Human lung spheroids as in Vitro niches of lung progenitor cells with distinctive paracrine and plasticity properties

Stem Cells Translational Medicine

Volumn 6, Issue 3, 2017, Pages 767-777

  Chimenti, Isotta ^a   Pagano, Francesca ^a   Angelini, Francesco ^a   Siciliano, Camilla ^a   Mangino, Giorgio ^a   Picchio, Vittorio ^a   De Falco, Elena ^a   Peruzzi, Mariangela ^a   Carnevale, Roberto ^a   Ibrahim, Mohsen ^a   Biondi Zoccai, Giuseppe ^a,b   Messina, Elisa ^c   Frati, Giacomo ^a,b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS NEUROMED   (Italy)

^c POLICLINICO UMBERTO I   (Italy)

Author keywords

Epithelial to mesenchymal transition; Lung stem cells; Pneumospheres; Stem cell niche; Three dimensional culture

Indexed keywords

FIBRONECTIN; GELATIN; LAMININ; VIMENTIN;

ADULT; ARTICLE; CELL PLASTICITY; CELL PROLIFERATION ASSAY; CELL TRANSDIFFERENTIATION; CLONOGENESIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOFLUOROMETRY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION ASSAY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IMMUNOPHENOTYPING; LUNG BIOPSY; LUNG PARENCHYMA; MALE; MESENCHYMAL STEM CELL; MICROENVIRONMENT; PARACRINE SIGNALING; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; RNA EXTRACTION; SIGNAL TRANSDUCTION; STEM CELL CULTURE; YOUNG ADULT; ADOLESCENT; CYTOLOGY; LUNG; METABOLISM; MULTICELLULAR SPHEROID; PHENOTYPE; STEM CELL; STEM CELL NICHE;

ADOLESCENT; ADULT; CELL PLASTICITY; FEMALE; HUMANS; LUNG; MALE; PARACRINE COMMUNICATION; PHENOTYPE; SPHEROIDS, CELLULAR; STEM CELL NICHE; STEM CELLS; YOUNG ADULT;

EID: 85017537015     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2015-0374     Document Type: Article

References (61)

1. European Respiratory Society. The burden of lung disease. Available at http://www erswhitebook.org/chapters/the-burden-oflung-disease/. Accessed September 18, 2016.
2. World Health Organization. World Health Statistics 2011. Available at http://www who.int/whosis/whostat/2011/en. Accessed November 30, 2015.
3. Kotton DN, Morrisey EE. Lung regeneration: Mechanisms, applications and emerging stem cell populations. Nat Med 2014;20: 822–832.
4. Beers MF, Morrisey EE. The three R’s of lung health and disease: Repair, remodeling, and regeneration. J Clin Invest 2011;121:2065–2073.
5. Herriges M, Morrisey EE. Lung development: Orchestrating the generation and regeneration of a complex organ. Development 2014;141: 502–513.
6. Tata PR, Mou H, Pardo-Saganta A et al. Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 2013; 503:218–223.
7. Chapman HA, Li X, Alexander JP et al. Integrin a6b4 identifies an adult distal lung epithelial population with regenerative potential in mice. J Clin Invest 2011;121: 2855–2862.
8. Kumar PA, Hu Y, Yamamoto Y et al. Distal airway stem cells yield alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 2011;147:525–538.
9. Tesei A, Zoli W, Arienti C et al. Isolation of stem/progenitor cells from normal lung tissue of adult humans. Cell Prolif 2009;42:298–308.
10. Fujino N, Kubo H, Suzuki T et al. Isolation of alveolar epithelial type II progenitor cells from adult human lungs. Lab Invest 2011;91: 363–378.
11. Rock JR, Onaitis MW, Rawlins EL et al. Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc Natl Acad Sci USA 2009;106:12771–12775.
12. Oeztuerk-Winder F, Guinot A, Ochalek A et al. Regulation of human lung alveolar multipotent cells by a novel p38a MAPK/miR-17-92 axis. EMBO J 2012;31:3431–3441.
13. Barkauskas CE, Cronce MJ, Rackley CR et al. Type 2 alveolar cells are stem cells in adult lung. J Clin Invest 2013;123:3025–3036.
14. Henry E, Cores J, Hensley MT et al. Adult lung spheroid cells contain progenitor cells and mediate regeneration in rodents with bleomycin-induced pulmonary fibrosis. STEM CELLS TRANSLATIONAL MEDICINE 2015;4: 1265–1274.
15. Wagner DE, Bonenfant NR, Parsons CS et al. Comparative decellularization and recellularization of normal versus emphysematous human lungs. Biomaterials 2014;35: 3281–3297.
16. Volckaert T, De Langhe S. Lung epithelial stem cells and their niches: Fgf10 takes center stage. Fibrogenesis Tissue Repair 2014;7:8.
17. Ornitz DM, Yin Y. Signaling networks regulating development of the lower respiratory tract. Cold Spring Harb Perspect Biol 2012;4:: a008318.
18. Ruiz EJ, Oeztuerk-Winder F, Ventura JJ. A paracrine network regulates the cross-talk betweenhumanlung stem cells and the stroma. Nat Commun 2014;5:3175.
19. Samadikuchaksaraei A, Bishop AE. Effects of growth factors on the differentiation of murine ESC into type II pneumocytes. Cloning Stem Cells 2007;9:407–416.
20. Fox E, Shojaie S, Wang J et al. Threedimensional culture and FGF signaling drive differentiation of murine pluripotent cells to distal lung epithelial cells. Stem Cells Dev 2015;24: 21–35.
21. Chapman HA. Epithelial responses to lung injury: Role of the extracellular matrix. Proc Am Thorac Soc 2012;9:89–95.
22. Lin YM, Zhang A, Rippon HJ et al. Tissue engineering of lung: The effect of extracellular matrix on the differentiation of embryonic stem cells to pneumocytes. Tissue Eng Part A 2010; 16:1515–1526.
23. Akram KM, Samad S, Spiteri MA et al. Mesenchymal stem cells promote alveolar epithelial cellwoundrepair in vitro through distinct migratory and paracrine mechanisms. Respir Res 2013;14:9.
24. Lin YM, Zhang A, Bismarck A et al. Effects of fibroblast growth factors on the differentiation of the pulmonary progenitors from murine embryonic stem cells. Exp Lung Res 2010;36: 307–320.
25. Shamir ER, Ewald AJ. Three-dimensional organotypic culture: Experimental models of mammalian biology and disease. Nat Rev Mol Cell Biol 2014;15:647–664.
26. Ader M, Tanaka EM. Modeling human development in 3D culture. Curr Opin Cell Biol 2014;31:23–28.
27. Ravi M, Paramesh V, Kaviya SR et al. 3D cell culture systems: Advantages and applications. J Cell Physiol 2015;230:16–26.
28. Chimenti I, Gaetani R, Barile L et al. Isolation and expansion of adult cardiac stem/progenitor cells in the form of cardiospheres from human cardiac biopsies and murine hearts. Methods Mol Biol 2012; 879:327–338.
29. Messina E, De Angelis L, Frati G et al. Isolation and expansion of adult cardiac stem cells from human and murine heart. Circ Res 2004; 95:911–921.
30. Siciliano C, Chimenti I, IbrahimMet al. Cardiosphere conditionedmedia influence the plasticity of human mediastinal adipose tissue-derived mesenchymal stem cells. Cell Transplant 2015; 24:2307–2322.
31. Siciliano C, Ibrahim M, Scafetta G et al. Optimization of the isolation and expansion method of human mediastinal-adipose tissue derived mesenchymal stem cells with virally inactivated GMP-grade platelet lysate. Cytotechnology 2015;67:165–174.
32. Pastrana E, Silva-Vargas V, Doetsch F. Eyes wide open: A critical review of sphereformation as an assay for stem cells. Cell Stem Cell 2011;8:486–498.
33. Ling TY, KuoMD, Li CL et al. Identification of pulmonary Oct-4+ stem/progenitor cells and demonstration of their susceptibility to SARS coronavirus (SARS-CoV) infection in vitro. Proc Natl Acad Sci USA 2006;103: 9530–9535.
34. Pirozzi G, Tirino V, Camerlingo R et al. Epithelial tomesenchymal transition byTGFß-1 induction increases stemness characteristics in primary non small cell lung cancer cell line. PLoS One 2011;6:e21548.
35. Forte E, Miraldi F, Chimenti I et al. TGFbdependent epithelial-to-mesenchymal transition is required to generate cardiospheres from human adult heart biopsies. Stem Cells Dev 2012; 21:3081–3090.
36. Mani SA, Guo W, Liao MJ et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133:704–715.
37. Fan X, Gay FP, Lim FW et al. Low-dose insulin-like growth factor binding proteins 1 and 2 and angiopoietin-like protein 3 coordinately stimulate ex vivo expansion of human umbilical cord blood hematopoietic stem cells as assayed in NOD/SCID gamma null mice. Stem Cell Res Ther 2014;5:71.
38. D’Elia P, Ionta V, Chimenti I et al. Analysis of pregnancy-associated plasma protein a production in human adult cardiac progenitor cells. Biomed Res Int. 2013;2013:190178.
39. Leeman KT, Fillmore CM, Kim CF. Lung stem and progenitor cells in tissue homeostasis and disease. Curr Top Dev Biol 2014;107: 207–233.
40. Huang Y, Johnston P, Zhang B et al. Kidney-derived stromal cells modulate dendritic and T cell responses. J Am Soc Nephrol 2009;20:831–841.
41. Puglisi MA, Giuliani L, Fierabracci A. Identificationand characterization of a novel expandable adult stem/progenitor cell population in the human exocrine pancreas. J Endocrinol Invest 2008;31:563–572.
42. Fierabracci A, Puglisi MA, Giuliani L et al. Identification of an adult stem/progenitor celllike population in the human thyroid. J Endocrinol 2008;198:471–487.
43. Farnie G, Clarke RB. Mammary stem cells and breast cancer–role of Notch signalling. Stem Cell Rev 2007;3:169–175.
44. Kotton DN. Next-generation regeneration: The hope and hype of lung stem cell research. Am J Respir Crit Care Med 2012;185: 1255–1260.
45. Hegab AE, Kubo H, Fujino N et al. Isolation and characterization of murine multipotent lung stem cells. Stem Cells Dev 2010;19: 523–536.
46. Wang XY, Keefe KM, Jensen-Taubman SM et al. Novel method for isolation of murine clara cell secretory protein-expressing cells with traces of stemness. PLoS One 2012;7:e43008.
47. Ficial M, Antonaglia C, Chilosi M et al. Keratin-14 expression in pneumocytes as a marker of lung regeneration/repair during diffuse alveolar damage. Am J Respir Crit Care Med 2014;189:1142–1145.
48. Desai TJ, Brownfield DG, KrasnowMA. Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 2014; 507:190–194.
49. Finigan JH, Downey GP, Kern JA. Human epidermal growth factor receptor signaling in acute lung injury. Am J Respir Cell Mol Biol 2012;47:395–404.
50. Horie M, Saito A, Noguchi S et al. Differential knockdown of TGF-ß ligands in a three-dimensional co-culture tumor- stromal interaction model of lung cancer. BMC Cancer 2014;14:580.
51. Kasai H, Allen JT, Mason RM et al. TGFbeta1 induceshumanalveolar epithelial to mesenchymal cell transition (EMT). Respir Res 2005; 6:56.
52. Zhou B, Liu Y, Kahn M et al. Interactions between b-catenin and transforming growth factor-b signaling pathways mediate epithelialmesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binding protein (CREB)-binding protein (CBP). J Biol Chem 2012;287:7026–7038.
53. Hackett TL, Warner SM, Stefanowicz D et al. Induction of epithelial-mesenchymal transition in primary airway epithelial cells from patients with asthma by transforming growth factor-beta1. Am J Respir Crit Care Med 2009; 180:122–133.
54. McQualter JL, Yuen K, Williams B et al. Evidence of an epithelial stem/progenitor cell hierarchy in the adult mouse lung. Proc Natl Acad Sci USA 2010;107:1414–1419.
55. Yamamoto H, Yun EJ, Gerber HP et al. Epithelial-vascular cross talk mediated by VEGF-A andHGFsignalingdirectsprimaryseptaeformation during distal lung morphogenesis. Dev Biol 2007; 308:44–53.
56. Rogel MR, Soni PN, Troken JR et al. Vimentin is sufficient and required for wound repair and remodeling in alveolar epithelial cells. FASEB J 2011;25:3873–3883.
57. Kovacic JC, Mercader N, Torres M et al. Epithelial-to-mesenchymal and endothelial-tomesenchymal transition: From cardiovascular development to disease. Circulation 2012;125: 1795–1808.
58. Liu X, Sun H, Qi J et al. Sequential introduction of reprogramming factors reveals a time-sensitive requirement for individual factors and a sequential EMT-MET mechanism for optimal reprogramming. Nat Cell Biol 2013; 15:829–838.
59. Cheng NC, Wang S, Young TH. The influence of spheroid formation of human adiposederived stemcells on chitosan films on stemness and differentiation capabilities. Biomaterials 2012;33:1748–1758.
60. Tanjore H, Degryse AL, Crossno PF et al. ß-catenin in the alveolar epithelium protects from lung fibrosis after intratracheal bleomycin. Am J Respir Crit Care Med 2013;187: 630–639.
61. Volckaert T, Campbell A, Dill E et al. Localized Fgf10 expression is not required for lung branching morphogenesis but prevents differentiation of epithelial progenitors. Development 2013;140: 3731–3742.