Differential temporal expression of milk miRNA during the lactation cycle of the marsupial tammar wallaby (Macropus eugenii)

BMC Genomics

Christophe Lefevre²  Kevin R Nicholas²  Julie A Sharp²  Lyn A Hinds¹  Amit Kumar²  Vengamanaidu Modepalli² 

[1] CSIRO Ecosystem Sciences, GPO Box 1700, Canberra, Act 2601, Australia;School of medicine, Deakin University, Pigdons Road, Geelong, Vic, Australia

关键词: Exosome;    Mammary gland;    Development;    Milk;    Micro RNA;    Marsupials;    Lactation;   

Others  :  1091429
DOI  :  10.1186/1471-2164-15-1012

 received in 2014-08-06, accepted in 2014-10-30,  发布年份 2014

【 摘 要 】

Background

Lactation is a key aspect of mammalian evolution for adaptation of various reproductive strategies along different mammalian lineages. Marsupials, such as tammar wallaby, adopted a short gestation and a relatively long lactation cycle, the newborn is immature at birth and significant development occurs postnatally during lactation. Continuous changes of tammar milk composition may contribute to development and immune protection of pouch young. Here, in order to address the putative contribution of newly identified secretory milk miRNA in these processes, high throughput sequencing of miRNAs collected from tammar milk at different time points of lactation was conducted. A comparative analysis was performed to find distribution of miRNA in milk and blood serum of lactating wallaby.

Results

Results showed that high levels of miRNA secreted in milk and allowed the identification of differentially expressed milk miRNAs during the lactation cycle as putative markers of mammary gland activity and functional candidate signals to assist growth and timed development of the young. Comparative analysis of miRNA distribution in milk and blood serum suggests that milk miRNAs are primarily expressed from mammary gland rather than transferred from maternal circulating blood, likely through a new putative exosomal secretory pathway. In contrast, highly expressed milk miRNAs could be detected at significantly higher levels in neonate blood serum in comparison to adult blood, suggesting milk miRNAs may be absorbed through the gut of the young.

Conclusion

The function of miRNA in mammary gland development and secretory activity has been proposed, but results from the current study also support a differential role of milk miRNA in regulation of development in the pouch young, revealing a new potential molecular communication between mother and young during mammalian lactation.

【 授权许可】

   
2014 Modepalli et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Hwang HW, Mendell JT: MicroRNAs in cell proliferation, cell death, and tumorigenesis. Brit J Cancer 2006, 94(6):776-780.
• [2]Song L, Tuan RS: MicroRNAs and cell differentiation in mammalian development. Birth Defects Res C Embryo Today 2006, 78(2):140-149.
• [3]Zhou Q, Li MZ, Wang XY, Li QZ, Wang T, Zhu Q, Zhou XC, Wang X, Gao XL, Li XW: Immune-related MicroRNAs are abundant in breast milk exosomes. Int J Biol Sci 2012, 8(1):118-123.
• [4]Michael A, Bajracharya SD, Yuen PST, Zhou H, Star RA, Illei GG, Alevizos I: Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis 2010, 16(1):34-38.
• [5]Caby MP, Lankar D, Vincendeau-Scherrer C, Raposo G, Bonnerot C: Exosomal-like vesicles are present in human blood plasma. Int Immunol 2005, 17(7):879-887.
• [6]Pisitkun T, Shen RF, Knepper MA: Identification and proteomic profiling of exosomes in human urine. Proc Natl Acad Sci U S A 2004, 101(36):13368-13373.
• [7]Kosaka N, Yoshioka Y, Hagiwara K, Tominaga N, Ochiya T: Functional analysis of exosomal microRNA in cell-cell communication research. Methods Mol Biol 2013, 1024:1-10.
• [8]Camussi G, Deregibus MC, Bruno S, Cantaluppi V, Biancone L: Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 2010, 78(9):838-848.
• [9]Ge Q, Zhou Y, Lu J, Bai Y, Xie X, Lu Z: MiRNA in plasma exosome is stable under different storage conditions. Molecules 2014, 19(2):1568-1575.
• [10]Munch EM, Harris RA, Mohammad M, Benham AL, Pejerrey SM, Showalter L, Hu M, Shope CD, Maningat PD, Gunaratne PH, Haymond M, Aagaard K: Transcriptome profiling of microRNA by next-Gen deep sequencing reveals known and novel miRNA species in the lipid fraction of human breast milk. PLoS ONE 2013, 8(2):e50564.
• [11]Donovan SM, Odle J: Growth-factors in milk as mediators of infant development. Annu Rev Nutr 1994, 14:147-167.
• [12]Nicholas KR: Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus-Eugenii). Biochem Biophys Res Commun 1988, 154(2):529-536.
• [13]Kosaka N, Izumi H, Sekine K, Ochiya T: microRNA as a new immune-regulatory agent in breast milk. Silence 2010, 1(1):7. BioMed Central Full Text
• [14]Hata T, Murakami K, Nakatani H, Yamamoto Y, Matsuda T, Aoki N: Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem Biophys Res Commun 2010, 396(2):528-533.
• [15]Chen T, Xi Q-Y, Ye R-S, Cheng X, Qi Q-E, Wang S-B, Shu G, Wang L-N, Zhu X-T, Jiang Q-Y, Zhang Y-L: Exploration of microRNAs in porcine milk exosomes. Bmc Genomics 2014, 15(1):100. BioMed Central Full Text
• [16]Ji ZB, Wang GZ, Xie ZJ, Zhang CL, Wang JM: Identification and characterization of microRNA in the dairy goat (Capra hircus) mammary gland by Solexa deep-sequencing technology. Mol Biol Rep 2012, 39(10):9361-9371.
• [17]Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RH: MicroRNA expression in zebrafish embryonic development. Science 2005, 309(5732):310-311.
• [18]Laurent LC: MicroRNAs in embryonic stem cells and early embryonic development. J Cell Mol Med 2008, 12(6A):2181-2188.
• [19]Trott JF, Simpson KJ, Moyle RL, Hearn CM, Shaw G, Nicholas KR, Renfree MB: Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 2003, 68(3):929-936.
• [20]Tyndale-Biscoe CH, Janssens PA: The Developing Marsupial: Models for Biomedical Research. Berlin: Springer; 1988.
• [21]Jenness R: Lactational performance of various mammalian-species. J Dairy Sci 1986, 69(3):869-885.
• [22]Renfree MB: Life in the pouch: womb with a view. Reprod Fert Develop 2006, 18(7):721-734.
• [23]Brennan AJ, Sharp JA, Digby MR, Nicholas KR: The tammar wallaby: a model to examine endocrine and local control of lactation. IUBMB Life 2007, 59(3):146-150.
• [24]Deane EM, Cooper DW: Immunology of pouch young marsupials. I. Levels of immunoglobulin transferrin and albumin in the blood and milk of euros and wallaroos (hill kangaroos:, marsupialia). Dev Comp Immunol 1984, 8(4):863-876.
• [25]Tizard I: The protective properties of milk and colostrum in non-human species. Adv Nutr Res 2001, 10:139-166.
• [26]Merchant JC, Sharman GB: Observations on the attatchment of marsupial pouch young to the teats and on the rearing of pouch young by foster-mothers of the same or different species. Aust J Zool 1966, 14(4):593-609.
• [27]Green B, Krause WJ, Newgrain K: Milk composition in the North American opossum (Didelphis virginiana). Comp Biochem Physiol B Biochem Mol Biol 1996, 113(3):619-623.
• [28]Bird PH, Hendry KA, Shaw DC, Wilde CJ, Nicholas KR: Progressive changes in milk protein gene expression and prolactin binding during lactation in the tammar wallaby (Macropus eugenii). J Mol Endocrinol 1994, 13(2):117-125.
• [29]Kevin RN: Asynchronous dual lactation in a marsupial, the tammar wallaby (Macropus eugenii). Biochem Bioph Res Co 1988, 154(2):529-536.
• [30]Ward KL, Renfree MB: Effects of progesterone on parturition in the tammar. Macropus eugenii J Reprod Fertil 1984, 72(1):21-28.
• [31]Messer M, Nicholas KR: Biosynthesis of marsupial milk oligosaccharides - characterization and developmental-changes of 2 galactosyltransferases in lactating mammary-glands of the tammar wallaby. Macropus-Eugenii Biochim Biophys Acta 1991, 1077(1):79-85.
• [32]Nicholas K, Simpson K, Wilson M, Trott J, Shaw D: The Tammar Wallaby: A Model to Study Putative Autocrine-Induced Changes in Milk Composition. J Mammary Gland Biol Neoplasia 1997, 2(3):299-310.
• [33]Green B, Griffiths M, Leckie RM: Qualitative and quantitative changes in milk fat during lactation in the tammar wallaby (Macropus eugenii). Aust J Biol Sci 1983, 36(5–6):455-461.
• [34]Nicholas K, Sharp J, Watt A, Wanyonyi S, Crowley T, Gillespie M, Lefevre C: The tammar wallaby: a model system to examine domain-specific delivery of milk protein bioactives. Semin Cell Dev Biol 2012, 23(5):547-556.
• [35]Sharp JA, Lefèvre C, Nicholas KR: Molecular evolution of monotreme and marsupial whey acidic protein genes. Evol Dev 2007, 9(4):378-392.
• [36]Gu Y, Li M, Wang T, Liang Y, Zhong Z, Wang X, Zhou Q, Chen L, Lang Q, He Z, Chen XH, Gong JJ, Gao XL, Li XW, Lv XB: Lactation-related microRNA expression profiles of porcine breast milk exosomes. Plos One 2012, 7(8):e43691.
• [37]Greenhill C: Nutrition: drinking cow’s milk alters vitamin D and iron stores in young children. Nat Rev Endocrinol 2013, 9(3):126.
• [38]Messer M, Kerry KR: Milk carbohydrates of the echidna and the platypus. Science 1973, 180(4082):201-203.
• [39]Ballard O, Morrow AL: Human milk composition nutrients and bioactive factors. Pediatr Clin N Am 2013, 60(1):49-+.
• [40]Wada Y, Lönnerdal B: Bioactive peptides derived from human milk proteins — mechanisms of action. J Nutr Biochem 2014, 25(5):503-514.
• [41]Kwek JH, Iongh RD, Digby MR, Renfree MB, Nicholas KR, Familari M: Cross-fostering of the tammar wallaby (Macropus eugenii) pouch young accelerates fore-stomach maturation. Mech Dev 2009, 126(5–6):449-463.
• [42]Knight CH, Peaker M: Development of the mammary gland. J Reprod Fertil 1982, 65(2):521-536.
• [43]Macias H, Hinck L: Mammary gland development. Wiley Interdiscip Rev Dev Biol 2012, 1(4):533-557.
• [44]Findlay L: The mammary-glands of the tammar wallaby (macropus-eugenii) during pregnancy and lactation. J Reprod Fertil 1982, 65(1):59.
• [45]Ucar A, Vafaizadeh V, Jarry H, Fiedler J, Klemmt PAB, Thum T, Groner B, Chowdhury K: miR-212 and miR-132 are required for epithelial stromal interactions necessary for mouse mammary gland development. Nat Genet 2010, 42(12):1101-U1100.
• [46]Li Z, Liu HY, Jin XL, Lo LJ, Liu JX: Expression profiles of microRNAs from lactating and non-lactating bovine mammary glands and identification of miRNA related to lactation. BMC Genomics 2012, 13:731. BioMed Central Full Text
• [47]Singh R, Mo YY: Role of microRNAs in breast cancer. Cancer Biol Ther 2013, 14(3):201-212.
• [48]Galio L, Droineau S, Yeboah P, Boudiaf H, Bouet S, Truchet S, Devinoy E: MicroRNA in the ovine mammary gland during early pregnancy: spatial and temporal expression of miR-21, miR-205, and miR-200. Physiol Genomics 2013, 45(4):151-161.
• [49]Nagaoka K, Zhang HL, Watanabe G, Taya K: Epithelial cell differentiation regulated by MicroRNA-200a in mammary glands. Plos One 2013, 8(6):e65127.
• [50]Kumar A, Wong AKL, Tizard ML, Moore RJ, Lefèvre C: miRNA_targets: a database for miRNA target predictions in coding and non-coding regions of mRNAs. Genomics 2012, 100(6):352-356.
• [51]Gailhouste L, Gomez-Santos L, Hagiwara K, Hatada I, Kitagawa N, Kawaharada K, Thirion M, Kosaka N, Takahashi R, Shibata T, Miyajima A, Ochiya T: miR-148a plays a pivotal role in the liver by promoting the hepatospecific phenotype and suppressing the invasiveness of transformed cells. Hepatology 2013, 58(3):1153-1165.
• [52]Chen Y, Song YX, Wang ZN: The MicroRNA-148/152 family: multi-faceted players. Mol Cancer 2013, 12(1):43. BioMed Central Full Text
• [53]Yang J, Kennelly JJ, Baracos VE: The activity of transcription factor Stat5 responds to prolactin, growth hormone, and IGF-I in rat and bovine mammary explant culture. J Anim Sci 2000, 78(12):3114-3125.
• [54]Liu XW, Robinson GW, Wagner KU, Garrett L, WynshawBoris A, Hennighausen L: Stat5a is mandatory for adult mammary gland development and lactogenesis. Gene Dev 1997, 11(2):179-186.
• [55]Labbaye C, Testa U: The emerging role of MIR-146A in the control of hematopoiesis, immune function and cancer. J Hematol Oncol 2012, 5:13. BioMed Central Full Text
• [56]Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M: MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res 2008, 18(5):549-557.
• [57]Lin SM, Li HM, Mu HP, Luo W, Li Y, Jia XZ, Wang SB, Jia XL, Nie QH, Li YG, Zhang XQ: Let-7b regulates the expression of the growth hormone receptor gene in deletion-type dwarf chickens. BMC Genomics 2012, 13:306. BioMed Central Full Text
• [58]Wang M, Moisa S, Khan MJ, Wang J, Bu D, Loor JJ: MicroRNA expression patterns in the bovine mammary gland are affected by stage of lactation. J Dairy Sci 2012, 95(11):6529-6535.
• [59]Henao-Mejia J, Williams A, Goff Loyal A, Staron M, Licona-Limón P, Kaech Susan M, Nakayama M, Rinn John L, Flavell Richard A: The MicroRNA miR-181 is a critical cellular metabolic rheostat essential for NKT cell ontogenesis and lymphocyte development and homeostasis. Immunity 2013, 38(5):984-997.
• [60]Neel JC, Lebrun JJ: Activin and TGFbeta regulate expression of the microRNA-181 family to promote cell migration and invasion in breast cancer cells. Cellular signalling 2013, 25(7):1556-1566.
• [61]Guo SL, Peng Z, Yang X, Fan KJ, Ye H, Li ZH, Wang Y, Xu XL, Li J, Wang YL, Teng Y, Yang X: miR-148a promoted cell proliferation by targeting p27 in gastric cancer cells. Int J Biol Sci 2011, 7(5):567-574.
• [62]Li P, Peng J, Hu J, Xu Z, Xie W, Yuan L: Localized expression pattern of miR-184 in Drosophila. Mol Biol Rep 2011, 38(1):355-358.
• [63]Liu CM, Teng ZQ, Santistevan NJ, Szulwach KE, Guo WX, Jin P, Zhao XY: Epigenetic regulation of miR-184 by MBD1 governs neural stem cell proliferation and differentiation. Cell Stem Cell 2010, 6(5):433-444.
• [64]McKiernan RC, Jimenez-Mateos EM, Sano T, Bray I, Stallings RL, Simon RP, Henshall DC: Expression profiling the microRNA response to epileptic preconditioning identifies miR-184 as a modulator of seizure-induced neuronal death. Exp Neurol 2012, 237(2):346-354.
• [65]Großhans H, Johnson T, Reinert KL, Gerstein M, Slack FJ: The temporal patterning MicroRNA let-7 regulates several transcription factors at the larval to adult transition in C. elegans. Dev Cell 2005, 8(3):321-330.
• [66]Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G: The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 2000, 403(6772):901-906.
• [67]Filipowicz W, Großhans H: The Liver-Specific MicroRNA miR-122: Biology and Therapeutic Potential. In Epigenetics and Disease. Volume 67. Edited by Gasser SM, Li E. Picassoplatz 4, 4052 Basel, Switzerland: Springer Basel AG; 2011::221-238. http://www.springer.com/gp/about-springer/company-information/locations/springer-basel-ag webcite
• [68]Xu H, He J-H, Xiao Z-D, Zhang Q-Q, Chen Y-Q, Zhou H, Qu L-H: Liver-enriched transcription factors regulate MicroRNA-122 that targets CUTL1 during liver development. Hepatology 2010, 52(4):1431-1442.
• [69]Wu X, Wu SQ, Tong L, Luan TA, Lin LX, Lu SL, Zhao WR, Ma QQ, Liu HM, Zhong ZH: miR-122 affects the viability and apoptosis of hepatocellular carcinoma cells. Scand J Gastroentero 2009, 44(11):1332-1339.
• [70]Jovicic A, Zaldivar Jolissaint JF, Moser R, Silva Santos MF, Luthi-Carter R: MicroRNA-22 (miR-22) overexpression is neuroprotective via general anti-apoptotic effects and may also target specific Huntington’s disease-related mechanisms. Plos One 2013, 8(1):e54222.
• [71]Choong ML, Yang HH, McNiece I: MicroRNA expression profiling during human cord blood-derived CD34 cell erythropoiesis. Exp Hematol 2007, 35(4):551-564.
• [72]Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RHA: Targeted inhibition of miRNA maturation with morpholinos reveals a role for miR-375 in pancreatic islet development. Plos Biol 2007, 5(8):1738-1749.
• [73]Poy MN, Hausser J, Trajkovski M, Braun M, Collins S, Rorsman P, Zavolan M, Stoffel M: miR-375 maintains normal pancreatic α- and β-cell mass. Proc Natl Acad Sci 2009, 106(14):5813-5818.
• [74]Avnit-Sagi T, Kantorovich L, Kredo-Russo S, Hornstein E, Walker MD: The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. Plos One 2009, 4(4):e5033.
• [75]Conte I, Carrella S, Avellino R, Karali M, Marco-Ferreres R, Bovolenta P, Banfi S: miR-204 is required for lens and retinal development via Meis2 targeting. Proc Natl Acad Sci 2010, 107(35):15491-15496.
• [76]Avellino R, Carrella S, Pirozzi M, Risolino M, Salierno FG, Franco P, Stoppelli P, Verde P, Banfi S, Conte I: miR-204 targeting of Ankrd13A controls both mesenchymal neural crest and lens cell migration. Plos One 2013, 8(4):e61099.
• [77]Agrawal R, Tran U, Wessely O: The miR-30 miRNA family regulates Xenopus pronephros development and targets the transcription factor Xlim1/Lhx1. Development 2009, 136(23):3927-3936.
• [78]Büssing I, Slack FJ, Großhans H: let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 2008, 14(9):400-409.
• [79]Biton M, Levin A, Slyper M, Alkalay I, Horwitz E, Mor H, Kredo-Russo S, Avnit-Sagi T, Cojocaru G, Zreik F, Bentwich Z, Poy MN, Artis D, Walker MD, Hornstein E, Pikarsky E, Ben-Neriah Y: Epithelial microRNAs regulate gut mucosal immunity via epithelium-T cell crosstalk. Nat Immunol 2011, 12(3):239-U275.
• [80]Mark RF, Marotte LR: Australian marsupials as models for the developing mammalian visual system. Trends Neurosci 1992, 15(2):51-57.
• [81]Jellinger KA: The neurobiology of Australian marsupials: brain evolution in the other mammalian radiation. Eur J Neurol 2011, 18(5):e52-e52.
• [82]Saunders N: Marsupials as Models for Studies of Development and Regeneration of the Central Nervous System. In Marsupial Biology: Recent Research, new Perspectives. LA SNH: University of New South Wales Press Ltd; 1997:380-405.
• [83]Wilkes G, Janssens P: Development of urine concentrating ability in pouch young of a marsupial, the tammar wallaby (Macropus eugenii). J Comp Physiol B 1986, 156(4):573-582.
• [84]Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, Neve EPA, Scheynius A, Gabrielsson S: Exosomes with immune modulatory features are present in human breast milk. J Immunol 2007, 179(3):1969-1978.
• [85]Lasser C, Alikhani VS, Ekstrom K, Eldh M, Paredes PT, Bossios A, Sjostrand M, Gabrielsson S, Lotvall J, Valadi H: Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med 2011, 9:9. BioMed Central Full Text
• [86]Creemers EE, Tijsen AJ, Pinto YM: Circulating MicroRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res 2012, 110(3):483-495.
• [87]Old JM, Deane EM: The lymphoid and immunohaematopoietic tissues of the embryonic brushtail possum (Trichosurus vulpecula). Anat Embryol 2003, 206(3):193-197.
• [88]Westrom BR, Svendsen J, Ohlsson BG, Tagesson C, Karlsson BW: Intestinal transmission of macromolecules (BSA and FITC-labelled dextrans) in the neonatal pig. Influence of age of piglet and molecular weight of markers. Biol Neonate 1984, 46(1):20-26.
• [89]Teichberg S, Wapnir RA, Moyse J, Lifshitz F: Development of the neonatal rat small intestinal barrier to nonspecific macromolecular absorption.2. Role of dietary corticosterone. Pediatr Res 1992, 32(1):50-57.
• [90]Lecce JG, Broughto CW: Cessation of uptake of macromolecules by neonatal guinea-pig, hamster and rabbit intestinal epithelium (Closure) and transport into blood. J Nutr 1973, 103(5):744-750.
• [91]van Niel G, Heyman M: II. Intestinal epithelial cell exosomes: perspectives on their structure and function. Am J Physiol Gastrointest Liver Physiol 2002, 283(2):G251-G255.
• [92]Hu G, Drescher KM, Chen X: Exosomal miRNAs: biological properties and therapeutic potential. Front Genet 2012, 3:56.
• [93]Meunier J, Lemoine F, Soumillon M, Liechti A, Weier M, Guschanski K, Hu H, Khaitovich P, Kaessmann H: Birth and expression evolution of mammalian microRNA genes. Genome Res 2013, 23(1):34-45.
• [94]Barrett T, Troup DB, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Muertter RN, Holko M, Ayanbule O, Yefanov A, Soboleva A: NCBI GEO: archive for functional genomics data sets–10 years on. Nucleic Acids Res 2011, 39(Database issue):D1005-D1010.
• [95]Amit Kumar LB, Kuruppath S, Ngo KP, Nicholas KR, Lefèvre C: The Emerging Role of Micro-RNAs in the Lactation Process. In Lactation: Natural Processes, Physiological Responses and Role in Maternity. Edited by Gutierrez LMRCDCO. [Hauppauge] New York: Nova Biomedical: Nova Science Publishers Inc; 2012.
• [96]Varkonyi-Gasic E, Wu RM, Wood M, Walton EF, Hellens RP: Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 2007, 3:12. BioMed Central Full Text