Rapamycin treatment of Mandibuloacral Dysplasia cells rescues localization of chromatin-associated proteins and cell cycle dynamics

Aging

Volumn 6, Issue 9, 2014, Pages 755-770

  Cenni, Vittoria ^a   Capanni, Cristina ^a   Mattioli, Elisabetta ^a   Columbaro, Marta ^a   Wehnert, Manfred ^b   Ortolani, Michela ^a   Fini, Milena ^a   Novelli, Giuseppe ^c   Bertacchini, Jessika ^d   Maraldi, Nadir M ^a   Marmiroli, Sandra ^d   D'Apice, Maria Rosaria ^c,e   Prencipe, Sabino ^a   Squarzoni, Stefano ^a   Lattanzi, Giovanna ^a  

^a RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^e TOR VERGATA UNIVERSITY HOSPITAL   (Italy)

Author keywords

Mandibuloacral Dysplasia (MADA); Oct 1; Prelamin A; Rapamycin; SIRT 1

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; CHROMATIN; DNA BINDING PROTEIN; LAMINA-ASSOCIATED POLYPEPTIDE 2; MEMBRANE PROTEIN; NUCLEAR PROTEIN; OCTAMER TRANSCRIPTION FACTOR 1; PRELAMIN A; PROTEIN PRECURSOR; RAPAMYCIN;

ACRO-OSTEOLYSIS; ADULT; CELL CULTURE; CELL CYCLE; CHROMATIN; CONGENITAL MALFORMATION; CONGENITAL SKIN DISEASE; CONTRACTURE; DNA REPAIR; DRUG EFFECTS; FIBROBLAST; GENETICS; HUMAN; LIPODYSTROPHY; MANDIBLE; METABOLISM; NEWBORN;

ACRO-OSTEOLYSIS; ADULT; ANTIBIOTICS, ANTINEOPLASTIC; CELL CYCLE; CELLS, CULTURED; CHROMATIN; CONTRACTURE; DNA REPAIR; DNA-BINDING PROTEINS; FIBROBLASTS; HUMANS; INFANT, NEWBORN; LIPODYSTROPHY; MANDIBLE; MEMBRANE PROTEINS; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-1; PROTEIN PRECURSORS; SIROLIMUS; SKIN ABNORMALITIES;

EID: 84907813329     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100680     Document Type: Article

References (68)

1. Davies BS, Coffinier C, Yang SH, Barnes RH, 2nd, Jung HJ, Young SG and Fong LG. Investigating the purpose of prelamin A processing. Nucleus. 2011; 2:4-9.
2. Capanni C, Del Coco R, Squarzoni S, Columbaro M, Mattioli E, Camozzi D, Rocchi A, Scotlandi K, Maraldi N, Foisner R and Lattanzi G. Prelamin A is involved in early steps of muscle differentiation. Experimental cell research. 2008; 314:3628-3637.
3. Mattioli E, Columbaro M, Capanni C, Maraldi NM, Cenni V, Scotlandi K, Marino MT, Merlini L, Squarzoni S and Lattanzi G. Prelamin A-mediated recruitment of SUN1 to the nuclear envelope directs nuclear positioning in human muscle. Cell death and differentiation. 2011; 18:1305-1315.
4. Lattanzi G, Ortolani M, Columbaro M, Prencipe S, Mattioli E, Lanzarini C, Maraldi NM, Cenni V, Garagnani P, Salvioli S, Storci G, Bonafe M, Capanni C, et al. Lamins are rapamycin targets that impact human longevity: a study in centenarians. Journal of cell science. 2014; 127:147-157.
5. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J and Shanahan CM. Prelamin A Acts to Accelerate Smooth Muscle Cell Senescence and Is a Novel Biomarker of Human Vascular Aging. Circulation. 2010;121:2200-2210.
6. Maraldi NM and Lattanzi G. Involvement of prelamin A in laminopathies. Crit Rev Eukaryot Gene Expr. 2007; 17:317-334.
7. Worman HJ, Ostlund C and Wang Y. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol. 2010; 2:a000760.
8. Columbaro M, Capanni C, Mattioli E, Novelli G, Parnaik VK, Squarzoni S, Maraldi NM and Lattanzi G. Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cellular and molecular life sciences: CMLS. 2005; 62:2669-2678.
9. Columbaro M, Mattioli E, Schena E, Capanni C, Cenni V, Levy N, Navarro CL, Del Coco R, Squarzoni S, Camozzi D, Hutchison CJ, Wehnert M and Lattanzi G. Prelamin A processing and functional effects in restrictive dermopathy. Cell cycle. 2010; 9:4766-4768.
10. Navarro CL, Cadinanos J, De Sandre-Giovannoli A, Bernard R, Courrier S, Boccaccio I, Boyer A, Kleijer WJ, Wagner A, Giuliano F, Beemer FA, Freije JM, Cau P, et al. Loss of ZMPSTE24 (FACE-1) causes autosomal recessive restrictive dermopathy and accumulation of Lamin A precursors. Human molecular genetics. 2005; 14:1503-1513.
11. Camozzi D, D'Apice MR, Schena E, Cenni V, Columbaro M, Capanni C, Maraldi NM, Squarzoni S, Ortolani M, Novelli G and Lattanzi G. Altered chromatin organization and SUN2 localization in mandibuloacral dysplasia are rescued by drug treatment. Histochemistry and cell biology. 2012; 138(4):643-651.
12. Capanni C, Mattioli E, Columbaro M, Lucarelli E, Parnaik VK, Novelli G, Wehnert M, Cenni V, Maraldi NM, Squarzoni S and Lattanzi G. Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Human molecular genetics. 2005; 14:1489-1502.
13. Gonzalez JM, Navarro-Puche A, Casar B, Crespo P and Andres V. Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. The Journal of cell biology. 2008; 183:653-666.
14. Ruiz de Eguino G, Infante A, Schlangen K, Aransay AM, Fullaondo A, Soriano M, Garcia-Verdugo JM, Martin AG and Rodriguez CI. Sp1 transcription factor interaction with accumulated prelamin a impairs adipose lineage differentiation in human mesenchymal stem cells: essential role of sp1 in the integrity of lipid vesicles. Stem cells translational medicine. 2012; 1:309-321.
15. Columbaro M, Mattioli E, Maraldi NM, Ortolani M, Gasparini L, D'Apice MR, Postorivo D, Nardone AM, Avnet S, Cortelli P, Liguori R and Lattanzi G. Oct-1 recruitment to the nuclear envelope in adult-onset autosomal dominant leukodystrophy. Biochimica et biophysica acta. 2013; 1832:411-420.
16. Cenni V, Capanni C, Columbaro M, Ortolani M, D'Apice MR, Novelli G, Fini M, Marmiroli S, Scarano E, Maraldi NM, Squarzoni S, Prencipe S and Lattanzi G. Autophagic degradation of farnesylated prelamin A as a therapeutic approach to laminlinked progeria. European journal of histochemistry: EJH. 2011;55:e36.
17. Wang P and Jin T. Hydrogen peroxide stimulates nuclear import of the POU homeodomain protein Oct-1 and its repressive effect on the expression of Cdx-2. BMC cell biology. 2010; 11:56.
18. Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A and Dalton M. The processing pathway of prelamin A. J Cell Sci. 1994; 107:61-67.
19. Filesi I, Gullotta F, Lattanzi G, D'Apice MR, Capanni C, Nardone AM, Columbaro M, Scarano G, Mattioli E, Sabatelli P, Maraldi NM, Biocca S and Novelli G. Alterations of nuclear envelope and chromatin organization in mandibuloacral dysplasia, a rare form of laminopathy. Physiological genomics. 2005; 23:150-158.
20. Marino G, Ugalde AP, Salvador-Montoliu N, Varela I, Quiros PM, Cadinanos J, van der Pluijm I, Freije JM and Lopez-Otin C. Premature aging in mice activates a systemic metabolic response involving autophagy induction. Human molecular genetics. 2008; 17:2196-2211.
21. Park YE, Hayashi YK, Bonne G, Arimura T, Noguchi S, Nonaka I and Nishino I. Autophagic degradation of nuclear components in mammalian cells. Autophagy. 2009; 5:795-804.
22. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, Blaauw B, Urciuolo A, Tiepolo T, Merlini L, Maraldi NM, Bernardi P, Sandri M, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med. 2011; 16:1313-1320.
23. Ni HM, Bockus A, Wozniak AL, Jones K, Weinman S, Yin XM and Ding WX. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy. 2011; 7:188-204.
24. Lattanzi G, Columbaro M, Mattioli E, Cenni V, Camozzi D, Wehnert M, Santi S, Riccio M, Del Coco R, Maraldi NM, Squarzoni S, Foisner R and Capanni C. Pre-Lamin A processing is linked to heterochromatin organization. Journal of cellular biochemistry. 2007; 102:1149-1159.
25. Marmiroli S, Bertacchini J, Beretti F, Cenni V, Guida M, De Pol A, Maraldi NM and Lattanzi G. A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward. Journal of cellular physiology. 2009; 220:553-561.
26. Cenni V, Bertacchini J, Beretti F, Lattanzi G, Bavelloni A, Riccio M, Ruzzene M, Marin O, Arrigoni G, Parnaik V, Wehnert M, Maraldi NM, de Pol A, et al. Lamin A Ser404 is a nuclear target of Akt phosphorylation in C2C12 cells. Journal of proteome research. 2008; 7:4727-4735.
27. Bertacchini J, Beretti F, Cenni V, Guida M, Gibellini F, Mediani L, Marin O, Maraldi NM, de Pol A, Lattanzi G, Cocco L and Marmiroli S. The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2013; 27:2145-2155.
28. Grumati P, Coletto L, Sandri M and Bonaldo P. Autophagy induction rescues muscular dystrophy. Autophagy. 2011; 7:426-428.
29. Madeo F, Tavernarakis N and Kroemer G. Can autophagy promote longevity? Nat Cell Biol. 2011; 12:842-846.
30. Moore SF, Hunter RW and Hers I. mTORC2 protein-mediated protein kinase B (Akt) serine 473 phosphorylation is not required for Akt1 activity in human platelets. J Biol Chem. 2011;286:24553-24560.
31. Cao K, Graziotto JJ, Blair CD, Mazzulli JR, Erdos MR, Krainc D and Collins FS. Rapamycin reverses cellular phenotypes and enhances mutant protein clearance in Hutchinson-Gilford progeria syndrome cells. Science translational medicine. 2011;3:89ra58.
32. Bellodi C, Lidonnici MR, Hamilton A, Helgason GV, Soliera AR, Ronchetti M, Galavotti S, Young KW, Selmi T, Yacobi R, Van Etten RA, Donato N, Hunter A, et al. Targeting autophagy potentiates tyrosine kinase inhibitor-induced cell death in Philadelphia chromosome-positive cells, including primary CML stem cells. J Clin Invest. 2009; 119:1109-1123.
33. Novelli G, Muchir A, Sangiuolo F, Helbling-Leclerc A, D'Apice MR, Massart C, Capon F, Sbraccia P, Federici M, Lauro R, Tudisco C, Pallotta R, Scarano G, et al. Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. American journal of human genetics. 2002; 71:426-431.
34. Adam SA, Butin-Israeli V, Cleland MM, Shimi T and Goldman RD. Disruption of lamin B1 and lamin B2 processing and localization by farnesyltransferase inhibitors. Nucleus. 2013;4:142-150.
35. Infante A, Gago A, de Eguino GR, Calvo-Fernandez T, Gomez-Vallejo V, Llop J, Schlangen K, Fullaondo A, Aransay AM, Martin A and Rodriguez CI. Prelamin A accumulation and stress conditions induce impaired Oct-1 activity and autophagy in prematurely aged human mesenchymal stem cell. Aging. 2014; 6:264-280.
36. Lombardi F, Gullotta F, Columbaro M, Filareto A, D'Adamo M, Vielle A, Guglielmi V, Nardone AM, Azzolini V, Grosso E, Lattanzi G, D'Apice MR, Masala S, et al. Compound heterozygosity for mutations in LMNA in a patient with a myopathic and lipodystrophic mandibuloacral dysplasia type A phenotype. The Journal of clinical endocrinology and metabolism. 2007; 92:4467-4471.
37. Bosch-Presegue L, Raurell-Vila H, Marazuela-Duque A, Kane-Goldsmith N, Valle A, Oliver J, Serrano L and Vaquero A. Stabilization of Suv39H1 by SirT1 is part of oxidative stress response and ensures genome protection. Molecular cell. 2011;42:210-223.
38. Vaquero A, Scher M, Erdjument-Bromage H, Tempst P, Serrano L and Reinberg D. SIRT1 regulates the histone methyltransferase SUV39H1 during heterochromatin formation. Nature. 2007; 450:440-444.
39. Shermoen AW, McCleland ML and O'Farrell PH. Developmental control of late replication and S phase length. Current biology: CB. 2010; 20:2067-2077.
40. di Masi A, D'Apice MR, Ricordy R, Tanzarella C and Novelli G. The R527H mutation in LMNA gene causes an increased sensitivity to ionizing radiation. Cell cycle. 2008; 7:2030-2037.
41. Butin-Israeli V, Adam SA and Goldman RD. Regulation of nucleotide excision repair by nuclear lamin b1. PloS one. 2013;8:e69169.
42. Richards SA, Muter J, Ritchie P, Lattanzi G and Hutchison CJ. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N-acetyl cysteine. Human molecular genetics. 2011; 20:3997-4004.
43. Pospelova TV, Demidenko ZN, Bukreeva EI, Pospelov VA, Gudkov AV and Blagosklonny MV. Pseudo-DNA damage response in senescent cells. Cell cycle. 2009; 8:4112-4118.
44. Leontieva OV, Lenzo F, Demidenko ZN and Blagosklonny MV. Hyper-mitogenic drive coexists with mitotic incompetence in senescent cells. Cell cycle. 2012; 11(24):4642-4649.
45. Blagosklonny MV. Cell cycle arrest is not yet senescence, which is not just cell cycle arrest: terminology for TOR-driven aging. Aging. 2012; 4:159-165.
46. Serrano M. Dissecting the role of mTOR complexes in cellular senescence. Cell cycle. 2012; 11:2231-2232.
47. Kolesnichenko M, Hong L, Liao R, Vogt PK and Sun P. Attenuation of TORC1 signaling delays replicative and oncogenic RAS-induced senescence. Cell cycle. 2012; 11:2391-2401.
48. Khapre RV, Kondratova AA, Patel S, Dubrovsky Y, Wrobel M, Antoch MP and Kondratov RV. BMAL1-dependent regulation of the mTOR signaling pathway delays aging. Aging. 2014; 6:48-57.
49. Camps J, Wangsa D, Falke M, Brown M, Case CM, Erdos MR and Ried T. Loss of lamin B1 results in prolongation of S phase and decondensation of chromosome territories. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2014.
50. Scaffidi P and Misteli T. Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med. 2005; 11:440-445.
51. Mijaljica D, Prescott M and Devenish RJ. The intricacy of nuclear membrane dynamics during nucleophagy. Nucleus. 2010; 1:213-223.
52. Ramos FJ, Chen SC, Garelick MG, Dai DF, Liao CY, Schreiber KH, MacKay VL, An EH, Strong R, Ladiges WC, Rabinovitch PS, Kaeberlein M and Kennedy BK. Rapamycin reverses elevated mTORC1 signaling in lamin A/C-deficient mice, rescues cardiac and skeletal muscle function, and extends survival. Science translational medicine. 2012; 4:144ra103.
53. Blagosklonny MV. Cell cycle arrest is not senescence. Aging. 2011; 3:94-101.
54. Wu JJ, Liu J, Chen EB, Wang JJ, Cao L, Narayan N, Fergusson MM, Rovira, II, Allen M, Springer DA, Lago CU, Zhang S, Dubois W, et al. Increased Mammalian Lifespan and a Segmental and Tissue-Specific Slowing of Aging after Genetic Reduction of mTOR Expression. Cell reports. 2013.
55. Kolosova NG, Vitovtov AO, Muraleva NA, Akulov AE, Stefanova NA and Blagosklonny MV. Rapamycin suppresses brain aging in senescence-accelerated OXYS rats. Aging. 2013;5:474-484.
56. Komarova EA, Antoch MP, Novototskaya LR, Chernova OB, Paszkiewicz G, Leontieva OV, Blagosklonny MV and Gudkov AV. Rapamycin extends lifespan and delays tumorigenesis in heterozygous p53+/- mice. Aging. 2012; 4:709-714.
57. Cenni V, Capanni C, Columbaro M, Ortolani M, D'Apice MR, Novelli G, Fini M, Marmiroli S, Scarano E, Maraldi NM, Squarzoni S, Prencipe S and Lattanzi G. Autophagic degradation of farnesylated prelamin A as a therapeutic approach to laminlinked progeria. Eur J Histochem. 2011; 55:e36.
58. Varela I, Pereira S, Ugalde AP, Navarro CL, Suarez MF, Cau P, Cadinanos J, Osorio FG, Foray N, Cobo J, de Carlos F, Levy N, Freije JM, et al. Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nature medicine. 2008; 14:767-772.
59. Gordon LB, Kleinman ME, Miller DT, Neuberg DS, Giobbie-Hurder A, Gerhard-Herman M, Smoot LB, Gordon CM, Cleveland R, Snyder BD, Fligor B, Bishop WR, Statkevich P, et al. Clinical trial of a farnesyltransferase inhibitor in children with Hutchinson-Gilford progeria syndrome. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109:16666-16671.
60. Richards SA, Muter J, Ritchie P, Lattanzi G and Hutchison CJ. The accumulation of un-repairable DNA damage in laminopathy progeria fibroblasts is caused by ROS generation and is prevented by treatment with N-acetyl cysteine. Hum Mol Genet. 2011; 20:3997-4004.
61. Avnet S, Pallotta R, Perut F, Baldini N, Pittis MG, Saponari A, Lucarelli E, Dozza B, Greggi T, Maraldi NM, Capanni C, Mattioli E, Columbaro M, et al. Osteoblasts from a mandibuloacral dysplasia patient induce human blood precursors to differentiate into active osteoclasts. Biochimica et biophysica acta. 2011; 1812:711-718.
62. Mehta IS, Eskiw CH, Arican HD, Kill IR and Bridger JM. Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford Progeria syndrome cells. Genome Biol. 2011;12:R74.
63. Kumaran RI, Muralikrishna B and Parnaik VK. Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription. The Journal of cell biology. 2002; 159:783-793.
64. Capanni C, Cenni V, Haraguchi T, Squarzoni S, Schuchner S, Ogris E, Novelli G, Maraldi NM and Lattanzi G. Lamin A precursor induces barrier-to-autointegration factor nuclear localization. Cell Cycle. 2010; 9: 2600-2610.
65. Dominici S, Fiori V, Magnani M, Schena E, Capanni C, Camozzi D, D'Apice MR, Le Dour C, Auclair M, Caron M, Novelli G, Vigouroux C, Maraldi NM, et al. Different prelamin A forms accumulate in human fibroblasts: a study in experimental models and progeria. European journal of histochemistry: EJH. 2009; 53:43-52.
66. Mattioli E, Columbaro M, Capanni C, Santi S, Maraldi NM, D'Apice MR, Novelli G, Riccio M, Squarzoni S, Foisner R and Lattanzi G. Drugs affecting prelamin A processing: effects on heterochromatin organization. Experimental cell research. 2008;314:453-462.
67. Cenni V, Bavelloni A, Beretti F, Tagliavini F, Manzoli L, Lattanzi G, Maraldi NM, Cocco L and Marmiroli S. Ankrd2/ARPP is a novel Akt2 specific substrate and regulates myogenic differentiation upon cellular exposure to H(2)O(2). Molecular biology of the cell. 2011; 22:2946-2956.
68. Pozarowski P and Darzynkiewicz Z. Analysis of cell cycle by flow cytometry. Methods in molecular biology. 2004; 281:301-311.