Molecular Interactions between Collagen and Fibronectin: A Reciprocal Relationship that Regulates De Novo Fibrillogenesis

Paten, Jeffrey A.; Martin, Cassandra; Wanis, Jamil T.; Siadat, Seyed Mohammad; Figueroa-Navedo, Amanda M.; Ruberti, Jeffrey W.; Deravi, Leila F.

doi:10.1016/j.chempr.2019.05.011

Cited by 42 publications

(50 citation statements)

References 70 publications

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“…Fluorescent labeling of COL COL was amine-labeled with either Alexa Fluor 546 NHS Ester (A546, A20002; Thermo Fisher Scientific) or Alexa Fluor 488 TFP (A488, A30005; Thermo Fisher Scientific) according to the protocol of Paten et al 43 COL was labeled with A488 solution in a 5:1 molar ratio of A488:COL and then purified by dialyzing the solution against 0.01 M hydrochloric acid at pH 2 using a 10,000 MWCO Slide-A-Lyzer dialysis cassette (66380; Thermo Fisher Scientific). The acidic conditions were chosen to prevent the COL from spontaneously assembling.…”

Section: Normalized Absorbancementioning

confidence: 99%

“…The same process was performed with A546 in a 5:1 molar ratio of A546:COL. Before use, the COL concentration was determined by a modified Lowry assay (DC-Protein Assay; Bio-Rad), and the labeling efficiency was determined according to previous reports. 43 We calculated a final molar ratio of 1.0:1 A488:COL and 1.5:1 A546:COL.…”

Section: Normalized Absorbancementioning

confidence: 99%

“…COL assembly in vitro is spontaneous down to a threshold concentration of *1 lg/mL 40,41 ; however, this is rather unlikely to be the threshold in vivo due to the influence of the *200 glycoproteins in the matrisome. 42 For instance, multiple studies demonstrate COL assembly dependence on the presence of fibronectin, binding availability of fibronectin, and integrin-binding interactions in vivo (see Paten et al 43 and references therein).…”

Section: Introductionmentioning

confidence: 99%

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A Role for Monosaccharides in Nucleation Inhibition and Transport of Collagen

et al. 2020

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Background: Collagenous tissues are composed of precisely oriented, tightly packed collagen fibril bundles to confer the maximal strength within the smallest volume. While this compact form benefits mobility, it consequentially restricts vascularity and cell density to a minimally viable level in some regions. These tissues reside in a homeostatic state with an unstable equilibrium, where perturbations to structure or molecular milieu cause descension into a long-term compromised state. Several studies have shown that glycosaminoglycans are key molecules required for healthy tissue maintenance. Our long-term goal is to determine if glycosaminoglycans serve a critical function of stabilizing soluble monomeric collagen in the interstitial fluid that bathes tissue for immediate availability in tissue development and repair in vivo. Materials and Methods: To test glycosaminoglycan and collagen interactions at the most fundamental level, we have explored the effect of the monosaccharides that populate the glycosaminoglycans of the extracellular matrix on collagen assembly kinetics, pre-established matrix stability, and collagen incorporation into a preassembled matrix. Results: Results showed that monosaccharides increased the threshold concentration required for spontaneous polymerization by at least three orders of magnitude. When the monosaccharides were introduced to a pre-existing collagen network, fibrillar dissociation was undetectable. Fluorescent-labeling studies illustrated that in the presence of the saccharide solution, soluble collagen maintains the functional capacity to integrate into a pre-existing network. Conclusion: This work demonstrates a feasible role for glycosaminoglycans in supporting tissue remodeling and highlights the potential importance of age-related deterioration of glycosaminoglycan biosynthesis in reference to the homeostasis of collagen-based tissues.

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Section: Normalized Absorbancementioning

confidence: 99%

Section: Normalized Absorbancementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Role for Monosaccharides in Nucleation Inhibition and Transport of Collagen

et al. 2020

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“…Fibronectin fibril assembly by cells is a highly regulated process requiring both integrin ligation and cell-derived mechanical forces [13]. Several acellular techniques to produce artificial fibronectin fibrils have been reported, typically via the application of mechanical force at a fluid-air interface [24,[38][39][40].…”

Section: Discussionmentioning

confidence: 99%

Acoustic Fabrication of Collagen–Fibronectin Composite Gels Accelerates Microtissue Formation

2020

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Ultrasound can influence biological systems through several distinct acoustic mechanisms that can be manipulated by varying reaction conditions and acoustic exposure parameters. We recently reported a new ultrasound-based fabrication technology that exploits the ability of ultrasound to generate localized mechanical forces and thermal effects to control collagen fiber microstructure non-invasively. Exposing solutions of type I collagen to ultrasound during the period of microfibril assembly produced changes in collagen fiber structure and alignment, and increased the biological activity of the resultant collagen hydrogels. In the extracellular matrix, interactions between fibronectin and collagen fibrils influence the biological activity of both proteins. Thus, in the present study, we examined how addition of fibronectin to collagen solutions prior to ultrasound exposure affects protein organization and the biological activity of the composite hydrogels. Results indicate that ultrasound can alter the distribution of fibronectin within 3D hydrogels via thermal and non-thermal mechanisms to produce composite hydrogels that support accelerated microtissue formation. The use of acoustic energy to drive changes in protein conformation to functionalize biomaterials has much potential as a unique, non-invasive technology for tissue engineering and regenerative medicine.

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“…(B) . Examples of ECM stiffness tuning based on collagen I ( 1 Chhetri et al, 2019 , 2 Levental et al, 2009 , 3 Paten et al, 2019 , 4 Chittiboyina et al, 2018 ). Other matrices of nonmammalian origin may also be used (e.g., agar, alginate, polyacrylamide) and are sometime mixed with ECM molecules (e.g., collagen I, fibronectin).…”

Section: Evidence Of Mechanotransduction To the Genome In Cell Culturmentioning

confidence: 99%

3D Cell Culture for the Study of Microenvironment-Mediated Mechanostimuli to the Cell Nucleus: An Important Step for Cancer Research

Chhetri

Rispoli

Lelièvre

2021

Front. Mol. Biosci.

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The discovery that the stiffness of the tumor microenvironment (TME) changes during cancer progression motivated the development of cell culture involving extracellular mechanostimuli, with the intent of identifying mechanotransduction mechanisms that influence cell phenotypes. Collagen I is a main extracellular matrix (ECM) component used to study mechanotransduction in three-dimensional (3D) cell culture. There are also models with interstitial fluid stress that have been mostly focusing on the migration of invasive cells. We argue that a major step for the culture of tumors is to integrate increased ECM stiffness and fluid movement characteristic of the TME. Mechanotransduction is based on the principles of tensegrity and dynamic reciprocity, which requires measuring not only biochemical changes, but also physical changes in cytoplasmic and nuclear compartments. Most techniques available for cellular rheology were developed for a 2D, flat cell culture world, hence hampering studies requiring proper cellular architecture that, itself, depends on 3D tissue organization. New and adapted measuring techniques for 3D cell culture will be worthwhile to study the apparent increase in physical plasticity of cancer cells with disease progression. Finally, evidence of the physical heterogeneity of the TME, in terms of ECM composition and stiffness and of fluid flow, calls for the investigation of its impact on the cellular heterogeneity proposed to control tumor phenotypes. Reproducing, measuring and controlling TME heterogeneity should stimulate collaborative efforts between biologists and engineers. Studying cancers in well-tuned 3D cell culture platforms is paramount to bring mechanomedicine into the realm of oncology.

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Molecular Interactions between Collagen and Fibronectin: A Reciprocal Relationship that Regulates De Novo Fibrillogenesis

Cited by 42 publications

References 70 publications

A Role for Monosaccharides in Nucleation Inhibition and Transport of Collagen

A Role for Monosaccharides in Nucleation Inhibition and Transport of Collagen

Acoustic Fabrication of Collagen–Fibronectin Composite Gels Accelerates Microtissue Formation

3D Cell Culture for the Study of Microenvironment-Mediated Mechanostimuli to the Cell Nucleus: An Important Step for Cancer Research

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