Streamlining sporozoite isolation from mosquitoes by leveraging the dynamics of migration to the salivary glands.
Anopheles stephensi
Density dependence
Extrinsic incubation period
Oocysts
Plasmodium berghei
Salivary glands
Sporozoites
Journal
Malaria journal
ISSN: 1475-2875
Titre abrégé: Malar J
Pays: England
ID NLM: 101139802
Informations de publication
Date de publication:
13 Sep 2022
13 Sep 2022
Historique:
received:
01
04
2022
accepted:
12
08
2022
entrez:
13
9
2022
pubmed:
14
9
2022
medline:
16
9
2022
Statut:
epublish
Résumé
Sporozoites isolated from the salivary glands of Plasmodium-infected mosquitoes are a prerequisite for several basic and pre-clinical applications. Although salivary glands are pooled to maximize sporozoite recovery, insufficient yields pose logistical and analytical hurdles; thus, predicting yields prior to isolation would be valuable. Preceding oocyst densities in the midgut is an obvious candidate. However, it is unclear whether current understanding of its relationship with sporozoite densities can be used to maximize yields, or whether it can capture the potential density-dependence in rates of sporozoite invasion of the salivary glands. This study presents a retrospective analysis of Anopheles stephensi mosquitoes infected with two strains of the rodent-specific Plasmodium berghei. Mean oocyst densities were estimated in the midguts earlier in the infection (11-15 days post-blood meal), with sporozoites pooled from the salivary glands later in the infection (17-29 days). Generalized linear mixed effects models were used to determine if (1) mean oocyst densities can predict sporozoite yields from pooled salivary glands, (2) whether these densities can capture differences in rates of sporozoite invasion of salivary glands, and (3), if the interaction between oocyst densities and time could be leveraged to boost overall yields. The non-linear effect of mean oocyst densities confirmed the role of density-dependent constraints in limiting yields beyond certain oocyst densities. Irrespective of oocyst densities however, the continued invasion of salivary glands by the sporozoites boosted recoveries over time (17-29 days post-blood meal) for either parasite strain. Sporozoite invasion of the salivary glands over time can be leveraged to maximize yields for P. berghei. In general, however, invasion of the salivary glands over time is a critical fitness determinant for all Plasmodium species (extrinsic incubation period, EIP). Thus, delaying sporozoite collection could, in principle, substantially reduce dissection effort for any parasite within the genus, with the results also alluding to the potential for changes in sporozoites densities over time to modify infectivity for the next host.
Sections du résumé
BACKGROUND
BACKGROUND
Sporozoites isolated from the salivary glands of Plasmodium-infected mosquitoes are a prerequisite for several basic and pre-clinical applications. Although salivary glands are pooled to maximize sporozoite recovery, insufficient yields pose logistical and analytical hurdles; thus, predicting yields prior to isolation would be valuable. Preceding oocyst densities in the midgut is an obvious candidate. However, it is unclear whether current understanding of its relationship with sporozoite densities can be used to maximize yields, or whether it can capture the potential density-dependence in rates of sporozoite invasion of the salivary glands.
METHODS
METHODS
This study presents a retrospective analysis of Anopheles stephensi mosquitoes infected with two strains of the rodent-specific Plasmodium berghei. Mean oocyst densities were estimated in the midguts earlier in the infection (11-15 days post-blood meal), with sporozoites pooled from the salivary glands later in the infection (17-29 days). Generalized linear mixed effects models were used to determine if (1) mean oocyst densities can predict sporozoite yields from pooled salivary glands, (2) whether these densities can capture differences in rates of sporozoite invasion of salivary glands, and (3), if the interaction between oocyst densities and time could be leveraged to boost overall yields.
RESULTS
RESULTS
The non-linear effect of mean oocyst densities confirmed the role of density-dependent constraints in limiting yields beyond certain oocyst densities. Irrespective of oocyst densities however, the continued invasion of salivary glands by the sporozoites boosted recoveries over time (17-29 days post-blood meal) for either parasite strain.
CONCLUSIONS
CONCLUSIONS
Sporozoite invasion of the salivary glands over time can be leveraged to maximize yields for P. berghei. In general, however, invasion of the salivary glands over time is a critical fitness determinant for all Plasmodium species (extrinsic incubation period, EIP). Thus, delaying sporozoite collection could, in principle, substantially reduce dissection effort for any parasite within the genus, with the results also alluding to the potential for changes in sporozoites densities over time to modify infectivity for the next host.
Identifiants
pubmed: 36100902
doi: 10.1186/s12936-022-04270-y
pii: 10.1186/s12936-022-04270-y
pmc: PMC9472382
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
264Informations de copyright
© 2022. The Author(s).
Références
Microbes Infect. 2006 Feb;8(2):308-15
pubmed: 16213176
Vaccine. 2002 Jan 15;20(7-8):1039-45
pubmed: 11803063
Vaccines (Basel). 2020 Jul 21;8(3):
pubmed: 32708179
Vaccine. 2015 Dec 22;33(52):7476-82
pubmed: 26409813
Proc Natl Acad Sci U S A. 2020 Mar 31;117(13):7363-7373
pubmed: 32165544
Malar J. 2015 Mar 18;14:117
pubmed: 25889522
PLoS One. 2012;7(5):e36508
pubmed: 22563506
Evol Appl. 2013 Jun;6(4):617-29
pubmed: 23789029
Proc Natl Acad Sci U S A. 2020 Oct 6;117(40):24900-24908
pubmed: 32929020
Parasit Vectors. 2019 May 6;12(1):206
pubmed: 31060594
Mol Microbiol. 2018 Aug;109(4):458-473
pubmed: 29873127
Proc Biol Sci. 2013 Sep 18;280(1770):20132030
pubmed: 24048159
Eur J Immunol. 2013 Mar;43(3):693-704
pubmed: 23229763
Nat Protoc. 2006;1(2):614-23
pubmed: 17406288
Malar J. 2010 May 27;9:145
pubmed: 20507620
Clin Vaccine Immunol. 2013 Jun;20(6):803-10
pubmed: 23536694
Nature. 1967 Oct 14;216(5111):160-2
pubmed: 6057225
PLoS Pathog. 2007 Dec 28;3(12):e195
pubmed: 18166078
J Exp Biol. 2001 Aug;204(Pt 16):2773-80
pubmed: 11683433
J Parasitol. 1966 Jun;52(3):559-64
pubmed: 5942531
Trends Parasitol. 2020 Aug;36(8):705-716
pubmed: 32620501
Trends Parasitol. 2007 Feb;23(2):63-70
pubmed: 17188574
Elife. 2017 May 16;6:
pubmed: 28506360
J Vector Borne Dis. 2018 Jan-Mar;55(1):9-13
pubmed: 29916442
Curr Opin Insect Sci. 2014 Sep 1;3:14-21
pubmed: 25309850
Infect Immun. 1999 Aug;67(8):4285-9
pubmed: 10417207
Int J Parasitol. 2018 Dec;48(14):1073-1078
pubmed: 30367865
Sci Rep. 2013 Dec 04;3:3418
pubmed: 24301557
Infect Immun. 2014 Mar;82(3):1164-72
pubmed: 24379288
Proc Biol Sci. 2020 Jul 29;287(1931):20201093
pubmed: 32693720
Int J Parasitol. 2018 Dec;48(14):1127-1136
pubmed: 30391497
J Exp Med. 2020 Jan 6;217(1):
pubmed: 31658986
Nat Commun. 2018 Aug 27;9(1):3474
pubmed: 30150763
PLoS One. 2017 May 22;12(5):e0177304
pubmed: 28531172
Vaccine. 2016 Jun 14;34(28):3229-34
pubmed: 27160038
Life Sci Alliance. 2019 May 29;2(3):
pubmed: 31142638
PLoS One. 2018 Feb 5;13(2):e0192315
pubmed: 29401525
Bio Protoc. 2014 Jul 20;7(14):
pubmed: 28932759
Front Cell Infect Microbiol. 2017 May 31;7:198
pubmed: 28620583
PLoS Pathog. 2019 Jul 26;15(7):e1007973
pubmed: 31348803
Parasit Vectors. 2014 Dec 14;7:593
pubmed: 25496502
J Pharmacol Pharmacother. 2011 Apr;2(2):140-2
pubmed: 21772786
R Soc Open Sci. 2020 Oct 7;7(10):192173
pubmed: 33204441
Genome Med. 2019 Oct 22;11(1):63
pubmed: 31640748
Ann Soc Belg Med Trop. 1981 Sep;61(3):349-68
pubmed: 7032427
Int J Parasitol. 2020 Oct;50(12):985-996
pubmed: 32681932
Front Immunol. 2019 Jun 05;10:1227
pubmed: 31231377
Trans R Soc Trop Med Hyg. 1989 Jan-Feb;83(1):67-70
pubmed: 2690418
J Exp Med. 2012 Jan 16;209(1):93-107
pubmed: 22184632
Parasit Vectors. 2018 Mar 12;11(1):178
pubmed: 29530073
Am J Trop Med Hyg. 1991 Nov;45(5):574-7
pubmed: 1951866
Malar J. 2009 Oct 12;8:228
pubmed: 19822012
Mol Biochem Parasitol. 2006 Jan;145(1):60-70
pubmed: 16242190
Nat Protoc. 2006;1(1):346-56
pubmed: 17406255
PeerJ. 2018 May 23;6:e4794
pubmed: 29844961
PLoS Pathog. 2005 Sep;1(1):e9
pubmed: 16201021
Front Microbiol. 2019 Nov 15;10:2651
pubmed: 31803169
Genome Biol. 2014 Sep 23;15(9):459
pubmed: 25244985
Malar J. 2018 Dec 6;17(1):457
pubmed: 30522507