Neural tube defects, folate, and immune modulation

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 97, Issue 9, 2013, Pages 602-609

  Denny, Kerina J ^a,b   Jeanes, Angela ^a   Fathe, Kristin ^c   Finnell, Richard H ^c   Taylor, Stephen M ^a   Woodruff, Trent M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

C5a; Complement; Folate; Neural tube defects; Neurulation

Indexed keywords

5 METHYLTETRAHYDROFOLIC ACID; FOLATE RECEPTOR; FOLATE TRANSPORTER; FOLIC ACID; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; REDUCED FOLATE CARRIER; VALPROIC ACID;

ANENCEPHALUS; ARTICLE; DRUG INDUCED DISEASE; DRUG MEGADOSE; ENCEPHALOCELE; FOLATE METABOLISM; FOLIC ACID DEFICIENCY; HUMAN; IMMUNE DYSREGULATION; IMMUNOMODULATION; INIENCEPHALY; NEURAL TUBE DEFECT; NEUROECTODERM; NEURULATION; NONHUMAN; PERINATAL MORBIDITY; PRIORITY JOURNAL; SPINAL DYSRAPHISM; VITAMIN SUPPLEMENTATION;

C5A; COMPLEMENT; FOLATE; NEURAL TUBE DEFECTS; NEURULATION;

ANTICONVULSANTS; AUTOANTIBODIES; CHEMOKINE CCL2; COMPLEMENT SYSTEM PROTEINS; FEMALE; FOLATE RECEPTORS, GPI-ANCHORED; HUMANS; IMMUNOLOGIC FACTORS; NEURAL TUBE DEFECTS; NEURULATION; PREGNANCY; PREGNANCY IN DIABETICS; RISK FACTORS; TETRAHYDROFOLATES; VALPROIC ACID;

EID: 84884717069     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.23177     Document Type: Article

References (101)

1. Attilakos A, Papakonstantinou E, Schulpis K, et al. 2006. Early effect of sodium valproate and carbamazepine monotherapy on homocysteine metabolism in children with epilepsy. Epilepsy Res 71:229-232.
2. Beaudin AE, Stover PJ. 2009. Insights into metabolic mechanisms underlying folate-responsive neural tube defects: a minireview. Birth Defects Res A Clin Mol Teratol 85:274-284.
3. Benard M, Raoult E, Vaudry D, et al. 2008. Role of complement anaphylatoxin receptors (C3aR, C5aR) in the development of the rat cerebellum. Mol Immunol 45:3767-3774.
4. Blom HJ, Shaw GM, den Heijer M, Finnell RH. 2006. Neural tube defects and folate: case far from closed. Nat Rev Neurosci 7:724-731.
5. Botto LD, Moore CA, Khoury MJ, Erickson JD. 1999. Neural-tube defects. N Engl J Med 341:1509-1519.
6. Boulet SL, Yang Q, Mai C, et al. 2008. Trends in the postfortification prevalence of spina bifida and anencephaly in the United States. Birth Defects Res A Clin Mol Teratol 82:527-532.
7. Boyles AL, Ballard JL, Gorman EB, et al. 2011. Association between inhibited binding of folic acid to folate receptor alpha in maternal serum and folate-related birth defects in Norway. Hum Reprod 26:2232-2238.
8. Brown KS, Huang Y, Lu ZY, et al. 2006. Mild folate deficiency induces a proatherosclerotic phenotype in endothelial cells. Atherosclerosis 189:133-141.
9. Cabrera RM, Shaw GM, Ballard JL, et al. 2008. Autoantibodies to folate receptor during pregnancy and neural tube defect risk. J Reprod Immunol 79:85-92.
10. Campbell LR, Dayton DH, Sohal GS. 1986. Neural tube defects: a review of human and animal studies on the etiology of neural tube defects. Teratology 34:171-187.
11. Carmona-Fontaine C, Theveneau E, Tzekou A, et al. 2011. Complement fragment C3a controls mutual cell attraction during collective cell migration. Dev Cell 21:1026-1037.
12. Christensen B, Arbour L, Tran P, et al. 1999. Genetic polymorphisms in methylenetetrahydrofolate reductase and methionine synthase, folate levels in red blood cells, and risk of neural tube defects. Am J Med Genet 84:151-157.
13. Copp AJ, Greene ND. 2000. Neural tube defects: prevention by folic acid and other vitamins. Indian J Pediatr 67:915-921.
14. Copp AJ, Greene ND. 2010. Genetics and development of neural tube defects. J Pathol 220:217-230.
15. Copp AJ, Greene ND, Murdoch JN. 2003. The genetic basis of mammalian neurulation. Nat Rev Genet 4:784-793.
16. Coulthard LGJ, Costantini KJ, Lor M, Simmons D, Taylor SM, Woodruff TM. 2010. Complement expression in mice throughout neural tube closure. Mol Immunol 47:238.
17. Craig J, Morrison P, Morrow J, Patterson V. 1999. Failure of periconceptual folic acid to prevent a neural tube defect in the offspring of a mother taking sodium valproate. Seizure 8:253-254.
18. da Costa M, Sequeira JM, Rothenberg SP, Weedon J. 2003. Antibodies to folate receptors impair embryogenesis and fetal development in the rat. Birth Defects Res A Clin Mol Teratol 67:837-847.
19. De-Regil LM, Fernandez-Gaxiola AC, Dowswell T, Pena-Rosas JP. 2010. Effects and safety of periconceptional folate supplementation for preventing birth defects. Cochrane Database Syst Rev 10:CD007950.
20. Deak KL, Siegel DG, George TM, et al. 2008. Further evidence for a maternal genetic effect and a sex-influenced effect contributing to risk for human neural tube defects. Birth Defects Res A Clin Mol Teratol 82:662-669.
21. Denny KJ, Coulthard LG, Jeanes A, et al. 2013. C5a receptor signaling prevents folate deficiency-induced neural tube defects in mice. J Immunol 190:3493-3499.
22. Dheen ST, Tay SS, Boran J, et al. 2009. Recent studies on neural tube defects in embryos of diabetic pregnancy: an overview. Curr Med Chem 16:2345-2354.
23. Duthie SJ, Horgan G, de Roos B, et al. 2010. Blood folate status and expression of proteins involved in immune function, inflammation, and coagulation: biochemical and proteomic changes in the plasma of humans in response to long-term synthetic folic acid supplementation. J Proteome Res 9:1941-1950.
24. Finnell RH, Gelineau-van Waes J, Bennett GD, et al. 2000. Genetic basis of susceptibility to environmentally induced neural tube defects. Ann N Y Acad Sci 919:261-277.
25. Gendron RL, Nestel FP, Lapp WS, Baines MG. 1991. Expression of tumor necrosis factor alpha in the developing nervous system. Int J Neurosci 60:129-136.
26. Giles C. 1966. An account of 335 cases of megaloblastic anaemia of pregnancy and the puerperium. J Clin Pathol 19:1-11.
27. Girardi G. 2008. Guilty as charged: all available evidence implicates complement's role in fetal demise. Am J Reprod Immunol 59:183-192.
28. Greene ND, Copp AJ. 2009a. Development of the vertebrate central nervous system: formation of the neural tube. Prenat Diagn 29:303-311.
29. Greene ND, Stanier P, Copp AJ. 2009b. Genetics of human neural tube defects. Hum Mol Genet 18:R113-R129.
30. Hamilton JA, Anderson GP. 2004. GM-CSF biology. Growth Factors 22:225-231.
31. Hammons AL, Summers CM, Woodside JV, et al. 2009. Folate/homocysteine phenotypes and MTHFR 677C>T genotypes are associated with serum levels of monocyte chemoattractant protein-1. Clin Immunol 133:132-137.
32. Harden CL, Hopp J, Ting TY, et al. 2009a. Management issues for women with epilepsy-Focus on pregnancy (an evidence-based review): I. Obstetrical complications and change in seizure frequency: report of the Quality Standards Subcommittee and Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and the American Epilepsy Society. Epilepsia 50:1229-1236.
33. Harden CL, Hopp J, Ting TY, et al. 2009b. Practice parameter update: management issues for women with epilepsy--focus on pregnancy (an evidence-based review): obstetrical complications and change in seizure frequency: report of the Quality Standards Subcommittee and Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology and American Epilepsy Society. Neurology 73:126-132.
34. Hernandez-Diaz S, Werler MM, Walker AM, Mitchell AA. 2000. Folic acid antagonists during pregnancy and the risk of birth defects. N Engl J Med 343:1608-1614.
35. Hrubec TC, Toops KA, Holladay SD. 2009. Modulation of diabetes-induced palate defects by maternal immune stimulation. Anat Rec (Hoboken) 292:271-276.
36. Hrubec TC, Yan M, Ye K, et al. 2006. Valproic acid-induced fetal malformations are reduced by maternal immune stimulation with granulocyte-macrophage colony-stimulating factor or interferon-gamma. Anat Rec A Discov Mol Cell Evol Biol 288:1303-1309.
37. Ichiyama T, Okada K, Lipton JM, et al. 2000. Sodium valproate inhibits production of TNF-alpha and IL-6 and activation of NF-kappaB. Brain Res 857:246-251.
38. Jakubowski H. 2005. Anti-N-homocysteinylated protein autoantibodies and cardiovascular disease. Clin Chem Lab Med 43:1011-1014.
39. Jakubowski H, Glowacki R. 2011. Chemical biology of homocysteine thiolactone and related metabolites. Adv Clin Chem 55:81-103.
40. Jensen LE, Etheredge AJ, Brown KS, et al. 2006. Maternal genotype for the monocyte chemoattractant protein 1 A(-2518)G promoter polymorphism is associated with the risk of spina bifida in offspring. Am J Med Genet A 140:1114-1118.
41. Jentink J, Bakker MK, Nijenhuis CM, et al. 2010. Does folic acid use decrease the risk for spina bifida after in utero exposure to valproic acid? Pharmacoepidemiol Drug Saf 19:803-807.
42. Kaaja E, Kaaja R, Hiilesmaa V. 2003. Major malformations in offspring of women with epilepsy. Neurology 60:575-579.
43. Kalter H. 2000. Folic acid and human malformations: a summary and evaluation. Reprod Toxicol 14:463-476.
44. Kieffer EC, Martin JA, Herman WH. 1999. Impact of maternal nativity on the prevalence of diabetes during pregnancy among U.S. ethnic groups. Diabetes Care 22:729-735.
45. Koren G, Kennedy D. 1999. Safe use of valproic acid during pregnancy. Can Fam Physician 45:1451-1453.
46. Krupp DR, Xu PT, Thomas S, et al. 2012. Transcriptome profiling of genes involved in neural tube closure during human embryonic development using long serial analysis of gene expression (long-SAGE). Birth Defects Res A Clin Mol Teratol 94:683-692.
47. Lake BB, Ford R, Kao KR. 2001. Xrel3 is required for head development in Xenopus laevis. Development 128:263-273.
48. Lathia JD, Okun E, Tang SC, et al. 2008. Toll-like receptor 3 is a negative regulator of embryonic neural progenitor cell proliferation. J Neurosci 28:13978-13984.
49. Li M, Chen J, Li YS, et al. 2007. Folic acid reduces chemokine MCP-1 release and expression in rats with hyperhomocystinemia. Cardiovasc Pathol 16:305-309.
50. Li Q, Estepa G, Memet S, et al. 2000. Complete lack of NF-kappaB activity in IKK1 and IKK2 double-deficient mice: additional defect in neurulation. Genes Dev 14:1729-1733.
51. Li R, Coulthard LG, Wu MC, Taylor SM. 2013. C5L2: a controversial receptor of complement anaphylatoxin, C5a. FASEB J 27:855-864.
52. Lieberam I, Agalliu D, Nagasawa T, et al. 2005. A Cxcl12-CXCR4 chemokine signaling pathway defines the initial trajectory of mammalian motor axons. Neuron 47:667-679.
53. Lomaga MA, Henderson JT, Elia AJ, et al. 2000. Tumor necrosis factor receptor-associated factor 6 (TRAF6) deficiency results in exencephaly and is required for apoptosis within the developing CNS. J Neurosci 20:7384-7393.
54. Lu ZY, Jensen LE, Huang Y, et al. 2009. The up-regulation of monocyte chemoattractant protein-1 (MCP-1) in Ea.hy 926 endothelial cells under long-term low folate stress is mediated by the p38 MAPK pathway. Atherosclerosis 205:48-54.
55. Makki N, Capecchi MR. 2011. Identification of novel Hoxa1 downstream targets regulating hindbrain, neural crest and inner ear development. Dev Biol 357:295-304.
56. McGrath KE, Koniski AD, Maltby KM, McGann JK, Palis J. 1999. Embryonic expression and function of the chemokine SDF-1 and its receptor, CXCR4. Dev Biol 213:442-456.
57. McLeod L, Ray JG. 2002. Prevention and detection of diabetic embryopathy. Community Genet 5:33-39.
58. McLin VA, Hu CH, Shah R, Jamrich M. 2008. Expression of complement components coincides with early patterning and organogenesis in Xenopus laevis. Int J Dev Biol 52:1123-1133.
59. McNulty H, Pentieva K. 2004. Folate bioavailability. Proc Nutr Soc 63:529-536.
60. Meador KJ, Baker GA, Finnell RH, et al. 2006. In utero antiepileptic drug exposure: fetal death and malformations. Neurology 67:407-412.
61. Mlodzikowska-Albrecht J, Steinborn B, Zarowski M. 2007. Cytokines, epilepsy and epileptic drugs--is there a mutual influence? Pharmacol Rep 59:129-138.
62. Morrow JI, Hunt SJ, Russell AJ, et al. 2009. Folic acid use and major congenital malformations in offspring of women with epilepsy: a prospective study from the UK Epilepsy and Pregnancy Register. J Neurol Neurosurg Psychiatry 80:506-511.
63. Moum KR, Holzman GS, Harwell TS, et al. 2004. Increasing rate of diabetes in pregnancy among American Indian and white mothers in Montana and North Dakota, 1989-2000. Matern Child Health J 8:71-76.
64. Ozumba BC, Obi SN, Oli JM. 2004. Diabetes mellitus in pregnancy in an African population. Int J Gynaecol Obstet 84:114-119.
65. Phelan PE, Mellon MT, Kim CH. 2005. Functional characterization of full-length TLR3, IRAK-4, and TRAF6 in zebrafish (Danio rerio). Mol Immunol 42:1057-1071.
66. Piedrahita JA, Oetama B, Bennett GD, et al. 1999. Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat Genet 23:228-232.
67. Prothmann C, Armstrong NJ, Rupp RA. 2000. The Toll/IL-1 receptor binding protein MyD88 is required for Xenopus axis formation. Mech Dev 97:85-92.
68. Ray JG, O'Brien TE, Chan WS. 2001. Preconception care and the risk of congenital anomalies in the offspring of women with diabetes mellitus: a meta-analysis. QJM 94:435-444.
69. Regnier CH, Masson R, Kedinger V, et al. 2002. Impaired neural tube closure, axial skeleton malformations, and tracheal ring disruption in TRAF4-deficient mice. Proc Natl Acad Sci U S A 99:5585-5590.
70. Robert E, Guibaud P. 1982. Maternal valproic acid and congenital neural tube defects. Lancet 2:937.
71. Rolls A, Shechter R, London A, et al. 2007. Toll-like receptors modulate adult hippocampal neurogenesis. Nat Cell Biol 9:1081-1088.
72. Rosano A, Botto LD, Botting B, Mastroiacovo P. 2000. Infant mortality and congenital anomalies from 1950 to 1994: an international perspective. J Epidemiol Community Health 54:660-666.
73. Rothenberg SP, da Costa MP, Sequeira JM, et al. 2004. Autoantibodies against folate receptors in women with a pregnancy complicated by a neural-tube defect. N Engl J Med 350:134-142.
74. Roy M, Leclerc D, Wu Q, et al. 2008. Valproic acid increases expression of methylenetetrahydrofolate reductase (MTHFR) and induces lower teratogenicity in MTHFR deficiency. J Cell Biochem 105:467-476.
75. Ruland J, Duncan GS, Elia A, et al. 2001. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell 104:33-42.
76. Saitsu H, Ishibashi M, Nakano H, Shiota K. 2003. Spatial and temporal expression of folate-binding protein 1 (Fbp1) is closely associated with anterior neural tube closure in mice. Dev Dyn 226:112-117.
77. Schoenwolf GC, Franks MV. 1984. Quantitative analyses of changes in cell shapes during bending of the avian neural plate. Dev Biol 105:257-272.
78. Shaw GM, Quach T, Nelson V, et al. 2003. Neural tube defects associated with maternal periconceptional dietary intake of simple sugars and glycemic index. Am J Clin Nutr 78:972-978.
79. Shiah IS, Yatham LN, Yeh CB, Ravindran AV. 2005. Effect of valproate on plasma levels of interleukin-6 in healthy male humans. Int Clin Psychopharmacol 20:295-298.
80. Shim JH, Xiao C, Paschal AE, et al. 2005. TAK1, but not TAB1 or TAB2, plays an essential role in multiple signaling pathways in vivo. Genes Dev 19:2668-2681.
81. Smithells RW, Sheppard S, Schorah CJ. 1976. Vitamin dificiencies and neural tube defects. Arch Dis Child 51:944-950.
82. Spiegelstein O, Mitchell LE, Merriweather MY, et al. 2004. Embryonic development of folate binding protein-1 (Folbp1) knockout mice: effects of the chemical form, dose, and timing of maternal folate supplementation. Dev Dyn 231:221-231.
83. Tang LS, Finnell RH. 2003. Neural and orofacial defects in Folp1 knockout mice [corrected]. Birth Defects Res A Clin Mol Teratol 67:209-218.
84. Taparia S, Gelineau-van Waes J, Rosenquist TH, Finnell RH. 2007. Importance of folate-homocysteine homeostasis during early embryonic development. Clin Chem Lab Med 45:1717-1727.
85. Thomas S, Thomas M, Wincker P, et al. 2008. Human neural crest cells display molecular and phenotypic hallmarks of stem cells. Hum Mol Genet 17:3411-3425.
86. Tissir F, Wang CE, Goffinet AM. 2004. Expression of the chemokine receptor Cxcr4 mRNA during mouse brain development. Brain Res Dev Brain Res 149:63-71.
87. Torchinsky A, Toder V, Savion S, Shepshelovich J, Orenstein H, Fein A. 1997. Immunostimulation increases the resistance of mouse embryos to the teratogenic effect of diabetes mellitus. Diabetologia 40:635-640.
88. Undas A, Perla J, Lacinski M, Trzeciak W, et al. 2004. Autoantibodies against N-homocysteinylated proteins in humans: implications for atherosclerosis. Stroke 35:1299-1304.
89. Van Straaten HW, Janssen HC, Peeters MC, et al. 1996. Neural tube closure in the chick embryo is multiphasic. Dev Dyn 207:309-318.
90. Wallingford JB, Niswander LA, Shaw GM, Finnell RH. 2013. The continuing challenge of understanding, preventing, and treating neural tube defects. Science 339:1222002.
91. Warning JC, McCracken SA, Morris JM. 2011. A balancing act: mechanisms by which the fetus avoids rejection by the maternal immune system. Reproduction 141:715-724.
92. Woodruff TM, Ager RR, Tenner AJ, et al. 2010. The role of the complement system and the activation fragment C5a in the central nervous system. Neuromolecular Med 12:179-192.
93. Woodruff TM, Pollitt S, Proctor LM, et al. 2005. Increased potency of a novel complement factor 5a receptor antagonist in a rat model of inflammatory bowel disease. J Pharmacol Exp Ther 314:811-817.
94. Wride MA, Sanders EJ. 1993. Expression of tumor necrosis factor-alpha (TNF alpha)-cross-reactive proteins during early chick embryo development. Dev Dyn 198:225-239.
95. Wu MC, Brennan FH, Lynch JP, et al. 2013. The receptor for complement component C3a mediates protection from intestinal ischemia-reperfusion injuries by inhibiting neutrophil mobilization. Proc Natl Acad Sci U S A 110:9439-9444.
96. Xu C, Mao D, Holers VM, et al. 2000. A critical role for murine complement regulator crry in fetomaternal tolerance. Science 287:498-501.
97. Yadav A, Saini V, Arora S. 2010. MCP-1: chemoattractant with a role beyond immunity: a review. Clin Chim Acta 411:1570-1579.
98. Yates JR, Ferguson-Smith MA, Shenkin A, et al. 1987. Is disordered folate metabolism the basis for the genetic predisposition to neural tube defects? Clin Genet 31:279-287.
99. Yi Y, Lindemann M, Colligs A, Snowball C. 2011. Economic burden of neural tube defects and impact of prevention with folic acid: a literature review. Eur J Pediatr 170:1391-1400.
100. Young HA, Hardy KJ. 1995. Role of interferon-gamma in immune cell regulation. J Leukoc Biol 58:373-381.
101. Zou YR, Kottmann AH, Kuroda M, Taniuchi I, Littman DR. 1998. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development. Nature 393:595-599.