Huangqi Jianzhong decoction improves gastric intestinal metaplasia in rats by regulating the gut‒thyroid axis
•GIM rats exhibited gastro-thyroid comorbidities with cold-intolerant. HQJZ treatment restored low-temperature-tropism behavior, enriching fecal butyrate-producing bacteria, and improved thyroid tissue lesions.•In vivo and in vitro experiments proved that butyrate improved thyroid tissue lesions, en...
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| Published in | Phytomedicine (Stuttgart) Vol. 135; p. 156174 |
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| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier GmbH
01.12.2024
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| Abstract | •GIM rats exhibited gastro-thyroid comorbidities with cold-intolerant. HQJZ treatment restored low-temperature-tropism behavior, enriching fecal butyrate-producing bacteria, and improved thyroid tissue lesions.•In vivo and in vitro experiments proved that butyrate improved thyroid tissue lesions, enhanced the expression of the thyroid TG, TPO, and TSHR genes, promoted T3 and T4 synthesis and secretion.•The gut microbiota-thyroid axis plays a key role in HQJZ improving the low-energy metabolism of GIM rats, which provides solid evidences for the clinical application of HQJZ in cold-intolerant PLGC patients.
Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood.
The present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis.
A GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3–1 cell model.
HQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3–1 cells through the upregulation of TG, TPO, and TSHR expression.
HQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria.
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| AbstractList | •GIM rats exhibited gastro-thyroid comorbidities with cold-intolerant. HQJZ treatment restored low-temperature-tropism behavior, enriching fecal butyrate-producing bacteria, and improved thyroid tissue lesions.•In vivo and in vitro experiments proved that butyrate improved thyroid tissue lesions, enhanced the expression of the thyroid TG, TPO, and TSHR genes, promoted T3 and T4 synthesis and secretion.•The gut microbiota-thyroid axis plays a key role in HQJZ improving the low-energy metabolism of GIM rats, which provides solid evidences for the clinical application of HQJZ in cold-intolerant PLGC patients.
Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood.
The present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis.
A GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3–1 cell model.
HQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3–1 cells through the upregulation of TG, TPO, and TSHR expression.
HQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria.
[Display omitted] Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood.BACKGROUNDGastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood.The present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis.OBJECTIVEThe present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis.A GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3-1 cell model.METHODSA GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3-1 cell model.HQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3-1 cells through the upregulation of TG, TPO, and TSHR expression.RESULTSHQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3-1 cells through the upregulation of TG, TPO, and TSHR expression.HQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria.CONCLUSIONSHQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria. Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood. The present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis. A GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3–1 cell model. HQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3–1 cells through the upregulation of TG, TPO, and TSHR expression. HQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria. Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading therapeutic strategy for treating GIM patients with cold intolerance in traditional Chinese medicine clinics, but the detailed mechanism remains poorly understood. The present study aimed to elucidate the molecular mechanism by which HQJZ alleviates GIM in a rat model on the basis of the gut microbiota‒thyroid axis. A GIM rat model was established by administering cold salicylic acid and sodium deoxycholate (SDC) for 12 weeks, followed by gavage treatment with HQJZ for an additional four weeks. Lianpu Yin (LPY) was used as a comparison formula. The cold tolerance characteristics of GIM rats were evaluated using cold tolerance and temperature‒tropism experiment experiments. Thyroid pathological changes were evaluated with HE staining, and thyroid function was measured via quantification of T3 and T4 levels with ELISA. The gut microbiota was analyzed using 16S rRNA gene sequencing, and fecal butyric acid and serum metabolites were quantified utilizing metabolomics. The key molecular mechanism was verified in the Nthy-ori 3-1 cell model. HQJZ, but not LPY, significantly improved gastric mucosa and thyroid tissue lesions in GIM rats, increased the serum levels of the thyroid hormones T3 and T4, and enhanced cold tolerance. HQJZ treatment promoted the enrichment of fecal butyrate-producing bacteria, specifically the bacteria Allobaculum and Bifidobacterium, resulting in a marked increase in fecal butyric acid concentrations. HQJZ treatment significantly diminished the levels of mitochondrial damage-related serum metabolites, including p-cresol sulfate and indoxyl sulfate. Mechanistically, in vivo investigations further demonstrated that butyric acid not only improved thyroid tissue lesions but also restored the fecal microbiota structure, as well as low-temperature tropism, in GIM rats. Furthermore, butyrate diminished the mitochondrial damage induced by SDC in these cells, as evidenced by decreased reactive oxygen species levels and increased ATP production and mitochondrial membrane potential. Importantly, in vitro studies revealed that butyrate protected against SDC-induced injury in Nthy-ori 3-1 cells through the upregulation of TG, TPO, and TSHR expression. HQJZ promotes cold tolerance and improves thyroid function in GIM rats by enriching gut butyrate-producing bacteria. |
| ArticleNumber | 156174 |
| Author | Ma, Wen-shuo Cheng, Chun Meng, Yu-fen Zhu, Wen-fei Zhang, Wei Chen, Lei Wu, Jian-ping Zhang, Jun-feng Xiao, Ling Cheng, Yu-qin Shi, Li-yun |
| Author_xml | – sequence: 1 givenname: Ling orcidid: 0000-0003-4810-619X surname: Xiao fullname: Xiao, Ling organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 2 givenname: Yu-qin surname: Cheng fullname: Cheng, Yu-qin organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 3 givenname: Wen-shuo orcidid: 0009-0002-5990-8745 surname: Ma fullname: Ma, Wen-shuo organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 4 givenname: Wen-fei surname: Zhu fullname: Zhu, Wen-fei organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 5 givenname: Jian-ping surname: Wu fullname: Wu, Jian-ping organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 6 givenname: Yu-fen surname: Meng fullname: Meng, Yu-fen organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 7 givenname: Li-yun surname: Shi fullname: Shi, Li-yun organization: School of Translational Medicine, Zhejiang Shuren University, Hangzhou, 310015, PR China – sequence: 8 givenname: Wei surname: Zhang fullname: Zhang, Wei organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 9 givenname: Lei surname: Chen fullname: Chen, Lei email: Newheart@189.cn organization: Department of Cardiothoracic Surgery, the Second Affiliated Hospital of Soochow University, Suzhou, 215004, PR China – sequence: 10 givenname: Chun surname: Cheng fullname: Cheng, Chun email: ccheng@ntu.edu.cn organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China – sequence: 11 givenname: Jun-feng surname: Zhang fullname: Zhang, Jun-feng email: zhangjunfeng419@njucm.edu.cn organization: School of Medical, Nanjing University of Chinese Medicine, Nanjing, 210023, PR China |
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| Keywords | Gastric intestinal metaplasia Huangqi Jianzhong decoction Gut microbiota‒thyroid axis Temperature‒tropism behavior Butyric acid |
| Language | English |
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| Snippet | •GIM rats exhibited gastro-thyroid comorbidities with cold-intolerant. HQJZ treatment restored low-temperature-tropism behavior, enriching fecal... Gastric intestinal metaplasia (GIM) is a crucial stage in the progression of gastric cancer. Huangqi Jianzhong decoction (HQJZ) has emerged as a leading... |
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| SubjectTerms | animal models Animals Bifidobacterium blood serum Butyric acid Butyric Acid - pharmacology cold Cold Temperature cold tolerance deoxycholic acid Disease Models, Animal Drugs, Chinese Herbal - pharmacology Gastric intestinal metaplasia gastric mucosa Gastrointestinal Microbiome - drug effects genes Gut microbiota‒thyroid axis Huangqi Jianzhong decoction Humans intestinal microorganisms intestines Male membrane potential metabolites metabolomics Metaplasia mitochondria mitochondrial membrane Oriental traditional medicine p-cresol Rats Rats, Sprague-Dawley reactive oxygen species salicylic acid stomach neoplasms sulfates Temperature‒tropism behavior therapeutics thyroid function Thyroid Gland - drug effects |
| Title | Huangqi Jianzhong decoction improves gastric intestinal metaplasia in rats by regulating the gut‒thyroid axis |
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