Bmi1 is required for the initiation of pancreatic cancer through an Ink4a-independent mechanism

Carcinogenesis

Volumn 36, Issue 7, 2015, Pages 730-738

  Bednar, Filip ^a   Schofield, Heather K ^b   Collins, Meredith A ^b   Yan, Wei ^a,c,i   Zhang, Yaqing ^a   Shyam, Nikhil ^b   Eberle, Jaime A ^d   Almada, Luciana L ^e   Olive, Kenneth P ^d   Bardeesy, Nabeel ^f   Fernandez Zapico, Martin E ^e   Nakada, Daisuke ^g   Simeone, Diane M ^a,b   Morrison, Sean J ^h   di Magliano, Marina Pasca ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d Harvard Medical School ^*  (United States)

^e MAYO CLINIC   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

ⁱ FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; BMI1 PROTEIN; INK4A PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; BMI1 PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; KRAS2 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN P21;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; EXPERIMENTAL MODEL; GENE LOCUS; MOUSE; NONHUMAN; PANCREAS CANCER; PRIORITY JOURNAL; ANIMAL; CELL TRANSFORMATION; EXPERIMENTAL NEOPLASM; GENETICS; KNOCKOUT MOUSE; METABOLISM; MUTANT MOUSE STRAIN; PANCREAS; PANCREAS TUMOR; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CYCLIN-DEPENDENT KINASE INHIBITOR P16; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NEOPLASMS, EXPERIMENTAL; PANCREAS; PANCREATIC NEOPLASMS; POLYCOMB REPRESSIVE COMPLEX 1; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS P21(RAS); REACTIVE OXYGEN SPECIES;

EID: 84941657530     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgv058     Document Type: Article

References (38)

1. Aguirre, A.J. et al. (2003) Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev., 17, 3112-3126.
2. Guerra, C. et al. (2007) Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice. Cancer Cell, 11, 291-302.
3. Hingorani, S.R. et al. (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell, 4, 437-450.
4. Hingorani, S.R. et al. (2005) Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell, 7, 469-483.
5. Jones, S. et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science, 321, 1801-1806.
6. Berdasco, M. et al. (2010) Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev. Cell, 19, 698-711.
7. Schuettengruber, B. et al. (2007) Genome regulation by polycomb and trithorax proteins. Cell, 128, 735-745.
8. van Lohuizen, M. et al. (1991) Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell, 65, 737-752.
9. Jacobs, J.J. et al. (1999) The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature, 397, 164-168.
10. van der Lugt, N.M. et al. (1994) Posterior transformation, neurological abnormalities, and severe hematopoietic defects in mice with a targeted deletion of the bmi-1 proto-oncogene. Genes Dev., 8, 757-769.
11. Molofsky, A.V. et al. (2005) Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev., 19, 1432-1437.
12. Bruggeman, S.W. et al. (2005) Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev., 19, 1438-1443.
13. Liu, J. et al. (2009) Bmi1 regulates mitochondrial function and the damage response pathway. Nature, 459, 387-392.
14. Dhawan, S. et al. (2009) Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation. Genes Dev., 23, 906-911.
15. Fukuda, A. et al. (2012) Bmi1 is required for regeneration of the exocrine pancreas in mice. Gastroenterology, 143, 821-831.e1.
16. Sangiorgi, E. et al. (2009) Bmi1 lineage tracing identifies a self-renewing pancreatic acinar cell subpopulation capable of maintaining pancreatic organ homeostasis. Proc. Natl Acad. Sci. USA, 106, 7101-7106.
17. Martínez-Romero, C. et al. (2009) The epigenetic regulators Bmi1 and Ring1B are differentially regulated in pancreatitis and pancreatic ductal adenocarcinoma. J. Pathol., 219, 205-213.
18. Proctor, E. et al. (2013) Bmi1 enhances tumorigenicity and cancer stem cell function in pancreatic adenocarcinoma. PLoS One, 8, e55820.
19. Song, W. et al. (2010) Bmi-1 is related to proliferation, survival and poor prognosis in pancreatic cancer. Cancer Sci., 101, 1754-1760.
20. Tateishi, K. et al. (2006) Dysregulated expression of stem cell factor Bmi1 in precancerous lesions of the gastrointestinal tract. Clin. Cancer Res., 12, 6960-6966.
21. DeNicola, G.M. et al. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature, 475, 106-109.
22. Bardeesy, N. et al. (2006) Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc. Natl Acad. Sci. USA, 103, 5947-5952.
23. Mich, J.K. et al. (2014) Prospective identification of functionally distinct stem cells and neurosphere-initiating cells in adult mouse forebrain. Elife, 3, e02669.
24. Collins, M.A. et al. (2012) Oncogenic Kras is required for both the initiation and maintenance of pancreatic cancer in mice. J. Clin. Invest., 122, 639-653.
25. Hruban, R.H. et al. (2006) Pancreatic cancer in mice and man: the Penn Workshop 2004. Cancer Res., 66, 14-17.
26. Mathew, E. et al. (2014) The transcription factor GLI1 modulates the inflammatory response during pancreatic tissue remodeling. J. Biol. Chem., 289, 27727-27743.
27. Sangiorgi, E. et al. (2008) Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet., 40, 915-920.
28. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
29. Morris, J.P. 4th. et al. (2010) Beta-catenin blocks Kras-dependent reprogramming of acini into pancreatic cancer precursor lesions in mice. J. Clin. Invest., 120, 508-520.
30. Guerra, C. et al. (2011) Pancreatitis-induced inflammation contributes to pancreatic cancer by inhibiting oncogene-induced senescence. Cancer Cell, 19, 728-739.
31. Carrière, C. et al. (2011) Acute pancreatitis accelerates initiation and progression to pancreatic cancer in mice expressing oncogenic Kras in the nestin cell lineage. PLoS One, 6, e27725.
32. Lee, K.E. et al. (2010) Oncogenic KRas suppresses inflammation-associated senescence of pancreatic ductal cells. Cancer Cell, 18, 448-458.
33. Dovey, J.S. et al. (2008) Bmi1 is critical for lung tumorigenesis and bron-chioalveolar stem cell expansion. Proc. Natl Acad. Sci. USA, 105, 11857-11862.
34. Bruggeman, S.W. et al. (2007) Bmi1 controls tumor development in an Ink4a/Arf-independent manner in a mouse model for glioma. Cancer Cell, 12, 328-341.
35. Sparmann, A. et al. (2006) Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer, 6, 846-856.
36. Cao, R. et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science, 298, 1039-1043.
37. Mallen-St Clair, J. et al. (2012) EZH2 couples pancreatic regeneration to neoplastic progression. Genes Dev, 26, 439-444.
38. Kreso, A. et al. (2014) Self-renewal as a therapeutic target in human colorectal cancer. Nat. Med., 20, 29-36.