The antidepressants maprotiline and fluoxetine have potent selective antiproliferative effects against Burkitt lymphoma independently of the norepinephrine and serotonin transporters

References

• Owens MJ, Morgan WN, Plott SJ, Nemeroff CB. Neurotransmitter receptor and transporter binding profile of antidepressants and their metabolites. J Pharmacol Exp Ther 1997;283:1305–1322.
   PubMed Web of Science ®Google Scholar
• Blakely RD, Ramamoorthy S, Schroeter S, et al Regulated phosphorylation and trafficking of antidepressant-sensitive serotonin transporter proteins. Biol Psychiatry 1998;44:169–178.
   PubMed Web of Science ®Google Scholar
• Tatsumi M, Groshan K, Blakely RD, Richelson E. Pharmacological profile of antidepressants and related compounds at human monoamine transporters. Eur J Pharmacol 1997;340:249–258.
   PubMed Web of Science ®Google Scholar
• Wade PR, Westfall JA. Ultrastructure of enterochromaffin cells and associated neural and vascular elements in the mouse duodenum. Cell Tissue Res 1985;241:557–563.
   PubMed Web of Science ®Google Scholar
• Gershon MD. Plasticity in serotonin control mechanisms in the gut. Curr Opin Pharmacol 2003;3:600–607.
   PubMed Web of Science ®Google Scholar
• Rudnick G. Active transport of 5-hydroxytryptamine by plasma membrane vesicles isolated from human blood platelets. J Biol Chem 1977;252:2170–2174.
   PubMed Web of Science ®Google Scholar
• Bryan-Lluka LJ, Westwood NN, O'Donnell SR. Vascular uptake of catecholamines in perfused lungs of the rat occurs by the same process as Uptake1 in noradrenergic neurones. Naunyn Schmiedebergs Arch Pharmacol 1992;345:319–326.
   PubMed Web of Science ®Google Scholar
• Ramamoorthy S, Prasad PD, Kulanthaivel P, Leibach FH, Blakely RD, Ganapathy V. Expression of a cocaine-sensitive norepinephrine transporter in the human placental syncytiotrophoblast. Biochemistry 1993;32:1346–1353.
   PubMed Web of Science ®Google Scholar
• Cleary S, Brouwers FM, Eisenhofer G, et al Expression of the noradrenaline transporter and phenylethanolamine N-methyltransferase in normal human adrenal gland and phaeochromocytoma. Cell Tissue Res 2005;322:443–453.
   PubMed Web of Science ®Google Scholar
• Meredith EJ, Holder MJ, Chamba A, et al The serotonin transporter (SLC6A4) is present in B-cell clones of diverse malignant origin: probing a potential antitumor target for psychotropics. FASEB J 2005;19:1187–1189.
   PubMed Web of Science ®Google Scholar
• Mairs RJ, Livingstone A, Gaze MN, Wheldon TE, Barrett A. Prediction of accumulation of 131I-labelled meta-iodobenzylguanidine in neuroblastoma cell lines by means of reverse transcription and polymerase chain reaction. Br J Cancer 1994;70:97–101.
   PubMed Web of Science ®Google Scholar
• Streich S, Bruss M, Bonisch H. Expression of the extraneuronal monoamine transporter (uptake2) in human glioma cells. Naunyn Schmiedebergs Arch Pharmacol 1996;353:328–333.
   PubMed Web of Science ®Google Scholar
• Binderup T, Knigge U, Mellon Mogensen A, Palnaes Hansen C, Kjaer A. Quantitative gene expression of somatostatin receptors and noradrenaline transporter underlying scintigraphic results in patients with neuroendocrine tumors. Neuroendocrinology 2008;87:223–232.
   PubMed Web of Science ®Google Scholar
• Huynh TT, Pacak K, Brouwers FM, et al Different expression of catecholamine transporters in phaeochromocytomas from patients with von Hippel-Lindau syndrome and multiple endocrine neoplasia type 2. Eur J Endocrinol 2005;153:551–563.
   PubMed Web of Science ®Google Scholar
• Arimochi H, Morita K. Characterization of cytotoxic actions of tricyclic antidepressants on human HT29 colon carcinoma cells. Eur J Pharmacol 2006;541:17–23.
   PubMed Web of Science ®Google Scholar
• Xia Z, Bergstrand A, DePierre JW, Nassberger L. The antidepressants imipramine, clomipramine, and citalopram induce apoptosis in human acute myeloid leukemia HL-60 cells via caspase-3 activation. J Biochem Mol Toxicol 1999;13:338–347.
   PubMed Web of Science ®Google Scholar
• Xia Z, DePierre JW, Nassberger L. Modulation of apoptosis induced by tricyclic antidepressants in human peripheral lymphocytes. J Biochem Mol Toxicol 1998;12:115–123.
   PubMed Web of Science ®Google Scholar
• Serafeim A, Grafton G, Chamba A, et al 5-Hydroxytryptamine drives apoptosis in biopsylike Burkitt lymphoma cells: reversal by selective serotonin reuptake inhibitors. Blood 2002;99:2545–2553.
   PubMed Web of Science ®Google Scholar
• Serafeim A, Holder MJ, Grafton G, et al Selective serotonin reuptake inhibitors directly signal for apoptosis in biopsy-like Burkitt lymphoma cells. Blood 2003;101:3212–3219.
   PubMed Web of Science ®Google Scholar
• Stepulak A, Rzeski W, Sifringer M, et al Fluoxetine inhibits the extracellular signal regulated kinase pathway and suppresses growth of cancer cells. Cancer Biol Ther 2008;7:1685–1693.
   PubMed Web of Science ®Google Scholar
• Bengel D, Isaacs KR, Heils A, Lesch KP, Murphy DL. The appetite suppressant d-fenfluramine induces apoptosis in human serotonergic cells. Neuroreport 1998;9:2989–2993.
   PubMed Web of Science ®Google Scholar
• Schmidt CJ, Taylor VL. Direct central effects of acute methylenedioxymethamphetamine on serotonergic neurons. Eur J Pharmacol 1988;156:121–131.
   PubMed Web of Science ®Google Scholar
• Azmitia EC, Murphy RB, Whitaker-Azmitia PM. MDMA (ecstasy) effects on cultured serotonergic neurons: evidence for Ca2(+)-dependent toxicity linked to release. Brain Res 1990;510:97–103.
   PubMed Web of Science ®Google Scholar
• Schuster C, Fernbach N, Rix U, et al Selective serotonin reuptake inhibitors – a new modality for the treatment of lymphoma/leukaemia? Biochem Pharmacol 2007;74:1424–1435.
   PubMed Web of Science ®Google Scholar
• Gordon J, Barnes N, Meredith E, Drayson M. In response to ‘Selective serotonin reuptake inhibitors – a new modality for the treatment of lymphoma/leukaemia?’ by C. Schuster, et al. [Biochem Pharmacol 74 (9) 2007 1424–1435]. Biochem Pharmacol 2008;75:e1–3; author reply e4–5.
   PubMedGoogle Scholar
• Chou CT, He S, Jan CR. Paroxetine-induced apoptosis in human osteosarcoma cells: activation of p38 MAP kinase and caspase-3 pathways without involvement of [Ca(2+)](i) elevation. Toxicol Appl Pharmacol 2007;218:265–273.
   PubMed Web of Science ®Google Scholar
• Karlsson H, Gu Y, DePierre J, Nassberger L. Induction of apoptosis in proliferating lymphocytes by tricyclic antidepressants. Apoptosis 1998;3:255–260.
   PubMed Web of Science ®Google Scholar
• Levkovitz Y, Gil-Ad I, Zeldich E, Dayag M, Weizman A. Differential induction of apoptosis by antidepressants in glioma and neuroblastoma cell lines: evidence for p-c-Jun, cytochrome c, and caspase-3 involvement. J Mol Neurosci 2005;27:29–42.
   PubMed Web of Science ®Google Scholar
• Reddy KK, Lefkove B, Chen LB, et al The antidepressant sertraline downregulates Akt and has activity against melanoma cells. Pigment Cell Melanoma Res 2008;21:451–456.
   PubMedGoogle Scholar
• Xia Z, Lundgren B, Bergstrand A, DePierre JW, Nassberger L. Changes in the generation of reactive oxygen species and in mitochondrial membrane potential during apoptosis induced by the antidepressants imipramine, clomipramine, and citalopram and the effects on these changes by Bcl-2 and Bcl-X(L). Biochem Pharmacol 1999;57:1199–1208.
   PubMed Web of Science ®Google Scholar
• Krishnan A, Hariharan R, Nair SA, Pillai MR. Fluoxetine mediates G0/G1 arrest by inducing functional inhibition of cyclin dependent kinase subunit (CKS)1. Biochem Pharmacol 2008;75:1924–1934.
   PubMed Web of Science ®Google Scholar
• Hanxian Huang M. Burkitt lymphoma. Emedicinecom, 2005. Available at: http://emedicine.medscape.com/hematology.
   Google Scholar
• Harris NL, Horning SJ. Burkitt's lymphoma – the message from microarrays. N Engl J Med 2006;354:2495–2498.
   PubMed Web of Science ®Google Scholar
• Burkitt D, O'Conor GT. Malignant lymphoma in African children. I. A clinical syndrome. Cancer 1961;14:258–269.
   PubMed Web of Science ®Google Scholar
• Spina M, Tirelli U, Zagonel V, et al Burkitt's lymphoma in adults with and without human immunodeficiency virus infection: a single-institution clinicopathologic study of 75 patients. Cancer 1998;82:766–774.
   PubMed Web of Science ®Google Scholar
• Grogg KL, Miller RF, Dogan A. HIV infection and lymphoma. J Clin Pathol 2007;60:1365–1372.
   PubMed Web of Science ®Google Scholar
• Biggar RJ, Curtis RE, Cote TR, Rabkin CS, Melbye M. Risk of other cancers following Kaposi's sarcoma: relation to acquired immunodeficiency syndrome. Am J Epidemiol 1994;139:362–368.
   PubMed Web of Science ®Google Scholar
• Rabkin CS. Epidemiology of AIDS-related malignancies. Curr Opin Oncol 1994;6:492–496.
   PubMedGoogle Scholar
• Tate CG, Haase J, Baker C, et al Comparison of seven different heterologous protein expression systems for the production of the serotonin transporter. Biochim Biophys Acta 2003;1610:141–153.
   PubMed Web of Science ®Google Scholar
• Lazar A, Reuveny S, Minai M, Traub A, Mizrahi A. Interferon production by a human lymphoblastoid cell line (DG-75) free of the Epstein-Barr genome. Antimicrob Agents Chemother 1981;20:151–154.
   PubMed Web of Science ®Google Scholar
• Ben-Bassat H, Goldblum N, Mitrani S, et al Establishment in continuous culture of a new type of lymphocyte from a ‘Burkitt like’ malignant lymphoma (line D.G.- 75). Int J Cancer 1977;19:27–33.
   PubMed Web of Science ®Google Scholar
• Baker MP, Eliopoulos AG, Young LS, Armitage RJ, Gregory CD, Gordon J. Prolonged phenotypic, functional, and molecular change in group I Burkitt lymphoma cells on short-term exposure to CD40 ligand. Blood 1998;92:2830–2843.
   PubMed Web of Science ®Google Scholar
• Gregory CD, Rowe M, Rickinson AB. Different Epstein-Barr virus-B cell interactions in phenotypically distinct clones of a Burkitt's lymphoma cell line. J Gen Virol 1990;71:1481–1495.
   PubMed Web of Science ®Google Scholar
• Klein E, Klein G, Nadkarni JS, Nadkarni JJ, Wigzell H, Clifford P. Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines. Cancer Res 1968;28:1300–1310.
   PubMed Web of Science ®Google Scholar
• Menezes J, Leibold W, Klein G, Clements G. Establishment and characterization of an Epstein-Barr virus (EBC)-negative lymphoblastoid B cell line (BJA-B) from an exceptional, EBV-genome-negative African Burkitt's lymphoma. Biomedicine 1975;22:276–284.
   PubMedGoogle Scholar
• Gazdar AF, Oie HK, Kirsch IR, Hollis GF. Establishment and characterization of a human plasma cell myeloma culture having a rearranged cellular myc proto-oncogene. Blood 1986;67:1542–1549.
   PubMed Web of Science ®Google Scholar
• Foley GE, Lazarus H, Farber S, Uzman BG, Boone BA, McCarthy RE. Continuous culture of human lymphoblasts from peripheral blood of a child with acute leukemia. Cancer 1965;18:522–529.
   PubMed Web of Science ®Google Scholar
• Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS. Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 1978;38:3751–3757.
   PubMed Web of Science ®Google Scholar
• Siciliano MJ, Barker PE, Cailleau R. Mutually exclusive genetic signatures of human breast tumor cell lines with a common chromosomal marker. Cancer Res 1979;39:919–922.
   PubMed Web of Science ®Google Scholar
• Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992;52:1399–1405.
   PubMed Web of Science ®Google Scholar
• Brandes LJ, Hermonat MW. Receptor status and subsequent sensitivity of subclones of MCF-7 human breast cancer cells surviving exposure to diethylstilbestrol. Cancer Res 1983;43:2831–2835.
   PubMed Web of Science ®Google Scholar
• Holder MJ, Barnes NM, Gregory CD, Gordon J. Lymphoma cells protected from apoptosis by dysregulated bcl-2 continue to bind annexin V in response to B-cell receptor engagement: a cautionary tale. Leuk Res 2006;30:77–80.
   PubMed Web of Science ®Google Scholar
• Qoronfleh MW, Benton B, Ignacio R, Kaboord B. Selective enrichment of membrane proteins by partition phase separation for proteomic studies. J Biomed Biotechnol 2003;2003:249–255.
   PubMedGoogle Scholar
• Xia Z, Ying G, Hansson AL, et al Antidepressant-induced lipidosis with special reference to tricyclic compounds. Prog Neurobiol 2000;60:501–512.
   PubMed Web of Science ®Google Scholar
• Brimmell M, Mendiola R, Mangion J, Packham G. BAX frameshift mutations in cell lines derived from human haemopoietic malignancies are associated with resistance to apoptosis and microsatellite instability. Oncogene 1998;16:1803–1812.
   PubMed Web of Science ®Google Scholar
• Qian Y, Melikian HE, Rye DB, Levey AI, Blakely RD. Identification and characterization of antidepressant-sensitive serotonin transporter proteins using site-specific antibodies. J Neurosci 1995;15:1261–1274.
   PubMed Web of Science ®Google Scholar
• Tejani-Butt SM, Brunswick DJ, Frazer A. [3H]nisoxetine: a new radioligand for norepinephrine uptake sites in brain. Eur J Pharmacol 1990;191:239–243.
   PubMed Web of Science ®Google Scholar
• Wong DT, Bymaster FP. Effect of nisoxetine on uptake of catecholamines in synaptosomes isolated from discrete regions of rat brain. Biochem Pharmacol 1976;25:1979–1983.
   PubMed Web of Science ®Google Scholar
• Richelson E, Nelson A. Antagonism by antidepressants of neurotransmitter receptors of normal human brain in vitro. J Pharmacol Exp Ther 1984;230:94–102.
   PubMed Web of Science ®Google Scholar
• Wong EHF, Sonders MS, Amara SG, et al Reboxetine: a pharmacologically potent, selective, and specific norepinephrine reuptake inhibitor. Biol Psychiatry 2000;47:818–829.
   PubMed Web of Science ®Google Scholar
• Ferguson J, Hill H. The pharmacokinetics of fluoxetine in elderly volunteers ages 65–85. Eur Neuropsychopharmacol 2003;13:S181.
   Web of Science ®Google Scholar
• Watanabe S, Yokoyama S, Kubo S, Iwai H, Kuyama C. Relationship between blood concentrations and clinical effects of a new antidepressant ‘maprotiline’. Folia Psychiatr Neurol Jpn 1980;34:147–156.
   PubMedGoogle Scholar
• Borys DJ, Setzer SC, Ling LJ, Reisdorf JJ, Day LC, Krenzelok EP. Acute fluoxetine overdose: a report of 234 cases. Am J Emerg Med 1992;10:115–120.
   PubMed Web of Science ®Google Scholar
• Borys DJ, Setzer SC, Ling LJ, Reisdorf JJ, Day LC, Krenzelok EP. The effects of fluoxetine in the overdose patient. J Toxicol Clin Toxicol 1990;28:331–340.
   PubMed Web of Science ®Google Scholar
• Sabbioni C, Bugamelli F, Varani G, et al A rapid HPLC-DAD method for the analysis of fluoxetine and norfluoxetine in plasma from overdose patients. J Pharm Biomed Anal 2004;36:351–356.
   PubMed Web of Science ®Google Scholar