Source: UNIV OF WISCONSIN submitted to NRP
CALCIUM HOMEOSTASIS IN TRANSITION DAIRY CATTLE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1000022
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Sep 1, 2013
Project End Date
Aug 31, 2018
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIV OF WISCONSIN
21 N PARK ST STE 6401
MADISON,WI 53715-1218
Performing Department
DAIRY SCIENCE
Non Technical Summary
Periparturient disorders are not only disastrous to the farmer but they are responsible for substantial decreases in overall herd health. Periparturient paresis results in a 14% decrease in milk production in the subsequent lactation, with a cost of $334/animal per incidence (Erb et al., 1984; Oetzel, 1988). Additionally, subclinical hypocalcemia affects 25-50% of cows and costs $125/animal/incidence. Prevention of hypocalcemia in dairy cattle could save the dairy industry approximately $140 million each year. This project focuses on delineating a novel pathway for the regulation of calcium mobilization of bone during the transition period. A cow that survives the transition period free of disease can be expected to have a successful lactation period, with high hopes for efficient reproductive performance. The ability to produce an adequate amount of milk, as well as to reproduce is absolutely critical to the dairy farmer maintaining economic viability of the farm operations, as well as to satisfy human food needs. Hypocalcemia has been demonstrated to be responsible for blunted immune cell response to stimuli, reduction of smooth muscle contraction, and increased risk for reproductive disorders placing animals at a higher risk of mastitis, retained fetal membranes, displaced abomasum, dystocia, and ketosis, all of which lead to a decreased production life (Erb et al., 1984; Kimura et al., 2006; Goff, 2008; Reinhardt et al., 2010). The average reduction in productive life of an animal overcome with milk fever is 3.4 yr (Horst et al., 1997). Reduced animal productivity is a major economic detriment to the dairy farmer, particularly when the primary source of income is derived from the amount of milk each animal successfully produces in a respective lactation cycle. Therefore, this project is important because it will be critical to demonstrating a novel mechanism for the regulation of hypocalcemia in transiton cattle.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
30534991020100%
Knowledge Area
305 - Animal Physiological Processes;

Subject Of Investigation
3499 - Dairy cattle, general/other;

Field Of Science
1020 - Physiology;
Goals / Objectives
To determine the role of serotonin in regulating calcium mobilzation during the periparturient period in dairy cattle.
Project Methods
Experiment 1. Determine circulating and milk concentrations of 5-HT, PTHrP and calcium in Holstein and Jersey cattle throughout their pregnancy/lactation cycle. This goal of this experiment is to determine the patterns of 5-HT, PTHrP and calcium in the circulation and milk throughout the pregnancy/lactation cycle (d -30 partum through an entire 305 day lactation cycle) of multiparous Holstein and Jersey cattle from local commercial dairy farms in Wisconsin. Whole blood will be collected to analyze 5-HT (ELISA, Enzo Life Sciences) and calcium ( Additionally, we seek to determine the bone turnover of jersey cattle throughout the pregnancy/lactation cycle (d -30 partum through an entire 305 day lactation cycle) through the measurement of a bone turnover marker, C-telopeptide (CTx) fragments of collagen type I in serum (Serum CrossLaps Elisa; Immunodiagnostics systems; Holtenius and Ekelund, 2005). Samples will be collected on d -20, and d -5 through d +5, d +30, d +60, d +90, d +150, and d +300 relative to parturition. Milk samples will be collected daily for the first 10 d post-partum to measure PTHrP and calcium. We will collect samples from 25 Jersey and 25 Holstein cows, for a total of 50 animals, as this will convey a power of 0.9786 when performing R-square tests for multiple correlations between variables. Additionally, in order to compare variables between breeds, 25 animals per breed will provide a power of 0.7915, with a detectable contrast of 0.80 when conducting a balanced ANOVA. Additionally, we will obtain herd records for each animal to determine the incidence of various transition related disorders, as well as to determine daily milk yield in each of these animals. Experiment 2a. Determine the ability of selective 5-HT receptor agonists to stimulate PTHrP, and the ability of selective 5-HT receptor antagonists to inhibit PTHrP in lactogenic cultures of bovine mammary epithelial cells. Primary bovine mammary epithelial cells (pBMEC) possess five 5-HT receptor subtypes (Hernandez et al., 2009). Studies suggest that the 5-HT2B receptor subtype is responsible for 5-HT induction of PTHrP in the mammary gland (Hernandez et al., 2012). However the contribution of the other four receptor subtypes have yet to be investigated in bovine mammary epithelial cells in relation to stimulation of PTHrP. pBMEC will be cultured in a 3-D lactogenic model as previously described (Stiening et al., 2008; Hernandez et al., 2008; Hernandez et al., 2009). After 8 d in culture with serum-free proliferation media, pBMEC will be switched to a lactogenic media in combination with gel release (Stiening et al., 2008; Hernandez et al., 2008; Hernandez et al., 2009). Concentration response curves (1/2 log) will be performed on pBMEC cultured in a 3-D lactogenic model and treated with the following selective agonists/antagonists, respectively, (5-HT1B: CP-94253 hydrochloride/SB-216641 hydrochloride; 5-HT2A: TCB-2/R-96544 hydrochloride; 5-HT2B: BW-732C86/SB-204741; 5-HT4: zacopride hydrochloride/GR-113808; 5-HT7: LP-44/SB-258719) for 72 hr. pBMEC will then be collected for RNA isolation using the TriReagent Protocol (Molecular Research Products) and subsequently will be reverse transcribed into cDNA (iScript Reverse Transcription Kit; BioRad). Quantitative real-time PCR (qPCR) will then be performed for PTHrP using ssoFast Eva Green (BioRad). qPCR data will be analyzed using the 2-ΔΔCt method (Livak and Schmittgen, 2001; Schimttgen and Livak, 2008). Results will be analyzed using a one-way analysis of variance (ANOVA) with a Tukey's post-test to make pair-wise comparisons. Experiment 2b. Delineation of the molecular signaling pathway responsible for 5-HT induction of PTHrP in the bovine mammary gland through siRNA-mediated knockdown of the 5-HT2B receptor. This experiment is designed as a follow-up to the pharmacological experiments performed demonstrating the role of the 5-HT2B receptor in calcium regulation in the mammary gland through 5-HT induction of PTHrP (preliminary experiments). We will utilize RNAi technology in pBMEC isolated from both Jersey and Holstein cattle to demonstrate the contribution of the 5-HT2B receptor to the regulation of PTHrP expression in the bovine mammary gland. We will be using either transient or stable expression of ON-TARGET plus siRNA dual strand chemical modification for receptor of interest in our experiments. This method has been validated by Dharmacon (Thermo Scientific) to reduce miRNA-induced off targets by preventing sense strand from being blocked by RISC uptake to favor the antisense strand loading and reducing sense strand-induce off targets. This protocol is also modified within seed region to destabilize miRNA-like activity and improve specificity to the desired targets for the most potent knockdown. Target sequences will be designed according to published and proprietary rules. Sequences will be BLAST aligned to the bovine genome sequences. At least four siRNA sequences for each target mRNA (5-HT2B) will be synthesized and tested for effectiveness at silencing the gene. Transfection will be performed using a lipid-based tranfection protocol, INTERFERin in vitro siRNA protocol (Polyplus) in pBMEC in monolayer cultures. A double transfection will be performed for the respective siRNAs to ensure effective silencing (of at least 70%) of the gene of interest. Additionally, a control gene siRNA (GAPDH) and non-targeting siRNA will be used as controls to determine transfection efficiency. Knockdown efficiency will be measured through qPCR for respective genes to demonstrate the percent inhibition of respective genes. The RNAi sequence for the 5-HT2B target that provides the most effective knockdown will be utilized for subsequent experiments. The variables that will be subsequently assayed upon silencing the 5-HT2B receptor include PTHrP mRNA expression and protein levels, and phospholipase C-β (PLC-β) activity levels. Additionally, we will examine PKC activity, as this molecule is downstream of PLC-β. We will also determine activity levels of ERK1/ERK2 MAP kinases, as this pathway has been shown to be regulated by the 5-HT2B receptor (Raymond et al., 2001). mRNA levels will be quantified using qPCR techniques previously described. Activity levels for PLC-β, PKC, and ERK1/2 MAP kinases will be determined using activity assays per manufacturer's instructions from Worthington Biochemical Corporation, Enzo Life Sciences, and Chemicon International, respectively.

Progress 09/01/13 to 08/31/18

Outputs
Target Audience:As a result of the research conducted through funding by this HATCH grant, we presented data at a hypocalcemia think tank led by an industry group who develops products for prevention of hypocalcemia. Data collected by this grant has been presented at numerous Nutirtion conferences across the country that are attended by Dairy nutritionists, Farmers, Sales representatives for various nutritional products, and scientists in the field (Southwest Nutrition Conference, 4-State Nutiriton Conference, Midwest ADSA Dairy Extesion Symposium, 8th International Conferece in Farm Animal Endocrinology, Annual Meeting of the European Federation of Animal Science, Cornell Nutrition Conference, Western Large Dairy Herd Management Conference, Tri-State Dairy Nutrition Conference, Minnesota Milk Conference, Vita Plus Dairy Summit, etc.). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A master's student, and 3 Ph.D. students were supported over the course of the grant. Three of the 4 students have graduated and the last student will defend in March of 2019. How have the results been disseminated to communities of interest?We have presented our data at numerous national meetings of the American Dairy Science Association, as well at conferences that are optimized to reach the dairy industry and nutrition community. Additionally, we have published numerous manuscripts in a variety of research journals. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Yes, we now have an idea of what normal circulating serotonin concentrations are in lactating dairy cattle, and we know that these concentrations change drastically around the time of calving in a similar fashion to circulating calcium concentration. We determined the optimal dose for use of 5-hydroxy-L-tryptophan prepartum to induce changes in calcium postpartum that improve postpartum calcium status. We determined that treatment with 5-hydroxy-L-tryptophan prepartum alters bone mobilization in dairy cows, and increases milk calcium excretion. We also observed that there are breed differences between Jersey and Holstein cows and how they respond to 5-hydroxy-L-tryptophan prepartum treatments postpartum. We also determined that treatment with 5-hydroxy-L-tryptophan prepartum did not effect postpartum energy metabolites, however we did see improvements in prolifeartion of liver cells.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Elevation of circulating serotonin improves calcium dynamics in the dairy cow transition period
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Weaver SR, Fricke HP, Xie C, Lipinski RJ, Vezina CM, Charles JF, Hernandez LL. Peripartum fluoxetine reduces maternal trabecular bone after weaning and elevates mammary gland serotonin and PTHrP. 2018. Endocrinology. 2018 Aug 1;159(8):2850-2862. doi: 10.1210/en.2018-00279.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Cheng AA, Hernandez LL, Li W. The effect of high-fat diet feeding and associated transcriptome changes in the peak lactation mammary gland in C57BL/6 dams. 2018. Physiol Genomics. 2018 Oct 19. doi: 10.1152/physiolgenomics.00052.2018. [Epub ahead of print].
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Weaver SR, Fricke HP, Xie C, Aiello RJ, Charles JF, Hernandez LL. Peripartum dietary supplementation of a small molecule inhibitor of tryptophan hydroxylase 1 compromises infant, but no maternal, bone. 2018. Am J Physiol Endocrinol Metab. 2018 Oct 23. doi: 10.1152/ajpendo.00198.2018. [Epub ahead of print]


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:The target audience of my research program are the members of the dairy industry. In particular, are members of the nutrition community who prepared diets for dairy herds. Also of importance are the farmers themselves to be aware of basics of physiology for cows during their at most-risk time period being early lactation. The research is also important for the scientific community of lactation biologists. The research we perform in the cow model is not only important for the dairy industry, but is also important for lactating mothers. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This proposal supports one graduate student will be finishing in Mary 2019 with a PhD. How have the results been disseminated to communities of interest?Data was presented at the American Dairy Science Association meeting in 2017 in Pittsburgh, PA. NIFA support was acknowledged on the posters. I have also presented previous data collected through this funding at meetings for nutritionists and farmers in the dairy science community (Tri-State Dairy Nutrition Conference (4/2017), Minnesota Nutrition Conference (9/2017), Minnesota Milk Producers (11/2017), and VitaPlus Dairy Summit (12/2017)). What do you plan to do during the next reporting period to accomplish the goals?We will be presenting new data this summer at the American Dairy Association Meeting in Knoxville, TN. We also will have two manuscripts prepared and hopefully accepted by the end of 2018. I plan to submit a new NIFA proposal when the call is available to the Nutrition, Growth, and Lactation section.

Impacts
What was accomplished under these goals? We completed a project in the Fall of 2017 in which we are processing tissues. The aim of this project was to determine if increasing sertonin epigenetially affects mammary gland calcium transport during lactation. We are currently processing these tissue samples and will be preparing abstracts for the American Dairy Science Association and a manuscript for submission in the upcoming year. Additionally, we have been able to associate the effects of serotonin on calcium homeostasis with immune function in early periparturient dairy cows. This data will be important in understanding the physiology of serotonin during early lactation in dairy cows. Better understanding of how serotonin effects calcium and immune function in this critical time period will be important for the overall health and welfare of the lactating dairy cow. The data generated from this study and others performed over the course of this grant has already been leveraged for one USDA-NIFA grant and will be used in this upcoming year to submit a new proposal to USDA-NIFA on the role of serotonin and epigentic control of mammary gland function as it pertains to calcium.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: TRIENNIAL LACTATION SYMPOSIUM/BOLFA: Serotonin and the regulation of calcium transport in dairy cows. Hernandez LL. J Anim Sci. 2017 Dec;95(12):5711-5719. doi: 10.2527/jas2017.1673.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Elevating serotonin pre-partum alters the Holstein dairy cow hepatic adaptation to lactation. Weaver SR, Prichard AS, Maerz NL, Prichard AP, Endres EL, Hern�ndez-Castellano LE, Akins MS, Bruckmaier RM, Hernandez LL. PLoS One. 2017 Sep 18;12(9):e0184939. doi: 10.1371/journal.pone.0184939. eCollection 2017.


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:We have presented data in several arenas. Data has been presented at 5 different technical conferences that are for the purpose of educating the dairy nutrition industry. Typically, dairy nutritionists of all levels attend these conferences in order to gather new information on how to better formulate diets for their dairy herds, as well as improve the overall health and well-being of those animals. Data was also presented at the American Dairy Science Association as well as at the European Animal Science Association Meetings this past year. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?I trained one graduate student. Her experience from working on this project the last two years prepared her to write a successful pre-doctoral grant. This allowed me to take another Ph.D. student into the laboratory. How have the results been disseminated to communities of interest?We have presented our data at several nutrition conferences, as well as at the American Dariy Science Association Meeting and the European Animal Science Assocation meetings. Finally, we have had popular press articles written in the agriculture community about our research we recently published in the Journal of Endocrinology (Agriculture News, etc.). What do you plan to do during the next reporting period to accomplish the goals?We are currently analyzing data from another animal experiment as well as from cell culture experiments that will aid in further understanding serotonin's actions.

Impacts
What was accomplished under these goals? We have demonstrated that giving the precursor to serotonin, 5-hydroxy-L-tryptophan, to pre-partum dairy cows improves calcium homeostasis during early lactation. Furthermore, we demonstrated that their are differences that exist between how Holstein and Jersey cows respond to this treatment to enusre improved calcium status post-partum. Additionally, we have demosntrated that treatment with 5-hydroxy-L-tryptophan pre-partum also decreases beta-hydroxybutyrate concentrations in post-partum dairy cows, suggesting a possiblity of application for the prevention of ketosis.

Publications

  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Elevation of circulating serotonin improves calcium dynamics in the peripartum dairy cow. J. Endocrinol. 230(1):105-123. 2016
  • Type: Journal Articles Status: Under Review Year Published: 2016 Citation: Prepartum infusions of 5-hydroxy-L-tryptophan alter the metabolic adaptation to lactation in the post-partum period. American Journal of Physiology.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2016 Citation: Novel concepts regarding calcium homeostasis during the transition period Proceedings of the Florida Ruminant Nutrition Conference. February 2016.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Serotonin and the physiology of calcium homeostasis during the transition period Proceedings of the Cornell Nutrition Conference.


Progress 10/01/14 to 09/30/15

Outputs
Target Audience:During this reporting period, we have presented data from experiments at the American Dairy Science Association and the International Congress on Farm Endocrinology. We have also presented data at the 4-State Nutrition Conference, which is targeted for producers and nutritionists in the dairy science field. We have also published two manuscripts related to this proposal in 2014, and three in 2015. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This proposal currently supports the education of a Ph.D. student. This student is completing research as well as taking courses. Additionaly, the student travled to two professional meetings to present regarding this project. How have the results been disseminated to communities of interest?We have presented data at the American Dairy Science Association Meetings, International Congress on Farm Animal Endocrinology and the 4-state nutrition conference for producers and nutrition professionals. Also, all publications by the PI are posted on her laboratory website. A review paper is being published based on the presentation at the International Congress and a conference paper was published in the proceeedings of the 4-state nutrition conference. What do you plan to do during the next reporting period to accomplish the goals?Several manuscripts are being prepared to be submitted regarding the goals of this experiments. Additionally, a new Hatch proposal will be written based on the findings we have made throughout the project.

Impacts
What was accomplished under these goals? We have determined that serotonin is a major regulator of calcium metabolism in dairy cows. Our reserach has demonstrated the serotonin regulates calcium sensing within the mammary gland and is responsible for triggering the production of PTHrP, which then is responsible for mobilizing the bone calcium necessary to maintain maternal calcium homeostasis during early lactation. We have shown that serotonin concentrations fluctuate widely over a lactation and established average circulating concentrations of serotonin in the cow. Furthermore, we have demonstrated that administration of a serotonergic precurso improve calcium status in the dairy cow, as well improving glucose metabolism. The implications of these resultsare that we can manipulate serotonin in the dairy cow to improve their transition from pregnancy to lactation. Not only have we more thoroughly delineated the mechanisms by which serotonin regulates calcium sensing and trafficking in the mammary gland, but we have also shown that serotonin is critical to the maintenance of energy homeostasis as well. These findings lay the framework for developing a novel way to improve the health of early lactating dairy cows.

Publications

  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Serotonin regulates calcium homeostasis in lactation by epigenetic activation of hedgehog signaling.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Peripheral serotonin regulates maternal calcium trafficking in mammary epithelial cells during lactation in mice.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Patterns of circulating serotonin and related metabolites in multiparous diary cows in the peripartum period.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Increasing serotonin concentrations alter calcium and energy metabolism in dairy cows.


Progress 10/01/13 to 09/30/14

Outputs
Target Audience: We presented at a meeting with a company that develops products relevant to prevention of hypocalcemia. We also made a presentation at a meetings for nutritionists, producers and scientists. We made an additional presentation at our annual American Dairy Science Association Meeting. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? A master's student completed their thesis work and succesfully defended their thesis. How have the results been disseminated to communities of interest? We have made three presentations at three different meetings regarding our data. Addtiionally we have a manuscript under review. What do you plan to do during the next reporting period to accomplish the goals? We are currently working on determining the molecular mechanisms underlying our responses in a cell culture model, as well as working on a method to deliver a serotonin precursor to transition dairy cows to prevent hypocalcemia.

Impacts
What was accomplished under these goals? We have now established normal circulating serotonin concentrations in lactating dairy cattle, and that they are dynamic over the course of a lactation. Specifically, they fluctuate around calving in a similar fashion to calcium.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2015 Citation: metabolites in multiparous dairy cows in the peripartum period Journal of Dairy Science


Progress 09/01/13 to 09/30/13

Outputs
Target Audience: We have collected all our blood and milk samples from the Jersey and Holstein Farms that are the focus of the Aim looking at patterns of circulating serotonin and calcium in multiparous dairy cattle over the course of an entire lactation. Early lab analysis indicates that serotonin concentrations in the circulation fluctuate in a similar pattern to that of ionized calcium. Additionally, it appears that Jersey cattle have more severe drops in calcium levels, which was expected, however we also seem to see this in terms of serotonin at the time of calving as well. We are currently running analysis of PTHrP concentrations in the circuation and serotonin concent in the milk. We aim to have a manuscript ready for submission by the summer of 2014 in regards to this particular experiment. Additionally, the master's student working on this project is scheduled to defend his thesis in August of 2014. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project supports one master's student currently. This student has collected all the samples for the commercial cow study and is currently running laboratory analyses. This student will defend their thesis in August 2014. Once this student has finished the commercial cow study and defended, a PhD student will begin the cell culture experiments described in the proposal. This portion of the project will begin in September 2014. How have the results been disseminated to communities of interest? A presentation will be given at the Southwest Nutrition Management Conference in Phoneix Arizona in 2014 that will report some of the findings from teh project. Once the laboratory analyses are conducted the manuscript will be written and submitted to the Journal of Dairy Science. What do you plan to do during the next reporting period to accomplish the goals? The laboratory analyses will be finished for the commerical cow study and then the manuscript for that portion of the project will be written and submitted. We have already identified the PhD student that wil begin in September 2015, working on the cell culture portion of the proposal.

Impacts
What was accomplished under these goals? We have demonstrated that serotonin does indeed follow a similar circulating pattern at the time of calving in multiparous dairy cattle to that of ionized calcium.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2013 Citation: Dairy Science Meetings, Indianapolis IN, 2013