Sorting of neuropeptides and neuropeptide receptors into secretory pathways

Progress in Neurobiology

Volumn 90, Issue 2, 2010, Pages 276-283

  Zhang, Xu ^a   Bao, Lan ^b   Ma, Guo Qiang ^b  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

Author keywords

Neuropeptide; Neuropeptide receptor; Opioid receptor; Secretory pathway; Sorting mechanism; Substance P

Indexed keywords

CALCIUM ION; CELL SURFACE RECEPTOR; DELTA OPIATE RECEPTOR; HORMONE PRECURSOR; MU OPIATE RECEPTOR; NEUROPEPTIDE; NEUROPEPTIDE RECEPTOR; OPIATE RECEPTOR; PEPTIDE DERIVATIVE; PROTACHYKININ; PROTEIN ANTIBODY; SUBSTANCE P; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANALYTIC METHOD; CALCIUM CELL LEVEL; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CELL NUCLEUS; EXOCYTOSIS; GOLGI COMPLEX; HUMAN; HYDROPHOBICITY; NEUROSECRETION; NEUROSECRETORY CELL; NONHUMAN; PEPTIDOMICS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN TARGETING; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SECRETORY GRANULE; SECRETORY VESICLE; SENSORY NERVE CELL; SPINAL GANGLION;

ANIMALS; CALCIUM; HUMANS; NEURONS; NEUROPEPTIDES; PROTEIN TRANSPORT; RECEPTORS, NEUROPEPTIDE; SECRETORY PATHWAY; SECRETORY VESICLES; TRANS-GOLGI NETWORK;

EID: 76849102925     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2009.10.011     Document Type: Review

References (94)

1. Ahn A.H., and Basbaum A.I. Tissue injury regulates serotonin 1D receptor expression: implications for the control of migraine and inflammatory pain. J. Neurosci. 26 (2006) 8332-8338
2. Ambrose-Lanci L.M., Peiris N.B., Unterwald E.M., and Van Bockstaele E.J. Cocaine withdrawal-induced trafficking of delta-opioid receptors in rat nucleus accumbens. Brain Res. 1210 (2008) 92-102
3. Ambrose L.M., Gallagher S.M., Unterwald E.M., and Van Bockstaele E.J. Dopamine-D1 and delta-opioid receptors co-exist in rat striatal neurons. Neurosci. Lett. 399 (2006) 191-196
4. Arvan P., and Castle D. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem. J. 332 Pt 3 (1998) 593-610
5. Assadi M., Sharpe J.C., Snell C., and Loh Y.P. The C-terminus of prohormone convertase 2 is sufficient and necessary for Raft association and sorting to the regulated secretory pathway. Biochemistry 43 (2004) 7798-7807
6. Bao L., Jin S.X., Zhang C., Wang L.H., Xu Z.Z., Zhang F.X., Wang L.C., Ning F.S., Cai H.J., Guan J.S., Xiao H.S., Xu Z.Q., He C., Hökfelt T., Zhou Z., and Zhang X. Activation of delta opioid receptors induces receptor insertion and neuropeptide secretion. Neuron 37 (2003) 121-133
7. Bernier V., Bichet D.G., and Bouvier M. Pharmacological chaperone action on G-protein-coupled receptors. Curr. Opin. Pharmacol. 4 (2004) 528-533
8. Besse D., Lombard M.C., and Besson J.M. Autoradiographic distribution of μ, δ and κ opioid binding sites in the superficial dorsal horn, over the rostrocaudal axis of the rat spinal cord. Brain Res. 548 (1991) 287-291
9. Besse D., Lombard M.C., Perrot S., and Besson J.M. Regulation of opioid binding sites in the superficial dorsal horn of the rat spinal cord following loose ligation of the sciatic nerve: comparison with sciatic nerve section and lumbar dorsal rhizotomy. Neuroscience 50 (1992) 921-933
10. Besse D., Lombard M.C., Zajac J.M., Roques B.P., and Besson J.M. Pre- and postsynaptic distribution of μ, δ and κ opioid receptors in the superficial layers of the cervical dorsal horn of the rat spinal cord. Brain Res. 521 (1990) 15-22
11. Brakch N., Allemandou F., Cavadas C., Grouzmann E., and Brunner H.R. Dibasic cleavage site is required for sorting to the regulated secretory pathway for both pro- and neuropeptide Y. J. Neurochem. 81 (2002) 1166-1175
12. Bukau B., Weissman J., and Horwich A. Molecular chaperones and protein quality control. Cell 125 (2006) 443-451
13. 2+ in isolated chromaffin vesicles. Biochemistry 24 (1985) 7760-7765
14. Burke N.V., Han W., Li D., Takimoto K., Watkins S.C., and Levitan E.S. Neuronal peptide release is limited by secretory granule mobility. Neuron 19 (1997) 1095-1102
15. Cahill C.M., McClellan K.A., Morinville A., Hoffert C., Hubatsch D., O'Donnell D., and Beaudet A. Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization. J. Comp. Neurol. 440 (2001) 65-84
16. Cahill C.M., Morinville A., Hoffert C., O'Donnell D., and Beaudet A. Up-regulation and trafficking of δ opioid receptor in a model of chronic inflammation: implications for pain control. Pain 101 (2003) 199-208
17. Cahill C.M., Morinville A., Lee M.C., Vincent J.P., Collier B., and Beaudet A. Prolonged morphine treatment targets delta opioid receptors to neuronal plasma membranes and enhances delta-mediated antinociception. J. Neurosci. 21 (2001) 7598-7607
18. Chalfie M., Tu Y., Euskirchen G., Ward W.W., and Prasher D.C. Green fluorescent protein as a marker for gene expression. Science 263 (1994) 802-805
19. Cheng P.Y., Liu-Chen L.Y., and Pickel V.M. Dual ultrastructural immunocytochemical labeling of μ and δ opioid receptors in the superficial layers of the rat cervical spinal cord. Brain Res. 778 (1997) 367-380
20. Cheng P.Y., Svingos A.L., Wang H., Clarke C.L., Jenab S., Beczkowska I.W., Inturrisi C.E., and Pickel V.M. Ultrastructural immunolabeling shows prominent presynaptic vesicular localization of δ-opioid receptor within both enkephalin- and nonenkephalin-containing axon terminals in the superficial layers of the rat cervical spinal cord. J. Neurosci. 15 (1995) 5976-5988
21. Colomer V., Kicska G.A., and Rindler M.J. Secretory granule content proteins and the luminal domains of granule membrane proteins aggregate in vitro at mildly acidic pH. J. Biol. Chem. 271 (1996) 48-55
22. Commons K.G. Translocation of presynaptic δ opioid receptors in the ventrolateral periaqueductal gray after swim stress. J. Comp. Neurol. 464 (2003) 197-207
23. Commons K.G., Beck S.G., Rudoy C., and Van Bockstaele E.J. Anatomical evidence for presynaptic modulation by the δ opioid receptor in the ventrolateral periaqueductal gray of the rat. J. Comp. Neurol. 430 (2001) 200-208
24. Cool D.R., Normant E., Shen F., Chen H.C., Pannell L., Zhang Y., and Loh Y.P. Carboxypeptidase E is a regulated secretory pathway sorting receptor: genetic obliteration leads to endocrine disorders in Cpe(fat) mice. Cell 88 (1997) 73-83
25. Courel M., Vasquez M.S., Hook V.Y., Mahata S.K., and Taupenot L. Sorting of the neuroendocrine secretory protein Secretogranin II into the regulated secretory pathway: role of N- and C-terminal alpha-helical domains. J. Biol. Chem. 283 (2008) 11807-11822
26. De Camilli P., and Jahn R. Pathways to regulated exocytosis in neurons. Annu. Rev. Physiol. 52 (1990) 625-645
27. Dickenson A.H., and Kieffer B.L. Opiates: basic mechanisms. In: McMahon S.B., and Koltzenburg M. (Eds). Wall and Melzack's Textbook of Pain (2005), Elsevier Churchill Livingstone, Philadelphia, Pennsylvania, United States 427-442
28. Dikeakos J.D., Lacombe M.J., Mercure C., Mireuta M., and Reudelhuber T.L. A hydrophobic patch in a charged alpha-helix is sufficient to target proteins to dense core secretory granules. J. Biol. Chem. 282 (2007) 1136-1143
29. Dikeakos J.D., and Reudelhuber T.L. Sending proteins to dense core secretory granules: still a lot to sort out. J. Cell Biol. 177 (2007) 191-196
30. Doly S., Fischer J., Brisorgueil M.J., Verge D., and Conrath M. Pre- and postsynaptic localization of the 5-HT7 receptor in rat dorsal spinal cord: immunocytochemical evidence. J. Comp. Neurol. 490 (2005) 256-269
31. Elde R., Hokfelt T., Johansson O., and Terenius L. Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience 1 (1976) 349-351
32. Ellgaard L., Molinari M., and Helenius A. Setting the standards: quality control in the secretory pathway. Science 286 (1999) 1882-1888
33. Farhadi H.F., Mowla S.J., Petrecca K., Morris S.J., Seidah N.G., and Murphy R.A. Neurotrophin-3 sorts to the constitutive secretory pathway of hippocampal neurons and is diverted to the regulated secretory pathway by coexpression with brain-derived neurotrophic factor. J. Neurosci. 20 (2000) 4059-4068
34. Fields H.L., Emson P.C., Leigh B.K., Gilbert R.F., and Iversen L.L. Multiple opiate receptor sites on primary afferent fibres. Nature 284 (1980) 351-353
35. Fisher J.M., Sossin W., Newcomb R., and Scheller R.H. Multiple neuropeptides derived from a common precursor are differentially packaged and transported. Cell 54 (1988) 813-822
36. Gerdes H.H., Rosa P., Phillips E., Baeuerle P.A., Frank R., Argos P., and Huttner W.B. The primary structure of human secretogranin II, a widespread tyrosine-sulfated secretory granule protein that exhibits low pH- and calcium-induced aggregation. J. Biol. Chem. 264 (1989) 12009-12015
37. Glombik M.M., and Gerdes H.-H. Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie 82 (2000) 315-326
38. Guan J.S., Xu Z.Z., Gao H., He S.Q., Ma G.Q., Sun T., Wang L.H., Zhang Z.N., Lena I., Kitchen I., Elde R., Zimmer A., He C., Pei G., Bao L., and Zhang X. Interaction with vesicle luminal protachykinin regulates surface expression of δ-opioid receptors and opioid analgesia. Cell 122 (2005) 619-631
39. Gulbenkian S., Merighi A., Wharton J., Varndell I.M., and Polak J.M. Ultrastructural evidence for the coexistence of calcitonin gene-related peptide and substance P in secretory vesicles of peripheral nerves in the guinea pig. J. Neurocytol. 15 (1986) 535-542
40. Gupta A., Decaillot F.M., Gomes I., Tkalych O., Heimann A.S., Ferro E.S., and Devi L.A. Conformation state-sensitive antibodies to G-protein-coupled receptors. J. Biol. Chem. 282 (2007) 5116-5124
41. Gupta A., Rozenfeld R., Gomes I., Raehal K.M., Decaillot F.M., Bohn L.M., and Devi L.A. Post-activation-mediated changes in opioid receptors detected by N-terminal antibodies. J. Biol. Chem. 283 (2008) 10735-10744
42. Hökfelt T., Kellerth J.O., Nilsson G., and Pernow B. Substance P: localization in the central nervous system and in some primary sensory neurons. Science 190 (1975) 889-890
43. Hökfelt T., Ljungdahl A., Terenius L., Elde R., and Nilsson G. Immunohistochemical analysis of peptide pathways possibly related to pain and analgesia: enkephalin and substance P. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 3081-3085
44. Hökfelt T., Zhang X., and Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci. 17 (1994) 22-30
45. Hanson D.A., and Ziegler S.F. Fusion of green fluorescent protein to the C-terminus of granulysin alters its intracellular localization in comparison to the native molecule. J. Negat. Results Biomed. 3 (2004) 2
46. Hosaka M., Suda M., Sakai Y., Izumi T., Watanabe T., and Takeuchi T. Secretogranin III binds to cholesterol in the secretory granule membrane as an adapter for chromogranin A. J. Biol. Chem. 279 (2004) 3627-3634
47. Keller P., and Simons K. Post-Golgi biosynthetic trafficking. J. Cell Sci. 110 Pt 24 (1997) 3001-3009
48. Kelly R.B. Pathways of protein secretion in eukaryotes. Science 230 (1985) 25-32
49. Kitamura A., Kiyota T., Tomohiro M., Umeda A., Lee S., Inoue T., and Sugihara G. Morphological behavior of acidic and neutral liposomes induced by basic amphiphilic alpha-helical peptides with systematically varied hydrophobic-hydrophilic balance. Biophys. J. 76 (1999) 1457-1468
50. Kiyota T., Lee S., and Sugihara G. Design and synthesis of amphiphilic alpha-helical model peptides with systematically varied hydrophobic-hydrophilic balance and their interaction with lipid- and bio-membranes. Biochemistry 35 (1996) 13196-13204
51. 2+-triggered peptide secretion in single cells imaged with green fluorescent protein and evanescent-wave microscopy. Neuron 18 (1997) 857-863
52. Levitan E.S. Using GFP to image peptide hormone and neuropeptide release in vitro and in vivo. Methods 33 (2004) 281-286
53. Loh Y.P., Maldonado A., Zhang C., Tam W.H., and Cawley N. Mechanism of sorting proopiomelanocortin and proenkephalin to the regulated secretory pathway of neuroendocrine cells. Ann. N. Y. Acad. Sci. 971 (2002) 416-425
54. Lou H., Kim S.K., Zaitsev E., Snell C.R., Lu B., and Loh Y.P. Sorting and activity-dependent secretion of BDNF require interaction of a specific motif with the sorting receptor carboxypeptidase E. Neuron 45 (2005) 245-255
55. Ludwig M., and Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat. Rev. Neurosci. 7 (2006) 126-136
56. Ma G.Q., Wang B., Wang H.B., Wang Q., and Bao L. Short elements with charged amino acids form clusters to sort protachykinin into large dense-core vesicles. Traffic (Copenhagen, Denmark) 9 (2008) 2165-2179
57. Mansour A., Fox C.A., Burke S., Meng F., Thompson R.C., Akil H., and Watson S.J. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350 (1994) 412-438
58. Markkanen P.M., and Petaja-Repo U.E. N-glycan-mediated quality control in the endoplasmic reticulum is required for the expression of correctly folded delta-opioid receptors at the cell surface. J. Biol. Chem. 283 (2008) 29086-29098
59. Mennicken F., Zhang J., Hoffert C., Ahmad S., Beaudet A., and O'Donnell D. Phylogenetic changes in the expression of delta opioid receptors in spinal cord and dorsal root ganglia. J. Comp. Neurol. 465 (2003) 349-360
60. Merighi A. Costorage and coexistence of neuropeptides in the mammalian CNS. Prog. Neurobiol. 66 (2002) 161-190
61. Minami M., Maekawa K., Yabuuchi K., and Satoh M. Double in situ hybridization study on coexistence of μ-, δ-, and κ-opioid receptor mRNAs with preprotachykinin A mRNA in the rat dorsal root ganglia. Mol. Brain Res. 30 (1995) 203-210
62. Morello J.P., Petaja-Repo U.E., Bichet D.G., and Bouvier M. Pharmacological chaperones: a new twist on receptor folding. Trends Pharmacol. Sci. 21 (2000) 466-469
63. Morinville A., Cahill C.M., Esdaile M.J., Aibak H., Collier B., Kieffer B.L., and Beaudet A. Regulation of δ-opioid receptor trafficking via mu-opioid receptor stimulation: evidence from μ-opioid receptor knock-out mice. J. Neurosci. 23 (2003) 4888-4898
64. Mouchantaf R., Kumar U., Sulea T., and Patel Y.C. A conserved alpha-helix at the amino terminus of prosomatostatin serves as a sorting signal for the regulated secretory pathway. J. Biol. Chem. 276 (2001) 26308-26316
65. Mulcahy L.R., Vaslet C.A., and Nillni E.A. Prohormone-convertase 1 processing enhances post-Golgi sorting of prothyrotropin releasing hormone-derived peptides. J. Biol. Chem. 280 (2005) 39818-39826
66. Perello M., Stuart R., and Nillni E.A. Prothyrotropin-releasing hormone targets its processing products to different vesicles of the secretory pathway. J. Biol. Chem. 283 (2008) 19936-19947
67. Petaja-Repo U.E., Hogue M., Bhalla S., Laperriere A., Morello J.P., and Bouvier M. Ligands act as pharmacological chaperones and increase the efficiency of delta opioid receptor maturation. EMBO J. 21 (2002) 1628-1637
68. Petaja-Repo U.E., Hogue M., Laperriere A., Walker P., and Bouvier M. Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human delta opioid receptor. J. Biol. Chem. 275 (2000) 13727-13736
69. Potrebic S., Ahn A.H., Skinner K., Fields H.L., and Basbaum A.I. Peptidergic nociceptors of both trigeminal and dorsal root ganglia express serotonin 1D receptors: implications for the selective antimigraine action of triptans. J. Neurosci. 23 (2003) 10988-10997
70. Salio C., Averill S., Priestley J.V., and Merighi A. Costorage of BDNF and neuropeptides within individual dense-core vesicles in central and peripheral neurons. Dev. Neurobiol. 67 (2007) 326-338
71. Sambrook J.F. The involvement of calcium in transport of secretory proteins from the endoplasmic reticulum. Cell 61 (1990) 197-199
72. Scherrer G., Tryoen-Toth P., Filliol D., Matifas A., Laustriat D., Cao Y.Q., Basbaum A.I., Dierich A., Vonesh J.L., Gaveriaux-Ruff C., and Kieffer B.L. Knockin mice expressing fluorescent δ-opioid receptors uncover G protein-coupled receptor dynamics in vivo. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 9691-9696
73. Shennan K.I., Taylor N.A., and Docherty K. Calcium- and pH-dependent aggregation and membrane association of the precursor of the prohormone convertase PC2. J. Biol. Chem. 269 (1994) 18646-18650
74. Song L., and Fricker L.D. Calcium- and pH-dependent aggregation of carboxypeptidase E. J. Biol. Chem. 270 (1995) 7963-7967
75. Stevens C.W., Lacey C.B., Miller K.E., Elde R.P., and Seybold V.S. Biochemical characterization and regional quantification of μ, δ and κ οpioid binding sites in rat spinal cord. Brain Res. 550 (1991) 77-85
76. Tooze S.A., Martens G.J., and Huttner W.B. Secretory granule biogenesis: rafting to the SNARE. Trends Cell Biol. 11 (2001) 116-122
77. Tran E.J., Bolger T.A., and Wente S.R. SnapShot: nuclear transport. Cell 131 (2007) 420
78. Wang H., Cuzon V.C., and Pickel V.M. Ultrastructural localization of delta-opioid receptors in the rat caudate-putamen nucleus during postnatal development: relation to synaptogenesis. J. Comp. Neurol. 467 (2003) 343-353
79. Wang H., and Wessendorf M.W. Equal proportions of small and large DRG neurons express opioid receptor mRNAs. J. Comp. Neurol. 429 (2001) 590-600
80. Wang H.B., Guan J.S., Bao L., and Zhang X. Distinct subcellular distribution of delta-opioid receptor fused with various tags in PC12 cells. Neurochem. Res. 33 (2008) 2028-2034
81. Wang Q.P., Ochiai H., Guan J.L., and Nakai Y. Ultrastructural localization of delta-1 opioid receptor in the dorsal raphe nucleus of the rat. Synapse 26 (1997) 243-253
82. Whim M.D., and Moss G.W. A novel technique that measures peptide secretion on a millisecond timescale reveals rapid changes in release. Neuron 30 (2001) 37-50
83. Wu M.M., Grabe M., Adams S., Tsien R.Y., Moore H.P., and Machen T.E. Mechanisms of pH regulation in the regulated secretory pathway. J. Biol. Chem. 276 (2001) 33027-33035
84. Xia X., Lessmann V., and Martin T.F. Imaging of evoked dense-core-vesicle exocytosis in hippocampal neurons reveals long latencies and kiss-and-run fusion events. J. Cell Sci. 122 (2009) 75-82
85. 2+-induced conformational change and aggregation of chromogranin B. Comparison with chromogranin A and implication in secretory vesicle biogenesis. J. Biol. Chem. 270 (1995) 12578-12583
86. 2+-induced conformational change and aggregation of chromogranin A. J. Biol. Chem. 265 (1990) 14414-14421
87. Zhang X., Bao L., Arvidsson U., Elde R., and Hökfelt T. Localization and regulation of the δ-opioid receptor in dorsal root ganglia and spinal cord of the rat and monkey: evidence for association with the membrane of large dense-core vesicles. Neuroscience 82 (1998) 1225-1242
88. Zhang X., Bao L., and Guan J.S. Role of delivery and trafficking of δ-opioid peptide receptors in opioid analgesia and tolerance. Trends Pharmacol. Sci. 27 (2006) 324-329
89. Zhang X., Bao L., Shi T.J., Ju G., Elde R., and Hökfelt T. Down-regulation of μ-opioid receptors in rat and monkey dorsal root ganglion neurons and spinal cord after peripheral axotomy. Neuroscience 82 (1998) 223-240
90. Zhang X., Bean A.J., Wiesenfeld-Hallin Z., and Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord-IV. Effects of peripheral axotomy with special reference to neuropeptide Y and vasoactive intestinal polypeptide/peptide histidine isoleucine. Neuroscience 64 (1995) 917-941
91. Zhang X., Bean A.J., Wiesenfeld-Hallin Z., Xu X.J., and Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord-III. Effects of peripheral axotomy with special reference to galanin. Neuroscience 64 (1995) 893-915
92. Zhang X., Nicholas A.P., and Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the spinal cord-I. Co-existence of galanin with other peptides in primary afferents in normal rats. Neuroscience 57 (1993) 365-384
93. Zhang X., Tong Y.G., Bao L., and Hökfelt T. The neuropeptide Y Y1 receptor is a somatic receptor on dorsal root ganglion neurons and a postsynaptic receptor on somatostatin dorsal horn neurons. Eur. J. Neurosci. 11 (1999) 2211-2225
94. Zhu Y., King M.A., Schuller A.G., Nitsche J.F., Reidl M., Elde R.P., Unterwald E., Pasternak G.W., and Pintar J.E. Retention of supraspinal δ-like analgesia and loss of morphine tolerance in δ opioid receptor knockout mice. Neuron 24 (1999) 243-252