Prognostic significance of the breast milk microRNA impact on the immune response of a newborn with intrauterine growth retardation

Authors

DOI:

https://doi.org/10.15574/SP.2021.113.53

Keywords:

intrauterine growth retardation, intrauterine growth restriction, IGR, breast milk, microRNA, miR, immune response, immunity, review

Abstract

This literature review provides current information about intrauterine growth retardation (IGR) as one of the causes of perinatal morbidity and mortality. There is a sustaining trend to augmentation of the UGR level despite the new methods of diagnostics, treatment and prevention development. Furthermore, there is high percentage of complications among children with IGR at any age. Therefore, early diagnostics of accompanying diseases in children with IGR sparks the interest, especially in view of the fact the new diagnostic methods incipience. The article highlights the features of the neonatal immune response, including the one in children with IGR. These data indicate the predominance of non-specific immune response over specific one, prevalence of generalized inflammation, decreased activity of phagocytes, neutrophils, specific antigen-presenting cells (APC) as a response to most of the Toll-like receptor agonists (TLRAs), high levels of interleukin-6 and interleuken-23. Moreover, analyzed sources demonstrate spurt of growth of the levels of proinflammatory factors, despite the fact of their relatively low levels in neonates with IGR right after birth. Increased levels of proinflammatory cytokines on the ground of systemic inflammation is an unfavorable factor of the course of the disease. In addition, the review contents the information about microRNA presence in the breast milk. MicroRNAs are small non-coding RNAs of 19–23 nucleotides in length that regulate the expression of the target gene. Breast milk microRNAs are resistant to the enzymes of the gastrointestinal tract of the child and are mainly absorbed. There are the data, proving the change of the transcriptome of the breast milk microRNA depending on the gestational age, the nature of labor, the mother's diet, her medication. According to the mentioned studies, the breast milk microRNA, that are detected in the early stages of lactation (miR-155, miR-148a, miR-146b, miR-181a, miR-181b, miR-17), probably change the levels of pro- and anti-inflammatory cytokines and regulate acuity of the child's immune response. Research of the breast milk microRNA may be important for the prediction of the presence of possible inflammatory complications in a child with IGR. We used such databases as Scopus, Web of Science, MedLine, PubMed, Google Scholar, CyberLeninka, RSCI for writing the article.

No conflict of interest was declared by the author.

Key words: intrauterine growth retardation, intrauterine growth restriction, IGR, breast milk, microRNA, miR, immune response, immunity, review.

Author Biographies

O.E. Abaturov, SI «Dnipropetrovsk Medical Academy of Ministry of Health of Ukraine», Dnipro

This literature review provides current information about intrauterine growth retardation (IGR) as one of the causes of perinatal morbidity and mortality. There is a sustaining trend to augmentation of the UGR level despite the new methods of diagnostics, treatment and prevention development. Furthermore, there is high percentage of complications among children with IGR at any age. Therefore, early diagnostics of accompanying diseases in children with IGR sparks the interest, especially in view of the fact the new diagnostic methods incipience. The article highlights the features of the neonatal immune response, including the one in children with IGR. These data indicate the predominance of non-specific immune response over specific one, prevalence of generalized inflammation, decreased activity of phagocytes, neutrophils, specific antigen-presenting cells (APC) as a response to most of the Toll-like receptor agonists (TLRAs), high levels of interleukin-6 and interleuken-23. Moreover, analyzed sources demonstrate spurt of growth of the levels of proinflammatory factors, despite the fact of their relatively low levels in neonates with IGR right after birth. Increased levels of proinflammatory cytokines on the ground of systemic inflammation is an unfavorable factor of the course of the disease. In addition, the review contents the information about microRNA presence in the breast milk. MicroRNAs are small non-coding RNAs of 19–23 nucleotides in length that regulate the expression of the target gene. Breast milk microRNAs are resistant to the enzymes of the gastrointestinal tract of the child and are mainly absorbed. There are the data, proving the change of the transcriptome of the breast milk microRNA depending on the gestational age, the nature of labor, the mother's diet, her medication. According to the mentioned studies, the breast milk microRNA, that are detected in the early stages of lactation (miR-155, miR-148a, miR-146b, miR-181a, miR-181b, miR-17), probably change the levels of pro- and anti-inflammatory cytokines and regulate acuity of the child's immune response. Research of the breast milk microRNA may be important for the prediction of the presence of possible inflammatory complications in a child with IGR. We used such databases as Scopus, Web of Science, MedLine, PubMed, Google Scholar, CyberLeninka, RSCI for writing the article.

No conflict of interest was declared by the author.

Key words: intrauterine growth retardation, intrauterine growth restriction, IGR, breast milk, microRNA, miR, immune response, immunity, review.

A.O. Tovarnytska, Limited Liability Company «Dnipropetrovsk Medical Institute of Traditional and Non$traditional Medicine», Dnipro, Ukraine

This literature review provides current information about intrauterine growth retardation (IGR) as one of the causes of perinatal morbidity and mortality. There is a sustaining trend to augmentation of the UGR level despite the new methods of diagnostics, treatment and prevention development. Furthermore, there is high percentage of complications among children with IGR at any age. Therefore, early diagnostics of accompanying diseases in children with IGR sparks the interest, especially in view of the fact the new diagnostic methods incipience. The article highlights the features of the neonatal immune response, including the one in children with IGR. These data indicate the predominance of non-specific immune response over specific one, prevalence of generalized inflammation, decreased activity of phagocytes, neutrophils, specific antigen-presenting cells (APC) as a response to most of the Toll-like receptor agonists (TLRAs), high levels of interleukin-6 and interleuken-23. Moreover, analyzed sources demonstrate spurt of growth of the levels of proinflammatory factors, despite the fact of their relatively low levels in neonates with IGR right after birth. Increased levels of proinflammatory cytokines on the ground of systemic inflammation is an unfavorable factor of the course of the disease. In addition, the review contents the information about microRNA presence in the breast milk. MicroRNAs are small non-coding RNAs of 19–23 nucleotides in length that regulate the expression of the target gene. Breast milk microRNAs are resistant to the enzymes of the gastrointestinal tract of the child and are mainly absorbed. There are the data, proving the change of the transcriptome of the breast milk microRNA depending on the gestational age, the nature of labor, the mother's diet, her medication. According to the mentioned studies, the breast milk microRNA, that are detected in the early stages of lactation (miR-155, miR-148a, miR-146b, miR-181a, miR-181b, miR-17), probably change the levels of pro- and anti-inflammatory cytokines and regulate acuity of the child's immune response. Research of the breast milk microRNA may be important for the prediction of the presence of possible inflammatory complications in a child with IGR. We used such databases as Scopus, Web of Science, MedLine, PubMed, Google Scholar, CyberLeninka, RSCI for writing the article.

No conflict of interest was declared by the author.

Key words: intrauterine growth retardation, intrauterine growth restriction, IGR, breast milk, microRNA, miR, immune response, immunity, review.

References

Abaturov AE, Stepanov YM, Zavgorodnyaya NY. (2019). MikroRNK pri nealkogol'noi zhirovoi bolezni pecheni u detei. MicroRNA in non-alcoholic fatty liver syndrom in children. Dnipro: DOMINANTA PRINT: 252.

Abaturov AE, Zavgorodnyaya NY, Babich VL. (2018). MikroRNK pri zabolevanijah gepatobiliarnoj sistemy. MicroRNA in diseases of the hepatobiliary system. Dnipro: DOMINANTA PRINT: 338.

Abaturov OE, Babych VL. (2017). The role of microRNA in diseases of the biliary system. ZDOROV'E REBENKA. 12 (7): 841-843. https://doi.org/10.22141/2224-0551.12.7.2017.116191

Abaturov OE. (2020). Severe combined immunodeficiency in young children. Dnipro: LIRA: 180.

Alsaweed M, Hartmann PE, Geddes DT, Kakulas F. (2015, Oct 30). MicroRNAs in Breastmilk and the Lactating Breast: Potential Immunoprotectors and Developmental Regulators for the Infant and the Mother. Int J Environ Res Public Health. 12 (11): 13981-14020. https://doi.org/10.3390/ijerph121113981; PMid:26529003 PMCid:PMC4661628

Alsaweed M, Hepworth AR, Lefevre C, Hartmann PE, Geddes DT, Hassiotou F. (2015, Oct). Human Milk MicroRNA and Total RNA Differ Depending on Milk Fractionation. J Cell Biochem. 116 (10): 2397-2407. URL: https://pubmed.ncbi.nlm.nih.gov/25925799. https://doi.org/10.1002/jcb.25207; PMid:25925799 PMCid:PMC5042114

Arntz OJ, Pieters BC, Oliveira MC, Mathijs GA Broeren, Miranda B Bennink, Marieke de Vries et al. (2015, Sep). Oral administration of bovine milk derived extracellular vesicles attenuates arthritis in two mouse models. Mol Nutr Food Res. 59 (9): 1701-1712. URL: https://pubmed.ncbi.nlm.nih.gov/26047123. https://doi.org/10.1002/mnfr.201500222; PMid:26047123

Babar IA, Cheng CJ, Booth CJ, Liang X, Weidhaas JB, Saltzman WM, Slack FJ. (2012, Jun 26). Nanoparticle-based therapy in an in vivo microRNA-155 (miR-155)-dependent mouse model of lymphoma. Proc Natl Acad Sci U S A. 109 (26): 1695-1704. https://doi.org/10.1073/pnas.1201516109; PMid:22685206 PMCid:PMC3387084

Basha S, Surendran N, Pichichero M. (2014). Immune responses in neonates. Expert Rev Clin Immunol. 10 (9): 1171-1184. https://doi.org/10.1586/1744666X.2014.942288; PMid:25088080 PMCid:PMC4407563

Belousova TV, Andriushina IV. (2018). Zaderzhka vnutriutrobnogo razvitiia i ee vliianie na sostoianie zdorov'ia. Sovremennye podkhody k vskarmlivaniiu detei. Fetal growth retardation and its impact on health. Modern approaches to feeding children. LECHASHCHII VRACH. ISSN: 2687-1181.

Carney MC, Tarasiuk A, DiAngelo SL, Silveyra P, Podany A, Birch LL et al. (2017, Aug). Metabolism>related microRNAs in maternal breast milk are influenced by premature delivery. Pediatr Res. 82 (2): 226-236. URL: www.ncbi.nlm.nih.gov/pmc/articles/PMC5552431/. https://doi.org/10.1038/pr.2017.54; PMid:28422941 PMCid:PMC5552431

Carr L, Bowlin AK, Elolimy AA, Byrum SD, Washam CL, Randolph CE. (2020, June 23). Neonatal Diet Impacts Circulatory miRNA Profile in a Porcine Model. Front Immunol. URL: https://www.frontiersin.org/https://doi.org/10.3389/fimmu.2020.01240. https://doi.org/10.3389/fimmu.2020.01240; PMid:32655560 PMCid:PMC7324749

Carrillo-Lozano E, Sebastian-Valles F, Knott-Torcal C. (2020). Circulating microRNAs in Breast Milk and Their Potential Impact on the Infant. Nutrients. 12 (10): 3066. Published 2020 Oct 8. https://doi.org/10.3390/nu12103066; PMid:33049923 PMCid:PMC7601398

Cheng HS, Sivachandran N, Lau A, Boudreau E, Zhao JL, Baltimore D, Delgado-Olguin P, Cybulsky MI, Fish JE. (2013, Jul). MicroRNA-146 represses endothelial activation by inhibiting pro-inflammatory pathways. EMBO Mol Med. 5 (7): 1017-1034. https://doi.org/10.1002/emmm.201202318; PMid:23733368 PMCid:PMC3721471

Colella M, Frerot A, Novais ARB, Baud O. (2018). Neonatal and Long-Term Consequences of Fetal Growth Restriction. Current Pediatric Reviews. 14 (4): 212-218. https://doi.org/10.2174/1573396314666180712114531; PMid:29998808 PMCid:PMC6416241

Dan C, Jinjun B, Zi-Chun H, Lin M, Wei C, Xu Z, Ri Z, Shun C, Wen-Zhu S, Qing-Cai J, Wu Y. (2015, Feb). Modulation of TNF-α mRNA stability by human antigen R and miR181s in sepsis-induced immunoparalysis. EMBO Mol Med. 7 (2): 140-157. https://doi.org/10.15252/emmm.201404797; PMid:25535255 PMCid:PMC4328645

Eissa MG, Artlett CM. (2019). The MicroRNA miR-155 Is Essential in Fibrosis. Non-Coding RNA. 5 (1): 23. URL: https://www.mdpi.com/2311-553X/5/1/23/htm. https://doi.org/10.3390/ncrna5010023; PMid:30871125 PMCid:PMC6468348

Golan-Gerstl R, Elbaum Shiff Y, Moshayoff V, Schecter D, Leshkowitz D, Reif S. (2017, Oct). 23 Characterization and biological function of milk-derived miRNAs. Mol Nutr Food Res. 61 (10). https://doi.org/10.1002/mnfr.201700009; PMid:28643865

Gromova AM, Berezhna VA. (2018). Etiological and pathogenetic aspects of intrauterine growth retardation. Current problems of modern medicine: Bulletin of the Ukrainian Medical Dental Academy. 3: 63. URL: https://cyberleninka.ru/.

Hajdukov SV, Zurochka AV. (2011). Analysis of T-helper subpopulations (Th1, Th2, Treg, Th17, activated T-helpers) by means of cytometry. MEDICINSKAJA IMMUNOLOGIJA. 13 (1,7-16). URL: https://www.mimmun.ru/. https://doi.org/10.15789/1563-0625-2011-1-7-16

Hanwei J, Nie X, Zhu H, Li B, Pang F, Yang X, Cao R, Yang X, Zhu S, Peng D, Li Y, Li G, Zhang Z, Huang H, Xu K, Zhao T, Cheng Y, Chen C, Du L, Wang F. (2020, Jan 19). miR-146b-5p Plays a Critical Role in the Regulation of Autophagy in Dper Brucella melitensis-Infected RAW264.7 Cells. Biomed Res Int: 1953242. https://doi.org/10.1155/2020/1953242; PMid:32051823 PMCid:PMC6995328

He Y, Lawlor NT, Newburg DS. (2016, Jan 15). Human Milk Components Modulate Toll-Like Receptor-Mediated Inflammation. Adv Nutr. 7 (1): 102-111. https://doi.org/10.3945/an.115.010090; PMid:26773018 PMCid:PMC4717889

Herwijnen van MJC, Driedonks TAP, Snoek BL, Kroon AMT, Kleinjan M, Jorritsma R, Pieterse CMJ, Hoen ENMN, Wauben MHM. (2018, Sep 18). Abundantly Present miRNAs in Milk-Derived Extracellular Vesicles Are Conserved Between Mammals. Front Nutr. 5: 81. https://doi.org/10.3389/fnut.2018.00081; PMid:30280098 PMCid:PMC6153340

Hutchison ER, Kawamoto EM, Taub DD, Lal A, Abdelmohsen K, Zhang Y, Wood WH 3rd, Lehrmann E, Camandola S, Becker KG, Gorospe M, Mattson MP. (2013, Jul). Evidence for miR-181 involvement in neuroin-flammatory responses of astrocytes. Glia. 61 (7): 1018-1028. https://doi.org/10.1002/glia.22483; PMid:23650073 PMCid:PMC4624280

Jiang K, Yang J, Yang C, Zhang T, Shaukat A, Yang X, Dai A, Wu H, Deng G. (2020, Jan). miR-148a suppresses inflammation in lipopolysaccharide-induced endometritis. J Cell Mol Med. 24 (1): 405-417. Epub 2019 Nov 22. https://doi.org/10.1111/jcmm.14744; PMid:31756048 PMCid:PMC6933404

Jiang X, Xu C, Lei F, Liao M, Wang W, Xu N, Zhang Y, Xie W. (2017, Jul 13). MiR-30a targets IL-1α and regulates islet functions as an inflammation buffer and response factor. Sci Rep. 7 (1): 5270. https://doi.org/10.1038/s41598-017-05560-1; PMid:28706254 PMCid:PMC5509704

Kosaka N, Izumi H, Sekine K, Ochiya T. (2010, Mar 1). microRNA as a new immune>regulatory agent in breast milk. Silence. 1 (1): 7. https://doi.org/10.1186/1758-907X-1-7; PMid:20226005 PMCid:PMC2847997

Kusuma RJ, Manca S, Friemel T, Sukreet S, Nguyen C, Zempleni J. (2016, May 15). Human vascular endothelial cells transport foreign exosomes from cow's milk by endocytosis. Am J Physiol Cell Physiol. 310 (10): C800-807. https://doi.org/10.1152/ajpcell.00169.2015; PMid:26984735 PMCid:PMC4895447

Kutty RK, Nagineni CN, Samuel W, Vijayasarathy C, Jaworski C, Duncan T, Cameron JE, Flemington EK, Hooks JJ, Redmond TM. (2013, Apr 3). Differential regulation of microRNA-146a and microRNA-146b-5p in human retinal pigment epithelial cells by interleukin-1β, tumor necrosis factor-α, and interferon-γ. Mol Vis. 19: 737-750. PMID: 23592910. PMCID: PMC3626297.

Leiferman A, Shu J, Upadhyaya B, Cui J, Zempleni J. (2019, Aug). Storage of Extracellular Vesicles in Human Milk, and MicroRNA Profiles in Human Milk Exosomes and Infant Formulas. 69 (2): 235>238. https://doi.org/10.1097/MPG.0000000000002363; PMid:31169664 PMCid:PMC6658346

Lezhenko GO, Usachova OV. (2011). Urodzhene ta rannje postnatal'ne infikuvannja plodu j novonarodzhenogo cytomegalovirusom: osoblyvosti perebigu, problemy diagnostyky, likuvannja ta profilaktyky. Congenital and early postnatal cytomegalovirus infection of fetus and newborn: peculiarities of the course, problems of diagnosis, treatment and prevention. DYTIACHYI LIKAR. 6 (13): 26-35. eISSN: 2522-4123.

Li G, Tang X, Chen H, Sun W, Yuan F. (2018). miR-148a inhibits pro-inflammatory cytokines released by intervertebral disc cells by regulating the p38/MAPK pathway. Exp Ther Med. 16 (3): 2665-2669. https://doi.org/10.3892/etm.2018.6516

Longo S, Bollani L, Decembrino L, Di Comite A, Angelini M, Stronati M. (2013, Feb). Short-term and long-term sequelae in intrauterine growth retardation (IUGR). J Matern Fetal Neonatal Med. 26 (3): 222-225. https://doi.org/10.3109/14767058.2012.715006; PMid:23030765

Lukasik A, Brzozowska I, Zielenkiewicz U, Zielenkiewicz P. (2018). Detection of Plant miRNAs Abundance in Human Breast Milk. Int J Mol Sci. 19: 37. https://doi.org/10.3390/ijms19010037; PMid:29295476 PMCid:PMC5795987

Mashima R. (2015, Jul). Physiological roles of miR-155. Immunology. 145 (3): 323-333. https://doi.org/10.1111/imm.12468; PMid:25829072 PMCid:PMC4479532

McCoy CE. (2017). miR-155 Dysregulation and Therapeutic Intervention in Multiple Sclerosis. Adv Exp Med Biol. 1024: 111-131. https://doi.org/10.1007/978-981-10-5987-2_5; PMid:28921467

McElrath TF, Allred EN, Van Marter L, Fichorova RN, Leviton A. (2013, Oct). ELGAN Study Investigators. Perinatal systemic inflammatory responses of growth-restricted preterm newborns. Acta Paediatr. 102 (10): e439-442. https://doi.org/10.1111/apa.12339; PMid:23819682 PMCid:PMC3773878

Melnik BC, SM J & Schmitz G. (2014). Milk: an exosomal microRNA transmitter promoting thymic regulatory T cell maturation preventing the development of atopy? J Transl Med. 12: 43. https://doi.org/10.1186/1479-5876-12-43; PMid:24521175 PMCid:PMC3930015

Neta GI, von Ehrenstein OS, Goldman LR et al. (2010). Umbilical cord serum cytokine levels and risks of small-for-gestational-age and preterm birth. Am J Epidemiol. 171 (8): 859-867. https://doi.org/10.1093/aje/kwq028; PMid:20348155 PMCid:PMC2877445

Ole B, Shuqiang R, Anders B, Per Torp S, Duc Ninh N. (2020). Impaired Neonatal Immunity and Infection Resistance Following Fetal Growth Restriction in Preterm Pigs. Frontiers in Immunology. 11. https://doi.org/10.3389/fimmu.2020.01808; PMid:32903565 PMCid:PMC7438575

Pels A, Beune IM, van Wassenaer>Leemhuis AG, Limpens J, Ganzevoort W. (2020, Feb). Early-onset fetal growth restriction: A systematic review on mortality and morbidity. Acta Obstet Gynecol Scand. 99 (2): 153-166. Epub 2019 Sep 10. https://doi.org/10.1111/aogs.13702; PMid:31376293 PMCid:PMC7004054

Perri M, Lucente M, Cannataro R, De Luca IF, Gallelli L, Moro G, De Sarro G, Caroleo MC, Cione E. (2018). Variation in Immune-Related microRNAs Profile in Human Milk Amongst Lactating Women Microrna. 7 (2): 107-114. https://doi.org/10.2174/2211536607666180206150503; PMid:29412128

Rodriguez A, Vigorito E, Clare S, Warren MV, Couttet P, Soond DR, van Dongen S, Grocock RJ, Das PP, Miska EA, Vetrie D, Okkenhaug K, Enright AJ, Dougan G, Turner M, Bradley A. (2007, Apr 27). Requirement of bic/microRNA-155 for normal immune function. Science. 316 (5824): 608-611. https://doi.org/10.1126/science.1139253; PMid:17463290 PMCid:PMC2610435

Ryspaeva DE, Kriachok IA. (2016). The role of microRNA in the individualization of treatment of breast cancer patients. KLINICHNA ONCOLOGIIA. 4: 24. URL: https://www.clinicaloncology.com.ua.

Schuller SS, Kramer BW, Villamor E, Spittler A, Berger A, Levy O. (2018). Immunomodulation to Prevent or Treat Neonatal Sepsis: Past, Present, and Future. Front Pediatr. 6: 199. Published 2018 Jul 19. https://doi.org/10.3389/fped.2018.00199; PMid:30073156 PMCid:PMC6060673

Sharma D, Shastri S, Sharma P. (2016). Intrauterine Growth Restriction: Antenatal and Postnatal Aspects. Clin Med Insights Pediatr. 10: 67-83. Published 2016 Jul 14. https://doi.org/10.4137/CMPed.S40070; PMid:27441006 PMCid:PMC4946587

Sokolova SS, Iakovtsova ІІ, Sergієnko LY, Postnіkov VO, Іvanova NV. (2016). 9 The Frequency of low weight children born with birth in Kharkiv region and the structure of this pathology. VISNYK PROBLEM BIOLOGIJI I MEDYCYNY. 2. URL: https://cyberleninka.ru/.

Sun X, Sit A, Feinberg MW. (2014, Apr). Role of miR-181 family in regulating vascular inflammation and immunity. Trends Cardiovasc Med. 24 (3): 105-112. https://doi.org/10.1016/j.tcm.2013.09.002; PMid:24183793 PMCid:PMC3943593

Tahamtan A, Teymoori-Rad M, Nakstad B, Salimi V. (2018, Jun 25). Anti-Inflammatory MicroRNAs and Their Potential for Inflammatory Diseases Treatment. Front Immunol. 9: 1377. https://doi.org/10.3389/fimmu.2018.01377; PMid:29988529 PMCid:PMC6026627

Ti D, Hao H, Fu X, Han W. (2016, Dec). Mesenchymal stem cells-derived exosomal microRNAs contribute to wound inflammation. Sci China Life Sci. 59 (12): 1305-1312. Epub 2016 Nov 18. https://doi.org/10.1007/s11427-016-0240-4; PMid:27864711

Tome-Carneiro J, Fernandez-Alonso N, Tomas-Zapico C, Visioli F, Iglesias-Gutierrez E, Davalos A. (2018, Jun). Breast milk microRNAs harsh journey towards potential effects in infant development and maturation. Lipid encapsulation can help. Pharmacol Res. 132: 21-32. Epub 2018 Apr 5. https://doi.org/10.1016/j.phrs.2018.04.003; PMid:29627443

Troger B, Muller T, Faust K, Bendiks M, Bohlmann MK, Thonnissen S, Herting E, Gopel W, Hartel C. (2013). Intrauterine growth restriction and the innate immune system in preterm infants of <32 weeks gestation. Neonatology. 103 (3): 199-204. https://doi.org/10.1159/000343260; PMid:23295537

Tsafaras GP, Ntontsi P, Xanthou G. (2020). Advantages and Limitations of the Neonatal Immune System. Front Pediatr. 8: 5. Published 2020 Jan 28. https://doi.org/10.3389/fped.2020.00005; PMid:32047730 PMCid:PMC6997472

Wang F, Wang H, Jin D, Zhang Y. (2018, June). Serum miR-17, IL-4, and IL-6 levels for diagnosis of endometriosis, Medicine. 97 (24): e10853. https://doi.org/10.1097/MD.0000000000010853; PMid:29901577 PMCid:PMC6023682

Williams A, Henao-Mejia J, Harman CC, Flavell RA. (2013). miR-181 and metabolic regulation in the immune system. Cold Spring Harb Symp Quant Biol. 78: 223-230. URL: https://pubmed.ncbi.nlm.nih.gov/24163395/. https://doi.org/10.1101/sqb.2013.78.020024; PMid:24163395

Wixey AJ, Chand KK, Colditz BP, Bjorkman ST. (2017). Neuroinflammation in intrauterine growth restriction. Placenta. 54: 117-124. ISSN 0143-4004. https://doi.org/10.1016/j.placenta.2016.11.012; PMid:27916232

Xie W, Li M, Xu N et al. (2013). MiR-181a regulates inflammation responses in monocytes and macrophages. PLoS One. 8 (3): e58639. https://doi.org/10.1371/journal.pone.0058639; PMid:23516523 PMCid:PMC3596280

Xie Y, Wang L, Sun H, Shang Q, Wang Y, Zhang G, Yang W, Jiang S. (2020, Oct 21). A polysaccharide extracted from alfalfa activates splenic B cells by TLR4 and acts primarily via the MAPK/p38 pathway. Food Funct. 11 (10): 9035-9047. https://doi.org/10.1039/D0FO01711F; PMid:33021613

Zempleni J, Sukreet S, Zhou F, Wu D, Mutai E. (2019, Feb 15). Milk-Derived Exosomes and Metabolic Regulation. Annu Rev Anim Biosci. 7: 245-262. https://doi.org/10.1146/annurev-animal-020518-115300; PMid:30285461

Zhang L, Dong L, Tang Y, Li M, Zhang M. (2020, Jan). MiR-146b protects against the inflammation injury in pediatric pneumonia through MyD88/NF-κB signaling pathway. Infect Dis (Lond). 52 (1): 23-32. https://doi.org/10.1080/23744235.2019.1671987; PMid:31583932

Zhang Y, Lu Y, Ong'achwa MJ, Ge L, Qian Y, Chen L, Hu X, Li F, Wei H, Zhang C, Li C, Wang Z. (2018, Dec 17). Resveratrol Inhibits the TGF-β1-Induced Proliferation of Cardiac Fibroblasts and Collagen Secretion by Downregulating miR-17 in Rat. Biomed Res Int. 2018: 8730593. https://doi.org/10.1155/2018/8730593; PMid:30648109 PMCid:PMC6311767

Zhou Q, Li M, Wang X, Li Q, Wang T, Zhu Q, Zhou X, Wang X, Gao X, Li X. (2012). Immune-related microRNAs are abundant in breast milk exosomes. Int J Biol Sci. 8 (1): 118-123. https://doi.org/10.7150/ijbs.8.118; PMid:22211110 PMCid:PMC3248653

Zhou X, Mao Y, Zhu J, Meng F, Chen Q, Tao L et al. (2016, Oct 11). TGF-β1 promotes colorectal cancer immune escape by elevating B7-H3 and B7-H4 via the miR-155/miR-143 axis. Oncotarget. 7 (41): 67196-67211. https://www.genecards.org/. https://doi.org/10.18632/oncotarget.11950; PMid:27626488 PMCid:PMC5341868

Published

2021-02-19