HIV protease inhibitors inhibit FACE1/ZMPSTE24: A mechanism for acquired lipodystrophy in patients on highly active antiretroviral therapy?

Biochemical Society Transactions

Volumn 38, Issue 1, 2010, Pages 292-296

  Goulbourne, Chris N ^a   Vaux, David J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Acquired lipodystrophy; Highly active antiretroviral therapy (HAART); HIV protease inhibitor; Nuclear envelope; Prelamin A; ZMPSTE24

Indexed keywords

DARUNAVIR; LAMIN A; METALLOPROTEINASE; PROTEIN FACE1; PROTEINASE INHIBITOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; FATTY ACID METABOLISM; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; LIPODYSTROPHY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; STEROL SYNTHESIS;

ANIMALS; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; HIV INFECTIONS; HIV PROTEASE INHIBITORS; HUMANS; LAMIN TYPE A; LIPODYSTROPHY; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; MICE; NUCLEAR ENVELOPE; PROTEIN PRECURSORS; STEROL REGULATORY ELEMENT BINDING PROTEINS;

EID: 76449116735     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0380292     Document Type: Article

References (48)

1. Chen, L., Lee, L., Kudlow, B.A., Dos Santos, H.G., Sletvold, O., Shafeghati, Y., Botha, E.G., Garg, E., Hanson, N.B., Martin, G.M. et al. (2003) LMNA mutations in atypical Werner's syndrome. Lancet 362, 440-445
2. Hegele, R.A., Cao, H., Liu, D.M., Costain, G.A., Charlton-Menys, V., Rodger, N.W. and Durrington, P.N. (2006) Sequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am. J. Hum. Genet. 79, 383-389
3. Hellemans, J., Preobrazhenska, O., Willaert, A., Debeer, P., Verdonk, P.C.M., Costa, T., Janssens, K., Menten, B., Van Roy, N., Vermeulen, S.J.T. et al. (2004) Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis. Nat. Genet. 36, 1213-1218
4. Charniot, J.C., Pascal, C., Bouchier, C., Sebillon, P., Salama, J., Duboscq-Bidot, L., Peuchmaurd, M., Desnos, M., Artigou, J.Y. and Komajda, M. (2003) Functional consequences of an LMNA mutation associated with a new cardiac and non-cardiac phenotype. Hum. Mutat. 21, 473-481
5. De Sandre-Giovannoli, A., Chaouch, M., Kozlov, S., Vallat, J.M., Tazir, M., Kassouri, N., Szepetowski, P., Hammadouche, T., Vandenberghe, A., Stewart, C.L. et al. (2002) Homozygous defects in LMNA, encoding lamin A/ C nuclear-envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am. J. Hum. Genet. 70, 726-736
6. Manilal, S., Nguyen, T.M., Sewry, C.A. and Morris, G.E. (1996) The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum. Mol. Genet. 5, 801-808
7. Bonne, G., Di Barletta, M.R., Varnous, S., Becane, H.M., Hammouda, E.H., Merlini, L., Muntoni, F., Greenberg, C.R., Gary, F., Urtizberea, J.A. et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21, 285-288
8. Raffaele di Barletta, M., Ricci, E., Galluzzi, G., Tonali, P., Mora, M., Morandi, L., Romorini, A., Voit, T., Orstavik, K.H., Merlini, L. et al. (2000) Different mutations in the LMNA gene cause autosomal dominant and autosomal recessive Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 66, 1407-1412
9. Cao, H. and Hegele, R.A. (2002) Nuclear lamin A/C R482Q mutation in Canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum. Mol. Genet. 9, 109-112
10. 14-reductase deficiency due to mutations in the lamin B receptor gene. Am. J. Hum. Genet. 72, 1013-1017
11. Muchir, A., Bonne, G., van der Kooi, A.J., van Meegen, M., Baas, F., Bolhuis, P.A., de Visser, M. and Schwartz, K. (2000) Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum. Mol. Genet. 9, 1453-1459
12. Caux, F., Dubosclard, E., Lascols, O., Buendia, B., Chazouilleres, O., Cohen, A., Courvalin, J.C., Laroche, L., Capeau, J., Vigouroux, C. and Christin-Maitre, S. (2003) A new clinical condition linked to a novel mutation in lamins A and C with generalized lipoatrophy, insulin-resistant diabetes, disseminated leukomelanodermic papules, liver steatosis, and cardiomyopathy. J. Clin. Endocr. Metab. 88, 1006-1013
13. Novelli, G., Muchir, A., Sangiuolo, F., Helbling-Leclerc, A., D'Apice, M.R., Massart, C., Capon, F., Sbraccia, P., Federici, M., Lauro, R. et al. (2002) Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. Am. J. Hum. Genet. 71, 426-431
14. Eriksson, M., Brown, W.T., Gordon, L.B., Glynn, M.W., Singer, J., Scott, L., Erdos, M.R., Robbins, C.M., Moses, T.Y., Berglund, P. et al. (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298
15. Agarwal, A.K., Fryns, J.P., Auchus, R.J. and Garg, A. (2003) Zinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Hum. Mol. Genet. 12, 1995-2001
16. Hoffmann, K., Dreger, C.K., Olins, A.L., Olins, D.E., Shultz, L.D., Lucke, B., Karl, H., Kaps, R., Muller, D., Vaya, A. et al. (2002) Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nat. Genet. 31, 410-414
17. Padiath, Q.S., Saigoh, K., Schiffmann, R., Asahara, H., Yamada, T., Koeppen, A., Hogan, K., Ptacek, L.J. and Fu, Y.H. (2006) Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat. Genet. 38, 1114-1123
18. Navarro, C.L., De Sandre-Giovannoli, A., Bernard, R., Boccaccio, I., Boyer, A., Genevieve, D., Hadj-Rabia, S., Gaudy-Marqueste, C., Smitt, H.S., Vabres, P. et al. (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identity restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 13, 2493-2503
19. Machiels, B.M., Zorenc, A.H., Endert, J.M., Kuijpers, H.J., van Eys, G.J., Ramaekers, F.C. and Broers, J.L. (1996) An alternative splicing product of the lamin A/C gene lacks exon 10. J. Biol. Chem. 271, 9249-9253
20. Beck, L.A., Hosick, T.J. and Sinensky, M. (1990) Isoprenylation is required for the processing of the lamin A precursor. J. Cell Biol. 110, 1489-1499
21. Corrigan, D.P., Kuszczak, D., Rusinol, A.E., Thewke, D.P., Hrycyna, C.A., Michaelis, S. and Sinensky, M.S. (2005) Prelamin A endoproteolytic processing in vitro by recombinant Zmpste24. Biochem. J. 387, 129-138
22. Weber, K., Plessmann, U. and Traub, P. (1989) Maturation of nuclear lamin A involves a specific carboxy-terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina. FEBS Lett. 257, 411-414
23. Mounkes, L.C., Kozlov, S., Hernandez, L., Sullivan, T. and Stewart, C.L. (2003) A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423, 298-301
24. Freije, J.M., Blay, P., Pendás, A.M., Cadiñanos, J., Crespo, P. and López-Otín, C. (1999) Identification and chromosomal location of two human genes encoding enzymes potentially involved in proteolytic maturation of farnesylated proteins. Genomics 58, 270-280
25. Gruber, J., Lampe, T., Osborn, M. and Weber, K. (2005) RNAi of FACE1 protease results in growth inhibition of human cells expressing lamin A: implications for Hutchinson-Gilford progeria syndrome. J. Cell Sci. 118, 689-696
26. Bergo, M.O., Gavino, B., Ross, J., Schmidt, W.K., Hong, C., Kendall, L.V., Mohr, A., Meta, M., Genant, H., Jiang, Y. et al. (2002) Zmpste24 deficiency in mice causes spontaneous bone fractures, muscle weakness, and a prelamin A processing defect. Proc. Natl. Acad. Sci. U.S.A. 99, 13049-13054
27. Fong, L.G., Ng, J.K., Meta, M., Cote, N., Yang, S.H., Stewart, C.L., Sullivan, T., Burghardt, A., Majumdar, S., Reue, K. et al. (2004) Heterozygosity for LMNA deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 101, 18111-18116
28. Varela, I., Cadiñanos, J., Pendás, A.M., Gutiérrez-Fernández, A., Folgueras, A.R., Sánchez, L.M., Zhou, Z., Rodríguez, F.J., Stewart, C.L., Vega, J.A. et al. (2005) Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature 437, 564-568
29. Mariño, G., Ugalde, A.P., Salvador-Montoliu, N., Varela, I., Quirós, P.M., Cadiñanos, J., van der Pluijm, I., Freije, J.M. and López-Otín, C. (2008) Premature aging in mice activates a systemic metabolic response involving autophagy induction. Hum. Mol. Genet. 17, 2196-2211
30. Caron, M., Auclair, M., Donadille, B., Béréziat, V., Guerci, B., Laville, M., Narbonne, H., Bodemer, C., Lascols, O., Capeau, J. and Vigouroux, C. (2007) Human lipodystrophies linked to mutations in A-type lamins and to HIV protease inhibitor therapy are both associated with prelamin A accumulation, oxidative stress and premature cellular senescence. Cell Death Differ. 14, 1759-1767
31. Coffinier, C., Hudon, S.E., Farber, E.A., Chang, S.Y., Hrycyna, C.A., Young, S.G. and Fong, L.G. (2007) HIV protease inhibitors block the zinc metalloproteinase ZMPSTE24 and lead to an accumulation of prelamin A in cells. Proc. Natl. Acad. Sci. U.S.A. 104, 13432-13437
32. Clarke, S.G. (2007) HIV protease inhibitors and nuclear lamin processing: getting the right bells and whistles. Proc. Natl. Acad. Sci. U.S.A. 104, 13857-13858
33. Coffinier, C., Hudon, S.E., Lee, R., Farber, E.A., Nobumori, C., Miner, J.H., Andres, D.A., Spielmann, H.P., Hrycyna, C.A., Fong, L.G. and Young, S.G. (2008) A potent HIV protease inhibitor, darunavir, does not inhibit ZMPSTE24 or lead to an accumulation of farnesyl-prelamin A in cells. J. Biol. Chem. 283, 9797-9804
34. Hudon, S.E., Coffinier, C., Michaelis, S., Fong, L.G., Young, S.G. and Hrycyna, C.A. (2008) HIV-protease inhibitors block the enzymatic activity of purified Ste24p. Biochem. Biophys. Res. Commun. 374, 365-368
35. Saillan-Barreau, C., Tabbakh, O., Chavoin, J.P., Casteilla, L. and Pénicaud, L. (2008) Drug-specific effect of nelfinavir and stavudine on primary culture of human preadipocytes. J. Acquired Immune Defic. Syndr. 48, 20-25
36. Carr, A. (2000) HIV protease inhibitor-related lipodystrophy syndrome. Clin. Infect. Dis. 30, (Suppl. 2), S135-S142
37. Vigouroux, C., Maachi, M., Nguyên, T.H., Coussieu, C., Gharakhanian, S., Funahashi, T., Matsuzawa, Y., Shimomura, I., Rozenbaum, W., Capeau, J. and Bastard, J.P. (2003) Serum adipocytokines are related to lipodystrophy and metabolic disorders in HIV-infected men under antiretroviral therapy. AIDS 17, 1503-1511
38. Sharma, D. and Bitterly, T.J. (2008) Buffalo hump in HIV patients: surgical management with liposuction. J. Plast. Reconstr. Aesthet. Surg. 62, 946-949
39. Rajagopalan, R., Laitinen, D. and Dietz, B. (2008) Impact of lipoatrophy on quality of life in HIV patients receiving anti-retroviral therapy. AIDS Care 20, 1197-1201
40. Paton, N.I., Earnest, A., Ng, Y.M., Karim, F. and Aboulhab, J. (2002) Lipodystrophy in a cohort of human immunodeficiency virus infected Asian patient: prevalence, associated factors, and psychological impact. Clin. Infect. Dis. 35, 1244-1249
41. Collins, E., Wagner, C. and Walmsley, S. (2000) Psychosocial impact of the lipodystrophy syndrome in HIV infection. AIDS Read. 10, 546-550
42. Power, R., Tate, H.L., McGill, S.M. and Taylor, C. (2003) A qualitative study of the psychosocial implications of lipodystrophy syndrome on HIV positive individuals. Sex. Transm. Infect. 79, 137-141
43. Tate, H. and George, R. (2001) The effect of weight loss on body image in HIV positive gay men. AIDS Care 13, 163-169
44. Wang, X., Sato, R., Brown, M.S., Hua, X. and Goldstein, J.L. (1994) SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis. Cell 77, 17-19
45. Tontonoz, P., Kim, J.B., Graves, R.A. and Spiegelman, B.M. (1993) ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol. Cell. Biol. 13, 4753-4759
46. Capanni, C., Mattioli, E., Columbaro, M., Lucarelli, E., Parnaik, V.K., Novelli, G., Wehnert, M., Cenni, V., Maraldi, N.M., Squarzoni, S. and Lattanzi, G. (2005) Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum. Mol. Genet. 14, 1489-1502
47. Falutz, J., Allas, S., Mamputu, J.C., Potvin, D., Kotler, D., Somero, M., Berger, D., Brown, S., Richmond, G., Fessel, J. et al. (2008) Long-term safety and effects of tesamorelin, a growth hormone-releasing factor analogue, in HIV patients with abdominal fat accumulation. AIDS 22, 1719-1728
48. Pan, Y., Garg, A. and Agarwal, A.K. (2007) Mislocalization of prelamin A Tyr646Phe mutant to the nuclear pore complex in human embryonic kidney 293 cells. Biochem. Biophys. Res. Commun. 355, 78-84