Skip to content

Mechanisms of Regulation and Dysregulation of the Immune System

Chapter 361 | Harrison's 22e · Part 11 – Rheumatology & Immunology · Chapter 361


Key Clinical Points

  1. Immune homeostasis requires a balance between protective immunity and the prevention of self-damage or overreaction.
  2. T-cell activation requires two signals: primary (MHC/peptide to TCR) and secondary (co-stimulation, primarily CD28 binding to B7-1/B7-2).
  3. Immune checkpoints (e.g., CTLA-4, PD-1) act as 'brakes' to prevent over-activation; their inhibition is a cornerstone of modern cancer immunotherapy.
  4. Cytokines are key soluble proteins mediating growth, activation, and inflammatory responses.
  5. Monoclonal antibodies targeting specific cytokines (TNF-α, IL-6, IL-17) are mainstay treatments for various autoimmune and inflammatory diseases.
  6. IVIg works by blocking reticuloendothelial cell function and immune complex clearance in conditions like ITP and Kawasaki disease.
  7. CAR T-cell therapy utilizes engineered receptors to bypass natural TCR limitations and target specific antigens (e.g., CD19) on malignant cells.
  8. Genetic mutations in genes like AIRE, FOXP3, and STATs lead to significant immune dysregulation and autoimmunity.
  9. Central tolerance occurs primarily in the thymus via T-cell deletion; peripheral tolerance involves anergy, inhibitory signaling, and Treg suppression.
  10. Specific autoantigens (e.g., GAD65, Myelin-basic protein) are linked to specific clinical conditions like Type 1 Diabetes or Multiple Sclerosis.

DEFINITION & CLASSIFICATION

Anergy:

Definition (Harrison's 22e): A reversible tolerance mechanism in which the T or B cell is in an unresponsive state following an antigen encounter but remains alive.

Chimeric antigen receptor T cells (CAR T):

Definition (Harrison's 22e): Synthetic hybrid receptors created by recombinant techniques that combine an extracellular domain, usually derived from an antibody single-chain variable fragment (scFv), with intracellular signaling domains from activating co-stimulatory molecules (from endogenous T-cell receptors [TCRs], CD28, or 4-1BB) that allow for retargeting of T cells to antigens on malignant cells.

Checkpoint inhibition therapy:

Definition (Harrison's 22e): A form of cancer immunotherapy where antibodies against T-cell or antigen-presenting cell regulators of immune cell inhibition are used to activate cytotoxic T cells to kill tumor cells.

Co-stimulation of T cells:

Definition (Harrison's 22e): A secondary signal that T cells require for activation following presentation of peptide antigen by major histocompatibility complex (MHC) molecules to TCRs on either CD4 or CD8 T cells. A prime mediator of co-stimulation is the T cell CD28 molecule binding to B7-1 (CD80, CD86) on antigen-presenting cells.

Cytokines:

Definition (Harrison's 22e): Soluble proteins that interact with specific cellular receptors that are involved in the regulation of the growth and activation of immune cells and mediate normal and pathologic inflammatory responses.

Immune homeostasis:

Definition (Harrison's 22e): Balanced protective immunity that does not overreact to pathogens and harm the host, and immunity that is not deficient and does not predispose the host to harmful infections or malignancies.

Immunoediting:

Definition (Harrison's 22e): Process of immunity selecting clones of cancer cells with reduced immunogenicity resulting in tumor escape.

Natural killer cells:

Definition (Harrison's 22e): Lymphocytes with cytotoxic potential for host cells must deliver an activating co-stimulating signal in addition to TCR ligation. To avoid responding to cells bearing self-antigens, T cells must also maintain immune tolerance.

T-cell exhaustion:

Definition (Harrison's 22e): State of T cells when the persistence of antigen disrupts memory T-cell function, resulting in defects in memory T-cell function.


ETIOLOGY & PATHOPHYSIOLOGY

Mechanisms of Immune Tolerance

Central Tolerance: Occurs in the Thymus. Mechanism: TCR editing by V(D)J, thymic negative selection, T-cell anergy and inhibitory signaling, and T regulatory cell differentiation.

Peripheral Tolerance: Occurs in Peripheral Lymphoid Tissues. Mechanisms: ◦ T-cell competition for cytokines: IL-2, IL-7, IL-15, and peptide-MHC. ◦ T-cell growth dependence on co-stimulatory molecules (e.g., CD28 ligands). ◦ Suppression of T- and B-cell responses by T regulatory cells and TGF-β, IL-10. ◦ Regulation of T follicular helper cell differentiation and function.

B-Cell Tolerance: Occurs in Bone Marrow. Mechanism: Immature B cell maturation arrest and deletion.

Peripheral B-cell Tolerance: Mechanisms: ◦ B-cell growth dependence on TCR ligands. ◦ BCR modulation of plasma cell differentiation. ◦ Germinal center B-cell dependence on T follicular helper cells (CD40L, IL-21).

Genetic Basis of Immune Dysregulation

Monogenetic Mutations: Several mutations lead to specific immune failures or autoimmunities (Table 361-1). ◦ RAG1, RAG2: Lead to severe combined immune deficiency (Omenn’s syndrome) with autoreactive T cells. ◦ AIRE: Deficiency leads to APECED syndrome (autoimmunity, polyneuropathy, candidiasis, ectodermal dysplasia). ◦ STAT-1/STAT-3: → STAT-1 deficiency → decreased IFN-γ, susceptibility to TB. → STAT-1 gain of function → chronic mucocutaneous candidiasis with autoimmune diseases. → STAT-3 deficiency → hyper-IgE syndrome (Job’s syndrome). → STAT-3 gain of function → lymphopenia, autoimmune cytopenias, diabetes, enteropathy. ◦ FcεRII, FcεRIII, C-reactive protein, complement receptor for C3bi (ITGAM or compliment receptor 3), COPA, tripeptidyl peptidase: Lack of removal of cell debris leads to systemic lupus erythematosus; COPA leads to autoimmune lung, renal, joint disease. ◦ AID (Activation-induced cytidine deaminase): Leads to Hyper IgM syndrome type 2, low IgA, IgG, and autoimmune cytopenias.


MANAGEMENT & TREATMENT

Cytokine Inhibitors

  1. TNF-α Blockade: Used in rheumatoid arthritis, psoriasis, Crohn’s disease, and ankylosing spondylitis. → Agents: Monoclonal antibodies (adalimumab, infliximab, golimumab), TNF-R Fc fusion proteins (etanercept), and IL-1ra (anakinra).
  2. IL-1 Inhibition: Inhibits pathogenic cytokines; soluble IL-1 receptor antagonist (anakinra) or other inhibitors.
  3. IL-6 Inhibition: Tocilizumab inhibits IL-6 activity.
  4. T-cell Differentiation & Signaling: Targeting IL-12, IL-23 (to inhibit T 17 CD4 T cell differentiation) or direct anti-IL-17 antibodies for psoriasis and psoriatic arthritis.
  5. IFN-γ Therapy: Used in the treatment of the phagocytic cell defect in chronic granulomatous disease.

Immune Modulatory Therapies

  1. Intravenous Immunoglobulin (IVIg): Mechanism: Blocks reticuloendothelial cell function and immune complex clearance. Indications: Immune cytopenias (e.g., ITP), Kawasaki disease, GvHD, MS, MG, GBS.
  2. Stem Cell Transplantation (SCT): Goal: Replace dysfunctional immune system with a normally reactive repertoire. Applications: SLE, MS, scleroderma. → Note: Patients homozygous for the 32-bp deletion in the CCR5 allele (Δ32) are resistant to HIV-1 strains using the CCR5 co-receptor.
  3. CAR T-cell Therapy: Mechanism: Uses engineered receptors (e.g., anti-CD19) to target malignant cells. Structure: Includes extracellular antigen recognition domain (scFv) and intracellular signaling/co-stimulatory domains (CD3ζ, CD28, or 4-1BB). Outcome: Leads to cell killing, proliferation, and cytokine release.

Checkpoint Inhibition

  1. Anti-CTLA-4: Blocks CTLA-4 to allow CD28 binding → Enhanced effector activity.
  2. Anti-PD-1/PD-L1: Blocks PD-1 interaction with ligands (PD-L1, PD-L2) → Prevents inhibition by SHP2 → Enhanced effector activity.
  3. Approved Agents (Table 361-2): → Ipilimumab (CTLA-4) → Nivolumab, Pembrolizumab (PD-1) → Atezolizumab, Durvalumab (PD-L1) → Relatlimab + Nivolumab (LAG-3 + PD-1) → Retifanlimab, Toripalimab (PD-1) for Merkle cell cancer.

KEY PEARLS & HIGH-YIELD POINTS

Immune Checkpoint Balance: The balance between co-stimulatory molecules (e.g., CD28, OX40) and inhibitory checkpoints (e.g., CTLA-4, PD-1) is critical for immune homeostasis. → Blockade of these 'brakes' is a primary strategy in cancer immunotherapy.

Autoantigen Specificity: Specific autoantigens are linked to distinct clinical syndromes (Table 361-4). → GAD65 → Type 1 diabetes, stiff-person syndrome. → Myelin-basic protein → Multiple sclerosis. → Citrullinated proteins → Rheumatoid arthritis.

Monoclonal Antibody Utility (Table 361-5): A wide range of monoclonal antibodies are approved for both autoimmune diseases and malignancies. → VEGF inhibitors: Bevacizumab, Ramucirumab, Aflibercept, Ranibizumab. → IL-4Rα: Dupilumab. → FcεR: Omalizumab. → α-4 integrin: Vedolizumab, Natalizumab. → Complement inhibitors: Eculizumab, Pozelimab. → FcRn: Rozanolixizumab. → IL-1 inhibitors: Canakinumab, Rilonacept. → IL-6 inhibitors: Siltuximab, Tocilizumab. → BAFF inhibitor: Belimumab. → SLAMF7 inhibitor: Elotuzumab.


Reference Tables

TABLE 361-1 Monogenetic Mutations That Lead to Immune Dysregulation and Autoimmunity

Harrison's 22e, p.2786

MUTATIONS AND FUNCTIONAL DEFICITS DISEASES OR SYNDROME
RAG1, RAG2; lymphopenia with recombinase deficiency Severe combined immune deficiency (Omenn’s syndrome) with autoreactive T cells
AIRE, deletion chromosome 22q11.2; decrease in central tolerance Ch. 22q11.2: DiGeorge’s syndrome with autoimmune T cells
AIRE: autoimmunity, polyneuropathy, candidiasis, ectodermal dysplasia (APECED syndrome)
STAT-1, STAT-3; modulation of type 1 interferons STAT-1 deficiency: decreased IFN-γ, susceptible to TB
STAT-1 gain of function: chronic mucocutaneous candidiasis with autoimmune diseases
STAT-3 deficiency: hyper-IgE syndrome (Job’s syndrome)
STAT-3 gain of function: lymphopenia, autoimmune cytopenias, diabetes, enteropathy
FcfRII, FcfRIII, C-reactive protein, complement receptor for C3bi
(ITGAM or compliment receptor 3), COPA, tripeptidyl peptidase;
lack of removal of cell debris
FcfII, FcfIII, CRP, complement receptor for C3bi: systemic lupus erythematosus
COPA: autoimmune lung, renal, joint disease
Tripeptidyl peptidase II: susceptibility to bacterial, viral, and fungal pathogens
Activation-induced cytidine deaminase (AID); class-impaired
B-cell development
Hyper IgM syndrome type 2, low IgA, IgG, recurrent bacterial switch recombination; infections,
autoimmune cytopenias, SLE

TABLE 361-2 Summary of the Tumor Types for Which Immune Checkpoint Blockade Therapies Are Approved by the U.S. Food and…

Harrison's 22e, p.2787

TUMOR TYPE THERAPEUTIC AGENT TARGET FDA APPROVAL YEAR
Melanoma Ipilimumab CTLA-4 2011
Nivolumab PD-1
Melanoma Pembrolizumab PD-1 2014
Nivolumab PD-1
Non-small-cell lung cancer Pembrolizumab PD-1 2015
Ipilimumab + nivolumab CTLA-4 + PD-1
Melanoma (adjuvant) Ipilimumab CTLA-4 2015
Nivolumab PD-1
Hodgkin’s lymphoma Nivolumab PD-1 2016
Atezolizumab PD-L1
Head and neck squamous cell carcinoma Nivolumab PD-1 2016
Pembrolizumab PD-1
Melanoma (any BRAF status) Ipilimumab + nivolumab CTLA-4 + PD-1 2016
Atezolizumab PD-L1
Hodgkin’s lymphoma Pembrolizumab PD-1 2017
Avelumab PD-L1
Urothelial carcinoma Avelumab PD-L1 2017
Durvalumab PD-L1
Urothelial carcinoma Nivolumab PD-1 2017
Pembrolizumab PD-1
MSI-high or MMR-deficient solid tumors of any histology Pembrolizumab PD-1 2017
Nivolumab PD-1
Pediatric melanoma Ipilimumab CTLA-4 2017
Nivolumab PD-1
Gastric and gastroesophageal carcinoma Pembrolizumab PD-1 2017
Durvalumab PD-L1
Renal cell carcinoma Ipilimumab + nivolumab CTLA-4 + PD-1 2018
Dostarlimab PD-1
Melanoma Relatlimab + nivolumab LAG-3 + PD-1 2022
Tremelimumab CTLA-4
Merkle cell cancer Retifanlimab PD-1 2023
Toripalimab PD-1

TABLE 361-3 Immune Tolerance Checkpoints in T- and B-Cell Immunity

Harrison's 22e, p.2789

CENTRAL TOLERANCE PERIPHERAL TOLERANCE
THYMUS PERIPHERAL LYMPHOID TISSUES
– TCR editing by V(D)J – B- and T-cell anergy and inhibitory signaling (CTLA-4, PD-1, and other checkpoint molecules)
– T-cell anergy and inhibitory signaling – T-cell competition for IL-2, IL-7, IL-15, and peptide-MHC
– T-cell growth dependence on CD28 ligands and other co-stimulatory molecules
– Suppression of T- and B-cell responses by T regulatory cells and TGF-β, IL-10
– Regulation of T follicular helper cell differentiation and function
BONE MARROW
– Immature B cell maturation arrest – B-cell growth dependence on TCR ligands
– Immature B cell deletion – BCR modulation of plasma cell differentiation
– Germinal center B-cell dependence on T follicular helper cells (CD40L, IL-21)

TABLE 361-4 AUTOANTIGEN Cell- or Organ-Specific Autoimmunity Acetylcholine receptor Actin Adenine nucleotide translator…

Harrison's 22e, p.2790

AUTOANTIGEN AUTOIMMUNE DISEASES AUTOANTIGEN AUTOIMMUNE DISEASES
Cell- or Organ-Specific Autoimmunity Aminoacyl-tRNA synthetase (several) Polymyositis, dermatomyositis
Acetylcholine receptor Myasthenia gravis Cardiolipin Systemic lupus erythematosus,
antiphospholipid syndrome
Actin Chronic active hepatitis, primary biliary
cirrhosis
Carbonic anhydrase II Systemic lupus erythematosus, Sjögren’s
syndrome, systemic sclerosis
Adenine nucleotide translator (ANT) Dilated cardiomyopathy, myocarditis
Collagen (multiple types) Rheumatoid arthritis, systemic lupus
erythematosus, progressive systemic
sclerosis
β-Adrenoreceptor Dilated cardiomyopathy
Aromatic l-amino acid decarboxylase Autoimmune polyendocrine syndrome
type 1 (APS-1)
Centromere-associated proteins Systemic sclerosis
Asialoglycoprotein receptor Autoimmune hepatitis
DNA-dependent nucleoside-
stimulated ATPase
Dermatomyositis
Bactericidal/permeability-increasing
protein (Bpi)
Cystic fibrosis vasculitides
Fibrillarin Scleroderma
Calcium-sensing receptor Acquired hypoparathyroidism
Fibronectin Systemic lupus erythematosus,
rheumatoid arthritis, morphea
Cholesterol side-chain cleavage
enzyme (CYP11a)
Autoimmune polyglandular syndrome 1
Glucose-6-phosphate isomerase Rheumatoid arthritis
Citrullinated proteins Rheumatoid arthritis
β2-Glycoprotein I (B2-GPI) Primary antiphospholipid syndrome
Collagen type IV-α3-chain Goodpasture’s syndrome
Golgin (95, 97, 160, 180) heat shock
protein
Sjögren’s syndrome, systemic lupus
erythematosus, rheumatoid arthritis,
various immune-related disorders
Cytochrome P450 2D6 (CYP2D6) Autoimmune hepatitis
Desmin Crohn’s disease, coronary artery disease
Desmoglein 1 Pemphigus foliaceus Hemidesmosomal protein 180 Bullous pemphigoid, herpes gestationis,
cicatricial pemphigoid
Desmoglein 3 Pemphigus vulgaris
Histone H2A-H2B-DNA Systemic lupus erythematosus
F-actin Autoimmune hepatitis
IgE receptor Chronic idiopathic urticaria
GM gangliosides Guillain-Barré syndrome
Keratin-8 Rheumatoid arthritis
Glutamate decarboxylase (GAD65) Type 1 diabetes, stiff-person syndrome
Ku-DNA-protein kinase Systemic lupus erythematosus
Glutamate receptor (GLUR) Rasmussen encephalitis
Ku-nucleoprotein La phosphoprotein
(La 55-B)
Connective tissue syndrome Sjögren’s
syndrome
H/K ATPase Autoimmune gastritis
17-α-Hydroxylase (CYP17) Autoimmune polyglandular syndrome 1 Myeloperoxidase Necrotizing and crescentic
glomerulonephritis, systemic vasculitis
21-Hydroxylase (CYP21) Addison’s disease
IA-2 (ICA512) Type 1 diabetes Proteinase 3 (PR3) Granulomatosis with polyangiitis
(Wegener’s), Churg-Strauss syndrome
Insulin Type 1 diabetes, insulin hypoglycemic
syndrome (Hirata’s disease)
RNA polymerase I–III (RNP) Systemic sclerosis, systemic lupus
erythematosus
Insulin receptor Type B insulin resistance, acanthosis,
systemic lupus erythematosus
Signal recognition protein (SRP54) Polymyositis
Intrinsic factor type 1 Pernicious anemia Topoisomerase-1 (Scl-70) Scleroderma, Raynaud’s syndrome
Leukocyte function-associated
antigen (LFA-1)
Treatment-resistant Lyme arthritis Tublin Chronic liver disease, visceral
leishmaniasis
Myelin-associated glycoprotein (MAG) Polyneuropathy Vimentin Systemic autoimmune disease
Myelin-basic protein Multiple sclerosis, demyelinating
diseases
Plasma Protein and Cytokine Autoimmunity
C1 inhibitor Autoimmune C1 deficiency
Myelin oligodendrocyte glycoprotein
(MOG)
Multiple sclerosis
C1q Systemic lupus erythematosus,
membrane proliferative
glomerulonephritis
Myosin Rheumatic fever
p-80-Collin Atopic dermatitis Cytokines (IL-1α, IL-1β, IL-6, TNF-α,
IFN-γ IL17A, IL-17F, GM-CSF)
IL-1α, IL-1β: rheumatoid arthritis,
systemic sclerosis, systemic lupus
erythematosus; IL-6: bacterial infections;
IFN-γ: bacterial infections, varicella-
zoster virus reactivation; IL-17A, IL-17F:
chronic mucocutaneous candidiasis;
GM-CSF: pulmonary alveolar proteinosis,
fungal infections
Pyruvate dehydrogenase complex-E2
(PDC-E2)
Primary biliary cirrhosis
Sodium iodide symporter (NIS) Graves’ disease, autoimmune
hypothyroidism
SOX-10 Vitiligo
Thyroid and eye muscle shared
protein
Thyroid-associated ophthalmopathy
Factor II, factor V, factor VII, factor
VIII, factor IX, factor X, factor XI,
thrombin vWF
Prolonged coagulation time
Thyroglobulin Autoimmune thyroiditis
Thyroid peroxidase Autoimmune Hashimoto’s thyroiditis
Glycoprotein IIb/IIIg and Ib/IX Autoimmune thrombocytopenia purpura
Thyrotropin receptor Graves’ disease
IgA Immunodeficiency associated with
systemic lupus erythematosus,
pernicious anemia, thyroiditis, Sjögren’s
syndrome, and chronic active hepatitis
Tissue transglutaminase Celiac disease
Transcription coactivator p75 Atopic dermatitis
Tryptophan hydroxylase Autoimmune polyglandular syndrome 1
Tyrosinase Vitiligo, metastatic melanoma Oxidized LDL (OxLDL) Atherosclerosis
Tyrosine hydroxylase Autoimmune polyglandular syndrome 1 Cancer and Paraneoplastic Autoimmunity
Systemic Autoimmunity Amphiphysin Neuropathy, small-cell lung cancer
Adrenocorticotropic hormone (ACTH) ACTH deficiency Cyclin B1 Hepatocellular carcinoma
Aminoacyl-tRNA histidyl synthetase Myositis, dermatomyositis DNA topoisomerase II Liver cancer

TABLE 361-5 Monoclonal Antibodies Approved for Clinical Use in Autoimmune Disease, Some of Which Are Also Used in…

Harrison's 22e, p.2792

TARGET
MOLECULE
FUNCTION FDA-APPROVED mAbs, TRAPS,
AND BISPECIFIC mAbs
AUTOIMMUNE/
INFLAMMATORY
MALIGNANCY OTHER/COMMENTS
Cytokine that stimulates
vasculogenesis
and angiogenesis.
Overproduced in some
inflammatory disorders and
tumors to induce increased
blood supply.
Bevacizumab (Avastin)
Ramucirumab (Cyramza)
Aflibercept (Eylea/Zaltrap)
Ranibizumab (Lucentis)
Age-related macular
degeneration, macular
edema, diabetic
macular edema, diabetic
retinopathy
Colorectal cancer,
nonsquamous
NSCLC,
breast cancer,
glioblastoma,
renal cell
carcinoma,
gastric cancer or
gastroesophageal
junction
adenocarcinoma
IL-4 receptor
alpha subunit
Receptor that mediates
IL-4 and IL-13-induced
inflammation
Dupilumab (Dupixent) Atopic dermatitis
(eczema), steroid-
dependent asthma
Binds to mast cells,
basophils, and other cells
that express Fc-epsilon
receptor and induces
release of inflammatory
cytokines
Omalizumab (Xolair) Asthma
Alpha-4 integrin Alpha-4 integrin facilitates
exit of inflammatory cells
from blood into intestine
or across the blood-brain
barrier
Vedolizumab (Entyvio)
Natalizumab (Tysabri)
Multiple sclerosis, Crohn’s
disease, and ulcerative
colitis
IgG4 natalizumab therapy has
been associated with PML
caused by John Cunningham
virus in immunocompromised
patients. IgG1k vedolizumab
may not be associated with
PML.
Inhibits complement
cascade
Eculizumab (Solaris)
Pozelimab (Vepoz)
Prevents destruction
of red blood cells by
activated complement
(paroxysmal nocturnal
hemoglobinuria)
Treats complement
hyperactivation,
angiopathic thrombosis,
and protein-losing
enteropathy (CHAPLE)
FcRn Delivers IgG antibodies to
tissues
Rozanolixizumab (Rustiggo) Myasthenia gravis IgG4. Rozanolixizumab binds
to human neonatal Fc receptor
(FcRn), thus reducing the
concentration of pathogenic
IgG autoantibodies.
Mutations in cryopyrin lead
to overproduction of IL-1
and inflammatory disease;
IL-1 also drives other
inflammatory diseases
Canakinumab (Ilaris)
Rilonacept (Arcalyst)a
Rare inflammatory
syndromes, active
juvenile arthritis, gouty
arthritis
IL-6 Overexpression of IL-6 is
associated with multiple
malignancies
Siltuximab (Sylvant) Pseudo-
malignancy:
Castleman’s
disease (similar to
lymphoma)
Murine/human chimeric IgG1κ
Current approvals based
on role of IL-6 in promoting
inflammatory autoimmune
disease
Tocilizumab (Actemra) Rheumatoid arthritis,
polyarticular juvenile
arthritis, juvenile
idiopathic arthritis
BAFF (tumor
necrosis factor
superfamily
member 13b)
Role in proliferation and
differentiation of B cells
Belimumab (Benlysta) Systemic lupus
erythematosus
IgG1-γ/λ
SLAMF7 triggers
the activation and
differentiation of a wide
variety of immune cells
(innate and adaptive
immune response) perhaps
primarily mediated by
natural killer cells and
myeloma cells
Elotuzumab (Empliciti) Multiple myeloma