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Abstract:

We evaluated the effects of protein malnutrition on liver morphology and physiology in rats subjected to different malnutrition schemes. Pregnant rats were fed with a control diet or a low protein diet (LPD). Male offspring rats received a LPD during gestation, lactation, and until they were 60 days old (MM group), a late LPD that began after weaning (CM), or a LPD administrated only during the gestation-lactation period followed by a control diet (MC). On day 60, blood was collected and the liver was dissected out. We found a decrease in MM rats’ total body (p < 0.001) and liver (p < 0.05) weight. These and CM rats showed obvious liver dysfunction reflected by the increase in serum glutamic pyruvic transaminase (SGOT) (MM p < 0.001) and serum glutamic pyruvic transaminase (SGPT) (MM and CM p < 0.001) enzymes, and liver content of cholesterol (MM and CM p < 0.001) and triglycerides (MM p < 0.01; CM p < 0.001), in addition to what we saw by histology. Liver dysfunction was also shown by the increase in gamma glutamyl transferase (GGT) (MM, MC, and CM p < 0.001) and GST-pi1 (MM and CM p < 0.001, MC p < 0.05) expression levels. MC rats showed the lowest increment in GST-pi1 expression (MC vs. MM; p < 0.001, MC vs. CM; p < 0.01). ROS production (MM, CM, and MC: p < 0.001), lipid peroxidation (MM, CM, and MC p < 0.001), content of carbonyl groups in liver proteins (MM and CM p < 0.001, MC p < 0.01), and total antioxidant capacity (MM, CM, and MC p < 0.001) were increased in the liver of all groups of malnourished animals. However, MM rats showed the highest increment. We found higher TNF-α (MM and CM p < 0.001), and IL-6 (MM and CM p < 0.001) serum levels and TGF-β liver content (MM p < 0.01; CM p < 0.05), in MM and CM groups, while MC rats reverted the values to normal levels. Pro-survival signaling pathways mediated by tyrosine or serine/threonine kinases (pAKT) (MM and CM p < 0.001; MC p < 0.01) and extrasellular signal-regulated kinase (pERKs) (MM p < 0.01; CM p < 0.05) appeared to be activated in the liver of all groups of malnourished rats, suggesting the presence of cells resistant to apoptosis which would become cancerous. In conclusion, a LPD induced liver damage whose magnitude was related to the developmental stage at which malnutrition occurs and to its length. © 2017, University of Navarra.

Registro:

Documento: Artículo
Título:Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats
Autor:Campisano, S.E.; Echarte, S.M.; Podaza, E.; Chisari, A.N.
Filiación:Departamento de Química, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Dean Funes 3350, Buenos Aires, Argentina
Instituto de Investigaciones Biológicas, CONICET-Universidad Nacional de Mar del Plata, 4th level Dean Funes 3250, Buenos Aires, Argentina
Palabras clave:Fetal programming; Liver damage; Low protein diet; Metabolic syndrome; Non-alcoholic fatty liver; Wistar rats
Año:2017
Volumen:73
Número:2
Página de inicio:275
Página de fin:285
DOI: http://dx.doi.org/10.1007/s13105-017-0549-1
ISSN:11387548
CODEN:JPBIF
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_11387548_v73_n2_p275_Campisano

Referencias:

  • Reddanna, A.S., P. and Thyagaraju. Does glutathione S-transferase pi (GST-pi) a marker protein for cancer? (2003) Mol Cell Biochem, 253 (1-2), pp. 319-327
  • Armitage, J.A., Taylor, P.D., Poston, L., Experimental models of developmental programming: consequences of exposure to an energy rich diet during development (2005) J Physiol, 565, pp. 3-8. , COI: 1:CAS:528:DC%2BD2MXkslyrurk%3D, PID: 15695245
  • Barker, D.J., Eriksson, J.G., Forsén, T., Fetal origins of adult disease: strength of effects and biological basis (2002) Int J Epidemiol, 31 (6), pp. 1235-1239. , COI: 1:STN:280:DC%2BD3s%2FosVOksw%3D%3D, PID: 12540728
  • Beyaert, R., Van Loo, G., Heyninck, K., Signaling to gene activation and cell death by tumor necrosis factor receptors and Fas (2002) Int Rev Cytol, 214, pp. 225-272. , COI: 1:CAS:528:DC%2BD38XlsVWrtrc%3D, PID: 11893167
  • Caballero, V.J., Mendieta, J.R., Giudici, A.M., Alternation between dietary protein depletion and normal feeding cause liver damage in mouse (2011) J Physiol Biochem, 67 (1), pp. 43-52. , COI: 1:CAS:528:DC%2BC3MXhs1Ghsr8%3D, PID: 20878513
  • D'Autreaux, B., Toledano, M.B., ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis (2007) Nat Rev Mol Cell Biol, 8 (10), pp. 813-824. , PID: 17848967
  • De Oliveira, I.M.V., Fujimori, E., Liver gamma-glutamyl transpeptidase activity and glutathione levels in lactating rats and pups: effect of dietary protein quantity and feed intake (1996) J Nutr Biochem, 7 (2), pp. 93-98
  • Desai, M., Crowther, N.J., Lucas, A., Organ-selective growth in the offspring of protein-restricted mothers (1996) Br J Nutr, 76 (4), pp. 591-603. , COI: 1:CAS:528:DyaK28Xnt1Kiur0%3D, PID: 8942365
  • Fagundes, A.T., Moura, E.G., Passos, M.C., Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring (2007) Br J Nutr, 98 (5), pp. 922-928. , COI: 1:CAS:528:DC%2BD2sXhtlSktLbL, PID: 17524178
  • Francés, D.E., Ingaramo, P.I., Ronco, M.T., Diabetes, an inflammatory process: oxidative stress and TNF-alpha involved in hepatic complication (2013) J Biomedical Science and Engineering, 6 (6), pp. 645-653
  • Fraser, A., Ebrahim, S., Smith, G.D., The associations between birth weight and adult markers of liver damage and function (2008) Paediatr Perinat Epidemiol, 22 (1), pp. 12-21. , PID: 18173779
  • Gabory, A., Attig, L., Junien, C., Sexual dimorphism in environmental epigenetic programming (2009) Mol Cell Endocrinol, 304, pp. 8-18. , COI: 1:CAS:528:DC%2BD1MXls1ylsLY%3D, PID: 19433243
  • George, L.A., Zhang, L., Tuersunjiang, N., Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring (2012) Am J Physiol Regul Integr Comp Physiol, 302 (7), pp. R795-R804. , COI: 1:CAS:528:DC%2BC38XmvFSjsL8%3D, PID: 22277936
  • Gosby, A.K., Maloney, C.A., Phuyal, J.L., Maternal protein restriction increase hepatic glycogen storage in young rats (2003) Pediatr Res, 54 (3), pp. 413-418. , COI: 1:CAS:528:DC%2BD3sXmtFGlsbo%3D, PID: 12788979
  • Grundy, S.M., Gamma-glutamyl transferase: another biomarker for metabolic syndrome and cardiovascular risk (2007) Arterioscler Thromb Vasc Biol, 27 (1), pp. 4-7. , COI: 1:CAS:528:DC%2BD2sXhtVygsrg%3D, PID: 17185620
  • Jahan-Mihan, A., Rodriguez, J., Christie, C., The role of maternal dietary proteins in development of metabolic syndrome in offspring (2015) Nutrients, 7 (11), pp. 9185-9217. , COI: 1:CAS:528:DC%2BC28XitVGltr%2FM, PID: 26561832
  • Jungst, C., Cheng, B., Gehrke, R., Oxidative damage is increased in human liver tissue adjacent to hepatocellular carcinoma (2004) Hepatology, 39 (6), pp. 1663-1672. , PID: 15185308
  • Kew, M.C., Hepatocellular carcinoma in developing countries: prevention, diagnosis and treatment (2012) World J Hepatol, 4 (3), pp. 99-104. , PID: 22489262
  • Kastl, L., Sauer, S.W., Ruppert, T., TNF-α mediates mitochondrial uncoupling and enhances ROS-dependent cell migration via NF-κB activation in liver cells (2014) FEBS Lett, 588 (1), pp. 175-183. , COI: 1:CAS:528:DC%2BC3sXhvFOhsbbL, PID: 24316229
  • Kirillova, I., Chaisson, M., Fausto, N., Tumor necrosis factor induces DNA replication in hepatic cells through nuclear factor kappa B activation (1999) Cell Growth Differ, 10 (12), pp. 819-828. , COI: 1:CAS:528:DC%2BD3cXhslagtw%3D%3D, PID: 10616907
  • Krishnamurthy, H.A., The serum gamma glutamyl transpeptidase—a non invasive diagnostic bio marker of chronic anicteric non alcoholic liver diseases (2013) J Clin Diagn Res, 7 (4), pp. 691-694. , COI: 1:CAS:528:DC%2BC3sXmsVKqt74%3D
  • Kunz, L.H., King, J.C., Impact of maternal nutrition and metabolism on health of the offspring (2007) Semin Fetal Neonatal Med, 12 (1), pp. 71-77. , PID: 17200031
  • Leonard, T.B., Neptun, D.A., Popp, J.A., Serum gamma glutamyl transferase as a specific indicator of bile duct lesions in the rat liver (1984) Am J Pathol, 116 (2), pp. 262-269. , COI: 1:CAS:528:DyaL2cXlt1ygsrg%3D, PID: 6147091
  • Li, J., Wang, H., Stoner, G.D., Dietary supplementation with cysteine prodrugs selectively restores tissue glutathione levels and redox status in protein malnourished mice (2002) J Nutr Biochem, 13 (10), pp. 625-633. , PID: 12550075
  • Li, M., Reynolds, C.M., Segovia, S.A., Developmental programming of nonalcoholic fatty liver disease: the effect of early life nutrition on susceptibility and disease severity in later life (2015) Biomed Res Int, 2015, p. 437107. , PID: 26090409
  • Liu, X., Qi, Y., Tian, B., Maternal protein restriction induces alterations in hepatic tumor necrosis factor-αCYP7A1 signaling and disorders regulation of cholesterol metabolism in the adult rat offspring (2014) J Clin Biochem Nutr, 55 (1), pp. 40-47. , COI: 1:CAS:528:DC%2BC2cXhsFGhtb%2FP, PID: 25120278
  • Maloney, C., Gosby, A.K., Phuyal, J.L., Site-specific change in the expression of fat-partitioning genes in weanling rats exposed to a low-protein diet in utero (2003) Obes Res, 11 (3), pp. 461-468. , COI: 1:CAS:528:DC%2BD3sXisVKgtbs%3D, PID: 12634446
  • Mao, J., Zhanga, X., Sielia, P.T., Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta (2010) PNAS, 107 (12), pp. 5557-5562. , COI: 1:CAS:528:DC%2BC3cXktFKhsLc%3D, PID: 20212133
  • Murata, M., Matzusaki, K., Yoshida, K., Hepatitis B virus X protein shifts human hepatic transforming growth factor (TGF)-beta signaling from tumor suppression to oncogenesis in early chronic hepatitis B (2009) Hepatology, 49 (4), pp. 1203-1217. , COI: 1:CAS:528:DC%2BD1MXkslWjsrw%3D, PID: 19263472
  • Nobili, V., Marcellini, M., Marchesini, G., Intrauterine growth retardation, insulin resistance, and nonalcoholic fatty liver disease in children (2007) Diabetes Care, 30 (10), pp. 2638-2640. , PID: 17536073
  • Oda, K., Uto, H., Mawatari, S., Clinical features of hepatocellular carcinoma associated with nonalcoholic fatty liver disease: a review of human studies (2015) Clin J Gastroenterol, 8 (1), pp. 1-9. , PID: 25575848
  • Ozcan, E., A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation (2004) Clin Biochem, 37 (4), pp. 277-285
  • Perumpail, R.B., Wong, R.J., Ahmed, A., Hepatocellular carcinoma in the setting of non-cirrhotic nonalcoholic fatty liver disease and the metabolic syndrome: US experience (2015) Dig Dis Sci, 60 (10), pp. 3142-3148. , COI: 1:CAS:528:DC%2BC2MXhtlelsbzP, PID: 26250831
  • Petry, C.J., Hales, C.N., Long-term effects on offspring of intrauterine exposure to deficits in nutrition (2000) Hum Reprod Update, 6 (6), pp. 578-586. , COI: 1:CAS:528:DC%2BD3cXptVWquro%3D, PID: 11129690
  • Podaza, E., Echarte, E.M., Chisari, A.N., A low maternal protein diet during pregnancy and lactation induce liver offspring dysfunction, in the rat (2015) Ann Nutr Disord & Ther, 2 (1), p. id1020
  • Rana, S., Sodhi, C.P., Mehta, S., Protein-energy malnutrition and oxidative injury in growing rats (1996) Hum Exp Toxicol, 15 (10), pp. 810-814. , COI: 1:CAS:528:DyaK28XntVersbY%3D, PID: 8906429
  • Ravelli, A.C.J., van Der Meulen, J.H., Osmond, C., Obesity at the age of 50 y in men and women exposed to famine prenatally (1999) Am J Clin Nutr, 70 (5), pp. 811-816. , COI: 1:CAS:528:DyaK1MXntFCgtbk%3D, PID: 10539740
  • Ronchi, V.P., Giudici, A.M., Mendieta, J.R., Oxidative stress in mouse liver caused by dietary amino acid deprivation: protective effect of methionine (2010) J Physiol Biochem, 66 (2), pp. 93-103. , COI: 1:CAS:528:DC%2BC3cXosl2ntLc%3D, PID: 20577846
  • Roseboom, T., de Rooij, S., Painter, R., The Dutch famine and its long-term consequences for adult health (2006) Early Hum Dev, 82 (8), pp. 485-491. , PID: 16876341
  • Ross, M.G., Beall, M.H., Adult sequelae of intrauterine growth restriction (2008) Semin Perinatol, 32 (3), pp. 213-218. , PID: 18482624
  • Simmons, R.A., Templeton, L.J., Gertz, S.J., Intrauterine growth retardation leads to the development of type 2 diabetes in the rat (2001) Diabetes, 50 (10), pp. 2279-2286. , COI: 1:CAS:528:DC%2BD3MXntlGhurc%3D, PID: 11574409
  • Teschke, R., Neuefeind, M., Nishimura, M., Hepatic gamma-glutamyltransferase activity in alcoholic fatty liver: comparison with other liver enzymes in man and rats (1983) Gut, 24 (7), pp. 625-630. , COI: 1:CAS:528:DyaL3sXltVSktbk%3D, PID: 6134656
  • Valgimigli, M., Valgimigli, L., Treré, D., Oxidative stress EPR measurement in human liver by radical-probe technique. Correlation with etiology, histology and cell proliferation (2002) Free Radic Res, 36 (9), pp. 939-948. , COI: 1:CAS:528:DC%2BD3sXit1WjsLw%3D, PID: 12448819
  • Weinberg, F., Hamanaka, R., Wheaton, W.W., Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity (2010) Proc Natl Acad Sci U S A, 107 (19), pp. 8788-8793. , COI: 1:CAS:528:DC%2BC3cXmsFWmurs%3D, PID: 20421486
  • Yamada, M., Wolfe, D., Han, G., Early onset of fatty liver in growth restricted rat fetuses and newborns (2011) Congenit Anom (Kyoto), 51 (4), pp. 167-173. , COI: 1:CAS:528:DC%2BC38XitFCksLo%3D
  • Yamada, Y., Webber, E.M., Kirillova, I., Analysis of liver regeneration in mice lacking type 1 or type 2 tumor necrosis factor receptor: requirement for type 1 but not type 2 receptor (1998) Hepatology, 28 (4), pp. 959-970. , COI: 1:CAS:528:DyaK1cXmvVSlurk%3D, PID: 9755232
  • Yang, Y.A., Zhang, G.M., Feigenbaum, L., Smad3 reduces susceptibility to hepatocarcinoma by sensitizing hepatocytes to apoptosis through downregulation of Bcl-2 (2006) Cancer Cell, 9 (6), pp. 445-457. , COI: 1:CAS:528:DC%2BD28Xmt1eksLc%3D, PID: 16766264
  • Zimmeran, H.J., Henry, J.B., Determinaciones de las enzimas séricas como ayuda diagnóstica (1978) Todd-Sanford. Diagnóstico clínico por el laboratorio, pp. 859-889. , Davidsohn I, Henry JB, (eds), Salvat, Barcelona

Citas:

---------- APA ----------
Campisano, S.E., Echarte, S.M., Podaza, E. & Chisari, A.N. (2017) . Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats, 73(2), 275-285.
http://dx.doi.org/10.1007/s13105-017-0549-1
---------- CHICAGO ----------
Campisano, S.E., Echarte, S.M., Podaza, E., Chisari, A.N. "Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats" 73, no. 2 (2017) : 275-285.
http://dx.doi.org/10.1007/s13105-017-0549-1
---------- MLA ----------
Campisano, S.E., Echarte, S.M., Podaza, E., Chisari, A.N. "Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats" , vol. 73, no. 2, 2017, pp. 275-285.
http://dx.doi.org/10.1007/s13105-017-0549-1
---------- VANCOUVER ----------
Campisano, S.E., Echarte, S.M., Podaza, E., Chisari, A.N. Protein malnutrition during fetal programming induces fatty liver in adult male offspring rats. 2017;73(2):275-285.
http://dx.doi.org/10.1007/s13105-017-0549-1