Role for Krüppel-Like Transcription Factor 11 in Mesenchymal Cell Function and Fibrosis

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Mathison, Angela ^a,b   Grzenda, Adrienne ^a,b   Lomberk, Gwen ^a,b   Velez, Gabriel ^a   Buttar, Navtej ^b   Tietz, Pamela ^b   Hendrickson, Helen ^b   Liebl, Ann ^a,b   Xiong, Yuning Y ^a,b   Gores, Gregory ^b   Fernandez Zapico, Martin ^c   LaRusso, Nicholas F ^b   Faubion, William ^a,b   Shah, Vijay H ^b   Urrutia, Raul ^a,b  

^a GIH Division   (United States)

^b MAYO CLINIC   (United States)

^c Schulze Center for Novel Therapeutics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; COLLAGEN 1A2; COLLAGEN FIBRIL; HETEROCHROMATIN PROTEIN 1; KRUPPEL LIKE FACTOR 10; KRUPPEL LIKE FACTOR 11; MATRIX METALLOPROTEINASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EPIGENETICS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; FIBROSIS; GENE EXPRESSION; GENE SILENCING; IN VIVO STUDY; LIVER INJURY; MALE; MESENCHYME CELL; MOUSE; NONHUMAN; PROTEIN FUNCTION;

ANIMALS; CARBON TETRACHLORIDE; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; COLLAGEN TYPE I; DNA-BINDING PROTEINS; DRUG-INDUCED LIVER INJURY; EXTRACELLULAR MATRIX; FIBROSIS; GENE EXPRESSION REGULATION; GENE SILENCING; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; MESENCHYMAL STROMAL CELLS; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84884265835     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075311     Document Type: Article

References (37)

1. Botella LM, Sánchez-Elsner T, Sanz-Rodriguez F, Kojima S, Shimada J, et al. (2002) Transcriptional activation of endoglin and transforming growth factor-beta signaling components by cooperative interaction between Sp1 and KLF6: their potential role in the response to vascular injury. Blood 100: 4001-4010. PubMed: 12433697.
2. Botella LM, Sanz-Rodriguez F, Komi Y, Fernandez LA, Varela E, et al. (2009) TGF-beta regulates the expression of transcription factor KLF6 and its splice variants and promotes co-operative transactivation of common target genes through a Smad3-Sp1-KLF6 interaction. Biochem J 419: 485-495. PubMed: 19076057.
3. Miele L, Beale G, Patman G, Nobili V, Leathart J, et al. (2008) The Kruppel-like factor 6 genotype is associated with fibrosis in nonalcoholic fatty liver disease. Gastroenterology 135: 282-291. PubMed: 18515091.
4. Ratziu V, Lalazar A, Wong L, Dang Q, Collins C, et al. (1998) Zf9, a Kruppel-like transcription factor up-regulated in vivo during early hepatic fibrosis. Proc Natl Acad Sci U S A 95: 9500-9505. PubMed: 9689109.
5. Stärkel P, Sempoux C, Leclercq I, Herin M, Deby C, et al. (2003) Oxidative stress, KLF6 and transforming growth factor-beta up-regulation differentiate non-alcoholic steatohepatitis progressing to fibrosis from uncomplicated steatosis in rats. J Hepatol 39: 538-546. PubMed: 12971963.
6. Amann T, Bataille F, Spruss T, Mühlbauer M, Gäbele E, et al. (2009) Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Cancer Sci 100: 646-653. PubMed: 19175606.
7. Jiao J, Friedman SL, Aloman C, (2009) Hepatic fibrosis. Curr Opin Gastroenterol 25: 223-229. PubMed: 19396960.
8. Xu L, Hui AY, Albanis E, Arthur MJ, O'Byrne SM, et al. (2005) Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 54: 142-151. PubMed: 15591520.
9. Mathison A, Liebl A, Bharucha J, Mukhopadhyay D, Lomberk G, et al. (2010) Pancreatic stellate cell models for transcriptional studies of desmoplasia-associated genes. Pancreatology 10: 505-516. PubMed: 20847583.
10. Lomberk G, Mathison AJ, Grzenda A, Seo S, DeMars CJ, et al. (2012) Sequence-specific recruitment of heterochromatin protein 1 via interaction with Krüppel-like factor 11, a human transcription factor involved in tumor suppression and metabolic diseases. J Biol Chem 287: 13026-13039. PubMed: 22318730.
11. Seo S, Lomberk G, Mathison A, Buttar N, Podratz J, et al. (2012) Krüppel-like factor 11 differentially couples to histone acetyltransferase and histone methyltransferase chromatin remodeling pathways to transcriptionally regulate dopamine D2 receptor in neuronal cells. J Biol Chem 287: 12723-12735. PubMed: 22375010.
12. Yang KL, Chang WT, Hung KC, Li EI, Chuang CC, (2008) Inhibition of transforming growth factor-beta-induced liver fibrosis by a retinoic acid derivative via the suppression of Col 1A2 promoter activity. Biochem Biophys Res Commun 373: 219-223. PubMed: 18558083.
13. Bonnefond A, Lomberk G, Buttar N, Busiah K, Vaillant E, et al. (2011) Disruption of a novel Kruppel-like transcription factor p300-regulated pathway for insulin biosynthesis revealed by studies of the c.-331 INS mutation found in neonatal diabetes mellitus. J Biol Chem 286: 28414-28424. PubMed: 21592955.
14. Das A, Shergill U, Thakur L, Sinha S, Urrutia R, et al. (2010) Ephrin B2/EphB4 pathway in hepatic stellate cells stimulates Erk-dependent VEGF production and sinusoidal endothelial cell recruitment. Am J Physiol Gastrointest Liver Physiol 298: G908-G915. PubMed: 20338920.
15. Ma X, Xu L, Wang S, Chen H, Xu J, et al. (2009) Loss of steroid receptor co-activator-3 attenuates carbon tetrachloride-induced murine hepatic injury and fibrosis. Lab Invest 89: 903-914. PubMed: 19488034.
16. Zhao XY, Wang BE, Li XM, Wang TL, (2008) Newly proposed fibrosis staging criterion for assessing carbon tetrachloride- and albumin complex-induced liver fibrosis in rodents. Pathol Int 58: 580-588. PubMed: 18801073.
17. Das A, Shergill U, Thakur L, Sinha S, Urrutia R, et al. (2010) Ephrin B2/EphB4 pathway in hepatic stellate cells stimulates Erk-dependent VEGF production and sinusoidal endothelial cell recruitment. Am J Physiol Gastrointest Liver Physiol 298: G908-G915. PubMed: 20338920.
18. Carpino G, Morini S, Ginanni Corradini S, Franchitto A, Merli M, et al. (2005) Alpha-SMA expression in hepatic stellate cells and quantitative analysis of hepatic fibrosis in cirrhosis and in recurrent chronic hepatitis after liver transplantation. Dig Liver Dis 37: 349-356. PubMed: 15843085.
19. Zhang H, Chen Q, Yang M, Zhu B, Cui Y, et al. (2013) Mouse KLF11 regulates hepatic lipid metabolism. J Hepatol, 58: 763-70. PubMed: 23183531.
20. Watanabe A, Hashmi A, Gomes DA, Town T, Badou A, et al. (2007) Apoptotic hepatocyte DNA inhibits hepatic stellate cell chemotaxis via toll-like receptor 9. Hepatology 46: 1509-1518. PubMed: 17705260.
21. Fernandez-Zapico ME, van Velkinburgh JC, Gutiérrez-Aguilar R, Neve B, Froguel P, et al. (2009) MODY7 gene, KLF11, is a novel p300-dependent regulator of Pdx-1 (MODY4) transcription in pancreatic islet beta cells. J Biol Chem 284: 36482-36490. PubMed: 19843526.
22. Lomberk G, Urrutia R, (2005) The family feud: turning off Sp1 by Sp1-like KLF proteins. Biochem J 392: 1-11. PubMed: 16266294.
23. Moore DL, Blackmore MG, Hu Y, Kaestner KH, Bixby JL, et al. (2009) KLF family members regulate intrinsic axon regeneration ability. Science 326: 298-301. PubMed: 19815778.
24. Lomberk G, Mathison AJ, Grzenda A, Seo S, DeMars CJ, et al. (2012) Sequence-specific recruitment of heterochromatin protein 1 via interaction with Krüppel-like factor 11, a human transcription factor involved in tumor suppression and metabolic diseases. J Biol Chem 287: 13026-13039. PubMed: 22318730.
25. Buttar NS, DeMars CJ, Lomberk G, Rizvi S, Bonilla-Velez J, et al. (2010) Distinct role of Kruppel-like factor 11 in the regulation of prostaglandin E2 biosynthesis. J Biol Chem 285: 11433-11444. PubMed: 20154088.
26. Grunewald M, Johnson S, Lu D, Wang Z, Lomberk G, et al. (2012) Mechanistic role for a novel glucocorticoid-KLF11 (TIEG2) protein pathway in stress-induced monoamine oxidase A expression. J Biol Chem 287: 24195-24206. PubMed: 22628545.
27. Lee UE, Friedman SL, (2011) Mechanisms of hepatic fibrogenesis. Best Pract Res Clin Gastroenterol 25: 195-206. PubMed: 21497738.
28. Wight TN, Potter-Perigo S, (2011) The extracellular matrix: an active or passive player in fibrosis? Am J Physiol Gastrointest Liver Physiol 301: G950-G955. PubMed: 21512158.
29. Wynn TA, (2012) Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18: 1028-1040. PubMed: 22772564.
30. Schuppan D, Kim YO, (2013) Evolving therapies for liver fibrosis. J Clin Invest 123: 1887-1901. PubMed: 23635787.
31. Erkan M, Hausmann S, Michalski CW, Fingerle AA, Dobritz M, Kleeff J, Friess H, (2012) The role of stroma in pancreatic cancer: diagnostic and therapeutic implications. Nat Rev Gastroenterol Hepatol 9: 454-467.
32. Yin C, Evason KJ, Asahina K, Stainier DY, (2013) Hepatic stellate cells in liver development, regeneration, and cancer. J Clin Invest 123: 1902-1910. PubMed: 23635788.
33. Apte MV, Wilson JS, Lugea A, Pandol SJ, (2013) A starring role for stellate cells in the pancreatic cancer microenvironment. Gastroenterology 144: 1210-1219. PubMed: 23622130.
34. Yin C, Evanson K, Asahina K, Stainier DY, (2013) Hepatic stellate cells in liver development, regeneration, and cancer. J Clin Invest 123: 1902-1910. PubMed: 23635788.
35. Lomberk G, Mathison AJ, Grzenda A, Urrutia R, (2008) The sunset of somatic genetics and the dawn of epigenetics: a new frontier in pancreatic cancer research. Curr Opin Gastroenterol 24: 597-602. PubMed: 19122501.
36. Hedin KE, Kaczynski JA, Gibson MR, Urrutia R, (2000) Transcription factors in cell biology, surgery, and transplantation. Surgery 128: 1-5. PubMed: 10876177.
37. Seo S, Grzenda A, Lomberk G, Ou XM, Cruciani RA, Urrutia R, (2013) Epigenetics: a promising paradigm for better understanding and managing pain. J Pain 14: 549-557. PubMed: 23602266.