The physiology and pathophysiology of rapamycin resistance: Implications for cancer

Cell Cycle

Volumn 10, Issue 7, 2011, Pages 1050-1058

  Gruppuso, Philip A ^a   Boylan, Joan M ^a   Sanders, Jennifer A ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Cell cycle; Cell signaling; Gene expression; Mammalian target of rapamycin; mTOR; Protein phosphorylation; Translation control

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; RAPAMYCIN; RAPAMYCIN DERIVATIVE; S6 KINASE;

ACUTE GRANULOCYTIC LEUKEMIA; ANTINEOPLASTIC ACTIVITY; CANCER CHEMOTHERAPY; CANCER RESISTANCE; DNA SYNTHESIS INHIBITION; DOSE RESPONSE; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GRAFT VERSUS HOST REACTION; HUMAN; IC 50; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY CANCER; LIVER CELL; LIVER DEVELOPMENT; LIVER REGENERATION; MICROARRAY ANALYSIS; NONHUMAN; PANCREAS CANCER; PERIVASCULAR EPITHELIOID CELL TUMOR; PROTEIN PROTEIN INTERACTION; REVIEW; SINGLE DRUG DOSE; TRANSCRIPTION REGULATION;

MAMMALIA; RATTUS;

EID: 79953668112     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.7.15230     Document Type: Review

References (59)

1. Vezina C, Kudelski A, Sehgal SN. Rapamycin (AY- 22,989), a new antifungal antibiotic. I. Taxonomy of the producing streptomycete and isolation of the active principle. J Antibiot (Tokyo) 1975; 28:721-6.
2. Eng CP, Sehgal SN, Vezina C. Activity of rapamycin (AY-22,989) against transplanted tumors. J Antibiot (Tokyo) 1984; 37:1231-7.
3. Siekierka JJ, Hung SH, Poe M, Lin CS, Sigal NH. A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature 1989; 341:755-7. (Pubitemid 19260892)
4. Heitman J, Movva NR, Hall MN. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 1991; 253:905-9. (Pubitemid 21917235)
5. Sabitini DM, Erdjument-Bromage H, Liu M, Tempst P, Snyder SH. RAFT1: A mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 1994; 78:35-43. (Pubitemid 24228298)
6. Abraham RT. Identification of TOR signaling complexes: More TORC for the cell growth engine. Cell 2002; 111:9-12.
7. Guertin DA, Sabatini DM. The pharmacology of mTOR inhibition. Sci Signal 2009; 2:24.
8. Gingras AC, Raught B, Sonenberg N. Regulation of translation initiation by FRAP/mTOR. Genes Dev 2001; 15:807-26. (Pubitemid 32295062)
9. 1-phase progression in eukaryotic cells. Prog Cell Cycle Res 1995; 1:53-71.
10. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett 2010; 584:1287-95.
11. Castedo M, Ferri KF, Kroemer G. Mammalian target of rapamycin (mTOR): pro- and anti-apoptotic. Cell Death Differ 2002; 9:99-100. (Pubitemid 34144768)
12. Polak P, Hall MN. mTOR and the control of whole body metabolism. Curr Opin Cell Biol 2009; 21:209-18.
13. Huang S, Houghton PJ. Targeting mTOR signaling for cancer therapy. Curr Opin Pharmacol 2003; 3:371-7. (Pubitemid 36908940)
14. Hidalgo M, Rowinsky EK. The rapamycin-sensitive signal transduction pathway as a target for cancer therapy. Oncogene 2000; 19:6680-6. (Pubitemid 32197708)
15. Sabatini DM. mTOR and cancer: insights into a complex relationship. Nat Rev Cancer 2006; 6:729-34.
16. Hosoi H, Dilling MB, Liu LN, Danks JK, Shikata T, Sekulic A, et al. Studies on the mechanism of resistance to rapamycin in human cancer cells. Mol Pharmacol 1998; 54:815-24. (Pubitemid 28523173)
17. Huang S, Bjornsti MA, Houghton PJ. Rapamycins: mechanism of action and cellular resistance. Cancer Biol Ther 2003; 2:222-32.
18. Choo AY, Blenis J. Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 2009; 8:567-72.
19. Perl AE, Kasner MT, Tsai DE, Vogl DT, Loren AW, Schuster SJ, et al. A phase I study of the mammalian target of rapamycin inhibitor sirolimus and MEC chemotherapy in relapsed and refractory acute myelogenous leukemia. Clin Cancer Res 2009; 15:6732-9.
20. Rini BI. New strategies in kidney cancer: therapeutic advances through understanding the molecular basis of response and resistance. Clin Cancer Res 2010; 16:1348-54.
21. Wolpin BM, Hezel AF, Abrams T, Blaszkowsky LS, Meyerhardt JA, Chan JA, et al. Oral mTOR inhibitor everolimus in patients with gemcitabine-refractory metastatic pancreatic cancer. J Clin Oncol 2009; 27:193-8.
22. Subbiah V, Trent JC, Kurzrock R. Resistance to mammalian target of rapamycin inhibitor therapy in perivascular epithelioid cell tumors. J Clin Oncol 2010; 28:415.
23. Treiber G. mTOR inhibitors for hepatocellular cancer: a forward-moving target. Expert Rev Anticancer Ther 2009; 9:247-61.
24. Shi Y, Sharma A, Wu H, Lichtenstein A, Gera J. Cyclin D1 and c-myc internal ribosome entry site (IRES)-dependent translation is regulated by AKT activity and enhanced by rapamycin through a p38 MAPK- and Erk-dependent parthway. J Biol Chem 2005; 280:10964-73. (Pubitemid 40418398)
25. Boylan JM, Anand P, Gruppuso PA. Ribosomal protein S6 phosphorylation and function during late gestation liver development in the rat. J Biol Chem 2001; 276:44457-63.
26. Nemenoff RA, Price DJ, Mendelsohn MJ, Carter EA, Avruch J. An S6 kinase activated during liver regeneration is related to the insulin-stimulated S6 kinase in H4 hepatoma cells. J Biol Chem 1988; 263:19455-60. (Pubitemid 19016423)
27. Francavilla A, Starzl TE, Scotti C, Carrieri G, Azzarone A, Zeng QH, et al. Inhibition of liver, kidney and intestine regeneration by rapamycin. Transplantation 1992; 53:496-8.
28. Palmes D, Zibert A, Budny T, Bahde R, Minin E, Kebschull L, et al. Impact of rapamycin on liver regeneration. Virchows Arch 2008; 452:545-57.
29. Sanders JA, Lakhani A, Phornphutkul C, Wu KY, Gruppuso PA. The effect of rapamycin on DNA synthesis in multiple tissues from late gestation fetal and postnatal rats. Am J Physiol Cell Physiol 2008; 295:406-13.
30. Anand P, Gruppuso PA. Rapamycin inhibits liver growth during refeeding in rats via control of ribosomal protein translation but not cap-dependent translation initiation. J Nutr 2006; 136:27-33. (Pubitemid 43156480)
31. Jiang YP, Ballou LM, Lin RZ. Rapamycin-insensitive regulation of 4E-BP1 in regenerating rat liver. J Biol Chem 2001; 276:10943-51. (Pubitemid 38089273)
32. Gruppuso PA, Tsai SW, Boylan JM, Sanders JA. Hepatic translation control in the late-gestation fetal rat. Am J Physiol Regul Integr Comp Physiol 2008; 295:558-67.
33. Jimenez RH, Boylan JM, Lee JS, Francesconi M, Castellani G, Sanders JA, et al. Rapamycin response in tumorigenic and non-tumorigenic hepatic cell lines. PLoS ONE 2009; 4:7373.
34. Pitot HC, Peraino C, Morse PA Jr, Potter VR. Hepatomas in tissue culture compared with adapting liver in vivo. Natl Cancer Inst Monogr 1964; 13:229-45.
35. Tsao MS, Smith JD, Nelson KG, Grisham JW. A diploid epithelial cell line from normal adult rat liver with phenotypic properties of 'oval' cells. Exp Cell Res 1984; 154:38-52.
36. Lee LW, Tsao MS, Grisham JW, Smith GJ. Emergence of neoplastic transformants spontaneously or after exposure to N-methyl-N′-nitro-N- nitrosoguanidine in populations of rat liver epithelial cells cultured under selective and nonselective conditions. Am J Pathol 1989; 135:63-71. (Pubitemid 19228991)
37. Hixson DC, McEntire KD, Obrink B. Alterations in the expression of a hepatocyte cell adhesion molecule by transplantable rat hepatocellular carcinomas. Cancer Res 1985; 45:3742-9. (Pubitemid 15226453)
38. Hixson DC, Brown J, McBride AC, Affigne S. Differentiation status of rat ductal cells and ethionine-induced hepatic carcinomas defined with surface-reactive monoclonal antibodies. Exp Mol Pathol 2000; 68:152-69. (Pubitemid 30337516)
39. Kip1 cyclin-dependent kinase inhibitor prevented by rapamycin. Nature 1994; 372:570-3.
40. kip during mitosis in BALB/c 3T3 cells. Cell Growth Differ 1995; 6:1199-205.
41. Barata JT, Cardoso AA, Nadler LM, Boussiotis VA. Interleukin-7 promotes survival and cell cycle progression of T-cell acute lymphoblastic leukemia cells by downregulating the cyclin-dependent kinase inhibitor p27(kip1). Blood 2001; 98:1524-31.
42. Kip1. Mol Cell Biol 1996; 16:6744-51.
43. Shapira M, Kakiashvili E, Rosenberg T, Hershko DD. The mTOR inhibitor rapamycin downregulates the expression of the ubiquitin ligase subunit Skp2 in breast cancer cells. Breast Cancer Res 2006; 8:46.
44. Rosner M, Freilinger A, Hengstschlager M. The tuberous sclerosis genes and regulation of the cyclin-dependent kinase inhibitor p27. Mutat Res 2006; 613:10-6. (Pubitemid 44382645)
45. 1 cell cycle arrest via the control of p27(Kip1) expression. Cell Cycle 2010; 9:3933-44.
46. Hong F, Larrea MD, Doughty C, Kwiatkowski DJ, Squillace R, Slingerland JM. mTOR-raptor binds and activates SGK1 to regulate p27 phosphorylation. Mol Cell 2008; 30:701-11. (Pubitemid 351815130)
47. Garcia-Martinez JM, Alessi DR. mTOR complex 2 (mTORC2) controls hydrophobic motif phosphorylation and activation of serum- and glucocorticoid-induced protein kinase 1 (SGK1). Biochem J 2008; 416:375-85.
48. 1 to S transition is mediated by effects on cyclin D1 mRNA and protein stability. J Biol Chem 1998; 273:14424-9.
49. Averous J, Fonseca BD, Proud CG. Regulation of cyclin D1 expression by mTORC1 signaling requires eukaryotic initiation factor 4E-binding protein 1. Oncogene 2008; 27:1106-13. (Pubitemid 351253179)
50. Pallet N, Thervet E, Le Corre D, Knebelmann B, Nusbaum P, Tomkiewicz C, et al. Rapamycin inhibits human renal epithelial cell proliferation: effect on cyclin D3 mRNA expression and stability. Kidney Int 2005; 67:2422-33. (Pubitemid 41623406)
51. Hleb M, Murphy S, Wagner EF, Hanna NN, Sharma N, Park J, et al. Evidence for cyclin D3 as a novel target of rapamycin in human T lymphocytes. J Biol Chem 2004; 279:31948-55. (Pubitemid 39037869)
52. Decker T, Hipp S, Ringshausen I, Bogner C, Oelsner M, Schneller F, et al. Rapamycin-induced G1 arrest in cycling B-CLL cells is associated with reduced expression of cyclin D3, cyclin E, cyclin A and survivin. Blood 2003; 101:278-85. (Pubitemid 36025919)
53. Jimenez RH, Lee JS, Francesconi M, Castellani G, Neretti N, Sanders JA, et al. Regulation of gene expression in hepatic cells by the mammalian Target of Rapamycin (mTOR). PLoS ONE 2010; 5:9084.
54. Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, et al. mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 2003; 23:8862-77. (Pubitemid 37433385)
55. Tsang CK, Liu H, Zheng XF. mTOR binds to the promoters of RNA polymerase I- and III-transcribed genes. Cell Cycle 2010; 9:953-7.
56. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007; 450:736-40. (Pubitemid 350207689)
57. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 2003; 34:267-73. (Pubitemid 36792858)
58. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102:15545-50. (Pubitemid 41528093)
59. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 2007; 12:9-22. (Pubitemid 47001784)