Hemocyte phagosomal proteome is dynamically shaped by cytoskeleton remodeling and interorganellar communication with endoplasmic reticulum during phagocytosis in a marine invertebrate, Crassostrea gigas

Mao, Fan1,2,3,4; Mu, Huawei5; Wong, Nai-Kei6; Liu, Kunna1,2,3,4; Song, Jingchen7; Qiu, Jianwen8,9; Lin, Yue1,2,3,4; Zhang, Xiangyu1,2,3,4; Xu, Duo1,2,3,4; Xiang, Zhiming1,2,3,4; Li, Jun1,2,3,4; Zhang, Yang1,2,3,4; Yu, Ziniu1,2,3,4

2020-04-20

10.1038/s41598-020-63676-3

Scientific Reports   影响因子和分区

2045-2322

Phagosomes are task-force organelles of innate immune systems, and evolutionary diversity and continuity abound in the protein machinery executing this coordinately regulated process. In order to clarify molecular mechanisms underlying phagocytosis, we studied phagocyte response to beads and Vibrio species, using hemocytes of the Pacific oysters (Crassostrea gigas) as a marine invertebrate model. Phagosomes from different stages of phagocytosis were isolated by density-gradient centrifugation, and more than 400 phagosome-associated proteins were subsequently identified via high-throughput quantitative proteomics. In modeling key networks of phagosomal proteins, our results support the essential roles of several processes driving phagosome formation and maturation, including cytoskeleton remodeling and signal transduction by Rab proteins. Several endoplasmic reticulum (ER)-associated proteins were identified, while live cell imaging confirms an apparent intimate interaction between the ER and phagosomes. In further quantitative proteomic analysis, the signal transducers CgRhoGDI and CgPI4K were implicated. Through experimental validation, CgRhoGDI was shown to negatively regulate actin cytoskeleton remodeling in the formation of oyster phagosomes, while CgPI4K signaling drives phagosome maturation and bacterial killing. Our current work illustrates the diversity and dynamic interplay of phagosomal proteins, providing a framework for better understanding host-microbe interactions during phagosome activities in under-examined invertebrate species.

SCI

英语

其他

National Key R&D Program of China[2018YFC1406505] ; National Science Foundation of China[31572640][31902404][31572661] ; Science and Technology Program of Guangzhou, China[201804020073] ; Guangdong Special Support Program of Youth Scientific and Technological Innovation[2015TQ01N139] ; Program of the Pearl River Young Talents of Science and Technology in Guangzhou of China[201806010003] ; Institution of South China Sea Ecology and Environmental Engineering, Chinese Academy of Sciences[ISEE2018PY01][ISEE2018PY03][ISEE2018ZD01] ; Science and Technology Planning Project of Guangdong Province, China[2017B030314052][201707010177]

Science & Technology - Other Topics

Multidisciplinary Sciences

WOS:000537155000007

NATURE PUBLISHING GROUP

Web of Science

1.Chinese Acad Sci, South China Sea Inst Oceanol, CAS Key Lab Trop Marine Bioresources & Ecol, Guangzhou, Peoples R China
2.Chinese Acad Sci, South China Sea Inst Oceanol, Guangdong Prov Key Lab Appl Marine Biol, Guangzhou, Peoples R China
3.Chinese Acad Sci, Innovat Acad South China Sea Ecol & Environm Engn, CAS, ISEE, Guangzhou, Peoples R China
4.Southern Marine Sci & Engn Guangdong Lab Guangzho, Guangzhou, Peoples R China
5.Univ Sci & Technol China, Sch Life Sci, Hefei, Peoples R China
6.Southern Univ Sci & Technol, Shenzhen Peoples Hosp 3, Dept Infect Dis, Hosp Affiliated 2, Shenzhen, Peoples R China
7.South China Agr Univ, Coll Oceanol, Guangzhou, Peoples R China
8.Hong Kong Baptist Univ, Croucher Inst Environm Sci, Hong Kong, Peoples R China
9.Hong Kong Baptist Univ, Dept Biol, Hong Kong, Peoples R China

Mao, Fan,Mu, Huawei,Wong, Nai-Kei,et al. Hemocyte phagosomal proteome is dynamically shaped by cytoskeleton remodeling and interorganellar communication with endoplasmic reticulum during phagocytosis in a marine invertebrate, Crassostrea gigas[J]. Scientific Reports,2020,10(1).

Mao, Fan.,Mu, Huawei.,Wong, Nai-Kei.,Liu, Kunna.,Song, Jingchen.,...&Yu, Ziniu.(2020).Hemocyte phagosomal proteome is dynamically shaped by cytoskeleton remodeling and interorganellar communication with endoplasmic reticulum during phagocytosis in a marine invertebrate, Crassostrea gigas.Scientific Reports,10(1).

Mao, Fan,et al."Hemocyte phagosomal proteome is dynamically shaped by cytoskeleton remodeling and interorganellar communication with endoplasmic reticulum during phagocytosis in a marine invertebrate, Crassostrea gigas".Scientific Reports 10.1(2020).