Syndecan-4 cytoplasmic domain regulation of turkey satellite cell focal adhesions and apoptosis

Molecular Biology Reports

Volumn 39, Issue 8, 2012, Pages 8251-8264

  Song, Yan ^a   McFarland, Douglas C ^b   Velleman, Sandra G ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b SOUTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Focal adhesion; Muscle; Satellite cell; Syndecan 4 cytoplasmic domain

Indexed keywords

BETA1 INTEGRIN; FOCAL ADHESION KINASE; GLYCOSAMINOGLYCAN; LYSYLLYSYLPROLYLISOLEUCYLTYROSYLLYSYLLYSINE; PAXILLIN; POLYPEPTIDE; SERINE; SYNDECAN 4; TYROSINE; UNCLASSIFIED DRUG; VINCULIN;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; FOCAL ADHESION; MALE; MOLECULAR CLONING; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SATELLITE CELL; TURKEY (BIRD); WILD TYPE; ANIMAL; CELL CULTURE; CHEMISTRY; GENETICS; METABOLISM; MUTATION; PROTEIN TRANSPORT; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; APOPTOSIS; CELLS, CULTURED; FOCAL ADHESIONS; MALE; MUTATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; SATELLITE CELLS, SKELETAL MUSCLE; SYNDECAN-4; TURKEYS;

EID: 84868661657     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-012-1673-1     Document Type: Article

References (41)

1. Rapraeger AC (2001) Molecular interactions of syndecans during development. Semin Cell Dev Biol 12:107-116. doi: 10.1006/scdb.2000.0239
2. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777. doi: 10.1146/annurev.biochem.68.1.729
3. Carey DJ (1997) Syndecans: multifunctional cell-surface co-receptors. Biochem J 327:1-16
4. Elenius K, Jalkanen M (1994) Function of the syndecans-a family of cell surface proteoglycans. J Cell Sci 107:2975-2982
5. Cornelison DD, Filla MS, Stanley HM, Rapraeger AC, Olwin BB (2001) Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev Biol 239:79-94. doi: 10.1006/dbio.2001.0416
6. Liu C, McFarland DC, Nestor KE, Velleman SG (2006) Differential expression of membrane-associated heparan sulfate proteoglycans in the skeletal muscle of turkeys with different growth rates. Poult Sci 85:422-428
7. Tanaka KK, Hall JK, Troy AA, Cornelison DD, Majka SM, Olwin BB (2009) Syndecan-4-expressing muscle progenitor cells in the SP engraft as satellite cells during muscle regeneration. Cell Stem Cell 4:217-225. doi: 10.1016/j.stem.2009.01.016
8. Sporer KR, Chiang W, Tempelman RJ, Ernst CW, Reed KM, Velleman SG, Strasburg GM (2011) Characterization of a 6 K oligonucleotide turkey skeletal muscle microarray. Anim Genet 42:75-82. doi: 10.1111/j.1365-2052.2010.02085.x
9. Echtermeyer F, Baciu PC, Saoncella S, Ge Y, Goetinck PF (1999) Syndecan-4 core protein is sufficient for the assembly of focal adhesions and actin stress fibers. J Cell Sci 112:3433-3441
10. Echtermeyer F, Streit M, Wilcox-Adelman S, Saoncella S, Denhez F, Detmar M, Goetinck P (2001) Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 107:R9-R14. doi: 10.1172/JCI10559
11. Jeong J, Han I, Lim Y, Kim J, Park I, Woods A, Couchman JR, Oh ES (2001) Rat embryo fibroblasts require both the cell-binding and the heparin-binding domains of fibronectin for survival. Biochem J 356:531-537
12. Burridge K, Chrzanowska-Wodnicka M (1996) Focal adhesions, contractility, and signaling. Annu Rev Cell Dev Biol 12:463-518. doi: 10.1146/annurev.cellbio. 12.1.463
13. Clark EA, Brugge JS (1995) Integrins and signal transduction pathways: the road taken. Science 268:233-239. doi: 10.1126/science.7716514
14. Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11-25. doi: 10.1016/0092-8674(92)90115-S
15. Woods A, Couchman JR, Johansson S, Hook M (1986) Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J 5:665-670
16. Saoncella S, Echtermeyer F, Denhez F, Nowlen JK, Mosher DF, Robinson SD, Hynes RO, Goetinck PF (1999) Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc Natl Acad Sci USA 96:2805-2810. doi: 10.1073/pnas.96.6.2805
17. Lyon M, Rushton G, Askari JA, Humphries MJ, Gallagher JT (2000) Elucidation of the structural features of heparan sulfate important for interaction with the Hep-2 domain of fibronectin. J Biol Chem 275:4599-4606. doi: 10.1074/jbc.275.7.4599
18. Woods A, Longley RL, Tumova S, Couchman JR (2000) Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374:66-72. doi: 10.1006/abbi.1999.1607
19. Longley RL, Woods A, Fleetwood A, Cowling GJ, Gallagher JT, Couchman JR (1999) Control of morphology, cytoskeleton and migration by syndecan-4. J Cell Sci 112:3421-3431
20. Oh ES, Woods A, Lim ST, Theibert AW, Couchman JR (1998) Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J Biol Chem 273:10624-10629. doi: 10.1074/jbc.273.17.10624
21. Horowitz A, Murakami M, Gao Y, Simons M (1999) Phosphatidylinositol-4,5- bisphosphate mediates the interaction of syndecan-4 with protein kinase C. Biochemistry 38:15871-15877. doi: 10.1021/bi991363i
22. Couchman JR, Vogt S, Lim ST, Lim Y, Oh ES, Prestwich GD, Theibert A, Lee W, Woods A (2002) Regulation of inositol phospholipid binding and signaling through syndecan-4. J Biol Chem 277:49296-49303. doi: 10.1074/jbc.M209679200
23. Oh ES, Woods A, Couchman JR (1997) Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J Biol Chem 272:8133-8136. doi: 10.1074/jbc.272.13.8133
24. Horowitz A, Simons M (1998) Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase C alpha. J Biol Chem 273:25548-25551. doi: 10.1074/jbc.273.40.25548
25. Sun XG, Rotenberg SA (1999) Overexpression of protein kinase C alpha in MCF-10A human breast cells engenders dramatic alterations in morphology, proliferation, and motility. Cell Growth Differ 10:343-352
26. Murakami M, Horowitz A, Tang S, Ware JA, Simons M (2002) Protein kinase C (PKC) delta regulates PKC alpha activity in a syndecan-4-dependent manner. J Biol Chem 277:20367-20371. doi: 10.1074/jbc.M202501200
27. Song Y, McFarland DC, Velleman SG (2012) Fibroblast growth factor 2 and protein kinase C alpha are involved in syndecan-4 cytoplasmic domain modulation of turkey myogenic satellite cell proliferation. Comp Biochem Physiol A 161:44-52. doi: 10.1016/j.cbpa.2011.09.001
28. Song Y, McFarland DC, Velleman SG (2011) Role of syndecan-4 side chains in turkey satellite cell growth and development. Dev Growth Differ 53:97-109. doi: 10.1111/j.1440-169X.2010.01230.x
29. Song Y, McFarland DC, Velleman SG (2012) Critical amino acids in syndecan-4 cytoplasmic domain modulation of turkey satellite cell growth and development. Comp Biochem Physiol A 161:271-278. doi: 10.1016/j.cbpa.2011.11.007
30. Velleman SG, Liu X, Nestor KE, McFarland DC (2000) Heterogeneity in growth and differentiation characteristics in male and female satellite cells isolated from turkey lines with different growth rates. Comp Biochem Physiol A 125:503-509. doi: 10.1016/S1095-6433(00)00178-1
31. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
32. Laemmli UK (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature (Lond) 237:680-685. doi: 10.1038/227680a0
33. LeBaron RG, Esko JD, Woods A, Johansson S, Hook M (1988) Adhesion of glycosaminoglycan-deficient Chinese hamster ovary cell mutants to fibronectin substrata. J Cell Biol 106:945-952
34. Lim ST, Longley RL, Couchman JR, Woods A (2003) Direct binding of syndecan-4 cytoplasmic domain to the catalytic domain of protein kinase C alpha (PKC alpha) increases focal adhesion localization of PKC alpha. J Biol Chem 278:13795-13802. doi: 10.1074/jbc.M208300200
35. Keum E, Kim Y, Kim J, Kwon S, Lim Y, Han I, Oh ES (2004) Syndecan-4 regulates localization, activity and stability of protein kinase C-alpha. Biochem J 378:1007-1014. doi: 10.1042/BJ20031734
36. Guan JL, Trevithick JE, Hynes RO (1991) Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul 2:951-964
37. Kornberg L, Earp HS, Parsons JT, Schaller M, Juliano RL (1992) Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J Biol Chem 267:23439-23442
38. Horowitz A, Simons M (1998) Regulation of syndecan-4 phosphorylation in vivo. J Biol Chem 273:10914-10918. doi: 10.1074/jbc.273.18.10914
39. Mould AP, Humphries MJ (2004) Regulation of integrin function through conformational complexity: Not simply a knee-jerk reaction? Curr Opin Cell Biol 16:544-551
40. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285:1028-1033. doi: 10.1126/science.285.5430.1028
41. Wilcox-Adelman SA, Denhez F, Goetinck PF (2002) Syndecan-4 modulates focal adhesion kinase phosphorylation. J Biol Chem 277:32970-32977. doi: 10.1074/jbc.M201283200