Epidermal growth factor receptor (EGFR) signaling regulates epiphyseal cartilage development through β-catenin-dependent and -independent pathways

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32229-32240

  Zhang, Xianrong ^a,b   Zhu, Ji ^a   Li, Yumei ^a,c   Lin, Tiao ^a,d   Siclari, Valerie A ^a   Chandra, Abhishek ^a   Candela, Elena M ^a   Koyama, Eiki ^a,e   Enomoto Iwamoto, Motomi ^a,e   Qin, Ling ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WUHAN UNIVERSITY   (China)

^c SHANGHAI UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^d Second Affiliated Hospital   (China)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL STUDIES; EPIDERMAL GROWTH FACTOR RECEPTORS; EPIPHYSEAL CARTILAGE; HYPERTROPHIC CHONDROCYTES; IMMUNOHISTOCHEMICAL ANALYSIS; MATRIX METALLOPROTEINASES; NUCLEAR TRANSLOCATIONS; OSSIFICATION CENTER;

CANALS; CARTILAGE; CELL DEATH; CHEMICAL ACTIVATION; HYDRAULIC STRUCTURES; MAMMALS; PLANTS (BOTANY);

BODY FLUIDS;

BETA CATENIN; COLLAGENASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; MATRIX METALLOPROTEINASE 14; OSTEOCLAST DIFFERENTIATION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CARTILAGE CELL; CHONDROGENESIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME INDUCTION; EPIPHYSEAL CARTILAGE; GROWTH REGULATION; IN VITRO STUDY; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCLAST; PERICHONDRIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

BETA-CATENIN; CARTILAGE BIOLOGY; CARTILAGE MATRIX DEGRADATION; EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR); EXTRACELLULAR MATRIX; MATRIX METALLOPROTEINASE (MMP); SECONDARY OSSIFICATION CENTER;

ANIMALS; BETA CATENIN; CHONDROCYTES; COLLAGENASES; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GROWTH PLATE; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; RANK LIGAND; RECEPTOR, EPIDERMAL GROWTH FACTOR; WNT SIGNALING PATHWAY;

EID: 84887501463     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.463554     Document Type: Article

References (50)

1. Kronenberg, H. M. (2003) Developmental regulation of the growth plate. Nature 423, 332-336
2. Mackie, E. J., Tatarczuch, L., and Mirams, M. (2011) The skeleton: a multifunctional complex organ: the growth plate chondrocyte and endochondral ossification. J. Endocrinol 211, 109-121
3. Blumer, M. J., Longato, S., and Fritsch, H. (2008) Structure, formation and role of cartilage canals in the developing bone. Ann. Anat. 190, 305-315
4. Lee, E. R., Lamplugh, L., Davoli, M. A., Beauchemin, A., Chan, K., Mort, J. S., and Leblond, C. P. (2001) Enzymes active in the areas undergoing cartilage resorption during the development of the secondary ossification center in the tibiae of rats ages 0-21 days: I. Two groups of proteinases cleave the core protein of aggrecan. Dev. Dyn. 222, 52-70
5. Alvarez, J., Costales, L., López-Muñiz, A., and López, J. M. (2005) Chondrocytes are released as viable cells during cartilage resorption associated with the formation of intrachondral canals in the rat tibial epiphysis. Cell Tissue Res. 320, 501-507
6. Sibilia, M., Kroismayr, R., Lichtenberger, B. M., Natarajan, A., Hecking, M., and Holcmann, M. (2007) The epidermal growth factor receptor: from development to tumorigenesis. Differentiation 75, 770-787
7. Miettinen, P. J., Berger, J. E., Meneses, J., Phung, Y., Pedersen, R. A., Werb, Z., and Derynck, R. (1995) Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376, 337-341
8. Sibilia, M., and Wagner, E. F. (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269, 234-238
9. Threadgill, D. W., Dlugosz, A. A., Hansen, L. A., Tennenbaum, T., Lichti, U., Yee, D., LaMantia, C., Mourton, T., Herrup, K., Harris, R. C., et al. (1995) Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230-234
10. Pines, G., Köstler, W. J., and Yarden, Y. (2010) Oncogenic mutant forms of EGFR: lessons in signal transduction and targets for cancer therapy. FEBS Lett. 584, 2699-2706
11. Schneider, M. R., Sibilia, M., and Erben, R. G. (2009) The EGFR network in bone biology and pathology. Trends Endocrinol Metab. 20, 517-524
12. Zhang, X., Siclari, V. A., Lan, S., Zhu, J., Koyama, E., Dupuis, H. L., Enomoto- Iwamoto, M., Beier, F., and Qin, L. (2011) The critical role of the epidermal growth factor receptor in endochondral ossification. J. Bone Miner Res. 26, 2622-2633
13. Lee, D., Cross, S. H., Strunk, K. E., Morgan, J. E., Bailey, C. L., Jackson, I. J., and Threadgill, D. W. (2004) Wa5 is a novel ENU-induced antimorphic allele of the epidermal growth factor receptor. Mamm Genome. 15, 525-536
14. Zhang, X., Tamasi, J., Lu, X., Zhu, J., Chen, H., Tian, X., Lee, T. C., Threadgill, D. W., Kream, B. E., Kang, Y., Partridge, N. C., and Qin, L. (2011) Epidermal growth factor receptor plays an anabolic role in bone metabolism in vivo. J. Bone Miner Res. 26, 1022-1034
15. Chun, J. S., Oh, H., Yang, S., and Park, M. (2008) Wnt signaling in cartilage development and degeneration. BMB Rep. 41, 485-494
16. Dao, D. Y., Jonason, J. H., Zhang, Y., Hsu, W., Chen, D., Hilton, M. J., and O'Keefe, R. J. (2012) Cartilage-specific β-catenin signaling regulates chondrocyte maturation, generation of ossification centers, and perichondrial bone formation during skeletal development. J. Bone Miner Res. 27, 1680-1694
17. Koyama, E., Young, B., Nagayama, M., Shibukawa, Y., Enomoto-Iwamoto, M., Iwamoto, M., Maeda, Y., Lanske, B., Song, B., Serra, R., and Pacifici, M. (2007) Conditional Kif3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134, 2159-2169
18. Yasuhara, R., Ohta, Y., Yuasa, T., Kondo, N., Hoang, T., Addya, S., Fortina, P., Pacifici, M., Iwamoto, M., and Enomoto-Iwamoto, M. (2011) Roles of β-catenin signaling in phenotypic expression and proliferation of articular cartilage superficial zone cells. Lab. Invest. 91, 1739-1752
19. Ueta, C., Iwamoto, M., Kanatani, N., Yoshida, C., Liu, Y., Enomoto- Iwamoto, M., Ohmori, T., Enomoto, H., Nakata, K., Takada, K., Kurisu, K., and Komori, T. (2001) Skeletal malformations caused by overexpression of Cbfa1 or its dominant negative form in chondrocytes. J. Cell Biol. 153, 87-100
20. Wuelling, M., and Vortkamp, A. (2011) Chondrocyte proliferation and differentiation. Endocr Dev. 21, 1-11
21. Krane, S. M., and Inada, M. (2008) Matrix metalloproteinases and bone. Bone. 43, 7-18
22. Edwards, J. R., and Mundy, G. R. (2011) Advances in osteoclast biology: old findings and new insights from mouse models. Nat. Rev. Rheumatol. 7, 235-243
23. Červenka, I., Wolf, J., Mašek, J., Krejci, P., Wilcox, W. R., Kozubík, A., Schulte, G., Gutkind, J. S., and Bryja, V. (2011) Mitogen-activated protein kinases promote WNT/β-catenin signaling via phosphorylation of LRP6. Mol. Cell. Biol. 31, 179-189
24. Bafico, A., Liu, G., Yaniv, A., Gazit, A., and Aaronson, S. A. (2001) Novel mechanism of Wnt signalling inhibition mediated by Dickkopf-1 interaction with LRP6/Arrow. Nat. Cell Biol. 3, 683-686
25. Fosang, A. J., Golub, S. B., East, C. J., and Rogerson, F. M. (2013) Abundant LacZ activity in the absence of Cre expression in the normal and inflamed synovium of adult Col2a1-Cre; ROSA26RLacZ reporter mice. Osteoarthritis Cartilage. 21, 401-404
26. Usmani, S. E., Pest, M. A., Kim, G., Ohora, S. N., Qin, L., and Beier, F. (2012) Transforming growth factor α controls the transition from hypertrophic cartilage to bone during endochondral bone growth. Bone. 51, 131-141
27. Renkiewicz, R., Qiu, L., Lesch, C., Sun, X., Devalaraja, R., Cody, T., Kaldjian, E., Welgus, H., and Baragi, V. (2003) Broad-spectrum matrix metalloproteinase inhibitor marimastat-induced musculoskeletal side effects in rats. Arthritis Rheum. 48, 1742-1749
28. Ortega, N., Behonick, D. J., and Werb, Z. (2004) Matrix remodeling during endochondral ossification. Trends Cell Biol. 14, 86-93
29. Inada, M., Wang, Y., Byrne, M. H., Rahman, M. U., Miyaura, C., López- Otín, C., and Krane, S. M. (2004) Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc. Natl. Acad. Sci. U.S.A. 101, 17192-17197
30. Stickens, D., Behonick, D. J., Ortega, N., Heyer, B., Hartenstein, B., Yu, Y., Fosang, A. J., Schorpp-Kistner, M., Angel, P., and Werb, Z. (2004) Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131, 5883-5895
31. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., and Werb, Z. (1998) MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422
32. Holmbeck, K., Bianco, P., Caterina, J., Yamada, S., Kromer, M., Kuznetsov, S. A., Mankani, M., Robey, P. G., Poole, A. R., Pidoux, I., Ward, J. M., and Birkedal-Hansen, H. (1999) MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92
33. Zhou, Z., Apte, S. S., Soininen, R., Cao, R., Baaklini, G. Y., Rauser, R. W., Wang, J., Cao, Y., and Tryggvason, K. (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc. Natl. Acad. Sci. U.S.A. 97, 4052-4057
34. Alvarez, J., Costales, L., Serra, R., Balbín, M., and López, J. M. (2005) Expression patterns of matrix metalloproteinases and vascular endothelial growth factor during epiphyseal ossification. J. Bone Miner Res. 20, 1011-1021
35. Ortega, N., Wang, K., Ferrara, N., Werb, Z., and Vu, T. H. (2010) Complementary interplay between matrix metalloproteinase-9, vascular endothelial growth factor and osteoclast function drives endochondral bone formation. Dis. Model. Mech. 3, 224-235
36. Blumer, M. J., Hausott, B., Schwarzer, C., Hayman, A. R., Stempel, J., and Fritsch, H. (2012) Role of tartrate-resistant acid phosphatase (TRAP) in long bone development. Mech. Dev. 129, 162-176
37. Xiong, J., Onal, M., Jilka, R. L., Weinstein, R. S., Manolagas, S. C., and O'Brien, C. A. (2011) Matrix-embedded cells control osteoclast formation. Nat. Med. 17, 1235-1241
38. Hu, T., and Li, C. (2010) Convergence between Wnt-β-catenin and EGFR signaling in cancer. Mol. Cancer 9, 236
39. Civenni, G., Holbro, T., and Hynes, N. E. (2003) Wnt1 and Wnt5a induce cyclin D1 expression through ErbB1 transactivation in HC11 mammary epithelial cells. EMBO Rep. 4, 166-171
40. Schlange, T., Matsuda, Y., Lienhard, S., Huber, A., and Hynes, N. E. (2007) Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonicalWNTpathway and EGFR transactivation. Breast Cancer Res. 9, R63
41. Ji, H., Wang, J., Nika, H., Hawke, D., Keezer, S., Ge, Q., Fang, B., Fang, X., Fang, D., Litchfield, D. W., Aldape, K., and Lu, Z. (2009) EGF-induced ERK activation promotes CK2-mediated disassociation of α-catenin from β-catenin and transactivation of β-catenin. Mol. Cell 36, 547-559
42. Krejci, P., Aklian, A., Kaucka, M., Sevcikova, E., Prochazkova, J., Masek, J. K., Mikolka, P., Pospisilova, T., Spoustova, T., Weis, M., Paznekas, W. A., Wolf, J. H., Gutkind, J. S., Wilcox, W. R., Kozubik, A., Jabs, E. W., Bryja, V., Salazar, L., Vesela, I., and Balek, L. (2012) Receptor tyrosine kinases activate canonical WNT/β-catenin signaling via MAP kinase/LRP6 pathway and direct β-catenin phosphorylation. PLoS One 7, e35826
43. Lee, C. H., Hung, H. W., Hung, P. H., and Shieh, Y. S. (2010) Epidermal growth factor receptor regulates β-catenin location, stability, and transcriptional activity in oral cancer. Mol. Cancer 9, 64
44. Lu, Z., Ghosh, S., Wang, Z., and Hunter, T. (2003) Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β-catenin, and enhanced tumor cell invasion. Cancer Cell 4, 499-515
45. Yang, W., Xia, Y., Ji, H., Zheng, Y., Liang, J., Huang, W., Gao, X., Aldape, K., and Lu, Z. (2011) Nuclear PKM2 regulates β-catenin transactivation upon EGFR activation. Nature 480, 118-122
46. Akiyama, H., Lyons, J. P., Mori-Akiyama, Y., Yang, X., Zhang, R., Zhang, Z., Deng, J. M., Taketo, M. M., Nakamura, T., Behringer, R. R., McCrea, P. D., and de Crombrugghe, B. (2004) Interactions between Sox9 and β-catenin control chondrocyte differentiation. Genes Dev. 18, 1072-1087
47. Day, T. F., Guo, X., Garrett-Beal, L., and Yang, Y. (2005) Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell 8, 739-750
48. Enomoto-Iwamoto, M., Kitagaki, J., Koyama, E., Tamamura, Y., Wu, C., Kanatani, N., Koike, T., Okada, H., Komori, T., Yoneda, T., Church, V., Francis-West, P. H., Kurisu, K., Nohno, T., Pacifici, M., and Iwamoto, M. (2002) The Wnt antagonist Frzb-1 regulates chondrocyte maturation and long bone development during limb skeletogenesis. Dev. Biol. 251, 142-156
49. Guo, X., Mak, K. K., Taketo, M. M., and Yang, Y. (2009) The Wnt/β- catenin pathway interacts differentially with PTHrP signaling to control chondrocyte hypertrophy and final maturation. PLoS One. 4, e6067
50. Tamamura, Y., Otani, T., Kanatani, N., Koyama, E., Kitagaki, J., Komori, T., Yamada, Y., Costantini, F., Wakisaka, S., Pacifici, M., Iwamoto, M., and Enomoto-Iwamoto, M. (2005) Developmental regulation of Wnt/β- catenin signals is required for growth plate assembly, cartilage integrity, and endochondral ossification. J. Biol. Chem. 280, 19185-19195