TRPM5-mediated calcium uptake regulates mucin secretion from human colon goblet cells

eLife

Volumn 2013, Issue 2, 2013, Pages

  Mitrovic, Sandra ^a   Nogueira, Cristina ^a   Cantero Recasens, Gerard ^b   Kiefer, Kerstin ^b   Fernández Fernández, José M ^b   Popoff, Jean François ^a   Casano, Laetitia ^a,d   Bard, Frederic A ^a,e   Gomez, Raul ^a   Valverde, Miguel A ^b   Malhotra, Vivek ^a,c  

^a CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CHEMOKINE RECEPTOR CCR9; CHEMOKINE RECEPTOR CX3CR1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 5AC; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; OBSCURIN; SODIUM CHANNEL NAV1.2; SODIUM CHANNEL NAV1.3; SULFONYLUREA RECEPTOR 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL M5; CALCIUM; MUCIN; PHORBOL 13 ACETATE 12 MYRISTATE; TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM5 PROTEIN, HUMAN;

ARTICLE; CALCIUM TRANSPORT; CELL DIFFERENTIATION; COLON; CONTROLLED STUDY; DOT HYBRIDIZATION; ELECTROPHYSIOLOGY; GOBLET CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS REGULATION; REAL TIME POLYMERASE CHAIN REACTION; CYTOLOGY; DRUG EFFECTS; GOLGI COMPLEX; METABOLISM; PHYSIOLOGY; SECRETION (PROCESS);

CALCIUM; COLON; GOBLET CELLS; GOLGI APPARATUS; HUMANS; MUCINS; TETRADECANOYLPHORBOL ACETATE; TRPM CATION CHANNELS;

EID: 84881533920     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00658     Document Type: Article

References (68)

1. Abdullah LH, Bundy JT, Ehre C, Davis CW. 2003. Mucin secretion and PKC isoforms in SPOC1 goblet cells: differential activation by purinergic agonist and PMA. Am J Physiol Lung Cell Mol Physiol 285:L149-60. doi: 10.1152/ajplung.00359.2002.
2. Abdullah LH, Conway JD, Cohn JA, Davis CW. 1997. Protein kinase C and Ca2+ activation of mucin secretion in airway goblet cells. Am J Physiol 273:L201-10.
3. Abdullah LH, Davis SW, Burch L, Yamauchi M, Randell SH, Nettesheim P, et al. 1996. P2u purinoceptor regulation of mucin secretion in SPOC1 cells, a goblet cell line from the airways. Biochem J 316(Pt 3):943-51.
4. Aittoniemi J, Fotinou C, Craig TJ, de Wet H, Proks P, Ashcroft FM. 2009. Review. SUR1: a unique ATP-binding cassette protein that functions as an ion channel regulator. Philos Trans R Soc Lond B Biol Sci 364:257-67. doi: 10.1098/rstb.2008.0142.
5. Arbuzova A, Schmitz AA, Vergeres G. 2002. Cross-talk unfolded: MARCKS proteins. Biochem J 362:1-12. doi: 10.1042/0264-6021:3620001.
6. Barcelo A, Claustre J, Abello J, Chayvialle JA, Plaisancie P. 2001. Selective involvement of calcium and calcium channels in stimulated mucin secretion from rat colon. Scand J Gastroenterol 36:1339-43. doi: 10.1080/003655201317097227.
7. Bartman AE, Sanderson SJ, Ewing SL, Niehans GA, Wiehr CL, Evans MK, et al. 1999. Aberrant expression of MUC5AC and MUC6 gastric mucin genes in colorectal polyps. Int J Cancer 80:210-8. doi: 10.1002/(SICI)1097-0215(19990118)80:2<210::AID-IJC9>3.0.CO;2-U.
8. Bertrand CA, Danahay H, Poll CT, Laboisse C, Hopfer U, Bridges RJ. 2004. Niflumic acid inhibits ATP-stimulated exocytosis in a mucin-secreting epithelial cell line. Am J Physiol Cell Physiol 286:C247-55. doi: 10.1152/ajpcell.00593.2002.
9. Bou-Hanna C, Berthon B, Combettes L, Claret M, Laboisse CL. 1994. Role of calcium in carbachol-and neurotensin-induced mucin exocytosis in a human colonic goblet cell line and cross-talk with the cyclic AMP pathway. Biochem J 299(Pt 2):579-85.
10. Breitling R, Armengaud P, Amtmann A, Herzyk P. 2004. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Lett 573:83-92. doi: 10.1016/j.febslet.2004.07.055.
11. Brideau C, Gunter B, Pikounis B, Liaw A. 2003. Improved statistical methods for hit selection in high-throughput screening. J Biomol Screen 8:634-47. doi: 10.1177/1087057103258285.
12. Brixel LR, Monteilh-Zoller MK, Ingenbrandt CS, Fleig A, Penner R, Enklaar T, et al. 2010. TRPM5 regulates glucose-stimulated insulin secretion. Pflugers Arch 460:69-76. doi: 10.1007/s00424-010-0835-z.
13. Bu XD, Li N, Tian XQ, Li L, Wang JS, Yu XJ, et al. 2010. Altered expression of MUC2 and MUC5AC in progression of colorectal carcinoma. World J Gastroenterol 16:4089-94. doi: 10.3748/wjg.v16.i32.4089.
14. Byrd JC, Bresalier RS. 2004. Mucins and mucin binding proteins in colorectal cancer. Cancer Metastasis Rev 23:77-99. doi: 10.1023/A:1025815113599.
15. Cantero-Recasens G, Fandos C, Rubio-Moscardo F, Valverde MA, Vicente R. 2010. The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum Mol Genet 19:111-21. doi: 10.1093/hmg/ddp471.
16. Colsoul B, Schraenen A, Lemaire K, Quintens R, Van Lommel L, Segal A, et al. 2010. Loss of high-frequency glucose-induced Ca2+ oscillations in pancreatic islets correlates with impaired glucose tolerance in Trpm5-/-mice. Proc Natl Acad Sci USA 107:5208-13. doi: 10.1073/pnas.0913107107.
17. Corfield AP, Carroll D, Myerscough N, Probert CS. 2001. Mucins in the gastrointestinal tract in health and disease. Front Biosci 6:D1321-57. doi: 10.2741/Corfield.
18. Davis CW, Dickey BF. 2008. Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70:487-512. doi: 10.1146/annurev.physiol.70.113006.100638.
19. Deshpande DA, Wang WC, Mcilmoyle EL, Robinett KS, Schillinger RM, An SS, et al. 2010. Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat Med 16:1299-304. doi: 10.1038/nm.2237.
20. di Stefano A, Caramori G, Oates T, Capelli A, Lusuardi M, Gnemmi I, et al. 2002. Increased expression of nuclear factor-kappaB in bronchial biopsies from smokers and patients with COPD. Eur Respir J 20:556-63. doi: 10.1183/09031936.02.00272002.
21. Earley S, Waldron BJ, Brayden JE. 2004. Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries. Circ Res 95:922-9. doi: 10.1161/01.RES.0000147311.54833.03.
22. Ehre C, Rossi AH, Abdullah LH, de Pestel K, Hill S, Olsen JC, et al. 2005. Barrier role of actin filaments in regulated mucin secretion from airway goblet cells. Am J Physiol Cell Physiol 288:C46-56. doi: 10.1152/ajpcell.00397.2004.
23. Ehre C, Zhu Y, Abdullah LH, Olsen J, Nakayama KI, Nakayama K, et al. 2007. nPKCepsilon, a P2Y2-R downstream effector in regulated mucin secretion from airway goblet cells. Am J Physiol Cell Physiol 293:C1445-54. doi: 10.1152/ajpcell.00051.2007.
24. Epple HJ, Kreusel KM, Hanski C, Schulzke JD, Riecken EO, Fromm M. 1997. Differential stimulation of intestinal mucin secretion by cholera toxin and carbachol. Pflugers Arch 433:638-47. doi: 10.1007/s004240050325.
25. Fernandes J, Lorenzo IM, Andrade YN, Garcia-Elias A, Serra SA, Fernandez-Fernandez JM, et al. 2008. IP3 sensitizes TRPV4 channel to the mechano-and osmotransducing messenger 5'-6'-epoxyeicosatrienoic acid. J Cell Biol 181:143-55. doi: 10.1083/jcb.200712058.
26. Forgue-Lafitte ME, Fabiani B, Levy PP, Maurin N, Flejou JF, Bara J. 2007. Abnormal expression of M1/MUC5AC mucin in distal colon of patients with diverticulitis, ulcerative colitis and cancer. Int J Cancer 121:1543-9. doi: 10.1002/ijc.22865.
27. Forstner G, Zhang Y, Mccool D, Forstner J. 1994. Regulation of mucin secretion in T84 adenocarcinoma cells by forskolin: relationship to Ca2+ and PKC. Am J Physiol 266:G606-12.
28. Fujisawa T, Velichko S, Thai P, Hung LY, Huang F, Wu R. 2009. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. J Immunol 183:6236-43. doi: 10.4049/jimmunol.0900614.
29. Hart LA, Krishnan VL, Adcock IM, Barnes PJ, Chung KF. 1998. Activation and localization of transcription factor, nuclear factor-kappaB, in asthma. Am J Respir Crit Care Med 158:1585-92. doi: 10.1164/ajrccm.158.5.9706116.
30. Hasnain SZ, Evans CM, Roy M, Gallagher AL, Kindrachuk KN, Barron L, et al. 2011. Muc5ac: a critical component mediating the rejection of enteric nematodes. J Exp Med 208:893-900. doi: 10.1084/jem.20102057.
31. Hofmann T, Chubanov V, Gudermann T, Montell C. 2003. TRPM5 is a voltage-modulated and Ca(2+)-activated monovalent selective cation channel. Curr Biol 13:1153-8. doi: 10.1016/S0960-9822(03)00431-7.
32. Iwamoto T, Watano T, Shigekawa M. 1996. A novel isothiourea derivative selectively inhibits the reverse mode of Na+/Ca2+ exchange in cells expressing NCX1. J Biol Chem 271:22391-7. doi: 10.1074/jbc.271.37.22391.
33. Jerdeva GV, Wu K, Yarber FA, Rhodes CJ, Kalman D, Schechter JE, et al. 2005. Actin and non-muscle myosin II facilitate apical exocytosis of tear proteins in rabbit lacrimal acinar epithelial cells. J Cell Sci 118:4797-812. doi: 10.1242/jcs.02573.
34. Kemp PA, Sugar RA, Jackson AD. 2004. Nucleotide-mediated mucin secretion from differentiated human bronchial epithelial cells. Am J Respir Cell Mol Biol 31:446-55. doi: 10.1165/rcmb.2003-0211OC.
35. Kocer B, Soran A, Erdogan S, Karabeyoglu M, Yildirim O, Eroglu A, et al. 2002. Expression of MUC5AC in colorectal carcinoma and relationship with prognosis. Pathol Int 52:470-7. doi: 10.1046/j.1440-1827.2002.01369.x.
36. Li D, Carozza RB, Shatos MA, Hodges RR, Dartt DA. 2012. Effect of histamine on Ca(2+)-dependent signaling pathways in rat conjunctival goblet cells. Invest Ophthalmol Vis Sci 53:6928-38. doi: 10.1167/iovs.12-10163.
37. Li M, Li Q, Yang G, Kolosov VP, Perelman JM, Zhou XD. 2011. Cold temperature induces mucin hypersecretion from normal human bronchial epithelial cells in vitro through a transient receptor potential melastatin 8 (TRPM8)-mediated mechanism. J Allergy Clin Immunol 128:626-34 e1-5. doi: 10.1016/j.jaci.2011.04.032.
38. Lippincott-Schwartz J, Yuan LC, Bonifacino JS, Klausner RD. 1989. Rapid redistribution of golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from golgi to ER. Cell 56:801-13. doi: 10.1016/0092-8674(89)90685-5.
39. Liu D, Liman ER. 2003. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA 100:15160-5. doi: 10.1073/pnas.2334159100.
40. Lu S, Liu H, Farley JM Sr. 2011. Macrolide antibiotics inhibit mucus secretion and calcium entry in Swine airway submucosal mucous gland cells. J Pharmacol Exp Ther 336:178-87. doi: 10.1124/jpet.110.171561.
41. McGuckin MA, Linden SK, Sutton P, Florin TH. 2011. Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265-78. doi: 10.1038/nrmicro2538.
42. Neco P, Giner D, Viniegra S, Borges R, Villarroel A, Gutierrez LM. 2004. New roles of myosin II during vesicle transport and fusion in chromaffin cells. J Biol Chem 279:27450-7. doi: 10.1074/jbc.M311462200.
43. Nishimura M, Kuboi Y, Muramoto K, Kawano T, Imai T. 2009. Chemokines as novel therapeutic targets for inflammatory bowel disease. Ann N Y Acad Sci 1173:350-6. doi: 10.1111/j.1749-6632.2009.04738.x.
44. Okada SF, Zhang L, Kreda SM, Abdullah LH, Davis CW, Pickles RJ, et al. 2010. Coupled nucleotide and mucin hypersecretion from goblet-cell metaplastic human airway epithelium. Am J Respir Cell Mol Biol 45:253-60. doi: 10.1165/rcmb.2010-0253OC.
45. Perez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, et al. 2002. A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169-76. doi: 10.1038/nn952.
46. Perez-Vilar J, Olsen JC, Chua M, Boucher RC. 2005. pH-dependent intraluminal organization of mucin granules in live human mucous/goblet cells. J Biol Chem 280:16868-81. doi: 10.1074/jbc.M413289200.
47. Phillips TE, Ramos R, Duncan SL. 1995. HT29-18N2 differentiation in a protein-free medium. In Vitro Cell Dev Biol Anim 31:421-3. doi: 10.1007/BF02634251.
48. Rose MC, Voynow JA. 2006. Respiratory tract mucin genes and mucin glycoproteins in health and disease. Physiol Rev 86:245-78. doi: 10.1152/physrev.00010.2005.
49. Rose SD, Lejen T, Casaletti L, Larson RE, Pene TD, Trifaro JM. 2003. Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion. J Neurochem 85:287-98. doi: 10.1046/j.1471-4159.2003.01649.x.
50. Rosker C, Graziani A, Lukas M, Eder P, Zhu MX, Romanin C, et al. 2004. Ca(2+) signaling by TRPC3 involves Na(+) entry and local coupling to the Na(+)/Ca(2+) exchanger. J Biol Chem 279:13696-704. doi: 10.1074/jbc.M308108200.
51. Rozen S, Skaletsky H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365-86.
52. Rubin BK. 2010. Mucus and mucins. Otolaryngol Clin North Am 43:27-34. doi: 10.1016/j.otc.2009.11.002.
53. Serra SA, Cuenca-Leon E, Llobet A, Rubio-Moscardo F, Plata C, Carreno O, et al. 2010. A mutation in the first intracellular loop of CACNA1A prevents P/Q channel modulation by SNARE proteins and lowers exocytosis. Proc Natl Acad Sci USA 107:1672-7. doi: 10.1073/pnas.0908359107.
54. Shah BP, Liu P, Yu T, Hansen DR, Gilbertson TA. 2012. TRPM5 is critical for linoleic acid-induced CCK secretion from the enteroendocrine cell line, STC-1. Am J Physiol Cell Physiol 302:C210-9. doi: 10.1152/ajpcell.00209.2011.
55. Sheehan JK, Brazeau C, Kutay S, Pigeon H, Kirkham S, Howard M, et al. 2000. Physical characterization of the MUC5AC mucin: a highly oligomeric glycoprotein whether isolated from cell culture or in vivo from respiratory mucous secretions. Biochem J 347(Pt 1):37-44. doi: 10.1042/0264-6021:3470037.
56. Sheehan JK, Kirkham S, Howard M, Woodman P, Kutay S, Brazeau C, et al. 2004. Identification of molecular intermediates in the assembly pathway of the MUC5AC mucin. J Biol Chem 279:15698-705. doi: 10.1074/jbc.M313241200.
57. Slomiany BL, Slomiany A. 2005. Gastric mucin secretion in response to beta-adrenergic G protein-coupled receptor activation is mediated by SRC kinase-dependent epidermal growth factor receptor transactivation. J Physiol Pharmacol 56:247-58.
58. Stanley CM, Phillips TE. 1994. Bradykinin modulates mucin secretion but not synthesis from an intestinal goblet cell line. Agents Actions 42:141-5. doi: 10.1007/BF01983480.
59. Stumpo DJ, BOCK CB, Tuttle JS, Blackshear PJ. 1995. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc Natl Acad Sci USA 92:944-8. doi: 10.1073/pnas.92.4.944.
60. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, et al. 2005. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022-5. doi: 10.1038/nature04248.
61. Thornton DJ, Carlstedt I, Howard M, Devine PL, Price MR, Sheehan JK. 1996. Respiratory mucins: identification of core proteins and glycoforms. Biochem J 316(Pt 3):967-75.
62. Thornton DJ, Rousseau K, Mcguckin MA. 2008. Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol 70:459-86. doi: 10.1146/annurev.physiol.70.113006.100702.
63. Uchida K, Tominaga M. 2011. The role of thermosensitive TRP (transient receptor potential) channels in insulin secretion. Endocr J 58:1021-8. doi: 10.1507/endocrj.EJ11-0130.
64. van Klinken BJ, Einerhand AW, Buller HA, Dekker J. 1998. The oligomerization of a family of four genetically clustered human gastrointestinal mucins. Glycobiology 8:67-75. doi: 10.1093/glycob/8.1.67.
65. Vennekens R, Olausson J, Meissner M, Bloch W, Mathar I, Philipp SE, et al. 2007. Increased IgE-dependent mast cell activation and anaphylactic responses in mice lacking the calcium-activated nonselective cation channel TRPM4. Nat Immunol 8:312-20. doi: 10.1038/ni1441.
66. Verdugo P. 1993. Polymer gel phase transition in condensation-decondensation of secretory products. In: Dušek K, editor. Advances in Polymer Science. Springer Berlin Heidelberg. SpringerLink. p. 146-56. doi: 10.1007/BFb0021131.
67. Wollman R, Meyer T. 2012. Coordinated oscillations in cortical actin and Ca(2+) correlate with cycles of vesicle secretion. Nat Cell Biol 14:1261-9. doi: 10.1038/ncb2614.
68. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, et al. 2003. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293-301. doi: 10.1016/S0092-8674(03)00071-0.