Biogenic Amines and Opiod Peptides

In Crustacea, biogenic amines function as neurotransmitters and neuromodulators, involving themselves in the regulation of a wide array of physiological activities (Table 9.2; Fig. 9.3) (Fingerman, 1997). Some amines also serve as neuroregulators that control the release of crustacean neurohormones. For instance, 5-HT stimulates the release of the crayfish hyperglycemic hormone, red pigment dispersing hormone, neurodepressing hormone, and MIH (Fingerman et al., 1994). The role of 5-HT in the ovarian development was first indicated by its stimulatory effect on the production of GSH in the brain and thoracic ganglia of the fiddler crab, U. pugilator (Richardson et al., 1991). Subsequently, Sarojini et al. (1995) demonstrated that 5-HT, under in vitro conditions, stimulated the release of GSH from the brain and thoracic ganglia of the crayfish P. clarkii. On the contrary, an endogenous opioid met-enkephalin inhibited ovarian development in the same crayfish by stimulating the GIH release from the XOSG and/or by a concomitant prohibition of the GSH release from the brain or thoracic ganglia.

In the spiny lobster Panulirus homarus, immunocytochemical localization of 5-HT in the brain and thoracic ganglia revealed a rise in the synthesis of this biogenic amine, correlated to ovarian maturation (Subramoniam and Kirubagaran, 2010). While the occurrence of 5-HT in the CNS has been reported in many more crustacean species, other forms of biogenic amines are also suggested to take part in the integrative control of ovarian maturation. For example, Sainath and Reddy (2011) found evidence that the freshwater crab Oziotelphusa senex senex responded to the injection of melatonin by increasing ovarian index, mean oocyte

Biogenic Amines and Opiods

Mode of Action

Site of Production

Target Organs/ Tissues

Species

Stimulation

Inhibition

Serotonin (5-HT)

Uca pugilator Procambarus clarkii Homarus americanus Libinia emarginata Litopenaeus stylirostris Liptopenaeus vannamei Penaeus vannamei Penaeus monodon Macrobrachium rosenbergii Oziotelphusa senex senex Anomalocera patersoni; Centropages typicus; Hemidiaptomus roubani Palaemon elegans

Ovarian development Agonists - ovarian maturation Testicular development Ovarian maturation Ovarian maturation and spawning Ovarian maturation and spawning Ovarian maturation and spawning VSH production and gonadal maturation Ovarian maturation Release of VSH Release of CHH

Low enhancement of eggextruding process Synthesis of MF from MO

XO-SG, brain, and TG XO-SG, brain, and TG XO-SG, brain, and TG

Gonads, HP, brain, and TG

XO-SG, brain and TG

XO-SG, brain, and TG

Melatonine

(N-acetyl-5-methoxy-

tryptamine)

Oziotelphusa senex senex Scylla serrata

Increased ovarian Vg levels

Hemolymph, eyestalk, and brain

Brain and TG

Dopamine (DA)

Procambarus clarkii Oziotelphusa senex senex Macrobrachium rosenbergii

Ovarian-stimulating action of 5-HT

Synthesis of VSH

XO-SG, brain and TG

CNS and ovary

Gonads, HP, brain, and TG

Leucine-enkephalin

Penaeus indicus Oziotelphusa senex senex

Mean ovarian index Mean ovarian index

CNS

Brain, TG, ovary, and HP

Methionine-

enkephalin

Procambarus clarkiii Procambarus clarkii

Decreased mean ovarian index Inhibits the synthesis of VSH

CNS

Brain, TG, ovary, and HP

Integrative role of biogenic amines

FIGURE 9.3 Integrative role of biogenic amines.

diameter, and ovarian vitellin level. Interestingly, acceleration of ovarian growth by melatonin was similar in both eyestalk-ablated and eyestalk-intact females.

An antagonistic role for the action of 5-HT in the stimulation of ovarian development by DA has been reported in a wide variety of decapod crustacean species. In the red swamp crayfish, Sarojini et al. (1995) demonstrated the in vitro inhibition by DA of 5-HT stimulated ovarian maturation. Using this antagonistic effect between these two amines, as well as their natural occurrence in the central nervous system, Alfaro et al. (2004) induced ovarian maturation and spawning in the penaeid shrimps, Litopenaeus stylirostris and L. vannamei by a combined treatment with 5-HT and the dopaminergic antagonist, spiperone. Chen et al. (2003) showed that in the giant freshwater river prawn M. rosenbergii the site of inhibitory action of DA against 5-HT was at the thoracic ganglia by inhibiting the release of GSH rather than enhancing secretion of VIH from XOSG. Furthermore, Meeratana et al. (2006) found supporting evidence on the inducement of ovarian maturation in M. rosenbergii by injecting 5-HT into the female carrying first stage (spent) ovary. Pretreatment with a 5-HT receptor antagonist, cyproheptadine, significantly suppressed the effect of this biogenic amine on ovarian inducement. Administration of 5-HT furthermore enhanced the synthesis and release of Vg into the hemolymph, in addition to increasing the total Vg mRNA in the hepatopancreas of this prawn (Kuo et al., 2009). However, the stimulation of Vg synthesis in hepatopancreas by 5-HT was complete only when it was injected into the eyestalk-ablated females. In a

Histological sections of ovarian tissues of Fenneropenaeus indicus on day 14 of treatment and stained with hematoxylin and eosin

FIGURE 9.4 Histological sections of ovarian tissues of Fenneropenaeus indicus on day 14 of treatment and stained with hematoxylin and eosin. Ovarian tissues from (A) control (10x), (B) 5-HT group (40x), (C) ESA group in early vitellogenic stage with numerous eosinophilic yolk granules in the peripheral ooplasm, (D) ESA group with early vitellogenic oocyte (100x), (E) 5-HT + ESA group with oocytes having club-shaped cortical rods extending toward the nucleus (10x), and (F) mature oocyte with cortical rods (40x). CR, cortical rod; Fl, follicle layer; N, nucleus; Yg, yolk granules. From Tomy, S., Saikrithi, P., James, N., Balasubramanian, C.P., Panigrahi, A., Otta, S.K., et al., 2016. Serotonin induced changes in the expression of ovarian gene network in the Indian white shrimp, Penaeus indicus. Aquaculture 452, 239-246. Fig. 1, p. 242; Elsevier, 2015.

recent study on the Indian white shrimp, Fenneropenaeus indicus, Tomy et al. (2016) found differential expression of ovarian genes involved in vitellogenesis (Vg and Vg receptor (VgR)) in serotonin-treated female shrimps. Increase in gene expression was, however, higher in the eyestalk-ablated females, after receiving serotonin treatment. Fig. 9.4 shows the effect of 5-HT and the combined effect of ESA on vitellogenesis in this penaeid shrimp. It is clear from these studies that 5-HT might not act directly on the ovary or other Vg synthetic sites to induce vitellogenesis, but it enhanced the release of gonad-stimulating neuropeptides in order that the latter can stimulate the proximate gonadotropic hormonal sources to initiate vitellogenesis, especially in the absence of VIH. Since the secretory activity of the biogenic amines is correlated to VIH and VSH release, a hierarchical control of biogenic amines on the synthesis and secretion of the regulatory neuropeptides of eyestalk and brain during the ovarian maturation is postulated (Fig. 9.3).

Tinikul et al. (2008) measured the levels of 5-HT and DA in the brain and thoracic ganglia along with the hemolymph Vg levels during the ovarian cycle of the freshwater prawn M. rosenbergii. They found a progressive increase of 5-HT in the brain during vitellogenesis, whereas the DA concentration showed a decreasing trend. Injection of 5-HT significantly increased the Vg concentration but the injection of DA and another neurotransmitter octopamine (OA) showed an opposite effect. Interestingly, the same result has also been found on the embryonic development in the brood. Delaying of brood development is also another way of slowing down the succeeding ovarian cycle in M. rosenbergii. Unless the brooded embryos are released, the next molting, which is a prerequisite for the ovulation, will not occur.

Tinikul et al. (2009) also observed a gradual rise in 5-HT in the ovary from stage I to IV of M. rosenbergii. On the contrary, DA concentration steadily decreased in the oocytes toward maturation of the ovary. It is of interest to note here that Ongvarrasopone et al. (2006) have reported expression of a 5-HT receptor, 5-HTI, in the membrane of mature oocyte in stages III and IV of the ovarian cycle in the tiger shrimp, P. monodon. Evidently, 5-HT may play a critical role in regulating meiotic maturation in this shrimp.

Different types of biogenic amines are synthesized in the CNS of crustaceans. In general, these biogenic amines can be categorized into two types with reference to their effect on the release of neuropeptides involved in the control of reproduction. The first category includes 5-HT/serotonin and melatonin having proven positive effect on the release of GSH from the brain and thoracic ganglion as described above. These compounds are derived from the amino acid tryptophan (see Fig. 9.5). The second category includes mainly the DA which shows an antagonistic action against 5-HT in inducing the release of GSH. Incidentally DA is a derivative of another aromatic amino acid namely tyrosine (see Fig. 9.5).

 
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