Role of MARCKS in regulated secretion from mast cells and airway goblet cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 10, 2014, Pages

  Haddock, Brookelyn J ^a,b   Zhu, Yunxiang ^a   Doyle, Sean P ^a   Abdullah, Lubna H ^a   Davis, C William ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Airway goblet cells; Exocytosis; MANS peptide; MARCKS; Mast cells; Mucin secretion

Indexed keywords

MARCKS PROTEIN; MUCIN; REGULATOR PROTEIN; BETA N ACETYLHEXOSAMINIDASE; MEMBRANE PROTEIN; MYRISTOYLATED ALANINE-RICH C KINASE SUBSTRATE; PEPTIDE FRAGMENT; SIGNAL PEPTIDE;

AIRWAY; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CELLULAR SECRETION; EXOCYTOSIS; GOBLET CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAST CELL; MOUSE; NONHUMAN; NULL CELL; PRIORITY JOURNAL; PROTEIN DEFECT; ANIMAL; BRONCHUS; C57BL MOUSE; CELL CULTURE; CYTOLOGY; HUMAN; KINETICS; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; BRONCHI; CELLS, CULTURED; EXOCYTOSIS; GOBLET CELLS; HEXOSAMINIDASES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETICS; MAST CELLS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MUCINS; PEPTIDE FRAGMENTS;

EID: 84900819613     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00213.2013     Document Type: Article

References (66)

1. Abdullah LH, Wolber C, Kesimer M, Sheehan JK, Davis CW. Studying mucin secretion from human bronchial epithelial cell primary cultures. Methods Mol Biol 842: 259-277, 2012.
2. Aderem A. The MARCKS brothers: a family of protein kinase C substrates. Cell 71: 713-716, 1992.
3. Agrawal A, Rengarajan S, Adler KB, Ram A, Ghosh B, Fahim M, Dickey BF. Inhibition of mucin secretion with MARCKS-related peptide improves airway obstruction in a mouse model of asthma. J Appl Physiol 102: 399-405, 2007.
4. Allen LA, Aderem A. Protein kinase C regulates MARCKS cycling between the plasma membrane and lysosomes in fibroblasts. EMBO J 14: 1109-1121, 1995.
5. Arbuzova A, Schmitz AA, Vergeres G. Cross-talk unfolded: MARCKS proteins. Biochem J 362: 1-12, 2002.
6. Barker JE. Development of the mouse hematopoietic system. I. Types of hemoglobin produced in embryonic yolk sac and liver. Dev Biol 18: 14-29, 1968.
7. Blackshear PJ. The MARCKS family of cellular protein kinase C substrates. J Biol Chem 268: 1501-1504, 1993.
8. Borovikov YS, Norman JC, Price LS, Weeds A, Koffer A. Secretion from permeabilised mast cells is enhanced by addition of gelsolin: contrasting effects of endogenous gelsolin. J Cell Sci 108: 657-666, 1995.
9. Chapman ER. How does synaptotagmin trigger neurotransmitter release? Annu Rev Biochem 77: 615-641, 2008.
10. Conway JD, Bartolotta T, Abdullah LH, Davis CW. Regulation of mucin secretion from human bronchial epithelial cells grown in murine hosted xenografts. Am J Physiol Lung Cell Mol Physiol 284: L945-L954, 2003.
11. Davis CW, Dickey BF. Regulated airway goblet cell mucin secretion. Annu Rev Physiol 70: 487-512, 2008.
12. Ehre C, Rossi AH, Abdullah LH, De Pestel K, Hill S, Olsen JC, Davis CW. Barrier role of actin filaments in regulated mucin secretion from airway goblet cells. Am J Physiol Cell Physiol 288: C46-C56, 2005.
13. Fang S, Crews AL, Chen W, Park J, Yin Q, Ren XR, Adler KB. MARCKS and HSP70 interactions regulate mucin secretion by human airway epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol 304: L511-L518, 2013.
14. Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 107: 183-206, 2005.
15. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader MF. Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15: 520-531, 2004.
16. Green TD, Crews AL, Park J, Fang S, Adler KB. Regulation of mucin secretion and inflammation in asthma: a role for MARCKS protein? Biochim Biophys Acta 1810: 1110-1113, 2011.
17. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC, Aderem A. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356: 618-622, 1992.
18. Hernandez JM, Stein A, Behrmann E, Riedel D, Cypionka A, Farsi Z, Walla PJ, Raunser S, Jahn R. Membrane fusion intermediates via directional and full assembly of the SNARE complex. Science 336: 1581-1584, 2012.
19. Hua X, Kovarova M, Chason KD, Nguyen M, Koller BH, Tilley SL. Enhanced mast cell activation in mice deficient in the A2b adenosine receptor. J Exp Med 204: 117-128, 2007.
20. Huang C, Sali A, Stevens RL. Regulation and function of mast cell proteases in inflammation. J Clin Immunol 18: 169-183, 1998.
21. Inomata N, Tomita H, Ikezawa Z, Saito H. Differential gene expression profile between cord blood progenitor-derived and adult progenitor-derived human mast cells. Immunol Lett 98: 265-271, 2005.
22. Jamur MC, Grodzki AC, Berenstein EH, Hamawy MM, Siraganian RP, Oliver C. Identification and characterization of undifferentiated mast cells in mouse bone marrow. Blood 105: 4282-4289, 2005.
23. Kim K, Petrova YM, Scott BL, Nigam R, Agrawal A, Evans CM, Azzegagh Z, Gomez A, Rodarte EM, Olkkonen VM, Bagirzadeh R, Piccotti L, Ren B, Yoon JH, McNew JA, Adachi R, Tuvim MJ, Dickey BF. Munc18b is an essential gene in mice whose expression is limiting for secretion by airway epithelial and mast cells. Biochem J 446: 383-394, 2012.
24. Koffer A, Tatham PE, Gomperts BD. Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J Cell Biol 111: 919-927, 1990.
25. Kruger-Krasagakes S, Grutzkau A, Krasagakis K, Hoffmann S, Henz BM. Adhesion of human mast cells to extracellular matrix provides a co-stimulatory signal for cytokine production. Immunology 98: 253-257, 1999.
26. Kuehn HS, Gilfillan AM. G protein-coupled receptors and the modification of FcRI-mediated mast cell activation. Immunol Lett 113: 59-69, 2007.
27. Li J, Aderem A. MacMARCKS, a novel member of the MARCKS family of protein kinase C substrates. Cell 70: 791-801, 1992.
28. Li Y, Martin LD, Spizz G, Adler KB. MARCKS protein is a key molecule regulating mucin secretion by human airway epithelial cells in vitro. J Biol Chem 276: 40982-40990, 2001.
29. Lin H, Carlson DM, St George JA, Plopper CG, Wu R. An ELISA method for the quantitation of tracheal mucins from human and nonhuman primates. Am J Respir Cell Mol Biol 1: 41-48, 1989.
30. Lorentz A, Baumann A, Vitte J, Blank U. The SNARE machinery in mast cell secretion. Front Immunol 3: 143, 2012.
31. Malacombe M, Bader MF, Gasman S. Exocytosis in neuroendocrine cells: new tasks for actin. Biochim Biophys Acta 1763: 1175-1183, 2006.
32. McLaughlin S, Murray D. Plasma membrane phosphoinositide organization by protein electrostatics. Nature 438: 605-611, 2005.
33. Melicoff E, Sansores-Garcia L, Gomez A, Moreira DC, Datta P, Thakur P, Petrova Y, Siddigi T, Murthy JN, Dickey BF, Heidelberg R, Adachi R. Synaptotagmin 2 controls regulated exocytosis but not other secretory responses of mast cells. J Biol Chem 284: 19445-19451, 2009.
34. Melicoff E, Sansores-Garcia L, Gomez A, Moreira DC, Datta P, Thakur P, Petrova Y, Siddiqi T, Murthy JN, Dickey BF, Heidelberger R, Adachi R. Synaptotagmin-2 controls regulated exocytosis but not other secretory responses of mast cells. J Biol Chem 284: 19445-19451, 2009.
35. 2+ signalling, and then a deluge of other phosphoinositide functions. Cell Calcium 45: 521-526, 2009.
36. Miklavc P, Hecht E, Hobi N, Wittekindt OH, Dietl P, Kranz C, Frick M. Actin coating and compression of fused secretory vesicles are essential for surfactant secretion-a role for Rho, formins and myosin II. J Cell Sci 125: 2765-2774, 2012.
37. Muallem S, Kwiatkowska K, Xu X, Yin HL. Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 128: 589-598, 1995.
38. Nelson AR, Borland L, Allbritton NL, Sims CE. Myristoyl-based transport of peptides into living cells. Biochemistry 46: 14771-14781, 2007.
39. Nightingale TD, Cutler DF, Cramer LP. Actin coats and rings promote regulated exocytosis. Trends Cell Biol 22: 329-337, 2012.
40. Nightingale TD, White IJ, Doyle EL, Turmaine M, Harrison-Lavoie KJ, Webb KF, Cramer LP, Cutler DF. Actomyosin II contractility expels von Willebrand factor from Weibel-Palade bodies during exocytosis. J Cell Biol 194: 613-629, 2011.
41. Park J, Fang S, Adler KB. Regulation of airway mucin secretion by MARCKS protein involves the chaperones heat shock protein 70 and cysteine string protein. Proc Am Thorac Soc 3: 493, 2006.
42. Park J, Fang S, Crews AL, Lin KW, Adler KB. MARCKS regulation of mucin secretion by airway epithelium in vitro: interaction with chaperones. Am J Respir Cell Mol Biol 39: 68-76, 2008.
43. Park JJ, Loh YP. How peptide hormone vesicles are transported to the secretion site for exocytosis. Mol Endocrinol 22: 2583-2595, 2008.
44. Richard JF, Petit L, Gibert M, Marvaud JC, Bouchaud C, Popoff MR. Bacterial toxins modifying the actin cytoskeleton. Int Microbiol 2: 185-194, 1999.
45. Rivera J, Gilfillan AM. Molecular regulation of mast cell activation. J Allergy Clin Immunol 117: 1214-1225, 2006.
46. Ryzhov S, Zaynagetdinov R, Goldstein AE, Novitskiy SV, Dikov MM, Blackburn MR, Biaggioni I, Feoktistov I. Effect of A2B adenosine receptor gene ablation on proinflammatory adenosine signaling in mast cells. J Immunol 180: 7212-7220, 2008.
47. Sheehan JK, Boot-Handford RP, Chantler E, Carlstedt I, Thornton DJ. Evidence for shared epitopes within the 'naked' protein domains of human mucus glycoproteins. A study performed by using polyclonal antibodies and electron microscopy. Biochem J 274: 293-296, 1991.
48. Singer M, Martin LD, Vargaftig BB, Park J, Gruber AD, Li Y, Adler KB. A MARCKS-related peptide blocks mucus hypersecretion in a mouse model of asthma. Nat Med 10: 193-196, 2004.
49. Spector I, Braet F, Shochet NR, Bubb MR. New anti-actin drugs in the study of the organization and function of the actin cytoskeleton. Microsc Res Tech 47: 18-37, 1999.
50. St George JA, Cranz DL, Zicker SC, Etchison JR, Dungworth DL, Plopper CG. An immunohistochemical characterization of rhesus monkey respiratory secretions using monoclonal antibodies. Am Rev Respir Dis 132: 556-563, 1985.
51. Stumpo DJ, Bock CB, Tuttle JS, Blackshear PJ. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc Natl Acad Sci USA 92: 944-948, 1995.
52. Stumpo DJ, Graff JM, Albert KA, Greengard P, Blackshear PJ. Molecular cloning, characterization, and expression of a cDNA encoding the "80-to 87-kDa" myristoylated alanine-rich C kinase substrate: a major cellular substrate for protein kinase C. Proc Natl Acad Sci USA 86: 4012-4016, 1989.
53. Sudhof TC, Rothman JE. Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477, 2009.
54. Sudo N, Tanaka K, Koga Y, Okumura Y, Kubo C, Nomoto K. Extracellular ATP activates mast cells via a mechanism that is different from the activation induced by the cross-linking of Fc receptors. J Immunol 156: 3970-3979, 1996.
55. Sundaram M, Cook HW, Byers DM. The MARCKS family of phospholipid binding proteins: regulation of phospholipase D and other cellular components. Biochem Cell Biol 82: 191-200, 2004.
56. Takashi S, Park J, Fang S, Koyama S, Parikh I, Adler KB. A peptide against the N-terminus of myristoylated alanine-rich C kinase substrate inhibits degranulation of human leukocytes in vitro. Am J Respir Cell Mol Biol 34: 647-652, 2006.
57. Trifaro JM, Gasman S, Gutierrez LM. Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) 192: 165-172, 2008.
58. Trifaro JM, Lejen T, Rose SD, Pene TD, Barkar ND, Seward EP. Pathways that control cortical F-actin dynamics during secretion. Neurochem Res 27: 1371-1385, 2002.
59. 2+-dependent actin filament severing protein that controls cortical actin network dynamics during secretion. Neurochem Res 25: 133-144, 2000.
60. Tsai M, Tam SY, Wedemeyer J, Galli SJ. Mast cells derived from embryonic stem cells: a model system for studying the effects of genetic manipulations on mast cell development, phenotype, and function in vitro and in vivo. Int J Hematol 75: 345-349, 2002.
61. 2+ signaling from endoplasmic reticulum. J Biol Chem 284: 9781-9787, 2009.
62. Valentijn K, Valentijn JA, Jamieson JD. Role of actin in regulated exocytosis and compensatory membrane retrieval: insights from an old acquaintance. Biochem Biophys Res Commun 266: 652-661, 1999.
63. Wang J, Gambhir A, Hangyas-Mihalyne G, Murray D, Golebiewska U, McLaughlin S. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J Biol Chem 277: 34401-34412, 2002.
64. 2+ correlate with cycles of vesicle secretion. Nat Cell Biol 14: 1261-1269, 2012.
65. Xia HZ, Du Z, Craig S, Klisch G, Noben-Trauth N, Kochan JP, Huff TH, Irani AM, Schwartz LB. Effect of recombinant human IL-4 on tryptase, chymase, and Fc epsilon receptor type I expression in recombinant human stem cell factor-dependent fetal liver-derived human mast cells. J Immunol 159: 2911-2921, 1997.
66. Zhang L, Mao YS, Janmey PA, Yin HL. Phosphatidylinositol 4, 5 bisphosphate and the actin cytoskeleton. Subcell Biochem 59: 177-215, 2012.