Drosophila Rbp6 Is an Orthologue of Vertebrate Msi-1 and Msi-2, but Does Not Function Redundantly with dMsi to Regulate Germline Stem Cell Behaviour

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Siddall, Nicole A ^a,b   Kalcina, Marina ^a,b   Johanson, Timothy M ^a   Monk, Adrian C ^a,b   Casagranda, Franca ^a   Been, Reeva P ^a   McLaughlin, Eileen A ^b,c   Hime, Gary R ^a,b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b Australian Government Australian Research Council   (Australia)

^c UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ISOPROTEIN; MUSASHI 1 PROTEIN; MUSASHI 2 PROTEIN; PROTEIN ANTIBODY; RNA BINDING PROTEIN; RNA BINDING PROTEIN 6; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; DROSOPHILA; GENE; GENE DELETION; GERM LINE; INSECT GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PROTEIN ANALYSIS; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RBP6 GENE; REGULATORY MECHANISM; RNA SPLICING; SPERMATOCYTE; SPERMATOGENESIS; STEM CELL;

ANIMALS; CELL DEATH; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE ORDER; GERM CELLS; JUVENILE HORMONES; ORGAN SPECIFICITY; PROTEIN BINDING; RNA-BINDING PROTEINS; SEQUENCE DELETION; SPERMATOGENESIS; STEM CELLS; VERTEBRATES;

VERTEBRATA;

EID: 84870283780     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049810     Document Type: Article

References (52)

1. Spradling A, Fuller MT, Braun RE, Yoshida S, (2011) Germline stem cells. Cold Spring Harbor perspectives in biology 3: a002642.
2. Harris RE, Ashe HL, (2011) Cease and desist: modulating short-range Dpp signalling in the stem-cell niche. EMBO reports 12: 519-526.
3. Callan MA, Zarnescu DC, (2011) Heads-up: new roles for the fragile × mental retardation protein in neural stem and progenitor cells. Genesis 49: 424-440.
4. Walker E, Manias JL, Chang WY, Stanford WL, (2011) PCL2 modulates gene regulatory networks controlling self-renewal and commitment in embryonic stem cells. Cell cycle 10: 45-51.
5. Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, et al. (2005) Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res 306: 349-356.
6. Nakamura M, Okano H, Blendy JA, Montell C, (1994) Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13: 67-81.
7. Okabe M, Imai T, Kurusu M, Hiromi Y, Okano H, (2001) Translational repression determines a neuronal potential in Drosophila asymmetric cell division. Nature 411: 94-98.
8. Hirota Y, Okabe M, Imai T, Kurusu M, Yamamoto A, et al. (1999) Musashi and seven in absentia downregulate Tramtrack through distinct mechanisms in Drosophila eye development. Mech Dev 87: 93-101.
9. Siddall NA, Hime GR, Pollock JA, Batterham P, (2009) Ttk69-dependent repression of lozenge prevents the ectopic development of R7 cells in the Drosophila larval eye disc. BMC Dev Biol 9: 64.
10. Siddall NA, McLaughlin EA, Marriner NL, Hime GR, (2006) The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proc Natl Acad Sci U S A 103: 8402-8407.
11. Akindahunsi AA, Bandiera A, Manzini G, (2005) Vertebrate 2xRBD hnRNP proteins: a comparative analysis of genome, mRNA and protein sequences. Comput Biol Chem 29: 13-23.
12. Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, et al. (2000) Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22: 139-153.
13. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, et al. (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176: 230-242.
14. Sakakibara S, Nakamura Y, Satoh H, Okano H, (2001) Rna-binding protein Musashi2: developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci 21: 8091-8107.
15. Sakakibara S, Nakamura Y, Yoshida T, Shibata S, Koike M, et al. (2002) RNA-binding protein Musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci U S A 99: 15194-15199.
16. Hitoshi S, Alexson T, Tropepe V, Donoviel D, Elia AJ, et al. (2002) Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev 16: 846-858.
17. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, et al. (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007.
18. Nishimura S, Wakabayashi N, Toyoda K, Kashima K, Mitsufuji S, (2003) Expression of Musashi-1 in human normal colon crypt cells: a possible stem cell marker of human colon epithelium. Dig Dis Sci 48: 1523-1529.
19. Potten CS, Booth C, Tudor GL, Booth D, Brady G, et al. (2003) Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 71: 28-41.
20. Akasaka Y, Saikawa Y, Fujita K, Kubota T, Ishikawa Y, et al. (2005) Expression of a candidate marker for progenitor cells, Musashi-1, in the proliferative regions of human antrum and its decreased expression in intestinal metaplasia. Histopathology 47: 348-356.
21. Clarke RB, Spence K, Anderson E, Howell A, Okano H, et al. (2005) A putative human breast stem cell population is enriched for steroid receptor-positive cells. Dev Biol 277: 443-456.
22. Sugiyama-Nakagiri Y, Akiyama M, Shibata S, Okano H, Shimizu H, (2006) Expression of RNA-binding protein Musashi in hair follicle development and hair cycle progression. Am J Pathol 168: 80-92.
23. Sureban SM, May R, George RJ, Dieckgraefe BK, McLeod HL, et al. (2008) Knockdown of RNA binding protein musashi-1 leads to tumor regression in vivo. Gastroenterology 134: 1448-1458.
24. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, et al. (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci U S A 100: 15178-15183.
25. Yokota N, Mainprize TG, Taylor MD, Kohata T, Loreto M, et al. (2004) Identification of differentially expressed and developmentally regulated genes in medulloblastoma using suppression subtraction hybridization. Oncogene 23: 3444-3453.
26. Gotte M, Wolf M, Staebler A, Buchweitz O, Kelsch R, et al. (2008) Increased expression of the adult stem cell marker Musashi-1 in endometriosis and endometrial carcinoma. J Pathol 215: 317-329.
27. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611.
28. Hope KJ, Sauvageau G, (2011) Roles for MSI2 and PROX1 in hematopoietic stem cell activity. Current opinion in hematology 18: 203-207.
29. Wuebben EL, Mallanna SK, Cox JL, Rizzino A, (2012) Musashi2 is required for the self-renewal and pluripotency of embryonic stem cells. PloS one 7: e34827.
30. Van Doren M, Williamson AL, Lehmann R, (1998) Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol 8: 243-246.
31. Parks AL, Cook KR, Belvin M, Dompe NA, Fawcett R, et al. (2004) Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome. Nature genetics 36: 288-292.
32. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
33. Rubin GM, Spradling AC, (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218: 348-353.
34. Tautz D, Pfeifle C, (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98: 81-85.
35. Bunt SM, Hime GR, (2004) Ectopic activation of Dpp signalling in the male Drosophila germline inhibits germ cell differentiation. Genesis 39: 84-93.
36. McCall K, Baum JS, Cullen K, Peterson JS, (2004) Visualizing apoptosis. Methods in molecular biology 247: 431-442.
37. Ruan J, Li H, Chen Z, Coghlan A, Coin LJ, et al. (2008) TreeFam: 2008 Update. Nucleic Acids Res 36: D735-740.
38. Maris C, Dominguez C, Allain FH, (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272: 2118-2131.
39. Ito T, Kwon HY, Zimdahl B, Congdon KL, Blum J, et al. (2010) Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 466: 765-768.
40. Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, et al. (2001) The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Molecular and cellular biology 21: 3888-3900.
41. Hardy RW, Tokuyasu KT, Lindsley DL, Garavito M, (1979) The germinal proliferation center in the testis of Drosophila melanogaster. J Ultrastruct Res 69: 180-190.
42. Fuller M (1993) Spermatogenesis. In: Bate M, Martinez-Arias A, editors. The Development of Drosophila Melanogaster. New York: Cold Spring Harbor Laboratory Press. 71-147.
43. Hime GR, Brill JA, Fuller MT, (1996) Assembly of ring canals in the male germ line from structural components of the contractile ring. Journal of cell science 109 (Pt 12): 2779-2788.
44. Leatherman JL, Dinardo S, (2008) Zfh-1 controls somatic stem cell self-renewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 3: 44-54.
45. Nakano A, Kanemura Y, Mori K, Kodama E, Yamamoto A, et al. (2007) Expression of the Neural RNA-binding protein Musashi1 in pediatric brain tumors. Pediatr Neurosurg 43: 279-284.
46. Schulenburg A, Cech P, Herbacek I, Marian B, Wrba F, et al. (2007) CD44-positive colorectal adenoma cells express the potential stem cell markers musashi antigen (msi1) and ephrin B2 receptor (EphB2). J Pathol 213: 152-160.
47. Toda M, Iizuka Y, Yu W, Imai T, Ikeda E, et al. (2001) Expression of the neural RNA-binding protein Musashi1 in human gliomas. Glia 34: 1-7.
48. Kharas MG, Lengner CJ, Al-Shahrour F, Bullinger L, Ball B, et al. (2010) Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nature medicine 16: 903-908.
49. Schierwater B, (2005) My favorite animal, Trichoplax adhaerens. Bioessays 27: 1294-1302.
50. Jakob W, Sagasser S, Dellaporta S, Holland P, Kuhn K, et al. (2004) The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary. Dev Genes Evol 214: 170-175.
51. Djiane A, Mlodzik M, (2010) The Drosophila GIPC homologue can modulate myosin based processes and planar cell polarity but is not essential for development. PloS one 5: e11228.
52. Myster SH, Cavallo R, Anderson CT, Fox DT, Peifer M, (2003) Drosophila p120catenin plays a supporting role in cell adhesion but is not an essential adherens junction component. The Journal of cell biology 160: 433-449.