Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Oncology Letters
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-1074 Online ISSN: 1792-1082
Journal Cover
December-2020 Volume 20 Issue 6

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
December-2020 Volume 20 Issue 6

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

New insights into testicular granulosa cell tumors (Review)

  • Authors:
    • Xin Fang
    • Qinglei Li
  • View Affiliations / Copyright

    Affiliations: Department of Veterinary Integrative Biosciences, College of Veterinary Medicine and Biomedical Sciences, Texas A&M University, College Station, TX 77843, USA
    Copyright: © Fang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 293
    |
    Published online on: September 25, 2020
       https://doi.org/10.3892/ol.2020.12156
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Testicular granulosa cell tumors (TGCTs) are rare tumors of sex cord‑stromal origin. TGCTs are mostly benign and can be classified into the adult type and the juvenile type. Due to the rarity of clinical cases and limited research efforts, the mechanism underpinning the development of TGCTs remains poorly understood. A landmark study has identified a forkhead box L2 mutation (C134W) in nearly all adult ovarian GCTs, but its implications in TGCTs are unclear. The present study focuses on reviewing the major signaling pathways (e.g., the transforming growth factor β signaling pathway) critical for the development of TGCTs, as revealed by genetically modified mouse models, with a goal of providing new insights into the pathogenesis of TGCTs and offering directions for future studies in this area. We posit that a comparative approach between testicular and ovarian GCTs is valuable, as granulosa cells and Sertoli cells arise from the same progenitor cells during gonadal development. Developing pre‑clinical mouse models that recapitulate TGCTs will help answer the remaining questions around this type of rare tumor.
View Figures

Figure 1

Figure 2

View References

1 

Scully RE: Ovarian tumors. A review. Am J Pathol. 87:686–720. 1977.PubMed/NCBI

2 

Sakr S, Abdulfatah E, Thomas S, Al-Wahab Z, Beydoun R, Morris R, Ali-Fehmi R and Bandyopadhyay S: Granulosa cell tumors: Novel predictors of recurrence in early-stage patients. Int J Gynecol Pathol. 36:240–252. 2017. View Article : Google Scholar : PubMed/NCBI

3 

Colombo N, Parma G, Zanagnolo V and Insinga A: Management of ovarian stromal cell tumors. J Clin Oncol. 25:2944–2951. 2007. View Article : Google Scholar : PubMed/NCBI

4 

Jamieson S and Fuller PJ: Molecular pathogenesis of granulosa cell tumors of the ovary. Endocr Rev. 33:109–144. 2012. View Article : Google Scholar : PubMed/NCBI

5 

Vassal G, Flamant F, Caillaud JM, Demeocq F, Nihoul-Fekete C and Lemerle J: Juvenile granulosa cell tumor of the ovary in children: A clinical study of 15 cases. J Clin Oncol. 6:990–995. 1988. View Article : Google Scholar : PubMed/NCBI

6 

Nasu K, Fukuda J, Yoshimatsu J, Takai N, Kashima K and Narahara H: Granulosa cell tumor associated with secondary amenorrhea and serum luteinizing hormone elevation. Int J Clin Oncol. 12:228–230. 2007. View Article : Google Scholar : PubMed/NCBI

7 

Szewczuk W, Szewczuk O, Czajkowski K, Grala B and Semczuk A: Ovarian adult-type granulosa cell tumor concomitant with simple endometrial hyperplasia: A case study with selected immunohistochemistry. J Int Med Res 300060519886984. 2019.(Epub ahead of print). View Article : Google Scholar

8 

Levin G, Zigron R, Haj-Yahya R, Matan LS and Rottenstreich A: Granulosa cell tumor of ovary: A systematic review of recent evidence. Eur J Obstet Gynecol Reprod Biol. 225:57–61. 2018. View Article : Google Scholar : PubMed/NCBI

9 

Schumer ST and Cannistra SA: Granulosa cell tumor of the ovary. J Clin Oncol. 21:1180–1189. 2003. View Article : Google Scholar : PubMed/NCBI

10 

Roth LM, Lyu B and Cheng L: Perspectives on testicular sex cord-stromal tumors and those composed of both germ cells and sex cord-stromal derivatives with a comparison to corresponding ovarian neoplasms. Hum Pathol. 65:1–14. 2017. View Article : Google Scholar : PubMed/NCBI

11 

Young RH: Sex cord-stromal tumors of the ovary and testis: Their similarities and differences with consideration of selected problems. Mod Pathol. 18 (Suppl 2):S81–S98. 2005. View Article : Google Scholar : PubMed/NCBI

12 

Fang X, Ni N, Gao Y, Vincent DF, Bartholin L and Li Q: A novel mouse model of testicular granulosa cell tumors. Mol Hum Reprod. 24:343–356. 2018.PubMed/NCBI

13 

Cheng L, Albers P, Berney DM, Feldman DR, Daugaard G, Gilligan T and Looijenga LHJ: Testicular cancer. Nat Rev Dis Primers. 4:292018. View Article : Google Scholar : PubMed/NCBI

14 

Moch H, Cubilla AL, Humphrey PA, Reuter VE and Ulbright TM: The 2016 WHO classification of tumours of the urinary system and male genital organs-Part A: Renal, penile, and testicular tumours. Eur Urol. 70:93–105. 2016. View Article : Google Scholar : PubMed/NCBI

15 

Idrees MT, Ulbright TM, Oliva E, Young RH, Montironi R, Egevad L, Berney D, Srigley JR, Epstein JI and Tickoo SK; Members of the International Society of Urological Pathology Testicular Tumour Panel, : The World Health Organization 2016 classification of testicular non-germ cell tumours: A review and update from the International Society of Urological Pathology Testis Consultation Panel. Histopathology. 70:513–521. 2017. View Article : Google Scholar : PubMed/NCBI

16 

Al-Agha OM and Axiotis CA: An in-depth look at Leydig cell tumor of the testis. Arch Pathol Lab Med. 131:311–317. 2007.PubMed/NCBI

17 

Kim I, Young RH and Scully RE: Leydig cell tumors of the testis. A clinicopathological analysis of 40 cases and review of the literature. Am J Surg Pathol. 9:177–192. 1985. View Article : Google Scholar : PubMed/NCBI

18 

Boyer A, Paquet M, Lague MN, Hermo L and Boerboom D: Dysregulation of WNT/CTNNB1 and PI3K/AKT signaling in testicular stromal cells causes granulosa cell tumor of the testis. Carcinogenesis. 30:869–878. 2009. View Article : Google Scholar : PubMed/NCBI

19 

Richards JS, Fan HY, Liu Z, Tsoi M, Lague MN, Boyer A and Boerboom D: Either Kras activation or Pten loss similarly enhance the dominant-stable CTNNB1-induced genetic program to promote granulosa cell tumor development in the ovary and testis. Oncogene. 31:1504–1520. 2012. View Article : Google Scholar : PubMed/NCBI

20 

Zugor V, Labanaris AP, Witt J, Seidler A, Weingartner K and Schott GE: Congenital juvenile granulosa cell tumor of the testis in newborns. Anticancer Res. 30:1731–1734. 2010.PubMed/NCBI

21 

Kao CS, Cornejo KM, Ulbright TM and Young RH: Juvenile granulosa cell tumors of the testis: A clinicopathologic study of 70 cases with emphasis on its wide morphologic spectrum. Am J Surg Pathol. 39:1159–1169. 2015. View Article : Google Scholar : PubMed/NCBI

22 

Raju U, Fine G, Warrier R, Kini R and Weiss L: Congenital testicular juvenile granulosa cell tumor in a neonate with X/XY mosaicism. Am J Surg Pathol. 10:577–583. 1986. View Article : Google Scholar : PubMed/NCBI

23 

Young RH, Lawrence WD and Scully RE: Juvenile granulosa cell tumor-another neoplasm associated with abnormal chromosomes and ambiguous genitalia. A report of three cases. Am J Surg Pathol. 9:737–743. 1985. View Article : Google Scholar : PubMed/NCBI

24 

Wu JT, Book L and Sudar K: Serum alpha fetoprotein (AFP) levels in normal infants. Pediatr Res. 15:50–52. 1981. View Article : Google Scholar : PubMed/NCBI

25 

Dieckmann KP, Bertolini J and Wulfing C: Adult granulosa cell tumor of the testis: A case report with a review of the literature. Case Rep Urol. 2019:71561542019.PubMed/NCBI

26 

Cornejo KM and Young RH: Adult granulosa cell tumors of the testis: A report of 32 cases. Am J Surg Pathol. 38:1242–1250. 2014. View Article : Google Scholar : PubMed/NCBI

27 

Jimenez-Quintero LP, Ro JY, Zavala-Pompa A, Amin MB, Tetu B, Ordonez NG and Ayala AG: Granulosa cell tumor of the adult testis: A clinicopathologic study of seven cases and a review of the literature. Hum Pathol. 24:1120–1125. 1993. View Article : Google Scholar : PubMed/NCBI

28 

Suppiah A, Musa MM, Morgan DR and North AD: Adult granulosa cell tumour of the testis and bony metastasis. A report of the first case of granulosa cell tumour of the testicle metastasising to bone. Urol Int. 75:91–93. 2005. View Article : Google Scholar : PubMed/NCBI

29 

Hanson JA and Ambaye AB: Adult testicular granulosa cell tumor: A review of the literature for clinicopathologic predictors of malignancy. Arch Pathol Lab Med. 135:143–146. 2011.PubMed/NCBI

30 

Pisarska MD, Barlow G and Kuo FT: Minireview: Roles of the forkhead transcription factor FOXL2 in granulosa cell biology and pathology. Endocrinology. 152:1199–1208. 2011. View Article : Google Scholar : PubMed/NCBI

31 

Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R, Kress J, Treier AC, Klugmann C, Klasen C, Holter NI, et al: Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell. 139:1130–1142. 2009. View Article : Google Scholar : PubMed/NCBI

32 

Kalfa N, Fellous M, Boizet-Bonhoure B, Patte C, Duvillard P, Pienkowski C, Jaubert F, Ecochard A and Sultan C: Aberrant expression of ovary determining gene FOXL2 in the testis and juvenile granulosa cell tumor in children. J Urol. 180 (Suppl 4):S1810–S1813. 2008. View Article : Google Scholar

33 

Shah SP, Kobel M, Senz J, Morin RD, Clarke BA, Wiegand KC, Leung G, Zayed A, Mehl E, Kalloger SE, et al: Mutation of FOXL2 in granulosa-cell tumors of the ovary. N Engl J Med. 360:2719–2729. 2009. View Article : Google Scholar : PubMed/NCBI

34 

Nonis D, McTavish KJ and Shimasaki S: Essential but differential role of FOXL2wt and FOXL2C134W in GDF-9 stimulation of follistatin transcription in co-operation with Smad3 in the human granulosa cell line COV434. Mol Cell Endocrinol. 372:42–48. 2013. View Article : Google Scholar : PubMed/NCBI

35 

Cheng JC, Chang HM, Qiu X, Fang L and Leung PC: FOXL2-induced follistatin attenuates activin A-stimulated cell proliferation in human granulosa cell tumors. Biochem Biophys Res Commun. 443:537–542. 2014. View Article : Google Scholar : PubMed/NCBI

36 

Leung DTH, Fuller PJ and Chu S: Impact of FOXL2 mutations on signaling in ovarian granulosa cell tumors. Int J Biochem Cell Biol. 72:51–54. 2016. View Article : Google Scholar : PubMed/NCBI

37 

Kim JH, Yoon S, Park M, Park HO, Ko JJ, Lee K and Bae J: Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (C134W). Oncogene. 30:1653–1663. 2011. View Article : Google Scholar : PubMed/NCBI

38 

Fleming NI, Knower KC, Lazarus KA, Fuller PJ, Simpson ER and Clyne CD: Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter. PLoS One. 5:e143892010. View Article : Google Scholar : PubMed/NCBI

39 

Lima JF, Jin L, de Araujo AR, Erikson-Johnson MR, Oliveira AM, Sebo TJ, Keeney GL and Medeiros F: FOXL2 mutations in granulosa cell tumors occurring in males. Arch Pathol Lab Med. 136:825–828. 2012. View Article : Google Scholar : PubMed/NCBI

40 

Fuller PJ, Chu S, Fikret S and Burger HG: Molecular pathogenesis of granulosa cell tumours. Mol Cell Endocrinol. 191:89–96. 2002. View Article : Google Scholar : PubMed/NCBI

41 

Kim SY: Insights into granulosa cell tumors using spontaneous or genetically engineered mouse models. Clin Exp Reprod Med. 43:1–8. 2016. View Article : Google Scholar : PubMed/NCBI

42 

Matzuk MM, Finegold MJ, Su JG, Hsueh AJ and Bradley A: Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature. 360:313–319. 1992. View Article : Google Scholar : PubMed/NCBI

43 

Li Y, Zhang L, Hu Y, Chen M, Han F, Qin Y, Chen M, Cui X, Duo S, Tang F and Gao F: β-Catenin directs the transformation of testis Sertoli cells to ovarian granulosa-like cells by inducing Foxl2 expression. J Biol Chem. 292:17577–17586. 2017. View Article : Google Scholar : PubMed/NCBI

44 

Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, et al: Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol. 28:248–257. 2008. View Article : Google Scholar : PubMed/NCBI

45 

Ying SY: Inhibins, activins, and follistatins: Gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocr Rev. 9:267–293. 1988. View Article : Google Scholar : PubMed/NCBI

46 

O'Connor AE and De Kretser DM: Inhibins in normal male physiology. Semin Reprod Med. 22:177–185. 2004. View Article : Google Scholar : PubMed/NCBI

47 

Kumar TR, Wang Y and Matzuk MM: Gonadotropins are essential modifier factors for gonadal tumor development in inhibin-deficient mice. Endocrinology. 137:4210–4216. 1996. View Article : Google Scholar : PubMed/NCBI

48 

Cipriano SC, Chen L, Burns KH, Koff A and Matzuk MM: Inhibin and p27 interact to regulate gonadal tumorigenesis. Mol Endocrinol. 15:985–996. 2001. View Article : Google Scholar : PubMed/NCBI

49 

Burns KH, Agno JE, Sicinski P and Matzuk MM: Cyclin D2 and p27 are tissue-specific regulators of tumorigenesis in inhibin alpha knockout mice. Mol Endocrinol. 17:2053–2069. 2003. View Article : Google Scholar : PubMed/NCBI

50 

Li Q, Graff JM, O'Connor AE, Loveland KL and Matzuk MM: SMAD3 regulates gonadal tumorigenesis. Mol Endocrinol. 21:2472–2486. 2007. View Article : Google Scholar : PubMed/NCBI

51 

Klaus A and Birchmeier W: Wnt signalling and its impact on development and cancer. Nat Rev Cancer. 8:387–398. 2008. View Article : Google Scholar : PubMed/NCBI

52 

Boerboom D, Paquet M, Hsieh M, Liu J, Jamin SP, Behringer RR, Sirois J, Taketo MM and Richards JS: Misregulated Wnt/beta-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Res. 65:9206–9215. 2005. View Article : Google Scholar : PubMed/NCBI

53 

Mitsiades CS, Mitsiades N and Koutsilieris M: The Akt pathway: Molecular targets for anti-cancer drug development. Curr Cancer Drug Targets. 4:235–256. 2004. View Article : Google Scholar : PubMed/NCBI

54 

Hay N: The Akt-mTOR tango and its relevance to cancer. Cancer Cell. 8:179–183. 2005. View Article : Google Scholar : PubMed/NCBI

55 

Haigis KM: KRAS alleles: The devil is in the detail. Trends Cancer. 3:686–697. 2017. View Article : Google Scholar : PubMed/NCBI

56 

Fan HY, Shimada M, Liu Z, Cahill N, Noma N, Wu Y, Gossen J and Richards JS: Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development. 135:2127–2137. 2008. View Article : Google Scholar : PubMed/NCBI

57 

Hannenhalli S and Kaestner KH: The evolution of Fox genes and their role in development and disease. Nat Rev Genet. 10:233–240. 2009. View Article : Google Scholar : PubMed/NCBI

58 

Uhlenhaut NH and Treier M: Forkhead transcription factors in ovarian function. Reproduction. 142:489–495. 2011. View Article : Google Scholar : PubMed/NCBI

59 

Belli M, Secchi C, Stupack D and Shimasaki S: FOXO1 negates the cooperative action of FOXL2C134W and SMAD3 in CYP19 expression in HGrC1 cells by sequestering SMAD3. J Endocr Soc. 3:2064–2081. 2019. View Article : Google Scholar : PubMed/NCBI

60 

Liu Z, Ren YA, Pangas SA, Adams J, Zhou W, Castrillon DH, Wilhelm D and Richards JS: FOXO1/3 and PTEN depletion in granulosa cells promotes ovarian granulosa cell tumor development. Mol Endocrinol. 29:1006–1024. 2015. View Article : Google Scholar : PubMed/NCBI

61 

Massague J: TGF-beta signal transduction. Annu Rev Biochem. 67:753–791. 1998. View Article : Google Scholar : PubMed/NCBI

62 

Fang X, Gao Y and Li Q: SMAD3 activation: A converging point of dysregulated TGF-Beta superfamily signaling and genetic aberrations in granulosa cell tumor development? Biol Reprod. 95:1052016. View Article : Google Scholar : PubMed/NCBI

63 

Massague J: TGFbeta in cancer. Cell. 134:215–230. 2008. View Article : Google Scholar : PubMed/NCBI

64 

Gao Y, Vincent DF, Davis AJ, Sansom OJ, Bartholin L and Li Q: Constitutively active transforming growth factor β receptor 1 in the mouse ovary promotes tumorigenesis. Oncotarget. 7:40904–40918. 2016. View Article : Google Scholar : PubMed/NCBI

65 

Boyer A, Hermo L, Paquet M, Robaire B and Boerboom D: Seminiferous tubule degeneration and infertility in mice with sustained activation of WNT/CTNNB1 signaling in sertoli cells. Biol Reprod. 79:475–485. 2008. View Article : Google Scholar : PubMed/NCBI

66 

Jamin SP, Arango NA, Mishina Y, Hanks MC and Behringer RR: Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet. 32:408–410. 2002. View Article : Google Scholar : PubMed/NCBI

67 

Tanwar PS, Kaneko-Tarui T, Zhang L, Rani P, Taketo MM and Teixeira J: Constitutive WNT/beta-catenin signaling in murine Sertoli cells disrupts their differentiation and ability to support spermatogenesis. Biol Reprod. 82:422–432. 2010. View Article : Google Scholar : PubMed/NCBI

68 

Albrecht KH and Eicher EM: Evidence that Sry is expressed in pre-Sertoli cells and Sertoli and granulosa cells have a common precursor. Dev Biol. 240:92–107. 2001. View Article : Google Scholar : PubMed/NCBI

69 

Muzumdar MD, Tasic B, Miyamichi K, Li L and Luo L: A global double-fluorescent Cre reporter mouse. Genesis. 45:593–605. 2007. View Article : Google Scholar : PubMed/NCBI

70 

Snyder CS, Harrington AR, Kaushal S, Mose E, Lowy AM, Hoffman RM and Bouvet M: A dual-color genetically engineered mouse model for multispectral imaging of the pancreatic microenvironment. Pancreas. 42:952–958. 2013. View Article : Google Scholar : PubMed/NCBI

71 

Gammon K: Mathematical modelling: Forecasting cancer. Nature. 491:S66–S67. 2012. View Article : Google Scholar : PubMed/NCBI

72 

Beerenwinkel N, Schwarz RF, Gerstung M and Markowetz F: Cancer evolution: Mathematical models and computational inference. Syst Biol. 64:e1–e25. 2015. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Fang X and Li Q: New insights into testicular granulosa cell tumors (Review). Oncol Lett 20: 293, 2020.
APA
Fang, X., & Li, Q. (2020). New insights into testicular granulosa cell tumors (Review). Oncology Letters, 20, 293. https://doi.org/10.3892/ol.2020.12156
MLA
Fang, X., Li, Q."New insights into testicular granulosa cell tumors (Review)". Oncology Letters 20.6 (2020): 293.
Chicago
Fang, X., Li, Q."New insights into testicular granulosa cell tumors (Review)". Oncology Letters 20, no. 6 (2020): 293. https://doi.org/10.3892/ol.2020.12156
Copy and paste a formatted citation
x
Spandidos Publications style
Fang X and Li Q: New insights into testicular granulosa cell tumors (Review). Oncol Lett 20: 293, 2020.
APA
Fang, X., & Li, Q. (2020). New insights into testicular granulosa cell tumors (Review). Oncology Letters, 20, 293. https://doi.org/10.3892/ol.2020.12156
MLA
Fang, X., Li, Q."New insights into testicular granulosa cell tumors (Review)". Oncology Letters 20.6 (2020): 293.
Chicago
Fang, X., Li, Q."New insights into testicular granulosa cell tumors (Review)". Oncology Letters 20, no. 6 (2020): 293. https://doi.org/10.3892/ol.2020.12156
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team