Sexual dimorphism of perineal muscles and motoneurons in spotted hyenas

Forger, Nancy G.; Frank, Laurence G.; Breedlove, S. Marc; Glickman, Stephen E.

doi:10.1002/(sici)1096-9861(19961111)375:2<333::aid-cne11>3.0.co;2-w

Cited by 47 publications

(29 citation statements)

References 57 publications

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“…Although the SNB neuromuscular system has been best studied in rats, the androgen dependence and developmental profile of the perineal muscles appears similar in mice (Wagner and Clemens, 1989;Forger et al, 1993;Park et al, 1999). Perineal muscle morphology is also altered by androgen manipulations during development in dogs, spotted hyenas, and gerbils (Forger and Breedlove, 1986;Forger et al, 1996;Siegford et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

Effects of Bax Gene Deletion on Muscle and Motoneuron Degeneration in a Sexually Dimorphic Neuromuscular System

Jacob

Bengston²,

Forger³

2005

Journal of Neuroscience

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Motoneurons in the spinal nucleus of the bulbocavernosus (SNB) and their target muscles in the perineum, bulbocavernosus (BC), and levator ani (LA) normally degenerate in female rodents. Death of the motoneurons and muscles can be prevented by androgen treatments around the time of birth. To identify the intracellular mechanisms underlying hormone-dependent survival of this neuromuscular system, we examined mice with a targeted disruption of the pro-death gene Bax. SNB motoneuron number was increased in female Bax؊/؊ mice, whether measured using immunolabeling for a motoneuron-specific marker or retrograde labeling with the fluorescent tracer Fluoro-Gold. Based on retrograde tracing, the sex difference in SNB cell number is eliminated in Bax؊/؊ mice. Thus, Bax is required for sexually dimorphic motoneuron death in the SNB, and motoneurons rescued by Bax deletion project their axons to the periphery. Mean soma size in the SNB of Bax؊/؊ females is reduced, however, and there is a subpopulation of very small cells in the SNB of female knock-outs. In addition, the BC muscle was not identified in any female, regardless of Bax gene status. All females possessed a small LA muscle, and Bax deletion resulted in a tripling of LA fiber number in females. This increase was small, however, relative to the Ͼ50-fold sex difference in LA muscle fiber number. Thus, the sex difference in the perineal muscles is mostly unaffected by the absence of Bax protein, and SNB motoneuron number is dissociated from target muscle size in Bax؊/؊ animals.

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Section: Discussionmentioning

confidence: 99%

Effects of Bax Gene Deletion on Muscle and Motoneuron Degeneration in a Sexually Dimorphic Neuromuscular System

Jacob

Bengston²,

Forger³

2005

Journal of Neuroscience

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“…Although the development of the SNB has been most intensively studied in rats, a similar sex difference (male > female) in the number of perineal motoneurons is seen in many mammals, including mice, gerbils, dogs, hyenas, monkeys, and humans (Forger and Breedlove, 1986;Wee et al, 1987;Ueyama et al, 1987;Ulibarri et al, 1995;Forger et al, 1996). In those cases in which it has been examined, these sex differences in other mammals also depend on differential exposure to androgens in males and females during development.…”

Section: Motoneuron Death and The Establishment Of Snb Cell Numbermentioning

confidence: 99%

The spinal nucleus of the bulbocavernosus: Firsts in androgen-dependent neural sex differences

Sengelaub

Forger

2008

Hormones and Behavior

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Cell number in the spinal nucleus of the bulbocavernosus (SNB) of rats was the first neural sex difference shown to differentiate under the control of androgens, acting via classical intracellular androgen receptors. SNB motoneurons reside in the lumbar spinal cord and innervate striated muscles involved in copulation, including the bulbocavernosus (BC) and levator ani (LA). SNB cells are much larger and more numerous in males than in females, and the BC/LA target muscles are reduced or absent in females. The relative simplicity of this neuromuscular system has allowed for considerable progress in pinpointing sites of hormone action, and identifying the cellular bases for androgenic effects. It is now clear that androgens act at virtually every level of the SNB system, in development and throughout adult life. In this review we focus on effects of androgens on developmental cell death of SNB motoneurons and BC/LA muscles; the establishment and maintenance of SNB motoneuron soma size and dendritic length; BC/LA muscle morphology and physiology; and behaviors controlled by the SNB system. We also describe new data on neurotherapeutic effects of androgens on SNB motoneurons after injury in adulthood.

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“…Internally, there are also sex differences in positioning of the retractor muscles, location of erectile tissues and surrounding fibroelastic tunica, and 'pleating' of the urogenital sinus (Neaves et al 1980, Cunha et al 2003, 2005. Treatment with anti-androgens during fetal life transforms the male penile phenotype into the clitoral phenotype of the female spotted hyena (Forger et al 1996, Drea et al 1998, Cunha et al 2005. Evidently, androgens arriving from the placenta (Licht et al 1992, Yalcinkaya et al 1993) are insufficient to 'masculinize' the female genital tubercle, which in males occurs between 30 and 45 days of gestational age (Cunha et al 2005).…”

Section: Introductionmentioning

confidence: 99%

Endocrine differentiation of fetal ovaries and testes of the spotted hyena (Crocuta crocuta): timing of androgen-independent versus androgen-driven genital development

Browne¹,

Place²,

Vidal³

et al. 2006

Reproduction

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Female spotted hyenas (Crocuta crocuta) have an erectile peniform clitoris and a pseudoscrotum but no external vagina, all established by day 35 of a 110-day gestation. Recent studies indicate that these events are androgen-independent, although androgen secretion by fetal ovaries and testis was hypothesized previously to induce phallic development in both sexes. We present the first data relating to the capacity of the ovaries and testes of the spotted hyena to synthesize androgens at different stages of fetal life. Specifically, spotted hyena fetal gonads were examined by immunohistochemistry at GD 30, 45, 48, 65, and 95 for androgen-synthesizing enzymes, as related to the morphological development. Enzymes included 17a-hydroxylase/17,20-lyase cytochrome P450 (P450c17), cytochrome b5, 3b-hydroxysteroid dehydrogenase (3bHSD), and cholesterol side-chain cleavage cytochrome P450 (P450scc). Anti-Mü llerian-hormone (AMH) expression was also examined. AMH was strongly expressed in fetal Sertoli cells from GD 30 and after. P450c17 expression was detected in Leydig cells of developing testes and surprisingly in Mü llerian duct epithelium. Fetal ovaries began to organize and differentiate by GD 45, and medullary cells expressed P450c17, cytochrome b5, 3bHSD, and P450scc. The findings support the hypothesis that external genital morphology is probably androgen-independent initially, but that fetal testicular androgens modify the secondary, male-specific phallic form and accessory organs. Fetal ovaries appear to develop substantial androgen-synthesizing capacity but not until phallic differentiation is complete, i.e. after GD 45 based on circulating androstenedione concentrations. During late gestation, fetal ovaries and testes synthesize androgens, possibly organizing the neural substrates of aggressive behaviors observed at birth in spotted hyenas. These data provide an endocrine rationale for sexual dimorphisms in phallic structure and reveal a potential source of androgenic support for neonatal aggression in female and male C. crocuta. Reproduction (2006) 132 649-659

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Sexual dimorphism of perineal muscles and motoneurons in spotted hyenas

Cited by 47 publications

References 57 publications

Effects of Bax Gene Deletion on Muscle and Motoneuron Degeneration in a Sexually Dimorphic Neuromuscular System

Effects of Bax Gene Deletion on Muscle and Motoneuron Degeneration in a Sexually Dimorphic Neuromuscular System

The spinal nucleus of the bulbocavernosus: Firsts in androgen-dependent neural sex differences

Endocrine differentiation of fetal ovaries and testes of the spotted hyena (Crocuta crocuta): timing of androgen-independent versus androgen-driven genital development

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