Abstract
Neuropeptide F in invertebrates is a homolog of neuropeptide Y in mammals and it is a member of FMRFamide-related peptides. In arthropods, such as insects, there are two types of neuropeptide F comprising long neuropeptide F (NPF) and short neuropeptide F (sNPF). Both NPFs are known to play a crucial role in the regulations of foraging, feeding-related behaviors, circadian rhythm, stress responses, aggression and reproduction in invertebrates. We have earlier found that in the giant freshwater prawn, Macrobrachium rosenbergii, there are three isoforms of NPF and four isoforms of sNPF and that NPFs are expressed in the eyestalks and brain. In the present study, we investigate further the tissue distribution of NPF-I in the ventral nerve cord (VNC) and its role in the development of testes in small male (SM) Macrobrachium rosenbergii. By immunolocalization, using the rabbit polyclonal antibody against NPF-I as a probe, we could detect NPF-I immunoreactivity in the neuropils and neuronal clusters of the subesophageal ganglia (SEG), thoracic ganglia (TG) and abdominal ganglia (AG) of the SM prawns. In functional assays, the administrations of synthetic NPF-I (KPDPTQLAAMADALKYLQELDKYYSQVSRPRFamide) and sNPF (APALRLRFamide) peptides significantly increased the growth rates of SM prawns and significantly increased the gonadosomatic index (GSI) and proliferations of early germ cells in the seminiferous tubules of their testes. It is, therefore, suggestive that NPFs may play critical roles in energy homeostasis towards promoting growth as well as testicular development in prawns that could be applied in the aquaculture of this species.
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References
Carlsson MA, Enell LE, Nassel DR (2013) Distribution of short neuropeptide F and its receptor in neuronal circuits related to feeding in larval Drosophila. Cell Tissue Res 353(3):511–523. https://doi.org/10.1007/s00441-013-1660-4
Christie AE, Cashman CR, Brennan HR, Ma M, Sousa GL, Li L et al (2008) Identification of putative crustacean neuropeptides using in silico analyses of publicly accessible expressed sequence tags. Gen Comp Endocrinol 156(2):246–264. https://doi.org/10.1016/j.ygcen.2008.01.018
Christie AE, Chapline MC, Jackson JM, Dowda JK, Hartline N, Malecha SR et al (2011) Identification, tissue distribution and orexigenic activity of neuropeptide F (NPF) in penaeid shrimp. J Exp Biol 214(Pt 8):1386–1396. https://doi.org/10.1242/jeb.053173
Corotto F, Voigt R, Atema J (1992) Spectral tuning of chemoreceptor cells of the third maxilliped of the lobster, Homarus americanus. Biol Bull 183(3):456–462. https://doi.org/10.2307/1542022
Derby CD, Atema J (1982) Chemosensitivity of walking legs of the lobster <em>Homarus Americanus</em>: neurophysiological response spectrum and thresholds. J Exp Biol 98(1):303–315
Elson RC (1996) Neuroanatomy of a crayfish thoracic ganglion: sensory and motor roots of the walking-leg nerves and possible homologies with insects. J Comp Neurol 365(1):1–17. https://doi.org/10.1002/(SICI)1096-9861(19960129)365:1<1::AID-CNE1>3.0.CO;2-7
Gard AL, Lenz PH, Shaw JR, Christie AE (2009) Identification of putative peptide paracrines/hormones in the water flea Daphnia pulex (Crustacea; Branchiopoda; Cladocera) using transcriptomics and immunohistochemistry. Gen Comp Endocrinol 160(3):271–287. https://doi.org/10.1016/j.ygcen.2008.12.014
Harzsch S (2003) Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Struct Dev 32(1):17–37. https://doi.org/10.1016/S1467-8039(03)00008-2
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(Pt 17):2465–2479
Johansson KUI, Schmidt M (1997) Dopaminergic modulation of spontaneous activity in the brain of the crayfish Cherax destructor (Decapoda, Crustacea). Can J Zool 75(1):18–26. https://doi.org/10.1139/z97-003
Kankuan W, Wanichanon C, Titone R, Engsusophon A, Sumpownon C, Suphamungmee W et al (2017) Starvation promotes autophagy-associated maturation of the ovary in the giant freshwater prawn, Macrobrachium rosenbergii. Front Physiol 8(300):300. https://doi.org/10.3389/fphys.2017.00300
Karl T, Herzog H (2007) Behavioral profiling of NPY in aggression and neuropsychiatric diseases. Peptides 28(2):326–333. https://doi.org/10.1016/j.peptides.2006.07.027
Kondoh Y, Hisada M (1986) Neuroanatomy of the terminal (sixth abdominal) ganglion of the crayfish, Procambarus clarkii (Girard). Cell Tissue Res 243(2):273–288. https://doi.org/10.1007/bf00251041
Kuris AM, Ra’anan Z, Sagi A, Cohen D (1987) Morphotypic differentiation of male Malaysian giant prawns, Macrobrachium Rosenbergii. J Crustac Biol 7(2):219–237. https://doi.org/10.2307/1548603
Leung PS, Brennan GP, Halton DW, Shaw C, Maule AG, Irvine GB (1994a) Immunocytochemical localization of neuropeptide F-immunoreactivity in the circumoesophageal ganglia of the gastropod mollusc, Helix aspersa using electron microscopy. Tissue Cell 26(1):115–122. https://doi.org/10.1016/0040-8166(94)90087-6
Leung PS, Shaw C, Johnston CF, Irvine GB (1994b) Immunocytochemical distribution of neuropeptide F (NPF) in the gastropod mollusc, Helix aspersa, and in several other invertebrates. Cell Tissue Res 275(2):383–393
Miyazaki T, Lin TY, Ito K, Lee CH, Stopfer M (2015) A gustatory second-order neuron that connects sucrose-sensitive primary neurons and a distinct region of the gnathal ganglion in the Drosophila brain. J Neurogenet 29(2–3):144–155. https://doi.org/10.3109/01677063.2015.1054993
Nagata S (2016) Chapter 41— neuropeptide F A2—Takei, Yoshio. In: Ando H, Tsutsui K (eds) Handbook of hormones. Academic Press, San Diego, pp 355–356
Nassel DR, Wegener C (2011) A comparative review of short and long neuropeptide F signaling in invertebrates: any similarities to vertebrate neuropeptide Y signaling? Peptides 32(6):1335–1355. https://doi.org/10.1016/j.peptides.2011.03.013
Pasztor VM (1968) The neurophysiology of respiration in decapod crustacea. I The motor system. Can J Zool 46(3):585–596
Poljaroen J, Tinikul Y, Phoungpetchara I, Kankoun W, Suwansa-ard S, Siangcham T et al (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(1):121–129. https://doi.org/10.1016/j.aquaculture.2011.08.022
Ranjeet K, Kurup B (2002) Heterogeneous individual growth of Macrobrachium rosenbergii male morphotypes. NAGA 25(2):13–18
Reichert H, Plummer MR, Hagiwara G, Roth RL, Wine JJ (1982) Local interneurons in the terminal abdominal ganglion of the crayfish. J Comp Physiol 149(2):145–162. https://doi.org/10.1007/bf00619210
Roller L, Yamanaka N, Watanabe K, Daubnerova I, Zitnan D, Kataoka H et al (2008) The unique evolution of neuropeptide genes in the silkworm Bombyx mori. Insect Biochem Mol Biol 38(12):1147–1157. https://doi.org/10.1016/j.ibmb.2008.04.009
Rungsin W, Paankhao N, Na-Nakorn U (2006) Production of all-male stock by neofemale technology of the Thai strain of freshwater prawn, Macrobrachium rosenbergii. Aquaculture 259(1):88–94. https://doi.org/10.1016/j.aquaculture.2006.05.041
Saetan J, Senarai T, Tamtin M, Weerachatyanukul W, Chavadej J, Hanna PJ et al (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(3):493–510. https://doi.org/10.1007/s00441-013-1650-6
Siangcham T, Tinikul Y, Poljaroen J, Sroyraya M, Changklungmoa N, Phoungpetchara I et al (2013) The effects of serotonin, dopamine, gonadotropin-releasing hormones, and corazonin, on the androgenic gland of the giant freshwater prawn, Macrobrachium rosenbergii. Gen Comp Endocrinol 193(supplement C):10–18. https://doi.org/10.1016/j.ygcen.2013.06.028
Smarandache-Wellmann CR (2016) Arthropod neurons and nervous system. Curr Biol 26(20):R960–R965. https://doi.org/10.1016/j.cub.2016.07.063
Spittaels K, Verhaert P, Shaw C, Johnston RN, Devreese B, Van Beeumen J et al (1996) Insect neuropeptide F (NPF)-related peptides: isolation from Colorado potato beetle (Leptinotarsa decemlineata) brain. Insect Biochem Mol Biol 26(4):375–382
Suwansa-Ard S, Thongbuakaew T, Wang T, Zhao M, Elizur A, Hanna PJ et al (2015) In silico neuropeptidome of female Macrobrachium rosenbergii based on transcriptome and peptide mining of eyestalk, central nervous system and ovary. PLoS One 10(5):e0123848. https://doi.org/10.1371/journal.pone.0123848
Thongrod S, Changklungmoa N, Chansela P, Siangcham T, Kruangkum T, Suwansa-Ard S et al (2017) Characterization and tissue distribution of neuropeptide F in the eyestalk and brain of the male giant freshwater prawn, Macrobrachium rosenbergii. Cell Tissue Res 367(2):181–195. https://doi.org/10.1007/s00441-016-2538-z
Thongrod S, Wanichanon C, Kankuan W, Siangcham T, Phadngam S, Morani F et al (2018) Autophagy-associated shrinkage of the hepatopancreas in fasting male Macrobrachium rosenbergii is rescued by neuropeptide F. Front Physiol 9:613. https://doi.org/10.3389/fphys.2018.00613
Tinikul Y, Engsusophon A, Kruangkum T, Thongrod S, Tinikul R, Sobhon P (2017) Neuropeptide F stimulates ovarian development and spawning in the female giant freshwater prawn, Macrobrachium rosenbergii, and its expression in the ovary during ovarian maturation cycle. Aquaculture 469(Supplement C):128–136. https://doi.org/10.1016/j.aquaculture.2016.11.026
Van Wielendaele P, Dillen S, Zels S, Badisco L, Vanden Broeck J (2013a) Regulation of feeding by neuropeptide F in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 43(1):102–114. https://doi.org/10.1016/j.ibmb.2012.10.002
Van Wielendaele P, Wynant N, Dillen S, Badisco L, Marchal E, Vanden Broeck J (2013b) In vivo effect of neuropeptide F on ecdysteroidogenesis in adult female desert locusts (Schistocerca gregaria). J Insect Physiol 59(6):624–630. https://doi.org/10.1016/j.jinsphys.2013.03.005
Van Wielendaele P, Wynant N, Dillen S, Zels S, Badisco L, Vanden Broeck J (2013c) Neuropeptide F regulates male reproductive processes in the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 43(3):252–259. https://doi.org/10.1016/j.ibmb.2012.12.004
Voigt R, Atema J (1992) Tuning of chemoreceptor cells of the second antenna of the American lobster (Homarus americanus) with a comparison of four of its other chemoreceptor organs. J Comp Physiol A 171(5):673–683. https://doi.org/10.1007/bf00194115
Wilkens JL (1976) Neuronal control of respiration in decapod crustacea. Fed Proc 35(9):2000–2006
Acknowledgments
We extend our gratitude to Capt. Piyachat Chansela, Dr. Morakot Sroyraya, Dr. Thanapong Kruangkum and Ms. Sineenart Songkoomkrong for their suggestions and technical advices.
Funding
This research was supported by a grant from the Office of Higher Education Commission (OHEC) and Mahidol University (MU) under the National Research University Initiatives and an OHEC-MU-Thailand Research Fund (TRF) Distinguished Research Professor Grant to Prasert Sobhon. This study was also supported by the Thailand Research Fund—the Royal Golden Jubilee Ph.D. Programme (TRF-RGJ Ph.D., PHD/0093/2553) co-funded by Mahidol University to Chaitip Wanichanon and Sirorat Thongrod and by National Research Council of Thailand (NRCT) scholarship (2016) to Sirorat Thongrod.
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Thongrod, S., Wanichanon, C. & Sobhon, P. Distribution of neuropeptide F in the ventral nerve cord and its possible role on testicular development and germ cell proliferation in the giant freshwater prawn, Macrobrachium rosenbergii. Cell Tissue Res 376, 471–484 (2019). https://doi.org/10.1007/s00441-019-02999-8
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DOI: https://doi.org/10.1007/s00441-019-02999-8