Maturation and long-term hypoxia-induced acclimatization responses in PKC-mediated signaling pathways in ovine cerebral arterial contractility

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 5, 2010, Pages

  Goyal, Ravi ^a   Mittal, Ashwani ^a   Chu, Nina ^a   Arthur, Rebecca Afiba ^a   Zhang, Lubo ^a   Longo, Lawrence D ^a  

^a LOMA LINDA UNIVERSITY   (United States)

Author keywords

20 kDa myosin light chain; CPI 17; ERK1 2; Fetus; High altitude; RhoA

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; CALCIUM; CPI 17; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYOSIN LIGHT CHAIN; PHORBOL DIBUTYRATE; PROTEIN KINASE C; PROTEIN TYROSINE PHOSPHATASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ALTITUDE ACCLIMATIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY CONSTRICTION; ARTICLE; BRAIN ARTERY; CALCIUM CELL LEVEL; CONTROLLED STUDY; FETUS; HYPOXIA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SENSITIZATION; SHEEP; SIGNAL TRANSDUCTION; TENSION;

ACCLIMATIZATION; AGE FACTORS; AGING; ANIMALS; ANOXIA; CALCIUM SIGNALING; CEREBRAL ARTERIES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; ENZYME ACTIVATORS; FETAL HYPOXIA; GESTATIONAL AGE; MAP KINASE KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOSIN LIGHT CHAINS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SHEEP; TIME FACTORS; VASOCONSTRICTION;

EID: 78149491379     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00344.2010     Document Type: Article

References (74)

1. Adam LP, Franklin MT, Raff GJ, Hathaway DR. Activation of mitogen-activated protein kinase in porcine carotid arteries. Circ Res 76: 183-190, 1995.
2. Alessandrini A, Crews CM, Erikson RL. Phorbol ester stimulates a protein-tyrosine/threonine kinase that phosphorylates and activates the Erk-1 gene product. Proc Natl Acad Sci USA 89: 8200-8204, 1992.
3. Allen WW, Power GG, Longo LD. Fetal O2 changes in response to hypoxic stress: a mathematical model. J Appl Physiol 42: 179-190, 1977.
4. Anderson NG, Maller JL, Tonks NK, Sturgill TW. Requirement for integration of signals from two distinct phosphorylation pathways for activation of MAP kinase. Nature 343: 651-653, 1990.
5. Bishai JM, Blood AB, Hunter CJ, Longo LD, Power GG. Fetal lamb cerebral blood flow (CBF) and oxygen tensions during hypoxia: a comparison of laser Doppler and microsphere measurements of CBF. J Physiol 546: 869-878, 2003.
6. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
7. Chang K, Xiao D, Huang X, Longo LD, Zhang L. Chronic hypoxia increases pressure-dependent myogenic tone of the uterine artery in pregnant sheep: role of ERK/PKC pathway. Am J Physiol Heart Circ Physiol 296: H1840-H1849, 2009.
8. Childs TJ, Watson MH, Sanghera JS, Campbell DL, Pelech SL, Mak AS. Phosphorylation of smooth muscle caldesmon by mitogen-activated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J Biol Chem 267: 22853-22859, 1992.
9. Deng JT, Sutherland C, Brautigan DL, Eto M, Walsh MP. Phosphorylation of the myosin phosphatase inhibitors, CPI-17 and PHI-1, by integrin-linked kinase. Biochem J 367: 517-524, 2002. (Pubitemid 35216828)
10. Dessy C, Kim I, Sougnez CL, Laporte R, Morgan KG. A role for MAP kinase in differentiated smooth muscle contraction evoked by α-adrenoceptor stimulation. Am J Physiol Cell Physiol 275: C1081-C1086, 1998.
11. Epstein AM, Throckmorton D, Brophy CM. Mitogen-activated protein kinase activation: an alternate signaling pathway for sustained vascular smooth muscle contraction. J Vasc Surg 26: 327-332, 1997.
12. Gao Y, Portugal AD, Negash S, Zhou W, Longo LD, Raj UJ. Role of Rho kinases in PKG-mediated relaxation of pulmonary arteries of fetal lambs exposed to chronic high-altitude hypoxia. Am J Physiol Lung Cell Mol Physiol 292: L678-L684, 2007.
13. Geary GG, Osol GJ, Longo LD. Development affects in vitro vascular tone and calcium sensitivity in ovine cerebral arteries. J Physiol 558: 883-896, 2004.
14. Gerthoffer WT, Yamboliev IA, Shearer M, Pohl J, Haynes R, Dang S, Sato K, Sellers JR. Activation of MAP kinases and phosphorylation of caldesmon in canine colonic smooth muscle. J Physiol 495: 597-609, 1996.
15. 2+ sensitization of smooth muscle myosin II. Am J Physiol Cell Physiol 281: C257-C269, 2001.
16. 2+ sensitization of smooth muscle. Proc Natl Acad Sci USA 93: 1340-1345, 1996.
17. Gorenne I, Su X, Moreland RS. Inhibition of p42 and p44 MAP kinase does not alter smooth muscle contraction in swine carotid artery. Am J Physiol Heart Circ Physiol 275: H131-H138, 1998. (Pubitemid 128733495)
18. Goyal R, Creel KD, Chavis E, Smith GD, Longo LD, Wilson SM. Maturation of intracellular calcium homeostasis in sheep pulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 295: L905-L914, 2008.
19. Goyal R, Mittal A, Chu N, Shi L, Zhang L, Longo LD. Maturation and the role of PKC-mediated contractility in ovine cerebral arteries. Am J Physiol Heart Circ Physiol 297: H2242-H2252, 2009.
20. 1- Adrenergic receptor subtype function in fetal and adult cerebral arteries. Am J Physiol Heart Circ Physiol 298: H1797-H1806, 2010.
21. Greenberg B, Kishiyama S. Endothelium-dependent and -independent responses to severe hypoxia in rat pulmonary artery. Am J Physiol Heart Circ Physiol 265: H1712-H1720, 1993.
22. Horowitz A, Menice CB, Laporte R, Morgan KG. Mechanisms of smooth muscle contraction. Physiol Rev 76: 967-1003, 1996.
23. Ihara E, MacDonald JA. The regulation of smooth muscle contractility by zipper-interacting protein kinase. Can J Physiol Pharmacol 85: 79-87, 2007.
24. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, Maekawa M, Narumiya S. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 57: 976-983, 2000.
25. Janssen LJ, Tazzeo T, Zuo J, Pertens E, Keshavjee S. KCl evokes contraction of airway smooth muscle via activation of RhoA and Rho-kinase. Am J Physiol Lung Cell Mol Physiol 287: L852-L858, 2004.
26. Jensen JB, Sperling B, Severinghaus JW, Lassen NA. Augmented hypoxic cerebral vasodilation in men during 5 days at 3,810 m altitude. J Appl Physiol 80: 1214-1218, 1996.
27. Jiang MJ, Morgan KG. Intracellular calcium levels in phorbol ester-induced contractions of vascular muscle. Am J Physiol Heart Circ Physiol 253: H1365-H1371, 1987.
28. Kamitomo M, Longo LD, Gilbert RD. Cardiac function in fetal sheep during two weeks of hypoxemia. Am J Physiol Regul Integr Comp Physiol 266: R1778-R1785, 1994.
29. Katoch SS, Moreland RS. Agonist and membrane depolarization induced activation of MAP kinase in the swine carotid artery. Am J Physiol Heart Circ Physiol 269: H222-H229, 1995.
30. Khalil RA, Morgan KG. PKC-mediated redistribution of mitogen-activated protein kinase during smooth muscle cell activation. Am J Physiol Cell Physiol 265: C406-C411, 1993.
31. Kurth CD, Wagerle LC. Cerebrovascular reactivity to adenosine analogues in 0.6-0.7 gestation and near-term fetal sheep. Am J Physiol Heart Circ Physiol 262: H1338-H1342, 1992.
32. Lagaud GJL, Lam E, Lui A, van Breemen C, Laher I. Nonspecific inhibition of myogenic tone by PD98059, a MEK1 inhibitor, in rat middle cerebral arteries. Biochem Biophys Res Commun 257: 523-527, 1999.
33. Lee SJ, Hatran DP, Tomimatsu T, Pereyra-Peña J, McAuley G, Longo LD. Fetal cerebral blood flow, electrocorticographic activity, and oxygenation: responses to acute hypoxia. J Physiol 587: 2033-2047, 2009.
34. Li L, Eto M, Lee MR, Morita F, Yazawa M, Kitazawa T. Possible involvement of the novel CPI-17 protein in protein kinase C signal transduction of rabbit arterial smooth muscle. J Physiol 508: 871-881, 1998. (Pubitemid 28220737)
35. Liao JK, Seto M, Noma K. Rho kinase (ROCK) inhibitors. J Cardiovasc Pharmacol 50: 17-24, 2007.
36. Liu J, Gao Y, Negash S, Longo LD, Raj JU. Long-term effects of prenatal hypoxia on endothelium-dependent relaxation responses in pulmonary arteries of adult sheep. Am J Physiol Lung Cell Mol Physiol 296: L547-L554, 2009.
37. Ca channel responses to long-term hypoxia. J Appl Physiol 92: 1692-1701, 2002.
38. i and tension in fetal and adult cerebral arteries. Am J Physiol Regul Integr Comp Physiol 277: R286-R294, 1999.
39. Longo LD, Hull AD, Long DM, Pearce WJ. Cerebrovascular adaptations to high-altitude hypoxemia in fetal and adult sheep. Am J Physiol Regul Integr Comp Physiol 264: R65-R72, 1993.
40. Longo LD, Pearce WJ. High altitude, hypoxic-induced modulation of noradrenergic-mediated responses in fetal and adult cerebral arteries. Comp Biochem Physiol A Mol Integr Physiol 119: 683-694, 1998.
41. 3 responses in cerebral arteries. Am J Physiol Heart Circ Physiol 270: H915-H923, 1996.
42. Longo LD, Zhao Y, Long W, Miguel C, Windemuth RS, Cantwell AM, Nanyonga AT, Saito T, Zhang L. Dual role of PKC in modulating pharmacomechanical coupling in fetal and adult cerebral arteries. Am J Physiol Regul Integr Comp Physiol 279: R1419-R1429, 2000.
43. McDonald TF, Pelzer S, Trautwein W, Pelzer DJ. Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev 74: 365-507, 1994.
44. Narumiya S, Ishizaki T, Uehata M. Use and properties of ROCKspecific inhibitor Y-27632. Methods Enzymol 325: 273-284, 2000.
45. Nelson KB. Can we prevent cerebral palsy? N Engl J Med 349: 1765-1769, 2003.
46. 2+ sensitivity in rabbit smooth muscle. J Physiol 487: 283-289, 1995.
47. Pearce WJ, Hull AD, Long DM, Longo LD. Developmental changes in ovine cerebral artery composition and reactivity. Am J Physiol Regul Integr Comp Physiol 261: R458-R465, 1991.
48. Pereyra-Peña J, Tomimatsu T, Hatran DP, McGill LL, Longo LD. Cerebral blood flow and oxygenation in ovine fetus: responses to super-imposed hypoxia at both low and high altitude. J Physiol 578: 359-370, 2007.
49. Rasmussen H, Forder J, Kojima I, Scriabine A. TPA-induced contraction of isolated rabbit vascular smooth muscle. Biochem Biophys Res Commun 122: 776-784, 1984.
50. Ratz PH. Regulation of ERK phosphorylation in differentiated arterial muscle of rabbits. Am J Physiol Heart Circ Physiol 281: H114-H123, 2001.
51. Rikitake Y, Kim HH, Huang Z, Seto M, Yano K, Asano T, Moskowitz MA, Liao JK. Inhibition of Rho kinase (ROCK) leads to increased cerebral blood flow and stroke protection. Stroke 36: 2251-2257, 2005.
52. Sato M, Tani E, Fujikawa H, Kaibuchi K. Involvement of Rho-kinase-mediated phosphorylation of myosin light chain in enhancement of cerebral vasospasm. Circ Res 87: 195-200, 2000.
53. Satoh S, Utsunomiya T, Tsurui K, Kobayashi T, Ikegaki I, Sasaki Y, Asano T. Pharmacological profile of hydroxy fasudil as a selective rho kinase inhibitor on ischemic brain damage. Life Sci 69: 1441-1453, 2001.
54. Schwartz MA, Shattil SJ. Signaling networks linking integrins and rho family GTPases. Trends Biochem Sci 25: 388-391, 2000.
55. Severinghaus JW, Chiodi H, Eger EI 2nd, Brandstater B, Hornbein TF. Cerebral blood flow in man at high altitude. Role of cerebrospinal fluid pH in normalization of flow in chronic hypocapnia. Circ Res 19: 274-282, 1966.
56. 2+ sensitivity of smooth muscle and non-muscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
57. Somlyo AP, Somlyo AV. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 522: 177-185, 2000.
58. Tomimatsu T, Pereyra-Peña J, Longo LD. Fetal hypercapnia and cerebral tissue oxygenation: studies in near-term sheep. Pediatr Res 60: 711-716, 2006.
59. Tomimatsu T, Pereyra-Peña J, Longo LD. Fetal hypercapnia in high-altitude acclimatized sheep: cerebral blood flow and cerebral oxygenation. Reprod Sci 14: 51-58, 2007.
60. Touyz RM, El Mabrouk M, He G, Wu XH, Schiffrin EL. Mitogen-activated protein/extracellular signal-regulated kinase inhibition attenuates angiotensin II-mediated signaling and contraction in spontaneously hypertensive rat vascular smooth muscle cells. Circ Res 84: 505-515, 1999.
61. 3 responses in cerebral arteries. Am J Physiol Regul Integr Comp Physiol 272: R669-R674, 1997.
62. Watts S. Serotonin activates the mitogen-activated protein kinase pathway in vascular smooth muscle: use of the mitogen-activated protein kinase kinase inhibitor PD098059. J Pharmacol Exp Ther 279: 1541-1550, 1996.
63. Winter S, Autry A, Boyle C, Yeargin-Allsopp M. Trends in the prevalence of cerebral palsy in a population-based study. Pediatrics 110: 1220-1225, 2002. (Pubitemid 35425199)
64. 2+ sensitivity of protein kinase C-induced contraction in rabbit smooth muscle. J Physiol 535: 553-564, 2001.
65. Xiao D, Huang X, Bae S, Ducsay CA, Longo LD, Zhang L. Cortisol-mediated regulation of uterine artery contractility: effect of chronic hypoxia. Am J Physiol Heart Circ Physiol 286: H716-H722, 2004. (Pubitemid 38140354)
66. 2+ sensitivity in permeabilized uterine arteries: effect of pregnancy. Am J Physiol Heart Circ Physiol 291: H413-H420, 2006.
67. 1-Adrenoceptor-mediated phosphorylation of MYPT-1 and CPI-17 in the uterine artery: role of ERK/PKC. Am J Physiol Heart Circ Physiol 288: H2828-H2835, 2005.
68. Xiao D, Pearce WJ, Longo LD, Zhang L. ERK-mediated uterine artery contraction: role of thick and thin filament regulatory pathways. Am J Physiol Heart Circ Physiol 286: H1615-H1622, 2004.
69. Xiao D, Zhang L. ERK MAP kinases regulate smooth muscle contraction in ovine uterine artery: effect of pregnancy. Am J Physiol Heart Circ Physiol 282: H292-H300, 2002.
70. Xue Q, Ducsay CA, Longo LD, Zhang L. Effect of long-term high-altitude hypoxia on fetal pulmonary vascular contractility. J Appl Physiol 104: 1786-1792, 2008.
71. Zhang L, Hu X, Longo LD. Effect of chronic hypoxia on adrenoceptor responses of ovine foetal umbilical vessels. Br J Pharmacol 125: 136-142, 1998.
72. Zhao Y, Long W, Zhang L, Longo LD. Extracellular signal-regulated kinases and contractile responses in ovine adult and fetal cerebral arteries. J Physiol 551: 691-703, 2003.
73. Zhao Y, Xiao H, Long W, Pearce WJ, Longo LD. Expression of several cytoskeletal proteins in ovine cerebral arteries: developmental and functional considerations. J Physiol 558: 623-632, 2004.
74. Zhao Y, Zhang L, Longo LD. PKC-induced ERK1/2 interactions and downstream effectors in ovine cerebral arteries. Am J Physiol Regul Integr Comp Physiol 289: R164-R171, 2005.