Hyperglycemia impairs left-right axis formation and thereby disturbs heart morphogenesis in mouse embryos

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 38, 2015, Pages E5300-E5307

  Hachisuga, Masahiro ^a   Oki, Shinya ^a   Kitajima, Keiko ^a   Ikuta, Satomi ^a   Sumi, Tomoyuki ^a   Kato, Kiyoko ^a   Wake, Norio ^a   Meno, Chikara ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Congenital heart defects; Diabetes; Heterotaxia; Left right axis

Indexed keywords

GLUCOSE; NOTCH RECEPTOR; PROTEIN NODAL; SMAD2 PROTEIN; STREPTOZOCIN; TRANSCRIPTION FACTOR PITX2; GLUCOSE BLOOD LEVEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONCENTRATION PROCESS; CONFERENCE PAPER; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO CULTURE; FEMALE; GENETIC ASSOCIATION; GLUCOSE BLOOD LEVEL; GLUCOSE INTAKE; HEART DEVELOPMENT; HEART FUNCTION; HETEROTAXY SYNDROME; HYPERGLYCEMIA; LEFT RIGHT AXIS FORMATION; MATERNAL DIABETES MELLITUS; MESODERM; MOLECULAR PATHOLOGY; MOUSE; MOUSE EMBRYO; NONHUMAN; ORGAN DISTRIBUTION; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; CYTOLOGY; DISEASE MODEL; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETICS; HEART; HEK293 CELL LINE; HUMAN; METABOLISM; MORPHOGENESIS; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SCANNING ELECTRON MICROSCOPY; TIME FACTOR;

ANIMALS; BLOOD GLUCOSE; BODY PATTERNING; DISEASE MODELS, ANIMAL; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; HEART; HEART DEFECTS, CONGENITAL; HEK293 CELLS; HUMANS; HYPERGLYCEMIA; MESODERM; MICE; MICROSCOPY, ELECTRON, SCANNING; MORPHOGENESIS; PHOSPHORYLATION; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 84942851446     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504529112     Document Type: Article

References (54)

1. Liu S, et al.; Canadian Perinatal Surveillance System (Public Health Agency of Canada) (2013) Association between maternal chronic conditions and congenital heart defects: A population-based cohort study. Circulation 128(6):583-589.
2. Dolk H, Loane M, Garne E; European Surveillance of Congenital Anomalies (EUROCAT) Working Group (2011) Congenital heart defects in Europe: Prevalence and perinatal mortality, 2000 to 2005. Circulation 123(8):841-849.
3. Jenkins KJ, et al.; American Heart Association Council on Cardiovascular Disease in the Young (2007) Noninherited risk factors and congenital cardiovascular defects: Current knowledge: A scientific statement from the American Heart Association Council on Cardiovascular Disease in the Young: Endorsed by the American Academy of Pediatrics. Circulation 115(23):2995-3014.
4. Correa A, et al. (2008) Diabetes mellitus and birth defects. Am J Obstet Gynecol 199(3):237.e1-237.e9.
5. Cockroft DL, Coppola PT (1977) Teratogenic effects of excess glucose on head-fold rat embryos in culture. Teratology 16(2):141-146.
6. Sadler TW (1980) Effects of maternal diabetes on early embryogenesis: II. Hyperglycemia-induced exencephaly. Teratology 21(3):349-356.
7. Horton WE, Jr, Sadler TW (1983) Effects of maternal diabetes on early embryogenesis. Alterations in morphogenesis produced by the ketone body, B-hydroxybutyrate. Diabetes 32(7):610-616.
8. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414(6865):813-820.
9. Zabihi S, Loeken MR (2010) Understanding diabetic teratogenesis: Where are we now and where are we going? Birth Defects Res A Clin Mol Teratol 88(10):779-790.
10. Phelan SA, Ito M, Loeken MR (1997) Neural tube defects in embryos of diabetic mice: Role of the Pax-3 gene and apoptosis. Diabetes 46(7):1189-1197.
11. Chang TI, et al. (2003) Oxidant regulation of gene expression and neural tube development: Insights gained from diabetic pregnancy on molecular causes of neural tube defects. Diabetologia 46(4):538-545.
12. Morgan SC, Relaix F, Sandell LL, Loeken MR (2008) Oxidative stress during diabetic pregnancy disrupts cardiac neural crest migration and causes outflow tract defects. Birth Defects Res A Clin Mol Teratol 82(6):453-463.
13. Pani L, Horal M, Loeken MR (2002) Rescue of neural tube defects in Pax-3-deficient embryos by p53 loss of function: Implications for Pax-3-dependent development and tumorigenesis. Genes Dev 16(6):676-680.
14. Morgan SC, et al. (2008) Cardiac outflow tract septation failure in Pax3-deficient embryos is due to p53-dependent regulation of migrating cardiac neural crest. Mech Dev 125(9-10):757-767.
15. Martínez-Frías ML (2001) Heterotaxia as an outcome of maternal diabetes: An epidemiological study. Am J Med Genet 99(2):142-146.
16. Lisowski LA, et al. (2010) Congenital heart disease in pregnancies complicated by maternal diabetes mellitus. An international clinical collaboration, literature review, and meta-analysis. Herz 35(1):19-26.
17. Morishima M, Yasui H, Ando M, Nakazawa M, Takao A (1996) Influence of genetic and maternal diabetes in the pathogenesis of visceroatrial heterotaxy in mice. Teratology 54(4):183-190.
18. Hamada H, Meno C, Watanabe D, Saijoh Y (2002) Establishment of vertebrate leftright asymmetry. Nat Rev Genet 3(2):103-113.
19. Lowe LA, Yamada S, Kuehn MR (2001) Genetic dissection of nodal function in patterning the mouse embryo. Development 128(10):1831-1843.
20. Yashiro K, Shiratori H, Hamada H (2007) Haemodynamics determined by a genetic programme govern asymmetric development of the aortic arch. Nature 450(7167):285-288.
21. Shiratori H, Yashiro K, Shen MM, Hamada H (2006) Conserved regulation and role of Pitx2 in situs-specific morphogenesis of visceral organs. Development 133(15):3015-3025.
22. Gage PJ, Suh H, Camper SA (1999) Dosage requirement of Pitx2 for development of multiple organs. Development 126(20):4643-4651.
23. Kitamura K, et al. (1999) Mouse Pitx2 deficiency leads to anomalies of the ventral body wall, heart, extra- and periocular mesoderm and right pulmonary isomerism. Development 126(24):5749-5758.
24. Yan YT, et al. (1999) Conserved requirement for EGF-CFC genes in vertebrate leftright axis formation. Genes Dev 13(19):2527-2537.
25. Lin CR, et al. (1999) Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401(6750):279-282.
26. Liu C, et al. (2002) Pitx2c patterns anterior myocardium and aortic arch vessels and is required for local cell movement into atrioventricular cushions. Development 129(21):5081-5091.
27. Yamamoto M, et al. (2003) Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development 130(9):1795-1804.
28. Collignon J, Varlet I, Robertson EJ (1996) Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381(6578):155-158.
29. Lowe LA, et al. (1996) Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381(6578):158-161.
30. Oki S, et al. (2007) Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 134(21):3893-3904.
31. Tanaka C, Sakuma R, Nakamura T, Hamada H, Saijoh Y (2007) Long-range action of Nodal requires interaction with GDF1. Genes Dev 21(24):3272-3282.
32. Marques S, et al. (2004) The activity of the Nodal antagonist Cerl-2 in the mouse node is required for correct L/R body axis. Genes Dev 18(19):2342-2347.
33. Kawasumi A, et al. (2011) Left-right asymmetry in the level of active Nodal protein produced in the node is translated into left-right asymmetry in the lateral plate of mouse embryos. Dev Biol 353(2):321-330.
34. Nakamura T, et al. (2006) Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. Dev Cell 11(4):495-504.
35. Oki S, et al. (2009) Reversal of left-right asymmetry induced by aberrant Nodal signaling in the node of mouse embryos. Development 136(23):3917-3925.
36. Saijoh Y, et al. (2000) Left-right asymmetric expression of lefty2 and nodal is induced by a signaling pathway that includes the transcription factor FAST2. Mol Cell 5(1):35-47.
37. Brennan J, Norris DP, Robertson EJ (2002) Nodal activity in the node governs left-right asymmetry. Genes Dev 16(18):2339-2344.
38. Norris DP, Brennan J, Bikoff EK, Robertson EJ (2002) The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129(14):3455-3468.
39. Shiratori H, et al. (2001) Two-step regulation of left-right asymmetric expression of Pitx2: Initiation by nodal signaling and maintenance by Nkx2. Mol Cell 7(1):137-149.
40. Furtado MB, Biben C, Shiratori H, Hamada H, Harvey RP (2011) Characterization of Pitx2c expression in the mouse heart using a reporter transgene. Dev Dyn 240(1):195-203.
41. Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF (1999) Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401(6750):276-278.
42. Meno C, et al. (1998) Lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94(3):287-297.
43. Meno C, et al. (2001) Diffusion of nodal signaling activity in the absence of the feedback inhibitor Lefty2. Dev Cell 1(1):127-138.
44. Ogawa K, et al. (2007) Activin-Nodal signaling is involved in propagation of mouse embryonic stem cells. J Cell Sci 120(Pt 1):55-65.
45. Alten L, et al. (2012) Differential regulation of node formation, nodal ciliogenesis and cilia positioning by Noto and Foxj1. Development 139(7):1276-1284.
46. Raya A, et al. (2003) Notch activity induces Nodal expression and mediates the establishment of left-right asymmetry in vertebrate embryos. Genes Dev 17(10):1213-1218.
47. Krebs LT, et al. (2003) Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev 17(10):1207-1212.
48. Kitajima K, Oki S, Ohkawa Y, Sumi T, Meno C (2013) Wnt signaling regulates left-right axis formation in the node of mouse embryos. Dev Biol 380(2):222-232.
49. Saga Y (2012) The mechanism of somite formation in mice. Curr Opin Genet Dev 22(4):331-338.
50. Splitt M, Wright C, Sen D, Goodship J (1999) Left-isomerism sequence and maternal type-1 diabetes. Lancet 354(9175):305-306.
51. Penton AL, Leonard LD, Spinner NB (2012) Notch signaling in human development and disease. Semin Cell Dev Biol 23(4):450-457.
52. Castori M (2013) Diabetic embryopathy: A developmental perspective from fertilization to adulthood. Mol Syndromol 4(1-2):74-86.
53. Ying QL, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453(7194):519-523.
54. Höfelmayr H, et al. (1999) Activated mouse Notch1 transactivates Epstein-Barr virus nuclear antigen 2-regulated viral promoters. J Virol 73(4):2770-2780.