Distribution and association of mTOR with its cofactors, raptor and rictor, in cumulus cells and oocytes during meiotic maturation in mice

Molecular Reproduction and Development

Volumn 80, Issue 4, 2013, Pages 334-348

  Kogasaka, Yuhei ^a   Hoshino, Yumi ^a   Hiradate, Yuuki ^a   Tanemura, Kentaro ^a   Sato, Eimei ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Actin; Centrosome, midbody; GVBD; MTOCs; Spindle

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIVISION; CHROMOSOME; CONTROLLED STUDY; CUMULUS CELL; CYTOPLASM; ENZYME PHOSPHORYLATION; IMMUNOLOCALIZATION; MEIOSIS; MITOSIS; MOUSE; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; RAPTOR; SPATIOTEMPORAL ANALYSIS; SPINDLE CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARRIER PROTEINS; CHROMOSOMES, MAMMALIAN; CUMULUS CELLS; FEMALE; MEIOSIS; MICE; MICE, INBRED ICR; MITOTIC SPINDLE APPARATUS; MULTIPROTEIN COMPLEXES; OOCYTES; TOR SERINE-THREONINE KINASES;

MAMMALIA; MUS; RAPTORES;

EID: 84876407556     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22166     Document Type: Article

References (76)

1. Alessi DR, Pearce LR, Garcia-Martinez JM. 2009. New insights into mTOR signaling: mTORC2 and beyond. Sci Signal 2:pe27.
2. Altomare DA, Wang HQ, Skele KL, De Rienzo A, Klein-Szanto AJ, Godwin AK, Testa JR. 2004. AKT and mTOR phosphorylation is frequently detected in ovarian cancer and can be targeted to disrupt ovarian tumor cell growth. Oncogene 23:5853-5857.
3. Astrinidis A, Senapedis W, Henske EP. 2006. Hamartin, the tuberous sclerosis complex 1 gene product, interacts with polo-like kinase 1 in a phosphorylation-dependent manner. Hum Mol Genet 15:287-297.
4. Astrinidis A, Kim J, Kelly CM, Olofsson BA, Torabi B, Sorokina EM, Azizkhan-Clifford J. 2010. The transcription factor SP1 regulates centriole function and chromosomal stability through a functional interaction with the mammalian target of rapamycin/raptor complex. Genes Chromosomes Cancer 49:282-297.
5. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, Verlhac MH. 2008. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 18:1514-1519.
6. Azoury J, Lee KW, Georget V, Hikal P, Verlhac MH. 2011. Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development 138:2903-2908.
7. Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J. 2002. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108:83-96.
8. Bhaskar PT, Hay N. 2007. The two TORCs and Akt. Dev Cell 12:487-502.
9. Bonatti S, Simili M, Galli A, Bagnato P, Pigullo S, Schiestl RH, Abbondandolo A. 1998. Inhibition of the Mr 70, 000 S6 kinase pathway by rapamycin results in chromosome malsegregation in yeast and mammalian cells. Chromosoma 107:498-506.
10. Bonatti S, Simili M, Benedetti PA, Morandi F, Menichini P, Del Carratore R, Barale R, Abbondandolo A. 2005. Altered centrosomes in ataxia-telangiectasia cells and rapamycin-treated Chinese hamster cells. Environ Mol Mutagen 46:164-173.
11. Brunet S, Maria AS, Guillaud P, Dujardin D, Kubiak JZ, Maro B. 1999. Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 146:1-12.
12. Byskov AG, Andersen CY, Nordholm L, Thogersen H, Xia G, Wassmann O, Andersen JV, Guddal E, Roed T. 1995. Chemical structure of sterols that activate oocyte meiosis. Nature 374:559-562.
13. Cha H, Wang X, Li H, Fornace AJ, Jr. 2007. A functional role for p38 MAPK in modulating mitotic transit in the absence of stress. J Biol Chem 282:22984-22992.
14. Choi JH, Adames NR, Chan TF, Zeng C, Cooper JA, Zheng XF. 2000. TOR signaling regulates microtubule structure and function. Curr Biol 10:861-864.
15. Choi JH, Bertram PG, Drenan R, Carvalho J, Zhou HH, Zheng XF. 2002. The FKBP12-rapamycin-associated protein (FRAP) is a CLIP-170 kinase. EMBO Rep 3:988-994.
16. Conti M, Hsieh M, Park JY, Su YQ. 2006. Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol 20:715-723.
17. Cybulski N, Hall MN. 2009. TOR complex 2: A signaling pathway of its own. Trends Biochem Sci 34:620-627.
18. Delaval B, Letard S, Lelievre H, Chevrier V, Daviet L, Dubreuil P, Birnbaum D. 2005. Oncogenic tyrosine kinase of malignant hemopathy targets the centrosome. Cancer Res 65:7231-7240.
19. Doghman M, El-Wakil A, Cardinaud B, Thomas E, Wang J, Zhao W, Peralta-Del Valle MH, Figueiredo BC, Zambetti GP, Lalli E. 2010. Regulation of insulin-like growth factor-mammalian target of rapamycin signaling by microRNA in childhood adrenocortical tumors. Cancer Res 70:4666-4675.
20. Downs SM, Ya R, Davis CC. 2010. Role of AMPK throughout meiotic maturation in the mouse oocyte: Evidence for promotion of polar body formation and suppression of premature activation. Mol Reprod Dev 77:888-899.
21. Dujardin D, Wacker UI, Moreau A, Schroer TA, Rickard JE, De Mey JR. 1998. Evidence for a role of CLIP-170 in the establishment of metaphase chromosome alignment. J Cell Biol 141:849-862.
22. Dunlop EA, Tee AR. 2009. Mammalian target of rapamycin complex 1: Signalling inputs, substrates and feedback mechanisms. Cell Signal 21:827-835.
23. Fingar DC, Blenis J. 2004. Target of rapamycin (TOR): An integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23:3151-3171.
24. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J. 2002. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 16:1472-1487.
25. Fingar DC, Richardson CJ, Tee AR, Cheatham L, Tsou C, Blenis J. 2004. mTOR controls cell cycle progression through its cell growth effectors S6K1 and 4E-BP1/eukaryotic translation initiation factor 4E. Mol Cell Biol 24:200-216.
26. Foster KG, Fingar DC. 2010. Mammalian target of rapamycin (mTOR): Conducting the cellular signaling symphony. J Biol Chem 285:14071-14077.
27. Foster KG, Acosta-Jaquez HA, Romeo Y, Ekim B, Soliman GA, Carriere A, Roux PP, Ballif BA, Fingar DC. 2010. Regulation of mTOR complex 1 (mTORC1) by raptor Ser863 and multisite phosphorylation. J Biol Chem 285:80-94.
28. Freudzon L, Norris RP, Hand AR, Tanaka S, Saeki Y, Jones TL, Rasenick MM, Berlot CH, Mehlmann LM, Jaffe LA. 2005. Regulation of meiotic prophase arrest in mouse oocytes by GPR3, a constitutive activator of the Gs G protein. J Cell Biol 171:255-265.
29. Gomez-Baldo L, Schmidt S, Maxwell CA, Bonifaci N, Gabaldon T, Vidalain PO, Senapedis W, Kletke A, Rosing M, Barnekow A, Rottapel R, Capella G, Vidal M, Astrinidis A, Piekorz RP, Pujana MA. 2010. TACC3-TSC2 maintains nuclear envelope structure and controls cell division. Cell Cycle 9:1143-1155.
30. Gonczy P. 2008. Mechanisms of asymmetric cell division: Flies and worms pave the way. Nat Rev 9:355-366.
31. Gui Y, He GH, Walsh MP, Zheng XL. 2007. Predisposition to tetraploidy in pulmonary vascular smooth muscle cells derived from the Eker rats. Am J Physiol 293:L702-L711.
32. Gwinn DM, Asara JM, Shaw RJ. 2010. Raptor is phosphorylated by cdc2 during mitosis. PLoS ONE 5:e9197.
33. Hashimoto S, Saeki K, Nagao Y, Minami N, Yamada M, Utsumi K. 1998. Effects of cumulus cell density during in vitro maturation of the developmental competence of bovine oocytes. Theriogenology 49:1451-1463.
34. Hernandez-Gonzalez I, Gonzalez-Robayna I, Shimada M, Wayne CM, Ochsner SA, White L, Richards JS. 2006. Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: Does this expand their role in the ovulation process? Mol Endocrinol 20:1300-1321.
35. Hoshino Y, Sato E. 2008. Protein kinase B (PKB/Akt) is required for the completion of meiosis in mouse oocytes. Dev Biol 314:215-223.
36. Hoshino Y, Yokoo M, Yoshida N, Sasada H, Matsumoto H, Sato E. 2004. Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol Reprod Dev 69:77-86.
37. Inoue A, Akiyama T, Nagata M, Aoki F. 2007. The perivitelline space-forming capacity of mouse oocytes is associated with meiotic competence. J Reprod Dev 53:1043-1052.
38. Jacinto E, Lorberg A. 2008. TOR regulation of AGC kinases in yeast and mammals. Biochem J 410:19-37.
39. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN. 2004. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6:1122-1128.
40. Kalous J, Solc P, Baran V, Kubelka M, Schultz RM, Motlik J. 2006. PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol Cell 98:111-123.
41. Kapeller R, Toker A, Cantley LC, Carpenter CL. 1995. Phosphoinositide 3-kinase binds constitutively to alpha/beta-tubulin and binds to gamma-tubulin in response to insulin. J Biol Chem 270:25985-25991.
42. Kim DH, Sabatini DM. 2004. Raptor and mTOR: Subunits of a nutrient-sensitive complex. Curr Top Microbiol Immunol 279:259-270.
43. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163-175.
44. Laplante M, Sabatini DM. 2009. mTOR signaling at a glance. J Cell Sci 122:3589-3594.
45. Lawrence JC, Lin TA, McMahon LP, Choi KM. 2004. Modulation of the protein kinase activity of mTOR. Curr Top Microbiol Immunol 279:199-213.
46. Lee SE, Sun SC, Choi HY, Uhm SJ, Kim NH. 2012. mTOR is required for asymmetric division through small GTPases in mouse oocytes. Mol Reprod Dev 79:356-366.
47. Leibfried-Rutledge ML, Critser ES, Parrish JJ, First NL. 1989. In vitro maturation and fertilization of bovine oocytes. Theriogenology 31:61-74.
48. Longo FJ, Chen DY. 1985. Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus. Dev Biol 107:382-394.
49. Lopez-Bonet E, Vazquez-Martin A, Perez-Martinez MC, Oliveras-Ferraros C, Perez-Bueno F, Bernado L, Menendez JA. 2010. Serine 2481-autophosphorylation of mammalian target of rapamycin (mTOR) couples with chromosome condensation and segregation during mitosis: Confocal microscopy characterization and immunohistochemical validation of PP-mTOR(Ser2481) as a novel high-contrast mitosis marker in breast cancer core biopsies. Int J Oncol 36:107-115.
50. Manandhar G, Schatten H, Sutovsky P. 2005. Centrosome reduction during gametogenesis and its significance. Biol Reprod 72:2-13.
51. Ramirez-Valle F, Badura ML, Braunstein S, Narasimhan M, Schneider RJ. 2010. Mitotic raptor promotes mTORC1 activity, G(2)/M cell cycle progression, and internal ribosome entry site-mediated mRNA translation. Mol Cell Biol 30:3151-3164.
52. Rickard JE, Kreis TE. 1990. Identification of a novel nucleotide-sensitive microtubule-binding protein in HeLa cells. J Cell Biol 110:1623-1633.
53. Rossi R, Pester JM, McDowell M, Soza S, Montecucco A, Lee-Fruman KK. 2007. Identification of S6K2 as a centrosome-located kinase. FEBS Lett 581:4058-4064.
54. Ruvinsky I, Meyuhas O. 2006. Ribosomal protein S6 phosphorylation: From protein synthesis to cell size. Trends Biochem Sci 31:342-348.
55. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14:1296-1302.
56. Schalm SS, Fingar DC, Sabatini DM, Blenis J. 2003. TOS motif-mediated raptor binding regulates 4E-BP1 multisite phosphorylation and function. Curr Biol 13:797-806.
57. Schatten H, Sun QY. 2009. The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 50:620-636.
58. Schuetz AW, Whittingham DG, Snowden R. 1996. Alterations in the cell cycle of mouse cumulus granulosa cells during expansion and mucification in vivo and in vitro. Reprod Fertil Dev 8:935-943.
59. Schuh M, Ellenberg J. 2007. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484-498.
60. Solc P, Schultz RM, Motlik J. 2010. Prophase I arrest and progression to metaphase I in mouse oocytes: Comparison of resumption of meiosis and recovery from G2-arrest in somatic cells. Mol Hum Reprod 16:654-664.
61. Szollosi D, Calarco P, Donahue RP. 1972. Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci 11:521-541.
62. van Duijnhoven MW, Hagenberg R, Pasch MC, van Erp PE, van de Kerkhof PC. 2005. Novel quantitative immunofluorescent technique reveals improvements in epidermal cell populations after mild treatment of psoriasis. Acta Derm Venereol 85:311-317.
63. Vazquez-Martin A, Oliveras-Ferraros C, Bernado L, Lopez-Bonet E, Menendez JA. 2009a. The serine 2481-autophosphorylated form of mammalian target of rapamycin (mTOR) is localized to midzone and midbody in dividing cancer cells. Biochem Biophys Res Commun 380:638-643.
64. Vazquez-Martin A, Oliveras-Ferraros C, Menendez JA. 2009b. The active form of the metabolic sensor: AMP-activated protein kinase (AMPK) directly binds the mitotic apparatus and travels from centrosomes to the spindle midzone during mitosis and cytokinesis. Cell Cycle 8:2385-2398.
65. Vazquez-Martin A, Cufi S, Oliveras-Ferraros C, Menendez JA. 2011. Raptor, a positive regulatory subunit of mTOR complex 1, is a novel phosphoprotein of the rDNA transcription machinery in nucleoli and chromosomal nucleolus organizer regions (NORs). Cell Cycle 10:3140-3152.
66. Vazquez-Martin A, Sauri-Nadal T, Menendez OJ, Oliveras-Ferraros C, Cufi S, Corominas-Faja B, Lopez-Bonet E, Menendez JA. 2012. Ser2481-autophosphorylated mTOR colocalizes with chromosomal passenger proteins during mammalian cell cytokinesis. Cell Cycle 11:4211-4221.
67. Verlhac MH, de Pennart H, Maro B, Cobb MH, Clarke HJ. 1993. MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158:330-340.
68. Verlhac MH, Lefebvre C, Guillaud P, Rassinier P, Maro B. 2000. Asymmetric division in mouse oocytes: With or without Mos. Curr Biol 10:1303-1306.
69. Wakefield JG, Stephens DJ, Tavare JM. 2003. A role for glycogen synthase kinase-3 in mitotic spindle dynamics and chromosome alignment. J Cell Sci 116:637-646.
70. Wang L, Lawrence JC Jr, Sturgill TW, Harris TE. 2009. Mammalian target of rapamycin complex 1 (mTORC1) activity is associated with phosphorylation of raptor by mTOR. J Biol Chem 284:14693-14697.
71. Wullschleger S, Loewith R, Oppliger W, Hall MN. 2005. Molecular organization of target of rapamycin complex 2. J Biol Chem 280:30697-30704.
72. Yaba A, Bianchi V, Borini A, Johnson J. 2008. A putative mitotic checkpoint dependent on mTOR function controls cell proliferation and survival in ovarian granulosa cells. Reprod Sci 15:128-138.
73. Yan-Chang WEI, Cai-Rong Y. 2009. The expression and effect of mTOR during mouse oocyte maturation. Prog Biochem Biophys 36:1334.
74. Yonezawa K, Yoshino KI, Tokunaga C, Hara K. 2004. Kinase activities associated with mTOR. Curr Top Microbiol Immunol 279:271-282.
75. Yu J, Yaba A, Kasiman C, Thomson T, Johnson J. 2011. mTOR controls ovarian follicle growth by regulating granulosa cell proliferation. PLoS ONE 6:e21415.
76. Yu J, Thomson TC, Johnson J. 2012. Cross talk between estradiol and mTOR kinase in the regulation of ovarian granulosa proliferation. Reprod Sci 19:143-151.