P21-activated kinase signaling in breast cancer

Breast Cancer Research

Volumn 7, Issue 1, 2005, Pages 5-12

  Gururaj, Anupama E ^a   Rayala, Suresh K ^a   Kumar, Rakesh ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Breast cancer; Hormone independence; Mouse model; p21 activated kinase; Rho GTPase

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATE; CEP 1347; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GUANOSINE TRIPHOSPHATASE; KT D606; PHOSPHOTRANSFERASE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE INHIBITOR; PROTEIN P21; PROTEIN SERINE THREONINE KINASE; RHO FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CARCINOGENESIS; CELL CYCLE; CELL DIFFERENTIATION; CELL GROWTH; COLON TUMOR; CYTOSKELETON; DISEASE MODEL; DRUG TARGETING; GENE TARGETING; HEAD AND NECK TUMOR; HUMAN; NONHUMAN; OVARY TUMOR; PANCREAS TUMOR; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TISSUE CULTURE; TISSUE DISTRIBUTION;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; FEMALE; GTP PHOSPHOHYDROLASES; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 13444263561     PISSN: 14655411     EISSN: None     Source Type: Journal    
DOI: 10.1186/bcr961     Document Type: Review

References (80)

1. Etienne-Manneville S, Hall A: Rho GTPases in cell biology. Nature 2002, 420:629-635.
2. Bokoch GM: Biology of the p21-activated kinases. Annu Rev Biochem 2003, 72:743-781.
3. Bokoch GM: Regulation of cell function by Rho family GTPases. Immunol Res 2000, 21:139-148.
4. Kumar R, Vadlamudi RK: Emerging functions of p21-activated kinases in human cancer cells. J Cell Physiol 2002, 193: 33-144.
5. Jaffer ZM, Chernoff J: p21-activated kinases: three more join the Pak. Int J Biochem Cell Biol 2002, 34:713-717.
6. Manser E, Leung T, Salihuddin H, Zhao ZS, Lim L: A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 1994, 367:40-46.
7. Tang Y, Zhou H, Chen A, Pittman RN, Field J: The Akt proto-oncogene links Ras to Pak and cell survival signals. J Biol Chem 2000, 275:9106-9109.
8. Bagheri Y, Mandal M, Taludker AH, Wang RA, Vadlamudi RK, Kung HJ, Kumar R: Etk/Bmx tyrosine kinase activates Pak1 and regulates tumorigenicity of breast cancer cells. J Biol Chem 2001, 276: 9403-29409.
9. Brzeska H, Knaus UG, Wang ZY, Bokoch GM, Korn ED: p21-activated kinase has substrate specificity similar to Acanthamoeba myosin I heavy chain kinase and activates Acanthamoeba myosin I. Proc Natl Acad Sci USA 1997, 94: 1092-1095.
10. Adam L, Vadlamudi R, Kondapaka SB, Chernoff J, Mendelsohn J, Kumar R: Heregulin regulates cytoskeletal reorganization and cell migration through the p21-activated kinase-1 via phosphatidylinositol-3 kinase. J Biol Chem 1998, 273:28238-28246.
11. Tang Y, Chen Z, Ambrose D, Liu J, Gibbs JB, Chernoff J, Field J: Kinase-defective Pak1 mutants inhibit ras transformation of Rat-1 fibroblasts. Mol Cell Biol 1997, 17:4454-4464.
12. Tang Y, Yu J, Field J: Signals from the Ras, Rac, and Rho GTPases converge on the Pak protein kinase in Rat-1 fibroblasts. Mol Cell Biol 1999, 19:1881-1891.
13. He H, Hirokawa Y, Manser E, Lim L, Levitzki A, Maruta H: Signal therapy for RAS-induced cancers in combination of AG 879 and PP1, specific inhibitors for ErbB2 and Src family kinases, that block PAK activation. Cancer J 2001, 7:191-202.
14. Carter JH, Douglass LE, Deddens JA, Colligan BM, Bhatt TR, Pemberton JO, Konicek S, Hom J, Marshall M, Graff JR: Pak-1 expression increases with progression of colorectal carcinomas to metastasis. Clin Cancer Res 2004, 10:3448-3456.
15. Jung ID, Lee J, Lee KB, Park CG, Kim YK, Seo DW, Park D, Lee HW, Han JW, Lee HY: Activation of p21-activated kinas 1 is required for lysophosphatidic acid-induced focal adhesion kinas phosphorylation and cell motility in human melanoma A2058 cells. Eur J Biochem 2004, 271:1557-1565.
16. Yang Z, Bagheri-Yarmand R, Wang RA, Adam L, Papadimitrakopoulou VV, Clayman GL, El-Naggar A, Lotan R, Barnes CJ, Hong WK, Kumar R: The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 (Iressa) suppresses c-Src and Pak1 pathways and invasiveness of human cancer cells. Clin Cancer Res 2004, 10: 58-667.
17. Dadke D, Fryer BH, Golemis EA, Field J: Activation of p21-activated kinase 1-nuclear factor kappaB signaling by Kaposi's sarcoma-associated herpes virus G protein-coupled receptor during cellular transformation. Cancer Res 2003, 63:8837-8847.
18. Schraml P, Schwerdtfeger G, Burkhalter F, Raggi A, Schmidt D, Ruffalo T, King W, Wilber K, Mihatsch MJ, Moch H: Combined array comparative genomic hybridization and tissue microarray analysis suggest PAK1 at 11q13.5-q14 as a critical oncogene target in ovarian carcinoma. Am J Pathol 2003, 163:985-992.
19. Callow MG, Clairvoyant F, Zhu S, Schryver B, Whyte DB, Bischoff JR, Jallal B, Smeal T: Requirement for PAK4 in the anchorage-independent growth of human cancer cell lines. J Biol Chem 2002, 277:550-558.
20. Xiao GH, Beeser A, Chernoff J, Testa JR: p21-activated kinase links Rac/Cdc42 signaling to marlin. J Biol Chem 2002, 277: 883-886.
21. Kissil JL, Wilker EW, Johnson KC, Eckman MS, Yaffe MB, Jacks T: Merlin, the product of the Nf2 tumor suppressor gene, is an inhibitor of the p21-activated kinase, Pak1. Mol Cell 2003, 12: 841-849.
22. Huang Z, Traugh JA, Bishop JM. Negative control of the Myc protein by the stress-responsive kinase Pak2. Mol Cell Biol 2004, 24:1582-1594.
23. Wang RA, Vadlamudi RK, Bagheri-Yarmand R, Beuvink I, Hynes NE, Kumar R: Essential functions of p21-activated kinase 1 in morphogenesis and differentiation of mammary glands. J Cell Biol 2003, 161:583-592.
24. Zhong JL, Banerjee MD, Nikolic M: Pak1 and its T212 phosphorylated form accumulate in neurones and epithelial cells of the developing rodent. Dev Dyn 2003, 228:121-127.
25. Wang RA, Mazumdar A, Vadlamudi RK, Kumar R: P21-activated kinase-1 phosphorylates and transactivates estrogen receptor-alpha and promotes hyperplasia in mammary epithelium. EMBO J 2002, 21: 437-5447.
26. Leung K, Nagy A, Gonzalez-Gomez I, Groffen J, Heisterkamp N, Kaartinen V: Targeted expression of activated Rac3 in mammary epithelium leads to defective postlactational involution and benign mammary gland lesions. Cells Tissues Organs 2003, 175: 2-83.
27. Balasenthil S, Sahin AA, Barnes CJ, Wang RA, Pestell RG, Vadlamudi RK, Kumar R: p21-activated kinase-1 signaling mediates cyclin D1 expression in mammary epithelial and cancer cells. J Biol Chem 2004, 279:1422-1428.
28. Stofega MR, Sanders LC, Gardiner EM, Bokoch GM: Constitutive p21-activated kinase (PAK) activation in breast cancer cells as a result of mislocalization of PAK to focal adhesions. Mol Biol Cell 2004, 15:2965-2977.
29. Salh B, Marotta A, Wagey R, Sayed M, Pelech S: Dysregulation of phosphatidylinositol 3-kinase and downstream effectors in human breast cancer. Int J Cancer 2002, 98:148-154.
30. Vadlamudi RK, Adam L, Wang RA, Mandal M, Nguyen D, Sahin A, Chernoff J, Kumar R: Regulatable expression of p21-activated kinase-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells. J Biol Chem 2000, 275:36238-36244.
31. Carlsson J, Nordgren H, Sjostrom J, Wester K, Villman K, Bengtsson NO, Ostenstad B, Lundqvist H, Blomqvist C: HER2 expression in breast cancer primary tumours and corresponding metastases. Original data and literature review. Br J Cancer 2004, 90: 344-2348.
32. Mira JP, Benard V, Groffen J, Sanders LC, Knaus UG: Endogenous, hyperactive Rac3 controls proliferation of breast cancer cells by a p21-activated kinase-dependent pathway. Proc Natl Acad Sci USA 2000, 97:185-189.
33. Schnelzer A, Prechtel D, Knaus U, Dehne K, Gerhard M, Graeff H, Harbeck N, Schmitt M, Lengyel E: Rac1 in human breast cancer: overexpression, mutation analysis, and characterization of a new isoform, Rac1b. Oncogene 2000, 19:3013-3020.
34. Ahn SJ, Chung KW, Lee RA, Park IA, Lee SH, Park DE, Noh DY: Overexpression of betaPix-a in human breast cancer tissues. Cancer Lett 2003, 193:99-107.
35. Barnes CJ, Vadlamudi RK, Mishra SK, Jacobson RH, Li F, Kumar R: Functional inactivation of a transcriptional corepressor by a signaling kinase. Nat Struct Biol 2003, 10:622-628.
36. Howe AK, Juliano RL: Regulation of anchorage-dependent signal transduction by protein kinase A and p21-activated kinase. Nat Cell Biol 2000, 2:593-600.
37. O'Connor KL, Mercurio AM: Protein kinase A regulates Rac and is required for the growth factor-stimulated migration of carcinoma cells. J Biol Chem 2001, 276:47895-47900.
38. Vadlamudi RK, Bagheri-Yarmand R, Yang Z, Balasenthil S, Nguyen D, Sahin AA, den Hollander P, Kumar R: Dynein light chain 1, a p21-activated kinase 1-interacting substrate, promotes cancerous phenotypes. Cancer Cell 2004, 5:575-585.
39. Faure S, Vigneron S, Galas S, Brassac T, Delsert C, Morin N: Control of G2/M transition in Xenopus by a member of the p21-activated kinase (PAK) family: a link between protein kinase A and PAK signaling pathways? J Biol Chem 1999, 274:3573-3579.
40. Thiel D, Reeder M, Pfaff A, Coleman T, Sells M, Chernoff J: Cell cycle-regulated phosphorylation of p21-activated kinase 1. Curr Biol 2002, 12:1227-1232.
41. Banerjee M, Worth D, Prowse D, Nikolic M: Pak1 phosphorylation on t212 affects microtubules in cells undergoing mitosis. Curr Biol 2002, 12:1233-1239.
42. Li F, Adam L, Vadlamudi RK, Zhou H, Sen S, Chernoff J, Mandal M, Kumar R: p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells. EMBO Rep 2002, 3: 67-773.
43. Schurmann A, Mooney AF, Sanders LC, Sells MA, Wang HG, Reed JC, Bokoch GM: p21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol Cell Biol 2000, 20:453-461.
44. Gnesutta N, Minden A: Death receptor-induced activation of initiator caspase 8 is antagonized by serine/threonine kinase PAK4. Mol Cell Biol 2003, 23:7838-7848.
45. Mazumdar A, Kumar R: Estrogen regulation of Pak1 and FKHR pathways in breast cancer cells. FEBS Lett 2003, 535:6-10.
46. Deacon K, Mistry P, Chernoff J, Blank JL, Patel R: p38 Mitogen-activated protein kinase mediates cell death and p21-activated kinase mediates cell survival during chemotherapeutic drug-induced mitotic arrest. Mol Biol Cell 2003, 14:2071-2087.
47. Gururaj A, Barnes CJ, Vadlamudi RK, Kumar R: Phosphoglucomutase 1 regulation by p21-activated kinase 1. Oncogene 2004, 23:8118-8127.
48. Bagheri-Yarmand R, Vadlamudi RK, Wang R, Mendelsohn J, Kumar R: Vascular endothelial growth factor upregulation via p21-activated kinase-1 signaling regulates heregulin-b1-mediated angiogenesis. J Biol Chem 2000, 275:39451-39457.
49. Chau CH, Chen KY, Deng HT, Kim KJ, Hosoya K, Terasaki T, Shih HM, Ann DK: Coordinating Etk/Bmx activation and VEGF upregulation to promote cell survival and proliferation. Oncogene 2002, 21: 817-8829.
50. Kiosses WB, Hood J, Yang S, Gerritsen ME, Cheresh DA, Alderson N, Schwartz MA: A dominant-negative p65 PAK peptide inhibits angiogenesis. Circ Res 2002, 90:697-702.
51. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL: HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 2001, 21:3995-4004.
52. Deroanne C, Vouret-Craviari V, Wang B, Pouyssegur J: EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J Cell Sci 2003, 116: 1367-1376.
53. Bayless KJ, Davis GE: Microtubule depolymerization rapidly collapses capillary tube networks in vitro and angiogenic vessels in vivo through the small GTPase Rho. J Biol Chem 2004, 279: 1686-11695.
54. Bekri S, Adelaide J, Merscher S, Grosgeorge J, Caroli B, Perucca L, Kelley PM, Pebusque MJ, Theillet C, Birnbaum D, Gaudray P: Detailed map of a region commonly amplified at 11q13?q14 in human breast carcinoma. Cytogenet Cell Genet 1997, 79: 125-131.
55. Woo MS, Ohta Y, Rabinovitz I, Stossel TP, Blenis J: Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol Cell Biol 2004, 24: 025-3035.
56. Michalides R, Griekspoor A, Balkenende A, Verwoerd D, Janssen L, Jalink K, Floore A, Velds A, van't Veer L, Neefjes J: Tamoxifen resistance by a conformational arrest of the estrogen receptor alpha after PKA activation in breast cancer. Cancer Cell 2004, 5: 97-605.
57. Balasenthil S, Barnes CJ, Rayala SK, Kumar R: Estrogen receptor activation at serine 305 is sufficient to upregulate cyclin D1 in breast cancer cells. FEBS Lett 2004, 567:243-247.
58. 1 promoter. Cancer Res 2003, 63: 802-6808.
59. Lee SR, Ramos SM, Ko A, Masiello D, Swanson KD, Lu ML, Balk SP: AR and ER interaction with a p21-activated kinase (PAK6). Mol Endocrinol 2002, 16:85-99.
60. Nheu TV, He H, Hirokawa Y, Tamaki K, Florin L, Schmitz ML, Suzuki-Takahashi I, Jorissen RN, Burgess AW, Nishimura S, et al.: The K252a derivatives, inhibitors for the PAK/MLK kinase family selectively block the growth of RAS transformants. Cancer J 2002, 8:328-336.
61. Lei M, Lu W, Meng W, Parrini MC, Eck MJ, Mayer BJ, Harrison SC: Structure of PAK1 in an autoinhibited conformation reveals a multistage activation switch. Cell 2000, 102:387-397.
62. Edwards DC, Sanders LC, Bokoch GM, Gill GN: Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1999, 1:253-259.
63. Ramos E, Wysolmerski RB, Masaracchia RA: Myosin phosphorylation by human cdc42-dependent S6/H4 kinase/gammaPAK from placenta and lymphoid cells. Recept Signal Transduct 1997, 7: 9-110.
64. Goeckeler ZM, Masaracchia RA, Zeng Q, Chew TL, Gallagher P, Wysolmerski RB: Phosphorylation of myosin light chain kinase by p21-activated kinase PAK2. J Biol Chem 2000, 275: 8366-18374.
65. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P: Inhibition of myosin light chain kinase by p21-activated kinase. Science 1999, 283:2083-2085.
66. Tu Y, Nayak SK, Woodson J, Ross EM: Phosphorylation-regulated inhibition of the Gz GTPase-activating protein activity of RGS proteins by synapsin I. J Biol Chem 2003, 278:52273-52281.
67. a2+-independent contraction of smooth muscle. J Biol Chem 1998, 273: 3433-23439.
68. Foster DB, Shen LH, Kelly J, Thibault P, Van Eyk JE, Mak AS: Phosphorylation of caldesmon by p21-activated kinase. Implications for the Ca(2+) sensitivity of smooth muscle contraction. J Biol Chem 2000, 275:1959-1965.
69. Daub H, Gevaert K, Vandekerckhove J, Sobel A, Hall A: Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem 2001, 276:1677-1680.
70. Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, Stossel TP, Kumar R: Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol 2002, 4: 681-690.
71. King AJ, Sun H, Diaz B, Barnard D, Miao W, Bagrodia S, Marshall MS: The protein kinase Pak3 positively regulates Raf-1 activity through phosphorylation of serine 338. Nature 1998, 396: 180-183.
72. Frost JA, Steen H, Shapiro P, Lewis T, Ahn N, Shaw PE, Cobb MH: Cross-cascade activation of ERKs and ternary complex factors by Rho family proteins. EMBO J. 1997, 16:6426-6438.
73. Knaus UG, Morris S, Dong HJ, Chernoff J, Bokoch GM: Regulation of human leukocyte p21-activated kinases through G protein-coupled receptors. Science 1995, 269:221-223.
74. Schurmann A, Mooney AF, Sanders LC, Sells MA, Wang HG, Reed JC, Bokoch GM: p21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol Cell Biol 2000, 20:453-461.
75. Wang J, Frost JA, Cobb MH, Ross EM: Reciprocal signaling between heterotrimeric G proteins and the p21-stimulated protein kinase. J Biol Chem 1999, 274:31641-31647.
76. Shalom-Barak T, Knaus UG: A p21-activated kinase-controlled metabolic switch up-regulates phagocyte NADPH oxidase. J Biol Chem 2002, 277:40659-40665.
77. Tuazon PT, Lorenson MY, Walker AM, Traugh JA: p21-activated protein kinase gamma-PAK in pituitary secretory granules phosphorylates prolactin. FEBS Lett 2002, 515:84-88.
78. DerMardirossian C, Schnelzer A, Bokoch GM: Phosphorylation of RhoGDI by Pak1 mediates dissociation of Rac GTPase. Mol Cell 2004, 15:117-127.
79. Goto H, Tanabe K, Manser E, Lim L, Yasui Y, Inagaki M: Phosphorylation and reorganization of vimentin by p21-activated kinase (PAK). Genes Cells 2002, 7:91-97.
80. Vadlamudi RK, Li F, Barnes CJ, Bagheri-Yarmand R, Kumar R: p41-Arc subunit of human Arp2/3 complex is a p21-activated kinase-1-interacting substrate. EMBO Rep 2004, 5:154-160.