Tissue transglutaminase (tTG), also known as transglutaminase 2 (TG2) or protein-glutamine γ-glutamyltransferase 2, is a multifunctional calcium-dependent enzyme that catalyzes the formation of isopeptide bonds between the γ-carboxamide group of glutamine residues and the ε-amino group of lysine residues in proteins, resulting in irreversible protein crosslinking and stabilization of the extracellular matrix.[1][2] This enzymatic activity, classified under EC 2.3.2.13, also enables deamidation of glutamine to glutamic acid under certain conditions, such as in the presence of water, and the enzyme exhibits additional GTP-binding and GTPase activities that regulate its conformation and non-enzymatic functions.[3][1]Structurally, tTG consists of four distinct domains: an N-terminal β-sandwich domain, a central catalytic core containing the active site cysteine residue, and two C-terminal β-barrel domains, allowing it to adopt either a compact "closed" conformation when bound to GTP (which inhibits transglutaminase activity) or an extended "open" conformation activated by calcium ions that promotes crosslinking.[1][3] This conformational flexibility underlies its dual roles as both an enzyme and a signaling protein, with widespread expression in tissues including the liver, brain, and endothelium, where it was first identified in 1957 through studies on guinea pig liver extracts demonstrating calcium-dependent incorporation of amines into proteins.[1][3]Beyond its enzymatic functions, tTG plays critical roles in cellular processes such as cell adhesion, migration, differentiation, wound healing, and apoptosis regulation by interacting with integrins, fibronectin, and other extracellular matrix components, thereby influencing tissue remodeling and homeostasis.[2][3] Dysregulation of tTG activity or expression is implicated in numerous pathologies; in celiac disease, it serves as the primary autoantigen by deamidating gluten peptides to enhance their immunogenicity, leading to an autoimmune response with high diagnostic sensitivity (98-100%) via anti-tTG IgA antibodies.[2] In neurodegenerative disorders like Alzheimer's and Parkinson's diseases, tTG promotes protein aggregation by crosslinking amyloid-β and α-synuclein, contributing to plaque and Lewy body formation.[1][3] Furthermore, elevated tTG levels are associated with cancer progression, including enhanced tumor cell migration, invasion, and chemoresistance in malignancies such as ovarian and pancreatic cancers, as well as fibrosis in organs like the liver and heart through excessive matrix stabilization.[3][2]
Structure
Gene
The TGM2 gene, which encodes tissue transglutaminase (also known as transglutaminase 2), is located on the long arm of human chromosome 20 at the cytogenetic band 20q11.23.[4] This positioning places it within a region that includes other genes involved in cellular signaling and structural processes.[5]The gene spans approximately 41 kb of genomic DNA and consists of 15 exons in its canonical transcript, encoding a primary protein isoform of 687 amino acids.[6][4] Alternative splicing produces additional isoforms, but the main form is widely studied for its multifunctional roles.[7]The promoter region of TGM2 contains regulatory elements responsive to retinoic acid, mediated by GC box motifs that facilitate transcriptional activation through interactions with transcription factors like Sp1.[8] It also includes a transforming growth factor β1 (TGF-β1) response element approximately 0.9 kb upstream of the transcription start site, enabling upregulation in response to inflammatory signals such as interleukin-1, interleukin-6, tumor necrosis factor-α, and TGF-β.[9] These elements contribute to stress-induced expression, including during hypoxia and endoplasmic reticulum stress, highlighting TGM2's role as a stress-responsive gene.[10]TGM2 is ubiquitously expressed across human tissues, with particularly high levels in endothelial cells, fibroblasts, and smooth muscle cells.[11] Expression is detected in placenta, endometrium, and fibromuscular tissues, often showing cytoplasmic localization.[12] Under inflammatory conditions, such as in chronic wounds or autoimmune responses, TGM2 transcription is upregulated, promoting adaptive cellular responses.[13]Regarding genetic variants, studies have investigated single nucleotide polymorphisms (SNPs) in TGM2 for associations with disease susceptibility, particularly celiacdisease, where the encoded protein serves as a key autoantigen. However, germlinemutations altering the protein sequence do not significantly contribute to celiacdisease risk.[14] Some polymorphisms, such as those identified in exon regions, have been detected in celiac patients and may modulate enzymefunction or expression levels, potentially influencing disease markers, though they are not primary susceptibility factors.[15]
Protein Structure
Tissue transglutaminase (TG2), also known as transglutaminase 2, is a 78 kDa multifunctional enzyme characterized by a modular architecture consisting of four distinct domains. The N-terminal β-sandwich domain (residues 1–139) forms a compact structure stabilized by hydrogen bonds and hydrophobic interactions, serving as a scaffold for interdomain contacts. Adjacent to this is the central catalytic core domain (residues 147–460), which adopts an α/β fold typical of papain-like cysteine proteases and houses the active site. The C-terminal region comprises two β-barrel domains: β-barrel 1 (residues 472–583) and β-barrel 2 (residues 591–687), each featuring antiparallel β-sheets that contribute to nucleotide binding and conformational dynamics.[16][17]The catalytic site within the core domain centers on Cys277, the nucleophilic cysteine that initiates the transglutaminase reaction by forming a transient thioester (thiol-acyl) intermediate with the γ-carboxamide group of glutamine residues in substrate proteins. This residue is part of a conserved catalytic triad (Cys277-His335-Asp358), where His335 acts as a general base to deprotonate Cys277, enhancing its nucleophilicity, and Asp358 stabilizes the histidine through hydrogen bonding, facilitating proton transfer during catalysis. The active site cleft is lined by residues such as Trp279 and Tyr306, which position substrates for efficient acyl transfer.[16][18][19]GTP and GDP binding occurs primarily at a site located at the interface between the catalytic core and β-barrel 1 domain, involving key residues such as Arg476, Val479, and Tyr583, which coordinate the nucleotide's phosphate groups and guanine base via hydrogen bonds and van der Waals interactions. A secondary binding mode may involve β-barrel 2, contributing to cooperative allosteric effects that inhibit transglutaminase activity by stabilizing the closed conformation. These sites enable TG2's dual role as a GTPase, distinct from its cross-linking function.[20][16][21]TG2 adopts distinct conformational states regulated by ligand binding: the "closed" state, promoted by GTP binding, compacts the structure with the β-barrel domains folding over the active site, rendering it inaccessible and inhibiting catalysis; in contrast, the "open" state, induced by Ca²⁺ binding to sites in the catalytic domain (e.g., involving Asp252 and Glu254), repositions the barrels away from the core, exposing the active site for substrate access. This interconversion relies on flexibility in the hinge regions (residues approximately 140–146, 461–471, and 584–590), linker segments connecting the domains, which undergo secondary structure changes, including α-helix to coil transitions, to accommodate the ~90° domain rotations observed in crystal structures.[22][18][1]Regarding post-translational modifications, TG2 possesses several predicted N-glycosylation sites (e.g., Asn247 and Asn367) based on sequence analysis, but experimental evidence indicates no glycosylation occurs in the native human protein, preserving its compact structure and activity. Other modifications, such as phosphorylation at Ser216, may influence conformation but are not integral to the core architecture.[23]
Tissue transglutaminase (TG2), also known as transglutaminase 2, primarily exerts its cross-linking activity through a calcium-dependent transamidation reaction that forms covalent bonds between proteins. In this process, a glutamine residue on one protein serves as the acyl donor, while the ε-amino group of a lysine residue on another protein acts as the acyl acceptor, resulting in the formation of an ε-(γ-glutamyl)lysineisopeptide bond and the release of ammonia.[24] This reaction is catalyzed within the active site of TG2, where calcium ions induce a conformational change from a closed, inactive state to an open, catalytically active form, enabling substrate binding.[24]The detailed mechanism begins with the deprotonation of the active-site cysteine residue (Cys277 in human TG2), which performs a nucleophilic attack on the γ-carboxamide group of the glutamine side chain, forming a thioester acyl-enzyme intermediate and liberating ammonia.[24] Subsequently, the ε-amino group of a lysine residue attacks this thioester intermediate, displacing the cysteine and forming the stable isopeptide bond. The general reaction can be represented as:Protein₁-Gln + Protein₂-Lys → Protein₁-(γ-glutamyl)-ε-lysine-Protein₂ + NH₃This transamidation is favored under conditions where primary amine donors are available, distinguishing it from deamidation reactions that occur with water as the acceptor.[24]Common substrates for TG2 cross-linking include extracellular matrix (ECM) components such as fibronectin, collagen, and fibrin, which contain accessible glutamine and lysine residues.[11] For instance, TG2 cross-links fibronectin to itself and other ECM proteins, enhancing matrix assembly, while it also incorporates into fibrin networks during coagulation.[25]The biological outcomes of this cross-linking activity include the stabilization of the ECM, which provides structural integrity to tissues, and the promotion of clot formation during wound healing by reinforcing fibrin scaffolds.[26] These modifications contribute to tissue remodeling and repair by creating insoluble, mechanically robust protein networks resistant to proteolysis.[27]Kinetic parameters for TG2 cross-linking indicate a requirement for millimolar concentrations of Ca²⁺, with an EC₅₀ around 0.27 mM and full activation typically observed at 5-10 mM, reflecting its regulation by intracellular calcium levels.[28] The enzyme operates optimally at a neutralpH of approximately 7-8, aligning with physiological conditions in extracellular environments.[29]
Deamidation Activity
Tissue transglutaminase (TG2), in the absence of primary amines, catalyzes the deamidation of glutamine residues in peptides and proteins, where water serves as the acyl acceptor to convert glutamine to glutamic acid while releasing ammonia.[30] This reaction introduces negative charges into the substrate, altering its properties without forming covalent cross-links between molecules.[31]The mechanism begins with the nucleophilic attack by the active sitecysteine (Cys277) on the δ-carbon of the glutamine side chain, forming a transient thioester acyl-enzyme intermediate and liberating ammonia.[30] In the subsequent step, water acts as the nucleophile to hydrolyze this intermediate, yielding the deamidated glutamic acid residue.[32] This process shares the initial acyl-enzyme formation with the cross-linking pathway but diverges by proceeding via hydrolysis rather than amine nucleophilic attack.[30]Key substrates for this activity include gluten-derived peptides such as gliadin, where TG2 selectively deamidates specific glutamine residues (e.g., in the α-gliadin peptide PFPQPQLPYPR), enhancing their binding affinity to HLA-DQ2/DQ8 molecules and thereby increasing immunogenicity in celiac disease.[33] Other examples encompass intracellular proteins like glyceraldehyde-3-phosphate dehydrogenase (GAPDH), where deamidation of multiple glutaminyl residues modulates enzymatic function.[34]Physiologically, TG2-mediated deamidation modifies proteins to influence signaling pathways, such as stabilizing the cyclin-dependent kinase inhibitor p21 by deamidating glutamine residues, which promotes cell cycle arrest.[35] It also facilitates protein degradation or alters aggregation propensity, as seen in the deamidation of β-amyloid peptides, which reduces their fibrillization.[36] Although less prevalent than cross-linking under typical cellular conditions, this activity holds critical importance in targeted pathologies like celiac disease.[30]In contrast to transamidation, deamidation predominates at low concentrations of primary amines and active TG2 enzyme, as well as under high substrate dilution, favoring hydrolysis over amine incorporation.[30] Both reactions are calcium-dependent, but deamidation can proceed efficiently in environments with limited amine availability, such as endolysosomal compartments.[32]
Tissue transglutaminase (tTG), also known as transglutaminase 2 (TG2), is allosterically regulated by guanine nucleotides such as GTP and GDP, which bind to sites within its two β-barrel domains (β1 and β2). This binding stabilizes a compact, closed conformation that masks the catalytic core, thereby inhibiting transglutaminase activity. The dissociation constant (Kd) for GTP binding is approximately 1.6 μM for wild-type TG2, while mutants like Y516F exhibit even higher affinity (Kd ≈ 0.8 μM), indicating tight nucleotide interaction under physiological conditions. GTP and GDP compete with Ca²⁺ for conformational control, as nucleotidebinding to residues such as Arg-579 in the β-barrel domain prevents the enzyme from adopting an active state even in the presence of moderate Ca²⁺ levels.[37]In contrast, Ca²⁺ serves as a positive allosteric effector by binding to five or six non-canonical EF-hand-like motifs primarily in the catalytic and β-barrel domains, inducing an open, extended conformation that exposes the active site Cys-277-His-335-Asp-358 triad. Activation requires Ca²⁺ concentrations in the millimolar range (apparent Km ≈ 3 mM), far exceeding typical intracellular levels, which ensures tTG remains dormant inside cells under normal conditions. High Ca²⁺ binding (e.g., 4–6 ions per molecule) not only promotes structural opening but also reduces GTP affinity, thereby overriding nucleotide inhibition.[38][39]The allosteric regulation follows a reciprocal model where GTP binding and hydrolysis via tTG's intrinsic GTPase activity modulate transglutaminase function, while Ca²⁺ binding reciprocally influences nucleotide affinity and GTPase efficiency. This bidirectional control allows tTG to switch between GTPase/scaffolding roles in low-Ca²⁺ environments and cross-linking/deamidation activities in high-Ca²⁺ settings. A recent discovery (as of 2024) reveals that TG2 also functions as an RNA-binding protein, with high affinity (K_D = 88 nM) for structured RNAs and poly(dG) sequences, preferentially in its open conformation. This RNA binding, mediated by superficial residues in the catalytic core (e.g., amino acids 173–177), may represent an additional layer of allosteric regulation influencing TG2's multifunctionality, though its precise physiological impacts require further investigation.[40][16][41]Physiologically, intracellular GTP levels (≈ 100–500 μM) maintain tTG in its inactive closed state, preventing unwanted protein cross-linking within the cytosol. Upon secretion or cellular stress, exposure to extracellular Ca²⁺ (1–2 mM) activates tTG, enabling extracellular matrix stabilization and other functions.[41][42]Experimental evidence from crystal structures confirms these conformational shifts: the GDP-bound closed form (PDB: 1KV3) shows nucleotide-induced compaction with blocked active site, while Ca²⁺-bound open structures (PDB: 6KZB) reveal domain separation and catalytic triad accessibility. GTP-complexed crystals (PDB: 4PYG) further demonstrate how nucleotide docking in the β-barrel cleft stabilizes inhibitory interactions, such as hydrogen bonding between Cys-277 and Tyr-516.[16][43][44]
Post-translational Modifications
Tissue transglutaminase (TG2) undergoes several post-translational modifications that modulate its enzymatic activity, stability, and cellular localization, primarily in response to oxidative stress and signaling cues. Oxidation of the catalytic site and adjacent cysteines is a key regulatory mechanism, where exposure to reactive oxygen species leads to the formation of disulfide bonds that inactivate TG2. Specifically, a redox-sensitive cysteine triad involving Cys230, Cys370, and Cys371 facilitates intramolecular disulfide bond formation, with Cys370 pairing preferentially with Cys230 under mild oxidation or with Cys371 under stronger oxidative conditions, resulting in conformational changes that inhibit transamidation activity.[45] This oxidation is reversible; thioredoxin-1 (TRX-1) reduces the Cys370-Cys371 disulfide bond, restoring TG2 activity with a catalytic efficiency of 1.6 μM⁻¹ min⁻¹.[46] Additionally, the endoplasmic reticulum-resident protein ERp57 accelerates TG2 oxidation by promoting the Cys370-Cys371 disulfide, inactivating it up to 2000-fold faster than small-molecule oxidants like H₂O₂, with an IC₅₀ of 60 nM.[46]Phosphorylation at specific serine and threonine residues further fine-tunes TG2 function. Protein kinase A (PKA) phosphorylates TG2 at Ser216, which inhibits its crosslinking activity while enhancing interactions that activate nuclear factor-κB (NF-κB) and downregulate phosphatase and tensin homolog (PTEN), promoting cell migration and S-phase progression in cancer cells by up to 54% in MCF-7breast cancer models.[47] Ser212 is another potential PKA site, and tyrosine residues such as Tyr219 and Tyr369 have been identified in cancer contexts, though their precise roles in localization or GTPase modulation remain under investigation.[47]Ubiquitination targets TG2 for proteasomal degradation, particularly under conditions of high oxidative stress and elevated calcium levels. Calcium influx, triggered by stressors like UV irradiation or H₂O₂, induces polyubiquitination of TG2, leading to its rapid degradation, which is blocked by proteasome inhibitors such as MG132.[48] This process is mediated by E3 ligases like CHIP, which ubiquitinates TG2 to control its levels and prevent excessive accumulation in pathological states.[49]These modifications collectively respond to the cellular redox environment, enhancing TG2 inhibition during inflammation and oxidative stress to prevent aberrant protein crosslinking, while allowing reactivation or degradation as needed for homeostasis. For instance, ERp57 knockdown in endothelial cells increases TG2 activity fourfold, underscoring the regulatory balance in inflammatory contexts.[46]
Biological Functions
Intracellular Roles
Tissue transglutaminase (tTG), also known as transglutaminase 2 (TG2), is primarily localized in the cytosol and nucleus in its inactive state, where it exists in a compact, GTP-bound conformation that suppresses its enzymatic activities. For example, in human neuroblastoma SH-SY5Y cells, approximately 93% of tTG is found in the cytosol, with about 7% in the nucleus, often associated with chromatin or the nuclear matrix; this distribution allows tTG to participate in intracellular signaling without immediate cross-linking.[50] Upon cellular stress or calcium influx, tTG can translocate between these compartments, modulating its interactions and functions while remaining distinct from its secreted extracellular forms.As a GTPase, tTG hydrolyzes GTP to GDP, enabling its role in signal transduction pathways, particularly as a Gα subunit in G-protein-coupled receptor signaling. This activity is crucial for coupling receptors such as α1-adrenergic and oxytocin receptors to phospholipase C (PLC), facilitating the hydrolysis of phosphatidylinositol 4,5-bisphosphate into inositol 1,4,5-trisphosphate and diacylglycerol.[11] In its GTP-bound state, tTG inhibits its own transamidation activity, prioritizing signaling; GTP-binding defective mutants enhance cross-linking but disrupt this regulatory balance, underscoring the GTPase function's dominance in non-stressed cells. Additionally, tTG exhibits kinase-like activity independent of GTP, phosphorylating substrates such as insulin-like growth factor-binding protein-3, which mimics kinase signaling to promote cell survival pathways.[51] Through GTP-independent binding, tTG also activates PLCδ1 by releasing it from inhibitory complexes, contributing to calcium mobilization without relying on canonical G-protein hydrolysis.[52]tTG possesses protein disulfide isomerase (PDI)-like activity that aids in protein folding within the reducing cytosolic environment, distinct from its transamidation domain and independent of calcium or nucleotides. This function involves catalyzing disulfide bond rearrangements in nascent or misfolded proteins, similar to classical PDIs, and is enhanced by oxidized glutathione while inhibited by bacitracin. In apoptosis, tTG plays dual roles: it promotes cell death by cross-linking intracellular proteins, stabilizing apoptotic bodies and preventing leakage of cellular contents, as seen in elevated expression during early apoptosis stages. Conversely, tTG inhibits apoptosis by cross-linking and inactivating caspases, such as caspase-3, thereby stabilizing anti-apoptotic factors and enhancing cell survival under certain stresses.[53][54]In cytoskeletal regulation, tTG modifies key components like actin and tubulin through transamidation or polyamination, influencing microtubule and microfilament dynamics essential for cell structure and migration. For instance, polyamination of tubulin by tTG stabilizes neuronal microtubules, promoting their polymerization and resistance to depolymerizing agents, which supports axonal integrity. Similarly, cross-linking of actin filaments enhances cytoskeletal rigidity, facilitating directed cell motility in processes like wound healing, without altering overall polymerization rates but improving filament stability. These modifications occur intracellularly in response to calcium signals, linking tTG to mechanotransduction and intracellular transport.[55]
Extracellular Roles
Tissue transglutaminase (TG2), also known as transglutaminase 2, is externalized to the extracellular space through unconventional secretion pathways that bypass the classical endoplasmic reticulum-Golgi route. This process involves delivery into recycling endosomes via phospholipid-dependent mechanisms, regulated by Rab11 GTPase and the N-terminal β-sandwich domain of TG2.[56][11] Such secretion enables TG2 to accumulate on the cell surface and within the extracellular matrix (ECM) in various cell types, including fibroblasts and endothelial cells, where it exerts its enzymatic and non-enzymatic functions.[57]In the ECM, TG2 enhances structural integrity by catalyzing the cross-linking of key components, including fibronectin, collagen IV, and laminin, which increases matrix rigidity and resistance to degradation.[11] This stabilization is critical for maintaining tissue architecture during remodeling, as TG2 forms ε-(γ-glutamyl)lysine isopeptide bonds between glutamine and lysine residues in these proteins.[57] Additionally, TG2 supports cell adhesion by acting as a co-receptor for integrins, such as α5β1, forming ternary complexes with fibronectin that promote focal adhesion assembly and downstream signaling via pathways like RhoA/ROCK.[58][11]TG2 contributes to wound healing by cross-linking fibrin to stabilize blood clots and facilitate fibroblastmigration into the injury site, thereby accelerating tissue repair.[11] In this context, TG2 upregulation at wound sites enhances ECM deposition and cell-matrix interactions essential for provisional matrix formation.[57] Conversely, TG2 modulates angiogenesis by interacting with vascular endothelial growth factor receptor (VEGFR) or modifying thrombospondin, which limits endothelial cell proliferation and vessel sprouting.[57][59] However, dysregulated TG2 activity leads to excessive ECM cross-linking, promoting scar tissue accumulation and contributing to fibrotic processes through increased matrix stiffness and reduced turnover.[60][11]
Clinical Significance
Role in Celiac Disease
Tissue transglutaminase (TG2), also known as transglutaminase 2, plays a central pathological role in celiac disease by deamidating gluten-derived gliadin peptides. This enzymatic modification converts neutral glutamine residues into negatively charged glutamic acid residues, thereby enhancing the peptides' binding affinity to HLA-DQ2 and HLA-DQ8 molecules on antigen-presenting cells.[61] The increased affinity facilitates presentation to CD4+ T cells, triggering a robust adaptive immune response characterized by cytokine production and inflammation in the intestinal mucosa.[62]TG2 also serves as the primary autoantigen in celiac disease, where immunoglobulin A (IgA) antibodies against TG2 (anti-tTG IgA) are a diagnostic hallmark. These autoantibodies exhibit high diagnostic accuracy, with sensitivity of more than 90% and specificity of more than 95% in untreated patients.[63] Their presence correlates with active disease and gluten exposure, reflecting the autoimmune component driven by TG2's interaction with deamidated gliadin.In the celiac intestine, TG2 is upregulated in the lamina propria, where its cross-linking activity contributes to extracellular matrix remodeling and immune complex formation, exacerbating villous atrophy and chronic inflammation.[64] This upregulation, often triggered by initial gluten-induced stress, amplifies tissue damage through stabilization of inflammatory mediators and promotion of mononuclear cell infiltration.[65]Genetic variations in the TGM2 gene, such as specific single nucleotide polymorphisms (SNPs), have been associated with increased susceptibility to celiac disease by altering TG2 expression or function.[15] Recent research up to 2025 has shown impaired regulatory T cell (Treg) function in celiac disease, with TG2 inhibitors showing potential to improve immune tolerance to gluten.[66] Additionally, TG2 inhibitors like ZED1227 have shown promise in phase 2 clinical trials, where they reduced gluten-induced mucosal inflammation and injury in celiac patients.[67]
Role in Cancer
Tissue transglutaminase (TG2), also known as transglutaminase 2, exhibits a dual role in cancer progression, acting as both a pro-tumorigenic and anti-tumorigenic factor depending on its localization, conformational state, and the tumor context. Intracellularly, TG2 functions as a GTPase that promotes cancer cell survival signaling, such as activation of NF-κB and PI3K/AKT pathways, which enhance proliferation, epithelial-mesenchymal transition (EMT), and resistance to apoptosis in various malignancies.[68] Extracellularly, TG2's cross-linking activity stabilizes the extracellular matrix (ECM) by forming rigid protein networks, which stiffens the tumor microenvironment and facilitates metastasis through increased cell adhesion and invasion via integrins like β1 and β5.[68][69]Conversely, TG2 can exert anti-tumor effects in certain scenarios, such as inducing apoptosis through stabilization of p53 when its cross-linking activity is inhibited, leading to reduced cell viability and proliferation. In some models, TG2-mediated ECM modifications inhibit angiogenesis by altering matrix composition, thereby limiting vascularization and tumor growth, as observed in melanoma where high TG2 expression correlates with reduced invasiveness.[70][68]TG2 is overexpressed in several cancers, including breast, pancreatic, and glioblastoma (GBM), where it drives tumor progression. In breast cancer, elevated TG2 promotes EMT, metastasis, and chemoresistance to agents like doxorubicin via Wnt/β-catenin signaling.[71] In pancreatic cancer, TG2 overexpression recruits tumor-associated macrophages and confers resistance to gemcitabine, associating with poor patient survival.[72] In GBM, TG2 enhances invasion and radioresistance by nuclear translocation and p53 degradation; recent studies show that TG2 knockdown in GBM cell lines like U87 reduces proliferation, colony formation, and tumor growth in xenografts while increasing apoptosis and DNA damage sensitivity post-irradiation.[73][74]This duality presents a therapeutic paradox: TG2 inhibition sensitizes cancer cells to chemotherapy by overcoming resistance mechanisms, as seen with inhibitors like NC9 enhancing apoptosis in resistant lines, yet it may paradoxically promote invasion by disrupting ECM integrity and reducing cell adhesion in some contexts, such as lung and colorectal cancers.[69][75]High TG2 expression generally correlates with poor prognosis in solid tumors, predicting worse overall survival in pancreatic adenocarcinoma and GBM, though outcomes vary in breast cancer subtypes.[68]
Roles in Other Diseases
Tissue transglutaminase (TG2) plays a significant role in neurodegeneration by catalyzing the cross-linking of key proteins into toxic aggregates. In Parkinson's disease, TG2 promotes the formation of Lewy bodies through ε-(γ-glutamyl)lysine isopeptide bonds that link α-synuclein monomers into oligomers and fibrils, contributing to neuronal toxicity and disease progression.[76] Similarly, in Alzheimer's disease, TG2 facilitates amyloid-β plaque development by cross-linking peptides into insoluble fibrils and induces tau aggregation into neurofibrillary tangles via dimerization and helical filament formation, exacerbating synaptic dysfunction and cognitive decline.[76] Recent studies have also implicated TG2 in Huntington's disease, where it cross-links mutant huntingtin into intraneuronal inclusions, driving striatal degeneration through mechanisms involving calcium dysregulation and oxidative stress.[77]In fibrotic disorders, TG2 contributes to extracellular matrix (ECM) remodeling by enhancing protein cross-linking, leading to tissue stiffness and pathological scarring. In liver fibrosis, TG2-mediated cross-linking of collagen and fibronectin during the inflammatory phase stabilizes the ECM, promoting progression to cirrhosis.[78] Lung fibrosis involves upregulated TG2 activity in myofibroblasts, which increases ECM deposition and rigidity, impairing respiratory function in conditions like idiopathic pulmonary fibrosis. In cardiac fibrosis, TG2 drives ventricular stiffening through collagen cross-linking in response to injury, contributing to diastolic dysfunction and heart failure.[79]TG2 influences cardiovascular pathologies beyond fibrosis by modulating vascular structure and stability. In atherosclerosis, TG2 is localized to plaque fibrous caps and shoulder regions, where its cross-linking activity stabilizes atheromatous lesions against rupture by forming resilient ECM networks.[80] Thrombin-induced upregulation of TG2 in endothelial cells further supports plaque integrity, potentially mitigating acute thrombotic events. In hypertension, TG2 mediates small artery inward remodeling and aortic stiffening, reducing vessel compliance and perpetuating elevated blood pressure through cytoskeletal reorganization in vascular smooth muscle cells.[81]TG2 exacerbates chronic inflammation in autoimmune and gastrointestinal disorders by promoting cytokine signaling. In rheumatoid arthritis, TG2 upregulation in synovial fibroblasts activates NF-κB pathways, inducing pro-inflammatory cytokines such as TNF-α and IL-6, which sustain joint inflammation and erosion.[82] In inflammatory bowel disease (IBD), TG2 is elevated in colonic mucosa, enhancing TNF-α and IL-6 production via macrophage activation, thereby amplifying mucosal damage and fibrosis in conditions like Crohn's disease.[82]Beyond these, TG2 is involved in wound healing disorders and diabetes-related complications, with emerging ties to broader autoimmunity. In hypertrophic scars and keloids, excessive TG2 activity leads to aberrant ECM cross-linking, resulting in over-deposition of collagen and prolonged fibrotic responses that impair normal tissue repair.[83] In diabetic nephropathy, hyperglycemia activates TG2, promoting glomerular fibrosis through TGF-β signaling and collagen accumulation, which contributes to progressive renal decline.[84] Recent investigations highlight TG2's role in regulatory T-cell (Treg) dysfunction, where its activity impairs Treg suppressive function in autoimmune contexts, potentially extending inflammatory dysregulation to diseases like type 1 diabetes and rheumatoid arthritis.[66]
Diagnostic Applications
Tissue transglutaminase (tTG) serves as a key autoantigen in serological diagnostics, particularly for celiac disease, where anti-tTG antibodies are detected via enzyme-linked immunosorbent assays (ELISAs). The IgA anti-tTG ELISA is the preferred initial screening test, exhibiting a sensitivity of 90.7% (95% CI: 87.3%-93.2%) and specificity of 96.4% (95% CI: 95.1%-97.4%) in a systematic review of 119 studies involving over 20,000 patients.[85] For patients with IgA deficiency, which affects approximately 2-3% of celiac cases, IgG anti-tTG or anti-deamidated gliadin peptide (DGP) IgG/IgA assays are recommended as alternatives or complements, improving detection rates when combined with IgA anti-tTG, with overall sensitivities reaching 93-98% and specificities around 95% in pediatric and adult cohorts.In tissue biopsies from the duodenal mucosa, immunohistochemistry (IHC) can visualize tTG expression, which is upregulated in active celiac disease, aiding in the confirmation of histopathological changes such as villous atrophy.[64] Additionally, endomysial antibody (EMA) tests, performed on biopsy sections or serum, indirectly target tTG as the autoantigen, offering high specificity (up to 99%) for celiac diagnosis when positive.[86]Point-of-care (POC) tests for anti-tTG IgA provide rapid results using finger-prick blood samples, with one novel assay demonstrating 98.31% sensitivity and 98.02% specificity in a study of 401 patients, facilitating immediate screening in clinical settings.[87] Emerging applications include urinary tTG levels or cross-linked products as non-invasive biomarkers for monitoring renal fibrosis in chronic kidney disease, where elevated urinary tTG correlates with interstitial fibrosis severity in posttransplant patients.[88]Diagnostic limitations include false negatives in selective IgA deficiency, necessitating total IgA measurement alongside testing, and reduced specificity in non-celiac autoimmune conditions. These applications are endorsed by the American Gastroenterological Association (AGA) and European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) guidelines, which recommend anti-tTG IgA as the first-line test for celiac screening, with biopsy-free diagnosis possible in symptomatic children if levels exceed 10 times the upper limit of normal and confirmed by EMA.
Therapeutic Targeting
Tissue transglutaminase (TG2) has emerged as a promising therapeutic target due to its dysregulation in various diseases, prompting the development of inhibitors that modulate its enzymatic activity. Small-molecule inhibitors targeting the active site, particularly at Cys277 in the catalytic domain, have shown potential in preclinical and clinical studies. For instance, KCC009, a selective TG2 inhibitor, disrupts fibronectin assembly in the extracellular matrix and has been investigated for its role in sensitizing glioblastoma cells to chemotherapy by blocking TG2-mediated cell survival pathways.[89] Similarly, ZED1227, another Cys277-directed covalent inhibitor, has advanced to phase 2b trials (CEC-004/CEL) as of 2025, demonstrating histologic improvements and reduced gluten-induced mucosal damage in patients with celiac disease when used as an adjunct to a gluten-free diet.[90][91]Disease-specific approaches leverage TG2's context-dependent roles. In cancer, particularly glioblastoma multiforme (GBM), RNA interference (RNAi) targeting TG2 has reduced tumor cell invasion and fibronectin remodeling in preclinical models, enhancing chemotherapy efficacy.[92] Anti-TG2 antibodies have also been developed to inhibit extracellular TG2 functions, showing antifibrotic effects in human cell models by blocking extracellular matrix accumulation, with potential extension to oncology where TG2 promotes metastasis.[93] For neurodegeneration and fibrosis, cystamine serves as an irreversible TG2 inhibitor that reduces protein cross-linking; it has alleviated symptoms in Huntington's disease models by mitigating neuronal damage and shown antifibrotic benefits in liver and kidney models by decreasing extracellular matrix deposition.[94][95]Therapeutic challenges include achieving isoform specificity, as TG2 shares structural similarities with other transglutaminases (e.g., TG1, TG3), necessitating selective inhibitors to avoid off-target effects.[96] Additionally, TG2's dual roles—protective in some contexts (e.g., wound healing) and pathological in others (e.g., fibrosis)—require context-dependent targeting strategies to balance inhibition without disrupting beneficial functions.[97]Recent developments from 2024–2025 highlight emerging modalities. Allosteric inhibitors binding the GTP site, such as LDN-27219, stabilize TG2's closed conformation to suppress transamidase activity, showing preclinical efficacy in reducing renal and vascular fibrosis by promoting antifibrotic macrophage polarization.[98][99] In celiac disease, TG2 inhibitors and Treg modulation have gained attention as separate or combined approaches to improve immune tolerance and reduce inflammation in preclinical models, as indicated by systematic reviews.[100]Clinical translation remains preclinical for most indications, with no approved TG2-targeted drugs as of 2025. However, preclinical studies in cardiac fibrosis models demonstrate that TG2 inhibition—via cystamine or selective small molecules—attenuates ventricular remodeling and improves function post-myocardial infarction by shifting macrophage phenotypes toward anti-inflammatory M2 states, positioning these agents as promising adjunct therapies, particularly for celiac disease.[101][102]
Protein Interactions
General Interactions
Tissue transglutaminase (TG2), also known as transglutaminase 2, participates in a wide array of protein-protein interactions that underpin its multifunctional roles in cellular adhesion, signaling, and matrix stabilization. Over 50 binding partners have been identified through techniques such as yeast two-hybrid screening and co-immunoprecipitation (co-IP), with these interactions often categorized by function, including extracellular matrix (ECM) components, cytoskeletal elements, and signaling effectors; a comprehensive database of transglutaminase substrates and interactions, including those of TG2, is available at TRANSDAB.[103][104] Such associations enable TG2 to influence diverse processes without relying solely on its enzymatic activity, as many interactions occur via non-covalent binding or GTPase-independent mechanisms.Among its substrates, TG2 prominently cross-links fibronectin at specific sites within the fibronectin type III (FNIII) domains, such as FNIII14–15, where lysine residues like Lys1837 and Lys1862 serve as reactive partners, thereby stabilizing ECM fibrils and enhancing matrix rigidity.[105] TG2 also binds directly to integrins, particularly the β1 subunit, to promote RGD-independent cell adhesion and focal contact formation, which activates downstream kinases like focal adhesion kinase (FAK) and Src.[58] Furthermore, TG2 interacts with phospholipase C δ1 (PLCδ1), inhibiting its activity through direct binding, with GTP-dependent dissociation of the complex relieving this inhibition and thereby modulating intracellular calcium release and phosphoinositide signaling pathways.[52]Regulatory interactions fine-tune TG2's activity through redox modifications; thioredoxin-1 (TRX-1) reduces oxidized cysteine residues on extracellular TG2, thereby restoring its transamidation function and preventing inactivation in oxidative environments.[106] In contrast, nitric oxide (NO) inhibits TG2 by S-nitrosylating critical cysteine residues, suppressing cross-linking activity and contributing to age-related vascular stiffness.[107]TG2 forms signaling complexes with transcription factors and adhesion molecules, such as NF-κB p65 (RelA), where it stabilizes the complex to upregulate genes like Snail and hypoxia-inducible factor 1α (HIF-1α), promoting inflammation and epithelial-mesenchymal transition.[108] It also associates with syndecan-4 in focal adhesions, recruiting protein kinase Cα (PKCα) to enhance β1-integrin co-signaling and fibril assembly.[109] Collectively, these general interactions modulate cell migration by stiffening the ECM and activating RhoA pathways, while supporting survival through anti-apoptotic signaling in stressed or tumorigenic contexts.[104]
Interaction with Erp57
Tissue transglutaminase (tTG), also known as TG2, interacts with endoplasmic reticulum protein 57 (Erp57, or PDIA3) through a redox-based mechanism involving thiol-disulfide exchange. Erp57 forms a transient mixed disulfide intermediate with the active-site cysteine residue Cys370 of tTG, which facilitates isomerization to an intramolecular disulfide bond between Cys370 and Cys371. This process oxidatively inactivates tTG, switching it from its catalytically active reduced state to an inactive oxidized conformation, with a bimolecular rate constant of 162 mM⁻¹ min⁻¹—approximately 400-fold faster than oxidation by cystine.[110]The Erp57-tTG complex forms primarily in the endoplasmic reticulum but can also occur extracellularly or in the cytosol under oxidative stress conditions, such as during inflammation or cellular secretion of Erp57. Although tTG activity is calcium-dependent, the Erp57-mediated oxidation occurs independently of Ca²⁺, allowing regulation even in low-calcium environments. Mass spectrometry has confirmed the mixed disulfide at Cys370, supporting direct binding.[110][111]Functionally, this interaction serves as a regulatory switch to prevent excessive tTG cross-linking activity, which could lead to pathological extracellular matrix accumulation; the oxidation is reversible by reductases like thioredoxin-1, maintaining tTG's redoxhomeostasis. Erp57 thus acts as a chaperone-like modulator, ensuring proper disulfide status without promoting irreversible inactivation. In vitro assays demonstrate that exogenous Erp57 reduces tTG activity to near-background levels.[110][112]Experimental evidence includes co-immunoprecipitation studies in human umbilical vein endothelial cells (HUVECs), where Erp57 colocalizes with and co-precipitates tTG, confirming complex formation. SiRNA knockdown of Erp57 in these cells increases tTG activity by up to fourfold, indicating enhanced reduction and less oxidation of tTG. Additionally, cryo-immunogold electron microscopy in duodenal biopsies shows reduced Erp57-tTG association in inflammatory conditions like celiac disease.[110][111]This interaction is particularly critical in oxidative environments, such as chronic inflammation, where dysregulated tTG contributes to fibrosis and autoimmunity; lower Erp57 levels correlate with heightened tTG activity and disease progression. Recent studies highlight its potential as a therapeutic target for redox modulation, including in cancer, where the Erp57-tTG complex influences tumor microenvironment stability and metastasis.[111][112]