PRIMARY CULTURE OF THYROCYTES, THYROID FOLLICLES AND MICROORGANS OF THE THYROID GLAND AS THE FIRST STAGE OF THE CREATION OF TISSUE ENGINEERING CONSTRUCTS

DOI: https://doi.org/10.29296/24999490-2018-05-02

N.S. Sergeeva(1, 3), Yu.D. Khesuani(2), I.K. Sviridova(1), P.A. Karalkin(1), A.P. Polyakov(1), V.A. Mironov(2), A.D. Kaprin(1) 1-P.A. Herzen Moscow Research Oncological Institute, branch of the National Medical Research Center of Radiology, 3, 2nd Botkinskiy pass, Moscow, 125284, Russian Federation; 2-Laboratory of Biotechnological Research, 3D Bioprinting Solutions, 68/2, Kashirskoe Highway, Moscow, 115409, Russian Federation; 3-N.I.Pirogov Russian National Research Medical University, 1, Ostrovitianova str., Moscow, 117997, Russian Federation E-mail: [email protected]

One of the ways to restore the lost functions of the thyroid gland is the creation of its tissue engineering constructs. The creation of adequate tissue engineering constructs requires either cultures of functionally active thyrocytes capable of forming thyroid follicles or cultures of thyroid follicles or micro-organs cultures of the thyroid gland. The development of such models is the subject of research by a number of laboratories. In this review, the main results of these studies are systematized.
Keywords: 
thyroid gland, primary cultures, thyrocytes, thyroid follicles, micro-organ сultures, tissue engineering constructs

Список литературы: 
  1. He`m A., Kormak D. Gistologiya. V 5-ti tomah. Tom 5. Per. s angl. V.L. Bykova i dr.; pod red. Yu.I. Afanas`eva, Yu.S. Chencova. M.: Mir, 1983; 296. [Ham A.W., Kormak D.H. Histology. Volume 5. M.: Mir, 1983; 296 (in Russian)]
  2. Toda S., Aoki S., Uchihashi K., Matsunobu A., Yamamoto M., Ootani A., Yamasaki F., Koike E., Sugihara H. Culture models for studying thyroid biology and disorders. I.S.R.N. Endocrinol. 2011; 2011: 275782. 9 pp.
  3. Spinel C., Herrera M., Rivera J. Thyroid Culture from Monolayer to Closed Follicles [Chapter in book]. Thyroid Hormone. Ed. by Agrawal N.K. InTech; 2012; Chapter 13.
  4. Bilyavskaya S.B., Bozhok G.A., Legach E.I., Borovoy I.A., Gella I.M., Malyukin Yu.V., Bondarenko T.P. Harakteristika pervichnoy kul`tury kletok iz neonatal`noy shhitovidnoy zhelezy sviney: follikulogenez, gormonal`naya i rostovaya aktivnost`. Citologiya. 2013; 55 (7): 482–91. [Bilyavskaya S.B., Bozhok G.A., Legach E.I., Borovoy I.A., Gella I.M., Malyukin Yu.V., Bondarenko T.P. Characteristics of primary cell culture from neonatal thyroid grand of pigs: folliculogenesis, hormone and growth. Tsitologiya. 2013; 55 (7): 482–91 (in Russian)]
  5. Bertoni A.P., Brum I.S., Hillebrand A.C., Furlanetto T.W. Progesterone Upregulates Gene Expression in Normal Human Thyroid Follicular Cells. Int. J. Endocrinol. 2015; 2015: 864852. 6 pp.
  6. Kogai T., Curcio F., Hyman S., Cornford E.M., Brent G.A., Hershman J.M. Induction of follicle formation in long-term cultured normal human thyroid cells treated with thyrotropin stimulates iodide uptake but not sodium/iodide symporter messenger RNA and protein expression. J. Endocrinol. 2000; 167 (1): 125–35.
  7. Ingeson-Carlsson C., Nilsson M. Switching from MAPK-dependent to MAPK-independent repression of the sodium-iodide symporter in 2D and 3D cultured normal thyroid cells. Mol. Cell Endocrinol. 2013; 381 (1–2): 241–54.
  8. Westermark B., Karlsson F.A., Wålinder O. Thyrotropin is not a growth factor for human thyroid cells in culture. Proc. Natl. Acad. Sci. USA. 1979; 76 (4): 2022–6.
  9. Morgan S.J., Neumann S., Marcus-Samuels B., Gershengorn M.C. Thyrotropin stimulates differentiation not proliferation of normal human thyrocytes in culture. Frontiers in Endocrin. 2016; 7: 168.
  10. Paternot S., Dumont J.E., Roger P.P. Differential utilization of cyclin D1 and cyclin D3 in the distinct mitogenic stimulations by growth factors and TSH of human thyrocytes in primary culture. Mol. Endocrinol. 2006; 20 (12): 3279–92.
  11. Ishido Y., Yamazaki K., Kammori M., Sugishita Y., Luo Y., Yamada E., Yamada T., Sellitti D.F., Suzuki K. Thyroglobulin suppresses thyroid-specific gene expression in cultures of normal but not neoplastic human thyroid follicular cells. J. Clin. Endocrinol. Metab. 2014; 99 (4): 694–702.
  12. Nilsson M., Husmark J., Nilsson B., Tisell L.E., Ericson L.E. Primary culture of human thyrocytes in Transwell bicameral chamber: thyrotropin promotes polarization and epithelial barrier function. Eur. J. Endocrinol. 1996; 135 (4): 469–80.
  13. Sastre-Perona A., Santisteban P. Wnt-independent role of β-catenin in thyroid cell proliferation and differentiation. Mol. Endocrinol. 2014; 28 (5): 681–95.
  14. Fayet G., Hovsépian S. Isolation of a normal human thyroid cell line: hormonal requirement for thyroglobulin regulation. Thyroid. 2002; 12 (7): 539–46.
  15. Ishido Y., Luo Y., Yoshihara A., Hayashi M., Yoshida A., Hisatome I., Suzuki K. Follicular thyroglobulin enhances gene expression necessary for thyroid hormone secretion. Endocr. J. 2015; 62 (11): 1007–15.
  16. Jeker L.T., Hejazi M., Burek C.L., Rose N.R., Caturegli P. Mouse thyroid primary culture. Biochem. Biophys. Res. Commun. 1999; 257 (2): 511–5.
  17. Kimura S., Van Keymeulen A., Golstein J., Fusco A., Dumont J.E., Roger P.P. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr. Rev. 2001; 22 (5): 631–56.
  18. Rapoport B., Filetti S., Takai N., Seto P., Halverson G. Studies on the cyclic AMP response to thyroid stimulating immunoglobulin (TSI) and thyrotropin (TSH) in human thyroid cell monolayers. Metabolism. 1982; 31 (11): 1159–67.
  19. Derwahl M., Manole D., Sobke A., Broecker M. Pathogenesis of toxic thyroid adenomas and nodules: relevance of activating mutations in the TSH-receptor and Gs-alpha gene, the possible role of iodine deficiency and secondary and TSH-independent molecular mechanisms. Exp. Clin. Endocrinol. Diabetes. 1998; 106 (4): 6–9.
  20. Ambesi-Impiombato F.S., Parks L.A., Coon H.G. Culture of hormone–dependent functional epithelial cells from rat thyroids. Proc. Natl. Acad. Sci. USA. 1980; 77 (6): 3455–9.
  21. Lee H.S., Crane G.G., Merok J.R., Tunstead J.R., Hatch N.L., Panchalingam K., Powers M.J., Griffith L.G., Sherley J.L. Clonal expansion of adult rat hepatic stem cell lines by suppression of asymmetric cell kinetics (SACK). Biotechnol. Bioeng. 2003; 83 (7): 760–71.
  22. Ossendorp F.A., Bruning P.F., Schuuring E.M., Van Den Brink J.A., van der Heide D., De Vijlder J.J., De Bruin T.W. Thyrotropin dependent and independent thyroid cell lines selected from FRTL-5 derived tumors grown in nude mice. Endocrinology. 1990; 127 (1): 419–30.
  23. Tasevski V., Benn D., Peters G., Luttrell B., Simpson A. The Fischer rat thyroid cell line FRTL-5 exhibits a nondiploid karyotype. Thyroid. 1998; 8 (7): 623–6.
  24. Pulvertaft R.J.V., Davies J.R., Weiss L., Wilkinson J.H. Studies on tissue cultures of human pathological thyroids. The Journal of Patology. 1959; 77 (1): 19–32.
  25. Takasu N. Primary culture of thyroid cells. Cell and Tissue Culture: Laboratory Procedures. 1996; 17B (1): 1–13.
  26. Toda S., Sugihara H. Primary culture of the thyroid: three-dimensional culture using extracellular matrix. Cell and Tissue Culture: Laboratory Procedures. 1996; 17B (2): 1–12.
  27. Toda S., Koike N., Sugihara H. Thyrocyte integration, and thyroid folliculogenesis and tissue regeneration: perspective for thyroid tissue engineering. Pathol. Int. 2001; 51 (6): 403–17.
  28. Murphy A., Mothersill C., O’Connor M.K., Malone J.F., Cullen M.J., Taaffe J.K. An investigation of the optimum culture conditions for a differentiated culture of sheep thyroid cells. Acta. Endocrinol. (Copenh.). 1983; 104 (4): 431–6.
  29. Lafferty K.J., Bootes A., Dart G., Talmage D.W. Effect of organ culture on the survival of thyroid allografts in mice. Transplantation. 1976; 22 (2): 138–49.
  30. Snell G.D. The homograft reaction. Annu. Rev. Microbiol. 1957; 11: 439–58.
  31. Suzuki K., Mitsutake N., Saenko V., Suzuki M., Matsuse M., Ohtsuru A., Kumagai A., Uga T., Yano H., Nagayama Y., Yamashita S. Dedifferentiation of human primary thyrocytes into multilineage progenitor cells without gene introduction. PLoS One. 2011; 6 (4): e19354.
  32. Wang Y., Li W., Phay J.E., Shen R., Pellegata N.S., Saju M., Rinder M.D., de Chapella A., He H. Primary cell culture systems for human thyroid studies. Thyroid. 2015; 26 (8): 1131–40.
  33. Tret`yak S.I., Hryshhanovich V.Ya. Sovremennye metody lecheniya gipotireoza: monografiya. Minsk: BGMU, 2011; 150. [Tret’jak S.I., Hryshhanovich V.Ja. Sovremennye metody lechenija gipotireoza: monografija. Minsk: BGMU, 2011; 150 (in Russian)]
  34. Tret`yak S.I., Goranov V.A., Hryshhanovich V.Ya. Sposob polucheniya kul`tury ksenogennyh tirocitov dlya lecheniya gipotireoza u cheloveka. Patent Belarusi №13931, 30.12.2010. [Tret’jak S.I., Goranov V.A., Hryshhanovich V.Ja. Sposob poluchenija kul’tury ksenogennyh tirocitov dlja lechenija gipotireoza u cheloveka. Patent Belarus. ID 13931, 30.12.2010 (in Russian)]
  35. Shi H., Lin W., Liang B.O., Cai H., Cai Q., Shi Y., Huang H. Presence of free triiodothyronine and free thyroxine in thyroid follicles may be correlated with the quick secretion of thyroid hormones under certain physiological conditions. Biomed. Rep. 2016; 4 (4): 467–470.
  36. Villacorte M., Delmarcelle A.S., Lernoux M., Bouquet M., Lemoine P., Bolsée J., Umans L., de Sousa Lopes S.C., Van Der Smissen P., Sasaki T., Bommer G., Henriet P., Refetoff S., Lemaigre F.P., Zwijsen A., Courtoy P.J., Pierreux C.E. Thyroid follicle development requires Smad1/5- and endothelial cell-dependent basement membrane assembly. Development. 2016; 143 (11): 1958–70.
  37. Elsdale T., Bard J. Collagen substrata for studies on cell behavior. J. Cell Biol. 1972; 54 (3): 626–37.
  38. Westermark K., Nilsson M., Ebendal T., Westermark B. Thyrocyte migration and histiotypic follicle regeneration are promoted by epidermal growth factor in primary culture of thyroid follicles in collagen gel. Endocrinology. 1991; 129 (4): 2180–6.
  39. Koumarianou P., Goméz-López G., Santisteban P. Pax8 controls thyroid follicular polarity through cadherin-16. J. Cell Sci. 2017; 130 (1): 219–31.
  40. Ingeson-Carlsson C., Nilsson M. Dual contribution of MAPK and PI3K in epidermal growth factor-induced destabilization of thyroid follicular integrity and invasion of cells into extracellular matrix. Exp. Cell Res. 2014; 326 (2): 210–8.
  41. Toda S., Watanabe K., Yokoi F., Matsumura S., Suzuki K., Ootani A., Aoki S., Koike N., Sugihara H. A new organotypic culture of thyroid tissue maintains three-dimensional follicles with C cells for a long term. Biochem. Biophys. Res. Commun. 2002; 294 (4): 906–11.
  42. Toda S., Aoki S., Suzuki K., Koike E., Ootani A., Watanabe K., Koike N., Sugihara H. 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.
  43. Toda S., Ootani A., Aoki S., Sugihara H. Thyroid Tissue-Organotypic Culture Using a New Approach for Overcoming the Disadvantages of Conventional Organ Culture. Cell Biology (Third Edition). A Laboratory Handbook. 2006; 1: 411–4.
  44. Ness G., Bjerkvig R., Akslen L., Lillehaug J., Varhaug J. Primary organ-culture of nonneoplastic and neoplastic thyroid-tissue as multicellular spheroids. Int. J. Oncol. 1995; 6 (5): 1071–8.
  45. Taylor M.J., London N.J., Thirdborough S.M., Lake S.P., James R.F. The cryobiology of rat and human dendritic cells: preservation and destruction of membrane integrity by freezing. Cryobiology. 1990; 27 (3): 269–78.
  46. Iwata H., Ikada Y. Agarose Cell Encapsulation Technology and Therapeutics. Ed. by Kuhtreiber W., Lanza R., Chik W. Berlin: Birkhauser Boston, Basel. 1999; 97–108.