Effects of protein deprivation and re-feeding on P2X2 receptors in enteric neurons

World Journal of Gastroenterology

Volumn 16, Issue 29, 2010, Pages 3651-3663

  Misawa, Rúbia ^a   Girotti, Priscila Azevedo ^a   Mizuno, Márcia Sanae ^a   Liberti, Edson Aparecido ^a   Furness, John Barton ^b   Castelucci, Patricia ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Chemical coding; Myenteric neurons; Submucosal neurons; Undernutrition

Indexed keywords

CALBINDIN; CALRETININ; CHOLINE ACETYLTRANSFERASE; NITRIC OXIDE SYNTHASE; PURINERGIC P2X2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; CYTOPLASM; FEMALE; GENE EXPRESSION; ILEUM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE INNERVATION; MALNUTRITION; MYENTERIC PLEXUS; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN MALNUTRITION; RAT; REFEEDING;

EID: 77955729008     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v16.i29.3651     Document Type: Article

References (62)

1. Burnstock G. The past, present and future of purine nucleotides as signalling molecules. Neuropharmacology 1997; 36: 1127-1139
2. Barajas-López C, Huizinga JD, Collins SM, Gerzanich V, Espinosa-Luna R, Peres AL. P2x-purinoceptors of myenteric neurones from the guinea-pig ileum and their unusual pharmacological properties. Br J Pharmacol 1996; 119: 1541-1548
3. Bian X, Bertrand PP, Bornstein JC. Descending inhibitory reflexes involve P2X receptor-mediated transmission from interneurons to motor neurons in guinea-pig ileum. J Physiol 2000; 528: 551-560
4. Galligan JJ, LePard KJ, Schneider DA, Zhou X. Multiple mechanisms of fast excitatory synaptic transmission in the enteric nervous system. J Auton Nerv Syst 2000; 81: 97-103
5. Galligan JJ. Ligand-gated ion channels in the enteric nervous system. Neurogastroenterol Motil 2002; 14: 611-623
6. Vulchanova L, Arvidsson U, Riedl M, Wang J, Buell G, Surprenant A, North RA, Elde R. Differential distribution of two ATP-gated channels (P2X receptors) determined by immunocytochemistry. Proc Natl Acad Sci USA 1996; 93: 8063-8067
7. Castelucci P, Robbins HL, Poole DP, Furness JB. The distribution of purine P2X(2) receptors in the guinea-pig enteric nervous system. Histochem Cell Biol 2002; 117: 415-422
8. Poole DP, Castelucci P, Robbins HL, Chiocchetti R, Furness JB. The distribution of P2X3 purine receptor subunits in the guinea pig enteric nervous system. Auton Neurosci 2002; 101: 39-47
9. Van Nassauw L, Brouns I, Adriaensen D, Burnstock G, Timmermans JP. Neurochemical identification of enteric neurons expressing P2X(3) receptors in the guinea-pig ileum. Histochem Cell Biol 2002; 118: 193-203
10. Hu HZ, Gao N, Lin Z, Gao C, Liu S, Ren J, Xia Y, Wood JD. P2X(7) receptors in the enteric nervous system of guinea-pig small intestine. J Comp Neurol 2001; 440: 299-310
11. Xiang Z, Burnstock G. Distribution of P2Y2 receptors in the guinea pig enteric nervous system and its coexistence with P2X2 and P2X3 receptors, neuropeptide Y, nitric oxide synthase and calretinin. Histochem Cell Biol 2005; 124: 379-390
12. Xiang Z, Burnstock G. P2X2 and P2X3 purinoceptors in the rat enteric nervous system. Histochem Cell Biol 2004; 121: 169-179
13. Xiang Z, Burnstock G. Development of nerves expressing P2X3 receptors in the myenteric plexus of rat stomach. Histochem Cell Biol 2004; 122: 111-119
14. Yu Q, Zhao Z, Sun J, Guo W, Fu J, Burnstock G, He C, Xiang Z. Expression of P2X6 receptors in the enteric nervous system of the rat gastrointestinal tract. Histochem Cell Biol 2010; 133: 177-188
15. Giaroni C, Knight GE, Ruan HZ, Glass R, Bardini M, Lecchini S, Frigo G, Burnstock G. P2 receptors in the murine gastrointestinal tract. Neuropharmacology 2002; 43: 1313-1323
16. Ruan HZ, Burnstock G. The distribution of P2X5 purinergic receptors in the enteric nervous system of mouse. Cell Tissue Res 2005; 319: 191-200
17. Cornblath DR, Brown MJ. Influence of malnutrition on developing rat peripheral nerves. Exp Neurol 1988; 99: 403-411
18. Santer RM, Conboy VB. Prenatal undernutrition permanently decreases enteric neuron number and sympathetic innervation of Auerbach's plexus in the rat. J Anat 1990; 168: 57-62
19. Leite-Mello EV, Stabille SR, Miranda Neto MH. Effect of maternal protein deprivation on morphological and quanti- tative aspects of the myenteric plexus neurons of proximal colon in rats. Arq Neuropsiquiatr 1997; 55: 106-113
20. Sant'ana Dde M, Miranda Neto MH, de Souza RR, Molinari SL. Morphological and quantitative study of the myenteric plexus of the ascending colon of rats subjected to proteic desnutrition. Arq Neuropsiquiatr 1997; 55: 687-695
21. Castelucci P, de Souza RR, de Angelis RC, Furness JB, Liberti EA. Effects of pre- and postnatal protein deprivation and postnatal refeeding on myenteric neurons of the rat large intestine: a quantitative morphological study. Cell Tissue Res 2002; 310: 1-7
22. Gomes OA, Castelucci P, de Vasconcellos Fontes RB, Liberti EA. Effects of pre- and postnatal protein deprivation and postnatal refeeding on myenteric neurons of the rat small intestine: a quantitative morphological study. Auton Neurosci 2006; 126-127: 277-284
23. Liberti EA, Fontes RB, Fuggi VM, Maifrino LB, Souza RR. Effects of combined pre- and post-natal protein deprivation on the myenteric plexus of the esophagus of weanling rats: a histochemical, quantitative and ultrastructural study. World J Gastroenterol 2007; 13: 3598-3604
24. Gomes SP, Nyengaard JR, Misawa R, Girotti PA, Castelucci P, Blazquez FH, de Melo MP, Ribeiro AA. Atrophy and neuron loss: effects of a protein-deficient diet on sympathetic neurons. J Neurosci Res 2009; 87: 3568-3575
25. Greggio FM, Fontes RB, Maifrino LB, Castelucci P, de Souza RR, Liberti EA. Effects of perinatal protein deprivation and recovery on esophageal myenteric plexus. World J Gastroenterol 2010; 16: 563-570
26. Cha CJ, Gelardi NL, Oh W. Growth and cellular composition in rats with intrauterine growth retardation: effects of postnatal nutrition. J Nutr 1987; 117: 1463-1468
27. Furness JB. Types of neurons in the enteric nervous system. J Auton Nerv Syst 2000; 81: 87-96
28. Brehmer A. Structure of enteric neurons. Adv Anat Embryol Cell Biol 2006; 186: 1-91
29. Furness JB. The Enteric Nervous System. Malden: Blackwell Publishing Inc., 2006
30. Qu ZD, Thacker M, Castelucci P, Bagyánszki M, Epstein ML, Furness JB. Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 2008; 334: 147-161
31. Mongardi Fantaguzzi C, Thacker M, Chiocchetti R, Furness JB. Identification of neuron types in the submucosal ganglia of the mouse ileum. Cell Tissue Res 2009; 336: 179-189
32. Ekblad E, Mulder H, Uddman R, Sundler F. NOS-containing neurons in the rat gut and coeliac ganglia. Neuropharmacology 1994; 33: 1323-1331
33. Mann PT, Furness JB, Southwell BR. Choline acetyltransferase immunoreactivity of putative intrinsic primary afferent neurons in the rat ileum. Cell Tissue Res 1999; 297: 241-248
34. Aimi Y, Kimura H, Kinoshita T, Minami Y, Fujimura M, Vincent SR. Histochemical localization of nitric oxide synthase in rat enteric nervous system. Neuroscience 1993; 53: 553-560
35. Jarvinen MK, Wollmann WJ, Powrozek TA, Schultz JA, Powley TL. Nitric oxide synthase-containing neurons in the myenteric plexus of the rat gastrointestinal tract: distribution and regional density. Anat Embryol (Berl) 1999; 199: 99-112
36. Nakajima K, Tooyama I, Yasuhara O, Aimi Y, Kimura H. Immunohistochemical demonstration of choline acetyltransferase of a peripheral type (pChAT) in the enteric nervous system of rats. J Chem Neuroanat 2000; 18: 31-40
37. Sayegh AI, Ritter RC. 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 Discov Mol Cell Evol Biol 2003; 271: 209-216
38. Kunze WA, Mao YK, Wang B, Huizinga JD, Ma X, Forsythe P, Bienenstock J. Lactobacillus reuteri enhances excitability of colonic AH neurons by inhibiting calcium-dependent potassium channel opening. J Cell Mol Med 2009; 13: 2261-2270
39. Brandão MCS, De Angelis RC, De-Souza RR, Fróes LB, Liberti EA. Effects of pre- and postnatal protein energy deprivation on the myenteric plexus of the small intestine: a morphometric study in weanling rats. Nutrition Res 2003; 23: 215-223
40. Lalo U, Pankratov Y, Wichert SP, Rossner MJ, North RA, Kirchhoff F, Verkhratsky A. P2X1 and P2X5 subunits form the functional P2X receptor in mouse cortical astrocytes. J Neurosci 2008; 28: 5473-5480
41. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H. Purinergic signalling in the nervous system: an overview. Trends Neurosci 2009; 32: 19-29
42. Vanderwinden JM, Timmermans JP, Schiffmann SN. Glial cells, but not interstitial cells, express P2X7, an ionotropic purinergic receptor, in rat gastrointestinal musculature. Cell Tissue Res 2003; 312: 149-154
43. Gabella G, Trigg P. Size of neurons and glial cells in the enteric ganglia of mice, guinea-pigs, rabbits and sheep. J Neurocytol 1984; 13: 49-71
44. Rühl A. Glial cells in the gut. Neurogastroenterol Motil 2005; 17: 777-790
45. Hoff S, Zeller F, von Weyhern CW, Wegner M, Schemann M, Michel K, Rühl A. Quantitative assessment of glial cells in the human and guinea pig enteric nervous system with an anti-Sox8/9/10 antibody. J Comp Neurol 2008; 509: 356-371
46. Franke H, Krügel U, Illes P. P2 receptors and neuronal injury. Pflugers Arch 2006; 452: 622-644
47. Chu Y, Mouat MF, Coffield JA, Orlando R, Grider A. Expression of P2X6, a purinergic receptor subunit, is affected by dietary zinc deficiency in rat hippocampus. Biol Trace Elem Res 2003; 91: 77-87
48. Seidel B, Bigl M, Franke H, Kittner H, Kiess W, Illes P, Krügel U. Expression of purinergic receptors in the hypothalamus of the rat is modified by reduced food availability. Brain Res 2006; 1089: 143-152
49. Krügel U, Seidel B, Spies O, Kitter H, Illes P, Kiess W. Chronic food restriction alters purinergic receptor mRNA expression in the nucleus accumbens of the rat. Drug Devel Res 2003; 59: 95-103
50. Kittner H, Franke H, Harsch JI, El-Ashmawy IM, Seidel B, Krügel U, Illes P. Enhanced food intake after stimulation of hypothalamic P2Y1 receptors in rats: modulation of feeding behaviour by extracellular nucleotides. Eur J Neurosci 2006; 24: 2049-2056
51. Cavaliere F, Florenzano F, Amadio S, Fusco FR, Viscomi MT, D'Ambrosi N, Vacca F, Sancesario G, Bernardi G, Molinari M, Volontè C. Up-regulation of P2X2, P2X4 receptor and ischemic cell death: prevention by P2 antagonists. Neuroscience 2003; 120: 85-98
52. Franke H, Günther A, Grosche J, Schmidt R, Rossner S, Reinhardt R, Faber-Zuschratter H, Schneider D, Illes P. P2X7 receptor expression after ischemia in the cerebral cortex of rats. J Neuropathol Exp Neurol 2004; 63: 686-699
53. Franke H, Illes P. Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol Ther 2006; 109: 297-324
54. Yiangou Y, Facer P, Baecker PA, Ford AP, Knowles CH, Chan CL, Williams NS, Anand P. ATP-gated ion channel P2X(3) is increased in human inflammatory bowel disease. Neurogastroenterol Motil 2001; 13: 365-369
55. Phillips RJ, Kieffer EJ, Powley TL. Aging of the myenteric plexus: neuronal loss is specific to cholinergic neurons. Auton Neurosci 2003; 106: 69-83
56. Chiocchetti R, Poole DP, Kimura H, Aimi Y, Robbins HL, Castelucci P, Furness JB. Evidence that two forms of choline acetyltransferase are differentially expressed in subclasses of enteric neurons. Cell Tissue Res 2003; 311: 11-22
57. 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: 39-53
58. Cowen T, Johnson RJ, Soubeyre V, Santer RM. Restricted diet rescues rat enteric motor neurones from age related cell death. Gut 2000; 47: 653-660
59. Heinicke EA, Kiernan JA, Wijsman J. Specific, selective, and complete staining of neurons of the myenteric plexus, using cuprolinic blue. J Neurosci Methods 1987; 21: 45-54
60. Phillips RJ, Hargrave SL, Rhodes BS, Zopf DA, Powley TL. Quantification of neurons in the myenteric plexus: an evaluation of putative pan-neuronal markers. J Neurosci Methods 2004; 133: 99-107
61. Marese AC, de Freitas P, Natali MR. Alterations of the number and the profile of myenteric neurons of Wistar rats promoted by age. Auton Neurosci 2007; 137: 10-18
62. Marçal Natali MR, Molinari SL, Valentini LC, Hubner de Miranda Neto M. Morphoquantitative evaluation of the duodenal myenteric neuronal population in rats fed with hypoproteic ration. Biocell 2005; 29: 39-46