Skip to main content
Erschienen in: European Journal of Nutrition 8/2018

23.09.2017 | Original Contribution

Intrauterine hyperglycemia-induced inflammatory signalling via the receptor for advanced glycation end products in the cardiac muscle of the infants of diabetic mother rats

verfasst von: Ritsuko Kawaharada, Haruna Masuda, Zhenyi Chen, Eric Blough, Tomoko Kohama, Akio Nakamura

Erschienen in: European Journal of Nutrition | Ausgabe 8/2018

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Gestational diabetes is associated with increased risk to the health of the mother and her offspring. In particular, the infants of diabetic mothers (IDMs) exhibit elevated levels of preterm birth, macrosomia, hypoglycemia, hypocalcemia, and cardiomyopathy. We have previously reported that IDMs showed abnormalities in cardiac Akt-related insulin signalling, and that these deficiencies in Akt-related signalling were attenuated by supplementing the maternal diet with fish-oil. Herein, we investigated whether the eicosapentaenoic acid (EPA) found in fish oil can be used to attenuate diabetes associated impairments in cardiomyocyte signalling.

Methods

Pregnant diabetic rats were administered streptozotocin before receiving EPA or water, and their infants were designated IDM/EPA, IDM/W. We assessed the potential molecular pathway for this effect in the primary cardiac cell from newborn rat hearts.

Results

Insulin resistance as determined by diminished GLUT4 translocation following insulin stimulation, the levels of advanced glycation end products (AGEs) and reactive oxygen species were elevated in the neonatal hearts of IDM/W compared with that seen in the offspring born from non-diabetic control animals. Similarly, the receptor of AGEs (RAGE) mRNA levels, reactive oxygen species and the amount of nuclear factor-κB (NF-κB), tumor necrosis factor-α (TNF-α), and interleukin 6 (IL-6) mRNA were higher in the hearts from the IDM/W when compared to that observed in the hearts of offspring born to non-diabetic animals. These deleterious effects of gestational diabetes were significantly decreased in the offspring of diabetic mothers receiving EPA supplementation.

Conclusions

Taken together, our data suggest that the EPA in fish oil may improve the impaired signalling and the excessive protein glycation in the cardiac muscles of infants exposed to intrauterine hyperglycemia.
Literatur
1.
Zurück zum Zitat Cordero L, Treuer SH, Landon MB, Gabbe SG (1998) Management of infants of diabetic mothers. Arch Pediatr Adolesc Med 152:249–254CrossRef Cordero L, Treuer SH, Landon MB, Gabbe SG (1998) Management of infants of diabetic mothers. Arch Pediatr Adolesc Med 152:249–254CrossRef
2.
Zurück zum Zitat Coetzee EJ, Levitt NS (2000) Maternal diabetes and neonatal outcome. Semin Neonatol 5:221–229CrossRef Coetzee EJ, Levitt NS (2000) Maternal diabetes and neonatal outcome. Semin Neonatol 5:221–229CrossRef
3.
Zurück zum Zitat Mimouni F, Miodovnik M, Siddiqi TA, Khoury J, Tsang RC (1988) Perinatal asphyxia in infants of insulin-dependent diabetic mothers. J Pediatr 113:345–353CrossRef Mimouni F, Miodovnik M, Siddiqi TA, Khoury J, Tsang RC (1988) Perinatal asphyxia in infants of insulin-dependent diabetic mothers. J Pediatr 113:345–353CrossRef
4.
Zurück zum Zitat Manco-Johnson MJ, Carver T, Jacobson LJ, Townsend SF, Hay WW Jr (1994) Hyperglycemia induced hyperinsulinemia decreases maternal and fetal plasma protein C concentration during ovine gestation. Pediatr Res 36:293–299CrossRef Manco-Johnson MJ, Carver T, Jacobson LJ, Townsend SF, Hay WW Jr (1994) Hyperglycemia induced hyperinsulinemia decreases maternal and fetal plasma protein C concentration during ovine gestation. Pediatr Res 36:293–299CrossRef
5.
Zurück zum Zitat Weindling MA (2009) Offspring of diabetic pregnancy: short-term outcomes. Semin Fetal Neonatal Med 14:111–118CrossRef Weindling MA (2009) Offspring of diabetic pregnancy: short-term outcomes. Semin Fetal Neonatal Med 14:111–118CrossRef
6.
Zurück zum Zitat Hunter DJ, Burrows RF, Mohide PT, Whyte RK (1993) Influence of maternal insulin-dependent diabetes mellitus on neonatal morbidity CMAJ. 149(1):47–52PubMed Hunter DJ, Burrows RF, Mohide PT, Whyte RK (1993) Influence of maternal insulin-dependent diabetes mellitus on neonatal morbidity CMAJ. 149(1):47–52PubMed
7.
Zurück zum Zitat Lisowski LA, Verheijen PM, Copel JA, Kleinman CS, Wassink S, Visser GH, Meijboom EJ (2010) Congenital heart disease in pregnancies complicated by maternal diabaetes mellitus. An international clinical collaboration, literature review, and meta-analysis. Herz 35:19–26CrossRef Lisowski LA, Verheijen PM, Copel JA, Kleinman CS, Wassink S, Visser GH, Meijboom EJ (2010) Congenital heart disease in pregnancies complicated by maternal diabaetes mellitus. An international clinical collaboration, literature review, and meta-analysis. Herz 35:19–26CrossRef
8.
Zurück zum Zitat Mann DL (2002) Inflammatory mediators and the failing heart: past, present and the foreseeable future. Circ Res 91:988–998CrossRef Mann DL (2002) Inflammatory mediators and the failing heart: past, present and the foreseeable future. Circ Res 91:988–998CrossRef
9.
Zurück zum Zitat Nian M, Lee P, Khaper N, Liu P (2004) Inflammatory cytokines and postmyocardial infarction remodeling. Circ Res 94:1543–1553CrossRef Nian M, Lee P, Khaper N, Liu P (2004) Inflammatory cytokines and postmyocardial infarction remodeling. Circ Res 94:1543–1553CrossRef
10.
Zurück zum Zitat Aukrust P, Gullestad L, Ueland T, Damås JK, Yndestad A (2005) Inflammatory and anti-inflammatory cytokines in chronic heart failure: potential therapeutic implications. Ann Med 37:74–85CrossRef Aukrust P, Gullestad L, Ueland T, Damås JK, Yndestad A (2005) Inflammatory and anti-inflammatory cytokines in chronic heart failure: potential therapeutic implications. Ann Med 37:74–85CrossRef
11.
Zurück zum Zitat Bourcier T, Sukhova G, Libby P (1997) The nuclear factor κB signaling pathway participates in dysregulation of vascular smooth muscle cells in vitro and in human atherosclerosis. J Biol Chem 272:15817–15824CrossRef Bourcier T, Sukhova G, Libby P (1997) The nuclear factor κB signaling pathway participates in dysregulation of vascular smooth muscle cells in vitro and in human atherosclerosis. J Biol Chem 272:15817–15824CrossRef
12.
Zurück zum Zitat Satoh H, Togo M, Hara M, Miyata T, Han K, Maekawa H, Ohno M, Hashimoto Y, Kurokawa K, Watanabe T (1997) Advanced glycation endproducts stimulate mitogen-activated protein kinase and proliferation in rabbit vascular smooth muscle cells. Biochem Biophys Res Commun 239:111–115CrossRef Satoh H, Togo M, Hara M, Miyata T, Han K, Maekawa H, Ohno M, Hashimoto Y, Kurokawa K, Watanabe T (1997) Advanced glycation endproducts stimulate mitogen-activated protein kinase and proliferation in rabbit vascular smooth muscle cells. Biochem Biophys Res Commun 239:111–115CrossRef
13.
Zurück zum Zitat Nasu-Kawaharada R, Nakamura A, Kakarla SK, Blough ER, Kohama K, Kohama T (2013) A maternal diet rich in fish oil may improve cardiac Akt-related signaling in the offspring of diabetic mother rats. Nutrition 29(4):688–692CrossRef Nasu-Kawaharada R, Nakamura A, Kakarla SK, Blough ER, Kohama K, Kohama T (2013) A maternal diet rich in fish oil may improve cardiac Akt-related signaling in the offspring of diabetic mother rats. Nutrition 29(4):688–692CrossRef
14.
Zurück zum Zitat Reinking BE, Wedemeyer EW, Weiss RM, Segar JL, Scholz TD (2009) Cardiomyopathy in offspring of diabetic rats is associated with activation of the MAPK and apoptotic pathways. Cardiovasc Diabetol 8:43CrossRef Reinking BE, Wedemeyer EW, Weiss RM, Segar JL, Scholz TD (2009) Cardiomyopathy in offspring of diabetic rats is associated with activation of the MAPK and apoptotic pathways. Cardiovasc Diabetol 8:43CrossRef
15.
Zurück zum Zitat Scott PH, Brunn GJ, Kohn AD, Roth RA, Lawrence JC (1998) Evidence of insulin-stimulated phos-phorylation and activation of the mammalian tar-get of rapamycin mediated by a protein kinase B signaling pathway. Proc Natl Acad Sci USA 95:7772–7777CrossRef Scott PH, Brunn GJ, Kohn AD, Roth RA, Lawrence JC (1998) Evidence of insulin-stimulated phos-phorylation and activation of the mammalian tar-get of rapamycin mediated by a protein kinase B signaling pathway. Proc Natl Acad Sci USA 95:7772–7777CrossRef
16.
Zurück zum Zitat Sale EM, Sale GJ (2008) Protein kinase B: signaling roles and therapeutic targeting. Cell Mol Life Sci 65:113–127CrossRef Sale EM, Sale GJ (2008) Protein kinase B: signaling roles and therapeutic targeting. Cell Mol Life Sci 65:113–127CrossRef
17.
Zurück zum Zitat Bryant NJ, Govers R, James DE (2002) Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3:267–277CrossRef Bryant NJ, Govers R, James DE (2002) Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol 3:267–277CrossRef
18.
Zurück zum Zitat Tanikawa T, Okada Y, Tanikawa R, Tanaka Y (2009) Advanced glycation end products induce calcification of vascular smooth muscle cells through RAGE/p38 mapk. J Vasc Res 46:572–580CrossRef Tanikawa T, Okada Y, Tanikawa R, Tanaka Y (2009) Advanced glycation end products induce calcification of vascular smooth muscle cells through RAGE/p38 mapk. J Vasc Res 46:572–580CrossRef
19.
Zurück zum Zitat Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM, Cave AC (2006) Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 113:1235–1243CrossRef Zhang M, Kho AL, Anilkumar N, Chibber R, Pagano PJ, Shah AM, Cave AC (2006) Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 113:1235–1243CrossRef
20.
Zurück zum Zitat Bierhaus A, Schiekofer S, Schwaninger M et al (2001) Diabetes-associated sustained activation of the transcription factor nuclear factor-B. Diabetes 50:2792–2808CrossRef Bierhaus A, Schiekofer S, Schwaninger M et al (2001) Diabetes-associated sustained activation of the transcription factor nuclear factor-B. Diabetes 50:2792–2808CrossRef
21.
Zurück zum Zitat Park S, Park Y (2009) Effects of dietary fish-oil and trans fat on rat aorta histopathology and cardiovascular risk markers. Nutr Res Pract 3(2):102–107CrossRef Park S, Park Y (2009) Effects of dietary fish-oil and trans fat on rat aorta histopathology and cardiovascular risk markers. Nutr Res Pract 3(2):102–107CrossRef
22.
Zurück zum Zitat Kromhout D, Geleijnse JM, de Goede J, Oude Griep LM, Mulder BJ, de Boer MJ, Deckers JW, Boersma E, Zock PL, Giltay EJ (2011) n-3 fatty acids, ventricular arrhythmia-related events, and fatal myocardial infarction in postmyocardial infarction patients with diabetes. Diabetes Care 34(12):2515–2520CrossRef Kromhout D, Geleijnse JM, de Goede J, Oude Griep LM, Mulder BJ, de Boer MJ, Deckers JW, Boersma E, Zock PL, Giltay EJ (2011) n-3 fatty acids, ventricular arrhythmia-related events, and fatal myocardial infarction in postmyocardial infarction patients with diabetes. Diabetes Care 34(12):2515–2520CrossRef
23.
Zurück zum Zitat Alexander DD, Miller PE, Van Elswyk ME, Kuratko CN, Bylsma LC (2017) A Meta-analysis of randomized controlled trials and prospective cohort studies of eicosapentaenoic and docosahexaenoic long-chain omega-3 fatty acids and coronary heart disease risk. Mayo Clin Proc 92(1):15–29CrossRef Alexander DD, Miller PE, Van Elswyk ME, Kuratko CN, Bylsma LC (2017) A Meta-analysis of randomized controlled trials and prospective cohort studies of eicosapentaenoic and docosahexaenoic long-chain omega-3 fatty acids and coronary heart disease risk. Mayo Clin Proc 92(1):15–29CrossRef
24.
Zurück zum Zitat Figueras M, Olivan M, Busquets S, López-Soriano FJ, Argilés JM (2011) Effects of eicosapentaenoic acid (EPA) treatment on insulin sensitivity in an animal model of diabetes: improvement of the inflammatory status. Obesity (Silver Spring) 19:362–369CrossRef Figueras M, Olivan M, Busquets S, López-Soriano FJ, Argilés JM (2011) Effects of eicosapentaenoic acid (EPA) treatment on insulin sensitivity in an animal model of diabetes: improvement of the inflammatory status. Obesity (Silver Spring) 19:362–369CrossRef
25.
Zurück zum Zitat Yuen VG, McNeill JH (1990) Comparison of the glucose oxidase method for glucose determination by manual assay and automated analyser. J Pharmacol Toxicol Methods 44(3):543–546CrossRef Yuen VG, McNeill JH (1990) Comparison of the glucose oxidase method for glucose determination by manual assay and automated analyser. J Pharmacol Toxicol Methods 44(3):543–546CrossRef
26.
Zurück zum Zitat Klotzsch SG, McNamara JR (1990) Triglyceride measurements: a review of methods and interferences. Clin Chem 36(9):1605–1613PubMed Klotzsch SG, McNamara JR (1990) Triglyceride measurements: a review of methods and interferences. Clin Chem 36(9):1605–1613PubMed
27.
Zurück zum Zitat Mitcheson JS, Hancox JC, Levi AJ (1998) Cultured adult cardiac myocytes: future applications, culture methods, morphological and electrophysiological properties. Cardiovasc Res 39:280–300CrossRef Mitcheson JS, Hancox JC, Levi AJ (1998) Cultured adult cardiac myocytes: future applications, culture methods, morphological and electrophysiological properties. Cardiovasc Res 39:280–300CrossRef
28.
Zurück zum Zitat Quon MJ, Chen H, Ing BL, Liu ML, Zarnowski MJ, Yonezawa K, Kasuga M, Cushman SW, Taylor SI (1995) Roles of 1-phosphatidylinositol 3-kinase and ras in regulating translocation of GLUT4 in transfected rat adipose cells. Mol Cell Biol 15(10):5403–5411CrossRef Quon MJ, Chen H, Ing BL, Liu ML, Zarnowski MJ, Yonezawa K, Kasuga M, Cushman SW, Taylor SI (1995) Roles of 1-phosphatidylinositol 3-kinase and ras in regulating translocation of GLUT4 in transfected rat adipose cells. Mol Cell Biol 15(10):5403–5411CrossRef
29.
Zurück zum Zitat Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M (1994) Essential role of phosphatidylinositol 3-kinase in insulininduced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem 269(5):3568–3573PubMed Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M (1994) Essential role of phosphatidylinositol 3-kinase in insulininduced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin. J Biol Chem 269(5):3568–3573PubMed
30.
Zurück zum Zitat Zhang Y, Yan W, Collins MA, Bednar F, Rakshit S, Zetter BR, Stanger BZ, Chung I, Rhim AD, di Magliano MP (2013) Interleukin-6 is required for pancreatic cancer progression by promoting MAPK signaling activation and oxidative stress resistance. Cancer Res 73(20):6359–6374CrossRef Zhang Y, Yan W, Collins MA, Bednar F, Rakshit S, Zetter BR, Stanger BZ, Chung I, Rhim AD, di Magliano MP (2013) Interleukin-6 is required for pancreatic cancer progression by promoting MAPK signaling activation and oxidative stress resistance. Cancer Res 73(20):6359–6374CrossRef
31.
Zurück zum Zitat Ostadrahimi A, Mohammad-Alizadeh S, Mirgafourvand M, Yaghoubi S, Shahrisa E, Farshbaf-Khalili A (2016) Effects of fish oil supplementation on gestational diabetes mellitus (GDM): a systematic review. Iran Red Crescent Med J 18:e24690PubMedPubMedCentral Ostadrahimi A, Mohammad-Alizadeh S, Mirgafourvand M, Yaghoubi S, Shahrisa E, Farshbaf-Khalili A (2016) Effects of fish oil supplementation on gestational diabetes mellitus (GDM): a systematic review. Iran Red Crescent Med J 18:e24690PubMedPubMedCentral
32.
Zurück zum Zitat Sano T, Umeda F, Hashimoto T, Nawata H, Utsumi H (1998) Oxidative stress measurement by in vivo electron spin resonance spectroscopy in rats with streptozotocin-induced diabetes. Diabetologia 41(11):1355–1360CrossRef Sano T, Umeda F, Hashimoto T, Nawata H, Utsumi H (1998) Oxidative stress measurement by in vivo electron spin resonance spectroscopy in rats with streptozotocin-induced diabetes. Diabetologia 41(11):1355–1360CrossRef
33.
Zurück zum Zitat Haffner SM (2006) The metabolic syndrome: inflammation, diabetes mellitus, and cardiovascular disease. Am J Cardiol 2A:3–11CrossRef Haffner SM (2006) The metabolic syndrome: inflammation, diabetes mellitus, and cardiovascular disease. Am J Cardiol 2A:3–11CrossRef
34.
Zurück zum Zitat Khullar M, Al-Shudiefat AA, Ludke A, Binepal G, Singal PK (2010) Oxidative stress: a key contributor to diabetic cardiomyopathy. Can J Physiol Pharmacol 88(3):233–240CrossRef Khullar M, Al-Shudiefat AA, Ludke A, Binepal G, Singal PK (2010) Oxidative stress: a key contributor to diabetic cardiomyopathy. Can J Physiol Pharmacol 88(3):233–240CrossRef
35.
Zurück zum Zitat Dinh W, Füth R, Nickl W, Krahn T, Ellinghaus P, Scheffold T, Bansemir L, Bufe A, Barroso MC, Lankisch M (2009) Elevated plasma levels of TNF-alpha and interleukin-6 in patients with diastolic dysfunction and glucose metabolism disorders. Cardiovasc Diabetol 8:58CrossRef Dinh W, Füth R, Nickl W, Krahn T, Ellinghaus P, Scheffold T, Bansemir L, Bufe A, Barroso MC, Lankisch M (2009) Elevated plasma levels of TNF-alpha and interleukin-6 in patients with diastolic dysfunction and glucose metabolism disorders. Cardiovasc Diabetol 8:58CrossRef
36.
Zurück zum Zitat Li J, Liu D, Sun L, Lu Y, Zhang Z (2012) Advanced glycation end products and neurodegenerative diseases: mechanisms and perspective. J Neurol Sci 317(1–2):1–5CrossRef Li J, Liu D, Sun L, Lu Y, Zhang Z (2012) Advanced glycation end products and neurodegenerative diseases: mechanisms and perspective. J Neurol Sci 317(1–2):1–5CrossRef
37.
Zurück zum Zitat Santos JC, Valentim IB, de Araújo OR, Ataide Tda R, Goulart MO (2013) Development of nonalcoholic hepatopathy: contributions of oxidative stress and advanced glycation end products. Int J Mol Sci 14(10):19846–19866CrossRef Santos JC, Valentim IB, de Araújo OR, Ataide Tda R, Goulart MO (2013) Development of nonalcoholic hepatopathy: contributions of oxidative stress and advanced glycation end products. Int J Mol Sci 14(10):19846–19866CrossRef
38.
Zurück zum Zitat Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21(2):195–214CrossRef Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21(2):195–214CrossRef
39.
Zurück zum Zitat Ko SY, Chang SS, Lin IH, Chen HI (2015) Suppression of antioxidant Nrf-2 and downstream pathway in H9c2 cells by advanced glycation end products (AGEs) via ERK phosphorylation. Biochimie 118:8–14CrossRef Ko SY, Chang SS, Lin IH, Chen HI (2015) Suppression of antioxidant Nrf-2 and downstream pathway in H9c2 cells by advanced glycation end products (AGEs) via ERK phosphorylation. Biochimie 118:8–14CrossRef
40.
Zurück zum Zitat Faria A, Persaud SJ (2017) Cardiac oxidative stress in diabetes: mechanisms and therapeutic potential. Pharmacol Ther 172:50–62CrossRef Faria A, Persaud SJ (2017) Cardiac oxidative stress in diabetes: mechanisms and therapeutic potential. Pharmacol Ther 172:50–62CrossRef
41.
Zurück zum Zitat Rom O, Reznick AZ (2015) The role of E3 ubiquitin-ligases MuRF-1 and MAFbx in loss of skeletal muscle mass. Free Radic Biol Med 98:218–230CrossRef Rom O, Reznick AZ (2015) The role of E3 ubiquitin-ligases MuRF-1 and MAFbx in loss of skeletal muscle mass. Free Radic Biol Med 98:218–230CrossRef
42.
Zurück zum Zitat Palomer X, Salvadó L, Barroso E, Vázquez-Carrera M (2013) An overview of the crosstalk between inflammatory processes and metabolic dysregulation during diabetic cardiomyopathy. Int J Cardiol 168(4):3160–3172CrossRef Palomer X, Salvadó L, Barroso E, Vázquez-Carrera M (2013) An overview of the crosstalk between inflammatory processes and metabolic dysregulation during diabetic cardiomyopathy. Int J Cardiol 168(4):3160–3172CrossRef
43.
Zurück zum Zitat Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, Li P, Lu WJ, Watkins SM, Olefsky JM (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin sensitizing effects. Cell 142(5):687–698CrossRef Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, Fan W, Li P, Lu WJ, Watkins SM, Olefsky JM (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin sensitizing effects. Cell 142(5):687–698CrossRef
44.
Zurück zum Zitat Miyamoto J, Hasegawa S, Kasubuchi M, Ichimura A, Nakajima A, Kimura I (2016) Nutritional signaling via free fatty acid receptors. Int J Mol Sci 17(4):450CrossRef Miyamoto J, Hasegawa S, Kasubuchi M, Ichimura A, Nakajima A, Kimura I (2016) Nutritional signaling via free fatty acid receptors. Int J Mol Sci 17(4):450CrossRef
45.
Zurück zum Zitat Serhan CN (2005) Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 73:141–162CrossRef Serhan CN (2005) Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 73:141–162CrossRef
46.
Zurück zum Zitat Shen J, Bi YL, Das UN (2014) Potential role of polyunsaturated fatty acids in diabetic retinopathy. Arch Med Sci 10:1167–1174CrossRef Shen J, Bi YL, Das UN (2014) Potential role of polyunsaturated fatty acids in diabetic retinopathy. Arch Med Sci 10:1167–1174CrossRef
Metadaten
Titel
Intrauterine hyperglycemia-induced inflammatory signalling via the receptor for advanced glycation end products in the cardiac muscle of the infants of diabetic mother rats
verfasst von
Ritsuko Kawaharada
Haruna Masuda
Zhenyi Chen
Eric Blough
Tomoko Kohama
Akio Nakamura
Publikationsdatum
23.09.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nutrition / Ausgabe 8/2018
Print ISSN: 1436-6207
Elektronische ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-017-1536-6

Weitere Artikel der Ausgabe 8/2018

European Journal of Nutrition 8/2018 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.