Porcine milk-derived exosomes promote proliferation of intestinal epithelial cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Chen, Ting ^a   Xie, Mei Ying ^a   Sun, Jia Jie ^a   Ye, Rui Song ^a   Cheng, Xiao ^a   Sun, Rui Ping ^a   Wei, Li Min ^a   Li, Meng ^a   Lin, De Lin ^a   Jiang, Qing Yan ^a   Xi, Qian Yun ^a   Zhang, Yong Liang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CELL LINE; CELL PROLIFERATION; CHEMISTRY; CYTOLOGY; EPITHELIUM CELL; EXOSOME; GENE EXPRESSION REGULATION; INTESTINE MUCOSA; METABOLISM; MILK; PIG;

ANIMALS; CELL LINE; CELL PROLIFERATION; EPITHELIAL CELLS; EXOSOMES; GENE EXPRESSION REGULATION; INTESTINAL MUCOSA; MILK; SWINE;

EID: 84988473826     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep33862     Document Type: Article

References (66)

1. Xu, R.-J. Development of the newborn GI tract and its relation to colostrum/milk intake: a review. Reproduction, Fertility and Development 8, 35-48 (1996).
2. Pha, J. Development of intestinal transport function in mammals. Physiological reviews 80, 1633-1667 (2000).
3. Guilloteau, P., Zabielski, R., Hammon, H. M., Metges, C. C. Nutritional programming of gastrointestinal tract development. Is the pig a good model for man Nutrition Research Reviews 23, 4-22 (2010).
4. Sheard, N. F., Walker, W. A. The role of breast milk in the development of the gastrointestinal tract. Nutrition Reviews 46, 1-8 (1988).
5. Alpers, D. H. Enteral feeding and gut atrophy. Current Opinion in Clinical Nutrition & Metabolic Care 5, 679-683 (2002).
6. Lebenthal, E., Lee, P., Heitlinger, L. A. Impact of development of the gastrointestinal tract on infant feeding. The Journal of pediatrics 102, 1-9 (1983).
7. Melnik, B. C. Milk-A Nutrient System of Mammalian Evolution Promoting mTORC1-Dependent Translation. International journal of molecular sciences 16, 17048-17087 (2015).
8. Blum, J. W., Baumrucker, C. R. In Bioactive components of milk 397-422 (Springer, 2008).
9. Reinhardt, T. A., Lippolis, J. D., Nonnecke, B. J., Sacco, R. E. Bovine milk exosome proteome. Journal of Proteomics 75, 1486-1492 (2012).
10. Admyre, C. et al. Exosomes with immune modulatory features are present in human breast milk. The Journal of immunology 179, 1969-1978 (2007).
11. Hata, T. et al. Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochemical and biophysical research communications 396, 528-533 (2010).
12. Lser, C. et al. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. Journal of translational medicine 9, 9 (2011).
13. Munagala, R., Aqil, F., Jeyabalan, J., Gupta, R. C. Bovine milk-derived exosomes for drug delivery. Cancer letters 371, 48-61 (2016).
14. Zhou, Q. et al. Immune-related microRNAs are abundant in breast milk exosomes. International journal of biological sciences 8, 118 (2012).
15. Kosaka, N., Izumi, H., Sekine, K., Ochiya, T. microRNA as a new immune-regulatory agent in breast milk. Silence 1, 7 (2010).
16. Lonnerdal, B., Du, X., Liao, Y., Li, J. Human milk exosomes resist digestion in vitro and are internalized by human intestinal cells. The FASEB Journal 29, 121.123 (2015).
17. Alsaweed, M., Hartmann, P. E., Geddes, D. T., Kakulas, F. MicroRNAs in breastmilk and the lactating breast: potential immunoprotectors and developmental regulators for the infant and the mother. International journal of environmental research and public health 12, 13981-14020 (2015).
18. Arntz, O. J. et al. Oral administration of bovine milk derived extracellular vesicles attenuates arthritis in two mouse models. Molecular nutrition & food research 59, 1701-1712 (2015).
19. Chen, T. et al. Exploration of microRNAs in porcine milk exosomes. BMC genomics 15, 100 (2014).
20. Conboy, I. M., Rando, T. A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Developmental cell 3, 397-409 (2002).
21. Ramdass, B. et al. Coexpression of Notch1 and NF-B signaling pathway components in human cervical cancer progression. Gynecologic oncology 104, 352-361 (2007).
22. Hynes, N. E., Stoelzle, T. Key signalling nodes in mammary gland development and cancer: Myc. Breast Cancer Research 11, 1 (2009).
23. Diesing, A.-K. et al. Mycotoxin deoxynivalenol (DON) mediates biphasic cellular response in intestinal porcine epithelial cell lines IPEC-1 and IPEC-J2. Toxicology letters 200, 8-18 (2011).
24. Reznikov, E. A., Comstock, S. S., Yi, C., Contractor, N., Donovan, S. M. Dietary bovine lactoferrin increases intestinal cell proliferation in neonatal piglets. The Journal of nutrition 144, 1401-1408 (2014).
25. Babyatsky, M., Podolsky, D. Growth and development of the gastrointestinal tract. Textbook of gastroenterology, 547-584 (1999).
26. Rubin, D. C., Shaker, A. Small intestine: anatomy and structural anomalies. Yamada's Textbook of Gastroenterology, 73-92 (2009).
27. Werling, R. W., Yaziji, H., Bacchi, C. E., Gown, A. M. CDX2, a highly sensitive and specific marker of adenocarcinomas of intestinal origin: an immunohistochemical survey of 476 primary and metastatic carcinomas. The American journal of surgical pathology 27, 303-310 (2003).
28. Silberg, D. G., Swain, G. P., Suh, E. R., Traber, P. G. Cdx1 and cdx2 expression during intestinal development. Gastroenterology 119, 961-971 (2000).
29. James, R., Erler, T., Kazenwadel, J. Structure of the murine homeobox gene cdx-2. Expression in embryonic and adult intestinal epithelium. Journal of Biological Chemistry 269, 15229-15237 (1994).
30. Waga, S., Hannon, G. J., Beach, D., Stillman, B. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369, 574-578 (1994).
31. Hall, P. et al. Proliferating cell nuclear antigen (PCNA) immunolocalization in paraffin sections: An index of cell proliferation with evidence of deregulated expression in some, neoplasms. The Journal of pathology 162, 285-294 (1990).
32. Vanamala, J., Reddivari, L., Radhakrishnan, S., Tarver, C. Resveratrol suppresses IGF-1 induced human colon cancer cell proliferation and elevates apoptosis via suppression of IGF-1R/Wnt and activation of p53 signaling pathways. BMC cancer 10, 238 (2010).
33. Levine, A. J., Momand, J., Finlay, C. A. The p53 tumour suppressor gene. Nature 351, 453-456 (1991).
34. Kubbutat, M. H., Jones, S. N., Vousden, K. H. Regulation of p53 stability by Mdm2. Nature 387, 299-303 (1997).
35. Haupt, Y., Maya, R., Kazaz, A., Oren, M. Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299 (1997).
36. Artavanis-Tsakonas, S., Rand, M. D., Lake, R. J. Notch signaling: cell fate control and signal integration in development. Science 284, 770-776 (1999).
37. Jia, C. Y. et al. MiR-223 suppresses cell proliferation by targeting IGF-1R. PLoS ONE 6, e27008 (2011).
38. Creighton, C. J. et al. Molecular profiling uncovers a p53-associated role for microRNA-31 in inhibiting the proliferation of serous ovarian carcinomas and other cancers. Cancer research 70, 1906-1915 (2010).
39. He, L. et al. A microRNA component of the p53 tumour suppressor network. Nature 447, 1130-1134 (2007).
40. Afanasyeva, E. A. et al. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death & Differentiation 18, 974-984 (2011).
41. Alexander, M., O'Connell, R. Exosomal miRNAs regulate inflammatory responses (IRM11P. 624). The Journal of Immunology 194, 132.133-132.133 (2015).
42. Baumgart, S., Heinzelmann, J., Stoeckle, M., Ostenfeld, M. S., Junker, K. Characterization of miRNA expression pattern from in-vitro obtained exosomes of different urinary bladder cancer cell lines. Cancer Research 75, 5182-5182 (2015).
43. Ding, G. et al. Pancreatic cancer-derived exosomes transfer miRNAs to dendritic cells and inhibit RFXAP expression via miR-212-3p. Oncotarget 6, 29877 (2015).
44. Baier, S. R., Nguyen, C., Xie, F., Wood, J. R., Zempleni, J. MicroRNAs are absorbed in biologically meaningful amounts from nutritionally relevant doses of cow milk and affect gene expression in peripheral blood mononuclear cells, HEK-293 kidney cell cultures, and mouse livers. The Journal of nutrition 144, 1495-1500 (2014).
45. Izumi, H. et al. Bovine milk exosomes contain microRNA and mRNA and are taken up by human macrophages. Journal of dairy science 98, 2920-2933 (2015).
46. Pieters, B. C. et al. Commercial cow milk contains physically stable extracellular vesicles expressing immunoregulatory TGF-. PLoS one 10, e0121123 (2015).
47. Wolf, T., Baier, S. R., Zempleni, J. The Intestinal Transport of Bovine Milk Exosomes Is Mediated by Endocytosis in Human Colon Carcinoma Caco-2 Cells and Rat Small Intestinal IEC-6 Cells. The Journal of nutrition, jn218586 (2015).
48. Kusuma, R., Friemel, T., Zempleni, J. Human Endothelial Cell Transport Bovine Extracellular Vesicles. The FASEB Journal 29, LB357 (2015).
49. Howard, K. M. et al. Loss of miRNAs during processing and storage of cow's (Bos taurus) milk. Journal of agricultural and food chemistry 63, 588-592 (2015).
50. Alsaweed, M., Lai, C. T., Hartmann, P. E., Geddes, D. T., Kakulas, F. Human milk miRNAs primarily originate from the mammary gland resulting in unique miRNA profiles of fractionated milk. Scientific reports 6 (2016).
51. Izumi, H. et al. Bovine milk contains microRNA and messenger RNA that are stable under degradative conditions. Journal of dairy science 95, 4831-4841 (2012).
52. Arce, C., Ramirez-Boo, M., Lucena, C., Garrido, J. Innate immune activation of swine intestinal epithelial cell lines (IPEC-J2 and IPI-2I) in response to LPS from Salmonella typhimurium. Comparative immunology, microbiology and infectious diseases 33, 161-174 (2010).
53. Ciapetti, G., Cenni, E., Pratelli, L., Pizzoferrato, A. In vitro evaluation of cell/biomaterial interaction by MTT assay. Biomaterials 14, 359-364 (1993).
54. Cheung, W. M., Hui, W. S., Chu, P. W., Chiu, S. W., Ip, N. Y. Ganoderma extract activates MAP kinases and induces the neuronal differentiation of rat pheochromocytoma PC12 cells. FEBS letters 486, 291-296 (2000).
55. Yu, X. et al. MicroRNA-10b promotes nucleus pulposus cell proliferation through RhoC-Akt pathway by targeting HOXD10 in intervetebral disc degeneration. PLoS ONE 8, e83080 (2013).
56. Sisdelli, L. et al. Incorporation of 5-ethynyl-2-deoxyuridine (EdU) as a novel strategy for identification of the skewed X inactivation pattern in balanced and unbalanced X-rearrangements. Human genetics 135, 185-192 (2016).
57. Flomerfelt, F. A., Gress, R. E. Analysis of cell proliferation and homeostasis using EdU labeling. T-Cell Development: Methods and Protocols 211-220 (2016).
58. He, Q., Man, L., Ji, Y., Ding, F. Comparison in the biological characteristics between primary cultured sensory and motor Schwann cells. Neuroscience letters 521, 57-61 (2012).
59. Sun, Y. et al. Multicolor flow cytometry analysis of the proliferations of Tlymphocyte subsets in vitro by EdU incorporation. Cytometry Part A 81, 901-909 (2012).
60. Feng, S. et al. MicroRNA-192 targeting retinoblastoma 1 inhibits cell proliferation and induces cell apoptosis in lung cancer cells. Nucleic acids research, gkr232 (2011).
61. Ye, R.-S. et al. Differentially expressed miRNAs after GnRH treatment and their potential roles in FSH regulation in porcine anterior pituitary cell. PLoS ONE 8, e57156 (2013).
62. Stoscheck, C. M. [6] Quantitation of protein. Methods in enzymology 182, 50-68 (1990).
63. Thy, C. et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. The Journal of Immunology 166, 7309-7318 (2001).
64. Liu, W. N., Leung, K. N. The Immunomodulatory Activity of Jacaric Acid, a Conjugated Linolenic Acid Isomer, on Murine Peritoneal Macrophages. PLoS one 10 (2015).
65. Hochstim, C. J., Choi, J. Y., Lowe, D., Masood, R., Rice, D. H. Biofilm detection with hematoxylin-eosin staining. Archives of Otolaryngology-Head & Neck Surgery 136, 453-456 (2010).
66. Cheng, X. et al. Critical role of miR-125b in lipogenesis by targeting stearoyl-CoA desaturase-1 (SCD-1). Journal of Animal Science 94, 65-76 (2016).