On the biomechanics of stem cell niche formation in the gut - Modelling growing organoids

FEBS Journal

Volumn 279, Issue 18, 2012, Pages 3475-3487

  Buske, Peter ^a   Przybilla, Jens ^a   Loeffler, Markus ^a   Sachs, Norman ^b   Sato, Toshiro ^b,c   Clevers, Hans ^b   Galle, Joerg ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c KEIO UNIVERSITY   (Japan)

Author keywords

computer model; crypt formation; intestinal tissue culture; mechanobiology; stem cell niche

Indexed keywords

CELL ADHESION; CELL COUNT; CELL EXPANSION; CELL FUNCTION; CELL LINEAGE; CELL PROLIFERATION; CELL SPECIFICITY; CELL STIMULATION; COMPLEX FORMATION; COMPUTER SIMULATION; CONFERENCE PAPER; FEEDBACK SYSTEM; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; ORGAN GROWTH; PANETH CELL; PRIORITY JOURNAL; STEM CELL NICHE; YOUNG MODULUS;

BIOMECHANICS; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; COMPUTER SIMULATION; EPITHELIAL CELLS; INTESTINES; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; ORGANOIDS; PANETH CELLS; STEM CELL NICHE; STEM CELLS;

EID: 84865978356     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08646.x     Document Type: Conference Paper

References (67)

1. Barker N, van de Wetering M, &, Clevers H, (2008) The intestinal stem cell. Genes Dev 22, 1856-1864. (Pubitemid 352008634)
2. Scoville DH, Sato T, He XC, &, Li L, (2008) Current view: intestinal stem cells and signaling. Gastroenterology 134, 849-864. (Pubitemid 351312767)
3. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265.
4. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 449, 1003-1007. (Pubitemid 350014593)
5. Buske P, Galle J, Barker N, Aust G, Clevers H, &, Loeffler M, (2011) A comprehensive model of the spatio-temporal stem cell and tissue organisation in the intestinal crypt. PLoS Comput Biol 7, e1001045.
6. van Leeuwen IM, Mirams GR, Walter A, Fletcher A, Murray P, Osborne J, Varma S, Young SJ, Cooper J, Doyle B, et al. (2009) An integrative computational model for intestinal tissue renewal. Cell Prolif 42, 617-636.
7. Meineke FA, Potten CS, &, Loeffler M, (2001) Cell migration and organization in the intestinal crypt using a lattice-free model. Cell Prolif 34, 253-266. (Pubitemid 32738648)
8. Potten CS, &, Loeffler M, (1987) A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol 127, 381-391.
9. Hannezo E, Prost J, &, Joanny JF, (2011) Instabilities of monolayered epithelia: shape and structure of villi and crypts. Phys Rev Lett 107, 078104.
10. Drasdo D, &, Forgacs G, (2000) Modeling the interplay of generic and genetic mechanisms in cleavage, blastulation, and gastrulation. Dev Dyn 219, 182-191.
11. Roeder I, Loeffler M, &, Glauche I, (2011) Towards a quantitative understanding of stem cell-niche interaction: experiments, models, and technologies. Blood Cells Mol Dis 46, 308-317.
12. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, &, Clevers H, (2011) Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418.
13. Mustata RC, Van Loy T, Lefort A, Libert F, Strollo S, Vassart G, &, Garcia MI, (2011) Lgr4 is required for Paneth cell differentiation and maintenance of intestinal stem cells ex vivo. EMBO Rep 12, 558-564.
14. Mammoto T, &, Ingber DE, (2010) Mechanical control of tissue and organ development. Development 137, 1407-1420.
15. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ, Spector AA, &, Chen CS, (2005) Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA 102, 11594-11599. (Pubitemid 41170771)
16. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, &, Chen CS, (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6, 483-495. (Pubitemid 38456178)
17. Chen CS, Mrksich M, Huang S, Whitesides GM, &, Ingber DE, (1997) Geometric control of cell life and death. Science 276, 1425-1428. (Pubitemid 27235413)
18. Lui C, Lee K, &, Nelson CM, (2011) Matrix compliance and RhoA direct the differentiation of mammary progenitor cells. Biomech Model Mechanobiol doi:10.1007/s10237-011-0362-7.
19. Engler AJ, Sen S, Sweeney HL, &, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689. (Pubitemid 44233625)
20. Miyoshi J, &, Takai Y, (2008) Structural and functional associations of apical junctions with cytoskeleton. Biochim Biophys Acta 1778, 670-691.
21. Yurchenco PD, &, Patton BL, (2009) Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15, 1277-1294.
22. Daley WP, Gulfo KM, Sequeira SJ, &, Larsen M, (2009) Identification of a mechanochemical checkpoint and negative feedback loop regulating branching morphogenesis. Dev Biol 336, 169-182.
23. Daley WP, Gervais EM, Centanni SW, Gulfo KM, Nelson DA, &, Larsen M, (2012) ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development 139, 411-422.
24. Kierfeld J, Niamploy O, Sa-yakanit V, &, Lipowsky R, (2004) Stretching of semiflexible polymers with elastic bonds. Eur Phys J E Soft Matter 14, 17-34. (Pubitemid 40877392)
25. Gompper G, &, Kroll DM, (1994) Phase diagram of fluid vesicles. Phys Rev Lett 73, 2139-2142. (Pubitemid 24977808)
26. Kroll DM, &, Gompper G, (1992) The conformation of fluid membranes: Monte Carlo simulations. Science 255, 968-971.
27. Galle J, Loeffler M, &, Drasdo D, (2005) Modeling the effect of deregulated proliferation and apoptosis on the growth dynamics of epithelial cell populations in vitro. Biophys J 88, 62-75. (Pubitemid 40070658)
28. Galle J, Hoffmann M, &, Aust G, (2009) From single cells to tissue architecture-a bottom-up approach to modelling the spatio-temporal organisation of complex multi-cellular systems. J Math Biol 58, 261-283.
29. Galle J, Preziosi L, &, Tosin A, (2009) Contact inhibition of growth described using a multiphase model and an individual cell based model. Appl Math Lett 22, 1483-1490.
30. Drasdo D, Hoehme S, &, Block M, (2007) On the role of physics in the growth and pattern formation of multi-cellular systems: what can we learn from individual-cell based models?. J Stat Phys 128, 287-345.
31. Green KJ, Getsios S, Troyanovsky S, &, Godsel LM, (2010) Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol 2, a000125.
32. Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, &, Ingber DE, (2005) Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232, 268-281. (Pubitemid 40129780)
33. Beaulieu JF, (1999) Integrins and human intestinal cell functions. Front Biosci 4, D310-D321.
34. Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, &, Jain RK, (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15, 778-783. (Pubitemid 27329482)
35. Deuling HJ, &, Helfrich W, (1976) Curvature elasticity of fluid membranes-catalog of vesicle shapes. J Phys France 37, 1335-1345.
36. Sprinzak D, Lakhanpal A, LeBon L, Garcia-Ojalvo J, &, Elowitz MB, (2011) Mutual inactivation of Notch receptors and ligands facilitates developmental patterning. PLoS Comput Biol 7, e1002069.
37. Benoit YD, Lussier C, Ducharme PA, Sivret S, Schnapp LM, Basora N, &, Beaulieu JF, (2009) Integrin α8β1 regulates adhesion, migration and proliferation of human intestinal crypt cells via a predominant RhoA/ROCK-dependent mechanism. Biol Cell 101, 695-708.
38. Stappenbeck TS, &, Gordon JI, (2000) Rac1 mutations produce aberrant epithelial differentiation in the developing and adult mouse small intestine. Development 127, 2629-2642. (Pubitemid 30426810)
39. Chauhan BK, Lou M, Zheng Y, &, Lang RA, (2011) Balanced Rac1 and RhoA activities regulate cell shape and drive invagination morphogenesis in epithelia. Proc Natl Acad Sci USA 108, 18289-18294.
40. Jilkine A, Maree AF, &, Edelstein-Keshet L, (2007) Mathematical model for spatial segregation of the Rho-family GTPases based on inhibitory crosstalk. Bull Math Biol 69, 1943-1978. (Pubitemid 47222246)
41. Cheng H, (1974) Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. IV. Paneth cells. Am J Anat 141, 521-535.
42. Keller R, Davidson LA, &, Shook DR, (2003) How we are shaped: the biomechanics of gastrulation. Differentiation 71, 171-205. (Pubitemid 36535222)
43. MacKintosh FC, Kas J, &, Janmey PA, (1995) Elasticity of semiflexible biopolymer networks. Phys Rev Lett 75, 4425-4428.
44. Drasdo D, (2000) Buckling instabilities of one-layered growing tissues. Phys Rev Lett 84, 4244-4247.
45. Dunn SJ, Fletcher AG, Chapman SJ, Gavaghan DJ, &, Osborne JM, (2011) Modelling the role of the basement membrane beneath a growing epithelial monolayer. J Theor Biol 298C, 82-91.
46. Nelson MR, Howard D, Jensen OE, King JR, Rose FR, &, Waters SL, (2011) Growth-induced buckling of an epithelial layer. Biomech Model Mechanobiol 10, 883-900.
47. Wang L, Murthy SK, Barabino GA, &, Carrier RL, (2010) Synergic effects of crypt-like topography and ECM proteins on intestinal cell behavior in collagen based membranes. Biomaterials 31, 7586-7598.
48. Evans GS, Flint N, Somers AS, Eyden B, &, Potten CS, (1992) The development of a method for the preparation of rat intestinal epithelial cell primary cultures. J Cell Sci 101, 219-231.
49. Rubio CA, (2004) Paneth cell adenoma of the ileum. Anticancer Res 24, 4187-4190. (Pubitemid 40468726)
50. Kazzaz BA, &, Eulderink F, (1989) Paneth cell-rich carcinoma of the stomach. Histopathology 15, 303-305. (Pubitemid 19232654)
51. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, et al. (2002) β-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111, 251-263. (Pubitemid 35292445)
52. Kullander K, &, Klein R, (2002) Mechanisms and functions of Eph and ephrin signalling. Nat Rev Mol Cell Biol 3, 475-486. (Pubitemid 34733429)
53. Eyckmans J, Boudou T, Yu X, &, Chen CS, (2011) A hitchhiker's guide to mechanobiology. Dev Cell 21, 35-47.
54. Gitelman I, (1997) Twist protein in mouse embryogenesis. Dev Biol 189, 205-214. (Pubitemid 27428363)
55. Tullio AN, Accili D, Ferrans VJ, Yu ZX, Takeda K, Grinberg A, Westphal H, Preston YA, &, Adelstein RS, (1997) Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc Natl Acad Sci USA 94, 12407-12412. (Pubitemid 27492541)
56. Ghajar CM, &, Bissell MJ, (2008) Extracellular matrix control of mammary gland morphogenesis and tumorigenesis: insights from imaging. Histochem Cell Biol 130, 1105-1118.
57. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254. (Pubitemid 41317594)
58. Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van den Brink S, Van Houdt WJ, Pronk A, Van Gorp J, Siersema PD, et al. (2011) Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-1772.
59. Huang S, &, Ingber DE, (2005) Cell tension, matrix mechanics, and cancer development. Cancer Cell 8, 175-176. (Pubitemid 41317587)
60. Wang Y, Azuma Y, Friedman DB, Coffey RJ, &, Neufeld KL, (2009) Novel association of APC with intermediate filaments identified using a new versatile APC antibody. BMC Cell Biol 10, 75.
61. Nathke I, (2006) Cytoskeleton out of the cupboard: colon cancer and cytoskeletal changes induced by loss of APC. Nat Rev Cancer 6, 967-974. (Pubitemid 44862681)
62. Dydensborg AB, Teller IC, Basora N, Groulx JF, Auclair J, Francoeur C, Escaffit F, Pare F, Herring E, Menard D, et al. (2009) Differential expression of the integrins α6Aβ4 and α6Bβ4 along the crypt-villus axis in the human small intestine. Histochem Cell Biol 131, 531-536.
63. Lussier C, Basora N, Bouatrouss Y, &, Beaulieu JF, (2000) Integrins as mediators of epithelial cell-matrix interactions in the human small intestinal mucosa. Microsc Res Tech 51, 169-178.
64. 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, et al. (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.
65. Harunaga J, Hsu JC, &, Yamada KM, (2011) Dynamics of salivary gland morphogenesis. J Dent Res 90, 1070-1077.
66. Toni R, Casa CD, Spaletta G, Marchetti G, Mazzoni P, Bodria M, Ravera S, Dallatana D, Castorina S, Riccioli V, et al. (2007) The bioartificial thyroid: a biotechnological perspective in endocrine organ engineering for transplantation replacement. Acta Biomed 78 (Suppl. 1), 129-155.
67. Campbell JJ, Davidenko N, Caffarel MM, Cameron RE, &, Watson CJ, (2011) A multifunctional 3D co-culture system for studies of mammary tissue morphogenesis and stem cell biology. PLoS One 6, e25661.