Achiote (Bixa orellana) Lipophilic Extract, Bixin, and δ-tocotrienol Effects on Lifespan and Stress Resistance in Caenorhabditis elegans

Abstract

The onset of many degenerative diseases related to aging has been associated with a decrease in the activity of antistress systems, and pharmacological interventions increasing stress resistance could be effective to prevent the development of such diseases. Achiote is a valuable source of carotenoid and tocotrienols, which have antioxidant activity. In this work, we explore the capacity of an achiote seed extract and its main compounds to modulate the lifespan and antistress responses on Caenorhabditis elegans, as well as the mechanisms involved in these effects. Achiote lipophilic extract, bixin, and δ-tocotrienol were applied on nematodes to carry out lifespan, stress resistance, and fertility assays. The achiote seed extract increased the median and maximum lifespan up to 35% and 27% and increased resistance against oxidative and thermal stresses without adverse effects on fertility. The beneficial effects were mimicked by a bixin+δ-tocotrienol mixture. All the effects on lifespan and stress resistance were independent of caloric restriction but dependent on the insulin/insulin growth factor-1 pathway. This study could provide insights for further research on a new beneficial use of this important crop in health and nutraceutical applications beyond its use as a source of natural pigments.

Key words

Bixaceae - Bixa Orellana - Caenorhabditis elegans - antioxidants - longevity - stress resistance

Publication History

Received: 07 April 2020

Accepted after revision: 14 September 2020

Article published online:
29 October 2020

• References

• 1 Epel ES, Lithgow GJ. Stress biology and aging mechanisms: toward understanding the deep connection between adaptation to stress and longevity. J Gerontol A Biol Sci Med Sci 2014; 69: S10-S16
• 2 Liu Y, Weng W, Gao R, Liu Y. New insights for cellular and molecular mechanisms of aging and aging-related diseases: herbal medicines as potential terapeutic approach. Oxid Med Cell Longev 2019; 2019: 4598167
• 3 Deepashree S, Niveditha S, Shivanandappa T, Ramesh SR. Oxidative stress resistance as a factor in aging: evidence form an extended longevity phenotype of Drosophila melanogaster . Biogerontology 2019; 20: 497-513
• 4 Peng C, Wang X, Chen J, Jiao R, Wang L, Li YM, Zuo Y, Liu Y, Lei L, Ma KY, Huang Y, Chen ZY. Biology of ageing and role of dietary antioxidants. Biomed Res Int 2014; 2014: 831-841
• 5 Rathor L, Pant A, Awasthi H, Mani D, Pandey R. An antidiabetic polyherbal phytomedicine confers stress resistance and extends lifespan in Caenorhabditis elegans . Biogerontology 2017; 18: 131-147
• 6 Gómez-Linton DR, Alavez S, Alarcón-Aguilar A, López-Diazguerrero NE, Konigsberg M, Pérez-Flores LJ. Some naturally occurring compounds that increase longevity and stress resistance in model organisms of aging. Biogerontology 2019; 20: 583-603
• 7 Partridge L. Intervening in ageing to prevent the diseases of ageing. Trends Endocrinol Metab 2014; 25: 555-557
• 8 López-Otín C, Galluzzi L, Freije J, Madeo F, Kroemer G. Metabolic control of longevity. Cell 2016; 166: 802-821
• 9 Li Y, Pham V, Bui M, Song L, Wu C, Walia A, Uchio E, Smith-Lu F, Zi X. Rhodiola rosea L.: an herb with anti-stress, anti-aging, and immunostimulating properties for cancer chemoprevention. Curr Pharmacol Rep 2017; 3: 384-395
• 10 Embuscado M. Species and herbs: Natural sources of antioxidants – a mini review. J Funct Foods 2015; 18: 811-819
• 11 Kayser O. Ethnobotany and medicinal plant biotechnology: from tradition to modern aspects of drug development. Planta Med 2018; 84: 834-838
• 12 Lucanic M, Lithgow G, Alavez S. Pharmacological lifespan extension of invertebrates. Ageing Res Rev 2013; 12: 445-458
• 13 Ríos JL, Giner RM, Marín M, Recio MC. A pharmacological update of ellagic acid. Planta Med 2018; 84: 1068-1093
• 14 Shaidu-ul-Islam. Rather L, Mohammad F. Phytochemistry, biological activities and potential of annatto in natural colorant production for industrial applications–a review. J Adv Res 2015; 7: 499-514
• 15 Ahsan H, Ahad A, Siddiqui W. A review of characterization of tocotrienols from plant oils and foods. J Chem Biol 2015; 8: 45-59
• 16 Rivera-Madrid R, Aguilar-Espinosa M, Cárdenas-Cornejo Y, Garza-Caligaris LE. Carotenoid derivates in achiote (Bixa orellana) sedes: synthesis and health promoting properties. Front Plant Sci 2016; 7: 1406
• 17 Malavolta M, Poerpaoli E, Giacconi R, Basso A, Cardelli M, Piacenza F, Provinciali M. Anti-inflammatory activity of tocotrienols in age-related pathologies: a SASPected involvement of cellular senescence. Biol Proced Online 2018; 20: 22
• 18 Golin-Pacheco SD, Gasparin AT, Alves-Jesus CH, Bittencourt-Sotomaior B, Ventura ACSSB, Belo-Redivo DD, Cabrini DA, Gaspari-Dias JF, Miguel MD, Gomes-Miguel O, Cunha JM. Antinociceptive and anti-inflammatory effects of bixin, a carotenoid extracted form the seeds of Bixa orellana . Planta Med 2019; 85: 1216-1224
• 19 Yazaki K, Yoshikoshi C, Oshiro S, Yanase S. Supplemental cellular protection by a carotenoid extends lifespan via Ins/IGF-1 signaling in Caenorhabditis elegans . Oxi Med Cell Longev 2011; 2011: 596240
• 20 Vayndorf E, Lee S, Liu RH. Whole apple extracts increase lifespan, healthspan and resistance to stress in Caenorhabditis elegans . J Funct Foods 2013; 5: 1235-1243
• 21 Cavinato M, Waltenberger B, Baraldo G, Grade C, Stuppner H, Jansen-Dürr P. Plant extracts and natural compounds used against UVB-induced photoaging. Biogerontology 2017; 18: 499-516
• 22 Villa-Hernández JM, Mendoza-Cardoso G, Mendoza-Espinoza JA, Vela-Hinojosa C, Díaz de León-Sánchez F, Rivera-Cabrera F, Alia-Tejacal I, Pérez-Flores LJ. Antioxidant capacity in vitro and in vivo of various ecotypes of Mexican plum (Spondias purpurea L.). J Food Sci 2017; 82: 2576-2582
• 23 Si H, Liu D. Dietary antiaging phytochemicals and mechanisms associated with prolonged survival. J Nutr Biochem 2014; 25: 581-591
• 24 Kim CK, Park JK, Lee JS, Park SK. Increased resistance to stress and an anti-aging effect due to Acanthopanax sessiliflorus roots in Caenorhabditis elegans . Food Sci Biotechnol 2014; 23: 1653-1659
• 25 Zhuang Z, Lv T, Li M, Zhang Y, Xue T, Yang L, Liu H, Zhang W. The lifespan-extending effects of Nymphaea hybrid root extract in the nematode Caenorhabditis elegans . Plant Foods Hum Nutr 2014; 69: 304-309
• 26 Adachi H, Ishii N. Effects of tocotrienols on life span and protein carbonylation in Caenorhabditis elegans . J Gerontol A Biol Sci Med Sci 2000; 55: B280-B285
• 27 Aan G, Zainudin M, Karim N, Wan W. Effect of tocotrienol-rich fraction on the lifespan and oxidative biomarkers in Caenorhabditis elegans under oxidative stress. Clin Sci 2013; 68: 599-604
• 28 Michaličková D, Belović M, Ilić N, Kotur-Stevuljeivć J, Ondřej S, Šobajić S. Comparison of polyphenols-enriched tomato juice and standard tomato juice for cardiovascular benefits in subjects with stage 1 hypertension: a randomized controlled study. Plant Foods Hum Nutr 2019; 74: 122-127
• 29 Abayomi M, Adebayo AS, Bennett D, Porter R, Selly-Campbell J. In vitro antioxidant activity of Bixa orellana (annatto) seed extract. J Appl Pharm Sci 2014; 4: 101-106
• 30 Park JS, Mathison BD, Zawlocki BM, Chew BP. Bixin uptake and antioxidatice effect and role in immunoregulation in domestic cats. J Anim Sci 2016; 94: 124-134
• 31 Xu Z, Kong XQ. Bixin ameliorates high fat diet-iduced cardiac injury in mice through inflammation and oxidative stress supression. Biomed Pharmacother 2017; 89: 991-1004
• 32 Fontana L, Partridge L, Longo V. Dietary restriction, growth factors and aging: from yeast to humans. Science 2010; 328: 321-326
• 33 Carmona JJ, Michan S. Biology of healthy aging and longevity. Rev Inves Clin 2016; 68: 7-16
• 34 Zamberland DC, Amaral GP, Arantes LP, Machado ML, Mizdal CR, Campos MMA, Soares FAA. Rosmarinus officinalis L increases Caenorhabditis elegans stress resistance and longevity in a DAF-16, HSF-1 and SKN-1-dependent manner. Braz J Med Biol Res 2016; 49: e5235
• 35 Cabreiro F, Ackerman D, Doonan R, Araiz C, Back P, Papp D, Braeckman BP, Gems D. Increased life span from overexpression of superoxide dismutase in Caenorhabditis elegans is not caused by decreased oxidative damage. Free Radic Biol Med 2011; 51: 1575-1582
• 36 Jones DP. Redox theory of aging. Redox Biol 2015; 5: 71-79
• 37 Havermann S, Humpf HU, Wätjen W. Baicalein modulates stress-resistance and life span in C. elegans via SKN-1 but not DAF-16. Fitoterapia 2016; 113: 123-127
• 38 Havermann S, Chovolou Y, Humpf HU, Wätjen W. Caffeic acid phenethylester increases stress resistance and enhances lifespan in Caenorhabditis eleganse by modulation of the insulin-like DAF-16 signalling pathway. PLoS One 2014; 9: e100256
• 39 Briga M, Verhulst S. What can long-lived mutants tell us about mechanisms causing aging and lifespan variation in natural environments?. Exp Gerontol 2015; 71: 21-26
• 40 Saul N, Pietsch K, Stürzenbaum SR, Menzel R, Steinberg CE. Diversity of polyphenols action in Caenorhabditis elegans: between toxicity and longevity. J Nat Prod 2011; 26: 1713-1720
• 41 Rahmalia W, Fabre JF, Mouloungui Z. Effects of cyclohexane/acetone ratio on bixin extraction yield by accelerated solvent extraction method. Procedia Chem 2015; 12: 455-464
• 42 Mène-Saffrané L, Jones D, DellaPenna D. Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis . Proc Natl Acad Sci U S A 2010; 107: 7815-7820
• 43 Alavez S, Vantipalli MC, Zucker DJS, Klang IM, Lithgow GJ. Amyloid-binding compounds maintain protein homeostasis during ageing and extend lifespan. Nature 2011; 472: 226-229
• 44 Chen Y, Onken B, Chen H, Xiao S, Liu X, Driscoll M, Cao Y, Huang Q. Mechanisms of longevity extension of Caenorhabditis elegans induced by pentagalloyl glucose isolated from eucalyptus leaves. J Agric Food Chem 2014; 62: 3422-3431