Apoptosis: Signaling pathways in pancreatic cancer pathogenesis

Pancreatic Cancer

Volumn , Issue , 2018, Pages 369-382

  McConkey, David J ^a,b   Choi, Woonyoung ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b DEPARTMENT OF PATHOLOGY   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

BCL 2 family; Cancer associated fibroblasts; EMT; IAPs; NF B; Stellate cells; Subtypes

Indexed keywords

EID: 84882748785     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4939-7193-0_14     Document Type: Chapter

References (71)

1. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26(4):239-57. PubMed PMID: 4561027.
2. Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980;284(5756):555-6. PubMed PMID: 6245367.
3. Ellis HM, Horvitz HR. Genetic control of programmed cell death in the nematode C. elegans. Cell. 1986;44(6):817-29. PubMed PMID: 3955651.
4. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell. 1993; 75(4):641-52. PubMed PMID: 8242740.
5. Hengartner MO. The biochemistry of apoptosis. Nature. 2000;407(6805):770-6. PubMed PMID: 11048727.
6. Liu X, Zou H, Slaughter C, Wang X. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell. 1997;89(2):175-84. PubMed PMID: 9108473.
7. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997;90(3):405-13. PubMed PMID: 9267021.
8. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem. 1999;274(17):11549-56. PubMed PMID: 10206961.
9. Tsujimoto Y, Cossman J, Jaffe E, Croce CM. Involvement of the bcl-2 gene in human follicular lymphoma. Science. 1985;228(4706):1440-3. PubMed PMID: 3874430.
10. Bakhshi A, Jensen JP, Goldman P, Wright JJ, McBride OW, Epstein AL, et al. Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell. 1985;41(3):899-906. PubMed PMID: 3924412.
11. McDonnell TJ, Deane N, Platt FM, Nunez G, Jaeger U, McKearn JP, et al. Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 1989;57(1):79-88. PubMed PMID: 2649247.
12. Boise LH, Gonzalez-Garcia M, Postema CE, Ding L, Lindsten T, Turka LA, et al. Bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell. 1993;74 (4):597-608. PubMed PMID: 8358789.
13. Hockenbery D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 1990;348 (6299):334-6. PubMed PMID: 2250705.
14. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 1993;74(4):609-19. PubMed PMID: 8358790.
15. Adams JM, Cory S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene. 2007;26(9):1324-37. PubMed PMID: 17322918.
16. Antignani A, Youle RJ. How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr Opin Cell Biol. 2006;18(6):685-9. PubMed PMID: 17046225.
17. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2002;2(3):183-92. PubMed PMID: 12242151.
18. Eckelman BP, Salvesen GS, Scott FL. Human inhibitor of apoptosis proteins: why XIAP is the black sheep of the family. EMBO Rep. 2006;7(10):988-94. PubMed PMID: 17016456.
19. Ashkenazi A, Dixit VM. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol. 1999;11(2):255-60. PubMed PMID: 10209153.
20. Jost PJ, Grabow S, Gray D, McKenzie MD, Nachbur U, Huang DC, et al. XIAP discriminates between type I and type II FAS-induced apoptosis. Nature. 2009;460(7258):1035-1039. https://doi.org/10.1038/nature08229. PubMed PMID: 19626005; PubMed Central PMCID: PMCPMC2956120.
21. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998;94(4):491-501. PubMed PMID: 9727492.
22. Beg AA, Baltimore D. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 1996;274(5288):782-4. PubMed PMID: 8864118.
23. Evan GI, Wyllie AH, Gilbert CS, Littlewood TD, Land H, Brooks M, et al. Induction of apoptosis in fibroblasts by c-myc protein. Cell. 1992;69(1):119-28. PubMed PMID: 1555236.
24. Clarke AR, Purdie CA, Harrison DJ, Morris RG, Bird CC, Hooper ML, et al. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature. 1993;362 (6423):849-52. PubMed PMID: 8479523.
25. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature. 1993;362(6423):847-9. PubMed PMID: 8479522.
26. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 1993;74(6):957-67. PubMed PMID: 8402885.
27. Jackson JG, Pant V, Li Q, Chang LL, Quintas-Cardama A, Garza D, et al. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell. 2012;21(6):793-806. https://doi.org/10.1016/j.ccr.2012.04.027. PubMed PMID: 22698404; PubMed Central PMCID: PMCPMC3376352.
28. Esserman LJ, Berry DA, Cheang MC, Yau C, Perou CM, Carey L, et al. Chemotherapy response and recurrence-free survival in neoadjuvant breast cancer depends on biomarker profiles: results from the I-SPY 1 TRIAL (CALGB 150007/150012; ACRIN 6657). Breast Cancer Res Treat. 2012;132(3):1049-62. https://doi.org/10.1007/s10549-011-1895-2. PubMed PMID: 22198468; PubMed Central PMCID: PMCPMC3332388.
29. Certo M, Del Gaizo MV, Nishino M, Wei G, Korsmeyer S, Armstrong SA, et al. Mitochondria primed by death signals determine cellular addiction to antiapoptoticBCL-2 family members. Cancer Cell. 2006;9(5):351-65. https://doi.org/10.1016/j.ccr.2006.03.027. PubMed PMID: 16697956.
30. Ni Chonghaile T, Sarosiek KA, Vo TT, Ryan JA, Tammareddi A, Moore Vdel G, et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science. 2011;334(6059):1129-33. https://doi.org/10.1126/science.1206727. PubMed PMID: 22033517; PubMed Central PMCID: PMCPMC3280949.
31. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science. 2008;321 (5897):1801-6. PubMed PMID: 18772397.
32. Bailey P, Chang DK, Nones K, Johns AL, Patch AM, Gingras MC, et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature. 2016;531(7592):47-52. https://doi. org/10.1038/nature16965. PubMed PMID: 26909576.
33. Basseres DS, Baldwin AS. Nuclear factor-kappaB and inhibitor of kappaB kinase pathways in oncogenic initiation and progression. Oncogene. 2006;25(51):6817-30. PubMed PMID: 17072330.
34. WangW, Abbruzzese JL, Evans DB, Larry L, Cleary KR, Chiao PJ. The nuclear factor-kappa B RelA transcription factor is constitutively activated in human pancreatic adenocarcinoma cells. Clin Cancer Res. 1999;5(1):119-27. PubMed PMID: 9918209.
35. Dong QG, Sclabas GM, Fujioka S, Schmidt C, Peng B, Wu T, et al. The function of multiple IkappaB: NF-kappaB complexes in the resistance of cancer cells to Taxol-induced apoptosis. Oncogene. 2002;21(42):6510-9. PubMed PMID: 12226754.
36. Khanbolooki S, Nawrocki ST, Arumugam T, Andtbacka R, Pino MS, Kurzrock R, et al. Nuclear factor-kappaB maintains TRAIL resistance in human pancreatic cancer cells. Mol Cancer Ther. 2006;5(9):2251-60. PubMed PMID: 16985059.
37. Finco TS, Westwick JK, Norris JL, Beg AA, Der CJ, Baldwin Jr AS. Oncogenic Ha-Rasinduced signaling activates NF-kappaB transcriptional activity, which is required for cellular transformation. J Biol Chem. 1997;272(39):24113-6. PubMed PMID: 9305854.
38. Ling J, Kang Y, Zhao R, Xia Q, Lee DF, Chang Z, et al. KrasG12D-induced IKK2/beta/NFkappaB activation by IL-1alpha and p62 feedforward loops is required for development of pancreatic ductal adenocarcinoma. Cancer Cell. 2012;21(1):105-20. https://doi.org/10.1016/j. ccr.2011.12.006. PubMed PMID: 22264792; PubMed Central PMCID: PMCPMC3360958.
39. Shah SA, Potter MW, Hedeshian MH, Kim RD, Chari RS, Callery MP. PI-30 kinase and NF-kappaB cross-signaling in human pancreatic cancer cells. J Gastrointest Surg. 2001;5 (6):603-12; discussion 12-3. PubMed PMID: 12086898.
40. Pan X, Arumugam T, Yamamoto T, Levin PA, Ramachandran V, Ji B, et al. Nuclear factorkappaB p65/relA silencing induces apoptosis and increases gemcitabine effectiveness in a subset of pancreatic cancer cells. Clin Cancer Res. 2008;14(24):8143-51. PubMed PMID: 19088029.
41. Nawrocki ST, Bruns CJ, Harbison MT, Bold RJ, Gotsch BS, Abbruzzese JL, et al. Effects of the proteasome inhibitor PS-341 on apoptosis and angiogenesis in orthotopic human pancreatic tumor xenografts. Mol Cancer Ther. 2002;1(14):1243-53. PubMed PMID: 12516957.
42. Marten A, Zeiss N, Serba S, Mehrle S, von Lilienfeld-Toal M, Schmidt J. Bortezomib is ineffective in an orthotopic mouse model of pancreatic adenocarcinoma. Mol Cancer Ther. 2008;7(11):3624-31. PubMed PMID: 19001444.
43. Alberts SR, Foster NR, Morton RF, Kugler J, Schaefer P, Wiesenfeld M, et al. PS-341 and gemcitabine in patients with metastatic pancreatic adenocarcinoma: a north central cancer treatment group (NCCTG) randomized phase II study. Ann Oncol. 2005;16(10):1654-61. PubMed PMID: 16085692.
44. Dhillon N, Aggarwal BB, Newman RA, WolffRA, Kunnumakkara AB, Abbruzzese JL, et al. Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin Cancer Res. 2008;14 (14):4491-9. PubMed PMID: 18628464.
45. Epelbaum R, Schaffer M, Vizel B, Badmaev V, Bar-Sela G. Curcumin and gemcitabine in patients with advanced pancreatic cancer. Nutr Cancer. 2010;62(8):1137-41. https://doi.org/10.1080/01635581.2010.513802. PubMed PMID: 21058202.
46. Kanai M, Yoshimura K, Asada M, Imaizumi A, Suzuki C, Matsumoto S, et al. A phase I/II study of gemcitabine-based chemotherapy plus curcumin for patients with gemcitabine-resistant pancreatic cancer. Cancer Chemother Pharmacol. 2011;68(1):157-64. https://doi.org/10.1007/s00280-010-1470-2. PubMed PMID: 20859741.
47. Asher GN, Xie Y, Moaddel R, Sanghvi M, Dossou KS, Kashuba AD, et al. Randomized Pharmacokinetic Crossover Study Comparing 2 Curcumin Preparations in Plasma and Rectal Tissue of Healthy Human Volunteers. J Clin Pharmacol. 2016; https://doi.org/10.1002/jcph.806. PubMed PMID: 27503249.
48. Storka A, Vcelar B, Klickovic U, Gouya G, Weisshaar S, Aschauer S, et al. Safety, tolerability and pharmacokinetics of liposomal curcumin in healthy humans. Int J Clin Pharmacol Ther. 2015;53(1):54-65. https://doi.org/10.5414/CP202076. PubMed PMID: 25500488.
49. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer. 2007;7(6):415-28. PubMed PMID: 17508028.
50. Mani SA, GuoW, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704-15. PubMed PMID: 18485877.
51. Arumugam T, Ramachandran V, Fournier KF, Wang H, Marquis L, Abbruzzese JL, et al. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009;69(14):5820-8. https://doi.org/10.1158/0008-5472.CAN-08-2819. PubMed PMID: 19584296; PubMed Central PMCID: PMCPMC4378690.
52. Haddad Y, Choi W, McConkey DJ. Delta-crystallin enhancer binding factor 1 controls the epithelial to mesenchymal transition phenotype and resistance to the epidermal growth factor receptor inhibitor erlotinib in human head and neck squamous cell carcinoma lines. Clin Cancer Res. 2009;15(2):532-42. PubMed PMID: 19147758.
53. Rho JK, Choi YJ, Lee JK, Ryoo BY, Na II, Yang SH, et al. Epithelial to mesenchymal transition derived from repeated exposure to gefitinib determines the sensitivity to EGFR inhibitors in A549, a non-small cell lung cancer cell line. Lung Cancer. 2009;63(2):219-26. PubMed PMID: 18599154.
54. Thomson S, Buck E, Petti F, Griffin G, Brown E, Ramnarine N, et al. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res. 2005;65(20):9455-62. PubMed PMID: 16230409.
55. Yauch RL, Januario T, Eberhard DA, Cavet G, Zhu W, Fu L, et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res. 2005;11(24 Pt 1):8686-98. PubMed PMID: 16361555.
56. Collisson EA, Sadanandam A, Olson P, Gibb WJ, Truitt M, Gu S, et al. Subtypes of pancreatic ductal adenocarcinoma and their differing responses to therapy. Nat Med. 2011;17(4):500-3. https://doi.org/10.1038/nm.2344. PubMed PMID: 21460848; PubMed Central PMCID: PMCPMC3755490.
57. Zheng X, Carstens JL, Kim J, Scheible M, Kaye J, Sugimoto H, et al. Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer. Nature. 2015;527(7579):525-30. https://doi.org/10.1038/nature16064. PubMed PMID: 26560028; PubMed Central PMCID: PMCPMC4849281.
58. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N, et al. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell. 2009;15(6):489-500. https://doi.org/10.1016/j.ccr.2009.03.022. PubMed PMID: 19477428; PubMed Central PMCID: PMCPMC2743093.
59. Genovese G, Carugo A, Tepper J, Robinson FS, Li L, Svelto M, et al. Synthetic vulnerabilities of mesenchymal subpopulations in pancreatic cancer. Nature. 2017;542(7641):362-6. https://doi.org/10.1038/nature21064. PubMed PMID: 28178232.
60. Witta SE, Gemmill RM, Hirsch FR, Coldren CD, Hedman K, Ravdel L, et al. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 2006;66(2):944-50. PubMed PMID: 16424029.
61. Jones SF, Bendell JC, Infante JR, Spigel DR, Thompson DS, Yardley DA, et al. A phase I study of panobinostat in combination with gemcitabine in the treatment of solid tumors. Clin Adv Hematol Oncol. 2011;9(3):225-30. PubMed PMID: 21475129.
62. Avan A, Crea F, Paolicchi E, Funel N, Galvani E, Marquez VE, et al. Molecular mechanisms involved in the synergistic interaction of the EZH2 inhibitor 3-deazaneplanocin A with gemcitabine in pancreatic cancer cells. Mol Cancer Ther. 2012;11(8):1735-46. https://doi.org/10.1158/1535-7163.MCT-12-0037. PubMed PMID: 22622284; PubMed Central PMCID: PMCPMC3416916.
63. Moffitt RA, Marayati R, Flate EL, Volmar KE, Loeza SG, Hoadley KA, et al. Virtual microdissection identifies distinct tumor-and stroma-specific subtypes of pancreatic ductal adenocarcinoma. Nat Genet. 2015;47(10):1168-78. https://doi.org/10.1038/ng.3398. PubMed PMID: 26343385; PubMed Central PMCID: PMCPMC4912058.
64. Vonlaufen A, Phillips PA, Xu Z, Goldstein D, Pirola RC, Wilson JS, et al. Pancreatic stellate cells and pancreatic cancer cells: an unholy alliance. Cancer Res. 2008;68(19):7707-10. PubMed PMID: 18829522.
65. Hwang RF, Moore T, Arumugam T, Ramachandran V, Amos KD, Rivera A, et al. Cancerassociated stromal fibroblasts promote pancreatic tumor progression. Cancer Res. 2008;68 (3):918-26. PubMed PMID: 18245495.
66. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science. 2009;324(5933):1457-61. https://doi.org/10.1126/science.1171362. PubMed PMID: 19460966; PubMed Central PMCID: PMCPMC2998180.
67. Kim EJ, Sahai V, Abel EV, Griffith KA, Greenson JK, Takebe N, et al. Pilot clinical trial of hedgehog pathway inhibitor GDC-0449 (vismodegib) in combination with gemcitabine in patients with metastatic pancreatic adenocarcinoma. Clin Cancer Res. 2014;20(23):5937-45. https://doi.org/10.1158/1078-0432.CCR-14-1269. PubMed PMID: 25278454; PubMed Central PMCID: PMCPMC4254161.
68. Catenacci DV, Junttila MR, Karrison T, Bahary N, Horiba MN, Nattam SR, et al. Randomized Phase Ib/II Study of Gemcitabine Plus Placebo or Vismodegib, a Hedgehog Pathway Inhibitor, in Patients With Metastatic Pancreatic Cancer. J Clin Oncol. 2015;33(36):4284-92. https://doi. org/10.1200/JCO.2015.62.8719. PubMed PMID: 26527777; PubMed Central PMCID: PMCPMC4678179.
69. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell. 2014;25(6):735-47. https://doi.org/10.1016/j.ccr.2014.04.021. PubMed PMID: 24856585; PubMed Central PMCID: PMCPMC4096698.
70. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell. 2014;25(6):719-34. https://doi.org/10.1016/j.ccr.2014.04.005. PubMed PMID: 24856586; PubMed Central PMCID: PMCPMC4180632.
71. Laklai H, Miroshnikova YA, Pickup MW, Collisson EA, Kim GE, Barrett AS, et al. Genotype tunes pancreatic ductal adenocarcinoma tissue tension to induce matricellular fibrosis and tumor progression. Nat Med. 2016;22(5):497-505. https://doi.org/10.1038/nm.4082. PubMed PMID: 27089513; PubMed Central PMCID: PMCPMC4860133.