Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-26T04:28:11.627Z Has data issue: false hasContentIssue false

Impact of the harsh Antarctic environment on mucosal immunity

Published online by Cambridge University Press:  08 September 2021

Brij Bhushan
Affiliation:
Defence Institute of Physiology and Allied Sciences (DIPAS), DRDO, Lucknow Road, Timarpur, New Delhi110054, India
Himanshi Tanwar
Affiliation:
Defence Institute of Physiology and Allied Sciences (DIPAS), DRDO, Lucknow Road, Timarpur, New Delhi110054, India
Malleswara Rao Eslavath
Affiliation:
Defence Institute of Physiology and Allied Sciences (DIPAS), DRDO, Lucknow Road, Timarpur, New Delhi110054, India
Shashi Bala Singh
Affiliation:
National Institute of Pharmaceutical Education and Research (NIPER), NH 9, Kukatpally Industrial Estate, Balanagar, Hyderabad, Telangana500037, India
Bhuvnesh Kumar
Affiliation:
Defence Institute of Physiology and Allied Sciences (DIPAS), DRDO, Lucknow Road, Timarpur, New Delhi110054, India
Lilly Ganju*
Affiliation:
Defence Institute of Physiology and Allied Sciences (DIPAS), DRDO, Lucknow Road, Timarpur, New Delhi110054, India

Abstract

Mucosal immunity of Indian Antarctic personnel was analysed during the 34th Indian Scientific Expedition to Antarctica (ISEA) by ship voyage. Serum and salivary IgA, IgA1 and IgA2 levels along with salivary cortisol and TGF-β were quantified by enzyme-linked immunosorbent assay. Samples were collected at three different time points (T1, T2 and T3) during the expedition. Serum and salivary IgA, IgA1 and IgA2 concentrations incrementally increased towards the end of the expedition as compared to the beginning of the expedition. Salivary IgA and TGF-β levels were significantly altered during the expedition. Levels of IgA1 (P = 0.0007) and IgA2 (P = 0.0135) increased significantly at T3 as compared to T1. Additionally, significant changes in serum IgA were observed, with peak levels at T3 (P = 0.0015) and T2 (P < 0.001). However, the level of serum IgA2 was also significantly altered at T3 (P < 0.05) and T2 (P = 0.0006) in comparison with T1. The exact cause of the changes in serum and salivary IgA, IgA1, IgA2 and TGF-β levels during the summer expedition are unknown; however, the changes are evident in mucosal immunity.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2021

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

Bhatia, A. & Pal, R. 2012. Morbidity pattern of the 27th Indian Scientific Expedition to Antarctica. Wilderness and Environmental Medicine, 23, 231238.CrossRefGoogle ScholarPubMed
Bishop, N.C. & Gleeson, M. 2009. Acute and chronic effects of exercise on markers of mucosal immunity. Frontiers in Bioscience, 14, 44444456.CrossRefGoogle ScholarPubMed
Brandtzaeg, P. 2009. Mucosal immunity: induction, dissemination, and effector functions. Scandinavian Journal of Immunology, 70, 505515.CrossRefGoogle ScholarPubMed
Brandtzaeg, P. & Johansen, F.E. 2005. Mucosal B cells: phenotypic characteristics, transcriptional regulation, and homing properties. Immunological Reviews, 206, 3263.CrossRefGoogle ScholarPubMed
Brenner, I., Shek, P.N. & Shephard, R.J. 1998. Stress hormones and the immunological responses to heat and exercise. International Journal of Sports Medicine, 19, 130143.CrossRefGoogle ScholarPubMed
Bruno, M.E., Rogier, E.W., Frantz, A.L., Stefka, A.T., Thompson, S.N. & Kaetzel, C.S. 2010. Regulation of the polymeric immunoglobulin receptor in intestinal epithelial cells by Enterobacteriaceae: implications for mucosal homeostasis. Immunological Investigations, 39, 356382.CrossRefGoogle ScholarPubMed
Carrère, S., Evans, G.W. & Stokols, D. 1991. Winter-over stress: physiological and psychological adaptation to an Antarctic isolated and confined environment. In Harrison, A.A., Clearwater, Y.A. & McKay, C.P., eds. From Antarctica to outer space. New York: Springer, 229237.CrossRefGoogle Scholar
Cattermole, T.J. 1999. The epidemiology of cold injury in Antarctica. Aviation, Space, and Environmental Medicine, 70, 135140.Google ScholarPubMed
Cavas, L., Arpinar, P. & Yurdakoc, K. 2005. Possible interactions between antioxidant enzymes and free sialic acids in saliva: a preliminary study on elite judoists. International Journal of Sports Medicine, 26, 832835.CrossRefGoogle Scholar
Cerutti, A. & Rescigno, M. 2008. The biology of intestinal immunoglobulin A responses. Immunity, 28, 740750.CrossRefGoogle ScholarPubMed
Cunningham-Rundles, C. 2001. Physiology of IgA and IgA deficiency. Journal of Clinical Immunology, 21, 303309.CrossRefGoogle ScholarPubMed
Delacroix, D.L., Dive, C., Rambaud, J.C. & Vaerman, J.P. 1982. IgA subclasses in various secretions and in serum. Immunology, 47, 383.Google ScholarPubMed
Dhabhar, F.S. & McEwen, B.S. 1997. Acute stress enhances while chronic stress suppresses cell-mediated immunity in vivo: a potential role for leukocyte trafficking. Brain, Behavior, and Immunity, 11, 286306.CrossRefGoogle ScholarPubMed
Drago-Serrano, M.E., Rivera-Aguilar, V., Reséndiz-Albor, A.A. & Campos-Rodríguez, R. 2010. Lactoferrin increases both resistance to Salmonella typhimurium infection and the production of antibodies in mice. Immunology Letters, 134, 3546.CrossRefGoogle ScholarPubMed
Fahlman, M.M., Engels, H.J., Morgan, A.L. & Kolokouri, I. 2001. Mucosal IgA response to repeated Wingate tests in females. International Journal of Sports Medicine, 22, 127131.CrossRefGoogle ScholarPubMed
Flavell, R.A., Sanjabi, S., Wrzesinski, S.H. & Licona-Limón, P. 2010. The polarization of immune cells in the tumour environment by TGFβ. Nature Reviews Immunology, 10, 554567.CrossRefGoogle ScholarPubMed
Fox, R.I. & Stern, M. 2002. Sjögren's syndrome: mechanisms of pathogenesis involve interaction of immune and neurosecretory systems. Scandinavian Journal of Rheumatology, 31, 313.Google Scholar
Gleeson, M. 2000. Mucosal immune responses and risk of respiratory illness in elite athletes. Exercise Immunology Review, 6, 542.Google ScholarPubMed
Gleeson, M., Hall, S.T., McDonald, W.A., Flanagan, A.J. & Clancy, R.L. 1999. Salivary IgA subclasses and infection risk in elite swimmers. Immunology and Cell Biology, 77, 351355.CrossRefGoogle ScholarPubMed
Graves, D. 2008. Cytokines that promote periodontal tissue destruction. Journal of Periodontology, 79, 15851591.CrossRefGoogle ScholarPubMed
Hübner-Woźniak, E., Sendecki, W. & Borkowski, L. 1998. The effect of maximal 30 s exercise on salivary immunoglobulin A. Biology of Sport, 15, 6164.Google Scholar
Hübner-Woźniak, E., Lutosławska, G., Sendecki, W. & Sitkowski, D. 1997. Exercise-induced changes in salivary immunoglobulin A levels. Biology of Sport, 14, 299304.Google Scholar
Jarillo-Luna, A., Rivera-Aguilar, V., Garfias, H.R., Lara-Padilla, E., Kormanovsky, A. & Campos-Rodríguez, R. 2007. Effect of repeated restraint stress on the levels of intestinal IgA in mice. Psychoneuroendocrinology, 32, 681692.CrossRefGoogle ScholarPubMed
Kerr, M.A. 1990. The structure and function of human IgA. Biochemical Journal, 271, 285296.CrossRefGoogle ScholarPubMed
Khan, S.F., Katti, G., Baba, I. & Khan, N. 2015. Age-related changes of salivary IgA among healthy subjects. Journal of Indian Academy of Oral Medicine and Radiology, 27, 203.CrossRefGoogle Scholar
Klentrou, P., Cieslak, T., MacNeil, M., Vintinner, A. & Plyley, M. 2002. Effect of moderate exercise on salivary immunoglobulin A and infection risk in humans. European Journal of Applied Physiology, 87, 153158.CrossRefGoogle ScholarPubMed
Lou, Z., Gu, X.H. & Zhong, H.Z. 2015. Medical care experiences of the 30th Chinese Antarctic Research Expedition: a retrospective study. Chinese Medical Journal, 128, 398400.CrossRefGoogle ScholarPubMed
Lugg, D. & Shepanek, M. 1999. Space analogue studies in Antarctica. Acta Astronautica, 44, 693699.CrossRefGoogle ScholarPubMed
Lugg, D.J., Ursin, H., Donovan, K., Muller, H.K. & Quinn, D. 1995. Immune responses during an Antarctic summer. Pathology, 27, 186190.CrossRefGoogle Scholar
Mackinnon, L.T. & Hooper, S. 1994. Mucosal (secretory) immune system responses to exercise of varying intensity and during overtraining. International Journal of Sports Medicine, 15, S179S183.CrossRefGoogle ScholarPubMed
Macpherson, A.J., McCoy, K.D., Johansen, F.E. & Brandtzaeg, P. 2008. The immune geography of IgA induction and function. Mucosal Immunology, 1, 1122.CrossRefGoogle ScholarPubMed
Maes, M., Hendriks, D., Van Gastel, A., Demedts, P., Wauters, A., Neels, H. et al. 1997. Effects of psychological stress on serum immunoglobulin, complement and acute phase protein concentrations in normal volunteers. Psychoneuroendocrinology, 22, 397409.CrossRefGoogle ScholarPubMed
Martínez-Carrillo, B.E., Godinez-Victoria, M., Jarillo-Luna, A., Oros-Pantoja, R., Abarca-Rojano, E., Rivera-Aguilar, V. et al. 2011. Repeated restraint stress reduces the number of IgA-producing cells in Peyer's patches. Neuroimmunomodulation, 18, 131141.CrossRefGoogle ScholarPubMed
Mestecky, J. & McGhee, J.R. 1987. Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response. Advances in Immunology, 40, 153245.CrossRefGoogle ScholarPubMed
Mestecky, J., Moro, I., Kerr, M.A. & Woof, J.M. 2005. Mucosal immunoglobulins. In Mestecky, J., ed. Mucosal immunology. Cambridge, MA: Academic Press, 153181.CrossRefGoogle Scholar
Mestecky, J., Lue, C., Tarkowski, A., Ladjeva, I., Peterman, J.H., Moldoveanu, Z. et al. 1989. Comparative studies of the biological properties of human IgA subclasses. In Peeters, H., ed. Protides of the biological fluids. Amsterdam: Elsevier, 173182.Google Scholar
Mishra, K.P., Chauhan, U.K. & Naik, S. 2006. Effect of lead exposure on serum immunoglobulins and reactive nitrogen and oxygen intermediate. Human & Experimental Toxicology, 25, 661665.CrossRefGoogle ScholarPubMed
Mishra, K.P., Yadav, A.P. & Ganju, L. 2012. Antarctic harsh environment as natural stress model: impact on salivary immunoglobulins, transforming growth factor-β and cortisol level. Indian Journal of Clinical Biochemistry, 27, 357362.CrossRefGoogle ScholarPubMed
Mishra, K.P., Yadav, A.P., Chanda, S., Majumdar, D. & Ganju, L. 2011. Serum levels of immunoglobulins (IgG, IgA, IgM) in Antarctic summer expeditioners and their relationship with seasickness. Cellular Immunology, 271, 2935.CrossRefGoogle ScholarPubMed
Mishra, K.P., Yadav, A.P., Shweta, , Chanda, S., Ganju, L., Majumdar, D. & Ilavazhagan, G. 2010. Ship-borne journey induces Th1 cytokines level in Antarctic summer expeditioners. Immunological Investigations, 39, 770779.CrossRefGoogle ScholarPubMed
Mitchell, J.B., Dugas, J.P., McFarlin, B.K. & Nelson, M.J. 2002. Effect of exercise, heat stress, and hydration on immune cell number and function. Medicine and Science in Sports and Exercise, 34, 19411950.CrossRefGoogle ScholarPubMed
Muchmore, H.G., Tatem, B.A., Worley, R.A., Shurley, J.T. & Scott, N. 1973. Immunoglobulins during south polar isolation. In Edholm, O.G. & Gunderson, E.K.E., eds. Polar human biology. Oxford: Butterworth-Heinemann, 135140.CrossRefGoogle Scholar
Nagler, R.M. & Nagler, A. 1999. Major salivary gland involvement in graft-versus-host disease: considerations related to pathogenesis, the role of cytokines and therapy. Cytokines, Cellular & Molecular Therapy, 5, 227232.Google ScholarPubMed
Nieman, D.C., Henson, D.A. & Fagoaga, O.R. 2002. Change in salivary IgA following a competitive marathon race. International Journal of Sports Medicine, 23, 6975.CrossRefGoogle ScholarPubMed
Norman, J.N. 1991. A comparison of the patterns of illness and injury occurring on offshore structures in the northern North Sea and the stations of the British Antarctic Survey. Arctic Medical Research, Suppl., 719721.Google ScholarPubMed
Palinkas, L.A. 1991. Effects of physical and social environments on the health and well-being of Antarctic winter-over personnel. Environment and Behavior, 23, 782799.CrossRefGoogle Scholar
Proctor, G.B. & Carpenter, G.H. 2007. Regulation of salivary gland function by autonomic nerves. Autonomic Neuroscience, 133, 318.CrossRefGoogle ScholarPubMed
Reed, H.L., Reedy, K.R., Palinkas, L.A., Van Do, N., Finney, N.S., Case, H.S. et al. 2001. Impairment in cognitive and exercise performance during prolonged Antarctic residence: effect of thyroxine supplementation in the polar triiodothyronine syndrome. Journal of Clinical Endocrinology and Metabolism, 86, 110116.Google ScholarPubMed
Reyna-Garfias, H., Miliar, A., Jarillo-Luna, A., Rivera-Aguilar, V., Pacheco-Yepez, J., Baeza, I. & Campos-Rodríguez, R. 2010. Repeated restraint stress increases IgA concentration in rat small intestine. Brain, Behavior, and Immunity, 24, 110118.CrossRefGoogle ScholarPubMed
Rhodus, N., Dahmer, L., Lindemann, K., Rudney, J., Mathur, A. & Bereuter, J. 1998. s-IgA and cytokine levels in whole saliva of Sjögren's syndrome patients before and after oral pilocarpine hydrochloride administration: a pilot study. Clinical Oral Investigations, 2, 191196.CrossRefGoogle ScholarPubMed
Roescher, N., Tak, P.P. & Illei, G.G. 2009. Cytokines in Sjögren's syndrome. Oral Diseases, 15, 519526.CrossRefGoogle ScholarPubMed
Sonoda, E.I., Matsumoto, R.Y., Hitoshi, Y.A., Ishii, T., Sugimoto, M., Araki, S. et al. 1989. Transforming growth factor beta induces IgA production and acts additively with interleukin 5 for IgA production. Journal of Experimental Medicine, 170, 14151420.CrossRefGoogle ScholarPubMed
Stone, A.A., Cox, D.S., Valdimarsdottir, H., Jandorf, L. & Neale, J.M. 1987. Evidence that secretory IgA antibody is associated with daily mood. Journal of Personality and Social Psychology, 52, 988.CrossRefGoogle ScholarPubMed
Tashpulatov, R.I. 1974. Microbial flora and human immunity in Antarctica. Antarktika. Doklady Komissi, 13, 183189.Google Scholar
Ursin, H., Bergan, T., Collet, J., Endresen, I.M., Lugg, D.J., Maki, P. et al. 1991. Psychobiological studies of individuals in small, isolated groups in the Antarctic and in space analogues. Environment and Behavior, 23, 766781.CrossRefGoogle Scholar
Wada, M., Orihara, K., Kamagata, M., Hama, K., Sasaki, H., Haraguchi, A. et al. 2017. Circadian clock-dependent increase in salivary IgA secretion modulated by sympathetic receptor activation in mice. Scientific Reports, 7, 8802.CrossRefGoogle ScholarPubMed
Walsh, N.P., Bishop, N.C., Blackwell, J., Wierzbicki, S.G. & Montague, J.C. 2002. Salivary IgA response to prolonged exercise in a cold environment in trained cyclists. Medicine and Science in Sports and Exercise, 34, 16321637.CrossRefGoogle Scholar
Walsh, N.P., Blannin, A.K., Clark, A.M., Cook, L., Robson, P.J. & Gleeson, M. 1999. The effects of high-intensity intermittent exercise on saliva IgA, total protein and alpha-amylase. Journal of Sports Science, 17, 129134.CrossRefGoogle ScholarPubMed
Weber-Mzell, D., Kotanko, P., Hauer, A.C., Goriup, U., Haas, J., Lanner, N. et al. 2004. Gender, age and seasonal effects on IgA deficiency: a study of 7293 Caucasians. European Journal of Clinical Investigation, 34, 224228.CrossRefGoogle ScholarPubMed
Williamson, D.M., White, M.C., Poole, C., Kleinbaum, D., Vogt, R. & North, K. 2006. Evaluation of serum immunoglobulins among individuals living near six superfund sites. Environmental Health Perspectives, 114, 10651071.CrossRefGoogle ScholarPubMed
Wood, J., Lugg, D.J., Hysong, S.J. & Harm, D.L. 1999. Psychological changes in hundred-day remote Antarctic field groups. Environment and Behavior, 31, 299337.CrossRefGoogle ScholarPubMed