Role of βarrestin1 in AT 1 R-mediated mitogen-activated protein kinase activation in Wistar and SHR brainstem astrocytes

Journal of Neurochemistry

Volumn 148, Issue 1, 2019, Pages 46-62

  Negussie, Shmuel ^a   Lymperopoulos, Anastasios ^a   Clark, Michelle A ^a  

^a NOVA SOUTHEASTERN UNIVERSITY   (United States)

Author keywords

Angiotensin type 1 receptor; astrocytes; beta arrestin; G protein coupled receptor; renin angiotensin aldosterone system; spontaneously hypertensive rat

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; BETA ARRESTIN 1; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN STEM; CONTROLLED STUDY; ENZYME ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SPONTANEOUSLY HYPERTENSIVE RAT; WISTAR RAT; ANIMAL; HYPERTENSION; METABOLISM; PHYSIOLOGY;

ANIMALS; ASTROCYTES; BETA-ARRESTIN 1; BRAIN STEM; ENZYME ACTIVATION; HYPERTENSION; MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, INBRED SHR; RATS, WISTAR; RECEPTOR, ANGIOTENSIN, TYPE 1;

EID: 85056389173     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.14620     Document Type: Article

References (79)

1. Ahn S., Wei H., Garrison T. R. and Lefkowitz R. J. (2004) Reciprocal regulation of angiotensin receptor-activated extracellular signal-regulated kinases by β-arrestins 1 and 2. J. Biol. Chem. 279, 7807–7811
2. Allen A. M., Dosanjh J. K., Erac M. et al. (2006) Expression of constitutively active angiotensin receptors in the rostral ventrolateral medulla increases blood pressure. Hypertension 47(6), 1054–1061
3. Amenta F., Tayebati S. K. and Tomassoni D. (2010) Spontaneously hypertensive rat neuroanatomy: applications to pharmacological research. Ital. J. Anat. Embryol. 115, 13–17
4. Attramadal H., Arriza J. L., Aoki C., Dawson T. M., Codina J., Kwatra M. M., Synders S. H., Caron M. G. and Lefkowitz R. J. (1992) Beta-arrestin2, a novel member of the arrestin/beta-arrestin gene family. J. Biol. Chem. 267, 17882–17890
5. Beindl W., Mitterauer T., Hohenegger M., Ijzerman A. P., Nanoff C. and Freissmuth M. (1996) Inhibition of receptor/G protein coupling by suramin analogues. Mol. Pharmacol. 50, 415–423
6. Bonde M. M., Hansen J. T., Sanni S. J., Haunsø S., Gammeltoft S., Lyngsø C. and Hansen J. L. (2010) Biased signaling of the angiotensin II type 1 receptor can be mediated through distinct mechanisms. PLoS ONE 5, e14135
7. Bourassa E. A., Kristen A., Stedenfeld K. A., Sved A. F. and Speth R. C. (2015) Selective C1 lesioning slightly decreases angiotensin II type I receptor expression in the rat rostral ventrolateral medulla (RVLM). Neurochem. Res. 40(10), 2113–2120
8. Chung W. and Kermode J. C. (2005) Suramin disrupts receptor-G protein coupling by blocking association of G protein alpha and betagamma subunits. J. Pharmacol. Exp. Ther. 313, 191–198
9. Clark M. A. and Gonzalez N. (2007) Angiotensin II stimulates rat astrocyte mitogen-activated protein kinase activity and growth through EGF and PDGF receptor transactivation. Regul. Pept. 144, 115–122
10. Clark M. A., Landrum M. H. and Tallant E. A. (2001) Angiotensin II activates mitogen-activated protein kinases and stimulates growth in rat medullary astrocytes. FASEB J. 15, 11698
11. Clark M. A., Guillaume G. and Pierre-Louis H. C. (2008) Angiotensin II induces proliferation of cultured rat astrocytes through c-Jun N-terminal kinase. Brain Res. Bull. 75, 101–106
12. Clark M. A., Tran H. and Nguyen C. (2011) Angiotensin III stimulates ERK1/2 mitogen-activated protein kinases and astrocyte growth in cultured rat astrocytes. Neuropeptides 45, 329–335
13. Clark M. A., Nguyen C. and Tran H. (2012) Angiotensin III induces C-jun N-terminal kinase leading to proliferation of rat astrocytes. Neurochem. Res. 37, 1475–1481
14. Dampney R. A. L. (2006) Angiotensin type 1A receptors on glial cells in rostral ventrolateral medulla and hypertension. Hypertension 47, 1052–1053
15. Delaney J., Chiarello R., Villar D., Kandalam U., Castejon A. M. and Clark M. A. (2008) Regulation of c-fos, c-jun and c-myc gene expression by angiotensin II in primary cultured rat astrocytes: role of ERK1/2 MAP kinases. Neurochem. Res. 33, 545–550
16. DeWire S. M., Ahn S., Lefkowitz R. J. and Shenoy S. K. (2007) β-Arrestins and cell signaling. Annu. Rev. Physiol. 69, 483–510
17. Drake M. T., Shenoy S. K. and Lefkowitz R. J. (2006) Trafficking of G protein-coupled receptors. Circ. Res. 99, 570–582
18. Drake M. T., Violin J. D., Whalen E. J., Wisler J. W., Shenoy S. K. and Lefkowitz R. J. (2008) beta-arrestin-biased agonism at the beta2-adrenergic receptor. J. Biol. Chem. 283, 5669–5676
19. Gadea A., Schinelli S. and Gallo V. (2008) Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J. Neurosc. 28, 2394–2408
20. Gao X., Zhang F., Han Y., Wang H., Zhang Y., Guo R. and Zhu G. (2004) AT1 receptor in rostral ventrolateral medulla mediating blunted baroreceptor reflex in spontaneously hypertensive rats. Acta Pharmacol. Sin. 25, 1433–1438
21. de Gasparo M., Catt K. J., Inagami T., Wright J. W. and Unger T. (2000) International Union of Pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 52, 415–472
22. Gesty-Palmer D., Chen M., Reiter E. et al. (2006) Distinct β-arrestin- and G protein-dependent pathways for parathyroid hormone receptor-stimulated ERK1/2 activation. J. Biol. Chem. 281, 10856–10864
23. Grassi G., Mark A. and Esler M. (2015) The sympathetic nervous system alterations in human hypertension. Circ. Res. 116, 976–990
24. Gurevich E. V., Benovic J. L. and Gurevich V. V. (2002) Arrestin2 and arrestin3 are differentially expressed in the rat brain during postnatal development. Neuroscience 109, 421–436
25. Haspula D. and Clark M. A. (2016) Heterologous regulation of the cannabinoid type 1 receptor by angiotensin II in astrocytes of spontaneously hypertensive rats. J. Neurochem. 139, 523–536
26. Haspula D. and Clark M. A. (2017) MAPK activation patterns of AT1R and CB1R in SHR versus Wistar astrocytes: evidence of CB1R hypofunction and crosstalk between AT1R and CB1R. Cell. Signal. 40, 81–90
27. Hupfeld C. J., Dalle S. and Olefsky J. M. (2003) Beta -Arrestin 1 down-regulation after insulin treatment is associated with supersensitization of beta 2 adrenergic receptor Galpha s signaling in 3T3-L1 adipocytes. Proc. Natl Acad. Sci. USA 100, 161–166
28. Isegawa K., Hirooka Y., Katsuki M., Kishi T. and Sunagawa K. (2014) Angiotensin II type 1 receptor expression in astrocytes is upregulated leading to increased mortality in mice with myocardial infarction-induced heart failure. Am. J. Physiol. Heart Circ. Physiol. 307, H1448–H1455
29. Kandalam U. and Clark M. A. (2010) Angiotensin II activates JAK2/ STAT3 pathway and induces interleukin-6 production in cultured rat brainstem astrocytes. Regul. Pept. 159, 110–116
30. Kearney P. M., Whelton M., Reynolds K., Muntner P., Whelton P. K. and He J. (2005) Global burden of hypertension: analysis of worldwide data. Lancet 365, 217–223
31. Kendall R. T., Strungs E. G., Rachidi S. M., Lee M. H., El-Shewy H. M., Luttrell D. K., Janech M. G. and Luttrell L. M. (2011) The β -arrestin pathway-selective type 1A angiotensin receptor (AT 1A) agonist [Sar1, Ile 4, Ile 8]angiotensin II regulates a robust G protein-independent signaling network. J. Biol. Chem. 286, 19880–19891
32. Kim J., Ahn S., Rajagopal K. and Lefkowitz R. J. (2009) Independent β-arrestin2 and Gq/protein kinase Cξ pathways for ERK stimulated by angiotensin type 1A receptors in vascular smooth muscle cells converge on transactivation of the epidermal growth factor receptor. J. Biol. Chem. 284, 11953–11962
33. Lefkowitz R. J. and Shenoy S. K. (2005) Transduction of receptor signals by beta-arrestins. Science 308, 512–517
34. Livak K. J. and Schmittgen T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25, 402–408
35. Luttrell L. M., Gesty-Palmer D. and Sibley D. R. (2010) Beyond desensitization: physiological relevance of arrestin-dependent signaling. Pharmacolo. Rev. 62, 305–330
36. Lymperopoulos A. and Negussie S. (2013) βarrestins in cardiac G protein-coupled receptor signaling and function: partners in crime or “good cop, bad cop”? Int. J. Mol. Sci. 14, 24726–24741
37. Lymperopoulos A., Rengo G., Zincarelli C., Kim J., Soltys S. and Koch W. J. (2009) An adrenal -arrestin 1-mediated signaling pathway underlies angiotensin II-induced aldosterone production in vitro and in vivo. Proc. Natl Acad. Sci. USA 106, 5825–5830
38. Lynch K. R., Hawelu-Johnson C. L. and Guyenet P. G. (1987) Localization of brain angiotensinogen mRNA by hybridization histochemistry. Mol. Brain Res. 388, 149–158
39. Maier T., Güell M. and Serrano L. (2009) Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583, 3966–3973
40. Maning J., Negussie S., Clark M. A. and Lymperopoulos A. (2017) Biased agonism/antagonism at the AngII-AT1 receptor: implications for adrenal aldosterone production and cardiovascular therapy. Pharmacol. Res. 125, 14–20
41. McCrink K. A., Maning J., Vu A., Jafferjee M., Marrero C., Brill A., Bathgate-Siryk A., Dabul S., Koch W. J. and Lymperopoulos A. (2017a) β-Arrestin2 improves post-myocardial infarction heart failure via Sarco(endo) plasmic reticulum Ca2+-ATPase-dependent positive inotropy in cardiomyocytes. Hypertension 70, 972–981
42. McCrink K. A., Maning J., Vu A., Jafferjee M., Marrero C., Brill A., Bathgate-Siryk A., Dabul S., Koch W. J. and Lymperopoulos A. (2017b) Cardiac βarrestin2 improves contractility and adverse remodeling in heart failure, but is underexpressed in humans. J. Am. Coll. Cardiol. 70, 2948–2949
43. McKinley M. J., Albiston A. L., Allen A. M., Mathai M. L., May C. N., McAllen R. M., Oldfield B. J., Mendelsohn F. A. and Chai S. Y. (2003) The brain renin-angiotensin system: location and physiological roles. Int. J. Biochem. Cell Biol. 35, 901–918
44. McLennan G. P., Kiss A., Miyatake M., Belcheva M. M., Chambers K. T., Pozek J. J., Mohabbat Y., Moyer R. A., Bohn M. L. and Coscia C. J. (2008) Kappa opioids promote the proliferation of astrocytes via Gβγ and β-arrestin 2-dependent MAPK-mediated pathways. J. Neurochem. 107, 1753–1765
45. Michel M. C. and Seifert R. (2015) Selectivity of pharmacological tools: implications for use in cell physiology. A Review in the Theme: cell Signaling: proteins, Pathways and Mechanisms. Am. J. Physiol. Cell Physiol. 308, C505–C520
46. Milsted A. M. Y., Barnaf B. P., Ransohoff R. M., Brosnihan K. B. and Ferrario C. M. (1990) Astrcoyte cultures derived from human brain tissue expression angiotensinogen mRNA. Proc. Natl Acad. Sci. USA 87, 5720–5723
47. Morinelli T. A., Kendall R. T., Luttrell L. M., Walker L. P. and Ullian M. E. (2009) Angiotensin II-induced cyclooxygenase 2 expression in rat aorta vascular smooth muscle cells does not require heterotrimeric G protein activation. J. Pharmacol. Exp. Ther. 330, 118–124
48. Oakley R. H., Laporte S. A., Holt J. A., Caron M. G. and Barak L. S. (2009) Differential affinities of visual arrestin, βarrestin1, and βarrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem. 275, 17201–17210
49. Oakley R. H., Revollo J. and Cidlowski J. A. (2012) Glucocorticoids regulate arrestin gene expression and redirect the signaling profile of G protein-coupled receptors. Proc. Natl Acad. Sci. USA 109, 17591–17596
50. Pinto Y. M., Paul M. and Ganten D. (1998) Lessons from rat models of hypertension: from Goldblatt to genetic engineering. Cardiovasc. Res. 39, 77–88
51. Raizada M. K., Stenstrom B., Phillips M. I. and Sumners C. (1984a) Angiotensin II in neuronal cultures from brains of normotensive and hypertensive rats. Am. J. Physiol. 247, C115–C119
52. Raizada M. K., Muther T. F. and Sumners C. (1984b) Increased angiotensin II receptors in neuronal cultures from hypertensive rat brain. Am. J. Physiol. 247, C364–C372
53. Raizada M. K., Phillips M. I. A. N., Crewst F. T. and Sumners C. (1987) Distinct angiotensin II receptor in primary cultures of glial cells from rat brain. Proc. Natl Acad. Sci. USA 84, 4655–4659
54. Rajagopal K., Whalen E. J., Violin J. D., Stiber J. A., Rosenberg P. B., Premont R. T., Coffman T. M., Rockman H. A. and Lefkowitz R. J. (2006) β-arrestin2-mediated inotropic effects of the angiotensin II type 1A in receptor in isolated cardiac myocytes. Proc. Natl Acad. Sci. USA 103, 16284–16289
55. Raman M., Chen W. and Cobb M. H. (2007) Differential regulation and properties of MAPKs. Oncogene 26, 3100–3112
56. Reid I. A. (1992) Interactions between ANG II, sympathetic nervous system, and baroreflexes in regulation of blood pressure. Am. J. Physiol. 262, E763–E778
57. Ren X.-R., Reiter E., Ahn S., Kim J., Chen W. and Lefkowitz R. J. (2005) Different G protein-coupled receptor kinases govern G protein and β-arrestin-mediated signaling of V2 vasopressin receptor. Proc. Natl Acad. Sci. USA 102, 1448–1453
58. Sakai K., Chapleau M. W., Morimoto S., Cassell M. D. and Sigmund C. D. (2004) Differential modulation of baroreflex control of heart rate by neuron- vs. glia-derived angiotensin II. Physiol. Genomics 20, 66–72
59. Scott M. G. H., Rouzic E., Le Périanin A., Pierotti V., Enslen H., Benichou S., Marullo S. and Benmerah A. (2002) Differential nucleocytoplasmic shuttling of β-arrestins. Characterization of a leucine-rich nuclear export signal in β-arrestin2. J. Biol. Chem. 277, 37693–37701
60. Seyedabadi M., Goodchild A. K. and Pilowsky P. M. (2001) Differential role of kinases in brain stem of hypertensive and normotensive rats. Hypertension 38, 1087–1092
61. Shenoy S. K. and Lefkowitz R. J. (2003) Multifaceted roles of β-arrestins in the regulation of seven-membrane-spanning receptor trafficking and signaling. Biochem. J. 375, 503–515
62. Shenoy S. K., Drake M. T., Nelson C. D., Houtz D. A., Xiao K., Madabushi S., Reiter E., Premont R. T., Lichtarge O. and Lefkowitz R. J. (2006) β-arrestin-dependent, G protein-independent ERK1/2 activation by the β2 adrenergic receptor. J. Biol. Chem. 281, 1261–1273
63. Sherrod M., Davis D. R., Zhou X., Cassell M. D. and Sigmund C. D. (2005). Glial- specific ablation of angiotensinogen lowers arterial pressure in renin and angiotensinogen transgenic mice. Am. J. Physiol. Regul. Integr. Comp. Physiol., 289, R1763–R1769
64. Stern J. E., Son S., Biancardi V. C., Zheng H., Sharma N. and Patel K. P. (2016) Astrocytes contribute to angiotensin II stimulation of hypothalamic neuronal activity and sympathetic outflow. Hypertension 68(6), 1483–1493
65. Stornetta R. L., Hawelu-Johnson C. L., Guyenet P. G. and Lynch K. R. (1988) Astrocytes synthesize angiotensinogen in brain. Science 242, 1444–1446
66. Sun J.-C., Liu B., Zhang R.-W., Jiao P.-L., Tan X., Wang Y.-K. and Wang W.-Z. (2018) Overexpression of ß-Arrestin1 in the rostral ventrolateral medulla downregulates angiotensin receptor and lowers blood pressure in hypertension. Front. Physiol. 9, 297
67. Tallant E. A. and Higson J. T. (1997) Angiotensin II activates distinct signal transduction pathways in astrocytes isolated from neonatal rat brain. Glia 19, 333–342
68. Tallant E. A., Diz D. I. and Ferrario C. M. (1996) Recent advances in cellular and molecular aspects of angiotensin receptors: identification of AT1 receptors on cultured astrocytes. Plenum Press, New York 13, 121–129
69. Thomas W. G. and Sernia C. (1988) Immunocytochemical localization of angiotensinogen in the rat brain. Neuroscience 25, 319–341
70. Tohgo A., Pierce K. L., Choy E. W., Lefkowitz R. J. and Luttrell L. M. (2002) β-arrestin scaffolding of the ERK cascade enhances cytosolic ERK activity but inhibits ERK-mediated transcription following angiotensin AT1a receptor stimulation. J. Biol. Chem. 277, 9429–9436
71. Veerasingham S. J. and Raizada M. K. (2003) Brain renin-angiotensin system dysfunction in hypertension: recent advances and perspectives. Br. J. Pharmacol. 139, 191–202
72. Wang P., Wu Y., Ge X., Ma L. and Pei G. (2003) Subcellular localization of β-arrestins is determined by their intact N domain and the nuclear export signal at the C terminus. J. Biol. Chem. 278, 11648–11653
73. Whalen E. J., Rajagopal S. and Lefkowitz R. J. (2011) Therapeutic potential of β-arrestin- and G protein-biased agonists. Trends Mol. Med. 17, 126–139
74. Wilkie N., Ng L. L. and Boarder M. R. (1997) Angiotensin II responses of vascular smooth muscle cells from hypertensive rats: enhancement at the level of p42 and p44 mitogen activated protein kinase. Br. J. Pharmacol. 122, 209–216
75. Willets J. M., Nash C. A., Rainbow R. D., Nelson C. P. and Challiss R. A. J. (2015) Defining the roles of arrestin2 and arrestin3 in vasoconstrictor receptor desensitization in hypertension. Am. J. Physiol. Cell Physiol. 309, C179–C189
76. Winklewski P. J., Radkowski M., Wszedybyl-Winklewska M. and Demkow U. (2015) Brain inflammation and hypertension: the chicken or the egg? J. Neuroinflammation 12, 85
77. Zhan X., Gimenez L. E., Gurevich V. V. and Spiller B. W. (2011) Crystal structure of arrestin-3 reveals the basis of the difference in receptor binding between two non-visual subtypes. J. Mol. Biol. 406, 467–478
78. Zhang W., Liu H. T. and Tu L. I. U. H. (2002) MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12, 9–18
79. Zhang H., Han G. W., Batyuk A. et al. (2017) Structural basis for selectivity and diversity in angiotensin II receptors. Nature 544, 327–332