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. 2022 Oct 5;13:997288. doi: 10.3389/fendo.2022.997288

Table 3.

Novel bioengineering and regenerative medicine approaches to produce treatments for hypothyroidism.

Reference Author Scaffold Material Cells Type Study Method Result
(146) Antonica et al., 2012 Matrigel Murine ESCs In vivo (mice) Recombinant tetracycline inducible NKX2.1 & PAX8 ESC lines generated, which were differentiated into embryoid bodies in hanging drops and into thyroid follicles in Matrigel-supported 3D culture with addition of rhTSH and Dox. The organoids were grafted under the renal capsule of hypothyroid female mice. Overexpression of NKX2.1 & PAX8 induced differentiation of ESCs into FTCs. Cells showed iodide organification activity and formed follicular organoid structures in vitro. These rescued thyroid hormone plasma levels in vivo.
(147) Arauchi et al., 2009 NA Primary rat thyroid cells In vivo (rats) Thyroids were minced & incubated with collagenase type II and IV before culturing on temperature responsive PIPAAm dishes. Cell sheets were implanted subcutaneously into the gluteus after 1-week of culture. Serum T3 and T4 significantly increased 1 week after transplant and were maintained for 4 weeks. Morphological analysis showed typical follicle organization, microvessel formation and the presence of follicle epithelial cells.
(148) Bulanova et al., 2017 Collagen hydrogel Primary murine thyroid cells & Allantoids In vivo (mice) Thyroid spheroids and allantoic spheroids were used as a source of thyrocytes and endothelial cells. These were printed in close association within a collagen hydrogel and implanted into mice. Epithelial cells invaded and vascularized thyrocytes leading to the progressive formation of follicles. These were able to restore body temperature and serum T4 levels in mice.
(149) Gabr et al., 2018 Decellularized porcine liver organoid Wharton Jelly derived MSCs In vivo (mice) Thyroid islets, produced through addition of Activin A and TSH, were loaded onto decellularized porcine liver organoids supplemented with TSH and iodine, then implanted intraperitoneal or intramuscular into mice. Organoid corrected the hypothyroid state and showed viability and function at both implantation sites. Intramuscular transplantation showed higher vascularity and iodine uptake.
(150) Kurmann et al., 2015 Matrigel Murine iPSCs In vitro Nkx2-1(GEP); Pax8(tdTomato trace) iPSCs were generated and differentiation directed towards thyroid with specific factors to induce Nkx2-1 expression. Cells were cultured 2D or in 3D Matrigel for organoid production. Successfully matured thyroid progenitors derived from mouse iPSCs into thyroid follicular organoids which secrete T3, T4 and TSH.
(151) Martin et al., 1993 Matrigel Human follicular thyroid cells In vivo (mice) Organoids were constructed from thyrocytes, embedded into a basement membrane preparation, and transplanted into SCID mice. Widespread neofollicle formation was observed after 4 weeks of transplant. Murine T4 levels were not altered but human Tg was secreted and increased in response to TSH stimulation.
(152) Mastrogiacomo, et al., 2012 3.5-5% PLLA in anhydrous dichloromethane/amylene or 3% PCL in anhydrous tetrahydrofuran/BHT Primary rat thyroid cells In vitro The biomaterial scaffolds were prepared on wet glass support and cells seeded, allowing 8 days for growth. Both biomaterial sheets promoted survival, adhesion, and proliferation of primary thyroid elements. T3 and T4 secretion varied but were a higher volume than in monolayer cultures.
(153) Pan et al., 2019 Decellularized thyroid gland (Male Lewis Rats) FRTL-5 or Primary human follicular thyroid & parathyroid cells In vitro Thyroid gland decellularized with 1% SDS and recellularized perfusion seeding Retained ECM and vascular network of native thyroid. Recellularized thyroid-maintained expression of Tg, thyroid peroxidase, and parathyroid hormone.
(154) Risheng Ma, 2015 Gelatin/Matrigel Human ESCs In vitro Human PAX8 and NKX2-1 were expressed in ESCs with pEZ-lentiviral vectors, followed by differentiation into thyroid cells directed by Activin A and TSH within Gelatin/Matrigel Double transfected cells expressed thyroid specific genes and the differentiation approach induced thyroid follicle formation. TSH stimulation induced dose-dependent cAMP generation and radioiodine uptake.
(155) Strusi, V., et al., 2012 Decellularized thyroid gland (Sprague-Dawley Male Rats) Primary follicular thyroid or ABCG2+ thyroid stem/precursor (S/P) cells In vitro Thyroid matrix obtained by freezing/detergent/enzyme processing. Cells were expanded in a monolayer or 3D Matrigel culture before scaffold recellularization. Thyroid architecture and SVS were maintained. S/P initiated follicle formation. Thyroid hormones were secreted for 7 days (minimum).
(156) Strusi, V., et al., 2011 Decellularized thyroid gland (Sprague-Dawley Male Rats) Primary rat thyroid cells In vitro Rat thyroids were decellularized through freezing/thawing and sequential washes with 0.02% trypsin/0.05% EDTA, 3% Triton-x100, 4% deoxycholic acid and 0.1% peracetic acid (1% P/S/Fungizone). Cells were seeded in the inner surface of the matrix. Native 3D architecture and the thyroid SVS were retained. Thyroid-derived cells aggregate, form intracytoplasmic cavities up to follicular coating and undergo secretory de-differentiation.
(157) Weng, et al., 2021 Decellularized thyroid gland (New Zealand White Rabbits) Human follicular thyroid cells In vitro Thyroid gland decellularized with 1% SDS and recellularized with HFTCs Maintained biomechanical properties, ECM, and cytokine composition of the native thyroid. Thyroid peroxidase secretion present. No cytotoxicity was induced.
(158) Yang et al., 2016 Alginate-poly-l-ornithine-alginate (APA) Primary porcine thyroid cells In vitro Porcine primary thyroid cells were obtained through dissociation and collagenase digestions. The cells were suspended in low-viscosity-high-mannuronic acid solution, and the inner alginate core was formed by a microfluidic device. The inner core was coated to form an APA multilayer following cross-linking in a calcium chloride solution The porcine cells successfully formed thyroid follicles in the microcapsule and displayed viability and proliferation. T4 was released significantly higher in encapsulated cells than unencapsulated cells.

NKX2.1, NK2 Homebox 1; PAX8, Paired Box 8; ESC, embryonic stem cell; rhTSH, recombinant human thyroid stimulating hormone; FTC, follicular thyroid cell; NA, Not applicable; PIPAAm, Poly(N-isopropylacrylamide); MSC, mesenchymal stem cell; iPSC, induced pluripotent stem cell; SCID, severe combined immunodeficient; Tg= Thyroglobulin; PLL, Poly-L-lactic acid; PCL, Poly-Ꜫ-caprolactone; BHT, butylated hydroxytoluene; FRTL-5, Fischer Rat Thyroid low serum 5%; SDS, Sodium Dodecyl Sulphate; ECM, extracellular matrix; EDTA, ethylenediaminetetraacetic acid; SVS, stromal vascular scaffold; S/P, Stem/Precursor; P/S, Penicillin/Streptomycin; HFTC, human follicular thyroid cell.