Skip to main content
Log in

Presence of gonadotropin-releasing hormone-like peptide in the central nervous system and reproductive organs of the male blue swimming crab, Portunus pelagicus, and its effect on spermatogenesis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Our previous studies have demonstrated that lamprey gonadotropin-releasing hormone-III (lGnRH-III)-like peptide occurs in the central nervous system (CNS) of decapod crustaceans (Macrobrachium rosenbergii, Penaeus monodon, Portunus pelagicus), and that lGnRH-III is the most potent in stimulating ovarian maturation compared with other GnRH isoforms. In this study, we examined the localization of lGnRH-III-like peptide in the CNS and male reproductive organs of the blue swimming crab by using anti-lGnRH-III as a probe. In the brain, lGnRH-III immunoreactivity (−ir) was detected in neurons of clusters 6, 10, 11, 14/15, 16, and 17 and in many neuropils. In the subesophageal ganglion, lGnRH-III-ir was present in neurons of the dorso-lateral and ventro-medial clusters. In the thoracic ganglia, lGnRH-III-ir was observed in the large-sized neurons between the thoracic neuropils and in the ventromedial cluster of the abdominal ganglia. In the testis, lGnRH-III-ir was detected in nurse cells, hemocytes, spermatids 2, and the outer and inner zones of the acrosomes of spermatozoa. Bioassay showed that lGnRH-III significantly increased the testis-somatic index, the percentage of late stages of seminiferous tubules (stages VII–IX), the diameter of the seminiferous tubules, and the number of BrdU-labeled early germ cells compared with the control groups. Thus, lGnRH-III-like peptide exists in the male crab and possibly enhances germ cell proliferation and maturation in the testes, leading to increased sperm production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andreu-Vieyra CV, Habibi HR (2001) Effects of salmon GnRH and chicken GnRH-II on testicular apoptosis in goldfish (Carassius auratus). Comp Biochem Physiol B Biochem Mol Biol 129:483–487

    Article  CAS  PubMed  Google Scholar 

  • Andreu-Vieyra CV, Buret AG, Habibi HR (2005) Gonadotropin-releasing hormone induction of apoptosis in the testes of goldfish (Carassius auratus). Endocrinology 146:1588–1596

    Article  CAS  PubMed  Google Scholar 

  • Anjum S, Krishna A, Sridaran R, Tsutsui K (2012) Localization of gonadotropin-releasing hormone (GnRH), gonadotropin-inhibitory hormone (GnIH), kisspeptin and GnRH receptor and their possible roles in testicular activities from birth to senescence in mice. J Exp Zool A Ecol Genet Physiol 317:630–644

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bahk JY, Hyun JS, Chung SH, Lee H, Kim MO, Lee BH, Choi WS (1995) Stage specific identification of the expression of GnRH mRNA and localization of the GnRH receptor in mature rat and adult human testis. J Urol 154:1958–1961

    Article  CAS  PubMed  Google Scholar 

  • Bigot L, Zatylny-Gaudin C, Rodet F, Bernay B, Boudry P, Favrel P (2012) Characterization of GnRH-related peptides from the Pacific oyster Crassostrea gigas. Peptides 34:303–310

    Article  CAS  PubMed  Google Scholar 

  • Botte MC, Chamagne AM, Carre MC, Counis R, Kottler ML (1998) Fetal expression of GnRH and GnRH receptor genes in rat testis and ovary. J Endocrinol 159:179–189

    Article  CAS  PubMed  Google Scholar 

  • Chansela P, Goto-Inoue N, Zaima N, Sroyraya M, Sobhon P, Setou M (2012) Visualization of neuropeptides in paraffin-embedded tissue of the central nervous system in the decapod crustacean, Penaeus monodon, by mass spectrometry. Peptides 34:10–18

    Article  CAS  PubMed  Google Scholar 

  • Chianese R, Ciaramella V, Scarpa D, Fasano S, Pierantoni R, Meccariello R (2012) Anandamide regulates the expression of GnRH1, GnRH2, and GnRH-Rs in frog testis. Am J Physiol Endocrinol Metab 303:475–487

    Article  Google Scholar 

  • D’Antonio M, Fasano S, Leeuw R de, Pierantoni R (1992) Effects of gonadotropin-releasing hormone variants on plasma and testicular androgen levels in intact and hypophysectomized male frogs, Rana esculenta. J Exp Zool 261:34–39

  • Decatur WA, Hall JA, Smith JJ, Li W, Sower SA (2013) Insight from the lemprey genome: glimpsing early vertebrate development via neuroendocrine-associated genes and shared syntery of gonadotropin-releasing hormone (GnRH). Gen Comp Endocrinol 192:237–245

    Article  CAS  PubMed  Google Scholar 

  • Dong KW, Duval P, Zeng Z, Gordon K, Williams RF, Hodgen GD, Jones G, Kerdelhue B, Roberts JL (1996) Multiple transcription start sites for the GnRH gene in rhesus and cynomolgus monkeys: a non-human primate model for studying GnRH gene regulation. Mol Cell Endocrinol 117:121–130

    Article  CAS  PubMed  Google Scholar 

  • Dubois EA, Zandbergen MA, Peute J, Goos HJ (2002) Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems in vertebrates. Brain Res Bull 57:413–418

    Article  CAS  PubMed  Google Scholar 

  • Fanenbruck M, Harzsch S, Wagele JW (2004) The brain of the Remipedia (Crustacea) and an alternative hypothesis on their phylogenetic relationships. Proc Natl Acad Sci U S A 101:3868–3873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer AHL, Scholtz G (2010) Axogenesis in the stomatopod crustacean Gonodactylacens falcatus (Malacostraca). Invertebr Biol 129:59–76

    Article  Google Scholar 

  • Guan ZB, Shui Y, Liao XR, Xu ZH, Zhou X (2014) Primary structure of a novel gonadotropin-releasing hormone (GnRH) in the ovary of red swamp crayfish Procambarus clarkii. Aquaculture 418:67–71

    Article  Google Scholar 

  • Harzsch S, Hansson BS (2008) Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci 9:58

    Article  PubMed  PubMed Central  Google Scholar 

  • Harzsch S, Miller J, Benton J, Dawirs RR, Beltz B (1998) Neurogenesis in the thoracic neuromeres of two crustaceans with different types of metamorphic development. J Exp Biol 201:2465–2479

    PubMed  Google Scholar 

  • Hauser F, Grimmelikhuijzen CJ (2014) Evolution of the AKH/corazonin/ACP/GnRH receptor superfamily and their ligands in the Protostomia. Gen Comp Endrocrinol 209:35–49

    Article  CAS  Google Scholar 

  • Hsueh AJ, Bambino TH, Zhuang LZ, Welsh TH Jr, Ling NC (1983) Mechanism of the direct action of gonadotropin-releasing hormone and its antagonist on androgen biosynthesis by cultured rat testicular cells. Endocrinology 112:1653–1661

    Article  CAS  PubMed  Google Scholar 

  • Huang H, Ye H, Li S, Wang G (2008) Immunocytological evidence for the presence of vertebrate FSH- and LH-like substances in the brain and thoracic ganglion of the swimming crab, Portunus trituberculatus. Prog Nat Sci 18:1453–1457

    Article  CAS  Google Scholar 

  • Huberman A (2000) Shrimp endocrinology. A review. Aquaculture 191:191–208

    Article  CAS  Google Scholar 

  • Iwakoshi-Ukena E, Ukena K, Takuwa-Kuroda K, Kanda A, Tsutsui K, Minakata H (2004) Expression and distribution of octopus gonadotropin-releasing hormone in the central nervous system and peripheral organs of the octopus (Octopus vulgaris) by in situ hybridization and immunohistochemistry. J Comp Neurol 477:310–323

    Article  PubMed  Google Scholar 

  • Jimenez-Linan M, Rubin BS, King JC (1997) Examination of guinea pig luteinizing hormone-releasing hormone gene reveals a unique decapeptide and existence of two transcripts in the brain. Endocrinology 138:4123–4130

    CAS  PubMed  Google Scholar 

  • Kanda A, Takahashi T, Satake H, Minakata H (2006) Molecular and functional characterization of a novel gonadotropin-releasing hormone receptor isolated from the common octopus (Octopus vulgaris). Biochem J 395:125–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klaus S, Münzner S, Modenbach AC, Streit B, Tudge CC (2013) Spermatophore formation and sperm ultrastructure of Sundathelphusa philippina (Crustacea: Brachyura: Gecarcinucidae). Acta Zool 94:267–272

    Article  Google Scholar 

  • Kornthong N, Tinikul Y, Khornchatri K, Saeton J, Magerd S, Suwansa-ard S, Kruangkum T, Hanna PJ, Sobhon P (2013) Neuronal classification and distribution in the central nervous system of the female mud crab, Scylla olivacea. Microsc Res Tech 77:189–200

    Article  PubMed  Google Scholar 

  • Krieger J, Sombke A, Seefluth F, Kenning M, Hansson BS, Harzsch S (2012) Comparative brain architecture of the European shore crab Carcinus maenas (Brachyura) and the common hermit crab Pagurus bernhardus (Anomura) with notes on other marine hermit crabs. Cell Tissue Res 348:47–69

    Article  PubMed  Google Scholar 

  • Lindemans M, Janssen T, Beets I, Temmerman L, Meelkop E, Schoofs L (2011) Gonadotropin-releasing hormone and adipokinetic hormone signaling systems share a common evolutionary origin. Front Endocrinol 2:1–6

    Article  Google Scholar 

  • Manochantr S, Sretarugsa P, Wanichanon C, Chavadej J, Sobhon P (2003) Classification of spermatogenic cells in Rana tigerina based on ultrastructure. ScienceAsia 29:241–254

    Article  Google Scholar 

  • Manochantr S, Sretarugsa P, Chavadej J, Sobhon P (2005) Chromatin organization and basic nuclear proteins in the male germ cells of Rana tigerina. Mol Reprod Dev 70:184–197

    Article  CAS  PubMed  Google Scholar 

  • Mathieu M, Lenoir F, Robbins I (1988) A gonial mitosis-stimulating factor in cerebral ganglia and hemolymph of the marine mussel Mytilus edulis L. Gen Comp Endocrinol 72:257–263

    Article  CAS  PubMed  Google Scholar 

  • McGuire NL, Bentley GE (2010) Neuropeptides in the gonads: from evolution to pharmacology. Front Pharmacol 1:1–13

    Article  Google Scholar 

  • Meeratana P, Withyachumnarnkul B, Damrongphol P, Wongprasert K, Suseangtham A, Sobhon P (2006) Serotonin induces ovarian maturation in giant freshwater prawn broodstock, Macrobrachium rosenbergii De Man. Aquaculture 260:315–325

    Article  CAS  Google Scholar 

  • Mikami S, Yamada S, Hasegawa Y, Miyamoto K (1988) Localization of avian LHRH immunoreactive neurons in the hypothalamus of the domestic fowl, Gallus domesticus, and the Japanese quail, Coturnix coturnix. Cell Tissue Res 251:51–58

    Article  CAS  PubMed  Google Scholar 

  • Minakata H, Shigeno S, Kano N, Haraguchi S, Osugi T, Tsutsui K (2009) Octopus gonadotrophin-releasing hormone: a multifunctional peptide in the endocrine and nervous systems of the cephalopod. J Neuroendocrinol 21:322–326

    Article  CAS  PubMed  Google Scholar 

  • Nakamura S, Osada M, Kijima A (2007) Involvement of GnRH neuron in the spermatogonial proliferation of the scallop, Patinopecten yessoensiss. Mol Reprod Dev 74:108–115

    Article  CAS  PubMed  Google Scholar 

  • Ngernsoungnern P, Ngernsoungnern A, Kavanaugh S, Sobhon P, Sower SA, Sretarugsa P (2008a) The presence and distribution of gonadotropin-releasing hormone-liked factor in the central nervous system of the black tiger shrimp, Penaeus monodon. Gen Comp Endocrinol 155:613–622

    Article  CAS  PubMed  Google Scholar 

  • Ngernsoungnern A, Ngernsoungnern P, Kavanaugh S, Sower SA, Sobhon P, Sretarugsa P (2008b) The identification and distribution of gonadotropin-releasing hormone-like peptides in the central nervous system and ovary of the giant freshwater prawn, Macrobrachium rosenbergii. Invertebr Neurosci 8:49–57

    Article  CAS  Google Scholar 

  • Ngernsoungnern A, Ngernsoungnern P, Weerachatyanukul W, Chavadej J, Sobhon P, Sretarugsa P (2008c) The existence of gonadotropin-releasing hormone (GnRH) immunoreactivity in the ovary and the effects of GnRHs on the ovarian maturation in the black tiger shrimp Penaeus monodon. Aquaculture 279:197–203

    Article  CAS  Google Scholar 

  • Ngernsoungnern P, Ngernsoungnern A, Sobhon P, Sretarugsa P (2009) Gonadotropin-releasing hormone (GnRH) and a GnRH analog induce ovarian maturation in the giant freshwater prawn, Macrobrachium rosenbergii. Invertebr Reprod Dev 53:125–135

    Article  CAS  Google Scholar 

  • Nuurai P, Poljaroen J, Tinikul Y, Cummins S, Sretarugsa P, Hanna P, Wanichanon C, Sobhon P (2010) The existence of gonadotropin-releasing hormone-like peptides in the neural ganglia and ovary of the abalone, Haliotis asinina L. Acta Histochem 112:557–566

    Article  CAS  PubMed  Google Scholar 

  • Okubo K, Nagahama Y (2008) Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol (Oxford) 193:3–15

    Article  CAS  Google Scholar 

  • Okuzawa K, Amano M, Kobayashi M, Aida K, Hanyu I, Hasegawa Y, Miyamoto K (1990) Differences in salmon GnRH and chicken GnRH-II contents in discrete brain areas of male and female rainbow trout according to age and stage of maturity. Gen Comp Endocrinol 80:116–126

    Article  CAS  PubMed  Google Scholar 

  • Osada M, Treen N (2013) Molluscan GnRH associated with reproduction. Gen Comp Endocrinol 181:254–258

    Article  CAS  PubMed  Google Scholar 

  • Osada M, Tawarayama H, Mori K (2004) Estrogen synthesis in relation to gonadal development of Japanese scallop, Patinopecten yessoensis: gonadal profile and immunolocalization of P450 aromatase and estrogen. Comp Biochem Physiol B Biochem Mol Biol 139:123–128

    Article  PubMed  Google Scholar 

  • Pazos AJ, Mathieu M (1999) Effects of five natural gonadotropin-releasing hormones on cell suspensions of marine bivalve gonad: stimulation of gonial DNA synthesis. Gen Comp Endocrinol 113:112–120

    Article  CAS  PubMed  Google Scholar 

  • Poljaroen J, Tinikul Y, Phoungpetchara I, Kankoun W, Suwansa-ard S, Siangcham T, Meeratana P, Cummins SF, Sretarugsa P, Hanna PJ, Sobhon P (2011) The effects of biogenic amines, gonadotropin-releasing hormones and corazonin on spermatogenesis in sexually mature small giant freshwater prawns, Macrobrachium rosenbergii (De Man, 1879). Aquaculture 321:121–129

    Article  CAS  Google Scholar 

  • Richter S, Loesel R, Purschke G, Schmidt-Rhaesa A, Scholtz G, Stach T, Vogt L, Wanninger A, Brenneis G, Doring C, Faller S, Fritsch M, Grobe P, Heuer CM, Kaul S, Moller OS, Muller CH, Rieger V, Rothe BH, Stegner ME, Harzsch S (2010) Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary. Front Zool 7:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Roch GJ, Busby ER, Sherwood NM (2011) Evolution of GnRH: diving deeper. Gen Comp Endocrinol 171:1–16

    Article  CAS  PubMed  Google Scholar 

  • Roch GJ, Busby ER, Sherwood NM (2014) GnRH receptors and peptides: skating backward. Gen Comp Endocrinol 209:118–134

    Article  CAS  PubMed  Google Scholar 

  • Saetan J, Senarai T, Tamtin M, Weerachatyanukul W, Chavadej J, Hanna PJ, Parhar I, Sobhon P, Sretarugsa P (2013) Histological organization of the central nervous system and distribution of a gonadotropin-releasing hormone-like peptide in the blue crab, Portunus pelagicus. Cell Tissue Res 353:493–510

    Article  CAS  PubMed  Google Scholar 

  • Sandeman D, Sanderman R, Aitken A (1988) Atlas of serotonin-containing neurons in the optic lobes and brain of the crayfish Cherax destructor. J Comp Neurol 269:465–478

    Article  CAS  PubMed  Google Scholar 

  • Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304–326

    Article  Google Scholar 

  • Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea+Hexapoda). Arthropod Struct Dev 34:257–299

    Article  Google Scholar 

  • Sherwood NM, Adams BA (2005) Gonadotropin-releasing hormone in fish: evolution, expression and regulation of the GnRH gene. In: Melamed P, Sherwood NM (eds) Molecular aspects of fish & marine biology, vol 4. Hormones and their receptors in fish reproduction. World Scientific, Singapore, pp 1–39

  • Simeo CG, Ribes E, Rotllant G (2009) Internal anatomy and ultrastructure of the male reproductive system of the spider crab Maja brachydactyla (Decapoda: Brachyura). Tissue Cell 41:345–361

    Article  CAS  PubMed  Google Scholar 

  • Sower SA (2003) The endocrinology of reproduction in lampreys and applications for male lamprey sterilization. J Great Lakes Res 29:50–65

    Article  Google Scholar 

  • Sower SA, Chiang YC, Lovas S, Conlon JM (1993) Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinology 132:1125–1131

    CAS  PubMed  Google Scholar 

  • Sower SA, Freamat M, Kavanaugh SI (2009) The origins of the vertebrate hypothalamic-pituitary-gonadal (HPG) and hypothalamic-pituitary-thyroid (HPT) endocrine systems: new insights from lampreys. Gen Comp Endocrinol 161:20–29

    Article  CAS  PubMed  Google Scholar 

  • Sroyraya M, Hanna PJ, Changklungmoa N, Senarai T, Siangcham T, Tinikul Y, Sobhon P (2013) Expression of the male reproduction-related gene in spermatic ducts of the blue swimming crab, Portunus pelagicus, and transfer of modified protein to the sperm acrosome. Microsc Res Tech 76:102–112

    Article  CAS  PubMed  Google Scholar 

  • Stewart MJ, Stewart P, Soonklang N, Linthong V, Hanna PJ, Duan W, Sobhon P (2010) Spermatogenesis in the blue swimming crab, Portunus pelagicus, and evidence for histones in mature sperm nuclei. Tissue Cell 42:137–150

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JM, Beltz BS (2004) Evolutionary changes in the olfactory projection neuron pathways of eumalacostracan crustaceans. J Comp Neurol 470:25–38

    Article  PubMed  Google Scholar 

  • Sun YM, Dunn IC, Baines E, Talbot RT, Illing N, Millar RP, Sharp PJ (2001) Distribution and regulation by oestrogen of fully processed and variant transcripts of gonadotropin releasing hormone I and gonadotropin releasing hormone receptor mRNAs in the male chicken. J Neuroendocrinol 13:37–49

    Article  CAS  PubMed  Google Scholar 

  • Tinikul Y, Poljaroen J, Nuurai P, Anuracpreeda P, Chotwiwatthanakun C, Phoungpetchara I, Kornthong N, Poomtong T, Hanna PJ, Sobhon P (2011) Existence and distribution of gonadotropin-releasing hormone-like peptides in the central nervous system and ovary of the Pacific white shrimp, Litopenaeus vannamei. Cell Tissue Res 343:579–593

    Article  CAS  PubMed  Google Scholar 

  • Treen N, Itoh N, Miura H, Kikuchi I, Ueda T, TakahashiKG UT, Yamamoto K, Sharp PJ, Tsutsui K, Osada M (2012) Mollusc gonadotropin-releasing hormone directly regulates gonadal functions: a primitive endocrine system controlling reproduction. Gen Comp Endocrinol 176:167–172

    Article  CAS  PubMed  Google Scholar 

  • Tsai PS, Zhang L (2008) The emergence and loss of gonadotropin-releasing hormone in protostomes: orthology, phylogeny, structure, and function. Biol Reprod 79:798–805

    Article  CAS  PubMed  Google Scholar 

  • Tsai PS, Maldonado TA, Lunden JB (2003) Localization of gonadotropin-releasing hormone in the central nervous system and a peripheral chemosensory organ of Aplysia californica. Gen Comp Endocrinol 130:20–28

    Article  CAS  PubMed  Google Scholar 

  • Tsai PS, Sun B, Rochester JR, Wayne NL (2010) Gonadotropin-releasing hormone-like molecule is not an acute reproductive activator in the gastropod, Aplysia californica. Gen Comp Endocrinol 166:280–288

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Huang H, Song P, Wang G (2010) The identification and distribution of progesterone receptors in the brain and thoracic ganglion in the mud crab Scylla paramamosain (Crustacea: Decapoda: Brachyura). Invertebr Neurosci 10:11–16

    Article  CAS  Google Scholar 

  • Ye H, Ma J, Lin Q, Wang G (2011) Occurrence of follicle-stimulating hormone-like substance in the kuruma prawn, Marsupenaeus japonicus, during ovarian maturation. Mar Biol Res 7:304–309

    Article  Google Scholar 

  • Young KG, Chang JP, Goldberg JI (1999) Gonadotropin-releasing hormone neuronal system of the freshwater snails Helisoma trivolvis and Lymnaea stagnalis: possible involvement in reproduction. J Comp Neurol 404:427–437

    Article  CAS  PubMed  Google Scholar 

  • Zeng H, Huang J, Li W, Huang H, Ye H (2011) Identification of differentially expressed genes in the thoracic ganglion of the mud crab, Scylla paramamosain during ovarian maturation. Mar Biol Res 7:617–622

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Prepee Sretarugsa.

Additional information

This research was financially supported by a Distinguished Research Professor Grant (co-funded by Thailand Research Fund, Office of the Higher Education Commission, and Mahidol University) to Prof. Prasert Sobhon, by a grant from the Office of Higher Education, and by Mahidol University under the National Research Universities Initiatives, Thailand Research Fund/Royal Golden Jubilee Ph.D. Program Scholarship to Prof. Prapee Sretarugsa and Thanyaporn Senarai.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Senarai, T., Saetan, J., Tamtin, M. et al. Presence of gonadotropin-releasing hormone-like peptide in the central nervous system and reproductive organs of the male blue swimming crab, Portunus pelagicus, and its effect on spermatogenesis. Cell Tissue Res 365, 265–277 (2016). https://doi.org/10.1007/s00441-016-2375-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-016-2375-0

Keywords

Navigation