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PMID: 34570913 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Regulatory roles of three miRNAs on allergen mRNA expression in Tyrophagus putrescentiae.

Allergy ·Vol. 77 ·No. 2 ·2022-00-00 ·Pages 469-482

Zhou Y, Li Q, Pan R, Wang Q, Zhu X, Yuan C, Cai F, Gao YD, Cui Y

Abstract

Tyrophagus putresecentiae is an important mite species in rural and urban environments, causing sensitization and allergic disease. While evidence suggests that microRNAs (miRNAs) may regulate the expression of allergen-encoding genes, no study has directly investigated this possibility. Here, this gap was addressed by profiling miRNAs and elucidating their target allergen messenger RNAs (mRNAs) in this mite species. Small RNA and transcriptome libraries were constructed for eggs, larvae, nymphs, and adults. After deep miRNA and whole-transcriptome sequencing were performed, the miRNA and allergen-encoding mRNA regulatory networks were explored. A total of 540 miRNAs were identified, including 155 with expression levels differing significantly across the four mite developmental stages (p < .01), 59 of which were novel. The mRNA expression for allergens was higher for Tyr p 1 in adults than in other developmental stages; Tyr p 2-5, 7, 10, 13, 33, and 34 in immature stages; and Tyr p 28, 35, and 36 in eggs and adults. A combined miRNA and transcriptome bioinformatics analysis showed that allergen Tyr p 3 was regulated by miRNA PC-5p-5698441_1, Tyr p 4 was regulated by PC-5p-7050653_1, and Tyr p 34 was regulated by PC-5p-5534223_1 and PC-5p-5698441_1. These three allergen mRNA and three miRNAs were identified using qRT-PCR, and their regulatory roles were confirmed by double-fluorescent reporter gene system and site-directed mutagenesis technology. For the first time, allergen mRNA expression and miRNAs were profiled throughout the life cycle for an allergen-producing mite, and the results showed that miRNAs bind to target allergen mRNAs to regulate their expression.

Keywords
Tyrophagus putrescentiae double-fluorescent reporter gene system microRNA qRT-PCR transcriptome
MeSH Terms
Acaridae Adult Allergens/genetics Animals Gene Expression Profiling Gene Regulatory Networks Humans Hypersensitivity/genetics,metabolism MicroRNAs/genetics,metabolism Mites RNA, Messenger/genetics Transcriptome
Chemicals
Allergens MicroRNAs RNA, Messenger
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Zhou Ying
Department of Pediatrics Laboratory, The Affiliated Wuxi Children's Hospital of Nanjing Medical University, Wuxi, China.
Li Qingqing
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Pan Ruilin
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Wang Qiong
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Zhu Xuming
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Yuan Cunyin
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Cai Fangfang
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
Gao Ya-Dong ORCID
Department of Allergology, Zhongnan Hospital of Wuhan University, Wuhan, China.
Cui Yubao ORCID
Department of Clinical Laboratory, The Affiliated Wuxi People's Hospital of Nanjing Medical University, Wuxi, China.
References (49)
49 references, click to expand
  1. Li L, Qian J, Zhou Y, Cui Y. Domestic mite-induced allergy: causes, diagnosis, and future prospects. Int J Immunopathol Pharmacol. 2018;32:1-8.
  2. Lee J, Kim JY, Yi MH, et al. Comparative microbiome analysis of Dermatophagoides farinae, Dermatophagoides pteronyssinus, and Tyrophagus putrescentiae. J Allergy Clin Immunol. 2019;143(4):1620-1623.
  3. Shen CY, Yen CY, Chien DK, Tsai JJ, Yu SJ, Liao EC. Influence of storage conditions on the infestation of Tyrophagus putrescentiae and prevalence of mite hypersensitivity in Taiwan. Exp Appl Acarol. 2020;80(3):381-398.
  4. Hubert J, Nesvorna M, Klimov P, Dowd SE, Sopko B, Erban T. Differential allergen expression in three Tyrophagus putrescentiae strains inhabited by distinct microbiome. Allergy. 2019;74(12):2502-2507.
  5. Green WF, Woolcock AJ. Tyrophagus putrescentiae: an allergenically important mite. Clin Exp Allergy. 2010;8(2):135-144.
  6. Yu CH, Tsai JJ, Lin YH, et al. Identification the cross-reactive or species-specific allergens of Tyrophagus putrescentiae and development molecular diagnostic kits for allergic diseases. Diagnostic. 2020;10(9):665.
  7. Zhang C, Li J, Lai X, et al. House dust mite and storage mite IgE reactivity in allergic patients from Guangzhou, China. Asian Pac J Allergy Immunol. 2012;30(4):294-300.
  8. Kondreddi PK, Elder BL, Morgan MS, et al. Importance of sensitization to Tyrophagus putrescentiae in the United States. Ann Allergy Asthma Immunol. 2006;96(1):124.
  9. Jõgi NO, Kleppe Olsen R, Svanes C, et al. Prevalence of allergic sensitization to storage mites in Northern Europe. Clin Exp Allergy. 2020;50(3):372-382.
  10. Cui Y, Yu L, Teng F, et al. Transcriptomic/proteomic identification of allergens in the mite Tyrophagus putrescentiae. Allergy. 2016;71(11):1635-1639.
  11. Bordas-Le Floch V, Le Mignon M, Bussieres L, et al. A combined transcriptome and proteome analysis extends the allergome of house dust mite Dermatophagoides species. PLoS One. 2017;12:e0185830.
  12. Miller JD. The role of dust mites in allergy. Clin Rev Allergy Immunol. 2018;66:1-18.
  13. Saliminejad K, Khorram Khorshid HR, Soleymani Fard S, Ghaffari SH. An overview of microRNAs: Biology, functions, therapeutics, and analysis methods. J Cell Physiol. 2019;234(5):5451-5465.
  14. Yuan Y, Weidhaas JB. Functional microRNA binding site variants. Mol Oncol. 2019;13(1):4-8.
  15. Liang H, Zen K, Zhang J, Zhang CY, Chen X. New roles for microRNAs in cross-species communication. RNA Biol. 2013r;10(3):367-370.
  16. Wang ZZ, Ye XQ, Shi M, et al. Parasitic insect-derived miRNAs modulate host development. Nat Commun. 2018;9(1):2205.
  17. Liu B, Dou W, Ding TB, et al. An analysis of the small RNA transcriptome of four developmental stages of the citrus red mite (Panonychus citri). Insect Mol Biol. 2014;23(2):216-229.
  18. Rong X, Zhang YK, Zhang KJ, Hong XY. Identification of Wolbachia-responsive microRNAs in the two-spotted spider mite, Tetranychus urticae. BMC Genom. 2014;15(1):1122.
  19. Vidal-Quist JC, Ortego F, Lombardero M, Castañera P, Hernández-Crespo P. Allergen expression in the European house dust mite Dermatophagoides pteronyssinus throughout development and response to environmental conditions. Med Vet Entomol. 2015;29(2):137-146.
  20. Fan QH, Zhang ZQ. Revision of some species of Tyrophagus (Acari: Acaridae) in the Oudemans Collection. Syst Appl Acarol. 2007;12(3-4):253-280.
  21. Haas BJ, Papanicolaou A, Yassour M, et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc. 2013;8(8):1494-1512.
  22. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.
  23. Chen Y, Qin C, Cui X, Geng W, Xian G, Wang Z. miR-4510 acts as a tumor suppressor in gastrointestinal stromal tumor by targeting APOC2. J Cell Physiol. 2020;235(7-8):5711-5721.
  24. Peng W, Yu S, Handler AM, et al. miRNA-1-3p is an early embryonic male sex-determining factor in the Oriental fruit fly Bactrocera dorsalis. Nat Commun. 2020;11(1):932.
  25. Sanchez B, Zhou X, Gardiner AS, et al. Serum-borne factors alter cerebrovascular endothelial microRNA expression following particulate matter exposure near an abandoned uranium mine on the Navajo Nation. Part Fibre Toxicol. 2020;17(1):29.
  26. Zhou F, Tang D, Xu Y, et al. Identification of microRNAs and their Endonucleolytic Cleavaged target mRNAs in colorectal cancer. BMC Cancer. 2020;20(1):242.
  27. Lin Z, Li Q, Yin Q, et al. Identification of novel miRNAs and their target genes in Eucalyptus grandis. Tree Genet Genomes. 2018;14(4):1-9.
  28. Drobna M, Szarzyńska B, Jaksik R, et al. hsa-miR-20b-5p and hsa-miR-363-3p affect expression of PTEN and BIM tumor suppressor genes and modulate survival of T-ALL cells in vitro. Cells. 2020;9(5):1137.
  29. Jeong KY, Kim CR, Un S, et al. Allergenicity of recombinant troponin C from Tyrophagus putrescentiae. Int Arch Allergy Immunol. 2010;151(3):207-213.
  30. Arbesman CE. Standardization of allergen extracts. Jpn J Allergol. 1977;26(3):118-119.
  31. Spiric J, Reuter A, Rabin RL. Mass spectrometry to complement standardization of house dust mite and other complex allergenic extracts. Clin Exp Allergy: J Br Soc Allergy Clin Immunol. 2017;47(5):604-617.
  32. Barber D, Diaz-Perales A, Escribese MM, et al. Molecular allergology and its impact in specific allergy diagnosis and therapy. Allergy. 2021;76(12):3642-3658.
  33. Johansson E, Johansson SG, Van Hage-Hamsten M. Allergenic characterization of Acarus siro and Tyrophagus putrescentiae and their crossreactivity with Lepidoglyphus destructor and Dermatophagoides pteronyssinus. Clin Exp Allergy: J Br Soc Allergy Clin Immunol. 1994;24(8):743-751.
  34. Eriksson TL, Johansson E, Whitley P, Schmidt M, Elsayed S, van Hage-Hamsten M. Cloning and characterisation of a group II allergen from the dust mite Tyrophagus putrescentiae. Eur J Biochem. 1998;251(1-2):443-447.
  35. Johansson E, Eriksson TL, Olsson S, et al. Evaluation of specific IgE to the recombinant group 2 mite allergens Lep d 2 and Tyr p 2 in the Pharmacia CAP system. Int Arch Allergy Immunol. 1999;120(1):43-49.
  36. Kronqvist M, Johansson E, Pershagen G, Johansson SG, van Hage-Hamsten M. Increasing prevalence of asthma over 12 years among dairy farmers on Gotland, Sweden: storage mites remain dominant allergens. Clin Exp Allergy: J Br Soc Allergy Clin Immunol. 1999;29(1):35-41.
  37. Liao EC, Hsu EL, Tsai JJ, Ho CM. Immunologic characterization and allergenicity of recombinant Tyr p 3 allergen from the storage mite Tyrophagus putrescentiae. Int Arch Allergy Immunol. 2009;150(1):15-24.
  38. Teng FX, Huang HF, Ge DZ, et al. Tyrophagus putrescentiae group 4 allergen allergenicity and epitope prediction. Allergol Immunopathol (Madr). 2020;48(6):619-625.
  39. Monsanto-Hearne V, Johnson KN. miRNAs in insects infected by animal and plant viruses. Viruses. 2018;10(7):354.
  40. Asgari S. Role of microRNAs in insect host-microorganism interactions. Front Physiol. 2011;2:48.
  41. Clément T, Salone V, Rederstorff M. Dual luciferase gene reporter assays to study miRNA function. Methods Mol Biol. 2015;1296:187-198.
  42. Deng JH, Zheng GY, Li HZ, Ji ZG. MiR-212-5p inhibits the malignant behavior of clear cell renal cell carcinoma cells by targeting TBX15. Eur Rev Med Pharmacol Sci. 2019;23(24):10699-10707.
  43. Zhang C, Wang MM, Zhang Y, Yang L, Zhu MS, Dong QR. Downregulation of miRNA-127-5p aggravates spinal cord injury through activating MAPK1. Eur Rev Med Pharmacol Sci. 2019;23(24):10617-10622.
  44. Zhou CL, Li F, Wu XW, et al. Overexpression of miRNA-433-5p protects acute spinal cord injury through activating MAPK1. Eur Rev Med Pharmacol Sci. 2020;24(6):2829-2835.
  45. Collison A, Mattes J, Plank M, Foster PS. Inhibition of house dust mite-induced allergic airways disease by antagonism of microRNA-145 is comparable to glucocorticoid treatment. J Allergy Clin Immunol. 2011;128(1):160-167.
  46. Dong X, Zhong N, Fang Y, et al. MicroRNA 27b-3p modulates SYK in pediatric asthma induced by dust mites. Front Pediatr. 2018;6:301.
  47. Jiang M, Sang X, Hong Z. Beyond nutrients: food-derived microRNAs provide cross-kingdom regulation. BioEssays. 2012;34(4):280-284.
  48. Zhang L, Hou D, Chen X, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell Res. 2012;22:107-126.
  49. Chin AR, Fong MY, Somlo G, et al. Cross-kingdom inhibition of breast cancer growth by plant miR159. Cell Res. 2016;26(2):217-228.
Article Info
Journal
Allergy
Abbr.
Allergy
ISSN
1398-9995
DOI
10.1111/all.15111
Published
2022-00-00
Epub
2021-00-04
Pages
469-482
Language
English
Region
Denmark
NLM ID
7804028
Subset
IM
Databases
RefSeq
DQ983318.1, EU302595.1, FJ534553.1, KF964489
External Links
PubMed source DOI: 10.1111/all.15111 View journal details
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