Resistance of Biomphalaria glabrata 13-16-R1 snails to Schistosoma mansoni PR1 is a function of haemocyte abundance and constitutive levels of specific transcripts in haemocytes

被引:41
作者
Larson, Maureen K. [1 ]
Bender, Randal C. [1 ]
Bayne, Christopher J. [1 ]
机构
[1] Oregon State Univ, Dept Zool, Corvallis, OR 97331 USA
基金
美国国家卫生研究院;
关键词
Biomphalaria; Schistosoma; Haemocyte; Haematocrit; Host-parasite; Resistance; Expression; Oxidative; INFLAMMATORY FACTOR-I; CIRCULATING HEMOCYTES; IMMUNE ACTIVATION; PEROXIREDOXIN; SUSCEPTIBILITY; INFECTION; SPOROCYSTS; SURFACE; GENE; EXPRESSION;
D O I
10.1016/j.ijpara.2013.11.004
中图分类号
R38 [医学寄生虫学]; Q [生物科学];
学科分类号
07 ; 0710 ; 09 ; 100103 ;
摘要
Continuing transmission of human intestinal schistosomiasis depends on the parasite's access to susceptible snail intermediate hosts (often Biomphalaria glabrata). Transmission fails when parasite larvae enter resistant individuals in wild snail populations. The genetic basis for differences in snail susceptibility/resistance is being intensively investigated as a means to devise novel control strategies based on resistance genes. Reactive oxygen species produced by the snail's defence cells (haemocytes) are effectors of resistance. We hypothesised that genes relevant to production and consumption of reactive oxygen species would be expressed differentially in the haemocytes of snail hosts with different susceptibility/resistance phenotypes. By restricting the genetic diversity of snails, we sought to facilitate identification of resistance genes. By inbreeding, we procured from a 13-16-R1 snail population with both susceptible and resistant individuals 52 lines of B. glabrata (expected homozygosity similar to 87.5%), and determined the phenotype of each in regard to susceptibility/resistance to Schistosoma mansoni. The inbred lines were found to have line-specific differences in numbers of spreading haemocytes; these were enumerated in both juvenile and adult snails. Lines with high cell numbers were invariably resistant to S. mansoni, whereas lines with lower cell numbers could be resistant or susceptible. Transcript levels in haemocytes were quantified for 18 potentially defence-related genes. Among snails with low cell numbers, the different susceptibility/resistance phenotypes correlated with differences in transcript levels for two redox-relevant genes: an inferred phagocyte oxidase component and a peroxiredoxin. Allograft inflammatory factor (potentially a regulator of-leucocyte activation) was expressed at higher levels in resistant snails regardless of spread cell number. Having abundant spreading haemocytes is inferred to enable a snail to kill parasite sporocysts. In contrast, snails with fewer spreading haemocytes seem to achieve resistance only if specific genes are expressed constitutively at levels that are high for the species. (C) 2014 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.
引用
收藏
页码:343 / 353
页数:11
相关论文
共 72 条
[1]   Differential transcriptomic responses of Biomphalaria glabrata (Gastropoda, Mollusca) to bacteria and metazoan parasites, Schistosoma mansoni and Echinostoma paraensei (Digenea, Platyhelminthes) [J].
Adema, Coen M. ;
Hanington, Patrick C. ;
Lun, Cheng-Man ;
Rosenberg, George H. ;
Aragon, Anthony D. ;
Stout, Barbara A. ;
Richard, Mara L. Lennard ;
Gross, Paul S. ;
Loker, Eric S. .
MOLECULAR IMMUNOLOGY, 2010, 47 (04) :849-860
[2]  
Barcante Thales A., 2012, Journal of Parasitology Research, P314723, DOI 10.1155/2012/314723
[3]   INTERPRETATION OF SNAIL-TREMATODE INFECTION RATES - SPECIFICITY BASED ON CONCORDANCE OF COMPATIBLE PHENOTYPES [J].
BASCH, PF .
INTERNATIONAL JOURNAL FOR PARASITOLOGY, 1975, 5 (04) :449-452
[4]   Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: A 2009 assessment [J].
Bayne, Christopher J. .
MOLECULAR AND BIOCHEMICAL PARASITOLOGY, 2009, 165 (01) :8-18
[5]   MACROPHAGE-LIKE HEMOCYTES OF RESISTANT BIOMPHALARIA-GLABRATA ARE CYTO-TOXIC FOR SPOROCYSTS OF SCHISTOSOMA-MANSONI INVITRO [J].
BAYNE, CJ ;
BUCKLEY, PM ;
DEWAN, PC .
JOURNAL OF PARASITOLOGY, 1980, 66 (03) :413-419
[6]  
Bayne CJ, 2001, PARASITOLOGY, V123, pS159
[7]   Variation in expression of Biomphalaria glabrata SOD1:: A potential controlling factor in susceptibility/resistance to Schistosoma mansoni [J].
Bender, Randall C. ;
Goodall, Cheri P. ;
Blouin, Michael S. ;
Bayne, Christopher J. .
DEVELOPMENTAL AND COMPARATIVE IMMUNOLOGY, 2007, 31 (09) :874-878
[8]   Three genes involved in the oxidative burst are closely linked in the genome of the snail, Biomphalaria glabrata [J].
Blouin, Michael S. ;
Bonner, Kaitlin M. ;
Cooper, Becky ;
Amarasinghe, Vindhya ;
O'Donnell, Ryan P. ;
Bayne, Christopher J. .
INTERNATIONAL JOURNAL FOR PARASITOLOGY, 2013, 43 (01) :51-55
[9]   Effects of Cu/Zn Superoxide Dismutase (sod1) Genotype and Genetic Background on Growth, Reproduction and Defense in Biomphalaria glabrata [J].
Bonner, Kaitlin M. ;
Bayne, Christopher J. ;
Larson, Maureen K. ;
Blouin, Michael S. .
PLOS NEGLECTED TROPICAL DISEASES, 2012, 6 (06)
[10]   Surface membrane proteins of Biomphalaria glabrata embryonic cells bind fucosyl determinants on the tegumental surface of Schistosoma mansoni primary sporocysts [J].
Castillo, Maria G. ;
Wu, Xiao-Jun ;
Dinguirard, Nathalie ;
Nyame, A. Kwame ;
Cummings, Richard D. ;
Yoshino, Timothy P. .
JOURNAL OF PARASITOLOGY, 2007, 93 (04) :832-840