Agrarian diet and diseases of affluence--do evolutionary novel dietary lectins cause leptin resistance?

Tommy Jönsson, Stefan Olsson, Bo Ahrén, Thorkild C Bøg-Hansen, Anita Dole, Staffan Lindeberg, Tommy Jönsson, Stefan Olsson, Bo Ahrén, Thorkild C Bøg-Hansen, Anita Dole, Staffan Lindeberg

Abstract

Background: The global pattern of varying prevalence of diseases of affluence, such as obesity, cardiovascular disease and diabetes, suggests that some environmental factor specific to agrarian societies could initiate these diseases.

Presentation of the hypothesis: We propose that a cereal-based diet could be such an environmental factor. Through previous studies in archaeology and molecular evolution we conclude that humans and the human leptin system are not specifically adapted to a cereal-based diet, and that leptin resistance associated with diseases of affluence could be a sign of insufficient adaptation to such a diet. We further propose lectins as a cereal constituent with sufficient properties to cause leptin resistance, either through effects on metabolism central to the proper functions of the leptin system, and/or directly through binding to human leptin or human leptin receptor, thereby affecting the function.

Testing the hypothesis: Dietary interventions should compare effects of agrarian and non-agrarian diets on incidence of diseases of affluence, related risk factors and leptin resistance. A non-significant (p = 0.10) increase of cardiovascular mortality was noted in patients advised to eat more whole-grain cereals. Our lab conducted a study on 24 domestic pigs in which a cereal-free hunter-gatherer diet promoted significantly higher insulin sensitivity, lower diastolic blood pressure and lower C-reactive protein as compared to a cereal-based swine feed. Testing should also evaluate the effects of grass lectins on the leptin system in vivo by diet interventions, and in vitro in various leptin and leptin receptor models. Our group currently conducts such studies.

Implications of the hypothesis: If an agrarian diet initiates diseases of affluence it should be possible to identify the responsible constituents and modify or remove them so as to make an agrarian diet healthier.

References

    1. McKeown T. The origins of human disease. , Basil Blackwell; 1988. p. vi,233p..
    1. Trowell HC, Burkitt DP. Western diseases: their emergence and prevention. London, Edward Arnold; 1981.
    1. Temple NJ, Burkitt DP. Western diseases : their dietary prevention and reversibility. Totowa, N.J., Humana Press; 1994. p. xiii, 453 p..
    1. Semaw S, Rogers MJ, Quade J, Renne PR, Butler RF, Dominguez-Rodrigo M, Stout D, Hart WS, Pickering T, Simpson SW. 2.6-Million-year-old stone tools and associated bones from OGS-6 and OGS-7, Gona, Afar, Ethiopia. J Hum Evol. 2003;45:169–177.
    1. Lindeberg S, Cordain L, Eaton B. Biological and Clinical Potential of a Palaeolithic Diet. Journal of Nutritional & Environmental Medicine. 2003;13:149–160.
    1. King H, Aubert RE, Herman WH. Global burden of diabetes, 1995-2025: prevalence, numerical estimates, and projections. Diabetes Care. 1998;21:1414–1431.
    1. van Dam RM. The epidemiology of lifestyle and risk for type 2 diabetes. Eur J Epidemiol. 2003;18:1115–1125.
    1. Walker AR, Walker BF, Segal I. Some puzzling situations in the onset, occurrence and future of coronary heart disease in developed and developing populations, particularly such in sub-Saharan Africa. J R Soc Health. 2004;124:40–46.
    1. Hu FB, Leitzmann MF, Stampfer MJ, Colditz GA, Willett WC, Rimm EB. Physical activity and television watching in relation to risk for type 2 diabetes mellitus in men. Arch Intern Med. 2001;161:1542–1548.
    1. Feigin VL, Lawes CM, Bennett DA, Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol. 2003;2:43–53.
    1. Hu FB. Protein, body weight, and cardiovascular health. Am J Clin Nutr. 2005;82:242S–247S.
    1. Kromhout D. Epidemiology of cardiovascular diseases in Europe. Public Health Nutr. 2001;4:441–457.
    1. Pavan L, Casiglia E, Braga LM, Winnicki M, Puato M, Pauletto P, Pessina AC. Effects of a traditional lifestyle on the cardiovascular risk profile: the Amondava population of the Brazilian Amazon. Comparison with matched African, Italian and Polish populations. J Hypertens. 1999;17:749–756.
    1. Lindeberg S. Apparent absence of cerebrocardiovascular disease in Melanesians. Risk factors and nutritional considerations - the Kitava Study. , University of Lund; 1994.
    1. Lindeberg S. Stroke in Papua New Guinea. Lancet Neurol. 2003;2:273; discussion 273.
    1. Dobzhansky T. Nothing in Biology Makes Sense Except in the Light of Evolution. American Biology Teacher. 1973;35:125–129.
    1. Willis KJ, McElwain JC. The evolution of plants. Oxford, Oxford University Press; 2002. p. x, 378 p. : ill. ; 25 cm., pbk..
    1. Sargis EJ. Paleontology. Primate origins nailed. Science. 2002;298:1564–1565.
    1. Jones S, Martin R, Pilbeam D. The Cambridge encyclopedia of human evolution. Cambridge, Cambridge University Press; 1992.
    1. Wood B, Brooks A. Human evolution. We are what we ate. Nature. 1999;400:219–220.
    1. Preuschoft H. Mechanisms for the acquisition of habitual bipedality: are there biomechanical reasons for the acquisition of upright bipedal posture? J Anat. 2004;204:363–384.
    1. Pickford M. Palaeoenvironments and hominoid evolution. Z Morphol Anthropol. 2002;83:337–348.
    1. Bramble DM, Lieberman DE. Endurance running and the evolution of Homo. Nature. 2004;432:345–352.
    1. Milton K. In: Primate Diets and Gut Morphology: Implications for Hominid Evolution: ; Philadelphia. Ross Eric B, Harris M and Wenner-Gren Foundation for Anthropological R, editor. Temple University Press; 1987. pp. pp 93–115.
    1. Richards MP. A brief review of the archaeological evidence for Palaeolithic and Neolithic subsistence. Eur J Clin Nutr. 2002;56:16 p following 1262.
    1. McDougall I, Brown FH, Fleagle JG. Stratigraphic placement and age of modern humans from Kibish, Ethiopia. Nature. 2005;433:733–736.
    1. Ingman M, Kaessmann H, Paabo S, Gyllensten U. Mitochondrial genome variation and the origin of modern humans. Nature. 2000;408:708–713.
    1. Kuhn SL, Stiner MC. The Antiquity of Hunter-gatherers. In: Panter-Brick C, Rowley-Conwy P and Layton R, editor. Hunter-gatherers : an interdisciplinary perspective. Cambridge, Cambridge University Press; 2001. pp. pp 99–142. (The Biosocial Society symposium series).
    1. Cronin CC, Shanahan F. Why is celiac disease so common in Ireland? Perspect Biol Med. 2001;44:342–352.
    1. Rostami K, Malekzadeh R, Shahbazkhani B, Akbari MR, Catassi C. Coeliac disease in Middle Eastern countries: a challenge for the evolutionary history of this complex disorder? Dig Liver Dis. 2004;36:694–697.
    1. Freeman S, Herron JC. Evolutionary analysis. 3rd ed. , Upper Saddle River; 2004. p. xiv, 802 p..
    1. Veniant MM, LeBel CP. Leptin: from animals to humans. Curr Pharm Des. 2003;9:811–818.
    1. El-Haschimi K, Lehnert H. Leptin resistance - or why leptin fails to work in obesity. Exp Clin Endocrinol Diabetes. 2003;111:2–7.
    1. El-Haschimi K, Pierroz DD, Hileman SM, Bjorbaek C, Flier JS. Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J Clin Invest. 2000;105:1827–1832.
    1. Halaas JL, Boozer C, Blair-West J, Fidahusein N, Denton DA, Friedman JM. Physiological response to long-term peripheral and central leptin infusion in lean and obese mice. Proc Natl Acad Sci U S A. 1997;94:8878–8883.
    1. Jequier E. Leptin signaling, adiposity, and energy balance. Ann N Y Acad Sci. 2002;967:379–388.
    1. Frederich RC, Hamann A, Anderson S, Lollmann B, Lowell BB, Flier JS. Leptin levels reflect body lipid content in mice: evidence for diet-induced resistance to leptin action. Nat Med. 1995;1:1311–1314.
    1. Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S, et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med. 1995;1:1155–1161.
    1. Unger RH. Longevity, lipotoxicity and leptin: the adipocyte defense against feasting and famine. Biochimie. 2005;87:57–64.
    1. Trayhurn P. Leptin--a critical body weight signal and a "master" hormone? Sci STKE. 2003;2003:PE7.
    1. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL. Serum immunoreactive-leptin concentrations in normal-weight and obese humans [see comments] N Engl J Med. 1996;334:292–295.
    1. Jameson JL. Molecular mechanisms of end-organ resistance. Growth Horm IGF Res. 2004;14 Suppl A:S45–50.
    1. Gaucher EA, Miyamoto MM, Benner SA. Evolutionary, structural and biochemical evidence for a new interaction site of the leptin obesity protein. Genetics. 2003;163:1549–1553.
    1. Doyon C, Drouin G, Trudeau VL, Moon TW. Molecular evolution of leptin. Gen Comp Endocrinol. 2001;124:188–198.
    1. Hoyo Josep , Arlott N, Elliott A, Sargatal J, Bierregaard R. Handbook of the birds of the world. Barcelona, Lynx Edicions; 1994. p. 638p.
    1. Nowak Ronald M, Walker Ernest P. Walker's mammals of the world. 5th ed. Baltimore, Johns Hopkins University Press; 1991.
    1. Corbet GB, Harris S, Mammal S. The handbook of British mammals. 3rd. ed. Oxford, Blackwell Scientific; 1991. p. 588p ; 26cm.
    1. Van Damme JME. Handbook of plant lectins : properties and biomedical applications. Chichester, John Wiley; 1998. p. xiv, 452p : ill ; 26cm.
    1. Sharon N, Lis H. Lectins. 2nd ed. Dordrecht ; London, Kluwer Academic Publishers; 2003. p. xviii, 454 p..
    1. Kolberg J, Wedege E, Sollid L. Immunoblotting detection of lectins in gluten and white rice flour. Biochem Biophys Res Commun. 1987;142:717–723.
    1. Silano M, De Vincenzi M. Bioactive antinutritional peptides derived from cereal prolamins: a review. Nahrung. 1999;43:175–184.
    1. Di Cagno R, De Angelis M, Lavermicocca P, De Vincenzi M, Giovannini C, Faccia M, Gobbetti M. Proteolysis by sourdough lactic acid bacteria: effects on wheat flour protein fractions and gliadin peptides involved in human cereal intolerance. Appl Environ Microbiol. 2002;68:623–633.
    1. Mercenier A, Pavan S, Pot B. Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr Pharm Des. 2003;9:175–191.
    1. Shewry PR, Halford NG. Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot. 2002;53:947–958.
    1. Minetti M, Aducci P, Teichner A. A new agglutinating activity from wheat flour inhibited by tryptophan. Biochim Biophys Acta. 1976;437:505–517.
    1. Nachbar MS, Oppenheim JD. Lectins in the United States diet: a survey of lectins in commonly consumed foods and a review of the literature. Am J Clin Nutr. 1980;33:2338–2345.
    1. Freed DLJ. Lectins in food: Their importance in health and disease. Journal of Nutritional Medicine. 1991;2:45–65.
    1. Wang Q, Yu LG, Campbell BJ, Milton JD, Rhodes JM. Identification of intact peanut lectin in peripheral venous blood. Lancet. 1998;352:1831–1832.
    1. Freed DL. Do dietary lectins cause disease? Bmj. 1999;318:1023–1024.
    1. Wang XY, Bergdahl K, Heijbel A, Liljebris C, Bleasdale JE. Analysis of in vitro interactions of protein tyrosine phosphatase 1B with insulin receptors. Mol Cell Endocrinol. 2001;173:109–120.
    1. Zeng FY, Benguria A, Kafert S, Andre S, Gabius HJ, Villalobo A. Differential response of the epidermal growth factor receptor tyrosine kinase activity to several plant and mammalian lectins. Mol Cell Biochem. 1995;142:117–124.
    1. Ponzio G, Debant A, Contreres JO, Rossi B. Wheat-germ agglutinin mimics metabolic effects of insulin without increasing receptor autophosphorylation. Cell Signal. 1990;2:377–386.
    1. Livingston JN, Purvis BJ. The effects of wheat germ agglutinin on the adipocyte insulin receptor. Biochim Biophys Acta. 1981;678:194–201.
    1. Hedo JA, Harrison LC, Roth J. Binding of insulin receptors to lectins: evidence for common carbohydrate determinants on several membrane receptors. Biochemistry. 1981;20:3385–3393.
    1. Fujii M, Sugamura K, Nakamura M, Ishii T, Hinuma Y. Selective inhibition of high- but not low-affinity interleukin 2 binding by lectins and anti-interleukin 2 receptor alpha antibody. Microbiol Immunol. 1988;32:857–867.
    1. Kilpatrick DC. Mechanisms and assessment of lectin-mediated mitogenesis. Mol Biotechnol. 1999;11:55–65.
    1. Ohmori T, Yatomi Y, Wu Y, Osada M, Satoh K, Ozaki Y. Wheat germ agglutinin-induced platelet activation via platelet endothelial cell adhesion molecule-1: involvement of rapid phospholipase C gamma 2 activation by Src family kinases. Biochemistry. 2001;40:12992–13001.
    1. Banks WA, Ibrahimi F, Farr SA, Flood JF, Morley JE. Effects of wheatgerm agglutinin and aging on the regional brain uptake of HIV-1GP120. Life Sci. 1999;65:81–89.
    1. Villegas JC, Broadwell RD. Transcytosis of protein through the mammalian cerebral epithelium and endothelium. II. Adsorptive transcytosis of WGA-HRP and the blood-brain and brain-blood barriers. J Neurocytol. 1993;22:67–80.
    1. Mares V, Borges LF, Sidman RL. Uptake and transport of lectins from the cerebrospinal fluid by cells of the immature mouse brain. Acta Histochem. 1984;74:11–19.
    1. Cordain L, Toohey L, Smith MJ, Hickey MS. Modulation of immune function by dietary lectins in rheumatoid arthritis. Br J Nutr. 2000;83:207–217.
    1. Geleff S, Bock P. Pancreatic duct glands. II. Lectin binding affinities of ductular epithelium, ductular glands, and Brunner glands. Histochemistry. 1984;80:31–38.
    1. Gabor F, Klausegger U, Wirth M. The interaction between wheat germ agglutinin and other plant lectins with prostate cancer cells Du-145. Int J Pharm. 2001;221:35–47.
    1. Davis HR, Glagov S. Lectin binding to distinguish cell types in fixed atherosclerotic arteries. Atherosclerosis. 1986;61:193–203.
    1. Kagami H, Uryu K, Okamoto K, Sakai H, Kaneda T, Sakanaka M. Differential lectin binding on walls of thoraco-cervical blood vessels and lymphatics in rats. Okajimas Folia Anat Jpn. 1991;68:161–170.
    1. Tchernychev B, Wilchek M. Natural human antibodies to dietary lectins. FEBS Lett. 1996;397:139–142.
    1. Shechter Y. Bound lectins that mimic insulin produce persistent insulin-like activities. Endocrinology. 1983;113:1921–1926.
    1. Cuatrecasas P, Tell GP. Insulin-like activity of concanavalin A and wheat germ agglutinin--direct interactions with insulin receptors. Proc Natl Acad Sci U S A. 1973;70:485–489.
    1. Damm I, Mikkat U, Kirchhoff F, Bockmann S, Jonas L. Inhibitory effect of the lectin wheat germ agglutinin on the binding of 125I-CCK-8s to the CCK-A and -B receptors of AR42J cells. Pancreas. 2004;28:31–37.
    1. Lascols O, Cherqui G, Munier A, Picard J, Capeau J. Differences in both glycosylation and binding properties between rat and mouse liver prolactin receptors. Cell Mol Biol (Noisy-le-grand) 1994;40:359–371.
    1. Chochola J, Fabre C, Bellan C, Luis J, Bourgerie S, Abadie B, Champion S, Marvaldi J, el Battari A. Structural and functional analysis of the human vasoactive intestinal peptide receptor glycosylation. Alteration of receptor function by wheat germ agglutinin. J Biol Chem. 1993;268:2312–2318.
    1. Johnson RJ, Simpson S, Van Epps DE, Chenoweth DE. Wheat germ agglutinin inhibits the C5a receptor interaction: implications for receptor microheterogeneity and ligand binding site. J Leukoc Biol. 1992;52:3–10.
    1. Elliott S, Lorenzini T, Asher S, Aoki K, Brankow D, Buck L, Busse L, Chang D, Fuller J, Grant J, Hernday N, Hokum M, Hu S, Knudten A, Levin N, Komorowski R, Martin F, Navarro R, Osslund T, Rogers G, Rogers N, Trail G, Egrie J. Enhancement of therapeutic protein in vivo activities through glycoengineering. Nat Biotechnol. 2003;21:414–421.
    1. Lammert A, Brockmann G, Renne U, Kiess W, Bottner A, Thiery J, Kratzsch J. Different isoforms of the soluble leptin receptor in non-pregnant and pregnant mice. Biochem Biophys Res Commun. 2002;298:798–804.
    1. Quinton ND, Lee AJ, Ross RJ, Eastell R, Blakemore AI. A single nucleotide polymorphism (SNP) in the leptin receptor is associated with BMI, fat mass and leptin levels in postmenopausal Caucasian women. Hum Genet. 2001;108:233–236.
    1. Thompson DB, Ravussin E, Bennett PH, Bogardus C. Structure and sequence variation at the human leptin receptor gene in lean and obese Pima Indians. Hum Mol Genet. 1997;6:675–679.
    1. Stefan N, Vozarova B, Del Parigi A, Ossowski V, Thompson DB, Hanson RL, Ravussin E, Tataranni PA. The Gln223Arg polymorphism of the leptin receptor in Pima Indians: influence on energy expenditure, physical activity and lipid metabolism. Int J Obes Relat Metab Disord. 2002;26:1629–1632.
    1. Chagnon YC, Chung WK, Perusse L, Chagnon M, Leibel RL, Bouchard C. Linkages and associations between the leptin receptor (LEPR) gene and human body composition in the Quebec Family Study. Int J Obes Relat Metab Disord. 1999;23:278–286.
    1. Wauters M, Mertens I, Chagnon M, Rankinen T, Considine RV, Chagnon YC, Van Gaal LF, Bouchard C. Polymorphisms in the leptin receptor gene, body composition and fat distribution in overweight and obese women. Int J Obes Relat Metab Disord. 2001;25:714–720.
    1. Ukkola O, Tremblay A, Despres JP, Chagnon YC, Campfield LA, Bouchard C. Leptin receptor Gln223Arg variant is associated with a cluster of metabolic abnormalities in response to long-term overfeeding. J Intern Med. 2000;248:435–439.
    1. Lakka TA, Rankinen T, Weisnagel SJ, Chagnon YC, Lakka HM, Ukkola O, Boule N, Rice T, Leon AS, Skinner JS, Wilmore JH, Rao DC, Bergman R, Bouchard C. Leptin and leptin receptor gene polymorphisms and changes in glucose homeostasis in response to regular exercise in nondiabetic individuals: the HERITAGE family study. Diabetes. 2004;53:1603–1608.
    1. Burr ML, Fehily AM, Gilbert JF, Rogers S, Holliday RM, Sweetnam PM, Elwood PC, Deadman NM. Effects of changes in fat, fish, and fibre intakes on death and myocardial reinfarction: diet and reinfarction trial (DART) [see comments] Lancet. 1989;2:757–761.
    1. van Dam RM, Rimm EB, Willett WC, Stampfer MJ, Hu FB. Dietary patterns and risk for type 2 diabetes mellitus in U.S. men. Ann Intern Med. 2002;136:201–209.
    1. Koh-Banerjee P, Franz M, Sampson L, Liu S, Jacobs DRJ, Spiegelman D, Willett W, Rimm E. Changes in whole-grain, bran, and cereal fiber consumption in relation to 8-y weight gain among men. Am J Clin Nutr. 2004;80:1237–1245.
    1. Wu Z, Bidlingmaier M, Liu C, De Souza EB, Tschop M, Morrison KM, Strasburger CJ. Quantification of the soluble leptin receptor in human blood by ligand-mediated immunofunctional assay. J Clin Endocrinol Metab. 2002;87:2931–2939.
    1. Landt M, Horowitz JF, Coppack SW, Klein S. Effect of short-term fasting on free and bound leptin concentrations in lean and obese women. J Clin Endocrinol Metab. 2001;86:3768–3771.
    1. Lindgarde F, Ercilla MB, Correa LR, Ahren B. Body adiposity, insulin, and leptin in subgroups of peruvian amerindians. High Alt Med Biol. 2004;5:27–31.
    1. Lindgarde F, Widen I, Gebb M, Ahren B. Traditional versus agricultural lifestyle among Shuar women of the Ecuadorian Amazon: effects on leptin levels. Metabolism. 2004;53:1355–1358.
    1. Magni P, Liuzzi A, Ruscica M, Dozio E, Ferrario S, Bussi I, Minocci A, Castagna A, Motta M, Savia G. Free and bound plasma leptin in normal weight and obese men and women: relationship with body composition, resting energy expenditure, insulin-sensitivity, lipid profile and macronutrient preference. Clin Endocrinol (Oxf) 2005;62:189–196.

Source: PubMed

Подписаться