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Mycobacterium vaccae Immunization to Pregnant BALB/c Mice Ameliorated Lung Histopathology and Bone Marrow Eosinophila in Ovalbumin Sensitized Offsprings

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DOI: 10.4236/oji.2014.42005    2,425 Downloads   3,538 Views   Citations

ABSTRACT

Context: One of the treatment strategies for atopic diseases is to skew immune response away from Th2 dominance by using Mycobacterial strains. Objective: We wanted to find out whether M. vaccae administration to pregnant mice had any preventive effect on the offsprings in the development of a murine asthma model. Materials and Methods: Pregnant BALB/c mice were divided into two groups; first group received heat-killed M. vaccae subcutaneously on 12th day of pregnancy and the latter group received PBS. After delivery, newborn mice of each group were further divided into two subgroups as M. vaccae/Ovalbumin (OVA), M. vaccae/control, PBS/OVA and PBS/ control. To establish experimental murine asthma model, mice were intraperitoneally sensitized and challenged intratracheally with Ovalbumin. We analysed airway histopathology, bone marrow eosinophil progenitors and splenic cell cytokine profiles of the offsprings. Results: Comparison of offsprings in M. vaccae/OVA group were not different than PBS controls with respect to thicknesses of airway epithelium, basement membrane, subepithelial smooth muscles and number of hyperplasic goblet cells as well as bronchial associated lymphoid tissue density and eosinophil progenitors in the bone marrow. Comparison of M. vaccae/OVA group to asthma model revealed significant differences and lower levels of OVA-induced IL-5. Conclusions: We propose that immunization of pregnant BALB/c with M. vaccae could prevent histopathological alterations in the airways related to the asthma model and down-regulates IL-5 secretion from splenocytes of offsprings.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Akkoc, T. , Ozdemir, C. , Yazi, D. , Yesil, O. , Bahceciler, N. and Barlan, I. (2014) Mycobacterium vaccae Immunization to Pregnant BALB/c Mice Ameliorated Lung Histopathology and Bone Marrow Eosinophila in Ovalbumin Sensitized Offsprings. Open Journal of Immunology, 4, 31-41. doi: 10.4236/oji.2014.42005.

References

[1] Burrows, B., Martinez, F.D., Halonen, M., Barbee, R.A. and Cline, M.G. (1989) Association of Asthma with Serum IgE Levels and Skin-Test Reactivity to Allergens. The New England Journal of Medicine, 320, 271-277.
http://dx.doi.org/10.1056/NEJM198902023200502
[2] Bousquet, J., Chanez, P., Lacoste, J.Y., Barneon, G., Ghavanian, N., Enander, I., Venge, P., Ahlstedt, S., Simony-Lafontaine, J., Godard, P. and Michel, F.B. (1990) Eosinophilic Inflammation in Asthma. The New England Journal of Medicine, 323, 1033-1039.
http://dx.doi.org/10.1056/NEJM199010113231505
[3] Shirakawa, T., Enomoto, T., Shimazu, S. and Hopkin, J.M. (1997) The Inverse Association between Tuberculin Responses and Atopic Disorder. Science, 275, 77-79.
http://dx.doi.org/10.1126/science.275.5296.77
[4] Obihara, C.C., Kimpen, J.L. and Beyers, N. (2007) The Potential of Mycobacterium to Protect against Allergy and Asthma. Current Allergy and Asthma Reports, 7, 223-230.
http://dx.doi.org/10.1007/s11882-007-0076-1
[5] Cohn, L., Elias, J.A. and Chupp, G.L. (2004) Asthma: Mechanisms of Disease Persistence and Progression. Annual Review of Immunology, 22, 789-815.
http://dx.doi.org/10.1146/annurev.immunol.22.012703.104716
[6] Ober, C. and Thompson, E.E. (2005) Rethinking Genetic Models of Asthma: The Role of Environmental Modifiers. Current Opinion in Immunology, 17, 670-678.
http://dx.doi.org/10.1016/j.coi.2005.09.009
[7] Wills-Karp, M., Santeliz, J. and Karp, C.L. (2001) The Germless Theory of Allergic Disease: Revisiting the Hygiene Hypothesis. Nature Reviews Immunology, 1, 69-75.
http://dx.doi.org/10.1038/35095579
[8] Martinez, F.D., Wright, A.L., Taussig, L.M., Holberg, C.J., Halonen, M., Morgan, W.J. (1995) Asthma and Wheezing in the First Six Years of Life. The Group Health Medical Associates. The New England Journal of Medicine, 332, 133-138.
http://dx.doi.org/10.1056/NEJM199501193320301
[9] Litonjua, A.A., Carey, V.J., Burge, H.A., Weiss, S.T. and Gold, D.R. (1998) Parental History and the Risk for Childhood Asthma: Does Mother Confer More Risk Than Father? American Journal of Respiratory and Critical Care Medicine, 158, 176-181.
http://dx.doi.org/10.1164/ajrccm.158.1.9710014
[10] Kurukulaaratchy, R.J., Matthews, S., Waterhouse, L. and Arshad, S.H. (2003) Factors Influencing Symptom Expression in Children with Bronchial Hyperresponsiveness at 10 Years of Age. Journal of Allergy and Clinical Immunology, 112, 311-316.
http://dx.doi.org/10.1067/mai.2003.1623
[11] Matson, A.P., Zhu, L., Lingenheld, E.G., Schramm, C.M., Clark, R.B., Selander, D.M., Thrall, R.S., Breen, E. and Puddington, L. (2007) Maternal Transmission of Resistance to Development of Allergic Airway Disease. The Journal of Immunology, 179, 1282-1291.
http://dx.doi.org/10.4049/jimmunol.179.2.1282
[12] Ho, Y.S., Adroub, S.A., Abadi, M., Alwan, B.A., Alkhateeb, R., Gao, G., Ragab, A., Shahjahan, A., van Soolingen, D., Bitter, W., Pain, A. and Abdallah, A.M. (2012) Complete Genome Sequence of Mycobacterium vaccae Type Strain ATCC 25954. Journal of Bacteriology, 194, 6339-6340.
http://dx.doi.org/10.1128/JB.01462-12
[13] Wang, C.C. and Rook, G.A. (1998) Inhibition of an Established Allergic Response to Ovalbumin in Balb/c Mice by Killed Mycobacterium vaccae. Immunology, 93, 307-313.
http://dx.doi.org/10.1046/j.1365-2567.1998.00432.x
[14] Hopfenspirger, M.T., Parr, S.K., Hopp, R.J., Townley, R.G. and Agrawal, D.K. (2001) Mycobacterial Antigens Attenuate Late Phase Response, Airway Hyperresponsiveness, and Bronchoalveolar Lavage Eosinophilia in a Mouse Model of Bronchial Asthma. International Immunopharmacology, 1, 1743-1751.
http://dx.doi.org/10.1016/S1567-5769(01)00084-4
[15] Zuany-Amorim, C., Manlius, C., Trifilieff, A., Brunet, L.R., Rook, G., Bowen, G., Pay, G. and Walker, C. (2002) Long-Term Protective and Antigen Specific Effect of Heat-Killed Mycobacterium vaccae in a Murine Model of Allergic Pulmonary Inflammation. The Journal of Immunology, 169, 1492-1499.
http://dx.doi.org/10.4049/jimmunol.169.3.1492
[16] Ozdemir, C., Akkoc, T., Bahceciler, N.N., Kucukercan, D., Barlan, I.B. and Basaran, M.M. (2003) Impact of Mycobacterium vaccae Immunization on Lung Histopathology in a Murine Model of Chronic Asthma. Clinical & Experimental Allergy, 33, 266-270.
http://dx.doi.org/10.1046/j.1365-2222.2003.01595.x
[17] Walker, C., Sawicka, E. and Rook, G.A. (2003) Immunotherapy with Mycobacteria. Current Opinion in Allergy & Clinical Immunology, 3, 481-486.
[18] Dunstan, J.A., Brothers, S., Bauer, J., Hodder, M., Jaksic, M.M., Asher, M.I. and Prescott, S.L. (2011) The Effects of Mycobacteria vaccae Derivative on Allergen-Specific Responses in Children with Atopic Dermatitis. Clinical & Experimental Immunology, 164, 321-329. http://dx.doi.org/10.1111/j.1365-2249.2011.04371.x
[19] Akkoc, T., Tolunay, S., Barlan, I. and Basaran, M. (2001) Airway Remodeling and Serum Total Immunoglobulin E (IgE) Levels in a Murine Model of Asthma. Journal of Asthma, 38, 585-591. http://dx.doi.org/10.1081/JAS-100107123
[20] Wegmann, T.G., Lin, H., Guilbert, L. and Mosmann, T.R. (1993) Bidirectional Cytokine Interactions in the Maternal-Fetal Relationship: Is Successful Pregnancy a TH2 Phenomenon? Immunology Today, 14, 353-356.
http://dx.doi.org/10.1016/0167-5699(93)90235-D
[21] Ostensen, M., Forger, F. and Villiger, P.M. (2006) Cytokines and Pregnancy in Rheumatic Disease. Annals of the New York Academy of Sciences, 1069, 353-363.
http://dx.doi.org/10.1196/annals.1351.033
[22] Hebisch, G., Neumaier-Wagner, P.M., Huch, R. and von Mandach, U. (2004) Maternal Serum Interleukin-1 Beta, -6 and -8 Levels and Potential Determinants in Pregnancy and Peripartum. Journal of Perinatal Medicine, 32, 475-480.
http://dx.doi.org/10.1515/JPM.2004.131
[23] Opsjon, S., Austgulen, R. and Waage, A. (1995) Interleukin-1, Interleukin-6 and Tumor Necrosis Factor at Delivery in Preeclamptic Disorders. Acta Obstetricia et Gynecologica Scandinavica, 74, 19-26.
http://dx.doi.org/10.3109/00016349509009937
[24] Makhseed, M., Raghupathy, R., Azizieh, F., Farhat, R., Hassan, N. and Bandar, A. (2000) Circulating Cytokines and CD30 in Normal Human Pregnancy and Recurrent Spontaneous Abortions. Human Reproduction, 15, 2011-2017.
http://dx.doi.org/10.1093/humrep/15.9.2011
[25] Ellis, J., Wennerholm, U.B., Bengtsson, A., Lilja, H., Pettersson, A., Sultan, B., Wennergren, M. and Hagberg, H. (2001) Levels of Dimethylarginines and Cytokines in Mild and Severe Preeclampsia. Acta Obstetricia et Gynecologica Scandinavica, 80, 602-608.
[26] Russwurm, G.P., Mackler, A.M., Fagoaga, O.R., Brown, W.S., Sakala, E.P., Yellon, S.M. and Nehlsen-Cannarella, S.L. (1997) Soluble Human Leukocyte Antigens, Interleukin-6, and Interferon-Gamma during Pregnancy. American Journal of Reproductive Immunology, 38, 256-262.
http://dx.doi.org/10.1111/j.1600-0897.1997.tb00512.x
[27] Tangri, S., Wegmann, T.G., Lin, H. and Raghupathy R. (1994) Maternal Anti-Placental Reactivity in Natural, Immunologically-Mediated Fetal Resorptions. The Journal of Immunology, 152, 4903-4911.
[28] Raghupathy, R. (2001) Pregnancy: Success and Failure within the TH1/TH2/Th3 Paradigm. Seminars in Immunology, 13, 219-227.
http://dx.doi.org/10.1111/j.1600-0897.1997.tb00512.x
[29] Raghupathy, R., Makhseed, M., Azizieh, F., Omu, A., Gupta, M. and Farhat, R. (2000) Cytokine Production by Maternal Lymphocytes during Normal Human Pregnancy and in Unexplained Recurrent Spontaneous Abortion. Human Reproduction, 15, 713-738.
http://dx.doi.org/10.1093/humrep/15.3.713
[30] Saito, S., Sakai, M., Sasaki, Y., Tanebe, K., Tsuda, H. and Michimata, T. (1999) Quantitative Analysis of Peripheral Blood Th0, TH1, TH2 and the TH1:TH2 Cell Ratio during Normal Human Pregnancy and Preeclampsia. Clinical and Experimental Immunology, 117, 550-555. http://dx.doi.org/10.1046/j.1365-2249.1999.00997.x
[31] Akdis, M., Verhagen, J., Taylor, A., Karamloo, F., Karagiannidis, C., Crameri, R., Thunberg, S., Deniz, G., Valenta, R., Fiebig, H., Kegel, C., Disch, R., Schmidt-Weber, C.B., Blaser, K. and Akdis, C.A. (2004) Immune Responses in Healthy and Allergic Individuals Are Characterized by a Fine Balance between Allergen-Specific T Regulatory 1 and T Helper 2 Cells. The Journal of Experimental Medicine, 199, 1567-1575.
http://dx.doi.org/10.1084/jem.20032058
[32] Kearley, J., Barker, J.E., Robinson, D.S. and Lloyd, C.M. (2005) Resolution of Airway Inflammation and Hyperreactivity after in Vivo Transfer of CD4+CD25+ Regulatory T Cells Is Interleukin 10 Dependent. The Journal of Experimental Medicine, 202, 1539-1547. http://dx.doi.org/10.1084/jem.20051166
[33] Schaub, B., Liu, J., Hoppler, S., Haug, S., Sattler, C., Lluis, A., Illi, S. and von Mutius, E. (2008) Impairment of T-Regulatory Cells in Cord Blood of Atopic Mothers. The Journal of Allergy and Clinical Immunology, 121, 1491-1499.
http://dx.doi.org/10.1016/j.jaci.2008.04.010
[34] Adams, V.C., Hunt, J.R., Martinelli, R., Palmer, R., Rook, G.A. and Brunet, L.R. (2004) Mycobacterium vaccae Induces a Population of Pulmonary CD11c+ Cells with Regulatory Potential in Allergic Mice. European Journal of Immunology, 34, 631-638.
http://dx.doi.org/10.1002/eji.200324659
[35] Hunt, J.R., Martinelli, R., Adams, V.C., Rook, G.A. and Brunet, L.R. (2005) Intragastric Administration of Mycobacterium vaccae Inhibits Severe Pulmonary Allergic Inflammation in a Mouse Model. Clinical & Experimental Allergy, 35, 685-690.
[36] Ricklin Gutzwiller, M.E., Reist, M., Peel, J.E., Seewald, W., Brunet, L.R. and Roosje, P.J. (2007) Intradermal Injection of Heat-Killed Mycobacterium vaccae in Dogs with Atopic Dermatitis: A Multicentre Pilot Study. Veterinary Dermatology, 18, 87-93.
http://dx.doi.org/10.1111/j.1365-3164.2007.00579.x
[37] Arkwright, P.D. and David, T.J. (2001) Intradermal Administration of a Killed Mycobacterium vaccae Suspension (SRL 172) Is Associated with Improvement in Atopic Dermatitis in Children with Moderate-to-Severe Disease. The Journal of Allergy and Clinical Immunology, 107, 531-534.
http://Dx.doi.org/10.1067/mai.2001.113081
[38] Nahori, M.A., Lagranderie, M., Lefort, J., Thouron, F., Joseph, D., Winter, N., Gicquel, B., Silva, J.R.L.E. and Vargaftig, B.B. (2001) Effects of Mycobacterium bovis BCG on the Development of Allergic Inflammation and Bronchial Hyperresponsiveness in Hyper-IgE BP2 Mice Vaccinated as Newborns. Vaccine, 19, 1484-1495.
http://dx.doi.org/10.1016/S0264-410X(00)00345-5
[39] Hopfenspirger, M.T., Parr, S.K., Hopp, J.R., Townley, R.G. and Agrawal, D.K. (2001) Mycobacterial Antigens Attenuate Late Phase Response, Airway Hyperresponsiveness, and Bronchoalveolar Lavage Eosinophilia in a Mouse Model of Bronchial Asthma. International Immunopharmacology, 1, 1743-1751.
http://dx.doi.org/10.1016/S1567-5769(01)00084-4
[40] Zuany-Amorim, C., Sawicka, E., Manlius, C., Le Moine, A., Brunet, L.R., Kemeny, D.M., Bowen, G., Rook, G. and Walker, C. (2002) Suppression of Airway Eosinophilia by Killed Mycobacterium vaccae-Induced Allergen-Specific Regulatory T-Cells. Nature Medicine, 8, 625-629.
http://dx.doi.org/10.1038/nm0602-625
[41] Erb, K.J., Holloway, J.W., Sobeck, A., Moll, H. and Le Gros, G. (1998) Infection of Mice with Mycobacterium bovis-Bacillus Calmette-Guérin (BCG) Suppresses Allergen-Induced Airway Eosinophilia. The Journal of Experimental Medicine, 187, 561-569.
http://dx.doi.org/10.1084/jem.187.4.561
[42] Ozdemir, C., Yazi, D., Aydogan, M., Akkoc, T., Bahceciler, N.N., Strong, P. and Barlan, I.B. (2006) Treatment with Chitin Microparticles Is Protective against Lung Histopathology in a Murine Asthma Model. Clinical & Experimental Allergy, 36, 960-968.
http://dx.doi.org/10.1111/j.1365-2222.2006.02515.x
[43] Yazi, D., Akkoc, T., Ozdemir, C., Yesil, O., Aydogan, M., Sancak, R., Bahceciler, N.N. and Barlan, I.B. (2007) Long-Term Modulatory Effect of Mycobacterium vaccae Treatment on Histopathologic Changes in a Murine Model of Asthma. Annals of Allergy, Asthma & Immunology, 98, 573-579.
http://dx.doi.org/10.1016/S1081-1206(10)60738-7
[44] Akkoc, T., Eifan, A., Ozdemir, C., Yazi, D., Yesil, O., Bahceciler, N.N. and Barlan, I.B. (2008) Mycobacterium vaccae Immunization to OVA Sensitized Pregnant BALB/c Mice Suppresses Placental and Postnatal IL-5 and Inducing IFN-Gamma Secretion Immunopharmacol. Immunopharmacology and Immunotoxicology, 30, 1-11.
http://dx.doi.org/10.1080/08923970701812159

  
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