Mouse models of laminopathies

Aging Cell

Volumn 12, Issue 1, 2013, Pages 2-10

  Zhang, Haoyue ^a   Kieckhaefer, Julia E ^a   Cao, Kan ^a  

^a Bldg 142   (United States)

Author keywords

Aging; Farnesylation; Lamin A; Laminopathies; Progeria

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; LAMIN A; LAMIN C; PRELAMIN C; PROGERIN; PROTEIN; PROTEIN FARNESYLTRANSFERASE INHIBITOR; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

AGING; ALLELE; EXPERIMENTAL MODEL; GENE DELETION; INTRON; KERATINOCYTE; LAMINOPATHY; MISSENSE MUTATION; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROGERIA; PROTEIN PROCESSING; REVIEW;

AGING; ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; LAMINS; MICE; MUTATION;

EUKARYOTA;

EID: 84872595364     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12021     Document Type: Review

References (55)

1. Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, Lacene E, Fromes Y, Toussaint M, Mura AM, Keller DI, Amthor H, Isnard R, Malissen M, Schwartz K, Bonne G (2005) Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum. Mol. Genet. 14, 155-169.
2. Bergo MO, Gavino B, Ross J, Schmidt WK, Hong C, Kendall LV, Mohr A, Meta M, Genant H, Jiang Y, Wisner ER, Van Bruggen N, Carano RA, Michaelis S, Griffey SM, Young SG (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.
3. Bokenkamp R, Raz V, Venema A, DeRuiter MC, Van Munsteren C, Olive M, Nabel EG, Gittenberger-de Groot AC (2011) Differential temporal and spatial progerin expression during closure of the ductus arteriosus in neonates. PLoS ONE 6, e23975.
4. Cao K, Capell BC, Erdos MR, Djabali K, Collins FS (2007) A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc. Natl Acad. Sci. USA 104, 4949-4954.
5. Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, Nabel EG, Collins FS (2011a) Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J. Clin. Invest. 121, 2833-2844.
6. Cao K, Graziotto JJ, Blair CD, Mazzulli JR, Erdos MR, Krainc D, Collins FS (2011b) Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci. Transl. Med. 3, 89ra58.
7. Capell BC, Collins FS (2006) Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940-952.
8. Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, Conneely KN, Gordon LB, Der CJ, Cox AD, Collins FS (2005) Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 102, 12879-12884.
9. Capell BC, Olive M, Erdos MR, Cao K, Faddah DA, Tavarez UL, Conneely KN, Qu X, San H, Ganesh SK, Chen X, Avallone H, Kolodgie FD, Virmani R, Nabel EG, Collins FS (2008) A farnesyltransferase inhibitor prevents both the onset and late progression of cardiovascular disease in a progeria mouse model. Proc. Natl Acad. Sci. USA 105, 15902-15907.
10. Coffinier C, Jung HJ, Li Z, Nobumori C, Yun UJ, Farber EA, Davies BS, Weinstein MM, Yang SH, Lammerding J, Farahani JN, Bentolila LA, Fong LG, Young SG (2010) Direct synthesis of lamin A, bypassing prelamin a processing, causes misshapen nuclei in fibroblasts but no detectable pathology in mice. J. Biol. Chem. 285, 20818-20826.
11. Davies BS, Barnes RH, Tu Y, Ren S, Andres DA, Spielmann HP, Lammerding J, Wang Y, Young SG, Fong LG (2010) An accumulation of non-farnesylated prelamin A causes cardiomyopathy but not progeria. Hum. Mol. Genet. 19, 2682-2694.
12. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853.
13. Dechat T, Adam SA, Taimen P, Shimi T, Goldman RD (2010) Nuclear lamins. Cold Spring Harb. Perspect. Biol. 2, a000547.
14. Diamond I, Owolabi T, Marco M, Lam C, Glick A (2000) Conditional gene expression in the epidermis of transgenic mice using the tetracycline-regulated transactivators tTA and rTA linked to the keratin 5 promoter. J. Invest. Dermatol. 115, 788-794.
15. Driscoll MK, Albanese JL, Xiong ZM, Mailman M, Losert W, Cao K (2012) Automated image analysis of nuclear shape: what can we learn from a prematurely aged cell? Aging 4, 119-132.
16. van Engelen BGM, Muchir A, Hutchison CJ, van der Kooi AJ, Bonne G, Lammens M (2005) The lethal phenotype of a homozygous nonsense mutation in the lamin A/C gene. Neurology 64, 374-376.
17. Fong LG, Frost D, Meta M, Qiao X, Yang SH, Coffinier C, Young SG (2006a) A protein farnesyltransferase inhibitor ameliorates disease in a mouse model of progeria. Science 311, 1621-1623.
18. Fong LG, Ng JK, Lammerding J, Vickers TA, Meta M, Cote N, Gavino B, Qiao X, Chang SY, Young SR, Yang SH, Stewart CL, Lee RT, Bennett CF, Bergo MO, Young SG (2006b) Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J. Clin. Invest. 116, 743-752.
19. Goldman RD, Shumaker DK, Erdos MR, Eriksson M, Goldman AE, Gordon LB, Gruenbaum Y, Khuon S, Mendez M, Varga R, Collins FS (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 101, 8963-8968.
20. Gruenbaum Y, Margalit A, Goldman RD, Shumaker DK, Wilson KL (2005) The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31.
21. Hernandez L, Roux KJ, Wong ES, Mounkes LC, Mutalif R, Navasankari R, Rai B, Cool S, Jeong JW, Wang H, Lee HS, Kozlov S, Grunert M, Keeble T, Jones CM, Meta MD, Young SG, Daar IO, Burke B, Perantoni AO, Stewart CL (2010) Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev. Cell 19, 413-425.
22. Hutchison CJ (2012) B-type lamins and their elusive roles in metazoan cell proliferation and senescence. EMBO J. 31, 1058-1059.
23. Jung HJ, Coffinier C, Choe Y, Beigneux AP, Davies BSJ, Yang SH, Barnes RH, Hong J, Sun T, Pleasure SJ, Young SG, Fong LG (2012) Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA. Proc. Natl Acad. Sci. USA 109, E423-E431.
24. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan CM, Gaiano N, Ko MS, Zheng Y (2011) Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334, 1706-1710.
25. Kubben N, Voncken JW, Konings G, Van Weeghel M, Van Den Hoogenhof MM, Gijbels M, van Erk A, Schoonderwoerd K, Van Den Bosch B, Dahlmans V, Calis C, Houten SM, Misteli T, Pinto YM (2011) Post-natal myogenic and adipogenic developmental: defects and metabolic impairment upon loss of A-type lamins. Nucleus 2, 195-207.
26. Li W, Yeo LS, Vidal C, McCorquodale T, Herrmann M, Fatkin D, Duque G (2011) Decreased bone formation and osteopenia in lamin a/c-deficient mice. PLoS ONE 6, e19313.
27. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, Djabali K (2007) The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS ONE 2, e1269.
28. Mounkes L, Kozlov S, Burke B, Stewart CL (2003a) The laminopathies: nuclear structure meets disease. Curr. Opin. Genet. Dev. 13, 223-230.
29. Mounkes LC, Kozlov S, Hernandez L, Sullivan T, Stewart CL (2003b) A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423, 298-301.
30. Mounkes LC, Kozlov SV, Rottman JN, Stewart CL (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum. Mol. Genet. 14, 2167-2180.
31. Olive M, Harten I, Mitchell R, Beers JK, Djabali K, Cao K, Erdos MR, Blair C, Funke B, Smoot L, Gerhard-Herman M, Machan JT, Kutys R, Virmani R, Collins FS, Wight TN, Nabel EG, Gordon LB (2010) Cardiovascular pathology in Hutchinson-Gilford progeria: correlation with the vascular pathology of aging. Arterioscler. Thromb. Vasc. Biol. 30, 2301-2309.
32. Osorio FG, Navarro CL, Cadinanos J, Lopez-Mejia IC, Quiros PM, Bartoli C, Rivera J, Tazi J, Guzman G, Varela I, Depetris D, de Carlos F, Cobo J, Andres V, De Sandre-Giovannoli A, Freije JM, Levy N, Lopez-Otin C (2011) Splicing-directed therapy in a new mouse model of human accelerated aging. Sci. Transl. Med. 3, 106ra107.
33. Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K, Lopez-Otin C (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat. Genet. 31, 94-99.
34. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J, Shanahan CM (2010) Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation 121, 2200-2210.
35. Ramos FJ, Chen SC, Garelick MG, Dai DF, Liao CY, Schreiber KH, Mackay VL, An EH, Strong R, Ladiges WC, Rabinovitch PS, Kaeberlein M, Kennedy BK (2012) Rapamycin reverses elevated mTORC1 signaling in lamin A/C-deficient mice, rescues cardiac and skeletal muscle function, and extends survival. Sci. Transl. Med. 4, 144ra103.
36. Rosengardten Y, McKenna T, Grochova D, Eriksson M (2011) Stem cell depletion in Hutchinson-Gilford progeria syndrome. Aging Cell 10, 1011-1020.
37. Sagelius H, Rosengardten Y, Hanif M, Erdos MR, Rozell B, Collins FS, Eriksson M (2008a) Targeted transgenic expression of the mutation causing Hutchinson-Gilford progeria syndrome leads to proliferative and degenerative epidermal disease. J. Cell Sci. 121, 969-978.
38. Sagelius H, Rosengardten Y, Schmidt E, Sonnabend C, Rozell B, Eriksson M (2008b) Reversible phenotype in a mouse model of Hutchinson-Gilford progeria syndrome. J. Med. Genet. 45, 794-801.
39. Scaffidi P, Misteli T (2005) Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat. Med. 11, 440-445.
40. Scaffidi P, Misteli T (2006) Lamin A-dependent nuclear defects in human aging. Science 312, 1059-1063.
41. Stewart CL, Kozlov S, Fong LG, Young SG (2007) Mouse models of the laminopathies. Exp. Cell Res. 313, 2144-2156.
42. Stuurman N, Heins S, Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J. Struct. Biol. 122, 42-66.
43. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J. Cell Biol. 147, 913-920.
44. Tong J, Li W, Vidal C, Yeo LS, Fatkin D, Duque G (2011) Lamin A/C deficiency is associated with fat infiltration of muscle and bone. Mech. Ageing Dev. 132, 552-559.
45. Tsai MY, Wang S, Heidinger JM, Shumaker DK, Adam SA, Goldman RD, Zheng Y (2006) A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893.
46. Varga R, Eriksson M, Erdos MR, Olive M, Harten I, Kolodgie F, Capell BC, Cheng J, Faddah D, Perkins S, Avallone H, San H, Qu X, Ganesh S, Gordon LB, Virmani R, Wight TN, Nabel EG, Collins FS (2006) Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gilford progeria syndrome. Proc. Natl Acad. Sci. USA 103, 3250-3255.
47. Vergnes L, Peterfy M, Bergo MO, Young SG, Reue K (2004) Lamin B1 is required for mouse development and nuclear integrity. Proc. Natl Acad. Sci. USA 101, 10428-10433.
48. Vorburger K, Kitten GT, Nigg EA (1989) Modification of nuclear lamin proteins by a mevalonic acid derivative occurs in reticulocyte lysates and requires the cysteine residue of the C-terminal CXXM motif. EMBO J. 8, 4007-4013.
49. Wang Y, Herron AJ, Worman HJ (2006) Pathology and nuclear abnormalities in hearts of transgenic mice expressing M371K lamin A encoded by an LMNA mutation causing Emery-Dreifuss muscular dystrophy. Hum. Mol. Genet. 15, 2479-2489.
50. Wang Y, Panteleyev AA, Owens DM, Djabali K, Stewart CL, Worman HJ (2008) Epidermal expression of the truncated prelamin A causing Hutchinson-Gilford progeria syndrome: effects on keratinocytes, hair and skin. Hum. Mol. Genet. 17, 2357-2369.
51. Worman HJ, Fong LG, Muchir A, Young SG (2009) Laminopathies and the long strange trip from basic cell biology to therapy. J. Clin. Invest. 119, 1825-1836.
52. Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, Sandoval S, Meta M, Bendale P, Gelb MH, Young SG, Fong LG (2005) Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc. Natl Acad. Sci. USA 102, 10291-10296.
53. Yang SH, Meta M, Qiao X, Frost D, Bauch J, Coffinier C, Majumdar S, Bergo MO, Young SG, Fong LG (2006) A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J. Clin. Invest. 116, 2115-2121.
54. Yang SH, Andres DA, Spielmann HP, Young SG, Fong LG (2008) Progerin elicits disease phenotypes of progeria in mice whether or not it is farnesylated. J. Clin. Invest. 118, 3291-3300.
55. Yang SH, Chang SY, Ren S, Wang Y, Andres DA, Spielmann HP, Fong LG, Young SG (2011) Absence of progeria-like disease phenotypes in knock-in mice expressing a non-farnesylated version of progerin. Hum. Mol. Genet. 20, 436-444.