E-cadherin roles in animal biology: A perspective on thyroid hormone-influence
© The Author(s). 2016
Received: 19 May 2016
Accepted: 26 October 2016
Published: 4 November 2016
The establishment, remodeling and maintenance of tissular architecture during animal development, and even across juvenile to adult life, are deeply regulated by a delicate interplay of extracellular signals, cell membrane receptors and intracellular signal messengers. It is well known that cell adhesion molecules (cell-cell and cell-extracellular matrix) play a critical role in these processes. Particularly, adherens junctions (AJs) mediated by E-cadherin and catenins determine cell-cell contact survival and epithelia function. Consequently, this review seeks to encompass the complex and prolific knowledge about E-cadherin roles during physiological and pathological states, particularly focusing on the influence exerted by the thyroid hormone (TH).
KeywordsE-cadherin Adherens junction Epithelia Development Evolution Thyroid hormones
Since the early 70s, prolific and significant research and hypotheses subscribe to the theory that unicellular to multicellular transition has occurred more than once during evolution through different genetic mechanisms for each kingdom in the tree of life. Particularly, cadherin and integrin cell adhesion molecules played a crucial role in metazoan transition [78, 171].
In addition, the interpretation of the cellular role of cadherin has changed over time, from a static membrane protein involved in cell-cell adhesion mechanic events to a membrane receptor involved in very dynamic intracellular signal transductions. These processes would be mediated not only from cell-cell junction platforms, but also from single receptors [29, 189, 216].
In different physiological contexts during development and adulthood, this adhesion is highly plastic, suffering remodeling due to numerous and complex signaling cascades finely coordinated in time and space. Thus, in pathological states such as cancer, the configuration of this adhesion is altered by genetic and epigenetic changes, resulting in modifications in the signaling pathways, loss of inhibition by contact, cell migration, and altered stromal interactions. A key group of these cell-cell adhesion molecules is the superfamily of cadherins, whose prototypical member is E-cadherin. This molecule was found for the first time in epithelial tissues [177, 215] and has been characterized as a potent suppressor of invasion and metastasis in studies dating back to 1990 (reviewed by ). E-cadherin plays a key role in determining cell polarity and differentiation, and thereby in the establisment and maintainance of tissue homeostasis. It is also important during development and during the whole life cycle of pluricelular organisms, mainly metazoans.
In this work, four major aspects bring E-cadherin into focus. First, epithelia are composed of cell phenotypes which exhibit the maximum polarity and whose epithelial identity is primarily specified by E-cadherin. Second, E-cadherin is involved in numerous processes such as, cell phenotype selection and migration, and morphogenetic movements occurring during metazoan development [26, 192, 193, 196]. Third, epithelia are usually located in direct contact with mutagenic and/or carcinogenic agents, so in men, 85–90 % of the cases can be attributed to epithelial cancers. Lastly, the complexity of in vivo animal studies has partly concealed the full spectrum of E-cadherin functions. Owing to the latter, the work-goal focuses on E-cadherin control mediated by thyroid hormones in a scarcely studied physio-pathological scenario.
E-cadherin function during metazoan development
Cadherins are a huge family of Ca2+-dependent cell surface adhesion glycoproteins, which are differentially expressed in tissues and ontogeny among broad groups of organisms, from unicellular choanoflagellates to invertebrates and all vertebrates classes. Therefore, cadherin evolution has special relevance for understanding metazoan origins [2, 62, 66, 77, 78, 80, 140, 143, 171, 192, 196].
Classical cadherins, like E(epithelial)-cadherin, bind to β-catenin via the cytoplasmic domain (CD) and promote cell-cell adhesion  or are rapidly degraded [32, 76, 86]. As development progresses, cadherins establish and maintain AJs through adaptor proteins to the cytoskeleton [63, 64, 129, 141]. These complex structural units are called cadhesomes , and act integrating signals from extracellular and intracellular environments [19, 62, 85–87, 138]. In vertebrates, E-cadherin mRNA and protein are maternally expressed, beginning their zygotic expression from 2-cell embryo or gastrulation [8, 9, 34, 91, 114, 191]. Although E-cadherin is principally expressed in the epidermal ectoderm , it has also been found in derivatives of neuroectoderm, mesoderm and endoderm [39, 85, 87]. In some species, embrionary E-cadherin is necessary for 8-cell stage compaction, for trophectoderm expansion [7, 108], and for maintaining epiboly integrity . Later during development, E-cadherin contributes to the morphogenesis of endodermal and neuroectodermal derivates , and digestive tract, kidney and skin remodeling [85–87, 179, 197]. In invertebrates, a vertebrate E-cadherin homolog is critical for cell rearrangement  and packing geometry .
Some studies suggest that three modern cadherin families —lefftyrins, coherins, and hedglings— were present in the last common ancestor of choanoflagellates and metazoans, and they may have evolved to diverse metazoan signaling and adhesion gene families . Several cadherin-analogous functions have been hypothesized in non metazoan unicellular lineages in spite of the fact that cadherins are undocumented in choanoflagellates. These organisms express members of key cell signaling and adhesion protein families that were previously thought to be exclusively found in animals [97, 98]. By studying cell differentiation and development in some choanoflagellates, it may be possible to characterize some ancestral functions (bacterial prey adhesive capture, attachment to environmental substrates, gamete recognition and hormonal signaling) of proteins that regulate animal development [46, 47, 98]. Interesting, numerous studies show interaction processes between bacteria or yeast and metazoan cadherins promoting host invasion [17, 36]. In addition, other studies inform that no receptors or ligands were identified from the nuclear hormone receptor, WNT and TGF-β signaling pathways . As we will explain later, the absence of nuclear hormone receptors and ligands, and molecules involved in Wnt signaling pathways suggest combined features and roles in a single molecule-type: the metazoan cadherins.
Taken together, these data and our results on TH-dependent E-cadherin control [56, 85], support the idea that classical cadherins could have emerged in the premetazoan to metazoan transition to respond to signaling mediated by nuclear hormone receptors and cytoskeleton connexions. Indeed, the development of complex multicellular organisms requires a genetic program regulated by nuclear hormone receptor signaling and dynamic cytoskeleton reorganizations.
E-cadherin structure, function and dysfunction
E-cadherin function control via EC
The mature classical E-cadherin is a single-pass transmembrane glycoprotein with five ectodomains (EC1–5), each made up of ~110 amino acid residues. Their NH2-terminal ectodomain mediates adhesive binding to cadherins present on the surfaces of neighboring cells. Their four interdomain junctions are characterized by three calcium binding sites ─DXD, DRE, and DXNDNAPXF sequence motifs─ . Cadherin function requires calcium to rigidify the EC domain [27, 112, 146] and to stabilize the protein [156, 159] avoiding proteolysis [79, 190], and allowing its proper localization [57, 156, 159].
E-cadherin mediates principally in cell-cell homophilic interactions through self-recognition of the conserved histidine-alanine-valine (HAV) sequence within EC1  (Fig. 1), and a strand-swapping interface. In this surface, a Tryptophan in position 2 (W2/Trp2) inserts into a hydrophobic pocket from another cis (from the same cell surface) or trans (from an adjacent cell) cadherin [100, 111, 182]. Although another cis dimerization has been postulated , several models disagree on the roles and numbers of the inner EC domains involved in cadherin homophilic interaction [31, 66, 112, 160].
Cleavage of the ~130 amino acids prodomain of immature cadherin represents the switch from a non adhesive to the functional form . Even though the specific E-cadherin endoprotease has not been identified yet , the E-cadherin proprotein contains a furin-cleavable motif [SSPGLRRQKR] (Fig. 1) [73, 136], and sequence specificity for other mammalian convertases . In contrast, mature E-cadherins are inactivated by cleavage in the EC domain mediated by matrix metalloproteinases  and others proteases [89, 153], in a process known as ectodomain shedding, thus promoting the invasion [44, 122, 187] (Fig. 1).
In addition, it has also been reported that E-cadherins can adhere heterophilically to integrins αEβ7 and α2β1 [30, 176, 205], killer-cell lectin-like receptors G1 , and numerous infectious agent proteins that target E-cadherins as an entry receptor [5, 36, 132].
E-cadherin function control via CD
In active functionally adhesion complexes E-cadherin associates with intracellular components forming AJs. E-cadherin CD interacts with several cytoplasmic proteins, being the catenins the best understood: β-catenin or γ-catenin, α-catenin, and p120-catenin (p120-ctn) [41, 128, 133, 134, 165]. A homolog of β-catenin, γ-catenin/plakoglobin , can substitute it under some circumstances . When they are fully incorporated in complexes with cadherins, these three catenins associate with a stoichiometry of one of each catenin per cadherin molecule [90, 147]. β-catenin binds directly to the distal ~72 amino acids of the E-cadherin CD through a 30-amino acid “core”, anchoring indirectly to α-catenin (Fig. 1) . P120-ctn binds independently to the ~29 amino acid membrane-proximal region of the cadherin CD [165, 199] (Fig. 1). α-Catenin associates with the actin cytoskeleton [167, 214] and numerous adaptor proteins to strengthen cell-cell adhesion [1, 199].
Several cleavage fragments of E-cadherin CD and disassembling of their adhesive complexes have been reported. During apoptosis or calcium influx, presenilin 1 (PS1)/γ-secretase cleaves between human E-cadherin residues Leu731 and Arg732  and caspase-3 cleaves on site 747-DTRD-750 and releases a 25-kDa fragment [93, 183]. In addition, during tumoral progression calpain mediates E-cadherin proteolysis  (Fig. 1).
As for α-catenin, it modulates the actin-cytoskeleton organization because it can occur either in a monomeric or a homodimeric form [13, 50, 65]. Upon the application of force on epithelia, the conformational change of monomeric αE-catenin uncovers the vinculin binding site, allowing vinculin to bind, and recruit additional F-actin to the cadherin-catenin complexes [126, 214]. Additionally, ZO-1, spectrin, vinculin  and Eplin  assemble F-actin to E-cadherin-catenin complexes. In parallel, the non-junctional cytosolic homodimeric αE-catenin pool inhibits the Arp2/3 complex, reducing membrane dynamics by preventing F-actin branch-formation .
Dynamics of E-cadherin-mediated cell-cell adhesion
Establishment of adherens junctions
It is known that catenins, including β-catenins, α-catenins, and p120-catenins, bind to immature E-cadherins while traveling through the endoplasmic reticulum and Golgi apparatus [40, 71]. Following synthesis in the rough endoplasmic reticulum and phosphorylation of the cytoplasmic domain, the E-cadherin pro-region is cleaved by furin proteases in the trans-Golgi network, an event that is mandatory for the mature cadherin to function in adhesion [59, 75, 116] (Fig. 2). Via golgin-97 dependent tubulovesicular carriers, E-cadherins leave the Golgi complex , and subsequently fuse with an intermediate recycling endosome, in route to the basolateral plasma membrane. This pathway for E-cadherins trafficking is tightly integrated with other proteins involved in epithelial polarity, such as Sec5, 6, and 15 [107, 193], Rab 11 , PALS (Protein Associated with Lin Seven 1), and aquaporin 3 (AQP3) , and it determines lumen formation  (Fig. 2).
The function and regulation of E-cadherins post-translational modifications in vivo have remained poorly defined. While the phosphorylations to eight serine residue cluster within a region that binds β-catenin modulate the β-catenin affinity and strengthen cell–cell adhesion , the E-cadherin cytoplasmic O-glycosylation (O-GlcNAc) blocks its cell surface transport, reducing intercellular adhesion . In addition, E-cadherins have four consensus sites Asn-X-Ser/Thr for N-glycosylation in EC4 and EC5 domains , most of them conserved among species (Fig. 1). It has been established that, while the N-glycans at Asn 633/483 are essential for E-cadherin folding, trafficking, and proper expression , their modification with complex N-glycans weakens AJs [121, 157] (Fig. 2).
Signaling and maintainance of adherens cell-cell junctions
Chemical [3, 85, 86, 149] and mechanical [110, 214] signals from cell-cell junctions can be transduced through E-cadherin-CD via β-, α- and p120-catenin to the cytoplasm or nucleus. Mechanical stimulation generated by tumor cell proliferation leads to β-catenin phosphorylation via Src kinase at the site of its interaction with E-cadherin, increasing β-catenin nuclear localization, and upregulating the oncogenes Myc and Twist1 . In physiological state, the formation of junctional complexes triggers activation of the phosphatidylinositol-3-kinase (PI3K)–Akt–protein kinase B pathway  because the PI3K-p85 subunit associates with AJs through direct binding to β-catenin  (Fig. 3). After recruitment of PI3K, phosphatidylinositol-(3,4,5)-triphosphate (PIP3) is generated, and guanine nucleotide exchange factors, that contain PIP3-binding pleckstrin homology domains, are recruited to the membrane and activate Rac1 [105, 210] or Cdc42 . This stimulates membrane actin dynamics adjacent to the initial contact site, increasing the probability of additional E-cadherin engagements. α-Catenins, in turn, homodimerizes and are released from the cadherin─catenin complexes to bind at actin and antagonize Arp2/3 function, inhibiting actin branching and facilitating belt formation of unbranched actin filaments. Simultaneously, other actin-binding proteins such as vinculin, afadin and α-actinin link with actin cytoskeleton, and β-catenin and p120-ctn link with tubulin cytoskeleton to route vesicles of E-cadherin─catenin to the cell-cell contact sites. Meanwhile, PtdIns(3,4,5)P3 accumulation in the membrane signals for the formation and expansion of the basolateral surface, whereas Rac1 promotes polarity orientation and lumen formation. In tissue and cell-type specific contexts, Rac1 also triggers the activation of downstream signaling effectors, promoting cell cycle arrest of confluent epithelial cells, and survival of polarized epithelial cells . Therefore, cadherins function in tissue morphogenesis by controlling both cell-cell adhesion and cell signaling. In this way, cadherins are involved in determining cell shape, position, migration [33, 68, 92, 125, 186], polarity [16, 200] and proliferation [96, 172], as well as tissular folding [201, 202]. In adherens junctions, E-cadherins and catenins determine cell-cell contact survival and epithelia function .
AJs are very dynamic structures that undergo constant remodeling. This can be low-scale remodelling involving replacement of individual or groups of molecules within the adhesive clusters without disrupting steady-state intercellular adhesions. It can also be large-scale junctional rearrangements that accompany breakdown and reformation of cell-cell contacts .
Growth factors (GFs) as specific regulators of E-cadherin─catenin traffic
Among genomic mechanisms, it is known that transcriptional repression of E-cadherins is mediated either by promoter CpG hypermethylation  or activation of repressors binded at E-boxes or brain-specific silencers, such as Snail and Slug , Twist  and E12/E47 (E2A gene product) . In contrast, the miR-200 family directly targets repressors ZEB1 and ZEB2, promoting E-cadherin expression upregulation [103, 104] (Fig. 1). In hormonal signaling routes, it is known that the activated androgen receptor binds to promoter and also represses E-cadherin gene expression, promoting metastasis by EMT .
Conversely, our results suggest that T3-TRs promote E-cadherin, β- and α-catenin gene expression in vivo and EMT inhibition [56, 85]. E-cadherin locus up-regulation can be mediated by an enhancer element at intron 1 [12, 25, 69, 70]. In addition, Stemler Stemmler et al.  reveal a complex mechanism of gene regulation at mouse E-cadherin locus intron 2. While in differentiated epithelia intron 2 sequences are required both to initiate transcriptional activation and additionally to maintain E-cadherin expression during embryogenesis, the level of intron 2-dependent E-cadherin expression is relative to the tissues and developmental timing. Thus, early embryogenesis requires intron 2 for the onset of expression, but at later stages, a second mechanism initiates E-cadherin expression independently of intron 2, although for high-level expression the support of the intron 2 enhancer elements is still required. The onset of the second wave of expression was detected in the surface ectoderm differentiate to form skin, and in the gut endoderm (around E12.5). A locus control region (LCR), in turn, might influence gene activity for proper activation and downregulation, sited upstream of cadherin clusters [184, 185] with a vital role for the large intron 2 (Fig. 1). Striking, cadherin superfamily genes display a higher average total intron number and significantly longer introns than other genes and across the entire vertebrate lineage . Particularly, the human genome has an uncommon high frequency of MIR and MaLR regulatory-associated repetitive elements at 5’-located introns, concomitant with increased de novo intronic transcription. Therefore, these intronic-specific sites may constitute targets of cadherin superfamily expression regulation, both in homeostasis and illness.
Even though TH signaling controls the proliferation of the intestinal epithelial progenitors in both amphibians and mammals, it has been suggested that TH control on the Wnt/β-catenin pathway does not appear to play a central role in amphibians [24, 178]. However, our in vivo experiments contradict this hypothesis, since we have detected early upregulation (24 hs) of E-cadherin, β- and α-catenin genes in the Xenopus laevis gut . During metamorphic climax, larval cell apoptosis coexists with pre-adult (juvenile) cell proliferation and differentiation, and with cell-cell junction assembly─disassembly, that require a complex signal network to control tissular homeostasis. We found that T3 modulates epithelial adhesive potential during gut remodeling in X. laevis development, early and directly activating E-cadherin, β-catenin and α-catenin genes, and downstream, modulating small GTPases and other proteins involved in adhesive epithelial properties. Using INSECT2.0 web server to predict the occurrence of Cis-Regulatory Modules (CRMs) , we found putative TERs in X. laevis E-cadherin, β-catenin and α-catenin genes, but not in the p120-ctn gene . Among evaluated small GTPases, gastrointestinal Rac1-mRNA levels significantly increased at 24 hs T3-treatment correlated with heightened “lamellipodia” or membrane protrusions. In contrast, at 5 days post T3-treatment RhoA-mRNA levels decrease while the important Rap1-mRNA increasing suggests that membrane Rap1-dependent E-cadherin recycling occurs at metamorphic climax end. Cdc42 and Arp2 actin nucleation protein became constant both during T3-induced and natural metamorphosis .
THs exert profound effects on tissues. Among them, cell-type dependent proliferation and differentiation both in mammalian skin [101, 113, 164, 195] and gut [158, 178], as in anuran kidney , skin  and gut [55, 56, 85]. These effects are regulated by phosphorilation levels of several partner proteins  and modulation of gen expression [56, 85]. Among the non-genomic effects of thyroid hormones, it appears that T3 activates PKA to in turn induce β-catenin nuclear translocation by phosphorylation at Ser675 site, thereby β-catenin modulates cyclin-D1 gene transcription and induces cell proliferation (Fig. 5) . In contrast, TH causes astrocyte differentiation through both initial PKA activity and later by phospho-MAP kinase (p-MAPK or p-ERK) . Postbirth, Schwann cell E-cadherin expression is highly regulated through cAMP-PKA activation for maintaining structural integrity . Thus, E-cadherin can negatively regulate, in an adhesion dependent manner, the ligand-dependent activation of divergent classes of RTKs, by inhibiting their ligand-dependent activation in association with a decrease in receptor mobility and in ligand-binding affinity  (Fig. 5).
Therefore, the function of THs and their TRs in cell proliferation, differentiation and apoptosis is not homogenous, because it depends strongly on the physio-pathological context; that is, the cell-type, ontogeny (progenitor or differentiated cell) and health (normal or tumoral cell). Although TH-dependent processes are highly coordinated, in turn, the local requirements cannot be governed by global mechanisms, such as an alteration of the thyroid gland function and variations in plasma TH concentrations. Instead, they require tissue-specific regulation mediated by deiodinases. Thus, in mammals, T3 induces type 2 deiodinase (D2) and E-cadherin expression, which sequesters β-catenin and reduces both β-catenin/TCF complex and type 3 deiodinase (D3) activation levels. Consequently, the local active T3-level increases and promotes cell differentiation and reduces its oncogenic effects in intestinal cells (Fig. 5) . Recently, this hypothesis has been again supported by Catalano and coworkers , who have found that increased intracellular TH concentration through D3 depletion induces cell differentiation and sharply mitigates tumor formation.
In this context, it is possible to postulate that during organ remodeling T3 induces epithelial stem cell proliferation via EGF-EGFR and cAMP-PKA signaling, and in parallel, T3 leads to repression of this via in a subgroup of these stem cells, and simultaneously increases E-cadherin, β- and α-catenin transcription via TH-RT to differentiate them to pre-adult (juvenile) gut epithelia cells (Fig. 5). In addition, the erichment of junctional E-cadherins sequestrates β-catenins, reducing their β-catenin nuclear translocalization and D3 disponibility, thereby strengthening cell differentiation.
Unquestionably, E-cadherin is deeply involved in establishing cell polarity and differentiation, and thereby in the establishment and maintenance of tissue homeostasis during the development and the entire life of pluricellular organisms, mainly metazoans. Therefore, this transmembrane receptor is a potent suppressor of tumoral invasion and metastasis. Thus, E-cadherin must continuously react both at extra- and intracellular signals, some of which are classical, and very well known.
This review summarizes findings supporting the central role of thyroid hormones in controlling the availability and functionality of E-cadherin, through membrane, cytoplasmic and gene expression activities that regulate cell proliferation, differentiation, migration, and thereby epithelial homeostasis.
Type 2 deiodinase
Type 3 deiodinase
Epidermal growth factor receptor
Epithelial to mesenchymal transitions
Mitogen-activated protein kinase
Protein Associated with Lin Seven 1
Thyroid hormone receptor
Membrane-receptor tyrosine kinase
Retinoid X receptor
T3 response element
We are grateful to Professor Diana Mónica Waigandt for her help with the revision of the English version of the manuscript for publication and to Dr. Alejandro Peralta Soler for his critical reading and valuable suggestions to improve the manuscript.
This work was supported by grants from: National Agency for Scientific and Technological Promotion-MINCYT, Argentina and UNER: PICTO-2009-209 (to Victor Hugo Casco). SCYTFRH-UNER 6019–1 (to Victor Hugo Casco); SCYTFRH-UNER 6067–1 (to Victor Hugo Casco); SCYTFRH-UNER 6088–1 (to María Fernanda Izaguirre).
Availability of data and materials
IMF and CVH devised and wrote the manuscript. Both authors have read and accepted the final version of the manuscript.
María Fernanda Izaguirre is BA in Biochemistry and PhD in Biological Sciences Victor Hugo Casco is BA and PhD in Biological Sciences. Both are Professors of Molecular and Cell Biology and carry out research on the function of cell-cell adhesion molecules during development and adult life of animals.
The authors declare that they have no competing interests.
Consent for publication
Ethical approval and consent to participate
The research protocol was approved by the local Research Institutional Ethics Committee of Entre Ríos National University.
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