Zfp521 is a target gene and key effector of parathyroid hormone-related peptide signaling in growth plate chondrocytes

Developmental Cell

Volumn 19, Issue 4, 2010, Pages 533-546

  Correa, Diego ^a   Hesse, Eric ^a   Seriwatanachai, Dutmanee ^a   Kiviranta, Riku ^a   Saito, Hiroaki ^a   Yamana, Kei ^a,b   Neff, Lynn ^a   Atfi, Azeddine ^a   Coillard, Lucie ^a   Sitara, Despina ^a   Maeda, Yukiko ^a   Warming, Soren ^c   Jenkins, Nancy A ^d   Copeland, Neal G ^d   Horne, William C ^a   Lanske, Beate ^a   Baron, Roland ^a,e  

^a HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^b TEIJIN PHARMA LIMITED   (Japan)

^c GENENTECH INC   (United States)

^d INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CASPASE 3; COLLAGEN TYPE 10; CYCLIN D1; GENE PRODUCT; HISTONE DEACETYLASE 4; PARATHYROID HORMONE RELATED PROTEIN; PROTEIN BCL 2; PROTEIN ZFP521; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; BIOLOGICAL MARKER; EVI3 PROTEIN, MOUSE; HDAC5 PROTEIN, MOUSE; HISTONE DEACETYLASE; REPRESSOR PROTEIN; RUNX2 PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; BONE GROWTH; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE; GENE DELETION; GROWTH PLATE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; THICKNESS; UPREGULATION; ZFP521 GENE; ANIMAL; BONE DEVELOPMENT; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; HYPERTROPHY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CHONDROCYTES; CORE BINDING FACTOR ALPHA 1 SUBUNIT; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH PLATE; HISTONE DEACETYLASES; HYPERTROPHY; MICE; MICE, KNOCKOUT; OSTEOGENESIS; PARATHYROID HORMONE-RELATED PROTEIN; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; BIOMARKERS;

ERINACEIDAE; MUS;

EID: 77957883340     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2010.09.008     Document Type: Article

References (48)

1. Amizuka N., Warshawsky H., Henderson J.E., Goltzman D., Karaplis A.C. Parathyroid hormone-related peptide-depleted mice show abnormal epiphyseal cartilage development and altered endochondral bone formation. J. Cell Biol. 1994, 126:1611-1623.
2. Amizuka N., Henderson J.E., Hoshi K., Warshawsky H., Ozawa H., Goltzman D., Karaplis A.C. Programmed cell death of chondrocytes and aberrant chondrogenesis in mice homozygous for parathyroid hormone-related peptide gene deletion. Endocrinology 1996, 137:5055-5067.
3. Amizuka N., Davidson D., Liu H., Valverde-Franco G., Chai S., Maeda T., Ozawa H., Hammond V., Ornitz D.M., Goltzman D., et al. Signalling by fibroblast growth factor receptor 3 and parathyroid hormone-related peptide coordinate cartilage and bone development. Bone 2004, 34:13-25.
4. Amling M., Neff L., Tanaka S., Inoue D., Kuida K., Weir E., Philbrick W.M., Broadus A.E., Baron R. Bcl-2 lies downstream of parathyroid hormone-related peptide in a signaling pathway that regulates chondrocyte maturation during skeletal development. J. Cell Biol. 1997, 136:205-213.
5. Arnold M.A., Kim Y., Czubryt M.P., Phan D., McAnally J., Qi X., Shelton J.M., Richardson J.A., Bassel-Duby R., Olson E.N. MEF2C transcription factor controls chondrocyte hypertrophy and bone development. Dev. Cell 2007, 12:377-389.
6. Beier F., Leask T.A., Haque S., Chow C., Taylor A.C., Lee R.J., Pestell R.G., Ballock R.T., LuValle P. Cell cycle genes in chondrocyte proliferation and differentiation. Matrix Biol. 1999, 18:109-120.
7. Beier F., Ali Z., Mok D., Taylor A.C., Leask T., Albanese C., Pestell R.G., LuValle P. TGFbeta and PTHrP control chondrocyte proliferation by activating cyclin D1 expression. Mol. Biol. Cell 2001, 12:3852-3863.
8. Bond H.M., Mesuraca M., Carbone E., Bonelli P., Agosti V., Amodio N., De Rosa G., Di Nicola M., Gianni A.M., Moore M.A.S., et al. Early hematopoietic zinc finger protein (EHZF), the human homolog to mouse Evi3, is highly expressed in primitive human hematopoietic cells. Blood 2004, 103:2062-2070.
9. Bond H.M., Mesuraca M., Amodio N., Mega T., Agosti V., Fanello D., Pelaggi D., Bullinger L., Grieco M., Moore M.A., et al. Early hematopoietic zinc finger protein-zinc finger protein 521: a candidate regulator of diverse immature cells. Int. J. Biochem. Cell Biol. 2008, 40:848-854.
10. Chen L., Adar R., Yang X., Monsonego E.O., Li C., Hauschka P.V., Yayon A., Deng C.X. Gly369Cys mutation in mouse FGFR3 causes achondroplasia by affecting both chondrogenesis and osteogenesis. J. Clin. Invest. 1999, 104:1517-1525.
11. Enomoto H., Enomoto-Iwamoto M., Iwamoto M., Nomura S., Himeno M., Kitamura Y., Kishimoto T., Komori T. Cbfa1 is a positive regulatory factor in chondrocyte maturation. J. Biol. Chem. 2000, 275:8695-8702.
12. Guo J., Chung U.I., Yang D., Karsenty G., Bringhurst F.R., Kronenberg H.M. PTH/PTHrP receptor delays chondrocyte hypertrophy via both Runx2-dependent and -independent pathways. Dev. Biol. 2006, 292:116-128.
13. Haberland M., Montgomery R.L., Olson E.N. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 2009, 10:32-42.
14. Hunziker E.B., Schenk R.K., Cruz-Orive L.M. Quantitation of chondrocyte performance in growth-plate cartilage during longitudinal bone growth. J. Bone Joint Surg. Am. 1987, 69:162-173.
15. Inada M., Yasui T., Nomura S., Miyake S., Deguchi K., Himeno M., Sato M., Yamagiwa H., Kimura T., Yasui N., et al. Maturational disturbance of chondrocytes in Cbfa1-deficient mice. Dev. Dyn. 1999, 214:279-290.
16. Iwamoto M., Kitagaki J., Tamamura Y., Gentili C., Koyama E., Enomoto H., Komori T., Pacifici M., Enomoto-Iwamoto M. Runx2 expression and action in chondrocytes are regulated by retinoid signaling and parathyroid hormone-related peptide (PTHrP). Osteoarthritis Cartilage 2003, 11:6-15.
17. Justice M.J., Morse H.C., Jenkins N.A., Copeland N.G. Identification of Evi-3, a novel common site of retroviral integration in mouse AKXD B-cell lymphomas. J. Virol. 1994, 68:1293-1300.
18. Kang J.S., Alliston T., Delston R., Derynck R. Repression of Runx2 function by TGF-beta through recruitment of class II histone deacetylases by Smad3. EMBO J. 2005, 24:2543-2555.
19. Kim I.S., Otto F., Zabel B., Mundlos S. Regulation of chondrocyte differentiation by Cbfa1. Mech. Dev. 1999, 80:159-170.
20. Kobayashi T., Chung U.I., Schipani E., Starbuck M., Karsenty G., Katagiri T., Goad D.L., Lanske B., Kronenberg H.M. PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 2002, 129:2977-2986.
21. Kozhemyakina E., Cohen T., Yao T.P., Lassar A.B. Parathyroid hormone-related peptide represses chondrocyte hypertrophy through a protein phosphatase 2A/histone deacetylase 4/MEF2 pathway. Mol. Cell. Biol. 2009, 29:5751-5762.
22. Kronenberg H.M. Developmental regulation of the growth plate. Nature 2003, 423:332-336.
23. Kronenberg H.M. PTHrP and skeletal development. Ann. N Y Acad. Sci. 2006, 1068:1-13.
24. La Rocca R., Fulciniti M., Lakshmikanth T., Mesuraca M., Ali T.H., Mazzei V., Amodio N., Catalano L., Rotoli B., Ouerfelli O., et al. Early hematopoietic zinc finger protein prevents tumor cell recognition by natural killer cells. J. Immunol. 2009, 182:4529-4537.
25. Lanske B., Amling M., Neff L., Guiducci J., Baron R., Kronenberg H.M. Ablation of the PTHrP gene or the PTH/PTHrP receptor gene leads to distinct abnormalities in bone development. J. Clin. Invest. 1999, 104:399-407.
26. Lefebvre V., Garofalo S., Zhou G., Metsaranta M., Vuorio E., De Crombrugghe B. Characterization of primary cultures of chondrocytes from type II collagen/beta-galactosidase transgenic mice. Matrix Biol. 1994, 14:329-335.
27. Li T.F., Dong Y., Ionescu A.M., Rosier R.N., Zuscik M.J., Schwarz E.M., O'Keefe R.J., Drissi H. Parathyroid hormone-related peptide (PTHrP) inhibits Runx2 expression through the PKA signaling pathway. Exp. Cell Res. 2004, 299:128-136.
28. Long F., Zhang X.M., Karp S., Yang Y., McMahon A.P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 2001, 128:5099-5108.
29. Lupu F., Terwilliger J.D., Lee K., Segre G.V., Efstratiadis A. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev. Biol. 2001, 229:141-162.
30. Maeda Y., Nakamura E., Nguyen M.T., Suva L.J., Swain F.L., Razzaque M.S., Mackem S., Lanske B. Indian Hedgehog produced by postnatal chondrocytes is essential for maintaining a growth plate and trabecular bone. Proc. Natl. Acad. Sci. USA 2007, 104:6382-6387.
31. Matsubara E., Sakai I., Yamanouchi J., Fujiwara H., Yakushijin Y., Hato T., Shigemoto K., Yasukawa M. The role of zinc finger protein 521/early hematopoietic zinc finger protein in erythroid cell differentiation. J. Biol. Chem. 2009, 284:3480-3487.
32. Nutt R.F., Caulfield M.P., Levy J.J., Gibbons S.W., Rosenblatt M., McKee R.L. Removal of partial agonism from parathyroid hormone (PTH)-related protein-(7-34)NH2 by substitution of PTH amino acids at positions 10 and 11. Endocrinology 1990, 127:491-493.
33. Porter A.G., Janicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 1999, 6:99-104.
34. Purev E., Neff L., Horne W.C., Baron R. c-Cbl and Cbl-b Act redundantly to protect osteoclasts from apoptosis and to displace HDAC6 from {beta}-tubulin, stabilizing microtubules and podosomes. Mol. Biol. Cell 2009, 20:4021-4030.
35. Razzaque M.S., Soegiarto D.W., Chang D., Long F., Lanske B. Conditional deletion of Indian hedgehog from collagen type 2alpha1-expressing cells results in abnormal endochondral bone formation. J. Pathol. 2005, 207:453-461.
36. Schipani E., Jensen G.S., Pincus J., Nissenson R.A., Gardella T.J., Juppner H. Constitutive activation of the cyclic adenosine 3',5'-monophosphate signaling pathway by parathyroid hormone (PTH)/PTH-related peptide receptors mutated at the two loci for Jansen's metaphyseal chondrodysplasia. Mol. Endocrinol. 1997, 11:851-858.
37. Schroeder T.M., Kahler R.A., Li X., Westendorf J.J. Histone deacetylase 3 interacts with Runx2 to repress the osteocalcin promoter and regulate osteoblast differentiation. J. Biol. Chem. 2004, 279:41998-42007.
38. Shukunami C., Shigeno C., Atsumi T., Ishizeki K., Suzuki F., Hiraki Y. Chondrogenic differentiation of clonal mouse embryonic cell line ATDC5 in vitro: differentiation-dependent gene expression of parathyroid hormone (PTH)/PTH-related peptide receptor. J. Cell Biol. 1996, 133:457-468.
39. Takeda S., Bonnamy J.P., Owen M.J., Ducy P., Karsenty G. Continuous expression of Cbfa1 in nonhypertrophic chondrocytes uncovers its ability to induce hypertrophic chondrocyte differentiation and partially rescues Cbfa1-deficient mice. Genes Dev. 2001, 15:467-481.
40. Ueta C., Iwamoto M., Kanatani N., Yoshida C., Liu Y., Enomoto-Iwamoto M., Ohmori T., Enomoto H., Nakata K., Takada K., et al. Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J. Cell Biol. 2001, 153:87-100.
41. Vega R.B., Matsuda K., Oh J., Barbosa A.C., Yang X., Meadows E., McAnally J., Pomajzl C., Shelton J.M., Richardson J.A., et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 2004, 119:555-566.
42. Warming S., Liu P., Suzuki T., Akagi K., Lindtner S., Pavlakis G.N., Jenkins N.A., Copeland N.G. Evi3, a common retroviral integration site in murine B-cell lymphoma, encodes an EBFAZ-related Krüppel-like zinc finger protein. Blood 2003, 101:1934-1940.
43. Weir E.C., Philbrick W.M., Amling M., Neff L.A., Baron R., Broadus A.E. Targeted overexpression of parathyroid hormone-related peptide in chondrocytes causes chondrodysplasia and delayed endochondral bone formation. Proc. Natl. Acad. Sci. USA 1996, 93:10240-10245.
44. Westendorf J.J., Zaidi S.K., Cascino J.E., Kahler R., van Wijnen A.J., Lian J.B., Yoshida M., Stein G.S., Li X. Runx2 (Cbfa1, AML-3) interacts with histone deacetylase 6 and represses the p21(CIP1/WAF1) promoter. Mol. Cell. Biol. 2002, 22:7982-7992.
45. Wu M., Hesse E., Morvan F., Zhang J.P., Correa D., Rowe G.C., Kiviranta R., Neff L., Philbrick W.M., Horne W.C., et al. Zfp521 antagonizes Runx2, delays osteoblast differentiation in vitro, and promotes bone formation in vivo. Bone 2009, 44:528-536.
46. Yamanaka Y., Tanaka H., Koike M., Nishimura R., Seino Y. PTHrP rescues ATDC5 cells from apoptosis induced by FGF receptor 3 mutation. J. Bone Miner. Res. 2003, 18:1395-1403.
47. Yamasaki N., Miyazaki K., Nagamachi A., Koller R., Oda H., Miyazaki M., Sasaki T., Honda Z.I., Wolff L., Inaba T., et al. Identification of Zfp521/ZNF521 as a cooperative gene for E2A-HLF to develop acute B-lineage leukemia. Oncogene 2010, 29:1963-1975.
48. Zheng Q., Zhou G., Morello R., Chen Y., Garcia-Rojas X., Lee B. Type X collagen gene regulation by Runx2 contributes directly to its hypertrophic chondrocyte-specific expression in vivo. J. Cell Biol. 2003, 162:833-842.