Lecture 6

Development of B Cells

 Ó 2007 by Alma Moon Novotny.  All rights reserved.

 

“Most of what we once thought we knew about global health has been proved wrong by the relentless advances of HIV/AIDS, tuberculosis and malaria…..There can be no more urgent cause facing us today.  In Africa, the enemy is already among us.  In Asia, the enemy is at the gates.” – Richard G. A. Feachem, Houston Chronicle, 1/21/03.

 

I.        B-Cell Maturation - review figure 5-1, page 112

This is the process that turns a hematopoietic stem cell into a naïve, but antigen-responsive, B cell, figure 11-1, page 272.

A.     Initial Steps (Bone Marrow)

 

1.      Stem cell commits to lymphoid line.

2.      Lymphoid progenitor commits to progenitor B cell, or pro-B cell, which develops a tyrosine receptor called CD45R and has Iga/Igb transmembrane signal (figure 4-22, page 102)

3.      Pro-B cells begin gene rearrangement and differentiate into pre-B cells upon stimulation by the stromal cells, figure 11-2, page 273.

 

B.     Differentiation and Gene Rearrangement (bone marrow), figure 11-3, page 274.  

 

1.      Pro-B cells bring DH and JH together, figure 5-5, page 118.

2.      Then they add leader plus VH to DHJH, and do the P and N nucleotide additions.

3.      If this produces a non-productive (frame shifted) gene rearrangement, then they try the other allele.

4.      If the rearrangement is productive, then the heavy chain is put into the membrane with a surrogate light chain, composed of the products of two genes that can function without rearrangement (figure 11-4, page 275). 

5.      The immature receptor associates with the Iga/Igb transmembrane signal (figure 4-22, page 102).

6.      Once there is a productive H chain gene, the cell is a pre-B cell.  If there is no productive rearrangement, the cell apoptoses.

7.      The pre-B cell then undergoes rearrangements of first one k, then the other, and one l, then the other, stopping as soon as there is a productive light chain arrangement and ultimately apoptosing if there is not.

8.      Once you have two productive rearrangements, you have an immature B cell, one that has a determined antigenic specificity (CDR) and uses the m CH region to produce membrane-bound antibody.

9.      Shortly thereafter, the cell also begins to express membrane-bound d CH, and become a mature (but naïve) B cell, expressing IgM and IgD on the cell surface.

10.  At this point the cells are released into the plasma and head to the peripheral (secondary) lymphoid organs: lymph nodes, spleen and mucosa.

 

C.     Removing Self-Reactive B Cells. 

 

1.      90% of the B cells produced by the above process never make it to the plasma. 

2.      The elimination is signaled by the crosslinking of IgM. 

3.      Artificially crosslinking IgM will lead to apoptosis of developing B cells.

4.      However, B cells can sometimes get a second chance. 

5.      If they have a k chain involved in the CDR for a self-antigen, they may try to replace it with a l.  If the new CDR does not recognize a self-antigen, then the cell is rescued and can enter the plasma.

II.     B-Cell Activation and Proliferation

 

A.     Antigen Exposure, figure 11-9, page 280

 

1.      If a circulating B cell does not encounter an antigen that can bind to its surface antibody, it will undergo apoptosis and die within a few weeks.

2.      Thymus independent (TI) antigens are those that can activate a B cell directly. These antigens also simultaneously activate toll-like receptors.

a.       Type 1 antigen - lipopolysaccharide such as those found in the outer bacterial cell walls of gram negative bacteria, which also activates TLR4

b.      Type 2 - repetitive polymeric proteins, such as bacterial flagellin, can cross link the membrane-bound immunoglobulins and kick off proliferation. 

3.      However, this process does not induce class switching (you mostly just make IgM) and does not produce memory cells.  For that you need TH cells. 

 

B.     Activating Signals

 

1.      Recall that while a mIgM or mIgD molecule can bind antibody, it doesn’t stick far enough into the cell to transduce this as a signal to the interior, figure 11-8, page 280.

2.      The cytoplasmic tails of the Iga/Igb stick into the cell and participate in a tyrosine kinase signaling pathway.  The tails of the molecules constitute the immunoreceptor tyrosine-based activation motif, or ITAM. 

3.      When an antigen cross-links one antibody with the next outside the cell, it brings together the internal receptor molecules.

4.      This causes the complex to change conformation and recruits src (the original enzymes were isolated from cells infected with Rous sarcoma virus) tyrosine kinases (blk, lyn, fyn) that add phosphates to the tyrosines of the BCR, figure 11-9b, page 280.

5.      This triggers multiple internal signaling pathways that lead to changes in gene expression, the transcription factor NF-κB being involved in this.  The is the same transcription factor activated by toll-like receptors, figure 11-10 page 282

6.      CD-22 signaling provides brakes on the system

C.     Role of TH cells, figure 11-12, page 285

 

1.      However, the BCR does not signal effectively without contact with a TH cell.

2.      When B cells bind antigen, they bring some it inside and hydrolyze it.

3.      Some of the hydrolyzed peptide winds up attached to class II MHC molecules, the genes for which are upregulated along with the one for B7.

4.      Thus the B cell can present some of the antigen to a TH cell and also contact the T cell using B7 to CD28.

5.      Te cells attach, forming a conjugate or immune synapse, figure 11-13, page 286.

6.      This causes the TH cell to produce CD40L, which is a juxtacrine factor that turns around and signals the B cell through CD40 receptor.

7.      The contact reorganizes the interior of the TH cell so that cytokines are released toward the B cell.

8.      The B cells begin producing receptors for the cytokines.

9.      Cytokine signaling activates the B cells and they begin proliferating and differentiating.

III.   Primary Versus Secondary Response, Table 11-4, page 290, figure 11-16, page 289

 

A.     The Primary Response

 

1.      naïve lymphocytes

2.      4 to 7 day lag time

3.      produces antibody secreting plasma cells and memory cells

4.      initial antibodies mostly IgM; IgG toward the end

B.     The Secondary Response: The Sadder, but Wiser, Immune System

 

1.      Produced primarily by memory cells

2.      1 to 3 day lag time

 

a.       The number of memory cells specific for the antigen increases.

b.      These memory cells are more easily activated.

c.       They have already been through affinity maturation, so they're better at binding antigen

3.      more antibody secreted, and over a longer time

4.      much higher proportion of IgG and other isotypes

 

IV.  B-Cell Maturation in Anatomical and Histological Context

 

A.     Lymph Nodes, figure 11-17, page 292 - primary site for B cell maturation. 

1.      Lymph drains from tissues and passes through these.

2.      Antigen enters. It can be

 

a.       "free" - particle from pathogen, or the whole bacteria or viruses themselves

b.      proteins or other antigens from the pathogens complexed with antibodies

c.       carried in by presenting cell (dendritic or macrophages) that have picked it up elsewhere

3.      Free and antibody-bound antigen in the plasma is likely to be picked up by

 

a.       interdigitating dendritic cells

b.      macrophages,

c.       follicular dendritic cells

4.      Naïve lymphocytes from the bone marrow enter via the lymph.

5.      Activation begins in the paracortex, the layer between the outer cortex and the inner medulla, where there is a high concentration of T cells, macrophages, and dendritic cells.

6.      First the macrophages and the dendritic cells activate the TH  cells.

7.      Naïve B cells contact the TH cells, presenting any antigen they have internalized via the class II MHC, and forming a conjugate (immune synapse) as previously discussed

8.      The B cell begins to divide, producing a clonal cluster (focus) at the boundary between the paracortex and cortex.

9.      A few activated B and TH cells migrate together from one of these foci to a primary follicle in the cortex.

10.  The follicle becomes a secondary follicle, one with a germinal center where B, TH, and follicular dendritic cells interact, figure 2-15, page 44

11.  A reminder about follicular dendritic cells: these are NOT regular sentinel dendritic cells.. 

B.     Germinal Centers (figure 11-20, page 294) 

1.      Activated B cells (centroblasts) proliferate and move to one edge or the follicle, forming a dark zone. At this stage the centroblasts:

 

a.       enlarge and begun to divide rapidly

b.      begin somatic hypermutation- mutating the regions in the heavy and light chain genes that code for the variable loops. 

c.       stop displaying the membrane Ig (recycles the original via membrane turnover) 

2.      The centroblasts differentiate into centrocytes which

 

a.       stop dividing

b.      begin expressing membrane Ig

c.       move into light zone

d.      contact follicular dendritic cells

e.       undergo selection B cells with more effective receptors will survive and multiply at a greater rate, out-competing those B cells with antibody receptors less capable of competing for antigen-antibody complexes.

3.      What happens in the follicles is a highly unusual form of accelerated natural selection. 

 

a.       random mutation (dark zone)

b.      excess reproduction (dark zone)

c.       selection (light zone) -

4.      The centrocytes leave the germinal center as plasma cells, lose their surface antibody again, and begin secreting antibodies.

5.      Most centrocytes do not contact an antigen that fits with their surface receptors, however, and these die by apoptosis, and are recycle by macrophages.

6.      Purpose  - The environment of the light zone selects for those centrocytes that express the most effective antibodies. 

a.       The maturing B cell that enters the germinal center and begins dividing does so if it can bind (with its surface antibody) to some degree an antigen currently arriving in the lymph node.

b.      It differentiates into a centroblast that undergoes random mutational events to the very region of the gene responsible for determining the effectiveness of this antigen binding (the CDR).

c.       The mutated centrocyte now displays the new antibody at its surface.

d.      As with most random mutations, most of the progeny centrocyte cells produced by this will bind antigen less effectively than the original cell.

e.       A few however, will bind the antigen more effectively.  These will compete more effectively in the next stage for the antigen-antibody beads supplied by the follicular dendritic cells.  Cells with improved receptors divide more rapidly than cells with less effective receptors.

            7.  Signals

 

a.       Follicular dendritic cells play an important role in the selection process. The (iccosome) beads are essentially a scarce resource, and the centrocytes have to compete for them.

b.      Thus the more effectively the centrocyte surface antigen binds to the antibody displayed by the follicular dendritic cell, the more likely it is to live.

c.       In addition, the centrocytes have to receive signals from the TH cells, especially the contact of CDC40L to the CDC40. 

C.     Class Switching – directed by TH cells, figure 11-22, page 296

 

1.      The next decision the future plasma cell must make is exactly what class of antibody to send out with the refined CDR region produced by affinity maturation.

2.      Cytokine signals from the TH cells will determine this (more later).

 

D.     To Remember or to Act: The Final Decision.

 

1.      Centrocyte now decides whether to become a plasmoblast and generate a plasma cell or become a memory cell and wait for a subsequent exposure to antigen.

2.      Recall that plasma cells do not express membrane-bound antibody. This means that the sequence of differentiation in the lymph node involves:

a.       dividing mature B cells with surface antigen

b.      dividing centroblasts with no surface antigen (undergoing hypermutation)

c.       non-dividing centrocytes expressing surface antibody and undergoing selection

d.      dividing plasma cells not expressing surface antibody secreting soluble (humoral) antibody

3.      The final differentiation to a plasma cell involves the switch that generates the splicing enzymes that do not add the membrane spanning exons to the mH chain message.

4.      Also transcription and translation levels generally rise as the cell begins cranking out antibody, as does the proportion of RER.

5.      Memory cells set aside from this process may resemble naïve B cells, but they have undergone class switching and make a variety of heavy chains, Table 11-6, page 297.

6.      The receptors of memory cells may therefore also be membrane-bound versions of IgG, IgA, and IgE.

V.     Regulation

 

A.     B-Cell Differentiation

 

1.      B-Cell Specific Activator Protein (BSAP) functions as master regulator.

2.      Present ONLY in members of the B cell lineage.

3.      Present in ALL members of the B cell lineage EXCEPT mature plasma cells, which are done differentiating.

4.      Binds to a variety of B-cell gene promoter regions, including those like the surrogate L chains and class switching regions that are involved in developmental decision making.

5.      High levels tend to maintain a cell as a memory cell, low levels tend to promote formation of plasma cells.

 

B.     Overall Immune Effector Response - Tolerance

 

1.      You would like NOT to make antibodies against your own proteins, and therefore tolerate them.

2.      On the other hand, you do NOT want to develop tolerance for foreign antigens, especially those associated with pathogenic infection. 

3.      Constant monitoring of your antigens by Treg cells suppresses immune responses to your own proteins and to those of benign commensal bacteria and fungi.

4.      Moreover, you need to apply brakes once an infection is under control

5.      If you introduce foreign antibodies to an antigen, this will tie up the antigen and prevent it from promoting an immune response on the part of the host:

 

a.       measles-mumps-rubella after 1 year

b.      biological warfare

 

B-lineage Development Summary

 

name

location

Surface receptor molecule

Other surface signaling molecules

activity

Pro B cell

Bone marrow

Igα/Igβ and co-receptor

C-kit, CD45R, VLA-4. IL-7 receptor, CD19, CD 43

Rearranging heavy chain gene

Pre B

Bone marrow

Heavy chain plus surrogate light chain and co-receptor

CD45R, VLA-4. IL-7 receptor, CD25 (α chain of IL-2 receptor)

Rearranging heavy gene

Immature B cell

Bone marrow

mIgM and co-receptor

No CD 25

Undergoing selection against self-recognition, changing RNA processing

Mature, naïve B cell

Circulates: plasma, secondary and tertiary lymphoid tissue

mIgM and mIgD and co-receptor

 

Trolling for antigen.  Antigen binding and activation necessary for next stage

Activated B cell - 1

Peripheral lymphoid tissue (lymph nodes as example) at paracortex

mIgM and mIgD and co-receptor

 

Begins clonal expansion

Activated B cell - 2

Cortex, primary follicle, which then become secondary, with germinal center

mIgM and mIgD and co-receptor

Up-regulate MHCII, CD 40, various cytokine receptors

Associate with T cells

centroblast

secondary follicle, periphery (dark zone) of the germinal center

No surface Ig receptor

 

Divide rapidly, mutate Ig genes at specific regions of CDR loops

centrocyte - 1

Cortex,  now secondary follicle, periphery, light zone

altered mIgM and mIgD and co-receptor

CD40 (sign from CD40L necessary, too)

Stop division, compete for antigen displayed on follicular dendritic cells.

centrocyte - 2

Cortex,  now secondary follicle, periphery, light zone

altered mIgM and mIgD and co-receptor

CD40 (sign from CD40L necessary, too)

Decide whether or not to class switch and whether or not to become a memory cell

plasmablast

Lymph node

none

 

Switch to non-membrane spanning heavy chain and up-regulation of Ig synthesis

plasma cell

Circulation, site of infection

none

 

Secretes antibody

 

Connections:

 

1.      Properties of antigen that affect binding to antibodies, Lecture 4, III

2.      Antigen-presenting cells and follicular dendritic cells, Lecture 2, II

3.      Lymph nodes and spleen, Lecture 2, V

4.      Generation of antibody diversity, Lecture 5, II

5.      Autoimmunity, Lecture 16

6.      TH cell cytokine signaling, Lecture 11, III

7.      Hypersensitivity (Allergy), Lecture 15

8.      Passive Immunity and Vaccines, Lecture 19

 

References and Links:

Bill and Melinda Gates Foundation 

Lecture outlines

 

 

Immunobiology Home

Rice Home