Stem Cell Antigen 1-positive Mesenchymal Cells Are the Origin of Follicular Cells During Thyroid Regeneration

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Nov 27

PMID 24278321

Citations 12

Authors

Minoru Okamoto

Suguru Hayase

Masaaki Miyakoshi

Tsubasa Murata

Shioko Kimura

Affiliations

Soon will be listed here.

Abstract

Many tissues are thought to contain adult stem/progenitor cells that are responsible for repair of the tissue where they reside upon damage and/or carcinogenesis, conditions when cellular homeostasis becomes uncontrolled. While the presence of stem/progenitor cells of the thyroid has been suggested, how these cells contribute to thyroid regeneration remains unclear. Here we show the origin of thyroid follicular cells and the process of their maturation to become follicular cells during regeneration. By using β-galactosidase (β-gal) reporter mice in conjunction with partial thyroidectomy as a model for thyroid regeneration, and bromodeoxyuridine (BrdU) long label-retaining cell analysis, we demonstrated that stem cell antigen 1 (Sca1) and BrdU-positive, but β-gal and NKX2-1 negative cells were found in the non-follicular mesenchymal area 7 days after partial thyroidectomy. They temporarily co-expressed cytokeratin 14, and were observed in part of follicles by day 35 post-partial thyroidectomy. Sca1, BrdU, β-gal, and NKX2-1-positive cells were found 120 days post-partial thyroidectomy. These results suggested that Sca1 and BrdU positive cells may participate in the formation of new thyroid follicles after partial thyroidectomy. The process of thyroid follicular cell regeneration was recapitulated in ex vivo thyroid slice collagen gel culture studies. These studies will facilitate research on thyroid stem/progenitor cells and their roles in thyroid diseases, particularly thyroid carcinomas.

Citing Articles

Progress Toward and Challenges Remaining for Thyroid Tissue Regeneration.

Romitti M, Costagliola S Endocrinology. 2023; 164(10).

PMID: 37690118 PMC: 10516459. DOI: 10.1210/endocr/bqad136.

Engineering a functional thyroid as a potential therapeutic substitute for hypothyroidism treatment: A systematic review.

Li L, Sheng Q, Zeng H, Li W, Wang Q, Ma G Front Endocrinol (Lausanne). 2022; 13:1065410.

PMID: 36531472 PMC: 9755335. DOI: 10.3389/fendo.2022.1065410.

Stem Cell Therapy for Thyroid Diseases: Progress and Challenges.

Ye S, Zhu Z Curr Ther Res Clin Exp. 2022; 96:100665.

PMID: 35371349 PMC: 8968462. DOI: 10.1016/j.curtheres.2022.100665.

Adult mouse and human organoids derived from thyroid follicular cells and modeling of Graves' hyperthyroidism.

van der Vaart J, Bosmans L, Sijbesma S, Knoops K, van de Wetering W, Otten H Proc Natl Acad Sci U S A. 2021; 118(51).

PMID: 34916298 PMC: 8713972. DOI: 10.1073/pnas.2117017118.

The Transient Human Thyroid Progenitor Cell: Examining the Thyroid Continuum from Stem Cell to Follicular Cell.

Davies T, Latif R, Sachidanandam R, Ma R Thyroid. 2021; 31(8):1151-1159.

PMID: 33678005 PMC: 8377509. DOI: 10.1089/thy.2020.0930.

References

Shimura H, Okajima F, Ikuyama S, Shimura Y, Kimura S, Saji M . Thyroid-specific expression and cyclic adenosine 3',5'-monophosphate autoregulation of the thyrotropin receptor gene involves thyroid transcription factor-1. Mol Endocrinol. 1994; 8(8):1049-69. DOI: 10.1210/mend.8.8.7997232. View

Radisky D, LaBarge M . Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell. 2008; 2(6):511-2. DOI: 10.1016/j.stem.2008.05.007. View

Burger P, Xiong X, Coetzee S, Salm S, Moscatelli D, Goto K . Sca-1 expression identifies stem cells in the proximal region of prostatic ducts with high capacity to reconstitute prostatic tissue. Proc Natl Acad Sci U S A. 2005; 102(20):7180-5. PMC: 1129148. DOI: 10.1073/pnas.0502761102. View

Osawa M, Hanada K, Hamada H, Nakauchi H . Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science. 1996; 273(5272):242-5. DOI: 10.1126/science.273.5272.242. View

Williams E, Toyn C, Harach H . The ultimobranchial gland and congenital thyroid abnormalities in man. J Pathol. 1989; 159(2):135-41. DOI: 10.1002/path.1711590208. View

Ozaki T, Nagashima K, Kusakabe T, Kakudo K, Kimura S . Development of thyroid gland and ultimobranchial body cyst is independent of p63. Lab Invest. 2010; 91(1):138-46. PMC: 2989347. DOI: 10.1038/labinvest.2010.137. View

Smith G . Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development. 2005; 132(4):681-7. DOI: 10.1242/dev.01609. View

Soriano P . Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet. 1999; 21(1):70-1. DOI: 10.1038/5007. View

Summer R, Kotton D, Sun X, Fitzsimmons K, Fine A . Translational physiology: origin and phenotype of lung side population cells. Am J Physiol Lung Cell Mol Physiol. 2004; 287(3):L477-83. DOI: 10.1152/ajplung.00020.2004. View

10.

Yamamoto Y, Yasumizu R, Amou Y, Watanabe N, Nishio N, Toki J . Characterization of peripheral blood stem cells in mice. Blood. 1996; 88(2):445-54. View

11.

Ozaki T, Matsubara T, Seo D, Okamoto M, Nagashima K, Sasaki Y . Thyroid regeneration: characterization of clear cells after partial thyroidectomy. Endocrinology. 2012; 153(5):2514-25. PMC: 3339649. DOI: 10.1210/en.2011-1365. View

12.

Gussoni E, Soneoka Y, Strickland C, Buzney E, Khan M, Flint A . Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature. 1999; 401(6751):390-4. DOI: 10.1038/43919. View

13.

Civitareale D, Castelli M, Falasca P, Saiardi A . Thyroid transcription factor 1 activates the promoter of the thyrotropin receptor gene. Mol Endocrinol. 1993; 7(12):1589-95. DOI: 10.1210/mend.7.12.8145764. View

14.

Lan L, Cui D, Nowka K, Derwahl M . Stem cells derived from goiters in adults form spheres in response to intense growth stimulation and require thyrotropin for differentiation into thyrocytes. J Clin Endocrinol Metab. 2007; 92(9):3681-8. DOI: 10.1210/jc.2007-0281. View

15.

Merok J, Lansita J, Tunstead J, Sherley J . Cosegregation of chromosomes containing immortal DNA strands in cells that cycle with asymmetric stem cell kinetics. Cancer Res. 2002; 62(23):6791-5. View

16.

Manley N, Capecchi M . Hox group 3 paralogs regulate the development and migration of the thymus, thyroid, and parathyroid glands. Dev Biol. 1998; 195(1):1-15. DOI: 10.1006/dbio.1997.8827. View

17.

Toda S, Aoki S, Suzuki K, Koike E, Ootani A, Watanabe K . Thyrocytes, but not C cells, actively undergo growth and folliculogenesis at the periphery of thyroid tissue fragments in three-dimensional collagen gel culture. Cell Tissue Res. 2003; 312(3):281-9. DOI: 10.1007/s00441-003-0718-0. View

18.

Asakura A, Rudnicki M . Side population cells from diverse adult tissues are capable of in vitro hematopoietic differentiation. Exp Hematol. 2002; 30(11):1339-45. DOI: 10.1016/s0301-472x(02)00954-2. View

19.

Haruna Y, Saito K, Spaulding S, Nalesnik M, Gerber M . Identification of bipotential progenitor cells in human liver development. Hepatology. 1996; 23(3):476-81. DOI: 10.1002/hep.510230312. View

20.

Burstein D, Nagi C, Wang B, Unger P . Immunohistochemical detection of p53 homolog p63 in solid cell nests, papillary thyroid carcinoma, and hashimoto's thyroiditis: A stem cell hypothesis of papillary carcinoma oncogenesis. Hum Pathol. 2004; 35(4):465-73. DOI: 10.1016/j.humpath.2003.10.027. View