Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease
Abstract Background The growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis modulates critical metabolic pathways; however, little is known regarding effects of augmenting pulsatile GH secretion on immune function in humans. This study used proteomics and gene set enrichment analysis to as...
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| Veröffentlicht in: | Clinical infectious diseases 2021-08, Vol.73 (4), p.621-630 |
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| creator | Stanley, Takara L Fourman, Lindsay T Wong, Lai Ping Sadreyev, Ruslan Billingsley, James M Feldpausch, Meghan N Zheng, Isabel Pan, Chelsea S Boutin, Autumn Lee, Hang Corey, Kathleen E Torriani, Martin Kleiner, David E Chung, Raymond T Hadigan, Colleen M Grinspoon, Steven K |
| description | Abstract
Background
The growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis modulates critical metabolic pathways; however, little is known regarding effects of augmenting pulsatile GH secretion on immune function in humans. This study used proteomics and gene set enrichment analysis to assess effects of a GH releasing hormone (GHRH) analog, tesamorelin, on circulating immune markers and liver tissue in people with human immunodeficiency virus (HIV) (PWH) and nonalcoholic fatty liver disease (NAFLD).
Methods
92 biomarkers associated with immunity, chemotaxis, and metabolism were measured in plasma samples from 61 PWH with NAFLD who participated in a double-blind, randomized trial of tesamorelin versus placebo for 12 months. Gene set enrichment analysis was performed on serial liver biopsies targeted to immune pathways.
Results
Tesamorelin, compared to placebo, decreased interconnected proteins related to cytotoxic T-cell and monocyte activation. Circulating concentrations of 13 proteins were significantly decreased, and no proteins increased, by tesamorelin. These included 4 chemokines (CCL3, CCL4, CCL13 [MCP4], IL8 [CXCL8]), 2 cytokines (IL-10 and CSF-1), and 4 T-cell associated molecules (CD8A, CRTAM, GZMA, ADGRG1), as well as ARG1, Gal-9, and HGF. Network analysis indicated close interaction among the gene pathways responsible for these proteins, with imputational analyses suggesting down-regulation of a closely related cluster of immune pathways. Targeted transcriptomics using liver tissue confirmed a significant end-organ signal of down-regulated immune activation pathways.
Conclusions
Long-term treatment with a GHRH analog reduced markers of T-cell and monocyte/macrophage activity, suggesting that augmentation of the GH axis may ameliorate immune activation in an HIV population with metabolic dysregulation, systemic and end organ inflammation.
Clinical Trials Registration. NCT02196831.
Treatment with a growth hormone releasing hormone analog in people with human immunodeficiency virus and nonalcoholic fatty liver disease decreased circulating proteins associated with immune activation pathways. Gene set enrichment analysis of RNA-seq in liver confirmed down-regulation of end-organ immune activation pathways. |
| doi_str_mv | 10.1093/cid/ciab019 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_proquest_miscellaneous_2513242975</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><oup_id>10.1093/cid/ciab019</oup_id><sourcerecordid>2513242975</sourcerecordid><originalsourceid>FETCH-LOGICAL-c412t-5b0bc95a6c5ade5f92021862fb3bbfc87807e0305c7cd4dff51bbec16b3f8cfb3</originalsourceid><addsrcrecordid>eNp9kU2PEyEcxidG477oybvhZEzMKC9lhrmYbOrutknVjVGvBBjYogxUYNr0O-6Hkkm7m_XigUB4fs_DnzxV9QrB9wh25IOyfVlCQtQ9qU4RJW3d0A49LWdIWT1jhJ1UZyn9ghAhBunz6oQQRnGL4Wl1dx3DLq_BIsQheA2-aadFsv720U0_Kp3A3EY1OpEn7bOIv3VMIBiwHIaxUBcq220RgwfWgxsRhXPagZ0t2ZfGaJUL7cFCbwqk7l03Iq93Yp8mz9L3dmv7Ubh0sC2WP2vrJ-uUKnwPvgQvnArr4ErElch5D1Z2qyP4ZFOZWr-onpli1y-P-3n14-ry-3xRr75eL-cXq1rNEM41lVCqjopGUdFrajoMMWINNpJIaRRrGWw1JJCqVvWz3hiKpNQKNZIYpgp1Xn085G5GOeheaZ_Lf_km2kHEPQ_C8n8Vb9f8Nmw5I03DMCsBb48BMfwZdcp8sElp54TXYUwcU0TwDHctLei7A6piSClq8_AMgnzqn5f--bH_Qr9-PNkDe194Ad4cgDBu_pv0F9bUwHY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2513242975</pqid></control><display><type>article</type><title>Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease</title><source>MEDLINE</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><source>Alma/SFX Local Collection</source><creator>Stanley, Takara L ; Fourman, Lindsay T ; Wong, Lai Ping ; Sadreyev, Ruslan ; Billingsley, James M ; Feldpausch, Meghan N ; Zheng, Isabel ; Pan, Chelsea S ; Boutin, Autumn ; Lee, Hang ; Corey, Kathleen E ; Torriani, Martin ; Kleiner, David E ; Chung, Raymond T ; Hadigan, Colleen M ; Grinspoon, Steven K</creator><creatorcontrib>Stanley, Takara L ; Fourman, Lindsay T ; Wong, Lai Ping ; Sadreyev, Ruslan ; Billingsley, James M ; Feldpausch, Meghan N ; Zheng, Isabel ; Pan, Chelsea S ; Boutin, Autumn ; Lee, Hang ; Corey, Kathleen E ; Torriani, Martin ; Kleiner, David E ; Chung, Raymond T ; Hadigan, Colleen M ; Grinspoon, Steven K</creatorcontrib><description>Abstract
Background
The growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis modulates critical metabolic pathways; however, little is known regarding effects of augmenting pulsatile GH secretion on immune function in humans. This study used proteomics and gene set enrichment analysis to assess effects of a GH releasing hormone (GHRH) analog, tesamorelin, on circulating immune markers and liver tissue in people with human immunodeficiency virus (HIV) (PWH) and nonalcoholic fatty liver disease (NAFLD).
Methods
92 biomarkers associated with immunity, chemotaxis, and metabolism were measured in plasma samples from 61 PWH with NAFLD who participated in a double-blind, randomized trial of tesamorelin versus placebo for 12 months. Gene set enrichment analysis was performed on serial liver biopsies targeted to immune pathways.
Results
Tesamorelin, compared to placebo, decreased interconnected proteins related to cytotoxic T-cell and monocyte activation. Circulating concentrations of 13 proteins were significantly decreased, and no proteins increased, by tesamorelin. These included 4 chemokines (CCL3, CCL4, CCL13 [MCP4], IL8 [CXCL8]), 2 cytokines (IL-10 and CSF-1), and 4 T-cell associated molecules (CD8A, CRTAM, GZMA, ADGRG1), as well as ARG1, Gal-9, and HGF. Network analysis indicated close interaction among the gene pathways responsible for these proteins, with imputational analyses suggesting down-regulation of a closely related cluster of immune pathways. Targeted transcriptomics using liver tissue confirmed a significant end-organ signal of down-regulated immune activation pathways.
Conclusions
Long-term treatment with a GHRH analog reduced markers of T-cell and monocyte/macrophage activity, suggesting that augmentation of the GH axis may ameliorate immune activation in an HIV population with metabolic dysregulation, systemic and end organ inflammation.
Clinical Trials Registration. NCT02196831.
Treatment with a growth hormone releasing hormone analog in people with human immunodeficiency virus and nonalcoholic fatty liver disease decreased circulating proteins associated with immune activation pathways. Gene set enrichment analysis of RNA-seq in liver confirmed down-regulation of end-organ immune activation pathways.</description><identifier>ISSN: 1058-4838</identifier><identifier>EISSN: 1537-6591</identifier><identifier>DOI: 10.1093/cid/ciab019</identifier><identifier>PMID: 33852720</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Biomarkers ; Double-Blind Method ; Growth Hormone-Releasing Hormone ; HIV Infections - complications ; HIV Infections - drug therapy ; Humans ; Major and Commentaries ; Non-alcoholic Fatty Liver Disease - drug therapy</subject><ispartof>Clinical infectious diseases, 2021-08, Vol.73 (4), p.621-630</ispartof><rights>The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com. 2021</rights><rights>The Author(s) 2021. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412t-5b0bc95a6c5ade5f92021862fb3bbfc87807e0305c7cd4dff51bbec16b3f8cfb3</citedby><cites>FETCH-LOGICAL-c412t-5b0bc95a6c5ade5f92021862fb3bbfc87807e0305c7cd4dff51bbec16b3f8cfb3</cites><orcidid>0000-0002-2336-2958</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,1584,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33852720$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Stanley, Takara L</creatorcontrib><creatorcontrib>Fourman, Lindsay T</creatorcontrib><creatorcontrib>Wong, Lai Ping</creatorcontrib><creatorcontrib>Sadreyev, Ruslan</creatorcontrib><creatorcontrib>Billingsley, James M</creatorcontrib><creatorcontrib>Feldpausch, Meghan N</creatorcontrib><creatorcontrib>Zheng, Isabel</creatorcontrib><creatorcontrib>Pan, Chelsea S</creatorcontrib><creatorcontrib>Boutin, Autumn</creatorcontrib><creatorcontrib>Lee, Hang</creatorcontrib><creatorcontrib>Corey, Kathleen E</creatorcontrib><creatorcontrib>Torriani, Martin</creatorcontrib><creatorcontrib>Kleiner, David E</creatorcontrib><creatorcontrib>Chung, Raymond T</creatorcontrib><creatorcontrib>Hadigan, Colleen M</creatorcontrib><creatorcontrib>Grinspoon, Steven K</creatorcontrib><title>Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease</title><title>Clinical infectious diseases</title><addtitle>Clin Infect Dis</addtitle><description>Abstract
Background
The growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis modulates critical metabolic pathways; however, little is known regarding effects of augmenting pulsatile GH secretion on immune function in humans. This study used proteomics and gene set enrichment analysis to assess effects of a GH releasing hormone (GHRH) analog, tesamorelin, on circulating immune markers and liver tissue in people with human immunodeficiency virus (HIV) (PWH) and nonalcoholic fatty liver disease (NAFLD).
Methods
92 biomarkers associated with immunity, chemotaxis, and metabolism were measured in plasma samples from 61 PWH with NAFLD who participated in a double-blind, randomized trial of tesamorelin versus placebo for 12 months. Gene set enrichment analysis was performed on serial liver biopsies targeted to immune pathways.
Results
Tesamorelin, compared to placebo, decreased interconnected proteins related to cytotoxic T-cell and monocyte activation. Circulating concentrations of 13 proteins were significantly decreased, and no proteins increased, by tesamorelin. These included 4 chemokines (CCL3, CCL4, CCL13 [MCP4], IL8 [CXCL8]), 2 cytokines (IL-10 and CSF-1), and 4 T-cell associated molecules (CD8A, CRTAM, GZMA, ADGRG1), as well as ARG1, Gal-9, and HGF. Network analysis indicated close interaction among the gene pathways responsible for these proteins, with imputational analyses suggesting down-regulation of a closely related cluster of immune pathways. Targeted transcriptomics using liver tissue confirmed a significant end-organ signal of down-regulated immune activation pathways.
Conclusions
Long-term treatment with a GHRH analog reduced markers of T-cell and monocyte/macrophage activity, suggesting that augmentation of the GH axis may ameliorate immune activation in an HIV population with metabolic dysregulation, systemic and end organ inflammation.
Clinical Trials Registration. NCT02196831.
Treatment with a growth hormone releasing hormone analog in people with human immunodeficiency virus and nonalcoholic fatty liver disease decreased circulating proteins associated with immune activation pathways. Gene set enrichment analysis of RNA-seq in liver confirmed down-regulation of end-organ immune activation pathways.</description><subject>Biomarkers</subject><subject>Double-Blind Method</subject><subject>Growth Hormone-Releasing Hormone</subject><subject>HIV Infections - complications</subject><subject>HIV Infections - drug therapy</subject><subject>Humans</subject><subject>Major and Commentaries</subject><subject>Non-alcoholic Fatty Liver Disease - drug therapy</subject><issn>1058-4838</issn><issn>1537-6591</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU2PEyEcxidG477oybvhZEzMKC9lhrmYbOrutknVjVGvBBjYogxUYNr0O-6Hkkm7m_XigUB4fs_DnzxV9QrB9wh25IOyfVlCQtQ9qU4RJW3d0A49LWdIWT1jhJ1UZyn9ghAhBunz6oQQRnGL4Wl1dx3DLq_BIsQheA2-aadFsv720U0_Kp3A3EY1OpEn7bOIv3VMIBiwHIaxUBcq220RgwfWgxsRhXPagZ0t2ZfGaJUL7cFCbwqk7l03Iq93Yp8mz9L3dmv7Ubh0sC2WP2vrJ-uUKnwPvgQvnArr4ErElch5D1Z2qyP4ZFOZWr-onpli1y-P-3n14-ry-3xRr75eL-cXq1rNEM41lVCqjopGUdFrajoMMWINNpJIaRRrGWw1JJCqVvWz3hiKpNQKNZIYpgp1Xn085G5GOeheaZ_Lf_km2kHEPQ_C8n8Vb9f8Nmw5I03DMCsBb48BMfwZdcp8sElp54TXYUwcU0TwDHctLei7A6piSClq8_AMgnzqn5f--bH_Qr9-PNkDe194Ad4cgDBu_pv0F9bUwHY</recordid><startdate>20210816</startdate><enddate>20210816</enddate><creator>Stanley, Takara L</creator><creator>Fourman, Lindsay T</creator><creator>Wong, Lai Ping</creator><creator>Sadreyev, Ruslan</creator><creator>Billingsley, James M</creator><creator>Feldpausch, Meghan N</creator><creator>Zheng, Isabel</creator><creator>Pan, Chelsea S</creator><creator>Boutin, Autumn</creator><creator>Lee, Hang</creator><creator>Corey, Kathleen E</creator><creator>Torriani, Martin</creator><creator>Kleiner, David E</creator><creator>Chung, Raymond T</creator><creator>Hadigan, Colleen M</creator><creator>Grinspoon, Steven K</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-2336-2958</orcidid></search><sort><creationdate>20210816</creationdate><title>Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease</title><author>Stanley, Takara L ; Fourman, Lindsay T ; Wong, Lai Ping ; Sadreyev, Ruslan ; Billingsley, James M ; Feldpausch, Meghan N ; Zheng, Isabel ; Pan, Chelsea S ; Boutin, Autumn ; Lee, Hang ; Corey, Kathleen E ; Torriani, Martin ; Kleiner, David E ; Chung, Raymond T ; Hadigan, Colleen M ; Grinspoon, Steven K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412t-5b0bc95a6c5ade5f92021862fb3bbfc87807e0305c7cd4dff51bbec16b3f8cfb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Biomarkers</topic><topic>Double-Blind Method</topic><topic>Growth Hormone-Releasing Hormone</topic><topic>HIV Infections - complications</topic><topic>HIV Infections - drug therapy</topic><topic>Humans</topic><topic>Major and Commentaries</topic><topic>Non-alcoholic Fatty Liver Disease - drug therapy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Stanley, Takara L</creatorcontrib><creatorcontrib>Fourman, Lindsay T</creatorcontrib><creatorcontrib>Wong, Lai Ping</creatorcontrib><creatorcontrib>Sadreyev, Ruslan</creatorcontrib><creatorcontrib>Billingsley, James M</creatorcontrib><creatorcontrib>Feldpausch, Meghan N</creatorcontrib><creatorcontrib>Zheng, Isabel</creatorcontrib><creatorcontrib>Pan, Chelsea S</creatorcontrib><creatorcontrib>Boutin, Autumn</creatorcontrib><creatorcontrib>Lee, Hang</creatorcontrib><creatorcontrib>Corey, Kathleen E</creatorcontrib><creatorcontrib>Torriani, Martin</creatorcontrib><creatorcontrib>Kleiner, David E</creatorcontrib><creatorcontrib>Chung, Raymond T</creatorcontrib><creatorcontrib>Hadigan, Colleen M</creatorcontrib><creatorcontrib>Grinspoon, Steven K</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Clinical infectious diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Stanley, Takara L</au><au>Fourman, Lindsay T</au><au>Wong, Lai Ping</au><au>Sadreyev, Ruslan</au><au>Billingsley, James M</au><au>Feldpausch, Meghan N</au><au>Zheng, Isabel</au><au>Pan, Chelsea S</au><au>Boutin, Autumn</au><au>Lee, Hang</au><au>Corey, Kathleen E</au><au>Torriani, Martin</au><au>Kleiner, David E</au><au>Chung, Raymond T</au><au>Hadigan, Colleen M</au><au>Grinspoon, Steven K</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease</atitle><jtitle>Clinical infectious diseases</jtitle><addtitle>Clin Infect Dis</addtitle><date>2021-08-16</date><risdate>2021</risdate><volume>73</volume><issue>4</issue><spage>621</spage><epage>630</epage><pages>621-630</pages><issn>1058-4838</issn><eissn>1537-6591</eissn><abstract>Abstract
Background
The growth hormone (GH)/insulin-like growth factor-1 (IGF-1) axis modulates critical metabolic pathways; however, little is known regarding effects of augmenting pulsatile GH secretion on immune function in humans. This study used proteomics and gene set enrichment analysis to assess effects of a GH releasing hormone (GHRH) analog, tesamorelin, on circulating immune markers and liver tissue in people with human immunodeficiency virus (HIV) (PWH) and nonalcoholic fatty liver disease (NAFLD).
Methods
92 biomarkers associated with immunity, chemotaxis, and metabolism were measured in plasma samples from 61 PWH with NAFLD who participated in a double-blind, randomized trial of tesamorelin versus placebo for 12 months. Gene set enrichment analysis was performed on serial liver biopsies targeted to immune pathways.
Results
Tesamorelin, compared to placebo, decreased interconnected proteins related to cytotoxic T-cell and monocyte activation. Circulating concentrations of 13 proteins were significantly decreased, and no proteins increased, by tesamorelin. These included 4 chemokines (CCL3, CCL4, CCL13 [MCP4], IL8 [CXCL8]), 2 cytokines (IL-10 and CSF-1), and 4 T-cell associated molecules (CD8A, CRTAM, GZMA, ADGRG1), as well as ARG1, Gal-9, and HGF. Network analysis indicated close interaction among the gene pathways responsible for these proteins, with imputational analyses suggesting down-regulation of a closely related cluster of immune pathways. Targeted transcriptomics using liver tissue confirmed a significant end-organ signal of down-regulated immune activation pathways.
Conclusions
Long-term treatment with a GHRH analog reduced markers of T-cell and monocyte/macrophage activity, suggesting that augmentation of the GH axis may ameliorate immune activation in an HIV population with metabolic dysregulation, systemic and end organ inflammation.
Clinical Trials Registration. NCT02196831.
Treatment with a growth hormone releasing hormone analog in people with human immunodeficiency virus and nonalcoholic fatty liver disease decreased circulating proteins associated with immune activation pathways. Gene set enrichment analysis of RNA-seq in liver confirmed down-regulation of end-organ immune activation pathways.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>33852720</pmid><doi>10.1093/cid/ciab019</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-2336-2958</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1058-4838 |
| ispartof | Clinical infectious diseases, 2021-08, Vol.73 (4), p.621-630 |
| issn | 1058-4838 1537-6591 |
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| source | MEDLINE; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals; Alma/SFX Local Collection |
| subjects | Biomarkers Double-Blind Method Growth Hormone-Releasing Hormone HIV Infections - complications HIV Infections - drug therapy Humans Major and Commentaries Non-alcoholic Fatty Liver Disease - drug therapy |
| title | Growth Hormone Releasing Hormone Reduces Circulating Markers of Immune Activation in Parallel with Effects on Hepatic Immune Pathways in Individuals with HIV-infection and Nonalcoholic Fatty Liver Disease |
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