Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumber<italic style="font-style: italic">Apostichopus japonicus</italic>post-evisceration

Jinlin JI; Zhenhui WANG; Wei ZHU; Qiang LI; Yinan WANG

doi:10.1007/s00343-021-1198-3

Your Location：

Home >

Browse articles >

Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration

Biology | Updated：2023-05-19

- Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration
- Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration
- 海洋湖沼学报（英文） 2022年40卷第5期页码：2028-2041
- Affiliations：
  
  1.College of Marine and Biology Engineering, Yancheng Institute of Technology, Yancheng 224051, China
  2.Dalian Ocean University, Dalian 116023, China
- Author bio：
  
  WANG Yinan,wangyinan@dlou.edu.cn
- Funds：
  
  the National Natural Science Foundation of China(31872544);the National Natural Science Foundation of China(42076112);the Scientific Research Foundation of Yancheng Institute of Technology(XJ201725);the Scientific Research Foundation of Yancheng Institute of Technology(XJ201726);© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2022Electronic supplementary materialSupplementary material (Supplementary Tables S1–S5) is available in the online version of this article athttps://doi.org/10.1007/s00343-021-1198-3.
- DOI：10.1007/s00343-021-1198-3
  中图分类号：
- 收稿：2021-06-28，
  
  录用：2021-9-23，
  
  网络首发：2021-12-04，
  
  纸质出版：2022-09
- Accepted：
Scan QR Code
Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration[J]. 海洋湖沼学报（英文）, 2022,40(5):2028-2041.

Jinlin JI, Zhenhui WANG, Wei ZHU, et al. Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration[J]. Journal of Oceanology and Limnology, 2022, 40(5): 2028-2041.
Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration[J]. 海洋湖沼学报（英文）, 2022,40(5):2028-2041. DOI： 10.1007/s00343-021-1198-3.

Jinlin JI, Zhenhui WANG, Wei ZHU, et al. Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration[J]. Journal of Oceanology and Limnology, 2022, 40(5): 2028-2041. DOI： 10.1007/s00343-021-1198-3.

摘要

Abstract

The Polian vesicle is the main accessory structure in the water vascular system of sea cucumbers. It can function to hold water vascular fluid under slight pressure and act as a hematopoiesis

excretory

and inflammatory response organ. Being the only organ to remain after evisceration

the Polian vesicle may function in the survival and regeneration of sea cucumber. We performed Tandem Mass Tag (TMT)-based proteomics to identify how proteins in the Polian vesicle of

Apostichopus japonicus

respond to evisceration. Among the 8 453 proteins identified from vesicle samples before evisceration (PV0h) and at 6-h post-evisceration (PV6h) and 3-d post-evisceration (PV3d)

we detected 222 differentially abundant proteins (DAPs). Most of the annotated DAPs were associated with cell growth and proliferation

immune response and wound healing

substance transport and metabolism

cytoskeleton/cilia/flagella

extracellular matrix

energy production and conversion

protein synthesis and modification

and signal recognition and transduction. Compared with PV0h

fewer DAPs were identified at PV6h

and more DAPs were found at PV3d

and these DAPs were widely distributed among multiple biological processes. Our results indicate that a wide range of biological processes was induced in Polian vesicles in response to evisceration. In particular

Polian vesicles may play important roles in the restoration of coelomocytes

immune defense

and wound healing in sea cucumber. We propose that the Polian vesicle may be involved in visceral regeneration through nutrition and energy supply and by promoting dedifferentiation and migration. Together

these results provided new insights into the function of the Polian vesicle in

japonicus

post-evisceration.

关键词

Keywords

references

Baccetti B, Rosati F. 1968. The fine structure of the Polian vesicles of Holothurians. Zeitschrift für Zellforschung und Mikroskopische Anatomie , 90( 1): 148-160, https://doi.org/10.1007/BF00496708.

Chen Y, Zhao J, Li D Z et al. 2018. TRIM56 suppresses multiple myeloma progression by activating TLR3/TRIF signaling. Yonsei Medical Journal , 59 (1): 43-50, https://doi.org/10.3349/ymj.2018.59.1.43.

Cui N, Hu M, Khalil R A. 2017. Biochemical and biological attributes of matrix metalloproteinases. Progress in Molecular Biology and Translational Science , 147 : 1-73, https://doi.org/10.1016/bs.pmbts.2017.02.005.

D'Ancona G, Rizzuto L, Canicattí C. 1989. Engagement of Polian vesicles during Holothuria Polii response to erythrocyte injection. Journal of Invertebrate Pathology , 54 (3): 300-305, https://doi.org/10.1016/0022-2011(89)90113-4.

Dolmatov I Y, Ginanova T T. 2009. Post-autotomy regeneration of respiratory trees in the holothurian Apostichopus japonicus (Holothuroidea, Aspidochirotida). Cell and Tissue Research , 336( 1): 41-58, https://doi.org/10.1007/s00441-009-0761-6.

Dolmatov I Y, Nizhnichenko V A, Dolmatova L S. 2021. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in echinoderms: structure and possible functions. Cells , 10( 9): 2331, https://doi.org/10.3390/cells10092331.

Dolmatov I Y. 2021. Molecular aspects of regeneration mechanisms in holothurians. Genes , 12 (2): 250, https://doi.org/10.3390/genes12020250.

Ge S F, Xiong Y, Wu X P et al. 2017. Role of growth factor receptor-bound 2 in CCl 4 -induced hepatic fibrosis. Biomedicine & Pharmacotherapy , 92 : 942-951, https://doi.org/10.1016/j.biopha.2017.05.142.

Grigorian M, Hartenstein V. 2013. Hematopoiesis and hematopoietic organs in arthropods. Development Genes and Evolution , 223 (1-2): 103-115, https://doi.org/10.1007/s00427-012-0428-2.

Gupta A, Leslie N R. 2016. Controlling PTEN (phosphatase and tensin homolog) stability: a dominant role for lysine66. Journal of Biological Chemistry , 291( 35): 18465-18473, https://doi.org/10.1074/jbc.M116.727750.

Houben T, Harder S, Schlüter H et al. 2019. Different forms of TFF3 in the human saliva: heterodimerization with IgG Fc Binding Protein (FCGBP). International Journal of Molecular Science , 20 (20): 5000, https://doi.org/10.3390/ijms20205000.

Huo D, Sun L N, Zhang L B et al. 2019. Global-warming-caused changes of temperature and oxygen alter the proteomic profile of sea cucumber Apostichopus japonicus . Journal of Proteomics , 193 : 27-43, https://doi.org/10.1016/j.jprot.2018.12.020.

Jiang J W, Zhao Z L, Pan Y J et al. 2020. Proteomics reveals the gender differences in humoral immunity and physiological characteristics associated with reproduction in the sea cucumber Apostichopus japonicus . Journal of Proteomics , 217 : 103687, https://doi.org/10.1016/j.jprot.2020.103687.

Jin Y X, Zhen Y, Haugsten E M et al. 2011. The driver of malignancy in KG-1a leukemic cells, FGFR1OP2 - FGFR1 , encodes an HSP90 addicted oncoprotein. Cellular Signalling , 23 (11): 1758-1766, https://doi.org/10.1016/j.cellsig.2011.06.010.

Jones P, Binns D, Chang H Y et al. 2014. InterProScan 5: genome-scale protein function classification. Bioinformatics . 30 (9): 1236-1240, https://doi.org/10.1093/bioinformatics/btu031.

Karamanos N K, Theocharis A D, Piperigkou Z et al. 2021. A guide to the composition and functions of the extracellular matrix. FEBS Journal , 288 (24): 6850-6912, https://doi.org/10.1111/febs.15776.

Krogh A, Larsson B, Von Heijne G et al. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology , 305 (3): 567-580, https://doi.org/10.1006/jmbi.2000.4315.

Lee H Y, Gao X F, Barrasa M I et al. 2015. PPAR-α and glucocorticoid receptor synergize to promote erythroid progenitor self-renewal. Nature , 522 (7557): 474-477, https://doi.org/10.1038/nature14326.

Li Q, Ren Y, Liang C L et al. 2018a. Regeneration of coelomocytes after evisceration in the sea cucumber, Apostichopus japonicus . Fish & Shellfish Immunology , 76 : 266-271, https://doi.org/10.1016/j.fsi.2018.03.013.

Li Q, Ren Y, Luan L L et al. 2019. Localization and characterization of hematopoietic tissues in adult sea cucumber, Apostichopus japonicus . Fish & Shellfish Immunology , 84 : 1-7, https://doi.org/10.1016/j.fsi.2018.09.058.

Li Y, Jin D X, Xie W X et al. 2018b. PPAR-γ and Wnt regulate the differentiation of MSCs into adipocytes and osteoblasts respectively. Current Stem Cell Research & Therapy , 13 (3): 185-192, https://doi.org/10.2174/1574888X12666171012141908.

Liao Y L. 1997. Fauna Sinica, Echinodermata, Holothurioidea. Science Press, Beijing. 334p. (in Chinese)

Liu M, Guan Z L, Shen Q et al. 2016. Ulk4 is essential for ciliogenesis and CSF flow. Journal of Neuroscience , 36 (29): 7589-7600, https://doi.org/10.1523/JNEUROSCI.0621-16.2016.

Lv Z M, Guo M, Li C H et al. 2019. Divergent proteomics response of Apostichopus japonicus suffering from skin ulceration syndrome and pathogen infection. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics , 30 : 196-205, https://doi.org/10.1016/j.cbd.2019.03.003.

Ma J, Chen T, Wu S F et al. 2019. iProX: an integrated proteome resource. Nucleic Acids Research , 47 (D1): D1211-D1217, https://doi.org/10.1093/nar/gky869.

Magadum A, Engel F B. 2018. PPARβ/δ: linking metabolism to regeneration. International Journal of Molecular Sciences , 19 (7): 2013, https://doi.org/10.3390/ijms19072013.

Masunaga H, Sugimoto Y, Magi S et al. 2017. Robustness analysis of the detailed kinetic model of an ErbB signaling network by using dynamic sensitivity. PLoS One , 12 (5): e0178250, https://doi.org/10.1371/journal.pone.0178250.

Miao T, Wan Z X, Sun L N et al. 2017. Extracellular matrix remodeling and matrix metalloproteinases (ajMMP-2 like and ajMMP-16 like) characterization during intestine regeneration of sea cucumber Apostichopus japonicus . Comparative Biochemistry and Physiology Part B : Biochemistry and Molecular Biology , 212 : 12-23, https://doi.org/10.1016/j.cbpb.2017.06.011.

Oh J E, Kook J K, Min B M. 2005. βig-h3 induces keratinocyte differentiation via modulation of involucrin and transglutaminase expression through the integrin α3β1 and the phosphatidylinositol 3-kinase/Akt signaling pathway. Journal of Biological Chemistry , 280 (22): 21629-21637, https://doi.org/10.1074/jbc.M412293200.

Ohira T, Kojima H, Kuroda Y et al. 2019. PITX1 protein interacts with ZCCHC10 to regulate hTERT mRNA transcription. PLoS One , 14 (8): e0217605, https://doi.org/10.1371/journal.pone.0217605.

Pan L Y, Tan Y T, Wang B et al. 2020. Caspase recruitment domain containing protein 9 suppresses non-small cell lung cancer proliferation and invasion via inhibiting MAPK/p38 pathway. Cancer Research and Treatment , 52 (3): 867-885, https://doi.org/10.4143/crt.2019.606.

Petersen T N, Brunak S, Von Heijne G et al. 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods , 8 (10): 785-786, https://doi.org/10.1038/nmeth.1701.

Platnich J M, Muruve D A. 2019. NOD-like receptors and inflammasomes: a review of their canonical and non-canonical signaling pathways. Archives of Biochemistry and Biophysics , 670 : 4-14, https://doi.org/10.1016/j.abb.2019.02.008.

Shi W B, Zhang J L, Wang Y N et al. 2020. Transcriptome analysis of sea cucumber ( Apostichopus japonicus ) Polian vesicles in response to evisceration. Fish & Shellfish Immunology , 97 : 108-113, https://doi.org/10.1016/j.fsi.2019.12.016.

Smith A C. 1978. A proposed phylogenetic relationship between sea cucumber Polian vesicles and the vertebrate lymphoreticular system. Journal of Invertebrate Pathology , 31 (3): 353-357, https://doi.org/10.1016/0022-2011(78)90228-8.

Smith E F. 2007. Hydin seek: finding a function in ciliarymotility. Journal of Cell Biology , 176 (4): 403-404, https://doi.org/10.1083/jcb.200701113.

Sun L N, Sun J C, Xu Q Z et al.2017a. Metabolic responses to intestine regeneration in sea cucumbers Apostichopus japonicus . Comparative Biochemistry and Physiology Part D : Genomics and Proteomics , 22 : 32-38, https://doi.org/10.1016/j.cbd.2017.02.003.

Sun L N, Xu D X, Xu Q Z et al. 2017b. iTRAQ reveals proteomic changes during intestine regeneration in the sea cucumber Apostichopus japonicus . Comparative Biochemistry and Physiology Part D: Genomics and Proteomics , 22 : 39-49, https://doi.org/10.1016/j.cbd.2017.02.004.

Sun L N, Yang H S, Chen M Y et al. 2013. RNA-seq reveals dynamic changes of gene expression in key stages of intestine regeneration in the sea cucumber Apostichopus japonicas . PLoS One , 8 (8): e69441, https://doi.org/10.1371/journal.pone.0069441.

Tan Y K, Li X, Duan J J. 2008. Energy metabolism and biochemical composition of Apostichopus japonicus during the regeneration of viscera. Journal of Fishery Sciences of China , 15 (4): 683-688, https://doi.org/10.3321/j.issn:1005-8737.2008.04.021.(inChinesewithEnglishabstract)

Varma V R, Varma S, An Y et al. 2017. Alpha-2 macroglobulin in Alzheimer's disease: a marker of neuronal injury through the RCAN1 pathway. Molecular Psychiatry , 22( 1): 13-23, https://doi.org/10.1038/mp.2016.206.

Walter S A, Cutler Jr R E, Martinez R et al. 2003. Stk10, a new member of the polo-like kinase kinase family highly expressed in hematopoietic tissue. Journal of Biological Chemistry , 278 (20): 18221-18228, https://doi.org/10.1074/jbc.M212556200.

Wang T M, Sun L N, Chen M Y. 2015. Chapter 11 - Aestivation and regeneration. Developments in Aquaculture and Fisheries Science , 39 : 177-209, https://doi.org/10.1016/B978-0-12-799953-1.00011-8.

Wirthgen E, Höflich C, Spitschak M et al. 2016. Quantitative Western ligand blotting reveals common patterns and differential features of IGFBP-fingerprints in domestic ruminant breeds and species. Growth Hormone & IGF Research , 26 : 42-49, https://doi.org/10.1016/j.ghir.2015.11.001.

Xu D X, Sun L N, Liu S L et al. 2016. Understanding the heat shock response in the sea cucumber Apostichopus japonicus , using iTRAQ-based proteomics. International Journal of Molecular Sciences , 17 (2): 150, https://doi.org/10.3390/ijms17020150.

Yamashita M, Nitta E, Suda T. 2015. Maintenance of hematopoietic stem cell integrity and regulation of leukemogenesis by p53 and its coactivator Aspp1. The Japanese Journal of Clinical Hematology , 56 (12): 2426-2433, https://doi.org/10.11406/rinketsu.56.2426.

Zang Y Q, Tian X L, Dong S L et al. 2012. Growth, metabolism and immune responses to evisceration and the regeneration of viscera in sea cucumber, Apostichopus japonicus . Aquaculture , 358-359 : 50-60, https://doi.org/10.1016/j.aquaculture.2012.06.007.

Zhang P, Li C H, Li Y et al. 2014. Proteomic identification of differentially expressed proteins in sea cucumber Apostichopus japonicus coelomocytes after Vibrio splendidus infection. Developmental & Comparative Immunology , 44 (2): 370-377, https://doi.org/10.1016/j.dci.2014.01.013.

Zhang R, Song C. 2014. Loss of CSMD1 or 2 may contribute to the poor prognosis of colorectal cancer patients. Tumor Biology , 35 (5): 4419-4423, https://doi.org/10.1007/s13277-013-1581-6.

Zhang X J, Sun L N, Yuan J B et al. 2017. The sea cucumber genome provides insights into morphological evolution and visceral regeneration. PLoS Biology , 15 (10): e2003790, https://doi.org/10.1371/journal.pbio.2003790.

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Metabolomic and proteomic responses ofPhaeodactylum tricornutumto hypoxia

Bacterial community composition in gut content and ambient sediment of two tropical wild sea cucumbers (Holothuria atra and H. leucospilota)

Triterpenoid saponin biosynthesis genes and their expression patterns during the development of sea cucumber Apostichopus japonicus

Positive selection analysis reveals the deep-sea adaptation of a hadal sea cucumber (Paelopatides sp.) to the Mariana Trench

Effects of different flow velocities on behavior and TRPA1 expression in the sea cucumber Apostichopus japonicas

Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration

Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumberApostichopus japonicuspost-evisceration

DOI：10.1007/s00343-021-1198-3

摘要

Abstract

关键词

Keywords

references