甲壳动物造血机制研究进展
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摘要
血细胞是甲壳动物的免疫细胞,可通过吞噬、包囊、结节、黑化,以及分泌免疫活性分子等方式杀死和清除入侵的病原体。活跃的造血机能对更新和补充损耗的循环血细胞、维持一个稳定有效的免疫系统是至关重要的。相对脊椎动物而言,人们对包括甲壳动物在内的无脊椎动物的造血机制了解比较有限。本文总结了近年来在甲壳动物造血机制方面的研究进展,主要介绍了血细胞的类型和功能、造血组织的结构和细胞组成、血细胞的分化途径、造血的调控机制,以及相关的细胞模型和体外实验技术等。并在此基础上分析了已有研究存在的缺陷,提出了需要进一步探究的问题。
Hemocytes are the major immune cells of crustaceans. They remove invading pathogens by phagocytosis,encapsulation,nodulation and releasing of immune reactive molecules. Hematopoiesis is important for renewal and replenishment of circulating hemocytes and maintenance of a functional immune system. Compared with the hematopoiesis of vertebrates,which has been intensively studied,the knowledge of the invertebrate hematopoiesis is limited. In this review,we summarize the current knowledge of crustacean hemocyte lineages and their function,the structure and cell content of hematopoietic tissue,the differentiation procedure of hemocytes,and the regulation of hematopoiesis. We also introduce the in vitro methods developed for the study of crustacean hematopoiesis. Finally,we raise the questions needed for the future study.
Hemocytes are the major immune cells of crustaceans. They remove invading pathogens by phagocytosis,encapsulation,nodulation and releasing of immune reactive molecules. Hematopoiesis is important for renewal and replenishment of circulating hemocytes and maintenance of a functional immune system. Compared with the hematopoiesis of vertebrates,which has been intensively studied,the knowledge of the invertebrate hematopoiesis is limited. In this review,we summarize the current knowledge of crustacean hemocyte lineages and their function,the structure and cell content of hematopoietic tissue,the differentiation procedure of hemocytes,and the regulation of hematopoiesis. We also introduce the in vitro methods developed for the study of crustacean hematopoiesis. Finally,we raise the questions needed for the future study.
引文
[1]CERENIUS L,JIRAVANICHPAISAL P,LIU H P,et al.Crustacean immunity[J].Advances in Experimental Medicine and Biology,2010,708:239-259．
[2]LEE S Y,SODERHALL K.Early events in crustacean innate immunity[J].Fish&Shellfish Immunology,2002,12(5):421-437．
[3]SODERHALL I.Crustacean hematopoiesis[J].Developmental&Comparative Immunology,2016,58:129-141．
[4]MARTIN G G,GRAVES B L.Fine structure and classification of shrimp hemocytes[J].Journal of Morphology,1985,185(3):339-348．
[5]LI F,CHANG X,XU L,et al.Different roles of crayfish hemocytes in the uptake of foreign particles[J].Fish&Shellfish Immunology,2018,77:112-119．
[6]LV S,XU J,ZHAO J,et al.Classification and phagocytosis of circulating haemocytes in Chinese mitten crab(Eriocheir sinensis)and the effect of extrinsic stimulation on circulating haemocytes in vivo[J].Fish&Shellfish Immunology,2014,39(2):415-422．
[7]JIRAVANICHPAISAL P,LEE B L,SODERHALL K.Cell-mediated immunity in arthropods:hematopoiesis,coagulation,melanization and opsonization[J].Immunobiology,2006,211(4):213-236．
[8]SODERHALL K,CERENIUS L.Role of the prophenoloxidase-activating system in invertebrate immunity[J].Current Opinion in Immunology,1998,10(1):23-28．
[9]FREDRICK W S,RAVICHANDRAN S.Hemolymph proteins in marine crustaceans[J].Asian Pacific Journal of Tropical Biomedicine,2012,2(6):496-502．
[10]SRICHAROEN S,KIM J J,TUNKIJJANUKIJ S,et al.Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish[J].Developmental&Comparative Immunology,2005,29(12):1 017-1 031．
[11]WU C,SODERHALL I,KIM Y A,et al.Hemocyte-lineage marker proteins in a crustacean,the freshwater crayfish,Pacifastacus leniusculus[J].Proteomics,2008,8(20):4 226-4 235．
[12]SODERHALL I,JUNKUNLO K.A comparative global proteomic analysis of the hematopoietic lineages in the crustacean Pacifastacus leniusculus[J].Developmental&Comparative Immunology,2019,92:170-178．
[13]KOIWAI K,ALENTON R R,SHIOMI R,et al.Two hemocyte sub-populations of kuruma shrimp Marsupenaeus japonicus[J].Molecular Immunology,2017,85:1-8．
[14]CHAGA O,LIGNELL M,SODERHALL K.The haematopoietic cells of the fresh water crayfish Pacifastacus leniusculus[J].Animal Biology,1995,4:59-70．
[15]LIN X,SODERHALL I.Crustacean hematopoiesis and the astakine cytokines[J].Blood,2011,117(24):6 417-6 424．
[16]LIN X,SODERHALL K,SODERHALL I.Transglutaminase activity in the hematopoietic tissue of a crustacean,Pacifastacus leniusculus,importance in hemocyte homeostasis[J].BMC Immunology,2008,9:58.DOI:10.1186/1471-2172-9-58．
[17]LI F,XU L,HUI X,et al.Directed differentiation of granular cells from crayfish hematopoietic tissue cells[J].Fish&Shellfish Immunology,2019,88:28-35．
[18]NOONIN C.Involvement of Serotonin in crayfish hematopoiesis[J].Developmental&Comparative Immunology,2018,86:189-195．
[19]SIRIKHARIN R,JUNKUNLO K,SODERHALL K,et al.Role of astakine1 in regulating transglutaminase activity[J].Developmental&Comparative Immunology,2017,76:77-82．
[20]VAN DE BRAAK C,BOTTERBLOM M,LIU W,et al.The role of the haematopoietic tissue in haemocyte production and maturation in the black tiger shrimp(Penaeus monodon)[J].Fish&Shellfish Immunology,2002,12(3):253-272．
[21]PRAPAVORARAT A,VATANAVICHARN T,SODERHALL K,et al.A novel viral responsive protein is involved in hemocyte homeostasis in the black tiger shrimp,Penaeus monodon[J].The Journal of Biological Chemistry,2010,285(28):21 467-21 477．
[22]HUANG C C,SRITUNYALUCKSANA K,SODERHALL K,et al.Molecular cloning and characterization of tiger shrimp(Penaeus monodon)transglutaminase[J].Developmental&Comparative Immunology,2004,28(4):279-294．
[23]CHANG Y T,LIN C Y,TSAI C Y,et al.The new face of the old molecules:crustin Pm4 and transglutaminase type I serving as RNPs down-regulate astakine-mediated hematopoiesis[J].PLo S ONE,2013,8(8):e72793．
[24]JIA Z,KAVUNGAL S,JIANG S,et al.The characterization of hematopoietic tissue in adult Chinese mitten crab Eriocheir sinensis[J].Developmental&Comparative Immunology,2016,60:12-22．
[25]GHIRETTI-MAGALDIC A,MILANESIG C,TOGNON G.Hemopoiesis in crustacea decapoda:origin and evolution of hemocytes and cyanocytes of Carcinus maenas[J].Cell Differentiation,1977,6(3):167-186．
[26]JIA Z,WANG M,WANG X,et al.The receptor for activated C kinase 1(RACK1)functions in hematopoiesis through JNKactivation in Chinese mitten crab Eriocheir sinensis[J].Fish&Shellfish Immunology,2016,57:252-261．
[27]MARTIN G G,HOSE J E,CHOI M,et al.Organization of hematopoietic tissue in the intermolt lobster,Homarus americanus[J].Journal of Morphology,1993,216(1):65-78．
[28]RUSAINI,OWENS L.Insight into the lymphoid organ of penaeid prawns:a review[J].Fish&Shellfish Immunology,2010,29(3):367-377．
[29]NOONIN C,LIN X,JIRAVANICHPAISAL P,et al.Invertebrate hematopoiesis:an anterior proliferation center as a link between the hematopoietic tissue and the brain[J].Stem Cells and Development,2012,21(17):3 173-3 186．
[30]HOSE J E,MARTIN G G,TIU S,et al.Patterns of hemocyte production and release throughout the molt cycle in the penaeid shrimp Sicyonia ingentis[J].The Biological Bulletin,1992,183:185-199．
[31]SODERHALL I,BANGYEEKHUN E,MAYO S,et al.Hemocyte production and maturation in an invertebrate animal;proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus[J].Developmental&Comparative Immunology,2003,27(8):661-672．
[32]HAMMOND J A,SMITH V J.Lipopolysaccharide induces DNA-synthesis in a sub-population of hemocytes from the swimming crab,Liocarcinus depurator[J].Developmental&Comparative Immunology,2002,26(3):227-236．
[33]SODERHALL I,KIM Y A,JIRAVANICHPAISAL P,et al.An ancient role for a prokineticin domain in invertebrate hematopoiesis[J].The Journal of Immunology,2005,174(10):6 153-6 160．
[34]ROULSTON C,SMITH V J.Isolation and in vitro characterisation of prohaemocytes from the spider crab,Hyas araneus(L.)[J].Developmental&Comparative Immunology,2011,35(5):537-544．
[35]LIN X,NOVOTNY M,SODERHALL K,et al.Ancient cytokines,the role of astakines as hematopoietic growth factors[J].The Journal of Biological Chemistry,2010,285(37):28 577-28 586．
[36]WATTHANASUROROT A,SODERHALL K,JIRAVANICHPAISAL P,et al.An ancient cytokine,astakine,mediates circadian regulation of invertebrate hematopoiesis[J].Cellular and Molecular Life Sciences,2011,68(2):315-323．
[37]LIN X,SODERHALL K,SODERHALL I.Invertebrate hematopoiesis:an astakine-dependent novel hematopoietic factor[J].The Journal of Immunology,2011,186(4):2 073-2 079．
[38]SAELEE N,NOONIN C,NUPAN B,et al．β-thymosins and hemocyte homeostasis in a crustacean[J].PLo S ONE,2013,8(4):e60974．
[39]LIN X,KIM Y A,LEE B L,et al.Identification and properties of a receptor for the invertebrate cytokine astakine,involved in hematopoiesis[J].Experimental Cell Research,2009,315(7):1 171-1 180．
[40]APITANYASAI K,NOONIN C,TASSANAKAJON A,et al.Characterization of a hemocyte homeostasis-associated-like protein(HHAP)in the freshwater crayfish Pacifastacus leniusculus[J].Fish&Shellfish Immunology,2016,58:429-435．
[41]AHMED M,FFRENCH-CONSTANT C.Extracellular matrix regulation of stem cell behavior[J].Current Stem Cell Reports,2016,2:197-206．
[42]JUNKUNLO K,SODERHALL K,SODERHALL I.Clotting protein-An extracellular matrix(ECM)protein involved in crustacean hematopoiesis[J].Developmental&Comparative Immunology,2018,78:132-140．
[43]JUNKUNLO K,SODERHALL K,NOONIN C,et al.PDGF/VEGF-related receptor affects transglutaminase activity to control cell migration during crustacean hematopoiesis[J].Stem Cells and Development,2017,26(20):1 449-1 459．
[44]MARKUS R,LAURINYECZ B,KURUCZ E,et al.Sessile hemocytes as a hematopoietic com-partment in Drosophila melanogaster[J].Proceedings of the National Academy of Sciences of the United States of America,2009,106(12):4 805-4 809．
[45]KOIWAI K,KONDO H,HIRONO I.The immune functions of sessile hemocytes in three organs of kuruma shrimp Marsupenaeus japonicus differ from those of circulating hemocytes[J].Fish&Shellfish Immunology,2018,78:109-113．
[46]ACCORSI A,OTTAVIANI E,MALAGOLI D.Effects of repeated hemolymph withdrawals on the hemocyte populations and hematopoiesis in Pomacea canaliculata[J].Fish&Shellfish Immunology,2014,38(1):56-64．
[47]SIGLE L T,HILLYER J F.Mosquito hemocytes associate with circulatory structures that support intracardiac retrograde hemolymph flow[J].Frontiers in Physiology,2018,9:1 187.DOI:10.3389/fphys.2018.01187．
[48]LIU H,SODERHALL I.Histone H2A as a transfection agent in crayfish hematopoietic tissue cells[J].Developmental&Comparative Immunology,2007,31(4):340-346．
[49]LIU H,JIRAVANICHPAISAL P,SODERHALL I,et al.Antilipopolysaccharide factor interferes with white spot syndrome virus replication in vitro and in vivo in the crayfish Pacifastacus leniusculus[J].Journal of Virology,2006,80(21):10 365-10 371．
[50]LIU H P,CHEN R Y,ZHANG Q X,et al.Differential gene expression profile from haematopoietic tissue stem cells of red claw crayfish,Cherax quadricarinatus,in response to WSSV infection[J].Developmental&Comparative Immunology,2011,35(7):716-724．
[51]HUANG J,LI F,WU J,et al.White spot syndrome virus enters crayfish hematopoietic tissue cells via clathrin-mediated endocytosis[J].Virology,2015,486:35-43．
[52]SHI H,RUAN L,SODERHALL I,et al.Transfection of crayfish hematopoietic tissue cells[J].Developmental&Comparative Immunology,2018,88:70-76.
[2]LEE S Y,SODERHALL K.Early events in crustacean innate immunity[J].Fish&Shellfish Immunology,2002,12(5):421-437．
[3]SODERHALL I.Crustacean hematopoiesis[J].Developmental&Comparative Immunology,2016,58:129-141．
[4]MARTIN G G,GRAVES B L.Fine structure and classification of shrimp hemocytes[J].Journal of Morphology,1985,185(3):339-348．
[5]LI F,CHANG X,XU L,et al.Different roles of crayfish hemocytes in the uptake of foreign particles[J].Fish&Shellfish Immunology,2018,77:112-119．
[6]LV S,XU J,ZHAO J,et al.Classification and phagocytosis of circulating haemocytes in Chinese mitten crab(Eriocheir sinensis)and the effect of extrinsic stimulation on circulating haemocytes in vivo[J].Fish&Shellfish Immunology,2014,39(2):415-422．
[7]JIRAVANICHPAISAL P,LEE B L,SODERHALL K.Cell-mediated immunity in arthropods:hematopoiesis,coagulation,melanization and opsonization[J].Immunobiology,2006,211(4):213-236．
[8]SODERHALL K,CERENIUS L.Role of the prophenoloxidase-activating system in invertebrate immunity[J].Current Opinion in Immunology,1998,10(1):23-28．
[9]FREDRICK W S,RAVICHANDRAN S.Hemolymph proteins in marine crustaceans[J].Asian Pacific Journal of Tropical Biomedicine,2012,2(6):496-502．
[10]SRICHAROEN S,KIM J J,TUNKIJJANUKIJ S,et al.Exocytosis and proteomic analysis of the vesicle content of granular hemocytes from a crayfish[J].Developmental&Comparative Immunology,2005,29(12):1 017-1 031．
[11]WU C,SODERHALL I,KIM Y A,et al.Hemocyte-lineage marker proteins in a crustacean,the freshwater crayfish,Pacifastacus leniusculus[J].Proteomics,2008,8(20):4 226-4 235．
[12]SODERHALL I,JUNKUNLO K.A comparative global proteomic analysis of the hematopoietic lineages in the crustacean Pacifastacus leniusculus[J].Developmental&Comparative Immunology,2019,92:170-178．
[13]KOIWAI K,ALENTON R R,SHIOMI R,et al.Two hemocyte sub-populations of kuruma shrimp Marsupenaeus japonicus[J].Molecular Immunology,2017,85:1-8．
[14]CHAGA O,LIGNELL M,SODERHALL K.The haematopoietic cells of the fresh water crayfish Pacifastacus leniusculus[J].Animal Biology,1995,4:59-70．
[15]LIN X,SODERHALL I.Crustacean hematopoiesis and the astakine cytokines[J].Blood,2011,117(24):6 417-6 424．
[16]LIN X,SODERHALL K,SODERHALL I.Transglutaminase activity in the hematopoietic tissue of a crustacean,Pacifastacus leniusculus,importance in hemocyte homeostasis[J].BMC Immunology,2008,9:58.DOI:10.1186/1471-2172-9-58．
[17]LI F,XU L,HUI X,et al.Directed differentiation of granular cells from crayfish hematopoietic tissue cells[J].Fish&Shellfish Immunology,2019,88:28-35．
[18]NOONIN C.Involvement of Serotonin in crayfish hematopoiesis[J].Developmental&Comparative Immunology,2018,86:189-195．
[19]SIRIKHARIN R,JUNKUNLO K,SODERHALL K,et al.Role of astakine1 in regulating transglutaminase activity[J].Developmental&Comparative Immunology,2017,76:77-82．
[20]VAN DE BRAAK C,BOTTERBLOM M,LIU W,et al.The role of the haematopoietic tissue in haemocyte production and maturation in the black tiger shrimp(Penaeus monodon)[J].Fish&Shellfish Immunology,2002,12(3):253-272．
[21]PRAPAVORARAT A,VATANAVICHARN T,SODERHALL K,et al.A novel viral responsive protein is involved in hemocyte homeostasis in the black tiger shrimp,Penaeus monodon[J].The Journal of Biological Chemistry,2010,285(28):21 467-21 477．
[22]HUANG C C,SRITUNYALUCKSANA K,SODERHALL K,et al.Molecular cloning and characterization of tiger shrimp(Penaeus monodon)transglutaminase[J].Developmental&Comparative Immunology,2004,28(4):279-294．
[23]CHANG Y T,LIN C Y,TSAI C Y,et al.The new face of the old molecules:crustin Pm4 and transglutaminase type I serving as RNPs down-regulate astakine-mediated hematopoiesis[J].PLo S ONE,2013,8(8):e72793．
[24]JIA Z,KAVUNGAL S,JIANG S,et al.The characterization of hematopoietic tissue in adult Chinese mitten crab Eriocheir sinensis[J].Developmental&Comparative Immunology,2016,60:12-22．
[25]GHIRETTI-MAGALDIC A,MILANESIG C,TOGNON G.Hemopoiesis in crustacea decapoda:origin and evolution of hemocytes and cyanocytes of Carcinus maenas[J].Cell Differentiation,1977,6(3):167-186．
[26]JIA Z,WANG M,WANG X,et al.The receptor for activated C kinase 1(RACK1)functions in hematopoiesis through JNKactivation in Chinese mitten crab Eriocheir sinensis[J].Fish&Shellfish Immunology,2016,57:252-261．
[27]MARTIN G G,HOSE J E,CHOI M,et al.Organization of hematopoietic tissue in the intermolt lobster,Homarus americanus[J].Journal of Morphology,1993,216(1):65-78．
[28]RUSAINI,OWENS L.Insight into the lymphoid organ of penaeid prawns:a review[J].Fish&Shellfish Immunology,2010,29(3):367-377．
[29]NOONIN C,LIN X,JIRAVANICHPAISAL P,et al.Invertebrate hematopoiesis:an anterior proliferation center as a link between the hematopoietic tissue and the brain[J].Stem Cells and Development,2012,21(17):3 173-3 186．
[30]HOSE J E,MARTIN G G,TIU S,et al.Patterns of hemocyte production and release throughout the molt cycle in the penaeid shrimp Sicyonia ingentis[J].The Biological Bulletin,1992,183:185-199．
[31]SODERHALL I,BANGYEEKHUN E,MAYO S,et al.Hemocyte production and maturation in an invertebrate animal;proliferation and gene expression in hematopoietic stem cells of Pacifastacus leniusculus[J].Developmental&Comparative Immunology,2003,27(8):661-672．
[32]HAMMOND J A,SMITH V J.Lipopolysaccharide induces DNA-synthesis in a sub-population of hemocytes from the swimming crab,Liocarcinus depurator[J].Developmental&Comparative Immunology,2002,26(3):227-236．
[33]SODERHALL I,KIM Y A,JIRAVANICHPAISAL P,et al.An ancient role for a prokineticin domain in invertebrate hematopoiesis[J].The Journal of Immunology,2005,174(10):6 153-6 160．
[34]ROULSTON C,SMITH V J.Isolation and in vitro characterisation of prohaemocytes from the spider crab,Hyas araneus(L.)[J].Developmental&Comparative Immunology,2011,35(5):537-544．
[35]LIN X,NOVOTNY M,SODERHALL K,et al.Ancient cytokines,the role of astakines as hematopoietic growth factors[J].The Journal of Biological Chemistry,2010,285(37):28 577-28 586．
[36]WATTHANASUROROT A,SODERHALL K,JIRAVANICHPAISAL P,et al.An ancient cytokine,astakine,mediates circadian regulation of invertebrate hematopoiesis[J].Cellular and Molecular Life Sciences,2011,68(2):315-323．
[37]LIN X,SODERHALL K,SODERHALL I.Invertebrate hematopoiesis:an astakine-dependent novel hematopoietic factor[J].The Journal of Immunology,2011,186(4):2 073-2 079．
[38]SAELEE N,NOONIN C,NUPAN B,et al．β-thymosins and hemocyte homeostasis in a crustacean[J].PLo S ONE,2013,8(4):e60974．
[39]LIN X,KIM Y A,LEE B L,et al.Identification and properties of a receptor for the invertebrate cytokine astakine,involved in hematopoiesis[J].Experimental Cell Research,2009,315(7):1 171-1 180．
[40]APITANYASAI K,NOONIN C,TASSANAKAJON A,et al.Characterization of a hemocyte homeostasis-associated-like protein(HHAP)in the freshwater crayfish Pacifastacus leniusculus[J].Fish&Shellfish Immunology,2016,58:429-435．
[41]AHMED M,FFRENCH-CONSTANT C.Extracellular matrix regulation of stem cell behavior[J].Current Stem Cell Reports,2016,2:197-206．
[42]JUNKUNLO K,SODERHALL K,SODERHALL I.Clotting protein-An extracellular matrix(ECM)protein involved in crustacean hematopoiesis[J].Developmental&Comparative Immunology,2018,78:132-140．
[43]JUNKUNLO K,SODERHALL K,NOONIN C,et al.PDGF/VEGF-related receptor affects transglutaminase activity to control cell migration during crustacean hematopoiesis[J].Stem Cells and Development,2017,26(20):1 449-1 459．
[44]MARKUS R,LAURINYECZ B,KURUCZ E,et al.Sessile hemocytes as a hematopoietic com-partment in Drosophila melanogaster[J].Proceedings of the National Academy of Sciences of the United States of America,2009,106(12):4 805-4 809．
[45]KOIWAI K,KONDO H,HIRONO I.The immune functions of sessile hemocytes in three organs of kuruma shrimp Marsupenaeus japonicus differ from those of circulating hemocytes[J].Fish&Shellfish Immunology,2018,78:109-113．
[46]ACCORSI A,OTTAVIANI E,MALAGOLI D.Effects of repeated hemolymph withdrawals on the hemocyte populations and hematopoiesis in Pomacea canaliculata[J].Fish&Shellfish Immunology,2014,38(1):56-64．
[47]SIGLE L T,HILLYER J F.Mosquito hemocytes associate with circulatory structures that support intracardiac retrograde hemolymph flow[J].Frontiers in Physiology,2018,9:1 187.DOI:10.3389/fphys.2018.01187．
[48]LIU H,SODERHALL I.Histone H2A as a transfection agent in crayfish hematopoietic tissue cells[J].Developmental&Comparative Immunology,2007,31(4):340-346．
[49]LIU H,JIRAVANICHPAISAL P,SODERHALL I,et al.Antilipopolysaccharide factor interferes with white spot syndrome virus replication in vitro and in vivo in the crayfish Pacifastacus leniusculus[J].Journal of Virology,2006,80(21):10 365-10 371．
[50]LIU H P,CHEN R Y,ZHANG Q X,et al.Differential gene expression profile from haematopoietic tissue stem cells of red claw crayfish,Cherax quadricarinatus,in response to WSSV infection[J].Developmental&Comparative Immunology,2011,35(7):716-724．
[51]HUANG J,LI F,WU J,et al.White spot syndrome virus enters crayfish hematopoietic tissue cells via clathrin-mediated endocytosis[J].Virology,2015,486:35-43．
[52]SHI H,RUAN L,SODERHALL I,et al.Transfection of crayfish hematopoietic tissue cells[J].Developmental&Comparative Immunology,2018,88:70-76.