P21, an important mediator of quiescence during pituitary tumor formation, is dispensable for normal pituitary development during embryogenesis

Mechanisms of Development

Volumn 128, Issue 11-12, 2012, Pages 640-652

  Monahan, Pamela ^a,b   Himes, Ashley D ^a   Parfieniuk, Agata ^a   Raetzman, Lori T ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cell cycle; P21; P27; Pituitary

Indexed keywords

CYCLIN B1; CYCLIN D1; CYCLIN D2; CYCLIN E; CYCLIN E1; HISTONE H3; KI 67 ANTIGEN; MESSENGER RNA; MYC PROTEIN; PROTEIN P21; PROTEIN P27; PROTEIN P57; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DENSITY; CELL EXPANSION; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; FEMALE; HYPOPHYSIS; MALE; MOUSE; MUTANT; NONHUMAN; ORGANOGENESIS; PITUITARY GLAND DEVELOPMENT; PITUITARY PROGENITOR CELL; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RATHKE POUCH; STEM CELL;

ANIMALS; CELL CYCLE PROTEINS; CELL PROLIFERATION; CELL SHAPE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; KI-67 ANTIGEN; MALE; MICE; MICE, KNOCKOUT; PITUITARY GLAND; STEM CELLS;

MUS;

EID: 84857787846     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2011.11.002     Document Type: Article

References (64)

1. Abbas T., Dutta A. P21 in cancer: intricate networks and multiple activities. Nature 2009, 9:400-414.
2. Cip1 promotes cyclin D1 nuclear accumulation via direct inhibition of nuclear export. J. Biol. Chem. 2002, 277:8517-8523.
3. Bamberger C.M., Fehn M., Bamberger A., Ludecke D.K., Beil F.U., Saeger W., Schulte H.M. Reduced expression levels of the cell-cycle inhibitor p21Kip1 in human pituitary adenomas. Eur. J. Endocrinol. 1999, 140:250-255.
4. Bilodeau S., Roussel-Gervais A., Drouin J. Distinct developmental roles of cell cycle inhibitors p57Kip1 and p27Kip2 distinguish pituitary progenitor cell cycle exit from cell cycle re-entry of differentiated cells. Mol. Cell. Biol. 2009, 29:1895-1908.
5. Brinkmeier M.L., Potok M.A., Davis S.W., Camper S.A. TCF4 deficiency expands ventral diencephalon signaling and increases induction of pituitary progenitors. Dev. Biol. 2007, 311:396-407.
6. Brugarolas J., Chandrasekaran C., Gordan J.I., Beach D., Jacks T., Hannon G.J. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 2002, 377:552-557.
7. Brugarolas J., Bronson R.T., Jacks T. P21 Is a critical CDK2 regulator essential for proliferation control in Rb-deficient cells. J. Cell Biol. 1998, 141:503-514.
8. Burrow G.N., Wortzman G., Rewcastle N.B., Holgate R.C., Kovacs K. Microadenomas of the pituitary and abnormal sellar tomograms in an unselected autopsy series. N. Engl. J. Med. 1981, 304:156-158.
9. Buurman H., Saeger W. Subclinical adenomas in postmortem pituitaries: classification and correlations to clinical data. Eur. J. Endocrinol. 2006, 154:753-758.
10. Chen J., Jackson P.K., Kirschner M.W., Dutta A. Separate domains of p21 involved in the inhibition of Cdk kinase and PCNA. Nature 2002, 374:386-388.
11. Kip1 CDK 'inhibitors' are essential activators of cyclin D-dependent kinases in murine fibroblasts. EMBO J. 1999, 18:1571-1583.
12. Chesnokova V., Kovacs K., Castro A., Zonis S., Melmed S. Pituitary hypoplasia in Pttg-/- mice is protective for Rb+/- pituitary tumorigenesis. Mol. Endocrinol. 2005, 19:2371-2379.
13. Cip1 restrains pituitary tumor growth. Proc. Natl. Acad. Sci. USA 2008, 105:17498-17503.
14. Chesnokova V., Wong C., Zonis S., Gruszka A., Wawrowsky K., Ren S.-G., BenShlomo A., Yu R. Diminished pancreatic β-cell mass in securin-null mice is caused by β-cell apoptosis and senescence. Endocrinology 2009, 150:2603-2610.
15. Daly A.F., Rixhon M., Adam C., Dempegioti A., Tichomirowa M.A., Beckers A. High prevalence of pituitary adenomas: a cross-sectional study in the province of Liege, Belgium. J. Clin. Endocrinol. Metab. 2006, 91:4769-4775.
16. CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995, 82:675-684.
17. Ezzat S., Asa S.L., Couldwell W.T., Barr C.E., Dodge W.E., Vance M.L., McCutcheon I.E. The prevalence of pituitary adenomas. Cancer 2004, 101:613-619.
18. Fauquier T., Rizzoti K., Dattani M., Lovell-Badge R., Robinson Iain C.A.F. SOX2-expressing progenitor cells generate all of the major cell types in the adult mouse pituitary gland. Proc. Natl. Acad. Sci. USA 2008, 105:2907-2912.
19. Fernandez A., Karavitaki N., Wass J.A. Prevalence of pituitary adenomas: a community-based, cross-sectional study in Banbury (Oxfordshire, UK). Clin. Endocrinol. 2010, 72:377-382.
20. Fero M.L., Rivkin M., Tasch M., Porter P., Carow C.E., Firpo E., Polyak K., Tsai L., Broudy V., Perimutter R.M., Kaushansky K., Roberts J.M. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis and female sterility in p27Kip1-deficient mice. Cell 1996, 85:733-744.
21. Fotedar R., Brickner H., Saadatmandi N., Rousselle T., Diederich L., Munshi A., Jung B., Reed J.C., Fotedar A. Effect of p21waf1/cip1 transgene on radiation induced apoptosis in T cells. Oncogene 1999, 18:3652-3658.
22. Franklin D.S., Godfrey V.L., Lee H., Kovalev G.I., Schoonhoven R., Chen-Kiang S., Su L., Xiong Y. CDK inhibitors p18INK4c and p27Kip1 mediate two separate pathways to collaboratively suppress pituitary tumorigenesis. Genes Dev. 1998, 12:2899-2911.
23. Franklin D.S., Godfrey V.L., O'Brien D.A., Deng C., Xiong Y. Functional collaboration between different cyclin-dependent kinase inhibitors suppresses tumor growth with distinct tissue specificity. Mol. Cell. Biol. 2000, 20:6147-6158.
24. 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. A GRFa2/Prop1/Stem (GPS) cell niche in the pituitary. PLoS One 2009, 4:1-16.
25. Georgitsi M., Raitila A., Karhu A., van der Luijt R.B., Aalfs C.M., Sane T., Vierimaa O., Mäkinen M.J., Tuppurainen K., Paschke R., Gimm O., Koch C.A., Gündogdu S., Lucassen A., Tischkowitz M., Izatt L., Aylwin S., Bano G., Hodgson S., De Menis E., Launonen V., Vahteristo P., Aaltonen L.A. Germline CDKN1B/p27Kip1 mutation in multiple endocrine neoplasia. J. Clin. Endocrinol. Metab. 2007, 92:3321-3325.
26. Goldberg L.B., Aujla P.K., Raetzman L.T. Persistent expression of activated Notch inhibits corticotrope and melanotrope differentiation and results in dysfunction of the HPA axis. Dev. Biol. 2011, 358:23-32.
27. Ikeda H., Yoshimoto T. Developmental changes in proliferative activity of cells of the murine Rathke's pouch. Cell Tissue Res. 1991, 263:41-47.
28. Jiang Z., Liang P., Leng R., Guo Z., Liu Y., Liu X., Bubnic S., Keating A., Murray D., Goss P., Zacksenhaus E. E2F1 and p53 are dispensable, whereas p21(Waf1/Cip1) cooperates with Rb to restrict endoreduplication and apoptosis during skeletal myogenesis. Dev. Biol. 2000, 227:8-41.
29. Jordan S., Lindhar K., Korbonits M., Lowe D.G., Grossman A.B. Cyclin D and cyclin E expression in normal and adenomatous pituitary. Eur. J. Endocrinol. 2000, 143:R1-R6.
30. Kadowaki Y., Fujiwara T., Fukazawa T., Shao J., Yasuda T., Itoshima T., Kagawa S., Hudson L.G., Roth J.A., Tanaka N. Induction of differentiation-dependent apoptosis in human esophageal squamous cell carcinoma by adenovirus-mediated p21 gene transfer. Clin. Cancer Res. 1999, 5:4233-4241.
31. Kang K.H., Kim W.H., Choi K.H. P21 promotes ceramide-induced apoptosis and antagonizes the antideath effect of Bcl-2 in human hepatocarcinoma cells. Exp. Cell Res. 1999, 253:403-412.
32. Karl J., Capel B. Sertoli cells of the mouse testis originate from the coelomic epithelium. Dev. Biol. 1998, 203:323-333.
33. 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., Wynshaw-Boris A., Rosenfeld M.G. Identification of a Wnt/Dvl/β-Catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 2002, 111:673-685.
34. Kiyokawa H., Kineman R.D., Manova-Todorova K.O., Soares V.C., Hoffman E.S., Ono M., Khanam D., Hayday A.C., Frohman L.A., Koff A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27Kip1. Cell 1996, 85:721-732.
35. LaBaer J., Garrett M.D., Stevenson L.F., Slingerland J.M., Sandhu C., Chou H.S., Fatteay A., Harlow E. New functional activities for the p21 family of CDK inhibitors. Genes Dev. 1997, 11:847-862.
36. Waf1/Cip1. EMBO J. 2007, 26:4683-4693.
37. Martin-Caballero J., Flores J.M., Garcia-Palencia P., Serrano M. Tumor susceptibility of p21Waf1/Cip1-deficient mice. Cancer Res. 2001, 61:6234-6238.
38. Monahan P., Rybak S., Raetzman L.T. The notch target gene HES1 regulates cell cycle inhibitor expression in the developing pituitary. Endocrinology 2009, 150:4386-4394.
39. Musat M., Vax V.V., Borboli N., Gueorguiev M., Bonner S., Korbonits M., Grossman A.B. Cell cycle dysregulation in pituitary oncogenesis. Front. Horm. Res. 2004, 32:34-62.
40. Miyatsuka T., Kosaka Y., Kim H., German M.S. Neurogenin3 inhibits proliferation in endocrine progenitors by inducing Cdkn1a. Proc. Natl. Acad. Sci. USA 2011, 108:185-190.
41. Nakayama K., Ishida N., Shirane M., Inomata A., Inoue T., Shishido N., Horii I., Loh D.Y., Nakayama K. Mice lacking p27Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 1996, 85:707-720.
42. Neto A.G., McCutcheon I.E., Vang R., Spencer M.L., Zhang W., Fuller G.N. Elevated expression of p21 (WAF1/Cip1) in hormonally active pituitary adenomas. Ann. Diagn. Pathol. 2005, 9:6-10.
43. Kip1 is required to maintain proliferative quiescence in the adult cochlea and pituitary. Cell Cycle 2011, 10:1237-1248.
44. Ozaki K., Hanazawa S. Porphyromonas gingivalis fimbriae inhibit caspase-3-mediated apoptosis of monocytic THP-1 cells under growth factor deprivation via extracellular signal-regulated kinase-dependent expression of p21 Cip/WAF1. Infect. Immun. 2001, 69:4944-4950.
45. Paramio J.M., Segrelles C., Ruiz S., Martin-Caballero J., Page A., Martinez J., Serrano M., Jorcano J.L. The ink4a/arf tumor suppressors cooperate with p21cip1/waf in the processes of mouse epidermal differentiation, senescence, and carcinogenesis. J. Biol. Chem. 2001, 276:44203-44211.
46. Park M.S., Rosai J., Nguyen H.T., Capodieci P., Cordon-Cardo C., Koff A. P27 and Rb are on overlapping pathways suppressing tumorigenesis in mice. Proc. Natl. Acad. Sci. USA 1999, 96:6382-6387.
47. Pellegata N.S., Quintanilla-Martinez L., Siggelkow H., Samson E., Bink K., Hofler H., Fend F., Graw J., Atkinson M.J. Germ-line mutations in p27Kip1 cause a multiple endocrine neoplasia syndrome in rat and humans. Proc. Natl. Acad. Sci. USA 2006, 103:15558-15563.
48. Qian X., Kulig E., Jin L., Lloyd R.V. Expression of D-type cyclins in normal and neoplastic rat pituitary. Endocrinology 1998, 139:2058-2066.
49. Quereda V., Malumbres M. Cell cycle control of pituitary development and disease. J. Mol. Endocrinol. 2009, 42:75-86.
50. Raetzman L.T., Ross S.A., Cook S., Dunwoodie S.L., Camper S.A., Thomas P.Q. Developmental regulation of Notch signaling genes in the embryonic pituitary: Prop1 deficiency affects Notch2 expression. Dev. Biol. 2004, 265:329-340.
51. Raetzman L.T., Cai J.X., Camper S.A. Hes1 is required for pituitary growth and melanotrope specification. Dev. Biol. 2007, 304:455-466.
52. Roussel-Gervais A., Biloideau S., Vallette S., Berthelet F., Lacroix A., Figarella-Branger D., Brue T., Drouin J. Cooperation between Cyclin E and p27Kip1 in pituitary tumorigenesis. Mol. Endocrinol. 2010, 24:1835-1845.
53. 2 DNA damage checkpoint. J. Biol. Chem. 2000, 275:30638-30643.
54. Taniguchi Y., Yasutaka S., Kominami R., Shinohara H. Mitoses of thyrotrophs contribute to the proliferation of the rat pituitary gland during the early postnatal period. Anat. Embryol. (Berl.) 2002, 206:67-72.
55. Taniguchi Y., Yasutaka S., Kominami R., Shinohara H. Proliferation and differentiation of pituitary somatotrophs and mammotrophs during late fetal and postnatal periods. Anat. Embryol. (Berl.) 2001, 204:469-475.
56. Taniguchi Y., Yasutaka S., Kominami R., Shinohara H. Proliferation and differentiation of thyrotrophs in the pars distalis of the rat pituitary gland during the fetal and postnatal period. Anat. Embryol. (Berl.) 2001, 203:250-253.
57. Taniguchi Y., Kominami R., Yasutaka S., Shinohara H. Mitoses of existing corticotrophs contribute to their proliferation in the rat pituitary during the late fetal period. Anat. Embryol. (Berl.) 2001, 203:89-93.
58. Taniguchi Y., Kominami R., Yasutaka S., Kawarai Y. Proliferation and differentiation of pituitary corticotrophs during the fetal and postnatal periods: a quantitative immunocytochemical study. Anat. Embryol. (Berl.) 2000, 201:229-234.
59. Tsao Y., Huang S., Chang J., Hsieh J., Pong R., Chen S. Adenovirus-Mediated p21(WAF1/SDII/CIP1) gene transfer induces apoptosis of human cervical cancer cell lines. J. Virol. 1999, 73:4983-4990.
60. Turner H.E., Nagy Z., Sullivan N., Esiri M.M., Wass J.A. Expression analysis of cyclins in pituitary adenomas and the normal pituitary gland. Clin. Endocrinol. 2000, 53:337-344.
61. Vasey D.B., Wolf C.R., Brown K., Whitelaw C.B. Spatial p21 expression profile in the mid-term mouse embryo. Transgenic Res. 2010, 20:23-28.
62. WAF1 enhances papilloma formation but not malignant conversion in experimental mouse skin carcinogenesis. Cancer Res. 1999, 59:2050-2054.
63. Waf1/Cip1 is an assembly factor required for platelet-derived growth factor-induced vascular smooth muscle cell proliferation. J. Biol. Chem. 2000, 275:10285-10290.
64. Zhu X., Zhang J., Tollkuhn J., Ohsawa R., Bresnick E.H., Guillemot F., Kageyama R., Rosenfeld M.G. Sustained Notch signaling in progenitors is required for sequential emergence of distinct cell lineages during organogenesis. Genes Dev. 2006, 20:2739-2753.