Myenteric plexus neurons have developmentally acquired differences in the medium molecular weight subunit of neurofilament protein

Eaker, Ervin Y.; Je, Sallustio; Jm, Harris; Shaw, Gerry

doi:10.1016/0306-4522(93)90221-z

Cited by 10 publications

(8 citation statements)

References 18 publications

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“…Positive cells increased in size during the perinatal period and represented the main population of neurons until 5 mo. Their proportion among neurons decreased thereafter to become minor during childhood, a finding consistent with previous observations by Eaker et al (18) in the postnatal period in rats using a panel of anti-NF antibody. Using NADPH diaphorase histochemistry, previously used for the indirect labeling of NO synthesizing cells, Brandt et al (19) also described a decrease in the density of stained neurons during the human fetal development, resulting in increased interspacing between myenteric ganglia.…”

Section: Discussionsupporting

confidence: 91%

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Fetal Intestinal Obstruction Induces Alteration of Enteric Nervous System Development in Human Intestinal Atresia

et al. 2004

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Intestinal motility disorders are a major cause of morbidity after surgical repair of intestinal atresia of unknown mechanism. We hypothesized that interruption of antenatal peristalsis may disturb the normal development of the enteric nervous system. Using a series of neuronal (synaptophysin, neuronal nitric oxide synthase, neurofilaments) and nonneuronal markers (glial acidic fibrillary protein and c-Kit) and immunohistochemistry, we have defined developmental steps of the enteric nervous system in normal intestine (12 fetuses, 15 children, and 4 adults) and their alterations above and below the obstacle in 22 human intestinal atresia compared with age-matched controls. Antisynaptophysin antibody revealed the progressive conversion of the myenteric plexus from a continuous belt into regularly spaced ganglions during normal fetal gut development and, by contrast, the significantly delayed appearance of individual neuronal ganglions in the distal segments of atresia (p Ͻ 0.05). Staging using three other markers for neuronal (neurofilaments and neuronal nitric oxide synthase) and nonneuronal cells (glial acidic fibrillary protein) confirmed that maturation of the myenteric plexus was significantly delayed below atresia (p Ͻ 0.01). These results indicate that intestinal atresia impairs the development of the enteric nervous system and provide an anatomical substrate for the motility disorders observed after surgical repair. They point to the role of peristalsis in normal gut development and suggest that stimulation of peristalsis might be used to accelerate recovery. Intestinal atresia is a common gut congenital disease with a prevalence of 2.8 for 10,000 births (1), detected by prenatal ultrasonography in the second or third trimester and confirmed at birth by intestinal obstruction. Treatment must be performed just after birth and consists of surgical resection of the atretic segment followed by primary anastomosis. Operative techniques and postoperative parenteral nutrition have improved the outcome, but prolonged intestinal motility disorders remain common in the postoperative period, even in the absence of any mechanical lesions (2). Although a dysfunction of the ENS has been suggested, the physiopathology of the motility disorders remains unknown (3,4).ENS comprises two main plexuses and schematically it can be assumed that the myenteric or Auerbach's plexus plays a major role in the regulation of motility and that the submucous or Meissner's plexus ensures regulation of intestinal secretion/ absorption (5,6). Intestinal motility appears early at 16 wk gestation (7) in fetal life and likely supports the nutritional function of the gut before birth (8,9). Intestinal atresia, by 0031-3998/04/5606-0975 PEDIATRIC RESEARCH Vol. 56, No. 6, 2004 Copyright © 2004 Printed in U.S.A. ABSTRACT975

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Section: Discussionsupporting

confidence: 91%

“…Twelve fetal intestines from 8 to 35 wk gestation (8,10,11,13,15,18,21,25,30,32,34, and 35 wk) were obtained from medical elective termination of pregnancies with the permission of the local ethical committee of Hôpital Necker Enfants-Malades. They were from jejunal and ileal portions of the gut.…”

Section: Patients and Tissue Collectionmentioning

confidence: 99%

Fetal Intestinal Obstruction Induces Alteration of Enteric Nervous System Development in Human Intestinal Atresia

et al. 2004

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“…On the other hand, there is the possibility that a selective decrease in the number of non-NF145 neurons after placement in culture without any change in the NF145-immunoreactive population may account for the increased proportion of NF145-immunoreactive neurons. The number of enteric neurons containing mediumsized neurofilaments reportedly was decreased or absent in the adult rat myenteric plexus (Eaker et al, 1993). Eaker and Sallustio (1998) found that the NF-M subunit was modified during the first week of culture for neonatal rat myenteric plexus and later disappeared entirely.…”

Section: Discussionmentioning

confidence: 98%

“…Developmental changes in the neurofilaments and their related proteins occur also in myenteric neurons of the neonatal enteric nervous system in culture outside the intestinal wall (Eaker et al, 1993;Eaker and Sallustio, 1998;Watanabe et al, 1997;Faussone-Pellegrini et al, 1999).…”

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confidence: 98%

“…In the peripheral nervous system, neurofilament protein triplets are found in the cell bodies and nerve fibers in celiac ganglia (Vickers et al, 1990), mesenteric ganglia , dorsal root ganglia , and enteric ganglia (Bjorklund et al, 1984;Costa et al, 1996). Neurofilament immunoreactivity (-IR) in the enteric nervous system is localized to a subgrouping of the neuronal population and differs from the central nervous system in this respect (Eaker et al, 1990(Eaker et al, , 1993Eaker and Sallustio, 1994). The existence of modified neurofilament structures in enteric neurons may reflect a compensatory adaptation that allows the neuron to function in the ever-changing spatial environment within the gut wall.…”

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confidence: 99%

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Chemical coding and electrophysiology of enteric neurons expressing neurofilament 145 in guinea pig gastrointestinal tract

Hu¹,

Gao²,

Zhong³

et al. 2001

J of Comparative Neurology

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Electrophysiologic recording and indirect immunofluorescence were combined to study localization of the medium-sized neurofilament 145 (NF145) component of the cytoskeleton in morphologically identified neurons in the myenteric and submucosal plexuses of the guinea pig enteric nervous system. Neuronal localization of chemical markers, including calbindin DK28, calretinin, nitric oxide synthase, choline-acetyltransferase, neuropeptide Y, serotonin, neurokinin 1 receptor protein, and somatostatin, was integrated with electrophysiologic and morphologic results for a more complete assessment. NF145 immunoreactivity (-IR) was present in ganglion cells with Dogiel type I morphology in the myenteric plexus of the stomach and small and large intestine. NF145-IR was not found in myenteric ganglion cells with Dogiel type II morphology. NF145-IR was not present in any of the ganglion cells in the submucosal plexus. NF145 was expressed in nerve fibers in both myenteric and submucosal plexuses. The majority of these fibers were identified as sympathetic postganglionic axons based on their disappearance in organotypic culture and on their expression of tyrosine hydroxylase. The myenteric ganglion cells with NF145-IR had electrophysiologic properties of S-type enteric neurons. NF145-IR was found in neurons with vasoactive intestinal peptide, serotonin, nitric oxide synthase, somatostatin, and neurokinin 1 receptor but not with neuropeptide Y or calbindin. The results in general suggest that NF145 is localized to distinct subsets of myenteric motor neurons and interneurons. Absence of NF145 from ganglion cells in the submucosal plexus is an example of differences between myenteric and submucosal components of the enteric nervous system.

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The cytoskeleton of the myenteric neurons during murine embryonic life

Faussone–Pellegrini

Matini

DeFelici

1999

Anatomy and Embryology

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The organization of the cytoskeleton has been studied during mouse differentiation in cells of the myenteric neuronal lineage. The entire gut was examined starting from day 12.5 of embryonic life (E12.5) until birth (P0). Immunocytochemistry was performed to evaluate the expression of five of the most represented neurofilaments proteins (the low, NF-L, medium, NF-M, and heavy, NF-H, molecular weight subunits, alpha-internexin and peripherin) and of two of the microtubule-associated proteins (MAPI and MAP2a+2b). In parallel, the appearance in the differentiating myenteric neurons of filamentous and microtubular structures and their intracytoplasmatic distribution were observed under the electron microscope. A differential immunohistochemical expression of the structural proteins was found. Immature cells expressed alpha-internexin, peripherin, NF-M and MAP1 by day E12.5; alpha-internexin expression was strong in these cells, but gradually decreased with age and was practically absent in adulthood. Conversely, the expression of the other three proteins increased with cell differentiation and was still present in adulthood. NF-L and NF-H expression appeared later, by day E16.5, and was weak for the entire pre- and postnatal life. MAP2a+2b was never expressed. Under the electron microscope, at day E12.5 the cytoskeleton was already organized in filamentous and microtubular structures. At this age neurofilaments were few and mainly located in the cell processes, and microtubules were numerous and mainly assembled in the neuritic growth cones, together with synaptic vesicles. With ageing, neurofilaments and microtubules were ubiquitous in the neuron. Data obtained demonstrate that cytoskeletal proteins gradually accumulate in the cells of the neuronal lineage in parallel with the organization of the cytoskeletal structures, which in turn mediate important neural events by the earliest stages of murine embryonic life, including growth of nerve processes and initiation of axonal transport.

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Myenteric plexus neurons have developmentally acquired differences in the medium molecular weight subunit of neurofilament protein

Cited by 10 publications

References 18 publications

Fetal Intestinal Obstruction Induces Alteration of Enteric Nervous System Development in Human Intestinal Atresia

Fetal Intestinal Obstruction Induces Alteration of Enteric Nervous System Development in Human Intestinal Atresia

Chemical coding and electrophysiology of enteric neurons expressing neurofilament 145 in guinea pig gastrointestinal tract

The cytoskeleton of the myenteric neurons during murine embryonic life

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