Lamins are rapamycin targets that impact human longevity: A study in centenarians

Journal of Cell Science

Volumn 127, Issue 1, 2014, Pages 147-157

  Lattanzi, Giovanna ^a   Ortolani, Michela ^a   Columbaro, Marta ^b   Prencipe, Sabino ^a,c   Mattioli, Elisabetta ^a,b   Lanzarini, Catia ^c   Maraldi, Nadir M ^a,b,c   Cenni, Vittoria ^a,b   Garagnani, Paolo ^c   Salvioli, Stefano ^c   Storci, Gianluca ^c   Bonafè, Massimiliano ^c   Capanni, Cristina ^a,b   Franceschi, Claudio ^c  

^a CNR   (Italy)

^b RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

53BP1; Centenarian; Chromatin organisation; Lamins; Prelamin a; Rapamycin

Indexed keywords

LAMIN; MEMBRANE PROTEIN; NUCLEAR PROTEIN; PRELAMIN A; PROTEIN 53BP1; PROTEIN SUN1; PROTEIN ZMPSTE24; RAPAMYCIN; UNCLASSIFIED DRUG;

AGING; ARTICLE; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; CHROMATIN STRUCTURE; CYTOPLASM; DNA DAMAGE; DOWN REGULATION; FIBROBLAST; HETEROCHROMATIN; HUMAN; HUMAN CELL; HUMAN TISSUE; LONGEVITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; SENESCENCE; VERY ELDERLY;

53BP1; CENTENARIAN; CHROMATIN ORGANISATION; LAMINS; PRELAMIN A; RAPAMYCIN;

AGED, 80 AND OVER; AGING; ANTIBIOTICS, ANTINEOPLASTIC; CELL AGING; CELL NUCLEUS; CHROMATIN; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LONGEVITY; MEMBRANE PROTEINS; METALLOENDOPEPTIDASES; NUCLEAR PROTEINS; OXIDATIVE STRESS; PROTEIN PRECURSORS; SIGNAL TRANSDUCTION; SIROLIMUS;

EID: 84891441519     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133983     Document Type: Article

References (52)

1. Atsumi, Y., Fujimori, H., Fukuda, H., Inase, A., Shinohe, K., Yoshioka, Y., Shikanai, M., Ichijima, Y., Unno, J., Mizutani, S. et al. (2011). Onset of quiescence following p53 mediated down-regulation of H2AX in normal cells. PLoS ONE 6, e23432.
2. Bandhakavi, S., Kim, Y. M., Ro, S. H., Xie, H., Onsongo, G., Jun, C. B., Kim, D. H. and Griffin, T. J. (2010). Quantitative nuclear proteomics identifies mTOR regulation of DNA damage response. Mol. Cell. Proteomics 9, 403-414.
3. Barascu, A., Le Chalony, C., Pennarun, G., Genet, D., Imam, N., Lopez, B. and Bertrand, P. (2012). Oxidative stress induces an ATM-independent senescence pathway through p38 MAPK-mediated lamin B1 accumulation. EMBO J. 31, 1080-1094.
4. Bertacchini, J., Beretti, F., Cenni, V., Guida, M., Gibellini, F., Mediani, L., Marin, O., Maraldi, N. M., de Pol, A., Lattanzi, G. et al. (2013). The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FASEB J. 27, 2145-2155.
5. Brachner, A. and Foisner, R. (2011). Lamins reach out to novel functions in DNA damage repair. Cell Cycle 10, 3426.
6. Burtner, C. R. and Kennedy, B. K. (2010). Progeria syndromes and ageing: what is the connection? Nat. Rev. Mol. Cell Biol. 11, 567-578.
7. Cao, K., Graziotto, J. J., Blair, C. D., Mazzulli, J. R., Erdos, M. R., Krainc, D. and Collins, F. S. (2011). Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Sci. Transl. Med. 3, 89ra58.
8. Capanni, C., Mattioli, E., Columbaro, M., Lucarelli, E., Parnaik, V. K., Novelli, G., Wehnert, M., Cenni, V., Maraldi, N. M., Squarzoni, S. et al. (2005). Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum. Mol. Genet. 14, 1489-1502.
9. Capanni, C., Cenni, V., Haraguchi, T., Squarzoni, S., Schü chner, S., Ogris, E., Novelli, G., Maraldi, N. M. and Lattanzi, G. (2010). Lamin A precursor induces barrier-to-autointegration factor nuclear localization. Cell Cycle 9, 2600-2610.
10. Capanni, C., Squarzoni, S., Cenni, V., D'Apice, M. R., Gambineri, A., Novelli, G., Wehnert, M., Pasquali, R., Maraldi, N. M. and Lattanzi, G. (2012). Familial partial lipodystrophy, mandibuloacral dysplasia and restrictive dermopathy feature barrier-to-autointegration factor (BAF) nuclear redistribution. Cell Cycle 11, 3568-3577.
11. Cenni, V., Bavelloni, A., Beretti, F., Tagliavini, F., Manzoli, L., Lattanzi, G., Maraldi, N. M., Cocco, L. and Marmiroli, S. (2011a). Ankrd2/ARPP is a novel Akt2 specific substrate and regulates myogenic differentiation upon cellular exposure to H(2)O(2). Mol. Biol. Cell 22, 2946-2956.
12. Cenni, V., Capanni, C., Columbaro, M., Ortolani, M., D'Apice, M. R., Novelli, G., Fini, M., Marmiroli, S., Scarano, E., Maraldi, N. M. et al. (2011b). Autophagic degradation of farnesylated prelamin A as a therapeutic approach to laminlinked progeria. Eur. J. Histochem. 55, e36.
13. Cevenini, E., Invidia, L., Lescai, F., Salvioli, S., Tieri, P., Castellani, G. and Franceschi, C. (2008). Human models of aging and longevity. Expert Opin. Biol. Ther. 8, 1393-1405.
14. Chevanne, M., Calia, C., Zampieri, M., Cecchinelli, B., Caldini, R., Monti, D., Bucci, L., Franceschi, C. and Caiafa, P. (2007). Oxidative DNA damage repair and parp 1 and parp 2 expression in Epstein-Barr virus-immortalized B lymphocyte cells from young subjects, old subjects, and centenarians. Rejuvenation Res. 10, 191-204.
15. Columbaro, M., Mattioli, E., Maraldi, N. M., Ortolani, M., Gasparini, L., D'Apice, M. R., Postorivo, D., Nardone, A. M., Avnet, S., Cortelli, P. et al. (2013). Oct-1 recruitment to the nuclear envelope in adult-onset autosomal dominant leukodystrophy. Biochim. Biophys. Acta 1832, 411-420.
16. De Cecco, M., Jeyapalan, J., Zhao, X., Tamamori-Adachi, M. and Sedivy, J. M. (2011). Nuclear protein accumulation in cellular senescence and organismal aging revealed with a novel single-cell resolution fluorescence microscopy assay. Aging (Albany, NY) 3, 955-967.
17. Di Micco, R., Sulli, G., Dobreva, M., Liontos, M., Botrugno, O. A., Gargiulo, G., dal Zuffo, R., Matti, V., d'Ario, G., Montani, E. et al. (2011). Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer. Nat. Cell Biol. 13, 292-302.
18. Dominici, S., Fiori, V., Magnani, M., Schena, E., Capanni, C., Camozzi, D., D'Apice, M. R., Le Dour, C., Auclair, M., Caron, M. et al. (2009). Different prelamin A forms accumulate in human fibroblasts: a study in experimental models and progeria. Eur. J. Histochem. 53, 43-52.
19. Dreesen, O., Chojnowski, A., Ong, P. F., Zhao, T. Y., Common, J. E., Lunny, D., Lane, E. B., Lee, S. J., Vardy, L. A., Stewart, C. L. et al. (2013). Lamin B1 fluctuations have differential effects on cellular proliferation and senescence. J. Cell Biol. 200, 605-617.
20. Freund, A., Laberge, R. M., Demaria, M. and Campisi, J. (2012). Lamin B1 loss is a senescence-associated biomarker. Mol. Biol. Cell 23, 2066-2075.
21. Gonzalez-Suarez, I., Redwood, A. B., Grotsky, D. A., Neumann, M. A., Cheng, E. H., Stewart, C. L., Dusso, A. and Gonzalo, S. (2011). A new pathway that regulates 53BP1 stability implicates cathepsin L and vitamin D in DNA repair. EMBO J. 30, 3383-3396.
22. Graziotto, J. J., Cao, K., Collins, F. S. and Krainc, D. (2012). Rapamycin activates autophagy in Hutchinson-Gilford progeria syndrome: implications for normal aging and age-dependent neurodegenerative disorders. Autophagy 8, 147-151.
23. Han, S. and Brunet, A. (2012). Histone methylation makes its mark on longevity. Trends Cell Biol. 22, 42-49.
24. Haque, F., Mazzeo, D., Patel, J. T., Smallwood, D. T., Ellis, J. A., Shanahan, C. M. and Shackleton, S. (2010). Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J. Biol. Chem. 285, 3487-3498.
25. Ibrahim, M. X., Sayin, V. I., Akula, M. K., Liu, M., Fong, L. G., Young, S. G. and Bergo, M. O. (2013). Targeting isoprenylcysteine methylation ameliorates disease in a mouse model of progeria. Science 340, 1330-1333.
26. Koch, C. M., Joussen, S., Schellenberg, A., Lin, Q., Zenke, M. and Wagner, W. (2012). Monitoring of cellular senescence by DNA-methylation at specific CpG sites. Aging Cell 11, 366-369.
27. Kosar, M., Bartkova, J., Hubackova, S., Hodny, Z., Lukas, J. and Bartek, J. (2011). Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type- and insult-dependent manner and follow expression of p16(ink4a). Cell Cycle 10, 457-468.
28. Krishnan, V., Chow, M. Z., Wang, Z., Zhang, L., Liu, B., Liu, X. and Zhou, Z. (2011). Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc. Natl. Acad. Sci. USA 108, 12325-12330.
29. Kueper, T., Grune, T., Prahl, S., Lenz, H., Welge, V., Biernoth, T., Vogt, Y., Muhr, G. M., Gaemlich, A., Jung, T. et al. (2007). Vimentin is the specific target in skin glycation. Structural prerequisites, functional consequences, and role in skin aging. J. Biol. Chem. 282, 23427-23436.
30. Lattanzi, G. (2011). Prelamin A-mediated nuclear envelope dynamics in normal and laminopathic cells. Biochem. Soc. Trans. 39, 1698-1704.
31. Lattanzi, G., Columbaro, M., Mattioli, E., Cenni, V., Camozzi, D., Wehnert, M., Santi, S., Riccio, M., Del Coco, R., Maraldi, N. M. et al. (2007). Pre-Lamin A processing is linked to heterochromatin organization. J. Cell. Biochem. 102, 1149-1159.
32. Liu, B., Wang, J., Chan, K. M., Tjia, W. M., Deng, W., Guan, X., Huang, J. D., Li, K. M., Chau, P. Y., Chen, D. J. et al. (2005). Genomic instability in laminopathybased premature aging. Nat. Med. 11, 780-785.
33. Liu, Y., Drozdov, I., Shroff, R., Beltran, L. E. and Shanahan, C. M. (2013). Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ. Res. 112, e99-e109.
34. Maraldi, N. M. and Lattanzi, G. (2007). Involvement of prelamin A in laminopathies. Crit. Rev. Eukaryot. Gene Expr. 17, 317-334.
35. Maraldi, N. M., Capanni, C., Cenni, V., Fini, M. and Lattanzi, G. (2011). Laminopathies and lamin-associated signaling pathways. J. Cell. Biochem. 112, 979-992.
36. Marmiroli, S., Bertacchini, J., Beretti, F., Cenni, V., Guida, M., De Pol, A., Maraldi, N. M. and Lattanzi, G. (2009). A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward. J. Cell. Physiol. 220, 553-561.
37. Matarrese, P., Tinari, A., Ascione, B., Gambardella, L., Remondini, D., Salvioli, S., Tenedini, E., Tagliafico, E., Franceschi, C. and Malorni, W. (2012). Survival features of EBV-stabilized cells from centenarians: morpho-functional and transcriptomic analyses. Age (Dordr.) 34, 1341-1359.
38. Mattioli, E., Columbaro, M., Capanni, C., Santi, S., Maraldi, N. M., D'Apice, M. R., Novelli, G., Riccio, M., Squarzoni, S., Foisner, R. et al. (2008). Drugs affecting prelamin A processing: effects on heterochromatin organization. Exp. Cell Res. 314, 453-462.
39. Mattioli, E., Columbaro, M., Capanni, C., Maraldi, N. M., Cenni, V., Scotlandi, K., Marino, M. T., Merlini, L., Squarzoni, S. and Lattanzi, G. (2011). Prelamin A-mediated recruitment of SUN1 to the nuclear envelope directs nuclear positioning in human muscle. Cell Death Differ. 18, 1305-1315.
40. Muñ oz-Najar, U. and Sedivy, J. M. (2011). Epigenetic control of aging. Antioxid. Redox Signal. 14, 241-259.
41. Muteliefu, G., Shimizu, H., Enomoto, A., Nishijima, F., Takahashi, M. and Niwa, T. (2012). Indoxyl sulfate promotes vascular smooth muscle cell senescence with upregulation of p53, p21, and prelamin A through oxidative stress. Am. J. Physiol. 303, C126-C134.
42. Pospelova, T. V., Leontieva, O. V., Bykova, T. V., Zubova, S. G., Pospelov, V. A. and Blagosklonny, M. V. (2012). Suppression of replicative senescence by rapamycin in rodent embryonic cells. Cell Cycle 11, 2402-2407.
43. Ragnauth, C. D., Warren, D. T., Liu, Y., McNair, R., Tajsic, T., Figg, N., Shroff, R., Skepper, J. and Shanahan, C. M. (2010). Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation 121, 2200-2210.
44. Ramos, F. J., Chen, S. C., Garelick, M. G., Dai, D. F., Liao, C. Y., Schreiber, K. H., MacKay, V. L., An, E. H., Strong, R., Ladiges, W. C. et al. (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.
45. Richards, S. A., Muter, J., Ritchie, P., Lattanzi, G. and Hutchison, C. J. (2011). The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with Nacetyl cysteine. Hum. Mol. Genet. 20, 3997-4004.
46. Schellenberg, A., Lin, Q., Schü ler, H., Koch, C. M., Joussen, S., Denecke, B., Walenda, G., Pallua, N., Suschek, C. V., Zenke, M. et al. (2011). Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging (Albany, NY) 3, 873-888.
47. Shimi, T., Butin-Israeli, V., Adam, S. A., Hamanaka, R. B., Goldman, A. E., Lucas, C. A., Shumaker, D. K., Kosak, S. T., Chandel, N. S. and Goldman, R. D. (2011). The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev. 25, 2579-2593.
48. Sikora, E., Arendt, T., Bennett, M. and Narita, M. (2011). Impact of cellular senescence signature on ageing research. Ageing Res. Rev. 10, 146-152.
49. Tesco, G., Vergelli, M., Grassilli, E., Salomoni, P., Bellesia, E., Sikora, E., Radziszewska, E., Barbieri, D., Latorraca, S., Fagiolo, U. et al. (1998). Growth properties and growth factor responsiveness in skin fibroblasts from centenarians. Biochem. Biophys. Res. Commun. 244, 912-916.
50. Ukekawa, R., Miki, K., Fujii, M., Hirano, H. and Ayusawa, D. (2007). Accumulation of multiple forms of lamin A with down-regulation of FACE-1 suppresses growth in senescent human cells. Genes Cells 12, 397-406.
51. Wilkinson, J. E., Burmeister, L., Brooks, S. V., Chan, C. C., Friedline, S., Harrison, D. E., Hejtmancik, J. F., Nadon, N., Strong, R., Wood, L. K. et al. (2012). Rapamycin slows aging in mice. Aging Cell 11, 675-682.
52. Zironi, I., Gaibani, P., Remondini, D., Salvioli, S., Altilia, S., Pierini, M., Aicardi, G., Verondini, E., Milanesi, L., Bersani, F. et al. (2010). Molecular remodeling of potassium channels in fibroblasts from centenarians: a marker of longevity? Mech. Ageing Dev. 131, 674-681.