Calcitonin receptor-stimulated migration of prostate cancer cells is mediated by urokinase receptor-integrin signaling

Clinical and Experimental Metastasis

Volumn 24, Issue 5, 2007, Pages 363-377

  Thomas, Shibu ^a   Chiriva Internati, Maurizio ^b   Shah, Girish V ^a  

^a UNIVERSITY OF LOUISIANA AT MONROE   (United States)

^b TEXAS TECH UNIVERSITY   (United States)

Author keywords

Adhesion; Calcitonin; Calcitonin receptor; Integrins; Migration; Prostate cancer cells

Indexed keywords

ALPHA6BETA5 INTEGRIN; CALCITONIN; CALCITONIN RECEPTOR; COLLAGEN; FIBRONECTIN; INTEGRIN; UNCLASSIFIED DRUG; UROKINASE; UROKINASE RECEPTOR; VITRONECTIN; VITRONECTIN RECEPTOR;

ARTICLE; CANCER CELL CULTURE; CANCER INVASION; CELL AGGREGATION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; METASTASIS POTENTIAL; PROSTATE CANCER; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SPHEROID CELL;

CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXTRACELLULAR MATRIX PROTEINS; HUMANS; INTEGRIN ALPHAVBETA3; MALE; NEOPLASM INVASIVENESS; PROSTATIC NEOPLASMS; RECEPTORS, CALCITONIN; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; UP-REGULATION; URINARY PLASMINOGEN ACTIVATOR;

EID: 34547237682     PISSN: 02620898     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10585-007-9073-y     Document Type: Article

References (59)

1. Presti JC Jr (2000) Prostate cancer: assessment of risk using digital rectal examination, tumor grade, prostate-specific antigen, and systematic biopsy. Radiol Clin North Am 38(1):49-58
2. Thompson IM, Pauler DK, Goodman PJ, Tangen CM, Lucia MS, Parnes HL, Minasian LM, Ford LG, Lippman SM, Crawford ED, Crowley JJ, Coltman CA Jr (2004) Prevalence of prostate cancer among men with a prostate-specific antigen level < or = 4.0 ng per milliliter. N Engl J Med 350(22):2239-2246
3. Furuya Y, Akakura K, Akimoto S, Inomiya H, Ito H (1999) Pattern of progression and survival in hormonally treated metastatic prostate cancer. Int J Urol 6(5):240-244
4. Segawa N, Mori I, Utsunomiya H, Nakamura M, Nakamura Y, Shan L, Kakudo K, Katsuoka Y (2001) Prognostic significance of neuroendocrine differentiation, proliferation activity and androgen receptor expression in prostate cancer. Pathol Int 51(6):452-459
5. Vilches J, Salido M, Fernandez-Segura E, Roomans GM (2004) Neuropeptides, apoptosis and ion changes in prostate cancer. Methods of study and recent developments. Histol Histopathol 19(3):951-961
6. Tilley WD, Buchanan G, Hickey TE, Bentel JM (1996) Mutations in the androgen receptor gene are associated with progression of human prostate cancer to androgen independence. Clin Cancer Res 2(2):277-285
7. Miyake H, Nelson C, Rennie PS, Gleave ME (2000) Acquisition of chemoresistant phenotype by overexpression of the antiapoptotic gene testosterone-repressed prostate message-2 in prostate cancer xenograft models. Cancer Res 60(9):2547-2554
8. Kaibuchi T, Furuya Y, Akakura K, Masai M, Ito H (2000) Changes in cell proliferation and apoptosis during local progression of prostate cancer. Anticancer Res 20(2B):1135-1139
9. Howell SB (2000) Resistance to apoptosis in prostate cancer cells. Mol Urol 4(3):225-229; Discussion 231
10. Winter RN, Kramer A, Borkowski A, Kyprianou N (2001) Loss of caspase-1 and caspase-3 protein expression in human prostate cancer. Cancer Res 61(3):1227-1232
11. Bonkhoff H (1996) Role of the basal cells in premalignant changes of the human prostate: a stem cell concept for the development of prostate cancer. Eur Urol 30:201-205
12. Rennie PS, Nelson CC (1998) Epigenetic mechanisms for progression of prostate cancer. Cancer Metastasis Rev 17:401-409
13. Chien J, Ren Y, Qing Wang Y, Bordelon W, Thompson E, Davis R, Rayford W, Shah G (2001) Calcitonin is a prostate epithelium-derived growth stimulatory peptide. Mol Cell Endocrinol 181(1-2):69-79
14. Sabbisetti VS, Chirugupati S, Thomas S, Vaidya KS, Reardon D, Chiriva-Internati M, Iczkowski KA, Shah GV (2005) Calcitonin increases invasiveness of prostate cancer cells: role for cyclic AMP-dependent protein kinase a in calcitonin action. Int J Cancer 117(4):551-560
15. Shah GV, Rayford W, Noble MJ, Austenfeld M, Weigel J, Vamos S, Mebust WK (1994) Calcitonin stimulates growth of human prostate cancer cells through receptor-mediated increase in cyclic adenosine 3',5'-monophosphates and cytoplasmic Ca2+ transients. Endocrinology 134(2):596-602
16. Ritchie CK, Thomas KG, Andrews LR, Tindall DJ, Fitzpatrick LA (1997) Effects of the calciotrophic peptides calcitonin and parathyroid hormone on prostate cancer growth and chemotaxis. Prostate 30:183-187
17. Chigurupati S, Kulkarni T, Thomas S, Shah G (2005) Calcitonin stimulates multiple stages of angiogenesis by directly acting on endothelial cells. Cancer Res 65(18):8519-8529
18. Thomas S, Chigurupati S, Anbalagan M, Shah G (2006) Calcitonin increases tumorigenicity of prostate cancer cells: evidence for the role of protein kinase a and urokinase-type plasminogen receptor. Mol Endocrinol 20(8):1894-1991
19. Pulukuri SM, Gondi CS, Lakka SS, Jutla A, Estes N, Gujrati M, Rao JS (2005) RNA interference-directed knockdown of urokinase plasminogen activator and urokinase plasminogen activator receptor inhibits prostate cancer cell invasion, survival, and tumorigenicity in vivo. J Biol Chem 280(43):36529-36540
20. Gondi CS, Lakka SS, Yanamandra N, Olivero WC, Dinh DH, Gujrati M, Tung CH, Weissleder R, Rao JS (2004) Adenovirus-mediated expression of antisense urokinase plasminogen activator receptor and antisense cathepsin B inhibits tumor growth, invasion, and angiogenesis in gliomas. Cancer Res 64(12):4069-4077
21. Sabbisetti V, Chigurupati S, Thomas S, Shah G (2006) Calcitonin stimulates the secretion of urokinase-type plasminogen activator from prostate cancer cells: its possible implications on tumor cell invasion. Int J Cancer 118(11):2694-2702
22. Chien J, Shah GV (2001) Role of stimulatory guanine nucleotide binding protein (GSalpha) in proliferation of PC-3M prostate cancer cells. Int J Cancer 91(1):46-54
23. Sabbisetti VS, Chigurupati S, Thomas S, Shah GV (2005) Calcitonin stimulates the secretion of urokinase-type plasminogen activator from prostate cancer cells: its possible implications on tumor cell invasion. Int J Cancer 118(11):2694-2702
24. Wei Y, Eble JA, Wang Z, Kreidberg JA, Chapman HA (2001) Urokinase receptors promote beta1 integrin function through interactions with integrin alpha3beta1. Mol Biol Cell 12(10):2975-2986
25. Chapman HA, Wei Y, Simon DI, Waltz DA (1999) Role of urokinase receptor and caveolin in regulation of integrin signaling. Thromb Haemost 82(2):291-297
26. Wary KK, Mariotti A, Zurzolo C, Giancotti FG (1998) A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94(5):625-634
27. Cohen MB, Griebling TL, Ahaghotu CA, Rokhlin OW, Ross JS (1997) Cellular adhesion molecules in urologic malignancies. Am J Clin Pathol 107:56-63
28. Fornaro M, Manes T, Languino LR (2001) Integrins and prostate cancer metastases. Cancer Metastasis Rev 20(3-4):321-331
29. Zheng DQ, Woodard AS, Fornaro M, Tallini G, Languino LR (1999) Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway. Cancer Res 59(7):1655-1664
30. Rabinovitz I, Nagle RB, Cress AE (1995) Integrin alpha 6 expression in human prostate carcinoma cells is associated with a migratory and invasive phenotype in vitro and in vivo. Clin Exp Metastasis 13(6):481-491
31. Tremblay L, Hauck W, Nguyen LT, Allard P, Landry F, Chapdelaine A, Chevalier S (1996) Regulation and activation of focal adhesion kinase and paxillin during the adhesion, proliferation, and differentiation of prostatic epithelial cells in vitro and in vivo. Mol Endocrinol 10:1010-1020
32. Tahiliani PD, Singh L, Auer KL, LaFlamme SE (1997) The role of conserved amino acid motifs within the integrin beta3 cytoplasmic domain in triggering focal adhesion kinase phosphorylation. J Biol Chem 272(12):7892-7898
33. Ren Y, Sun Y-P, Shah GV (2003) Calcitonin inhibits prolactin promoter activity in rat pituitary GGH3 cells: evidence for the involvement of p42/44 mitogen-activated protein kinase in calcitonin action. Endocrine 20(1-2):13-22
34. Shah GV, Deftos LJ, Crowley WR (1993) Synthesis and release of calcitonin-like immunoreactivity by anterior pituitary cells: evidence for a role in paracrine regulation of prolactin secretion. Endocrinology 132(3):1367-1372
35. Nagakawa O, Ogasawara M, Fujii H, Murakami K, Murata J, Fuse H, Saiki I (1998) Effect of prostatic neuropeptides on invasion and migration of PC-3 prostate cancer cells. Cancer Lett 133(1):27-33
36. Thomas S, GV S (2005) Calcitonin induces apoptosis resistance in prostate cancer cell lines against cytotoxic drugs via the Akt/survivin pathway. Cancer Biol Ther 4(11):1226-1233
37. Salido M, Vilches J, Lopez A (2000) Neuropeptides bombesin and calcitonin induce resistance to etoposide induced apoptosis in prostate cancer cell lines. Histol Histopathol 15(3):729-738
38. Heuser M, Ringert RH, Zoeller G, Hemmerlein B (2003) Dynamic assessment of angiogenesis in renal cell carcinoma spheroids by intravital microscopy. J Urol 169(4):1267-1270
39. Hoevel T, Macek R, Swisshelm K, Kubbies M (2004) Reexpression of the TJ protein CLDN1 induces apoptosis in breast tumor spheroids. Int J Cancer 108(3):374-383
40. Waltz DA, Chapman HA (1994) Reversible cellular adhesion to vitronectin linked to urokinase receptor occupancy. J Biol Chem 269(20):14746-14750
41. Ghosh S, Johnson JJ, Sen R, Mukhopadhyay S, Liu Y, Zhang F, Wei Y, Chapman HA, Stack MS (2006) Functional relevance of urinary-type plasminogen activator receptor-alpha3beta1 integrin association in proteinase regulatory pathways. J Biol Chem 281(19):13021-13029
42. Llinas P, Le Du MH, Gardsvoll H, Dano K, Ploug M, Gilquin B, Stura EA, Menez A (2005) Crystal structure of the human urokinase plasminogen activator receptor bound to an antagonist peptide. Embo J 24(9):1655-1663
43. Aprikian AG, Tremblay L, Han K, Chevalier S (1997) Bombesin stimulates the motility of human prostate-carcinoma cells through tyrosine phosphorylation of focal adhesion kinase and of integrin-associated proteins. Int J Cancer 72(3):498-504
44. Kugler MC, Wei Y, Chapman HA (2003) Urokinase receptor and integrin interactions. Curr Pharm Des 9(19):1565-1574
45. Wei Y, Lukashev M, Simon DI, Bodary SC, Rosenberg S, Doyle MV, Chapman HA (1996) Regulation of integrin function by the urokinase receptor. Science 273(5281):1551-1555
46. Xue W, Mizukami I, Todd RF III, Petty HR (1997) Urokinase-type plasminogen activator receptors associate with beta1 and beta3 integrins of fibrosarcoma cells: dependence on extracellular matrix components. Cancer Res 57(9):1682-1689
47. Degryse B, Orlando S, Resnati M, Rabbani SA, Blasi F (2001) Urokinase/urokinase receptor and vitronectin/alpha(v)beta(3) integrin induce chemotaxis and cytoskeleton reorganization through different signaling pathways. Oncogene 20(16):2032-2043
48. Hapke S, Kessler H, Arroyo de Prada N, Benge A, Schmitt M, Lengyel E, Reuning U (2001) Integrin alpha(v)beta(3)/vitronectin interaction affects expression of the urokinase system in human ovarian cancer cells. J Biol Chem 276(28):26340-26348
49. Cary LA, Guan JL (1999) Focal adhesion kinase in integrin-mediated signaling. Front Biosci 4:D102-D113
50. Tilghman RW, Slack-Davis JK, Sergina N, Martin KH, Iwanicki M, Hershey ED, Beggs HE, Reichardt LF, Parsons JT (2005) Focal adhesion kinase is required for the spatial organization of the leading edge in migrating cells. J Cell Sci 118(Pt 12):2613-2623
51. Cary LA, Han DC, Polte TR, Hanks SK, Guan JL (1998) Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 140(1):211-221
52. Cary LA, Chang JF, Guan JL (1996) Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J Cell Sci 109(Pt 7):1787-1794
53. Zhang Z, Baron R, Horne WC (2000) Integrin engagement, the actin cytoskeleton, and c-Src are required for the calcitonin-induced tyrosine phosphorylation of paxillin and HEF1, but not for calcitonin-induced Erk1/2 phosphorylation. J Biol Chem 275(47):37219-37223
54. Lacoste J, Aprikian AG, Chevalier S (2005) Focal adhesion kinase is required for bombesin-induced prostate cancer cell motility. Mol Cell Endocrinol 235(1-2):51-61
55. Liu D, Aguirre Ghiso J, Estrada Y, Ossowski L (2002) EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma. Cancer Cell 1(5):445-457
56. Slack JK, Adams RB, Rovin JD, Bissonette EA, Stoker CE, Parsons JT (2001) Alterations in the focal adhesion kinase/Src signal transduction pathway correlate with increased migratory capacity of prostate carcinoma cells. Oncogene 20(10):1152-1163
57. Sumitomo M, Shen R, Walburg M, Dai J, Geng Y, Navarro D, Boileau G, Papandreou CN, Giancotti FG, Knudsen B, Nanus DM (2000) Neutral endopeptidase inhibits prostate cancer cell migration by blocking focal adhesion kinase signaling. J Clin Invest 106(11):1399-1407
58. Slack-Davis JK, Parsons JT (2004) Emerging views of integrin signaling: implications for prostate cancer. J Cell Biochem 91(1):41-46
59. Nemeth JA, Cher ML, Zhou Z, Mullins C, Bhagat S, Trikha M (2003) Inhibition of alpha(v)beta3 integrin reduces angiogenesis, bone turnover, and tumor cell proliferation in experimental prostate cancer bone metastases. Clin Exp Metastasis 20(5):413-420