Specific requirement of putrescine for the mitogenic action of juvenile hormone on adult insect neuroblasts

Abstract

Persistent neurogenesis in an adult insect brain was recently shown to be stimulated by juvenile hormone (JH). This morphogenetic hormone was also shown to act on polyamine biosynthesis. To analyze the possible involvement of polyamines in the neurogenic action of JH, two series of experiments were carried out with adult female crickets, Acheta domesticus: (i) inhibition of the first key enzyme in polyamine biosynthesis, ornithine decarboxylase, with ␣-dif luoromethylornithine (␣-DFMO), and examination of the effects of this treatment on the neuroblast proliferation response to JH; and (ii) examination of the effects of putrescine supplementation on the mitotic index of JH-deprived and ␣-DFMO-treated females. In control females, ␣-DFMO treatment, as well as JH deprivation, greatly reduced neuroblast proliferation. Putrescine supplementation in ␣-DFMOtreated insects overcame the effects of ␣-DFMO, and allowed for detection of putrescine in the neural tissue and stimulation of brain neurogenesis. In JH-deprived females, ␣-DFMO treatment completely prevented the stimulatory action of JH on neuroblast proliferation and on brain putrescine levels. By contrast, putrescine feeding of JH-deprived animals was able to mimic the stimulatory effect of JH: brain putrescine levels increased and neuroblast proliferation was restored. To our knowledge, this report demonstrates for the first time that in vivo administration of putrescine can mimic the effects of a morphogenetic hormone on adult neuroblast proliferation, and shows the importance of polyamines, especially putrescine, in the transduction of JH message in neural tissue.The pleiotropic action of juvenile hormone (JH) in insects has been widely demonstrated (1-3). However, JH receptors have not yet been characterized, and, despite numerous attempts, the precise molecular mechanisms of action of JH are far from being understood (1-3). Recently, persistent neurogenesis modulated by hormones was demonstrated in one of the main integrative areas of adult cricket brain, the mushroom bodies (4, 5). † Neuroblast proliferation was depressed in the absence of JH, whereas JH injection significantly stimulated the mitotic activity of the proliferative area. Although in adult females the most studied role of JH is action on fat body and ovaries to induce vitellogenesis, it is now apparent that neural tissue is also a target for JH action. It has also been shown that in the neural tissue, lack of JH depresses the activities of ornithine decarboxylase (ODC) and S-adenosylmethionine decarboxylase (AdoMetDC), the two key enzymes in polyamine biosynthesis, resulting in a significant lowering of polyamine titres, an effect that was reversed by JH injection (7). In the cricket, oviposition behavior requires the action of JH, and a strong reduction of oviposition results from inhibition of ODC (8). These findings allowed us to hypothesize that JH can act through polyamine metabolism. The naturally occurring polyamines, putrescine, spermidine, and spermine, are ubiquitous polycati...

Metabolomic Analysis of Diapausing and Noni-diapausing Larvae of the European Corn Borer Ostrinia nubilalis (Hbn.) (Lepidoptera: Crambidae)

“…46 Putrescine has been shown to modulate the action of juvenile hormone during neural development in crickets. 47 The potential physiological role of putrescine in O. nubilalis larvae remains an open question.…”

Reproductive ground plan may mediate colony-level selection effects on individual foraging behavior in honey bees

“…In addition to their gonotrophic role, these hormones govern shifts between behavioral states in the reproductive cycle, e.g., by controlling the shift from nectar to blood-host foraging in female Culex nigripalpus mosquitoes (52), the shift from feeding and sexual behavior to fasting and parental activity in the earwig Labidura riparia (53), the initiation of oviposition in crickets (54), the initiation of sexual behavior of male Agrotis ipsilon moths (55), and shifts between periods of intense flight activity and reproductive behavior in several taxa (34). JH and ecdysteroids affect adult behavior by regulating the growth and central processing of sensory and motor neurons (26,(56)(57)(58)(59), and their coordinated regulatory modes have been shown to result in synchronized changes in sensory perception, locomotor activity, and reproductive physiology (26,60).…”

Hormonal and sensory inputs regulate distinct neuroblast cell cycle properties in adult cricket brain

“…4B) was significantly reduced by sensory deprivation (0.733 6 0.03 vs. 0.640 6 0.05; P ¼ 0.03), indicating a lengthening of the cell cycle in the hemisphere ipsilateral to the lesion. JH has been shown to stimulate neurogenesis via the polyamine pathway (Cayre et al, 1997), so we investigated whether polyamines were also involved in the stimulatory action of sensory inputs. Brains of unilaterally sensory-deprived crickets were divided into four parts: the protocerebron, the part containing the proliferative center, and the deuto-/tritocerebron ipsilateral or contralateral to the Fig.…”

“…Putrescine levels were determined by high-performance liquid chromatography according to methods previously described (Cayre et al, 1997). Because putrescine titers are very low in individual brains, experiments were conducted on pools of 12 brains.…”