Developmental changes in postnatal murine intestinal interstitial cell of cajal network structure and function

Annals of Biomedical Engineering

Volumn 42, Issue 8, 2014, Pages 1729-1739

  Gao, Jerry ^a   Sathar, Shameer ^a   O'Grady, Gregory ^a,b   Han, Juan ^c   Cheng, Leo K ^a,d  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c The 324 Hospital of PLA   (China)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Confocal microscopy; Gastrointestinal; Pruning

Indexed keywords

CONFOCAL MICROSCOPY; CURRICULA; MAMMALS; PACEMAKERS;

COMPUTATIONAL MODEL; DEVELOPMENTAL CHANGES; FUNCTIONAL OUTPUTS; GASTROINTESTINAL; GASTROINTESTINAL TRACT; INTERSTITIAL CELLS OF CAJAL; POSTNATAL DEVELOPMENT; PRUNING;

DIGESTIVE SYSTEM;

CALCIUM ION;

ANIMAL CELL; ARTICLE; CELL DENSITY; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CELL VOLUME; INTERSTITIAL CELL OF CAJAL; ION CURRENT; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SIMULATION; SMALL INTESTINE; AGING; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL RHYTHM; CYTOLOGY; PHYSIOLOGY;

AGING; ANIMALS; BIOLOGICAL CLOCKS; INTERSTITIAL CELLS OF CAJAL; MICE, INBRED BALB C;

EID: 84904384625     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-014-1021-9     Document Type: Article

References (36)

1. Burns, A. J., R. R. Roberts, J. C. Bornstein, and H. M. Young. Development of the enteric nervous system and its role in intestinal motility during fetal and early postnatal stages. Semin. Pediatr. Surg. 18:196-205, 2009.
2. Corrias, A., and M. L. Buist. Quantitative cellular description of gastric slow wave activity. Am. J. Physiol. Gastrointest. Liver Physiol. 294:G989-G995, 2008.
3. Du, P., G. O'Grady, S. J. Gibbons, R. Yassi, R. Lees-Green, G. Farrugia, L. K. Cheng, and A. J. Pullan. Tissue-specific mathematical models of slow wave entrainment in wild-type and 5-HT(2B) knockout mice with altered interstitial cells of Cajal networks. Biophys. J. 98:1772-1781, 2010.
4. Farrugia, G. Interstitial cells of Cajal in health and disease. Neurogastroenterol. Motil. 20:54-63, 2008.
5. Faussone-Pellegrini, M. S. Morphogenesis of the special circular muscle layer and of the interstitial cells of Cajal related to the plexus muscularis profundus of mouse intestinal muscle coat. Anat. Embryol. 169:151-158, 1984.
6. Faussone-Pellegrini, M. S. Cytodifferentiation of the interstitial cells of Cajal related to the myenteric plexus of mouse intestinal muscle coat. Anat. Embryol. 171:163-169, 1985.
7. Foong, J. P. P., T. V. Nguyen, J. B. Furness, J. C. Bornstein, and H. M. Young. Myenteric neurons of the mouse small intestine undergo significant electrophysiological and morphological changes during postnatal development. J. Physiol. 590:2375-2390, 2012.
8. Gao, J., P. Du, R. Archer, G. O'Grady, S. J. Gibbons, G. Farrugia, L. K. Cheng, and A. J. Pullan. A stochastic multi-scale model of electrical function in normal and depleted ICC networks. IEEE Trans. Biomed. Eng. 58:3451-3455, 2011.
9. Gao, J., P. Du, G. O'Grady, R. Archer, G. Farrugia, S. J. Gibbons, and L. K. Cheng. Numerical metrics for automated quantification of interstitial cell of Cajal network structural properties. J. R. Soc. Interface 10:20130421, 2013.
10. Henning, S. J. Postnatal development: coordination of feeding, digestion, and metabolism. Am. J. Physiol. Gastrointest. Liver Physiol. 241:G199-G214, 1981.
11. Henriquez, C. S. Simulating the electrical behavior of cardiac tissue using the bidomain model. Crit. Rev. Biomed. Eng. 21:1-77, 1993.
12. Huizinga, J. D., L. Thuneberg, M. Klüppel, J. Malysz, H. B. Mikkelsen, and A. Bernstein. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 373:347-349, 1995.
13. Kenny, S., J. Vanderwinden, R. Rintala, M. Connell, D. Lloyd, J. Vanderhaegen, and M. De Laet. Delayed maturation of the interstitial cells of Cajal: a new diagnosis for transient neonatal pseudoobstruction. Report of two cases. J. Pediatr. Surg. 33:94-98, 1998.
14. Klein, S., B. Seidler, A. Kettenberger, A. Sibaev, M. Rohn, R. Feil, H. D. Allescher, J. M. Vanderwinden, F. Hofmann, M. Schemann, R. Rad, M. A. Storr, R. M. Schmid, G. Schneider, and D. Saur. Interstitial cells of Cajal integrate excitatory and inhibitory neurotransmission with intestinal slow-wave activity. Nat. Commun. 4:1630, 2013.
15. Klüppel, M., J. D. Huizinga, J. Malysz, and A. Bernstein. Developmental origin and Kit-dependent development of the interstitial cells of Cajal in the mammalian small intestine. Dev. Dyn. 211:60-71, 1998.
16. Klüppel, M., D. L. Nagle, M. Bucan, and A. Bernstein. Long-range genomic rearrangements upstream of Kit dysregulate the developmental pattern of Kit expression in W57 and Wbanded mice and interfere with distinct steps in melanocyte development. Development 124:65-77, 1997.
17. Komuro, T., and D. S. Zhou. Anti-c-kit protein immunoreactive cells corresponding to the interstitial cells of Cajal in the guinea-pig small intestine. J. Auton. Nerv. Syst. 61:169-174, 1996.
18. Liu, L., L. Thuneberg, and J. Huizinga. Development of pacemaker activity and interstitial cells of Cajal in the neonatal mouse small intestine. Dev. Dyn. 213:271-282, 1998.
19. Low, L. K., and H. J. Cheng. A little nip and tuck: axon refinement during development and axonal injury. Curr. Opin. Neurobiol. 15:549-556, 2005.
20. Low, L. K., and H. J. Cheng. Axon pruning: an essential step underlying the developmental plasticity of neuronal connections. Philos. Trans. R. Soc. Lond. B 361:1531-1544, 2006.
21. Luo, L., and D. D. M. O'Leary. Axon retraction and degeneration in development and disease. Annu. Rev. Neurosci. 28:127-156, 2005.
22. Maeda, H., A. Yamagata, S. Nishikawa, K. Yoshinaga, S. Kobayashi, K. Nishi, and S. Nishikawa. Requirement of c-kit for development of intestinal pacemaker system. Development 116:369-375, 1992.
23. Mei, F., J. Zhu, S. Guo, D. S. Zhou, J. Han, B. Yu, S. F. Li, Z. Y. Jiang, and C. J. Xiong. An age-dependent proliferation is involved in the postnatal development of interstitial cells of Cajal in the small intestine of mice. Histochem. Cell Biol. 131:43-53, 2009.
24. Mirams, G. R., C. J. Arthurs, M. O. Bernabeu, R. Bordas, J. Cooper, A. Corrias, Y. Davit, S. J. Dunn, A. G. Fletcher, D. G. Harvey, M. E. Marsh, J. M. Osborne, P. Pathmanathan, J. Pitt-Francis, J. Southern, N. Zemzemi, and D. J. Gavaghan. Chaste: an open source C++ library for computational physiology and biology. PLoS Comput. Biol. 9:e1002970, 2013.
25. O'Grady, G., T. R. Angeli, P. Du, C. Lahr, W. J. E. P. Lammers, J. A. Windsor, T. L. Abell, G. Farrugia, A. J. Pullan, and L. K. Cheng. Abnormal initiation and conduction of slow-wave activity in gastroparesis, defined by high-resolution electrical mapping. Gastroenterology 143:589-598, 2012.
26. Park, K., G. Hennig, H. Lee, N. Spencer, S. Ward, T. Smith, and K. Sanders. Spatial and temporal mapping of pacemaker activity in interstitial cells of Cajal in mouse ileum in situ. Am. J. Physiol. Cell Physiol. 290:C1411-C1427, 2006.
27. Rich, A., M. Hanani, L. G. Ermilov, J. Malysz, V. Belzer, J. H. Szurszewski, and G. Farrugia. Physiological study of interstitial cells of Cajal identified by vital staining. Neurogastroenterol. Motil. 14:189-196, 2002.
28. Sathar, S., M. L. Trew, P. Du, G. O'Grady, and L. K. Cheng. A biophysically based finite-state machine model for analyzing gastric experimental entrainment and pacing recordings. Ann. Biomed. Eng. 42:858-870, 2014.
29. Schäfer, K. H., A. Hänsgen, and P. Mestres. Morphological changes of the myenteric plexus during early postnatal development of the rat. Anat. Rec. 256:20-28, 1999.
30. Tharayil, V. S., M. M. Wouters, J. E. Stanich, J. L. Roeder, S. Lei, A. Beyder, P. J. Gomez-Pinilla, M. D. Gershon, L. Maroteaux, S. J. Gibbons, and G. Farrugia. Lack of serotonin 5-HT2B receptor alters proliferation and network volume of interstitial cells of Cajal in vivo. Neurogastroenterol. Motil. 22:462-469, 2010.
31. Torihashi, S., T. Fujimoto, C. Trost, and S. Nakayama. Calcium oscillation linked to pacemaking of interstitial cells of Cajal: requirement of calcium influx and localization of TRP4 in caveolae. J. Biol. Chem. 277:19191-19197, 2002.
32. Torihashi, S., S. M. Ward, S. I. Nishikawa, K. Nishi, S. Kobayashi, and K. M. Sanders. C-kit-dependent development of interstitial cells and electrical activity in the murine gastrointestinal tract. Cell Tissue Res. 280:97-111, 1995.
33. Torihashi, S., S. Ward, and K. Sanders. Development of c-Kit-positive cells and the onset of electrical rhythmicity in murine small intestine. Gastroenterology 112:144-155, 1997.
34. van Helden, D. F., D. R. Laver, J. Holdsworth, and M. S. Imtiaz. Generation and propagation of gastric slow waves. Clin. Exp. Pharmacol. Physiol. 37:516-524, 2010.
35. Vanderwinden, J., H. Liu, M. De Laet, and J. Vanderhaeghen. Study of the interstitial cells of Cajal in infantile hypertrophic pyloric stenosis. Gastroenterology 111:279-288, 1996.
36. Ward, S. M., T. Ördög, S. D. Koh, S. Abu Baker, J. Y. Jun, G. Amberg, K. Monaghan, and K. M. Sanders. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J. Physiol. 525:355-361, 2000.