Source: MICHIGAN STATE UNIV submitted to NRP
BOVINE LEUKEMIA VIRUS INFECTION AND ITS EFFECT ON THE IMMUNE COMPETENCE OF DAIRY CATTLE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1008004
Grant No.
2016-67011-24713
Cumulative Award Amt.
$79,000.00
Proposal No.
2015-03626
Multistate No.
(N/A)
Project Start Date
Dec 15, 2015
Project End Date
Dec 14, 2017
Grant Year
2016
Program Code
[A7101]- AFRI Predoctoral Fellowships
Recipient Organization
MICHIGAN STATE UNIV
(N/A)
EAST LANSING,MI 48824
Performing Department
Animal Science
Non Technical Summary
Bovine leukemia virus (BLV) is a common infection in U.S. dairy herds. A 2007 USDA NAHMS study estimated that 83% of U.S. dairy herds are infected with BLV, and approximately 25%-50% of animals within aBLV-positiveherd are infected with BLV. Until recently, BLV was not considered to be economically important to dairy production in the U.S. In contrast, 21 European countries aggressively eradicated the disease and are now considered BLV-free. BLV infection rates in the U.S. are too high for aggressive strategies. Instead, lowering BLV infection rates will depend on producers and management strategies to reduce BLV infection.BLV infection rates in the U.S. are so high because the infection was thought to cause disease very rarely. Only 1%-10% of BLV-infected cows will develop cancer in their lifetime. However, it is likely that BLV has more negative effects on dairy herd health beyond cancer.BLV already costs the dairy industry $520 million every year, due to the lower milk production and shorter life expectancy of BLV-positivecows. BLV infection also likely causes immune suppression, which would put BLV-positivecows at risk for developing other infectious diseases that have a major economic impact on dairy production. The purpose of this project is to determineif BLV-positivecows are immune suppressed. Studying the immune system of BLV-positivecows is important for understanding overall herd health and production in U.S. dairy herds, which makes this project highly relevant to USDA-NIFA.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
31134101090100%
Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
3410 - Dairy cattle, live animal;

Field Of Science
1090 - Immunology;
Goals / Objectives
The first goal of this project is to determineif bovine leukemia virus (BLV)-infected dairy cows are less able to mount adaptive immune responses to other stimuli when compared to healthy, BLV-uninfected cows. This goal is in line with the larger investigation into whether BLV increases the susceptibility of dairy cows to other infectious diseases of econoomic importance. Because BLV is so widespread in American dairy herds, any immune suppressive effects of BLV infection could have a large, negative impact on both the welfare and production of dairy herds.The second goal of this project is to develop the skills and career of the project director as a scientist. The demands on the project director will enable learning critical skills including, but not limited to, managing a grant, directing a scientific program, scientific writing andgiving scientific presentations.
Project Methods
Experiment 1To characterize the strength of the primary immune response, adult lactating Holstein dairy cattle will be divided into three cohorts: BLV-, BLV+ aleukemic (AL) and BLV+ persistent lymphocytosis (PL). Each cohort will contain 20 animals, based on previous results and our power analysis. Disease status will be determined via BLV ELISA for positive or negative status and relative percent B cell prevalence in peripheral blood for AL or PL status. Keyhold limpet hemocyanin (KLH), a potent, non-pathogenic immune stimulant,will be used with the synthetic adjuvant dimethyl dioctadecyl ammonium bromide (DDA) as a novel antigen to stimulate a primary immune response that will mimic a primary pathogen exposure without causing an infection. A subset of animals will receive only adjuvant (3 BLV-, 3 BLV+ AL and 3 BLV+ PL). Animals will receive a subcutaneous injection of KLH and DDA or DDA only in the neck. Peripheral blood will be collected from the coccygeal (tail) vein of cattle on day 0, prior to immunization with KLH, and on days 7, 14, 21, 28, 35 and 50 after immunization. Animals will be boosted with KLH or DDA only, as appropriate, on day 14 post-immunization. This timeline of blood collection is based upon a previous study using KLH in cattle.A serum ELISA will be used to measure KLH-specific IgM, IgG1 and IgG2. PBMCs will be isolated from whole blood and RNA will be extracted to measure expression of interferon-gamma(IFNg), tumor necrosis factor-alpha(TNFa) and interleukin-2 (IL-2) mRNA. On days 0, 14, 28 and 50 post-inoculation, PBMCs will be isolated and cultured in the presence of no stimulant, KLH or PWM to measure antigen-specific B or T cell activation. B cell activation will be measured using multi-color flow cytometry: surface IgM (SIgM) as a marker for mature B cells, BLV gp51 as a marker of BLV expression, CD45R0 as a memory marker and CD25 as a marker of activation. T cell activation will also be measured using CD4 and CD8 as lineage specific markers, CD45R0 for memory cells and CD25 as a marker of activation.Once the initial immune response has waned, as measured by a return of serum antibody levels close to baseline, cattle will receive a booster of KLH and DDA (the negative control animals will receive a booster of only DDA). Peripheral blood will be collected prior to immunization on day 0, as well on days 3, 5, 7, 14, 21 and 35 post-immunization. The accelerated blood collection timeline is due to the expectation of a more rapid secondary immune response to KLH. Blood will be processed and immune responses assessed exactly as described above for the primary immune response.Experiment 2As in experiment 1, age-matched, adult, lactating dairy cattle will be divided into three groups based upon BLV status: BLV-, BLV+ AL and BLV+ PL. Cattle will be assigned to their groups based upon criteria discussed in experiment 1. 10 cattle will be enrolled in each group. Cattle will receive a booster dose of BoviShield Gold FP4 + L5 on their regular schedule.Whole blood will be collected from the coccygeal vein. Blood collection will occur on day 0 prior to the boost, as well as on days 7 and 14 post-boost. BHV-1-, BVDV-, BRSV- and Leptospira-specific IgM, IgG1 and IgG2 antibodies will be quantified by commercial ELISA. PBMCs will be isolated and separate aliquots used for RNA extraction and quantification of IFNg, TNFaand IL-2 expression and cultured with appropriate antigens for measurement of B and T cell activation using multi-color flow cytometry, as described in experiment 1.

Progress 12/15/15 to 12/14/17

Outputs
Target Audience: Other scientists studying bovine leukemia virus Veterinarians interested in the control and management of bovine leukemia virus infection Dairy farmers interested in control and management of bovine leukemia virus infection ? Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This project has provided multple opportunities for training and professional development activities. These have included writing scientific publications; presenting at national meetings including the Immunology 2017 conference; leading large projects involving commercial dairy herds and numerous undergraduate researchers; and collaborating with scientists within and outside of Michigan State University to further research into the effect of BLV infection on herd health and productivity. How have the results been disseminated to communities of interest? The results have been disseminated through two separate publications in the journal Frontiers in Veterinary Science, scientific presentations at national meetings and scientific presentations at a BLV-specific meeting hosted at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? It was important to establish whether BLV+ cattle have weakened immune systems because of the widespread prevalence of BLV infection in US dairy herds. Recent work from collaborators at Michigan State University suggests that over 90% of all dairy herds in the US are infected with BLV. Within an infected dairy herd, approximately 42% of cattle are infected, and today in the United States it is estimated that over 40% of all dairy cows are BLV+. When BLV was first discovered in the 1960s, it was determined that BLV did not affect the immune system of infected cattle. However, BLV was only found in 10% of dairy herds and more recent research suggested that BLV did negatively impact the immune function in infected cattle. With BLV infection rates as high as they are today, it was essential to determine whether BLV infection was negatively impacting herd health and production in US dairy herds. During the reporting period, we made significant advances in our understanding of the immune function in dairy cows naturally infected with BLV. We investigated both B and T cell responsesin vivoafter cattle were exposed to keyhole limpet hemocyanin to measure both primary and secondary immune responses to antigenic stimulation. The major findings of that study were that 1) antigen-specific IgM production was reduced in BLV+ cows even upon primary antigen exposure; 2) both memory B and memory gamma delta T cell populations were decreased in circulation in BLV+ cows; 3) BLV proviral load increased after antigenic exposure; 4) B cells from BLV+ cows responded abnormally to in vitrostimulation, regardless of active BLV viral expression; and 5) T cells from BLV+ cows exhibited a cytokine profile suggestive of Th2 polarization over Th1 polarization afterin vitrostimulation. The results of this study were published in July 2017 and demonstrate that BLV+ cows exhibit abnormal B and T cell immunity even after a primary immune exposure. We then investigated how BLV might directly affect IgM production in naturally infected cows. We collected circulating IgM+ B cells from BLV+ cows to quantify the level of BLV TAX transcription and BLV microRNA expression and compare those transcript levels to 1) circulating IgM levels and 2) transcript levels of B cell transcriptional regulators. We found that both BLV TAX and BLV microRNAs were found to correlate with changing levels of transcription factor transcripts, suggesting that BLV infection specifically interferes with B cell plasma cell development. This suggests a direct mechanism by which BLV interferes with antibody production in BLV+ cows and provides new exciting potential biomarkers that can be used as improved diagnostics to help reduce BLV infection rates within dairy herds. The results of this study were published in January 2018. Significant advancement was also achieved for the professional development of the PD. In addition to managing the final year of the grant, two first-author publications were written and another oral presentation was given at a national conference. Finally, collaborations with other scientists were strengthened to allow for multiple avenues of BLV research to come from the results of these research studies.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Frie, M.C., Sporer, K.R., Benitez, O.J., Wallace, J.C., Droscha, C.J., Bartlett, P.C., Coussens, P.M., 2017. Dairy cows naturally infected with bovine leukemia virus (BLV) exhibit abnormal B and T cell phenotypes after primary and secondary exposure to keyhole limpet hemocyanin. Frontiers in Veterinary Science, 4:112. doi: 10.3389/fvets.2017.00112
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Frie M.C., Droscha C.J., Greenlick A.E. and Coussens P.M., 2018. MicroRNAs Encoded by Bovine Leukemia Virus (BLV) Are Associated with Reduced Expression of B Cell Transcriptional Regulators in Dairy Cattle Naturally Infected with BLV. Frontiers in Veterinary Science 4:245. doi: 10.3389/fvets.2017.00245


Progress 12/15/15 to 12/14/16

Outputs
Target Audience:Other scientists studying bovine leukemia virus Veterinarians interested in the control and management of bovine leukemia virus infection Dairy farmers interested in control and management of bovine leukemia virus infection Changes/Problems:The initial project design included experiments to investigate the immune responses of BLV+ cows to both routine vaccination and primary and secondary immune stimulation. The results of the vaccine project have been published and all of the data for the primary and secondary immune stimulation has been collected and only requireanalysis. As a result of the common results between the two experiments showing lower IgM in BLV+ cows, and as a result of recently published work exploring the role of BLV microRNAs in viral pathogenesis, a new set of experiments has been designed to investigate the role of viral microRNAs in lower IgM production observed in BLV+ cows. This project will complement the proposed experiments that have already beencompleted. What opportunities for training and professional development has the project provided?The project has provided numerous training and professional development opportunities. These have included writing scientific publications;presenting at national meetings including the annual Association for American Immunologists meeting and the annual Conference for Research Workers in Animal Diseases meeting, where I received first place in the graduate student competition for oral presentations from the American Association of Veterinary Immunologists; overseeing and completing large projects involving commercial dairy herds, as well as the technical aid of numerous undergraduates and a post-doc; and collaborations with other researchers studying bovine leukemia virus at my own university, as well as at other organizations. How have the results been disseminated to communities of interest?The results have been disseminated through the publication of this work in the journal Veterinary Immunology and Immunopathology, as well as at annual scientific meetings and at a local meeting specifically about bovine leukemia virus at Michigan State University. What do you plan to do during the next reporting period to accomplish the goals?As the PD, I will complete analysis on the recent set of experiments investigating both primary and secondary B and T cell responses to stimulation in BLV- and BLV+ cows. Once analysis is complete, the results will be written up for publication in a scientific journal. In addition, a final project will investigate how BLV itself interferes with IgM production in BLV+ cows. This final project will investigate the role of viral microRNAs from BLV and how they negativly impact immunity in infected cows.

Impacts
What was accomplished under these goals? During the reporting period, significant gains have been made in understanding how well the adaptive immune system functions in BLV+ dairy cows. We completed a project investigating both B and T cell immunity in BLV+ cows in response to a boost with a mulitvalent vaccinetypically received by lactating dairy cows. We found that BLV+ cows produced lower levels of antigen-specific antibodies against both viral and bacterial antigens, and that BLV+ cows exhibited abnormal gamma delta T cell responses to antigen-specific stimulation in vitro. Surprisingly, we did not detect any significant differences in the activity of either CD4+ or CD8+ T cells in response toin vitrostimulation. The results of this study were published in December 2016 and support our hypothesis that BLV+ cows mount weaker adaptive immune responses to vaccination. In addition, the results of that study indicate that BLV+ cows may not be as protected against other infections after vaccination in comparison to healthy, BLV- cows. In addition, a second study was done to investigate the strength of BLV+ adaptive immunity in response to a novel antigen. Both the primary and secondary B and T cellresponses to immune stimulation were measured in both BLV- and BLV+ cows. The study began in September 2016 and was completed in mid-December 2016 and the results of this study are currently under analysis. During the reporting period, professional development for the PD progressed well. In 2016, I completed a major set of experiments as well as designed, initiated and completed a second major set of experiments to investigate immune competence in BLV+ cows. This undertaking involved both creating a budget for supplies and organizing large-scale sample collections at a commercial dairy farm. In addition, I completed my first first-author research publication and presented the results of my research at two annual meetings. In addition, I developed professional research collaborations with scientists at Michigan State University and at a private company associated with Michigan State University.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Frie MC, Sporer KR, Wallace JC, Maes RK, Sordillo LM, Bartlett PC, Coussens PM. 2016. Reduced humoral immunity and atypical cell-mediated immunity in response to vaccination in cows naturally infected with bovine leukemia virus. Vet Immunol Immunopathol 182:125-135.