Enteric-delivered rapamycin enhances resistance of aged mice to pneumococcal pneumonia through reduced cellular senescence

Experimental Gerontology

Volumn 47, Issue 12, 2012, Pages 958-965

  Hinojosa, Cecilia A ^a   Mgbemena, Victoria ^a   Van Roekel, Sabrina ^b   Austad, Steven N ^a,c   Miller, Richard A ^b   Bose, Santanu ^a   Orihuela, Carlos J ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Aging; Cellular senescence; Pneumonia; Rapamycin; Streptococcus pneumoniae

Indexed keywords

CYTOKERATIN 10; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; LAMININ RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P21; RAPAMYCIN; RETINOBLASTOMA PROTEIN; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL AGING; CONTROLLED STUDY; DISEASE RESISTANCE; DISEASE SEVERITY; DRUG EFFECT; FEMALE; IMMUNOBLOTTING; INFECTION SENSITIVITY; LUNG HOMOGENATE; LUNG INJURY; MALE; MONOTHERAPY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; PROTEIN EXPRESSION; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL AGING; CYTOKINES; DISEASE SUSCEPTIBILITY; DRUG EVALUATION, PRECLINICAL; FEMALE; LUNG; MALE; MICE; MICE, INBRED C57BL; PNEUMONIA, PNEUMOCOCCAL; RECEPTORS, IMMUNOLOGIC; SIROLIMUS; STREPTOCOCCUS PNEUMONIAE; TABLETS, ENTERIC-COATED;

BACTERIA (MICROORGANISMS); MUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84868302065     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2012.08.013     Document Type: Article

References (45)

1. Albert S., Serova M., Dreyer C., Sablin M.P., Faivre S., Raymond E. New inhibitors of the mammalian target of rapamycin signaling pathway for cancer. Expert Opin. Investig. Drugs 2010, 19:919-930.
2. Araki K., Turner A.P., Shaffer V.O., Gangappa S., Keller S.A., Bachmann M.F., Larsen C.P., Ahmed R. mTOR regulates memory CD8 T-cell differentiation. Nature 2009, 460:108-112.
3. Avadhanula V., Rodriguez C.A., Ulett G.C., Bakaletz L.O., Adderson E.E. Nontypeable Haemophilus influenzae adheres to intercellular adhesion molecule 1 (ICAM-1) on respiratory epithelial cells and upregulates ICAM-1 expression. Infect. Immun. 2006, 74:830-838.
4. Barbier M., Oliver A., Rao J., Hanna S.L., Goldberg J.B., Alberti S. Novel phosphorylcholine-containing protein of Pseudomonas aeruginosa chronic infection isolates interacts with airway epithelial cells. J. Infect. Dis. 2008, 197:465-473.
5. Battaglia M., Stabilini A., Roncarolo M.G. Rapamycin selectively expands CD4+CD25+FoxP3+ regulatory T cells. Blood 2005, 105:4743-4748.
6. Caccamo A., Majumder S., Deng J.J., Bai Y., Thornton F.B., Oddo S. Rapamycin rescues TDP-43 mislocalization and the associated low molecular mass neurofilament instability. J. Biol. Chem. 2009, 284:27416-27424.
7. Caccamo A., Majumder S., Richardson A., Strong R., Oddo S. Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: effects on cognitive impairments. J. Biol. Chem. 2010, 285:13107-13120.
8. Campisi J., d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 2007, 8:729-740.
9. Chen C., Liu Y., Zheng P. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci. Signal. 2009, 2:ra75.
10. Child E.S., Mann D.J. The intricacies of p21 phosphorylation: protein/protein interactions, subcellular localization and stability. Cell Cycle 2006, 5:1313-1319.
11. Conners R., Hill D.J., Borodina E., Agnew C., Daniell S.J., Burton N.M., Sessions R.B., Clarke A.R., Catto L.E., Lammie D., Wess T., Brady R.L., Virji M. The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled-coil. EMBO J. 2008, 27:1779-1789.
12. Cundell D.R., Gerard N.P., Gerard C., Idanpaan-Heikkila I., Tuomanen E.I. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature 1995, 377:435-438.
13. D'Alessio F.R., Tsushima K., Aggarwal N.R., West E.E., Willett M.H., Britos M.F., Pipeling M.R., Brower R.G., Tuder R.M., McDyer J.F., King L.S. CD4+CD25+Foxp3+ Tregs resolve experimental lung injury in mice and are present in humans with acute lung injury. J. Clin. Invest. 2009, 119:2898-2913.
14. Demidenko Z.N., Blagosklonny M.V. Growth stimulation leads to cellular senescence when the cell cycle is blocked. Cell Cycle 2008, 7:3355-3361.
15. Demidenko Z.N., Zubova S.G., Bukreeva E.I., Pospelov V.A., Pospelova T.V., Blagosklonny M.V. Rapamycin decelerates cellular senescence. Cell Cycle 2009, 8:1888-1895.
16. Fielhaber J.A., Carroll S.F., Dydensborg A.B., Shourian M., Triantafillopoulos A., Harel S., Hussain S.N., Bouchard M., Qureshi S.T., Kristof A.S. Inhibition of mammalian target of rapamycin augments lipopolysaccharide-induced lung injury and apoptosis. J. Immunol. 2012, 188:4535-4542.
17. Finckenberg P., Mervaala E. Novel regulators and drug targets of cardiac hypertrophy. J. Hypertens. 2010, 28(Suppl. 1):S33-S38.
18. Groth C.G., Backman L., Morales J.M., Calne R., Kreis H., Lang P., Touraine J.L., Claesson K., Campistol J.M., Durand D., Wramner L., Brattstrom C., Charpentier B. Sirolimus (rapamycin)-based therapy in human renal transplantation: similar efficacy and different toxicity compared with cyclosporine. Sirolimus European Renal Transplant Study Group. Transplantation 1999, 67:1036-1042.
19. Hackstein H., Taner T., Zahorchak A.F., Morelli A.E., Logar A.J., Gessner A., Thomson A.W. Rapamycin inhibits IL-4 - induced dendritic cell maturation in vitro and dendritic cell mobilization and function in vivo. Blood 2003, 101:4457-4463.
20. Harrison D.E., Strong R., Sharp Z.D., Nelson J.F., Astle C.M., Flurkey K., Nadon N.L., Wilkinson J.E., Frenkel K., Carter C.S., Pahor M., Javors M.A., Fernandez E., Miller R.A. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 2009, 460:392-395.
21. Hinojosa E., Boyd A.R., Orihuela C.J. Age-associated inflammation and toll-like receptor dysfunction prime the lungs for pneumococcal pneumonia. J. Infect. Dis. 2009, 200:546-554.
22. Hughes K.J., Kennedy B.K. Cell biology. Rapamycin paradox resolved. Science 2012, 335:1578-1579.
23. Husain S., Alexander B.D., Munoz P., Avery R.K., Houston S., Pruett T., Jacobs R., Dominguez E.A., Tollemar J.G., Baumgarten K., Yu C.M., Wagener M.M., Linden P., Kusne S., Singh N. Opportunistic mycelial fungal infections in organ transplant recipients: emerging importance of non-Aspergillus mycelial fungi. Clin. Infect. Dis. 2003, 37:221-229.
24. Johansson N., Kalin M., Tiveljung-Lindell A., Giske C.G., Hedlund J. Etiology of community-acquired pneumonia: increased microbiological yield with new diagnostic methods. Clin. Infect. Dis. 2010, 50:202-209.
25. Kreiling J.A., Tamamori-Adachi M., Sexton A.N., Jeyapalan J.C., Munoz-Najar U., Peterson A.L., Manivannan J., Rogers E.S., Pchelintsev N.A., Adams P.D., Sedivy J.M. Age-associated increase in heterochromatic marks in murine and primate tissues. Aging Cell 2011, 10:292-304.
26. Leontieva O.V., Blagosklonny M.V. DNA damaging agents and p53 do not cause senescence in quiescent cells, while consecutive re-activation of mTOR is associated with conversion to senescence. Aging (Albany NY) 2010, 2:924-935.
27. Lexau C.A., Lynfield R., Danila R., Pilishvili T., Facklam R., Farley M.M., Harrison L.H., Schaffner W., Reingold A., Bennett N.M., Hadler J., Cieslak P.R., Whitney C.G. Changing epidemiology of invasive pneumococcal disease among older adults in the era of pediatric pneumococcal conjugate vaccine. JAMA 2005, 294:2043-2051.
28. Lopez A.D., Mathers C.D., Ezzati M., Jamison D.T., Murray C.J. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 2006, 367:1747-1757.
29. Manning A.L., Dyson N.J. pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol. 2011, 21:433-441.
30. Miller R.A., Harrison D.E., Astle C.M., Baur J.A., Boyd A.R., de Cabo R., Fernandez E., Flurkey K., Javors M.A., Nelson J.F., Orihuela C.J., Pletcher S., Sharp Z.D., Sinclair D., Starnes J.W., Wilkinson J.E., Nadon N.L., Strong R. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J. Gerontol. A Biol. Sci. Med. Sci. 2011, 66:191-201.
31. Minino A.M., Heron M.P., Smith B.L. Deaths: preliminary data for 2004. Natl. Vital Stat. Rep. 2006, 54:1-49.
32. O'Brien L.M., Walsh E.J., Massey R.C., Peacock S.J., Foster T.J. Staphylococcus aureus clumping factor B (ClfB) promotes adherence to human type I cytokeratin 10: implications for nasal colonization. Cell. Microbiol. 2002, 4:759-770.
33. Orihuela C.J., Tuomanen E. Streptococcus pneumoniae: invasion and inflammation. Gram-positive Pathogens 2006, ASM Press, Washington D.C. V.A. Fischetti, R.P. Novick, J.J. Ferretti, D.A. Portnoy, J.I. Rood (Eds.).
34. Orihuela C.J., Gao G., Francis K.P., Yu J., Tuomanen E.I. Tissue-specific contributions of pneumococcal virulence factors to pathogenesis. J. Infect. Dis. 2004, 190:1661-1669.
35. Orihuela C.J., Mahdavi J., Thornton J., Mann B., Wooldridge K.G., Abouseada N., Oldfield N.J., Self T., Ala'Aldeen D.A., Tuomanen E.I. Laminin receptor initiates bacterial contact with the blood brain barrier in experimental meningitis models. J. Clin. Invest. 2009, 119:1638-1646.
36. Shivshankar P., Sanchez C., Rose L.F., Orihuela C.J. The Streptococcus pneumoniae adhesin PsrP binds to Keratin 10 on lung cells. Mol. Microbiol. 2009, 73:663-679.
37. Shivshankar P., Boyd A.R., Le Saux C.J., Yeh I.T., Orihuela C.J. Cellular senescence increases expression of bacterial ligands in the lungs and is positively correlated with increased susceptibility to pneumococcal pneumonia. Aging Cell 2011, 10:798-806.
38. Spilman P., Podlutskaya N., Hart M.J., Debnath J., Gorostiza O., Bredesen D., Richardson A., Strong R., Galvan V. Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS One 2010, 5:e9979.
39. Sun Y., Li C., Shu Y., Ju X., Zou Z., Wang H., Rao S., Guo F., Liu H., Nan W., Zhao Y., Yan Y., Tang J., Zhao C., Yang P., Liu K., Wang S., Lu H., Li X., Tan L., Gao R., Song J., Gao X., Tian X., Qin Y., Xu K.F., Li D., Jin N., Jiang C. Inhibition of autophagy ameliorates acute lung injury caused by avian influenza A H5N1 infection. Sci. Signal. 2012, 5:ra16.
40. Swords W.E., Buscher B.A., Ver Steeg Ii K., Preston A., Nichols W.A., Weiser J.N., Gibson B.W., Apicella M.A. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 2000, 37:13-27.
41. Tettelin H., Nelson K.E., Paulsen I.T., Eisen J.A., Read T.D., Peterson S., Heidelberg J., DeBoy R.T., Haft D.H., Dodson R.J., Durkin A.S., Gwinn M., Kolonay J.F., Nelson W.C., Peterson J.D., Umayam L.A., White O., Salzberg S.L., Lewis M.R., Radune D., Holtzapple E., Khouri H., Wolf A.M., Utterback T.R., Hansen C.L., McDonald L.A., Feldblyum T.V., Angiuoli S., Dickinson T., Hickey E.K., Holt I.E., Loftus B.J., Yang F., Smith H.O., Venter J.C., Dougherty B.A., Morrison D.A., Hollingshead S.K., Fraser C.M. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 2001, 293:498-506.
42. Tirado O.M., Mateo-Lozano S., Notario V. Rapamycin induces apoptosis of JN-DSRCT-1 cells by increasing the Bax:Bcl-xL ratio through concurrent mechanisms dependent and independent of its mTOR inhibitory activity. Oncogene 2005, 24:3348-3357.
43. Webster A.C., Lee V.W., Chapman J.R., Craig J.C. Target of rapamycin inhibitors (sirolimus and everolimus) for primary immunosuppression of kidney transplant recipients: a systematic review and meta-analysis of randomized trials. Transplantation 2006, 81:1234-1248.
44. Yan Y., Silvennoinen-Kassinen S., Leinonen M., Saikku P. Rapamycin can inhibit the development of Chlamydia pneumoniae, which might partly contribute to the prevention of in-stent restenosis. Cardiovasc. Drugs Ther. 2010, 24:189-195.
45. Zhang Q., Raoof M., Chen Y., Sumi Y., Sursal T., Junger W., Brohi K., Itagaki K., Hauser C.J. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010, 464:104-107.