Adaptive mechanisms in pathogens: Universal aneuploidy in Leishmania

Trends in Parasitology

Volumn 28, Issue 9, 2012, Pages 370-376

  Mannaert, An ^a   Downing, Tim ^b,c   Imamura, Hideo ^a   Dujardin, Jean Claude ^a  

^a INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Aneuploidy (experimental and natural); Clonality; Fitness; Genome instability; Leishmania; Population genetics; Recombination

Indexed keywords

ANEUPLOIDY; CELL PROLIFERATION; CHROMOSOME 1; CHROMOSOME LOSS; CHROMOSOME REPLICATION; CRYPTOCOCCUS NEOFORMANS; DNA DAMAGE; DOWN REGULATION; FUNGAL GENE; GENE DOSAGE; GENE EXPRESSION; GENOMIC INSTABILITY; LEISHMANIA; NONHUMAN; POLYPLOIDY; PROTIST LIFE CYCLE STAGE; PROTOZOAL GENETICS; REVIEW;

ADAPTATION, BIOLOGICAL; ANEUPLOIDY; GENOME; LEISHMANIA;

EUKARYOTA; FUNGI; PROTOZOA;

EID: 84865172945     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2012.06.003     Document Type: Review

References (76)

1. Otto S.P., Whitton J. Polyploid incidence and evolution. Annu. Rev. Genet. 2000, 34:401-437.
2. Wolfe K.H., Shields D.C. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 1997, 387:708-713.
3. Blanc G., Wolfe K.H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 2004, 16:1667-1678.
4. McLysaght A., et al. Extensive genomic duplication during early chordate evolution. Nat. Genet. 2002, 31:200-204.
5. Dehal P., Boore J.L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005, 3:e314.
6. Torres E.M., et al. Aneuploidy: cells losing their balance. Genetics 2008, 179:737-746.
7. Pagès M., et al. Chromosome size and number polymorphisms in Leishmania infantum suggest amplification/deletion and possible genetic exchange. Mol. Biochem. Parasitol. 1989, 36:161-168.
8. Bastien P., et al. Interclonal variations in molecular karyotype in Leishmania infantum imply a 'mosaic' strain structure. Mol. Biochem. Parasitol. 1990, 40:53-61.
9. Rovai L., et al. Recurrent polymorphisms in small chromosomes of Leishmania tarentolae after nutrient stress or subcloning. Mol. Biochem. Parasitol. 1992, 50:115-125.
10. Ubeda J.M., et al. Modulation of gene expression in drug resistant Leishmania is associated with gene amplification, gene deletion and chromosome aneuploidy. Genome Biol. 2008, 9:R115.
11. Leprohon P., et al. Gene expression modulation is associated with gene amplification, supernumerary chromosomes and chromosome loss in antimony-resistant Leishmania infantum. Nucleic Acids Res. 2009, 37:1387-1399.
12. Pearson R.D., Sousa A.Q. Clinical spectrum of Leishmaniasis. Clin. Infect. Dis. 1996, 22:1-13.
13. Croft S.L., Olliaro P. Leishmaniasis chemotherapy - challenges and opportunities. Clin. Microbiol. Infect. 2011, 17:1478-1483.
14. Ivens A.C., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 2005, 309:436-442.
15. Peacock C.S., et al. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet. 2007, 39:839-847.
16. Downing T., et al. Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. Genome Res. 2011, 21:2143-2156.
17. Rogers M.B., et al. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res. 2011, 21:2129-2142.
18. Raymond F., et al. Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species. Nucleic Acids Res. 2012, 40:1131-1147.
19. Wincker P., et al. The Leishmania genome comprises 36 chromosomes conserved across widely divergent human pathogenic species. Nucleic Acids Res. 1996, 24:1688-1694.
20. Britto C., et al. Conserved linkage groups associated with large-scale chromosomal rearrangements between Old World and New World Leishmania genomes. Gene 1998, 222:107-117.
21. Blaineau C., et al. Long-range restriction maps of size-variable homologous chromosomes in Leishmania infantum. Mol. Biochem. Parasitol. 1991, 46:292-302.
22. Bastien P., et al. Leishmania: sex, lies and karyotype. Parasitol. Today 1992, 8:174-177.
23. Ravel C., et al. Medium-range restriction maps of five chromosomes of Leishmania infantum and localization of size-variable regions. Genomics 1996, 35:509-516.
24. Dujardin J.C., et al. Molecular epidemiology and diagnosis of Leishmania: what have we learnt from genome structure, dynamics and function?. Trans. R. Soc. Trop. Med. Hyg. 2002, 96(Suppl. 1):S81-S86.
25. Sunkin S.M., et al. The size difference between Leishmania major Friedlin chromosome one homologues is localized to sub-telomeric repeats at one chromosomal end. Mol. Biochem. Parasitol. 2000, 109:1-15.
26. Sterkers Y., et al. FISH analysis reveals aneuploidy and continual generation of chromosomal mosaicism in Leishmania major. Cell. Microbiol. 2011, 13:274-283.
27. Cruz A.K., et al. Plasticity in chromosome number and testing of essential genes in Leishmania by targeting. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:1599-1603.
28. Mottram J.C., et al. Gene disruptions indicate an essential function for the LmmCRK1 cdc2-related kinase of Leishmania mexicana. Mol. Microbiol. 1996, 22:573-583.
29. Dumas C., et al. Disruption of the trypanothione reductase gene of Leishmania decreases its ability to survive oxidative stress in macrophages. EMBO J. 1997, 16:2590-2598.
30. Martínez-Calvillo S., et al. Ploidy changes associated with disruption of two adjacent genes on Leishmania major chromosome 1. Int. J. Parasitol. 2005, 35:419-429.
31. Llewellyn M.S., et al. Extraordinary Trypanosoma cruzi diversity within single mammalian reservoir hosts implies a mechanism of diversifying selection. Int. J. Parasitol. 2011, 41:609-614.
32. Minning T.A., et al. Widespread, focal copy number variations (CNV) and whole chromosome aneuploidies in Trypanosoma cruzi strains revealed by array comparative genomic hybridization. BMC Genomics 2011, 12:139.
33. Williams B.R., et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 2008, 322:703-709.
34. Sheltzer J.M., Amon A. The aneuploidy paradox: costs and benefits of an incorrect karyotype. Trends Genet. 2011, 27:446-453.
35. Torres E.M., et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 2007, 317:916-924.
36. Sheltzer J.M., et al. Aneuploidy drives genomic instability in yeast. Science 2011, 333:1026-1030.
37. Beroukhim R., et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
38. Lengauer C., et al. Genetic instabilities in human cancers. Nature 1998, 396:643-649.
39. Weaver B.A., Cleveland D.W. Does aneuploidy cause cancer?. Curr. Opin. Cell Biol. 2006, 18:658-667.
40. Bannon J.H., Mc Gee M.M. Understanding the role of aneuploidy in tumorigenesis. Biochem. Soc. Trans. 2009, 37:910-913.
41. Thompson S.L., Compton D.A. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J. Cell Biol. 2010, 188:369-381.
42. Legrand M., et al. Role of DNA mismatch repair and double-strand break repair in genome stability and antifungal drug resistance in Candida albicans. Eukaryot. Cell 2007, 6:2194-2205.
43. Bañuls A.L., et al. Molecular epidemiology and evolutionary genetics of Leishmania parasites. Int. J. Parasitol. 1999, 29:1137-1147.
44. Tibayrenc M., Ayala F.J. The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol. 2002, 18:405-410.
45. Rougeron V., et al. Extreme inbreeding in Leishmania braziliensis. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:10224-10229.
46. Akopyants N.S., et al. Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 2009, 324:265-268.
47. Clayton C.E. Life without transcriptional control? From fly to man and back again. EMBO J. 2002, 21:1881-1888.
48. Clayton C., Shapira M. Post-transcriptional regulation of gene expression in trypanosomes and leishmanias. Mol. Biochem. Parasitol. 2007, 156:93-101.
49. Upender M.B., et al. Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells. Cancer Res. 2004, 64:6941-6949.
50. Gao C., et al. Chromosome instability, chromosome transcriptome, and clonal evolution of tumor cell populations. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:8995-9000.
51. Rancati G., et al. Aneuploidy underlies rapid adaptive evolution of yeast cells deprived of a conserved cytokinesis motor. Cell 2008, 135:879-893.
52. Torres E.M., et al. Thoughts on aneuploidy. Cold Spring Harbor Symp. Quant. Biol. 2010, 75:445-451.
53. Pavelka N., et al. Dr Jekyll and Mr Hyde: role of aneuploidy in cellular adaptation and cancer. Curr. Opin. Cell Biol. 2010, 22:809-815.
54. Selmecki A., et al. Genomic plasticity of the human fungal pathogen Candida albicans. Eukaryot. Cell 2010, 9:991-1008.
55. Selmecki A.M., et al. Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLoS Genet. 2009, 5:e1000705.
56. Poláková S., et al. Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2688-2693.
57. Hu G., et al. Variation in chromosome copy number influences the virulence of Cryptococcus neoformans and occurs in isolates from AIDS patients. BMC Genomics 2011, 12:526.
58. Alcolea P.J., et al. Temperature increase prevails over acidification in gene expression modulation of amastigote differentiation in Leishmania infantum. BMC Genomics 2010, 11:31.
59. Dujardin J.C., et al. Clonal propagation and the fast generation of karyotype diversity: an in vitro Leishmania model. Parasitology 2007, 134:33-39.
60. Forche A., et al. Evolution in Candida albicans populations during a single passage through a mouse host. Genetics 2009, 182:799-811.
61. Gisselsson D. Classification of chromosome segregation errors in cancer. Chromosoma 2008, 117:511-519.
62. Compton D.A. Mechanisms of aneuploidy. Curr. Opin. Cell Biol. 2011, 23:109-113.
63. Yih L.H., et al. Sodium arsenite disturbs mitosis and induces chromosome loss in human fibroblasts. Cancer Res. 1997, 57:5051-5059.
64. Bessat M., Ersfeld K. Functional characterization of cohesin SMC3 and separase and their roles in the segregation of large and minichromosomes in Trypanosoma brucei. Mol. Microbiol. 2009, 71:1371-1385.
65. Passos-Silva D.G., et al. Overview of DNA repair in Trypanosoma cruzi, Trypanosoma brucei, and Leishmania major. J. Nucleic Acids 2010, 2010:840768.
66. Shackney S.E., et al. Model for the genetic evolution of human solid tumors. Cancer Res. 1989, 49:3344-3354.
67. Forche A., et al. The parasexual cycle in Candida albicans provides an alternative pathway to meiosis for the formation of recombinant strains. PLoS Biol. 2008, 6:e110.
68. Mark Welch D., Meselson M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 2000, 288:1211-1215.
69. Butlin R. Evolution of sex: The costs and benefits of sex: new insights from old asexual lineages. Nat. Rev. Genet. 2002, 3:311-317.
70. Bailey J.A., Eichler E.E. Primate segmental duplications: crucibles of evolution, diversity and disease. Nat. Rev. Genet. 2006, 7:552-564.
71. Jiang R., et al. Population genetic inference from resequencing data. Genetics 2009, 181:187-197.
72. Lynch M. Estimation of allele frequencies from high-coverage genome-sequencing projects. Genetics 2009, 182:295-301.
73. Futschik A., Schlotterer C. The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics 2010, 186:207-218.
74. Smith A.M., et al. Highly-multiplexed barcode sequencing: an efficient method for parallel analysis of pooled samples. Nucleic Acids Res. 2010, 38:e142.
75. Vilela M.M., et al. Pathogenicity and virulence of Candida dubliniensis: comparison with C. albicans. Med. Mycol. 2002, 40:249-257.
76. Jackson A.P., et al. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res. 2009, 19:2231-2244.