DISCOVERIES (ISSN 2359-7232), 2014, July-September

CITATION: 

Hammel I and Meilijson I. Quantal Basis of Secretory Granule Biogenesis and Inventory Maintenance: the Surreptitious Nano-machine Behind It. Discoveries 2014, Jul-Sep; 2(3): e21. DOI: 10.15190/d.2014.13 

Submitted: June 11, 2014; Revised: August 14, 2014; Accepted: August 25, 2014; Published: September 02, 2014; 

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Quantal Basis of Secretory Granule Biogenesis and Inventory Maintenance: the Surreptitious Nano-machine Behind It

Ilan Hammel (1)* and Isaac Meilijson (2)*

(1) Sackler Faculty of Medicine, Department of Pathology, Tel Aviv University, Tel Aviv 6997801, Israel

(2) Raymond and Beverly Sackler Faculty of Exact Sciences, School of Mathematical Sciences, Department of Statistics and Operations Research, Tel Aviv University, Tel Aviv 6997801, Israel 

*Correspondence to: 

Professor Ilan Hammel, Department of Pathology, Tel Aviv University, Tel Aviv 6997801, Israel; Phone: +972-3-640-8408; Fax: +972-3-640-9141; E-mail: ilanh@patholog.tau.ac.il;

Professor Isaac Meilijson, Department of Statistics and Operations Research, Tel Aviv University, Tel Aviv 6997801, Israel; Phone: +972-3-640-8826; Fax: +972-3-640-9357 (Fax); E-mail: isaco@math.tau.ac.il  

Abstract

Proteins are molecular machines with the capacity to perform diverse physical work as response to signals from the environment. Proteins may be found as monomers or polymers, two states that represent an important subset of protein interactions and generate considerable functional diversity, leading to regulatory mechanisms closely akin to decision-making in service systems. Polymerization is not unique to proteins. Other cell compartments (e.g. secretory granules) or tissue states (e.g. miniature end plate potential) are associated with polymerization of some sort, leading to information transport. This data-processing mechanism has similarities with (and led us to the investigation of) granule homotypic polymerization kinetics. Using information theory, we demonstrate the role played by the heterogeneity induced by polymerization: granule size distribution and the stealthy machine behind granule life cycle increase system entropy, which modulates the source/receiver potential that affects communication between the cell and its environment. The granule inventory management by the same nano-machine is discussed.

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References:

1. Gatlin LL. (1972) Information Theory and the Living System. (Columbia Univ. Press, New York).

2. Del Castillo J, Katz B. Statistical nature of facilitation at a single nerve-muscle junction. Nature. 1953;171:1016-7.

3. Del Castillo J, Katz B. Quantal components of the end-plate potential. J Physiol. 1954;124:560-73.

4. Katz B. Elementary components of synaptic transmission. Naturwissenschaften. 1979;66:606-10.

5. Hammel I, Lagunoff D, Galli SJ. Regulation of secretory granule size by the precise generation and fusion of unit granules. J Cell Mol Med. 2010;14:1904-16.

6. Weiss A, Schlessinger J. Switching signals on or off by receptor dimerization. Cell. 1998;94:277-80.

7. Muñoz LM, Holgado BL, Martínez-A C, Rodríguez-Frade JM, Mellado M. Chemokine receptor oligomerization: a further step toward chemokine function. Immunol Lett. 2012;145:23-9. 

8. Nitzany E, Hammel I, Meilijson I. Quantal basis of vesicle growth and information content, a unified approach. J Theor Biol. 2010;266:202-9.

9. Hammel I, Meilijson I. Function suggests nano-structure: electrophysiology supports that granule membranes play dice. J R Soc Interface. 2012;9:2516-26.

10. Burwen SJ, Satir BH. A freeze-fracture study of early membrane events during mast cell secretion. J Cell Biol. 1977;73:660-71.

11. Hammel I, Meilijson I. Function suggests nano-structure: towards a unified theory for secretion rate, a statistical mechanics approach. J R Soc Interface. 2013;10:20130640. doi: 10.1098/rsif.2013.0640

12. Dancoff SM, Quastler H. (1953). The Information Content and Error Rate of Living Things. In Henry Quastler (Ed.). Essays on the Use of Information Theory in Biology. Urbana: University of Illinois Press.

13. Adami C. The use of information theory in evolutionary biology. Ann N Y Acad Sci. 2012;1256:49-65

14. Ulanowicz RE. Information theory in ecology. Comput Chem. 2001;25:393-9.

15. Shannon CE, Weaver W (1949) The Mathematical Theory of Communication. The University of Illinois Press, Urbana, Illinois.

16. Flory P. (1953) Principles of Polymer Chemistry. Cornell University Press. 

17. Flory P. (1969) Statistical Mechanics of Chain Molecules. Interscience

18. Hammel I, Lagunoff D, Wysolmerski R. Theoretical considerations on the formation of secretory granules in the rat pancreas. Exp Cell Res. 1993;204:1-5.

19. Hammel I, Anaby D. Imaging of zymogen granules in fully wet cells: evidence for restricted mechanism of granule growth. Microsc Res Tech. 2007;70:790-5.

20. Papahadjopoulos D, Nir S, Düzgünes N. Molecular mechanisms of calcium-induced membrane fusion. J Bioenerg Biomembr. 1990;22:157-79.

21. Hammel I, Meilijson I. The stealthy nano-machine behind mast cell granule size distribution. Mol Immunol. pii: 2014;S0161-5890(14)00032-7. doi:10.1016/ j.molimm.2014.02.005.

22. Dodge FA Jr, Rahamimoff R. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J Physiol. 1967;193:419-32.

23. Peled ES, Newman ZL, Isacoff EY. Evoked and spontaneous transmission favored by distinct sets of synapses. Curr Biol. 2014;24:484-93.

24. Payne CM. Phylogenetic considerations of neurosecretory granule contents: role of nucleotides and basic hormone/transmitter packaging mechanisms. Arch Histol Cytol. 1989;52 Suppl:277-92.

25. Choi BJ, Imlach WL, Jiao W, Wolfram V, Wu Y, Grbic M, Cela C, Baines RA, Nitabach MN, McCabe BD. Miniature neurotransmission regulates Drosophila synaptic structural maturation. Neuron. 2014;82:618-34. 

26. Pang ZP, Südhof TC. Cell biology of Ca2+-triggered exocytosis. Curr Opin Cell Biol. 2010;22:496-505

27. Neher E, Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 2008;59:861-72.

28. Page ES. Continuous Inspection Scheme. Biometrika 1954;41:100–115. 

29. Lorden G. Procedures for reacting to a change in distribution. Ann Math Statist. 1971;42: 1897-1908.

30. Moustakides  GV. Optimal stopping times for detecting changes in distributions. Ann Statist. 1986;14:1379–87.

31. Neyman J, Pearson ES. On the Problem of the Most Efficient Tests of Statistical Hypotheses. Philos T R Soc A 1933;231:289–337

32. Ritov Y, Raz A, Bergman H. Detection of onset of neuronal activity by allowing for heterogeneity in the change points. J Neurosci Methods. 2002;122:25-42.

33. Pillow JW, Ahmadian Y, Paninski L. Model-based decoding, information estimation, and change-point detection techniques for multineuron spike trains. Neural Comput. 2011;23:1-45. 

34. Case RM. Synthesis, intracellular transport and discharge of exportable proteins in the pancreatic acinar cell and other cells. Biol Rev Camb Philos Soc. 1978:53, 211-354.

35. Arvan P, Castle D. Sorting and storage during secretory granule biogenesis: looking backward and looking forward. Biochem J. 1998;332:593-610.

36. Kögel T, Gerdes HH. Maturation of secretory granules. Results Probl Cell Differ. 2010;50:1-20.

37. Azouz NP, Zur N, Efergan A, Ohbayashi N, Fukuda M, Amihai D, Hammel I, Rothenberg ME, Sagi-Eisenberg R. Rab5 is a novel regulator of mast cell secretory granules: impact on size, cargo, and exocytosis. J Immunol. 2014;192:4043-53.

38. Galli SJ, Tsai M. Mast cells: versatile regulators of inflammation, tissue remodeling, host defense and homeostasis. J Dermatol Sci. 2008;49:7-19. 

39. Galli SJ, Borregaard N, Wynn TA. Phenotypic and functional plasticity of cells of innate immunity: macrophages, mast cells and neutrophils. Nat Immunol. 2011;12:1035-44. 

40. Mason-Jones R, Towill DR. Information enrichment: designing the supply chain for competitive advantage. Supply Chain Manag 1997;2:137-149.

41.Christopher M, Towill D. Developing market specific supply chain strategies. Int J Logist Manag. 2002;13:1-14.

42. Cohen MA, Pekelman D.  LIFO inventory systems. Management Science. 1978;24:1150-1162

43. Dietl P, Haller T. Exocytosis of lung surfactant: from the secretory vesicle to the air-liquid interface. Annu Rev Physiol. 2005;67:595-621.

44. Adelson JW, Miller PE. Heterogeneity of the exocrine pancreas. Am J Physiol. 1989; 256:G817-25.

45. Adelson JW, Clarizio R, Coutu JA.. Pancreatic digestive enzyme secretion in the rabbit: rapid cyclic variations in enzyme composition. Proc Natl Acad Sci USA. 1995;92:2553-7.

46. Solimena M, Gerdes HH. Secretory granules: and the last shall be first. Trends Cell Biol. 2003;13, 399-402.

47. Rorsman P, Braun M. Regulation of insulin secretion in human pancreatic islets. Annu Rev Physiol. 2013;75:155-79.

48. Hammel I, Lagunoff D, Krüger PG. Recovery of rat mast cells after secretion: a morphometric study. Exp Cell Res. 1989;184:518-23.

49. Elmalek M, Hammel I. Morphometric evidence that the maturation of the eosinophil granules is independent of volume change. J Submicrosc Cytol. 1987;19:265-8.

50. Padawer J. Uptake of colloidal thorium dioxide by mast cells. J Cell Biol. 1969;40:747-60.

51. Lew S, Hammel I,  Galli SJ. Cytoplasmic granule formation in mouse pancreatic acinar cells. Evidence for formation of immature granules (condensing vacuoles) by aggregation and fusion of progranules of unit size, and for reductions in membrane surface area and immature granule volume during granule maturation. Cell Tissue Res. 1994; 278, 327-36.

52. Jena BP. Functional organization of the porosome complex and associated structures facilitating cellular secretion. Physiology (Bethesda) 2009;24:367-76.

53. Jena BP. Role of SNAREs in Membrane Fusion. Adv Exp Med Biol. 2011;713:13-32.

54. Chernomordik LV, Kozlov MM. Mechanics of membrane fusion. Nat Struct Mol Biol. 2008;15:675–683.

55. Hua Y, Scheller RH. Three SNARE complexes cooperate to mediate membrane fusion. Proc Natl Acad Sci USA. 2001;98:8065–8070.

56. Jahn R. Principles of exocytosis and membrane fusion. Ann N Y Acad Sci. 2004;1014:170-8.

57. Montecucco C, Schiavo G, Pantano S. SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem Sci. 2005;30:367-72.

58. Wickner W. Membrane fusion: five lipids, four SNAREs, three chaperones, two nucleotides, and a Rab, all dancing in a ring on yeast vacuoles. Annu Rev Cell Dev Biol. 2010;26:115-36.

59. Goubau C, Buyse GM, Di Michele M, Van Geet C, Freson K. Regulated granule trafficking in platelets and neurons: a common molecular machinery. Eur J Paediatr Neurol. 2013;17:117-25.

60. Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood. 1997; 89:3503-21. 

61. Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007;28:340-5. 

62. Häger M, Cowland JB, Borregaard N. Neutrophil granules in health and disease. J Intern Med. 2010;268:25-34.

63. Rendu F, Brohard-Bohn B. The platelet release reaction: granules' constituents, secretion and functions. Platelets. 2001;12:261-73

64. Reed GL. Platelet secretory mechanisms. Semin Thromb Hemost. 2004;30:441-50. 

65. Koseoglu S, Flaumenhaft R. Advances in platelet granule biology. Curr Opin Hematol. 2013;20:464-71. 

66. Kavalali ET, Chung C, Khvotchev M, Leitz J, Nosyreva E, Raingo J, Ramirez DM. Spontaneous neurotransmission: an independent pathway for neuronal signaling? Physiology (Bethesda). 2011;26:45-53.

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