RARα and RARγ reciprocally control K5⁺ progenitor cell expansion in developing salivary glands

REFERENCES

• Niederreither K, Vermot J, Le Roux I, Schuhbaur B, Chambon P, Dollé P. The regional pattern of retinoic acid synthesis by RALDH2 is essential for the development of posterior pharyngeal arches and the enteric nervous system. Dev Camb Engl. 2003;130(11):2525-2534.
   PubMed Web of Science ®Google Scholar
• Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P. Function of retinoic acid receptor gamma in the mouse. Cell. 1993; 73(4):643-658.
   PubMed Web of Science ®Google Scholar
• Lohnes D, Mark M, Mendelsohn C, Dollé P, Dierich A, Gorry P, Gansmuller A, Chambon P. Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Dev Camb Engl. 1994; 120(10):2723-2748.
   PubMed Web of Science ®Google Scholar
• Schuger L, Varani J, Mitra R, Gilbride K. Retinoic acid stimulates mouse lung development by a mechanism involving epithelial-mesenchymal interaction and regulation of epidermal growth factor receptors. Dev Biol. 1993; 159(2):462-473. doi:10.1006/dbio.1993.1256.
   PubMed Web of Science ®Google Scholar
• Gijbels MJ, van der Ham F, van Bennekum AM, Hendriks HF, Roholl PJ. Alterations in cytokeratin expression precede histological changes in epithelia of vitamin A-deficient rats. Cell Tissue Res. 1992; 268(1):197-203.
   PubMed Web of Science ®Google Scholar
• Kautsky MB, Fleckman P, Dale BA. Retinoic acid regulates oral epithelial differentiation by two mechanisms. J Invest Dermatol. 1995; 104(2):224-230.
   PubMed Web of Science ®Google Scholar
• Malpel S, Mendelsohn C, Cardoso WV. Regulation of retinoic acid signaling during lung morphogenesis. Dev Camb Engl. 2000; 127(14):3057-3067.
   PubMed Web of Science ®Google Scholar
• Wright DM, Buenger DE, Abashev TM, Lindeman RP, Ding J, Sandell LL. Retinoic acid regulates embryonic development of mammalian submandibular salivary glands. Dev Biol. 2015; 407(1):57-67. doi:10.1016/j.ydbio.2015.08.008.
   PubMed Web of Science ®Google Scholar
• Abashev TM, Metzler MA, Wright DM, Sandell LL. Retinoic acid signaling regulates Krt5 and Krt14 independently of stem cell markers in submandibular salivary gland epithelium. Dev Dyn Off Publ Am Assoc Anat. 2017; 246(2):135-147. doi:10.1002/dvdy.24476.
   Web of Science ®Google Scholar
• Wongtrakool C, Malpel S, Gorenstein J, Sedita J, Ramirez MI, Underhill TM, Cardoso WV. Down-regulation of Retinoic Acid Receptor α Signaling Is Required for Sacculation and Type I Cell Formation in the Developing Lung. J Biol Chem. 2003; 278(47):46911-46918. doi:10.1074/jbc.M307977200.
   PubMed Web of Science ®Google Scholar
• Kastner P, Lawrence HJ, Waltzinger C, Ghyselinck NB, Chambon P, Chan S. Positive and negative regulation of granulopoiesis by endogenous RARalpha. Blood. 2001; 97(5):1314-1320.
   PubMed Web of Science ®Google Scholar
• Rosselot C, Spraggon L, Chia I, Batourina E, Riccio P, Lu B, Niederreither K, Dolle P, Duester G, Chambon P, et al. Non-cell-autonomous retinoid signaling is crucial for renal development. Dev Camb Engl. 2010; 137(2):283-292. doi:10.1242/dev.040287.
   PubMed Web of Science ®Google Scholar
• Bourguet W, Germain P, Gronemeyer H. Nuclear receptor ligand-binding domains: three-dimensional structures, molecular interactions and pharmacological implications. Trends Pharmacol Sci. 2000; 21(10):381-388.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf DJ, Evans RM. The RXR heterodimers and orphan receptors. Cell. 1995; 83(6):841-850.
   PubMed Web of Science ®Google Scholar
• See AW-M, Kaiser ME, White JC, Clagett-Dame M. A nutritional model of late embryonic vitamin A deficiency produces defects in organogenesis at a high penetrance and reveals new roles for the vitamin in skeletal development. Dev Biol. 2008; 316(2):171-190. doi:10.1016/j.ydbio.2007.10.018.
   PubMed Web of Science ®Google Scholar
• Chytil F. Retinoids in lung development. FASEB J Off Publ Fed Am Soc Exp Biol. 1996; 10(9):986-992.
   PubMed Web of Science ®Google Scholar
• Niederreither K, Subbarayan V, Dollé P, Chambon P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet. 1999; 21(4):444-448. doi:10.1038/7788.
   PubMed Web of Science ®Google Scholar
• Sandell LL, Lynn ML, Inman KE, McDowell W, Trainor PA. RDH10 Oxidation of Vitamin A Is a Critical Control Step in Synthesis of Retinoic Acid during Mouse Embryogenesis. PLoS ONE. 2012; 7(2):e30698. doi:10.1371/journal.pone.0030698.
   PubMed Web of Science ®Google Scholar
• Wang Z, Dollé P, Cardoso WV, Niederreither K. Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev Biol. 2006; 297(2):433-445. doi:10.1016/j.ydbio.2006.05.019.
   PubMed Web of Science ®Google Scholar
• Dollé P, Fraulob V, Gallego-Llamas J, Vermot J, Niederreither K. Fate of retinoic acid-activated embryonic cell lineages. Dev Dyn Off Publ Am Assoc Anat. 2010; 239(12):3260-3274. doi:10.1002/dvdy.22479.
   Web of Science ®Google Scholar
• Knosp WM, Knox SM, Hoffman MP. Salivary gland organogenesis. Wiley Interdiscip Rev Dev Biol. 2012; 1(1):69-82. doi:10.1002/wdev.4.
   PubMed Web of Science ®Google Scholar
• Nelson DA, Manhardt C, Kamath V, Sui Y, Santamaria-Pang A, Can A, Bello M, Corwin A, Dinn SR, Lazare M, et al. Quantitative single cell analysis of cell population dynamics during submandibular salivary gland development and differentiation. Biol Open. 2013; 2(5):439-447. doi:10.1242/bio.20134309.
   PubMed Web of Science ®Google Scholar
• Gervais EM, Desantis KA, Pagendarm N, Nelson DA, Enger T, Skarstein K, Liaaen Jensen J, Larsen M. Changes in the Submandibular Salivary Gland Epithelial Cell Subpopulations During Progression of Sjögren's Syndrome-Like Disease in the NOD/ShiLtJ Mouse Model. Anat Rec Hoboken NJ 2007. 2015; 298(9):1622-1634. doi:10.1002/ar.23190.
   Google Scholar
• Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature. 2014; 506(7488):322-327. doi:10.1038/nature12948.
   PubMed Web of Science ®Google Scholar
• Knox SM, Lombaert IMA, Reed X, Vitale-Cross L, Gutkind JS, Hoffman MP. Parasympathetic innervation maintains epithelial progenitor cells during salivary organogenesis. Science. 2010; 329(5999):1645-1647. doi:10.1126/science.1192046.
   PubMed Web of Science ®Google Scholar
• Jászai J, Janich P, Farkas LM, Fargeas CA, Huttner WB, Corbeil D. Differential expression of Prominin-1 (CD133) and Prominin-2 in major cephalic exocrine glands of adult mice. Histochem Cell Biol. 2007; 128(5):409-419. doi:10.1007/s00418-007-0334-2.
   PubMed Web of Science ®Google Scholar
• Karbanová J, Missol-Kolka E, Fonseca A-V, Lorra C, Janich P, Hollerová H, Jászai J, Ehrmann J, Kolár Z, Liebers C, et al. The Stem Cell Marker CD133 (Prominin-1) Is Expressed in Various Human Glandular Epithelia. J Histochem Cytochem. 2008; 56(11):977-993. doi:10.1369/jhc.2008.951897.
   PubMed Web of Science ®Google Scholar
• Nedvetsky PI, Emmerson E, Finley J, Ettinger A, Cruz-Pacheco N, Prochazka J, Haddox CL, Northrup E, Hodges C, Mostov KE, et al. Parasympathetic innervation regulates tubulogenesis in the developing salivary gland. Dev Cell. 2014; 30(4):449-462. doi:10.1016/j.devcel.2014.06.012.
   PubMed Web of Science ®Google Scholar
• Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al. Fiji – an Open Source platform for biological image analysis. Nat Methods. 2012; 9(7):676–682. doi:10.1038/nmeth.2019.
   PubMed Web of Science ®Google Scholar
• Lowry R. VassarStats.; 2008. http://vasssarstats.net.
   Google Scholar
• Haimes J, Kelley M. Demonstration of a ddCq calculation method to compute relative gene expression from qPCR data. GE Healthc Tech Note. 2014.
   Google Scholar
• Clagett-Dame M, McNeill EM, Muley PD. Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J Neurobiol. 2006; 66(7):739-756. doi:10.1002/neu.20241.
   PubMedGoogle Scholar
• Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol. 2000; 182(3):311-322. doi:10.1002/(SICI)1097-4652(200003)182:3<311::AID-JCP1>3.0.CO;2-9.
   PubMed Web of Science ®Google Scholar
• Buck SB, Bradford J, Gee KR, Agnew BJ, Clarke ST, Salic A. Detection of S-phase cell cycle progression using 5-ethynyl-2’-deoxyuridine incorporation with click chemistry, an alternative to using 5-bromo-2’-deoxyuridine antibodies. BioTechniques. 2008; 44(7):927-929. doi:10.2144/000112812.
   PubMed Web of Science ®Google Scholar
• Tapia C, Kutzner H, Mentzel T, Savic S, Baumhoer D, Glatz K. Two mitosis-specific antibodies, MPM-2 and phospho-histone H3 (Ser28), allow rapid and precise determination of mitotic activity. Am J Surg Pathol. 2006; 30(1):83-89.
   PubMed Web of Science ®Google Scholar
• Salvesen GS, Dixit VM. Caspases: intracellular signaling by proteolysis. Cell. 1997; 91(4):443-446.
   PubMed Web of Science ®Google Scholar
• Janesick A, Wu SC, Blumberg B. Retinoic acid signaling and neuronal differentiation. Cell Mol Life Sci CMLS. 2015; 72(8):1559-1576. doi:10.1007/s00018-014-1815-9.
   PubMed Web of Science ®Google Scholar
• Wainwright LJ, Lasorella A, Iavarone A. Distinct mechanisms of cell cycle arrest control the decision between differentiation and senescence in human neuroblastoma cells. Proc Natl Acad Sci U S A. 2001; 98(16):9396-9400. doi:10.1073/pnas.161288698.
   PubMed Web of Science ®Google Scholar
• Boylan JF, Lufkin T, Achkar CC, Taneja R, Chambon P, Gudas LJ. Targeted disruption of retinoic acid receptor alpha (RAR alpha) and RAR gamma results in receptor-specific alterations in retinoic acid-mediated differentiation and retinoic acid metabolism. Mol Cell Biol. 1995; 15(2):843-851.
   PubMed Web of Science ®Google Scholar
• Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J Off Publ Fed Am Soc Exp Biol. 1996; 10(9):940-954.
   PubMed Web of Science ®Google Scholar
• Massaro GD, Massaro D. Retinoic acid treatment abrogates elastase-induced pulmonary emphysema in rats. Nat Med. 1997; 3(6):675-677.
   PubMed Web of Science ®Google Scholar
• Hind M, Maden M. Retinoic acid induces alveolar regeneration in the adult mouse lung. Eur Respir J. 2004; 23(1):20-27.
   PubMed Web of Science ®Google Scholar
• Frankenberger M, Heimbeck I, Möller W, Mamidi S, Kassner G, Pukelsheim K, Wjst M, Neiswirth M, Kroneberg P, Lomas D, et al. Inhaled all-trans retinoic acid in an individual with severe emphysema. Eur Respir J. 2009; 34(6):1487-1489. doi:10.1183/09031936.00105309.
   PubMed Web of Science ®Google Scholar
• Mao JT, Goldin JG, Dermand J, Ibrahim G, Brown MS, Emerick A, McNitt-Gray MF, Gjertson DW, Estrada F, Tashkin DP, et al. A pilot study of all-trans-retinoic acid for the treatment of human emphysema. Am J Respir Crit Care Med. 2002; 165(5):718-723. doi:10.1164/ajrccm.165.5.2106123.
   PubMed Web of Science ®Google Scholar
• Roth MD, Connett JE, D'Armiento JM, Foronjy RF, Friedman PJ, Goldin JG, Louis TA, Mao JT, Muindi JR, O'Connor GT, et al. Feasibility of retinoids for the treatment of emphysema study. Chest. 2006; 130(5):1334-1345. doi:10.1378/chest.130.5.1334.
   PubMed Web of Science ®Google Scholar
• Di Rocco A, Uchibe K, Larmour C, Berger R, Liu M, Barton ER, Iwamoto M. Selective Retinoic Acid Receptor γ Agonists Promote Repair of Injured Skeletal Muscle in Mouse. Am J Pathol. 2015; 185(9):2495-2504. doi:10.1016/j.ajpath.2015.05.007.
   PubMed Web of Science ®Google Scholar
• Hind M, Stinchcombe S. Palovarotene, a novel retinoic acid receptor gamma agonist for the treatment of emphysema. Curr Opin Investig Drugs Lond Engl. 2000. 2009; 10(11):1243-1250.
   PubMed Web of Science ®Google Scholar
• Oh DK, Kim Y-S, Oh Y-M. Lung regeneration therapy for chronic obstructive pulmonary disease. Tuberc Respir Dis. 2017; 80(1):1-10. doi:10.4046/trd.2017.80.1.1.
   PubMed Web of Science ®Google Scholar
• Ruijtenberg S, van den Heuvel S. Coordinating cell proliferation and differentiation: Antagonism between cell cycle regulators and cell type-specific gene expression. Cell Cycle. 2016; 15(2):196-212. doi:10.1080/15384101.2015.1120925.
   PubMed Web of Science ®Google Scholar
• Kim YH, Larsen HL, Rué P, Lemaire LA, Ferrer J, Grapin-Botton A. Cell Cycle–Dependent Differentiation Dynamics Balances Growth and Endocrine Differentiation in the Pancreas. PLoS Biol. 2015; 13(3). doi:10.1371/journal.pbio.1002111.
   Web of Science ®Google Scholar
• Yu Z, Lin J, Xiao Y, Han J, Zhang X, Jia H, Tang Y, Li Y. Induction of cell-cycle arrest by all-trans retinoic acid in mouse embryonic palatal mesenchymal (MEPM) cells. Toxicol Sci Off J Soc Toxicol. 2005; 83(2):349-354. doi:10.1093/toxsci/kfi030.
   PubMed Web of Science ®Google Scholar
• Kopan R, Fuchs E. The use of retinoic acid to probe the relation between hyperproliferation-associated keratins and cell proliferation in normal and malignant epidermal cells. J Cell Biol. 1989; 109(1):295-307.
   PubMed Web of Science ®Google Scholar