A BAFFling tale: how does fingolimod affect B cells?

A
Fingolimod is an effective DMT which binds to the sphingosine-1-phosphate receptor on white blood cells. We don’t fully understand why it works in MS, but the most popular theory is that it traps lymphocytes inside the lymph nodes, preventing them from entering the blood and therefore from penetrating into the CNS. It may also have direct anti-inflammatory effects, protect the integrity of the blood-brain barrier, and (possibly) act directly in the CNS as a neuroprotective agent.

After people receive fingolimod, the number of B cells in the peripheral blood is suppressed. In addition, the B cells which remain in the blood are immature, so-called ‘transitional’ B cells. It is not fully understood how fingolimod does this, or whether this is relevant to the mechanism of benefit in MS.

BAFF is a signalling molecule involved in regulating the survival and proliferation of B cells. BAFF has received lots of attention in MS and other autoimmune diseaseas for a few reasons…
  1.  A rare variant in the gene for BAFF is associated with increased risk of MS and SLE, another autoimmune disease.
  2. BAFF levels go up after B cell depletion with drugs like ocrelizumab and rituximab.
  3. Atacicept, a BAFF inhibitor, made MS worse in a clinical trial.
  4. BAFF is an important regulator of B cells, and there is lots of emerging evidence we’ve blogged about elsewhere that B cells are central players in MS.

A new study investigated the relationship between BAFFlevels and B cell counts in response to fingolimod therapy. To do this, they first measured BAFF levels in the blood of 30 pwMS treated with fingolimod, 32 pwMS on no DMTs, and 25 healthy controls. Most of the people in the untreated group had never had DMTs (27/32) whereas 5 had had beta-interferon. The fingolimod-treated group had higher BAFF levels than both other groups. This suggested that fingolimod might increase BAFF levels in the blood. In support of a causal link, 3 people who had blood taken before and after fingolimod showed an increased in blood BAFF levels after starting treatment.


The authors then asked whether this increase in BAFF levels is related to changes in the numbers and types of B cells found in the blood after fingolimod treatment. Interestingly, BAFF levels were correlated with the total number of B cells. When these cells were looked at in a bit more detail, the authors found that increasing BAFF levels were associated with a shift in the relative make-up of these B cells: more BAFF was related to a higher proportion of transitional, immature B cells, and a lower proportion of memory B cells.

Here is a picture of the key graphs which I’ve rehashed:  

This study, for me, provides another important piece of evidence that BAFF is a master regulator of B cell pools in health, disease, and following administration of drugs, like fingolimod, which affect B cell numbers in the blood.

The emerging picture is that the body senses a decrease in the circulating B cell pool, aims to counteract this by producing more BAFF, and this subsequently leads to the release of transitional, immature B cells from the bone marrow, as we seen after B cell depletion therapy. The really interesting questions for me are
1) What is the sensor?
2) What is the key cell type (or types) responsible for producing BAFF in the body?




A better understanding of the relationship between BAFF and B cell pools will almost certainly improve our understanding of MS and other autoimmune diseases. As the atacicept nightmare tale shows us, hitting the BAFF axis can have a dramatic impact on disease activity. Knowing more about this axis will hopefully allow us to target BAFF in a way that benefits pwMS.  


***

Abstract

Patients with multiple sclerosis (MS) who are treated with fingolimod have an increased proportion of transitional B cells in the circulation, but the underlying mechanism is not known. We hypothesized that B cell-activating factor of the tumor necrosis factor family (BAFF) is involved in the process. Compared with healthy controls and untreated MS patients, fingolimod-treated MS patients had significantly higher serum concentrations of BAFF, which positively correlated with the proportions and the absolute numbers of transitional B cells in blood. Despite the elevated concentrations of BAFF in fingolimod-treated MS patients, serum levels of soluble transmembrane activator and calcium-modulating cyclophilin ligand interactor, and B cell maturation antigen were not elevated. Our results show that fingolimod induces BAFF in the circulation and expands transitional B cells, but does not activate memory B cells or plasma cells in MS, which is favorable for the treatment of this disease.

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17 comments

  • Contradictory?

    Fingolimod, an oral compound used for treatment of active MS, significantly reduces peripheral
    blood B cells but has only little impact on CSF B cell numbers in MS patients [83]. Moreover, fingolimod
    modulates the composition of circulating B cells; regulatory subsets, including those producing
    IL-10, are markedly increased and the cytokine profile is shifted towards a more anti-inflammatory
    phenotype [84,85]. In vitro, regulatory B cells exposed to fingolimod had an enhanced transmigrational
    capacity, which may explain why their frequency was increased in the CSF [85]. Ultimately, an increased
    influx of regulatory B cells may account for the apparent contradictory finding that the overall number
    of B cells in the CSF was not markedly reduced. Interestingly, a recent study demonstrated that
    fingolimod constrains the formation of organized B cell aggregates in the meninges in a B cell-driven
    EAE model, although the numbers of infiltrating B cells and plasma cells in the CNS parenchyma was
    not altered by fingolimod [86]

    Deciphering the Role of B Cells in Multiple
    Sclerosis—Towards Specific Targeting of
    Pathogenic Function

    Ps:They talk about barts paper…. 🙂

    Obrigado

  • What is the key cell type (or types) responsible for producing BAFF in the body?

    Expression of BAFF, APRIL and their receptors

    BAFF and APRIL are mainly produced by innate
    immune cells such as neutrophils, macrophages, monocytes,
    dendritic cells (DCs) and follicular DCs (FDCs)
    (reviewed in ReF. 31). Their expression is increased in the
    presence of type I interferons (IFNs), IFNγ, IL-10 and
    granulocyte colony-stimulating factor (G-CSF)31,32, as
    well as by the activation of Toll-like receptors (TLRs)
    such as TLR4 (ReF. 31) or TLR9 (ReF. 33). T cells34, activated
    B cells35 and B cell chronic lymphocytic leukaemia
    (BCLL) cells can also produce BAFF and APRIL and, in
    the case of BCLL, this contributes to tumour cell survival36.
    The production of BAFF and APRIL by innate
    immune cells and some lymphocytes supports ongoing
    immune responses

    https://www.ncbi.nlm.nih.gov/pubmed/19521398

    What is the role of BAFF in the decision that leads to
    B-cell maturation? T1 cells are present in normal numbers
    in BAFF-deficient mice, which indicates that T1
    cells do not depend on BAFF for survival48,49. Either differentiation
    to the T2 stage and/or the survival of T2
    cells must require BAFF-R signalling, but, at present,
    these two possibilities cannot be distinguished (FIG. 3).
    The BAFF-dependent survival of T2 cells is more probable,
    because BAFF promotes the survival of T2 B cells
    in vitro, stimulates the expression of the pro-survival
    oncoproteins Bcl-2 and Bcl-xL, and decreases the
    expression of the pro-apoptotic factors Bak and, potentially,
    Blk43,47,55.As B cells at this stage are vulnerable toapoptosis, BAFF could induce transitional B cells to
    overcome death signals that are triggered through their
    B-cell receptor (BCR). Therefore, pro-survival BAFF
    signalling might counter-balance the pro-apoptotic signals
    that are induced by the BCR.Maturation occurs
    only when the survival signals outweigh death signals
    (FIG. 4); mice that overexpress BAFF might disturb this
    balance and, hence, might be able to survive stronger
    death signals that are triggered by autoantigens. The
    result of this scenario would be the emergence of
    autoreactive B cells (FIG. 5).

    BAFF: A FUNDAMENTAL SURVIVAL
    FACTOR FOR B CELLS doi:10.1038/nri844

    Obrigado

  • The role of BAFF in autoimmunity
    Baff-transgenic mice develop severe autoimmune symptoms
    that are similar to systemic lupus erythematosus
    (SLE) and Sjögren’s syndrome in humans (reviewed in
    ReF. 31). However, as excessive BAFF production seems
    to support the survival of low-affinity self-reactive
    B cells in a complex B cell repertoire rather than resulting
    in a complete breakdown of B cell tolerance, can this
    event alone explain the devastating autoimmune disease
    that develops in Baff-transgenic mice? The current
    published literature on SLE agrees that the disease is
    mediated by several types of dysregulated immune cell:
    B cells, which can produce auto antibodies or present
    antigen to T cells; innate immune cells such as plasmacytoid
    DCs, which can produce high levels of stimulatory
    cytokines such as type I IFNs; and T cells, which
    are key players in the pathogenesis of SLE (reviewed
    in ReFS 88,89). Baff-transgenic mice have more effector
    T cells, but they also have a larger regulatory
    T cell compartment50. Furthermore, autoimmunity
    develops to the same extent in T cell-sufficent and
    T cell-deficient Baff-transgenic mice (FIG. 5), the first
    described animal model of T cell-independent lupus50,
    which indicates that T cells are not responsible for the
    autoimmune disorder of Baff-transgenic mice. T cellindependent
    activation of self-reactive B cells is not
    unique to the Baff-transgenic model, as similar conclusions
    were reached in another mouse model of
    autoimmunity90. Collectively, these findings show that
    chronic activation or survival of T cell-independent
    low-affinity self-reactive B cells mediated by BAFF can
    lead to a form of SLE. This suggests that some patients
    with SLE might benefit from B cell-depleting or
    BAFF-antagonist therapies.

    HGS
    and GSK have also agreed to test Lymphostat-B in
    patients with multiple sclerosis, as increased levels of
    BAFF have been detected in multiple sclerosis lesions44
    The second programme is led by ZymoGenetics in
    partnership with Merck Serono and is testing a TACI–Fc
    fusion protein (Atacicept), which blocks both BAFF and
    APRIL (unlike Lymphostat-B)99. Phase II and III clinical
    trials are currently in progress for the treatment of
    SLE, lupus nephritis, rheumatoid arthritis and relapsing
    multiple sclerosis. other haematological conditions are
    being tested in Phase I clinical trials. In general, Atacicept is
    well tolerated100 and has a good safety profile. Atacicept
    seems to be particularly promising for the treatment of
    SLE and rheumatoid arthritis and it could help patients
    who are not responding to TNF antagonists.
    An important question is whether the targeting of
    B cells through the BAFF and APRIL system will be
    as efficient as currently approved treatments for rheumatoid
    arthritis. Indeed, TNF antagonists and CD20-
    specific agents have set the bar high, and the lacklustre
    results from the Lymphostat-B Phase II clinical trial in
    rheumatoid arthritis indicate that inhibition of BAFF
    alone might not compare favourably with currently
    used treatments for rheumatoid arthritis. A caveat (or
    advantage) of blocking BAFF is that it targets mainly
    precursor B cell subpopulations rather than established
    antibody-producing clones or memory B cells56.
    Eliminating the de novo production of self-reactive
    B cells is crucial, but in some disease
    settings the elimination
    of established long-lived memory self-reactive
    B cells or autoantibody-producing cells might be as
    important

    Cracking the BAFF code
    Obrigado

  • These are nice – don't think this contradicts the idea that fingolimod enhances generation of regulatory B cells. This paper shows it clears them out quite well from the peripheral blood, immature B cells get released, and this is probably controlled by BAFF. During the repopulation it might be that the cells that come back are biased towards a Breg phenotype

  • Thanks for reply

    "fingolimod had an enhanced transmigrational"

    I thought that Fingo…Prevent Migracion of lymphocytes in the brain?

    Obrigado

  • Help to the lay person with MS. I went off Fingolimod and started ocrelizumab. In this article I am trying to understand which is the better drug. I know everyone is different etc.

    • "ask which depletes memory B cells the best and then you ha(v)e an answer"

      Well..that's what I am asking..but I can't find an answer or
      direct comparison.

      Memory B cell depletion percentage

      1._____________
      2._____________
      3._____________

  • Great post thanks Ben. B b b brilliant to see more B cell research!
    Dear Luis, I carefully read the post and think I'm getting there. …then you produce more to read! Thanks, I'll do my best to keep up 😉
    Have a good weekend everyone, thanks for posts and comments 🙂

  • This study suggest that Baff-var status should be accessed and guide treatment decisions

    Nevertheless, besides supporting BAFF as a
    target in multiple sclerosis and SLE, our results
    have implications for clinical research. A pertinent
    one, to be assessed in further studies,

    would be that patients stratified according to
    BAFF-var status might show a differential benefit
    from anti-BAFF therapies. One might also
    anticipate that patients carrying BAFF-var would
    have a weaker response to B-cell–depleting
    therapies owing to a faster resurgence of memory
    B cells.32 In fact, patients with SLE with
    higher basal levels of BAFF have been found to
    have poorer or shorter clinical responses to
    rituximab than those with lower levels.33,34

    Overexpression of the Cytokine BAFF and Autoimmunity Risk

    DOI: 10.1056/NEJMoa1610528

    Obrigado

  • Hi all – yeah monitoring BAFF for treatment response is an interesting idea. We and others have started talking about monitoring memory B cell return in people being treated with B cell-depleting drugs. This has been done for neuromyelitis optica already. If BAFF levels in the blood are predictive of how quickly the B cells are repopulating then yes, it's definitely a candidate biomarker for looking at treatment response. Not enough good data on it yet though

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