PPARγ activation induces autophagy in breast cancer cells

International Journal of Biochemistry and Cell Biology

Volumn 41, Issue 11, 2009, Pages 2334-2342

  Zhou, Jie ^a   Zhang, Wei ^a,c   Liang, Bing ^a,d   Casimiro, Mathew C ^a   Whitaker Menezes, Diana ^a   Wang, Min ^a   Lisanti, Michael P ^a,b   Lanza Jacoby, Susan ^a   Pestell, Richard G ^a,b   Wang, Chenguang ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^d NATIONAL CENTER OF BIOMEDICAL ANALYSIS   (China)

Author keywords

Autophagy; BNIP3; Breast cancer; HIF1 ; PPAR

Indexed keywords

ACRIDINE ORANGE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; MUTANT PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN BNIP3; ROSIGLITAZONE; SHORT HAIRPIN RNA; TROGLITAZONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; BNIP3 PROTEIN, HUMAN; CHROMAN DERIVATIVE; HIF1A PROTEIN, HUMAN; LIGAND; MEMBRANE PROTEIN; ONCOPROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GENE ACTIVATION; GENE EXPRESSION; GENOME ANALYSIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN INDUCTION; ANIMAL; BREAST TUMOR; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; PATHOLOGY; TUMOR CELL LINE; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; AUTOPHAGY; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMANS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIGANDS; MEMBRANE PROTEINS; MICE; PPAR GAMMA; PROTO-ONCOGENE PROTEINS; THIAZOLIDINEDIONES; TRANSCRIPTION, GENETIC;

EID: 70349298359     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2009.06.007     Document Type: Article

References (58)

1. Aiello A., Pandini G., Frasca F., Conte E., Murabito A., Sacco A., et al. Peroxisomal proliferator-activated receptor-gamma agonists induce partial reversion of epithelial-mesenchymal transition in anaplastic thyroid cancer cells. Endocrinology 147 (2006) 4463-4475
2. Azad M.B., Chen Y., Henson E.S., Cizeau J., McMillan-Ward E., Israels S.J., et al. Hypoxia induces autophagic cell death in apoptosis-competent cells through a mechanism involving BNIP3. Autophagy 4 (2008) 195-204
3. Bacon A.L., and Harris A.L. Hypoxia-inducible factors and hypoxic cell death in tumour physiology. Ann Med 36 (2004) 530-539
4. Bellot G., Garcia-Medina R., Gounon P., Chiche J., Roux D., Pouyssegur J., et al. Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol Cell Biol 29 (2009) 2570-2581
5. Boutros P.C., Moffat I.D., Franc M.A., Tijet N., Tuomisto J., Pohjanvirta R., et al. Dioxin-responsive AHRE-II gene battery: identification by phylogenetic footprinting. Biochem Biophys Res Commun 321 (2004) 707-715
6. Brockman J.A., Gupta R.A., and Dubois R.N. Activation of PPARgamma leads to inhibition of anchorage-independent growth of human colorectal cancer cells. Gastroenterology 115 (1998) 1049-1055
7. Bromberg J.F., Wrzeszczynska M.H., Devgan G., Zhao Y., Pestell R.G., Albanese C., et al. Stat3 as an oncogene. Cell 98 (1999) 295-303
8. Carew J.S., Nawrocki S.T., Kahue C.N., Zhang H., Yang C., Chung L., et al. Targeting autophagy augments the anticancer activity of the histone deacetylase inhibitor SAHA to overcome Bcr-Abl-mediated drug resistance. Blood 110 (2007) 313-322
9. Chawla A., Barak Y., Nagy L., Liao D., Tontonoz P., and Evans R.M. PPAR-gamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med 7 (2001) 48-52
10. Chen J.H., Enloe B.M., Weybright P., Campbell N., Dorfman D., Fletcher C.D., et al. Biochemical correlates of thiazolidinedione-induced adipocyte differentiation by high-resolution magic angle spinning NMR spectroscopy. Magn Reson Med 48 (2002) 602-610
11. Clay C.E., Monjazeb A., Thorburn J., Chilton F.H., and High K.P. 15-Deoxy-delta(12,14)-prostaglandin J(2)-induced apoptosis does not require PPARgamma in breast cancer cells. J Lipid Res 43 (2002) 1818-1828
12. Clay C.E., Namen A.M., Atsumi G., Willingham M.C., High K.P., Kute T.E., et al. Influence of J series prostaglandins on apoptosis and tumorigenesis of breast cancer cells. Carcinogenesis 20 (1999) 1905-1911
13. Cosse J.P., and Michiels C. Tumour hypoxia affects the responsiveness of cancer cells to chemotherapy and promotes cancer progression. Anticancer Agents Med Chem 8 (2008) 790-797
14. Elstner E., Muller C., Koshizuka K., Williamson E.A., Park D., Asou H., et al. Ligands for peroxisome proliferator-activated receptorγ and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc Natl Acad Sci U S A 95 (1998) 8806-8811
15. Elstner E., Muller C., Koshizuka K., Williamson E.A., Park D., Asou H., et al. Ligands for peroxisome proliferator-activated receptorgamma and retinoic acid receptor inhibit growth and induce apoptosis of human breast cancer cells in vitro and in BNX mice. Proc Natl Acad Sci U S A 95 (1998) 8806-8811
16. Girnun G.D., Chen L., Silvaggi J., Drapkin R., Chirieac L.R., Padera R.F., et al. Regression of drug-resistant lung cancer by the combination of rosiglitazone and carboplatin. Clin Cancer Res 14 (2008) 6478-6486
17. Girnun G.D., Naseri E., Vafai S.B., Qu L., Szwaya J.D., Bronson R., et al. Synergy between PPARgamma ligands and platinum-based drugs in cancer. Cancer Cell 11 (2007) 395-406
18. Hippert M.M., O'Toole P.S., and Thorburn A. Autophagy in cancer: good, bad, or both?. Cancer Res 66 (2006) 9349-9351
19. Hirota K., Fukuda R., Takabuchi S., Kizaka-Kondoh S., Adachi T., Fukuda K., et al. Induction of hypoxia-inducible factor 1 activity by muscarinic acetylcholine receptor signaling. J Biol Chem 279 (2004) 41521-41528
20. Hoyer-Hansen M., Bastholm L., Mathiasen I.S., Elling F., and Jaattela M. Vitamin D analog EB1089 triggers dramatic lysosomal changes and Beclin 1-mediated autophagic cell death. Cell Death Differ 12 (2005) 1297-1309
21. Hrzenjak A., Kremser M.L., Strohmeier B., Moinfar F., Zatloukal K., and Denk H. SAHA induces caspase-independent, autophagic cell death of endometrial stromal sarcoma cells by influencing the mTOR pathway. J Pathol 216 (2008) 495-504
22. Ishida M., Sunamura M., Furukawa T., Akada M., Fujimura H., Shibuya E., et al. Elucidation of the relationship of BNIP3 expression to gemcitabine chemosensitivity and prognosis. World J Gastroenterol 13 (2007) 4593-4597
23. Kato M., Nagaya T., Fujieda M., Saito K., Yoshida J., and Seo H. Expression of PPARgamma and its ligand-dependent growth inhibition in human brain tumor cell lines. Jpn J Cancer Res 93 (2002) 660-666
24. Lang S.A., Moser C., Gaumann A., Klein D., Glockzin G., Popp F.C., et al. Targeting heat shock protein 90 in pancreatic cancer impairs insulin-like growth factor-I receptor signaling, disrupts an interleukin-6/signal-transducer and activator of transcription 3/hypoxia-inducible factor-1alpha autocrine loop, and reduces orthotopic tumor growth. Clin Cancer Res 13 (2007) 6459-6468
25. Lee R.J., Albanese C., Stenger R.J., Watanabe G., Inghirami G., Haines III G.K., et al. pp60(v-src) induction of cyclin D1 requires collaborative interactions between the extracellular signal-regulated kinase, p38, and Jun kinase pathways. A role for cAMP response element-binding protein and activating transcription factor-2 in pp60(v-src) signaling in breast cancer cells. J Biol Chem 274 (1999) 7341-7350
26. Lefebvre A.M., Chen I., Desreumaux P., Najib J., Fruchart J.C., Geboes K., et al. Activation of the peroxisome proliferator-activated receptor gamma promotes the development of colon tumors in C57BL/6J-APCMin/+ mice. Nat Med 4 (1998) 1053-1057
27. Lu J., Imamura K., Nomura S., Mafune K., Nakajima A., Kadowaki T., et al. Chemopreventive effect of peroxisome proliferator-activated receptor gamma on gastric carcinogenesis in mice. Cancer Res 65 (2005) 4769-4774
28. Martelli M.L., Iuliano R., Le Pera I., Sama I., Monaco C., Cammarota S., et al. Inhibitory effects of peroxisome poliferator-activated receptor gamma on thyroid carcinoma cell growth. J Clin Endocrinol Metab 87 (2002) 4728-4735
29. Matthiessen M.W., Pedersen G., Albrektsen T., Adamsen S., Fleckner J., and Brynskov J. Peroxisome proliferator-activated receptor expression and activation in normal human colonic epithelial cells and tubular adenomas. Scand J Gastroenterol 40 (2005) 198-205
30. Mehta R.G., Williamson E., Patel M.K., and Koeffler H.P. A ligand of peroxisome proliferator-activated receptor gamma, retinoids, and prevention of preneoplastic mammary lesions. J Natl Cancer Inst 92 (2000) 418-423
31. Mody M., Dharker N., Bloomston M., Wang P.S., Chou F.S., Glickman T.S., et al. Rosiglitazone sensitizes MDA-MB-231 breast cancer cells to anti-tumour effects of tumour necrosis factor-alpha, CH11 and CYC202. Endocr Relat Cancer 14 (2007) 305-315
32. Morote-Garcia J.C., Rosenberger P., Kuhlicke J., and Eltzschig H.K. HIF-1-dependent repression of adenosine kinase attenuates hypoxia-induced vascular leak. Blood 111 (2008) 5571-5580
33. Mueller E., Sarraf P., Tontonoz P., Evans R.M., Martin K.J., Zhang M., et al. Terminal differentiation of human breast cancer through PPARγ. Mol Cell 1 (1998) 465-470
34. Neumeister P., Pixley F.J., Xiong Y., Xie H., Wu K., Ashton A., et al. Cyclin D1 governs adhesion and motility of macrophages. Mol Biol Cell 14 (2003) 2005-2015
35. Nicol C.J., Yoon M., Ward J.M., Yamashita M., Fukamachi K., Peters J.M., et al. PPARgamma influences susceptibility to DMBA-induced mammary, ovarian and skin carcinogenesis. Carcinogenesis 25 (2004) 1747-1755
36. Nwankwo J.O., and Robbins M.E. Peroxisome proliferator-activated receptor-gamma expression in human malignant and normal brain, breast and prostate-derived cells. Prostaglandins Leukot Essent Fatty Acids 64 (2001) 241-245
37. Peraza M.A., Burdick A.D., Marin H.E., Gonzalez F.J., and Peters J.M. The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR). Toxicol Sci 90 (2006) 269-295
38. Pighetti G.M., Novosad W., Nicholson C., Hitt D.C., Hansens C., Hollingsworth A.B., et al. Therapeutic treatment of DMBA-induced mammary tumors with PPAR ligands. Anticancer Res 21 (2001) 825-829
39. Pignatelli M., Cortes-Canteli M., Lai C., Santos A., and Perez-Castillo A. The peroxisome proliferator-activated receptor gamma is an inhibitor of ErbBs activity in human breast cancer cells. J Cell Sci 114 (2001) 4117-4126
40. Renn S.C., Aubin-Horth N., and Hofmann H.A. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5 (2004) 42
41. Ricote M., Huang J., Fajas L., Li A., Welch J., Najib J., et al. Expression of the peroxisome proliferator-activated receptor gamma (PPARgamma) in human atherosclerosis and regulation in macrophages by colony stimulating factors and oxidized low density lipoprotein. Proc Natl Acad Sci U S A 95 (1998) 7614-7619
42. Rosen E.D., and Spiegelman B.M. PPARγ: a nuclear regulator of metabolism, differentiation, and cell growth. J Biol Chem 276 (2001) 37731-37734
43. Saez E., Rosenfeld J., Livolsi A., Olson P., Lombardo E., Nelson M., et al. PPAR gamma signaling exacerbates mammary gland tumor development. Genes Dev 18 (2004) 528-540
44. Saez E., Tontonoz P., Nelson M.C., Alvarez J.G., Ming U.T., Baird S.M., et al. Activators of the nuclear receptor PPARgamma enhance colon polyp formation. Nat Med 4 (1998) 1058-1061
45. Samaddar J.S., Gaddy V.T., Duplantier J., Thandavan S.P., Shah M., Smith M.J., et al. A role for macroautophagy in protection against 4-hydroxytamoxifen-induced cell death and the development of antiestrogen resistance. Mol Cancer Ther 7 (2008) 2977-2987
46. Sarraf P., Mueller E., Jones D., King F.J., DeAngelo D.J., Partridge J.B., et al. Differentiation and reversal of malignant changes in colon cancer through PPARgamma. Nat Med 4 (1998) 1046-1052
47. Sato T. A modified method for lead staining of thin sections. J Electron Microsc (Tokyo) 17 (1968) 158-159
48. Shimada T., Kojima K., Yoshiura K., Hiraishi H., and Terano A. Characteristics of the peroxisome proliferator activated receptor gamma (PPARgamma) ligand induced apoptosis in colon cancer cells. Gut 50 (2002) 658-664
49. Shintani T., and Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 306 (2004) 990-995
50. Suh N., Wang Y., Williams C.R., Risingsong R., Gilmer T., Willson T.M., et al. A new ligand for the peroxisome proliferator-activated receptor-gamma (PPAR-gamma), GW7845, inhibits rat mammary carcinogenesis. Cancer Res 59 (1999) 5671-5673
51. Tontonoz P., Hu E., and Spiegelman B.M. Stimulation of adipogenesis in fibroblasts by PPARγ2, a lipid-activated transcription factor. Cell 79 (1994) 1147-1156
52. Toyoda M., Takagi H., Horiguchi N., Kakizaki S., Sato K., Takayama H., et al. A ligand for peroxisome proliferator activated receptor gamma inhibits cell growth and induces apoptosis in human liver cancer cells. Gut 50 (2002) 563-567
53. Wang C., Fu M., D'Amico M., Albanese C., Zhou J.N., Brownlee M., et al. Inhibition of cellular proliferation through IkappaB kinase-independent and peroxisome proliferator-activated receptor gamma-dependent repression of cyclin D1. Mol Cell Biol 21 (2001) 3057-3070
54. Wang C., Pattabiraman N., Zhou J.N., Fu M., Sakamaki T., Albanese C., et al. Cyclin D1 repression of peroxisome proliferator-activated receptor gamma expression and transactivation. Mol Cell Biol 23 (2003) 6159-6173
55. Wang Y.L., Frauwirth K.A., Rangwala S.M., Lazar M.A., and Thompson C.B. Thiazolidinedione activation of peroxisome proliferator-activated receptor gamma can enhance mitochondrial potential and promote cell survival. J Biol Chem 277 (2002) 31781-31788
56. Yoshizawa K., Cioca D.P., Kawa S., Tanaka E., and Kiyosawa K. Peroxisome proliferator-activated receptor gamma ligand troglitazone induces cell cycle arrest and apoptosis of hepatocellular carcinoma cell lines. Cancer 95 (2002) 2243-2251
57. Yu H.N., Lee Y.R., Noh E.M., Lee K.S., Kim J.S., Song E.K., et al. Induction of G1 phase arrest and apoptosis in MDA-MB-231 breast cancer cells by troglitazone, a synthetic peroxisome proliferator-activated receptor gamma (PPARgamma) ligand. Cell Biol Int 32 (2008) 906-912
58. Yu S., Matsusue K., Kashireddy P., Cao W.-Q., Yeldandi V.V.A.A., Yeldandi M.Y., et al. Adipocyte-specific gene expression and adipogenic steatosis in the mouse liver due to peroxisome proliferator-activated receptor 1 (PPAR1) overexpression. J Biol Chem 278 (2003) 498-505