title: The potential role of polyamines in gill epithelial remodeling during extreme hypoosmotic challenges in the Gulf killifish, Fundulus grandis.
abstract: Polyamines are a family of low molecular weight organic cations produced in part by the coordinated actions of arginase II (Arg II) and ornithine decarboxylase (Odc). Although gill polyamine homeostasis is affected by acute transfer to fresh water, little is known of its function in fish osmoregulation. The current study investigated the role of polyamines in the compensatory response of hypoosmotic challenge in the euryhaline fish, Fundulus grandis. Adult F. grandis were acclimated to 5 ppt water, transferred abruptly to 5, 2, 1, 0.5 and 0.1 ppt water, and assessed for osmoregulatory function, gill morphology, and polyamine homeostasis. The plasma osmolality, Na(+) concentration, and Cl(-) concentration were only significantly reduced during exposure to salinities at or below 0.5 ppt, although these effects were transient except in the 0.1 ppt treatment. The phenotype of mitochondrion-rich cells (MRCs) shifted from a seawater-type to a freshwater-type only at salinities that also produced a plasma osmotic disturbance. Hypoosmotic exposure increased the concentrations of putrescine, spermidine, and spermine in the gill over the entire 7 day period. Exposure to 0.1 ppt water also transiently increased gill caspase-3 activity and gill mRNA levels of the immediate-early response genes, c-fos and c-myc, thus tightly associating polyamines with gill remodeling during freshwater acclimation. Furthermore, arginase II and ornithine decarboxylase mRNA levels were most highly expressed in MRCs, and these levels were further increased only in the 0.1 ppt treatment. Reduction of gill polyamine levels following administration of the Odc inhibitor, alpha-dl-difluoromethylornithine (DFMO), inhibited gill caspase-3 activity, but surprisingly reduced the magnitude of the plasma osmotic imbalance elicited by exposure to 0.1 ppt water. We used isolated opercular epithelia mounted on Ussing chambers to assess the influence of polyamines on the attenuating response of hypotonic shock on active Cl(-) secretion. Spermidine partially reduced the decrease of short-circuit current (Isc) and membrane conductance (Gt) produced by hypotonic exposure. These data suggest polyamines blunt the hypotonic inhibition of NaCl secretion and may lead to early apoptosis of seawater ionocytes and their replacement by FW-type ionocytes.
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA; Department of Biostatistics, School of Public Health and Tropical Medicine, Southern Medical University (Guangdong Provincial Key Laboratory of Tropical Disease Research), Guangzhou, Guangdong, 510515, China. Electronic address: ynguan@echobelt.org.
authors.forename: Ying
authors.initials: Y
authors.lastname: Guan
authors.affiliation: Department of Environmental Health, School of Public Health and Tropical Medicine, Southern Medical University (Guangdong Provincial Key Laboratory of Tropical Disease Research), Guangzhou, Guangdong, 510515, China.
authors.forename: Guo-Xia
authors.initials: GX
authors.lastname: Zhang
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA; Department of Spinal Surgery of the First Affiliated Hospital of University of South, Hengyang, Hunan, 421001, China.
authors.forename: Shujun
authors.initials: S
authors.lastname: Zhang
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
authors.forename: Beau
authors.initials: B
authors.lastname: Domangue
authors.affiliation: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
authors.forename: Fernando
authors.initials: F
authors.lastname: Galvez
mesh_terms: D056151:Airway Remodeling / Q000187:drug effects; D000818:Animals; D017209:Apoptosis / Q000187:drug effects; D001119:Arginase / Q000235:genetics / Q000378:metabolism; D053148:Caspase 3 / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D029941:Fish Proteins / Q000037:antagonists & inhibitors / Q000235:genetics / Q000378:metabolism; D023781:Fundulidae / Q000097:blood / Q000502:physiology*; D005786:Gene Expression Regulation / Q000187:drug effects; D005880:Gills / Q000187:drug effects / Q000378:metabolism* / Q000648:ultrastructure; D060851:Gulf of America; D007527:Isoenzymes / Q000235:genetics / Q000378:metabolism; D008145:Louisiana; D008564:Membrane Potentials / Q000187:drug effects; D009955:Ornithine Decarboxylase / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D065108:Ornithine Decarboxylase Inhibitors / Q000494:pharmacology; D064587:Osmoregulation / Q000187:drug effects; D011073:Polyamines / Q000037:antagonists & inhibitors / Q000097:blood / Q000378:metabolism*; D011897:Random Allocation; D054712:Salinity; D012965:Sodium Chloride / Q000097:blood / Q000378:metabolism; D013312:Stress, Physiological / Q000187:drug effects
chemical_list: D029941:Fish Proteins; D007527:Isoenzymes; D065108:Ornithine Decarboxylase Inhibitors; D011073:Polyamines; D012965:Sodium Chloride; D053148:Caspase 3; D001119:Arginase; D009955:Ornithine Decarboxylase
keywords: Apoptosis; Cell signaling; Cell volume regulation; Ionocytes; Polyamines