Differential effects of undernourishment on the differentiation and maturation of rat enteric neurons

Cell and Tissue Research

Volumn 353, Issue 3, 2013, Pages 367-380

  Girotti, Priscila Azevedo ^a   Misawa, Rúbia ^a   Palombit, Kelly ^a   Mendes, Cristina Eusébio ^a   Bittencourt, Jackson Cioni ^a   Castelucci, Patricia ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Myenteric neuron; P2X2 receptor; P2X7 receptor; Rat (Wistar); Submucosal neuron; Undernourishment

Indexed keywords

ACETYLCHOLINESTERASE; CALBINDIN; CALRETININ; NITRIC OXIDE SYNTHASE; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X7 RECEPTOR; CALB2 PROTEIN, RAT; CHOLINE ACETYLTRANSFERASE; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CELL DENSITY; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; INTESTINE INNERVATION; LARGE INTESTINE; MALE; MALNUTRITION; MYENTERIC PLEXUS; NERVE CELL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN RESTRICTION; RAT; REFEEDING; ANIMAL; GROWTH, DEVELOPMENT AND AGING; INNERVATION; MESENTERY; METABOLISM; PATHOLOGY; PREGNANCY; PRENATAL EXPOSURE; PROTEIN DEFICIENCY; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; CALBINDIN 2; CALBINDINS; CHOLINE O-ACETYLTRANSFERASE; FEMALE; MALE; MESENTERY; NERVE TISSUE PROTEINS; NEURONS; NITRIC OXIDE SYNTHASE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROTEIN DEFICIENCY; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2X2; RECEPTORS, PURINERGIC P2X7;

EID: 84883247430     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1620-z     Document Type: Article

References (45)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19-29
2. Bian XC, Bertrand PP, Bornstein JC (2000) Descending inhibitory reflexes involve P2X receptor-mediated transmission from interneurons to motor neurons in guinea-pig ileum. J Physiol (Lond) 528:551-560
3. Bornstein JC (2008) Purinergic mechanism in the control of gastrointestinal motility. Purinergic Signal 4:197-212
4. Burnstock G (2007) Physiology and pathophysyiology of purinergic neurotransmission. Physiol Rev 87:659-797
5. Castelucci P, De Souza RR, De Angelis RC, Furness JB, Liberti EA (2002a) Effects of pre- and postnatal protein deprivation and postnatal re-feeding on myenteric neurons of the rat large intestine: A quantitative morphological study. Cell Tissue Res 310:1-7
6. 2 receptors in the guinea pig enteric nervous system. Histochem Cell Biol 117:415-422
7. Castelucci P, Robbins HL, Furness JB (2003) P2X(2) purine receptor immunoreactivity of intraganglionic laminar endings in the mouse gastrointestinal tract. Cell Tissue Res 312:167-174
8. Cha CJM, Gelardi NL, Oh W (1987) Growth and cellular composition in rats with intrauterine growth retardation: effects of posnatal nutrition. J Nutr 154:1463-1468
9. 6, a purinergic receptor subunit, is affected by dietary zinc deficiency in rat hippocampus. Biol Trace Elem Res 91:77-87
10. Conboy VB, Santer RM, Swift GL (1987) Effects of prenatal undernutrition on prevertebral sympathetic neurons in the rat: A morphological and fluorescence histochemical study. J Anat 154:47-53
11. Cordero ME, Valenzuela CY, Rodriguez A, Aboitiz F (2003) Dendritic morphology and orientation of pyramidal cells of the neocortex in two groups of early postnatal undernourished-rehabilitated rats. Brain Res Dev Brain Res 142:37-45
12. Cowen T, Johnson RJR, Soubeyre V, Santer RM (2000) Restricted diet rescues rat enteric motor neurons from age related cell death. Gut 47:553-660
13. D'Orlando C, Fellay B, Schwaller B, Salicio V, Bloc A, Gotzos V, Celio MR (2001) Calretinin and calbindin D-28k delay the onset of cell death after excitotoxic stimulation in transfected P19 cells. Brain Res 909:145-158
14. Franke H, Krüel U, Illes P (2006) P2 receptors and neuronal injury. Eur J Physiol 452:622-644
15. Furness JB (2006) The enteric nervous system. Wiley-Blackwell, New York
16. Giaroni C, Knight GE, Ruan H-Z, Glass R, Bardini M, Lecchini S, Frigo G, Burnstock G (2002) P2 receptors in the murine gastrointestinal tract. Neuropharmacology 43:1313-1323
17. Gomes OA, Castelucci P, Fontes RBV, Liberti EA (2006) Effects of pre- and postnatal protein and postnatal re-feeding on myenteric neurons of the rat small intestine: A quantitative morphological study. Auton Neurosci 126:277-284
18. Gomes SP, Nyengaard JR, Misawa R, Girotti PA, Castelucci P, Blazquez FH, de Melo MP, Ribeiro AA (2009) Atrophy and neuron loss: effects of a protein-deficient diet on sympathetic neurons. J Neurosci Res 87:3568-3575
19. Greggio FM, Fontes RBV, Maifrino LBM, Castelucci P, Souza RR, Liberti EA (2010) Effects of perinatal protein deprivation and recovery on esophageal myenteric plexus. World J Gastroenterol 16:563-570
20. 7 receptors in the enteric nervous system of guinea-pig small intestine. J Comp Neurol 440:299-310
21. Hwang IK, Kang TC, Lee JC (2003) Chronological alterations of calbindin D-28k immunoreactivity in the gerbil main olfactory bulb after ischemic insult. Brain Res 971:250-254
22. King RS, Kemper TL, Debassio WA, Ramzan M, Blatt GJ, Rosene DL, Galler JR (2002) Birthdates and number of neurons in the serotonergic raphe nuclei in the rat with prenatal protein malnutrition. Nutr Neurosci 5:391-397
23. Kwon OJ, Kim JY, Kim SY, Jeon CJ (2005) Alterations in the localization of calbindin D28K-, calretinin-, and parvalbumin-immunoreactive neurons of rabbit retinal ganglion cell layer from ischemia and reperfusion. Mol Cells 19:382-390
24. Lister JP, Blatt GJ, Kemper TL, Tonkiss J, DeBassio WA, Galler JR, Rosene DL (2011) Prenatal protein malnutrition alters the proportion but not numbers of parvalbumin-immunoreactive interneurons in the hippocampus of the adult Sprague-Dawley rat. Nutr Neurosci 14:165-178
25. Lukas W, Jones KA (1994) Cortical neurons containing calretinin are selectively resistant to calcium overload and excitotoxicity in vitro. Neuroscience 61:307-316
26. 2 receptors in enteric neurons. World J Gastroenterol 16:3651-3663
27. 2 receptor in different classes of ileum myenteric neurons in the female obese ob/ob mouse. World J Gastroenterol 18:4693-4703
28. Monro RL, Bornstein JC, Bertrand PP (2008) Synaptic transmission from the submucosal plexus to the myenteric plexus in guinea-pig ileum. Neurogastroenterol Motil 20:1165-1173
29. Orrenius S, Nicotera P (1994) The calcium ion and cell death. J Neural Transm Suppl 43:1-11
30. 2 receptor expressing neurons of the rat ileum enteric nervous system. Dig Dis Sci 56:2262-2277
31. 3 purine receptor subunits in the guinea-pig enteric nervous system. Auton Neurosci 101:39-47
32. Potier B, Krzywkowski P, Lamour Y, Dutar P (1994) Loss of calbindin-immunoreactivity in CA1 hippocampal stratum radiatum and stratum lacunosum-moleculare interneurons in the aged rat. Brain Res 661:181-188
33. 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
34. 2 subunits contribute to fast synaptic excitation in myenteric neurons of the mouse small intestine. J Physiol (Lond) 552:809-821
35. Rivera LR, Thacker M, Castelucci P, Bron R, Furness JB (2009) The reactions of specific neuron types to intestinal ischemia in the guinea-pig enteric nervous system. Acta Neuropathol 24:1-10
36. 5 purinergic receptors in the enteric nervous system of mouse. Cell Tissue Res 319:191-200
37. Santer RM, Conboy VB (1990) Prenatal undernutrition permanently decreases enteric neuron number and sympathetic innervation of Auerbach's plexus in the rat. J Anat 168:57-62
38. Sperlágh B, Vizi ES, Wirkner K, Illes P (2006) P2X7 receptors in the nervous system. Prog Neurobiol 78:327-346
39. Van Nassauw L, Brouns I, Adraensen D, Burnstock G, Timmermans JP (2002) Neurochemical identification of enteric neurons expressing P2X(3) receptors in the guinea-pig ileum. Histochem Cell Biol 118:193-203
40. 7, an ionotropic purinergic receptor, in rat gastrointestinal musculature. Cell Tissue Res 312:149-154
41. Vulchanova L, Arvidsson U, Riedl M, Wang J, Buell G, Suprenant A, Nort RA (1996) Differential distribution of two ATP-gated ion channels (P2X receptors) determined by immunohistochemistry. Proc Natl Acad Sci USA 93:8063-8067
42. 3 purinoceptors in the rat enteric nervous system. Histochem Cell Biol 12:169-179
43. 3 receptors, neuropeptide Y, nitric oxide synthase and calretinin. Histochem Cell Biol 124:379-390
44. 6 receptors in the enteric nervous system of the rat gastrointestinal tract. Histochem Cell Biol 133:177-188
45. Zhang JH, Morita Y, Hironaka T, Emson PC, Tohyama M (1990) Ontological study of calbindin-D28k-like and parvalbumin-like immunoreactivities in rat spinal cord and dorsal root ganglia. J Comp Neurol 302:715-728