Hepatic caecum of amphioxus and origin of vertebrate liver

Shicui Zhang; Zhaokang Shen; Haifeng Li

doi:10.1007/s13131-023-2259-6

Volume 42 Issue 11

Nov. 2023

Turn off MathJax

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2023 > 42(11): 1-8

Shicui Zhang, Zhaokang Shen, Haifeng Li. Hepatic caecum of amphioxus and origin of vertebrate liver[J]. Acta Oceanologica Sinica, 2023, 42(11): 1-8. doi: 10.1007/s13131-023-2259-6

Citation:

Shicui Zhang, Zhaokang Shen, Haifeng Li. Hepatic caecum of amphioxus and origin of vertebrate liver[J]. Acta Oceanologica Sinica, 2023, 42(11): 1-8. doi: 10.1007/s13131-023-2259-6

Shicui Zhang, Zhaokang Shen, Haifeng Li. Hepatic caecum of amphioxus and origin of vertebrate liver[J]. Acta Oceanologica Sinica, 2023, 42(11): 1-8. doi: 10.1007/s13131-023-2259-6

Citation:

Shicui Zhang, Zhaokang Shen, Haifeng Li. Hepatic caecum of amphioxus and origin of vertebrate liver[J]. Acta Oceanologica Sinica, 2023, 42(11): 1-8. doi: 10.1007/s13131-023-2259-6

PDF( 2344 KB)

Hepatic caecum of amphioxus and origin of vertebrate liver

doi: 10.1007/s13131-023-2259-6

1.
College of Life and Geographic Sciences, Key Laboratory of Biological Resources and Ecology of Pamirs Plateau in Xinjiang Uygur Autonomous Region, Kashi University, Kashi 844000, China
2.
Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China

Funds: The National Natural Science Foundation of China under contract No. 32270434.

More Information

Corresponding author: E-mail: sczhang@ouc.edu.cn
Received Date: 2023-05-23
Accepted Date: 2023-07-26

Available Online: 2023-12-11

Publish Date: 2023-11-01

Abstract

Abstract

Liver is characteristic of all vertebrates. As a critical hub for many physiological processes including metabolism, innate immunity, protein synthesis and detoxification, its evolutionary origin was largely underappreciated in history, and only received due attention in recent decades. It has been suggested by morphological, ultrastructural and immunohistochemical studies that the hepatic caecum of amphioxus is homologous to the liver of vertebrate species. Molecular biology studies demonstrated that amphioxus hepatic caecum expresses plenty of vertebrate liver-specific genes. Our functional studies revealed significant similarities between amphioxus hepatic caecum and vertebrate liver. We also found that the functions of hepatic caecum are subjected to the regulation of pituitary hormones just as the liver does. These provide solid evidences supporting the notion that the hepatic caecum is the homologue of liver, which may represent the first stage in chordate evolution, laying a foundation for the subsequent formation of the liver as we know it in vertebrates. Further studies on the specification and morphogenesis of hepatic caecum in amphioxus will shed more lights on the origin and evolution of vertebrate liver.
- protochordate,
- amphioxus,
- hepatic caecum,
- liver,
- evolution

FullText(HTML)

References(85)

References

Abdel-Misih S R Z, Bloomston M. 2010. Liver anatomy. Surgical Clinics of North America, 90(4): 643–653. doi: 10.1016/j.suc.2010.04.017

Abildgaard U. 1979. A review of anti-thrombin III. In: Collen D, Wilman B, Verstraete M, eds. The Physiological Inhibitors of Blood Coagulation and Fibrinolysis. Amsterdam: Elsevier/North-Holland Biochemical, 19–29

Ahearn G A, Mandal P K, Mandal A. 2004. Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review. Journal of Comparative Physiology B, 174(6): 439–452

Arrese E L, Soulages J L. 2010. Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology, 55: 207–225. doi: 10.1146/annurev-ento-112408-085356

Arvy L. 1969. Les enzymes chez les crustacés. Annales de Biologie, 8: 505–580

Barrington E J W. 1937. The digestive system of Amphioxus ( Branchiostoma) lanceolatus. Philosophical Transactions of the Royal Society B: Biological Sciences, 228(553): 269–312

Beklemishev V N. 1969. Principles of Comparative Anatomy of Invertebrates. 3rd ed. Edinburgh: Oliver & Boyd

Bhattacharya H, Zhang Shicui, Xiao Qin. 2008. Comparison of histopathological alterations due to sublethal CCl₄ on rosy barb ( Puntius conchonius) and amphioxus ( Branchiostoma belcheri) with implications of liver ontogeny. Toxicology Mechanisms and Methods, 18(8): 627–633. doi: 10.1080/15376510701623540

Cereghini S. 1996. Liver-enriched transcription factors and hepatocyte differentiation. FASEB Journal, 10(2): 267–282. doi: 10.1096/fasebj.10.2.8641560

Chao Yeqing, Fan Chunxin, Liang Yujun, et al. 2012. A novel serpin with antithrombin-like activity in Branchiostoma japonicum: implications for the presence of a primitive coagulation system. PLoS One, 7(3): e32392. doi: 10.1371/journal.pone.0032392

Chapman R F. 1998. The Insects: Structure and Function. 4th ed. New York: Cambridge University Press

Collen D, Lijnen H R. 1991. Basic and clinical aspects of fibrinolysis and thrombolysis. Blood, 78(12): 3114–3124. doi: 10.1182/blood.V78.12.3114.3114

Cortes C, Ohtola J A, Saggu G, et al. 2013. Local release of properdin in the cellular microenvironment: role in pattern recognition and amplification of the alternative pathway of complement. Frontiers in Immunology, 3: 412

Danielsson Ȧ, Björk I. 1982. Mechanism of inactivation of trypsin by antithrombin. Biochemical Journal, 207(1): 21–28. doi: 10.1042/bj2070021

Danielsson A, Björk I. 1983. Properties of antithrombin-thrombin complex formed in the presence and in the absence of heparin. Biochemical Journal, 213(2): 345–353. doi: 10.1042/bj2130345

Delsuc F, Brinkmann H, Chourrout D, et al. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature, 439(7079): 965–968. doi: 10.1038/nature04336

Doolittle R F. 1990. The structure and evolution of vertebrate fibrinogen: a comparison of the lamprey and mammalian proteins. In: Liu C Y, Chien S, eds. Fibrinogen, Thrombosis, Coagulation, and Fibrinolysis. Boston: Springer, 25–37

Doolittle R F, Surgenor D M. 1962. Blood coagulation in fish. American Journal of Physiology-Legacy Content, 203(5): 964–970. doi: 10.1152/ajplegacy.1962.203.5.964

Eaton D L, Bammler T K. 1999. Concise review of the glutathione S-transferases and their significance to toxicology. Toxicological Sciences, 49(2): 156–164. doi: 10.1093/toxsci/49.2.156

Endo Y, Nonaka M, Saiga H, et al. 2003. Origin of mannose-binding lectin-associated serine protease (MASP)-1 and MASP-3 involved in the lectin complement pathway traced back to the invertebrate, amphioxus. The Journal of Immunology, 170(9): 4701–4707. doi: 10.4049/jimmunol.170.9.4701

Fan Chunxin, Zhang Shicui, Li Lei, et al. 2008. Fibrinogen-related protein from amphioxus Branchiostoma belcheri is a multivalent pattern recognition receptor with a bacteriolytic activity. Molecular Immunology, 45(12): 3338–3346. doi: 10.1016/j.molimm.2008.04.019

Fan Chunxin, Zhang Shicui, Liu Zhenhui, et al. 2007. Identification and expression of a novel class of glutathione- S-transferase from amphioxus Branchiostoma belcheri with implications to the origin of vertebrate liver. International Journal of Biochemistry & Cell Biology, 39(2): 450–461

Frost C L, Naudé R J, Muramoto K. 2002. Ostrich antithrombin III: kinetics and mechanism of inhibition of ostrich thrombin. The International Journal of Biochemistry & Cell Biology, 34(9): 1164–1171

Gao Bin, Jeong W I, Tian Zhigang. 2008. Liver: an organ with predominant innate immunity. Hepatology, 47(2): 729–736

Gao Zhan, Li Mengyang, Ma Jie, et al. 2014. An amphioxus gC1q protein binds human IgG and initiates the classical pathway: implications for a C1q-mediated complement system in the basal chordate. European Journal of Immunology, 44(12): 3680–3695. doi: 10.1002/eji.201444734

Gao Zhan, Li Mengyang, Wu Jie, et al. 2013. Interplay between invertebrate C3a with vertebrate macrophages: functional characterization of immune activities of amphioxus C3a. Fish & Shellfish Immunology, 35(4): 1249–1259

Gao Zhan, Ma Zengyu, Qu Baozhen, et al. 2017. Identification and characterization of properdin in amphioxus: implications for a functional alternative complement pathway in the basal chordate. Fish & Shellfish Immunology, 65: 1–8

Gillott C. 1995. Entomology. 2nd ed. New York: Plenum Press

Goddard C K, Martin A W. 1966. Carbohydrate metabolism. In: Wilbur K M, Yonge C M, eds. Physiology of Mollusca, Vol II. New York: Academic, 275–308

Guo Bin, Zhang Shicui, Wang Shaohui, et al. 2009. Expression, mitogenic activity and regulation by growth hormone of growth hormone/insulin-like growth factor in Branchiostoma belcheri. Cell and Tissue Research, 338(1): 67–77. doi: 10.1007/s00441-009-0824-8

He Yanan, Tang Bo, Zhang Shicui, et al. 2008. Molecular and immunochemical demonstration of a novel member of Bf/C2 homolog in amphioxus Branchiostoma belcheri: implications for involvement of hepatic cecum in acute phase response. Fish & Shellfish Immunology, 24(6): 768–778

Huang Huiqing, Huang Shengfeng, Yu Yingcai, et al. 2011. Functional characterization of a ficolin-mediated complement pathway in amphioxus. Journal of Biological Chemistry, 286(42): 36739–36748. doi: 10.1074/jbc.M111.245944

Huang Shengfeng, Yuan Shaochun, Guo Lei, et al. 2008. Genomic analysis of the immune gene repertoire of amphioxus reveals extraordinary innate complexity and diversity. Genome Research, 18(7): 1112–1126. doi: 10.1101/gr.069674.107

Jastrow M. 1907. The liver in antiquity and the beginnings of anatomy. Transactions of the College of Physicians of Philadelphia, 29: 117–139

Jing Xiaoli, Zhang Shicui. 2011. An ancient molecule with novel function: alanine aminotransferase as a lipopolysaccharide binding protein with bacteriocidal activity. Developmental & Comparative Immunology, 35(1): 94–104

Keeley L L. 1985. Physiology and biochemistry of the fat body. In: Kerkut G A, Gilbert L I, eds. Integument, Respiration and Circulation. Oxford: Pergamon Press, 211–248

Leung L Y, Woo N Y S. 2010. Effects of growth hormone, insulin-like growth factor I, triiodothyronine, thyroxine, and cortisol on gene expression of carbohydrate metabolic enzymes in sea bream hepatocytes. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 157(3): 272–282

Li Mengyang, Gao Zhan, Ji Dongrui, et al. 2014a. Functional characterization of GH-like homolog in amphioxus reveals an ancient origin of GH/GH receptor system. Endocrinology, 155(12): 4818–4830. doi: 10.1210/en.2014-1377

Li Mengyang, Gao Zhan, Wang Yu, et al. 2014b. Identification, expression and bioactivity of hexokinase in amphioxus: insights into evolution of vertebrate hexokinase genes. Gene, 535(2): 318–326. doi: 10.1016/j.gene.2013.10.068

Li Mengyang, Jiang Chengyan, Zhang Yu, et al. 2017. Activities of amphioxus GH-like protein in osmoregulation: insight into origin of vertebrate GH family. International Journal of Endocrinology, 2017: 9538685

Li Zhimin, Zhang Shicui, Wang Changfa, et al. 2008. Complement-mediated killing of Vibrio species by the humoral fluids of amphioxus Branchiostoma belcheri: implications for a dual role of O-antigens in the resistance to bactericidal activity. Fish & Shellfish Immunology, 24(2): 215–222

Liang Yujun, Zhang Shicui. 2006. Demonstration of plasminogen-like protein in amphioxus with implications for the origin of vertebrate liver. Acta Zoology, 87(2): 141–145. doi: 10.1111/j.1463-6395.2006.00228.x

Liang Yujun, Zhang Shicui, Lun Limin, et al. 2006. Presence and localization of antithrombin and its regulation after acute lipopolysaccharide exposure in amphioxus, with implications for the origin of vertebrate liver. Cell and Tissue Research, 323(3): 537–541. doi: 10.1007/s00441-005-0088-x

Liu Mingying, Zhang Shicui. 2009. A kringle-containing protease with plasminogen-like activity in the basal chordate Branchiostoma belcheri. Bioscience Reports, 29(6): 385–395. doi: 10.1042/BSR20080173

Liu Mingying, Zhang Shicui. 2011. Amphioxus IGF-like peptide induces mouse muscle cell development via binding to IGF receptors and activating MAPK and PI3K/Akt signaling pathways. Molecular and Cellular Endocrinology, 343(1–2): 45–54. doi: 10.1016/j.mce.2011.06.004

Liu Jia, Zhang Shicui, Li Lei. 2009. A transferrin-like homolog in amphioxus Branchiostoma belcheri: identification, expression and functional characterization. Molecular Immunology, 46(15): 3117–3124. doi: 10.1016/j.molimm.2009.06.001

Longstaff C, Thelwell C. 2005. Understanding the enzymology of fibrinolysis and improving thrombolytic therapy. FEBS Letters, 579(15): 3303–3309. doi: 10.1016/j.febslet.2005.03.058

Lun Limin, Zhang Shicui, Liang Yujun. 2006. Alanine aminotransferase in amphioxus: presence, localization and up-regulation after acute lipopolysaccharide exposure. Korean Society for Biochemistry and Molecular Biology, 39(5): 511–515

Mansour-Bek J J. 1954. The digestive enzymes in invertebrata and protochordata. Digestion, 75–367

Mizuta T, Kubokawa K. 2007. Presence of sex steroids and cytochrome P450 genes in amphioxus. Endocrinology, 148(8): 3554–3565. doi: 10.1210/en.2007-0109

Ober E A, Lemaigre F P. 2018. Development of the liver: insights into organ and tissue morphogenesis. Journal of Hepatology, 68(5): 1049–1062. doi: 10.1016/j.jhep.2018.01.005

Olson S T, Björk I. 1994. Regulation of thrombin activity by antithrombin and heparin. Seminars in Thrombosis and Hemostasis, 20(4): 373–409. doi: 10.1055/s-2007-1001928

Orito W, Ohhira F, Ogasawara M. 2015. Gene expression profiles of FABP genes in protochordates, Ciona intestinalis and B ranchiostoma belcheri. Cell and Tissue Research, 362(2): 331–345. doi: 10.1007/s00441-015-2198-4

Putnam N H, Butts T, Ferrier D E K, et al. 2008. The amphioxus genome and the evolution of the chordate karyotype. Nature, 453(7198): 1064–1071. doi: 10.1038/nature06967

Rähr H. 1979. The circulatory system of amphioxus ( Branchiostoma lanceolatum (Pallas))—A light-microscopic investigation based on intravascular injection technique. Acta Zoologica, 60(1): 1–18. doi: 10.1111/j.1463-6395.1979.tb00594.x

Rijken D C, Sakharov D V. 2001. Basic principles in thrombolysis: regulatory role of plasminogen. Thrombosis Research, 103: S41–S49. doi: 10.1016/S0049-3848(01)00296-1

Riva M A, Riva E, Spicci M, et al. 2011. “The city of Hepar”: Rituals, gastronomy, and politics at the origins of the modern names for the liver. Journal of Hepatology, 55(5): 1132–1136. doi: 10.1016/j.jhep.2011.05.011

Roma G C, Bueno O C, Mathias M I C. 2005. Comparative study of the fat body in some genera of the Attini tribe (Hymenoptera: Formicidae). Sociobiology, 45(2): 449–462

Rőszer T. 2014. The invertebrate midintestinal gland (“hepatopancreas”) is an evolutionary forerunner in the integration of immunity and metabolism. Cell and Tissue Research, 358(3): 685–695. doi: 10.1007/s00441-014-1985-7

Sarma J V, Ward P A. 2011. The complement system. Cell and Tissue Research, 343(1): 227–235. doi: 10.1007/s00441-010-1034-0

Snodgrass R E. 1935. Principles of Insect Morphology. New York: McGraw-Hill

Subbotin V M. 2018. Privileged portal metastasis of hepatocellular carcinoma in light of co-evolution of a visceral portal system and the liver in the chordate lineage: a search for therapeutic targets. Drug Discovery Today, 23(3): 548–564. doi: 10.1016/j.drudis.2018.01.020

Subbotin V M. 2019. A hypothesis on paradoxical privileged portal vein metastasis of hepatocellular carcinoma. Can organ evolution shed light on patterns of human pathology, and vice versa?. Medical Hypotheses, 126: 109–128

Sumner A T. 1965. The cytology and histochemistry of the digestive gland cells of Helix. The Quarterly Journal of Microscopic Science, s3-106(74): 173–192

Suzuki M M, Satoh N, Nonaka M. 2002. C6-like and C3-like molecules from the cephalochordate, amphioxus, suggest a cytolytic complement system in invertebrates. Journal of Molecular Evolution, 54(5): 671–679. doi: 10.1007/s00239-001-0068-z

Tian Jianxiao, Zhang Shicui, Liu Zhenhui, et al. 2007. Characterization and tissue-specific expression of phosphatidylcholine transfer protein gene from amphioxus Branchiostoma belcheri. Cell and Tissue Research, 330(1): 53–61. doi: 10.1007/s00441-007-0465-8

Trefts E, Gannon M, Wasserman D H. 2017. The liver. Current Biology, 27(21): R1147–R1151. doi: 10.1016/j.cub.2017.09.019

van Weel P B. 1961. The comparative physiology of digestion in molluscs. American Zoologist, 1(2): 245–252. doi: 10.1093/icb/1.2.245

van Weel P B. 1970. Digestion in crustacea. In: Florkin M, Scheer B T, eds. Chemical Zoology, Vol. 5. New York: Academic Press, 97–115

van Weel P B. 1974. Hepatopancpreas?. Comparative Biochemistry and Physiology Part A: Physiology, 47(1): 1–9

von Siebold C. 1848. Lehrbuch der vergleichenden Anatomie der Wirbellosen Thiere. Erster Theil. In: von Siebold C T, Stannius H, eds. Lehrbuch der Vergleichenden Anatomie. Berlin: Verlag von Veit & Comp

von Müller J. 1844. Über den Bau und Die Lebenserscheinungen des Branchiostoma lubricum Costa, Amphioxus Lanceolatus Yarrell: Gelesen in der Königlichen Akademie der Wissenschaften zu Berlin am 6. December 1841. Berlin: Gedruckt in der Druckerei der Königlichen Akademie der Wissenschaften, 79–116

Vonk H J. 1960. Digestion and metabolism. In: Waterman T H, ed. Metabolism and Growth. New York: Academic Press, 291–316

Wang Peng, Liu Shousheng, Yang Qingyun, et al. 2018. Functional characterization of thyrostimulin in amphioxus suggests an ancestral origin of the TH signaling pathway. Endocrinology, 159(10): 3536–3548. doi: 10.1210/en.2018-00550

Wang Yu, Wang Hui, Li Mengyang, et al. 2015. Identification, expression and regulation of amphioxus G6Pase gene with an emphasis on origin of liver. General and Comparative Endocrinology, 214: 9–16. doi: 10.1016/j.ygcen.2014.12.021

Wang Yuan, Zhang Shicui. 2011. Identification and expression of liver-specific genes after LPS challenge in amphioxus: the hepatic cecum as liver-like organ and “pre-hepatic” acute phase response. Functional & Integrative Genomics, 11(1): 111–118

Wang Yongjun, Zhang Yuequn, Zhang Shicui, et al. 2008a. Tissue- and stage-specific expression of a fatty acid binding protein-like gene from amphioxus Branchiostoma belcheri. Acta Biochimica Polonica, 55(1): 27–34. doi: 10.18388/abp.2008_3197

Wang Shaohui, Zhang Shicui, Zhao Bosheng, et al. 2009. Up-regulation of C/EBP by thyroid hormones: a case demonstrating the vertebrate-like thyroid hormone signaling pathway in amphioxus. Molecular and Cellular Endocrinology, 313(1–2): 57–63. doi: 10.1016/j.mce.2009.08.024

Welsch U. 1975. The fine structure of the pharynx, cyrtopodocytes and digestive caecum of amphioxus (Branchiostoma lanceolatum). Symposium on Zoological Society of London, 36: 17–41

Wang Yongjun, Zhao Bosheng, Ding Fei, et al. 2008b. Gut-specific expression of cathepsin L and B in amphioxus Branchiostoma belcheri tsingtauense larvae. European Journal of Cell Biology, 87(3): 185–193. doi: 10.1016/j.ejcb.2007.10.002

Zaret K S. 2000. Liver specification and early morphogenesis. Mechanisms of Development, 92(1): 83–88. doi: 10.1016/S0925-4773(99)00326-3

Zaret K S. 2016. From endoderm to liver bud: paradigms of cell type specification and tissue morphogenesis. Current Topics in Developmental Biology, 117: 647–669

Zhang Shicui. 2020. Evolutionary Biology of Amphioxus: Tracing Origin of Vertebrate (in Chinese). Beijing: Scientific Press, 102–114

Zhang Shicui, Ji Xiaohan. 2022. Hatschek’s pit and origin of pituitary gland. Acta Oceanologica Sinica, 41(12): 1–6

Zhang Shicui, Liang Yujun, Ji Guangdong, et al. 2009. Protochordate amphioxus is an emerging model organism for comparative immunology. Progress in Natural Science, 19(8): 923–929. doi: 10.1016/j.pnsc.2008.07.025

Relative Articles

Supplements(0)

Cited By

Proportional views