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Temperature Dramatically Shapes Mosquito Gene Expression With Consequences for Mosquito-Zika Virus Interactions.

ABSTRACT: Vector-borne flaviviruses are emerging threats to human health. For successful transmission, the virus needs to efficiently enter mosquito cells and replicate within and escape several tissue barriers while mosquitoes elicit major transcriptional responses to flavivirus infection. This process will be affected not only by the specific mosquito-pathogen pairing but also by variation in key environmental variables such as temperature. Thus far, few studies have examined the molecular responses triggered by temperature and how these responses modify infection outcomes, despite substantial evidence showing strong relationships between temperature and transmission in a diversity of systems. To define the host transcriptional changes associated with temperature variation during the early infection process, we compared the transcriptome of mosquito midgut samples from mosquitoes exposed to Zika virus (ZIKV) and non-exposed mosquitoes housed at three different temperatures (20, 28, and 36°C). While the high-temperature samples did not show significant changes from those with standard rearing conditions (28°C) 48 h post-exposure, the transcriptome profile of mosquitoes housed at 20°C was dramatically different. The expression of genes most altered by the cooler temperature involved aspects of blood-meal digestion, ROS metabolism, and mosquito innate immunity. Further, we did not find significant differences in the viral RNA copy number between 24 and 48 h post-exposure at 20°C, suggesting that ZIKV replication is limited by cold-induced changes to the mosquito midgut environment. In ZIKV-exposed mosquitoes, vitellogenin, a lipid carrier protein, was most up-regulated at 20°C. Our results provide a deeper understanding of the temperature-triggered transcriptional changes in Aedes aegypti and can be used to further define the molecular mechanisms driven by environmental temperature variation.

SUBMITTER: Ferreira PG

PROVIDER: S-EPMC7303344 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Temperature Dramatically Shapes Mosquito Gene Expression With Consequences for Mosquito-Zika Virus Interactions.

Ferreira Priscila Gonçalves PG Tesla Blanka B Horácio Elvira Cynthia Alves ECA Nahum Laila Alves LA Brindley Melinda Ann MA de Oliveira Mendes Tiago Antônio TA Murdock Courtney Cuinn CC

Frontiers in microbiology 20200612

Vector-borne flaviviruses are emerging threats to human health. For successful transmission, the virus needs to efficiently enter mosquito cells and replicate within and escape several tissue barriers while mosquitoes elicit major transcriptional responses to flavivirus infection. This process will be affected not only by the specific mosquito-pathogen pairing but also by variation in key environmental variables such as temperature. Thus far, few studies have examined the molecular responses tri ...[more]

PMID: 32595607

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Project description:Because of the increasing threat that Zika virus (ZIKV) poses to more sub-tropical area due to increased global travel, there is a need for better understanding of the effect(s) of temperature on the establishment potential of ZIKV within these subtropical, temperate, and/or seasonal Ae. aegypti populations. The first step to determining risk establishment of ZIKV in these regions is to assess ZIKV's ability to infect mosquitoes at less tropical temperatures, and thus be detected through common surveillance programs. To that end, the effect of two rearing temperatures (RT) and extrinsic incubation temperatures (EIT) on infection and dissemination rates was evaluated, as well as the interactions of such. Total, there were four combinations (RT24-EIT24, RT24-EIT28, RT28-EIT24, RT28-EIT28). Further, a stochastic SEIR framework was adapted to determine whether observed data could lead to differential success of establishment of ZIKV in naive mosquito populations. There was no consistent pattern in significant differences found across treatments for either infection or dissemination rates (p>0.05), where only a significant difference was found in infection rates between RT24-EIT24 (44%) and RT28-EIT24 (82.6%). Across all temperature conditions, the model predicted between a 76.4% and 95.4% chance of successful establishment of ZIKV in naive mosquito populations under model assumptions. We further show that excluding the maximum observed infection and dissemination rates likely overestimates the probability of local establishment of ZIKV. These results indicate that 1) there is no straightforward relationship between RT, EIT, and infection/dissemination rates, 2) in more temperate climates, ZIKV may still have the ability to establish in populations of Aedes aegypti, 3) despite an overall lack of significant differences in infection/dissemination rates, temperature may still alter the kinetics of ZIKV within the mosquito enough to affect the likelihood of infection establishment and detection within the context of mosquito surveillance programs, and 4) both the temporal and magnitude qualities of vector competence are necessary for parameterization of within-mosquito virus kinetics.

Project description:While progress has been made in characterizing humoral immunity to Zika virus (ZIKV) in humans, little is known regarding the corresponding T cell responses to ZIKV. Here, we investigate the kinetics and viral epitopes targeted by T cells responding to ZIKV and address the critical question of whether preexisting dengue virus (DENV) T cell immunity modulates these responses. We find that memory T cell responses elicited by prior infection with DENV or vaccination with tetravalent dengue attenuated vaccines (TDLAV) recognize ZIKV-derived peptides. This cross-reactivity is explained by the sequence similarity of the two viruses, as the ZIKV peptides recognized by DENV-elicited memory T cells are identical or highly conserved in DENV and ZIKV. DENV exposure prior to ZIKV infection also influences the timing and magnitude of the T cell response. ZIKV-reactive T cells in the acute phase of infection are detected earlier and in greater magnitude in DENV-immune patients. Conversely, the frequency of ZIKV-reactive T cells continues to rise in the convalescent phase in DENV-naive donors but declines in DENV-preexposed donors, compatible with more efficient control of ZIKV replication and/or clearance of ZIKV antigen. The quality of responses is also influenced by previous DENV exposure, and ZIKV-specific CD8 T cells from DENV-preexposed donors selectively upregulated granzyme B and PD1, unlike DENV-naive donors. Finally, we discovered that ZIKV structural proteins (E, prM, and C) are major targets of both the CD4 and CD8 T cell responses, whereas DENV T cell epitopes are found primarily in nonstructural proteins.IMPORTANCE The issue of potential ZIKV and DENV cross-reactivity and how preexisting DENV T cell immunity modulates Zika T cell responses is of great relevance, as the two viruses often cocirculate and Zika virus has been spreading in geographical regions where DENV is endemic or hyperendemic. Our data show that memory T cell responses elicited by prior infection with DENV recognize ZIKV-derived peptides and that DENV exposure prior to ZIKV infection influences the timing, magnitude, and quality of the T cell response. Additionally, we show that ZIKV-specific responses target different proteins than DENV-specific responses, pointing toward important implications for vaccine design against this global threat.

Dataset Information

Temperature Dramatically Shapes Mosquito Gene Expression With Consequences for Mosquito-Zika Virus Interactions.

Publications

Temperature Dramatically Shapes Mosquito Gene Expression With Consequences for Mosquito-Zika Virus Interactions.

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