Fibroblast-derived neuregulin 1 promotes Compensatory ErbB3 receptor signaling in mutant BRAF melanoma

Journal of Biological Chemistry

Volumn 290, Issue 40, 2015, Pages 24267-24277

  Capparelli, Claudia ^a   Rosenbaum, Sheera ^a   Berger, Adam C ^a   Aplin, Andrew E ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CHEMICAL ACTIVATION; DERMATOLOGY; ONCOLOGY; TUMORS;

CONDITIONED MEDIUM; DERMAL FIBROBLASTS; GROWTH FACTOR RECEPTORS; GROWTH PROPERTIES; PARACRINE MANNERS; PROTECTIVE EFFECTS; RECEPTOR SIGNALING; TUMOR MICROENVIRONMENT;

FIBROBLASTS;

B RAF KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; NEU DIFFERENTIATION FACTOR; PROTEIN KINASE B; VEMURAFENIB; BRAF PROTEIN, HUMAN; ERBB3 PROTEIN, HUMAN; INDOLE DERIVATIVE; LIGAND; NRG1 PROTEIN, HUMAN; RECOMBINANT PROTEIN; SMALL INTERFERING RNA; SULFONAMIDE;

ARTICLE; CANCER ASSOCIATED FIBROBLAST; CANCER GROWTH; CANCER RESISTANCE; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FIBROBLAST; HUMAN; HUMAN CELL; MELANOMA; MELANOMA CELL; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; BIOPSY; CELL PROLIFERATION; CHEMISTRY; COCULTURE; DNA SEQUENCE; GENE EXPRESSION REGULATION; METABOLISM; MUTATION; SKIN; SKIN TUMOR; TUMOR CELL LINE; UPREGULATION;

BIOPSY; CELL LINE, TUMOR; CELL PROLIFERATION; COCULTURE TECHNIQUES; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLES; LIGANDS; MELANOMA; MUTATION; NEUREGULIN-1; PROTO-ONCOGENE PROTEINS B-RAF; RECEPTOR, ERBB-3; RECOMBINANT PROTEINS; RNA, SMALL INTERFERING; SEQUENCE ANALYSIS, DNA; SIGNAL TRANSDUCTION; SKIN; SKIN NEOPLASMS; SULFONAMIDES; UP-REGULATION;

EID: 84943339598     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.657270     Document Type: Article

References (49)

1. Flaherty, K. T., Infante, J. R., Daud, A., Gonzalez, R., Kefford, R. F., Sosman, J., Hamid, O., Schuchter, L., Cebon, J., Ibrahim, N., Kudchadkar, R., Burris, H. A., 3rd., Falchook, G., Algazi, A., Lewis, K., Long, G. V., Puzanov, I., Lebowitz, P., Singh, A., Little, S., Sun, P., Allred, A., Ouellet, D., Kim, K. B., Patel, K., and Weber, J. (2012) Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N. Engl. J. Med. 367, 1694-1703
2. Sosman, J. A., Kim, K. B., Schuchter, L., Gonzalez, R., Pavlick, A. C., Weber, J. S., McArthur, G. A., Hutson, T. E., Moschos, S. J., Flaherty, K. T., Hersey, P., Kefford, R., Lawrence, D., Puzanov, I., Lewis, K. D., Amaravadi, R. K., Chmielowski, B., Lawrence, H. J., Shyr, Y., Ye, F., Li, J., Nolop, K. B., Lee, R. J., Joe, A. K., and Ribas, A. (2012) Survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N. Engl. J. Med. 366, 707-714
3. Hauschild, A., Grob, J. J., Demidov, L. V., Jouary, T., Gutzmer, R., Millward, M., Rutkowski, P., Blank, C. U., Miller, W. H., Jr., Kaempgen, E., Martín-Algarra, S., Karaszewska, B., Mauch, C., Chiarion-Sileni, V., Martin, A. M., Swann, S., Haney, P., Mirakhur, B., Guckert, M. E., Goodman, V., and Chapman, P. B. (2012) Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3randomised controlled trial. Lancet 380, 358-365
4. Hartsough, E., Shao, Y., and Aplin, A. E. (2014) Resistance to RAF inhibitors revisited. J. Invest. Dermatol. 134, 319-325
5. Nazarian, R., Shi, H., Wang, Q., Kong, X., Koya, R. C., Lee, H., Chen, Z., Lee, M. K., Attar, N., Sazegar, H., Chodon, T., Nelson, S. F., McArthur, G., Sosman, J. A., Ribas, A., and Lo, R. S. (2010) Melanomas acquire resistance to B-RAF (V600E) inhibition by RTK or N-RAS upregulation. Nature 468, 973-977
6. Poulikakos, P. I., Persaud, Y., Janakiraman, M., Kong, X., Ng, C., Moriceau, G., Shi, H., Atefi, M., Titz, B., Gabay, M. T., Salton, M., Dahlman, K. B., Tadi, M., Wargo, J. A., Flaherty, K. T., Kelley, M. C., Misteli, T., Chapman, P. B., Sosman, J. A., Graeber, T. G., Ribas, A., Lo, R. S., Rosen, N., and Solit, D. B. (2011) RAF inhibitor resistance is mediated by dimerization of aberrantly spliced BRAF (V600E). Nature 480, 387-390
7. Hartsough, E. J., Basile, K. J., and Aplin, A. E. (2014) Beneficial effects of RAF inhibitor in mutant BRAF splice variant-expressing melanoma. Mol. Cancer Res. 12, 795-802
8. Basile, K. J., Abel, E. V., Dadpey, N., Hartsough, E. J., Fortina, P., and Aplin, A. E. (2013) In vivo MAPK reporting reveals the heterogeneity in tumoral selection of resistance to RAF inhibitors. Cancer Res. 73, 7101-7110
9. Villanueva, J., Vultur, A., and Herlyn, M. (2011) Resistance to BRAF inhibitors: unraveling mechanisms and future treatment options. Cancer Res. 71, 7137-7140
10. Abel, E. V., Basile, K. J., Kugel, C. H., 3rd., Witkiewicz, A. K., Le, K., Amaravadi, R. K., Karakousis, G. C., Xu, X., Xu, W., Schuchter, L. M., Lee, J. B., Ertel, A., Fortina, P., and Aplin, A. E. (2013) Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulationof ERBB3. J. Clin. Invest. 123, 2155-2168
11. Girotti, M. R., Pedersen, M., Sanchez-Laorden, B., Viros, A., Turajlic, S., Niculescu-Duvaz, D., Zambon, A., Sinclair, J., Hayes, A., Gore, M., Lorigan, P., Springer, C., Larkin, J., Jorgensen, C., and Marais, R. (2013) Inhibiting EGF receptor or SRC family kinase signaling overcomes BRAF inhibitor resistance in melanoma. Cancer Discov. 3, 158-167
12. Kugel, C. H., 3rd, and Aplin, A. E. (2014) Adaptive resistance to RAF inhibitors in melanoma. Pigment Cell Melanoma Res. 27, 1032-1038
13. Mueller, M. M., and Fusenig, N. E. (2004) Friends or foes: bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 4, 839-849
14. Lee, K. W., Yeo, S. Y., Sung, C. O., and Kim, S. H. (2015) Twist1 is a key regulator of cancer-associated fibroblasts. Cancer Res. 75, 73-85
15. Kugel, C. H., 3rd, Hartsough, E. J., Davies, M. A., Setiady, Y. Y., and Aplin, A. E. (2014) Function-blocking ERBB3 antibody inhibits the adaptive response to RAF inhibitor. Cancer Res. 74, 4122-4132
16. Fedorenko, I. V., Abel, E. V., Koomen, J. M., Fang, B., Wood, E. R., Chen, Y. A., Fisher, K. J., Iyengar, S., Dahlman, K. B., Wargo, J. A., Flaherty, K. T., Sosman, J. A., Sondak, V. K., Messina, J. L., Gibney, G. T., and Smalley, K. S. (2015) Fibronectin induction abrogates the BRAF inhibitor response of BRAF V600E/PTEN-null melanoma cells. Oncogene 10.1038/onc.2015.188
17. Guy, P. M., Platko, J. V., Cantley, L. C., Cerione, R. A., and Carraway, K. L., 3rd (1994) Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc. Natl. Acad. Sci. U. S. A. 91, 8132-8136
18. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137
19. Sun, C., Hobor, S., Bertotti, A., Zecchin, D., Huang, S., Galimi, F., Cottino, F., Prahallad, A., Grernrum, W., Tzani, A., Schlicker, A., Wessels, L. F., Smit, E. F., Thunnissen, E., Halonen, P., Lieftink, C., Beijersbergen, R. L., Di Nicolantonio, F., Bardelli, A., Trusolino, L., and Bernards, R. (2014) Intrinsic resistance to MEK inhibition in KRAS mutant lung and colon cancer through transcriptional induction of ERBB3. Cell Rep. 7, 86-93
20. Montero-Conde, C., Ruiz-Llorente, S., Dominguez, J. M., Knauf, J. A., Viale, A., Sherman, E. J., Ryder, M., Ghossein, R. A., Rosen, N., and Fagin, J. A. (2013) Reliefof feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAF-mutant thyroid carcinomas. Cancer Discov. 3, 520-533
21. Wilson, T. R., Fridlyand, J., Yan, Y., Penuel, E., Burton, L., Chan, E., Peng, J., Lin, E., Wang, Y., Sosman, J., Ribas, A., Li, J., Moffat, J., Sutherlin, D. P., Koeppen, H., Merchant, M., Neve, R., and Settleman, J. (2012) Widespread potential for growth-factor-driven resistance to anticancer kinase inhibitors. Nature 487, 505-509
22. Lin, M. C., Rojas, K. S., Cerione, R. A., and Wilson, K. F. (2014) Identification of mTORC2 as a necessary component of HRG/ErbB2-dependent cellular transformation. Mol. Cancer Res. 12, 940-952
23. Hatzivassiliou, G., Song, K., Yen, I., Brandhuber, B. J., Anderson, D. J., Alvarado, R., Ludlam, M. J., Stokoe, D., Gloor, S. L., Vigers, G., Morales, T., Aliagas, I., Liu, B., Sideris, S., Hoeflich, K. P., Jaiswal, B. S., Seshagiri, S., Koeppen, H., Belvin, M., Friedman, L. S., and Malek, S. (2010) RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 464, 431-435
24. Heidorn, S. J., Milagre, C., Whittaker, S., Nourry, A., Niculescu-Duvas, I., Dhomen, N., Hussain, J., Reis-Filho, J. S., Springer, C. J., Pritchard, C., and Marais, R. (2010) Kinase-dead BRAF and oncogenic RAS cooperate to drive tumor progression through CRAF. Cell 140, 209-221
25. Kaplan, F. M., Shao, Y., Mayberry, M. M., and Aplin, A. E. (2011) Hyperactivation of MEK-ERK1/2 signaling and resistance to apoptosis induced by the oncogenic B-RAF inhibitor, PLX4720, in mutant N-RAS melanoma cells. Oncogene 30, 366-371
26. Halaban, R., Zhang, W., Bacchiocchi, A., Cheng, E., Parisi, F., Ariyan, S., Krauthammer, M., McCusker, J. P., Kluger, Y., and Sznol, M. (2010) PLX4032, a selective BRAF (V600E) kinase inhibitor, activates the ERK pathway and enhances cell migration and proliferation of BRAF melanoma cells. Pigment Cell Melanoma Res. 23, 190-200
27. Le, K., Blomain, E. S., Rodeck, U., and Aplin, A. E. (2013) Selective RAF inhibitor impairs ERK1/2 phosphorylation and growth in mutant NRAS, vemurafenib-resistant melanoma cells. Pigment Cell Melanoma Res. 26, 509-517
28. Rettig, W. J., Garin-Chesa, P., Healey, J. H., Su, S. L., Ozer, H. L., Schwab, M., Albino, A. P., and Old, L. J. (1993) Regulation and heteromeric structure of the fibroblast activation protein in normal and transformed cells of mesenchymal and neuroectodermal origin. Cancer Res. 53, 3327-3335
29. Cirri, P., and Chiarugi, P. (2011) Cancer associated fibroblasts: the dark side of the coin. Am. J. Cancer Res. 1, 482-497
30. Mei, L., and Xiong, W. C. (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9, 437-452
31. Sheng, Q., Liu, X., Fleming, E., Yuan, K., Piao, H., Chen, J., Moustafa, Z., Thomas, R. K., Greulich, H., Schinzel, A., Zaghlul, S., Batt, D., Ettenberg, S., Meyerson, M., Schoeberl, B., Kung, A. L., Hahn, W. C., Drapkin, R., Livingston, D. M., and Liu, J. F. (2010) An activated ErbB3/NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 17, 298-310
32. Baselga, J., and Swain, S. M. (2009) Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat. Rev. Cancer 9, 463-475
33. Buac, K., Xu, M., Cronin, J., Weeraratna, A. T., Hewitt, S. M., and Pavan, W. J. (2009) NRG1/ERBB3 signaling in melanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res. 22, 773-784
34. Choi, W., Wolber, R., Gerwat, W., Mann, T., Batzer, J., Smuda, C., Liu, H., Kolbe, L., and Hearing, V. J. (2010) The fibroblast-derived paracrine factor neuregulin-1 has a novel role in regulating the constitutive color and melanocyte function in human skin. J. CellSci. 123, 3102-3111
35. Liles, J. S., Arnoletti, J. P., Kossenkov, A. V., Mikhaylina, A., Frost, A. R., Kulesza, P., Heslin, M. J., and Frolov, A. (2011) Targeting ErbB3-mediated stromal-epithelial interactions in pancreatic ductal adenocarcinoma. Br. J. Cancer 105, 523-533
36. Zhang, K., Wong, P., Zhang, L., Jacobs, B., Borden, E. C., Aster, J. C., and Bedogni, B. (2012) A Notch1-neuregulin1 autocrine signaling loop contributes to melanoma growth. Oncogene 31, 4609-4618
37. Zhang, K., Wong, P., Duan, J., Jacobs, B., Borden, E. C., and Bedogni, B. (2013) An ERBB3/ERBB2 oncogenic unit plays a key role in NRG1 signaling and melanoma cell growth and survival. Pigment Cell Melanoma Res. 26, 408-414
38. Capparelli, C., Rosenbaum, S., Berman-Booty, L. D., Salhi, A., Gaborit, N., Zhan, T., Chervoneva, I., Roszik, J., Woodman, S. E., Davies, M. A., Setiady, Y. Y., Osman, I., Yarden, Y., and Aplin, A. E. (2015) ErbB3/ErbB2 complexes as a therapeutic target in a subset of wild-type BRAF/NRAS cutaneous melanomas. Cancer Res. 10.1158/0008-5472
39. Lito, P., Pratilas, C. A., Joseph, E. W., Tadi, M., Halilovic, E., Zubrowski, M., Huang, A., Wong, W. L., Callahan, M. K., Merghoub, T., Wolchok, J. D., de Stanchina, E., Chandarlapaty, S., Poulikakos, P. I., Fagin, J. A., and Rosen, N. (2012) Relief of profound feedback inhibition of mitogenic signaling by RAF inhibitors attenuates their activity in BRAFV600E melanomas. Cancer Cell 22, 668-682
40. Wang, T., Xiao, M., Ge, Y., Krepler, C., Belser, E., Lopez-Coral, A., Xu, X., Zhang, G., Azuma, R., Liu, Q., Liu, R., Li, L., Amaravadi, R. K., Xu, W., Karakousis, G., Gangadhar, T. C., Schuchter, L. M., Lieu, M., Khare, S., Halloran, M. B., Herlyn, M., and Kaufman, R. E. (2015) BRAF inhibition stimulates melanoma-associated macrophages to drive tumor growth. Clin. Cancer Res. 21, 1652-1664
41. Basile, K. J., Le, K., Hartsough, E. J., and Aplin, A. E. (2014) Inhibition of mutant BRAF splice variant signaling by next-generation, selective RAF inhibitors. Pigment Cell Melanoma Res. 27, 479-484
42. Straussman, R., Morikawa, T., Shee, K., Barzily-Rokni, M., Qian, Z. R., Du, J., Davis, A., Mongare, M. M., Gould, J., Frederick, D. T., Cooper, Z. A., Chapman, P. B., Solit, D. B., Ribas, A., Lo, R. S., Flaherty, K. T., Ogino, S., Wargo, J. A., and Golub, T. R. (2012) Tumour micro-environment elicits innate resistance to RAF inhibitors through HGF secretion. Nature 487, 500-504
43. Liu, F., Cao, J., Wu, J., Sullivan, K., Shen, J., Ryu, B., Xu, Z., Wei, W., and Cui, R. (2013) Stat3-targeted therapies overcome the acquired resistance to vemurafenib in melanomas. J. Invest. Dermatol. 133, 2041-2049
44. Baselga, J., Cortés, J., Kim, S. B., Im, S. A., Hegg, R., Im, Y. H., Roman, L., Pedrini, J. L., Pienkowski, T., Knott, A., Clark, E., Benyunes, M. C., Ross, G., Swain, S. M., and CLEOPATRA Study Group (2012) Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N. Engl. J. Med. 366, 109-119
45. Lindzen, M., Carvalho, S., Starr, A., Ben-Chetrit, N., Pradeep, C. R., Köstler, W. J., Rabinkov, A., Lavi, S., Bacus, S. S., and Yarden, Y. (2012) A recombinant decoy comprising EGFR and ErbB-4 inhibits tumor growth and metastasis. Oncogene 31, 3505-3515
46. Togo, S., Polanska, U. M., Horimoto, Y., and Orimo, A. (2013) Carcinomaassociated fibroblasts are a promising therapeutic target. Cancers 5, 149-169
47. Garner, A. P., Bialucha, C. U., Sprague, E. R., Garrett, J. T., Sheng, Q., Li, S., Sineshchekova, O., Saxena, P., Sutton, C. R., Chen, D., Chen, Y., Wang, H., Liang, J., Das, R., Mosher, R., Gu, J., Huang, A., Haubst, N., Zehetmeier, C., Haberl, M., Elis, W., Kunz, C., Heidt, A. B., Herlihy, K., Murtie, J., Schuller, A., Arteaga, C. L., Sellers, W. R., and Ettenberg, S. A. (2013) An antibody that locks HER3 in the inactive conformation inhibits tumor growth driven by HER2 or neuregulin. Cancer Res. 73, 6024-6035
48. Garrett, J. T., Sutton, C. R., Kurupi, R., Bialucha, C. U., Ettenberg, S. A., Collins, S. D., Sheng, Q., Wallweber, J., Defazio-Eli, L., and Arteaga, C L. (2013) Combination of antibody that inhibits ligand-independent HER3 dimerization and a p110α inhibitor potently blocks PI3K signaling and growth of HER2+ breast cancers. Cancer Res. 73, 6013-6023
49. Reschke, M., Mihic-Probst, D., van der Horst, E. H., Knyazev, P., Wild, P. J., Hutterer, M., Meyer, S., Dummer, R., Moch, H., and Ullrich, A. (2008) HER3 is a determinant for poor prognosis in melanoma. Clin. Cancer Res. 14, 5188-5197