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Effects of the neonatal treatment with monosodium glutamate on myenteric neurons and the intestine wall in the ileum of rats

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Abstract

Background

The neonatal administration of a 4 mg/g dose of monosodium glutamate (MSG) to rodents leads to neuronal death in the hypothalamus arcuate nucleus, which leads in turn to obesity in the adult animal. However, few studies have investigated the effects on the enteric nervous system. This study evaluated the effects of the neonatal administration of MSG on the frequency and morphometry of the myenteric as well as the ileum wall morphometry of adult Wistar male rats.

Methods

Whole-mount preparations of ileum samples were stained by the Giemsa or NADH-diaphorase histochemical methods. For histological processing, hematoxylin and eosin staining was used.

Results

The treatment with MSG led to obesity, as shown by the higher values for Lee’s index and the weights of periepididimal and retroperitoneal adipose tissues. The Giemsa staining revealed a significantly larger neuronal density in the MSG group, which is explained by smaller physical growth and a reduction in the weight of the small intestine. The mean neuronal profile did not change between groups. The NADH-diaphorase-positive neuronal subpopulation kept its neuronal density but its average cellular profile was reduced in the MSG group. A morphometric analysis of the intestinal wall, muscular layer, villi, and intestinal crypts showed that their characteristics did not change.

Conclusions

The treatment with MSG did not cause alteration of the total myenteric population of the ileum, but it influenced the NADH-diaphorase-positive subpopulation. From the maintenance of the morphometric parameters of the ileum intestinal wall, we inferred that intestinal function was preserved in obese animals.

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References

  1. M Nedergaard T Takano AJ Hansen (2002) ArticleTitleBeyond the role of glutamate as a neurotransmitter Nature 3 748–55 Occurrence Handle1:CAS:528:DC%2BD38Xmslagsro%3D

    CAS  Google Scholar 

  2. M-T Liu JD Rothstein MD Gershon AL Kirchgessner (1997) ArticleTitleGlutamatergic enteric neurons J Neurosci 17 4764–84 Occurrence Handle1:CAS:528:DyaK2sXjvFCrsr4%3D Occurrence Handle9169536

    CAS  PubMed  Google Scholar 

  3. AL Kirchgessner M-T Liu F Alcantara (1997) ArticleTitleExcitotoxicity in the enteric nervous system J Neurosci 17 8804–16 Occurrence Handle1:CAS:528:DyaK2sXnsFaltrs%3D Occurrence Handle9348349

    CAS  PubMed  Google Scholar 

  4. A Larzabal J Losada JM Mateos R Benítez IJ Garmilla R Kuhn et al. (1999) ArticleTitleDistribution of the group II metabotropic glutamate receptors (mGluR2/3) in the enteric nervous system of the rat Neurosci Lett 276 91–4 10.1016/S0304-3940(99)00814-9 Occurrence Handle10.1016/S0304-3940(99)00814-9 Occurrence Handle1:CAS:528:DyaK1MXntlemurg%3D Occurrence Handle10624799

    Article  CAS  PubMed  Google Scholar 

  5. M-T Liu AL Kirchgessner (2000) ArticleTitleAgonist- and reflex-evoked internalization of metabotropic glutamate receptor 5 in enteric neurons J Neurosci 20 3200–5 Occurrence Handle1:CAS:528:DC%2BD3cXivFKht7Y%3D Occurrence Handle10777784

    CAS  PubMed  Google Scholar 

  6. F Moroni S Luzzi S Franchi-Micheli L Zilletti (1986) ArticleTitleThe presence of N-methyl-D-aspartate-type receptors for glutamic acid in the guinea pig myenteric plexus Neurosci Lett 68 57–62 10.1016/0304-3940(86)90229-6 Occurrence Handle10.1016/0304-3940(86)90229-6 Occurrence Handle1:CAS:528:DyaL28XksFGitL4%3D Occurrence Handle2873540

    Article  CAS  PubMed  Google Scholar 

  7. JW Olney (1969) ArticleTitleBrain lesions, obesity, and other disturbances in mice treated with monosodium glutamate Science 164 719–21 Occurrence Handle10.1126/science.164.3880.719 Occurrence Handle1:CAS:528:DyaF1MXktFWhurw%3D Occurrence Handle5778021

    Article  CAS  PubMed  Google Scholar 

  8. MA Romagnano WH Pilcher C Bennett-Clarke TL Chafel SA Joseph (1982) ArticleTitleDistribution of somatostatin in the mouse brain: effects of neonatal MSG treatment Brain Res 234 387–98 10.1016/0006-8993(82)90878-2 Occurrence Handle10.1016/0006-8993(82)90878-2 Occurrence Handle1:CAS:528:DyaL38XhtlKgurY%3D Occurrence Handle6120749

    Article  CAS  PubMed  Google Scholar 

  9. L Seress (1982) ArticleTitleDivergent effects of acute and chronic monosodium L-glutamate treatment on the anterior and posterior parts of the arcuate nucleus Neuroscience 7 2207–16 10.1016/0306-4522(82)90131-2 Occurrence Handle10.1016/0306-4522(82)90131-2 Occurrence Handle1:CAS:528:DyaL38XmtFCnsbg%3D Occurrence Handle7145092

    Article  CAS  PubMed  Google Scholar 

  10. K Tanaka M Shimada A Sasahara N Oya Y Fujiyama S Hosoda (1983) ArticleTitleNeonatal monosodium glutamate-induced lesions of hypothalamus increase intestinal fat absorption in adult mice Exp Neurol 79 141–51 10.1016/0014-4886(83)90385-0 Occurrence Handle10.1016/0014-4886(83)90385-0 Occurrence Handle1:STN:280:DyaL3s7gsFCrtg%3D%3D Occurrence Handle6337055

    Article  CAS  PubMed  Google Scholar 

  11. K Tanaka M Shimada K Nakao T Kusunoki (1978) ArticleTitleHypothalamic lesion induced by injection of monosodium glutamate in suckling period and subsequent development of obesity Exp Neurol 62 191–9 10.1016/0014-4886(78)90050-X Occurrence Handle10.1016/0014-4886(78)90050-X Occurrence Handle1:STN:280:DyaE1M%2Fos1Sjug%3D%3D Occurrence Handle729669

    Article  CAS  PubMed  Google Scholar 

  12. AJF Barbosa (1978) ArticleTitleTécnica histológica para gânglios nervosos intramurais em preparados espessos (in Portuguese with English abstract) Rev Bras Pesqui Méd Biol 11 95–7 Occurrence Handle1:STN:280:DyaE1c3kvFKmsA%3D%3D Occurrence Handle80017

    CAS  PubMed  Google Scholar 

  13. G Gabella (1969) ArticleTitleDetection of nerve cells by histochemical technique Experientia 25 218–9 10.1007/BF01899135 Occurrence Handle10.1007/BF01899135 Occurrence Handle1:STN:280:DyaF1M3gvV2jtw%3D%3D Occurrence Handle5786120

    Article  CAS  PubMed  Google Scholar 

  14. K Hamaoka T Kusunoki (1986) ArticleTitleMorphological and cell proliferative study on the growth of visceral organs in monosodium L-glutamate-treated obese mice J Nutr Sci Vitaminol 32 395–411 Occurrence Handle1:CAS:528:DyaL28Xmt1Gitrg%3D Occurrence Handle3806254

    CAS  PubMed  Google Scholar 

  15. RB Kanarek R Marks-Kaufman (1981) ArticleTitleIncreased carbohydrate consumption induced by neonatal administration of monosodium glutamate to rats Neurobehav Toxicol Teratol 3 343–50 Occurrence Handle1:CAS:528:DyaL3MXlvVGlur4%3D Occurrence Handle7290289

    CAS  PubMed  Google Scholar 

  16. Š Mozeš Z Šefčíková L Lenhardt L Raček (2004) ArticleTitleEffect of adrenalectomy on the activity of small intestine enzymes in monosodium glutamate obese rats Physiol Res 53 415–22 Occurrence Handle15312001

    PubMed  Google Scholar 

  17. Š Mozeš Z Šefčíková L Lenhardt L Raček (2004) ArticleTitleObesity and changes of alkaline phosphatase activity in the small intestine of 40- and 80-day-old rats subjected to early postnatal overfeeding or monosodium glutamate Physiol Res 53 177–86 Occurrence Handle15046554

    PubMed  Google Scholar 

  18. K Oida T Nakai T Hayashi S Miyabo R Takeda (1984) ArticleTitlePlasma lipoproteins of monosodium glutamate-induced obese rats Int J Obes 8 385–91 Occurrence Handle1:CAS:528:DyaL2MXhs1CrtL8%3D Occurrence Handle6394519

    CAS  PubMed  Google Scholar 

  19. PC Papa AM Vargas JLT Silva MT Nunes UF Machado (2002) ArticleTitleGLUT4 protein is differently modulated during development of obesity in monosodium glutamate-treated mice Life Sci 71 1917–28 10.1016/S0024-3205(02)01948-3 Occurrence Handle10.1016/S0024-3205(02)01948-3 Occurrence Handle1:CAS:528:DC%2BD38XlvF2rsbw%3D

    Article  CAS  Google Scholar 

  20. L Raček L Lenhardt Š Mozeš (2001) ArticleTitleEffect of fasting and refeeding on duodenal alkaline phosphatase activity in monosodium glutamate obese rats Physiol Res 50 365–72 Occurrence Handle11551142

    PubMed  Google Scholar 

  21. R Racotta A Hernandez-Garcia (1989) ArticleTitleGender differences between the effect of monosodium glutamate on food intake in rats Physiol Behav 46 331–2 Occurrence Handle1:CAS:528:DyaL1MXlvV2jsbk%3D Occurrence Handle2602476

    CAS  PubMed  Google Scholar 

  22. T Yoshida H Nishioka Y Nakamura M Kondo (1984) ArticleTitleReduced norepinephrine turnover in mice with monosodium glutamate-induced obesity Metab Clin Exp 33 1060–3 Occurrence Handle1:CAS:528:DyaL2cXls1ymt7k%3D Occurrence Handle6493048

    CAS  PubMed  Google Scholar 

  23. Dawson RJr DR Wallace SM Gabriel (1989) ArticleTitleA pharmacological analysis of food intake regulation in rats treated neonatally with monosodium L-glutamate (MSG) Pharmacol Biochem Behav 32 391–8 10.1016/0091-3057(89)90168-8 Occurrence Handle10.1016/0091-3057(89)90168-8

    Article  Google Scholar 

  24. A Stricker-Krongrad C Burlet B Beck (1998) ArticleTitleBehavioral deficits in monosodium glutamate rats: specific changes in the structure of feeding behavior Life Sci 62 2127–32 10.1016/S0024-3205(98)00187-8 Occurrence Handle10.1016/S0024-3205(98)00187-8 Occurrence Handle1:CAS:528:DyaK1cXjtFeqs70%3D Occurrence Handle9627091

    Article  CAS  PubMed  Google Scholar 

  25. MK Badman JS Flier (2005) ArticleTitleThe gut and energy balance: visceral allies in the obesity wars Science 307 1909–14 10.1126/science.1109951 Occurrence Handle10.1126/science.1109951 Occurrence Handle1:CAS:528:DC%2BD2MXisVyiu74%3D Occurrence Handle15790843

    Article  CAS  PubMed  Google Scholar 

  26. SJ Konturek JW Konturek T Pawlik T Brzozowki (2004) ArticleTitleBraIn–gut axis and its role In the control of food intake J Physiol Pharmacol 55 137–54 Occurrence Handle1:CAS:528:DC%2BD2cXjs1Orurc%3D Occurrence Handle15082874

    CAS  PubMed  Google Scholar 

  27. A Martinková L Lenhardt Š Mozeš (2000) ArticleTitleEffect of neonatal MSG treatment on day–night alkaline phosphatase activity in the rat duodenum Physiol Res 49 339–45 Occurrence Handle11043921

    PubMed  Google Scholar 

  28. MH Miranda-Neto SL Molinari MRM Natali DMG Sant’ana (2001) ArticleTitleRegional differences in the number and type of myenteric neurons of the ileum of rats Arq Neuropsiquiatr 59 54–9 Occurrence Handle1:STN:280:DC%2BD3M3gvFWqsQ%3D%3D Occurrence Handle11299432

    CAS  PubMed  Google Scholar 

  29. B Meister S Ceccatelli T Hökfelt N-E Andén M Andén E Theodorsson (1989) ArticleTitleNeurotransmitters, neuropeptides and binding sites in the rat mediobasal hypothalamus: effects of monosodium glutamate (MSG) lesions Exp Brain Res 76 343–68 10.1007/BF00247894 Occurrence Handle10.1007/BF00247894 Occurrence Handle1:CAS:528:DyaL1MXls1yrsbk%3D Occurrence Handle2569986

    Article  CAS  PubMed  Google Scholar 

  30. SP Kalra MG Dube S Pu B Xu T Horvath S Kalra (1999) ArticleTitleInteracting appetite-regulating pathways in the hypothalamic regulation of body weight Endocr Rev 20 68–100 10.1210/er.20.1.68 Occurrence Handle10.1210/er.20.1.68 Occurrence Handle1:CAS:528:DyaK1MXhsV2mtL0%3D Occurrence Handle10047974

    Article  CAS  PubMed  Google Scholar 

  31. L Macho M Ficková D Ježová Š Zórad (2000) ArticleTitleLate effects of postnatal administration of monosodium glutamate on insulin action in adult rats Physiol Res 49 S79–85 Occurrence Handle1:CAS:528:DC%2BD3cXksVChu7o%3D Occurrence Handle10984075

    CAS  PubMed  Google Scholar 

  32. MM Torrejais MRM Natali CI Conegero MH Miranda-Neto (1995) ArticleTitleEffects of proteic malnutrition after breast-feeding on the morphology of the intestinal wall and myenteric neurons of the ileum of rats Rev Unimar 17 315–27

    Google Scholar 

  33. MRM Natali MH Miranda-Neto (1996) ArticleTitleEffects of maternal proteic undernutrition on the neurons of the myenteric plexus of the duodenum of rats Arq Neuropsiquiatr 54 273–9 Occurrence Handle1:STN:280:DyaK2s7gsVKiug%3D%3D Occurrence Handle8984985

    CAS  PubMed  Google Scholar 

  34. MCS Brandão RC De Angelis RR De Souza LB Froes EA Liberti (2003) ArticleTitleEffects of pre- and postnatal protein energy deprivation on the myenteric plexus of the small intestine: a morphometric study in weanling rats Nutr Res 75 7–15

    Google Scholar 

  35. MRM Natali MH Miranda-Neto AM Orsi (2003) ArticleTitleMorphometry and quantification of the myenteric neurons of the duodenum of adult rats fed with hypoproteic chow Int J Morphol 21 273–7

    Google Scholar 

  36. E Bor-Seng-Shu G Chadi F Bor-Jiun-Shu CA Ferraz-de-Carvalho RR De-Souza (1994) ArticleTitleMyenteric neurons of the mouse small intestine. Morphometry and acetylcholinesterase activity Braz J Med Biol Res 27 101–8 Occurrence Handle1:STN:280:DyaK2c3islOmug%3D%3D Occurrence Handle8173525

    CAS  PubMed  Google Scholar 

  37. HM Young JB Furness P Sewell EF Burcher CJ Kandiah (1993) ArticleTitleTotal numbers of neurons in myenteric ganglia of the guinea-pig small intestine Cell Tissue Res 272 197–200 10.1007/BF00323587 Occurrence Handle10.1007/BF00323587 Occurrence Handle1:STN:280:DyaK3s3ksFaltQ%3D%3D Occurrence Handle8481953

    Article  CAS  PubMed  Google Scholar 

  38. RJ Phillips EJ Kieffer TL Powley (2003) ArticleTitleAging of the myenteric plexus: neuronal loss is specific to cholinergic neurons Auton Neurosci 106 69–83 10.1016/S1566-0702(03)00072-9 Occurrence Handle10.1016/S1566-0702(03)00072-9 Occurrence Handle12878075

    Article  PubMed  Google Scholar 

  39. RJR Johnson M Schemann RM Santer T Cowen (1998) ArticleTitleThe effects of age on the overall population and on sub-populations of myenteric neurons in the rat small intestine J Anat 192 479–88 10.1046/j.1469-7580.1998.19240479.x Occurrence Handle10.1046/j.1469-7580.1998.19240479.x Occurrence Handle9723975

    Article  PubMed  Google Scholar 

  40. A Fiorini SL Molinari MRM Natali MH Miranda-Neto (1999) ArticleTitleQuantitative morphological analysis of the myenteric neurons of the ileum in rats under experimental desnutrition Acta Sci 21 409–13

    Google Scholar 

  41. D Badillo-Martinez N Nicotera PD Butler AL Kirchgessner RJ Bodnar (1984) ArticleTitleImpairments in analgesic, hypothermic, and glucoprivic stress responses following neonatal monosodium glutamate Neuroendocrinology 38 438–46 Occurrence Handle10.1159/000123932 Occurrence Handle1:CAS:528:DyaL2cXks1OhtL0%3D Occurrence Handle6738808

    Article  CAS  PubMed  Google Scholar 

  42. PC Goldsmith (2000) ArticleTitleNeuroglial responses to elevated glutamate in the medial basal hypothalamus of the infant mouse J Nutr 130 1032–8S

    Google Scholar 

  43. EA Cavalheiro JW Olney (2001) ArticleTitleGlutamate antagonists: deadly liaisons with cancer Proc Natl Acad Sci U S A 98 5947–8 10.1073/pnas.121179198 Occurrence Handle10.1073/pnas.121179198 Occurrence Handle1:CAS:528:DC%2BD3MXktVWlu7s%3D Occurrence Handle11371628

    Article  CAS  PubMed  Google Scholar 

  44. MD Gershon S Bursztajn (1978) ArticleTitleProperties of the enteric nervous system: limitation of access of intravascular macromolecules to the myenteric plexus and muscular externa J Comp Neurol 180 467–88 10.1002/cne.901800305 Occurrence Handle10.1002/cne.901800305 Occurrence Handle1:STN:280:DyaE1c7psVKnsA%3D%3D Occurrence Handle659670

    Article  CAS  PubMed  Google Scholar 

  45. RM Santer DM Baker (1988) ArticleTitleEnteric neuron numbers and sizes in Auerbach’s plexus in the small and large intestine of adult and aged rats J Auton Nerv Syst 25 59–67 10.1016/0165-1838(88)90008-2 Occurrence Handle10.1016/0165-1838(88)90008-2 Occurrence Handle1:STN:280:DyaL1M7ktVWmug%3D%3D Occurrence Handle3225382

    Article  CAS  PubMed  Google Scholar 

  46. M Wilhelm Z Bátori I Pásztor R Gábriel (1998) ArticleTitleNADPH-diaphorase positive myenteric neurons in the ileum of guinea-pig, rat, rabbit and cat: a comparative study Eur J Morphol 36 143–52 10.1076/ejom.36.3.143.4770 Occurrence Handle10.1076/ejom.36.3.143.4770 Occurrence Handle1:STN:280:DyaK1M%2FlvFeqsQ%3D%3D Occurrence Handle9845260

    Article  CAS  PubMed  Google Scholar 

  47. MMDP Furlan S Molinari MH Miranda-Neto (2002) ArticleTitleMorphoquantitative effects of acute diabetes on the myenteric neurons of the proximal colon of adult rats Arq Neuropsiquiatr 60 576–81 Occurrence Handle12244395

    PubMed  Google Scholar 

  48. EA Heinicke JA Kiernan J Wijsman (1987) ArticleTitleSpecific, selective, and complete staining of neurons of the myenteric plexus, using cuprolinic blue J Neurosci Methods 21 45–54 10.1016/0165-0270(87)90101-4 Occurrence Handle10.1016/0165-0270(87)90101-4 Occurrence Handle1:STN:280:DyaL1c%2Fht1KhtA%3D%3D Occurrence Handle2443768

    Article  CAS  PubMed  Google Scholar 

  49. EJA Araújo DMG Sant’ana SL Molinari MH Miranda-Neto (2003) ArticleTitleRegional differences in the number and type of myenteric neurons in the descending colon of rats Arq Neuropsiquiatr 61 220–5 Occurrence Handle12806500

    PubMed  Google Scholar 

  50. A Djazayery DS Miller MJ Stock (1979) ArticleTitleEnergy balances in obese mice Nutr Metab 23 357–67 10.1159/000176281 Occurrence Handle10.1159/000176281 Occurrence Handle1:STN:280:DyaL3c%2Fht1Wgug%3D%3D Occurrence Handle384301

    Article  CAS  PubMed  Google Scholar 

  51. A Firmansyah S Sunoto (1989) ArticleTitleEffect of malnutrition during different periods on the small intestine of the rat Japan J Exp Med 59 1–7 Occurrence Handle1:STN:280:DyaL1M3psVWgsg%3D%3D

    CAS  Google Scholar 

  52. RB Hill J Prosper JS Hirschfield F Kern (1968) ArticleTitleProtein starvation and the small intestine. I. The growth and morphology of the small intestine in weanling rats Exp Mol Pathol 8 66–74 10.1016/0014-4800(68)90006-3 Occurrence Handle10.1016/0014-4800(68)90006-3 Occurrence Handle5637108

    Article  PubMed  Google Scholar 

  53. M Steiner HR Bourges LS Freedman SJ Gray (1968) ArticleTitleEffect of starvation on the tissue composition of the small intestine in the rat Am J Physiol 215 75–7 Occurrence Handle1:STN:280:DyaF1czhs1ertA%3D%3D Occurrence Handle5659346

    CAS  PubMed  Google Scholar 

  54. CM Young P-C Lee E Lebenthal (1987) ArticleTitleMaternal dietary restriction during pregnancy and lactation: effect on digestive organ development in suckling rats Am J Clin Nutr 46 36–40 Occurrence Handle1:STN:280:DyaL2s3mslektw%3D%3D Occurrence Handle2440296

    CAS  PubMed  Google Scholar 

  55. JC Waterlow (1996) Malnutrición proteico-energética Organización Panamericana de la Salud Washington, D.C

    Google Scholar 

  56. H Lorenz-Meyer F Thiel H Menge H Gottesbüren EO Riecken (1977) ArticleTitleStructural and functional studies on the transformation of the intestinal mucosa in rats with experimental diabetes Res Exp Med 170 89–99 10.1007/BF01851379 Occurrence Handle10.1007/BF01851379 Occurrence Handle1:CAS:528:DyaE2sXltFGrtLo%3D

    Article  CAS  Google Scholar 

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Soares, A., Schoffen, J., De Gouveia, E. et al. Effects of the neonatal treatment with monosodium glutamate on myenteric neurons and the intestine wall in the ileum of rats. J Gastroenterol 41, 674–680 (2006). https://doi.org/10.1007/s00535-006-1839-5

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