PTEN regulates PDGF ligand switch for β-PDGFR signaling in prostate cancer

American Journal of Pathology

Volumn 180, Issue 3, 2012, Pages 1017-1027

  Conley Lacomb, M Katie ^a   Huang, Wei ^a   Wang, Shihua ^b   Shi, Dongping ^a   Jung, Young Suk ^a   Najy, Abdo ^a   Fridman, Rafael ^a   Bonfil, R Daniel ^a   Cher, Michael L ^a   Chen, Yong Q ^b   Kim, Hyeong Reh Choi ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR D; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; ENZYME ACTIVITY; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; SIGNAL TRANSDUCTION; UPREGULATION;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; HUMANS; LIGANDS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; PHOSPHATIDYLINOSITOL 3-KINASES; PLATELET-DERIVED GROWTH FACTOR; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 84863145254     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.11.021     Document Type: Article

References (63)

1. A. Jemal, R. Siegel, J. Xu, E. Ward Cancer statistics, 2010 CA Cancer J Clin 60 2010 277 300
2. J. Yu, C. Ustach, H.R. Kim Platelet-derived growth factor signaling and human cancer J Biochem Mol Biol 36 2003 49 59
3. L.R. Chaudhary, A.M. Hofmeister, K.A. Hruska Differential growth factor control of bone formation through osteoprogenitor differentiation Bone 34 2004 402 411
4. S.L. Godwin, S.P. Soltoff Extracellular calcium and platelet-derived growth factor promote receptor-mediated chemotaxis in osteoblasts through different signaling pathways J Biol Chem 272 1997 11307 11312
5. M. Mehrotra, S.M. Krane, K. Walters, C. Pilbeam Differential regulation of platelet-derived growth factor stimulated migration and proliferation in osteoblastic cells J Cell Biochem 93 2004 741 752
6. K. Kubota, C. Sakikawa, M. Katsumata, T. Nakamura, K. Wakabayashi Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor J Bone Miner Res 17 2002 257 265
7. M. Himeno, H. Enomoto, W. Liu, K. Ishizeki, S. Nomura, Y. Kitamura, T. Komori Impaired vascular invasion of Cbfa1-deficient cartilage engrafted in the spleen J Bone Miner Res 17 2002 1297 1305
8. J.R. Robbins, P.G. McGuire, B. Wehrle-Haller, S.L. Rogers Diminished matrix metalloproteinase 2 (MMP-2) in ectomesenchyme-derived tissues of the Patch mutant mouse: regulation of MMP-2 by PDGF and effects on mesenchymal cell migration Dev Biol 212 1999 255 263
9. Y.J. Ko, E.J. Small, F. Kabbinavar, A. Chachoua, S. Taneja, D. Reese, A. DePaoli, A. Hannah, S.P. Balk, G.J. Bubley A multi-institutional phase II study of SU101, a platelet-derived growth factor receptor inhibitor, for patients with hormone-refractory prostate cancer Clin Cancer Res 7 2001 800 805
10. D. Singh, P.G. Febbo, K. Ross, D.G. Jackson, J. Manola, C. Ladd, P. Tamayo, A.A. Renshaw, A.V. D'Amico, J.P. Richie, E.S. Lander, M. Loda, P.W. Kantoff, T.R. Golub, W.R. Sellers Gene expression correlates of clinical prostate cancer behavior Cancer Cell 1 2002 203 209
11. C.V. Ustach, W. Huang, M.K. Conley-Lacomb, C.Y. Lin, M. Che, J. Abrams, H.R. Kim A novel signaling axis of matriptase/PDGF-D/β-PDGFR in human prostate cancer Cancer Res 70 2010 9631 9640
12. C.V. Ustach, M.E. Taube, N.J. Hurst Jr, S. Bhagat, R.D. Bonfil, M.L. Cher, L. Schuger, H.R. Kim A potential oncogenic activity of platelet-derived growth factor d in prostate cancer progression Cancer Res 64 2004 1722 1729
13. T. Maehama, J.E. Dixon The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate J Biol Chem 273 1998 13375 13378
14. L. Salmena, A. Carracedo, P.P. Pandolfi Tenets of PTEN tumor suppression Cell 133 2008 403 414
15. I.C. Gray, L.M. Stewart, S.M. Phillips, J.A. Hamilton, N.E. Gray, G.J. Watson, N.K. Spurr, D. Snary Mutation and expression analysis of the putative prostate tumour-suppressor gene PTEN Br J Cancer 78 1998 1296 1300
16. Y.E. Whang, X. Wu, H. Suzuki, R.E. Reiter, C. Tran, R.L. Vessella, J.W. Said, W.B. Isaacs, C.L. Sawyers Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression Proc Natl Acad Sci U S A 95 1998 5246 5250
17. A. Di Cristofano, P.P. Pandolfi The multiple roles of PTEN in tumor suppression Cell 100 2000 387 390
18. S. Wang, J. Gao, Q. Lei, N. Rozengurt, C. Pritchard, J. Jiao, G.V. Thomas, G. Li, P. Roy-Burman, P.S. Nelson, X. Liu, H. Wu Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer Cancer Cell 4 2003 209 221
19. I.M. Berquin, Y. Min, R. Wu, J. Wu, D. Perry, J.M. Cline, M.J. Thomas, T. Thornburg, G. Kulik, A. Smith, I.J. Edwards, R. D'Agostino, H. Zhang, H. Wu, J.X. Kang, Y.Q. Chen Modulation of prostate cancer genetic risk by omega-3 and omega-6 fatty acids J Clin Invest 117 2007 1866 1875
20. W.W. Barclay, S.D. Cramer Culture of mouse prostatic epithelial cells from genetically engineered mice Prostate 63 2005 291 298
21. W.W. Barclay, L.S. Axanova, W. Chen, L. Romero, S.L. Maund, S. Soker, C.J. Lees, S.D. Cramer Characterization of adult prostatic progenitor/stem cells exhibiting self-renewal and multilineage differentiation Stem Cells 26 2008 600 610
22. C.V. Ustach, H.R. Kim Platelet-derived growth factor D is activated by urokinase plasminogen activator in prostate carcinoma cells Mol Cell Biol 25 2005 6279 6288
23. C.V. Ustach, W. Huang, M.K. Conley-LaComb, C.Y. Lin, M. Che, J. Abrams, H.R. Kim A novel signaling axis of matriptase/PDGF-D/β-PDGFR in human prostate cancer Cancer Res 70 2010 9631 9640
24. Y.J. Zhou, Y.X. Xiong, X.T. Wu, D. Shi, W. Fan, T. Zhou, Y.C. Li, X. Huang Inactivation of PTEN is associated with increased angiogenesis and VEGF overexpression in gastric cancer World J Gastroenterol 10 2004 3225 3229
25. H. Zhao, J. Dupont, S. Yakar, M. Karas, D. LeRoith PTEN inhibits cell proliferation and induces apoptosis by downregulating cell surface IGF-IR expression in prostate cancer cells Oncogene 23 2004 786 794
26. E. Bergsten, M. Uutela, X. Li, K. Pietras, A. Ostman, C.H. Heldin, K. Alitalo, U. Eriksson PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor Nat Cell Biol 3 2001 512 516
27. W.J. LaRochelle, M. Jeffers, W.F. McDonald, R.A. Chillakuru, N.A. Giese, N.A. Lokker, C. Sullivan, F.L. Boldog, M. Yang, C. Vernet, C.E. Burgess, E. Fernandes, L.L. Deegler, B. Rittman, J. Shimkets, R.A. Shimkets, J.M. Rothberg, H.S. Lichenstein PDGF-D, a new protease-activated growth factor Nat Cell Biol 3 2001 517 521
28. D.G. Hardie AMPK: a key regulator of energy balance in the single cell and the whole organism Int J Obes (Lond) 32 Suppl 4 2008 S7 S12
29. D.B. Shackelford, R.J. Shaw The LKB1-AMPK pathway: metabolism and growth control in tumour suppression Nat Rev Cancer 9 2009 563 575
30. M. Lee, J.T. Hwang, H. Yun, E.J. Kim, M.J. Kim, S.S. Kim, J. Ha Critical roles of AMP-activated protein kinase in the carcinogenic metal-induced expression of VEGF and HIF-1 proteins in DU145 prostate carcinoma Biochem Pharmacol 72 2006 91 103
31. K.M. Neurath, M.P. Keough, T. Mikkelsen, K.P. Claffey AMP-dependent protein kinase alpha 2 isoform promotes hypoxia-induced VEGF expression in human glioblastoma Glia 53 2006 733 743
32. H. Yun, M. Lee, S.S. Kim, J. Ha Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma J Biol Chem 280 2005 9963 9972
33. A. Chott, Z. Sun, D. Morganstern, J. Pan, T. Li, M. Susani, I. Mosberger, M.P. Upton, G.J. Bubley, S.P. Balk Tyrosine kinases expressed in vivo by human prostate cancer bone marrow metastases and loss of the type 1 insulin-like growth factor receptor Am J Pathol 155 1999 1271 1279
34. P. Mathew, P.F. Thall, C.D. Bucana, W.K. Oh, M.J. Morris, D.M. Jones, M.M. Johnson, S. Wen, L.C. Pagliaro, N.M. Tannir, S.M. Tu, A.A. Meluch, L. Smith, L. Cohen, S.J. Kim, P. Troncoso, I.J. Fidler, C.J. Logothetis Platelet-derived growth factor receptor inhibition and chemotherapy for castration-resistant prostate cancer with bone metastases Clin Cancer Res 13 2007 5816 5824
35. K. Fudge, D.G. Bostwick, M.E. Stearns Platelet-derived growth factor A and B chains and the alpha and beta receptors in prostatic intraepithelial neoplasia Prostate 29 1996 282 286
36. K. Fudge, C.Y. Wang, M.E. Stearns Immunohistochemistry analysis of platelet-derived growth factor A and B chains and platelet-derived growth factor alpha and beta receptor expression in benign prostatic hyperplasias and Gleason-graded human prostate adenocarcinomas Mod Pathol 7 1994 549 554
37. K. Lin, J.R. Taylor Jr, T.D. Wu, J. Gutierrez, J.M. Elliott, J.M. Vernes, H. Koeppen, H.S. Phillips, F.J. de Sauvage, Y.G. Meng TMEFF2 is a PDGF-AA binding protein with methylation-associated gene silencing in multiple cancer types including glioma PLoS One 6 2011 e18608
38. S.M. Sintich, M.L. Lamm, J.A. Sensibar, C. Lee Transforming growth factor-beta1-induced proliferation of the prostate cancer cell line, TSU-Pr1: the role of platelet-derived growth factor Endocrinology 140 1999 3411 3415
39. S.S. Ng, G.R. MacPherson, M. Gutschow, K. Eger, W.D. Figg Antitumor effects of thalidomide analogs in human prostate cancer xenografts implanted in immunodeficient mice Clin Cancer Res 10 2004 4192 4197
40. H.G. van der Poel Smart drugs in prostate cancer Eur Urol 45 2004 1 17
41. H. Uehara, S.J. Kim, T. Karashima, D.L. Shepherd, D. Fan, R. Tsan, J.J. Killion, C. Logothetis, P. Mathew, I.J. Fidler Effects of blocking platelet-derived growth factor-receptor signaling in a mouse model of experimental prostate cancer bone metastases J Natl Cancer Inst 95 2003 458 470
42. S.J. Kim, H. Uehara, S. Yazici, R.R. Langley, J. He, R. Tsan, D. Fan, J.J. Killion, I.J. Fidler Simultaneous blockade of platelet-derived growth factor-receptor and epidermal growth factor-receptor signaling and systemic administration of paclitaxel as therapy for human prostate cancer metastasis in bone of nude mice Cancer Res 64 2004 4201 4208
43. M.W. Deininger, S.G. O'Brien, J.M. Ford, B.J. Druker Practical management of patients with chronic myeloid leukemia receiving imatinib J Clin Oncol 21 2003 1637 1647
44. F. Guilhot Indications for imatinib mesylate therapy and clinical management Oncologist 9 2004 271 281
45. R. Kerkela, L. Grazette, R. Yacobi, C. Iliescu, R. Patten, C. Beahm, B. Walters, S. Shevtsov, S. Pesant, F.J. Clubb, A. Rosenzweig, R.N. Salomon, R.A. Van Etten, J. Alroy, J.B. Durand, T. Force Cardiotoxicity of the cancer therapeutic agent imatinib mesylate Nat Med 12 2006 908 916
46. N. Chalhoub, S.J. Baker PTEN and the PI3-kinase pathway in cancer Annu Rev Pathol 4 2009 127 150
47. J.J. Gildea, M. Herlevsen, M.A. Harding, K.M. Gulding, C.A. Moskaluk, H.F. Frierson, D. Theodorescu PTEN can inhibit in vitro organotypic and in vivo orthotopic invasion of human bladder cancer cells even in the absence of its lipid phosphatase activity Oncogene 23 2004 6788 6797
48. N.R. Leslie, X. Yang, C.P. Downes, C.J. Weijer PtdIns(3,4,5)P(3)- dependent and -independent roles for PTEN in the control of cell migration Curr Biol 17 2007 115 125
49. J. Gu, M. Tamura, R. Pankov, E.H. Danen, T. Takino, K. Matsumoto, K.M. Yamada Shc and FAK differentially regulate cell motility and directionality modulated by PTEN J Cell Biol 146 1999 389 403
50. J.L. Liu, X. Sheng, Z.K. Hortobagyi, Z. Mao, G.E. Gallick, W.K. Yung Nuclear PTEN-mediated growth suppression is independent of Akt down-regulation Mol Cell Biol 25 2005 6211 6224
51. O. Gimm, A. Perren, L.P. Weng, D.J. Marsh, J.J. Yeh, U. Ziebold, E. Gil, R. Hinze, L. Delbridge, J.A. Lees, G.L. Mutter, B.G. Robinson, P. Komminoth, H. Dralle, C. Eng Differential nuclear and cytoplasmic expression of PTEN in normal thyroid tissue, and benign and malignant epithelial thyroid tumors Am J Pathol 156 2000 1693 1700
52. J. Puc, R. Parsons PTEN loss inhibits CHK1 to cause double stranded-DNA breaks in cells Cell Cycle 4 2005 927 929
53. W.H. Shen, A.S. Balajee, J. Wang, H. Wu, C. Eng, P.P. Pandolfi, Y. Yin Essential role for nuclear PTEN in maintaining chromosomal integrity Cell 128 2007 157 170
54. B. Zhang, F. Gu, C. She, H. Guo, W. Li, R. Niu, L. Fu, N. Zhang, Y. Ma Reduction of Akt2 inhibits migration and invasion of glioma cells Int J Cancer 125 2009 585 595
55. B. Boyer, A.M. Valles, N. Edme Induction and regulation of epithelial-mesenchymal transitions Biochem Pharmacol 60 2000 1091 1099
56. S.J. Grille, A. Bellacosa, J. Upson, A.J. Klein-Szanto, F. van Roy, W. Lee-Kwon, M. Donowitz, P.N. Tsichlis, L. Larue The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines Cancer Res 63 2003 2172 2178
57. L. Larue, A. Bellacosa Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways Oncogene 24 2005 7443 7454
58. J. Zhou, W. Huang, R. Tao, S. Ibaragi, F. Lan, Y. Ido, X. Wu, Y.O. Alekseyev, M.E. Lenburg, G.F. Hu, Z. Luo Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells Oncogene 28 2009 1993 2002
59. I. Ben Sahra, K. Laurent, A. Loubat, S. Giorgetti-Peraldi, P. Colosetti, P. Auberger, J.F. Tanti, Y. Le Marchand-Brustel, F. Bost The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level Oncogene 27 2008 3576 3586
60. H.U. Park, S. Suy, M. Danner, V. Dailey, Y. Zhang, H. Li, D.R. Hyduke, B.T. Collins, G. Gagnon, B. Kallakury, D. Kumar, M.L. Brown, A. Fornace, A. Dritschilo, S.P. Collins AMP-activated protein kinase promotes human prostate cancer cell growth and survival Mol Cancer Ther 8 2009 733 741
61. R.R. Chhipa, Y. Wu, C. Ip AMPK-mediated autophagy is a survival mechanism in androgen-dependent prostate cancer cells subjected to androgen deprivation and hypoxia Cell Signal 23 2011 1466 1472
62. P. Bork Complement components C1r/C1s, bone morphogenic protein 1 and Xenopus laevis developmentally regulated protein UVS.2 share common repeats FEBS Lett 282 1991 9 12
63. M. Ehnman, H. Li, L. Fredriksson, K. Pietras, U. Eriksson The uPA/uPAR system regulates the bioavailability of PDGF-DD: implications for tumour growth Oncogene 28 2009 534 544