Measurement of liver collagen synthesis by heavy water labeling: Effects of profibrotic toxicants and antifibrotic interventions

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 292, Issue 6, 2007, Pages

  Gardner, James L ^a   Turner, Scott M ^a   Bautista, Abraham ^a   Lindwall, Glen ^a   Awada, Mohamad ^a   Hellerstein, Marc K ^b,c  

^a KINEMED INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Fibrogenesis; Hydroxyproline; In vivo; Strain differences

Indexed keywords

ALANINE; ANTIFIBROTIC AGENT; ATORVASTATIN; CARBON TETRACHLORIDE; COLLAGEN; DEUTERIUM OXIDE; DRINKING WATER; ENALAPRIL; GAMMA INTERFERON; GRISEOFULVIN; HYDROXYPROLINE; ROSIGLITAZONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; FIBROGENESIS; GAS CHROMATOGRAPHY; LIVER; MASS SPECTROMETRY; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; RADIOACTIVITY; RAT; RAT STRAIN; STATISTICAL SIGNIFICANCE;

ADMINISTRATION, ORAL; ALANINE; ANIMALS; CARBON TETRACHLORIDE; COLLAGEN; DEUTERIUM OXIDE; DRUG EVALUATION, PRECLINICAL; ENALAPRIL; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GRISEOFULVIN; HEPTANOIC ACIDS; HYDROXYPROLINE; INTERFERON TYPE II; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCIBILITY OF RESULTS; SPECIES SPECIFICITY; THIAZOLIDINEDIONES; TIME FACTORS;

EID: 34447540249     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00209.2006     Document Type: Article

References (44)

1. Babraj J, Cuthbertson DJ, Rickhuss P, Meier-Augenstein W, Smith K, Bohe J, Wolfe RR, Gibson JN, Adams C, Rennie MJ. Sequential extracts of human bone show differing collagen synthetic rates. Biochem Soc Trans 30: 61-65, 2002.
2. Baroni GS, D'Ambrosio L, Curto P, Casini A, Mancini R, Jezequel AM, Benedetti A. Interferon γ decreases hepatic stellate cell activation and extracellular matrix deposition in rat liver fibrosis. Hepatology 23: 1189-1199, 1996.
3. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 115: 209-218, 2005.
4. 13C-labeled algal protein used to determine amino acid essentiality in vivo. Proc Natl Acad Sci USA 88: 8091-8095, 1991.
5. Bishop JE, Rhodes S, Laurent GJ, Low RB, Stirewalt WS. Increased collagen synthesis and decreased collagen degradation in right ventricular hypertrophy induced by pressure overload. Cardiovasc Res 28: 1581-1585, 1994.
6. Bissell DM. Hepatic fibrosis as wound repair: a progress report. J Gastroenterol 33: 295-302, 1998.
7. Bowry VW, Ingold KU, Stocker R. Vitamin E in human low-density lipoprotein. When and how this antioxidant becomes a pro-oxidant. Biochem J 288: 341-344, 1992.
8. Bowry VW, Mohr D, Cleary J, Stocker R. Prevention of tocopherol-mediated peroxidation in ubiquinol-10-free human low density lipoprotein. J Biol Chem 270: 5756-5763, 1995.
9. Busch R, Kim YK, Neese RA, Schade-Serin V, Collins D, Awada M, Gardner JL, Beysen C, Marino MM, Misell LM, Hellerstein MK. Measurement of protein turnover rates by heavy water labeling of nonessential amino acids. Biochim Biophys Acta 1760: 730-744, 2006.
10. Chen JL, Peacock E, Samady W, Turner SM, Neese RA, Hellerstein MK, Murphy EJ. Physiologic and pharmacologic factors influencing glyceroneogenic contribution to triacylglyceride glycerol measured by mass isotopomer distribution analysis. J Biol Chem 280: 25396-25402, 2005.
11. Colley KJ, Baenziger JU. Identification of the post-translational modifications of the core-specific lectin. The core-specific lectin contains hydroxyproline, hydroxylysine, and glucosylgalactosylhydroxylysine residues. J Biol Chem 262: 10290-10295, 1987.
12. Eberlein M, Heusinger-Ribeiro J, Goppelt-Struebe M. Rho-dependent inhibition of the induction of connective tissue growth factor (CTGF) by HMG CoA reductase inhibitors (statins). Br J Pharmacol 133: 1172-1180, 2001.
13. Fanara P, Turner S, Busch R, Killion S, Awada M, Turner H, Mahsut A, Laprade KL, Stark JM, Hellerstein MK. In vivo measurement of microtubule dynamics using stable isotope labeling with heavy water. Effect of taxanes. J Biol Chem 279: 49940-49947, 2004.
14. Friedman SL. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J Biol Chem 275: 2247-2250, 2000.
15. Galli A, Crabb DW, Ceni E, Salzano R, Mello T, Svegliati-Baroni G, Ridolfi F, Trozzi L, Surrenti C, Casini A. Antidiabetic thiazolidinediones inhibit collagen synthesis and hepatic stellate cell activation in vivo and in vitro. Gastroenterology 122: 1924-1940, 2002.
16. Gant TW, Baus PR, Clothier B, Riley J, Davies R, Judah DJ, Edwards RE, George E, Greaves P, Smith AG. Gene expression profiles associated with inflammation, fibrosis, and cholestasis in mouse liver after griseofulvin. EHP Toxicogenomics 111: 37-43, 2003.
17. Guo G, Morrissey J, McCracken R, Tolley T, Liapis H, Klahr S. Contributions of angiotensin II and tumor necrosis factor-α to the development of renal fibrosis. Am J Physiol Renal Physiol 280: F777-F785, 2001.
18. Hellerstein MK. In vivo measurement of fluxes through metabolic pathways: the missing link in functional genomics and pharmaceutical research. Annu Rev Nutr 23: 379-402, 2003.
19. Hellerstein MK, Hoh RA, Hanley MB, Cesar D, Lee D, Neese RA, McCune JM. Subpopulations of long-lived and short-lived T cells in advanced HIV-1 infection. J Clin Invest 112: 956-966, 2003.
20. Hellerstein MK, Neese RA. Mass isotopomer distribution analysis at eight years: theoretical, analytic, and experimental considerations. Am J Physiol Endocrinol Metab 276: E1146-E1170, 1999.
21. 2O incorporation into non-essential amino acids (NEAA) and application of mass isotopomer distribution analysis (MIDA) (Abstract). FASEB J 16: A256, 2002.
22. Koletzko B, Sauerwald T, Demmelmair H. Safety of stable isotope use. Eur J Pediatr 156, Suppl 1: S12-S17, 1997.
23. Mays C, Rosenberry TL. Characterization of pepsin-resistant collagenlike tail subunit fragments of 18S and 14S acetylcholinesterase from Electrophorus electricus. Biochemistry 20: 2810-2817, 1981.
24. Mays PK, McAnulty RJ, Laurent GJ. Age-related changes in lung collagen metabolism. A role for degradation in regulating lung collagen production. Am Rev Respir Dis 140: 410-416, 1989.
25. Messmer BT, Messmer D, Allen SL, Kolitz JE, Kudalkar P, Cesar D, Murphy EJ, Koduru P, Ferrarini M, Zupo S, Cutrona G, Damle RN, Wasil T, Rai KR, Hellerstein MK, Chiorazzi N. In vivo measurements document the dynamic cellular kinetics of chronic lymphocytic leukemia B cells. J Clin Invest 115: 755-764, 2005.
26. 2O labeling of the deoxyribose moiety of DNA. Proc Natl Acad Sci USA 99: 15345-15350, 2002.
27. Pahor M, Bernabei R, Sgadari A, Gambassi G Jr, Lo Giudice P, Pacifici L, Ramacci M, Lagrasta C, Olivetti G, Carbonin P. Enalapril prevents cardiac fibrosis and arrhythmias in hypertensive rats. Hypertension 18: 148-157, 1991.
28. Parks EJ, Krauss RM, Christiansen MP, Neese RA, Hellerstein MK. Effects of a low-fat, high-carbohydrate diet on VLDL-triglyceride assembly, production, and clearance. J Clin Invest 104: 1087-1096, 1999.
29. Patthy L. Is lung surfactant protein a lectin-collagen hybrid? Nature 325: 490, 1987.
30. Porter RR, Reid KB. The biochemistry of complement. Nature 275: 699-704, 1978.
31. Rosenbloom J. Elastin: an overview. Methods Enzymol 144: 172-196, 1987.
32. Sato K, Guo YH, Feng J, Sugiyama S, Ichinomiya M, Tsukamasa Y, Minegishi Y, Sakata A, Komiya K, Yamasaki Y, Nakamura Y, Ohtsuki K, Kawabata M. Direct fractionation of proteins in particle-containing feedstocks by a filter paper pieces-based DEAE-cellulose column chromatography. Rapid, robust and low-cost capturing procedure for protein. J Chromatogr A 811: 69-76, 1998.
33. Sato K, Tanahashi-Shiina T, Jun F, Watanabe-Kawamura A, Ichinomiya M, Minegishi Y, Tsukamasa Y, Nakamura Y, Kawabata M, Ohtsuki K. Simple and rapid chromatographic purification of type V collagen from a pepsin digest of porcine intestinal connective tissue, an unmanageable starting material for conventional column chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 790: 277-283, 2003.
34. Schacker TW, Nguyen PL, Beilman GJ, Wolinsky S, Larson M, Reilly C, Haase AT. Collagen deposition in HIV-1 infected lymphatic tissues and T cell homeostasis. J Clin Invest 110: 1133-1139, 2002.
35. Schuppan D, Porov Y. Hepatic fibrosis: from bench to bedside. J Gastroenterol Hepatol 17, Suppl 3: S300-S305, 2002.
36. Shi Z, Wakil AE, Rockey DC. Strain-specific differences in mouse hepatic wound healing are mediated by divergent T helper cytokine responses. Proc Natl Acad Sci USA 94: 10663-10668, 1997.
37. 2O. Am J Physiol Endocrinol Metab 286: E577-E588, 2004.
38. Tamayo RP, Montfort I, Pardo A. What controls collagen resorption in vivo? Med Hypotheses 6: 711-726, 1980.
39. Tan A, Levrey H, Dahm C, Polunovsky VA, Rubins J, Bitterman PB. Lovastatin induces fibroblast apoptosis in vitro and in vivo. A possible therapy for fibroproliferative disorders. Am J Respir Crit Care Med 159:220-227, 1999.
40. Turner SM, Hellerstein MK. Emerging applications of kinetic biomarkers in preclinical and clinical drug development. Curr Opin Drug Discov Devel 8: 115-126, 2005.
41. 2O incorporation into the glycerol moiety and application of MIDA. Am J Physiol Endocrinol Metab 285: E790-E803, 2003.
42. Vater CA, Harris ED Jr, Siegel RC. Native cross-links in collagen fibrils induce resistance to human synovial collagenase. Biochem J 181: 639-645, 1979.
43. Watts KL, Spiteri MA. Connective tissue growth factor expression and induction by transforming growth factor-β is abrogated by simvastatin via a Rho signaling mechanism. Am J Physiol Lung Cell Mol Physiol 287: L1323-L1332, 2004.
44. Witting PK, Bowry VW, Stocker R. Inverse deuterium kinetic isotope effect for peroxidation in human low-density lipoprotein (LDL): a simple test for tocopherol-mediated peroxidation of LDL lipids. FEBS Lett 375: 45-49, 1995.