Human TSC-associated renal angiomyolipoma cells are hypersensitive to ER stress

American Journal of Physiology - Renal Physiology

Volumn 303, Issue 6, 2012, Pages

  Siroky, Brian J ^a   Yin, Hong ^a   Babcock, Justin T ^b   Lu, Lu ^a   Hellmann, Anna R ^a   Dixon, Bradley P ^a   Quilliam, Lawrence A ^b   Bissler, John J ^a  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiomyolipoma; ER stress; mTOR; TSC

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CASPASE 3; EVEROLIMUS; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; TUBERIN;

ARTICLE; AUTOPHAGY; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSTASIS; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; FAR WESTERN BLOTTING; GENE MUTATION; HUMAN; HUMAN CELL; HYPERSENSITIVITY; KIDNEY HEMANGIOMYOLIPOMA; MORBIDITY; MORTALITY; PRIORITY JOURNAL; TUBEROUS SCLEROSIS; TUMOR CELL;

EID: 84866360622     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00441.2011     Document Type: Article

References (41)

1. Babcock JT, Quilliam LA. Rheb/mTOR activation and regulation in cancer: novel treatment strategies beyond rapamycin. Curr Drug Targets.
2. Bissler JJ, McCormack FX, Young LR, Elwing JM, Chuck G, Leonard JM, Schmithorst VJ, Laor T, Brody AS, Bean J, Salisbury S, Franz DN. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med 358: 140-151, 2008.
3. Catley L, Weisberg E, Kiziltepe T, Tai YT, Hideshima T, Neri P, Tassone P, Atadja P, Chauhan D, Munshi NC, Anderson KC. Aggresome induction by proteasome inhibitor bortezomib and alpha-tubulin hyperacetylation by tubulin deacetylase (TDAC) inhibitor LBH589 are synergistic in myeloma cells. Blood 108: 3441-3449, 2006.
4. Cocciolone RA, Crotty KA, Andrews L, Haass NK, Moloney FJ. Multiple desmoplastic melanomas in Birt-Hogg-Dube syndrome and a proposed signaling link between folliculin, the mTOR pathway, and melanoma susceptibility. Arch Dermatol 146: 1316-1318.
5. Davenport EL, Moore HE, Dunlop AS, Sharp SY, Workman P, Morgan GJ, Davies FE. Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells. Blood 110: 2641-2649, 2007.
6. Davies DM, Johnson SR, Tattersfield AE, Kingswood JC, Cox JA, McCartney DL, Doyle T, Elmslie F, Saggar A, de Vries PJ, Sampson JR. Sirolimus therapy in tuberous sclerosis or sporadic lymphangioleiomyomatosis. N Engl J Med 358: 200-203, 2008.
7. Denton D, Nicolson S, Kumar S. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 19: 87-95, 2012.
8. Di Nardo A, Kramvis I, Cho N, Sadowski A, Meikle L, Kwiatkowski DJ, Sahin M. Tuberous sclerosis complex activity is required to control neuronal stress responses in an mTOR-dependent manner. J Neurosci 29: 5926-5937, 2009.
9. Fu W, Wu X, Li J, Mo Z, Yang Z, Huang W, Ding Q. Upregulation of GRP78 in renal cell carcinoma and its significance. Urology 75: 603-607.
10. Furukawa T, Duguid WP, Rosenberg L, Viallet J, Galloway DA, Tsao MS. Long-term culture and immortalization of epithelial cells from normal adult human pancreatic ducts transfected by the E6E7 gene of human papilloma virus 16. Am J Pathol 148: 1763-1770, 1996.
11. Gass JN, Gunn KE, Sriburi R, Brewer JW. Stressed-out B cells? Plasma-cell differentiation and the unfolded protein response. Trends Immunol 25: 17-24, 2004.
12. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 18: 1926-1945, 2004.
13. Henske EP, Neumann HP, Scheithauer BW, Herbst EW, Short MP, Kwiatkowski DJ. Loss of heterozygosity in the tuberous sclerosis (TSC2) region of chromosome band 16p13 occurs in sporadic as well as TSCassociated renal angiomyolipomas. Genes Chromosomes Cancer 13: 295-298, 1995.
14. Hideshima T, Mitsiades C, Akiyama M, Hayashi T, Chauhan D, Richardson P, Schlossman R, Podar K, Munshi NC, Mitsiades N, Anderson KC. Molecular mechanisms mediating antimyeloma activity of proteasome inhibitor PS-341. Blood 101: 1530-1534, 2003.
15. Hideshima T, Richardson P, Chauhan D, Palombella VJ, Elliott PJ, Adams J, Anderson KC. The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells. Cancer Res 61: 3071-3076, 2001.
16. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM. mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 30: 701-711, 2008.
17. Inagi R. Endoplasmic reticulum stress in the kidney as a novel mediator of kidney injury. Nephron Exp Nephrol 112: e1-9, 2009.
18. Kang YJ, Lu MK, Guan KL. The TSC1 and TSC2 tumor suppressors are required for proper ER stress response and protect cells from ER stressinduced apoptosis. Cell Death Differ 18: 133-144, 2011.
19. Lee DH, Goldberg AL. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8: 397-403, 1998.
20. Levine B, Yuan J. Autophagy in cell death: an innocent convict? J Clin Invest 115: 2679-2688, 2005.
21. Liu Y, Hangoc G, Campbell TB, Goodman M, Tao W, Pollok K, Srour EF, Broxmeyer HE. Identification of parameters required for efficient lentiviral vector transduction and engraftment of human cord blood CD34(+) NOD/SCID-repopulating cells. Exp Hematol 36: 947-956, 2008.
22. Mimnaugh EG, Xu W, Vos M, Yuan X, Isaacs JS, Bisht KS, Gius D, Neckers L. Simultaneous inhibition of hsp 90 and the proteasome promotes protein ubiquitination, causes endoplasmic reticulum-derived cytosolic vacuolization, and enhances antitumor activity. Mol Cancer Ther 3: 551-566, 2004.
23. Mimnaugh EG, Xu W, Vos M, Yuan X, Neckers L. Endoplasmic reticulum vacuolization and valosin-containing protein relocalization result from simultaneous hsp90 inhibition by geldanamycin and proteasome inhibition by velcade. Mol Cancer Res 4: 667-681, 2006.
24. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 3: 542-545, 2007.
25. Noda T, Ohsumi Y. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273: 3963-3966, 1998.
26. Ozcan U, Ozcan L, Yilmaz E, Duvel K, Sahin M, Manning BD, Hotamisligil GS. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol Cell 29: 541-551, 2008.
27. Parkhitko A, Myachina F, Morrison TA, Hindi KM, Auricchio N, Karbowniczek M, Wu JJ, Finkel T, Kwiatkowski DJ, Yu JJ, Henske EP. Tumorigenesis in tuberous sclerosis complex is autophagy and p62/ sequestosome 1 (SQSTM1)-dependent. Proc Natl Acad Sci USA 108: 12455-12460, 2011.
28. Qin L, Wang Z, Tao L, Wang Y. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 6: 239-247.
29. Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 32: 469-476, 2007.
30. Schleicher SM, Moretti L, Varki V, Lu B. Progress in the unraveling of the endoplasmic reticulum stress/autophagy pathway and cancer: implications for future therapeutic approaches. Drug Resist Updat 13: 79-86, 2010.
31. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 74: 739-789, 2005.
32. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P. Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187: 525-536, 2009.
33. Serra AL, Poster D, Kistler AD, Krauer F, Raina S, Young J, Rentsch KM, Spanaus KS, Senn O, Kristanto P, Scheffel H, Weishaupt D, Wuthrich RP. Sirolimus and kidney growth in autosomal dominant polycystic kidney disease. N Engl J Med 363: 820-829.
34. Shepherd CW, Gomez MR, Lie JT, Crowson CS. Causes of death in patients with tuberous sclerosis. Mayo Clin Proc 66: 792-796, 1991.
35. Siroky BJ, Yin H, Bissler JJ. Clinical and molecular insights into tuberous sclerosis complex renal disease. Pediatr Nephrol 26: 839-852, 2011.
36. Sunwoo JB, Chen Z, Dong G, Yeh N, Crowl Bancroft C, Sausville E, Adams J, Elliott P, Van Waes C. Novel proteasome inhibitor PS-341 inhibits activation of nuclear factor-kappa B, cell survival, tumor growth, and angiogenesis in squamous cell carcinoma. Clin Cancer Res 7: 1419-1428, 2001.
37. Tergaonkar V, Pando M, Vafa O, Wahl G, Verma I. p53 stabilization is decreased upon NFkappaB activation: a role for NFkappaB in acquisition of resistance to chemotherapy. Cancer Cell 1: 493-503, 2002.
38. Walz G, Budde K, Mannaa M, Nurnberger J, Wanner C, Sommerer C, Kunzendorf U, Banas B, Horl WH, Obermuller N, Arns W, Pavenstadt H, Gaedeke J, Buchert M, May C, Gschaidmeier H, Kramer S, Eckardt KU. Everolimus in patients with autosomal dominant polycystic kidney disease. N Engl J Med 363: 830-840.
39. Wang CY, Cusack JC Jr, Liu R, Baldwin AS Jr. Control of inducible chemoresistance: enhanced anti-tumor therapy through increased apoptosis by inhibition of NF-kappaB. Nat Med 5: 412-417, 1999.
40. Wek RC, Jiang HY, Anthony TG. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34: 7-11, 2006.
41. Yu J, Astrinidis A, Howard S, Henske EP. Estradiol and tamoxifen stimulate LAM-associated angiomyolipoma cell growth and activate both genomic and nongenomic signaling pathways. Am J Physiol Lung Cell Mol Physiol 286: L694-L700, 2004.