Adrenomedullin and CGRP interact with endogenous calcitonin-receptor-like receptor in endothial cells and induce its desensitisation by different mechanism

Journal of Cell Science

Volumn 119, Issue 5, 2006, Pages 910-922

  Nikitenko, Leonid L ^a,b,c   Blucher, Nicola ^a   Fox, Stephen B ^a   Bicknell, Roy ^b   Smith, David M ^d   Rees, Margaret C P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d ASTRAZENECA   (United Kingdom)

Author keywords

Adrenomedullin; CGRP; CRLR; Endogenous CL; Endothelial cell

Indexed keywords

ADRENOMEDULLIN; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; CALCITONIN RECEPTOR LIKE RECEPTOR; PROTEIN ANTIBODY; PROTEIN KINASE B;

ARTICLE; CARDIOVASCULAR DISEASE; CELL CULTURE; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; DIABETES MELLITUS; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; RECEPTOR INTRINSIC ACTIVITY; REGULATORY MECHANISM;

ADRENOMEDULLIN; CALCITONIN GENE-RELATED PEPTIDE; CELL LINE; CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; PEPTIDES; RECEPTORS, CALCITONIN; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; RECEPTORS, PEPTIDE; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY;

EID: 33645223704     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.02783     Document Type: Article

References (55)

1. Aiyar, N., Rand, K., Elshourbagy, N. A., Zeng, Z., Adamou, J. E., Bergsma, D. J. and Li, Y. (1996). A cDNA encoding the calcitonin gene-related peptide type 1 receptor. J. Biol. Chem. 271, 11325-11329.
2. Aiyar, N., Disa, J., Dang, K., Pronin, A. N., Benovic, J. L. and Nambi, P. (2000). Involvement of G protein-coupled receptor kinase-6 in desensitization of CGRP receptors. Eur J. Pharmacol. 403, 1-7.
3. Bomberger, J. M., Spielman, W. S., Hall, C. S., Weinmann, E. J. and Paramesarwaran, N. (2005). Receptor activity-modifying protein (RAMP) isoform-specific regulation of adrenomedullin receptor trafficking by NHERF-1. J. Biol. Chem. 280, 23926-23935.
4. Brain, S. D. and Cambridge, H. (1996). Calcitonin gene-related peptide: vasoactive effects and potential therapeutic role. Gen. Pharmacol. 27, 607-611.
5. Brain, S. D. and Grant, A. D. (2004). Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol. Rev. 84, 903-934.
6. Brell, B., Temmesfeld-Wollbruck, B., Altzschner, I., Frisch, E., Schmeck, B., Hocke, A. C., Suttorp, N. and Hippenstiel, S. (2005). Adrenomedullin reduces Staphylococcus aureus alpha-toxin-induced rat ileum microcirculatory damage. Crit. Care Med. 33, 819-826.
7. Doods, H., Hallermayer, G., Wu, D., Entzeroth, M., Rudolf, K., Engel, W. and Eberlein, W. (2000). Pharmacological profile of BIBN4096BS, the first selective small molecule CGRP antagonist. Br. J. Pharmacol. 129, 420-423.
8. Evans, B. N., Rosenblatt, M. I., Mnayer, L. O., Oliver, K. A. and Dickerson, I. M. (2000). CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors. J. Biol. Chem. 275, 31438-31443.
9. Fox, S. B., Bragança, J., Turley, H., Campo, L., Han, C., Gatter, K. C., Bhattacharya, S. and Harris, A. L. (2004). CITED4 inhibits hypoxia-activated transcription in cancer cells, and its cytoplasmic location in breast cancer is associated with elevated expression of tumor cell hypoxia-inducible factor 1alpha. Cancer Res. 64, 6075-6081.
10. Haegerstrand, A., Dalsgaard, C. J., Jonzon, B., Larsson, O. and Nilsson, J. (1990). Calcitonin gene-related peptide stimulates proliferation of human endothelial cells. Proc. Natl. Acad. Sci. USA 87, 3299-3303.
11. Hagner, S., Stahl, U., Knoblauch, B., McGregor, G. P. and Lang, R. E. (2002). Calcitonin receptor-like receptor: identification and distribution in human peripheral tissues. Cell Tissue Res. 310, 41-50.
12. Hay, D. L., Poyner, D. R. and Smith, D. M. (2003). Desensitisation of adrenomedullin and CGRP receptors. Regul. Pept. 112, 139-145.
13. Hay, D. L., Conner, A. C., Howitt, S. G., Takhshid, M. A., Simms, J., Mahmoud, K. and Poyner, D. R. (2004). The pharmacology of CGRP-responsive receptors in cultured and transfected cells. Peptides 25, 2019-2026.
14. Hay, D. L., Christopoulos, G., Christopoulos, A., Poyner, D. R. and Sexton, P. M. (2005). Pharmacological discrimination of calcitonin receptor: receptor activity-modifying protein complexes. Mol. Pharmacol. 67, 1655-1665.
15. Hilairet, S., Foord, S. M., Marshall, F. H. and Bouvier, M. (2001a). Protein-protein interaction and not glycosylation determines the binding selectivity of heterodimers between the calcitonin receptor-like receptor and the receptor activity-modifying proteins. J. Biol. Chem. 276, 29575-29581.
16. Hilairet, S., Belanger, C., Bertrand, J., Laperriere, A., Foord, S. M. and Bouvier, M. (2001b). Agonist-promoted internalization of a ternary complex between calcitonin receptor-like receptor, receptor activity-modifying protein 1 (RAMP1), and beta-arrestin. J. Biol. Chem. 276, 42182-42190.
17. Hinson, J. P., Kapas, S. and Smith, D. M. (2000). Adrenomedullin, a multifunctional regulatory peptide. Endocr. Rev. 21, 138-167.
18. Hippenstiel, S., Witzenrath, M., Schmeck, B., Hocke, A., Krisp, M., Krull, M., Seybold, J., Seeger, W., Rascher, W., Schutte, H. et al. (2002). Adrenomedullin reduces endothelial hyperpermeability. Circ. Res. 91, 618-625.
19. Ilan, N., Mahooti, S. and Madri, J. A. (1998). Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J. Cell Sci. 111, 3621-3631.
20. Kamitani, S., Asakawa, M., Shimekake, Y., Kuwasako, K., Nakahara, K. and Sakata, T. (1999). The RAMP2/CRLR complex is a functional adrenomedullin receptor in human endothelial and vascular smooth muscle cells. FEBS Lett. 448, 111-114.
21. Kato, H., Shichiri, M., Marumo, F. and Hirata, Y. (1997). Adrenomedullin as an autocrine/paracrine apoptosis survival factor for rat endothelial cells. Endocrinology 138, 2615-2620.
22. Kawai, J., Ando, K., Tojo, A., Shimosawa, T., Takahashi, K., Onozato, M. L., Yamasaki, M., Ogita, T., Nakaoka, T. and Fujita, T. (2004). Endogenous adrenomedullin protects against vascular response to injury in mice. Circulation 109, 1147-1153.
23. Kim, W., Moon, S. O., Sung, M. J., Kim, S. H., Lee, S., So, J. N. and Park, S. K. (2003). Angiogenic role of adrenomedullin through activation of Akt, mitogen-activated protein kinase, and focal adhesion kinase in endothelial cells. FASEB J. 17, 1937-1939.
24. Koenig, J. A. and Edwardson, J. M. (1997). Endocytosis and recycling of G protein-coupled receptors. Trends Pharmacol. Sci. 18, 276-287.
25. Kononen, J., Bubendorf, L., Kallioniemi, A., Barlund, M., Schraml, P., Leighton, S., Torhorst, J., Mihatsch, M. J., Sauter, G. and Kallioniemi, O. P. (1998). Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat. Med. 4, 844-847.
26. Krupnick, J. G. and Benovic, J. L. (1998). The role of receptor kinases and arrestins in G protein-coupled receptor regulation. Annu. Rev. Pharmacol. Toxicol. 38, 289-319.
27. Kuwasako, K., Shimekake, Y., Masuda, M., Nakahara, K., Yoshida, T., Kitaura, M., Kitamura, K., Eto, T. and Sakata, T. (2000). Visualization of the calcitonin receptor-like receptor and its receptor activity-modifying proteins during internalization and recycling. J. Biol. Chem. 275, 29602-29609.
28. Kuwasako, K., Cao, Y. N., Nagoshi, Y., Kitamura, K. and Eto, T. (2004). Adrenomedullin receptors: pharmacological features and possible pathophysiological roles. Peptides 25, 2003-2012.
29. LeCouter, J. and Ferrara, N. (2003). EG-VEGF and Bv8. a novel family of tissue-selective mediators of angiogenesis, endothelial phenotype, and function. Trends Cardiovasc. Med. 13, 276-282.
30. Liu, S., Premont, R. T., Kontos, C. D., Zhu, S. and Rockey, D. C. (2005). A crucial role for GRK2 in regulation of endothelial cell nitric oxide synthase function in portal hypertension. Nat. Med. 11, 952-958.
31. Maguire, J. J. and Davenport, A. P. (2005). Regulation of vascular reactivity by established and emerging GPCRs. Trends Pharmacol. Sci. 26, 448-454.
32. Martinez, A., Vos, M., Guedez, L., Kaur, G., Chen, Z., Garayoa, M., Pio, R., Moody, T., Stetler-Stevenson, W. G., Kleinman, H. K. et al. (2002). The effects of adrenomedullin overexpression in breast tumor cells. J. Natl. Cancer Inst. 94, 1226-1237.
33. Martinez, A., Julian, M., Bregonzio, C., Notari, L., Moody, T. W. and Cuttitta, F. (2004). Identification of vasoactive nonpeptidic positive and negative modulators of adrenomedullin using a neutralizing antibody-based screening strategy. Endocrinology 145, 3858-3865.
34. Matsui, H., Shimosawa, T., Itakura, K., Guanqun, X., Ando, K. and Fujita, T. (2004). Adrenomedullin can protect against pulmonary vascular remodeling induced by hypoxia. Circulation 109, 2246-2251.
35. McLatchie, L. M., Fraser, N. J., Main, M. J., Wise, A., Brown, J., Thompson, N., Solari, R., Lee, M. G. and Foord, S. M. (1998). RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393, 333-339.
36. Muff, R., Leuthauser, K., Buhlmann, N., Foord, S. M., Fischer, J. A. and Born, W. (1998). Receptor activity modifying proteins regulate the activity of a calcitonin gene-related peptide receptor in rabbit aortic endothelial cells. FEBS Lett. 441, 366-368.
37. Nakamura, M., Yoshida, H., Makita, S., Arakawa, N., Niinuma, H. and Hiramori, K. (1997). Potent and long-lasting vasodilatory effects of adrenomedullin in humans. Comparisons between normal subjects and patients with chronic heart failure. Circulation 95, 1214-1221.
38. Nikitenko, L. L., MacKenzie, I. Z., Rees, M. C. P. and Bicknell, R. (2000). Adrenomedullin is an autocrine regulator of endothelial growth in human endometrium. Mol. Hum. Reprod. 6, 811-819.
39. Nikitenko, L. L., Brown, N. S., Smith, D. M., MacKenzie, I. Z., Bicknell, R. and Rees, M. C. P. (2001). Differential and cell-specific expression of calcitonin receptor-like receptor and receptor activity modifying proteins in the human uterus. Mol. Hum. Reprod. 7, 655-664.
40. Nikitenko, L. L., Smith, D. M., Bicknell, R. and Rees, M. C. P. (2003). Transcriptional regulation of the CRLR gene in human microvascular endothelial cells by hypoxia. FASEB J. 17, 1499-1501.
41. Njuki, F., Nicholl, C. G., Howard, A., Mak, J. C., Barnes, P. J., Girgis, S.I. and Legon, S. (1993). A new calcitonin-receptor-like sequence in rat pulmonary blood vessels. Clin. Sci. 85, 385-388.
42. Oehler, M. K., Hague, S., Rees, M. C. and Bicknell, R. (2002). Adrenomedullin promotes formation of xenografted endometrial tumors by stimulation of autocrine growth and angiogenesis. Oncogene 21, 2815-2821.
43. Penn, R. B., Pronin, A. N. and Benovic, J. L. (2000). Regulation of G-protein coupled rece3ptor kinases. Trends Cardiovasc. Med. 10, 81-89.
44. Poyner, D. R., Sexton, P. M., Marshall, I., Smith, D. M., Quirion, R., Born, W., Muff, R., Fischer, J. A. and Foord, S. M. (2002). International Union of Pharmacology. XXXII. The mammalian calcitonin gene-related peptides, adrenomedullin, amylin, and calcitonin receptors. Pharmacol. Rev. 54, 233-246.
45. Roh, J., Chang, C. L., Bhalla, A., Klein, C. and Hsu, S. Y. (2004). Intermedin is a calcitonin/calcitonin gene-related peptide family peptide acting through the calcitonin receptor-like receptor/receptor activity-modifying protein receptor complexes. J. Biol. Chem. 279, 7264-7274.
46. Satoh, F., Takahashi, K., Murakami, O., Totsune, K., Sone, M., Ohneda, M., Abe, K., Miura, Y., Hayashi, Y., Sasano, H. et al. (1995). Adrenomedullin in human brain, adrenal glands and tumor tissues of pheochromocytoma, ganglioneuroblastoma and neuroblastoma. J. Clin. Endocrinol. Metab. 80, 1750-1752.
47. Schotten, U., Filzmaier, K., Borghardt, B., Kulka, S., Schoendube, F., Schumacher, C. and Hanrath, P. (2000). Changes of beta-adrenergic signaling in compensated human cardiac hypertrophy depend on the underlying disease. Am. J. Physiol. Heart Circ. Physiol. 278, H2076-H2083.
48. Sexton, P. M., Albiston, A., Morfis, M. and Tilakaratne, M. (2001). Receptor activity modifying proteins. Cell. Signal. 13, 73-83.
49. Shichiri, M., Kato, H., Doi, M., Marumo, F. and Hirata, Y. Induction of max by adrenomedullin and calcitonin gene-regulated peptide antagonizes endothelial apoptosis. Mol. Endocrinol. 13, 1353-1363.
50. Shindo, T., Kurihara, H., Maemura, K., Kurihara, Y., Kuwaki, T., Izumida, T., Minamino, N., Ju, K. H., Morita, H., Oh-hashi, Y. et al. (2000). Hypotension and resistance to lipopolysaccharide-induced shock in transgenic mice overexpressing adrenomedullin in their vasculature. Circulation 101, 2309-2316.
51. Shindo, T., Kurihara, Y., Nishimatsu, H., Moriyama, N., Kakoki, M., Wang, Y., Imai, Y., Ebihara, A., Kuwaki, T. and Ju, K. H. et al. (2001). Vascular abnormalities and elevated blood pressure in mice lacking adrenomedullin gene. Circulation 104, 1964-1971.
52. Thakali, K., Fink, G. D. and Watts, S. W. (2000). Arteries and veins desensitize differently to endothelin. J. Cardiovasc. Pharmacol. 43, 387-393.
53. Tokes, Z. A., Gendler, S. J. and Dermer, G. B. (1981). The synthesis of a proteinase inhibitor, alpha-1-antichymotrypsin, by human breast epithelial cells. J. Supramol. Struct. Cell Biochem. 17, 69-77.
54. Wierland, S. J., Gong, Q., Poblete, H., Fletcher, J. E., Chen, L. Q., Kallen, R. G. (1996). Modulation of human muscle sodium channels by intracellular fatty acids is dependent on the channel isoform. J. Biol. Chem. 271, 19037-19041.
55. Zhang, X. and Hintze, T. H. (2001). cAMP signal transduction cascade, a novel pathway for the regulation of endothelial nitric oxide production in coronary blood vessels. Arterioscler. Thromb. Vasc. Biol. 21, 797-803.