Genetic deletion of osteopontin in TRAMP mice skews prostate carcinogenesis from adenocarcinoma to aggressive human-like neuroendocrine cancers

Oncotarget

Volumn 7, Issue 4, 2016, Pages 3905-3920

  Mauri, Giorgio ^a   Jachetti, Elena ^a   Comuzzi, Barbara ^a   Dugo, Matteo ^a   Arioli, Ivano ^a   Miotti, Silvia ^a   Sangaletti, Sabina ^a   Di Carlo, Emma ^b   Tripodo, Claudio ^c   Colombo, Mario P ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF CHIETI   (Italy)

^c UNIVERSITY OF PALERMO   (Italy)

Author keywords

Extracellular matrix; Neuroendocrine; Osteopontin; Prostate cancer

Indexed keywords

ANDROGEN RECEPTOR; FILAMIN; KI 67 ANTIGEN; LAMININ; NERVE CELL ADHESION MOLECULE; OSTEOPONTIN; PROTEIN P63; PROTEIN TAG; SMAD3 PROTEIN; TRANSCRIPTION FACTOR E2F2; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PROGNOSIS; CARCINOGENESIS; CCND1 GENE; CCNE2 GENE; CONTROLLED STUDY; CORRELATIONAL STUDY; DOWN REGULATION; E2F2 GENE; FILAMIN GENE; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; MALE; MOUSE; NEUROENDOCRINE TUMOR; NONHUMAN; OPN GENE; PROSTATE ADENOCARCINOMA; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SMAD3 GENE; TGFB1 GENE; TUMOR GROWTH; TUMOR VOLUME; UPREGULATION; ADENOCARCINOMA; ANIMAL; C57BL MOUSE; CELL TRANSFORMATION; DISEASE COURSE; DISEASE MODEL; ENZYME IMMUNOASSAY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; PROSTATE TUMOR; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

ADENOCARCINOMA; ANIMALS; BLOTTING, WESTERN; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FLUORESCENT ANTIBODY TECHNIQUE; GENE DELETION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOENZYME TECHNIQUES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROENDOCRINE TUMORS; OSTEOPONTIN; PROSTATIC NEOPLASMS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84958012436     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6678     Document Type: Article

References (57)

1. Siegel R, Ma J, Zou Z and Jemal A. Cancer statistics, 2014. CA Cancer J Clin. 2014; 64:9-29.
2. Chiodoni C, Colombo MP and Sangaletti S. Matricellular proteins: from homeostasis to inflammation, cancer, and metastasis. Cancer Metastasis Rev. 2010; 29:295-307.
3. Grassinger J, Haylock DN, Storan MJ, Haines GO, Williams B, Whitty GA, Vinson AR, Be CL, Li S, Sorensen ES, Tam PP, Denhardt DT, Sheppard D, Choong PF and Nilsson SK. Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha9beta1 and alpha4beta1 integrins. Blood. 2009; 114:49-59.
4. Castellano G, Malaponte G, Mazzarino MC, Figini M, Marchese F, Gangemi P, Travali S, Stivala F, Canevari S and Libra M. Activation of the osteopontin/matrix metalloproteinase-9 pathway correlates with prostate cancer progression. Clin Cancer Res. 2008; 14:7470-7480.
5. Thalmann GN, Sikes RA, Devoll RE, Kiefer JA, Markwalder R, Klima I, Farach-Carson CM, Studer UE and Chung LW. Osteopontin: possible role in prostate cancer progression. Clin Cancer Res. 1999; 5:2271-2277.
6. Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, Cunha GR, Donjacour AA, Matusik RJ and Rosen JM. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A. 1995; 92:3439-3443.
7. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, Humphrey PA, Sundberg JP, Rozengurt N, Barrios R, Ward JM and Cardiff RD. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee. Cancer Res. 2004; 64:2270-2305.
8. di Sant'Agnese PA. Neuroendocrine differentiation in prostatic carcinoma: an update on recent developments. Ann Oncol. 2001; 12:S135-140.
9. Terry S and Beltran H. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol. 2014; 4:60.
10. Bostwick DG, Dousa MK, Crawford BG and Wollan PC. Neuroendocrine differentiation in prostatic intraepithelial neoplasia and adenocarcinoma. Am J Surg Pathol. 1994; 18:1240-1246.
11. Komiya A, Suzuki H, Imamoto T, Kamiya N, Nihei N, Naya Y, Ichikawa T and Fuse H. Neuroendocrine differentiation in the progression of prostate cancer. International journal of urology: official journal of the Japanese Urological Association. 2009; 16:37-44.
12. Chiaverotti T, Couto SS, Donjacour A, Mao JH, Nagase H, Cardiff RD, Cunha GR and Balmain A. Dissociation of epithelial and neuroendocrine carcinoma lineages in the transgenic adenocarcinoma of mouse prostate model of prostate cancer. Am J Pathol. 2008; 172:236-246.
13. Gingrich JR, Barrios RJ, Kattan MW, Nahm HS, Finegold MJ and Greenberg NM. Androgen-independent prostate cancer progression in the TRAMP model. Cancer Res. 1997; 57:4687-4691.
14. Zhang ZX, Xu QQ, Huang XB, Zhu JC and Wang XF. Early and delayed castrations confer a similar survival advantage in TRAMP mice. Asian J Androl. 2009; 11:291-297.
15. Greenberg NM, DeMayo FJ, Sheppard PC, Barrios R, Lebovitz R, Finegold M, Angelopoulou R, Dodd JG, Duckworth ML, Rosen JM et al. The rat probasin gene promoter directs hormonally and developmentally regulated expression of a heterologous gene specifically to the prostate in transgenic mice. Mol Endocrinol. 1994; 8:230-239.
16. Bono AV, Montironi R, Pannellini T, Sasso F, Mirone V, Musiani P and Iezzi M. Effects of castration on the development of prostate adenocarcinoma from its precursor HGPIN and on the occurrence of androgen-independent, poorly differentiated carcinoma in TRAMP mice. Prostate Cancer Prostatic Dis. 2008; 11:377-383.
17. Mazzoleni S, Jachetti E, Morosini S, Grioni M, Piras IS, Pala M, Bulfone A, Freschi M, Bellone M and Galli R. Gene signatures distinguish stage-specific prostate cancer stem cells isolated from transgenic adenocarcinoma of the mouse prostate lesions and predict the malignancy of human tumors. Stem Cells Transl Med. 2013; 2:678-689.
18. Huss WJ, Gray DR, Tavakoli K, Marmillion ME, Durham LE, Johnson MA, Greenberg NM and Smith GJ. Origin of androgen-insensitive poorly differentiated tumors in the transgenic adenocarcinoma of mouse prostate model. Neoplasia. 2007; 9:938-950.
19. Davis LD, Zhang W, Merseburger A, Young D, Xu L, Rhim JS, Moul JW, Srivastava S and Sesterhenn IA. p63 expression profile in normal and malignant prostate epithelial cells. Anticancer Res. 2002; 22:3819-3825.
20. Ferronika P, Triningsih FX, Ghozali A, Moeljono A, Rahmayanti S, Shadrina AN, Naim AE, Wudexi I, Arnurisa AM, Nanwani ST and Harijadi A. p63 cytoplasmic aberrance is associated with high prostate cancer stem cell expression. Asian Pac J Cancer Prev. 2012; 13:1943-1948.
21. Dhillon PK, Barry M, Stampfer MJ, Perner S, Fiorentino M, Fornari A, Ma J, Fleet J, Kurth T, Rubin MA and Mucci LA. Aberrant cytoplasmic expression of p63 and prostate cancer mortality. Cancer Epidemiol Biomarkers Prev. 2009; 18:595-600.
22. Miki J and Rhim JS. Prostate cell cultures as in vitro models for the study of normal stem cells and cancer stem cells. Prostate Cancer Prostatic Dis. 2008; 11:32-39.
23. Shukla S, Maclennan GT, Marengo SR, Resnick MI and Gupta S. Constitutive activation of P I3 K-Akt and NF-kappaB during prostate cancer progression in autochthonous transgenic mouse model. Prostate. 2005; 64:224-239.
24. Kumar AP, Bhaskaran S, Ganapathy M, Crosby K, Davis MD, Kochunov P, Schoolfield J, Yeh IT, Troyer DA and Ghosh R. Akt/cAMP-responsive element binding protein/cyclin D1 network: a novel target for prostate cancer inhibition in transgenic adenocarcinoma of mouse prostate model mediated by Nexrutine, a Phellodendron amurense bark extract. Clin Cancer Res. 2007; 13:2784-2794.
25. Sasaki A, Masuda Y, Ohta Y, Ikeda K and Watanabe K. Filamin associates with Smads and regulates transforming growth factor-beta signaling. J Biol Chem. 2001; 276:17871-17877.
26. Salm SN, Burger PE, Coetzee S, Goto K, Moscatelli D and Wilson EL. TGF-{beta} maintains dormancy of prostatic stem cells in the proximal region of ducts. J Cell Biol. 2005; 170:81-90.
27. Beltran H, Rickman DS, Park K, Chae SS, Sboner A, MacDonald TY, Wang Y, Sheikh KL, Terry S, Tagawa ST, Dhir R, Nelson JB, de la Taille A, et al. Molecular characterization of neuroendocrine prostate cancer and identification of new drug targets. Cancer Discov. 2011; 1:487-495.
28. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med. 1986; 315:1650-1659.
29. Sung SY and Chung LW. Prostate tumor-stroma interaction: molecular mechanisms and opportunities for therapeutic targeting. Differentiation. 2002; 70:506-521.
30. Brown LF, Papadopoulos-Sergiou A, Berse B, Manseau EJ, Tognazzi K, Perruzzi CA, Dvorak HF and Senger DR. Osteopontin expression and distribution in human carcinomas. Am J Pathol. 1994; 145:610-623.
31. Thoms JW, Dal Pra A, Anborgh PH, Christensen E, Fleshner N, Menard C, Chadwick K, Milosevic M, Catton C, Pintilie M, Chambers AF and Bristow RG. Plasma osteopontin as a biomarker of prostate cancer aggression: relationship to risk category and treatment response. Br J Cancer. 2012; 107:840-846.
32. Chaplet M, Waltregny D, Detry C, Fisher LW, Castronovo V and Bellahcene A. Expression of dentin sialophosphoprotein in human prostate cancer and its correlation with tumor aggressiveness. Int J Cancer. 2006; 118:850-856.
33. Bandopadhyay M, Bulbule A, Butti R, Chakraborty G, Ghorpade P, Ghosh P, Gorain M, Kale S, Kumar D, Kumar S, Totakura KV, Roy G, Sharma P, et al. Osteopontin as a therapeutic target for cancer. Expert Opin Ther Targets. 2014; 18:883-895.
34. Johnson MA, Iversen P, Schwier P, Corn AL, Sandusky G, Graff J and Neubauer BL. Castration triggers growth of previously static androgen-independent lesions in the transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Prostate. 2005; 62:322-338.
35. Caldon CE, Sergio CM, Schutte J, Boersma MN, Sutherland RL, Carroll JS and Musgrove EA. Estrogen regulation of cyclin E2 requires cyclin D1 but not c-Myc. Mol Cell Biol. 2009; 29:4623-4639.
36. Ellem SJ and Risbridger GP. Treating prostate cancer: a rationale for targeting local oestrogens. Nat Rev Cancer. 2007; 7:621-627.
37. Shukla S, Bhaskaran N, Babcook MA, Fu P, Maclennan GT and Gupta S. Apigenin inhibits prostate cancer progression in TRAMP mice via targeting PI3K/Akt/FoxO pathway. Carcinogenesis. 2014; 35:452-460.
38. Khor TO, Yu S, Barve A, Hao X, Hong JL, Lin W, Foster B, Huang MT, Newmark HL and Kong AN. Dietary feeding of dibenzoylmethane inhibits prostate cancer in transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 2009; 69:7096-7102.
39. Shukla S, MacLennan GT, Flask CA, Fu P, Mishra A, Resnick MI and Gupta S. Blockade of beta-catenin signaling by plant flavonoid apigenin suppresses prostate carcinogenesis in TRAMP mice. Cancer Res. 2007; 67:6925-6935.
40. Tzelepi V, Zhang J, Lu JF, Kleb B, Wu G, Wan X, Hoang A, Efstathiou E, Sircar K, Navone NM, Troncoso P, Liang S, Logothetis CJ, Maity SN and Aparicio AM. Modeling a lethal prostate cancer variant with small-cell carcinoma features. Clin Cancer Res. 2012; 18:666-677.
41. Margiotti K, Wafa LA, Cheng H, Novelli G, Nelson CC and Rennie PS. Androgen-regulated genes differentially modulated by the androgen receptor coactivator L-dopa decarboxylase in human prostate cancer cells. Mol Cancer. 2007; 6:38.
42. Wafa LA, Palmer J, Fazli L, Hurtado-Coll A, Bell RH, Nelson CC, Gleave ME, Cox ME and Rennie PS. Comprehensive expression analysis of L-dopa decarboxylase and established neuroendocrine markers in neoadjuvant hormone-treated versus varying Gleason grade prostate tumors. Hum Pathol. 2007; 38:161-170.
43. Stier S, Ko Y, Forkert R, Lutz C, Neuhaus T, Grunewald E, Cheng T, Dombkowski D, Calvi LM, Rittling SR and Scadden DT. Osteopontin is a hematopoietic stem cell niche component that negatively regulates stem cell pool size. J Exp Med. 2005; 201:1781-1791.
44. Massague J. TGFbeta in Cancer. Cell. 2008; 134:215-230.
45. Kim SG, Kim HA, Jong HS, Park JH, Kim NK, Hong SH, Kim TY and Bang YJ. The endogenous ratio of Smad2 and Smad3 influences the cytostatic function of Smad3. Mol Biol Cell. 2005; 16:4672-4683.
46. Wolfraim LA, Fernandez TM, Mamura M, Fuller WL, Kumar R, Cole DE, Byfield S, Felici A, Flanders KC, Walz TM, Roberts AB, Aplan PD, Balis FM and Letterio JJ. Loss of Smad3 in acute T-cell lymphoblastic leukemia. N Engl J Med. 2004; 351:552-559.
47. Patel SJ, Molinolo AA, Gutkind S and Crawford NP. Germline genetic variation modulates tumor progression and metastasis in a mouse model of neuroendocrine prostate carcinoma. PLoS One. 2013; 8:e61848.
48. Said N, Frierson HF, Jr., Chernauskas D, Conaway M, Motamed K and Theodorescu D. The role of SPARC in the TRAMP model of prostate carcinogenesis and progression. Oncogene. 2009; 28:3487-3498.
49. Derosa CA, Furusato B, Shaheduzzaman S, Srikantan V, Wang Z, Chen Y, Seifert M, Ravindranath L, Young D, Nau M, Dobi A, Werner T, McLeod DG, et al. Elevated osteonectin/SPARC expression in primary prostate cancer predicts metastatic progression. Prostate Cancer Prostatic Dis. 2012; 15:150-156.
50. Wirtzfeld LA, Wu G, Bygrave M, Yamasaki Y, Sakai H, Moussa M, Izawa JI, Downey DB, Greenberg NM, Fenster A, Xuan JW and Lacefield JC. A new three-dimensional ultrasound microimaging technology for preclinical studies using a transgenic prostate cancer mouse model. Cancer Res. 2005; 65:6337-6345.
51. Li S, Hu MG, Sun Y, Yoshioka N, Ibaragi S, Sheng J, Sun G, Kishimoto K and Hu GF. Angiogenin mediates androgen-stimulated prostate cancer growth and enables castration resistance. Mol Cancer Res. 2013; 11:1203-1214.
52. Sangaletti S, Tripodo C, Sandri S, Torselli I, Vitali C, Ratti C, Botti L, Burocchi A, Porcasi R, Tomirotti A, Colombo MP and Chiodoni C. Osteopontin shapes immunosuppression in the metastatic niche. Cancer Res. 2014; 74:4706-4719.
53. Chirgwin JM, Przybyla AE, MacDonald RJ and Rutter WJ. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979; 18:5294-5299.
54. Du P, Kibbe WA and Lin SM. lumi: a pipeline for processing Illumina microarray. Bioinformatics. 2008; 24:1547-1548.
55. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004; 3:Article3.
56. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genomewide expression profiles. Proc Natl Acad Sci U S A. 2005; 102:15545-15550.
57. Merico D, Isserlin R, Stueker O, Emili A and Bader GD. Enrichment map: a network-based method for gene-set enrichment visualization and interpretation. PLoS One. 2010; 5:e13984.