β3-adrenoreceptor blockade reduces tumor growth and increases neuronal differentiation in neuroblastoma via SK2/S1P
Adrenergic beta-3 Receptor Antagonists
/ pharmacology
Animals
Carcinogenesis
/ drug effects
Cell Differentiation
/ drug effects
Cell Proliferation
/ drug effects
Gene Expression Regulation, Neoplastic
/ drug effects
Heterografts
Humans
Lysophospholipids
/ metabolism
Mice
Neuroblastoma
/ drug therapy
Neurons
/ drug effects
Propanolamines
/ pharmacology
Receptors, Adrenergic, beta-3
/ genetics
Signal Transduction
/ drug effects
Small-Conductance Calcium-Activated Potassium Channels
/ genetics
Sphingosine
/ analogs & derivatives
Sphingosine-1-Phosphate Receptors
/ genetics
Tumor Hypoxia
/ drug effects
Journal
Oncogene
ISSN: 1476-5594
Titre abrégé: Oncogene
Pays: England
ID NLM: 8711562
Informations de publication
Date de publication:
01 2020
01 2020
Historique:
received:
10
01
2019
accepted:
03
06
2019
revised:
14
05
2019
pubmed:
4
9
2019
medline:
18
4
2020
entrez:
4
9
2019
Statut:
ppublish
Résumé
Neuroblastoma (NB) is the most frequently observed among extracranial pediatric solid tumors. It displays an extreme clinical heterogeneity, in particular for the presentation at diagnosis and response to treatment, often depending on cancer cell differentiation/stemness. The frequent presence of elevated hematic and urinary levels of catecholamines in patients affected by NB suggests that the dissection of adrenergic system is crucial for a better understanding of this cancer. β3-adrenoreceptor (β3-AR) is the last identified member of adrenergic receptors, involved in different tumor conditions, such as melanoma. Multiple studies have shown that the dysregulation of the bioactive lipid sphingosine 1-phosphate (S1P) metabolism and signaling is involved in many pathological diseases including cancer. However, whether S1P is crucial for NB progression and aggressiveness is still under investigation. Here we provide experimental evidence that β3-AR is expressed in NB, both human specimens and cell lines, where it is critically involved in the activation of proliferation and the regulation between stemness/differentiation, via its functional cross-talk with sphingosine kinase 2 (SK2)/S1P receptor 2 (S1P
Identifiants
pubmed: 31477835
doi: 10.1038/s41388-019-0993-1
pii: 10.1038/s41388-019-0993-1
pmc: PMC6949192
doi:
Substances chimiques
3-(2-ethylphenoxy)-1-(1,2,3,4-tetrahydronaphth-1-ylamino)-2-propanol oxalate
0
Adrenergic beta-3 Receptor Antagonists
0
KCNN2 protein, human
0
Lysophospholipids
0
Propanolamines
0
Receptors, Adrenergic, beta-3
0
S1PR2 protein, human
0
Small-Conductance Calcium-Activated Potassium Channels
0
Sphingosine-1-Phosphate Receptors
0
sphingosine 1-phosphate
26993-30-6
Sphingosine
NGZ37HRE42
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
368-384Références
Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet. 2007;369:2106–20.
pubmed: 17586306
Brodeur GM. Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer. 2003;3:203–16.
pubmed: 12612655
Cohn SL, Pearson ADJ, London WB, Monclair T, Ambros PF, Brodeur GM, et al. The International Neuroblastoma Risk Group (INRG) Classification System: An INRG Task Force Report. J Clin Oncol. 2009;27:289–97.
pubmed: 19047291
pmcid: 2650388
London WB, Bagatell R, Weigel BJ, Fox E, Guo D, Van Ryn C, et al. Historical time-to-progression (TTP) and progression-free survival (PFS) in relapsed/refractory neuroblastoma modern-era (2002-14) patients from Children’s Oncology Group (COG) early-phase trials. Cancer. 2017;123:4914–23.
pubmed: 28885700
pmcid: 5716896
Garaventa A, Parodi S, De Bernardi B, Dau D, Manzitti C, Conte M, et al. Outcome of children with neuroblastoma after progression or relapse. A retrospective study of the Italian neuroblastoma registry. Eur J Cancer. 2009;45:2835–42.
pubmed: 19616426
Léauté-Labrèze C, de la Roque ED, Hubiche T, Boralevi F, Thambo J-B, Taïeb A. Propranolol for Severe Hemangiomas of Infancy. 2009. https://doi.org/10.1056/NEJMc0708819 .
pubmed: 18550886
Stiles J, Amaya C, Pham R, Rowntree RK, Lacaze M, Mulne A, et al. Propranolol treatment of infantile hemangioma endothelial cells: a molecular analysis. Exp Ther Med. 2012;4:594–604.
pubmed: 23170111
pmcid: 3501380
Daguzé J, Saint-Jean M, Peuvrel L, Cassagnau E, Quéreux G, Khammari A, et al. Visceral metastatic angiosarcoma treated effectively with oral cyclophosphamide combined with propranolol. JAAD Case Rep. 2016;2:497–9.
pubmed: 28004027
pmcid: 5161779
Montoya A, Amaya CN, Belmont A, Diab N, Trevino R, Villanueva G, et al. Use of non-selective β-blockers is associated with decreased tumor proliferative indices in early stage breast cancer. Oncotarget. 2016;8:6446–60.
pmcid: 5351644
Watkins JL, Thaker PH, Nick AM, Ramondetta LM, Kumar S, Urbauer DL, et al. Clinical impact of selective and non-selective beta blockers on survival in ovarian cancer patients. Cancer. 2015;121:3444–51.
pubmed: 26301456
pmcid: 4575637
Moretti S, Massi D, Farini V, Baroni G, Parri M, Innocenti S, et al. β-adrenoceptors are upregulated in human melanoma and their activation releases pro-tumorigenic cytokines and metalloproteases in melanoma cell lines. Lab Invest. 2013;93:279–90.
pubmed: 23318885
Yang EV, Kim S, Donovan EL, Chen M, Gross AC, Webster Marketon JI, et al. Norepinephrine upregulates VEGF, IL-8, and IL-6 expression in human melanoma tumor cell lines: implications for stress-related enhancement of tumor progression. Brain Behav Immun. 2009;23:267–75.
pubmed: 18996182
Pérez-Sayáns M, Somoza-Martín JM, Barros-Angueira F, Diz PG, Gándara Rey JM, García-García A. Beta-adrenergic receptors in cancer: therapeutic implications. Oncol Res. 2010;19:45–54.
pubmed: 21141740
Lamkin DM, Sloan EK, Patel AJ, Chiang BS, Pimentel MA, Ma JCY, et al. Chronic stress enhances progression of acute lymphoblastic leukemia via β-adrenergic signaling. Brain Behav Immun. 2012;26:635–41.
pubmed: 22306453
pmcid: 3322262
Chisholm KM, Chang KW, Truong MT, Kwok S, West RB, Heerema-McKenney AE. β-Adrenergic receptor expression in vascular tumors. Mod Pathol. 2012;25:1446–51.
pubmed: 22743651
Perrone MG, Notarnicola M, Caruso MG, Tutino V, Scilimati A. Upregulation of β3-Adrenergic Receptor mRNA in Human Colon Cancer: A Preliminary Study. Oncology. 2008;75:224–9.
pubmed: 18852493
Rains SL, Amaya CN, Bryan BA. Beta-adrenergic receptors are expressed across diverse cancers. Oncoscience. 2017;4:95–105.
pubmed: 28966942
pmcid: 5616202
Dal Monte M, Casini G, Filippi L, Nicchia GP, Svelto M, Bagnoli P. Functional involvement of β3-adrenergic receptors in melanoma growth and vascularization. J Mol Med. 2013;91:1407–19.
pubmed: 23907236
Calvani M, Pelon F, Comito G, Taddei ML, Moretti S, Innocenti S, et al. Norepinephrine promotes tumor microenvironment reactivity through β3-adrenoreceptors during melanoma progression. Oncotarget. 2014;6:4615–32.
pmcid: 4467103
Pasquier E, Street J, Pouchy C, Carre M, Gifford AJ, Murray J, et al. β-blockers increase response to chemotherapy via direct antitumour and anti-angiogenic mechanisms in neuroblastoma. Br J Cancer. 2013;108:2485–94.
pubmed: 23695022
pmcid: 3694229
Wolter JK, Wolter NE, Blanch A, Partridge T, Cheng L, Morgenstern DA, et al. Anti-tumor activity of the beta-adrenergic receptor antagonist propranolol in neuroblastoma. Oncotarget. 2013;5:161–72.
pmcid: 3960198
Strub GM, Maceyka M, Hait NC, Milstien S, Spiegel S. Extracellular and intracellular actions of sphingosine-1-phosphate. Adv Exp Med Biol. 2010;688:141–55.
pubmed: 20919652
pmcid: 2951632
Pyne NJ, Pyne S. Sphingosine 1-phosphate and cancer. Nat Rev Cancer. 2010;10:489–503.
pubmed: 20555359
Weigert A, Schiffmann S, Sekar D, Ley S, Menrad H, Werno C, et al. Sphingosine kinase 2 deficient tumor xenografts show impaired growth and fail to polarize macrophages towards an anti-inflammatory phenotype. Int J Cancer. 2009;125:2114–21.
pubmed: 19618460
Wallington-Beddoe CT, Powell JA, Tong D, Pitson SM, Bradstock KF, Bendall LJ. Sphingosine kinase 2 promotes acute lymphoblastic leukemia by enhancing MYC expression. Cancer Res. 2014;74:2803–15.
pubmed: 24686171
Chumanevich AA, Poudyal D, Cui X, Davis T, Wood PA, Smith CD, et al. Suppression of colitis-driven colon cancer in mice by a novel small molecule inhibitor of sphingosine kinase. Carcinogenesis. 2010;31:1787–93.
pubmed: 20688834
pmcid: 2981458
Li M-H, Hla T, Ferrer F. Sphingolipid modulation of angiogenic factor expression in neuroblastoma. Cancer Prev Res Philos Pa. 2011;4:1325–32.
Bossard F, Silantieff É, Lavazais-Blancou E, Robay A, Sagan C, Rozec B, et al. β1, β2, and β3 Adrenoceptors and Na+/H+ exchanger regulatory factor 1 expression in human bronchi and their modifications in cystic fibrosis. Am J Respir Cell Mol Biol. 2011;44:91–8.
pubmed: 20203292
Li M-H, Hla T, Ferrer F. FTY720 Inhibits tumor growth and enhances the tumor-suppressive effect of topotecan in neuroblastoma by interfering with the sphingolipid signaling pathway. Pediatr Blood Cancer. 2013;60. https://doi.org/10.1002/pbc.24564 .
Cannavo A, Rengo G, Liccardo D, Pun A, Gao E, George AJ, et al. β1-Blockade prevents post-ischemic myocardial decompensation via sphingosine-1 phosphate signaling. J Am Coll Cardiol. 2017;70:182–92.
pubmed: 28683966
pmcid: 5527977
Ross RA, Spengler BA, Domenech C, Porubcin M, Rettig WJ, Biedler JL. Human neuroblastoma I-type cells are malignant neural crest stem cells. Cell Growth Differ. 1995;6:449.
pubmed: 7794812
Walton JD, Kattan DR, Thomas SK, Spengler BA, Guo H-F, Biedler JL, et al. Characteristics of stem cells from human neuroblastoma cell lines and in tumors. Neoplasia N Y N. 2004;6:838–45.
Reynolds CP, Matthay KK, Villablanca JG, Maurer BJ. Retinoid therapy of high-risk neuroblastoma. Cancer Lett. 2003;197:185–92.
pubmed: 12880980
Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D, et al. Long-Term Results for Children With High-Risk Neuroblastoma Treated on a Randomized Trial of Myeloablative Therapy Followed by 13-cis-Retinoic Acid: A Children’s Oncology Group Study. J Clin Oncol. 2009;27:1007–13.
pubmed: 19171716
pmcid: 2738615
Mora J, Cheung N-KV, Juan G, Illei P, Cheung I, Akram M, et al. Neuroblastic and Schwannian stromal cells of neuroblastoma are derived from a tumoral progenitor cell. Cancer Res. 2001;61:6892–8.
pubmed: 11559566
Buhagiar A, Ayers D. Chemoresistance, cancer stem cells, and miRNA influences: The Case for Neuroblastoma. Anal Cell Pathol Amst. 2015;2015. https://doi.org/10.1155/2015/150634 .
Shimada H, Ambros IM, Dehnler LP, Hata J, Joshi VV, Roald B, et al. The International Neuroblastoma Pathology Classification (The Shimada system). Cancer. 1999;86:364–72.
pubmed: 10421273
Pinto NR, Applebaum MA, Volchenboum SL, Matthay KK, London WB, Ambros PF, et al. Advances in risk classification and treatment strategies for neuroblastoma. J Clin Oncol. 2015;33:3008–17.
pubmed: 26304901
pmcid: 4567703
Huang P, Kishida S, Cao D, Murakami-Tonami Y, Mu P, Nakaguro M, et al. The neuronal differentiation factor neuroD1 downregulates the neuronal repellent factor slit2 expression and promotes cell motility and tumor formation of neuroblastoma. Cancer Res. 2011;71:2938–48.
pubmed: 21349947
Takenobu H, Shimozato O, Nakamura T, Ochiai H, Yamaguchi Y, Ohira M, et al. CD133 suppresses neuroblastoma cell differentiation via signal pathway modification. Oncogene. 2011;30:97–105.
pubmed: 20818439
Tong Q-S, Zheng L-D, Tang S-T, Ruan Q-L, Liu Y, Li S-W, et al. Expression and clinical significance of stem cell marker CD133 in human neuroblastoma. World J Pedia. 2008;4:58–62.
Hansford LM, McKee AE, Zhang L, George RE, Gerstle JT, Thorner PS, et al. Neuroblastoma cells isolated from bone marrow metastases contain a naturally enriched tumor-initiating cell. Cancer Res. 2007;67:11234–43.
pubmed: 18056449
Voigt A, Häfer R, Gruhn B, Zintl F. Expression of CD34 and other haematopoietic antigens on neuroblastoma cells: consequences for autologous bone marrow and peripheral blood stem cell transplantation. J Neuroimmunol. 1997;78:117–26.
pubmed: 9307235
Häfer R, Voigt A, Gruhn B, Zintl F. Neuroblastoma cells can express the hematopoietic progenitor cell antigen CD34 as detected at surface protein and mRNA level. J Neuroimmunol. 1999;96:201–6.
pubmed: 10337918
Choi HS, Koh SH, Park ES, Shin HY, Ahn HS. CNS recurrence following CD34+ peripheral blood stem cell transplantation in stage 4 neuroblastoma. Pedia Blood Cancer. 2005;45:68–71.
Zhang W, Mottillo EP, Zhao J, Gartung A, VanHecke GC, Lee J-F, et al. Adipocyte Lipolysis-stimulated Interleukin-6 Production Requires Sphingosine Kinase 1 Activity. J Biol Chem. 2014;289:32178–85.
pubmed: 25253697
pmcid: 4231693
Du W, Takuwa N, Yoshioka K, Okamoto Y, Gonda K, Sugihara K et al. S1P2, the G protein–coupled receptor for sphingosine-1-phosphate, negatively regulates tumor angiogenesis and tumor growth in vivo in mice. Cancer Res 2010; 0008-5472.CAN-09-2722.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C
pubmed: 18546601
Bruno G, Cencetti F, Bernacchioni C, Donati C, Blankenbach KV, Thomas D, et al. Bradykinin mediates myogenic differentiation in murine myoblasts through the involvement of SK1/Spns2/S1P2 axis. Cell Signal. 2018;45:110–21.
pubmed: 29408301
Cencetti F, Bernacchioni C, Nincheri P, Donati C, Bruni P. Transforming growth factor-β1 induces transdifferentiation of myoblasts into myofibroblasts via up-regulation of sphingosine kinase-1/S1P3 axis. Mol Biol Cell. 2010;21:1111–24.
pubmed: 20089836
pmcid: 2836962