Roles of MEK/ERK Pathway in Vascular and Renal Tubular Actions of Angiotensin II

Chronic kidney disease (CKD) is now widely recognized as a significant risk factor for cardiovascular disease (CVD). Chronic angiotensin II (Ang II) stimulation facilitates tissue hyperplasia, hypertrophy, and inflammation, and the current medical strategy for CKD is primarily based on the suppression of rein-angiotensin system. Since Ang II induces hypertension through both vasoconstriction and sodium retention, the understanding of vascular and renal actions of Ang II is essential for the better management of CKD and CVD. Ang II is coupled to a variety of intracellular signaling path- ways depending on cell types, and Ang II type 1 receptor (AT1) is thought to be responsible for most, if not all, of the car- diovascular effects of Ang II. Recent studies have suggested that the MEK/ERK pathway plays an important role in Ang II-mediated vascular smooth muscle contraction, where cytosolic phospholipase A2 (cPLA2)/P450 pathway has a positive feedback effect. Interestingly, the MEK/ERK pathway has been also shown to mediate the stimulatory effect of Ang II on renal proximal transport. However, the cPLA2/P450 pathway has a negative feedback effect on the Ang II-mediated ERK activation in renal proximal tubules. Thus, arachidonic acid metabolites seem to play quite contrasting roles in the Ang II- mediated ERK activation in vascular and renal tissues. This article will be focused on the roles of MEK/ERK pathway in vascular and renal tubular actions of Ang II.

[1]  W. Gonzalez,et al.  Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. , 2000, Arteriosclerosis, thrombosis, and vascular biology.

[2]  A. Danser,et al.  Nongenomic Effects of Aldosterone in the Human Heart: Interaction With Angiotensin II , 2005, Hypertension.

[3]  L. Smeeth,et al.  Effect of inhibitors of the renin-angiotensin system and other antihypertensive drugs on renal outcomes: systematic review and meta-analysis , 2005, The Lancet.

[4]  R. Robey,et al.  A central role for Pyk2-Src interaction in coupling diverse stimuli to increased epithelial NBC activity. , 2002, American journal of physiology. Renal physiology.

[5]  C T Wang,et al.  Concentrations and actions of intraluminal angiotensin II. , 1999, Journal of the American Society of Nephrology : JASN.

[6]  Takao Shimizu,et al.  Regulatory mechanism and physiological role of cytosolic phospholipase A2. , 2004, Biological & pharmaceutical bulletin.

[7]  P. Houillier,et al.  Signaling pathways in the biphasic effect of angiotensin II on apical Na/H antiport activity in proximal tubule. , 1996, Kidney international.

[8]  C. Chang,et al.  Role of phospholipase A2 isozymes in agonist-mediated signaling in proximal tubular epithelium. , 1998, Hypertension.

[9]  M. Romero,et al.  An epoxygenase metabolite of arachidonic acid 5,6 epoxy-eicosatrienoic acid mediates angiotensin-induced natriuresis in proximal tubular epithelium. , 1991, Advances in prostaglandin, thromboxane, and leukotriene research.

[10]  S. Eguchi,et al.  Identification of an Essential Signaling Cascade for Mitogen-activated Protein Kinase Activation by Angiotensin II in Cultured Rat Vascular Smooth Muscle Cells , 1996, The Journal of Biological Chemistry.

[11]  H. Jacobson,et al.  Angiotensin II directly stimulates sodium transport in rabbit proximal convoluted tubules. , 1984, The Journal of clinical investigation.

[12]  M. Wellner,et al.  A peroxisome proliferator-activated receptor-alpha activator induces renal CYP2C23 activity and protects from angiotensin II-induced renal injury. , 2004, The American journal of pathology.

[13]  B. Andresen,et al.  Angiotensin II Activates Extracellular Signal-Regulated Kinase Independently of Receptor Tyrosine Kinases in Renal Smooth Muscle Cells: Implications for Blood Pressure Regulation , 2008, Journal of Pharmacology and Experimental Therapeutics.

[14]  P. Harris,et al.  Dose-dependent stimulation and inhibition of proximal tubular sodium reabsorption by angiotensin II in the rat kidney , 1977, Pflügers Archiv.

[15]  S. Alper Genetic diseases of acid-base transporters. , 2002, Annual review of physiology.

[16]  A. Clerk,et al.  Regulation of the ERK subgroup of MAP kinase cascades through G protein-coupled receptors. , 1997, Cellular signalling.

[17]  M. Peach,et al.  Angiotensin II Induces Hypertrophy, not Hyperplasia, of Cultured Rat Aortic Smooth Muscle Cells , 1988, Circulation research.

[18]  S. Ball,et al.  Comparative pharmacology of recombinant rat AT1A, AT1B and human AT1 receptors expressed by transfected COS‐M6 cells , 1994, British journal of pharmacology.

[19]  R. Alexander,et al.  Angiotensin II receptor coupling to phospholipase D is mediated by the betagamma subunits of heterotrimeric G proteins in vascular smooth muscle cells. , 1999, Molecular pharmacology.

[20]  J. Zhuo,et al.  Localization of angiotensin AT1 and AT2 receptors. , 1999, Journal of the American Society of Nephrology : JASN.

[21]  T. Sugaya,et al.  Biphasic Regulation of Na+-HCO3− Cotransporter by Angiotensin II Type 1A Receptor , 2002, Hypertension.

[22]  K. Griendling,et al.  Angiotensin II cell signaling: physiological and pathological effects in the cardiovascular system. , 2007, American journal of physiology. Cell physiology.

[23]  A. A. Spector,et al.  Action of epoxyeicosatrienoic acids on cellular function. , 2007, American journal of physiology. Cell physiology.

[24]  R. Alexander,et al.  Temporal dispersion of activation of phospholipase C-beta1 and -gamma isoforms by angiotensin II in vascular smooth muscle cells. Role of alphaq/11, alpha12, and beta gamma G protein subunits. , 1998, The Journal of biological chemistry.

[25]  R. Bain,et al.  The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. , 1993 .

[26]  B. Hogan,et al.  Effects on blood pressure and exploratory behaviour of mice lacking angiotensin II type-2 receptor , 1995, Nature.

[27]  L. Tankó,et al.  Involvement of Rho-Kinase and the Actin Filament Network in Angiotensin II–Induced Contraction and Extracellular Signal–Regulated Kinase Activity in Intact Rat Mesenteric Resistance Arteries , 2001, Arteriosclerosis, thrombosis, and vascular biology.

[28]  D. Harrison,et al.  Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. , 1996, The Journal of clinical investigation.

[29]  Hyung-Suk Kim,et al.  Distinct roles for the kidney and systemic tissues in blood pressure regulation by the renin-angiotensin system. , 2005, The Journal of clinical investigation.

[30]  G. Wolf,et al.  Reactive oxygen species stimulate p44/42 mitogen-activated protein kinase and induce p27(Kip1): role in angiotensin II-mediated hypertrophy of proximal tubular cells. , 2000, Journal of the American Society of Nephrology : JASN.

[31]  E. Schiffrin,et al.  Role of extracellular signal-regulated kinases in angiotensin II-stimulated contraction of smooth muscle cells from human resistance arteries. , 1999, Circulation.

[32]  M. Weir,et al.  Effects of renin-angiotensin system inhibition on end-organ protection: can we do better? , 2007, Clinical therapeutics.

[33]  T. Sugaya,et al.  Biphasic regulation of renal proximal bicarbonate absorption by luminal AT(1A) receptor. , 2003, Journal of the American Society of Nephrology : JASN.

[34]  H. Nishimura,et al.  Targeting deletion of angiotensin type 1B receptor gene in the mouse. , 1997, The American journal of physiology.

[35]  R. Alexander,et al.  Angiotensin receptors and their therapeutic implications. , 1996, Annual review of pharmacology and toxicology.

[36]  M. Waterman,et al.  Salt-sensitive hypertension is associated with dysfunctional Cyp4a10 gene and kidney epithelial sodium channel. , 2006, The Journal of clinical investigation.

[37]  R. Carey,et al.  Newly recognized components of the renin-angiotensin system: potential roles in cardiovascular and renal regulation. , 2003, Endocrine reviews.

[38]  O. Moe,et al.  Role of c-SRC and ERK in acid-induced activation of NHE3. , 2002, Kidney international.

[39]  L. Adam,et al.  Inhibition of ERK attenuates force development by lowering myosin light chain phosphorylation. , 2002, American journal of physiology. Heart and circulatory physiology.

[40]  R. Wetzker,et al.  Transactivation joins multiple tracks to the ERK/MAPK cascade , 2003, Nature Reviews Molecular Cell Biology.

[41]  M. Taub,et al.  Mechanism of regulation of Na+ transport by angiotensin II in primary renal cells. , 2000, Kidney international.

[42]  IsseiKomuro,et al.  Rho Family Small G Proteins Play Critical Roles in Mechanical Stress–Induced Hypertrophic Responses in Cardiac Myocytes , 1999 .

[43]  M. Wellner,et al.  A peroxisome proliferator-activated receptor-alpha activator induces renal CYP2C23 activity and protects from angiotensin II-induced renal injury. , 2004, The American journal of pathology.

[44]  R. Alexander,et al.  Temporal Dispersion of Activation of Phospholipase C-β1 and -γ Isoforms by Angiotensin II in Vascular Smooth Muscle Cells , 1998, The Journal of Biological Chemistry.

[45]  K. Malik,et al.  20-Hydroxyeicosatetraenoic acid mediates calcium/calmodulin-dependent protein kinase II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[46]  M. G. Cogan,et al.  Angiotensin II stimulates early proximal bicarbonate absorption in the rat by decreasing cyclic adenosine monophosphate. , 1989, The Journal of clinical investigation.

[47]  R. Alexander,et al.  Reactive Oxygen Species Mediate the Activation of Akt/Protein Kinase B by Angiotensin II in Vascular Smooth Muscle Cells* , 1999, The Journal of Biological Chemistry.

[48]  H. Endou Distribution and some characteristics of cytochrome P-450 in the kidney. , 1983, The Journal of toxicological sciences.

[49]  M. Soleimani,et al.  Physiologic and molecular aspects of the Na+:HCO3- cotransporter in health and disease processes. , 2000, Kidney international.

[50]  M. Waterman,et al.  Functional Variant of CYP4A11 20-Hydroxyeicosatetraenoic Acid Synthase Is Associated With Essential Hypertension , 2005, Circulation.

[51]  Takao Shimizu,et al.  Roles of ERK and cPLA2 in the angiotensin II-mediated biphasic regulation of Na+-HCO3(-) transport. , 2008, Journal of the American Society of Nephrology : JASN.

[52]  P. Ortiz de Montellano,et al.  Inhibitors of cytochrome P-450 attenuate the myogenic response of dog renal arcuate arteries. , 1991, Circulation research.

[53]  J. Imig Epoxide hydrolase and epoxygenase metabolites as therapeutic targets for renal diseases. , 2005, American journal of physiology. Renal physiology.

[54]  R. Bain,et al.  The effect of angiotensin-converting-enzyme inhibition on diabetic nephropathy. The Collaborative Study Group. , 1993, The New England journal of medicine.

[55]  J. Falck,et al.  Cytochrome P450 and arachidonic acid bioactivation. Molecular and functional properties of the arachidonate monooxygenase. , 2000, Journal of lipid research.

[56]  Teven,et al.  EFFECTS OF LOSARTAN ON RENAL AND CARDIOVASCULAR OUTCOMES IN TYPE 2 DIABETES AND NEPHROPATHY EFFECTS OF LOSARTAN ON RENAL AND CARDIOVASCULAR OUTCOMES IN PATIENTS WITH TYPE 2 DIABETES AND NEPHROPATHY , 2001 .

[57]  J. Bauer,et al.  Combined Effects of Low-dose Oral Spironolactone and Captopril Therapy in a Rat Model of Spontaneous Hypertension and Heart Failure , 2003, Journal of cardiovascular pharmacology.

[58]  R. Roman,et al.  Formation and action of a P-450 4A metabolite of arachidonic acid in cat cerebral microvessels. , 1994, The American journal of physiology.

[59]  R. Alexander,et al.  Vascular smooth muscle Na+-H+ exchanger kinetics and its activation by angiotensin II. , 1988, The American journal of physiology.

[60]  C. Liebmann,et al.  Regulation of MAP kinase activity by peptide receptor signalling pathway: paradigms of multiplicity. , 2001, Cellular signalling.

[61]  P. Graceffa,et al.  Mammal-specific, ERK-dependent, Caldesmon Phosphorylation in Smooth Muscle , 1999, The Journal of Biological Chemistry.

[62]  W. Boron,et al.  Role of endogenously secreted angiotensin II in the CO2-induced stimulation of HCO3 reabsorption by renal proximal tubules. , 2008, American journal of physiology. Renal physiology.

[63]  N. Dulin,et al.  Phospholipase A2-mediated activation of mitogen-activated protein kinase by angiotensin II. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[64]  S. Eguchi,et al.  Redox-dependent protein kinase regulation by angiotensin II: mechanistic insights and its pathophysiology. , 2005, Antioxidants & redox signaling.

[65]  V. Cachofeiro,et al.  Insulin resistance, inflammatory biomarkers, and adipokines in patients with chronic kidney disease: effects of angiotensin II blockade. , 2006, Journal of the American Society of Nephrology : JASN.

[66]  P. Timmermans,et al.  Angiotensin II receptors and angiotensin II receptor antagonists. , 1993, Pharmacological reviews.

[67]  E. Schiffrin,et al.  Mitogen-activated protein/extracellular signal-regulated kinase inhibition attenuates angiotensin II-mediated signaling and contraction in spontaneously hypertensive rat vascular smooth muscle cells. , 1999, Circulation research.

[68]  M. Berridge,et al.  Spatial and temporal signalling by calcium. , 1994, Current opinion in cell biology.

[69]  E. Frömter,et al.  An electrophysiological study of angiotensin II regulation of Na-HCO3 cotransport and K conductance in renal proximal tubules , 1994, Pflügers Archiv.

[70]  A. Hall,et al.  Small GTP-binding proteins and the regulation of the actin cytoskeleton. , 1994, Annual review of cell biology.

[71]  Jian-Mei Li,et al.  Aldosterone and Angiotensin II Synergistically Induce Mitogenic Response in Vascular Smooth Muscle Cells , 2005, Circulation research.

[72]  M. Waterman,et al.  Alterations in the regulation of androgen-sensitive Cyp 4a monooxygenases cause hypertension , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[73]  G. Wolf,et al.  Reactive Oxygen Species Stimulate p44/42 Mitogen-Activated Protein Kinase and Induce p27Kip1 Role in Angiotensin II-Mediated Hypertrophy of Proximal Tubular Cells , 2000 .

[74]  H. Gröne,et al.  Autoradiographic characterization of angiotensin receptor subtypes in fetal and adult human kidney. , 1992, The American journal of physiology.

[75]  J. Douglas,et al.  Renal proximal tubular AT2 receptor: signaling and transport. , 1999, Journal of the American Society of Nephrology : JASN.

[76]  A. Strosberg,et al.  Angiotensin II type 2 receptors mediate inhibition of mitogen-activated protein kinase cascade and functional activation of SHP-1 tyrosine phosphatase. , 1997, The Biochemical journal.

[77]  Phillip Ruiz,et al.  Angiotensin II causes hypertension and cardiac hypertrophy through its receptors in the kidney , 2006, Proceedings of the National Academy of Sciences.

[78]  R Clinton Webb,et al.  Smooth muscle contraction and relaxation. , 2003, Advances in physiology education.

[79]  D. Guo,et al.  Molecular biology of angiotensin II receptors: an overview. , 1994, Journal of hypertension. Supplement : official journal of the International Society of Hypertension.

[80]  W. Boron,et al.  Angiotensin II stimulates both Na(+)-H+ exchange and Na+/HCO3- cotransport in the rabbit proximal tubule. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[81]  R. Roman,et al.  P-450 metabolites of arachidonic acid in the control of cardiovascular function. , 2002, Physiological reviews.

[82]  A. Garg,et al.  Review: the renoprotective effects of ACE inhibitors and ARBs independent of blood pressure control are uncertain , 2006, Evidence-based medicine.

[83]  E. Fleck,et al.  Central role of the MAPK pathway in ang II-mediated DNA synthesis and migration in rat vascular smooth muscle cells. , 1999, Arteriosclerosis, thrombosis, and vascular biology.

[84]  C. Ferrario Role of Angiotensin II in Cardiovascular Disease — Therapeutic Implications of More Than a Century of Research , 2006, Journal of the renin-angiotensin-aldosterone system : JRAAS.

[85]  Wuding Zhou,et al.  Apical proteins stimulate complement synthesis by cultured human proximal tubular epithelial cells. , 1999, Journal of the American Society of Nephrology : JASN.

[86]  D. Sorescu,et al.  NAD(P)H oxidase: role in cardiovascular biology and disease. , 2000, Circulation research.