Isolation and characterization of new exon 11-associated N-terminal splice variants of the human mu opioid receptor gene

Journal of Neurochemistry

Volumn 108, Issue 4, 2009, Pages 962-972

  Xu, Jin ^a   Xu, Mingming ^a   Hurd, Yasmin L ^b   Pasternak, Gavril W ^a   Pan, Ying Xian ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

G protein; Morphine; Mu opioid receptor (MOR); Mu opioid receptor 1; Opioid receptor; Splicing

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; MU OPIATE RECEPTOR; OPIATE;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; EXON; GENE ACTIVATION; GENETIC VARIABILITY; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA SPLICING;

ALTERNATIVE SPLICING; ANIMALS; CHO CELLS; CONSERVED SEQUENCE; CRICETINAE; CRICETULUS; DNA; EVOLUTION, MOLECULAR; EXONS; GENE EXPRESSION; HUMANS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, OPIOID, MU; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SPECIES SPECIFICITY;

ANIMALIA; CRICETULUS GRISEUS; MUS; RATTUS;

EID: 58749098046     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05833.x     Document Type: Article

References (64)

1. Abbadie C., Gultekin S. H. Pasternak G. W. (2000a) Immunohistochemical localization of the carboxy terminus of the novel mu opioid receptor splice variant MOR-1C within the human spinal cord. Neuroreport 11, 1953 1957.
2. Abbadie C., Pan Y. X. Pasternak G. W. (2000b) Differential distribution in rat brain of mu opioid receptor carboxy terminal splice variants MOR-1C-like and MOR-1-like immunoreactivity: evidence for region-specific processing. J. Comp. Neurol. 419, 244 256.
3. Abbadie C., Pan Y.-X., Drake C. T. Pasternak G. W. (2000c) Comparative immunhistochemical distributions of carboxy terminus epitopes from the mu opioid receptor splice variants MOR-1D, MOR-1 and MOR-1C in the mouse and rat central nervous systems. Neuroscience 100, 141 153.
4. Abbadie C., Pasternak G. W. Aicher S. A. (2001) Presynaptic localization of the carboxy-terminus epitopes of the mu opioid receptor splice variants MOR-1C and MOR-1D in the superficial laminae of the rat spinal cord. Neuroscience 106, 833 842.
5. Abbadie C., Pan Y. X. Pasternak G. W. (2004) Immunohistochemical study of the expression of exon11-containing mu opioid receptor variants in mouse brain. Neuroscience 127, 419 430.
6. Bare L. A., Mansson E. Yang D. (1994) Expression of two variants of the human μ opioid receptor mRNA in SK-N-SH cells and human brain. FEBS Lett. 354, 213 216.
7. Bender E., Pindon A., Van Oers I., Zhang Y. B., Gommeren W., Verhasselt P., Jurzak M., Leysen J. Luyten W. (2000) Structure of the human serotonin 5-HT4 receptor gene and cloning of a novel 5-HT4 splice variant. J. Neurochem. 74, 478 489.
8. Blondel O., Gastineau M., Dahmoune Y., Langlois M. Fischmeister R. (1998) Cloning, expression, and pharmacology of four human 5-hydroxytryptamine 4 receptor isoforms produced by alternative splicing in the carboxyl terminus. J. Neurochem. 70, 2252 2261.
9. Bolan E. A., Pan Y. X. Pasternak G. W. (2004) Functional analysis of MOR-1 splice variants of the mouse mu opioid receptor gene Oprm. Synapse 51, 11 18.
10. Cadet P., Mantione K. J. Stefano G. B. (2003) Molecular identification and functional expression of mu 3, a novel alternatively spliced variant of the human mu opiate receptor gene. J. Immunol. 170, 5118 5123.
11. Canton H., Emeson R. B., Barker E. L., Backstrom J. R., Lu J. T., Chang M. S. Sanders-Bush E. (1996) Identification, molecular cloning, and distribution of a short variant of the 5-hydroxytryptamine2C receptor produced by alternative splicing. Mol. Pharmacol. 50, 799 807.
12. Chang A., Emmel D. W., Rossi G. C. Pasternak G. W. (1998) Methadone analgesia in morphine-insensitive CXBK mice. Eur. J. Pharmacol. 351, 189 191.
13. Chen Y., Mestek A., Liu J., Hurley J. A. Yu L. (1993) Molecular cloning and functional expression of a μ-opioid receptor from rat brain. Mol. Pharmacol. 44, 8 12.
14. 50) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099 3108.
15. Cherny N., Ripamonti C., Pereira J., Davis C., Fallon M., McQuay H., Mercadante S., Pasternak G. Ventafridda V. (2001) Strategies to manage the adverse effects of oral morphine: an evidence-based report. J. Clin. Oncol. 19, 2542 2554.
16. Choi H. S., Kim C. S., Hwang C. K., Song K. Y., Wang W., Qiu Y., Law P. Y., Wei L. N. Loh H. H. (2006) The opioid ligand binding of human mu-opioid receptor is modulated by novel splice variants of the receptor. Biochem. Biophys. Res. Commun. 343, 1132 1140.
17. Chomczynski P. Sacchi N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156 159.
18. Doyle G. A., Sheng X. R., Lin S. S., Press D. M., Grice D. E., Buono R. J., Ferraro T. N. Berrettini W. H. (2007a) Identification of three mouse micro-opioid receptor (MOR) gene (Oprm1) splice variants containing a newly identified alternatively spliced exon. Gene 388, 135 147.
19. Doyle G. A., Sheng X. R., Lin S. S., Press D. M., Grice D. E., Buono R. J., Ferraro T. N. Berrettini W. H. (2007b) Identification of five mouse mu-opioid receptor (MOR) gene (Oprm1) splice variants containing a newly identified alternatively spliced exon. Gene 395, 98 107.
20. Du Y.-L., Elliot K., Pan Y.-X., Pasternak G. W. Inturrisi C. E. (1997) A splice variant of the mu opioid receptor is present in human SHSY-5Y cells. Soc. Neurosci. 23, 1206.
21. Foley K. M. (1985) Management of cancer pain, in Cancer: Principles and Practice of Oncology (DeVita V. T., Hellman S. Rosenberg S. A., eds pp. 1940 1961. Lippincott, New York.
22. Guest P. C., Salim K., Skynner H. A., George S. E., Bresnick J. N. McAllister G. (2000) Identification and characterization of a truncated variant of the 5-hydroxytryptamine(2A) receptor produced by alternative splicing. Brain Res. 876, 238 244.
23. Hope A. G., Downie D. L., Sutherland L., Lambert J. J., Peters J. A. Burchell B. (1993) Cloning and functional expression of an apparent splice variant of the murine 5-HT3 receptor A subunit. Eur. J. Pharmacol. 245, 187 192.
24. Jasper J. R., Kosaka A., To Z. P., Chang D. J. Eglen R. M. (1997) Cloning, expression and pharmacology of a truncated splice variant of the human 5-HT7 receptor (h5-HT7b). Br. J. Pharmacol. 122, 126 132.
25. Johnson J. M., Castle J., Garrett-Engele P., Kan Z., Loerch P. M., Armour C. D., Santos R., Schadt E. E., Stoughton R. Shoemaker D. D. (2003) Genome-wide survey of human alternative pre-mRNA splicing with exon junction microarrays. Science 302, 2141 2144.
26. Ling G. S. F., MacLeod J. M., Lee S., Lockhart S. H. Pasternak G. W. (1984) Separation of morphine analgesia from physical dependence. Science 226, 462 464.
27. Ling G. S. F., Spiegel K., Lockhart S. H. Pasternak G. W. (1985) Separation of opioid analgesia from respiratory depression: evidence for different receptor mechanisms. J. Pharmacol. Exp. Ther. 232, 149 155.
28. Lord J. A. H., Waterfield A. A., Hughes J. Kosterlitz H. W. (1977) Endogenous opioid peptides: multiple agonists and receptors. Nature 267, 495 499.
29. Martin W. R., Eades C. G., Thompson J. A., Huppler R. E. Gilbert P. E. (1976) The effects of morphine and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197, 517 532.
30. Monsma F. J., McVittie L. D., Gerfen C. R., Mahan L. C. Sibley D. R. (1989) Multiple D2 dopamine receptors produced by alternative RNA splicing. Nature 342, 926 929.
31. Moulin D. E., Ling G. S. F. Pasternak G. W. (1988) Unidirectional analgesic cross tolerance between morphine and levorphanol in the rat. Pain 33, 233 239.
32. Namba T., Sugimoto Y., Negishi M., Irie A., Ushikubi F., Kakizuka A., Ito S., Ichikawa A. Narumiya S. (1993) Alternative splicing of C-terminal tail of prostaglandin E receptor subtype EP3 determines G-protein specificity. Nature 365, 166 170.
33. Olsen M. A., Nawoschik S. P., Schurman B. R., Schmitt H. L., Burno M., Smith D. L. Schechter L. E. (1999) Identification of a human 5-HT6 receptor variant produced by alternative splicing. Brain Res. Mol. Brain Res. 64, 255 263.
34. Pan Y. X. (2002) Identification and characterization of a novel promoter of the mouse mu opioid receptor gene (Oprm) that generates eight splice variants. Gene 295, 97 108.
35. Pan Y. X. (2005) Diversity and complexity of the mu opioid receptor gene: alternative pre-mRNA splicing and promoters. DNA Cell Biol. 24, 736 750.
36. Pan Y. X., Cheng J., Xu J., Rossi G., Jacobson E., RyanMoro J., Brooks A. I., Dean G. E., Standifer K. M. Pasternak G. W. (1995) Cloning and functional-characterization through antisense mapping of a kappa(3)-related opioid receptor. Mol. Pharmacol. 47, 1180 1188.
37. Pan Y. X., Xu J., RyanMoro J., Mathis J., Hom J. S. H., Mei J. F. Pasternak G. W. (1996) Dissociation of affinity and efficacy in KOR-3 chimeras. FEBS Lett. 395, 207 210.
38. Pan Y. X., Xu J., Bolan E., Abbadie C., Chang A., Zuckerman A., Rossi G. Pasternak G. W. (1999) Identification and characterization of three new alternatively spliced mu-opioid receptor isoforms. Mol. Pharmacol. 56, 396 403.
39. Pan Y. X., Xu J., Bolan E., Chang A., Mahurter L., Rossi G. Pasternak G. W. (2000) Isolation and expression of a novel alternatively spliced mu opioid receptor isoform, MOR-1F. FEBS Lett. 466, 337 340.
40. Pan Y. X., Xu J., Mahurter L., Bolan E., Xu M. Pasternak G. W. (2001) Generation of the mu opioid receptor (MOR-1) protein by three new splice variants of the Oprm gene. Proc. Natl Acad. Sci. USA 98, 14084 14089.
41. Pan Y. X., Xu J., Mahurter L., Xu M. M., Gilbert A. K. Pasternak G. W. (2003) Identification and characterization of two new human mu opioid receptor splice variants, hMOR-1O and hMOR-1X. Biochem. Biophys. Res. Commun. 301, 1057 1061.
42. Pan L., Xu J., Yu R., Xu M. M., Pan Y. X. Pasternak G. W. (2005a) Identification and characterization of six new alternatively spliced variants of the human mu opioid receptor gene, Oprm. Neuroscience 133, 209 220.
43. Pan Y. X., Xu J., Bolan E., Moskowitz H. S., Xu M. Pasternak G. W. (2005b) Identification of four novel exon 5 splice variants of the mouse mu-opioid receptor gene: functional consequences of C-terminal splicing. Mol. Pharmacol. 68, 866 875.
44. Pasternak G. W. (1993) Pharmacological mechanisms of opioid analgesics. Clin. Neuropharmacol. 16, 1 18.
45. Pasternak G. W. (2001) The pharmacology of mu analgesics: from patients to genes. Neuroscientist 7, 220 231.
46. Pasternak G. W. (2004) Multiple opiate receptors: deja vu all over again. Neuropharmacology 47 (Suppl 1 312 323.
47. Pasternak D. A., Pan L., Xu J., Yu R., Xu M. M., Pasternak G. W. Pan Y. X. (2004) Identification of three new alternatively spliced variants of the rat mu opioid receptor gene: dissociation of affinity and efficacy. J. Neurochem. 91, 881 890.
48. Payne R. Pasternak G. W. (1992) Pain, in Principles of Drug Therapy in Neurology (Johnston M. V., Macdonald R. L. Young A. B., eds pp. 268 301. F.A. Davis, Philadelphia.
49. Portenoy R. K. (1996) Opioid analgesics, in Pain Management: Theory and Practice (Portenoy R. K. Kanner R. M., eds pp. 248 276. F.A. Davis, Philadelphia.
50. Rossi G. C., Pan Y.-X., Brown G. P. Pasternak G. W. (1995a) Antisense mapping the MOR-1 opioid receptor: evidence for alternative splicing and a novel morphine-6β-glucuronide receptor. FEBS Lett. 369, 192 196.
51. Rossi G. C., Standifer K. M. Pasternak G. W. (1995b) Differential blockade of morphine and morphine-6β-glucuronide analgesia by antisense oligodeoxynucleotides directed against MOR-1 and G-protein α subunits in rats. Neurosci. Lett. 198, 99 102.
52. Rossi G. C., Leventhal L., Pan Y. X., Cole J., Su W., Bodnar R. J. Pasternak G. W. (1997) Antisense mapping of MOR-1 in rats: distinguishing between morphine and morphine-6beta-glucuronide antinociception. J. Pharmacol. Exp. Ther. 281, 109 114.
53. Schnell S. A. Wessendorf M. W. (2004) Expression of MOR1C-like mu-opioid receptor mRNA in rats. J. Comp. Neurol. 473, 213 232.
54. Schuller A. G., King M. A., Zhang J. et al. (1999) Retention of heroin and morphine-6 beta-glucuronide analgesia in a new line of mice lacking exon 1 of MOR-1. Nat. Neurosci. 2, 151 156.
55. Stamm S., Riethoven J. J., Le Texier V., Gopalakrishnan C., Kumanduri V., Tang Y., Barbosa-Morais N. L. Thanaraj T. A. (2006) ASD: a bioinformatics resource on alternative splicing. Nucleic Acids Res. 34, D46 D55.
56. Sugimoto Y. Narumiya S. (2007) Prostaglandin E receptors. J. Biol. Chem. 282, 11613 11617.
57. Thompson R. C., Mansour A., Akil H. Watson S. J. (1993) Cloning and pharmacological characterization of a rat μ opioid receptor. Neuron 11, 903 913.
58. Vanetti M., Kouba M., Wang X., Vogt G. Hollt V. (1998) Cloning and expression of a novel mouse somatostatin receptor (SSTR2B). FEBS Lett. 311, 290 294.
59. Vukusic I., Grellscheid S. N. Wiehe T. (2007) Applying genetic programming to the prediction of alternative mRNA splice variants. Genomics 89, 471 479.
60. Wang J. B., Imai Y., Eppler C. M., Gregor P., Spivak C. E. Uhl G. R. (1993) μ opiate receptor: cDNA cloning and expression. Proc. Natl Acad. Sci. USA 90, 10230 10234.
61. Wolozin B. L. Pasternak G. W. (1981) Classification of multiple morphine and enkephalin binding sites in the central nervous system. Proc. Natl Acad. Sci. USA 78, 6181 6185.
62. Xu J., Xu M. Pan Y. X. (2006) Characterizing exons 11 and 1 promoters of the mu opioid receptor (Oprm) gene in transgenic mice. BMC Mol. Biol. 7, 41.
63. Zhang Y., Pan Y. X., Kolesnikov Y. Pasternak G. W. (2006) Immunohistochemical labeling of the mu opioid receptor carboxy terminal splice variant mMOR-1B4 in the mouse central nervous system. Brain Res. 1099, 33 43.
64. Zimprich A., Simon T. Hollt V. (1995) Cloning and expression of an isoform of the rat μ opioid receptor (rMOR 1 B) which differs in agonist induced desensitization from rMOR1. FEBS Lett. 359, 142 146.