Release of macrophage migration inhibitory factor by neuroendocrinedifferentiated LNCaP cells sustains the proliferation and survival of prostate cancer cells

Endocrine-Related Cancer

Volumn 20, Issue 1, 2013, Pages 137-149

  Tawadros, Thomas ^a   Alonso, Florian ^a   Jichlinski, Patrice ^a   Clarke, Noel ^b   Calandra, Thierry ^a   Haefliger, Jacques Antoine ^a   Roger, Thierry ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Apoptosis; Macrophage migration inhibitory factor; Neuroendocrine differentiation; Proliferation; Prostate cancer

Indexed keywords

CYCLIC AMP; MACROPHAGE MIGRATION INHIBITION FACTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PACLITAXEL; PROTEIN KINASE B;

ANDROGEN DEPRIVATION THERAPY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CANCER RECURRENCE; CELL PROLIFERATION; CELL STRAIN LNCAP; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; NEUROSECRETORY CELL; PROMOTER REGION; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; INTRAMOLECULAR OXIDOREDUCTASES; MACROPHAGE MIGRATION-INHIBITORY FACTORS; MALE; NEUROENDOCRINE CELLS; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 84874028672     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0286     Document Type: Article

References (61)

1. Abrahamsson PA, Wadstrom LB, Alumets J, Falkmer S & Grimelius L 1987 Peptide-hormone- and serotonin-immunoreactive tumour cells in carcinoma of the prostate. Pathology, Research and Practice 182 298-307. (doi:10.1016/S0344- 0338(87)80065-1)
2. Ayala G, Thompson T, Yang G, Frolov A, Li R, Scardino P, Ohori M, Wheeler T & Harper W 2004 High levels of phosphorylated form of Akt-1 in prostate cancer and non-neoplastic prostate tissues are strong predictors of biochemical recurrence. Clinical Cancer Research 10 6572-6578. (doi:10.1158/1078-0432.CCR- 04-0477)
3. Berthold DR, Pond GR, Soban F, deWit R, Eisenberger M & Tannock IF 2008 Docetaxel plus prednisone ormitoxantrone plus prednisone for advanced prostate cancer: updated survival in the TAX 327 study. Journal of Clinical Oncology 26 242-245. (doi:10.1200/JCO.2007.12.4008)
4. Bucala R & Donnelly SC 2007 Macrophage migration inhibitory factor: a probable link between inflammation and cancer. Immunity 26 281-285. (doi:10.1016/j.immuni.2007.03.005)
5. Burchardt T, Burchardt M, Chen MW, Cao Y, de la Taille A, Shabsigh A, Hayek O, Dorai T & Buttyan R 1999 Transdifferentiation of prostate cancer cells to a neuroendocrine cell phenotype in vitro and in vivo. Journal of Urology 162 1800-1805. (doi:10.1016/S0022-5347(05)68241-9)
6. Calandra T & Roger T 2003 Macrophage migration inhibitory factor: a regulator of innate immunity. Nature Reviews. Immunology 3 791-800. (doi:10.1038/nri1200)
7. Calandra T, Froidevaux C, Martin C & Roger T 2003 Macrophage migration inhibitory factor and host innate immune defenses against bacterial sepsis. Journal of Infectious Diseases 187 (Suppl 2) S385-S390. (doi:10.1086/374752)
8. Chen Y, Sawyers CL & Scher HI 2008 Targeting the androgen receptor pathway in prostate cancer. Current Opinion in Pharmacology 8 440-448. (doi:10.1016/j.coph.2008.07.005)
9. Chen YC, Zhang XW, Niu XH, Xin DQ, Zhao WP, Na YQ & Mao ZB 2010 Macrophage migration inhibitory factor is a direct target of HBP1- mediated transcriptional repression that is overexpressed in prostate cancer. Oncogene 29 3067-3078. (doi:10.1038/onc.2010.97)
10. Chesney J,MetzC, BacherM, Peng T,Meinhardt A&Bucala R 1999 An essential role for macrophage migration inhibitory factor (MIF) in angiogenesis and the growth of a murine lymphoma. Molecular Medicine 5 181-191.
11. Cheville JC, Tindall D, Boelter C, Jenkins R, Lohse CM, Pankratz VS, Sebo TJ, Davis B&Blute ML 2002 Metastatic prostate carcinoma to bone: clinical and pathologic features associated with cancer-specific survival. Cancer 95 1028-1036. (doi:10.1002/cncr.10788)
12. Cox ME, Deeble PD, Lakhani S & Parsons SJ 1999 Acquisition of neuroendocrine characteristics by prostate tumor cells is reversible: implications for prostate cancer progression. Cancer Research 59 3821-3830.
13. Delaloye J, De Bruin IJ, Darling KE, Reymond MK, Sweep FC, Roger T, Calandra T & Cavassini M 2012 Increased macrophage migration inhibitory factor (MIF) plasma levels in acute HIV-1 infection. Cytokine 60 338-340. (doi:10.1016/j.cyto.2012.07.027)
14. Dessein AF, Stechly L, Jonckheere N, Dumont P, Monte D, Leteurtre E, Truant S, Pruvot FR, FigeacM, HebbarMet al. 2010 Autocrine induction of invasive and metastatic phenotypes by the MIF-CXCR4 axis in drug-resistant human colon cancer cells. Cancer Research 70 4644-4654. (doi:10.1158/0008-5472.CAN-09-3828)
15. Domanska UM, Timmer-Bosscha H, Nagengast WB, Oude Munnink TH, Kruizinga RC, Ananias HJ, Kliphuis NM, Huls G, De Vries EG, de Jong IJ et al. 2012 CXCR4 inhibition with AMD3100 sensitizes prostate cancer to docetaxel chemotherapy. Neoplasia 14 709-718.
16. Ferrer FA, Miller LJ, Lindquist R, Kowalczyk P, Laudone VP, Albertsen PC & Kreutzer DL 1999 Expression of vascular endothelial growth factor receptors in human prostate cancer. Urology 54 567-572. (doi:10.1016/ S0090-4295(99)00156-9)
17. Fingerle-Rowson G, PetrenkoO,Metz CN, Forsthuber TG, Mitchell R, Huss R, Moll U, MullerW& Bucala R 2003 The p53-dependent effects of macrophagemigration inhibitory factor revealed by gene targeting. PNAS 100 9354-9359. (doi:10.1073/pnas.1533295100)
18. Flieger O, Engling A, Bucala R, Lue H, Nickel W & Bernhagen J 2003 Regulated secretion of macrophage migration inhibitory factor is mediated by a non-classical pathway involving an ABC transporter. FEBS Letters 551 78-86. (doi:10.1016/S0014-5793(03)00900-1)
19. Fromont G, Godet J, Pires C, Yacoub M, Dore B & Irani J 2012 Biological significance of perineural invasion (PNI) in prostate cancer. Prostate 72 542-548. (doi:10.1002/pros.21456)
20. Gao H, Ouyang X, Banach-Petrosky WA, Gerald WL, Shen MM & Abate- Shen C 2006 Combinatorial activities of Akt and B-Raf/Erk signaling in a mouse model of androgen-independent prostate cancer. PNAS 103 14477-14482. (doi:10.1073/pnas.0606836103)
21. Gioeli D 2005 Signal transduction in prostate cancer progression. Clinical Science 108 293-308. (doi:10.1042/CS20040329)
22. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ & Beach DH 1999 A proinflammatory cytokine inhibits p53 tumor suppressor activity. Journal of Experimental Medicine 190 1375-1382. (doi:10.1084/ jem.190.10.1375)
23. Jemal A, Siegel R, Xu J & Ward E 2010 Cancer statistics, 2010. CA: A Cancer Journal for Clinicians 60 277-300. (doi:10.3322/caac.20073)
24. Jin RJ,Wang Y,Masumori N, Ishii K, Tsukamoto T, Shappell SB, Hayward SW, Kasper S & Matusik RJ 2004 NE-10 neuroendocrine cancer promotes the LNCaP xenograft growth in castrated mice. Cancer Research 64 5489-5495. (doi:10.1158/0008-5472.CAN-03-3117)
25. Keller M, Ruegg A,Werner S & Beer HD 2008 Active caspase-1 is a regulator of unconventional protein secretion. Cell 132 818-831. (doi:10.1016/ j.cell.2007.12.040)
26. Kreisberg JI, Malik SN, Prihoda TJ, Bedolla RG, Troyer DA, Kreisberg S & Ghosh PM 2004 Phosphorylation of Akt (Ser473) is an excellent predictor of poor clinical outcome in prostate cancer. Cancer Research 64 5232-5236. (doi:10.1158/0008-5472.CAN-04-0272)
27. Liao H, Bucala R & Mitchell RA 2003 Adhesion-dependent signaling by macrophage migration inhibitory factor (MIF). Journal of Biological Chemistry 278 76-81. (doi:10.1074/jbc.M208820200)
28. Lue H, Thiele M, Franz J, Dahl E, Speckgens S, Leng L, Fingerle-Rowson G, Bucala R, Luscher B & Bernhagen J 2007 Macrophage migration inhibitory factor (MIF) promotes cell survival by activation of the Akt pathway and role for CSN5/JAB1 in the control of autocrine MIF activity. Oncogene 26 5046-5059. (doi:10.1038/sj.onc.1210318)
29. Lugrin J, Ding XC, Le Roy D, Chanson AL, Sweep FC, Calandra T & Roger T 2009 Histone deacetylase inhibitors repress macrophage migration inhibitory factor (MIF) expression by targeting MIF gene transcription through a local chromatin deacetylation. Biochimica et Biophysica Acta 1793 1749-1758. (doi:10.1016/j.bbamcr.2009.09.007)
30. Merk M, Baugh J, Zierow S, Leng L, Pal U, Lee SJ, Ebert AD,Mizue Y, Trent JO, Mitchell R et al. 2009 The Golgi-associated protein p115 mediates the secretion of macrophage migration inhibitory factor. Journal of Immunology 182 6896-6906. (doi:10.4049/jimmunol.0803710)
31. Meyer-Siegler KL, Leifheit EC & Vera PL 2004 Inhibition of macrophage migration inhibitory factor decreases proliferation and cytokine expression in bladder cancer cells. BMC Cancer 4 34. (doi:10.1186/1471-2407-4-34)
32. Meyer-Siegler KL, Iczkowski KA & Vera PL 2005 Further evidence for increased macrophage migration inhibitory factor expression in prostate cancer. BMC Cancer 5 73. (doi:10.1186/1471-2407-5-73)
33. Meyer-Siegler KL, Vera PL, Iczkowski KA, Bifulco C, Lee A, Gregersen PK, Leng L & Bucala R 2007 Macrophage migration inhibitory factor (MIF) gene polymorphisms are associated with increased prostate cancer incidence. Genes and Immunity 8 646-652. (doi:10.1038/sj.gene.6364427)
34. Mitchell RA 2004 Mechanisms and effectors of MIF-dependent promotion of tumorigenesis. Cellular Signalling 16 13-19. (doi:10.1016/j.cellsig. 2003.07.002)
35. Mitchell RA, Metz CN, Peng T & Bucala R 1999 Sustained mitogenactivated protein kinase (MAPK) and cytoplasmic phospholipase A2 activation by macrophage migration inhibitory factor (MIF). Regulatory role in cell proliferation and glucocorticoid action. Journal of Biological Chemistry 274 18100-18106. (doi:10.1074/jbc.274.25.18100)
36. Munaut C, Boniver J, Foidart JM & Deprez M 2002 Macrophage migration inhibitory factor (MIF) expression in human glioblastomas correlates with vascular endothelial growth factor (VEGF) expression. Neuropathology and Applied Neurobiology 28 452-460. (doi:10.1046/j.1365-2990.2002.00416.x)
37. Muramaki M, Miyake H, Yamada Y & Hara I 2006 Clinical utility of serum macrophage migration inhibitory factor in men with prostate cancer as a novel biomarker of detection and disease progression. Oncology Reports 15 253-257.
38. Ouyang X, Jessen WJ, Al-Ahmadie H, Serio AM, Lin Y, Shih WJ, Reuter VE, Scardino PT, Shen MM, Aronow BJ et al. 2008 Activator protein-1 transcription factors are associated with progression and recurrence of prostate cancer. Cancer Research 68 2132-2144. (doi:10.1158/ 0008-5472.CAN-07-6055)
39. Petrenko O, Fingerle-Rowson G, Peng T, Mitchell RA & Metz CN 2003 Macrophage migration inhibitory factor deficiency is associated with altered cell growth and reduced susceptibility to Ras-mediated transformation. Journal of Biological Chemistry 278 11078-11085. (doi:10.1074/jbc.M211985200)
40. Quinn DI, Henshall SM & Sutherland RL 2005 Molecular markers of prostate cancer outcome. European Journal of Cancer 41 858-887. (doi:10.1016/j.ejca.2004.12.035)
41. Ren Y, Chan HM, Li Z, Lin C, Nicholls J, Chen CF, Lee PY, Lui V, BacherM& Tam PK 2004 Upregulation ofmacrophage migration inhibitory factor contributes to induced N-Myc expression by the activation of ERK signaling pathway and increased expression of interleukin-8 and VEGF in neuroblastoma. Oncogene 23 4146-4154. (doi:10.1038/sj.onc.1207490)
42. Rendon BE, Roger T, Teneng I, Zhao M, Al-Abed Y, Calandra T & Mitchell RA 2007 Regulation of human lung adenocarcinoma cell migration and invasion by macrophage migration inhibitory factor. Journal of Biological Chemistry 282 29910-29918. (doi:10.1074/jbc. M704898200)
43. Rendon BE, Willer SS, Zundel W & Mitchell RA 2009 Mechanisms of macrophage migration inhibitory factor (MIF)-dependent tumor microenvironmental adaptation. Experimental and Molecular Pathology 86 180-185. (doi:10.1016/j.yexmp.2009.01.001)
44. Renner P, Roger T, Bochud PY, Sprong T, Sweep FC, Bochud M, Faust SN, Haralambous E, Betts H, Chanson AL et al. 2012 A functional microsatellite of the macrophage migration inhibitory factor gene associated with meningococcal disease. FASEB Journal 26 907-916. (doi:10.1096/fj.11-195065)
45. Roger T, Out T, Mukaida N, Matsushima K, Jansen H & Lutter R 1998a Enhanced AP-1 and NF-kB activities and stability of interleukin 8 (IL-8) transcripts are implicated in IL-8 mRNA superinduction in lung epithelial H292 cells. Biochemical Journal 330 429-435.
46. Roger T, Out TA, Jansen HM & Lutter R 1998b Superinduction of interleukin-6 mRNA in lung epithelial H292 cells depends on transiently increased C/EBP activity and durable increased mRNA stability. Biochimica et Biophysica Acta 1398 275-284. (doi:10.1016/ S0167-4781(98)00075-X)
47. Roger T, Froidevaux C, Martin C & Calandra T 2003 Macrophage migration inhibitory factor (MIF) regulates host responses to endotoxin through modulation of toll-like receptor 4 (TLR4). Journal of Endotoxin Research 9 119-123.
48. Roger T, Ding X, Chanson AL, Renner P & Calandra T 2007 Regulation of constitutive and microbial pathogen-induced human macrophage migration inhibitory factor (MIF) gene expression. European Journal of Immunology 37 3509-3521. (doi:10.1002/eji.200737357)
49. Roger T, Lugrin J, Le Roy D, Goy G, Mombelli M, Koessler T, Ding XC, Chanson AL, Reymond MK, Miconnet I et al. 2011 Histone deacetylase inhibitors impair innate immune responses to toll-like receptor agonists and to infection. Blood 117 1205-1217. (doi:10.1182/blood- 2010-05-284711)
50. Sagnak L, Topaloglu H, Ozok U & Ersoy H 2011 Prognostic significance of neuroendocrine differentiation in prostate adenocarcinoma. Clinical Genitourinary Cancer 9 73-80. (doi:10.1016/j.clgc.2011.07.003)
51. Salido M, Vilches J & Roomans GM 2004 Changes in elemental concentrations in LNCaP cells are associated with a protective effect of neuropeptides on etoposide-induced apoptosis. Cell Biology International 28 397-402. (doi:10.1016/j.cellbi.2004.03.008)
52. Schwartz V, Lue H, Kraemer S, Korbiel J, Krohn R, Ohl K, Bucala R, Weber C & Bernhagen J 2009 A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Letters 583 2749-2757. (doi:10.1016/j.febslet. 2009.07.058)
53. Segal NH, Cohen RJ, Haffejee Z & Savage N 1994 BCL-2 proto-oncogene expression in prostate cancer and its relationship to the prostatic neuroendocrine cell. Archives of Pathology & Laboratory Medicine 118 616-618. Sun Y, Niu J & Huang J 2009 Neuroendocrine differentiation in prostate cancer. American Journal of Translational Research 1 148-162.
54. Tawadros T, Formenton A, Dudler J, Thompson N, Nicod P, Leisinger HJ, Waeber G & Haefliger JA 2002 The scaffold protein IB1/JIP-1 controls the activation of JNK in rat stressed urothelium. Journal of Cell Science 115 385-393.
55. Tawadros T, Martin D, Abderrahmani A, Leisinger HJ, Waeber G & Haefliger JA 2005 IB1/JIP-1 controls JNK activation and increased during prostatic LNCaP cells neuroendocrine differentiation. Cellular Signalling 17 929-939. (doi:10.1016/j.cellsig.2004.11.013)
56. Uzgare AR & Isaacs JT 2004 Enhanced redundancy in Akt and mitogenactivated protein kinase-induced survival of malignant versus normal prostate epithelial cells. Cancer Research 64 6190-6199. (doi:10.1158/ 0008-5472.CAN-04-0968)
57. Vaday GG, Hua SB, Peehl DM, Pauling MH, Lin YH, Zhu L, Lawrence DM, Foda HD & Zucker S 2004 CXCR4 and CXCL12 (SDF-1) in prostate cancer: inhibitory effects of human single chain Fv antibodies. Clinical Cancer Research 10 5630-5639. (doi:10.1158/1078-0432.CCR-03-0633)
58. Vilches J, SalidoM, Fernandez-Segura E&RoomansGM2004 Neuropeptides, apoptosis and ion changes in prostate cancer. Methods of study and recent developments. Histology and Histopathology 19 951-961.
59. Wang X, Raulji P, Mohapatra SS, Patel R, Hellermann G, Kong X, Vera PL, Meyer-Siegler KL, Coppola D & Mohapatra S 2011 Natriuretic peptide receptor a as a novel target for prostate cancer. Molecular Cancer 10 56. (doi:10.1186/1476-4598-10-56)
60. Wu Z, Cho H, Hampton GM & Theodorescu D 2009 Cdc6 and cyclin E2 are PTEN-regulated genes associated with human prostate cancer metastasis. Neoplasia 11 66-76.
61. Zelefsky MJ, Eastham JA & Sartor AO 2011. Cancer of the prostate. In Cancer: principles and practice of oncology. 9th edn, pp 1220-1271. Eds VT DeVita, S Hellman S & SA Rosenberg. Philadelphia, PA, USA: Lippincott Williams and Wilkins.