Surface topography regulates wnt signaling through control of primary cilia structure in mesenchymal stem cells

Scientific Reports

Volumn 3, Issue , 2013, Pages

  McMurray, R J ^a   Wann, A K T ^a   Thompson, C L ^a   Connelly, J T ^b   Knight, M M ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; AMIDE; AXIN; AXIN2 PROTEIN, HUMAN; BETA CATENIN; ENZYME INHIBITOR; IFT88 PROTEIN, HUMAN; MYOSIN; PYRIDINE DERIVATIVE; RHO KINASE; SMALL INTERFERING RNA; TUMOR SUPPRESSOR PROTEIN; WNT3A PROTEIN; WNT3A PROTEIN, HUMAN;

ACTIN FILAMENT; ARTICLE; BIOSYNTHESIS; BONE MARROW CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CULTURE TECHNIQUE; DRUG ANTAGONISM; EUKARYOTIC FLAGELLUM; GENETICS; HUMAN; MECHANOTRANSDUCTION; MESENCHYMAL STROMA CELL; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RNA INTERFERENCE; SURFACE PROPERTY; WNT SIGNALING PATHWAY;

ACTIN CYTOSKELETON; AMIDES; AXIN PROTEIN; BETA CATENIN; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CILIA; ENZYME INHIBITORS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; MYOSINS; PYRIDINES; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; RNA, SMALL INTERFERING; STRESS, PHYSIOLOGICAL; SURFACE PROPERTIES; TUMOR SUPPRESSOR PROTEINS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84894063727     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep03545     Document Type: Article

References (46)

1. Kim, S. et al. Nde1-mediated inhibition of ciliogenesis affects cell cycle re-entry. Nat Cell Biol 13, 351-60 (2011).
2. Schneider, L. et al. Directional cell migration and chemotaxis in wound healing response to PDGF-AA are coordinated by the primary cilium in fibroblasts. Cell Physiol Biochem 25, 279-92 (2010).
3. Zhu, D., Shi, S., Wang, H. & Liao, K. Growth arrest induces primary-cilium formation and sensitizes IGF-1-receptor signaling during differentiation induction of 3T3-L1 preadipocytes. J Cell Sci 122, 2760-8 (2009).
4. Ezratty, E. J. et al. A role for the primary cilium in Notch signaling and epidermal differentiation during skin development. Cell 145, 1129-41 (2011).
5. Caspary, T., Larkins, C. E. & Anderson, K. V. The graded response to Sonic Hedgehog depends on cilia architecture. Dev Cell 12, 767-78 (2007).
6. Lancaster, M. A., Schroth, J. & Gleeson, J. G. Subcellular spatial regulation of canonical Wnt signalling at the primary cilium. Nat Cell Biol 13, 700-7 (2011).
7. Neugebauer, J. M., Amack, J. D., Peterson, A. G., Bisgrove, B. W. & Yost, H. J. FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 458, 651-4 (2009).
8. Wann, A.K. & Knight, M.M.Primary cilia elongation inresponsetointerleukin-1 mediates the inflammatory response. Cell Mol Life Sci 69, 2967-77 (2012).
9. Wann, A. K. et al. Primary cilia mediate mechanotransduction through control of ATP-induced Ca21 signaling in compressed chondrocytes. Faseb J 26, 1663-71 (2012).
10. Pazour, G. J. & Witman, G. B. The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 15, 105-10 (2003).
11. Nauli, S. M. et al. Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33, 129-37 (2003).
12. Malone, A. M. et al. Primary cilia mediate mechanosensing in bone cells by a calcium-independent mechanism. Proc Natl Acad Sci U S A 104, 13325-30 (2007).
13. Eggenschwiler, J. T. & Anderson, K. V. Cilia and developmental signaling. Annu Rev Cell Dev Biol 23, 345-73 (2007).
14. Haycraft, C. J., Swoboda, P., Taulman, P. D., Thomas, J. H. & Yoder, B. K. The C. elegans homolog of the murine cystic kidney disease gene Tg737 functions in a ciliogenic pathway and is disrupted in osm-5 mutant worms. Development 128, 1493-505 (2001).
15. Pazour, G. J. et al. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151, 709-18 (2000).
16. Abdul-Majeed, S., Moloney, B. C. & Nauli, S. M. Mechanisms regulating cilia growth and cilia function in endothelial cells. Cell Mol Life Sci 69, 165-73 (2011).
17. Besschetnova, T. Y. et al. Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr Biol 20, 182-7 (2010).
18. Kim, J. et al. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464, 1048-51 (2010).
19. Marszalek, J. R. et al. Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102, 175-87 (2000).
20. Massinen, S. et al. Increased Expression of the Dyslexia Candidate Gene DCDC2 Affects Length and Signaling of Primary Cilia in Neurons. PLoS One 6, e20580 (2011).
21. Tran, P. V. et al. THM1 negatively modulates mouse sonic hedgehog signal transduction and affects retrograde intraflagellar transport in cilia. Nat Genet 40, 403-10 (2008).
22. Rohatgi, R., Milenkovic, L. & Scott, M. P. Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372-6 (2007).
23. Simons, M. et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37, 537-43 (2005).
24. Lienkamp, S., Ganner, A. & Walz, G. Inversin, Wnt signaling and primary cilia. Differentiation 83, S49-55 (2012).
25. Clement, C. A. et al. The primary cilium coordinates early cardiogenesis and hedgehog signaling in cardiomyocyte differentiation. J Cell Sci 122, 3070-82 (2009).
26. Li, A. et al. Ciliary transition zone activation of phosphorylated Tctex-1 controls ciliary resorption, S-phase entry and fate of neural progenitors. Nat Cell Biol 13, 402-11.
27. Tummala, P., Arnsdorf, E. J. & Jacobs, C. R. The Role of Primary Cilia in Mesenchymal Stem Cell Differentiation: A Pivotal Switch in Guiding Lineage Commitment. Cell Mol Bioeng 3, 207-212 (2010).
28. Yang, S. & Wang, C. The intraflagellar transport protein IFT80 is required for cilia formation and osteogenesis. Bone 51, 407-17 (2012).
29. Hoey, D. A., Tormey, S., Ramcharan, S., O'Brien, F. J. & Jacobs, C. R. Primary cilia-mediated mechanotransduction inhuman mesenchymal stem cells. Stem Cells 30, 2561-70 (2012).
30. Ou, Y. et al. Adenylate cyclase regulates elongation of mammalian primary cilia. Exp Cell Res 315, 2802-17 (2009).
31. Bershteyn, M., Atwood, S.X., Woo, W. M., Li, M. & Oro, A. E. MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev Cell 19, 270-83 (2010).
32. Pitaval, A., Tseng, Q., Bornens, M. & Thery, M. Cell shape and contractility regulate ciliogenesis in cell cycle-arrested cells. J Cell Biol 191, 303-12 (2010).
33. Engler, A. J., Sen, S., Sweeney, H. L. & Discher, D. E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-89 (2006).
34. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. & Chen, C. S. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6, 483-95 (2004).
35. McMurray, R. J. et al. Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat Mater 10, 637-44 (2011).
36. Cavalcanti-Adam, E. A. et al. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys J 92, 2964-74 (2007).
37. Biggs, M. J. et al. Interactions with nanoscale topography: adhesion quantification and signal transduction in cells of osteogenic and multipotent lineage. J Biomed Mater Res A 91, 195-208 (2009).
38. Biggs, M. J. et al. Adhesion formation of primary human osteoblasts and the functional response of mesenchymal stem cells to 330 nm deep microgrooves. J R Soc Interface 5, 1231-42 (2008).
39. Yim, E. K., Darling, E. M., Kulangara, K., Guilak, F. & Leong, K. W. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 31, 1299-306 (2010).
40. Yim, E. K., Pang, S. W. & Leong, K. W. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 313, 1820-9 (2007).
41. Chen, C. S., Alonso, J. L., Ostuni, E., Whitesides, G. M. & Ingber, D. E. Cell shape provides global controloffocal adhesion assembly. Biochem Biophys Res Commun 307, 355-61 (2003).
42. Chen, C. S., Mrksich, M., Huang, S., Whitesides, G. M. & Ingber, D. E. Geometric control of cell life and death. Science 276, 1425-8 (1997).
43. Kilian, K. A., Bugarija, B., Lahn, B. T. & Mrksich, M. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A 107, 4872-7 (2010).
44. Brydone, A. S., Dalby, M. J., Berry, C.C., Dominic Meek, R. M. & McNamara, L.E. Grooved surface topography alters matrix-metalloproteinase production by human fibroblasts. Biomed Mater 6, 035005 (2011).
45. Donnelly, E., Ascenzi, M. G. & Farnum, C. Primary cilia are highly oriented with respect to collagen direction and long axis of extensor tendon. J Orthop Res 28, 77-82 (2010).
46. Logan, C. Y. & Nusse, R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20, 781-810 (2004).