Startseite Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
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Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia

  • Jamila S. Al Malki ORCID logo und Nahed Ahmed Hussien ORCID logo EMAIL logo
Veröffentlicht/Copyright: 27. November 2021
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Open Life Sciences
Aus der Zeitschrift Open Life Sciences Band 16 Heft 1

Abstract

Taeniids, consisting of two genera Echinococcus and Taenia, are obligatory tapeworms of mammals, and their pathogenicity was due to infection with larval stages. Hydatid (the larval stage of Echinococcus granulosus) and coenurus (the larval stage of Taenia multiceps) cysts are prevalent in domestic, wild ruminants, livestock, swine, and dogs, and accidentally they could also be found in humans. They lead to different clinical manifestations that cause economic loss in livestock and human morbidity. In Saudi Arabia, few studies were performed on hydatid and coenurus cyst genetic variations. The main goal of the present study was to identify E. granulosus and T. multiceps cyst isolates collected from slaughtered Harri sheep in Saudi Arabia by partial sequencing with PCR amplification of the cytochrome C oxidase 1 (COX1) gene. Molecular and phylogenetic evaluation based on COX1 sequences indicated that cyst isolates belong to E. granulosus and T. multiceps, respectively, successfully submitted in NCBI Genbank. Molecular characterization showed a low nucleotide diversity with two submitted isolates of coenurus with related isolates of Genbank. Conversely, E. granulosus isolates showed higher nucleotide diversity. The reported data could serve as a foundation for future molecular epidemiological and biological studies.

Keywords: Echinococcus granulosus ; Taenia multiceps ; coenurus; COX1; NAD1; Taif; Saudi Arabia

1 Introduction

Taeniid tapeworms belong to subclass Eucestoda, order Cyclophyllidea, and family Taeniidae, and they represent zoonotic parasites of mammals and livestock. Family Taeniidae consists of two genera, Echinococcus and Taenia, and they are mainly focused on for their socioeconomic impact by causing human morbidity and loss of livestock [1,2].

Echinococcus granulosus causes hydatidosis disease due to its larval stage infection. Hydatidosis (cystic echinococcosis) is widely distributed, and its prevalence varies according to climate and their contact with livestock [3]. Hydatid cysts have been reported in different livestock, including sheep, camels, cattle, and goats, with various incidence rates, resulting in significant economic losses [4,5,6]. Recently, it was recorded that the monetary burden of surgically treated human cystic echinococcosis increased that differs from one country to another [7]. In addition, it was reported that about 2.5% of humans infected with hydatidosis died after resorting to surgery [8]. There are three possibilities for cystic echinococcosis management: medical treatment with albendazole, percutaneous procedures, and surgery that depends on cyst stage, state, and organ location [9].

Coenurus represents the infective larval stage of Taenia multiceps; they are also widely distributed mainly in the tropical countries in Africa, Asia, and the Middle East [10]. T. multiceps are found as an obligate intestinal tapeworm of dogs, also commonly found in sheep and goats, as an intermediate host for the parasite, but the infection was extended to cattle and humans [11]. Mainly, coenurus cysts present in the brain in either acute or chronic form also could be frequently found in intramuscular and subcutaneous tissues [12,13,14]. Coenurosis leads to different clinical manifestations according to the location and extent of the coenuri. Coenurus cysts in the brain cause fever, muscle tremors, hemorrhagic retinal lesions, paralysis, ataxia, blindness, nystagmus, dysmetria, and scoliosis [15,16]. However, coenuri cysts in the subcutaneous and intramuscular tissues damage the functioning of normal organs and lead to muscular pain [11].

Due to the veterinary and medical significance of both E. granulosus and T. multiceps, there has been an intensive focus on their ecological, epidemiological, and taxonomic studies. Molecular characterization among many species found within Taeniidae, especially for the genus Echinococcus, has been well documented, but this was scarce with coenurus. However, there are very few documented studies on genetic variability regarding Taeniids in Saudi Arabia.

The present study aimed to (i) genetically characterize hydatid (larval stage of E. granulosus) and coenurus (larval stage of T. multiceps) cysts isolated from slaughtered Harri sheep in Taif, Saudi Arabia, by using mitochondrial cytochrome C oxidase 1 (COX1) and NADH dehydrogenase subunit 1 (NAD1) genes. Also, the study aimed to (ii) report the genetic relationship between selected genes loci of Taif isolates and other isolates present in other countries in Genbank.

2 Material and methods

2.1 Sample collection

The present study was carried out on Harri sheep from an animal slaughterhouse in Taif governorate (21.2819°N, 40.3841°E), Mecca Province, Saudi Arabia. During postmortem veterinary examination, meat was systematically inspected for hydatid and coenurus cysts occurrence by applying procedures of the routine meat inspection (sampling period from January to October 2020). Hydatid cysts were found in muscles, liver, and viscera, but coenurus cysts were found only in muscles. Therefore, we have collected samples from 20 sheep (gender, female; age, 1–2 years), about 200–300 g of muscles from each animal, which contains either hydatid or coenurus cysts from slaughtered sheep under permission from the Ministry of Environment, Water and Agriculture (KSA). Each cyst from a different animal was labeled and handled as a different isolate before carrying out the examination.

2.2 Microscopic examination

Ten samples of hydatid cysts (of E. granulosus) and the other ten samples of coenurus cysts (of T. multiceps) were collected from animal meat and carefully opened with the help of a sterile scalpel. First, protoscolices of hydatid and coenurus cysts were scraped off the inner wall of their cysts. Then, protoscolices were loaded on glass slides, covered, and examined under a light microscope without staining.

2.3 DNA extraction of protoscolices

About 300 µL of lysis buffer TNES (10 mM Tris, 400 mM NaCl, 100 mM Na2EDTA, 0.6% SDS, pH 7.5) was added to hydatid protoscolices in a microtube; then samples were frozen (in liquid nitrogen) and thawed (5×). To facilitate sample digestion, samples were ground before proteinase K (8 µL, 20 mg/mL) and incubated overnight at 37°C. Next, phenol/chloroform (100 µL) was added to the sample and centrifuged (16,500 g) for 5 min, and then, the clear upper phase was transferred into a new 1.5 mL Eppendorf. Next, for DNA precipitation, the same volume of absolute ethyl alcohol and sodium acetate (1%, 3 mol) was added to the sample and stored overnight (−20°C). Finally, samples were centrifuged (16,500 g) for 5 min, the supernatant was discarded, the pellet containing DNA was left to dry, and the pellet was finally dissolved in 100 µL sterile deionized water [17]. DNA was extracted from coenurus protoscolices with the same previous procedure using TNES lysis buffer and phenol/chloroform, but there was no need for freezing, thawing, or grinding.

2.4 PCR amplification

We have targeted two mitochondrial COX1 and NAD1 regions of E. granulosus and T. multiceps cysts by using two different primers JB3: 5′-TTTTTTGGGCATCCTGAGGTTTAT-3′, JB4.5: 5′-TAAAGAAAGAACATAATGAAAATG-3′ and JB11 5′-AGATTCGTAAGGGGCCTAATA-3′, JB12: 5′-ACCACTAACTAATTCACTTTC-3′, respectively [17]. The PCR reaction was set up with initial denaturation at 95°C (5 min), 40 cycles of denaturation at 94°C (45 s), primer annealing at 51°C (COX1) or 55°C (NAD1) (35 s), and then primer extension at 72°C (45 s). Final extension at 72°C (10 min) was necessary for complete amplification (Programmable Thermal Cycler, PTC-100TM thermal cycler, Model 96; MJ Research, Inc., Watertown, MA). PCR products were separated on 1% tris-borate/EDTA agarose gels and ethidium bromide staining and then visualized under gel documentation (Bio-Rad, USA) [18].

2.5 Sequencing and phylogenetic evaluation

Different PCR products of COX1 and NAD1 of E. granulosus and T. multiceps cysts were randomly selected and subjected to sequencing using an ABI Prism 3730 Genetic Analyzer automated sequencer. Four sequences of COX1 regions (two of each hydatid and coenurus cysts) were directly submitted in NCBI Genbank to have accession numbers. Sequences of COX1 and NAD1 were aligned with different sequences in Genbank using online NCBI BLAST, phylogenetically estimated, and finally viewed as rectangular cladogram in the phylogenetic Tree View [19].

3 Results

3.1 Morphological and microscopic examination of cysts

Hydatid and coenurus cysts appeared as fluid-filled round/oval sacs with different sizes embedded in the muscles of sheep. Protoscolices of both cysts were carefully scraped off the inner wall of their cyst rather than collecting them from cysts’ inner fluid. E. granulosus protoscolices appeared as an oval body with an invaginated scolex provided with several hooks (Figure 1). Visual examination showed numerous scolices in the inner wall of coenurus cysts. Microscopically, the isolated protoscolex showed both large and small rostellar taeniid hooks and four scup-shaped suckers (Figure 2).

Figure 1 Echinococcus granulosus protoscolices at 10× (a), and 40× (b) magnifications. Scale-bars: 100 µm.
Figure 1

Echinococcus granulosus protoscolices at 10× (a), and 40× (b) magnifications. Scale-bars: 100 µm.

Figure 2 (a) Coenurus cyst attached to a muscle. (b) Multiple scolices appeared after cyst opening. (c) Isolated protoscolex large and small rostellar hooks: blue arrow and 4 suckers: red arrows. (d) Isolated rostellar hooks. Scale bars: 100 µm.
Figure 2

(a) Coenurus cyst attached to a muscle. (b) Multiple scolices appeared after cyst opening. (c) Isolated protoscolex large and small rostellar hooks: blue arrow and 4 suckers: red arrows. (d) Isolated rostellar hooks. Scale bars: 100 µm.

3.2 PCR, sequencing, and phylogenetic analysis

Mitochondrial DNA was used to amplify two separate gene loci, COX1 and NAD1, for both E. granulosus and T. multiceps cysts to yield amplicons of 446 bp and 520 bp, respectively. The present results report the success of PCR amplification for both selected portions (Figures 3 and 4). However, NAD1 amplification shows other lower nonspecific bands.

Figure 3 Representative agarose gel stained with ethidium bromide (1.5%) showing PCR product (446 bp) of COX1 of E. granulosus (lanes 1 and 2) and T. multiceps (lanes 3 and 4) cysts. Lane M: low-molecular-weight marker (50–1,500 bp).
Figure 3

Representative agarose gel stained with ethidium bromide (1.5%) showing PCR product (446 bp) of COX1 of E. granulosus (lanes 1 and 2) and T. multiceps (lanes 3 and 4) cysts. Lane M: low-molecular-weight marker (50–1,500 bp).

Figure 4 Representative 1.5% agarose gel showing PCR product (main amplicon size 520 bp) of NAD1 of E. granulosus (lanes 1 and 2) and T. multiceps (lanes 3 and 4) cysts. Low bands are nonspecific bands. Lane M: low-molecular-weight marker (50–1,500 bp).
Figure 4

Representative 1.5% agarose gel showing PCR product (main amplicon size 520 bp) of NAD1 of E. granulosus (lanes 1 and 2) and T. multiceps (lanes 3 and 4) cysts. Low bands are nonspecific bands. Lane M: low-molecular-weight marker (50–1,500 bp).

Randomly selected PCR products from the two loci were sequenced by using their forward/reverse primers. Sequences of COX1 were deposited in Genbank and have been assigned different accession numbers: E. granulosus (COX1) MZ345697.1 and MZ350810.1; and T. multiceps coenurus cyst (COX1) MZ346598.1 and MZ348363.1, respectively. MZ345697.1, MZ350810.1, MZ346598.1, and MZ348363.1 were blasted with other related sequences in different countries. Phylogenetic trees were constructed from those sequences according to higher percentage identity and query coverage range, as shown in Figures 5 and 6. Sequences of NAD1 could not be blasted with other sequences nor submitted in Genbank due to the presence of nonspecific bands in PCR products that lead to the high noisy background in FASTA sequence (data not shown).

Figure 5 Phylogenetic relationships between Taif_Sheep E. granulosus (COX1) MZ345697.1 and MZ350810.1 (yellow highlights) with other reference sequences of E. granulosus from NCBI GenBank. GenBank sequences were shown by their name and accession numbers. Bar scale represents 0.05 nucleotide substitution per site.
Figure 5

Phylogenetic relationships between Taif_Sheep E. granulosus (COX1) MZ345697.1 and MZ350810.1 (yellow highlights) with other reference sequences of E. granulosus from NCBI GenBank. GenBank sequences were shown by their name and accession numbers. Bar scale represents 0.05 nucleotide substitution per site.

Figure 6 Phylogenetic relationships between Taif_Sheep coenurus cyst of T. multiceps (COX1) MZ346598.1 and MZ348363.1 (yellow highlights) with other reference sequences of T. multiceps from NCBI GenBank. GenBank sequences were shown by their name and accession numbers. Bar scale represents 0.007 nucleotide substitution per site.
Figure 6

Phylogenetic relationships between Taif_Sheep coenurus cyst of T. multiceps (COX1) MZ346598.1 and MZ348363.1 (yellow highlights) with other reference sequences of T. multiceps from NCBI GenBank. GenBank sequences were shown by their name and accession numbers. Bar scale represents 0.007 nucleotide substitution per site.

For E. granulosus (COX1): The BLAST analysis showed that Taif sheep isolate of COX1 sequence exhibited percentage identity 84–95.67% with Query coverage ranging from 94 to 100% of E. granulosus in GenBank isolates that were collected from other different countries. Alignment of MZ345697.1 with the other isolate MZ350810.1 showed identity with 94.95%. MZ345697.1 showed a higher alignment identity (95.67%) with E. granulosus KX017221.1 from dog stool in Palestine. MZ345697.1 showed 85% homology with Iran isolates KU359037.1, MW549010.1, MW567459.1, MW315464.1, MW549013.1, KU220240.1, and KU376099.1 from different hosts such as camel, sheep, and goat. MZ345697.1 showed 85% identity with E. granulosus isolates from Egypt MZ348909.1 and MZ348904.1 in camel and Homo sapiens, respectively. In addition, the COX1 isolate of Taif sheep showed the same identity percentage with other isolates from buffalos (MH428014.1 and MH428013.1) in India, cattle (HF947565.1) in Portugal, goat (KX379145.1) in Italy, pig (JF828338.1) in Brazil, and sheep (GQ502208.1) in Chile (Figure 5). MZ345697.1 showed lower homology (84%) with isolates from cattle in Turkey (KM100577.1, KM100574.1, MT380278.1, MT380277.1, and MT380265.1), Portugal (HF947576.1), Homo sapiens in India (JX854033.1), Iran (MK291233.1), and Homo sapiens in Poland (MH301007.1).

For larval stage (coenurus) of T. multiceps (COX1): The BLAST analysis showed that COX1 sequence (Taif-sheep isolate) exhibited a higher percentage identity 99–98% (Query coverage 100–97%) with that of T. multiceps COX1 in GenBank isolates that were collected from other different countries. Taif isolate 1, MZ346598.1, showed 97% homology with our second isolate, MZ348363.1, in the present study. MZ346598.1 showed a higher alignment identity (99%) with coenurus cyst isolates found in brains of sheep in Egypt (LC271737.1 and LC271703.1), isolates from sheep and humans in China (JX535575.1, FJ495086.1, and KT258024.1), Greece (KR604810.1), and Turkey (EF393620.1). In addition, MZ346598.1 showed 98% identity with coenurus (larval stage of T. multiceps) isolates from different hosts of China (KX547633.1, KX547641.1, MW546063.1, KX522551.1, KX547654.1, KX522552.1, JX535568.1, GQ228818.1, and JX507228.1), from goat brain, dog intestine, goat muscle, and brain of domestic yak. Moreover, MZ346598.1 showed 98% homology with coenurus COX1 isolates from Italy (DQ309767.1 and DQ309768.1), Greece (KR604811.1), and Egypt (LC271711.1). Lower identity percent was found in MZ346598.1 alignment (97%) with isolates from China (KX522555.1, MW546062.1, and KX522546.1) and Greece (KR604809.1).

4 Discussion

Cystic echinococcosis and coenurosis are zoonotic diseases that affect humans and livestock due to infection with the larval stages of Echinococcus granulosus and of Taenia multiceps cysts, leading to economic loss that increases annually [4,9,11]. Dogs, especially stray unvaccinated dogs, are definitive hosts for different cestodes of Taeniidae family, including E. granulosus and T. multiceps. Dogs were commonly associated with extensive livestock herding to protect domestic animals against predators that could lead to their infection [20,21]. For the first time, the present study reports the genetic characterization of two different parasite cysts, hydatid (the larval stage of E. granulosus) and coenurus (the larval stage of T. multiceps), in Taif governorate, Makkah Province, Saudi Arabia.

Sheep, goats, cattle, and camels represent the primary livestock species producing red meat in Saudi Arabia, with an estimated total population of 13,444,435 heads [22]. Sheep represent the significant population (72%) of the livestock, and they import large numbers of sheep to satisfy the needs of Saudi citizens. Awassi, Harri, and Najdi are the most available sheep species in Saudi Arabia [23]. Any endemic infection for livestock, such as hydatidosis and coenurosis, could lead to economic setbacks; therefore, there is a need to highlight their study, especially in KSA.

Hydatidosis and coenurosis due to E. granulosus and T. multiceps larval infection, respectively, cause significant damage in livestock that leads to production losses, especially in endemic areas [2,24]. Moreover, these parasites were distributed worldwide in different intermediate hosts, especially in sheep and goats, accidentally humans, reflecting their medical and veterinary importance [25].

The present study aims to identify two Taeniids parasites found in slaughtered Harri sheep meat based on COX1 and NAD1 partial sequencing and phylogenetic relationship. It was reported that the development of molecular techniques rather than traditional morphological criteria has provided improved tools for taeniid species identification and investigating relationships among them. Sequencing of mitochondrial DNA, especially COX1 and NAD1 loci, has been successfully used for molecular characterization and identification of taeniids tapeworm [26,27].

Our choice to use mitochondrial DNA (mtDNA) sequence, especially COX1 and NAD1, for molecular characterization of E. granulosus and T. multiceps larva was based on the previous assessment. mtDNA is widely used in molecular characterization and phylogenetic evaluation studies. COX1 gene represents the most common gene of mtDNA for phylogenetic analysis and evolutionary biology of helminth parasites to determine interspecific and/or intraspecific variation [8,28,29,30]. The mitochondrial COX1 gene is very suitable for genetic diversity detection and haplotype analysis. Its evolutionary change rate is slow enough for the same species but fast enough for differentiation between different species. Therefore, the mitochondrial COX1 gene has been selected for use in the creation of DNA barcodes and species differentiation of different helminths as our present study [31,32].

Worldwide, there have been well-documented research studies about the genetic variability among many species found within the Taeniidae, especially for the genus Echinococcus. Still, there are a few related species of Taenia, especially for T. multiceps [33]. However, there is a scarcity of studies related to the genetic characterization of E. granulosus and T. multiceps larval stages in KSA and their phylogenetic relationship.

In the current study, a genetically characterized sample based on COX1 isolated from a hydatid cyst of MZ345697.1 showed identity about 94.95% with the other isolate MZ350810.1. For coenurus cyst, isolate1 MZ346598.1 showed 97% homology with the second isolate MZ348363.1. In addition, comparing partial sequences of Taif COX1 isolates from both cysts showed different identities with other isolates from organs present in various hosts found in other countries. The present results are inconsistent with previous studies, in which Al-Hizab et al. [34] and AL-Mutairi et al. [35] have reported E. granulosus species variation based on molecular characterization in infected sheep and camels in the Arabian Peninsula and KSA. AL-Mutairi et al. [35] have reported the phenotypic and genetic characterization of hydatid cysts isolated from sheep and camel meat in Al-Madinah, KSA. Genetic characterization of E. granulosus was based on random amplified polymorphic DNA polymerase chain reaction (RAPD-PCR) for the whole genome, PCR amplification of COX1 and 12S rRNA genes followed by single-stranded conformation polymorphism (SSCP), and then sequencing. They have investigated that cyst isolates slightly vary from each other and other isolates found in Genbank. They have concluded that there is an intraspecific variation in E. granulosus found in camels and local sheep.

In addition, Christodoulopoulos et al. [36] have investigated COX1 nucleotide diversity of coenurus cyst isolates from sheep and goats in Pakistan, and their phylogenetic analysis shows high related homology with China isolates but highly different from other isolates from different countries. They have reported that coenurus cerebralis commonly found in the brain (cerebral form) could also be found in other non-cerebral tissue such as intramuscular and subcutaneous tissues.

Diversity in the nucleotide sequences of the presently studied isolates was recorded before within the same region, such as in Iran [5,13], China [26], and Italy [37,38]. Most of their phylogenetic analysis depends on one or more mtDNA sequences such as nad1, cox1, and 12S rRNA. They have concluded that there are no monophyletic groups based on the intermediate host species, the organ from which the parasite was isolated, and geographical origin [33,36]. However, reporting parasite characterization and genetic identification will be crucial for controlling and preventing parasitic infections [8].

The limitation of this study is the use of the limited sample size, and only partial sequencing was done for the COX1 gene that could have implications on data interpretation. Thus, we recommend future studies considering a larger sample size, complete sequencing COX1, and other characterization-related genes in a massive epidemiological survey for further evaluation.

5 Conclusion

The present study reports the molecular characterization of hydatid (the larval stage of E. granulosus) and coenurus (the larval stage of T. multiceps) cysts present in slaughtered sheep meat in Taif, KSA. We have determined sequences differences within isolates of the same species that we submitted in GenBank and other isolates found in Genbank from different host organs in different countries. For a more precise identification and characterization of Taeniids in KSA, additional isolates from other hosts, other geographic areas, different molecular protocols, long-sequenced genes in the mitochondrial and nuclear genome, and further information concerning biological characteristics may be necessary to increase our understanding of the epidemiological distribution in KSA.

Acknowledgments

This work was supported by Taif University Researchers Supporting Project number (TURSP-2020/299), Taif University, Taif, Saudi Arabia. The authors would like to thank the Ministry of Environment, Water and Agriculture in Taif governorate (KSA) for facilitating data and sample collections.

  1. Funding information: Taif University Researchers Supporting Project number (TURSP-2020/299).

  2. Author contributions: J.M., and N.H. participated in the design of the study. J.M. collected samples and performed parasitological assay. J.M. and N.H. carried out the molecular evaluation. N.H. performed data analysis and wrote the article draft. J.M., and N.H. read and approved the final manuscript.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Ethics approval: Data and samples were collected from veterinarians as per their periodic examination according to the ministerial recommendation. We have a permission letter from the Ministry of Environment, Water, and Agriculture (KSA) to collect cattle samples from different locations in Taif for our research study with the number 106082/1074/1442, dated 21-02-1442H. Sample collection and all experimental procedures were performed in accordance with a national ethical requirement. National Committee of Bioethics (NCBE) at King Abdulaziz City for Science and Technology (KACST) with number: 10023117, valid till October 1, 2023.

  5. Data availability statement: The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2021-08-07
Revised: 2021-11-12
Accepted: 2021-11-12
Published Online: 2021-11-27

© 2021 Jamila S. Al Malki and Nahed Ahmed Hussien, published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

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https://doi.org/10.1515/biol-2021-0131
Schlagwörter für diesen Artikel
Echinococcus granulosus; Taenia multiceps; coenurus; COX1; NAD1; Taif; Saudi Arabia
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Biomedical Sciences
  2. Research progress on the mechanism of orexin in pain regulation in different brain regions
  3. Adriamycin-resistant cells are significantly less fit than adriamycin-sensitive cells in cervical cancer
  4. Exogenous spermidine affects polyamine metabolism in the mouse hypothalamus
  5. Iris metastasis of diffuse large B-cell lymphoma misdiagnosed as primary angle-closure glaucoma: A case report and review of the literature
  6. LncRNA PVT1 promotes cervical cancer progression by sponging miR-503 to upregulate ARL2 expression
  7. Two new inflammatory markers related to the CURB-65 score for disease severity in patients with community-acquired pneumonia: The hypersensitive C-reactive protein to albumin ratio and fibrinogen to albumin ratio
  8. Circ_0091579 enhances the malignancy of hepatocellular carcinoma via miR-1287/PDK2 axis
  9. Silencing XIST mitigated lipopolysaccharide (LPS)-induced inflammatory injury in human lung fibroblast WI-38 cells through modulating miR-30b-5p/CCL16 axis and TLR4/NF-κB signaling pathway
  10. Protocatechuic acid attenuates cerebral aneurysm formation and progression by inhibiting TNF-alpha/Nrf-2/NF-kB-mediated inflammatory mechanisms in experimental rats
  11. ABCB1 polymorphism in clopidogrel-treated Montenegrin patients
  12. Metabolic profiling of fatty acids in Tripterygium wilfordii multiglucoside- and triptolide-induced liver-injured rats
  13. miR-338-3p inhibits cell growth, invasion, and EMT process in neuroblastoma through targeting MMP-2
  14. Verification of neuroprotective effects of alpha-lipoic acid on chronic neuropathic pain in a chronic constriction injury rat model
  15. Circ_WWC3 overexpression decelerates the progression of osteosarcoma by regulating miR-421/PDE7B axis
  16. Knockdown of TUG1 rescues cardiomyocyte hypertrophy through targeting the miR-497/MEF2C axis
  17. MiR-146b-3p protects against AR42J cell injury in cerulein-induced acute pancreatitis model through targeting Anxa2
  18. miR-299-3p suppresses cell progression and induces apoptosis by downregulating PAX3 in gastric cancer
  19. Diabetes and COVID-19
  20. Discovery of novel potential KIT inhibitors for the treatment of gastrointestinal stromal tumor
  21. TEAD4 is a novel independent predictor of prognosis in LGG patients with IDH mutation
  22. circTLK1 facilitates the proliferation and metastasis of renal cell carcinoma by regulating miR-495-3p/CBL axis
  23. microRNA-9-5p protects liver sinusoidal endothelial cell against oxygen glucose deprivation/reperfusion injury
  24. Long noncoding RNA TUG1 regulates degradation of chondrocyte extracellular matrix via miR-320c/MMP-13 axis in osteoarthritis
  25. Duodenal adenocarcinoma with skin metastasis as initial manifestation: A case report
  26. Effects of Loofah cylindrica extract on learning and memory ability, brain tissue morphology, and immune function of aging mice
  27. Recombinant Bacteroides fragilis enterotoxin-1 (rBFT-1) promotes proliferation of colorectal cancer via CCL3-related molecular pathways
  28. Blocking circ_UBR4 suppressed proliferation, migration, and cell cycle progression of human vascular smooth muscle cells in atherosclerosis
  29. Gene therapy in PIDs, hemoglobin, ocular, neurodegenerative, and hemophilia B disorders
  30. Downregulation of circ_0037655 impedes glioma formation and metastasis via the regulation of miR-1229-3p/ITGB8 axis
  31. Vitamin D deficiency and cardiovascular risk in type 2 diabetes population
  32. Circ_0013359 facilitates the tumorigenicity of melanoma by regulating miR-136-5p/RAB9A axis
  33. Mechanisms of circular RNA circ_0066147 on pancreatic cancer progression
  34. lncRNA myocardial infarction-associated transcript (MIAT) knockdown alleviates LPS-induced chondrocytes inflammatory injury via regulating miR-488-3p/sex determining region Y-related HMG-box 11 (SOX11) axis
  35. Identification of circRNA circ-CSPP1 as a potent driver of colorectal cancer by directly targeting the miR-431/LASP1 axis
  36. Hyperhomocysteinemia exacerbates ischemia-reperfusion injury-induced acute kidney injury by mediating oxidative stress, DNA damage, JNK pathway, and apoptosis
  37. Potential prognostic markers and significant lncRNA–mRNA co-expression pairs in laryngeal squamous cell carcinoma
  38. Gamma irradiation-mediated inactivation of enveloped viruses with conservation of genome integrity: Potential application for SARS-CoV-2 inactivated vaccine development
  39. ADHFE1 is a correlative factor of patient survival in cancer
  40. The association of transcription factor Prox1 with the proliferation, migration, and invasion of lung cancer
  41. Is there a relationship between the prevalence of autoimmune thyroid disease and diabetic kidney disease?
  42. Immunoregulatory function of Dictyophora echinovolvata spore polysaccharides in immunocompromised mice induced by cyclophosphamide
  43. T cell epitopes of SARS-CoV-2 spike protein and conserved surface protein of Plasmodium malariae share sequence homology
  44. Anti-obesity effect and mechanism of mesenchymal stem cells influence on obese mice
  45. Long noncoding RNA HULC contributes to paclitaxel resistance in ovarian cancer via miR-137/ITGB8 axis
  46. Glucocorticoids protect HEI-OC1 cells from tunicamycin-induced cell damage via inhibiting endoplasmic reticulum stress
  47. Prognostic value of the neutrophil-to-lymphocyte ratio in acute organophosphorus pesticide poisoning
  48. Gastroprotective effects of diosgenin against HCl/ethanol-induced gastric mucosal injury through suppression of NF-κβ and myeloperoxidase activities
  49. Silencing of LINC00707 suppresses cell proliferation, migration, and invasion of osteosarcoma cells by modulating miR-338-3p/AHSA1 axis
  50. Successful extracorporeal membrane oxygenation resuscitation of patient with cardiogenic shock induced by phaeochromocytoma crisis mimicking hyperthyroidism: A case report
  51. Effects of miR-185-5p on replication of hepatitis C virus
  52. Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis
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  61. CTLA-4 promotes lymphoma progression through tumor stem cell enrichment and immunosuppression
  62. WDR74 promotes proliferation and metastasis in colorectal cancer cells through regulating the Wnt/β-catenin signaling pathway
  63. Down-regulation of IGHG1 enhances Protoporphyrin IX accumulation and inhibits hemin biosynthesis in colorectal cancer by suppressing the MEK-FECH axis
  64. Curcumin suppresses the progression of gastric cancer by regulating circ_0056618/miR-194-5p axis
  65. Scutellarin-induced A549 cell apoptosis depends on activation of the transforming growth factor-β1/smad2/ROS/caspase-3 pathway
  66. lncRNA NEAT1 regulates CYP1A2 and influences steroid-induced necrosis
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  68. Isolation of microglia from retinas of chronic ocular hypertensive rats
  69. Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study
  70. Calcineurin Aβ gene knockdown inhibits transient outward potassium current ion channel remodeling in hypertrophic ventricular myocyte
  71. Aberrant expression of PI3K/AKT signaling is involved in apoptosis resistance of hepatocellular carcinoma
  72. Clinical significance of activated Wnt/β-catenin signaling in apoptosis inhibition of oral cancer
  73. circ_CHFR regulates ox-LDL-mediated cell proliferation, apoptosis, and EndoMT by miR-15a-5p/EGFR axis in human brain microvessel endothelial cells
  74. Resveratrol pretreatment mitigates LPS-induced acute lung injury by regulating conventional dendritic cells’ maturation and function
  75. Ubiquitin-conjugating enzyme E2T promotes tumor stem cell characteristics and migration of cervical cancer cells by regulating the GRP78/FAK pathway
  76. Carriage of HLA-DRB1*11 and 1*12 alleles and risk factors in patients with breast cancer in Burkina Faso
  77. Protective effect of Lactobacillus-containing probiotics on intestinal mucosa of rats experiencing traumatic hemorrhagic shock
  78. Glucocorticoids induce osteonecrosis of the femoral head through the Hippo signaling pathway
  79. Endothelial cell-derived SSAO can increase MLC20 phosphorylation in VSMCs
  80. Downregulation of STOX1 is a novel prognostic biomarker for glioma patients
  81. miR-378a-3p regulates glioma cell chemosensitivity to cisplatin through IGF1R
  82. The molecular mechanisms underlying arecoline-induced cardiac fibrosis in rats
  83. TGF-β1-overexpressing mesenchymal stem cells reciprocally regulate Th17/Treg cells by regulating the expression of IFN-γ
  84. The influence of MTHFR genetic polymorphisms on methotrexate therapy in pediatric acute lymphoblastic leukemia
  85. Red blood cell distribution width-standard deviation but not red blood cell distribution width-coefficient of variation as a potential index for the diagnosis of iron-deficiency anemia in mid-pregnancy women
  86. Small cell neuroendocrine carcinoma expressing alpha fetoprotein in the endometrium
  87. Superoxide dismutase and the sigma1 receptor as key elements of the antioxidant system in human gastrointestinal tract cancers
  88. Molecular characterization and phylogenetic studies of Echinococcus granulosus and Taenia multiceps coenurus cysts in slaughtered sheep in Saudi Arabia
  89. ITGB5 mutation discovered in a Chinese family with blepharophimosis-ptosis-epicanthus inversus syndrome
  90. ACTB and GAPDH appear at multiple SDS-PAGE positions, thus not suitable as reference genes for determining protein loading in techniques like Western blotting
  91. Facilitation of mouse skin-derived precursor growth and yield by optimizing plating density
  92. 3,4-Dihydroxyphenylethanol ameliorates lipopolysaccharide-induced septic cardiac injury in a murine model
  93. Downregulation of PITX2 inhibits the proliferation and migration of liver cancer cells and induces cell apoptosis
  94. Expression of CDK9 in endometrial cancer tissues and its effect on the proliferation of HEC-1B
  95. Novel predictor of the occurrence of DKA in T1DM patients without infection: A combination of neutrophil/lymphocyte ratio and white blood cells
  96. Investigation of molecular regulation mechanism under the pathophysiology of subarachnoid hemorrhage
  97. miR-25-3p protects renal tubular epithelial cells from apoptosis induced by renal IRI by targeting DKK3
  98. Bioengineering and Biotechnology
  99. Green fabrication of Co and Co3O4 nanoparticles and their biomedical applications: A review
  100. Agriculture
  101. Effects of inorganic and organic selenium sources on the growth performance of broilers in China: A meta-analysis
  102. Crop-livestock integration practices, knowledge, and attitudes among smallholder farmers: Hedging against climate change-induced shocks in semi-arid Zimbabwe
  103. Food Science and Nutrition
  104. Effect of food processing on the antioxidant activity of flavones from Polygonatum odoratum (Mill.) Druce
  105. Vitamin D and iodine status was associated with the risk and complication of type 2 diabetes mellitus in China
  106. Diversity of microbiota in Slovak summer ewes’ cheese “Bryndza”
  107. Comparison between voltammetric detection methods for abalone-flavoring liquid
  108. Composition of low-molecular-weight glutenin subunits in common wheat (Triticum aestivum L.) and their effects on the rheological properties of dough
  109. Application of culture, PCR, and PacBio sequencing for determination of microbial composition of milk from subclinical mastitis dairy cows of smallholder farms
  110. Investigating microplastics and potentially toxic elements contamination in canned Tuna, Salmon, and Sardine fishes from Taif markets, KSA
  111. From bench to bar side: Evaluating the red wine storage lesion
  112. Establishment of an iodine model for prevention of iodine-excess-induced thyroid dysfunction in pregnant women
  113. Plant Sciences
  114. Characterization of GMPP from Dendrobium huoshanense yielding GDP-D-mannose
  115. Comparative analysis of the SPL gene family in five Rosaceae species: Fragaria vesca, Malus domestica, Prunus persica, Rubus occidentalis, and Pyrus pyrifolia
  116. Identification of leaf rust resistance genes Lr34 and Lr46 in common wheat (Triticum aestivum L. ssp. aestivum) lines of different origin using multiplex PCR
  117. Investigation of bioactivities of Taxus chinensis, Taxus cuspidata, and Taxus × media by gas chromatography-mass spectrometry
  118. Morphological structures and histochemistry of roots and shoots in Myricaria laxiflora (Tamaricaceae)
  119. Transcriptome analysis of resistance mechanism to potato wart disease
  120. In silico analysis of glycosyltransferase 2 family genes in duckweed (Spirodela polyrhiza) and its role in salt stress tolerance
  121. Comparative study on growth traits and ions regulation of zoysiagrasses under varied salinity treatments
  122. Role of MS1 homolog Ntms1 gene of tobacco infertility
  123. Biological characteristics and fungicide sensitivity of Pyricularia variabilis
  124. In silico/computational analysis of mevalonate pyrophosphate decarboxylase gene families in Campanulids
  125. Identification of novel drought-responsive miRNA regulatory network of drought stress response in common vetch (Vicia sativa)
  126. How photoautotrophy, photomixotrophy, and ventilation affect the stomata and fluorescence emission of pistachios rootstock?
  127. Apoplastic histochemical features of plant root walls that may facilitate ion uptake and retention
  128. Ecology and Environmental Sciences
  129. The impact of sewage sludge on the fungal communities in the rhizosphere and roots of barley and on barley yield
  130. Domestication of wild animals may provide a springboard for rapid variation of coronavirus
  131. Response of benthic invertebrate assemblages to seasonal and habitat condition in the Wewe River, Ashanti region (Ghana)
  132. Molecular record for the first authentication of Isaria cicadae from Vietnam
  133. Twig biomass allocation of Betula platyphylla in different habitats in Wudalianchi Volcano, northeast China
  134. Animal Sciences
  135. Supplementation of probiotics in water beneficial growth performance, carcass traits, immune function, and antioxidant capacity in broiler chickens
  136. Predators of the giant pine scale, Marchalina hellenica (Gennadius 1883; Hemiptera: Marchalinidae), out of its natural range in Turkey
  137. Honey in wound healing: An updated review
  138. NONMMUT140591.1 may serve as a ceRNA to regulate Gata5 in UT-B knockout-induced cardiac conduction block
  139. Radiotherapy for the treatment of pulmonary hydatidosis in sheep
  140. Retraction
  141. Retraction of “Long non-coding RNA TUG1 knockdown hinders the tumorigenesis of multiple myeloma by regulating microRNA-34a-5p/NOTCH1 signaling pathway”
  142. Special Issue on Reuse of Agro-Industrial By-Products
  143. An effect of positional isomerism of benzoic acid derivatives on antibacterial activity against Escherichia coli
  144. Special Issue on Computing and Artificial Techniques for Life Science Applications - Part II
  145. Relationship of Gensini score with retinal vessel diameter and arteriovenous ratio in senile CHD
  146. Effects of different enantiomers of amlodipine on lipid profiles and vasomotor factors in atherosclerotic rabbits
  147. Establishment of the New Zealand white rabbit animal model of fatty keratopathy associated with corneal neovascularization
  148. lncRNA MALAT1/miR-143 axis is a potential biomarker for in-stent restenosis and is involved in the multiplication of vascular smooth muscle cells
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Heruntergeladen am 7.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/biol-2021-0131/html?lang=de
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