L-arginine inhibits apoptosis via a NO-dependent mechanism in Nb2 lymphoma cells

Journal of Cellular Biochemistry

Volumn 77, Issue 4, 2000, Pages 624-634

  Dodd, Faith ^a   Limoges, Mireille ^a   Boudreau, Robert T M ^a   Rowden, Geoffrey ^a   Murphy, Paul R ^a   Too, Catherine K L ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Apoptosis; Nb2 lymphoma cells; Nitric oxide; Prolactin

Indexed keywords

ARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROLACTIN; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CELL SURVIVAL; DOWN REGULATION; GENE EXPRESSION; GROWTH DISORDER; IMMUNOCOMPETENT CELL; LYMPHOMA CELL LINE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; ARGININE; BLOTTING, WESTERN; CELL DIVISION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM; IN SITU NICK-END LABELING; LIPOPOLYSACCHARIDES; LYMPHOMA; MALE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; PRECIPITIN TESTS; PROLACTIN; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIME FACTORS; TUMOR CELLS, CULTURED; UP-REGULATION;

EID: 0034032466     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(20000615)77:4<624::AID-JCB10>3.0.CO;2-M     Document Type: Article

References (51)

1. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. 1998. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol 160:5729-5734.
2. Brown JF, Tepperman BL. 1997. Ontogeny of nitric oxide synthase activity and endotoxin-mediated damage in the neonatal rat colon. Pediatr Res 41:635-640.
3. Clevenger CV, Russell DH, Appasamy PM, Prystowsky MB. 1990. Regulation of IL-2-driven T-lymphocyte proliferation by prolactin. Proc Natl Acad Sci USA 87:6460-6464.
4. Clevenger CV, Sillman AL, Hanley-Hyde J, Prystowsky MB. 1992. Requirement for prolactin during cell cycle regulated gene expression in cloned T-lymphocytes. Endocrinology 130:3216-3222.
5. Clevenger CV, Thickman K, Ngo W, Chang WP, Takayama S, Reed JC. 1997. Role of Bag-1 in the survival and proliferation of the cytokine-dependent lymphocyte lines, Ba/F3 and Nb2. Mol Endocrinol 11:608-618.
6. Clevenger CV, Freir DO, Kline JB. 1998. Prolactin receptor signal transduction in cells of the immune system. J Endocrinol 157:187-197.
7. Cruz MT, Carmo A, Carvalho AP, Lopes MC. 1998. Calcium-dependent nitric oxide synthase activity in rat thymocytes. Biochem Biophys Res Commun 248:98-103.
8. Cymeryng CB, Dada LA, Colonna C, Mendez CF, Podesta EJ. 1999. Effects of L-arginine in rat adrenal cells: involvement of nitric oxide synthase. Endocrinology 140: 2962-2967.
9. DiMattia GE, Gellersen B, Bohnet HG, Friesen HG. 1988. A human B-lymphoblastoid cell line produces prolactin. Endocrinology 122:2508-2517.
10. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. 1999. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399:601-605.
11. Duhe RJ, Evans GA, Erwin RA, Kirken RA, Cox GW, Farrar WL. 1998. Nitric oxide and thiol redox regulation of Janus kinase activity. Proc Natl Acad Sci USA 95: 126-131.
12. Fehsel K, Kroncke KD, Meyer KL, Huber H, Wahn V, Kolb-Bachofen V. 1995. Nitric oxide induces apoptosis in mouse thymocytes. J Immunol 155:2858-2865.
13. Feng Y, Venema VJ, Venema RC, Tsai N, Caldwell RB. 1999. VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun 256:192-197.
14. Fleming WH, Pettigrew NM, Matusik RJ, Friesen HG. 1982. Thymic origin of the prolactin-dependent Nb2 lymphoma cell line. Cancer Res 42:3138-3141.
15. Fleming WH, Murphy PR, Murphy LJ, Hatton TW, Matusik RJ, Friesen HG. 1985. Human growth hormone induces and maintains c-myc gene expression in Nb2 lymphoma cells. Endocrinology 117:2547-2549.
16. Fletcher-Chiappini SE, Comptom MM, La VHA, Day EB, Witorsch RJ. 1993. Glucocorticoid-prolactin interactions in Nb2 lymphoma cells: antiproliferative versus anticytolytic effects. Proc Soc Exp Biol Med 202:345-352.
17. Friesen HG, DiMattia GE, Too CKL. 1991. PNEI review. Lymphoid tumor cells as models for studies of prolactin gene regulation and action. Prog NeuroEndocrinImmunol 4:1-9.
18. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. J Cell Biol 119:493-500.
19. Geller DA, Billiar TR. 1998. Molecular biology of nitric oxide synthases. Cancer Metastasis Rev 17:7-23.
20. Geller DA, Lowenstein CJ, Shapiro RA, Nussler AK, Di SM, Wang SC, Nakayama DK, Simmons RL, Synder SH, Billiar TR. 1993. Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc Natl Acad Sci USA 90:3491-3495.
21. Genaro AM, Hortelano S, Alvarez A, Martinez C, Bosca L. 1995. Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J Clin Invest 95:1884-1890.
22. Goetz RM, Thatte HS, Prabhakar P, Cho MR, Michel T, Golan DE. 1999. Estradiol induces the calcium-dependent translocation of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 96:2788-2793.
23. Gout PW, Horsman DE, Fox K, De Jong G, Ma S, Bruchovsky N. 1994. The rat Nb2 lymphoma: a novel model for tumor progression. Anticancer Res 14:2485-2492.
24. Hooghe R, Merchav S, Gaidano G, Naessens F, Matera L. 1998. A role for growth hormone and prolactin in leukaemia and lymphoma? Cell Mol Life Sci 54:1095-1101.
25. Hosokawa Y, Yang M, Kaneko S, Tanaka M, Nakashima K. 1996. Prolactin induces switching of T-cell receptor gene expression from alpha to gamma in rat Nb2 pre-T lymphoma cells. Biochem Biophys Res Commun 220:958-962.
26. Kim YM, Bombeck CA, Billiar TR. 1999. Nitric oxide as a bifunctional regulator of apoptosis. Circ Res 84:253-256.
27. Knowles RG, Moncada S. 1994. Nitric oxide synthases in mammals. Biochem J 298:249-258.
28. Kroncke KD, Fehsel K, Kolb-Bachofen V. 1997. Nitric oxide: cytotoxicity versus cytoprotection - how, why, when, and where? Nitric Oxide 1:107-120.
29. Krumenacker JS, Buckley DJ, Leff MA, McCormack JT, de Jong G, Gout PW, Reed JC, Miyashita T, Magnuson NS, Buckley AR. 1998. Prolactin-regulated apoptosis of Nb2 lymphoma cells: pim-1, bcl-2, and bax expression. Endocrine 9:163-170.
30. Kumar A, Singh SM, Sodhi A. 1997. Effect of prolactin on nitric oxide and interleukin-1 production of murine peritoneal macrophages: role of Ca2+ and protein kinase C. Int J Immunopharmacol 19:129-133.
31. LaVoie HA, Witorsch RJ. 1995. Investigation of intracellular signals mediating the anti-apoptotic action of prolactin in Nb2 lymphoma cells. Proc Soc Exp Biol Med 209: 257-269.
32. Leff MA, Buckley DJ, Krumenacker JS, Reed JC, Miyashita T, Buckley AR. 1996. Rapid modulation of the apoptosis regulatory genes, bcl-2 and bax by prolactin in rat Nb2 lymphoma cells. Endocrinology 137:5456-5462.
33. Mannick JB, Asano K, Izumi K, Kieff E, Stamier JS. 1994. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 79: 1137-1146.
34. Maragos CM, Wang JM, Hrabie JA, Oppenheim JJ, Keefer LK. 1993. Nitric oxide/nucleophile complexes inhibit the in vitro proliferation of A375 melanoma cells via nitric oxide release. Cancer Res 53:564-568.
35. Meli R, Raso GM, Bentivoglio C, Nuzzo I, Galdiero M, Di Carlo R. 1996. Recombinant human prolactin induces protection against Salmonella typhimurium infection in the mouse: role of nitric oxide. Immunopharmacology 34:1-7.
36. Meli R, Raso GM, Gualillo O, Pacilio M, Di Carlo R. 1997. Prolactin modulation of nitric oxide and TNF-alpha production by peripheral neutrophils in rats. Life Sci 61: 1395-1403.
37. Misko TP, Moore WM, Kasten TP, Nickols GA, Corbett JA, Tilton RG, McDaniel ML, Williamson JR, Currie MG. 1993. Selective inhibition of the inducible nitric oxide synthase by aminoguanidine. Eur J Pharmacol 233:119-125.
38. Mohr S, Zech B, Lapetina EG, Brune B. 1997. Inhibition of caspase-3 by S-nitrosation and oxidation caused by nitric oxide. Biochem Biophys Res Commun 238:387-391.
39. Neal KD, Montgomery DW, Truong TM, Yu-Lee L-Y. 1992. Prolactin gene expression in human thymocytes. Mol Cell Endocrinol 87:19-23.
40. Pellegrini I, Lebrun J-J, Ali S, Kelly PA. 1992. Expression of prolactin and its receptor in human lymphoid cells. Mol Endocrinol 6:1023-1031.
41. Prabhakar P, Thatte HS, Goetz RM, Cho MR, Golan DE, Michel T. 1998. Receptor-regulated translocation of endothelial nitric-oxide synthase. J Biol Chem 273:27383-27388.
42. Puissant C, Houdebine L-M. 1990. An improvement of the single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Biotechniques 8:148-149.
43. 2+/calmodulin-dependent isoform in human B and T lymphocytes. Eur J Immunol 26:511-516.
44. Smyth CE, Knee R, Wilkinson M, Murphy PR. 1997. Decline in basic fibroblast growth factor (FGF-2) mRNA expression in female rat hypothalamus at puberty. J Neuroendocrinol 9:151-159.
45. Suschek CV, Krischel V, Bruch-Gerharz D, Berendji D, Krutmann J, Kroncke KD, Kolb-Bachofen V. 1999. Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 upregulation. J Biol Chem 274:6130-6137.
46. + exchange in rat Nb2 node lymphoma cells. Stimulation by 12-0-tetradecanoyl-phorbol-13-acetate. Endocrinology 121:1503-1511.
47. nrb-related mRNA in rat lymphoma cells. Mol Cell Endocrinol 137:187-195.
48. Velkeniers B, Dogusan Z, Naessens F, Hooghe R, Hooghe-Peters EL. 1998. Prolactin, growth hormone and the immune system in humans. Cell Mol Life Sci 54:1102-1108.
49. Witorsch RJ, Day EB, LaVoie HA, Hashemi N, Taylor JK. 1993. Comparison of glucocorticoid-induced effects in prolactin-dependent and autonomous rat Nb2 lymphoma cells. Proc Soc Exp Biol Med 203:454-460.
50. Yoshizumi M, Perrella MA, Burnett JC Jr, Lee ME. 1993. Tumor necrosis factor downregulates an endothelial nitric oxide synthase mRNA by shortening its half-life. Circ Res 73:205-209.
51. Yu-Lee L, Luo G, Moutoussamy S, Finidori J. 1998. Prolactin and growth hormone signal transduction in lymphohaemopoietic cells. Cell Mol Life Sci 54:1067-1075.