Compliant 3D microenvironment improves β-cell cluster insulin expression through mechanosensing and β-catenin signaling

Tissue Engineering - Part A

Volumn 20, Issue 13-14, 2014, Pages 1888-1895

  Nyitray, Crystal E ^a   Chavez, Miquella G ^a,b   Desai, Tejal A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; GLUCOSE; INSULIN; MAINTENANCE; SCAFFOLDS (BIOLOGY); STIFFNESS;

INSULIN EXPRESSIONS; INSULIN SENSITIVITY; MECHANICAL CONTROL; MICROENVIRONMENTS; MYOSIN LIGHT CHAIN KINASE; REVERSIBLE CONTROL; STIMULATION INDICES; THERAPEUTIC SOLUTIONS;

CELL SIGNALING;

BETA CATENIN; COMPLEMENTARY DNA; GLUCOSE; INSULIN; MESSENGER RNA; MYOSIN LIGHT CHAIN KINASE; POLYACRYLAMIDE; RHO KINASE; WNT PROTEIN; ACRYLIC ACID RESIN; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL SURVIVAL; CHRONIC DISEASE; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HYDROGEL; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; INSULIN SENSITIVITY; MEASUREMENT; MICROENVIRONMENT; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RIGIDITY; TISSUE ENGINEERING; ANIMAL; CELL AGGREGATION; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; MECHANOTRANSDUCTION; METABOLISM; NUCLEAR SHAPE; TUMOR MICROENVIRONMENT;

ACRYLIC RESINS; ANIMALS; BETA CATENIN; CELL AGGREGATION; CELL NUCLEUS SHAPE; CELLULAR MICROENVIRONMENT; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MECHANOTRANSDUCTION, CELLULAR; MICE; MYOSIN-LIGHT-CHAIN KINASE; RHO-ASSOCIATED KINASES;

EID: 84904216607     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2013.0692     Document Type: Article

References (45)

1. Ryan, E.A., Paty, B.W., Senior, P.A., Bigam, D., Alfadhli, E., Kneteman, N.M., et al. Five-year follow-up after clinical islet transplantation. Diabetes 54, 2060, 2005.
2. Barton, F.B., Rickels, M.R., Alejandro, R., Hering, B.J., Wease, S., Naziruddin, B., et al. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care 35, 1436, 2012.
3. Stanekzai, J., Isenovic, E.R., and Mousa, S.A. Treatment options for diabetes: Potential role of stem cells. Diabetes Res Clin Pract 98, 359, 2012.
4. Caicedo, A. Paracrine and autocrine interactions in the human islet: more than meets the eye. Semin Cell Dev Biol 24, 11, 2013.
5. Barker, C.J., Leibiger, I.B., and Berggren, P.-O. The pancreatic islet as a signaling hub. Adv Biol Regul 53, 156, 2013.
6. Hauge-Evans, A.C., Squires, P.E., Persaud, S.J., and Jones, P.M. Pancreatic beta-cell-to-beta-cell interactions are required for integrated responses to nutrient stimuli: enhanced Ca2 + and insulin secretory responses of MIN6 pseudoislets. Diabetes 48, 1402, 1999.
7. Mendelsohn, A.D., Nyitray, C., Sena, M., and Desai, T.A. Size-controlled insulin-secreting cell clusters. Acta Biomater 8, 4278, 2012.
8. Chowdhury, A., Satagopam, V.P., Manukyan, L., Artemenko, K.A., Fung, Y.M.E., Schneider, R., et al. Signaling in insulin-secreting MIN6 pseudoislets and monolayer cells. J Proteome Res 12, 5954, 2013.
9. Chowdhury, A., Dyachok, O., Tengholm, A., Sandler, S., and Bergsten, P. Functional differences between aggregated and dispersed insulin-producing cells. Diabetologia 56, 1557, 2013.
10. Discher, D.E., Janmey, P., and Wang, Y.-L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139, 2005.
11. Butcher, D.T., Alliston, T., and Weaver, V.M. A tense situation: forcing tumour progression. Nat Rev Cancer 9, 108, 2009.
12. Lee, D.A., Knight, M.M., Campbell, J.J., and Bader, D.L. Stem cell mechanobiology. J Cell Biochem 112, 1, 2011.
13. Kraning-Rush, C.M., and Reinhart-King, C.A. Controlling matrix stiffness and topography for the study of tumor cell migration. Cell Adh Migr 6, 274, 2012.
14. Dahl, K.N., Booth-Gauthier, E.A., and Ladoux, B. In the middle of it all: mutual mechanical regulation between the nucleus and the cytoskeleton. J Biomech 43, 2, 2010.
15. Dahl, K.N., Ribeiro, A.J.S., and Lammerding, J. Nuclear shape, mechanics, and mechanotransduction. Circ Res 102, 1307, 2008.
16. Kim, A., Miller, K., Jo, J., Kilimnik, G., Wojcik, P., and Hara, M. Islet architecture: a comparative study. Islets 1, 129, 2009.
17. Yang, K.-C., Wu, C.-C., Yang, S.-H., Chiu, C.-C., Sumi, S., and Lee, H.-S. Investigating the suspension culture on aggregation and function of mouse pancreatic b-cells. J Biomed Mater Res A 101, 2273, 2013.
18. Kuehn, C., Dubiel, E.A., Sabra, G., and Vermette, P. Culturing INS-1 cells on CDPGYIGSR-, RGD- and fibronectin surfaces improves insulin secretion and cell proliferation. Acta Biomater 8, 619, 2012.
19. Merkwitz, C., Blaschuk, O.W., Schulz, A., Lochhead, P., Meister, J., Ehrlich, A., et al. The ductal origin of structural and functional heterogeneity between pancreatic islets. Prog Histochem Cytochem 48, 103, 2013.
20. Kshitiz, Park, J., Kim, P., Helen, W., Engler, A.J., Levchenko, A., et al. Control of stem cell fate and function by engineering physical microenvironments. Integr Biol (Camb) 4, 1008, 2012.
21. Cai, E.P., Casimir, M., Schroer, S.A., Luk, C.T., Shi, S.Y., Choi, D., et al. In vivo role of focal adhesion kinase in regulating pancreatic -cell mass and function through insulin signaling, actin dynamics, and granule trafficking. Diabetes 61, 1708, 2012.
22. Mitra, S.K., Hanson, D.A., and Schlaepfer, D.D. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 6, 56, 2005.
23. Provenzano, P.P., and Keely, P.J. The role of focal adhesion kinase in tumor initiation and progression. Cell Adh Migr 3, 347, 2009.
24. Zebda, N., Dubrovskyi, O., and Birukov, K.G. Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc Res 83, 71, 2012.
25. Amano, M., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y., et al. Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308, 1997.
26. Vicente-Manzanares, M., Ma, X., Adelstein, R.S., and Horwitz, A.R. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10, 778, 2009.
27. Hartshorne, D.J., Ito, M., and Erdödi, F. Myosin light chain phosphatase: subunit composition, interactions and regulation. J Muscle Res Cell Motil 19, 325, 1998.
28. Kamm, K.E., and Stull, J.T. Dedicated myosin light chain kinases with diverse cellular functions. J Biol Chem 276, 4527, 2001.
29. Somlyo, A.P., and Somlyo, A.V. Ca2 + sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83, 1325, 2003.
30. Gautel, M. Cytoskeletal protein kinases: titin and its relations in mechanosensing. Pflugers Arch 462, 119, 2011.
31. Leckband, D.E., le Duc, Q., Wang, N., and de Rooij, J. Mechanotransduction at cadherin-mediated adhesions. Curr Opin Cell Biol 23, 523, 2011.
32. Abiola, M., Favier, M., Christodoulou-Vafeiadou, E., Pichard, A.-L., Martelly, I., and Guillet-Deniau, I. Activation of Wnt/b-catenin signaling increases insulin sensitivity through a reciprocal regulation of Wnt10b and SREBP-1c in skeletal muscle cells. PLoS One 4, e8509, 2009.
33. Yoon, J.C., Ng, A., Kim, B.H., Bianco, A., Xavier, R.J., and Elledge, S.J. Wnt signaling regulates mitochondrial physiology and insulin sensitivity. Genes Dev 24, 1507, 2010.
34. Hohmeier, H.E., Mulder, H., Chen, G., Henkel-Rieger, R., Prentki, M., and Newgard, C.B. Isolation of INS-1-derived cell lines with robust ATP-sensitive K+ channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424, 2000.
35. Orive, G., Tam, S.K., Pedraz, J.L., and Hallé, J.-P. Biocompatibility of alginate-poly-L-lysine microcapsules for cell therapy. Biomaterials 27, 3691, 2006.
36. Martin, Y., and Vermette, P. Bioreactors for tissue mass culture: design, characterization, and recent advances. Biomaterials 26, 7481, 2005.
37. Weber, L.M., Hayda, K.N., and Anseth, K.S. Cell-matrix interactions improve beta-cell survival and insulin secretion in three-dimensional culture. Tissue Eng Part A 14, 1959, 2008.
38. Lim, D.-J., Antipenko, S.V., Vines, J.B., Andukuri, A., Hwang, P.T.J., Hadley, N.T., et al. Improved MIN6 b-cell function on self-assembled peptide amphiphile nanomatrix inscribed with extracellular matrix-derived cell adhesive ligands. Macromol Biosci 13, 1404, 2013.
39. Raza, A., Ki, C.S., and Lin, C.-C. The influence of matrix properties on growth and morphogenesis of human pancreatic ductal epithelial cells in 3D. Biomaterials 34, 5117, 2013.
40. Maillard, E., Sencier, M.-C., Langlois, A., Bietiger, W., Krafft, M., Pinget, M., et al. Extracellular matrix proteins involved in pseudoislets formation. Islets 1, 232, 2009.
41. Riopel, M., Stuart, W., and Wang, R. Fibrin improves beta (INS-1) cell function, proliferation and survival through integrin avb3. Acta Biomater 9, 8140, 2013.
42. Yee, K.L., Weaver, V.M., and Hammer, D.A. Integrinmediated signalling through the MAP-kinase pathway. IET Syst Biol 2, 8, 2008.
43. Versaevel, M., Grevesse, T., and Gabriele, S. Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat Commun 3, 671, 2012.
44. Thomas, C.H., Collier, J.H., Sfeir, C.S., and Healy, K.E. Engineering gene expression and protein synthesis by modulation of nuclear shape. Proc Natl Acad Sci U S A 99, 1972, 2002.
45. Guilak, F. Compression-induced changes in the shape and volume of the chondrocyte nucleus. J Biomech 28, 1529, 1995.