Preparation and biomedical application of a nonpolymer coated superparamagnetic nanoparticle

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1 RIGINAL RESEARCH Preprtion n iomeil pplition of nonpolymer ote superprmgneti nnoprtile Lin Du 1 Jinzho Chen 1 Ynting Qi 1 Dn Li 1 Chonggng Yun 1 Mrie C Lin 3 Dvi T Yew 4 HsingFu Kung 5 Jimmy C Yu 2 Lihui Li 1 1 Institute of Moleulr n Chemil Biology, Est Chin Norml University, Shnghi, Chin; 2 Deprtment of Chemistry, The Chinese University of Hong Kong, Hong Kong, Chin; 3 Deprtment of Chemistry, pen Lortory of Chemil Biology of the Institute of Moleulr Tehnology for Drug Disovery n Synthesis, The University of Hong Kong, Pokfulm, Hong Kong, Chin; 4 Deprtment of Antomy, Fulty of Meiine, The Chinese University of Hong Kong, Hong Kong, Chin; 5 Centre for Emerging Infetious Diseses, Fulty of Meiine, The Chinese University of Hong Kong, Chin Corresponene: Lihui Li Institute of Moleulr n Chemil Biology, Est Chin Norml University, N Zhongshn R., Shnghi 262, Chin Tel/Fx Emil Astrt: We report the preprtion of nonpolymer ote superprmgneti nnoprtile tht is stle n ioomptile oth in vitro n in vivo. The nonpolymer, etine, is nturl methylting gent in mmmlin liver with tive surfe property. Upon systemi ministrtion, the nnoprtile hs preferentil ioistriution in mmmlin liver n exhiits goo reution of relxivity time n negtive enhnement for the etetion of heptom noules in rts using MRI. ur t emonstrte tht the nonpolymer ote superprmgneti nnoprtile shoul hve potentil pplitions in iomeiine. Keywors: SPI nnoprtile, etine, heptom, MRI Introution The pplitions of superprmgneti iron oxie nnoprtiles (SPI) in iomeiine hve een tively pursue in reent yers (Wilkinson 23; Gupt n Gupt 25; Hu n Yu 26). However, reltively little work hs een rrie out on the nonpolymer ote superprmgneti nnoprtiles with entire size smller thn 1 nm. It hs een emonstrte tht the size of iron oxie prtile n the oting hve notle influene on its mgneti property, ellulr uptke n ell viility. Generlly speking, the nnoprtiles employe for in vivo pplitions shoul e suffiiently smll, stle t physiologil onition without ggregtion n present superprmgneti ehvior t room temperture. All SPI nnoprtiles presently unergoing prelinil or linil testing re ote with polymeri mteril (eg, extrn, roxyextrn, polyethylene glyol). Dextrn limits the tolerne of the ompoun, whih n therefore only e ministere s slow infusion (Pnym n Lhsetwr 23). In ft, ll polymers use, even the welltolerte polyethylene glyol, hve limittions in tissue istriution, penetrtion, metoli lerne n proue verse retions (Zhng et l 22). Reently, nonpolymer (itrte) ote superprmgneti nnoprtile hs een investigte in MR ngiogrphy (Shnorr et l 22; Tupitz et l 2; Wgner et l 22). Here we report nonpolymer ote SPI nnoprtile, whih hs n overll size roun 9 nm n is stle n ioomptile oth in vitro n in vivo. Following systemi ministrtion, the nnoprtile hs preferentil ioistriution in mmmlin liver n exhiits goo reution of relxivity time n negtive enhnement for the etetion of heptom noules in rt moel using mgneti resonne imging (MRI). The surfe hemistry of nnoprtiles is importnt for their potentil pplitions in iomeiine. In this report, we use etine s stilizing gent for the preprtion of SPI nnoprtiles. We hoose etine for this purpose se on the following onsiertions: (1) etine is moleule omprising mphiphili hrter, whih is stle over wie ph rnge in iologil onitions; (2) etine is nturl methylting gent in mmmlin liver, whih hs een foun to protet the livers of experimentl nimls Interntionl Journl of Nnomeiine 27:2(4) Dove Meil Press Limite. All rights reserve
2 Du et l ginst the heptotoxi ethnol n ron tetrhlorie; n (3) etine is n effetive hyrotrope with smll size, whih possesses welltolerte in tissue penetrtion n metoli lerne in vivo (Brk et l 1996). The im of this stuy is to generte etine ote SPI nnoprtile n investigte its potentil pplitions in vivo. ur preliminry t emonstrte tht the nonpolymer ote nnoprtile is useful s n MRI ontrst gent. Methos n results Preprtion n hrteriztion of SPI nnoprtiles For the preprtion of mgnetite nnoprtiles, 1 M FeCl 3.6H 2 (>99%) ws mixe with 2 M FeCl 2.4H 2 (>99%) t the rtio 2:1 n then 28.6% (w/w) Betine hyrohlorie (Fluk Biohemik) ws issolve in the solution y stirring. The ph of retion solution ws juste with the 3M NH until rehing ph vlue of 11. After stirring vigorously for 15 min, the solution ph ws juste to 4 y ing 2M HCl ropwise. The etine ote Fe 3 prtiles were ollete y mgneti seprtion y pplying permnent mgnet for 3 min n wshe with eionize wter three times. To remove exess ions n etine further, the prout ws ilyze ginst with eionize wter overnight. Following this, the solution ws entrifuge t 35 g t RT for 1 min. Finlly the prout ws psse though.22 μm filter n use for investigtions. Eletron mirogrphs of the mgnetite ispersions were rrie out using rop of the smple onto opper mesh ote with n morphous ron film. This mesh ws then rie in vuum esitor. TEM imges were performe using type JELJEMCXΙΙ with working onition kv. Figure 1 shows TEM imge of the iron oxie suspensions with wellisperse feture. Intensity nm θ/ _ CH 3 + CH 3 N CH 3 etine %Trnsmittne R 1 R1 R 1 R 1 R 1 R 2 R 2 + N N + H R H Wvenumers (m) Fe R=CH 13 R =CH CH 2 2 Fe Figure 1 Chrteriztion of the SPI nnoprtile. () TEM imge of the SPI nnoprtiles from the ssynthesize olloil suspensions following entrifugtion t 1, rpm, Br 5 nm, mgnifi tion 2,, () Xry power iffrtion ptterns of the SPI nnoprtiles, () FTIR spetrum of the SPI nnoprtiles, n () hemil struture of etine (ove) n the propose eletrostti intertion of the etine with Fe 3 (elow). 86 Interntionl Journl of Nnomeiine 27:2(4)
3 A nonpolymer ote SPI nnoprtile To hrterize the prouts further, prtil prouts were rie in vuum oven t 25 C for 12 h n use for Xry iffrtion (XRD) nlysis (Tupitz et l 22). XRD t were ollete on Rigku D/mx 255 V Xry iffrtometer employing CuK rition (λ = A t 4 kv n ma). Figure 1 isplys the XRD ptterns for the spreipitte powers orresponing to Figure 1. As mgnetite (Fe 3 ) my e onverte to mghemite (gmm Fe 2 3 ) in the presene of oxygen, it is possile tht the ore of the resulting nnoprtiles n onsist of mghemite s it hs een emonstrte reently (Thünemnn et l 26). The surfe properties were hrterize using FTIR. The iron oxie preipittes were rie n groun with KBr for IR mesurements y Nexus 67 FTIR spetrophotometer with resolution of 2 m 1. FTIR nlysis ws performe to hrterize the surfe nture of the resulting mgnetite nnoprtiles, s epite in Figure 1. A virtionl feture t 1628 m 1 is foun n ssigne to the C N strething motion, whih oul e erive from etine tht ws ote on Fe 3. The ro pek ppere in the region m 1 region orrespons to the H strething virtion s the iron oxie surfes re reily overe with hyroxyl groups in n queous environment (Cheng et l 25). The propose eletrostti intertion of the etine with Fe 3 ws shown in sheme in Figure 1. To investigte the mgneti properties of the SPI nnoprtile, mgnetiztion mesurements hve een me t 23 C with respet to the prtile size using virting smple mgnetometer (VSM, JDM13) t 18 e H 18 e. The superprmgneti ehvior of the SPI nnoprtile ws eviene y zero oerivity n remnene on the mgnetiztion loop n sturtion mgnetiztion of 56.8 emu/g ws etermine (Figure 2). The Fe 3 onentrtions were mesure y treting the iron oxies with nitri i n were lulte on the sis of the verge imeter of the iron oxie prtiles. Moreover,.3T NMR spetrometer with n extremity 5 m oil ws use for the r1; r2 mesurement of SPI nnoprtiles in the wter. The T1 n T2 mesurements were rrie out using the inversion reovery n CrrPurellMeioomGill (CPMG) sequenes, respetively. Smples were issolve into eionize wter n were nlyze for susequent etermintion of the r1 n r2 properties. The ommeril GDTPA ws lso nlyze for omprtive stuy. At onentrtion of.1 mm of the mgnetite prtiles, the longituinl relxtion time (T1) ws reue from 2117 ms for pure wter to 48 ms (Figure 2), while the T2 relxtion time ws reue from 239 to 18 ms (Figure 2). A omprison of T1 n T2 vlues of H 2, GDTPA n SPI tht were mesure using eh pulse for refousing in the multieho sequene is given in Tle 1. ur t emonstrte tht the SPI nnoprtile strongly reue oth T1 n T2 relxtion times with T2 signifintly lower thn T1. Therefore, this prtile my hve the potentil for MR imging s ontrst gent. Cytotoxiity evlution Cell lines inluing SMMC7721 n HL772 were ulture in DME meium supplemente with 1% fetl ovine serum, 2 mm lglutmine n 5 mg/ml gentmiin t ells/ well in 24well pltes t 37 C uner humiifie tmosphere of 95% ir n 5% C 2. After 24 h, the ells were pplie with seril 5fol ilutions of the SPI nnoprtile n GDTPA (Shering AG, Germny) in triplite with finl onentrtions rnging from.2 to 5 mm for 4 h. Following replenishment with fresh meium, the ells were inute for ition 48 h. Histohemistry nlysis ws rrie out with Prussin lue stining for the presene of iron. Figure Mgneti Fiel (ke) Signl (logrithmi sle) Signl (logrithmi sle) y =.22x R 2 = TI (ms) y =.93x R 2 = TE(ms) Figure 2 Mgneti properties of the SPI nnoprtile. The mgneti hysteresis loops of the prtile were mesure t room temperture n sturtion mgnetiztion of 56.8 emu/g ws etermine (). Both r1 n r2 of the SPI nnoprtile (.1 mm in the wter t 23 C) were evlute y.3 T MR imger. The longituinl relxtion time (T1) ws reue from 2117 ms for pure wter to 48 ms (), while the T2 relxtion time ws reue from 239 to 18 ms (). Inversionreovery ws prepre with vriety of inversion time from 1 to 5 ms n the CPMG spin eho with vriety of eho time from TE = 1 4 ms. Interntionl Journl of Nnomeiine 27:2(4) 87
4 Du et l Tle 1 A omprison of T 1 n T 2 vlues of GDTPA n the SPI prtile in wter, whih were mesure using eh pulse for refousing in the multieho sequene Regents T 1 T 2 H ms 239 ms GDTPA 63 ms 559 ms SPIN 48 ms 18 ms shows the viilities of oth SMMC7721 n HL772 ells expose to the ferrofluis t vrious iron onentrtions. Cell viility ws etermine y using the 5imethylthizol 2yl2, 5iphenyl tetrzolium romie (MTT) ssy. The ells use for this purpose were fixe with 3% formlehye n wshe with PBS, followe y the inution with 2% potssium ferroynie in 6% hyrohlori i for 3 min. After wsh, the ells were ounterstine with Giems solution. The viility of the ells ws expresse s the men ± S.E. of the perentge of sorne of ontrols where % equle viility of untrete ontrol ells. Prussin lue stining of the trnsfete ells showe the uptking of the SPI nnoprtiles in the ytoplsm () n no stining ws oserve in the ytoplsm of the ells trnsfete with GDTPA () n the notrnsfete SMMC7721 (). In ition, the SPI nnoprtiles were ministrte into the Wistr rts vi lterl til vein t ose 1mg/kg for hemolysis ssy (Weissleer et l 199). The numer n morphology of loo ells were evlute 24 h ltter (e n f) n the feek of the rts in the following 3 months ws exmine. These t strongly suggeste tht the SPI nnoprtile woul e generlly onsiere to e ioomptile. Mgneti resonne imging Animls were purhse from Shnghi SLAC lortory niml Co. LTD n heptom moel of rt ws evelope with DEN s esrie elsewhere (Mthew et l 198; Willims et l 1996). MRI exmintions were performe on 1.5 T GE tweenspee MR imger using ommerilly ville extremity 7.6 m oil. To evlute the potentil of the SPI nnoprtile in linil MR imging further, the signl intensity ltertions Tle 2 The relxivities of GDTPA n the SPI nnoprtile t the sme mgneti fi el strength Smples Mgneti fiel r1 r2 r2/r1 strength (T) L/mmol.se 1 (L/mmol.se 1 ) GDTPA SPIN influene y intertions etween nnoprtiles n wter or whole loo were nlyze using ifferent imging sequenes. Seril 1fol ilutions of the SPI nnoprtiles were prepre in the eionize wter n humn whole loo to the finl onentrtions, rnging from 1 2 to 1 7 M. The sme onentrtion grients of GDTPA were lso prepre for omprtive oservtion. 1.5 ml of eh preprtion ws loe into n rry of 1.5 ml Eppenorf tues in plsti rk. The imge ws tken using the esigne sequenes y 3 quisitions with the fiel of view eing 8 8 mm 2. The prmeters for T1 imge ws spin eho (SE) with repetition time (TR) 46 ms, eho time (TE) 9. ms in mtrix size of , for T2 imge ws fst spin eho (FSE) with TR/TE = 3 ms/7.1 ms, eho trin length (ET) = 17 ms in mtrix size of n for T2 weighte imge ws grient eho with TR/TE/flip ngle = 34 ms/17ms/ 3 in mtrix size of The signl intensity of eh smple ws etermine y stnr regionofinterest mesurements of ross setionl imge of eh iniviul tue using the provie imge quntifition tool. In Figure 4, the representtive imges from T1 (), T2 () n T2W () revele tht MR signl intensity ws ffete y the ion onentrtions of the two ontrst gents. The ispersion of the SPI nnoprtile in n rry of onentrtion grient of humn whole loo rnge from 1 2 to 1 5 M iron onentrtion showe signifint eresing of signl intensity t 1 3 M (), espeilly in T2 weighte MR imge. In vitro MR imges of SPI nnoprtiles were highly onsistent with the results of r1 n r2 mesurements esrie ove. For the pplition of the SPI nnoprtile to etet heptom noules, the rts were nesthetize for MR imging y mens of intrmusulr injetion of 5 mg/kg ketmine hyrohlorie n the ontrst meium ws injete into lterl til vein. As the USPI nnoprtiles hve prolonge loo hlflife, the SPI nnoprtiles were use the lst to voi ny resiul effet on the stuies when performe with the GDTPA. The prmeters for T1 imge ws spin eho (SE) with repetition time (TR) 46 ms, eho time (TE) 9. ms in mtrix size of , for T1 weighte imge ws SE with TR/TE = 42 ms/9. ms in mtrix size of , for T2 imge ws fst spin eho (FSE) with TR/TE = 3 ms/69.9 ms, eho trin length (ET) = 17 ms in mtrix size of n for T2 weighte imge ws grient eho with TR/TE/flip ngle = 34 ms/17 ms/ 3 in mtrix size of In ition, onentrtion of SPI nnoprtiles t.18 mmol Fe/kg ws employe for in vivo stuies, whih roughly orrespons to ose of.7 88 Interntionl Journl of Nnomeiine 27:2(4)
5 A nonpolymer ote SPI nnoprtile % Cell viility SPIN + SMMC7721 SPIN + HL772 GDTPA + SMMC7721 GDTPA + HL772 ontrol Iron onentrtion (mm) 2 SPIN Control 2 e 2 SPIN Control 2 Figure 3 Evlution of the ytotoxiity of the SPI nnoprtile oth in vitro n in vivo. Two humn hepti elllines were employe for MTT ssy (). Prussin lue stining of the trnsfete ells showe the uptking of the SPI nnoprtiles in the ytoplsm (), n no stining ws oserve in the ytoplsm of the ells trnsfete with GDTPA () n the notrnsfete SMMC7721 (). In ition, hemolysis ssy ws rrie out n no verse effets on re loo ells regring its numer n shpe 24h lter following systemi ministrtion of the nnoprtiles (1mg/kg) in rts (e, the ilution of isolte RBCs ws 1:2). ur results emonstrte tht the prepre SPI nnoprtile woul e ioomptile. mmol Fe/kg ssuming tht the loo volume is 7 ml/kg.w. in mmmls. This ose results in inresing T2 shortening, whih le to negtive enhnement or lkout of the liver (Figure 5). As result, the SPI nnoprtile ws use for MRI etetion of heptom noules roun 1mm in imeters in the liver of rts (Figure 5). In Figure 6, HCC lesions in rt liver showe low signl intensity on the T1weighte SE (Figures 6 n 6) n isointensive noules on the T2 weighte SE (Figures 6 n 6). All the MRI finings were further onfirme y neropsy n histologil exmintions. The GDTPA ws use for omprtive oservtion (Figures 6e n 6f). Disussion Betine is liverorn Senosylmethionine (SAM) genertor with tive surfe property. It hs een known Interntionl Journl of Nnomeiine 27:2(4) 89
6 Du et l SPIN T1 Signl Intensity (T1) SPIN T2W Signl Intensity (T2W) G T G T2W G SPIN Smple Iron Conentrtion (M) G SPIN Smple Iron Conentrtion (M) SPIN T2 Signl Intensity (T2) Signl Intensity T1 T2 T2W 25 G T T1 T2 T2W G SPIN Smple Iron Conentrtion (M) Smple Iron Conentrtion (M) 12 Figure 4 The signl intensity ltertions infl uene y intertions etween nnoprtiles n wter or whole loo were nlyze using ifferent imging sequenes. The smples were ilute in wter or humn whole loo t ifferent onentrtions. The representtive imges of Figures 1 n 1 were quire from T1 n T2 respetively. The T2 weighte MR signl intensity ws ffete y the ion onentrtions of the two ontrst gents (). The nnoprtile in humn whole loo rnge from 1 2 to 1 5 M. Signifi nt eresing of signl intensity t 1 3 M, espeilly in T2 weighte MR imge, ws oserve (). tht etine is involve in the retion of methionine metolism in mmmlin liver n it is promising lterntive to expensive SAM gent in the tretment of liver ysfuntion n other humn mlies (Brk et l 1996). Tking the vntge of etine s liverorn SAM genertor with tive surfe property, we hypothesize tht etine moifition oul hnge oth the physil n iologil properties of the nnoprtiles n therey woul offer improvement of their iosfety profiles n phrmokineti properties. There re two reent reports of nonpolymer ote SPI nnoprtiles. The VSPC91 (Ferrophrm, Teltow, Germny) ote with itrte monomer is hrterize y fvorle rtio of T2 relxivity (r2) to T1 relxivity (r1) in omintion with long loo pool hlflife (Reimer et l 1992; Chouly et l 1996). In nother stuy, SPI nnoprtile inorporte with (CH3)4N+ ws investigte using 1.5 T linil MR imger, in whih signifint reution of the kgroun meium signl ws foun in the T2weighte n the T2*weighte sequene in the serum n whole loo (Tupitz et l 22) in vitro. In our pproh, the SPI nnoprtiles were stilize y etine monomer n were systemtilly investigte oth in vitro n in vivo. Kineti stuies of the liver MR ontrst gents suggest tht hyrophoi surfe my enhne the uptke of the nnoprtiles y the liver, while hyrophili oting n surfe hrges my influene their retention perio in the irultion (Tupitz et l 2; Shnorr et l 22; Wgner et l 22). In this stuy, we foun tht the etine ote SPI nnoprtile presente signifint reution of the kgroun signl in the T2weighte sequene, whih le to equte performne in the etetion of heptom noules vrie 1 25 mm t low 81 Interntionl Journl of Nnomeiine 27:2(4)
7 A nonpolymer ote SPI nnoprtile e Figure 5 MR imge n histologil exmintion of heptom noule in rt moel. Following ministrtion of SPI nnoprtiles 45 min, MR imges for the lmost sme xil slie of the liver on the T1weighte SE () n on the T2weighte SE () were performe. n the T2weighte SE MR imge, the enhnement of negtive signls of liver n smll noules isointensive to liver ws foun. At neropsy 1h lter fter MRI, heptom noules were foun in the liver of rt (). Hemtoxylin stining of the resete prffin speimen from the rt showe wellifferentite heptom ells (), ompring with norml ontrols (e). The histologil results onfirme the MRI n neropsy finings further. SPIN T1 45 min SPIN T2 55 min SPIN T2 24h SPIN T2 24h GDTPA T1 5 min GDTPA T2 5 min e f Figure 6 MR imges of heptom lesions in rt liver. Following ministrtion of SPI nnoprtiles 45 min n 24 hours lter, the heptom noules were shown low signl intensity on the T1weighte SE ( n ), isointensive noules were foun on the T2weighte SE ( n ). The GDTPA ws use s ontrol (e n f). To voi ny resiul effet on the stuy, the SPI nnoprtiles were ministrte 48 hours lter following injetion of the ommeril GDTPA. Interntionl Journl of Nnomeiine 27:2(4) ose. In ition, the nnoprtiles frite in the wter phse hve itionl vntges over those synthesize in the orgni phse or those require itionl polymer protetion for stiliztion. This oul not only provie more physiologil retion kgroun for the tgge iomoleules, ut hve istint ioistriution n metoli lerne proﬁle thn the onventionl polymer ote prtiles. Moreover, etine moiﬁtion oul improve the iosfety proﬁles of the SPI nnoprtile n oul e promising SAM rrier for the tretment of some liver ysfuntion. Aknowlegments The uthors woul like to thnk Dr. Jinqi Li in Deprtment of Physis, Est Chin Norml University, Dr. Weijun Peng in Deprtment of Riology, Cner Hospitl of Fun University, for their ssistnt to performing MRI. This work ws supporte y Shnghi metropolitn fun for reserh n evelopment (4DZ145 n 4JC1496) n y key progrms of NSFC (34324). Author s Contriution Lin Du n Jinzho Chen Contriute eqully to this work. 811
8 Du et l Referenes Brk AJ, Bekenhuer HC, Tum DJ Betine, ethnol n the liver: review. Alohol, 13: Cheng Fu, Su CH, Yng YS, et l. 25. Chrteriztion of queous ispersions of Fe 3 nnoprtiles n their iomeil pplitions. Biomterils, 26: Chouly C, Pouliquen D, Luet I, et l Development of superprmgneti nnoprtiles for MRI: effet of prtile size, hrge n surfe nture on ioistriution. J Miroenpsul, 13: Gupt AK, Gupt M. 25. Synthesis n surfe engineering of iron oxie nnoprtiles for iomeil pplition. Biomteril, 26: Hu XL, Yu JC. 26. Mirowvessiste synthesis of superprmgneti surfefuntionlize porous Fe 3 /C nnoomposite. Chem Asin J, 1:65 1. Mthew T, Krunnithy R, Yee MH, et l Heptotoxiity of imethylformmie n imethylsulfoxie t n ove the levels use in some fltoxin stuies. L Invest, 42: Pnym J, Lhsetwr V. 23. Bioegrle nnoprtiles for rug n gene elivery to ells n tissue. Av Drug Del Rev, 55: Reimer P, Kwong KK, Weisskoff R, et l Dynmi signl intensity hnges in liver with superprmgneti MR ontrst gents. J Mgn Reson Imging, 2: Shnorr J, Wgner S, Pilgrimm H, et l. 22. Prelinil hrteriztion of monomerstilize very smll superprmgneti iron oxie prtiles (VSP) s loo pool ontrst meium for MR ngiogrphy. A Riol, 9(Suppl 2):S37 9. Tupitz M, Shnorr J, Armjuk A, et l. 2. New genertion of monomerstilize very smll superprmgneti iron oxie prtiles (vsop) s ontrst meium for ngiogrphy: prelinil results in rts n rits. Journl of Mgneti Resonne Imging, 12: Tupitz M, Shnorr J, Wgner S, et l. 22. Coronry MR ngiogrphy: experimentl results with monomer stilize loo pool ontrst meium. Riology, 222:12 6. Thünemnn AF, Shütt D, Kufner L, et l. 26. Mghemite nnoprtiles protetively ote with poly (ethyleneimine) n poly (ethylene oxie) lokpoly(glutmi i). Lngmuir, 22: Wgner S, Shnorr J, Pilgrimm H, et l. 22. Monomerote very smll superprmgneti iron oxie prtiles s ontrst meium for mgneti resonne imging: prelinil in vivo hrteriztion. Invest Riol, 37: Weissleer R, Elizono G, Wittenerg J, et l Ultrsmll superprmgneti iron oxie: hrteriztion of new lss of ontrst gents for MR imging. Riology, 175: Wilkinson JM. 23. Nnotehnology pplitions in meiine. Me Devie Tehnol, 14: Willims GM, Itropoulos MJ, Wng CX, et l Diethylnitrosmine exposureresponses for DNA mge, entriloulr ytotoxiity, ell prolifertion n rinogenesis in rt liver exhiit some nonlinerities. Crinogenesis, 1: Zhng Y, Kohler N, Zhng M. 22. Surfe moifition of superprmgneti mgnetite nnoprtiles n their intrellulr uptke. Biomterils, 23: Interntionl Journl of Nnomeiine 27:2(4)
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