Heat-induced alterations in embryonic cytoskeletal and stress proteins precede somite malformations in rat embryos

Teratogenesis Carcinogenesis and Mutagenesis

Volumn 16, Issue 1, 1996, Pages 49-64

  Fisher, Benjamin R ^a,d   Heredia, Dinorah J ^b   Brown, Ken M ^c  

^a Ctr Devices and Radiological Hlth   (United States)

^b Biocon Inc   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d CENTER FOR DEVICES AND RADIOLOGICAL HEALTH   (United States)

Author keywords

Cytoskeletal proteins; Heat shock; Malformation; Segmentation; Somites; Stress proteins; Vimentin; Whole embryo culture

Indexed keywords

ACTIN; HEAT SHOCK PROTEIN; TUBULIN; VIMENTIN;

ANIMAL TISSUE; ARTICLE; CYTOSKELETON; EMBRYO; EMBRYO CULTURE; HEAT SHOCK; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SKELETON MALFORMATION;

ANIMALS; BLOTTING, WESTERN; CULTURE TECHNIQUES; CYTOSKELETON; EMBRYO; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; HEAT; HEAT-SHOCK PROTEINS; MALE; MESODERM; PREGNANCY; PROTEIN BIOSYNTHESIS; RATS; RATS, SPRAGUE-DAWLEY; VIMENTIN;

EID: 0030054448     PISSN: 02703211     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1520-6866(1996)16:1<49::AID-TCM6>3.0.CO;2-G     Document Type: Article

References (60)

1. Edwards MJ: Hyperthermia as a teratogen: A review of experimental studies and their clinical significance. Teratogen Carcinogen Mutagen 6:563-582, 1986.
2. Mirkes PE: Effects of acute exposure to elevated temperatures on rat embryo growth and development in vitro. Teratology 32:259-266, 1985.
3. Walsh DA, Li K, Speirs J, Crowther CE, Edwards MJ: Regulation of the inducible heat shock 71 gene in early neural development of cultured rat embryos. Teratology 40:321-334, 1989.
4. Poswillo D, Nummerley A, Sopher D: Hyperthermia as a teratogenic agent. Ann R Coll Surg Engl 55:171-174, 1974.
5. Hendrickx AG, Stone GW, Hendrickson RV, Matayoshi K: Teratogenic effects of hyperthermia in the bonnet monkey. Teratology 19:177-183, 1979.
6. Primmett DRN, Stern CD, Keynes RJ: Heat shock causes repeated segmental anomalies in the chick embryo. Development 104:331-339, 1988.
7. Arora KL, Cohen BJ, Beaudoin AR: Fetal and placental response to artificially induced hyperthermia in rats. Teratology 19:251-259, 1979.
8. Kimmel CA, Cuff JM, Kimmel GL, Heredia DJ, Brown NT: Skeletal development following heat exposure in the rat. Teratology 47:229-242, 1993.
9. Cuff JM, Kimmel GL, Kimmel CA, Heredia DJ, Tudor NT, Chen J: The relationship between abnormal somite development and thoracic skeletal defects in rats following heat exposure. Teratology 48:259-266, 1993.
10. Langenfeld KB, Garbis-Berkvens JM, Verhoef A, Peters PWJ: Histology of the rat embryo cultivated in vitro (18-22 somites). Toxicol In Vitro 2:149-161, 1988.
11. Lindquist S: The heat-shock response. Annu Rev Biochem 55:1151-1191, 1986.
12. Nover L: "Heat Shock Response." Boca Raton, FL: CRC Press, 1991.
13. Welch WJ: Mammalian stress response: Cell physiology, structure/function of stress proteins, and implications for medicine and disease. Physiol Rev 72:1063-1081, 1992.
14. Landry J, Bernier D, Chretien P, Nicole LM, Tanguay RM, Marceau N: Synthesis and degradation of heat shock proteins during development and decay of thermotolerance. Cancer Res 42:2457-2461, 1982.
15. Li GC, Werb Z: Correlation between synthesis of heat shock proteins and development of thermotolerance in Chinese hamster fibroblast. Proc Natl Acad Sci USA 79:3218-3222, 1982.
16. Walsh DA, Klein NW, Hightower LE, Edwards MJ: Heat shock and thermotolerance during early rat embryo development. Teratology 31:30A, 1985.
17. Mirkes PE: Hyperthermia-induced heat shock response and thermotolerance in postimplantation rat embryos. Dev Biol 119:115-122, 1987.
18. Welch WJ, Mizzen LA: Characterization of the thermotolerant cell. II. Effects on the intercellular distribution of heat-shock protein 70, intermediate filaments, and small nuclear ribonucleoprotein complexes. J Cell Biol 106:1117-1130, 1988.
19. New DAT: Whole-embryo culture and the study of mammalian embryos during organogenesis. Biol Rev 53:81-122, 1978.
20. Kimmel GL, Cuff JM, Kimmel CA, Heredia DJ, Brown NT, Silverman PM: Embryonic development in vitro following short-duration exposure to heat. Teratology 47:243-251, 1993.
21. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ: Protein measurement with the folin phenol reagent. J Biol Chem 193:265-275, 1951.
22. Goering PL, Fisher BR, Chaudhary PP, Dick CA: Relationships between stress protein induction in rat kidney by mercuric chloride and nephrotoxicity. Toxicol Appl Pharmacol 113:184-191, 1992.
23. Welch WJ, Suhan JP: Cellular and biochemical events in mammalian cells during and after recovery from physiological stress. J Cell Biol 103:2035-2052, 1986.
24. Kilgore JL, Timson BF, Saunders DK, Kraemer RR, Klemm RD, Ross CR: Stress protein induction in skeletal muscle: Comparison of laboratory models to naturally occurring hypertrophy. J Appl Physiol 76:598-601, 1994.
25. Benyamin Y, Roger M, Gabrion J, Robin Y, van Thoai N: Immunological comparison of muscle actins from mammal, bird and fish: A quantitative approach. FEBS Lett 102:69-74, 1979.
26. Frank WW, Schmid E, Winter S, Osborn M, Weber K: Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Exp Cell Res 123:25-46, 1979.
27. Shelanski ML, Gaskin F, Canto CR: Microtubule assembly in the absence of added nucleotides. Proc Natl Acad Sci USA 70:765-768, 1973.
28. Veini M, Bellairs R: Heat shock effects in chick embryos. In Bellairs R, Ede DA, Lash JW: "Somites in Developing Embryos." New York: Plenum Press, 1986, pp 135-145.
29. Elsdale T, Pearson M, Whitehead M: Abnormalities in somite segmentation following heat shock to Xenopus embryos. J Embryol Exp Morphol 35:625-635, 1976.
30. Cooke J: Somite abnormalities caused by short heat shock to pre-neurula stages of Xenopus laevis. J Embryol Exp Morphol 45:283-294, 1978.
31. Lazarides E: Intermediate filaments: A chemically heterogenous, developmentally regulated class of proteins. Annu Rev Biochem 51:210-250, 1982.
32. Welch WJ, Feramisco JR: Disruption of the three cytoskeletal networks in mammalian cells does not affect transcription, translation, or protein translocation changes induced by heat shock. Mol Cell Biol 5:1571-1581, 1985.
33. Welch WJ, Suhan JP: Morphological study of the mammalian stress response: Characterization of changes in cytoplasmic organelles, cytoskeleton, and nucleoli, and appearance of intranuclear actin filaments in rat fibroblasts after heat-shock treatment. J Cell Biol 101:1198-1211, 1985.
34. Welch WJ, Feramisco JR, Blose SH: The mammalian stress response and the cytoskeleton: Alteration in intermediate filaments. Ann NY Acad Sci 455:57-67, 1985.
35. Weller NK: A 70 kDa microtubule-associated protein in NIL8 cells comigrates with the 70 kDa heat shock protein. Biol Cell 63:307-317, 1988.
36. Kitano Y, Okada N: Organization and disorganization of actin filaments in human epidermal keratinocytes: Heat-shock treatment and recovery process. Cell Tissue Res 261:269-274, 1990.
37. Loomis WF, Wheeler S: Heat shock response to Dictostelium. Dev Biol 79:399-408, 1980.
38. Ron A, Zeuthen E: Tubulin synthesis and heat shock-induced cell synchrony in Tetrahymena. Exp Cell Res 128:303-309, 1980.
39. Findley RC, Pederson T: Regulated transcription of the genes for actin and heat-shock proteins in cultured Drosophila cells. J Cell Biol 88:323-328, 1981.
40. Schlesinger MJ: Heat shock proteins. J Biol Chem 265:12111-12114, 1990.
41. Welch WJ: The mammalian stress response: Cell physiology and biochemistry of stress proteins. In Morimoto RI, Tissieres A, Georgopoulos C: "Stress Proteins in Biology and Medicine." Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1990, pp 223-278.
42. Walter MF, Petersen NS, Biessmann H: Heat shock causes the collapse of the intermediate filament cytoskeleton in Drosophilia embryos. Dev Genet 11:270-279, 1990.
43. Ritossa FM: A new puffing pattern induced by heat shock and DNP in Drosophila. Experientia 18:571-573, 1962.
44. Goering PL, Fisher BR, Kish CL: Stress protein synthesis induced in rat liver by cadmium precedes hepatotoxicity. Toxicol Appl Pharmacol 122:139-148, 1993.
45. Anson JF, Laborde JB, Pipkin JL, Hinson WG, Hansen DK, Sheehan DM, Young JF: Target tissue specificity of retinoic acid-induced stress proteins and malformations in mice. Teratology 44:19-28, 1991.
46. Fisher BR, Heredia DJ, Brown KM: Induction of hsp72 in heat-treated rat embryos: A tissue-specific response. Teratology 52:90-100, 1995.
47. Blake MJ, Gershon D, Fargnoli J, Holbrook NJ: Discordant expression of heat shock proteins mRNAs in tissues of heat-stressed rats. J Biol Chem 265:15275-15279, 1990.
48. Clark BD, Brown IR: A retinal heat shock protein is associated with elements of the cytoskeleton and binds to calmodulin, Biochem Biophys Res Commun 139:974-981, 1986.
49. Koyasu S, Nishida E, Kaowaski T, Matsuzaki F, Iida K, Harada F, Kasuga M, Sakai H, Yahara I: Two mammalian heat shock proteins. HSP90 and HSP100, are actin-binding proteins. Proc Natl Acad Sci USA 83:8054-8058, 1986.
50. Nishida E, Koyasu S, Sakai H, Yahara I: Calmodulin-regulated binding of the 90-kDa heat shock protein to actin filaments. J Biol Chem 261:16033-16036, 1986.
51. Gupta RS: Mitochondria, molecular chaperone proteins and the in vivo assembly of microtubules. Trends Biochem Sci 15:415-418, 1990.
52. Fostinis Y, Theodoropoulos PA, Gravanis A, Stournaras C: Heat shock protein hsp90 and its association with the cytoskeleton: A morphological study. Biochem Cell Biol 70:779-786, 1992.
53. Lavoie JN, Hickey E, Weber LA, Landry J: Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. J Biol Chem 268:24210-24214, 1993.
54. Tsang TC: New model for 70 kDa heat-shock proteins' potential mechanisms of function. FEBS 323:1-3, 1993.
55. Lee Y-C, Lai Y-K: Integrity of intermediate filaments is associated with the development of acquired thermotolerance in 9L rat brain tumor cells. J Cell Biochem 57:150-162, 1995.
56. Subjeck JR, Shyy T, Shen J, Johnson RJ: Association between mammalian 110,000 dalton heat shock protein and nucleoli. J Cell Biol 97:1389-1398, 1983.
57. Gudi T, Gupta CM: Hsp70-!ike protein in rhesus erythrocyte cytosol and its interactions with membrane skeleton under heat and pathologic stress. J Biol Chem 268:21344-21350, 1993.
58. Lavoie JN, Gingras-Breton G, Tanguay RM, Landry J: Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock: HSP27 stabilization of the microfilament organization. J Biol Chem 268:3420-3429, 1993.
59. van Bergen en Henegouwen PM, Linnemans AM: Heat shock gene expression and cytoskeletal alterations in mouse neuroblastoma cells. Exp Cell Res 171:367-375, 1987.
60. Collier NC, Sheetz MP, Schlesinger MJ: Concomitant changes in mitochondria and intermediate filaments during heat shock and recovery of chicken embryo fibroblasts. J Cell Biochem 52:297-307, 1993.