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PfmPif97-like regulated by Pfm-miR-9b-5p participates in shell formation in Pinctada fucata martensii


Autoři: Xinwei Xiong aff001;  Bingyi Xie aff001;  Zhe Zheng aff001;  Yuewen Deng aff001;  Yu Jiao aff001;  Xiaodong Du aff001
Působiště autorů: Fishery College, Guangdong Ocean University, Zhanjiang, China aff001;  Guangdong Technology Research Center for Pearl Aquaculture and Process, Guangdong Ocean University, Zhanjiang, China aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226367

Souhrn

Mollusk shell matrix proteins are important for the formation of organic frameworks, crystal nucleation, and crystal growth in Pinctada fucata martensii (P. f. martensii). MicroRNAs (miRNAs) are endogenous small non-coding RNAs that play important roles in many biological processes, including shell formation. In this study, we obtained the full-length sequence of Pif97-like gene in P. f. martensii (PfmPif97-like). PfmPif97-like was mainly distributed in mantle pallial and mantle edge. Correlation analysis indicated that the average shell thickness and weight showed a positive correlation with PfmPif97-like expression (P < 0.05). The inner surface of the nacreous layer and prismatic layer showed atypical growth when we knocked down the expression of PfmPif97-like by RNA interference (RNAi). We used a luciferase reporter assay to identify that miR-9b-5p of P. f. martensii (Pfm-miR-9b-5p) downregulated the expression of PfmPif97-like by interacting with the 3′-untranslated region (UTR) while we obtained the same result by injecting the Pfm-miR-9b-5p mimics in vivo. After injecting the mimics, we also observed abnormal growth in nacre layer and prismatic layer which is consistent with the result of RNAi. We proposed that PfmPif97-like regulated by Pfm-miR-9b-5p participates in shell formation of P. f. martensii. These findings provide important clues about the molecular mechanisms that regulate biomineralization in P. f. martensii.

Klíčová slova:

Sequence motif analysis – MicroRNAs – Reverse transcriptase-polymerase chain reaction – Protein sequencing – Larvae – Scanning electron microscopy – Oysters – Biomineralization


Zdroje

1. Ehrlich H. Chitin and collagen as universal and alternative templates in biomineralization. International Geology Review. 2010; 52(7–8): 661–699. http://dx.doi.org/10.1080/00206811003679521

2. Weiner S, Traub W, Parker SB. Macromolecules in Mollusc Shells and Their Functions in Biomineralization. Philosophical Transactions of the Royal Society B: Biological Sciences.1984; 304(1121): 425–434. https://doi.org/10.1098/rstb.1984.0036

3. Addadi L, Joester D, Nudelman F, Steve W. Mollusk shell formation: a source of new concepts for understanding biomineralization processes. Chemistry—A European Journal. 2006; 12(4):980–987. http://dx.doi.org/10.1002/chem.200500980

4. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE. Control of Crystal Phase Switching and Orientation by Soluble Mollusk-Shell Proteins. Nature. 1996; 381(6577):56–58. http://dx.doi.org/10.1038/381056a0

5. Miyamoto H, Miyashita T, Okushima M, Nakano S, Morita T, Matsushiro A. A carbonic anhydrase from the nacreous layer in oyster pearls. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(18): 9657–9660. doi: 10.1073/pnas.93.18.9657 8790386

6. Sudo S, Fujikawa T, Nagakura T, Ohkubo T, Sakaguchi K, Tanaka M, et al. Structures of mollusc shell framework proteins. Nature. 1997; 387(6633):563–564. http://dx.doi.org/10.1038/42391

7. Yano M, Nagai K, Morimoto K, Miyamoto H. A novel nacre protein N19 in the pearl oyster Pinctada fucata. Biochem Biophys Res Commun. 2007; 362 (1):158–163. doi: 10.1016/j.bbrc.2007.07.172 17698035

8. Samata T, Hayashi N, Kono M, Hasegawa K, Horita C, Akera S. A new matrix protein family related to the nacreous layer formation of Pinctada fucata. Febs Letters. 1999; 462(1–2):225–229. doi: 10.1016/s0014-5793(99)01387-3 10580124

9. Suzuki M, Saruwatari K, Kogure T, Yamamoto Y, Nishimura T, Kato T, Nagasawa H. An acidic matrix protein, Pif, is a key macromolecule for nacre formation. Science. 2009; 325(5946):1388–1390. doi: 10.1126/science.1173793 19679771

10. Zhang C, Li S, Ma ZJ, Xie LP, Zhang RQ. A Novel Matrix Protein P10 From The Nacre Of Pearl Oyster (Pinctada Fucata) and Its effects On Both Caco3 Crystal Formation and Mineralogenic Cells. Marine Biotechnology. 2006; 8(6):624–633. doi: 10.1007/s10126-006-6037-1 16972140

11. Zhang Y, Xie LP, Meng QX, Jiang TM, Pu RL, Chen L, et al. A novel matrix protein participating in the nacre framework formation of pearl oyster, Pinctada fucata. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology. 2003; 135(3):565–573. http://dx.doi.org/10.1016/S1096-4959(03)00138-6

12. Tsukamoto D, Sarashina I, Endo K. Structure and expression of an unusually acidic matrix protein of pearl oyster shells. Biochemical & Biophysical Research Communications. 2004; 320(4):1175–1180. http://dx.doi.org/10.1016/j.bbrc.2004.06.072

13. Kong YW, Jing G, Yan ZG, Li CZ, Gong NP, Zhu FJ, et al. Cloning and characterization of Prisilkin-39, a novel matrix protein serving a dual role in the prismatic layer formation from the oyster Pinctada fucata. Journal of Biological Chemistry. 2009; 284(16):10841–10854. doi: 10.1074/jbc.M808357200 19233851

14. Michio S, Emi M, Hirotaka I, Ooriaki O, Hidekazu T, Toshihiro K, et al. Characterization of Prismalin-14, a novel matrix protein from the prismatic layer of the Japanese pearl oyster (Pinctada fucata). Biochemical Journal. 2004; 382(1):205–213. http://dx.doi.org/10.1042/BJ20040319

15. Zhang C, Xie LP, Huang J, Liu XL, Zhang RQ. A novel matrix protein family participating in the prismatic layer framework formation of pearl oyster, Pinctada fucata. Biochemical & Biophysical Research Communications. 2006; 344(3):735–740. http://dx.doi.org/10.1016/j.bbrc.2006.03.179

16. Takagi R, Miyashita T, Prismin: A New Matrix Protein Family in the Japanese Pearl Oyster (Pinctada fucata) Involved in Prismatic Layer Formation. Zoological Science. 2010; 27(5):416–426. doi: 10.2108/zsj.27.416 20443689

17. Yano M, Nagai K, Morimoto K, Miyamoto H. Shematrin: a family of glycine-rich structural proteins in the shell of the pearl oyster Pinctada fucata. Comparative Biochemistry & Physiology Part B. 2006; 144(2):254–262. http://dx.doi.org/10.1016/j.cbpb.2006.03.004

18. Yan Y, Yang D, Yang X, Liu C, Xie J, Zheng G, et al. A Novel Matrix Protein, PfY2, Functions as a Crucial Macromolecule during Shell Formation. Scientific Reports. 2017; 7(1):6021. doi: 10.1038/s41598-017-06375-w 28729529

19. Kong J.J, Liu C, Yang D, Yan Y, Chen Y, Liu YJ, et al. A Novel Basic Matrix Protein of Pinctada fucata, PNU9, functions as Inhibitor during Crystallization of Aragonite. CrystEngComm. 2019; 21(8):1250–1261. http://dx.doi.org/10.1039/C8CE02194E

20. Du XD, Fan GY, Jiao Y, Zhang H, Guo XM, Huang RL, et al. The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization. Gigascience. 2017; 6(8):1–12. http://dx.doi.org/10.1093/gigascience/gix059

21. Chang E P, Evans, J S. Pif97, a von Willebrand and Peritrophin biomineralization protein, organizes mineral nanoparticles and creates intracrystalline nanochambers. Biochemistry, 2015; 54(34), 5348–5355. doi: 10.1021/acs.biochem.5b00842 26258941

22. Bahn SY, Jo BH, Hwang BH, Choi YS, Cha HJ. Role of Pif97 in Nacre Biomineralization: In Vitro Characterization of Recombinant Pif97 as a Framework Protein for the Association of Organic–Inorganic Layers in Nacre. Crystal Growth & Design. 2015; 15(8):3666–3673. http://dx.doi.org/10.1021/acs.cgd.5b00275

23. Jain G, Pendola M, Huang YC, Gebauer D, Koutsoumpeli E, Johnson S, et al. Selective Synergism Created by Interactive Nacre Framework-Associated Proteins Possessing EGF and vWA Motifs: Implications for Mollusk Shell Formation. Biochemistry. 2018; 57(18):2657–2666. doi: 10.1021/acs.biochem.8b00119 29620882

24. Wang XT, Song XR, Wang T, Zhu QH, Miao GY, Chen YX, et al. Evolution and functional analysis of the Pif97 gene of the Pacific oyster Crassostrea gigas. Current Zoology. 2013; 59(1):109–115. http://dx.doi.org/10.1093/czoolo/59.1.109

25. Lian JB, Stein GS, Van WAJ, Stein JL, Hassan MQ, Gaur T, et al. MicroRNA control of bone formation and homeostasis. Nature Reviews Endocrinology. 2012; 8(4):212–227. doi: 10.1038/nrendo.2011.234 22290358

26. Jiao Y, Zheng Z, Du XD, Wang QH, Huang RL, Deng YW, et al. Identification and characterization of microRNAs in pearl oyster Pinctada martensii by Solexa deep sequencing. Marine Biotechnology. 2014; 16(1):54–62. doi: 10.1007/s10126-013-9528-x 23877619

27. Tian RR, Zhe Z, Huang RL, Jiao Y, Du XD. miR-29a Participated in nacre formation and immune response by targeting Y2R in Pinctada martensii. International Journal of Molecular Sciences. 2015; 16(12):29436–29445. doi: 10.3390/ijms161226182 26690410

28. Zheng Z, Du XD, Xiong XW, Jiao Y, Deng Y, Wang Q, et al. PmRunt regulated by Pm-miR-183 participates in nacre formation possibly through promoting the expression of collagen VI-like and Nacrein in pearl oyster Pinctada martensii. Plos One. 2017; 12(6):e0178561. doi: 10.1371/journal.pone.0178561 28570710

29. Jiao Y, Zheng Z, Tian RR, Du XD, Wang QH, Huang RL. MicroRNA, Pm-miR-2305, Participates in Nacre Formation by Targeting Pearlin in Pearl Oyster Pinctada martensii. International Journal of Molecular Sciences. 2015; 16(9):21442–21453. doi: 10.3390/ijms160921442 26370972

30. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS biology. 2004; 2(11):e363. doi: 10.1371/journal.pbio.0020363 15502875

31. Krüger J, Rehmsmeier M, RNAhybrid: microRNA target prediction easy, fast and flexible. Nucleic Acids Research. 2006; 34(web server):451–454. doi: 10.1093/nar/gkj455

32. Zhang ZN, Xie YT, Xu XR, Pan HH, Tang RK. Transformation of amorphous calcium carbonate into aragonite. Journal of Crystal Growth. 2012; 343(1):62–67. http://dx.doi.org/10.1016/j.jcrysgro.2012.01.025

33. Fabio N, Eyal S, Eugenia K, Rousseau M, Bourrat X, Lopez E, et al. Forming nacreous layer of the shells of the bivalves Atrina rigida and Pinctada margaritifera: an environmental-and cryo-scanning electron microscopy study. Journal of Structural Biology. 2008; 162(2):290–300. doi: 10.1016/j.jsb.2008.01.008 18328730

34. Suzuki M, Sakuda S, Nagasawa H. Identification of chitin in the prismatic layer of the shell and a chitin synthase gene from the Japanese pearl oyster, Pinctada fucata. Bioscience, biotechnology, and biochemistry. 2007; 71(7):1735–1744. doi: 10.1271/bbb.70140 17617722

35. Li HM, Wang DQ, Deng ZH, Huang GJ, Fan SG, Zhou DZ, et al. Molecular characterization and expression analysis of chitinase from the pearl oyster Pinctada fucata. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology. 2017; 203:141–148. http://dx.doi.org/10.1016/j.cbpb.2016.10.007

36. Suzuki M, Iwashima A, Kimura M, Kogure T, Nagasawa H. The Molecular Evolution of the Pif Family Proteins in Various Species of mollusks. Marine Biotechnology. 2013; 15(2):145–158. doi: 10.1007/s10126-012-9471-2 22847736

37. Whittaker CA, Hynes RO. Distribution and evolution of von Willebrand/integrin a domains: Widely dispersed adhesion and elsewhere. Molecular Biology of the Cell. 2002; 13(10):3369–3387. doi: 10.1091/mbc.E02-05-0259 12388743

38. Benjamin M, Caroline J, Alexandre T, Zanella CI, Belliaard C, Piguemal D, et al. Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell. Proc Natl Acad Sci USA. 2012; 109(51):20986–20991. doi: 10.1073/pnas.1210552109 23213212

39. Liao Z, Bao LF, Fan MH, Gao P, Wang XX, Qin Cl, et al. In-depth proteomic analysis of nacre, prism, and myostracum of Mytilus shell. Journal of Proteomics. 2015; 122:26–40. doi: 10.1016/j.jprot.2015.03.027 25857279

40. Zhang GF, Fang XD, Guo XM, Li L, Luo RB, Xu F, et al. The oyster genome reveals stress adaptation and complexity of shell formation. Nature. 2012; 490(7418):49–54. doi: 10.1038/nature11413 22992520

41. Marie B, Jackson DJ, Ramos-Silva P, Zanella-Cleon I, Guichard N, Marin F. The shell-forming proteome of Lottia gigantea reveals both deep conservations and lineage-specific novelties. Febs Journal. 2013; 280(1):214–232. doi: 10.1111/febs.12062 23145877

42. Kong JJ, Liu C, Wang TP, Yang D, Yan Y, Chen Y, et al. Cloning, characterization and functional analysis of an Alveoline-like protein in the shell of Pinctada fucata. Scientific Reports. 2018; 8(1):12258. doi: 10.1038/s41598-018-29743-6 30115934

43. Huang J.L, Liu Y.J, Jiang T.F, et al. Direct control of shell regeneration by the mantle tissue in the pearl oyster Pinctada fucata via accelerating CaCO3 nucleation. bioRxiv. 2019., published online by bioRxiv 9 march 2019. http://dx.doi.org/10.1101/572024

44. Li H, Zhang B, Huang GJ, Liu BS, Fan SG, Zhang DL, et al. Differential Gene Expression during Larval Metamorphic Development in the Pearl Oyster, Pinctada fucata, based on Transcriptome Analysis. International Journal of Genomics. 2016; 2016:1–15. http://dx.doi.org/10.1155/2016/2895303

45. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature. 2005; 433(7027):769–773. doi: 10.1038/nature03315 15685193

46. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Research. 2008; 19(1):92–105. doi: 10.1101/gr.082701.108 18955434


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