Hypoxic microenvironment within an embryo induces apoptosis and is essential for proper morphological development

Teratology

Volumn 60, Issue 4, 1999, Pages 215-225

  Chen, Eunice Y ^a   Fujinaga, Masahiko ^a,b   Giaccia, Amato J ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BRANCHIAL ARCH; CELL DEATH; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; GESTATIONAL AGE; HYPOXIA; NEURAL TUBE; NEURAL TUBE DEFECT; NONHUMAN; PRIORITY JOURNAL; RAT; RHOMBENCEPHALON; SOMITE;

ANIMALS; ANOXIA; APOPTOSIS; BRAIN; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; MICROCEPHALY; MORPHOGENESIS; NEURAL TUBE DEFECTS; OXYGEN; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA;

EID: 0032882169     PISSN: 00403709     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9926(199910)60:4<215::AID-TERA6>3.0.CO;2-2     Document Type: Article

References (54)

1. Berk M, Desai SY, Heyman HC, Colmenares C. 1997. Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes Dev 11:2029-2039.
2. Brown JM, Giaccia AJ. 1998. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res 58:1408-1416.
3. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
4. Carmeliet P, Dor Y, Herbert J, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch C, Ratcliffe P, Moons L, Jain R, Collen D, Keshert E. 1998. Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394:485-490.
5. Chard T. 1994. Insulin-like growth factors and their binding proteins in normal and abnormal human fetal growth. Growth Regul 4:91-100.
6. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
7. Evans SM, Joiner B, Jenkins WT, Laughlin KM, Lord EM, Koch CJ. 1995. Identification of hypoxia in cells and tissues of epigastric 9L rat glioma using EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl) acetamide]. Br J Cancer 72:875-882.
8. Evans S, Jenkins W, Joiner B, Lord E, Koch C. 1996. 2-nitroimidazole (EF5) binding predicts radiation resistance in individual 9L s.c. tumors. Cancer Res 56:405-411.
9. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
10. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16:4604-4613.
11. Fujinaga M, Jackson E, Baden J. 1990. Interlitter variability and developmental stage of day 11 rat embryos produced by overnight and morning short-period breeding regimens. Teratology 42:535-540.
12. Fujinaga M, Brown N, Baden J. 1992. Comparison of staging systems for the gastrulation and early neurulation period in rodents: a proposed new system. Teratology 46:183-190.
13. Fujinaga M, Hoffman BB, Baden JM. 1995. Axial rotation in rat embryos: morphological analysis and microsurgical study on the role of the allantois. Teratology 51:94-106.
14. Genbacev O, Zhou Y, Ludlow JW, Fisher SJ. 1997. Regulation of human placental development by oxygen tension. Science 277:1669-1672.
15. Gersony WM, Morishima HO, Daniel SS, Kohl S, Cohen H, Brown W, James LS. 1976. The hemodynamic effects of intrauterine hypoxia: an experimental model in newborn lambs. J Pediatr 89:631-635.
16. Gottlieb E, Haffner R, King A, Asher G, Gruss P, Lonai P, Oren M. 1997. Transgenic mouse model for studying the transcriptional activity of the p53 protein: age- and tissue-dependent changes in radiation-induced activation during embryogenesis. EMBO J 16: 1381-1390.
17. Graeber TG, Peterson JF, Tsai M, Monica K, Fornace AJ Jr, Giaccia AJ. 1994. Hypoxia induces accumulation of p53 protein, but activation of a G1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 14:6264-6277.
18. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379:88-91.
19. Guillemin K, Krasnow MA. 1997. The hypoxic response: huffing and HIFing. Cell 89:9-12.
20. Guillemin K, Groppe J, Ducker K, Treisman R, Hafen E, Affolter M, Krasnow MA. 1996. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122:1353-1362.
21. Harris MJ, Juriloff DM. 1997. Genetic landmarks for defects in mouse neural tube closure. Teratology 56:177-187.
22. Ibara S, Tokunaga M, Ikenoue T, Murata Y, Hirano T, Asano H, Uemura Y. 1994. Histologic observation of the ductus arteriosus in premature infants with intrauterine growth retardation. J Perinatol 14:411-416.
23. Isaac DD, Andrew DJ. 1996. Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes Dev 10:103-117.
24. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev 12:149-162.
25. Kaufman MH. 1990. Morphological stages of postimplantation embryonic development. In: Copp AJ, Cockroft DL, editors. Postimplantation mammalian embryos: a practical approach. Oxford, UK: IRL Press, p 81-91.
26. Koch CJ, Evans SM, Lord EM. 1995. Oxygen dependence of cellular uptake of EF5 [2-(2-nitro-1H-imidazol-1-yl)-N-(2,2,3,3,3-pentafluoropropyl)acetamide]: analysis of drug adducts by fluorescent antibodies vs. bound radioactivity. Br J Cancer 72:869-874.
27. Koch C, Chasan J, Jenkins W, Chan C, Laughlin K, Evans S. 1998. Co-localization of hypoxia and apoptosis in irradiated and untreated HCT116 human colon carcinoma xenografts. Adv Exp Med Biol 454:611-618.
28. Kozak KR, Abbott B, Hankinson O. 1997. ARNT-deficient mice and placental differentiation. Dev Biol 191:297-305.
29. Lee J, Siemann D, Koch C, Lord E. 1996. Direct relationship between radiobiological hypoxia in tumors and monoclonal antibody detection of EF5 cellular adducts. Int J Cancer 67:372-378.
30. Lord EM, Harwell L, Koch CJ. 1993. Detection of hypoxic cells by monoclonal antibody recognizing 2-nitroimidazole adducts. Cancer Res 53:5721-5726.
31. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403-407.
32. Manning G, Krasnow MA. 1993. Development of the Drosophila tracheal system. In: Bate M, Martinez Arias A, editors. The development of Drosophila melanogaster. New York: Cold Spring Harbor Laboratory Press. p 609-685.
33. Mazure NM, Chen EY, Laderoute KR, Giaccia AJ. 1997. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 90:3322-3331.
34. Merten DF, Goetzman BW, Wennberg RP. 1977. Persistent fetal circulation: an evolving clinical and radiographic concept of pulmonary hypertension of the newborn. Pediatr Radiol 6:74-80.
35. Morriss GM, New DAT. 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.
36. New DAT. 1990. Introduction. In: Copp AJ, Cockroft DL, editors. Postimplantation mammalian embryos: a practical approach. Oxford, UK: IRL Press, p 1-14.
37. Ochikubo CG, Waffarn F, Turbow R, Kanakriyeh M. 1997. Echocardiographic evidence of improved hemodynamics during inhaled nitric oxide therapy for persistent pulmonary hypertension of the newborn. Pediatric Cardiol 18:282-287.
38. Phelan SA, Ito M, Loeken MR. 1997. Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis. Diabetes 46:1189-1197.
39. Ryan HE, Lo J, Johnson RS. 1998. HIF-1a is required for solid tumor formation and embryonic vascularization. EMBO J 17:3005-3015.
40. Sah VP, Attardi LD, Mulligan GJ, Williams BO, Bronson RT, Jacks T. 1995. A subset of p53-deficient embryos exhibits exencephaly. Nat Genet 10:175-180.
41. Shweiki D, Itin A, Soffer D, Keshet E. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843-845.
42. Shweiki D, Neeman M, Itin A, Keshet E. 1995. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc Natl Acad Sci USA 92:768-772.
43. Sulik KK, Dehart DB. 1988. Retinoic-acid-induced limb malformations resulting from apical ectodermal ridge cell death. Teratology 37:527-537.
44. Tapanainen PJ, Bang P, Muller HL, Wilson K, Rosenfeld RG. 1997. Hypoxia-induced changes in insulin-like growth factors and their binding proteins in pregnant rats. Horm Res 48:227-234.
45. Theiler K. 1989. The house mouse: atlas of embryonic development. New York: Springer-Verlag. p 1-168.
46. Unger C, Weiser JK, McCullough RE, Keefer S, Moore LG. 1988. Altitude, low birth weight, and infant mortality in Colorado. JAMA 259:3427-3432.
47. Waleh N, Brody M, Knapp M, Mendonca H, Lord E, Koch C, Laderoute K, Sutherland R. 1995. Mapping of the vascular endothelial growth factor-producing hypoxic cells in multicellular tumor spheroids using a hypoxia-specific marker. Cancer Res 55:6222-6226.
48. Wang GL, Semenza GL. 1993. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90:4304-4308.
49. Wang GL, Semenza GL. 1995. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270:1230-1237.
50. Wang GL, Jiang BH, Rue EA, Semenza GL. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 92:5510-5514.
51. Weil M, Jacobson MD, Raff MC. 1997. Is programmed cell death required for neural tube closure? Curr Biol 7:281-284.
52. Wenger RH, Gassmann M. 1997. Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 378:609-616.
53. Zhang Z, Galileo DS. 1997. Direct in situ end-labeling for detection of apoptotic cells in tissue sections. Biotechniques 22:834-836.
54. Zhao Q, Behringer RR, 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.