Intrauterine growth restriction disrupts developmental epigenetics around distal growth hormone response elements on the rat hepatic IGF-1 gene

FASEB Journal

Volumn 29, Issue 4, 2015, Pages 1176-1184

  Fu, Qi ^a   McKnight, Robert A ^b   Callaway, Christopher W ^b   Yu, Xing ^b   Lane, Robert H ^a   Majnik, Amber V ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

DNA; Enhancer; Histone; Methylation; Prenatal

Indexed keywords

DEOXYRIBONUCLEASE I; GROWTH HORMONE; LYSINE; SOMATOMEDIN C; STAT5B PROTEIN; HISTONE; STAT5 PROTEIN; STAT5B PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY LIGATION; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA METHYLATION; ENHANCER REGION; EPIGENETICS; FEMALE; GROWTH HORMONE RESPONSE ELEMENT; HISTONE METHYLATION; HORMONE RESPONSIVE ELEMENT; INTRAUTERINE GROWTH RESTRICTION; INTRAUTERINE GROWTH RETARDATION; INTRON; NONHUMAN; PRIORITY JOURNAL; PROGENY; RAT; UTERINE ARTERY; ANIMAL; CPG ISLAND; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LIVER; MALE; METABOLISM; NEWBORN; PREGNANCY; SPRAGUE DAWLEY RAT;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; BINDING SITES; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; INSULIN-LIKE GROWTH FACTOR I; LIVER; MALE; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RESPONSE ELEMENTS; STAT5 TRANSCRIPTION FACTOR;

EID: 84931304700     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-258442     Document Type: Article

References (79)

1. Yakar, S., Liu, J. L., Fernandez, A. M., Wu, Y., Schally, A. V., Frystyk, J., Chernausek, S. D., Mejia, W., and Le Roith, D. (2001) Liver-specific igf-1 gene deletion leads to muscle insulin insensitivity. Diabetes 50, 1110-1118
2. Yu, R., Yakar, S., Liu, Y. L., Lu, Y., LeRoith, D., Miao, D., and Liu, J. L. (2003) Liver-specific IGF-I gene deficient mice exhibit accelerated diabetes in response to streptozotocin, associated with early onset of insulin resistance. Mol. Cell. Endocrinol. 204, 31-42
3. Conti, E., Carrozza, C., Capoluongo, E., Volpe, M., Crea, F., Zuppi, C., and Andreotti, F. (2004) Insulin-like growth factor-1 as a vascular protective factor. Circulation 110, 2260-2265
4. Werner, H., and Leroith, D. (2014) Insulin and insulin-like growth factor receptors in the brain: physiological and pathological aspects [Epub ahead of print]. Eur. Neuropsychopharmacol. 10.1016/j.euroneuro.2014.01.020
5. Bates, K. A., Verdile, G., Li, Q. X., Ames, D., Hudson, P., Masters, C. L., and Martins, R. N. (2009) Clearance mechanisms of Alzheimer's amyloid-beta peptide: implications for therapeutic design and diagnostic tests. Mol. Psychiatry 14, 469-486
6. Torres-Aleman, I. (2010) Toward a comprehensive neurobiology of IGF-I. Dev. Neurobiol. 70, 384-396
7. Daughaday, W. H., and Rotwein, P. (1989) Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr. Rev. 10, 68-91
8. Kikuchi, K., Bichell, D. P., and Rotwein, P. (1992) Chromatin changes accompany the developmental activation of insulin-like growth factor I gene transcription. J. Biol. Chem. 267, 21505-21511
9. Eleswarapu, S., Gu, Z., and Jiang, H. (2008) Growth hormone regulation of insulin-like growth factor-I gene expression may be mediated by multiple distal signal transducer and activator of transcription 5 binding sites. Endocrinology 149, 2230-2240
10. Wang, Y., and Jiang, H. (2005) Identification of a distal STAT5-binding DNA region that may mediate growth hormone regulation of insulin-like growth factor-I gene expression. J. Biol. Chem. 280, 10955-10963
11. Woelfle, J., Chia, D. J., and Rotwein, P. (2003) Mechanisms of growth hormone (GH) action. Identification of conserved Stat5 binding sites that mediate GH-induced insulin-like growth factor-I gene activation. J. Biol. Chem. 278, 51261-51266
12. Chia, D. J., Ono, M., Woelfle, J., Schlesinger-Massart, M., Jiang, H., and Rotwein, P. (2006) Characterization of distinct Stat5b binding sites that mediate growth hormone-stimulated IGF-I gene transcription. J. Biol. Chem. 281, 3190-3197
13. Chia, D. J., Varco-Merth, B., and Rotwein, P. (2010) Dispersed chromosomal Stat5b-binding elements mediate growth hormone-activated insulin-like growth factor-I gene transcription. J. Biol. Chem. 285, 17636-17647
14. Rotwein, P. (2012) Mapping the growth hormone - Stat5b - IGF-I transcriptional circuit. Trends Endocrinol. Metab. 23, 186-193
15. Bichell, D. P., Kikuchi, K., and Rotwein, P. (1992) Growth hormone rapidly activates insulin-like growth factor I gene transcription in vivo. Mol. Endocrinol. 6, 1899-1908
16. Chia, D. J., Young, J. J., Mertens, A. R., and Rotwein, P. (2010) Distinct alterations in chromatin organization of the two IGF-I promoters precede growth hormone-induced activation of IGF-I gene transcription. Mol. Endocrinol. 24, 779-789
17. Fu, Q., Yu, X., Callaway, C. W., Lane, R. H., and McKnight, R. A. (2009) Epigenetics: intrauterine growth retardation (IUGR) modifies the histone code along the rat hepatic IGF-1 gene. FASEB J. 23, 2438-2449
18. Simmons, R. A., Templeton, L. J., and Gertz, S. J. (2001) Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes 50, 2279-2286
19. Bussey, M. E., Finley, S., LaBarbera, A., and Ogata, E. S. (1985) Hypoglycemia in the newborn growth-retarded rat: delayed phosphoenolpyruvate carboxykinase induction despite increased glucagon availability. Pediatr. Res. 19, 363-367
20. Lane, R. H., Chandorkar, A. K., Flozak, A. S., and Simmons, R. A. (1998) Intrauterine growth retardation alters mitochondrial gene expression and function in fetal and juvenile rat skeletal muscle. Pediatr. Res. 43, 563-570
21. Lane, R. H., Crawford, S. E., Flozak, A. S., and Simmons, R. A. (1999) Localization and quantification of glucose transporters in liver of growth-retarded fetal and neonatal rats. Am. J. Physiol. 276, E135-E142
22. Lane, R. H., Flozak, A. S., Ogata, E. S., Bell, G. I., and Simmons, R. A. (1996) Altered hepatic gene expression of enzymes involved in energy metabolism in the growth-retarded fetal rat. Pediatr. Res. 39, 390-394
23. Lane, R. H., Flozak, A. S., and Simmons, R. A. (1996) Measurement of GLUT mRNA in liver of fetal and neonatal rats using a novel method of quantitative polymerase chain reaction. Biochem. Mol. Med. 59, 192-199
24. Lane, R. H., Kelley, D. E., Gruetzmacher, E. M., and Devaskar, S. U. (2001) Uteroplacental insufficiency alters hepatic fatty acid-metabolizing enzymes in juvenile and adult rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R183-R190
25. Lane, R. H., Maclennan, N. K., Daood, M. J., Hsu, J. L., Janke, S. M., Pham, T. D., Puri, A. R., and Watchko, J. F. (2003) IUGR alters postnatal rat skeletal muscle peroxisome proliferator-activated receptor-gamma coactivator-1 gene expression in a fiber specific manner. Pediatr. Res. 53, 994-1000
26. Lane, R. H., MacLennan, N. K., Hsu, J. L., Janke, S. M., and Pham, T. D. (2002) Increased hepatic peroxisome proliferator-activated receptor-gamma coactivator-1 gene expression in a rat model of intrauterine growth retardation and subsequent insulin resistance. Endocrinology 143, 2486-2490
27. Lane, R. H., Ramirez, R. J., Tsirka, A. E., Kloesz, J. L., McLaughlin, M. K., Gruetzmacher, E. M., and Devaskar, S. U. (2001) Uteroplacental insufficiency lowers the threshold towards hypoxia-induced cerebral apoptosis in growth-retarded fetal rats. Brain Res. 895, 186-193
28. Ogata, E. S., Bussey, M. E., and Finley, S. (1986) Altered gas exchange, limited glucose and branched chain amino acids, and hypoinsulinism retard fetal growth in the rat. Metabolism 35, 970-977
29. Ogata, E. S., Bussey, M. E., LaBarbera, A., and Finley, S. (1985) Altered growth, hypoglycemia, hypoalaninemia, and ketonemia in the young rat: postnatal consequences of intrauterine growth retardation. Pediatr. Res. 19, 32-37
30. Pham, T. D., MacLennan, N. K., Chiu, C. T., Laksana, G. S., Hsu, J. L., and Lane, R. H. (2003) Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full term IUGR rat kidney. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R962-R970
31. Sadiq, H. F., Das, U. G., Tracy, T. F., and Devaskar, S. U. (1999) Intra-uterine growth restriction differentially regulates perinatal brain and skeletal muscle glucose transporters. Brain Res. 823, 96-103
32. Tsirka, A. E., Gruetzmacher, E. M., Kelley, D. E., Ritov, V. H., Devaskar, S. U., and Lane, R. H. (2001) Myocardial gene expression of glucose transporter 1 and glucose transporter 4 in response to uteroplacental insufficiency in the rat. J. Endocrinol. 169, 373-380
33. World Medical Association; American Physiological Society. (2002) Guiding principles for research involving animals and human beings. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283, R281-R283
34. Baserga, M., Hale, M. A., McKnight, R. A., Yu, X., Callaway, C. W., and Lane, R. H. (2005) Uteroplacental insufficiency alters hepatic expression, phosphorylation, and activity of the glucocorticoid receptor in fetal IUGR rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1348-R1353
35. Fu, Q., McKnight, R. A., Yu, X., Callaway, C. W., and Lane, R. H. (2006) Growth retardation alters the epigenetic characteristics of hepatic dual specificity phosphatase 5. FASEB J. 20, 2127-2129
36. Fu, Q., McKnight, R. A., Yu, X., Wang, L., Callaway, C. W., and Lane, R. H. (2004) Uteroplacental insufficiency induces site-specific changes in histone H3 covalent modifications and affects DNA-histone H3 positioning in day 0 IUGR rat liver. Physiol. Genomics 20, 108-116
37. Ke, X., Lei, Q., James, S. J., Kelleher, S. L., Melnyk, S., Jernigan, S., Yu, X., Wang, L., Callaway, C. W., Gill, G., Chan, G. M., Albertine, K. H., McKnight, R. A., and Lane, R. H. (2006) Uteroplacental insufficiency affects epigenetic determinants of chromatin structure in brains of neonatal and juvenile IUGR rats. Physiol. Genomics 25, 16-28
38. Ke, X., McKnight, R. A., Wang, Z. M., Yu, X., Wang, L., Callaway, C. W., Albertine, K. H., and Lane, R. H. (2005) Nonresponsiveness of cerebral p53-MDM2 functional circuit in newborn rat pups rendered IUGR via uteroplacental insufficiency. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R1038-R1045
39. Berger, S. L. (2007) The complex language of chromatin regulation during transcription. Nature 447, 407-412
40. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837
41. Tanaka, S., Motomura, Y., Suzuki, Y., Yagi, R., Inoue, H., Miyatake, S., and Kubo, M. (2011) The enhancer HS2 critically regulates GATA-3-mediated Il4 transcription in T(H)2 cells. Nat. Immunol. 12, 77-85
42. Bernstein, B. E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D. K., Huebert, D. J., McMahon, S., Karlsson, E. K., Kulbokas III, E. J., Gingeras, T. R., Schreiber, S. L., and Lander, E. S. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120, 169-181
43. Bannister, A. J., Schneider, R., Myers, F. A., Thorne, A. W., Crane-Robinson, C., and Kouzarides, T. (2005) Spatial distribution of di- and tri-methyl lysine 36 of histone H3 at active genes. J. Biol. Chem. 280, 17732-17736
44. Zinkhan, E. K., Fu, Q., Wang, Y., Yu, X., Callaway, C. W., Segar, J. L., Scholz, T. D., McKnight, R. A., Joss-Moore, L., and Lane, R. H. (2012) Maternal hyperglycemia disrupts histone 3 lysine 36 trimethylation of the IGF-1 gene. J. Nutr. Metab. 2012, 930364
45. Gerber, M., and Shilatifard, A. (2003) Transcriptional elongation by RNA polymerase II and histone methylation. J. Biol. Chem. 278, 26303-26306
46. Hampsey, M., and Reinberg, D. (2003) Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 113, 429-432
47. Xiao, T., Hall, H., Kizer, K. O., Shibata, Y., Hall, M. C., Borchers, C. H., and Strahl, B. D. (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17, 654-663
48. Xiao, T., Shibata, Y., Rao, B., Laribee, R. N., O'Rourke, R., Buck, M. J., Greenblatt, J. F., Krogan, N. J., Lieb, J. D., and Strahl, B. D. (2007) The RNA polymerase II kinase Ctk1 regulates positioning of a 5′ histone methylation boundary along genes. Mol. Cell. Biol. 27,721-731
49. Chia, D. J., and Rotwein, P. (2010) Defining the epigenetic actions of growth hormone: acute chromatin changes accompany GH-activated gene transcription. Mol. Endocrinol. 24, 2038-2049
50. Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W., Ching, K. A., Antosiewicz-Bourget, J. E., Liu, H., Zhang, X., Green, R. D., Lobanenkov, V. V., Stewart, R., Thomson, J. A., Crawford, G. E., Kellis, M., and Ren, B. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112
51. Rosenfeld, J. A., Wang, Z., Schones, D. E., Zhao, K., DeSalle, R., and Zhang, M. Q. (2009) Determination of enriched histone modifications in non-genic portions of the human genome. BMC Genomics 10, 143
52. Santos-Rosa, H., Schneider, R., Bannister, A. J., Sherriff, J., Bernstein, B. E., Emre, N. C., Schreiber, S. L., Mellor, J., and Kouzarides, T. (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419, 407-411
53. Snowden, A. W., Gregory, P. D., Case, C. C., and Pabo, C. O. (2002) Gene-specific targeting of H3K9 methylation is sufficient for initiating repression in vivo. Curr. Biol. 12, 2159-2166
54. Tachibana, M., Nozaki, M., Takeda, N., and Shinkai, Y. (2007) Functional dynamics of H3K9 methylation during meiotic prophase progression. EMBO J. 26, 3346-3359
55. Rosenfeld, R. G. (2009) The future of research into growth hormone responsiveness. Horm. Res. 71(Suppl 2), 71-74
56. Stadler, M. B., Murr, R., Burger, L., Ivanek, R., Lienert, F., Schöler, A., van Nimwegen, E., Wirbelauer, C., Oakeley, E. J., Gaidatzis, D., Tiwari, V. K., and Schübeler, D. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495
57. Schmidl, C., Klug, M., Boeld, T. J., Andreesen, R., Hoffmann, P., Edinger, M., and Rehli, M. (2009) Lineage-specific DNA methylation in T cells correlates with histone methylation and enhancer activity. Genome Res. 19, 1165-1174
58. Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., Gnirke, A., Jaenisch, R., and Lander, E. S. (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770
59. Santhanam, M., and Chia, D. J. (2013) Hepatic-specific accessibility of Igf1 gene enhancers is independent of growth hormone signaling. Mol. Endocrinol. 27, 2080-2092
60. Davey, H. W., Xie, T., McLachlan, M. J., Wilkins, R. J., Waxman, D. J., and Grattan, D. R. (2001) STAT5b is required for GH-induced liver IGF-I gene expression. Endocrinology 142, 3836-3841
61. Udy, G. B., Towers, R. P., Snell, R. G., Wilkins, R. J., Park, S. H., Ram, P. A., Waxman, D. J., and Davey, H. W. (1997) Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression. Proc. Natl. Acad. Sci. USA 94, 7239-7244
62. Woelfle, J., Billiard, J., and Rotwein, P. (2003) Acute control of insulin-like growth factor-I gene transcription by growth hormone through Stat5b. J. Biol. Chem. 278, 22696-22702
63. Darnell, Jr., J. E., (1997) STATs and gene regulation. Science 277, 1630-1635
64. Lanning, N. J., and Carter-Su, C. (2006) Recent advances in growth hormone signaling. Rev. Endocr. Metab. Disord. 7, 225-235
65. Zhang, Y., Laz, E. V., and Waxman, D. J. (2012) Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver. Mol. Cell. Biol. 32, 880-896
66. Vidal, O. M., Merino, R., Rico-Bautista, E., Fernandez-Perez, L., Chia, D. J., Woelfle, J., Ono, M., Lenhard, B., Norstedt, G., Rotwein, P., and Flores-Morales, A. (2007) In vivo transcript profiling and phylogenetic analysis identifies suppressor of cytokine signaling 2 as a direct signal transducer and activator of transcription 5b target in liver. Mol. Endocrinol. 21, 293-311
67. Clodfelter, K. H., Holloway, M. G., Hodor, P., Park, S. H., Ray, W. J., and Waxman, D. J. (2006) Sex-dependent liver gene expression is extensive and largely dependent upon signal transducer and activator of transcription 5b (STAT5b): STAT5b-dependent activation of male genes and repression of female genes revealed by microarray analysis. Mol. Endocrinol. 20, 1333-1351
68. Sugathan, A., and Waxman, D. J. (2013) Genome-wide analysis of chromatin states reveals distinct mechanisms of sex-dependent gene regulation in male and female mouse liver. Mol. Cell. Biol. 33, 3594-3610
69. Barker, D. J., Hales, C. N., Fall, C. H., Osmond, C., Phipps, K., and Clark, P. M. (1993) Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62-67
70. Flanagan, D. E., Moore, V. M., Godsland, I. F., Cockington, R. A., Robinson, J. S., and Phillips, D. I. (2000) Fetal growth and the physiological control of glucose tolerance in adults: a minimal model analysis. Am. J. Physiol. Endocrinol. Metab. 278, E700-E706
71. Lane, R. H., Maclennan, N. K., Shi, T., Fang, C. T., and Chiu, C. T. (2003) IUGR affects postnatal hepatic gene expression of enzymes involved in sterol synthesis in 21-day-old rats. Pediatr. Res. 53, 852 (abstr.)
72. Kolasinska-Zwierz, P., Down, T., Latorre, I., Liu, T., Liu, X. S., and Ahringer, J. (2009) Differential chromatin marking of introns and expressed exons by H3K36me3. Nat. Genet. 41, 376-381
73. Schwartz, S., Meshorer, E., and Ast, G. (2009) Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 16, 990-995
74. Tilgner, H., Nikolaou, C., Althammer, S., Sammeth, M., Beato, M., Valcárcel, J., and Guigó, R. (2009) Nucleosome positioning as a determinant of exon recognition. Nat. Struct. Mol. Biol. 16, 996-1001
75. Wilhelm, B. T., Marguerat, S., Aligianni, S., Codlin, S., Watt, S., and Bähler, J. (2011) Differential patterns of intronic and exonic DNA regions with respect to RNA polymerase II occupancy, nucleosome density and H3K36me3 marking in fission yeast. Genome Biol. 12, R82
76. Ekram, M. B., Kang, K., Kim, H., and Kim, J. (2012) Retrotransposons as a major source of epigenetic variations in the mammalian genome. Epigenetics 7, 370-382
77. Brinkman, A. B., Roelofsen, T., Pennings, S. W., Martens, J. H., Jenuwein, T., and Stunnenberg, H. G. (2006) Histonemodification patterns associated with the human X chromosome. EMBO Rep. 7, 628-634
78. Kim, A., Kiefer, C. M., and Dean, A. (2007) Distinctive signatures of histone methylation in transcribed coding and noncoding human beta-globin sequences. Mol. Cell. Biol. 27, 1271-1279
79. Vakoc, C. R., Sachdeva, M. M., Wang, H., and Blobel, G. A. (2006) Profile of histone lysine methylation across transcribed mammalian chromatin. Mol. Cell. Biol. 26, 9185-9195