Exp Clin Endocrinol Diabetes 2019; 127(09): 590-597
DOI: 10.1055/s-0043-109696
Article
© Georg Thieme Verlag KG Stuttgart · New York

High Glucose Level Induces Cardiovascular Dysplasia During Early Embryo Development

Yi-mei Jin
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
,
Shu-zhu Zhao
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
,
Zhao-long Zhang
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
,
Yao Chen
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
,
Xin Cheng
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
,
Manli Chuai
2   Division of Cell and Developmental Biology, University of Dundee, Dundee DD1 5EH, UK
,
Guo-sheng Liu
3   Department of Neonates, Institute of Fetal-Preterm Labor Medicine, The first Affiliated Hospital of Jinan University, Guangzhou 510632, China
,
Kenneth Ka Ho Lee
4   Stem Cell and Regeneration Thematic Research Programme, School of Biomedical Sciences, Chinese University of Hong Kong, Shatin, Hong Kong
,
Xuesong Yang
1   Division of Histology and Embryology, Key Laboratory for Regenerative Medicine of the Ministry of Education, Medical College, Jinan University, Guangzhou 510632, China
› Author Affiliations
Further Information

Publication History

received 12 January 2013
first decision 02 May 2013

accepted 04 June 2013

Publication Date:
26 September 2017 (online)

Abstract

The incidence of gestational diabetes mellitus (GDM) has increased dramatically amongst multiethnic population. However, how gestational diabetes mellitus damages the developing embryo is still unknown. In this study, we used yolk sac membrane (YSM) model to investigate angiogenesis in the developing chick embryo. We determined that in the presence of high glucose, it retarded the growth and extension of the embryonic vascular plexus and it also reduced the density of the vasculature in yolk sac membrane model. Using the same strategy, we used the chorioallantoic membrane (CAM) as a model to investigate the influence of high glucose on the vasculature. We established that high glucose inhibited development of the blood vessel plexus and the blood vessels formed had a narrower diameter than control vessels. Concurrent with the abnormal angiogenesis, we also examined how it impacted cardiogenesis. We determined the myocardium in the right ventricle and left atrium were significantly thicker than the control and also there was a reduction in glycogen content in cardiomyocytes. The high glucose also induced excess reactive oxygen species (ROS) production in the cardiomyocytes. We postulated that it was the excess reactive oxygen species that damaged the cardiomyocytes resulting in cardiac hyperplasia.

 
  • References

  • 1 Nagel W. A summary of recommendations. Top Health Care Financ 1988; 15: 75-80
  • 2 Dabelea D, Snell-Bergeon JK, Hartsfield CL. et al. Increasing prevalence of gestational diabetes mellitus (GDM) over time and by birth cohort: Kaiser Permanente of Colorado GDM Screening Program. Diabetes Care 2005; 28: 579-584
  • 3 Jovanovic L, Pettitt DJ. Gestational diabetes mellitus. JAMA 2001; 286: 2516-2518
  • 4 Buchanan TA, Metzger BE, Freinkel N. et al. Insulin sensitivity and B-cell responsiveness to glucose during late pregnancy in lean and moderately obese women with normal glucose tolerance or mild gestational diabetes. Am J Obstet Gynecol 1990; 162: 1008-1014
  • 5 Catalano PM, Tyzbir ED, Wolfe RR. et al. Carbohydrate metabolism during pregnancy in control subjects and women with gestational diabetes. Am J Physiol 1993; 264: E60-E67
  • 6 Homko C, Sivan E, Chen X. et al. Insulin secretion during and after pregnancy in patients with gestational diabetes mellitus. J Clin Endocrinol Metab 2001; 86: 568-573
  • 7 Pettitt DJ, Baird HR, Aleck KA. et al. Excessive obesity in offspring of Pima Indian women with diabetes during pregnancy. N Engl J Med 1983; 308: 242-245
  • 8 Pettitt DJ, Aleck KA, Baird HR. et al. Congenital susceptibility to NIDDM. Role of intrauterine environment. Diabetes 1988; 37: 622-628
  • 9 Boney CM, Verma A, Tucker R. et al. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics 2005; 115: e290-e296
  • 10 Cho NH, Silverman BL, Rizzo TA. et al. Correlations between the intrauterine metabolic environment and blood pressure in adolescent offspring of diabetic mothers. J Pediatr 2000; 136: 587-592
  • 11 Silverman BL, Metzger BE, Cho NH. et al. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care 1995; 18: 611-617
  • 12 Krishnaveni GV, Hill JC, Leary SD. et al. Anthropometry, glucose tolerance, and insulin concentrations in Indian children: Relationships to maternal glucose and insulin concentrations during pregnancy. Diabetes Care 2005; 28: 2919-2925
  • 13 Jordan WR. The pregnant diabetic. South Med J 1967; 60: 1213-1217
  • 14 Freinkel N. Banting Lecture 1980. Of pregnancy and progeny. Diabetes 1980; 29: 1023-1035
  • 15 Costa EV, Jimenez GC, Barbosa CT et al. Fractal analysis of extraembryonic vascularization in Japanese quail embryos exposed to extremely low frequency magnetic fields. Bioelectromagnetics 2012
  • 16 Lokman NA, Elder AS, Ricciardelli C. et al. Chick chorioallantoic membrane (cam) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci 2012; 13: 9959-9970
  • 17 Valko M, Leibfritz D, Moncol J. et al. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84
  • 18 Covarrubias L, Hernandez-Garcia D, Schnabel D. et al. Function of reactive oxygen species during animal development: Passive or active?. Dev Biol 2008; 320: 1-11
  • 19 Wan J, Winn LM. In utero-initiated cancer: The role of reactive oxygen species. Birth Defects Res C Embryo Today 2006; 78: 326-332
  • 20 Dennery PA. Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 2007; 81: 155-162
  • 21 Hamburger V, Hamilton HL. A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 1992; 195: 231-272
  • 22 Abaci A, Oguzhan A, Kahraman S. et al. Effect of diabetes mellitus on formation of coronary collateral vessels. Circulation 1999; 99: 2239-2242
  • 23 Ning H, Qiu X, Baine L. et al. Effects of high glucose on human cavernous endothelial cells. Urology 2012; 80: 1162 e1167-1162 e1111
  • 24 Venkatesan B, Valente AJ, Das NA. et al. CIKS (Act1 or TRAF3IP2) mediates high glucose-induced endothelial dysfunction. Cell Signal 2013; 25: 359-371
  • 25 Liu J, Mak TC, Banigesh A. et al. Aldolase B knockdown prevents high glucose-induced methylglyoxal overproduction and cellular dysfunction in endothelial cells. PLoS One 7: e41495
  • 26 Sheng G. Primitive and definitive erythropoiesis in the yolk sac: A bird's eye view. Int J Dev Biol 54: 1033-1043
  • 27 Deryugina EI, Quigley JP. Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis. Histochem Cell Biol 2008; 130: 1119-1130
  • 28 Ribatti D. The chick embryo chorioallantoic membrane in the study of tumor angiogenesis. Rom J Morphol Embryol 2008; 49: 131-135
  • 29 Li SY, Sigmon VK, Babcock SA. et al. Advanced glycation endproduct induces ROS accumulation, apoptosis, MAP kinase activation and nuclear O-GlcNAcylation in human cardiac myocytes. Life Sci 2007; 80: 1051-1056
  • 30 Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes 2005; 54: 1615-1625
  • 31 Wei J, Liu M, Liu H et al. Oleanolic acid arrests cell cycle and induces apoptosis via ROS-mediated mitochondrial depolarization and lysosomal membrane permeabilization in human pancreatic cancer cells. J Appl Toxicol 2012