WNT/β-catenin signaling is involved in regulation of osteoclast differentiation by human immunodeficiency virus protease inhibitor ritonavir: Relationship to human immunodeficiency virus-linked bone mineral loss

American Journal of Pathology

Volumn 174, Issue 1, 2009, Pages 123-135

  Modarresi, Rozbeh ^a   Xiang, Zhaoying ^a   Yin, Michael ^b   Laurence, Jeffrey ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3BETA; GLYCOPROTEIN GP 120; GROWTH FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDINAVIR; NELFINAVIR; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEINASE INHIBITOR; RITONAVIR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; VIRUS GLYCOPROTEIN; WNT PROTEIN;

ADENOVIRUS; ARTICLE; BONE DENSITY; BONE MINERAL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; OSTEOCLAST; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL; UBIQUITINATION; UPREGULATION;

EID: 58249094863     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2009.080484     Document Type: Article

References (60)

1. Knobel H, Guelar A, Vallecillo G, Nogues X, Diez A: Osteopenia in HIV-infected patients: is it the disease or is it the treatment? AIDS 2001, 15:807-808
2. Brown TT, Qaqish RB: Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS 2006, 20:2165-2174
3. Serrano S, Marinoso ML, Soriano JC: Bone remodelling in human immunodeficiency virus-1-infected patients. A histomorphometric study. Bone 1995, 16:185-191
4. Aukrust P, Haug CJ, Ueland T, Lien E, Muller F, Espevik T, Bollerslev J, Froland SS: Decreased bone formative and enhanced resorptive markers in human immunodeficiency virus infection: indication of normalization of the bone-remodeling process during highly active antiretroviral therapy. J Clin Endocrinol Metab 1999, 84:145-150
5. Nolan D, Upton R, McKinnon E: Stable or increasing bone mineral density in HIV-infected patients treated with nelfinavir or indinavir. AIDS 2001, 15:1275-1280
6. Laurence J, Modarresi R: Modeling metabolic effects of the HIV protease inhibitor ritonavir in vitro. Am J Pathol 2007, 171:1724-1725
7. Jain RG, Lenhard JM: Select HIV protease inhibitors alter bone and fat metabolism ex vivo. J Biol Chem 2002, 277:19247-19250
8. Wang MW-H, Wei S, Faccio R, Takeshita S, Tebas P, Powderly WG, Teitelbaum SL, Ross FP: The HIV protease inhibitor ritonavir blocks osteoclastogenesis and function by impairing RANKL induced signaling. J Clin Invest 2004, 114:206-213
9. Fakruddin JM, Laurence J: HIV envelope gp120-mediated regulation of osteoclastogenesis via receptor of nuclear factor κB ligand (RANKL) secretion and its modulation by certain HIV protease inhibitors through interferon-γ/RANKL cross-talk. J Biol Chem 2003, 278:48251-48258
10. Konishi M, Takahashi K, Yoshimoto E, Uno K, Kashara K, Mikasa K: Association between osteopenia/osteoporosis and the serum RANKL in HIV-infected patients. AIDS 2005, 19:1240-1241
11. Spencer GJ, Utting JC, Etheridge SL, Arnett TR, Genever PG: Wnt signalling in osteoblasts regulates expression of the receptor activator of NFκB ligand and inhibits osteoclastogenesis in vitro. J Cell Sci 2006, 119:1283-1296
12. Glass II DA, Bialek P, Ahn JD, Starbuck M, Patei MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, Karsenty G: Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 2005, 8:751-764
13. Park BK, Zhang H, Zeng Q, Dai J, Keller ET, Giordano T, Gu K, Shah V, Zarbo RJ, McCauley L, Shi S, Chen S, Wang C-Y: NF-κB in breast cancer cells promotes osteolytic bone metastasis by inducing osteoclastogenesis via GM-CSF. Nat Med 2007, 13:62-69
14. Yamada N, Niwa S, Tsujimura T, Iwasaki T, Sugihara A, Futani J, Hayashi S, Okamura H, Akedo H, Terada N: Interleukin-18 and interleukin-12 synergistically inhibit osteoclastic bone-resorbing activity. Bone 2002, 30:901-908
15. Gorny G, Shaw A, Oursler MJ: IL-6, LIF, and TNF-α regulation of GM-CSF inhibition of osteoclastogenesis in vitro. Exp Cell Res 2004, 294:149-158
16. Day CJ, Kim MS, Stephens SRJ, Simcock WE, Aitken CJ, Nicholson GC, Morrison NA: Gene array identification of osteoclast genes: differential inhibition of osteoclastogenesis by cyclosporin A and granulocyte macrophage colony stimulating factor. J Cell Biochem 2004, 91:303-315
17. Esser R, Glienke W, Andressen R, Unger RE, Kreutz M, Rubsamen-Waigmann H, von Briesen H: Individual cell analysis of the cytokine repertoire in human immunodeficiency virus-1-infected monocytes/macrophages by a combination of immunocytochemistry and in situ hybridization. Blood 1998, 91:4752-4760
18. Susa M, Luong-Nguyen NH, Cappellen D, Zamurovic N, Gamse R: Human primary osteoclasts: in vitro generation and applications as pharmacological and clinical assay. J Transl Med 2004, 2:6
19. Fuchs D, Hausen A, Reibnegger G, Werner ER, Werner-Felmayer G, Dierich MP, Wachter H: Interferon-γ concentrations are increased in sera from individuals infected with human immunodeficiency virus type 1. J Acquir Immune Defic Syndr 1989, 2:158-162
20. Fakruddin JM, Yin M, Laurence J: Pathophysiologic correlates of RANKL deregulation in HIV infection and its therapy. Program and Abstracts 12th Conference on Retroviruses and Opportunistic Infections, Feb 22-25, 2005, Boston, MA, Abst. 822
21. Hanriot D, Bello G, Ropars A, Seguin-Devaux C, Poitevin G, Grosjean S, Latger-Cannard V, Devaux Y, Zannad F, Regnault V, Lacolley P, Mertes P-M, Hess K, Longrois D: C-reactive protein induces pro- and anti-inflammatory effects, including activation of the liver X receptor α, on human monocytes. Thromb Haemost 2008, 99:558-569
22. Dantuma NP, Lindsten K, Glas R, Jeline M, Masucci MG: Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat Biotechnol 2000, 18:538-543
23. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, Takaoba A, Taniguchi T: T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ. Nature 2000, 408:600-605
24. Cappellen D, Luong-Nguyen N-H, Bongiovanni S, Grenet O, Wanke C, Susa M: Transcriptional program of mouse osteoclast differentiation governed by the macrophage colony-stimulating factor and the ligand for the receptor of NFγB. J Biol Chem 2002, 277:21971-21982
25. Ishida N, Hayashi K, Hoshijima M, Ogawa T, Koga S, Miyatake Y, Kumegawa M, Kimura T, Takeya T: Large scale gene expression analysis of osteoclastogenesis in vitro and elucidation of NFAT2 as a key regulator. J Biol Chem 2002, 277:41147-41156
26. Zheng H, Yu X, Collin-Osdoby P, Osdoby P: RANKL stimulates inducible nitric-oxide synthetase expression and nitric oxide production in developing osteoclasts. An autocrine negative feedback mechanism triggered by RANKL-induced interferon-β via NF-κB that restrains osteoclastogenesis and bone resorption. J Biol Chem 2006, 281:15809-15820
27. Lagumdzija A, Pernow Y, Bucht E, Gonon A, Petersson M: The effects of arg-vasopression on osteoblast-like cells in endothelial nitric oxide synthetase-knockout mice and their wild-type counterparts. Peptides 2005, 26:1661-1666
28. 3 co-transporter NBCn1. Endocrinology 2007, 148:831-840
29. Lacey DL, Tan HL, Lu J, Kaufman S, Van G, Qiu W, Rattan A, Scully S, Fletcher F, Juan T, Kelley M, Burgess TL, Boyle WJ, Polverino AJ: Osteoprotegerin ligand modulates murine osteoclast survival in vitro and in vivo. Am J Pathol 2000, 157:435-448
30. Adamopoulos IE, Xia Z, Lau YS, Athanasou NA: Hepatocyte growth factor can substitute for M-CSF to support osteoclastogenesis. BBRC 2006, 350:478-483
31. Mbalaviele G, Nishimura R, Myoi A, Niewolna M, Reddy SV, Chen D, Feng J, Roodman D, Mundy GR, Yoneda T: Cadherin-6 mediates the heterotypic interactions between the hemopoietic osteoclast cell lineage and stromal cells in a murine model of osteoclast differentiation. J Cell Biol 1998, 141:1467-1476
32. Mao D, Epple H, Uthgenannt B, Novack DV, Faccio R: PLCγ2 regulates osteoclastogenesis via its interaction with ITAM proteins and GAB2. J Clin Invest 2006, 116:2869-2879
33. Ruocco MG, Maeda S, Park JM, Lawrence T, Hsu L-C, Cao Y, Schett G, Wagner EF, Karin M: IκB kinase (IKK)β, but not IKKα, is a critical mediator of osteoclast survival and is required for inflammation-induced bone loss. J Exp Med 2005, 201:1677-1687
34. Yamamoto A, Miyazaki T, Kadono Y, Takayanagi H, Miura T, Nishina H, Katada T, Wakabayashi K, Oda H, Nakamura K, Tanaka S: Possible involvement of IκB kinase 2 and MKK7 in osteoclastogenesis induced by receptor activator of nuclear factor κB ligand. J Bone Miner Res 2002, 17:612-621
35. Bai S, Kitaura H, Zhao H, Chen J, Muller JM, Schuk R, Darnay B, Novack DV, Ross FP, Teitelbaum SL: FHL2 inhibits the activated osteoclast in a TRAF6-dependent manner. J Clin Invest 2005, 115:2742-2751
36. Glass II DA, Karsenty G: Minireview: in vivo analysis of Wnt signaling in bone. Endocrinology 2007, 148:2630-2634
37. Krishnan V, Bryant HU, MacDougal OA: Regulation of bone mass by Wnt signaling. J Clin Invest 2006, 116:1202-1209
38. Nakamura Y, Nawata M, Wakitani S: Expression profiles and functional analysis of Wnt-related genes in human joint disorders. Am J Pathol 2005, 167:97-105
39. Clément-Lacroix P, Ai M, Morvan F, Roman-Roman S, Vayssiere B, Belleville C, Estrera K, Warman ML, Baron R, Rawadi G: Lrp5-independent activation of Wnt signaling by lithium chloride increases bone formation and bone mass in mice. Proc Natl Acad Sci USA 2005, 102:17406-17411
40. Schmidtke G, Holzhutter H-G, Bogyo M, Kairies N, Groll M, de Giuli R, Emch S, Groettrup M: How an inhibitor of the HIV-1 protease modulates proteasome activity. J Biol Chem 1999, 274:35734-35740
41. André P, Groettrup M, Klenerman P, de Giuli R, Booth Jr BL, Cerundolo V, Zinkernagel RM, Lotteau V: An inhibitor of HIV-1 protease modulates proteasome activity, antigen presentation, and T cell responses. Proc Natl Acad Sci USA 1998, 95:13120-13124
42. Heink S, Ludwig D, Kloetzel P-M, Kruger E: IFN-γ-induced immune adaptation of the proteasome system is an accelerated and transient response. Proc Natl Acad Sci USA 2005, 102:9241-9246
43. Arnsten JH, Freeman R, Howard AA, Floris-Moore M, Lo Y, Klein RS: Decreased bone mineral density and increased fracture risk in aging men with or at risk for HIV infection. AIDS 2007, 21:617-623
44. Triant VA, Brown TT, Lee H, Grinspoon SK: Fracture prevalence among human immunodeficiency virus (HIV)-infected versus non-HIV-infected patients in a large U.S. healthcare system. J Clin Endocrinol Metab 2008, 93:3499-3504
45. Piliero PJ, Gianoukakis AG: Ritonavir-associated hyperparathyroidism, osteopenia and bone pain. AIDS 2002, 16:1565-1566
46. Rivas P, Gorgolas M, Garcia-Delgado R, Diaz-Curiel M, Goyenechea A, Fernandez-Guerrero ML: Evolution of bone mineral density in AIDS patients on treatment with zidovudine/lamivudine plus abacavir or lopinavir/ritonavir. HIV Med 2008, 9:89-95
47. Zhou H, Pandak Jr WM, Lydall V, Natarajan R, Hylemon PB: HIV protease inhibitors activate the unfolded protein response in macrophages: implication for atherosclerosis and cardiovascular disease. Mol Pharmacol 2005, 68:690-700
48. Goldring SR, Goldring MB: Eating bone or adding to it: the Wnt pathway decides. Nat Med 2007, 13:133-134
49. Jimi E, Aoki K, Saito H, D'Acquisto F, May MJ, Nakamura I, Sudo T, Kojima T, Okamoto F, Fukushima H, Okabe K, Ohya K, Ghosh S: Selective inhibition of NF-κB blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 2004, 10:617-624
50. Häusler KD, Horwood NJ, Yoshiro C, Fisher JL, Ellis J, Martin TJ, Rubin JS, Gillespie MT: Secreted frizzled-related protein-1 inhibits RANKL-dependent osteoclast formation. J Bone Miner Res 2004, 19:1873-1881
51. Glass II DA, Karsenty G: Canonical Wnt signaling in osteoblasts is required for osteoclast differentiation. Ann NY Acad Sci 2006, 1068:117-130
52. Diarra D, Stolina M, Polzer K, Zwerina J, Ominsky MS, Dwyer D, Korb A, Smolen J, Hoffman M, Scheinecker C, van der Heide D, Landewe R, Lacey D, Richards WG, Schett G: Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007, 13:156-163
53. Monaghan H, Bubb VJ, Sirimujalin R, Millward-Sadler SJ, Salter DM: Adenomatous polyposis coli (APC), β-catenin, and cadherin are expressed in human bone and cartilage. Histopathology 2001, 39:611-619
54. Malizia AP, Cotter E, Crew N, Powderly WG, Doran PP: HIV protease inhibitors selectively induce gene expression alterations associated with reduced calcium deposition in primary human osteoblasts. AIDS Res Hum Retroviruses 2007, 23:243-250
55. Qiang Y-W, Shaughnessy Jr JD, Yaccoby S: Wnt3a signaling within bone inhibits multiple myeloma bone disease and tumor growth. Blood 2008, 112:374-382
56. Cheng S-L, Shao J-S, Cai J, Sierra OL, Towler DA: Msx2 exerts bone anabolism via canonical Wnt signaling. J Biol Chem 2008, 283:20505-20522
57. Garrett IR, Chen D, Gutierrez G, Zhao M, Escobedo A, Rossini G, Harris SE, Gallwitz W, Kim KB, Hu S, Crews CM, Mundy GR: Selective inhibitors of the osteoblast proteasome stimulate bone formation in vivo and in vitro. J Clin Invest 2003, 111:1771-1782
58. Bose S, Stratford FLL, Broadfoot KI, Mason GGF, Rivett AJ: Phosphorylation of 20S proteasome alpha subunit C8 (α7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by γ-interferon. Biochem J 2004, 378:177-184
59. Xiao J-H, Ghosn C, Hinchman C, Forbes C, Wang J, Snider N, Cordrey A, Zhao Y, Chandraratna RAS: Adenomatous polyposis coli (APC)-independent regulation of β-catenin degradation via a retinoid X receptor-mediated pathway. J Biol Chem 2003, 278:29954-29962
60. Ulloa L, Doody J, Massague J: Inhibition of transforming growth factor-β/SMAD signalling by the interferon-γ/STAT pathway. Nature 1999, 397:710-713