Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum

Qi Sun1, Xi Chen1, Jianxiong Yu1, Ke Zen1,2(), Chen-Yu Zhang1(), Liang Li1()

PDF(1417 KB)
PDF(1417 KB)
Protein Cell ›› 2013, Vol. 4 ›› Issue (3) : 197-210. DOI: 10.1007/s13238-013-2119-9
RESEARCH ARTICLE
RESEARCH ARTICLE

Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum

  • Qi Sun1, Xi Chen1, Jianxiong Yu1, Ke Zen1,2(), Chen-Yu Zhang1(), Liang Li1()
Author information +
History +

Abstract

Colostrum provides essential nutrients and immunologically active factors that are beneficial to newborns. Our previous work demonstrated that milk contains large amounts of miRNA that is largely stored in milk-derived microvesicles (MVs). In the present study, we found that the MVs from colostrum contain signifi cantly higher levels of several immune-related miRNAs. We hypothesized that the colostrum MVs may transfer the immune-related miRNAs into cells, which contribute to its immune modulatory feature. We isolated colostrum MVs by ultracentrifugation and demonstrated several immune modulation features associated with miRNAs. We also provide evidence that the physical structure of milk-derived MVs is essential for transfer miRNAs and following immune modulation effect. Moreover, we found that colostrum powder-derived MVs also contains higher levels of immune-related miRNAs that display similar immune modulation effects. Taken together, these results show that MV-containing immunerelated miRNAs may be a novel mechanism by which colostrum modulates body immune response.

Keywords

colostrum / miRNAs / microvesicles / immune modulation

Cite this article

Download citation ▾
Qi Sun, Xi Chen, Jianxiong Yu, Ke Zen, Chen-Yu Zhang, Liang Li. Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum. Prot Cell, 2013, 4(3): 197‒210 https://doi.org/10.1007/s13238-013-2119-9

References

[1] Admyre, C., Johansson, S.M., Qazi, K.R., Filen, J.J., Lahesmaa, R., Norman, M., Neve, E.P., Scheynius, A., and Gabrielsson, S. (2007). Exosomes with immune modulatory features are present in human breast milk. J Immunol 179, 1969-1978 .
[2] Agarwal, S., Karmaus, W., Davis, S., and Gangur, V. (2011). Immune markers in breast milk and fetal and maternal body fluids: a systematic review of perinatal concentrations. J Hum Lact 27, 171-186 .10.1177/0890334410395761
[3] Bandres, E., Bitarte, N., Arias, F., Agorreta, J., Fortes, P., Agirre, X., Zarate, R., Diaz-Gonzalez, J.A., Ramirez, N., Sola, J.J., . (2009). microRNA-451 regulates macrophage migration inhibitory factor production and proliferation of gastrointestinal cancer cells. Clin Cancer Res 15, 2281-2290 . 10.1158/1078-0432.CCR-08-1818
[4] Chen, X., Ba, Y., Ma, L., Cai, X., Yin, Y., Wang, K., Guo, J., Zhang, Y., Chen, J., Guo, X., . (2008). Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18, 997-1006 . 10.1038/cr.2008.282
[5] Chen, X., Gao, C., Li, H., Huang, L., Sun, Q., Dong, Y., Tian, C., Gao, S., Dong, H., Guan, D., . (2010). Identifi cation and characterization of microRNAs in raw milk during different periods of lactation, commercial fl uid, and powdered milk products. Cell Res20, 1128-1137 .10.1038/cr.2010.80
[6] El Gazzar, M., and McCall, C.E. (2012). MicroRNAs regulatory networks in myeloid lineage development and differentiation: regulators of the regulators. Immunol Cell Biol 90, 587-593 .10.1038/icb.2011.74
[7] Fahim, M., Millar, A.A., Wood, C.C., and Larkin, P.J. (2012). Resistance to Wheat streak mosaic virus generated by expression of an artifi- cial polycistronic microRNA in wheat. Plant Biotechnol J 2, 150-163 . 10.1111/j.1467-7652.2011.00647.x
[8] Feng, R., Zhao, C., Li, M., Harrison, T.J., Qiao, Z., Feng, Y., Ma, Z., and Wang, Y. (2011). Infection dynamics of hepatitis E virus in naturally infected pigs in a Chinese farrow-to-fi nish farm. Infect Genet Evol 11, 1727-1731 .10.1016/j.meegid.2011.07.009
[9] Hata , T., Murakami, K., Nakatani, H., Yamamoto, Y., Matsuda, T., and Aoki, N. (2010). Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem Biophys Res Commun 396, 528-533 .10.1016/j.bbrc.2010.04.135
[10] Honorio-Franca, A.C., Carvalho, M.P., Isaac, L., Trabulsi, L.R., and Carneiro-Sampaio, M.M. (1997). Colostral mononuclear phagocytes are able to kill enteropathogenic Escherichia coli opsonized with colostral IgA. Scand J Immunol 46, 59-66 .10.1046/j.1365-3083.1997.d01-86.x
[11] Honorio-Franca, A.C., Launay, P., Carneiro-Sampaio, M.M., and Monteiro, R.C. (2001). Colostral neutrophils express Fc alpha receptors (CD89) lacking gamma chain association and mediate noninfl ammatory properties of secretory IgA. J Leukoc Biol 69, 289-296 .
[12] Huang, S., and He, X. (2010). microRNAs: tiny RNA molecules, huge driving forces to move the cell. Protein Cell 1, 916-926 .10.1007/s13238-010-0116-9
[13] Huan g , Y., Zou, Q., Song, H., Song, F., Wang, L., Zhang, G., and Shen, X. (2010). A study of miRNAs targets prediction and experimental validation. Protein Cell 1, 979-986 .10.1007/s13238-010-0129-4
[14] Kimura, M., Oh, S., Narabayashi, S., and Taguchi, T. (2012). Usefulness of lymphocyte stimulation test for the diagnosis of intestinal cow's milk allergy in infants. Int Arch Allergy Immunol 157, 58-64 .10.1159/000323896
[15] Kosaka, N., Izumi, H., Sekine, K., and Ochiya, T. (2010). microRNA as a new immune-regulatory agent in breast milk. Silence 1, 7.10.1186/1758-907X-1-7
[16] Macchiaverni, P., Arslanian, C., Frazao, J.B., Palmeira, P., Russo, M., Verhasselt, V., and Condino-Neto, A. (2011). Mother to child transfer of IgG and IgA antibodies against Dermatophagoides pteronyssinus. Scand J Immunol 6, 619-627 .10.1111/j.1365-3083.2011.02615.x
[17] Oishi, N., and Wang, X.W. (2011). Novel therapeutic strategies for targeting liver cancer stem cells. Int J Biol Sci 7, 517-535 .10.7150/ijbs.7.517
[18] Patiroglu, T., and Kondolot, M. (2011). The effect of bovine colostrum on viral upper respiratory tract infections in children with immunoglobulin A deficiency. Clin Respir J .10.1111/j.1752- 699X.2011.00268.x.
[19] Pigati, L., Yaddanapudi, S.C., Iyengar, R., Kim, D.J., Hearn, S.A., Danforth, D., Hastings, M.L., and Duelli, D.M. (2010). Selective release of microRNA species from normal and malignant mammary epithelial cells. PLoS One 5, e13515.10.1371/journal.pone.0013515
[20] Qin, L., Chen, Y., Niu, Y., Chen, W., Wang, Q., Xiao, S., Li, A., Xie, Y., Li, J., Zhao, X., . (2010). A deep investigation into the adipogenesis mechanism: profi le of microRNAs regulating adipogenesis by modulating the canonical Wnt/beta-catenin signaling pathway. BMC Genomics 11, 320.10.1186/1471-2164-11-320
[21] Sharma, A., Kumar, M., Aich, J., Hariharan, M., Brahmachari, S.K., Agrawal, A., and Ghosh, B. (2009). Posttranscriptional regulation of interleukin-10 expression by hsa-miR-106a. Proc Natl Acad Sci U S A 106, 5761-5766 .10.1073/pnas.0808743106
[22] Skog, J., Wurdinger, T., van Rijn, S., Meijer, D.H., Gainche, L., Sena-Esteves, M., Curry, W.T., Jr., Carter, B.S., Krichevsky, A.M., and Breakefield, X.O. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10, 1470-1476 .10.1038/ncb1800
[23] Sonkoly, E., Stahle, M., and Pivarcsi, A. (2008). MicroRNAs and immunity: novel players in the regulation of normal immune function and infl ammation. Semin Cancer Biol 18, 131-140 .10.1016/j.semcancer.2008.01.005
[24] Vickers, K.C., Palmisano, B.T., Shoucri, B.M., Shamburek, R.D., and Remaley, A.T. (2011). MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol 13, 423-433 .10.1038/ncb2210
[25] Zhang, L., Hou, D., Chen, X., Li, D., Zhu, L., Zhang, Y., Li, J., Bian, Z., Liang, X., Cai, X., . (2012). Exogenous plant MIR168a specifi- cally targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res 22, 107-126 .10.1038/cr.2011.158
[26] Zhang, Y., Liu, D., Chen, X., Li, J., Li, L., Bian, Z., Sun, F., Lu, J., Yin, Y., Cai, X., . (2010). Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39, 133-144 .10.1016/j.molcel.2010.06.010
[27] Zhou , Q., Li, M., Wang, X., Li, Q., Wang, T., Zhu, Q., Zhou, X., Wang, X., Gao, X., and Li, X. (2012). Immune-related microRNAs are abundant in breast milk exosomes. Int J Biol Sci 8, 118-123 .10.7150/ijbs.8.118
AI Summary AI Mindmap
PDF(1417 KB)

Accesses

Citations

Detail

Sections
Recommended

/