Investigating the mechanical properties of zona pellucida of whole human oocytes by atomic force spectroscopy

Andolfi, Laura; Masiero, Elena; Giolo, Elena; Martinelli, Monica; Luppi, Stefania; Zilio, Simone Dal; Delfino, Ines; Bortul, Roberta; Zweyer, Marina; Ricci, Giuseppe; Lazzarino, Marco

doi:10.1039/c6ib00044d

Cited by 39 publications

(39 citation statements)

References 39 publications

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“…The elastic response of the ZP outer layer is different and distinguishable from the rest of ZP-HO for all maturation stages. Furthermore, these elasticity values are observed to change with maturation stage and the quality of the oocytes [67]. Similar AFM indentation measurements on vitrified oocytes confirmed this mechanical response and demonstrate that the elasticity of cryopreserved oocyte remains unchanged after thawing and is not affected by the freezing procedure [68].…”

Section: The Mechanical Properties Of the Oocytesupporting

confidence: 64%

Scanning Probe Microscopies: Imaging and Biomechanics in Reproductive Medicine Research

Andolfi

Battistella

Zanetti

et al. 2021

IJMS

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Basic and translational research in reproductive medicine can provide new insights with the application of scanning probe microscopies, such as atomic force microscopy (AFM) and scanning near-field optical microscopy (SNOM). These microscopies, which provide images with spatial resolution well beyond the optical resolution limit, enable users to achieve detailed descriptions of cell topography, inner cellular structure organization, and arrangements of single or cluster membrane proteins. A peculiar characteristic of AFM operating in force spectroscopy mode is its inherent ability to measure the interaction forces between single proteins or cells, and to quantify the mechanical properties (i.e., elasticity, viscoelasticity, and viscosity) of cells and tissues. The knowledge of the cell ultrastructure, the macromolecule organization, the protein dynamics, the investigation of biological interaction forces, and the quantification of biomechanical features can be essential clues for identifying the molecular mechanisms that govern responses in living cells. This review highlights the main findings achieved by the use of AFM and SNOM in assisted reproductive research, such as the description of gamete morphology; the quantification of mechanical properties of gametes; the role of forces in embryo development; the significance of investigating single-molecule interaction forces; the characterization of disorders of the reproductive system; and the visualization of molecular organization. New perspectives of analysis opened up by applying these techniques and the translational impacts on reproductive medicine are discussed.

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Section: The Mechanical Properties Of the Oocytesupporting

confidence: 64%

Scanning Probe Microscopies: Imaging and Biomechanics in Reproductive Medicine Research

Andolfi

Battistella

Zanetti

et al. 2021

IJMS

Self Cite

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“…This work contributes to a larger body of work on measuring the mechanical properties of the ovary 31,39,40,46,[54][55][56][57][58][59][60] and related specialized ECMs, the cumulus oophorus 61,62 and zona pellucida. 63,64 The mechanical properties of mammalian ovary and related cells and ECMs have been investigated using numerous techniques, including nanoindentation, SW elastography (ultrasound and MR), tensile testing, and rheology. These studies, even those using similar techniques, often report different physical properties (e.g., Young's modulus vs. tensile strength; strain ratio vs. SW velocity), making comparisons between studies difficult or sometimes impossible.…”

Section: Limitationsmentioning

confidence: 99%

Ultrasound Shear Wave Velocity Varies Across Anatomical Region in Ex Vivo Bovine Ovaries

Gargus

Jakubowski

Arenas

et al. 2020

Tissue Engineering Part A

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The physical properties of the ovarian extracellular matrix (ECM) regulate the function of ovarian cells, specifically the ability of the ovary to maintain a quiescent primordial follicle pool while allowing a subset of follicles to grow and mature in the estrous cycle. Design of a long-term, cycling artificial ovary has been hindered by the limited information regarding the mechanical properties of the ovary. In particular, differences in the mechanical properties of the two ovarian compartments, the cortex and medulla, have never been quantified. Shear wave (SW) ultrasound elastography is an imaging modality that enables assessment of material properties, such as the mechanical properties, based on the velocity of SWs, and visualization of internal anatomy, when coupled with B-mode ultrasound. We used SW ultrasound elastography to assess whole, ex vivo bovine ovaries. We demonstrated, for the first time, a difference in mechanical properties, as inferred from SW velocity, between the cortex and medulla, as measured along the length (cortex: 2.57-0.53 m/s, medulla: 2.87-0.77 m/s, p < 0.0001) and width (cortex: 2.99-0.81 m/s, medulla: 3.24-0.97 m/s, p < 0.05) and that the spatial distribution and magnitude of SW velocity vary between these two anatomical planes. This work contributes to a larger body of literature assessing the mechanical properties of the ovary and related cells and specialized ECMs and will enable the rational design of biomimetic tissue engineered models and durable bioprostheses. Impact Statement Shear wave (SW) ultrasound elastography can be used to simultaneously assess the material properties and tissue structures when accompanied with B-mode ultrasound. We report a quantitative difference in mechanical properties, as inferred from SW velocity, between the cortex and medulla, with SW velocity being 11.4% and 8.4% higher in the medulla than the cortex when measured along the length and width, respectively. This investigation into the spatial and temporal variation in SW velocity in bovine ovaries will encourage and improve design of more biomimetic scaffolds for ovarian tissue engineering.

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“… 2006 ; Andolfi et al. 2016 ) of the oocyte change with maturation. The ooplasm (OP) is surrounded by the oolemma, the perivitelline space, and the zona pellucida (ZP).…”

Section: Introductionmentioning

confidence: 99%

“… 2012 , 2014 ; Andolfi et al. 2016 ), indentation (Khalilian et al. 2013 ), micropipette aspiration (Drobnis et al.…”

Section: Introductionmentioning

confidence: 99%

Visco- and poroelastic contributions of the zona pellucida to the mechanical response of oocytes

Stracuzzi

Dittmann

Böl

et al. 2021

Biomech Model Mechanobiol

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Probing mechanical properties of cells has been identified as a means to infer information on their current state, e.g. with respect to diseases or differentiation. Oocytes have gained particular interest, since mechanical parameters are considered potential indicators of the success of in vitro fertilisation procedures. Established tests provide the structural response of the oocyte resulting from the material properties of the cell’s components and their disposition. Based on dedicated experiments and numerical simulations, we here provide novel insights on the origin of this response. In particular, polarised light microscopy is used to characterise the anisotropy of the zona pellucida, the outermost layer of the oocyte composed of glycoproteins. This information is combined with data on volumetric changes and the force measured in relaxation/cyclic, compression/indentation experiments to calibrate a multi-phasic hyper-viscoelastic model through inverse finite element analysis. These simulations capture the oocyte’s overall force response, the distinct volume changes observed in the zona pellucida, and the structural alterations interpreted as a realignment of the glycoproteins with applied load. The analysis reveals the presence of two distinct timescales, roughly separated by three orders of magnitude, and associated with a rapid outflow of fluid across the external boundaries and a long-term, progressive relaxation of the glycoproteins, respectively. The new results allow breaking the overall response down into the contributions from fluid transport and the mechanical properties of the zona pellucida and ooplasm. In addition to the gain in fundamental knowledge, the outcome of this study may therefore serve an improved interpretation of the data obtained with current methods for mechanical oocyte characterisation.

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Investigating the mechanical properties of zona pellucida of whole human oocytes by atomic force spectroscopy

Cited by 39 publications

References 39 publications

Scanning Probe Microscopies: Imaging and Biomechanics in Reproductive Medicine Research

Scanning Probe Microscopies: Imaging and Biomechanics in Reproductive Medicine Research

Ultrasound Shear Wave Velocity Varies Across Anatomical Region in Ex Vivo Bovine Ovaries

Visco- and poroelastic contributions of the zona pellucida to the mechanical response of oocytes

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