MTORC1 enhancement of STIM1-mediated store-operated Ca2+ entry constrains tuberous sclerosis complex-related tumor development

Oncogene

Volumn 32, Issue 39, 2013, Pages 4702-4711

  Wang, J ^a,b   Peng, H ^a   Liu, J ^b   Sun, Q ^c   Chen, R ^a   Wang, Y ^a   Duan, J ^a   Li, C ^a   Li, B ^a   Jing, Y ^a   Chen, X ^a   Mao, Q ^d   Xu, K F ^d   Walker, C L ^e   Li, J ^f   Zhang, H ^a,d  

^a PEKING UNION MEDICAL COLLEGE   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

^d PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^e TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^f HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

calcium; mTORC1; STIM1; TSC; tumorigenesis

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; RAPAMYCIN; STROMAL INTERACTION MOLECULE 1;

ARTICLE; CALCIUM TRANSPORT; CARCINOGENESIS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; PRIORITY JOURNAL; STORE OPERATED CALCIUM ENTRY; TUBEROUS SCLEROSIS; TUMOR GROWTH; UPREGULATION;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL LINE; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; FIBROBLASTS; HUMANS; KIDNEY NEOPLASMS; LEIOMYOMA; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, NUDE; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS; TUMOR SUPPRESSOR PROTEINS; UTERINE NEOPLASMS;

MAMMALIA;

EID: 84884906813     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.481     Document Type: Article

References (50)

1. Crino PB, Nathanson KL, Henske EP. The tuberous sclerosis complex. N Engl J Med 2006; 355: 13451356.
2. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003; 13: 12591268.
3. Alessi DR, Pearce LR, Garcia-Martinez JM. New insights into mTOR signaling: mTORC2 and beyond. Sci Signal 2009; 2: pe27.
4. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012; 149: 274293.
5. Gough NR. Focus issue: TOR signaling, a tale of two complexes. Sci Signal 2012; 5: eg4.
6. Yecies JL, Manning BD. Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res 2011; 71: 28152820.
7. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011; 13: 132141.
8. Roczniak-Ferguson A, Petit CS, Froehlich F, Qian S, Ky J, Angarola B et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal 2012; 5: ra42.
9. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004; 18: 19261945.
10. Yang Q, Guan K-L. Expanding mTOR signaling. Cell Res 2007; 17: 666681.
11. Davies DM, de Vries PJ, Johnson SR, McCartney DL, Cox JA, Serra AL et al. Sirolimus therapy for angiomyolipoma in tuberous sclerosis and sporadic lymphangioleiomyomatosis: a phase 2 trial. Clin Cancer Res 2011; 17: 40714081.
12. Bissler JJ, McCormack FX, Young LR, Elwing JM, Chuck G, Leonard JM et al. Sirolimus for angiomyolipoma in tuberous sclerosis complex or lymphangioleiomyomatosis. N Engl J Med 2008; 358: 140151.
13. Choo AY, Blenis J. Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 2009; 8: 567572.
14. Zhang H, Bajraszewski N, Wu E, Wang H, Moseman AP, Dabora SL et al. PDGFRs are critical for PI3K/Akt activation and negatively regulated by mTOR. J Clin Invest 2007; 117: 730738.
15. Shah OJ, Wang Z, Hunter T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr Biol 2004; 14: 16501656.
16. Hsu PP, Kang SA, Rameseder J, Zhang Y, Ottina KA, Lim D et al. The mTORregulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 2011; 332: 13171322.
17. Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villen J et al. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 2011; 332: 13221326.
18. Harrington LS, Findlay GM, Lamb RF. Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem Sci 2005; 30: 3542.
19. Clapham DE. Calcium signaling. Cell 2007; 131: 10471058.
20. Parekh AB, Putney Jr JW. Store-operated calcium channels. Physiol Rev 2005; 85: 757810.
21. Lewis RS. The molecular choreography of a store-operated calcium channel. Nature 2007; 446: 284287.
22. Derler I, Madl J, Schutz G, Romanin C. Structure, regulation and biophysics of I(CRAC), STIM/Orai1. Adv Exp Med Biol 2012; 740: 383410.
23. Engh A, Somasundaram A, Prakriya M. Permeation and gating mechanisms in store-operated CRAC channels. Front Biosci 2012; 17: 16131626.
24. Feske S, Picard C, Fischer A. Immunodeficiency due to mutations in ORAI1 and STIM1. Clin Immunol 2010; 135: 169182.
25. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting Ca2 transport. Nat Rev Cancer 2007; 7: 519530.
26. Roderick HL, Cook SJ. Ca2 signalling checkpoints in cancer: remodelling Ca2 for cancer cell proliferation and survival. Nat Rev Cancer 2008; 8: 361375.
27. Feske S. CRAC channelopathies. Pflugers Arch 2010; 460: 417435.
28. Yang S, Zhang JJ, Orai1 Huang XY. STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 2009; 15: 124134.
29. Feng M, Grice DM, Faddy HM, Nguyen N, Leitch S, Wang Y et al. Store-independent activation of orai1 by SPCA2 in mammary tumors. Cell 2010; 143: 8498.
30. El Boustany C, Bidaux G, Enfissi A, Delcourt P, Prevarskaya N, Capiod T. Capacitative calcium entry and transient receptor potential canonical 6 expression control human hepatoma cell proliferation. Hepatology 2008; 47: 20682077.
31. Chen YF, Chiu WT, Chen YT, Lin PY, Huang HJ, Chou CY et al. Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc Natl Acad Sci USA 2011; 108: 1522515230.
32. Zhang H, Cicchetti G, Onda H, Koon HB, Asrican K, Bajraszewski N et al. Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR. J Clin Invest 2003; 112: 12231233.
33. El-Hashemite N, Zhang H, Walker V, Hoffmeister KM, Kwiatkowski DJ. Perturbed IFN-gamma-Jak-signal transducers and activators of transcription signaling in tuberous sclerosis mouse models: synergistic effects of rapamycin-IFN-gamma treatment. Cancer Res 2004; 64: 34363443.
34. Pollizzi K, Malinowska-Kolodziej I, Doughty C, Betz C, Ma J, Goto J et al. A hypomorphic allele of Tsc2 highlights the role of TSC1/TSC2 in signaling to AKT and models mild human TSC2 alleles. Hum Mol Genet 2009; 18: 23782387.
35. Lee L, Sudentas P, Donohue B, Asrican K, Worku A, Walker V et al. Efficacy of a rapamycin analog (CCI-779) and IFN-gamma in tuberous sclerosis mouse models. Genes Chromosomes Cancer 2005; 42: 213227.
36. Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 2006; 16: 20732079.
37. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S et al. STIM1 carboxylterminus activates native SOC, Icrac and TRPC1 channels. Nat Cell Biol 2006; 8: 10031010.
38. Roskoski Jr R. Vascular endothelial growth factor (VEGF) signaling in tumor progression. Crit Rev Oncol Hematol 2007; 62: 179213.
39. Howe SR, Gottardis MM, Everitt JI, Goldsworthy TL, Wolf DC, Walker C. Rodent model of reproductive tract leiomyomata. Establishment and characterization of tumor-derived cell lines. Am J Pathol 1995; 146: 15681579.
40. Kobayashi T, Hirayama Y, Kobayashi E, Kubo Y, Hino O. A germline insertion in the tuberous sclerosis (Tsc2) gene gives rise to the Eker rat model of dominantly inherited cancer. Nat Genet 1995; 9: 7074.
41. Ma J, Meng Y, Kwiatkowski DJ, Chen X, Peng H, Sun Q et al. Mammalian target of rapamycin regulates murine and human cell differentiation through STAT3/p63/Jagged/Notch cascade. J Clin Invest 2010; 120: 103114.
42. Guertin DA, Sabatini DM. Defining the role of mTOR in cancer. Cancer Cell 2007; 12: 922.
43. Ogawa A, Firth AL, Smith KA, Maliakal MV, Yuan JX. PDGF enhances store-operated Ca2 entry by upregulating STIM1/Orai1 via activation of Akt/mTOR in human pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 2012; 302: C405C411.
44. Sabbioni S, Barbanti-Brodano G, Croce CM, Negrini M. GOK: a gene at 11p15 involved in rhabdomyosarcoma and rhabdoid tumor development. Cancer Res 1997; 57: 44934497.
45. Suyama E, Wadhwa R, Kaur K, Miyagishi M, Kaul SC, Kawasaki H et al. Identification of metastasis-related genes in a mouse model using a library of randomized ribozymes. J Biol Chem 2004; 279: 3808338086.
46. Flourakis M, Lehenkyi V, Beck B, Raphael M, Vandenberghe M, Abeele FV et al. Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis 2010; 1: e75.
47. Gilio K, van Kruchten R, Braun A, Berna-Erro A, Feijge MA, Stegner D et al. Roles of platelet STIM1 and Orai1 in glycoprotein VI-and thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem 2010; 285: 2362923638.
48. Grosse J, Braun A, Varga-Szabo D, Beyersdorf N, Schneider B, Zeitlmann L et al. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest 2007; 117: 35403550.
49. El-Hashemite N, Walker V, Zhang H, Kwiatkowski DJ. Loss of Tsc1 or Tsc2 induces vascular endothelial growth factor production through mammalian target of rapamycin. Cancer Res 2003; 63: 51735177.
50. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X et al. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci USA 2011; 108: 41294134.