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      Prostaglandin F2α Agonists Negatively Modulate the Size of 3D Organoids from Primary Human Orbital Fibroblasts

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          Abstract

          Purpose

          To elucidate the molecular etiology of deepening of the upper eyelid sulcus (DUES) induced by prostaglandin (PG) analogs, a three-dimensional (3D) tissue culture system was employed using human orbital fibroblasts (HOFs).

          Methods

          During adipogenesis, changes in HOF 3D organoid sizes, as well as their lipids stained by BODIPY and expression of the extracellular matrix (ECM) by immunolabeling and/or quantitative PCR, were studied in the presence or absence of either 100-nM bimatoprost acid or 100-nM prostaglandin F2α.

          Results

          The size of the 3D organoids increased remarkably during adipogenesis, but such increases were significantly inhibited by the presence of PG analogs. Staining intensities by BODIPY and mRNA expression of peroxisome proliferator-activated receptor gamma were significantly increased upon adipogenesis but were not influenced by the presence of PG analogs. Unique changes in ECM expression observed with or without adipogenic differentiation were significantly modified by the presence of PG analogs.

          Conclusions

          Our present study indicates that PG analogs have the potential to modulate the ECM network within HOF 3D organoids. Thus, a 3D tissue culture system may be a suitable strategy for understanding the disease etiology of DUES.

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          Most cited references41

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          Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Collaborative Normal-Tension Glaucoma Study Group.

          (1998)
          To determine if intraocular pressure plays a part in the pathogenic process of normal-tension glaucoma. One eye of each eligible subject was randomized either to be untreated as a control or to have intraocular pressure lowered by 30% from baseline. Eyes were randomized if they met criteria for diagnosis of normal-tension glaucoma and showed documented progression or high-risk field defects that threatened fixation or the appearance of a new disk hemorrhage. The clinical course (visual field and optic disk) of the group with lowered intraocular pressure was compared with the clinical course when intraocular pressure remained at its spontaneous untreated level. One hundred-forty eyes of 140 patients were used in this study. Sixty-one were in the treatment group, and 79 were untreated controls. Twenty-eight (35%) of the control eyes and 7 (12%) of the treated eyes reached end points (specifically defined criteria of glaucomatous optic disk progression or visual field loss). An overall survival analysis showed a statistically significant difference between the two groups (P < .0001). The mean survival time +/-SD of the treated group was 2,688 +/- 123 days and for the control group, 1,695 +/- 143 days. Of 34 cataracts developed during the study, 11 (14%) occurred in the control group and 23 (38%) in the treated group (P = .0075), with the highest incidence in those whose treatment included filtration surgery. Intraocular pressure is part of the pathogenic process in normal-tension glaucoma. Therapy that is effective in lowering intraocular pressure and free of adverse effects would be expected to be beneficial in patients who are at risk of disease progression.
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            Cell interactions with three-dimensional matrices.

            Edna Cukierman, Roumen Pankov, Kenneth M. Yamada (2002)
            Signaling and other cellular functions differ in three-dimensional compared with two-dimensional systems. Cell adhesion structures can evolve in vitro towards in-vivo-like adhesions with distinct biological activities. In this review, we examine recent advances in studies of interactions of fibroblasts with collagen gels and fibronectin-containing matrices that mimic in vivo three-dimensional microenvironments. These three-dimensional systems are illuminating mechanisms of cell-matrix interactions in living organisms.
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              Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions.

              Jane Sottile, Denise C. Hocking (2002)
              Remodeling of extracellular matrices occurs during development, wound healing, and in a variety of pathological processes including atherosclerosis, ischemic injury, and angiogenesis. Thus, identifying factors that control the balance between matrix deposition and degradation during tissue remodeling is essential for understanding mechanisms that regulate a variety of normal and pathological processes. Using fibronectin-null cells, we found that fibronectin polymerization into the extracellular matrix is required for the deposition of collagen-I and thrombospondin-1 and that the maintenance of extracellular matrix fibronectin fibrils requires the continual polymerization of a fibronectin matrix. Further, integrin ligation alone is not sufficient to maintain extracellular matrix fibronectin in the absence of fibronectin deposition. Our data also demonstrate that the retention of thrombospondin-1 and collagen I into fibrillar structures within the extracellular matrix depends on an intact fibronectin matrix. An intact fibronectin matrix is also critical for maintaining the composition of cell-matrix adhesion sites; in the absence of fibronectin and fibronectin polymerization, neither alpha5beta1 integrin nor tensin localize to fibrillar cell-matrix adhesion sites. These data indicate that fibronectin polymerization is a critical regulator of extracellular matrix organization and stability. The ability of fibronectin polymerization to act as a switch that controls the organization and composition of the extracellular matrix and cell-matrix adhesion sites provides cells with a means of precisely controlling cell-extracellular matrix signaling events that regulate many aspects of cell behavior including cell proliferation, migration, and differentiation.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Invest Ophthalmol Vis Sci
                Journal ID (iso-abbrev): Invest. Ophthalmol. Vis. Sci
                Journal ID (pmc): iovs
                Journal ID (publisher-id): IOVS
                Title: Investigative Ophthalmology & Visual Science
                Publisher: The Association for Research in Vision and Ophthalmology
                ISSN (Print): 0146-0404
                ISSN (Electronic): 1552-5783
                Publication date (Electronic): 05 June 2020
                Publication date Collection: June 2020
                Volume: 61
                Issue: 6
                Electronic Location Identifier: 13
                Affiliations
                [1]Department of Ophthalmology, Sapporo Medical University School of Medicine, Sapporo, Japan
                Author notes
                [* ]Correspondence: Fumihito Hikage, Sapporo Medical University School of Medicine, 17 Chome Minami 1 Jonishi, Chuo Ward, Sapporo, Hokkaido 060-8556, Japan; fuhika@ 123456gmail.com .

                KI and FH contributed equally to the work presented here and therefore should be regarded as equivalent authors.

                Article
                Publisher ID: IOVS-20-29438
                DOI: 10.1167/iovs.61.6.13
                PMC ID: 7415291
                PubMed ID: 32503053
                SO-VID: 38f0f96e-5fea-488d-a2a2-ccce9fcd8773
                Copyright © Copyright 2020 The Authors
                License:

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

                History
                Date accepted : 03 May 2020
                Date received : 27 January 2020
                Page count
                Pages: 9
                Categories
                Subject: Glaucoma
                Subject: Glaucoma

                Keywords: deepening of the upper eyelid sulcus,prostaglandin analogs,three-dimensional tissue culture
                Data availability:
                Keywords: deepening of the upper eyelid sulcus, prostaglandin analogs, three-dimensional tissue culture

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