A strategy for tissue self-organization that is robust to cellular heterogeneity and plasticity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 7, 2015, Pages 2287-2292

  Cerchiari, Alec E ^a,b,c   Garbe, James C ^b,c   Jee, Noel Y ^c   Todhunter, Michael E ^c   Broaders, Kyle E ^c   Peehl, Donna M ^d   Desai, Tejal A ^a,b   LaBarge, Mark A ^c   Thomsonf, Matthew ^e   Gartner, Zev J ^a,c,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell sorting; Differential adhesion; Heterogeneity; Mammary; Prostate

Indexed keywords

ADAPTOR PROTEIN; CATENIN; MATRIGEL; PROTEIN P120; PROTEIN TALIN1; SMALL INTERFERING RNA; TISSUE ADHESIVE; UNCLASSIFIED DRUG;

ARTICLE; BREAST EPITHELIUM CELL; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL INTERACTION; CELLS BY BODY ANATOMY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTACT ANGLE; CONTROLLED STUDY; CYTOARCHITECTURE; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; INNER LUMINAL CELL; MAMMARY GLAND; MYOEPITHELIUM CELL; PRIMARY CELL; PRIORITY JOURNAL; PROSTATE; TISSUE SELF ORGANIZATION; TISSUE STRUCTURE; CELL COMMUNICATION; CYTOLOGY; EPITHELIUM CELL;

CELL COMMUNICATION; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; MAMMARY GLANDS, HUMAN;

EID: 84923197391     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1410776112     Document Type: Article

References (40)

1. Sasai Y (2013) Cytosystems dynamics in self-organization of tissue architecture. Nature 493(7432):318-326.
2. Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128(1):53-120.
3. Xiong F, et al. (2013) Specified neural progenitors sort to form sharp domains after noisy Shh signaling. Cell 153(3):550-561.
4. Dietrich J-E, Hiiragi T (2007) Stochastic patterning in the mouse pre-implantation embryo. Development 134(23):4219-4231.
5. Maître J-L, et al. (2012) Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338(6104):253-256.
6. Steinberg MS (1963) Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141(3579):401-408.
7. Chanson L, et al. (2011) Self-organization is a dynamic and lineage-intrinsic property of mammary epithelial cells. Proc Natl Acad Sci USA 108(8):3264-3269.
8. Runswick SK, O'Hare MJ, Jones L, Streuli CH, Garrod DR (2001) Desmosomal adhesion regulates epithelial morphogenesis and cell positioning. Nat Cell Biol 3(9):823-830.
9. Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z (2008) Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 14(4):570-581.
10. Mailleux AA, et al. (2007) BIM regulates apoptosis duringmammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 12(2):221-234.
11. Radice GL, et al. (1997) Precocious mammary gland development in P-cadherindeficient mice. J Cell Biol 139(4):1025-1032.
12. Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R (2002) E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 115(1-2):53-62.
13. Altschuler SJ, Wu LF (2010) Cellular heterogeneity: Do differences make a difference? Cell 141(4):559-563.
14. Moreira JMAJ, et al. (2010) Tissue proteomics of the human mammary gland: Towards an abridged definition of the molecular phenotypes underlying epithelial normalcy. Mol Oncol 4(6):539-561.
15. Keller PJ, et al. (2010) Mapping the cellular and molecular heterogeneity of normal and malignant breast tissues and cultured cell lines. Breast Cancer Res 12(5):R87.
16. ShehataM, et al. (2012) Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland. Breast Cancer Res 14(5):R134.
17. Bloushtain-Qimron N, et al. (2008) Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 105(37):14076-14081.
18. Shamir ER, et al. (2014) Twist1-induced dissemination preserves epithelial identity and requires E-cadherin. J Cell Biol 204(5):839-856.
19. Bissell MJ, Hall HG, Parry G (1982) How does the extracellular matrix direct gene expression? J Theor Biol 99(1):31-68.
20. Cerchiari A, et al. (2014) Formation of spatially and geometrically controlled threedimensional tissues in soft gels by sacrificial micromolding. Tissue Eng Part C Methods, in press.
21. Kleinman HK, et al. (1986) Basement membrane complexes with biological activity. Biochemistry 25(2):312-318.
22. Liu JS, Farlow JT, Paulson AK, Labarge MA, Gartner ZJ (2012) Programmed cell-to-cell variability in Ras activity triggers emergent behaviors during mammary epithelial morphogenesis. Cell Reports 2(5):1461-1470.
23. Selden NS, et al. (2012) Chemically programmed cell adhesion with membrane-anchored oligonucleotides. J Am Chem Soc 134(2):765-768.
24. Gartner ZJ, Bertozzi CR (2009) Programmed assembly of 3-dimensional microtissues with defined cellular connectivity. Proc Natl Acad Sci USA 106(12):4606-4610.
25. Zhang X, et al. (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol 10(9):1062-1068.
26. Robinson EE, Zazzali KM, Corbett SA, Foty RA (2003) Alpha5beta1 integrin mediates strong tissue cohesion. J Cell Sci 116(Pt 2):377-386.
27. Garbe JC, et al. (2012) Accumulation of multipotent progenitors with abasal differentiation bias during aging of human mammary epithelia. Cancer Res 72(14):3687-3701.
28. Ohnishi Y, et al. (2014) Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. Nat Cell Biol 16(1):27-37.
29. Krieg M, et al. (2008) Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10(4):429-436.
30. Keller R, Davidson LA, Shook DR (2003) How we are shaped: The biomechanics of gastrulation. Differentiation 71(3):171-205.
31. Dill KA, et al. (1995) Principles of protein folding-a perspective from simple exact models. Protein Sci 4(4):561-602.
32. Evers B, et al. (2010) A tissue reconstitution model to study cancer cell-intrinsic and -extrinsic factors in mammary tumourigenesis. J Pathol 220(1):34-44.
33. Kurley SJ, et al. (2012) p120-catenin is essential for terminal end bud function and mammary morphogenesis. Development 139(10):1754-1764.
34. Klinowska TC, et al. (2001) Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 233(2):449-467.
35. van Miltenburg MHAM, et al. (2009) Complete focal adhesion kinase deficiency in the mammary gland causes ductal dilation and aberrant branching morphogenesis through defects in Rho kinase-dependent cell contractility. FASEB J 23(10):3482-3493.
36. Adriance MC, Inman JL, Petersen OW, Bissell MJ (2005) Myoepithelial cells: Good fences make good neighbors. Breast Cancer Res 7(5):190-197.
37. Gudjonsson T, et al. (2002) Normal and tumor-derived myoepithelial cells differ in their ability to interact with luminal breast epithelial cells for polarity and basement membrane deposition. J Cell Sci 115(Pt 1):39-50.
38. Keller PJ, et al. (2012) Defining the cellular precursors to human breast cancer. Proc Natl Acad Sci USA 109(8):2772-2777.
39. Cheung KJ, Gabrielson E, Werb Z, Ewald AJ (2013) Collective invasion in breast cancer requires a conserved basal epithelial program. Cell 155(7):1639-1651.
40. Rudland PS (1991) Histochemical organization and cellular composition of ductal buds in developing human breast: Evidence of cytochemical intermediates between epithelial and myoepithelial cells. J Histochem Cytochem 39(11):1471-1484.