ITPR1 protects renal cancer cells against natural killer cells by inducing autophagy

Cancer Research

Volumn 74, Issue 23, 2014, Pages 6820-6832

  Messai, Yosra ^a   Noman, Muhammad Zaeem ^a   Hasmim, Meriem ^a   Janji, Bassam ^b   Tittarelli, Andrés ^a   Boutet, Marie ^a   Baud, Éronique ^c,d,e   Viry, Elodie ^b   Billot, Katy ^c,d,e   Nanbakhsh, Arash ^a   Safta, Thouraya Ben ^a   Richon, Catherine ^f   Ferlicot, Sophie ^g   Donnadieu, Emmanuel ^h   Couve, Sophie ^a   Gardie, Betty ^a   Orlucci, Florence ⁱ   Albiges, Laurence ^d   Thiery, Jerome ^a   Olive, Daniel ⁱ   Escudier, Bernard ^d   Chouaib, Salem ^a   more..

^a Unite Inst Natl de la S et de la Rech Med U753 Immunol des Tumeurs Humaines   (France)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^c INSERM   (France)

^d CNRS   (France)

^e LIPADE   (France)

^f Universite Sorbonne Paris Cite   (France)

^g INSTITUT GUSTAVE ROUSSY   (France)

^h UNIVERSITÉ PARIS SACLAY   (France)

ⁱ INSTITUT COCHIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; GRANZYME B; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR TYPE 1; UNCLASSIFIED DRUG; VON HIPPEL LINDAU PROTEIN; APOPTOSIS REGULATORY PROTEIN; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BECN1 PROTEIN, HUMAN; ENDOTHELIAL PAS DOMAIN-CONTAINING PROTEIN 1; ITPR1 PROTEIN, HUMAN; MEMBRANE PROTEIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; KIDNEY CARCINOMA; MAJOR CLINICAL STUDY; MOUSE; NATURAL KILLER CELL; NONHUMAN; RENAL CANCER CELL LINE; TUMOR CELL DESTRUCTION; TUMOR REGRESSION; ANIMAL; BAGG ALBINO MOUSE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KIDNEY TUMOR; METABOLISM; TUMOR CELL LINE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; KIDNEY NEOPLASMS; KILLER CELLS, NATURAL; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; TRANSCRIPTOME;

EID: 84917705638     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0303     Document Type: Article

References (50)

1. Gupta K, Miller JD, Li JZ, Russell MW, Charbonneau C. Epidemiologic and socioeconomic burden of metastatic renal cell carcinoma (mRCC): a literature review. Cancer Treat Rev 2008;34:193-205.
2. Inman BA, Harrison MR, George DJ. Novel immunotherapeutic strategies in development for renal cell carcinoma. Eur Urol 2013; 63:881-9.
3. Albiges L, Oudard S, Negrier S, Caty A, Gravis G, Joly F, et al. Complete remission with tyrosine kinase inhibitors in renal cell carcinoma. J Clin Oncol 2012;30:482-7.
4. Coppin C, Le L, Porzsolt F, Wilt T. Targeted therapy for advanced renal cell carcinoma. Cochrane Database Syst Rev. 2008:CD006017.
5. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011;331:44-9.
6. Eckl J, Buchner A, Prinz PU, Riesenberg R, Siegert SI, Kammerer R, et al. Transcript signature predicts tissue NK cell content and defines renal cell carcinoma subgroups independent of TNM staging. J Mol Med (Berl) 2012;90:55-66.
7. Escudier B. Emerging immunotherapies for renal cell carcinoma. Ann Oncol 2012;23 Suppl):viii35 -40.
8. Iliopoulou EG, Kountourakis P, Karamouzis MV, Doufexis D, Ardavanis A, Baxevanis CN, et al. A phase I trial of adoptive transfer of allogeneic natural killer cells in patients with advanced non-small cell lung cancer. Cancer Immunol Immunother 2010;59:1781-9.
9. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002;295:2097-100.
10. Abe H, Kamai T. Recent advances in the treatment of metastatic renal cell carcinoma. Int J Urol. 2013;20:944-55.
11. Locatelli F, Pende D, Mingari MC, Bertaina A, Falco M, Moretta A, et al. Cellular and molecular basis of haploidentical hematopoietic stem cell transplantation in the successful treatment of high-risk leukemias: role of alloreactive NK cells. Front Immunol 2013;4:15.
12. Jemal A, Siegel R, Ward E, Murray T, Xu J, Smigal C, et al. Cancer statistics, 2006. CA Cancer J Clin 2006;56:106-30.
13. Kaelin WG Jr. The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res 2007;13:680s-684s.
14. Iliopoulos O, Kibel A, Gray S, KaelinWGJr. Tumour suppression by the human von Hippel-Lindau gene product. Nat Med 1995;1:822-6.
15. Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol 2003;23:9361-74.
16. Keith B, Johnson RS, Simon MC. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat Rev Cancer 2012;12:9-22.
17. Kaelin WG Jr. The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer 2008;8:865-73.
18. Kondo K, Kim WY, Lechpammer M, Kaelin WG Jr. Inhibition of HIF2alpha is sufficient to suppress pVHL-defective tumor growth. PLoS Biol 2003;1:E83.
19. Noman MZ, Buart S, Van Pelt J, Richon C, Hasmim M, Leleu N, et al. The cooperative induction of hypoxia-inducible factor-1 alpha and STAT3 during hypoxia induced an impairment of tumor susceptibility to CTL-mediated cell lysis. J Immunol 2009;182:3510-21.
20. HasmimM, Noman MZ, Lauriol J, Benlalam H, Mallavialle A, Rosselli F, et al. Hypoxia-dependent inhibition of tumor cell susceptibility to CTLmediated lysis involves NANOG induction in target cells. J Immunol 2011;187:4031-9.
21. Noman MZ, Messai Y, Carre T, Akalay I, Meron M, Janji B, et al. Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit Rev Immunol 2011;31: 357-77.
22. Murphy GP, Hrushesky WJ. A murine renal cell carcinoma. J Natl Cancer Inst 1973;50:1013-25.
23. Noman MZ, Janji B, Kaminska B, Van Moer K, Pierson S, Przanowski P, et al. Blocking hypoxia-induced autophagy in tumors restores cytotoxic T-cell activity and promotes regression. Cancer Res 2011;71: 5976-86.
24. Jacque E, Billot K, Authier H, Bordereaux D, Baud V. RelB inhibits cell proliferation and tumor growth through p53 transcriptional activation. Oncogene 2013;32:2661-9.
25. Thiery J, Walch M, Jensen DK, Martinvalet D, Lieberman J. Isolation of cytotoxic T cell and NK granules and purification of their effector proteins. Curr Protoc Cell Biol 2010;Chapter 3:Unit3.37.
26. Thiery J, Keefe D, Boulant S, Boucrot E, Walch M, Martinvalet D, et al. Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol 2011;12:770-7.
27. Baginska J, Viry E, Berchem G, Poli A, Noman MZ, van Moer K, et al. Granzyme B degradation by autophagy decreases tumor cell susceptibility to natural killer-mediated lysis under hypoxia. Proc Natl Acad Sci U S A 2013;110:17450-5.
28. Noman MZ, Buart S, Romero P, Ketari S, Janji B, Mari B, et al. Hypoxia-induciblemiR-210 regulates the susceptibility of tumor cells to lysis by cytotoxic T cells. Cancer Res 2012;72:4629-41.
29. Parys JB, Decuypere JP, Bultynck G. Role of the inositol 1,4,5-trisphosphate receptor/Ca2+-release channel in autophagy. Cell Commun Signaling 2012;10:17.
30. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-KuriyamaY. A novel bHLH-PAS factor with close sequence similarity to hypoxiainducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci U S A 1997;94:4273-8.
31. Abud EM, Maylor J, Undem C, Punjabi A, Zaiman AL, Myers AC, et al. Digoxin inhibits development of hypoxic pulmonary hypertension in mice. Proc Natl Acad Sci U S A 2012;109:1239-44.
32. Richard S, Gardie B, Couve S, Gad S. Von Hippel-Lindau: how a rare disease illuminates cancer biology. Semin Cancer Biol 2013;23: 26-37.
33. Raval RR, Lau KW, Tran MG, Sowter HM, Mandriota SJ, Li JL, et al. Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol 2005;25:5675-86.
34. Shen C, Beroukhim R, Schumacher SE, Zhou J, Chang M, Signoretti S, et al. Genetic and functional studies implicate HIF1alpha as a 14q kidney cancer suppressor gene. Cancer Discov 2011;1:222-35.
35. Koh MY, Powis G. Passing the baton: the HIF switch. Trends Biochem Sci 2012;37:364-72.
36. Perier A, Fregni G, Wittnebel S, Gad S, Allard M, Gervois N, et al. Mutations of the von Hippel-Lindau gene confer increased susceptibility to natural killer cells of clear-cell renal cell carcinoma. Oncogene 2011;30:2622-32.
37. Sarkar S, Germeraad WT, Rouschop KM, Steeghs EM, van Gelder M, Bos GM, et al. Hypoxia induced impairment of NK Cell cytotoxicity against multiple myeloma can be overcomeby IL-2 activation of theNK cells. PLoS One 2013;8:e64835.
38. Siemens DR, Hu N, Sheikhi AK, Chung E, Frederiksen LJ, Pross H, et al. Hypoxia increases tumor cell shedding of MHC class I chain-related molecule: role of nitric oxide. Cancer Res 2008;68:4746-53.
39. Adkins CE, Morris SA, De Smedt H, Sienaert I, Torok K, Taylor CW. Ca2+-calmodulin inhibits Ca2+ release mediated by type-1, -2 and -3 inositol trisphosphate receptors. Biochem J 2000;345:357-63.
40. Blondel O, Takeda J, Janssen H, Seino S, Bell GI. Sequence and functional characterization of a third inositol trisphosphate receptor subtype, IP3R-3, expressed in pancreatic islets, kidney, gastrointestinal tract, and other tissues. J Biol Chem 1993;268:11356-63.
41. Echevarria W, Leite MF, Guerra MT, Zipfel WR, Nathanson MH. Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat Cell Biol 2003;5:440-6.
42. Decuypere JP, Monaco G, Bultynck G, Missiaen L, De Smedt H, Parys JB. The IP(3) receptor-mitochondria connection in apoptosis and autophagy. Biochim Biophys Acta 2011;1813:1003-13.
43. Menrad H, Werno C, Schmid T, Copanaki E, Deller T, Dehne N, et al. Roles of hypoxia-inducible factor-1alpha (HIF-1alpha) versus HIF-2alpha in the survival of hepatocellular tumor spheroids. Hepatology 2010;51:2183-92.
44. Bohensky J, Terkhorn SP, Freeman TA, Adams CS, Garcia JA, Shapiro IM, et al. Regulation of autophagy in human and murine cartilage: hypoxia-inducible factor 2 suppresses chondrocyte autophagy. Arthritis Rheum 2009;60:1406-15.
45. Buchser WJ, Laskow TC, Pavlik PJ, Lin HM, Lotze MT. Cell-mediated autophagy promotes cancer cell survival. Cancer Res 2012; 72:2970-9.
46. Engedal N, Torgersen ML, Guldvik IJ, Barfeld SJ, Bakula D, Saetre F, et al. Modulation of intracellular calcium homeostasis blocks autophagosome formation. Autophagy 2013;9:1475-90.
47. Decuypere JP, Welkenhuyzen K, Luyten T, Ponsaerts R, Dewaele M, Molgo J, et al. Ins(1,4,5)P3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy 2011;7: 1472-89.
48. Jurkovicova D, Sedlakova B, Lacinova L, Kopacek J, Sulova Z, Sedlak J, et al. Hypoxia differently modulates gene expression of inositol 1,4,5-trisphosphate receptors in mouse kidney and HEK 293 cell line. Ann N Y Acad Sci 2008;1148:421-7.
49. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL, et al. Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 1998;92:2260-8.
50. Shibao K, Fiedler MJ, Nagata J, Minagawa N, Hirata K, Nakayama Y, et al. The type III inositol 1,4,5-trisphosphate receptor is associated with aggressiveness of colorectal carcinoma. Cell Calcium 2010;48: 315-23.