Effects of prenatal glucocorticoid exposure on cardiac calreticulin and calsequestrin protein expression during early development and in adulthood

Biochemical Journal

Volumn 371, Issue 1, 2003, Pages 61-69

  Langdown, Maria L ^a   Holness, Mark J ^a   Sugden, Mary C ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Calcium binding protein; Dexamethasone; Heart

Indexed keywords

CALCIUM; CARDIOLOGY; DISEASES; OSMOSIS;

PRENATAL GLUCOCORTICOID EXPOSURES;

PROTEINS;

CALRETICULIN; CALSEQUESTRIN; DEXAMETHASONE; GLUCOCORTICOID;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR RISK; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; FEMALE; FETUS DEVELOPMENT; FETUS HEART; GESTATIONAL AGE; HEART DISEASE; HYPERTENSION; INTRAUTERINE GROWTH RETARDATION; MOLECULAR WEIGHT; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RAT; ANIMAL; CHEMICALLY INDUCED DISORDER; GROWTH, DEVELOPMENT AND AGING; HEART; HEART MUSCLE; METABOLISM; PREGNANCY; PRENATAL DEVELOPMENT; WISTAR RAT;

ANIMALIA;

ANIMALS; ANIMALS, NEWBORN; CALRETICULIN; CALSEQUESTRIN; DEXAMETHASONE; EMBRYONIC AND FETAL DEVELOPMENT; FEMALE; FETAL GROWTH RETARDATION; GESTATIONAL AGE; GLUCOCORTICOIDS; HEART; MYOCARDIUM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR;

EID: 0037393115     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021771     Document Type: Article

References (41)

1. Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. and Opas, M. (1999) Calreticulin: one protein, one gene, many functions. Biochem. J. 344, 281-292
2. 2+ binding to cardiac calsequestrin. Biochem. Biophys. Res. Commun. 209, 310-315
3. Enyedi, P., Szabadkai, G., Krause, K. H., Lew, D. P. and Spat, A. (1993) Inositol 1,4,5-trisphosphate binding sites copurify with the putative Ca-storage protein calreticulin in rat liver. Cell Calcium 14, 485-492
4. 2+ influx. J. Biol. Chem. 271, 9332-9339
5. Mesaeli, N., Nakamura, K., Zvaritch, E., Diokie, P., Dziak, E., Krause, K. H., Opas, M., MacLennan, D. H. and Michalak, M. (1999) Calreticulin is essential for cardiac development. J. Cell Biol. 144, 857-868
6. Rauch, F., Prud'homme, J., Arabian, A., Dedhar, S. and St Arnaud, R. (2000) Heart, brain, and body wall defects in mice lacking calreticulin. Exp. Cell Res. 256, 105-111
7. Nakamura, K., Robertson, M., Liu, G., Dickie, P., Nakamura, K., Guo, J. Q., Duff, H. J., Opas, M., Kavanagh, K. and Michalak, M. (2001) Complete heart block and sudden death in mice overexpressing calreticulin. J. Clin. Invest. 107, 1245-1253
8. 2+-binding proteins. Semin. Cell Biol. 1, 265-275
9. Fliegel, L., Ohnishi, M., Carpenter, M. R., Khanna, V. K., Reithmeier, R. A and MacLennan, D. H. (1987) Amino acid sequence of rabbit fast-twitch skeletal muscle calsequestrin deduced from cDNA and peptide sequencing. Proc. Natl. Acad. Sci. U.S.A. 84, 1167-1171
10. Fliegel, L., Burns, K., MacLennan, D. H., Reithmeier, R. A. and Michalak, M. (1989) Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 264, 21522-21528
11. Scott, B. T., Simmerman, H. K., Collins, J. H., Nadal-Ginard, B. and Jones, L. R. (1988) Complete amino acid sequence of canine cardiac calsequestrin deduced by cDNA cloning. J. Biol. Chem. 263, 8958-8964
12. Cho, M. C., Rapacciuolo, A., Koch, W. J., Kobayashi, Y., Jones, L. R. and Rockman, H. A. (1999) Defective beta-adrenergic receptor signaling precedes the development of dilated cardiomyopathy in transgenic mice with calsequestrin overexpression. J. Biol. Chem. 274, 22251-22256
13. Koyabu, S., Imanaka-Yoshida, K., Ioshii, S. O., Nakano, T. and Yoshida, T. (1994) Switching of the dominant calcium sequestering protein during skeletal muscle differentiation. Cell Motil. Cytoskeleton 29, 259-270
14. 2+-ATPase and calsequestrin genes in rat heart during ontogenic development and aging. Circ. Res. 69, 1380-1388
15. 2+-storing proteins in endo/sarcoplasmic reticulum during differentiation of rat cardiomyocytes. J. Mol. Cell Cardiol. 28, 553-562
16. 2+ signalling in transgenic mouse cardiac myocytes overexpressing calsequestrin. J. Clin. Invest. 101, 1385-1393
17. Yasue, H., Yoshimura, M., Sumida, H., Kikuta, K., Kugiyama, K., Jougasaki, M., Ogawa, H., Okumura, K., Mukoyama, M. and Nakao, K. (1994) Localization and mechanism of secretion of B-type natriuretic peptide in comparison with those of A-type natriuretic peptide in normal subjects and patients with heart failure. Circulation 90, 195-203
18. Barker, D. J. (2000) In utero programming of cardiovascular disease. Theriogenology 53, 555-574
19. Holness, M. J., Langdown, M. L. and Sugden, M. C. (2000) Early-life programming of susceptibility to dysregulation of glucose metabolism and the development of Type 2 diabetes mellitus. Biochem. J. 349, 657-665
20. Seckl, J. R. (2001) Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol. Cell Endocrinol. 185, 61-71
21. Langdown, M. L., Holness, M. J. and Sugden, M. C. (2001) Early growth retardation induced by excessive exposure to glucocorticoids in utero selectively increases cardiac GLUT1 protein expression and Akt/protein kinase B activity in adulthood. J. Endocrinol. 169, 11-22
22. Burns, K., Duggan, B., Atkinson, E. A., Famulski, K. S., Nemer, M., Bleackley, R. C. and Michalak, M. (1994) Modulation of gene expression by calreticulin binding to the glucocorticoid receptor. Nature (London) 367, 476-480
23. Michalak, M., Burns, K., Andrin, C., Mesaeli, N., Jass, G. H., Busaan, J. L. and Opas, M. (1996) Endoplasmic reticulum form of calreticulin modulates glucocorticoid-sensitive gene expression. J. Biol. Chem. 271, 29436-29445
24. Holaska, J. M., Black, B. E., Love, D. C., Hanover, J. A., Leszyk, J. and Paschal, B. M. (2001) Calreticulin Is a receptor for nuclear export. J. Cell Biol. 152, 127-140
25. Chatelain, A., Dupouy, J. P. and Allaume, P. (1980) Fetal-maternal adrenocorticotropin and corticosterone relationships in the rat: effects of maternal adrenalectomy. Endocrinology 106, 1297-1303
26. Benediktsson, R., Lindsay, R. S., Noble, J., Seckl, J. R. and Edwards, C. R. (1993) Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 341, 339-341
27. Dodic, M., May, C. N., Wintour, E. M. and Coghlan, J. P. (1998) An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin. Sci. 94, 149-155
28. Holness, M. J., Kraus, A., Harris, R. A. and Sugden, M. C. (2000) Targeted upregulation of pyruvate dehydrogenase kinase (PDK)-4 in slow-twitch skeletal muscle underlies the stable modification of the regulatory characteristics of PDK induced by high-fat feeding. Diabetes 49, 775-781
29. Sugden, M. C., Bulmer, K., Augustine, D. and Holness, M. J. (2001) Selective modification of pyruvate dehydrogenase kinase isoform expression in rat pancreatic islets elicited by starvation and activation of peroxisome proliferator-activated receptor. α: implications for glucose-stimulated insulin secretion. Diabetes 50, 2729-2736
30. Wuytack, F., Raeymaekers, L., Verbist, J., Jones, L. R. and Casteels, R. (1987) Smooth-muscle endoplasmic reticulum contains a cardiac-like form of calsequestrin. Biochim. Biophys. Acta 899, 151-158
31. Fliegel, L., Leberer, E., Green, N. M. and MacLennan, D. H. (1989) The fast-twitch muscle calsequestrin isoform predominates in rabbit slow-twitch soleus muscle. FEBS Lett. 242, 297-300
32. Aquila-Pastir, L. A., DiPaola, N. R., Matteo, R. G., Smedira, N. G., McCarthy, P. M. and Moravec, C. S. (2002) Quantitation and distribution of β-tubulin in human cardiac myocytes. J. Mol. Cell Cardiol. 34, 1513-1523
33. Fliegel, L., Burns, K., Opas, M. and Michalak, M. (1989) The high-affinity calcium binding protein of sarcoplasmic reticulum. Tissue distribution, and homology with calregulin. Biochim. Biophys. Acta 982, 1-8
34. Milner, R. E., Baksh, S., Shemanko, C., Carpenter, M. R., Smillie, L., Vance, J. E., Opas, M. and Michalak, M. (1991) Calreticulin, and not calsequestrin, is the major calcium binding protein of smooth muscle sarcoplasmic reticulum and liver endoplasmic reticulum. J. Biol. Chem. 266, 7155-7165
35. Tharin, S., Hamel, P. A., Conway, E. M., Michalak, M. and Opas, M. (1996) Regulation of calcium binding proteins calreticulin and calsequestrin during differentiation in the myogenic cell line L6. J. Cell Physiol. 166, 547-560
36. 2+. J. Membr. Biol. 159, 179-185
37. Rendon-Huerta, E., Mendoza-Hernandez, G. and Robles-Flores, M. (1999) Characterization of calreticutin as a protein interacting with protein kinase C. Biochem. J. 344, 469-475
38. Sato, Y., Ferguson, D. G., Sako, H. Dorn, G. W., Kadambi, V. J., Yatani, A., Hoit, B. D., Walsh, R. A. and Kranias, E. G. (1998) Cardiac-specific overexpression of mouse cardiac calsequestrin is associated with depressed cardiovascular function and hypertrophy in transgenic mice. J. Biol. Chem. 273, 28470-28477
39. Arai, M., Otsu, K., MacLennan, D. H. and Periasamy, M. (1992) Regulation of sarcoplasmic reticulum gene expression during cardiac and skeletal muscle development. Am. J. Physiol. Cell Physiol. 262, C614-C620
40. Levitt, N. S., Lindsay, R. S., Holmes, M. C. and Seckl, J. R. (1996) Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 64, 412-418
41. Lindsay, R. S., Lindsay, R. M., Waddell, B. J. and Seckl, J. R. (1996) Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 β-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 39, 1299-1305