Food restriction enhances oxidative status in aging rats with neuroprotective effects on myenteric neuron populations in the proximal colon

Experimental Gerontology

Volumn 51, Issue 1, 2014, Pages 54-64

  Schoffen, João Paulo Ferreira ^a   Santi Rampazzo, Ana Paula ^b   Cirilo, Carla Possani ^b   Zapater, Mariana Cristina Umada ^b   Vicentini, Fernando Augusto ^b   Comar, Jurandir Fernando ^b   Bracht, Adelar ^b   Natali, Maria Raquel Marçal ^b  

^a UNIVERSIDADE ESTADUAL DO NORTE DO PARANÁ   (Brazil)

^b STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

Aging; Food restriction; Muscle layer; Myenteric plexus; Oxidative stress

Indexed keywords

CATALASE; CHOLESTEROL; GLOBULIN; GLUTATHIONE; GLUTATHIONE PEROXIDASE; NEURONAL NITRIC OXIDE SYNTHASE; PEPTIDES AND PROTEINS; PROTEIN HUC; PROTEIN HUD; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIOXIDANT ASSAY; ARTICLE; ASCENDING COLON; BLOOD ANALYSIS; CELL SUBPOPULATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET RESTRICTION; GLIA CELL; INTESTINE MUSCLE; MALE; MUSCLE HYPERTROPHY; MUSCLE THICKNESS; MYENTERIC PLEXUS; NEUROPROTECTION; NONHUMAN; NUTRITIONAL STATUS; OXIDATIVE STRESS; PERIKARYON; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; STRUCTURE ANALYSIS;

AGING; FOOD RESTRICTION; MUSCLE LAYER; MYENTERIC PLEXUS; OXIDATIVE STRESS;

ANALYSIS OF VARIANCE; ANIMALS; CALORIC RESTRICTION; CELL SURVIVAL; COLON; ENERGY INTAKE; MALE; MUSCLES; MYENTERIC PLEXUS; NEUROGLIA; NEURONS; NUTRITIONAL STATUS; OXIDATIVE STRESS; RATS, WISTAR;

EID: 84893130378     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2014.01.001     Document Type: Article

References (83)

1. Abdo H., Derkinderen P., Gomes P., Chevalier J., Aubert P., Masson D., et al. Enteric glial cells protect neurons from oxidative stress in part via reduced glutathione. FASEB J. 2010, 24:1082-1094.
2. Abdo H., Mah M.M., Derkinderen P., Bach-Ngohou K., Neunlist M., Lardeux B. The omega-6 fatty acid derivative 15-deoxy-^12,14-prostaglandin J2 is involved in neuroprotection by enteric glial cells against oxidative stress. J. Physiol. 2012, 590:2739-2750.
3. Aebi H. Catalase. Methods of Enzymatic Analysis 1974, 674-678. Verlag Chemie-Academic Press, London. H.U. Bergmeyer (Ed.).
4. Araújo E.J.A., Sant'Ana D.M.G., Molinari S.L., Miranda-Neto M.H. Biometric and food consumption parameters of rats subjected to hypoproteic and hipercaloric diet. Arq. Ciên. Vet. Zool. UNIPAR 2005, 8:131-138.
5. Barja G. Endogenous oxidative stress: relationship to aging, longevity and caloric restriction. Ageing Res. Rev. 2002, 1:397-411.
6. Barzilai N., Banerjee S., Hawkins R., Chen W., Rossetti L. Caloric restriction reverses hepatic insulin resistance in aging rats by decreasing visceral fat. J. Clin. Invest. 1998, 101:1353-1361.
7. Bassotti G., Villanacci V., Fisogni S., Rossi E., Baronio P., Clerici C., et al. Enteric glial cells and their role in gastrointestinal motor abnormalities: introducing the neuro-gliopathies. World J. Gastroenterol. 2007, 13:4035-4041.
8. Belai A., Cooper S., Burnstock G. Effect of age on NADPH-diaphorase containing myenteric neurons of rat ileum and proximal colon. Cell Tissue Res. 1995, 279:379-383.
9. Bernard C.E., Gibbons S.J., Gomez-Pinilla P.J., Lurken M.S., Schmalz P.F., Roeder J.L., et al. Effect of age on the enteric nervous system of the human colon. Neurogastroenterol. Motil. 2009, 21:746-e46.
10. Bernardis L.L., Patterson B.D. Correlation between Lee index and carcass fat content in wealing and adult female rats with hypothalamic lesions. J. Endocrinol. 1968, 40:527-528.
11. Bordone L., Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat. Rev. Mol. Cell Biol. 2006, 6:298-305.
12. Bouras E.P., Tangalos E.G. Chronic constipation in the elderly. Gastroenterol. Clin. N. Am. 2009, 38:463-480.
13. Bross R., Storer T., Bhasin S. Aging and muscle loss. Trends Endocrinol. Metab. 2000, 10:194-198.
14. Buege J.A., Aust S.D. Microsomal lipid peroxidation. Methods Enzymol. 1978, 52:302-310.
15. Buttow N.C., Zucoloto S., Espreafico E.M., Gama P., Alvares E. Substance P enhances neuronal area and epithelial cell proliferation after colon denervation in rats. Dig. Dis. Sci. 2003, 48:2069-2076.
16. Cabarrocas J., Savidge T.C., Liblau R.S. Role of enteric glial cells in inflammatory bowel disease. Glia 2003, 41:81-93.
17. Cho C.G., Kim H.J., Chung S.W., Jung K.J., Shim K.H., Yu B.P., et al. Modulation of glutathione and thioredoxin systems by calorie restriction during the aging process. Exp. Gerontol. 2003, 38:539-548.
18. Cirilo C.P., Schoffen J.P.F., Santi-Rampazzzo A.P., Zapater M.C.V.U., Vicentini F.A., Comar J.F., et al. Dietary restriction interferes with oxidative status and intrinsic intestinal innervation in aging rats. Nutrition 2013, 29:673-680.
19. Coggan A.R. Effects of gender and aging on substrate metabolism during exercise in humans. Perspective in Exercise Science and Sports Medicine 1999, 355-387. Cooper Publishing Group, Carmel. D.R. Lamb, R. Murray (Eds.).
20. Cowen T., Johnson R.J., Soubeyre V., Santer R.M. Restricted diet rescues rat enteric motor neurons from age related cell death. Gut 2000, 47:653-660.
21. Duffy P.H., Leakey J.E.A., Pipkin J.L., Turturro A., Hart R.W. The physiologic, neurologic, and behavioral effects of caloric restriction related to aging, disease, and environmental factors. Environ. Res. 1997, 73:242-248.
22. El-Salhy M., Sandström O., Holmlund F. Age-induced changes in the enteric nervous system in the mouse. Mech. Ageing Dev. 1999, 107:93-103.
23. Erel O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem. 2004, 37:277-281.
24. Finkel T., Holbrook N.J. Oxidants, oxidative stress, and biology of aging. Nature 2000, 400:239-247.
25. Friedlander R.M. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 2003, 348:1365-1375.
26. Gagliardo C.M., Clebis N.K., Stabille S.R., Mari R.B., Sousa J.M.A., De Souza R.R. Exercise reduces inhibitory neuroactivity and protects myenteric neurons from age-related neurodegeneration. Auton. Neurosci. 2008, 141:31-37.
27. Gamage P.P.K.M., Ranson R.N., Patel B.A., Yeoman M.S., Saffrey M.J. Myenteric neuron numbers are maintained in aging mouse distal colon. Neurogastroenterol. Motil. 2013, 25:e495-e505.
28. Giancamillo A.D., Vitari F., Bosi G., Savoini G., Domeneghini C. The chemical code of porcine enteric neurons and the number of enteric glial cells are altered by dietary probiotics. Neurogastroenterol. Motil. 2010, 22:271-278.
29. Gomes O.A., Souza R.R., Liberti E.A. A preliminary investigation of the effects of aging on the nerve cell number in the myenteric ganglia of the human colon. Gerontology 1997, 43:210-217.
30. Gommers A., Dehez-Delhaye M., Caucheteux D. Morphological and metabolic alterations in adipose tissue of very old rats. J. Gerontol. 1983, 38:666-672.
31. Hamden K., Carreau S., Ayadi F., Masmoudi H., El Feki A. Inhibitory effect of estrogens, phytoestrogens, and caloric restriction on oxidative stress and hepato-toxicity in aged rats. Biomed. Environ. Sci. 2009, 22:381-387.
32. Hanani M., Fellig Y., Udassin R., Freund H.R. Age-related changes in the morphology of the myenteric plexus of the human colon. Auton. Neurosci. 2004, 113:71-78.
33. Hillyer E.V., Quesenberry K.E. Ferrets, Rabbits and Rodents Clinical Medicine and Surgery 1997, Saunders, London.
34. Hissin P.J., Hilf R. A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 1976, 74:214-226.
35. Hoyle C.H., Saffrey M.J. Effects of aging on cholinergic neuromuscular transmission in isolated small intestine of ad libitum fed and calorically-restricted rats. Neurogastroenterol. Motil. 2012, 24:586-592.
36. Johnson R.J.R., Schemann M., Santer R.M., Cowen T. The effects of age on the overall population and on sub-populations of myenteric neurons in the rat small intestine. J. Anat. 1998, 192:479-488.
37. Kuyvenhoven J.P., Meinders A.E. Oxidative stress and diabetes mellitus: pathogenesis of long-term complications. Eur. J. Intern. Med. 1999, 10:9-19.
38. Liu W., Yue W., Wu R. Effects of diabetes on expression of glial fibrillary acidic protein and neurotrophins in rat colon. Auton. Neurosci. 2010, 154:79-83.
39. Madsen J.L., Graff J. Effects of ageing on gastrointestinal motor function. Age Ageing 2004, 33:154-159.
40. Marese A.C.M., Freitas P., Natali M.R.M. Alterations of the number and the profile of myenteric neurons of Wistar rats promoted by age. Auton. Neurosci. 2007, 137:10-18.
41. Mattson M.P. Calcium and neurodegeneration. Aging Cell 2007, 6:337-350.
42. Mattson M.P., Magnus T. Ageing and neuronal vulnerability. Nat. Rev. Neurosci. 2006, 7:278-294.
43. Mehdi M.M., Singh P., Rizvi S.I. Erytrocyte sialic acid content during aging in humans: correlation with markers stress. Dis. Markers 2012, 32:179-186.
44. 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.
45. Natali M.R.M., Miranda-Neto M.H., Orsi A.M. Effects of hypoproteic diet supply on adult Wistar rats (Rattus norvegicus). Acta Sci. Biol. Sci. 2000, 22:567-571.
46. Natali M.R.M., Miranda-Neto M.H., Orsi A.M. Morphometry and quantification of the myenteric neurons of the duodenum of adult rats fed with hypoproteic chow. Int. J. Morphol. 2003, 21:273-277.
47. Neunlist M., Van Landeghem L.M., Bourreille A., Savidge T. Neuro-glial crosstalk in inflammatory bowel disease. J. Intern. Med. 2008, 263:577-583.
48. Oliveira M.C., Schoffen J.P.F. Oxidative stress action in cellular aging. Braz. Arch. Biol. Technol. 2010, 53:1333-1342.
49. Oliveira J.C., Scomparin D.X., Andreazzi A.E., Branco R.C.S., Martins A.G., Gravena C., et al. Metabolic imprinting by maternal protein malnourishment impairs vagal activity in adult rats. J. Neuroendocrinol. 2011, 23:148-157.
50. Paglia E.D., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 19:158-169.
51. Palomero J., Galán A.I., Muñoz M.A.E., Tuñón M.A.J., González-Gallego J., Jiménez R. Effects of aging on the susceptibility to the toxic effects of cyclosporin a in rats. Changes in liver glutathione and antioxidant enzymes. Free Radic. Biol. Med. 2001, 30:836-845.
52. Peck C.J., Samsuria S.D., Harrington A.M., King S.K., Hutson J.M., Southwell B.R. Fall in density, but not number of myenteric neurons and circular muscle nerve fibres in guinea-pig colon with ageing. Neurogastroenterol. Motil. 2009, 21:1075-e90.
53. Phillips R.J., Powley T.L. As the gut ages: timetables for aging of innervation vary by organ in the Fischer 344 rat. J. Comp. Neurol. 2001, 434:358-377.
54. Phillips R.J., Powley T.L. Innervation of the gastrointestinal tract: patterns of aging. Auton. Neurosci. 2007, 136:1-19.
55. Phillips R.J., Kieffer E.J., Powley T.L. Aging of the myenteric plexus: neuronal loss is specific to cholinergic neurons. Auton. Neurosci. 2003, 106:69-83.
56. Phillips R.J., Kieffer E.J., Powley T.L. Loss of glia and neurons in the myenteric plexus of the aged Fischer 344 rat. Anat. Embryol. 2004, 209:19-30.
57. Phillips R.J., Rhodes B.S., Powley T.L. Effects of age on sympathetic innervation of the myenteric plexus and gastrointestinal smooth muscle of Fischer 344 rats. Anat. Embryol. 2006, 211:673-683.
58. Porto G.S., Pereira J.N.B., Tibúrcio V.G., Stabille S.R., Faria H.G., Germano R.M., et al. Effect of caloric restriction on myenteric neuroplasticity in the rat duodenum during aging. Auton. Neurosci. 2012, 168:43-47.
59. Ruhl A. Glial cells in the gut. Neurogastroenterol. Motil. 2005, 17:777-790.
60. Saffrey M.J. Cellular changes in the enteric nervous system during ageing. Dev. Biol. 2013, 382:344-355.
61. Santer R.M. Survival of population of NADH-diaforase stained myenteric neurons in small intestine of aged rats. J. Auton. Nerv. Syst. 1994, 49:115-121.
62. Schoffen J.P.F., Soares A., Freitas P., Buttow N.C., Natali M.R.M. Effects of a hypoproteic diet on myosin-V immunostained myenteric neurons and the proximal colon wall of aging rats. Auton. Neurosci. 2005, 122:77-83.
63. Sharma S., Kaur G. Dietary restriction enhances kainate-induced increase in NCAM while blocking the glial activation in adult rat brain. Neurochem. Res. 2008, 33:1178-1188.
64. Siqueira I.R., Fochesatto C., Andrade A., Santos M., Hagen M., Bello-Klein A., et al. Total antioxidant capacity is impaired in different structures from aged rat brain. Int. J. Dev. Neurosci. 2005, 23:663-671.
65. Soares A., Schoffen J.P.F., Gouveia E.M., Natali M.R.M. Effects of the neonatal treatment with monosodium glutamate on myenteric neurons and intestine wall in the ileum of rats. J. Gastroenterol. 2006, 41:674-680.
66. Sohal R.S., Weindruch R. Oxidative stress, caloric restriction, and aging. Science 1996, 273:59-63.
67. Souza R.R., Moratelli H.B., Borges N., Liberti E.A. Age-induced nerve cell loss in the myenteric plexus of the small intestine in man. Gerontology 1993, 39:183-188.
68. Speakman J.R., Mitchell S.E. Caloric restriction. Mol. Aspects Med. 2011, 32:159-221.
69. Starnes J.W., Cantu G., Farrar R.P., Kehrer J.P. Skeletal muscle lipid peroxidation in exercised and food-restricted rats during aging. J. Appl. Physiol. 1989, 67:69-75.
70. Takahashi T., Qoubaitary A., Owyang C., Wiley J.W. Decreased expression of nitric oxide synthase in the colonic myenteric plexus of aged rats. Brain Res. 2000, 883:15-21.
71. Tappel A.L. Glutathione peroxidase and hydroperoxides. Methods Enzymol. 1978, 52:506-513.
72. Thrasivoulou C., Soubeyre V., Ridha H., Giuliani D., Giaroni C., Michael G.J., et al. Reactive oxygen species, dietary restriction and neurotrophic factors in age-related loss of myenteric neurons. Aging Cell 2006, 5:247-257.
73. Valle A., Sastre-Serra J., Roca P., Oliver J. Modulation of white adipose tissue proteome by aging and calorie restriction. Aging Cell 2010, 9:882-894.
74. Vasiljković N.L., Pešić V., Tanić N., Milanović D., Popić J., Kanazir S., et al. Changes in markers of neuronal and glial plasticity after cortical injury induced by food restriction. Exp. Neurol. 2009, 220:198-206.
75. Von Boyen G., Steinkamp M. The enteric glia and neurotrophic factors. Gastroenterology 2006, 44:985-990.
76. Wachsman J.T. The beneficial effects of dietary restriction: reduced oxidative damage and enhanced apoptosis. Mutat. Res. 1996, 350:25-34.
77. Wade P.R. Aging and neural control of the GI tract I. Age-related changes in the enteric nervous system. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 283:G489-G495.
78. Wiley J.W. Aging of neural control of the GI tract. Senescent enteric nervous system: lessons from extraintestinal sites and nonmammalian species. Am. J. Physiol. Gastrointest. Liver Physiol. 2002, 46:1020-1026.
79. Wiskur B., Meerveld B.G. The aging colon: the role of enteric neurodegeneration in constipation. Curr. Gastroenterol. Rep. 2010, 12:507-512.
80. Wu M., Nassauw L.V., Adriaensen A.B.A.K.D., Timmermans J.P. Myenteric nitrergic neurons along the rat esophagus: evidence for regional and strain differences in age-related changes. Histochem. Cell Biol. 2003, 119:395-403.
81. Zanoni J.N., Buttow N.C., Bazotte R.B., Miranda-Neto M.H. Evaluation of the population of NADPH-diaphorase-stained and myosin-V myenteric neurons in the ileum of chronically streptozotocin-diabetic rats treated with ascorbic acid. Auton. Neurosci. 2003, 104:32-38.
82. Zhang Y., Herman B. Ageing Apoptosis Mech. Ageing Dev. 2002, 123:245-260.
83. Zucoloto S., Deus D.A., Martins A.A., Muglia V.F., Kajiwara J.K., Garcia S.B. The relationship between myenteric neuronal denervation, smooth muscle thickening and epithelial cell proliferation in the rat colon. Res. Exp. Med. 1997, 197:117-124.