Modulation of TGFbeta 2 levels by lamin A in U2-OS osteoblast-like cells: Understanding the osteolytic process triggered by altered lamins

Oncotarget

Volumn 6, Issue 10, 2015, Pages 7424-7437

  Evangelisti, Camilla ^a   Bernasconi, Pia ^b   Cavalcante, Paola ^b   Cappelletti, Cristina ^b   D'Apice, Maria Rosaria ^c   Sbraccia, Paolo ^d   Novelli, Giuseppe ^d   Prencipe, Sabino ^a   Lemma, Silvia ^e   Baldini, Nicola ^e   Avnet, Sofia ^e   Squarzoni, Stefano ^a   Martelli, Alberto M ^f   Lattanzi, Giovanna ^a  

^a CNR   (Italy)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c TOR VERGATA UNIVERSITY HOSPITAL   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

^e RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^f UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Akt signaling; Lamin A; Osteoclasts; RAD001; TGFbeta2

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; CATHEPSIN K; EVEROLIMUS; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LAMIN A; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MEVINOLIN; MITOGEN ACTIVATED PROTEIN KINASE 1; NEUTRALIZING ANTIBODY; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PROTEIN KINASE B; PROTEIN S6; RANTES; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; S6 KINASE; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; MTOR PROTEIN, HUMAN; PRELAMIN A; TARGET OF RAPAMYCIN KINASE;

ADULT; ARTICLE; BONE REMODELING; BONE TURNOVER; CASE REPORT; CELL DIFFERENTIATION; CHILD; CONTROLLED STUDY; CULTURE MEDIUM; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; GENE; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; LAMINOPATHY; LMNA GENE; MALE; MANDIBULOACRAL DYSPLASIA; MANDIBULOFACIAL DYSOSTOSIS; OSTEOBLAST; OSTEOLYSIS; OSTEOSARCOMA CELL LINE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; UPREGULATION; WESTERN BLOTTING; BIOSYNTHESIS; CYTOLOGY; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL DIFFERENTIATION; CELL LINE, TUMOR; EVEROLIMUS; HUMANS; LAMIN TYPE A; OSTEOBLASTS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA2;

EID: 84928387799     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3232     Document Type: Article

References (57)

1. Camozzi D, Capanni C, Cenni V, Mattioli E, Columbaro M, Squarzoni S, Lattanzi G. Diverse lamin-dependent mechanisms interact to control chromatin dynamics: Focus on laminopathies. Nucleus. 2014; 5:427-440.
2. Gonzalez JM, Navarro-Puche A, Casar B, Crespo P, Andres V. Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J Cell Biol. 2008; 183:653-666.
3. Tilgner K, Wojciechowicz K, Jahoda C, Hutchison C, Markiewicz E. Dynamic complexes of A-type lamins and emerin influence adipogenic capacity of the cell via nucleocytoplasmic distribution of beta-catenin. J Cell Sci. 2009; 122:401-413.
4. 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, Cocco L, Marmiroli S. Lamin A Ser404 is a nuclear target of Akt phosphorylation in C2C12 cells. J Proteome Res. 2008; 7:4727-4735.
5. Bertacchini J, Beretti F, Cenni V, Guida M, Gibellini F, Mediani L, Marin O, Maraldi NM, de Pol A, Lattanzi G, Cocco L, Marmiroli S. The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FASEB J. 2013; 27:2145-2155.
6. Maraldi NM, Capanni C, Cenni V, Fini M, Lattanzi G. Laminopathies and lamin-associated signaling pathways. J Cell Biochem. 2011; 112:979-992.
7. Qi YX, Jiang J, Jiang XH, Wang XD, Ji SY, Han Y, Long DK, Shen BR, Yan ZQ, Chien S, Jiang ZL. PDGF-BB and TGF-{beta}1 on cross-talk between endothelial and smooth muscle cells in vascular remodeling induced by low shear stress. Proc Natl Acad Sci U S A. 2011; 108:1908-1913.
8. Chatzifrangkeskou M, Bonne G, Muchir A. Nuclear envelope and striated muscle diseases. Curr Opin Cell Biol. 2014; 32C:1-6.
9. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J, 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.
10. Osorio FG, Barcena C, Soria-Valles C, Ramsay AJ, de Carlos F, Cobo J, Fueyo A, Freije JM, Lopez-Otin C. Nuclear lamina defects cause ATM-dependent NF-kappaB activation and link accelerated aging to a systemic inflammatory response. Genes Dev. 2012; 26:2311-2324.
11. 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, Lattanzi G. Osteoblasts from a mandibuloacral dysplasia patient induce human blood precursors to differentiate into active osteoclasts. Biochim Biophys Acta. 2011; 1812:711-718.
12. Bidault G, Garcia M, Vantyghem MC, Ducluzeau PH, Morichon R, Thiyagarajah K, Moritz S, Capeau J, Vigouroux C, Bereziat V. Lipodystrophy-linked LMNA p.R482W mutation induces clinical early atherosclerosis and in vitro endothelial dysfunction. Arterioscler Thromb Vasc Biol. 2013; 33:2162-2171.
13. Muchir A, Pavlidis P, Decostre V, Herron AJ, Arimura T, Bonne G, Worman HJ. Activation of MAPK pathways links LMNA mutations to cardiomyopathy in Emery-Dreifuss muscular dystrophy. J Clin Invest. 2007; 117:1282-1293.
14. Zhang Y, Yu H, Xu M, Han F, Tian C, Kim S, Fredman E, Zhang J, Benedict-Alderfer C, Zheng QY. Pathological features in the LmnaDhe/+ mutant mouse provide a novel model of human otitis media and laminopathies. Am J Pathol. 2012; 181:761-774.
15. Fox SW, Lovibond AC. Current insights into the role of transforming growth factor-beta in bone resorption. Mol Cell Endocrinol. 2005; 243:19-26.
16. Yang T, Grafe I, Bae Y, Chen S, Chen Y, Bertin TK, Jiang MM, Ambrose CG, Lee B. E-selectin ligand 1 regulates bone remodeling by limiting bioactive TGF-beta in the bone microenvironment. Proc Natl Acad Sci U S A. 2013; 110:7336-7341.
17. Dallas SL, Park-Snyder S, Miyazono K, Twardzik D, Mundy GR, Bonewald LF. Characterization and autoregulation of latent transforming growth factor beta (TGF beta) complexes in osteoblast-like cell lines. Production of a latent complex lacking the latent TGF beta-binding protein. J Biol Chem. 1994; 269:6815-6821.
18. Hering S, Isken E, Knabbe C, Janott J, Jost C, Pommer A, Muhr G, Schatz H, Pfeiffer AF. TGFbeta1 and TGFbeta2 mRNA and protein expression in human bone samples. Exp Clin Endocrinol Diabetes. 2001; 109:217-226.
19. Oreffo RO, Mundy GR, Seyedin SM, Bonewald LF. Activation of the bone-derived latent TGF beta complex by isolated osteoclasts. Biochem Biophys Res Commun. 1989; 158:817-823.
20. 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, Dallapiccola B, Merlini L, Bonne G. Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. Am J Hum Genet. 2002; 71:426-431.
21. Shen JJ, Brown CA, Lupski JR, Potocki L. Mandibuloacral dysplasia caused by homozygosity for the R527H mutation in lamin A/C. J Med Genet. 2003; 40:854-857.
22. Camozzi D, D'Apice MR, Schena E, Cenni V, Columbaro M, Capanni C, Maraldi NM, Squarzoni S, Ortolani M, Novelli G, Lattanzi G. Altered chromatin organization and SUN2 localization in mandibuloacral dysplasia are rescued by drug treatment. Histochem Cell Biol. 2012; 138:643-651.
23. Rivas D, Li W, Akter R, Henderson JE, Duque G. Accelerated features of age-related bone loss in zmpste24 metalloproteinase-deficient mice. J Gerontol A Biol Sci Med Sci. 2009; 64:1015-1024.
24. 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, Lopez-Otin C. Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat Med. 2008; 14:767-772.
25. 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, Novelli G. Alterations of nuclear envelope and chromatin organization in mandibuloacral dysplasia, a rare form of laminopathy. Physiol Genomics. 2005; 23:150-158.
26. Columbaro M, Capanni C, Mattioli E, Novelli G, Parnaik VK, Squarzoni S, Maraldi NM, Lattanzi G. Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell Mol Life Sci. 2005; 62:2669-2678.
27. 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, Lattanzi G. Prelamin A processing and functional effects in restrictive dermopathy. Cell Cycle. 2010; 9:4766-4768.
28. Lattanzi G. Prelamin A-mediated nuclear envelope dynamics in normal and laminopathic cells. Biochem Soc Trans. 2011; 39:1698-1704.
29. Zini N, Avnet S, Ghisu S, Maraldi NM, Squarzoni S, Baldini N, Lattanzi G. Effects of prelamin A processing inhibitors on the differentiation and activity of human osteoclasts. J Cell Biochem. 2008; 105:34-40.
30. Koulouvaris P, Ly K, Ivashkiv LB, Bostrom MP, Nestor BJ, Sculco TP, Purdue PE. Expression profiling reveals alternative macrophage activation and impaired osteogenesis in periprosthetic osteolysis. J Orthop Res. 2008; 26:106-116.
31. Liu Y, Drozdov I, Shroff R, Beltran LE, Shanahan CM. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ Res. 2013; 112:e99-109.
32. Zhang YE. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009; 19:128-139.
33. Cenni V, Capanni C, Mattioli E, Columbaro M, Wehnert M, Ortolani M, Fini M, Novelli G, Bertacchini J, Maraldi NM, Marmiroli S, D'Apice MR, Prencipe S, Squarzoni S, Lattanzi G. Rapamycin treatment of Mandibuloacral Dysplasia cells rescues localization of chromatin-associated proteins and cell cycle dynamics. Aging (Albany NY). 2014; 6:755-770.
34. Gordon LB, Cao K, Collins FS. Progeria: translational insights from cell biology. J Cell Biol. 2012; 199:9-13.
35. Sun W, Lee TS, Zhu M, Gu C, Wang Y, Zhu Y, Shyy JY. Statins activate AMP-activated protein kinase in vitro and in vivo. Circulation. 2006; 114:2655-2662.
36. Sylvius N, Bonne G, Straatman K, Reddy T, Gant TW, Shackleton S. MicroRNA expression profiling in patients with lamin A/C-associated muscular dystrophy. FASEB J. 2011; 25:3966-3978.
37. Marmiroli S, Bertacchini J, Beretti F, Cenni V, Guida M, De Pol A, Maraldi NM, Lattanzi G. A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward. J Cell Physiol. 2009; 220:553-561.
38. Martinet W, De Loof H, De Meyer GR. mTOR inhibition: a promising strategy for stabilization of atherosclerotic plaques. Atherosclerosis. 2014; 233:601-607.
39. Mattioli E, Columbaro M, Capanni C, Maraldi NM, Cenni V, Scotlandi K, Marino MT, Merlini L, Squarzoni S, Lattanzi G. Prelamin A-mediated recruitment of SUN1 to the nuclear envelope directs nuclear positioning in human muscle. Cell Death Differ. 2011; 18:1305-1315.
40. Favreau C, Delbarre E, Courvalin JC, Buendia B. Differentiation of C2C12 myoblasts expressing lamin A mutated at a site responsible for Emery-Dreifuss muscular dystrophy is improved by inhibition of the MEK-ERK pathway and stimulation of the PI3-kinase pathway. Exp Cell Res. 2008; 314:1392-1405.
41. Emerson LJ, Holt MR, Wheeler MA, Wehnert M, Parsons M, Ellis JA. Defects in cell spreading and ERK1/2 activation in fibroblasts with lamin A/C mutations. Biochim Biophys Acta. 2009; 1792:810-821.
42. Martinotti S, Mazzucco L, Balbo V, Patrone M, Mozzati M, Ranzato E, Burlando B. Platelet-rich plasma induces mixed osteogenic/osteoclastogenic phenotype in osteosarcoma SaOS-2 cells: role of TGF-beta. Curr Pharm Biotechnol. 2014; 15:120-126.
43. Mandelin J, Hukkanen M, Li TF, Korhonen M, Liljestrom M, Sillat T, Hanemaaijer R, Salo J, Santavirta S, Konttinen YT. Human osteoblasts produce cathepsin K. Bone. 2006; 38:769-777.
44. Morko J, Kiviranta R, Mulari MT, Ivaska KK, Vaananen HK, Vuorio E, Laitala-Leinonen T. Overexpression of cathepsin K accelerates the resorption cycle and osteoblast differentiation in vitro. Bone. 2009; 44:717-728.
45. Scaffidi P, Misteli T. Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol. 2008; 10:452-459.
46. Xu Q, Hou W, Zheng Y, Liu C, Gong Z, Lu C, Lai W, Maibach HI. Ultraviolet A-induced cathepsin K expression is mediated via MAPK/AP-1 pathway in human dermal fibroblasts. PLoS One. 2014; 9:e102732.
47. Pallotta R, Morgese G. Mandibuloacral dysplasia: a rare progeroid syndrome. Two brothers confirm autosomal recessive inheritance. Clin Genet. 1984; 26:133-138.
48. Venuraju SM, Yerramasu A, Corder R, Lahiri A. Osteoprotegerin as a predictor of coronary artery disease and cardiovascular mortality and morbidity. J Am Coll Cardiol. 2010; 55:2049-2061.
49. Narazaki R, Makimura M, Sanefuji M, Fukamachi S, Akiyoshi H, So H, Yamamura K, Doisaki S, Kojima S, Ihara K, Hara T, Ohga S. Bilateral stenosis of carotid siphon in Hutchinson-Gilford progeria syndrome. Brain Dev. 2013; 35:690-693.
50. Erlebacher A, Derynck R. Increased expression of TGFbeta 2 in osteoblasts results in an osteoporosis-like phenotype. J Cell Biol. 1996; 132:195-210.
51. Quinn JM, Itoh K, Udagawa N, Hausler K, Yasuda H, Shima N, Mizuno A, Higashio K, Takahashi N, Suda T, Martin TJ, Gillespie MT. Transforming growth factor beta affects osteoclast differentiation via direct and indirect actions. J Bone Miner Res. 2001; 16:1787-1794.
52. Hernandez-Vallejo SJ, Beaupere C, Larghero J, Capeau J, Lagathu C. HIV protease inhibitors induce senescence and alter osteoblastic potential of human bone marrow mesenchymal stem cells: beneficial effect of pravastatin. Aging Cell. 2013; 12:955-965.
53. 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, Franceschi C. Lamins are rapamycin targets that impact human longevity: a study in centenarians. J Cell Sci. 2014; 127:147-157.
54. Lin F, Morrison JM, Wu W, Worman HJ. MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factorbeta signaling. Hum Mol Genet. 2005; 14:437-445.
55. Bourgeois B, Gilquin B, Tellier-Lebegue C, Ostlund C, Wu W, Perez J, El Hage P, Lallemand F, Worman HJ, Zinn-Justin S. Inhibition of TGF-beta signaling at the nuclear envelope: characterization of interactions between MAN1, Smad2 and Smad3, and PPM1A. Sci Signal. 2013; 6:ra49.
56. Capanni C, Cenni V, Haraguchi T, Squarzoni S, Schuchner S, Ogris E, Novelli G, Maraldi N, Lattanzi G. Lamin A precursor induces barrier-to-autointegration factor nuclear localization. Cell Cycle. 2010; 9:2600-2610.
57. Capanni C, Squarzoni S, Cenni V, D'Apice MR, Gambineri A, Novelli G, Wehnert M, Pasquali R, Maraldi NM, Lattanzi G. Familial partial lipodystrophy, mandibuloacral dysplasia and restrictive dermopathy feature barrier-to-autointegration factor (BAF) nuclear redistribution. Cell Cycle. 2012; 11:3568-3577.