Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix

Kubow, Kristopher E.; Vukmirovic, Radmila; Zhe, Liu; Klotzsch, Enrico; Smith, Michael L.; Gourdon, Delphine; Luna, Sheila; Vogel, Viola

doi:10.1038/ncomms9026

Cited by 277 publications

(276 citation statements)

References 68 publications

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“…2D). Consistent with this notion, imaging studies employing fluorescence probes as an indicator of strain exerted on FN fibrils indicate that collagen associates preferentially with relaxed fibrils, as freshly elaborated FN fibrils are known to be (Kubow et al, 2015)…”

Section: Binding Of Plasma Fn To Collagenmentioning

confidence: 72%

Dynamic structure of plasma fibronectin

Maurer

Mosher

2016

Critical Reviews in Biochemistry and Molecular Biology

103

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Fibronectin is a large vertebrate glycoprotein that is found in soluble and insoluble forms and involved in diverse processes. Protomeric fibronectin is a dimer of subunits, each of which comprises 29 to 31 modules—12 type I, two type II, and 15-17 type III. Plasma fibronectin is secreted by hepatocytes and circulates in a compact conformation before it binds to cell surfaces, converts to an extended conformation, and is assembled into fibronectin fibrils. Here we review biophysical and structural studies that have shed light on how plasma fibronectin transitions from the compact to the extended conformation. The three types of modules each have a well-organized secondary and tertiary structure as defined by NMR and crystallography and have been likened to “beads on a string”. There are flexible sequences in the N-terminal tail, between the fifth and sixth type I modules, between the first two and last two of the type III modules, and at the C-terminus. Several specific module-module interactions have been identified that likely maintain the compact quaternary structure of circulating fibronectin. The quaternary structure is perturbed in response to binding events, including binding of fibronectin to the surface of vertebrate cells for fibril assembly and to bacterial adhesins.

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Section: Binding Of Plasma Fn To Collagenmentioning

confidence: 72%

Dynamic structure of plasma fibronectin

Maurer

Mosher

2016

Critical Reviews in Biochemistry and Molecular Biology

103

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“…The schematic summary of the sequential deposition of tissue components during growth given in figure 5b, is reminiscent of the geometrical model proposed to describe the organization of tensile cells on a curved surface [44], and indicates a transfer of this same organization to the fibrous components of the ECM as previously suggested [45]. It has been shown that collagen can self-organize into highly aligned, chiral and cholesteric liquid crystal-like structures in a completely cell-free system [66][67][68][69], while it can only be assembled in cell culture in the presence of fibronectin [65]. Our results on the coalignment of collagen with previously deposited cells and fibronectin, and on the importance of cellular tension for ECM organization, emphasize the importance of active cellular control over such self-organizing processes.…”

Section: Discussionmentioning

confidence: 97%

Gradual conversion of cellular stress patterns into pre-stressed matrix architecture during in vitro tissue growth

Bidan

Kollmannsberger

Gering

et al. 2016

J. R. Soc. Interface.

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The complex arrangement of the extracellular matrix (ECM) produced by cells during tissue growth, healing and remodelling is fundamental to tissue function. In connective tissues, it is still unclear how both cells and the ECM become and remain organized over length scales much larger than the distance between neighbouring cells. While cytoskeletal forces are essential for assembly and organization of the early ECM, how these processes lead to a highly organized ECM in tissues such as osteoid is not clear. To clarify the role of cellular tension for the development of these ordered fibril architectures, we used an in vitro model system, where pre-osteoblastic cells produced ECM-rich tissue inside channels with millimetre-sized triangular cross sections in ceramic scaffolds. Our results suggest a mechanical handshake between actively contracting cells and ECM fibrils: the build-up of a long-range organization of cells and the ECM enables a gradual conversion of cell-generated tension to pre-straining the ECM fibrils, which reduces the work cells have to generate to keep mature tissue under tension.

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“…Collagen I (Col I) is another prominent ECM protein with multiple contributions to tumorigenesis [7,8]. Col I deposition is primarily dependent on previously assembled Fn matrices [9–12]. Therefore, assessing how Fn-Col I interactions are altered during tumorigenesis is critical to our understanding of tumor stroma modifications that mediate invasive tumor growth.…”

Section: Introductionmentioning

confidence: 99%

Breast cancer cells alter the dynamics of stromal fibronectin-collagen interactions

Wang

Seo

et al. 2017

Matrix Biology

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Breast cancer cells recruit surrounding stromal cells, such as cancer-associated fibroblasts (CAFs), to remodel their extracellular matrix (ECM) and promote invasive tumor growth. Two major ECM components, fibronectin (Fn) and collagen I (Col I), are known to interact with each other to regulate cellular behavior. In this study, we seek to understand how Fn and Col I interplay and promote a dysregulated signaling pathway to facilitate tumor progression. Specifically, we investigated the evolution of tumor-conditioned stromal ECM composition, structure, and relaxation. Furthermore, we assessed how evolving Fn-Col I interactions gradually affected pro-angiogenic signaling. Our data first indicate that CAFs initially assembled a strained, viscous, and unfolded Fn matrix. This early altered Fn matrix was later remodeled into a thick Col I-rich matrix that was characteristic of a dense tumor mass. Next, our results suggest that this ECM remodeling was primarily mediated by matrix metalloproteinases (MMPs). This MMP activity caused profound structural and mechanical changes in the developing ECM, which then modified vascular endothelial growth factor (VEGF) secretion by CAFs and matrix sequestration. Collectively, these findings enhance our understanding of the mechanisms by which Fn and Col I synergistically interplay in promoting a sustained altered signaling cascade to remodel the breast tumor stroma for invasive breast tumor growth.

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Mechanical forces regulate the interactions of fibronectin and collagen I in extracellular matrix

Cited by 277 publications

References 68 publications

Dynamic structure of plasma fibronectin

Dynamic structure of plasma fibronectin

Gradual conversion of cellular stress patterns into pre-stressed matrix architecture during in vitro tissue growth

Breast cancer cells alter the dynamics of stromal fibronectin-collagen interactions

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