Tackling the tumor microenvironment: What challenge does it pose to anticancer therapies?

Protein and Cell

Volumn 5, Issue 11, 2014, Pages 816-826

  Chen, Fei ^a   Qi, Xinyi ^b   Qian, Min ^a   Dai, Yue ^a   Sun, Yu ^a,b,c,d  

^a Chinese Academy of Sciences   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c VA Seattle Medical Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

clinical intervention; DNA damage; genotoxicity; secretory phenotype; therapy resistance; tumor microenvironment

Indexed keywords

AMPHIREGULIN; ANGIOPOIETIN; BLEOMYCIN; CAMPTOTHECIN; CARBOPLATIN; CHLORMETHINE; CISPLATIN; CYCLOPHOSPHAMIDE; CYTARABINE; DOCETAXEL; DOXORUBICIN; EPIREGULIN; FLUOROURACIL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MATRIX METALLOPROTEINASE; MERCAPTOPURINE; MITOMYCIN; MITOXANTRONE; NITROSOUREA; PIPERAZINE; PROCARBAZINE; PSORALEN; TEMOZOLOMIDE; TRIAZENE DERIVATIVE; UNINDEXED DRUG; VASCULOTROPIN; VINBLASTINE; VINCRISTINE; ANTINEOPLASTIC AGENT; CCAAT ENHANCER BINDING PROTEIN BETA;

ARTICLE; BIOPSY; CANCER RECURRENCE; CANCER THERAPY; CELL PROLIFERATION; DNA DAMAGE; EPITHELIAL MESENCHYMAL TRANSITION; GENE TARGETING; GENOTOXICITY; HUMAN; MACROPHAGE; METABOLIC RATE; NATURAL KILLER CELL; NONHUMAN; PATHOPHYSIOLOGY; PHAGOCYTE; PHASE 2 CLINICAL TRIAL (TOPIC); PHENOTYPE; PROSTATE CANCER; PROTEIN EXPRESSION; SENESCENCE; STROMA CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; UPREGULATION; BIOLOGICAL MODEL; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; PERSONALIZED MEDICINE; PROCEDURES; SIGNAL TRANSDUCTION; TRENDS;

ANTINEOPLASTIC AGENTS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; HUMANS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; NEOPLASMS; NF-KAPPA B; PRECISION MEDICINE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84920125252     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-014-0097-1     Document Type: Article

References (64)

1. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda di Fagagna F, Bernard D, Hernando E, Gil J (2008) Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133:1006–1018
2. Alspach E, Flanagan KC, Luo X, Ruhland MK, Huang H, Pazolli E, Donlin MJ, Marsh T, Piwnica-Worms D, Monahan J, Novack DV, McAllister SS, Stewart SA (2014) p38MAPK plays a crucial role in stromal-mediated tumorigenesis. Cancer Discov 4:716–729
3. Bhaumik D, Scott GK, Schokrpur S, Patil CK, Orjalo AV, Rodier F, Lithgow GJ, Campisi J (2009) MicroRNAs miR-146a/b negatively modulate the senescence-associated inflammatory mediators IL-6 and IL-8. Aging (Albany NY) 1:402–411
4. Blasi F, Carmeliet P (2002) uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 3:932–943
5. Borodkina A, Shatrova A, Abushik P, Nikolsky N, Burova E (2014) Interaction between ROS dependent DNA damage, mitochondria and p38 MAPK underlies senescence of human adult stem cells. Aging (Albany NY) 6:481–495
6. Bourzac K (2014) Biology: three known unknowns. Nature 509:S69–S71
7. Campisi J (2013) Aging, cellular senescence, and cancer. Annu Rev Physiol 75:685–705
8. Campisi J (2014) Cell biology: the beginning of the end. Nature 505:35–36
9. Chandler H, Peters G (2013) Stressing the cell cycle in senescence and aging. Curr Opin Cell Biol 6:765–771
10. Chien Y, Scuoppo C, Wang X, Fang X, Balgley B, Bolden JE, Premsrirut P, Luo W, Chicas A, Lee CS, Kogan SC, Lowe SW (2011) Control of the senescence-associated secretory phenotype by NF-κB promotes senescence and enhances chemosensitivity. Genes Dev 25:2125–2136
11. Collado M, Serrano M (2010) Senescence in tumours: evidence from mice and humans. Nat Rev Cancer 10:51–57
12. 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
13. 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
14. Coppé J-P, Rodier F, Patil CK, Freund A, Desprez PY, Campisi J (2011) Tumor suppressor and aging biomarker p16INK4a induces cellular senescence without the associated inflammatory secretory phenotype. J Biol Chem 286:36396–36403
15. Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, Haber JE, Iliakis G, Kallioniemi OP, Halazonetis TD (2014) Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 343:88–91
16. Coussens LM, Zitvogel L, Palucka AK (2013) Neutralizing tumor-promoting chronic inflammation: a magic bullet? Science 339:286–291
17. d’Adda di Fagagna F (2008) Living on a break: cellular senescence as a DNA-damage response. Nat Rev Cancer 8:512–522
18. Davalos AR, Coppe JP, Campisi J, Desprez PY (2010) Senescent cells as a source of inflammatory factors for tumor progression. Cancer Metastasis Rev 29:273–283
19. de Bono JS, Sandhu S, Attard G (2011) Beyond hormone therapy for prostate cancer with PARP inhibitors. Cancer Cell 19:573–574
20. Freund A, Orjalo AV, Desprez PY, Campisi J (2010) Inflammatory networks during cellular senescence: causes and consequences. Trends Mol Med 16:238–246
21. Freund A, Patil PK, Campisi J (2011) p38MAPK is a novel DNA damage response-independent regulator of the senescence-associated secretory phenotype. EMBO J 30:1536–1548
22. Fumagalli M, d’Adda di Fagagna F (2009) SASPense and DDRama in cancer and ageing. Nat Cell Biol 11:921–923
23. Garber K (2013) PARP inhibitors bounce back. Nat Rev Drug Discov 12:725–727
24. Gilbert LA, Hemann MT (2010) DNA damage-mediated induction of a chemoresistant niche. Cell 143:355–366
25. Gilbert LA, Hemann MT (2011) Chemotherapeutic resistance: surviving stressful situations. Cancer Res 71:5062–5066
26. Goruppi S, Dotto GP (2013) Mesenchymal stroma: primary determinant and therapeutic target for epithelial cancer. Trends Cell Biol 23:593–602
27. Gupta SC, Sung B, Prasad S, Webb LJ, Aggarwal BB (2013) Cancer drug discovery by repurposing: teaching new tricks to old dogs. Trends Pharmacol Sci 34:508–517
28. Hallek M, Chen J, Hemann MT (2014) Sensitizing protective tumor microenvironments to antibody-mediated therapy. Cell 156:590–602
29. Harrison C (2013) Pharmacokinetics: single-cell imaging adds insight into drug action. Nat Rev Drug Discov 12:264
30. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA (2008) DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 8:193–204
31. Helleday T, Eshtad S, Nik-Zainal S (2014) Mechanisms underlying mutational signatures in human cancers. Nat Rev Genet 15:585–598
32. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461:1071–1078
33. Junttila MR, de Sauvage FJ (2013) Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501:346–354
34. Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141:52–67
35. Kim JJ, Tannock IF (2005) Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5:516–525
36. Köpper F, Bierwirth C, Schön M, Kunze M, Elvers I, Kranz D, Saini P, Menon MB, Walter D, Sørensen CS, Gaestel M, Helleday T, Schön MP, Dobbelstein M (2013) Damage-induced DNA replication stalling relies on MAPK-activated protein kinase 2 activity. Proc Natl Acad Sci USA 110:16856–16861
37. Kuilman T, Peeper DS (2009) Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 9:81–94
38. 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
39. Liu D, Hornsby PJ (2007) Senescent human fibroblasts increase the early growth of xenograft tumors via matrix metalloproteinase secretion. Cancer Res 67:3117–3126
40. Moiseeva O, Deschênes-Simard X, St-Germain E, Igelmann S, Huot G, Cadar AE, Bourdeau V, Pollak MN, Ferbeyre G (2013) Metformin inhibits the senescence-associated secretory phenotype by interfering with IKK/NF-κB activation. Aging Cell 12:489–498
41. Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9:274–284
42. Norton L, Simon R (1986) The Norton-Simon hypothesis revisited. Cancer Treat Rep 70:163–169
43. Ohanna M, Giuliano S, Bonet C, Imbert V, Hofman V, Zangari L, Bille K, Robert C, Bressac-de Paillerets B, Hofman P, Rocchi S, Peyron JF, Lacour JP, Ballotti R, Bertolotto C (2011) Senescent cells develop a PARP-1 and nuclear factor-êB-associated secretome (PNAS). Genes Dev 25:1245–1261
44. Orjalo A, BhaumikD Gengler B, ScottGK Campisi J (2009) Cell surface IL-1α is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci USA 106:17031–17036
45. Ozdemir BC, Pentcheva-Hoang T, Carstens JL, Zheng X, Wu CC, Simpson TR, Laklai H, Sugimoto H, Kahlert C, Novitskiy SV, De Jesus-Acosta A, Sharma P, Heidari P, Mahmood U, Chin L, Moses HL, Weaver VM, Maitra A, Allison JP, LeBleu VS, Kalluri R (2014) Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25:719–734
46. Pallasch CP, Leskov I, Braun CJ, Vorholt D, Drake A, Soto-Feliciano YM, Bent EH, Schwamb J, Iliopoulou B, Kutsch N, van Rooijen N, Frenzel LP, Wendtner CM, Heukamp L, Kreuzer KA, Palucka K, Banchereau J (2014) SnapShot: cancer vaccines. Cell 157:516
47. Palucka K, Banchereau J (2014) SnapShot: cancer vaccines. Cell 157:516–516
48. Patel KJ, Lee C, Tan Q, Tannock IF (2013) Use of the proton pump inhibitor pantoprazole to modify the distribution and activity of doxorubicin: a potential strategy to improve the therapy of solid tumors. Clin Cancer Res 19:6766–6776
49. Pulukuri SMK, Knost JA, Estes N, Rao JS (2009) Small interfering RNA–directed knockdown of uracil DNA glycosylase induces apoptosis and sensitizes human prostate cancer cells to genotoxic stress. Mol Cancer Res 7:1285–1293
50. Rhim AD, Oberstein PE, Thomas DH, Mirek ET, Palermo CF, Sastra SA, Dekleva EN, Saunders T, Becerra CP, Tattersall IW, Westphalen CB, Kitajewski J, Fernandez-Barrena MG, Fernandez-Zapico ME, Iacobuzio-Donahue C, Olive KP, Stanger BZ (2014) Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25:735–747
51. 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
52. Rodier F, Munoz DP, Teachenor R, Chu V, Le O, Bhaumik D, Coppé JP, Campeau E, Beauséjour CM, Kim SH, Davalos AR, Campisi J (2011) DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 124:68–81
53. Sale JE, Lehmann AR, Woodgate R (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13:141–152
54. Schmitt CA (2003) Senescence, apoptosis and therapy—cutting the lifelines of cancer. Nat Rev Cancer 3:286–295
55. Sun Y, Nelson PS (2012) Molecular pathways: involving microenvironment damage responses in cancer therapy resistance. Clin Cancer Res 18:4019–4025
56. 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
57. Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006) NF-kB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. PNAS 103:12481–12486
58. Tell G, Wilson DM III (2010) Targeting DNA repair proteins for cancer treatment. Cell Mol Life Sci 67:3569–3572
59. Tentori L, Muzi A, Dorio AS, Scarsella M, Leonetti C, Shah GM, Xu W, Camaioni E, Gold B, Pellicciari R, Dantzer F, Zhang J, Graziani G (2010) Pharmacological inhibition of poly(ADPribose) polymerase (PARP) activity in PARP-1 silenced tumour cells increases chemosensitivity to temozolomide and to a N3-adenine selective methylating agent. Curr Cancer Drug Targets 10:368–383
60. Tomé M, Sepúlveda JC, Delgado M, Andrades JA, Campisi J, González MA, Bernad A (2014) MiR-335 correlates with senescence/aging in human mesenchymal stem cells and inhibits their therapeutic actions through inhibition of AP-1 activity. Stem Cells 32:2299–2344
61. Visvader JE, Lindeman GJ (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat Rev Cancer 8:755–768
62. Wang Z, Chen W (2013) Emerging roles of SIRT1 in cancer drug resistance. Genes Cancer 4:82–90
63. Yu M, Tannock IF (2012) Targeting tumor architecture to favor drug penetration: a new weapon to combat chemoresistance in pancreatic cancer? Cancer Cell 21:327–329
64. Yu M, Ocana A, Tannock IF (2013) Reversal of ATP-binding cassette drug transporter activity to modulate chemoresistance: why has it failed to provide clinical benefit? Cancer Metastasis Rev 32:211–227