Abstract
Onuf’s nucleus is a small group of neurons located in the ventral horns of the sacral spinal cord. The motor neurons (MNs) of Onuf’s nucleus innervate striated voluntary muscles of the pelvic floor and are histologically and biochemically comparable to the other somatic spinal MNs. However, curiously, these neurons also show some autonomic-like features as, for instance, they receive a strong peptidergic innervation. The review provides an overview of the histological, biochemical, metabolic, and gene expression peculiarities of Onuf’s nucleus. Moreover, it describes the aging-related pathologies as well as several traumatic and neurodegenerative disorders in which its neurons are involved: indeed, Onuf’s nucleus is affected in Parkinson’s disease (PD) and Shy-Drager Syndrome (SDS), whereas it is spared in Amyotrophic Lateral Sclerosis (ALS), Spinal Muscular Atrophy (SMA), Duchenne Muscular Dystrophy (DMD). We summarize here the milestone studies that have contributed to clarifying the nature of Onuf’s neurons and in understanding what makes them either vulnerable or resistant to damage. Altogether, these works can offer the possibility to develop new therapeutic strategies for counteracting neurodegeneration.
Highlights
In 1899, for the first time, the Russian neuroanatomist Bronislaw Onuf (Onufrowicz) identified and described a group of neurons located in the human sacral spinal cord and involved in the innervation of the pelvic floor: he called this formation ‘‘nucleus X,’’ later renamed after him ‘‘Onuf’s nucleus.’’Onuf’s nucleus (Figure 1) has been identified in different locations through the species, similar in the cat, dog, monkey, and man, differently from the rat, Mongolian gerbil, and domestic pig
Despite the pelvic organ stimulating center (POSC) influences subcortical and cortical regions and several micturition centers are located in the cerebral cortex, basal ganglia, and brainstem (Fowler et al, 2008), no direct cortical projections to Onuf’s nuclei have been demonstrated in humans (Iwatsubo et al, 1990; Mannen, 2000); they were observed in South America monkey Saimiri, in which corticospinal projections start from the tail portion of cortical area 4 and end bilaterally on Onuf’s nuclei (Nakagawa, 1980)
Among the 14 opposite-regulated genes, some are involved in neurogenesis and apoptosis regulation (Ephrin type-A receptor 7, sparc/osteonectin1), in the regulation of proteins associated with the cytoskeleton (PDZ and LIM Domain 1), in the degradation of transmembrane proteins (Rasrelated protein RAB12), in the stabilization of cell membrane potential and maintenance of intracellular pH (CLIC1) and in receptor assembly and activity (e.g., Progestin and AdipoQ Receptor Family Member 8, gamma-aminobutyric acid type A receptor alpha1 subunit, Gamma-Aminobutyric Acid Type A Receptor Subunit β1; Allodi et al, 2019)
Summary
In 1899, for the first time, the Russian neuroanatomist Bronislaw Onuf (Onufrowicz) identified and described a group of neurons located in the human sacral spinal cord and involved in the innervation of the pelvic floor: he called this formation ‘‘nucleus X,’’ later renamed after him ‘‘Onuf’s nucleus.’’. Despite the POSC influences subcortical and cortical regions (e.g., hypothalamus, locus coeruleus, PAG, and the medial prefrontal cortex; Michels et al, 2015; Malykhina, 2017) and several micturition centers are located in the cerebral cortex, basal ganglia, and brainstem (Fowler et al, 2008), no direct cortical projections to Onuf’s nuclei have been demonstrated in humans (Iwatsubo et al, 1990; Mannen, 2000); they were observed in South America monkey Saimiri, in which corticospinal projections start from the tail portion of cortical area 4 and end bilaterally on Onuf’s nuclei (Nakagawa, 1980). The neurochemical properties of Onuf’s neurons have been initially studied since the later ‘80s It has been demonstrated, in both human and laboratory animals, that Onuf’s nucleus is densely innervated by CPON(C-terminal Flanking Peptide of Neuropeptide Y), enkephalinand somatostatin-immunopositive fibers, suggesting an autonomic nature of these cells. It is still unclear if either: (i) these MNs are more resistant to neuroinflammation per se; or (ii) the astrogliosis is less intense around these resistant nuclei; or (iii) astrocytes surrounding Onuf’s nucleus differently react to degeneration (Nijssen et al, 2017)
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