The effect of chronic long-term intermittent hypobaric hypoxia on bone mineral density in rats: Role of nitric oxide

Biological Trace Element Research

Volumn 154, Issue 2, 2013, Pages 262-267

  Guner, Ibrahim ^a   Uzun, Duygu D ^a   Yaman, Muhittin O ^a   Genc, Habibe ^a   Gelisgen, Remisa ^a   Korkmaz, Gulcan G ^b   Hallac, Metin ^a   Yelmen, Nermin ^a   Sahin, Gulderen ^a   Karter, Yesari ^a   Simsek, Gonul ^a  

^a ISTANBUL UNIVERSITY   (Turkey)

^b KIRKLARELI UNIVERSITY   (Turkey)

Author keywords

Bone metabolism; Bone mineral density; Cytokines; Intermittent hypoxia; l NAME; Nitric oxide

Indexed keywords

ALKALINE PHOSPHATASE BONE ISOENZYME; CALCIUM; INTERLEUKIN 1BETA; INTERLEUKIN 6; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PARATHYROID HORMONE; PHOSPHATE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BONE DENSITY; BONE METABOLISM; CALCIUM BLOOD LEVEL; CHRONIC INTERMITTENT HYPOXIA; CHRONIC LONG TERM INTERMITTENT HYPOBARIC HYPOXIA; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME BLOOD LEVEL; MALE; MOLECULAR DYNAMICS; NONHUMAN; PARATHYROID HORMONE BLOOD LEVEL; PHOSPHATE BLOOD LEVEL; RAT;

ALKALINE PHOSPHATASE; ANIMALS; ANOXIA; BONE DENSITY; CHRONIC DISEASE; CYTOKINES; ENZYME INHIBITORS; HUMANS; MALE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; PARATHYROID HORMONE; RATS; RATS, WISTAR; TIME FACTORS;

ANIMALIA; RATTUS;

EID: 84880284566     PISSN: 01634984     EISSN: 15590720     Source Type: Journal    
DOI: 10.1007/s12011-013-9722-8     Document Type: Article

References (63)

1. Neubauer JA (2001) Physiological and pathophysiological responses to intermittent hypoxia. J Appl Physiol 90:1593-1599
2. Dempsey JA, Hanson PG, Henderson KS (1984) Exercise induced arterial hypoxemia in healthy human subjects at sea level. J Physiol 355:161-175
3. Cottrell JJ (1998) Altitude exposures during aircraft flight: flying higher. Chest 93:81-84
4. Hurtado A (1960) Some clinical aspects of life at high altitudes. Ann Intern Med 53:247-258
5. McNicholas WT (1990) Sleep apnea. J Ir Coll Phys Surg 19:53-56
6. Zhang Y, Zhong N, Gia J, Zhou Z (2004) Effects of chronic intermittent hypoxia on the hemodynamics of systemic circulation in rats. Jpn J Physiol 54:171-174
7. Anatskaya OV, Vinogradov AE (2007) Genome multiplication as adaptation to tissue survival: evidence from gene expression in mammalian heart and liver. Genomics 89:70-80
8. Zhu XH, Yan HC, Zhang J, Qu HD, Qiu XS, Chen L, Li SJ, Cao X, Bean JC, Chen LH, Qin XH, Liu JH, Bai XC, Mei L, Gao TM (2010) Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci 30:12653-12663
9. Serebrovskaya TV, Swanson RJ, Kolesnikova EE (2003) Intermittent hypoxia: mechanisms of action and some applications to bronchial asthma treatment. J Physiol Pharmacol 54:35-41
10. Shi M, Cui F, Liu AJ, Li J, Ma HJ, Cheng M, Yang J, Zhang Y (2011) Protection of chronic intermittent hypobaric hypoxia against collagen-induced arthritis in rat through increasing apoptosis. Acta Physiol Sin 63:115-123
11. Roels B, Bentley DJ, Coste O, Mercier J, Millet GP (2007) Effects of intermittent hypoxic training on cycling performance in well-trained athletes. Eur J Appl Physiol 101:359-368
12. Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, Meghji S (2003) Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol 196:2-8
13. Utting JC, Robins SP, Brandao-Burch A, Orriss IR, Behar J, Arnett TR (2006) Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 312:1693-1702
14. Papaioannou A, Parkinson W, Ferko N, Probyn L, Ioannidis G, Jurriaans E, Cox G, Cook RJ, Kumbhare D, Adachi JD (2003) Prevalence of vertebral fracture among patients with chronic obstructive pulmonary disease in Canada. Osteoporos Int 14:913-917
15. Miller RG, Segal JB, Ashar BH, Leung S, Ahmed S, Siddique S, Rice T, Lanzkron S (2006) High prevalence and correlates of low bone mineral density in young adults with sickle cell disease. Am J Hematol 81:236-241
16. Mineo TC, Ambrogi V, Mineo D, Fabbri A, Fabbrini E, Massoud R (2005) Bone mineral density improvement after lung volume reduction surgery for severe emphysema. Chest 127:1960-1966
17. Agusti AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X (2003) Systemic effects of chronic obstructive pulmonary disease. Eur Respir J 21:347-360
18. Manukhina EB, Downey HF, Mallet RT (2006) Role of nitric oxide in cardiovascular. Exp Biol Med 231:343-365
19. Hukkanen M, Platts LAM, Lawes T, Girgis SI, Konttinen YT, Goodship AE, MacIntyre I, Polak JM (2003) Effect of nitric oxidedonor nitroglycerin on bone mineral density in a rat model of estrogen deficiency-induced osteopenia. Bone 32:142-149
20. Simsek G, Uzun H, Aydin S, Karter Y, Benian A, Dariyerli N, Kaya S, Yigit G (2005) The role of nitricoxide on bone metabolism in ovariectomized rats following chronic ethanol intake. Life Sci 76:1965-1974
21. Guner I, Yelmen N, Sahin G, Oruc T, Sipahi S, Yaman MO (2007) Respiratory alterations due to chronic long-term intermittent hypobaric hypoxia in rabbits; importance of peripheral chemoreceptors. Arch Med Res 38:739-745
22. Yelmen N, Ozdemir S, Guner I, Toplan S, Sahin G, Yaman MO, Sipahi S (2011) The effects of chronic long-term intermittent hypobaric hypoxia on blood rheology parameters. Gen Physiol Biophys 30:389-395
23. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1996) Analysis of nitrate, nitrite, and [15N] nitrate in biological fluids. Anal Biochem 126:131-138
24. Pumarino H, Pumarino MG (1996) Cytokines, growth factors and metabolic bone disease. Rev Med Chil 124:248-257
25. Simsek G, Karter Y, Aydin S, Uzun H (2003) Osteoporotic cytokines and bone metabolism on rats with induced hyperthyroidism; changes as a result of reversal to euthyroidism. Chin J Physiol 46:181-186
26. Sozer V, Uzun H, Guner I, Aydin S, Yucel R, Karter Y, Simsek C, Kaya S, Yigit G, Simsek G (2006) Bone metabolism in ovariectomized rats with induced hyperthyroidism: the effect of estrogen replacement. Chin J Physiol 49:335-341
27. Gregory R, Mundy MD (2007) Osteoporosis and inflammation. Nutr Rev 65:S147-S151
28. McLean RR (2009) Proinflammatory cytokines and osteoporosis. Curr Osteoporos Rep 7:134-139
29. Kwan Tat S, Padrines M, Théoleyre S, Heymann D, Fortun Y (2004) IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev 15:49-60
30. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D (2004) The molecular triad OPG/RANK/RANKL: involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev 15:457-475
31. Bai P, Sun Y, Jin J, Hou J, Li R, Zhang Q, Wang Y (2011) Disturbance of the OPG/RANK/RANKL pathway and systemic inflammation in COPD patients with emphysema and osteoporosis. Respir Res 12:157
32. Khosla S (2001) Minireview: the OPG/RANKL/RANK system. Endocrinology 142:5050-5055
33. Tanaka S, Nakamura K, Takahasi N, Suda T (2005) Role of RANKL in physiological and pathological bone resorption and therapeutics targeting the RANKL-RANK signaling system. Immunol Rev 208:30-49
34. Lam SY, Liu Y, Ng KM, Lau CF, Liong EC, Tipoe GL, Fung ML (2012) Chronic intermittent hypoxia induces local inflammation of the rat carotid body via functional upregulation of proinflammatory cytokine pathways. Histochem Cell Biol 137:303-317
35. Kubes P, McCafferty DM (2000) Nitric oxide and intestinal inflammation. Am J Med 109:150-158
36. Damoulis PD, Hauschka PV (1994) Cytokines induce nitric oxide production in mouse osteoblasts. Biochem Biophys Res Commun 201:924-931
37. Ralston SH, Ho LP, Helfrich MH, Grabowski PS, Johnston PW, Benjamin N (1995) Nitric oxide: a cytokine-induced regulator of bone resorption. J Bone Miner Res 10:1040-1049
38. van't Hof RJ, Ralston SH (1997) Cytokine-induced nitric oxide inhibits bone resorption by inducing apoptosis of osteoclast progenitors and suppressing osteoclast activity. J Bone Miner Res 12:1797-1804
39. van't Hof RJ, Ralston SH (2001) Nitric oxide and bone. Immunology 103:255-261
40. Riancho JA, Zarrabeitia MT, Fernandez-Luna JL, Gonzalez-Macias J (1995) Mechanisms controlling nitric oxide synthesis in osteoblasts. Mol Cell Endocrinol 107:87-92
41. Garnero P, Vassy V, Bertholin A, Riou JP, Delmas PD (1994) Markers of bone turnover in hyperthyroidism and the effects of treatment. J Clin Endocrinol Metab 78:955-959
42. Fan X, Rahnert JA, Murphy TC, Nanes MS, Greenfield EM, Rubin J (2006) Response to mechanical strain in an immortalized pre-osteoblast cell is dependent on ERK1/2. J Cell Physiol 207:454-460
43. Wang J, Shang F, Mei Q, Wang J, Zhang R, Wang S (2008) NO-donating genistein prodrug alleviates bone loss in ovariectomised rats. Swiss Med Wkly 138:602-607
44. Rahnert J, Fan X, Case N, Murphy TC, Grassi F, Sen B, Rubin J (2008) The role of nitric oxide in the mechanical repression of RANKL in bone stromal cells. Bone 43:48-54
45. Tomiyama H, Okazaki R, Inoue D, Ochiai H, Shiina K, Takata Y, Hashimoto H, Yamashina A (2008) Link between obstructive sleep apnea and increased bone resorption in men. Osteoporos Int 19:1185-1192
46. Litovka IH (2008) Alimentary and oxygen deprivation as the modulator of the bone tissue physiological remodelling rate in young rats (Ukrainian article, English abstract). Fiziol Zh 54:85-93
47. Ralston SH, Grabowski PS (1996) Mechanisms of cytokine induced bone resorption: role of nitric oxide, cyclic guanosine monophosphate, and prostaglandins. Bone 19:29-33
48. Holliday LS, Dean AD, Lin RH, Greenwald JE, Gluck SL (1997) Low NO concentrations inhibit osteoclast formation in mouse marrow cultures by cGMP-dependent mechanism. Am J Physiol 272:F283-F291
49. Fan X, Roy E, Zhu L, Murphy TC, Ackert-Bicknell C, Hart CM, Rosen C, Nanes MS, Rubin J (2004) Nitric oxide regulates receptor activator of nuclear factor-kappa B ligand and osteoprotegerin expression in bone marrow stromal cells. Endocrinology 145:751-759
50. Zheng H, Yu X, Collin-Osdoby P, Osdoby P (2006) RANKL stimulates inducible nitric-oxide synthase expression and nitric oxide production in developing osteoclasts. An autocrine negative feedback mechanism triggered by RANKL-induced interferon-beta via NF-kappaB that restrains osteoclastogenesis and bone resorption. J Biol Chem 281:15809-15820
51. Rosselli M, Imthurn B, Keller PJ, Jackson EK, Dubey RK (1995) Circulating nitric oxide (nitrite/nitrate) levels in postmenopausal women substituted with 17 beta-estradiol and norethisterone acetate. A two-year follow-up study. Hypertension 25:848-853
52. Cicinelli E, Ignarro LJ, Lograno M, Matteo G, Falco N, Schonauer LM (1997) Acute effects of transdermal estradiol administration on plasma levels of nitric oxide in postmenopausal women. Fertil Steril 67:63-66
53. Cicinelli E, Ignarro LJ, Schonauer LM, Matteo MG, Galantino P, Balzano G (1998) Effects of short-term transdermal estradiol administration on plasma levels of nitric oxide in postmenopausal women. Fertil Steril 69:58-61
54. Stacey E, Korkia P, Hukkanen MV, Polak JM, Rutherford OM (1998) Decreased nitric oxide levels and bone turnover in amenorrheic athletes with spinal osteopenia. J Clin Endocrinol Metab 83:3056-3061
55. Elshal MF, Bernawi AE, Al-Ghamdy MA, Jalal JA (2012) The association of bone mineral density and parathyroid hormone with serum magnesium in adult patients with sickle-cell anaemia. Arch Med Sci 8:270-276
56. Simsek G, Andican G, Unal E, Hatemi H, Yigit G, Candan G (1997) Calcium, magnesium, and zinc status in experimental hyperthyroidism. Biol Trace Elem Res 57:131-137
57. Simsek G, Uzun H, Karter Y, Aydin S, Yigit G (2003) Effects of osteoporotic cytokines in ovary-intact and ovariectomised rats with induced hyperthyroidism; is skeletal responsiveness to thyroid hormone altered in estrogen deficiency? Tohoku J Exp Med 201:81-89
58. Ryan S, Taylor CT, McNicholas WT (2005) Selective activation of inflammatory pathways by intermittent hypoxia in obstructive sleep apnea syndrome. Circulation 112:2660-2667
59. Serebrovs'ka TV, Safronova OS, HordiÄ SK (1999) Free radical processes under different conditions of body oxygen allowance (Ukrainian, English abstract). Fiziol Zh 45:92-103
60. Yang S, Ries WL, Key LL Jr (1998) Nicotinamide adenine dinucleotide phosphate oxidase in the formation of superoxide in osteoclasts. Calcif Tissue Int 63:346-350
61. Jun JH, Lee SH, Kwak HB, Lee ZH, Seo SB, Woo KM, Ryoo HM, Kim GS, Baek JH (2008) N-Acetylcysteine stimulates osteoblastic differentiation of mouse calvarial cells. J Cell Biochem 103:1246-1255
62. Del Rio R, Muñoz C, Arias P, Court FA, Moya EA, Iturriaga R (2011) Chronic intermittent hypoxia-induced vascular enlargement and VEGF upregulation in the rat carotid body is not prevented by antioxidant treatment. Am J Physiol Lung Cell Mol Physiol 301:L702-L711
63. Maes C, Carmeliet P, Moermans K, Stockmans I, Smets N, Collen D, Bouillon R, Carmeliet G (2002) Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev 111:61-73