Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse

Journal of Cell Biology

Volumn 193, Issue 5, 2011, Pages 935-951

  Wilson, Deanna G ^a   Phamluong, Khanhky ^a   Li, Li ^a   Sun, Mei ^a   Cao, Tim C ^a   Liu, Peter S ^a   Modrusan, Zora ^a   Sandoval, Wendy N ^a   Rangell, Linda ^a   Carano, Richard A D ^a   Peterson, Andrew S ^a   Solloway, Mark J ^a  

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 3; COLLAGEN TYPE 4; COLLAGEN TYPE 7; COLLAGEN TYPE 9; MELANOMA INHIBITORY ACTIVITY MEMBER 3; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CARTILAGE CELL; CELL MATURATION; COLLAGEN DEFECT; CONTROLLED STUDY; DWARFISM; EMBRYO; ENDOPLASMIC RETICULUM; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FIBROBLAST; MOUSE; NEWBORN DISEASE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SECRETION;

ANIMALS; ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELLS, CULTURED; COLLAGEN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

MUS;

EID: 79959414324     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201007162     Document Type: Article

References (53)

1. Adiguzel, E., P.J. Ahmad, C. Franco, and M.P. Bendeck. 2009. Collagens in the progression and complications of atherosclerosis. Vasc. Med. 14:73-89.
2. Arndt, S., and A.K. Bosserhoff. 2006. TANGO is a tumor suppressor of malignant melanoma. Int. J. Cancer. 119:2812-2820.
3. Arndt, S., and A.K. Bosserhoff. 2007. Reduced expression of TANGO in colon and hepatocellular carcinomas. Oncol. Rep. 18:885-891.
4. Baldi, P., and A.D. Long. 2001. A Bayesian framework for the analysis of microarray expression data: regularized t -test and statistical inferences of gene changes. Bioinformatics. 17:509-519.
5. Bard, F., L. Casano, A. Mallabiabarrena, E. Wallace, K. Saito, H. Kitayama, G. Guizzunti, Y. Hu, F. Wendler, R. Dasgupta, et al. 2006. Functional genomics reveals genes involved in protein secretion and Golgi organization. Nature. 439:604-607.
6. Barlowe, C., L. Orci, T. Yeung, M. Hosobuchi, S. Hamamoto, N. Salama, M.F. Rexach, M. Ravazzola, M. Amherdt, and R. Schekman. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell. 77:895-907.
7. Bosserhoff, A.K., R. Stoll, J.P. Sleeman, F. Bataille, R. Buettner, and T.A. Holak. 2003. Active detachment involves inhibition of cell-matrix contacts of malignant melanoma cells by secretion of melanoma inhibitory activity. Lab. Invest. 83:1583-1594.
8. Boyadjiev, S.A., J.C. Fromme, J. Ben, S.S. Chong, C. Nauta, D.J. Hur, G. Zhang, S. Hamamoto, R. Schekman, M. Ravazzola, et al. 2006. Craniolenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking. Nat. Genet. 38:1192-1197.
9. Cohen-Salmon, M., D. Frenz, W. Liu, E. Verpy, S. Voegeling, and C. Petit. 2000. Fdp, a new fibrocyte-derived protein related to MIA/CD-RAP, has an in vitro effect on the early differentiation of the inner ear mesenchyme. J. Biol. Chem. 275:40036-40041.
10. Dombrowski, K.E., and D.J. Prockop. 1988. Cleavage of type I and type II procollagens by type I/II procollagen N-proteinase. Correlation of kinetic constants with the predicted conformations of procollagen substrates. J. Biol. Chem. 263:16545-16552.
11. Eyre, D.R. 2004. Collagens and cartilage matrix homeostasis. Clin. Orthop. Relat. Res. 427(Suppl.):S118-S122.
12. Fromme, J.C., and R. Schekman. 2005. COPII-coated vesicles: flexible enough for large cargo? Curr. Opin. Cell Biol. 17:345-352.
13. Fromme, J.C., M. Ravazzola, S. Hamamoto, M. Al-Balwi, W. Eyaid, S.A. Boyadjiev, P. Cosson, R. Schekman, and L. Orci. 2007. The genetic basis of a craniofacial disease provides insight into COPII coat assembly. Dev. Cell. 13:623-634.
14. Hecht, J.T., D. Montufar-Solis, G. Decker, J. Lawler, K. Daniels, and P.J. Duke. 1998. Retention of cartilage oligomeric matrix protein (COMP) and cell death in redifferentiated pseudoachondroplasia chondrocytes. Matrix Biol. 17:625-633.
15. Holden, P., R.S. Meadows, K.L. Chapman, M.E. Grant, K.E. Kadler, and M.D. Briggs. 2001. Cartilage oligomeric matrix protein interacts with type IX collagen, and disruptions to these interactions identify a pathogenetic mechanism in a bone dysplasia family. J. Biol. Chem. 276:6046-6055.
16. Ishida, Y., H. Kubota, A. Yamamoto, A. Kitamura, H.P. Bächinger, and K. Nagata. 2006. Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol. Biol. Cell. 17:2346-2355.
17. Kathiresan, S., B.F. Voight, S. Purcell, K. Musunuru, D. Ardissino, P.M. Mannucci, S. Anand, J.C. Engert, N.J. Samani, H. Schunkert, et al; Myocardial Infarction Genetics Consortium; Wellcome Trust Case Control Consortium. 2009. Genome-wide association of early-onset myocardial infarction with single nucleotide polymorphisms and copy number variants. Nat. Genet. 41:334-341. (published erratum appears in Nat. Genet. 2009. 41:762)
18. Kim, R.Y., E.J. Robertson, and M.J. Solloway. 2001. Bmp6 and Bmp7 are required for cushion formation and septation in the developing mouse heart. Dev. Biol. 235:449-466.
19. Kondo, S., A. Saito, S. Hino, T. Murakami, M. Ogata, S. Kanemoto, S. Nara, A. Yamashita, K. Yoshinaga, H. Hara, and K. Imaizumi. 2007. BBF2H7, a novel transmembrane bZIP transcription factor, is a new type of endoplasmic reticulum stress transducer. Mol. Cell. Biol. 27:1716-1729.
20. Kronenberg, H.M. 2003. Developmental regulation of the growth plate. Nature. 423:332-336.
21. Lamandé, S.R., and J.F. Bateman. 1999. Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones. Semin. Cell Dev. Biol. 10:455-464.
22. Lang, M.R., L.A. Lapierre, M. Frotscher, J.R. Goldenring, and E.W. Knapik. 2006. Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation. Nat. Genet. 38:1198-1203.
23. Li, S.W., A.L. Sieron, A. Fertala, Y. Hojima, W.V. Arnold, and D.J. Prockop. 1996. The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenic protein-1. Proc. Natl. Acad. Sci. USA. 93:5127-5130.
24. Long, F., X.M. Zhang, S. Karp, Y. Yang, and A.P. McMahon. 2001. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development. 128:5099-5108.
25. Lougheed, J.C., J.M. Holton, T. Alber, J.F. Bazan, and T.M. Handel. 2001. Structure of melanoma inhibitory activity protein, a member of a recently identified family of secreted proteins. Proc. Natl. Acad. Sci. USA. 98:5515-5520.
26. Ma, Y., and L.M. Hendershot. 2004. ER chaperone functions during normal and stress conditions. J. Chem. Neuroanat. 28:51-65.
27. Mancias, J.D., and J. Goldberg. 2008. Structural basis of cargo membrane protein discrimination by the human COPII coat machinery. EMBO J. 27:2918-2928.
28. Moser, M., A.K. Bosserhoff, E.B. Hunziker, L. Sandell, R. Fässler, and R. Buettner. 2002. Ultrastructural cartilage abnormalities in MIA/CDRAP-deficient mice. Mol. Cell. Biol. 22:1438-1445.
29. Mungrue, I.N., J. Pagnon, O. Kohannim, P.S. Gargalovic, and A.J. Lusis. 2009. CHAC1/MGC4504 is a novel proapoptotic component of the unfolded protein response, downstream of the ATF4-ATF3-CHOP cascade. J. Immunol. 182:466-476.
30. Nagai, N., M. Hosokawa, S. Itohara, E. Adachi, T. Matsushita, N. Hosokawa, and K. Nagata. 2000. Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J. Cell Biol. 150:1499-1506.
31. Ohisa, S., K. Inohaya, Y. Takano, and A. Kudo. 2010. sec24d encoding a component of COPII is essential for vertebra formation, revealed by the analysis of the medaka mutant, vbi. Dev. Biol. 342:85-95.
32. Ohoka, N., S. Yoshii, T. Hattori, K. Onozaki, and H. Hayashi. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 24:1243-1255.
33. Robertson, N.G., S. Heller, J.S. Lin, B.L. Resendes, S. Weremowicz, C.S. Denis, A.M. Bell, A.J. Hudspeth, and C.C. Morton. 2000. A novel conserved cochlear gene, OTOR: identification, expression analysis, and chromosomal mapping. Genomics. 66:242-248.
34. Saito, A., S. Hino, T. Murakami, S. Kanemoto, S. Kondo, M. Saitoh, R. Nishimura, T. Yoneda, T. Furuichi, S. Ikegawa, et al. 2009a. Regulation of endoplasmic reticulum stress response by a BBF2H7-mediated Sec23a pathway is essential for chondrogenesis. Nat. Cell Biol. 11:1197-1204.
35. Saito, K., M. Chen, F. Bard, S. Chen, H. Zhou, D. Woodley, R. Polischuk, R. Schekman, and V. Malhotra. 2009b. TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites. Cell. 136:891-902.
36. Samani, N.J., J. Erdmann, A.S. Hall, C. Hengstenberg, M. Mangino, B. Mayer, R.J. Dixon, T. Meitinger, P. Braund, H.E. Wichmann, et al; WTCCC and the Cardiogenics Consortium. 2007. Genomewide association analysis of coronary artery disease. N. Engl. J. Med. 357:443-453.
37. Sarmah, S., A. Barrallo-Gimeno, D.B. Melville, J. Topczewski, L. Solnica-Krezel, and E.W. Knapik. 2010. Sec24D-dependent transport of extracellular matrix proteins is required for zebrafish skeletal morphogenesis. PLoS ONE. 5:e10367.
38. Schoenhagen, P., E.M. Tuzcu, and S.G. Ellis. 2002. Plaque vulnerability, plaque rupture, and acute coronary syndromes: (multi)-focal manifestation of a systemic disease process. Circulation. 106:760-762.
39. Smith, E.B. 1965. The influence of age and atherosclerosis on the chemistry of aortic intima.2. Collagen and mucopolysaccharides. J. Atheroscler. Res. 5:241-248.
40. Solloway, M.J., A.T. Dudley, E.K. Bikoff, K.M. Lyons, B.L. Hogan, and E.J. Robertson. 1998. Mice lacking Bmp6 function. Dev. Genet. 22:321-339.
41. Stephens, D.J., and R. Pepperkok. 2002. Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport in mammalian cells. J. Cell Sci. 115:1149-1160.
42. St-Jacques, B., M. Hammerschmidt, and A.P. McMahon. 1999. Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev. 13:2072-2086.
43. Storey, J.D., and R. Tibshirani. 2003. Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol. Biol. 224:149-157.
44. Subramanian, A., P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA. 102:15545-15550.
45. Townley, A.K., Y. Feng, K. Schmidt, D.A. Carter, R. Porter, P. Verkade, and D.J. Stephens. 2008. Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development. J. Cell Sci. 121:3025-3034.
46. Vertel, B.M., A. Velasco, S. LaFrance, L. Walters, and K. Kaczman-Daniel. 1989. Precursors of chondroitin sulfate proteoglycan are segregated within a subcompartment of the chondrocyte endoplasmic reticulum. J. Cell Biol. 109:1827-1836.
47. Vogel, B.E., R.R. Minor, M. Freund, and D.J. Prockop. 1987. A point mutation in a type I procollagen gene converts glycine 748 of the alpha 1 chain to cysteine and destabilizes the triple helix in a lethal variant of osteogenesis imperfecta. J. Biol. Chem. 262:14737-14744.
48. Vogel, B.E., R. Doelz, K.E. Kadler, Y. Hojima, J. Engel, and D.J. Prockop. 1988. A substitution of cysteine for glycine 748 of the alpha 1 chain produces a kink at this site in the procollagen I molecule and an altered N-proteinase cleavage site over 225 nm away. J. Biol. Chem. 263:19249-19255.
49. Vu, T.H., J.M. Shipley, G. Bergers, J.E. Berger, J.A. Helms, D. Hanahan, S.D. Shapiro, R.M. Senior, and Z. Werb. 1998. MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell. 93:411-422.
50. Wendeler, M.W., J.P. Paccaud, and H.P. Hauri. 2007. Role of Sec24 isoforms in selective export of membrane proteins from the endoplasmic reticulum. EMBO Rep. 8:258-264.
51. Yang, X., K. Matsuda, P. Bialek, S. Jacquot, H.C. Masuoka, T. Schinke, L. Li, S. Brancorsini, P. Sassone-Corsi, T.M. Townes, et al. 2004. ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry Syndrome. Cell. 117:387-398.
52. Zaucke, F., and S. Grässel. 2009. Genetic mouse models for the functional analysis of the perifibrillar components collagen IX, COMP and matrilin-3: Implications for growth cartilage differentiation and endochondral ossification. Histol. Histopathol. 24:1067-1079.
53. Zhang, P., B. McGrath, S. Li, A. Frank, F. Zambito, J. Reinert, M. Gannon, K. Ma, K. McNaughton, and D.R. Cavener. 2002. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22:3864-3874.