IGFBP-3 is a metastasis suppression gene in prostate cancer

Cancer Research

Volumn 71, Issue 15, 2011, Pages 5154-5163

  Mehta, Hemal H ^a   Gao, Qinglei ^a   Galet, Colette ^b   Paharkova, Vladislava ^a   Wan, Junxiang ^a   Said, Jonathan ^b   Sohn, Joanne J ^b   Lawson, Gregory ^b   Cohen, Pinchas ^a   Cobb, Laura J ^a   Lee, Kuk Wha ^a  

^a MATTEL CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED CANCER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CARCINOGENESIS; CASTRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE DELETION; GENE FUNCTION; IGFBP 3 GENE; KNOCKOUT MOUSE; LUNG METASTASIS; MALE; METASTASIS; METASTASIS INHIBITION; MOUSE; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; SPLEEN TUMOR; SPLENIC LYMPHOMA; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA; ANDROGENS; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CROSSES, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENES, MYC; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; LUNG NEOPLASMS; LYMPHOMA, NON-HODGKIN; MALE; MICE; MICE, KNOCKOUT; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS, HORMONE-DEPENDENT; ORCHIECTOMY; PHENOTYPE; PROSTATIC NEOPLASMS; SPLENIC NEOPLASMS; TUMOR BURDEN; TUMOR STEM CELL ASSAY;

EID: 79960939160     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-4513     Document Type: Article

References (55)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
2. Nelson WG, De Marzo AM, Isaacs WB. Prostate cancer. N Engl J Med 2003;349:366-81. (Pubitemid 36886244)
3. Berthold DR, Pond GR, Soban F, de Wit R, Eisenberger M, Tannock IF. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. J Clin Oncol 2008;26:242-5.
4. Kantoff PW, Higano CS, Shore ND, Berger ER, Small EJ, Penson DF, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med 2010;363:411-22.
5. Yamada PM, Lee KW. Perspectives in mammalian IGFBP-3 biology: local vs. systemic action. Am J Physiol Cell Physiol 2009;296:C954-76.
6. Nickerson T, Huynh H, Pollak M. Insulin-like growth factor binding protein-3 induces apoptosis in MCF7 breast cancer cells. Biochem Biophys Res Commun 1997;237:690-3. (Pubitemid 27434749)
7. Schwarze SR, DePrimo SE, Grabert LM, Fu VX, Brooks JD, Jarrard DF. Novel pathways associated with bypassing cellular senescence in human prostate epithelial cells. J Biol Chem 2002;277:14877-83. (Pubitemid 34952561)
8. Massoner P, Colleselli D, Matscheski A, Pircher H, Geley S, Jansen Durr P, et al. Novel mechanism of IGF-binding protein-3 action on prostate cancer cells: inhibition of proliferation, adhesion, and motility. Endocr Relat Cancer 2009;16:795-808.
9. Thelen P, Burfeind P, Grzmil M, Voigt S, Ringert RH, Hemmerlein B. cDNA microarray analysis with amplified RNA after isolation of intact cellular RNA from neoplastic and non-neoplastic prostate tissue separated by laser microdissections. Int J Oncol 2004;24:1085-92.
10. Liu B, Lee KW, Li H, Ma L, Lin GL, Chandraratna RA, et al. Combination therapy of insulin-like growth factor binding protein-3 and retinoid X receptor ligands synergize on prostate cancer cell apoptosis in vitro and in vivo. Clin Cancer Res 2005;11:4851-6. (Pubitemid 41557205)
11. Liu B, Lee KW, Anzo M, Zhang B, Zi X, Tao Y, et al. Insulin-like growth factor-binding protein-3 inhibition of prostate cancer growth involves suppression of angiogenesis. Oncogene 2007;26:1811-9. (Pubitemid 46426204)
12. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, et al. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998;279:563-6. (Pubitemid 28067285)
13. Chan JM, Stampfer MJ, Ma J, Gann P, Gaziano JM, Pollak M, et al. Insulin-like growth factor-I (IGF-I) and IGF binding protein-3 as predictors of advanced-stage prostate cancer. J Natl Cancer Inst 2002;94:1099-106. (Pubitemid 34830730)
14. Shariat SF, Lamb DJ, Kattan MW, Nguyen C, Kim J, Beck J, et al. Association of preoperative plasma levels of insulin-like growth factor I and insulin-like growth factor binding proteins-2 and -3 with prostate cancer invasion, progression, and metastasis. J Clin Oncol 2002;20:833-41. (Pubitemid 34111393)
15. Wang L, Habuchi T, Tsuchiya N, Mitsumori K, Ohyama C, Sato K, et al. Insulin-like growth factor-binding protein-3 gene -202 A/C polymorphism is correlated with advanced disease status in prostate cancer. Cancer Res 2003;63:4407-11. (Pubitemid 36951011)
16. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, Matusik R, et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003;4:223-38. (Pubitemid 37163836)
17. Yamada PM, Mehta HH, Hwang D, Roos KP, Hevener AL, Lee KW. Evidence of a role for insulin-like growth factor binding protein (IGFBP)-3 in metabolic regulation. Endocrinology 2010;151:5741-50.
18. Hwang DL, Lee PD, Cohen P. Quantitative ontogeny of murine insulin-like growth factor (IGF)-I, IGF-binding protein-3 and the IGF-related acid-labile subunit. Growth Horm IGF Res 2008;18:65-74. (Pubitemid 351228809)
19. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
20. Nickerson T, Miyake H, Gleave ME, Pollak M. Castration-induced apoptosis of androgen-dependent shionogi carcinoma is associated with increased expression of genes encoding insulin-like growth factor-binding proteins. Cancer Res 1999;59:3392-5. (Pubitemid 29334498)
21. Bruyninx M, Ammar H, Reiter E, Cornet A, Closset J. Genes upregulated during castration-induced rat prostatic apoptosis: cloning and characterization of new cDNAs. BJU Int 2000;85:1134-42. (Pubitemid 30348814)
22. Fink D, Fazli L, Aronow B, Gleave ME, Ong CJ. Clusterin is not essential for androgen-regulated involution and regeneration of the normal mouse prostate. Prostate 2006;66:1445-54. (Pubitemid 44350370)
23. Bruckheimer EM, Cho S, Brisbay S, Johnson DJ, Gingrich JR, Greenberg N, et al. The impact of bcl-2 expression and bax deficiency on prostate homeostasis in vivo. Oncogene 2000;19:2404-12. (Pubitemid 30323473)
24. Berges RR, Furuya Y, Remington L, English HF, Jacks T, Isaacs JT. Cell proliferation, DNA repair, and p53 function are not required for programmed death of prostatic glandular cells induced by androgen ablation. Proc Natl Acad Sci U S A 1993;90:8910-4. (Pubitemid 23306420)
25. Colombel M, Radvanyi F, Blanche M, Abbou C, Buttyan R, Donehower LA, et al. Androgen suppressed apoptosis is modified in p53 deficient mice. Oncogene 1995;10:1269-74.
26. Buckbinder L, Talbott R, Velasco-Miguel S, Takenaka I, Faha B, Seizinger BR, et al. Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature 1995;377:646-9.
27. Nimptsch K, Platz EA, Pollak MN, Kenfield SA, Stampfer MJ, Willett WC, et al. Plasma insulin-like growth factor 1 is positively associated with low-grade prostate cancer in the Health Professionals Follow-up Study 1993-2004. Int J Cancer 2011;128:660-7.
28. Silha JV, Sheppard PC, Mishra S, Gui Y, Schwartz J, Dodd JG, et al. Insulin-like growth factor (IGF) binding protein-3 attenuates prostate tumor growth by IGF-dependent and IGF-independent mechanisms. Endocrinology 2006;147:2112-21.
29. Cohen P. Insulin-like growth factor binding protein-3: insulin-like growth factor independence comes of age. Endocrinology 2006;147:2109-11.
30. Lee KS, Lee YS, Lee JM, Ito K, Cinghu S, Kim JH, et al. Runx3 is required for the differentiation of lung epithelial cells and suppression of lung cancer. Oncogene 2010;29;3349-61.
31. Jeanes A, Gottardi CJ, Yap AS. Cadherins and cancer: how does cadherin dysfunction promote tumor progression? Oncogene 2008;27:6920-9.
32. Tanaka H, Kono E, Tran CP, Miyazaki H, Yamashiro J, Shimomura T, et al. Monoclonal antibody targeting of N-cadherin inhibits prostate cancer growth, metastasis and castration resistance. Nat Med 2010;16:1414-20.
33. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, Zhang J, et al. SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 2011;470:269-73.
34. Lee JM, Dedhar S, Kalluri R, Thompson EW. The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 2006;172:973-81.
35. Graham TR, Zhau HE, Odero-Marah VA, Osunkoya AO, Kimbro KS, Tighiouart M, et al. Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells. Cancer Res 2008;68:2479-88. (Pubitemid 351521824)
36. Prasad PD, Stanton JA, Assinder SJ. Expression of the actin-associated protein transgelin (SM22) is decreased in prostate cancer. Cell Tissue Res 2010;339:337-47.
37. Rajah R, Valentinis B, Cohen P. Insulin-like growth factor (IGF)-binding protein-3 induces apoptosis and mediates the effects of transforming growth factor-beta1 on programmed cell death through a p53- and IGF-independent mechanism. J Biol Chem 1997;272:12181-8. (Pubitemid 27202802)
38. Harms KL, Chen X. The C terminus of p53 family proteins is a cell fate determinant. Mol Cell Biol 2005;25:2014-30. (Pubitemid 40280163)
39. Lee KW, Ma L, Yan X, Liu B, Zhang XK, Cohen P. Rapid apoptosis induction by IGFBP-3 involves an insulin-like growth factor-independent nucleomitochondrial translocation of RXRalpha/Nur77. J Biol Chem 2005;280:16942-8. (Pubitemid 41389154)
40. Lee KW, Liu B, Ma L, Li H, Bang P, Koeffler HP, et al. Cellular internalization of insulin-like growth factor binding protein-3: distinct endocytic pathways facilitate re-uptake and nuclear localization. J Biol Chem 2004;279:469-76. (Pubitemid 38044848)
41. Burrows C, Holly JM, Laurence NJ, Vernon EG, Carter JV, Clark MA, et al. Insulin-like growth factor binding protein 3 has opposing actions on malignant and nonmalignant breast epithelial cells that are each reversible and dependent upon cholesterol-stabilized integrin receptor complexes. Endocrinology 2006;147:3484-500. (Pubitemid 43901140)
42. Lee KW, Cobb LJ, Paharkova-Vatchkova V, Liu B, Milbrandt J, Cohen P. Contribution of the orphan nuclear receptor Nur77 to the apoptotic action of IGFBP-3. Carcinogenesis 2007;28:1653-8. (Pubitemid 47289026)
43. Paharkova-Vatchkova V, Lee KW. Nuclear export and mitochondrial and endoplasmic reticulum localization of IGF-binding protein 3 regulate its apoptotic properties. Endocr Relat Cancer 2010;17;293-302.
44. Torng PL, Lee YC, Huang CY, Ye JH, Lin YS, Chu YW, et al. Insulin-like growth factor binding protein-3 (IGFBP-3) acts as an invasion-metastasis suppressor in ovarian endometrioid carcinoma. Oncogene 2008;27:2137-47.
45. Oh SH, Lee OH, Schroeder CP, Oh YW, Ke S, Cha HJ, et al. Antimetastatic activity of insulin-like growth factor binding protein-3 in lung cancer is mediated by insulin-like growth factor-independent urokinase-type plasminogen activator inhibition. Mol Cancer Ther 2006;5:2685-95. (Pubitemid 44848995)
46. Fuchs CS, Goldberg RM, Sargent DJ, Meyerhardt JA, Wolpin BM, Green EM, et al. Plasma insulin-like growth factors, insulin-like binding protein-3, and outcome in metastatic colorectal cancer: results from intergroup trial N9741. Clin Cancer Res 2008;14:8263-9.
47. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J, et al. Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003;4:209-21. (Pubitemid 37163835)
48. Gingrich JR, Barrios RJ, Morton RA, Boyce BF, DeMayo FJ, Finegold MJ, et al. Metastatic prostate cancer in a transgenic mouse. Cancer Res 1996;56:4096-102. (Pubitemid 26304996)
49. Zhou Z, Flesken-Nikitin A, Corney DC, Wang W, Goodrich DW, Roy-Burman P, et al. Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res 2006;66:7889-98. (Pubitemid 44299151)
50. Iwata T, Schultz D, Hicks J, Hubbard GK, Mutton LN, Lotan TL, et al. MYCoverexpression induces prostatic intraepithelial neoplasia andloss of Nkx3.1 in mouse luminal epithelial cells. PLoS One 2010;5:e9427.
51. Nandana S, Ellwood-Yen K, Sawyers C, Wills M, Weidow B, Case T, et al. Hepsin cooperates with MYC in the progression of adenocarcinoma in a prostate cancer mouse model. Prostate 2010;70:591-600.
52. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 2007;21:1050-63. (Pubitemid 46686474)
53. Dimri M, Bommi PV, Sahasrabuddhe AA, Khandekar JD, Dimri GP. Dietary omega-3 polyunsaturated fatty acids suppress expression of EZH2 in breast cancer cells. Carcinogenesis 2010;31:489-95.
54. Kim MS, Kim SY, Arunachalam S, Hwang PH, Yi HK, Nam SY, et al. c-myb stimulates cell growth by regulation of insulin-like growth factor (IGF) and IGF-binding protein-3 in K562 leukemia cells. Biochem Biophys Res Commun 2009;385:38-43.
55. Muhlbradt E, Asatiani E, Ortner E, Wang A, Gelmann EP. NKX3.1 activates expression of insulin-like growth factor binding protein-3 to mediate insulin-like growth factor-I signaling and cell proliferation. Cancer Res 2009;69:2615-22.