PAX3-FOXO1 induces cannabinoid receptor 1 to enhance cell invasion and metastasis

Cancer Research

Volumn 71, Issue 24, 2011, Pages 7471-7480

  Marshall, Amy D ^a   Lagutina, Irina ^a   Grosveld, Gerard C ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; CANNABINOID 1 RECEPTOR; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PAX3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; DRUG TARGETING; EX VIVO STUDY; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; LUNG PARENCHYMA; METASTASIS; MOUSE; MYOBLAST; NONHUMAN; PATHOPHYSIOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; RHABDOMYOSARCOMA; TREATMENT DURATION;

ANIMALS; BLOTTING, WESTERN; CELL LINE, TUMOR; CELL MOVEMENT; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MYOBLASTS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS, EXPERIMENTAL; ONCOGENE PROTEINS, FUSION; PAIRED BOX TRANSCRIPTION FACTORS; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA, ALVEOLAR; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 84255200394     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-0924     Document Type: Article

References (48)

1. Wexler L, Meyer W, Helman L. Rhabdomyosarcoma and the undifferentiated sarcomas. In: Pizzo P, Poplack D, editors. Principles and practice of pediatric oncology. 5th ed. Philidelphia, PA: Lippincott Williams and Wilkins; 2006. p. 971-1001.
2. Punyko JA, Mertens AC, Baker KS, Ness KK, Robison LL, Gurney JG. Long-term survival probabilities for childhood rhabdomyosarcoma. A population-based evaluation. Cancer 2005;103:1475-83. (Pubitemid 40410745)
3. Sorensen PH, Lynch JC, Qualman SJ, Tirabosco R, Lim JF, Maurer HM, et al. PAX3-FKHR and PAX7-FKHR gene fusions are prognostic indicators in alveolar rhabdomyosarcoma: a report from the children's oncology group. J Clin Oncol 2002;20:2672-9. (Pubitemid 34575640)
4. Galili N, Davis RJ, Fredericks WJ, Mukhopadhyay S, Rauscher FJ III, Emanuel BS, et al. Fusion of a fork head domain gene to PAX3 in the solid tumour alveolar rhabdomyosarcoma. Nat Genet 1993;5:230-5. (Pubitemid 23330384)
5. Davis RJ, D'Cruz CM, Lovell MA, Biegel JA, Barr FG. Fusion of PAX7 to FKHR by the variant t(1;13)(p36;q14) translocation in alveolar rhabdomyosarcoma. Cancer Res 1994;54:2869-72. (Pubitemid 24187765)
6. Fredericks WJ, Galili N, Mukhopadhyay S, Rovera G, Bennicelli J, Barr FG, et al. The PAX3-FKHR fusion protein created by the t(2;13) translocation in alveolar rhabdomyosarcomas is a more potent transcriptional activator than PAX3. Mol Cell Biol 1995;15:1522-35.
7. Wachtel M, Dettling M, Koscielniak E, Stegmaier S, Treuner J, Simon-Klingenstein K, et al. Gene expression signatures identify rhabdomyosarcoma subtypes and detect a novel t(2;2)(q35;p23) translocation fusing PAX3 to NCOA1. Cancer Res 2004;64:5539-45. (Pubitemid 39095545)
8. Davicioni E, Finckenstein FG, Shahbazian V, Buckley JD, Triche TJ, Anderson MJ. Identification of a PAX-FKHR gene expression signature that defines molecular classes and determines the prognosis of alveolar rhabdomyosarcomas. Cancer Res 2006;66:6936-46. (Pubitemid 44197668)
9. Lae M, Ahn E, Mercado G, Chuai S, Edgar M, Pawel B, et al. Global gene expression profiling of PAX-FKHR fusion-positive alveolar and PAX-FKHR fusion-negative embryonal rhabdomyosarcomas. J Pathol 2007;212:143-51. (Pubitemid 46852092)
10. Begum S, Emani N, Cheung A, Wilkins O, Der S, Hamel PA. Cell-type-specific regulation of distinct sets of gene targets by Pax3 and Pax3/FKHR. Oncogene 2005;24:1860-72. (Pubitemid 40462788)
11. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999;283:401-4.
12. Gye MC, Kang HH, Kang HJ. Expression of cannabinoid receptor 1 in mouse testes. Arch Androl 2005;51:247-55. (Pubitemid 40656009)
13. Cavuoto P, McAinch AJ, Hatzinikolas G, Janovska A, Game P, Wittert GA. The expression of receptors for endocannabinoids in human and rodent skeletal muscle. Biochem Biophys Res Commun 2007;364:105-10. (Pubitemid 47599452)
14. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci U S A 1999;96:5780-5. (Pubitemid 29234695)
15. Esposito I, Proto MC, Gazzerro P, Laezza C, Miele C, Alberobello AT, et al. The cannabinoid CB1 receptor antagonist rimonabant stimulates 2-deoxyglucose uptake in skeletal muscle cells by regulating the expression of phosphatidylinositol-3-kinase. Mol Pharmacol 2008;74:1678-86.
16. Bouaboula M, Perrachon S, Milligan L, Canat X, Rinaldi-Carmona M, Portier M, et al. A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. Evidence for a new model of receptor/ligand interactions. J Biol Chem 1997;272:22330-9. (Pubitemid 27382869)
17. Demuth DG, Molleman A. Cannabinoid signalling. Life Sci 2006;78:549-63. (Pubitemid 41785760)
18. Bifulco M, Laezza C, Portella G, Vitale M, Orlando P, De Petrocellis L, et al. Control by the endogenous cannabinoid system of ras oncogene-dependent tumor growth. FASEB J 2001;15:2745-7.
19. Song ZH, Zhong M. CB1 cannabinoid receptor-mediated cell migration. J Pharmacol Exp Ther 2000;294:204-9. (Pubitemid 30434688)
20. Rajesh M, Mukhopadhyay P, Hasko G, Pacher P. Cannabinoid CB1 receptor inhibition decreases vascular smooth muscle migration and proliferation. Biochem Biophys Res Commun 2008;377:1248-52.
21. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996;85:27-37. (Pubitemid 26116804)
22. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, et al. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997;91:649-59. (Pubitemid 27513656)
23. Rando TA, Blau HM. Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J Cell Biol 1994;125:1275-87. (Pubitemid 24189532)
24. Bois PR, Grosveld GC. FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J 2003;22:1147-57. (Pubitemid 36313598)
25. Lugo TG, Witte ON. The BCR-ABL oncogene transforms Rat-1 cells and cooperates with v-myc. Mol Cell Biol 1989;9:1263-70. (Pubitemid 19071695)
26. Nie J, Lewis DL. Structural domains of the CB1 cannabinoid receptor that contribute to constitutive activity and G-protein sequestration. J Neurosci 2001;21:8758-64. (Pubitemid 33054839)
27. Pear WS, Nolan GP, Scott ML, Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A 1993;90:8392-6. (Pubitemid 23277674)
28. Barr FG, Chatten J, D'Cruz CM, Wilson AE, Nauta LE, Nycum LM, et al. Molecular assays for chromosomal translocations in the diagnosis of pediatric soft tissue sarcomas. JAMA 1995;273:553-7.
29. Lam PY, Sublett JE, Hollenbach AD, Roussel MF. The oncogenic potential of the Pax3-FKHR fusion protein requires the Pax3 homeodomain recognition helix but not the Pax3 paired-box DNA binding domain. Mol Cell Biol 1999;19:594-601. (Pubitemid 29018461)
30. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 2006;20:2673-86. (Pubitemid 44498378)
31. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 2005;174:6477-89. (Pubitemid 40663843)
32. Oesch S, Walter D, Wachtel M, Pretre K, Salazar M, Guzman M, et al. Cannabinoid receptor 1 is a potential drug target for treatment of translocation-positive rhabdomyosarcoma. Mol Cancer Ther 2009;8:1838-45.
33. Picchione F, Pritchard C, Lagutina I, Janke L, Grosveld GC. IRIZIO: a novel gene cooperating with PAX3-FOXO1 in alveolar rhabdomyosarcoma (ARMS). Carcinogenesis 2010;32:452-61.
34. Keller C, Arenkiel BR, Coffin CM, El-Bardeesy N, DePinho RA, Capecchi MR. Alveolar rhabdomyosarcomas in conditional Pax3:Fkhr mice: cooperativity of Ink4a/ARF and Trp53 loss of function. Genes Dev 2004;18:2614-26. (Pubitemid 39453101)
35. Naini S, Etheridge KT, Adam SJ, Qualman SJ, Bentley RC, Counter CM, et al. Defining the cooperative genetic changes that temporally drive alveolar rhabdomyosarcoma. Cancer Res 2008;68:9583-8.
36. Wexler LH, Ladanyi M. Diagnosing alveolar rhabdomyosarcoma: morphology must be coupled with fusion confirmation. J Clin Oncol 2010;28:2126-8.
37. Wang D, Wang H, Ning W, Backlund MG, Dey SK, DuBois RN. Loss of cannabinoid receptor 1 accelerates intestinal tumor growth. Cancer Res 2008;68:6468-76.
38. Joseph J, Niggemann B, Zaenker KS, Entschladen F. Anandamide is an endogenous inhibitor for the migration of tumor cells and T lymphocytes. Cancer Immunol Immunother 2004;53:723-8. (Pubitemid 38962066)
39. Gary-Bobo M, Elachouri G, Scatton B, Le Fur G, Oury-Donat F, Bensaid M. The cannabinoid CB1 receptor antagonist rimonabant (SR141716) inhibits cell proliferation and increases markers of adipocyte maturation in cultured mouse 3T3 F442A preadipocytes. Mol Pharmacol 2006;69:471-8. (Pubitemid 43121944)
40. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010;10:550-60.
41. Sarnataro D, Pisanti S, Santoro A, Gazzerro P, Malfitano AM, Laezza C, et al. The cannabinoid CB1 receptor antagonist rimonabant (SR141716) inhibits human breast cancer cell proliferation through a lipid raft-mediated mechanism. Mol Pharmacol 2006;70:1298-306. (Pubitemid 44435982)
42. Sarfaraz S, Afaq F, Adhami VM, Malik A, Mukhtar H. Cannabinoid receptor agonist-induced apoptosis of human prostate cancer cells LNCaP proceeds through sustained activation of ERK1/2 leading to G1 cell cycle arrest. J Biol Chem 2006;281:39480-91. (Pubitemid 46041908)
43. Jacobsson SO, Wallin T, Fowler CJ. Inhibition of rat C6 glioma cell proliferation by endogenous and synthetic cannabinoids. Relative involvement of cannabinoid and vanilloid receptors. J Pharmacol Exp Ther 2001;299:951-9. (Pubitemid 33104965)
44. Santoro A, Pisanti S, Grimaldi C, Izzo AA, Borrelli F, Proto MC, et al. Rimonabant inhibits human colon cancer cell growth and reduces the formation of precancerous lesions in the mouse colon. Int J Cancer 2009;125:996-1003.
45. Cianchi F, Papucci L, Schiavone N, Lulli M, Magnelli L, Vinci MC, et al. Cannabinoid receptor activation induces apoptosis through tumor necrosis factor alpha-mediated ceramide de novo synthesis in colon cancer cells. Clin Cancer Res 2008;14:7691-700.
46. www.sanofi-aventis.com. Available from: http://en.sanofi.com/Images/ 14245-20081105-rimonabant-en.pdf (press release from Sanofi-Aventis dated Nov 5 2008).
47. Parasuraman S, Langston J, Rao BN, Poquette CA, Jenkins JJ, Merchant T, et al. Brain metastases in pediatric Ewing sarcoma and rhabdomyosarcoma: the St. Jude Children's Research Hospital experience. J Pediatr Hematol Oncol 1999;21:370-7. (Pubitemid 30306005)
48. LoVerme J, Duranti A, Tontini A, Spadoni G, Mor M, Rivara S, et al. Synthesis and characterization of a peripherally restricted CB1 cannabinoid antagonist, URB447, that reduces feeding and body-weight gain in mice. Bioorg Med Chem Lett 2009;19:639-43.