Skip to main content
Log in

New insights into the role and origin of pituitary S100β-positive cells

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

Abstract

In the anterior pituitary, S100β protein (S100β) has been assumed to be a marker of folliculo-stellate cells, which are one of the non-hormone-producing cells existing in the parenchyma of the adult anterior lobe and are composed of subpopulations with various functions. However, recent accumulating studies on S100β-positive cells, including non-folliculo-stellate cells lining the marginal cell layer (MCL), have shown the novel aspect that most S100β-positive cells in the MCL and parenchyma of the adult anterior lobe are positive for sex determining region Y-box 2 (SOX2), a marker of pituitary stem/progenitor cells. From the viewpoint of SOX2-positive cells, the majority of these cells in the MCL and in the parenchyma are positive for S100β, suggesting that S100β plays a role in the large population of stem/progenitor cells in the anterior lobe of the adult pituitary. Reportedly, S100β/SOX2-double positive cells are able to differentiate into hormone-producing cells and various types of non-hormone-producing cells. Intriguingly, it has been demonstrated that extra-pituitary lineage cells invade the pituitary gland during prenatal pituitary organogenesis. Among them, two S100β-positive populations have been identified: one is SOX2-positive population which invades at the late embryonic period through the pituitary stalk and another is a SOX2-negative population that invades at the middle embryonic period through Atwell’s recess. These two populations are likely the substantive origin of S100β-positive cells in the postnatal anterior pituitary, while S100β-positive cells emerging from oral ectoderm-derived cells remain unclear.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allaerts W, Vankelecom H (2005) History and perspectives of pituitary folliculo-stellate cell research. Eur J Endocrinol 153:1–12

    Article  CAS  PubMed  Google Scholar 

  • Andoniadou CL, Matsushima D, Mousavy Gharavy SN, Signore M, Mackintosh AI, Schaeffer M, Gaston-Massuet C, Mollard P, Jacques TS, Le Tissier P, Dattani MT, Pevny LH, Martinez-Barbera JP (2013) Sox2(+) stem/progenitor cells in the adult mouse pituitary support organ homeostasis and have tumor-inducing potential. Cell Stem Cell 13:433–445

    Article  CAS  PubMed  Google Scholar 

  • Aquino JB, Hjerling-Leffler J, Koltzenburg M, Edlund T, Villar MJ, Ernfors P (2006) In vitro and in vivo differentiation of boundary cap neural crest stem cells into mature Schwann cells. Exp Neurol 198:438–449

    Article  CAS  PubMed  Google Scholar 

  • Bragdon BC, Bahney CS (2018) Origin of reparative stem cells in fracture healing. Curr Osteoporos Rep 16:490–503

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Crabbe A, Van Duppen V, Vankelecom H (2006) The notch signaling system is present in the postnatal pituitary: marked expression and regulatory activity in the newly discovered side population. Mol Endocrinol 20:3293–3307

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Hersmus N, Van Duppen V, Caesens P, Denef C, Vankelecom H (2005) The adult pituitary contains a cell population displaying stem/progenitor cell and early embryonic characteristics. Endocrinology 146:3985–3998

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Maruyama D, Sugiyama M, Sakai T, Mogi C, Kato M, Kurotani R, Shirasawa N, Takaki A, Renner U, Kato Y, Inoue K (2000) Cytological characterization of a pituitary folliculo-stellate-like cell line, Tpit/F1, with special reference to adenosine triphosphate-mediated neural nitric oxide synthetase expression and nitric oxide secretion. Endocrinology 141:3603–3610

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Kato T, Higuchi M, Yoshida S, Yako H, Kanno N, Kato Y (2013) Coxsackievirus and adenovirus receptor-positive cells compose the putative stem/progenitor cell niches in the marginal cell layer and parenchyma of the rat anterior pituitary. Cell Tissue Res 354:823–836

    Article  CAS  PubMed  Google Scholar 

  • Cocchia D, Miani N (1980) Immunocytochemical localization of the brain-specific S-100 protein in the pituitary gland of adult rat. J Neurocytol 9:771–782

    Article  CAS  PubMed  Google Scholar 

  • Couly GF, Le Douarin NM (1985) Mapping of the early neural primordium in quail-chick chimeras. I. Developmental relationships between placodes, facial ectoderm, and prosencephalon. Dev Biol 110:422–439

    Article  CAS  PubMed  Google Scholar 

  • Couly GF, Le Douarin NM (1987) Mapping of the early neural primordium in quail-chick chimeras. II. The prosencephalic neural plate and neural folds: implications for the genesis of cephalic human congenital abnormalities. Dev Biol 120:198–214

    Article  CAS  PubMed  Google Scholar 

  • Daikoku S, Kawano H, Abe K, Yoshinaga K (1981) Topographical appearance of adenohypophysial cells with special reference to the development of the portal system. Arch Histol Jpn 44:103–116

    Article  CAS  PubMed  Google Scholar 

  • Davis FM, Stewart TA, Thompson EW, Monteith GR (2014) Targeting EMT in cancer: opportunities for pharmacological intervention. Trends Pharmacol Sci 35:479–488

    Article  CAS  PubMed  Google Scholar 

  • Davis SW, Mortensen AH, Keisler JL, Zacharias AL, Gage PJ, Yamamura K, Camper SA (2016) beta-catenin is required in the neural crest and mesencephalon for pituitary gland organogenesis. BMC Dev Biol 16:16

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Devnath S, Inoue K (2008) An insight to pituitary folliculo-stellate cells. J Neuroendocrinol 20:687–691

    Article  CAS  PubMed  Google Scholar 

  • Donato R, Sorci G, Riuzzi F, Arcuri C, Bianchi R, Brozzi F, Tubaro C, Giambanco I (2009) S100B’s double life: intracellular regulator and extracellular signal. Biochim Biophys Acta 1793:1008–1022

    Article  CAS  PubMed  Google Scholar 

  • Fauquier T, Rizzoti K, Dattani M, Lovell-Badge R, Robinson IC (2008) SOX2-expressing progenitor cells generate all of the major cell types in the adult mouse pituitary gland. Proc Natl Acad Sci USA 105:2907–2912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujiwara S, Hoshikawa S, Ueno T, Hirata M, Saito T, Ikeda T, Kawaguchi H, Nakamura K, Tanaka S, Ogata T (2014) SOX10 transactivates S100B to suppress Schwann cell proliferation and to promote myelination. PLoS One 9:e115400

  • Fujiwara K, Tsukada T, Horiguchi K, Fujiwara Y, Takemoto K, Nio-Kobayashi J, Ohno N, Inoue K (2020) Aldolase C is a novel molecular marker for folliculo-stellate cells in rodent pituitary. Cell Tissue Res 381:273–284

    Article  CAS  PubMed  Google Scholar 

  • Gleiberman AS, Michurina T, Encinas JM, Roig JL, Krasnov P, Balordi F, Fishell G, Rosenfeld MG, Enikolopov G (2008) Genetic approaches identify adult pituitary stem cells. Proc Natl Acad Sci USA 105:6332–6337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldsmith S, Lovell-Badge R, Rizzoti K (2016) SOX2 is sequentially required for progenitor proliferation and lineage specification in the developing pituitary. Development (cambridge, England) 143:2376–2388

    CAS  Google Scholar 

  • Gremeaux L, Fu Q, Chen J, Vankelecom H (2012) Activated phenotype of the pituitary stem/progenitor cell compartment during the early-postnatal maturation phase of the gland. Stem Cells Dev 21:801–813

    Article  CAS  PubMed  Google Scholar 

  • Higuchi M, Kanno N, Yoshida S, Ueharu H, Chen M, Yako H, Shibuya S, Sekita M, Tsuda M, Mitsuishi H, Kato T, Kato Y (2014) GFP-expressing S100β-positive cells of the rat anterior pituitary differentiate into hormone-producing cells. Cell Tissue Res 357:767–779

    Article  CAS  PubMed  Google Scholar 

  • Higuchi M, Yoshida S, Kanno N, Mitsuishi H, Ueharu H, Chen M, Nishimura N, Kato T, Kato Y (2017) Clump formation in mouse pituitary-derived non-endocrine cell line Tpit/F1 promotes differentiation into growth-hormone-producing cells. Cell Tissue Res 369:353–368

    Article  CAS  PubMed  Google Scholar 

  • Higuchi M, Yoshida S, Ueharu H, Chen M, Kato T, Kato Y (2015) PRRX1- and PRRX2-positive mesenchymal stem/progenitor cells are involved in vasculogenesis during rat embryonic pituitary development. Cell Tissue Res 361:557–565

    Article  CAS  PubMed  Google Scholar 

  • Horiguchi K, Fujiwara K, Yoshida S, Nakakura T, Arae K, Tsukada T, Hasegawa R, Takigami S, Ohsako S, Yashiro T, Kato T, Kato Y (2018) Isolation and characterisation of CD9-positive pituitary adult stem/progenitor cells in rats. Sci Rep 8:5533

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Horiguchi K, Yako H, Yoshida S, Fujiwara K, Tsukada T, Kanno N, Ueharu H, Nishihara H, Kato T, Yashiro T, Kato Y (2016) S100β-positive cells of mesenchymal origin reside in the anterior lobe of the embryonic pituitary gland. PLoS One 11:e0163981

  • Horiguchi K, Yoshida S, Tsukada T, Fujiwara K, Nakakura T, Hasegawa R, Takigami S, Ohsako S (2021) Cluster of differentiation (CD) 9-positive mouse pituitary cells are adult stem/progenitor cells. Histochem Cell Biol 155:391–404

    Article  CAS  PubMed  Google Scholar 

  • Itakura E, Odaira K, Yokoyama K, Osuna M, Hara T, Inoue K (2007) Generation of transgenic rats expressing green fluorescent protein in S-100beta-producing pituitary folliculo-stellate cells and brain astrocytes. Endocrinology 148:1518–1523

    Article  CAS  PubMed  Google Scholar 

  • Jayakody SA, Andoniadou CL, Gaston-Massuet C, Signore M, Cariboni A, Bouloux PM, Le Tissier P, Pevny LH, Dattani MT, Martinez-Barbera JP (2012) SOX2 regulates the hypothalamic-pituitary axis at multiple levels. J Clin Invest 122:3635–3646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelberman D, Rizzoti K, Lovell-Badge R, Robinson IC, Dattani MT (2009) Genetic regulation of pituitary gland development in human and mouse. Endocr Rev 30:790–829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kioussi C, Carriere C, Rosenfeld MG (1999) A model for the development of the hypothalamic-pituitary axis: transcribing the hypophysis. Mech Dev 81:23–35

    Article  CAS  PubMed  Google Scholar 

  • Kouki T, Imai H, Aoto K, Eto K, Shioda S, Kawamura K, Kikuyama S (2001) Developmental origin of the rat adenohypophysis prior to the formation of Rathke’s pouch. Development 128:959–963

    Article  CAS  PubMed  Google Scholar 

  • Langlais D, Couture C, Kmita M, Drouin J (2013) Adult pituitary cell maintenance: lineage-specific contribution of self-duplication. Mol Endocrinol 27:1103–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lepore DA, Jokubaitis VJ, Simmons PJ, Roeszler KN, Rossi R, Bauer K, Thomas PQ (2006) A role for angiotensin-converting enzyme in the characterization, enrichment, and proliferation potential of adult murine pituitary colony-forming cells. Stem Cells 24:2382–2390

    Article  CAS  PubMed  Google Scholar 

  • Lepore DA, Roeszler K, Wagner J, Ross SA, Bauer K, Thomas PQ (2005) Identification and enrichment of colony-forming cells from the adult murine pituitary. Exp Cell Res 308:166–176

    Article  CAS  PubMed  Google Scholar 

  • Lin H (2002) The stem-cell niche theory: lessons from flies. Nat Rev Genet 3:931–940

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto H, Ishibashi Y, Ohtaki T, Hasegawa Y, Koyama C, Inoue K (1993) Newly established murine pituitary folliculo-stellate-like cell line (TtT/GF) secretes potent pituitary glandular cell survival factors, one of which corresponds to metalloproteinase inhibitor. Biochem Biophys Res Commun 194:909–915

    Article  CAS  PubMed  Google Scholar 

  • Mogi C, Miyai S, Nishimura Y, Fukuro H, Yokoyama K, Takaki A, Inoue K (2004) Differentiation of skeletal muscle from pituitary folliculo-stellate cells and endocrine progenitor cells. Exp Cell Res 292:288–294

    Article  CAS  PubMed  Google Scholar 

  • Moore BW (1965) A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun 19:739–744

    Article  CAS  PubMed  Google Scholar 

  • Nakajima T, Yamaguchi H, Takahashi K (1980) S100 protein in folliculostellate cells of the rat pituitary anterior lobe. Brain Res 191:523–531

    Article  CAS  PubMed  Google Scholar 

  • Nitzan E, Krispin S, Pfaltzgraff ER, Klar A, Labosky PA, Kalcheim C (2013) A dynamic code of dorsal neural tube genes regulates the segregation between neurogenic and melanogenic neural crest cells. Development 140:2269–2279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nolan LA, Kavanagh E, Lightman SL, Levy A (1998) Anterior pituitary cell population control: basal cell turnover and the effects of adrenalectomy and dexamethasone treatment. J Neuroendocrinol 10:207–215

    Article  CAS  PubMed  Google Scholar 

  • Nolan LA, Lunness HR, Lightman SL, Levy A (1999) The effects of age and spontaneous adenoma formation on trophic activity in the rat pituitary gland: a comparison with trophic activity in the human pituitary and in human pituitary adenomas. J Neuroendocrinol 11:393–401

    Article  CAS  PubMed  Google Scholar 

  • O’Hara L, Christian HC, Jeffery N, Le Tissier P, Smith LB (2020) Characterisation of a mural cell network in the murine pituitary gland. J Neuroendocrinol 32:e12903

  • Osuna M, Sonobe Y, Itakura E, Devnath S, Kato T, Kato Y, Inoue K (2012) Differentiation capacity of native pituitary folliculostellate cells and brain astrocytes. J Endocrinol 213:231–237

    Article  CAS  PubMed  Google Scholar 

  • Perera SN, Kerosuo L (2021) On the road again: establishment and maintenance of stemness in the neural crest from embryo to adulthood. Stem Cells 39:7–25

    Article  PubMed  Google Scholar 

  • Perez Millan MI, Brinkmeier ML, Mortensen AH, Camper SA (2016) PROP1 triggers epithelial-mesenchymal transition-like process in pituitary stem cells. Elife 5:e14470

  • Pierret C, Spears K, Maruniak JA, Kirk MD (2006) Neural crest as the source of adult stem cells. Stem Cells Dev 15:286–291

    Article  CAS  PubMed  Google Scholar 

  • Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707–1710

    Article  CAS  PubMed  Google Scholar 

  • Rizzoti K (2015) Genetic regulation of murine pituitary development. J Mol Endocrinol 54:R55-73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizzoti K, Akiyama H, Lovell-Badge R (2013) Mobilized adult pituitary stem cells contribute to endocrine regeneration in response to physiological demand. Cell Stem Cell 13:419–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rizzoti K, Lovell-Badge R (2017) Pivotal role of median eminence tanycytes for hypothalamic function and neurogenesis. Mol Cell Endocrinol 445:7–13

    Article  CAS  PubMed  Google Scholar 

  • Roose H, Cox B, Boretto M, Gysemans C, Vennekens A, Vankelecom H (2017) Major depletion of SOX2(+) stem cells in the adult pituitary is not restored which does not affect hormonal cell homeostasis and remodelling. Sci Rep 7:16940

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sheng HZ, Moriyama K, Yamashita T, Li H, Potter SS, Mahon KA, Westphal H (1997) Multistep control of pituitary organogenesis. Science 278:1809–1812

    Article  CAS  PubMed  Google Scholar 

  • Shirasawa N, Kihara H, Yamaguchi S, Yoshimura F (1983) Pituitary folliculo-stellate cells immunostained with S-100 protein antiserum in postnatal, castrated and thyroidectomized rats. Cell Tissue Res 231:235–249

    Article  CAS  PubMed  Google Scholar 

  • Simoes-Costa M, Bronner ME (2015) Establishing neural crest identity: a gene regulatory recipe. Development 142:242–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sornson MW, Wu W, Dasen JS, Flynn SE, Norman DJ, O’Connell SM, Gukovsky I, Carriere C, Ryan AK, Miller AP, Zuo L, Gleiberman AS, Andersen B, Beamer WG, Rosenfeld MG (1996) Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature 384:327–333

    Article  CAS  PubMed  Google Scholar 

  • Tremblay JJ, Lanctot C, Drouin J (1998) The pan-pituitary activator of transcription, Ptx1 (pituitary homeobox 1), acts in synergy with SF-1 and Pit-1 and is an upstream regulator of the Lim-homeodomain gene Lim3/Lhx3. Mol Endocrinol 12:428–441

    Article  CAS  PubMed  Google Scholar 

  • Tsukada T, Isowa Y, Kito K, Yoshida S, Toneri S, Horiguchi K, Fujiwara K, Yashiro T, Kato T, Kato Y (2019) Identification of TGFβ-induced proteins in non-endocrine mouse pituitary cell line TtT/GF by SILAC-assisted quantitative mass spectrometry. Cell Tissue Res 376:281–293

    Article  CAS  PubMed  Google Scholar 

  • Tsukada T, Yoshida S, Kito K, Fujiwara K, Yako H, Horiguchi K, Isowa Y, Yashiro T, Kato T, Kato Y (2017) TGFbeta signaling reinforces pericyte properties of the non-endocrine mouse pituitary cell line TtT/GF. Cell Tissue Res 371:339–350

    Article  PubMed  CAS  Google Scholar 

  • Ueharu H, Yoshida S, Kanno N, Horiguchi K, Nishimura N, Kato T, Kato Y (2018) SOX10-positive cells emerge in the rat pituitary gland during late embryogenesis and start to express S100beta. Cell Tissue Res 372:77–90

    Article  CAS  PubMed  Google Scholar 

  • Ueharu H, Yoshida S, Kikkawa T, Kanno N, Higuchi M, Kato T, Osumi N, Kato Y (2017) Gene tracing analysis reveals the contribution of neural crest-derived cells in pituitary development. J Anat 230:373–380

    Article  CAS  PubMed  Google Scholar 

  • Vankelecom H (2007a) Non-hormonal cell types in the pituitary candidating for stem cell. Semin Cell Dev Biol 18:559–570

    Article  CAS  PubMed  Google Scholar 

  • Vankelecom H (2007b) Stem cells in the postnatal pituitary? Neuroendocrinology 85:110–130

    Article  CAS  PubMed  Google Scholar 

  • Vankelecom H (2012) Pituitary stem cells drop their mask. Curr Stem Cell Res Ther 7:36–71

    Article  CAS  PubMed  Google Scholar 

  • Vankelecom H, Chen J (2014) Pituitary stem cells: where do we stand? Mol Cell Endocrinol 385:2–17

    Article  CAS  PubMed  Google Scholar 

  • Vankelecom H, Gremeaux L (2010) Stem cells in the pituitary gland: a burgeoning field. Gen Comp Endocrinol 166:478–488

    Article  CAS  PubMed  Google Scholar 

  • Vega-Lopez GA, Cerrizuela S, Tribulo C, Aybar MJ (2018) Neurocristopathies: new insights 150 years after the neural crest discovery. Dev Biol 444(Suppl 1):S110–S143

    Article  CAS  PubMed  Google Scholar 

  • Vila-Porcile E (1972) The network of the folliculo-stellate cells and the follicles of the adenohypophysis in the rat (pars distalis). Z Zellforsch Mikrosk Anat 129:328–369

    Article  CAS  PubMed  Google Scholar 

  • Vives V, Alonso G, Solal AC, Joubert D, Legraverend C (2003) Visualization of S100B-positive neurons and glia in the central nervous system of EGFP transgenic mice. J Comp Neurol 457:404–419

    Article  CAS  PubMed  Google Scholar 

  • Wei XY, Zhao CH, Liu YY, Wang YZ, Ju G (2009) Immuohistochemical markers for pituicyte. Neurosci Lett 465:27–30

    Article  CAS  PubMed  Google Scholar 

  • Yamashita M, Qian ZR, Sano T, Horvath E, Kovacs K (2005) Immunohistochemical study on so-called follicular cells and folliculostellate cells in the human adenohypophysis. Pathol Int 55:244–247

  • Yang L-N, Huang W-K, Li X-L, Bai Y-Z, Zhang S-C (2020) Sox10 is a specific biomarker for neural crest stem cells in immunohistochemical staining in Wistar rats. Dis Markers 2020:8893703

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Higuchi M, Ueharu H, Nishimura N, Tsuda M, Nishihara H, Mitsuishi H, Kato T, Kato Y (2014) Characterization of murine pituitary-derived cell lines Tpit/F1, Tpit/E and TtT/GF. J Reprod Dev 60:295–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Kato T, Chen M, Higuchi M, Ueharu H, Nishimura N, Kato Y (2015) Localization of juxtacrine factor ephrin-B2 in pituitary stem/progenitor cell niches throughout life. Cell Tissue Res 359:755–766

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Kato T, Higuchi M, Yako H, Chen M, Kanno N, Ueharu H, Kato Y (2013) Rapid transition of NESTIN-expressing dividing cells from PROP1-positive to PIT1-positive advances prenatal pituitary development. J Neuroendocrinol 25:779–791

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Kato T, Kanno N, Nishimura N, Nishihara H, Horiguchi K, Kato Y (2017) Cell type-specific localization of Ephs pairing with ephrin-B2 in the rat postnatal pituitary gland. Cell Tissue Res 370:99–112

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Kato T, Kato Y (2016a) EMT Involved in migration of stem/progenitor cells for pituitary development and regeneration. J Clin Med 5:43

    Article  PubMed Central  CAS  Google Scholar 

  • Yoshida S, Kato T, Yako H, Susa T, Cai LY, Osuna M, Inoue K, Kato Y (2011) Significant quantitative and qualitative transition in pituitary stem/progenitor cells occurs during the postnatal development of the rat anterior pituitary. J Neuroendocrinol 23:933–943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Nishimura N, Ueharu H, Kanno N, Higuchi M, Horiguchi K, Kato T, Kato Y (2016b) Isolation of adult pituitary stem/progenitor cell clusters located in the parenchyma of the rat anterior lobe. Stem Cell Res 17:318–329

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Nishimura N, Yurino H, Kobayashi M, Horiguchi K, Yano K, Hashimoto S, Kato T, Kato Y (2018) Differentiation capacities of PS-clusters, adult pituitary stem/progenitor cell clusters located in the parenchymal-niche, of the rat anterior lobe. PLoS One 13:e0196029

  • Yoshimura F, Soji T, Kiguchi Y (1977a) Relationship between the follicular cells and marginal layer cells of the anterior pituitary. Endocr J 24:301–305

    Article  CAS  Google Scholar 

  • Yoshimura F, Soji T, Sato S, Yokoyama M (1977b) Development and differentiation of rat pituitary follicular cells under normal and some experimental conditions with special reference to an interpretation of renewal cell system. Endocr J 24:435–449

    Article  CAS  Google Scholar 

  • Zhang D, Ighaniyan S, Stathopoulos L, Rollo B, Landman K, Hutson J, Newgreen D (2014) The neural crest: a versatile organ system. Birth Defects Res C Embryo Today 102:275–298

    Article  PubMed  CAS  Google Scholar 

  • Zhu X, Gleiberman AS, Rosenfeld MG (2007) Molecular physiology of pituitary development: signaling and transcriptional networks. Physiol Rev 87:933–963

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, Zhang J, Tollkuhn J, Ohsawa R, Bresnick EH, Guillemot F, Kageyama R, Rosenfeld MG (2006) Sustained Notch signaling in progenitors is required for sequential emergence of distinct cell lineages during organogenesis. Genes Dev 20:2739–2753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yukio Kato.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

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

Kato, Y., Yoshida, S. & Kato, T. New insights into the role and origin of pituitary S100β-positive cells. Cell Tissue Res 386, 227–237 (2021). https://doi.org/10.1007/s00441-021-03523-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-021-03523-7

Keywords

Navigation