The first intestinal motility patterns in fetal mice are not mediated by neurons or interstitial cells of Cajal

Roberts, Rachael R.; Ellis, Melina; Gwynne, Rachel M; Bergner, Annette J.; Lewis, Martin; Beckett, Elizabeth; Bornstein, Joel C.; Young, Heather M.

doi:10.1113/jphysiol.2009.185421

Cited by 90 publications

(95 citation statements)

References 55 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The developmental aspects of spontaneous rhythmic activity in vitro and of motor complexes in vivo have been studied in some detail before (1,2,(5)(6)(7)30). Slow waves generated by interstitial cells of Cajal can be detected in mice some 6 h after birth (5) having a similar frequency as the rhythmic contractions at 37 o C in our study.…”

Section: Articlessupporting

confidence: 56%

Neonatal mouse ileum: functional properties and protein composition of the contractile machinery

et al. 2014

View full text Add to dashboard Cite

Background: Immature motility of the ileum may contribute to life-threatening diseases. Little is known about the normal biomechanics of the neonatal ileum in relation to the protein composition of its contractile machinery. Methods: We analyzed the tissue architecture, the biomechanics in intact and β-escin-permeabilized preparations, and the protein composition in neonatal (P0) and adult murine ileum. results: Muscle thickness of the P0 ileum was −50% of the adult ileum and passive compliance was higher. Carbachol-and KCl-elicited contractions were tonic rather than phasic as in the adult. Ca 2+ sensitivity was higher and relaxation rate was slower in β-escin-permeabilized P0 compared with adult ileum. The expression level of β-actin relative to α-actin was higher, and those of total actin, myosin, myosin light chain kinase, the catalytic subunit of myosin phosphatase and telokin were lower compared with the adult. The expression level of MYPT1 was similar, but P0 ileum expressed only the M133; the adult ileum also expressed the M130 isoform. conclusion: The mechanical features and protein composition of the P0 ileum are similar to those of adult tonic smooth muscles. We propose that this is highly adaptive during fetal life allowing the small intestine to act predominantly as a container. d uring development from fetal to newborn and adult life, the gastrointestinal tract (GIT) gradually establishes its mature structure and function. Anatomic features of the digestive tract are present already in human fetal life by 8 wk gestational age (1). However, gastrointestinal motility of preterm individuals is reduced (2). Obviously, this poses severe problems regarding oral food intake which are aggravated by the fact that the immaturity of the GIT, singly or in concert with other perinatal risk factors, may contribute to complications such as spontaneous intestinal perforation, not uncommon in extremely low-birth-weight infants (3). The underlying cause of spontaneous intestinal perforation, one of the leading risk factors of death in neonatal medicine, is still poorly understood. Conceivably an immature intestinal motility is an important determinant leading to stasis of the intestinal contents and overgrowth of infectious enteritis pathogens (4). The ensuing inflammatory response leads to a viscous cycle by not only further impairing of propulsive gut movements but also derogating vascular smooth muscle (SM) function, leading to reduced blood supply and finally to necrosis.Intestinal motility is driven by the concerted action of enteric neurons, pacemaker, and SM cells (2). Although several studies addressed different aspects of the fetal and postnatal maturation of innervation, electrical activity, and global contractile activity of the GIT (5-7), only few studies addressed in some depth the properties of the downstream effector, the SM. Investigations from avian (8) and mammalian stomach (9-11), and guinea pig gallbladder (12) as well as from non-GIT organs like urinary bladder (13,14), revealed major difference...

show abstract

Section: Articlessupporting

confidence: 56%

Neonatal mouse ileum: functional properties and protein composition of the contractile machinery

et al. 2014

View full text Add to dashboard Cite

show abstract

“…It is likely that these two oscillations originate at two discrete locations within the colonic wall, with one set of pacemakers perhaps close to the myenteric plexus and the other at the submucosal border, as has been described in the dog colon (38). It is also possible that these second type of ripples we observed may not be due to underlying slow waves (33).…”

Section: Two Types Of Myogenic Pacemaker Activity In the Proximal Colmentioning

confidence: 59%

“…Ripples are myogenic in origin since they were not blocked by tetrodotoxin. Although during development "ripples" may be generated by smooth muscle (33), in the adult animals they are most likely generated by intrinsic networks of interstitial cells of Cajal (ICCs) that act as pacemakers (22), driving smooth muscle slow waves, which generate muscle contractions. Electromyographic recording from proximal and distal colon showed slow waves with very similar frequencies to the myogenic ripples recorded in the present study (1,34) and which occur with a similar, relatively low frequency along the entire colon.…”

Section: Myogenic Motor Activity In All Regions Of Rabbit Colonmentioning

confidence: 99%

Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon

Dinning

Costa

Brookes

et al. 2012

American Journal of Physiology-Gastrointestinal and Liver Physi

View full text Add to dashboard Cite

Dinning PG, Costa M, Brookes SJ, Spencer NJ. Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon. Am J Physiol Gastrointest Liver Physiol 303: G83-G92, 2012. First published May 3, 2012 doi:10.1152/ajpgi.00429.2011The rabbit colon consists of four distinct regions. The motility of each region is controlled by myogenic and neurogenic mechanisms. Associating these mechanisms with specific motor patterns throughout all regions of the colon has not previously been achieved. Three sections of the colon (the proximal, mid, and distal colon) were removed from euthanized rabbits. The proximal colon consists of a triply teniated region and a single tenia region. Spatio-temporal maps were constructed from video recordings of colonic wall diameter, with associated intraluminal pressure recorded from the aboral end. Hexamethonium (100 M) and tetrodotoxin (TTX; 0.6 M) were used to inhibit neural activity. Four distinct patterns of motility were detected: 1 myogenic and 3 neurogenic. The myogenic activity consisted of circular muscle (CM) contractions (ripples) that occurred throughout the colon and propagated in both antegrade (anal) and retrograde (oral) directions. The neural activity of the proximal colon consisted of slowly (0.1 mm/s) propagating colonic migrating motor complexes, which were abolished by hexamethonium. These complexes were observed in the region of the proximal colon with a single band of tenia. In the distal colon, tetrodotoxin-sensitive, thus neurally mediated, but hexamethonium-resistant, peristaltic (anal) and antiperistaltic (oral) contractions were identified. The distinct patterns of neurogenic and myogenic motor activity recorded from isolated rabbit colon are specific to each anatomically distinct region. The regional specificity motor pattern is likely to facilitate orderly transit of colonic content from semi-liquid to solid composition of feces.colon; ripples; peristalsis; antiperistalsis; non-nicotinic transmission CONTROLLED PROPULSION AND MIXING of content along the digestive tract is essential for normal life. This is achieved by a repertoire of motor patterns that ensure net flow rates appropriate for the breakdown of food, absorption of nutrients, and excretion of waste. These movements are due to coordinated contractions and relaxations of the internal circular smooth muscle layer and the external longitudinal smooth muscle. These smooth muscle layers are controlled by both myogenic mechanisms [initiated by interstitial cells of Cajal (ICCs)] and neurogenic mechanisms (via the enteric nervous system), which interact to generate diverse motor patterns (21, 31).In the rabbit colon, four distinct colonic regions have been described (2,16,17,35,39). The first three regions form the proximal colon, and the fourth region comprises the distal colon. The first region is ϳ10 cm in length and is characterized by three bands of longitudinal muscle (tenia), which form the characteristic haustral pouches. The second region is ϳ20 cm in length and possesses a single ten...

show abstract

“…Although mice lacking ICC are able to swallow and obtain nutrition (Ward et al, 1994), postnatal blockade of ICC function results in profound cessation of peristalsis (Maeda et al, 1992), suggesting developmental compensation in the mice lacking ICC. Since a role for ICC in peristalsis appears to begin around birth (Roberts et al, 2010), impaired pacemaker function of ICC is unlikely to be developmentally compensated in our mice. Therefore, combined dysfunctional Ca 2+ signaling in ICC and esophageal smooth muscle may collaborate to abolish peristaltic waves necessary for swallowing.…”

Section: Discussionmentioning

confidence: 99%

Comparative phenotypic analysis of the two major splice isoforms of phosphatidylinositol phosphate kinase type Iγ in vivo

Legate

Montag

Böttcher

et al. 2012

Journal of Cell Science

View full text Add to dashboard Cite

Localized production of polyphosphoinositides is critical for their signaling function. To examine the biological relevance of specific pools of phosphatidylinositol 4,5-bisphosphate we compared the consequences of genetically ablating all isoforms of PIP kinase Type Iγ (PIPKIγ) versus ablation of a specific splice isoform, PIPKIγ_i2, with respect to three reported PIPKIγ functions. Ablation of PIPKIγ_i2 caused a neuron-specific endocytosis defect similar to that found in PIPKIγ −/− mice, while agonist-induced calcium signaling was blunted in PIPKIγ −/− cells, but was not affected in the absence of PIPKIγ_i2. A reported contribution of PIPKIγ to epithelial integrity was not evident in PIPKIγ −/− mice. As mice lacking PIPKIγ_i2 live a normal lifespan whereas PIPKIγ −/− mice die shortly after birth, we propose that PIPKIγ-mediated metabotropic calcium signaling may represent an essential function of PIPKIγ, whereas functions specific to the PIPKIγ_i2 splice isoform are not essential for survival.

show abstract

The first intestinal motility patterns in fetal mice are not mediated by neurons or interstitial cells of Cajal

Cited by 90 publications

References 55 publications

Neonatal mouse ileum: functional properties and protein composition of the contractile machinery

Neonatal mouse ileum: functional properties and protein composition of the contractile machinery

Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon

Comparative phenotypic analysis of the two major splice isoforms of phosphatidylinositol phosphate kinase type Iγ in vivo

Contact Info

Product

Resources

About