Skip to main content

Advertisement

SpringerLink
Log in

Follicular cell lineage in persistent ultimobranchial remnants of mammals

  • Review
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

It has been a subject of much debate whether thyroid follicular cells originate from the ultimobranchial body, in addition to median thyroid primordium. Ultimobranchial remnants are detected in normal dogs, rats, mice, cattle, bison and humans and also in mutant mice such as Eya1 homozygotes, Hox3 paralogs homozygotes, Nkx2.1 heterozygotes and FRS2α2F/2F. Besides C cells, follicular cell lineages immunoreactive for thyroglobulin are located within these ultimobranchial remnants. In dogs, the C cell complexes, i.e., large cell clusters consisting of C cells and undifferentiated cells, are present together with parathyroid IV and thymus IV in or close to the thyroid lobe. In addition, follicular cells in various stages of differentiation, including follicular cell groups and primitive and minute follicles storing colloid, are intermingled with C cells in some complexes. This review elaborates the transcription factors and signaling molecules involved in folliculogenesis and it is supposed why the follicular cells in the ultimobranchial remnants are sustained in immature stages. Pax8, a transcription factor crucial for the development of follicular cells, is expressed in the fourth pharyngeal pouch and the ultimobranchial body in human embryos. Pax8 expression is also detected in the ultimobranchial remnants of Eya1 and Hes1 null mutant mice. To determine whether the C cells and follicular cells in the ultimobranchial remnants consist of dual lineage cells or are derived from the common precursor, the changes of undifferentiated cells in dog C cell complexes are examined after chronically induced hypercalcemia or antithyroid drug treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andersson L, Westerlund J, Liang S, Carlsson T, Amendola E, Fagman H, Nilsson M (2011) Role of EphA4 receptor signaling in thyroid development: regulation of folliculogenesis and propagation of the C-cell lineage. Endocrinology 152:1154–1164

    Article  CAS  PubMed  Google Scholar 

  • Antonica F, Kasprzyk DF, Opitz R, Lacovino M, Liao XH, Dumitrescu AM, Refetoff S, Peremans K, Manto M, Kyba M, Costagliola S (2012) Generation of functional thyroid from embryonic stem cells. Nature 491:66–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Autelitano F, Santeusanio G, Tondo UD, Costantino M, Renda F, Autelitano M (1987) Immunohistochemical study of solid cell nests of the thyroid gland found from an autopsy study. Cancer 59:477–483

    Article  CAS  PubMed  Google Scholar 

  • Bignami A, Raju T, Dahl D (1982) Localization of vimentin, the nonspecific intermediate filament protein, in embryonal glia and in early differentiation neurons: in vivo and in vitro immunofluorescence study of the rat embryo with vimentin and neurofilament antisera. Dev Biol 91:286–295

    Article  CAS  PubMed  Google Scholar 

  • Burstein DE, Nagi C, Wang BY, Unger P (2004) 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 35:465–473

    Article  CAS  PubMed  Google Scholar 

  • Calvert R (1972) Electron microscopic observations on the contribution of the ultimobranchial bodies to thyroid histogenesis in the rat. Am J Anat 133:269–290

    Article  CAS  PubMed  Google Scholar 

  • Cameselle-Teijeiro J, Varela-Durán J, Sambade C, Villanueva JP, Varela-Núnez R, Sobriho-Simoes M (1994) Solid cell nests of the thyroid: light microscopy and immunohisochemical profile. Hum Pathol 25:684–693

    Article  CAS  PubMed  Google Scholar 

  • Carre A, Rachdi L, Tron E, Richard B, Castanet M et al (2011) Hes1 is required for appropriate morphogenesis and differentiation during mouse thyroid gland development. PLoS One 6:e16752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castro-Munozledo F, Meza-Aguilar DG, Dominguez-Castillo R, Hernández-Zequinely V, Sánchez-Guzimán E (2017) Vimentin as a marker of early differentiating, highly motile corneal epithelial cells. J Cell Physiol 232:818–830

    Article  CAS  PubMed  Google Scholar 

  • Chisaka O, Kameda Y (2005) Hoxa3 regulates the proliferation and differentiation of the third pharyngeal arch mesenchyme in mice. Cell Tissue Res 320:77–89

    Article  CAS  PubMed  Google Scholar 

  • Colin IM, Denef JF, Lengelé B, Many MC, Gérard AC (2013) Recent insights into the cell biology of thyroid angiofollicular units. Endocr Rev 34:209–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conde E, Moreno AM, Martin-Lacave I, Galera AFH (1992) Immunocytochemical study of the ultimobranchial tubule in Wistar rats. Anat Histol Embryol 21:94–100

    Article  CAS  PubMed  Google Scholar 

  • De Felice M, Di Lauro R (2004) Thyroid development and its disorders: genetics and molecular mechanisms. Endocr Rev 25:722–746

    Article  CAS  PubMed  Google Scholar 

  • De Felice M, Di Lauro R (2011) Minireview: intrinsic and extrinsic factors in thyroid gland development: an update. Endocrinology 152:2948–2956

    Article  CAS  PubMed  Google Scholar 

  • Fagman H, Grӓnde M, Gritli-Linde A, Nilsson M (2004) Genetic deletion of Sonic hedgehog causes hemiagenesis and ectopic development of the thyroid in mouse. Am J Pathol 164:1865–1872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fagman H, Andersson L, Nilsson M (2006) The developing mouse thyroid: embryonic vessel contacts and parenchymal growth pattern during specification, budding, migration, and lobulation. Dev Dyn 235:444–455

    Article  CAS  PubMed  Google Scholar 

  • Frezzetti D, Reale C, Cali G, Nitsch L, Fagman H, Nilsson O, Scarfò M, De Vita G, Di Lauro R (2011) The microRNA-processing enzyme Dicer is essential for thyroid function. PLoS One 6:e27648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenburg G, Hay ED (1988) Cytoskeleton and thyroglobulin expression change during transformation of thyroid epithelium to mesenchyme-like cells. Development 102:605–622

    CAS  PubMed  Google Scholar 

  • Hadari YR, Gotoh N, Kouhara H, Lax I, Schlessinger J (2001) Critical role for the docking-protein FRS2α in FGF receptor-mediated signal transduction pathways. Proc Natl Acad Sci U S A 98:8578–8583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hales M, Rosenau W, Okerlund MD, Galante M (1982) Carcinoma of the thyroid with a mixed medullary and follicular pattern: morphologic, immunohistochemical, and clinical laboratory studies. Cancer 50:1352–1359

    Article  CAS  PubMed  Google Scholar 

  • Harach HR (1985) Solid cell nests of the thyroid. An anatomical survey and immunohistochemical study for the presence of thyroglobulin. Acta Anat 122:249–253

    Article  CAS  PubMed  Google Scholar 

  • Harach HR (1988) Solid cell nests of the thyroid. J Pathol 155:191–200

    Article  CAS  PubMed  Google Scholar 

  • Harmon BG, Kelley LC (2001) Immunohistochemistry of ultimobranchial thyroid carcinomas in seven slaughtered cows and one bull. J Vet Diagn Investig 13:101–105

    Article  CAS  Google Scholar 

  • Hick AC, Delmarcelle AS, Bouquet M, Klotz S, Copetti T et al (2013) Reciprocal epithelial:endothelial paracrine interactions during thyroid development govern follicular organization and C-cells differentiation. Dev Biol 381:227–240

    Article  CAS  PubMed  Google Scholar 

  • Jacobs JW, Lund PK, Potts JT Jr, Bell NH, Habener JF (1981) Procalcitonin is a glycoprotein. J Biol Chem 256:2803–2807

    CAS  PubMed  Google Scholar 

  • Janzer RC, Weber E, Hedinger C (1979) The relation between solid cell nests and C cells of the thyroid gland: an immunohistochemical and morphometric investigation. Cell Tissue Res 197:295–312

    Article  CAS  PubMed  Google Scholar 

  • Johansson E, Andersson L, Ornros J, Carlsson T, Ingeson-Carlsson C et al (2015) Revising the embryonic origin of thyroid C cells. Development 142:3519–3528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnston D, Hatzis D, Sunday ME (1998) Expression of v-Ha-ras driven by the calcitonin/calcitonin gene-related peptide promotor: a novel transgenic murine model for medullary thyroid carcinoma. Oncogene 16:167–177

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1970) Increased mitotic activity of the parafollicular cells of the dog thyroid in experimentally induced hypercalcemia. Arch Histol Jpn 32:179–192

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1971) The occurrence of a special parafollicular cell complex in and beside the dog thyroid gland. Arch Histol Jpn 33:115–132

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1973) Electron microscopic studies on the parafollicular cells and parafollicular cell complexes in the dog. Arch Histol Jpn 36:89–105

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1974a) Light and electron microscopic alterations of the dog parafollicular cells induced by antithyroid drug. Arch Histol Jpn 36:205–220

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1974b) Relationship between the thyroid parafollicular cells and pituitary gland. Arch Histol Jpn 37:225–244

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1977) Electron microscopical and immunohistochemical study on parafollicular cell complex with reference to parafollicular cell as a paraneuron. Arch Histol Jpn 40(suppl):133–145

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1982a) The cysts in C cell complexes of dog thyroids studied by immunoperoxidase staining and autoradiography. Arch Histol Jpn 45:437–448

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1982b) Degranulation and appearance of vesicular inclusions in canine C cells after administration of antithyroid drug. Cell Tissue Res 225:315–318

    CAS  PubMed  Google Scholar 

  • Kameda Y (1983) Distribution of C cells in monkey thyroid glands as studied by the immunoperoxidase method using anti-calcitonin and anti-C-thyroglobulin antisera. Arch Histol Jpn 46:221–228

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1984) Dog thyroid glands after chronic administration of antithyroid drugs. Am J Pathol 117:316–325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kameda Y (1987) Immunohistochemical demonstration of keratins in the cysts of thyroid glands, parathyroid glands, and C-cell complexes of the dog. Amer J Anat 180:87–99

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1995a) Evidence to support the distal vagal ganglion as the origin of C cells of the ultimobranchial gland in the chick. J Comp Neurol 359:1–14

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1995b) Co-expression of vimentin and 19S-thyroglobulin in follicular cells located in the C-cell complex of dog thyroid gland. J Histochem Cytochem 43:1097–1106

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (1996) Differential distribution of S-100 protein and vimentin in the hypophyseal pars tuberalis of the guinea pig. J Histochem Cytochem 44:501–510

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (2016) Cellular and molecular events on the development of mammalian thyroid C cells. Dev Dyn 245:323–341

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y (2017) Morphological and molecular evolution of the ultimobranchial gland of nonmammalian vertebrates, with special reference to the chicken C cells. Dev Dyn 246:719–739

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y, Ikeda A (1980a) Immunohistochemical study of the C-cell complex of dog thyroid glands with reference to the reactions of calcitonin, C-thyroglobulin and 19S thyroglobulin. Cell Tissue Res 208:405–415

    CAS  PubMed  Google Scholar 

  • Kameda Y, Ikeda A (1980b) Immunohistochemical study of C-cell complexes in dogs after induced hypercalcemica, antithyroid drug treatment and hypophysectomy. Cell Tissue Res 208:417–432

    CAS  PubMed  Google Scholar 

  • Kameda Y, Shigemoto H, Ikeda A (1980) Development and cytodifferentiation of C cell complexes in dog fetal thyroid. Cell Tissue Res 206:403–415

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y, Ikeda K, Ikeda A (1981) Uptake of radioiodine in follicles of dog C-cell complexes studied by autoradiograph and immunoperoxidase staining. Anat Rec 200:461–470

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y, Nishimaki T, Chisaka O, Iseki S, Sucov HM (2007a) Expression of the epithelial marker E-cadherin by thyroid C cells and their precursors during murine development. J Histochem Cytochem 55:1075–1088

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y, Nishimaki T, Miura M, Jiang SX, Guillemot F (2007b) Mash1 regulates the development of C cells in mouse thyroid glands. Dev Dyn 236:262–270

    Article  CAS  PubMed  Google Scholar 

  • Kameda Y, Ito M, Nishimaki T, Gotoh N (2009) FRS2α is required for the separation, migration, and survival of pharyngeal-endoderm derived organs including thyroid, ultimobranchial body, parathyroid, and thymus. Dev Dyn 238:503–513

    Article  PubMed  Google Scholar 

  • Kameda Y, Saitoh T, Nemoto N, Katoh T, Iseki S, Fujimura T (2013) Hes1 is required for the development of pharyngeal organs and survival of neural crest-derived mesenchymal cells in pharyngeal arches. Cell Tissue Res 353:9–25

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Hara Y, Pineau T, Fernandez-Salguero P, Fox CH, Ward JM, Gonzalez FJ (1996) The T/ebp null mouse: thyroid-specific enhancer-binding protein is essential for the organogenesis of the thyroid, lung, ventral forebrain, and pituitary. Genes Dev 10:60–69

    Article  CAS  PubMed  Google Scholar 

  • Koster MI, Roop DR (2004) The role of p63 in development and differentiation of the epidermis. J Dermatol Sci 34:3–9

    Article  CAS  PubMed  Google Scholar 

  • Koumarianou P, Goméz-López G, Santisteban P (2017) Pax8 controls thyroid follicular polarity through cadherin-16. J Cell Sci 130:219–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusakabe T, Hoshi N, Kimura S (2006a) Origin of the ultimobranchial body cyst: T/ebp/Nkx2.1 expression is required for development and fusion of the ultimobranchial body to the thyroid. Dev Dyn 235:1300–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusakabe T, Kawaguchi A, Hoshi N, Kawaguchi R, Hoshi S, Kimura S (2006b) Thyroid-specific enhancer-binding protein/NKX2.1 is required for the maintenance of ordered architecture and function of the differentiated thyroid. Mol Endocrinol 20:1796–1809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane EB, Hogan BL, Kurkinen M, Garrels JI (1983) Co-expression of vimentin and cytokeratins in parietal endodermal cells of early mouse embryo. Nature 303:701–704

    Article  CAS  PubMed  Google Scholar 

  • Lazzaro D, Price M, De Felice M, Di Lauro R (1991) The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development 113:1093–1104

    CAS  PubMed  Google Scholar 

  • Le Douarin N, Fontaine J, Le Lièvre C (1974) New studies on the neural crest origin of the avian ultimobranchial glandular cells—interspecific combinations and cytochemical characterization of C cells based on the uptake of biogenic amine precursors. Histochemistry 38:297–305

    Article  PubMed  Google Scholar 

  • Le Lièvre CS, Le Douarin NM (1975) Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos. J Embryol Exp Morph 34:125–154

    PubMed  Google Scholar 

  • Liang S, Johansson E, Barila G, Altschuler DL, Fagman H, Nilsson M (2018) A branching morphogenesis program governs embryonic growth of the thyroid gland. Development 145:dev146829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ljungberg O, Nilsson PO (1985) Hyperplastic and neoplastic changes in ultimobranchial remnants and in parafollicular (C) cells in bulls: a histologic and immunohistochemical study. Vet Pathol 22:95–103

    Article  CAS  PubMed  Google Scholar 

  • Ljungberg O, Ericsson UB, Bondeson L, Thorell J (1983) A compound follicular-parafollicular cell carcinoma of the thyroid: a new tumor entity? Cancer 52:1053–1061

    Article  CAS  PubMed  Google Scholar 

  • Macias MJ, Martin-Malpartida P, Massagué J (2015) Structural determinants of SMAD function in TGF-β signaling. Trends Biochem Sci 40:296–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manley NR, Capecchi MR (1995) The role of Hoxa-3 in mouse thymus and thyroid development. Development 121:1989–2003

    CAS  PubMed  Google Scholar 

  • Manley NR, Capecchi MR (1998) Hox group3 paralogs regulate the development and migration of the thymus, thyroid, and parathyroid glands. Dev Biol 195:1–15

    Article  CAS  PubMed  Google Scholar 

  • Mansouri A, Chowdhury K, Gruss P (1998) Follicular cells of the thyroid gland require Pax8 gene function. Nature Genet 19:87–90

    Article  CAS  PubMed  Google Scholar 

  • Martin-Lacave I, Borrero MJ, Utrilla JC, Fernández-Santos JM, de Miguel M, Morillo J, Guerrero JM, Garcia-Marin R, Conde E (2009) C cells evolve at the same rhythm as follicular cells when thyroidal status changes in rats. J Anat 214:301–309

    Article  PubMed  PubMed Central  Google Scholar 

  • Matias-Guiu X (1999) Mixed medullary and follicular carcinoma of the thyroid. Am J Pathol 155:1413–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizukami Y, Nonomura A, Michigishi T, Noguchi M, Hashimoto T, Nakamura S, Ishizaki T (1994) Solid cell nests of the thyroid; a histologic and immunohistochemical study. Am J Clin Pathol 101:186–191

    Article  CAS  PubMed  Google Scholar 

  • Morillo-Bernal J, Fernández-Santos JM, Utrilla JC, de Miguel M, Garcia-Marin R, Martin-Lacave I (2009) Functional expression of the thyrotropin receptor in C cells: new insights into their involvement in the hypothalamic-pituitary-thyroid axis. J Anat 215:150–158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson M, Fagman H (2017) Development of the thyroid gland. Development 144:2123–2140

    Article  CAS  PubMed  Google Scholar 

  • Nilsson M, Williams D (2016) On the origin of cells and derivation of thyroid cancer: C cell story revisited. Eur Thyroid J 5:79–93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noel M, Delehaye MC, Segond N, Lasmoles F, Caillou B, Gardet P, Fragu P, Moukhtar MS (1991) Study of calcitonin and thyroglobulin gene expression in human mixed follicular and medullary thyroid carcinoma. Thyroid 1:249–256

    Article  CAS  PubMed  Google Scholar 

  • Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000) FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277:643–649

    Article  CAS  PubMed  Google Scholar 

  • Ozaki T, Nagashimma K, Kusakabe T, Kakudo K, Kimura S (2011) Development of thyroid gland and ultimobranchial body cyst in independent of p63. Lab Investig 91:138–146

    Article  CAS  PubMed  Google Scholar 

  • Pagan R, Martin I, Alonso A, Llobera M, Vilaró S (1996) Vimentin filaments follow the preexisting cytokeratin network during epithelial-mesenchymal transition of cultured neonatal rat hepatocytes. Exp Cell Res 222:333–344

    Article  CAS  PubMed  Google Scholar 

  • Papotti M, Negro F, Carney JA, Bussolati G, Lloyd RV (1997) Mixed medullary-follicular carcinoma of the thyroid. A morphological, immunohistochemical and in situ hybridization analysis of 11 cases. Virchows Arch 430:397–405

    Article  CAS  PubMed  Google Scholar 

  • Parlato R, Rosica A, Rodriguez-Mallon A, Affuso A, Postiglione MP, Arra C, Mansouri A, Kimura S, Di Lauro R, De Felice M (2004) An integrated regulatory network controlling survival and migration in thyroid organogenesis. Dev Biol 276:464–475

    Article  CAS  PubMed  Google Scholar 

  • Pasca di Magliano M, Di Lauro R, Zannini M (2000) Pax8 has a key role in thyroid cell differentiation. Proc Natl Acad Sci U S A 97:13144–13149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng TC, Cooper CW, Petrusz P, Volpert EM (1975) Identification of C-cells in normal and goitrous rat thyroid tissues using antiserum to rat thyrocalcitonin and the immunoperoxidase bridge technique. Endocrinology 97:1537–1544

    Article  CAS  PubMed  Google Scholar 

  • Pfaltz M, Hedinger CE, Mühlethaler JP (1983) Mixed medullary and follicular carcinoma of the thyroid. Virch Arch A Pathol Anat Histopathol 400:53–59

    Article  CAS  Google Scholar 

  • Preto A, Cameselle-Teijeiro J, Moldes-Boullosa J, Soares P, Cameselle-Teijeiro JF et al (2004) Telomerase expression and proliferative activity suggest a stem cell role for thyroid solid cell nests. Mod Pathol 17:819–826

    Article  CAS  PubMed  Google Scholar 

  • Reis-Filho JS, Preto A, Soares P, Ricardo S, Cameselle-Teijeiro J, Sobrinho-Simoes M (2003) P63 expression in solid cell nests of the thyroid: further evidence for a stem cell origin. Mod Pathol 16:43–48

    Article  PubMed  Google Scholar 

  • Reynolds L, Jones K, Winton DJ, Cranston A, Houghton C, Howard L, Ponder BAJ, Smith DP (2001) C-cell and thyroid epithelial tumours and altered follicular development in transgenic mice expressing the long isoform of Men 2A RET. Oncogene 20:3986–3994

    Article  CAS  PubMed  Google Scholar 

  • Rios Moreno MJ, Galera-Ruiz H, De Miguel M, López MIC, Illanes M, Galera-Davidson H (2011) Immunohistochemical profile of solid cell nest of thyroid gland. Endocr Pathol 22:35–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez W, Jin L, Janssens V, Pierreux C, Hick AC, Urizar E, Costagliola S (2012) Deletion of the RNaseIII enzyme Dicer in thyroid follicular cells causes hypothyroidism with signs of neoplastic alterations. PLoS One 7:e29929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sawicki B, Zabel M (1997) Immunocytochemical study of parafollicular cells of the thyroid and ultimobranchial remnants of the European bison. Acta Histochem 99:223–230

    Article  CAS  PubMed  Google Scholar 

  • Schmid KW (2015) Histopathology of C cells and medullary thyroid carcinoma. Recent Results Cancer Rec 204:41–60

    Article  Google Scholar 

  • Senoo M, Pinto F, Crum CP, McKeon F (2007) p63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129:523–536

    Article  CAS  PubMed  Google Scholar 

  • Silberschmidt D, Rodriguez-Mallon A, Mithboakar P, Cali G, Amendola E et al (2011) In vivo role of different domains and of phosphorylation in the transcription factor Nkx2-1. BMC Dev Biol 11:9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teshima TH, Lourenco SV, Tucker AS (2016) Multiple cranial organ defects after conditionally knocking out Fgf10 in the neural crest. Front Physiol 7:488

    Article  PubMed  PubMed Central  Google Scholar 

  • Trueba SS, Augé J, Mattei G, Etchevers H, Martinovic J, Czernichow P, Vekemans M, Polak M, Attie-Bitach (2005) PAX8, TITF1, and FOXE1 gene expression patterns during human development: new insights into human thyroid development and thyroid dysgenesis-associated malformations. J Clin Endocrinol Metab 90:455–462

    Article  CAS  PubMed  Google Scholar 

  • Vázquez-Román V, Utrilla JC, Fernández-Santos JM, Martin-Lacave I (2017) Immunohistochemical profiling of the ultimobranchial remnants in the rat postnatal thyroid gland. J Morphol 278:1114–1124

    Article  CAS  PubMed  Google Scholar 

  • Velez-delValle C, Marsch-Moreno M, Castro-Munozledo, Galván-Mendoza IJ, Kuri-Harcuch W (2016) Epithelial cell migration requires the interaction between the vimentin and keratin intermediate filaments. Sci Rep 6:24389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Villacorte M, Delmarcelle AS, Lernoux M, Bouquet M et al (2016) Thyroid follicle development requires Smad1/5- and endothelial cell-dependent basement membrane assembly. Development 143:1958–1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volante M, Papotti M, Roth J, Saremaslani P, Speel EJM, Lloyd RV, Carney JA, Heitz PU, Bussolati G, Komminoth P (1999) Mixed medullary-follicular thyroid carcinoma. Am J Pathol 155:1499–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westerlund J, Andersson L, Carlsson T, Fagman H, Nilsson M (2013) Misguided migration of C cell precursors to extra-thyroidal locations related to defective pharyngeal pouch development in Shh deficient mice. Cell Dev Biol 2(issue 4):1000129

    Google Scholar 

  • Williams ED, Toyn CE, Harach R (1989) The ultimobranchial gland and congenital thyroid abnormalities in man. J Pathol 159:135–141

    Article  CAS  PubMed  Google Scholar 

  • Wollman SH, Hilfer R (1977) Embryologic origin of various epithelial cell types in the thyroid gland of the rat. Anat Rec 189:467–478

    Article  CAS  PubMed  Google Scholar 

  • Wollman SH, Hilfer R (1978) Embryologic origin of the various epithelial cell types in the second kind of thyroid follicle in the C3H mouse. Anat Rec 191:111–122

    Article  CAS  PubMed  Google Scholar 

  • Wollman SH, Nève P (1971a) Postnatal development and properties of ultimobranchial follicles in the rat thyroid. Anat Rec 171:247–258

    Article  CAS  PubMed  Google Scholar 

  • Wollman SH, Nève P (1971b) Ultimobranchial follicles in the thyroid glands of rats and mice. Recent Progr Horm Res 27:213–234

    CAS  PubMed  Google Scholar 

  • Xu PX, Zheng W, Laclef C, Maire P, Maas RL, Peters H, Xu X (2002) Eya1 is required for the morphogenesis of mammalian thymus, parathyroid and thyroid. Development 129:3033–3044

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang A, Schweitzer R, Sun D, Kaghad M, Walker N et al (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398:714–718

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy, Kitasato University School of Medicine, Sagamihara, Kanagawa, 252-0374, Japan

    Yoko Kameda

Authors
  1. Yoko Kameda
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoko Kameda.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kameda, Y. Follicular cell lineage in persistent ultimobranchial remnants of mammals. Cell Tissue Res 376, 1–18 (2019). https://doi.org/10.1007/s00441-018-02982-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-018-02982-9

Keywords

Search

Navigation