A Notch1neuregulin1 autocrine signaling loop contributes to melanoma growth

Oncogene

Volumn 31, Issue 43, 2012, Pages 4609-4618

  Zhang, K ^a   Wong, P ^a   Zhang, L ^a   Jacobs, B ^b   Borden, E C ^b   Aster, J C ^c   Bedogni, B ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

ERBB: erythroblastic leukemia viral oncogene homolog or EGF (epidermal growth factor) family of transmembrane receptor tyrosine kinases; NIC: Notch1 intracellular domain; Notch1 TM: transmembrane Notch1; NRG1: neuregulin1; p27KIP1: CDKN1B: cyclin dependent kinase inhibitor 1B

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1B; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; NEU DIFFERENTIATION FACTOR; NOTCH1 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECOMBINANT PROTEIN; NOTCH1 PROTEIN, HUMAN; NRG1 PROTEIN, HUMAN;

ARTICLE; AUTOCRINE EFFECT; CANCER GROWTH; CANCER INHIBITION; CONTROLLED STUDY; DRUG TARGETING; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MELANOMA; PRIORITY JOURNAL; PROMOTER REGION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; GENETICS; METABOLISM; PATHOLOGY; SKIN TUMOR;

HUMANS; MELANOMA; NEUREGULIN-1; PROMOTER REGIONS, GENETIC; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; SKIN NEOPLASMS;

EID: 84867897035     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.606     Document Type: Article

References (53)

1. Altekruse SF KC, Krapcho M, Neyman N, Aminou R, Waldron W, Ruhl J et al. SEER Cancer Statistics Review 1975. 20072010.
2. Herzog C, Pappo A, Bondy M, Bleyer A, Kirkwood J. Cancer epidemiology in older adolescents and young adults. SEER AYA Monograph 2007; 53-63.
3. Hardy KM, Kirschmann DA, Seftor EA, Margaryan NV, Postovit LM, Strizzi L et al. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res 2010; 70: 10340-10350.
4. Zhou K, Huang L, Zhou Z, Hu C, Liu W, Zhou J et al. Wnt and Notch signaling pathways selectively regulating hematopoiesis. Ann Hematol 2010; 89: 749-757.
5. Brabletz S, Schmalhofer O, Brabletz T. Gastrointestinal stem cells in development and cancer. J Pathol 2009; 217: 307-317.
6. Imayoshi I, Sakamoto M, Yamaguchi M, Mori K, Kageyama R. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J Neurosci 2010; 30: 3489-3498.
7. 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. (Pubitemid 121001701)
8. Konishi J, Kawaguchi KS, Vo H, Haruki N, Gonzalez A, Carbone DP et al. Gammasecretase inhibitor prevents Notch3 activation and reduces proliferation in human lung cancers. Cancer Res 2007; 67: 8051-8057. (Pubitemid 47395139)
9. Pahlman S, Stockhausen MT, Fredlund E, Axelson H. Notch signaling in neuroblastoma. Semin Cancer Biol 2004; 14: 365-373. (Pubitemid 38993638)
10. Rangarajan A, Syal R, Selvarajah S, Chakrabarti O, Sarin A, Krishna S. Activated Notch1 signaling cooperates with papillomavirus oncogenes in transformation and generates resistance to apoptosis on matrix withdrawal through PKB/Akt. Virology 2001; 286: 23-30. (Pubitemid 32675462)
11. Santagata S, Demichelis F, Riva A, Varambally S, Hofer MD, Kutok JL et al. JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res 2004; 64: 6854-6857. (Pubitemid 39330990)
12. 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.
13. Gilbert CA, Daou MC, Moser RP, Ross AH. Gamma-secretase inhibitors enhance temozolomide treatment of human gliomas by inhibiting neurosphere repopulation and xenograft recurrence. Cancer Res 2010; 70: 6870-6879.
14. Hovinga KE, Shimizu F, Wang R, Panagiotakos G, Van Der Heijden M, Moayedpardazi H et al. Inhibition of notch signaling in glioblastoma targets cancer stem cells via an endothelial cell intermediate. Stem Cells 2010; 28: 1019-1029.
15. Osawa M, Fisher DE. Notch and melanocytes: diverse outcomes from a single signal. J Invest Dermatol 2008; 128: 2571-2574.
16. Bedogni B, Warneke JA, Nickoloff BJ, Giaccia AJ, Powell MB. Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest 2008; 118: 3660-3670.
17. Pinnix CC, Lee JT, Liu ZJ, McDaid R, Balint K, Beverly LJ et al. Active Notch1 confers a transformed phenotype to primary human melanocytes. Cancer Res 2009; 69: 5312-5320.
18. Liu ZJ, Xiao M, Balint K, Smalley KS, Brafford P, Qiu R et al. Notch1 signaling promotes primary melanoma progression by activating mitogen-activated protein kinase/phosphatidylinositol 3-kinase-Akt pathways and up-regulating N-cadherin expression. Cancer Res 2006; 66: 4182-4190.
19. Balint K, Xiao M, Pinnix CC, Soma A, Veres I, Juhasz I et al. Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J Clin Invest 2005; 115: 3166-3176. (Pubitemid 41567581)
20. Wieduwilt MJ, Moasser MM. The epidermal growth factor receptor family: biology driving targeted therapeutics. Cell Mol Life Sci 2008; 65: 1566-1584.
21. Buac K, Xu M, Cronin J, Weeraratna AT, Hewitt SM, Pavan WJ. NRG1/ERBB3 signaling in melanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res 2009; 22: 773-784.
22. Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M et al. HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res 2008; 14: 5188-5197.
23. Prickett TD, Agrawal NS, Wei X, Yates KE, Lin JC, Wunderlich JR et al. Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat Genet 2009; 41: 1127-1132.
24. Woodhoo A, Alonso MB, Droggiti A, Turmaine M, D'Antonio M, Parkinson DB et al. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat Neurosci 2009; 12: 839-847.
25. Magnifico A, Albano L, Campaner S, Delia D, Castiglioni F, Gasparini P et al. Tumorinitiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res 2009; 15: 2010-2021.
26. Korkaya H, Paulson A, Iovino F, Wicha MS. HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene 2008; 27: 6120-6130.
27. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004; 6: 1-6. (Pubitemid 38391943)
28. Talantov D, Mazumder A, Yu JX, Briggs T, Jiang Y, Backus J et al. Novel genes associated with malignant melanoma but not benign melanocytic lesions. Clin Cancer Res 2005; 11: 7234-7242. (Pubitemid 41507680)
29. Riker AI, Enkemann SA, Fodstad O, Liu S, Ren S, Morris C et al. The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med Genomics 2008; 1: 13.
30. Johansson P, Pavey S, Hayward N. Confirmation of a BRAF mutation-associated gene expression signature in melanoma. Pigment Cell Res 2007; 20: 216-221. (Pubitemid 46776377)
31. Hoek KS, Schlegel NC, Brafford P, Sucker A, Ugurel S, Kumar R et al. Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res 2006; 19: 290-302. (Pubitemid 44015592)
32. Calvo M, Zhu N, Grist J, Ma Z, Loeb JA, Bennett DL. Following nerve injury neuregulin-1 drives microglial proliferation and neuropathic pain via the MEK/ERK pathway. Glia 2011; 59: 554-568.
33. Ieguchi K, Fujita M, Ma Z, Davari P, Taniguchi Y, Sekiguchi K et al. Direct binding of the EGF-like domain of neuregulin-1 to integrins ({alpha}v{beta}3 and {alpha}6{beta}4) is involved in neuregulin-1/ErbB signaling. J Biol Chem 2010; 285: 31388-31398.
34. Fukazawa R, Miller TA, Kuramochi Y, Frantz S, Kim YD, Marchionni MA et al. Neuregulin-1 protects ventricular myocytes from anthracycline-induced apoptosis via erbB4-dependent activation of PI3-kinase/Akt. J Mol Cell Cardiol 2003; 35: 1473-1479. (Pubitemid 37491190)
35. Liang J, Slingerland JM. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003; 2: 339-345.
36. Shin I, Rotty J, Wu FY, Arteaga CL. Phosphorylation of p27Kip1 at Thr-157 interferes with its association with importin alpha during G1 and prevents nuclear re-entry. J Biol Chem 2005; 280: 6055-6063. (Pubitemid 40280089)
37. Shin I, Yakes FM, Rojo F, Shin NY, Bakin AV, Baselga J et al. PKB/Akt mediates cellcycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat Med 2002; 8: 1145-1152. (Pubitemid 35175970)
38. Lin HK, Wang G, Chen Z, Teruya-Feldstein J, Liu Y, Chan CH et al. Phosphorylationdependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol 2009; 11: 420-432.
39. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 2009; 11: 397-408.
40. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009; 9: 463-475.
41. Chen X, Levkowitz G, Tzahar E, Karunagaran D, Lavi S, Ben-Baruch N et al. An immunological approach reveals biological differences between the two NDF/heregulin receptors, ErbB-3 and ErbB-4. J Biol Chem 1996; 271: 7620-7629. (Pubitemid 26107041)
42. Rasul S, Balasubramanian R, Filipovic A, Slade MJ, Yague E, Coombes RC. Inhibition of gamma-secretase induces G2/M arrest and triggers apoptosis in breast cancer cells. Br J Cancer 2009; 100: 1879-1888.
43. Pancewicz J, Taylor JM, Datta A, Baydoun HH, Waldmann TA, Hermine O et al. Notch signaling contributes to proliferation and tumor formation of human T-cell leukemia virus type 1-associated adult T-cell leukemia. Proc Natl Acad Sci USA 2010; 107: 16619-16624.
44. Birchmeier C. ErbB receptors and the development of the nervous system. Exp Cell Res 2009; 315: 611-618.
45. Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V et al. Phospho-proteomic screen identifies potential therapeutic targets in melanoma. Mol Cancer Res 2011.
46. 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 activating the IGF-1R pathway. Oncogene 2010; 29: 2488-2498.
47. Osipo C, Patel P, Rizzo P, Clementz AG, Hao L, Golde TE et al. ErbB-2 inhibition activates Notch-1 and sensitizes breast cancer cells to a gamma-secretase inhibitor. Oncogene 2008; 27: 5019-5032.
48. Dong Y, Li A, Wang J, Weber JD, Michel LS. Synthetic lethality through combined Notch-epidermal growth factor receptor pathway inhibition in basal-like breast cancer. Cancer Res 2010; 70: 5465-5474.
49. Gupta PB, Kuperwasser C, Brunet JP, Ramaswamy S, Kuo WL, Gray JW et al. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet 2005; 37: 1047-1054. (Pubitemid 41486656)
50. Razorenova OV, Agapova LS, Budanov AV, Ivanov AV, Strunina SM, Chumakov PM. [Retroviral reporter systems for the assessment of activity of stress-induced signal transduction pathways controlled by p53, HIF-1 and HSF-1 transcription factors]. Mol Biol (Mosk) 2005; 39: 286-293. (Pubitemid 44558335)
51. Palomero T, Lim WK, Odom DT, Sulis ML, Real PJ, Margolin A et al. NOTCH1 directly regulates c-MYC and activates a feed-forward-loop transcriptional network promoting leukemic cell growth. Proc Natl Acad Sci USA 2006; 103: 18261-18266. (Pubitemid 44871646)
52. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997; 88: 593-602. (Pubitemid 27152402)
53. Arbiser JL, Moses MA, Fernandez CA, Ghiso N, Cao Y, Klauber N et al. Oncogenic H-ras stimulates tumor angiogenesis by two distinct pathways. Proc Natl Acad Sci USA 1997; 94: 861-866. (Pubitemid 27074412)