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Mechanotransduction and the Myogenic Response in Diabetes

  • Sewon Lee
  • Srijita Dhar
  • Kwangseok Hong
  • Yan Yang
  • Michael A. HillEmail author
Chapter
  • 1k Downloads
Part of the Studies in Mechanobiology, Tissue Engineering and Biomaterials book series (SMTEB, volume 16)

Abstract

Tissues of the body possess intrinsic control mechanisms for regulating hemodynamics at the local level. These mechanisms largely occur independently of innervation and circulating factors and allow blood flow to be matched to local metabolic requirements. In the case of the myogenic response, or pressure-induced vasoconstriction, this mechanism is dependent on the cells of the vessel wall detecting and responding to a mechanical stimulus. This mechanical event then must be conveyed across the smooth muscle cell membrane to the contractile proteins to affect an appropriate contractile response. Diabetes and related metabolic disorders that lead to hyperglycemia may interfere with this process by either alterations to the vessel wall (for example, remodeling events, increased stiffness, decreased distensibility) or impairment of signal transduction mechanisms (including ion channel function, Ca2+ handling and contractile protein interactions). This chapter reviews the cellular mechanisms underlying myogenic contraction and how these may be altered in hyperglycemic states.

Keywords

Intraluminal Pressure BKCa Channel Amadori Product Myogenic Response Myogenic Tone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AGE

Advanced glycation endproducts

AT1R

Angiotensin II type 1 receptor

DAG

Diacylglycerol

ECM

Extracellular matrix

EM

Membrane potential

GK

Goto-Kakizaki

GPCRs

G-protein coupled receptors

MLCK

Myosin light chain kinase

MYPT1

Myosin targeting subunit of myosin phosphatase

NSCCs

Non-selective cation channels

OZR

Obese zucker rat

PKC

Protein kinase C

RAGE

Receptor for advanced glycation endproducts

ROS

Reactive oxygen species

S-1-P

Sphingosine-1-phosphate

SACs

Stretch-activated channels

SD

Sprague dawley

SK

Src kinase

SR

Sarcoplasmic reticulum

STZ

Streptozotocin

TK

Tyrosine kinase

Trp

Transient receptor potential

VGCCs

Voltage-gated Ca2+ channels

VSM

Vascular smooth muscle

VSMC

Vascular smooth muscle cells

Notes

Acknowledgments

Aspects of work presented in this chapter were supported by NIH grants (HL085119 and HL092241) to MAH.

References

  1. 1.
    Clifford PS (2011) Local control of blood flow. Adv Physiol Educ 35:5–15Google Scholar
  2. 2.
    Davis MJ, Hill MA (1999) Signaling mechanisms underlying the vascular myogenic response. Physiol Rev 79:387–423Google Scholar
  3. 3.
    Davis MJ, Hill MA, Kuo L (2008) Local regulation of microvascular perfusion. In: Tuma RF, Duran WN, Ley K (eds) Handbook of physiology. Microcirculation. Academic, San DiegoGoogle Scholar
  4. 4.
    Meininger GA, Faber JE (1991) Adrenergic facilitation of myogenic response in skeletal muscle arterioles. Am J Physiol 260:H1424–H1432Google Scholar
  5. 5.
    Meininger GA, Trzeciakowski JP (1990) Combined effects of autoregulation and vasoconstrictors on hindquarters vascular resistance. Am J Physiol 258:H1032–H1041Google Scholar
  6. 6.
    The diabetes control and complications trial research group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977–986Google Scholar
  7. 7.
    UK prospective diabetes study group (1998) Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. BMJ 317:703–713Google Scholar
  8. 8.
    Hill MA, Meininger GA, Davis MJ, Laher I (2009) Therapeutic potential of pharmacologically targeting arteriolar myogenic tone. Trends Pharmacol Sci 30:363–374Google Scholar
  9. 9.
    Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414:813–820Google Scholar
  10. 10.
    Brownlee M (2005) The pathobiology of diabetic complications: a unifying mechanism. Diabetes 54:1615–1625Google Scholar
  11. 11.
    Kilpatrick ES, Rigby AS, Atkin SL (2009) The diabetes control and complications trial: the gift that keeps giving. Nat Rev Endocrinol 5:537–545Google Scholar
  12. 12.
    Schalkwijk CG, Stehouwer CD (2005) Vascular complications in diabetes mellitus: the role of endothelial dysfunction. Clin Sci (Lond) 109:143–159Google Scholar
  13. 13.
    Stolar M (2010) Glycemic control and complications in type 2 diabetes mellitus. Am J Med 123:S3–S11Google Scholar
  14. 14.
    Kuo L, Chilian WM, Davis MJ (1991) Interaction of pressure- and flow-induced responses in porcine coronary resistance vessels. Am J Physiol 261:H1706–H1715Google Scholar
  15. 15.
    Falcone JC, Davis MJ, Meininger GA (1991) Endothelial independence of myogenic response in isolated skeletal muscle arterioles. Am J Physiol 260:H130–H135Google Scholar
  16. 16.
    Kuo L, Chilian WM, Davis MJ (1990) Coronary arteriolar myogenic response is independent of endothelium. Circ Res 66:860–866Google Scholar
  17. 17.
    McCarron JG, Osol G, Halpern W (1989) Myogenic responses are independent of the endothelium in rat pressurized posterior cerebral arteries. Blood Vessels 26:315–319Google Scholar
  18. 18.
    Hill MA, Meininger GA (2012) Arteriolar vascular smooth muscle cells: mechanotransducers in a complex environment. Int J Biochem Cell Biol 44:1505–1510Google Scholar
  19. 19.
    Kauffenstein G, Laher I, Matroughi K, Guerineau NC, Henrion D (2012) Emerging role of G-protein coupled receptors in microvascular myogenic tone. Cardiovasc Res 95:223–232Google Scholar
  20. 20.
    Storch U, Mederos y Schnitzler M, Gudermann T (2012) G protein-mediated stretch reception. Am J Physiol Heart Circ Physiol 302:H1241–H1249Google Scholar
  21. 21.
    Harder DR (1984) Pressure-dependent membrane depolarization in cat middle cerebral artery. Circ Res 55:197–202Google Scholar
  22. 22.
    Knot HJ, Nelson MT (1998) Regulation of arterial diameter and wall [ca2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol 508(Pt 1):199–209Google Scholar
  23. 23.
    Zou H, Ratz PH, Hill MA (1995) Role of myosin phosphorylation and [ca2+]i in myogenic reactivity and arteriolar tone. Am J Physiol 269:H1590–H1596Google Scholar
  24. 24.
    Knot HJ, Nelson MT (1995) Regulation of membrane potential and diameter by voltage-dependent k+ channels in rabbit myogenic cerebral arteries. Am J Physiol 269:H348–H355Google Scholar
  25. 25.
    Kotecha N, Hill MA (2005) Myogenic contraction in rat skeletal muscle arterioles: smooth muscle membrane potential and ca(2+) signaling. Am J Physiol Heart Circ Physiol 289:H1326–H1334Google Scholar
  26. 26.
    Wolfle SE, Schmidt VJ, Hoepfl B, Gebert A, Alcolea S, Gros D, de Wit C (2007) Connexin45 cannot replace the function of connexin40 in conducting endothelium-dependent dilations along arterioles. Circ Res 101:1292–1299Google Scholar
  27. 27.
    Welsh DG, Nelson MT, Eckman DM, Brayden JE (2000) Swelling-activated cation channels mediate depolarization of rat cerebrovascular smooth muscle by hyposmolarity and intravascular pressure. J Physiol 527(Pt 1):139–148Google Scholar
  28. 28.
    Davis MJ, Donovitz JA, Hood JD (1992) Stretch-activated single-channel and whole cell currents in vascular smooth muscle cells. Am J Physiol 262:C1083–C1088Google Scholar
  29. 29.
    McCarron JG, Crichton CA, Langton PD, MacKenzie A, Smith GL (1997) Myogenic contraction by modulation of voltage-dependent calcium currents in isolated rat cerebral arteries. J Physiol 498(Pt 2):371–379Google Scholar
  30. 30.
    Wu X, Davis GE, Meininger GA, Wilson E, Davis MJ (2001) Regulation of the l-type calcium channel by alpha 5beta 1 integrin requires signaling between focal adhesion proteins. J Biol Chem 276:30285–30292Google Scholar
  31. 31.
    Gui P, Chao JT, Wu X, Yang Y, Davis GE, Davis MJ (2010) Coordinated regulation of vascular ca2+ and k+ channels by integrin signaling. Adv Exp Med Biol 674:69–79Google Scholar
  32. 32.
    Wu X, Davis MJ (2001) Characterization of stretch-activated cation current in coronary smooth muscle cells. Am J Physiol Heart Circ Physiol 280:H1751–H1761Google Scholar
  33. 33.
    Clapham DE, Runnels LW, Strubing C (2001) The trp ion channel family. Nat Rev Neurosci 2:387–396Google Scholar
  34. 34.
    Earley S, Brayden JE (2010) Transient receptor potential channels and vascular function. Clin Sci (Lond) 119:19–36Google Scholar
  35. 35.
    Earley S, Gonzales AL (2010) (Sub) family feud: crosstalk between trpc channels in vascular smooth muscle cells during vasoconstrictor agonist stimulation. J Physiol 588:3637–3638Google Scholar
  36. 36.
    Shi J, Ju M, Saleh SN, Albert AP, Large WA (2010) Trp c6 channels stimulated by angiotensin II are inhibited by trp c1/c5 channel activity through a ca2+- and pkc-dependent mechanism in native vascular myocytes. J Physiol 588:3671–3682Google Scholar
  37. 37.
    Reading SA, Brayden JE (2007) Central role of trpm4 channels in cerebral blood flow regulation. Stroke 38:2322–2328Google Scholar
  38. 38.
    Dietrich A, Mederos YSM, Gollasch M, Gross V, Storch U, Dubrovska G, Obst M, Yildirim E, Salanova B, Kalwa H, Essin K, Pinkenburg O, Luft FC, Gudermann T, Birnbaumer L (2005) Increased vascular smooth muscle contractility in trp c6-/- mice. Mol Cell Biol 25:6980–6989Google Scholar
  39. 39.
    Reading SA, Earley S, Waldron BJ, Welsh DG, Brayden JE (2005) Trpc3 mediates pyrimidine receptor-induced depolarization of cerebral arteries. Am J Physiol Heart Circ Physiol 288:H2055–H2061Google Scholar
  40. 40.
    Gottlieb P, Folgering J, Maroto R, Raso A, Wood TG, Kurosky A, Bowman C, Bichet D, Patel A, Sachs F, Martinac B, Hamill OP, Honore E (2008) Revisiting trpc1 and trpc6 mechanosensitivity. Pflugers Arch 455:1097–1103Google Scholar
  41. 41.
    Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) Trpc1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185Google Scholar
  42. 42.
    Dietrich A, Kalwa H, Storch U, Mederos y Schnitzler M, Salanova B, Pinkenberg O, Dubrovska G, Essin K, Gollasch M, Birnbaumer L, Gudermann T (2007) Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of trpc1. Pflugers Arch 455:465–477Google Scholar
  43. 43.
    Vogel V (2006) Mechanotransduction involving multimodular proteins: converting force into biochemical signals. Annu Rev Biophys Biomol Struct 35:459–488Google Scholar
  44. 44.
    Qian F, Wei W, Germino G, Oberhauser A (2005) The nanomechanics of polycystin-1 extracellular region. J Biol Chem 280:40723–40730Google Scholar
  45. 45.
    Narayanan D, Bulley S, Leo MD, Burris SK, Gabrick KS, Boop FA, Jaggar JH (2013) Smooth muscle cell transient receptor potential polycystin-2 (TRPP2) channels contribute to the myogenic response in cerebral arteries. J Physiol 591:5031--5046Google Scholar
  46. 46.
    Johnson PC (1986) Autoregulation of blood flow. Circ Res 59:483–495Google Scholar
  47. 47.
    Qian Q, Hunter LW, Li M, Marin-Padilla M, Prakash YS, Somlo S, Harris PC, Torres VE, Sieck GC (2003) Pkd2 haploinsufficiency alters intracellular calcium regulation in vascular smooth muscle cells. Hum Mol Genet 12:1875–1880Google Scholar
  48. 48.
    Qian Q, Hunter LW, Du H, Ren Q, Han Y, Sieck GC (2007) Pkd2+/− vascular smooth muscles develop exaggerated vasocontraction in response to phenylephrine stimulation. J Am Soc Nephrol 18:485–493Google Scholar
  49. 49.
    Sharif-Naeini R, Folgering JH, Bichet D, Duprat F, Lauritzen I, Arhatte M, Jodar M, Dedman A, Chatelain FC, Schulte U, Retailleau K, Loufrani L, Patel A, Sachs F, Delmas P, Peters DJ, Honore E (2009) Polycystin-1 and -2 dosage regulates pressure sensing. Cell 139:587–596Google Scholar
  50. 50.
    Drummond IA (2011) Polycystins, focal adhesions and extracellular matrix interactions. Biochim Biophys Acta 1812:1322–1326Google Scholar
  51. 51.
    Jackson TY, Sun Z, Martinez-Lemus LA, Hill MA, Meininger GA (2010) N-cadherin and integrin blockade inhibit arteriolar myogenic reactivity but not pressure-induced increases in intracellular ca. Front Physiol 1:165Google Scholar
  52. 52.
    Earley S, Heppner TJ, Nelson MT, Brayden JE (2005) Trpv4 forms a novel ca2+signaling complex with ryanodine receptors and bkca channels. Circ Res 97:1270–1279Google Scholar
  53. 53.
    Bagher P, Beleznai T, Kansui Y, Mitchell R, Garland CJ, Dora KA (2012) Low intravascular pressure activates endothelial cell trpv4 channels, local ca2+ events, and ikca channels, reducing arteriolar tone. Proc Natl Acad Sci U.S.A 109:18174–18179Google Scholar
  54. 54.
    Drummond HA, Grifoni SC, Jernigan NL (2008) A new trick for an old dogma: Enac proteins as mechanotransducers in vascular smooth muscle. Physiology (Bethesda) 23:23–31Google Scholar
  55. 55.
    Fronius M, Clauss WG (2008) Mechano-sensitivity of enac: may the (shear) force be with you. Pflugers Arch 455:775–785Google Scholar
  56. 56.
    Carattino MD, Sheng S, Kleyman TR (2004) Epithelial na+ channels are activated by laminar shear stress. J Biol Chem 279:4120–4126Google Scholar
  57. 57.
    Drummond HA, Gebremedhin D, Harder DR (2004) Degenerin/epithelial na+ channel proteins: components of a vascular mechanosensor. Hypertension 44:643–648Google Scholar
  58. 58.
    Jernigan NL, Drummond HA (2005) Vascular enac proteins are required for renal myogenic constriction. Am J Physiol Renal Physiol 289:F891–F901Google Scholar
  59. 59.
    Guan Z, Pollock JS, Cook AK, Hobbs JL, Inscho EW (2009) Effect of epithelial sodium channel blockade on the myogenic response of rat juxtamedullary afferent arterioles. Hypertension 54:1062–1069Google Scholar
  60. 60.
    Wang X, Breaks J, Loutzenhiser K, Loutzenhiser R (2007) Effects of inhibition of the na+/k+/2cl− cotransporter on myogenic and angiotensin II responses of the rat afferent arteriole. Am J Physiol Renal Physiol 292:F999–F1006Google Scholar
  61. 61.
    Gannon KP, Vanlandingham LG, Jernigan NL, Grifoni SC, Hamilton G, Drummond HA (2008) Impaired pressure-induced constriction in mouse middle cerebral arteries of asic2 knockout mice. Am J Physiol Heart Circ Physiol 294:H1793–H1803Google Scholar
  62. 62.
    Grifoni SC, Chiposi R, McKey SE, Ryan MJ, Drummond HA (2010) Altered whole kidney blood flow autoregulation in a mouse model of reduced beta-enac. Am J Physiol Renal Physiol 298:F285–F292Google Scholar
  63. 63.
    Drummond HA, Grifoni SC, Abu-Zaid A, Gousset M, Chiposi R, Barnard JM, Murphey B, Stec DE (2011) Renal inflammation and elevated blood pressure in a mouse model of reduced {beta} ENaC. Am J Physiol Renal Physiol 301:F443–F449Google Scholar
  64. 64.
    Nelson MT, Conway MA, Knot HJ, Brayden JE (1997) Chloride channel blockers inhibit myogenic tone in rat cerebral arteries. J Physiol 502(Pt 2):259–264Google Scholar
  65. 65.
    Bulley S, Neeb ZP, Burris SK, Bannister JP, Thomas-Gatewood CM, Jangsangthong W, Jaggar JH (2012) Tmem16a/ano1 channels contribute to the myogenic response in cerebral arteries. Circ Res 111:1027–1036Google Scholar
  66. 66.
    Osol G, Laher I, Kelley M (1993) Myogenic tone is coupled to phospholipase c and g protein activation in small cerebral arteries. Am J Physiol 265:H415–H420Google Scholar
  67. 67.
    Narayanan J, Imig M, Roman RJ, Harder DR (1994) Pressurization of isolated renal arteries increases inositol trisphosphate and diacylglycerol. Am J Physiol 266:H1840–H1845Google Scholar
  68. 68.
    Blodow S, Schneider H, Storch U, Wizemann R, Forst AL, Gudermann T, Mederos YSM (2013) Novel role of mechanosensitive at receptors in myogenic vasoconstriction. Pflugers Arch (Epub ahead of print)Google Scholar
  69. 69.
    Mederos y Schnitzler M, Storch U, Meibers S, Nurwakagari P, Breit A, Essin K, Gollasch M, Gudermann T (2008) Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J 27:3092–3103Google Scholar
  70. 70.
    Yasuda N, Miura S, Akazawa H, Tanaka T, Qin Y, Kiya Y, Imaizumi S, Fujino M, Ito K, Zou Y, Fukuhara S, Kunimoto S, Fukuzaki K, Sato T, Ge J, Mochizuki N, Nakaya H, Saku K, Komuro I (2008) Conformational switch of angiotensin ii type 1 receptor underlying mechanical stress-induced activation. EMBO Rep 9:179–186Google Scholar
  71. 71.
    Gudi S, Nolan JP, Frangos JA (1998) Modulation of gtpase activity of g proteins by fluid shear stress and phospholipid composition. Proc Natl Acad Sci U.S.A 95:2515–2519Google Scholar
  72. 72.
    Chachisvilis M, Zhang YL, Frangos JA (2006) G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc Natl Acad Sci U.S.A 103:15463–15468Google Scholar
  73. 73.
    Spassova MA, Hewavitharana T, Xu W, Soboloff J, Gill DL (2006) A common mechanism underlies stretch activation and receptor activation of trpc6 channels. Proc Natl Acad Sci U.S.A 103:16586–16591Google Scholar
  74. 74.
    Earley S (2013) Trpm4 channels in smooth muscle function. Pflugers Arch 465:1223–1231Google Scholar
  75. 75.
    Yatani A, Brown AM (1989) Rapid beta-adrenergic modulation of cardiac calcium channel currents by a fast g protein pathway. Science 245:71–74Google Scholar
  76. 76.
    Hill MA, Zou H, Potocnik SJ, Meininger GA, Davis MJ (2001) Invited review: arteriolar smooth muscle mechanotransduction: Ca(2+) signaling pathways underlying myogenic reactivity. J Appl Physiol 91:973–983Google Scholar
  77. 77.
    Potocnik SJ, Hill MA (2001) Pharmacological evidence for capacitative ca(2+) entry in cannulated and pressurized skeletal muscle arterioles. Br J Pharmacol 134:247–256Google Scholar
  78. 78.
    Hill MA, Meininger GA (1994) Calcium entry and myogenic phenomena in skeletal muscle arterioles. Am J Physiol 267:H1085–H1092Google Scholar
  79. 79.
    Loutzenhiser R, Epstein M (1990) Renal microvascular actions of calcium antagonists. J Am Soc Nephrol 1:S3–S12Google Scholar
  80. 80.
    McCarron JG, Olson ML (2008) A single luminally continuous sarcoplasmic reticulum with apparently separate ca2+ stores in smooth muscle. J Biol Chem 283:7206–7218Google Scholar
  81. 81.
    Nelson MT, Quayle JM (1995) Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 268:C799–C822Google Scholar
  82. 82.
    Jaggar JH, Wellman GC, Heppner TJ, Porter VA, Perez GJ, Gollasch M, Kleppisch T, Rubart M, Stevenson AS, Lederer WJ, Knot HJ, Bonev AD, Nelson MT (1998) Ca2+ channels, ryanodine receptors and ca(2+)-activated k+ channels: a functional unit for regulating arterial tone. Acta Physiol Scand 164:577–587Google Scholar
  83. 83.
    Yang Y, Murphy TV, Ella SR, Grayson TH, Haddock R, Hwang YT, Braun AP, Peichun G, Korthuis RJ, Davis MJ, Hill MA (2009) Heterogeneity in function of small artery smooth muscle bkca: iInvolvement of the beta1-subunit. J Physiol 587:3025–3044Google Scholar
  84. 84.
    Yang Y, Sohma Y, Nourian Z, Ella SR, Li M, Stupica A, Korthuis RJ, Davis MJ, Braun AP, Hill MA (2013) Mechanisms underlying regional differences in the ca2+ sensitivity of bk(ca) current in arteriolar smooth muscle. J Physiol 591:1277–1293Google Scholar
  85. 85.
    Jaggar JH (2001) Intravascular pressure regulates local and global ca(2+) signaling in cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 281:C439–C448Google Scholar
  86. 86.
    Ella SR, Davis MJ, Meininger GA, Yang Y, Dora KA, Hill MA (2009) Mechanisms underlying smooth muscle ca2+ waves in cremaster muscle arterioles. Faseb J 23:767.8Google Scholar
  87. 87.
    Mufti RE, Brett SE, Tran CH, Abd El-Rahman R, Anfinogenova Y, El-Yazbi A, Cole WC, Jones PP, Chen SR, Welsh DG (2010) Intravascular pressure augments cerebral arterial constriction by inducing voltage-insensitive ca2+ waves. J Physiol 588:3983–4005Google Scholar
  88. 88.
    Cole WC, Welsh DG (2011) Role of myosin light chain kinase and myosin light chain phosphatase in the resistance arterial myogenic response to intravascular pressure. Arch Biochem Biophys 510:160–173Google Scholar
  89. 89.
    Zou H, Ratz PH, Hill MA (2000) Temporal aspects of ca(2+) and myosin phosphorylation during myogenic and norepinephrine-induced arteriolar constriction. J Vasc Res 37:556–567Google Scholar
  90. 90.
    El-Yazbi AF, Johnson RP, Walsh EJ, Takeya K, Walsh MP, Cole WC (2010) Pressure-dependent contribution of rho kinase-mediated calcium sensitization in serotonin-evoked vasoconstriction of rat cerebral arteries. J Physiol 588:1747–1762Google Scholar
  91. 91.
    Johnson RP, El-Yazbi AF, Takeya K, Walsh EJ, Walsh MP, Cole WC (2009) Ca2+ sensitization owing to rho kinase-dependent phosphorylation of mypt1-t855 contributes to myogenic control of arterial diameter. J Physiol 587:2537–2553Google Scholar
  92. 92.
    Hill MA, Falcone JC, Meininger GA (1990) Evidence for protein kinase c involvement in arteriolar myogenic reactivity. Am J Physiol 259:H1586–H1594Google Scholar
  93. 93.
    Osol G, Laher I, Cipolla M (1991) Protein kinase c modulates basal myogenic tone in resistance arteries from the cerebral circulation. Circ Res 68:359–367Google Scholar
  94. 94.
    Dessy C, Matsuda N, Hulvershorn J, Sougnez CL, Sellke FW, Morgan KG (2000) Evidence for involvement of the pkc-alpha isoform in myogenic contractions of the coronary microcirculation. Am J Physiol Heart Circ Physiol 279:H916–H923Google Scholar
  95. 95.
    Hill MA, Davis MJ, Song J, Zou H (1996) Calcium dependence of indolactam-mediated contractions in resistance vessels. J Pharmacol Exp Ther 276:867–874Google Scholar
  96. 96.
    Bolz SS, Vogel L, Sollinger D, Derwand R, Boer C, Pitson SM, Spiegel S, Pohl U (2003) Sphingosine kinase modulates microvascular tone and myogenic responses through activation of rhoa/rho kinase. Circulation 108:342–347Google Scholar
  97. 97.
    Salomone S, Soydan G, Ip PC, Hopson KM, Waeber C (2010) Vessel-specific role of sphingosine kinase 1 in the vasoconstriction of isolated basilar arteries. Pharmacol Res 62:465–474Google Scholar
  98. 98.
    Hoefer J, Azam MA, Kroetsch JT, Leong-Poi H, Momen MA, Voigtlaender-Bolz J, Scherer EQ, Meissner A, Bolz SS, Husain M (2010) Sphingosine-1-phosphate-dependent activation of p38 mapk maintains elevated peripheral resistance in heart failure through increased myogenic vasoconstriction. Circ Res 107:923–933Google Scholar
  99. 99.
    Huang S, Sun Z, Li Z, Martinez-Lemus LA, Meininger GA (2010) Modulation of microvascular smooth muscle adhesion and mechanotransduction by integrin-linked kinase. Microcirculation 17:113–127Google Scholar
  100. 100.
    Amin AH, Abd Elmageed ZY, Partyka M, Matrougui K (2011) Mechanisms of myogenic tone of coronary arteriole: role of down stream signaling of the egfr tyrosine kinase. Microvasc Res 81:135–142Google Scholar
  101. 101.
    Spurrell BE, Murphy TV, Hill MA (2003) Intraluminal pressure stimulates mapk phosphorylation in arterioles: temporal dissociation from myogenic contractile response. Am J Physiol Heart Circ Physiol 285:H1764–H1773Google Scholar
  102. 102.
    Murphy TV, Spurrell BE, Hill MA (2001) Tyrosine phosphorylation following alterations in arteriolar intraluminal pressure and wall tension. Am J Physiol Heart Circ Physiol 281:H1047–H1056Google Scholar
  103. 103.
    Simandle SA, Erdos B, Snipes JA, Miller AW, Busija DW (2005) Insulin resistance does not impair contractile responses of cerebral arteries. Life Sci 77:2262–2272Google Scholar
  104. 104.
    Howitt L, Grayson TH, Morris MJ, Sandow SL, Murphy TV (2012) Dietary obesity increases no and inhibits bkca-mediated, endothelium-dependent dilation in rat cremaster muscle artery: association with caveolins and caveolae. Am J Physiol Heart Circ Physiol 302:H2464–H2476Google Scholar
  105. 105.
    Sweazea KL, Walker BR (2012) Impaired myogenic tone in mesenteric arteries from overweight rats. Nutr Metab (Lond) 9:18Google Scholar
  106. 106.
    Butcher JT, Goodwill AG, Stanley SC, Frisbee JC (2013) Differential impact of dilator stimuli on increased myogenic activation of cerebral and skeletal muscle resistance arterioles in obese zucker rats. Microcirculation 20:579–589Google Scholar
  107. 107.
    Kurtz TW, Morris RC, Pershadsingh HA (1989) The zucker fatty rat as a genetic model of obesity and hypertension. Hypertension 13:896–901Google Scholar
  108. 108.
    Stepp DW, Frisbee JC (2002) Augmented adrenergic vasoconstriction in hypertensive diabetic obese zucker rats. Am J Physiol Heart Circ Physiol 282:H816–H820Google Scholar
  109. 109.
    Frisbee JC, Maier KG, Stepp DW (2002) Oxidant stress-induced increase in myogenic activation of skeletal muscle resistance arteries in obese zucker rats. Am J Physiol Heart Circ Physiol 283:H2160–H2168Google Scholar
  110. 110.
    Phillips SA, Sylvester FA, Frisbee JC (2005) Oxidant stress and constrictor reactivity impair cerebral artery dilation in obese zucker rats. Am J Physiol Regul Integr Comp Physiol 288:R522–R530Google Scholar
  111. 111.
    Hill MA, Ege EA (1994) Active and passive mechanical properties of isolated arterioles from stz-induced diabetic rats. Effect of aminoguanidine treatment. Diabetes 43:1450–1456Google Scholar
  112. 112.
    Hill MA, Meininger GA (1993) Impaired arteriolar myogenic reactivity in early experimental diabetes. Diabetes 42:1226–1232Google Scholar
  113. 113.
    Zimmermann PA, Knot HJ, Stevenson AS, Nelson MT (1997) Increased myogenic tone and diminished responsiveness to atp-sensitive k+ channel openers in cerebral arteries from diabetic rats. Circ Res 81:996–1004Google Scholar
  114. 114.
    Matsumoto T, Yoshiyama S, Kobayashi T, Kamata K (2004) Mechanisms underlying enhanced contractile response to endothelin-1 in diabetic rat basilar artery. Peptides 25:1985–1994Google Scholar
  115. 115.
    Ungvari Z, Pacher P, Kecskemeti V, Papp G, Szollar L, Koller A (1999) 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 43:1018–1028Google Scholar
  116. 116.
    Belmadani S, Palen DI, Gonzalez-Villalobos RA, Boulares HA, Matrougui K (2008) Elevated epidermal growth factor receptor phosphorylation induces resistance artery dysfunction in diabetic db/db mice. Diabetes 57:1629–1637Google Scholar
  117. 117.
    Lagaud GJ, Masih-Khan E, Kai S, van Breemen C, Dube GP (2001) Influence of type ii diabetes on arterial tone and endothelial function in murine mesenteric resistance arteries. J Vasc Res 38:578–589Google Scholar
  118. 118.
    Su J, Lucchesi PA, Gonzalez-Villalobos RA, Palen DI, Rezk BM, Suzuki Y, Boulares HA, Matrougui K (2008) Role of advanced glycation end products with oxidative stress in resistance artery dysfunction in type 2 diabetic mice. Arterioscler Thromb Vasc Biol 28:1432–1438Google Scholar
  119. 119.
    Xie Z, Su W, Guo Z, Pang H, Post SR, Gong MC (2006) Up-regulation of cpi-17 phosphorylation in diabetic vasculature and high glucose cultured vascular smooth muscle cells. Cardiovasc Res 69:491–501Google Scholar
  120. 120.
    Bagi Z, Erdei N, Toth A, Li W, Hintze TH, Koller A, Kaley G (2005) Type 2 diabetic mice have increased arteriolar tone and blood pressure: enhanced release of cox-2-derived constrictor prostaglandins. Arterioscler Thromb Vasc Biol 25:1610–1616Google Scholar
  121. 121.
    Rutkai I, Feher A, Erdei N, Henrion D, Papp Z, Edes I, Koller A, Kaley G, Bagi Z (2009) Activation of prostaglandin e2 ep1 receptor increases arteriolar tone and blood pressure in mice with type 2 diabetes. Cardiovasc Res 83:148–154Google Scholar
  122. 122.
    Moien-Afshari F, Ghosh S, Elmi S, Khazaei M, Rahman MM, Sallam N, Laher I (2008) Exercise restores coronary vascular function independent of myogenic tone or hyperglycemic status in db/db mice. Am J Physiol Heart Circ Physiol 295:H1470–H1480Google Scholar
  123. 123.
    Goto Y, Kakizaki M, Masaki N (1976) Production of spontaneous diabetic rats by repetition of selective breeding. Tohoku J Exp Med 119:85–90Google Scholar
  124. 124.
    Seica RM, Martins MJ, Pessa PB, Santos RM, Rosario LM, Suzuki KI (2003) Martins MI [morphological changes of islet of langerhans in an animal model of type 2 diabetes]. Acta Med Port 16:381–388Google Scholar
  125. 125.
    Seica RM, Suzuki KI, Santos RM (2004) Do Rosario LM [impaired insulin secretion in isolated islets of goto-kakizaki rats, an animal model of non obese type 2 diabetes, is a primary event]. Acta Med Port 17:42–48Google Scholar
  126. 126.
    Kelly-Cobbs A, Elgebaly MM, Li W, Ergul A (2011) Pressure-independent cerebrovascular remodelling and changes in myogenic reactivity in diabetic goto-kakizaki rat in response to glycaemic control. Acta Physiol (Oxf) 203:245–251Google Scholar
  127. 127.
    Kelly-Cobbs AI, Prakash R, Coucha M, Knight RA, Li W, Ogbi SN, Johnson M, Ergul A (2012) Cerebral myogenic reactivity and blood flow in type 2 diabetic rats: role of peroxynitrite in hypoxia-mediated loss of myogenic tone. J Pharmacol Exp Ther 342:407–415Google Scholar
  128. 128.
    Kold-Petersen H, Brondum E, Nilsson H, Flyvbjerg A, Aalkjaer C (2012) Impaired myogenic tone in isolated cerebral and coronary resistance arteries from the goto-kakizaki rat model of type 2 diabetes. J Vasc Res 49:267–278Google Scholar
  129. 129.
    Harris AK, Elgebaly MM, Li W, Sachidanandam K, Ergul A (2008) Effect of chronic endothelin receptor antagonism on cerebrovascular function in type 2 diabetes. Am J Physiol Regul Integr Comp Physiol 294:R1213–R1219Google Scholar
  130. 130.
    Ishida K, Matsumoto T, Taguchi K, Kamata K, Kobayashi T (2012) Protein kinase C delta contributes to increase in ep3 agonist-induced contraction in mesenteric arteries from type 2 diabetic goto-kakizaki rats. Pflugers Arch 463:593–602Google Scholar
  131. 131.
    Tirabassi RS, Flanagan JF, Wu T, Kislauskis EH, Birckbichler PJ, Guberski DL (2004) The bbzdr/wor rat model for investigating the complications of type 2 diabetes mellitus. ILAR J 45:292–302Google Scholar
  132. 132.
    Jarajapu YP, Guberski DL, Grant MB, Knot HJ (2008) Myogenic tone and reactivity of cerebral arteries in type ii diabetic bbzdr/wor rat. Eur J Pharmacol 579:298–307Google Scholar
  133. 133.
    Ito I, Jarajapu YP, Guberski DL, Grant MB, Knot HJ (2006) Myogenic tone and reactivity of rat ophthalmic artery in acute exposure to high glucose and in a type II diabetic model. Invest Ophthalmol Vis Sci 47:683–692Google Scholar
  134. 134.
    Feng J, Liu Y, Khabbaz KR, Hagberg R, Robich MP, Clements RT, Bianchi C, Sellke FW (2011) Decreased contractile response to endothelin-1 of peripheral microvasculature from diabetic patients. Surgery 149:247–252Google Scholar
  135. 135.
    Schofield I, Malik R, Izzard A, Austin C, Heagerty A (2002) Vascular structural and functional changes in type 2 diabetes mellitus: evidence for the roles of abnormal myogenic responsiveness and dyslipidemia. Circulation 106:3037–3043Google Scholar
  136. 136.
    Lorenzi M, Feke GT, Pitler L, Berisha F, Kolodjaschna J, McMeel JW (2010) Defective myogenic response to posture change in retinal vessels of well-controlled type 1 diabetic patients with no retinopathy. Invest Ophthalmol Vis Sci 51:6770–6775Google Scholar
  137. 137.
    Miura H, Wachtel RE, Loberiza FR Jr, Saito T, Miura M, Nicolosi AC, Gutterman DD (2003) Diabetes mellitus impairs vasodilation to hypoxia in human coronary arterioles: reduced activity of atp-sensitive potassium channels. Circ Res 92:151–158Google Scholar
  138. 138.
    Szerafin T, Erdei N, Fulop T, Pasztor ET, Edes I, Koller A, Bagi Z (2006) Increased cyclooxygenase-2 expression and prostaglandin-mediated dilation in coronary arterioles of patients with diabetes mellitus. Circ Res 99:e12–e17Google Scholar
  139. 139.
    Wu X, Yang Y, Gui P, Sohma Y, Meininger GA, Davis GE, Braun AP, Davis MJ (2008) Potentiation of large conductance, ca2+-activated k+ (bk) channels by alpha5beta1 integrin activation in arteriolar smooth muscle. J Physiol 586:1699–1713Google Scholar
  140. 140.
    Cherney DZ, Sochett EB, Lai V, Dekker MG, Slorach C, Scholey JW, Bradley TJ (2010) Renal hyperfiltration and arterial stiffness in humans with uncomplicated type 1 diabetes. Diabetes Care 33:2068–2070Google Scholar
  141. 141.
    Flynn MD, Edmonds ME, Tooke JE, Watkins PJ (1988) Direct measurement of capillary blood flow in the diabetic neuropathic foot. Diabetologia 31:652–656Google Scholar
  142. 142.
    Shore AC, Price KJ, Sandeman DD, Tripp JH, Tooke JE (1994) Posturally induced vasoconstriction in diabetes mellitus. Arch Dis Child 70:22–26Google Scholar
  143. 143.
    Turk Z (2010) Glycotoxines, carbonyl stress and relevance to diabetes and its complications. Physiol Res 59:147–156Google Scholar
  144. 144.
    Ulrich P, Cerami A (2001) Protein glycation, diabetes, and aging. Recent Prog Horm Res 56:1–21Google Scholar
  145. 145.
    Martinez-Lemus LA, Wu X, Wilson E, Hill MA, Davis GE, Davis MJ, Meininger GA (2003) Integrins as unique receptors for vascular control. J Vasc Res 40:211–233Google Scholar
  146. 146.
    Martinez-Lemus LA, Hill MA, Meininger GA (2009) The plastic nature of the vascular wall: a continuum of remodeling events contributing to control of arteriolar diameter and structure. Physiology (Bethesda) 24:45–57Google Scholar
  147. 147.
    Curtis TM, McKeown-Longo PJ, Vincent PA, Homan SM, Wheatley EM, Saba TM (1995) Fibronectin attenuates increased endothelial monolayer permeability after rgd peptide, anti-alpha 5 beta 1, or tnf-alpha exposure. Am J Physiol 269:L248–L260Google Scholar
  148. 148.
    Qiao RL, Yan W, Lum H, Malik AB (1995) Arg-gly-asp peptide increases endothelial hydraulic conductivity: comparison with thrombin response. Am J Physiol 269:C110–C117Google Scholar
  149. 149.
    Berrou J, Tostivint I, Verrecchia F, Berthier C, Boulanger E, Mauviel A, Marti HP, Wautier MP, Wautier JL, Rondeau E, Hertig A (2009) Advanced glycation end products regulate extracellular matrix protein and protease expression by human glomerular mesangial cells. Int J Mol Med 23:513–520Google Scholar
  150. 150.
    DeGroot J, Verzijl N, Budde M, Bijlsma JW, Lafeber FP, TeKoppele JM (2001) Accumulation of advanced glycation end products decreases collagen turnover by bovine chondrocytes. Exp Cell Res 266:303–310Google Scholar
  151. 151.
    Spinetti G, Kraenkel N, Emanueli C, Madeddu P (2008) Diabetes and vessel wall remodelling: from mechanistic insights to regenerative therapies. Cardiovasc Res 78:265–273Google Scholar
  152. 152.
    Goldin A, Beckman JA, Schmidt AM, Creager MA (2006) Advanced glycation end products: sparking the development of diabetic vascular injury. Circulation 114:597–605Google Scholar
  153. 153.
    Owen WF Jr, Hou FF, Stuart RO, Kay J, Boyce J, Chertow GM, Schmidt AM (1998) Beta 2-microglobulin modified with advanced glycation end products modulates collagen synthesis by human fibroblasts. Kidney Int 53:1365–1373Google Scholar
  154. 154.
    Sakaguchi T, Yan SF, Yan SD, Belov D, Rong LL, Sousa M, Andrassy M, Marso SP, Duda S, Arnold B, Liliensiek B, Nawroth PP, Stern DM, Schmidt AM, Naka Y (2003) Central role of rage-dependent neointimal expansion in arterial restenosis. J Clin Invest 111:959–972Google Scholar
  155. 155.
    Schmidt AM, Hori O, Chen JX, Li JF, Crandall J, Zhang J, Cao R, Yan SD, Brett J, Stern D (1995) Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (vcam-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 96:1395–1403Google Scholar
  156. 156.
    Schmidt AM, Yan SD, Brett J, Mora R, Nowygrod R, Stern D (1993) Regulation of human mononuclear phagocyte migration by cell surface-binding proteins for advanced glycation end products. J Clin Invest 91:2155–2168Google Scholar
  157. 157.
    Vlassara H (1994) Recent progress on the biologic and clinical significance of advanced glycosylation end products. J Lab Clin Med 124:19–30Google Scholar
  158. 158.
    Zhao LM, Su XL, Wang Y, Li GR, Deng XL (2013) Kca3.1 channels mediate the increase of cell migration and proliferation by advanced glycation endproducts in cultured rat vascular smooth muscle cells. Lab Invest 93:159–167Google Scholar
  159. 159.
    Dhar S, Sun Z, Yang Y, Meininger GA, Hill MA (2012) Increased adhesion of glycated proteins to arteriolar vascular smooth muscle cells as determined by atomic force microscopy. Biophys J 102(suppl 1):587aGoogle Scholar
  160. 160.
    Yu G, Zou H, Prewitt RL, Hill MA (1999) Impaired arteriolar mechanotransduction in experimental diabetes mellitus. J Diabetes Complications 13:235–242Google Scholar
  161. 161.
    Miyata T, Sugiyama S, Saito A, Kurokawa K (2001) Reactive carbonyl compounds related uremic toxicity (“Carbonyl stress”). Kidney Int Suppl 78:S25–S31Google Scholar
  162. 162.
    Cohen MP, Ziyadeh FN, Chen S (2006) Amadori-modified glycated serum proteins and accelerated atherosclerosis in diabetes: pathogenic and therapeutic implications. J Lab Clin Med 147:211–219Google Scholar
  163. 163.
    Thornalley PJ (2008) Protein and nucleotide damage by glyoxal and methylglyoxal in physiological systems—role in ageing and disease. Drug Metab. Drug Interact 23:125–150Google Scholar
  164. 164.
    Katz PS, Trask AJ, Souza-Smith FM, Hutchinson KR, Galantowicz ML, Lord KC, Stewart JA Jr, Cismowski MJ, Varner KJ, Lucchesi PA (2011) Coronary arterioles in type 2 diabetic (db/db) mice undergo a distinct pattern of remodeling associated with decreased vessel stiffness. Basic Res Cardiol 106:1123–1134Google Scholar
  165. 165.
    Souza-Smith FM, Katz PS, Trask AJ, Stewart JA Jr, Lord KC, Varner KJ, Vassallo DV, Lucchesi PA (2011) Mesenteric resistance arteries in type 2 diabetic db/db mice undergo outward remodeling. PLoS ONE 6:e23337Google Scholar
  166. 166.
    Trask AJ, Cismowski MJ, Halleck K, Lucchesi PA (2013) Proteomic analysis of aortic and coronary resistance microvessel tissue in type 2 diabetic db/db mice. FASEB J 27:924.11Google Scholar
  167. 167.
    Hill MA, Zou H, Davis MJ, Potocnik SJ, Price S (2000) Transient increases in diameter and [ca(2+)](i) are not obligatory for myogenic constriction. Am J Physiol Heart Circ Physiol 278:H345–H352Google Scholar
  168. 168.
    Bubolz AH, Li H, Wu Q, Liu Y (2005) Enhanced oxidative stress impairs camp-mediated dilation by reducing kv channel function in small coronary arteries of diabetic rats. Am J Physiol Heart Circ Physiol 289:H1873–H1880Google Scholar
  169. 169.
    Dong L, Zheng YM, van Riper D, Rathore R, Liu QH, Singer HA, Wang YX (2008) Functional and molecular evidence for impairment of calcium-activated potassium channels in type-1 diabetic cerebral artery smooth muscle cells. J Cereb Blood Flow Metab 28:377–386Google Scholar
  170. 170.
    Liu Y, Terata K, Rusch NJ, Gutterman DD (2001) High glucose impairs voltage-gated k(+) channel current in rat small coronary arteries. Circ Res 89:146–152Google Scholar
  171. 171.
    Lu T, Wang XL, He T, Zhou W, Kaduce TL, Katusic ZS, Spector AA, Lee HC (2005) Impaired arachidonic acid-mediated activation of large-conductance ca2+-activated k+ channels in coronary arterial smooth muscle cells in zucker diabetic fatty rats. Diabetes 54:2155–2163Google Scholar
  172. 172.
    Mokelke EA, Dietz NJ, Eckman DM, Nelson MT, Sturek M (2005) Diabetic dyslipidemia and exercise affect coronary tone and differential regulation of conduit and microvessel k+ current. Am J Physiol Heart Circ Physiol 288:H1233–H1241Google Scholar
  173. 173.
    Hein TW, Potts LB, Xu W, Yuen JZ, Kuo L (2012) Temporal development of retinal arteriolar endothelial dysfunction in porcine type 1 diabetes. Invest Ophthalmol Vis Sci 53:7943–7949Google Scholar
  174. 174.
    Hayashi K, Epstein M, Loutzenhiser R, Forster H (1992) Impaired myogenic responsiveness of the afferent arteriole in streptozotocin-induced diabetic rats: role of eicosanoid derangements. J Am Soc Nephrol 2:1578–1586Google Scholar
  175. 175.
    Sachidanandam K, Hutchinson JR, Elgebaly MM, Mezzetti EM, Wang MH (2009) Differential effects of diet-induced dyslipidemia and hyperglycemia on mesenteric resistance artery structure and function in type 2 diabetes. J Pharmacol Exp Ther 328:123–130Google Scholar
  176. 176.
    Adebiyi A, Zhao G, Cheranov SY, Ahmed A, Jaggar JH (2007) Caveolin-1 abolishment attenuates the myogenic response in murine cerebral arteries. Am J Physiol Heart Circ Physiol 292:H1584–H1592Google Scholar
  177. 177.
    Howitt L, Sandow SL, Grayson TH, Ellis ZE, Morris MJ, Murphy TV (2011) Differential effects of diet-induced obesity on bkca {beta}1-subunit expression and function in rat skeletal muscle arterioles and small cerebral arteries. Am J Physiol Heart Circ Physiol 301:H29–H40Google Scholar
  178. 178.
    Straub SV, Girouard H, Doetsch PE, Hannah RM, Wilkerson MK, Nelson MT (2009) Regulation of intracerebral arteriolar tone by k(v) channels: effects of glucose and PKC. Am J Physiol Cell Physiol 297:C788–C796Google Scholar
  179. 179.
    Cipolla MJ, McCall AL, Lessov N, Porter JM (1997) Reperfusion decreases myogenic reactivity and alters middle cerebral artery function after focal cerebral ischemia in rats. Stroke 28:176–180Google Scholar
  180. 180.
    Nobe K, Nezu Y, Tsumita N, Hashimoto T, Honda K (2008) Intra- and extrarenal arteries exhibit different profiles of contractile responses in high glucose conditions. Br J Pharmacol 155:1204–1213Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Sewon Lee
    • 1
  • Srijita Dhar
    • 1
    • 2
  • Kwangseok Hong
    • 1
    • 2
  • Yan Yang
    • 1
  • Michael A. Hill
    • 1
    • 2
    Email author
  1. 1.Dalton Cardiovascular Research CenterUniversity of MissouriColumbiaUSA
  2. 2.Department of Medical Pharmacology and PhysiologyUniversity of MissouriColumbiaUSA

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