Maternal dietary choline deficiency alters angiogenesis in fetal mouse hippocampus

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

Volumn 107, Issue 29, 2010, Pages 12834-12839

  Mehedint, Mihai G ^a   Craciunescu, Corneliu N ^a   Zeisel, Steven H ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

ANGPT2; Brain; Diet; Endothelial cell; VEGFC

Indexed keywords

ANGIOPOIETIN 2; CHOLINE; CYTOSINE; GUANINE NUCLEOTIDE; MESSENGER RNA; PHOSPHATE; PHOSPHORYLCHOLINE; VASCULOTROPIN C; VON WILLEBRAND FACTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DIETARY INTAKE; DNA METHYLATION; ENDOTHELIUM CELL; FETUS; GENE EXPRESSION; HIPPOCAMPUS; MOUSE; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; VITAMIN DEFICIENCY;

ANGIOGENESIS INDUCING AGENTS; ANIMALS; BLOOD VESSELS; CELL COUNT; CELL PROLIFERATION; CELLS, CULTURED; CHOLINE DEFICIENCY; DIET; DNA METHYLATION; ENDOTHELIAL CELLS; FEMALE; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; LIVER; MATERNAL-FETAL RELATIONS; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PHYSIOLOGIC; NEURONS; PHOSPHORYLCHOLINE; PREGNANCY; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; TRANSCRIPTION INITIATION SITE;

MUS;

EID: 77955635459     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0914328107     Document Type: Article

References (77)

1. Institute of Medicine & National Academy of Sciences USA (1998) Dietary reference intakes for folate, thiamin, riboflavin, niacin, vitamin B12, panthothenic acid, biotin, and choline (National Academy Press, Washington D.C.), pp 390-422.
2. Zeisel SH (2006) Choline: critical role during fetal development and dietary requirements in adults. Annu Rev Nutr 26:229-250.
3. Jensen HH, Batres-Marquez SP, Carriquiry A, Schalinske KL (2007) Choline in the diets of the U.S. population: NHANES, 2003-2004. Faseb J 21:lb219.
4. Sweiry JH, Page KR, Dacke CG, Abramovich DR, Yudilevich DL (1986) Evidence of saturable uptake mechanisms at maternal and fetal sides of the perfused human placenta by rapid paired-tracer dilution: studies with calcium and choline. J Dev Physiol 8:435-445.
5. Zeisel SH, Wurtman RJ (1981) Developmental changes in rat blood choline concentration. Biochem J 198:565-570.
6. Ozarda Ilcol Y, Uncu G, Ulus IH (2002) Free and phospholipid-bound choline concentrations in serum during pregnancy, after delivery and in newborns. Arch Physiol Biochem 110:393-399. (Pubitemid 35454399)
7. Albright CD, et al. (2005) Regulation of choline deficiency apoptosis by epidermal growth factor in CWSV-1 rat hepatocytes. Cell Physiol Biochem 15:59-68.
8. Craciunescu CN, Albright CD, Mar MH, Song J, Zeisel SH (2003) Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J Nutr 133:3614-3618. (Pubitemid 37409496)
9. Niculescu MD, Craciunescu CN, Zeisel SH (2006) Dietary choline deficiency alters global and gene-specific DNA methylation in the developing hippocampus of mouse fetal brains. Faseb J 20:43-49.
10. Niculescu MD, Yamamuro Y, Zeisel SH (2004) Choline availability modulates human neuroblastoma cell proliferation and alters the methylation of the promoter region of the cyclin-dependent kinase inhibitor 3 gene. J Neurochem 89:1252-1259. (Pubitemid 38715843)
11. Albright CD, Tsai AY, Friedrich CB, Mar MH, Zeisel SH (1999) Choline availability alters embryonic development of the hippocampus and septum in the rat. Brain Research 113:13-20.
12. Albright CD, Friedrich CB, Brown EC, Mar MH, Zeisel SH (1999) Maternal dietary choline availability alters mitosis, apoptosis and the localization of TOAD-64 protein in the developing fetal rat septum. Brain Research 115:123-129.
13. Albright CD, Mar MH, Craciunescu CN, Song J, Zeisel SH (2005) Maternal dietary choline availability alters the balance of netrin-1 and DCC neuronal migration proteins in fetal mouse brain hippocampus. Brain Research 159:149-154.
14. Albright CD, Mar MH, Friedrich CB, Brown EC, Zeisel SH (2001) Maternal choline availability alters the localization of p15Ink4B and p27Kip1 cyclin-dependent kinase inhibitors in the developing fetal rat brain hippocampus. Dev Neurosci 23:100-106.
15. Albright CD, et al. (2003) Choline availability during embryonic development alters the localization of calretinin in developing and aging mouse hippocampus. Nutr Neurosci 6:129-134. (Pubitemid 36417045)
16. Jones JP, MeckW, Williams CL, Wilson WA, Swartzwelder HS (1999) Choline availability to the developing rat fetus alters adult hippocampal long-term potentiation. Brain Research 118:159-167.
17. Cheng RK, MacDonald CJ, Williams CL, Meck WH (2008) Prenatal choline supplementation alters the timing, emotion, and memory performance (TEMP) of adult male and female rats as indexed by differential reinforcement of low-rate schedule behavior. Learning & memory, (Cold Spring Harbor, Cold Spring Harbor, N.Y), 15, pp 153-162.
18. MeckW, Williams C (1997) Perinatal choline supplementation increases the threshold for chunking in spatial memory. Neuroreport 8:3053-3059.
19. Meck WH, Smith RA, Williams CL (1988) Pre- and postnatal choline supplementation produces long-term facilitation of spatial memory. Dev Psychobiol 21:339-353.
20. Meck WH, Williams CL (1999) Choline supplementation during prenatal development reduces proactive interference in spatial memory. Brain Research 118:51-59.
21. Risau W (1997) Mechanisms of angiogenesis. Nature 386:671-674.
22. Greenberg DA, Jin K (2005) From angiogenesis to neuropathology. Nature 438:954-959.
23. Brockington A, Lewis C, Wharton S, Shaw PJ (2004) Vascular endothelial growth factor and the nervous system. Neuropathol Appl Neurobiol 30:427-446. (Pubitemid 39423031)
24. Eichmann A, Corbel C, Le Douarin NM (1998) Segregation of the embryonic vascular and hemopoietic systems. Biochem Cell Biol 76:939-946. (Pubitemid 29450562)
25. Giblin JP, Hewlett LJ, Hannah MJ (2008) Basal secretion of von Willebrand factor from human endothelial cells.. Blood 112:957-964.
26. Munoz-Chapuli R, et al. (1999) Differentiation of hemangioblasts from embryonic mesothelial cells? A model on the origin of the vertebrate cardiovascular system. Differentiation 64:133-141. (Pubitemid 29213879)
27. Kinder SJ, Loebel DA, Tam PP (2001) Allocation and early differentiation of cardiovascular progenitors in the mouse embryo. Trends Cardiovasc Med 11:177-184.
28. Coffin JD, Harrison J, Schwartz S, Heimark R (1991) Angioblast differentiation and morphogenesis of the vascular endothelium in the mouse embryo. Dev Biol 148:51-62. (Pubitemid 121004746)
29. Zhu Y, et al. (2006) Effects of angiopoietin-1 on vascular endothelial growth factor-induced angiogenesis in the mouse brain. Acta Neurochirurgica Supplement 96:438-443.
30. Zacharek A, et al. (2007) Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J Cereb Blood Flow Metab 27:1684-1691. (Pubitemid 47476100)
31. Patan S (2004) Vasculogenesis and angiogenesis. Cancer Treatments 117:3-32.
32. Coultas L, Chawengsaksophak K, Rossant J (2005) Endothelial cells and VEGF in vascular development. Nature 438:937-945. (Pubitemid 43093959)
33. Zhang H, Vutskits L, Pepper MS, Kiss JZ (2003) VEGF is a chemoattractant for FGF-2-stimulated neural progenitors. J Cell Biol 163:1375-1384. (Pubitemid 38032097)
34. Hirschi KK, Rohovsky SA, D'Amore PA (1997) Cell-cell interactions in vessel assembly: a model for the fundamentals of vascular remodelling. Transpl Immunol 5:177-178.
35. Pfaff D, Fiedler U, Augustin HG (2006) Emerging roles of the Angiopoietin-Tie and the ephrin-Eph systems as regulators of cell trafficking. J Leukocyte Biol 80:719-726. (Pubitemid 44835887)
36. Suri C, et al. (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87:1171-1180. (Pubitemid 27010101)
37. Niculescu MD, Craciunescu CN, Zeisel SH (2005) Gene expression profiling of choline-deprived neural precursor cells isolated from mouse brain. Brain Research 134:309-322.
38. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95:343-353. (Pubitemid 39100452)
39. Fuks F (2005) DNA methylation and histone modifications: teaming up to silence genes. Curr Opin Genet Dev 15:490-495.
40. Wang W, Wang YJ, Kelner DN (2003) Coagulation factor VIII: structure and stability. Int J Pharm 259:1-15. (Pubitemid 36638549)
41. Peng Y, Jahroudi N (2003) The NFY transcription factor inhibits von Willebrand factor promoter activation in non-endothelial cells through recruitment of histone deacetylases. J Biol Chem 278:8385-8394.
42. Brussaard HE, Leuven JA, Krans HM, Kluft C (2002) The effect of 17 beta-oestradiol on variables of coagulation and fibrinolysis in postmenopausal women with type 2 diabetes mellitus. Vascul Pharmacol 39:141-147.
43. Lentz SR, Sadler JE (1993) Homocysteine inhibits von Willebrand factor processing and secretion by preventing transport from the endoplasmic reticulum. Blood 81:683-689.
44. Shin OH, et al. (1997) Methyl-group donors cannot prevent apoptotic death of rat hepatocytes induced by choline-deficiency. J Cell Biochem 64:196-208.
45. Chang PY, et al. (2008) Homocysteine inhibits arterial endothelial cell growth through transcriptional downregulation of fibroblast growth factor-2 involving G protein and DNA methylation. Circ Res 102:933-941.
46. Lobov IB, Brooks PC, Lang RA (2002) Angiopoietin-2 displays VEGF-dependent modulation of capillary structure and endothelial cell survival in vivo. Proc Natl Acad Sci USA 99:11205-11210.
47. Gelinas DS, Bernatchez PN, Rollin S, Bazan NG, Sirois MG (2002) Immediate and delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K, PKC, and PLC pathways. Br J Pharmacol 137:1021-1030. (Pubitemid 35440742)
48. Kanazawa H (2007) VEGF, angiopoietin-1 and -2 in bronchial asthma: new molecular targets in airway angiogenesis and microvascular remodeling. Recent Patents in Inflammation, Allergy, and Drug Discovery 1:1-8.
49. Le Bras B, et al. (2006) VEGFC is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nature neurosci 9:340-348.
50. Mehedint MG, Niculescu MD, Craciunescu CN, Zeisel SH (2010) Choline deficiency alters global histone methylation and epigenetic marking at the Re1 site of the calbindin 1 gene. Faseb J 24:184-195.
51. Kurukuti S, et al. (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci USA 103:10684-10689. (Pubitemid 44078037)
52. Ballas N, Grunseich C, Lu DD, Speh JC, Mandel G (2005) REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis. Cell 121:645-657. (Pubitemid 40720016)
53. Nan X, et al. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389. (Pubitemid 28269714)
54. Song Y, et al. (2009) Sp-1 and c-Myc mediate lysophosphatidic acid-induced expression of vascular endothelial growth factor in ovarian cancer cells via a hypoxia-inducible factor-1-independent mechanism. Clin Cancer Res 15:492-501.
55. Yin Y, et al. (2009) JNK/AP-1 pathway is involved in tumor necrosis factor-alpha induced expression of vascular endothelial growth factor in MCF7 cells. Biomed Pharmacother 63:429-435.
56. Watari K, et al. (2008) Role of macrophages in inflammatory lymphangiogenesis: Enhanced production of vascular endothelial growth factor C and D through NF-kappaB activation. Biochem Biophys Res Commun 377:826-831.
57. Simon MP, Tournaire R, Pouyssegur J (2008) The angiopoietin-2 gene of endothelial cells is up-regulated in hypoxia by a HIF binding site located in its first intron and by the central factors GATA-2 and Ets-1. J Cell Physiol 217:809-818.
58. Luo M, et al. (2008) Inhibition of tumor angiogenesis by cell-permeable dominant negative SOX18 mutants. Med Hypotheses 70:880-882. (Pubitemid 351318070)
59. Wynder C, Hakimi MA, Epstein JA, Shilatifard A, Shiekhattar R (2005) Recruitment of MLL by HMG-domain protein iBRAF promotes neural differentiation. Cell Bio 7:1113-1117.
60. Grosschedl R, Giese K, Pagel J (1994) HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet 10:94-100. (Pubitemid 24075089)
61. Partch CL, Card PB, Amezcua CA, Gardner KH (2009) Molecular basis of coiled coil coactivator recruitment by the aryl hydrocarbon receptor nuclear translocator (ARNT). J Biol Chem 284:15184-15192.
62. Chintalgattu V, Harris GS, Akula SM, Katwa C (2007) PPAR-gamma agonists induce the expression of VEGF and its receptors in cultured cardiac myofibroblasts. Cardiovasc Res 74:140-150. (Pubitemid 46366953)
63. da Costa KA, et al. (2006) Common genetic polymorphisms affect the human requirement for the nutrient choline. Faseb J 20:1336-1344.
64. Fischer LM, et al. (2007) Sex and menopausal status influence human dietary requirements for the nutrient choline. Am J Clin Nutr 85:1275-1285.
65. Resseguie M, et al. (2007) Phosphatidylethanolamine N-methyltransferase (PEMT) gene expression is induced by estrogen in human and mouse primary hepatocytes. Faseb J 21:2622-2632.
66. McMahon KE, Farrell PM (1985) Measurement of free choline concentrations in maternal and neonatal blood by micropyrolysis gas chromatography. Clin Chim Acta 149:1-12.
67. Zeisel SH, Mar M-H, Zhou Z-W, da Costa K-A (1995) Pregnancy and lactation are associated with diminished concentrations of choline and its metabolites in rat liver. J Nutr 125:3049-3054.
68. Shaw GM, Carmichael SL, Yang W, Selvin S, Schaffer DM (2004) Periconceptional dietary intake of choline and betaine and neural tube defects in offspring. Am J Epidemiol 160:102-109. (Pubitemid 38962995)
69. Shaw GM, Carmichael SL, Laurent C, Rasmussen SA (2006) Maternal nutrient intakes and risk of orofacial clefts. Epidemiology 17:285-291. (Pubitemid 43755731)
70. Park JJ, Baum MJ, Paredes RG, Tobet SA (1996) Neurogenesis and cell migration into the sexually dimorphic preoptic area/anterior hypothalamus of the fetal ferret. J Neurobiol 30:315-328.
71. Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474-475.
72. Laitinen L (1987) Griffonia simplicifolia lectins bind specifically to endothelial cells and some epithelial cells in mouse tissues. Histochem J 19:225-234.
73. Furuta C, et al. (2006) Discordant developmental waves of angioblasts and hemangioblasts in the early gastrulating mouse embryo. Development 133:2771-2779. (Pubitemid 44177896)
74. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
75. Rauch T, Pfeifer GP (2005) Methylated-CpG island recovery assay: a new technique for the rapid detection of methylated-CpG islands in cancer. Lab Invest 85:1172-1180.
76. Pomfret EA, da Costa K, Zeisel SH (1990) Effects of choline deficiency and methotrexate treatment upon rat liver. J Nutr Biochem 1:533-541.
77. Koc H, Mar MH, Ranasinghe A, Swenberg JA, Zeisel SH (2002) Quantitation of choline and its metabolites in tissues and foods by liquid chromatography/electrospray ionization-isotope dilution mass spectrometry. Analytical Chemistry 74:4734-4740.