Research advances on the effects of helminth infection on bile acid metabolism

doi:10.12140/j.issn.1000-7423.2024.05.013

Abstract

Abstract:

Parasitic helminths are widely distributed globally and have a significant impact on animal husbandry and public health. Helminth infection can affect metabolic and immune processes in the host. The latest research shows that helminth infection significantly alters host bile acid metabolism, which in turn directly or indirectly affects the host’s health and immune homeostasis. This article reviews the advances in research on the effects of nematodes, tapeworms, and flukes on host bile acid metabolism to provide new research ideas for the diagnosis, treatment, and prevention of related diseases.

Key words: Helminth infection, Bile acids, Metabolism

CLC Number:

R532

ZHANG Ying, WANG Yugui, SHI Zhiqi, WANG Shuai. Research advances on the effects of helminth infection on bile acid metabolism[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2024, 42(5): 648-652.

References 47

[1]	Papaiakovou M, Littlewood DTJ, Doyle SR, et al. Worms and bugs of the gut: the search for diagnostic signatures using barcoding, and metagenomics-metabolomics[J]. Parasit Vectors, 2022, 15(1): 118.
[2]	Peachey LE, Jenkins TP, Cantacessi C. This gut ain’t big enough for both of us. Or is it? Helminth-microbiota interactions in veterinary species[J]. Trends Parasitol, 2017, 33(8): 619-632.
[3]	Llinás-Caballero K, Caraballo L. Helminths and bacterial microbiota: the interactions of two of humans’ “old friends”[J]. Int J Mol Sci, 2022, 23(21): 13358.
[4]	Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity[J]. Mucosal Immunol, 2018, 11(4): 1039-1046.
[5]	Zaiss MM, Rapin A, Lebon L, et al. The intestinal microbiota contributes to the ability of helminths to modulate allergic inflammation[J]. Immunity, 2015, 43(5): 998-1010.
[6]	Reed EK, Smith KA. Using our understanding of interactions between helminth metabolism and host immunity to target worm survival[J]. Trends Parasitol, 2024, 40(7): 549-561.
[7]	Chen ML, Takeda K, Sundrud MS. Emerging roles of bile acids in mucosal immunity and inflammation[J]. Mucosal Immunol, 2019, 12(4): 851-861.
[8]	Li JN, Dawson PA. Animal models to study bile acid metabolism[J]. Biochim Biophys Acta BBA Mol Basis Dis, 2019, 1865(5): 895-911.
[9]	Wahlstr?m A, Sayin SI, Marschall HU, et al. Intestinal crosstalk between bile acids and microbiota and its impact on host metabolism[J]. Cell Metab, 2016, 24(1): 41-50.
[10]	Johnston CJ, Robertson E, Harcus Y, et al. Cultivation of Heligmosomoides polygyrus: an immunomodulatory nematode parasite and its secreted products[J]. J Vis Exp, 2015(98): e52412.
[11]	Monte MJ, Marin JJG, Antelo A, et al. Bile acids: chemistry, physiology, and pathophysiology[J]. World J Gastroenterol, 2009, 15(7): 804-816.
[12]	Lane JM, Brosschot TP, Gatti DM, et al. Chronic small intestinal helminth infection perturbs bile acid homeostasis and disrupts bile acid signaling in the murine small intestine[J]. Front Parasitol, 2023, 2: 1214136.
[13]	Magnaval JF, Glickman LT, Dorchies P, et al. Highlights of human toxocariasis[J]. Korean J Parasitol, 2001, 39(1): 1-11.
[14]	Smith H, Holland C, Taylor M, et al. How common is human toxocariasis? Towards standardizing our knowledge[J]. Trends Parasitol, 2009, 25(4): 182-188.
[15]	Zheng WB, Zou Y, Elsheikha HM, et al. Serum metabolomic alterations in Beagle dogs experimentally infected with Toxocara canis[J]. Parasit Vectors, 2019, 12(1): 447.
[16]	Pittman J, Shepherd G, Thacker B,et al. Trichuris suis in fini- shing pigs: case report and review[J]. J Swine Health Prod, 2010, 18(6): 306-313.
[17]	Dawson HD, Chen C, Li RW, et al. Molecular and metabolomic changes in the proximal colon of pigs infected with Trichuris suis[J]. Sci Rep, 2020, 10(1): 12853.
[18]	Zhang YX, Zhang BG. Research progress on the interaction between human helminth infection and intestinal flora[J]. J Trop Dis Parasitol, 2022, 20(5): 295-299. (in Chinese)
	(张艺馨, 张本光. 人体蠕虫感染对肠道菌群影响的研究进展[J]. 热带病与寄生虫学, 2022, 20(5): 295-299.)
[19]	Sun XM, Hao CY, Wu AQ,et al. Trichinella spiralis-induced immunomodulation signatures on gut microbiota and metabolic pathways in mice[J]. PLoS Pathog, 2024, 20(1): e1011893.
[20]	Kalia N, Hardcastle J, Keating C, et al. Intestinal secretory and absorptive function in Trichinella spiralis mouse model of postinfective gut dysfunction: role of bile acids[J]. Gut, 2008, 57(1): 41-49.
[21]	Smout MJ, Laha T, Mulvenna J, et al. A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells[J]. PLoS Pathog, 2009, 5(10): e1000611.
[22]	Sithithaworn P, Andrews RH, Nguyen VD, et al. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin[J]. Parasitol Int, 2012, 61(1): 10-16.
[23]	Sripa B, Pairojkul C. Cholangiocarcinoma: lessons from Thailand[J]. Curr Opin Gastroenterol, 2008, 24(3): 349-356.
[24]	Vale N, Gouveia MJ, Botelho M, et al. Carcinogenic liver fluke Opisthorchis viverrini oxysterols detected by LC-MS/MS survey of soluble fraction parasite extract[J]. Parasitol Int, 2013, 62(6): 535-542.
[25]	Mairiang E, Mairiang P. Clinical manifestation of opisthorchiasis and treatment[J]. Acta Trop, 2003, 88(3): 221-227.
[26]	Choi D, Lim JH, Lee KT, et al. Cholangiocarcinoma and Clonorchis sinensis infection: a case-control study in Korea[J]. J Hepatol, 2006, 44(6): 1066-1073.
[27]	Xu M, Jiang ZH, Huang W, et al. Altered gut microbiota composition in subjects infected with Clonorchis sinensis[J]. Front Microbiol, 2018, 9: 2292.
[28]	Qian MB, Utzinger J, Keiser J, et al. Clonorchiasis[J]. Lancet, 2016, 387(10020): 800-810.
[29]	Huang YL, Huang DN, Geng YJ, et al. An integrated control strategy takes Clonorchis sinensis under control in an endemic area in South China[J]. Vector Borne Zoonotic Dis, 2017, 17(12): 791-798.
[30]	Cho PY, Kim TI, Whang SM, et al. Gene expression profile of Clonorchis sinensis metacercariae[J]. Parasitol Res, 2008, 102(2): 277-282.
[31]	Matern H, Boermans H, Lottspeich F, et al. Molecular cloning and expression of human bile acid beta-glucosidase[J]. J Biol Chem, 2001, 276(41): 37929-37933.
[32]	Zhang XL, Han S, Jiang X, et al. Comparative analysis of bile metabolic profile in patients with biliary obstruction complicated by Clonorchis sinensis infection[J]. Front Cell Infect Microbiol, 2023, 13: 1254016.
[33]	Ling ZX, Zhu ML, Yan XM, et al. Structural and functional dysbiosis of fecal microbiota in Chinese patients with Alzheimer’s disease[J]. Front Cell Dev Biol, 2021, 8: 634069.
[34]	Litvak Y, Byndloss MX, Tsolis RM, et al. Dysbiotic Proteobacteria expansion: a microbial signature of epithelial dysfunction[J]. Curr Opin Microbiol, 2017, 39: 1-6.
[35]	Chen R, Li X, Ding J, et al. Profiles of biliary microbiota in biliary obstruction patients with Clonorchis sinensis infection[J]. Front Cell Infect Microbiol, 2023, 13: 1281745.
[36]	Pereira TA, Syn WK, Machado MV, et al. Schistosome-induced cholangiocyte proliferation and osteopontin secretion correlate with fibrosis and portal hypertension in human and murine schistosomiasis mansoni[J]. Clin Sci, 2015, 129(10): 875-883.
[37]	Loebermann M, Sombetzki M, Langner C, et al. Imbalance of pro- and antifibrogenic genes and bile duct injury in murine Schistosoma mansoni infection-induced liver fibrosis[J]. Trop Med Int Health, 2009, 14(11): 1418-1425.
[38]	Rath EA, Walkey M. Fatty acid and cholesterol synthesis in mice infected with the tapeworm Hymenolepis microstoma[J]. Parasitology, 1987, 95(Pt 1): 79-92.
[39]	Surgan MH, Roberts LS. Adsorption of bile salts by the cestodes, Hymenolepis diminuta and H. Microstoma[J]. J Parasitol, 1976, 62(1): 78-86.
[40]	Corbin I, Blackburn BJ, Wolowiec T, et al. Metabolic profile of the liver of mice infected with cysticerci of Taenia crassiceps[J]. Parasitol Res, 1996, 82(3): 273-275.
[41]	Gottstein B, Hemphill A. Echinococcus multilocularis: the parasite-host interplay[J]. Exp Parasitol, 2008, 119(4): 447-452.
[42]	Craig P. Echinococcus multilocularis[J]. Curr Opin Infect Dis, 2003, 16(5): 437-444.
[43]	Hemphill A, Stadelmann B, Rufener R, et al. Treatment of echinococcosis: albendazole and mebendazole: what else?[J]. Parasite, 2014, 21: 70.
[44]	Graeter T, Ehing F, Oeztuerk S, et al. Hepatobiliary complications of alveolar echinococcosis: a long-term follow-up study[J]. World J Gastroenterol, 2015, 21(16): 4925-4932.
[45]	Gómez C, Jebbawi F, Weingartner M, et al. Impact on bile acid concentrations by alveolar echinococcosis and treatment with albendazole in mice[J]. Metabolites, 2021, 11(7): 442.
[46]	Briggs MH. Metabolism of steroid hormones by schistosomes[J]. Biochim Biophys Acta, 1972, 280(3): 481-485.
[47]	Sukhdeo MV, Croll NA. The location of parasites within their hosts: bile and the site selection behaviour of nematospiroides Dubius[J]. Int J Parasitol, 1981, 11(2): 157-162.