Salivary Gland Bioengineering
Abstract
:1. Introduction
2. Learning from Salivary Gland Biology and Pathology
2.1. Salivary Gland Development and Function
2.1.1. Salivary Glands and Their Functional Units
2.1.2. Coordination of Saliva Secretion
2.1.3. Salivary Gland Development
Branching Morphogenesis Creates the Adult Gland Structure
Epithelium, Endothelium, and Neural Crest-Derived Cells Regulate Early Salivary Gland Development
2.2. Fibrosis, Cellular Senescence, and Salivary Gland Pathology
2.2.1. SASP Signaling Drives Neighboring Proliferation-Competent Cells to Senescence (Bystander Effect)
2.2.2. Senescence and Its Impact on Normal Fibroblast Dynamics in Healing and Fibrosis
2.2.3. Senolytics and SASP Depressants Support Healing, Reduce Fibrosis, and Improve Transplant Engraftment
3. Cell Selection for Salivary Gland Bioengineering
3.1. Salivary Gland Cell Lines
Species | Cell Lines | Tissue Sources | Cell Types | Characteristics |
---|---|---|---|---|
Human | HSY | Parotid gland adenocarcinoma | Ductal epithelial cells | Form desmosomes and tight junctions (TJs) and exhibit polarization [126,135]; express amylase [136]; respond to muscarinic and β-adrenergic autonomic agonists [137]. |
HSG | Irradiated SMG | Intercalated duct epithelial cells | Form desmosomes with sporadic TJ and no AQP expression on plastics [138]; differentiate into acinar structures and express amylase on Matrigel; respond to muscarinic and purinergic agonists; express ductal differentiation markers (EGF, NGF, and renin) [125]; express TJs (claudin-1, -2, -3, -4,ccludingn, JAM-A, and ZO-1) and AQP (AQP5) on Matrigel-coated permeable supports [139]. Report to be contaminated with Hela cells [128]. | |
Mouse | SIMS | A 22-day-old transgenic SMG | Immortalized ductal epithelial cells | Exhibit polarity and express E-cadherin and ZO-1 and duct-specific cytokeratins on Matrigel-coated surfaces; form duct-like structures (cysts) on collagen Type I gels (Col I); When grown on a filter support SIMS cells form a tight monolayer, exhibit vectorial transport function and show exclusive Na+, K(+)-ATPase localization to the basolateral domain [140]; express EGF, NGF, and renin [129]. |
SIMP | A 12-day-old PyLT transgenic SMG | Immortalized striated ductal epithelial cells | Exhibit polarity and express E-cadherin and ZO-1 and duct-specific cytokeratins on Matrigel-coated surfaces; form duct-like structures on Col I; express duct-specific cytokeratins and differentiation markers (EGF, NGF, and renin) [140] | |
mSG-DUC1 | SMG | Genetically modified mice, homozygous for floxed alleles of the integrin α3 subunit | mSG-DUC1 cells express the ductal markers, keratin-7 and keratin-19, and form lumenized spheroids [130]. | |
mSG-PAC1 | SMG | Genetically modified mice, homozygous for floxed alleles of the integrin α3 subunit | Express the ductal markers, keratin-7 and keratin-19, and form lumenized spheroids; express the pro-acinar markers SOX10 and aquaporin-5 [130]. | |
Rat | SMIE | SMG | Immortalized salivary glandular epithelium-like cells | Form TJs on collagen-coated filters [131]; resemble salivary glandular epithelium with an immature lumen; express ZO-1 and E-cadherin, but low level claudin-3 [141]; have a low level transepithelial resistance (TER) that can be regulated by IGF-1 [142] |
RSMT-A5 | SMG | Transformed ductal cells | Exhibit a ductal epithelial phenotype and a high density of α1-adrenergic receptors [143]. | |
SMG-C6 | SMG | Immortalized submandibular acinar epithelial cells | Form TJs and desmosomes, enabling polarization [133]; exhibit secretory features (i.e., domes, granules, and canaliculi) and more cytodifferentiation than SMG-C10 [144]; respond to muscarinic and purinergic agonists (but not to α1 agonists) by increasing [Ca2+]i and respond to β-adrenergic agonists by increasing [cAMP]; lack ductal marker cytokeratin 19 expression and exhibit high TER on collagen-coated polycarbonate filters [145]. | |
SMG-C10 | SMG | Immortalized submandibular acinar epithelial cells | Form TJs and desmosomes, enabling polarization; respond to β-adrenergic agonists; exhibit high TER on collagen-coated polycarbonate filters; modulate Na+ transport and regulate salivary cell volume [125,133,145,146,147]. | |
Par-C5 | Rat parotid glands | Immortalized acinar epithelial cells | Form layers of plump cells containing intercellular lumen-like invaginations on their medial surfaces; form secretory granules, TJs, intermediate junctions, desmosomes, and microvilli; respond to α1-adrenergic agonists by increasing [cAMP] [133]; respond to cholinergic, muscarinic, and α1-adrenergic agonists by increasing [Ca2+]i [148,149]; express functional amylase [134]. | |
Par-C10 | Immortalized acinar epithelial cells | Form monolayers of cuboidal cells with thick ECM at their bases; form secretory granules, TJs, intermediate junctions, desmosomes, and microvilli [133]; respond to α1-adrenergic agonists by increasing [cAMP] [148]; respond to cholinergic, muscarinic, and α1-adrenergic agonists by increasing [Ca2+] [133,148,149]; do not express amylase [134]; exhibit high TER [150,151,152]; express sodium bicarbonate cotransporters and anion exchange proteins on basolateral surfaces, which regulate transepithelial transport. Par-C10 cells achieve transepithelial transport that is sensitive to both intracellular Ca(2+)- and cAMP-dependent stimulation [151]; form 3D differentiated acinar-like spheres on growth-factor-reduced Matrigel, expressing TJs, ion transporters, M3 muscarinic receptors, and AQP3, increasing AQP5 expression under osmotic stress and showing changes in potential difference in response to muscarinic agonist stimulation [152]. |
3.2. Primary Salivary Gland Cells
3.3. Progenitor Cells of the Developing Salivary Gland
3.3.1. Salivary Gland Stem and Progenitor Cells during Development
3.3.2. Stromal-Epithelial Interactions during Development
3.4. Stem Cells for Salivary Gland Tissue Engineering
3.4.1. Salivary Gland Stem Cells (SGSCs)
Stem Cell Marker | Salivary Gland Location | Method of Identification | Progenitor or Stem | Reference Number |
---|---|---|---|---|
c-KIT (CD117) | Ducts | Gene expression | Stem | [177] |
SCA-1 | Ducts | Gene expression | Stem | [177] |
Keratin-5 (K5) | Ducts (developing) | Cytoskeletal protein expression, in vivo lineage tracing | Progenitor | [41,178,179] |
Keratin-14 (K14) | Ducts (developing) | Cytoskeletal protein expression, in vivo lineage tracing | Progenitor | [179] |
LGR5 | Ducts (human parotid and submandibular) | Gene expression | Stem | [67] |
CD44 | Not specified | MSC surface antigen | Stem | [67,180,181,182,183] |
CD49f (integrin) | Not specified | MSC surface antigen | Stem | [67,180,181,182,183] |
CD90 | Not specified | MSC surface antigen | Stem | [67,180,181,182,183] |
CD105 | Not specified | MSC surface antigen | Stem | [67,180,181,182,183] |
3.4.2. Mesenchymal Stem Cells (MSCs)
3.4.3. Pluripotent Stem Cells (PSCs): ESCs and iPSCs
4. Biomaterials for Salivary Gland Cell Survival, Differentiation, and Engraftment
4.1. Cell Support System Overview
4.2. Scaffold Fabrication Approaches to Salivary Gland Tissue Engineering
4.2.1. Electrospinning to Synthesize Fibrous Matrices
4.2.2. Phase Separation to Produce Composite Scaffolds
4.2.3. Freeze-Drying to Fabricate Porous Scaffolds
4.2.4. Hydrogel Synthesis to Form Injectable Cell Delivery Vehicles
4.2.5. Self-Assembly to Generate Cellular Clusters and Organoids
5. Potential Engineering Strategies to Improve Salivary Gland Tissue Vascularization, Innervation, and Engraftment
5.1. Prospects for Engineering Vascularized Salivary Gland Tissue
5.2. Prospects for Engineering Innervated Salivary Gland Tissue
5.2.1. Mesh Electronics and Bio-Hybrid Systems
5.2.2. Biocompatible, Endocytosed Nanotubes in Salivary Gland Tissue
5.2.3. Bioprinting of Neurons and Innervation of Tissues
5.2.4. Nanoparticles to Offer Essential Spatiotemporal Control over Scaffold Development and Engraftment
5.2.5. Injectable Engineered Salivary Gland Transplants
6. Conclusions and Future Perspectives
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Fabrication Method | Biomaterial and Dimensionality | Cell Type | Advantages and Disadvantages |
---|---|---|---|
Thermal molding | 2D PLLA and PGA (flat disks) | HSG | Pros: Biodegradable; able to form into coverslip-like disks suitable for cell seeding; versatile permitting melt-processing polymer pellets between sheets of aluminum foil using a Carver press at 350 °F, 450 °F, 175 °F, and 200 °F for PLLA, PGA, 50/50 PLGA, and 85/15 PLGA, respectively [232,233]. Cons: Require ECM coating to support cell attachment; lack 3D cues. |
Electrospinning | PLGA (fibrous scaffolds) | SIMS | Pros: Provide topographic cues (e.g., nanofibers, curvature); exhibit more rounded and clustered cell shape vs. 2D flat disks; enhance cell-polarization effects and expression of water channel proteins [234,235]. Cons: Require laminin coating for cell polarization and tight junctions; lack in vivo-like viscoelasticity. |
PLGA (fibrous scaffolds) | Par-C10 | ||
Freeze-drying | Silk fibroin (porous scaffolds) | Primary salivary gland epithelial cells from rat SMG and parotid gland | Pros: Provide topographical cues; promote epithelial cell growth; facilitate the secretion of ECM proteins; retain the differentiated function [236,237]. Cons: Require fibronectin coating; mimic the basement membrane for epithelial cells but might not be ideal for stromal cell culture; lack in vivo-like viscoelasticity. |
Hydrogel synthesis | HA hydrogels (cell culture insert) | Primary human salivary gland acinar-like cells from the parotid gland | Pros: Mimic the hydrogel component of ECM; exhibit acini-like structures with tight junctions, α-amylase expression, and an apoptotic central lumen on HA gels with an elastic modulus of 2000 Pa and incorporating peptide derived from domain IV of perlecan [238]. Cons: Require coupling bioactive peptides; or form acinar-like structures that are less organized or slowly growing in 2D or 2.5D than those in 3D HA hydrogels. |
3D HA/PEG hydrogels (cell culture insert) | Primary human salivary gland acinar-like cells from the parotid gland | Pros: Provide 3D microenvironment for encapsulated cells; facilitate cell self-assembly into acini-like spheroids of ~50 µm in size; demonstrate neurotransmitter-stimulated protein secretion and fluid production; integration in an in vivo rat model with no obvious signs of inflammation [239,240]. Cons: Indicate reverse polarity; lack essential machinery for full salivary restoration. | |
[PEG(RGD)-C12]n microfibers | Human primary salivary gland myoepithelial cells | Pros: Fabricate meter-long multiblock copolymer microfibers via straightforward interfacial bioorthogonal polymerization; provide guidance cues for the attachment and elongation of myoepithelial cells [17]. Cons: Cannot use for cell encapsulation; culture cells on the surface two dimensionally rather inside the microfiber three dimensionally. | |
3D PEG hydrogels | A mixture of primary acinar and ductal cells from mouse SMG | Pros: Improve cell viability and proliferation and facilitate cell–cell contacts by encapsulation of pre-assembled spheroids [241]. Cons: Remain as single cells without forming organized acini-like structures after cell encapsulation in 3D PEG hydrogels. | |
2D polyacrylamide gels | Mouse E13 SMG | Pros: Promote branching morphogenesis; partially rescue acini structure and differentiation by transferring glands from stiff to soft gels or by adding exogenous TGFβ1 [242] Cons: Require addition of exogenous TGFβ1 to polyacrylamide gels for partial acini structure rescue; lack 3D cues. | |
2D RGD-modified alginate hydrogel sheet | Mouse E13 mesenchymal cells and SMG | Pros: Promote mesenchymal (not epithelial) cell adhesion by RGD surface modification; enhance the bud expansion and cleft formation in SMG by softer gels, whereas stiffer gels attenuate them and decrease gene expression of FGF7 and FGF10; partially rescue acini structure and differentiation by adding exogenous FGF7 or FGF10, or by transferring SMGs from stiff to soft gels [243]. Cons: Stiffer RGD-modified alginate hydrogel sheets attenuate bud expansion and decrease gene expression of FGF7 and FGF10. | |
3D Alginate hydrogel microtubes | Co-culture of SIMS with mouse NIH 3T3 fibroblasts or E16 mesenchyme cells | Pros: Provide 3D microenvironment in hydrogel that is easy to handle; allow for high density cell growth; facilitate 3D mesenchymal-epithelial interaction; allow salivary gland epithelial cell organization into 3D cavitated structures with lumen formation; exhibit potential for formation of uniform organoids and functional units [244]. Cons: Require 3D arrangement of microtubes with organoids and additional elements to construct the full machinery of the salivary gland. | |
2D Fibrin-based hydrogels | Par-C10 | Pros: Support differentiation of salivary gland cell clusters with mature lumens [245] Cons: 2D culture on the hydrogel surface; require laminin-111 peptide-modification. | |
Fibrin-based hydrogels | Acellular, laminin I peptide functionalized | Pros: Mitigate the risk of tumor development; results in restoration of functional salivary tissue [246]. Cons: Require decoration with laminin-1 peptides; require injection of liquid followed by internal gelation to avoid hydrogel clogging the needle. | |
Gelatin-based hydrogel sheet | Acellular, controlled release of growth factors (EGF, FGF, NGF) | Pros: Demonstrate atrophy and regeneration of the SMG; enable observation of effects of sustained release of physiologically active substances contained within an implanted hydrogel sheet. Cons: Collapse of the hydrogel mesh began by day 7, in conjunction with invasion of surrounding fibrotic connective tissue, without regeneration of the salivary gland tissue [247]. | |
Cryoelectrospinning | 3D Alginate-elastin cryoelectrospinning scaffolds | NIH 3T3 fibroblasts | Pros: Produce porous nanofiber-sponge scaffolds that recapitulate the topography and viscoelasticity of salivary gland ECM; allow cell penetration deeply and 3D culture; support stromal cell viability and homeostatic marker expression [230]. Cons: Require dynamic seeding to achieve high seeding efficiency; require dynamic culture to achieve high density cell growth. |
Bioprinting | Magnetic 3D bioprinting (M3DB) | Neural crest-derived MSCs and human dental pulp stem cells | Pros: Develop innervated secretory epithelial organoids in the presence of FGF using cells tagged with magnetic nanoparticles that are ordered using magnetic dots. Cons: Require magnetic nanoparticles; challenge to determine an apicobasal polarization due to tightly packed epithelial cells; exhibit limited vascularization in the organoids [248]. |
Category | Details and Strategies |
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Origins and development |
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Histological features of hypofunctioning tissue |
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Fabrication strategies for scaffolds |
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Major challenges |
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Emerging technologies |
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Outlook |
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Rose, S.C.; Larsen, M.; Xie, Y.; Sharfstein, S.T. Salivary Gland Bioengineering. Bioengineering 2024, 11, 28. https://doi.org/10.3390/bioengineering11010028
Rose SC, Larsen M, Xie Y, Sharfstein ST. Salivary Gland Bioengineering. Bioengineering. 2024; 11(1):28. https://doi.org/10.3390/bioengineering11010028
Chicago/Turabian StyleRose, Stephen C., Melinda Larsen, Yubing Xie, and Susan T. Sharfstein. 2024. "Salivary Gland Bioengineering" Bioengineering 11, no. 1: 28. https://doi.org/10.3390/bioengineering11010028