Source: NORTH CAROLINA STATE UNIV submitted to NRP
DEFINING THE MECHANISM OF ACTION OF BERBERINE AGAINST THE INFLUENZA A VIRUS
Sponsoring Institution
State Agricultural Experiment Station
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0227389
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2011
Project End Date
Jul 1, 2013
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
NORTH CAROLINA STATE UNIV
(N/A)
RALEIGH,NC 27695
Performing Department
Microbiology
Non Technical Summary
Our laboratory is seeking to discover new treatments for influenza, also known as the flu; a respiratory disease caused by the influenza A virus. influenza is accompanied by a range of symptoms; from mild to moderate respiratory disease in healthy adults to severe, life-threatening infections in infants and the elderly. Indeed, over 30,000 Americans die annually from infections with influenza A. Vaccines, both inactivated and attenuated, can be used effectively to prevent influenza; however, many individuals are non-compliant and there are several segments of the population who do not derive full benefits from vaccination. infants under six months are not eligible for vaccination (they do not respond) and influenza infections in this group are often complicated by other infections, pneumonia, and hospitalization. the other major susceptible group is the elderly, who respond less well to the vaccine likely due to age-related decline in immune function. Two types of anti-viral drugs are also used to treat influenza; M2 pump inhibitors such as amantadine and rimantidine, and neuraminidase inhibitors including zanamivir and oseltamivir. Several problems are associated with the use of these drugs as well, including; viral resistance, side effects, and limited delivery options. Clearly there is a pressing need for the development of new methods to treat influenza A virus and inhibit the production of the inflammatory alkaloid berberine, which is found in high concentration in goldenseal extracts. Our goal is to define the molecular mechanisms underlying these effects. Understanding these mechanisms will determine, in part, whether berberine should be recommended for use in humans as a treatment of influenza
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
72240301090100%
Knowledge Area
722 - Zoonotic Diseases and Parasites Affecting Humans;

Subject Of Investigation
4030 - Viruses;

Field Of Science
1090 - Immunology;
Goals / Objectives
The general objective of this research is to define the molecular mechanisms underlying the anti-influenza effects of berberine and berberine-containing extracts of the goldenseal plant. Results from these investigations will be key to determining whether these materials should be recommended for the treatment of influenza in humans. We have divided our objective into three specific aims. Aim 1. Determine the mechanism by which berberine inhibits the growth of influenza A. Our studies to date show that while berberine strongly inhibits the projection of infectious virus, it does not block production of viral RNA'a, including vRNA, cRNA, and viral mRNA. In sedition, the projection of viral proteins is not inhibited by berberine. We have found, however, that in the presence of berberine, the viral HA protein does not localize to its normal position on the plasma membrane. Instead, large "aggregates" of the protein are formed in the perinuclear region o the cell. We hypothesize that berberine is causing this and other viral protein to accumulate in the ER thereby blocking formation of the infectious virions. We anticipate that it will take 1 year to complete this objective. If incorrect, and the aggregates we have observed are not located in the ER, we would seek to identify the nature of the aggregates and their position in the cell. Aim2. Determine the mechanism by which berberine inhibits the influenza A-induced production of the TNF. Our studies have shown that berberine inhibits production of mRNA. Our studies will be focused on determining the mechanism underlying this inhibitory effect. The amount of viral ligands (vRNA and cRNA) are not altered by berberine suggesting that its inhibitory effect targets the signaling pathway between cellular TLR and NLR receptors and transcription factors. We anticipate that these studies will take 2-3 years to complete. Aim 3. Determine the mechanism by which berberine inhibits the influenza A-induced production of PGE2. Our preliminary studies suggest that berberine is exerting both upstream and downstream effects on this pathway. Our data has lead us to hypothesize that a portion of the inhibitory action of berberine stems for effect(s) on one or more on the MAP kinases know to cause cPLA2activation. Experiments focused on the downstream effect of the berberine have failed to reveal an effect on the expression of activity of COX-2 or mPGES-2, the two key enzymes in this pathway. However, for pathway activity, these enzymes must assemble in a complex where product from one is passed directly to the other. Our working hypothesis is therefore that berberine is interfering with complex formation thereby blocking production of PGE@. These studies will be initiated after the completion of Aim 2, and we anticipate that they will take 2-3 years to complete.
Project Methods
Aim 1. Determine the mechanism by which berberine inhibits the growth of influenza A. Immunofluorescence microscopy will be used to determine whether know ER markers colocalize with HA in berberine treated cells. In addition we will use cell fractionation to determine whether HA and other viral proteins are preferentially found in the ER fraction. Aim2. Determine the mechanism by which berberine inhibits the influenza A-induced production of TNF. Inhibitors and interfering RNAs will be used to determine which specific TLRs and MLRs are active in the TNF pathway. Markers on those pathways will then be examined for susceptibility to inhibition by berberine. Reporter and ChlP assays will also be used in these studies. Aim 3. Determine the mechanism by which berberine inhibits the influenza A-induced projection of PGE2. Phosphospcific antibodies will then be used in western blots to estimate kinase activation status. Ratio imaging florescence microscopy to quantify the effects of berberine on levels of intracellular calcium. Immunofluorescience, confocal microscopy, and HPLC will also be used in these studies.

Progress 10/01/11 to 07/01/13

Outputs
Target Audience: Scientific peers Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? This project has served as the training vehicle for two PhD graduates, Chad Cecil and Bola Oyegunwa. How have the results been disseminated to communities of interest? Both PhD dissertations have been completed and published What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? The results of our experiments confirm that berberine is acting at multiple target points in the cell to interfere with influenza virus replication and the influenza-induced production of cytokines and inflammatory lipids. For example, we have noted partial inhiibition of the activity of cPLA2 by berberine during infleunza infection that results in partial inhibition of PGE2 production. We have also noted that berberine exerts an inhibitory effect on the final secretory stage of PGE2 production. Cumulatively, these effects result in strong net inhibition of PGE2 production. Similarly, multiple partial inhibitory effects were noted which account for the strong inhibition of TNF-a production. Berberine reduced, partially, production of TNF-a mRNA. Berberine also blocks the final stage of TNF-a production, release from the cell membrane. Previously, we have shown that berberine interferes with the intracellular movement of influenza A proteins. Together these results highlight the effects of berberine on the cellular machinery responsible for protein movment and secretory processes.

Publications


    Progress 10/01/11 to 09/30/12

    Outputs
    OUTPUTS: Our laboratory is investigating new treatments for influenza virus and its accompanying inflammation. We are studying the effects of extracts of the goldenseal plant (Hydrastis canadensis) and its major alkaloid berberine. We are also studying the effects of extracts of echinacea (Echinacea purpurea) and its alkylamides. We monitor inflammation via a number of parameters including signal transduction, transcription factor activation, and secretion of cytokines, chemokines, and inflammatory lipids. We utilize a number of different techniques including; virus growth assays, PCR, ELISAs, western blots, immunofluorescence and flow cytometry. Our results are disseminated in written form through the scientific literature and orally through seminars and scientific conferences. PARTICIPANTS: Cech, N. Collaborator. Dr. Cech is a medicinal chemist from UNC-Greensboro collaborating with us on this project. Davis, J. Collaborator. Dr. Davis is a horticulturalist from NCSU collaborating with us on this project. Oyegunwa, B. Post-doctoral fellow. Dr. Oyegunwa is a post-doctoral fellow working with us on this project. Gulledge, T. Graduate student. Mr. Gulledge is a PhD student working on this project. TARGET AUDIENCES: The target audience for our research is the academic/industrial community developing treatments for inflammation and virus infection. PROJECT MODIFICATIONS: Not relevant to this project.

    Impacts
    Our laboratory has shown previously that extracts of goldenseal, and its major alkaloid berberine, will inhibit the secretion of cytokines, chemokines, and inflammatory lipids from influenza A-infected cells. The results of our investigations suggest that this occurs via an effect on protein secretion. RT-PCR did not detect an effect of goldenseal extract or berberine on levels of TNF mRNA. Similarly, we did not detect an effect on intracellular levels of TNF by western blot or flow cytometry. We hypothesize therefore that one of the proteases induced during influenza infection is responsible for cytokine degradation soon after secretion. This mechanism would be novel and support continued investigation of goldenseal and its alkaloids for the treatment of inflammation.

    Publications

    • Cecil, C.E., Cech, N., Davis, J., and S.M. Laster. 2011. Inhibition of H1N1 influenza A virus growth and induction of inflammatory mediators by the isoquinoline alkaloid berberine and extracts of goldenseal (Hydrastis canadensis). Int. Immunopharm. 11:1706-1714.
    • Pollara, J.J., Spesock, A.H., Pickup, D.J., Laster, S.M., and I.T.D. Petty. 2012. Production of prostaglandin E2 in response to infection with modified Vaccinia Ankara Virus. Virology, 428:146-155.