Stable, covalent attachment of laminin to microposts improves the contractility of mouse neonatal cardiomyocytes

ACS Applied Materials and Interfaces

Volumn 6, Issue 17, 2014, Pages 15516-15526

  Ribeiro, Alexandre J S ^a,b   Zaleta Rivera, Kathia ^b,c   Ashley, Euan A ^b,c   Pruitt, Beth L ^a,b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

3 aminopropyltriethoxysilane; 3 glycidoxypropyltrimethoxysilane; contractility; glutaraldehyde; neonatal cardiomyocytes; poly(dimethylsiloxane) microposts; surface functionalization

Indexed keywords

BIOCHEMISTRY; CARDIOLOGY; HEART; POLYDIMETHYLSILOXANE; PROTEINS; SILICONES; STABILITY; SURFACE MEASUREMENT;

3-AMINOPROPYLTRIETHOXYSILANE; 3-GLYCIDOXYPROPYLTRIMETHOXYSILANE; CARDIOMYOCYTES; CONTRACTILITY; GLUTARALDEHYDES; SURFACE FUNCTIONALIZATION;

DISEASES;

3-GLYCIDOXYPROPYLTRIMETHOXYSILANE; AMINO-PROPYL-TRIETHOXYSILANE; BAYSILON; DIMETICONE; ELASTOMER; LAMININ; PROPYLAMINE; SILANE DERIVATIVE;

ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FLUORESCENCE; HEART CONTRACTION; HEART MUSCLE CELL; IMMOBILIZED CELL; MOUSE; NEWBORN; PHYSIOLOGY; TIME;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CELLS, IMMOBILIZED; DIMETHYLPOLYSILOXANES; ELASTOMERS; FLUORESCENCE; LAMININ; MICE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PROPYLAMINES; SILANES; TIME FACTORS;

EID: 84907829546     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/am5042324     Document Type: Article

References (70)

1. Go, A. S.; Mozaffarian, D.; Roger, V. r. L.; Benjamin, E. J.; Berry, J. D.; Borden, W. B.; Bravata, D. M.; Dai, S.; Ford, E. S.; Fox, C. S.; Franco, S.; Fullerton, H. J.; Gillespie, C.; Hailpern, S. M.; Heit, J. A.; Howard, V. J.; Huffman, M. D.; Kissela, B. M.; Kittner, S. J.; Lackland, D. T.; Lichtman, J. H.; Lisabeth, L. D.; Magid, D.; Marcus, G. M.; Marelli, A.; Matchar, D. B.; McGuire, D. K.; Mohler, E. R.; Moy, C. S.; Mussolino, M. E.; Nichol, G.; Paynter, N. P.; Schreiner, P. J.; Sorlie, P. D.; Stein, J.; Turan, T. N.; Virani, S. S.; Wong, N. D.; Woo, D.; Turner, M. B. Heart Disease and Stroke Statistics-2013 Update: A Report from the American Heart Association Circulation 2013, 127, e6-e245
2. Strobeck, J. E.; Krueger, J.; Sonnenblick, E. H. Load and Time Considerations in the Force-Length Relation of Cardiac Muscle Fed. Proc. 1980, 39, 175-182
3. Fan, G. C.; Yuan, Q.; Zhao, W.; Chu, G.; Kranias, E. G. Junctin Is a Prominent Regulator of Contractility in Cardiomyocytes Biochem. Biophys. Res. Commun. 2007, 352, 617-622
4. Iribe, G.; Helmes, M.; Kohl, P. Force-Length Relations in Isolated Intact Cardiomyocytes Subjected to Dynamic Changes in Mechanical Load Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H1487-H1497
5. Oliveira, S. M.; Zhang, Y. H.; Solis, R. S.; Isackson, H.; Bellahcene, M.; Yavari, A.; Pinter, K.; Davies, J. K.; Ge, Y.; Ashrafian, H.; Walker, J. W.; Carling, D.; Watkins, H.; Casadei, B.; Redwood, C. Amp-Activated Protein Kinase Phosphorylates Cardiac Troponin I and Alters Contractility of Murine Ventricular Myocytes Circ. Res. 2012, 110, 1192-1201
6. Lockhart, M.; Wirrig, E.; Phelps, A.; Wessels, A. Extracellular Matrix and Heart Development Birth Defects Res., Part A 2011, 91, 535-550
7. Spinale, F. G.; Zile, M. R. Integrating the Myocardial Matrix into Heart Failure Recognition and Management Circ. Res. 2013, 113, 725-738
8. Mishra, P. K.; Givvimani, S.; Chavali, V.; Tyagi, S. C. Cardiac Matrix: A Clue for Future Therapy Biochim. Biophys. Acta 2013, 1832, 2271-2276
9. Taylor, R. E.; Kim, K.; Sun, N.; Park, S. J.; Sim, J. Y.; Fajardo, G.; Bernstein, D.; Wu, J. C.; Pruitt, B. L. Sacrificial Layer Technique for Axial Force Post Assay of Immature Cardiomyocytes Biomed. Microdevices 2013, 15, 171-181
10. Rodriguez, A. G.; Han, S. J.; Regnier, M.; Sniadecki, N. J. Substrate Stiffness Increases Twitch Power of Neonatal Cardiomyocytes in Correlation with Changes in Myofibril Structure and Intracellular Calcium Biophys. J. 2011, 101, 2455-2464
11. Domke, J.; Parak, W. J.; George, M.; Gaub, H. E.; Radmacher, M. Mapping the Mechanical Pulse of Single Cardiomyocytes with the Atomic Force Microscope Eur. Biophys. J. 1999, 28, 179-186
12. Sweitzer, N. K.; Moss, R. L. Determinants of Loaded Shortening Velocity in Single Cardiac Myocytes Permeabilized with Alpha-Hemolysin Circ. Res. 1993, 73, 1150-1162
13. Louch, W. E.; Sheehan, K. A.; Wolska, B. M. Methods in Cardiomyocyte Isolation, Culture, and Gene Transfer J. Mol. Cell. Cardiol. 2011, 51, 288-298
14. Bird, S. D.; Doevendans, P. A.; van Rooijen, M. A.; Brutel de la Riviere, A.; Hassink, R. J.; Passier, R.; Mummery, C. L. The Human Adult Cardiomyocyte Phenotype Cardiovasc. Res. 2003, 58, 423-434
15. McCain, M. L.; Parker, K. K. Mechanotransduction: The Role of Mechanical Stress, Myocyte Shape, and Cytoskeletal Architecture on Cardiac Function Pfluegers Arch. 2011, 462, 89-104
16. Schoen, I.; Pruitt, B. L.; Vogel, V. The Yin-Yang of Rigidity Sensing: How Forces and Mechanical Properties Regulate the Cellular Response to Materials Annu. Rev. Mater. Res. 2013, 43, 589-618
17. Wipff, P. J.; Majd, H.; Acharya, C.; Buscemi, L.; Meister, J. J.; Hinz, B. The Covalent Attachment of Adhesion Molecules to Silicone Membranes for Cell Stretching Applications Biomaterials 2009, 30, 1781-1789
18. Kuddannaya, S.; Chuah, Y. J.; Lee, M. H.; Menon, N. V.; Kang, Y.; Zhang, Y. Surface Chemical Modification of Poly(Dimethylsiloxane) for the Enhanced Adhesion and Proliferation of Mesenchymal Stem Cells ACS Appl. Mater. Interfaces 2013, 5, 9777-9784
19. Rocha-Resende, C.; Roy, A.; Resende, R.; Ladeira, M. S.; Lara, A.; de Morais Gomes, E. R.; Prado, V. F.; Gros, R.; Guatimosim, C.; Prado, M. A.; Guatimosim, S. Non- Neuronal Cholinergic Machinery Present in Cardiomyocytes Offsets Hypertrophic Signals J. Mol. Cell. Cardiol. 2012, 53, 206-216
20. Berk, B. C.; Fujiwara, K.; Lehoux, S. Ecm Remodeling in Hypertensive Heart Disease J. Clin. Invest. 2007, 117, 568-575
21. Donker, D. W.; Maessen, J. G.; Verheyen, F.; Ramaekers, F. C.; Spatjens, R. L.; Kuijpers, H.; Ramakers, C.; Schiffers, P. M.; Vos, M. A.; Crijns, H. J.; Volders, P. G. Impact of Acute and Enduring Volume Overload on Mechanotransduction and Cytoskeletal Integrity of Canine Left Ventricular Myocardium Am. J. Physiol. Heart Circ. Physiol. 2007, 292, H2324-H2332
22. Hein, S.; Schaper, J. The Extracellular Matrix in Normal and Diseased Myocardium J. Nucl. Cardiol. 2001, 8, 188-196
23. Colognato, H.; Winkelmann, D. A.; Yurchenco, P. D. Laminin Polymerization Induces a Receptor-Cytoskeleton Network J. Cell Biol. 1999, 145, 619-631
24. Dennis, R. G.; Kosnik, P. E., II. Excitability and Isometric Contractile Properties of Mammalian Skeletal Muscle Constructs Engineered in Vitro In Vitro Cell. Dev. Biol.: Anim. 2000, 36, 327-335
25. Innocenzi, P.; Kidchob, T.; Yoko, T. Hybrid Organic-Inorganic Sol-Gel Materials Based on Epoxy-Amine Systems J. Sol-Gel Sci. Technol. 2005, 35, 225-235
26. Vandenberg, E. T.; Krull, U. J. The Prevention of Adsorption of Interferents to Radiolabelled Protein by Tween 20 J. Biochem. Biophys. Methods 1991, 22, 269-277
27. Weetall, H. H. Preparation of Immobilized Proteins Covalently Coupled through Silane Coupling Agents to Inorganic Supports Appl. Biochem. Biotechnol. 1993, 41, 157-188
28. Toworfe, G. K.; Bhattacharyya, S.; Composto, R. J.; Adams, C. S.; Shapiro, I. M.; Ducheyne, P. Effect of Functional End Groups of Silane Self-Assembled Monolayer Surfaces on Apatite Formation, Fibronectin Adsorption and Osteoblast Cell Function J. Tissue Eng. Regener. Med. 2009, 3, 26-36
29. Devic, E.; Xiang, Y.; Gould, D.; Kobilka, B. Beta-Adrenergic Receptor Subtype- Specific Signaling in Cardiac Myocytes from Beta(1) and Beta(2) Adrenoceptor Knockout Mice Mol. Pharmacol. 2001, 60, 577-583
30. Kuhn, J. R.; Poenie, M. Dynamic Polarization of the Microtubule Cytoskeleton During Ctl-Mediated Killing Immunity 2002, 16, 111-121
31. Wu, Y.; Hussain, M.; Fassihi, R. Development of a Simple Analytical Methodology for Determination of Glucosamine Release from Modified Release Matrix Tablets J. Pharm. Biomed. Anal. 2005, 38, 263-269
32. Abass, A. K. Study the Effects Influencing the Adsorption of Toluidine Blue O (Tbo) Dye onto Mno2 Surface Iraqi Natl. J. Chem. 2008, 306-322
33. Dancey, C.; Reidy, J.; Rowe, R. Statistics for the Health Sciences: A Non-Mathematical Introduction; SAGE Publications: Thousand Oaks, CA, 2012; Chapter 7, pp 237-240.
34. Ramos-Vara, J. A. Technical Aspects of Immunohistochemistry Vet. Pathol. 2005, 42, 405-426
35. Chen, X.; Cui, D.; Li, H.; Cai, H.; Sun, J.; Chen, J. Microfluidics-Based Immunoassays by Using an Integrated Fluorescence Detection System Microsyst. Technol. 2010, 16, 2049-2055
36. Lee, M. H.; Brass, D. A.; Morris, R.; Composto, R. J.; Ducheyne, P. The Effect of Non- Specific Interactions on Cellular Adhesion Using Model Surfaces Biomaterials 2005, 26, 1721-1730
37. Lee, D.; Yang, S. Surface Modification of Pdms by Atmospheric-Pressure Plasma- Enhanced Chemical Vapor Deposition and Analysis of Long-Lasting Surface Hydrophilicity Sens. Actuators, B 2012, 162, 425-434
38. Ekblom, P.; Lonai, P.; Talts, J. F. Expression and Biological Role of Laminin-1 Matrix Biol. 2003, 22, 35-47
39. Mohanty, B.; Bohidar, H. B. Systematic of Alcohol-Induced Simple Coacervation in Aqueous Gelatin Solutions Biomacromolecules 2003, 4, 1080-1086
40. Cheng, Y. S.; Champliaud, M. F.; Burgeson, R. E.; Marinkovich, M. P.; Yurchenco, P. D. Self-Assembly of Laminin Isoforms J. Biol. Chem. 1997, 272, 31525-31532
41. Lee, M. H.; Boettiger, D.; Ducheyne, P.; Composto, R. J. Self-Assembled Monolayers of Omega-Functional Silanes: A Platform for Understanding Cellular Adhesion at the Molecular Level. In Silanes and Other Coupling Agents, Vol. 4; Mittal, K. L., Ed.; CRC Press, Taylor & Francis Group, LLC: Boca Raton, FL, 2007; Part 1, pp 163-178.
42. Zhou, J.; Ellis, A. V.; Voelcker, N. H. Recent Developments in PDMS Surface Modification for Microfluidic Devices Electrophoresis 2010, 31, 2-16
43. Wang, A.; Tang, H.; Cao, T.; Salley, S. O.; Ng, K. Y. In Vitro Stability Study of Organosilane Self-Assemble Monolayers and Multilayers J. Colloid Interface Sci. 2005, 291, 438-447
44. Bray, M. A.; Sheehy, S. P.; Parker, K. K. Sarcomere Alignment Is Regulated by Myocyte Shape Cell Motil. Cytoskeleton 2008, 65, 641-651
45. Ruggiero, C.; Mantelli, M.; Curtis, A.; Zhang, S.; Rolfe, P. Computer Modelling of the Adsorption of Proteins on Solid Surfaces under the Influence of Double Layer and Van Der Waals Energy Med. Biol. Eng. Comput. 1999, 37, 119-124
46. Williams, R. L.; Wilson, D. J.; Rhodes, N. P. Stability of Plasma-Treated Silicone Rubber and Its Influence on the Interfacial Aspects of Blood Compatibility Biomaterials 2004, 25, 4659-4673
47. Koo, L. Y.; Irvine, D. J.; Mayes, A. M.; Lauffenburger, D. A.; Griffith, L. G. Co-Regulation of Cell Adhesion by Nanoscale RGD Organization and Mechanical Stimulus J. Cell Sci. 2002, 115, 1423-1433
48. Zielinski, R.; Mihai, C.; Kniss, D.; Ghadiali, S. N. Finite Element Analysis of Traction Force Microscopy: Influence of Cell Mechanics, Adhesion, and Morphology J. Biomech. Eng. 2013, 135, 71009
49. Gad, A. K.; Ronnlund, D.; Spaar, A.; Savchenko, A. A.; Petranyi, G.; Blom, H.; Szekely, L.; Widengren, J.; Aspenstrom, P. Rho GTPases Link Cellular Contractile Force to the Density and Distribution of Nanoscale Adhesions FASEB J. 2012, 26, 2374-2382
50. Khan, R.; Sheppard, R. Fibrosis in Heart Disease: Understanding the Role of Transforming Growth Factor-Beta in Cardiomyopathy, Valvular Disease and Arrhythmia Immunology 2006, 118, 10-24
51. LaFramboise, W. A.; Scalise, D.; Stoodley, P.; Graner, S. R.; Guthrie, R. D.; Magovern, J. A.; Becich, M. J. Cardiac Fibroblasts Influence Cardiomyocyte Phenotype in Vitro Am. J. Physiol.: Cell Physiol. 2007, 292, C1799-1808
52. Stastna, M.; Chimenti, I.; Marban, E.; Van Eyk, J. E. Identification and Functionality of Proteomes Secreted by Rat Cardiac Stem Cells and Neonatal Cardiomyocytes Proteomics 2010, 10, 245-253
53. Simpson, P.; McGrath, A.; Savion, S. Myocyte Hypertrophy in Neonatal Rat Heart Cultures and Its Regulation by Serum and by Catecholamines Circ. Res. 1982, 51, 787-801
54. Deng, X. F.; Rokosh, D. G.; Simpson, P. C. Autonomous and Growth Factor-Induced Hypertrophy in Cultured Neonatal Mouse Cardiac Myocytes. Comparison with Rat Circ. Res. 2000, 87, 781-788
55. Husse, B.; Wussling, M. Developmental Changes of Calcium Transients and Contractility During the Cultivation of Rat Neonatal Cardiomyocytes Mol. Cell. Biochem. 1996, 163-164, 13-21
56. 2+Currents from Newborn Rat Cardiomyocytes in Primary Culture Pfluegers Arch. 1994, 428, 241-249
57. Roa Romero, L. M.; Felgueiras, H.; Migonney, V.; Sommerfeld, S.; Murthy, N. S.; Kohn, J., Competitive Adsorption of Albumin, Fibronectin and Collagen Type I on Different Biomaterial Surfaces: A Qcm-D Study. In XIII Mediterranean Conference on Medical and Biological Engineering and Computing 2013; Springer International Publishing: New York, 2013; pp 1597-1600.
58. Hohenester, E.; Engel, J. Domain Structure and Organisation in Extracellular Matrix Proteins Matrix Biol. 2002, 21, 115-128
59. Graf, J.; Iwamoto, Y.; Sasaki, M.; Martin, G. R.; Kleinman, H. K.; Robey, F. A.; Yamada, Y. Identification of an Amino Acid Sequence in Laminin Mediating Cell Attachment, Chemotaxis, and Receptor Binding Cell 1987, 48, 989-996
60. Anand, G.; Sharma, S.; Dutta, A. K.; Kumar, S. K.; Belfort, G. Conformational Transitions of Adsorbed Proteins on Surfaces of Varying Polarity Langmuir 2010, 26, 10803-10811
61. De Arcangelis, A.; Neuville, P.; Boukamel, R.; Lefebvre, O.; Kedinger, M.; Simon- Assmann, P. Inhibition of Laminin Alpha 1-Chain Expression Leads to Alteration of Basement Membrane Assembly and Cell Differentiation J. Cell Biol. 1996, 133, 417-430
62. Castaldo, C.; Di Meglio, F.; Nurzynska, D.; Romano, G.; Maiello, C.; Bancone, C.; Muller, P.; Bohm, M.; Cotrufo, M.; Montagnani, S. Cd117-Positive Cells in Adult Human Heart Are Localized in the Subepicardium, and Their Activation Is Associated with Laminin-1 and Alpha6 Integrin Expression Stem Cells 2008, 26, 1723-1731
63. Adachi, T.; Shibata, S.; Okamoto, Y.; Sato, S.; Fujisawa, S.; Ohba, T.; Ono, K. The Mechanism of Increased Postnatal Heart Rate and Sinoatrial Node Pacemaker Activity in Mice J. Physiol. Sci. 2013, 63, 133-146
64. Luyken, J.; Hannan, R. D.; Cheung, J. Y.; Rothblum, L. I. Regulation of Rdna Transcription During Endothelin-1-Induced Hypertrophy of Neonatal Cardiomyocytes. Hyperphosphorylation of Upstream Binding Factor, an Rdna Transcription Factor Circ. Res. 1996, 78, 354-361
65. Hill, C.; Wurfel, A.; Heger, J.; Meyering, B.; Schluter, K. D.; Weber, M.; Ferdinandy, P.; Aronheim, A.; Schulz, R.; Euler, G. Inhibition of Ap-1 Signaling by Jdp2 Overexpression Protects Cardiomyocytes against Hypertrophy and Apoptosis Induction Cardiovasc. Res. 2013, 99, 121-128
66. Sharov, V. G.; Sabbah, H. N.; Shimoyama, H.; Ali, A. S.; Levine, T. B.; Lesch, M.; Goldstein, S. Abnormalities of Contractile Structures in Viable Myocytes of the Failing Heart Int. J. Cardiol. 1994, 43, 287-297
67. Hamrell, B. B.; Alpert, N. R. The Mechanical Characteristics of Hypertrophied Rabbit Cardiac Muscle in the Absence of Congestive Heart Failure: The Contractile and Series Elastic Elements Circ. Res. 1977, 40, 20-25
68. Wang, Q.; Moncman, C. L.; Winkelmann, D. A. Mutations in the Motor Domain Modulate Myosin Activity and Myofibril Organization J. Cell Sci. 2003, 116, 4227-4238
69. Kuo, P. L.; Lee, H.; Bray, M. A.; Geisse, N. A.; Huang, Y. T.; Adams, W. J.; Sheehy, S. P.; Parker, K. K. Myocyte Shape Regulates Lateral Registry of Sarcomeres and Contractility Am. J. Pathol. 2012, 181, 2030-2037
70. Trappmann, B.; Gautrot, J. E.; Connelly, J. T.; Strange, D. G.; Li, Y.; Oyen, M. L.; Cohen Stuart, M. A.; Boehm, H.; Li, B.; Vogel, V.; Spatz, J. P.; Watt, F. M.; Huck, W. T. Extracellular-Matrix Tethering Regulates Stem-Cell Fate Nat. Mater. 2012, 11, 642-649