The SUN Protein Mps3 Is Required for Spindle Pole Body Insertion into the Nuclear Membrane and Nuclear Envelope Homeostasis

1. Strambio-De-CastilliaCNiepelMRoutMP 2010 The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11 490 501

2. ByersBGoetschL 1975 Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae. J Bacteriol 124 511 523

3. JaspersenSLWineyM 2004 The budding yeast spindle pole body: structure, duplication, and function. Annu Rev Cell Dev Biol 20 1 28

4. ChialHJRoutMPGiddingsTHWineyM 1998 Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies. J Cell Biol 143 1789 1800

5. LauCKGiddingsTHJrWineyM 2004 A novel allele of Saccharomyces cerevisiae NDC1 reveals a potential role for the spindle pole body component Ndc1p in nuclear pore assembly. Eukaryotic Cell 3 447 458

6. OnischenkoEStantonLHMadridASKieselbachTWeisK 2009 Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J Cell Biol 185 475 491

7. MakioTStantonLHLinCCGoldfarbDSWeisK 2009 The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J Cell Biol 185 459 473

8. ChadrinAHessBSan RomanMGattiXLombardB 2010 Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. The Journal of Cell Biology 189 795 811

9. WineyMGoetschLBaumPByersB 1991 MPS1 and MPS2: novel yeast genes defining distinct steps of spindle pole body duplication. J Cell Biol 114 745 754

10. ArakiYLauCKMaekawaHJaspersenSLGiddingsTHJr 2006 The Saccharomyces cerevisiae spindle pole body (SPB) component Nbp1p is required for SPB membrane insertion and interacts with the integral membrane proteins Ndc1p and Mps2p. Mol Biol Cell 17 1959 1970

11. SchrammCElliottSShevchenkoASchiebelE 2000 The Bbp1p-Mps2p complex connects the SPB to the nuclear envelope and is essential for SPB duplication. Embo J 19 421 433

12. KupkeTDi CeccoLMullerHMNeunerAAdolfF 2011 Targeting of Nbp1 to the inner nuclear membrane is essential for spindle pole body duplication. EMBO J 30 3337 3352

13. DrinGCasellaJFGautierRBoehmerTSchwartzTU 2007 A general amphipathic alpha-helical motif for sensing membrane curvature. Nature Struct Mol Biol 14 138 146

14. AlberFDokudovskayaSVeenhoffLMZhangWKipperJ 2007 Determining the architectures of macromolecular assemblies. Nature 450 683 694

15. AlberFDokudovskayaSVeenhoffLMZhangWKipperJ 2007 The molecular architecture of the nuclear pore complex. Nature 450 695 701

16. DrinGAntonnyB 2010 Amphipathic helices and membrane curvature. FEBS Letters 584 1840 1847

17. DoucetCMTalamasJAHetzerMW 2010 Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 141 1030 1041

18. DawsonTRLazarusMDHetzerMWWenteSR 2009 ER membrane-bending proteins are necessary for de novo nuclear pore formation. J Cell Biol 184 659 675

19. SchneiterRHitomiMIvessaASFaschEVKohlweinSD 1996 A yeast acetyl coenzyme A carboxylase mutant links very-long-chain fatty acid synthesis to the structure and function of the nuclear membrane-pore complex. Mol Cell Biol 16 7161 7172

20. ScarcelliJJHodgeCAColeCN 2007 The yeast integral membrane protein Apq12 potentially links membrane dynamics to assembly of nuclear pore complexes. J Cell Biol 178 799 812

21. HodgeCAChoudharyVWolyniakMJScarcelliJJSchneiterR 2010 Integral membrane proteins Brr6 and Apq12 link assembly of the nuclear pore complex to lipid homeostasis in the endoplasmic reticulum. J Cell Sci 123 141 151

22. LiuQPanteNMisteliTElsaggaMCrispM 2007 Functional association of Sun1 with nuclear pore complexes. J Cell Biol 178 785 798

23. LuWGotzmannJSironiLJaegerVMSchneiderM 2008 Sun1 forms immobile macromolecular assemblies at the nuclear envelope. Biochim Biophys Acta 1783 2415 2426

24. TalamasJAHetzerMW 2011 POM121 and Sun1 play a role in early steps of interphase NPC assembly. J Cell Biol 194 27 37

25. SezenBSeedorfMSchiebelE 2009 The SESA network links duplication of the yeast centrosome with the protein translation machinery. Genes Dev 23 1559 1570

26. WitkinKLFriederichsJMCohen-FixOJaspersenSL 2010 Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 186 867 883

27. GreenlandKBDingHCostanzoMBooneCDavisTN 2010 Identification of Saccharomyces cerevisiae spindle pole body remodeling factors. PLoS ONE 5 e15426 doi:10.1371/journal.pone.0015426

28. GardnerJMSmoyerCJStensrudESAlexanderRGogolM 2011 Targeting of the SUN protein Mps3 to the inner nuclear membrane by the histone variant H2A.Z. J Cell Biol 193 489 507

29. AitchisonJDRoutMPMarelliMBlobelGWozniakRW 1995 Two novel related yeast nucleoporins Nup170p and Nup157p: complementation with the vertebrate homologue Nup155p and functional interactions with the yeast nuclear pore-membrane protein Pom152p. J Cell Biol 131 1133 1148

30. JaspersenSLGiddingsTHJrWineyM 2002 Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J Cell Biol 159 945 956

31. NishikawaSTerazawaYNakayamaTHirataAMakioT 2003 Nep98p is a component of the yeast spindle pole body and essential for nuclear division and fusion. J Biol Chem 278 9938 9943

32. JaspersenSLMartinAEGlazkoGGiddingsTHJrMorganG 2006 The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J Cell Biol 174 665 675

33. RazafskyDHodzicD 2009 Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 186 461 472

34. FridkinAPenknerAJantschVGruenbaumY 2009 SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 66 1518 1533

35. StarrDAFridolfssonHN 2010 Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 26 421 444

36. WilliamsAJPaulsonHL 2008 Polyglutamine neurodegeneration: protein misfolding revisited. Trends Neurosci 31 521 528

37. van HamTJBreitlingRSwertzMANollenEA 2009 Neurodegenerative diseases: Lessons from genome-wide screens in small model organisms. EMBO Mol Med 1 360 370

38. SarasteMSibbaldPRWittinghoferA 1990 The P-loop–a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15 430 434

39. MaBGChenLJiHFChenZHYangFR 2008 Characters of very ancient proteins. Biochem Biophys Res Commun 366 607 611

40. AntoniacciLMKennaMAUetzPFieldsSSkibbensRV 2004 The spindle pole body assembly component Mps3p/Nep98p functions in sister chromatid cohesion. J Biol Chem 279 49542 49550

41. BuppJMMartinAEStensrudESJaspersenSL 2007 Telomere anchoring at the nuclear periphery requires the budding yeast Sad1-UNC-84 domain protein Mps3. J Cell Biol 179 845 854

42. AntoniacciLMKennaMASkibbensRV 2007 The nuclear envelope and spindle pole body-associated Mps3 protein bind telomere regulators and function in telomere clustering. Cell Cycle 6 75 79

43. ConradMNLeeCYWilkersonJLDresserME 2007 MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 104 8863 8868

44. OzaPJaspersenSLMieleADekkerJPetersonCL 2009 Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 23 912 927

45. SchoberHFerreiraHKalckVGehlenLRGasserSM 2009 Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev 23 928 938

46. ConradMNLeeCYChaoGShinoharaMKosakaH 2008 Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133 1175 1187

47. KoszulRKimKPPrentissMKlecknerNKameokaS 2008 Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133 1188 1201

48. HorigomeCOkadaTShimazuKGasserSMMizutaK 2011 Ribosome biogenesis factors bind a nuclear envelope SUN domain protein to cluster yeast telomeres. EMBO J 30 3799 811

49. ChanJNPoonBPSalviJOlsenJBEmiliA 2011 Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. Developmental cell 20 867 879

50. WineyMHoytMAChanCGoetschLBotsteinD 1993 NDC1: a nuclear periphery component required for yeast spindle pole body duplication. J Cell Biol 122 743 751

51. DonaldsonADKilmartinJV 1996 Spc42p: a phosphorylated component of the S. cerevisiae spindle pole body (SPD) with an essential function during SPB duplication. J Cell Biol 132 887 901

52. BullittERoutMPKilmartinJVAkeyCW 1997 The yeast spindle pole body is assembled around a central crystal of Spc42p. Cell 89 1077 1086

53. CampbellJLLorenzAWitkinKLHaysTLoidlJ 2006 Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol Biol Cell 17 1768 1778

54. MarelliMLuskCPChanHAitchisonJDWozniakRW 2001 A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J Cell Biol 153 709 724

55. WineyMYararDGiddingsTHJrMastronardeDN 1997 Nuclear pore complex number and distribution throughout the Saccharomyces cerevisiae cell cycle by three-dimensional reconstruction from electron micrographs of nuclear envelopes. Mol Biol Cell 8 2119 2132

56. CampbellRNLeverentzMKRyanLAReeceRJ 2008 Metabolic control of transcription: paradigms and lessons from Saccharomyces cerevisiae. Biochem J 414 177 187

57. LampingELucklJPaltaufFHenrySAKohlweinSD 1994 Isolation and characterization of a mutant of Saccharomyces cerevisiae with pleiotropic deficiencies in transcriptional activation and repression. Genetics 137 55 65

58. CarrozzaMJFlorensLSwansonSKShiaW-JAndersonS 2005 Stable incorporation of sequence specific repressors Ash1 and Ume6 into the Rpd3L complex. Biochim Biophys Acta 1731 77 87

59. BlackPNDiRussoCC 2007 Yeast acyl-CoA synthetases at the crossroads of fatty acid metabolism and regulation. Biochim Biophys Acta 1771 286 298

60. KnollLJJohnsonDRGordonJI 1994 Biochemical studies of three Saccharomyces cerevisiae acyl-CoA synthetases, Faa1p, Faa2p, and Faa3p. J Biol Chem 269 16348 16356

61. ChoiJYMartinCE 1999 The Saccharomyces cerevisiae FAT1 gene encodes an acyl-CoA synthetase that is required for maintenance of very long chain fatty acid levels. J Biol Chem 274 4671 4683

62. WatkinsPALuJFSteinbergSJGouldSJSmithKD 1998 Disruption of the Saccharomyces cerevisiae FAT1 gene decreases very long-chain fatty acyl-CoA synthetase activity and elevates intracellular very long-chain fatty acid concentrations. J Biol Chem 273 18210 18219

63. KamisakaYTomitaNKimuraKKainouKUemuraH 2007 DGA1 (diacylglycerol acyltransferase gene) overexpression and leucine biosynthesis significantly increase lipid accumulation in the Deltasnf2 disruptant of Saccharomyces cerevisiae. Biochem J 408 61 68

64. MurataNLosDA 1997 Membrane Fluidity and Temperature Perception. Plant Physiology 115 875 879

65. ZhangYMRockCO 2008 Membrane lipid homeostasis in bacteria. Nat Rev Microbiol 6 222 233

66. HardwickKGWeissELucaFCWineyMMurrayAW 1996 Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption. Science 273 953 956

67. JaspersenSLCharlesJFTinker-KulbergRLMorganDO 1998 A late mitotic regulatory network controlling cyclin destruction in Saccharomyces cerevisiae. Mol Biol Cell 9 2803 2817

68. PatranyGRyderNSStutzA 1984 Allylamine derivatives: new class of synthetic antifungal agents inhibiting fungal squalene epoxidase. Science v224 p1239(1233)

69. MaloneCJFixsenWDHorvitzHRHanM 1999 UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126 3171 3181

70. CrispMLiuQRouxKRattnerJBShanahanC 2006 Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172 41 53

71. HaqueFLloydDJSmallwoodDTDentCLShanahanCM 2006 SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26 3738 3751

72. WrightRBassonMD'AriLRineJ 1988 Increased amounts of HMG-CoA reductase induce “karmellae”: a proliferation of stacked membrane pairs surrounding the yeast nucleus. J Cell Biol 107 101 114

73. ParrishMLSengstagCRineJDWrightRL 1995 Identification of the sequences in HMG-CoA reductase required for karmellae assembly. Mol Biol Cell 6 1535 1547

74. ProfantDARobertsCJWrightRL 2000 Mutational analysis of the karmellae-inducing signal in Hmg1p, a yeast HMG-CoA reductase isozyme. Yeast 16 811 827

75. KoningAJRobertsCJWrightRL 1996 Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations. Mol Biol Cell 7 769 789

76. BastosRLinAEnarsonMBurkeB 1996 Targeting and function in mRNA export of nuclear pore complex protein Nup153. J Cell Biol 134 1141 1156

77. RalleTGrundCFrankeWWStickR 2004 Intranuclear membrane structure formations by CaaX-containing nuclear proteins. J Cell Sci 117 6095 6104

78. HattierTAndrulisEDTartakoffAM 2007 Immobility, inheritance and plasticity of shape of the yeast nucleus. BMC Cell Biol 8 47

79. SiniossoglouSSantos-RosaHRappsilberJMannMHurtE 1998 A novel complex of membrane proteins required for formation of a spherical nucleus. EMBO J 17 6449 6464

80. Santos-RosaHLeungJGrimseyNPeak-ChewSSiniossoglouS 2005 The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J 24 1931 1941

81. O'HaraLHanGSPeak-ChewSGrimseyNCarmanGM 2006 Control of phospholipid synthesis by phosphorylation of the yeast lipin Pah1p/Smp2p Mg2+-dependent phosphatidate phosphatase. J Biol Chem 281 34537 34548

82. DreierLRapoportTA 2000 In vitro formation of the endoplasmic reticulum occurs independently of microtubules by a controlled fusion reaction. J Cell Biol 148 883 898

83. ZimmerbergJKozlovMM 2006 How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7 9 19

84. Lippincott-SchwartzJPhairRD 2010 Lipids and cholesterol as regulators of traffic in the endomembrane system. Annu Rev of Biophy 39 559 578

85. LeesNDSkaggsBKirschDRBardM 1995 Cloning of the late genes in the ergosterol biosynthetic pathway of Saccharomyces cerevisiae–a review. Lipids 30 221 226

86. CostanzoMBaryshnikovaABellayJKimYSpearED 2010 The genetic landscape of a cell. Science 327 425 431

87. LeiKZhangXDingXGuoXChenM 2009 SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci U S A 106 10207 10212

88. SchulzIBaumannOSamereierMZoglmeierCGrafR 2009 Dictyostelium Sun1 is a dynamic membrane protein of both nuclear membranes and required for centrosomal association with clustered centromeres. Eur J Cell Biol 88 621 638

89. ZhouKRollsMMHallDHMaloneCJHanna-RoseW 2009 A ZYG-12-dynein interaction at the nuclear envelope defines cytoskeletal architecture in the C. elegans gonad. J Cell Biol 186 229 241

90. BurkeBRouxKJ 2009 Nuclei take a position: managing nuclear location. Dev Cell 17 587 597

91. MikiFKurabayashiATangeYOkazakiKShimanukiM 2004 Two-hybrid search for proteins that interact with Sad1 and Kms1, two membrane-bound components of the spindle pole body in fission yeast. Mol Genet Genomics 270 449 461

92. SaitohSTakahashiKNabeshimaKYamashitaYNakasekoY 1996 Aberrant mitosis in fission yeast mutants defective in fatty acid synthetase and acetyl CoA carboxylase. J Cell Biol 134 949 961

93. LongtineMSMcKenzieA3rdDemariniDJShahNGWachA 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14 953 961

94. SheffMAThornKS 2004 Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21 661 670

95. JonesGMStalkerJHumphraySWestACoxT 2008 A systematic library for comprehensive overexpression screens in Saccharomyces cerevisiae. Nat Methods 5 239 241

96. LangCGravaSFinlaysonMTrimbleRPhilippsenP 2010 Structural mutants of the spindle pole body cause distinct alteration of cytoplasmic microtubules and nuclear dynamics in multinucleated hyphae. Mol Biol Cell 21 753 766

97. WindgassenMSturmDCajigasIJGonzalezCISeedorfM 2004 Yeast shuttling SR proteins Npl3p, Gbp2p, and Hrb1p are part of the translating mRNPs, and Npl3p can function as a translational repressor. Mol Cell Biol 24 10479 10491

98. DevaiahSPRothMRBaughmanELiMTamuraP 2006 Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry 67 1907 1924

99. WeltiRLiWLiMSangYBiesiadaH 2002 Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277 31994 32002

100. HanXGrossRW 2001 Quantitative analysis and molecular species fingerprinting of triacylglyceride molecular species directly from lipid extracts of biological samples by electrospray ionization tandem mass spectrometry. Anal Biochem 295 88 100

101. YoderTJMcElwainMAFrancisSEBagleyJMullerEG 2005 Analysis of a spindle pole body mutant reveals a defect in biorientation and illuminates spindle forces. Mol Biol Cell 16 141 152

102. HofmannKStoffelW 1993 TMbase-A database of membrane spanning protein segments. Biol Chem 374 166