The R439C mutation in LMNA causes lamin oligomerization and susceptibility to oxidative stress

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 5, 2009, Pages 959-971

  Verstraeten, Valerie L R M ^a,b,m,n   Caputo, Sandrine ^c,d,e   Van Steensel, Maurice A M ^a,b   Duband Goulet, Isabelle ^f   Zinn Justin, Sophie ^c   Kamps, Miriam ^a,b   Kuijpers, Helma J H ^b   Östlund, Cecilia ^g   Worman, Howard J ^g   Briedé, Jacob J ^b   Le Dour, Caroline ^h,i   Marcelis, Carlo L M ^j   Van Geel, Michel ^a,b   Steijlen, Peter M ^a,b   Van Den Wijngaard, Arthur ^a   Ramaekers, Frans C S ^b,k   Broers, Jos L V ^b,l  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^d CNRS   (France)

^e ECOLE POLYTECHNIQUE   (France)

^f INSTITUT JACQUES MONOD   (France)

^g Columbia University ^*  (United States)

^h INSERM   (France)

ⁱ SORBONNE UNIVERSITÉ   (France)

^j RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^k MAASTRICHT UNIVERSITY   (Netherlands)

^l EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^m BRIGHAM AND WOMEN S HOSPITAL   (United States)

ⁿ Partners Research Facility   (United States)

more..

Author keywords

Cysteine; Disulphide bond; DNA; FPLD; Laminopathy; Lipodystrophy; Oligomerization; Oxidative stress; ROS

Indexed keywords

EID: 67249111692     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00690.x     Document Type: Article

References (40)

1. Broers JLV, Ramaekers FCS, Bonne G, Yaou RB, Hutchison CJ. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev. 2006 86 : 967 1008. (Pubitemid 44042881)
2. Verstraeten VL, Broers JL, Ramaekers FC, van Steensel MA. The nuclear envelope, a key structure in cellular integrity and gene expression. Curr Med Chem. 2007 14 : 1231 48.
3. Broers JLV, Machiels BM, van Eys GJ, Kuijpers HJ, Manders EM, van Driel R, Ramaekers FCS. Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J Cell Sci. 1999 112 : 3463 75.
4. Moir RD, Yoon M, Khuon S, Goldman RD. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol. 2000 151 : 1155 68.
5. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP. Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 2002 16 : 533 47.
6. Hutchison CJ. Lamins: building blocks or regulators of gene expression? Nat Rev Mol Cell Biol. 2002 3 : 848 58.
7. Shelton KR, Guthrie VH, Cochran DL. Oligomeric structure of the major nuclear envelope protein lamin B. J Biol Chem. 1982 257 : 4328 32.
8. Dessev GN, Iovcheva-Dessev C, Goldman RD. Lamin dimers. Presence in the nuclear lamina of surf clam oocytes and release during nuclear envelope breakdown. J Biol Chem. 1990 265 : 12636 41.
9. Garg A, Vinaitheerthan M, Weatherall PT, Bowcock AM. Phenotypic heterogeneity in patients with familial partial lipodystrophy (Dunnigan variety) related to the site of missense mutations in lamin a-c gene. J Clin Endocrinol Metab. 2001 86 : 59 65. (Pubitemid 32109776)
10. Haque WA, Oral EA, Dietz K, Bowcock AM, Agarwal AK, Garg A. Risk factors for diabetes in familial partial lipodystrophy, Dunnigan variety. Diabetes Care. 2003 26 : 1350 5.
11. Hegele RA, Anderson CM, Wang J, Jones DC, Cao H. Association between nuclear lamin A-C R482Q mutation and partial lipodystrophy with hyperinsulinemia, dyslipidemia, hypertension, and diabetes. Genome Res. 2000 10 : 652 8.
12. Krimm I, Ostlund C, Gilquin B, Couprie J, Hossenlopp P, Mornon J P, Bonne G, Courvalin JC, Worman HJ, Zinn-Justin S. The Ig-like structure of the C-terminal domain of lamin A-C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy. Structure. 2002 10 : 811 23.
13. Caron M, Auclair M, Donadille B, Bereziat V, Guerci B, Laville M, Narbonne H, Bodemer C, Lascols O, Capeau J, Vigouroux C. Human lipodys-trophies 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. 2007 14 : 1759 67.
14. Charniot JC, Bonnefont-Rousselot D, Marchand C, Zerhouni K, Vignat N, Peynet J, Plotkine M, Legrand A, Artigou JY. Oxidative stress implication in a new phenotype of amyotrophic quadricipital syndrome with cardiac involvement due to lamin A-C mutation. Free Radic Res. 2007 41 : 424 31.
15. Leichert LI, Jakob U. Global methods to monitor the thiol-disulfide state of proteins in vivo. Antioxid Redox Signal. 2006 8 : 763 72.
16. Decaudain A, Vantyghem MC, Guerci B, Hecart AC, Auclair M, Reznik Y, Narbonne H, Ducluzeau PH, Donadille B, Lebbe C, Bereziat V, Capeau J, Lascols O, Vigouroux C. New metabolic phenotypes in laminopathies: LMNA mutations in patients with severe metabolic syndrome. J Clin Endocrinol Metab. 2007 92 : 4835 44.
17. Vigouroux C, Magre J, Vantyghem MC, Bourut C, Lascols O, Shackleton S, Lloyd DJ, Guerci B, Padova G, Valensi P, Grimaldi A, Piquemal R, Touraine P, Trembath RC, Capeau J. Lamin A-C gene: sex-determined expression of mutations in Dunnigan-type familial partial lipodystrophy and absence of coding mutations in congenital and acquired generalized lipoatrophy. Diabetes. 2000 49 : 1958 62.
18. Verstraeten VL, Broers JL, van Steensel MA, Zinn-Justin S, Ramaekers FC, Steijlen PM, Kamps M, Kuijpers HJ, Merckx D, Smeets HJ, Hennekam RC, Marcelis CL, van den Wijngaard A. Compound heterozygosity for mutations in LMNA causes a progeria syndrome without prelamin A accumulation. Hum Mol Genet. 2006 15 : 2509 22.
19. Dyer JA, Kill IR, Pugh G, Quinlan RA, Lane EB, Hutchison CJ. Cell cycle changes in A-type lamin associations detected in human dermal fibroblasts using monoclonal antibodies. Chromosome Res. 1997 5 : 383 94.
20. Hozak P, Sasseville AM, Raymond Y, Cook PR. Lamin proteins form an internal nucleoskeleton as well as a peripheral lamina in human cells. J Cell Sci. 1995 108 : 635 44.
21. Venables RS, McLean S, Luny D, Moteleb E, Morley S, Quinlan RA, Lane EB, Hutchison CJ. Expression of individual lamins in basal cell carcinomas of the skin. Br J Cancer. 2001 84 : 512 9.
22. Broers JLV, Bronnenberg NM, Kuijpers HJ, Schutte B, Hutchison CJ, Ramaekers FCS. Partial cleavage of A-type lamins concurs with their total disintegration from the nuclear lamina during apoptosis. Eur J Cell Biol. 2002 81 : 677 91.
23. Machiels BM, Broers JLV, Raymond Y, de Ley L, Kuijpers HJ, Caberg NE, Ramaekers FCS. Abnormal A-type lamin organization in a human lung carcinoma cell line. Eur J Cell Biol. 1995 67 : 328 35.
24. Chaudhary N, Courvalin JC. Stepwise reassembly of the nuclear envelope at the end of mitosis. J Cell Biol. 1993 122 : 295 306.
25. Bridger JM, Kill IR, O'Farrell M, Hutchison CJ. Internal lamin structures within G1 nuclei of human dermal fibroblasts. J Cell Sci. 1993 104 : 297 306.
26. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet. 1994 8 : 323 7.
27. Nigro V, Bruni P, Ciccodicola A, Politano L, Nigro G, Piluso G, Cappa V, Covone AE, Romeo G, D'Urso M. SSCP detection of novel mutations in patients with Emery-Dreifuss muscular dystrophy: definition of a small C-terminal region required for emerin function. Hum Mol Genet. 1995 4 : 2003 4.
28. Sinensky M, Fantle K, Dalton M. An antibody which specifically recognizes prelamin A but not mature lamin A: application to detection of blocks in farnesylation-dependent protein processing. Cancer Res. 1994 54 : 3229 32.
29. Capanni C, Mattioli E, Columbaro M, Lucarelli E, Parnaik VK, Novelli G, Wehnert M, Cenni V, Maraldi NM, Squarzoni S, Lattanzi G. Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum Mol Genet. 2005 14 : 1489 502.
30. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 227 : 680 5.
31. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 1979 76 : 4350 4.
32. Stierle V, Couprie J, Ostlund C, Krimm I, Zinn-Justin S, Hossenlopp P, Worman HJ, Courvalin JC, Duband-Goulet I. The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochemistry. 2003 42 : 4819 28.
33. Duband-Goulet I, Courvalin JC. Inner nuclear membrane protein LBR preferentially interacts with DNA secondary structures and nucleosomal linker. Biochemistry. 2000 39 : 6483 8.
34. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 2nd ed. Plainview, NY : Cold Spring Harbor Laboratory Press 1989.
35. Briede JJ, Pot RG, Kuipers EJ, van Vliet AH, Kleinjans JC, Kusters JG. The presence of the cag pathogenicity island is associated with increased superoxide anion radical scavenging activity by Helicobacter pylori. FEMS Immunol Med Microbiol. 2005 44 : 227 32.
36. Burke B, Tooze J, Warren G. A monoclonal antibody which recognises each of the nuclear lamin polypeptides in mammalian cells. EMBO J. 1983 2 : 361 7.
37. Dhe-Paganon S, Werner ED, Chi YI, Shoelson SE. Structure of the globular tail of nuclear lamin. J Biol Chem. 2002 277 : 17381 4.
38. Vigouroux C, Auclair M, Dubosclard E, Pouchelet M, Capeau J, Courvalin JC, Buendia B. Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q-W mutations in the lamin A-C gene. J Cell Sci. 2001 114 : 4459 68.
39. Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, Huang JD, Li KM, Chau PY, Chen DJ, Pei D, Pendas AM, Cadinanos J, Lopez-Otin C, Tse H F, Hutchison C, Chen J, Cao Y, Cheah KS, Tryggvason K, Zhou Z. Genomic instability in laminopathy-based premature aging. Nat Med. 2005 11 : 780 5.
40. Vytopil M, Benedetti S, Ricci E, Galluzzi G, Dello Russo A, Merlini L, Boriani G, Gallina M, Morandi L, Politano L, Moggio M, Chiveri L, Hausmanova-Petrusewicz I, Ricotti R, Vohanka S, Toman J, Toniolo D. Mutation analysis of the lamin A-C gene (LMNA) among patients with different cardiomuscular phenotypes. J Med Genet. 2003 40 : 132.