A senescence secretory switch mediated by PI3K/AKT/mTOR activation controls chemoprotective endothelial secretory responses

Genes and Development

Volumn 30, Issue 16, 2016, Pages 1811-1821

  Bent, Eric H ^a,b   Gilbert, Luke A ^a,b   Hemann, Michael T ^a,b  

^a David H Koch Institute for Integrative Cancer Research   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Chemoresistance; Endothelial cell; Paracrine; SASP; Senescence; Tumor microenvironment

Indexed keywords

DOXORUBICIN; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; ANTINEOPLASTIC AGENT; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER RESISTANCE; CELL AGING; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SECRETORY PATHWAY; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL AGING; CELL LINE; CELLS, CULTURED; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; ENDOTHELIAL CELLS; ENZYME ACTIVATION; HUMANS; INTERLEUKIN-6; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; TOR SERINE-THREONINE KINASES; TUMOR MICROENVIRONMENT;

EID: 84986917873     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.284851.116     Document Type: Article

References (55)

1. Acosta JC, O’Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, et al. 2008.Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133: 1006-1018.
2. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S, Palmiter RD, Brinster RL. 1985. The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538.
3. Baker DJ, Wijshake T, Tchkonia T, LeBrasseur NK, Childs BG, van de Sluis B, Kirkland JL, van Deursen JM. 2011. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 479: 232-236.
4. Baker DJ, Childs BG, Durik M, Wijers ME, Sieben CJ, Zhong J, Saltness RA, Jeganathan KB, Verzosa GC, Pezeshki A, et al. 2016. Naturally occurring p16(Ink4a)-positive cells shorten healthy lifespan. Nature 530: 184-189.
5. Butler JM, Kobayashi H, Rafii S. 2010. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer 10: 138-146.
6. Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, Sevillano M, Palomo-Ponce S, Tauriello DV, Byrom D, et al. 2015. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet 47: 320-329.
7. Campisi J. 2013. Aging, cellular senescence, and cancer. Annu Rev Physiol 75: 685-705.
8. Canino C, Mori F, Cambria A, Diamantini A, Germoni S, Alessandrini G, Borsellino G, Galati R, Battistini L, Blandino R, et al. 2012. SASP mediates chemoresistance and tumor-initiating-activity of mesothelioma cells. Oncogene 31: 3148-3163.
9. Cao Z, Ding BS, Guo P, Lee SB, Butler JM, Casey SC, Simons M, Tam W, Felsher DW, Shido K, et al. 2014. Angiocrine factors deployed by tumor vascular niche induce B cell lymphoma invasiveness and chemoresistance. Cancer cell 25:350-365.
10. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, Premsrirut P, Luo W, Chicas A, Lee CS, et al. 2011. Control of the senescence-associated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev 25: 2125-2136.
11. Coppe JP, Patil CK, Rodier F, Sun Y, Munoz DP, Goldstein J, Nelson PS, Desprez PY, Campisi J. 2008. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6: 2853-2868.
12. Coppe JP, Desprez PY, Krtolica A, Campisi J. 2010. The senescence-associated secretory phenotype: the dark side of tumor suppression. Annu Rev Pathol 5: 99-118.
13. Cuenda A, Rousseau S. 2007. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim Biophys Acta 1773: 1358-1375.
14. Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, Mittal V, Kobayashi H, Shido K, Lyden D, et al. 2010. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 468: 310-315.
15. Ding L, Saunders TL, Enikolopov G, Morrison SJ. 2012. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481: 457-462.
16. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. 1999. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13: 2658-2669.
17. Fan Y, Potdar AA, Gong Y, Eswarappa SM, Donnola S, Lathia JD, Hambardzumyan D, Rich JN, Fox PL. 2014. Profilin-1 phosphorylation directs angiocrine expression and glioblastoma progression through HIF-1α accumulation. Nat Cell Biol 16: 445-456.
18. Gilbert LA, Hemann MT. 2010. DNA damage-mediated induction of a chemoresistant niche. Cell 143: 355-366.
19. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144: 646-674.
20. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, et al. 2009. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-395.
21. Herranz N, Gallage S, Mellone M, Wuestefeld T, Klotz S, Hanley CJ, Raguz S, Acosta JC, Innes AJ, Banito A, et al. 2015. mTOR regulates MAPKAPK2 translation to control the senescenceassociated secretory phenotype. Nat Cell Biol 17: 1205-1217.
22. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, et al. 2011. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 479: 547-551.
23. Karin M, Clevers H. 2016. Reparative inflammation takes charge of tissue regeneration. Nature 529: 307-315.
24. Kim JJ, Tannock IF. 2005. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5: 516-525.
25. Klemm F, Joyce JA. 2015. Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol 25: 198-213.
26. Krizhanovsky V, Yon M, Dickins RA, Hearn S, Simon J, Miething C, Yee H, Zender L, Lowe SW. 2008. Senescence of activated stellate cells limits liver fibrosis. Cell 134: 657-667.
27. Kuilman T, Michaloglou C, Vredeveld LC, Douma S, van Doorn R, Desmet CJ, Aarden LA, Mooi WJ, Peeper DS. 2008. Oncogene-induced senescence relayed by an interleukin-dependent inflammatory network. Cell 133: 1019-1031.
28. Laberge RM, Sun Y, Orjalo AV, Patil CK, Freund A, Zhou L, Curran SC, Davalos AR, Wilson-Edell KA, Liu S, et al. 2015. MTOR regulates the pro-tumorigenic senescence-associated secretory phenotype by promoting IL1A translation. Nat Cell Biol 17: 1049-1061.
29. Lenz G, Wright G, Dave SS, Xiao W, Powell J, Zhao H, Xu W, Tan B, Goldschmidt N, Iqbal J, et al. 2008. Stromal gene signatures in large-B-cell lymphomas. N Engl J Med 359: 2313-2323.
30. Longley DB, Johnston PG. 2005. Molecular mechanisms of drug resistance. J Pathol 205: 275-292.
31. Meads MB, Gatenby RA, Dalton WS. 2009. Environment-mediated drug resistance: a major contributor to minimal residual disease. Nat Rev Cancer 9: 665-674.
32. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I. 2002. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation 105: 1541-1544.
33. Mittal M, Siddiqui MR, Tran K, Reddy SP, Malik AB. 2014. Reactive oxygen species in inflammation and tissue injury. Antioxid Redox Signal 20: 1126-1167.
34. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. 2007.A global double-fluorescent Cre reporter mouse. Genesis 45: 593-605.
35. Narita M, Young AR, Arakawa S, Samarajiwa SA, Nakashima T, Yoshida S, Hong S, Berry LS, Reichelt S, Ferreira M, et al. 2011. Spatial coupling of mTOR and autophagy augments secretory phenotypes. Science 332: 966-970.
36. Nathan C, Ding A. 2010. Nonresolving inflammation. Cell 140: 871-882.
37. Obenauf AC, Zou Y, Ji AL, Vanharanta S, Shu W, Shi H, Kong X, Bosenberg MC, Wiesner T, Rosen N, et al. 2015. Therapy-induced tumour secretomes promote resistance and tumour progression. Nature 520: 368-372.
38. Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, Meadows AT, Friedman DL, Marina N, Hobbie W, Kadan-Lottick NS, et al. 2006. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med 355: 1572-1582.
39. Ohanna M, Giuliano S, Bonet C, Imbert V, Hofman V, Zangari J, Bille K, Robert C, Bressac-De Paillerets B, Hofman P, et al. 2011. Senescent cells develop a PARP-1 and nuclear factor-B-associated secretome (PNAS). Genes Dev 25: 1245-1261.
40. Perez-Mancera PA, Young AR, Narita M. 2014. Inside and out: the activities of senescence in cancer. Nat Rev Cancer 14: 547-558.
41. Pober JS, Sessa WC. 2007. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7: 803-815.
42. Quintana A, Erta M, Ferrer B, Comes G, Giralt M, Hidalgo J. 2013. Astrocyte-specific deficiency of interleukin-6 and its receptor reveal specific roles in survival, body weight and behavior. Brain Behav Immun 27: 162-173.
43. Ray PD, Huang BW, Tsuji Y. 2012. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24: 981-990.
44. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR, Freund A, Campeau E, Davalos AR, Campisi J. 2009. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11: 973-979.
45. Salama R, Sadaie M, Hoare M, Narita M. 2014. Cellular senescence and its effector programs. Genes Dev 28: 99-114.
46. Seandel M, Butler JM, Kobayashi H, Hooper AT, White IA, Zhang F, Vertes EL, Kobayashi M, Zhang Y, Shmelkov SV, et al. 2008. Generation of a functional and durable vascular niche by the adenoviral E4ORF1 gene. Proc Natl Acad Sci 105: 19288-19293.
47. Seymour JF, Talpaz M, Cabanillas F, Wetzler M, Kurzrock R. 1995. Serum interleukin-6 levels correlate with prognosis in diffuse large-cell lymphoma. J Clin Oncol 13: 575-582.
48. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I, True L, Nelson PS. 2012. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 18: 1359-1368.
49. Tavora B, Reynolds LE, Batista S, Demircioglu F, Fernandez I, Lechertier T, Lees DM, Wong PP, Alexopoulou A, Elia G, et al. 2014. Endothelial-cell FAK targeting sensitizes tumours to DNA-damaging therapy. Nature 514: 112-116.
50. Tiedje C, Ronkina N, Tehrani M, Dhamija S, Laass K, Holtmann H, Kotlyarov A, Gaestel M. 2012. The p38/MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation. PLoS Genet 8: e1002977.
51. Tomimatsu K, Narita M. 2015. Translating the effects of mTOR on secretory senescence. Nat Cell Biol 17: 1230-1232.
52. Toso A, Revandkar A, Di Mitri D, Guccini I, Proietti M, Sarti M, Pinton S, Zhang J, Kalathur M, Civenni G, et al. 2014. Enhancing chemotherapy efficacy in Pten-deficient prostate tumors by activating the senescence-associated antitumor immunity. Cell Rep 9: 75-89.
53. Wajapeyee N, Serra RW, Zhu X, Mahalingam M, Green MR. 2008. Oncogenic BRAF induces senescence and apoptosis through pathways mediated by the secreted protein IGFBP7. Cell 132: 363-374.
54. Wang Y, Nakayama M, Pitulescu ME, Schmidt TS, Bochenek ML, Sakakibara A, Adams S, Davy A, Deutsch U, Luthi U, et al. 2010. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465: 483-486.
55. Zhang S, Liu X, Bawa-Khalfe T, Lu LS, Lyu YL, Liu LF, Yeh ET. 2012. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat Med 18: 1639-1642.