Conditional inactivation of MRG15 gene function limits survival during larval and adult stages of Drosophila melanogaster

Experimental Gerontology

Volumn 45, Issue 11, 2010, Pages 825-833

  Zhang, Hongjun ^a   Li, Yishi ^a,c   Yang, Junsheng ^a,d   Tominaga, Kaoru ^b   Pereira Smith, Olivia M ^b   Tower, John ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

^c LOS ANGELES BIOMEDICAL RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Aging; Chromatin; Epigenetics; Senescence; Stem cells

Indexed keywords

CHROMOSOME PROTEIN; DOXYCYCLINE; MORF4 RELATED GENE ON CHROMOSOME 15 PROTEIN; UNCLASSIFIED DRUG;

ADULTHOOD; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; FEMALE FERTILITY; GENE CONSTRUCT; GENE FUNCTION; GENE INACTIVATION; GENE OVEREXPRESSION; INVERTED REPEAT; LARVAL DEVELOPMENT; LIFESPAN; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; RNA INTERFERENCE; SURVIVAL TIME; TRANSGENE;

AGING; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, NORTHERN; BLOTTING, WESTERN; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; FERTILITY; GENE EXPRESSION; GENE SILENCING; LARVA; LONGEVITY; MALE; MUTATION; REPRODUCTION; RNA; RNA INTERFERENCE; SURVIVAL; TRANSGENES;

DROSOPHILA MELANOGASTER; MAMMALIA; MUS;

EID: 77957768302     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2010.06.002     Document Type: Article

References (50)

1. Allikian M.J., Deckert-Cruz D., Rose M.R., Landis G.N., Tower J. Doxycycline-induced expression of sense and inverted-repeat constructs modulates phosphogluconate mutase (Pgm) gene expression in adult Drosophila melanogaster. Genome Biol. 2002, 3. research0021.
2. Allis C.D., Berger S.L., Cote J., Dent S., Jenuwien T., Kouzarides T., Pillus L., Reinberg D., Shi Y., Shiekhattar R., Shilatifard A., Workman J., Zhang Y. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131:633-636.
3. Bertram M.J., Berube N.G., Hang-Swanson X., Ran Q., Leung J.K., Bryce S., Spurgers K., Bick R.J., Baldini A., Ning Y., Clark L.J., Parkinson E.K., Barrett J.C., Smith J.R., Pereira-Smith O.M. Identification of a gene that reverses the immortal phenotype of a subset of cells and is a member of a novel family of transcription factor-like genes. Mol. Cell. Biol. 1999, 19:1479-1485.
4. Bieschke E.T., Wheeler J.C., Tower J. Doxycycline-induced transgene expression during Drosophila development and aging. Mol. Gen. Genet. 1998, 258:571-579.
5. Boyle M., Wong C., Rocha M., Jones D.L. Decline in self-renewal factors contributes to aging of the stem cell niche in the Drosophila testis. Cell Stem Cell 2007, 1:470-478.
6. Carrozza M.J., Li B., Florens L., Suganuma T., Swanson S.K., Lee K.K., Shia W.J., Anderson S., Yates J., Washburn M.P., Workman J.L. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 2005, 123:581-592.
7. Chen M., Takano-Maruyama M., Pereira-Smith O.M., Gaufo G.O., Tominaga K. MRG15, a component of HAT and HDAC complexes, is essential for proliferation and differentiation of neural precursor cells. J. Neurosci. Res. 2009, 87:1522-1531.
8. Curran S.P., Wu X., Riedel C.G., Ruvkun G. A soma-to-germline transformation in long-lived Caenorhabditis elegans mutants. Nature 2009, 459:1079-1084.
9. Dimauro T., David G. Chromatin modifications: the driving force of senescence and aging?. Aging Albany NY 2009, 1:182-190.
10. Ford D., Hoe N., Landis G.N., Tozer K., Luu A., Bhole D., Badrinath A., Tower J. Alteration of Drosophila life span using conditional, tissue-specific expression of transgenes triggered by doxycycline or RU486/Mifepristone. Exp. Gerontol. 2007, 42:483-497.
11. Frankel S., Rogina B. Drosophila longevity is not affected by heterochromatin-mediated gene silencing. Aging Cell 2005, 4:53-56.
12. Fujita M., Takasaki T., Nakajima N., Kawano T., Shimura Y., Sakamoto H. MRG-1, a mortality factor-related chromodomain protein, is required maternally for primordial germ cells to initiate mitotic proliferation in C. elegans. Mech. Dev. 2002, 114:61-69.
13. Gorrini C., Squatrito M., Luise C., Syed N., Perna D., Wark L., Martinato F., Sardella D., Verrecchia A., Bennett S., Confalonieri S., Cesaroni M., Marchesi F., Gasco M., Scanziani E., Capra M., Mai S., Nuciforo P., Crook T., Lough J., Amati B. Tip60 is a haplo-insufficient tumour suppressor required for an oncogene-induced DNA damage response. Nature 2007, 448:1063-1067.
14. Hartman P.S., Ishii N. Chromosome dosage as a life span determinant in Caenorhabiditis elegans. Mech. Ageing Dev. 2007, 128:437-443.
15. Hilfiker A., Hilfiker-Kleiner D., Pannuti A., Lucchesi J.C. mof, a putative acetyl transferase gene related to the Tip60 and MOZ human genes and to the SAS genes of yeast, is required for dosage compensation in Drosophila. EMBO J. 1997, 16:2054-2060.
16. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
17. Ikura T., Tashiro S., Kakino A., Shima H., Jacob N., Amunugama R., Yoder K., Izumi S., Kuraoka I., Tanaka K., Kimura H., Ikura M., Nishikubo S., Ito T., Muto A., Miyagawa K., Takeda S., Fishel R., Igarashi K., Kamiya K. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 2007, 27:7028-7040.
18. Joshi A.A., Struhl K. Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol. Cell 2005, 20:971-978.
19. Kang H.L., Benzer S., Min K.T. Life extension in Drosophila by feeding a drug. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:838-843.
20. Keogh M.C., Kurdistani S.K., Morris S.A., Ahn S.H., Podolny V., Collins S.R., Schuldiner M., Chin K., Punna T., Thompson N.J., Boone C., Emili A., Weissman J.S., Hughes T.R., Strahl B.D., Grunstein M., Greenblatt J.F., Buratowski S., Krogan N.J. Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 2005, 123:593-605.
21. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates J.R., Abmayr S.M., Washburn M.P., Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 2004, 306:2084-2087.
22. Landis G.N., Bhole D., Tower J. A search for doxycycline-dependent mutations that increase Drosophila melanogaster life span identifies the VhaSFD, Sugar baby, filamin, fwd and Cctl genes. Genome Biol. 2003, 4:R8.
23. Li Y., Tower J. Adult-specific over-expression of the Drosophila genes magu and hebe increases life span and modulates late-age female fecundity. Mol. Genet. Genomics 2009, 281:147-162.
24. Li H., Mitchell J.R., Hasty P. DNA double-strand breaks: a potential causative factor for mammalian aging?. Mech. Ageing Dev. 2008, 129:416-424.
25. Micchelli C.A., Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006, 439:475-479.
26. Morales V., Regnard C., Izzo A., Vetter I., Becker P.B. The MRG domain mediates the functional integration of MSL3 into the dosage compensation complex. Mol. Cell. Biol. 2005, 25:5947-5954.
27. Ohlstein B., Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 2006, 439:470-474.
28. Olgun A., Aleksenko T., Pereira-Smith O.M., Vassilatis D.K. Functional analysis of MRG-1: the ortholog of human MRG15 in Caenorhabditis elegans. J. Gerontol. A Biol. Sci. Med. Sci. 2005, 60:543-548.
29. Pan L., Chen S., Weng C., Call G., Zhu D., Tang H., Zhang N., Xie T. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 2007, 1:458-469.
30. Pardo P.S., Leung J.K., Lucchesi J.C., Pereira-Smith O.M. MRG15, a novel chromodomain protein, is present in two distinct multiprotein complexes involved in transcriptional activation. J. Biol. Chem. 2002, 277:50860-50866.
31. Pena A.N., Pereira-Smith O.M. The role of the MORF/MRG family of genes in cell growth, differentiation, DNA repair, and thereby aging. Ann. N.Y. Acad. Sci. 2007, 1100:299-305.
32. Pereira-Smith O.M., Smith J.R. Genetic analysis of indefinite division in human cells: identification of four complementation groups. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:6042-6046.
33. Qi D., Jin H., Lilja T., Mannervik M. Drosophila Reptin and other TIP60 complex components promote generation of silent chromatin. Genetics 2006, 174:241-251.
34. Rogina B., Helfand S.L. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:15998-16003.
35. Rogina B., Helfand S.L., Frankel S. Longevity regulation by Drosophila Rpd3 deacetylase and caloric restriction. Science 2002, 298:1745.
36. Rubin, G.M, Spradling, A.C., 1982. Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
37. Shen J., Curtis C., Tavaré S., Tower J. A screen of apoptosis and senescence regulatory genes for life span effects when over-expressed in Drosophila. Impact Aging 2009, 1:191-211.
38. Siebold A.P., Banerjee R., Tie F., Kiss D.L., Moskowitz J., Harte P.J. Polycomb Repressive Complex 2 and Trithorax modulate Drosophila longevity and stress resistance. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:169-174.
39. Singh S.R., Liu W., Hou S.X. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 2007, 1:191-203.
40. Spradling A.C., Stern D., Beaton A., Rhem E.J., Laverty T., Mozden N., Misra S., Rubin G.M. The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999, 153:135-177.
41. Squatrito M., Gorrini C., Amati B. Tip60 in DNA damage response and growth control: many tricks in one HAT. Trends Cell Biol. 2006, 16:433-442.
42. Takasaki T., Liu Z., Habara Y., Nishiwaki K., Nakayama J., Inoue K., Sakamoto H., Strome S. MRG-1, an autosome-associated protein, silences X-linked genes and protects germline immortality in Caenorhabditis elegans. Development 2007, 134:757-767.
43. Thomas T., Voss A.K. The diverse biological roles of MYST histone acetyltransferase family proteins. Cell Cycle 2007, 6:696-704.
44. Tominaga K., Kirtane B., Jackson J.G., Ikeno Y., Ikeda T., Hawks C., Smith J.R., Matzuk M.M., Pereira-Smith O.M. MRG15 regulates embryonic development and cell proliferation. Mol. Cell. Biol. 2005, 25:2924-2937.
45. Tower J. Sex-specific regulation of aging and apoptosis. Mech. Ageing Dev. 2006, 127:705-718.
46. Tyteca S., Legube G., Trouche D. To die or not to die: a HAT trick. Mol. Cell 2006, 24:807-808.
47. Wallenfang M.R., Nayak R., DiNardo S. Dynamics of the male germline stem cell population during aging of Drosophila melanogaster. Aging Cell 2006, 5:297-304.
48. Waskar M., Li Y., Tower J. Stem cell aging in the Drosophila ovary. AGE 2005, 27:201-212.
49. Willis-Martinez D., Richards H.W., Timchenko N.A., Medrano E.E. Role of HDAC1 in senescence, aging, and cancer. Exp. Gerontol. 2010, 45:279-285.
50. Yoshida K., Fujisawa T., Hwang J.S., Ikeo K., Gojobori T. Degeneration after sexual differentiation in hydra and its relevance to the evolution of aging. Gene 2006, 385:64-70.