Ci a ion: G ueso EM, Gi aldéz-Pé ez RM and P ado-Go o R. E ec o Gold Nanopa icle Agg ega ion on he
Kine ic Aspec o AuNPs/DNA In e ac ions. Aus in J Nanomed Nano echnol. 2021; 9(1): 1062.
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Abs ac
Since success ul he apy o cu ing cance and o he s gene ic diseases
equi es he anspo o DNA in o he cell by deli e y ehicles, he unde s anding
o he ac o s ha con ol he complexa ion and condensa ion o he DNA is
a key p oblem. Du ing he las decade, esea che s ha e de eloped some
uses o nanopa icles-DNA sys ems, he majo i y o hese s udies dealing
wi h nanopa icles (NPs), which a e co alen ly bound o he DNA. Howe e ,
he kine ic aspec o AuNPs/DNA sys em by non-co alen in e ac ions is less
explo ed. Mo eo e , he ole o high sal concen a ions in hese s udies is o
g ea in e es due o he majo i y o nanopa icles ha e a g ea endency o
agg ega e upon exposu e o biological medium, signi ican ly al e he up ake
ex en , a e, and mechanism o AuNPs/DNA in e ac ion. As a con ibu ion o
his ield, we ha e s udied kine ics aspec s o he binding o small iop onin gold
nanopa icles, AuNPs, o double s anded DNA in a high sal concen a ion
by using he s opped- low echnique. The kine ic cu es a e biexponen ial and
e eal he p esence o wo kine ic s eps. Mo eo e , AFM s udies e eal AuNPs
agg ega ion in he p esence o high sal con en , while he same pa icle a e
well-dispe sed in wa e . A wo-s ep se ies mechanism eac ion scheme was
p oposed. Acco ding o he eac ion scheme, he o ma ion o an in e media e
complex o med by agg ega ed gold nanopa icles and DNA p ecedes he a e-
de e mining s ep o he eac ion.
Keywo ds: DNA; Gold nanopa icles; Kine ic; AuNPs-agg ega ion
Resea ch A icle
E ec o Gold Nanopa icle Agg ega ion on he Kine ic
Aspec o AuNPs/DNA In e ac ions
G ueso EM1*, Gi aldéz-Pé ez RM2 and P ado-
Go o R1
1Uni e si y o Se ille, Depa men o Physical Chemis y,
Spain
2Uni e si y o Có doba, Facul y o Science, Depa men o
Cellula Biology, Physiology and Immunology, Spain
*Co esponding au ho : G ueso EM, Depa men o
Physical Chemis y, Uni e si y o Se ille, Spain; Email:
[email p o ec ed]
Recei ed: Feb ua y 05, 2021; Accep ed: Ma ch 03,
2021; Published: Ma ch 10, 2021
In oduc ion
The unde s anding and dealing o nanopa icle/DNA in e ac ions
has become an impo an eme ging a ea o esea ch due o he high
numbe o diagnos ic and he apeu ic applica ions de i ed om hese
sys ems [1-4]. In pa icula , he comp ehensi e s udy o DNA-AuNPs
a ini y in e ac ions ha e con ibu ed o he p omising challenge
o he use o hese sys ems o ea diseases, speci ically, he edi a y
diseases by he inse ion o genes in o he human cells is so called
gene he apy. Impo an ly, he gene ans ec ion s a egies need, as a
p e- equisi e, he e ec i e complexa ion and he collapse o ex ended
DNA chains in o compac DNA s uc u es [5]. O pa icula no e,
non-co alen in e ac ions be ween nanopa icles and DNA ha e been
ecognized o con ol physicochemical aspec s o he in e ac ion. In
his sense o each nanopa icle-DNA sys ems a global e ec is exe ed
in conjunc ion by bo h he me al clus e co e and he capping agen s
ha con ibu e o s abilize he nanosys em [6]. Rega ding he me al
clus e co e, especially elec os a ic in e ac ions [7,8], hyd ophobic
o ces [9], and he speci ic bonding be ween he chemical g oups o
DNA bases and he me al cen e con ol hese in e ac ions [10].
In ela ion o his, unde s anding he in e ac ions o agg ega es o
isola ed nanopa icles wi h DNA is de e minan o hei use in i o
deli e y o d ugs and e icacious nanomedicine design. In ac , he
explo a ion o new nanopa icle sys ems ha a e capable o changing
he agg ega ion s a e wi hin he physiological en i onmen cons i u es
an eme ging concep [11]. In a p e ious pape , he e ec o e anol on
he kine ic o agg ega ion o AuNPs/DNA was explo ed, e ealing
no only a change in he binding mode induced by he sol en bu also
on he mechanism o i s in e ac ion [12]. Howe e , he e ec o high
sal concen a ion on AuNPs/DNA mechanism is unexplo ed. Since
nanopa icles may agg ega e upon exposu e o biological medium,
due o he p esence o agg ega ion-inducing molecules/species
(such as sal ), explo ing e ec o high sal concen a ion on he
kine ic and he modynamic o AuNPs/DNA in e ac ions is a opic
o g ea in e es . In ac , he p esence o high sal concen a ion may
signi ican ly al e he up ake ex en , a e and mechanism o AuNPs/
DNA in e ac ion [13]. In a p e ious wo k, he in e ac ion o small
iop onin gold nanopa icles, Au@ iop onin, wi h DNA biopolyme
was e alua ed a e y low [NaCl] (0.001-0.015 M) [14]. The esul
demons a ed ha he kine ic esul s a e compa ible wi h a h ee-
s ep se ies mechanism eac ion scheme, in which he g oo e binding
in e ac ions o DNA and gold nanopa icles we e go e ned by
sol a ion and iscosi y ac o s [14]. In his s udy we ha e in es iga ed
he e ec o high sal concen a ions on he kine ic o Au@ iop onin
wi h DNA. In he p esen s udy, he simples mechanism consis en
wi h he kine ic esul s in ol es a mo e simple eac ion scheme wi h
wo-s ep eac ions. The i s s ep co esponds o a e y as s ep ha
is ela ed o a di usion con olled o ma ion o an ex e nal p ecu so
complex be ween agg ega ed gold nanopa icles and DNA. The
second s ep in ol es he o ma ion o an ex e nal complex, as a esul
o he binding a ini y be ween hyd ophilic g oups o he agg ega ed
iop onin nanopa icles and he DNA g oo es. As a summa y, his
s udy e eals ha kine ic o AuNPs/DNA in e ac ion is con olled
by AuNPs agg ega ion s a e, e ealing he impo ance o ake g ea
ca e in con ol o he sol en media o diagnos ic and he apeu ic
applica ions de i ed om hese sys ems.
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Ma e ials and Me hods
All chemicals we e o Anal. R. g ade and we e used wi hou
u he pu i ica ion. Hyd ogen e achlo oau ea e (III) ihyd a e,
3-Aminop opyl ie hoxilane (APTES), NaCl and BaClO4 we e
pu chased om Sigma-Ald ich; N-(2-me cap op opionyl)glycine
om Fluky; NaBH4 om Lancas e . Cal hymus DNA was
pu chased om Pha macia and used wi hou u he pu i ica ion,
because p elimina y expe imen s showed ha pu i ica ion does no
p oduce any changes in he expe imen al esul s. The abso bance
a io o DNA s ock solu ions a 260nm and 280nm was moni o ed
and ound o be be ween 1.8 and 1.9 (A260/A280 = 1.87), indica ing no
p o ein con amina ion [15]. An aga ose gel elec opho esis es using
e hidium b omide indica ed ha he a e age numbe o base pai s pe
DNA molecule is abo e 10,000 bp [16]. Polynucleo ide concen a ions
we e de e mined spec opho ome ically om he mola abso p i i y
(6600M-1cm-1 a 258nm in o de o ha e he DNA concen a ion
in phospha e uni s) [17]. Solu ions we e p epa ed wi h de-ionized
wa e , i s conduc i i y being less han 10-6Sm-1. Tiop onin gold
nanopa icles, Au@ iop onin we e syn hesized by using Temple on
e al.’s p ocedu e [18]. Gold nanopa icles we e cha ac e ized by
isible abso p ion spec a, TEM and mic oanalysis (11.8% C; 1.86%
H; 2.89% N; 5.80% S; Au 70.88%, C410H656O246N82S82Au197). A alue o
(1.6 ± 0.2) nm was ob ained o he diame e o he gold nanopa icle
in he absence o any added sal (Figu e 1). Acco ding o hese da a,
he ela ionship be ween he numbe o Au a oms and iop onin
ligands was 197/82.
Kine ics
The kine ic expe imen s we e pe o med a 298.0K by using a
Biologic SF 300 s opped- low ins umen and moni o ing he cou se
o he eac ion in he CD de ec ion mode. This de ec ion mode was
employed because he signal- o-noise a io was ound o be mo e
a o able compa ed o he abso bance mode. The acqui ed signal
was eco ded on a PC and hen analyzed by using he Jandell AISN
so wa e p og am. The Au@ iop onin concen a ion was 1.0×10-
6M in all expe imen s, and he DNA concen a ion was a ied.
All he kine ic expe imen s we e pe o med unde pseudo i s -
o de condi ions ([DNA] >10 [Au@ iop onin]). Each expe imen
was epea ed a leas 10 imes, and he ele an kine ic aces we e
accumula ed in o de o educe he signal- o-noise a io. The sp ead
o ime cons an s was ound o be wi hin 10%.
TEM measu emen s
Fo TEM isualiza ion, a single d op (10mL) o an AuNPs
aqueous solu ion was placed on a ca bon ilm coa ed coppe g id,
which was hen le o ai d y o 2 hou s a oom empe a u e. TEM
analysis was ca ied ou using a Philips CM 200 elec on mic oscope
wo king a 200kV, and he esul ing images we e analyzed by using
Image J ee so wa e.
Ci cula Dich oism (CD) spec a
Elec onic CD spec a we e eco ded using a BioLogic Mos-450
spec opola ime e . A s anda d qua z cell o 10mm pa h leng h was
used. The spec a we e exp essed in e ms o mola ellip ici y. Scans
we e aken om 220nm o 310nm o he in insic egion. Fo each
spec um, 5-10 uns we e a e aged a a cons an empe a u e o
25.0ºC, wi h a 5 min equilib a ion be o e each scan. All he spec a
we e eco ded a a ixed concen a ion o double-s anded DNA,
CDNA = 1.0×10-4M, and CNaCl = 0.50M.
AFM measu emen s
Images we e ob ained in ai and in apping mode using a
Molecula Imaging PicoPlus 2500 AFM (Agilen Technologies).
Silicon can ile e s (Model Poin p obe, Nanowo ld) wi h a esonance
equency o a ound 240kHz and a nominal o ce cons an o 42Nm-1
we e used. All AFM images we e eco ded wi h scan speeds o abou
0.5Hz, and da a we e collec ed in a 256×256 pixel o ma . Fo AFM
imaging o AuNPs in wa e and in he p esence o high sal , a 100
µL d ople o he sample was deposi ed on a eshly clea ed mica
su ace, which had been p e iously modi ied wi h 0.1% ( / ) APTES
solu ion, and incuba ed o 40 min. The su ace was hen washed wi h
ul apu e wa e and inally ai -d ied. All images p esen ed he e a e
he o iginal da a, excep ha a la en command was used o emo e
he backg ound slope [19].
Resul and Discussion
Small Au@ iop onin gold nanopa icles induce a con o ma ional
change in double s anded DNA upon binding which can be ollowed
by he ci cula dich oism echnique (Figu e 2). Double s anded
DNA shows a CD spec um cha ac e is ic o he igh -handed
B- o m in he a UV egion (220-320 nm). S uc u al al e a ions
o he biomolecule caused by i s in e ac ion wi h gold nanopa icles
as ligand a e e lec ed in changes in his in insic CD spec um.
Figu e 2 (black colou ) shows a CD spec um wi h he cha ac e is ic
ea u es o ds-DNA in B- o m, ha ing a posi i e peak a 278nm and
a nega i e peak a 247nm. These bands a ises by s acking in e ac ions
and he helical supe s uc u e o he polynucleo ide ha p o ide
an asymme ic en i onmen o he bases [20]. Upon he addi ion
o 5.0µM o Au@ iop onin gold nanopa icles o he DNA in wa e
solu ion, he mola ellip ici y dec eases a app oxima ely 278nm, and
inc eases a app oxima ely 247nm. These changes a e coupled wi h
Figu e 1: TEM image o Au@ iop onin gold nanopa icles in wa e solu ion
and he co esponding his og am o size dis ibu ion.
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a shi in he maximum wa eleng h o he posi i e band, indica ing
pa ial dena u a ion and he double helix unwinding (Figu e 2, g een
colou ) [14]. Howe e , he e ec o adding high sal concen a ion
in DNA s uc u e, bo h in he p esence and in he absence o gold
nanopa icles, is ho oughly di e en (Figu e 2, ed and blue colou ).
Namely, when CNaCl = 0.5M was added o he solu ion bo h bands
a e displaced o a lowe wa eleng h and a dec ease in he in ensi y
o posi i e band oge he wi h an inc ease in he in ensi y o he
nega i e CD band is egis e ed. No e ha his change in CD spec a
is compa ible wi h a con o ma ional change om B o C- o m o
DNA, which is in p og ess due o changes in sol en condi ions. In
ac , he con o ma ional change om B o C-DNA o m causes a
dec ease in a speci ic CD band as well as he p og essi e dehyd a ion
o DNA as sal concen a ion inc eases; hus, he sh inkage o he
double helix yields mo e condensed o packed DNA s uc u es [21].
I is impo an o no e ha inc easing in he size and dep h o he
majo g oo e, which accompanies his ansi ion, may be impo an
o he mode o binding ha iop onin gold nanopa icles expe ience
in i s in e ac ion wi h DNA [12]. In ac , Figu e 2 shows ha DNA
unde goes a less p onounced change in CD spec a, when CAu@ iop onin
= 5µM was added o he DNA solu ion, in he p esence o high sal
concen a ion. No e ha his beha io could be compa ible wi h an
ex e nal binding o gold nanopa icles o he biomolecule.
To explo e he e ec o adding high sal on Au@ iop onin
agg ega ion s a e, AFM expe imen s we e ca ied ou in he absence
and in he p esence o NaCl (Figu e 3). AFM measu emen s in wa e
e eal he p esence o isola ed Au@ iop onin (Figu e 3A-3B) wi h
a mean diame e o 1.6 ± 0.1 nm in z-di ec ion, in good ag eemen
wi h TEM measu emen s (Figu e 1). Howe e , AuNPs mo phology
is modi ied a CNaCl = 0.5M (Figu e 3C-3D), isualizing di e en
z-agg ega es wi h a mean diame e o 6.5 ± 1.6 nm, e ealing ha
an a e age o 4 nanopa icles cons i u es he agg ega e in sal . This
inding is ele an o possible biomedical applica ions o Au@
iop onin/DNA sys em. Thus, acco ding o Albanese e al. he
up ake pa e ns in di e en cell lines is di e en be ween single
and agg ega ed nanopa icles, e ealing he impo ance o AuNPs-
agg ega ion in media ing a ge ing and in acellula a icking [22].
As ega ds he kine ic s udy o Au@ iop onin binding o DNA
in he p esence o high sal concen a ion, he kine ic cu es we e
app op ia ely i ed by wo exponen ials, whose elaxa ion imes, τ1
and τ2, di e by abou 1 o de o magni ude. An example o a ypical
kine ic expe imen appea s in Figu e 4. The kine ic beha io o he
sys em can be a ionalized on he basis o he wo-s ep se ies model
depic ed in Scheme I:
DNA + (AuNPs)AGG ⇌ (DNA/(AuNPs)AGG)I ⇌ (DNA/(AuNPs)AGG)II
(I)
whe e (DNA/(AuNPs)AGG)I and (DNA/(AuNPs)AGG)I ep esen wo
di e en DNA-AuNPs complexes and (AuNPs)AGG co esponds
o he Au@ iop onin agg ega es o med a high sal con en . A
commen abou he change in he mechanism o in e ac ion o Au@
iop onin wi h DNA espec o he same sys em s udied in wa e and
low NaCl con en ( om 0 o 0.015 M) seems o be pe inen . Thus, he
h ee-s ep mechanism obse ed a low sal e ol es o a wo-s ep se ies
Figu e 2: CD spec a o Au@ iop onin/DNA sys ems in di e en expe imen al
condi ions, CDNA = 100µM in all he spec a. (A) CAu@ iop onin = 0.0µM and CNaCl
= 0.0M, black spec um; (B) CAu@ iop onin = 5.0µM and CNaCl = 0.0M, g een
spec um; (C) CAu@ iop onin = 0.0µM and CNaCl = 0.5M, blue spec um; (D) CAu@
iop onin = 5.0µM and CNaCl = 0.5M, ed spec um.
Figu e 3: AFM opog aphic images o Au@ iop onin gold nanopa icles in
wa e (A) and NaCl: 0.5M (C). Figu es B and D co espond o c oss sec ional
analysis o he heigh s along he selec ed lines o images (A) and (C),
espec i ely.
Figu e 4: Plo o ellip ici y s ime, , in a ypical kine ic expe imen . The do s
ep esen expe imen al alues, and he cu e is he bes i o he expe imen al
da a o a biexponen ial equa ion.
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mechanism when sal concen a ion inc eases [14]. In his s udy, he
dependence o he ecip ocal o he as elaxa ion ime, 1/τ1, on he
DNA concen a ion is linea , acco ding o eq. 1 [23].
1
1
1
DNA
k C k
τ
−
= × + (1)
The e o e, indi idual k1 and k-1 kine ic cons an s can be ob ained
om he plo o 1/τ1 e sus he DNA concen a ion. Examples o his
kind o plo a e shown in Figu e 5A and 6A in he p esence o 0.5M
o NaCl and BaClO4, espec i ely. Subsequen ly, once k1 and k-1 ha e
been ob ained om eq. 1, he alue o he indi idual equilib ium
binding cons an o he i s s ep, K1, is calcula ed as k1/k-1. Mo eo e ,
Figu e 5B and 6B show ha he dependence o he ecip ocal slow
elaxa ion ime, 1/τ2, on he DNA concen a ions is cu e and ends
o a pla eau in ag eemen wi h eq. 2 [23].
2 1 2
2 1
1
1
DNA
DNA
k K C k
K C
τ
−
×
= +
+ × (2)
The alue o K1 ob ained om equa ion 1 as k1/k-1 is in oduced
in o eq. 2 as a known pa ame e , while k2 and k-2 a e e alua ed by
da a i o eq. 2 (Figu e 5B and 6B). Subsequen ly, he alue o K2
is calcula ed as k2/k-2. Once indi idual kine ic and he modynamic
pa ame e s a e calcula ed, he alue o he global equilib ium binding
cons an is ob ained as ollow om K = K1×(1+K2); he eac ion
pa ame e s ob ained a e collec ed in (Table 1).
Conce ning he s abili y o he in e media e complex (DNA/
(AuNPs)AGG)I, i can be hypo hesized ha he binding could be
media ed undamen ally by non-elec os a ic in e ac ions in
acco dance wi h o he uncha ged ligand/DNA sys ems [16]. This is
due o in he p esen sys em and eac ion condi ion, Au@ iop onin
nanopa icles a e sligh ly anionic and hyd ophilic [14]; hus, he
elec os a ic in e ac ions could be neglec ed and he s abili y o he
ex e nal complex could be media ed by hyd ogen bonding be ween
he hyd ophilic g oups o he iop onin chain and he DNA bases.
Mo eo e , Table 1 shows ha k1 and k-1 dec eases as inc eases he
ionic s eng h in he media om NaCl 0.5M (I = 0.5M) o BaClO4
(I = 1.25M), which is in acco dance wi h he idea ha a p og essi e
dehyd a ion o he DNA occu in he ansi ion om B o C-like
o m as ionic s eng h inc eases. The e o e, his ac could hinde
he hyd ophilic in e ac ions ha a e needed o s abilize he (DNA/
(AuNPs)AGG)I complex as ionic s eng h inc eases.
On he o he hand, conce ning he a ia ions o k2 and k-2 wi h he
ionic s eng h, i could easonably suppose ha a eo ganiza ion o
he (DNA/(AuNPs)AGG)I complex o a mo e compac ed o m, (DNA/
(AuNPs)AGG)II, go e ns he a e-de e mining s ep o he eac ion
and i s e e se p ocess. No e ha he a ia ion endency o k2 and k2
wi h ionic s eng h is he opposi e han ha obse ed o k1 and k-1
indi idual cons an s. This inding highligh s ha he o ma ion o he
inal packed DNA/AuNPs s uc u es is a o ed a high ionic s eng h
due o he s a ing DNA con o ma ion is close o he inal condensed
s age.
Finally, i is wo hy o no e he alues ob ained o he global
equilib ium binding cons an , K = 3.47×104 and 4.0×103M-1, in he
Sal ype K ( M-1) K1 (M-1) K2k1 (M-1s-1) k-1 (s-1) k2 (s-1) k-2 (s-1)
[NaCl] = 0.5M 34.7×1033.0×10310.5 1.91×10563 1.3 0.12
[BaClO4] = 0.5M 4.0×1037.0×1024.7 2.05×10429 4.4 0.93
Table 1: Equilib ium and Ra e Cons an s o he In e ac ion o DNA wi h Au@ iop onin in he p esence o high sal concen a ions.
Figu e 5: Recip ocal as (1/τ1, A) and slow (1/τ2, B) elaxa ion imes
dependence on DNA concen a ion a 298.0K in he p esence o [NaCl] =
0.5M.
Figu e 6: Recip ocal as (1/τ1, A) and slow (1/τ2, B) elaxa ion imes
dependence on DNA concen a ion a 298.0K in he p esence o [BaClO4]
= 0.5M.
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p esence o 0.5M o NaCl and 0.5M BaClO4, espec i ely, a e g ea e
aking in o accoun he high sal condi ion. In ac , compa ing he
K alues o DNA/AuNPs sys em collec ed in (Table 1) wi h hose
ob ained o 1-PyCHO/DNA sys em, in which he dye is also o
neu al cha ac e as in he case o Au@ iop onin, (K = 1.0×104 a
0.5M o NaClO4 and 3.0×103 a 0.5M o BaClO4), i is ob ious ha
he o ma ion o DNA/AuNPs complexes is op imal a he selec ed
high ionic s eng h [24]. No e ha binding cons an s alues in he
104-106 ange, as ha ound he e a high NaCl con en , a e epo ed
as op imal o he complexa ion o he ligands and he consequen
elease once eached he a ge si e [25]. Speci ically, in he con ex
o cellula applica ions, i was demons a ed ha a high alue o he
DNA/AuNPs binding cons an would leads o be e in acellula
binding o he a ge molecule, he eby inc easing he e ec i eness o
an isense gene egula ion [26]. The a o able in e ac ion be ween Au@
iop onin and ds-DNA explo ed a high sal can he e o e suppo
he bioa ailabili y o he sys em in physiological en i onmen , o
possible medical applica ions.
Conclusion
De ails on he kine ic and he modynamic o he binding o small
iop onin gold nanopa icles o double s anded DNA in he p esence
o high sal ha e been he e p o ided h ough he use o s opped-
low and CD spec oscopic echniques. Mo eo e , he agg ega ion
s a e o nanopa icles was analyzed by using he ul asensi i e AFM
echnique. The p oposed mechanism consis en wi h analysis o he
da a p o ided in ol es a wo-s ep se ies eac ion scheme. In he i s
s ep, agg ega ed gold nanopa icles o ms an in e media e ex e nal
complex wi h DNA media ed by non-elec os a ic in e ac ion.
Then, in he second s ep, a mo e DNA/AuNPs packed s uc u e is
o med, which is a o ed kine ically a high ionic s eng h. On he
whole, we can say ha his s udy con ibu es o ob aining a deepe
comp ehension o he up ake pa e ns in cell in which he DNA/
AuNPs a e in ol ed. The change o binding mode and mechanism
ha DNA/AuNPs sys em unde go a high sal con en e eals he
impo ance o s udy AuNPs agg ega ion in media ing a ge ing and
in acellula a icking o DNA/AuNPs sys ems.
Acknowledgmen s
This wo k was inanced by he Uni e si y o Se ille, Spain V PP
USO SSGG (2019/00000570) and VI PP USO SSGG (2020/00001068).
The au ho s a e g a e ul o he Mic oscopy and Func ional
Cha ac e iza ion Se ice o he Resea ch, Technology and Inno a ion
Cen e o he Uni e si y o Se ille (CITIUS).
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