All-trans-retinoid acid (ATRA) suppresses chondrogenesis of rat primary hind limb bud mesenchymal cells by downregulating p63 and cartilage-specific molecules

Environmental Toxicology and Pharmacology

Volumn 38, Issue 2, 2014, Pages 460-468

  Wang, Yun Guo ^a   Xie, Peng ^a   Wang, Yun Gong ^b   Li, Xue Dong ^c   Zhang, Tao Gen ^c   Liu, Zhao Yong ^c   Hong, Quan ^c   Du, Shi Xin ^a  

^a SECOND HOSPITAL OF TIANJIN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH CHINA   (China)

^c SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

Chondrogenesis; Col2a1; Hind limb bud mesenchymal cells; P63; Retinoic acid; Sox9

Indexed keywords

COL2A1 PROTEIN, RAT; COLLAGEN TYPE 2; PROTEIN P53; RETINOIC ACID; TRANSCRIPTION FACTOR SOX9; TRP63 PROTEIN, RAT; COL2A1 PROTEIN; MESSENGER RNA; PROTEIN P63; UNCLASSIFIED DRUG;

ANIMAL; CELL CULTURE; CELL PROLIFERATION; CHONDROGENESIS; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; EMBRYOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HINDLIMB; LIMB BUD; MALE; METABOLISM; RAT; SPRAGUE DAWLEY RAT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION; GROWTH INHIBITION; IN VITRO STUDY; MESENCHYME CELL; NONHUMAN; PROTEIN EXPRESSION; RNA TRANSCRIPTION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHONDROGENESIS; COLLAGEN TYPE II; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION; HINDLIMB; LIMB BUDS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SOX9 TRANSCRIPTION FACTOR; TRETINOIN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84906063614     PISSN: 13826689     EISSN: 18727077     Source Type: Journal    
DOI: 10.1016/j.etap.2014.07.008     Document Type: Article

References (47)

1. Ahrens P.B., Solursh M., Reiter R.S. Stage-related capacity for limb chondrogenesis in cell culture. Dev. Biol. 1977, 60(1):69-82.
2. Andrea D.Weston, Rosen Vicki, Roshantha A.S., Chandraratna T., Underhill Michael Regulation of skeletal progenitor differentiation by the Bmp and retinoid signaling pathways. J. Cell Biol. 2000, 21(148(4)):679-690.
3. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., De Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev. 2002, 16:2813-2828.
4. Allen J.L., Cooke M.E., Alliston T. ECM stiffness primes the TGFβ pathway to promote chondrocyte differentiation. Mol. Biol. Cell 2012, 23:3731-3742.
5. Bell D.M., Leung K.K., Wheatley S.C., Ng L.J., Zhou S., Ling K.W., Sham M.H., Koopman P., Tam P.P., Cheah K.S. SOX9 directly regulates the type-II collagen gene. Nat. Genet. 1997, 16:174-178.
6. Bruce S.J., Butterfield N.C., Metzis V., Town L., McGlinn E., Wicking C. Inactivation of Patched1 in the mouse limb has novel inhibitory effects on the chondrogenic program. J. Biol. Chem. 2010, 285(36):27967-27981.
7. Chimal-Monroy J., Rodriguez-Leon J., Montero J.A., Gañan Y., Macias D., Merino R., Hurle J.M. Analysis of the molecular cascade responsible for mesodermal limb chondrogenesis: Sox genes and BMP signaling. Dev. Biol. 2003, 257(2):292-301.
8. Chen C.W., Tsai Y.H., Deng W.P., Shih S.N., Fang C.L., Burch J.G., Chen W.H., Lai W.F. Type I and II collagen regulation of chondrogenic differentiation by mesenchymal progenitor cells. J. Orthop. Res. 2005, 23(2):446-453.
9. Lorda-Diez Carlos I., Montero Juan A., Carmen Martinez-Cue, Garcia-Porrero Juan A., Hurle Juan M. Transforming growth factors β coordinate cartilage and tendon differentiation in the developing limb mesenchyme. J. Biol. Chem. 2009, 284(43):29988-29996.
10. de Crombrugghe B., Lefebvre V., Nakashima K. Regulatory mechanisms in the pathways of cartilage and bone formation. Curr. Opin. Cell Biol. 2001, 13(6):721-727.
11. Dietz S., Rother K., Bamberger C., Schmale H., Mössner J., Engeland K. Differential regulation of transcription and induction of programmed cell death by human p53-family members p63 and p73. FEBS Lett. 2002, 525(1-3):93-99.
12. Eames B.F., de la Fuente L., Helms J.A. Molecular ontogeny of the skeleton. Birth Defects Res. C 2003, 69:93-101.
13. Finlan L.E., Hupp T.R. p63: the phantom of the tumor suppressor. Cell Cycle 2007, 6(9):1062-1071.
14. Fernandez-Teran M., Ros M.A. The apical ectodermal ridge: morphological aspects and signaling pathways. Int. J. Dev. Biol. 2008, 52(7):857-871.
15. Gruber H.E., Norton H.J., Ingram J.A., Hanley E.N. The SOX9 transcription factor in the human disc: decreased immunolocalization with age and disc degeneration. Spine (Phila Pa 1976) 2005, 30(6):625-630.
16. Goldring M.B., Tsuchimochi K., Ijiri K. The control of chondrogenesis. J. Cell. Biochem. 2006, 97(1):33-44.
17. Gu J., Lu Y., Qiao L., Ran D., Li N., Cao H., Gao Y., Zheng Q. Mouse p63 variants and chondrogenesis. Int. J. Clin. Exp. Pathol. 2013, 6(12):2872-2879.
18. Huang W., Zhou X., Lefebvre V., de Crombrugghe B. Phosphorylation of SOX9 by cyclic AMP-dependent protein kinase A enhances SOX9's ability to transactivate a Col2a1 chondrocyte-specific enhancer. Mol. Biol. Cell 2000, 20(11):4149-4158.
19. Ide H., Aono H. Retinoic acid promotes proliferation and chondrogenesis in the distal mesodermal cells of chick limb bud. Dev. Biol. 1988, 130(2):767-773.
20. Ikeda T., Kawaguchi H., Kamekura S., Ogata N., Mori Y., Nakamura K., Ikegawa S., Chung U.I. Distinct roles of Sox5, Sox6, and Sox9 in different stages of chondrogenic differentiation. J. Bone Miner. Metab. 2005, 23(5):337-340.
21. Jiang H., Soprano D.R., Li S.W., Soprano K.J., Penner J.D., Gyda M., Kochhar D.M. Modulationoflimb budchondrogenesis byretinoic acid and retinoic acidreceptors. Int. J. Dev. Biol. 1995, 39(4):617-627.
22. Kochhar D.M., Penner J.D., Tellone C.I. Comparative teratogenic activities of two retinoids: effects on palate and limb development. Teratogen. Carcin. Mut. 1984, 4(4):377-387.
23. Kouwenhoven E.N., van Heeringen S.J., Tena J.J., Oti M., Dutilh B.E., Alonso M.E., de la Calle-Mustienes E., Smeenk L., Rinne T., Parsaulian L., Bolat E., Jurgelenaite R., Huynen M.A., Hoischen A., Veltman J.A., Brunner H.G., Roscioli T., Oates E., Wilson M., Manzanares M., Gómez-Skarmeta J.L., Stunnenberg H.G., Lohrum M., van Bokhoven H., Zhou H. Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet. 2010, 6(8):e1001065.
24. Lee G.S., Kochhar D.M., Collins M.D. Retinoid-induced limb malformations. Curr. Pharm. Des. 2004, 10(22):2657-2699.
25. Liu Z.Y., Li X.D., Chen B., Zheng C.Y., Zhong Y.S., Jia Y.L., Du S.X. Retinoic acid retards fetal and hindlimb skeletal development asymmetrically in a retinoic acid-induced clubfoot model. Exp. Toxicol. Pathol. 2010, 62(6):663-670.
26. Lu Y., Abbassi S., Li F., Ding M., Wu G., Gu J., Zheng Q. Distinct function of P63 isoforms during embryonic skeletal development. Gene 2013, 519:251-259.
27. Li F., Lu Y., Ding M., Wu G., Sinha S., Wang S., Zheng Q. Putative function of TAP63α during endochondral bone formation. Gene 2012, 495(2):95-103.
28. Mills A.A., Zheng B., Wang X.J., Vogel H., Roop D.R., Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999, 398(6729):708-713.
29. Mills A.A. P63: oncogene or tumor suppressor?. Curr. Opin. Genet. Dev. 2006, 16:38-44.
30. Ng L.J., Wheatley S., Muscat G.E., Conway-Campbell J., Bowles J., Wright E., Bell D.M., Tam P.P., Cheah K.S., Koopman P. SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev. Biol. 1997, 183:108-121.
31. Paulsen D.F., Chen W.D., Okello D., Johnson B. Stage- and regiondependent responses of chick wing-bud mesenchymal cells to retinoic acid in serum-free microcultures. Dev. Dyn. 1994, 201(4):310-323.
32. Paulsen D.F., Chen W.D., Pang L., Johnson B., Okello D. Stage- and region-dependent chondrogenesis and growth of chick wing-bud mesenchyme in serum-containing and defined tissue culture media. Dev. Dyn. 1994, 200(1):39-52.
33. Perez C.A., Pietenpol J.A. Transcriptional programs regulated by p63 in normal epithelium and tumors. Cell Cycle 2007, 6(3):246-254.
34. Pennimpede T., Cameron D.A., MacLean G.A., Petkovich M. Analysis of Cyp26b1/Rarg compound-null mice reveals two genetically separable effects of retinoic acid on limb outgrowth. Dev. Biol. 2010, 339:179-186.
35. Reisler T.T., Patton M.A., Meagher P.P. Further phenotypic and genetic variation in ADULT syndrome. Am. J. Med. Genet. A 2006, 140(22):2495-2500.
36. Rinne T., Brunner H.G., van Bokhoven H. P63-associated disorders. Cell Cycle 2007, 6(3):262-268.
37. Rouleau M., Medawar A., Hamon L., Shivtiel S., Wolchinsky Z., Zhou H., De Rosa L., Candi E., de la Forest Divonne S., Mikkola M.L., van Bokhoven H., Missero C., Melino G., Pucéat M., Aberdam D. TAp63 is important for cardiac differentiation of embryonic stem cells and heart development. Stem Cells 2011, 29:1672-1683.
38. Santos-Alvarez I., Martos-Rodríguez A., Delgado-Baeza E. Embryonic blastemic changes in retinoic acid-induced hindlimb deformity. Cells Tissues Organs 2003, 173:217-226.
39. Trink B., Osada M., Ratovitski E., Sidransky D. p63 transcriptional regulation of epithelial integrity and cancer. Cell Cycle 2007, 6(3):240-245.
40. Tadini G., Santagada F., Brena M., Pezzani L., Nannini P. Ectodermal dysplasias: the p63 tail. Giornale Italiano DI Dermatologiae Venereologia 2013, 148(1):53-58.
41. van Bokhoven H., Hamel B.C., Bamshad M., Sangiorgi E., Gurrieri F., Duijf P.H., Vanmolkot K.R., van Beusekom E., van Beersum S.E., Celli J., Merkx G.F., Tenconi R., Fryns J.P., Verloes A., Newbury-Ecob R.A., Raas-Rotschild A., Majewski F., Beemer F.A., Janecke A., Chitayat D., Crisponi G., Kayserili H., Yates J.R., Neri G., Brunner H.G. p63 gene mutations in EEC syndrome, limb-mammary syndrome, and isolated split hand-split foot malformation suggest a genotype-phenotype correlation. Am. J. Hum. Genet. 2001, 69(3):481-492.
42. Wu G., Nomoto S., Hoque M.O., Dracheva T., Osada M., Lee C.C., Dong S.M., Guo Z., Benoit N., Cohen Y., Rechthand P., Califano J., Moon C.S., Ratovitski E., Jen J., Sidransky D., Trink B. DeltaNp63alpha and TAp63alpha regulate transcription of genes with distinct biological functions in cancer and development. Cancer Res. 2003, 63(10):2351-2357.
43. Wu G., Osada M., Guo Z., Fomenkov A., Begum S., Zhao M., Upadhyay S., Xing M., Wu F., Moon C., Westra W.H., Koch W.M., Mantovani R., Califano J.A., Ratovitski E., Sidransky D., Trink B. DeltaNp63alpha up-regulates the Hsp70 gene in human cancer. Cancer Res. 2005, 65(3):758-766.
44. Yang A., Schweitzer R., Sun D., Kaghad M., Walker N., Bronson R.T., Tabin C., Sharpe A., Caput D., Crum C., McKeon F. p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 1999, 398(6729):714-718.
45. Yu Z., Xing Y. All-trans retinoic acid inhibited chondrogenesis of mouse embryonic palate mesenchymal cells by down-regulation of TGF-beta/Smad signaling. Biochem. Biophys. Res. Commun. 2006, 340(3):929-934.
46. Zhou J., Kochhar D.M. Cellular anomalies underlying retinoid-induced phocomelia. Reprod. Toxicol. 2004, 19:103-110.
47. Zhong Y.S., Zheng C., Jia Y., Xu G.T., Liu Z.Y., Chen B., Du S.X. Quantitative evaluation in vivo of the degree of differentiation of hindlimb cartilage in a rat clubfoot model. Toxicol. Mech. Method 2009, 19(4):292-297.