Opposing role of Notch1 and Notch2 in a Kras G12D -driven murine non-small cell lung cancer model

Oncogene

Volumn 34, Issue 5, 2015, Pages 578-588

  Baumgart, A ^a   Mazur, P K ^b   Anton, M ^a   Rudelius, M ^a   Schwamborn, K ^a   Feuchtinger, A ^c   Behnke, K ^a   Walch, A ^c   Braren, R ^a   Peschel, C ^a   Duyster, J ^d   Siveke, J T ^a   Dechow, T ^a,e  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b STANFORD UNIVERSITY   (United States)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e Onkologie Ravensburg   (Germany)

Author keywords

beta catenin; DUSP1; mouse model; Notch; Ras

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; BETA CATENIN; DUSP1 PROTEIN, MOUSE; HES1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; KRAS2 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; NOTCH1 PROTEIN, MOUSE; NOTCH1 RECEPTOR; NOTCH2 PROTEIN, MOUSE; NOTCH2 RECEPTOR; PROTEIN P21;

ANIMAL; BIOSYNTHESIS; CELL PROLIFERATION; CELL TRANSFORMATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MOUSE; NON SMALL CELL LUNG CANCER; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BETA CATENIN; CARCINOMA, NON-SMALL-CELL LUNG; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DUAL SPECIFICITY PHOSPHATASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MICE; PROTO-ONCOGENE PROTEINS P21(RAS); RECEPTOR, NOTCH1; RECEPTOR, NOTCH2; SIGNAL TRANSDUCTION;

EID: 84893199350     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.592     Document Type: Article

References (56)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics. CA: a cancer journal for clinicians 2010; 60: 277-300.
2. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999; 284: 770-776.
3. Bray SJ. Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 2006; 7: 678-689.
4. Ellisen LW, Bird J, West DC, Soreng AL, Reynolds TC, Smith SD et al. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 1991; 66: 649-661.
5. Baumgart A, Seidl S, Vlachou P, Michel L, Mitova N, Schatz N et al. ADAM17 regulates ep idermal growth factor receptor expression through the activation of Notch1 in non-small cell lung cancer. Cancer Res 2010; 70: 5368-5378.
6. Mazur PK, Gruner BM, Nakhai H, Sipos B, Zimber-Strobl U , Strobl LJ et al. Identification of epidermal Pdx1 expression discloses different roles of Notch1 and Notch2 in murine Kras(G12D)-induced skin carcinogenesis in vivo. PLoS One 2010; 5: e13578.
7. Ma zur PK, Einwachter H, Lee M, Sipos B, Nakhai H, Rad R et al. Notch2 is required for progression of pancreatic intraepithelial neoplasia and development of pancreatic ductal adenocarcinoma. Proc Natl Acad Sci USA 2010 ; 107: 13438-13443.
8. Weijzen S, Rizzo P, Braid M, Vaishnav R, Jonkheer SM, Zlobin A et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nature Med 2002; 8: 979-986.
9. Talora C, Sgroi DC, Crum CP, Dotto GP. Specific down-modulation of Notch1 signaling in cervical cancer cells is required for sustained HPV-E6/E7 expression and late s teps of malignant transformation. Genes Develop 2002; 16: 2252-2263.
10. Westhoff B, Colaluca IN, D'Ario G, Donzelli M, Tosoni D, Volorio S et al. Alterations of the Notch pathway in l ung cancer. Proc Natl Acad Sci USA 2009; 106: 22293-22298.
11. Konishi J, Kawaguchi KS, Vo H, Haruki N, Gonzalez A, Carbone DP et al. Gamma-secretase inhibitor prevents Notch3 activati on and reduces proliferation in human lung cancers. Cancer Res 2007; 67: 8051-8057.
12. Zheng Y, de la Cruz CC, Sayles LC, Alleyne-Chin C, Vaka D, Knaak TD et al. A rare population of CD24(+)ITGB4(+ )Notch(hi) cells drives tumor propagation in NSCLC and requires Notch3 for self-renewal. Cancer Cell 2013; 24: 59-74.
13. ClinicalTrals.gov http://clinicaltrials.gov/
14. Maraver A, Serrano M. Notching up a new therapeutic strategy for non-small cell lung carcinoma (NSCLC). Oncotarget 2012; 3: 917-918.
15. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M et al. Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 2003; 33: 416-421.
16. Sriuranpong V, Borges MW, Ravi RK, Arnold DR, Nelkin BD, B aylin SB et al. Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res 2001; 61: 3200-3205.
17. Jackson EL, Willis N, Mercer K, Bronson RT, Crowley D, Mo ntoya R et al. Analysis of lung tumor initiation and progression using conditional expression of oncogenic K-ras. Genes Develop 2001; 15: 3243-3248.
18. DuPage M, Dooley AL, Jacks T. Conditional mouse lung cancer models using adenoviral or lentiviral delivery of Cre recombinase. Nat Protocols 2009; 4: 1064-1072.
19. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 2009; 137: 216-233.
20. Junttila MR, Karnezis AN, Garcia D, Madriles F, Kortlever RM, Rostker F et al. Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 2010; 468: 567-571.
21. Maraver A, Fernandez-Marcos PJ, Herranz D, Canamero M, Munoz-Martin M, Gomez-Lopez G et al. Therapeutic effect of gamma-secretase i nhibition in KrasG12V-driven non-small cell lung carcinoma by derepression of DUSP1 and inhibition of ERK. Cancer Cell 2012; 22: 222-234.
22. Hanlon L, Avila JL, Demarest RM, Troutman S, Allen M, Ratti F et al. Notch1 functions as a tumor suppressor in a model of K-ras-induced pancreatic ductal adenocarcinoma. Cancer Res 2010; 70: 4280-4286.
23. Fan X, Mikolaenko I, Elhassan I, Ni X, Wang Y, Ball D et al. Notch1 and notch2 have opposite effects on embryonal brain tumor growth. Cancer Res 2004; 64: 7787-7793.
24. Rodenhuis S, Slebos RJ, Boot AJ, Evers SG, Mo oi WJ, Wagenaar SS et al. Incidence and possible clinical significance of K-ras oncogene activation in adenocarcinoma of the human lung. Cancer Res 1988; 48: 5738-5741.
25. Sato M, Vaughan MB, Girard L, Peyton M, Lee W, Shames DS et al. Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res 2006; 66: 2116-2128.
26. Radtke F, Raj K. The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nature Rev Cancer 2003; 3: 756-767.
27. Besseyrias V, Fiorini E, Strobl LJ, Zimber-Strobl U, Dumortier A, Koch U et al. Hierarchy of Notch-Delta interactions promoting T cell lineage commitment and maturation. J Exp Med 2007; 204: 331-343.
28. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21: 70-71.
29. Feldser DM, Kostova KK, Winslow MM, Taylor SE, Cashman C, Whit taker CA et al. Stage-specific sensitivity to p53 restoration during lung cancer progression. Nature 2010; 468: 572-575.
30. Haruki N, Kawaguchi KS, Eichenberger S, Massion PP, Olson S, Gonzalez A et al. Dominant-negative Notch3 receptor inhibits mitogen-activated protein kinase pathway and the growth of human lung cancers. Cancer Res 2005; 65: 3555-3561.
31. Kim MY, Park JH, Choi EJ, Park HS. Presenilin acts as a positive regulator of basal level activity of ERK through the Raf-MEK1 signaling pathway. Biochem Biophys Res Commun 2005; 332: 609-613.
32. Michie AM, Chan AC, Ciofani M, Carleton M, Lefebvre JM, He Y et al. Constitutive Notch signalling promotes CD4 CD8 thymocyte differentiation in the absence of the pre-TCR complex, by mimicking pre-TCR signals. Int Immunol 2007; 19: 1421-1430.
33. Kim HA, Koo BK, Cho JH, Kim YY, Seong J, Chang HJ et al. Notch1 counteracts WNT/beta-catenin signaling through chromatin modification in colorectal cancer. J Clin Invest 2012; 122: 3248-3259.
34. Pacheco-Pinedo EC,Durham AC,Stewart KM,Goss AM,Lu MM,Demayo FJ,et al Wnt/beta-catenin signaling accelerates mouse lung tumorigenesis by imposing an embryonic distal prog enitor phenotype on lung epithelium J Clin Invest 2011 121, 1935-1945.
35. Peignon G, Durand A, Cacheux W, Ayrault O, Terris B, Laurent-Puig P et al. Complex interplay between b eta-catenin signalling and Notch effectors in intestinal tumorigenesis. Gut 2011; 60: 166-176.
36. Jackson EL, Olive KP, Tuveson DA, Bronson R, Crowley D, Brown M et al. The different ial effects of mutant p53 alleles on advanced murine lung cancer. Cancer Res 2005; 65: 10280-10288.
37. Asnaghi L, Vass WC, Quadri R, Day PM, Qian X, Braverman R et al. E-cadherin nega tively regulates neoplastic growth in non-small cell lung cancer: role of Rho GTPases. Oncogene 2010; 29: 2760-2771.
38. Bremnes RM, Veve R, Hirsch FR, Franklin WA. The E-cadherin cell-cell adhesion complex and lung cancer invasion, metastasis, and prognosis. Lung Cancer 2002; 36: 115-124.
39. Wang XQ, Li H, Van Putten V, Winn RA, Heasley LE, Nemenoff RA. Oncogenic K-Ras regulates proliferation and cell junctions in lung epithelial cells through induction of cyclooxygenase-2 and activation of metalloproteinase-9. Mol Biol Cell 2009; 20: 791-800.
40. Ma L, Young J, Prabhala H, P an E, Mestdagh P, Muth D et al. miR-9, a MYC/MYCNactivated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol 2010; 12: 247-256.
41. Saad AG, Yeap BY, Thunnissen FB, Pinkus GS, Pinkus JL, Loda M et al. Immunohistochemical markers associated with brain metastases in patients with nonsmall cell lung carcinoma. Cancer 2008; 113: 2129-2138.
42. von Burstin J, Eser S, Paul MC, Seidler B, Brandl M, Messer M et al. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex. Gastroenterol ogy 2009; 137: 361-371371 e361-365.
43. Myong NH. Reduced expression of E-cadherin in human non-small cell lung carcinoma. Cancer Res Treatment 2004; 36: 56-61.
44. Sjolund J, Johansson M, Manna S, Norin C, Pietras A, Beckman S et al. Suppression of renal cell carcinoma growth by inhibition of Notch signaling in vitro and in vivo. J Clin Invest 2008; 118: 217-228.
45. Huynh C, Poliseno L, Segura MF, Medicherla R, Haimovic A, Menendez S et al. The novel gamma secretase inhibitor RO4929097 reduces the tumor initiating potential of melanoma. PLoS One 2011; 6: e25 264.
46. van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H et al. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Na ture 2005; 435: 959-963.
47. Wu Y, Cain-Hom C, Choy L, Hagenbeek TJ, de Leon GP, Chen Y et al. Therapeutic antibody targeting of individual Notch receptors. Nature 2010; 464: 1052-1057.
48. Allen TD, Rodriguez EM, Jones KD, Bishop JM. Activated Notch1 induces lung adenomas in mice and cooperates with Myc in the generation of lung adenocarcinoma. Cancer Res 2011; 71: 6010-6018.
49. Osanyingbemi-Obidi J, Dobromilskaya I, Illei PB, Hann CL, Rudin CM. Notch signaling contributes to lung cancer clonogenic capacity in vitro but may be circumvented in tumorigenesis in vivo. Mol Cancer Res 2011; 9: 1746-1754.
50. Eliasz S, Liang S, Chen Y, De Marco MA, Machek O, Skucha S et al. Notch-1 stimulates survival of lung adenocarcinoma cells during hypoxia by acti vating the IGF-1R pathway. Oncogene 2010; 29: 2488-2498.
51. Graziani I, Eliasz S, De Marco MA, Chen Y, Pass HI, De May RM et al. Opposite effects of Notch-1 and Notch-2 on mesothelio ma cell survival under hypoxia are exerted through the Akt pathway. Cancer Res 2008; 68: 9678-9685.
52. Cheng HT, Kim M, Valerius MT, Surendran K, Schuster-Gossler K, Gossler A et al. Notch2, but not Notch1, is required for proximal fate acquisition in the mammalian nephron. Development 2007; 134: 801-811.
53. Chu D, Zheng J, Wang W, Zhao Q, Li Y, Li J et al. Notch2 expression is decreased in colorectal cancer and related to tumor differentiation status. Ann Surg Oncol 2009; 16: 3259-3266.
54. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonal d HR et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 1999; 10: 547-558.
55. Bettstetter M, Berezowska S, Keller G, Walch A, Feuchtinger A, Slotta-Huspenina J et al. Epidermal growth factor receptor, phosphatidylinositol-3-kinase catalytic subunit/PTEN, and KRAS/NRAS/BRAF in primary resected esophageal adenocarcinomas: loss of PTEN is associated with worse clinical outcome. Human Pathol 2013; 44: 829-836.
56. Slotta-Huspenina J,Koch I,de Leval L,Keller G,Klier M,Bink K,et al The impact of cyclin D1 mRNA isoforms, morpholog y and p53 in mantle cell lymphoma: p53 alterations and blastoid morphology are strong predictors of a high proliferation index Haematologica 2012 97: 1422-1430.