Altered pre-lamin A processing is a common mechanism leading to lipodystrophy

Human Molecular Genetics

Volumn 14, Issue 11, 2005, Pages 1489-1502

  Capanni, Cristina ^a   Mattioli, Elisabetta ^b   Columbaro, Marta ^b   Lucarelli, Enrico ^c   Parnaik, Veena K ^d   Novelli, Giuseppe ^e   Wehnert, Manfred ^f   Cenni, Vittoria ^b   Maraldi, Nadir M ^a,b   Squarzoni, Stefano ^a   Lattanzi, Giovanna ^a  

^a CNR   (Italy)

^b Laboratory of Cell Biology   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

^f UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN A; LAMIN C; MEVINOLIN; N [[5 [(2 AMINO 3 MERCAPTOPROPYL)AMINO][1,1' BIPHENYL] 2 YL]CARBONYL]METHIONINE METHYL ESTER; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PRELAMIN A; PROTEIN INHIBITOR; PROTEIN PRECURSOR; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TROGLITAZONE; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; BONE DYSPLASIA; CELL DIFFERENTIATION; CONTROLLED STUDY; FAMILIAL DISEASE; FIBROBLAST; HUMAN; HUMAN CELL; INSULIN RESISTANCE; LIPID METABOLISM; LIPODYSTROPHY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; WERNER SYNDROME;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL NUCLEUS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOPRECIPITATION; LIPODYSTROPHY; MICE; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 20444449733     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddi158     Document Type: Article

References (59)

1. Hegele, R.A. (2003) Monogenic forms of insulin resistance: apertures that expose the common metabolic syndrome. Trends Endocrinol. Metab., 14, 371-377.
2. Shacketon, S., Lloyd, D.J., Jackson, SN., Evans, R., Niermeijer, M.F., Singh, B.M., Schmidt, H., Brabant, G., Kumar, S. et al. (2000) LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat. Genet., 24, 153-156.
3. 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.
4. Bhayana, S., Siu, V.M., Joubert, G.I., Clarson, C.L., Cao, H. and Hegele, R.A. (2002) Cardiomyopathy in congenital complete lipodystrophy. Clin. Genet., 61, 283-287.
5. Magre, J.J., Delepine, M., Khallouf, E., Gedde-Dahl, T., Jr, van Maldergem, L., Sobel, E., Papp, J., Meier, M., Megarbane, A., Bachy, A. et al. (2001) Identification of the gene altered in Berardinelli-Seip congenital lipodystrophy on chromosome 11q13. Nat. Genet., 28, 365-370.
6. Hegele, R.A., Cao, H., Frankowski, C., Mathews, S.T. and Leff, T. (2002) PPARG F388L, a transactivation-deficient mutant, in familial partial lipodystrophy. Diabetes, 51, 3586-3590.
7. Caron, M., Auclair, M., Sterlingot, H., Kornprobst, M. and Capeau, J. (2003) Some HIV protease inhibitors alter lamin A/C maturation and stability, SREBP-1 nuclear localization and adipocyte differentiation. AIDS, 17, 2437-2444.
8. de Sandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C.L., Munnich, A., Le Merrer, M. et al (2003) Lamin a truncation in Hutchinson-Gilford progeria. Science, 300, 2055.
9. 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.
10. Cao, H. and Hegele, R.A. (2003) LMNA is mutated in Hutchinson-Gilford progeria (MIM 176670) but not in Wiedemann-Rautenstrauch progeroid syndrome (MIM 264090). J. Hum. Genet., 48, 271-274.
11. Chen, L., Lee, L., Kudlow, B.A., Dos Santos, H.G., Sletvold, O., Shafeghati, Y., Botha, E.G., Garg, A., Hanson, N.B., Martin, G.M. et al. (2003) LMNA mutations in atypical Werner's syndrome. Lancet, 362, 440-445.
12. Corrigan, D.P., Kuszczak, D., Rusinol, A.E., Thewke, D.P., Hrycyna, C.A., Michaelis, S., Sinensky, M.S. (2005) Prelamin A endoproteolytic processing in vitro by recombinant Zmpste24. Biochem. J., 387, 129-138.
13. 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.
14. 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. USA, 99, 13049-13054.
15. Pendas, A.M., Zhou, Z., Cadinanos, J., Freije, J.M., Wang, J., Hultenby, K., Astudillo, A., Wernerson, A., Rodriguez, F., Tryggvason, K. et al (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat. Genet., 31, 94-99.
16. Caron, M., Auclair, M., Vigouroux, C., Glorian, M., Forest, C. and Capeau, J. (2001) The HIV protease inhibitor indinavir impairs sterol regulatory element-binding protein-1 intranuclear localization, inhibits preadipocyte differentiation, and induces insulin resistance. Diabetes, 50, 1378-1388.
17. Spiegelman, B.M. (1998) PPAR-gamma: adipogenic regulator and thiazolidinedione receptor. Diabetes, 47, 507-514.
18. Agarwal, A.K. and Garg, A. (2002) A novel heterozygous mutation in peroxisome proliferator-activated receptor-gamma gene in a patient with familial partial lipodystrophy. J. Clin. Endocrinol. Metab., 87, 408 -411.
19. Al-Shali, K., Cao, H., Knoers, N., Hermus, A.R., Tack, C.J., Hegele, R.A. (2004) A single-base mutation in the peroxisome proliferator-activated receptor {gamma} promoter associated with altered in vitro expression and partial lipodystrophy. J. Clin. Endocrinol. Metab., 89, 5655-5660.
20. Zastrow, M.S., Vlcek, S. and Wilson, K.L. (2004) Proteins that bind A-type lamins: integrating isolated clues. J. Cell. Sci., 117, 979-987.
21. Sasseville, A.M. and Raymond, Y. (1995) Lamin A precursor is localized to intranuclear foci. J. Cell. Sci., 108, 273-285.
22. Stuurman, N., Heins, S. and Aebi, U. (1998) Nuclear lamins: their structure, assembly, and interactions. J. Struct. Biol., 122, 42-66.
23. Sakaki, M., Koike, H., Takahashi, N., Sasagawa, N., Tomioka, S., Arahata, K. and Ishiura, S. (2001) Interaction between emerin and nuclear lamins. J. Biochem., 129, 321-327.
24. Markiewicz, E., Dechat, T., Foisner, R., Quinlan, R.A. and Hutchison, C.J. (2002) Lamin A/C binding protein LAP2alpha is required for nuclear anchorage of retinoblastoma protein. Mol. Biol. Cell, 13, 4401-4413.
25. Sasseville, A.M. and Langelier, Y. (1998) In vitro interaction of the carboxy-terminal domain of lamin A with actin. FEBS Lett., 425, 485-489.
26. Lattanzi, G., Cenni, V., Marmiroli, S., Capanni, C., Mattioli, E., Merlini, L., Squarzoni, S. and Maraldi, N.M. (2003) Association of emerin with nuclear and cytoplasmic actin is regulated in differentiating myoblasts. Biochem. Biophys. Res. Commun., 303, 764-770.
27. Mancini, M.A., Shan, B., Nickerson, J.A., Penman, S. and Lee, W.H. (1994) The retinoblastoma gene product is a cell cycle-dependent, nuclear matrix-associated protein. Proc. Natl Acad. Sci. USA, 91, 418-422.
28. Novelli, G. and D'Apice, M.R. (2003) The strange case of the 'lumper' lamin A/C gene and human premature ageing. Trends Mol. Med., 9, 370-375.
29. Bonne, G., Raffaele-Di Barletta, M., 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.
30. 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.
31. Fatkin, D., MacRae, C., Sasaki, T., Wolff, M.R., Porcu, M., Frenneaux, M., Atherton, J., Vidaillet, H.J., Jr, Spudich, S., de Girolami, U. et al. (1999) Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N. Engl. J. Med., 341, 1715-1724.
32. 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.
33. Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C.L. and Burke, B. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell. Biol., 147, 913-920.
34. Lloyd, D.J., Trembath, R.C. and Shackleton S. (2002) A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum. Mol. Genet., 11, 769-777.
35. Krimm, I., Ostlund, C., Gilquin, B., Couprie, J., Hossenlopp, P., Mornon, J.P., Bonne, G., Courvalin, J.C., Worman, H.J. and Zinn-Justin, S. (2002) The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure, 10, 811-823.
36. Nikolova, V., Leimena, C., McMahon, A.C., Tan, J.C., Chandar, S., Jogia, D., Kesteven, S.H., Michalicek, J., Otway, R., Verheyen, F. et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J. Clin. Invest., 113, 357-369.
37. Lammerding, J., Schulze, P.C., Takahashi, T., Kozlov, S., Sullivan, T., Kamm, R.D., Stewart, C.L. and Lee, R.T. (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest., 113, 370-378.
38. Sabatelli, P., Lattanzi, G., Ognibene, A., Columbaro, M., Capanni, C., Merlini, L. Maraldi, N.M. and Squarzoni, S. (2001) Nuclear alterations in autosomal-dominant Emery-Dreifuss muscular dystrophy. Muscle Nerve, 24, 826-829.
39. Maraldi, N.M., Lattanzi, G., Marmiroli, S., Squarzoni, S. and Manzoli, F.A. (2004) New roles for lamins, nuclear envelope proteins and actin in the nucleus. Adv. Enzyme Regul., 44, 155-172.
40. Stierle, V., Couprie, J., Ostlund, C., Krimm, I., Zinn-Justin, S., Hossenlopp, P., Worman, H.J., Courvalin, J.C. and Duband-Goulet, I. (2003) The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochemistry, 42, 4819-4828.
41. Muchir, A., van Engelen, B.G., Lammens, M., Mislow, J.M., McNally, E., Schwartz, K. and Bonne, G. (2003) Nuclear envelope alterations in fibroblasts from LGMD1B patients carrying nonsense Y259X heterozygous or homozygous mutation in lamin A/C gene. Exp. Cell Res., 291, 352-362.
42. Capanni, C., Cenni, V., Mattioli, E., Sabatelli, P., Ognibene, A., Columbaro, M., Parnaik, V.K., Wehnert, M., Maraldi, N.M., Squarzoni, S. et al. (2003) Failure of lamin A/C to functionally assemble in R482L mutated familial partial lipodystrophy fibroblasts: altered intermolecular interaction with emerin and implications for gene transcription. Exp. Cell Res., 291, 122-134.
43. 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.
44. Kim, J.B. and Spiegelman, B.M. (1996) ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev., 10, 1096-1107.
45. Ericsson, J., Jackson, S.M., Kim, J.B., Spiegelman, B.M. and Edwards, P.A. (1997) Identification of glycerol-3-phosphate acyltransferase as an adipocyte determination and differentiation factor 1-and sterol regulatory element-binding protein-responsive gene. J. Biol. Chem., 272, 7298-7305.
46. Kim, J.B., Wright, H.M., Wright, M. and Spiegelman, B.M. (1998) ADD1/SREBP1 activates PPARgamma through the production of endogenous ligand. Proc. Natl Acad. Sci. USA, 95, 4333-4337.
47. 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, 53-62.
48. Hegele, R.A. (2001) Molecular basis of partial lipodystrophy and prospects for therapy. Trends Mol. Med., 7, 121-126.
49. 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., Faivre, L. et al. (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet., 13, 2493-2503.
50. Maraldi, N.M., Squarzoni, S., Sabatelli, P., Capanni, C., Mattioli, E., Ognibene, A. and Lattanzi, G. (2005) Laminopathies: involvement of structural nuclear proteins in the pathogenesis of an increasing number of human diseases. J. Cell Physiol., 203, 319-327.
51. Nishio, E., Tomiyama, K., Nakata, H. and Watanabe, Y. (1996) 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitor impairs cell differentiation in cultured adipogenic cells (3T3-L1). Eur. J. Pharmacol., 301, 203-206.
52. Solomon, C.S., Leitner, J.W. and Goalstone, M.L. (2003) Dominant negative alpha-subunit of farnesyl- and geranylgeranyl-transferase I inhibits insulin-induced differentiation of 3T3-L1 pre-adipocytes. Int. J. Obes. Relat. Metab. Disord., 27, 40-47.
53. Hennekes, H. and Nigg, E.A. (1994) The role of isoprenylation in membrane attachment of nuclear lamins. A single point mutation prevents proteolytic cleavage of the lamin A precursor and confers membrane binding properties. J. Cell Sci., 107, 1019-1029.
54. Adjei, A.A., Davis, J.N., Erlichman, C., Svingen, P.A. and Kaufmann, S.H. (2000) Comparison of potential markers of farnesyltransferase inhibition. Clin. Cancer Res., 6, 2318-2325.
55. Sewter, C.P., Blows, F., Vidal-Puig, A. and O'Rahilly, S. (2002) Regional differences in the response of human pre-adipocytes to PPARgamma and RXRalpha agonists. Diabetes, 51, 718-723.
56. Owen, K.R., Donohoe, M., Ellard, S. and Hattersley, A.T. (2003) Response to treatment with rosiglitazone in familial partial lipodystrophy due to a mutation in the LMNA gene. Diabet. Med., 20, 823-827.
57. Parpal, S., Karlsson, M., Thorn, H. and Stralfors, P. (2001) Cholesterol depletion disrupts caveolae and insulin receptor signaling for metabolic control via insulin receptor substrate-1, but not for mitogen-activated protein kinase control. J. Biol. Chem., 276, 9670-9678.
58. Kumaran, R.I., Muralikrishna, B. and Parnaik, V.K. (2002) Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA-polymerase II transcription. J. Cell Biol., 159, 783-793.
59. Sinensky, M., Beck, L.A., Leonard, S. and Evans, R. (1990) Differential inhibitory effects of lovastatin on protein isoprenylation and sterol synthesis. J. Biol. Chem., 265, 19937-19941.