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Collagen Structure Deterioration in the Skin of Patients with Pelvic Organ Prolapse Determined by Atomic Force Microscopy

Published online by Cambridge University Press:  05 March 2015

Svetlana L. Kotova ,
Peter S. Timashev ,
Anna E. Guller ,
Anatoly B. Shekhter ,
Pavel I. Misurkin ,
Victor N. Bagratashvili  and
Anna B. Solovieva
Svetlana L. Kotova*
Affiliation:
N.N. Semenov Institute of Chemical Physics, Department of Polymers and Composites, 4 Kosygin St., 119991, Moscow, Russia
Peter S. Timashev
Affiliation:
Institute of Laser and Information Technologies, 2 Pionerskaya St., 142092, Troitsk, Moscow, Russia
Anna E. Guller
Affiliation:
Research Institute of Molecular Medicine, I.M. Sechenov First Moscow Medical University, 8 Trubetskaya St., Bldg. 2, 119991, Moscow, Russia
Anatoly B. Shekhter
Affiliation:
Research Institute of Molecular Medicine, I.M. Sechenov First Moscow Medical University, 8 Trubetskaya St., Bldg. 2, 119991, Moscow, Russia
Pavel I. Misurkin
Affiliation:
N.N. Semenov Institute of Chemical Physics, Department of Polymers and Composites, 4 Kosygin St., 119991, Moscow, Russia
Victor N. Bagratashvili
Affiliation:
Institute of Laser and Information Technologies, 2 Pionerskaya St., 142092, Troitsk, Moscow, Russia
Anna B. Solovieva
Affiliation:
N.N. Semenov Institute of Chemical Physics, Department of Polymers and Composites, 4 Kosygin St., 119991, Moscow, Russia
*
*Corresponding author.[email protected]
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Abstract

We used atomic force microscopy (AFM) to diagnose pathological changes in the extracellular matrix (ECM) of skin connective tissue in patients with pelvic organ prolapse (POP). POP is a common condition affecting women that considerably decreases the patients’ quality of life. Deviations from normal morphology of the skin ECM from patients with POP occur including packing and arrangement of individual collagen fibers and arrangement of collagen fibrils. The nanoindentation study revealed significant deterioration of the mechanical properties of collagen fibril bundles in the skin of POP patients as compared with the skin of healthy subjects. Changes in the skin ECM appeared to correlate well with changes in the ECM of the pelvic ligament tissue associated with POP. AFM data on the ECM structure of normal and pathologically altered connective tissue were in agreement with results of the standard histological study on the same clinical specimens. Thus, AFM and related techniques may serve as independent or complementary diagnostic tools for tracking POP-related pathological changes of connective tissue.

Keywords

atomic force microscopycollagenextracellular matrixconnective tissuenanoindentationflicker-noise spectroscopypelvic organ prolapse
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 21 , Issue 2 , April 2015 , pp. 324 - 333
Copyright
© Microscopy Society of America 2015 

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Footnotes

†

Current address: MQ Biofocus Research Centre, Macquarie University, NSW 2109, Sydney, Australia.

References

Casuso, I., Rico, F. & Scheuring, S. (2011). Biological AFM: where we come from—where we are—where we may go. J Mol Recogn 24, 406–413.Google Scholar
Choy, J., Mathieu-Costello, O. & Kassab, G. (2005). The effect of fixation and histological preparation on coronary artery dimensions. Ann Biomed Eng 33(8), 1027–1033.Google Scholar
Cross, S.E., Jin, Y.-S., Tondre, J., Wong, R., Rao, J. & Gimzewski, J.K. (2008). AFM-based analysis of human metastatic cancer cells. Nanotechnology 19, 384003.Google Scholar
Dorph-Petersen, K.A., Nyengaard, J.R. & Gundersen, H.J. (2001). Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204, 232–246.CrossRefGoogle ScholarPubMed
Flint, M.H. & Merrilees, M.J. (1977). Relationship between the axial periodicity and staining of collagen by the masson trichrome procedure. Histochem J 9, 1–13.Google Scholar
Graham, H.K., Hodson, N.W., Hoyland, J.A., Millward-Sadler, S.J., Garrod, D., Scothern, A., Griffiths, C.E.M., Watson, R.E.B., Cox, T.R., Erler, J.T., Trafford, A.W. & Sherratt, M.J. (2010). Tissue section AFM: In situ ultrastructural imaging of native biomolecules. Matrix Biol 29, 254–260.Google Scholar
Huml, M., Silye, R., Zauner, G., Hutterer, S. & Schilcher, K. (2013). Brain tumor classification using AFM in combination with data mining techniques. BioMed Res Int, Article ID 176519, 11pp.Google ScholarPubMed
Kerkhof, M.H., Hendriks, L. & Brölmann, H.A.M. (2009). Changes in connective tissue in patients with pelvic organ prolapse—A review of the current literature. Int Urogynecol J 20, 461–474.Google Scholar
Kotova, S.L., Shekhter, A.B., Timashev, P.S., Guller, A.E., Mudrov, A.A., Timofeeva, V.A., Panchenko, V.Ya., Bagratashvili, V.N. & Solovieva, A.B. (2014). AFM study of the extracellular connective tissue matrix in patients with pelvic organ prolapse. J Surf Investig. X-ray, Synchrotron and Neutron Techniques 8, 754–760.Google Scholar
Lammers, K., Lince, S.L., Spath, M.A., van Kempen, L.C.L.T., Hendriks, J.C.M., Vierhout, M.E. & Kluivers, K.B. (2012). Pelvic organ prolapse and collagen-associated disorders. Int Urogynecol J 23, 313–319.Google Scholar
Lee, G.Y.H. & Lim, C.T. (2007). Biomechanics approaches to studying human diseases. TRENDS Biotechnol 25, 111–118.CrossRefGoogle ScholarPubMed
Lee, S.J., Choi, S., Kim, M.S., Cheong, Y., Kwak, H.-W., Park, H.-K. & Jin, K.-H. (2013). Short-term effect of cryotherapy on human scleral tissue by atomic force microscopy. Scanning 35, 302–307.CrossRefGoogle ScholarPubMed
Li, Y. & Douglas, E.P. (2013). Effects of various salts on structural polymorphism of reconstituted type I collagen fibrils. Colloid Surface B 112, 42–50.CrossRefGoogle ScholarPubMed
Mirsaidov, U., Timashev, S.F., Polyakov, Y.S., Misurkin, P.I., Musaev, I. & Polyakov, S.V. (2011). Analytical method for parameterizing the random profile components of nanosurfaces imaged by atomic force microscopy. Analyst 136, 570–576.Google Scholar
Orgel, J.P.R.O., Irving, T.C., Miller, A. & Wess, T.J. (2006). Microfibrillar structure of type I collagen in situ . Proc Natl Acad Sci USA 103, 9001–9005.Google Scholar
Persu, C., Chapple, C.R., Cauni, V., Gutue, S. & Geavlete, P. (2011). Pelvic organ prolapse quantification system (POP-Q)—A new era in pelvic prolapse staging. J Med Life 4, 75–81.Google ScholarPubMed
Phillips, C.H., Anthony, F., Benyon, C. & Monga, A.K. (2006). Urogynaecology: Collagen metabolism in the uterosacral ligaments and vaginal skin of women with uterine prolapse. BJOG—Int J Obstet Gynecol 113, 39–46.CrossRefGoogle ScholarPubMed
Rigozzi, S., Muller, R., Stemmer, A. & Snedeker, J.G. (2013). Tendon glycosaminoglycan proteoglycan side chains promote collagen fibril sliding—AFM observations at the nanoscale. J Biomech 46, 813–818.Google Scholar
Sivasankar, M. & Ivanisevic, A. (2007). Atomic force microscopy investigation of vocal fold collagen. Laryngoscope 117, 1876–1881.CrossRefGoogle ScholarPubMed
Sridharan, I., Ma, Y., Kim, T., Kobak, W., Rotmensch, J. & Wang, R. (2012). Structural and mechanical profiles of native collagen fibers in vaginal wall connective tissues. Biomaterials 33, 1520–1527.CrossRefGoogle ScholarPubMed
Stolz, M., Gottardi, R., Raiteri, R., Miot, S., Martin, I., Imer, R., Staufer, U., Raducanu, A., Duggelin, M., Baschong, W., Daniels, A.U., Friederich, N.F., Aszodi, A. & Aebi, U. (2009). Early detection of aging cartilage and osteoarthritis in mice and patient samples using atomic force microscopy. Nat Nanotechnol 4, 186–192.CrossRefGoogle ScholarPubMed
Strasser, S., Zink, A., Janko, M., Heckl, W.M. & Thalhammer, S. (2007). Structural investigations on native collagen type I fibrils using AFM. Biochem Biophys Res Commun 354, 27–32.Google Scholar
Stylianou, A. & Yova, D. (2013). Surface nanoscale imaging of collagen thin films by atomic force microscopy. Mater Sci Eng C 33, 2947–2957.CrossRefGoogle ScholarPubMed
Thomasy, S.M., Raghunathan, V.K., Winkler, M., Reilly, C.M., Sadeli, A.R., Russell, P., Jester, J.V. & Murphy, C.J. (2014). Elastic modulus and collagen organization of the rabbit cornea: Epithelium to endothelium. Acta Biomater 10, 785–791.CrossRefGoogle ScholarPubMed
Wallace, J.M. (2012). Applications of atomic force microscopy for the assessment of nanoscale morphological and mechanical properties of bone. Bone 50, 420–427.CrossRefGoogle ScholarPubMed
Wang, L., Guo, Y., Li, P. & Song, Y. (2014). Anion-specific effects on the assembly of collagen layers mediated by magnesium ion on mica surface. J Phys Chem B 118, 511–518.Google Scholar
Wen, C.-Y., Wu, C.-B., Tang, B., Wang, T., Yan, C.-H., Lu, W.W., Pan, H., Hu, Y. & Chiu, K.-Y. (2012). Collagen fibril stiffening in osteoarthritic cartilage of human beings revealed by atomic force microscopy. Osteoarthr Cartilage 20, 916–922.Google Scholar
Xing, X., Jin, H., Lu, Y., Wang, Q., Pan, Y., Cai, J. & Wang, H. (2011). Detection of erythrocytes in patient with elliptocytosis complicating ITP using atomic force microscopy. Micron 42, 42–46.CrossRefGoogle ScholarPubMed
Yang, L., van der Werf, K.O., Fitie, C.F.C., Bennink, M.L., Dijkstra, P.J. & Feijen, J. (2008). Mechanical properties of native and cross-linked type i collagen fibrils. Biophys J 94, 2204–2211.Google Scholar