Development of Calbindin- and Calretinin-Immunopositive Neurons in the Enteric Ganglia of Rats

Abrahám H, Veszprémi B, Kravják A, Kovács K, Gömöri E, Seress L (2009) Ontogeny of calbindin immunoreactivity in the human hippocampal formation with a special emphasis on granule cells of the dentate gyrus. Int J Dev Neurosci 27:115–127

Amenta F, Cavalotta D, Del Valle ME, Mancini M, Sabbatini M, Torres JM, Vega JA (1994) Calbindin D-28k immunoreactivity in the rat cerebellar cortex: age-related changes. Neurosci Lett 178:131–134

Andressen C, Blumcke I, Celio MR (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181–208

Antal M, Freund TF, Polgar E (1990) Calcium-binding proteins, parvalbumin- and calbindin-D 28k immunoreactive neurons in the rat spinal cord and dorsal root ganglia: a light and electron microscopic study. J Comp Neurol 295:467–484

Arabadzisz D, Ylinen A, Emri Z (2002) Increased inter-spike intervals and fast after-hyperpolarization of action potentials in rat hippocampal pyramidal cells accompanied with altered calbindin immunoreactivity 10-12 months after global forebrain ischemia. Neurosci Lett 331:103–106

Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308

Bastianelli E (2003) Distribution of calcium-binding proteins in the cerebellum. Cerebellum 2:242–262

Bergner AJ, Stamp LA, Gonsalvez DG, Allison MB, Olson DP, Myers MG Jr, Anderson CR, Young HM (2014) Birthdating of myenteric neuron subtypes in the small intestine of the mouse. J Comp Neurol 522:514–527

Brookes SJH, Steele PA, Costa M (1991) Calretinin immunoreactivity in cholinergic motor neurones, interneurones and vasomotor neurones in the guinea-pig small intestine. Cell Tissue Res 263:471–481

Camp AJ, Wijesinghe R (2009) Calretinin: modulator of neuronal excitability. Int J Biochem Cell Biol 41:2118–2121

Collins J, Borojevic R, Verdu EF, Huizinga JD, Ratcliffe EM (2014) Intestinal microbiota influence the early postnatal development of the enteric nervous system. Neurogastroenterol Motil 26:98–107

Foo KS, Hellysaz A, Broberger C (2014) Expression and colocalization patterns of calbindin-D28k, calretinin and parvalbumin in the rat hypothalamic arcuate nucleus. J Chem Neuroanat 61–62:20–32

Foong JP (2016) Postnatal development of the mouse enteric nervous system. Adv Exp Med Biol 891:135–143

Foong JP, Nguyen TV, Furness JB, Bornstein JC, Young HM (2012) Myenteric neurons of the mouse small intestine undergo significant electrophysiological and morphological changes during postnatal development. J Physiol 590:2375–2390

Furness JB (2000) Types of neurons in the enteric nervous system. J Auton Nerv Syst 81:87–96

Furness JB, Trussell DC, Pompolo S, Bornstein JC, Smith TK (1990) Calbindin neurons of the guinea-pig small intestine: quantitative analysis of their numbers and projections. Cell Tissue Res 260:261–272

Furness JB, Kunze WA, Bertrand PP, Clerc N, Bornstein JC (1998) Intrinsic primary afferent neurons of the intestine. Prog Neurobiol 54:1–18

Gershon MD, Epstein ML, Hegstrand L (1980) Colonization of the chick gut by progenitors of enteric serotonergic neurons: distribution, differentiation, and maturation within the gut. Dev Biol 77:41–51

Hao MM, Young HM (2009) Development of enteric neuron diversity. J Cell Mol Med 13:1193–1210

Hao MM, Moore RE, Roberts RR, Nguyen T, Furness JB, Anderson RB, Young HM (2010) The role of neural activity in the migration and differentiation of enteric neuron precursors. Neurogastroenterol Motil 22:e127–e137

Hao MM, Lomax AE, McKeown SJ, Reid CA, Young HM, Bornstein JC (2012) Early development of electrical excitability in the mouse enteric nervous system. J Neurosci 32:10949–10960

Hao MM, Bornstein JC, Vanden Berghe P, Lomax AE, Young HM, Foong JP (2013) The emergence of neural activity and its role in the development of the enteric nervous system. Dev Biol 382:365–374

Heiman MG, Shaham S (2010) Twigs into branches: how a filopodium becomes a dendrite. Curr Opin Neurobiol 20:86–91

Heizmann CW, Braun K (1992) Changes in Ca(2+)-binding proteins in human neurodegenerative disorders. Trends Neurosci 15:259–264

Hirst GD, Holman ME, Spence I (1974) Two types of neurones in the myenteric plexus of duodenum in the guinea-pig. J Physiol 236:303–326

Hof PR, Glezer II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Weisenhorn DMV (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77–116

Iacopino AM, Christakos S (1990) Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87:4078–4082

Isaacs KR, Winsky L, Strauss KI, Jacobowitz DM (1995) Quadruple colocalization of calretinin, calcitonin gene-related peptide, vasoactive intestinal peptide, and substance P in fibers within the villi of the rat intestine. Cell Tissue Res 280:639–651

Kapur R, Yost C, Palmiter R (1992) A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development 116:167–175

Mann PT, Southwell BR, Ding YQ, Shigemoto R, Mizuno N, Furness JB (1997) Localisation of neurokinin 3 (NK3) receptor immunoreactivity in the rat gastrointestinal tract. Cell Tissue Res 289:1–9

Mann PT, Furness JB, Southwell BR (1999) Choline acetyltransferase immunoreactivity of putative intrinsic primary afferent neurons in the rat ileum. Cell Tissue Res 297:241–248

Masliukov PM, Korobkin AA, Nozdrachev AD, Timmermans JP (2012a) Calbindin-D28k immunoreactivity in sympathetic ganglionic neurons during development. Auton Neurosci 167:27–33

Masliukov PM, Korobkin AA, Konovalov VV, Porseva VV, Emanuĭlov AI (2012b) Age-related development of calbindin-immunopositive neurons of rat sympathetic ganglia. Morfologiia 141:77–80

Masliukov PM, Emanuilov AI, Madalieva LV, Moiseev KY, Bulibin AV, Korzina MB, Porseva VV, Korobkin AA, Smirnova VP (2014) Development of nNOS-positive neurons in the rat sensory and sympathetic ganglia. Neuroscience 256:271–281

Masliukov PM, Emanuilov AI, Moiseev K, Nozdrachev AD, Dobrotvorskaya S, Timmermans JP (2015) Development of non-catecholaminergic sympathetic neurons in para- and prevertebral ganglia of cats. Int J Dev Neurosci 40:76–84

Masliukov PM, Nozdrachev AD, Emanuilov AI (2016) Age-related features in expression of calcium-binding proteins in autonomic ganglionic neurons. Adv Gerontol 6:298–303

Maslyukov PM, Nozdrachev AD, Timmermans JP (2007) Age-related characteristics of the neurotransmitter composition of neurons in the stellate ganglion. Neurosci Behav Physiol 37:349–353

Maslyukov PM, Korzina MB, Emanuilov AI, Shilkin VV (2010) Neurotransmitter composition of neurons in the cranial cervical and celiac sympathetic ganglia in postnatal ontogenesis. Neurosci Behav Physiol 40:143–147

McVey NKA, Perez-Burgos A, Mao YK, Bienenstock J, Kunze WA (2015) The gut microbiome restores intrinsic and extrinsic nerve function in germ-free mice accompanied by changes in calbindin. Neurogastroenterol Motil 27:627–636

Michaelsen K, Lohmann C (2010) Calcium dynamics at developing synapses: mechanisms and functions. Eur J Neurosci 32:218–223

Misawa R, Girotti PA, Mizuno MS, Liberti EA, Furness JB, Castelucci P (2010) Effects of protein deprivation and re-feeding on P2X2 receptors in enteric neurons. World J Gastroenterol 16:3651–3663

Mitsui R (2011) Immunohistochemical analysis of substance P-containing neurons in rat small intestine. Cell Tissue Res 343:331–341

Newgreen DF, Hartley L (1995) Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat (Basel) 154:243–260

Oh MM, Oliveira FA, Waters J, Disterhoft JF (2013) Altered calcium metabolism in aging CA1 hippocampal pyramidal neurons. J Neurosci 33:7905–7911

Pham TD, Gershon MD, Rothman TP (1991) Time of origin of neurons in the murine enteric nervous system: sequence in relation to phenotype. J Comp Neurol 314:789–798

Qu ZD, Thacker M, Castelucci P, Bagyánszki M, Epstein ML, Furness JB (2008) Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 334:147–161

Resibois A, Vienne G, Pochet R (1988) Calbindin-D28K and the peptidergic neuroendocrine system in rat gut: an immunohistochemical study. Biol Cell 63:67–75

Richardson RJ, Grkovic I, Allen AM, Anderson CR (2006) Separate neurochemical classes of sympathetic postganglionic neurons project to the left ventricle of the rat heart. Cell Tissue Res 324:9–16

Sang Q, Young HM (1996) Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284:39–53

Sayegh AI, Ritter RC (2003) Morphology and distribution of nitric oxide synthase-, neurokinin-1 receptor-, calretinin-, calbindin-, and neurofilament-M-immunoreactive neurons in the myenteric and submucosal plexuses of the rat small intestine. Anat Rec A 271:209–216

Schwaller B (2012) The use of transgenic mouse models to reveal the functions of Ca2+ buffer proteins in excitable cells. Biochim Biophys Acta 1820:1294–1303

Shetty AK, Turner DA (1998) Hippocampal interneurons expressing glutamic acid decarboxylase and calcium-binding proteins decrease with aging in Fischer 344 rats. J Comp Neurol 394:252–269

Siechen S, Yang S, Chiba A, Saif T (2009) Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals. Proc Natl Acad Sci USA 106:12611–12616

Song ZM, Brookes SJ, Costa M (1994) All calbindin-immunoreactive myenteric neurons project to the mucosa of the guinea-pig small intestine. Neurosci Lett 180:219–222

Timmermans JP, Adriaensen D, Cornelissen W, Scheuermann DW (1997) 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 118:331–340

Villa A, Podini P, Panzeri MC, Racchetti G, Meldolesi J (1994) Cytosolic Ca2+ binding proteins during rat brain ageing: loss of calbindin and calretinin in the hippocampus, with no change in the cerebellum. Eur J Neurosci 6:1491–1499

Wilhelm M, Lawrence JJ, Gábriel R (2015) Enteric plexuses of two choline-acetyltransferase transgenic mouse lines: chemical neuroanatomy of the fluorescent protein-expressing nerve cells. Brain Res Bull 111:76–83

Young HM (2008) Functional development of the enteric nervous system-from migration to motility. Neurogastroenterol Motil 20(Suppl 1):20–31

Young HM, Torihashi S, Ciampoli D, Sanders KM (1998) Identification of neurons that express stem cell factor in the mouse small intestine. Gastroenterology 115:898–908