Differential modulation of N-type calcium channels by µ-opioid receptors in oxytocinergic versus vasopressinergic neurohypophysial terminals
Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have previously shown that µ‐opioid receptor (MOR) activation induces a stronger inhibition of oxytocin (OT) than vasopressin (AVP) release from isol...
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| Published in | Journal of cellular physiology Vol. 225; no. 1; pp. 276 - 288 |
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| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
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| Abstract | Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have previously shown that µ‐opioid receptor (MOR) activation induces a stronger inhibition of oxytocin (OT) than vasopressin (AVP) release from isolated MCN terminals. This higher sensitivity of OT release is due, at least in part, to the selective targeting of R‐type calcium channels. We now describe the underlying basis for AVP's weaker inhibition by MOR activation and provide a more complete explanation of the complicated effects on neuropeptide release. We found that N‐type calcium channels in AVP terminals are differentially modulated by MOR; enhanced at lower concentrations but increasingly inhibited at higher concentrations of agonists. On the other hand, N‐type calcium channels in OT terminals were always inhibited. The response pattern in co‐labeled terminals was analogous to that observed in AVP‐containing terminals. Changes in intracellular calcium concentration and neuropeptide release corroborated these results as they showed a similar pattern of enhancement and inhibition in AVP terminals contrasting with solely inhibitory responses in OT terminals to MOR agonists. We established that fast translocation of Ca2+ channels to the plasma membrane was not mediating current increments and thus, changes in channel kinetic properties are most likely involved. Finally, we reveal a distinct Ca‐channel β‐subunit expression between each type of nerve endings that could explain some of the differences in responses to MOR activation. These results help advance our understanding of the complex modulatory mechanisms utilized by MORs in regulating presynaptic neuropeptide release. J. Cell. Physiol. 225: 276–288, 2010. © 2010 Wiley‐Liss, Inc. |
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| AbstractList | Abstract
Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have previously shown that µ‐opioid receptor (MOR) activation induces a stronger inhibition of oxytocin (OT) than vasopressin (AVP) release from isolated MCN terminals. This higher sensitivity of OT release is due, at least in part, to the selective targeting of R‐type calcium channels. We now describe the underlying basis for AVP's weaker inhibition by MOR activation and provide a more complete explanation of the complicated effects on neuropeptide release. We found that N‐type calcium channels in AVP terminals are differentially modulated by MOR; enhanced at lower concentrations but increasingly inhibited at higher concentrations of agonists. On the other hand, N‐type calcium channels in OT terminals were always inhibited. The response pattern in co‐labeled terminals was analogous to that observed in AVP‐containing terminals. Changes in intracellular calcium concentration and neuropeptide release corroborated these results as they showed a similar pattern of enhancement and inhibition in AVP terminals contrasting with solely inhibitory responses in OT terminals to MOR agonists. We established that fast translocation of Ca
2+
channels to the plasma membrane was not mediating current increments and thus, changes in channel kinetic properties are most likely involved. Finally, we reveal a distinct Ca‐channel β‐subunit expression between each type of nerve endings that could explain some of the differences in responses to MOR activation. These results help advance our understanding of the complex modulatory mechanisms utilized by MORs in regulating presynaptic neuropeptide release. J. Cell. Physiol. 225: 276–288, 2010. © 2010 Wiley‐Liss, Inc. Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have previously shown that µ‐opioid receptor (MOR) activation induces a stronger inhibition of oxytocin (OT) than vasopressin (AVP) release from isolated MCN terminals. This higher sensitivity of OT release is due, at least in part, to the selective targeting of R‐type calcium channels. We now describe the underlying basis for AVP's weaker inhibition by MOR activation and provide a more complete explanation of the complicated effects on neuropeptide release. We found that N‐type calcium channels in AVP terminals are differentially modulated by MOR; enhanced at lower concentrations but increasingly inhibited at higher concentrations of agonists. On the other hand, N‐type calcium channels in OT terminals were always inhibited. The response pattern in co‐labeled terminals was analogous to that observed in AVP‐containing terminals. Changes in intracellular calcium concentration and neuropeptide release corroborated these results as they showed a similar pattern of enhancement and inhibition in AVP terminals contrasting with solely inhibitory responses in OT terminals to MOR agonists. We established that fast translocation of Ca2+ channels to the plasma membrane was not mediating current increments and thus, changes in channel kinetic properties are most likely involved. Finally, we reveal a distinct Ca‐channel β‐subunit expression between each type of nerve endings that could explain some of the differences in responses to MOR activation. These results help advance our understanding of the complex modulatory mechanisms utilized by MORs in regulating presynaptic neuropeptide release. J. Cell. Physiol. 225: 276–288, 2010. © 2010 Wiley‐Liss, Inc. Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have previously shown that μ-opioid receptor (MOR) activation induces a stronger inhibition of oxytocin (OT) than vasopressin (AVP) release from isolated MCN terminals. This higher sensitivity of OT release is due, at least in part, to the selective targeting of R-type calcium channels. We now describe the underlying basis for AVP's weaker inhibition by MOR activation and provide a more complete explanation of the complicated effects on neuropeptide release. We found that N-type calcium channels in AVP terminals are differentially modulated by MOR; enhanced at lower concentrations but increasingly inhibited at higher concentrations of agonists. On the other hand, N-type calcium channels in OT terminals were always inhibited. The response pattern in co-labeled terminals was analogous to that observed in AVP-containing terminals. Changes in intracellular calcium concentration and neuropeptide release corroborated these results as they showed a similar pattern of enhancement and inhibition in AVP terminals contrasting with solely inhibitory responses in OT terminals to MOR agonists. We established that fast translocation of Ca 2+ channels to the plasma membrane was not mediating current increments and thus, changes in channel kinetic properties are most likely involved. Finally, we reveal a distinct Ca-channel β-subunit expression between each type of nerve endings that could explain some of the differences in responses to MOR activation. These results help advance our understanding of the complex modulatory mechanisms utilized by MORs in regulating presynaptic neuropeptide release. |
| Author | Treistman, Steven N. Custer, Edward E. Ortiz-Miranda, Sonia I. Dayanithi, Govindan Velázquez-Marrero, Cristina Lemos, José R. |
| AuthorAffiliation | 1 Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts 3 INSERM 583, INM-Hópital St. Eloi, Montpellier Cedex, France 2 Brudnick Neuropsychiatric Institute, University of Massachusetts Medical School, Worcester, Massachusetts |
| AuthorAffiliation_xml | – name: 1 Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts – name: 3 INSERM 583, INM-Hópital St. Eloi, Montpellier Cedex, France – name: 2 Brudnick Neuropsychiatric Institute, University of Massachusetts Medical School, Worcester, Massachusetts |
| Author_xml | – sequence: 1 givenname: Sonia I. surname: Ortiz-Miranda fullname: Ortiz-Miranda, Sonia I. email: sonia.ortiz-miranda@umassmed.edu organization: Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts – sequence: 2 givenname: Govindan surname: Dayanithi fullname: Dayanithi, Govindan organization: INSERM 583, INM-Hópital St. Eloi, Montpellier Cedex, France – sequence: 3 givenname: Cristina surname: Velázquez-Marrero fullname: Velázquez-Marrero, Cristina organization: Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts – sequence: 4 givenname: Edward E. surname: Custer fullname: Custer, Edward E. organization: Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts – sequence: 5 givenname: Steven N. surname: Treistman fullname: Treistman, Steven N. organization: Brudnick Neuropsychiatric Institute, University of Massachusetts Medical School, Worcester, Massachusetts – sequence: 6 givenname: José R. surname: Lemos fullname: Lemos, José R. organization: Department of Physiology & Program in Neuroscience, University of Massachusetts Medical School, Worcester, Massachusetts |
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| CitedBy_id | crossref_primary_10_1016_j_ceca_2012_01_008 crossref_primary_10_1111_acer_12057 crossref_primary_10_1085_jgp_201311110 crossref_primary_10_14814_phy2_14198 crossref_primary_10_1016_j_peptides_2011_09_020 crossref_primary_10_1016_j_pneurobio_2013_08_005 crossref_primary_10_1523_JNEUROSCI_2505_13_2014 |
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| Copyright | Copyright © 2010 Wiley‐Liss, Inc. 2010 Wiley-Liss, Inc. 2010 |
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| Notes | UMass Medical School FDSP - No. P60037094900000 National Institute Alcohol Abuse - No. AA08003 istex:CE98F626775354E7FCA9069CF26662CDAEDF4DB2 ark:/67375/WNG-F34J4LMS-Q ArticleID:JCP22263 National Institute of Health - No. NS24970 National Institute of Drug Abuse - No. DA10487 Steven N. Treistman's present address is Instituto de Neurobiologia, Boulevard del Valle 201, San Juan 00901, Puerto Rico. Govindan Dayanithi's present address is Department of Cellular Neurophysiology, Academy of Sciences of the Czech Republic, Institute of Experimental Medicine, v.v.i. EU Research Centre of Excellence, Vdenska, 1083, 142 20 Prague 4, Czech Republic. |
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The alpha1 2004; 7 2004; 24 1998; 119 2004; 6 2003; 15 1994; 24 1982; 220 2008; 865 1988; 462 1998; 513 2008; 73 1987; 390 2003a; 35 1998; 273 1981; 391 1992; 90 1992; 92 1997; 502 2000; 12 1987; 114 1999; 19 1988a; 396 1988; 48 2000; 525 2003b; 55 1995; 21 1997; 17 1988; 84 1979; 282 2001; 98 1986; 119 1987; 121 1991; 37 1985; 5 1987; 325 2010 2007; 163 2006; 58 1984; 309 2002; 2 2009; 134 1988b; 20 1999; 1 1985; 260 1995; 6 1995; 270 1990; 2 1986; 61 1989; 244 2000; 36 1993; 94 1992; 574 2002; 22 1999; 274 2003; 24 1996; 271 1998; 30 1991; 129 2005; 17 2003; 100 2006; 224 1999; 515 e_1_2_6_51_1 e_1_2_6_32_1 e_1_2_6_30_1 Slizgi GR (e_1_2_6_53_1) 1982; 220 e_1_2_6_19_1 e_1_2_6_13_1 e_1_2_6_36_1 e_1_2_6_59_1 e_1_2_6_11_1 e_1_2_6_34_1 e_1_2_6_17_1 e_1_2_6_55_1 Lemos JR (e_1_2_6_33_1) 2002; 2 e_1_2_6_15_1 e_1_2_6_38_1 e_1_2_6_57_1 e_1_2_6_62_1 e_1_2_6_64_1 e_1_2_6_43_1 e_1_2_6_20_1 e_1_2_6_41_1 e_1_2_6_60_1 e_1_2_6_9_1 e_1_2_6_5_1 e_1_2_6_7_1 Paronis CA (e_1_2_6_44_1) 1995; 21 e_1_2_6_24_1 e_1_2_6_49_1 e_1_2_6_3_1 e_1_2_6_22_1 e_1_2_6_28_1 e_1_2_6_45_1 e_1_2_6_26_1 e_1_2_6_47_1 e_1_2_6_52_1 e_1_2_6_54_1 e_1_2_6_10_1 e_1_2_6_31_1 e_1_2_6_50_1 e_1_2_6_14_1 e_1_2_6_35_1 e_1_2_6_12_1 e_1_2_6_18_1 e_1_2_6_39_1 e_1_2_6_56_1 e_1_2_6_16_1 e_1_2_6_37_1 e_1_2_6_58_1 e_1_2_6_63_1 e_1_2_6_42_1 e_1_2_6_65_1 e_1_2_6_21_1 e_1_2_6_40_1 e_1_2_6_8_1 e_1_2_6_4_1 Velázquez‐Marrero C (e_1_2_6_61_1) 2008; 865 e_1_2_6_6_1 e_1_2_6_25_1 e_1_2_6_48_1 e_1_2_6_23_1 e_1_2_6_2_1 e_1_2_6_29_1 e_1_2_6_27_1 e_1_2_6_46_1 |
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| Snippet | Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We have... Abstract Opioids modulate the electrical activity of magnocellular neurons (MCN) and inhibit neuropeptide release at their terminals in the neurohypophysis. We... |
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| Title | Differential modulation of N-type calcium channels by µ-opioid receptors in oxytocinergic versus vasopressinergic neurohypophysial terminals |
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