Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices

Amargant, Farners; Manuel, Sharrón L.; Tu, Qing; Parkes, Wendena S.; Rivas, Felipe; Zhou, Luhan T.; Rowley, Jennifer E.; Villanueva, Cecilia E.; Hornick, Jessica E.; Shekhawat, Gajendra S.; Wei, Jian Jun; Pavone, Mary Ellen; Hall, Adam R.; Pritchard, Michele T.; Duncan, Francesca E.

doi:10.1111/acel.13259

Cited by 146 publications

(164 citation statements)

References 46 publications

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“…Recently, Tanaka et al analyzed plasma proteins of all age groups and identified ~650 age-associated proteins in which extracellular matrix-related proteins were enriched [ 67 ]. Another recent study demonstrated that abundance of hyaluronan, an ECM glycosaminoglycan, gradually decreased with age, leading to the alteration in biomechanical properties of ECM [ 68 ]. As a critical factor for skin moisture, hyaluronan preserves the hydration of skin, thereby suppresses skin aging.…”

Section: Molecular Profile Changes With Age In the Periodontiummentioning

confidence: 99%

Effect of Aging on Homeostasis in the Soft Tissue of the Periodontium: A Narrative Review

Kim

Lee

Bae

et al. 2021

JPM

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Aging is characterized by a progressive decline or loss of physiological functions, leading to increased susceptibility to disease or death. Several aging hallmarks, including genomic instability, cellular senescence, and mitochondrial dysfunction, have been suggested, which often lead to the numerous aging disorders. The periodontium, a complex structure surrounding and supporting the teeth, is composed of the gingiva, periodontal ligament, cementum, and alveolar bone. Supportive and protective roles of the periodontium are very critical to sustain life, but the periodontium undergoes morphological and physiological changes with age. In this review, we summarize the current knowledge of molecular and cellular physiological changes in the periodontium, by focusing on soft tissues including gingiva and periodontal ligament.

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Section: Molecular Profile Changes With Age In the Periodontiummentioning

confidence: 99%

Effect of Aging on Homeostasis in the Soft Tissue of the Periodontium: A Narrative Review

Kim

Lee

Bae

et al. 2021

JPM

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“…In this study, we demonstrated, to our knowledge, the first non-invasive mechanical mapping, with micron-level spatial resolution, of ovarian mechanics in situ. From a biological perspective, our work represents a first step towards addressing the mechanical aspects of folliculogenesis, which has gained recognition due to emerging evidence that mechanical stress in the ovary can influence the quality of the growing oocytes through ECM stiffness 40,41 , Hippo signalling pathway 42,43 and increased fibrosis 44,45 .…”

Section: Discussionmentioning

confidence: 99%

“…3). This may be due to the fact that the theca cells are associated with increased expression of hyaluronic acid, which is known to promote tissue hydration 45 . The theca cell layer therefore provides a softer microenvironment that may serve as a mechanical 'sponge' to buffer the oocyte and somatic cells against external mechanical stress through stress dissipation.…”

Section: Discussionmentioning

confidence: 99%

Mechanical mapping of mammalian follicle development using Brillouin microscopy

Chan

Bevilacqua

Prevedel

2021

Preprint

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In early mammalian development, the maturation of follicles containing the immature oocytes is an important biological process as the functional oocytes provide the bulk genetic and cytoplasmic materials for successful reproduction. Despite recent work demonstrating the regulatory role of mechanical stress in oocyte growth, quantitative studies of ovarian mechanical properties remain lacking both in vivo and ex vivo. In this work, we quantify the material properties of ooplasm, follicles and connective tissues in intact mouse ovaries at distinct stages of follicle development using Brillouin microscopy, a non-invasive tool to probe mechanics in three-dimensional (3D) tissues. We find that the ovarian cortex and its interior stroma have distinct material properties associated with extracellular matrix deposition, and that intra-follicular mechanical compartments emerge during follicle maturation. Our work provides a novel approach to study the role of mechanics in follicle morphogenesis and pave the way for future understanding of mechanotransduction in reproductive biology, with potential implications for infertility diagnosis and treatment.

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“…An important component of the stromal compartment is the ECM and, in particular, its ubiquitous component, hyaluronan; a linear polysaccharide with pleiotropic roles in tissue structure, cell signaling and inflammation (Rowley et al, 2020;Takasugi et al, 2020). In the context of the ovary, recent work has demonstrated that total hyaluronan content in the ovarian stroma decreases with age and is effectively "replaced" by collagen leading to dramatic changes in ovarian biomechanics pertaining to increased stiffness (Amargant et al, 2020). Importantly, these age-associated changes are conserved between the mouse and humans (Amargant et al, 2020) and may be associated with the production of oocytes with compromised morphology, poor meiotic competence, and impaired granulosa cell function (Amargant et al, 2020;Rowley et al, 2020).…”

Section: Ovarian Tissue Aging and Reproductive Disordersmentioning

confidence: 99%

“…In the context of the ovary, recent work has demonstrated that total hyaluronan content in the ovarian stroma decreases with age and is effectively "replaced" by collagen leading to dramatic changes in ovarian biomechanics pertaining to increased stiffness (Amargant et al, 2020). Importantly, these age-associated changes are conserved between the mouse and humans (Amargant et al, 2020) and may be associated with the production of oocytes with compromised morphology, poor meiotic competence, and impaired granulosa cell function (Amargant et al, 2020;Rowley et al, 2020). In pathological states or during tissue aging, it also known that the fragmentation of hyaluronan yields a low molecular weight polymer (<250 kDa) linked to inflammation, fibrotic disease (Takasugi et al, 2020).…”

Section: Ovarian Tissue Aging and Reproductive Disordersmentioning

confidence: 99%

Proteostasis in the Male and Female Germline: A New Outlook on the Maintenance of Reproductive Health

Cafe

Nixon

Ecroyd

et al. 2021

Front. Cell Dev. Biol.

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For fully differentiated, long lived cells the maintenance of protein homeostasis (proteostasis) becomes a crucial determinant of cellular function and viability. Neurons are the most well-known example of this phenomenon where the majority of these cells must survive the entire course of life. However, male and female germ cells are also uniquely dependent on the maintenance of proteostasis to achieve successful fertilization. Oocytes, also long-lived cells, are subjected to prolonged periods of arrest and are largely reliant on the translation of stored mRNAs, accumulated during the growth period, to support meiotic maturation and subsequent embryogenesis. Conversely, sperm cells, while relatively ephemeral, are completely reliant on proteostasis due to the absence of both transcription and translation. Despite these remarkable, cell-specific features there has been little focus on understanding protein homeostasis in reproductive cells and how/whether proteostasis is “reset” during embryogenesis. Here, we seek to capture the momentum of this growing field by highlighting novel findings regarding germline proteostasis and how this knowledge can be used to promote reproductive health. In this review we capture proteostasis in the context of both somatic cell and germline aging and discuss the influence of oxidative stress on protein function. In particular, we highlight the contributions of proteostasis changes to oocyte aging and encourage a focus in this area that may complement the extensive analyses of DNA damage and aneuploidy that have long occupied the oocyte aging field. Moreover, we discuss the influence of common non-enzymatic protein modifications on the stability of proteins in the male germline, how these changes affect sperm function, and how they may be prevented to preserve fertility. Through this review we aim to bring to light a new trajectory for our field and highlight the potential to harness the germ cell’s natural proteostasis mechanisms to improve reproductive health. This manuscript will be of interest to those in the fields of proteostasis, aging, male and female gamete reproductive biology, embryogenesis, and life course health.

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Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 146 publications

References 46 publications

Effect of Aging on Homeostasis in the Soft Tissue of the Periodontium: A Narrative Review

Effect of Aging on Homeostasis in the Soft Tissue of the Periodontium: A Narrative Review

Mechanical mapping of mammalian follicle development using Brillouin microscopy

Proteostasis in the Male and Female Germline: A New Outlook on the Maintenance of Reproductive Health

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