Pituitary stem /progenitor cells: Embryonic players in the adult gland?

European Journal of Neuroscience

Volumn 32, Issue 12, 2010, Pages 2063-2081

  Vankelecom, Hugo ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Epithelial mesenchymal transition; Pituitary stem cell model; Side population; Sox2

Indexed keywords

ALDEHYDE DEHYDROGENASE; BETA CATENIN; BMI1 PROTEIN; BREAST CANCER RESISTANCE PROTEIN; CD133 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CYCLIN D2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN DEPENDENT KINASE INHIBITOR 1C; CYTOKERATIN 18; CYTOKERATIN 8; EPITHELIAL CELL ADHESION MOLECULE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; HERMES ANTIGEN; NESTIN; NOTCH RECEPTOR; NUCLEAR RECEPTOR DAX 1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN S100B; SONIC HEDGEHOG PROTEIN; STAGE SPECIFIC EMBRYO ANTIGEN 1; STEM CELL ANTIGEN 1; TRANSCRIPTION FACTOR HESX1; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX9; UVOMORULIN; WNT PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL POPULATION; CELL RENEWAL; CELL TYPE; EMBRYO DEVELOPMENT; HYPOPHYSIS STEM CELL; MEDICAL RESEARCH; MULTIPOTENT STEM CELL; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; PHENOTYPE; PITUITARY GLAND; PITUITARY HORMONES; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS;

EID: 78650006101     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07523.x     Document Type: Article

References (140)

1. Allaerts, W. & Vankelecom, H. (2005) History and perspectives of pituitary folliculo-stellate cell research. Eur. J. Endocrinol., 153, 1-12.
2. Alvarez-Buylla, A. & Lim, D.A. (2004) For the long run: maintaining germinal niches in the adult brain. Neuron, 41, 683-686.
3. Andersen, B., Pearse, R.V., Jenne, K., Sornson, M., Lin, S.C., Bartke, A. & Rosenfeld, M.G. (1995) The ames dwarf gene is required for pit 1 gene activation. Dev. Biol., 172, 495-503.
4. Androutsellis-Theotokis, A., Leker, R.R., Soldner, F., Hoeppner, D.J., Ravin, R., Poser, S.W., Rueger, M.A., Bae, S.K., Kittappa, R. & Mckay, R.D.G. (2006) Notch signalling regulates stem cell numbers in vitro and in vivo. Nature, 442, 823-826.
5. Asa, S.L. & Ezzat, S. (2002) The pathogenesis of pituitary tumours. Nat. Rev. Cancer, 2, 836-849.
6. Barker, N., Van Es, J.H., Kuipers, J., Kujala, P., Van Den Born, B.M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P.J. & Clevers, H. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature, 449, 1003-1007.
7. Beltrami, A.P., Barlucchi, L., Torella, D., Baker, M., Limana, F., Chimenti, S., Kasahara, H., Rota, M., Musso, E., Urbanek, K., Leri, A., Kajstura, J., Nadal-Ginard, B. & Anversa, P. (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell, 114, 763-776.
8. Bilodeau, S., Roussel-Gervais, A. & Drouin, J. (2009) Distinct developmental roles of cell cycle inhibitors p57Kip2 and p27Kip1 distinguish pituitary progenitor cell cycle exit from cell cycle reentry of differentiated cells. Mol. Cell. Biol., 29, 1895-1908.
9. Borrelli, E., Heyman, R.A., Arias, C., Sawchenko, P.E. & Evans, R.M. (1989) Transgenic mice with inducible dwarfism. Nature, 339, 538-541.
10. Brabletz, T., Jung, A., Spaderna, S., Hlubek, F. & Kirchner, T. (2005) Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. Cancer, 5, 744-749.
11. Brinkmeier, M.L., Potok, M.A., Cha, K.B., Gridley, T., Stifani, S., Meeldijk, J., Clevers, H. & Camper, S.A. (2003) TCF and Groucho-related genes influence pituitary growth and development. Mol. Endocrinol., 17, 2152-2161.
12. Brinkmeier, M.L., Potok, M.A., Davis, S.W. & Camper, S.A. (2007) TCF4 deficiency expands ventral diencephalon signaling and increases induction of pituitary progenitors. Dev. Biol., 311, 396-407.
13. Capela, A. & Temple, S. (2002) LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron, 35, 865-875.
14. Carbajo-Perez, E. & Watanabe, Y.G. (1990) Cellular proliferation in the anterior pituitary of the rat during the postnatal period. Cell Tissue Res., 261, 333-338.
15. Challen, G.A. & Little, M.H. (2006) A side order of stem cells: the SP phenotype. Stem Cells, 24, 3-12.
16. Charles, M.A., Suh, H., Hjalt, T.A., Drouin, J., Camper, S.A. & Gage, P.J. (2005) PITX genes are required for cell survival and Lhx3 activation. Mol. Endocrinol., 19, 1893-1903.
17. Chauvet, N., El-Yandouzi, T., Mathieu, M.N., Schlernitzauer, A., Galibert, E., Lafont, C., Le Tissier, P., Robinson, I.C., Mollard, P. & Coutry, N. (2009) Characterization of adherens junction protein expression and localization in pituitary cell networks. J. Endocrinol., 202, 375-387.
18. 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.
19. 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.
20. Chen, J., Gremeaux, L., Fu, Q., Liekens, D., Van Laere, S. & Vankelecom, H. (2009) Pituitary progenitor cells tracked down by side population dissection. Stem Cells, 27, 1182-1195.
21. Childs, G.V. (2002) Development of gonadotropes may involve cyclic transdifferentiation of growth hormone cells. Arch. Physiol. Biochem., 110, 42-49.
22. Colvin, S.C., Mullen, R.D., Pfaeffle, R.W. & Rhodes, S.J. (2009) LHX3 and LHX4 transcription factors in pituitary development and disease. Pediatr. Endocrinol. Rev., 6(Suppl 2), 283-290.
23. Conboy, I.M. & Rando, T.A. (2002) The regulation of notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell, 3, 397-409.
24. Correr, S. & Motta, P.M. (1981) The rat pituitary cleft: a correlated study by scanning and transmission electron microscopy. Cell Tissue Res., 215, 515-529.
25. Corti, S., Locatelli, F., Papadimitriou, D., Donadoni, C., Salani, S., Del Bo, R., Strazzer, S., Bresolin, N. & Comi, G.P. (2006) Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cells, 24, 975-985.
26. Cushman, L.J., Watkins-Chow, D.E., Brinkmeier, M.L., Raetzman, L.T., Radak, A.L., Lloyd, R.V. & Camper, S.A. (2001) Persistent Prop1 expression delays gonadotrope differentiation and enhances pituitary tumor susceptibility. Hum. Mol. Genet., 10, 1141-1153.
27. Dattani, M.T., Martinez-Barbera, J.P., Thomas, P.Q., Brickman, J.M., Gupta, R., Martensson, I.L., Toresson, H., Fox, M., Wales, J.K., Hindmarsh, P.C., Krauss, S., Beddington, R.S. & Robinson, I.C. (1998) Mutations in the homeobox gene HESX1/Hesx1 associated with septo-optic dysplasia in human and mouse. Nat. Genet., 19, 125-133.
28. Devnath, S. & Inoue, K. (2008) An insight to pituitary folliculo-stellate cells. J. Neuroendocrinol., 20, 687-691.
29. Diaczok, D., Romero, C., Zunich, J., Marshall, I. & Radovick, S. (2008) A novel dominant negative mutation of OTX2 associated with combined pituitary hormone deficiency. J. Clin. Endocrinol. Metab., 93, 4351-4359.
30. Donangelo, I. & Melmed, S. (2006) Implication of pituitary tropic status on tumor development. Front. Horm. Res., 35, 1-8.
31. Dontu, G., Abdallah, W.M., Foley, J.M., Jackson, K.W., Clarke, M.F., Kawamura, M.J. & Wicha, M.S. (2003) In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev., 17, 1253-1270.
32. Dor, Y. & Melton, D.A. (2008) Facultative endocrine progenitor cells in the adult pancreas. Cell, 132, 183-184.
33. Drouin, J. (2006) Molecular mechanisms of pituitary differentiation and regulation: implications for hormone deficiencies and hormone resistance syndromes. Front. Horm. Res., 35, 74-87.
34. Ericson, J., Norlin, S., Jessell, T.M. & Edlund, T. (1998) Integrated FGF and BMP signaling controls the progression of progenitor cell differentiation and the emergence of pattern in the embryonic anterior pituitary. Development, 125, 1005-1015.
35. Fauquier, T., Rizzoti, K., Dattani, M., Lovell-Badge, R. & Robinson, I.C. (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.
36. Van Der Flier, L.G., Van Gijn, M.E., Hatzis, P., Kujala, P., Haegebarth, A., Stange, D.E., Begthel, H., Van Den Born, M., Guryev, V., Oving, I., Van Es, J.H., Barker, N., Peters, P.J., Van De Wetering, M. & Clevers, H. (2009) Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell, 136, 903-912.
37. Fontana, S. & Cohn, R.D. (2009) SP-litting the satellite niche to repopulate muscle. Cell Stem Cell, 4, 194-195.
38. Fujiwara, K., Kikuchi, M., Takigami, S., Kouki, T. & Yashiro, T. (2007) Expression of retinaldehyde dehydrogenase 1 in the anterior pituitary glands of adult rats. Cell Tissue Res., 329, 321-327.
39. Gage, F.H. (2000) Mammalian neural stem cells. Science, 287, 1433-1438.
40. Gage, P.J., Brinkmeier, M.L., Scarlett, L.M., Knapp, L.T., Camper, S.A. & Mahon, K.A. (1996) The Ames dwarf gene, df, is required early in pituitary ontogeny for the extinction of Rpx transcription and initiation of lineage- specific cell proliferation. Mol. Endocrinol., 10, 1570-1581.
41. Gage, P.J., Suh, H. & Camper, S.A. (1999) Dosage requirement of Pitx2 for development of multiple organs. Development, 126, 4643-4651.
42. Galichet, C., Lovell-Badge, R. & Rizzoti, K. (2010) Nestin-Cre mice are affected by hypopituitarism, which is not due to significant activity of the transgene in the pituitary gland. PLoS ONE, 5, e11443.
43. Gang, E.J., Bosnakovski, D., Figueiredo, C.A., Visser, J.W. & Perlingeiro, R.C. (2007) SSEA-4 identifies mesenchymal stem cells from bone marrow. Blood, 109, 1743-1751.
44. Garcia-Lavandeira, M., Quereda, V., Flores, I., Saez, C., Diaz-Rodriguez, E., Japon, M.A., Ryan, A.K., Blasco, M.A., Dieguez, C., Malumbres, M. & Alvarez, C.V. (2009) A GRFa2/Prop1/stem (GPS) cell niche in the pituitary. PLoS ONE, 4, e4815.
45. Gleiberman, A.S., Michurina, T., Encinas, J.M., Roig, J.L., Krasnov, P., Balordi, F., Fishell, G., Rosenfeld, M.G. & Enikolopov, G. (2008) Genetic approaches identify adult pituitary stem cells. Proc. Natl Acad. Sci. USA, 105, 6332-6337.
46. Goodell, M.A., Brose, K., Paradis, G., Conner, A.S. & Mulligan, R.C. (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med., 183, 1797-1806.
47. Graham, V., Khudyakov, J., Ellis, P. & Pevny, L. (2003) SOX2 functions to maintain neural progenitor identity. Neuron, 39, 749-765.
48. Hayashida, T., Takahashi, F., Chiba, N., Brachtel, E., Takahashi, M., Godin-Heymann, N., Gross, K.W., Vivanco, M.M., Wijendran, V., Shioda, T., Sgroi, D., Donahoe, P.K. & Maheswaran, S. (2010) HOXB9, a gene overexpressed in breast cancer, promotes tumorigenicity and lung metastasis. Proc. Natl Acad. Sci. USA, 107, 1100-1105.
49. Heddleston, J.M., Li, Z., Lathia, J.D., Bao, S., Hjelmeland, A.B. & Rich, J.N. (2010) Hypoxia inducible factors in cancer stem cells. Br. J. Cancer, 102, 789-795.
50. Horvath, E. & Kovacs, K. (2002) Folliculo-stellate cells of the human pituitary: a type of adult stem cell? Ultrastruct. Pathol., 26, 219-228.
51. Hugo, H., Ackland, M.L., Blick, T., Lawrence, M.G., Clements, J.A., Williams, E.D. & Thompson, E.W. (2007) Epithelial - mesenchymal and mesenchymal - epithelial transitions in carcinoma progression. J. Cell. Physiol., 213, 374-383.
52. Hussain, S.Z., Strom, S.C., Kirby, M.R., Burns, S., Langemeijer, S., Ueda, T., Hsieh, M. & Tisdale, J.F. (2005) Side population cells derived from adult human liver generate hepatocyte-like cells in vitro. Dig. Dis. Sci., 50, 1755-1763.
53. Jaks, V., Barker, N., Kasper, M., Van Es, J.H., Snippert, H.J., Clevers, H. & Toftgard, R. (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet., 40, 1291-1299.
54. Jandial, R. & Snyder, E.Y. (2009) A safer stem cell: on guard against cancer. Nat. Med., 15, 999-1001.
55. Jensen, J.N., Cameron, E., Garay, M.V.R., Starkey, T.W., Gianani, R. & Jensen, J. (2005) Recapitulation of elements of embryonic development in adult mouse pancreatic regeneration. Gastroenterology, 128, 728-741.
56. Jensen, K.B., Collins, C.A., Nascimento, E., Tan, D.W., Frye, M., Itami, S. & Watt, F.M. (2009) Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell, 4, 427-439.
57. Jones, P. & Simons, B.D. (2008) Epidermal homeostasis: do committed progenitors work while stem cells sleep? Nat. Rev. Mol. Cell Biol., 9, 82-88.
58. Kalluri, R. & Weinberg, R.A. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest., 119, 1420-1428.
59. Kerr, J., Wood, W. & Ridgway, E.C. (2008) Basic science and clinical research advances in the pituitary transcription factors: Pit-1 and Prop-1. Curr. Opin. Endocrinol. Diabetes Obes., 15, 359-363.
60. Kim, M. & Morshead, C.M. (2003) Distinct populations of forebrain neural stem and progenitor cells can be isolated using side-population analysis. J. Neurosci., 23, 10703-10709.
61. Kim, A.C., Barlaskar, F.M., Heaton, J.H., Else, T., Kelly, V.R., Krill, K.T., Scheys, J.O., Simon, D.P., Trovato, A., Yang, W.H. & Hammer, G.D. (2009) In search of adrenocortical stem and progenitor cells. Endocr. Rev., 30, 241-263.
62. Kioussi, C., O'Connell, S., St-Onge, L., Treier, M., Gleiberman, A.S., Gruss, P. & Rosenfeld, M.G. (1999) Pax6 is essential for establishing ventral-dorsal cell boundaries in pituitary gland development. Proc. Natl Acad. Sci. USA, 96, 14378-14382.
63. Kioussi, C., Briata, P., Baek, S.H., Rose, D.W., Hamblet, N.S., Herman, T., Ohgi, K.A., Lin, C., Gleiberman, A., Wang, J., Brault, V., Ruiz-Lozano, P., Nguyen, H.D., Kemler, R., Glass, C.K., Wynshaw-Boris, A. & Rosenfeld, M.G. (2002) Identification of a Wnt/Dvl/beta-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development. Cell, 111, 673-685.
64. Kita, A., Imayoshi, I., Hojo, M., Kitagawa, M., Kokubu, H., Ohsawa, R., Ohtsuka, T., Kageyama, R. & Hashimoto, N. (2007) Hes1 and Hes5 control the progenitor pool, intermediate lobe specification, and posterior lobe formation in the pituitary development. Mol. Endocrinol., 21, 1458-1466.
65. Krylyshkina, O., Chen, J., Mebis, L., Denef, C. & Vankelecom, H. (2005) Nestin-immunoreactive cells in rat pituitary are neither hormonal nor typical folliculo-stellate cells. Endocrinology, 146, 2376-2387.
66. Kunisato, A., Chiba, S., Nakagami-Yamaguchi, E., Kumano, K., Saito, T., Masuda, S., Yamaguchi, T., Osawa, M., Kageyama, R., Nakauchi, H., Nishikawa, M. & Hirai, H. (2003) HES-1 preserves purified hematopoietic stem cells ex vivo and accumulates side population cells in vivo. Blood, 101, 1777-1783.
67. Landolt, A.M. (1973) Regeneration of human pituitary. J. Neurosurg., 39, 35-41.
68. Lendahl, U., Zimmerman, L.B. & Mckay, R.D.G. (1990) CNS stem-cells express a new class of intermediate filament protein. Cell, 60, 585-595.
69. Leong, K.G., Wang, B.E., Johnson, L. & Gao, W.Q. (2008) Generation of a prostate from a single adult stem cell. Nature, 456, 804-808.
70. Lepore, D.A., Roeszler, K., Wagner, J., Ross, S.A., Bauer, K. & Thomas, P.Q. (2005) Identification and enrichment of colony-forming cells from the adult murine pituitary. Exp. Cell Res., 308, 166-176.
71. Lepore, D.A., Jokubaitis, V.J., Simmons, P.J., Roeszler, K., Rossi, R., Bauer, K. & Thomas, P.Q. (2006) A role for angiotensin converting enzyme in the charcterisation, enrichment and proliferation potential of adult murine pituitary colony forming cells. Stem Cells, 24, 2382-2390.
72. Levy, A. (2002) Physiological implications of pituitary trophic activity. J. Endocrinol., 174, 147-155.
73. Levy, A. (2008) Stem cells, hormones and pituitary adenomas. J. Neuroendocrinol., 20, 139-140.
74. Li, X., Perissi, V., Liu, F., Rose, D.W. & Rosenfeld, M.G. (2002) Tissue-specific regulation of retinal and pituitary precursor cell proliferation. Science, 297, 1180-1183.
75. Li, X., Oghi, K.A., Zhang, J., Krones, A., Bush, K.T., Glass, C.K., Nigam, S.K., Aggarwal, A.K., Maas, R., Rose, D.W. & Rosenfeld, M.G. (2003) Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature, 426, 247-254.
76. Lim, E., Wu, D., Pal, B., Bouras, T., Asselin-Labat, M.L., Vaillant, F., Yagita, H., Lindeman, G.J., Smyth, G.K. & Visvader, J.E. (2010) Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res., 12, R21.
77. Lin, C.R., Kioussi, C., O'Connell, S., Briata, P., Szeto, D., Liu, F., Izpisua-Belmonte, J.C. & Rosenfeld, M.G. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature, 401, 279-282.
78. Liu, Y.C., Tanaka, S., Inoue, K. & Kurosumi, K. (1989) Localization of fibronectin in the folliculo-stellate cells of the rat anterior-pituitary by the double bridge peroxidase-antiperoxidase method. Histochemistry, 92, 43-45.
79. Mani, S.A., Guo, W., Liao, M.J., Eaton, E.N., Ayyanan, A., Zhou, A.Y., Brooks, M., Reinhard, F., Zhang, C.C., Shipitsin, M., Campbell, L.L., Polyak, K., Brisken, C., Yang, J. & Weinberg, R.A. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell, 133, 704-715.
80. Marin, F., Boya, J. & Lopez-Carbonell, A. (1989) Immunocytochemical localization of vimentin in stellate cells (folliculo-stellate cells) of the rat, cat and rabbit pituitary pars-distalis. Anat. Embryol. (Berl.), 179, 491-495.
81. McNicol, A.M. & Carbajo-Perez, E. (1999) Aspects of anterior pituitary growth, with special reference to corticotrophs. Pituitary, 1, 257-268.
82. Mehta, A. & Dattani, M.T. (2008) Developmental disorders of the hypothalamus and pituitary gland associated with congenital hypopituitarism. Best Pract. Res. Clin. Endocrinol. Metab., 22, 191-206.
83. Melmed, S. (2003) Mechanisms for pituitary tumorigenesis: the plastic pituitary. J. Clin. Invest., 112, 1603-1618.
84. Molofsky, A.V., Pardal, R., Iwashita, T., Park, I.K., Clarke, M.F. & Morrison, S.J. (2003) Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature, 425, 962-967.
85. Monahan, P., Rybak, S. & Raetzman, L.T. (2009) The notch target gene HES1 regulates cell cycle inhibitor expression in the developing pituitary. Endocrinology, 150, 4386-4394.
86. Mullen, R.D., Colvin, S.C., Hunter, C.S., Savage, J.J., Walvoord, E.C., Bhangoo, A.P., Ten, S., Weigel, J., Pfäffle, R.W. & Rhodes, S.J. (2007) Roles of the LHX3 and LHX4 LIM-homeodomain factors in pituitary development. Mol. Cell. Endocrinol., 265-266, 190-195.
87. Nakajima, T., Yamaguchi, H. & Takahashi, K. (1980) S100 Protein in folliculostellate cells of the rat pituitary anterior aobe. Brain Res., 191, 523-531.
88. Nasonkin, I.O., Ward, R.D., Raetzman, L.T., Seasholtz, A.F., Saunders, T.L., Gillespie, P.J. & Camper, S.A. (2004) Pituitary hypoplasia and respiratory distress syndrome in Prop1 knockout mice. Hum. Mol. Genet., 13, 2727-2735.
89. Nica, G., Herzog, W., Sonntag, C., Nowak, M., Schwarz, H., Zapata, A.G. & Hammerschmidt, M. (2006) Eya1 is required for lineage-specific differentiation, but not for cell survival in the zebrafish adenohypophysis. Dev. Biol., 292, 189-204.
90. Nolan, L.A. & Levy, A. (2006) A population of non-luteinising hormone/non-adrenocorticotrophic hormone-positive cells in the male rat anterior pituitary responds mitotically to both gonadectomy and adrenalectomy. J. Neuroendocrinol., 18, 655-661.
91. Nolan, L.A. & Levy, A. (2009) The trophic effects of oestrogen on male rat anterior pituitary lactotrophs. J. Neuroendocrinol., 21, 457-464.
92. Nolan, L.A., Kavanagh, E., Lightman, S.L. & Levy, A. (1998) Anterior pituitary cell population control: basal cell turnover and the effects of adrenalectomy and dexamethasone treatment. J. Neuroendocrinol., 10, 207-215.
93. Nowak, J.A., Polak, L., Pasolli, H.A. & Fuchs, E. (2008) Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell, 3, 33-43.
94. Olson, L.E., Tollkuhn, J., Scafoglio, C., Krones, A., Zhang, J., Ohgi, K.A., Wu, W., Taketo, M.M., Kemler, R., Grosschedl, R., Rose, D., Li, X. & Rosenfeld, M.G. (2006) Homeodomain-mediated beta-catenin-dependent switching events dictate cell-lineage determination. Cell, 125, 593-605.
95. Peter, M.E. (2010) Regulating cancer stem cells the miR way. Cell Stem Cell, 6, 4-6.
96. Pogoda, H.M., Von Der Hardt, S., Herzog, W., Kramer, C., Schwarz, H. & Hammerschmidt, M. (2006) The proneural gene ascl1a is required for endocrine differentiation and cell survival in the zebrafish adenohypophysis. Development, 133, 1079-1089.
97. Polyak, K. & Weinberg, R.A. (2009) Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer, 9, 265-273.
98. Porter, T.E., Wiles, C.D. & Frawley, L.S. (1991) Evidence for bidirectional interconversion of mammotropes and somatotropes: rapid reversion of acidophilic cell types to pregestational proportions after weaning. Endocrinology, 129, 1215-1220.
99. Potok, M.A., Cha, K.B., Hunt, A., Brinkmeier, M.L., Leitges, M., Kispert, A. & Camper, S.A. (2008) WNT signaling affects gene expression in the ventral diencephalon and pituitary gland growth. Dev. Dyn., 237, 1006-1020.
100. Radisky, D.C. & LaBarge, M.A. (2008) Epithelial-mesenchymal transition and the stem cell phenotype. Cell Stem Cell, 2, 511-512.
101. Raetzman, L.T., Ward, R. & Camper, S.A. (2002) Lhx4 and Prop1 are required for cell survival and expansion of the pituitary primordia. Development, 129, 4229-4239.
102. Raetzman, L.T., Ross, S.A., Cook, S., Dunwoodie, S.L., Camper, S.A. & Thomas, P.Q. (2004) Developmental regulation of Notch signaling genes in the embryonic pituitary: Prop1 deficiency affects Notch2 expression. Dev. Biol., 265, 329-340.
103. Raetzman, L.T., Wheeler, B.S., Ross, S.A., Thomas, P.Q. & Camper, S.A. (2006) Persistent expression of notch2 delays gonadotrope differentiation. Mol. Endocrinol., 20, 2898-2908.
104. Raetzman, L.T., Cai, J.X. & Camper, S.A. (2007) Hes1 is required for pituitary growth and melanotrope specification. Dev. Biol., 304, 455-466.
105. Rando, T.A. (2006) Stem cells, ageing and the quest for immortality. Nature, 441, 1080-1086.
106. Reya, T., Duncan, A.W., Ailles, L., Domen, J., Scherer, D.C., Willert, K., Hintz, L., Nusse, R. & Weissman, I.L. (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 423, 409-414.
107. Reynolds, B.A. & Rietze, R.L. (2005) Neural stem cells and neurospheres - re-evaluating the relationship. Nat. Methods, 2, 333-336.
108. Rock, J.R., Onaitis, M.W., Rawlins, E.L., Lu, Y., Clark, C.P., Xue, Y., Randell, S.H. & Hogan, B.L. (2009) Basal cells as stem cells of the mouse trachea and human airway epithelium. Proc. Natl Acad. Sci. USA, 106, 12771-12775.
109. Romero, C.J., Nesi-Franca, S. & Radovick, S. (2009) The molecular basis of hypopituitarism. Trends Endocrinol. Metab., 20, 506-516.
110. Roskams, T. (2006) Different types of liver progenitor cells and their niches. J. Hepatol., 45, 1-4.
111. Saeger, W. & Warnecke, H. (1980) Ultrastructural examination of the regeneration of the rat adenohypophysis after partial hypophysectomy. Virchows Arch. A-Pathol. Anat. Histopathol., 387, 279-288.
112. Scheithauer, B.W., Sano, T., Kovacs, K.T., Young, W.F. Jr, Ryan, N. & Randall, R.V. (1990) The pituitary gland in pregnancy: a clinicopathologic and immunohistochemical study of 69 cases. Mayo Clin. Proc., 65, 461-474.
113. Seymour, P.A., Freude, K.K., Tran, M.N., Mayes, E.E., Jensen, J., Kist, R., Scherer, G. & Sander, M. (2007) SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proc. Natl Acad. Sci. USA, 104, 1865-1870.
114. Sheng, H.Z., Zhadanov, A.B., Mosinger, B., Fujii, T., Bertuzzi, S., Grinberg, A., Lee, E.J., Huang, S.P., Mahon, K.A. & Westphal, H. (1996) Specification of pituitary cell lineages by the lim homeobox gene lhx3. Science, 272, 1004-1007.
115. Sheng, H.Z., Moriyama, K., Yamashita, T., Li, H., Potter, S.S., Mahon, K.A. & Westphal, H. (1997) Multistep control of pituitary organogenesis. Science, 278, 1809-1812.
116. Slack, J.M. (2008) Origin of stem cells in organogenesis. Science, 322, 1498-1501.
117. Snippert, H.J., Haegebarth, A., Kasper, M., Jaks, V., Van Es, J.H., Barker, N., Van De Wetering, M., Van Den Born, M., Begthel, H., Vries, R.G., Stange, D.E., Toftgard, R. & Clevers, H. (2010) Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science, 327, 1385-1389.
118. Sornson, M.W., Wu, W., Dasen, J.S., Flynn, S.E., Norman, D.J., O'Connell, S.M., Gukovsky, I., Carriere, C., Ryan, A.K., Miller, A.P., Zuo, L., Gleiberman, A.S., Andersen, B., Beamer, W.G. & Rosenfeld, M.G. (1996) Pituitary lineage determination by the Prophet of Pit-1 homeodomain factor defective in Ames dwarfism. Nature, 384, 327-333.
119. Susa, T., Ishikawa, A., Kato, T., Nakayama, M. & Kato, Y. (2009) Molecular cloning of paired related homeobox 2 (Prx2) as a novel pituitary transcription factor. J. Reprod. Dev., 55, 502-511.
120. Tajima, T., Ohtake, A., Hoshino, M., Amemiya, S., Sasaki, N., Ishizu, K. & Fujieda, K. (2009) OTX2 loss of function mutation causes anophthalmia and combined pituitary hormone deficiency with a small anterior and ectopic posterior pituitary. J. Clin. Endocrinol. Metab., 94, 314-319.
121. Takuma, N., Sheng, H.Z., Furuta, Y., Ward, J.M., Sharma, K., Hogan, B.L., Pfaff, S.L., Westphal, H., Kimura, S. & Mahon, K.A. (1998) Formation of Rathke's pouch requires dual induction from the diencephalon. Development, 125, 4835-4840.
122. Taniguchi, Y., Yasutaka, S., Kominami, R. & Shinohara, H. (2002) Proliferation and differentiation of rat anterior pituitary cells. Anat. Embryol., 206, 1-11.
123. Thiery, J.P., Acloque, H., Huang, R.Y. & Nieto, M.A. (2009) Epithelial-mesenchymal transitions in development and disease. Cell, 139, 871-890.
124. Toma, J.G., Akhavan, M., Fernandes, K.J.L., Barnabe-Heider, F., Sadikot, A., Kaplan, D.R. & Miller, F.D. (2001) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol., 3, 778-784.
125. Vankelecom, H. (2007a) Non-hormonal cell types in the pituitary candidating for stem cell. Semin. Cell Dev. Biol., 18, 559-570.
126. Vankelecom, H. (2007b) Stem cells in the postnatal pituitary? Neuroendocrinology, 85, 110-130.
127. th Annual Meeting of the International Society for Stem Cell Research (ISSCR), Philadelphia, PA, USA.
128. Vidal, S., Horvath, E., Kovacs, K., Lloyd, R.V. & Smyth, H.S. (2001) Reversible transdifferentiation: interconversion of somatotrophs and lactotrophs in pituitary hyperplasia. Mod. Pathol., 14, 20-28.
129. Wagers, A.J. & Conboy, I.M. (2005) Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell, 122, 659-667.
130. Ward, R.D., Raetzman, L.T., Suh, H., Stone, B.M., Nasonkin, I.O. & Camper, S.A. (2005) Role of PROP1 in pituitary gland growth. Mol. Endocrinol., 19, 698-710.
131. Ward, R.D., Stone, B.M., Raetzman, L.T. & Camper, S.A. (2006) Cell proliferation and vascularization in mouse models of pituitary hormone deficiency. Mol. Endocrinol., 20, 1378-1390.
132. Weiss, S., Siebzehnrubl, F.A., Kreutzer, J., Blumcke, I. & Buslei, R. (2009) Evidence for a progenitor cell population in the human pituitary. Clin. Neuropathol., 28, 309-318.
133. Wilson, D.B. (1986) Distribution of 3H-thymidine in the postnatal hypophysis of the C57BL mouse. Acta Anat. (Basel), 126, 121-126.
134. Wouters, J., Vankelecom, H. & Van Den Oord, J. (2009) Cancer stem cells in cutaneous melanoma. Expert. Rev. Dermatol., 4, 225-235.
135. Wulf, G.G., Luo, K.L., Jackson, K.A., Brenner, M.K. & Goodell, M.A. (2003) Cells of the hepatic side population contribute to liver regeneration and can be replenished by bone marrow stem cells. Haematologica, 88, 368-378.
136. Yoshimura, F., Soji, T. & Kiguchi, Y. (1977) Relationship between the follicular cells and marginal layer cells of the anterior pituitary. Endocrinol. Jpn., 24, 301-305.
137. Zhu, X. & Rosenfeld, M.G. (2004) Transcriptional control of precursor proliferation in the early phases of pituitary development. Curr. Opin. Genet. Dev., 14, 567-574.
138. Zhu, X., Lin, C.R., Prefontaine, G.G., Tollkuhn, J. & Rosenfeld, M.G. (2005) Genetic control of pituitary development and hypopituitarism. Curr. Opin. Genet. Dev., 15, 332-340.
139. Zhu, X., Zhang, J., Tollkuhn, J., Ohsawa, R., Bresnick, E.H., Guillemot, F., Kageyama, R. & Rosenfeld, M.G. (2006) Sustained Notch signaling in progenitors is required for sequential emergence of distinct cell lineages during organogenesis. Genes Dev., 20, 2739-2753.
140. Zhu, X., Gleiberman, A.S. & Rosenfeld, M.G. (2007) Molecular physiology of pituitary development: signaling and transcriptional networks. Physiol. Rev., 87, 933-963.