A role for matrix stiffness in the regulation of cardiac side population cell function

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 9, 2015, Pages H990-H997

  Qiu, Yiling ^a   Bayomy, Ahmad F ^a,b   Gomez, Marcus V ^a   Bauer, Michael ^a   Du, Ping ^c   Yang, Yanfei ^a   Zhang, Xin ^c   Liao, Ronglih ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c Boston University   (United States)

Author keywords

Cardiac side population cell; Cell cycle regulation; Cellular ageing; Differentiation; Matrix stiffness; Proliferation

Indexed keywords

DIMETICONE; DNA NUCLEOTIDYLEXOTRANSFERASE; LAMININ; BAYSILON;

ADULT; ANIMAL CELL; ARTICLE; CARDIAC SIDE POPULATION CELL; CARDIAC STEM CELL; CELL ADHESION; CELL AGING; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL DIVISION; CELL FUNCTION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; MALE; MATRIX STIFFNESS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; RIGIDITY; SIDE POPULATION CELL; TUNEL ASSAY; UPREGULATION; YOUNG MODULUS; ADULT STEM CELL; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL CYCLE; CHEMISTRY; COCULTURE; HEART MUSCLE CELL; MECHANOTRANSDUCTION; METABOLISM; PHENOTYPE; PHYSIOLOGY; SHEEP; STEM CELL NICHE; TIME;

ADULT STEM CELLS; ANIMALS; CELL ADHESION; CELL AGING; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DIMETHYLPOLYSILOXANES; ELASTIC MODULUS; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE, INBRED C57BL; MYOCYTES, CARDIAC; PHENOTYPE; SHEEP; SIDE-POPULATION CELLS; STEM CELL NICHE; TIME FACTORS;

EID: 84929698433     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00935.2014     Document Type: Article

References (50)

1. Ai H, Lvov YM, Mills DK, Jennings M, Alexander JS, Jones SA. Coating and selective deposition of nanofilm on silicone rubber for cell adhesion and growth. Cell Biochem Biophys 38: 103–114, 2003.
2. American Type Culture Collection. ATCC Animal Cell Culture Guide: Tips and Techniques for Continuous Cell Lines. Manassas, VA: ATCC, 2014. http://www.atcc.org/-/media/PDFs/Culture%20Guides/AnimCellCulture_Guide.ashx.
3. Banks JM, Mozdzen LC, Harley BAC, Bailey RC. The combined effects of matrix stiffness and growth factor immobilization on the bioactivity and differentiation capabilities of adipose-derived stem cells. Biomaterials 35: 8951–8959, 2014.
4. Beltrami AP, Barlucchi L, Torella D, Baker M, Limana F, Chimenti S, Kasahara H, Rota M, Musso E, Urbanek K, Leri A, Kajstura J, Nadal-Ginard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114: 763–776, 2003.
5. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisen J. Evidence for cardiomyocyte renewal in humans. Science 324: 98–102, 2009.
6. Berry MF, Engler AJ, Woo YJ, Pirolli TJ, Bish LT, Jayasankar V, Morine KJ, Gardner TJ, Discher DE, Sweeney HL. Mesenchymal stem cell injection after myocardial infarction improves myocardial compliance. Am J Physiol Heart Circ Physiol 290: H2196–H2203, 2006.
7. Brown XQ, Ookawa K, Wong JY. Evaluation of polydimethylsiloxane scaffolds with physiologically-relevant elastic moduli: interplay of substrate mechanics and surface chemistry effects on vascular smooth muscle cell response. Biomaterials 26: 3123–3129, 2005.
8. Campisi J, Kim Sh Lim CS, Rubio M. Cellular senescence, cancer and aging: the telomere connection. Exp Gerontol 36: 1619–1637, 2001.
9. Derradji H, Bekaert S, van Oostveldt P, Baatout S. Comparison of different protocols for telomere length estimation by combination of quantitative fluorescence in situ hybridization (Q-FISH) and flow cytometry in human cancer cell lines. Anticancer Res 25: 1039–1050, 2005.
10. Discher DE, Mooney DJ, Zandstra PW. Growth factors, matrices, and forces combine and control stem cells. Science 324: 1673–1677, 2009.
11. Engler AJ, Carag-Krieger C, Johnson CP, Raab M, Tang HY, Speicher DW, Sanger JW, Sanger JM, Discher DE. Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 121: 3794–3802, 2008.
12. Evans ND, Minelli C, Gentleman E, LaPointe V, Patankar SN, Kallivretaki M, Chen X, Roberts CJ, Stevens MM. Substrate stiffness affects early differentiation events in embryonic stem cells. Eur Cell Mater 18: 1–13, 2009.
13. Fisch S, Gray S, Heymans S, Haldar SM, Wang B, Pfister O, Cui L, Kumar A, Lin Z, Sen-Banerjee S, Das H, Petersen CA, Mende U, Burleigh BA, Zhu Y, Pinto Y, Liao R, Jain MK. Kruppel-like factor 15 is a regulator of cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 104: 7074–7079, 2007.
14. Gershlak JR, Resnikoff JI, Sullivan KE, Williams C, Wang RM, Black LD. Mesenchymal stem cells ability to generate traction stress in response to substrate stiffness is modulated by the changing extracellular matrix composition of the heart during development. Biochem Biophys Res Commun 439: 161–166, 2013.
15. Gulino A, Di Marcotullio L, Screpanti I. The multiple functions of Numb. Exp Cell Res 316: 900–906, 2010.
16. Heras-Bautista CO, Katsen-Globa A, Schloerer NE, Dieluweit S, Abd El Aziz OM, Peinkofer G, Attia WA, Khalil M, Brockmeier K, Hescheler J, Pfannkuche K. The influence of physiological matrix conditions on permanent culture of induced pluripotent stem cell-derived cardiomyocytes. Biomaterials 35: 7374–7385, 2014.
17. Hierlihy AM, Seale P, Lobe CG, Rudnicki MA, Megeney LA. The post-natal heart contains a myocardial stem cell population. FEBS Lett 530: 239–243, 2002.
18. Hiesinger W, Brukman MJ, McCormick RC, Fitzpatrick JR, Frederick JR, Yang EC, Muenzer JR, Marotta NA, Berry MF, Atluri P, Woo YJ. Myocardial tissue elastic properties determined by atomic force microscopy after stromal cell-derived factor 1alpha angiogenic therapy for acute myocardial infarction in a murine model. J Thorac Cardiovasc Surg 143: 962–966, 2012.
19. Hsieh PC, Segers VF, Davis ME, MacGillivray C, Gannon J, Molkentin JD, Robbins J, Lee RT. Evidence from a genetic fate-mapping study that stem cells refresh adult mammalian cardiomyocytes after injury. Nat Med 13: 970–974, 2007.
20. Huang S, Ingber DE. The structural and mechanical complexity of cell-growth control. Nat Cell Biol 1: E131–E138, 1999.
21. Jacot JG, Dianis S, Schnall J, Wong JY. A simple microindentation technique for mapping the microscale compliance of soft hydrated materials and tissues. J Biomed Mater Res A 79: 485–494, 2006.
22. Jacot JG, McCulloch AD, Omens JH. Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 95: 3479–3487, 2008.
23. Kissel CK, Lehmann R, Assmus B, Aicher A, Honold J, Fischer- Rasokat U, Heeschen C, Spyridopoulos I, Dimmeler S, Zeiher AM. Selective functional exhaustion of hematopoietic progenitor cells in the bone marrow of patients with postinfarction heart failure. J Am Coll Cardiol 49: 2341–2349, 2007.
24. Klug WS, Cummings MR, Spencer CA, Palladino MA (editors). Concepts of Genetics. San Francisco: Pearson, 2011.
25. Kothapalli CR, Kamm RD. 3D matrix microenvironment for targeted differentiation of embryonic stem cells into neural and glial lineages. Biomaterials 34: 5995–6007, 2013.
26. Kubo H, Jaleel N, Kumarapeli A, Berretta RM, Bratinov G, Shan X, Wang H, Houser SR, Margulies KB. Increased cardiac myocyte progenitors in failing human hearts. Circulation 118: 649–657, 2008.
27. Lee IC, Wu YC, Cheng EM, Yang WT. Biomimetic niche for neural stem cell differentiation using poly-L-lysine/hyaluronic acid multilayer films. J Biomater Appl 2014 Dec 12. pii: 0885328214563341. [Epub ahead of print].
28. Leri A, Kajstura J, Anversa P. Cardiac stem cells and mechanisms of myocardial regeneration. Physiol Rev 85: 1373–1416, 2005.
29. Li Z, Guo X, Palmer AF, Das H, Guan J. High-efficiency matrix modulus-induced cardiac differentiation of human mesenchymal stem cells inside a thermosensitive hydrogel. Acta Biomater 8: 3586–3595, 2012.
30. Lin IK, Ou KS, Liao YM, Liu Y, Chen KS, Zhang X. Viscoelastic characterization and modeling of polymer transducers for biological applications. J Microelectromech Syst 18: 1087–1099, 2009.
31. Morrison SJ, Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441: 1068–1074, 2006.
32. Mouquet F, Pfister O, Jain M, Oikonomopoulos A, Ngoy S, Summer R, Fine A, Liao R. Restoration of cardiac progenitor cells after myocardial infarction by self-proliferation and selective homing of bone marrowderived stem cells. Circ Res 97: 1090–1092, 2005.
33. Nii M, Lai JH, Keeney M, Han LH, Behn A, Imanbayev G, Yang F. The effects of interactive mechanical and biochemical niche signaling on osteogenic differentiation of adipose-derived stem cells using combinatorial hydrogels. Acta Biomater 9: 5475–5483, 2013.
34. Oeseburg H, Westenbrink BD, de Boer RA, van Gilst WH, van Veldhuisen DJ, van der Harst P. Can critically short telomeres cause functional exhaustion of progenitor cells in postinfarction heart failure? J Am Coll Cardiol 50: 1911–1912, 2007.
35. Oh H, Bradfute SB, Gallardo TD, Nakamura T, Gaussin V, Mishina Y, Pocius J, Michael LH, Behringer RR, Garry DJ, Entman ML, Schneider MD. Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100: 12313–12318, 2003.
36. Park JS, Chu JS, Tsou AD, Diop R, Tang Z, Wang A, Li S. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-O. Biomaterials 32: 3921–3930, 2011.
37. Pek YS, Wan ACA, Ying JY. The effect of matrix stiffness on mesenchymal stem cell differentiation in a 3D thixotropic gel. Biomaterials 31: 385–391, 2010.
38. Pfister O, Mouquet F, Jain M, Summer R, Helmes M, Fine A, Colucci WS, Liao R. CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97: 52–61, 2005.
39. Rowlands AS, George PA, Cooper-White JJ. Directing osteogenic and myogenic differentiation of MSCs: interplay of stiffness and adhesive ligand presentation. Am J Physiol Cell Physiol 295: C1037–C1044, 2008.
40. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, Kashiwagi S, Fukami K, Miyata T, Miyoshi H, Imamura T, Ogawa M, Masai H, Miyawaki A. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132: 487–498, 2008.
41. Sereti KI, Oikonomopoulos A, Unno K, Cao X, Qiu Y, Liao R. ATP-binding cassette G-subfamily transporter 2 regulates cell cycle progression and asymmetric division in mouse cardiac side population progenitor cells. Circ Res 112: 27–34, 2013.
42. Sereti KI, Oikonomopoulos A, Unno K, Liao R. Methods to study the proliferation and differentiation of cardiac side population (CSP) cells. Methods Mol Biol 1036: 95–106, 2013.
43. Shapira-Schweitzer K, Seliktar D. Matrix stiffness affects spontaneous contraction of cardiomyocytes cultured within a PEGylated fibrinogen biomaterial. Acta Biomater 3: 33–41, 2007.
44. Shih YR, Tseng KF, Lai HY, Lin CH, Lee OK. Matrix stiffness regulation of integrin-mediated mechanotransduction during osteogenic differentiation of human mesenchymal stem cells. J Bone Miner Res 26: 730–738, 2011.
45. Sullivan KE, Quinn KP, Tang KM, Georgakoudi I, Black LD. Extracellular matrix remodeling following myocardial infarction influences the therapeutic potential of mesenchymal stem cells. Stem Cell Res Ther 5: 14–14, 2014.
46. Urbanek K, Torella D, Sheikh F, De Angelis A, Nurzynska D, Silvestri F, Beltrami CA, Bussani R, Beltrami AP, Quaini F, Bolli R, Leri A, Kajstura J, Anversa P. Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc Natl Acad Sci USA 102: 8692–8697, 2005.
47. Wang LS, Boulaire J, Chan PPY, Chung JE, Kurisawa M. The role of stiffness of gelatin-hydroxyphenylpropionic acid hydrogels formed by enzyme-mediated crosslinking on the differentiation of human mesenchymal stem cell. Biomaterials 31: 8608–8616, 2010.
48. Wozniak MA, Chen CS. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 10: 34–43, 2009.
49. Yu H, Tay CY, Pal M, Leong WS, Li H, Wen F, Leong DT, Tan LP. A bio-inspired platform to modulate myogenic differentiation of human mesenchymal stem cells through focal adhesion regulation. Adv Healthc Mater 2: 442–449, 2013.
50. Zhang S, Ma X, Yao K, Zhu H, Huang Z, Shen L, Qian J, Zou Y, Sun A, Ge J. Combination of CD34-positive cell subsets with infarcted myocardium-like matrix stiffness: a potential solution to cell-based cardiac repair. J Cell Mol Med 18: 1236–1238, 2014.