Species- and Strain-Specific Adaptation of the HSP70 Super Family in Pathogenic Trypanosomatids

被引:21
作者
Drini, Sima [1 ,2 ]
Criscuolo, Alexis [3 ]
Lechat, Pierre [3 ]
Imamura, Hideo [4 ]
Skalicky, Tomas [5 ,6 ]
Rachidi, Najma [1 ,2 ]
Lukes, Julius [5 ,6 ,7 ]
Dujardin, Jean-Claude [4 ,8 ]
Spath, Gerald F. [1 ,2 ]
机构
[1] Inst Pasteur, Dept Parasites & Insect Vectors, Unite Parasitol Mol & Signalisat, Paris, France
[2] INSERM, U1201, Paris, France
[3] Inst Pasteur, Hub Bioinformat & Biostat, C3BI, Dept Genomes & Genet,USR IP CNRS 3756, Paris, France
[4] Inst Trop Med, Dept Biomed Sci, Mol Parasitol Unit, Antwerp, Belgium
[5] Czech Acad Sci, Ctr Biol, Inst Parasitol, Ceske Budejovice, Czech Republic
[6] Univ South Bohemia, Fac Sci, Ceske Budejovice, Czech Republic
[7] Canadian Inst Adv Res, Toronto, ON, Canada
[8] Univ Antwerp, Dept Biomed Sci, Antwerp, Belgium
关键词
Leishmania; heat shock protein; HSP70; evolution; phylogeny; synteny; copy number variation; gene loss; PROTOZOAN PARASITE LEISHMANIA; HEAT-SHOCK; NUCLEOTIDE EXCHANGE; MAXIMUM-LIKELIHOOD; MOLECULAR CHAPERONE; COCHAPERONE DNAJ; DRUG-RESISTANCE; PROTEIN; EXPRESSION; DONOVANI;
D O I
10.1093/gbe/evw140
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
All eukaryotic genomes encode multiple members of the heat shock protein 70 ( HSP70) family, which evolved distinctive structural and functional features in response to specific environmental constraints. Phylogenetic analysis of this protein family thus can inform on genetic and molecular mechanisms that drive species-specific environmental adaptation. Here we use the eukaryotic pathogen Leishmania spp. as a model system to investigate the evolution of the HSP70 protein family in an early-branching eukaryote that is prone to gene amplification and adapts to cytotoxic host environments by stress-induced and chaperone-dependent stage differentiation. Combining phylogenetic and comparative analyses of trypanosomatid genomes, draft genome of Paratrypanosoma and recently published genome sequences of 204 L. donovani field isolates, we gained unique insight into the evolutionary dynamics of the Leishmania HSP70 protein family. We provide evidence for ( i) significant evolutionary expansion of this protein family in Leishmania through gene amplification and functional specialization of highly conserved canonical HSP70 members, ( ii) evolution of trypanosomatid-specific, non-canonical family members that likely gained ATPase-independent functions, and ( iii) loss of one atypical HSP70 member in the Trypanosoma genus. Finally, we reveal considerable copy number variation of canonical cytoplasmic HSP70 in highly related L. donovani field isolates, thus identifying this locus as a potential hot spot of environment-genotype interaction. Our data draw a complex picture of the genetic history of HSP70 in trypanosomatids that is driven by the remarkable plasticity of the Leishmania genome to undergo massive intra-chromosomal gene amplification to compensate for the absence of regulated transcriptional control in these parasites.
引用
收藏
页码:1980 / 1995
页数:16
相关论文
共 78 条
[1]   The Revised Classification of Eukaryotes [J].
Adl, Sina M. ;
Simpson, Alastair G. B. ;
Lane, Christopher E. ;
Lukes, Julius ;
Bass, David ;
Bowser, Samuel S. ;
Brown, Matthew W. ;
Burki, Fabien ;
Dunthorn, Micah ;
Hampl, Vladimir ;
Heiss, Aaron ;
Hoppenrath, Mona ;
Lara, Enrique ;
le Gall, Line ;
Lynn, Denis H. ;
McManus, Hilary ;
Mitchell, Edward A. D. ;
Mozley-Stanridge, Sharon E. ;
Parfrey, Laura W. ;
Pawlowski, Jan ;
Rueckert, Sonja ;
Shadwick, Laura ;
Schoch, Conrad L. ;
Smirnov, Alexey ;
Spiegel, Frederick W. .
JOURNAL OF EUKARYOTIC MICROBIOLOGY, 2012, 59 (05) :429-493
[2]   Gapped BLAST and PSI-BLAST: a new generation of protein database search programs [J].
Altschul, SF ;
Madden, TL ;
Schaffer, AA ;
Zhang, JH ;
Zhang, Z ;
Miller, W ;
Lipman, DJ .
NUCLEIC ACIDS RESEARCH, 1997, 25 (17) :3389-3402
[3]   A soluble secretory reporter system in Trypanosoma brucei - Studies on endoplasmic reticulum targeting [J].
Bangs, JD ;
Brouch, EM ;
Ransom, DM ;
Roggy, JL .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1996, 271 (31) :18387-18393
[4]  
Blatch GL, 1999, BIOESSAYS, V21, P932, DOI 10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.3.CO
[5]  
2-E
[6]  
BOORSTEIN WR, 1994, J MOL EVOL, V38, P1
[7]   The heat shock protein HSP70 and heat shock cognate protein HSC70 contribute to antimony tolerance in the protozoan parasite Leishmania [J].
Brochu, C ;
Haimeur, A ;
Ouellette, M .
CELL STRESS & CHAPERONES, 2004, 9 (03) :294-303
[8]   Distinct mitochondrial HSP70 homologues conserved in various Leishmania species suggest novel biological functions [J].
Campos, Rodrigo M. ;
Nascimento, Mirna ;
Candido Ferraz, J. ;
Pereira, Mariana M. C. ;
Rocha, Pollyanna O. ;
Thompson, Gloria M. ;
Cysne-Finkelstein, Lea ;
Figueiredo, Regina C. B. Q. ;
de Melo Neto, Osvaldo P. .
MOLECULAR AND BIOCHEMICAL PARASITOLOGY, 2008, 160 (02) :157-162
[9]   Life without transcriptional control? From fly to man and back again [J].
Clayton, CE .
EMBO JOURNAL, 2002, 21 (08) :1881-1888
[10]   BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments [J].
Criscuolo, Alexis ;
Gribaldo, Simonetta .
BMC EVOLUTIONARY BIOLOGY, 2010, 10