Project title: Transcriptome and methylome of pancreatic NETs with and without ATRX/DAXX mutations

Nickolas Papadopoulos, PhD Johns Hopkins School of Medicine, Baltimore

Nickolas Papadopoulos, PhD
  • Status: Completed
  • Year(s): 2010
  • Research Type: Basic
  • Primary Site: Pancreas
  • Area of Inquiry: Mapping NET dependencies

General Description

Nickolas Papadopoulos, PhD, and his team published the results published the results of the first large-scale genome sequencing study of pancreatic neuroendocrine tumors in Science as part of a two-year NETRF grant. Given the importance of the finding, the grant was extended for another two years to explore further the role of DAXX and ATRX mutations in neuroendocrine tumors. 

Dr. Papadopoulos announced the discovery of mutations in two genes (DAXX and ATRX) not previously associated with cancer. Further study of these genes suggests they may play a broader role in the development of not only neuroendocrine cancers but certain types of adult and pediatric brain tumors as well. Identification of mutations within these genes suggests a novel approach to neuroendocrine cancer diagnostics and treatment by targeting epigenetic processes.

DAXX and ATRX are epigenetic regulators, meaning they determine which genes are turned on or off under specific conditions in a cell. While genes contain the instructions for assembling proteins, it is through epigenetic regulation that cells are able to control whether those proteins are actually produced. Mutations within these epigenetic regulating genes can cause them to malfunction, leading to the inactivation of a cancer-suppressing gene, or activation of a cancer-driving gene.

Research Objectives

  1. To determine the epigenetic landscape of pancreatic neuroendocrine tumors by studying the gene expression and methylation patterns of pancreatic neuroendocrine tumors with or without DAXX or ATRX mutations.
  2. To develop novel therapeutic approaches for patients with neuroendocrine tumors.
  3. To study the role of epigenetic regulation in neuroendocrine cancer development.

Abstract

Virtually all the biologic properties of cancer cells are governed by the genetic changes present in them. With the help of CFCF, we have defined the genomic landscapes of pancreatic neuroendocrine tumors. The most intriguing and novel components of these landscapes were mutations of genes called DAXX and ATRX. These genes are master regulators of chromatin packaging – proteins that surround DNA in the nucleus of the cell and determine which genes are turned on or off under specific conditions. In the next phase of our work, we will explore which genes are actually turned on or off in pancreatic neuroendocrine tumors containing mutations of either of these two genes. The long-term objective is to use this information to develop new therapeutic approaches based on a better understanding of these commonly altered pathways in pancreatic neuroendocrine tumors.

Research Publications

Jiao Y, Shi C, Edil BH, de Wilde RF, Klimstra DS, Maitra A, Schulick RD, Tang LH, Wolfgang CL, Choti MA, Velculescu VE, Diaz LA Jr, Vogelstein B, Kinzler KW, Hruban RH, Papadopoulos N. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science. 2011 Mar 4;331(6021):1199-203. doi: 10.1126/science.1200609. Epub 2011 Jan 20.

1: Raj N, Shah R, Stadler Z, Mukherjee S, Chou J, Untch B, Li J, Kelly V, Saltz LB, Mandelker D, Ladanyi M, Berger MF, Klimstra DS, Reidy-Lagunes D, Osoba M. Real-Time Genomic Characterization of Metastatic Pancreatic Neuroendocrine Tumors Has Prognostic Implications and Identifies Potential Germline Actionability. JCO Precis Oncol. 2018;2018. doi: 10.1200/PO.17.00267. Epub 2018 Apr 19. PubMed PMID: 30687805; PubMed Central PMCID: PMC6345401.

2: Cacchione S, Biroccio A, Rizzo A. Emerging roles of telomeric chromatin alterations in cancer. J Exp Clin Cancer Res. 2019 Jan 17;38(1):21. doi: 10.1186/s13046-019-1030-5. Review. PubMed PMID: 30654820; PubMed Central PMCID: PMC6337846.

3: Liverani C, Bongiovanni A, Mercatali L, Foca F, Pieri F, De Vita A, Spadazzi C, Miserocchi G, Recine F, Riva N, Nicolini S, Severi S, Martinelli G, Ibrahim T. Grading of Neuroendocrine Carcinomas: Correlation of (68)Ga-PET/CT Scan with Tissue Biomarkers. Dis Markers. 2018 Dec 2;2018:6878409. doi: 10.1155/2018/6878409. eCollection 2018. PubMed PMID: 30627226; PubMed Central PMCID: PMC6304840.

4: Young CC, Baker RM, Howlett CJ, Hryciw T, Herman JE, Higgs D, Gibbons R, Crawford H, Brown A, Pin CL. The Loss of ATRX Increases Susceptibility to Pancreatic Injury and Oncogenic KRAS in Female But Not Male Mice. Cell Mol Gastroenterol Hepatol. 2018 Sep 14;7(1):93-113. doi: 10.1016/j.jcmgh.2018.09.004. eCollection 2019. PubMed PMID: 30510993; PubMed Central PMCID: PMC6260375.

5: Lewis CS, Elnakat Thomas H, Orr-Asman MA, Green LC, Boody RE, Matiash K, Karve A, Hisada YM, Davis HW, Qi X, Mercer CA, Lucas FV, Aronow BJ, Mackman N, Versteeg HH, Bogdanov VY. mTOR kinase inhibition reduces tissue factor expression and growth of pancreatic neuroendocrine tumors. J Thromb Haemost. 2019 Jan;17(1):169-182. doi: 10.1111/jth.14342. Epub 2018 Dec 25. PubMed PMID: 30472780; PubMed Central PMCID: PMC6345540.

6: Khoo LT, Chen LY. Role of the cGAS-STING pathway in cancer development and oncotherapeutic approaches. EMBO Rep. 2018 Dec;19(12). pii: e46935. doi: 10.15252/embr.201846935. Epub 2018 Nov 16. Review. PubMed PMID: 30446584; PubMed Central PMCID: PMC6280650.

7: Chan CS, Laddha SV, Lewis PW, Koletsky MS, Robzyk K, Da Silva E, Torres PJ, Untch BR, Li J, Bose P, Chan TA, Klimstra DS, Allis CD, Tang LH. ATRX, DAXX or MEN1 mutant pancreatic neuroendocrine tumors are a distinct alpha-cell signature subgroup. Nat Commun. 2018 Oct 12;9(1):4158. doi: 10.1038/s41467-018-06498-2. PubMed PMID: 30315258; PubMed Central PMCID: PMC6185985.

8: He R, Yin Y, Yin W, Li Y, Zhao J, Zhang W. Prevention of pancreatic acinar cell carcinoma by Roux-en-Y Gastric Bypass Surgery. Nat Commun. 2018 Oct 10;9(1):4183. doi: 10.1038/s41467-018-06571-w. PubMed PMID: 30305629; PubMed Central PMCID: PMC6180124.

9: Chamberlain CE, German MS, Yang K, Wang J, VanBrocklin H, Regan M, Shokat KM, Ducker GS, Kim GE, Hann B, Donner DB, Warren RS, Venook AP, Bergsland EK, Lee D, Wang Y, Nakakura EK. A Patient-derived Xenograft Model of Pancreatic Neuroendocrine Tumors Identifies Sapanisertib as a Possible New Treatment for Everolimus-resistant Tumors. Mol Cancer Ther. 2018 Dec;17(12):2702-2709. doi: 10.1158/1535-7163.MCT-17-1204. Epub 2018 Sep 25. PubMed PMID: 30254185; PubMed Central PMCID: PMC6279485.

10: Brosnan-Cashman JA, Yuan M, Graham MK, Rizzo AJ, Myers KM, Davis C, Zhang R, Esopi DM, Raabe EH, Eberhart CG, Heaphy CM, Meeker AK. ATRX loss induces multiple hallmarks of the alternative lengthening of telomeres (ALT) phenotype in human glioma cell lines in a cell line-specific manner. PLoS One. 2018 Sep 18;13(9):e0204159. doi: 10.1371/journal.pone.0204159. eCollection 2018. PubMed PMID: 30226859; PubMed Central PMCID: PMC6143253.

11: Takahashi D, Kojima M, Suzuki T, Sugimoto M, Kobayashi S, Takahashi S, Konishi M, Gotohda N, Ikeda M, Nakatsura T, Ochiai A, Nagino M. Profiling the Tumour Immune Microenvironment in Pancreatic Neuroendocrine Neoplasms with Multispectral Imaging Indicates Distinct Subpopulation Characteristics Concordant with WHO 2017 Classification. Sci Rep. 2018 Sep 3;8(1):13166. doi: 10.1038/s41598-018-31383-9. PubMed PMID: 30177687; PubMed Central PMCID: PMC6120899.

12: da Silva A, Bowden M, Zhang S, Masugi Y, Thorner AR, Herbert ZT, Zhou CW, Brais L, Chan JA, Hodi FS, Rodig S, Ogino S, Kulke MH. Characterization of the Neuroendocrine Tumor Immune Microenvironment. Pancreas. 2018 Oct;47(9):1123-1129. doi: 10.1097/MPA.0000000000001150. PubMed PMID: 30153220; PubMed Central PMCID: PMC6131026.

13: Rindi G, Klimstra DS, Abedi-Ardekani B, Asa SL, Bosman FT, Brambilla E, Busam KJ, de Krijger RR, Dietel M, El-Naggar AK, Fernandez-Cuesta L, Klöppel G, McCluggage WG, Moch H, Ohgaki H, Rakha EA, Reed NS, Rous BA, Sasano H, Scarpa A, Scoazec JY, Travis WD, Tallini G, Trouillas J, van Krieken JH, Cree IA. A common classification framework for neuroendocrine neoplasms: an International Agency for Research on Cancer (IARC) and World Health Organization (WHO) expert consensus proposal. Mod Pathol. 2018 Dec;31(12):1770-1786. doi: 10.1038/s41379-018-0110-y. Epub 2018 Aug 23. PubMed PMID: 30140036; PubMed Central PMCID: PMC6265262.

14: Hendifar AE, Dhall D, Strosberg JR. The Evolving Treatment Algorithm for Advanced Neuroendocrine Neoplasms: Diversity and Commonalities Across Tumor Types. Oncologist. 2019 Jan;24(1):54-61. doi: 10.1634/theoncologist.2018-0187. Epub 2018 Aug 13. Review. PubMed PMID: 30104288; PubMed Central PMCID: PMC6324634.

15: Kyriakopoulos G, Mavroeidi V, Chatzellis E, Kaltsas GA, Alexandraki KI. Histopathological, immunohistochemical, genetic and molecular markers of neuroendocrine neoplasms. Ann Transl Med. 2018 Jun;6(12):252. doi: 10.21037/atm.2018.06.27. Review. PubMed PMID: 30069454; PubMed Central PMCID: PMC6046289.

16: Lawrence B, Blenkiron C, Parker K, Tsai P, Fitzgerald S, Shields P, Robb T, Yeong ML, Kramer N, James S, Black M, Fan V, Poonawala N, Yap P, Coats E, Woodhouse B, Ramsaroop R, Yozu M, Robinson B, Henare K, Koea J, Johnston P, Carroll R, Connor S, Morrin H, Elston M, Jackson C, Reid P, Windsor J, MacCormick A, Babor R, Bartlett A, Damianovich D, Knowlton N, Grimmond S, Findlay M, Print C. Recurrent loss of heterozygosity correlates with clinical outcome in pancreatic neuroendocrine cancer. NPJ Genom Med. 2018 Jul 20;3:18. doi: 10.1038/s41525-018-0058-3. eCollection 2018. PubMed PMID: 30062048; PubMed Central PMCID: PMC6054670.

17: Ogura K, Hosoda F, Arai Y, Nakamura H, Hama N, Totoki Y, Yoshida A, Nagai M, Kato M, Arakawa E, Mukai W, Rokutan H, Kawai A, Tanaka S, Shibata T. Integrated genetic and epigenetic analysis of myxofibrosarcoma. Nat Commun. 2018 Jul 17;9(1):2765. doi: 10.1038/s41467-018-03891-9. PubMed PMID: 30018380; PubMed Central PMCID: PMC6050269.

18: Wasylishen AR, Estrella JS, Pant V, Chau GP, Lozano G. Daxx Functions Are p53-Independent In Vivo. Mol Cancer Res. 2018 Oct;16(10):1523-1529. doi: 10.1158/1541-7786.MCR-18-0281. Epub 2018 Jun 14. PubMed PMID: 29903771; PubMed Central PMCID: PMC6233723.

19: Haase S, Garcia-Fabiani MB, Carney S, Altshuler D, Núñez FJ, Méndez FM, Núñez F, Lowenstein PR, Castro MG. Mutant ATRX: uncovering a new therapeutic target for glioma. Expert Opin Ther Targets. 2018 Jul;22(7):599-613. doi: 10.1080/14728222.2018.1487953. Epub 2018 Jun 20. Review. PubMed PMID: 29889582; PubMed Central PMCID: PMC6044414.

20: Waldum HL, Öberg K, Sørdal ØF, Sandvik AK, Gustafsson BI, Mjønes P, Fossmark R. Not only stem cells, but also mature cells, particularly neuroendocrine cells, may develop into tumours: time for a paradigm shift. Therap Adv Gastroenterol. 2018 May 27;11:1756284818775054. doi: 10.1177/1756284818775054. eCollection 2018. Review. PubMed PMID: 29872453; PubMed Central PMCID: PMC5974566.

21: Noë M, Pea A, Luchini C, Felsenstein M, Barbi S, Bhaijee F, Yonescu R, Ning Y, Adsay NV, Zamboni G, Lawlor RT, Scarpa A, Offerhaus GJA, Brosens LAA, Hruban RH, Roberts NJ, Wood LD. Whole-exome sequencing of duodenal neuroendocrine tumors in patients with neurofibromatosis type 1. Mod Pathol. 2018 Oct;31(10):1532-1538. doi: 10.1038/s41379-018-0082-y. Epub 2018 May 30. PubMed PMID: 29849115; PubMed Central PMCID: PMC6168403.

22: Diplas BH, He X, Brosnan-Cashman JA, Liu H, Chen LH, Wang Z, Moure CJ, Killela PJ, Loriaux DB, Lipp ES, Greer PK, Yang R, Rizzo AJ, Rodriguez FJ, Friedman AH, Friedman HS, Wang S, He Y, McLendon RE, Bigner DD, Jiao Y, Waitkus MS, Meeker AK, Yan H. The genomic landscape of TERT promoter wildtype-IDH wildtype glioblastoma. Nat Commun. 2018 May 25;9(1):2087. doi: 10.1038/s41467-018-04448-6. PubMed PMID: 29802247; PubMed Central PMCID: PMC5970234.

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24: Polchi A, Magini A, Meo DD, Tancini B, Emiliani C. mTOR Signaling and Neural Stem Cells: The Tuberous Sclerosis Complex Model. Int J Mol Sci. 2018 May 16;19(5). pii: E1474. doi: 10.3390/ijms19051474. Review. PubMed PMID: 29772672; PubMed Central PMCID: PMC5983755.

25: Lee L, Ito T, Jensen RT. Everolimus in the treatment of neuroendocrine tumors: efficacy, side-effects, resistance, and factors affecting its place in the treatment sequence. Expert Opin Pharmacother. 2018 Jun;19(8):909-928. doi: 10.1080/14656566.2018.1476492. Epub 2018 May 24. PubMed PMID: 29757017; PubMed Central PMCID: PMC6064188.

26: Gaspar TB, Sá A, Lopes JM, Sobrinho-Simões M, Soares P, Vinagre J. Telomere Maintenance Mechanisms in Cancer. Genes (Basel). 2018 May 3;9(5). pii: E241. doi: 10.3390/genes9050241. Review. PubMed PMID: 29751586; PubMed Central PMCID: PMC5977181.

27: Wang Z, Liu L, Luo J, Guo J, Zhai M, Zhang W, Yang Z. Uncovering the heterogeneous genetic variations in two insulin-expressing tumors in a patient with MEN1. Oncol Lett. 2018 May;15(5):7123-7131. doi: 10.3892/ol.2018.8184. Epub 2018 Mar 6. PubMed PMID: 29725435; PubMed Central PMCID: PMC5920406.

28: Udugama M, Sanij E, Voon HPJ, Son J, Hii L, Henson JD, Chan FL, Chang FTM, Liu Y, Pearson RB, Kalitsis P, Mann JR, Collas P, Hannan RD, Wong LH. Ribosomal DNA copy loss and repeat instability in ATRX-mutated cancers. Proc Natl Acad Sci U S A. 2018 May 1;115(18):4737-4742. doi: 10.1073/pnas.1720391115. Epub 2018 Apr 18. PubMed PMID: 29669917; PubMed Central PMCID: PMC5939086.

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31: Martin DR, LaBauve E, Pomo JM, Chiu VK, Hanson JA, Gullapalli RR. Site-Specific Genomic Alterations in a Well-Differentiated Pancreatic Neuroendocrine Tumor With High-Grade Progression. Pancreas. 2018 Apr;47(4):502-510. doi: 10.1097/MPA.0000000000001030. PubMed PMID: 29521944; PubMed Central PMCID: PMC5884111.

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