scholarly journals Identification of heat responsive genes in pea stipules and anthers through transcriptional profiling

2021 ◽  
Author(s):  
Shaoming Huang ◽  
Krishna K. Kishore ◽  
Reddy V.B. Lachagari ◽  
Navajeet Chakravartty ◽  
Rosalind A. Bueckert ◽  
...  
Keyword(s):  
Heat Tolerance ◽  
Cellular Response ◽  
Molecular Mechanisms ◽  
Transcriptional Profiling ◽  
Field Performance ◽  
Enrichment Analysis ◽  
Field Pea ◽  
Biological Processes ◽  
Legume Crop ◽  
Heat Tolerant

AbstractField pea (Pisum sativum L.), a cool-season legume crop, is known for poor heat tolerance. Our previous work identified PR11-2 and PR11-90 as heat tolerant and susceptible lines in a recombinant inbred population. CDC Amarillo, a Canadian elite pea variety, was considered as another heat tolerant variety based on its similar field performance as PR11-2. This study aimed to characterize the differential transcription. Plants of these three varieties were stressed for 3h at 38°C prior to self-pollination, and RNAs from heat stressed anthers and stipules on the same flowering node were extracted and sequenced via the Illumina NovaSeq platform for the characterization of heat responsive genes. In silico results were further validated by qPCR assay. Differentially expressed genes (DEGs) were identified at log2 fold change, the three varieties shared 588 DEGs which were up-regulated and 220 genes which were down-regulated in anthers when subjected to heat treatment. In stipules, 879 DEGs (463/416 upregulation/downregulation) were consistent among varieties. The above heat-induced genes of the two plant organs were related to several biological processes i.e., response to heat, protein folding and DNA templated transcription. Ten gene ontology (GO) terms were over-represented in the consistently down-regulated DEGs of the two organs, and these terms were mainly related to cell wall macromolecule metabolism, lipid transport, lipid localization, and lipid metabolic processes. GO enrichment analysis on distinct DEGs of individual pea varieties suggested that heat affected biological processes were dynamic, and variety distinct responses provide insight into molecular mechanisms of heat-tolerance response. Several biological processes, e.g., cellular response to DNA damage stimulus in stipule, electron transport chain in anther that were only observed in heat induced PR11-2 and CDC Amarillo, and their relevance to field pea heat tolerance is worth further validation.

scholarly journals Network pharmacology and molecular docking study on the active ingredients of qidengmingmu capsule for the treatment of diabetic retinopathy

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Mingxu Zhang ◽  
Jiawei Yang ◽  
Xiulan Zhao ◽  
Ying Zhao ◽  
Siquan Zhu
Keyword(s):  
Diabetic Retinopathy ◽  
Molecular Docking ◽  
Molecular Mechanisms ◽  
Hypoxia Inducible Factor ◽  
Enrichment Analysis ◽  
Docking Study ◽  
Network Pharmacology ◽  
Biological Processes ◽  
Active Ingredients ◽  
Molecular Docking Study

AbstractDiabetic retinopathy (DR) is a leading cause of irreversible blindness globally. Qidengmingmu Capsule (QC) is a Chinese patent medicine used to treat DR, but the molecular mechanism of the treatment remains unknown. In this study, we identified and validated potential molecular mechanisms involved in the treatment of DR with QC via network pharmacology and molecular docking methods. The results of Ingredient-DR Target Network showed that 134 common targets and 20 active ingredients of QC were involved. According to the results of enrichment analysis, 2307 biological processes and 40 pathways were related to the treatment effects. Most of these processes and pathways were important for cell survival and were associated with many key factors in DR, such as vascular endothelial growth factor-A (VEGFA), hypoxia-inducible factor-1A (HIF-1Α), and tumor necrosis factor-α (TNFα). Based on the results of the PPI network and KEGG enrichment analyses, we selected AKT1, HIF-1α, VEGFA, TNFα and their corresponding active ingredients for molecular docking. According to the molecular docking results, several key targets of DR (including AKT1, HIF-1α, VEGFA, and TNFα) can form stable bonds with the corresponding active ingredients of QC. In conclusion, through network pharmacology methods, we found that potential biological mechanisms involved in the alleviation of DR by QC are related to multiple biological processes and signaling pathways. The molecular docking results also provide us with sound directions for further experiments.

scholarly journals Downregulation of PyHRG1, encoding a novel secretory protein in the red alga Pyropia yezoensis, enhances heat tolerance

ALGAE ◽  
2021 ◽  
Vol 36 (3) ◽  
pp. 207-217
Author(s):  
Narae Han ◽  
Jiwoong Wi ◽  
Sungoh Im ◽  
Ka-Min Lim ◽  
Hun-Dong Lee ◽  
...  
Keyword(s):  
Heat Stress ◽  
Heat Tolerance ◽  
Red Algae ◽  
Molecular Mechanisms ◽  
Seawater Temperature ◽  
Secretory Protein ◽  
Red Alga ◽  
Pyropia Yezoensis ◽  
Tolerant Mutant ◽  
Heat Tolerant

An increase in seawater temperature owing to global warming is expected to substantially limit the growth of marine algae, including Pyropia yezoensis, a commercially valuable red alga. To improve our knowledge of the genes involved in the acquisition of heat tolerance in P. yezoensis, transcriptomes sequences were obtained from both the wild-type SG104 P. yezoensis and heat-tolerant mutant Gy500. We selected 1,251 differentially expressed genes that were up- or downregulated in response to the heat stress condition and in the heat-tolerant mutant Gy500, based on fragment per million reads expression values. Among them, PyHRG1 was downregulated under heat stress in SG104 and expressed at a low level in Gy500. PyHRG1 encodes a secretory protein of 26.5 kDa. PyHRG1 shows no significant sequence homology with any known genes deposited in public databases to date. However, PyHRG1 homologs were found in other red algae, including other Pyropia species. When PyHRG1 was introduced into the single-cell green alga Chlamydomonas reinhardtii, transformed cells overexpressing PyHRG1 showed severely retarded growth. These results demonstrate that PyHRG1 encodes a novel red algae-specific protein and plays a role in heat tolerance in algae. The transcriptome sequences obtained in this study, which include PyHRG1, will facilitate future studies to understand the molecular mechanisms involved in heat tolerance in red algae.

scholarly journals Transcriptomic profiling revealed key signaling pathways for cold tolerance and acclimation of two carp species

2020 ◽  
Author(s):  
Guodong Ge ◽  
Yong Long ◽  
Lianyu Shi ◽  
Jing Ren ◽  
Junjun Yan ◽  
...  
Keyword(s):  
Signaling Pathways ◽  
Cold Acclimation ◽  
Cold Tolerance ◽  
Drug Transport ◽  
Molecular Mechanisms ◽  
Protein Transport ◽  
Secondary Alcohol ◽  
Enrichment Analysis ◽  
Biological Processes ◽  
Mirror Carp

Abstract Background Closely related species of the carp family ( Cyprinidae ) have evolved distinctive abilities to survive under cold stress, but molecular mechanisms underlying the generation of cold resistance remain largely unknow. In this study, we compared transcriptomic profiles of two carp species to identify key factors and pathways for cold tolerance and acclimation. Results Larvae of Songpu mirror carp and Barbless carp that were pretreated at 18°C for 24 hours significantly improved their survival rates under lethal cold temperature at 8°C or 10°C, indicating that two carp species possess the ability of cold acclimation. However, Songpu mirror carp exhibited stronger abilities of cold tolerance and acclimation than Barbless carp. Transcriptomic profiles of Songpu mirror carp and Barbless carp larvae at 28°C and 18°C were compared during cold acclimation through RNA-seq. Differentially expressed genes that are closely associated with the differences in cold acclimation between two carp species were identified through bioinformatics and Venn's diagram analysis. GO enrichment analysis of these genes indicated that cellular component assembly involved in morphogenesis, secondary alcohol metabolism and drug transport were the most up-regulated biological processes during cold acclimation of Songpu mirror carp. Conversely, positive regulation of macroautophagy, intracellular protein transport, and organonitrogen compound catabolism were the most down-regulated biological processes during cold acclimation of Barbless carp. KEGG enrichment analysis revealed that factors in the FoxO-related signaling pathways are mainly responsible for the development of differences in cold tolerance and acclimation between two carp species since altering the phosphorylation of key proteins in the FoxO-related signaling pathways with inhibitors or an activator significantly decreased the cold tolerance and acclimation of Songpu mirror carp. These data provided key clues for dissection of molecular mechanisms underlying the development of cold tolerance and acclimation in carps. Conclusions These findings indicate that larvae of two carp species possess different abilities of cold tolerance and can build cold acclimation under mild low temperature. Multiple biological processes and FoxO-related signaling pathways are closely associated with the development of differences in cold tolerance and acclimation between two carp species.

PS02.037: NETWORK AND PATHWAY-BASED ANALYSIS OF GENES ASSOCIATED WITH ESOPHAGEAL SQUAMOUS CELL CARCINOMA

2018 ◽  
Vol 31 (Supplement_1) ◽  
pp. 130-130
Author(s):  
Wenwu He ◽  
Yongtao Han ◽  
Kun Yuan ◽  
Peng Lin
Keyword(s):  
Cell Proliferation ◽  
Squamous Cell Carcinoma ◽  
Esophageal Squamous Cell Carcinoma ◽  
Cell Carcinoma ◽  
Squamous Cell ◽  
Cellular Response ◽  
Molecular Mechanisms ◽  
Diagnostic Methods ◽  
Biological Processes ◽  
Pathway Crosstalk

Abstract Background As a highly malignant and aggressive tumor, Esophageal Squamous Cell Carcinoma (ESCC) is not sensitive to chemoradiotherapy and chemotherapy. Although diagnostic methods and treatments have improved over the last few years, the 5-year survival rate of ESCC patients remains generally poor. The development of high-throughput technology has witnessed the great achievements in localization ESCC related genes/proteins, and many genes/proteins are considered as potential targets for detection or treatment. To take a further quest for a thorough understanding of the biological processes involved in the pathogenesis of ESCC at the molecular level, the potential pathogenesis of ESCC needs to be deciphered at a phylogenetic level. Methods The interaction of these genes was explored by collecting genes associated with ESCC, using gene enrichment assays, pathway enrichment assays, pathway crosstalk analysis and extraction of ESCC-specific subnetwork to describe the relevant biochemical processes. Results Through GO enrichment analysis, many molecular functions related to response to chemical, cellular response to stimulus and cell proliferation were found to be significantly enriched in ESCC-related genes. The results of pathway and pathway crosstalk analysis showed that pathways associated with multiple malignant tumors, the immune system and metabolic processes were significantly enriched in ESCC-related genes. Through the analysis of specific subnetwork, we obtained some novel ESCC-related potential genes, such as MUC13, GSTO1, FIN, GRB2, CDC25C and so on. Conclusion The molecular mechanism of ESCC is extremely complex. Some inducing factors change the expression status of many genes. The abnormal expression of genes mediates the biological processes involved in immunity and metabolism, apoptosis and cell proliferation, leading to the occurrence of tumors. Gene MUC13, RYK, FIN may be potential prognostic indicators of ESCC. GRB2 and CDC25C may be potential targets of ESCC in proliferation. Our work may provide valuable information for understanding the molecular mechanisms for the development of ESCC. Disclosure All authors have declared no conflicts of interest.

scholarly journals Cytosine methylations in the promoter regions of genes involved in the cellular oxidation equilibrium pathways affect rice heat tolerance

2020 ◽  
Author(s):  
Chao He ◽  
Hong-Yu Zhang ◽  
Yong-Xin Zhang ◽  
Pei Fu ◽  
Li-Li You ◽  
...  
Keyword(s):  
Rna Polymerase Ii ◽  
Heat Tolerance ◽  
Molecular Mechanisms ◽  
Pentatricopeptide Repeat ◽  
Ros Scavenging ◽  
Promoter Regions ◽  
Tolerant Strain ◽  
Rice Strain ◽  
Heat Tolerant ◽  
Methylation Patterns

Abstract Background: High temperatures, particularly at night, decrease rice yield and quality. As high nighttime temperatures (HNTs) become increasingly frequent due to climate change, it is imperative to develop rice crops that tolerate HNTs. DNA methylation may represent a potential avenue for HNT-tolerant rice strain development, as this mechanism regulates gene activity and cellular phenotype in response to adverse environmental conditions without changing the nucleotide sequence.Results: After HNT exposure, the methylation patterns of cytosines in the CHH context differed noticeably between two coisogenic rice strains with significantly different levels in heat tolerance. Methylation differences between strains were primarily observed on successive cytosines in the promoter or downstream regions of transcription factors and transposon elements. In contrast to the heat-sensitive rice strain, the regions 358–359 bp and 2–60 bp downstream of two basal transcriptional factors (TFIID subunit 11 and mediator of RNA polymerase II transcription subunit 31, respectively) were fully demethylated in the heat-tolerant strain after HNT exposure. In the heat-tolerant strain, HNTs reversed the methylation patterns of successive cytosines in the promoter regions of various genes involved in abscisic acid (ABA)-related reactive oxygen species (ROS) equilibrium pathways, including the pentatricopeptide repeat domain gene PPR (LOC_Os07g28900) and the homeobox domain gene homeobox (LOC_Os01g19694). Indeed, PRR expression was inhibited in heat-sensitive rice strains, and the methylation rates of the cytosines in the promoter region of PRR were greater in heat-sensitive strains as compared to heat-tolerant strains.Conclusions: After HNT exposure, cytosines in the CHH context were more likely than cytosines in other contexts to be methylated differently between the heat-sensitive and heat-tolerant rice strains. Methylation in the promoter regions of the genes associated with ABA-related oxidation and ROS scavenging improved heat tolerance in rice. Our results help to clarify the molecular mechanisms underlying rice heat tolerance.

scholarly journals Transcriptome Analysis Reveals Potential Regulatory Genes Related to Heat Tolerance in Holstein Dairy Cattle

Genes ◽  
2020 ◽  
Vol 11 (1) ◽  
pp. 68
Author(s):  
Shenhe Liu ◽  
Tingting Yue ◽  
Muhammad Jamil Ahmad ◽  
Xiangwei Hu ◽  
Xinxin Zhang ◽  
...  
Keyword(s):  
Dairy Cows ◽  
Heat Tolerance ◽  
Molecular Mechanisms ◽  
High Throughput Sequencing ◽  
Principal Component ◽  
Production Performance ◽  
Value Analysis ◽  
Chinese Holstein ◽  
Heat Tolerant ◽  
Holstein Dairy Cows

Heat stress affects the physiology and production performance of Chinese Holstein dairy cows. As such, the selection of heat tolerance in cows and elucidating its underlying mechanisms are vital to the dairy industry. This study aimed to investigate the heat tolerance associated genes and molecular mechanisms in Chinese Holstein dairy cows using a high-throughput sequencing approach and bioinformatics analysis. Heat-induced physiological indicators and milk yield changes were assessed to determine heat tolerance levels in Chinese Holstein dairy cows by Principal Component Analysis method following Membership Function Value Analysis. Results indicated that rectal temperature (RT), respiratory rate (RR), and decline in milk production were significantly lower (p < 0.05) in heat tolerant (HT) cows while plasma levels of heat shock protein (HSP: HSP70, HSP90), and cortisol were significantly higher (p < 0.05) when compared to non-heat tolerant (NHT) Chinese Holstein dairy cows. By applying RNA-Seq analysis, we identified 200 (81 down-regulated and 119 up-regulated) significantly (|log2fold change| ≥ 1.4 and p ≤ 0.05) differentially expressed genes (DEGs) in HT versus NHT Chinese Holstein dairy cows. In addition, 14 of which were involved in protein–protein interaction (PPI) network. Importantly, several hub genes (OAS2, MX2, IFIT5 and TGFB2) were significantly enriched in immune effector process. These findings might be helpful to expedite the understanding for the mechanism of heat tolerance in Chinese Holstein dairy cows.

scholarly journals Transcriptomic profiling revealed key signaling pathways for cold tolerance and acclimation of two carp species

2019 ◽  
Author(s):  
Guodong Ge ◽  
Yong Long ◽  
Lianyu Shi ◽  
Jing Ren ◽  
Junjun Yan ◽  
...  
Keyword(s):  
Signaling Pathways ◽  
Cold Acclimation ◽  
Cold Tolerance ◽  
Drug Transport ◽  
Molecular Mechanisms ◽  
Secondary Alcohol ◽  
Enrichment Analysis ◽  
Biological Processes ◽  
Rna Seq ◽  
Mirror Carp

Abstract Background Closely related species of the carp family ( Cyprinidae ) have evolved distinctive abilities to survive under cold stress, but molecular mechanisms underlying the generation of cold resistance remain largely unknow. In this study, we compared transcriptomic profiles of two carp species to identify key factors and pathways for cold tolerance and acclimation. Results Larvae of Songpu mirror carp and Barbless carp that were pretreated at 18°C for 24 hours significantly improved their survival rates under lethal cold temperature at 8°C or 10°C, indicating that two carp species possess the ability of cold acclimation. However, Songpu mirror carp exhibited stronger abilities of cold tolerance and acclimation than Barbless carp. Transcriptomic profiles of Songpu mirror carp and Barbless carp larvae at 28°C and 18°C were compared during cold acclimation through RNA-seq. Differentially expressed genes that are closely associated with the differences in cold acclimation between two carp species were identified through bioinformatics and Venn's diagram analysis. GO enrichment analysis of these genes indicated that cellular component assembly involved in morphogenesis, secondary alcohol metabolism and drug transport were the most up-regulated biological processes during cold acclimation of Songpu mirror carp. Conversely, positive regulation of macroautophagy, intracellular protein transport, and organonitrogen compound catabolism were the most down-regulated biological processes during cold acclimation of Barbless carp. KEGG enrichment analysis revealed that factors in the FoxO-related signaling pathways are mainly responsible for the development of differences in cold tolerance and acclimation between two carp species since altering the phosphorylation of key proteins in the FoxO-related signaling pathways with inhibitors or an activator significantly decreased the cold tolerance and acclimation of Songpu mirror carp. These data provided key clues for dissection of molecular mechanisms underlying the development of cold tolerance and acclimation in carps. Conclusions These findings indicate that larvae of two carp species possess different abilities of cold tolerance and can build cold acclimation under mild low temperature. Multiple biological processes and FoxO-related signaling pathways are closely associated with the development of differences in cold tolerance and acclimation between two carp species. Keywords: Carp; cold tolerance; cold acclimation; RNA-Seq; biological process; signaling pathways

scholarly journals Transcriptomic profiling revealed key signaling pathways for cold tolerance and acclimation of two carp species

2020 ◽  
Author(s):  
Guodong Ge ◽  
Yong Long ◽  
Lianyu Shi ◽  
Jing Ren ◽  
Junjun Yan ◽  
...  
Keyword(s):  
Signaling Pathways ◽  
Cold Acclimation ◽  
Cold Tolerance ◽  
Drug Transport ◽  
Molecular Mechanisms ◽  
Protein Transport ◽  
Secondary Alcohol ◽  
Enrichment Analysis ◽  
Biological Processes ◽  
Mirror Carp

Abstract Background: Closely related species of the carp family (Cyprinidae) have evolved distinctive abilities to survive under cold stress, but molecular mechanisms underlying the generation of cold resistance remain largely unknown. In this study, we compared transcriptomic profiles of two carp species to identify key factors and pathways for cold tolerance and acclimation. Results: Larvae of Songpu mirror carp and Barbless carp that were pretreated at 18°C for 24 hours significantly improved their survival rates under lethal cold temperature at 8°C or 10°C, indicating that two carp species possess the ability of cold acclimation. However, Songpu mirror carp exhibited stronger abilities of cold tolerance and acclimation than Barbless carp. Transcriptomic profiles of Songpu mirror carp and Barbless carp larvae at 28°C and 18°C were compared during cold acclimation through RNA-seq. Differentially expressed genes that are closely associated with the differences in cold acclimation between two carp species were identified through bioinformatics and Venn's diagram analysis. GO enrichment analysis of these genes indicated that cellular component assembly involved in morphogenesis, secondary alcohol metabolism and drug transport were the most up-regulated biological processes during cold acclimation of Songpu mirror carp. Conversely, positive regulation of macroautophagy, intracellular protein transport, and organonitrogen compound catabolism were the most down-regulated biological processes during cold acclimation of Barbless carp. KEGG enrichment analysis revealed that factors in the FoxO-related signaling pathways are mainly responsible for the development of differences in cold tolerance and acclimation between two carp species since altering the phosphorylation of key proteins in the FoxO-related signaling pathways with inhibitors or an activator significantly decreased the cold tolerance and acclimation of Songpu mirror carp. These data provided key clues for dissection of molecular mechanisms underlying the development of cold tolerance and acclimation in carps. Conclusions: These findings indicate that larvae of two carp species possess different abilities of cold tolerance and can build cold acclimation under mild low temperature. Multiple biological processes and FoxO-related signaling pathways are closely associated with the development of differences in cold tolerance and acclimation between two carp species.

scholarly journals GeneTrail 3: advanced high-throughput enrichment analysis

2020 ◽  
Vol 48 (W1) ◽  
pp. W515-W520 ◽  
Author(s):  
Nico Gerstner ◽  
Tim Kehl ◽  
Kerstin Lenhof ◽  
Anne Müller ◽  
Carolin Mayer ◽  
...  
Keyword(s):  
Web Service ◽  
Molecular Mechanisms ◽  
Enrichment Analysis ◽  
Model Organisms ◽  
Data Sets ◽  
Biological Processes ◽  
Comprehensive Collection ◽  
Rich Functionality ◽  
Identification Analysis ◽  
Cell Data

Abstract We present GeneTrail 3, a major extension of our web service GeneTrail that offers rich functionality for the identification, analysis, and visualization of deregulated biological processes. Our web service provides a comprehensive collection of biological processes and signaling pathways for 12 model organisms that can be analyzed with a powerful framework for enrichment and network analysis of transcriptomic, miRNomic, proteomic, and genomic data sets. Moreover, GeneTrail offers novel workflows for the analysis of epigenetic marks, time series experiments, and single cell data. We demonstrate the capabilities of our web service in two case-studies, which highlight that GeneTrail is well equipped for uncovering complex molecular mechanisms. GeneTrail is freely accessible at: http://genetrail.bioinf.uni-sb.de.

Mechanisms of Signaling through Urokinase Receptor and the Cellular Response

1999 ◽  
Vol 82 (08) ◽  
pp. 305-311 ◽  
Author(s):  
Yuri Koshelnick ◽  
Monika Ehart ◽  
Hannes Stockinger ◽  
Bernd Binder
Keyword(s):  
Cell Surface ◽  
Proteolytic Activity ◽  
Tumor Invasion ◽  
Cellular Response ◽  
Transmembrane Protein ◽  
Urokinase Receptor ◽  
Biological Processes ◽  
In Vivo Models ◽  
Proteolytic Activation ◽  
Core Proteins

IntroductionThe urokinase-urokinase receptor (u-PA-u-PAR) system seems to play a crucial role in a number of biological processes, including local fibrinolysis, tumor invasion, angiogenesis, neointima and atherosclerotic plaque formation, inflammation, and matrix remodeling during wound healing and development.1-6 Binding of urokinase to its specific receptor provides cells with a localized proteolytic potential. It stimulates conversion of cell surface-bound plasminogen into active plasmin, which, in turn, is required for proteolytic degradation of basement membrane components, including fibronectin, collagen, laminin, and proteoglycan core proteins.7 Moreover, plasmin activates other matrix-degrading enzymes, such as matrix metalloproteinases.8 Overexpression of u-PA/u-PAR correlates with tumor invasion and metastasis formation,9-13 while reduction of cell-surface bound u-PA and inhibition of u-PAR expression leads to a significant decrease of invasive and metastatic activity.14 Specific antagonists that suppress binding of u-PA to u-PAR have been shown to inhibit cell-surface plasminogen activation, tumor growth, and angiogenesis both in vitro and in vivo models.15,16 Independently of its proteolytic activity, u-PA is implicated in many biological processes that seem to require u-PAR-mediated intracellular signal transduction, such as proliferation, chemotactic movement and adhesion, migration, and differentiation.17 Data obtained in the late 1980s indicated that u-PA not only provides cells with local proteolytic activity, but might also be capable of transducing signals to the cell.18-22 At that time, however, the u-PAR has just been isolated, cloned, and identified as a glycosylphosphatidylinositol (GPI)-linked protein and not a transmembrane protein. Signaling via the u-PAR was, therefore, regarded as being unlikely, and the effects of u-PA on cell proliferation18-22 were thought to be mediated by proteolytic activation of latent growth factors. The assumption of direct signaling via u-PAR was, in fact, considered controversial, until about 10 years later when a physical association between u-PAR and signaling proteins was found.23 From this report on, several proteins associated with u-PAR have been identified. Now, u-PAR seems to be part of a large “signalosome” associated and interacting with several proteins on both the outside and inside of the cell.

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