Interactions between corn starch and lingonberry polyphenols and their effects on starch digestion and glucose transport

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International Journal of Biological Macromolecules 271 (2024) 132444

Available online 24 May 2024

Interactions between corn starch and lingonberry polyphenols and their

effects on starch digestion and glucose transport

Fengfeng Li

, Xinhua Zhang

, Xu Liu

, Jing Zhang

, Dandan Zang

, Xiuling Zhang

Meili Shao

College of Food Science, Northeast Agricultural University, Harbin, Heilongjiang 150030, China

Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Harbin, Heilongjiang 150081, China

ARTICLE INFO

Keywords:

Corn starch

Polyphenols

Lingonberry

Interaction

Starch digestion

Glucose transport

ABSTRACT

This study investigated the interaction mechanism between corn starch (CS) and lingonberry polyphenols (LBP)

during starch gelatinization, focusing on their effects on starch structure and physicochemical properties.

Moreover, it explored the effect of this interaction on starch digestion and glucose transport. The results indi-

cated that LBP interacted non-covalently with CS during starch gelatinization, disrupted the short-range ordered

structure of starch, decreased gelatinization enthalpy of starch, and formed a dense network structure.

Furthermore, the incorporation of LBP remarkably reduced the digestibility of CS. In particular, the addition of

10 % LBP decreased the terminal digestibility (C∞) from 77.87 % to 60.43 % and increased the amount of

resistant starch (RS) by 21.63 %. LBP was found to inhibit

-amylase and

-glucosidase in a mixed manner.

Additionally, LBP inhibited glucose transport in Caco-2 cells following starch digestion. When 10 % LBP was

added, there was a 34.17 % decrease in glucose transport compared with starch digestion without LBP. This

study helps establish the foundation for the development of LBP-containing starch or starch-based healthy foods

and provides new insights into the mechanism by which LBP lowers blood glucose.

1. Introduction

Corn is a globally signicant crop, and its main component is corn

starch (CS). As an essential dietary energy source, starch is closely

related to postprandial blood sugar levels during digestion and uptake

[1]. Notably, postprandial hyperglycemia is a precursor of developing

type 2 diabetes [2]. As of 2021, approximately 536.6 million people

(10.5 %) aged 20–79 years had diabetes worldwide. This number is

expected to increase to 12.2 % (equivalent to 783.2 million individuals)

by 2045 [3,4]. Therefore, understanding and regulating starch digestion

and absorption are critical to ght against the global epidemic of type 2

diabetes.

Polyphenols have been identied as potent regulators of starch

digestion and absorption, which reduce postprandial blood glucose

levels [5,6]. On the one hand, polyphenols reduce starch digestion by

changing the structure and physicochemical properties of starch and

inhibiting

-amylase and

-glucosidase [7,8]. Interactions between

polyphenols and starch can form inclusion and noninclusion complexes

[9]. The inclusion complexes with specic V-shaped crystal patterns will

assemble when polyphenols are integrated into the hydrophobic cavity

of the starch molecule through hydrophobic interactions, which con-

tributes to the production of resistant starch, thus inducing a decrease in

starch digestibility [10]. For noninclusion complexes, hydrogen

bonding, hydrophobicity, electrostatic and ionic interactions are mainly

involved among polyphenols and starch [11]. These complexes usually

do not affect the crystal structure of starch, and their main effect is to

inhibit the binding of digestive enzymes to starch, which leads to a

slowing down of the digestive process [12]. On the other hand, Poly-

phenols inhibit glucose transport in the small intestine by targeting

glucose transporter proteins, thereby affecting starch absorption

[13,14]. Therefore, exploring phenolic substances for ‘green’ modica-

tion of starch is necessary [15]. Lingonberry (Vaccinium vitis-idaea L.) is a

rich source of phenolic compounds, and previous studies have reported

that lingonberry polyphenols (LBP) reduce blood glucose levels and

exhibit antidiabetic activity [16–18]. However, to our knowledge,

whether LBP can lower blood glucose by interacting with starch and

inhibiting digestive enzymes and glucose transport is unknown.

This study aimed to investigate the interactions between CS and LBP

* Corresponding authors.

E-mail addresses: zhangxiuling1968@126.com (X. Zhang), shml0915@163.com (M. Shao).

Contents lists available at ScienceDirect

International Journal of Biological Macromolecules

journal homepage: www.elsevier.com/locate/ijbiomac

https://doi.org/10.1016/j.ijbiomac.2024.132444

Received 4 August 2023; Received in revised form 6 April 2024; Accepted 15 May 2024

International Journal of Biological Macromolecules 271 (2024) 132444

and analyze the effects of these interactions on starch digestion and

glucose transport. First, is the interaction of LBP with CS, focusing on

changes in starch structure and physicochemical properties including

iodine-binding capacity, Fourier transforms infrared spectroscopy

(FTIR), X-ray diffraction (XRD), thermal properties (differential scan-

ning calorimetry, DSC), rheology, scanning electron microscope (SEM)

and confocal laser scanning microscopy (CLSM). Next, the effects of LBP

on CS digestibility and inhibition of starch digestive enzymes (

-amylase

and

-glucosidase) were evaluated. Finally, the effect of LBP on glucose

transport after starch digestion was investigated using the Caco-2

monolayer cell model. This study contributes to the development of

low glycemic index (GI) LBP starch-based foods and provides a theo-

retical basis for the industrial production of polyphenol–starch coexis-

tence systems.

2. Materials and methods

2.1. Materials

Lingonberry fruits were purchased from Gaotai Food Co., Ltd.

(Harbin, China). Corn starch (CS) (99 % purity) was purchased from

Yuanye Biotechnology Co., Ltd. (Shanghai, China).

-glucosidase (from

Saccharomyce cerevisiae) (EC 3.2.1.20) was purchased from Sigma-

Aldrich Shanghai Trading Co., Ltd. (Shanghai, China).

-amylase

(from porcine pancreas) was purchased from Yuanye Biotechnology Co.,

Ltd. (Shanghai, China), and uorescein 5-isothiocyanate (FITC) and

rhodamine B were purchased from Beijing Solarbio Technology Co., Ltd.

(Beijing, China). A glucose oxidase kit (GOPOD) was obtained from

Jiancheng Institute of Bioengineering (Nanjing, China). Caco-2 cells

were obtained from the Institute of Cells, Chinese Academy of Science.

2.2. Preparation of LBP

The extraction of LBP was performed according to the procedure of

Wang, Zhu, Meng, Liu, Mu and Ning [19] with some modications. First,

200 g of lingonberry fruits were crushed using a blender. The crushed

fruits were then subjected to ultrasound-assisted extraction with 2 L of

80 % (v/v) aqueous ethanol at 250 W for 1.5 h at 40 ◦C. The resulting

mixture was centrifuged (4000 rpm, 10 min) and then concentrated at

40 ◦C using a vacuum rotary evaporator (RE-5210A, shanghai Ya Rong

Biochemical Instrument Factory, China) to remove the solvent. Subse-

quently, the crude extract was puried using AB-8 macroporous resin to

eradicate traces of sugars and proteins and obtain puried polyphenols.

Finally, the obtained product was freeze-dried (LGJ-1A-50, Beijing Yatai

Kelong Instrument Technology Co., Ltd., China) and stored at −20 ◦C to

facilitate further experiments.

The total phenolic content was evaluated using the Folin–Ciocalteu

technique [20]. The total phenolic content of LBP was 603.33 ±12.03

mg GAE/g DE.

2.3. Analysis of LBP by HPLC-MS/MS

HPLC-MS/MS analysis was used to determine the composition of LBP

with reference to the method of Cao, Teng, Wei, Huang and Xia [21].

Samples were processed as follows: 0.01 g of LBP was dissolved in 70 %

methanol solution in constant volume to 10 mL, passed through a 0.22

m lter membrane, and the stock solution or 10-fold diluted before

HPLC-MS/MS analysis.

Phenolic composition of LBP was analyzed by LC-MS/MS (Agilent

1100; Triple quadrupole mass spectrometry API4000). The column was

a C18 column (3 ×50 mm, 2.7

m, Poroshell 120 EC, Agilent, CA, USA).

Mobile phase A was 0.5 % aqueous formic acid. The mobile phase B was

acetonitrile solution. The column temperature was set at 35 ◦C. The ow

rate was 0.6 mL/min and the injection volume was 10

L. The elution

gradient was set as follows: 0–1 min, 95 % A; 1–8 min, 75 % A; 8–12

min, 40 % A; 13 min, 0 % A; 16 min, 0 % A; 16.1–20 min, 95 % A. The

mass spectrometry conditions were set as follows: negative ion mode:

spray voltage 4500 v; desolventization temperature 500 ◦C; desolven-

tization gas (N2) 1000 L/h. LBP was detected by MRM (multiple reaction

monitoring) technique using a self-constructed database. Identication

and quantication were achieved by comparing the retention time,

parent ion, daughter ion, and retention time (RT) with standards,

referring to the information published in the literature.

2.4. Effects and interactions of LBP on CS

2.4.1. Preparation of the CS-LBP complex

CS (1 g) was mixed with various concentrations of LBP, specically 2

%, 5 %, and 10 %, based on the dry weight of the starch. Further, the

mixture was diluted with 40 mL of distilled water and boiled for 30 min

with continuous stirring using a glass rod. The CS–LBP complex was

nally cooled to room temperature and utilized for further analysis. In

addition, a control sample of pure CS with no additional LBP were

produced for comparison.

2.4.2. Color measurement

Colors were measured using a CR-10 Plus colorimeter (Konica Min-

olta, Tokyo, Japan) and recorded as L*, a*, and b*, as dened by Huang,

Wu and Chen [22]. The L* values represented luminance, and ranged

from 0 (black) to 100 (white); the a* values represented positive and

negative readings for redness and greenness, respectively; and the b*

values represented positive and negative readings for yellowness and

blueness, respectively. In addition, the hue and chroma were determined

using the following equations:

Hue =tanb*

a*–1

(1)

Chroma =

a*2 +b*2

(2)

2.4.3. Iodine binding capacity

Iodine binding capacity was determined by Ultraviolet (UV) spec-

troscopy [23]. The CS-LBP complex (0.1 mL) was combined with an

equal amount of iodine reagent, diluted with distilled water to 5 mL, and

a UV absorption spectrum of 500–850 nm was recorded.

2.4.4. FTIR

FTIR measurements followed the method of Pourfarzad, Youse and

Ako [24]. First, the CS-LBP complex was freeze-dried. Then, it was

mixed with KBr at a ratio of 1:100 and subsequently pulverized and

pressed. FTIR (IRTracer-100, Shimadzu, Japan) scans were obtained at

room temperature in the wavelength of 4000–400 cm

−1

with 16 scans

and a resolution of 2 cm

−1

2.4.5. XRD

XRD was conducted according to the conditions described by Miao,

Xu, Jia, Zhang, Niu and Zhao [25]. The CS-LBP complex was freeze-

dried and performed with an X-ray diffractometer (D/MAX 2500 V,

Rigaku Corporation, Japan). The scan area was set to 5◦–40◦(2θ), with a

scan speed of 4◦/min and a scan step of 0.02◦. Starch relative crystal-

linity (RC) was calculated using MDI-Jade 6.5 software (Material Data

Inc., Livermore, California, USA).

2.4.6. Thermal properties

DSC 250 (TA Instruments, USA) was used to evaluate the thermal

characteristics of the samples. Following the procedure described by Lin,

Yu, Gao, Mei, Zhu and Du [26], each sample (3 mg, dry weight) was

deposited in an aluminum crucible with deionized water (approximately

10 mg), sealed and equilibrated at 25 ◦C for 24 h. The onset temperature

), peak temperature (T

), conclusion temperature (T

) and enthalpy

of gelatinization (ΔH

) were determined by heating all samples from

F. Li et al.

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