DNA from dead cancer cells induces TLR9-mediated invasion and inflammation in living cancer cells

Breast Cancer Research and Treatment

Volumn 142, Issue 3, 2013, Pages 477-487

  Tuomela, Johanna ^a,b   Sandholm, Jouko ^a,b   Kaakinen, Mika ^c   Patel, Ankita ^b   Kauppila, Joonas H ^c,d   Ilvesaro, Joanna ^a,b   Chen, Dongquan ^e   Harris, Kevin W ^a,b,f   Graves, David ^b   Selander, Katri S ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF OULU   (Finland)

^d OULU UNIVERSITY HOSPITAL   (Finland)

^e and Clinical Center   (United States)

^f BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

DNA; Inflammation; Invasion; Toll like receptor 9; Triple negative breast cancer

Indexed keywords

ANTINEOPLASTIC AGENT; CATHEPSIN; CELL DNA; DOXORUBICIN; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 9;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CANCER CELL; CELL DEATH; CELL INVASION; CELL SIZE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TREATMENT RESPONSE; TRIPLE NEGATIVE BREAST CANCER;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DNA; FEMALE; HETEROGRAFTS; HUMANS; INFLAMMATION; MICE; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; RNA INTERFERENCE; TOLL-LIKE RECEPTOR 9; TUMOR BURDEN;

EID: 84890309796     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-013-2762-0     Document Type: Article

References (57)

1. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. (2000) A toll-like receptor recognizes bacterial DNA. Nature 408:740-745
2. Akira S, Hemmi H (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 85:85-95
3. Hoque R, Malik AF, Gorelick F, Mehal WZ (2012) Sterile inflammatory response in acute pancreatitis. Pancreas 41:353-357
4. Huang H, Evankovich J, Yan W, Nace G, Zhang L, et al. (2011) Endogenous histones function as alarmins in sterile inflammatory liver injury through toll-like receptor 9 in mice. Hepatology 54:999-1008
5. Imaeda AB, Watanabe A, Sohail MA, Mahmood S, Mohamadnejad M, et al. (2009) Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest 119:305-314
6. Ilvesaro JM, Merrell MA, Li L, Wakchoure S, Graves D, et al. (2008) Toll-like receptor 9 mediates CpG oligonucleotide-induced cellular invasion. Mol Cancer Res 6:1534-1543
7. Jukkola-Vuorinen A, Rahko E, Vuopala KS, Desmond R, Lehenkari PP, et al. (2009) Toll-like receptor-9 expression is inversely correlated with estrogen receptor status in breast cancer. J Innate Immun 1:59-68
8. Sandholm J, Kauppila JH, Pressey C, Tuomela J, Jukkola-Vuorinen A, et al. (2012) Estrogen receptor-alpha and sex steroid hormones regulate toll-like receptor-9 expression and invasive function in human breast cancer cells. Breast Cancer Res Treat 132:411-419
9. Tuomela J, Sandholm J, Karihtala P, Ilvesaro J, Vuopala KS, et al. (2012) Low TLR9 expression defines an aggressive subtype of triple-negative breast cancer. Breast Cancer Res Treat 135:481-493
10. Väisänen MR, Väisänen T, Jukkola-Vuorinen A, Vuopala KS, Desmond R, et al. (2010) Expression of toll-like receptor-9 is increased in poorly differentiated prostate tumors. Prostate 70:817-824
11. Ilvesaro JM, Merrell MA, Swain TM, Davidson J, Zayzafoon M, et al. (2007) Toll like receptor-9 agonists stimulate prostate cancer invasion in vitro. Prostate 67:774-781
12. Merrell MA, Ilvesaro JM, Lehtonen N, Sorsa T, Gehrs B, et al. (2006) Toll-like receptor 9 agonists promote cellular invasion by increasing matrix metalloproteinase activity. Mol Cancer Res 4:437-447
13. Takala H, Kauppila JH, Soini Y, Selander KS, Vuopala KS, et al. (2011) Toll-like receptor 9 is a novel biomarker for esophageal squamous cell dysplasia and squamous cell carcinoma progression. J Innate Immun 3:631-638
14. Kauppila JH, Takala H, Selander KS, Lehenkari PP, Saarnio J, et al. (2011) Increased toll-like receptor 9 expression indicates adverse prognosis in oesophageal adenocarcinoma. Histopathology 59:643-649
15. Lande R, Gregorio J, Facchinetti V, Chatterjee B, Wang YH, et al. (2007) Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 449:564-569
16. Sandgren S, Wittrup A, Cheng F, Jonsson M, Eklund E, et al. (2004) The human antimicrobial peptide LL-37 transfers extracellular DNA plasmid to the nuclear compartment of mammalian cells via lipid rafts and proteoglycan- dependent endocytosis. J Biol Chem 279:17951-17956
17. Scott MG, Davidson DJ, Gold MR, Bowdish D, Hancock RE (2002) The human antimicrobial peptide LL-37 is a multifunctional modulator of innate immune responses. J Immunol 169:3883-3891
18. Heilborn JD, Nilsson MF, Jimenez CI, Sandstedt B, Borregaard N, et al. (2005) Antimicrobial protein hCAP18/LL-37 is highly expressed in breast cancer and is a putative growth factor for epithelial cells. Int J Cancer 114:713-719
19. Weber G, Chamorro CI, Granath F, Liljegren A, Zreika S, et al. (2009) Human antimicrobial protein hCAP18/LL-37 promotes a metastatic phenotype in breast cancer. Breast Cancer Res 11:R6
20. Sandholm J, Tuomela JM, Kauppila JH, Harris KW, Graves D, et al. (2013) Hypoxia regulates toll-like receptor-9 expression and invasive function in human brain cancer cells in vitro. Oncol Lett (in press)
21. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111
22. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511-515
23. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621-628
24. Xing Y, Yu T, Wu YN, Roy M, Kim J, et al. (2006) An expectation- maximization algorithm for probabilistic reconstructions of full-length isoforms from splice graphs. Nucleic Acids Res 34:3150-3160
25. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470-476
26. Kojima K, Bowersock GJ, Kojima C, Klug CA, Grizzle WE, et al. (2012) Validation of a robust proteomic analysis carried out on formalin-fixed paraffin-embedded tissues of the pancreas obtained from mouse and human. Proteomics 12:3393-3402
27. Wärri AM, Huovinen RL, Laine AM, Martikainen PM, Härkönen PL (1993) Apoptosis in toremifene-induced growth inhibition of human breast cancer cells in vivo and in vitro. J Natl Cancer Inst 85:1412-1418
28. Johnson MS, Jumbo-Lucioni P, Watts AJ, Allison DB, Nagy TR (2007) Effect of dairy supplementation on body composition and insulin resistance in mice. Nutrition 23:836-843
29. Kim JE, Kim HJ, Choi JM, Lee KH, Kim TY, et al. (2010) The antimicrobial peptide human cationic antimicrobial protein-18/cathelicidin LL-37 as a putative growth factor for malignant melanoma. Br J Dermatol 163:959-967
30. Nurmenniemi S, Kuvaja P, Lehtonen S, Tiuraniemi S, Alahuhta I, et al. (2010) Toll-like receptor 9 ligands enhance mesenchymal stem cell invasion and expression of matrix metalloprotease-13. Exp Cell Res 316:2676-2682
31. Asagiri M, Hirai T, Kunigami T, Kamano S, Gober HJ, et al. (2008) Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 319:624-627
32. Ronkainen H, Hirvikoski P, Kauppila S, Vuopala KS, Paavonen TK, et al. (2011) Absent toll-like receptor-9 expression predicts poor prognosis in renal cell carcinoma. J Exp Clin Cancer Res 30:84
33. Kauppila JH, Karttunen TJ, Saarnio J, Nyberg P, Salo T, et al. (2012) Short DNA sequences and bacterial DNA induce esophageal, gastric, and colorectal cancer cell invasion. APMIS 121:511-522
34. Wang C, Cao S, Yan Y, Ying Q, Jiang T, et al. (2010) TLR9 expression in glioma tissues correlated to glioma progression and the prognosis of GBM patients. BMC Cancer 10:415
35. Gonzalez-Reyes S, Marin L, Gonzalez L, Gonzalez LO, del Casar JM, et al. (2010) Study of TLR3, TLR4 and TLR9 in breast carcinomas and their association with metastasis. BMC Cancer 10:665
36. Lamphier MS, Sirois CM, Verma A, Golenbock DT, Latz E (2006) TLR9 and the recognition of self and non-self nucleic acids. Ann N Y Acad Sci 1082:31-43
37. Rifkin IR, Leadbetter EA, Busconi L, Viglianti G, Marshak-Rothstein A (2005) Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 204:27-42
38. Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, et al. (2011) Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med 3:73ra19
39. Widlak P, Garrard WT (2009) Roles of the major apoptotic nuclease-DNA fragmentation factor-in biology and disease. Cell Mol Life Sci 66:263-274
40. Napirei M, Wulf S, Mannherz HG (2004) Chromatin breakdown during necrosis by serum DNAse1 and the plasminogen system. Arthritis Rheum 50:1873-1883
41. Tsou KC, Yip KF (1976) Effect of deoxyribonuclease on adriamycin-polynucleotide complexes. Cancer Res 36:3367-3373
42. Park B, Brinkmann MM, Spooner E, Lee CC, Kim YM, et al. (2008) Proteolytic cleavage in an endolysosomal compartment is required for activation of toll-like receptor 9. Nat Immunol 9:1407-1414
43. Ewald SE, Engel A, Lee J, Wang M, Bogyo M, et al. (2011) Nucleic acid recognition by toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J Exp Med 208:643-651
44. Laginha KM, Verwoert S, Charrois GJ, Allen TM (2005) Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors. Clin Cancer Res 11:6944-6949
45. Stallard S, Morrison JG, George WD, Kaye SB (1990) Distribution of doxorubicin to normal breast and tumour tissue in patients undergoing mastectomy. Cancer Chemother Pharmacol 25:286-290
46. Jahr S, Hentze H, Englisch S, Hardt D, Fackelmayer FO, et al. (2001) DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res 61:1659-1665
47. Umetani N, Giuliano AE, Hiramatsu SH, Amersi F, Nakagawa T, et al. (2006) Prediction of breast tumor progression by integrity of free circulating DNA in serum. J Clin Oncol 24:4270-4276
48. Ng B, Wolf RF, Weksler B, Brennan MF, Burt M (1993) Growth hormone administration preserves lean body mass in sarcoma-bearing rats treated with doxorubicin. Cancer Res 53:5483-5486
49. Hajjaji N, Couet C, Besson P, Bougnoux P (2012) DHA effect on chemotherapy-induced body weight loss: an exploratory study in a rodent model of mammary tumors. Nutr Cancer 64:1000-1007
50. Tsai VW, Husaini Y, Manandhar R, Lee-Ng KK, Zhang HP, et al. (2012) Anorexia/cachexia of chronic diseases: a role for the TGF-beta family cytokine MIC-1/GDF15. J Cachexia Sarcopenia Muscle 3:239-243
51. Wakchoure S, Swain TM, Hentunen TA, Bauskin AR, Brown DA, et al. (2009) Expression of macrophage inhibitory cytokine-1 in prostate cancer bone metastases induces osteoclast activation and weight loss. Prostate 69:652-661
52. Song B, Zhang D, Wang S, Zheng H, Wang X (2009) Association of interleukin-8 with cachexia from patients with low-third gastric cancer. Comput Funct Genomics 2009:212345
53. Baumgarten AJ, Fiebig HH, Burger AM (2007) Molecular analysis of xenograft models of human cancer cachexia - possibilities for therapeutic intervention. Cancer Genomics Proteomics 4:223-231
54. Tisdale MJ (2003) Pathogenesis of cancer cachexia. J Support Oncol 1:159-168
55. Kono H, Rock KL (2008) How dying cells alert the immune system to danger. Nat Rev Immunol 8:279-289
56. Chen GY, Nunez G (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10:826-837
57. Wagner H (2010) Hemozoin: malaria's "built-in" adjuvant and TLR9 agonist. Cell Host Microbe 7:5-6