AKAP150 contributes to enhanced vascular tone by facilitating large-conductance Ca2+-activated K+ channel remodeling in hyperglycemia and diabetes mellitus

Circulation Research

Volumn 114, Issue 4, 2014, Pages 607-615

  Nystoriak, Matthew A ^a   Nieves Cintrón, Madeline ^a   Nygren, Patrick J ^c   Hinke, Simon A ^c   Nichols, C Blake ^a   Chen, Chao Yin ^a   Puglisi, Jose L ^a   Izu, Leighton T ^a   Bers, Donald M ^a   Dell'acqua, Mark L ^b   Scott, John D ^c   Santana, Luis F ^d   Navedo, Manuel F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

calcineurin; hyperglycemia; hypertension; ion channels; potassium channels

Indexed keywords

CALCINEURIN; HYPERGLYCEMIA; HYPERTENSION; ION CHANNELS; POTASSIUM CHANNELS;

A KINASE ANCHOR PROTEINS; ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIETARY FATS; GENE KNOCK-IN TECHNIQUES; HYPERGLYCEMIA; HYPERTENSION; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNEL BETA SUBUNITS; LARGE-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MUSCLE, SMOOTH, VASCULAR; NFATC TRANSCRIPTION FACTORS; PEPTIDES; SIGNAL TRANSDUCTION; TOXINS, BIOLOGICAL; VASOCONSTRICTION;

EID: 84894480266     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.302168     Document Type: Article

References (41)

1. National high blood pressure education program working group report on hypertension in diabetes. Hypertension. 1994;23:145-158; discussion 159-160
2. Barbagallo M, Shan J, Pang PK, Resnick LM. Glucose-induced alterations of cytosolic free calcium in cultured rat tail artery vascular smooth muscle cells. J Clin Invest. 1995;95:763-767
3. Ungvari Z, Pacher P, Kecskemeti V, Papp G, Szollár L, Koller A. Increased myogenic tone in skeletal muscle arterioles of diabetic rats. Possible role of increased activity of smooth muscle Ca2+ channels and protein kinase C. Cardiovasc Res. 1999;43:1018-1028
4. Navedo MF, Amberg GC, Votaw VS, Santana LF. Constitutively active L-Type Ca2+ channels. Proc Natl Acad Sci U S A. 2005;102:11112-11117
5. Navedo MF, Takeda Y, Nieves-Cintrón M, Molkentin JD, Santana LF. Elevated Ca2+ sparklet activity during acute hyperglycemia and diabetes in cerebral arterial smooth muscle cells. Am J Physiol Cell Physiol. 2010;298:C211-C220
6. Nieves-Cintrón M, Amberg GC, Navedo MF, Molkentin JD, Santana LF. The control of Ca2+ influx and NFATc3 signaling in arterial smooth muscle during hypertension. Proc Natl Acad Sci U S A. 2008;105:15623-15628
7. Gomez MF, Stevenson AS, Bonev AD, Hill-Eubanks DC, Nelson MT. Opposing actions of inositol 1,4,5-Trisphosphate and ryanodine receptors on nuclear factor of activated T-cells regulation in smooth muscle. J Biol Chem. 2002;277:37756-37764
8. Gao T, Yatani A, Dell'Acqua ML, Sako H, Green SA, Dascal N, Scott JD, Hosey MM. cAMP-dependent regulation of cardiac L-Type Ca2+ channels requires membrane targeting of PKA and phosphorylation of channel subunits. Neuron. 1997;19:185-196
9. Oliveria SF, Dell'Acqua ML, Sather WA. AKAP79/150 anchoring of calcineurin controls neuronal L-Type Ca2+ channel activity and nuclear signaling. Neuron. 2007;55:261-275
10. Li H, Pink MD, Murphy JG, Stein A, Dell'Acqua ML, Hogan PG. Balanced interactions of calcineurin with AKAP79 regulate Ca2+-calcineurin-NFAT signaling. Nat Struct Mol Biol. 2012;19:337-345
11. Amberg GC, Rossow CF, Navedo MF, Santana LF. NFATc3 regulates Kv2.1 expression in arterial smooth muscle. J Biol Chem. 2004;279:47326-47334
12. Nieves-Cintrón M, Amberg GC, Nichols CB, Molkentin JD, Santana LF. Activation of NFATc3 down-regulates the beta1 subunit of large conductance, calcium-Activated K+ channels in arterial smooth muscle and contributes to hypertension. J Biol Chem. 2007;282:3231-3240
13. Nelson MT, Patlak JB, Worley JF, Standen NB. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol. 1990;259:C3-C18
14. Tanaka Y, Meera P, Song M, Knaus HG, Toro L. Molecular constituents of maxi KCa channels in human coronary smooth muscle: Predominant alpha+ beta subunit complexes. J Physiol. 1997;502(Pt 3):545-557
15. Brenner R, Peréz GJ, Bonev AD, Eckman DM, Kosek JC, Wiler SW, Patterson AJ, Nelson MT, Aldrich RW. Vasoregulation by the beta1 subunit of the calcium-Activated potassium channel. Nature. 2000;407:870-876
16. Sanderson JL, Gorski JA, Gibson ES, Lam P, Freund RK, Chick WS, Dell'Acqua ML. AKAP150-Anchored calcineurin regulates synaptic plasticity by limiting synaptic incorporation of Ca2+-permeable AMPA receptors. J Neurosci. 2012;32:15036-15052
17. Surwit RS, Kuhn CM, Cochrane C, McCubbin JA, Feinglos MN. Dietinduced type II diabetes in C57BL/6J mice. Diabetes. 1988;37:1163-1167
18. Winzell MS, Ahrén B. The high-fat diet-fed mouse: A model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes. 2004;53(Suppl 3):S215-S219
19. Knot HJ, Nelson MT. Regulation of arterial diameter and wall [Ca2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol. 1998;508(Pt 1):199-209
20. Jaggar JH, Porter VA, Lederer WJ, Nelson MT. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol. 2000;278:C235-C256
21. Dick GM, Sanders KM. (Xeno)estrogen sensitivity of smooth muscle BK channels conferred by the regulatory beta1 subunit: A study of beta1 knockout mice. J Biol Chem. 2001;276:44835-44840
22. Dell'Acqua ML, Dodge KL, Tavalin SJ, Scott JD. Mapping the protein phosphatase-2B anchoring site on AKAP79. Binding and inhibition of phosphatase activity are mediated by residues 315-360. J Biol Chem. 2002;277:48796-48802
23. Okamura H, Aramburu J, García-Rodríguez C, Viola JP, Raghavan A, Tahiliani M, Zhang X, Qin J, Hogan PG, Rao A. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol Cell. 2000;6:539-550
24. Rahmouni K, Morgan DA, Morgan GM, Mark AL, Haynes WG. Role of selective leptin resistance in diet-induced obesity hypertension. Diabetes. 2005;54:2012-2018
25. Mills E, Kuhn CM, Feinglos MN, Surwit R. Hypertension in CB57BL/6J mouse model of non-insulin-dependent diabetes mellitus. Am J Physiol. 1993;264:R73-R78
26. Hinke SA, Navedo MF, Ulman A, Whiting JL, Nygren PJ, Tian G, Jimenez-Caliani AJ, Langeberg LK, Cirulli V, Tengholm A, Dell'Acqua ML, Santana LF, Scott JD. Anchored phosphatases modulate glucose homeostasis. EMBO J. 2012;31:3991-4004
27. Tunquist BJ, Hoshi N, Guire ES, Zhang F, Mullendorff K, Langeberg LK, Raber J, Scott JD. Loss of AKAP150 perturbs distinct neuronal processes in mice. Proc Natl Acad Sci U S A. 2008;105:12557-12562
28. Navedo MF, Amberg GC, Nieves M, Molkentin JD, Santana LF. Mechanisms underlying heterogeneous Ca2+ sparklet activity in arterial smooth muscle. J Gen Physiol. 2006;127:611-622
29. Navedo MF, Nieves-Cintrón M, Amberg GC, Yuan C, Votaw VS, Lederer WJ, McKnight GS, Santana LF. AKAP150 is required for stuttering persistent Ca2+ sparklets and angiotensin II-induced hypertension. Circ Res. 2008;102:e1-e11
30. Nilsson J, Nilsson LM, Chen YW, Molkentin JD, Erlinge D, Gomez MF. High glucose activates nuclear factor of activated T cells in native vascular smooth muscle. Arterioscler Thromb Vasc Biol. 2006;26:794-800
31. Gomez MF, Bosc LV, Stevenson AS, Wilkerson MK, Hill-Eubanks DC, Nelson MT. Constitutively elevated nuclear export activity opposes Ca2+-dependent NFATc3 nuclear accumulation in vascular smooth muscle: Role of JNK2 and Crm-1. J Biol Chem. 2003;278:46847-46853
32. de Frutos S, Caldwell E, Nitta CH, Kanagy NL, Wang J, Wang W, Walker MK, Gonzalez Bosc LV. NFATc3 contributes to intermittent hypoxia-induced arterial remodeling in mice. Am J Physiol Heart Circ Physiol. 2010;299:H356-H363
33. Kim F, Pham M, Maloney E, Rizzo NO, Morton GJ, Wisse BE, Kirk EA, Chait A, Schwartz MW. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol. 2008;28:1982-1988
34. Nilsson-Berglund LM, Zetterqvist AV, Nilsson-Ohman J, Sigvardsson M, González Bosc LV, Smith ML, Salehi A, Agardh E, Fredrikson GN, Agardh CD, Nilsson J, Wamhoff BR, Hultgårdh-Nilsson A, Gomez MF. Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetes-induced hyperglycemia. Arterioscler Thromb Vasc Biol. 2010;30:218-224
35. Lu T, Zhang DM, Wang XL, He T, Wang RX, Chai Q, Katusic ZS, Lee HC. Regulation of coronary arterial BK channels by caveolae-mediated angiotensin II signaling in diabetes mellitus. Circ Res. 2010;106:1164-1173
36. Zhang DM, He T, Katusic ZS, Lee HC, Lu T. Muscle-specific f-box only proteins facilitate bk channel β(1) subunit downregulation in vascular smooth muscle cells of diabetes mellitus. Circ Res. 2010;107:1454-1459
37. Lu T, Chai Q, Yu L, d'Uscio LV, Katusic ZS, He T, Lee HC. Reactive oxygen species signaling facilitates FOXO-3a/FBXO-dependent vascular BK channel β1 subunit degradation in diabetic mice. Diabetes. 2012;61:1860-1868
38. Lamb FS, Webb RC. Cyclosporine augments reactivity of isolated blood vessels. Life Sci. 1987;40:2571-2578
39. Robert N, Wong GW, Wright JM. Effect of cyclosporine on blood pressure. Cochrane Database Syst Rev. 2010:CD007893
40. Lyson T, McMullan DM, Ermel LD, Morgan BJ, Victor RG. Mechanism of cyclosporine-induced sympathetic activation and acute hypertension in rats. Hypertension. 1994;23:667-675
41. Zhang W, Li JL, Hosaka M, Janz R, Shelton JM, Albright GM, Richardson JA, Südhof TC, Victor RG. Cyclosporine A-induced hypertension involves synapsin in renal sensory nerve endings. Proc Natl Acad Sci U S A. 2000;97:9765-9770