OpenLB
Open Library of Bioscience
Advanced Search
Frontiers in endocrinology
2022;13 826920.

Pituitary Gonadotropin Gene Expression During Induced Onset of Postsmolt Maturation in Male Atlantic Salmon: and Tissue Culture Studies.

Diego Crespo, Kai Ove Skaftnesmo, Erik Kjærner-Semb, Ozlem Yilmaz, Birgitta Norberg, Sara Olausson, Petra Vogelsang, Jan Bogerd, Lene Kleppe, Rolf B Edvardsen, Eva Andersson, Anna Wargelius, Tom J Hansen, Per Gunnar Fjelldal, Rüdiger W Schulz
Author Information
  1. Diego Crespo: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  2. Kai Ove Skaftnesmo: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  3. Erik Kjærner-Semb: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  4. Ozlem Yilmaz: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Austevoll Research Station, Storebø, Norway.
  5. Birgitta Norberg: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Austevoll Research Station, Storebø, Norway.
  6. Sara Olausson: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Austevoll Research Station, Storebø, Norway.
  7. Petra Vogelsang: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  8. Jan Bogerd: Reproductive Biology Group, Division Developmental Biology, Department Biology, Science Faculty, Utrecht University, Utrecht, Netherlands.
  9. Lene Kleppe: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  10. Rolf B Edvardsen: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  11. Eva Andersson: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  12. Anna Wargelius: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
  13. Tom J Hansen: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Matre Research Station, Matredal, Norway.
  14. Per Gunnar Fjelldal: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Matre Research Station, Matredal, Norway.
  15. Rüdiger W Schulz: Research Group Reproduction and Developmental Biology, Institute of Marine Research, Bergen, Norway.
PMID: 35370944 DOI: 10.3389/fendo.2022.826920

Abstract

Precocious male maturation causes reduced welfare and increased production costs in Atlantic salmon () aquaculture. The pituitary produces and releases follicle-stimulating hormone (Fsh), the gonadotropin triggering puberty in male salmonids. However, little is known about how Fsh production is regulated in Atlantic salmon. We examined, and , transcriptional changes of gonadotropin-related genes accompanying the initial steps of testis maturation, in pituitaries of males exposed to photoperiod and temperature conditions promoting maturation (constant light and 16°C). Pituitary , and transcripts increased in maturing males (gonado-somatic index > 0.1%). RNA sequencing (RNAseq) analysis using pituitaries from genetically similar males carrying the same genetic predisposition to mature, but differing by responding or not responding to stimulatory environmental conditions, revealed 144 differentially expressed genes, ~2/3rds being up-regulated in responders, including and other pituitary hormones, steroid-related and other puberty-associated transcripts. Functional enrichment analyses confirmed gene involvement in hormone/steroid production and gonad development. In studies, whole pituitaries were exposed to a selection of hormones and growth factors. Gonadotropin-releasing hormone (Gnrh), 17β-estradiol (E) and 11-ketotestosterone (11-KT) up-regulated and , while was up-regulated by Gnrh but down-regulated by 11-KT in pituitaries from immature males. Also pituitaries from maturing males responded to Gnrh and sex steroids by increased and transcript levels, but expression remained unchanged. Growth factors (inhibin A, activin A and insulin-like growth factor 1) did not change , or transcript levels in pituitaries either from immature or maturing males. Additional pituitary studies on candidates identified by RNAseq showed that these transcripts were preferentially regulated by Gnrh and sex steroids, but not by growth factors, and that Gnrh/sex steroids were less effective when incubating pituitaries from maturing males. Our results suggest that a yet to be characterized mechanism up-regulating expression in the salmon pituitary is activated in response to stimulatory environmental conditions prior to morphological signs of testis maturation, and that the transcriptional program associated with this mechanism becomes unresponsive or less responsive to most stimulators once males had entered pubertal developmental .

Keywords

Atlantic salmon follicle-stimulating hormone pituitary puberty transcriptomics

References

  1. J Endocrinol. 2019 Feb 1;240(2):361-377 [PMID: 30594119]
  2. BMC Genomics. 2014 Feb 19;15:141 [PMID: 24548379]
  3. PLoS Genet. 2015 Nov 09;11(11):e1005628 [PMID: 26551894]
  4. Int J Clin Exp Pathol. 2015 Apr 01;8(4):3556-67 [PMID: 26097538]
  5. Endocrinology. 2015 Jun;156(6):2313-22 [PMID: 25856429]
  6. Fish Physiol Biochem. 1993 Jul;11(1-6):175-82 [PMID: 24202474]
  7. Mol Reprod Dev. 2008 Feb;75(2):403-13 [PMID: 17874455]
  8. Gen Comp Endocrinol. 2010 Feb 1;165(3):438-55 [PMID: 19393655]
  9. J Chem Neuroanat. 2008 Jan;35(1):33-48 [PMID: 17629451]
  10. Hum Reprod. 2012 May;27(5):1460-5 [PMID: 22416012]
  11. Mol Endocrinol. 2011 Jul;25(7):1184-96 [PMID: 21527504]
  12. Amino Acids. 2006 Oct;31(3):251-72 [PMID: 16820980]
  13. Endocrinology. 2017 Jun 1;158(6):1827-1837 [PMID: 28379327]
  14. Endocrinology. 2014 Nov;155(11):4531-41 [PMID: 25105781]
  15. Biol Reprod. 1996 Jun;54(6):1375-82 [PMID: 8724367]
  16. J Mol Endocrinol. 1998 Dec;21(3):291-306 [PMID: 9845670]
  17. Proc Natl Acad Sci U S A. 2021 Feb 2;118(5): [PMID: 33500349]
  18. Front Endocrinol (Lausanne). 2021 Aug 23;12:719843 [PMID: 34497587]
  19. J Mol Endocrinol. 2007 Feb;38(1-2):207-19 [PMID: 17293441]
  20. Endocrinology. 2002 Sep;143(9):3243-9 [PMID: 12193535]
  21. Mol Cell Endocrinol. 2014 Mar 25;385(1-2):18-27 [PMID: 24145126]
  22. Nature. 2015 Dec 17;528(7582):405-8 [PMID: 26536110]
  23. Am J Physiol Regul Integr Comp Physiol. 2000 Jun;278(6):R1572-8 [PMID: 10848525]
  24. J Endocrinol. 2020 Apr;245(1):21-37 [PMID: 31977313]
  25. Nucleic Acids Res. 2019 Jul 2;47(W1):W199-W205 [PMID: 31114916]
  26. Int J Mol Sci. 2021 Jun 17;22(12): [PMID: 34204216]
  27. Sci Rep. 2016 Feb 18;6:21284 [PMID: 26888627]
  28. Gen Comp Endocrinol. 2009 Jun;162(2):134-8 [PMID: 19298819]
  29. BMC Genet. 2020 Nov 12;21(1):123 [PMID: 33183224]
  30. Gen Comp Endocrinol. 2020 Nov 1;298:113568 [PMID: 32710898]
  31. Endocrinology. 2013 Nov;154(11):4365-76 [PMID: 24002037]
  32. J Mol Endocrinol. 2005 Dec;35(3):571-83 [PMID: 16326841]
  33. J Clin Endocrinol Metab. 2000 Jan;85(1):263-9 [PMID: 10634397]
  34. J Endocrinol. 1997 Apr;153(1):139-50 [PMID: 9135579]
  35. Nat Methods. 2019 Dec;16(12):1226-1232 [PMID: 31570887]
  36. Endocrinology. 2020 Dec 1;161(12): [PMID: 33045050]
  37. Biol Reprod. 2014 Jan 16;90(1):6 [PMID: 24258209]
  38. Nucleic Acids Res. 2019 Jul 2;47(W1):W191-W198 [PMID: 31066453]
  39. Endocrinology. 2009 Jan;150(1):357-65 [PMID: 18755797]
  40. Gen Comp Endocrinol. 2015 Jan 15;211:52-61 [PMID: 25435279]
  41. Gen Comp Endocrinol. 2020 Jan 1;285:113293 [PMID: 31580881]
  42. Nat Genet. 2000 May;25(1):25-9 [PMID: 10802651]
  43. PLoS One. 2013 Oct 23;8(10):e76684 [PMID: 24194844]
  44. Comp Biochem Physiol B Biochem Mol Biol. 2001 Jun;129(2-3):489-502 [PMID: 11399484]
  45. Fish Physiol Biochem. 1989 Jun;7(1-6):169-76 [PMID: 24221769]
  46. Gen Comp Endocrinol. 2010 Feb 1;165(3):483-515 [PMID: 19442666]
  47. Reprod Biol Endocrinol. 2019 Jun 21;17(1):48 [PMID: 31226998]
  48. Comp Biochem Physiol A Mol Integr Physiol. 2009 Aug;153(4):408-16 [PMID: 19345741]
  49. BMC Bioinformatics. 2021 Sep 10;22(1):433 [PMID: 34507520]
  50. Braz J Med Biol Res. 2005 Oct;38(10):1487-94 [PMID: 16172741]
  51. Endocrinology. 1995 Aug;136(8):3486-93 [PMID: 7628385]
  52. Endocrinology. 2010 May;151(5):2349-60 [PMID: 20308533]
  53. Biol Reprod. 2018 Sep 1;99(3):504-513 [PMID: 29757344]
  54. PLoS Biol. 2018 Jul 3;16(7):e2005970 [PMID: 29969450]
  55. Endocrinology. 2018 Feb 1;159(2):980-993 [PMID: 29272351]
  56. PLoS One. 2013;8(3):e59058 [PMID: 23536856]
  57. Comp Biochem Physiol A Mol Integr Physiol. 2018 May;219-220:48-57 [PMID: 29496550]
  58. Gen Comp Endocrinol. 2010 Jul 1;167(3):387-96 [PMID: 19800342]
  59. Gen Comp Endocrinol. 1990 Mar;77(3):348-57 [PMID: 2186958]
  60. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  61. J Endocrinol. 2014 Jun;221(3):429-40 [PMID: 24709578]
  62. PLoS One. 2017 Jun 29;12(6):e0179789 [PMID: 28662143]
  63. Biol Reprod. 2001 May;64(5):1358-65 [PMID: 11319139]
  64. Gen Comp Endocrinol. 2008 Sep 1;158(2):178-82 [PMID: 18664367]
  65. Nat Methods. 2012 Mar 04;9(4):357-9 [PMID: 22388286]
  66. Gen Comp Endocrinol. 2013 Sep 15;191:247-58 [PMID: 23856539]
  67. Life Sci. 2004 Feb 6;74(12):1445-63 [PMID: 14729395]
  68. Endocrinology. 2015 Nov;156(11):4163-73 [PMID: 26261873]
  69. Gen Comp Endocrinol. 1999 Mar;113(3):413-28 [PMID: 10068502]
  70. Development. 2001 Jan;128(2):147-54 [PMID: 11124111]
  71. Front Endocrinol (Lausanne). 2014 Oct 22;5:182 [PMID: 25379037]
  72. J Clin Endocrinol Metab. 2010 Jul;95(7):3491-6 [PMID: 20463092]
  73. Gen Comp Endocrinol. 2009 Jan 15;160(2):183-93 [PMID: 19063890]
  74. Gen Comp Endocrinol. 1999 Oct;116(1):81-9 [PMID: 10525364]
  75. Endocrinology. 2015 Jun;156(6):2185-99 [PMID: 25849727]
  76. Biol Reprod. 1995 Mar;52(3):697-704 [PMID: 7756464]
  77. J Clin Invest. 2008 Aug;118(8):2822-31 [PMID: 18596921]
  78. Front Endocrinol (Lausanne). 2019 Jul 12;10:469 [PMID: 31354632]
  79. Gen Comp Endocrinol. 2019 Dec 1;284:113244 [PMID: 31415728]
  80. J Endocrinol. 2014 Feb 10;220(3):319-32 [PMID: 24363452]
  81. Mol Cell Endocrinol. 2018 Mar 5;463:116-130 [PMID: 28342855]
  82. Gen Comp Endocrinol. 2012 Jan 1;175(1):82-91 [PMID: 22019479]
  83. Endocrinology. 2014 Dec;155(12):4831-42 [PMID: 25211586]
  84. Gen Comp Endocrinol. 2020 Feb 1;287:113344 [PMID: 31794734]
  85. Gen Comp Endocrinol. 1997 Oct;108(1):152-60 [PMID: 9378269]
  86. Methods. 2001 Dec;25(4):402-8 [PMID: 11846609]
  87. Gen Comp Endocrinol. 1988 Dec;72(3):394-401 [PMID: 3240849]
  88. Cells. 2021 Aug 04;10(8): [PMID: 34440752]
  89. Front Endocrinol (Lausanne). 2021 Mar 03;11:534343 [PMID: 33763023]
  90. Sci Rep. 2017 Oct 3;7(1):12584 [PMID: 28974703]
  91. J Mol Endocrinol. 2012 Jun 26;49(1):21-33 [PMID: 22586143]
  92. Reproduction. 2009 Oct;138(4):709-19 [PMID: 19602521]
  93. Annu Rev Anim Biosci. 2022 Feb 15;10:107-130 [PMID: 34788545]
  94. Cell Tissue Res. 2019 Jan;375(1):227-241 [PMID: 30284083]
  95. Gen Comp Endocrinol. 2010 Feb 1;165(3):390-411 [PMID: 19348807]
  96. Endocrinology. 2017 Jul 1;158(7):2319-2329 [PMID: 28444173]
  97. Biol Reprod. 2001 Dec;65(6):1807-12 [PMID: 11717145]
  98. Bioinformatics. 2009 Aug 15;25(16):2078-9 [PMID: 19505943]
  99. Zoolog Sci. 2008 Mar;25(3):299-306 [PMID: 18393567]
  100. Gen Comp Endocrinol. 2000 Jun;118(3):436-49 [PMID: 10843795]
  101. Gen Comp Endocrinol. 2010 Feb 1;165(3):412-37 [PMID: 19686749]
  102. Reprod Biol Endocrinol. 2008 Sep 15;6:42 [PMID: 18793397]
  103. Biol Reprod. 2006 Jun;74(6):993-8 [PMID: 16481592]
  104. Gen Comp Endocrinol. 1992 Feb;85(2):217-29 [PMID: 1601254]
  105. Zoolog Sci. 2003 Jan;20(1):69-73 [PMID: 12560603]
  106. Front Endocrinol (Lausanne). 2020 Dec 07;11:605068 [PMID: 33365013]
  107. Hum Mol Genet. 2017 Sep 15;26(18):3585-3599 [PMID: 28911201]
  108. Sci Rep. 2016 Mar 31;6:23777 [PMID: 27029812]
  109. PLoS Genet. 2009 Mar;5(3):e1000420 [PMID: 19282985]
  110. Physiol Rev. 2012 Jan;92(1):1-38 [PMID: 22298650]
  111. Endocrinology. 2015 Feb;156(2):627-37 [PMID: 25422875]
  112. BMC Genomics. 2019 Jun 11;20(1):475 [PMID: 31185904]
  113. Genome Biol. 2006;7(10):R100 [PMID: 17076895]
  114. Gen Comp Endocrinol. 1999 Apr;114(1):142-50 [PMID: 10094867]

MeSH Term

Animals
Gene Expression
Gonadotropins
Gonadotropins, Pituitary
Male
Salmo salar
Sexual Maturation

Chemicals

Gonadotropins
Gonadotropins, Pituitary
Journal Article
Article has an altmetric score of 4

Word Cloud

Created with Highcharts 10.0.0malespituitariespituitarymaturationAtlanticsalmonmaturingGnrhincreasedproductionhormoneconditionstranscriptsup-regulatedgrowthfactorssteroidsmalefollicle-stimulatingFshpubertyregulatedtranscriptionalgenestestisexposedPituitaryRNAseqrespondingstimulatoryenvironmentalhormonesstudies11-KTimmaturesextranscriptlevelsexpressionlessmechanismPrecociouscausesreducedwelfarecostsaquacultureproducesreleasesgonadotropintriggeringsalmonidsHoweverlittleknownexaminedchangesgonadotropin-relatedaccompanyinginitialstepsphotoperiodtemperaturepromotingconstantlight16°Cgonado-somaticindex>01%RNAsequencinganalysisusinggeneticallysimilarcarryinggeneticpredispositionmaturedifferingrevealed144differentiallyexpressed~2/3rdsrespondersincludingsteroid-relatedpuberty-associatedFunctionalenrichmentanalysesconfirmedgeneinvolvementhormone/steroidgonaddevelopmentwholeselectionGonadotropin-releasing17β-estradiolE11-ketotestosteronedown-regulatedAlsorespondedremainedunchangedGrowthinhibinactivininsulin-likefactor1changeeitherAdditionalcandidatesidentifiedshowedpreferentiallyGnrh/sexeffectiveincubatingresultssuggestyetcharacterizedup-regulatingactivatedresponsepriormorphologicalsignsprogramassociatedbecomesunresponsiveresponsivestimulatorsenteredpubertaldevelopmentalGonadotropinGeneExpressionInducedOnsetPostsmoltMaturationMaleSalmon:TissueCultureStudiestranscriptomics

Similar Articles

Cited By (1)