Anti-androgen enzalutamide enhances prostate cancer neuroendocrine (NE) differentiation via altering the infiltrated mast cells → androgen receptor (AR) → miRNA32 signals

Molecular Oncology

Volumn 9, Issue 7, 2015, Pages 1241-1251

  Dang, Qiang ^a,b   Li, Lei ^a,b   Xie, Hongjun ^a,b   He, Dalin ^a   Chen, Jiaqi ^a   Song, Wenbing ^a,b   Chang, Luke S ^a   Chang, Hong Chiang ^b   Yeh, Shuyuan ^b   Chang, Chawnshang ^b,c  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

IL8; Mast cells; MiRNA32; NE differentiation; Prostate cancer

Indexed keywords

ANDROGEN RECEPTOR; BICALUTAMIDE; ENZALUTAMIDE; INTERLEUKIN 8; MICRORNA; MICRORNA 32; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ANTIANDROGEN; MIRN32 MICRORNA, HUMAN; PHENYLTHIOHYDANTOIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; DRUG MECHANISM; EPITHELIUM CELL; HUMAN; HUMAN CELL; MALE; MAST CELL; NEUROENDOCRINE DIFFERENTIATION; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER CELL LINE; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; METABOLISM; MOUSE; NEUROSECRETORY CELL; NUDE MOUSE; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ANDROGEN ANTAGONISTS; ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; HUMANS; MALE; MAST CELLS; MICE; MICE, NUDE; MICRORNAS; NEUROENDOCRINE CELLS; PHENYLTHIOHYDANTOIN; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; SIGNAL TRANSDUCTION;

EID: 84938210508     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2015.02.010     Document Type: Article

References (44)

1. Abrahamsson P.A. Neuroendocrine differentiation in prostatic carcinoma. The Prostate 1999, 39:135-148.
2. Alonzeau J., Alexandre D., Jeandel L., Courel M., Hautot C., Yamani F.-Z.E., Gobet F., Leprince J., Magoul R., Amarti A. The neuropeptide 26RFa is expressed in human prostate cancer and stimulates the neuroendocrine differentiation and the migration of androgeno-independent prostate cancer cells. Eur. J. Cancer 2013 Jan, 49(2):511-519.
3. Araki S., Omori Y., Lyn D., Singh R.K., Meinbach D.M., Sandman Y., Lokeshwar V.B., Lokeshwar B.L. Interleukin-8 is a molecular determinant of androgen independence and progression in prostate cancer. Cancer Res. 2007, 67:6854-6862.
4. Chang C., Kokontis J., Liao S. Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7211-7215.
5. Chang C., Lee S.O., Yeh S., Chang T.M. Androgen receptor (AR) differential roles in hormone-related tumors including prostate, bladder, kidney, lung, breast and liver. Oncogene 2014 Jun 19, 33(25):3225-3234.
6. Chang C.S., Kokontis J., Liao S.T. Molecular cloning of human and rat complementary DNA encoding androgen receptors. Science 1988, 240:324-326.
7. Cortés M.A., Cariaga-Martinez A.E., Lobo M.V., Orozco R.M.M., Motiño O., Rodríguez-Ubreva F.J., Angulo J., López-Ruiz P., Colás B. EGF promotes neuroendocrine-like differentiation of prostate cancer cells in the presence of LY294002 through increased ErbB2 expression independent of the phosphatidylinositol 3-kinase-AKT pathway. Carcinogenesis 2012, 33:1169-1177.
8. DaSilva J.O., Amorino G.P., Casarez E.V., Pemberton B., Parsons S.J. Neuroendocrine-derived peptides promote prostate cancer cell survival through activation of IGF-1R signaling. Prostate 2013 Jun, 73(8):801-812.
9. Deeble P.D., Cox M.E., Frierson H.F., Sikes R.A., Palmer J.B., Davidson R.J., Casarez E.V., Amorino G.P., Parsons S.J. Androgen-independent growth and tumorigenesis of prostate cancer cells are enhanced by the presence of PKA-differentiated neuroendocrine cells. Cancer Res. 2007, 67:3663-3672.
10. Feuser K., Thon K.P., Bischoff S.C., Lorentz A. Human intestinal mast cells are a potent source of multiple chemokines. Cytokine 2012, 58:178-185.
11. Fleischmann A., Schlomm T., Kollermann J., Sekulic N., Huland H., Mirlacher M., Sauter G., Simon R., Erbersdobler A. Immunological microenvironment in prostate cancer: high mast cell densities are associated with favorable tumor characteristics and good prognosis. Prostate 2009, 69:976-981.
12. Franck-Lissbrant I., Haggstrom S., Damber J.E., Bergh A. Testosterone stimulates angiogenesis and vascular regrowth in the ventral prostate in castrated adult rats. Endocrinology 1998, 139:451-456.
13. Gounaris E., Erdman S.E., Restaino C., Gurish M.F., Friend D.S., Gounari F., Lee D.M., Zhang G., Glickman J.N., Shin K., Rao V.P., Poutahidis T., Weissleder R., McNagny K.M., Khazaie K. Mast cells are an essential hematopoietic component for polyp development. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19977-19982.
14. Halova I., Draberova L., Draber P. Mast cell chemotaxis - chemoattractants and signaling pathways. Front. Immunol. 2012, 3:119.
15. Heinlein C.A., Chang C. Androgen receptor (AR) coregulators: an overview. Endocr. Rev. 2002, 23:175-200.
16. Heinlein C.A., Chang C. Androgen receptor in prostate cancer. Endocr. Rev. 2004, 25:276-308.
17. Inamura H., Kurosawa M., Okano A., Kayaba H., Majima M. Expression of the interleukin-8 receptors CXCR1 and CXCR2 on cord-blood-derived cultured human mast cells. Int. Arch. Allergy Immunol. 2002, 128:142-150.
18. Jiao L., Deng Z., Xu C., Yu Y., Li Y., Yang C., Chen J., Liu Z., Huang G., Li L.C. MicroRNA-663 induces castration-resistant prostate cancer transformation and predicts clinical recurrence. J. Cell Physiol. 2014 Jul, 229(7):834-844.
19. Johansson A., Rudolfsson S., Hammarsten P., Halin S., Pietras K., Jones J., Stattin P., Egevad L., Granfors T., Wikstrom P., Bergh A. Mast cells are novel independent prognostic markers in prostate cancer and represent a target for therapy. Am. J. Pathol. 2010, 177:1031-1041.
20. Lee H.W., Lee E.H., Ha S.Y., Lee C.H., Chang H.K., Chang S., Kwon K.Y., Hwang I.S., Roh M.S., Seo J.W. Altered expression of microRNA miR-21, miR-155, and let-7a and their roles in pulmonary neuroendocrine tumors. Pathol. Int. 2012, 62:583-591.
21. Li Z., Chen C.J., Wang J.K., Hsia E., Li W., Squires J., Sun Y., Huang J. Neuroendocrine differentiation of prostate cancer. Asian J. Androl. 2013 May, 15(3):328-332.
22. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
23. Lin T., Izumi K., Lee S., Lin W., Yeh S., Chang C. Anti-androgen receptor ASC-J9 versus anti-androgens MDV3100 (enzalutamide) or casodex (bicalutamide) leads to opposite effects on prostate cancer metastasis via differential modulation of macrophage infiltration and STAT3-CCL2 signaling. Cell Death Dis. 2013, 4:e764.
24. Lin T.H., Lee S.O., Niu Y., Xu D., Liang L., Li L., Yeh S.D., Fujimoto N., Yeh S., Chang C. Differential androgen deprivation therapies with anti-androgens casodex/bicalutamide or MDV3100/Enzalutamide versus anti-androgen receptor ASC-J9(R) Lead to promotion versus suppression of prostate cancer metastasis. J. Biol. Chem. 2013, 288:19359-19369.
25. Liu Q., Russell M.R., Shahriari K., Jernigan D.L., Lioni M.I., Garcia F.U., Fatatis A. Interleukin-1β promotes skeletal colonization and progression of metastatic prostate cancer cells with neuroendocrine features. Cancer Res. 2013, 73:3297-3305.
26. Luo X., Zhang J., Wang H., Du Y., Yang L., Zheng F., Ma D. PolyA RT-PCR-based quantification of microRNA by using universal TaqMan probe. Biotechnol. Lett. 2012, 34:627-633.
27. Nilsson G., Mikovits J.A., Metcalfe D.D., Taub D.D. Mast cell migratory response to interleukin-8 is mediated through interaction with chemokine receptor CXCR2/Interleukin-8RB. Blood 1999, 93:2791-2797.
28. Niu Y., Altuwaijri S., Yeh S., Lai K.P., Yu S., Chuang K.H., Huang S.P., Lardy H., Chang C. Targeting the stromal androgen receptor in primary prostate tumors at earlier stages. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12188-12193.
29. Niu Y., Chang T.M., Yeh S., Ma W.L., Wang Y.Z., Chang C. Differential androgen receptor signals in different cells explain why androgen-deprivation therapy of prostate cancer fails. Oncogene 2010, 29:3593-3604.
30. Park M., Lee H., Lee C., You S., Kim D., Park B., Kang M., Heo W., Shin E., Schwartz M. p21-Activated kinase 4 promotes prostate cancer progression through CREB. Oncogene 2012, 32:2475-2482.
31. Prussin C., Metcalfe D.D. 4. IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 2003, 111:S486-S494.
32. Qiu Y., Robinson D., Pretlow T.G., Kung H.-J. Etk/Bmx, a tyrosine kinase with a pleckstrin-homology domain, is an effector of phosphatidylinositol 3'-kinase and is involved in interleukin 6-induced neuroendocrine differentiation of prostate cancer cells. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:3644-3649.
33. Seaton A., Scullin P., Maxwell P.J., Wilson C., Pettigrew J., Gallagher R., O'Sullivan J.M., Johnston P.G., Waugh D.J. Interleukin-8 signaling promotes androgen-independent proliferation of prostate cancer cells via induction of androgen receptor expression and activation. Carcinogenesis 2008, 29:1148-1156.
34. Shen R., Dorai T., Szaboles M., Katz A.E., Olsson C.A., Buttyan R. Transdifferentiation of Cultured Human Prostate cancer Cells to a Neuroendocrine Cell Phenotype in a Hormone-depleted Medium, Urologic Oncology: Seminars and Original Investigations 1997, 67-75. Elsevier.
35. Siegel R., Naishadham D., Jemal A. Cancer statistics, 2013. CA Cancer J. Clin 2013, 63:11-30.
36. Soucek L., Lawlor E.R., Soto D., Shchors K., Swigart L.B., Evan G.I. Mast cells are required for angiogenesis and macroscopic expansion of Myc-induced pancreatic islet tumors. Nat. Med. 2007, 13:1211-1218.
37. Taverna G., Giusti G., Seveso M., Hurle R., Colombo P., Stifter S., Grizzi F. Mast cells as a potential prognostic marker in prostate cancer. Dis. Markers 2013, 35:711-720.
38. Tawadros T., Alonso F., Jichlinski P., Clarke N., Calandra T., Haefliger J.-A., Roger T. Release of macrophage migration inhibitory factor by neuroendocrine-differentiated LNCaP cells sustains the proliferation and survival of prostate cancer cells. Endocrine-Related Cancer 2013, 20:137-149.
39. Uchida K., Masumori N., Takahashi A., Itoh N., Kato K., Matusik R.J., Tsukamoto T. Murine androgen-independent neuroendocrine carcinoma promotes metastasis of human prostate cancer cell line LNCaP. The Prostate 2006, 66:536-545.
40. Waugh D.J., Wilson C. The interleukin-8 pathway in cancer. Clin. Cancer Res. 2008, 14:6735-6741.
41. Wright M.E., Tsai M.J., Aebersold R. Androgen receptor represses the neuroendocrine transdifferentiation process in prostate cancer cells. Mol. Endocrinol. 2003, 17:1726-1737.
42. Yuan T.C., Veeramani S., Lin M.F. Neuroendocrine-like prostate cancer cells: neuroendocrine transdifferentiation of prostate adenocarcinoma cells. Endocr. Relat. Cancer 2007, 14:531-547.
43. Zheng C., Yinghao S., Li J. MiR-221 expression affects invasion potential of human prostate carcinoma cell lines by targeting DVL2. Med. Oncol. 2012, 29:815-822.
44. Zudaire E., Martinez A., Garayoa M., Pio R., Kaur G., Woolhiser M.R., Metcalfe D.D., Hook W.A., Siraganian R.P., Guise T.A., Chirgwin J.M., Cuttitta F. Adrenomedullin is a cross-talk molecule that regulates tumor and mast cell function during human carcinogenesis. Am. J. Pathol. 2006, 168:280-291.