Crystalline fibril structure of type II collagen in lamprey notochord sheath

Eikenberry, Eric F.; Childs, Barrett H.; Sheren, Scott B.; Parry, David; Craig, A. S.; Brodsky, Barbara

doi:10.1016/0022-2836(84)90424-8

Cited by 63 publications

(35 citation statements)

References 14 publications

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“…These surface components presumably stabilize the fibril diameter by preventing further lateral accretion of collagen molecules. Our prediction for the diameter of the hydrated thin fibrils (16.1 nm) agrees well with the value (16 nm) predicted from x-ray fiber diffraction of lamprey notochord, which is rich in cartilage-like collagen fibrils (20). The 10ϩ4 microfibril structure is consistent with an assembly mechanism that generates 16-nm-diameter thin cartilage fibrils despite variations in the ratio of ambient collagen II͞XI molecules.…”

Section: Discussionsupporting

confidence: 86%

The 10+4 microfibril structure of thin cartilage fibrils

Holmes

Kadler

2006

Proc. Natl. Acad. Sci. U.S.A.

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Determining the structure of cartilage collagen fibrils will provide insights into how mutations in collagen genes affect cartilage formation during skeletal morphogenesis and understanding the mechanism of fibril growth. The fibrils are indeterminate in size, heteropolymeric, and highly cross-linked, which make them refractory to analysis by conventional high-resolution structure determination techniques. Electron microscopy has been limited to making simple measurements of fibril diameter and immunolocalizing certain molecules at the fibril surface. Consequently, structural information on the fibrils is limited. In this study we have used scanning transmission electron microscopic mass mapping, analysis of axial stain exclusion pattern, and r-weighted back-projection techniques to determine the intermediate resolution (to Ϸ4 nm) structure of thin collagen fibrils from embryonic cartilage. The analyses show that the fibrils are constructed from a 10؉4 microfibrillar arrangement in which a core of four microfibrils is surrounded by a ring of 10 microfibrils. Accurate mass measurements predict that each microfibril contains five collagen molecules in cross-section. Based on the proportion of collagen II, IX, and XI in the fibrils, the fibril core comprises two microfibrils each of collagen II and collagen XI. Single molecules of collagen IX presumably occur at the fibril surface between the extended N-terminal domains of collagen XI. The 10؉4 microfibril structure explains the mechanism of diameter limitation in the narrow fibrils and the absence of narrow collagen fibrils in cartilage lacking collagen XI.chondrodysplasia ͉ collagen ͉ electron microscopy ͉ mass mapping ͉ reconstruction T he ability of cartilage to withstand cycles of compression and relaxation relies on a felt-like extracellular matrix (ECM) of insoluble collagen fibrils within a concentrated solution of proteoglycans and glycoconjugates. The collagen fibrils withstand the swelling pressure exerted on the ECM by the hydrated glycosaminoglycan side chains of the proteoglycans. However, this apparently simple role of the collagen fibrils belies enormous effort over many years to understand fibril structure and function as a means of explaining how mutations in cartilage fibril genes produce developmental defects. In particular, it is perplexing why cartilage has two distinct populations of collagen fibrils; one thin (Ϸ20-nm diameter) and the other thick (Ϸ40-nm diameter). Also, it is a quandary why cartilage fibrils of diameter between 20 and 40 nm do not exist in cartilage; also whereas the thin fibrils are all Ϸ20 nm in diameter, the thick fibrils have a much broader diameter distribution. In this respect, the thick fibrils are more like fibrils in noncartilagenous tissues, which can range from 30 to 500 nm in diameter (1). We reasoned that determination of the structure of the thin fibrils was an essential first step in understanding cartilage fibril structure and function.Cartilage fibrils are D-periodic (where D Ϸ 67 nm), indeterminate in leng...

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Section: Discussionsupporting

confidence: 86%

The 10+4 microfibril structure of thin cartilage fibrils

Holmes

Kadler

2006

Proc. Natl. Acad. Sci. U.S.A.

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“…This means that x-ray diffraction experiments on whole intact tissue samples can provide information concerning the axial organization of collagen. Such structural data have been obtained previously (15,16) but were less detailed than that seen recently for collagen type I (obtained by our group) (17)(18)(19). In this study, we applied techniques developed during earlier investigations of type I collagen structure (17, 19 -21), to better define the D-periodic structure of type II collagen fibrils in situ.…”

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confidence: 88%

“…Type II collagen fibrils have an intrinsically crystalline D-periodic structure, even though their lateral arrangement is less well ordered (15,16). This means that x-ray diffraction experiments on whole intact tissue samples can provide information concerning the axial organization of collagen.…”

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confidence: 99%

In Situ D-periodic Molecular Structure of Type II Collagen

Antipova

Orgel

2010

Journal of Biological Chemistry

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Collagens are essential components of extracellular matrices in multicellular animals. Fibrillar type II collagen is the most prominent component of articular cartilage and other cartilagelike tissues such as notochord. Its in situ macromolecular and packing structures have not been fully characterized, but an understanding of these attributes may help reveal mechanisms of tissue assembly and degradation (as in osteo-and rheumatoid arthritis). In some tissues such as lamprey notochord, the collagen fibrillar organization is naturally crystalline and may be studied by x-ray diffraction. We used diffraction data from native and derivative notochord tissue samples to solve the axial, D-periodic structure of type II collagen via multiple isomorphous replacement. The electron density maps and heavy atom data revealed the conformation of the nonhelical telopeptides and the overall D-periodic structure of collagen type II in native tissues, data that were further supported by structure prediction and transmission electron microscopy. These results help to explain the observed differences in collagen type I and type II fibrillar architecture and indicate the collagen type II cross-link organization, which is crucial for fibrillogenesis. Transmission electron microscopy data show the close relationship between lamprey and mammalian collagen fibrils, even though the respective larger scale tissue architecture differs.

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“…Previous attempts to study the high-resolution structure of collagen fibrils have used primarily x-ray fiber diffraction of rat tail tendon (e.g., ref. 1 and references therein) and lamprey notochord (2) in which the fibrils are aligned and composed mostly of one genetic type of collagen. This method has yielded information about the triple-helical structure of the collagen molecules.…”

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confidence: 99%

Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization

Holmes

Gilpin

Baldock

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

214

142

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The ability of the cornea to transmit light while being mechanically resilient is directly attributable to the formation of an extracellular matrix containing orthogonal sheets of collagen fibrils. The detailed structure of the fibrils and how this structure underpins the mechanical properties and organization of the cornea is understood poorly. In this study, we used automated electron tomography to study the three-dimensional organization of molecules in corneal collagen fibrils. The reconstructions show that the collagen molecules in the 36-nm diameter collagen fibrils are organized into microfibrils (Ϸ4-nm diameter) that are tilted by Ϸ15°to the fibril long axis in a right-handed helix. An unexpected finding was that the microfibrils exhibit a constant-tilt angle independent of radial position within the fibril. This feature suggests that microfibrils in concentric layers are not always parallel to each other and cannot retain the same neighbors between layers. Analysis of the lateral structure shows that the microfibrils exhibit regions of order and disorder within the 67-nm axial repeat of collagen fibrils. Furthermore, the microfibrils are ordered at three specific regions of the axial repeat of collagen fibrils that correspond to the N-and C-telopeptides and the d-band of the gap zone. The reconstructions also show macromolecules binding to the fibril surface at sites that correspond precisely to where the microfibrils are most orderly.automated electron tomography ͉ microfibril ͉ filaments T he cornea is a highly specialized tissue that combines optical transparency with mechanical resilience. These properties are directly attributable to the formation of an extracellular matrix containing narrow-diameter (Ϸ36 nm) and heterotypic collagen fibrils that are spaced and organized uniformly into sheets of parallel fibrils. Each sheet is arranged orthogonal to its neighbor and to the path of light through the cornea. We reasoned that an understanding of the morphogenesis of the corneal stroma requires detailed knowledge of the structure of individual collagen fibrils.Corneal fibrils are D-periodic (axial periodicity of collagen fibrils, where D Ϸ67 nm), uniformly narrow (Ϸ30-35 nm in diameter), and indeterminate in length, particularly in older animals. The D-periodicity of the fibril arises from side-to-side associations of triple-helical collagen molecules that are Ϸ300 nm in length (i.e., the molecular length ϭ 4.4 ϫ D) and are staggered by D. The D-stagger of collagen molecules produces alternating regions of protein density in the fibril, which explains the characteristic gap and overlap appearance of fibrils negatively contrasted for transmission electron microscopy. Previous attempts to study the high-resolution structure of collagen fibrils have used primarily x-ray fiber diffraction of rat tail tendon (e.g., ref. 1 and references therein) and lamprey notochord (2) in which the fibrils are aligned and composed mostly of one genetic type of collagen. This method has yielded information about the triple...

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Crystalline fibril structure of type II collagen in lamprey notochord sheath

Cited by 63 publications

References 14 publications

The 10+4 microfibril structure of thin cartilage fibrils

The 10+4 microfibril structure of thin cartilage fibrils

In Situ D-periodic Molecular Structure of Type II Collagen

Corneal collagen fibril structure in three dimensions: Structural insights into fibril assembly, mechanical properties, and tissue organization

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