Advertisement

Histone stress: an unexplored source of chromosomal instability in cancer?

  • Douglas Maya Miles
  • Chantal Desdouets
  • Vincent GéliEmail author
Review
  • 105 Downloads

Abstract

Ploidy is stably maintained in most human somatic cells by a sequential and tight coordination of cell cycle events. Undesired whole genome doublings or duplications are frequent in tumours and have been quite recently described as macro-evolutionary events associated with poor prognosis. In vitro and in vivo studies suggest that polyploidy can favour genome instability, facilitate the formation and progression of tumours, and modify their sensitivity to chemotherapeutic agents. Stress is strongly related to changes in ploidy and whole genome doublings. In this review, we summarize different mechanisms that promote polyploidization, describe a new type of stress able to trigger WGDs in S. cerevisiae, histone stress, and provide some examples and theoretical scenarios that support that cancer cells might suffer from this type of stress. We finally highlight some results showing that the kinase Swe1 (Wee1 in humans) has a role in sensing histone levels before cells enter mitosis, thereby avoiding their undesired consequences on chromosome segregation and ploidy control.

Keywords

Histones Whole genome duplication Polyploidy Swe1 Genome instability Cancer 

Notes

Acknowledgements

We thank Sebastian Chavez, Manuel Mendoza and Marie-Noelle Simon for discussions. Work in V.G. laboratory was supported by “Ligue contre le Cancer” (Equipe Labéllisée 2018).

References

  1. Au WC, Crisp MJ, DeLuca SZ, Rando OJ, Basrai MA (2008) Altered dosage and mislocalization of histone H3 and Cse4p lead to chromosome loss in Saccharomyces cerevisiae. Genetics 179:263–275Google Scholar
  2. Bielski CM, Zehir A, Penson AV, Donoghue MTA, Chatila W, Armenia J, Chang MT, Schram AM, Jonsson P, Bandlamudi C, Razavi P, Iyer G, Robson ME, Stadler ZK, Schultz N, Baselga J, Solit DB, Hyman DM, Berger MF, Taylor BS (2018) Genome doubling shapes the evolution and prognosis of advanced cancers. Nat Genet 50(8):1189–1195Google Scholar
  3. Botchkarev VV, Haber JE (2018) Functions and regulation of the Polo-like kinase Cdc5 in the absence and presence of DNA damage. Curr Genet 64:87Google Scholar
  4. Brocato J, Fang L, Chervona Y, Chen D, Kiok K, Sun H, Tseng HC, Xu D, Shamy M, Jin C, Costa M (2014) Arsenic induces polyadenylation of canonical histone mRNA by down-regulating stem-loop-binding protein gene expression. J Biol Chem 289(46):31751–31764Google Scholar
  5. Brocato J, Chen D, Liu J, Fang L, Jin C, Costa M (2015) A potential new mechanism of arsenic carcinogenesis: depletion of stem-loop binding protein and increase in polyadenylated canonical histone H3.1 mRNA. Biol Trace Elem Res 166:72–81Google Scholar
  6. Castillo AG, Mellone BG, Partridge JF, Richardson W, Hamilton GL, Allshire RC, Pidoux AL (2007) Plasticity of fission yeast CENP-A chromatin driven by relative levels of histone H3 and H4. PLoS Genet 3:e121Google Scholar
  7. Chambers AL, Ormerod G, Durley SC, Sing TL, Brown GW, Kent NA, Downs JA (2012) The INO80 chromatin remodeling complex prevents polyploidy and maintains normal chromatin structure at centromeres. Genes Dev 26(23):2590–2603Google Scholar
  8. Chervona Y, Arita A, Costa M (2012) Carcinogenic metals and the epigenome: understanding the effect of nickel, arsenic, and chromium. Metallomics 4(7):619–627Google Scholar
  9. Clément C, Orsi GA, Gatto A, Boyarchuk E, Forest A, Hajj B, Miné-Hattab J, Garnier M, Gurard-Levin ZA, Quivy JP, Almouzni G (2018) High-resolution visualization of H3 variants during replication reveals their controlled recycling. Nat Commun 9(1):3181Google Scholar
  10. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, Chu CS, Schuldiner M, Gebbia M, Recht J, Shales M, Ding H, Xu H, Han J, Ingvarsdottir K, Cheng B, Andrews B, Boone C, Berger SL, Hieter P, Zhang Z, Brown GW, Ingles CJ, Emili A, Allis CD, Toczyski DP, Weissman JS, Greenblatt JF, Krogan NJ (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446(7137):806–810Google Scholar
  11. Cook AJ, Gurard-Levin ZA, Vassias L, Almouzni G (2011) A specific function for the histone chaperone NASP to fine-tune a reservoir of soluble H3-H4 in the histone supply chain. Mol Cell 44:918–927Google Scholar
  12. D’Avino PP, Giansanti MG, Petronczki M (2015) Cytokinesis in animal cells. Cold Spring Harb Perspect Biol 7:a015834Google Scholar
  13. Davoli T, de Lange T (2011) The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 27:585–610Google Scholar
  14. Dewhurst SM, McGranahan N, Burrell RA, Rowan AJ, Gronroos E, Endesfelder D, Joshi T, Mouradov D, Gibbs P, Ward RL, Hawkins NJ, Szallasi Z, Sieber OM, Swanton C et al (2014) Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov 4:175–185Google Scholar
  15. Duelli D, Lazebnik Y (2007) Cell-to-cell fusion as a link between viruses and cancer. Nat Rev Cancer 7:968–976Google Scholar
  16. Duronio RJ, Marzluff WF (2017) Coordinating cell cycle-regulated histone gene expression through assembly and function of the histone locus body. RNA Biol 14(6):726–738Google Scholar
  17. Dürrbaum M, Storchová Z (2016) Effects of aneuploidy on gene expression: implications for cancer. FEBS J 283(5):791–802Google Scholar
  18. Eriksson PR, Ganguli D, Nagarajavel V, Clark DJ (2012) Regulation of histone gene expression in budding yeast. Genetics 191(1):7–20Google Scholar
  19. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D (2005) Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437:1043–1047Google Scholar
  20. Ganem NJ, Storchova Z, Pellman D (2007) Tetraploidy, aneuploidy and cancer. Curr Opin Genet Dev 17:157–162Google Scholar
  21. Gao P, Zheng J (2011) Oncogenic virus-mediated cell fusion: new insights into initiation and progression of oncogenic viruses-related cancers. Cancer Lett 303:1–8Google Scholar
  22. Gentric G, Desdouets C (2014) Polyploidization in liver tissue. Am J Pathol 184:322–331Google Scholar
  23. Gentric G, Celton-Morizur S, Desdouets C (2015) Polyploidy and liver proliferation. Clin Res Hepatol Gastroenterol 36:29–34Google Scholar
  24. Gokhman D, Livyatan I, Sailaja BS, Melcer S (2013) Meshorer E (2013) Multilayered chromatin analysis reveals E2f, Smad and Zfx as transcriptional regulators of histones. Nat Struct Mol Biol. 20(1):119–126Google Scholar
  25. Groth A, Ray-Gallet D, Quivy JP, Lukas J, Bartek J, Almouzni G (2005) Human Asf1 regulates the flow of S phase histones during replicational stress. Mol Cell 17:301–311Google Scholar
  26. Groth A, Rocha W, Verreault A, Almouzni G (2007) Chromatin challenges during DNA replication and repair. Cell 128(4):721–733Google Scholar
  27. Gunesdogan U, Jackle H, Herzig A (2014) Histone supply regulates S phase timing and cell cycle progression. Elife 3:e02443Google Scholar
  28. Gunjan A, Verreault A (2003) A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115:537–549Google Scholar
  29. Harari Y, Ram Y, Rappoport N, Hadany L, Kupiec M (2018a) Spontaneous changes in ploidy are common in yeast. Curr Biol 28(6):825–835Google Scholar
  30. Harari Y, Ram Y, Kupiec M (2018b) Frequent ploidy changes in growing yeast cultures. Curr Genet 64(5):1001–1004Google Scholar
  31. Henikoff S, Smith MM (2015) Histone variants and epigenetics. Cold Spring Harbor Perspect Biol 7(1):a019364Google Scholar
  32. Howell AS, Lew DJ (2012) Morphogenesis and the cell cycle. Genetics 190:51–77Google Scholar
  33. Jackson S, Chen ZJ (2010) Genomic and expression plasticity of polyploidy. Curr Opin Plant Biol 13(2):153–159Google Scholar
  34. Jamal-Hanjani M, Wilson GA, McGranahan N, Birkbak NJ, Watkins TBK, Veeriah S et al (2017) Tracking the evolution of non-small-cell lung cancer. N Engl J Med 376:2109–2121Google Scholar
  35. Jang CW, Shibata Y, Starmer J, Yee D, Magnuson T (2015) Histone H3.3 maintains genome integrity during mammalian development. Genes Dev 29(13):1377–1392Google Scholar
  36. Jordan A, Zhang X, Li J, Laulicht-Glick F, Sun H, Costa M (2017) Nickel and cadmium-induced SLBP depletion: a potential pathway to metal mediated cellular transformation. PLoS One 12(3):e0173624Google Scholar
  37. Kari V, Karpiuk O, Tieg B, Kriegs M, Dikomey E, Krebber H, Begus-Nahrmann Y, Johnsen SA (2013) A subset of histone H2B genes produces polyadenylated mRNAs under a variety of cellular conditions. PLoS One 8(5):e63745.  https://doi.org/10.1371/journal.pone.0063745 Google Scholar
  38. Khare SP, Sharma A, Deodhar KK, Gupta S (2011) Overexpression of histone variant H2A.1 and cellular transformation are related in N-nitrosodiethylamine-induced sequential hepatocarcinogenesis. Exp Biol Med 236:30–35Google Scholar
  39. Lacroix B, Maddox AS (2012) Cytokinesis, ploidy and aneuploidy. J Pathol 226:338–351Google Scholar
  40. Lanzotti DJ, Kaygun H, Yang X, Duronio RJ, Marzluff WF (2002) Developmental control of histone mRNA and dSLBP synthesis during Drosophila embryogenesis and the role of dSLBP in histone mRNA 3′ end processing in vivo. Mol Cell Biol 22(7):2267–2282Google Scholar
  41. Larsson LI, Bjerregaard B, Talts JF (2008) Cell fusions in mammals. Histochem Cell Biol 129:551–561Google Scholar
  42. Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483Google Scholar
  43. Lew DJ (2000) Cell-cycle checkpoints that ensure coordination between nuclear and cytoplasmic events in Saccharomyces cerevisiae. Curr Opin Genet Dev 10:47–53Google Scholar
  44. Mahajan K, Fang B, Koomen JM, Mahajan NP (2012) H2B Tyr37 phosphorylation suppresses expression of replication-dependent core histone genes. Nat Struct Mol Biol 19:930–937Google Scholar
  45. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80(5):487–498Google Scholar
  46. Marzluff WF, Wagner EJ, Duronio RJ (2008) Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9:843–854Google Scholar
  47. Maya Miles D, Peñate Salas X, Sanmartín Olmo T, Jourquin F, de la Cruz Muñoz Centeno M, Mendoza M, Simon MN, Chávez S, Géli V (2018) High levels of histones promote whole-genome-duplications and trigger a Swe1WEE1 dependent phosphorylation of Cdc28CDK1. Elife 7:e35337Google Scholar
  48. Maya D, Morillo-Huesca M, Delgado L, Chavez S, Munoz-Centeno MC (2013) A histone cycle. In: Stuart D (ed) The mechanisms of DNA replication. InTech, RijekaGoogle Scholar
  49. Mei Q, Huang J, Chen W, Tang J, Xu C, Yu Q, Cheng Y, Ma L, Yu X, Li S (2017) Regulation of DNA replication-coupled histone gene expression. Oncotarget 8(55):95005–95022Google Scholar
  50. Melters DP, Nye J, Zhao H, Dalal Y (2015) Chromatin dynamics in vivo: a game of musical chairs. Genes 6(3):751–776Google Scholar
  51. Mendiratta S, Gatto A, Almouzni G (2019) Histone supply: multitiered regulation ensures chromatin dynamics throughout the cell cycle. J Cell Biol 218(1):39–54Google Scholar
  52. Miettinen TP, Pessa HK, Caldez MJ, Fuhrer T, Diril MK, Sauer U, Kaldis P, Björklund M (2014) Identification of transcriptional and metabolic programs related to mammalian cell size. Curr Biol CB 24(6):598–608Google Scholar
  53. Mullen TE, Marzluff WF (2008) Degradation of histone mRNA requires oligouridylation followed by decapping and simultaneous degradation of the mRNA both 5′ to 3′ and 3′ to 5′. Genes Dev 22(1):50–65Google Scholar
  54. Murillo-Pineda M, Cabello-Lobato MJ, Clemente-Ruiz M, Monje-Casas F, Prado F (2014) Defective histone supply causes condensin-dependent chromatin alterations, SAC activation and chromosome decatenation impairment. Nucleic Acids Res 42:12469–12482Google Scholar
  55. Orr-Weaver TL (2015) When bigger is better: the role of polyploidy in organogenesis. Trends Genet 31:307–315Google Scholar
  56. Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–462Google Scholar
  57. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Annu Rev Genet 34:401–437Google Scholar
  58. Ovrebo JI, Edgar BA (2018) Polyploidy in tissue homeostasis and regeneration. Development 145(14):dev156034Google Scholar
  59. Palou R, Palou G, Quintana DG (2017) A role for the spindle assembly checkpoint in the DNA damage response. Curr Genet 63:275Google Scholar
  60. Pandit SK, Westendorp B, de Bruin A (2013) Physiological significance of polyploidization in mammalian cells. Trends Cell Biol 23:556–566Google Scholar
  61. Prado F, Maya D (2017) Regulation of replication fork advance and stability by nucleosome assembly. Genes 8(2):49Google Scholar
  62. Quénet D (2018) Histone variants and disease. Int Rev Cell Mol Biol 335:1–39Google Scholar
  63. Ramsey J, Schemske DW (1998) Pathways, mechanisms and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501Google Scholar
  64. Rattray AM, Müller B (2012) The control of histone gene expression. Biochem Soc Trans 40(4):880–885.  https://doi.org/10.1042/BST20120065 Google Scholar
  65. Reverón-Gómez N, González-Aguilera C, Stewart-Morgan KR, Petryk N, Flury V, Graziano S, Johansen JV, Jakobsen JS, Alabert C, Groth A (2018) Accurate recycling of parental histones reproduces the histone modification landscape during DNA replication. Mol Cell 72(2):239.e5–249.e5Google Scholar
  66. Riedmann C, Ma Y, Melikishvili M, Godfrey SG, Zhang Z, Chen KC, Rouchka EC, Fondufe-Mittendorf YN (2015) Inorganic Arsenic-induced cellular transformation is coupled with genome wide changes in chromatin structure, transcriptome and splicing patterns. BMC Genom 16(1):212Google Scholar
  67. Salzler HR, Davidson JM, Montgomery ND, Duronio RJ (2009) Loss of the histone pre-mRNA processing factor stem-loop binding protein in Drosophila causes genomic instability and impaired cellular proliferation. PLoS One 4:e8168Google Scholar
  68. Santaguida S, Amon A (2015) Short- and long-term effects of chromosome mis-segregation and aneuploidy. Nat Rev Mol Cell Biol 16:473–485Google Scholar
  69. Santos GC, Zielenska M, Prasad M, Squire JA (2007) Chromosome 6p amplification and cancer progression. J Clin Pathol 60:1–7Google Scholar
  70. Schoenfelder KP, Fox DT (2015) The expanding implications of polyploidy. J Cell Biol 209:485–491Google Scholar
  71. Scholes DR, Paige KN (2015) Plasticity in ploidy: a generalized response to stress. Trends Plant Sci 20(3):165–175Google Scholar
  72. Sharma S, Zeng JY, Zhuang CM, Zhou YQ, Yao HP, Hu X, Zhang R, Wang MH (2013) Small-molecule inhibitor BMS-777607 induces breast cancer cell polyploidy with increased resistance to cytotoxic chemotherapy agents. Mol Cancer Ther 12(5):725–736Google Scholar
  73. Shi Q, King RW (2005) Chromosome nondisjunction yields tetraploid rather than aneuploid cells in human cell lines. Nature 437:1038–1042Google Scholar
  74. Skene PJ, Henikoff S (2013) Histone variants in pluripotency and disease. Development 140(12):2513–2524Google Scholar
  75. Sullivan E, Santiago C, Parker ED, Dominski Z, Yang X, Lanzotti DJ, Ingledue TC, Marzluff WF, Duronio RJ (2001) Drosophila stem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression. Genes Dev 15(2):173–187Google Scholar
  76. Takayama Y, Mamnun YM, Trickey M, Dhut S, Masuda F, Yamano H, Toda T, Saitoh S (2010) Hsk1- and SCF(Pof3)-dependent proteolysis of S. pombe Ams2 ensures histone homeostasis and centromere function. Dev Cell 18:385–396Google Scholar
  77. Talbert PB, Henikoff S (2014) Environmental responses mediated by histone variants. Trends Cell Biol 24(11):642–650Google Scholar
  78. Talbert PB, Henikoff S (2017) Histone variants on the move: substrates for chromatin dynamics. Nat Rev Mol Cell Biol 18(2):115–126Google Scholar
  79. Talbert PB, Ahmad K, Almouzni G, Ausió J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SW, Cross GA, Cui L, Dimitrov SI, Doenecke D, Eirin-López JM, Gorovsky MA, Hake SB, Hamkalo BA, Holec S, Jacobsen SE, Kamieniarz K, Khochbin S, Ladurner AG, Landsman D, Latham JA, Loppin B, Malik HS, Marzluff WF, Pehrson JR, Postberg J, Schneider R, Singh MB, Smith MM, Thompson E, Torres-Padilla ME, Tremethick DJ, Turner BM, Waterborg JH, Wollmann H, Yelagandula R, Zhu B, Henikoff S (2012) A unified phylogeny-based nomenclature for histone variants. Epigenetics Chromatin 21(5):7Google Scholar
  80. Tomonaga T, Matsushita K, Yamaguchi S, Oohashi T, Shimada H, Ochiai T, Yoda K, Nomura F (2003) Overexpression and mistargeting of centromere protein-A in human primary colorectal cancer. Cancer Res. 63(13):3511–3516Google Scholar
  81. Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424Google Scholar
  82. Wang T, Chuffart F, Bourova-Flin E, Wang J, Mi J, Rousseaux S, Khochbin S (2018) Histone variants: critical determinants in tumour heterogeneity. Front Med.  https://doi.org/10.1007/s11684-018-0667-3 Google Scholar
  83. Wertheim B, Beukeboom LW, van de Zande L (2013) Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology. Cytogenet Genome Res 140:256–269Google Scholar
  84. Yant L, Bomblies K (2015) Genome management and mismanagement—cell-level opportunities and challenges of whole-genome duplication. Genes Dev 29(23):2405–2419Google Scholar
  85. Zack TL, Schumacher SE, Carter SL, Cherniack AD, Saksena G, Tabak B, Lawrence MS, Zhsng CZ, Wala J, Mermel CH, Sougnez C, Gabriel SB, Hernandez B, Shen H, Laird PW, Getz G, Meyerson M, Beroukhim R (2013) Pan-cancer patterns of somatic copy number alteration. Nat Genet 45:1134–1140Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Marseille Cancer Research Centre (CRCM), U1068 Inserm, UMR7258, CNRSAix-Marseille Université, Institut Paoli-Calmettes, Equipe labellisée LigueMarseilleFrance
  2. 2.Centre de Recherche des Cordeliers, UMR 1162, InsermUniversité Paris DescartesParisFrance

Personalised recommendations