Mechanisms of intermittent hypoxia induced hypertension

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 1-2, 2010, Pages 3-17

  Bosc, Laura V González ^a   Resta, Thomas ^a   Walker, Benjimen ^a   Kanagy, Nancy L ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelin; HIF; Inflammation; Nervous system; NF B; NFAT; Pulmonary hypertension; ROS; Sleep apnoea; Systemic hypertension

Indexed keywords

REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR;

ANIMAL; ANOXIA; BLOOD PRESSURE; DISEASE MODEL; HEMODYNAMICS; HUMAN; HYPERTENSION; METABOLISM; NERVOUS SYSTEM; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SLEEP APNEA SYNDROME;

ANIMALS; ANOXIA; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; HEMODYNAMICS; HUMANS; HYPERTENSION; NERVOUS SYSTEM; REACTIVE OXYGEN SPECIES; SLEEP APNEA, OBSTRUCTIVE; TRANSCRIPTION FACTORS;

ANIMALIA; RODENTIA;

EID: 77951961591     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00929.x     Document Type: Review

References (227)

1. Brooks D, Horner RL, Kozar LF. Obstructive sleep apnea as a cause of systemic hypertension. Evidence from a canine model. J Clin Invest. 1997, 99:106-9.
2. Jun J, Polotsky VY. Metabolic consequences of sleep-disordered breathing. ILAR J. 2009, 50:289-306.
3. Tasali E, Ip MSM. Obstructive sleep apnea and metabolic syndrome: alterations in glucose metabolism and inflammation. Proc Am Thorac Soc. 2008, 5:207-17.
4. Kanagy NL. Vascular effects of intermittent hypoxia. ILAR J. 2009, 50:282-8.
5. Dematteis M, Julien C, Guillermet C. Intermittent hypoxia induces early functional cardiovascular remodeling in mice. Am J Respir Crit Care Med. 2008, 177:227-35.
6. Fletcher EC, Bao G. The rat as a model of chronic recurrent episodic hypoxia and effect upon systemic blood pressure. Sleep. 1996, 19:S210-2.
7. Neubauer JA. Physiological and genomic consequences of intermittent hypoxia: invited review: physiological and pathophysiological responses to intermittent hypoxia. J Appl Physiol. 2001, 90:1593-9.
8. Savransky V, Bevans S, Nanayakkara A. Chronic intermittent hypoxia causes hepatitis in a mouse model of diet-induced fatty liver. Am J Physiol Gastrointest Liver Physiol. 2007, 293:G871-7.
9. Sica AL, Greenberg HE, Ruggiero DA. Chronic-intermittent hypoxia: a model of sympathetic activation in the rat. Respir Physiol. 2000, 121:173-84.
10. Tahawi Z, Orolinova N, Joshua IG. Physiological and genomic consequences of intermittent hypoxia: selected contribution: altered vascular reactivity in arterioles of chronic intermittent hypoxic rats. J Appl Physiol. 2001, 90:2007-13.
11. Tarasiuk A, Scharf SM. Cardiovascular effects of periodic obstructive and central apneas in dogs. Am J Respir Crit Care Med. 1994, 150:83-9.
12. Al Mobeireek AF, Al Kassimi FA, Al Majed SA. Clinical profile of sleep apnea syndrome. A study at a university hospital. Saudi Med J. 2000, 21:180-3.
13. Bananian S, Lehrman SG, Maguire GP. Cardiovascular consequences of sleep-related breathing disorders. Heart Dis. 2002, 4:296-305.
14. Barthlen GM. Sleep disorders. Obstructive sleep apnea syndrome, restless legs syndrome, and insomnia in geriatric patients. Geriatrics. 2002, 57:34-9.
15. Berger HA, Somers VK, Phillips BG. Sleep disordered breathing and hypertension. Curr Opin Pulm Med. 2001, 7:386-90.
16. Fogel RB, White DP. Obstructive sleep apnea. Adv Intern Med. 2000, 45:351-89.
17. Goodday RH, Percious DS, Morrison AD. Obstructive sleep apnea syndrome: diagnosis and management. J Can Dent Assoc. 2001, 67:652-8.
18. Waldhorn RE. Sleep apnea syndrome. Am Fam Physician. 1985, 32:149-66.
19. Fletcher EC. Invited review: physiological consequences of intermittent hypoxia: systemic blood pressure. J Appl Physiol. 2001, 90:1600-5.
20. Fletcher EC, Lesske J, Qian W. Repetitive, episodic hypoxia causes diurnal elevation of blood pressure in rats. Hypertension. 1992, 19:555-61.
21. Greenberg HE, Sica A, Batson D. Chronic intermittent hypoxia increases sympathetic responsiveness to hypoxia and hypercapnia. J Appl Physiol. 1999, 86:298-305.
22. Kraiczi H, Magga J, Sun XY. Hypoxic pressor response, cardiac size, and natriuretic peptides are modified by long-term intermittent hypoxia. J Appl Physiol. 1999, 87:2025-31.
23. Kanagy NL, Walker BR, Nelin LD. Role of endothelin in intermittent hypoxia-induced hypertension. Hypertension. 2001, 37:511-5.
24. Tahawi Z, Orolinova N, Joshua IG. Altered vascular reactivity in arterioles of chronic intermittent hypoxic rats. J Appl Physiol. 2001, 90:2007-13.
25. Peng Y, Yuan G, Overholt JL. Systemic and cellular responses to intermittent hypoxia: evidence for oxidative stress and mitochondrial dysfunction. Adv Exp Med Biol. 2003, 536:559-64.
26. Phillips SA, Olson EB, Morgan BJ. Chronic intermittent hypoxia impairs endothelium-dependent dilation in rat cerebral and sckeletal muscle resistance arteries. Am J Physiol Heart Circ Physiol. 2003, 286:H388-93.
27. Campen MJ, Shimoda LA, O'Donnell CP. Acute and chronic cardiovascular effects of intermittent hypoxia in C57BL/6J mice. J Appl Physiol. 2005, 99:2028-35.
28. Lai CJ, Yang CCH, Hsu YY. Enhanced sympathetic outflow and decreased baroreflex sensitivity are associated with intermittent hypoxia-induced systemic hypertension in conscious rats. J Appl Physiol. 2006, 100:1974-82.
29. De Frutos S, Duling L, Alo D. NFATc3 is required for intermittent hypoxia-induced hypertension. Am J Physiol Heart Circ Physiol. 2008, 294:H2382-90.
30. Savransky V, Nanayakkara A, Li J. Chronic intermittent hypoxia induces atherosclerosis. Am J Respir Crit Care Med. 2007, 175:1290-7.
31. Soukhova-O'Hare GK, Ortines RV, Gu Y. Postnatal intermittent hypoxia and developmental programming of hypertension in spontaneously hypertensive rats: the role of reactive oxygen species and L-Ca2+ channels. Hypertension. 2008, 52:156-62.
32. Tamisier R, Gilmartin GS, Launois SH. A new model of chronic intermittent hypoxia in humans: effect on ventilation, sleep and blood pressure. J Appl Physiol. 2009, 107:17-24.
33. Braga VA, Soriano RN, Machado BH. Sympathoexcitatory response to peripheral chemoreflex activation is enhanced in juvenile rats exposed to chronic intermittent hypoxia. Exp Physiol. 2006, 91:1025-31.
34. Dick TE, Hsieh YH, Wang N. Acute intermittent hypoxia increases both phrenic and sympathetic nerve activities in the rat. Exp Physiol. 2007, 92:87-97.
35. Fletcher EC. Effect of episodic hypoxia on sympathetic activity and blood pressure. Respir Physiol. 2000, 119:189-97.
36. Lesske J, Fletcher EC, Bao G. Hypertension caused by chronic intermittent hypoxia-influence of chemoreceptors and sympathetic nervous system. J Hypertens. 1997, 15:1593-603.
37. Zoccal DB, Bonagamba LGH, Oliveira FoRT. Increased sympathetic activity in rats submitted to chronic intermittent hypoxia. Exp Physiol. 2007, 92:79-85.
38. Zoccal DB, Simms AE, Bonagamba LGH. Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J Physiol. 2008, 586:3253-65.
39. Kumar GK, Rai V, Sharma SD. Chronic intermittent hypoxia induces hypoxia-evoked catecholamine efflux in adult rat adrenal medulla via oxidative stress. J Physiol. 2006, 575:229-39.
40. Bao G, Metreveli N, Li R. Blood pressure response to chronic episodic hypoxia: role of the sympathetic nervous system. J Appl Physiol. 1997, 83:95-101.
41. Kuri BA, Khan SA, Chan SA. Increased secretory capacity of mouse adrenal chromaffin cells by chronic intermittent hypoxia: involvement of protein kinase C. J Physiol. 2007, 584:313-9.
42. Souvannakitti D, Kumar GK, Fox A. Neonatal intermittent hypoxia leads to long-lasting facilitation of acute hypoxia-evoked catecholamine secretion from rat chromaffin cells. J Neurophysiol. 2009, 101:2837-46.
43. Soukhova-O'Hare GK, Cheng ZJ, Roberts AM. Postnatal intermittent hypoxia alters baroreflex function in adult rats. Am J Physiol Heart Circ Physiol. 2006, 290:H1157-64.
44. Peng YJ, Overholt JL, Kline D. Induction of sensory long-term facilitation in the carotid body by intermittent hypoxia: implications for recurrent apneas. Proc Natl Acad Sci USA. 2003, 100:10073-8.
45. Peng YJ, Yuan G, Ramakrishnan D. Heterozygous HIF-1[alpha] deficiency impairs carotid body-mediated systemic responses and reactive oxygen species generation in mice exposed to intermittent hypoxia. J Physiol Online. 2006, 577:705-16.
46. Greenberg HE, Sica AL, Scharf SM. Expression of c-fos in the rat brainstem after chronic intermittent hypoxia. Brain Res. 1999, 816:638-45.
47. Machaalani R, Waters KA. Increased neuronal cell death after intermittent hypercapnic hypoxia in the developing piglet brainstem. Brain Res. 2003, 985:127-34.
48. Sica AL, Greenberg HE, Scharf SM. Immediate-early gene expression in cerebral cortex following exposure to chronic-intermittent hypoxia. Brain Res. 2000, 870:204-10.
49. Zhu Y, Fenik P, Zhan G. Selective loss of catecholaminergic wake active neurons in a murine sleep apnea model. J Neurosci. 2007, 27:10060-71.
50. Ogawa S, Kitao Y, Hori O. Ischemia-induced neuronal cell death and stress response. Antioxid Redox Signal. 2007, 9:573-87.
51. Zhu Y, Fenik P, Zhan G. Eif-2a protects brainstem motoneurons in a murine model of sleep apnea. J Neurosci. 2008, 28:2168-78.
52. Raghuraman G, Rai V, Peng Y. Pattern-specific sustained activation of tyrosine hydroxylase by intermittent hypoxia: role of reactive oxygen species-dependent downregulation of protein phosphatase 2A and upregulation of protein kinases. Antioxid Redox Signal. 2009, 11:1777-89.
53. Sharma SD, Raghuraman G, Lee MS. Intermittent hypoxia activates peptidylglycine [alpha]-amidating monooxygenase in rat brain stem via reactive oxygen species-mediated proteolytic processing. J Appl Physiol. 2009, 106:12-9.
54. Fletcher EC, Lesske J, Behm R. Carotid chemoreceptors, systemic blood pressure, and chronic episodic hypoxia mimicking sleep apnea. J Appl Physiol. 1992, 72:1978-84.
55. Prabhakar NR, Peng YJ, Jacono FJ. Cardiovascular alterations by chronic intermittent hypoxia: importance of carotid body chemoreflexes. Clin Exp Pharmacol Physiol. 2005, 32:447-9.
56. Peng YJ, Prabhakar NR. Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J Appl Physiol. 2003, 94:2342-9.
57. Peng Y, Nanduri J, Yuan G. NADPH oxidase is required for the sensory plasticity of the carotid body by chronic intermittent hypoxia. J Neurosci. 2009, 29:4903-10.
58. Rey S, Iturriaga R. Endothelins and nitric oxide: vasoactive modulators of carotid body chemoreception. Curr Neurovasc Res. 2004, 1:465-73.
59. Rey S, Del Rio R, Iturriaga R. Contribution of endothelin-1 and endothelin A and B receptors to the enhanced carotid body chemosensory responses induced by chronic intermittent hypoxia. Adv Exp Med Biol. 2008, 605:228-32.
60. Rey S, Del Rio R, Iturriaga R. Contribution of endothelin-1 to the enhanced carotid body chemosensory responses induced by chronic intermittent hypoxia. Brain Res. 2006, 1086:152-9.
61. Liu Y, Ji ES, Xiang S. Exposure to cyclic intermittent hypoxia increases expression of functional NMDA receptors in the rat carotid body. J Appl Physiol. 2009, 106:259-67.
62. Row BW, Liu R, Xu W. Intermittent hypoxia is associated with oxidative stress and spatial learning deficits in the rat. Am J Respir Crit Care Med. 2003, 167:1548-53.
63. Troncoso Brindeiro CM, da Silva AQ, Allahdadi KJ. Reactive oxygen species contribute to sleep apnea-induced hypertension in rats. Am J Physiol Heart Circ Physiol. 2007, 293:H2971-6.
64. Fletcher EC, Bao G, Li R. Renin activity and blood pressure in response to chronic episodic hypoxia. Hypertension. 1999, 34:309-14.
65. Fletcher EC, Orolinova N, Bader M. Blood pressure response to chronic episodic hypoxia: the renin-angiotensin system. J Appl Physiol. 2002, 92:627-33.
66. Yuan ZM, Chen BY, Wang PX. Changes of angiotensin II and its receptor during the development of chronic intermittent hypoxia-induced hypertension in rats. Zhonghua Jie He He Hu Xi Za Zhi. 2004, 27:577-80.
67. Allahdadi KJ, Walker BR, Kanagy NL. Augmented endothelin vasoconstriction in intermittent hypoxia-induced hypertension. Hypertension. 2005, 45:705-9.
68. Allahdadi KJ, Cherng TW, Pai H. Endothelin type A receptor antagonist normalizes blood pressure in rats exposed to eucapnic intermittent hypoxia. Am J Physiol Heart Circ Physiol. 2008, 295:H434-40.
69. Belaidi E, Joyeux-Faure M, Ribuot C. Major role for hypoxia inducible factor-1 and the endothelin system in promoting myocardial infarction and hypertension in an animal model of obstructive sleep apnea. Journal of the American College of Cardiology. 2009, 53:1309-17.
70. Prabhakar NR, Kumar GK, Nanduri J. ROS signaling in systemic and cellular responses to chronic intermittent hypoxia. Antioxid Redox Signal. 2007, 9:1397-403.
71. Dyugovskaya L, Lavie P, Lavie L. Increased adhesion molecules expression and production of reactive oxygen species in leukocytes of sleep apnea patients. Am J Respir Crit Care Med. 2002, 165:934-9.
72. Sedeek M, Hebert RL, Kennedy CR. Molecular mechanisms of hypertension: role of Nox family NADPH oxidases. Curr Opin Nephrol Hypertens. 2009, 18:122-7.
73. Carriere A, Galinier A, Fernandez Y. [Physiological and physiopathological consequences of mitochondrial reactive oxygen species]. Med Sci. 2006, 22:47-53.
74. Wang W, Fang H, Groom L. Superoxide flashes in single mitochondria. Cell. 2008, 134:279-90.
75. Korge P, Ping P, Weiss JN. Reactive oxygen species production in energized cardiac mitochondria during hypoxia/reoxygenation: modulation by nitric oxide. Circ Res. 2008, 103:873-80.
76. Shan X, Chi L, Ke Y. Manganese superoxide dismutase protects mouse cortical neurons from chronic intermittent hypoxia-mediated oxidative damage. Neurobiology of Disease. 2007, 28:206-15.
77. Kim SY, Seo M, Kim Y. Stimulatory heterotrimeric GTP-binding protein inhibits hydrogen peroxide-induced apoptosis by repressing BAK induction in SH-SY5Y human neuroblastoma cells. J Biol Chem. 2008, 283:1350-61.
78. Han KY, Yang D, Chang EJ. Inhibition of osteoclast differentiation and bone resorption by sauchinone. Biochem Pharmacol. 2007, 74:911-23.
79. Porta S, Serra SA, Huch M. RCAN1 (DSCR1) increases neuronal susceptibility to oxidative stress: a potential pathogenic process in neurodegeneration. Hum Mol Genet. 2007, 16:1039-50.
80. Frossi B, Rivera J, Hirsch E. Selective activation of Fyn/PI3K and p38 MAPK regulates IL-4 production in BMMC under nontoxic stress condition. J Immunol. 2007, 178:2549-55.
81. Tu VC, Sun H, Bowden GT. Involvement of oxidants and AP-1 in angiotensin II-activated NFAT3 transcription factor. Am J Physiol Cell Physiol. 2007, 292:C1248-55.
82. Ke Q, Li J, Ding J. Essential role of ROS-mediated NFAT activation in TNF-[alpha] induction by crystalline silica exposure. Am J Physiol Lung Cell Mol Physiol. 2006, 291:L257-64.
83. Phillips SA, Olson EB, Lombard JH. Chronic intermittent hypoxia alters NE reactivity and mechanics of skeletal muscle resistance arteries. J Appl Physiol. 2006, 100:1117-23.
84. Earley S, Nelin LD, Chicoine LG. Hypoxia-induced pulmonary endothelin-1 expression is unaltered by nitric oxide. J Appl Physiol. 2002, 92:1152-8.
85. Gertler JP, Ocasio VH. Endothelin production by hypoxic human endothelium. J Vasc Surg. 1993, 18:178-82.
86. Kagamu H, Suzuki T, Arakawa M. Low oxygen enhances endothelin-1 (ET-1) production and responsiveness to ET-1 in cultured cardiac myocytes. Biochem Biophys Res Commun. 1994, 202:1612-8.
87. Kourembanas S, McQuillan LP, Leung GK. Nitric oxide regulates the expression of vasoconstrictors and growth factors by vascular endothelium under both normoxia and hypoxia. J Clin Invest. 1993, 92:99-104.
88. Kaehler J, Sill B, Koester R. Endothelin-1 mRNA and protein in vascular wall cells is increased by reactive oxygen species. Clin Sci. 2002, 103:176S-8S.
89. Pawar A, Nanduri J, Yuan G. Reactive oxygen species-dependent endothelin signaling is required for augmented hypoxic sensory response of the neonatal carotid body by intermittent hypoxia. Am J Physiol Regul Integr Comp Physiol. 2009, 296:R735-42.
90. Allahdadi KJ, Duling LC, Walker BR. Eucapnic intermittent hypoxia augments endothelin-1 vasoconstriction in rats: role of PKC[delta]. Am J Physiol Heart Circ Physiol. 2008, 294:H920-7.
91. Brezniceanu ML, Wei CC, Zhang SL. Transforming growth factor-beta 1 stimulates angiotensinogen gene expression in kidney proximal tubular cells. Kidney Int. 2006, 69:1977-85.
92. Hsieh TJ, Fustier P, Wei CC. Reactive oxygen species blockade and action of insulin on expression of angiotensinogen gene in proximal tubular cells. J Endocrinol. 2004, 183:535-50.
93. Hsu YH, Chen JJ, Chang NC. Role of reactive oxygen species-sensitive extracellular signal-regulated kinase pathway in angiotensin II-induced endothelin-1 gene expression in vascular endothelial cells. J Vasc Res. 2004, 41:64-74.
94. Knappe D, Sill B, Tharun B. Endothelin-1 in humans is increased by oxygen-derived radicals ex vivo and in vivo. J Investig Med. 2007, 55:306-14.
95. Sedeek MH, Llinas MT, Drummond H. Role of reactive oxygen species in endothelin-induced hypertension. Hypertension. 2003, 42:806-10.
96. Hanna IR, Taniyama Y, Szocs K. NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling. Antioxid Redox Signal. 2002, 4:899-914.
97. Weber DS, Rocic P, Mellis AM. Angiotensin II-induced hypertrophy is potentiated in mice overexpressing p22phox in vascular smooth muscle. Am J Physiol Heart Circ Physiol. 2005, 288:H37-42.
98. Wilcox CS. Reactive oxygen species: roles in blood pressure and kidney function. Curr Hypertens Rep. 2002, 4:160-6.
99. Moller DS, Lind P, Strunge B. Abnormal vasoactive hormones and 24-hour blood pressure in obstructive sleep apnea. Am J Hypertens. 2003, 16:274-80.
100. Takahashi S, Nakamura Y, Nishijima T. Essential roles of angiotensin II in vascular endothelial growth factor expression in sleep apnea syndrome. Respiratory Medicine. 2005, 99:1125-31.
101. Gjorup PH, Sadauskiene L, Wessels J. Abnormally increased endothelin-1 in plasma during the night in obstructive sleep apnea: relation to blood pressure and severity of disease. Am J Hypertens. 2007, 20:44-52.
102. Benjamin JA, Moller M, Ebden P. Serum angiotensin converting enzyme and the obstructive sleep apnea hypopnea syndrome. J Clin Sleep Med. 2008, 4:325-31.
103. Gjorup PH, Sadauskiene L, Wessels J. Increased nocturnal sodium excretion in obstructive sleep apnoea. Relation to nocturnal change in diastolic blood pressure. Scand J Clin Lab Invest. 2008, 68:11-21.
104. Kizawa T, Nakamura Y, Takahashi S. Pathogenic role of angiotensin II and oxidized LDL in obstructive sleep apnoea. Eur Respir J. 2009, [Epub ahead of print]
105. Sen R, Baltimore D. Inducibility of [kappa] immunoglobulin enhancer-binding protein NF-[kappa]B by a posttranslational mechanism. Cell. 1986, 47:921-8.
106. Fraser CC. G Protein-Coupled Receptor Connectivity to NF-kB in Inflammation and Cancer. Int Rev Immunol. 2008, 27:320-50.
107. Garvey JF, Taylor CT, McNicholas WT. Cardiovascular disease in obstructive sleep apnoea syndrome: the role of intermittent hypoxia and inflammation. Eur Respir J. 2009, 33:1195-205.
108. Ryan S, Taylor CT, McNicholas WT. Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation. 2005, 112:2660-7.
109. Ryan S, McNicholas WT, Taylor CT. A critical role for p38 map kinase in NF-[kappa]B signaling during intermittent hypoxia/reoxygenation. Biochem Biophys Res Commun. 2007, 355:728-33.
110. Ryan S, Taylor CT, McNicholas WT. Predictors of elevated nuclear factor-[kappa]b-dependent genes in obstructive sleep apnea syndrome. Am J Respir Crit Care Med. 2006, 174:824-30.
111. Greenberg H, Ye X, Wilson D. Chronic intermittent hypoxia activates nuclear factor-[kappa]B in cardiovascular tissues in vivo. Biochem Biophys Res Commun. 2006, 343:591-6.
112. Htoo A, Greenberg H, Tongia S. Activation of nuclear factor kB in obstructive sleep apnea: a pathway leading to systemic inflammation. Sleep Breath. 2006, 10:43-50.
113. Foncea R, Carvajal C, Almarza C. Endothelial cell oxidative stress and signal transduction. Biol Res. 2000, 33:89-96.
114. Lavie L. Sleep-disordered breathing and cerebrovascular disease: a mechanistic approach. Neurologic Clinics. 2005, 23:1059-75.
115. Hill-Eubanks DC, Gomez MF, Stevenson AS. NFAT Regulation in Smooth Muscle. Trends Cardiovasc Med. 2003, 13:56-62.
116. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol. 1997, 15:707-47.
117. Decker EL, Skerka C, Zipfel PF. The early growth response protein (EGR-1) regulates interleukin-2 transcription by synergistic interaction with the nuclear factor of activated T cells. J Biol Chem. 1998, 273:26923-30.
118. Decker EL, Nehmann N, Kampen E. Early growth response proteins (EGR) and nuclear factors of activated T cells (NFAT) form heterodimers and regulate proinflammatory cytokine gene expression. Nucleic Acids Res. 2003, 31:911-21.
119. Chen L, Glover JN, Hogan PG. Structure of the DNA-binding domains from NFAT, Fos and Jun bound specifically to DNA. Nature. 1998, 392:42-8.
120. Macian F, Lopez-Rodriguez C, Rao A. Partners in transcription: NFAT and AP-1. Oncogene. 2001, 20:2476-89.
121. Sweetser MT, Hoey T, Sun YL. The roles of nuclear factor of activated T cells and ying-yang 1 in activation-induced expression of the interferon-gamma promoter in T cells. J Biol Chem. 1998, 273:34775-83.
122. Crabtree GR, Olson EN. NFAT signaling: choreographing the social lives of cells. Cell. 2002, 109:S67-79.
123. McKinsey TA, Zhang CL, Olson EN. MEF2: a calcium-dependent regulator of cell division, differentiation and death. Trends Biochem Sci. 2002, 27:40-7.
124. Olson EN, Williams RS. Calcineurin signaling and muscle remodeling. Cell. 2000, 101:689-92.
125. Molkentin JD, Lu JR, Antos CL. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 1998, 93:215-28.
126. Wada H, Hasegawa K, Morimoto T. Calcineurin-GATA-6 pathway is involved in smooth muscle-specific transcription. J Cell Biol. 2002, 156:983-91.
127. Hogan PG, Chen L, Nardone J. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 2003, 17:2205-32.
128. Amberg GC, Rossow CF, Navedo MF. NFATc3 regulates Kv2.1 expression in arterial smooth muscle. J Biol Chem. 2004, 279:47326-34.
129. Chen J, Amasaki Y, Kamogawa Y. Role of NFATx (NFAT4/NFATc3) in expression of immunoregulatory genes in murine peripheral CD4+ T cells. J Immunol. 2003, 170:3109-17.
130. Han S, Lu J, Zhang Y. Recruitment of histone deacetylase 4 by transcription factors represses interleukin-5 transcription. Biochem J. 2006, 400:439-48.
131. Nieves-Cintron M, Amberg GC, Nichols CB. Activation of NFATC3 down-regulates the beta 1 subunit of large conductance, calcium-activated K+ channels in arterial smooth muscle and contributes to hypertension. J Biol Chem. 2006, 282:3231-40.
132. Stevenson AS, Gomez MF, Hill-Eubanks DC. NFAT4 movement in native smooth muscle. A role for differential Ca(2+) signaling. J Biol Chem. 2001, 276:15018-24.
133. Gomez MF, Stevenson AS, Bonev AD. 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, 277:37756-64.
134. Gomez MF, Gonzalez Bosc LV, Stevenson AS. 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, 278:46847-53.
135. Gonzalez Bosc LV, Wilkerson MK, Bradley KN. Intraluminal pressure is a stimulus for NFATc3 nuclear accumulation - Role of calcium, endothelium-derived nitric oxide, and cGMP-dependent protein kinase. J Biol Chem. 2004, 279:10702-9.
136. Nilsson J, Nilsson LM, Chen YW. High glucose activates nuclear factor of activated t cells in native vascular smooth muscle. Arterioscler Thromb Vasc Biol. 2006, 26:794-800.
137. Graef IA, Chen F, Crabtree GR. NFAT signaling in vertebrate development. Curr Opin Genet Dev. 2001, 11:505-12.
138. Graef IA, Chen F, Chen L. Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell. 2001, 105:863-75.
139. Ohkawa Y, Hayashi K, Sobue K. Calcineurin-mediated pathway involved in the differentiated phenotype of smooth muscle cells. Biochem Biophys Res Commun. 2003, 301:78-83.
140. Gonzalez Bosc LV, Layne J, Nelson MT. Nuclear factor of activated T-cells and serum response factor cooperatively regulate an α-actin intronic enhancer. J Biol Chem. 2004, 280:26113-20.
141. Layne JJ, Werner ME, Hill-Eubanks DC. NFATc3 regulates BK channel function in murine urinary bladder smooth muscle. Am J Physiol Cell Physiol. 2008, 295:C611-23.
142. Boss V, Abbott KL, Wang XF. The cyclosporin A-sensitive nuclear factor of activated T cells (NFAT) proteins are expressed in vascular smooth muscle cells. Differential localization of NFAT isoforms and induction of NFAT-mediated transcription by phospholipase C-coupled cell surface receptors. J Biol Chem. 1998, 273:19664-71.
143. De Frutos S, Spangler R, Alo D. NFATc3 mediates chronic hypoxia-induced pulmonary arterial remodeling with alpha -actin up-regulation. J Biol Chem. 2007, 282:15081-9.
144. Kaminuma O, Kitamura F, Kitamura N. Differential contribution of NFATc2 and NFATc1 to TNF-alpha gene expression in T cells. J Immunol. 2008, 180:319-26.
145. Nilsson LM, Sun ZW, Nilsson J. Novel blocker of NFAT activation inhibits IL-6 production in human myometrial arteries and reduces vascular smooth muscle cell proliferation. Am J Physiol Cell Physiol. 2007, 292:C1167-78.
146. Weigmann B, Lehr HA, Yancopoulos G. The transcription factor NFATc2 controls IL-6-dependent T cell activation in experimental colitis. J Exp Med. 2008, 205:2099-110.
147. Nilsson LM. Nuclear Factor of Activated T-Cells is involved in the regulation of osteopontin expression in vascular smooth muscle. FASEB J. 2007, 21. 905.20
148. Alberti A, Sarchielli P, Gallinella E. Plasma cytokine levels in patients with obstructive sleep apnea syndrome: a preliminary study. J Sleep Res. 2003, 12:305-11.
149. Yudkin JS, Kumari M, Humphries SE. Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link. Atherosclerosis. 2000, 148:209-14.
150. Lindmark E, Diderholm E, Wallentin L. Relationship between interleukin 6 and mortality in patients with unstable coronary artery disease: effects of an early invasive or noninvasive strategy. JAMA. 2001, 286:2107-13.
151. Ridker PM, Rifai N, Stampfer MJ. Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation. 2000, 101:1767-72.
152. Scatena M, Liaw L, Giachelli CM. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol. 2007, 27:2302-9.
153. Graf K, Do YS, Ashizawa N. Myocardial osteopontin expression is associated with left ventricular hypertrophy. Circulation. 1997, 96:3063-71.
154. Kurata M, Okura T, Watanabe S. Osteopontin and carotid atherosclerosis in patients with essential hypertension. Clin Sci. 2006, 111:319-24.
155. Ohmori R, Momiyama Y, Taniguchi H. Plasma osteopontin levels are associated with the presence and extent of coronary artery disease. Atherosclerosis. 2003, 170:333-7.
156. Uenoyama M, Ogata S, Nakanishi K. Osteopontin expression in normal and hypobaric hypoxia-exposed rats. Acta physiologica. 2008, 193:291-301.
157. Denhardt DT, Giachelli CM, Rittling SR. Role of osteopontin in cellular signaling and toxicant injury. Annu Rev Pharmacol Toxicol. 2001, 41:723-49.
158. Denhardt DT, Noda M, O'Regan AW. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. J Clin Invest. 2001, 107:1055-61.
159. Nau GJ, Guilfoile P, Chupp GL. A chemoattractant cytokine associated with granulomas in tuberculosis and silicosis. Proc Natl Acad Sci USA. 1997, 94:6414-9.
160. Vaschetto R, Nicola S, Olivieri C. Serum levels of osteopontin are increased in SIRS and sepsis. Intensive Care Med. 2008, 34:2176-84.
161. Muteliefu G, Enomoto A, Jiang P. Indoxyl sulphate induces oxidative stress and the expression of osteoblast-specific proteins in vascular smooth muscle cells. Nephrol Dial Transplant. 2009, 24:2051-8.
162. Hu T, Luan R, Zhang H. Hydrogen peroxide enhances the osteopontin expression and matrix metalloproteinase activity in aortic vascular smooth muscle cells. Clin Exp Pharmacol Physiol. 2008, 36:626-30.
163. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992, 12:5447-54.
164. Semenza GL, Agani F, Booth G. Structural and functional analysis of hypoxia-inducible factor 1. Kidney Int. 1997, 51:553-5.
165. Ivan M, Haberberger T, Gervasi DC. Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc Natl Acad Sci USA. 2002, 99:13459-64.
166. Papandreou I, Cairns RA, Fontana L. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metabolism. 2006, 3:187-97.
167. Fandrey J. Oxygen-dependent and tissue-specific regulation of erythropoietin gene expression. Am J Physiol Regul Integr Comp Physiol. 2004, 286:R977-88.
168. Snow JB, Kitzis V, Norton CE. Differential effects of chronic hypoxia and intermittent hypocapnic and eucapnic hypoxia on pulmonary vasoreactivity. J Appl Physiol. 2008, 104:110-8.
169. Hoffstein V, Herridge M, Mateika S. Hematocrit levels in sleep apnea. Chest. 1994, 106:787-91.
170. Cramer T, Yamanishi Y, Clausen BrE. HIF-1[alpha] is essential for myeloid cell-mediated inflammation. Cell. 2003, 112:645-57.
171. Imagawa S, Yamaguchi Y, Higuchi M. Levels of vascular endothelial growth factor are elevated in patients with obstructive sleep apnea-hypopnea syndrome. Blood. 2001, 98:1255-7.
172. Cummins E, Taylor C. Hypoxia-responsive transcription factors. Pflugers Arch. 2005, 450:363-71.
173. Yuan G, Nanduri J, Bhasker CR. Ca2+/Calmodulin kinase-dependent activation of hypoxia inducible factor 1 transcriptional activity in cells subjected to intermittent hypoxia. J Biol Chem. 2005, 280:4321-8.
174. Toffoli S Ã, Roegiers A, Feron O. Intermittent hypoxia is an angiogenic inducer for endothelial cells: role of HIF-1. Angiogenesis. 2009, 12:47-67.
175. Hu J, Discher DJ, Bishopric NH. Hypoxia regulates expression of the endothelin-1 gene through a proximal hypoxia-inducible factor-1 binding site on the antisense strand. Biochem Biophys Res Commun. 1998, 245:894-9.
176. Minchenko A, Caro J. Regulation of endothelin-1 gene expression in human microvascular endothelial cells by hypoxia and cobalt: role of hypoxia responsive element. Mol Cell Biochem. 2000, 208:53-62.
177. Yamashita K, Discher DJ, Hu J. Molecular regulation of the endothelin-1 gene by hypoxia. Contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2, and p300/CBP. J Biol Chem. 2001, 276:12645-53.
178. Lam SY, Tipoe GL, Liong EC. Hypoxia-inducible factor (HIF)-1alpha and endothelin-1 expression in the rat carotid body during intermittent hypoxia. Adv Exp Med Biol. 2006, 580:21-7.
179. Yuan G, Nanduri J, Khan S. Induction of HIF-1alpha expression by intermittent hypoxia: involvement of NADPH oxidase, Ca2+ signaling, prolyl hydroxylases, and mTOR. J Cell Physiol. 2008, 217:674-85.
180. Bonello S, Zahringer C, Belaiba RS. Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol. 2007, 27:755-61.
181. Gorlach A, Bonello S. The cross-talk between NF-kappaB and HIF-1: further evidence for a significant liaison. Biochem J. 2008, 412:e17-9.
182. Rius J, Guma M, Schachtrup C. NF-[κ]B links innate immunity to the hypoxic response through transcriptional regulation of HIF-1[α]. Nature. 2008, 453:807-11.
183. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 1997, 11:72-82.
184. Ema M, Taya S, Yokotani N. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA. 1997, 94:4273-8.
185. Holmquist-Mengelbier L, Fredlund E, Löfstedt T. Recruitment of HIF-1[alpha] and HIF-2[alpha] to common target genes is differentially regulated in neuroblastoma: HIF-2[alpha] promotes an aggressive phenotype. Cancer Cell. 2006, 10:413-23.
186. Nanduri J, Wang N, Yuan G. Intermittent hypoxia degrades HIF-2+ via calpains resulting in oxidative stress: implications for recurrent apnea-induced morbidities. Proc Natl Acad Sci USA. 2009, 106:1199-204.
187. Sajkov D, Mcevoy RD. Obstructive sleep apnea and pulmonary hypertension. Prog Cardiovasc Dis. 2009, 51:363-70.
188. Schafer H, Hasper E, Ewig S. Pulmonary haemodynamics in obstructive sleep apnoea: time course and associated factors. Eur Respir J. 1998, 12:679-84.
189. Weitzenblum E, Chaouat A, Kessler R. Overlap syndrome: obstructive sleep apnea in patients with chronic obstructive pulmonary disease. Proc Am Thorac Soc. 2008, 5:237-41.
190. Somers VK, White DP, Amin R. Sleep apnea and cardiovascular disease. An American Heart Association/American College of Cardiology Foundation Scientific Statement From the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council on Cardiovascular Nursing Council. Circulation. 2008, 118:1080-111.
191. Sajkov D, Wang T, Saunders NA. Continuous positive airway pressure treatment improves pulmonary hemodynamics in patients with obstructive sleep apnea. Am J Respir Crit Care Med. 2002, 165:152-8.
192. Arias MA, Garcia-Rio F, Alonso-Fernandez A. Pulmonary hypertension in obstructive sleep apnoea: effects of continuous positive airway pressure: a randomized, controlled cross-over study. Eur Heart J. 2006, 27:1106-13.
193. Alchanatis M, Tourkohoriti G, Kakouros S. Daytime pulmonary hypertension in patients with obstructive sleep apnea: the effect of continuous positive airway pressure on pulmonary hemodynamics. Respiration. 2001, 68:566-72.
194. Zielinski J. Effects of intermittent hypoxia on pulmonary haemodynamics: animal models versus studies in humans. Eur Respir J. 2005, 25:173-80.
195. Sanner BM, Doberauer C, Konermann M. Pulmonary hypertension in patients with obstructive sleep apnea syndrome. Arch Intern Med. 1997, 157:2483-7.
196. Bady E, Achkar A, Pascal S. Pulmonary arterial hypertension in patients with sleep apnoea syndrome. Thorax. 2000, 55:934-9.
197. Shahar E, Whitney CW, Redline S. Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med. 2001, 163:19-25.
198. Golbin JM, Somers VK, Caples SM. Obstructive sleep apnea, cardiovascular disease, and pulmonary hypertension. Proc Am Thorac Soc. 2008, 5:200-6.
199. Bradford A. Effects of chronic intermittent asphyxia on haematocrit, pulmonary arterial pressure and skeletal muscle structure in rats. Exp Physiol. 2004, 89:44-52.
200. Fagan KA. Selected contribution: pulmonary hypertension in mice following intermittent hypoxia. J Appl Physiol. 2001, 90:2502-7.
201. Nisbet RE, Graves AS, Kleinhenz DJ. The role of NADPH oxidase in chronic intermittent hypoxia-induced pulmonary hypertension in mice. Am J Respir Cell Mol Biol. 2009, 40:601-9.
202. Fletcher EC, Bao G, Miller CC. Effect of recurrent episodic hypocapnic, eucapnic, and hypercapnic hypoxia on systemic blood pressure. J Appl Physiol. 1995, 78:1516-21.
203. Resta TC, Chicoine LG, Omdahl JL. Maintained upregulation of pulmonary eNOS gene and protein expression during recovery from chronic hypoxia. Am J Physiol Heart Circ Physiol. 1999, 276:H699-708.
204. Nagaoka T, Fagan KA, Gebb SA. Inhaled Rho kinase inhibitors are potent and selective vasodilators in rat pulmonary hypertension. Am J Respir Crit Care Med. 2005, 171:494-9.
205. Nagaoka T, Morio Y, Casanova N. Rho/Rho kinase signaling mediates increased basal pulmonary vascular tone in chronically hypoxic rats. Am J Physiol Lung Cell Mol Physiol. 2004, 287:L665-72.
206. Broughton BR, Walker BR, Resta TC. Chronic hypoxia induces Rho kinase-dependent myogenic tone in small pulmonary arteries. Am J Physiol Lung Cell Mol Physiol. 2008, 294:L797-806.
207. Jernigan NL, Walker BR, Resta TC. Reactive oxygen species mediate RhoA/Rho kinase-induced Ca2+ sensitization in pulmonary vascular smooth muscle following chronic hypoxia. Am J Physiol Lung Cell Mol Physiol. 2008, 295:L515-29.
208. Jernigan NL, Walker BR, Resta TC. Endothelium-derived reactive oxygen species and endothelin-1 attenuate NO-dependent pulmonary vasodilation following chronic hypoxia. Am J Physiol Lung Cell Mol Physiol. 2004, 287:L801-8.
209. Paffett ML, Naik JS, Resta TC. Reduced store-operated Ca2+ entry in pulmonary endothelial cells from chronically hypoxic rats. Am J Physiol Lung Cell Mol Physiol. 2007, 293:L1135-42.
210. Murata T, Sato K, Hori M. Decreased endothelial nitric-oxide synthase (eNOS) activity resulting from abnormal interaction between eNOS and its regulatory proteins in hypoxia-induced pulmonary hypertension. J Biol Chem. 2002, 277:44085-92.
211. Dicarlo VS, Chen SJ, Meng QC. ETA-receptor antagonist prevents and reverses chronic hypoxia-induced pulmonary hypertension in rat. Am J Physiol. 1995, 269:L690-7.
212. Bonvallet ST, Zamora MR, Hasunuma K. BQ123, an ETA-receptor antagonist, attenuates hypoxic pulmonary hypertension in rats. Am J Physiol Heart Circ Physiol. 1994, 266:H1327-31.
213. Chen SJ, Chen YF, Meng QC. Endothelin-receptor antagonist bosentan prevents and reverses hypoxic pulmonary hypertension in rats. J Appl Physiol. 1995, 79:2122-31.
214. Snow J, Kanagy N, Walker B. Intermittent hypoxia increases PKCα/β- and reactive oxygen species dependent myofilament Ca2+ sensitization in small pulmonary arteries. FASEB J. 2009, 23. 770.6
215. Liu JQ, Zelko IN, Erbynn EM. Hypoxic pulmonary hypertension: role of superoxide and NADPH oxidase (gp91phox). Am J Physiol Lung Cell Mol Physiol. 2006, 290:L2-10.
216. Elmedal B, de Dam MY, Mulvany MJ. The superoxide dismutase mimetic, tempol, blunts right ventricular hypertrophy in chronic hypoxic rats. Br J Pharmacol. 2004, 141:105-13.
217. Matsui H, Shimosawa T, Itakura K. Adrenomedullin can protect against pulmonary vascular remodeling induced by hypoxia. Circulation. 2004, 109:2246-51.
218. Grobe AC, Wells SM, Benavidez E. Increased oxidative stress in lambs with increased pulmonary blood flow and pulmonary hypertension: role of NADPH oxidase and endothelial NO synthase. Am J Physiol Lung Cell Mol Physiol. 2006, 290:L1069-77.
219. Fresquet F, Pourageaud F, Leblais V. Role of reactive oxygen species and gp91phox in endothelial dysfunction of pulmonary arteries induced by chronic hypoxia. Br J Pharmacol. 2006, 148:714-23.
220. Brennan LA, Steinhorn RH, Wedgwood S. Increased superoxide generation is associated with pulmonary hypertension in fetal lambs: a role for NADPH oxidase. Circ Res. 2003, 92:683-91.
221. Fike CD, Slaughter JC, Kaplowitz MR. Reactive oxygen species from NADPH oxidase contribute to altered pulmonary vascular responses in piglets with chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol. 2008, 295:L881-8.
222. Hoshikawa Y, Ono S, Suzuki S. Generation of oxidative stress contributes to the development of pulmonary hypertension induced by hypoxia. J Appl Physiol. 2001, 90:1299-306.
223. Jankov RP, Kantores C, Pan J. Contribution of xanthine oxidase-derived superoxide to chronic hypoxic pulmonary hypertension in neonatal rats. Am J Physiol Lung Cell Mol Physiol. 2008, 294:L233-45.
224. Shimoda LA, Manalo DJ, Sham JSK. Partial HIF-1[alpha] deficiency impairs pulmonary arterial myocyte electrophysiological responses to hypoxia. Am J Physiol Lung Cell Mol Physiol. 2001, 281:L202-8.
225. Alford NJ, Fletcher EC, Nickeson D. Acute oxygen in patients with sleep apnea and COPD. Chest. 1986, 89:30-8.
226. Ooi H, Cadogan E, Sweeney M. Chronic hypercapnia inhibits hypoxic pulmonary vascular remodeling. Am J Physiol Heart Circ Physiol. 2000, 278:H331-8.
227. Kantores C, McNamara PJ, Teixeira L. Therapeutic hypercapnia prevents chronic hypoxia-induced pulmonary hypertension in the newborn rat. Am J Physiol Lung Cell Mol Physiol. 2006, 291:L912-22.