Progesterone receptor membrane component 1 is a functional part of the glucagon-like peptide-1 (GLP-1) receptor complex in pancreatic β cells

Molecular and Cellular Proteomics

Volumn 13, Issue 11, 2014, Pages 3049-3062

  Zhang, Ming ^a,b   Robitaille, Mélanie ^c   Showalter, Aaron D ^d   Huang, Xinyi ^a,b   Liu, Ying ^a   Bhattacharjee, Alpana ^a   Willard, Francis S ^d   Han, Junfeng ^e   Froese, Sean ^a,b   Wei, Li ^e   Gaisano, Herbert Y ^a   Angers, Stéphane ^c   Sloop, Kyle W ^d   Dai, Feihan F ^a   Wheeler, Michael B ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d ELI LILLY AND COMPANY   (United States)

^e SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CAND1 PROTEIN; CAVEOLIN 1; CELL MEMBRANE PROTEIN; CELL SURFACE RECEPTOR; COPB1 PROTEIN; COPB2 PROTEIN; COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; CYCLIC AMP; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GNB1 PROTEIN; GNG12 PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; NEUROGRANIN; PGRMC1 PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROGESTERONE RECEPTOR; PROGESTERONE RECEPTOR MEMBRANE COMPONENT 1; PROTEIN 14 3 3; PROTEIN HYDROLYSATE; RAB34 PROTEIN; RAB5B PROTEIN; RAB5C PROTEIN; TMED10 PROTEIN; TMEM33 PROTEIN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; INSULIN; MEMBRANE PROTEIN; PGRMC1 PROTEIN, MOUSE; RAB PROTEIN;

AFFINITY PURIFICATION MASS SPECTROMETRY; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; CHO CELL LINE; CONTROLLED STUDY; CYTOPLASM; EC50; EXOCYTOSIS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; INSULIN RELEASE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MIN6 CELL LINE; MOUSE; NONHUMAN; ONCOGENE SRC; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CRICETULUS; GENETICS; HAMSTER; HUMAN; METABOLISM; RAT; SECRETION (PROCESS);

ADENYLATE CYCLASE; ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; CYCLIC AMP; GLUCAGON-LIKE PEPTIDE 1; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MASS SPECTROMETRY; MEMBRANE PROTEINS; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; RAB5 GTP-BINDING PROTEINS; RATS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, GLUCAGON; RECEPTORS, PROGESTERONE;

EID: 84910636973     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.040196     Document Type: Article

References (55)

1. Nauck, M. A., Heimesaat, M. M., Orskov, C., Holst, J. J., Ebert, R., and Creutzfeldt, W. (1993) Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J. Clin. Invest. 91, 301-307
2. Pratley, R. E., and Gilbert, M. (2008) Targeting incretins in type 2 diabetes: role of GLP-1 receptor agonists and DPP-4 inhibitors. Rev. Diabetic Studies 5, 73-94
3. Drucker, D. J. (2013) Incretin action in the pancreas: potential promise, possible perils, and pathological pitfalls. Diabetes 62, 3316-3323
4. Fehmann, H. C., and Habener, J. F. (1992) Insulinotropic hormone glucagonlike peptide-I(7-37) stimulation of proinsulin gene expression and proinsulin biosynthesis in insulinoma beta TC-1 cells. Endocrinology 130, 159-166
5. Kinzig, K. P., D'Alessio, D. A., and Seeley, R. J. (2002) The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness. J. Neurosci. 22, 10470-10476
6. Nauck, M. A., Niedereichholz, U., Ettler, R., Holst, J. J., Orskov, C., Ritzel, R., and Schmiegel, W. H. (1997) Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. Am. J. Physiol. 273, E981-E988
7. Richter, G., Feddersen, O., Wagner, U., Barth, P., Goke, R., and Goke, B. (1993) GLP-1 stimulates secretion of macromolecules from airways and relaxes pulmonary artery. Am. J. Physiol. 265, L374-L381
8. Moreno, C., Mistry, M., and Roman, R. J. (2002) Renal effects of glucagonlike peptide in rats. Eur. J. Pharmacol. 434, 163-167
9. Yamamoto, H., Lee, C. E., Marcus, J. N., Williams, T. D., Overton, J. M., Lopez, M. E., Hollenberg, A. N., Baggio, L., Saper, C. B., Drucker, D. J., and Elmquist, J. K. (2002) Glucagon-like peptide-1 receptor stimulation increases blood pressure and heart rate and activates autonomic regulatory neurons. J. Clin. Invest. 110, 43-52
10. Richards, P., Parker, H. E., Adriaenssens, A. E., Hodgson, J. M., Cork, S. C., Trapp, S., Gribble, F. M., and Reimann, F. (2014) Identification and characterisation of glucagon-like peptide-1 receptor expressing cells using a new transgenic mouse model. Diabetes 63, 1224-1233
11. Bullock, B. P., Heller, R. S., and Habener, J. F. (1996) Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137, 2968-2978
12. Gier, B., Butler, P. C., Lai, C. K., Kirakossian, D., DeNicola, M. M., and Yeh, M. W. (2012) Glucagon like peptide-1 receptor expression in the human thyroid gland. J. Clin. Endocrinol. Metab. 97, 121-131
13. Jorgensen, R., Martini, L., Schwartz, T. W., and Elling, C. E. (2005) Characterization of glucagon-like peptide-1 receptor beta-Arrestin 2 interaction: a high-Affinity receptor phenotype. Mol. Endocrinol. 19, 812-823
14. Sonoda, N., Imamura, T., Yoshizaki, T., Babendure, J. L., Lu, J. C., and Olefsky, J. M. (2008) Beta-Arrestin-1 mediates glucagon-like peptide-1 signaling to insulin secretion in cultured pancreatic beta cells. Proc. Natl. Acad. Sci. U.S.A. 105, 6614-6619
15. Syme, C. A., Zhang, L., and Bisello, A. (2006) Caveolin-1 regulates cellular trafficking and function of the glucagon-like Peptide 1 receptor. Mol. Endocrinol. 20, 3400-3411
16. Schelshorn, D., Joly, F., Mutel, S., Hampe, C., Breton, B., Mutel, V., and Lutjens, R. (2012) Lateral allosterism in the glucagon receptor family: glucagon-like peptide 1 induces G-protein-coupled receptor heteromer formation. Mol. Pharmacol. 81, 309-318
17. Huang, X., Dai, F. F., Gaisano, G., Giglou, K., Han, J., Zhang, M., Kittanakom, S., Wong, V., Wei, L., Showalter, A. D., Sloop, K. W., Stagljar, I., and Wheeler, M. B. (2013) The identification of novel proteins that interact with the GLP-1 receptor and restrain its activity. Mol. Endocrinol. 27, 1550-1563
18. Kittanakom, S., Chuk, M., Wong, V., Snyder, J., Edmonds, D., Lydakis, A., Zhang, Z., Auerbach, D., and Stagljar, I. (2009) Analysis of membrane protein complexes using the split-ubiquitin membrane yeast two-hybrid (MYTH) system. Methods Mol. Biol. 548, 247-271
19. Ahmed, S. M., Daulat, A. M., and Angers, S. (2011) Tandem affinity purification and identification of heterotrimeric g protein-Associated proteins. Methods Mol. Biol. 756, 357-370
20. Chen, G. I., and Gingras, A. C. (2007) Affinity-purification mass spectrometry (AP-MS) of serine/threonine phosphatases. Methods 42, 298-305
21. Anastas, J. N., Biechele, T. L., Robitaille, M., Muster, J., Allison, K. H., Angers, S., and Moon, R. T. (2012) A protein complex of SCRIB, NOS1AP and VANGL1 regulates cell polarity and migration, and is associated with breast cancer progression. Oncogene 31, 3696-3708
22. Allister, E. M., Robson-Doucette, C. A., Prentice, K. J., Hardy, A. B., Sultan, S., Gaisano, H. Y., Kong, D., Gilon, P., Herrera, P. L., Lowell, B. B., and Wheeler, M. B. (2013) UCP2 regulates the glucagon response to fasting and starvation. Diabetes 62, 1623-1633
23. Liu, G., Zhang, J., Larsen, B., Stark, C., Breitkreutz, A., Lin, Z. Y., Breitkreutz, B. J., Ding, Y., Colwill, K., Pasculescu, A., Pawson, T., Wrana, J. L., Nesvizhskii, A. I., Raught, B., Tyers, M., and Gingras, A. C. (2010) ProHits: integrated software for mass spectrometry-based interaction proteomics. Nat. Biotechnol. 28, 1015-1017
24. Miteva, Y. V., and Cristea, I. M. (2014) A proteomic perspective of SIRT6 phosphorylation and interactions, and their dependence on its catalytic activity. Mol. Cell. Proteomics 13, 168-183
25. von Mering, C., Huynen, M., Jaeggi, D., Schmidt, S., Bork, P., and Snel, B. (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Res. 31, 258-261
26. Saito, R., Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L., Lotia, S., Pico, A. R., Bader, G. D., and Ideker, T. (2012) A travel guide to Cytoscape plugins. Nat. Methods 9, 1069-1076
27. Hardy, A. B., Fox, J. E., Giglou, P. R., Wijesekara, N., Bhattacharjee, A., Sultan, S., Gyulkhandanyan, A. V., Gaisano, H. Y., MacDonald, P. E., and Wheeler, M. B. (2009) Characterization of Erg K- channels in alpha-And beta-cells of mouse and human islets. J. Biol. Chem. 284, 30441-30452
28. Dai, F. F., Zhang, Y., Kang, Y., Wang, Q., Gaisano, H. Y., Braunewell, K. H., Chan, C. B., and Wheeler, M. B. (2006) The neuronal Ca2- sensor protein visinin-like protein-1 is expressed in pancreatic islets and regulates insulin secretion. J. Biol. Chem. 281, 21942-21953
29. Thomas, P., Pang, Y., and Dong, J. (2014) Enhancement of cell surface expression and receptor functions of membrane progestin receptor alpha (mPRalpha) by progesterone receptor membrane component 1 (PGRMC1): evidence for a role of PGRMC1 as an adaptor protein for steroid receptors. Endocrinology 155, 1107-1119
30. Drake, M. T., Shenoy, S. K., and Lefkowitz, R. J. (2006) Trafficking of G protein-coupled receptors. Circulat. Res. 99, 570-582
31. Mifsud, W., and Bateman, A. (2002) Membrane-bound progesterone receptors contain a cytochrome b5-like ligand-binding domain. Genome Biol. 3, RESEARCH0068
32. Peluso, J. J. (2013) Progesterone receptor membrane component 1 and its role in ovarian follicle growth. Front. Neurosci. 7, 99
33. Thomas, P. (2008) Characteristics of membrane progestin receptor alpha (mPRalpha) and progesterone membrane receptor component 1 (PGMRC1) and their roles in mediating rapid progestin actions. Front. Neuroendocrinol. 29, 292-312
34. Peluso, J. J., Romak, J., and Liu, X. (2008) Progesterone receptor membrane component-1 (PGRMC1) is the mediator of progesterone's antiapoptotic action in spontaneously immortalized granulosa cells as revealed by PGRMC1 small interfering ribonucleic acid treatment and functional analysis of PGRMC1 mutations. Endocrinology 149, 534-543
35. MacDonald, P. E., Wang, X., Xia, F., El-kholy, W., Targonsky, E. D., Tsushima, R. G., and Wheeler, M. B. (2003) Antagonism of rat beta-cell voltage-dependent K- currents by exendin 4 requires dual activation of the cAMP/protein kinase A and phosphatidylinositol 3-kinase signaling pathways. J. Biol. Chem. 278, 52446-52453
36. Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P., and Grant, S. G. (2000) Proteomic analysis of NMDA receptor-Adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669
37. Becamel, C., Alonso, G., Galeotti, N., Demey, E., Jouin, P., Ullmer, C., Dumuis, A., Bockaert, J., and Marin, P. (2002) Synaptic multiprotein complexes associated with 5-HT(2C) receptors: a proteomic approach. EMBO J. 21, 2332-2342
38. Raju, R., Rakocevic, G., Chen, Z., Hoehn, G., Semino-Mora, C., Shi, W., Olsen, R., and Dalakas, M. C. (2006) Autoimmunity to GABAA-receptorassociated protein in stiff-person syndrome. Brain 129, 3270-3276
39. Petersen, S. L., Intlekofer, K. A., Moura-Conlon, P. J., Brewer, D. N., Del Pino Sans, J., and Lopez, J. A. (2013) Novel progesterone receptors: neural localization and possible functions. Front. Neurosci. 7, 164
40. Xu, J., Zeng, C., Chu, W., Pan, F., Rothfuss, J. M., Zhang, F., Tu, Z., Zhou, D., Zeng, D., Vangveravong, S., Johnston, F., Spitzer, D., Chang, K. C., Hotchkiss, R. S., Hawkins, W. G., Wheeler, K. T., and Mach, R. H. (2011) Identification of the PGRMC1 protein complex as the putative sigma-2 receptor binding site. Nat. Commun. 2, 380
41. Cahill, M. A. (2007) Progesterone receptor membrane component 1: an integrative review. J. Steroid Biochem. Mol. Biol. 105, 16-36
42. Peluso, J. J., Liu, X., Gawkowska, A., and Johnston-MacAnanny, E. (2009) Progesterone activates a progesterone receptor membrane component 1-dependent mechanism that promotes human granulosa/luteal cell survival but not progesterone secretion. J. Clin. Endocrinol. Metab. 94, 2644-2649
43. Ashby, J. P., Shirling, D., and Baird, J. D. (1978) Effect of progesterone on insulin secretion in the rat. J. Endocrinol. 76, 479-486
44. Costrini, N. V., and Kalkhoff, R. K. (1971) Relative effects of pregnancy, estradiol, and progesterone on plasma insulin and pancreatic islet insulin secretion. J. Clin. Invest. 50, 992-999
45. Flock, G. B., Cao, X., Maziarz, M., and Drucker, D. J. (2013) Activation of enteroendocrine membrane progesterone receptors promotes incretin secretion and improves glucose tolerance in mice. Diabetes 62, 283-290
46. Beck, P. (1970) Reversal of progesterone-enhanced insulin production by human chorionic somatommammotropin. Endocrinology 87, 311-315
47. Willard, F. S., and Sloop, K. W. (2012) Physiology and emerging biochemistry of the glucagon-like peptide-1 receptor. Exp. Diabetes Res. 2012, 470851
48. Holz, G. G. (2004) Epac: a new cAMP-binding protein in support of glucagon-like peptide-1 receptor-mediated signal transduction in the pancreatic beta-cell. Diabetes 53, 5-13
49. Ahmed, I. S., Rohe, H. J., Twist, K. E., and Craven, R. J. (2010) Pgrmc1 (progesterone receptor membrane component 1) associates with epidermal growth factor receptor and regulates erlotinib sensitivity. J. Biol. Chem. 285, 24775-24782
50. Buteau, J., Foisy, S., Joly, E., and Prentki, M. (2003) Glucagon-like peptide 1 induces pancreatic beta-cell proliferation via transactivation of the epidermal growth factor receptor. Diabetes 52, 124-132
51. Lee, H. Y., Yea, K., Kim, J., Lee, B. D., Chae, Y. C., Kim, H. S., Lee, D. W., Kim, S. H., Cho, J. H., Jin, C. J., Koh, D. S., Park, K. S., Suh, P. G., and Ryu, S. H. (2008) Epidermal growth factor increases insulin secretion and lowers blood glucose in diabetic mice. J. Cell. Mol. Med. 12, 1593-1604
52. MacDonald, P. E., Sewing, S., Wang, J., Joseph, J. W., Smukler, S. R., Sakellaropoulos, G., Wang, J., Saleh, M. C., Chan, C. B., Tsushima, R. G., Salapatek, A. M., and Wheeler, M. B. (2002) Inhibition of Kv2.1 voltage-dependent K- channels in pancreatic beta-cells enhances glucose-dependent insulin secretion. J. Biol. Chem. 277, 44938-44945
53. Basford, C. L., Prentice, K. J., Hardy, A. B., Sarangi, F., Micallef, S. J., Li, X., Guo, Q., Elefanty, A. G., Stanley, E. G., Keller, G., Allister, E. M., Nostro, M. C., and Wheeler, M. B. (2012) The functional and molecular characterisation of human embryonic stem cell-derived insulin-positive cells compared with adult pancreatic beta cells. Diabetologia 55, 358-371
54. Van de Velde, S., Hogan, M. F., and Montminy, M. (2011) mTOR links incretin signaling to HIF induction in pancreatic beta cells. Proc. Natl. Acad. Sci. U.S.A. 108, 16876-16882
55. Prentice, K. J., Luu, L., Allister, E. M., Liu, Y., Jun, L. S., Sloop, K. W., Hardy, A. B., Wei, L., Jia, W., Fantus, I. G., Sweet, D. H., Sweeney, G., Retnakaran, R., Dai, F. F., and Wheeler, M. B. (2014) The furan fatty acid metabolite CMPF is elevated in diabetes and induces beta cell dysfunction. Cell Metab. 19, 653-666