Mechanoresponsive, omni-directional and local matrix-degrading actin protrusions in human mesenchymal stem cells microencapsulated in a 3D collagen matrix

Biomaterials

Volumn 53, Issue , 2015, Pages 392-405

  Ho, Fu Chak ^a   Zhang, Wei ^a   Li, Yuk Yin ^a   Chan, Barbara Pui ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Actin protrusions; Cell matrix interface; Collagen microencapsulation; Human mesenchymal stem cells; Mechanopodia; Mechanoresponsive

Indexed keywords

ALIGNMENT; CELL CULTURE; COLLAGEN; MICROENCAPSULATION;

ACTIN PROTRUSIONS; CELL MATRIX; HUMAN MESENCHYMAL STEM CELLS; MECHANOPODIA; MECHANORESPONSIVE;

STEM CELLS;

ACTIN; BETA ACTIN; COLLAGEN; F ACTIN; G ACTIN; MATRIX METALLOPROTEINASE 14; PROTEIN CDC42;

ACTIN FILAMENT; ARTICLE; BIODEGRADABILITY; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL COMPONENT; CELL COMPOSITION; CELL FATE; CELL FUNCTION; CELL STRUCTURE; COLLAGEN DEGRADATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FILOPODIA; HUMAN; HUMAN CELL; INVADOPODIA; MECHANICAL STIMULATION; MECHANOPODIA; MESENCHYMAL STROMA CELL; MICROENCAPSULATION; MOLECULAR STABILITY; PODOSOME; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; CELL CULTURE; CYTOLOGY; DRUG FORMULATION; METABOLISM;

CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; COLLAGEN; DRUG COMPOUNDING; EXTRACELLULAR MATRIX; HUMANS; MESENCHYMAL STROMAL CELLS; SIGNAL TRANSDUCTION;

EID: 84927928303     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.102     Document Type: Article

References (50)

1. Wang Y.K., Chen C.S. Cell adhesion and mechanical stimulation in the regulation of mesenchymal stem cell differentiation. JCell Mol Med 2013, 17(7):823-832.
2. Subramony S.D., Dargis B.R., Castillo M., Azeloglu E.U., Tracey M.S., Su A., et al. The guidance of stem cell differentiation by substrate alignment and mechanical stimulation. Biomaterials 2013, 34(8):1942-1953.
3. Goli-Malekabadi Z., Tafazzoli-Shadpour M., Rabbani M., Janmaleki M. Effect of uniaxial stretch on morphology and cytoskeleton of human mesenchymal stem cells: static vs. dynamic loading. Biomed Tech (Berl) 2011, 56(5):259-265.
4. Vunjak-Novakovic G., Meinel L., Altman G., Kaplan D. Bioreactor cultivation of osteochondral grafts. Orthod Craniofac Res 2005, 8(3):209-218.
5. Thomopoulos S., Das R., Birman V., Smith L., Ku K., Elson E.L., et al. Fibrocartilage tissue engineering: the role of the stress environment on cell morphology and matrix expression. Tissue Eng Part A 2011, 17(7-8):1039-1053.
6. Au-yeung K.L., Sze K.Y., Sham M.H., Chan B.P. Development of a micromanipulator-based loading device for mechanoregulation study of human mesenchymal stem cells in 3D collagen constructs. Tissue Eng Part C 2010, 16(1):93-107.
7. Kwok C.B., Ho F.C., Li C.W., Ngan A.H., Chan D., Chan B.P. Compression induced alignment and elongation of human mesenchymal stem cell (hMSC) in 3D collagen constructs is collagen concentration dependent. JBiomed Mater Res Part A 2012, 101(6):1716-1725.
8. Chik T.K., Chooi W.H., Li Y.Y., Ho F.C., Cheng H.W., Choy T.H., et al. Bioengineering a multicomponent spinal motion segment construct-a 3D model for complex tissue engineering. Adv Healthc Mater 2014, 10.1002/adhm.201400192.
9. Frank C., MacFarlane B., Edwards P., Rangayyan R., Liu Z.Q., Walsh S., et al. Aquantitative analysis of matrix alignment in ligament scars: a comparison of movement versus immobilization in an immature rabbit model. JOrthop Res 1991, 9:219-227.
10. Cha J.M., Park S.N., Noh S.H., Suh H. Time-dependent modulation of alignment and differentiation of smooth muscle cells seeded on a porous substrate undergoing cyclic mechanical strain. Artif Organs 2006, 30:250-258.
11. Hirschy A., Schatzmann F., Ehler E., Perriard J.C. Establishment of cardiac cytoarchitecture in the developing mouse heart. Dev Biol 2006, 289:430-441.
12. Turner K.G., Ahmed N., Santerre J.P., Kandel R.A. Modulation of annulus fibrosus cell alignment and function on oriented nanofibrous polyurethane scaffolds under tension. Spine J 2014, 14(3):424-434.
13. Dominguez D., Holmes K.C. Actin structure and function. Annu Rev Biophys 2011, 40:169-186.
14. Murphy D.A., Courtneidge S.A. The 'ins' and 'outs' of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 2011, 12(7):413-426.
15. Heckman C.A., Plummer H.K. Filopodia as sensors. Cell Signal 2013, 25(11):2298-2311.
16. Kozma R., Ahmed S., Best A., Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol 1995, 15:1942-1952.
17. Gimona M., Buccione R., Courtneidge S.A., Linder S. Assembly and biological role of podosomes and invadopodia. Curr Opin Cell Biol 2008, 20(2):235-241.
18. Inui T., Ishibashi O., Origane Y., Fujimori K., Kokubo T., Nakajima M. Matrix metalloproteinases and lysosomal cysteine proteases in osteoclasts contribute to bone resorption through distinct modes of action. Biochem Biophys Res Commun 1999, 258(1):173-178.
19. Van Goethem E., Guiet R., Balor S., Charrière G.M., Poincloux R., Labrousse A., et al. Macrophage podosomes go 3D. Eur J Cell Biol 2011, 90(2-3):224.
20. Weaver A.M. Invadopodia: specialized cell structures for cancer invasion. Clin Exp Metastasis 2006, 23(2):97-105.
21. Stylli S.S., Kaye A.H., Lock P. Invadopodia: at the cutting edge of tumour invasion. JClin Neurosci 2008, 15(7):725-737.
22. Varon C., Tatin F., Moreau V., Van Obberghen-Schilling E., Fernandez-Sauze S., Reuzeau E., et al. Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol Cell Biol 2006, 26(9):3582-3594.
23. Diaz B., Shani G., Pass I., Anderson D., Quintavalle M., Courtneidge S.A. Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci Signal 2009, 2(88):ra53. 10.1126/scisignal.2000368.
24. Quintavalle M., Elia L., Condorelli G., Courtneidge S.A. MicroRNA control of podosome formation in vascular smooth muscle cells invivo and invitro. JCell Biol 2010, 189(1):13-22.
25. Collin O., Na S., Chowdhury F., Hong M., Shin M.E., Wang F., et al. Self-organized podosomes are dynamic mechanosensors. Curr Biol 2008, 18(17):1288-1294.
26. Alexander N.R., Branch K.M., Parekh A., Clark E.S., Iwueke I.C., Guelcher S.A., et al. Extracellular matrix rigidity promotes invadopodia activity. Curr Biol 2008, 18(17):1295-1299.
27. Chan B.P., Hui T.Y., Yeung C.W., Li J., Mo I., Chan G.C. Self-assembled collagen-human mesenchymal stem cell microspheres for regenerative medicine. Biomaterials 2007, 28:4652-4666.
28. Carlier M.F., Pantaloni D. Control of actin dynamics in cell motility. JMol Biol 1997, 269(4):459-467.
29. Mandelkow E., Mandelkow E.M. Microtubules and microtubule-associated proteins. Curr Opin Cell Biol 1995, 7:72-81.
30. Pekny M., Lane E.B. Intermediate filaments and stress. Exp Cell Res 2007, 313(10):2244-2254.
31. Yamaguchi H., Lorenz M., Kempiak S., Sarmiento C., Coniglio S., Symons M., et al. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. JCell Biol 2005, 168(3):441-452.
32. Li A., Dawson J.C., Forero-Vargas M., Spence H.J., Yu X., König I., et al. The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol 2010, 20(4):339-345.
33. Bowden E.T., Barth M., Thomas D., Glazer R.I., Mueller S.C. An invasion-related complex of cortactin, paxillin and PKCmu associates with invadopodia at sites of extracellular matrix degradation. Oncogene 1999, 18(31):4440-4449.
34. Hirooka S., Akashi T., Ando N., Suzuki Y., Ishida N., Kurata M., et al. Localization of the invadopodia-related proteins actinin-1 and cortactin to matrix-contact-side cytoplasm of cancer cells in surgically resected lung adenocarcinomas. Pathobiology 2011, 78(1):10-23.
35. Clark E.S., Whigham A.S., Yarbrough W.G., Weaver A.M. Cortactin is an essential regulator of matrix metalloproteinase secretion and extracellular matrix degradation in invadopodia. Cancer Res 2007, 67(9):4227-4235.
36. Nakahara H., Mueller S.C., Nomizu M., Yamada Y., Yeh Y., Chen W.T. Activation of beta1 integrin signaling stimulates tyrosine phosphorylation of p190RhoGAP and membrane-protrusive activities at invadopodia. JBiol Chem 1998, 273(1):9-12.
37. Hotary K., Allen E., Punturieri A., Yana I., Weiss S.J. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. JCell Biol 2000, 149(6):1309-1323.
38. Billinghurst R.C., Dahlberg L., Ionescu M., Reiner A., Bourne R., Rorabeck C., et al. Enhanced cleavage of type II collagen by collagenases in osteoarthritic articular cartilage. JClin Invest. 1997, 99(7):1534-1545.
39. Vignjevic D., Kojima S., Aratyn Y., Danciu O., Svitkina T., Borisy G.G. Role of fascin in filopodial protrusion. JCell Biol 2006, 174(6):863-875.
40. Surviladze Z., Waller A., Strouse J.J., Bologa C., Ursu O., Salas V., et al. Of Cdc42 GTPase. Probe reports from the NIH molecular libraries program 2010, National Center for Biotechnology Information (US), Bethesda (MD), 2010 Feb 27 [updated 2010 Dec 16].
41. Baker M.W., Macagno E.R. Invivo imaging of growth cone and filopodial dynamics: evidence for contact-mediated retraction of filopodia leading to the tiling of sibling processes. JComp Neurol 2007, 500(5):850-862.
42. Roberts L.A., Glenn H., Hahn C.S., Jacobson B.S. Cdc42 and RhoA are differentially regulated during arachidonate-mediated HeLa cell adhesion. JCell Physiol 2003, 196:196-205.
43. Sander E.E., ten Klooster, van Delft J.P., van der Kammen S., Collard R.A., Rac J.G., et al. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. JCell Biol 1999, 147:1009-1022.
44. Goldyn A.M., Rioja B.A., Spatz J.P., Ballestrem C., Kemkemer R. Force-induced cell polarisation is linked to RhoA-driven microtubule-independent focal-adhesion sliding. JCell Sci 2009, 122(20):3644-3651.
45. Moshfegh Y., Bravo-Cordero J.J., Miskolci V., Condeelis J., Hodgson L. ATrio-Rac1-Pak1 signalling axis drives invadopodia disassembly. Nat Cell Biol 2014, 16(6):574-586.
46. Di Martino J., Paysan L., Gest L.C., Lagrée V., Juin A., Saltel F., et al. Cdc42 and Tks5: a minimal and universal molecular signature for functional invadosomes. Cell Adh Migr 2014, 8(3):280-292.
47. Billottet C., Rottiers P., Tatin F., Varon C., Reuzeau E., Maître J.L., et al. Regulatory signals for endothelial podosome formation. Eur J Cell Biol 2008, 87(8-9):543-554.
48. Schliwa M. Action of cytochalasin D on cytoskeletal networks. JCell Biol 1982, 92(1):79-91.
49. Luo W., Yu C.H., Lieu Z.Z., Allard J., Mogilner A., Sheetz M.P., et al. Analysis of the local organization and dynamics of cellular actin networks. JCell Biol 2013, 202(7):1057-1073.
50. Eastwood M., Mudera V.C., McGrouther D.A., Brown R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil Cytoskelet 1998, 40:13-21.