Misexpression of cyclin D1 in embryonic germ cells promotes testicular teratoma initiation

References

• Kunwar PS, Siekhaus DE, Lehmann R. In vivo migration: a germ cell perspective. AnnuRevCell DevBiol 2006; 22:237-65.
   PubMed Web of Science ®Google Scholar
• Aponte PM, van Bragt MP, de Rooij DG, van Pelt AM. Spermatogonial stem cells: characteristics and experimental possibilities. APMIS 2005; 113:727-42; PMID:16480445; http://dx.doi.org/10.1111/j.1600-0463.2005.apm_302.x
   PubMed Web of Science ®Google Scholar
• Stevens L. Development of resistance to teratocarcinogenesis by primordial germ cells in mice. J Natl Cancer Inst 1966; 37:859-67; PMID:6005945
   PubMedGoogle Scholar
• Looijenga LH, Stoop H, de Leeuw HP, de Gouveia Brazao CA, Gillis AJ, van Roozendaal KE, van Zoelen EJ, Weber RF, Wolffenbuttel KP, van DH, et al. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res 2003; 63:2244-50; PMID:12727846
   PubMed Web of Science ®Google Scholar
• Almstrup K, Hoei-Hansen CE, Wirkner U, Blake J, Schwager C, Ansorge W, Nielsen JE, Skakkebaek NE, Rajpert-de ME, Leffers H. Embryonic stem cell-like features of testicular carcinoma in situ revealed by genome-wide gene expression profiling. Cancer Res 2004; 64:4736-43; PMID:15256440; http://dx.doi.org/10.1158/0008-5472.CAN-04-0679
   PubMed Web of Science ®Google Scholar
• Oosterhuis JW, Looijenga LH. Testicular germ-cell tumours in a broader perspective. NatRevCancer 2005; 5:210-22
   Google Scholar
• Heaney JD, Nadeau JH. Testicular germ cell tumors in mice: new ways to study a genetically complex trait. Methods MolBiol 2008; 450:211-31
   PubMedGoogle Scholar
• Bustamante-Marin X, Garness JA, Capel B. Testicular teratomas: an intersection of pluripotency, differentiation and cancer biology. The International journal of developmental biology 2013; 57:201-10; PMID:23784831; http://dx.doi.org/10.1387/ijdb.130136bc
   PubMed Web of Science ®Google Scholar
• Stevens L, Hummel K. A description of spontaneous congenital testicular teratomas in strain 129 mice. JNatlCancer Inst 1957; 18:719-47.
   PubMed Web of Science ®Google Scholar
• Stevens L. Testicular teratomas in fetal mice. J Natl Cancer Inst 1962; 28:247-67; PMID:13917068
   PubMedGoogle Scholar
• Stevens L. The biology of teratomas. Adv Morphog 1967; 6:1-31; PMID:4894128; http://dx.doi.org/10.1016/B978-1-4831-9953-5.50005-6
   PubMedGoogle Scholar
• Stevens L. Origin of testicular teratomas from primordial germ cells in mice. JNatlCancer Inst 1967; 38:549-52.
   PubMed Web of Science ®Google Scholar
• Heaney JD, Lam MY, Michelson MV, Nadeau JH. Loss of the transmembrane but not the soluble kit ligand isoform increases testicular germ cell tumor susceptibility in mice. Cancer Res 2008; 68:5193-7; PMID:18593919; http://dx.doi.org/10.1158/0008-5472.CAN-08-0779
   PubMed Web of Science ®Google Scholar
• Kimura T, Suzuki A, Fujita Y, Yomogida K, Lomeli H, Asada N, Ikeuchi M, Nagy A, Mak TW, Nakano T. Conditional loss of PTEN leads to testicular teratoma and enhances embryonic germ cell production. Development 2003; 130:1691-700; PMID:12620992; http://dx.doi.org/10.1242/dev.00392
   PubMed Web of Science ®Google Scholar
• Krentz AD, Murphy MW, Kim S, Cook MS, Capel B, Zhu R, Matin A, Sarver AL, Parker KL, Griswold MD, et al. The DM domain protein DMRT1 is a dose-sensitive regulator of fetal germ cell proliferation and pluripotency. ProcNatlAcadSciUSA 2009; 106:22323-8; http://dx.doi.org/10.1073/pnas.0905431106
   PubMed Web of Science ®Google Scholar
• Kanetsky PA, Mitra N, Vardhanabhuti S, Li M, Vaughn DJ, Letrero R, Ciosek SL, Doody DR, Smith LM, Weaver J, et al. Common variation in KITLG and at 5q31.3 predisposes to testicular germ cell cancer. NatGenet 2009; 41(7):811-5; PMID:19483682
   PubMedGoogle Scholar
• Turnbull C, Rapley EA, Seal S, Pernet D, Renwick A, Hughes D, Ricketts M, Linger R, Nsengimana J, Deloukas P, et al. Variants near DMRT1, TERT and ATF7IP are associated with testicular germ cell cancer. NatGenet 2010; 42:604-7
   Google Scholar
• Andreassen KE, Kristiansen W, Karlsson R, Aschim EL, Dahl O, Fossa SD, Adami HO, Wiklund F, Haugen TB, Grotmol T. Genetic variation in AKT1, PTEN and the 8q24 locus, and the risk of testicular germ cell tumor. HumReprod 2013; 28:1995-2002
   Google Scholar
• Noguchi T, STEVENS LC. Primordial germ cell proliferation in fetal testes in mouse strains with high and low incidences of congenital testicular teratomas. JNatlCancer Inst 1982; 69:907-13
   PubMed Web of Science ®Google Scholar
• Cook MS, Munger SC, Nadeau JH, Capel B. Regulation of male germ cell cycle arrest and differentiation by DND1 is modulated by genetic background. Development 2011; 138:23-32; PMID:21115610; http://dx.doi.org/10.1242/dev.057000
   PubMed Web of Science ®Google Scholar
• Youngren KK, Coveney D, Peng X, Bhattacharya C, Schmidt LS, Nickerson ML, Lamb BT, Deng JM, Behringer RR, Capel B, et al. The Ter mutation in the dead end gene causes germ cell loss and testicular germ cell tumours. Nature 2005; 435:360-4; PMID:15902260; http://dx.doi.org/10.1038/nature03595
   PubMed Web of Science ®Google Scholar
• Harvey M, McArthur MJ, Montgomery CA, Jr., Bradley A, Donehower LA. Genetic background alters the spectrum of tumors that develop in p53-deficient mice. FASEB J 1993; 7:938-43; PMID:8344491
   PubMed Web of Science ®Google Scholar
• Krentz AD, Murphy MW, Zhang T, Sarver AL, Jain S, Griswold MD, Bardwell VJ, Zarkower D. Interaction between DMRT1 function and genetic background modulates signaling and pluripotency to control tumor susceptibility in the fetal germ line. DevBiol 2013; 377:67-78
   Google Scholar
• Schemmer J, Arauzo-Bravo MJ, Haas N, Schafer S, Weber SN, Becker A, Eckert D, Zimmer A, Nettersheim D, Schorle H. Transcription factor TFAP2C regulates major programs required for murine fetal germ cell maintenance and haploinsufficiency predisposes to teratomas in male mice. PloS one 2013; 8:e71113; PMID:23967156; http://dx.doi.org/10.1371/journal.pone.0071113
   PubMedGoogle Scholar
• Matin A, Collin GB, Varnum DS, Nadeau JH. Testicular teratocarcinogenesis in mice-a review. APMIS 1998; 106:174-82; PMID:9524576; http://dx.doi.org/10.1111/j.1699-0463.1998.tb01333.x
   PubMed Web of Science ®Google Scholar
• Park SY, Jameson JL. Minireview: transcriptional regulation of gonadal development and differentiation. Endocrinology 2005; 146:1035-42; PMID:15604204; http://dx.doi.org/10.1210/en.2004-1454
   PubMed Web of Science ®Google Scholar
• McLaren A. Germ and somatic cell lineages in the developing gonad. MolCell Endocrinol 2000; 163:3-9; http://dx.doi.org/10.1016/S0303-7207(99)00234-8
   Web of Science ®Google Scholar
• McLaren A. Meiosis and differentiation of mouse germ cells. SympSocExpBiol 1984; 38:7-23.
   Google Scholar
• Adams IR, McLaren A. Sexually dimorphic development of mouse primordial germ cells: switching from oogenesis to spermatogenesis. Development 2002; 129:1155-64; PMID:11874911
   PubMed Web of Science ®Google Scholar
• Koubova J, Menke DB, Zhou Q, Capel B, Griswold MD, Page DC. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. ProcNatlAcadSciUSA 2006; 103:2474-9; http://dx.doi.org/10.1073/pnas.0510813103
   PubMed Web of Science ®Google Scholar
• Bowles J, Knight D, Smith C, Wilhelm D, Richman J, Mamiya S, Yashiro K, Chawengsaksophak K, Wilson MJ, Rossant J, et al. Retinoid signaling determines germ cell fate in mice. Science 2006; 312:596-600; PMID:16574820; http://dx.doi.org/10.1126/science.1125691
   PubMed Web of Science ®Google Scholar
• Lin Y, Gill ME, Koubova J, Page DC. Germ cell-intrinsic and -extrinsic factors govern meiotic initiation in mouse embryos. Science 2008; 322:1685-7; PMID:19074348; http://dx.doi.org/10.1126/science.1166340
   PubMed Web of Science ®Google Scholar
• Bowles J, Koopman P. Retinoic acid, meiosis and germ cell fate in mammals. Development 2007; 134:3401-11; PMID:17715177; http://dx.doi.org/10.1242/dev.001107
   PubMed Web of Science ®Google Scholar
• Bowles J, Feng CW, Spiller C, Davidson TL, Jackson A, Koopman P. FGF9 suppresses meiosis and promotes male germ cell fate in mice. DevCell 2010; 19:440-9
   Google Scholar
• Miles DC, Wakeling SI, Stringer JM, van den Bergen JA, Wilhelm D, Sinclair AH, Western PS. Signaling through the TGF beta-activin receptors ALK4/5/7 regulates testis formation and male germ cell development. PloS one 2013; 8:e54606; PMID:23342175; http://dx.doi.org/10.1371/journal.pone.0054606
   PubMedGoogle Scholar
• Moniot B, Ujjan S, Champagne J, Hirai H, Aritake K, Nagata K, Dubois E, Nidelet S, Nakamura M, Urade Y, et al. Prostaglandin D2 acts through the Dp2 receptor to influence male germ cell differentiation in the foetal mouse testis. Development 2014; 141:3561-71; PMID:25142465; http://dx.doi.org/10.1242/dev.103408
   PubMed Web of Science ®Google Scholar
• Yamaguchi S, Kimura H, Tada M, Nakatsuji N, Tada T. Nanog expression in mouse germ cell development. Gene ExprPatterns 2005; 5:639-46
   Web of Science ®Google Scholar
• Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17:126-40; PMID:12514105; http://dx.doi.org/10.1101/gad.224503
   PubMed Web of Science ®Google Scholar
• Pesce M, Wang X, Wolgemuth DJ, Scholer H. Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation. MechDev 1998; 71:89-98
   Google Scholar
• Western PS, Miles DC, van den Bergen JA, Burton M, Sinclair AH. Dynamic regulation of mitotic arrest in fetal male germ cells. Stem Cells 2008; 26:339-47; PMID:18024419; http://dx.doi.org/10.1634/stemcells.2007-0622
   PubMed Web of Science ®Google Scholar
• Spiller CM, Wilhelm D, Koopman P. Retinoblastoma 1 protein modulates XY germ cell entry into G1/G0 arrest during fetal development in mice. Biology of reproduction 2010; 82:433-43; PMID:19864318; http://dx.doi.org/10.1095/biolreprod.109.078691
   PubMed Web of Science ®Google Scholar
• Deshpande A, Sicinski P, Hinds PW. Cyclins and cdks in development and cancer: a perspective. Oncogene 2005; 24:2909-15; PMID:15838524; http://dx.doi.org/10.1038/sj.onc.1208618
   PubMed Web of Science ®Google Scholar
• Matin A, Collin GB, Asada Y, Varnum D, Nadeau JH. Susceptibility to testicular germ-cell tumours in a 129.MOLF-Chr 19 chromosome substitution strain. NatGenet 1999; 23:237-40.
   Google Scholar
• Heaney JD, Anderson EL, Michelson MV, Zechel JL, Conrad PA, Page DC, Nadeau JH. Germ cell pluripotency, premature differentiation and susceptibility to testicular teratomas in mice. Development 2012; 139:1577-86; PMID:22438569; http://dx.doi.org/10.1242/dev.076851
   PubMed Web of Science ®Google Scholar
• Heaney JD, Michelson MV, Youngren KK, Lam MY, Nadeau JH. Deletion of eIF2beta suppresses testicular cancer incidence and causes recessive lethality in agouti-yellow mice. HumMolGenet 2009; 18:1395-404
   Google Scholar
• Beumer TL, Roepers-Gajadien HL, Gademan IS, Kal HB, de Rooij DG. Involvement of the D-type cyclins in germ cell proliferation and differentiation in the mouse. BiolReprod 2000; 63:1893-8
   Web of Science ®Google Scholar
• Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010; 463:899-905; PMID:20164920; http://dx.doi.org/10.1038/nature08822
   PubMed Web of Science ®Google Scholar
• Fu M, Wang C, Li Z, Sakamaki T, Pestell RG. Minireview: Cyclin D1: normal and abnormal functions. Endocrinology 2004; 145:5439-47; PMID:15331580; http://dx.doi.org/10.1210/en.2004-0959
   PubMed Web of Science ®Google Scholar
• Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nature reviews Cancer 2011; 11:558-72; PMID:21734724; http://dx.doi.org/10.1038/nrc3090
   PubMed Web of Science ®Google Scholar
• Yu Q, Geng Y, Sicinski P. Specific protection against breast cancers by cyclin D1 ablation. Nature 2001; 411:1017-21; PMID:11429595; http://dx.doi.org/10.1038/35082500
   PubMed Web of Science ®Google Scholar
• Sherr CJ, Roberts JM. Living with or without cyclins and cyclin-dependent kinases. Genes Dev 2004; 18:2699-711; PMID:15545627; http://dx.doi.org/10.1101/gad.1256504
   PubMed Web of Science ®Google Scholar
• Wolgemuth DJ, Roberts SS. Regulating mitosis and meiosis in the male germ line: critical functions for cyclins. PhilosTransRSocLond B BiolSci 2010; 365:1653-62.
   Google Scholar
• Yoshimizu T, Sugiyama N, De Felice M, Yeom YI, Ohbo K, Masuko K, Obinata M, Abe K, Scholer HR, Matsui Y. Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. DevGrowth Differ 1999; 41:675-84; http://dx.doi.org/10.1046/j.1440-169x.1999.00474.x
   PubMed Web of Science ®Google Scholar
• Sicinski P, Donaher JL, Parker SB, Li T, Fazeli A, Gardner H, Haslam SZ, Bronson RT, Elledge SJ, Weinberg RA. Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 1995; 82:621-30; PMID:7664341; http://dx.doi.org/10.1016/0092-8674(95)90034-9
   PubMed Web of Science ®Google Scholar
• Schrans-Stassen BH, van de Kant HJ, de Rooij DG, van Pelt AM. Differential expression of c-kit in mouse undifferentiated and differentiating type A spermatogonia. Endocrinology 1999; 140:5894-900; PMID:10579355; http://dx.doi.org/10.1210/endo.140.12.7172
   PubMed Web of Science ®Google Scholar
• Nebel BR, Amarose AP, Hacket EM. Calendar of gametogenic development in the prepuberal male mouse. Science 1961; 134:832-3; PMID:13728067; http://dx.doi.org/10.1126/science.134.3482.832
   PubMed Web of Science ®Google Scholar
• Stevens L, Mackensen JA. Genetic and environmental influences on teratocarcinogenesis in mice. JNatlCancer Inst 1961; 27:443-53
   Google Scholar
• Singh AM, Dalton S. The cell cycle and Myc intersect with mechanisms that regulate pluripotency and reprogramming. Cell Stem Cell 2009; 5:141-9; PMID:19664987; http://dx.doi.org/10.1016/j.stem.2009.07.003
   PubMed Web of Science ®Google Scholar
• Wang Y, Blelloch R. Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res 2009; 69:4093-6; PMID:19435891; http://dx.doi.org/10.1158/0008-5472.CAN-09-0309
   PubMed Web of Science ®Google Scholar
• Filipczyk AA, Laslett AL, Mummery C, Pera MF. Differentiation is coupled to changes in the cell cycle regulatory apparatus of human embryonic stem cells. Stem Cell Res 2007; 1:45-60; PMID:19383386; http://dx.doi.org/10.1016/j.scr.2007.09.002
   PubMed Web of Science ®Google Scholar
• Herrera RE, Chen F, Weinberg RA. Increased histone H1 phosphorylation and relaxed chromatin structure in Rb-deficient fibroblasts. ProcNatlAcadSciUSA 1996; 93:11510-5; http://dx.doi.org/10.1073/pnas.93.21.11510
   PubMed Web of Science ®Google Scholar
• Mummery CL, van Rooijen MA, van den Brink SE, de Laat SW. Cell cycle analysis during retinoic acid induced differentiation of a human embryonal carcinoma-derived cell line. Cell Differ 1987; 20:153-60; PMID:3568136; http://dx.doi.org/10.1016/0045-6039(87)90429-5
   PubMedGoogle Scholar
• Jonk LJ, de Jonge ME, Kruyt FA, Mummery CL, van der Saag PT, Kruijer W. Aggregation and cell cycle dependent retinoic acid receptor mRNA expression in P19 embryonal carcinoma cells. MechDev 1992; 36:165-72.
   Google Scholar
• Western PS, Ralli RA, Wakeling SI, Lo C, van den Bergen JA, Miles DC, Sinclair AH. Mitotic arrest in teratoma susceptible fetal male germ cells. PLoSONE 2011; 6:e20736; http://dx.doi.org/10.1371/journal.pone.0020736
   Google Scholar
• Gidekel S, Pizov G, Bergman Y, Pikarsky E. Oct-3/4 is a dose-dependent oncogenic fate determinant. Cancer Cell 2003; 4:361-70; PMID:14667503; http://dx.doi.org/10.1016/S1535-6108(03)00270-8
   PubMed Web of Science ®Google Scholar
• Spiller CM, Feng CW, Jackson A, Gillis AJ, Rolland AD, Looijenga LH, Koopman P, Bowles J. Endogenous Nodal signaling regulates germ cell potency during mammalian testis development. Development 2012; 139:4123-32; PMID:23034635; http://dx.doi.org/10.1242/dev.083006
   PubMed Web of Science ®Google Scholar
• Jorgensen A, Nielsen JE, Almstrup K, Toft BG, Petersen BL, Rajpert-De Meyts E. Dysregulation of the mitosis-meiosis switch in testicular carcinoma in situ. The Journal of pathology 2013; 229:588-98; PMID:23303528; http://dx.doi.org/10.1002/path.4154
   PubMed Web of Science ®Google Scholar
• Adamah DJ, Gokhale PJ, Eastwood DJ, Rajpert De-Meyts E, Goepel J, Walsh JR, Moore HD, Andrews PW. Dysfunction of the mitotic:meiotic switch as a potential cause of neoplastic conversion of primordial germ cells. IntJAndrol 2006; 29:219-27.
   Web of Science ®Google Scholar
• Noel EE, Yeste-Velasco M, Mao X, Perry J, Kudahetti SC, Li NF, Sharp S, Chaplin T, Xue L, McIntyre A, et al. The association of CCND1 overexpression and cisplatin resistance in testicular germ cell tumors and other cancers. AmJPathol 2010; 176:2607-15.
   Google Scholar
• Freemantle SJ, Vaseva AV, Ewings KE, Bee T, Krizan KA, Kelley MR, Hattab EM, Memoli VA, Black CC, Spinella MJ, et al. Repression of cyclin D1 as a target for germ cell tumors. IntJOncol 2007; 30:333-40.
   Google Scholar
• Choi YJ, Li X, Hydbring P, Sanda T, Stefano J, Christie AL, Signoretti S, Look AT, Kung AL, von BH, et al. The requirement for cyclin D function in tumor maintenance. Cancer Cell 2012; 22:438-51; PMID:23079655; http://dx.doi.org/10.1016/j.ccr.2012.09.015
   PubMed Web of Science ®Google Scholar
• Lam MY, Youngren KK, Nadeau JH. Enhancers and suppressors of testicular cancer susceptibility in single- and double-mutant mice. Genetics 2004; 166:925-33; PMID:15020477; http://dx.doi.org/10.1534/genetics.166.2.925
   PubMed Web of Science ®Google Scholar
• Molyneaux KA, Schaible K, Wylie C. GP130, the shared receptor for the LIF/IL6 cytokine family in the mouse, is not required for early germ cell differentiation, but is required cell-autonomously in oocytes for ovulation. Development 2003; 130:4287-94; PMID:12900446; http://dx.doi.org/10.1242/dev.00650
   PubMed Web of Science ®Google Scholar
• Jeong YJ, Choi HW, Shin HS, Cui XS, Kim NH, Gerton GL, Jun JH. Optimization of real time RT-PCR methods for the analysis of gene expression in mouse eggs and preimplantation embryos. MolReprodDev 2005; 71:284-9.
   Web of Science ®Google Scholar