Tumor-derived IL-6 and trans-signaling among tumor, fat, and muscle mediate pancreatic cancer cachexia

Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These phenocopied donor weight loss. Furthermore, muscle wasting correlated with mortality and murine IL-6, and human IL-6 associated with the grea...

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Veröffentlicht in:The Journal of experimental medicine Jg. 218; H. 6
Hauptverfasser: Rupert, Joseph E, Narasimhan, Ashok, Jengelley, Daenique H A, Jiang, Yanlin, Liu, Jianguo, Au, Ernie, Silverman, Libbie M, Sandusky, George, Bonetto, Andrea, Cao, Sha, Lu, Xiaoyu, O'Connell, Thomas M, Liu, Yunlong, Koniaris, Leonidas G, Zimmers, Teresa A
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Veröffentlicht: United States 07.06.2021
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Abstract Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These phenocopied donor weight loss. Furthermore, muscle wasting correlated with mortality and murine IL-6, and human IL-6 associated with the greatest murine cachexia. In cell culture and mice, PDAC cells elicited adipocyte IL-6 expression and IL-6 plus IL-6 receptor (IL6R) in myocytes and blood. PDAC induced adipocyte lipolysis and muscle steatosis, dysmetabolism, and wasting. Depletion of IL-6 from malignant cells halved adipose wasting and abolished myosteatosis, dysmetabolism, and atrophy. In culture, adipocyte lipolysis required soluble (s)IL6R, while IL-6, sIL6R, or palmitate induced myotube atrophy. PDAC cells activated adipocytes to induce myotube wasting and activated myotubes to induce adipocyte lipolysis. Thus, PDAC cachexia results from tissue crosstalk via a feed-forward, IL-6 trans-signaling loop. Malignant cells signal via IL-6 to muscle and fat, muscle to fat via sIL6R, and fat to muscle via lipids and IL-6, all targetable mechanisms for treatment of cachexia.
AbstractList Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These phenocopied donor weight loss. Furthermore, muscle wasting correlated with mortality and murine IL-6, and human IL-6 associated with the greatest murine cachexia. In cell culture and mice, PDAC cells elicited adipocyte IL-6 expression and IL-6 plus IL-6 receptor (IL6R) in myocytes and blood. PDAC induced adipocyte lipolysis and muscle steatosis, dysmetabolism, and wasting. Depletion of IL-6 from malignant cells halved adipose wasting and abolished myosteatosis, dysmetabolism, and atrophy. In culture, adipocyte lipolysis required soluble (s)IL6R, while IL-6, sIL6R, or palmitate induced myotube atrophy. PDAC cells activated adipocytes to induce myotube wasting and activated myotubes to induce adipocyte lipolysis. Thus, PDAC cachexia results from tissue crosstalk via a feed-forward, IL-6 trans-signaling loop. Malignant cells signal via IL-6 to muscle and fat, muscle to fat via sIL6R, and fat to muscle via lipids and IL-6, all targetable mechanisms for treatment of cachexia.Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These phenocopied donor weight loss. Furthermore, muscle wasting correlated with mortality and murine IL-6, and human IL-6 associated with the greatest murine cachexia. In cell culture and mice, PDAC cells elicited adipocyte IL-6 expression and IL-6 plus IL-6 receptor (IL6R) in myocytes and blood. PDAC induced adipocyte lipolysis and muscle steatosis, dysmetabolism, and wasting. Depletion of IL-6 from malignant cells halved adipose wasting and abolished myosteatosis, dysmetabolism, and atrophy. In culture, adipocyte lipolysis required soluble (s)IL6R, while IL-6, sIL6R, or palmitate induced myotube atrophy. PDAC cells activated adipocytes to induce myotube wasting and activated myotubes to induce adipocyte lipolysis. Thus, PDAC cachexia results from tissue crosstalk via a feed-forward, IL-6 trans-signaling loop. Malignant cells signal via IL-6 to muscle and fat, muscle to fat via sIL6R, and fat to muscle via lipids and IL-6, all targetable mechanisms for treatment of cachexia.
Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These phenocopied donor weight loss. Furthermore, muscle wasting correlated with mortality and murine IL-6, and human IL-6 associated with the greatest murine cachexia. In cell culture and mice, PDAC cells elicited adipocyte IL-6 expression and IL-6 plus IL-6 receptor (IL6R) in myocytes and blood. PDAC induced adipocyte lipolysis and muscle steatosis, dysmetabolism, and wasting. Depletion of IL-6 from malignant cells halved adipose wasting and abolished myosteatosis, dysmetabolism, and atrophy. In culture, adipocyte lipolysis required soluble (s)IL6R, while IL-6, sIL6R, or palmitate induced myotube atrophy. PDAC cells activated adipocytes to induce myotube wasting and activated myotubes to induce adipocyte lipolysis. Thus, PDAC cachexia results from tissue crosstalk via a feed-forward, IL-6 trans-signaling loop. Malignant cells signal via IL-6 to muscle and fat, muscle to fat via sIL6R, and fat to muscle via lipids and IL-6, all targetable mechanisms for treatment of cachexia.
Author Bonetto, Andrea
Liu, Jianguo
O'Connell, Thomas M
Narasimhan, Ashok
Sandusky, George
Au, Ernie
Koniaris, Leonidas G
Rupert, Joseph E
Liu, Yunlong
Silverman, Libbie M
Cao, Sha
Lu, Xiaoyu
Jengelley, Daenique H A
Jiang, Yanlin
Zimmers, Teresa A
Author_xml – sequence: 1
  givenname: Joseph E
  surname: Rupert
  fullname: Rupert, Joseph E
  organization: Department of Biochemistry, Indiana University School of Medicine, Indianapolis, IN
– sequence: 2
  givenname: Ashok
  surname: Narasimhan
  fullname: Narasimhan, Ashok
  organization: Department of Surgery, Indiana University School of Medicine, Indianapolis, IN
– sequence: 3
  givenname: Daenique H A
  surname: Jengelley
  fullname: Jengelley, Daenique H A
  organization: Department of Biochemistry, Indiana University School of Medicine, Indianapolis, IN
– sequence: 4
  givenname: Yanlin
  surname: Jiang
  fullname: Jiang, Yanlin
  organization: Department of Surgery, Indiana University School of Medicine, Indianapolis, IN
– sequence: 5
  givenname: Jianguo
  surname: Liu
  fullname: Liu, Jianguo
  organization: Department of Surgery, Indiana University School of Medicine, Indianapolis, IN
– sequence: 6
  givenname: Ernie
  surname: Au
  fullname: Au, Ernie
  organization: Department of Biochemistry, Indiana University School of Medicine, Indianapolis, IN
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  givenname: Libbie M
  surname: Silverman
  fullname: Silverman, Libbie M
  organization: Department of Surgery, Indiana University School of Medicine, Indianapolis, IN
– sequence: 8
  givenname: George
  surname: Sandusky
  fullname: Sandusky, George
  organization: Department of Pathology, Indiana University School of Medicine, Indianapolis, IN
– sequence: 9
  givenname: Andrea
  surname: Bonetto
  fullname: Bonetto, Andrea
  organization: Indiana Center for Musculoskeletal Health, Indiana University School of Medicine, Indianapolis, IN
– sequence: 10
  givenname: Sha
  surname: Cao
  fullname: Cao, Sha
  organization: Department of Biostatistics, Indiana University School of Medicine, Indianapolis, IN
– sequence: 11
  givenname: Xiaoyu
  surname: Lu
  fullname: Lu, Xiaoyu
  organization: Department of Biostatistics, Indiana University School of Medicine, Indianapolis, IN
– sequence: 12
  givenname: Thomas M
  surname: O'Connell
  fullname: O'Connell, Thomas M
  organization: Indiana Center for Musculoskeletal Health, Indiana University School of Medicine, Indianapolis, IN
– sequence: 13
  givenname: Yunlong
  surname: Liu
  fullname: Liu, Yunlong
  organization: Center for Computational Biology and Bioinformatics, Indiana University School of Medicine, Indianapolis, IN
– sequence: 14
  givenname: Leonidas G
  surname: Koniaris
  fullname: Koniaris, Leonidas G
  organization: Indiana Center for Musculoskeletal Health, Indiana University School of Medicine, Indianapolis, IN
– sequence: 15
  givenname: Teresa A
  surname: Zimmers
  fullname: Zimmers, Teresa A
  organization: Richard L. Roudebush Veterans Administration Medical Center, Indianapolis, IN
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33851955$$D View this record in MEDLINE/PubMed
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Snippet Most patients with pancreatic adenocarcinoma (PDAC) suffer cachexia; some do not. To model heterogeneity, we used patient-derived orthotopic xenografts. These...
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SubjectTerms 3T3 Cells
Adenocarcinoma - metabolism
Adenocarcinoma - pathology
Adipocytes - metabolism
Adipose Tissue - metabolism
Adipose Tissue - pathology
Aged
Aged, 80 and over
Animals
Cachexia - metabolism
Cachexia - pathology
Cell Line
Cell Line, Tumor
Disease Models, Animal
Female
Humans
Interleukin-6 - metabolism
Lipolysis - physiology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Muscle Fibers, Skeletal - metabolism
Muscle Fibers, Skeletal - pathology
Muscle, Skeletal - metabolism
Muscle, Skeletal - pathology
Pancreatic Neoplasms - metabolism
Pancreatic Neoplasms - pathology
Signal Transduction - physiology
Title Tumor-derived IL-6 and trans-signaling among tumor, fat, and muscle mediate pancreatic cancer cachexia
URI https://www.ncbi.nlm.nih.gov/pubmed/33851955
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