Regulatory domain selectivity in the cell-type specific PKN-dependence of cell migration

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Lachmann, Sylvie ^a   Jevons, Amy ^a   de Rycker, Manu ^a   Casamassima, Adele ^a   Radtke, Simone ^a   Collazos, Alejandra ^a   Parker, Peter J ^a,b  

^a London Research Institute   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; PROTEIN KINASE; PROTEIN KINASE 1; PROTEIN KINASE 2; PROTEIN KINASE 3; UNCLASSIFIED DRUG; ISOENZYME; PROTEIN KINASE C; PROTEIN KINASE N;

ARTICLE; BLADDER TUMOR; CELL INVASION; CELL MIGRATION; CHIMERA; CONTROLLED STUDY; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR CELL; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; ANTIBODY SPECIFICITY; CANCER INVASION; CATTLE; CELL MOTION; CHEMISTRY; ENZYMOLOGY; GENE SILENCING; GENETICS; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE; WOUND HEALING;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CELL LINE, TUMOR; CELL MOVEMENT; GENE KNOCKDOWN TECHNIQUES; HUMANS; ISOENZYMES; MOLECULAR SEQUENCE DATA; NEOPLASM INVASIVENESS; ORGAN SPECIFICITY; PROTEIN KINASE C; PROTEIN STRUCTURE, TERTIARY; URINARY BLADDER NEOPLASMS; WOUND HEALING;

EID: 79959923151     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021732     Document Type: Article

References (49)

1. Vega FM, Ridley AJ, (2008) Rho GTPases in cancer cell biology. FEBS Lett 582: 2093-2101.
2. Raftopoulou M, Hall A, (2004) Cell migration: Rho GTPases lead the way. Dev Biol 265: 23-32.
3. Bustelo XR, Sauzeau V, Berenjeno IM, (2007) GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays 29: 356-370.
4. Vincent S, Settleman J, (1997) The PRK2 Kinase is a potential effector target of both Rho and Rac GTPases and regulates actin cytoskeletal organisation. Mol Cell Biol 17: 2247-2256.
5. Flynn P, Mellor H, Palmer R, Panayotou G, Parker PJ, (1998) Multiple interactions of PRK1 with RhoA. Functional assignment of the HR1 repeat motif. J Biol Chem 273: 2698-2705.
6. Mellor H, Flynn P, Nobes CD, Hall A, Parker PJ, (1998) PRK1 is targetted to endosomes by the small GTPase, RhoB. J Biol Chem 273: 4811-4814.
7. Maesaki R, Ihara K, Shimizu T, Kuroda S, Kaibuchi K, et al. (1999) The structural basis of Rho effector recognition revealed by the crystal structure of human RhoA complexed with the effector domain of PKN/PRK1. Mol Cell 4: 793-803.
8. Lim WG, Tan BJ, Zhu Y, Zhou S, Armstrong JS, et al. (2006) The very C-terminus of PRK1/PKN is essential for its activation by RhoA and downstream signaling. Cell Signal 18: 1473-1481.
9. Lim MA, Yang L, Zheng Y, Wu H, Dong LQ, et al. (2004) Roles of PDK-1 and PKN in regulating cell migration and cortical actin formation of PTEN-knockout cells. Oncogene 23: 9348-9358.
10. Palmer RH, Dekker LV, Woscholski R, Le Good JA, Gigg R, et al. (1995) Activation of PRK1 by phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 3,4,5-trisphosphate. A comparison with protein kinase C isotypes. J Biol Chem 270: 22412-22416.
11. Mukai H, Kitagawa M, Shibata H, Takanaga H, Mori K, et al. (1994) Activation of pkn, a novel 120-kda protein-kinase with leucine zipper-like sequences, by unsaturated fatty-acids and by limited proteolysis. Biochem Biophys Res Commun 204: 348-356.
12. Kitagawa M, Mukai H, Shibata H, Ono Y, (1995) Purification and characterization of a fatty acid-activated protein kinase (PKN) from rat testis. Biochem J 310: 657-664.
13. Lim WG, Zhu Y, Wang CH, Tan BJ, Armstrong JS, et al. (2005) The last five amino acid residues at the C-terminus of PRK1/PKN is essential for full lipid responsiveness. Cell Signal 17: 1084-1097.
14. Oishi K, Mukai H, Shibata H, Takahashi M, Ona Y, (1999) Identification and characterization of PKNbeta, a novel isoform of protein kinase PKN: expression and arachidonic acid dependency are different from those of PKNalpha. Biochem Biophys Res Commun 261: 808-814.
15. Metzger E, Muller JM, Ferrari S, Buettner R, Schule R, (2003) A novel inducible transactivation domain in the androgen receptor: implications for PRK in prostate cancer. EMBO J 22: 270-280.
16. Metzger E, Yin N, Wissmann M, Kunowska N, Fischer K, et al. (2008) Phosphorylation of histone H3 at threonine 11 establishes a novel chromatin mark for transcriptional regulation. Nat Cell Biol 10: 53-60.
17. Bourguignon LY, Gilad E, Peyrollier K, Brightman A, Swanson RA, (2007) Hyaluronan-CD44 interaction stimulates Rac1 signaling and PKN gamma kinase activation leading to cytoskeleton function and cell migration in astrocytes. J Neurochem 101: 1002-1017.
18. Leenders F, Mopert K, Schmiedeknecht A, Santel A, Czauderna F, et al. (2004) PKN3 is required for malignant prostate cell growth downstream of activated PI 3-kinase. EMBO J 23: 3303-3313.
19. Gotoh Y, Oishi K, Shibata H, Yamagiwa A, Isagawa T, et al. (2004) Protein kinase PKN1 associates with TRAF2 and is involved in TRAF2-NF-kappaB signaling pathway. Biochem Biophys Res Commun 314: 688-694.
20. Quilliam LA, Lambert QT, Mickelson-Young LA, Westwick JK, Sparks AB, et al. (1996) Isolation of a NCK-associated kinase, PRK2, an SH3-binding protein and potential effector of Rho protein signaling. J Biol Chem 271: 28772-28776.
21. Shibata H, Oishi K, Yamagiwa A, Matsumoto M, Mukai H, et al. (2001) PKNbeta interacts with the SH3 domains of Graf and a novel Graf related protein, Graf2, which are GTPase activating proteins for Rho family. J Biochem 130 (Tokyo): 23-31.
22. Palmer RH, Ridden J, Parker PJ, (1995) Cloning and expression patterns of two members of a novel protein-kinase-C-related kinase family. Eur J Biochem 227: 344-351.
23. Dong LQ, Landa LR, Wick MJ, Zhu L, Mukai H, et al. (2000) Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc Natl Acad Sci U S A 97: 5089-5094.
24. Mukai H, Toshimori M, Shibata H, Takanaga H, Kitagawa M, et al. (1997) Interaction of PKN with alpha-actinin. J Biol Chem 272: 4740-4746.
25. Ammer AG, Weed SA, (2008) Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 65: 687-707.
26. Hamaguchi T, Ito M, Feng J, Seko T, Koyama M, et al. (2000) Phosphorylation of CPI-17, an inhibitor of myosin phosphatase, by protein kinase N. Biochem Biophys Res Commun 274: 825-830.
27. Matsuzawa K, Kosako H, Inagaki N, Shibata H, Mukai H, et al. (1997) Domain-specific phosphorylation of vimentin and glial fibrillary acidic protein by PKN. Biochem Biophys Res Commun 234: 621-625.
28. Mukai H, Toshimori M, Shibata H, Kitagawa M, Shimakawa M, et al. (1996) PKN associates and phosphorylates the head-rod domain of neurofilament protein. J Biol Chem 271: 9816-9822.
29. Kato T Jr, Gotoh Y, Hoffmann A, Ono Y, (2008) Negative regulation of constitutive NF-kappaB and JNK signaling by PKN1-mediated phosphorylation of TRAF1. Genes Cells 13: 509-520.
30. Takahashi M, Gotoh Y, Isagawa T, Nishimura T, Goyama E, et al. (2003) Regulation of a mitogen-activated protein kinase kinase kinase, MLTK by PKN. J Biochem (Tokyo) 133: 181-187.
31. Deaton RA, Su C, Valencia TG, Grant SR, (2005) Transforming growth factor-beta1-induced expression of smooth muscle marker genes involves activation of PKN and p38 MAPK. J Biol Chem 280: 31172-31181.
32. Turner N, Lambros MB, Horlings HM, Pearson A, Sharpe R, et al. (2010) Integrative molecular profiling of triple negative breast cancers identifies amplicon drivers and potential therapeutic targets. Oncogene 29: 2013-2023.
33. Friedl P, Brocker EB, (2000) The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci 57: 41-64.
34. Yu W, Liu J, Morrice NA, Wettenhall RE, (1997) Isolation and characterization of a structural homologue of human PRK2 from rat liver. Distinguishing substrate and lipid activator specificities. J Biol Chem 272: 10030-10034.
35. Owen D, Lowe PN, Nietlispach D, Brosnan CE, Chirgadze DY, et al. (2003) Molecular dissection of the interaction between the small G proteins Rac1 and RhoA and protein kinase C-related kinase 1 (PRK1). J Biol Chem 278: 50578-50587.
36. Blumenstein L, Ahmadian MR, (2004) Models of the cooperative mechanism for Rho effector recognition: implications for RhoA-mediated effector activation. J Biol Chem 279: 53419-53426.
37. Lim WG, Chen X, Liu JP, Tan BJ, Zhou S, et al. (2008) The C-terminus of PRK2/PKNgamma is required for optimal activation by RhoA in a GTP-dependent manner. Arch Biochem Biophys 479: 170-178.
38. Braverman LE, Quilliam LA, (1999) Identification of Grb4/Nckbeta, a src homology 2 and 3 domain-containing adapter protein having similar binding and biological properties to Nck. J Biol Chem 274: 5542-5549.
39. Lu Y, Settleman J, (1999) The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev 13: 1168-1180.
40. Wood W, Jacinto A, Grose R, Woolner S, Gale J, et al. (2002) Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4: 907-912.
41. Betson M, Settleman J, (2007) A rho-binding protein kinase C-like activity is required for the function of protein kinase N in Drosophila development. Genetics 176: 2201-2212.
42. Sahai E, Marshall CJ, (2003) Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5: 711-719.
43. Calautti E, Grossi M, Mammucari C, Aoyama Y, Pirro M, et al. (2002) Fyn tyrosine kinase is a downstream mediator of Rho/PRK2 function in keratinocyte cell-cell adhesion. J Cell Biol 156: 137-148.
44. Kim JH, Kim HW, Jeon H, Suh PG, Ryu SH, (2006) Phospholipase D1 regulates cell migration in a lipase activity-independent manner. J Biol Chem 281: 15747-15756.
45. Monami G, Gonzalez EM, Hellman M, Gomella LG, Baffa R, et al. (2006) Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res 66: 7103-7110.
46. Naumanen P, Lappalainen P, Hotulainen P, (2008) Mechanisms of actin stress fibre assembly. J Microsc 231: 446-454.
47. Marinissen MJ, Chiariello M, Gutkind JS, (2001) Regulation of gene expression by the small GTPase Rho through the ERK6 (p38 gamma) MAP kinase pathway. Genes Dev 15: 535-553.
48. Torbett NE, Casamassima A, Parker PJ, (2003) Hyperosmotic-induced protein kinase N 1 activation in a vesicular compartment is dependent upon Rac1 and 3-phosphoinositide-dependent kinase 1. J Biol Chem 278: 32344-32351.
49. 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.