Anti-TNF-α treatment modulates SASP and SASP-related microRNAs in endothelial cells and in circulating angiogenic cells

Oncotarget

Volumn 7, Issue 11, 2016, Pages 11945-11958

  Prattichizzo, Francesco ^a,b,e   Giuliani, Angelica ^a   Recchioni, Rina ^c   Bonafè, Massimiliano ^d   Marcheselli, Fiorella ^c   De Carolis, Sabrina ^d   Campanati, Anna ^a   Giuliodori, Katia ^a   Rippo, Maria Rita ^a   Brugè, Francesca ^a   Tiano, Luca ^a   Micucci, Carla ^a   Ceriello, Antonio ^b,e   Offidani, Annamaria ^a   Procopio, Antonio Domenico ^a,c   Olivieri, Fabiola ^a,c  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INRCA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

^e IRCCS MULTIMEDICA   (Italy)

Author keywords

Gerotarget; HUVEC; miR 126 3p; miR 146 5p; Replicative senescence; SASP

Indexed keywords

ADALIMUMAB; BETA GALACTOSIDASE; CELL MARKER; CYCLIN DEPENDENT KINASE INHIBITOR 2A; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 6; MICRORNA; MICRORNA 126 3P; MICRORNA 146A 5P; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN SPRED1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IL6 PROTEIN, HUMAN; MIRN126 MICRORNA, HUMAN; MIRN146 MICRORNA, HUMAN; TUMOR NECROSIS FACTOR;

ADULT; ARTICLE; CELL AGING; CELL AGING, CELL DEGENERATION AND CELL SURVIVAL; CELL MIGRATION; CELL MOTILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; EPIGENETICS; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; MCF 7 CELL LINE; MIDDLE AGED; SENESCENCE ASSOCIATED SECRETORY PHENOTYPE; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL PROLIFERATION; CONDITIONED MEDIUM; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; PHARMACOLOGY; PHYSIOLOGY; PSORIASIS; VASCULAR ENDOTHELIUM;

ADALIMUMAB; CELL PROLIFERATION; CELLS, CULTURED; CELLULAR SENESCENCE; CULTURE MEDIA, CONDITIONED; ENDOTHELIUM, VASCULAR; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-6; MALE; MCF-7 CELLS; MICRORNAS; MIDDLE AGED; PSORIASIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84962808708     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.7858     Document Type: Article

References (55)

1. Tchkonia T, Zhu Y, van Deursen J, Campisi J, Kirkland JL. Cellular senescence and the senescent secretory phenotype: therapeutic opportunities. J Clin Invest. 2013; 123:966-72.
2. Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E, De Benedictis G. Inflamm-aging: an evolutionary perspective on immunosenescence. Ann N Y Acad Sci. 2000; 908:244-54.
3. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol. 2007; 8:729-40.
4. Freund A, Orjalo AV, Desprez PY, Campisi J. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med. 2010; 16:238-46.
5. Childs BG, Durik M, Baker DJ, van Deursen JM. Cellular senescence in aging and age-related disease: from mechanisms to therapy. Nat Med. 2015 Dec;21:1424-35.
6. Newgard CB, Sharpless NE. Coming of age: molecular drivers of aging and therapeutic opportunities. J Clin Invest. 2013 Mar;123(3):946-50. doi: 10.1172/JCI68833
7. Salminen A, Kauppinen A, Kaarniranta K. Emerging role of NF-κB signaling in the induction of senescence-associated secretory phenotype (SASP). Cell Signal. 2012; 24:835-45.
8. Jurk D, Wilson C, Passos JF, Oakley F, Correia-Melo C, Greaves L, Saretzki G, Fox C, Lawless C, Anderson R, Hewitt G, Pender SL, Fullard N, et al. Chronic inflammation induces telomere dysfunction and accelerates ageing in mice. Nat Commun. 2014; 2:4172.
9. Acosta JC, Banito A, Wuestefeld T, Georgilis A, Janich P, Morton JP, Athineos D, Kang TW, Lasitschka F, Andrulis M, Pascual G, Morris KJ, Khan S, et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol. 2013; 15:978-90.
10. Zhang G, Li J, Purkayastha S, Tang Y, Zhang H, Yin Y, Li B, Liu G, Cai D. Hypothalamic programming of systemic ageing involving IKK-β, NF-κB and GnRH. Nature. 2013; 497:211-6.
11. Youm YH, Grant RW, McCabe LR, Albarado DC, Nguyen KY, Ravussin A, Pistell P, Newman S, Carter R, Laque A, Münzberg H, Rosen CJ, Ingram DK, et al. Canonical Nlrp3 inflammasome links systemic low-grade inflammation to functional decline in aging. Cell Metab. 2013; 18:519-32.
12. Ferrand M, Kirsh O, Griveau A, Vindrieux D, Martin N, Defossez PA, Bernard D. Screening of a kinase library reveals novel pro-senescence kinases and their common NF-κB-dependent transcriptional program. Aging (Albany NY). 2015; 7:986-1003.
13. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature. 2011; 479:232-6.
14. Waaijer ME, Parish WE, Strongitharm BH, van Heemst D, Slagboom PE, de Craen AJ, Sedivy JM, Westendorp RG, Gunn DA, Maier AB. The number of p16INK4a positive cells in human skin reflects biological age. Aging Cell. 2012; 11:722-5.
15. Olivieri F, Lazzarini R, Babini L, Prattichizzo F, Rippo MR, Tiano L, Di Nuzzo S, Graciotti L, Festa R, Brugè F, Orlando P, Silvestri S, Capri M, et al. Anti-inflammatory effect of ubiquinol-10 on young and senescent endothelial cells via miR-146a modulation. Free Radic Biol Med. 2013; 63:410-20.
16. Kozieł R, Ruckenstuhl C, Albertini E, Neuhaus M, Netzberger C, Bust M, Madeo F, Wiesner RJ, Jansen-Dürr P. Methionine restriction slows down senescence in human diploid fibroblasts. Aging Cell. 2014; 13:1038-48.
17. Laberge RM, Zhou L, Sarantos MR, Rodier F, Freund A, de Keizer PL, Liu S, Demaria M, Cong YS, Kapahi P, Desprez PY, Hughes RE, Campisi J. Glucocorticoids suppress selected components of the senescence-associated secretory phenotype. Aging Cell. 2012; 11:569-78.
18. Freund A, Patil CK, Campisi J. p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J. 2011; 30:1536-48.
19. Wu Z, Yu Y, Liu C, Xiong Y, Montani JP, Yang Z, Ming XF. Role of p38 mitogen-activated protein kinase in vascular endothelial aging: interaction with Arginase-II and S6K1 signaling pathway. Aging (Albany NY). 2015; 7:70-81.
20. Lim H, Park H, Kim HP. Effects of flavonoids on senescence-associated secretory phenotype formation from bleomycin-induced senescence in BJ fibroblasts. Biochem Pharmacol. 2015; pii: S0006-2952 00329-9.
21. Zhu Y, Tchkonia T, Pirtskhalava T, Gower AC, Ding H, Giorgadze N, Palmer AK, Ikeno Y, Hubbard GB, Lenburg M, O'Hara SP, LaRusso NF, Miller JD, et al. The Achilles' heel of senescent cells: from transcriptome to senolytic drugs. Aging Cell. 2015; 14:644-58.
22. Hubackova S, Krejcikova K, Bartek J, Hodny Z. IL1- and TGFβ-Nox4 signaling, oxidative stress and DNA damage response are shared features of replicative, oncogene-induced, and drug-induced paracrine 'bystander senescence'. Aging (Albany NY). 2012; 4:932-51.
23. Nelson DM, McBryan T, Jeyapalan JC, Sedivy JM, Adams PD. A comparison of oncogene-induced senescence and replicative senescence: implications for tumor suppression and aging. Age (Dordr). 2014; 36:9637.
24. Purcell M, Kruger A, Tainsky MA. Gene expression profiling of replicative and induced senescence. Cell Cycle. 2014; 13, 3927-37.
25. Donato AJ, Black AD, Jablonski KL, Gano LB, Seals DR. Aging is associated with greater nuclear NF kappa B, reduced I kappa B-α, and increased expression of proinflammatory cytokines in vascular endothelial cells of healthy humans. Aging Cell. 2008; 7:805-12.
26. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell. 2008; 133:1019-31.
27. Zhang Y, Herbert BS, Rajashekhar G, Ingram DA, Yoder MC, Clauss M, Rehman J. Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factor-alpha via the p38 mitogen-activated protein kinase pathway. FASEB J. 2009; 23:1358-65.
28. Carracedo J, Buendía P, Merino A, Madueño JA, Peralbo E, Ortiz A, Martín-Malo A, Aljama P, Rodríguez M, Ramírez R. Klotho modulates the stress response in human senescent endothelial cells. Mech Ageing Dev. 2012; 133:647-54.
29. Zhang H, Park Y, Wu J, Chen Xp, Lee S, Yang J, Dellsperger KC, Zhang C. Role of TNF-alpha in vascular dysfunction. Clin Sci (Lond). 2009; 116:219-30.
30. Brezinski EA, Follansbee MR, Armstrong EJ, Armstrong AW. Endothelial dysfunction and the effects of TNF inhibitors on the endothelium in psoriasis and psoriatic arthritis: a systematic review. Curr Pharm Des. 2014; 20:513-28.
31. Avgerinou G, Tousoulis D, Siasos G, Oikonomou E, Maniatis K, Papageorgiou N, Paraskevopoulos T, Miliou A, Koumaki D, Latsios G, Therianiou A, Trikas A, Kampoli AM, et al. Anti-tumor necrosis factor α treatment with adalimumab improves significantly endothelial function and decreases inflammatory process in patients with chronic psoriasis. Int J Cardiol. 2011; 151:382-3.
32. Campanati A, Moroncini G, Ganzetti G, Pozniak KN, Goteri G, Giuliano A, Martina E, Liberati G, Ricotti F, Gabrielli A, Offidani A. adalimumab modulates angiogenesis in psoriatic skin eur j inflam. 2013;11:489-498
33. De Simone C, Amerio P, Amoruso G, Bardazzi F, Campanati A, Conti A, Gisondi P, Gualdi G, Guarneri C, Leoni L, Loconsole F, Mazzotta A, Musumeci ML, Piaserico S, Potenza C, Prestinari F. Immunogenicity of anti-TNFα therapy in psoriasis: a clinical issue? Expert Opin Biol Ther. 2013;13:1673-82.
34. Campanati A, Goteri G, Simonetti O, Ganzetti G, Giuliodori K, Giuliano A, Sabato S, Stramazzotti D, Gulini E, Dusi D, De Blasio S, Fabris G, Offidani A. Angiogenesis in psoriatic skin and its modifications after administration of etanercept: videocapillaroscopic, histological and immunohistochemical evaluation. Int J Immunopathol Pharmacol. 2009;22:371-7.
35. Inui M, Martello G, Piccolo S. MicroRNA control of signal transduction. Nat Rev Mol Cell Biol. 2010; 11:252-63.
36. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A. 1995; 92:9363-7.
37. Veitonmäki N, Fuxe J, Hultdin M, Roos G, Pettersson RF, Cao Y. Immortalization of bovine capillary endothelial cells by hTERT alone involves inactivation of endogenous p16INK4A/pRb. FASEB J. 2003; 17:764-6.
38. Kortlever RM, Higgins PJ, Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat Cell Biol. 2006; 8:877-84.
39. Matsushita H, Chang E, Glassford AJ, Cooke JP, Chiu CP, Tsao PS. eNOS activity is reduced in senescent human endothelial cells: Preservation by hTERT immortalization. Circ Res. 2001; 89:793-8.
40. den Broeder A, van de Putte L, Rau R, Schattenkirchner M, Van Riel P, Sander O, Binder C, Fenner H, Bankmann Y, Velagapudi R, Kempeni J, Kupper H. A single dose, placebo controlled study of the fully human anti-tumor necrosis factor-alpha antibody adalimumab (D2E7) in patients with rheumatoid arthritis. J Rheumatol. 2002; 29:2288-98.
41. Oglesby IK, Bray IM, Chotirmall SH, Stallings RL, O'Neill SJ, McElvaney NG, Greene CM. miR-126 is downregulated in cystic fibrosis airway epithelial cells and regulates TOM1 expression. J Immunol. 2010; 184:1702-9.
42. Zacarias-Fluck MF, Morancho B, Vicario R, Luque Garcia A, Escorihuela M, Villanueva J, Rubio IT, Arribas J. Effect of cellular senescence on the growth of HER2-positive breast cancers. J Natl Cancer Inst. 2015; 107pii: djv020.
43. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB, Chieco P, Bonafè M. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest. 2015; 117:3988-4002.
44. Papi A, Storci G, Guarnieri T, De Carolis S, Bertoni S, Avenia N, Sanguinetti A, Sidoni A, Santini D, Ceccarelli C, Taffurelli M, Orlandi M, Bonafé M. Peroxisome proliferator activated receptor-α/hypoxia inducible factor-1α interplay sustains carbonic anhydrase IX and apoliprotein E expression in breast cancer stem cells. PLoS One. 2013;8:e54968.
45. Papi A, De Carolis S, Bertoni S, Storci G, Sceberras V, Santini D, Ceccarelli C, Taffurelli M, Orlandi M, Bonafé M. PPARγ and RXR ligands disrupt the inflammatory cross-talk in the hypoxic breast cancer stem cells niche. J Cell Physiol. 2014;229:1595-606.
46. Henseler T, Christophers E. Disease concomitance in psoriasis. J Am Acad Dermatol. 1995; 32:982-6.
47. Hugh J, Van Voorhees AS, Nijhawan RI, Bagel J, Lebwohl M, Blauvelt A, Hsu S, Weinberg JM. From the Medical Board of the National Psoriasis Foundation: The risk of cardiovascular disease in individuals with psoriasis and the potential impact of current therapies. J Am Acad Dermatol. 2014; 70:168-77.
48. McCarthy DA, Clark RR, Bartling TR, Trebak M, Melendez JA. Redox control of the senescence regulator interleukin-1α and the secretory phenotype. J Biol Chem. 2013; 288:32149-59.
49. Maggio M, Guralnik JM, Longo DL, Ferrucci L. Interleukin-6 in aging and chronic disease: a magnificent pathway. J Gerontol A Biol Sci Med Sci. 2006; 61:575-84.
50. Steyers CM 3rd, Miller FJ Jr. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci. 2014; 15:11324-49.
51. Balistreri CR, Candore G, Accardi G, Colonna-Romano G, Lio D. NF-κB pathway activators as potential ageing biomarkers: targets for new therapeutic strategies. Immun Ageing. 2013;10:24.
52. Stepanova M, Rodriguez E, Birerdinc A, Baranova A (2015) Age-independent rise of inflammatory scores may contribute to accelerated aging in multi-morbidity. Oncotarget. 2015; 6: 1414-21. doi: 10.18632/oncotarget.2725.
53. Longo VD, Antebi A, Bartke A, Barzilai N, Brown-Borg HM, Caruso C, Curiel TJ, de Cabo R, Franceschi C, Gems D, Ingram DK, Johnson TE, Kennedy BK, et al. Interventions to slow aging in humans: are we ready? Aging Cell. 2015; 14: 497-510.
54. Prattichizzo F, Bonafe M, Ceka A, Giuliani A, Rippo MR, Re M, Antonicelli R, Procopio AD, Olivieri F. Endothelial cell senescence and inflammaging: microRNAs as biomarkers and innovative therapeutic tools. Curr Drug Targets. 2015; [Epub ahead of print].
55. Olivieri F, Bonafè M, Spazzafumo L, Gobbi M, Prattichizzo F, Recchioni R, Marcheselli F, La Sala L, Galeazzi R, Rippo MR, Fulgenzi G, Angelini S, Lazzarini R, et al. Age- and glycemia-related miR-126-3p levels in plasma and endothelial cells. Aging (Albany NY). 2014; 6:771-87.