Shigella mediated depletion of macrophages in a murine breast cancer model is associated with tumor regression

PLoS ONE

Volumn 5, Issue 3, 2010, Pages

  Galmbacher, Katharina ^a,d   Heisig, Martin ^a,b   Hotz, Christian ^a,e   Wischhusen, Joerg ^c   Galmiche, Antoine ^a,f   Bergmann, Birgit ^a,b   Gentschev, Ivaylo ^a,g   Goebel, Werner ^b,e   Rapp, Ulf R ^a,h   Fensterle, Joachim ^a,i  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

^d INTERLAB international cent lab GmbH   (Germany)

^e UNIVERSITY OF MUNICH   (Germany)

^f UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

^g GENELUX CORPORATION   (United States)

^h MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

ⁱ ÆTerna Zentaris   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER REGRESSION; CONTROLLED STUDY; FEMALE; HELA CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; SHIGELLA FLEXNERI; TRANSGENIC MOUSE; TUMOR ASSOCIATED LEUKOCYTE; XENOTRANSPLANTATION; ANIMAL; CANCER INVASION; CANCER TRANSPLANTATION; CELL SEPARATION; DISEASE COURSE; EXPERIMENTAL NEOPLASM; HUMAN; MACROPHAGE; METABOLISM; MUTATION; SHIGELLA; TUMOR CELL LINE;

BACTERIA (MICROORGANISMS); MOUSE MAMMARY TUMOR VIRUS; MURINAE; MUS; MUS MUSCULUS; SHIGELLA; SHIGELLA FLEXNERI;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL SEPARATION; DISEASE PROGRESSION; FEMALE; HELA CELLS; HUMANS; MACROPHAGES; MAMMARY NEOPLASMS, ANIMAL; MICE; MICE, TRANSGENIC; MUTATION; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; SHIGELLA;

EID: 77949668375     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009572     Document Type: Article

References (38)

1. Coley WB (1991) The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res. pp 3-11.
2. Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, et al. (2004) Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol 22: 313-320.
3. Van Mellaert L, Barbé S, Anné J (2006) Clostridium spores as anti-tumour agents. Trends in Microbiology 14: 190-196.
4. Agrawal N, Bettegowda C, Cheong I, Geschwind JF, Drake CG, et al. (2004) Bacteriolytic therapy can generate a potent immune response against experimental tumors. Proc Natl Acad Sci U S A 101: 15172-15177.
5. Weibel S, Stritzker J, Eck M, Goebel W, Szalay AA (2008) Colonization of experimental murine breast tumours by Escherichia coli K-12 significantly alters the tumour microenvironment. Cell Microbiol.
6. Forbes NS, Munn LL, Fukumura D, Jain RK (2003) Sparse initial entrapment of systemically injected Salmonella typhimurium leads to heterogeneous accumulation within tumors. Cancer Res 63: 5188-5193.
7. Kasinskas RW, Forbes NS (2007) Salmonella typhimurium Lacking Ribose Chemoreceptors Localize in Tumor Quiescence and Induce Apoptosis. Cancer Res 67: 3201-3209.
8. Zhao M, Yang M, Ma H, Li X, Tan X, et al. (2006) Targeted Therapy with a Salmonella Typhimurium Leucine-Arginine Auxotroph Cures Orthotopic Human Breast Tumors in Nude Mice. Cancer Res 66: 7647-7652.
9. Westphal K, Leschner S, Jablonska J, Loessner H, Weiss S (2008) Containment of tumor-colonizing bacteria by host neutrophils. Cancer Res 68: 2952-2960.
10. Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407: 249-257.
11. Zhao M, Yang M, Li XM, Jiang P, Baranov E, et al. (2005) Tumor-targeting bacterial therapy with amino acid auxotrophs of GFP-expressing Salmonella typhimurium. Proc Natl Acad Sci U S A 102: 755-760.
12. Vassaux G, Nitcheu J, Jezzard S, Lemoine NR (2006) Bacterial gene therapy strategies. The Journal of Pathology 208: 290-298.
13. Pilgrim S, Stritzker J, Schoen C, Kolb-Maurer A, Geginat G, et al. (2003) Bactofection of mammalian cells by Listeria monocytogenes: improvement and mechanism of DNA delivery. Gene Ther 10: 2036-2045.
14. Pawelek JM, Low KB, Bermudes D (1997) Tumor-targeted Salmonella as a Novel Anticancer Vector. Cancer Res 57: 4537-4544.
15. Mueller MM, Fusenig NE (2004) Friends or foes - bipolar effects of the tumour stroma in cancer. Nat Rev Cancer 4: 839-849.
16. Lewis CE, Pollard JW (2006) Distinct Role of Macrophages in Different Tumor Microenvironments. Cancer Res 66: 605-612.
17. Kurahara H, Shinchi H, Mataki Y, Maemura K, Noma H, et al. (2009) Significance of M2-Polarized Tumor-Associated Macrophage in Pancreatic Cancer. J Surg Res.
18. Low KB, Ittensohn M, Le T, Platt J, Sodi S, et al. (1999) Lipid A mutant Salmonella with suppressed virulence and TNFalpha induction retain tumor-targeting in vivo. Nat Biotechnol 17: 37-41.
19. Mantovani A, Schioppa T, Porta C, Allavena P, Sica A (2006) Role of tumor-associated macrophages in tumor progression and invasion. Cancer and Metastasis Reviews 25: 315-322.
20. Qian B, Deng Y, Im JH, Muschel RJ, Zou Y, et al. (2009) A Distinct Macrophage Population Mediates Metastatic Breast Cancer Cell Extravasation, Establishment and Growth. PLoS ONE 4: e6562.
21. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, et al. (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 16: 183-194.
22. Cheng H-L, Trink B, Tzai T-S, Liu H-S, Chan S-H, et al. (2002) Overexpression of c-met as a Prognostic Indicator for Transitional Cell Carcinoma of the Urinary Bladder: A Comparison With p53 Nuclear Accumulation. J Clin Oncol 20: 1544-1550.
23. Zychlinsky A, Kenny B, Menard R, Prevost MC, Holland IB, et al. (1994) IpaB mediates macrophage apoptosis induced by Shigella flexneri. Mol Microbiol 11: 619-627.
24. Maurelli AT, Blackmon B, Curtiss R, 3rd (1984) Temperature-dependent expression of virulence genes in Shigella species. Infect Immun 43: 195-201.
25. Sansonetti PJ, Kopecko DJ, Formal SB (1982) Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun 35: 852-860.
26. Buchrieser C, Glaser P, Rusniok C, Nedjari H, D'Hauteville H, et al. (2000) The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38: 760-771.
27. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
28. Elsinghorst EA (1994) Measurement of invasion by gentamicin resistance. Methods Enzymol 236: 405-420.
29. Rymsa B, Becker HD, Lauchart W, de Groot H (1990) Hypoxia/reoxygenation injury in liver: Kupffer cells are much more vulnerable to reoxygenation than to hypoxia. Res Commun Chem Pathol Pharmacol 68: 263-266.
30. Fensterle J, Bergmann B, Yone, CLRP, Hotz C, Meyer SR, et al. (2008) Cancer immunotherapy based on recombinant Salmonella enterica serovar Typhimurium aroA strains secreting prostatespecific antigen and cholera toxin subunit B. Cancer Gene Therapy 15: 85-93.
31. Volpers C, Thirion C, Biermann V, Hussmann S, Kewes H, et al. (2003) Antibody-mediated targeting of an adenovirus vector modified to contain a synthetic immunoglobulin g-binding domain in the capsid. J Virol 77: 2093-2104.
32. Sansonetti PJ, Ryter A, Clerc P, Maurelli AT, Mounier J (1986) Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect Immun 51: 461-469.
33. Lin EY, Gouon-Evans V, Nguyen AV, Pollard JW (2002) The Macrophage Growth Factor CSF-1 in Mammary Gland Development and Tumor Progression. Journal of Mammary Gland Biology and Neoplasia 7: 147-162.
34. Lin EY, Nguyen AV, Russell RG, Pollard JW (2001) Colony-Stimulating Factor 1 Promotes Progression of Mammary Tumors to Malignancy. J Exp Med 193: 727-740.
35. Hoiseth SK, Stocker BA (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
36. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer-Hofer K, et al. (2006) Clodronate-liposome-mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 95: 272-281.
37. Lewis C, Murdoch C (2005) Macrophage responses to hypoxia: implications for tumor progression and anti-cancer therapies. Am J Pathol 167: 627-635.
38. Loessner H, Endmann A, Leschner S, Bauer H, Zelmer A, et al. (2008) Improving live attenuated bacterial carriers for vaccination and therapy. Int J Med Microbiol 298: 21-26.