CXCR4 pharmacogical inhibition reduces bone and soft tissue metastatic burden by affecting tumor growth and tumorigenic potential in prostate cancer preclinical models

Prostate

Volumn 75, Issue 12, 2015, Pages 1227-1246

  Gravina, Giovanni Luca ^a   Mancini, Andrea ^a   Muzi, Paola ^b   Ventura, Luca ^c   Biordi, Leda ^a   Ricevuto, Enrico ^a   Pompili, Simona ^d   Mattei, Claudia ^a   Di Cesare, Ernesto ^a   Jannini, Emmanuele A ^e   Festuccia, Claudio ^a  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b Prevention and Translational Research Oral Diseases and Systemic Interactions Study Group   (Italy)

^c SAN SALVATORE HOSPITAL   (Italy)

^d Department of Biotechnological and Applied Clinical Sciences Laboratory of Human Anatomy   (Italy)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

bone metastases; CXCR4; Plerixafor; prostate cancer

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR4 ANTAGONIST; COLLAGEN TYPE 1; CTE 9908; GELATINASE A; GELATINASE B; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG; UROKINASE; ANTINEOPLASTIC AGENT; ANTIVIRUS AGENT; CTCE-9908; HETEROCYCLIC COMPOUND; PEPTIDE; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; CANCER GROWTH; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; COCULTURE; CONTROLLED STUDY; DRUG ACTIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; MALE; METASTASIS INHIBITION; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SOFT TISSUE METASTASIS; STROMA CELL; TUMOR MICROENVIRONMENT; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE TUMOR; CELL ADHESION; CELL MOTION; COMPUTER ASSISTED TOMOGRAPHY; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; LYMPH NODE; LYMPH NODE METASTASIS; METABOLISM; NUDE MOUSE; PATHOLOGY; PROSTATE TUMOR; SECONDARY; TUMOR CELL CULTURE; WESTERN BLOTTING; XENOGRAFT;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTIVIRAL AGENTS; BLOTTING, WESTERN; BONE NEOPLASMS; CELL ADHESION; CELL MOVEMENT; CHEMOKINE CXCL12; COCULTURE TECHNIQUES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; HETEROCYCLIC COMPOUNDS; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPH NODES; LYMPHATIC METASTASIS; MALE; MICE; MICE, NUDE; PEPTIDES; PROSTATIC NEOPLASMS; RECEPTORS, CXCR4; TOMOGRAPHY, X-RAY COMPUTED; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84937459791     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.23007     Document Type: Article

References (68)

1. Ferlay J, Parkin DM, Steliarova-Foucher E,. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 2010; 46: 765-781.
2. Ye XC, Choueiri M, Tu SM, Lin SH,. Biology and clinical management of prostate cancer bone metastasis. Front Biosci 2007; 2: 3273-3286.
3. Hadaschik BA, Gleave ME,. Therapeutic options for hormone-refractory prostate cancer in. Urol Oncol 2007; 25: 413-419.
4. Larsson R, Mongan NP, Johansson M, Shcherbina L, Abrahamsson PA, Gudas LJ, Sterner O, Persson. JL,. Clinical trial update and novel therapeutic approaches for metastatic prostate cancer. Curr Med Chem 2011; 18: 4440-4453.
5. Bradbury P, Fabry B, O'Neill GM,. Occupy tissue: The movement in cancer metastasis. Cell Adh Migr 2012; 6: 424-432.
6. Yamaguchi H,. Pathological roles of invadopodia in cancer invasion and metastasis. Eur J Cell Biol 2012; 91: 902-907.
7. Festuccia C, Giunciuglio D, Guerra F, Villanova I, Angelucci A, Manduca P, Teti A, Albini A, Bologna M,. Osteoblasts modulate secretion of urokinase-type plasminogen activator (uPA) and matrix metalloproteinase-9 (MMP-9) in human prostate cancer cells promoting migration and matrigel invasion. Oncol Res 1999; 11: 17-31.
8. Perez M, Migliaccio S, Taranta A, Festuccia C, Orru L, Brama M, Bologna M, Faraggiana T, Baron R, Teti A,. Melanoma cells stimulate osteoclastogenesis, c-Src expression and osteoblast cytokines. Eur J Cancer 2001; 37: 629-640.
9. Festuccia C, Teti A, Bianco P, Guerra F, Vicentini C, Tennina R, Villanova I, Sciortino G, Bologna M,. Human prostatic tumour cells in culture produce growth and differentiation factors active on osteoblasts: A new biological and clinical parameter for prostatic carcinoma. Oncol Res 1997; 9: 419-431.
10. Darash-Yahana M, Pikarsky E, Abramovitch R, Zeira E, Pal B, Karplus R, Beider K, Avniel S, Kasem S, Galun E, Peled A,. Role of high expression levels of CXCR4 in tumour growth, vascularisation, and metastasis. FASEB J 2004; 18: 1240-1242.
11. Smith MC, Luker KE, Garbow JR, Prior JL, Jackson E, Piwnica-Worms D, Luker GD,. CXCR4 regulates growth of both primary and metastatic breast cancer. Cancer Res 2004; 64: 8604-8612.
12. Akashi T, Koizumi K, Tsuneyama K, Saiki I, Takano Y, Fuse H,. Chemokine receptor CXCR4 expression and prognosis in patients with metastatic prostate cancer. Cancer Sci 2008; 99: 539-542.
13. Arya M, Patel HR, McGurk C, Tatoud R, Klocker H, Masters J, Williamson M,. The importance of the CXCL12-CXCR4 chemokine ligand-receptor interaction in prostate cancer metastasis. J Exp Ther Oncol 2004; 4: 291-303.
14. Pan J, Mestas J, Burdick MD, Phillips RJ, Thomas GV, Reckamp K, Belperio JA, Strieter RM,. Stromal derived factor-1 (SDF-1/CXCL12) and CXCR4 in renal cell carcinoma metastasis. Mol Cancer 2006; 5: 56.
15. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, McCauley LK,. Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 2002; 62: 1832-1837.
16. Liekens S, Schols D, Hatse S,. CXCL12-CXCR4 axis in angiogenesis, metastasis and stem cell mobilization. Curr Pharm Des 2010; 16: 3903-3920. Review.
17. Ping YF, Yao XH, Jiang JY, Zhao LT, Yu SC, Jiang T, Lin MC, Chen JH, Wang B, Zhang R, Cui YH, Qian C, Wang Jm, Bian XW,. The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K/AKT signalling. J Pathol 2011; 224: 344-354.
18. Wang Q, Diao X, Sun J, Chen Z,. Regulation of VEGF, MMP-9 and metastasis by CXCR4 in a prostate cancer cell line. Cell Biol Int 2011; 35: 897-904.
19. Li KC, Huang YH, Ho CY, Chu CY, Cha ST, Tsai HH, Ko JY, Chang CC, Tan CT,. The role of IL-8 in the SDF-1α/CXCR4-induced angiogenesis of laryngeal and hypopharyngeal squamous cell carcinoma. Oral Oncol 2012; 48: 507-515.
20. Chinni SR, Sivalogan S, Dong Z, Filho JC, Deng X, Bonfil RD, Cher ML,. CXCL12/CXCR4 signalling activates Akt-1 and MMP-9 expression in prostate cancer cells: The role of bone microenvironment-associated CXCL12. Prostate 2006; 66: 32-48.
21. Engl T, Relja B, Marian D, Blumenberg C, Muller I, Beecken WD, Jones J, Ringel EM, Bereiter-Hahn J, Jonas D, Blaheta RA,. CXCR4 chemokine receptor mediates prostate tumour cell adhesion through alpha5 and beta3 integrins. Neoplasia 2006; 8: 290-301.
22. Sun YX, Fang M, Wang J, Cooper CR, Pienta KJ, Taichman RS,. Expression and activation of alpha v beta 3 integrins by SDF-1/CXC12 increases the aggressiveness of prostate cancer cells. Prostate 2007; 67: 61-73.
23. 2 receptor signalling facilitates tumour colonisation through P-selectin-mediated interaction of tumour cells with platelets and endothelial cells. Cancer Sci 2012; 103: 700-707.
24. Wang L, Huang T, Chen W, Gao X, Zhou T, Wu Z, Sun Y,. Silencing of CXCR4 by RNA interference inhibits cell growth and metastasis in human renal cancer cells. Oncol Rep 2012; 28: 2043-2048.
25. Feng Y, Hu J, Ma J, Feng K, Zhang X, Yang S, Wang W, Zhang J, Zhang Y,. RNAi-mediated silencing of VEGF-C inhibits non-small cell lung cancer progression by simultaneously downregulating the CXCR4, CCR7, VEGFR-2 and VEGFR-3-dependent axes-induced ERK, p38 and AKT signalling pathways. Eur J Cancer 2011; 47: 2353-2363.
26. Nervi B, Ramirez P, Rettig MP, Uy GL, Holt MS, Ritchey JK, Prior JL, Piwnica-Worms D, Bridger G, Ley TJ, DiPersio JF,. Mobilisation and chemosensitisation of AML with the CXCR4 antagonist plerixafor (AMD3100): A phase I/II study of AMD3100 + MEC in patients with relapsed or refractory disease. Blood 2009; 113 (24): 6206-6214.
27. Uy GL, Rettig MP, McFarland K, Hladnik L, Kulkarni S, Abboud CN, Cashen AF, Stockerl- Goldstein K, Vij R, Westervelt P, DiPersio JF,. A phase I/II study of chemosensitisation with the CXCR4 antagonist plerixafor in relapsed or refractory AML. Blood 2012; 119 (17): 3917-3924.
28. Domanska UM, Timmer-Bosscha H, Nagengast WB, Oude Munnink TH, Kruizinga RC, Ananias HJ, Kliphuis NM, Huls G, De Vries EG, de Jong IJ, Walenkamp AM,. CXCR4 inhibition with AMD3100 sensitises prostate cancer to docetaxel chemotherapy. Neoplasia 2012; 14: 709-718.
29. Drenckhan A, Kurschat N, Dohrmann T, Raabe N, Koenig AM, Reichelt U, Kaifi JT, Izbicki JR, Gros SJ,. Effective inhibition of metastases and primary tumour growth with CTCE-9908 in oesophageal cancer. J Surg Res 2013; 182: 250-256.
30. Huang EH, Singh B, Cristofanilli M, Gelovani J, Wei C, Vincent L, Cook KR, Lucci A,. A CXCR4 antagonist CTCE-9908 inhibits primary tumour growth and metastasis of breast cancer. J Surg Res 2009; 155: 231-236.
31. Porvasnik S, Sakamoto N, Kusmartsev S, Eruslanov E, Kim WJ, Cao W, Urbanek C, Wong D, Goodison S, Rosser CJ,. Effects of CXCR4 antagonist CTCE-9908 on prostate tumour growth. Prostate 2009; 69: 1460-1469.
32. Uchida D, Onoue T, Kuribayashi N, Tomizuka Y, Tamatani T, Nagai H, Miyamoto Y,. Blockade of CXCR4 in oral squamous cell carcinoma inhibits lymph node metastases. Eur J Cancer 2011; 47: 452-459.
33. Zhao BC, Wang ZJ, Mao WZ, Ma HC, Han JG, Zhao B, Xu HM,. CXCR4/SDF-1 axis is involved in lymph node metastasis of gastric carcinoma. World J Gastroenterol 2011; 17: 2389-2396.
34. Gros SJ, Kurschat N, Drenckhan A, Dohrmann T, Forberich E, Effenberger K, Reichelt U, Hoffman RM, Pantel K, Kaifi JT, Izbicki JR,. Involvement of CXCR4 chemokine receptor in metastatic HER2-positive oesophageal cancer. PLoS ONE 2012; 7 (10): e47287.
35. Lin G, Yang R, Banie L, Wang G, Ning H, Li LC, Lue TF, Lin CS,. Effects of transplantation of adipose tissue-derived stem cells on prostate tumour. Prostate 2010; 70: 1066-1073.
36. Chinni SR, Yamamoto H, Dong Z, Sabbota A, Bonfil RD, Cher ML,. CXCL12/CXCR4 transactivates HER2 in lipid rafts of prostate cancer cells and promotes growth of metastatic deposits in bone. Mol Cancer Res. 2008; 6: 446-457.
37. Wong D, Kandagatla P, Korz W, Chinni SR,. Targeting CXCR4 with CTCE-9908 inhibits prostate tumor metastasis. BMC Urol 2014; 14: 12.
38. Angelucci A, Gravina GL, Rucci N, Festuccia C, Muzi P, Vicentini C, Teti A, Bologna M,. Evaluation of metastatic potential in prostate carcinoma: An in vivo model. Int J Oncol 2004; 25: 1713-1720.
39. Angelucci A, Gravina GL, Rucci N, Millimaggi D, Festuccia C, Muzi P, Teti A, Vicentini C, Bologna M,. Suppression of EGF-R signaling reduces the incidence of prostate cancer metastasis in nude mice. Endocr Relat Cancer 2006; 13: 197-210.
40. Pettaway CA1, Pathak S, Greene G, Ramirez E, Wilson MR, Killion JJ, Fidler IJ,. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res 1996; 2: 1627-1636.
41. Lin DL, Tarnowski CP, Zhang J, Dai J, Rohn E, Patel AH, Morris MD, Keller ET,. Bone metastatic LNCaP-derivative C4-2B prostate cancer cell line mineralizes in vitro. Prostate 2001; 47: 212-221.
42. Craft N, Shostak Y, Carey M, Sawyers CL,. A mechanism for hormone-independent prostate cancer through modulation of androgen receptor signaling by the HER-2/neu tyrosine kinase. Nat Med 1999; 5: 280-285.
43. Pretlow TG, Wolman SR, Micale MA, Pelley RJ, Kursh ED, Resnick MI, Bodner DR, Jacobberger JW, Delmoro CM, Giaconia JM, Theresa P. Pretlow,. Xenografts of primary human prostatic carcinoma. J Natl Cancer Inst 1993; 85: 394-398.
44. Korenchuk S, Lehr JE, MClean L, Lee YG, Whitney S, Vessella R, Lin DL, Pienta KJ,. VCaP, a cell-based model system of human prostate cancer. In Vivo 2001; 15: 163-168.
45. Gravina GL, Mancini A, Ranieri G, Di Pasquale B, Marampon F, Di Clemente L, Ricevuto E, Festuccia C,. Phenotypic characterization of human prostatic stromal cells in primary cultures derived from human tissue samples. Int J Oncol 2013; 42: 2116-2122.
46. Gravina GL, Tortoreto M, Mancini A, Addis A, Di Cesare E, Lenzi A, Landesman Y, McCauley D, Kauffman M, Shacham S, Zaffaroni N, Festuccia C,. XPO1/CRM1-Selective Inhibitors of Nuclear Export (SINE) reduce tumor spreading and improve overall survival in preclinical models of prostate cancer (PCa). J Hematol Oncol 2014; 7: 46-54.
47. van Bokhoven A, Varella-Garcia M, Korch C, Johannes WU, Smith EE, Miller HL, Nordeen SK, Miller GJ, Lucia MS,. Molecular characterization of human prostate carcinoma cell lines. Prostate 2003; 57: 205-225.
48. Angelucci A, Schenone S, Gravina GL, Muzi P, Festuccia C, Vicentini C, Botta M, Bologna M,. Pyrazolo[3,4-d]pyrimidines c-Src inhibitors reduce epidermal growth factor-induced migration in prostate cancer cells. Eur J Cancer 2006; 42: 2838-2845.
49. Festuccia C, Angelucci A, Gravina G, Eleuterio E, Vicentini C, Bologna M,. Bombesindependent pro-MMP-9 activation in prostatic cancer cells requires beta1 integrin engagement. Exp Cell Res 2002; 280: 1-11.
50. Festuccia C, Vincentini C, di Pasquale AB, Aceto G, Zazzeroni F, Miano L, Bologna M,. Plasminogen activator activities in short-term tissue cultures of benign prostatic hyperplasia and prostatic carcinoma. Oncol Res 1995; 7: 131-138.
51. Festuccia C, Gravina GL, Muzi P, Pomante R, Ventura L, Vessella RL, Vicentini C, Bologna M,. Bicalutamide increases phospho-Akt levels through Her2 in patients with prostate cancer. Endocr Relat Cancer 2007; 14: 601-611.
52. Gravina GL, Marampon F, Petini F, Biordi L, Sherris D, Jannini EA, Tombolini V, Festuccia C,. The TORC1/TORC2 inhibitor, Palomid 529, reduces tumour growth and sensitises to docetaxel and cisplatin in aggressive and hormone-refractory prostate cancer cells. Endocr Relat Cancer 2011; 18: 385-400.
53. Bruzzese F, Di Gennaro E, Avallone A, Pepe S, Arra C, Caraglia M, Tagliaferri P, Budillon A,. Synergistic antitumor activity of epidermal growth factor receptor tyrosine kinase inhibitor gefitinib and IFN-alpha in head and neck cancer cells in vitro and in vivo. Clin Cancer Res 2006; 12: 617-625.
54. Yang M, Burton DW, Geller J, Hillegonds DJ, Hastings RH, Deftos LJ, Hoffman RM,. The bisphosphonate olpadronate inhibits skeletal prostate cancer progression in a green fluorescent protein nude mouse model. Clin Cancer Res 2006; 12: 2602-2606.
55. Domanska UM1, Timmer-Bosscha H, Nagengast WB, Oude Munnink TH, Kruizinga RC, Ananias HJ, Kliphuis NM, Huls G, De Vries EG, de Jong IJ, Walenkamp AM,. CXCR4 inhibition with AMD3100 sensitizes prostate cancer to docetaxel chemotherapy. Neoplasia. 2012; 14: 709-718.
56. Lee Y, Kim SJ, Park HD, Park EH, Huang SM, Jeon SB, Kim JM, Lim DS, Koh SS,. PAUF functions in the metastasis of human pancreatic cancer cells and upregulates CXCR4 expression. Oncogene 2010; 29: 56-67.
57. Ping YF, Yao XH, Jiang JY, Zhao LT, Yu SC, Jiang T, Lin MC, Chen JH, Wang B, Zhang R, Cui YH, Qian C, Wang Jm, Bian XW,. The chemokine CXCL12 and its receptor CXCR4 promote glioma stem cell-mediated VEGF production and tumour angiogenesis via PI3K/AKT signalling. J Pathol 2011; 224: 344-354.
58. Hasegawa T, Chosa N, Asakawa T, Yoshimura Y, Fujihara Y, Kitamura T, Tanaka M, Ishisaki A, Mitome M,. Differential effects of TGF-β1 and FGF-2 on SDF-1α expression in human periodontal ligament cells derived from deciduous teeth in vitro. Int J Mol Med 2012; 30: 35-40.
59. Addadi Y, Moskovits N, Granot D, Lozano G, Carmi Y, Apte RN, Neeman M, Oren M,. P53 status in stromal fibroblasts modulates tumour growth in an SDF1-dependent manner. Cancer Res 2010; 70: 9650-9658.
60. Richert MM, Vaidya KS, Mills CN, Wong D, Korz W, Hurst DR, Welch DR,. Inhibition of CXCR4 by CTCE-9908 inhibits breast cancer metastasis to lung and bone. Oncol Rep 2009; 21: 761-767.
61. Porvasnik S, Sakamoto N, Kusmartsev S, Eruslanov E, Kim WJ, Cao W, Urbanek C, Wong D, Goodison S, Rosser CJ,. Effects of CXCR4 antagonist CTCE-9908 on prostate tumor growth. Prostate 2009; 69: 1460-1469.
62. Uchida D, Onoue T, Kuribayashi N, Tomizuka Y, Tamatani T, Nagai H, Miyamoto Y,. Blockade of CXCR4 in oral squamous cell carcinoma inhibits lymph node metastases. Eur J Cancer 2011; 47: 452-459.
63. Sun YX, Schneider A, Jung Y, Wang J, Dai J, Wang J, Cook K, Osman NI, Koh-Paige AJ, Shim H, Pienta KJ, Keller ET, McCauley LK, Taichman RS,. Skeletal localization and neutralization of the SDF-1(CXCL12)/CXCR4 axis blocks prostate cancer metastasis and growth in osseous sites in vivo. J Bone Miner Res 2005; 20: 318-329.
64. Huang EH, Singh B, Cristofanilli M, Gelovani J, Wei C, Vincent L, Cook KR, Lucci A,. A CXCR4 antagonist CTCE-9908 inhibits primary tumor growth and metastasis of breast cancer. J Surg Res 2009; 155: 231-236.
65. Porvasnik S, Sakamoto N, Kusmartsev S, Eruslanov E, Kim WJ, Cao W, Urbanek C, Wong D, Goodison S, Rosser CJ,. Effects of CXCR4 antagonist CTCE-9908 on prostate tumor growth. Prostate 2009; 69: 1460-1469.
66. Hatano K, Yamaguchi S, Nimura K, Murakami K, Nagahara A, Fujita K, Uemura M, Nakai Y, Tsuchiya M, Nakayama M, Nonomura N, Kaneda Y,. Residual prostate cancer cells after docetaxel therapy increase the tumorigenic potential via constitutive signaling of CXCR4, ERK1/2 and c-Myc. Mol Cancer Res 2013; 11: 1088-1100.
67. Schulte J, Weidig M, Balzer P, Richter P, Franz M, Junker K, Gajda M, Friedrich K, Wunderlich H, Ostman A, Petersen I, Berndt A,. Expression of the E-cadherin repressors Snail, Slug and Zeb1 in urothelial carcinoma of the urinary bladder: Relation to stromal fibroblast activation and invasive behaviour of carcinoma cells. Histochem Cell Biol 2012; 138: 847-860.
68. Yu S, Xia S, Yang D, Wang K, Yeh S, Gao Z, Chang C,. Androgen receptor in human prostate cancer-associated fibroblasts promotes prostate cancer epithelial cell growth and invasion. Med Oncol 2013; 30: 674.