研究生: |
沈婉萍 Wan-Ping Shen |
---|---|
論文名稱: |
青鱂魚仔魚在鹽度適應過程之離子細胞功能研究–離子細胞功能之可塑性 The functional study of Mitochondrion-Rich Cells in medaka larvae subjected to salinity changes – Functional plasticity of Mitochondrion-Rich Cells |
指導教授: |
林豊益
Lin, Li-Yih |
學位類別: |
碩士 Master |
系所名稱: |
生命科學系 Department of Life Science |
論文出版年: | 2010 |
畢業學年度: | 98 |
語文別: | 英文 |
論文頁數: | 55 |
中文關鍵詞: | 青鱂魚 、離子細胞 、鹽度適應 、離子調節 、掃描式離子選擇電極 、富含粒線體的細胞 |
英文關鍵詞: | Mitochondrion-Rich cells, scanning ion-selective electrode technique, salinity changes, accessory cells, ion regulation, Japanese medaka |
論文種類: | 學術論文 |
相關次數: | 點閱:208 下載:5 |
分享至: |
查詢本校圖書館目錄 查詢臺灣博碩士論文知識加值系統 勘誤回報 |
魚類鰓上富含粒線體的細胞 ( mitochondrion-rich cells , MRCs ) 被認為是具有離子調節功能的細胞,在海水的環境中,這類細胞負責將過多的離子由魚體內排出至外界環境中,在淡水下則是負責離子吸收的功能。在海水中,Cl-主要是由MRCs的頂膜排出 ; 而Na+被認為由MRCs與輔助細胞 ( accessory cells , ACs ) 間形成的不緊密的細胞間隙擴散排出。前人研究發現在鹽度適應過程中,MRCs能持續存在於鹽度適應的過程,顯示MRCs可能進行功能轉變以因應鹽度轉變。然而,這些MRCs是否能夠直接在淡水型與海水型功能間轉換仍缺乏直接的證據。因此本研究目的是提出細胞功能轉變的直接證據,並探討在淡、海水轉移中MRCs型態與功能轉變間的相互關係。利用掃描式離子選擇電極(SIET)在青鱂魚仔魚表皮上分析MRCs的Na, Cl運送與型態變化。結果發現,在海水馴養下的青鱂魚仔魚體表可觀察到兩類型的MRCs : ( 一 ) 單一存在具有明顯對外開口的MRCs ( single-mitochondrion-rich cells, s-MRCs ) ; ( 二 ) 由AC與1~2顆 MRCs組成的多細胞複合體型態 (multicellular complex-mitochondrion-rich cells, mc-MRCs)。在有AC伴隨的MRCs的開口上,有明顯較高的Na+、Cl-排出; 無AC伴隨的s-MRCs開口上只有明顯的Cl-排出,無明顯的Na+排出,證明AC確實對排Na+扮演重要功能。此外,隨著適應的鹽度提昇,mc-MRCs出現比例會提高。利用SIET測量仔魚體表的Na+, Cl-濃度梯度變化,發現仔魚由淡水轉移至海水過程中,在轉移3小時內Na+呈現吸收,隨後逐漸轉為排出,至第5小時後達到與海水控制組相同的量,而Cl-排放在轉移後2小時即快速達到與海水適應組相同的量,顯示海水適應過程中Cl- 調節比Na+ 調節快。此外,由海水轉移至淡水過程中,在轉移30分鐘內,體表Na+, Cl-排出即快速降低至與淡水適應組相同的程度。在單一MRCs上測量Na+, Cl-離子流(ionic flux)發現,由海水轉移至淡水3-5分鐘內,MRCs 上Na+的排出量快速降低至原本的2-3 %以下,顯示出MRCs快速的調節能力。而利用活體的連續觀測方式,追蹤mc-MRCs及s-MRCs在海水轉移至淡水環境後,發現MRCs的開口有逐漸變大的現象。此外,mc-MRCs的AC會逐漸遠離MRC開口。本實驗直接證明海水型MRCs能夠在淡水適應過程中,直接轉變為淡水型的MRCs。
Mitochondrion-rich (MR) cells (also called chloride cells) are specialized ionocytes in fish gill. These cells are involved in the ion secretion in seawater (SW) and ion uptake in fresh water (FW). It is believed that Cl− is secreted through the apical membrane of MRCs in SW, meanwhile, Na+ secretion occurs down its electrochemical gradient via a paracellular pathway between MRCs and accessory cells (ACs). Previous studies suggested that MRCs can change their morphology and function during extremely salinity changes such as FW to SW or vice versa, implying that MRCs posses a functional plasticity in ion regulation, i.e. taking up ions in FW and secreting ions in SW. However, evidence that can support this hypothesis is few and not convincing. In this study, a non-invasive technique, scanning ion-selective electrode technique (SIET) was applied to sequentially detect the Na+ and Cl- fluxes at the same MRCs in medaka larvae subjected to salinity changes. In vivo observation of SW-acclimated larvae revealed two types of MRCs: (1) single-MRCs (s-MRCs) which do not have a associated accessory cells (ACs) (2) multicellular complex- MRCs (mc-MRCs) which are consisted of MRCs and companied ACs. Using SIET, significant outward fluxes of Na+ and Cl- were detected at the apical surface of mc-MRCs, whereas only an outward flux of Cl- but not Na+ was detected at s-MRCs, indicating that ACs is required for Na+ secretion in SW fish. The presence of ACs increased with the salinity of medium to which the larvae were acclimated. During the transfer from FW to SW or vice versa, time-course changes of Na+ and Cl- gradients at the skin of the larvae were measured with SIET. An inward Na+ gradient was detected at the skin within 3 hrs after the FW to SW transfer, however, an outward Na+ gradient was detected after 3 hrs and the gradients gradually increased with time and reached a relatively steady value after 5 hrs. In addition, an outward Cl- gradient was also detected during the transfer and the value increased with time and reached a steady value at 2 hrs after the transfer, suggesting that Cl- regulation is faster than Na+ regulation in medaka larvae. In contrast, when the larvae were transferred from SW to FW, an instantaneous drop of outward Na+ and Cl- gradients was detected within 30 mins. At individual MRCs, a rapid decline of Na+ and Cl- fluxes also occurred after the SW to FW transfer. At the same time, both s-MRCs and mc-MRCs increased their apical opening sizes, and the ACs were found to depart from mc-MRCs during the transfer. Most importantly, a dramatic alteration of Na+ fluxes was found by sequentially measuring the same MRCs subjected to the transfer. Our data demonstrated that MRCs posses duel functions (ion uptake and ion secretion) and most importantly they can change their function from an ion secreting to an ion absorbing MRCs within 5 hrs.
References
1.Alper SL, Darman RB, Chernova MN, Dahl NK. The AE gene
family of Cl-/HCO3- exchangers. J Nephrol 15, Suppl 5:
S41–S53, 2002.
2.Alper SL. Molecular physiology of SLC4 anion exchangers.
Exp Physiol 91: 153–161, 2006.
3.Bayaa M, Vulesevic B, Esbaugh A, Braun M, Ekker M,
Grosell M, Perry SF. The involvement of SLC26 anion
exchangers in Cl-/HCO3-exchange in zebrafish (Danio
rerio) larvae. J Exp Biol 212: 3283-3295, 2009.
4.Chretien M, Pisam M. Cell renewal and differentiation in
the gill epithelium of fresh- or salt-water-adapted
euryhaline fish as revealed by [3H]-thymidine
radioautography. Biol. Cell 56: 137–150, 1986.
5.Chang IC, Lee T H, Yang C H, Wei YY, Chou FI, Hwang PP.
Morphology and function of gill mitochondria-rich cells
in fish acclimated to different environments. Physiol
Biochem Zool 74: 111-119, 2001.
6.Chang IC, Wei YY, Chou FI, Hwang PP. Stimulation of Cl-
uptake and morphological changes in gill mitochondria-
rich cells in freshwater tilapia(Oreochromis
mossambicus). Physiol Biochem Zool 76: 544-552, 2003.
7.Claude P, and Goodenough D A. Fracture faces of zonulae
occludentes from "tight" and "leaky" epithelia. J Cell
Biol 58: 390-400, 1973.
8.Daborn K, Cozzi RR F, Marshall WS. Dynamics of pavement
cell–chloride cell interactions during abrupt salinity
change in Fundulus heteroclitus. J Exp Biol 204: 1889-
1899, 2001.
9.Degnan KJ, Zadunaisky J A. Passive Sodium Movements
Across the Opercular Epithelium: The Paracellular Shunt
Pathway and Ionic Conductance.J Membrane Biol 55: 175-
185, 1980.
10.Degnan KJ. The role of K+ and Cl- conductances in
chloride secretion by the opercular epithelium. J Exp
Zool 236: 19- 25, 1985.
11.Esaki M, Hoshijima K, Kobayashi S, Fukuda H, Kawakami K,
Hirose S.Visualization in zebrafish larvae of Na+ uptake
in mitochondria-rich cells whose differentiation is
dependent on foxi3a. Am J Physiol Regul Integr Comp
Physiol 292: R470-R480, 2007.
12.Evans DH. Kinetic studies of ion transport by fish gill
epithelium. Am J Physiol Regul Integr Comp Physiol 238:
R224–R230, 1980.
13.Evans DH, Piermarini PM, Choe KP. The multifunctional
fish gill: dominant site of gas exchange,osmoregulation,
acid-base regulation, and excretion of nitrogenous
waste. Physiol Rev 85: 97-177, 2005.
14.Evans DH. Teleost fish osmoregulation: what have we
learned since August Krogh, Homer Smith, and Ancel Keys.
Am J Physiol Regul Integr Comp Physiol 295: R704–R713,
2008.
15.Flemmer AW, Monette MY, Djurisic M, Dowd B, Darman R,
Gimenez I, Forbush B. Phosphorylation state of the Na+-
K+-Cl- cotransporter ( NKCC1 ) in the gills of Atlantic
killifish (Fundulus heteroclitus ) during acclimaion to
water of varying salinity. J Exp Biol213: 1558-1566,
2010.
16.Foskett JK, Scheffey C. The chloride cell: definitive
identification as the salt-secretory cell in
teleosts.Science 215: 164–166, 1982.
17.Flynt AS, Thatcher EJ, Burkewitz K, Li N, Liu Y, Patton
JG. miR-8 microRNAs regulate the response to osmotic
stress in zebrafish embryos. J Cell Biol 185: 115–127,
2009.
18.Galvez F, Reid SD., Hawkings G, Goss GG. Isolation and
characterization of mitochondria-rich cell types from
the gill of freshwater rainbow trout. Am. J. Physiol.
Regul Integr Comp Physiol 282: R658-R668, 2002.
19.Hiroi J, Kaneko T, Tanaka, M. In vivo sequential changes
in chloride cell morphology in the yolk-sac membrane of
Mozambique tilapia (Oreochromis mossambicus) embryos and
larvae during seawater adaptation. J Exp Biol202: 3485-
3495, 1999.
20.Hiroi J, McCormick SD, Ohtani-Kaneko R, Kaneko T.
Functional classification of mitochondrion-rich cells in
euryhaline Mozambique tilapia (Oreochromis mossambicus)
embryos, by means of triple immunofluorescence staining
for Na+/K+-ATPase, Na+/K+/2Cl– cotransporter and CFTR
anion channel. J ExpBiol208: 2023-2036, 2005.
21.Hiroi J, Yasumasu S, McCormick SD, Hwang PP, Kaneko T.
Evidence for an apical Na-Cl cotransporter involved in
ion uptake in a teleost fish. J Exp Biol 211: 2584-2599,
2008.
22.Hoffmann EK, Schettino T, Marshall WS. The role of
volume-sensitive ion transport systems in regulation of
epithelial transport. Comparative Biochemistry and
Physiology, Part A 148: 29-43, 2007.
23.Hossler FE. Gill arch of the mullet, Mugil cephalus,
III: rate of response to salinity change. Am J Physiol.
238: R160–R164, 1980.
24.Hootman SR, Philpott CW. Accessory cells in teleost
branchial epithelium. Am J Physiol Regul Integr Comp
Physiol 238: R199–R206, 1980.
25.Horng JL, Hwang PP, Shih TH, Wen ZH, Lin, CS, Lin LY.
Chloride transport in mitochondrion-rich cells of
euryhaline tilapia (Oreochromis mossambicus) larvae. Am
J Physiol Cell Physiol 297: C845–C854, 2009.
26.Hwang PP, Sun CM, Wu SM. Changes of plasma osmolality,
chloride concentration and gill Na-K-ATPases activity in
tilapia Oreochromis mossambicus during seawater
acclimation. Mar Biol 100: 295–299, 1989.
27.Hwang PP, Hirano R. Effects of environmental salinity of
intercellular organization and junctional structure of
chloride cells in early stages of teleost development. J
Exp Zool 236:115-126, 1985.
28.Hwang PP. Salinity effects on development of chloride
cells in the larvae of ayu(Plecoglossus
altivelis).MarBiol107: 1-7, 1990.
29.Hwang PP, Lee TH. New insights into fish ion regulation
and mitochondrion-rich cells. Comp Biochem Physiol, Part
A 148: 479-497, 2007.
30.Hwang PP. Ion uptake and acid secretion in zebrafish
(Danio rerio).J ExpBiol212: 1745-1752, 2009.
31.Inokuchi M, Hiroi J, Watanabe S, Lee KM, Kaneko T. Gene
expression and morphological localization of NHE3, NCC
and NKCC1a in branchial mitochondria-rich cells of
Mozambique tilapia (Oreochromis mossambicus)
acclimated to a wide range of salinities. Comp Biochem
Physiol A Mol Integr Physiol 151: 151-158, 2008.
32.Inoue K, Takei Y. Diverse adaptability in Oryzias
species to high environmental salinity. Zoological
Science 19:727–734, 2002.
33.Inoue K, Takei Y. Asian medaka fishes offer new models
for studying mechanisms of seawater adaptation. Comp
Biochem Physiol, Part B 136:635–645, 2003.
34.Karnaky KJJ, Kinter LB, Kinter WB, Stirling CE. Teleost
chloride cell. II. Autoradiographic localization of gill
Na,K-ATPase in killifish Fundulus heteroclitus adapted
to low and high salinity environments. J Cell Biol 70:
157–177, 1976.
35.Katoh F, Kaneko T. Short-term transformation and long-
term replacement of branchial chloride cells in
killifish transferred from seawater to freshwater,
revealed by morphofunctional observations and a newly
established‘time-differential double fluorescent
staining’ technique. J Exp Biol 206:4113-4123, 2003.
36.Keys AB, Willmer EN. “Chloride-secreting cells” in the
gills of fishes with special reference to the common
eel. J Physiol Lond 76: 368–378, 1932.
37.Krogh A. Osmotic regulation in freshwater fishes by
active absorption of chloride ions. Z Vergl Physiol 24:
656–666, 1937.
38.Lasker R, Threadgold L. "Chloride cells" in the skin of
the larval sardine. Exp.Cell Res. 52: 582-590, 1968.
39.Laurent P, Dunel S. Morphology of gill epithelia in
fish. Am J Physiol Regul Integr Comp Physiol 238: R147–
R159, 1980.
40.Lee TH, Hwang PP, Lin HC, Huang FL. Mitochondria-rich
cells in the branchial epithelium of the teleost,
Oreochromis mossambicus, acclimated to various hypotonic
environments. Fish Physiol Biochem 15: 513-523, 1996.
41.Lehrich RW, Aller SG, Webster P, Marino CR, Forrest JN,
Jr.Vasoactive intestinal peptide, forskolin, and
genistein increase apical CFTR trafficking in the rectal
gland of the spiny dogfish, Squalus acanthias. Acute
regulation of CFTR trafficking in an intact epithelium.
J Clin Invest 101: 737–745, 1998.
42.Lin CH, Huang CL, Yang CH, Lee TH, Hwang PP. Time-course
changes in the expression of Na, K-ATPase and the
morphometry of mitochondrion-rich cells in gills of
euryhaline tilapia (Oreochromis mossambicus) during
freshwater acclimation. J Exp Zool A Comp Exp Biol
301A:85-96, 2004.
43.Lin LY, Hwang PP. Modification of morphology and
function of integument mitochondria-rich cells in
tilapia larvae (Oreochromis mossambicus) acclimated
to ambient chloride levels. Physiol Biochem Zool 74: 469-
476, 2001.
44.Lin LY, Horng JL, Kunkel JG, Hwang PP. Proton pump-rich
cell secretes acid in skin of zebrafish larvae. Am J
Physiol Cell Physiol 290: C371–C378, 2006.
45.Maetz J. Aspects of adaptation to hypo-and hyper-osmotic
environments. In: Biochemical and Biophysical
Perspectives in Marine Biology, vol. 1, edited by
Malins DC, Sargeant JR., London: Academic Press, 1974,
p. 1-167.
46.Mancera JM, McCormick SD. Rapid activation of gill
Na+,K+- ATPase in the euryhaline teleost Fundulus
heteroclitus. J Exp Zool 287: 263–274, 2000.
47.Mandel LJ, Curran PF. Response of the frog skin to
steady-state voltage clamping. I. The shunt pathway. J.
Gen.Physiol. 59: 503, 1972.
48.Marshall WS, Bryson SE, Garg D.α2-adrenergic inhibition
of chloride transport by opercular epithelium is
mediated by intracellular Ca2+. Proc Natl Acad Sci USA
90: 5504-5508, 1993.
49.Marshall WS, Bryson SE. Transport mechanisms of seawater
teleost chloride cells, an inclusive model of a
multifunctional cell. Comp. Biochem. Physiol. 119A: 97–
106, 1998.
50.Marshall WS, Bryson SE, Luby T. Control of Epithelial Cl- Secretion by basolateral osmolality in the euryhaline
teleost Fundulus Heteroclitus .The Journal of
Experimental Biology 203: 1897–1905, 2000.
51.Marshall WS, Lynch EM, Cozzi RR. Redistribution of
immunofluorescence of CFTR anion channel and NKCC
cotransporter in chloride cells during adaptation of the
killifish Fundulus heteroclitus to sea water.
J Exp Biol 205: 1265–1273, 2002.
52.Marshall WS. Rapid regulation of NaCl secretion by
estuarine teleost fish:coping strategies for short-
duration freshwater exposures. Biochim Biophys Acta
1618: 95-105, 2003.
53.Marshall WS, Cozzi RR, Pelis RM, McCormick SD. Cortisol
receptor blockade and seawater adaptation in the
euryhaline teleost Fundulus heteroclitus. J Exp Zoolog A
Comp Exp Biol 303:132-142,2005a.
54.Marshall WS, Ossum CG, Hoffmann EK. Hypotonic shock
mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in
osmosensing chloride secreting cells of killifish
opercular epithelium. The Journal of Experimental
Biology 208: 1063-1077, 2005b.
55.Marshall WS, Katoh F, Main HP, Sers N, Cozzi RRF. Focal
adhesion kinase and β1 integrin regulation of Na+, K+,
2Cl− cotransporter in osmosensing ion transporting cells
of killifish, Fundulus heteroclitus. Comp Biochem
Physiol A.150:288-300, 2008.
56.Marsigliante S, Muscella A,Vilella S, Storelli C.
Dexamethasone modulates the activity of the eel
branchial Na+/K+ATPase in both chloride and
pavement cells. Life Sci 66:1663–1673.2000.
57.McCormick SD. Hormonal control of gill Na+,K+-ATPase and
chloride cell function. In: Wood CM, Shuttleworth TJ
(eds) Cellular and molecular approaches to fish ionic
regulation.Academic Press, San Diego,1995, pp
285–315.
58.McLamore ES, Porterfield DM, Banks MK. Non-invasive self-
referencing electrochemical sensors for quantifying real-
time biofilm analyte flux. Biotechnology Bioengineering
102: 791-799, 2009.
59.Miyamoto T, Machida T, Kawashima S. Influence of
environmental salinity on the development of chloride
cells of freshwater and brackish-water medaka,
Oryzias latipes. ZoolSci3: 859–865, 1986.
60.Ohana E, Yang D, Shcheynikov N, Muallem S. Diverse
transport modes by the Solute Carrier 26 family of anion
transporters. J Physiol 587: 2179–2185, 2009.
61.Perry SF. The chloride cell: structure and function in
the gills of freshwater fishes. Annu Rev Physiol 59: 325-
347, 1997.
62.Perry SF, Vulesevic B, Grosell M, Bayaa M. Evidence that
SLC26 anion transporters mediate branchial chloride
uptake in adult zebrafish (Danio rerio). Am J Physiol
Regul Integr Comp Physiol 297: R988-R997, 2009.
63.Philpott CW. Tubular system membranes of teleost
chloride cells: osmotic response and transport sites. Am
J Physiol 238: R171–184, 1980.
64.Pisam M, Caroff A, Rambourg A. Two types of chloride
cells in the gill epithelium of a freshwater-adapted
euryhaline fish: Lebistes reticulatus; their
modification during adaptation to salt water. Am J Anat
179: 40-50, 1987.
65.Pisam M, Auperin B, Prunet P, Rambourg A. Effects of
prolactin on alpha and beta chloride cells in the gill
epithelium of the saltwater adapted tilapia
"Oreochromis niloticus". Anat Rec 235: 275-284, 1993.
66.Pisam M, LeMoal C, Auperin B, Prunet P, Rambourg A.
Apicalstructures of “mitochondria-rich” alpha and beta
cells in euryhaline fish gill: their behavior in various
living conditions. Anat Rec 241: 13-24, 1995.
67.Pushkin A, Kurtz I. SLC4 base ( HCO3-, CO32-)
transporters: classification,function, structure,
genetic diseases, and knockout models. Am J Physiol
Renal Physiol 290: F580–F599, 2006.
68.Randall DJ, Burggren WW, French K. Eckert Animal
Physiology:Mechanisms and Adaptations. 5th edition. New
York: Freeman, 2002, p.588-620.
69.Reid SD, Hawkings G S, Galvez F, Goss GG. Localization
and characterization of phenamil-sensitive Na+ influx in
isolated rainbow trout gill epithelial cells. J Exp Biol
206: 551-559, 2003.
70.Romero MF, Fulton CM, Boron WF. The SLC4 family of HCO3-
transporters. Pflugers Arch 447: 495–509, 2004.
71.Romero MF, Chang MH, Plata C, Zandi-Nejad K, Mercado A,
Broumand V, Sussman CR, Mount DB. Physiology of
electrogenic SLC26 paralogues.Novartis Found Symp 273:
126–138, 2006.
72.Sakamoto T, Yokota S, Ando M. Rapid morphological
oscillation of mitochondria-rich cell in estuarine
mudskipper following salinity changes. J
Exp Zool 286: 666-669, 2000.
73.Sardet C, Pisam M, Maetz J. The surface epithelium of
teleostean fish gills. J Cell Biol 80: 96–117, 1979.
74.Shaw JR, Denry Sato J, VanderHeide J, LaCasse T,
Stanton CR, Lankowski A, Stanton SE, Chapline C,
Coutermarsh B, Barnaby R,Karlson K, Stanton B.A. The
role of SGK and CFTR in acute adaptation to
seawater in Fundulus Heteroclitus. Cell Physiol Biochem
22: 69-78, 2008.
75.Shih TH, Horng JL, Hwang PP, Lin LY. Ammonia excretion
by the skin of zebrafish (Danio rerio) larvae. Am J
Physiol Cell Physiol 295: C1625-C1632,2008.
76.Shiraishi K, Kaneko T, Hasegawa S, Hirano T. Development
of multicellular complexes of chloride cells in the yolk-
sac membrane of tilapia(Oreochromis mossambicus) embryos
and larvae in seawater. Cell Tissue Res 288: 583–590,
1997.
77.Sindic A, Chang MH, Mount DB, Romero MF. Renal
physiology of SLC26 anion exchangers. Curr Opin Nephrol
Hypertens 16: 484–490, 2007.
78.Smith PJS, Hammar K, Porterfield DM, Sanger RH,
Trimarchi JR.Self-referencing, non-invasive, ion
selective electrode for single cell detection
of trans-plasma membrane calcium flux. Microscopy
Research and Technique 46: 398-417, 1999.
79.Smith HW. The absorption and excretion of water and
salts by marine teleosts. Am J Physiol 93: 480–505,
1930.
80.Soleimani M, Xu J. SLC26 chloride/base exchangers in the
kidney in health and disease. Seminars in Nephrology 26:
375–385, 2006.
81.Towle DW, Gilman ME, Hempel JD. Rapid modulation of gill
Na++K+-dependent ATPase activity during rapid
acclimation of the killifish Fundulus heteroclitus to
salinity change. J Exp Zool 202: 179–186, 1977.
82.Tsai JC, Hwang PP. Effects of wheat germ agglutinin and
colchicines on microtubules of the mitochondria-rich
cells and Ca2+ uptake in tilapia(Oreochromis
mossambicus) larvae. J Exp Biol 201: 2263-2271, 1998.
83.Uchida K, Kaneko T, Miyazaki H, Hasegawa S, Hirano T.
Excellent salinity tolerance of Mozambique tilapia
(Oreochromis mossambicus): Elevated chloride cell
activity in the branchial and opercular epithelia of the
fish adapted to concentrated seawater. Zool Sci 17: 149-
160, 2000.
84.Wang YF, Tseng YC, Yan JJ, Hiroi J, Hwang PP. Role of
SLC12A10.2, a Na-Cl cotransporter-like protein, in a Cl
uptake mechanism in zebrafish (Danio rerio). Am J
Physiol Regul Integr Comp Physiol 296: R1650-R1660,2009.
85.Wendelaar Bonga S, van der Meij CJM. Degeneration and
death, by apoptosis and necrosis, of the pavement and
chloride cells in the gills of the teleost Oreochromis
mossambicus. Cell Tissue Res 255: 235–243, 1989.
86.Wu S C, Horng J L, Liu ST, Hwang PP, Wen ZH, Lin C S,
Lin, LY. Ammonium dependent sodium uptake in
mitochondrion-rich cells of medaka (Oryzias latipes)
larvae. Am J Physiol Cell Physiol 298:C237-C250,2010.
87.Zadunaisky JA. The chloride cell: the active transport
of chloride and the paracellular pathways. In: Fish
Physiology. Vol. 10B, edited by Hoar WS,
Randall DJ. Orlando: Academic Press, 1984, p. 129-176.
88.Zadunaisky J A, Balla M, Colon DE. A reduction in
chloride secretion by lowered osmolarity in chloride
cells of Fundulus heteroclitus. Bull. Mt Desert
Island Biol. Lab. 24, 52 (Abstract), 1997.