Hypoxia-Inducible Factor/MAZ-Dependent Induction of Caveolin-1 Regulates Colon Permeability through Suppression of Occludin, Leading to Hypoxia-Induced Inflammation

REFERENCES

• Semenza GL. 2012. Hypoxia-inducible factors in physiology and medicine. Cell 148:399–408. http://dx.doi.org/10.1016/j.cell.2012.01.021.
   PubMed Web of Science ®Google Scholar
• Smith TG, Robbins PA, Ratcliffe PJ. 2008. The human side of hypoxia-inducible factor. Br. J. Haematol. 141:325–334. http://dx.doi.org/10.1111/j.1365-2141.2008.07029.x.
   PubMed Web of Science ®Google Scholar
• Kallio PJ, Okamoto K, O'Brien S, Carrero P, Makino Y, Tanaka H, Poellinger L. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17:6573–6586. http://dx.doi.org/10.1093/emboj/17.22.6573.
   PubMed Web of Science ®Google Scholar
• Pugh CW, Chang GW, Cockman M, Epstein AC, Gleadle JM, Maxwell PH, Nicholls LG, O'Rourke JF, Ratcliffe PJ, Raybould EC, Tian YM, Wiesener MS, Wood M, Wykoff CC, Yeates KM. 1999. Regulation of gene expression by oxygen levels in mammalian cells. Adv. Nephrol. Necker Hosp. 29:191–206.
   PubMedGoogle Scholar
• Pandey BD, Nabeshima T, Pandey K, Rajendra SP, Shah Y, Adhikari BR, Gupta G, Gautam I, Tun MM, Uchida R, Shrestha M, Kurane I, Morita K. 2013. First isolation of dengue virus from the 2010 epidemic in Nepal. Trop. Med. Health 41:103–111. http://dx.doi.org/10.2149/tmh.2012-17.
   PubMedGoogle Scholar
• Furuta GT, Turner JR, Taylor CT, Hershberg RM, Comerford K, Narravula S, Podolsky DK, Colgan SP. 2001. Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193:1027–1034. http://dx.doi.org/10.1084/jem.193.9.1027.
   PubMed Web of Science ®Google Scholar
• Louis NA, Hamilton KE, Kong T, Colgan SP. 2005. HIF-dependent induction of apical CD55 coordinates epithelial clearance of neutrophils. FASEB J. 19:950–959. http://dx.doi.org/10.1096/fj.04-3251com.
   PubMed Web of Science ®Google Scholar
• Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, Eltzschig HK, Hansen KR, Thompson LF, Colgan SP. 2002. Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J. Clin. Invest. 110:993–1002. http://dx.doi.org/10.1172/JCI0215337.
   PubMed Web of Science ®Google Scholar
• Cummins EP, Seeballuck F, Keely SJ, Mangan NE, Callanan JJ, Fallon PG, Taylor CT. 2008. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134:156–165. http://dx.doi.org/10.1053/j.gastro.2007.10.012.
   PubMed Web of Science ®Google Scholar
• Tambuwala MM, Cummins EP, Lenihan CR, Kiss J, Stauch M, Scholz CC, Fraisl P, Lasitschka F, Mollenhauer M, Saunders SP, Maxwell PH, Carmeliet P, Fallon PG, Schneider M, Taylor CT. 2010. Loss of prolyl hydroxylase-1 protects against colitis through reduced epithelial cell apoptosis and increased barrier function. Gastroenterology 139:2093–2101. http://dx.doi.org/10.1053/j.gastro.2010.06.068.
   PubMed Web of Science ®Google Scholar
• Robinson A, Keely S, Karhausen J, Gerich ME, Furuta GT, Colgan SP. 2008. Mucosal protection by hypoxia-inducible factor prolyl hydroxylase inhibition. Gastroenterology 134:145–155. http://dx.doi.org/10.1053/j.gastro.2007.09.033.
   PubMed Web of Science ®Google Scholar
• Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, Haase VH. 2004. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 114:1098–1106. http://dx.doi.org/10.1172/JCI200421086.
   PubMed Web of Science ®Google Scholar
• Xue X, Ramakrishnan S, Anderson E, Taylor M, Zimmermann EM, Spence JR, Huang S, Greenson JK, Shah YM. 2013. Endothelial PAS domain protein 1 activates the inflammatory response in the intestinal epithelium to promote colitis in mice. Gastroenterology 145:831–841. http://dx.doi.org/10.1053/j.gastro.2013.07.010.
   PubMedGoogle Scholar
• Shah YM, Ito S, Morimura K, Chen C, Yim SH, Haase VH, Gonzalez FJ. 2008. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology 134:2036–2048. http://dx.doi.org/10.1053/j.gastro.2008.03.009.
   PubMedGoogle Scholar
• Xue X, Shah YM. 2013. Hypoxia-inducible factor-2alpha is essential in activating the COX2/mPGES-1/PGE2 signaling axis in colon cancer. Carcinogenesis 34:163–169. http://dx.doi.org/10.1093/carcin/bgs313.
   PubMed Web of Science ®Google Scholar
• Xue X, Taylor M, Anderson E, Hao C, Qu A, Greenson JK, Zimmermann EM, Gonzalez FJ, Shah YM. 2012. Hypoxia-inducible factor-2alpha activation promotes colorectal cancer progression by dysregulating iron homeostasis. Cancer Res. 72:2285–2293. http://dx.doi.org/10.1158/0008-5472.CAN-11-3836.
   PubMed Web of Science ®Google Scholar
• Palade GE. 1953. An electron microscope study of the mitochondrial structure. J. Histochem. Cytochem. 1:188–211. http://dx.doi.org/10.1177/1.4.188.
   PubMed Web of Science ®Google Scholar
• Williams TM, Lisanti MP. 2005. Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am. J. Physiol. Cell Physiol. 288:C494–C506. http://dx.doi.org/10.1152/ajpcell.00458.2004.
   PubMed Web of Science ®Google Scholar
• Parton RG, Simons K. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8:185–194. http://dx.doi.org/10.1038/nrm2122.
   PubMed Web of Science ®Google Scholar
• Bender FC, Reymond MA, Bron C, Quest AF. 2000. Caveolin-1 levels are down-regulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res. 60:5870–5878.
   PubMed Web of Science ®Google Scholar
• Cantiani L, Manara MC, Zucchini C, De Sanctis P, Zuntini M, Valvassori L, Serra M, Olivero M, Di Renzo MF, Colombo MP, Picci P, Scotlandi K. 2007. Caveolin-1 reduces osteosarcoma metastases by inhibiting c-Src activity and Met signaling. Cancer Res. 67:7675–7685. http://dx.doi.org/10.1158/0008-5472.CAN-06-4697.
   PubMed Web of Science ®Google Scholar
• Chidlow JHJr, Greer JJ, Anthoni C, Bernatchez P, Fernandez-Hernando C, Bruce M, Abdelbaqi M, Shukla D, Granger DN, Sessa WC, Kevil CG. 2009. Endothelial caveolin-1 regulates pathologic angiogenesis in a mouse model of colitis. Gastroenterology 136:575–584. http://dx.doi.org/10.1053/j.gastro.2008.10.085.
   PubMedGoogle Scholar
• Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, Muller WJ, Chopra NG, Scherer PE, Pestell RG, Lisanti MP. 2004. Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J. Biol. Chem. 279:51630–51646. http://dx.doi.org/10.1074/jbc.M409214200.
   PubMed Web of Science ®Google Scholar
• Wang Y, Roche O, Xu C, Moriyama EH, Heir P, Chung J, Roos FC, Chen Y, Finak G, Milosevic M, Wilson BC, Teh BT, Park M, Irwin MS, Ohh M. 2012. Hypoxia promotes ligand-independent EGF receptor signaling via hypoxia-inducible factor-mediated upregulation of caveolin-1. Proc. Natl. Acad. Sci. U. S. A. 109:4892–4897. http://dx.doi.org/10.1073/pnas.1112129109.
   PubMed Web of Science ®Google Scholar
• Taylor M, Qu A, Anderson ER, Matsubara T, Martin A, Gonzalez FJ, Shah YM. 2011. Hypoxia-inducible factor-2alpha mediates the adaptive increase of intestinal ferroportin during iron deficiency in mice. Gastroenterology 140:2044–2055. http://dx.doi.org/10.1053/j.gastro.2011.03.007.
   PubMed Web of Science ®Google Scholar
• Shah YM, Matsubara T, Ito S, Yim SH, Gonzalez FJ. 2009. Intestinal hypoxia-inducible transcription factors are essential for iron absorption following iron deficiency. Cell Metab. 9:152–164. http://dx.doi.org/10.1016/j.cmet.2008.12.012.
   PubMed Web of Science ®Google Scholar
• Kathuria H, Cao YX, Ramirez MI, Williams MC. 2004. Transcription of the caveolin-1 gene is differentially regulated in lung type I epithelial and endothelial cell lines. A role for ETS proteins in epithelial cell expression. J. Biol. Chem. 279:30028–30036. http://dx.doi.org/10.1074/jbc.M402236200.
   PubMed Web of Science ®Google Scholar
• Yan X, Zhang Y, Zhang H, Wang PG, Chu X, Wang X. 2014. Amphiphilic polyethylenimine (PEI) as highly efficient non-viral gene carrier. Org. Biomol. Chem. 12:1975–1982. http://dx.doi.org/10.1039/c3ob42279h.
   PubMedGoogle Scholar
• Ramakrishnan SK, Taylor M, Qu A, Ahn SH, Suresh MV, Raghavendran K, Gonzalez FJ, Shah YM. 2014. Loss of Von Hippel-Lindau (VHL) increases systemic cholesterol level through targeting HIF-2alpha and regulation of bile acid homeostasis. Mol. Cell. Biol. 34:1208–1220. http://dx.doi.org/10.1128/MCB.01441-13.
   PubMedGoogle Scholar
• Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, von Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468–472. http://dx.doi.org/10.1126/science.1059796.
   PubMed Web of Science ®Google Scholar
• Salceda S, Caro J. 1997. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 272:22642–22647.
   PubMed Web of Science ®Google Scholar
• Huang LE, Gu J, Schau M, Bunn HF. 1998. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. U. S. A. 95:7987–7992. http://dx.doi.org/10.1073/pnas.95.14.7987.
   PubMed Web of Science ®Google Scholar
• Jiang BH, Rue E, Wang GL, Roe R, Semenza GL. 1996. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J. Biol. Chem. 271:17771–17778. http://dx.doi.org/10.1074/jbc.271.30.17771.
   PubMed Web of Science ®Google Scholar
• Rolfs A, Kvietikova I, Gassmann M, Wenger RH. 1997. Oxygen-regulated transferrin expression is mediated by hypoxia-inducible factor-1. J. Biol. Chem. 272:20055–20062. http://dx.doi.org/10.1074/jbc.272.32.20055.
   PubMed Web of Science ®Google Scholar
• Ray A, Dhar S, Shakya A, Ray P, Okada Y, Ray BK. 2009. SAF-3, a novel splice variant of the SAF-1/MAZ/Pur-1 family, is expressed during inflammation. FEBS J. 276:4276–4286. http://dx.doi.org/10.1111/j.1742-4658.2009.07136.x.
   PubMedGoogle Scholar
• Couet J, Sargiacomo M, Lisanti MP. 1997. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272:30429–30438.
   PubMed Web of Science ®Google Scholar
• Marchiando AM, Shen L, Graham WV, Weber CR, Schwarz BT, Austin JRII, Raleigh DR, Guan Y, Watson AJ, Montrose MH, Turner JR. 2010. Caveolin-1-dependent occludin endocytosis is required for TNF-induced tight junction regulation in vivo. J. Cell Biol. 189:111–126. http://dx.doi.org/10.1083/jcb.200902153.
   PubMed Web of Science ®Google Scholar
• Murakami T, Felinski EA, Antonetti DA. 2009. Occludin phosphorylation and ubiquitination regulate tight junction trafficking and vascular endothelial growth factor-induced permeability. J. Biol. Chem. 284:21036–21046. http://dx.doi.org/10.1074/jbc.M109.016766.
   PubMed Web of Science ®Google Scholar
• Grivennikov SI, Wang K, Mucida D, Stewart CA, Schnabl B, Jauch D, Taniguchi K, Yu GY, Osterreicher CH, Hung KE, Datz C, Feng Y, Fearon ER, Oukka M, Tessarollo L, Coppola V, Yarovinsky F, Cheroutre H, Eckmann L, Trinchieri G, Karin M. 2012. Adenoma-linked barrier defects and microbial products drive IL-23/IL-17-mediated tumour growth. Nature 491:254–258. http://dx.doi.org/10.1038/nature11465.
   PubMed Web of Science ®Google Scholar
• Schwarz BT, Wang F, Shen L, Clayburgh DR, Su L, Wang Y, Fu YX, Turner JR. 2007. LIGHT signals directly to intestinal epithelia to cause barrier dysfunction via cytoskeletal and endocytic mechanisms. Gastroenterology 132:2383–2394. http://dx.doi.org/10.1053/j.gastro.2007.02.052.
   PubMed Web of Science ®Google Scholar
• Glover LE, Bowers BE, Saeedi B, Ehrentraut SF, Campbell EL, Bayless AJ, Dobrinskikh E, Kendrick AA, Kelly CJ, Burgess A, Miller L, Kominsky DJ, Jedlicka P, Colgan SP. 2013. Control of creatine metabolism by HIF is an endogenous mechanism of barrier regulation in colitis. Proc. Natl. Acad. Sci. U. S. A. 110:19820–19825. http://dx.doi.org/10.1073/pnas.1302840110.
   PubMed Web of Science ®Google Scholar
• Fine SW, Lisanti MP, Galbiati F, Li M. 2001. Elevated expression of caveolin-1 in adenocarcinoma of the colon. Am. J. Clin. Pathol. 115:719–724. http://dx.doi.org/10.1309/YL54-CCU7-4V0P-FDUT.
   PubMed Web of Science ®Google Scholar
• Mori Y, Cai K, Cheng Y, Wang S, Paun B, Hamilton JP, Jin Z, Sato F, Berki AT, Kan T, Ito T, Mantzur C, Abraham JM, Meltzer SJ. 2006. A genome-wide search identifies epigenetic silencing of somatostatin, tachykinin-1, and 5 other genes in colon cancer. Gastroenterology 131:797–808. http://dx.doi.org/10.1053/j.gastro.2006.06.006.
   PubMed Web of Science ®Google Scholar
• Williams TM, Lisanti MP. 2004. The caveolin genes: from cell biology to medicine. Ann. Med. 36:584–595. http://dx.doi.org/10.1080/07853890410018899.
   PubMed Web of Science ®Google Scholar
• Cohen AW, Razani B, Schubert W, Williams TM, Wang XB, Iyengar P, Brasaemle DL, Scherer PE, Lisanti MP. 2004. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes 53:1261–1270. http://dx.doi.org/10.2337/diabetes.53.5.1261.
   PubMed Web of Science ®Google Scholar
• Friedrich T, Richter B, Gaiser T, Weiss C, Janssen KP, Einwachter H, Schmid RM, Ebert MP, Burgermeister E. 2013. Deficiency of caveolin-1 in Apc(min/+) mice promotes colorectal tumorigenesis. Carcinogenesis 34:2109–2118. http://dx.doi.org/10.1093/carcin/bgt142.
   PubMed Web of Science ®Google Scholar
• Williams TM, Lee H, Cheung MW, Cohen AW, Razani B, Iyengar P, Scherer PE, Pestell RG, Lisanti MP. 2004. Combined loss of INK4a and caveolin-1 synergistically enhances cell proliferation and oncogene-induced tumorigenesis: role of INK4a/CAV-1 in mammary epithelial cell hyperplasia. J. Biol. Chem. 279:24745–24756. http://dx.doi.org/10.1074/jbc.M402064200.
   PubMed Web of Science ®Google Scholar
• Williams TM, Lisanti MP. 2004. The caveolin proteins. Genome Biol. 5:214. http://dx.doi.org/10.1186/gb-2004-5-3-214.
   PubMed Web of Science ®Google Scholar
• Satoh T, Yang G, Egawa S, Addai J, Frolov A, Kuwao S, Timme TL, Baba S, Thompson TC. 2003. Caveolin-1 expression is a predictor of recurrence-free survival in pT2N0 prostate carcinoma diagnosed in Japanese patients. Cancer 97:1225–1233. http://dx.doi.org/10.1002/cncr.11198.
   PubMed Web of Science ®Google Scholar
• Yang G, Truong LD, Wheeler TM, Thompson TC. 1999. Caveolin-1 expression in clinically confined human prostate cancer: a novel prognostic marker. Cancer Res. 59:5719–5723.
   PubMed Web of Science ®Google Scholar
• Ho CC, Huang PH, Huang HY, Chen YH, Yang PC, Hsu SM. 2002. Up-regulated caveolin-1 accentuates the metastasis capability of lung adenocarcinoma by inducing filopodia formation. Am. J. Pathol. 161:1647–1656. http://dx.doi.org/10.1016/S0002-9440(10)64442-2.
   PubMed Web of Science ®Google Scholar
• Bailey KM, Liu J. 2008. Caveolin-1 up-regulation during epithelial to mesenchymal transition is mediated by focal adhesion kinase. J. Biol. Chem. 283:13714–13724. http://dx.doi.org/10.1074/jbc.M709329200.
   PubMedGoogle Scholar
• Cokakli M, Erdal E, Nart D, Yilmaz F, Sagol O, Kilic M, Karademir S, Atabey N. 2009. Differential expression of caveolin-1 in hepatocellular carcinoma: correlation with differentiation state, motility and invasion. BMC Cancer 9:65. http://dx.doi.org/10.1186/1471-2407-9-65.
   PubMed Web of Science ®Google Scholar
• Chou YT, Lin HH, Lien YC, Wang YH, Hong CF, Kao YR, Lin SC, Chang YC, Lin SY, Chen SJ, Chen HC, Yeh SD, Wu CW. 2010. EGFR promotes lung tumorigenesis by activating miR-7 through a Ras/ERK/Myc pathway that targets the Ets2 transcriptional repressor ERF. Cancer Res. 70:8822–8831. http://dx.doi.org/10.1158/0008-5472.CAN-10-0638.
   PubMed Web of Science ®Google Scholar
• Fraguas S, Barberan S, Cebria F. 2011. EGFR signaling regulates cell proliferation, differentiation and morphogenesis during planarian regeneration and homeostasis. Dev. Biol. 354:87–101. http://dx.doi.org/10.1016/j.ydbio.2011.03.023.
   PubMedGoogle Scholar
• Gazdar AF, Minna JD. 2008. Deregulated EGFR signaling during lung cancer progression: mutations, amplicons, and autocrine loops. Cancer Prev. Res. (Phila.) 1:156–160. http://dx.doi.org/10.1158/1940-6207.CAPR-08-0080.
   PubMed Web of Science ®Google Scholar
• Ray A, Ray BK. 1996. A novel cis-acting element is essential for cytokine-mediated transcriptional induction of the serum amyloid A gene in nonhepatic cells. Mol. Cell. Biol. 16:1584–1594.
   PubMed Web of Science ®Google Scholar
• Ray A, Ray BK. 1998. Isolation and functional characterization of cDNA of serum amyloid A-activating factor that binds to the serum amyloid A promoter. Mol. Cell. Biol. 18:7327–7335.
   PubMedGoogle Scholar