Sculpturing digit shape by cell death

Apoptosis

Volumn 15, Issue 3, 2010, Pages 365-375

  Montero, Juan A ^a   Hurlé, Juan M ^a,b  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

BMP; Caspases; Cathepsins; FGF; Interdigital cell death; Retinoic acid

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CASPASE 2; CASPASE 9; CYTOCHROME C; DICKKOPF 1 PROTEIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 8; NOTCH RECEPTOR; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; RETINOIC ACID; RETINOIC ACID RECEPTOR BETA; RETINOIC ACID RECEPTOR GAMMA; WNT PROTEIN;

APOPTOSIS; CARTILAGE; CELL ADHESION; CELL DEATH; CELL STRUCTURE; CELL SURVIVAL; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; INTERDIGITAL MESENCHYME; INTERDIGITAL NECROTIC ZONE; LIMB BUD; LIMB DEVELOPMENT; LYSOSOMAL PERMEABILIZATION; LYSOSOME; MACROPHAGE; MEMBRANE PERMEABILITY; MESENCHYME; MESODERM; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL PERMEABILIZATION; NONHUMAN; OUTER MEMBRANE; PHAGOCYTOSIS; PHYSIOLOGICAL CELL DEATH; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYNDACTYLY;

ANIMALS; CELL DEATH; EXTREMITIES; MORPHOGENESIS; REACTIVE OXYGEN SPECIES; VERTEBRATES;

AVES; MUS; VERTEBRATA;

EID: 77951665973     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-009-0444-5     Document Type: Review

References (111)

1. Z Zakeri RA Lockshin 2008 Cell death: history and future Adv Exp Med Biol 615 1 11 18437888
2. JW Saunders Jr 1966 Death in embryonic systems Science 154 604 612 5332319
3. V Zuzarte-Luis JM Hurle 2005 Programmed cell death in the embryonic vertebrate limb Semin Cell Dev Biol 16 261 269 15797836
4. MA Fernandez-Teran JR Hinchliffe MA Ros 2006 Birth and death of cells in limb development: a mapping study Dev Dyn 235 2521 2537 16881063
5. V Zuzarte-Luis JA Montero N Torre-Perez JA Garcia-Porrero JM Hurle 2007 Cathepsin D gene expression outlines the areas of physiological cell death during embryonic development Dev Dyn 236 880 885 17260350
6. M Rodriguez-Guzman JA Montero E Santesteban Y Ganan D Macias JM Hurle 2007 Tendon-muscle crosstalk controls muscle bellies morphogenesis, which is mediated by cell death and retinoic acid signaling Dev Biol 302 267 280 17070795
7. C Mori N Nakamura S Kimura H Irie T Takigawa K Shiota 1995 Programmed cell death in the interdigital tissue of the fetal mouse limb is apoptosis with DNA fragmentation Anat Rec 242 103 110 7604973
8. JR Hinchliffe DA Ede 1973 Cell death and the development of limb form and skeletal pattern in normal and wingless (Ws) chick embryos J Embryol Exp Morphol 30 753 772 4272514
9. Y Chen X Zhao 1998 Shaping limbs by apoptosis J Exp Zool 282 691 702 9846381
10. CM Bouldin BD Harfe 2009 Aberrant FGF signaling, independent of ectopic hedgehog signaling, initiates preaxial polydactyly in dorking chickens Dev Biol 334 133 141 19616534
11. JM Hurle E Colvee MA Fernandez-Teran 1985 Vascular regression during the formation of the free digits in the avian limb bud: a comparative study in chick and duck embryos J Embryol Exp Morphol 85 239 250 3989451
12. JM Hurle MA Fernandez-Teran 1983 Fine structure of the regressing interdigital membranes during the formation of the digits of the chick embryo leg bud J Embryol Exp Morphol 78 195 209 6663225
13. JM Hurle MA Fernandez-Teran 1984 Fine structure of the interdigital membranes during the morphogenesis of the digits of the webbed foot of the duck embryo J Embryol Exp Morphol 79 201 210 6716044
14. JF Fallon J Cameron 1977 Interdigital cell death during limb development of the turtle and lizard with an interpretation of evolutionary significance J Embryol Exp Morphol 40 285 289 915430
15. E Salas-Vidal C Valencia L Covarrubias 2001 Differential tissue growth and patterns of cell death in mouse limb autopod morphogenesis Dev Dyn 220 295 306 11307164
16. R Hernandez-Martinez S Castro-Obregon L Covarrubias 2009 Progressive interdigital cell death: regulation by the antagonistic interaction between fibroblast growth factor 8 and retinoic acid Development 136 3669 3678 19820185
17. SD Weatherbee RR Behringer JJ Rasweiler LA Niswander 2006 Interdigital webbing retention in bat wings illustrates genetic changes underlying amniote limb diversification Proc Natl Acad Sci USA 103 15103 15107 17015842
18. Y Ganan D Macias RD Basco R Merino JM Hurle 1998 Morphological diversity of the avian foot is related with the pattern of Msx gene expression in the developing autopod Dev Biol 196 33 41 9527879
19. JA Cameron JF Fallon 1977 The absence of cell death during development of free digits in amphibians Dev Biol 55 331 338 838123
20. T Vlaskalin CJ Wong C Tsilfidis 2004 Growth and apoptosis during larval forelimb development and adult forelimb regeneration in the newt (Notophthalmus Viridescens) Dev Genes Evol 214 423 431 15322877
21. RA Franssen S Marks D Wake N Shubin 2005 Limb Chondrogenesis of the Seepage Salamander, Desmognathus Aeneus (Amphibia: Plethodontidae) J Morphol 265 87 101 15880507
22. V Garcia-Martinez D Macias Y Ganan JM Garcia-Lobo MV Francia MA Fernandez-Teran JM Hurle 1993 Internucleosomal DNA fragmentation and programmed cell death (Apoptosis) in the interdigital tissue of the embryonic chick leg bud J Cell Sci 106 Pt 1 201 208 8270624
23. W Wood M Turmaine R Weber V Camp RA Maki SR McKercher P Martin 2000 Mesenchymal cells engulf and clear apoptotic footplate cells in macrophageless PU.1 null mouse embryos Development 127 5245 5252 11076747
24. V García-Martínez V Climent 1985 Apoptosis and necrosis in the areas of interdigital cell death of the developing chick embryo limb bud An Desarr 29 119 129
25. V Zuzarte-Luis MT Berciano M Lafarga JM Hurle 2006 Caspase redundancy and release of mitochondrial apoptotic factors characterize interdigital apoptosis Apoptosis 11 701 715 16532376
26. H Makarenkova H Sugiura K Yamagata G Owens 2005 Alternatively spliced variants of protocadherin 8 exhibit distinct patterns of expression during mouse development Biochim Biophys Acta 1681 150 156 15627506
27. JM Hurle G Corson K Daniels RS Reiter LY Sakai M Solursh 1994 Elastin exhibits a distinctive temporal and spatial pattern of distribution in the developing chick limb in association with the establishment of the cartilaginous skeleton J Cell Sci 107 Pt 9 2623 2634 7844176
28. V Dupe NB Ghyselinck V Thomazy L Nagy PJ Davies P Chambon M Mark 1999 Essential roles of retinoic acid signaling in interdigital apoptosis and control of BMP-7 expression in mouse autopods Dev Biol 208 30 43 10075839
29. DR McCulloch C Le Goff S Bhatt LJ Dixon JD Sandy SS Apte 2009 Adamts5, the gene encoding a proteoglycan-degrading metalloprotease, is expressed by specific cell lineages during mouse embryonic development and in adult tissues Gene Expr Patterns 9 314 323 19250981
30. DR McCulloch CM Nelson LJ Dixon DL Silver JD Wylie V Lindner T Sasaki MA Cooley WS Argraves SS Apte 2009 ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression Dev Cell 17 687 698 19922873
31. JH Miner J Cunningham JR Sanes 1998 Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain J Cell Biol 143 1713 1723 9852162
32. E Arteaga-Solis B Gayraud SY Lee L Shum L Sakai F Ramirez 2001 Regulation of limb patterning by extracellular microfibrils J Cell Biol 154 275 281 11470817
33. P Debeer EF Schoenmakers WO Twal WS Argraves L De Smet JP Fryns WJ Van De Ven 2002 The fibulin-1 gene (FBLN1) is disrupted in a t(12;22) associated with a complex type of synpolydactyly J Med Genet 39 98 104 11836357
34. I Smyth X Du MS Taylor MJ Justice B Beutler IJ Jackson 2004 The extracellular matrix gene frem1 is essential for the normal adhesion of the embryonic epidermis Proc Natl Acad Sci USA 101 13560 13565 15345741
35. K Bose R Nischt A Page BL Bader M Paulsson N Smyth 2006 Loss of nidogen-1 and -2 results in syndactyly and changes in limb development J Biol Chem 281 39620 39629 17023412
36. F Ramirez LY Sakai 2010 Biogenesis and Function of Fibrillin Assemblies Cell Tissue Res 339 71 82 19513754
37. T Lindsten AJ Ross A King WX Zong JC Rathmell HA Shiels E Ulrich KG Waymire P Mahar K Frauwirth, et al. 2000 The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues Mol Cell 6 1389 1399 11163212
38. J Hutcheson JC Scatizzi E Bickel NJ Brown P Bouillet A Strasser H Perlman 2005 Combined loss of proapoptotic genes bak or bax with bim synergizes to cause defects in hematopoiesis and in thymocyte apoptosis J Exp Med 201 1949 1960 15967824
39. A Crocoll U Herzer NB Ghyselinck P Chambon AC Cato 2002 Interdigital apoptosis and downregulation of BAG-1 expression in mouse autopods Mech Dev 111 149 152 11804787
40. K Nakanishi M Maruyama T Shibata N Morishima 2001 Identification of a caspase-9 substrate and detection of its cleavage in programmed cell death during mouse development J Biol Chem 276 41237 41244 11514563
41. M Chautan G Chazal F Cecconi P Gruss P Golstein 1999 Interdigital cell death can occur through a necrotic and caspase-independent pathway Curr Biol 9 967 970 10508592
42. K Kuida TF Haydar CY Kuan Y Gu C Taya H Karasuyama MS Su P Rakic RA Flavell 1998 Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9 Cell 94 325 337 9708735
43. C Pop GS Salvesen 2009 Human caspases: activation, specificity, and regulation J Biol Chem 284 21777 21781 19473994
44. CE Milligan D Prevette H Yaginuma S Homma C Cardwell LC Fritz KJ Tomaselli RW Oppenheim LM Schwartz 1995 Peptide inhibitors of the ICE protease family arrest programmed cell death of motoneurons in vivo and in vitro Neuron 15 385 393 7646891
45. K Kuida TS Zheng S Na C Kuan D Yang H Karasuyama P Rakic RA Flavell 1996 Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice Nature 384 368 372 8934524
46. TS Zheng S Hunot K Kuida RA Flavell 1999 Caspase knockouts: matters of life and death Cell Death Differ 6 1043 1053 10578172
47. Y Guo SM Srinivasula A Druilhe T Fernandes-Alnemri ES Alnemri 2002 Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria J Biol Chem 277 13430 13437 11832478
48. J Grossmann K Walther M Artinger S Kiessling J Scholmerich 2001 Apoptotic signaling during initiation of detachment-induced apoptosis ("Anoikis") of primary human intestinal epithelial cells Cell Growth Differ 12 147 155 11306515
49. L Bergeron GI Perez G Macdonald L Shi Y Sun A Jurisicova S Varmuza KE Latham JA Flaws JC Salter, et al. 1998 Defects in regulation of apoptosis in caspase-2-deficient mice Genes Dev 12 1304 1314 9573047
50. V Zuzarte-Luis JA Montero Y Kawakami JC Izpisua-Belmonte JM Hurle 2007 Lysosomal cathepsins in embryonic programmed cell death Dev Biol 301 205 217 16987511
51. L Covarrubias D Hernandez-Garcia D Schnabel E Salas-Vidal S Castro-Obregon 2008 Function of reactive oxygen species during animal development: passive or active? Dev Biol 320 1 11 18555213
52. E Salas-Vidal H Lomeli S Castro-Obregon R Cuervo D Escalante-Alcalde L Covarrubias 1998 Reactive oxygen species participate in the control of mouse embryonic cell death Exp Cell Res 238 136 147 9457066
53. SW Shan MK Tang DQ Cai YL Chui PH Chow L Grotewold KK Lee 2005 Comparative proteomic analysis identifies protein disulfide isomerase and peroxiredoxin 1 as new players involved in embryonic interdigital cell death Dev Dyn 233 266 281 15858817
54. D Schnabel E Salas-Vidal V Narvaez R Sanchez-Carbente Mdel D Hernandez-Garcia R Cuervo L Covarrubias 2006 Expression and regulation of antioxidant enzymes in the developing limb support a function of ros in interdigital cell death Dev Biol 291 291 299 16445905
55. RA Kirkland JA Windelborn JM Kasprzak JL Franklin 2002 A bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death J Neurosci 22 6480 6490 12151527
56. M Leist M Jaattela 2001 Four deaths and a funeral: from caspases to alternative mechanisms Nat Rev Mol Cell Biol 2 589 598 11483992
57. W Li X Yuan G Nordgren H Dalen GM Dubowchik RA Firestone UT Brunk 2000 Induction of cell death by the lysosomotropic detergent MSDH FEBS Lett 470 35 39 10722841
58. T Kirkegaard M Jaattela 2009 Lysosomal involvement in cell death and cancer Biochim Biophys Acta 1793 746 754 18948147
59. AE Feldstein NW Werneburg Z Li SF Bronk GJ Gores 2006 Bax inhibition protects against free fatty acid-induced lysosomal permeabilization Am J Physiol Gastrointest Liver Physiol 290 G1339 G1346 16484678
60. R Castino N Bellio G Nicotra C Follo NF Trincheri C Isidoro 2007 Cathepsin D-bax death pathway in oxidative stressed neuroblastoma cells Free Radic Biol Med 42 1305 1316 17395004
61. P Boya G Kroemer 2008 Lysosomal membrane permeabilization in cell death Oncogene 27 6434 6451 18955971
62. P Boya K Andreau D Poncet N Zamzami JL Perfettini D Metivier DM Ojcius M Jaattela G Kroemer 2003 Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion J Exp Med 197 1323 1334 12756268
63. Y Ishizaki MD Jacobson MC Raff 1998 A role for caspases in lens fiber differentiation J Cell Biol 140 153 158 9425163
64. P Saftig M Hetman W Schmahl K Weber L Heine H Mossmann A Koster B Hess M Evers K von Figura 1995 Mice deficient for the lysosomal proteinase cathepsin D exhibit progressive atrophy of the intestinal mucosa and profound destruction of lymphoid cells EMBO J 14 3599 3608 7641679
65. J Deussing W Roth P Saftig C Peters HL Ploegh JA Villadangos 1998 Cathepsins B and D are dispensable for major histocompatibility complex class II-mediated antigen presentation Proc Natl Acad Sci USA 95 4516 4521 9539769
66. W Roth J Deussing VA Botchkarev M Pauly-Evers P Saftig A Hafner P Schmidt W Schmahl J Scherer I Anton-Lamprecht, et al. 2000 Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling FASEB J 14 2075 2086 11023992
67. D Macias Y Ganan MA Ros JM Hurle 1996 In vivo inhibition of programmed cell death by local administration of FGF-2 and FGF-4 in the interdigital areas of the embryonic chick leg bud Anat Embryol (Berl) 193 533 541
68. AO Wilkie SJ Patey SH Kan AM van den Ouweland BC Hamel 2002 FGFs, their receptors, and human limb malformations: clinical and molecular correlations Am J Med Genet 112 266 278 12357470
69. X Sun FV Mariani GR Martin 2002 Functions of FGF signalling from the apical ectodermal ridge in limb development Nature 418 501 508 12152071
70. S Pajni-Underwood CP Wilson C Elder Y Mishina M Lewandoski 2007 BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling Development 134 2359 2368 17537800
71. FV Mariani CP Ahn GR Martin 2008 Genetic evidence that FGFs have an instructive role in limb proximal-distal patterning Nature 453 401 405 18449196
72. JA Montero Y Ganan D Macias J Rodriguez-Leon JJ Sanz-Ezquerro R Merino J Chimal-Monroy MA Nieto JM Hurle 2001 Role of FGFs in the control of programmed cell death during limb development Development 128 2075 2084 11493529
73. S Ota ZQ Zhou DR Keene P Knoepfler PJ Hurlin 2007 Activities of N-Myc in the developing limb link control of skeletal size with digit separation Development 134 1583 1592 17360777
74. DM Maatouk KS Choi CM Bouldin BD Harfe 2009 In the limb AER Bmp2 and Bmp4 are required for dorsal-ventral patterning and interdigital cell death but not limb outgrowth Dev Biol 327 516 523 19210962
75. S Pizette C Abate-Shen L Niswander 2001 BMP controls proximodistal outgrowth, via induction of the apical ectodermal ridge, and dorsoventral patterning in the vertebrate limb Development 128 4463 4474 11714672
76. MF Bastida R Sheth MA Ros 2009 A BMP-Shh negative-feedback loop restricts Shh expression during limb development Development 136 3779 3789 19855020
77. D Macias Y Ganan TK Sampath ME Piedra MA Ros JM Hurle 1997 Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development Development 124 1109 1117 9102298
78. H Zou R Wieser J Massague L Niswander 1997 Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage Genes Dev 11 2191 2203 9303535
79. R Merino D Macias Y Ganan AN Economides X Wang Q Wu N Stahl KT Sampath P Varona JM Hurle 1999 Expression and function of Gdf-5 during digit skeletogenesis in the embryonic chick leg bud Dev Biol 206 33 45 9918693
80. JA Montero JM Hurle 2007 Deconstructing digit chondrogenesis Bioessays 29 725 737 17621635
81. JA Montero CI Lorda-Diez Y Ganan D Macias JM Hurle 2008 Activin/TGFbeta and BMP crosstalk determines digit chondrogenesis Dev Biol 321 343 356 18602912
82. PH Francis-West KE Robertson DA Ede C Rodriguez JC Izpisua-Belmonte B Houston DW Burt C Gribbin PM Brickell C Tickle 1995 Expression of genes encoding bone morphogenetic proteins and sonic hedgehog in talpid (ta3) limb buds: their relationships in the signalling cascade involved in limb patterning Dev Dyn 203 187 197 7655081
83. CK Wang M Omi D Ferrari HC Cheng G Lizarraga HJ Chin WB Upholt CN Dealy RA Kosher 2004 Function of BMPs in the apical ectoderm of the developing mouse limb Dev Biol 269 109 122 15081361
84. P Geetha-Loganathan S Nimmagadda R Huang M Scaal B Christ 2006 Expression pattern of BMPs during chick limb development Anat Embryol (Berl) 211 Suppl 1 87 93
85. V Zuzarte-Luis JA Montero J Rodriguez-Leon R Merino JC Rodriguez-Rey JM Hurle 2004 A new role for BMP5 during limb development acting through the synergic activation of Smad and MAPK pathways Dev Biol 272 39 52 15242789
86. R Merino J Rodriguez-Leon D Macias Y Ganan AN Economides JM Hurle 1999 The BMP antagonist gremlin regulates outgrowth, chondrogenesis and programmed cell death in the developing limb Development 126 5515 5522 10556075
87. Y Yokouchi J Sakiyama T Kameda H Iba A Suzuki N Ueno A Kuroiwa 1996 BMP-2/-4 mediate programmed cell death in chicken limb buds Development 122 3725 3734 9012494
88. H Zou L Niswander 1996 Requirement for BMP signaling in interdigital apoptosis and scale formation Science 272 738 741 8614838
89. U Guha WA Gomes T Kobayashi RG Pestell JA Kessler 2002 In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb Dev Biol 249 108 120 12217322
90. L Grotewold M Plum R Dildrop T Peters U Ruther 2001 Bambi is coexpressed with Bmp-4 during mouse embryogenesis Mech Dev 100 327 330 11165491
91. N Vargesson E Laufer 2009 Negative Smad expression and regulation in the developing chick limb PLoS One 4 e5173 19352514
92. SA Ross PJ McCaffery UC Drager LM De Luca 2000 Retinoids in embryonal development Physiol Rev 80 1021 1054 10893430
93. N Mercader E Leonardo ME Piedra C Martinez-A MA Ros M Torres 2000 Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes Development 127 3961 3970 10952894
94. X Zhao IO Sirbu FA Mic N Molotkova A Molotkov S Kumar G Duester 2009 Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning Curr Biol 19 1050 1057 19464179
95. P Dolle E Ruberte P Kastner M Petkovich CM Stoner LJ Gudas P Chambon 1989 Differential expression of genes encoding alpha, beta and gamma retinoic acid receptors and CRABP in the developing limbs of the mouse Nature 342 702 705 2556642
96. P Kuss P Villavicencio-Lorini F Witte J Klose AN Albrecht P Seemann J Hecht S Mundlos 2009 Mutant Hoxd13 induces extra digits in a mouse model of synpolydactyly directly and by decreasing retinoic acid synthesis J Clin Invest 119 146 156 19075394
97. J Rodriguez-Leon R Merino D Macias Y Ganan E Santesteban JM Hurle 1999 Retinoic acid regulates programmed cell death through BMP signalling Nat Cell Biol 1 125 126 10559885
98. HS Ahuja W James Z Zakeri 1997 Rescue of the limb deformity in hammertoe mutant mice by retinoic acid-induced cell death Dev Dyn 208 466 481 9097019
99. K Yashiro X Zhao M Uehara K Yamashita M Nishijima J Nishino Y Saijoh Y Sakai H Hamada 2004 Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb Dev Cell 6 411 422 15030763
100. JC Francis F Radtke MP Logan 2005 Notch1 signals through Jagged2 to regulate apoptosis in the apical ectodermal ridge of the developing limb bud Dev Dyn 234 1006 1015 16245338
101. A Sidow MS Bulotsky AW Kerrebrock RT Bronson MJ Daly MP Reeve TL Hawkins BW Birren R Jaenisch ES Lander 1997 Serrate2 is disrupted in the mouse limb-development mutant syndactylism Nature 389 722 725 9338782
102. R Jiang Y Lan HD Chapman C Shawber CR Norton DV Serreze G Weinmaster T Gridley 1998 Defects in limb, craniofacial, and thymic development in Jagged2 mutant mice Genes Dev 12 1046 1057 9531541
103. Y Pan Z Liu J Shen R Kopan 2005 Notch1 and 2 cooperate in limb ectoderm to receive an early Jagged2 signal regulating interdigital apoptosis Dev Biol 286 472 482 16169548
104. J Chimal-Monroy JA Montero Y Ganan D Macias JA Garcia-Porrero JM Hurle 2002 Comparative analysis of the expression and regulation of Wnt5a, Fz4, and Frzb1 during digit formation and in micromass cultures Dev Dyn 224 314 320 12112461
105. J Knobloch U Ruther 2008 Shedding light on an old mystery: thalidomide suppresses survival pathways to induce limb defects Cell Cycle 7 1121 1127 18418038
106. L Grotewold U Ruther 2002 The Wnt antagonist Dickkopf-1 is regulated by Bmp signaling and c-Jun and modulates programmed cell death EMBO J 21 966 975 11867524
107. M Mukhopadhyay S Shtrom C Rodriguez-Esteban L Chen T Tsukui L Gomer DW Dorward A Glinka A Grinberg SP Huang, et al. 2001 Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse Dev Cell 1 423 434 11702953
108. L Grotewold U Ruther 2002 Bmp, Fgf and Wnt signalling in programmed cell death and chondrogenesis during vertebrate limb development: the role of Dickkopf-1 Int J Dev Biol 46 943 947 12455632
109. EB Johnson RE Hammer J Herz 2005 Abnormal development of the apical ectodermal ridge and polysyndactyly in Megf7-deficient mice Hum Mol Genet 14 3523 3538 16207730
110. R Morello TK Bertin S Schlaubitz CA Shaw S Kakuru E Munivez P Hermanns Y Chen B Zabel B Lee 2008 Brachy-syndactyly caused by loss of Sfrp2 function J Cell Physiol 217 127 137 18446812
111. B Garcia-Moreno 2009 Adaptations of proteins to cellular and subcellular pH J Biol 8 98 20017887