Rat Parotid Gland Cell Differentiation in Three-dimensional Culture

Overview

Journal Tissue Eng Part C Methods

Specialties Anatomy & Histology
Biotechnology

Date 2010 Feb 4

PMID 20121592

Citations 29

Authors

Olga J Baker

David J Schulz

Jean M Camden

Zhongji Liao

Troy S Peterson

Cheikh I Seye

Michael J Petris

Gary A Weisman

Affiliations

Soon will be listed here.

Abstract

The use of polarized salivary gland cell monolayers has contributed to our understanding of salivary gland physiology. However, these cell models are not representative of glandular epithelium in vivo, and, therefore, are not ideal for investigating salivary epithelial functions. The current study has developed a three-dimensional (3D) cell culture model for rat Par-C10 parotid gland cells that forms differentiated acinar-like spheres on Matrigel. These 3D Par-C10 acinar-like spheres display characteristics similar to differentiated acini in salivary glands, including cell polarization, tight junction (TJ) formation required to maintain transepithelial potential difference, basolateral expression of aquaporin-3 and Na+/K+/2Cl- cotransporter-1, and responsiveness to the muscarinic receptor agonist carbachol that is decreased by the anion channel blocker diphenylamine-2-carboxylic acid or chloride replacement with gluconate. Incubation of the spheres in the hypertonic medium increased the expression level of the water channel aquaporin-5. Further, the proinflammatory cytokines tumor necrosis factor-alpha and interferon-gamma induced alterations in TJ integrity in the acinar-like spheres without affecting individual cell viability, suggesting that cytokines may affect salivary gland function by altering TJ integrity. Thus, 3D Par-C10 acinar-like spheres represent a novel in vitro model to study physiological and pathophysiological functions of differentiated acini.

Citing Articles

Bioprinting salivary gland models and their regenerative applications.

Klangprapan J, Souza G, Ferreira J BDJ Open. 2024; 10(1):39.

PMID: 38816372 PMC: 11139920. DOI: 10.1038/s41405-024-00219-2.

A combination treatment of low-dose dexamethasone and aspirin-triggered resolvin D1 reduces Sjögren syndrome-like features in a mouse model.

Dos Santos H, Maslow F, Nam K, Trump B, Weisman G, Baker O JADA Found Sci. 2023; 2.

PMID: 37622089 PMC: 10448398. DOI: 10.1016/j.jfscie.2022.100016.

Slow hydrogel matrix degradation enhances salivary gland mimetic phenotype.

Mereness J, Piraino L, Chen C, Moyston T, Song Y, Shubin A Acta Biomater. 2023; 166():187-200.

PMID: 37150277 PMC: 10330445. DOI: 10.1016/j.actbio.2023.05.005.

Current experimental methods to investigate the impact of specialized pro-resolving lipid mediators on Sjögren's syndrome.

Dos Santos H, Nam K, Gil D, Yellepeddi V, Baker O Front Immunol. 2023; 13:1094278.

PMID: 36713415 PMC: 9878840. DOI: 10.3389/fimmu.2022.1094278.

Hydrogels for Salivary Gland Tissue Engineering.

Pillai S, Munguia-Lopez J, Tran S Gels. 2022; 8(11).

PMID: 36354638 PMC: 9690182. DOI: 10.3390/gels8110730.

References

Martinez J, Cassity N . Salivary secretion induced from isolated, perfused rat submandibular glands by sympathomimetic agents. Arch Oral Biol. 1983; 28(12):1101-8. DOI: 10.1016/0003-9969(83)90165-6. View

Peppi M, Ghabriel M . Tissue-specific expression of the tight junction proteins claudins and occludin in the rat salivary glands. J Anat. 2004; 205(4):257-66. PMC: 1571348. DOI: 10.1111/j.0021-8782.2004.00332.x. View

Qi A, Wolff S, Nicholas R . The apical targeting signal of the P2Y2 receptor is located in its first extracellular loop. J Biol Chem. 2005; 280(32):29169-75. DOI: 10.1074/jbc.M501301200. View

Castle A, Huang A, Castle J . The minor regulated pathway, a rapid component of salivary secretion, may provide docking/fusion sites for granule exocytosis at the apical surface of acinar cells. J Cell Sci. 2002; 115(Pt 14):2963-73. DOI: 10.1242/jcs.115.14.2963. View

Turner J, Redman R, Camden J, Landon L, Quissell D . A rat parotid gland cell line, Par-C10, exhibits neurotransmitter-regulated transepithelial anion secretion. Am J Physiol. 1998; 275(2):C367-74. DOI: 10.1152/ajpcell.1998.275.2.C367. View

Hansen A, Galtung H . Aquaporin expression and cell volume regulation in the SV40 immortalized rat submandibular acinar cell line. Pflugers Arch. 2006; 453(6):787-96. DOI: 10.1007/s00424-006-0158-2. View

DAmico F, Skarmoutsou E, Sanfilippo S, Camakaris J . Menkes protein localization in rat parotid acinar cells. Acta Histochem. 2005; 107(5):373-8. DOI: 10.1016/j.acthis.2005.07.003. View

Aframian D, Palmon A . Current status of the development of an artificial salivary gland. Tissue Eng Part B Rev. 2008; 14(2):187-98. DOI: 10.1089/ten.teb.2008.0044. View

Shoshani L, Contreras R, Roldan M, Moreno J, Lazaro A, Balda M . The polarized expression of Na+,K+-ATPase in epithelia depends on the association between beta-subunits located in neighboring cells. Mol Biol Cell. 2004; 16(3):1071-81. PMC: 551474. DOI: 10.1091/mbc.e04-03-0267. View

10.

Turner J, Weisman G, Camden J . Upregulation of P2Y2 nucleotide receptors in rat salivary gland cells during short-term culture. Am J Physiol. 1997; 273(3 Pt 1):C1100-7. DOI: 10.1152/ajpcell.1997.273.3.C1100. View

11.

Pedersen P, Braunstein T, Jorgensen A, Larsen P, Holstein-Rathlou N, Frederiksen O . Stimulation of aquaporin-5 and transepithelial water permeability in human airway epithelium by hyperosmotic stress. Pflugers Arch. 2006; 453(6):777-85. DOI: 10.1007/s00424-006-0157-3. View

12.

Hoffert J, Leitch V, Agre P, King L . Hypertonic induction of aquaporin-5 expression through an ERK-dependent pathway. J Biol Chem. 2000; 275(12):9070-7. DOI: 10.1074/jbc.275.12.9070. View

13.

Joraku A, Sullivan C, Yoo J, Atala A . In-vitro reconstitution of three-dimensional human salivary gland tissue structures. Differentiation. 2007; 75(4):318-24. DOI: 10.1111/j.1432-0436.2006.00138.x. View

14.

Kurihara K, Nakanishi N, Turner R . Phosphorylation of the salivary Na(+)-K(+)-2Cl(-) cotransporter. Am J Physiol Cell Physiol. 2002; 282(4):C817-23. DOI: 10.1152/ajpcell.00352.2001. View

15.

Martinez J, Holzgreve H, Frick A . Micropuncture study of submaxillary glands of adult rats. Pflugers Arch Gesamte Physiol Menschen Tiere. 1966; 290(2):124-33. DOI: 10.1007/BF00363690. View

16.

Fox R, Kang H, Ando D, Abrams J, Pisa E . Cytokine mRNA expression in salivary gland biopsies of Sjögren's syndrome. J Immunol. 1994; 152(11):5532-9. View

17.

Baker O, Camden J, Rome D, Seye C, Weisman G . P2Y2 nucleotide receptor activation up-regulates vascular cell adhesion molecule-1 [corrected] expression and enhances lymphocyte adherence to a human submandibular gland cell line. Mol Immunol. 2007; 45(1):65-75. PMC: 2064040. DOI: 10.1016/j.molimm.2007.05.009. View

18.

Melvin J, Yule D, Shuttleworth T, Begenisich T . Regulation of fluid and electrolyte secretion in salivary gland acinar cells. Annu Rev Physiol. 2005; 67:445-69. DOI: 10.1146/annurev.physiol.67.041703.084745. View

19.

Merritt J, Rink T . Regulation of cytosolic free calcium in fura-2-loaded rat parotid acinar cells. J Biol Chem. 1987; 262(36):17362-9. View

20.

Maria O, Kim J, Gerstenhaber J, Baum B, Tran S . Distribution of tight junction proteins in adult human salivary glands. J Histochem Cytochem. 2008; 56(12):1093-8. PMC: 2583906. DOI: 10.1369/jhc.2008.951780. View