Regulation of cell proliferation by the opioid growth factor receptor is dependent on karyopherin β and Ran for nucleocytoplasmic trafficking

Experimental Biology and Medicine

Volumn 235, Issue 9, 2010, Pages 1093-1101

  Cheng, Fan ^a   McLaughlin, Patricia J ^a   Zagon, Ian S ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Cell proliferation; DNA synthesis; Enkephalin; Green fluorescent protein; Karyopherin importin; Nucleocytoplasmic transport; Opioid growth factor; Opioid growth factor receptor; Ran; siRNA

Indexed keywords

BROXURIDINE; ENHANCED GREEN FLUORESCENT PROTEIN; GROWTH FACTOR RECEPTOR; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; HYBRID PROTEIN; KARYOPHERIN ALPHA; KARYOPHERIN ALPHA 1; KARYOPHERIN ALPHA 2; KARYOPHERIN ALPHA 3; KARYOPHERIN ALPHA 4; KARYOPHERIN ALPHA 6; KARYOPHERIN BETA; KARYOPHERIN BETA 1; OPIATE RECEPTOR; OPIOID GROWTH FACTOR RECEPTOR; RAN PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; METHIONINE-ENKEPHALIN RECEPTOR; NUCLEAR LOCALIZATION SIGNAL;

ARTICLE; CANCER CELL CULTURE; CELL LABELING; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; GENETIC TRANSFECTION; HEAD AND NECK CARCINOMA; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LABELING INDEX; NUCLEAR IMPORT; NUCLEOCYTOPLASMIC TRANSPORT; SQUAMOUS CELL CARCINOMA; ACTIVE TRANSPORT; CELL LINE; DRUG EFFECTS; GENETICS; METABOLISM; NUCLEAR LOCALIZATION SIGNAL; PATHOLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; BETA KARYOPHERINS; CARCINOMA, SQUAMOUS CELL; CELL LINE; CELL PROLIFERATION; CYTOPLASM; DOWN-REGULATION; HUMANS; NUCLEAR ENVELOPE; NUCLEAR LOCALIZATION SIGNALS; RECEPTORS, OPIOID; RNA, SMALL INTERFERING;

EID: 77957166100     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2010.010139     Document Type: Article

References (40)

1. Terry LJ, Shows B, Wente SR. Crossing the nuclear envelope: hierarchical regulation of nucelocytoplasmic transport. Science 2007;318:1412-16
2. Chahine MN, Pierce GN. Therapeutic targeting of nuclear protein mport in pathological cell conditions. Pharmacol Rev 2009;61:358-72
3. McLane LM, Corbett AH. Nuclear localization signals and human disease. IUBMB Life 2009;61:697-706
4. Mosammaparast N, Pemberton LF. Karopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol 2004;14:547-56 (Pubitemid 39296617)
5. Wagstaff KM, Jans DA. Importins and beyond: non-conventional nuclear transport mechanisms. Traffic 2009;10:1188-98
6. Yudin D, Fainsilber M. Ran on tracks - cytoplasmic roles for a nuclear regulator. J Cell Sci 2009;122:587-93
7. Peters R. Functionalization of a nanopore: the nuclear pore complex paradigm. Biochem Biophys Acta 2009;1793:1533-9
8. Hughes J, Smith TW, Kosterlitz HW, Fothergill LA, Morgan BA, Morris HR. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 1975;258:577-80
9. Akil H, Watson SJ, Young E, Lewis ME, Khachaturian H, Walker JM. Endogenous opioids: biology and function. Ann Rev Neurosci 1984;7:223-55
10. Leslie FM. Methods used for the study of opioid receptors. Pharmacol Rev 1987;39:197-249
11. Zagon IS, Verderame MF, McLaughlin PJ. The biology of the opioid growth factor receptor (OGFr). Brain Res Rev 2002;38:351-76
12. Zagon IS, Verderame MF, Allen SS, McLaughlin PJ. Cloning, sequencing, chromosomal location, and function of a cDNA encoding the opioid growth factor receptor (OGFr) in humans. Brain Res 2000;856:75-83
13. Cheng F, Zagon IS, Verderame MF, McLaughlin PJ. The OGF-OGFr axis utilizes the p16 pathway to inhibit progression of human squamous cell carcinoma of the head and neck. Cancer Res 2007;67:10511-18
14. Cheng F, McLaughlin PJ, Verderame MF, Zagon IS. The OGF-OGFr axis utilizes the p21 pathway to restrict progression of human pancreatic cancer. Mol Cancer 2008;7:5-17
15. WAF1/CIP1 pathways to restrict normal cell proliferation. Mol Biol Cell 2009;20:319-27
16. Donahue RN, McLaughlin PJ, Zagon IS. Cell proliferation of human ovarian cancer is regulated by the opioid growth factor-opioid growth factor receptor axis. Am J Physiol 2009;296:R1716-25
17. Goldenberg D, Zagon IS, Fedok F, Crist H, McLaughlin PJ. The presence of the opioid growth factor (OGF)-OGF receptor (OGFr) axis in human non-medullary thyroid cancer. Thyroid 2008;18:1165-70
18. 5]-enkephalin, and the zeta opioid receptor in head and neck squamous cell carcinoma. Laryngoscope 1997;107:335-9
19. McLaughlin PJ, Levin RJ, Zagon IS. Regulation of human head and neck squamous cell carcinoma growth in tissue culture by opioid growth factor. Int J Oncol 1999;14:991-8
20. Zagon IS, Ruth TB, McLaughlin PJ. Nucleocytoplasmic distribution of opioid growth factor and its receptor in tongue epithelium. Anat Rec A 2005;282:24-37
21. Zagon IS, Ruth TB, Leure-duPree AE, Sassani JW, McLaughlin PJ. Immunoelectron microscopic localization of the opioid growth factor receptor (OGFr) and OGF in the cornea. Brain Res 2003;967:37-47
22. Cheng F, McLaughlin PJ, Verderame MF, Zagon IS. Dependence on nuclear localization signals of the opioid growth factor receptor in the regulation of cell proliferation. Exp Biol Med 2009;234:532-41
23. Frankel MB, Knoll LJ. The ins and outs of nuclear trafficking: unusual aspects in Apicomplexan parasites. DNA Cell Biol 2009;28:277-84
24. Quensel C, Friedrich B, Sommer T, Hartmann E, Kohler M. In vivo analysis of importin alpha proteins reveals cellular proliferation inhibition and substrate specificity. Mol Cell Biol, 2004;24:10246-55
25. Borlido J, Zecchini V, Mills IG. Nuclear trafficking and functions of endocytic proteins implicated in oncogenesis. Traffic 2009;10:1209-20
26. Kau TR, Way JC, Silver PA. Nuclear transport and cancer: from mechanism to intervention. Nat Rev Cancer 2004;4:106-17
27. Dahl E, Kristiansen G, Gottlob K, Klaman I, Ebner E, Hinzman B, Hermann K, Pilarsky C, Durst M, Klinkhammer-Schalke M, Blaszyk H, Knuechel R, Hartmann A, Rosenthal A, Wild PJ. Molecular profiling of laser-microdissected matched tumor and normal breast tissue identifies karyopherin a2 as a potential novel prognostic marker in breast cancer. Clin Cancer Res 2006;12:3950-60
28. Winnepenninckx V, Lazar V, Michiels S, Dessen P, Stas M, Alonso SR, Avril M-F, Romero PLO, Robert T, Balacescu O, Eggermont AMM, Lenoir G, Sarasin A, Tursz T, van den Oord JJ, Spatz A. Gene expression profiling of primary cutaneous melanoma and clinical outcome. J Natl Cancer Inst 2006;98:472-82
29. Brand K, Page S, Rogler G, Bartsch A, Brandl R, Knueschel R, Page M, Kaltschmidt C, Baeuerle PA, Neumeier D. Activated transcription factor nuclear-kappa B is present in the atherosclerotic lesion. J Clin Invest 1996;97:1715-22
30. Lee CH, Jeon YT, Kim SH, Song YS. NF-kappaB as a potential molecular target for cancer therapy. Biofactors 2007;29:19-35 (Pubitemid 46985299)
31. Kim I-S, Kim D-H, Han S-M, Chin M-U, Nam H-J, Cho H-P, Choi S-Y, Song B-J, Kim E-R, Bae Y-S, Moon Y-H. Truncated form of importin a identified in breast cancer cell inhibits nuclear import of p53. J Biol Chem 2000;275:23139-45
32. Moll UM, Riou G, Levine A. Two distinct mechanisms alters p53 in breast cancer: mutation and nuclear exclusion. Proc Natl Acad Sci USA 1992;89:7262-6
33. Moll UM, LaQuaglia M, Benard J, Riou G. Wild-type p53 protein undergoes cytoplasmic sequestration in undifferentiated neuroblastomas but not in differentiated tumors. Proc Natl Acad Sci USA 1995;92:4407-11
34. Smith JP, Conter RL, Bingaman SI, Harvey HA, Mauger DT, Ahmad M, Demers LM, Stanley WB, McLaughlin PJ, Zagon IS. Treatment of advanced pancreatic cancer with opioid growth factor: phase I. Anti-Cancer Drugs 2004;15:203-9 (Pubitemid 38429411)
35. Smith JP, Bingaman SI, Mauger DT, Harvey HA, Demers LM, Zagon IS. Opioid growth factor (OGF) improves clinical benefit and survival in patients with advanced pancreatic cancer. Open Access J Clin Trials 2010;2:1-12
36. Jaglowski JR, Zagon IS, Stack BC, Verderame MF, Leure-duPree AE, Manning JD, McLaughlin PJ. Opioid growth factor (OGF) enhances tumor growth inhibition and increases the survival of paclitaxel-treated mice with squamous cell carcinoma of the head and neck. Cancer Chemother Pharmacol 2005;56:97-104
37. McLaughlin PJ, Jaglowski JR, Verderame MF, Stack BC, Leure-duPree AE, Zagon IS. Enhanced growth inhibition of squamous cell carcinoma of the head and neck by combination therapy of paclitaxel and opioid growth factor. Int J Oncol 2005;26:809-16
38. Zagon IS, Jaglowski JR, Verderame MF, Smith JP, Leure-duPree AE, McLaughlin PJ. Combination chemotherapy with gemcitabine and biotherapy with opioid growth factor (OGF) enhances the growth inhibition of pancreatic adenocarcinoma. Cancer Chemother Pharmacol 2005;56:510-20
39. McLaughlin PJ, Levin RJ, Zagon IS. Opioid growth factor (OGF) inhibits the progression of human squamous cell carcinoma of the head and neck transplanted into nude mice. Cancer Lett 2003;199:209-17
40. Cheng F, McLaughlin PJ, Banks WA, Zagon IS. Passive diffusion of naltrexone into human and animal cells and upregulation of cell proliferation. Am J Physiol Regul Integr Comp Physiol 2009;297:R844-52