Cannabinoid receptor CB1 regulates STAT3 activity and its expression dictates the responsiveness to SR141716 treatment in human glioma patients' cells

Oncotarget

Volumn 6, Issue 17, 2015, Pages 15464-15481

  Ciaglia, Elena ^a   Torelli, Giovanni ^b,c   Pisanti, Simona ^a   Picardi, Paola ^a   D'Alessandro, Alba ^a   Laezza, Chiara ^d,e   Malfitano, Anna Maria ^a   Fiore, Donatella ^a   Pagano Zottola, Antonio Christian ^a   Proto, Maria Chiara ^a   Catapano, Giuseppe ^b   Gazzerro, Patrizia ^a   Bifulco, Maurizio ^a  

^a UNIVERSITY OF SALERNO   (Italy)

^b 'GRummo' Medical Hospital Department of Neurosurgery   (Italy)

^c UNIVERSITY HOSPITAL SAN GIOVANNI DI DIO E RUGGI D ARAGONA   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

CB1; Gliomas; MICA; NK cells; STAT3

Indexed keywords

ANTINEOPLASTIC AGENT; CANNABINOID 1 RECEPTOR; HLA ANTIGEN CLASS 1; MHC CLASS I-RELATED CHAIN A; PIPERIDINE DERIVATIVE; PYRAZOLE DERIVATIVE; RIMONABANT; SMALL INTERFERING RNA; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; ASTROCYTE; BIOSYNTHESIS; BRAIN NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; G1 PHASE CELL CYCLE CHECKPOINT; GENETICS; GLIOMA; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; NATURAL KILLER CELL; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SECRETION (PROCESS); TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; ASTROCYTES; BRAIN NEOPLASMS; CELL LINE, TUMOR; G1 PHASE CELL CYCLE CHECKPOINTS; GLIOMA; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; MICE; MICE, NUDE; PIPERIDINES; PYRAZOLES; RECEPTOR, CANNABINOID, CB1; RNA INTERFERENCE; RNA, SMALL INTERFERING; STAT3 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA1; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84934323718     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3895     Document Type: Article

References (54)

1. Kesari S. Understanding glioblastoma tumor biology: the potential to improve current diagnosis and treatments. Semin Oncol. 2011; 38:S2-10.
2. Pisanti S, Picardi P, D'Alessandro A, Laezza C, Bifulco M. The endocannabinoid signaling system in cancer. Trends Pharmacol Sci. 2013; 34:273-82. Review.
3. Velasco G, Sánchez C, Guzmán M. Towards the use of cannabinoids as antitumour agents. Nat Rev Cancer. 2012; 12:436-44.
4. Katona I, Freund TF. Endocannabinoid signaling as a synaptic circuit breaker in neurological disease. Nat Med. 2008; 14:923-30.
5. Aguado T, Monory K, Palazuelos J, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzmán M, Galve-Roperh I. The endocannabinoid system drives neural progenitor proliferation. FASEB J. 2005; 19:1704-6.
6. Aguado T, Palazuelos J, Monory K, Stella N, Cravatt B, Lutz B, Marsicano G, Kokaia Z, Guzmán M, Galve-Roperh I. The endocannabinoid system promotes astroglial differentiation by acting on neural progenitor cells. J Neurosci. 2006; 26:1551-61.
7. Chung SC, Hammarsten P, Josefsson A, Stattin P, Granfors T, Egevad L, Mancini G, Lutz B, Bergh A, Fowler CJ. A high cannabinoid CB receptor immunoreactivity is associated with disease severity and outcome in prostate cancer. Eur J Cancer. 2009; 45:174-82.
8. Michalski CW, Oti FE, Erkan M, Sauliunaite D, Bergmann F, Pacher P, Batkai S, Müller MW, Giese NA, Friess H, Kleeff J. Cannabinoids in pancreatic cancer: correlation with survival and pain. Int J Cancer. 2008; 122:742-50.
9. Messalli EM, Grauso F, Luise R, Angelini A, Rossiello R. Cannabinoid receptor type 1 immunoreactivity and disease severity in human epithelial ovarian tumors. Am J Obstet Gynecol. 2014; 211:234.e1-6.
10. Gustafsson SB, Palmqvist R, Henriksson ML, Dahlin AM, Edin S, Jacobsson SO, Öberg Å, Fowler CJ. High tumour cannabinoid CB1 receptor immunoreactivity negatively impacts disease-specific survival in stage II microsatellite stable colorectal cancer. PLoS One. 2011; 6:e23003.
11. Held-Feindt J, Dörner L, Sahan G, Mehdorn HM, Mentlein R. Cannabinoid receptors in human astroglial tumors. J Neurochem. 2006; 98:886-93.
12. Wu X, Han L, Zhang X, Li L, Jiang C, Qiu Y, Huang R, Xie B, Lin Z, Ren J, Fu J. Alteration of endocannabinoid system in human gliomas. J Neurochem. 2012; 120:842-9.
13. Marshall AD, Lagutina I, Grosveld GC. PAX3-FOXO1 induces cannabinoid receptor 1 to enhance cell invasion and metastasis. Cancer Res. 2011; 71:7471-80.
14. Petersen G, Moesgaard B, Schmid PC, Schmid HH, Broholm H, Kosteljanetz M, Hansen HS. Endocannabinoid metabolism in human glioblastomas and meningiomas compared to human non-tumour brain tissue. J Neurochem. 2005; 93:299-309.
15. Bifulco M, Grimaldi C, Gazzerro P, Pisanti S, Santoro A. Rimonabant: just an antiobesity drug? Current evidence on its pleiotropic effects. Mol Pharmacol. 2007; 71:1445-56.Review.
16. Malfitano AM, Laezza C, Galgani M, Matarese G, D'Alessandro A, Gazzerro P, Bifulco M. The CB1 receptor antagonist rimonabant controls cell viability and ascitic tumour growth in mice. Pharmacol Res. 2012; 65:365-71.
17. Gallotta D, Nigro P, Cotugno R, Gazzerro P, Bifulco M, Belisario MA. Rimonabant-induced apoptosis in leukemia cell lines: activation of caspase-dependent and-independent pathways. Biochem Pharmacol. 2010; 80:370-80.
18. Santoro A, Pisanti S, Grimaldi C, Izzo AA, Borrelli F, Proto MC, Malfitano AM, Gazzerro P, Laezza C, Bifulco M. 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.
19. Pisanti S, Picardi P, Prota L, Proto MC, Laezza C, McGuire PG, Morbidelli L, Gazzerro P, Ziche M, Das A, Bifulco M. Genetic and pharmacologic inactivation of cannabinoid CB1 receptor inhibits angiogenesis. Blood. 2011; 117:5541-50.
20. Flygare J, Gustafsson K, Kimby E, Christensson B, Sander B. Cannabinoid receptor ligands mediate growth inhibition and cell death in mantle cell lymphoma. FEBS Lett. 2005; 579:6885-9.
21. Friese MA, Platten M, Lutz SZ, Naumann U, Aulwurm S, Bischof F, Bühring HJ, Dichgans J, Rammensee HG, Steinle A, Weller M. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res. 2003; 63:8996-9006.
22. Hudspeth K, Silva-Santos B, Mavilio D. Natural cytotoxicity receptors: broader expression patterns and functions in innate and adaptive immune cells. Front Immunol. 2014; 4:69.
23. Zitvogel L, Apetoh L, Ghiringhelli F, André F, Tesniere A, Kroemer G. The anticancer immune response: indispensable for therapeutic success? J Clin Invest. 2008; 118:1991-2001. Review.
24. Roy LO, Poirier MB, Fortin D. Transforming growth factor-beta and its implication in the malignancy of gliomas. Target Oncol. 2014; [Epub ahead of print].
25. Wu A, Wei J, Kong LY, Wang Y, Priebe W, Qiao W, Sawaya R, Heimberger AB. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol. 2010; 12:1113-25.
26. Igney FH, Krammer PH. Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol. 2002; 71:907-20.
27. Jin K, Xie L, Kim SH, Parmentier-Batteur S, Sun Y, Mao XO, Childs J, Greenberg DA. Defective adult neurogenesis in CB1 cannabinoid receptor knockout mice. Mol Pharmacol. 2004; 66:204-8.
28. 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.
29. Teixeira-Clerc F, Julien B, Grenard P, Tran Van Nhieu J, Deveaux V, Li L, Serriere-Lanneau V, Ledent C, Mallat A, Lotersztajn S. CB1 cannabinoid receptor antagonism: a new strategy for the treatment of liver fibrosis. Nat Med. 2006; 12:671-6.
30. Mukhopadhyay B, Schuebel K, Mukhopadhyay P, Cinar R, Godlewski G, Xiong K, Mackie K, Lizak M, Yuan Q, Goldman D, Kunos G. Cannabinoid receptor 1 promotes hepatocellular carcinoma initiation and progression through multiple mechanisms. Hepatology. 2015; 61:1615-26.
31. Bifulco M, Ciaglia E. Cannabinoid receptor 1 antagonism in hepatocellular carcinoma: killing two birds with one stone. Eur J Gastroenterol Hepatol. 2015; 27:747-8.
32. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE Jr. Stat3 as an oncogene. Cell. 1999; 98:295-303.
33. Bedel R, Thiery-Vuillemin A, Grandclement C, Balland J, Remy-Martin JP, Kantelip B, Pallandre JR, Pivot X, Ferrand C, Tiberghien P, Borg C. Novel role for STAT3 in transcriptional regulation of NK immune cell targeting receptor MICA on cancer cells. Cancer Res. 2011; 71:1615-26.
34. Alvarez JV, Frank DA. Genome-wide analysis of STAT target genes: elucidating the mechanism of STAT-mediated oncogenesis. Cancer Biol Ther. 2004; 3:1045-50.
35. Bosier B, Bellocchio L, Metna-Laurent M, Soria-Gomez E, Matias I, Hebert-Chatelain E, Cannich A, Maitre M, Leste-Lasserre T, Cardinal P, Mendizabal-Zubiaga J, Canduela MJ, Reguero L, et al. Astroglial CB1 cannabinoid receptors regulate leptin signaling in mouse brain astrocytes. Mol Metab. 2013; 2:393-404.
36. Zhou H, Zhang Z, Wei H, Wang F, Guo F, Gao Z, Marsicano G, Wang Q, Xiong L. Activation of STAT3 is involved in neuroprotection by electroacupuncture pretreatment via cannabinoid CB1 receptors in rats. Brain Res. 2013; 1529:154-64.
37. Janssen JW, Steenvoorden AC, Schmidtberger M, Bartram CR. Activation of the mas oncogene during transfection of monoblastic cell line DNA. Leukemia. 1988; 2:318-320.
38. Julius D, Livelli TJ, Jessell TM, Axel R. Ectopic expression of the serotonin 1c receptor and the triggering of malignant transformation. Science. 1989; 244:1057-1062.
39. Alberich Jordà M, Rayman N, Tas M, Verbakel SE, Battista N, van Lom K, Löwenberg B, Maccarrone M, Delwel R. The peripheral cannabinoid receptor Cb2, frequently expressed on AML blasts, either induces a neutrophilic differentiation block or confers abnormal migration properties in a ligand-dependent manner. Blood. 2004; 104:526-34.
40. Kapur A, Zhao P, Sharir H, Bai Y, Caron MG, Barak LS, Abood ME. Atypical responsiveness of the orphan receptor GPR55 to cannabinoid ligands. J Biol Chem. 2009; 284:29817-27.
41. Andradas C, Caffarel MM, Pérez-Gómez E, Salazar M, Lorente M, Velasco G, Guzmán M, Sánchez C. The orphan G protein-coupled receptor GPR55 promotes cancer cell proliferation via ERK. Oncogene. 2011; 30:245-52.
42. Pérez-Gómez E, Andradas C, Flores JM, Quintanilla M, Paramio JM, Guzmán M, Sánchez C. The orphan receptor GPR55 drives skin carcinogenesis and is upregulated in human squamous cell carcinomas. Oncogene. 2013; 32:2534-42.
43. Moreno E, Andradas C, Medrano M, Caffarel MM, Pérez-Gómez E, Blasco-Benito S, Gómez-Cañas M, Pazos MR, Irving AJ, Lluís C, Canela EI, Fernández-Ruiz J, Guzmán M, et al. Targeting CB2-GPR55 Receptor Heteromers Modulates Cancer Cell Signaling. J Biol Chem. 2014; Jun 18; pii: jbc.M114.561761.
44. Navarro G, Ferré S, Cordomi A, Moreno E, Mallol J, Casadó V, Cortés A, Hoffmann H, Ortiz J, Canela EI, Lluís C, Pardo L, Franco R, Woods AS. Interactions between intracellular domains as key determinants of the quaternary structure and function of receptor heteromers. J Biol Chem. 2010; 285:27346-27359.
45. Rios C, Gomes I, Devi L. mu opioid and CB1 cannabinoid receptor interactions: reciprocal inhibition of receptor signaling and neuritogenesis. Br J Pharmacol. 2006; 148:387-395.
46. Ellis J, Pediani JD, Canals M, Milasta S, Milligan G. Orexin-1 receptor cannabinoid CB1 receptor heterodimerization results in both ligand-dependent and-independent coordinated alterations of receptor localization and function. J Biol Chem. 2006; 281:38812-38824.
47. Rozenfeld R, Gupta A, Gagnidze K, Lim MP, Gomes I, Lee-Ramos D, Nieto N, Devi LA. AT1R-CB(1)R heteromerization reveals a new mechanism for the pathogenic properties of angiotensin II. EMBO J. 2011; 30:2350-2363.
48. Kargl J, Balenga N, Parzmair GP, Brown AJ, Heinemann A, Waldhoer M. The cannabinoid receptor CB1 modulates the signaling properties of the lysophosphatidylinositol receptor GPR55. J Biol Chem. 2012; 287:44234-48.
49. Mirandola P, Ponti C, Gobbi G, Sponzilli I, Vaccarezza M, Cocco L, Zauli G, Secchiero P, Manzoli FA, Vitale M. Activated human NK and CD8+ T cells express both TNF-related apoptosis-inducing ligand (TRAIL) and TRAIL receptors but are resistant to TRAIL-mediated cytotoxicity. Blood. 2004; 104:2418-24.
50. Niu G, Wright KL, Ma Y, Wright GM, Huang M, Irby R, Briggs J, Karras J, Cress WD, Pardoll D, Jove R, Chen J, Yu H. Role of Stat3 in regulating p53 expression and function. Mol Cell Biol. 2005; 25:7432-40.
51. Li H, Lakshmikanth T, Garofalo C, Enge M, Spinnler C, Anichini A, Szekely L, Kärre K, Carbone E, Selivanova G. Pharmacological activation of p53 triggers anticancer innate immune response through induction of ULBP2. Cell Cycle. 2011; 10:3346-58.
52. Ciaglia E, Pisanti S, Picardi P, Laezza C, Malfitano AM, D'Alessandro A, Gazzerro P, Vitale M, Carbone E, Bifulco M. N6-isopentenyladenosine, an endogenous isoprenoid end product, directly affects cytotoxic and regulatory functions of human NK cells through FDPS modulation. J Leukoc Biol. 2013; 94:1207-19.
53. Ciaglia E, Pisanti S, Picardi P, Laezza C, Sosa S, Tubaro A, Vitale M, Gazzerro P, Malfitano AM, Bifulco M. N6-isopentenyladenosine affects cytotoxic activity and cytokines production by IL-2 activated NK cells and exerts topical anti-inflammatory activity in mice. Pharmacol Res. 2014; 89:1-10.
54. Hammarsten P, Karalija A, Josefsson A, Rudolfsson SH, Wikström P, Egevad L, Granfors T, Stattin P, Bergh A. Low levels of phosphorylated epidermal growth factor receptor in nonmalignant and malignant prostate tissue predict favorable outcome in prostate cancer patients. Clin Cancer Res. 2010; 16:1245-55.