Atomic Force Microscopy for Collagen-Based Nanobiomaterials

Novel nanobiomaterials are increasingly gaining ground in bioengineering research. Among the numerous biomaterials, collagen-nanobiomaterials, such as collagen thin films, are of great interest since they present a wide range of applications in the fields of biomaterials, tissue engineering, and biomedicine. Collagen type I is the most abundant protein within extracellular matrix and, due to its unique characteristics, is widely used as biomaterial. A thorough characterization of the structure and properties of nanomaterials can be achieved by Atomic Force Microscopy (AFM). AFM is a very powerful tool which can be used to obtain qualitative or quantitative information without destroying the collagen fibrillar structure. This mini review covers issues related to the use of AFM for studying the structure and mechanical properties of collagen-based nanobiomaterials, collagen-substrate interactions during the formation of collagen thin films, collagen-cells interactions, and the collagen-optical radiation interactions.

[1]  Jacques Prost,et al.  Compressive stress inhibits proliferation in tumor spheroids through a volume limitation. , 2014, Biophysical journal.

[2]  Peter Fratzl,et al.  Collagen : structure and mechanics , 2008 .

[3]  A. Sionkowska,et al.  Surface properties of UV-irradiated poly(vinyl alcohol) films containing small amount of collagen , 2009 .

[4]  Mitchel J Doktycz,et al.  Atomic force microscopy of biological samples. , 2010, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[5]  D. Jackson Collagens , 1978 .

[6]  A. Sionkowska,et al.  Collagen fibrils in UV irradiated poly(vinyl pyrrolidone) films , 2008 .

[7]  M. Pritzker,et al.  Modification of Hydrophilic and Hydrophobic Surfaces Using an Ionic-Complementary Peptide , 2007, PloS one.

[8]  Kostas Politopoulos,et al.  Mechanical properties of collagen fibrils on thin films by Atomic Force Microscopy nanoindentation , 2012, 2012 IEEE 12th International Conference on Bioinformatics & Bioengineering (BIBE).

[9]  A M Rubenchik,et al.  Collagen structure and nonlinear susceptibility: Effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity , 2000, Lasers in surgery and medicine.

[10]  Daniel J Müller,et al.  Atomic force microscopy as a multifunctional molecular toolbox in nanobiotechnology. , 2008, Nature nanotechnology.

[11]  A. Sionkowska,et al.  Mechanical properties of UV irradiated rat tail tendon (RTT) collagen. , 2004, International journal of biological macromolecules.

[12]  Dido Yova,et al.  Surface nanoscale imaging of collagen thin films by Atomic Force Microscopy. , 2013, Materials science & engineering. C, Materials for biological applications.

[13]  Claudio Nicolini,et al.  Biomaterials for orthopedics: a roughness analysis by atomic force microscopy. , 2007, Journal of biomedical materials research. Part A.

[14]  E. Marsano,et al.  Thermal and mechanical properties of UV irradiated collagen/chitosan thin films , 2006 .

[15]  Watt W Webb,et al.  Interpreting second-harmonic generation images of collagen I fibrils. , 2005, Biophysical journal.

[16]  S. Teoh,et al.  Surface modification of ultra thin poly (ε-caprolactone) films using acrylic acid and collagen , 2004 .

[17]  T. V. van Kuppevelt,et al.  Evaluation of methods for the construction of collagenous scaffolds with a radial pore structure for tissue engineering , 2011, Journal of tissue engineering and regenerative medicine.

[18]  D. Mantovani,et al.  Low doses of ultraviolet radiation stimulate cell activity in collagen‐based scaffolds , 2008, Biotechnology progress.

[19]  P. Gröning,et al.  Cleavage mechanism and surface chemical characterization of phengitic Muscovite and Muscovite as constrained by X-Ray Photoelectron Spectroscopy , 1998 .

[20]  Ricardo Garcia,et al.  Biomechanical Remodeling of the Microenvironment by Stromal Caveolin-1 Favors Tumor Invasion and Metastasis , 2011, Cell.

[21]  A. Stylianou,et al.  Atomic force microscopy investigation of the interaction of low-level laser irradiation of collagen thin films in correlation with fibroblast response , 2015, Lasers in Medical Science.

[22]  Kostas Politopoulos,et al.  Atomic Force Microscopy surface nanocharacterization of UV-irradiated collagen thin films , 2012, 2012 IEEE 12th International Conference on Bioinformatics & Bioengineering (BIBE).

[23]  Eleni Alexandratou,et al.  Investigation of the influence of UV irradiation on collagen thin films by AFM imaging. , 2014, Materials science & engineering. C, Materials for biological applications.

[24]  Santiago D. Solares,et al.  Mapping of conservative and dissipative interactions in bimodal atomic force microscopy using open-loop and phase-locked-loop control of the higher eigenmode , 2011 .

[25]  M. Goh,et al.  A statistically derived parameterization for the collagen triple‐helix , 2002, Protein science : a publication of the Protein Society.

[26]  G. Pharr,et al.  Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology , 2004 .

[27]  M. Niemz Laser-Tissue Interactions , 1996 .

[28]  Gerber,et al.  Atomic Force Microscope , 2020, Definitions.

[29]  Y. Uesu,et al.  Optical Second Harmonic Generation Microscopy as a Tool of Material Diagnosis , 2012 .

[30]  E. Darling,et al.  Force scanning: a rapid, high-resolution approach for spatial mechanical property mapping , 2011, Nanotechnology.

[31]  Virginijus Barzda,et al.  Nonlinear optical properties of type I collagen fibers studied by polarization dependent second harmonic generation microscopy. , 2011, The journal of physical chemistry. B.

[32]  K. Eliceiri,et al.  Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. , 2009, Molecular biology of the cell.

[33]  N. Thomson,et al.  Dynamic mechanical analysis of collagen fibrils at the nanoscale. , 2012, Journal of the mechanical behavior of biomedical materials.

[34]  P. Sowa,et al.  Optical radiation in modern medicine , 2013, Postepy dermatologii i alergologii.

[35]  Chen Wang,et al.  Patterning of 293T fibroblasts on a mica surface , 2009, Analytical and bioanalytical chemistry.

[36]  Guillaume Lamour,et al.  High intrinsic mechanical flexibility of mouse prion nanofibrils revealed by measurements of axial and radial Young's moduli. , 2014, ACS nano.

[37]  H. Hertz Ueber die Berührung fester elastischer Körper. , 1882 .

[38]  Joseph W Freeman,et al.  3D in vitro bioengineered tumors based on collagen I hydrogels. , 2011, Biomaterials.

[39]  J. Alcaraz,et al.  Erratum to: Fibroblast viability and phenotypic changes within glycated stiffened three-dimensional collagen matrices , 2015, Respiratory Research.

[40]  Lay Poh Tan,et al.  Micro-/nano-engineered cellular responses for soft tissue engineering and biomedical applications. , 2011, Small.

[41]  B Ohler Perspectives on Over Twenty Years of Life Science Research with Atomic Force Microscopy and a Look Toward the Future , 2010 .

[42]  H. Suh,et al.  Evaluation of calcification in porcine valves treated by ultraviolet ray and glutaraldehyde , 2000 .

[43]  H. Ryssel,et al.  An overview of current biomaterials in aesthetic soft tissue augmentation , 2012, European Journal of Plastic Surgery.

[44]  Cell behaviors on micro-patterned porous thin films , 2010 .

[45]  Seeram Ramakrishna,et al.  An aligned nanofibrous collagen scaffold by electrospinning and its effects on in vitro fibroblast culture. , 2006, Journal of biomedical materials research. Part A.

[46]  Aufried T. M. Lenferink,et al.  Combined AFM and confocal fluorescence microscope for applications in bio‐nanotechnology , 2005, Journal of microscopy.

[47]  S. Ricard-Blum,et al.  The Collagen Superfamily , 2005 .

[48]  A. Sionkowska,et al.  UV-vis and FT-IR spectra of ultraviolet irradiated collagen in the presence of antioxidant ascorbic acid. , 2010, Ecotoxicology and environmental safety.

[49]  Leslie M Loew,et al.  Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms , 2003, Nature Biotechnology.

[50]  J. Massagué,et al.  Field Cancerization: Something New Under the Sun , 2012, Cell.

[51]  John T Elliott,et al.  Cell response to matrix mechanics: focus on collagen. , 2009, Biochimica et biophysica acta.

[52]  Ricardo Garcia,et al.  Nanomechanical mapping of soft matter by bimodal force microscopy , 2013 .

[53]  Ying Mei,et al.  The effect of surface chemistry on the formation of thin films of native fibrillar collagen. , 2007, Biomaterials.

[54]  Cynthia A. Reinhart-King,et al.  Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior. , 2013, Acta biomaterialia.

[55]  A. P. Gunning,et al.  Atomic Force Microscopy for Biologists , 1999 .

[56]  P. Friedl,et al.  Strain Stiffening of Fibrillar Collagen during Individual and Collective Cell Migration Identified by AFM Nanoindentation. , 2016, ACS applied materials & interfaces.

[57]  Dido Yova,et al.  Assessing Collagen Nanoscale Thin Films Heterogeneity by AFM Multimode Imaging and Nanoindetation for NanoBioMedical Applications , 2014 .

[58]  F. Rossi,et al.  Fabrication of Bio-Functionalised Polypyrrole Nanoarrays for Bio-Molecular Recognition , 2011 .

[59]  H. Shibata,et al.  Effect of ultraviolet radiation on photodegradation of collagen , 1999 .

[60]  I. Rău,et al.  Collagen-based biomaterials for ibuprofen delivery , 2016 .

[61]  M. Dunn,et al.  Synergistic effects of glucose and ultraviolet irradiation on the physical properties of collagen. , 2002, Journal of biomedical materials research.

[62]  P. Rouxhet,et al.  AFM Study of the Interaction of Collagen with Polystyrene and Plasma-Oxidized Polystyrene , 2001 .

[63]  M. Dunn,et al.  Changes in mechanical properties and cellularity during long-term culture of collagen fiber ACL reconstruction scaffolds. , 2005, Journal of biomedical materials research. Part A.

[64]  Xiaoqin Zhu,et al.  Quantitative biomarkers of human skin photoaging based on intrinsic second harmonic generation signal. , 2013, Scanning.

[65]  Dido Yova,et al.  Atomic force imaging microscopy investigation of the interaction of ultraviolet radiation with collagen thin films , 2013, Photonics West - Biomedical Optics.

[66]  N. Gadegaard,et al.  Atomic force microscopy in biology: technology and techniques , 2006, Biotechnic & histochemistry : official publication of the Biological Stain Commission.

[67]  T. Ramasami,et al.  Effect of UV irradiation on stabilized collagen: role of chromium(III). , 2008, Colloids and surfaces. B, Biointerfaces.

[68]  J. Petruska,et al.  A SUBUNIT MODEL FOR THE TROPOCOLLAGEN MACROMOLECULE. , 1964, Proceedings of the National Academy of Sciences of the United States of America.

[69]  D A Weitz,et al.  Glioma expansion in collagen I matrices: analyzing collagen concentration-dependent growth and motility patterns. , 2005, Biophysical journal.

[70]  Ueli Aebi,et al.  Dynamic elastic modulus of porcine articular cartilage determined at two different levels of tissue organization by indentation-type atomic force microscopy. , 2004, Biophysical journal.

[71]  John T. Woodward,et al.  Thin Films of Collagen Affect Smooth Muscle Cell Morphology , 2003 .

[72]  F. Variola Atomic force microscopy in biomaterials surface science. , 2015, Physical chemistry chemical physics : PCCP.

[73]  Tilman E. Schäffer,et al.  High-speed force mapping on living cells with a small cantilever atomic force microscope. , 2014, The Review of scientific instruments.

[74]  Stergios Logothetidis,et al.  Atomic force microscopy probing in the measurement of cell mechanics , 2010, International journal of nanomedicine.

[75]  Xiaohong Fang,et al.  Living cell study at the single-molecule and single-cell levels by atomic force microscopy. , 2012, Nanomedicine.

[76]  A. Stylianou,et al.  Atomic force microscopy quantitative and qualitative nanoscale characterization of collagen thin films , 2012 .

[77]  J. Howard,et al.  Assembly of collagen into microribbons: effects of pH and electrolytes. , 2004, Journal of structural biology.

[78]  Chen-Yuan Dong,et al.  Second harmonic generation microscopy: principles and applications to disease diagnosis , 2011 .

[79]  Allison Hubel,et al.  Microstructural Characteristics of Extracellular Matrix Produced by Stromal Fibroblasts , 2006, Annals of Biomedical Engineering.

[80]  Jonathon Howard,et al.  Creating nanoscopic collagen matrices using atomic force microscopy , 2004, Microscopy research and technique.

[81]  I Jurisica,et al.  Integrin α11β1 regulates cancer stromal stiffness and promotes tumorigenicity and metastasis in non-small cell lung cancer , 2015, Oncogene.

[82]  Jens Friedrichs,et al.  Molecular-scale topographic cues induce the orientation and directional movement of fibroblasts on two-dimensional collagen surfaces. , 2005, Journal of molecular biology.

[83]  N. Spencer,et al.  Orthogonal nanometer-micrometer roughness gradients probe morphological influences on cell behavior. , 2012, Biomaterials.

[84]  Peter Fratzl,et al.  Collagen: Structure and Mechanics, an Introduction , 2008 .

[85]  Joseph M. Wallace,et al.  Nanoscale morphology of Type I collagen is altered in the Brtl mouse model of Osteogenesis Imperfecta. , 2011, Journal of structural biology.

[86]  V. P. Ivanova,et al.  A current viewpoint on structure and evolution of collagens. I. Fibrillar collagens , 2012, Journal of Evolutionary Biochemistry and Physiology.

[87]  Maxence Bigerelle,et al.  Relative influence of surface topography and surface chemistry on cell response to bone implant materials. Part 2: Biological aspects , 2010, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[88]  S. Ricard-Blum The collagen family. , 2011, Cold Spring Harbor perspectives in biology.

[89]  Ming Sun,et al.  Surface-templated formation of protein microfibril arrays. , 2008, Langmuir : the ACS journal of surfaces and colloids.

[90]  Kirk C Hansen,et al.  Collagen architecture in pregnancy-induced protection from breast cancer , 2013, Journal of Cell Science.

[91]  M. Ferrarini,et al.  Innovative Models to Assess Multiple Myeloma Biology and the Impact of Drugs , 2013 .

[92]  L. Moldovan,et al.  Collagen–based scaffolds for skin tissue engineering , 2011, Journal of medicine and life.

[93]  A. Stylianou,et al.  Surface Characterization of Collagen Films by Atomic Force Microscopy , 2010 .

[94]  Joseph W Freeman,et al.  Collagen self-assembly and the development of tendon mechanical properties. , 2003, Journal of biomechanics.

[95]  Jeng-Wei Tjiu,et al.  Prediction of heat-induced collagen shrinkage by use of second harmonic generation microscopy. , 2006, Journal of biomedical optics.

[96]  J. Jansen,et al.  Cell and tissue behavior on micro-grooved surfaces , 2001, Odontology.

[97]  K. Kivirikko,et al.  Collagens and collagen-related diseases , 2001, Annals of medicine.

[98]  B. Nair,et al.  Effect of UV irradiation on the physicochemical properties of collagen stabilized using aldehydes , 2007 .

[99]  Diego Mantovani,et al.  On the effects of UV-C and pH on the mechanical behavior, molecular conformation and cell viability of collagen-based scaffold for vascular tissue engineering. , 2010, Macromolecular bioscience.

[100]  Daniel J Müller,et al.  Atomic force microscopy: a nanoscopic window on the cell surface. , 2011, Trends in cell biology.

[101]  Kostas Politopoulos,et al.  Combined information from AFM imaging and SHG signal analysis of collagen thin films , 2011, Biomed. Signal Process. Control..

[102]  M. Ho,et al.  Probing characteristics of collagen molecules on various surfaces via atomic force microscopy , 2012 .

[103]  Sanjay Kumar,et al.  Measuring the elastic properties of living cells with atomic force microscopy indentation. , 2013, Methods in molecular biology.

[104]  I. Sokolov CHAPTER 1 Atomic Force Microscopy in Cancer Cell Research , 2006 .

[105]  Guanqing Ou,et al.  A 3D tension bioreactor platform to study the interplay between ECM stiffness and tumor phenotype. , 2015, Journal of biotechnology.

[106]  Wei Liu,et al.  Collagen Tissue Engineering: Development of Novel Biomaterials and Applications , 2008, Pediatric Research.

[107]  Manish J. Butte,et al.  Strain-enhanced stress relaxation impacts nonlinear elasticity in collagen gels , 2016, Proceedings of the National Academy of Sciences.

[108]  M. Horton,et al.  Collagen fibrils: nanoscale ropes. , 2007, Biophysical journal.

[109]  B. Weigelt,et al.  The need for complex 3D culture models to unravel novel pathways and identify accurate biomarkers in breast cancer. , 2014, Advanced drug delivery reviews.

[110]  Andreas Stylianou,et al.  Atomic Force Microscopy Probing of Cancer Cells and Tumor Microenvironment Components , 2016 .

[111]  Daniel J. Muller,et al.  Creating ultrathin nanoscopic collagen matrices for biological and biotechnological applications. , 2007, Small.

[112]  J. Jansen,et al.  The threshold at which substrate nanogroove dimensions may influence fibroblast alignment and adhesion. , 2007, Biomaterials.

[113]  Dido Yova,et al.  The effects of UV irradiation on collagen D-band revealed by atomic force microscopy. , 2015, Scanning.

[114]  Kam W Leong,et al.  Nanopattern-induced changes in morphology and motility of smooth muscle cells. , 2005, Biomaterials.

[115]  Brian Seed,et al.  Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation , 2003, Nature Medicine.

[116]  A. Stylianou,et al.  Atomic Force Microscopy Imaging of the Nanoscale Assembly of Type I Collagen on Controlled Polystyrene Particles Surfaces , 2011 .

[117]  V. Weaver,et al.  Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-β-deficient mouse mammary carcinomas. , 2013, Cancer research.

[118]  D. Hulmes Collagen Diversity, Synthesis and Assembly , 2008 .

[119]  Ronald T Raines,et al.  Collagen structure and stability. , 2009, Annual review of biochemistry.

[120]  A. Kühnle,et al.  How flat is an air-cleaved mica surface? , 2008, Nanotechnology.

[121]  Mikala Egeblad,et al.  Matrix Crosslinking Forces Tumor Progression by Enhancing Integrin Signaling , 2009, Cell.

[122]  V. Gkretsi,et al.  Remodeling Components of the Tumor Microenvironment to Enhance Cancer Therapy , 2015, Front. Oncol..

[123]  C. Franz,et al.  Quantitative analysis of type I collagen fibril regulation by lumican and decorin using AFM. , 2013, Journal of structural biology.

[124]  A. Sionkowska,et al.  Surface characterization of collagen/elastin based biomaterials for tissue regeneration , 2009 .

[125]  Dido Yova,et al.  AFM Multimode Imaging and Nanoindetation Method for Assessing Collagen Nanoscale Thin Films Heterogeneity , 2014 .

[126]  A. Stylianou,et al.  Combined SHG signal information with AFM imaging to assess conformational changes in collagen , 2009, 2009 9th International Conference on Information Technology and Applications in Biomedicine.

[127]  Ueli Aebi,et al.  Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. , 2009, Nature nanotechnology.

[128]  P. Zorlutuna,et al.  Nanobiomaterials: a review of the existing science and technology, and new approaches , 2006, Journal of biomaterials science. Polymer edition.

[129]  Hertz On the Contact of Elastic Solids , 1882 .

[130]  R. Cameron,et al.  Regeneration and repair of tendon and ligament tissue using collagen fibre biomaterials. , 2011, Acta biomaterialia.

[131]  J P Stegemann,et al.  Strategies for directing the structure and function of three-dimensional collagen biomaterials across length scales. , 2014, Acta biomaterialia.

[132]  C. Gerber,et al.  Exogenous collagen cross‐linking recovers tendon functional integrity in an experimental model of partial tear , 2012, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[133]  B. Brodsky,et al.  UV damage of collagen: insights from model collagen peptides. , 2012, Biopolymers.

[134]  E. Georgiou,et al.  Thermally Induced Irreversible Conformational Changes in Collagen Probed by Optical Second Harmonic Generation and Laser-induced Fluorescence , 2002, Lasers in Medical Science.

[135]  Ricardo Garcia,et al.  Dynamic atomic force microscopy methods , 2002 .

[136]  Mi Li,et al.  Nanoscale monitoring of drug actions on cell membrane using atomic force microscopy , 2015, Acta Pharmacologica Sinica.

[137]  T. Desai,et al.  Influence of chitosan on cell viability and proliferation in three dimensional collagen gels , 2000, Proceedings of the 22nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Cat. No.00CH37143).

[138]  Eleni Alexandratou,et al.  Nanotopography of collagen thin films in correlation with fibroblast response , 2013 .