Acute hypoxia and osteoclast activity: A balance between enhanced resorption and increased apoptosis

Journal of Pathology

Volumn 218, Issue 2, 2009, Pages 256-264

  Knowles, Helen J ^a   Athanasou, Nicholas A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Apoptosis; Bone resorption; Hypoxia; Hypoxia inducible factor (HIF); Osteoclast; Reoxygenation

Indexed keywords

CATHEPSIN K; HYPOXIA INDUCIBLE FACTOR 1ALPHA; OXYGEN; SMALL INTERFERING RNA; THROMBIN RECEPTOR ACTIVATING PEPTIDE;

APOPTOSIS; ARTICLE; BONE ATROPHY; CELL ACTIVITY; CELL DIFFERENTIATION; CELL HYPOXIA; CELL MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MEMBRANE STRUCTURE; OSTEOCLAST; OSTEOCLASTOMA; PRIORITY JOURNAL; REOXYGENATION; RNA INTERFERENCE;

APOPTOSIS; BIOLOGICAL MARKERS; BONE RESORPTION; CATHEPSINS; CELL DIFFERENTIATION; CELL HYPOXIA; CELL MEMBRANE; COLORING AGENTS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IN SITU NICK-END LABELING; OSTEOCLASTS; OXYGEN; RECEPTORS, THROMBIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; TRYPAN BLUE;

EID: 66849097919     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.2534     Document Type: Article

References (59)

1. 2! See what HIF can do! Ann Rheum Dis 2005;64:971-980.
2. Watanabe Y, Terashima Y, Takenaka N, Kobayashi M, Matsushita T. Prediction of avascular necrosis of the femoral head by measuring intramedullary oxygen tension after femoral neck fracture. J Orthop Trauma 2007;21:456-461. (Pubitemid 47356971)
3. Dunst J, Ahrens S, Paulussen M, Burdach S, Jurgens H. Prognostic impact of tumor perfusion in MR-imaging studies in Ewing tumors. Strahlenther Onkol 2001;177:153-159. (Pubitemid 32220425)
4. Hiraga T, Kizaka-Kondoh S, Hirota K, Hiraoka M, Yoneda T. Hypoxia and hypoxia-inducible factor-1 expression enhance osteolytic bone metastases of breast cancer. Cancer Res 2007;67:4157-4163. (Pubitemid 46815061)
5. Maurer P, Meyer L, Eckert AW, Berginski M, Schubert J. Measurement of oxygen partial pressure in the mandibular bone using a polarographic fine needle probe. Int J Oral Maxillofac Surg 2006;35:231-236. (Pubitemid 43154390)
6. Ishikawa Y, Ito T. Kinetics of hemopoietic stem cells in a hypoxic culture. Eur J Haematol 1988;40:126-129. (Pubitemid 18098107)
7. Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood 2002;99:394. (Pubitemid 34533016)
8. Brighton CT, Krebs AG. Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg 1972;54:323-332.
9. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 1989;49:6449-6465. (Pubitemid 20008770)
10. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nature Rev Cancer 2002;2:38-47. (Pubitemid 37328806)
11. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001;107:43-54. (Pubitemid 32972036)
12. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294:1337-1340. (Pubitemid 33063099)
13. Utting JC, Robins SP, Brandao-Burch A, Orriss IR, Behar J, Arnett TR. Hypoxia inhibits the growth, differentiation and bone-forming capacity of rat osteoblasts. Exp Cell Res 2006;312:1693-1702. (Pubitemid 43776006)
14. Steinbrech DS, Mehrara BJ, Saadeh PB, Chin G, Dudziak ME, Gerrets RP, et al. Hypoxia regulates VEGF expression and cellular proliferation by osteoblasts in vitro. Plastic Reconstructive Surg 1999;104:738-747. (Pubitemid 29383700)
15. Lennon DP, Edmison JM, Caplan AI. Cultivation of rat marrow-derived mesenchymal stem cells in reduced oxygen tension: effects on in vitro and in vivo osteochondrogenesis. J Cell Physiol 2001;187:345-355. (Pubitemid 32378359)
16. Akeno N, Czyzyk-Krzeska MF, Gross TS, Clemens TL. Hypoxia induces vascular endothelial growth factor gene transcription in human osteoblast-like cells through the hypoxia-inducible factor-2alpha. Endocrinol 2001;142:959-962. (Pubitemid 32222447)
17. Kim HH, Lee SE, Chung WJ, Choi Y, Kwack K, Kim SW, et al. Stabilization of hypoxia-inducible factor-1alpha is involved in the hypoxic stimuli-induced expression of vascular endothelial growth factor in osteoblastic cells. Cytokine 2002;17:14-27. (Pubitemid 34925852)
18. Knowles HJ, Athanasou NA. Hypoxia-inducible factor is expressed in giant cell tumour of bone and mediates paracrine effects of hypoxia on monocyte-osteoclast differentiation via induction of VEGF. J Pathol 2008;215:56-66.
19. Tamiya H, Ikeda T, Jeong JH, Saito T, Yano F, Jung YK, et al. Analysis of the Runx2 promoter in osseous and non-osseous cells and identification of HIF2A as a potent transcription activator. Gene 2008;416:53-60.
20. Wang Y, Wan C, Deng L, Liu X, Cao X, Gilbert SR, et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 2007;117:1616-1626. (Pubitemid 46871346)
21. Wan C, Gilbert SR, Wang Y, Cao X, Shen X, Ramaswamy G, et al. Activation of the hypoxia-inducible factor-1alpha pathway accelerates bone regeneration. Proc Natl Acad Sci U S A 2008;105:686-691.
22. Wang Y, Wan C, Gilbert SR, Clemens TL. Oxygen sensing and osteogenesis. Ann N Y Acad Sci 2007;1117:1-11. (Pubitemid 350191282)
23. Dodd JS, Raleigh JA, Gross TS. Osteocyte hypoxia: a novel mechanotransduction pathway. Am J Physiol 1999;277:C598-C602. (Pubitemid 29458195)
24. Gross TS, Akeno N, Clemens TL, Komarova S, Srinivasan S, Weimer DA, et al. Selected contribution: osteocytes upregulate HIF-1alpha in response to acute disuse and oxygen deprivation. J Appl Physiol 2001;90:2514-2519.
25. Gross TS, King KA, Rabaia NA, Pathare P, Srinivasan S. Upregulation of osteopontin by osteocytes deprived of mechanical loading or oxygen. J Bone Miner Res 2005;20:250-256.
26. Muzylak M, Price JS, Horton MA. Hypoxia induces giant osteoclast formation and extensive bone resorption in the cat. Calcif Tissue Int 2006;79:301-309. (Pubitemid 44900153)
27. Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, et al. Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol 2003;196:2-8. (Pubitemid 36676438)
28. Srinivasan S, Avadhani NG. Hypoxia-mediated mitochondrial stress in RAW264.7 cells induces osteoclast-like TRAP-positive cells. Ann N Y Acad Sci 2007;1117:51-61. (Pubitemid 350191286)
29. Fukuoka H, Aoyama M, Miyazawa K, Asai K, Goto S. Hypoxic stress enhances osteoclast differentiation via increasing IGF2 production by non-osteoclastic cells. Biochem Biophys Res Commun 2005;328:885-894. (Pubitemid 40238720)
30. Arnett TR, Massey H, Utting JC, Orriss IR, Flanagan AM. Hypoxia is a major stimulator of osteoclast formation from human peripheral blood. Calcif Tissue Int 2003;72:345-346.
31. Utting JC, Brandao-Baruch A, Arnett TR. Effects of hypoxia and acidosis on the formation and activation of human osteoclasts: evidence for a key role of the vasculature in one remodelling. Bone 2004;34:S28.
32. Bozec A, Bakiri L, Hoebertz A, Eferl R, Schilling AF, Komnenovic V, et al. Osteoclast size is controlled by Fra-2 through LIF/LIF-receptor signalling and hypoxia. Nature 2008;454:221-225.
33. Joyner CJ, Quinn JM, Triffitt JT, Owen ME, Athanasou NA. Phenotypic characterisation of mononuclear and multinucleated cells of giant cell tumour of bone. Bone Miner 1992;16:37-48.
34. Perez-Amodio S, Jansen DC, Schoenmaker T, Vogels IM, Reinheckel T, Hayman AR, et al. Calvarial osteoclasts express a higher level of tartrate-resistant acid phosphatase than long bone osteoclasts and activation does not depend on cathepsin K or L activity. Calcif Tissue Int 2006;79:245-254. (Pubitemid 44673718)
35. Xia L, Kilb J, Wex H, Li Z, Lipyansky A, Breuil V, et al. Localization of rat cathepsin K in osteoclasts and resorption pits: inhibition of bone resorption and cathepsin K-activity by peptidyl vinyl sulfones. Biol Chem 1999;380:679-687. (Pubitemid 29322358)
36. Aibe K, Yazawa H, Abe K, Teramura K, Kumegawa M, Kawashima H, et al. Substrate specificity of recombinant osteoclast-specific cathepsin K from rabbits. Biol Pharm Bull 1996;19:1026-1031. (Pubitemid 26303361)
37. Akiyama T, Miyazaki T, Bouillet P, Nakamura K, Strasser A, Tanaka S. In vitro and in vivo assays for osteoclast apoptosis. Biol Proced Online 2005;7:48-59. (Pubitemid 41358165)
38. Adlard BP, De Souza SW. The effect of anoxia on cerebral acid hydrolases in the five-day-old rat. Biochem J 1972;129:1079-1084.
39. Butur G, Nicolau N, Laky D. Histochemical and ultrastructural alterations of lysosomes and acid phosphatase reaction in human chronic hypoxic myocardium. Rom J Morphol Embryol 1992;38:123-127.
40. Stepan JJ, Pospichal J, Schreiber V, Kanka J, Mensik J, Presl J, et al. The application of plasma tartrate-resistant acid phosphatase to assess changes in bone resorption in response to artificial menopause and its treatment with estrogen or norethisterone. Calcif Tissue Int 1989;45:273-280. (Pubitemid 19271418)
41. Hayman AR, Jones SJ, Boyde A, Foster D, Colledge WH, Carlton MB, et al. Mice lacking tartrate-resistant acid phosphatase (Acp 5) have disrupted endochondral ossification and mild osteopetrosis. Development. 1996;122:3151-3162. (Pubitemid 26371980)
42. Hollberg K, Hultenby K, Hayman A, Cox T, Andersson G. Osteoclasts from mice deficient in tartrate-resistant acid phosphatase have altered ruffled borders and disturbed intracellular vesicular transport. Exp Cell Res 2002;279:227-238. (Pubitemid 35217551)
43. Bull H, Murray PG, Thomas D, Fraser AM, Nelson PN. Acid phosphatases. Mol Pathol 2002;55:65-72. (Pubitemid 34293405)
44. Daumer KM, Taparowsky EJ, Hall DJ, Steinbeck MJ. Transcription from the tartrate-resistant acid phosphatase promoter is negatively regulated by the Myc oncoprotein. J Bone Miner Res 2002;17:1701-1709. (Pubitemid 34940686)
45. Gordan JD, Bertout JA, Hu CJ, Diehl JA, Simon MC. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007;11:335-347. (Pubitemid 46518312)
46. Yang Q, McHugh KP, Patntirapong S, Gu X, Wunderlich L, Hauschka PV. VEGF enhancement of osteoclast survival and bone resorption involves VEGF receptor-2 signaling and beta(3)-integrin. Matrix Biol 2008;27:589-599.
47. Nakagawa M, Kaneda T, Arakawa T, Morita S, Sato T, Yomada T, et al. Vascular endothelial growth factor (VEGF) directly enhances osteoclastic bone resorption and survival of mature osteoclasts. FEBS Lett 2000;473:161-164. (Pubitemid 30254282)
48. Fuller K, Kirstein B, Chambers TJ. Regulation and enzymatic basis of bone resorption by human osteoclasts. Clin Sci (London) 2007;112:567-575. (Pubitemid 46849547)
49. Thelestam M, Mollby R. Survival of cultured cells after functional and structural disorganization of plasma membrane by bacterial haemolysins and phospholipases. Toxicon 1983;21:805-815. (Pubitemid 14206678)
50. Pena C, Zhou Y, Lust D, Pilar G. Restoration of mitochondrial function reverses developmental neuronal death in vitro. J Comp Neurol 2001;440:156-176. (Pubitemid 33032443)
51. Hammill AK, Uhr JW, Scheuermann RH. Annexin V staining due to loss of membrane asymmetry can be reversible and precede commitment to apoptotic death. Exp Cell Res 1999;251:16-21. (Pubitemid 29406515)
52. Yang MY, Chuang H, Chen RF, Yang KD. Reversible phosphatidylserine expression on blood granulocytes related to membrane perturbation but not DNA strand breaks. J Leukocyte Biol 2002;71:231-237.
53. Martin S, Pombo I, Poncet P, David B, Arock M, Blank U. Immunologic stimulation of mast cells leads to the reversible exposure of phosphatidylserine in the absence of apoptosis. Int Arch Allergy Immunol 2000;123:249-258.
54. Minamikawa T, Williams DA, Bowser DN, Nagley P. Mitochondrial permeability transition and swelling can occur reversibly without inducing cell death in intact human cells. Exp Cell Res 1999;246:26-37. (Pubitemid 29393743)
55. Postovit LM, Abbott DE, Payne SL, Wheaton WW, Margaryan NV, Sullivan R, et al. Hypoxia/reoxygenation: a dynamic regulator of lysyl oxidase-facilitated breast cancer migration. J Cell Biochem 2008;103:1369-1378.
56. Cairns RA, Kalliomaki T, Hill RP. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 2001;61:8903-8908. (Pubitemid 34013907)
57. Rupec RA, Baeuerle PA. The genomic response of tumor cells to hypoxia and reoxygenation. Differential activation of transcription factors AP-1 and NF-kappa B. Euro J Biochem/FEBS 1995;234:632-640.
58. Moeller BJ, Cao Y, Li CY, Dewhirst MW. Radiation activates HIF-1 to regulate vascular radiosensitivity in tumors: role of reoxygenation, free radicals, and stress granules. Cancer Cell 2004;5:429-441. (Pubitemid 38610245)
59. Iotsova V, Caamano J, Loy J, Yang Y, Lewin A, Bravo R. Osteopetrosis in mice lacking NF-kappaB1 and NF-kappaB2. Nature Med 1997;3:1285-1289. (Pubitemid 27508833)