Constitutive activation of smoothened leads to female infertility and altered uterine differentiation in the mouse

Biology of Reproduction

Volumn 82, Issue 5, 2010, Pages 991-999

  Franco, Heather L ^a   Lee, Kevin Y ^a   Rubel, Cory A ^a   Creighton, Chad J ^a   White, Lisa D ^a   Broaddus, Russell R ^b   Lewis, Michael T ^a   Lydon, John P ^a   Jeong, Jae Wook ^a   DeMayo, Francesco J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Differentiation; Implantation; Mouse; Smoothened; Uterus

Indexed keywords

CRE RECOMBINASE; PROGESTERONE; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECIDUA; EMBRYO; ENDOMETRIUM; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; FEMALE INFERTILITY; FIRST TRIMESTER PREGNANCY; MICROARRAY ANALYSIS; MORPHOLOGY; MOUSE; NIDATION; NONHUMAN; OVULATION; PERINATAL PERIOD; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; TISSUE DIFFERENTIATION;

ANIMALS; CELL DIFFERENTIATION; DECIDUA; EMBRYO IMPLANTATION; FEMALE; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; INFERTILITY, FEMALE; METABOLOME; MICE; MICE, MUTANT STRAINS; PREGNANCY; PROGESTERONE; PROTEIN ARRAY ANALYSIS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; UTERUS;

ERINACEIDAE; MURINAE; MUS;

EID: 77953826432     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.081513     Document Type: Article

References (49)

1. Yin Y, Ma L. Development of the mammalian female reproductive tract. J Biochem 2005; 137:677-683.
2. Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. Developmental biology of uterine glands. Biol Reprod 2001; 65:1311-1323.
3. Gray CA, Taylor KM, Ramsey WS, Hill JR, Bazer FW, Bartol FF, Spencer TE. Endometrial glands are required for preimplantation conceptus elongation and survival. Biol Reprod 2001; 64:1608-1613.
4. Franco HL, Jeong JW, Tsai SY, Lydon JP, DeMayo FJ. In vivo analysis of progesterone receptor action in the uterus during embryo implantation. Semin Cell Dev Biol 2008; 19:178-186.
5. Matsumoto H, Zhao X, Das SK, Hogan BL, Dey SK. Indian hedgehog as a progesterone-responsive factor mediating epithelial-mesenchymal interactions in the mouse uterus. Dev Biol 2002; 245:280-290.
6. Takamoto N, Zhao B, Tsai SY, DeMayo FJ. Identification of Indian hedgehog as a progesterone-responsive gene in the murine uterus. Mol Endocrinol 2002; 16:2338-2348.
7. Varjosalo M, Taipale J. Hedgehog: functions and mechanisms. Genes Dev 2008; 22:2454-2472.
8. Krishnan V, Elberg G, Tsai MJ, Tsai SY. Identification of a novel sonic hedgehog response element in the chicken ovalbumin upstream promoter- transcription factor II promoter. Mol Endocrinol 1997; 11:1458-1466.
9. Krishnan V, Pereira FA, Qiu Y, Chen CH, Beachy PA, Tsai SY, Tsai MJ. Mediation of Sonic hedgehog-induced expression of COUP-TFII by a protein phosphatase. Science 1997; 278:1947-1950.
10. St-Jacques B, Hammerschmidt M, McMahon AP. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 1999; 13:2072-2086.
11. Day TF, Yang Y. Wnt and hedgehog signaling pathways in bone development. J Bone Joint Surg Am 2008; 90(suppl 1):19-24.
12. Long F, Zhang XM, Karp S, Yang Y, McMahon AP. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001; 128:5099-5108. (Pubitemid 34086893)
13. Lee K, Jeong J, Kwak I, Yu CT, Lanske B, Soegiarto DW, Toftgard R, Tsai MJ, Tsai S, Lydon JP, DeMayo FJ. Indian hedgehog is a major mediator of progesterone signaling in the mouse uterus. Nat Genet 2006; 38:1204-1209.
14. Soyal SM, Mukherjee A, Lee KY, Li J, Li H, DeMayo FJ, Lydon JP. Cremediated recombination in cell lineages that express the progesterone receptor. Genesis 2005; 41:58-66.
15. Talbi S, Hamilton AE, Vo KC, Tulac S, Overgaard MT, Dosiou C, Le Shay N, Nezhat CN, Kempson R, Lessey BA, Nayak NR, Giudice LC. Molecular phenotyping of human endometrium distinguishes menstrual cycle phases and underlying biological processes in normo-ovulatory women. Endocrinology 2006; 147:1097-1121.
16. Burney RO, Talbi S, Hamilton AE, Vo KC, Nyegaard M, Nezhat CR, Lessey BA, Giudice LC. Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis. Endocrinology 2007; 148:3814-3826.
17. Kurihara I, Lee DK, Petit FG, Jeong J, Lee K, Lydon JP, DeMayo FJ, Tsai MJ, Tsai SY. COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS Genet 2007; 3:e102.
18. Takamoto N, Kurihara I, Lee K, Demayo FJ, Tsai MJ, Tsai SY. Haploinsufficiency of chicken ovalbumin upstream promoter transcription factor II in female reproduction. Mol Endocrinol 2005; 19:2299-2308.
19. Xie J, Murone M, Luoh SM, Ryan A, Gu Q, Zhang C, Bonifas JM, Lam CW, Hynes M, Goddard A, Rosenthal A, Epstein EH Jr, de Sauvage FJ. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998; 391:90-92.
20. Jeong J, Mao J, Tenzen T, Kottmann AH, McMahon AP. Hedgehog signaling in the neural crest cells regulates the patterning and growth of facial primordia. Genes Dev 2004; 18:937-951.
21. Hogan B, Costantini F, Lacy E. Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1986.
22. Finn CA, Martin L. Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biol Reprod 1972; 7:82-86.
23. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997; 277: 1109-1113.
24. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21:70-71.
25. Creighton CJ, Casa A, Lazard Z, Huang S, Tsimelzon A, Hilsenbeck SG, Osborne CK, Lee AV. Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis. J Clin Oncol 2008; 26:4078-4085.
26. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 2003; 4:P3.
27. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57.
28. Besnard V, Wert SE, Hull WM, Whitsett JA. Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 2004; 5:193-208.
29. McCluggage WG, Sumathi VP, Maxwell P. CD10 is a sensitive and diagnostically useful immunohistochemical marker of normal endometrial stroma and of endometrial stromal neoplasms. Histopathology 2001; 39: 273-278.
30. Mrugala D, Dossat N, Ringe J, Delorme B, Coffy A, Bony C, Charbord P, Haupl T, Daures JP, Noel D, Jorgensen C. Gene expression profile of multipotent mesenchymal stromal cells: identification of pathways common to TGFbeta3/BMP2-induced chondrogenesis. Cloning Stem Cells 2009; 23:711-723.
31. Funari VA, Day A, Krakow D, Cohn ZA, Chen Z, Nelson SF, Cohn DH. Cartilage-selective genes identified in genome-scale analysis of non-cartilage and cartilage gene expression. BMC Genomics 2007; 8:165.
32. Yang Y, Topol L, Lee H, Wu J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 2003; 130:1003-1015.
33. Lai LP, Mitchell J. Indian hedgehog: its roles and regulation in endochondral bone development. J Cell Biochem 2005; 96:1163-1173.
34. Aszterbaum M, Epstein J, Oro A, Douglas V, LeBoit PE, Scott MP, Epstein EH Jr. Ultraviolet and ionizing radiation enhance the growth of BCCs and trichoblastomas in patched heterozygous knockout mice. Nat Med 1999; 5:1285-1291.
35. Corcoran RB, Scott MP. A mouse model for medulloblastoma and basal cell nevus syndrome. J Neurooncol 2001; 53:307-318.
36. Hahn H, Wojnowski L, Zimmer AM, Hall J, Miller G, Zimmer A. Rhabdomyosarcomas and radiation hypersensitivity in a mouse model of Gorlin syndrome. Nat Med 1998; 4:619-622.
37. Mao J, Ligon KL, Rakhlin EY, Thayer SP, Bronson RT, Rowitch D, McMahon AP. A novel somatic mouse model to survey tumorigenic potential applied to the Hedgehog pathway. Cancer Res 2006; 66:10171-10178.
38. Ren Y, Cowan RG, Harman RM, Quirk SM. Dominant activation of the hedgehog signaling pathway in the ovary alters theca development and prevents ovulation. Mol Endocrinol 2009; 11:61-76.
39. Suarez SS, Pacey AA. Sperm transport in the female reproductive tract. Hum Reprod Update 2006; 12:23-37. (Pubitemid 43013744)
40. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Kontgen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 1992; 359:76-79.
41. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L, Stewart CL. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000; 141:4365-4372.
42. Bartol FF, Wiley AA, Coleman DA, Wolfe DF, Riddell MG. Ovine uterine morphogenesis: effects of age and progestin administration and withdrawal on neonatal endometrial development and DNA synthesis. J Anim Sci 1988; 66:3000-3009.
43. Donofrio G, Franceschi V, Capocefalo A, Cavirani S, Sheldon IM. Bovine endometrial stromal cells display osteogenic properties. Reprod Biol Endocrinol 2008; 6:65.
44. Wolff EF, Wolff AB, Hongling D, Taylor HS. Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis. Reprod Sci 2007; 14:524-533.
45. Adolphe C, Narang M, Ellis T, Wicking C, Kaur P, Wainwright B. An in vivo comparative study of sonic, desert and Indian hedgehog reveals that hedgehog pathway activity regulates epidermal stem cell homeostasis. Development 2004; 131:5009-5019.
46. Kurita T, Cunha GR, Robboy SJ, Mills AA, Medina RT. Differential expression of p63 isoforms in female reproductive organs. Mech Dev 2005; 122:1043-1055.
47. Kurita T, Mills AA, Cunha GR. Roles of p63 in the diethylstilbestrolinduced cervicovaginal adenosis. Development 2004; 131:1639-1649.
48. Mericskay M, Kitajewski J, Sassoon D. Wnt5a is required for proper epithelial-mesenchymal interactions in the uterus. Development 2004; 131:2061-2072. (Pubitemid 38702039)
49. Miller C, Sassoon DA. Wnt-7a maintains appropriate uterine patterning during the development of the mouse female reproductive tract. Development 1998; 125:3201-3211. (Pubitemid 28434418)