Teneurin C-terminal associated peptides (TCAP): Modulators of corticotropin-releasing factor (CRF) physiology and behavior

Frontiers in Neuroscience

Volumn , Issue 7 SEP, 2013, Pages

  Chen, Yani ^a   Xu, Mei ^a   Almeida, Reuben De ^a   Lovejoy, David A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cytoskeleton; Dystroglycan; ERK1 2; Glucocorticoids; HPA axis; Peptide evolution; Stress

Indexed keywords

COMPLEMENTARY DNA; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; MEMBRANE PROTEIN; SYNTHETIC PEPTIDE; TENEURIN 1 PROTEIN; TENEURIN C TERMINAL ASSOCIATED PEPTIDE; TENEURIN C TERMINAL ASSOCIATED PEPTIDE 1; TENEURIN PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMPHIBIA; ANIMAL BEHAVIOR; ARTHROPOD; BEHAVIOR; CARBOXY TERMINAL SEQUENCE; CARTILAGINOUS FISH; CELL ACTIVITY; CELL STIMULATION; CELLS; CHORDATA; CYTOSKELETON; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INVERTEBRATE; MAMMAL; MOLECULAR EVOLUTION; NERVE CELL; NEUROMODULATION; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE;

EID: 84899742720     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00166     Document Type: Review

References (38)

1. Al Chawaf, A., St. Amant, K., Belsham, D., and Lovejoy, D. A. (2007a). Regulation of neurite growth in immortalized mouse hypothalamic neurons and rat hippocampal primary cultures by teneurin C-terminal-associated peptide-1. Neuroscience 144, 1241-1254. doi: 10.1016/j.neuroscience.2006.09.062
2. Al Chawaf, A., Xu, K., Tan, L., Vaccarino, F. J., and Lovejoy, D. A. (2007). Corticotropin-releasing factor (CRF)-induced behaviors are modulated by intravenous administration of teneurin C-terminal associated peptide-1 (TCAP-1). Peptides 28, 1406-1415. doi: 10.1016/j.peptides.2007.05.014
3. Barsyte, D., Tipping, D. R., Smart, D., Conlon, J. M., Baker, B. I., and Lovejoy, D. A. (1999). Rainbow trout (Oncorhynchus mykiss) urotensin-I: structural differences between urotensins-I and urocortins. Gen. Comp. Endocrinol. 115, 169-177. doi: 10.1006/gcen.1999.7290
4. Chand, D., Casatti, C. A., de Lannoy, L., Song, L., Kollara, A., Barsyte-Lovejoy, D., et al. (2012a). C-terminal processing of the teneurin proteins: independent actions of a teneurin C-terminal associated peptide in hippocampal cells. Mol. Cell. Neurosci. 52C, 38-50. doi: 10.1016/j.mcn.2012.09.006
5. Chand, D., Song, L., Delannoy, L., Barsyte-Lovejoy, D., Ackloo, S., Boutros, P. C., et al. (2012b). C-terminal region of teneurin-1 co-localizes with dystroglycan and modulates cytoskeletal organization through an extracellular signal-related kinase-dependent stathmin- and filamin A-mediated mechanism in hippocampal cells. Neuroscience 219, 255-270. doi: 10.1016/j.neuroscience.2012.05.069
6. Chand, D., de Lannoy, L., Tucker, R., and Lovejoy, D. A. (2013). Origin of chordate peptides by horizontal protozoan gene transfer in early metazoans and protists: evolution of the teneurin C-terminal associated peptides (TCAP). Gen. Comp. Endocrinol. 188, 144-150. doi: 10.1016/j.ygcen.2013.02.006
7. Chen, Y., Dube, C. M., Rice, C. J., and Baram, T. Z. (2008). Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J. Neurosci. 28, 2903-2911. doi: 10.1523/JNEUROSCI.0225-08.2008
8. de Lannoy, L., and Lovejoy, D. A. (in press). Evolution and phylogeny of the corticotropin-releasing factor (CRF) family of peptides: expansion and specialization in the vertebrates. J. Chem. Neuroanat.
9. Denver, R. J. (2009). Structural and functional evolution of vertebrate neuroendocrine stress systems. Ann. N.Y. Acad. Sci. 1163, 1-16. doi: 10.1111/j.1749-6632.2009.04433.x
10. Donaldson, C. J., Sutton, S. W., Perrin, M. P., Corrigan, A. Z., Lewis, K. A., Rivier, J. E., et al. (1996). Cloning and characterization of human urocortin. Endocrinology 137, 2167-2170. doi: 10.1210/en.137.5.2167
11. Hauger, R. L., Risbrough, V., Brauns, O., and Dautzenberg, F. M. (2006). Corticotropin Releasing Factor (CRF) receptor signalling in the central nervous system: new molecular targets. CNS Neurol. Disord. Drug Targets 5, 453-479. doi: 10.2174/187152706777950684
12. Kenzelmann, D., Chiquet-Ehrismann, R., and Tucker, R. P. (2007). Teneurins, a transmembrane protein family involved in cell communication during neuronal development. Cell. Mol. Life Sci. 64, 1452-1456. doi: 10.1007/s00018-007-7108-9
13. Kovacs, K. J. (1998). c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem. Int. 33, 287-297. doi: 10.1016/S0197-0186(98)00023-0
14. Kupferschmidt, D. A., Lovejoy, D. A., Rotzinger, S., and Erb, S. (2010). Teneurin C-terminal associated peptide-1 blocks the effects of corticotropin-releasing factor on reinstatement of cocaine seeking and on cocaine-induced behavioural sensitization. Br. J. Pharmacol. 162, 574-583. doi: 10.1111/j.1476-5381.2010.01055.x
15. Lewis, K., Li, C., Perrin, M. H., Blount, A., Kunitake, K., Donaldson, C., et al. (2001). Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proc. Natl. Acad. Sci. U.S.A. 98, 7570-7575. doi: 10.1073/pnas.121165198
16. Lovejoy, D. A. (2009). Structural evolution of urotensin-I: retaining ancestral functions before corticotropin-releasing hormone evolution. Gen. Comp. Endocrinol. 164, 15-19. doi: 10.1016/j.ygcen.2009.04.014
17. Lovejoy, D. A., Al Chawaf, A., and Cadinouche, M. (2006). Teneurin C-terminal associated peptides: an enigmatic family of neuropeptides with structural similarity to the corticotrophin-releasing factor and calcitonin families of peptides. Gen. Comp. Endocrinol. 148, 299-305. doi: 10.1016/j.ygcen.2006.01.012
18. Lovejoy, D. A., and Balment, R. J. (1999). Evolution and physiology of the corticotropin-releasing factor (CRF) family of neuropeptides in vertebrates. Gen. Comp. Endocrinol. 155, 1-22. doi: 10.1006/gcen.1999.7298
19. Lovejoy, D. A., and Jahan, S. (2006). Phylogeny and evolution of the corticotropin releasing factor family of peptides. Gen. Comp. Endocrinol. 146, 1-8. doi: 10.1016/j.ygcen.2005.11.019
20. Lovejoy, D. A., Rotzinger, S., and Barsyte-Lovejoy, D. (2009). Evolution of complementary peptide systems: teneurin C-terminal-associated peptides and corticotropin-releasing factor superfamilies. Ann. N.Y. Acad. Sci. 1163, 215-220. doi: 10.1111/j.1749-6632.2008.03629.x
21. Martins, J. M., Kastin, A. J., and Banks, W. A. (1996). Unidirectional specific and modulated brain to blood transport of corticotropin-releasing hormone. Neuroendocrinology 63, 338-348. doi: 10.1159/000126974
22. Qian, X., Barsyte-Lovejoy, D., Wang, L., Chewpoy, B., Gautam, N., Al Chawaf, A., et al. (2004). Cloning and characterization of teneurin C-terminal associated peptide (TCAP)-3 from the hypothalamus of an adult rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 137, 205-216. doi: 10.1016/j.ygcen.2004.02.007
23. Reyes, T. M., Lewis, K., Perrin, M. H., Kunitake, K. S., Vaughan, J., Arias, C. A., et al. (2001). Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF receptors. Proc. Natl. Acad. Sci. U.S.A. 98, 2843-2848. doi: 10.1073/pnas.051626398
24. Rotzinger, S., Lovejoy, D. A., and Tan, L. A. (2010). Behavioural effects of neuropeptides in rodent models of depression and anxiety. Peptides 31, 736-756. doi: 10.1016/j.peptides.2009.12.015
25. Swinny, J. D., and Valentino, R. J. (2006). Corticotropin-releasing factor promotes growth of brain norepinephrine neuronal processes through Rho GTPase regulators of the actin cytoskeleton in rat. Eur. J. Neurosci. 24, 2481-2490. doi: 10.1111/j.1460-9568.2006.05129.x
26. Tan, L. A., Al Chawaf, A., Vaccarino, F. J., Boutros, P. C., and Lovejoy, D. A. (2011). Teneurin C-terminal associated peptide (TCAP)-1 modulates dendritic morphology in hippocampal neurons and decreases anxiety-like behaviors in rats. Physiol. Behav. 104, 199-204. doi: 10.1016/j.physbeh.2011.03.015
27. Tan, L. A., Xu, K., Vaccarino, F. J., Lovejoy, D. A., and Rotzinger, S. (2008). Repeated intracerebral teneurin C-terminal associated peptide (TCAP)-1 injections produce enduring changes in behavioral responses to corticotropin-releasing factor (CRF) in rat models of anxiety. Behav. Brain Res. 188, 195-200. doi: 10.1016/j.bbr.2007.10.032
28. Tan, L. A., Xu, K., Vaccarino, F. J., Lovejoy, D. A., and Rotzinger, S. (2009). Teneurin C-terminal associated peptide (TCAP)-1 attenuates corticotropin-releasing factor (CRF)-induced c-Fos expression in the limbic system and modulates anxiety behavior in male Wistar rats. Behav. Brain Res. 201, 198-206. doi: 10.1016/j.bbr.2009.02.013
29. Tsigos, C., and Chrousos, G. P. (2002). Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J. Psychosom. Res. 53, 865-871. doi: 10.1016/S0022-3999(02)00429-4
30. Tucker, R. P. (2013). Horizontal gene transfer in choanoflagellates. J. Exp. Zoo. B Mol. Dev. Evol. 320, 1-9. doi: 10.1002/jez.b.22480
31. Tucker, R. P., Beckmann, J., Leachman, N. T., Scholer, J., and Chiquet-Ehrismann, R. (2012). Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol. Biol. Evol. 29, 1019-1029. doi: 10.1093/molbev/msr271
32. Tucker, R. P., Kenzelmann, D., Trzebiatowska, A., and Chiquet-Ehrismann, R. (2007). Teneurins: transmembrane proteins with fundamental roles in development. Int. J. Biochem. Cell Biol. 39, 292-297. doi: 10.1016/j.biocel.2006.09.012
33. Ulrich-Lai, Y. M., and Herman, J. P. (2009). Neural regulation of endocrine and autonomic stress and responses. Nat. Rev. Neurosci. 10, 397-409. doi: 10.1038/nrn2647
34. Vaughan, J., Donaldson, C., Bittencourt, J., Perrin, M. H., Lewis, K., Sutton, S., et al. (1995). Urocortin, a mammalian neuropeptide related to fish urotensin-I and to corticotropin-releasing factor. Nature 378, 287-292. doi: 10.1038/378287a0
35. Wang, L., Rotzinger, S., Al Chawaf, A., Elias, C. F., Barsyte-Lovejoy, D., Qian, X., et al. (2005). Teneurin proteins possess a carboxy terminal sequence with neuromodulatory activity. Mol. Brain Res. 133, 253-265. doi: 10.1016/j.molbrainres.2004.10.019
36. Wang, X. D., Chen, Y., Wolf, M., Wagner, K. V., and Liebl, C. (2011). Forebrain CRHR1 deficiency attenuates chronic stress-induced cognitive deficits and dendritic remodeling. Neurobiol. Dis. 42, 300-310. doi: 10.1016/j.nbd.2011.01.020
37. Young, T. R., and Leamey, C. A. (2009). Teneurins: important regulators of neural circuitry. Int. J. Biochem. Cell Biol. 41, 990-993. doi: 10.1016/j.biocel.2008.06.014
38. Zhang, D., deSouza, R. F., Anantharaman, V., Iyer, L. M., and Aravind, L. (2012). Polymorphic toxin systems: comprehensive characterization of trafficking modes, mechanism of action, immunity and ecology using comparative genomics. Biol. Direct. 7, 18. doi: 10.1186/1745-6150-7-18