RAB26 and RAB3D Are Direct Transcriptional Targets of MIST1 That Regulate Exocrine Granule Maturation

REFERENCES

• Barnes, W. M. 2003. Ribocloning, chapter 29 . In C. W. Dieffenbach and G. S. Dveksler (ed.), PCR primer: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
   Google Scholar
• Barnes, W. M. 1994. PCR amplification of up to 35-kb DNA with high fidelity and high yield from lambda bacteriophage templates. Proc. Natl. Acad. Sci. U. S. A. 91:2216–2220.
   PubMed Web of Science ®Google Scholar
• Baron, R. A., R. Tavare, A. C. Figueiredo, K. M. Blazewska, B. A. Kashemirov, C. E. McKenna, F. H. Ebetino, A. Taylor, M. J. Rogers, F. P. Coxon, and M. C. Seabra. 2009. Phosphonocarboxylates inhibit the second geranylgeranyl addition by Rab geranylgeranyl transferase. J. Biol. Chem. 284:6861–6868.
   PubMed Web of Science ®Google Scholar
• Bhattacharya, D., M. T. Cheah, C. B. Franco, N. Hosen, C. L. Pin, W. C. Sha, and I. L. Weissman. 2007. Transcriptional profiling of antigen-dependent murine B cell differentiation and memory formation. J. Immunol. 179:6808–6819.
   PubMed Web of Science ®Google Scholar
• Bredemeyer, A. J., J. H. Geahlen, V. G. Weis, W. J. Huh, B. H. Zinselmeyer, S. Srivatsan, M. J. Miller, A. S. Shaw, and J. C. Mills. 2009. The gastric epithelial progenitor cell niche and differentiation of the zymogenic (chief) cell lineage. Dev. Biol. 325:211–224.
   PubMedGoogle Scholar
• Capoccia, B. J., W. J. Huh, and J. C. Mills. 2009. How form follows functional genomics: gene expression profiling gastric epithelial cells with a particular discourse on the parietal cell. Physiol. Genomics 37:67–78.
   PubMedGoogle Scholar
• Chen, X., J. A. Edwards, C. D. Logsdon, S. A. Ernst, and J. A. Williams. 2002. Dominant negative Rab3D inhibits amylase release from mouse pancreatic acini. J. Biol. Chem. 277:18002–18009.
   PubMed Web of Science ®Google Scholar
• Cohen, M. M., Jr. 2003. The hedgehog signaling network. Am. J. Med. Genet. A 123A:5–28.
   PubMed Web of Science ®Google Scholar
• Cox, G. A., C. L. Mahaffey, A. Nystuen, V. A. Letts, and W. N. Frankel. 2000. The mouse fidgetin gene defines a new role for AAA family proteins in mammalian development. Nat. Genet. 26:198–202.
   PubMedGoogle Scholar
• Coxon, F. P., F. H. Ebetino, E. H. Mules, M. C. Seabra, C. E. McKenna, and M. J. Rogers. 2005. Phosphonocarboxylate inhibitors of Rab geranylgeranyl transferase disrupt the prenylation and membrane localization of Rab proteins in osteoclasts in vitro and in vivo. Bone 37:349–358.
   PubMed Web of Science ®Google Scholar
• Davis, R. L., A. E. Shrimpton, R. W. Carrell, D. A. Lomas, L. Gerhard, B. Baumann, D. A. Lawrence, M. Yepes, T. S. Kim, B. Ghetti, P. Piccardo, M. Takao, F. Lacbawan, M. Muenke, R. N. Sifers, C. B. Bradshaw, P. F. Kent, G. H. Collins, D. Larocca, and P. D. Holohan. 2002. Association between conformational mutations in neuroserpin and onset and severity of dementia. Lancet 359:2242–2247.
   PubMed Web of Science ®Google Scholar
• Davis, R. L., A. E. Shrimpton, P. D. Holohan, C. Bradshaw, D. Feiglin, G. H. Collins, P. Sonderegger, J. Kinter, L. M. Becker, F. Lacbawan, D. Krasnewich, M. Muenke, D. A. Lawrence, M. S. Yerby, C. M. Shaw, B. Gooptu, P. R. Elliott, J. T. Finch, R. W. Carrell, and D. A. Lomas. 1999. Familial dementia caused by polymerization of mutant neuroserpin. Nature 401:376–379.
   PubMed Web of Science ®Google Scholar
• Doherty, J. M., M. J. Geske, T. S. Stappenbeck, and J. C. Mills. 2008. Diverse adult stem cells share specific higher-order patterns of gene expression. Stem Cells 26:2124–2130.
   PubMedGoogle Scholar
• Ea, C. K., L. Sun, J. Inoue, and Z. J. Chen. 2004. TIFA activates IkappaB kinase (IKK) by promoting oligomerization and ubiquitination of TRAF6. Proc. Natl. Acad. Sci. U. S. A. 101:15318–15323.
   PubMedGoogle Scholar
• Fukuda, M. 2008. Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol. Life Sci. 65:2801–2813.
   PubMed Web of Science ®Google Scholar
• Gerson, K. D., C. D. Foster, P. Zhang, Z. Zhang, M. M. Rosenblatt, and S. H. Guttentag. 2008. Pepsinogen C proteolytic processing of surfactant protein B. J. Biol. Chem. 283:10330–10338.
   PubMedGoogle Scholar
• Grosshans, B. L., D. Ortiz, and P. Novick. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. U. S. A. 103:11821–11827.
   PubMed Web of Science ®Google Scholar
• Guo, X., L. Cheng, Y. Liu, W. Fan, and D. Lu. 2007. Cloning, expression, and functional characterization of zebrafish Mist1. Biochem. Biophys. Res. Commun. 359:20–26.
   PubMedGoogle Scholar
• Hamanaka, Y., D. Park, Y. Ping, T. Edwards, J. W. Sweedler, I. A. Meinertzhagen, and P. H. Taghert. 2010. Transcriptional orchestration of the regulated secretory pathway in neurons by the bHLH protein DIMM. Curr. Biol. 20:9–18.
   PubMedGoogle Scholar
• Hewes, R. S., D. Park, S. A. Gauthier, A. M. Schaefer, and P. H. Taghert. 2003. The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila. Development 130:1771–1781.
   PubMed Web of Science ®Google Scholar
• Hulsen, T., J. de Vlieg, and W. Alkema. 2008. BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9:488.
   PubMed Web of Science ®Google Scholar
• Im, H., J. A. Grass, K. D. Johnson, M. E. Boyer, J. Wu, and E. H. Bresnick. 2004. Measurement of protein-DNA interactions in vivo by chromatin immunoprecipitation. Methods Mol. Biol. 284:129–146.
   PubMedGoogle Scholar
• Inase, N., K. Fushimi, K. Ishibashi, S. Uchida, M. Ichioka, S. Sasaki, and F. Marumo. 1995. Isolation of human aquaporin 3 gene. J. Biol. Chem. 270:17913–17916.
   PubMedGoogle Scholar
• Jia, D., Y. Sun, and S. F. Konieczny. 2008. Mist1 regulates pancreatic acinar cell proliferation through p21 CIP1/WAF1. Gastroenterology 135:1687–1697.
   PubMedGoogle Scholar
• Jiang, M., X. Gu, X. Feng, Z. Fan, F. Ding, and Y. Liu. 2009. The molecular characterization of the brain protein 44-like (Brp44l) gene of Gekko japonicus and its expression changes in spinal cord after tail amputation. Mol. Biol. Rep. 36:215–220.
   PubMedGoogle Scholar
• Johnson, C. L., A. S. Kowalik, N. Rajakumar, and C. L. Pin. 2004. Mist1 is necessary for the establishment of granule organization in serous exocrine cells of the gastrointestinal tract. Mech. Dev. 121:261–272.
   PubMedGoogle Scholar
• Kanamori, M., H. Suzuki, R. Saito, M. Muramatsu, and Y. Hayashizaki. 2002. T2BP, a novel TRAF2 binding protein, can activate NF-kappaB and AP-1 without TNF stimulation. Biochem. Biophys. Res. Commun. 290:1108–1113.
   PubMedGoogle Scholar
• Karam, S. M., and C. P. Leblond. 1993. Dynamics of epithelial cells in the corpus of the mouse stomach. I. Identification of proliferative cell types and pinpointing of the stem cell. Anat. Rec. 236:259–279.
   PubMedGoogle Scholar
• Karam, S. M., and C. P. Leblond. 1993. Dynamics of epithelial cells in the corpus of the mouse stomach. III. Inward migration of neck cells followed by progressive transformation into zymogenic cells. Anat. Rec. 236:297–313.
   PubMedGoogle Scholar
• Kaser, A., A. H. Lee, A. Franke, J. N. Glickman, S. Zeissig, H. Tilg, E. E. Nieuwenhuis, D. E. Higgins, S. Schreiber, L. H. Glimcher, and R. S. Blumberg. 2008. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134:743–756.
   PubMed Web of Science ®Google Scholar
• Kostenko, E. V., O. O. Olabisi, S. Sahay, P. L. Rodriguez, and I. P. Whitehead. 2006. Ccpg1, a novel scaffold protein that regulates the activity of the Rho guanine nucleotide exchange factor Dbs. Mol. Cell. Biol. 26:8964–8975.
   PubMedGoogle Scholar
• Kowalik, A. S., C. L. Johnson, S. A. Chadi, J. Y. Weston, E. N. Fazio, and C. L. Pin. 2007. Mice lacking the transcription factor Mist1 exhibit an altered stress response and increased sensitivity to caerulein-induced pancreatitis. Am. J. Physiol. Gastrointest. Liver Physiol. 292:G1123–G1132.
   PubMed Web of Science ®Google Scholar
• Lee, A. H., G. C. Chu, N. N. Iwakoshi, and L. H. Glimcher. 2005. XBP-1 is required for biogenesis of cellular secretory machinery of exocrine glands. EMBO J. 24:4368–4380.
   PubMed Web of Science ®Google Scholar
• Luo, X., D. M. Shin, X. Wang, S. F. Konieczny, and S. Muallem. 2005. Aberrant localization of intracellular organelles, Ca2+ signaling, and exocytosis in Mist1 null mice. J. Biol. Chem. 280:12668–12675.
   PubMedGoogle Scholar
• Ma, Y., A. Erkner, R. Gong, S. Yao, J. Taipale, K. Basler, and P. A. Beachy. 2002. Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 111:63–75.
   PubMed Web of Science ®Google Scholar
• Mannan, A. U., E. Roussa, C. Kraus, M. Rickmann, J. Maenner, K. Nayernia, K. Krieglstein, A. Reis, and W. Engel. 2004. Mutation in the gene encoding lysosomal acid phosphatase (Acp2) causes cerebellum and skin malformation in mouse. Neurogenetics 5:229–238.
   PubMedGoogle Scholar
• Marchelletta, R. R., D. T. Jacobs, J. E. Schechter, R. E. Cheney, and S. F. Hamm-Alvarez. 2008. The class V myosin motor, myosin 5c, localizes to mature secretory vesicles and facilitates exocytosis in lacrimal acini. Am. J. Physiol. Cell Physiol. 295:C13–C28.
   PubMedGoogle Scholar
• Millar, A. L., N. J. Pavios, J. Xu, and M. H. Zheng. 2002. Rab3D: a regulator of exocytosis in non-neuronal cells. Histol. Histopathol. 17:929–936.
   PubMed Web of Science ®Google Scholar
• Mills, J. C., N. Andersson, C. V. Hong, T. S. Stappenbeck, and J. I. Gordon. 2002. Molecular characterization of mouse gastric epithelial progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 99:14819–14824.
   PubMedGoogle Scholar
• Nashida, T., A. Imai, and H. Shimomura. 2006. Relation of Rab26 to the amylase release from rat parotid acinar cells. Arch. Oral Biol. 51:89–95.
   PubMed Web of Science ®Google Scholar
• Obholz, K. L., A. Akopyan, K. G. Waymire, and G. R. MacGregor. 2006. FNDC3A is required for adhesion between spermatids and Sertoli cells. Dev. Biol. 298:498–513.
   PubMed Web of Science ®Google Scholar
• Ohnishi, H., S. A. Ernst, N. Wys, M. McNiven, and J. A. Williams. 1996. Rab3D localizes to zymogen granules in rat pancreatic acini and other exocrine glands. Am. J. Physiol. 271:G531–G538.
   PubMedGoogle Scholar
• Oka, S., H. Masutani, W. Liu, H. Horita, D. Wang, S. Kizaka-Kondoh, and J. Yodoi. 2006. Thioredoxin-binding protein-2-like inducible membrane protein is a novel vitamin D3 and peroxisome proliferator-activated receptor (PPAR)gamma ligand target protein that regulates PPARgamma signaling. Endocrinology 147:733–743.
   PubMedGoogle Scholar
• Ovcharenko, I., M. A. Nobrega, G. G. Loots, and L. Stubbs. 2004. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucleic Acids Res. 32:W280–W286.
   PubMed Web of Science ®Google Scholar
• Park, D., O. T. Shafer, S. P. Shepherd, H. Suh, J. S. Trigg, and P. H. Taghert. 2008. The Drosophila basic helix-loop-helix protein DIMMED directly activates PHM, a gene encoding a neuropeptide-amidating enzyme. Mol. Cell. Biol. 28:410–421.
   PubMed Web of Science ®Google Scholar
• Park, D., and P. H. Taghert. 2009. Peptidergic neurosecretory cells in insects: organization and control by the bHLH protein DIMMED. Gen. Comp. Endocrinol. 162:2–7.
   PubMedGoogle Scholar
• Patel, S., and M. Latterich. 1998. The AAA team: related ATPases with diverse functions. Trends Cell Biol. 8:65–71.
   PubMed Web of Science ®Google Scholar
• Pin, C. L., A. C. Bonvissuto, and S. F. Konieczny. 2000. Mist1 expression is a common link among serous exocrine cells exhibiting regulated exocytosis. Anat. Rec. 259:157–167.
   PubMedGoogle Scholar
• Pin, C. L., J. M. Rukstalis, C. Johnson, and S. F. Konieczny. 2001. The bHLH transcription factor Mist1 is required to maintain exocrine pancreas cell organization and acinar cell identity. J. Cell Biol. 155:519–530.
   PubMedGoogle Scholar
• Ramsey, V. G., J. M. Doherty, C. C. Chen, T. S. Stappenbeck, S. F. Konieczny, and J. C. Mills. 2007. The maturation of mucus-secreting gastric epithelial progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134:211–222.
   PubMedGoogle Scholar
• Riedel, D., W. Antonin, R. Fernandez-Chacon, G. Alvarez de Toledo, T. Jo, M. Geppert, J. A. Valentijn, K. Valentijn, J. D. Jamieson, T. C. Sudhof, and R. Jahn. 2002. Rab3D is not required for exocrine exocytosis but for maintenance of normally sized secretory granules. Mol. Cell. Biol. 22:6487–6497.
   PubMed Web of Science ®Google Scholar
• Rukstalis, J. M., A. Kowalik, L. Zhu, D. Lidington, C. L. Pin, and S. F. Konieczny. 2003. Exocrine specific expression of Connexin32 is dependent on the basic helix-loop-helix transcription factor Mist1. J. Cell Sci. 116:3315–3325.
   PubMedGoogle Scholar
• Saftig, P., D. Hartmann, R. Lullmann-Rauch, J. Wolff, M. Evers, A. Koster, M. Hetman, K. von Figura, and C. Peters. 1997. Mice deficient in lysosomal acid phosphatase develop lysosomal storage in the kidney and central nervous system. J. Biol. Chem. 272:18628–18635.
   PubMedGoogle Scholar
• Sardiello, M., M. Palmieri, A. di Ronza, D. L. Medina, M. Valenza, V. A. Gennarino, C. Di Malta, F. Donaudy, V. Embrione, R. S. Polishchuk, S. Banfi, G. Parenti, E. Cattaneo, and A. Ballabio. 2009. A gene network regulating lysosomal biogenesis and function. Science 325:473–477.
   PubMed Web of Science ®Google Scholar
• Seabra, M. C., J. L. Goldstein, T. C. Sudhof, and M. S. Brown. 1992. Rab geranylgeranyl transferase. A multisubunit enzyme that prenylates GTP-binding proteins terminating in Cys-X-Cys or Cys-Cys. J. Biol. Chem. 267:14497–14503.
   PubMed Web of Science ®Google Scholar
• Shaffer, A. L., M. Shapiro-Shelef, N. N. Iwakoshi, A. H. Lee, S. B. Qian, H. Zhao, X. Yu, L. Yang, B. K. Tan, A. Rosenwald, E. M. Hurt, E. Petroulakis, N. Sonenberg, J. W. Yewdell, K. Calame, L. H. Glimcher, and L. M. Staudt. 2004. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21:81–93.
   PubMed Web of Science ®Google Scholar
• Shan, S. W., D. Y. Lee, Z. Deng, T. Shatseva, Z. Jeyapalan, W. W. Du, Y. Zhang, J. W. Xuan, S. P. Yee, V. Siragam, and B. B. Yang. 2009. MicroRNA MiR-17 retards tissue growth and represses fibronectin expression. Nat. Cell Biol. 11:1031–1038.
   PubMedGoogle Scholar
• Snapp, E. L., R. S. Hegde, M. Francolini, F. Lombardo, S. Colombo, E. Pedrazzini, N. Borgese, and J. Lippincott-Schwartz. 2003. Formation of stacked ER cisternae by low affinity protein interactions. J. Cell Biol. 163:257–269.
   PubMed Web of Science ®Google Scholar
• Sriburi, R., H. Bommiasamy, G. L. Buldak, G. R. Robbins, M. Frank, S. Jackowski, and J. W. Brewer. 2007. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem. 282:7024–7034.
   PubMedGoogle Scholar
• Stoeckli, E. T., P. F. Lemkin, T. B. Kuhn, M. A. Ruegg, M. Heller, and P. Sonderegger. 1989. Identification of proteins secreted from axons of embryonic dorsal-root-ganglia neurons. Eur. J. Biochem. 180:249–258.
   PubMedGoogle Scholar
• Takatsuna, H., H. Kato, J. Gohda, T. Akiyama, A. Moriya, Y. Okamoto, Y. Yamagata, M. Otsuka, K. Umezawa, K. Semba, and J. Inoue. 2003. Identification of TIFA as an adapter protein that links tumor necrosis factor receptor-associated factor 6 (TRAF6) to interleukin-1 (IL-1) receptor-associated kinase-1 (IRAK-1) in IL-1 receptor signaling. J. Biol. Chem. 278:12144–12150.
   PubMed Web of Science ®Google Scholar
• Tran, T., D. Jia, Y. Sun, and S. F. Konieczny. 2007. The bHLH domain of Mistl is sufficient to activate gene transcription. Gene Expr. 13:241–253.
   PubMedGoogle Scholar
• Valentijn, J. A., L. van Weeren, A. Ultee, and A. J. Koster. 2007. Novel localization of Rab3D in rat intestinal goblet cells and Brunner's gland acinar cells suggests a role in early Golgi trafficking. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G165–G177.
   PubMedGoogle Scholar
• Wagner, A. C., M. Z. Strowski, B. Goke, and J. A. Williams. 1995. Molecular cloning of a new member of the Rab protein family, Rab 26, from rat pancreas. Biochem. Biophys. Res. Commun. 207:950–956.
   PubMed Web of Science ®Google Scholar
• Williams, J. A., X. Chen, and M. E. Sabbatini. 2009. Small G proteins as key regulators of pancreatic digestive enzyme secretion. Am. J. Physiol. Endocrinol. Metab. 296:E405–E414.
   PubMed Web of Science ®Google Scholar
• Wu, M. S., Y. S. Lin, Y. T. Chang, C. T. Shun, M. T. Lin, and J. T. Lin. 2005. Gene expression profiling of gastric cancer by microarray combined with laser capture microdissection. World J. Gastroenterol. 11:7405–7412.
   PubMedGoogle Scholar
• Yoshie, S., A. Imai, T. Nashida, and H. Shimomura. 2000. Expression, characterization, and localization of Rab26, a low molecular weight GTP-binding protein, in the rat parotid gland. Histochem. Cell Biol. 113:259–263.
   PubMed Web of Science ®Google Scholar
• Zhao, Y., C. Johansson, T. Tran, R. Bettencourt, Y. Itahana, P. Y. Desprez, and S. F. Konieczny. 2006. Identification of a basic helix-loop-helix transcription factor expressed in mammary gland alveolar cells and required for maintenance of the differentiated state. Mol. Endocrinol. 20:2187–2198.
   PubMedGoogle Scholar
• Zhong, S., C. Li, and W. H. Wong. 2003. ChipInfo: software for extracting gene annotation and gene ontology information for microarray analysis. Nucleic Acids Res. 31:3483–3486.
   PubMed Web of Science ®Google Scholar
• Zhou, B., and J. Gitschier. 1997. hCTR1: a human gene for copper uptake identified by complementation in yeast. Proc. Natl. Acad. Sci. U. S. A. 94:7481–7486.
   PubMed Web of Science ®Google Scholar
• Zhou, G., Z. Q. Bao, and J. E. Dixon. 1995. Components of a new human protein kinase signal transduction pathway. J. Biol. Chem. 270:12665–12669.
   PubMed Web of Science ®Google Scholar
• Zhu, L., T. Tran, J. M. Rukstalis, P. Sun, B. Damsz, and S. F. Konieczny. 2004. Inhibition of Mist1 homodimer formation induces pancreatic acinar-to-ductal metaplasia. Mol. Cell. Biol. 24:2673–2681.
   PubMed Web of Science ®Google Scholar