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
Molecular Medicine Reports
Join Editorial Board Propose a Special Issue
Print ISSN: 1791-2997 Online ISSN: 1791-3004
Journal Cover
March-2019 Volume 19 Issue 3

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
March-2019 Volume 19 Issue 3

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
Article Open Access

ATP synthase is required for male fertility and germ cell maturation in Drosophila testes

  • Authors:
    • Jun Yu
    • Binghai Chen
    • Bo Zheng
    • Chen Qiao
    • Xia Chen
    • Yidan Yan
    • Xiaojin Luan
    • Bing Xie
    • Jiajia Liu
    • Cong Shen
    • Zeyu He
    • Xing Hu
    • Mingxi Liu
    • Hong Li
    • Qixiang Shao
    • Jie Fang
  • View Affiliations / Copyright

    Affiliations: Department of Gynecology, Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 212001, P.R. China, Department of Urology, Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 21200, P.R. China, Department of Histology and Embryology, State Key Laboratory of Reproductive Medicine, Nanjing Medical University, Nanjing, Jiangsu 211166, P.R. China, Department of Clinical Pharmacy, Affiliated Hospital of Jiangsu University, Zhenjiang, Jiangsu 212001, P.R. China, Center for Reproduction and Genetics, Suzhou Municipal Hospital, Nanjing Medical University Affiliated Suzhou Hospital, Suzhou, Jiangsu 215002, P.R. China, Department of Clinical Medicine, China Medical University, Shenyang, Liaoning 110001, P.R. China, Reproductive Sciences Institute of Jiangsu University, Zhenjiang, Jiangsu 212001, P.R. China
    Copyright: © Yu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 1561-1570
    |
    Published online on: January 8, 2019
       https://doi.org/10.3892/mmr.2019.9834
  • 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

Germ cell maturation is essential for spermatogenesis and testis homeostasis. ATP synthase serves significant roles in energy storage in germ cell survival and is catalyzed by alterations in the mitochondrial membrane proton concentration. The intrinsic cellular mechanisms governing stem cell maturation remain largely unknown. In the present study, in vivo RNA interference (RNAi) screening of major ATP synthase subunits was performed, and the function of ATP synthase for male fertility and spermatogenesis in Drosophila was explored. A Upstream Activation Sequence/Gal4 transcription factor system was used to knock down gene expression in specific cell types, and immunofluorescence staining was conducted to assess the roles of ATP synthase subunits in Drosophila testes. It was identified that knockdown of ATP synthase resulted in male infertility and abnormal spermatogenesis in Drosophila testes. In addition, knockdown of the ATP synthase β subunit in germ cells resulted in defects in male infertility and germ cell maturation, while the hub and cyst cell populations were maintained. Other major ATP synthase subunits were also examined and similar phenotypes in Drosophila testes were identified. Taken together, the data from the present study revealed that ATP synthase serves important roles for male fertility during spermatogenesis by regulating germ cell maturation in Drosophila testes.
View Figures

Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

View References

1 

Hu Z, Li Z, Yu J, Tong C, Lin Y, Guo X, Lu F, Dong J, Xia Y, Wen Y, et al: Association analysis identifies new risk loci for non-obstructive azoospermia in Chinese men. Nat Commun. 5:38572014. View Article : Google Scholar : PubMed/NCBI

2 

Yu J, Liu Y, Lan X, Wu H, Wen Y, Zhou Z, Hu Z, Sha J, Guo X and Tong C: CHES-1-like, the ortholog of a non-obstructive azoospermia-associated gene, blocks germline stem cell differentiation by upregulating Dpp expression in Drosophila testis. Oncotarget. 7:42303–42313. 2016.PubMed/NCBI

3 

Yu J, Wu H, Wen Y, Liu Y, Zhou T, Ni B, Lin Y, Dong J, Zhou Z, Hu Z, et al: Identification of seven genes essential for male fertility through a genome-wide association study of non-obstructive azoospermia and RNA interference-mediated large-scale functional screening in Drosophila. Hum Mol Genet. 24:1493–1503. 2015. View Article : Google Scholar : PubMed/NCBI

4 

Wu H, Sun L, Wen Y, Liu Y, Yu J, Mao F, Wang Y, Tong C, Guo X, Hu Z, et al: Major spliceosome defects cause male infertility and are associated with nonobstructive azoospermia in humans. Proc Natl Acad Sci USA. 113:4134–4139. 2016. View Article : Google Scholar : PubMed/NCBI

5 

Hackstein JH, Hochstenbach R and Pearson PL: Towards an understanding of the genetics of human male infertility: Lessons from flies. Trends Genet. 16:565–572. 2000. View Article : Google Scholar : PubMed/NCBI

6 

de Cuevas M and Matunis EL: The stem cell niche: Lessons from the Drosophila testis. Development. 138:2861–2869. 2011. View Article : Google Scholar : PubMed/NCBI

7 

Spradling A, Fuller MT, Braun RE and Yoshida S: Germline stem cells. Cold Spring Harb Perspect Biol. 3:a0026422011. View Article : Google Scholar : PubMed/NCBI

8 

Fuller MT and Spradling AC: Male and female Drosophila germline stem cells: Two versions of immortality. Science. 316:402–404. 2007. View Article : Google Scholar : PubMed/NCBI

9 

Xu EY, Lee DF, Klebes A, Turek PJ, Kornberg TB and Reijo Pera RA: Human BOULE gene rescues meiotic defects in infertile flies. Hum Mol Genet. 12:169–175. 2003. View Article : Google Scholar : PubMed/NCBI

10 

White-Cooper H: Studying how flies make sperm-investigating gene function in Drosophila testes. Mol Cell Endocrinol. 306:66–74. 2009. View Article : Google Scholar : PubMed/NCBI

11 

Yu J, Lan X, Chen X, Yu C, Xu Y, Liu Y, Xu L, Fan HY and Tong C: Protein synthesis and degradation are essential to regulate germline stem cell homeostasis in Drosophila testes. Development. 143:2930–2945. 2016. View Article : Google Scholar : PubMed/NCBI

12 

He J, Ford HC, Carroll J, Ding S, Fearnley IM and Walker J: Persistence of the mitochondrial permeability transition in the absence of subunit c of human ATP synthase. Proc Natl Acad Sci USA. 114:3409–3414. 2017. View Article : Google Scholar : PubMed/NCBI

13 

Junge W and Nelson N: ATP synthase. Annu Rev Biochem. 84:631–657. 2015. View Article : Google Scholar : PubMed/NCBI

14 

Walker JE: The ATP synthase: The understood, the uncertain and the unknown. Biochem Soc Trans. 41:1–16. 2013. View Article : Google Scholar : PubMed/NCBI

15 

Mitchell P: Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. 1966. Biochim Biophys Acta 1807. 1507–1538. 2011.

16 

Kucharczyk R, Zick M, Bietenhader M, Rak M, Couplan E, Blondel M, Caubet SD and di Rago JP: Mitochondrial ATP synthase disorders: Molecular mechanisms and the quest for curative therapeutic approaches. Biochim Biophys Acta 1793. 186–199. 2009.

17 

Velours J, Paumard P, Soubannier V, Spannagel C, Vaillier J, Arselin G and Graves PV: Organisation of the yeast ATP synthase F(0): A study based on cysteine mutants, thiol modification and cross-linking reagents. Biochim Biophys Acta 1458. 443–456. 2000.

18 

Hendriks WK, Colleoni S, Galli C, Paris DB, Colenbrander B, Roelen BA and Stout TA: Maternal age and in vitro culture affect mitochondrial number and function in equine oocytes and embryos. Reprod Fertil Dev. 27:957–968. 2015. View Article : Google Scholar : PubMed/NCBI

19 

Sawyer EM, Brunner EC, Hwang Y, Ivey LE, Brown O, Bannon M, Akrobetu D, Sheaffer KE, Morgan O, Field CO, et al: Testis-specific ATP synthase peripheral stalk subunits required for tissue-specific mitochondrial morphogenesis in Drosophila. BMC Cell Biol. 18:162017. View Article : Google Scholar : PubMed/NCBI

20 

Ramió-Lluch L, Yeste M, Fernández-Novell JM, Estrada E, Rocha L, Cebrián-Pérez JA, Muiño-Blanco T, Concha II, Ramírez A and Rodríguez-Gil JE: Oligomycin A-induced inhibition of mitochondrial ATP-synthase activity suppresses boar sperm motility and in vitro capacitation achievement without modifying overall sperm energy levels. Reprod Fertil Dev. 26:883–897. 2014. View Article : Google Scholar : PubMed/NCBI

21 

Maccarinelli F, Regoni M, Carmona F, Poli M, Meyron-Holtz EG and Arosio P: Mitochondrial ferritin deficiency reduces male fertility in mice. Reprod Fertil Dev. 29:2005–2010. 2017. View Article : Google Scholar : PubMed/NCBI

22 

Teixeira FK, Sanchez CG, Hurd TR, Seifert JR, Czech B, Preall JB, Hannon GJ and Lehmann R: ATP synthase promotes germ cell differentiation independent of oxidative phosphorylation. Nat Cell Biol. 17:689–696. 2015. View Article : Google Scholar : PubMed/NCBI

23 

Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, Shim HS, Tao R, Handler D, Karpowicz P, et al: A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 8:405–407. 2011. View Article : Google Scholar : PubMed/NCBI

24 

Liu M, Lim TM and Cai Y: The Drosophila female germline stem cell lineage acts to spatially restrict DPP function within the niche. Sci Signal. 3:ra572010. View Article : Google Scholar : PubMed/NCBI

25 

White-Cooper H: Tissue, cell type and stage-specific ectopic gene expression and RNAi induction in the Drosophila testis. Spermatogenesis. 2:11–22. 2012. View Article : Google Scholar : PubMed/NCBI

26 

Singh SR, Zhen W, Zheng Z, Wang H, Oh SW, Liu W, Zbar B, Schmidt LS and Hou SX: The Drosophila homolog of the human tumor suppressor gene BHD interacts with the JAK-STAT and Dpp signaling pathways in regulating male germline stem cell maintenance. Oncogene. 25:5933–5941. 2006. View Article : Google Scholar : PubMed/NCBI

27 

Huang da W, Sherman BT and Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 4:44–57. 2009. View Article : Google Scholar : PubMed/NCBI

28 

Huang da W, Sherman BT and Lempicki RA: Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37:1–13. 2009. View Article : Google Scholar : PubMed/NCBI

29 

Furuya M, Qadota H, Chisholm AD and Sugimoto A: The C. elegans eyes absent ortholog EYA-1 is required for tissue differentiation and plays partially redundant roles with PAX-6. Dev Biol. 286:452–463. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Karandikar UC, Jin M, Jusiak B, Kwak S, Chen R and Mardon G: Drosophila eyes absent is required for normal cone and pigment cell development. PLoS One. 9:e1021432014. View Article : Google Scholar : PubMed/NCBI

31 

Fabrizio JJ, Boyle M and DiNardo S: A somatic role for eyes absent (eya) and sine oculis (so) in Drosophila spermatocyte development. Dev Biol. 258:117–128. 2003. View Article : Google Scholar : PubMed/NCBI

32 

Bunt SM and Hime GR: Ectopic activation of Dpp signalling in the male Drosophila germline inhibits germ cell differentiation. Genesis. 39:84–93. 2004. View Article : Google Scholar : PubMed/NCBI

33 

Shivdasani AA and Ingham PW: Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-beta signaling in Drosophila spermatogenesis. Curr Biol. 13:2065–2072. 2003. View Article : Google Scholar : PubMed/NCBI

34 

Yan D, Neumüller RA, Buckner M, Ayers K, Li H, Hu Y, Yang-Zhou D, Pan L, Wang X, Kelley C, et al: A regulatory network of Drosophila germline stem cell self-renewal. Dev Cell. 28:459–473. 2014. View Article : Google Scholar : PubMed/NCBI

35 

Chen JV and Megraw TL: Spermitin: A novel mitochondrial protein in Drosophila spermatids. PLoS One. 9:e1088022014. View Article : Google Scholar : PubMed/NCBI

36 

Wu CH, Zong Q, Du AL, Zhang W, Yao HC, Yu XQ and Wang YF: Knockdown of Dynamitin in testes significantly decreased male fertility in Drosophila melanogaster. Dev Biol. 420:79–89. 2016. View Article : Google Scholar : PubMed/NCBI

37 

Collins CM, Malacrida B, Burke C, Kiely PA and Dunleavy EM: ATP synthase F1 subunits recruited to centromeres by CENP-A are required for male meiosis. Nat Commun. 9:27022018. View Article : Google Scholar : PubMed/NCBI

38 

Midzak AS, Chen H, Aon MA, Papadopoulos V and Zirkin BR: ATP synthesis, mitochondrial function, and steroid biosynthesis in rodent primary and tumor Leydig cells. Biol Reprod. 84:976–985. 2011. View Article : Google Scholar : PubMed/NCBI

39 

Wen J, Duan H, Bejarano F, Okamura K, Fabian L, Brill JA, Bortolamiol-Becet D, Martin R, Ruby JG and Lai EC: Adaptive regulation of testis gene expression and control of male fertility by the Drosophila hairpin RNA pathway. Mol Cell. 57:165–178. 2015. View Article : Google Scholar : PubMed/NCBI

40 

Kawasaki I, Hanazawa M, Gengyo-Ando K, Mitani S, Maruyama I and Iino Y: ASB-1, a germline-specific isoform of mitochondrial ATP synthase b subunit, is required to maintain the rate of germline development in Caenorhabditis elegans. Mech Dev. 124:237–251. 2007. View Article : Google Scholar : PubMed/NCBI

41 

Chen YN, Wu CH, Zheng Y, Li JJ, Wang JL and Wang YF: Knockdown of ATPsyn-b caused larval growth defect and male infertility in Drosophila. Arch Insect Biochem Physiol. 88:144–54. 2015. View Article : Google Scholar : PubMed/NCBI

42 

Davies KM, Anselmi C, Wittig I, Faraldo-Gómez JD and Kühlbrandt W: Structure of the yeast F1FO-ATP synthase dimer and its role in shaping the mitochondrial cristae. Proc Natl Acad Sci USA. 109:13602–13607. 2012. View Article : Google Scholar : PubMed/NCBI

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Yu J, Chen B, Zheng B, Qiao C, Chen X, Yan Y, Luan X, Xie B, Liu J, Shen C, Shen C, et al: ATP synthase is required for male fertility and germ cell maturation in Drosophila testes. Mol Med Rep 19: 1561-1570, 2019.
APA
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y. ... Fang, J. (2019). ATP synthase is required for male fertility and germ cell maturation in Drosophila testes. Molecular Medicine Reports, 19, 1561-1570. https://doi.org/10.3892/mmr.2019.9834
MLA
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y., Luan, X., Xie, B., Liu, J., Shen, C., He, Z., Hu, X., Liu, M., Li, H., Shao, Q., Fang, J."ATP synthase is required for male fertility and germ cell maturation in Drosophila testes". Molecular Medicine Reports 19.3 (2019): 1561-1570.
Chicago
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y., Luan, X., Xie, B., Liu, J., Shen, C., He, Z., Hu, X., Liu, M., Li, H., Shao, Q., Fang, J."ATP synthase is required for male fertility and germ cell maturation in Drosophila testes". Molecular Medicine Reports 19, no. 3 (2019): 1561-1570. https://doi.org/10.3892/mmr.2019.9834
Copy and paste a formatted citation
x
Spandidos Publications style
Yu J, Chen B, Zheng B, Qiao C, Chen X, Yan Y, Luan X, Xie B, Liu J, Shen C, Shen C, et al: ATP synthase is required for male fertility and germ cell maturation in Drosophila testes. Mol Med Rep 19: 1561-1570, 2019.
APA
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y. ... Fang, J. (2019). ATP synthase is required for male fertility and germ cell maturation in Drosophila testes. Molecular Medicine Reports, 19, 1561-1570. https://doi.org/10.3892/mmr.2019.9834
MLA
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y., Luan, X., Xie, B., Liu, J., Shen, C., He, Z., Hu, X., Liu, M., Li, H., Shao, Q., Fang, J."ATP synthase is required for male fertility and germ cell maturation in Drosophila testes". Molecular Medicine Reports 19.3 (2019): 1561-1570.
Chicago
Yu, J., Chen, B., Zheng, B., Qiao, C., Chen, X., Yan, Y., Luan, X., Xie, B., Liu, J., Shen, C., He, Z., Hu, X., Liu, M., Li, H., Shao, Q., Fang, J."ATP synthase is required for male fertility and germ cell maturation in Drosophila testes". Molecular Medicine Reports 19, no. 3 (2019): 1561-1570. https://doi.org/10.3892/mmr.2019.9834
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