Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function

Matheson, Stephen; Levine, Richard B.

doi:10.1002/(sici)1097-4695(199901)38:1<27::aid-neu3>3.0.co;2-u

Cited by 39 publications

(9 citation statements)

References 80 publications

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“…Hormones can influence dendritic and axonal structure both in vertebrates and invertebrates (DeVoogd and Nottebohm, 1981; Cooke and Woolley, 2005; Williams and Truman, 2005). In insects, ecdysteroids, which drive metamorphosis and act as sex hormones, are thought to influence dendritic and axonal growth and branching (Bowen et al, 1984; Truman and Reiss, 1988, 1995; Weeks and Ernst-Utzschneider, 1989; Levine et al, 1991; Prugh et al, 1992; Kraft et al, 1998; Matheson and Levine, 1999; Cayre et al, 2000; Williams and Truman, 2005; Horch et al, 2011). For example, during metamorphosis in Manduca and Drosophila , certain classes of CNS motor neurons dramatically reorganize their dendritic arborizations in response to shifts in hormones (Duch and Levine, 2000; Consoulas et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus

Pfister¹,

Johnson²,

Ellers³

et al. 2013

Front. Physiol.

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Dendrite and axon growth and branching during development are regulated by a complex set of intracellular and external signals. However, the cues that maintain or influence adult neuronal morphology are less well understood. Injury and deafferentation tend to have negative effects on adult nervous systems. An interesting example of injury-induced compensatory growth is seen in the cricket, Gryllus bimaculatus. After unilateral loss of an ear in the adult cricket, auditory neurons within the central nervous system (CNS) sprout to compensate for the injury. Specifically, after being deafferented, ascending neurons (AN-1 and AN-2) send dendrites across the midline of the prothoracic ganglion where they receive input from auditory afferents that project through the contralateral auditory nerve (N5). Deafferentation also triggers contralateral N5 axonal growth. In this study, we quantified AN dendritic and N5 axonal growth at 30 h, as well as at 3, 5, 7, 14, and 20 days after deafferentation in adult crickets. Significant differences in the rates of dendritic growth between males and females were noted. In females, dendritic growth rates were non-linear; a rapid burst of dendritic extension in the first few days was followed by a plateau reached at 3 days after deafferentation. In males, however, dendritic growth rates were linear, with dendrites growing steadily over time and reaching lengths, on average, twice as long as in females. On the other hand, rates of N5 axonal growth showed no significant sexual dimorphism and were linear. Within each animal, the growth rates of dendrites and axons were not correlated, indicating that independent factors likely influence dendritic and axonal growth in response to injury in this system. Our findings provide a basis for future study of the cellular features that allow differing dendrite and axon growth patterns as well as sexually dimorphic dendritic growth in response to deafferentation.

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Section: Discussionmentioning

confidence: 99%

Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus

Pfister¹,

Johnson²,

Ellers³

et al. 2013

Front. Physiol.

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“…Our data demonstrate that ecdysone does not affect Kenyon cell morphology or branching complexity but only enhances neurite outgrowth. By contrast with Manduca motor neurons, which respond to 20‐hydroxyecdysone by increased branching at growth cones (Matheson & Levine 1999), the adult Kenyon cells from Acheta are similar to pupal Drosophila Kenyon cells, in which 20‐hydroxyecdysone enhances total neurite length but does not induce a selective increase of neuritic branching (Kraft et al . 1998).…”

Section: Discussionmentioning

confidence: 99%

“…1998). Recent data indicate that ecdysteroids enhance neuritic branching by altering growth cone structure and function (Matheson & Levine 1999). In contrast, the morphological development of cultured antennal lobe neurons from Manduca pupae was only weakly affected by addition of 20‐hydroxyecdysone to the culture medium (Oland & Hayashi 1993).…”

Section: Introductionmentioning

confidence: 99%

Dual effect of ecdysone on adult cricket mushroom bodies

Cayre

Strambi

et al. 2000

Eur J of Neuroscience

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Mushroom bodies, which are the main integrative centre for insect sensorial information, play a critical role in associative olfactory learning and memory. This paired brain structure contains interneurons grouped in a cortex, sending their axons into organized neuropiles. In the house cricket (Acheta domesticus) brain, persistent neuroblasts proliferate throughout adult life. Juvenile hormone (JH) has been shown to stimulate this proliferation [Cayre, M., Strambi, C. & Strambi, A. (1994) Nature, 368, 57-59]. In the present study, the effect of morphogenetic hormones on mushroom body cells maintained in primary culture was examined. Whereas JH did not significantly affect neurite growth, ecdysone significantly stimulated neurite elongation. Moreover, ecdysone also acted on neuroblast proliferation, as demonstrated by the reduced number of cells labelled with 5-bromodeoxyuridine following ecdysone application. Heterospecific antibodies raised against ecdysone receptor protein and ultraspiracle protein, the two heterodimers of ecdysteroid receptors, showed positive immunoreactivity in nervous tissue extracts and in nuclei of mushroom body cells, indicating the occurrence of putative ecdysteroid receptors in cricket mushroom body cells. These data indicate a dual role for ecdysone in adult cricket mushroom bodies: this hormone inhibits neuroblast proliferation and stimulates interneuron differentiation. These results suggest that a constant remodelling of mushroom body structure could result from physiological changes in hormone titres during adult life.

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“…contribute to increased network connectivity (Portera-Cailliau et al, 2005). Although both mechanisms can occur simultaneously in the same neuron, the relative importance of splitting versus interstitial branching is highly divergent from one neuron type to the other (Bastmeyer and O'Leary, 1996;Matheson and Levine, 1999;Portera-Cailliau et al, 2005).…”

Section: Axon Growthmentioning

confidence: 99%

Cellular and molecular mechanisms underlying axon formation, growth, and branching

Lewis

Courchet

Polleux

2013

Journal of Cell Biology

155

126

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Proper brain wiring during development is pivotal for adult brain function. Neurons display a high degree of polarization both morphologically and functionally, and this polarization requires the segregation of mRNA, proteins, and lipids into the axonal or somatodendritic domains. Recent discoveries have provided insight into many aspects of the cell biology of axonal development including axon specification during neuronal polarization, axon growth, and terminal axon branching during synaptogenesis.

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Steroid hormone enhancement of neurite outgrowth in identified insect motor neurons involves specific effects on growth cone form and function

Cited by 39 publications

References 80 publications

Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus

Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus

Dual effect of ecdysone on adult cricket mushroom bodies

Cellular and molecular mechanisms underlying axon formation, growth, and branching

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