Age-related changes in neurons containing neuronal nitric oxide synthase in the colon of rats
Petr M. Masliukov , Daria A. Aryaeva , Antonina F. Budnik
Morphology ›› 2021, Vol. 159 ›› Issue (4) : 145 -152.
Age-related changes in neurons containing neuronal nitric oxide synthase in the colon of rats
BACKGROUND: The density of both terminals in the circular muscle of the intestine increases sharply in the first 10 days of life. However, the age-related aspects of neuronal NO synthase (nNOS) expression in metasympathetic intramural enteric ganglia remain unclear.
AIM: To identify the localization, percentage, and morphometric characteristics of nNOS-immunoreactive (IR) neurons in the intramural ganglia of the myenteric plexus (MP) and submucous plexus (SP) of the large intestine of rats of different age groups.
MATERIAL AND METHODS: The study examined Wistar rats aged 1, 10, 20, 30, and 60 days and 2 years using immunohistochemical methods.
RESULTS: nNOS-IR neurons were found in the large intestine at birth and during the remaining periods. In the intramural ganglia of the MP, the largest percentage of nNOS-IR neurons was detected in newborn rats and decreased in ontogenesis up to 60 days of life and did not change until senescence. In the SP, nNOS-IR neurons were abundant in newborns, the percentage decreased significantly by day 20, and they were not detected in days 30 and 60, but again appeared in large numbers in older rats. The average cross-sectional area of nNOS-IR neurons increased in the MP from birth during the first 2 months of life. In the SP, the average size of nNOS-IR cells increased in the first 30 days of life and became significantly larger in old rats than in rats of other ages.
CONCLUSIONS: The expression of nNOS in intramural nodes’ neurons in the large intestine decreased in early postnatal ontogenesis and subsequently increased in aged rats.
rats / neuronal NO synthase / nNOS / intramural ganglia / large intestine / ontogenesis
| [1] |
Foong JP. Postnatal Development of the Mouse Enteric Nervous System. Adv Exp Med Biol. 2016;891:135–143. doi: 10.1007/978-3-319-27592-5_13 |
| [2] |
Foong J.P. Postnatal Development of the Mouse Enteric Nervous System // Adv Exp Med Biol. 2016. Vol. 891. P. 135–143. doi: 10.1007/978-3-319-27592-5_13 |
| [3] |
Foong JP, Tough IR, Cox HM, Bornstein JC. Properties of cholinergic and non-cholinergic submucosal neurons along the mouse colon. J Physiol. 2014;592(4):777–793. doi: 10.1113/jphysiol.2013.265686 |
| [4] |
Foong J.P., Tough I.R., Cox H.M., Bornstein J.C. Properties of cholinergic and non-cholinergic submucosal neurons along the mouse colon // J Physiol. 2014. Vol. 592, N 4. P. 777–793. doi: 10.1113/jphysiol.2013.265686 |
| [5] |
Sang Q, Young HM. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res. 1996;284(1):39–53. doi: 10.1007/s004410050565 |
| [6] |
Sang Q., Young H.M. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse // Cell Tissue Res. 1996. Vol. 284, N 1. P. 39–53. doi: 10.1007/s004410050565 |
| [7] |
Qu ZD, Thacker M, Castelucci P, et al. Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res. 2008;334(2):147–161. doi: 10.1007/s00441-008-0684-7 |
| [8] |
Qu Z.D., Thacker M., Castelucci P., et al. Immunohistochemical analysis of neuron types in the mouse small intestine // Cell Tissue Res. 2008. Vol. 334, N 2. P. 147–161. doi: 10.1007/s00441-008-0684-7 |
| [9] |
Furness JB. The enteric nervous system. Oxford: Blackwell Publishing; 2006. 288 p. |
| [10] |
Furness J.B. The enteric nervous system. Oxford: Blackwell Publishing, 2006. 288 p. |
| [11] |
Furness JB, Stebbing MJ. The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems. Neurogastroenterol Motil. 2018;30(2). doi: 10.1111/nmo.13234 |
| [12] |
Furness J.B., Stebbing M.J. The first brain: Species comparisons and evolutionary implications for the enteric and central nervous systems // Neurogastroenterol Motil. 2018. Vol. 30, N 2. doi: 10.1111/nmo.13234 |
| [13] |
Timmermans JP, Adriaensen D, Cornelissen W, Scheuermann DW. Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes. Comp Biochem Physiol A Physiol. 1997;118(2):331–340. doi: 10.1016/s0300-9629(96)00314-3 |
| [14] |
Timmermans J.P., Adriaensen D., Cornelissen W., Scheuermann D.W. Structural organization and neuropeptide distribution in the mammalian enteric nervous system, with special attention to those components involved in mucosal reflexes // Comp Biochem Physiol A Physiol. 1997. Vol. 118, N 2. P. 331–340. doi: 10.1016/s0300-9629(96)00314-3 |
| [15] |
Hao MM, Bornstein JC, Young HM. Development of myenteric cholinergic neurons in ChAT-Cre;R26R-YFP mice. J Comp Neurol. 2013;521(14):3358–3370. doi: 10.1002/cne.23354 |
| [16] |
Hao M.M., Bornstein J.C., Young H.M. Development of myenteric cholinergic neurons in ChAT-Cre;R26R-YFP mice // J Comp Neurol. 2013. Vol. 521, N 14. P. 3358–3370. doi: 10.1002/cne.23354 |
| [17] |
Vannucchi MG, Faussone-Pellegrini MS. Differentiation of cholinergic cells in the rat gut during pre- and postnatal life. Neurosci Lett. 1996;206(2-3):105–108. doi: 10.1016/s0304-3940(96)12440-x |
| [18] |
Vannucchi M.G., Faussone-Pellegrini M.S. Differentiation of cholinergic cells in the rat gut during pre- and postnatal life // Neurosci Lett. 1996. Vol. 206, N 2-3. P. 105–108. doi: 10.1016/s0304-3940(96)12440-x |
| [19] |
Hao MM, Fung C, Boesmans W, et al. Development of the intrinsic innervation of the small bowel mucosa and villi. Am J Physiol Gastrointest Liver Physiol. 2020;318(1):G53–G65. doi: 10.1152/ajpgi.00264.2019 |
| [20] |
Hao M.M., Fung C., Boesmans W., et al. Development of the intrinsic innervation of the small bowel mucosa and villi // Am J Physiol Gastrointest Liver Physiol. 2020. Vol. 318, N 1. P. G53–G65. doi: 10.1152/ajpgi.00264.2019 |
| [21] |
Bergner AJ, Stamp LA, Gonsalvez DG, et al. Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J Comp Neurol. 2014;522(3):514–527. doi: 10.1002/cne.23423 |
| [22] |
Bergner A.J., Stamp L.A., Gonsalvez D.G., et al. Birthdating of myenteric neuron subtypes in the small intestine of the mouse // J Comp Neurol. 2014. Vol. 522, N 3. P. 514–527. doi: 10.1002/cne.23423 |
| [23] |
Young HM, Ciampoli D. Transient expression of neuronal nitric oxide synthase by neurons of the submucous plexus of the mouse small intestine. Cell Tissue Res. 1998;291(3):395–401. doi: 10.1007/s004410051009 |
| [24] |
Young H.M., Ciampoli D. Transient expression of neuronal nitric oxide synthase by neurons of the submucous plexus of the mouse small intestine // Cell Tissue Res. 1998. Vol. 291, N 3. P. 395–401. doi: 10.1007/s004410051009 |
| [25] |
Masliukov PM, Budnik AF, Nozdrachev AD. Developmental changes of neurotransmitter properties in sympathetic neurons. Advances in Gerontology. 2017;30(3):347–355. (In Russ). |
| [26] |
Маслюков П.М., Будник А.Ф., Ноздрачев А.Д. Нейрохимические особенности узлов метасимпатической системы в онтогенезе // Успехи геронтологии. 2017. Т. 30, № 3. С. 347–355. |
| [27] |
Masliukov PM, Emanuilov AI, Nozdrachev AD. Developmental changes of neurotransmitter properties in sympathetic neurons. Advances in Gerontology. 2016;29(3):442–453. (In Russ). |
| [28] |
Маслюков П.М., Емануйлов А.И., Ноздрачёв А.Д. Возрастные изменения нейротрансмиттерного состава нейронов симпатических узлов // Успехи геронтологии. 2016. Т. 29, № 3. С. 442–453. |
| [29] |
Wright JW, Schwinof KM, Snyder MA, Copenhaver PF. A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons. Dev Biol. 1998;204(1):15–33. doi: 10.1006/dbio.1998.9066 |
| [30] |
Wright J.W., Schwinof K.M., Snyder M.A., Copenhaver P.F. A delayed role for nitric oxide-sensitive guanylate cyclases in a migratory population of embryonic neurons // Dev Biol. 1998. Vol. 204, N 1. P. 15–33. doi: 10.1006/dbio.1998.9066 |
| [31] |
Li Z, Hao MM, Van den Haute C, et al. Regional complexity in enteric neuron wiring reflects diversity of motility patterns in the mouse large intestine. Elife. 2019;8:e42914. doi: 10.7554/eLife.42914 |
| [32] |
Li Z., Hao M.M., Van den Haute C., et al. Regional complexity in enteric neuron wiring reflects diversity of motility patterns in the mouse large intestine // Elife. 2019. Vol. 8. P. e42914. doi: 10.7554/eLife.42914 |
| [33] |
Hao MM, Moore RE, Roberts RR, et al. The role of neural activity in the migration and differentiation of enteric neuron precursors. Neurogastroenterol Motil. 2010;22(5):e127–137. doi: 10.1111/j.1365-2982.2009.01462.x |
| [34] |
Hao M.M., Moore R.E., Roberts R.R., et al. The role of neural activity in the migration and differentiation of enteric neuron precursors // Neurogastroenterol Motil. 2010. Vol. 22, N 5. P. e127–137. doi: 10.1111/j.1365-2982.2009.01462.x |
| [35] |
Brooks LA, Fowler KL, Veras LV, et al. Resection margin histology may predict intermediate-term outcomes in children with rectosigmoid Hirschsprung disease. Pediatr Surg Int. 2020;36(8):875–882. doi: 10.1007/s00383-020-04689-x |
| [36] |
Brooks L.A., Fowler K.L., Veras L.V., et al. Resection margin histology may predict intermediate-term outcomes in children with rectosigmoid Hirschsprung disease // Pediatr Surg Int. 2020. Vol. 36, N 8. P. 875–882. doi: 10.1007/s00383-020-04689-x |
| [37] |
Patel BA, Dai X, Burda JE, et al. Inhibitory neuromuscular transmission to ileal longitudinal muscle predominates in neonatal guinea pigs. Neurogastroenterol Motil. 2010;22(8):909–918. |
| [38] |
Patel B.A., Dai X., Burda J.E., et al. Inhibitory neuromuscular transmission to ileal longitudinal muscle predominates in neonatal guinea pigs // Neurogastroenterol Motil. 2010. Vol. 22, N 8. P. 909–918. doi: 10.1111/j.1365-2982.2010.01508.x |
| [39] |
Tomita R, Tanjoh K, Fujisaki S, et al. Regulation of the enteric nervous system in the colon of patients with slow transit constipation. Hepatogastroenterology. 2002;49(48):1540–1544. |
| [40] |
Tomita R., Tanjoh K., Fujisaki S., et al. Regulation of the enteric nervous system in the colon of patients with slow transit constipation // Hepatogastroenterology. 2002. Vol. 49, N 48. P. 1540–1544. |
Eco-Vector
/
| 〈 |
|
〉 |