Skin collagen fiber molecular order: a pattern of distributional fiber orientation as assessed by optical anisotropy and image analysis
Birefringence can reveal much of the morphology, molecular order, heterogeneity of fiber orientation, and nonlinear optical properties of biopolymers such as collagen. However, the detailed characterization of skin collagen fibers using optical anisotropy methods remains elusive. A clear understandi...
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| description | Birefringence can reveal much of the morphology, molecular order, heterogeneity of fiber orientation, and nonlinear optical properties of biopolymers such as collagen. However, the detailed characterization of skin collagen fibers using optical anisotropy methods remains elusive. A clear understanding of collagen fiber organization in skin tissues may be important in the interpretation of their structural-functional relationships under normal and pathological conditions. In this study, fiber orientation in collagen bundles (CBs) and their supramolecular organization were examined in rat skin using polarization microscopy and image analysis.
Image variations with rotation of the microscope stage and selection of the in-depth focus plane were investigated in unstained sections of varying thicknesses from rat skin fragments. Total birefringence (image analysis) and form and intrinsic birefringence (Sénarmont's method) were estimated. Based on the birefringent images, CBs were found to contain intercrossing points with a twisted helical distribution of collagen fibers (chiral elements) and frequently presented circular structures. Collagen fibers were observed to extend from the surface level to deeper planes, creating a 3D-network of oriented intertwined CBs. At least three levels of birefringent brilliance intensity were revealed by image analysis, indicating a heterogeneous spatial organization of the CBs. Slight differences in optical retardations were found for CBs immersed in some of the fluids used in a comparison of 170- and 240-day old rats.
Polarization microscopy studies provide detailed high-quality structural information on rat skin CBs. A 3D-network structure based on image analysis and birefringence compensation for collagen fibers is suggested for CBs. Form and intrinsic birefringence evaluation can reveal differences in the rat skin associated with age at the levels of collagen fiber crystallinity and macromolecular organization. These findings may inspire future studies of the feedback mechanisms by which spatial, bioelectrical and biomechanical information is transmitted from CBs to skin cells. |
| doi_str_mv | 10.1371/journal.pone.0054724 |
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Image variations with rotation of the microscope stage and selection of the in-depth focus plane were investigated in unstained sections of varying thicknesses from rat skin fragments. Total birefringence (image analysis) and form and intrinsic birefringence (Sénarmont's method) were estimated. Based on the birefringent images, CBs were found to contain intercrossing points with a twisted helical distribution of collagen fibers (chiral elements) and frequently presented circular structures. Collagen fibers were observed to extend from the surface level to deeper planes, creating a 3D-network of oriented intertwined CBs. At least three levels of birefringent brilliance intensity were revealed by image analysis, indicating a heterogeneous spatial organization of the CBs. Slight differences in optical retardations were found for CBs immersed in some of the fluids used in a comparison of 170- and 240-day old rats.
Polarization microscopy studies provide detailed high-quality structural information on rat skin CBs. A 3D-network structure based on image analysis and birefringence compensation for collagen fibers is suggested for CBs. Form and intrinsic birefringence evaluation can reveal differences in the rat skin associated with age at the levels of collagen fiber crystallinity and macromolecular organization. These findings may inspire future studies of the feedback mechanisms by which spatial, bioelectrical and biomechanical information is transmitted from CBs to skin cells.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0054724</identifier><identifier>PMID: 23349957</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animal tissues ; Animals ; Anisotropy ; Bioelectricity ; Biology ; Biomechanics ; Biopolymers ; Birefringence ; Collagen ; Collagen - chemistry ; Cornea ; Diabetes ; Extracellular Matrix - chemistry ; Extracellular Matrix - ultrastructure ; Fiber orientation ; Fibers ; Fourier transforms ; Image analysis ; Image processing ; Image processing equipment ; Image Processing, Computer-Assisted ; Macromolecules ; Male ; Medicine ; Microscopy ; Microscopy, Polarization ; Optical fibers ; Optical properties ; Planes ; Polarization ; Rats ; Skin ; Skin & tissue grafts ; Skin - chemistry ; Skin - ultrastructure ; Structure-function relationships ; Studies ; Tendons ; Ultrasonic imaging</subject><ispartof>PloS one, 2013-01, Vol.8 (1), p.e54724-e54724</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Ribeiro et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Ribeiro et al 2013 Ribeiro et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7b1e6b1007b6c6e86784577e75aacdc934791da6cf66adada5acaace3474381d3</citedby><cites>FETCH-LOGICAL-c692t-7b1e6b1007b6c6e86784577e75aacdc934791da6cf66adada5acaace3474381d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3548803/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3548803/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23349957$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Brandner, Johanna M.</contributor><creatorcontrib>Ribeiro, Juliana Fulan</creatorcontrib><creatorcontrib>dos Anjos, Eli Heber Martins</creatorcontrib><creatorcontrib>Mello, Maria Luiza S</creatorcontrib><creatorcontrib>de Campos Vidal, Benedicto</creatorcontrib><title>Skin collagen fiber molecular order: a pattern of distributional fiber orientation as assessed by optical anisotropy and image analysis</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Birefringence can reveal much of the morphology, molecular order, heterogeneity of fiber orientation, and nonlinear optical properties of biopolymers such as collagen. However, the detailed characterization of skin collagen fibers using optical anisotropy methods remains elusive. A clear understanding of collagen fiber organization in skin tissues may be important in the interpretation of their structural-functional relationships under normal and pathological conditions. In this study, fiber orientation in collagen bundles (CBs) and their supramolecular organization were examined in rat skin using polarization microscopy and image analysis.
Image variations with rotation of the microscope stage and selection of the in-depth focus plane were investigated in unstained sections of varying thicknesses from rat skin fragments. Total birefringence (image analysis) and form and intrinsic birefringence (Sénarmont's method) were estimated. Based on the birefringent images, CBs were found to contain intercrossing points with a twisted helical distribution of collagen fibers (chiral elements) and frequently presented circular structures. Collagen fibers were observed to extend from the surface level to deeper planes, creating a 3D-network of oriented intertwined CBs. At least three levels of birefringent brilliance intensity were revealed by image analysis, indicating a heterogeneous spatial organization of the CBs. Slight differences in optical retardations were found for CBs immersed in some of the fluids used in a comparison of 170- and 240-day old rats.
Polarization microscopy studies provide detailed high-quality structural information on rat skin CBs. A 3D-network structure based on image analysis and birefringence compensation for collagen fibers is suggested for CBs. Form and intrinsic birefringence evaluation can reveal differences in the rat skin associated with age at the levels of collagen fiber crystallinity and macromolecular organization. These findings may inspire future studies of the feedback mechanisms by which spatial, bioelectrical and biomechanical information is transmitted from CBs to skin cells.</description><subject>Animal tissues</subject><subject>Animals</subject><subject>Anisotropy</subject><subject>Bioelectricity</subject><subject>Biology</subject><subject>Biomechanics</subject><subject>Biopolymers</subject><subject>Birefringence</subject><subject>Collagen</subject><subject>Collagen - chemistry</subject><subject>Cornea</subject><subject>Diabetes</subject><subject>Extracellular Matrix - chemistry</subject><subject>Extracellular Matrix - ultrastructure</subject><subject>Fiber orientation</subject><subject>Fibers</subject><subject>Fourier transforms</subject><subject>Image analysis</subject><subject>Image processing</subject><subject>Image processing equipment</subject><subject>Image Processing, Computer-Assisted</subject><subject>Macromolecules</subject><subject>Male</subject><subject>Medicine</subject><subject>Microscopy</subject><subject>Microscopy, Polarization</subject><subject>Optical fibers</subject><subject>Optical properties</subject><subject>Planes</subject><subject>Polarization</subject><subject>Rats</subject><subject>Skin</subject><subject>Skin & tissue grafts</subject><subject>Skin - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ribeiro, Juliana Fulan</au><au>dos Anjos, Eli Heber Martins</au><au>Mello, Maria Luiza S</au><au>de Campos Vidal, Benedicto</au><au>Brandner, Johanna M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Skin collagen fiber molecular order: a pattern of distributional fiber orientation as assessed by optical anisotropy and image analysis</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-01-18</date><risdate>2013</risdate><volume>8</volume><issue>1</issue><spage>e54724</spage><epage>e54724</epage><pages>e54724-e54724</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Birefringence can reveal much of the morphology, molecular order, heterogeneity of fiber orientation, and nonlinear optical properties of biopolymers such as collagen. However, the detailed characterization of skin collagen fibers using optical anisotropy methods remains elusive. A clear understanding of collagen fiber organization in skin tissues may be important in the interpretation of their structural-functional relationships under normal and pathological conditions. In this study, fiber orientation in collagen bundles (CBs) and their supramolecular organization were examined in rat skin using polarization microscopy and image analysis.
Image variations with rotation of the microscope stage and selection of the in-depth focus plane were investigated in unstained sections of varying thicknesses from rat skin fragments. Total birefringence (image analysis) and form and intrinsic birefringence (Sénarmont's method) were estimated. Based on the birefringent images, CBs were found to contain intercrossing points with a twisted helical distribution of collagen fibers (chiral elements) and frequently presented circular structures. Collagen fibers were observed to extend from the surface level to deeper planes, creating a 3D-network of oriented intertwined CBs. At least three levels of birefringent brilliance intensity were revealed by image analysis, indicating a heterogeneous spatial organization of the CBs. Slight differences in optical retardations were found for CBs immersed in some of the fluids used in a comparison of 170- and 240-day old rats.
Polarization microscopy studies provide detailed high-quality structural information on rat skin CBs. A 3D-network structure based on image analysis and birefringence compensation for collagen fibers is suggested for CBs. Form and intrinsic birefringence evaluation can reveal differences in the rat skin associated with age at the levels of collagen fiber crystallinity and macromolecular organization. These findings may inspire future studies of the feedback mechanisms by which spatial, bioelectrical and biomechanical information is transmitted from CBs to skin cells.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23349957</pmid><doi>10.1371/journal.pone.0054724</doi><tpages>e54724</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animal tissues Animals Anisotropy Bioelectricity Biology Biomechanics Biopolymers Birefringence Collagen Collagen - chemistry Cornea Diabetes Extracellular Matrix - chemistry Extracellular Matrix - ultrastructure Fiber orientation Fibers Fourier transforms Image analysis Image processing Image processing equipment Image Processing, Computer-Assisted Macromolecules Male Medicine Microscopy Microscopy, Polarization Optical fibers Optical properties Planes Polarization Rats Skin Skin & tissue grafts Skin - chemistry Skin - ultrastructure Structure-function relationships Studies Tendons Ultrasonic imaging |
| title | Skin collagen fiber molecular order: a pattern of distributional fiber orientation as assessed by optical anisotropy and image analysis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-13T03%3A11%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Skin%20collagen%20fiber%20molecular%20order:%20a%20pattern%20of%20distributional%20fiber%20orientation%20as%20assessed%20by%20optical%20anisotropy%20and%20image%20analysis&rft.jtitle=PloS%20one&rft.au=Ribeiro,%20Juliana%20Fulan&rft.date=2013-01-18&rft.volume=8&rft.issue=1&rft.spage=e54724&rft.epage=e54724&rft.pages=e54724-e54724&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0054724&rft_dat=%3Cgale_plos_%3EA478229472%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1327279550&rft_id=info:pmid/23349957&rft_galeid=A478229472&rft_doaj_id=oai_doaj_org_article_fa215ef47e454946ac9a4277d5019410&rfr_iscdi=true |