Hyperthermia, teratogenesis and the heat shock response in mammalian embryos in culture

International Journal of Developmental Biology

Volumn 41, Issue 2, 1997, Pages 345-358

  Edwards, Marshall J ^a   Walsh, David A ^a   Li, Zhe ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

developmental defects; embryo culture; heat shock proteins; heat stres; thermotolerance

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BIRTH DEFECT; CHICKEN; CLINICAL ARTICLE; EMBRYO CULTURE; HEAT TOLERANCE; HUMAN; HYPERTHERMIA; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE SENSITIVITY; TERATOGENESIS;

ABNORMALITIES; ANIMALS; CULTURE TECHNIQUES; EMBRYO; FEMALE; FEVER; HEAT; HEAT-SHOCK RESPONSE; HUMANS; MICE; PREGNANCY; RATS;

EID: 0030972125     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (93)

1. ALSOP, F.M. (1919). The effect of abnormal temperatures upon the developing nervous system in the chick embryos. Anat. Rec 15: 307-331.
2. ANGLES, J.M., WALSH, D.A., LI, K., BARNETT, S.B and EDWARDS, M.J. (1990). Effects of pulsed ultrasound and temperature on the development of rat embryos in culture. Teratology 42: 285-293.
3. BELL, A.W. (1987). Consequences of severe heat stress for fetal development. In Heat Stress. Physical Exertion and Environment (Eds. J.R S. Hales and D.A B Richards). Exerpta Medica, Elsevier Science, Amsterdam, pp. 313-333.
4. BRINSMADE, A B. and RUBSAAMEN, H. (1957). Zur teratogenetischen Wirkung von unspezifischem Fieber auf den sich entwickelnden Kaninchemembryo. Beitr. Pathol Anat. 117: 154-164.
5. BROWN, N.A. and FABRO, S. (1981) Quantitation of rat embryonic development in vitro. a morphological scoring system. Teratology 24: 65-78.
6. BROWN-WOODMAN, P.D.C., HADLEY, J A., WATERHOUSE, J and WEBSTER, W.S. (1988). Teratogenic effects of exposure to radiofrequency radiation (27.12 MHz) from a shortwave diathermy unit. Ind. Health 26: 1-10
7. COCKROFT, D L and NEW, D.A.T. (1975). Effects of hyperthermia on rat embryos in culture. Nature 258: 604-606
8. COCKROFT, D L and NEW, D A.T. (1978). Abnormalities induced in cultured rat embryos by hyperthermia. Teratology 17 277-284.
9. COWLES, R.B. (1965). Hyperthermia, aspermia, mutation rates and evolution Q. Rev Biol. 40: 341-367
10. CUFF, J.M., KIMMEL, G.L., KIMMEL, C.A., HEREDIA, D.J., TUDOR, N and CHEN, J. (1993). The relationship between abnormal somite development and thoracic skeletal defects in rats following heat exposure. Teratology 48 259-266.
11. DARESTE, C. (1877). Recherches sur la Production Artificielle des Monstruosites, ou Essais de Teratogenie Experimentale Reinwald, Paris.
12. DONE, J.T , WRATHALL, A E. and RICHARDSON, C (1982) Fetopathogenicity of maternal hyperthermia at mid-gestation. Proc. Int. Pig Vet. Soc., Mexico, pp. 252
13. EDWARDS, M J. (1968). Congenital malformations in the rat following induced hyperthermia during gestation Teratology 1: 173-177.
14. EDWARDS, M J (1969a) Congenital defects in guinea pigs: fetal resorptions, abortions and malformations following induced hyperthermia during early gestation Teratology 2: 313-328
15. EDWARDS, M.J. (1969b) Congenital defects in guinea pigs retardation of brain growth of guinea pigs following hyperthermia during gestation Teratology 2: 329-336.
16. EDWARDS, M J (1979) Is hyperthermia a human teratogen? Am Heart J 98: 277-280.
17. EDWARDS, M J (1981) Clinical disorders of fetal brain development defects due to hyperthermia In Fetal Brain Disorders - Recent Approaches to the Problem of Mental Deficiency (Eds B.S Hetzel and R M. Smith). Elsevier/North Holland Biomedical Press, Amsterdam, pp. 335-364
18. EDWARDS, M.J (1986) Hyperthermia as a teratogen. a review of experimental studies and their clinical significance Teratogenesis Carcinog Mutagen. 6. 563-58.
19. EDWARDS, M J and BEATSON, J. (1984). Effects of lead and hyperthermia on prenatal brain growth of guinea pigs Teratology 30 413-421
20. EDWARDS, M.J., MULLEY, R C , RING, S and WANNER, R.A. (1974). Mitotic cell death and delay of mitotic activity in guinea-pig embryos following brief maternal hyperthermia J Embryol Exp Morphol. 32: 593-602
21. EDWARDS, M J , SHIOTA, K., SMITH, M S R. and WALSH, D.A. (1995). Hyperthermia and birth defects. Reprod Toxicol 9: 411-425.
22. EDWARDS, M J , WANNER, R.A and MULLEY, R C (1976) Growth and development of the brain in normal and heat-retarded guinea pigs. Neuropathol Appl. Neurobiol. 2 439-450.
23. FERM, V H and FERM, R.R (1979) Teratogenic interaction of hyperthermia and vitamin A Biol. Neonate 36 168-172.
24. FERM, V.H and KILHAM, L (1977) Synergistic teratogenic effects of arsenic and hyperthermia in hamsters Environ Res 14: 483-486.
25. FINNELL, R.H., MOON, S.P., ABBOTT, L C., GOLDEN, J A. and CHERNOFF, G.F. (1986). Strain differences in heat-induced neural tube defects in mice. Teratology 33: 247-252.
26. FISHER, B.R , HEREDIA, D.J. and BROWN, K.M. (1995). Induction of hsp72 in heat-treated rat embryos: a tissue-specific response. Teratology 52: 90-100
27. FRASER, F C. and SKELTON, J. (1978) Possible teratogenicity of maternal fever. Lancet 2: 684.
28. FUKUI, Y., HOSHINO, K., INOUYE, M. and KAMEYAMA, Y. (1992). Effects of hyperthermia induced by microwave irradiation on brain development in mice. J. Radiat. Res. 33: 1-10
29. GERMAIN, M-A., WEBSTER, W.S. and EDWARDS, M J (1985). Hyperthermia as a teratogen: parameters determining hyperthermia-induced head defects in the rat. Teratology 31: 265-272.
30. GERMAN, J. (1984). Embryonic stress hypothesis of teratogenesis. Am. J. Med. 76: 293-301.
31. GLUCKSMANN, A (1951). Cell deaths in normal vertebrate ontogeny. Biol Rev 26: 59-86.
32. GRAHAM, J M and EDWARDS, M.J. (1988). Teratogenic effects of maternal hyperthermia Ann. Res. Inst Environ Med. Nagoya 40: 365-374
33. GRAHAM, J M., EDWARDS, M.J., LIPSON, A H., WEBSTER, W.S. and EDWARDS, M. (1988). Gestational hyperthermia as a cause for Moebius syndrome. Teratology 37: 461-462 (Abstr.).
34. HARDING, A.J. and EDWARDS, M J (1993). Micrencephaly in rats caused by maternal hyperthermia on days 13 and 14 of pregnancy. Cong Anom. 33: 203-209
35. HARRIS, C., JUCHAU, M R. and MIRKES, P.E (1991). Role of glutathione and HSP70 in the acquisition of thermotolerance in postimplantation rat embryos. Teratology 43: 229-239.
36. HARTLEY, W.J , ALEXANDER, G and EDWARDS, M J. (1974). Brain cavitation and micrencephaly in lambs exposed to prenatal hyperthermia Teratology 9:299-303.
37. HEIKKILA, J J., MILLER, J.G.O., SCHULTZ, G.A , KLOC, M. and BROWDER, L.W. (1985). Heat shock gene expression during early animal development. In Changes in Eukaryote Gene Expression in Response to Environmental Stress (Eds B G Atkinson and D B. Walden). Academic Press, Orlando, pp 135-138
38. HELLMANN, W (1977) Endotoxin fever and anomalies of development in rabbits. Arzneimittelforsch. 29: 1062-1064
39. HENDRICKX, A.G , STONE, G.W., HENDRICKSON, R.V. and MATAYOSHI, K (1979). Teratogenic effects of hyperthermia in the bonnet monkey (Macaca radiata). Teratology 19: 177-182.
40. HIGHTOWER, L.E. (1991) Heat shock, stress proteins, chaperons and proteotoxicity Cell 66: 1-20
41. HILBELINK, D.R , CHEN, L.T and BRYANT, M. (1986). Endotoxin-induced hyperthermia in pregnant golden hamsters. Teratogenesis Carcinog. Mutagen. 6: 209-217.
42. HIRSEKORN, J M. (1980) The effects of hyperthermia on the developing nervous system in the mouse embryo. Anat Rec 196: 79A
43. HOFMANN, D and DIETZEL, F. (1966) Aborte und Missbildungen nacht Kurzwellendurchflutung in der Schwangerschaft Geburtshilfe Fraunheilkd. 26: 378-390
44. HSU, C-Y. (1948). Influence of temperature on development of rat embryos. Anat. Rec 100: 307-324.
45. HUNTER, A.G W. (1984) Neural tube defects in eastern Ontario and western Quebec: demography and family data Am. J. Med. Genet. 19: 45-63
46. JOHNSON, H A. and PAVELEC, M. (1972). Thermal injury due to normal body temperature Am. J. Pathol. 66: 557-564
47. KAPRON-BRAS, C.M. and HALES, B F (1991) Heat-shock induced tolerance to the embryotoxic effects of hyperthermia and cadmium in mouse embryos in vitro. Teratology 43: 83-94
48. KHERA, K.S (1985). Maternal toxicity a possible etiological factor in embryo/fetal deaths and malformations of rodent-rabbit species Teratology 31: 129-153
49. KILHAM, L. and FERM, V.H (1976) Exencephaly in fetal hamsters following exposure to hyperthermia Teratology 14: 323-326.
50. KIMMEL, C.A , CUFF, J.M., KIMMEL, G L, HEREDIA, D.J., TUDOR, N., SILVERMAN, P M. and CHEN, J. (1993) Skeletal development following heat exposure in the rat. Teratology 47 229-242.
51. KIMMEL, G L., CUFF, J.M., KIMMEL, CA, HEREDIA, D.J., TUDOR, N and SILVERMAN, P.M. (1993). Embryonic development in vitro following short-duration exposure to heat. Teratology 47: 243-251.
52. KUNG, A.L., SHERWOOD, S.W and SCHIMKE, R.T. (1990). Cell line specific differences in the control of cell cycle progression in the absence of mitosis Proc. Natl. Acad. Sci. USA 87: 9553-9557.
53. LARY, J.M , CONOVER, D.L., FOLEY, E.D and HANSER, P.L. (1982). Teratogenic effects of 27.12 MHz radiofrequency in rats. Teratology 26: 299-309.
54. LARY, J.M., CONOVER, D.L., JOHNSON, P.H. and BURG, J.A (1983). Teratogenicity of 27 12 MHz radiation in rats is related to duration of hyperthermic exposure. Bioelectromagnetics 4: 249-255.
55. LECYK, M. (1966). The effect of hyperthermia applied in the given stages of pregnancy on the number and form of vertebrae in the offspring of white mice. Experientia 22: 254-255.
56. LINDQUIST, S. (1986). The heat shock response. Annu. Rev. Biochem 55: 1151-1191.
57. LIPSON, A. (1988). Hirschsprung disease in the offspring of mothers exposed to hyperthermia during pregnancy. Am J. Med Genet. 29: 117-124
58. LOMAX, P (1987) Implications of drugs for heat and exercise tolerance In Heat Stress. Physical Exertion and Environment(Eds.J.R.S. Hales and D.A.B. Richards). Exerpta Medica, Elsevier Science, Amsterdam, pp. 399-418.
59. MEZGER, V., LEGAGNEUX, V , BABINET, C., MORANGE, M. and BENSAUDE, O. (1991). Heat shock synthesis in preimplantation mouse embryos and embryonal carcinoma cells. In Heat Shock and Development (Eds. L. Hightower and L. Nover). Springer-Verlag, Berlin, pp. 153-166.
60. MILUNSKY, A., ULCICAS, M., ROTHMAN, K.J., WILLETT, W., JICK, S.S. and JICK, H. (1992). Maternal heat exposure and neural tube defects J. Am Med. Assoc 268: 882-885.
61. MIRKES, P E. (1985). Effects of acute exposure to elevated temperatures on rat embryo growth and development in vitro. Teratology 32: 259-266
62. MIRKES, P.E. (1987). Hyperthermia-induced heat shock response and thermotolerance in postimplantation rat embryos. Dev. Biol. 119: 115-122.
63. MIRKES, P E. and CORNEL, L. (1992). A comparison of sodium arsenite- and hyperthermia-induced stress responses and abnormal development in cultured postimplantation rat embryos. Teratology 46: 251-259.
64. MIRKES, P E. and DOGGETT, B (1992). Accumulation of heat shock protein 72 (hsp72) in postimplantation rat embryos after exposure to various periods of hyperthermia (40°-43°C) in vitro: evidence that heat shock protein 72 is a biomarker of heat-induced embryotoxicity. Teratology 46: 301-309.
65. MIRKES, P.E., GRACE, R.H. and LITTLE, S.A. (1991) Developmental regulation of heat shock protein synthesis and HSP70 RNA accumulation during postimplantation rat embryogenesis. Teratology 44: 77-89
66. MIRSKY, A.E. and PAULING, L. (1936). On the structure of native, denatured, and coagulated proteins Proc Natl. Acad Sci USA 22: 439-447.
67. MORANGE, M., DIU, A., BENSAUDE, O. and BABINET, C (1984). Altered expression of heat shock proteins in embryonal carcinoma cells and mouse early embryonic cells. Mol Cell. Biol 4: 730-735.
68. MORIMOTO, R. (1993) Cells in stress transcriptional activation of heat shock genes. Science 259: 1409-1410.
69. NAGATA, K , HIRAYOSHI, K , OBARA, M , SAGA, S. and YAMADA, K. (1988) Biosynthesis of a novel transformation-sensitive heat shock protein that binds to collagen. J Biol Chem 263: 8344-8349.
70. NAKASHIMA, K , KAWAMATA, A , FUJIKI, I and FUJIKI, Y. (1991) The individual and combined effects of X-irradiation and hyperthermia on early somite mouse embryos in culture. Teratology 44: 635-639
71. NEW, D A.T , COPPOLA, P T and TERRY, S. (1973) Culture of explanted rat embryos in rotating tubes. J. Reprod Fertil. 35: 135-138.
72. NILSEN, N.O (1985) Vascular abnormalities due to hyperthermia in chick embryos Teratology 30: 237-251
73. PLEET, H., GRAHAM, J.M. and SMITH, D.W. (1981). Central nervous system and facial defects associated with maternal hyperthermia at 4 to 14 weeks gestation. Pediatrics 67: 785-789
74. POSWILLO, D., NUNNERLEY, H , SOPHER, D and KEITH, J. (1974). Hyperthermia as a teratogenic agent. Ann. Roy Coll. Surg. Engl. 55: 171-174
75. RITOSSA, F.M (1962) A new puffing pattern induced by heat shock and DNP in Drosophila Expenentia 18: 571-573.
76. SCHLESINGER, M.J. (1990) Heat shock proteins. J. Biol Chem 265: 12111-12114.
77. SHEPARD, T H. (1989) Catalog of Teratogenic Agents. The Johns Hopkins University Press, Baltimore.
78. SHIOTA, K. (1982). Neural tube defects and maternal hyperthermia in early pregnancy: Epidemiology in a human population Am J. Med Genet. 12: 281-288.
79. SHIOTA, K (1988) Induction of neural tube defects and skeletal malformations in mice following brief hyperthermia in utero. Biol. Neonate 53: 86-97.
80. SHIOTA, K., SHIONOYA, Y., IDE, M., UENOBE, F , KUWAHARA, C. and FUKUI, Y. (1988). Teratogeinc interaction of ethanol and hyperthermia in mice. Proc. Soc. Exp. Biol. Med. 187: 142-148.
81. SKREB, N. and FRANK, Z (1963). Developmental abnormalities in the rat induced by heat shock J. Embryol. Exp. Morphol. 11: 445-457.
82. SPRAGGETT, K and FRASER, F.C. (1982). Teratogenicity of maternal fever in women - a retrospective study. Teratology 25 78 (Abstr.).
83. UPFOLD, J.B., SMITH, M.S.R and EDWARDS, M J. (1989). Quantitative study of the effects of maternal hyperthermia on cell death and proliferation in the guinea pig brain on day 21 of pregnancy. Teratology 39: 173-179.
84. WALSH, D.A. and MORRIS, V.B. (1989) Heat shock affects cell cycling in the neural plate of cultured rat embryos: a flow cytometric study. Teratology 40: 583-592.
85. WALSH, D.A., HIGHTOWER, L E., KLEIN, N.W. and EDWARDS, M.J. (1985). The induction of the heat shock proteins during early mammalian development Heat shock. Cold Spring Harbor Laboratory Symposium, Vol. 2, pp 92 (Abstr.).
86. WALSH, D A., KLEIN, N W , HIGHTOWER, L.E. and EDWARDS, M.J. (1987). Heat shock and thermotolerance during early rat embryo development. Teratology 36: 181-191
87. WALSH, D, LI, K., CROWTHER, C., MARSH, D. and EDWARDS, M. (1991) Thermotolerance and heat shock response during early development of the mammalian embryo. In Results and Problems in Cell Differentiation. 17. Heat Shock and Development (Eds. L E. Hightower and L. Nover) Springer-Verlag, Berlin, pp. 58-70.
88. WALSH, D.A., LI, K., SPEIRS, J., CROWTHER, C.E and EDWARDS, M.J. (1989). Regulation of the inducible heat shock 71 genes in early neural development of cultured rat embryos Teratology 40: 312-334
89. WALSH, D., LI, K , WASS, J., DOLNIKOV, A., ZENG, F., LI, Z. and EDWARDS, M (1993). Heat-shock gene expression and cell cycle changes during mammalian embryonic development. Dev. Genet. 14: 127-136.
90. WALSH, D A., ZHE, L., ZENG, F , YAN, W. and EDWARDS, M.J. (1994) Heat shock genes and cell cycle regulation during early mammalian development. Environ. Med 30: 1-6.
91. WANNER, R A., EDWARDS, M.J. and WRIGHT, R.G. (1976). The effect of hyperthermia on the neuroepithelium of the 21-day guinea-pig foetus histologic and ultrastructural study. J. Pathol 118: 235-244.
92. WEBSTER, W.S. and EDWARDS, M.J (1984). Hyperthermia and the induction of neural tube defects in mice. Teratology 29: 417-425.
93. WEBSTER, W S., GERMAIN, M-A and EDWARDS, M.J (1985) The induction of microphthalmia, encephalocele and other head defects following hyperthermia during the gastrulation process in the rat. Teratology 31: 73-82