Noninvasive imaging of infection after treatment with tumor-homing bacteria using Chemical Exchange Saturation Transfer (CEST) MRI

Magnetic Resonance in Medicine

Volumn 70, Issue 6, 2013, Pages 1690-1698

  Liu, Guanshu ^a,b   Bettegowda, Chetan ^b,c   Qiao, Yuan ^c   Staedtke, Verena ^b   Chan, Kannie W Y ^b   Bai, Renyuan ^b   Li, Yuguo ^b   Riggins, Gregory J ^b   Kinzler, Kenneth W ^c   Bulte, Jeff W M ^a,b   McMahon, Michael T ^a,b   Gilad, Assaf A ^b   Vogelstein, Bert ^c   Zhou, Shibin ^c   Van Zijl, Peter C M ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

bacteria imaging; CEST MRI; endogenous CEST contrast; molecular imaging

Indexed keywords

CLOSTRIDIUM; CULTIVATION; MAGNETIC RESONANCE IMAGING; MAMMALS; PATHOLOGY; TUMORS;

BACTERIAL SUSPENSIONS; BROAD FREQUENCY RANGE; CEST MRIS; CHEMICAL EXCHANGE SATURATION TRANSFER; COLORECTAL TUMORS; ENDOGENOUS CEST CONTRAST; GRAM-POSITIVE BACTERIUM; NON-INVASIVE IMAGING;

MOLECULAR IMAGING;

ANTINEOPLASTIC AGENT; BACTERIUM LIPOPOLYSACCHARIDE; CHEMICAL EXCHANGE SATURATION TRANSFER CONTRAST MEDIUM; CONTRAST MEDIUM; ONCOLYTIC CLOSTRIDIUM NOVYI NT SPORE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; BACTERIAL SPORE; BACTERIOLYSIS; BACTERIUM DETECTION; CANCER CELL; CANCER THERAPY; CELL PH; CELLS; CHEMICAL EXCHANGE SATURATION TRANSFER MAGNETIC RESONANCE IMAGING; CLOSTRIDIUM; CLOSTRIDIUM INFECTION; CLOSTRIDIUM NOVYI NT; COLON CARCINOMA; COLORECTAL TUMOR; CONTROLLED STUDY; DIFFUSION WEIGHTED IMAGING; FEMALE; GERMINATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; SPORE GERMINATION; TUMOR BLEEDING;

BACTERIA IMAGING; CEST MRI; ENDOGENOUS CEST CONTRAST; MOLECULAR IMAGING;

ANIMALS; BIOLOGICAL THERAPY; CELL LINE, TUMOR; CLOSTRIDIUM; CLOSTRIDIUM INFECTIONS; COLORECTAL NEOPLASMS; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MICE; MICE, INBRED BALB C; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84888012495     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.24955     Document Type: Article

References (76)

1. St. Jean AT, Zhang M, Forbes NS,. Bacterial therapies: completing the cancer treatment toolbox. Curr Opin Biotechnol 2008; 19: 511-517.
2. Wei MQ, Mengesha A, Good D, Anne J,. Bacterial targeted tumour therapy-dawn of a new era. Cancer Lett 2008; 259: 16-27.
3. Forbes NS,. Engineering the perfect (bacterial) cancer therapy. Nat Rev Cancer 2010; 10: 785-794.
4. Coley WB,. The treatment of malignat tumors by repeated inoculations of erysipelas: with a report of ten original cases. Am J Med Sci 1893; 105: 487.
5. Coley WB,. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin Orthop Relat Res 1991: 3-11.
6. Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, Gentschev I, Goebel W, Szalay AA,. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol 2004; 22: 313-320.
7. Morrissey D, O'Sullivan GC, Tangney M,. Tumour targeting with systemically administered bacteria. Curr Gene Ther 2010; 10: 3-14.
8. Connell HC,. The study and treatment of cancer by proteolytic enzymes: preliminary report. Can Med Assoc J 1935; 33: 364-370.
9. Challis GB, Stam HJ,. The spontaneous regression of cancer. A review of cases from 1900 to 1987. Acta Oncol 1990; 29: 545-550.
10. Yazawa K, Fujimori M, Amano J, Kano Y, Taniguchi S,. Bifidobacterium longum as a delivery system for cancer gene therapy: selective localization and growth in hypoxic tumors. Cancer Gene Ther 2000; 7: 269-274.
11. Dang L, Bettegowda C, Huso D, Kinzler K, Vogelstein B,. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc Natl Acad Sci U S A 2001; 98: 15155-15160.
12. Vassaux G, Nitcheu J, Jezzard S, Lemoine NR,. Bacterial gene therapy strategies. J Pathol 2006; 208: 290-298.
13. Groot AJ, Mengesha A, van der Wall E, van Diest PJ, Theys J, Vooijs M,. Functional antibodies produced by oncolytic clostridia. Biochem Biophys Res Commun 2007; 364: 985-989.
14. Liu F, Zhang L, Hoffman RM, Zhao M,. Vessel destruction by tumor-targeting Salmonella typhimurium A1-R is enhanced by high tumor vascularity. Cell Cycle 2010; 9: 4518-4524.
15. Zhao M, Yang M, Ma H, Li X, Tan X, Li S, Yang Z, Hoffman RM,. Targeted therapy with a Salmonella typhimurium leucine-arginine auxotroph cures orthotopic human breast tumors in nude mice. Cancer Res 2006; 66: 7647-7652.
16. Low KB, Ittensohn M, Le T, et al. Lipid A mutant Salmonella with suppressed virulence and TNF[alpha] induction retain tumor-targeting in vivo. Nat Biotechnol 1999; 17: 37-41.
17. Pawelek JM, Low KB, Bermudes D,. Tumor-targeted Salmonella as a novel anticancer vector. Cancer Res 1997; 57: 4537-4544.
18. Bettegowda C, Huang X, Lin J, et al. The genome and transcriptomes of the anti-tumor agent Clostridium novyi-NT. Nat Biotechnol 2006; 24: 1573-1580.
19. Dang LH, Bettegowda C, Agrawal N, et al. Targeting vascular and avascular compartments of tumors with C. novyi-NT and anti-microtubule agents. Cancer Biol Ther 2004; 3: 326-337.
20. Stritzker J, Weibel S, Hill PJ, Oelschlaeger TA, Goebel W, Szalay AA,. Tumor-specific colonization, tissue distribution, and gene induction by probiotic Escherichia coli Nissle 1917 in live mice. Int J Med Microbiol 2007; 297: 151-162.
21. Agrawal N, Bettegowda C, Cheong I, Geschwind J, Drake C, Hipkiss E, Tatsumi M, Dang L, Diaz L, Pomper M,. Bacteriolytic therapy can generate a potent immune response against experimental tumors. Proc Natl Acad Sci U S A 2004; 101: 15172-15177.
22. Bettegowda C, Dang L, Abrams R, Huso D, Dillehay L, Cheong I, Agrawal N, Borzillary S, McCaffery J, Watson E,. Overcoming the hypoxic barrier to radiation therapy with anaerobic bacteria. Proc Natl Acad Sci U S A 2003; 100: 15083-15088.
23. Min JJ, Nguyen VH, Kim HJ, Hong Y, Choy HE,. Quantitative bioluminescence imaging of tumor-targeting bacteria in living animals. Nat Protoc 2008; 3: 629-636.
24. Hutchens M, Luker GD,. Applications of bioluminescence imaging to the study of infectious diseases. Cell Microbiol 2007; 9: 2315-2322.
25. Contag CH, Contag PR, Mullins JI, Spilman SD, Stevenson DK, Benaron DA,. Photonic detection of bacterial pathogens in living hosts. Mol Microbiol 1995; 18: 593-603.
26. Ning X, Lee S, Wang Z, Kim D, Stubblefield B, Gilbert E, Murthy N,. Maltodextrin-based imaging probes detect bacteria in vivo with high sensitivity and specificity. Nat Mater 2011; 10: 602-607.
27. Hope-Roberts M, Wainwright M, Horobin RW,. Real-time imaging of bacteria in living mice using a fluorescent dye. Biotech Histochem 2011; 86: 104-107.
28. Soghomonyan SA, Doubrovin M, Pike J, et al. Positron emission tomography (PET) imaging of tumor-localized Salmonella expressing HSV1-TK. Cancer Gene Ther 2005; 12: 101-108.
29. Bettegowda C, Foss CA, Cheong I, Wang Y, Diaz L, Agrawal N, Fox J, Dick J, Dang LH, Zhou S,. Imaging bacterial infections with radiolabeled 1-(2-deoxy-2-fluoro-D-arabinofuranosyl)-5-iodouracil. Proc Natl Acad Sci U S A 2005; 102: 1145-1150.
30. Haimes AB, Zimmerman RD, Morgello S, Weingarten K, Becker RD, Jennis R, Deck MD,. MR imaging of brain abscesses. AJR Am J Roentgenol 1989; 152: 1073-1085.
31. Leuthardt EC, Wippold FJ Jr, Oswood MC, Rich KM,. Diffusion-weighted MR imaging in the preoperative assessment of brain abscesses. Surg Neurol 2002; 58: 395-402.
32. Chang SC, Lai PH, Chen WL, Weng HH, Ho JT, Wang JS, Chang CY, Pan HB, Yang CF,. Diffusion-weighted MRI features of brain abscess and cystic or necrotic brain tumors: comparison with conventional MRI. Clin Imaging 2002; 26: 227-236.
33. Garg M, Misra MK, Chawla S, Prasad KN, Roy R, Gupta RK,. Broad identification of bacterial type from pus by 1H MR spectroscopy. Eur J Clin Invest 2003; 33: 518-524.
34. Dev R, Gupta RK, Poptani H, Roy R, Sharma S, Husain M,. Role of in vivo proton magnetic resonance spectroscopy in the diagnosis and management of brain abscesses. Neurosurgery 1998; 42: 37-42.
35. Lai PH, Ho JT, Chen WL, Hsu SS, Wang JS, Pan HB, Yang CF,. Brain abscess and necrotic brain tumor: discrimination with proton MR spectroscopy and diffusion-weighted imaging. AJNR Am J Neuroradiol 2002; 23: 1369-1377.
36. Himmelreich U, Accurso R, Malik R, Dolenko B, Somorjai RL, Gupta RK, Gomes L, Mountford CE, Sorrell TC,. Identification of Staphylococcus aureus brain abscesses: rat and human studies with 1H MR spectroscopy. Radiology 2005; 236: 261-270.
37. Goffeney N, Bulte JW, Duyn J, Bryant LH Jr, van Zijl PC,. Sensitive NMR detection of cationic-polymer-based gene delivery systems using saturation transfer via proton exchange. J Am Chem Soc 2001; 123: 8628-8629.
38. Ward KM, Aletras AH, Balaban RS,. A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). J Magn Reson 2000; 143: 79-87.
39. van Zijl PC, Yadav NN,. Chemical exchange saturation transfer (CEST): what is in a name and what isn't? Magn Reson Med 2011; 65: 927-948.
40. Hancu I, Dixon WT, Woods M, Vinogradov E, Sherry AD, Lenkinski RE,. CEST and PARACEST MR contrast agents. Acta Radiol 2010; 51: 910-923.
41. Terreno E, Castelli DD, Aime S,. Encoding the frequency dependence in MRI contrast media: the emerging class of CEST agents. Contrast Media Mol Imaging 2010; 5: 78-98.
42. Liu G, Song X, Chan KW, McMahon MT,. Nuts and bolts of chemical exchange saturation transfer MRI. NMR Biomed 2013; 26: 810-828.
43. Jones CK, Schlosser MJ, van Zijl PC, Pomper MG, Golay X, Zhou J,. Amide proton transfer imaging of human brain tumors at 3T. Magn Reson Med 2006; 56: 585-592.
44. Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PCM,. Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 2003; 50: 1120-1126.
45. Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC,. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 2003; 9: 1085-1090.
46. Haris M, Singh A, Cai K, Nath K, Crescenzi R, Kogan F, Hariharan H, Reddy R,. MICEST: a potential tool for non-invasive detection of molecular changes in Alzheimer's disease. J Neurosci Methods 2013; 212: 87-93.
47. Haris M, Nanga RP, Singh A, Cai K, Kogan F, Hariharan H, Reddy R,. Exchange rates of creatine kinase metabolites: feasibility of imaging creatine by chemical exchange saturation transfer MRI. NMR Biomed 2012; 25: 1305-1309.
48. Cai K, Haris M, Singh A, Kogan F, Greenberg JH, Hariharan H, Detre JA, Reddy R,. Magnetic resonance imaging of glutamate. Nat Med 2012; 18: 302-306.
49. van Zijl PC, Jones CK, Ren J, Malloy CR, Sherry AD,. MRI detection of glycogen in vivo by using chemical exchange saturation transfer imaging (glycoCEST). Proc Natl Acad Sci U S A 2007; 104: 4359-4364.
50. Schleifer KH, Stackebrandt E,. Molecular systematics of prokaryotes. Ann Rev Microbiol 1983; 37: 143-187.
51. Mader I, Rauer S, Gall P, Klose U,. (1)H MR spectroscopy of inflammation, infection and ischemia of the brain. Eur J Radiol 2008; 67: 250-257.
52. Zhao JM, Har-el YE, McMahon MT, Zhou J, Sherry AD, Sgouros G, Bulte JW, van Zijl PC,. Size-induced enhancement of chemical exchange saturation transfer (CEST) contrast in liposomes. J Am Chem Soc 2008; 130: 5178-5184.
53. Aime S, Delli Castelli D, Terreno E,. Highly sensitive MRI chemical exchange saturation transfer agents using liposomes. Angew Chem 2005; 117: 5649-5651.
54. Dehoux MJM, van Beneden RP, Lause PL, Thissen JPM,. Induction of MafBx and Murf ubiquitin ligase mRNAs in rat skeletal muscle after LPS injection. FEBS Lett 2003; 544: 214-217.
55. Adler H, Crow W, Hadden C, Hall J, Machanoff R,. New techniques for growing anaerobic bacteria: experiments with Clostridium butyricum and Clostridium acetobutylicum. Oak Ridge, Tennessee: Oak Ridge National Lab; 1983.
56. Liu G, Gilad AA, Bulte JW, van Zijl PC, McMahon MT,. High-throughput screening of chemical exchange saturation transfer MR contrast agents. Contrast Media Mol Imaging 2010; 5: 162-170.
57. Lowe SE, Jain MK, Zeikus JG,. Biology, ecology, and biotechnological applications of anaerobic bacteria adapted to environmental stresses in temperature, pH, salinity, or substrates. Microbiol Rev 1993; 57: 451-509.
58. Raatjes G, Smelt J,. Clostridium botulinum can grow and form toxin at pH values lower than 4.6. Nature 1979; 281: 398-399.
59. Kim M, Gillen J, Landman BA, Zhou J, van Zijl PC,. Water saturation shift referencing (WASSR) for chemical exchange saturation transfer (CEST) experiments. Magn Reson Med 2009; 61: 1441-1450.
60. Liu G, Liang Y, Bar-Shir A, et al. Monitoring enzyme activity using a diamagnetic chemical exchange saturation transfer magnetic resonance imaging contrast agent. J Am Chem Soc 2011; 133: 16326-16329.
61. Qiao Y, Huang X, Nimmagadda S, et al. A robust approach to enhance tumor-selective accumulation of nanoparticles. Oncotarget 2011; 2: 59-68.
62. Chicoine MR, Won EK, Zahner MC,. Intratumoral injection of lipopolysaccharide causes regression of subcutaneously implanted mouse glioblastoma multiforme. Neurosurgery 2001; 48: 607-614; discussion 614-615.
63. Zhao XN, Wen ZB, Zhang G, Huang FH, Lu SL, Wang XL, Hu SG, Chen M, Zhou JY,. Three-dimensional turbo-spin-echo amide proton transfer MR imaging at 3-Tesla and its application to high-grade human brain tumors. Mol Imaging Biol 2013; 15: 114-122.
64. Zhou J, Blakeley JO, Hua J, Kim M, Laterra J, Pomper MG, van Zijl PC,. Practical data acquisition method for human brain tumor amide proton transfer (APT) imaging. Magn Reson Med 2008; 60: 842-849.
65. Haris M, Cai K, Singh A, Hariharan H, Reddy R,. In vivo mapping of brain myo-inositol. Neuroimage 2011; 54: 2079-2085.
66. Ling W, Regatte RR, Navon G, Jerschow A,. Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST). Proc Natl Acad Sci U S A 2008; 105: 2266-2270.
67. McMahon MT, Gilad AA, DeLiso MA, Berman SM, Bulte JW, van Zijl PC,. New "multicolor" polypeptide diamagnetic chemical exchange saturation transfer (DIACEST) contrast agents for MRI. Magn Reson Med 2008; 60: 803-812.
68. Gilad AA, McMahon MT, Walczak P, Winnard PT Jr, Raman V, van Laarhoven HW, Skoglund CM, Bulte JW, van Zijl PC,. Artificial reporter gene providing MRI contrast based on proton exchange. Nat Biotechnol 2007; 25: 217-219.
69. Snoussi K, Bulte JW, Gueron M, van Zijl PC,. Sensitive CEST agents based on nucleic acid imino proton exchange: detection of poly(rU) and of a dendrimer-poly(rU) model for nucleic acid delivery and pharmacology. Magn Reson Med 2003; 49: 998-1005.
70. Powell JF, Strange R,. Biochemical changes occurring during the germination of bacterial spores. Biochem J 1953; 54: 205.
71. Keilin D, Hartree E,. Comparative study of spores and vegetative forms of Bacillus Subtilis. Antonie van Leeuwenhoek 1947; 12: 115-128.
72. Sunde EP, Setlow P, Hederstedt L, Halle B,. The physical state of water in bacterial spores. Proc Natl Acad Sci U S A 2009; 106: 19334-19339.
73. Plomp M, McCaffery JM, Cheong I, Huang X, Bettegowda C, Kinzler KW, Zhou S, Vogelstein B, Malkin AJ,. Spore coat architecture of Clostridium novyi NT spores. J Bacteriol 2007; 189: 6457-6468.
74. Sun PZ, Zhou J, Sun W, Huang J, van Zijl PCM,. Detection of the ischemic penumbra using pH-weighted MRI. J Cereb Blood Flow Metab 2006; 27: 1129-1136.
75. Song X, Gilad AA, Joel S, et al. CEST phase mapping using a length and offset varied saturation (LOVARS) scheme. Magn Reson Med 2012; 68: 1074-1086.
76. Terreno E, Stancanello J, Longo D, Castelli DD, Milone L, Sanders HM, Kok MB, Uggeri F, Aime S,. Methods for an improved detection of the MRI-CEST effect. Contrast Media Mol Imaging 2009; 4: 237-247.