Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-24T13:50:56.696Z Has data issue: false hasContentIssue false

Sex differences in the early life correlates of natural antibody concentrations

Published online by Cambridge University Press:  17 August 2015

A. C. Palmer*
Affiliation:
Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
K. J. Schulze
Affiliation:
Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
S. K. Khatry
Affiliation:
Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA Nepal Nutrition Intervention Project, Sarlahi, Nepal National Society for the Prevention of Blindness, Kathmandu, Nepal
L. M. De Luca
Affiliation:
Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
K. P. West Jr
Affiliation:
Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
*
*Address for correspondence: Dr A. C. Palmer, Department of International Health, Center for Human Nutrition, Johns Hopkins Bloomberg School of Public Health, 615 N. Wolfe Street, Baltimore, MD 21205, USA. (Email [email protected])

Abstract

Innate-like B1a lymphocytes arise from long-lived progenitors produced exclusively by fetal stem cells. Any insults coinciding with this early lymphopoietic wave could have a permanent impact on the B1a population and its unique protein products, the natural antibodies (NAb). We investigated early life nutritional influences on NAb concentrations of pre-adolescent children (n=290) in rural Nepal for whom we had extensive information on exposures from pregnancy and early infancy. Infant size and growth were strongly associated with NAb concentrations at 9–13 years of age among males (e.g., for neonatal weight: βBOYS=0.43; P<0.001), but not females (e.g., for neonatal weight: βGIRLS=−0.16; P=0.26). In females, season of birth was associated with NAb concentrations, with marked reductions among girls born during the pre-monsoon (March–May; βGIRLS=−0.39; P=0.01) and pre-harvest (September–November; βGIRLS=−0.35; P=0.03) seasons. Our findings suggest that nutritional or other environmental influences on immune development may vary by sex, with potential consequences for immune function during infancy and long-term risk of immune-mediated disease.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Palmer, AC. Nutritionally mediated programming of the developing immune system. Adv Nutr. 2011; 2, 377395.CrossRefGoogle ScholarPubMed
2. Moore, SE, Cole, TJ, Collinson, AC, et al.. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol. 1999; 28, 10881095.CrossRefGoogle ScholarPubMed
3. Moore, SE, Richards, AA, Goldblatt, D, et al.. Early-life and contemporaneous nutritional and environmental predictors of antibody response to vaccination in young Gambian adults. Vaccine. 2012; 30, 48424848.CrossRefGoogle ScholarPubMed
4. Moore, SE, Jalil, F, Ashraf, R, et al.. Birth weight predicts response to vaccination in adults born in an urban slum in Lahore, Pakistan. Am J Clin Nutr. 2004; 80, 453459.CrossRefGoogle Scholar
5. McDade, TW, Beck, MA, Kuzawa, C, Adair, LS. Prenatal undernutrition, postnatal environments, and antibody response to vaccination in adolescence. Am J Clin Nutr. 2001; 74, 543548.CrossRefGoogle ScholarPubMed
6. Fulford, AJ, Moore, SE, Arifeen, SE, et al. Disproportionate early fetal growth predicts postnatal thymic size in humans. J Dev Orig Health Dis. 2013; 4, 223231.CrossRefGoogle ScholarPubMed
7. Collinson, AC, Moore, SE, Cole, TJ, Prentice, AM. Birth season and environmental influences on patterns of thymic growth in rural Gambian infants. Acta Paediatr. 2003; 92, 10141020.CrossRefGoogle ScholarPubMed
8. Moore, SE, Collinson, AC, Tamba N’gom, P, Aspinall, R, Prentice, AM. Early immunological development and mortality from infectious disease in later life. Proc Nutr Soc. 2006; 65, 311318.CrossRefGoogle ScholarPubMed
9. McDade, TW, Beck, MA, Kuzawa, CW, Adair, LS. Prenatal undernutrition and postnatal growth are associated with adolescent thymic function. J Nutr. 2001; 131, 12251231.CrossRefGoogle ScholarPubMed
10. Dorshkind, K, Montecino-Rodriguez, E. Fetal B-cell lymphopoiesis and the emergence of B-1-cell potential. Nat Rev Immunol. 2007; 7, 213219.CrossRefGoogle ScholarPubMed
11. Baumgarth, N, Tung, JW, Herzenberg, LA. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin Immunopathol. 2005; 26, 347362.CrossRefGoogle ScholarPubMed
12. Avrameas, S. Natural autoantibodies: from ‘horror autotoxicus’ to ‘gnothi seauton’. Immunol Today. 1991; 12, 154159.Google ScholarPubMed
13. Coutinho, A, Kazatchkine, MD, Avrameas, S. Natural autoantibodies. Curr Opin Immunol. 1995; 7, 812818.CrossRefGoogle ScholarPubMed
14. Casali, P, Schettino, EW. Structure and function of natural antibodies. Curr Top Microbiol Immunol. 1996; 210, 167179.Google ScholarPubMed
15. Capolunghi, F, Rosado, MM, Sinibaldi, M, Aranburu, A, Carsetti, R. Why do we need IgM memory B cells? Immunol Lett. 2013; 152, 114120.CrossRefGoogle ScholarPubMed
16. Tsiantoulas, D, Diehl, CJ, Witztum, JL, Binder, CJ. B cells and humoral immunity in atherosclerosis. Circ Res. 2014; 114, 17431756.CrossRefGoogle ScholarPubMed
17. Vollmers, HP, Brandlein, S. Natural antibodies and cancer. N Biotechnol. 2009; 25, 294298.CrossRefGoogle ScholarPubMed
18. West, KP Jr, Katz, J, Khatry, SK, et al. Double blind, cluster randomised trial of low dose supplementation with vitamin A or beta carotene on mortality related to pregnancy in Nepal. The NNIPS-2 Study Group. BMJ. 1999; 318, 570575.CrossRefGoogle ScholarPubMed
19. Palmer, AC, Schulze, KJ, Khatry, SK, De Luca, LM, West, KP Jr. Maternal vitamin A supplementation increases natural antibody concentrations of preadolescent offspring in rural Nepal. Nutrition. 2015; 31, 813819.CrossRefGoogle ScholarPubMed
20. Wu, L, Katz, J, Mullany, LC, et al. Association between nutritional status and positive childhood disability screening using the ten questions plus tool in Sarlahi, Nepal. J Health Popul Nutr. 2010; 28, 585594.CrossRefGoogle ScholarPubMed
21. Christian, P, Katz, J, Wu, L, et al. Risk factors for pregnancy-related mortality: a prospective study in rural Nepal. Public Health. 2008; 122, 161172.CrossRefGoogle ScholarPubMed
22. Jiang, T, Christian, P, Khatry, SK, Wu, L, West, KP Jr. Micronutrient deficiencies in early pregnancy are common, concurrent, and vary by season among rural Nepali pregnant women. J Nutr. 2005; 135, 11061112.CrossRefGoogle ScholarPubMed
23. Christian, P, Khatry, SK, Katz, J, et al. Effects of alternative maternal micronutrient supplements on low birth weight in rural Nepal: double blind randomised community trial. BMJ. 2003; 326, 571.CrossRefGoogle ScholarPubMed
24. Mullany, LC, Katz, J, Li, YM, et al. Breast-feeding patterns, time to initiation, and mortality risk among newborns in southern Nepal. J Nutr. 2008; 138, 599603.CrossRefGoogle ScholarPubMed
25. Gibson, RS. Principles of Nutritional Assessment, 2nd edn, 2005. Oxford University Press: New York, NY.CrossRefGoogle Scholar
26. Hahn, BH. Antibodies to DNA. N Engl J Med. 1998; 338, 13591368.CrossRefGoogle ScholarPubMed
27. Witte, T, Hartung, K, Sachse, C, et al. IgM anti-dsDNA antibodies in systemic lupus erythematosus: negative association with nephritis. SLE study group. Rheumatol Int. 1998; 18, 8591.CrossRefGoogle ScholarPubMed
28. Merbl, Y, Zucker-Toledano, M, Quintana, FJ, Cohen, IR. Newborn humans manifest autoantibodies to defined self molecules detected by antigen microarray informatics. J Clin Invest. 2007; 117, 712718.CrossRefGoogle ScholarPubMed
29. Wärnberg, J, Nova, E, Romeo, J, et al.. Lifestyle-related determinants of inflammation in adolescence. Br J Nutr. 2007; 98, S116S120.CrossRefGoogle Scholar
30. Liang, KY, Zeger, SL. Regression analysis for correlated data. Annu Rev Public Health. 1993; 14, 4368.CrossRefGoogle ScholarPubMed
31. World Health Organization. WHO Child Growth Standards: Length/Height-for-Age, Weight-for-Age, Weight-for-Length, Weight-for-Height and Body Mass Index-for-Age: Methods and Development. 2006. World Health Organization: Geneva.Google Scholar
32. Butterworth, M, McClellan, B, Allansmith, M. Influence of sex in immunoglobulin levels. Nature. 1967; 214, 12241225.CrossRefGoogle ScholarPubMed
33. Halliday, GM, Salaman, MR, Seifert, MH, Johnson, KJ, Malcolm, AD. Evaluation of an ELISA system for determination of class-specific antibodies to native and denatured DNA in man. Ann Rheum Dis. 1985; 44, 507513.CrossRefGoogle ScholarPubMed
34. Clark, J, Bourne, T, Salaman, MR, Seifert, MH, Isenberg, DA. B lymphocyte hyperactivity in families of patients with systemic lupus erythematosus. J Autoimmun. 1996; 9, 5965.CrossRefGoogle ScholarPubMed
35. Hulthe, J, Wikstrand, J, Lidell, A, et al.. Antibody titers against oxidized LDL are not elevated in patients with familial hypercholesterolemia. Arterioscler Thromb Vasc Biol. 1998; 18, 12031211.CrossRefGoogle Scholar
36. Frostegard, J, Tao, W, Georgiades, A, et al.. Atheroprotective natural anti-phosphorylcholine antibodies of IgM subclass are decreased in Swedish controls as compared to non-westernized individuals from New Guinea. Nutr Metab (Lond). 2007; 4, 7.CrossRefGoogle ScholarPubMed
37. Lleo, A, Battezzati, PM, Selmi, C, Gershwin, ME, Podda, M. Is autoimmunity a matter of sex? Autoimmun Rev. 2008; 7, 626630.CrossRefGoogle ScholarPubMed
38. Rah, JH, Shamim, AA, Arju, UT, et al.. Age of onset, nutritional determinants, and seasonal variations in menarche in rural Bangladesh. J Health Popul Nutr. 2009; 27, 802807.Google ScholarPubMed
39. Hughes, MM, Katz, J, Mullany, LC, et al. Seasonality of birth outcomes in rural Sarlahi District, Nepal: a population-based prospective cohort. BMC Pregnancy Childbirth. 2014; 14, 310.CrossRefGoogle Scholar
40. Panter-Brick, C. Seasonal growth patterns in rural Nepali children. Ann Hum Biol. 1997; 24, 118.CrossRefGoogle ScholarPubMed
41. Ngom, PT, Collinson, AC, Pido-Lopez, J, et al.. Improved thymic function in exclusively breastfed infants is associated with higher interleukin 7 concentrations in their mothers’ breast milk. Am J Clin Nutr. 2004; 80, 722728.CrossRefGoogle ScholarPubMed
42. Prentice, AM, Cole, TJ, Moore, SE, Collinson, AC. Programming the adult immune system. In Fetal Programming: Influence on Development and Disease in Later Life Proceedings of the 36th RCOG Study Group (eds. O’Brien PMS, Wheeler T, Barker DJP), 1999; pp. 399423. John Libbey & Son: London.Google Scholar
43. Turner, PC, Moore, SE, Hall, AJ, Prentice, AM, Wild, CP. Modification of immune function through exposure to dietary aflatoxin in Gambian children. Environ Health Perspect. 2003; 111, 217220.CrossRefGoogle ScholarPubMed
44. Ofordile, ON, Prentice, AM, Moore, SE, Holladay, SD. Early pesticide exposure and later mortality in rural Africa: a new hypothesis. J Immunotoxicol. 2005; 2, 3340.CrossRefGoogle Scholar
45. Waterland, RA, Kellermayer, R, Laritsky, E, et al. Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet. 2010; 6, e1001252.CrossRefGoogle ScholarPubMed
46. Panter-Brick, C, Ellison, PT. Seasonality of workloads and ovarian function in Nepali women. Ann N Y Acad Sci. 1994; 709, 234235.CrossRefGoogle ScholarPubMed
47. Victora, GD, Bilate, AMB, Socorro-Silva, A, et al. Mother–child immunological interactions in early life affect long-term humoral autoreactivity to heat shock protein 60 at age 18 years. J Autoimmun. 2007; 29, 3843.CrossRefGoogle ScholarPubMed
48. Phillips, DI, Cooper, C, Fall, C, et al. Fetal growth and autoimmune thyroid disease. Q J Med. 1993; 86, 247253.Google ScholarPubMed
49. Edwards, CJ, Syddall, H, Goswami, R, et al.. Infections in infancy and the presence of antinuclear antibodies in adult life. Lupus. 2006; 15, 213217.CrossRefGoogle ScholarPubMed
50. Tarrade, A, Panchenko, P, Junien, C, Gabory, A. Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J Exp Biol. 2015; 218, 5058.CrossRefGoogle ScholarPubMed
51. Cox, LA, Li, C, Glenn, JP, et al. Expression of the placental transcriptome in maternal nutrient reduction in baboons is dependent on fetal sex. J Nutr. 2013; 143, 16981708.CrossRefGoogle ScholarPubMed
52. Gabory, A, Ferry, L, Fajardy, I, et al. Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS One. 2012; 7, e47986.CrossRefGoogle ScholarPubMed
53. Mao, J, Zhang, X, Sieli, PT, et al.. Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta. Proc Natl Acad Sci U S A. 2010; 107, 55575562.CrossRefGoogle ScholarPubMed
54. Chen, PY, Ganguly, A, Rubbi, L, et al. Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiol Genomics. 2013; 45, 565576.CrossRefGoogle ScholarPubMed
55. Gabory, A, Roseboom, TJ, Moore, T, Moore, LG, Junien, C. Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol Sex Differences. 2013; 4, 5.CrossRefGoogle Scholar
56. Janeway, C, Travers, PJ, Walport, M, Shlomchik, MJ. Immunobiology: The Immune System in Health and Disease, 6th edn, 2005. Garland Science Publishing: New York, NY.Google Scholar
57. Carsetti, R, Rosado, MM, Wardmann, H. Peripheral development of B cells in mouse and man. Immunol Rev. 2004; 197, 179191.CrossRefGoogle ScholarPubMed
58. Azizah, MR, Azila, MN, Zulkifli, MN, Norita, TY. The prevalence of antinuclear, anti-dsDNA, anti-Sm and anti-RNP antibodies in a group of healthy blood donors. Asian Pac J Allergy Immunol. 1996; 14, 125128.Google Scholar
59. Williams, WM, Isenberg, DA. A cross-sectional study of anti-DNA antibodies in the serum and IgG and IgM fraction of healthy individuals, patients with systemic lupus erythematosus and their relatives. Lupus. 1996; 5, 576586.CrossRefGoogle ScholarPubMed
60. Binder, CJ. Natural IgM antibodies against oxidation-specific epitopes. J Clin Immunol. 2010; 30(Suppl. 1), S56S60.CrossRefGoogle ScholarPubMed
61. Watzlawik, JO, Wootla, B, Painter, MM, Warrington, AE, Rodriguez, M. Cellular targets and mechanistic strategies of remyelination-promoting IgMs as part of the naturally occurring autoantibody repertoire. Expert Rev Neurother. 2013; 13, 10171029.CrossRefGoogle ScholarPubMed
62. Holodick, NE, Tumang, JR, Rothstein, TL. Immunoglobulin secretion by B1 cells: differential intensity and IRF4-dependence of spontaneous IgM secretion by peritoneal and splenic B1 cells. Eur J Immunol. 2010; 40, 30073016.CrossRefGoogle ScholarPubMed
63. Fesel, C, Goulart, LF, Silva Neto, A, et al. Increased polyclonal immunoglobulin reactivity toward human and bacterial proteins is associated with clinical protection in human Plasmodium infection. Malar J. 2005; 4, 5.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Palmer supplementary material

Palmer supplementary material 1

Download Palmer supplementary material(PDF)
PDF 60 KB