The opioid growth factor-opioid growth factor receptor axis: Homeostatic regulator of cell proliferation and its implications for health and disease

Biochemical Pharmacology

Volumn 84, Issue 6, 2012, Pages 746-755

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

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Cancer; Cyclin dependent inhibitory kinases; DNA synthesis; Dry eye; Enkephalins; Naltrexone; Wound repair

Indexed keywords

ANTINEOPLASTIC AGENT; CASPASE 3; COLLAGEN TYPE 4; DACTINOMYCIN; ENKEPHALIN; FIBRONECTIN; FLUOROURACIL; GEMCITABINE; GROWTH FACTOR RECEPTOR; KARYOPHERIN; LAMININ; NALOXONE; NALTREXONE; OPIATE ANTAGONIST; OPIATE RECEPTOR; OPIOID GROWTH FACTOR; OPIOID GROWTH FACTOR RECEPTOR; PROTEIN P16; PROTEIN P21; PUROMYCIN; UNCLASSIFIED DRUG;

ADVANCED CANCER; ALLERGIC ENCEPHALOMYELITIS; AMINO TERMINAL SEQUENCE; APOPTOSIS; ASTROCYTE; BINDING KINETICS; BIOCHEMICAL COMPOSITION; BIOLOGICAL THERAPY; CARBOXY TERMINAL SEQUENCE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; COLON ADENOCARCINOMA; CORNEA EPITHELIUM; CROHN DISEASE; CYTOPLASM; DISEASE MODEL; DOWN REGULATION; DRUG EFFICACY; DRY EYE; HEAD AND NECK CANCER; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; INSULIN DEPENDENT DIABETES MELLITUS; KERATINOCYTE; KIDNEY CANCER; LIVER CELL CARCINOMA; LOW DRUG DOSE; MULTIPLE SCLEROSIS; NEUROBLASTOMA CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; OVARY CANCER; PANCREAS ADENOCARCINOMA; PANCREAS CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; RNA SYNTHESIS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION; UPREGULATION; WOUND CLOSURE; WOUND HEALING;

EID: 84864953326     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2012.05.018     Document Type: Note

References (80)

1. E.J. Simon, J.M. Hiller, and I. Edelman Stereospecific binding of the potent narcotic analgesic [3H]-etorphine to rat-brain homogenate Proc Natl Acad Sci USA 70 1973 1947 1949
2. L. Terenius Characteristics of the 'receptor' for narcotic analgesics in synaptic plasma membrane from rat brain Acta Pharmacol Toxicol 33 1973 377 384
3. J. Hughes, T.W. Smith, H.W. Kosterlitz, L.H. Fothergill, B.A. Morgan, and H.R. Morris Identification of two pentapeptides from the brain with potent opiate agonist activity Nature 258 1975 577 579
4. H. Akil, S.J. Watson, E. Young, M.E. Lewis, H. Katchaturian, and J.M. Walter Endogenous opioids: biology and function Annu Rev Neurosci 7 1984 223 255
5. R. Simantov Opioid peptide enkephalin: immunohistochemical mapping in rat central nervous system Proc Natl Acad Sci USA 74 1977 2167 2171
6. S.H. Snyder Opiate receptors and beyond: 30 years of neural signaling research Neuropharmacology 47 2004 274 285
7. H.L. Fields, P.C. Emson, D.K. Leigh, R. Gilbert, and L.L. Iversen Multiple opiate receptor sites on primary afferent fibers Nature 284 5754 1980 351 353
8. D. Kew, and D.L. Kilpatrick Widespread organ expression of the rat proenkephalin gene during early postnatal development Mol Endocrinol 4 1990 337 340
9. A.W. Mudge, S.E. Leeman, and G.D. Fischbach Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration Proc Natl Acad Sci USA 77 1979 526 530
10. I.M. Coupar The peristaltic reflex in the rat ileum: evidence for functional mu- and delta-opiate receptors J Pharm Pharmacol 47 1995 643 646
11. L. Terenius, and B. Johansson The opioid systems - panacea and nemesis Biochem Biophys Res Commun 396 2010 140 142
12. I.S. Zagon, and P.J. McLaughlin Endogenous opioid systems regulate cell proliferation in the developing rat brain Brain Res 412 1987 68 72
13. I.S. Zagon, and P.J. McLaughlin Endogenous opioids and the growth regulation of a neural tumor Life Sci 43 1988 1313 1318
14. I.S. Zagon, and P.J. McLaughlin Identification of opioid peptides regulating proliferation of neurons and glia in the developing nervous system Brain Res 542 1991 318 323
15. I.S. Zagon, and P.J. McLaughlin An opioid growth factor regulates the replication of microorganisms Life Sci 50 1992 1179 1187
16. I.S. Zagon, P.J. McLaughlin, S.R. Goodman, and R.E. Rhodes Opioid receptors and endogenous opioids in diverse human and animal cancers J Natl Cancer Inst 79 1987 1059 1065
17. I.S. Zagon, J.P. Smith, and P.J. McLaughlin Human pancreatic cancer cell proliferation in tissue culture is tonically inhibited by opioid growth factor Int J Oncol 14 1999 577 584
18. I.S. Zagon, Y. Wu, and P.J. McLaughlin Opioid growth factor is present in human and mouse gastrointestinal tract and inhibits DNA synthesis Am J Physiol 272 1997 R1094 R1104
19. I.S. Zagon, and P.J. McLaughlin Maternal exposure to opioids and the developing nervous system: laboratory findings I.S. Zagon, T.A. Slotkin, Maternal substance abuse and the developing nervous system 1992 Academic Press New York 241 282
20. 5]-enkephalin, and the zeta opioid receptor in vertebrate cornea Brain Res 671 1995 105 111
21. I.S. Zagon, T.B. Ruth, A.E. Leure-duPree, J.W. Sassani, and P.J. McLaughlin Immunoelectron microscopic localization of the opioid growth factor receptor (OGFr) and OGF in the cornea Brain Res 967 2003 37 47
22. I.S. Zagon, R.B. Ruth, and P.J. McLaughlin Nucleocytoplasmic distribution of opioid growth factor and its receptor in tongue epithelium Anat Rec 282A 2005 24 37
23. I.S. Zagon, R.N. Donahue, and P.J. McLaughlin Opioid growth factor-opioid growth factor receptor axis is a physiological determinant of cell proliferation in diverse human cancers Am J Physiol 297 2009 R1154 R1161
24. 5]-enkephalin, is dependent on clathrin-mediated endocytosis for downregulation of cell proliferation Am J Physiol 299 2010 R774 R785
25. R.N. Donahue, P.J. McLaughlin, and I.S. Zagon Cell proliferation of human ovarian cancer is regulated by the opioid growth factor-opioid growth factor receptor axis Am J Physiol 296 2009 R1716 R1725
26. I.S. Zagon, K.A. Rahn, and P.J. McLaughlin Opioids and migration, chemotaxis, invasion, and adhesion of human cancer cells Neuropeptides 41 2007 441 452
27. I.S. Zagon, and P.J. McLaughlin Opioids and the apoptotic pathway in human cancer cells Neuropeptides 37 2003 79 88
28. I.S. Zagon, and P.J. McLaughlin Opioids and differentiation in human cancer cells Neuropeptides 39 2005 495 505
29. F. Cheng, I.S. Zagon, M.F. Verderame, and P.J. McLaughlin The opioid growth factor (OGF)-OGF receptor axis uses the p16 pathway to inhibit head and neck cancer Cancer Res 67 2007 10511 10518
30. F. Cheng, P.J. McLaughlin, M.F. Verderame, and I.S. Zagon The OGF-OGFr axis utilizes the p21 pathway to restrict progression of human pancreatic cancer Mol Cancer 7 2008 5
31. WAF1/CIP1 pathways to restrict normal cell proliferation Mol Biol Cell 20 2009 319 327
32. I.S. Zagon, and P.J. McLaughlin Endogenous opioids regulate growth of neural tumor cells in culture Brain Res 490 1989 14 25
33. P.J. McLaughlin, I.S. Zagon, and J. Skitzki Human neuroblastoma cell growth in tissue culture is regulated by opioid growth factor Int J Oncol 14 1999 373 380
34. P.J. McLaughlin, R.J. Levin, and I.S. Zagon Regulation of human head and neck squamous cell carcinoma growth in tissue culture by opioid growth factor Int J Oncol 14 1999 991 998
35. I.S. Zagon, R.N. Donahue, R.H. Bonneau, and P.J. McLaughlin. B lymphocyte proliferation is suppressed by the opioid growth factor-opioid growth factor receptor axis: implication for the treatment of autoimmune diseases Immunobiology 216 2011 173 183
36. 5]-enkephalin)-opioid growth factor receptor axis: implication for the treatment of autoimmune diseases Immunobiology 216 2011 579 590
37. I.S. Zagon, M.F. Verderame, and P.J. McLaughlin The biology of the opioid growth factor receptor (OGFr) Brain Res Rev 38 2002 351 376
38. I.S. Zagon, D.M. Gibo, and P.J. McLaughlin Zeta (ζ), a growth-related opioid receptor in developing rat cerebellum: identification and characterization Brain Res 551 1991 28 35
39. I.S. Zagon, D.M. Gibo, and P.J. McLaughlin Ontogeny of zeta (ζ), the opioid growth factor receptor, in the rat brain Brain Res 596 1992 149 156
40. I.S. Zagon, S.R. Goodman, and P.J. McLaughlin Zeta (ζ), the opioid growth factor receptor: identification and characterization of binding subunits Brain Res 605 1993 50 56
41. 5]-enkephalin Brain Res 849 1999 147 154
42. I.S. Zagon, M.F. Verderame, S. Allen, and P.J. McLaughlin Cloning, sequencing, chromosomal location, and function of cDNAs encoding an opioid growth factor receptor (OGFr) in humans Brain Res 856 2000 75 83
43. I.S. Zagon, M.F. Verderame, W.E. Zimmer, and P.J. McLaughlin Molecular characterization and distribution of the opioid growth factor receptor (OGFr) in mouse Mol Brain Res 84 2000 106 114
44. F. Cheng, P.J. McLaughlin, M.F. Verderame, and I.S. Zagon Dependence on nuclear localization signals of the opioid growth factor receptor in the regulation of cell proliferation Exp Biol Med 234 2009 532 541
45. F. Cheng, P.J. McLaughlin, and I.S. Zagon Regulation of cell proliferation by the opioid growth factor is dependent on karyopherin β and Ran for nucleocytoplasmic trafficking Exp Biol Med 235 2010 1093 1101
46. I.S. Zagon, J.W. Sassani, E.R. Kane, and McLaughlin. Homeostasis of ocular surface epithelium in the rat is regulated by opioid growth factor Brain Res 759 1997 92 102
47. I.S. Zagon, J.W. Sassani, and P.J. McLaughlin Adaptation of homeostatic ocular surface epithelium to chronic treatment with the opioid antagonist naltrexone Cornea 25 2006 821 829
48. I.S. Zagon, J.W. Sassani, M.F. Verderame, and P.J. McLaughlin Particle-mediated gene transfer of OGFr cDNA regulates cell proliferation of the corneal epithelium Cornea 24 2005 614 619
49. I.S. Zagon, T. Isayama, and P.J. McLaughlin Opioid growth factor and retinal morphogenesis Adv Neural Sci 2 1995 89 105
50. I.S. Zagon, Y. Wu, and P.J. McLaughlin Opioid growth factor inhibits DNA synthesis in mouse tongue epithelium in a circadian rhythm-dependent manner Am J Physiol Regul Integr Comp Physiol 267 1994 R645 R652
51. I.S. Zagon, J.W. Sassani, and P.J. McLaughlin Reepithelialization of the human cornea is regulated by endogenous opioid Invest Ophthalmol Vis Sci 41 2000 73 81
52. P.J. McLaughlin, S. Kreiner, C.R. Morgan, and I.S. Zagon Prevention and delay in progression of human squamous cell carcinoma of the head and neck in nude mice by stable overexpression of the opioid growth factor receptor Int J Oncol 33 2008 751 757
53. P.J. McLaughlin, M.F. Verderame, J.L. Hankins, and I.S. Zagon Overexpression of the opioid growth factor receptor downregulates cell proliferation of human squamous carcinoma cells of the head and neck Int J Mol Med 17 2007 421 428
54. I.S. Zagon, M.F. Verderame, J.L. Hankins, and P.J. McLaughlin Overexpression of the opioid growth factor receptor potentiates growth inhibition in human pancreatic cancer cells Int J Oncol 30 2007 775 783
55. R.N. Donahue, P.J. McLaughlin, and I.S. Zagon Overexpression of the opioid growth factor receptor (OGFr) in human ovarian cancer cells downregulates cell proliferation in vitro and inhibits tumorigenesis in mice J Cancer Ther 4 2011 579 594
56. R.N. Donahue, P.J. McLaughlin, and I.S. Zagon Under-expression of the opioid growth factor receptor promotes progression of human ovarian cancer Exp Biol Med 237 2012 167 177
57. R. Martin Opioid antagonists Pharmacol Rev 19 1967 462 521
58. H. Blumberg, and H.B. Dayton Naloxone, naltrexone, and related noroxymorphones Adv Biochem Pscyhopharmacol 8 1973 33 43
59. F. Cheng, P.J. McLaughlin, W.A. Banks, and I.S. Zagon Passive diffusion of naltrexone into human and animal cells and upregulation of cell proliferation Am J Physiol Regul Integr Comp Physiol 297 2009 R844 R852
60. I.S. Zagon, and P.J. McLaughlin Duration of opiate receptor blockade determines tumorigenic response in mice with neuroblastoma: a role for endogenous opioid systems in cancer Life Sci 1984 409 416
61. I.S. Zagon, and P.J. McLaughlin Increased brain size and cellular content in infant rats treated with an opiate antagonist Science 221 1983 1179 1180
62. I.S. Zagon, and P.J. McLaughlin Naltrexone modulates tumor response in mice with neuroblastoma Science 221 1983 671 673
63. R.N. Donahue, P.J. McLaughlin, and I.S. Zagon Low-dose naltrexone targets the opioid growth factor-opioid growth factor receptor pathway to inhibit cell proliferation: mechanistic evidence from a tissue culture model Exp Biol Med 236 2011 1036 1050
64. J.P. Smith, R.L. Conter, S.I. Bingman, H.A. Harvey, D.R. Mauger, and M. Ahmad Treatment of advanced pancreatic cancer with opioid growth factor: Phase 1 Anticancer Drugs 15 2004 203 209
65. J.P. Smith, S.I. Bingaman, D.T. Mauger, H.H. Harvey, L.M. Demers, and I.S. Zagon Opioid growth factor improves clinical benefit and survival in patients with advanced pancreatic cancer Open Access J Clin Trials 2 2010 37 48
66. J. Ziaber, Z. Baj, J. Pasnik, H. Chmielewski, and H. Tchorzewski Increased expression of neutral endopeptidase (NEP) and animopeptidase N (APN) on peripheral blood mononuclear cells in patients with multiple sclerosis Immunol Lett 71 2000 127 129
67. M. Gironi, V. martinelli, E. Brambilla, R. Furlan, A.E. Panerai, and G. Comi Beta-endorphin concentrations in peripheral blood mononuclear cells of patients with multiple sclerosis: effects of treatment with interferon beta Arch Neurol 57 2000 1178 1181
68. J.P. Smith, S.I. Bingaman, F. Ruggiero, D.T. Mauger, A. Mukherjee, and C.O. McGovern Therapy with the opioid antagonist naltrexone promotes mucosal healing in active Crohn's disease: a randomized placebo-controlled trial Dig Dis Sci 56 2011 2088 2097
69. B.A.C. Cree, E. Kornyeyeva, and D.S. Goodin Pilot trial of low dose naltrexone and quality of life in MS Ann Neurol 68 2010 124 125
70. S. Mackey, and J. Younger Fibromyalgia symptoms are reduced by low-dose naltrexone: a pilot study Pain Med 10 2009 663 672
71. I.S. Zagon, K.A. Rahn, A.P. Turel, and P.J. McLaughlin Endogenous opioids regulate expression of experimental autoimmune encephalomyelitis: a new paradigm for the treatment of multiple sclerosis Exp Biol Med 234 2009 1383 1392
72. K.A. Rahn, P.J. McLaughlin, and I.S. Zagon Prevention and diminished expression of experimental autoimmune encephalomyelitis by low dose naltrexone (LDN) or opioid growth factor (OGF) for an extended period: therapeutic implications for multiple sclerosis Brain Res 1381 2011 243 253
73. K. Timmers, N.R. Voyles, C. Zalenski, S. Wilkins, and L. Recant Altered β-endorphin, met- and leu-enkephalins, and enkephalin-containing peptides in pancreas and pituitary of genetically obese diabetic (db/db) mice during development of diabetic syndrome Diabetes 35 1986 1143 1151
74. I.S. Zagon, J.B. Jenkins, J.W. Sassani, J.D. Wylie, T.B. Ruth, and J.L. Fry Naltrexone, an opioid antagonist, facilitates re-epithelialization of the cornea in diabetic rat Diabetes 51 2002 3055 3062
75. M.S. Klocek, J.W. Sassani, P.J. McLaughlin, and I.S. Zagon Topically applied naltrexone restores corneal reepithelialization in diabetic rats J Ocul Pharmacol Ther 23 2007 89 102
76. I.S. Zagon, M.S. Klocek, J.W. Sassani, and P.J. McLaughlin Dry eye reversal and corneal sensation restoration with topical naltrexone in diabetes mellitus Arch Ophthalmol 127 2009 1468 1473
77. P.J. McLaughlin, C.A. Pothering, J.A. Immonen, and I.S. Zagon Topical treatment with the opioid antagonist naltrexone facilitates closure of full-thickness wounds in diabetic rats Exp Biol Med 236 2011 1122 1132
78. F. Fallucca, G. Tonnarini, N. Di Biase, M. D'Alessandro, and M. Negri Plasma met-enkephalin levels in diabetic patients: Influence of autonomic neuropathy Metabolism 45 1996 1065 1068
79. M. Negri, G. Tonnarini, M. D'Alessandro, and F. Fallucca Plasma met-enkephalin in type 1 diabetes Metabolism 41 1992 460 461
80. G.M. Pieper, H. Mizoguchi, M. Ohsawa, J. Kamel, H. Nagase, and L.F. Tseng Decreased opioid-induced antinociception but unaltered G-protein activation in the genetic-diabetic NOD mouse Eur J Pharmacol 401 2000 375 379