Cinacalcet inhibits neuroblastoma tumor growth and upregulates cancer-testis antigens

Oncotarget

Volumn 7, Issue 13, 2016, Pages 16112-16129

  Rodríguez Hernández, Carlos J ^a   Mateo Lozano, Silvia ^a   García, Marta ^a   Casalà, Carla ^a   Briansó, Ferran ^b   Castrejón, Nerea ^a   Rodríguez, Eva ^a   Suñol, Mariona ^a   Carcaboso, Angel M ^a   Lavarino, Cinzia ^a   Mora, Jaume ^a   De Torres, Carmen ^a  

^a HOSPITAL SANT JOAN DE DÉU   (Spain)

^b HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Calcium sensing receptor; Cancer testis antigens; Cinacalcet; Er stress; Neuroblastoma

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; CALCIUM SENSING RECEPTOR; CANCER TESTIS ANTIGEN; CINACALCET; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; PHOSPHOLIPASE C; PROTEIN P53; ANTINEOPLASTIC AGENT; CASR PROTEIN, HUMAN; MYCN PROTEIN, HUMAN; N MYC PROTO ONCOGENE PROTEIN; TUMOR ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CANCER INHIBITION; CELL CYCLE; CELL SURVIVAL; CONTROLLED STUDY; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; FEMALE; FIBROSIS; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; MYCN GENE; NEUROBLASTOMA; NEUROBLASTOMA CELL LINE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TRB3 GENE; TUMOR DIFFERENTIATION; TUMOR MICROENVIRONMENT; TUMOR XENOGRAFT; UPREGULATION; X CHROMOSOME; AGONISTS; ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; DRUG EFFECTS; DRUG SCREENING; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL PROLIFERATION; CINACALCET HYDROCHLORIDE; HUMANS; MICE; MICE, NUDE; N-MYC PROTO-ONCOGENE PROTEIN; NEUROBLASTOMA; RECEPTORS, CALCIUM-SENSING; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84971645660     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7448     Document Type: Article

References (50)

1. Cheung NK, Dyer MA. Neuroblastoma: developmental biology, cancer genomics and immunotherapy. Nat Rev Cancer. 2013; 13:397-411.
2. Maris JM. Recent advances in neuroblastoma. N Engl J Med. 2010; 362:2202-2211.
3. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM. Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science. 1984; 224:1121-1124.
4. Pugh TJ, Morozova O, Attiyeh EF, Asgharzadeh S, Wei JS, Auclair D, Carter SL, Cibulskis K, Hanna M, Kiezun A, Kim J, Lawrence MS, Lichenstein L, et al. The genetic landscape of high-risk neuroblastoma. Nat Genet. 2013; 45:279-284.
5. George RE, Sanda T, Hanna M, Fröhling S, Luther W 2nd, Zhang J, Ahn Y, Zhou W, London WB, McGrady P, Xue L, Zozulya S, Gregor VE, et al. Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature. 2008; 455:97597-97598.
6. Shimada H, Umehara S, Monobe Y, Hachitanda Y, Nakagawa A, Goto S, Gerbing RB, Stram DO, Lukens JN, Matthay KK. International neuroblastoma pathology classification for prognostic evaluation of patients with peripheral neuroblastic tumors: a report from the Children's Cancer Group. Cancer. 2001; 92:2451-2461.
7. Thiele CJ, Reynolds CP, Israel MA. Decreased expression of Nmyc precedes retinoic acidinduced morphological differentiation of human neuroblastoma. Nature. 1985; 313:404-406.
8. Janardhanan R, Banik NL, Ray SK. NMyc down regulation induced differentiation, early cell cycle exit, and apoptosis in human malignant neuroblastoma cells having wild type or mutant p53. Biochem Pharmacol. 2009; 78:1105-1114.
9. Påhlman S, Ruusala AI, Abrahamsson L, Mattsson ME, Esscher T. Retinoic acidinduced differentiation of cultured human neuroblastoma cells. Cell Differ. 1984; 14:135-144.
10. Hölzel M, Huang S, Koster J, Ora I, Lakeman A, Caron H, Nijkamp W, Xie J, Callens T, Asgharzadeh S, Seeger RC, Messiaen L, Versteeg R, Bernards R. NF1 is a tumor suppressor in neuroblastoma that determines retinoic acid response and disease outcome. Cell. 2010; 142:218-229.
11. Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, HaasKogan D, Gerbing RB, London WB, Villablanca JG. Longterm results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13cisretinoic acid. J Clin Oncol. 2009; 27:1007-1013.
12. Brown EM, Gamba G, Riccardi D, Lombardi M, Butters R, Kifor O, Sun A, Hediger MA, Lytton J, Hebert SC. Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid. Nature. 1993; 366:575-580.
13. Brennan SC, Thiem U, Roth S, Aggarwal A, Fetahu ISh, Tennakoon S, Gomes AR, Brandi ML, Bruggeman F, Mentaverri R, Riccardi D, Kallay E. Calcium sensing receptor signalling in physiology and cancer. Biochim Biophys Acta. 2013; 1833:1732-1744.
14. de Torres C, Beleta H, Díaz R, Toran N, Rodríguez E, Lavarino C, García I, Acosta S, Suñol M, Mora J. The calciumsensing receptor and parathyroid hormonerelated protein are expressed in differentiated, favorable neuroblastic tumors. Cancer. 2009; 115:2792-2803.
15. Casalà C, GilGuiñón E, Ordóñez JL, MiguelQueralt S, Rodríguez E, Galván P, Lavarino C, Munell F, de Alava E, Mora J, de Torres C. The calciumsensing receptor is silenced by genetic and epigenetic mechanisms in unfavorable neuroblastomas and its reactivation induces ERK1/2-dependent apoptosis. Carcinogenesis. 2013; 34:268-276.
16. Masvidal L, Iniesta I, Casalà C, Galván P, Rodríguez E, Rodríguez E, Lavarino C, Mora J, de Torres C. Polymorphisms in the calcium-sensing receptor gene are associated with clinical outcome of neuroblastoma. PLoS One. 2013; 8:e59762.
17. Nemeth EF, Steffey ME, Hammerland LG, Hung BC, Van Wagenen BC, DelMar G, Balandrin MF. Calcimimetics with potent and selective activity on the parathyroid calcium receptor. Proc Natl Acad Sci U S A. 1998; 95:4040-4045.
18. Hjälm G, MacLeod RJ, Kifor O, Chattopadhyay N, Brown EM. FilaminA binds to the carboxylterminal tail of the calciumsensing receptor, an interaction that participates in CaRmediated activation of mitogenactivated protein kinase. J Biol Chem. 2001; 276:34880-34887.
19. Hitomi J, Katayama T, Eguchi Y, Kudo T, Taniguchi M, Koyama Y, Manabe T, Yamagishi S, Bando Y, Imaizumi K, Tsujimoto Y, Tohyama M. Involvement of caspase-4 in endoplasmic reticulum stressinduced apoptosis and Aβ-induced cell death. J Cell Biol. 2004; 165:347-356.
20. Qing G, Li B, Vu A, Skuli N, Walton ZE, Liu X, Mayes PA, Wise DR, Thompson CB, Maris JM, Hogarty MD, Simon MC. ATF4 regulates MYCmediated neuroblastoma cell death upon glutamine deprivation. Cancer Cell. 2012; 22:631-644.
21. Ciccarone V, Spengler BA, Meyers MB, Biedler JL, Ross RA. Phenotypic diversification in human neuroblastoma cells: expression of distinct neural crest lineages. Cancer Res. 1989; 49:219-225.
22. Luo B, Lee AS. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene. 2013; 32:805-818.
23. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stressinducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005; 24:1243-1255.
24. Santulli G, Pagano G, Sardu C, Xie W, Reiken S, D'Ascia SL, Cannone M, Marziliano N, Trimarco B, Guise TA, Lacampagne A, Marks AR. Calcium release channel RyR2 regulates insulin release and glucose homeostasis. J Clin Invest. 2015; 125:1968-1978.
25. Martin AC, Willoughby D, Ciruela A, Ayling LJ, Pagano M, Wachten S, Tengholm A, Cooper DM. Capacitative Ca2+ entry via Orai1 and stromal interacting molecule 1 (STIM1) regulates adenylyl cyclase type 8. Mol Pharmacol. 2009; 75:830-842.
26. Parnell E, Smith BO, Yarwood SJ. The cAMP sensors, EPAC1 and EPAC2, display distinct subcellular distributions despite sharing a common nuclear pore localisation signal. Cell Signal. 2015; 27:989-996.
27. Roberts SS, Mori M, Pattee P, Lapidus J, Mathews R, O'Malley JP, Hsieh YC, Turner MA, Wang Z, Tian Q, Rodland MJ, Reynolds CP, Seeger RC, Nagalla SR. GABAergic system gene expression predicts clinical outcome in patients with neuroblastoma. J Clin Oncol. 2004; 22:4127-4134.
28. Nakagawara A, ArimaNakagawara M, Scavarda NJ, Azar CG, Cantor AB, Brodeur GM. Association between high levels of expression of the TRK gene and favorable outcome in human neuroblastoma. N Engl J Med. 1993; 328:847-854.
29. Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature. 2000; 407:592-598.
30. Gualdrini F, Corvetta D, Cantilena S, Chayka O, Tanno B, Raschellà G, Sala A. Addiction of MYCN amplified tumours to BMYB underscores a reciprocal regulatory loop. Oncotarget. 2010; 1:278-288. doi: 10.18632/oncotarget.138
31. Liu T, Chung MJ, Ullenbruch M, Yu H, Jin H, Hu B, Choi YY, Ishikawa F, Phan SH. Telomerase activity is required for bleomycin-induced pulmonary fibrosis in mice. J Clin Invest. 2007; 117:3800-3809.
32. Koppen A, AitAissa R, Hopman S, Koster J, Haneveld F, Versteeg R, Valentijn LJ. Dickkopf1 is downregulated by MYCN and inhibits neuroblastoma cell proliferation. Cancer Lett. 2007; 256:218-228.
33. Chen L, Tweddle DA. p53, SKP2, and DKK3 as MYCN Target Genes and Their Potential Therapeutic Significance. Front Oncol. 2012; 2:173.
34. Fratta E, Coral S, Covre A, Parisi G, Colizzi F, Danielli R, Nicolay HJ, Sigalotti L, Maio M. The biology of cancer testis antigens: putative function, regulation and therapeutic potential. Mol Oncol. 2011; 5:164-182.
35. Rao M, Chinnasamy N, Hong JA, Zhang Y, Zhang M, Xi S, Liu F, Marquez VE, Morgan RA, Schrump DS. Inhibition of histone lysine methylation enhances cancer-testis antigen expression in lung cancer cells: implications for adoptive immunotherapy of cancer. Cancer Res. 2011; 71:4192-4204.
36. Renaud S, Pugacheva EM, Delgado MD, Braunschweig R, Abdullaev Z, Loukinov D, Benhattar J, Lobanenkov V. Expression of the CTCFparalogous cancertestis gene, brother of the regulator of imprinted sites (BORIS), is regulated by three alternative promoters modulated by CpG methylation and by CTCF and p53 transcription factors. Nucleic Acids Res. 2007; 35:7372-7388.
37. Vatolin S, Abdullaev Z, Pack SD, Flanagan PT, Custer M, Loukinov DI, Pugacheva E, Hong JA, Morse H 3rd, Schrump DS, Risinger JI, Barrett JC, Lobanenkov VV. Conditional expression of the CTCFparalogous transcriptional factor BORIS in normal cells results in demethylation and derepression of MAGEA1 and reactivation of other cancertestis genes. Cancer Res. 2005; 65:7751-7762.
38. Cheung IY, Cheung NK. Molecular detection of GAGE expression in peripheral blood and bone marrow: utility as a tumor marker for neuroblastoma. Clin Cancer Res. 1997; 3:821-826.
39. Caballero OL, Cohen T, Gurung S, Chua R, Lee P, Chen YT, Jat P, Simpson AJ. Effects of CTXp gene knock down in melanoma cell lines. Oncotarget. 2013; 4:531-541. doi: 10.18632/oncotarget.921
40. Freitas M, Malheiros S, Stávale JN, Biassi TP, Zamunér FT, de Souza Begnami M, Soares FA, Vettore AL. Expression of cancer/testis antigens is correlated with improved survival in glioblastoma. Oncotarget. 2013; 4:636-646. doi: 10.18632/oncotarget.950
41. Zhang X, Zhang T, Wu J, Yu X, Zheng D, Yang F, Li T, Wang L, Zhao Y, Dong S, Zhong X, Fu S, Xu CQ, Lu F, Zhang WH. Calcium sensing receptor promotes cardiac fibroblast proliferation and extracellular matrix secretion. Cell Physiol Biochem. 2014; 33:557-568.
42. Wu M, Tang R, Liu H, Xu M, Pan M, Liu B. Cinacalcet attenuates the renal endothelialtomesenchymal transition in rats with adenineinduced renal failure. Am J Physiol Renal Physiol. 2014; 306:F138-146.
43. Aggarwal A, PrinzWohlgenannt M, Gröschel C, Tennakoon S, Meshcheryakova A, Chang W, Brown EM, Mechtcheriakova D, Kállay E. The calcium-sensing receptor suppresses epithelialtomesenchymal transition and stem celllike phenotype in the colon. Mol Cancer. 2015; 14:61.
44. Johnson A, DiPietro LA. Apoptosis and angiogenesis: an evolving mechanism for fibrosis. FASEB J. 2013; 27:3893-3901.
45. Tanjore H, Lawson WE, Blackwell TS. Endoplasmic reticulum stress as a pro-fibrotic stimulus. Biochim Biophys Acta. 2013; 1832:940-947.
46. Ghosh AK, Bhattacharyya S, Varga J. The tumor suppressor p53 abrogates Smaddependent collagen gene induction in mesenchymal cells. J Biol Chem. 2004; 279:47455-47463.
47. Brennan SC, Mun HC, Leach K, Kuchel PW, Christopoulos A, Conigrave AD. Receptor expression modulates calcium-sensing receptor mediated intracellular Ca2+ mobilization. Endocrinology. 2015; 156:1330-1342.
48. Irizarry RA, Hobbs B, Collin F, BeazerBarclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4:249-264.
49. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, IsselTarver L, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000; 25:25-29.
50. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003; 4:P3.