A systematic genomic screen implicates nucleocytoplasmic transport and membrane growth in nuclear size control

1. Meer GV, Voelker DR, and Feigenson GW. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008; 9: 112–124. doi: 10.1038/nrm2330 18216768

2. Wilson EB. The Karyoplasmic Ratio. In The Cell in Development and Heredity (New York: The Macmillan Company); 1925. pp. 727–733.

3. Gregory T. Genome size evolution in animals. In The Evolution of the Genome, Gregory T., ed. (London: Elsevier Academic Press); 2005. pp. 4–87.

4. Jorgensen P, Edgington NP, Schneider BL, Rupes I, Tyers M, and Futcher B. The size of the nucleus increases as yeast cells grow. Mol. Biol. Cell 2007; 18: 3523–3532. doi: 10.1091/mbc.E06-10-0973 17596521

5. Neumann FR, and Nurse P. Nuclear size control in fission yeast. J. Cell Biol. 2007; 179: 593–600. doi: 10.1083/jcb.200708054 17998401

6. Hara Y, and Merten CA. Dynein-based accumulation of membranes regulates nuclear expansion in Xenopus laevis egg extracts. Dev. Cell 2015; 33: 562–575. doi: 10.1016/j.devcel.2015.04.016 26004509

7. Harris H. The reactivation of the red cell nucleus. J. Cell Sci. 1967; 2: 23–32. 6031005

8. Gurdon JB. Injected nuclei in frog oocytes: fate, enlargement, and chromatin dispersal. J. Embryol. Exp. Morph. 1976; 36: 523–540. 1010977

9. Levy DL, and Heald R. Nuclear size is regulated by importin α and Ntf2 in Xenopus. Cell 2010; 143: 288–298. doi: 10.1016/j.cell.2010.09.012 20946986

10. Jevtić P, Edens LJ, Li X, Nguyen T, Chen P, and Levy DL. Concentration-dependent effects of nuclear lamins on nuclear size in Xenopus and Mammalin cells. J. Biol. Chem. 2015; 290: 27557–27571. doi: 10.1074/jbc.M115.673798 26429910

11. Kim DU, Hayles J, Kim D, Wood V, Park HO, Won M, Yoo HS, Duhig T, Nam M, Palmer G, et al. Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 2010; 28: 617–623. doi: 10.1038/nbt.1628 20473289

12. Koning AJ, Lum PY, Williams JM, and Wright R. DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil. Cytoskeleton 1993; 25: 111–128. doi: 10.1002/cm.970250202 7686821

13. Thakurta AG, Gopal G, Yoon JH, Kozak L, and Dhar R. Homolog of BRCA2-interacting Dss1p and Uap56p link Mlo3p and Rae1p for mRNA export in fission yeast. EMBO J. 2005; 24: 2512–2523. doi: 10.1038/sj.emboj.7600713 15990877

14. Makarova M, Gu Y, Chen JS, Beckley JR, Gould KL, and Oliferenko S. Temporal regulation of lipin activity diverged to account for differences in mitotic programs. Curr. Biol. 2016; 26: 237–243. doi: 10.1016/j.cub.2015.11.061 26774782

15. Brown JA, Bharathi A, Ghosh A, Whalen W, Fitzgerald E, and Dhar R. A mutation in the Schizosaccharomyces pombe rae1 gene causes defects in poly(A)+ RNA export and in the cytoskeleton. J. Biol. Chem. 1995; 270: 7411–7419. 7706287

16. Mendell JT, Medghalchi SM, Lake RG, Noensie EN, and Dietz HC. Novel Upf2p orthologues suggest a functional link between translation initiation and nonsense surveillance complexes. Mol. Cell. Biol. 2000; 20: 8944–8957. 11073994

17. Grigull J, Mnaimneh S, Pootoolal J, Robinson MD, and Hughes TR. Genome-wide analysis of mRNA stability using transcription inhibitors and microarrays reveals posttranscriptional control of ribosome biogenesis factors. Mol. Cell. Biol. 2004; 24: 5534–5547. doi: 10.1128/MCB.24.12.5534-5547.2004 15169913

18. Thakurta AG, Yoon JH, and Dhar R. Schizosaccharomyces pombe spPABP, a homologue of Saccharomyces cerevisiae Pab1p, is a non-essential, shuttling protein that facilitates mRNA export. Yeast 2002; 19: 803–810. doi: 10.1002/yea.876 12112233

19. Matsuyama A, Arai R, Yashiroda Y, Shirai A, Kamata A, Sekido S, Kobayashi Y, Hashimoto A, Hamamoto M, Hiraoka Y. et al. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 2006; 24: 841–847. doi: 10.1038/nbt1222 16823372

20. Polanshek MM. Effects of heat shock and cycloheximide on growth and division of the fission yeast, Schizosaccharomyces pombe. J. Cell Sci. 1977; 23: 1–23. 893531

21. Cox J, and Mann M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics 2012; 13(Suppl 16); S12.

22. Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, and Bähler J. Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 2003; 14: 214–229. doi: 10.1091/mbc.E02-08-0499 12529438

23. Mata J, Lyne R, Burns G, and Bähler J. The transcriptional program of meiosis and sporulation in fission yeast. Nat. Genet. 2002; 32: 143–147. doi: 10.1038/ng951 12161753

24. Mata J, Wilbrey A, and Bähler J. Transcriptional regulatory network for sexual differentiation in fission yeast. Genome Biol. 2007; 8 (R217).

25. Santos-Rosa H, Leung J, Grimsey N, Peak-Chew S, and Siniossoglou S. The yeast lipin Smp2 couples phospholipid biosynthesis to nuclear membrane growth. EMBO J. 2005; 24: 1931–1941. doi: 10.1038/sj.emboj.7600672 15889145

26. Tange Y, Hirata A, and Niwa O. An evolutionarily conserved fission yeast protein, Ned1, implicated in normal nuclear morphology and chromosome stability, interacts with Dis3, Pim1/RCC1 and an essential nucleoporin. J. Cell Sci. 2002; 115: 4375–4385. 12376568

27. Yam C, He Y, Zhang D, Chiam KH, and Oliferenko S. Divergent strategies for controlling the nuclear membrane satisfy geometric constraints during nuclear division. Curr. Biol. 2011; 21: 1314–1319. doi: 10.1016/j.cub.2011.06.052 21802294

28. Saitoh S, Takahashi K, Nabeshima K, Yamashita Y, Nakaseko Y, Hirata A, and Yanagida M. Aberrant mitosis in fission yeast mutants defective in fatty acid synthetase and acetyl CoA carboxylase. J. Cell Biol. 1996; 134: 949–961. 8769419

29. Jonstrup AT, Andersen KR, Van LB, and Brodersen DE. The 1.4-Å crystal structure of the S. pombe Pop2 deadenylase subunit unveils the configuration of an active enzyme. Nucleic Acid Res. 2007; 35: 3153–3164. doi: 10.1093/nar/gkm178 17452359

30. Miller JE and Reese JC. Ccr4-Not complex: the control freak of eukaryotic cells. Crit. Rev. Biochem. Mol. Biol. 2012; 47:315–333. doi: 10.3109/10409238.2012.667214 22416820

31. Takeda K, and Yanagida M. Regulation of nuclear proteasome by Rho6/Ubc2 through ubiquitination and destruction of the sensor and anchor Cut8. Cell 2005; 122: 393–405. doi: 10.1016/j.cell.2005.05.023 16096059

32. Ideue T, Azad AK, Yoshida J, Matsusaka T, Yanagida M, Ohshima Y and Tani T. The nucleolus is involved in mRNA export from the nucleus in fission yeast. J. Cell Sci. 2004; 117: 2887–2895. doi: 10.1242/jcs.01155 15161942

33. Jossé L, Harley ME, Pires IM and Hughes DA. Fission yeast Dss1 associates with the proteasome and is required for efficient ubiquitin-dependent proteolysis. Biochem. J. 2006; 393:303–309. doi: 10.1042/BJ20051238 16149916

34. Martin DE, Soulard A, and Hall MN. TOR regulates ribosomal protein gene expression via PKA and the forkhead transcription factor FHL1. Cell 2004; 119: 969–979. doi: 10.1016/j.cell.2004.11.047 15620355

35. Sardana R, and Johnson AW. The methyltransferase adaptor protein Trm112 is involved in biogenesis of both ribosomal subunits. Mol. Biol. Cell 2012; 23: 4313–4322. doi: 10.1091/mbc.E12-05-0370 22956767

36. Vuković LD, Jevtić P, Zhang Z, Stohr BA, and Levy DL. Nuclear size is sensitive to NTF2 protein levels in a manner dependent on Ran binding. J. Cell. Sci. 2016; 129: 1115–1127. doi: 10.1242/jcs.181263 26823604

37. Raucher D, and Sheetz MP. Characteristics of a membrane reservoir buffering membrane tension. Biophys. J. 1999; 77: 1992–2002. doi: 10.1016/S0006-3495(99)77040-2 10512819

38. Webster M, Witkin KL, and Cohen-Fix O. Sizing up the nucleus: nuclear shape, size and nuclear envelope assembly. J. Cell Sci. 2009; 122: 1477–1486. doi: 10.1242/jcs.037333 19420234

39. Zink D, Fischer AH, and Nickerson JA. Nuclear structure in cancer cells. Nat. Rev. Cancer 2004; 9: 677–687.

40. Bähler J, Wu JQ, Longtine MS, Shah NG, McKenzie A 3rd, Steever AB, Wach A, Philippsen P, and Pringle JR. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 1998; 14: 943–951. doi: 10.1002/(SICI)1097-0061(199807)14:10<943::AID-YEA292>3.0.CO;2-Y 9717240

41. Moreno S, Klar A, and Nurse P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 1991; 194: 795–823. 2005825

42. Bicho CC, de Lima Alves F, Chen ZA, Rappsilber J, and Sawin KE. A genetic engineering solution to the “arginine conversion problem” in stable isotope labeling by amino acids in cell culture (SILAC). Mol. Cell Proteomics 2010; 9: 1567–1577. doi: 10.1074/mcp.M110.000208 20460254

43. Amberg DC, Goldstein AL, and Cole CN. Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev. 1992; 6: 1173–1189. 1628825

44. Wu H, Zheng X, Araki Y, Sahara H, Takagi H and Shimoi H. Global gene expression analysis of yeast cells during sake brewing. Appl. Environ. Microbiol. 2006; 72: 7353–7358. doi: 10.1128/AEM.01097-06 16997994

45. Vizcaíno JA, Csordas A, del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T, et al. 2016 update of the PRIDE database and related tools. Nucleic Acids Res. 2016; 44(D1): D447–D456. doi: 10.1093/nar/gkv1145 26527722

46. Shimizu M, Roth SY, Szent-Gyorgyi C, and Simpson RT. Nucleosomes are positioned with base pair precision adjacent to the alpha 2 operator in Saccharomyces cerevisiae. EMBO J. 1991; 10: 3033–3041. 1915278

47. Alfa C, Fantes P, Hyams J, McLeod M, and Warbrick E. Experiments with fission yeast: A laboratory course manual: Cold Spring Harbor Lab. Press; 1993.