Akt1 mediates prostate cancer cell microinvasion and chemotaxis to metastatic stimuli via integrin Β 3 affinity modulation

British Journal of Cancer

Volumn 107, Issue 4, 2012, Pages 713-723

  Goc, A ^a,b   Liu, J ^a   Byzova, T V ^c   Somanath, P R ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Akt1; bone matrix; chemotaxis; integrin v 3; invasion; prostate cancer

Indexed keywords

BETA3 INTEGRIN; FIBRINOGEN; MAMMALIAN TARGET OF RAPAMYCIN; OSTEOPONTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AKT1; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; VITRONECTIN;

ANIMAL CELL; ARTICLE; BONE METASTASIS; CANCER CELL; CANCER INVASION; CELL MIGRATION; CELL MOTILITY; CHEMOTAXIS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOTAXIS; ENDOTHELIUM; HUMANS; INTEGRIN BETA3; MALE; MICE; NEOPLASM MICROMETASTASIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84864876133     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2012.295     Document Type: Article

References (47)

1. Briest F, Berndt A, Clement J, Junker K, Eggeling F, Grimm S, Friedrich K (2012) Tumor-stroma interactions in tumorigenesis: lessons from stem cell biology. Front Biosci (Elite Ed) 4: 1871-1887
2. Chen J, Somanath PR, Razorenova O, Chen WS, Hay N, Bornstein P, Byzova TV (2005) Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med 11: 1188-1196
3. Chung CY, Potikyan G, Firtel RA (2001) Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa. Mol Cell 7: 937-947
4. Clarke NW, Hart CA, Brown MD (2009) Molecular mechanisms of metastasis in prostate cancer. Asian J Androl 11: 57-67
5. Cooper CR, Chay CH, Pienta KJ (2002) The role of alpha(v)beta(3) in prostate cancer progression. Neoplasia 4: 191-194
6. Enomoto A, Murakami H, Asai N, Morone N, Watanabe T, Kawai K, Murakumo Y, Usukura J, Kaibuchi K, Takahashi M (2005) Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev Cell 9: 389-402
7. Feng W, McCabe NP, Mahabeleshwar GH, Somanath PR, Phillips DR, Byzova TV (2008) The angiogenic response is dictated by beta3 integrin on bone marrow-derived cells. J Cell Biol 183: 1145-1157
8. Fornaro M, Manes T, Languino LR (2001) Integrins and prostate cancer metastases. Cancer Metastasis Rev 20: 321-331
9. Fornaro M, Tallini G, Zheng DQ, Flanagan WM, Manzotti M, Languino LR (1999) p27(kip1) acts as a downstream effector of and is coexpressed with the beta1C integrin in prostatic adenocarcinoma. J Clin Invest 103: 321-329
10. Gertler F, Condeelis J (2011) Metastasis: tumor cells becoming MENAcing. Trends Cell Biol 21: 81-90
11. Goc A, Al-Husein B, Kochuparambil ST, Liu J, Heston WW, Somanath PR (2011) PI3 kinase integrates Akt and MAP kinase signaling pathways in the regulation of prostate cancer. Int J Oncol 38: 267-277
12. Goel HL, Alam N, Johnson IN, Languino LR (2009) Integrin signaling aberrations in prostate cancer. Am J Transl Res 1: 211-220
13. Grant S (2008) Cotargeting survival signaling pathways in cancer. J Clin Invest 118: 3003-3006
14. Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69: 11-25
15. Jiang P, Enomoto A, Jijiwa M, Kato T, Hasegawa T, Ishida M, Sato T, Asai N, Murakumo Y, Takahashi M (2008) An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res 68: 1310-1318
16. Kandel ES, Hay N (1999) The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp Cell Res 253: 210-229
17. Kinkade CW, Castillo-Martin M, Puzio-Kuter A, Yan J, Foster TH, Gao H, Sun Y, Ouyang X, Gerald WL, Cordon-Cardo C, Abate-Shen C (2008) Targeting AKT/mTOR and ERK MAPK signaling inhibits hormonerefractory prostate cancer in a preclinical mouse model. J Clin Invest 118: 3051-3064
18. Kirk RI, Sanderson MR, Lerea KM (2000) Threonine phosphorylation of the beta 3 integrin cytoplasmic tail, at a site recognized by PDK1 and Akt/PKB in vitro, regulates Shc binding. J Biol Chem 275: 30901-30906
19. Kochuparambil ST, Al-Husein B, Goc A, Soliman S, Somanath PR (2011) Anticancer efficacy of simvastatin on prostate cancer cells and tumor xenografts is associated with inhibition of Akt and reduced prostatespecific antigen expression. J Pharmacol Exp Ther 336: 496-505
20. McCabe NP, De S, Vasanji A, Brainard J, Byzova TV (2007) Prostate cancer specific integrin alphavbeta3 modulates bone metastatic growth and tissue remodeling. Oncogene 26: 6238-6243
21. McCabe NP, Madajka M, Vasanji A, Byzova TV (2008) Intraosseous injection of RM1 murine prostate cancer cells promotes rapid osteolysis and periosteal bone deposition. Clin Exp Metastasis 25: 581-590
22. Muller EJ, Williamson L, Kolly C, Suter MM (2008) Outside-in signaling through integrins and cadherins: a central mechanism to control epidermal growth and differentiation? J Invest Dermatol 128: 501-516
23. Murant SJ, Handley J, Stower M, Reid N, Cussenot O, Maitland NJ (1997) Co-ordinated changes in expression of cell adhesion molecules in prostate cancer. Eur J Cancer 33: 263-271
24. Nagle RB, Knox JD, Wolf C, Bowden GT, Cress AE (1994) Adhesion molecules, extracellular matrix, and proteases in prostate carcinoma. J Cell Biochem Suppl 19: 232-237
25. Pankov R, Endo Y, Even-Ram S, Araki M, Clark K, Cukierman E, Matsumoto K, Yamada KM (2005) A Rac switch regulates random vs directionally persistent cell migration. J Cell Biol 170: 793-802
26. Perlino E, Lovecchio M, Vacca RA, Fornaro M, Moro L, Ditonno P, Battaglia M, Selvaggi FP, Mastropasqua MG, Bufo P, Languino LR (2000) Regulation of mRNA and protein levels of beta1 integrin variants in human prostate carcinoma. Am J Pathol 157: 1727-1734
27. Plow EF, Haas TA, Zhang L, Loftus J, Smith JW (2000) Ligand binding to integrins. J Biol Chem 275: 21785-21788
28. Porkka KP, Visakorpi T (2004) Molecular mechanisms of prostate cancer. Eur Urol 45: 683-691
29. Qian Y, Zhong X, Flynn DC, Zheng JZ, Qiao M, Wu C, Dedhar S, Shi X, Jiang BH (2005) ILK mediates actin filament rearrangements and cell migration and invasion through PI3K/Akt/Rac1 signaling. Oncogene 24: 3154-3165
30. Ramsay AG, Marshall JF, Hart IR (2007) Integrin trafficking and its role in cancer metastasis. Cancer Metastasis Rev 26: 567-578
31. Roberts MS, Woods AJ, Dale TC, Van Der Sluijs P, Norman JC (2004) Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol Cell Biol 24: 1505-1515
32. Schmitz M, Grignard G, Margue C, Dippel W, Capesius C, Mossong J, Nathan M, Giacchi S, Scheiden R, Kieffer N (2007) Complete loss of PTEN expression as a possible early prognostic marker for prostate cancer metastasis. Int J Cancer 120: 1284-1292
33. Schneider JG, Amend SR, Weilbaecher KN (2011) Integrins and bone metastasis: integrating tumor cell and stromal cell interactions. Bone 48: 54-65
34. Shin S, Wolgamott L, Yoon SO (2012) Integrin trafficking and tumor progression. Int J Cell Biol 2012: 516789
35. Shiojima I, Walsh K (2002) Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 90: 1243-1250
36. Sikes RA, Nicholson BE, Koeneman KS, Edlund NM, Bissonette EA, Bradley MJ, Thalmann GN, Cecchini MG, Pienta KJ, Chung LW (2004) Cellular interactions in the tropism of prostate cancer to bone. Int J Cancer 110: 497-503
37. Somanath PR, Byzova TV (2009) 14-3-3beta-Rac1-p21 activated kinase signaling regulates Akt1-mediated cytoskeletal organization, lamellipodia formation and fibronectin matrix assembly. J Cell Physiol 218: 394-404
38. Somanath PR, Chen J, Byzova TV (2008) Akt1 is necessary for the vascular maturation and angiogenesis during cutaneous wound healing. Angiogenesis 11: 277-288
39. Somanath PR, Ciocea A, Byzova TV (2009a) Integrin and growth factor receptor alliance in angiogenesis. Cell Biochem Biophys 53: 53-64
40. Somanath PR, Kandel ES, Hay N, Byzova TV (2007) Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J Biol Chem 282: 22964-22976
41. Somanath PR, Razorenova OV, Chen J, Byzova TV (2006) Akt1 in endothelial cell and angiogenesis. Cell Cycle 5: 512-518
42. Somanath PR, Vijai J, Kichina JV, Byzova T, Kandel ES (2009b) The role of PAK-1 in activation of MAP kinase cascade and oncogenic transformation by Akt. Oncogene 28: 2365-2369
43. Sroka IC, Anderson TA, McDaniel KM, Nagle RB, Gretzer MB, Cress AE (2010) The laminin binding integrin alpha6beta1 in prostate cancer perineural invasion. J Cell Physiol 224: 283-288
44. Sroka IC, Sandoval CP, Chopra H, Gard JM, Pawar SC, Cress AE (2011) Macrophage-dependent cleavage of the laminin receptor alpha6beta1 in prostate cancer. Mol Cancer Res 9: 1319-1328
45. Stewart DA, Cooper CR, Sikes RA (2004) Changes in extracellular matrix (ECM) and ECM-associated proteins in the metastatic progression of prostate cancer. Reprod Biol Endocrinol 2: 2
46. Zhang P, Ozdemir T, Chung CY, Robertson GP, Dong C (2011) Sequential binding of alphaVbeta3 and ICAM-1 determines fibrin-mediated melanoma capture and stable adhesion to CD11b/CD18 on neutrophils. J Immunol 186: 242-254
47. Zheng DQ, Woodard AS, Fornaro M, Tallini G, Languino LR (1999) Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res 59: 1655-1664