Notch signalling in cancer progression and bone metastasis

British Journal of Cancer

Volumn 105, Issue 12, 2011, Pages 1805-1810

  Sethi, N ^a,b   Kang, Y ^a,c  

^a PRINCETON UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Bone metastasis; Jagged1; Notch signalling; Tumour progression

Indexed keywords

GELATINASE B; INTERLEUKIN 6; JAGGED1; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; TOCILIZUMAB; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; NOTCH RECEPTOR;

ANGIOGENESIS; APOPTOSIS; BONE METASTASIS; BREAST CANCER; CANCER GROWTH; CANCER STAGING; CARCINOGENESIS; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CYTOKINE RELEASE; DROSOPHILA; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; KAPOSI SARCOMA; LUNG NON SMALL CELL CANCER; LYMPHATIC LEUKEMIA; MEDULLOBLASTOMA; MELANOMA; NONHUMAN; OSTEOBLAST; OVARY CARCINOMA; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; SIGNAL TRANSDUCTION; T CELL LEUKEMIA; TUMOR GROWTH; TUMOR MICROENVIRONMENT; BONE TUMOR; DISEASE COURSE; METABOLISM; METASTASIS;

BONE NEOPLASMS; DISEASE PROGRESSION; HUMANS; NEOPLASM METASTASIS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

EID: 84856008970     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2011.497     Document Type: Review

References (74)

1. Ara T, Song L, Shimada H, Keshelava N, Russell HV, Metelitsa LS, Groshen SG, Seeger RC, DeClerck YA (2009) Interleukin-6 in the bone marrow microenvironment promotes the growth and survival of neuroblastoma cells. Cancer Res 69: 329-337
2. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284: 770-776 (Pubitemid 29291335)
3. Balint K, Xiao M, Pinnix CC, Soma A, Veres I, Juhasz I, Brown EJ, Capobianco AJ, Herlyn M, Liu ZJ (2005) Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J Clin Invest 115: 3166-3176 (Pubitemid 41567581)
4. Bedogni B, Warneke JA, Nickoloff BJ, Giaccia AJ, Powell MB (2008) Notch1 is an effector of Akt and hypoxia in melanoma development. J Clin Invest 118: 3660-3670
5. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689 (Pubitemid 44268213)
6. Brou C, Logeat F, Gupta N, Bessia C, LeBail O, Doedens JR, Cumano A, Roux P, Black RA, Israel A (2000) A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin-metalloprotease TACE. Mol Cell 5: 207-216 (Pubitemid 30628080)
7. Curry CL, Reed LL, Golde TE, Miele L, Nickoloff BJ, Foreman KE (2005) Gamma secretase inhibitor blocks Notch activation and induces apoptosis in Kaposi's sarcoma tumor cells. Oncogene 24: 6333-6344 (Pubitemid 41486467)
8. D'Souza B, Miyamoto A, Weinmaster G (2008) The many facets of Notch ligands. Oncogene 27: 5148-5167
9. Dalton HE, Denton D, Foot NJ, Ho K, Mills K, Brou C, Kumar S (2011) Drosophila Ndfip is a novel regulator of Notch signaling. Cell Death Differ 18: 1150-1160
10. Dang TP, Gazdar AF, Virmani AK, Sepetavec T, Hande KR, Minna JD, Roberts JR, Carbone DP (2000) Chromosome 19 translocation, overexpression of Notch3, and human lung cancer. J Natl Cancer Inst 92: 1355-1357 (Pubitemid 30660597)
11. Dievart A, Beaulieu N, Jolicoeur P (1999) Involvement of Notch1 in the development of mouse mammary tumors. Oncogene 18: 5973-5981 (Pubitemid 29535009)
12. Ellisen LW, Bird J, West DC, Soreng AL, Reynolds TC, Smith SD, Sklar J (1991) TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66: 649-661 (Pubitemid 121001701)
13. Emmenegger U, Kerbel RS (2010) Cancer: Chemotherapy counteracted. Nature 468: 637-638
14. Francia G, Man S, Lee CJ, Lee CR, Xu P, Mossoba ME, Emmenegger U, Medin JA, Kerbel RS (2009) Comparative impact of trastuzumab and cyclophosphamide on HER-2-positive human breast cancer xenografts. Clin Cancer Res 15: 6358-6366
15. Gallahan D, Callahan R (1987) Mammary tumorigenesis in feral mice: identification of a new int locus in mouse mammary tumor virus (Czech II)-induced mammary tumors. J Virol 61: 66-74 (Pubitemid 17212445)
16. Gray GE, Mann RS, Mitsiadis E, Henrique D, Carcangiu ML, Banks A, Leiman J, Ward D, Ish-Horowitz D, Artavanis-Tsakonas S (1999) Human ligands of the Notch receptor. Am J Pathol 154: 785-794 (Pubitemid 29122597)
17. Greenwald I (1994) Structure/function studies of lin-12/Notch proteins. Curr Opin Genet Dev 4: 556-562 (Pubitemid 24249574)
18. Greenwald I (1998) LIN-12/Notch signaling: lessons from worms and flies. Gene Dev 12: 1751-1762 (Pubitemid 28304327)
19. Hallahan AR, Pritchard JI, Hansen S, Benson M, Stoeck J, Hatton BA, Russell TL, Ellenbogen RG, Bernstein ID, Beachy PA, Olson JM (2004) The SmoA1 mouse model reveals that notch signaling is critical for the growth and survival of sonic hedgehog-induced medulloblastomas. Cancer Res 64: 7794-7800 (Pubitemid 39446912)
20. Hamidi H, Gustafason D, Pellegrini M, Gasson J (2011) Identification of novel targets of CSL-dependent Notch signaling in hematopoiesis. PLoS One 6: e20022
21. Heitzler P, Simpson P (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64: 1083-1092 (Pubitemid 121001195)
22. Honjo T (1996) The shortest path from the surface to the nucleus: RBP-J kappa/Su(H) transcription factor. Genes Cells 1: 1-9 (Pubitemid 126673102)
23. Iso T, Kedes L, Hamamori Y (2003) HES and HERP families: multiple effectors of the Notch signaling pathway. J Cell Physiol 194: 237-255 (Pubitemid 36176887)
24. Jarriault S, Brou C, Logeat F, Schroeter EH, Kopan R, Israel A (1995) Signalling downstream of activated mammalian Notch. Nature 377: 355-358
25. Jhappan C, Gallahan D, Stahle C, Chu E, Smith GH, Merlino G, Callahan R (1992) Expression of an activated Notch-related int-3 transgene interferes with cell differentiation and induces neoplastic transformation in mammary and salivary glands. Genes Dev 6: 345-355
26. Kang Y, He W, Tulley S, Gupta GP, Serganova I, Chen CR, Manova-Todorova K, Blasberg R, Gerald WL, Massague J (2005) Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc Natl Acad Sci USA 102: 13909-13914 (Pubitemid 41377677)
27. Kang Y, Siegel PM, Shu W, Drobnjak M, Kakonen SM, Cordon-Cardo C, Guise TA, Massague J (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3: 537-549 (Pubitemid 36808649)
28. Karaczyn A, Bani-Yaghoub M, Tremblay R, Kubu C, Cowling R, Adams TL, Prudovsky I, Spicer D, Friesel R, Vary C, Verdi JM (2010) Two novel human NUMB isoforms provide a potential link between development and cancer. Neural Development 5: 31
29. Karlou M, Tzelepi V, Efstathiou E (2010) Therapeutic targeting of the prostate cancer microenvironment. Nat Rev Urol 7: 494-509
30. Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233
31. Korpal M, Kang Y (2010) Targeting the transforming growth factor-beta signalling pathway in metastatic cancer. Eur J Cancer 46: 1232-1240
32. Korpal M, Yan J, Lu X, Xu S, Lerit DA, Kang Y (2009) Imaging transforming growth factor-beta signaling dynamics and therapeutic response in breast cancer bone metastasis. Nat Med 15: 960-966
33. Leong KG, Niessen K, Kulic I, Raouf A, Eaves C, Pollet I, Karsan A (2007) Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J Exp Med 204: 2935-2948 (Pubitemid 350179562)
34. Logeat F, Bessia C, Brou C, LeBail O, Jarriault S, Seidah NG, Israel A (1998) The Notch1 receptor is cleaved constitutively by a furin-like convertase. Proc Natl Acad Sci USA 95: 8108-8112 (Pubitemid 28326074)
35. Lu X, Wang Q, Hu G, Van Poznak C, Fleisher M, Reiss M, Massague J, Kang Y (2009) ADAMTS1 and MMP1 proteolytically engage EGF-like ligands in an osteolytic signaling cascade for bone metastasis. Gene Dev 23: 1882-1894
36. Man S, Bocci G, Francia G, Green SK, Jothy S, Hanahan D, Bohlen P, Hicklin DJ, Bergers G, Kerbel RS (2002) Antitumor effects in mice of lowdose (metronomic) cyclophosphamide administered continuously through the drinking water. Cancer Res 62: 2731-2735 (Pubitemid 34525751)
37. Mitsiades CS, Mitsiades NS, Munshi NC, Richardson PG, Anderson KC (2006) The role of the bone microenvironment in the pathophysiology and therapeutic management of multiple myeloma: interplay of growth factors, their receptors and stromal interactions. Eur J Cancer 42: 1564-1573 (Pubitemid 44118771)
38. Mullendore ME, Koorstra JB, Li YM, Offerhaus GJ, Fan X, Henderson CM, Matsui W, Eberhart CG, Maitra A, Feldmann G (2009) Ligand-dependent Notch signaling is involved in tumor initiation and tumor maintenance in pancreatic cancer. Clin Cancer Res 15: 2291-2301
39. Mumm JS, Schroeter EH, Saxena MT, Griesemer A, Tian X, Pan DJ, Ray WJ, Kopan R (2000) A ligand-induced extracellular cleavage regulates gammasecretase-like proteolytic activation of Notch1. Mol Cell 5: 197-206 (Pubitemid 30628079)
40. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G (2006) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 444: 1032-1037 (Pubitemid 46018516)
41. Park JT, Li M, Nakayama K, Mao TL, Davidson B, Zhang Z, Kurman RJ, Eberhart CG, Shih Ie M, Wang TL (2006) Notch3 gene amplification in ovarian cancer. Cancer Res 66: 6312-6318
42. Pear WS, Aster JC, Scott ML, Hasserjian RP, Soffer B, Sklar J, Baltimore D (1996) Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J Exp Med 183: 2283-2291 (Pubitemid 26158919)
43. Raafat A, Bargo S, Anver MR, Callahan R (2004) Mammary development and tumorigenesis in mice expressing a truncated human Notch4/Int3 intracellular domain (h-Int3sh). Oncogene 23: 9401-9407 (Pubitemid 40069672)
44. Radtke F, Raj K (2003) The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer 3: 756-767 (Pubitemid 37328814)
45. Radtke F, Wilson A, Stark G, Bauer M, van Meerwijk J, MacDonald HR, Aguet M (1999) Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10: 547-558 (Pubitemid 29262657)
46. Reedijk M, Odorcic S, Chang L, Zhang H, Miller N, McCready DR, Lockwood G, Egan SE (2005) High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer Res 65: 8530-8537 (Pubitemid 41330622)
47. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M (2006) Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444: 1083-1087 (Pubitemid 46018529)
48. Rodilla V, Villanueva A, Obrador-Hevia A, Robert-Moreno A, Fernandez-Majada V, Grilli A, Lopez-Bigas N, Bellora N, Alba MM, Torres F, Dunach M, Sanjuan X, Gonzalez S, Gridley T, Capella G, Bigas A, Espinosa L (2009) Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci USA 106: 6315-6320
49. Sahlgren C, Gustafsson MV, Jin S, Poellinger L, Lendahl U (2008) Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci USA 105: 6392-6397 (Pubitemid 351758356)
50. Salgado R, Junius S, Benoy I, Van Dam P, Vermeulen P, Van Marck E, Huget P, Dirix LY (2003) Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer 103: 642-646 (Pubitemid 36091468)
51. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB, Chieco P, Bonafe M (2007) IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 117: 3988-4002 (Pubitemid 350224108)
52. Santagata S, Demichelis F, Riva A, Varambally S, Hofer MD, Kutok JL, Kim R, Tang J, Montie JE, Chinnaiyan AM, Rubin MA, Aster JC (2004) JAGGED1 expression is associated with prostate cancer metastasis and recurrence. Cancer Res 64: 6854-6857 (Pubitemid 39330990)
53. Sasser AK, Sullivan NJ, Studebaker AW, Hendey LF, Axel AE, Hall BM (2007) Interleukin-6 is a potent growth factor for ER-alpha-positive human breast cancer. FASEB J 21: 3763-3770 (Pubitemid 350075164)
54. Sassoli C, Pini A, Mazzanti B, Quercioli F, Nistri S, Saccardi R, Zecchi-Orlandini S, Bani D, Formigli L (2011) Mesenchymal stromal cells affect cardiomyocyte growth through juxtacrine Notch-1/Jagged-1 signaling and paracrine mechanisms: clues for cardiac regeneration. J Mol Cell Cardiol 51: 399-408
55. Schroeter EH, Kisslinger JA, Kopan R (1998) Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393: 382-386 (Pubitemid 28269713)
56. Sethi N, Kang Y (2011) Dysregulation of developmental pathways in bone metastasis. Bone 48: 16-22
57. Sethi N, Dai X, Winter CG, Kang Y (2011) Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells. Cancer Cell 19: 192-205
58. Sethi N, Yan Y, Quek D, Schupbach T, Kang Y (2010) Rabconnectin-3 is a functional regulator of mammalian Notch signaling. J Biol Chem 285: 34757-34764
59. Shih Ie M, Wang TL (2007) Notch signaling, gamma-secretase inhibitors, and cancer therapy. Cancer Res 67: 1879-1882
60. Six E, Ndiaye D, Laabi Y, Brou C, Gupta-Rossi N, Israel A, Logeat F (2003) The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase. Proc Natl Acad Sci USA 100: 7638-7643 (Pubitemid 36760022)
61. Sprinzak D, Lakhanpal A, Lebon L, Santat LA, Fontes ME, Anderson GA, Garcia-Ojalvo J, Elowitz MB (2010) Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465: 86-90
62. Studebaker AW, Storci G, Werbeck JL, Sansone P, Sasser AK, Tavolari S, Huang T, Chan MW, Marini FC, Rosol TJ, Bonafe M, Hall BM (2008) Fibroblasts isolated from common sites of breast cancer metastasis enhance cancer cell growth rates and invasiveness in an interleukin-6-dependent manner. Cancer Res 68: 9087-9095
63. Stylianou S, Clarke RB, Brennan K (2006) Aberrant activation of notch signaling in human breast cancer. Cancer Res 66: 1517-1525 (Pubitemid 43259933)
64. Timmerman LA, Grego-Bessa J, Raya A, Bertran E, Perez-Pomares JM, Diez J, Aranda S, Palomo S, McCormick F, Izpisua-Belmonte JC, de la Pompa JL (2004) Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Gene dev 18: 99-115 (Pubitemid 38090691)
65. Wang XY, Yin Y, Yuan H, Sakamaki T, Okano H, Glazer RI (2008) Musashi1 modulates mammary progenitor cell expansion through proliferin-mediated activation of the Wnt and Notch pathways. Mol cell biol 28: 3589-3599 (Pubitemid 351732897)
66. Wang Z, Banerjee S, Li Y, Rahman KM, Zhang Y, Sarkar FH (2006) Down-regulation of notch-1 inhibits invasion by inactivation of nuclear factor-kappaB, vascular endothelial growth factor, and matrix metalloproteinase-9 in pancreatic cancer cells. Cancer Res 66: 2778-2784
67. Weijzen S, Rizzo P, Braid M, Vaishnav R, Jonkheer SM, Zlobin A, Osborne BA, Gottipati S, Aster JC, Hahn WC, Rudolf M, Siziopikou K, Kast WM, Miele L (2002) Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med 8: 979-986 (Pubitemid 35033702)
68. Weng AP, Ferrando AA, Lee W, Morris JPt, Silverman LB, Sanchez-Irizarry C, Blacklow SC, Look AT, Aster JC (2004) Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271 (Pubitemid 39336870)
69. Wu L, Aster JC, Blacklow SC, Lake R, Artavanis-Tsakonas S, Griffin JD (2000) MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat Genet 26: 484-489
70. Zang S, Ji C, Qu X, Dong X, Ma D, Ye J, Ma R, Dai J, Guo D (2007) A study on Notch signaling in human breast cancer. Neoplasma 54: 304-310
71. Zavadil J, Cermak L, Soto-Nieves N, Bottinger EP (2004) Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. Embo J 23: 1155-1165 (Pubitemid 38436879)
72. Zeng Q, Li S, Chepeha DB, Giordano TJ, Li J, Zhang H, Polverini PJ, Nor J, Kitajewski J, Wang CY (2005) Crosstalk between tumor and endothelial cells promotes tumor angiogenesis by MAPK activation of Notch signaling. Cancer Cell 8: 13-23 (Pubitemid 40991811)
73. Zhang GJ, Adachi I (1999) Serum interleukin-6 levels correlate to tumor progression and prognosis in metastatic breast carcinoma. Anticancer Res 19: 1427-1432 (Pubitemid 29257471)
74. Zunich SM, Douglas T, Valdovinos M, Chang T, Bushman W, Walterhouse D, Iannaccone P, Lamm ML (2009) Paracrine sonic hedgehog signalling by prostate cancer cells induces osteoblast differentiation. Mol cancer 8: 12