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Article ; Online: The econobiology of pancreatic acinar cells granule inventory and the stealthy nano-machine behind it.

Hammel, Ilan / Meilijson, Isaac

2016 Volume 118, Issue 2, Page(s) 194–202

Abstract: The pancreatic gland secretes most of the enzymes and many other macromolecules needed for food digestion in the gastrointestinal tract. These molecules play an important role in digestion, host defense and lubrication. The secretion of pancreatic ... ...

Abstract	The pancreatic gland secretes most of the enzymes and many other macromolecules needed for food digestion in the gastrointestinal tract. These molecules play an important role in digestion, host defense and lubrication. The secretion of pancreatic proteins ensures the availability of the correct mix of proteins when needed. This review describes model systems available for the study of the econobiology of secretory granule content. The secretory pancreatic molecules are stored in large dense-core secretory granules that may undergo either constitutive or evoked secretion, and constitute the granule inventory of the cell. It is proposed that the Golgi complex functions as a distribution center for secretory proteins in pancreatic acinar cells, packing the newly formed secretory molecules into maturing secretory granules, also known functionally as condensing vacuoles. Mathematical modelling brings forward a process underlying granule inventory maintenance at various physiological states of condensation and aggregation by homotypic fusion. These models suggest unique but simple mechanisms accountable for inventory buildup and size, as well as for the distribution of secretory molecules into different secretory pathways in pancreatic acinar cells.
MeSH term(s)	Acinar Cells/secretion ; Acinar Cells/ultrastructure ; Animals ; Cytoplasmic Granules/physiology ; Diet ; Humans ; Pancreas/secretion ; Pancreas/ultrastructure ; Protein Transport ; Secretory Vesicles/physiology
Language	English
Publishing date	2016-03
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	77-2
ISSN	1618-0372 ; 0065-1281
ISSN (online)	1618-0372
ISSN	0065-1281
DOI	10.1016/j.acthis.2015.11.011
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Article ; Online: Function Suggests Nano-Structure: Quantitative Structural Support for SNARE-Mediated Pore Formation.

Hammel, Ilan / Meilijson, Isaac

Neurotoxicity research

2016 Volume 29, Issue 1, Page(s) 1–9

Abstract: Granule secretory content is released in either basal or calcium-activated complete exocytosis mode. A vital element in these processes is the establishment of a fusion pore between the granule membrane and the plasma membrane, initiated by the formation ...

Abstract	Granule secretory content is released in either basal or calcium-activated complete exocytosis mode. A vital element in these processes is the establishment of a fusion pore between the granule membrane and the plasma membrane, initiated by the formation of a circular rosette docking arrangement of SNARE protein complexes. The controversially disputed number of SNARE complexes needed for granule priming leading to the formation of the fusion pore, is granule-size dependent and varies between secretion modes. Resorting to a statistical mechanics approach that views SNARE complexes and Ca(2+) ions as interacting particles, we have developed a relationship that links secretion rate to SNARE rosette size, Ca(2+) concentration and Ca(2+) ion cooperativity. Data are presented and discussed which suggest this SNARE-dependent generalization of existing narrow-range biophysical models that correlate secretion rate with Ca(2+) concentration and maximal Ca(2+) ion cooperativity. Evidence from dozens of examples in the literature advocate for this relation, which holds through the entire biological range. The coalescence of so many areas of diverse research methodologies has greatly augmented our understanding of so many different sequences of granule life cycle. Accordingly, these new tools may become valuable in a variety of electrophysiological experiments.
MeSH term(s)	Animals ; Astacoidea ; Botulinum Toxins/pharmacology ; Exocytosis/drug effects ; Exocytosis/genetics ; Exocytosis/physiology ; Mice ; Mice, Knockout ; Neuromuscular Junction/drug effects ; Neuromuscular Junction/metabolism ; SNARE Proteins/genetics ; SNARE Proteins/metabolism ; Tetanus Toxin/pharmacology ; Vesicle-Associated Membrane Protein 1/deficiency ; Vesicle-Associated Membrane Protein 1/metabolism ; Vesicle-Associated Membrane Protein 2/deficiency ; Vesicle-Associated Membrane Protein 2/metabolism
Chemical Substances	SNARE Proteins ; Tetanus Toxin ; Vesicle-Associated Membrane Protein 1 ; Vesicle-Associated Membrane Protein 2 ; vesicle-associated membrane protein 1, mouse ; vesicle-associated membrane protein 2, mouse ; Botulinum Toxins (EC 3.4.24.69)
Language	English
Publishing date	2016-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	2036826-4
ISSN	1476-3524 ; 1029-8428
ISSN (online)	1476-3524
ISSN	1029-8428
DOI	10.1007/s12640-015-9559-3
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Article ; Online: The stealthy nano-machine behind mast cell granule size distribution.

Hammel, Ilan / Meilijson, Isaac

Molecular immunology

2015 Volume 63, Issue 1, Page(s) 45–54

Abstract: The classical model of mast cell secretory granule formation suggests that newly synthesized secretory mediators, transported from the rough endoplasmic reticulum to the Golgi complex, undergo post-transitional modification and are packaged for secretion ...

Abstract	The classical model of mast cell secretory granule formation suggests that newly synthesized secretory mediators, transported from the rough endoplasmic reticulum to the Golgi complex, undergo post-transitional modification and are packaged for secretion by condensation within membrane-bound granules of unit size. These unit granules may fuse with other granules to form larger granules that reside in the cytoplasm until secreted. A novel stochastic model for mast cell granule growth and elimination (G&E) as well as inventory management is presented. Resorting to a statistical mechanics approach in which SNAP (Soluble NSF Attachment Protein) REceptor (SNARE) components are viewed as interacting particles, the G&E model provides a simple 'nano-machine' of SNARE self-aggregation that can perform granule growth and secretion. Granule stock is maintained as a buffer to meet uncertainty in demand by the extracellular environment and to serve as source of supply during the lead time to produce granules of adaptive content. Experimental work, mathematical calculations, statistical modeling and a rationale for the emergence of nearly last-in, first out inventory management, are discussed.
MeSH term(s)	Animals ; Biological Transport ; Cell Fusion ; Cytoplasmic Granules/immunology ; Cytoplasmic Granules/secretion ; Humans ; Mast Cells/immunology ; Mice ; Models, Statistical ; Rats ; Rosette Formation ; SNARE Proteins/immunology ; Secretory Vesicles/immunology
Chemical Substances	SNARE Proteins
Language	English
Publishing date	2015-01
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	424427-8
ISSN	1872-9142 ; 0161-5890
ISSN (online)	1872-9142
ISSN	0161-5890
DOI	10.1016/j.molimm.2014.02.005
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Article ; Online: Quantal Basis of Secretory Granule Biogenesis and Inventory Maintenance: the Surreptitious Nano-machine Behind It.

Hammel, Ilan / Meilijson, Isaac

Discoveries (Craiova, Romania)

2014 Volume 2, Issue 3, Page(s) e21

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 ... ...

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.
Language	English
Publishing date	2014-09-02
Publishing country	Romania
Document type	Journal Article
ISSN	2359-7232
ISSN (online)	2359-7232
DOI	10.15190/d.2014.13
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Article: The stealthy nano-machine behind mast cell granule size distribution

Hammel, Ilan / Isaac Meilijson

Molecular Immunology. 2015 Jan., v. 63

2015

Abstract	The classical model of mast cell secretory granule formation suggests that newly synthesized secretory mediators, transported from the rough endoplasmic reticulum to the Golgi complex, undergo post-transitional modification and are packaged for secretion by condensation within membrane-bound granules of unit size. These unit granules may fuse with other granules to form larger granules that reside in the cytoplasm until secreted. A novel stochastic model for mast cell granule growth and elimination (G&E) as well as inventory management is presented. Resorting to a statistical mechanics approach in which SNAP (Soluble NSF Attachment Protein) REceptor (SNARE) components are viewed as interacting particles, the G&E model provides a simple ânano-machineâ of SNARE self-aggregation that can perform granule growth and secretion. Granule stock is maintained as a buffer to meet uncertainty in demand by the extracellular environment and to serve as source of supply during the lead time to produce granules of adaptive content. Experimental work, mathematical calculations, statistical modeling and a rationale for the emergence of nearly last-in, first out inventory management, are discussed.
Keywords	Golgi apparatus ; granules ; inventories ; mast cells ; mechanics ; rough endoplasmic reticulum ; secretion ; secretory granules ; statistical models ; stochastic processes ; uncertainty
Language	English
Dates of publication	2015-01
Size	p. 45-54.
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	424427-8
ISSN	1872-9142 ; 0161-5890
ISSN (online)	1872-9142
ISSN	0161-5890
DOI	10.1016/j.molimm.2014.02.005
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Function suggests nano-structure: towards a unified theory for secretion rate, a statistical mechanics approach.

Hammel, Ilan / Meilijson, Isaac

Journal of the Royal Society, Interface

2013 Volume 10, Issue 88, Page(s) 20130640

Abstract: The inventory of secretory granules along the plasma membrane can be viewed as maintained in two restricted compartments. The release-ready pool represents docked granules available for an initial stage of fast, immediate secretion, followed by a second ... ...

Abstract	The inventory of secretory granules along the plasma membrane can be viewed as maintained in two restricted compartments. The release-ready pool represents docked granules available for an initial stage of fast, immediate secretion, followed by a second stage of granule set-aside secretion pool, with significantly slower rate. Transmission electron microscopy ultra-structural investigations correlated with electrophysiological techniques and mathematical modelling have allowed the categorization of these secretory vesicle compartments, in which vesicles can be in various states of secretory competence. Using the above-mentioned approaches, the kinetics of single vesicle exocytosis can be worked out. The ultra-fast kinetics, explored in this study, represents the immediately available release-ready pool, in which granules bound to the plasma membrane are exocytosed upon Ca(2+) influx at the SNARE rosette at the base of porosomes. Formalizing Dodge and Rahamimoff findings on the effect of calcium concentration and incorporating the effect of SNARE transient rosette size, we postulate that secretion rate (rate), the number (X) of intracellular calcium ions available for fusion, calcium capacity (0 ≤ M ≤ 5) and the fusion nano-machine size (as measured by the SNARE rosette size K) satisfy the parsimonious M-K relation rate ≈ C × [Ca(2+)](min(X,M))e(-K/2).
MeSH term(s)	Animals ; Calcium/metabolism ; Humans ; Kinetics ; Membrane Fusion/physiology ; Models, Biological ; SNARE Proteins/metabolism ; Secretory Pathway/physiology ; Secretory Vesicles/metabolism ; Secretory Vesicles/ultrastructure
Chemical Substances	SNARE Proteins ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2013-09-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2156283-0
ISSN	1742-5662 ; 1742-5689
ISSN (online)	1742-5662
ISSN	1742-5689
DOI	10.1098/rsif.2013.0640
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Article ; Online: Function suggests nano-structure: electrophysiology supports that granule membranes play dice.

Hammel, Ilan / Meilijson, Isaac

Journal of the Royal Society, Interface

2012 Volume 9, Issue 75, Page(s) 2516–2526

Abstract: Cellular communication depends on membrane fusion mechanisms. SNARE proteins play a fundamental role in all intracellular fusion reactions associated with the life cycle of secretory vesicles, such as vesicle-vesicle and vesicle plasma membrane fusion at ...

Abstract	Cellular communication depends on membrane fusion mechanisms. SNARE proteins play a fundamental role in all intracellular fusion reactions associated with the life cycle of secretory vesicles, such as vesicle-vesicle and vesicle plasma membrane fusion at the porosome base in the cell plasma membrane. We present growth and elimination (G&E), a birth and death model for the investigation of granule growth, its evoked and spontaneous secretion and their information content. Using a statistical mechanics approach in which SNARE components are viewed as interacting particles, the G&E model provides a simple 'nano-machine' of SNARE self-aggregation behind granule growth and secretion. Results from experimental work, mathematical calculations and statistical modelling suggest that for vesicle growth a minimal aggregation of three SNAREs is required, while for the evoked secretion one SNARE is enough. Furthermore, the required number of SNARE aggregates (which varies between cell types and is nearly proportional to the square root of the mean granule diameter) affects and is statistically identifiable from the size distributions of spontaneous and evoked secreted granules. The new statistical mechanics approach to granule fusion is bound to have a significant changing effect on the investigation of the pathophysiology of secretory mechanisms and methodologies for the investigation of secretion.
MeSH term(s)	Cell Communication/physiology ; Computer Simulation ; Cytoplasmic Granules/physiology ; Cytoplasmic Granules/ultrastructure ; Electrophysiological Phenomena ; Markov Chains ; Membrane Fusion/physiology ; Microscopy, Atomic Force ; Microscopy, Electron, Transmission ; Models, Biological ; SNARE Proteins/physiology ; Secretory Vesicles/physiology ; Secretory Vesicles/ultrastructure ; Structure-Activity Relationship
Chemical Substances	SNARE Proteins
Language	English
Publishing date	2012-05-23
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2156283-0
ISSN	1742-5662 ; 1742-5689
ISSN (online)	1742-5662
ISSN	1742-5689
DOI	10.1098/rsif.2012.0161
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Article ; Online: Quantitative microscopy of mole rat eosinophil granule morphology.

Amihai, Dina / Meilijson, Isaac / Terkel, Joseph / Hammel, Ilan

Cell and tissue research

2015 Volume 362, Issue 1, Page(s) 139–151

Abstract: Mole rat bone marrow cells and peritoneal eosinophils are used to study granule morphological maturation by quantitative microscopy. The bulk eosinophil granule content is pre-stored in unique granular structures known as crystalloid or secondary ... ...

Abstract	Mole rat bone marrow cells and peritoneal eosinophils are used to study granule morphological maturation by quantitative microscopy. The bulk eosinophil granule content is pre-stored in unique granular structures known as crystalloid or secondary granules. Mole rat eosinophil granules exhibit the basic structure of an electron-dense crystalloid core surrounded by a lighter, homogeneous matrix. Morphometric analysis demonstrated that bone marrow-derived eosinophil sphere-like granules display a periodic, multimodal granule volume distribution. In contrast, peritoneal eosinophils display cigar-shaped granules, whose crystalloid cores are more variable in size and shape as compared to bone marrow eosinophil granules. Using a morphometric approach, we deduced that the basic granule volume quantum is similar in both cases, suggesting that the sphere-like young eosinophil granules turn into dense ellipsoidal ones by intragranular processes in which both volume and membrane surface are conserved. Crystalloid granule mediators are known to be widely associated with allergic inflammatory events, which may damage the host tissue following secretion to the extracellular environment. Based on mathematical modeling, we suggest that this deviation from sphere-like to ellipsoidal shape reflects an adaptive response of the mole rat to its unique solitary life.
MeSH term(s)	Animals ; Cytoplasmic Granules/physiology ; Eosinophils/physiology ; Microscopy/methods ; Mole Rats ; Rats
Language	English
Publishing date	2015-10
Publishing country	Germany
Document type	Journal Article
ZDB-ID	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-015-2189-5
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Article ; Online: Statistical analysis of the quantal basis of secretory granule formation.

Křepelová-Dror, Marika / Hammel, Ilan / Meilijson, Isaac

Microscopy research and technique

2014 Volume 77, Issue 1, Page(s) 1–10

Abstract: The size distribution of vesicles exocytosed from secretory cells displays quantal nature, vesicle volume is periodic multi-modal, suggesting that these heterogeneous vesicles are aggregate sums of a variable number of homogeneous basic granules. Whether ...

Abstract	The size distribution of vesicles exocytosed from secretory cells displays quantal nature, vesicle volume is periodic multi-modal, suggesting that these heterogeneous vesicles are aggregate sums of a variable number of homogeneous basic granules. Whether heterogeneity is a lumping-together artifact of the measurement or an inherent intra-cell feature of the vesicles is an unresolved question. Recent empirical evidence will be provided for the quantal nature of intra-cell vesicle volume, supporting the controversial paradigm of homotypic fusion: basic cytoplasmic granules fuse with each other to create heterogeneously sized vesicles. An EM-algorithm-based method is presented for the conversion of multi-modal to quantal data that provides as by-product estimates of means and variances of basic granule packaging.
MeSH term(s)	Animals ; Cell Biology/statistics & numerical data ; Cytoplasmic Granules/chemistry ; Cytoplasmic Granules/metabolism ; Data Interpretation, Statistical ; Humans ; Particle Size ; Proteins/metabolism ; Secretory Vesicles/chemistry ; Secretory Vesicles/metabolism ; Synaptic Vesicles/chemistry ; Synaptic Vesicles/metabolism
Chemical Substances	Proteins
Language	English
Publishing date	2014-01
Publishing country	United States
Document type	Journal Article
ZDB-ID	1099714-3
ISSN	1097-0029 ; 1059-910X
ISSN (online)	1097-0029
ISSN	1059-910X
DOI	10.1002/jemt.22305
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Article ; Online: Characterization of mast cell secretory granules and their cell biology.

Azouz, Nurit Pereg / Hammel, Ilan / Sagi-Eisenberg, Ronit

DNA and cell biology

2014 Volume 33, Issue 10, Page(s) 647–651

Abstract: Exocytosis and secretion of secretory granule (SG) contained inflammatory mediators is the primary mechanism by which mast cells exert their protective immune responses in host defense, as well as their pathological functions in allergic reactions and ... ...

Abstract	Exocytosis and secretion of secretory granule (SG) contained inflammatory mediators is the primary mechanism by which mast cells exert their protective immune responses in host defense, as well as their pathological functions in allergic reactions and anaphylaxis. Despite their central role in mast cell function, the molecular mechanisms underlying the biogenesis and secretion of mast cell SGs remain largely unresolved. Early studies have established the lysosomal nature of the mast cell SGs and implicated SG homotypic fusion as an important step occurring during both their biogenesis and compound secretion. However, the molecular mechanisms that account for key features of this process largely remain to be defined. A novel high-resolution imaging based methodology allowed us to screen Rab GTPases for their phenotypic and functional impact and identify Rab networks that regulate mast cell secretion. This screen has identified Rab5 as a novel regulator of homotypic fusion of the mast cell SGs that thereby regulates their size and cargo composition.
MeSH term(s)	Bone Marrow Cells/cytology ; Exocytosis ; Humans ; Inflammation Mediators/immunology ; Lysosomes ; Mast Cells/immunology ; Mast Cells/ultrastructure ; Membrane Fusion ; Secretory Vesicles/physiology ; rab5 GTP-Binding Proteins/metabolism
Chemical Substances	Inflammation Mediators ; rab5 GTP-Binding Proteins (EC 3.6.5.2)
Language	English
Publishing date	2014-07-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1024454-2
ISSN	1557-7430 ; 0198-0238 ; 1044-5498
ISSN (online)	1557-7430
ISSN	0198-0238 ; 1044-5498
DOI	10.1089/dna.2014.2543
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