How to form and close the brain: Insight into the mechanism of cranial neural tube closure in mammals

Cellular and Molecular Life Sciences

Volumn 70, Issue 17, 2013, Pages 3171-3186

  Yamaguchi, Yoshifumi ^a   Miura, Masayuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Brain development; Exencephaly; Live imaging; Neural tube closure; Tissue fusion

Indexed keywords

GROWTH FACTOR;

APOPTOSIS; AUTOPHAGY; BRAIN DEVELOPMENT; BRAIN REGION; CARBON METABOLISM; CELL DIFFERENTIATION; CELL DIVISION; CELL ELONGATION; CELL FUSION; CELL INTERACTION; CELL KINETICS; CELL POLARITY; EMBRYO DEVELOPMENT; EPIDERMIS; EPIGENETICS; GENETIC SUSCEPTIBILITY; HUMAN; MAMMAL; MATERNAL NUTRITION; MESENCHYME; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEURAL TUBE; NEUROECTODERM; NEURULATION; NONHUMAN; PROTEIN FUNCTION; REVIEW; TISSUE DISTRIBUTION;

ANENCEPHALY; ANIMALS; BRAIN; HUMANS; MUTATION; NEURAL TUBE; NEURAL TUBE DEFECTS;

MAMMALIA;

EID: 84882448130     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1227-7     Document Type: Review

References (179)

1. Mitchell L (2005) Epidemiology of neural tube defects. Am J Med Genet C Semin Med Genet 135C:88-94
2. Copp A, Greene N, Murdoch J (2003) The genetic basis of mammalian neurulation. Nat Rev Genet 4:784-793
3. Copp A, Greene N (2010) Genetics and development of neural tube defects. J Pathol 220:217-230
4. Juriloff D, Harris M (2000) Mouse models for neural tube closure defects. Hum Mol Genet 9:993-1000
5. Beaudin A, Stover P (2007) Folate-mediated one-carbon metabolism and neural tube defects: balancing genome synthesis and gene expression. Birth Defects Res C Embryo Today 81:183-203
6. Obican S, Finnell R, Mills J, Shaw G, Scialli A (2010) Folic acid in early pregnancy: a public health success story. FASEB J 24:4167-4174
7. Blom H, Shaw G, den Heijer M, Finnell R (2006) Neural tube defects and folate: case far from closed. Nat Rev Neurosci 7:724-731
8. Copp A (2005) Neurulation in the cranial region-normal and abnormal. J Anat 207:623-635
9. Harris M, Juriloff D (2010) An update to the list of mouse mutants with neural tube closure defects and advances toward a complete genetic perspective of neural tube closure. Birth Defects Res A Clin Mol Teratol 88:653-669
10. Copp A, Brook F, Estibeiro J, Shum A, Cockroft D (1990) The embryonic development of mammalian neural tube defects. Prog Neurobiol 35:363-403
11. Morriss-Kay G (1981) Growth and development of pattern in the cranial neural epithelium of rat embryos during neurulation. J Embryol Exp Morphol 65(Suppl):225-241
12. Geelen J, Langman J (1977) Closure of the neural tube in the cephalic region of the mouse embryo. Anat Rec 189:625-640
13. Sakai Y (1989) Neurulation in the mouse: manner and timing of neural tube closure. Anat Rec 223:194-203
14. Macdonald K, Juriloff D, Harris M (1989) Developmental study of neural tube closure in a mouse stock with a high incidence of exencephaly. Teratology 39:195-213
15. Juriloff D, Harris M, Tom C, MacDonald K (1991) Normal mouse strains differ in the site of initiation of closure of the cranial neural tube. Teratology 44:225-233
16. Golden J, Chernoff G (1993) Intermittent pattern of neural tube closure in two strains of mice. Teratology 47:73-80
17. Fleming A, Copp A (2000) A genetic risk factor for mouse neural tube defects: defining the embryonic basis. Hum Mol Genet 9:575-581
18. Van Straaten H, Janssen H, Peeters M, Copp A, Hekking J (1996) Neural tube closure in the chick embryo is multiphasic. Dev Dyn 207:309-318
19. Morriss G, New D (1979) Effect of oxygen concentration on morphogenesis of cranial neural folds and neural crest in cultured rat embryos. J Embryol Exp Morphol 54:17-35
20. Waterman R (1976) Topographical changes along the neural fold associated with neurulation in the hamster and mouse. Am J Anat 146:151-171
21. Matsumoto A, Hatta T, Moriyama K, Otani H (2002) Sequential observations of exencephaly and subsequent morphological changes by mouse exo utero development system: analysis of the mechanism of transformation from exencephaly to anencephaly. Anat Embryol (Berl) 205:7-18
22. Wood L, Smith M (1984) Generation of anencephaly: 1. Aberrant neurulation and 2. Conversion of exencephaly to anencephaly. J Neuropathol Exp Neurol 43:620-633
23. Eom D, Amarnath S, Fogel J, Agarwala S (2011) Bone morphogenetic proteins regulate neural tube closure by interacting with the apicobasal polarity pathway. Development 138:3179-3188
24. Margolis B, Borg J (2005) Apicobasal polarity complexes. J Cell Sci 118:5157-5159
25. McMahon J, Takada S, Zimmerman L, Fan C, Harland R, McMahon A (1998) Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev 12:1438-1452
26. Stottmann R, Berrong M, Matta K, Choi M, Klingensmith J (2006) The BMP antagonist Noggin promotes cranial and spinal neurulation by distinct mechanisms. Dev Biol 295:647-663
27. Ybot-Gonzalez P, Gaston-Massuet C, Girdler G, Klingensmith J, Arkell R, Greene N, Copp A (2007) Neural plate morphogenesis during mouse neurulation is regulated by antagonism of Bmp signalling. Development 134:3203-3211
28. Ybot-Gonzalez P, Cogram P, Gerrelli D, Copp A (2002) Sonic Hedgehog and the molecular regulation of mouse neural tube closure. Development 129:2507-2517
29. Dessaud E, McMahon A, Briscoe J (2008) Pattern formation in the vertebrate neural tube: a Sonic Hedgehog morphogen-regulated transcriptional network. Development 135:2489-2503
30. Ulloa F, Martí E (2010) Wnt won the war: antagonistic role of Wnt over Shh controls dorso-ventral patterning of the vertebrate neural tube. Dev Dyn 239:69-76
31. Jeong J, McMahon A (2005) Growth and pattern of the mammalian neural tube are governed by partially overlapping feedback activities of the hedgehog antagonists patched 1 and Hhip1. Development 132:143-154
32. Ribes V, Briscoe J (2009) Establishing and interpreting graded Sonic Hedgehog signaling during vertebrate neural tube patterning: the role of negative feedback. Cold Spring Harb Perspect Biol 1:a002014
33. Pinson K, Brennan J, Monkley S, Avery B, Skarnes W (2000) An LDL-receptor-related protein mediates Wnt signalling in mice. Nature 407:535-538
34. Kokubu C, Heinzmann U, Kokubu T, Sakai N, Kubota T, Kawai M, Wahl M, Galceran J, Grosschedl R, Ozono K, Imai K (2004) Skeletal defects in ringelschwanz mutant mice reveal that Lrp6 is required for proper somitogenesis and osteogenesis. Development 131:5469-5480
35. Backman M, Machon O, Mygland L, van den Bout C, Zhong W, Taketo M, Krauss S (2005) Effects of canonical Wnt signaling on dorso-ventral specification of the mouse telencephalon. Dev Biol 279:155-168
36. Kim S, Shindo A, Park T, Oh E, Ghosh S, Gray R, Lewis R, Johnson C, Attie-Bittach T, Katsanis N, Wallingford J (2010) Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329:1337-1340
37. Mansouri A, Pla P, Larue L, Gruss P (2001) Pax3 acts cell autonomously in the neural tube and somites by controlling cell surface properties. Development 128:1995-2005
38. Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K (2000) Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci USA 97:1618-1623
39. Inoue T, Hatayama M, Tohmonda T, Itohara S, Aruga J, Mikoshiba K (2004) Mouse Zic5 deficiency results in neural tube defects and hypoplasia of cephalic neural crest derivatives. Dev Biol 270:146-162
40. Böhm J, Buck A, Borozdin W, Mannan A, Matysiak-Scholze U, Adham I, Schulz-Schaeffer W, Floss T, Wurst W, Kohlhase J, Barrionuevo F (2008) Sall1, sall2, and sall4 are required for neural tube closure in mice. Am J Pathol 173:1455-1463
41. Chiang C, Litingtung Y, Lee E, Young K, Corden J, Westphal H, Beachy P (1996) Cyclopia and defective axial patterning in mice lacking Sonic Hedgehog gene function. Nature 383:407-413
42. Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298:1950-1954
43. Wallingford J, Harland R (2002) Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 129:5815-5825
44. Ueno N, Greene N (2003) Planar cell polarity genes and neural tube closure. Birth Defects Res C Embryo Today 69:318-324
45. Wang Y, Nathans J (2007) Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134:647-658
46. Murdoch J, Doudney K, Paternotte C, Copp A, Stanier P (2001) Severe neural tube defects in the loop-tail mouse result from mutation of Lpp 1, a novel gene involved in floor plate specification. Hum Mol Genet 10:2593-2601
47. Murdoch J, Henderson D, Doudney K, Gaston-Massuet C, Phillips H, Paternotte C, Arkell R, Stanier P, Copp A (2003) Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum Mol Genet 12:87-98
48. Kibar Z, Vogan K, Groulx N, Justice M, Underhill D, Gros P (2001) Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat Genet 28:251-255
49. Curtin J, Quint E, Tsipouri V, Arkell R, Cattanach B, Copp A, Henderson D, Spurr N, Stanier P, Fisher E, Nolan P, Steel K, Brown S, Gray I, Murdoch J (2003) Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13:1129-1133
50. Wang J, Hamblet N, Mark S, Dickinson M, Brinkman B, Segil N, Fraser S, Chen P, Wallingford J, Wynshaw-Boris A (2006) Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133:1767-1778
51. Ybot-Gonzalez P, Savery D, Gerrelli D, Signore M, Mitchell C, Faux C, Greene N, Copp A (2007) Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134:789-799
52. Schoenwolf G, Alvarez I (1989) Roles of neuroepithelial cell rearrangement and division in shaping of the avian neural plate. Development 106:427-439
53. Sausedo R, Schoenwolf G (1993) Cell behaviors underlying notochord formation and extension in avian embryos: quantitative and immunocytochemical studies. Anat Rec 237:58-70
54. Sausedo R, Schoenwolf G (1994) Quantitative analyses of cell behaviors underlying notochord formation and extension in mouse embryos. Anat Rec 239:103-112
55. Tuckett F, Morriss-Kay G (1985) The kinetic behaviour of the cranial neural epithelium during neurulation in the rat. J Embryol Exp Morphol 85:111-119
56. Baker P, Schroeder T (1967) Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube. Dev Biol 15:432-450
57. Sadler T, Greenberg D, Coughlin P, Lessard J (1982) Actin distribution patterns in the mouse neural tube during neurulation. Science 215:172-174
58. Morriss-Kay G, Tuckett F (1985) The role of microfilaments in cranial neurulation in rat embryos: effects of short-term exposure to cytochalasin D. J Embryol Exp Morphol 88:333-348
59. Schoenwolf G, Folsom D, Moe A (1988) A reexamination of the role of microfilaments in neurulation in the chick embryo. Anat Rec 220:87-102
60. Ybot-Gonzalez P, Copp A (1999) Bending of the neural plate during mouse spinal neurulation is independent of actin microfilaments. Dev Dyn 215:273-283
61. Kinoshita N, Sasai N, Misaki K, Yonemura S (2008) Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol Biol Cell 19:2289-2299
62. Nishimura T, Takeichi M (2008) Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135:1493-1502
63. Koleske A, Gifford A, Scott M, Nee M, Bronson R, Miczek K, Baltimore D (1998) Essential roles for the Abl and Arg tyrosine kinases in neurulation. Neuron 21:1259-1272
64. Gurniak C, Perlas E, Witke W (2005) The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev Biol 278:231-241
65. Brouns M, Matheson S, Hu K, Delalle I, Caviness V, Silver J, Bronson R, Settleman J (2000) The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development 127:4891-4903
66. Stumpo D, Bock C, Tuttle J, Blackshear P (1995) MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc Natl Acad Sci USA 92:944-948
67. Chen J, Chang S, Duncan S, Okano H, Fishell G, Aderem A (1996) Disruption of the MacMARCKS gene prevents cranial neural tube closure and results in anencephaly. Proc Natl Acad Sci USA 93:6275-6279
68. Lanier L, Gates M, Witke W, Menzies A, Wehman A, Macklis J, Kwiatkowski D, Soriano P, Gertler F (1999) Mena is required for neurulation and commissure formation. Neuron 22:313-325
69. Menzies A, Aszodi A, Williams S, Pfeifer A, Wehman A, Goh K, Mason C, Fassler R, Gertler F (2004) Mena and vasodilator-stimulated phosphoprotein are required for multiple actin-dependent processes that shape the vertebrate nervous system. J Neurosci 24:8029-8038
70. Wu M, Chen D, Sasaoka T, Tonegawa S (1996) Neural tube defects and abnormal brain development in F52-deficient mice. Proc Natl Acad Sci USA 93:2110-2115
71. Luo H, Liu X, Wang F, Huang Q, Shen S, Wang L, Xu G, Sun X, Kong H, Gu M, Chen S, Chen Z, Wang Z (2005) Disruption of palladin results in neural tube closure defects in mice. Mol Cell Neurosci 29:507-515
72. Hildebrand J, Soriano P (1999) Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 99:485-497
73. Xu W, Baribault H, Adamson E (1998) Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327-337
74. Nishimura T, Honda H, Takeichi M (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149:1084-1097
75. Sullivan-Brown J, Goldstein B (2012) Neural tube closure: the curious case of shrinking junctions. Curr Biol 22:R574-R576
76. Yoshida T, Vivatbutsiri P, Morriss-Kay G, Saga Y, Iseki S (2008) Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 125:797-808
77. Chen Z, Behringer R (1995) twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 9:686-699
78. Zhao Q, Behringer R, de Crombrugghe B (1996) Prenatal folic acid treatment suppresses acrania and meroanencephaly in mice mutant for the Cart1 homeobox gene. Nat Genet 13:275-283
79. Zohn I, Anderson K, Niswander L (2007) The Hectd1 ubiquitin ligase is required for development of the head mesenchyme and neural tube closure. Dev Biol 306:208-221
80. Lakhwani S, García-Sanz P, Vallejo M (2010) Alx3-deficient mice exhibit folic acid-resistant craniofacial midline and neural tube closure defects. Dev Biol 344:869-880
81. Jacobson A, Moury J (1995) Tissue boundaries and cell behavior during neurulation. Dev Biol 171:98-110
82. Moury J, Schoenwolf G (1995) Cooperative model of epithelial shaping and bending during avian neurulation: autonomous movements of the neural plate, autonomous movements of the epidermis, and interactions in the neural plate/epidermis transition zone. Dev Dyn 204:323-337
83. Alvarez I, Schoenwolf G (1992) Expansion of surface epithelium provides the major extrinsic force for bending of the neural plate. J Exp Zool 261:340-348
84. Hackett D, Smith J, Schoenwolf G (1997) Epidermal ectoderm is required for full elevation and for convergence during bending of the avian neural plate. Dev Dyn 210:397-406
85. Bray S, Kafatos F (1991) Developmental function of Elf-1: an essential transcription factor during embryogenesis in Drosophila. Genes Dev 5:1672-1683
86. Mace K, Pearson J, McGinnis W (2005) An epidermal barrier wound repair pathway in Drosophila is mediated by grainy head. Science 308:381-385
87. Ting S, Wilanowski T, Auden A, Hall M, Voss A, Thomas T, Parekh V, Cunningham J, Jane S (2003) Inositol- and folate-resistant neural tube defects in mice lacking the epithelial-specific factor Grhl-3. Nat Med 9:1513-1519
88. Werth M, Walentin K, Aue A, Schönheit J, Wuebken A, Pode-Shakked N, Vilianovitch L, Erdmann B, Dekel B, Bader M, Barasch J, Rosenbauer F, Luft F, Schmidt-Ott K (2010) The transcription factor grainyhead-like 2 regulates the molecular composition of the epithelial apical junctional complex. Development 137:3835-3845
89. Rifat Y, Parekh V, Wilanowski T, Hislop N, Auden A, Ting S, Cunningham J, Jane S (2010) Regional neural tube closure defined by the Grainy head-like transcription factors. Dev Biol 345:237-245
90. Pyrgaki C, Liu A, Niswander L (2011) Grainyhead-like 2 regulates neural tube closure and adhesion molecule expression during neural fold fusion. Dev Biol 353:38-49
91. Lee H, Adler P (2004) The grainy head transcription factor is essential for the function of the frizzled pathway in the Drosophila wing. Mech Dev 121:37-49
92. Caddy J, Wilanowski T, Darido C, Dworkin S, Ting S, Zhao Q, Rank G, Auden A, Srivastava S, Papenfuss T, Murdoch J, Humbert P, Parekh V, Boulos N, Weber T, Zuo J, Cunningham J, Jane S (2010) Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev Cell 19:138-147
93. Wilanowski T, Caddy J, Ting S, Hislop N, Cerruti L, Auden A, Zhao L, Asquith S, Ellis S, Sinclair R, Cunningham J, Jane S (2008) Perturbed desmosomal cadherin expression in grainy head-like 1-null mice. EMBO J 27:886-897
94. Hislop N, Caddy J, Ting S, Auden A, Vasudevan S, King S, Lindeman G, Visvader J, Cunningham J, Jane S (2008) Grhl3 and Lmo4 play coordinate roles in epidermal migration. Dev Biol 321:263-272
95. Boglev Y, Wilanowski T, Caddy J, Parekh V, Auden A, Darido C, Hislop N, Cangkrama M, Ting S, Jane S (2011) The unique and cooperative roles of the Grainy head-like transcription factors in epidermal development reflect unexpected target gene specificity. Dev Biol 349:512-522
96. Dworkin S, Jane S, Darido C (2011) The planar cell polarity pathway in vertebrate epidermal development, homeostasis and repair. Organogenesis 7:202-208
97. Camerer E, Barker A, Duong D, Ganesan R, Kataoka H, Cornelissen I, Darragh M, Hussain A, Zheng Y, Srinivasan Y, Brown C, Xu S, Regard J, Lin C, Craik C, Kirchhofer D, Coughlin S (2010) Local protease signaling contributes to neural tube closure in the mouse embryo. Dev Cell 18:25-38
98. Geelen J, Langman J (1979) Ultrastructural observations on closure of the neural tube in the mouse. Anat Embryol (Berl) 156:73-88
99. Pyrgaki C, Trainor P, Hadjantonakis A, Niswander L (2010) Dynamic imaging of mammalian neural tube closure. Dev Biol 344:941-947
100. Yamaguchi Y, Shinotsuka N, Nonomura K, Takemoto K, Kuida K, Yosida H, Miura M (2011) Live imaging of apoptosis in a novel transgenic mouse highlights its role in neural tube closure. J Cell Biol 195:1047-1060
101. Ray H, Niswander L (2012) Mechanisms of tissue fusion during development. Development 139:1701-1711
102. Hatta K, Takeichi M (1986) Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320:447-449
103. Wheelock M, Shintani Y, Maeda M, Fukumoto Y, Johnson K (2008) Cadherin switching. J Cell Sci 121:727-735
104. Luo Y, High F, Epstein J, Radice G (2006) N-cadherin is required for neural crest remodeling of the cardiac outflow tract. Dev Biol 299:517-528
105. Bronner-Fraser M, Wolf J, Murray B (1992) Effects of antibodies against N-cadherin and N-CAM on the cranial neural crest and neural tube. Dev Biol 153:291-301
106. Chen B, Hales B (1995) Antisense oligonucleotide down-regulation of E-cadherin in the yolk sac and cranial neural tube malformations. Biol Reprod 53:1229-1238
107. Zohn I, Li Y, Skolnik E, Anderson K, Han J, Niswander L (2006) p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 125:957-969
108. Carver E, Jiang R, Lan Y, Oram K, Gridley T (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21:8184-8188
109. Onder T, Gupta P, Mani S, Yang J, Lander E, Weinberg R (2008) Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68:3645-3654
110. Holmberg J, Clarke D, Frisén J (2000) Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408:203-206
111. Abdul-Aziz N, Turmaine M, Greene N, Copp A (2009) EphrinA-EphA receptor interactions in mouse spinal neurulation: implications for neural fold fusion. Int J Dev Biol 53:559-568
112. Tan S, Morriss-Kay G (1986) Analysis of cranial neural crest cell migration and early fates in postimplantation rat chimaeras. J Embryol Exp Morphol 98:21-58
113. Serbedzija G, Bronner-Fraser M, Fraser S (1992) Vital dye analysis of cranial neural crest cell migration in the mouse embryo. Development 116:297-307
114. Breau M, Pietri T, Stemmler M, Thiery J, Weston J (2008) A nonneural epithelial domain of embryonic cranial neural folds gives rise to ectomesenchyme. Proc Natl Acad Sci USA 105:7750-7755
115. Glücksmann A (1951) Cell deaths in normal vertebrate ontogeny. Biol Rev 26(1):59-86. doi: 10.1111/j.1469-185X.1951.tb00774.x
116. Fuchs Y, Steller H (2011) Programmed cell death in animal development and disease. Cell 147:742-758
117. Miura M (2011) Active participation of cell death in development and organismal homeostasis. Dev Growth Differ 53:125-136
118. Massa V, Savery D, Ybot-Gonzalez P, Ferraro E, Rongvaux A, Cecconi F, Flavell R, Greene N, Copp A (2009) Apoptosis is not required for mammalian neural tube closure. Proc Natl Acad Sci USA 106:8233-8238
119. Kuida K, Haydar T, Kuan C, Gu Y, Taya C, Karasuyama H, Su M, Rakic P, Flavell R (1998) Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94:325-337
120. Honarpour N, Du C, Richardson AJ, Hammer RE, Wang X, Herz J (2000) Adult Apaf-1-Deficient Mice Exhibit Male Infertility. Dev Biol 218:248-258
121. Honarpour N, Gilbert S, Lahn B, Wang X, Herz J (2001) Apaf-1 deficiency and neural tube closure defects are found in fog mice. Proc Natl Acad Sci USA 98:9683-9687
122. Hao Z, Duncan GS, Chang CC, Elia A, Fang M, Wakeham A, Okada H, Calzascia T, Jang Y, You-Ten A, Yeh WC, Ohashi P, Wang X, Mak TW (2005) Specific ablation of the apoptotic functions of cytochrome C reveals a differential requirement for cytochrome C and Apaf-1 in apoptosis. Cell 121(4):579-591. doi: 10.1016/j.cell.2005.03.016
123. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22(4):667-676
124. Toyama Y, Peralta X, Wells A, Kiehart D, Edwards G (2008) Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science 321:1683-1686
125. Rosenblatt J, Raff M, Cramer L (2001) An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 11:1847-1857
126. Slattum G, McGee K, Rosenblatt J (2009) P115 RhoGEF and microtubules decide the direction apoptotic cells extrude from an epithelium. J Cell Biol 186:693-702
127. Ryoo H, Gorenc T, Steller H (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev Cell 7:491-501
128. Chera S, Ghila L, Dobretz K, Wenger Y, Bauer C, Buzgariu W, Martinou J, Galliot B (2009) Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 17:279-289
129. Li F, Huang Q, Chen J, Peng Y, Roop D, Bedford J, Li C (2010) Apoptotic cells activate the "phoenix rising" pathway to promote wound healing and tissue regeneration. Sci Signal 3(110):ra13
130. Huang Q, Li F, Liu X, Li W, Shi W, Liu F, O'Sullivan B, He Z, Peng Y, Tan A, Zhou L, Shen J, Han G, Wang X, Thorburn J, Thorburn A, Jimeno A, Raben D, Bedford J, Li C (2011) Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy. Nat Med 17:860-866
131. Morata G, Shlevkov E, Pérez-Garijo A (2011) Mitogenic signaling from apoptotic cells in Drosophila. Dev Growth Differ 53:168-176
132. Pérez-Garijo A, Martín F, Struhl G, Morata G (2005) Dpp signaling and the induction of neoplastic tumors by caspase-inhibited apoptotic cells in Drosophila. Proc Natl Acad Sci USA 102:17664-17669
133. Iseki S (2011) Disintegration of the medial epithelial seam: is cell death important in palatogenesis? Dev Growth Differ 53:259-268
134. Tait S, Green D (2008) Caspase-independent cell death: leaving the set without the final cut. Oncogene 27:6452-6461
135. Degterev A, Yuan J (2008) Expansion and evolution of cell death programmes. Nat Rev Mol Cell Biol 9:378-390
136. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Investig 115(10):2679-2688. doi: 10.1172/JCI26390
137. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F (2007) Ambra1 regulates autophagy and development of the nervous system. Nature 447(7148):1121-1125. doi: 10.1038/nature05925
138. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N (2004) The role of autophagy during the early neonatal starvation period. Nature 432(7020):1032-1036. doi: 10.1038/nature03029
139. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169(3):425-434. doi: 10.1083/jcb.200412022
140. Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimizu S (2009) Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature 461(7264):654-658. doi: 10.1038/nature08455
141. Cecconi F, Levine B (2008) The role of autophagy in mammalian development: cell makeover rather than cell death. Dev Cell 15(3):344-357. doi: 10.1016/j.devcel.2008.08.012
142. McLaughlin M, Kruger G, Slocum K, Crowley D, Michaud N, Huang J, Magendantz M, Jacks T (2007) The Nf2 tumor suppressor regulates cell-cell adhesion during tissue fusion. Proc Natl Acad Sci USA 104:3261-3266
143. Finnell R, Moon S, Abbott L, Golden J, Chernoff G (1986) Strain differences in heat-induced neural tube defects in mice. Teratology 33:247-252
144. Wlodarczyk B, Palacios A, Chapa C, Zhu H, George T, Finnell R (2011) Genetic basis of susceptibility to teratogen induced birth defects. Am J Med Genet C Semin Med Genet 157:215-226
145. Armstrong J, Kaufman M, Harrison D, Clarke A (1995) High-frequency developmental abnormalities in p53-deficient mice. Curr Biol 5:931-936
146. Leonard J, Klocke B, D'Sa C, Flavell R, Roth K (2002) Strain-dependent neurodevelopmental abnormalities in caspase-3-deficient mice. J Neuropathol Exp Neurol 61:673-677
147. Yoshida H, Kong Y, Yoshida R, Elia A, Hakem A, Hakem R, Penninger J, Mak T (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750
148. Okamoto H, Shiraishi H, Yoshida H (2006) Histological analyses of normally grown, fertile Apaf1-deficient mice. Cell Death Differ 13:668-671
149. Günther T, Struwe M, Aguzzi A, Schughart K (1994) Open brain, a new mouse mutant with severe neural tube defects, shows altered gene expression patterns in the developing spinal cord. Development 120:3119-3130
150. Kasarskis A, Manova K, Anderson K (1998) A phenotype-based screen for embryonic lethal mutations in the mouse. Proc Natl Acad Sci USA 95:7485-7490
151. Takeuchi T, Yamazaki Y, Katoh-Fukui Y, Tsuchiya R, Kondo S, Motoyama J, Higashinakagawa T (1995) Gene trap capture of a novel mouse gene, jumonji, required for neural tube formation. Genes Dev 9:1211-1222
152. Takeuchi T, Kojima M, Nakajima K, Kondo S (1999) jumonji gene is essential for the neurulation and cardiac development of mouse embryos with a C3H/He background. Mech Dev 86:29-38
153. Gunn T, Juriloff D, Vogl W, Harris M, Miller J (1993) Histological study of the cranial neural folds of mice genetically liable to exencephaly. Teratology 48:459-471
154. Ogura Y, Sakaue-Sawano A, Nakagawa M, Satoh N, Miyawaki A, Sasakura Y (2011) Coordination of mitosis and morphogenesis: role of a prolonged G2 phase during chordate neurulation. Development 138:577-587
155. Wallingford J (2006) Planar cell polarity, ciliogenesis and neural tube defects. Hum Mol Genet 15 Spec No 2:R227-R234
156. Suzuki M, Hara Y, Takagi C, Yamamoto T, Ueno N (2010) MID1 and MID2 are required for Xenopus neural tube closure through the regulation of microtubule organization. Development 137:2329-2339
157. Suzuki M, Morita H, Ueno N (2012) Molecular mechanisms of cell shape changes that contribute to vertebrate neural tube closure. Dev Growth Differ 54:266-276
158. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, Kashiwagi S, Fukami K, Miyata T, Miyoshi H, Imamura T, Ogawa M, Masai H, Miyawaki A (2008) Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132:487-498
159. Aoki K, Komatsu N, Hirata E, Kamioka Y, Matsuda M (2012) Stable expression of FRET biosensors: a new light in cancer research. Cancer Sci 103:614-619
160. Kamioka Y, Sumiyama K, Mizuno R, Sakai Y, Hirata E, Kiyokawa E, Matsuda M (2012) Live imaging of protein kinase activities in transgenic mice expressing FRET biosensors. Cell Struct Funct 37:65-73
161. Zohn IE, Sarkar AA (2010) The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation. Birth Defects Res A Clin Mol Teratol 88(8):593-600. doi: 10.1002/bdra.20705
162. Piedrahita J, Oetama B, Bennett G, van Waes J, Kamen B, Richardson J, Lacey S, Anderson R, Finnell R (1999) Mice lacking the folic acid-binding protein Folbp1 are defective in early embryonic development. Nat Genet 23:228-232
163. Spiegelstein O, Eudy J, Finnell R (2000) Identification of two putative novel folate receptor genes in humans and mouse. Gene 258:117-125
164. Moscow J, Gong M, He R, Sgagias M, Dixon K, Anzick S, Meltzer P, Cowan K (1995) Isolation of a gene encoding a human reduced folate carrier (RFC1) and analysis of its expression in transport-deficient, methotrexate-resistant human breast cancer cells. Cancer Res 55:3790-3794
165. Qiu A, Jansen M, Sakaris A, Min S, Chattopadhyay S, Tsai E, Sandoval C, Zhao R, Akabas M, Goldman I (2006) Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell 127:917-928
166. Zhao R, Russell R, Wang Y, Liu L, Gao F, Kneitz B, Edelmann W, Goldman I (2001) Rescue of embryonic lethality in reduced folate carrier-deficient mice by maternal folic acid supplementation reveals early neonatal failure of hematopoietic organs. J Biol Chem 276:10224-10228
167. Spiegelstein O, Mitchell L, Merriweather M, Wicker N, Zhang Q, Lammer E, Finnell R (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
168. Tang L, Finnell R (2003) Neural and orofacial defects in Folp1 knockout mice [corrected]. Birth Defects Res A Clin Mol Teratol 67:209-218
169. 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(1):112-117. doi: 10.1002/dvdy.10203
170. Zhu H, Wlodarczyk B, Scott M, Yu W, Merriweather M, Gelineau-van Waes J, Schwartz R, Finnell R (2007) Cardiovascular abnormalities in Folr1 knockout mice and folate rescue. Birth Defects Res A Clin Mol Teratol 79:257-268
171. Marean A, Graf A, Zhang Y, Niswander L (2011) Folic acid supplementation can adversely affect murine neural tube closure and embryonic survival. Hum Mol Genet 20:3678-3683
172. Pickell L, Brown K, Li D, Wang X, Deng L, Wu Q, Selhub J, Luo L, Jerome-Majewska L, Rozen R (2011) High intake of folic acid disrupts embryonic development in mice. Birth Defects Res A Clin Mol Teratol 91:8-19
173. Finnell R, Spiegelstein O, Wlodarczyk B, Triplett A, Pogribny I, Melnyk S, James J (2002) DNA methylation in Folbp1 knockout mice supplemented with folic acid during gestation. J Nutr 132:2457S-2461S
174. Ichi S, Costa FF, Bischof JM, Nakazaki H, Shen YW, Boshnjaku V, Sharma S, Mania-Farnell B, McLone DG, Tomita T, Soares MB, Mayanil CS (2010) Folic acid remodels chromatin on Hes1 and Neurog2 promoters during caudal neural tube development. J Biol Chem 285(47):36922-36932. doi: 10.1074/jbc.M110.126714
175. Bohnsack BL, Hirschi KK (2004) Nutrient regulation of cell cycle progression. Annu Rev Nutr 24:433-453. doi: 10.1146/annurev.nutr.23.011702. 073203
176. Okano M, Bell D, Haber D, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247-257
177. Welstead G, Creyghton M, Bilodeau S, Cheng A, Markoulaki S, Young R, Jaenisch R (2012) X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc Natl Acad Sci USA 109:13004-13009
178. Juriloff DM, Harris MJ (2012) Hypothesis: the female excess in cranial neural tube defects reflects an epigenetic drag of the inactivating x chromosome on the molecular mechanisms of neural fold elevation. Birth Defects Res A Clin Mol Teratol. doi: 10.1002/bdra.23036
179. Narisawa A, Komatsuzaki S, Kikuchi A, Niihori T, Aoki Y, Fujiwara K, Tanemura M, Hata A, Suzuki Y, Relton C, Grinham J, Leung K, Partridge D, Robinson A, Stone V, Gustavsson P, Stanier P, Copp A, Greene N, Tominaga T, Matsubara Y, Kure S (2012) Mutations in genes encoding the glycine cleavage system predispose to neural tube defects in mice and humans. Hum Mol Genet 21:1496-1503