Disruption of PPARγ signaling results in mouse prostatic intraepithelial neoplasia involving active autophagy

Cell Death and Differentiation

Volumn 17, Issue 3, 2010, Pages 469-481

  Jiang, M ^a   Fernandez, S ^a   Jerome, W G ^b   He, Y ^b   Yu, X ^a   Cai, H ^b   Boone, B ^b   Yi, Y ^b   Magnuson, M A ^c   Roy Burman, P ^d   Matusik, R J ^a,b   Shappell, S B ^b   Hayward, S W ^a,b  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b Department of Cancer Biology ^*  (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Autophagy; Differentiation; Oxidative Stress; PPAR Peroxisome proliferator activated receptor gamma (g)

Indexed keywords

BECLIN 1; LIPID; MOLECULAR MARKER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PROTEIN LC 3; UNCLASSIFIED DRUG; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; ISOPROTEIN; ROSIGLITAZONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CELL CYCLE REGULATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EPITHELIUM CELL; GENE EXPRESSION PROFILING; HISTOPATHOLOGY; IN VITRO STUDY; KNOCKOUT MOUSE; LIPID DEGRADATION; LIPID OXIDATION; LYSOSOME; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROSTATE HYPERTROPHY; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; CELL LINE; CYTOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; PROSTATE; PROSTATE TUMOR; TRANSGENIC MOUSE; ULTRASTRUCTURE; XENOGRAFT;

MUS;

ANIMALS; AUTOPHAGY; CELL LINE; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HYPOGLYCEMIC AGENTS; MALE; MICE; MICE, SCID; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PHENOTYPE; PPAR GAMMA; PROSTATE; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; THIAZOLIDINEDIONES; TRANSPLANTATION, HETEROLOGOUS;

EID: 76749130074     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2009.148     Document Type: Article

References (39)

1. Yu K, Bayona W, Kallen CB, Harding HP, Ravera CP, McMahon G et al. Differential activation of peroxisome proliferator-activated receptors by eicosanoids. J Biol Chem 1995; 270: 23975-23983.
2. Hihi AK, Michalik L, Wahli W. PPARs: transcriptional effectors of fatty acids and their derivatives. Cell Mol Life Sci 2002; 59: 790-798.
3. Tontonoz P, Hu E, Graves RA, Budavari AI, Spiegelman BM. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes & development 1994; 8: 1224-1234.
4. Michalik L, Desvergne B, Dreyer C, Gavillet M, Laurini RN, Wahli W. PPAR expression and function during vertebrate development. The International journal of developmental biology 2002; 46: 105-114.
5. Mao-Qiang M, Fowler AJ, Schmuth M, Lau P, Chang S, Brown BE et al. Peroxisome-proliferator-activated receptor (PPAR)-gamma activation stimulates keratinocyte differentiation. J Invest Dermatol 2004; 123: 305-312.
6. Sarraf P, Mueller E, Jones D, King FJ, DeAngelo DJ, Partridge JB et al. Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nature medicine 1998; 4: 1046-1052.
7. Saez E, Tontonoz P, Nelson MC, Alvarez JG, Ming UT, Baird SM et al. Activators of the nuclear receptor PPARgamma enhance colon polyp formation. Nature medicine 1998; 4: 1058-1061.
8. Shappell SB, Gupta RA, Manning S, Whitehead R, Boeglin WE, Schneider C et al. 15S-Hydroxyeicosatetraenoic acid activates peroxisome proliferator- activated receptor gamma and inhibits proliferation in PC3 prostate carcinoma cells. Cancer research 2001; 61: 497-503.
9. Hsi LC, Wilson LC, Eling TE. Opposing effects of 15-lipoxygenase-1 and-2 metabolites on MAPK signaling in prostate. Alteration in peroxisome proliferator-activated receptor gamma. J Biol Chem 2002; 277: 40549-40556.
10. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 2000; 18: 621-663.
11. Michalik L, Desvergne B, Wahli W. Peroxisome-proliferator-activated receptors and cancers: complex stories. Nature reviews 2004; 4: 61-70.
12. Mueller E, Smith M, Sarraf P, Kroll T, Aiyer A, Kaufman DS et al. Effects of ligand activation of peroxisome proliferator-activated receptor gamma in human prostate cancer. Proceedings of the National Academy of Sciences of the United States of America 2000; 97: 10990-10995.
13. Hisatake JI, Ikezoe T, Carey M, Holden S, Tomoyasu S, Koeffler HP. Down-Regulation of prostate-specific antigen expression by ligands for peroxisome proliferator-activated receptor gamma in human prostate cancer. Cancer research 2000; 60: 5494-5498.
14. Smith MR, Kantoff PW. Peroxisome proliferator-activated receptor gamma (PPargamma) as a novel target for prostate cancer. Invest New Drugs 2002; 20: 195-200.
15. Li M, Jiang X, Liu D, Na Y, Gao GF, Xi Z. Autophagy protects LNCaP cells under androgen deprivation conditions. Autophagy 2008; 4: 54-60.
16. Chang CL, Liao JJ, Huang WP, Lee H. Lysophosphatidic acid inhibits serum deprivation-induced autophagy in human prostate cancer PC-3 cells. Autophagy 2007; 3: 268-270.
17. Cao C, Subhawong T, Albert JM, Kim KW, Geng L, Sekhar KR et al. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer research 2006; 66: 10040-10047.
18. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer research 2004; 64: 2270-2305.
19. Park JH, Walls JE, Galvez JJ, Kim M, Abate-Shen C, Shen MM et al. Prostatic intraepithelial neoplasia in genetically engineered mice. The American journal of pathology 2002; 161: 727-735.
20. Day KC, McCabe MT, Zhao X, Wang Y, Davis JN, Phillips J et al. Rescue of embryonic epithelium reveals that the homozygous deletion of the retinoblastoma gene confers growth factor independence and immortality but does not influence epithelial differentiation or tissue morphogenesis. J Biol Chem 2002; 277: 44475-44484.
21. Brockman JA, Gupta RA, Dubois RN. Activation of PPARgamma leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology 1998; 115: 1049-1055.
22. Munafo DB, Colombo MI. A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. Journal of cell science 2001; 114 (Pt 20): 3619-3629.
23. Zhang J, Fu M, Cui T, Xiong C, Xu K, Zhong W et al. Selective disruption of PPARgamma 2 impairs the development of adipose tissue and insulin sensitivity. Proceedings of the National Academy of Sciences of the United States of America 2004; 101: 10703-10708.
24. Yang MS, Ji KA, Jeon SB, Jin BK, Kim SU, Jou I et al. Interleukin-13 enhances cyclooxygenase-2 expression in activated rat brain microglia: implications for death of activated microglia. J Immunol 2006; 177: 1323-1329.
25. Jiang M, Shappell SB, Hayward SW. Approaches to understanding the importance and clinical implications of peroxisome proliferator-activated receptor gamma (PPARg) signaling in prostate cancer. J Cell Biochem 2004; 91: 513-527.
26. Pathak SK, Sharma RA, Steward WP, Mellon JK, Griffiths TR, Gescher AJ. Oxidative stress and cyclooxygenase activity in prostate carcinogenesis: targets for chemopreventive strategies. Eur J Cancer 2005; 41: 61-70.
27. Shappell SB, Boeglin WE, Olson SJ, Kasper S, Brash AR. 15-lipoxygenase-2 (15-LOX-2) is expressed in benign prostatic epithelium and reduced in prostate adenocarcinoma. The American journal of pathology 1999; 155: 235-245.
28. Shappell SB, Keeney DS, Zhang J, Page R, Olson SJ, Brash AR. 15-Lipoxygenase-2 expression in benign and neoplastic sebaceous glands and other cutaneous adnexa. J Invest Dermatol 2001; 117: 36-43.
29. Kirschenbaum A, Liotta DR, Yao S, Liu XH, Klausner AP, Unger P et al. Immunohistochemical localization of cyclooxygenase-1 and cyclooxygenase-2 in the human fetal and adult male reproductive tracts. The Journal of clinical endocrinology and metabolism 2000; 85: 3436-3441.
30. Bostwick DG, Meiers I, Shanks JH. Glutathione S-transferase: differential expression of alpha, mu, and pi isoenzymes in benign prostate, prostatic intraepithelial neoplasia, and prostatic adenocarcinoma. Human pathology 2007; 38: 1394-1401.
31. Keen HL, Ryan MJ, Beyer A, Mathur S, Scheetz TE, Gackle BD et al. Gene expression profiling of potential PPARgamma target genes in mouse aorta. Physiological genomics 2004; 18: 33-42.
32. Perera RJ, Marcusson EG, Koo S, Kang X, Kim Y, White N et al. Identification of novel PPARgamma target genes in primary human adipocytes. Gene 2006; 369: 90-99.
33. Hippert MM, O'Toole PS, Thorburn A. Autophagy in cancer: good, bad, or both? Cancer research 2006; 66: 9349-9351.
34. Bergmann A. Autophagy and cell death: no longer at odds. Cell 2007; 131: 1032-1034.
35. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer cell 2006; 10: 51-64.
36. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 2007; 8: 741-752.
37. Jones JR, Shelton KD, Guan Y, Breyer MD, Magnuson MA. Generation and functional confirmation of a conditional null PPARgamma allele in mice. Genesis 2002; 32: 134-137.
38. Wu X, Wu J, Huang J, Powell WC, Zhang J, Matusik RJ et al. Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissue-specific gene ablation. Mechanisms of development 2001; 101: 61-69.
39. Duan SZ, Ivashchenko CY, Russell MW, Milstone DS, Mortensen RM. Cardiomyocyte-specific knockout and agonist of peroxisome proliferator-activated receptor-gamma both induce cardiac hypertrophy in mice. Circulation research 2005; 97: 372-379.