Vascular patterning regulates interdigital cell death by a ros-mediated mechanism

Development (Cambridge)

Volumn 142, Issue 4, 2015, Pages 672-680

  Eshkar Oren, Idit ^a   Krief, Sharon ^a   Ferrara, Napoleone ^b   Elliott, Alison M ^c   Zelzer, Elazar ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b GENENTECH INC   (United States)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Interdigit; Limb development; Oxygen; Programmed cell death; Reactive oxygen species; Syndactyly; Vascular patterning

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; OXYGEN; PROTEIN; PROTEIN PRX1; REACTIVE OXYGEN METABOLITE; TOXIC SUBSTANCE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; EMBRYO; EX VIVO STUDY; FEMALE; IN VIVO STUDY; LIMB DEVELOPMENT; MALE; MORPHOGENESIS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SYNDACTYLY; TISSUE OXYGENATION; VASCULARIZATION; ANIMAL; CELL DEATH; EMBRYOLOGY; GENE EXPRESSION REGULATION; LIMB; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; PREGNANCY;

MUS;

ANIMALS; CELL DEATH; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; ORGAN CULTURE TECHNIQUES; PREGNANCY; REACTIVE OXYGEN SPECIES;

EID: 84922496655     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.120279     Document Type: Article

References (63)

1. Abuelo, D. N., Forman, E. N. and Rubin, L. P. (1997). Limb defects and congenital anomalies of the genitalia in an infant with homozygous alpha-thalassemia. Am. J. Med. Genet. 68, 158-161.
2. Adam, M. P., Chueh, J., El-Sayed, Y. Y., Stenzel, A., Vogel, H., Weaver, D. D. and Hoyme, H. E. (2005). Vascular-type disruptive defects in fetuses with homozygous alpha-thalassemia: report of two cases and review of the literature. Prenat. Diagn. 25, 1088-1096.
3. Belteki, G., Haigh, J., Kabacs, N., Haigh, K., Sison, K., Costantini, F., Whitsett, J., Quaggin, S. E. and Nagy, A. (2005). Conditional and inducible transgene expression in mice through the combinatorial use of Cre-mediated recombination and tetracycline induction. Nucleic Acids Res. 33, e51.
4. Benjamin, L. E. and Keshet, E. (1997). Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc. Natl. Acad. Sci. USA 94, 8761-8766.
5. Bokov, A., Chaudhuri, A. and Richardson, A. (2004). The role of oxidative damage and stress in aging. Mech. Ageing Dev. 125, 811-826.
6. Brichard, B., Vermylen, C., Scheiff, J. M., Michaux, J. L., Ninane, J. and Cornu, G. (1994). Two cases of congenital dyserythropoietic anaemia type I associated with unusual skeletal abnormalities of the limbs. Br. J. Haematol. 86, 201-202.
7. Carmeliet, P. (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936.
8. Chandel, N. S., Maltepe, E., Goldwasser, E., Mathieu, C. E., Simon, M. C. and Schumacker, P. T. (1998). Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95, 11715-11720.
9. Cleaver, O. and Melton, D. A. (2003). Endothelial signaling during development. Nat. Med. 9, 661-668.
10. Coffin, J. D. and Poole, T. J. (1988). Embryonic vascular development: immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryos. Development 102, 735-748.
11. Cooper, K. L., Hu, J. K.-H., ten Berge, D., Fernandez-Teran, M., Ros, M. A. and Tabin, C. J. (2011). Initiation of proximal-distal patterning in the vertebrate limb by signals and growth. Science 332, 1083-1086.
12. Coultas, L., Chawengsaksophak, K. and Rossant, J. (2005). Endothelial cells and VEGF in vascular development. Nature 438, 937-945.
13. Covarrubias, L., Hernández-García, D., Schnabel, D., Salas-Vidal, E. and Castro-Obregón, S. (2008). Function of reactive oxygen species during animal development: passive or active? Dev. Biol. 320, 1-11.
14. Crivellato, E., Nico, B. and Ribatti, D. (2007). Contribution of endothelial cells to organogenesis: a modern reappraisal of an old Aristotelian concept. J. Anat. 211, 415-427.
15. Díaz-Mendoza, M. J., Lorda-Diez, C. I., Montero, J. A., García-Porrero, J. A. and Hurlé, J. M. (2013). Interdigital cell death in the embryonic limb is associated with depletion of Reelin in the extracellular matrix. Cell Death Dis. 4, pe800.
16. Dor, Y., Camenisch, T. D., Itin, A., Fishman, G. I., McDonald, J. A., Carmeliet, P. and Keshet, E. (2001). A novel role for VEGF in endocardial cushion formation and its potential contribution to congenital heart defects. Development 128, 1531-1538.
17. Drake, C. J., Hungerford, J. E. and Little, C. D. (1998). Morphogenesis of the first blood vessels. Ann. N. Y. Acad. Sci. 857, 155-179.
18. Dunwoodie, S. L. (2009). The role of hypoxia in development of the Mammalian embryo. Dev. Cell 17, 755-773.
19. Dupé, V., Ghyselinck, N. B., Thomazy, V., Nagy, L., Davies, P. J. A., Chambon, P. and Mark, M. (1999).Essential roles of retinoic acid signaling in interdigital apoptosis and control of BMP-7 expression in mouse autopods. Dev. Biol. 208, 30-43.
20. Eshkar-Oren, I., Viukov, S. V., Salameh, S., Krief, S., Oh, C.-d., Akiyama, H., Gerber, H.-P., Ferrara, N. and Zelzer, E. (2009). The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation of Vegf. Development 136, 1263-1272.
21. Fallon, J. F. and Cameron, J. (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.
22. Feinberg, R. N., Latker, C. H. and Beebe, D. C. (1986). Localized vascular regression during limb morphogenesis in the chicken embryo. I. Spatial and temporal changes in the vascular pattern. Anat. Rec. 214, 405-409.
23. Fernandez-Teran, M. and Ros, M. A. (2008). The apical ectodermal ridge: morphological aspects and signaling pathways. Int. J. Dev. Biol. 52, 857-871.
24. Fernández-Terán, M. A., Hinchliffe, J. R. and Ros, M. A. (2006). Birth and death of cells in limb development: a mapping study. Dev. Dyn. 235, 2521-2537.
25. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O’Shea, K. S., Powell-Braxton, L., Hillan, K. J. and Moore, M. W. (1996). Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380, 439-442.
26. Folkman, J. (2003). Fundamental concepts of the angiogenic process. Curr. Mol. Med. 3, 643-651.
27. Gao, X., Chen, X., Taglienti, M., Rumballe, B., Little, M. H. and Kreidberg, J. A. (2005). Angioblast-mesenchyme induction of early kidney development is mediated by Wt1 and Vegfa. Development 132, 5437-5449.
28. Gerber, H. P., Hillan, K. J., Ryan, A. M., Kowalski, J., Keller, G. A., Rangell, L., Wright, B. D., Radtke, F., Aguet, M. and Ferrara, N. (1999). VEGF is required for growth and survival in neonatal mice. Development 126, 1149-1159.
29. Gossen, M., Freundlieb, S., Bender, G., Muller, G., Hillen, W. and Bujard, H. (1995). Transcriptional activation by tetracyclines in mammalian cells. Science 268, 1766-1769.
30. Guha, U., Gomes, W. A., Kobayashi, T., Pestell, R. G. and Kessler, J. A. (2002). In vivo evidence that BMP signaling is necessary for apoptosis in the mouse limb. Dev. Biol. 249, 108-120.
31. Guzy, R. D. and Schumacker, P. T. (2006). Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp. Physiol. 91, 807-819.
32. Hall, B. K. and Miyake, T. (1992). The membranous skeleton: the role of cell condensations in vertebrate skeletogenesis. Anat. Embryol. (Berl.) 186, 107-124.
33. Hernández-Martíinez, R. and Covarrubias, L. (2011). Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev. Growth Differ. 53, 245-258.
34. Hernandez-Martinez, R., Castro-Obregon, S. and Covarrubias, L. (2009). Progressive interdigital cell death: regulation by the antagonistic interaction between fibroblast growth factor 8 and retinoic acid. Development 136, 3669-3678.
35. Hurle, J. M., Colvee, E. and Fernandez-Teran, M. A. (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.
36. Hurle, J. M., Fernandez-Teran, M. A. and Colvee, E. (1986). Regression of the interdigital tissue during the formation of the digits. Acta Histochem. Suppl. 32, 165-169.
37. Hurle, J. M., Ros, M. A., Garcia-Martinez, V., Macias, D. and Ganan, Y. (1995). Cell death in the embryonic developing limb. Scanning Microsc. 9, 519-533; discussion 533-514.
38. Johnson, R. L. and Tabin, C. J. (1997). Molecular models for vertebrate limb development. Cell 90, 979-990.
39. Lallemand, Y., Nicola, M.-A., Ramos, C., Bach, A., Cloment, C. S. and Robert, B. (2005). Analysis of Msx1; Msx2 double mutants reveals multiple roles for Msx genes in limb development. Development 132, 3003-3014.
40. Lammert, E., Cleaver, O. and Melton, D. (2001). Induction of pancreatic differentiation by signals from blood vessels. Science 294, 564-567.
41. Logan, M., Martin, J. F., Nagy, A., Lobe, C., Olson, E. N. and Tabin, C. J. (2002). Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77-80.
42. Maatouk, D. M., Choi, K.-S., Bouldin, C. M. and Harfe, B. D. (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.
43. Macias, D., Ganan, Y., Sampath, T. K., Piedra, M. E., Ros, M. A. and Hurle, J. M. (1997). Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124, 1109-1117.
44. Matsumoto, K., Yoshitomi, H., Rossant, J. and Zaret, K. S. (2001). Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294, 559-563.
45. McLeod, M. J. (1980). Differential staining of cartilage and bone in whole mouse fetuses by alcian blue and alizarin red S. Teratology 22, 299-301.
46. Montero, J. A. and Hurlé, J. M. (2010). Sculpturing digit shape by cell death. Apoptosis 15, 365-375.
47. Montero, J. A., Ganan, Y., Macias, D., Rodriguez-Leon, J., Sanz-Ezquerro, J. J., Merino, R., Chimal-Monroy, J., Nieto, M. A. and Hurle, J. M. (2001). Role of FGFs in the control of programmed cell death during limb development. Development 128, 2075-2084.
48. Nikolova, G. and Lammert, E. (2003). Interdependent development of blood vessels and organs. Cell Tissue Res. 314, 33-42.
49. Pajni-Underwood, S., Wilson, C. P., Elder, C., Mishina, Y. and Lewandoski, M. (2007). BMP signals control limb bud interdigital programmed cell death by regulating FGF signaling. Development 134, 2359-2368.
50. Riddle, R. D., Johnson, R. L., Laufer, E. and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
51. Risau, W. and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91.
52. Rodriguez-Leon, J., Merino, R., Macias, D., Gañan, Y., Santesteban, E. and Hurle, J. M. (1999). Retinoic acid regulates programmed cell death through BMP signalling. Nat. Cell Biol. 1, 125-126.
53. Sabin, R. (1920). Studies on the origin of blood vessels and of red blood corpuscles as seen in the living blastoderm of chick during the second day of incubation. Contrib. Embryol. Carnegie Inst. 9, 215-262.
54. Sadler, T. W. and Rasmussen, S. A. (2010). Examining the evidence for vascular pathogenesis of selected birth defects. Am. J. Med. Genet. A 152A, 2426-2436.
55. Salas-Vidal, E., Lomeli, H., Castro-Obregón, S., Cuervo, R., Escalante-Alcalde, D. and Covarrubias, L. (1998). Reactive oxygen species participate in the control of mouse embryonic cell death. Exp. Cell Res. 238, 136-147.
56. Salas-Vidal, E., Valencia, C. and Covarrubias, L. (2001). Differential tissue growth and patterns of cell death in mouse limb autopod morphogenesis. Dev. Dyn. 220, 295-306.
57. Sato, T. and Loughna, S. (2002). Vasculogenesis and angiogenesis. In Mouse Development, pp. 211-230. Academic Press.
58. Schnabel, D., Salas-Vidal, E., Narváez, V., Sánchez-Carbente, M. d. R., Hernández-García, D., Cuervo, R. and Covarrubias, L. (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.
59. Seichert, V. and Rychter, Z. (1972). Vascularization of the developing anterior limb of the chick embryo. 3. Developmental changes in the perimetacarpal capillary network. Folia Morphol. (Praha) 20, 397-405.
60. Tirziu, D. and Simons, M. (2009). Endothelium as master regulator of organ development and growth. Vascul. Pharmacol. 50, 1-7.
61. Zeller, R., López-Ríos, J. and Zuniga, A. (2009). Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 10, 845-858.
62. Zou, H. and Niswander, L. (1996). Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272, 738-741.
63. Zuzarte-Luis, V. and Hurle, J. M. (2002). Programmed cell death in the developing limb. Int. J. Dev. Biol. 46, 871-876.