Differential effects of several retinoid receptor-selective ligands on squamous differentiation and apoptosis in airway epithelial cells

Cell and Tissue Research

Volumn 300, Issue 1, 2000, Pages 67-81

  Boisvieux Ulrich, Emmanuelle ^a   Le Pechon Vallée, Caroline ^b   Million, Karine ^a   Baeza Squiban, Armelle ^a   Houcine, Odile ^a   Guennou, Christiane ^a   Reichert, Uwe ^c   Marano, Francelyne ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c Galderma R and D   (France)

Author keywords

Airway epithelial cells; Apoptosis; CD437; Cell culture; Cytokeratins; Rabbit; Retinoid receptors; Squamous metaplasia

Indexed keywords

4 (5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 ANTHRYL)BENZOIC ACID; 6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; 6 [4 METHOXY 3 (1 METHYLCYCLOHEXYL)PHENYL] 2 NAPHTHOIC ACID; BROXURIDINE; CYTOKERATIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; RECEPTOR SUBTYPE; RETINOIC ACID RECEPTOR; RETINOID RECEPTOR; RETINOID X RECEPTOR; UNCLASSIFIED DRUG; VITAMIN RECEPTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; BASAL CELL; CELL CULTURE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL LABELING; CELL PROLIFERATION; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA CLEAVAGE; ELECTRON MICROSCOPY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FLOW CYTOMETRY; KERATINIZATION; MITOSIS INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; RECEPTOR INTRINSIC ACTIVITY; RESPIRATORY EPITHELIUM; SQUAMOUS CELL METAPLASIA;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZOATES; CELL DIFFERENTIATION; CELLS, CULTURED; DNA FRAGMENTATION; EPITHELIAL CELLS; KERATINS; LIGANDS; METAPLASIA; MICROSCOPY, ELECTRON; NAPHTHALENES; NECROSIS; RABBITS; RECEPTORS, RETINOIC ACID; RETINOIDS; S PHASE; TERATOGENS; TETRAHYDRONAPHTHALENES; TRACHEA;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0034035646     PISSN: 0302766X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004410050048     Document Type: Article

References (78)

1. Achtstäetter T, Hatzfeld M, Quilan RA, Parmelee DC, Franke WW (1986) Separation of cytokeratin polypeptides by gel electrophoresis and Chromatographic techniques and their identification by immunoblotting. Methods Enzymol 134:355-371
2. Adachi H, Preston G, Harvat B, Dawson M, Jetten AM (1998a) Inhibition of cell proliferation and induction of apoptosis by the retinoid AHPN in human lung carcinoma cells. Am J Respir Cell Mol Biol 18:323-333
3. Adachi H, Adams A, Hughes FM, Zhang J, Cidlowski JA, Jetten AM (1998b) Induction of apoptosis by the novel retinoid AHPN in human T-cell lymphoma cells involves caspase-dependent and independent pathways. Cell Death Differ 5:973-983
4. Arends MJ, Wyllie AH (1991) Apoptosis: mechanisms and roles in pathology. Int Rev Exp Pathol 32:223-254
5. Baeza-Squiban A, Romet S, Moreau A, Marano F (1991) Progress in outgrowth culture from rabbit tracheal explants balance between proliferation and maintenance of differentiated state in epithelial cells. In Vitro Cell Dev Biol 27A:453460
6. Baeza-Squiban A, Boisvieux-Ulrich E, Guillianelli C, Houcine O, Geraud G, Guennou C, Marano F (1994) Extracellular matrix dependent differentiation of rabbit tracheal epithelial cells in primary culture. In Vitro Cell Dev Biol 30A:56-67
7. Bernard BA, Bernardon JM, Delescluse C, Martin B, Lenoir MC, Maignan J, Charpentier B, Pilgrim WR, Reichert U, Shroot B (1992) Identification of synthetic retinoids with a selectivity for human nuclear retinoic acid receptor. Biochem Biophys Res Comm 186:977-983
8. 3. J Invest Dermatol 98:42S-49S
9. Boers JE, Ten Velde GPM, Thunnissen BJM (1996) P53 in squamous metaplasia: a marker for risk of respiratory tract carcinoma. Am J Respir Crit Care Med 153:411-416
10. 1 promotes actin cytoskeleton reorganization and migratory phenotype in epithelial tracheal cells in primary culture. J Cell Sci 109:2207-2219
11. Broaddus VC, Yang L, Scavo LM, Ernst JD, Boylan AM (1996) Asbestos induces apoptosis of human and rabbit pleural mesothelial cells via reactive oxygen species. J Clin Invest 98: 2050-2059
12. Cardoso WV (1995) Transcription factors and pattern formation in the developing lung. Am J Physiol (Lung Cell Mol Physiol 13):L429-L442
13. Chiba H, Clifford J, Metzger D, Chambon P (1997) Specific and redundant functions of retinoid X/retinoic acid receptor heterodimers in differentiation, proliferation, and apoptosis of F9 embryonal carcinoma cells. J Cell Biol 139:735-747
14. Chytil F (1992) The lungs and vitamin A. Am J Physiol (Lung Cell Mol Physiol 6):L517-L527
15. Crowe DL, Hu L, Gudas LJ, Rheinwald JG (1991) Variable expression of retinoic acid receptor (RARβ) mRNA in human oral epidermal keratinocytes; relation to keratin 19 expression and keratinization potential. Differentiation 48:199-208
16. Darwiche NN, Celli GG, Tennenbaum T, Glick AB, Yuspa SH, De Luca LM (1995) Mouse skin tumor progression results in differential expression of retinoic acid and retinoid X receptors. Cancer Res 55:2774-2782
17. De Luca LM (1991) Retinoids and their receptors in differentiation, embryogenesis, and neoplasia. FASEB J 5:2924-2933
18. Dolle P, Rubert E, Leroy P, Moriss-Kay G, Chambon P (1990) Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development 110:1133-1151
19. Elledge RM, Lee WH (1995) Life and death by p53. Bioessays 17:923-930
20. Feldmann G (1995) L'apoptose ou la mort cellulaire programmée. Ann Pathol 15:92-109
21. Fisher GJ, Talwar HS, Xiao JS, Datta SC, Reddy AP, Gaub MP, Rochette-Egly C, Chambon P, Voorhees JJ (1994) Immunological identification and functional quantitation of retinoic acid and retinoid X receptor proteins in human skin. J Biol Chem: 269 20629-20635
22. Floyd EE, Jetten AM (1989) Regulation of type I (epidermal) transglutaminase mRNA levels during squamous differentiation: down regulation by retinoids. Mol Cell Biol 9:4846-4851
23. Fuchs E (1990) Epidermal differentiation: the bare essentials. J Cell Biol 111:2807-2814
24. Fuchs E (1995) Keratins and the skin. Ann Rev Cell Dev Biol 11:123-154
25. Fuchs E, Green H (1981) Regulation of terminal differentiation of cultured human keratinocytes by vitamin A. Cell 25:617-625
26. Glass CK (1994) Differential recognition of target genes by nuclear receptor monomers, dimers and heterodimers. Endocr Rev 15:1503-1519
27. Green H (1977) Terminal differentiation of cultured human epidermal cells. Cell 11:405-415
28. Heyman RA, Mangelsdorf DJ, Dyck JA, Stein RB, Eichele G, Evans RM, Thaller C (1992) 9-cis retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68:397-406
29. Hsu CA, Rishi AK, Su-Li X, Gerald TM, Dawson MI, Schiffer C, Reichert U, Shoot B, Poirier GC, Fontana JA (1997) Retinoid induced apoptosis in leukemia cells through a retinoic acid nuclear receptor-independent pathway. Blood 89:4470-4479
30. Jetten AM (1989) Multistep process of squamous differentiation in tracheobronchial epithelial cells in vitro: analogy with epidermal differentiation. Environ Health Perspect 80:149-160
31. Jetten AM (1991) Growth and differentiation factors in tracheobronchial epithelium. Am J Physiol 260 (Lung Cell Mol Physiol 4):L361-1373
32. Jetten AM, Shirley JE (1986) Characterization of transglutaminase activity in rabbit tracheal epithelial cells. J Biol Chem 261: 15097-15101
33. Jetten AM, George MA, Smits HL, Vollberg TM (1989) Keratin 13 is linked to squamous differentiation in rabbit tracheal epithelial cells and down-regulated by retinoic acid. Exp Cell Res 182:622-634
34. Jetten AM, Vollberg TM, Nervi C, George MD (1990) Positive and negative regulation of proliferation and differentiation in tracheobronchial epithelial cells. Am Rev Respir Dis 142:S36-S39
35. Kaartinen L, Nettesheim P, Adler KB, Randell SH (1993) Rat tracheal epithelial cell differentiation in vitro. In Vitro Cell Dev Biol 29:481-492
36. Klein N, Vignaud JM, Sadmi M, Plenat F, Borelly J, Duprez A, Martinet Y, Martinet M (1993) Squamous metaplasia expression of proto-oncogenes and P53 in lung cancer patients. Lab Invest 68:26-32
37. Kopan R, Traska G, Fuchs E (1987) Retinoids as important regulators of terminal differentiation: examining keratin expression in individual epidermal cells at various stages of keratinization. J Cell Biol 105:427-440
38. Lazebnik YA, Cole S, Cooke CA, Nelson WG, Earnshaw WC (1993) Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J Cell Biol 123:7-22
39. Lee HY, Dawson MI, Claret FX, Chen JD, Walsh GL, Hong WK, Kurie JM (1997) Evidence of a retinoid signalling alteration involving the activator protein 1 complex in tumorigenic human bronchial epithelial cells and non-small cell lung cancer cells. Cell Growth Differ 8:283-291
40. Leube RE, Rustad TJ (1991) Squamous metaplasia in the human lung: molecular characteristics of epithelial stratification. Virchows Arch B 61:227-253
41. waf1/cip1 expression in human breast carcinoma cells. Cancer Res 56:5055-5062
42. Lotan R (1994) Suppression of squamous cell carcinoma growth and differentiation by retinoids. Cancer Res 54:1987s-1990s
43. Martin B, Bernardon J-M, Cavey MT, Bernard B, Carlavan I, Charpentier B, Pilgrim WR, Shroot B, Reichert U (1992) Selective synthetic ligands for human retinoic acid receptors. Skin Pharmacol 5:57-65
44. Melino G, Draoui M, Bellincampi L, Bernassola F, Bernardini S, Piacentini M, Reichert U, Cohen P (1997) Retinoic acid receptors α and γ mediate the induction of "tissue" transglutaminase activity and apoptosis in human neuroblastoma cells. Exp Cell Res 235:55-61
45. Michel S, Reichert U, Isnard JL, Shroot B, Schmidt R (1989) Retinoic acid controls expression of epidermal transglutaminase at the pre-translational level. FEBS Lett 258:35-38
46. Monzon RI, LaPres JJ, Hudson LG (1996) Regulation of involucrin gene expression by retinoic acid and glucocorticoids. Cell Growth Differ 7:1751-1759
47. Nervi C, Vollberg TM, George MD, Zelent A, Chambon P, Jetten AM (1991) Expression of nuclear retinoic receptors in normal tracheobronchial cells and in lung carcinoma cells. Exp Cell Res 195:163-170
48. Piedrafita FJ, Pfahl M (1997) Retinoid-induced apoptosis and Sp1 cleavage occur independently of transcription and require caspase activation. Mol Cell Biol 17:6348-6358
49. Oridate N, Higuchi M, Suzuki S, Shroot B, Hong WK, Lotan R (1997) Rapid induction of apoptosis in human C33 cervical carcinoma cells by the synthetic retinoid 6-[3-(1-adamantyl)hydroxyphenyl]-2-naphthalene carboxylic acid (CD437). Int J Cancer 70:484-487
50. Orren DK, Petersen LN, Bohr VA (1997) Persistent damage inhibits S-phase and G2 progression, and results in apoptosis. Mol Biol Cell 8:1129-1142
51. Reichert U, Bernardon JM, Charpentier R, Nedoncelle P, Martin B, Bernard BA, Asselineau D, Michel S, Lenoir MC, Delescluse C, Pilgrim WR, Darmon YM, Shroot B (1993a) Synthetic retinoids: receptor selectivity and biological activity. In: Bernard BA, Shroot B (eds) From molecular biology to therapeutics. Pharmacol skin, vol 5. Karger, Basel, pp 117-127
52. Reichert U, Michel S, Schmidt R (1993b) The cornified envelope: a key structure of terminally differentiating keratinocytes. In: Darmon M (ed) Molecular biology of the skin: the keratinocytes. Academic Press, Nice, France, pp 107-150
53. Rice RH, Green H (1979) Presence in human epidermal cells of a soluble protein precursor of the cross-linked envelope: activation of the crosslinking by calcium ions. Cell 18:681-694
54. Rubin AL, Rice RH (1986) Differential regulation by retinoic acid and calcium of transglutaminases in cultured neoplastic and normal keratinocytes. Cancer Res 46:2356-2361
55. Saunders NA, Bernacki SH, Vollberg TM, Jetten AM (1993) Regulation of transglutaminase type I expression in squamous differentiating rabbit tracheal epithelial cells and human epidermal keratinocytes: effects of retinoic acid and phorbol esters. Mol Endocrinol 7:387-398
56. Schadendorf D, Worm M, Jurkovsky K, Dippel E, Michel S, Charpentier B, Bernardon JM, Reichert U, Czarnetzki BM (1995) Retinoic acid receptor-γ-selective retinoids exert antiproliferative effects on human melanoma cell growth in vitro. Int J Oncol 5:1325-1331
57. Schadendorf D, Kern MA, Artuc M, Pahl HL, Rosenbach T, Fichtner I, Nürnberg W, Stüting S, Stebut E, Worm M, Makki A, Jurgovsky K, Kolde G, Hens B (1996) Treatment with the synthetic retinoid CD 437 induces apoptosis via activation of AP-1 in vitro, and causes growth inhibition in xenografts in vivo. J Cell Biol 135:1889-1898
58. Schmidt R, Michel S, Shoot B, Reichert U (1988a) Plasma membrane transglutaminase and cytosolic transglutaminase form distinct envelope-like structures in transformed human keratinocytes. FEBS Lett 229:193-196
59. Schmidt R, Michel S, Shoot B, Reichert U (1988b) Transglutaminases in normal and transformed human keratinocytes in culture. J Invest Dermatol 90:475-479
60. Schwartzman RA, Cidlowski JA (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocr Rev 14:133-150
61. Shalinsky DR, Bischoff ED, Gregory ML, Gottardis MM, Hayes JS, Lamph WW, Heyman RA, Shirley MA, Cooke TA, Davies PJA, Thomazy V (1995) Retinoid-induced suppression of squamous cell differentiation in human oral squamous cell carcinoma xenografts (Line 1483) in athymic nude mice. Cancer Res 55:3183-3191
62. 1 arrest and apoptosis induced by a novel retinoid in human breast cancer cells. Oncogene 11:493-504
63. Shroot B, Martin B, Bernardon JM, Cavey MT, Bernard A, Carlavan I, Charpentier B, Pilgrim WR, Reichert U (1993) Selective synthetic ligands for nuclear retinoic acid receptor sub-types. In: Livrea MA, Packer L (eds) Retinoids. Progress in research and clinical applications. Marcel Dekker, New York, pp 261-268
64. Spanjaard RA, Ikeda M, Lee PJ, Charpentier B, Chin WW, Eberlein TJ (1997) Specific activation of retinoic acid receptors (RARs) and retinoid X receptors reveal a unique role for RAR gamma in induction of differentiation and apoptosis of S91 melanoma cells. J Biol Chem 272:18990-18999
65. Stahlman MT, Gray ME, Chytil F, Sundell H (1988) Effect of retinal on fetal lamb tracheal epithelium, with and without epidermal growth factor. Lab Invest 59:25-35
66. Stoler A, Kopan R, Duvic M, Fuchs E (1988) Use of monospecific antisera and cRNA probes to localize the major changes in keratin expression during normal and abnormal epidermal differentiation. J Cell Biol 107:427-446
67. Stosiek P, Kasper M, Moll R (1992) Changes in cytokeratin expression accompany squamous metaplasia of the human respiratory epithelium. Virchows Arch A Pathol Anat 421:133-141
68. Swisshelm K, Ryan K, Lee X, Tsou HC, Peacocke M, Sager R (1994) Down-regulation of retinoic acid receptor β in mammary carcinoma cell lines and its up-regulation in senescing normal mammary epithelial cells. Cell Growth Differ 5:133-141
69. Szondy Z, Reichert U, Bernardon JM, Michel S, Toth R, Ancian P, Ajzner E, Fésüs L (1997) Induction of apoptosis by retinoids and RARγ selective compounds in mouse thymocytes through a novel apoptosis pathway. Mol Pharmacol 51:972-982
70. Szondy Z, Reichert U, Fésüs L (1998) Retinoic acids regulate apoptosis of T lymphocytes through an interplay between RAR and RXR receptors. Cell Death Differ 5:4-10
71. Thacher SM, Rice RH (1985) Keratinocyte-specific transglutaminase of cultured human epidermal cells: relation to cross-linked envelope formation and terminal differentiation. Cell 40:685-695
72. Tomic M, Jiang CK, Epstein HS, Freedberg IM, Samuels HH, Blumenberg M (1990) Nuclear receptors for retinoic acid and thyroid hormone regulate transcription of keratin genes. Cell Regul 1:965-973
73. Tomic-Canic M, Sunjevaric I, Freedberg IM, Blumenberg M (1992) Identification of the retinoic acid and thyroid hormone receptor-responsive element in the human K14 keratin gene. J Invest Dermatol 99:842-847
74. van Engeland M, Kuijpers HJH, Ramaekers FCS, Reutelingsperger CPM, Schutte B (1997) Plasma membrane alterations and cytoskeletal changes in apoptosis. Exp Cell Res 235:421-430
75. van Muijen GNP, Ruiter DJ, Franke WW, Achtstäetter T, Haasnoot WHB, Ponec M, Warnaar SO (1986) Cell type heterogeneity of cytokeratin expression in complex epithelia and carcinomas as demonstrated by monoclonal antibodies specific for cytokeratins nos. 4 and 13. Exp Cell Res 162:97-113
76. Weiss RA, Eichner R, Sun TT (1984) Monoclonal antibody analysis of keratin expression in epidermal diseases: a 48 kd and a 56 kd keratin as molecular markers for hyperproliferative keratinocytes. J Cell Biol 98:1397-1406
77. Wyllie AH, Kerr JFR, Curie AR (1980) Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306
78. Zhang LX, Mills KJ, Dawson MI, Collins SJ, Jetten AM (1995) Evidence for the involvement of retinoic acid receptor RARα-dependent signaling pathway in the induction of tissue transglutaminase and apoptosis. J Biol Chem 270:6022-6029