Insulin like growth factor 2 expression in the rat brain both in basal condition and following learning predominantly derives from the maternal allele

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Ye, Xiaojing ^a   Kohtz, Amy ^a,b   Pollonini, Gabriella ^a   Riccio, Andrea ^c,d   Alberini, Cristina M ^a  

^a NEW YORK UNIVERSITY   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d INSTITUTE OF GENETICS AND BIOPHYSICS ADRIANO BUZZATI TRAVERSO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOMEDIN B; IGF2 PROTEIN, HUMAN; MESSENGER RNA;

ADULT; ALLELE; ANIMAL TISSUE; ARTICLE; BRAIN REGION; COGNITION; CONTROLLED STUDY; DEVELOPMENT; FEMALE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENOME IMPRINTING; GROWTH; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; MATERNAL ALLELE; NONHUMAN; PREFRONTAL CORTEX; PROTEIN EXPRESSION; RAT; ANIMAL; AVOIDANCE BEHAVIOR; CHEMISTRY; CROSS BREEDING; DNA METHYLATION; FISCHER 344 RAT; GENETICS; KIDNEY; LIVER; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SEQUENCE ALIGNMENT; SEX DIFFERENCE; SPLEEN;

ALLELES; ANIMALS; AVOIDANCE LEARNING; BASE SEQUENCE; CROSSES, GENETIC; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION; GENOMIC IMPRINTING; HIPPOCAMPUS; INSULIN-LIKE GROWTH FACTOR II; KIDNEY; LIVER; MALE; MEMORY, LONG-TERM; MOLECULAR SEQUENCE DATA; PREFRONTAL CORTEX; RATS; RATS, INBRED F344; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEX FACTORS; SPLEEN;

EID: 84949757272     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141078     Document Type: Article

References (41)

1. DeChiara TM, Robertson EJ, Efstratiadis A. Parental imprinting of the mouse insulin-like growth factor II gene. Cell. 1991; 64(4):849-59. Epub 1991/02/22. PMID: 1997210.
2. Giannoukakis N, Deal C, Paquette J, Goodyer CG, Polychronakos C. Parental genomic imprinting of the human IGF2 gene. Nature genetics. 1993; 4(1):98-101. Epub 1993/05/01. doi: 10.1038/ng0593-98 PMID: 8099843.
3. Pedone PV, Cosma MP, Ungaro P, Colantuoni V, Bruni CB, Zarrilli R, et al. Parental imprinting of rat insulin-like growth factor II gene promoters is coordinately regulated. The Journal of biological chemistry. 1994; 269(39):23970-5. Epub 1994/09/30. PMID: 7929045.
4. Sasaki H, Jones PA, Chaillet JR, Ferguson-Smith AC, Barton SC, Reik W, et al. Parental imprinting: potentially active chromatin of the repressed maternal allele of the mouse insulin-like growth factor II (Igf2) gene. Genes & development. 1992; 6(10):1843-56. Epub 1992/10/01. PMID: 1383088.
5. Hu JF, Vu TH, Hoffman AR. Differential biallelic activation of three insulin-like growth factor II promoters in the mouse central nervous system. Molecular endocrinology. 1995; 9(5):628-36. Epub 1995/05/01. doi: 10.1210/mend.9.5.7565809 PMID: 7565809.
6. Ohlsson R, Franklin G. Normal development and neoplasia: the imprinting connection. The International journal of developmental biology. 1995; 39(5):869-76. Epub 1995/10/01. PMID: 8645571.
7. Hetts SW, Rosen KM, Dikkes P, Villa-Komaroff L, Mozell RL. Expression and imprinting of the insulin-like growth factor II gene in neonatal mouse cerebellum. Journal of neuroscience research. 1997; 50 (6):958-66. Epub 1998/02/06. PMID: 9452010.
8. Lee JT, Bartolomei MS. X-inactivation, imprinting, and long noncoding RNAs in health and disease. Cell. 2013; 152(6):1308-23. Epub 2013/03/19. doi: 10.1016/j.cell.2013.02.016 PMID: 23498939.
9. Mabb AM, Judson MC, Zylka MJ, Philpot BD. Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes. Trends in neurosciences. 2011; 34(6):293-303. Epub 2011/05/20. doi: 10.1016/j.tins.2011.04.001 PMID: 21592595; PubMed Central PMCID: PMC3116240.
10. Barlow DP, Bartolomei MS. Genomic imprinting in mammals. Cold Spring Harbor perspectives in biology. 2014; 6(2). Epub 2014/02/05. doi: 10.1101/cshperspect.a018382 PMID: 24492710.
11. Wilkins JF, Ubeda F. Diseases associated with genomic imprinting. Progress in molecular biology and translational science. 2011; 101:401-45. Epub 2011/04/22. doi: 10.1016/B978-0-12-387685-0.00013-5 PMID: 21507360.
12. Gray A, Tam AW, Dull TJ, Hayflick J, Pintar J, Cavenee WK, et al. Tissue-specific and developmentally regulated transcription of the insulin-like growth factor 2 gene. DNA. 1987; 6(4):283-95. Epub 1987/08/01. PMID: 3652904.
13. Beck F, Samani NJ, Byrne S, Morgan K, Gebhard R, Brammar WJ. Histochemical localization of IGF-I and IGF-II mRNA in the rat between birth and adulthood. Development. 1988; 104(1):29-39. Epub 1988/09/01. PMID: 3253059.
14. Stylianopoulou F, Herbert J, Soares MB, Efstratiadis A. Expression of the insulin-like growth factor II gene in the choroid plexus and the leptomeninges of the adult rat central nervous system. Proceedings of the National Academy of Sciences of the United States of America. 1988; 85(1):141-5. Epub 1988/01/01. PMID: 3422410; PubMed Central PMCID: PMC279499.
15. Lund PK, Moats-Staats BM, Hynes MA, Simmons JG, Jansen M, D'Ercole AJ, et al. Somatomedin-C/insulin-like growth factor-I and insulin-like growth factor-II mRNAs in rat fetal and adult tissues. The Journal of biological chemistry. 1986; 261(31):14539-44. Epub 1986/11/05. PMID: 3771541.
16. Chen DY, Stern SA, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, et al. A critical role for IGF-II in memory consolidation and enhancement. Nature. 2011; 469(7331):491-7. Epub 2011/01/29. doi: 10.1038/nature09667 PMID: 21270887; PubMed Central PMCID: PMC3908455.
17. Stern SA, Kohtz AS, Pollonini G, Alberini CM. Enhancement of Memories by Systemic Administration of Insulin-Like Growth Factor II. Neuropsychopharmacology: official publication of the American College of Neuropsychopharmacology. 2014; 39(9):2179-90. Epub 2014/03/20. doi: 10.1038/npp.2014.69 PMID: 24642597; PubMed Central PMCID: PMC4104337.
18. Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. The EMBO journal. 2011; 30 (19):4071-83. Epub 2011/08/30. doi: 10.1038/emboj.2011.293 PMID: 21873981; PubMed Central PMCID: PMC3209781.
19. Mellott TJ, Pender SM, Burke RM, Langley EA, Blusztajn JK. IGF2 ameliorates amyloidosis, increases cholinergic marker expression and raises BMP9 and neurotrophin levels in the hippocampus of the APPswePS1dE9 Alzheimer's disease model mice. PloS one. 2014; 9(4):e94287. Epub 2014/04/16. doi: 10.1371/journal.pone.0094287 PMID: 24732467; PubMed Central PMCID: PMC3986048.
20. Pascual-Lucas M, Viana da Silva S, Di Scala M, Garcia-Barroso C, Gonzalez-Aseguinolaza G, Mulle C, et al. Insulin-like growth factor 2 reverses memory and synaptic deficits in APP transgenic mice. EMBO molecular medicine. 2014. Epub 2014/08/08. doi: 10.15252/emmm.201404228 PMID: 25100745.
21. Pham NV, Nguyen MT, Hu JF, Vu TH, Hoffman AR. Dissociation of IGF2 and H19 imprinting in human brain. Brain research. 1998; 810(1-2):1-8. Epub 1998/11/14. PMID: 9813220.
22. Milekic MH, Pollonini G, Alberini CM. Temporal requirement of C/EBPbeta in the amygdala following reactivation but not acquisition of inhibitory avoidance. Learning & memory. 2007; 14(7):504-11. Epub 2007/07/24. doi: 10.1101/lm.598307 PMID: 17644752; PubMed Central PMCID: PMC1934346.
23. VanGuilder HD, Vrana KE, Freeman WM. Twenty-five years of quantitative PCR for gene expression analysis. BioTechniques. 2008; 44(5):619-26. Epub 2008/05/14. doi: 10.2144/000112776 PMID: 18474036.
24. Caraguel CG, Stryhn H, Gagne N, Dohoo IR, Hammell KL. Selection of a cutoff value for real-time polymerase chain reaction results to fit a diagnostic purpose: analytical and epidemiologic approaches. Journal of veterinary diagnostic investigation: official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc. 2011; 23(1):2-15. Epub 2011/01/11. PMID: 21217022.
25. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, et al. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science. 2010; 329(5992):643-8. Epub 2010/07/10. doi: 10.1126/science.1190830 PMID: 20616232; PubMed Central PMCID: PMC3005244.
26. DeVeale B, van der Kooy D, Babak T. Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS genetics. 2012; 8(3):e1002600. Epub 2012/04/06. doi: 10.1371/journal.pgen.1002600 PMID: 22479196; PubMed Central PMCID: PMC3315459.
27. Harper KM, Tunc-Ozcan E, Graf EN, Herzing LB, Redei EE. Intergenerational and parent of origin effects of maternal calorie restriction on Igf2 expression in the adult rat hippocampus. Psychoneuroendocrinology. 2014; 45:187-91. Epub 2014/05/23. doi: 10.1016/j.psyneuen.2014.04.002 PMID: 24845189; PubMed Central PMCID: PMC4076822.
28. Baran Y, Subramaniam M, Biton A, Tukiainen T, Tsang EK, Rivas MA, et al. The landscape of genomic imprinting across diverse adult human tissues. Genome research. 2015; 25(7):927-36. Epub 2015/05/09. doi: 10.1101/gr.192278.115 PMID: 25953952; PubMed Central PMCID: PMC4484390.
29. Jouvenot Y, Poirier F, Jami J, Paldi A. Biallelic transcription of Igf2 and H19 in individual cells suggests a post-transcriptional contribution to genomic imprinting. Current biology: CB. 1999; 9(20):1199-202. Epub 1999/10/26. doi: 10.1016/S0960-9822(00)80026-3 PMID: 10531031.
30. Phillips JE, Corces VG. CTCF: master weaver of the genome. Cell. 2009; 137(7):1194-211. Epub 2009/07/01. doi: 10.1016/j.cell.2009.06.001 PMID: 19563753; PubMed Central PMCID: PMC3040116.
31. Bell AC, Felsenfeld G. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature. 2000; 405(6785):482-5. Epub 2000/06/06. doi: 10.1038/35013100 PMID: 10839546.
32. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature. 2000; 405(6785):486-9. Epub 2000/06/06. doi: 10.1038/35013106 PMID: 10839547.
33. Schoenherr CJ, Levorse JM, Tilghman SM. CTCF maintains differential methylation at the Igf2/H19 locus. Nature genetics. 2003; 33(1):66-9. Epub 2002/12/04. doi: 10.1038/ng1057 PMID: 12461525.
34. Sparago A, Cerrato F, Vernucci M, Ferrero GB, Silengo MC, Riccio A. Microdeletions in the human H19 DMR result in loss of IGF2 imprinting and Beckwith-Wiedemann syndrome. Nature genetics. 2004; 36 (9):958-60. Epub 2004/08/18. doi: 10.1038/ng1410 PMID: 15314640.
35. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, et al. A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Developmental cell. 2008; 15(4):547-57. Epub 2008/10/16. doi: 10.1016/j.devcel.2008.08.014 PMID: 18854139; PubMed Central PMCID: PMC2593089.
36. Quenneville S, Verde G, Corsinotti A, Kapopoulou A, Jakobsson J, Offner S, et al. In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Molecular cell. 2011; 44(3):361-72. Epub 2011/11/08. doi: 10.1016/j.molcel.2011.08.032 PMID: 22055183; PubMed Central PMCID: PMC3210328.
37. Singh P, Lee DH, Szabo PE. More than insulator: multiple roles of CTCF at the H19-Igf2 imprinted domain. Frontiers in genetics. 2012; 3:214. Epub 2012/10/23. doi: 10.3389/fgene.2012.00214 PMID: 23087708; PubMed Central PMCID: PMC3471092.
38. Han L, Lee DH, Szabo PE. CTCF is the master organizer of domain-wide allele-specific chromatin at the H19/Igf2 imprinted region. Molecular and cellular biology. 2008; 28(3):1124-35. Epub 2007/11/28. doi: 10.1128/MCB.01361-07 PMID: 18039862; PubMed Central PMCID: PMC2223393.
39. Murrell A, Heeson S, Bowden L, Constancia M, Dean W, Kelsey G, et al. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO reports. 2001; 2(12):1101-6. Epub 2001/12/18. doi: 10.1093/embo-reports/kve248 PMID: 11743023; PubMed Central PMCID: PMC1084166.
40. Jones BK, Levorse J, Tilghman SM. Deletion of a nuclease-sensitive region between the Igf2 and H19 genes leads to Igf2 misregulation and increased adiposity. Human molecular genetics. 2001; 10 (8):807-14. Epub 2001/04/04. PMID: 11285246.
41. Garfield AS, Cowley M, Smith FM, Moorwood K, Stewart-Cox JE, Gilroy K, et al. Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature. 2011; 469(7331):534-8. Epub 2011/01/29. doi: 10.1038/nature09651 PMID: 21270893; PubMed Central PMCID: PMC3031026.