J, Greiner DL, Handgretinger R. 2005. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. The Journal of Immunology 174:6477-6489. doi: 10.4049/jimmunol.174.10.6477
63. Singh I, Mehta A, Contreras A, Boettger T, Carraro G, Wheeler M, Cabrera-Fuentes HA, Bellusci S, Seeger W, Braun T, Barreto G. 2014. Hmga2 is required for canonical WNT signaling during lung development. BMC Biology 12:21. doi: 10.1186/1741-7007-12-21
64. Stahlman MT, Besnard V, Wert SE, Weaver TE, Dingle S, Xu Y, von Zychlin K, Olson SJ, Whitsett JA. 2007. Expression of ABCA3 in developing lung and other tissues. Journal of Histochemistry and Cytochemistry 55: 71-83. doi: 10.1369/jhc.6A6962.2006
65. Swarr DT, Morrisey EE. 2015. Lung endoderm morphogenesis: gasping for form and function. Annual Review of Cell and Developmental Biology 31:553-573. doi: 10.1146/annurev-cellbio-100814-125249
66. Toskala E, Smiley-Jewell SM, Wong VJ, King D, Plopper CG. 2005. Temporal and spatial distribution of ciliogenesis in the tracheobronchial airways of mice. AJP: Lung Cellular and Molecular Physiology 289:L454-L459. doi: 10.1152/ajplung.00036.2005
67. Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL, Espinoza FH, Desai TJ, Krasnow MA, Quake SR. 2014. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 509: 371-375. doi: 10.1038/nature13173
68. Volckaert T, Campbell A, Dill E, Li C, Minoo P, De Langhe S. 2013. Localized Fgf10 expression is not required for lung branching morphogenesis but prevents differentiation of epithelial progenitors. Development 140:3731-3742. doi: 10.1242/dev.096560
69. Volckaert T, De Langhe SP. 2015. Wnt and FGF mediated epithelial-mesenchymal crosstalk during lung development. Developmental Dynamics 244:342-366. doi: 10.1002/dvdy.24234
70. Wang Y, Tian Y, Morley MP, Lu MM, Demayo FJ, Olson EN, Morrisey EE. 2013. Development and regeneration of Sox2+ endoderm progenitors are regulated by a Hdac1/2-Bmp4/Rb1 regulatory pathway. Developmental Cell 24:345-358. doi: 10.1016/j.devcel.2013.01.012
71. Wuenschell CW, Sunday ME, Singh G, Minoo P, Slavkin HC, Warburton D. 1996. Embryonic mouse lung epithelial progenitor cells co-express immunohistochemical markers of diverse mature cell lineages. Journal of Histochemistry and Cytochemistry 44:113-123. doi: 10.1177/44.2.8609367
72. Yin X, Farin HF, van Es JH, Clevers H, Langer R, Karp JM. 2014. Niche-independent high-purity cultures of Lgr5+intestinal stem cells and their progeny. Nature Methods 11:106-112. doi: 10.1038/nmeth.2737
73. Zhang Y, Goss AM, Cohen ED, Kadzik R, Lepore JJ, Muthukumaraswamy K, Yang J, DeMayo FJ, Whitsett JA, Parmacek MS, Morrisey EE. 2008. A Gata6-Wnt pathway required for epithelial stem cell development and airway regeneration. Nature Genetics 40:862-870. doi: 10.1038/ng.157
74. Zhang M, Shi J, Huang Y, Lai L. 2012. Expression of canonical WNT/b-CATENIN signaling components in the developing human lung. BMC Developmental Biology 12:21. doi: 10.1186/1471-213X-12-21