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Proteomic Analysis of a Bioactive Aloe vera Extract

Article in Current Proteomics · September 2018

DOI: 10.2174/1570164615666180925150839

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Current Proteomics, 2019, 16, 000-000 1

RESEARCH ARTICLE

Proteomic Analysis of a Bioactive Aloe vera Extract

Ethel Daniela Cabello-Ruiz1, Víctor Manuel Torres-de la Cruz2,3,*, Catalina Rivas-Morales1,

Gloria María Molina-Salinas4, María Adriana Núñez-González1, María Julia Verde-Star1 and
Catalina Leos-Rivas1

1
Facultad de Ciencias Biológicas, Universidad Autónoma de Nuevo León; 2Unidad de Investigación Médica Yucatán,
Unidad Médica de Alta Especialidad Hospital de Especialidades 1 Mérida, Yucatán, Instituto Mexicano del Seguro So-
cial, México; 3Centro de Investigación Biomédica del Noreste, Instituto Mexicano del Seguro Social, Monterrey, Nuevo
León, México; 4Departamento de Genética, Facultad de Medicina, Universidad Autónoma de Nuevo León, México

ARTICLE HISTORY
Received: October 14, 2017
Revised: December 09, 2017
Accepted: September 11, 2018
DOI:
10.2174/1570164615666180925150839
Abstract: Background: Aloe vera, a plant belonging to the family Xanthorrhoeaceae, has received
special interest in recent years, not only for the commercial importance of its derivatives, but also be-
cause of the identification of new molecules from this plant. The latter may provide a scientific support
for ethnobotany, which has been beneficial to mankind for centuries.
Objective: Recently, the pharmacological activity of proteins derived from natural sources, including
plants, is being explored. We report on the extraction and identification of proteins from A. vera with
antimicrobial activity.
Result: The protein extract (yield, 0.15%) contained 15 peptides or proteins, whose sequences were as-
sociated with membrane proteins, enzymes, and proteins involved in stress tolerance and defense
against pathogens. The latter is consistent with the previously reported antimicrobial activity of an
A. vera protein extract.

Keywords: Aloe vera, extraction, protein, antimicrobial.

1. INTRODUCTION
Pre-hispanic knowledge on the healing power of plants
has been transmitted from generation to generation and
forms the basis of traditional medicine, which is still widely
practiced in Mexico. Whereas the history of traditional
medicine dates back thousands of years, modern medicine
has a relatively short existence of about a hundred years.
However, the combination of traditional with modern medi-
cine may provide more effective treatments than either one
on itself [1]. Indeed, the search for active substances in
plants used in traditional medicine has led to the discovery of
new molecules. Some of these molecules have been included
in the collection of modern pharmacological formulations
and their working mechanisms have been elucidated [2].
Use of plants for nutritional and medicinal purposes is
common among members of the large family of Liliaceae
*Address correspondence to this author at the Genetic Department of Medi-
cine School of Universidad Autónoma de Nuevo León, Zip code 64460,
México; Tel: 52+ (81) 8329 4154; E-mail: torresv84@hotmail.com
sensu lato, and A. vera is among its most well-known and
well-studied species. In traditional Hindu medicine, A. vera
is used in the treatment against gastrointestinal and derma-
tological problems. Furthermore, it provides a rapid relief in
case of minor burns and wounds because of its anti-
inflammatory and skin regenerating effects [3]. In Mexico,
A. vera is also used to treat cough, diabetes, erysipelas,
stomachache, skin inflammation and infections, and as an
anti-helminthic [4]. These applications reflect the numerous
pharmacological activities attributed to this plant, such as:
anti-inflammatory, immunomodulatory, skin regenerative,
antitumor, antimicrobial, antihelminthic, antidiabetic, antiul-
cer, and hepatoprotective, amongst others [5]. A. vera has
also been considered a “natural” ingredient in the modern
Food and Drugs Industry. Considering the wide variety of
effects of A. vera, there has been an effort to identify the
responsible bioactive substances. As a result, various secon-
dary metabolites (flavonoids, terpenoids, cholesterol deriva-
tives, anthraquinones, and saccharides) have been described
[6]. A more recent tendency is the quest for plant-derived
proteins, and A. vera has not been exempted. The contrary,
three interesting lectins have been found: a 35-kDa lectin

1570-1646/19 $58.00+.00 © 2019 Bentham Science Publishers

2 Current Proteomics, 2019, Vol. 16, No. 0 Cabello-Ruiz et al.

with lymphoproliferative activity [7] and two immunomodu-
latory lectines, aloptine A (7.5 kDa) and aloptine B (24 kDa)
[8]. Furthermore, three glycoproteins have been described:
aloectine A with antitumoral and antiulcer effects, a 29-kDa
substance that stimulates the proliferation of human dermal
cells [9], and G1G1M1DI2, a 5.5-kDa molecule that stimu-
lates mitosis and cellular migration [10]. In addition, an oc-
tapeptide with antitumoral and antioxidant activities [11] and
a 14-kDa protein with antifungic activity against Candida
paraprilosis, C. krusei and C. albicans have been reported
[12]. Similarly, we previously reported that the protein frac-
tion of a lyophilized gel of A. vera had antimicrobial activity
against C. albicans and Staphylococcus aureus [13]. Here,
we aimed to identify the components in this protein extract
(PE) by means of quantitative time-of-fligh mass spectrome-
try (qTOF-MS) coupled to bidimensional nanochromatogra-
phy.
2. MATERIALS Y METHODS
2.1. Extraction and Purification of the Protein Extract of
an A. vera gel
A. vera gel was kindly provided by Aloe Jaumave® (Jau-
mave, Tamps. Mex). The PE of the lyophilized gel was ob-
tained from a phenol-based extraction process followed by
cleaning a concentration through 3-kDa membranes accord-
ing Cabello et al. (2015) [13]. A total of 15 extractions was
obtained, each fraction was analyzed following the next pro-
cedure.
Waters corp, MA, USA) as a trap column; the low pH sepa-
ration utilized a gradient with 0.1% formic acid and 0% to
42% ACN, and an analytical column (1.7 µ, 75 µ x 25 cm);
column temperature, 40ºC. The system was connected to the
nanoelectroSpray interface. The injection volume was 1.0
µL, each sample was online fractioned at 6 fractions and
during the run was infused the lock mass at 200 fmol/µL at
1.0 µl/min with a 10 mL Hamilton syringe.
2.5. Data Processing
All fractions were analyzed with a Cuadrupole Time of
Flight spectrometer q-TOF Premier XE instrument of Waters
Corp and Masslynx v4.1 software using MSe experiment with
a ramp of energy of 12 to 40V, 10,000 of resolution in V way
and a nanolockSpray with infusion of Glu-fibrinopeptide
monitoring 785.8427 of mass charge ratio value and ex-
ported to be processed by ProteinLinx Global Server v3.0
software using the MASCOT parser v2.4.0.0 (Copyrigth@
Matrix Science 1999-2011) and the Arabidopsis thaliana
data base, downloaded from Uniprot web site(accessed
March 2016) with 89,239 entries and saved as local in PLGS
in Fasta format.
The parameters of data processing include:
Apex3D Parameters
Atribute Value
TOF resolution 10,000

LockSpray tolerance 0.1 Da

2.2. Fractioning and Concentration of the PE
Low energy Threshold 20 counts
The PE was resuspended in 100 µL NH4HCO3 (100
mM); 50 µL was separated and analyzed by HPLC (Waters Elevated energy Threshold 10 counts
Alliance 2695 XE) using an Atlantis C18 column (5µm, 4.6 Intensity Threshold 100 counts
x 75 mm) at a column temperature of 45oC, and a 95/5
H2O/acetonitrile (ACN) gradient; analysis time, 25 min. Pro- The work flow parameters are as follows:
teins were detected at 280 nm with a photodiode array detec-
tor (Water modelo 996). The recovered protein fractions Mode: ElectroSpray MSe , Databank Search Query
were concentrated till a near-dry state in a CENTRIVAP
(Labconco, KS, USA), and stored in 100 µL 100 mM Atribute Value
NH4HCO3 until use.
Peptide tolerance automatic

2.3. Trypsin Digestion of the PE Fragment tolerance automatic

The PE (100 µL of a 1.0 mg/mL solution, i.e. 100 µg) was Min ion fragment match per peptide 3
incubated with 5 µL dithiothreitol (DTT; reducing agent) at
Min ion match per protein 7
65ºC for 45 min. After the additon of 20 µL iodoacetamide
(derivatizing agent), incubation was continued for another 45 Min peptides matches per protein 3
min in the dark before being stopped by adding 20 µL DTT
(45 min). Next, the PE was enzymatically digested with 5 µL Monoisotopic or average Monoisotopic
trypsin (PROMEGA®; 1.0 µg/mL) at 37ºC for 16 h. 10 µL Charge +1
trifluoroacetic acid (TFA) was added to stop the reaction and
the sample was centrifuged for 10 min. at 1062 x G/10 min.
3. RESULTS AND DISCUSSION
2.4. 2D-chromatographic Separation of the PE
The mean protein yield of 15 extractions with phenol was
The nanoACQUITY UPLC® system with 2D technology 14.9 mg/mL (SD ± 1.24), and each sample was fractioned in
(Waters corp, MA, USA) was used in the 2D on-line with six and showed in the complementary information. Fifteen
dilution modality. A high pH separation was accomplished proteins were identified in the A. vera PE with antimicrobial
with a gradient of 20 mM ammonium formate and 0% to 42% activity against S. aureus y C. albicans [13]. The high qual-
ACN using a Symmetry C18 column (5 µ, 150 µ x 2 cm; ity of the obtained spectra showned good sensitivity and low
Proteomic Analysis of a Bioactive Aloe vera Extract Current Proteomics, 2019, Vol. 16, No. 0 3

(Fig. 1) Contd….
4 Current Proteomics, 2019, Vol. 16, No. 0 Cabello-Ruiz et al.

Fig. (1). Demonstrative information about the protein identification in the extract of the gel leave of Aloe vera.

noise to detect parents ions and fragments and we showed in
Fig. (1). After sequencing the proteins, three sequences (Ta-
ble 1; P5, P8, and P12) could not be associated with any ac-
tivity or organism [14]. This requires further research to an-
notate function or similarity to proteins in other organisms.
Three other proteins could not be characterized with Arabi-
dopsis thaliana (Table 1; P1, P7, and P10). P1 presents simi-
larity with a protein of Brassica rapa, with an unknown
function. P7 is not homologous with any reported sequence,
and as such, of unknown activity. P10 on the other hand,
presents similarity with proteins from different organisms, A.
lyrata, Brassica rapa, Vitis vinífera, Sorghum bicolor, Zea
mays, and Oryza sativa Japonica amongst others, but no
function has been attributed to any of them [15].
Proteomic Analysis of a Bioactive Aloe vera Extract Current Proteomics, 2019, Vol. 16, No. 0 5

Table 1. Sequences identified in the Aloe vera PE with similarities to reported proteins.

Confidence
Accession Protein Name Organism pI Mw Score Peptides Coverage Products
%

P1 A0MDU1 Putative uncharacterized Arabbidosis thaliana 4.5 8586 439.9 5 46.5 100 39

Photosystem II reaction
P2 P62109 Arabbidosis thaliana 4.1 3780 447.7 4 100 100 26
center

P3 Q19EC5 RPP1 Disease resistence Arabbidosis thaliana 4.6 44943 203.6 9 47.8 99 102

P4 Q8L3T0 PLAC8 Family protein Arabbidosis thaliana 4.7 27245 258.2 5 48.8 95 15

P5 Q9M237 Uncharacterized Arabbidosis thaliana 4.9 69221 316.7 31 40.3 95 143

ARATH 4-Substituted
P6 Q9LYU4 benzoates-Glutamate Arabbidosis thaliana 4.7 65086 208.9 10 37 95 44
ligase

P7 B3H5A2 Uncharacterized Arabbidosis thaliana 4.1 25695 334.6 15 53.2 100 67

P8 Q9LD59 Putative uncharacterized Arabbidosis thaliana 4.7 82930 303.2 35 40.8 95 180

P9 Q9FGA6 ARATH AT5G50050 OS Arabbidosis thaliana 4.7 18642 205.7 5 58.3 92 35

P10 B3H569 Uncharacterized Arabbidosis thaliana 4.4 17475 246.8 3 26.0 90 14

P11 Q0WNN2 Putative Cytosolic factor Arabbidosis thaliana 4.4 15602 214.0 5 35.5 95 25

P12 O64570 Putative uncharacterized Arabbidosis thaliana 11.6 13775 421.9 6 58.8 99 28

Inner membrane protein

P13 F4IJM1 Arabbidosis thaliana 9.7 47042 135.4 12 53.0 99 52
ALBINO3

P14 F4JZA2 ATP/ADP Transporter Arabbidosis thaliana 9.7 50541 174.4 12 51.0 99 58

Protein sensitive to proton

P15 Q2V4J0 Arabbidosis thaliana 6.6 38803 205.5 10 38.6 100 60
rhizotoxicity 1

A probable biological significance was found for the re-
maining nine sequences (Table 1). P2 was recognized as the
photosystem II reaction center protein M [15]. As such, the
protein is part of a complex of proteins, pigments and cofac-
tors that provides the plant with energy by means of photo-
synthesis [16]. Balsera et al. (2004) [17] reported a subunit
M protein of the photosystem II from Spinacia oleracea.
Though no function could be attributed to the 3.8-kDa pro-
tein, it seemed important to form photosystem II dimers in-
volved in electron transfer processes.
The P4 sequence seemed to belong to the PLAC8 motif-
containing family (Table 1). This large family occurs in
various eukaryotic kingdoms, including fungi, green algae,
plants, and animals [15]. Proteins of this family tend to be
integral membrane proteins with two membrane-spanning α-
helices. Often, the function of PLAC8-containing proteins is
unknown, but in plants they are involved with the control of
the number of cells in fruits [18] or as cations transporters.
So far, PLAC8-containing proteins have not been reported in
A. vera.
The P11 sequence had similarities with the PATL1 pro-
tein (Table 1), which is involved in the transport of hydro-
phobic molecules across membranes of different cell com-
partments. Furthermore, PATL1 proteins are important for
the formation of the cell plate during plant cytokinesis [19].
Based on the results of a genome study of A. thaliana, it has
been suggested that PATL1 is recluted from the cytoplasm to
the expanding and maturing cell plate and binds phosphoi-
nositides required for the process [20].
The P14 sequence has similarites with a membranal ATP/
ADP transporter (Table 1) [15]. A. vera may use these trans-
porters to compensate its limited capacity to syntesize nu-
cleotides. Indeed, the same protein, composed of 2 isomers
(AtNTT1 y AtNTT2), has been reported in A. thaliana.
Plants without these transporters not only develop more
slowly, but also displayed a chlorotic phenotype and sponta-
neous necrotic lesions [21].
The P6 sequence was associated with PBS3, an enzyme
that catalyzes the conjugation of specific amino acids (Glu,
and possibly, His, Lys, and Met) to their preferred acyl sub-
strates [15]. In A. thaliana, PBS3 allowed for plant growth
despite the presence of a highly virulent strain of Pseudo-
monas syringae, indicating that PBS3 has a function in the
restriction of the spreading of virulent pathogens [22]. It is
therefore deduced that A. vera produces this protein as a de-
fense response. So far, the A. vera PE has not been tested for
antimicrobial activity against P. syringae. Thus, it is neces-
sary to verify whether the A. vera PE extract has antimicro-
bial activity against P. syringae. Furthermore, it should be
6 Current Proteomics, 2019, Vol. 16, No. 0 Cabello-Ruiz et al.

verified whether the P6 sequence is responsible for the an- teins were identified. Proteins that seemed membrane-
timicrobial activity against different microbes. associated (P2, P4, P11, P13, and P14) were supposed to be
involved in the transfer of electrons (light absorption), ions,
The P9 sequence (Table 1) was related to the enzyme hydrophobic substances, and ATP/ADP, chaperoning pro-
pectin methylesterase/invertase [15]. This enzyme has a do- teins into membranes, as well as in the physiological devel-
main that is involved in the regulation of carbohydrate me- opment of plants (regulation of cell number determines fruit
tabolism, cell wall growth, and fruit development. Enzyme size). Besides, a sequence was similar to a protein (P15) in-
activity has been reported in root development, stem length- volved in stress tolerance in acid soils. Finally, three se-
ening, and fruit maturation. Besides, it has been suggested to quences were identified that seemed to be involved in de-
have antimicrobial activity [23]. The protein is also impli- fense against pathogens (P3, P6, and P9), therefore A. vera
cated in plant-pathogen interactions as it functions as a re- may be a promising new source of antimicrobial agents.
ceptor for pathogens as has been reported for the tobacco
mosaic virus [24]. Altogether, it seems that A. vera produces
LIST OF ABREVIATIONS
this enzyme for growth and defense purposes. Therefore, the
P9 sequence might have been responsible for antimicrobial ACN = Acetonitrile
activity of the A. vera PE. Confirmation studies similar to the
ones mentioned for the P6 sequence are required. ATP = Adenosine triphosphateADP.- Adenosine
diphosphate
The P13 sequence has similarities with the membrane
insertase like ALB3 (Table 1), which is present in the thy- kDa = Kilo Daltons
lakoid membrane of chloroplasts with a function homolo- MASCOT = Matrix Science database
gous to Oxa1p of the external membranes of mitochondria
[25]. ALB3 functions as a thylakoid membrane insertase for q-TOF-MS = Ortogonal Time if flight Mass Spectrome-
light-harvesting complex proteins (LHCP). ALB4, an ALB3 try
homolog in Arabidopsis was thought to participate in the
stabilization of the ATP synthase complex. However, it has ETHICS APPROVAL AND CONSENT TO PARTICI-
been demonstrated that ALB3 and ALB4 share significant PATE
functional overlap and that both are needed for the insertion Not applicable.
of cytochrome F in membranes (Trösch et al., 2015) [26].
Furthermore, the P3 sequence has similarities with a HUMAN AND ANIMAL RIGHTS
pathogen-resistance protein of the Toll/Interleukin 1 recep- No Animals/Humans were used for studies that are the
tor, nucleotide-binding site, leucine-rich repeat (TIR-NBS- basis of this research.
LRR) type (Table 1), [15]. So far, this is the first report of
this plant disease resistance protein in A. vera, though TIR-
CONSENT FOR PUBLICATION
NBS-LRRs had been reported in other plants such as the
tabacco plant (against the tabacco mosaic virus), flax Not applicable.
(against the fungus Melampsora lini), and Arabidopsis
(against the fungus Peronospora parasítica). The mentioned CONFLICT OF INTEREST
plant pathogens are not related to the pathogens to which the
A. vera PE has antimicrobial activity, but, considering that EDCR received a postgraduate grant from CONACYT
TIR-NBS-LRR is a non-specific pathogen resistance protein, (393911). The authors thank the Fundación Educación Supe-
it may be assumed that it has the same effect against the mi- rior-Empresa (FESE) and Aloe Jaumave S.A. de C.V. for
crobes inhibited by the A. vera PE. project support.
Finally, the P15 sequence seemed related to sensitive-to- ACKNOWLEDGEMENTS
proton rhizotoxicity1 (STOP1; 499 amino acids), a zinc-
finger tanscription factor that controls the expression of All the authors, contributors and acknowledged and a
genes (f.e. ALMT1 and MATE) in response to acid stress, special thank to Dra Laura E. Martínez for allowing the use
like protons (H+) and aluminum (Al3+) [15]. Hoekenga et al. of the proteomic laboratory facilities of the Genetic depart-
(2006) [27] suggest that STOP1 is important for aluminum ment.
tolerance in Arabidopsis. A transcriptome analysis revealed
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