Asprosin regulates male reproduction in teleosts: an in vitro study in Channa punctata

in Journal of Endocrinology
Authors:
Priyanka Sathoria Department of Zoology, Maitreyi College, University of Delhi, Delhi, India

Search for other papers by Priyanka Sathoria in
Current site
Google Scholar
PubMed Close
,
Bhawna Chuphal Department of Zoology, Miranda House, University of Delhi, Delhi, India

Search for other papers by Bhawna Chuphal in
Current site
Google Scholar
PubMed Close
,
Umesh Rai University of Jammu, Jammu, Jammu and Kashmir, India

Search for other papers by Umesh Rai in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0002-2684-4311
, and
Brototi Roy Department of Zoology, Maitreyi College, University of Delhi, Delhi, India

Search for other papers by Brototi Roy in
Current site
Google Scholar
PubMed Close
https://orcid.org/0000-0001-9140-4032

Correspondence should be addressed to B Roy or U Rai: broy@maitreyi.du.ac.in or rai_u@rediffmail.com
DOI:
https://doi.org/10.1530/JOE-24-0146
Volume/Issue:
Volume 263: Issue 3
Article Type:
Research Article
Article ID:
e240146
Online Publication Date:
29 Oct 2024
Copyright:
© the author(s) 2024
Restricted access
Rent on DeepDyve

Sign up for journal news

The novel adipokine asprosin, produced by the furin enzymatic cleavage of profibrillin 1 protein (encoded by the Fbn1 gene), is implicated in regulating many physiological functions, including reproduction in mammals. In males, asprosin is reported to increase sperm density, sperm motility, and steroid production by interacting with Olfr734, which belongs to the G-protein-coupled receptor family (GPCR). In 2023, our group predicted and characterized asprosin in silico for the first time and demonstrated the robust expression of fbn1, and furin in the gonads of teleost spotted snakehead (ss) Channa punctata. Taking it forward, in the current study, we have investigated the effect of asprosin on the testicular functions of the spotted snakehead. As C. punctata is a seasonal breeder, the reproductive-phase-dependent expression of fbn1 in the testis was analyzed, showing significant upregulation during the preparatory and post-spawning phases. Additionally, bacterially overexpressed recombinant asprosin of C. punctata was purified to study the effect of ss asprosin on gametogenesis and steroidogenesis. Ex vivo treatment with recombinant asprosin resulted in significant upregulation of spermatogenic marker genes pcna, aldh1a2, cyp26a1, and sycp3. Asprosin also enhanced the gene expression of gonadotropin receptors, as well as sex steroid receptors, in addition to steroidogenic genes star and cyp17a1. Further exploring the downstream signaling cascade, the second messenger of GPCRs, cAMP levels following asprosin treatment were analyzed. Asprosin treatment prominently enhanced cAMP levels, thereby indicating the involvement of GPCR in the transduction of asprosin action. Hence, the study elucidates the regulation of male reproductive function by asprosin in spotted snakeheads.

Journal of Endocrinology is committed to supporting researchers in demonstrating the impact of their articles published in the journal.

The two types of article metrics we measure are (i) more traditional full-text views and pdf downloads, and (ii) Altmetric data, which shows the wider impact of articles in a range of non-traditional sources, such as social media.

More information is on the Reasons to publish page.

Sept 2018 onwards Past Year Past 30 Days
Full Text Views 118 118 32
PDF Downloads 124 124 29

 

  • Collapse
  • Expand
Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© the author(s) 2024
Article ID:
e240146
Article Type:
Research Article
Received Date:
14 May 2024
Accepted Date:
20 Sep 2024
Print Publication Date:
01 Dec 2024
Online Publication Date:
29 Oct 2024
Keywords:
asprosin; reproduction; spermatogenesis; steroidogenesis; teleost

  • Basak R, Roy A & & Rai U 2016 Seasonality of reproduction in male spotted murrel Channa punctatus: correlation of environmental variables and plasma sex steroids with histological changes in testis. Fish Physiology and Biochemistry 42 1249–1258. (https://doi.org/10.1007/s10695-016-0214-6)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Basak R, Roy A & & Rai U 2018 In silico analysis, temporal expression and gonadotropic regulation of receptors for follicle‐stimulating hormone and luteinizing hormone in testis of spotted snakehead Channa punctata. Journal of Fish Biology 93 53–71. (https://doi.org/10.1111/jfb.13727)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Batalha IM, Maylem ER, Spicer LJ, Bello CA, Archilia EC & & Schütz LF 2023 Effects of asprosin on estradiol and progesterone secretion and proliferation of bovine granulosa cells. Molecular and Cellular Endocrinology 565 111890. (https://doi.org/10.1016/j.mce.2023.111890)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chuphal B, Sathoria P, Rai U & & Roy B 2024a Sexual dimorphism in NLR transcripts and its downstream signaling protein IL-1β in teleost Channa punctata (Bloch, 1793). Scientific Reports 14 1923. (https://doi.org/10.1038/s41598-024-51702-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chuphal B, Rai U & & Roy B 2024b Exploring the possible role of estradiol in the regulation of reproductive phase-dependent expression of NOD-like receptors in female Channa punctata. Aquaculture International 32 709–724. (https://doi.org/10.1007/s10499-023-01184-7)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Du Sert NP, Ahluwalia A, Alam S, Avey MT, Baker M, Browne WJ, Clark A, Cuthill IC, Dirnagl U, Emerson M, et al.2020 Reporting animal research: explanation and elaboration for the ARRIVE Guidelines 2.0. PLoS Biology 18 e3000411. (https://doi.org/10.1371/journal.pbio.3000411)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Farrag M, Ait Eldjoudi D, González-Rodríguez M, Cordero-Barreal A, Ruiz-Fernandez C, Capuozzo M, Gonzalez-Gay MA, Mera A, Lago F, Soffar A, et al.2023 Asprosin in health and disease, a new glucose sensor with central and peripheral metabolic effects. Frontiers in Endocrinology 13 1101091. (https://doi.org/10.3389/fendo.2022.1101091)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Feng R, Fang L, Cheng Y, He X, Jiang W, Dong R, Shi H, Jiang D, Sun L & & Wang D 2015 Retinoic acid homeostasis through aldh1a2 and cyp26a1 mediates meiotic entry in Nile tilapia (Oreochromis niloticus). Scientific Reports 5 10131. (https://doi.org/10.1038/srep10131)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • García-Lopez A, Bogerd J, Granneman JC, van Dijk W, Trant JM, Taranger GL & & Schulz RW 2009 Leydig cells express follicle-stimulating hormone receptors in African catfish. Endocrinology 150 357–365. (https://doi.org/10.1210/en.2008-0447)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ikeuchi T, Todo T, Kobayashi T & & Nagahama Y 2001 Two subtypes of androgen and progestogen receptors in fish testes. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 129 449–455. (https://doi.org/10.1016/S1096-4959(0100375-X)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Keskin T, Erden Y & & Tekin S 2021 Intracerebroventricular asprosin administration strongly stimulates hypothalamic-pituitary-testicular axis in rats. Molecular and Cellular Endocrinology 538 111451. (https://doi.org/10.1016/j.mce.2021.111451)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kim JE, Kim JS, Jo MJ, Cho E, Ahn SY, Kwon YJ & & Ko GJ 2022 The roles and associated mechanisms of adipokines in development of metabolic syndrome. Molecules 27 334. (https://doi.org/10.3390/molecules27020334)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Labrie F, Luu-The V, Lin SX, Labrie C, Simard J, Breton R & & Bélanger A 1997 The key role of 17β-hydroxysteroid dehydrogenases in sex steroid biology. Steroids 62 148–158. (https://doi.org/10.1016/S0039-128X(9600174-2)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lee T, Yun S, Jeong JH & & Jung TW 2019 Asprosin impairs insulin secretion in response to glucose and viability through TLR4/JNK-mediated inflammation. Molecular and Cellular Endocrinology 486 96–104. (https://doi.org/10.1016/j.mce.2019.03.001)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Livak KJ & & Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25 402–408. (https://doi.org/10.1006/meth.2001.1262)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maurya S, Krishna A, Lal B & & Singh A 2022 Asprosin promotes steroidogenesis and spermatogenesis with improved glucose metabolism in adult mice testis. Andrologia 54 e14579. (https://doi.org/10.1111/and.14579)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maylem ER, Spicer LJ, Atabay EP, Atabay EC, Batalha I & & Schutz LF 2022 A potential role of fibrillin-1 (FBN1) mRNA and asprosin in follicular development in water buffalo. Theriogenology 178 67–72. (https://doi.org/10.1016/j.theriogenology.2021.11.004)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Maylem ER, Spicer LJ, Batalha I & & Schutz LF 2021 Discovery of a possible role of asprosin in ovarian follicular function. Journal of Molecular Endocrinology 66 35–44. (https://doi.org/10.1530/JME-20-0218)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miller WL 2007 StAR search—what we know about how the steroidogenic acute regulatory protein mediates mitochondrial cholesterol import. Molecular Endocrinology 21 589–601. (https://doi.org/10.1210/me.2006-0303)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mishra I, Xie WR, Bournat JC, He Y, Wang C, Silva ES, Liu H, Ku Z, Chen Y, Erokwu BO, et al.2022 Protein tyrosine phosphatase receptor δ serves as the orexigenic asprosin receptor. Cell Metabolism 34 549–563.e8. (https://doi.org/10.1016/j.cmet.2022.02.012)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Miura C, Miura T & & Yamashita M 2002 PCNA protein expression during spermatogenesis of the Japanese eel (Anguilla japonica). Zoological Science 19 87–91. (https://doi.org/10.2108/zsj.19.87)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Moldovan GL, Pfander B & & Jentsch S 2007 PCNA, the maestro of the replication fork. Cell 129 665–679. (https://doi.org/10.1016/j.cell.2007.05.003)

  • Ohta T, Miyake H, Miura C, Kamei H, Aida K & & Miura T 2007 Follicle-stimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica. Biology of Reproduction 77 970–977. (https://doi.org/10.1095/biolreprod.107.062299)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Olaniyi KS & Areloegbe SE & Fiemotongha FE 2024 Cardiac energy depletion in a rat model of polycystic ovarian syndrome is reversed by acetate and associated with inhibitory effect of HDAC2/mTOR. European Journal of Pharmacology 962 176243. (https://doi.org/10.1016/j.ejphar.2023.176243)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Park M, Shin E, Won M, Kim JH, Go H, Kim HL, Ko JJ, Lee K & & Bae J 2010 FOXL2 interacts with steroidogenic factor-1 (SF-1) and represses SF-1-induced CYP17 transcription in granulosa cells. Molecular Endocrinology 24 1024–1036. (https://doi.org/10.1210/me.2009-0375)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Planas JV, Swanson P & & Dickhoff WW 1993 Regulation of testicular steroid production in vitro by gonadotropins (GTH I and GTH II) and cyclic AMP in coho salmon (Oncorhynchus kisutch). General and Comparative Endocrinology 91 8–24. (https://doi.org/10.1006/gcen.1993.1099)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Romere C, Duerrschmid C, Bournat J, Constable P, Jain M, Xia F, Saha PK, Del Solar M, Zhu B, York B, et al.2016 Asprosin, a fasting-induced glucogenic protein hormone. Cell 165 566–579. (https://doi.org/10.1016/j.cell.2016.02.063)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Roy A, Basak R & & Rai U 2017 De novo sequencing and comparative analysis of testicular transcriptome from different reproductive phases in freshwater spotted snakehead Channa punctatus. PLOS ONE 12 e0173178. (https://doi.org/10.1371/journal.pone.0173178)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sathoria P, Chuphal B, Rai U & & Roy B 2023 Molecular cloning, characterization and 3D modelling of spotted snakehead fbn1 C-terminal region encoding asprosin and expression analysis of fbn1. Scientific Reports 13 4470. (https://doi.org/10.1038/s41598-023-31271-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Schulz RW, de França LR, Lareyre JJ, LeGac F, Chiarini-Garcia H, Nobrega RH & & Miura T 2010 Spermatogenesis in fish. General and Comparative Endocrinology 165 390–411. (https://doi.org/10.1016/j.ygcen.2009.02.013)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Syrjänen JL, Pellegrini L & & Davies OR 2014 A molecular model for the role of SYCP3 in meiotic chromosome organisation. eLife 3 e02963. (https://doi.org/10.7554/eLife.02963)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wei F, Long A & & Wang Y 2019 The Asprosin-OLFR734 hormonal signaling axis modulates male fertility. Cell Discovery 5 55. (https://doi.org/10.1038/s41421-019-0122-x)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Yuan M, Li W, Zhu Y, Yu B & & Wu J 2020 Asprosin: a novel player in metabolic diseases. Frontiers in Endocrinology 11 64. (https://doi.org/10.3389/fendo.2020.00064)