Progress on Bioavailability of Calcium and Calcium-Peptide Complexes

LIU Jiachen; CHENG Yongqiang; TANG Ning

doi:10.13386/j.issn1002-0306.2023020067

Volume 44 Issue 23

Nov. 2023

Turn off MathJax

Article Contents

Abstract

References

Science and Technology of Food Industry > 2023 > 44(23): 354-365. > DOI: 10.13386/j.issn1002-0306.2023020067

LIU Jiachen, CHENG Yongqiang, TANG Ning. Progress on Bioavailability of Calcium and Calcium-Peptide Complexes[J]. Science and Technology of Food Industry, 2023, 44(23): 354−365. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2023020067.

Citation:

PDF (1571 KB)

Progress on Bioavailability of Calcium and Calcium-Peptide Complexes

College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China

More Information

Received Date: February 07, 2023
Available Online: September 24, 2023

Graphical Abstract

Abstract

Abstract

Calcium is an essential nutrient for human health and plays a crucial role in various physiological processes such as bone formation, muscle contraction, nerve transmission, and blood clotting. Calcium absorption mainly occurs in the small intestine where the calcium enters the enterocytes through active transport or passive diffusion. However, the free calcium ions dissolved in gastric acid may form insoluble precipitates with other dietary components (such as phytate, oxalate, fiber) in the slightly alkaline intestinal environment, leading to decreased calcium absorption and bioavailability. Decreased calcium absorption can result in a range of bone metabolic diseases, such as rickets and osteoporosis. Therefore, it is important to choose foods or supplements that can provide highly soluble and bioavailable forms of calcium. Some organic calcium salts such as calcium gluconate and calcium citrate have been shown to form supersaturated solutions in the intestinal tract, which can enhance calcium absorption by increasing the concentration gradient across the intestinal epithelium. Furthermore, calcium-peptide complexes are proven to be very effective for improving calcium absorption without causing any side effects. Calcium-peptide complexes can serve as a novel calcium supplement. In this paper, the effects of food components on calcium absorption and bioavailability are reviewd, and the mechanisms underlying the enhancement of calcium absorption by some organic salts (such as calcium gluconate and calcium citrate) and peptides are summarized. And the potential applications of calcium-peptide complexes in human nutrition are also discussed, aiming to provide new insights that can aid in the development of safe and effective calcium supplements
- calcium,
- calcium salts,
- calcium-peptide complexes,
- bioavailability

FullText(HTML)

References (154)

References

[1]	ZHANG H, ZHAO L, SHEN Q, et al. Preparation of cattle bone collagen peptides-calcium chelate and its structural characterization and stability[J]. LWT,2021,144:111264. doi: 10.1016/j.lwt.2021.111264
[2]	VANNUCCI L, FOSSI C, QUATTRINI S, et al. Calcium intake in bone health:A focus on calcium-rich mineral waters[J]. Nutrients,2018,10(12):1930. doi: 10.3390/nu10121930
[3]	LIAO W, CHEN H, JIN W, et al. Three newly isolated calcium-chelating peptides from tilapia bone collagen hydrolysate enhance calcium absorption activity in intestinal Caco-2 cells[J]. Journal of Agricultural and Food Chemistry,2020,68(7):2091−2098. doi: 10.1021/acs.jafc.9b07602
[4]	MINE Y, SHAHIDI F. Nutraceutical proteins and peptides in health and disease[M]. Boca Raton:CRC Press, 2005.
[5]	ZHANG M, LIU K. Calcium supplements and structure-activity relationship of peptide-calcium chelates:A review[J]. Food Science and Biotechnology,2022,31(9):1111−1122. doi: 10.1007/s10068-022-01128-6
[6]	CHANG G R L, TU M Y, CHEN Y H, et al. KFP-1, a novel calcium-binding peptide isolated from kefir, promotes calcium influx through TRPV6 channels[J]. Molecular Nutrition & Food Research,2021,65(22):e2100182.
[7]	MILLER G D, JARVIS J K, MCBEAN L D. The importance of meeting calcium needs with foods[J]. Journal of the American College of Nutrition, 2001, 20(2 Suppl):168S-185S.
[8]	CHAROENPHUN N, CHEIRSILP B, SIRINUPONG N, et al. Calcium-binding peptides derived from tilapia ( Oreochromis niloticus) protein hydrolysate[J]. European Food Research and Technology,2013,236(1):57−63. doi: 10.1007/s00217-012-1860-2
[9]	SHI J, LE MAGUER M. Lycopene in tomatoes:Chemical and physical properties affected by food processing[J]. Critical Reviews in Biotechnology,2000,20(4):293−334. doi: 10.1080/07388550091144212
[10]	STRAUB D A. Calcium supplementation in clinical practice:A review of forms, doses, and indications[J]. Nutrition in Clinical Practice:Official Publication of the American Society for Parenteral and Enteral Nutrition,2007,22(3):286−296. doi: 10.1177/0115426507022003286
[11]	VAVRUSOVA M, SKIBSTED L H. Calcium nutrition. Bioavailability and fortification[J]. LWT-Food Science and Technology, 2014, 59(2, Part 2):1198-1204.
[12]	VOGEL H J. Calcium-binding protein protocols[M]. Humana Press, 2002.
[13]	RÉRAT A, NUNES C S, MENDY F, et al. Amino acid absorption and production of pancreatic hormones in non-anaesthetized pigs after duodenal infusions of a milk enzymic hydrolysate or of free amino acids[J]. British Journal of Nutrition,1988,60:121−136. doi: 10.1079/BJN19880082
[14]	MCDONAGH D, FITZGERALD R J. Production of caseinophosphopeptides (CPPs) from sodium caseinate using a range of commercial protease preparations[J]. International Dairy Journal,1998,8(1):39−45. doi: 10.1016/S0958-6946(98)00019-3
[15]	PEREGO S, DEL FAVERO E, DE LUCA P, et al. Calcium bioaccessibility and uptake by human intestinal like cells following in vitro digestion of casein phosphopeptide-calcium aggregates[J]. Food and Function,2015,6(6):1796−1807. doi: 10.1039/C4FO00672K
[16]	HEANEY R P. Calcium intake and disease prevention[J]. Arquivos Brasileiros de Endocrinologia e Metabologia,2006,50(4):685−693. doi: 10.1590/S0004-27302006000400014
[17]	SHKEMBI B, HUPPERTZ T. Calcium absorption from food products:food matrix effects[J]. Nutrients,2021,14(1):180. doi: 10.3390/nu14010180
[18]	ILICH J Z, KERSTETTER J E. Nutrition in bone health revisited:A story beyond calcium[J]. Journal of the American College of Nutrition,2000,19:715−737. doi: 10.1080/07315724.2000.10718070
[19]	RUTTER G A, FASOLATO C, RIZZUTO R. Calcium and organelles:A two-sided story[J]. Biochemical and Biophysical Research Communications,1998,253(3):549−557.
[20]	WILLIAMS G R, DOWNS J W, WOLF C E, et al. Evaluation of strontium interference in calcium measurement procedures and content in supplements as measured by ICP-MS[J]. The Journal of Applied Laboratory Medicine,2023,8(2):307−318. doi: 10.1093/jalm/jfac092
[21]	WANG L, MANSON J E, SESSO H D. Calcium intake and risk of cardiovascular disease[J]. American Journal of Cardiovascular Drugs,2012,12(2):105−116. doi: 10.2165/11595400-000000000-00000
[22]	PARK Y W. Overview of bioactive components in milk and dairy products[M]. John Wiley & Sons, Inc, 2009.
[23]	ZHU K, PRINCE R L. Calcium and bone[J]. Clinical Biochemistry,2012,45(12):936−942. doi: 10.1016/j.clinbiochem.2012.05.006
[24]	RIZZOLI R. Dairy products, yogurts, and bone health[J]. The American Journal of Clinical Nutrition, 2014, 99(5 Suppl):1256S−1262S.
[25]	TORRES M R S G, FRANCISCHETTI E A, GENELHU V, et al. Effect of a high-calcium energy-reduced diet on abdominal obesity and cardiometabolic risk factors in obese Brazilian subjects[J]. International Journal of Clinical Practice,2010,64(8):1076−1083. doi: 10.1111/j.1742-1241.2009.02312.x
[26]	TORRES M R S G, SANJULIANI A F. Does calcium intake affect cardiovascular risk factors and/or events?[J]. Clinics (Sao Paulo, Brazil),2012,67(7):839−844. doi: 10.6061/clinics/2012(07)22
[27]	VINAROVA L, VINAROV Z, TCHOLAKOVA S, et al. The mechanism of lowering cholesterol absorption by calcium studied by using an in vitro digestion model.[J]. Food & Function,2016,7(1):151−163.
[28]	FERNÁNDEZ-JALAO I, SÁNCHEZ-MORENO C, ANCOS B D. Influence of food matrix and high-pressure processing on onion flavonols and antioxidant activity during gastrointestinal digestion[J]. Journal of Food Engineering,2017,213:60−68.
[29]	CARBONELL-CAPELLA J M, BUNIOWSKA M, BARBA F J, et al. Analytical methods for determining bioavailability and bioaccessibility of bioactive compounds from fruits and vegetables:A review[J]. Comprehensive Reviews in Food Science and Food Safety,2014,13(2):155−171. doi: 10.1111/1541-4337.12049
[30]	CIAN R E, GARZÓN A G, ANCONA D B, et al. Chelating properties of peptides from red seaweed pyropia columbina and its effect on iron bio-accessibility[J]. Plant Foods for Human Nutrition (Dordrecht, Netherlands),2016,71(1):96−101. doi: 10.1007/s11130-016-0533-x
[31]	WANG X, ZHOU J, TONG P S, et al. Zinc-binding capacity of yak casein hydrolysate and the zinc-releasing characteristics of casein hydrolysate-zinc complexes[J]. Journal of Dairy Science,2011,94(6):2731−2740. doi: 10.3168/jds.2010-3900
[32]	BUDSEEKOAD S, YUPANQUI C T, SIRINUPONG N, et al. Structural and functional characterization of calcium and iron-binding peptides from mung bean protein hydrolysate[J]. Journal of Functional Foods,2018,49:333−341. doi: 10.1016/j.jff.2018.07.041
[33]	NIE X, JIN H, WEN G, et al. Estrogen regulates duodenal calcium absorption through differential role of estrogen receptor on calcium transport proteins[J]. Digestive Diseases and Sciences,2020,65(12):3502−3513. doi: 10.1007/s10620-020-06076-x
[34]	WEBER D R, O’BRIEN K O, SCHWARTZ G J. Evidence of disordered calcium metabolism in adolescent girls with type 1 diabetes:An observational study using a dual-stable calcium isotope technique[J]. Bone,2017,105:184−190. doi: 10.1016/j.bone.2017.09.001
[35]	WONGDEE K, RODRAT M, TEERAPORNPUNTAKIT J, et al. Factors inhibiting intestinal calcium absorption:Hormones and luminal factors that prevent excessive calcium uptake[J]. The Journal of Physiological Sciences:JPS,2019,69(5):683−696.
[36]	D’AMELIO P, SASSI F. Gut microbiota, immune system, and bone[J]. Calcified Tissue International,2018,102(4):415−425. doi: 10.1007/s00223-017-0331-y
[37]	MOUSA A, NAQASH A, LIM S. Macronutrient and micronutrient intake during pregnancy:An overview of recent evidence[J]. Nutrients,2019,11(2):443. doi: 10.3390/nu11020443
[38]	KATRIEN C, LIEVE V, MATTHIAS L, et al. Thin bones:Vitamin D and calcium handling after bariatric surgery[J]. Bone Reports,2018,8:57−63. doi: 10.1016/j.bonr.2018.02.002
[39]	CHRISTAKOS S, VELDURTHY V, PATEL N, et al. Intestinal regulation of calcium:Vitamin D and bone physiology[J]. Advances in Experimental Medicine and Biology,2017,1033:3−12.
[40]	SIRICHAKWAL P P, KAMCHANSUPPASIN A, AKOH C C, et al. Vitamin D status is positively associated with calcium absorption among postmenopausal thai women with low calcium intakes[J]. The Journal of Nutrition,2015,145(5):990−995. doi: 10.3945/jn.114.207290
[41]	MAURYA V K, AGGARWAL M. Factors influencing the absorption of vitamin D in GIT:An overview[J]. Journal of Food Science and Technology,2017,54(12):3753−3765. doi: 10.1007/s13197-017-2840-0
[42]	BANDALI E, WANG Y, LAN Y, et al. The influence of dietary fat and intestinal pH on calcium bioaccessibility:An in vitro study[J]. Food & Function,2018,9(3):1809−1815.
[43]	WANG Y, DELLATORE P, DOUARD V, et al. High fat diet enriched with saturated, but not monounsaturated fatty acids adversely affects femur, and both diets increase calcium absorption in older female mice[J]. Nutrition Research,2016,36(7):742−750. doi: 10.1016/j.nutres.2016.03.002
[44]	SZILAGYI A, ISHAYEK N. Lactose intolerance, dairy avoidance, and treatment options[J]. Nutrients,2018,10(12):1994. doi: 10.3390/nu10121994
[45]	HODGES J K, CAO S, CLADIS D P, et al. Lactose intolerance and bone health:The challenge of ensuring adequate calcium intake[J]. Nutrients,2019,11(4):E718. doi: 10.3390/nu11040718
[46]	GRIESSEN M, COCHET B, INFANTE F, et al. Calcium absorption from milk in lactase-deficient subjects[J]. The American Journal of Clinical Nutrition,1989,49(2):377−384. doi: 10.1093/ajcn/49.2.377
[47]	TREMAINE W J, NEWCOMER A D, LAWRENCE RIGGS B, et al. Calcium absorption from milk in lactase-deficient and lactase-sufficient adults[J]. Digestive Diseases and Sciences,1986,31(4):376−378. doi: 10.1007/BF01311672
[48]	COCHET B, JUNG A, GRIESSEN M, et al. Effects of lactose on intestinal calcium absorption in normal and lactase-deficient subjects[J]. Gastroenterology,1983,84(5Pt1):935−940.
[49]	COUDRAY C, BELLANGER J, CASTIGLIA-DELAVAUD C, et al. Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men[J]. European Journal of Clinical Nutrition,1997,51(6):375−380. doi: 10.1038/sj.ejcn.1600417
[50]	ALBARRACÍN M, WEISSTAUB A R, ZULETA A, et al. Extruded whole grain diets based on brown, soaked and germinated rice. Effects on the lipid profile and antioxidant status of growing Wistar rats. Part II[J]. Food & Function,2016,7(6):2729−2735.
[51]	DAI Z, ZHANG Y, LU N, et al. Association between dietary fiber intake and bone loss in the framingham offspring study[J]. Journal of Bone and Mineral Research: The Official Journal of the American Society for Bone and Mineral Research,2018,33(2):241−249. doi: 10.1002/jbmr.3308
[52]	KIEFER-HECKER B, KIENZLE E, DOBENECKER B. Effects of low phosphorus supply on the availability of calcium and phosphorus, and musculoskeletal development of growing dogs of two different breeds[J]. Journal of Animal Physiology and Animal Nutrition,2018,102(3):789−798. doi: 10.1111/jpn.12868
[53]	ZHAO L, LI M, SUN H. Effects of dietary calcium to available phosphorus ratios on bone metabolism and osteoclast activity of the OPG /RANK/RANKL signalling pathway in piglets[J]. Journal of Animal Physiology and Animal Nutrition,2019,103(4):1224−1232. doi: 10.1111/jpn.13115
[54]	SILVA E O, BRACARENSE A P F R L. Phytic acid:From antinutritional to multiple protection factor of organic systems[J]. Journal of Food Science,2016,81(6):R1357−1362.
[55]	LESJAK M, K S SRAI S. Role of dietary flavonoids in iron homeostasis[J]. Pharmaceuticals,2019,12(3):119. doi: 10.3390/ph12030119
[56]	LO D, WANG H I, WU J, et al. Anti-nutrient components and their concentrations in edible parts in vegetable families[J]. CABI Reviews,2018,2018:1−30.
[57]	NAQVI M A, IRANI K A, KATANISHOOSHTARI M, et al. Disorder in milk proteins:Formation, structure, function, isolation and applications of casein phosphopeptides[J]. Current Protein & Peptide Science,2016,17(4):368−379.
[58]	SUN S, LIU F, LIU G, et al. Effects of casein phosphopeptides on calcium absorption and metabolism bioactivity in vitro and in vivo[J]. Food & Function,2018,9(10):5220−5229.
[59]	LUO M, XIAO J, SUN S, et al. Deciphering calcium-binding behaviors of casein phosphopeptides by experimental approaches and molecular simulation[J]. Food & Function,2020,11(6):5284−5292.
[60]	ZHU B, HOU T, HE H. Calcium-binding casein phosphopeptides-loaded chitosan oligosaccharides core-shell microparticles for controlled calcium delivery:Fabrication, characterization, and in vivo release studies[J]. International Journal of Biological Macromolecules,2020,154:1347−1355. doi: 10.1016/j.ijbiomac.2019.11.014
[61]	REID I R, BRISTOW S M, BOLLAND M J. Calcium supplements:Benefits and risks[J]. Journal of Internal Medicine,2015,278(4):354−368.
[62]	GENANT H K, COOPER C, POOR G, et al. Interim report and recommendations of the World Health Organization Task-Force for Osteoporosis[J]. Osteoporosis International,1999,10(4):259−264. doi: 10.1007/s001980050224
[63]	EFSA Panel on Food Additives and Nutrient Sources Added to Food (EFSA ANS Panel), MAGED Y, PETER A, et al. Evaluation of di-calcium malate, used as a novel food ingredient and as a source of calcium in foods for the general population, food supplements, total diet replacement for weight control and food for special medical purposes[J]. EFSA Journal,2018,16(6):e05291.
[64]	BAILEY R L, DODD K W, GOLDMAN J A, et al. Estimation of total usual calcium and vitamin D intakes in the United States[J]. The Journal of Nutrition,2010,140(4):817−822. doi: 10.3945/jn.109.118539
[65]	KELLER J L, LANOU A, BARNARD N D. The consumer cost of calcium from food and supplements[J]. Journal of the American Dietetic Association,2002,102(11):1669−1671. doi: 10.1016/S0002-8223(02)90355-X
[66]	BRONNER F, PANSU D. Nutritional aspects of calcium absorption[J]. The Journal of Nutrition,1999,129(1):9−12.
[67]	VAVRUSOVA M, RAITIO R, ORLIEN V, et al. Calcium hydroxy palmitate:Possible precursor phase in calcium precipitation by palmitate[J]. Food Chemistry,2013,138(4):2415−2420. doi: 10.1016/j.foodchem.2012.12.012
[68]	PAK C Y, HARVEY J A, HSU M C. Enhanced calcium bioavailability from a solubilized form of calcium citrate[J]. The Journal of Clinical Endocrinology and Metabolism,1987,65(4):801−805. doi: 10.1210/jcem-65-4-801
[69]	VAVRUSOVA M, SKIBSTED L H. Spontaneous supersaturation of calcium D-gluconate during isothermal dissolution of calcium L-lactate in aqueous sodium D-gluconate[J]. Food & Function,2014,5(1):85−91.
[70]	VAVRUSOVA M, LIANG R, SKIBSTED L H. Thermodynamics of dissolution of calcium hydroxycarboxylates in water[J]. Journal of Agricultural and Food Chemistry,2014,62(24):5675−5681. doi: 10.1021/jf501453c
[71]	BRONNER F. Current concepts of calcium absorption:An overview[J]. The Journal of Nutrition,1992,122(Suppl_3):641−643.
[72]	GOSS S L, LEMONS K A, KERSTETTER J E, et al. Determination of calcium salt solubility with changes in pH and P(CO(2)), simulating varying gastrointestinal environments[J]. The Journal of Pharmacy and Pharmacology,2007,59(11):1485−1492.
[73]	TANG N, SKIBSTED L H. Calcium binding to amino acids and small glycine peptides in aqueous solution:Toward peptide design for better calcium bioavailability[J]. Journal of Agricultural and Food Chemistry,2016,64(21):4376−4389. doi: 10.1021/acs.jafc.6b01534
[74]	LUMB R F, MARTELL A E. Metal chelating tendencies of glutamic and aspartic acids[J]. Journal of Physical Chemistry, 1953.
[75]	VAVRUSOVA M, SKIBSTED L H. Calcium binding to dipeptides of aspartate and glutamate in comparison with orthophosphoserine[J]. Journal of Agricultural and Food Chemistry,2013,61(22):5380−5384. doi: 10.1021/jf400741e
[76]	WU W, LI B, HOU H, et al. Isolation and identification of calcium-chelating peptides from Pacific cod skin gelatin and their binding properties with calcium[J]. Food & Function,2017,8(12):4441−4448.
[77]	HOU H, WANG S, ZHU X, et al. A novel calcium-binding peptide from Antarctic krill protein hydrolysates and identification of binding sites of calcium-peptide complex[J]. Food Chemistry,2018,243:389−395. doi: 10.1016/j.foodchem.2017.09.152
[78]	HE J, GUO H, ZHANG M, et al. Purification and characterization of a novel calcium-binding heptapeptide from the hydrolysate of tilapia bone with its osteogenic activity[J]. Foods (Basel, Switzerland),2022,11(3):468.
[79]	LÜ Y, LIU H, REN J, et al. The positive effect of soybean protein hydrolysates-calcium complexes on bone mass of rapidly growing rats[J]. Food & Function,2013,4(8):1245−1251.
[80]	BAO Z, ZHANG P, SUN N, et al. Elucidating the calcium-binding site, absorption activities, and thermal stability of egg white peptide-calcium chelate[J]. Foods,2021,10(11):2565. doi: 10.3390/foods10112565
[81]	CAETANO-SILVA M E, NETTO F M, BERTOLDO-PACHECO M T, et al. Peptide-metal complexes:Obtention and role in increasing bioavailability and decreasing the pro-oxidant effect of minerals[J]. Critical Reviews in Food Science and Nutrition,2021,61(9):1470−1489. doi: 10.1080/10408398.2020.1761770
[82]	PORATH J. Amino acid side chain interaction with chelate-liganded crosslinked dextran, agarose and TSK gel. A mini review of recent work[J]. Journal of Molecular Recognition,1990,3(3):123−127. doi: 10.1002/jmr.300030306
[83]	BELL C, ATKINS P. Principles and applications of metal chelation[M]. Clarendon Press, 1977.
[84]	ASHMEAD S D. The chemistry of ferrous bis-glycinate chelate[J]. Archivos Latinoamericanos De Nutricion, 2001, 51(1 Suppl 1):7−12.
[85]	LIN Y, CAI X, WU X, et al. Fabrication of snapper fish scales protein hydrolysate-calcium complex and the promotion in calcium cellular uptake[J]. Journal of Functional Foods,2020,65:103717. doi: 10.1016/j.jff.2019.103717
[86]	CARLTON D D, SCHUG K A. A review on the interrogation of peptide-metal interactions using electrospray ionization-mass spectrometry[J]. Analytica Chimica Acta,2011,686(1-2):19−39. doi: 10.1016/j.aca.2010.11.050
[87]	UDECHUKWU M C, DOWNEY B, UDENIGWE C C. Influence of structural and surface properties of whey-derived peptides on zinc-chelating capacity, and in vitro gastric stability and bioaccessibility of the zinc-peptide complexes[J]. Food Chemistry,2018,240:1227−1232. doi: 10.1016/j.foodchem.2017.08.063
[88]	SI K, GONG T, DING S, et al. Binding mechanism and bioavailability of a novel phosvitin phosphopeptide (Glu-Asp-Asp-pSer-pSer) calcium complex[J]. Food Chemistry,2023,404:134567. doi: 10.1016/j.foodchem.2022.134567
[89]	ZHANG Y Y, STOCKMANN R, NG K, et al. Opportunities for plant-derived enhancers for iron, zinc, and calcium bioavailability:A review[J]. Comprehensive Reviews in Food Science and Food Safety,2021,20(1):652−685. doi: 10.1111/1541-4337.12669
[90]	KHARE E, HOLTEN-ANDERSEN N, BUEHLER M J. Transition-metal coordinate bonds for bioinspired macromolecules with tunable mechanical properties[J]. Nature Reviews Materials,2021,6(5):421−436.
[91]	CHEN M, JI H, ZHANG Z, et al. A novel calcium-chelating peptide purified from Auxis thazard protien hydrolysate and its binding properties with calcium[J]. Journal of Functional Foods,2019,60:103447. doi: 10.1016/j.jff.2019.103447
[92]	ZHANG X, JIA Q, LI M, et al. Isolation of a novel calcium-binding peptide from phosvitin hydrolysates and the study of its calcium chelation mechanism[J]. Food Research International,2021,141:110169. doi: 10.1016/j.foodres.2021.110169
[93]	FERRARETTO A, GRAVAGHI C, FIORILLI A, et al. Casein-derived bioactive phosphopeptides:Role of phosphorylation and primary structure in promoting calcium uptake by HT-29 tumor cells[J]. FEBS letters,2003,551(1-3):92−98. doi: 10.1016/S0014-5793(03)00741-5
[94]	SUN N, WANG Y, BAO Z, et al. Calcium binding to herring egg phosphopeptides:Binding characteristics, conformational structure and intermolecular forces[J]. Food Chemistry,2020,310:125867.
[95]	ZHAO M, LI S, AHN D U, et al. Phosvitin phosphopeptides produced by pressurized hea-trypsin hydrolysis promote the differentiation and mineralization of MC3T3-E1 cells via the OPG/RANKL signaling pathways[J]. Poultry Science,2021,100(2):527−536. doi: 10.1016/j.psj.2020.10.053
[96]	PEREGO S, ZABEO A, MARASCO E, et al. Casein phosphopeptides modulate calcium uptake and apoptosis in Caco2 cells through their interaction with the TRPV6 calcium channel[J]. Journal of Functional Foods,2013,5(2):847−857. doi: 10.1016/j.jff.2013.01.032
[97]	JIANG B, MINE Y. Preparation of novel functional oligophosphopeptides from hen egg yolk phosvitin[J]. Journal of Agricultural and Food Chemistry,2000,48(4):990−994. doi: 10.1021/jf990600l
[98]	JIANG B, MINE Y. Phosphopeptides derived from hen egg yolk phosvitin:effect of molecular size on the calcium-binding properties[J]. Bioscience, Biotechnology, and Biochemistry,2001,65(5):1187−1190. doi: 10.1271/bbb.65.1187
[99]	LUO J, YAO X, SOLADOYE O P, et al. Phosphorylation modification of collagen peptides from fish bone enhances their calcium-chelating and antioxidant activity[J]. LWT,2022,155:112978. doi: 10.1016/j.lwt.2021.112978
[100]	ZONG H, PENG L, ZHANG S, et al. Effects of molecular structure on the calcium-binding properties of phosphopeptides[J]. European Food Research and Technology,2012,235(5):811−816.
[101]	BAO X L, LV Y, YANG B C, et al. A study of the soluble complexes formed during calcium binding by soybean protein hydrolysates[J]. Journal of Food Science,2008,73(3):C117−121. doi: 10.1111/j.1750-3841.2008.00673.x
[102]	ZHANG K, LI J, HOU H, et al. Purification and characterization of a novel calcium-biding decapeptide from pacific cod ( Gadus macrocephalus) bone:Molecular properties and calcium chelating modes[J]. Journal of Functional Foods,2019,52:670−679. doi: 10.1016/j.jff.2018.11.042
[103]	LIU F R, WANG L, WANG R, et al. Calcium-binding capacity of wheat germ protein hydrolysate and characterization of peptide-calcium complex[J]. Journal of Agricultural and Food Chemistry,2013,61(31):7537−7544. doi: 10.1021/jf401868z
[104]	CUI P, LIN S, JIN Z, et al. In vitro digestion profile and calcium absorption studies of a sea cucumber ovum derived heptapeptide-calcium complex[J]. Food & Function,2018,9(9):4582−4592.
[105]	ZHAO L, HUANG Q, HUANG S, et al. Novel peptide with a specific calcium-binding capacity from whey protein hydrolysate and the possible chelating mode[J]. Journal of Agricultural and Food Chemistry,2014,62(42):10274−10282. doi: 10.1021/jf502412f
[106]	AN J, ZHANG Y, YING Z, et al. The formation, structural characteristics, absorption pathways and bioavailability of calcium-peptide chelates[J]. Foods (Basel, Switzerland),2022,11(18):2762.
[107]	HOENDEROP J G J, NILIUS B, BINDELS R J M. Calcium absorption across epithelia[J]. Physiological Reviews,2005,85(1):373−422. doi: 10.1152/physrev.00003.2004
[108]	DIAZ DE BARBOZA G, GUIZZARDI S, TOLOSA D T N. Molecular aspects of intestinal calcium absorption[J]. World Journal of Gastroenterology,2015,21(23):7142−7154. doi: 10.3748/wjg.v21.i23.7142
[109]	PÉREZ A V, PICOTTO G, CARPENTIERI A R, et al. Minireview on regulation of intestinal calcium absorption[J]. Digestion,2008,77(1):22−34. doi: 10.1159/000116623
[110]	BIANCO S D, PENG J B, TAKANAGA H, et al. Marked disturbance of calcium homeostasis in mice with targeted disruption of the trpv6 calcium channel gene[J]. Journal of Bone and Mineral Research,2006,22(2):274−285.
[111]	DEN DEKKER E, HOENDEROP J G J, NILIUS B, et al. The epithelial calcium channels, TRPV5 & TRPV6:From identification towards regulation[J]. Cell Calcium,2003,33(5-6):497−507. doi: 10.1016/S0143-4160(03)00065-4
[112]	MCGOLDRICK L L, SINGH A K, SAOTOME K, et al. Opening of the human epithelial calcium channel TRPV6[J]. Nature,2018,553(7687):233−237. doi: 10.1038/nature25182
[113]	WONGDEE K, CHANPAISAENG K, TEERAPORNPUNTAKIT J, et al. Intestinal calcium absorption[J]. Comprehensive Physiology,2021,11(3):2047−2073.
[114]	SCHWALLER B. Cytosolic Ca²⁺ buffers are inherently Ca²⁺ signal modulators[J]. Cold Spring Harbor Perspectives in Biology,2020,12(1):a035543. doi: 10.1101/cshperspect.a035543
[115]	HONG E J, JEUNG E B. Biological significance of calbindin-D9k within duodenal epithelium[J]. International Journal of Molecular Sciences,2013,14(12):23330−23340. doi: 10.3390/ijms141223330
[116]	FLEET J C. Regulation of intestinal calcium and phosphate absorption[M]. ACADEMIC Press, 2018:329-342.
[117]	GHIJSEN W E J M, DE J M D, VAN O C H. Kinetic properties of Na⁺/Ca²⁺ exchange in basolateral plasma membranes of rat small intestine[J]. BBA-Biomembranes, 1983.
[118]	GUÉGUEN L, POINTILLART A. The bioavailability of dietary calcium[J]. Journal of the American College of Nutrition, 2000:119S-136S.
[119]	SHARMA R V, BUTTERS C A, MCELDOON J P, et al. Characterization of Ca²⁺ uptake in plasma membrane vesicles isolated from guinea pig ileum smooth muscle[J]. Cell Calcium,1987,8(1):65−77. doi: 10.1016/0143-4160(87)90037-6
[120]	LIU C, WENG H, CHEN L, et al. Impaired intestinal calcium absorption in protein 4.1R-deficient mice due to altered expression of plasma membrane calcium atpase 1b (PMCA1b)[J]. Journal of Biological Chemistry,2013,288(16):11407−11415. doi: 10.1074/jbc.M112.436659
[121]	DORKKAM N, WONGDEE K, SUNTORNSARATOON P, et al. Prolactin stimulates the L-type calcium channel-mediated transepithelial calcium transport in the duodenum of male rats[J]. Biochemical and Biophysical Research Communications,2013,430(2):711−716.
[122]	TSUCHITA H, SUZUKI T, KUWATA T. The effect of casein phosphopeptides on calcium absorption from calcium-fortified milk in growing rats[J]. The British Journal of Nutrition,2001,85(1):5−10. doi: 10.1079/BJN2000206
[123]	CHAROENPHANDHU N, LIMLOMWONGSE L, KRISHNAMRA N. Prolactin directly enhanced Na⁺/K⁺- and Ca²⁺-ATPase activities in the duodenum of female rats[J]. Canadian Journal of Physiology and Pharmacology,2006,84(5):555−563. doi: 10.1139/y05-161
[124]	JANTARAJIT W, THONGON N, PANDARANANDAKA J, et al. Prolactin-stimulated transepithelial calcium transport in duodenum and Caco-2 monolayer are mediated by the phosphoinositide 3-kinase pathway[J]. American Journal of Physiology. Endocrinology and Metabolism,2007,293(1):E372−384.
[125]	FUJITA H, SUGIMOTO K, INATOMI S, et al. Tight junction proteins claudin-2 and -12 are critical for vitamin D-dependent Ca²⁺ absorption between enterocytes[J]. Molecular Biology of the Cell,2008,19(5):1912−1921. doi: 10.1091/mbc.e07-09-0973
[126]	TSUKITA S, FURUSE M, ITOH M. Multifunctional strands in tight junctions[J]. Nature Reviews. Molecular Cell Biology,2001,2(4):285−293. doi: 10.1038/35067088
[127]	CURRY J N, SAURETTE M, ASKARI M, et al. Claudin-2 deficiency associates with hypercalciuria in mice and human kidney stone disease[J]. The Journal of Clinical Investigation,2020,130(4):1948−1960. doi: 10.1172/JCI127750
[128]	COLEGIO O R, ITALLIE C V, RAHNER C, et al. Claudin extracellular domains determine paracellular charge selectivity and resistance but not tight junction fibril architecture[J]. American Journal of Physiology-Cell Physiology,2003,284(6):C1346−C1354.
[129]	HIROKI F, HIDEKI C, HIROSHI Y, et al. Differential expression and subcellular localization of claudin-7, -8, -12, -13, and -15 along the mouse intestine[J]. Journal of Histochemistry & Cytochemistry, 2007:933-944.
[130]	VAN ITALLIE C M, FANNING A S, ANDERSON J M. Reversal of charge selectivity in cation or anion-selective epithelial lines by expression of different claudins[J]. American Journal of Physiology. Renal Physiology,2003,285(6):F1078−1084. doi: 10.1152/ajprenal.00116.2003
[131]	ALEXANDER R T, RIEVAJ J, DIMKE H. Paracellular calcium transport across renal and intestinal epithelia[J]. Biochemistry and Cell Biology = Biochimie et Biologie Cellulaire,2014,92(6):467−480. doi: 10.1139/bcb-2014-0061
[132]	KOPIC S, GEIBEL J P. Gastric acid, calcium absorption, and their impact on bone health[J]. Physiological Reviews,2013,93(1):189−268. doi: 10.1152/physrev.00015.2012
[133]	YE L, MORSE L R, ZHANG L, et al. Osteopetrorickets due to Snx10 deficiency in mice results from both failed osteoclast activity and loss of gastric acid-dependent calcium absorption[J]. PLoS Genetics,2015,11(3):e1005057. doi: 10.1371/journal.pgen.1005057
[134]	SCHINKE T, SCHILLING A F, BARANOWSKY A, et al. Impaired gastric acidification negatively affects calcium homeostasis and bone mass[J]. Nature Medicine,2009,15(6):674−681. doi: 10.1038/nm.1963
[135]	CARRASCO F, BASFI-FER K, ROJAS P, et al. Calcium absorption may be affected after either sleeve gastrectomy or Roux-en-Y gastric bypass in premenopausal women:A 2-y prospective study[J]. The American Journal of Clinical Nutrition,2018,108(1):24−32. doi: 10.1093/ajcn/nqy071
[136]	SUGITA M, MATSUMOTO M, TSUKANO Y, et al. Gastric emptying time after breakfast in healthy adult volunteers using ultrasonography[J]. Journal of Anesthesia,2019,33(6):697−700. doi: 10.1007/s00540-019-02694-6
[137]	LU Z, DING L, LU Q, et al. Claudins in intestines:Distribution and functional significance in health and diseases[J]. Tissue Barriers,2013,1(3):e24978. doi: 10.4161/tisb.24978
[138]	DUFLOS C, BELLATON C, PANSU D, et al. Calcium solubility, intestinal sojourn time and paracellular permeability codetermine passive calcium absorption in rats[J]. The Journal of Nutrition,1995,125(9):2348−2355. doi: 10.1093/jn/125.9.2348
[139]	FLEET J C, SCHOCH R D. Molecular mechanisms for regulation of intestinal calcium absorption by vitamin D and other factors[J]. Critical Reviews in Clinical Laboratory Sciences,2010,47(4):181−195. doi: 10.3109/10408363.2010.536429
[140]	MORGAN E L, MACE O J, HELLIWELL P A, et al. A role for Cav1.3 in rat intestinal calcium absorption[J]. Biochemical and Biophysical Research Communications,2003,312(2):487−493. doi: 10.1016/j.bbrc.2003.10.138
[141]	FLEET J C, EKSIR F, HANCE K W, et al. Vitamin D-inducible calcium transport and gene expression in three Caco-2 cell lines[J]. American Journal of Physiology-Gastrointestinal and Liver Physiology,2002,283(3):G618−625. doi: 10.1152/ajpgi.00269.2001
[142]	KARBACH U. Paracellular calcium transport across the small intestine[J]. The Journal of Nutrition, 1992, 122(3 Suppl):672−677.
[143]	PANSU D, BELLATON C, ROCHE C, et al. Duodenal and ileal calcium absorption in the rat and effects of vitamin D[J]. American Journal of Physiology-Gastrointestinal and Liver Physiology,1983,244(6):G695−G700. doi: 10.1152/ajpgi.1983.244.6.G695
[144]	CRAMER C F, COPP D H. Progress and rate of absorption of radiostrontium through intestinal tracts of rats[J]. Experimental Biology and Medicine,1959,102(2):514−517. doi: 10.3181/00379727-102-25301
[145]	BEGGS M R, LEE J J, BUSCH K, et al. TRPV6 and Cav1.3 mediate distal small intestine calcium absorption before weaning[J]. Cellular and Molecular Gastroenterology and Hepatology,2019,8(4):625−642. doi: 10.1016/j.jcmgh.2019.07.005
[146]	RIEVAJ J, PAN W, CORDAT E, et al. The Na⁺/H⁺ exchanger isoform 3 is required for active paracellular and transcellular Ca²⁺ transport across murine cecum[J]. American Journal of Physiology-Gastrointestinal and Liver Physiology,2013,305(4):G303−G313. doi: 10.1152/ajpgi.00490.2012
[147]	WASSERMAN R H. Vitamin D and the dual processes of intestinal calcium absorption[J]. The Journal of Nutrition,2004,134(11):3137−3139. doi: 10.1093/jn/134.11.3137
[148]	HOENDEROP J G, VENNEKENS R, MÜLLER D, et al. Function and expression of the epithelial Ca(²⁺) channel family:Comparison of mammalian ECaC1 and 2[J]. The Journal of Physiology, 2001, 537(Pt 3):747-761.
[149]	KORHONEN H. Milk-derived bioactive peptides:From science to applications[J]. Journal of Functional Foods,2009,1(2):177−187. doi: 10.1016/j.jff.2009.01.007
[150]	WANG X, ZHANG Z, XU H, et al. Preparation of sheep bone collagen peptide-calcium chelate using enzymolysis-fermentation methodology and its structural characterization and stability analysis[J]. RSC Advances,2020,10(20):11624−11633. doi: 10.1039/D0RA00425A
[151]	SHEN W, MATSUI T. Intestinal absorption of small peptides:A review[J]. International Journal of Food Science & Technology,2019,54(6):1942−1948.
[152]	FERNÁNDEZ-MUSOLES R, ISIDRA R, JUAN B S, et al. Bioavailability of antihypertensive lactoferricin B-derived peptides:Transepithelial transport and resistance to intestinal and plasma peptidase[J]. International Dairy Journal,2013,32(2):169−174.
[153]	MEREDITH D, PRICE R A. Molecular modeling of PepT1-towards a structure[J]. The Journal of Membrane Biology,2006,213(2):79−88. doi: 10.1007/s00232-006-0876-6
[154]	KATIMBA H A, WANG R, CHENG C. Current findings support the potential use of bioactive peptides in enhancing zinc absorption in humans[J]. Critical Reviews in Food Science and Nutrition, 2021:1−21.

[1]	SUN Ruiyin, WANG Ruixue, E Jingjing, YAO Caiqing, HE Zongbai, ZHANG Qiaoling, CHEN Zichao, MA Rongze, BAO Qiuhua, WANG Junguo. Effect of Calcium Ions on the Freeze-drying Resistance of Lactobacillus plantarum LIP-1[J]. Science and Technology of Food Industry, 2021, 42(17): 100-106. DOI: 10.13386/j.issn1002-0306.2020110151
[2]	ZOU Yong, WEI Rifeng, HUANG Weiqing, ZHOU Fengfang, LIN Shan, ZHENG Shizhong, JIANG Shengtao, LI Dongdong, LIU Wei. Effects of Chimonanthus salicifolius Aleoholic Extracts on Growth, Muscle Quality and Intestinal Morphology of Larimichthys crocea[J]. Science and Technology of Food Industry, 2021, 42(4): 18-25. DOI: 10.13386/j.issn1002-0306.2020050157
[3]	JIA Zhen-yu, SUN Hui-hui, HAO Xu-sheng, KANG Shen-min, ZHENG Xiao-ying, GUO Du, SUN Yi, SHI Chao, XIA Xiao-dong. Inhibitory Activity of Thymol and Carvacrol Against Cronobacter sakazakii[J]. Science and Technology of Food Industry, 2018, 39(20): 79-86. DOI: 10.13386/j.issn1002-0306.2018.20.014
[4]	LIU Shuai, ZHAO Guan-hua, YANG Qing-qing, TONG Chang-qing, LI Wei. Effect of a lectin CSL on the morphology of yeast Saccharomyces cerevisiae[J]. Science and Technology of Food Industry, 2017, (24): 114-119. DOI: 10.13386/j.issn1002-0306.2017.24.023
[5]	CHU Thi-le-hoa, XIE Jia, HE Song-gui, YU Jian-xia, LI Wei-gang, WU Zhen-qiang. Evaluation of immersion using warm water on the removal of off-flavor from raw pork and its weight loss[J]. Science and Technology of Food Industry, 2016, (23): 328-332. DOI: 10.13386/j.issn1002-0306.2016.23.053
[6]	YANG Xu-qiu, CHEN Jian-feng, ZHENG Xiang-nan, XIE You-ping. Effects of light intensity and nitrogen limitation on cell growth and cell composition of Chlorella sorokiniana[J]. Science and Technology of Food Industry, 2016, (18): 246-250. DOI: 10.13386/j.issn1002-0306.2016.18.038
[7]	WANG Peng-fei, DI Qian-qian, LIU Bin, ZHOU Xiao-jing. Effect of freezing rate on some structural parameters of carrot cells[J]. Science and Technology of Food Industry, 2015, (10): 125-129. DOI: 10.13386/j.issn1002-0306.2015.10.017
[8]	LIU Bin, LI Yuan-yuan, WANG Xiao-ming, CAO Feng-bo, HUO Gui-cheng, YANG Li-jie. Effect of colostrum growth factors extracts on proliferation and migration of CaCO-2 cells[J]. Science and Technology of Food Industry, 2015, (07): 354-358. DOI: 10.13386/j.issn1002-0306.2015.07.066
[9]	SHEN Yu-zhen, YU Hai-ning, ZHANG Cheng-cheng, ZENG Si-min, SHEN Sheng-rong. Effects of condensed fish oil on the growth of prostate cells in vitro[J]. Science and Technology of Food Industry, 2014, (12): 358-364. DOI: 10.13386/j.issn1002-0306.2014.12.070
[10]	WANG Dan, LEI Yong-dong, MA Yue, ZHANG Li, ZHAO Xiao-yan. Effect of anthocyanins from three kind of purple plants on ST cells growth[J]. Science and Technology of Food Industry, 2013, (23): 104-107. DOI: 10.13386/j.issn1002-0306.2013.23.024

Supplements (0)

Cited By

Cited by

Periodical cited type(11)

1.	王鑫，杨梦媛，修伟业，遇世友，王景阳，马永强. 甜玉米芯多糖铁配合物的工艺优化及体外活性. 精细化工. 2024(10): 2280-2289 .
2.	鲍彤彤，崔海燕，段然，纪龙翔，吕向云，高乐，吴信. 大豆蛋白肽-微量元素螯合物的制备及结构表征. 食品与发酵工业. 2024(21): 170-174 .
3.	李小军，马晓辉，段国建，姜红，曾凡逵，高作旺，董文静，王引权，晋玲. 兰州百合多糖铁(Ⅲ)配合物制备工艺的Box-Behnken响应面法优化及其体外抗氧化活性评价. 现代食品科技. 2024(12): 201-208 .
4.	杜国丰，尹梦琪，梁飞龙，姜宁，陈红漫，矫继峰，刘凤翊. 微波辅助H_2O_2/V_C降解制备低分子量浒苔多糖的研究. 食品工业科技. 2023(12): 37-44 . 本站查看
5.	高然，苏贇，陈俊德，郑美华. 硫酸软骨素螯合锌的制备、表征及体外生物活性. 食品工业科技. 2022(09): 194-202 . 本站查看
6.	毛嘉敏，陈昱瑶，宋洁，张燕，王婧贤，李馨雨，范柳萍，成向荣. 具有铁螯合能力的驴骨胶原肽酶解条件优化及微观形态. 粮油食品科技. 2022(05): 188-196 .
7.	钟普鹏，胡嘉宁，胡德宝，秦顺义，洪亮，马吉飞，李桂霞，李瑞忠. 姬松茸多糖铁(Ⅲ)合成方法的研究. 食品科技. 2021(03): 232-237 .
8.	舒畅，夏洁，袁帅，赵帅，张西锋，鄢又玉. 响应面优化羧甲基茯苓多糖铁复合物的制备. 食品研究与开发. 2019(08): 188-194+211 .
9.	张喜峰，崔晶，王文琴，罗光宏，杨生辉. 螺旋藻多糖铁(Ⅲ)配合物的制备、抗氧化及淋巴细胞增殖活性. 精细化工. 2019(06): 1097-1103 .
10.	景永帅，张瑞娟，吴兰芳，郑玉光，高心悦，郝彤宇，张丹参. 多糖铁复合物的结构特征和生理活性研究进展. 食品研究与开发. 2019(22): 203-208 .
11.	李石清，袁强，蒋福升，张婷，张春椿. 制首乌多糖Fe(Ⅲ)配合物的合成及吸附动力学研究. 中国现代中药. 2019(10): 1382-1385 .