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Journal of Osteoporosis
Volume 2013, Article ID 571418, 8 pages
http://dx.doi.org/10.1155/2013/571418
Review Article

HIV and Bone Disease: A Perspective of the Role of microRNAs in Bone Biology upon HIV Infection

Department of Physiology, Fels Institute for Cancer Research and Molecular Biology, Temple University School of Medicine, 3307 North Broad Street, Philadelphia, PA 19140, USA

Received 21 March 2013; Revised 15 August 2013; Accepted 11 September 2013

Academic Editor: Jun Iwamoto

Copyright © 2013 Fabiola E. Del Carpio-Cano et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Division of HIV/AIDS Prevention, CDC, National Center for HIV/AIDS VH, STD and TB Prevention, HIV in the United States: At a Glance, 2012.
  2. D. G. McNeil Jr., “After marrow transplants, 2 more patients appear H.I.V.-free without drugs,” New York Times, July 2013, http://www.nytimes.com/2013/07/04/health/post-transplant-and-off-drugs-hiv-patients-are-apparently-virus-free.html?_r=1. View at Google Scholar
  3. G. Hutter, D. Nowak, M. Mossner et al., “Long-term control of HIV by CCR5 delta32/delta32 stem-cell transplantation,” The New England Journal of Medicine, vol. 360, no. 7, pp. 692–698, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Saez-Cirion, C. Bacchus, L. Hocqueloux et al., “Post-treatment HIV-1 controllers with a long-term virological remission after the interruption of early initiated antiretroviral therapy ANRS VISCONTI Study,” PLoS Pathogens, vol. 9, no. 3, Article ID e1003211, 2013. View at Google Scholar
  5. J. Sugarman, “HIV cure research: expanding the ethical considerations,” Annals of Internal Medicine, 2013. View at Publisher · View at Google Scholar
  6. B. Peters, F. Post, A. Wierzbicki et al., “Screening for chronic comorbid diseases in people with HIV: the need for a strategic approach,” HIV Medicine, vol. 14, supplement 1, pp. 1–11, 2013. View at Publisher · View at Google Scholar
  7. B. Stone, D. Dockrell, C. Bowman, and E. McCloskey, “HIV and bone disease,” Archives of Biochemistry and Biophysics, vol. 503, no. 1, pp. 66–77, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. R. Guerri-Fernandez, P. Vestergaard, C. Carbonell et al., “HIV infection is strongly associated with hip fracture risk, independently of age, gender, and comorbidities: a population-based cohort study,” Journal of Bone and Mineral Research, vol. 28, no. 6, pp. 1259–1263, 2013. View at Google Scholar
  9. A. I. Caplan, “Mesenchymal stem cells,” Journal of Orthopaedic Research, vol. 9, no. 5, pp. 641–650, 1991. View at Google Scholar · View at Scopus
  10. A. Yamaguchi, T. Komori, and T. Suda, “Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1,” Endocrine Reviews, vol. 21, no. 4, pp. 393–411, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. Y.-L. Li and Z.-S. Xiao, “Advances in Runx2 regulation and its isoforms,” Medical Hypotheses, vol. 68, no. 1, pp. 169–175, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Tou, N. Quibria, and J. M. Alexander, “Transcriptional regulation of the human Runx2/Cbfa1 gene promoter by bone morphogenetic protein-7,” Molecular and Cellular Endocrinology, vol. 205, no. 1-2, pp. 121–129, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. E.-J. Jeon, K.-Y. Lee, N.-S. Choi et al., “Bone morphogenetic protein-2 stimulates Runx2 acetylation,” Journal of Biological Chemistry, vol. 281, no. 24, pp. 16502–16511, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Mbalaviele, S. Sheikh, J. P. Stains et al., “β-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation,” Journal of Cellular Biochemistry, vol. 94, no. 2, pp. 403–418, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. K. M. Sinha and X. Zhou, “Genetic and molecular control of osterix in skeletal formation,” Journal of Cellular Biochemistry, vol. 114, no. 5, pp. 975–984, 2013. View at Publisher · View at Google Scholar
  16. B. L. M. Hogan, “Bone morphogenetic proteins: multifunctional regulators of vertebrate development,” Genes and Development, vol. 10, no. 13, pp. 1580–1594, 1996. View at Google Scholar · View at Scopus
  17. J. Massague, “How cells read TGF-beta signals,” Nature Reviews Molecular Cell Biology, vol. 1, pp. 169–178, 2000. View at Google Scholar
  18. J. Massagué and Y.-G. Chen, “Controlling TGF-β signaling,” Genes and Development, vol. 14, no. 6, pp. 627–644, 2000. View at Google Scholar · View at Scopus
  19. K. Miyazono, P. ten Dijke, and C.-H. Heldin, “TGF-β signaling by Smad proteins,” Advances in Immunology, vol. 75, pp. 115–157, 2000. View at Google Scholar · View at Scopus
  20. X. Wang, H.-Y. Kua, Y. Hu et al., “p53 functions as a negative regulator of osteoblastogenesis, osteoblast-dependent osteoclastogenesis, and bone remodeling,” Journal of Cell Biology, vol. 172, no. 1, pp. 115–125, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Nohe, E. Keating, P. Knaus, and N. O. Petersen, “Signal transduction of bone morphogenetic protein receptors,” Cellular Signalling, vol. 16, no. 3, pp. 291–299, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. C. A. Gregory, D. J. Prockop, and J. L. Spees, “Non-hematopoietic bone marrow stem cells: molecular control of expansion and differentiation,” Experimental Cell Research, vol. 306, no. 2, pp. 330–335, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. M. E. Nuttall and J. M. Gimble, “Controlling the balance between osteoblastogenesis and adipogenesis and the consequent therapeutic implications,” Current Opinion in Pharmacology, vol. 4, no. 3, pp. 290–294, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Meunier, J. Aaron, C. Edouard, and G. Vignon, “Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies,” Clinical Orthopaedics and Related Research, vol. 80, pp. 147–154, 1971. View at Google Scholar · View at Scopus
  25. C. Hartmann, “A Wnt canon orchestrating osteoblastogenesis,” Trends in Cell Biology, vol. 16, no. 3, pp. 151–158, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. T. P. Hill, D. Später, M. M. Taketo, W. Birchmeier, and C. Hartmann, “Canonical Wnt/β-catenin signaling prevents osteoblasts from differentiating into chondrocytes,” Developmental Cell, vol. 8, no. 5, pp. 727–738, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. T. F. Day, X. Guo, L. Garrett-Beal, and Y. Yang, “Wnt/β-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis,” Developmental Cell, vol. 8, no. 5, pp. 739–750, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Hu, M. J. Hilton, X. Tu, K. Yu, D. M. Ornitz, and F. Long, “Sequential roles of Hedgehog and Wnt signaling in osteoblast development,” Development, vol. 132, no. 1, pp. 49–60, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. D. A. Glass II, P. Bialek, J. D. Ahn et al., “Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation,” Developmental Cell, vol. 8, no. 5, pp. 751–764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. S. L. Holmen, C. R. Zylstra, A. Mukherjee et al., “Essential role of β-catenin in postnatal bone acquisition,” Journal of Biological Chemistry, vol. 280, no. 22, pp. 21162–21168, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Jackson, B. Vayssière, T. Garcia et al., “Gene array analysis of Wnt-regulated genes in C3H10T1/2 cells,” Bone, vol. 36, no. 4, pp. 585–598, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. G. J. Spencer, J. C. Utting, S. L. Etheridge, T. R. Arnett, and P. G. Genever, “Wnt signalling in osteoblasts regulates expression of the receptor activator of NFκB ligand and inhibits osteoclastogenesis in vitro,” Journal of Cell Science, vol. 119, no. 7, pp. 1283–1296, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. C. Y. Logan and R. Nusse, “The Wnt signaling pathway in development and disease,” Annual Review of Cell and Developmental Biology, vol. 20, pp. 781–810, 2004. View at Publisher · View at Google Scholar · View at Scopus
  34. A. J. van Wijnen, J. van de Peppel, J. P. van Leeuwen et al., “MicroRNA functions in osteogenesis and dysfunctions in osteoporosis,” Current Osteoporosis Reports, vol. 11, no. 2, pp. 72–82, 2013. View at Publisher · View at Google Scholar
  35. Y. Gong, R. B. Slee, N. Fukai et al., “LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development,” Cell, vol. 107, no. 4, pp. 513–523, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. G. Karsenty and E. F. Wagner, “Reaching a genetic and molecular understanding of skeletal development,” Developmental Cell, vol. 2, no. 4, pp. 389–406, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. W. J. Boyle, W. S. Simonet, and D. L. Lacey, “Osteoclast differentiation and activation,” Nature, vol. 423, no. 6937, pp. 337–342, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Hsu, D. L. Lacey, C. R. Dunstan et al., “Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 7, pp. 3540–3545, 1999. View at Publisher · View at Google Scholar · View at Scopus
  39. T. C. A. Phan, J. Xu, and M. H. Zheng, “Interaction between osteoblast and osteoclast: impact in bone disease,” Histology and Histopathology, vol. 19, no. 4, pp. 1325–1344, 2004. View at Google Scholar · View at Scopus
  40. K. Fuller, B. Wong, S. Fox, Y. Choi, and T. J. Chambers, “TRANCE is necessary and sufficient for osteoblast-mediated activation of bone resorption in osteoclasts,” Journal of Experimental Medicine, vol. 188, no. 5, pp. 997–1001, 1998. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Sugatani and K. A. Hruska, “Down-regulation of miR-21 biogenesis by estrogen action contributes to osteoclastic apoptosis,” Journal of Cellular Biochemistry, vol. 114, no. 6, pp. 1217–1222, 2013. View at Publisher · View at Google Scholar
  42. M. Q. Hassan, Y. Maeda, H. Taipaleenmaki et al., “miR-218 directs a Wnt signaling circuit to promote differentiation of osteoblasts and osteomimicry of metastatic cancer cells,” The Journal of Biological Chemistry, vol. 287, no. 50, pp. 42084–42092, 2012. View at Google Scholar
  43. P. Cheng, C. Chen, H. B. He et al., “miR-148a regulates osteoclastogenesis by targeting V-maf musculoaponeurotic fibrosarcoma oncogene homolog B,” Journal of Bone and Mineral Research, vol. 28, no. 5, pp. 1180–1190, 2013. View at Publisher · View at Google Scholar
  44. B. R. Troen, “Molecular mechanisms underlying osteoclast formation and activation,” Experimental Gerontology, vol. 38, no. 6, pp. 605–614, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. L. C. Hofbauer, S. Khosla, C. R. Dunstan, D. L. Lacey, T. C. Spelsberg, and B. L. Riggs, “Estrogen stimulates gene expression and protein production of osteoprotegerin in human osteoblastic cells,” Endocrinology, vol. 140, no. 9, pp. 4367–4370, 1999. View at Google Scholar · View at Scopus
  46. S. Khosla, E. J. Atkinson, C. R. Dunstan, and W. M. O'Fallon, “Effect of estrogen versus testosterone on circulating osteoprotegerin and other cytokine levels in normal elderly men,” Journal of Clinical Endocrinology and Metabolism, vol. 87, no. 4, pp. 1550–1554, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. N. K. Shevde, A. C. Bendixen, K. M. Dienger, and J. W. Pike, “Estrogens suppress RANK ligand-induced osteoclast differentiation via a stromal cell independent mechanism involving c-Jun repression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 14, pp. 7829–7834, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Srivastava, G. Toraldo, M. N. Weitzmann, S. Cenci, F. P. Ross, and R. Pacifici, “Estrogen decreases osteoclast formation by down-regulating receptor activator of NF-kappa B ligand (RANKL)-induced JNK activation,” Journal of Biological Chemistry, vol. 276, no. 12, pp. 8836–8840, 2001. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Srivastava, M. N. Weitzmann, S. Cenci, F. P. Ross, S. Adler, and R. Pacifici, “Estrogen decreases TNF gene expression by blocking JNK activity and the resulting production of c-Jun and JunD,” The Journal of Clinical Investigation, vol. 104, no. 4, pp. 503–513, 1999. View at Google Scholar · View at Scopus
  50. M. Zaidi, H. C. Blair, B. S. Moonga, E. Abe, and C. L.-H. Huang, “Osteoclastogenesis, bone resorption, and osteoclast-based therapeutics,” Journal of Bone and Mineral Research, vol. 18, no. 4, pp. 599–609, 2003. View at Google Scholar · View at Scopus
  51. V. Ambros and X. Chen, “The regulation of genes and genomes by small RNAs,” Development, vol. 134, no. 9, pp. 1635–1641, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. B. R. Cullen, “Transcription and processing of human microRNA precursors,” Molecular Cell, vol. 16, no. 6, pp. 861–865, 2004. View at Publisher · View at Google Scholar · View at Scopus
  53. I. Bentwich, A. Avniel, Y. Karov et al., “Identification of hundreds of conserved and nonconserved human microRNAs,” Nature Genetics, vol. 37, no. 7, pp. 766–770, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. Y. Lee, K. Jeon, J.-T. Lee, S. Kim, and V. N. Kim, “MicroRNA maturation: stepwise processing and subcellular localization,” The EMBO Journal, vol. 21, no. 17, pp. 4663–4670, 2002. View at Publisher · View at Google Scholar · View at Scopus
  55. M. Lagos-Quintana, R. Rauhut, W. Lendeckel, and T. Tuschl, “Identification of novel genes coding for small expressed RNAs,” Science, vol. 294, no. 5543, pp. 853–858, 2001. View at Publisher · View at Google Scholar · View at Scopus
  56. Y. Mizuno, Y. Tokuzawa, Y. Ninomiya et al., “miR-210 promotes osteoblastic differentiation through inhibition of AcvR1b,” FEBS Letters, vol. 583, no. 13, pp. 2263–2268, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Mizuno, K. Yagi, Y. Tokuzawa et al., “miR-125b inhibits osteoblastic differentiation by down-regulation of cell proliferation,” Biochemical and Biophysical Research Communications, vol. 368, no. 2, pp. 267–272, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Luzi, F. Marini, S. C. Sala, I. Tognarini, G. Galli, and M. L. Brandi, “Osteogenic differentiation of human adipose tissue-derived stem cells is modulated by the miR-26a targeting of the SMAD1 transcription factor,” Journal of Bone and Mineral Research, vol. 23, no. 2, pp. 287–295, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. Z. Li, M. Q. Hassan, S. Volinia et al., “A microRNA signature for a BMP2-induced osteoblast lineage commitment program,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 37, pp. 13906–13911, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. J. Huang, L. Zhao, L. Xing, and D. Chen, “MicroRNA-204 regulates Runx2 protein expression and mesenchymal progenitor cell differentiation,” Stem Cells, vol. 28, no. 2, pp. 357–364, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Kapinas, C. B. Kessler, and A. M. Delany, “miR-29 suppression of osteonectin in osteoblasts: regulation during differentiation and by canonical Wnt signaling,” Journal of Cellular Biochemistry, vol. 108, no. 1, pp. 216–224, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. T. Itoh, Y. Nozawa, and Y. Akao, “MicroRNA-141 and -200a are involved in bone morphogenetic protein-2-induced mouse pre-osteoblast differentiation by targeting distal-less homeobox 5,” Journal of Biological Chemistry, vol. 284, no. 29, pp. 19272–19279, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Li, H. Xie, W. Liu et al., “A novel microRNA targeting HDAC5 regulates osteoblast differentiation in mice and contributes to primary osteoporosis in humans,” The Journal of Clinical Investigation, vol. 119, no. 12, pp. 3666–3677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Hu, W. Liu, H. Li et al., “A Runx2/miR-3960/miR-2861 regulatory feedback loop during mouse osteoblast differentiation,” Journal of Biological Chemistry, vol. 286, no. 14, pp. 12328–12339, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Mori, H. Nakagami, G. Rodriguez-Araujo, K. Nimura, and Y. Kaneda, “Essential role for miR-196a in brown adipogenesis of white fat progenitor cells,” PLoS Biology, vol. 10, no. 4, Article ID e1001314, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Tomé, P. López-Romero, C. Albo et al., “miR-335 orchestrates cell proliferation, migration and differentiation in human mesenchymal stem cells,” Cell Death and Differentiation, vol. 18, no. 6, pp. 985–995, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Zhang, Q. Tu, L. F. Bonewald et al., “Effects of miR-335-5p in modulating osteogenic differentiation by specifically downregulating Wnt antagonist DKK1,” Journal of Bone and Mineral Research, vol. 26, no. 8, pp. 1953–1963, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. A. M. Schaap-Oziemlak, R. A. Raymakers, S. M. Bergevoet et al., “MicroRNA hsa-miR-135b regulates mineralization in osteogenic differentiation of human unrestricted somatic stem cells,” Stem Cells and Development, vol. 19, no. 6, pp. 877–885, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. Z. Li, M. Q. Hassan, M. Jafferji et al., “Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation,” Journal of Biological Chemistry, vol. 284, no. 23, pp. 15676–15684, 2009. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Eskildsen, H. Taipaleenmäki, J. Stenvang et al., “MicroRNA-138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 15, pp. 6139–6144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. J.-F. Zhang, W.-M. Fu, M.-L. He et al., “MiRNA-20a promotes osteogenic differentiation of human mesenchymal stem cells by co-regulating BMP signaling,” RNA Biology, vol. 8, no. 5, pp. 829–838, 2011. View at Google Scholar · View at Scopus
  72. J.-F. Zhang, W.-M. Fu, M.-L. He et al., “MiR-637 maintains the balance between adipocytes and osteoblasts by directly targeting Osterix,” Molecular Biology of the Cell, vol. 22, no. 21, pp. 3955–3961, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. S. K. Laine, J. J. Alm, S. P. Virtanen, H. T. Aro, and T. K. Laitala-Leinonen, “MicroRNAs miR-96, miR-124, and miR-199a regulate gene expression in human bone marrow-derived mesenchymal stem cells,” Journal of Cellular Biochemistry, vol. 113, no. 8, pp. 2687–2695, 2012. View at Publisher · View at Google Scholar
  74. S. Suomi, H. Taipaleenmäki, A. Seppänen et al., “MicroRNAs regulate osteogenesis and chondrogenesis of mouse bone marrow stromal cells,” Gene Regulation and Systems Biology, vol. 2, pp. 177–191, 2008. View at Google Scholar · View at Scopus
  75. T. Sugatani, J. Vacher, and K. A. Hruska, “A microRNA expression signature of osteoclastogenesis,” Blood, vol. 117, no. 13, pp. 3648–3657, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. L. Y. Zhu, C. Qiu, J. X. Lv, and J. Q. Xu, “HIV-1 infection changes miRNA expression profile in the whole blood,” Bing Du Xue Bao, vol. 29, no. 3, pp. 323–329, 2013. View at Google Scholar
  77. M. H. G. P. Raaijmakers, S. Mukherjee, S. Guo et al., “Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia,” Nature, vol. 464, no. 7290, pp. 852–857, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. T. Sugatani and K. A. Hruska, “Impaired micro-RNA pathways diminish osteoclast differentiation and function,” Journal of Biological Chemistry, vol. 284, no. 7, pp. 4667–4678, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Sugatani and K. A. Hruska, “MicroRNA-223 is a key factor in osteoclast differentiation,” Journal of Cellular Biochemistry, vol. 101, no. 4, pp. 996–999, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. Y. Wang, L. Li, B. T. Moore et al., “Mir-133a in human circulating monocytes: a potential biomarker associated with postmenopausal osteoporosis,” PLoS ONE, vol. 7, no. 4, Article ID e34641, 2012. View at Publisher · View at Google Scholar · View at Scopus
  81. M. T. Yin, C. A. Zhang, D. J. McMahon et al., “Higher rates of bone loss in postmenopausal HIV-infected women: a longitudinal study,” Journal of Clinical Endocrinology and Metabolism, vol. 97, no. 2, pp. 554–562, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. C. Cazanave, M. Dupon, V. Lavignolle-Aurillac et al., “Reduced bone mineral density in HIV-infected patients: prevalence and associated factors,” AIDS, vol. 22, no. 3, pp. 395–402, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Yin, J. Dobkin, K. Brudney et al., “Bone mass and mineral metabolism in HIV+ postmenopausal women,” Osteoporosis International, vol. 16, no. 11, pp. 1345–1352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Jones, D. Restrepo, A. Kasowitz et al., “Risk factors for decreased bone density and effects of HIV on bone in the elderly,” Osteoporosis International, vol. 19, no. 7, pp. 913–918, 2008. View at Publisher · View at Google Scholar · View at Scopus
  85. A. Carr, J. Miller, J. A. Eisman, and D. A. Cooper, “Osteopenia in HIV-infected men: association with asymptomatic lactic acidemia and lower weight pre-antiretroviral therapy,” AIDS, vol. 15, no. 6, pp. 703–709, 2001. View at Publisher · View at Google Scholar · View at Scopus
  86. C. Amiel, A. Ostertag, L. Slama et al., “BMD is reduced in HIV-infected men irrespective of treatment,” Journal of Bone and Mineral Research, vol. 19, no. 3, pp. 402–409, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. K. Mondy, K. Yarasheski, W. G. Powderly et al., “Longitudinal evolution of bone mineral density and bone markers in human immunodeficiency virus-infected individuals,” Clinical Infectious Diseases, vol. 36, no. 4, pp. 482–490, 2003. View at Publisher · View at Google Scholar · View at Scopus
  88. D. Gibellini, E. de Crignis, C. Ponti et al., “HIV-1 triggers apoptosis in primary osteoblasts and HOBIT cells through TNFα activation,” Journal of Medical Virology, vol. 80, no. 9, pp. 1507–1514, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. V. Amorosa and P. Tebas, “Bone disease and HIV infection,” Clinical Infectious Diseases, vol. 42, no. 1, pp. 108–114, 2006. View at Publisher · View at Google Scholar · View at Scopus
  90. G. Pan, M. Kilby, and J. M. McDonald, “Modulation of osteoclastogenesis induced by nucleoside reverse transcriptase inhibitors,” AIDS Research and Human Retroviruses, vol. 22, no. 11, pp. 1131–1141, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. D. Gibellini, M. Borderi, E. de Crignis et al., “RANKL/OPG/TRAIL plasma levels and bone mass loss evaluation in antiretroviral naive HIV-1-positive men,” Journal of Medical Virology, vol. 79, no. 10, pp. 1446–1454, 2007. View at Publisher · View at Google Scholar · View at Scopus
  92. S. Wei, H. Kitaura, P. Zhou, F. Patrick Ross, and S. L. Teitelbaum, “IL-1 mediates TNF-induced osteoclastogenesis,” The Journal of Clinical Investigation, vol. 115, no. 2, pp. 282–290, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. J. M. Fakruddin and J. Laurence, “HIV envelope gp120-mediated regulation of osteoclastogenesis via receptor activator of nuclear factor kappa B ligand (RANKL) secretion and its modulation by certain HIV protease inhibitors through interferon-gamma/RANKL cross-talk,” Journal of Biological Chemistry, vol. 278, no. 48, pp. 48251–48258, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. J. M. Fakruddin and J. Laurence, “HIV-1 Vpr enhances production of receptor of activated NF-κB ligand (RANKL) via potentiation of glucocorticoid receptor activity,” Archives of Virology, vol. 150, no. 1, pp. 67–78, 2005. View at Publisher · View at Google Scholar · View at Scopus
  95. J.-P. Herbeuval, A. Boasso, J.-C. Grivel et al., “TNF-related apoptosis-inducing ligand (TRAIL) in HIV-1-infected patients and its in vitro production by antigen-presenting cells,” Blood, vol. 105, no. 6, pp. 2458–2464, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. Y. Yang, I. Tikhonov, T. J. Ruckwardt et al., “Monocytes treated with human immunodeficiency virus Tat kill uninfected CD4+ cells by a tumor necrosis factor-related apoptosis-induced ligand-mediated mechanism,” Journal of Virology, vol. 77, no. 12, pp. 6700–6708, 2003. View at Publisher · View at Google Scholar · View at Scopus
  97. B. R. Wong, D. Besser, N. Kim et al., “TRANCE, a TNF family member, activates Akt/PKB through a signaling complex involving TRAF6 and c-Src,” Molecular Cell, vol. 4, no. 6, pp. 1041–1049, 1999. View at Google Scholar · View at Scopus
  98. G. Pan, Z. Yang, S. W. Ballinger, and J. M. McDonald, “Pathogenesis of osteopenia/osteoporosis induced by highly active anti-retroviral therapy for AIDS,” Annals of the New York Academy of Sciences, vol. 1068, no. 1, pp. 297–308, 2006. View at Publisher · View at Google Scholar · View at Scopus
  99. L. Salmena, L. Poliseno, Y. Tay, L. Kats, and P. P. Pandolfi, “A ceRNA hypothesis: the rosetta stone of a hidden RNA language?” Cell, vol. 146, no. 3, pp. 353–358, 2011. View at Publisher · View at Google Scholar · View at Scopus
  100. S. T. Chang, P. Sova, X. Peng et al., “Next-generation sequencing reveals HIV-1-mediated suppression of T cell activation and RNA processing and regulation of noncoding RNA expression in a CD4+ T cell line,” mBio, vol. 2, no. 5, 2011. View at Publisher · View at Google Scholar · View at Scopus
  101. A. T. Navare, P. Sova, D. E. Purdy et al., “Quantitative proteomic analysis of HIV-1 infected CD4+ T cells reveals an early host response in important biological pathways: protein synthesis, cell proliferation, and T-cell activation,” Virology, vol. 429, no. 1, pp. 37–46, 2012. View at Publisher · View at Google Scholar · View at Scopus
  102. M. L. Yeung, Y. Bennasser, T. G. Myers, G. Jiang, M. Benkirane, and K.-T. Jeang, “Changes in microRNA expression profiles in HIV-1-transfected human cells,” Retrovirology, vol. 2, article 81, 2005. View at Publisher · View at Google Scholar · View at Scopus
  103. L. Houzet, M. L. Yeung, V. de Lame, D. Desai, S. M. Smith, and K.-T. Jeang, “MicroRNA profile changes in human immunodeficiency virus type 1 (HIV-1) seropositive individuals,” Retrovirology, vol. 5, article 118, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. S. T. Chang, M. J. Thomas, P. Sova, R. R. Green, R. E. Palermo, and M. G. Katze, “Next-generation sequencing of small RNAs from HIV-infected cells identifies phased microrna expression patterns and candidate novel microRNAs differentially expressed upon infection,” mBio, vol. 4, no. 1, 2013. View at Publisher · View at Google Scholar