JNK and PTEN cooperatively control the development of invasive adenocarcinoma of the prostate

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 30, 2012, Pages 12046-12051

  Hübner, Anette ^a,h   Mulholland, David J ^b   Standen, Claire L ^a   Karasarides, Maria ^a,i   Cavanagh Kyros, Julie ^c   Barrett, Tamera ^c   Chi, Hongbo ^d   Greiner, Dale L ^a   Tournier, Cathy ^e   Sawyers, Charles L ^f   Flavell, Richard A ^g   Wu, Hong ^b   Davis, Roger J ^a,c  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^g YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h NOVARTIS PHARMA AG   (Switzerland)

ⁱ Infinity Pharmaceuticals Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE DELETION; HISTOPATHOLOGY; INVASIVE CARCINOMA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE EPITHELIUM; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; HISTOLOGICAL TECHNIQUES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE;

MUS;

EID: 84864365646     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1209660109     Document Type: Article

References (59)

1. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
2. Cellurale C, et al. (2012) Role of JNK in mammary gland development and breast cancer. Cancer Res 72:472-481.
3. Tournier C, et al. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288:870-874. (Pubitemid 30257738)
4. Lamb JA, Ventura JJ, Hess P, Flavell RA, Davis RJ (2003) JunD mediates survival signaling by the JNK signal transduction pathway. Mol Cell 11:1479-1489. (Pubitemid 36776535)
5. Das M, et al. (2007) Suppression of p53-dependent senescence by the JNK signal transduction pathway. Proc Natl Acad Sci USA 104:15759-15764. (Pubitemid 350035373)
6. Hess P, Pihan G, Sawyers CL, Flavell RA, Davis RJ (2002) Survival signaling mediated by c-Jun NH(2)-terminal kinase in transformed B lymphoblasts. Nat Genet 32:201-205. (Pubitemid 34977219)
7. Cellurale C, et al. (2011) Requirement of c-Jun NH(2)-terminal kinase for Ras-initiated tumor formation. Mol Cell Biol 31:1565-1576.
8. Hui L, Zatloukal K, Scheuch H, Stepniak E, Wagner EF (2008) Proliferation of human HCC cells and chemically induced mouse liver cancers requires JNK1-dependent p21 downregulation. J Clin Invest 118:3943-3953.
9. Das M, Garlick DS, Greiner DL, Davis RJ (2011) The role of JNK in the development of hepatocellular carcinoma. Genes Dev 25:634-645.
10. Sakurai T, Maeda S, Chang L, Karin M (2006) Loss of hepatic NF-kappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc Natl Acad Sci USA 103:10544-10551. (Pubitemid 44078014)
11. Chen N, et al. (2001) Suppression of skin tumorigenesis in c-Jun NH(2)-terminal kinase-2-deficient mice. Cancer Res 61:3908-3912. (Pubitemid 32720949)
12. Schramek D, et al. (2011) The stress kinase MKK7 couples oncogenic stress to p53 stability and tumor suppression. Nat Genet 43:212-219.
13. Cellurale C, et al. (2010) Role of JNK in a Trp53-dependent mouse model of breast cancer. PLoS ONE 5:e12469.
14. She QB, Chen N, Bode AM, Flavell RA, Dong Z (2002) Deficiency of c-Jun-NH(2)-terminal kinase-1 in mice enhances skin tumor development by 12-O-tetradecanoyl-phorbol-13-acetate. Cancer Res 62:1343-1348. (Pubitemid 34407790)
15. Chen P, et al. (2010) Jnk2 effects on tumor development, genetic instability and replicative stress in an oncogene-driven mouse mammary tumor model. PLoS ONE 5:e10443.
16. Vlietstra RJ, van Alewijk DC, Hermans KG, van Steenbrugge GJ, Trapman J (1998) Frequent inactivation of PTEN in prostate cancer cell lines and xenografts. Cancer Res 58:2720-2723. (Pubitemid 28311897)
17. Li J, et al. (1997) PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275:1943-1947. (Pubitemid 27148818)
18. Whang YE, et al. (1998) Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci USA 95:5246-5250. (Pubitemid 28208583)
19. Wang S, et al. (2003) Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4:209-221. (Pubitemid 37163835)
20. Vivanco I, et al. (2007) Identification of the JNK signaling pathway as a functional target of the tumor suppressor PTEN. Cancer Cell 11:555-569. (Pubitemid 46856910)
21. Kim HL, et al. (2001) Mitogen-activated protein kinase kinase 4 metastasis suppressor gene expression is inversely related to histological pattern in advancing human prostatic cancers. Cancer Res 61:2833-2837. (Pubitemid 32691920)
22. Chen Z, et al. (2005) Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature 436:725-730. (Pubitemid 41117277)
23. Ding Z, et al. (2011) SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 470:269-273.
24. Fuchs SY, et al. (1998) JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes Dev 12:2658-2663. (Pubitemid 28420646)
25. Tournier C, et al. (2001) MKK7 is an essential component of the JNK signal transduction pathway activated by proinflammatory cytokines. Genes Dev 15:1419-1426. (Pubitemid 32524648)
26. Craft N, Sawyers CL (1998-1999) Mechanistic concepts in androgen-dependence of prostate cancer. Cancer Metastasis Rev 17:421-427.
27. El Hilali N, Rubio N, Martinez-Villacampa M, Blanco J (2002) Combined noninvasive imaging and luminometric quantification of luciferase-labeled human prostate tumors and metastases. Lab Invest 82:1563-1571. (Pubitemid 35332915)
28. Rubio N, Villacampa MM, El Hilali N, Blanco J (2000) Metastatic burden in nude mice organs measured using prostate tumor PC-3 cells expressing the luciferase gene as a quantifiable tumor cell marker. Prostate 44:133-143. (Pubitemid 30419188)
29. Liao CP, et al. (2007) Mouse models of prostate adenocarcinoma with the capacity to monitor spontaneous carcinogenesis by bioluminescence or fluorescence. Cancer Res 67:7525-7533.
30. Wang S, et al. (2006) Pten deletion leads to the expansion of a prostatic stem/progenitor cell subpopulation and tumor initiation. Proc Natl Acad Sci USA 103: 1480-1485. (Pubitemid 43191191)
31. Xin L, Lukacs RU, Lawson DA, Cheng D, Witte ON (2007) Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 25: 2760-2769. (Pubitemid 350127860)
32. Korsten H, Ziel-van der Made A, Ma X, van der Kwast T, Trapman J (2009) Accumulating progenitor cells in the luminal epithelial cell layer are candidate tumor initiating cells in a Pten knockout mouse prostate cancer model. PLoS ONE 4:e5662.
33. Wang X, et al. (2009) A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 461:495-500.
34. Mulholland DJ, et al. (2009) Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res 69:8555-8562.
35. Lotan TL, et al. (2007) Up-regulation of MKK4, MKK6 and MKK7 during prostate cancer progression: An important role for SAPK signalling in prostatic neoplasia. J Pathol 212:386-394. (Pubitemid 47099015)
36. Cunha GR (1994) Role of mesenchymal-epithelial interactions in normal and abnormal development of the mammary gland and prostate. Cancer 74(3, Suppl):1030-1044.
37. Robinson VL, et al. (2008) Mitogen-activated protein kinase kinase 4/c-Jun NH2-terminal kinase kinase 1 protein expression is subject to translational regulation in prostate cancer cell lines. Mol Cancer Res 6:501-508. (Pubitemid 351416540)
38. Marasa BS, et al. (2009) Increased MKK4 abundance with replicative senescence is linked to the joint reduction of multiple microRNAs. Sci Signal 2:ra69.
39. Yoshida BA, et al. (1999) Mitogen-activated protein kinase kinase 4/stress-activated protein/Erk kinase 1 (MKK4/SEK1), a prostate cancer metastasis suppressor gene encoded by human chromosome 17. Cancer Res 59:5483-5487. (Pubitemid 29526462)
40. Taylor JL, et al. (2008) New paradigms for the function of JNKK1/MKK4 in controlling growth of disseminated cancer cells. Cancer Lett 272:12-22.
41. Khamis ZI, Iczkowski KA, Sang QX (2011) Metastasis suppressors in human benign prostate, intraepithelial neoplasia, and invasive cancer: Their prospects as therapeutic agents. Med Res Rev, 10.1002/med.20232.
42. Teng DH, et al. (1997) Human mitogen-activated protein kinase kinase 4 as a candidate tumor suppressor. Cancer Res 57:4177-4182. (Pubitemid 27413418)
43. Yamada SD, et al. (2002) Mitogen-activated protein kinase kinase 4 (MKK4) acts as a metastasis suppressor gene in human ovarian carcinoma. Cancer Res 62:6717-6723. (Pubitemid 35364143)
44. Whitmarsh AJ, Davis RJ (2007) Role of mitogen-activated protein kinase kinase 4 in cancer. Oncogene 26:3172-3184. (Pubitemid 46763013)
45. Kan Z, et al. (2010) Diverse somatic mutation patterns and pathway alterations in human cancers. Nature 466:869-873.
46. Greenman C, et al. (2007) Patterns of somatic mutation in human cancer genomes. Nature 446:153-158. (Pubitemid 46398669)
47. Berger MF, et al. (2011) The genomic complexity of primary human prostate cancer. Nature 470:214-220.
48. Magi-Galluzzi C, et al. (1997) Mitogen-activated protein kinase phosphatase 1 is overexpressed in prostate cancers and is inversely related to apoptosis. Lab Invest 76:37-51. (Pubitemid 27058196)
49. Carver BS, et al. (2011) Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell 19:575-586.
50. Mulholland DJ, et al. (2011) Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 19:792-804.
51. Carver BS, et al. (2009) Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 41:619-624.
52. King JC, et al. (2009) Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 41:524-526.
53. Clegg NJ, et al. (2011) MYC cooperates with AKT in prostate tumorigenesis and alters sensitivity to mTOR inhibitors. PLoS ONE 6:e17449.
54. Ventura JJ, Kennedy NJ, Flavell RA, Davis RJ (2004) JNK regulates autocrine expression of TGF-beta1. Mol Cell 15:269-278. (Pubitemid 38950973)
55. Dong C, et al. (1998) Defective T cell differentiation in the absence of Jnk1. Science 282:2092-2095. (Pubitemid 29001267)
56. Yang DD, et al. (1998) Differentiation of CD4+ T cells to Th1 cells requires MAP kinase JNK2. Immunity 9:575-585. (Pubitemid 28499208)
57. Wang X, et al. (2007) Targeted deletion of themitogen-activated protein kinase kinase 4 gene in the nervous system causes severe brain developmental defects and premature death. Mol Cell Biol 27:7935-7946. (Pubitemid 350086426)
58. Lesche R, et al. (2002) Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis 32:148-149. (Pubitemid 34211723)
59. Wu X, et al. (2001) Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissue-specific gene ablation. Mech Dev 101:61-69. (Pubitemid 32186310)