International Review of Cell and Molecular Biology

332 Pages·2012·6.665 MB·1-332\332

by  Kwang W. Jeon (Eds.)

International Review of Cell
and Molecular Biology
Series Editors
GEOFFREY H. BOURNE 1949–1988
JAMES F. DANIELLI 1949–1984
KWANG W. JEON 1967–
MARTIN FRIEDLANDER 1984–1992
JONATHAN JARVIK 1993–1995
Editorial Advisory Board
ISAIAH ARKIN WALLACE F. MARSHALL
PETER L. BEECH BRUCE D. MCKEE
ROBERT A. BLOODGOOD MICHAEL MELKONIAN
DEAN BOK KEITH E. MOSTOV
KEITH BURRIDGE ANDREAS OKSCHE
HIROO FUKUDA MADDY PARSONS
RAY H. GAVIN MANFRED SCHLIWA
MAY GRIFFITH TERUO SHIMMEN
WILLIAM R. JEFFERY ROBERT A. SMITH
KEITH LATHAM ALEXEY TOMILIN
VOLUME TWONINETY -NINE
I R
NTERNATIONAL EVIEW OF
CELL AND MOLECULAR
BIOLOGY
Edited by
KWANG W. JEON
Department of Biochemistry
University of Tennessee
Knoxville, Tennessee
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CONTRIBUTORS
Vanessa Bell
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University, Durham,NC;Department ofBiology, North Carolina CentralUniversity,
Durham,NC
Sarah Cohen
Department of Zoology, University of BritishColumbia, Vancouver, BC, Canada
Gregory J.Cole
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University, Durham,NC;Department ofBiology, North Carolina CentralUniversity,
Durham,NC
Frank P.Conte
Department of Zoology, Oregon State University, Corvallis, OR
Shailendra Devkota
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University, Durham,NC
Igor Etingov
Department of Zoology, University of BritishColumbia, Vancouver, BC, Canada
Mara Gladstone
Department of Molecular, Cellular andDevelopmental Biology,University of Colorado,
Boulder, CO,USA
Marjorie C.Gondré-Lewis
Laboratory for Neurodevelopment, Department of Anatomy, Howard University College
of Medicine, Washington, DC, USA
Natalia V. Katolikova
Institute of Cytology, Russian Academy of Sciences,St Petersburg, Russia
Y. Peng Loh
Section onCellular Neurobiology, Program on Developmental Neuroscience, Eunice
Kennedy Shriver NationalInstitute of ChildHealth and HumanDevelopment, National
Institutes of Health,Bethesda, MD, USA
Somnath Mukhopadhyay
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University, Durham,NC;Department ofChemistry, North Carolina CentralUniversity,
Durham,NC
j
ix
x Contributors
Princess Ojiaku
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University,Durham, NC;Department of Biology, North CarolinaCentral University,
Durham,NC
NellyPanté
Department of Zoology, University of BritishColumbia, Vancouver, BC,Canada
Joshua J.Park
Department of Neurosciences, University of Toledo School of Medicine, Toledo,OH,
USA
Valery A.Pospelov
Institute ofCytology, Russian Academy ofSciences, StPetersburg, Russia; StPetersburg
State University, Russia
Domenico Ribatti
Department of Basic MedicalSciences, Section of HumanAnatomy and Histology,
University of Bari MedicalSchool, Bari,Italy
Tin Tin Su
Department of Molecular, Cellular andDevelopmental Biology,University of Colorado,
Boulder, CO,USA
Irina I.Suvorova
Institute ofCytology, Russian Academy ofSciences, StPetersburg, Russia; StPetersburg
State University, Russia
Chengjin Zhang
JuliusL.ChambersBiomedical/Biotechnology ResearchInstitute,NorthCarolinaCentral
University,Durham, NC
CHAPTER ONE
Origin and Differentiation of
Ionocytes in Gill Epithelium
of Teleost Fish
Frank P. Conte
DepartmentofZoology,OregonStateUniversity,Corvallis,OR
Contents
1. Introduction 2
2. BiologyofEpithelialCellsoftheGill 3
2.1. MorphologyofGillEpithelium 3
2.1.1. MRCinFW-Fish 3
2.1.2. MRCinSWFish 3
2.2. OriginofICinAdultGillEpithelium 4
2.3. ProgenitorIonocyteandOrigininEmbryonicTissues 5
2.3.1. YolkMembraneMRCActingaspICforLarvalSkin 5
2.3.2. IBinPre-gillEpidermisandFormationofpIC 6
2.4. CellularRenewalinGillEpithelium 7
2.4.1. ApoptosisMechanism 7
2.4.2. ApoptosisinAdultGillIC 8
2.4.3. Non-apoptosisinEmbryonicskIC 8
2.4.4. ApoptoticReceptorMoleculesLocatedintheApicalPlasmalemma 8
2.5. SubcellularDifferentiationinGillIC 9
2.5.1. AquaporinDomainasOsmosensorReceptorSiteinApicalCrypt 10
2.5.2. RecyclingofApicalPlasmaMembraneinAdultGillEpithelium 11
2.5.3. RecyclingofIntracellularMembraneNetworkinSkinandOpercular 11
Epithelium
3. SalinityAdaptationinDevelopmentofOpercular/SkinEpitheliumversus 13
FilamentalGillEpithelium
4. GenomicPathwaysUnderlyingFunctionalDualisminFilamentalGillIC 16
4.1. FoxOGenesandInitiationofApoptosis 17
4.2. Grainyhead/CP2GenesandIntercellularJunctionalComplexes 17
4.3. Isotocin(Isotocin-Neurophysin)orOsmopoietinasHeteroproteinRegulator 18
5. ConcludingRemarks 18
GlossaryofTerms 21
Acknowledgments 22
References 22
InternationalReviewofCellandMolecularBiology,Volume299 (cid:1)2012ElsevierInc. j
1
ISSN1937-6448, Allrightsreserved.
http://dx.doi.org/10.1016/B978-0-12-394310-1.00001-1
2 FrankP.Conte
Abstract
This paper focuses on the environmental cues that transform the gills of euryhaline
teleost fish from an oxygen exchange structure into a bifunctional organ that can
control both gaseous movement and water/ion transport. The cellular development
thatallowsthisstructuretoaccomplishthesetasksbeginsshortlyafterfertilizationof
theegg.Itinvolvesalterationsofstructureandfunctionofembryoniccells[ionoblasts
(IB)] that are shed from the pharyngeal anlage area of the embryo. These IB contain
uniqueprotein-receptordomainsintheplasmamembrane.Thesereceptorsrespond
specifically to the environmental cues effecting a calcium-binding protein receptor
[calcium-sensing receptor (CaSR)]. The CaSR containing IB act as stem cells and are
acted upon by isotocin, a heteroprotein regulator which induces them to form
progenitorionocytes(pIC).ThepICformtwotypesofcells.Thefirsttypebecomesan
aquaphilicionocytewhichregulatesuptakeofionsandthroughaquaporinmolecules
transportswateroutofthecellandcontrolsbodyfluidsofthefish.Thismechanismis
essential for freshwater living. The second type becomes a halophilic ionocyte and
transports ions out of the cell and controls cell shrinkage by uptake of water via
aquaporin molecules. This mechanism isessential forseawater living.These differen-
tiating eventsin thepICarecontrolledbythecrosstalkingofgenomic mechanisms
foundintheprecursorIB.Tounravelthecrosstalkingeventsitisnecessarytouncover
howthesegeneticpathwaysareregulatedbytranscriptionalandtranslationalevents
coming from complementary DNA. Variousgene familiesare involvedsuch asthose
found in apoptosis mechanisms, regulatory volume regulators and ionic transport
systems(cysticfibrosistransmembraneconductanceregulator).
1. INTRODUCTION
Theadulteuryhalineteleostfishcontainsanepitheliuminthegillarch
that undergoes molecular rearrangements which provide the fish with
physiological mechanisms to live in both freshwater (FW) and seawater
environments (Evans et al., 1999, 2005; Marshall and Bellamy, 2010;
Kaneko et al., 2008; Hwang et al., 2011). These investigations have not
focusedonhowthegeneticpathwaysunderlyingthesephysiologicalevents
occurduringvariousstagesoffishdevelopment.Thepurposeofthischapter
is to review how the environmental cues that act upon the surface
membrane osmoreceptor sites activate plasma membrane phosphorylation
kinases to initiate differentiation in embryonic epidermal cells [ionoblasts
(IB)].TheseIBarestemcellswhichformmatureionocytes(IC).Thekinases
begintheintracellulareventsinIBviacrosstalkingofgeneticfamilies,such
as GCM2, FoxO, Notch, Grainyhead, etc. These gene products start
restructure of the intracellular membrane network which is responsible for
water and ion movement across or into the cell from the environment.
OriginandDifferentiationofIonocytesinGillEpitheliumofTeleostFish 3
These intracellular events appear to involve in apoptosis mechanisms or its
inhibition by autoregulatory mechanisms that occur between nuclear and
mitochondrial genes.
2. BIOLOGY OF EPITHELIAL CELLS OF THE GILL
2.1. Morphology of Gill Epithelium
The filamental epithelial cells found in the region between respiratory
leafletsareofthreetypesofmaturecells.Theyarethepavementcell(PVC),
the mitochondria-rich cell (MRC), and the accessory cell (AC). The
anatomicalandultrastructuralfeaturesofthesecellsweredescribedindetail
by Wilson and Laurent (2002).
2.1.1. MRC in FW-Fish
TheroleofMRCinbothFWandsaltwater(SW)fishhadbeencalledearlier
as being a "chloride cell" by Keys and Wilmer (1932) and involved in ion
regulation.Lignotetal.(2002)andWatanabeetal.(2005)demonstratedthe
presenceoflargeamountsofanisoformofaquaporinmolecules(AQP3)in
thesecells.Thismoleculeregulateswaterpermeability.Subsequently,Perry
(1997) and Hwang and Perry (2010) reported that in FW-fish, MRCs
contain large numbers of proteins that transport ions. They have been
described as being proteomic ion pumps (Wheatly and Gao, 2004). These
proteomicionpumps are proteinsthatare translated frommessenger RNA
(mRNA)whicharesubjectedtoawidevarietyofchemicalmodificationsin
differentiatingcells.InFW-fish,theMRCsfacilitatesodiumion(Naþ)and
calcium ion (Ca2þ) uptake while removing protons (Hþ) and bicarbonate
(cid:2)
ions(HCO ).Therefore,theseMRCsareinvolvedinseveralcomplexion
3
regulatorymechanisms.Inaddition,thesecellsregulatewatermovementvia
control of plasma volume (Hoffman et al., 2009). While it appears that
MRCs also deal with changes of fluid volume and acid-base balance, they
clearlyarenotjustchloridecellsorMRCs.TheyfunctionasICbutdueto
the complex array of functions should more appropriately be called aqua-
philic ionocytes (aqIC).
2.1.2. MRC in SW Fish
In SW fish, the role of the MRCs has been shown to be the cells which
containothertypesofproteomicionpump(WheatlyandGao,2004).These
þ
protein pumps handle several other types of ions, such as sodium (Na ),
4 FrankP.Conte
Figure1.1 ModelofICinseawater.FordetailsreferSection1.2.2inthetext.Ref.Hwang
etal.(2011).
calcium (Ca2þ), potassium (Kþ) and chloride (Cl(cid:2)) ions. A currently
accepted model (Fig. 1.1) for salt excretion by MRC cells consists of the
cooperative action of three major enzymatic ion transporters: Na/K-
ATPase,Na/K/2Clco-transporter,andcysticfibrosisconductanceregulator
[cysticfibrosistransmembraneconductanceregulator(CFTR)]attheapical
pit which together with NHE2 and NHE3 apical membrane transporters
maintain ion movement via the intracellular membrane network forming
thechloridechannel(Hwangetal.,2011).Therefore,itismoreappropriate
to refer to these epithelial cells as not being just large cells containing
numerousmitochondriaorMRCs.ThesearecomplexICwhichhavemany
intracellular mechanism(s) required for salt excretion and water retention
and should be called halophilic ionocytes (haIC).
2.2. Origin of IC in Adult Gill Epithelium
Ionocytogenesis was a term first proposed by Conte (1980), in which any
typeofnoninvasivephysicalorchemicalforcethatcandamagethegillarch
initiates a replacement of the damaged cells. These replacement cells were
derived from MRC found in the filamental region and not from the
OriginandDifferentiationofIonocytesinGillEpitheliumofTeleostFish 5
respiratoryleafletarea.Thus,thegill’sabilitytofunctionasanion-excretory
organ depended upon this cellular renewal within the filamental region
(Conte, 1965; Conte and Lin, 1967; Motais, 1970). These new MRCs
required DNA replication to form postmitotic daughter cells. These
daughter cells, containing newly formed DNA, could continue to follow
genetic transcriptional and cellular translational pathways to conclude
differentiating events that eventually produced mature IC. These pIC cells
were located in the undifferentiated MRCs in contact with the basement
membrane (Chretien and Pisam, 1986; Uchida and Kaneko, 1996). Thus,
there was an urgency to find out what was the environmental cue that
initiates cellular differentiation and makes them behave as if they were
inducibleadultstemcells.Unfortunately,thisconceptlanguishedduetothe
inability of investigators at that time to carry out the necessary experiments
whichwouldprovetheexistenceornonexistenceofadultstemcells.What
turnsouttobeanimportanteventwasthefindingthatturnovertimeofthe
newlyformedmatureICwasaboutthesamenumberofdays(5-7)inorder
tocompletethefullformationofnumerousmatureICneededinlong-term
SW residency.
2.3. Progenitor Ionocyte and Origin in Embryonic Tissues
Recent investigations of the various forms of MRCs in zebra fish embryos
have led to the role of presumptive epidermal blastocysts (IB) being trans-
formedintowanderingprogenitorcells[progenitorionocyte(pIC)]forboth
aqIC and haIC. It was thought that the epidermal cell, being a blastocyst,
could act as a pluripotential type of stem cell. This cell could then form all
types of mature IC (Hwang et al., 2011; Jancike et al., 2010; Chou et al.,
2011).
2.3.1. Yolk Membrane MRC Acting as pIC for Larval Skin
Priortotheworkonthedevelopmentofzebrafishembryos,theearlychum
salmon embryo had demonstrated that the embryo had the physiological
abilitytofunctionhypoosmotically.Inthelateembryonicstate(eyedstage)
the embryo could regulate perivitelline fluid osmotically and ionically
followingtransfertofullseawater(Kanekoetal.,1995,2008).Theseresults
suggestedthattheeyed-stageembryoofchumsalmonhadalreadyacquired
some type of IC mechanism.
Sincetheexperimentalevidenceforthesubstantiationofadultstemcell
differentiatingintopICinthesefishhadnotyetbeenfound,itwasbelieved