Orbit/CLASP Is Required for Germline Cyst Formation through Its Developmental Control of Fusomes and Ring Canals in Drosophila Males

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Miyauchi, Chie ^a   Kitazawa, Daishi ^a   Ando, Itaru ^a   Hayashi, Daisuke ^a   Inoue, Yoshihiro H ^a  

^a KYOTO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; INSECT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; PROTEIN CLASP; ROTEIN ORBIT; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPOSITION; CELL ELONGATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CENTROMERE; CENTROSOME; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; DEPOLYMERIZATION; DROSOPHILA; ENZYME ACTIVITY; FEMALE; FUSOME; GERM LINE; MALE; MICROTUBULE; MITOSIS; NONHUMAN; PROTEIN FUNCTION; SPERMATOGENESIS; SPERMATOGONIUM; STEM CELL;

ACTINS; ANIMALS; CENTROSOME; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; SPERMATOGONIA; STEM CELLS;

EID: 84874763533     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058220     Document Type: Article

References (53)

1. de Cuevas M, Lilly MA, Spradling AC, (1997) Germline cyst formation in Drosophila. Annu Rev Genet 31: 405-428.
2. Pepling ME, de Cuevas M, Spradling AC, (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9: 257-262.
3. Fulle MT (1993) Spermatogenesis. In The Development of Drosophila, (M. Martinez-Arias and M. Bate, eds.) Cold Spring Harbor Press, Cold Spring Harbor, New York. 71-147.
4. Inoue YH, Miyauchi C, Ogata T, Kitazawa D (2012) Dynamic alteration of cellular component of male meiosis in Drosophila. In Meiosis, (A. Swan, eds.) InTech, Open Access Publisher. ISBN 979-953-307-212-7.
5. Kiger AA, Jones DL, Schulz C, Rogers MB, Fuller MT, (2001) Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294: 2542-2545.
6. Fuller MT, Spradling A, (2007) Male and Female Drosophila Germline Stem Cells: Two Versions of Immortality. Science 316: 402-404.
7. Hime GR, Brill JA, Fuller MT, (1996) Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci 109: 2779-2788.
8. Spradling AC (1993) Developmental genetics of oogenesis. In The Development of Drosophila, (M. Martinez-Arias and M. Bate, eds.) Cold Spring Harbor Press, Cold Spring Harbor, New York. 1-70.
9. Robinson DN, Cooley L, (1994) Morphogenesis of Drosophila ovarian ring canals. Development 120: 2015-2025.
10. Tilney LG, Tilney MS, Guild GM, (1996) Formation of actin filament bundles in the ring canals of developing Drosophila follicles. J Cell Biol 133: 61-74.
11. Xue F, Cooley L, (1993) kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72: 681-693.
12. Li MG, Serr M, Edwards K, Ludmann S, Yamamoto D, et al. (1999) Filamin is required for ring canal assembly and actin organization during Drosophila oogenesis. J Cell Biol 146: 1061-1074.
13. Mathe E, Inoue YH, Palframan W, Brown G, Glover DM, (2003) Orbit/Mast, the CLASP orthologue of Drosophila, is required for asymmetric stem cell and cystocyte divisions and development of the polarised microtubule network that interconnects oocyte and nurse cells during oogenesis. Development 130: 901-915.
14. Yue L, Spradling AC, (1992) hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis encodes a homolog of adducing. Genes Dev 6: 2443-2454.
15. Field CM, Alberts BM, (1995) Anillin, a contractile ring protein that cycles from the nucleus to the cell cortex. J Cell Biol 131: 165-178.
16. Carmena M, Riparbelli MG, Minestrini G, Tavares AM, Adams R, et al. (1998) Drosophila polo kinase is required for cytokinesis. J Cell Biol 143: 659-671.
17. Montembault E, Zhang W, Przewloka MR, Archambault V, Sevin EW, et al. (2010) Nessun Dorma, a novel centralspindlin partner, is required for cytokinesis in Drosophila spermatocytes. J Cell Biol 191: 1351-1365.
18. Huyuh JR, St. Johnston D, (2004) The origin of asymmetry: early polarization of the Drosophila germline cyst and oocyte. Curr Biol 14: R438-R449.
19. Lin H, Yue L, Spradling AC, (1994) The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120: 947-956.
20. Deng W, Lin H, (1997) Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev Biol 189: 79-94.
21. Röper K, Brown NH, (2004) A spectraplakin is enriched on the fusome and organizes microtubules during oocyte specification in Drosophila. Curr Biol 14: 99-110.
22. de Cuevas M, Lee JK, Spradling AC, (1996) alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122: 3959-3968.
23. Petrella LN, Smith-Leiker T, Cooley L, (2007) The Ovhts polyprotein is cleaved to produce fusome and ring canal protein required for Drosophila oogenesis. Development 134: 703-712.
24. Snapp EL, Iida T, Frescas D, Lippincott-Schwartz J, Lilly MA, (2004) The fusome mediates intercellular endoplasmic reticulum connectivity in Drosophila ovarian cysts. Mol Biol Cell 15: 4512-4521.
25. Röper K, (2007) Rtnl1 is enriched in a specialized germline ER that associates with ribonucleoprotein granule components. J Cell Sci 120: 1081-1092.
26. Lighthouse DV, Buszczak M, Spradling AC, (2008) New components of the Drosophila fusome suggest it plays novel roles in signaling and transport. Dev Biol 317: 59-71.
27. Bogard N, Lan L, Xu J, Cohen RS, (2007) Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development 134: 3413-3418.
28. McGrail M, Hays TS, (1997) The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124: 2409-2419.
29. Wilson PG, (1999) Centrosome inheritance in the male germ line of Drosophila requires hu-li tai-shao function. Curr Biol 9: 923-926.
30. Liu Z, Xie T, Steward R, (1999) Lis1, the Drosophila homolog of human lissencephaly disease gene, is required for germline cell division and oocyte differentiation. Development 126: 4477-4488.
31. Grieder NC, de Cuevas M, Spradling AC, (2000) The fusome organizes the microtubule network during oocyte differentiation in Drosophila. Development 127: 4253-4264.
32. Tates AD (1971) Cytodifferentiation during spermatogenesis in Drosophila melanogaster: An electron microscope study. Ph.D. thesis. Rijksuniversiteit, Leiden, The Netherlands.
33. Inaba M, Yuan H, Salzmann V, Fuller MT, Yamashita YM, (2010) E-cadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells. PLoS One 5: e12473.
34. Yuan H, Chiang CY, Cheng J, Salzman V, Yamashita YM, (2012) Regulation of cyclin localization downstream of Par-1 function is critical for the centrosome orientation checkpoint in Drosophila male germline stem cells. Dev Biol 361: 57-67.
35. Inoue YH, do Carmo Avides M, Shiraki M, Deak P, et al. (2000) Orbit, a novel microtubule associated protein essential for mitosis in Drosophila melanogaster. J Cell Biol 149: 153-166.
36. Lemos CL, Sampaio P, Maiato H, Costa M, Omel'yanchuk LV, et al. (2000) Mast, a conserved microtubule-associated protein required for bipolar mitotic spindle organization. EMBO J 19: 3668-3682.
37. Maiato H, Sampaio P, Lemos CL, Findlay J, Carmena M, et al. (2002) Mast/Orbit has a role in microtubule-kinetochore attachment and is essential for chromosome alignment and maintenance of spindle bipolarity. J Cell Biol 157: 749-760.
38. Maiato H, Fairley EAF, Rieder CL, Swedlow JR, Sunkel CE, et al. (2003) Human CLASP1 is an outer kinetochore component that regulates spindle microtubule dynamics. Cell 113: 891-904.
39. Akhmanova A, Hoogenraad CC, Drabek K, Stepanova T, Dortland B, et al. (2001) CLASPs are CLIP-115 and-170 associating proteins involved in the regional regulation of microtubule dynamics in motile fibroblasts. Cell 104: 923-935.
40. Aonuma M, Miyamoto M, Inoue YH, Tamai K, Sakai H, et al. (2005) Microtubule bundle formation and cell death induced by the human CLASP/Orbit N-terminal fragment. Cell Struct Funct 30: 7-13.
41. Inoue YH, Savoian M, Suzuki T, Yamamoto M, Glover DM, (2004) Mutation in orbit/mast, reveal that the central spindle is comprised of two microtubule populations; those that initiate cleavage and those that propagate furrow ingression. J Cell Biol 116: 1-12.
42. Giansanti MG, Bonaccorsi S, Williams B, Williams EV, Santolamazza C, et al. (1998) Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev 12: 396-410.
43. Andrade MA, Bork P, (1995) HEAT repeats in the Huntington's disease protein. Nat Genet 11: 115-116.
44. Tsvetkov AS, Samsonov A, Akhmanova A, Galiart N, Popov SV, (2007) Microtubule-binding protein CLASP1 and CLASP2 interact with actin filament. Cell Motil Cytoskeleton 64: 519-530.
45. Lee KS, Yoon J, Park JS, Kang YK, (2010) Drosophila G9a is implicated in germ cell development. Insect Mol Biol 19: 131-139.
46. Deng H, Lee JK, Goldstein LSB, Branton D, (1995) Drosophila development requires spectrin network formation. J Cell Biol 128: 71-79.
47. Pielage J, Fetter RD, Davis GW, (2006) A postsynaptic spectrin scaffold defines active zone size, spacing and efficacy at the Drosophila neuromuscular junction. J Cell Biol 175: 491-503.
48. Robinson DN, Cooley L, (1997) Drosophila kelch is an oligomeric ring canal actin organizer. J Cell Biol 138: 799-810.
49. Goldbach P, Wong R, Beise N, Sarpal R, Trimble WS, et al. (2010) Stabilization of the actomyosin ring enables spermatocyte cytokinesis in Drosophila. Mol Biol Cell 21: 1482-1493.
50. Kitazawa D, Yamaguchi M, Mori H, Inoue YH (2012) COPI-mediated membrane trafficking is required for cytokinesis in Drosophila male meiotic divisions. J Cell Sci in press. doi: 10.1242/jcs.103317.
51. Yamashita YM, Yuan H, Cheng J, Hunt AJ, (2010) Polarity in stem cell division: asymmetric stem cell division in tissue homeostasis. Cold Spring Harb Perspect Biol 2: a001313.
52. Yamashita YM, Jones DL, Fuller MT, (2003) Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301: 1547-1550.
53. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT, (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315: 518-521.