P53 down regulates PDGF-induced formation of circular dorsal ruffles in rat aortic smooth muscle cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Payne, Laura J ^a   Eves, Robert L ^a   Jia, Lilly ^a   Mak, Alan S ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; LIPID; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE; PIFITHRIN ALPHA; PLATELET DERIVED GROWTH FACTOR; PROTEIN CDC42; PROTEIN P53; PROTEIN WAVE1; PROTEIN WAVE2; RAC PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; AORTA MEDIA; ARTICLE; CELL IMMORTALIZATION; CELLULAR PARAMETERS; CIRCULAR DORSAL RUFFLE FORMATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RAT; SMOOTH MUSCLE FIBER; UPREGULATION; ANIMAL; AORTA; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; VASCULAR SMOOTH MUSCLE;

RATTUS;

ANIMALS; AORTA; CELL LINE; DOWN-REGULATION; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PLATELET-DERIVED GROWTH FACTOR; RATS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84907586348     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108257     Document Type: Article

References (51)

1. Louis SF, Zahradka P (2010) Vascular smooth muscle cell motility: From migration to invasion. Exp Clin Cardiol 15: e75-e85.
2. Bravo-Cordero JJ, Hodgson L, Condeelis J (2012) Directed cell invasion and migration during metastasis. Curr Opin Cell Biol 24: 277-283.
3. Linder S, Wiesner C, Himmel M (2011) Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 27: 185-211.
4. Buccione R, Orth JD, McNiven MA (2004) Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles. Nature Reviews Molecular Cell Biology 5: 647-657.
5. Itoh T, Hasegawa J (2013) Mechanistic insights into the regulation of circular dorsal ruffle formation. J Biochem 153: 21-29.
6. Hoon JL, Wong WK, Koh CG (2012) Functions and regulation of circular dorsal ruffles. Mol Cell Biol 32: 4246-4257.
7. Orth JD, McNiven MA (2006) Get off my back! Rapid receptor internalization through circular dorsal ruffles. Cancer Research 66: 11094-11096.
8. Gu Z, Noss EH, Hsu VW, Brenner MB (2011) Integrins traffic rapidly via circular dorsal ruffles and macropinocytosis during stimulated cell migration. J Cell Biol 193: 61-70.
9. Grotendorst GR, Chang T, Seppa HE, Kleinman HK, Martin GR (1982) Platelet-derived growth factor is a chemoattractant for vascular smooth muscle cells. J Cell Physiol 113: 261-266.
10. Ucuzian AA, Brewster LP, East AT, Pang Y, Gassman AA, et al. (2010) Characterization of the chemotactic and mitogenic response of SMCs to PDGFBB and FGF-2 in fibrin hydrogels. J Biomed Mater Res A 94: 988-996.
11. Bishop AL, Hall A (2000) Rho GTPases and their effector proteins. Biochem J 348 Pt 2: 241-255.
12. Ladwein M, Rottner K (2008) On the Rhod: The regulation of membrane protrusions by Rho-GTPases. Febs Letters 582: 2066-2074.
13. Hall A (2005) Rho GTPases and the control of cell behaviour. Biochem Soc Trans 33: 891-895.
14. Suetsugu S, Yamazaki D, Kurisu S, Takenawa T (2003) Differential roles of WAVE1 and WAVE2 in dorsal and peripheral ruffle formation for fibroblast cell migration. Dev Cell 5: 595-609.
15. Legg JA, Bompard G, Dawson J, Morris HL, Andrew N, et al. (2007) N-WASP involvement in dorsal ruffle formation in mouse embryonic fibroblasts. Molecular Biology of the Cell 18: 678-687.
16. Muller PA, Vousden KH, Norman JC (2011) p53 and its mutants in tumor cell migration and invasion. J Cell Biol 192: 209-218.
17. Gadea G, de Toledo M, Anguille C, Roux P (2007) Loss of p53 promotes RhoAROCK-dependent cell migration and invasion in 3D matrices. Journal of Cell Biology 178: 23-30.
18. Mak AS (2011) p53 regulation of podosome formation and cellular invasion in vascular smooth muscle cells. Cell Adh Migr 5: 144-149.
19. Mukhopadhyay UK, Mak AS (2009) p53: is the guardian of the genome also a suppressor of cell invasion? Cell Cycle 8: 2481.
20. Mak AS (2014) p53 in cell invasion, podosomes, and invadopodia. Cell Adh Migr 8. 27841 [pii].
21. Guo F, Gao Y, Wang L, Zheng Y (2003) p19Arf-p53 tumor suppressor pathway regulates cell motility by suppression of phosphoinositide 3-kinase and Rac1 GTPase activities. J Biol Chem 278: 14414-14419.
22. Guo F, Zheng Y (2004) Rho family GTPases cooperate with p53 deletion to promote primary mouse embryonic fibroblast cell invasion. Oncogene 23: 5577-5585.
23. Mukhopadhyay UK, Mooney P, Jia L, Eves R, Raptis L, et al. (2010) Doubles game: Src-Stat3 versus p53-PTEN in cellular migration and invasion. Mol Cell Biol 30: 4980-4995.
24. De Stanchina E, Querido E, Narita M, Davuluri RV, Pandolfi PP, et al. (2004) PML is a direct p53 target that modulates p53 effector functions. Mol Cell 13: 523-535.
25. Paddison PJ, Cleary M, Silva JM, Chang K, Sheth N, et al. (2004) Cloning of short hairpin RNAs for gene knockdown in mammalian cells. Nat Methods 1: 163-167.
26. Mukhopadhyay UK, Eves R, Jia L, Mooney P, Mak AS (2009) p53 suppresses Src-induced podosome and rosette formation and cellular invasiveness through the upregulation of caldesmon. Mol Cell Biol 29: 3088-3098.
27. Eves R, Webb BA, Zhou ST, Mak AS (2006) Caldesmon is an integral component of podosomes in smooth muscle cells. Journal of Cell Science 119: 1691-1702.
28. Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G (1992) Cultured aortic smooth muscle cells from newborn and adult rats show distinct cytoskeletal features. Differentiation 49: 175-185.
29. Webb BA, Eves R, Crawley SW, Zhou ST, Cote GP, et al. (2005) PAK1 induces podosome formation in A7r5 vascular smooth muscle cells in a PAK-interacting exchange factor-dependent manner. American Journal of Physiology-Cell Physiology 289: C898-C907.
30. Ashur-Fabian O, Avivi A, Trakhtenbrot L, Adamsky K, Cohen M, et al. (2004) Evolution of p53 in hypoxia-stressed Spalax mimics human tumor mutation. Proc Natl Acad Sci U S A 101: 12236-12241.
31. Spiering D, Hodgson L (2011) Dynamics of the Rho-family small GTPases in actin regulation and motility. Cell Adh Migr 5: 170-180. 14403 [pii].
32. Poon JS, Eves R, Mak AS (2010) Both lipid-and protein-phosphatase activities of PTEN contribute to the p53-PTEN anti-invasion pathway. Cell Cycle 9: 4450-4454.
33. Leslie NR, Yang X, Downes CP, Weijer CJ (2007) PtdIns(3,4,5)P(3)-dependent and-independent roles for PTEN in the control of cell migration. Curr Biol 17: 115-125.
34. Davidson L, Maccario H, Perera NM, Yang X, Spinelli L, et al. (2010) Suppression of cellular proliferation and invasion by the concerted lipid and protein phosphatase activities of PTEN. Oncogene 29: 687-697.
35. Furnari FB, Huang HJ, Cavenee WK (1998) The phosphoinositol phosphatase activity of PTEN mediates a serum-sensitive G1 growth arrest in glioma cells. Cancer Res 58: 5002-5008.
36. Eden S (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck.
37. Szczepanowska J (2009) Involvement of Rac/Cdc42/PAK pathway in cytoskeletal rearrangements. Acta Biochim Pol 56: 225-234. 20091831 [pii].
38. Zhao ZS, Manser E (2012) PAK family kinases: Physiological roles and regulation. Cell Logist 2: 59-68.
39. Sanematsu F, Nishikimi A, Watanabe M, Hongu T, Tanaka Y, et al. (2013) Phosphatidic acid-dependent recruitment and function of the Rac activator DOCK1 during dorsal ruffle formation. J Biol Chem 288: 8092-8100.
40. Peleg B, Disanza A, Scita G, Gov N (2011) Propagating cell-membrane waves driven by curved activators of actin polymerization. PLoS One 6: e18635.
41. Levkowitz G, Waterman H, Ettenberg SA, Katz M, Tsygankov AY, et al. (1999) Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1. Mol Cell 4: 1029-1040.
42. Joazeiro CA, Wing SS, Huang H, Leverson JD, Hunter T, et al. (1999) The tyrosine kinase negative regulator c-Cbl as a RING-type, E2-dependent ubiquitin-protein ligase. Science 286: 309-312. 7886 [pii].
43. Yokouchi M, Kondo T, Houghton A, Bartkiewicz M, Horne WC, et al. (1999) Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J Biol Chem 274: 31707-31712.
44. Weissmueller S, Manchado E, Saborowski M, Morris JP, Wagenblast E, et al. (2014) Mutant p53 Drives Pancreatic Cancer Metastasis through Cell-Autonomous PDGF Receptor beta Signaling. Cell 157: 382-394.
45. Yang W, Wetterskog D, Matsumoto Y, Funa K (2008) Kinetics of repression by modified p53 on the PDGF beta-receptor promoter. Int J Cancer 123: 2020-2030.
46. Quintavalle M, Elia L, Condorelli G, Courtneidge SA (2010) MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J Cell Biol 189: 13-22.
47. Elia L, Quintavalle M, Zhang J, Contu R, Cossu L, et al. (2009) The knockout of miR-143 and-145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 16: 1590-1598.
48. Destaing O, Planus E, Bouvard D, Oddou C, Badowski C, et al. (2010) beta1A integrin is a master regulator of invadosome organization and function. Mol Biol Cell 21: 4108-4119.
49. Shen B, Zhao X, OBrien KA, Stojanovic-Terpo A, Delaney MK, et al. (2013) A directional switch of integrin signalling and a new anti-thrombotic strategy. Nature 503: 131-135.
50. Beaty BT, Sharma VP, Bravo-Cordero JJ, Simpson MA, Eddy RJ, et al. (2013) beta1 integrin regulates Arg to promote invadopodial maturation and matrix degradation. Mol Biol Cell 24: 1661-11.
51. Janouskova H, Ray AM, Noulet F, Lelong-Rebel I, Choulier L, et al. (2013) Activation of p53 pathway by Nutlin-3a inhibits the expression of the therapeutic target alpha5 integrin in colon cancer cells. Cancer Lett 336: 307-318.